Generic placeholder image

Current Medicinal Chemistry


ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Protective Role of Natural Products in Glioblastoma Multiforme: A Focus on Nitric Oxide Pathway

Author(s): Amir R. Afshari, Hamid Mollazadeh, Elmira Mohtashami, Arash Soltani, Mohammad Soukhtanloo, Azar Hosseini, Mohammad Jalili-Nik, Mohammad Mahdi Vahedi, Mostafa Karimi Roshan and Amirhossein Sahebkar*

Volume 28, Issue 2, 2021

Published on: 30 January, 2020

Page: [377 - 400] Pages: 24

DOI: 10.2174/0929867327666200130104757

Price: $65


In spite of therapeutic modalities such as surgical resection, chemotherapy, and radiotherapy, Glioblastoma Multiforme (GBM) remains an incurable fatal disease. This necessitates further therapeutic options that could enhance the efficacy of existing modalities. Nitric Oxide (NO), a short-lived small molecule, has been revealed to play a crucial role in the pathophysiology of GBM. Several studies have demonstrated that NO is involved in apoptosis, metastasis, cellular proliferation, angiogenesis, invasion, and many other processes implicated in GBM pathobiology. Herein, we elaborate on the role of NO as a therapeutic target in GBM and discuss some natural products affecting the NO signaling pathway.

Keywords: Glioblastoma multiforme, nitric oxide, apoptosis, metastasis, angiogenesis, natural products.

Afshari, A.R.; Jalili-Nik, M.; Soukhtanloo, M.; Ghorbani, A.; Sadeghnia, H.R.; Mollazadeh, H.; Karimi Roshan, M.; Rahmani, F.; Sabri, H.; Vahedi, M.M.; Mousavi, S.H. Auraptene-induced cytotoxicity mechanisms in human malignant glioblastoma (U87) cells: role of reactive oxygen species (ROS). EXCLI J., 2019, 18, 576-590.
[] [PMID: 31611741]
Jalili-Nik, M.; Sabri, H.; Zamiri, E.; Soukhtanloo, M.; Roshan, M.K.; Hosseini, A.; Mollazadeh, H.; Vahedi, M.M.; Afshari, A.R.; Mousavi, S.H. Cytotoxic effects of Ferula latisecta on human glioma U87 cells. Drug Res. (Stuttg.), 2019, 69(12), 665-670.
[] [PMID: 31499542]
Afshari, A.R.; Karimi Roshan, M.; Soukhtanloo, M.; Ghorbani, A.; Rahmani, F.; Jalili-Nik, M.; Vahedi, M.M.; Hoseini, A.; Sadeghnia, H.R.; Mollazadeh, H.; Mousavi, S.H. Cytotoxic effects of auraptene against a human malignant glioblastoma cell line. Avicenna J. Phytomed., 2019, 9(4), 334-346.
[PMID: 31309072]
Lee, S.Y. Temozolomide resistance in glioblastoma multiforme. Genes Dis., 2016, 3(3), 198-210.
[] [PMID: 30258889]
Eckel-Passow, J.E.; Lachance, D.H.; Molinaro, A.M.; Walsh, K.M.; Decker, P.A.; Sicotte, H.; Pekmezci, M.; Rice, T.; Kosel, M.L.; Smirnov, I.V.; Sarkar, G.; Caron, A.A.; Kollmeyer, T.M.; Praska, C.E.; Chada, A.R.; Halder, C.; Hansen, H.M.; McCoy, L.S.; Bracci, P.M.; Marshall, R.; Zheng, S.; Reis, G.F.; Pico, A.R.; O’Neill, B.P.; Buckner, J.C.; Giannini, C.; Huse, J.T.; Perry, A.; Tihan, T.; Berger, M.S.; Chang, S.M.; Prados, M.D.; Wiemels, J.; Wiencke, J.K.; Wrensch, M.R.; Jenkins, R.B. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N. Engl. J. Med., 2015, 372(26), 2499-2508.
[] [PMID: 26061753]
Crespo, I.; Vital, A.L.; Gonzalez-Tablas, M.; Patino, M.C.; Otero, A.; Lopes, M.C.; de Oliveira, C.; Domingues, P.; Orfao, A.; Tabernero, M.D. Molecular and genomic alterations in glioblastoma multiforme. Am. J. Pathol., 2015, 185(7), 1820-1833.
[] [PMID: 25976245]
Pearson, J.R.D.; Regad, T. Targeting cellular pathways in glioblastoma multiforme. Signal Transduct. Target. Ther., 2017, 2, 17040.
[] [PMID: 29263927]
Altieri, R.; Fontanella, M.; Agnoletti, A.; Panciani, P.P.; Spena, G.; Crobeddu, E.; Pilloni, G.; Tardivo, V.; Lanotte, M.; Zenga, F.; Ducati, A.; Garbossa, D. Role of nitric oxide in glioblastoma therapy: another step to resolve the terrible puzzle? Transl. Med. UniSa, 2014, 12, 54-59.
[PMID: 26535188]
Vahora, H.; Khan, M.A.; Alalami, U.; Hussain, A. The potential role of nitric oxide in halting cancer progression through chemoprevention. J. Cancer Prev., 2016, 21(1), 1-12.
[] [PMID: 27051643]
Vasudevan, D.; Bovee, R.C.; Thomas, D.D. Nitric oxide, the new architect of epigenetic landscapes. Nitric Oxide, 2016, 59, 54-62.
[] [PMID: 27553128]
Trajkovic, V.; Stosic-Grujicic, S.; Samardzic, T.; Markovic, M.; Miljkovic, D.; Ramic, Z.; Mostarica Stojkovic, M. Interleukin-17 stimulates inducible nitric oxide synthase activation in rodent astrocytes. J. Neuroimmunol., 2001, 119(2), 183-191.
[] [PMID: 11585620]
Maccallini, C.; Gallorini, M.; Amoia, P.; Ammazzalorso, A.; Filippis, B.D.; Fantacuzzi, M. Inhibitors of the inducible nitric oxide synthase as antiglioma agents.MDPI Proceedings MDPI Proceedings 2019, 22(1), p. 52.
Tran, A.N.; Boyd, N.H.; Walker, K.; Hjelmeland, A.B. NOS expression and NO function in glioma and implications for patient therapies. Antioxid. Redox Signal., 2017, 26(17), 986-999.
[] [PMID: 27411305]
Yin, D.; Wang, X.; Konda, B.M.; Ong, J.M.; Hu, J.; Sacapano, M.R.; Ko, M.K.; Espinoza, A.J.; Irvin, D.K.; Shu, Y.; Black, K.L. Increase in brain tumor permeability in glioma-bearing rats with nitric oxide donors. Clin. Cancer Res., 2008, 14(12), 4002-4009.
[] [PMID: 18559623]
Barna, M.; Komatsu, T.; Reiss, C.S. Activation of type III nitric oxide synthase in astrocytes following a neurotropic viral infection. Virology, 1996, 223(2), 331-343.
[] [PMID: 8806568]
Broholm, H.; Rubin, I.; Kruse, A.; Braendstrup, O.; Schmidt, K.; Skriver, E.B.; Lauritzen, M. Nitric oxide synthase expression and enzymatic activity in human brain tumors. Clin. Neuropathol., 2003, 22(6), 273-281.
[PMID: 14672505]
Giannopoulou, E.; Ravazoula, P.; Kalofonos, H.; Makatsoris, T.; Kardamakis, D. Expression of HIF-1α and iNOS in astrocytic gliomas: a clinicopathological study. In Vivo, 2006, 20(3), 421-425.
[PMID: 16724682]
Shinoda, J.; Whittle, I.R. Nitric oxide and glioma: a target for novel therapy? Br. J. Neurosurg., 2001, 15(3), 213-220.
[] [PMID: 11478055]
Hara, A.; Okayasu, I. Cyclooxygenase-2 and inducible nitric oxide synthase expression in human astrocytic gliomas: correlation with angiogenesis and prognostic significance. Acta Neuropathol., 2004, 108(1), 43-48.
[] [PMID: 15088099]
Heckler, M.; Osterberg, N.; Guenzle, J.; Thiede-Stan, N.K.; Reichardt, W.; Weidensteiner, C.; Saavedra, J.E.; Weyerbrock, A. The nitric oxide donor JS-K sensitizes U87 glioma cells to repetitive irradiation. Tumour Biol., 2017, 39(6)1010428317703922
[] [PMID: 28653883]
Yang, D-I.; Yin, J-H.; Ju, T-C.; Chen, L-S.; Hsu, C.Y. Nitric oxide and BCNU chemoresistance in C6 glioma cells: role of S-nitrosoglutathione. Free Radic. Biol. Med., 2004, 36(10), 1317-1328.
[] [PMID: 15110396]
Li, X.; Liu, D.; Liu, X.; Jiang, W.; Zhou, W.; Yan, W.; Cen, Y.; Li, B.; Cao, G.; Ding, G.; Pang, X.; Sun, J.; Zheng, J.; Zhou, H. CpG ODN107 potentiates radiosensitivity of human glioma cells via TLR9-mediated NF-κB activation and NO production. Tumour Biol., 2012, 33(5), 1607-1618.
[] [PMID: 22739939]
Guenzle, J.; Garrelfs, N.W.C.; Goeldner, J.M.; Weyerbrock, A. cyclooxygenase (cox) inhibition by acetyl salicylic acid (ASA) enhances antitumor effects of nitric oxide in glioblastoma in vitro. Mol. Neurobiol., 2019, 56(9), 6046-6055.
[] [PMID: 30715649]
Thomsen, L.L.; Scott, J.M.; Topley, P.; Knowles, R.G.; Keerie, A-J.; Frend, A.J. Selective inhibition of inducible nitric oxide synthase inhibits tumor growth in vivo: studies with 1400W, a novel inhibitor. Cancer Res., 1997, 57(15), 3300-3304.
[PMID: 9242464]
Jadeski, L.C.; Lala, P.K. Nitric oxide synthase inhibition by N(G)-nitro-L-arginine methyl ester inhibits tumor-induced angiogenesis in mammary tumors. Am. J. Pathol., 1999, 155(4), 1381-1390.
[] [PMID: 10514420]
Kon, K.; Fujii, S.; Kosaka, H.; Fujiwara, T. Nitric oxide synthase inhibition by N(G)-nitro-L-arginine methyl ester retards vascular sprouting in angiogenesis. Microvasc. Res., 2003, 65(1), 2-8.
[] [PMID: 12535865]
Tozer, G.M.; Prise, V.E.; Chaplin, D.J. Inhibition of nitric oxide synthase induces a selective reduction in tumor blood flow that is reversible with L-arginine. Cancer Res., 1997, 57(5), 948-955.
[PMID: 9041200]
Wang, B.; Xiong, Q.; Shi, Q.; Tan, D.; Le, X.; Xie, K. Genetic disruption of host nitric oxide synthase II gene impairs melanoma-induced angiogenesis and suppresses pleural effusion. Int. J. Cancer, 2001, 91(5), 607-611.
[<:AID-IJC1109>3.0.CO;2-D] [PMID: 11267968]
Konopka, T.E.; Barker, J.E.; Bamford, T.L.; Guida, E.; Anderson, R.L.; Stewart, A.G. Nitric oxide synthase II gene disruption: implications for tumor growth and vascular endothelial growth factor production. Cancer Res., 2001, 61(7), 3182-3187.
[PMID: 11306506]
Oyoshi, T.; Nomoto, M.; Hirano, H.; Kuratsu, J. Pathodynamics of nitric oxide production within implanted glioma studied with an in vivo microdialysis technique and immunohistochemistry. J. Pharmacol. Sci., 2003, 91(1), 15-22.
[] [PMID: 12686726]
Towner, R.A.; Gillespie, D.L.; Schwager, A.; Saunders, D.G.; Smith, N.; Njoku, C.E.; Krysiak, R.S. III.; Larabee, C.; Iqbal, H.; Floyd, R.A.; Bourne, D.W.; Abdullah, O.; Hsu, E.W.; Jensen, R.L. Regression of glioma tumor growth in F98 and U87 rat glioma models by the Nitrone OKN-007. Neuro-oncol., 2013, 15(3), 330-340.
[] [PMID: 23328810]
Hoang, T.; Huang, S.; Armstrong, E.; Eickhoff, J.C.; Harari, P.M. Augmentation of radiation response with the vascular targeting agent ZD6126. Int. J. Radiat. Oncol. Biol. Phys., 2006, 64(5), 1458-1465.
[] [PMID: 16488554]
Liang, D.; Song, Y.; Fan, G.; Ji, D.; Zhang, T.; Nie, E.; Liu, X.; Liang, J.; Yu, R.; Gao, S. Effects of long form of capon overexpression on glioma cell proliferation are dependent on AKT/mTOR/P53 signaling. Int. J. Med. Sci., 2019, 16(4), 614-622.
[] [PMID: 31171914]
Rieger, J.; Ständer, M.; Löschmann, P.A.; Heneka, M.; Dichgans, J.; Klockgether, T.; Weller, M. Synthesis and biological effects of NO in malignant glioma cells: modulation by cytokines including CD95L and TGF-β, dexamethasone, and p53 gene transfer. Oncogene, 1998, 17(18), 2323-2332.
[] [PMID: 9811463]
Lam-Himlin, D.; Espey, M.G.; Perry, G.; Smith, M.A.; Castellani, R.J. Malignant glioma progression and nitric oxide. Neurochem. Int., 2006, 49(8), 764-768.
[] [PMID: 16971023]
Xu, W.; Liu, L.; Smith, G.C.; Charles, G. Nitric oxide upregulates expression of DNA-PKcs to protect cells from DNA-damaging anti-tumour agents. Nat. Cell Biol., 2000, 2(6), 339-345.
[] [PMID: 10854324]
Eyler, C.E.; Wu, Q.; Yan, K.; MacSwords, J.M.; Chandler-Militello, D.; Misuraca, K.L.; Lathia, J.D.; Forrester, M.T.; Lee, J.; Stamler, J.S.; Goldman, S.A.; Bredel, M.; McLendon, R.E.; Sloan, A.E.; Hjelmeland, A.B.; Rich, J.N. Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell, 2011, 146(1), 53-66.
[] [PMID: 21729780]
Kashfi, K.; Vannini, F. Nitric oxide and cancer: to inhibit or to induce iNOS: that is the question?Therapeutic Application of Nitric Oxide in Cancer and Inflammatory Disorders; Academic Press, 2019, pp. 93-111.
du Plessis, S.S.; Hagenaar, K.; Lampiao, F. The in vitro effects of melatonin on human sperm function and its scavenging activities on NO and ROS. Andrologia, 2010, 42(2), 112-116.
[] [PMID: 20384801]
Blokhina, O.; Fagerstedt, K.V. Oxidative metabolism, ROS and NO under oxygen deprivation. Plant Physiol. Biochem., 2010, 48(5), 359-373.
[] [PMID: 20303775]
Qiao, S.; Li, W.; Tsubouchi, R.; Haneda, M.; Murakami, K.; Yoshino, M. Involvement of peroxynitrite in capsaicin-induced apoptosis of C6 glioma cells. Neurosci. Res., 2005, 51(2), 175-183.
[] [PMID: 15681035]
Flores, E.R.; Tsai, K.Y.; Crowley, D.; Sengupta, S.; Yang, A.; McKeon, F.; Jacks, T. p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature, 2002, 416(6880), 560-564.
[] [PMID: 11932750]
Lv, L.; Zheng, L.; Dong, D.; Xu, L.; Yin, L.; Xu, Y.; Qi, Y.; Han, X.; Peng, J. Dioscin, a natural steroid saponin, induces apoptosis and DNA damage through reactive oxygen species: a potential new drug for treatment of glioblastoma multiforme. Food Chem. Toxicol., 2013, 59, 657-669.
[] [PMID: 23871826]
Ho, E.; Ames, B.N. Low intracellular zinc induces oxidative DNA damage, disrupts p53, NFκB, and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proc. Natl. Acad. Sci. USA, 2002, 99(26), 16770-16775.
[] [PMID: 12481036]
Kim, Y.A.; Lim, S-Y.; Rhee, S-H.; Park, K.Y.; Kim, C-H.; Choi, B.T.; Lee, S.J.; Park, Y.M.; Choi, Y.H. Resveratrol inhibits inducible nitric oxide synthase and cyclooxygenase-2 expression in β-amyloid-treated C6 glioma cells. Int. J. Mol. Med., 2006, 17(6), 1069-1075.
[] [PMID: 16685418]
Quincozes-Santos, A.; Andreazza, A.C.; Nardin, P.; Funchal, C.; Gonçalves, C-A.; Gottfried, C. Resveratrol attenuates oxidative-induced DNA damage in C6 Glioma cells. Neurotoxicology, 2007, 28(4), 886-891.
[] [PMID: 17498806]
Chen, T-J.; Jeng, J-Y.; Lin, C-W.; Wu, C-Y.; Chen, Y-C. Quercetin inhibition of ROS-dependent and -independent apoptosis in rat glioma C6 cells. Toxicology, 2006, 223(1-2), 113-126.
[] [PMID: 16647178]
Yoshino, Y.; Aoyagi, M.; Tamaki, M.; Duan, L.; Morimoto, T.; Ohno, K. Activation of p38 MAPK and/or JNK contributes to increased levels of VEGF secretion in human malignant glioma cells. Int. J. Oncol., 2006, 29(4), 981-987.
[] [PMID: 16964394]
Turkowski, K.; Brandenburg, S.; Mueller, A.; Kremenetskaia, I.; Bungert, A.D.; Blank, A.; Felsenstein, M.; Vajkoczy, P. VEGF as a modulator of the innate immune response in glioblastoma. Glia, 2018, 66(1), 161-174.
[] [PMID: 28948650]
Iyer, A.K.V.; Ramesh, V.; Castro, C.A.; Kaushik, V.; Kulkarni, Y.M.; Wright, C.A.; Venkatadri, R.; Rojanasakul, Y.; Azad, N. Nitric oxide mediates bleomycin-induced angiogenesis and pulmonary fibrosis via regulation of VEGF. J. Cell. Biochem., 2015, 116(11), 2484-2493.
[] [PMID: 25919965]
Yousfi, N.; Pruvot, B.; Lopez, T.; Magadoux, L.; Franche, N.; Pichon, L.; Salvadori, F.; Solary, E.; Garrido, C.; Laurens, V.; Chluba, J. The impact of tumor nitric oxide production on VEGFA expression and tumor growth in a zebrafish rat glioma xenograft model. PLoS One, 2015, 10(3)e0120435
[] [PMID: 25768009]
Goertz, O.; Haddad, H.; von der Lohe, L.; Lauer, H.; Hirsch, T.; Daigeler, A.; Lehnhardt, M.; Kolbenschlag, J. Influence of ISDN, L-NAME and selenium on microcirculation, leukocyte endothelium interaction and angiogenesis after frostbite. Burns, 2015, 41(1), 145-152.
[] [PMID: 24957357]
Ng, Q-S.; Goh, V.; Milner, J.; Stratford, M.R.; Folkes, L.K.; Tozer, G.M.; Saunders, M.I.; Hoskin, P.J. Effect of nitric-oxide synthesis on tumour blood volume and vascular activity: a phase I study. Lancet Oncol., 2007, 8(2), 111-118.
[] [PMID: 17267325]
Kimura, H.; Weisz, A.; Kurashima, Y.; Hashimoto, K.; Ogura, T.; D’Acquisto, F.; Addeo, R.; Makuuchi, M.; Esumi, H. Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood, 2000, 95(1), 189-197.
[] [PMID: 10607702]
Schnyder, S.; Handschin, C. Skeletal muscle as an endocrine organ: PGC-1α, myokines and exercise. Bone, 2015, 80, 115-125.
[] [PMID: 26453501]
Atif, F.; Yousuf, S.; Stein, D.G. Anti-tumor effects of progesterone in human glioblastoma multiforme: role of PI3K/Akt/mTOR signaling. J. Steroid Biochem. Mol. Biol., 2015, 146, 62-73.
[] [PMID: 24787660]
Kim, E.H.; Song, H.S.; Yoo, S.H.; Yoon, M. Tumor treating fields inhibit glioblastoma cell migration, invasion and angiogenesis. Oncotarget, 2016, 7(40), 65125-65136.
[] [PMID: 27556184]
Wang, Y.; Yan, W.; Lu, X.; Qian, C.; Zhang, J.; Li, P.; Shi, L.; Zhao, P.; Fu, Z.; Pu, P.; Kang, C.; Jiang, T.; Liu, N.; You, Y. Overexpression of osteopontin induces angiogenesis of endothelial progenitor cells via the avβ3/PI3K/AKT/eNOS/NO signaling pathway in glioma cells. Eur. J. Cell Biol., 2011, 90(8), 642-648.
[] [PMID: 21616556]
Miyata, H.; Ashizawa, T.; Iizuka, A.; Kondou, R.; Nonomura, C.; Sugino, T.; Urakami, K.; Asai, A.; Hayashi, N.; Mitsuya, K.; Nakasu, Y.; Yamaguchi, K.; Akiyama, Y. Combination of a STAT3 inhibitor and an mTOR inhibitor against a temozolomide-resistant glioblastoma cell line. Ca. Gen. Prote., 2017, 14(1), 83-91.
[] [PMID: 28031240]
Xu, X.; Malave, A. P38 MAPK, but not p42/p44 MAPK mediated inducible nitric oxide synthase expression in C6 glioma cells. Life Sci., 2000, 67(26), 3221-3230.
[] [PMID: 11191629]
Hambardzumyan, D.; Gutmann, D.H.; Kettenmann, H. The role of microglia and macrophages in glioma maintenance and progression. Nat. Neurosci., 2016, 19(1), 20-27.
[] [PMID: 26713745]
Leblond, M.M.; Gérault, A.N.; Corroyer-Dulmont, A.; MacKenzie, E.T.; Petit, E.; Bernaudin, M.; Valable, S. Hypoxia induces macrophage polarization and re-education toward an M2 phenotype in U87 and U251 glioblastoma models. OncoImmunology, 2015, 5(1)e1056442
[] [PMID: 26942063]
Achyut, B.R.; Angara, K.; Jain, M.; Borin, T.F.; Rashid, M.H.; Iskander, A.S.M.; Ara, R.; Kolhe, R.; Howard, S.; Venugopal, N.; Rodriguez, P.C.; Bradford, J.W.; Arbab, A.S. Canonical NFκB signaling in myeloid cells is required for the glioblastoma growth. Sci. Rep., 2017, 7(1), 13754.
[] [PMID: 29062041]
Szulzewsky, F.; Pelz, A.; Feng, X.; Synowitz, M.; Markovic, D.; Langmann, T.; Holtman, I.R.; Wang, X.; Eggen, B.J.; Boddeke, H.W.; Hambardzumyan, D.; Wolf, S.A.; Kettenmann, H. Glioma-associated microglia/macrophages display an expression profile different from M1 and M2 polarization and highly express Gpnmb and Spp1. PLoS One, 2015, 10(2)e0116644
[] [PMID: 25658639]
Nusblat, L.M.; Carroll, M.J.; Roth, C.M. Crosstalk between M2 macrophages and glioma stem cells. Cell Oncol. (Dordr.), 2017, 40(5), 471-482.
[] [PMID: 28643230]
Iranshahi, M.; Sahebkar, A.; Takasaki, M.; Konoshima, T.; Tokuda, H. Cancer chemopreventive activity of the prenylated coumarin, umbelliprenin, in vivo. Eur. J. Cancer Prev., 2009, 18(5), 412-415.
[] [PMID: 19531956]
Karimian, M.S.; Pirro, M.; Majeed, M.; Sahebkar, A. Curcumin as a natural regulator of monocyte chemoattractant protein-1. Cytokine Growth Factor Rev., 2017, 33, 55-63.
[] [PMID: 27743775]
Rezaee, R.; Momtazi, A.A.; Monemi, A.; Sahebkar, A. Curcumin: a potentially powerful tool to reverse cisplatin-induced toxicity. Pharmacol. Res., 2017, 117, 218-227.
[] [PMID: 28042086]
Panahi, Y.; Kianpour, P.; Mohtashami, R.; Jafari, R.; Simental-Mendía, L.E.; Sahebkar, A. Efficacy and safety of phytosomal curcumin in non-alcoholic fatty liver disease: a randomized controlled trial. Drug Res., 2017, 67(4), 244-251.
[] [PMID: 28158893]
Mollazadeh, H.; Cicero, A.F.G.; Blesso, C.N.; Pirro, M.; Majeed, M.; Sahebkar, A. Immune modulation by curcumin: the role of interleukin-10. Crit. Rev. Food Sci. Nutr., 2019, 59(1), 89-101.
[] [PMID: 28799796]
Mukherjee, S.; Fried, A.; Hussaini, R.; White, R.; Baidoo, J.; Yalamanchi, S.; Banerjee, P. Phytosomal curcumin causes natural killer cell-dependent repolarization of glioblastoma (GBM) tumor-associated microglia/macrophages and elimination of GBM and GBM stem cells. J. Exp. Clin. Cancer Res., 2018, 37(1), 168.
[] [PMID: 30041669]
Goldstein, M.; Rudra, S.; Dahiya, S.; Tsien, C.; Huang, J. Prognostic value of EGFR amplification in glioblastoma patients treated with radiation therapy and concurrent temozolomide. J. Exp. Clin. Cancer Res., 2019, 38(1), 168.
[] [PMID: 30995926]
Kavoosi, G.; Teixeira da Silva, J.A.; Saharkhiz, M.J. Inhibitory effects of Zataria multiflora essential oil and its main components on nitric oxide and hydrogen peroxide production in lipopolysaccharide-stimulated macrophages. J. Pharm. Pharmacol., 2012, 64(10), 1491-1500.
[] [PMID: 22943180]
Zhao, H-W.; Li, X-Y.; Ginkgolide, A.; Ginkgolide, A.; Ginkgolide, A. B, and huperzine A inhibit nitric oxide-induced neurotoxicity. Int. Immunopharmacol., 2002, 2(11), 1551-1556.
[] [PMID: 12433056]
Kundu, M.; Das, S.; Dhara, D.; Mandal, M. Prospect of natural products in glioma: a novel avenue in glioma management. Phytother. Res., 2019, 33(10), 2571-2584.
[] [PMID: 31359523]
Lee, D.H.; Shin, J-S.; Kang, S-Y.; Lee, S-B.; Lee, J.S.; Ryu, S.M.; Lee, K.T.; Lee, D.; Jang, D.S. Iridoids from the roots of Patrinia scabra and their inhibitory potential on LPS-induced nitric oxide production. J. Nat. Prod., 2018, 81(6), 1468-1473.
[] [PMID: 29799195]
Zhou, Y.; Liu, S-Q.; Yu, L.; He, B.; Wu, S-H.; Zhao, Q.; Xia, S.Q.; Mei, H.J. Berberine prevents nitric oxide-induced rat chondrocyte apoptosis and cartilage degeneration in a rat osteoarthritis model via AMPK and p38 MAPK signaling. Apoptosis, 2015, 20(9), 1187-1199.
[] [PMID: 26184498]
Ryu, J-H.; Ahn, H.; Jin Lee, H. Inhibition of nitric oxide production on LPS-activated macrophages by kazinol B from Broussonetia kazinoki. Fitoterapia, 2003, 74(4), 350-354.
[] [PMID: 12781805]
Hiransai, P.; Tangpong, J.; Kumbuar, C.; Hoonheang, N.; Rodpech, O.; Sangsuk, P. Anti-nitric oxide production, anti-proliferation and antioxidant effects of the aqueous extract from Tithonia diversifolia. Asian Pac. J. Trop. Biomed., 2016, 6(11), 950-956.
Autore, G.; Rastrelli, L.; Lauro, M.R.; Marzocco, S.; Sorrentino, R.; Sorrentino, U.; Pinto, A.; Aquino, R. Inhibition of nitric oxide synthase expression by a methanolic extract of Crescentia alata and its derived flavonols. Life Sci., 2001, 70(5), 523-534.
[] [PMID: 11811897]
Joo, T.; Sowndhararajan, K.; Hong, S.; Lee, J.; Park, S-Y.; Kim, S.; Jhoo, J.W. Inhibition of nitric oxide production in LPS-stimulated RAW 264.7 cells by stem bark of Ulmus pumila L. Saudi J. Biol. Sci., 2014, 21(5), 427-435.
[] [PMID: 25313277]
Lee, K.Y.; Jeon, Y.J. Macrophage activation by polysaccharide isolated from Astragalus membranaceus. Int. Immunopharmacol., 2005, 5(7-8), 1225-1233.
[] [PMID: 15914327]
Punturee, K.; Wild, C.P.; Vinitketkumneun, U. Thai medicinal plants modulate nitric oxide and tumor necrosis factor-α in J774.2 mouse macrophages. J. Ethnopharmacol., 2004, 95(2-3), 183-189.
[] [PMID: 15507334]
Chu, C-Y.; Lee, M-J.; Liao, C-L.; Lin, W-L.; Yin, Y-F.; Tseng, T-H. Inhibitory effect of hot-water extract from dried fruit of Crataegus pinnatifida on low-density lipoprotein (LDL) oxidation in cell and cell-free systems. J. Agric. Food Chem., 2003, 51(26), 7583-7588.
[] [PMID: 14664511]
Chung, H-S.; Jeong, H-J.; Kim, J-S.; Jeong, S-I.; Kim, K-S.; Kim, K-S.; Kang, B.K.; Ahn, J.W.; Baek, S.H.; Kim, H.M. Activation of inducible nitric oxide synthase by Euonymus alatus in mouse peritoneal macrophages. Clin. Chim. Acta, 2002, 318(1-2), 113-120.
[] [PMID: 11880120]
Chung, H-S.; Jeong, H-J.; Han, M-J.; Park, S-T.; Seong, K-K.; Baek, S-H.; Jeong, D.M.; Kim, M.J.; Kim, H.M. Nitric oxide and tumor necrosis factor-α production by Ixeris dentata in mouse peritoneal macrophages. J. Ethnopharmacol., 2002, 82(2-3), 217-222.
[] [PMID: 12241998]
Tai, J.; Cheung, S.; Chan, E.; Hasman, D. In vitro culture studies of Sutherlandia frutescens on human tumor cell lines. J. Ethnopharmacol., 2004, 93(1), 9-19.
[] [PMID: 15182898]
Wang, S-Y.; Chang, H-N.; Lin, K-T.; Lo, C-P.; Yang, N-S.; Shyur, L-F. Antioxidant properties and phytochemical characteristics of extracts from Lactuca indica. J. Agric. Food Chem., 2003, 51(5), 1506-1512.
[] [PMID: 12590506]
Chung, H-S.; Kang, M.; Cho, C.; Park, S.; Kim, H.; Yoon, Y-S.; Kang, J.; Shin, M.K.; Hong, M.C.; Bae, H. Inhibition of lipopolysaccharide and interferon-gamma-induced expression of inducible nitric oxide synthase and tumor necrosis factor-alpha by Lithospermi radix in mouse peritoneal macrophages. J. Ethnopharmacol., 2005, 102(3), 412-417.
[] [PMID: 16054790]
Mahmood, M.S.; Gilani, A.H.; Khwaja, A.; Rashid, A.; Ashfaq, M.K. The in vitro effect of aqueous extract of Nigella sativa seeds on nitric oxide production. Phytother. Res., 2003, 17(8), 921-924.
[] [PMID: 13680825]
Chung, H-S.; Jeong, H-J.; Hong, S-H.; Kim, M-S.; Kim, S-J.; Song, B-K.; Jeong, I.S.; Lee, E.J.; Ahn, J.W.; Baek, S.H.; Kim, H.M. Induction of nitric oxide synthase by Oldenlandia diffusa in mouse peritoneal macrophages. Biol. Pharm. Bull., 2002, 25(9), 1142-1146.
[] [PMID: 12230105]
Kim, I-T.; Park, Y-M.; Shin, K-M.; Ha, J.; Choi, J.; Jung, H-J.; Park, H.J.; Lee, K.T. Anti-inflammatory and anti-nociceptive effects of the extract from Kalopanax pictus, Pueraria thunbergiana and Rhus verniciflua. J. Ethnopharmacol., 2004, 94(1), 165-173.
[] [PMID: 15261979]
Mehrotra, S.; Mishra, K.P.; Maurya, R.; Srimal, R.C.; Yadav, V.S.; Pandey, R.; Singh, V.K. Anticellular and immunosuppressive properties of ethanolic extract of Acorus calamus rhizome. Int. Immunopharmacol., 2003, 3(1), 53-61.
[] [PMID: 12538034]
Chiang, Y-M.; Chuang, D-Y.; Wang, S-Y.; Kuo, Y-H.; Tsai, P-W.; Shyur, L-F. Metabolite profiling and chemopreventive bioactivity of plant extracts from Bidens pilosa. J. Ethnopharmacol., 2004, 95(2-3), 409-419.
[] [PMID: 15507368]
Pae, H.O.; Oh, G.S.; Choi, B.M.; Shin, S.; Chai, K.Y.; Oh, H.; Kim, J.M.; Kim, H.J.; Jang, S.I.; Chung, H.T. Inhibitory effects of the stem bark of Catalpa ovata G. Don. (Bignoniaceae) on the productions of tumor necrosis factor-α and nitric oxide by the lipopolisaccharide-stimulated RAW 264.7 macrophages. J. Ethnopharmacol., 2003, 88(2-3), 287-291.
[] [PMID: 12963157]
Saha, K.; Lajis, N.H.; Israf, D.A.; Hamzah, A.S.; Khozirah, S.; Khamis, S.; Syahida, A. Evaluation of antioxidant and nitric oxide inhibitory activities of selected Malaysian medicinal plants. J. Ethnopharmacol., 2004, 92(2-3), 263-267.
[] [PMID: 15138010]
Napolitano, D.R.; Mineo, J.R.; de Souza, M.A.; de Paula, J.E.; Espindola, L.S.; Espindola, F.S. Down-modulation of nitric oxide production in murine macrophages treated with crude plant extracts from the Brazilian Cerrado. J. Ethnopharmacol., 2005, 99(1), 37-41.
[] [PMID: 15848017]
Song, Y.S.; Kim, S-H.; Sa, J-H.; Jin, C.; Lim, C-J.; Park, E-H. Anti-angiogenic and inhibitory activity on inducible nitric oxide production of the mushroom Ganoderma lucidum. J. Ethnopharmacol., 2004, 90(1), 17-20.
[] [PMID: 14698502]
Choi, E-M.; Hwang, J-K. Effects of methanolic extract and fractions from Litsea cubeba bark on the production of inflammatory mediators in RAW264.7 cells. Fitoterapia, 2004, 75(2), 141-148.
[] [PMID: 15030918]
Blonska, M.; Bronikowska, J.; Pietsz, G.; Czuba, Z.P.; Scheller, S.; Krol, W. Effects of ethanol extract of propolis (EEP) and its flavones on inducible gene expression in J774A.1 macrophages. J. Ethnopharmacol., 2004, 91(1), 25-30.
[] [PMID: 15036463]
Hu, C.; Kitts, D.D. Dandelion (Taraxacum officinale) flower extract suppresses both reactive oxygen species and nitric oxide and prevents lipid oxidation in vitro. Phytomedicine, 2005, 12(8), 588-597.
[] [PMID: 16121519]
Banskota, A.H.; Tezuka, Y.; Nguyen, N.T.; Awale, S.; Nobukawa, T.; Kadota, S. DPPH radical scavenging and nitric oxide inhibitory activities of the constituents from the wood of Taxus yunnanensis. Planta Med., 2003, 69(6), 500-505.
[] [PMID: 12865966]
Grande, S.; Bogani, P.; de Saizieu, A.; Schueler, G.; Galli, C.; Visioli, F. Vasomodulating potential of mediterranean wild plant extracts. J. Agric. Food Chem., 2004, 52(16), 5021-5026.
[] [PMID: 15291469]
Jun, C-D.; Pae, H-O.; Kim, Y-C.; Jeong, S-J.; Yoo, J-C.; Lee, E-J.; Choi, B.M.; Chae, S.W.; Park, R.K.; Chung, H.T. Inhibition of nitric oxide synthesis by butanol fraction of the methanol extract of Ulmus davidiana in murine macrophages. J. Ethnopharmacol., 1998, 62(2), 129-135.
[] [PMID: 9741885]
Ryu, J.H.; Ahn, H.; Kim, J.Y.; Kim, Y.K. Inhibitory activity of plant extracts on nitric oxide synthesis in LPS-activated macrophages. Phytother. Res., 2003, 17(5), 485-489.
[] [PMID: 12748984]
Engwerda, C.R.; Andrew, D.; Murphy, M.; Mynott, T.L. Bromelain activates murine macrophages and natural killer cells in vitro. Cell. Immunol., 2001, 210(1), 5-10.
[] [PMID: 11485347]
Chen, Y-H.; Dai, H-J.; Chang, H-P. Suppression of inducible nitric oxide production by indole and isothiocyanate derivatives from Brassica plants in stimulated macrophages. Planta Med., 2003, 69(8), 696-700.
[] [PMID: 14531017]
Koo, H-N.; Hong, S-H.; Seo, H-G.; Yoo, T-S.; Lee, K-N.; Kim, N-S.; Kim, C.H.; Kim, H.M. Inulin stimulates NO synthesis via activation of PKC-α and protein tyrosine kinase, resulting in the activation of NF-kappaB by IFN-γ-primed RAW 264.7 cells. J. Nutr. Biochem., 2003, 14(10), 598-605.
[] [PMID: 14559111]
Jang, M.K.; Lee, H.J.; Kim, J.S.; Ryu, J-H. A curcuminoid and two sesquiterpenoids from Curcuma zedoaria as inhibitors of nitric oxide synthesis in activated macrophages. Arch. Pharm. Res., 2004, 27(12), 1220-1225.
[] [PMID: 15646795]
Rininger, J.A.; Kickner, S.; Chigurupati, P.; McLean, A.; Franck, Z. Immuno-pharmacological activity of Echinacea preparations following simulated digestion on murine macrophages and human peripheral blood mononuclear cells. J. Leukoc. Biol., 2000, 68(4), 503-510.
[PMID: 11037971]
Stevenson, L.M.; Matthias, A.; Banbury, L.; Penman, K.G.; Bone, K.M.; Leach, D.L.; Lehmann, R.P. Modulation of macrophage immune responses by Echinacea. Molecules, 2005, 10(10), 1279-1285.
[] [PMID: 18007520]
Cheung, F.; Siow, Y.L.; Chen, W.Z. O, K. Inhibitory effect of Ginkgo biloba extract on the expression of inducible nitric oxide synthase in endothelial cells. Biochem. Pharmacol., 1999, 58(10), 1665-1673.
[] [PMID: 10535759]
Kim, G-Y.; Choi, G-S.; Lee, S-H.; Park, Y-M. Acidic polysaccharide isolated from Phellinus linteus enhances through the up-regulation of nitric oxide and tumor necrosis factor-α from peritoneal macrophages. J. Ethnopharmacol., 2004, 95(1), 69-76.
[] [PMID: 15374609]
Hong, C.H.; Hur, S.K.; Oh, O-J.; Kim, S.S.; Nam, K.A.; Lee, S.K. Evaluation of natural products on inhibition of inducible cyclooxygenase (COX-2) and nitric oxide synthase (iNOS) in cultured mouse macrophage cells. J. Ethnopharmacol., 2002, 83(1-2), 153-159.
[] [PMID: 12413723]
Amirghofran, Z.; Malek-Hosseini, S.; Golmoghaddam, H.; Kalantar, F.; Shabani, M. Inhibition of nitric oxide production and proinflammatory cytokines by several medicinal plants. Iran. J. Immunol., 2011, 8(3), 159-169.
[PMID: 21931202]
El Hasasna, H.; Saleh, A.; Al Samri, H.; Athamneh, K.; Attoub, S.; Arafat, K.; Benhalilou, N.; Alyan, S.; Viallet, J.; Al-Dhaheri, Y.; Eid, A.; Iratni, R. Rhus coriaria suppresses angiogenesis, metastasis and tumor growth of breast cancer through inhibition of STAT3, NFκB and nitric oxide pathways. Sci. Rep., 2016, 6, 21144.
[] [PMID: 26888313]
Do, H.; Pyo, S.; Sohn, E-H. Suppression of iNOS expression by fucoidan is mediated by regulation of p38 MAPK, JAK/STAT, AP-1 and IRF-1, and depends on up-regulation of scavenger receptor B1 expression in TNF-α- and IFN-γ-stimulated C6 glioma cells. J. Nutr. Biochem., 2010, 21(8), 671-679.
[] [PMID: 19576750]
Lee-Hilz, Y.Y.; Boerboom, A-M.J.; Westphal, A.H.; Berkel, W.J.; Aarts, J.M.; Rietjens, I.M. Pro-oxidant activity of flavonoids induces EpRE-mediated gene expression. Chem. Res. Toxicol., 2006, 19(11), 1499-1505.
[] [PMID: 17112238]
Suh, N.; Paul, S.; Hao, X.; Simi, B.; Xiao, H.; Rimando, A.M.; Reddy, B.S. Pterostilbene, an active constituent of blueberries, suppresses aberrant crypt foci formation in the azoxymethane-induced colon carcinogenesis model in rats. Clin. Cancer Res., 2007, 13(1), 350-355.
[] [PMID: 17200374]
Wang, Z.; Lee, Y.; Eun, J.S.; Bae, E.J. Inhibition of adipocyte inflammation and macrophage chemotaxis by butein. Eur. J. Pharmacol., 2014, 738, 40-48.
[] [PMID: 24877688]
Liu, H-T.; Du, Y-G.; He, J-L.; Chen, W-J.; Li, W-M.; Yang, Z.; Wang, Y.X.; Yu, C. Tetramethylpyrazine inhibits production of nitric oxide and inducible nitric oxide synthase in lipopolysaccharide-induced N9 microglial cells through blockade of MAPK and PI3K/Akt signaling pathways, and suppression of intracellular reactive oxygen species. J. Ethnopharmacol., 2010, 129(3), 335-343.
[] [PMID: 20371283]
Hayashi, T.; Yamada, K.; Esaki, T.; Muto, E.; Chaudhuri, G.; Iguchi, A. Physiological concentrations of 17β-estradiol inhibit the synthesis of nitric oxide synthase in macrophages via a receptor-mediated system. J. Cardiovasc. Pharmacol., 1998, 31(2), 292-298.
[] [PMID: 9475272]
Ippoushi, K.; Azuma, K.; Ito, H.; Horie, H.; Higashio, H. [6]-Gingerol inhibits nitric oxide synthesis in activated J774.1 mouse macrophages and prevents peroxynitrite-induced oxidation and nitration reactions. Life Sci., 2003, 73(26), 3427-3437.
[] [PMID: 14572883]
Lin, C-M.; Huang, S-T.; Liang, Y-C.; Lin, M-S.; Shih, C-M.; Chang, Y-C.; Chen, T.Y.; Chen, C.T. Isovitexin suppresses lipopolysaccharide-mediated inducible nitric oxide synthase through inhibition of NF-kappa B in mouse macrophages. Planta Med., 2005, 71(8), 748-753.
[] [PMID: 16142640]
Zhao, F.; Nozawa, H.; Daikonnya, A.; Kondo, K.; Kitanaka, S. Inhibitors of nitric oxide production from hops (Humulus lupulus L.). Biol. Pharm. Bull., 2003, 26(1), 61-65.
[] [PMID: 12520174]
Daikonya, A.; Katsuki, S.; Kitanaka, S. Antiallergic agents from natural sources 9. Inhibition of nitric oxide production by novel chalcone derivatives from Mallotus philippinensis (Euphorbiaceae). Chem. Pharm. Bull. (Tokyo), 2004, 52(11), 1326-1329.
[] [PMID: 15516755]
Kim, H.K.; Cheon, B.S.; Kim, Y.H.; Kim, S.Y.; Kim, H.P. Effects of naturally occurring flavonoids on nitric oxide production in the macrophage cell line RAW 264.7 and their structure-activity relationships. Biochem. Pharmacol., 1999, 58(5), 759-765.
[] [PMID: 10449184]
Chen, Y-C.; Shen, S-C.; Chen, L-G.; Lee, T.J.; Yang, L-L. Wogonin, baicalin, and baicalein inhibition of inducible nitric oxide synthase and cyclooxygenase-2 gene expressions induced by nitric oxide synthase inhibitors and lipopolysaccharide. Biochem. Pharmacol., 2001, 61(11), 1417-1427.
[] [PMID: 11331078]
Nicholas, C.; Batra, S.; Vargo, M.A.; Voss, O.H.; Gavrilin, M.A.; Wewers, M.D.; Guttridge, D.C.; Grotewold, E.; Doseff, A.I. Apigenin blocks lipopolysaccharide-induced lethality in vivo and proinflammatory cytokines expression by inactivating NF-kappaB through the suppression of p65 phosphorylation. J. Immunol., 2007, 179(10), 7121-7127.
[] [PMID: 17982104]
Jun, M.; Hong, J.; Jeong, W.S.; Ho, C.T. Suppression of arachidonic acid metabolism and nitric oxide formation by kudzu isoflavones in murine macrophages. Mol. Nutr. Food Res., 2005, 49(12), 1154-1159.
[] [PMID: 16254887]
Sheu, F.; Lai, H-H.; Yen, G-C. Suppression effect of soy isoflavones on nitric oxide production in RAW 264.7 macrophages. J. Agric. Food Chem., 2001, 49(4), 1767-1772.
[] [PMID: 11308324]
Hartog, A.; Smit, H.F.; van der Kraan, P.M.; Hoijer, M.A.; Garssen, J. In vitro and in vivo modulation of cartilage degradation by a standardized Centella asiatica fraction. Exp. Biol. Med. (Maywood), 2009, 234(6), 617-623.
[] [PMID: 19307458]
Yun, K-J.; Shin, J-S.; Choi, J-H.; Back, N-I.; Chung, H-G.; Lee, K-T. Quaternary alkaloid, pseudocoptisine isolated from tubers of Corydalis turtschaninovi inhibits LPS-induced nitric oxide, PGE(2), and pro-inflammatory cytokines production via the down-regulation of NF-kappaB in RAW 264.7 murine macrophage cells. Int. Immunopharmacol., 2009, 9(11), 1323-1331.
[] [PMID: 19666143]
Kang, S.R.; Park, K.I.; Park, H.S.; Lee, D.H.; Kim, J.A.; Nagappan, A. Anti-inflammatory effect of flavonoids isolated from Korea Citrus aurantium L. on lipopolysaccharide-induced mouse macrophage RAW 264.7 cells by blocking of nuclear factor-kappa B (NF-κB) and mitogen-activated protein kinase (MAPK) signalling pathways. Food Chem., 2011, 129(4), 1721-1728.
Fan, G-W.; Zhang, Y.; Jiang, X.; Zhu, Y.; Wang, B.; Su, L.; Cao, W.; Zhang, H.; Gao, X. Anti-inflammatory activity of baicalein in LPS-stimulated RAW264.7 macrophages via estrogen receptor and NF-κB-dependent pathways. Inflammation, 2013, 36(6), 1584-1591.
[] [PMID: 23892998]
Kim, J-Y.; Park, S.J.; Yun, K-J.; Cho, Y-W.; Park, H-J.; Lee, K-T. Isoliquiritigenin isolated from the roots of Glycyrrhiza uralensis inhibits LPS-induced iNOS and COX-2 expression via the attenuation of NF-kappaB in RAW 264.7 macrophages. Eur. J. Pharmacol., 2008, 584(1), 175-184.
[] [PMID: 18295200]
Morikawa, T.; Tao, J.; Ando, S.; Matsuda, H.; Yoshikawa, M. Absolute stereostructures of new arborinane-type triterpenoids and inhibitors of nitric oxide production from Rubia yunnanensis. J. Nat. Prod., 2003, 66(5), 638-645.
[] [PMID: 12762798]
Chung, J.W.; Choi, R.J.; Seo, E-K.; Nam, J-W.; Dong, M-S.; Shin, E.M.; Guo, L.Y.; Kim, Y.S. Anti-inflammatory effects of (Z)-ligustilide through suppression of mitogen-activated protein kinases and nuclear factor-κB activation pathways. Arch. Pharm. Res., 2012, 35(4), 723-732.
[] [PMID: 22553066]
Kang, J.; Zhang, Y.; Cao, X.; Fan, J.; Li, G.; Wang, Q.; Diao, Y.; Zhao, Z.; Luo, L.; Yin, Z. Lycorine inhibits lipopolysaccharide-induced iNOS and COX-2 up-regulation in RAW264.7 cells through suppressing P38 and STATs activation and increases the survival rate of mice after LPS challenge. Int. Immunopharmacol., 2012, 12(1), 249-256.
[] [PMID: 22155741]
Xia, G-Y.; Yao, T.; Zhang, B-Y.; Li, Y.; Kang, N.; Cao, S-J.; Ding, L.Q.; Chen, L.X.; Qiu, F. Withapubesides A-D: natural inducible nitric oxide synthase (iNOS) inhibitors from Physalis pubescens. Org. Biomol. Chem., 2017, 15(47), 10016-10023.
[] [PMID: 29164214]
Soliman, K.F.; Mazzio, E.A. In vitro attenuation of nitric oxide production in C6 astrocyte cell culture by various dietary compounds. Proc. Soc. Exp. Biol. Med., 1998, 218(4), 390-397.
[] [PMID: 9714085]
Balkhi, H.M.; Gul, T.; Banday, M.Z.; Haq, E. Antineoplastic Action of CAPE in in vitro model of glioma. Int. J. Adv. Res. (JAR), 2015, 3(10), 653-660.
Chakrabarti, M.; Ray, S.K. Anti-tumor activities of luteolin and silibinin in glioblastoma cells: overexpression of miR-7-1-3p augmented luteolin and silibinin to inhibit autophagy and induce apoptosis in glioblastoma in vivo. Apoptosis, 2016, 21(3), 312-328.
[] [PMID: 26573275]
Park, J-Y.; Kim, H.; Lim, D-W.; Kim, J-E.; Park, W-H.; Park, S-D. Ethanol extract of Lycopodium serratum thunb. Attenuates lipopolysaccharide-induced c6 glioma cells migration via matrix metalloproteinase-9 expression. Chin. J. Integr. Med., 2018, 24(11), 860-866.
[] [PMID: 29335864]
Mediesse, F.K.; Boudjeko, T.; Hasitha, A.; Gangadhar, M.; Mbacham, W.F.; Yogeeswari, P. Inhibition of lipopolysaccharide (LPS)-induced neuroinflammatory response by polysaccharide fractions of Khaya grandifoliola (C.D.C.) stem bark, Cryptolepis sanguinolenta (Lindl.) Schltr. and Cymbopogon citratus Stapf. leaves in raw 264.7 macrophages and U87 glioblastoma cells. BMC Complement. Altern. Med., 2018, 18(1), 86.
[] [PMID: 29530027]
Khazaei, M.; Pazhouhi, M.; Khazaei, S. Evaluation of hydro-alcoholic extract of Trifolium pratens L. for Its anti-cancer potential on U87MG cell line. Cell J., 2018, 20(3), 412-421.
[] [PMID: 29845796]
Choi, S.Y.; Kim, J.H.; Quilantang, N.G.; Lee, S.; Cho, E.J. Acer okamotoanum inhibit the hydrogen peroxide-induced oxidative stress in C6 glial cells. Nat. Prod. Sci., 2018, 24(3), 148-154.
Lee, A.Y.; Wu, T.T.; Hwang, B.R.; Lee, J.; Lee, M-H.; Lee, S.; Cho, E.J. The neuro-protective effect of the methanolic extract of Perilla frutescens var. japonicaand rosmarinic acid against H2O2-induced oxidative stress in C6 glial cells. Biomol. Ther. (Seoul), 2016, 24(3), 338-345.
[] [PMID: 27133263]
Khan, M.; Bi, Y.; Qazi, J.I.; Fan, L.; Gao, H. Evodiamine sensitizes U87 glioblastoma cells to TRAIL via the death receptor pathway. Mol. Med. Rep., 2015, 11(1), 257-262.
[] [PMID: 25333675]
Kim, H.; Kim, Y.S.; Kim, S.Y.; Suk, K. The plant flavonoid wogonin suppresses death of activated C6 rat glial cells by inhibiting nitric oxide production. Neurosci. Lett., 2001, 309(1), 67-71.
[] [PMID: 11489548]
Kim, Y.A.; Kim, G-Y.; Park, K-Y.; Choi, Y.H. Resveratrol inhibits nitric oxide and prostaglandin E2 production by lipopolysaccharide-activated C6 microglia. J. Med. Food, 2007, 10(2), 218-224.
[] [PMID: 17651055]
Bi, X.L.; Yang, J.Y.; Dong, Y.X.; Wang, J.M.; Cui, Y.H.; Ikeshima, T.; Zhao, Y.Q.; Wu, C.F. Resveratrol inhibits nitric oxide and TNF-α production by lipopolysaccharide-activated microglia. Int. Immunopharmacol., 2005, 5(1), 185-193.
[] [PMID: 15589480]
Quincozes-Santos, A.; Bobermin, L.D.; Latini, A.; Wajner, M.; Souza, D.O.; Gonçalves, C-A.; Gottfried, C. Resveratrol protects C6 astrocyte cell line against hydrogen peroxide-induced oxidative stress through heme oxygenase 1. PLoS One, 2013, 8(5)e64372
[] [PMID: 23691207]
Esposito, G.; Izzo, A.A.; Di Rosa, M.; Iuvone, T. Selective cannabinoid CB1 receptor-mediated inhibition of inducible nitric oxide synthase protein expression in C6 rat glioma cells. J. Neurochem., 2001, 78(4), 835-841.
[] [PMID: 11520904]
Choi, S-S.; Lee, J-K.; Han, E-J.; Han, K-J.; Lee, H-K.; Lee, J.; Suh, H.W. Effect of ginsenoside Rd on nitric oxide system induced by lipopolysaccharide plus TNF-α in C6 rat glioma cells. Arch. Pharm. Res., 2003, 26(5), 375-382.
[] [PMID: 12785733]
Zhao, H.W.; Li, X.Y. Ginkgolide, A, B, and huperzine A inhibit nitric oxide production from rat C6 and human BT325 glioma cells. Zhongguo Yao Li Xue Bao., 1999, 20(10), 941-943.
[PMID: 11270996]
Wang, C.N.; Shiao, Y.J.; Lin, Y.L.; Chen, C.F. Nepalolide A inhibits the expression of inducible nitric oxide synthase by modulating the degradation of IkappaB-α and IkappaB-β in C6 glioma cells and rat primary astrocytes. Br. J. Pharmacol., 1999, 128(2), 345-356.
[] [PMID: 10510444]
Pazhouhi, M.; Sariri, R.; Rabzia, A.; Khazaei, M. Thymoquinone synergistically potentiates temozolomide cytotoxicity through the inhibition of autophagy in U87MG cell line. Iran. J. Basic Med. Sci., 2016, 19(8), 890-898.
[PMID: 27746872]
Esposito, E.; Dal Toso, R.; Pressi, G.; Bramanti, P.; Meli, R.; Cuzzocrea, S. Protective effect of verbascoside in activated C6 glioma cells: possible molecular mechanisms. Naunyn Schmiedebergs Arch. Pharmacol., 2010, 381(1), 93-105.
[] [PMID: 19904526]
Ahn, J.H.; Choi, J.W.; Choi, J.M.; Maeda, T.; Fujii, H.; Yokozawa, T.; Cho, E.J. Protective role of oligonol from oxidative stress-induced inflammation in C6 glial cell. Nutr. Res. Pract., 2015, 9(2), 123-128.
[] [PMID: 25861417]
Chakrabarti, M.; Ray, S.K. Synergistic anti-tumor actions of luteolin and silibinin prevented cell migration and invasion and induced apoptosis in glioblastoma SNB19 cells and glioblastoma stem cells. Brain Res., 2015, 1629, 85-93.
[] [PMID: 26471408]
Sangngern, M. Evaluation of natural products derived from Physalis peruviana (poha) as anticancer agents. Pharmaceutical Science, 2016.
Kim, Y-J.; Hwang, S-Y.; Han, I-O. Insoluble matrix components of glioma cells suppress LPS-mediated iNOS/NO induction in microglia. Biochem. Biophys. Res. Commun., 2006, 347(3), 731-738.
[] [PMID: 16843440]
Haregewoin, A.; Alexander, E., III; Black, P.M.; Loeffler, J.S. Autocrine regulation of the production of the gaseous messenger nitric oxide in a glioblastoma cell line. Exp. Cell Res., 1994, 210(1), 137-139.
[] [PMID: 8269990]
Kitamura, Y.; Furukawa, M.; Matsuoka, Y.; Tooyama, I.; Kimura, H.; Nomura, Y.; Taniguchi, T. In vitro and in vivo induction of heme oxygenase-1 in rat glial cells: possible involvement of nitric oxide production from inducible nitric oxide synthase. Glia, 1998, 22(2), 138-148.
[<138:AID-GLIA5>3.0.CO;2-3] [PMID: 9537834]
Eun, C-S.; Lim, J-S.; Lee, J.; Lee, S-P.; Yang, S-A. The protective effect of fermented Curcuma longa L. on memory dysfunction in oxidative stress-induced C6 gliomal cells, proinflammatory-activated BV2 microglial cells, and scopolamine-induced amnesia model in mice. BMC Complement. Altern. Med., 2017, 17(1), 367.
[] [PMID: 28716085]
Sun, G.Y.; Li, R.; Cui, J.; Hannink, M.; Gu, Z.; Fritsche, K.L.; Lubahn, D.B.; Simonyi, A. Withania somnifera and its withanolides attenuate oxidative and inflammatory responses and up-regulate antioxidant responses in BV-2 microglial cells. Neuromolecular Med., 2016, 18(3), 241-252.
[] [PMID: 27209361]
Lee, S-J.; Lee, I-S.; Mar, W. Inhibition of inducible nitric oxide synthase and cyclooxygenase-2 activity by 1,2,3,4,6-penta-O-galloyl-β-D-glucose in murine macrophage cells. Arch. Pharm. Res., 2003, 26(10), 832-839.
[] [PMID: 14609132]
Kim, H-J.; Kang, C-H.; Jayasooriya, R.G.P.T.; Dilshara, M.G.; Lee, S.; Choi, Y.H.; Seo, Y.T.; Kim, G.Y. Hydrangenol inhibits lipopolysaccharide-induced nitric oxide production in BV2 microglial cells by suppressing the NF-κB pathway and activating the Nrf2-mediated HO-1 pathway. Int. Immunopharmacol., 2016, 35, 61-69.
[] [PMID: 27032067]
Ko, H.J.; Lee, H.; Lee, D-S.; Woo, E-R. Chemical constituents from the aerial parts of Artemisia absinthium and its inhibitory effects of nitric oxide production in RAW264. 7 and BV2 microglia. Korean J. Pharmacogn., 2018, 49(1), 1-6.
Li, X.J.; Kim, K.W.; Ko, W.; Kim, D-C.; Yoon, C-S.; Liu, X.Q.; Oh, H.; Kim, Y-C. Triterpenes with inhibitory effects of nitric oxide production from the fruit galls of Actinidia polygama on LPS-induced RAW264. 7 and BV2 cells. Korean J. Pharmacogn., 2017, 48(2), 108-112.
Hwang, J.H.; Kumar, V.R.; Kang, S.Y.; Jung, H.W.; Park, Y-K. Effects of flower buds extract of Tussilago farfara on focal cerebral ischemia in rats and inflammatory response in BV2 microglia. Chin. J. Integr. Med., 2018, 24(11), 844-852.
[] [PMID: 30090976]
Onasanwo, S.A.; Velagapudi, R.; El-Bakoush, A.; Olajide, O.A. Inhibition of neuroinflammation in BV2 microglia by the biflavonoid kolaviron is dependent on the Nrf2/ARE antioxidant protective mechanism. Mol. Cell. Biochem., 2016, 414(1-2), 23-36.
[] [PMID: 26838169]
Pan, L-L.; Xu, P.; Luo, X-L.; Wang, L-J.; Liu, S-Y.; Zhu, Y-Z.; Hu, J.F.; Liu, X.H. Shizukaol B, an active sesquiterpene from Chloranthus henryi, attenuates LPS-induced inflammatory responses in BV2 microglial cells. Biomed. Pharmacother., 2017, 88, 878-884.
[] [PMID: 28178617]
Folashade, A.O.; Mutalib, A.A.; Satyajit, D.S.; Olajide, O. Zanthoxylum zanthoxyoides root extract inhibits hemozoininduced neuroinflammation in BV2 microglia. Planta Medica. Int. Open, 2017, 4(S01), S1-S202.
Chen, C.; Yuanyuan, Q. Effect of wasabi extract on inflammatory response of BV2 cells induced by lipopolysaccharide. E3S Web Conf. 2019, 7801011.
Al-Abd, N.M.; Kassim, M.; Zajmi, A. The inhibitory effect of galangin on cytokines and nitric oxide in microglia BV2 cell line. Malaysian J. Sci., 2017, 36(3), 145-156.
Xu, P.; Huang, M-W.; Xiao, C-X.; Long, F.; Wang, Y.; Liu, S-Y.; Jia, W.W.; Wu, W.J.; Yang, D.; Hu, J.F.; Liu, X.H.; Zhu, Y.Z. Matairesinol suppresses neuroinflammation and migration associated with Src and ERK1/2-NF-κB pathway in activating BV2 microglia. Neurochem. Res., 2017, 42(10), 2850-2860.
[] [PMID: 28512713]
Kim, D-C.; Yoon, C-S.; Quang, T.H.; Ko, W.; Kim, J-S.; Oh, H.; Kim, Y.C. Prenylated flavonoids from Cudrania tricuspidata suppress lipopolysaccharide-induced neuroinflammatory activities in BV2 microglial cells. Int. J. Mol. Sci., 2016, 17(2), 255.
[] [PMID: 26907256]
Lee, H.H.; Jeong, J-W.; Hong, S.H.; Park, C.; Kim, B.W.; Choi, Y.H. Diallyl trisulfide suppresses the production of lipopolysaccharide-induced inflammatory mediators in BV2 microglia by decreasing the NF-κB pathway activity associated with toll-like receptor 4 and CXCL12/CXCR4 pathway blockade. J. Cancer Prev., 2018, 23(3), 134-140.
[] [PMID: 30370258]
Yoo, G.; Park, S.J.; Lee, T.H.; Yang, H.; Baek, Y.S.; Kim, N.; Kim, Y.J.; Kim, S.H. Flavonoids isolated from Lespedeza cuneata G. Don and their inhibitory effects on nitric oxide production in lipopolysaccharide-stimulated BV-2 microglia cells. Pharmacogn. Mag., 2015, 11(43), 651-656.
[] [PMID: 26246745]
Lee, K.P.; Choi, N.H.; Kim, H-S.; Ahn, S.; Park, I-S.; Lee, D.W. Anti-neuroinflammatory effects of ethanolic extract of black chokeberry (Aronia melanocapa L.) in lipopolysaccharide-stimulated BV2 cells and ICR mice. Nutr. Res. Pract., 2018, 12(1), 13-19.
[] [PMID: 29399292]
Choi, Y.H. Catalpol attenuates lipopolysaccharide-induced inflammatory responses in BV2 microglia through inhibiting the TLR4-mediated NF-κB pathway. Gen. Physiol. Biophys., 2019, 38(2), 111-122.
[] [PMID: 30806632]
Park, B-K.; Kim, Y.H.; Kim, Y.R.; Choi, J.J.; Yang, C.; Jang, I.S.; Lee, M.Y. Antineuroinflammatory and neuroprotective effects of gyejibokryeong-hwan in lipopolysaccharide-stimulated BV2 microglia. Evid. Based Complement. Alternat. Med., 2019, 20197585896
[] [PMID: 31057653]
Lee, S.R.; Kim, M.S.; Kim, S.; Hwang, K.W.; Park, S.Y. Constituents from Scutellaria barbata inhibiting nitric oxide production in LPS‐stimulated microglial cells. Chem. Biodivers., 2017, 14(11)e1700231
[] [PMID: 28805952]
Jones, E; Govindarajulu, M; Ramesh, S; Dhanasekaran, M Honokiol attenuates amyloid-beta induced neuroinflammatory microglial polarization in BV2 microglial cells.The FASEB J., 201933(1_supplement). , 501-505.
Qian, Y.; Xin, Z.; Lv, Y.; Wang, Z.; Zuo, L.; Huang, X.; Li, Y.; Xin, H.B. Asiatic acid suppresses neuroinflammation in BV2 microglia via modulation of the Sirt1/NF-κB signaling pathway. Food Funct., 2018, 9(2), 1048-1057.
[] [PMID: 29354820]
Cho, K-H.; Kim, D-C.; Yoon, C.S.; Ko, W.M.; Lee, S.J.; Sohn, J.H.; Jang, J.H.; Ahn, J.S.; Kim, Y.C.; Oh, H. Anti-neuroinflammatory effects of citreohybridonol involving TLR4-MyD88-mediated inhibition of NF-кB and MAPK signaling pathways in lipopolysaccharide-stimulated BV2 cells. Neurochem. Int., 2016, 95, 55-62.
[] [PMID: 26724567]
Oh, S-J.; Joung, E-J.; Kwon, M-S.; Lee, B.; Utsuki, T.; Oh, C-W.; Kim, H.R. Anti-inflammatory effect of ethanolic extract of Sargassum serratifolium in lipopolysaccharide-stimulated BV2 microglial cells. J. Med. Food, 2016, 19(11), 1023-1031.
[] [PMID: 27845863]
Kim, S.Y.; Jin, C.Y.; Kim, C.H.; Yoo, Y.H.; Choi, S.H.; Kim, G.Y.; Yoon, H.M.; Park, H.T.; Choi, Y.H. Isorhamnetin alleviates lipopolysaccharide-induced inflammatory responses in BV2 microglia by inactivating NF-κB, blocking the TLR4 pathway and reducing ROS generation. Int. J. Mol. Med., 2019, 43(2), 682-692.
[] [PMID: 30483725]
Mairuae, N.; Cheepsunthorn, P.; Cheepsunthorn, C.L.; Tongjaroenbuangam, W. Okra (Abelmoschus esculentus Linn.) inhibits lipopolysaccharide-induced inflammatory mediators in BV2 microglial cells. Trop. J. Pharm. Res., 2017, 16(6), 1285-1292.
Mairuae, N.; Cheepsunthorn, P.; Buranrat, B. Anti-inflammatory and anti-oxidative effects of Centella asiatica extract in lipopolysaccharide-stimulated BV2 microglial cells. Pharmacogn. Mag., 2019, 15(60), 140.
Guo, C.; Yang, L.; Wan, C-X.; Xia, Y-Z.; Zhang, C.; Chen, M-H.; Wang, Z.D.; Li, Z.R.; Li, X.M.; Geng, Y.D.; Kong, L.Y. Anti-neuroinflammatory effect of Sophoraflavanone G from Sophora alopecuroides in LPS-activated BV2 microglia by MAPK, JAK/STAT and Nrf2/HO-1 signaling pathways. Phytomedicine, 2016, 23(13), 1629-1637.
[] [PMID: 27823627]
Yu, J-Y.; Ha, J.Y.; Kim, K-M.; Jung, Y-S.; Jung, J-C.; Oh, S. Anti-inflammatory activities of licorice extract and its active compounds, glycyrrhizic acid, liquiritin and liquiritigenin, in BV2 cells and mice liver. Molecules, 2015, 20(7), 13041-13054.
[] [PMID: 26205049]
Kim, D-C.; Quang, T.H.; Yoon, C-S.; Ngan, N.T.T.; Lim, S-I.; Lee, S-Y.; Kim, Y.C.; Oh, H. Anti-neuroinflammatory activities of indole alkaloids from kanjang (Korean fermented soy source) in lipopolysaccharide-induced BV2 microglial cells. Food Chem., 2016, 213, 69-75.
[] [PMID: 27451156]
Wu, W-Y.; Wu, Y-Y.; Huang, H.; He, C.; Li, W.Z.; Wang, H-L.; Chen, H.Q.; Yin, Y.Y. Biochanin A attenuates LPS-induced pro-inflammatory responses and inhibits the activation of the MAPK pathway in BV2 microglial cells. Int. J. Mol. Med., 2015, 35(2), 391-398.
[] [PMID: 25483920]
Luo, X-L.; Liu, S-Y.; Wang, L-J.; Zhang, Q-Y.; Xu, P.; Pan, L-L.; Hu, J.F. A tetramethoxychalcone from Chloranthus henryi suppresses lipopolysaccharide-induced inflammatory responses in BV2 microglia. Eur. J. Pharmacol., 2016, 774, 135-143.
[] [PMID: 26852953]
Kim, H-Y.; Jang, S-Y.; Jeong, J.; Shin, H. The effects of gokgisaeng on anti-inflammation and Rat C6 glioma cell migration. J. Intern. Korean Med., 2013, 34(1), 31-45.
[] [PMID: 24574831]
Patel, S.S.; Mahindroo, N.; Udayabanu, M. Urtica dioica leaves modulates hippocampal smoothened-glioma associated oncogene-1 pathway and cognitive dysfunction in chronically stressed mice. Biomed. Pharmacother., 2016, 83, 676-686.
[] [PMID: 27470568]
Yamaguchi, S.; Bell, H.S.; Shinoda, J.; Holmes, M.C.; Wharton, S.B.; Whittle, I.R. Glioma tumourgenicity is decreased by iNOS knockout: experimental studies using the C6 striatal implantation glioma model. Br. J. Neurosurg., 2002, 16(6), 567-572.
[] [PMID: 12617238]
Guo, J.S.; Cheng, C.L.; Koo, M.W.L. Inhibitory effects of Centella asiatica water extract and asiaticoside on inducible nitric oxide synthase during gastric ulcer healing in rats. Planta Med., 2004, 70(12), 1150-1154.
[] [PMID: 15643549]
Kim, Y.H.; Ko, W.S.; Ha, M.S.; Lee, C.H.; Choi, B.T.; Kang, H.S.; Kim, H.D. The production of nitric oxide and TNF-α in peritoneal macrophages is inhibited by Dichroa febrifuga Lour. J. Ethnopharmacol., 2000, 69(1), 35-43.
[] [PMID: 10661882]
Goel, V.; Chang, C.; Slama, J.; Barton, R.; Bauer, R.; Gahler, R.; Basu, T. Echinacea stimulates macrophage function in the lung and spleen of normal rats. J. Nutr. Biochem., 2002, 13(8), 487-492.
[] [PMID: 12165361]
Ganju, L.; Karan, D.; Chanda, S.; Srivastava, K.K.; Sawhney, R.C.; Selvamurthy, W. Immunomodulatory effects of agents of plant origin. Biomed. Pharmacother., 2003, 57(7), 296-300.
[] [PMID: 14499177]
Kwan, C-Y.; Zhang, W-B.; Deyama, T.; Nishibe, S. Endothelium-dependent vascular relaxation induced by Eucommia ulmoides Oliv. bark extract is mediated by NO and EDHF in small vessels. Naunyn Schmiedebergs Arch. Pharmacol., 2004, 369(2), 206-211.
[] [PMID: 14673511]
Rawal, A.K.; Muddeshwar, M.G.; Biswas, S.K. Rubia cordifolia, Fagonia cretica Linn. and Tinospora cordifolia exert neuroprotection by modulating the antioxidant system in rat hippocampal slices subjected to oxygen glucose deprivation. BMC Complement. Altern. Med., 2004, 4(1), 11.
[] [PMID: 15310392]
Ferreira, A.P.; Soares, G.L.; Salgado, C.A.; Gonçalves, L.S.; Teixeira, F.M.; Teixeira, H.C.; Kaplan, M.A. Immunomodulatory activity of Mollugo verticillata L. Phytomedicine, 2003, 10(2-3), 154-158.
[] [PMID: 12725569]
Makino, T.; Ono, T.; Muso, E.; Honda, G.; Sasayama, S. Suppressive effects of Perilla frutescens on spontaneous IgA nephropathy in ddY mice. Nephron, 1999, 83(1), 40-46.
[] [PMID: 10461034]
Medeiros, I.A.; Santos, M.R.; Nascimento, N.M.; Duarte, J.C. Cardiovascular effects of Sida cordifolia leaves extract in rats. Fitoterapia, 2006, 77(1), 19-27.
[] [PMID: 16257496]
Ko, W.S.; Kim, Y.H.; Yoon, J.W.; Yoon, S.W.; Kim, H.D. Inhibitory effect of Spirodela polyrhixa on the secretion of NO in LPS-stimulated macrophages. Am. J. Chin. Med., 2004, 32(01), 65-73.
[] [PMID: 15154286]
Voisin, P.; Bouchaud, V.; Merle, M.; Diolez, P.; Duffy, L.; Flint, K.; Franconi, J-M.; Bouzier-Sore, A-K. Microglia in close vicinity of glioma cells: correlation between phenotype and metabolic alterations. Front. Neuroenergetics, 2010, 2, 131.
[] [PMID: 21031160]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy