The Cytoprotective and Anti-cancer Potential of Bisbenzylisoquinoline Alkaloids from Nelumbo nucifera

Author(s): Prasath Manogaran, Narasimha Murthy Beeraka, Viswanadha Vijaya Padma*

Journal Name: Current Topics in Medicinal Chemistry

Volume 19 , Issue 32 , 2019

DOI : 10.2174/1568026619666191116160908

  Journal Home
Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Natural product therapy has been gaining therapeutic importance against various diseases, including cancer. The failure of chemotherapy due to its associated adverse effects promoted adjunct therapy with natural products. Phytochemicals exert anti-carcinogenic activities through the regulation of various cell signaling pathways such as cell survival, inflammation, apoptosis, autophagy and metastasis. The ‘small molecule-chemosensitizing agents’ from plants induce apoptosis in drug-resistant and host-immune resistant cancer cells in in vitro as well as in vivo models. For example, alkaloids from Nelumbo nucifera, liensinine, isoliensinine and neferine exert the anticancer activity through enhanced ROS generation, activation of MAP kinases, followed by induction of autophagy and apoptotic cell death. Likewise, these alkaloids also exert their cytoprotective action against cerebrovascular stroke/ischemic stroke, diabetes, and chemotherapy-induced cytotoxicity. Therefore, the present review elucidates the pharmacological activities of these bisbenzylisoquinoline alkaloids which include the cytoprotective, anticancer and chemosensitizing abilities against various diseases such as cardiovascular diseases, neurological diseases and cancer.

Keywords: Bisbenzylisoquinoline alkaloids, Neferine, Isoliensinine, Cell signaling pathways, Apoptosis, Autophagy, Inflammation, Cytoprotective, Anticancer, Chemosensitizing effect.

[1]
Demain, A.L.; Vaishnav, P. Natural products for cancer chemotherapy. Microb. Biotechnol., 2011, 4(6), 687-699.
[http://dx.doi.org/10.1111/j.1751-7915.2010.00221.x] [PMID: 21375717]
[2]
Zhang, H.; Yu, T.; Wen, L.; Wang, H.; Fei, D.; Jin, C. Curcumin enhances the effectiveness of cisplatin by suppressing CD133+ cancer stem cells in laryngeal carcinoma treatment. Exp. Ther. Med., 2013, 6(5), 1317-1321.
[http://dx.doi.org/10.3892/etm.2013.1297] [PMID: 24223665]
[3]
Yunos, N.M.; Beale, P.; Yu, J.Q.; Huq, F. Synergism from sequenced combinations of curcumin and epigallocatechin-3-gallate with cisplatin in the killing of human ovarian cancer cells. Anticancer Res., 2011, 31(4), 1131-1140.
[PMID: 21508356]
[4]
Wei, Y.; Pu, X.; Zhao, L. Preclinical studies for the combination of paclitaxel and curcumin in cancer therapy (Review). Oncol. Rep., 2017, 37(6), 3159-3166.
[http://dx.doi.org/10.3892/or.2017.5593] [PMID: 28440434]
[5]
Lu, Y.; Wang, J.; Liu, L.; Yu, L.; Zhao, N.; Zhou, X.; Lu, X. Curcumin increases the sensitivity of Paclitaxel-resistant NSCLC cells to Paclitaxel through microRNA-30c-mediated MTA1 reduction. Tumour Biol., 2017, 39(4) 1010428317698353
[http://dx.doi.org/10.1177/1010428317698353] [PMID: 28443468]
[6]
Quispe-Soto, E.T.; Calaf, G.M. Effect of curcumin and paclitaxel on breast carcinogenesis. Int. J. Oncol., 2016, 49(6), 2569-2577.
[http://dx.doi.org/10.3892/ijo.2016.3741] [PMID: 27779649]
[7]
Paudel, K.R.; Panth, N. Phytochemical profile and biological activity of Nelumbo nucifera. Evid. Based Complement. Alternat. Med., 2015, 2015 789124
[8]
Mukherjee, P.K.; Mukherjee, D.; Maji, A.K.; Rai, S.; Heinrich, M. The sacred lotus (Nelumbo nucifera) - phytochemical and therapeutic profile. J. Pharm. Pharmacol., 2009, 61(4), 407-422.
[http://dx.doi.org/10.1211/jpp.61.04.0001] [PMID: 19298686]
[9]
Wang, C.; Chen, Y.F.; Quan, X.Q.; Wang, H.; Zhang, R.; Xiao, J.H.; Wang, J.L.; Zhang, C.T.; Xiang, J.Z.; Tang, Q. Effects of neferine on Kv4.3 channels expressed in HEK293 cells and ex vivo electrophysiology of rabbit hearts. Acta Pharmacol. Sin., 2015, 36(12), 1451-1461.
[http://dx.doi.org/10.1038/aps.2015.83] [PMID: 26592512]
[10]
Qian, J.Q. Cardiovascular pharmacological effects of bisbenzylisoquinoline alkaloid derivatives. Acta Pharmacol. Sin., 2002, 23(12), 1086-1092.
[PMID: 12466045]
[11]
Xu, L.; Zhang, X.; Li, Y.; Lu, S.; Lu, S.; Li, J.; Wang, Y.; Tian, X.; Wei, J.J.; Shao, C.; Liu, Z. Neferine induces autophagy of human ovarian cancer cells via p38 MAPK/JNK activation. Tumour Biol., 2016, 37(7), 8721-8729.
[http://dx.doi.org/10.1007/s13277-015-4737-8] [PMID: 26738868]
[12]
Poornima, P.; Kumar, V.B.; Weng, C.F.; Padma, V.V. Doxorubicin induced apoptosis was potentiated by neferine in human lung adenocarcima, A549 cells. Food Chem. Toxicol., 2014, 68, 87-98.
[http://dx.doi.org/10.1016/j.fct.2014.03.008] [PMID: 24632453]
[13]
Poornima, P.; Quency, R.S.; Padma, V.V. Neferine induces reactive oxygen species mediated intrinsic pathway of apoptosis in HepG2 cells. Food Chem., 2013, 136(2), 659-667.
[http://dx.doi.org/10.1016/j.foodchem.2012.07.112] [PMID: 23122111]
[14]
Poornima, P.; Weng, C.F.; Padma, V.V. Neferine from Nelumbo nucifera induces autophagy through the inhibition of PI3K/Akt/mTOR pathway and ROS hyper generation in A549 cells. Food Chem., 2013, 141(4), 3598-3605.
[http://dx.doi.org/10.1016/j.foodchem.2013.05.138] [PMID: 23993526]
[15]
Jung, H.A.; Jin, S.E.; Choi, R.J.; Kim, D.H.; Kim, Y.S.; Ryu, J.H.; Kim, D-W.; Son, Y.K.; Park, J.J.; Choi, J.S. Anti-amnesic activity of neferine with antioxidant and anti-inflammatory capacities, as well as inhibition of ChEs and BACE1. Life Sci., 2010, 87(13-14), 420-430.
[http://dx.doi.org/10.1016/j.lfs.2010.08.005] [PMID: 20736023]
[16]
Zhou, H.; Jiang, H.; Yao, T.; Zeng, S. Fragmentation study on the phenolic alkaloid neferine and its analogues with anti-HIV activities by electrospray ionization tandem mass spectrometry with hydrogen/deuterium exchange and its application for rapid identification of in vitro microsomal metabolites of neferine. Rapid Commun. Mass Spectrom., 2007, 21(13), 2120-2128.
[http://dx.doi.org/10.1002/rcm.3070] [PMID: 17546644]
[17]
Li, X.C.; Tong, G.X.; Zhang, Y.; Liu, S.X.; Jin, Q.H.; Chen, H.H.; Chen, P. Neferine inhibits angiotensin II-stimulated proliferation in vascular smooth muscle cells through heme oxygenase-1. Acta Pharmacol. Sin., 2010, 31(6), 679-686.
[http://dx.doi.org/10.1038/aps.2010.57] [PMID: 20523338]
[18]
Hu, X.; Guo, Z.; Zhou, B.; Luo, S.; Cai, H. Quantitative determination of neferine in plumula Nelumbinis by thin layer chromatography scanning. Zhongguo Zhongyao Zazhi, 1997, 22(1), 41-42, 62.
[PMID: 10683912]
[19]
Chen, Y.; Fan, G.; Wu, H.; Wu, Y.; Mitchell, A. Separation, identification and rapid determination of liensine, isoliensinine and neferine from embryo of the seed of Nelumbo nucifera Gaertn. by liquid chromatography coupled to diode array detector and tandem mass spectrometry. J. Pharm. Biomed. Anal., 2007, 43(1), 99-104.
[http://dx.doi.org/10.1016/j.jpba.2006.06.016] [PMID: 16846715]
[20]
Fang, Y.; Li, Q.; Shao, Q.; Wang, B.; Wei, Y. A general ionic liquid pH-zone-refining countercurrent chromatography method for separation of alkaloids from Nelumbo nucifera Gaertn. J. Chromatogr. A, 2017, 1507, 63-71.
[http://dx.doi.org/10.1016/j.chroma.2017.05.048] [PMID: 28571916]
[21]
Wang, Y.; Zhang, L.; Zhou, H.; Guo, X.; Wu, S. K-targeted strategy for isolation of phenolic alkaloids of Nelumbo nucifera Gaertn by counter-current chromatography using lysine as a pH regulator. J. Chromatogr. A, 2017, 1490, 115-125.
[http://dx.doi.org/10.1016/j.chroma.2017.02.022] [PMID: 28236459]
[22]
Huang, Y.; Bai, Y.; Zhao, L.; Hu, T.; Hu, B.; Wang, J.; Xiang, J. Pharmacokinetics and metabolism of neferine in rats after a single oral administration. Biopharm. Drug Dispos., 2007, 28(7), 361-372.
[http://dx.doi.org/10.1002/bdd.556] [PMID: 17654697]
[23]
Zhou, H.; Li, L.; Jiang, H.; Zeng, S. Identification of three new N-demethylated and O-demethylated bisbenzylisoquinoline alkaloid metabolites of isoliensinine from dog hepatic microsomes. Molecules, 2012, 17(10), 11712-11720.
[http://dx.doi.org/10.3390/molecules171011712] [PMID: 23027371]
[24]
Li, G.R.; Li, X.G.; Lü, F.H. Effects of neferine on transmembrane potentials of guinea pig myocardium. Zhongguo Yao Li Xue Bao, 1989, 10(5), 406-410.
[PMID: 2618727]
[25]
Yu, J.; Hu, W. Effects of neferine on platelet aggregation and concentration of cytoplasmic free calcium. Zhongguo Yaolixue Yu Dulixue Zazhi, 1996, 10(2), 120-122.
[26]
Lalitha, G.; Poornima, P.; Archanah, A.; Padma, V.V. Protective effect of neferine against isoproterenol-induced cardiac toxicity. Cardiovasc. Toxicol., 2013, 13(2), 168-179.
[http://dx.doi.org/10.1007/s12012-012-9196-5] [PMID: 23274852]
[27]
Priya, L.B.; Baskaran, R.; Huang, C-Y.; Padma, V.V. Neferine ameliorates cardiomyoblast apoptosis induced by doxorubicin: possible role in modulating NADPH oxidase/ROS-mediated NFκB redox signaling cascade. Sci. Rep., 2017, 7(1), 12283.
[http://dx.doi.org/10.1038/s41598-017-12060-9] [PMID: 28947826]
[28]
Bharathi Priya, L.; Baskaran, R.; Huang, C.Y.; Vijaya Padma, V. Neferine modulates IGF-1R/Nrf2 signaling in doxorubicin treated H9c2 cardiomyoblasts. J. Cell. Biochem., 2018, 119(2), 1441-1452.
[http://dx.doi.org/10.1002/jcb.26305] [PMID: 28731223]
[29]
Sugimoto, Y.; Furutani, S.; Nishimura, K.; Itoh, A.; Tanahashi, T.; Nakajima, H.; Oshiro, H.; Sun, S.; Yamada, J. Antidepressant-like effects of neferine in the forced swimming test involve the serotonin1A (5-HT1A) receptor in mice. Eur. J. Pharmacol., 2010, 634(1-3), 62-67.
[http://dx.doi.org/10.1016/j.ejphar.2010.02.016] [PMID: 20176013]
[30]
Wong, V.K.; Wu, A.G.; Wang, J.R.; Liu, L.; Law, B.Y. Neferine attenuates the protein level and toxicity of mutant huntingtin in PC-12 cells via induction of autophagy. Molecules, 2015, 20(3), 3496-3514.
[http://dx.doi.org/10.3390/molecules20033496] [PMID: 25699594]
[31]
Kim, E.S.; Weon, J.B.; Yun, B-R.; Lee, J.; Eom, M.R.; Oh, K-H.; Ma, C.J. Cognitive enhancing and neuroprotective effect of the embryo of the Nelumbo nucifera seed. Evid. Based Complement. Alternat. Med., 2014, 2014 869831
[http://dx.doi.org/10.1155/2014/869831]
[32]
Wu, C.; Chen, J.; Yang, R.; Duan, F.; Li, S.; Chen, X. Mitochondrial protective effect of neferine through the modulation of nuclear factor erythroid 2-related factor 2 signalling in ischaemic stroke. Br. J. Pharmacol., 2019, 176(3), 400-415.
[http://dx.doi.org/10.1111/bph.14537] [PMID: 30414381]
[33]
Qin, Y.; Stokman, G.; Yan, K.; Ramaiahgari, S.; Verbeek, F.; de Graauw, M.; van de Water, B.; Price, L.S. cAMP signalling protects proximal tubular epithelial cells from cisplatin-induced apoptosis via activation of Epac. Br. J. Pharmacol., 2012, 165(4b), 1137-1150.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01594.x] [PMID: 21745194]
[34]
Kim, T-W.; Kim, Y-J.; Kim, H-T.; Park, S-R.; Lee, M-Y.; Park, Y-D.; Lee, C-H.; Jung, J-Y. NQO1 deficiency leads enhanced autophagy in cisplatin-induced acute kidney injury through the AMPK/TSC2/mTOR signaling pathway. Antioxid. Redox Signal., 2016, 24(15), 867-883.
[http://dx.doi.org/10.1089/ars.2015.6386]
[35]
Li, H.; Tang, Y.; Wen, L.; Kong, X.; Chen, X.; Liu, P.; Zhou, Z.; Chen, W.; Xiao, C.; Xiao, P.; Xiao, X. Neferine reduces cisplatin-induced nephrotoxicity by enhancing autophagy via the AMPK/mTOR signaling pathway. Biochem. Biophys. Res. Commun., 2017, 484(3), 694-701.
[http://dx.doi.org/10.1016/j.bbrc.2017.01.180] [PMID: 28161641]
[36]
Baskaran, R.; Poornima, P.; Huang, C.Y.; Padma, V.V. Neferine prevents NF-κB translocation and protects muscle cells from oxidative stress and apoptosis induced by hypoxia. Biofactors, 2016, 42(4), 407-417.
[http://dx.doi.org/10.1002/biof.1286] [PMID: 27041079]
[37]
Baskaran, R.; Poornima, P.; Priya, L.B.; Huang, C-Y.; Padma, V.V. Neferine prevents autophagy induced by hypoxia through activation of Akt/mTOR pathway and Nrf2 in muscle cells. Biomed. Pharmacother., 2016, 83, 1407-1413.
[http://dx.doi.org/10.1016/j.biopha.2016.08.063] [PMID: 27583981]
[38]
Baskaran, R.; Priya, L.B.; Kalaiselvi, P.; Poornima, P.; Huang, C-Y.; Padma, V.V. Neferine from Nelumbo nucifera modulates oxidative stress and cytokines production during hypoxia in human peripheral blood mononuclear cells. Biomed. Pharmacother., 2017, 93, 730-736.
[http://dx.doi.org/10.1016/j.biopha.2017.07.003] [PMID: 28700977]
[39]
Zhou, J.; Li, P.; Xue, X.; He, S.; Kuang, Y.; Zhao, H.; Chen, S.; Zhi, Q.; Guo, X. Salinomycin induces apoptosis in cisplatin-resistant colorectal cancer cells by accumulation of reactive oxygen species. Toxicol. Lett., 2013, 222(2), 139-145.
[http://dx.doi.org/10.1016/j.toxlet.2013.07.022] [PMID: 23916687]
[40]
Eid, W.; Abdel-Rehim, W. Neferine enhances the antitumor effect of mitomycin‐C in hela cells through the activation of p38‐MAPK pathway. J. Cell. Biochem., 2017, 118(10), 3472-3479.
[http://dx.doi.org/10.1002/jcb.26006] [PMID: 28328092]
[41]
Baharuddin, P.; Satar, N.; Fakiruddin, K.S.; Zakaria, N.; Lim, M.N.; Yusoff, N.M.; Zakaria, Z.; Yahaya, B.H. Curcumin improves the efficacy of cisplatin by targeting cancer stem-like cells through p21 and cyclin D1-mediated tumour cell inhibition in non-small cell lung cancer cell lines. Oncol. Rep., 2016, 35(1), 13-25.
[http://dx.doi.org/10.3892/or.2015.4371] [PMID: 26531053]
[42]
Kumar, P.; Barua, C.C.; Sulakhiya, K.; Sharma, R.K. Curcumin ameliorates cisplatin-induced nephrotoxicity and potentiates its anticancer activity in SD rats: potential role of curcumin in breast cancer chemotherapy. Front. Pharmacol., 2017, 8, 132.
[http://dx.doi.org/10.3389/fphar.2017.00132] [PMID: 28420987]
[43]
Mohajeri, M.; Sahebkar, A. Protective effects of curcumin against doxorubicin-induced toxicity and resistance: A review. Crit. Rev. Oncol. Hematol., 2018, 122, 30-51.
[http://dx.doi.org/10.1016/j.critrevonc.2017.12.005] [PMID: 29458788]
[44]
Wei, Y.; Yang, P.; Cao, S.; Zhao, L. The combination of curcumin and 5-fluorouracil in cancer therapy. Arch. Pharm. Res., 2018, 41(1), 1-13.
[http://dx.doi.org/10.1007/s12272-017-0979-x] [PMID: 29230689]
[45]
Cragg, G.M.; Pezzuto, J.M. Natural products as a vital source for the discovery of cancer chemotherapeutic and chemopreventive agents. Med. Princ. Pract., 2016, 25(Suppl. 2), 41-59.
[http://dx.doi.org/10.1159/000443404] [PMID: 26679767]
[46]
Wang, H.; Oo Khor, T.; Shu, L.; Su, Z.-Y.; Fuentes, F.; Lee, J.-H.; Tony Kong, A.-N. A.-N. Plants vs. cancer: a review on natural phytochemicals in preventing and treating cancers and their druggability. Anti-Cancer Agents Med. Chem. (Formerly Curr. Med. Chem.-Anti-Cancer Agents), 2012, 12(10), 1281-1305.
[47]
Meybodi, N.M.; Mortazavian, A.M.; Monfared, A.B.; Sohrabvandi, S.; Meybodi, F.A. Phytochemicals in cancer prevention: a review of the evidence. Iran. J. Cancer Prev., 2017, 10(1) e7219
[48]
Marthandam Asokan, S.; Mariappan, R.; Muthusamy, S.; Velmurugan, B.K. Pharmacological benefits of neferine - A comprehensive review. Life Sci., 2018, 199, 60-70.
[http://dx.doi.org/10.1016/j.lfs.2018.02.032] [PMID: 29499283]
[49]
Poornima, P.; Weng, C.F.; Padma, V.V. Neferine, an alkaloid from lotus seed embryo, inhibits human lung cancer cell growth by MAPK activation and cell cycle arrest. Biofactors, 2014, 40(1), 121-131.
[http://dx.doi.org/10.1002/biof.1115] [PMID: 23983146]
[50]
Sivalingam, K.; Amirthalingam, V.; Ganasan, K.; Huang, C-Y.; Viswanadha, V.P. Neferine suppresses diethylnitrosamine-induced lung carcinogenesis in Wistar rats. Food Chem. Toxicol., 2019, 123, 385-398.
[http://dx.doi.org/10.1016/j.fct.2018.11.014] [PMID: 30423403]
[51]
Carmeliet, P.; Jain, R.K. Angiogenesis in cancer and other diseases. Nature, 2000, 407(6801), 249-257.
[http://dx.doi.org/10.1038/35025220] [PMID: 11001068]
[52]
Carmeliet, P. VEGF as a key mediator of angiogenesis in cancer. Oncology, 2005, 69(Suppl. 3), 4-10.
[http://dx.doi.org/10.1159/000088478] [PMID: 16301830]
[53]
Cortez, A.J.; Tudrej, P.; Kujawa, K.A.; Lisowska, K.M. Advances in ovarian cancer therapy. Cancer Chemother. Pharmacol., 2018, 81(1), 17-38.
[http://dx.doi.org/10.1007/s00280-017-3501-8] [PMID: 29249039]
[54]
Riman, T.; Persson, I.; Nilsson, S. Hormonal aspects of epithelial ovarian cancer: review of epidemiological evidence. Clin. Endocrinol. (Oxf.), 1998, 49(6), 695-707.
[http://dx.doi.org/10.1046/j.1365-2265.1998.00577.x] [PMID: 10209555]
[55]
Zhang, Q.; Li, Y.; Miao, C.; Wang, Y.; Xu, Y.; Dong, R.; Zhang, Z.; Griffin, B.B.; Yuan, C.; Yan, S.; Yang, X.; Liu, Z.; Kong, B. Anti-angiogenesis effect of Neferine via regulating autophagy and polarization of tumor-associated macrophages in high-grade serous ovarian carcinoma. Cancer Lett., 2018, 432, 144-155.
[http://dx.doi.org/10.1016/j.canlet.2018.05.049] [PMID: 29879497]
[56]
Rammohan, A.; Sathyanesan, J.; Rajendran, K.; Pitchaimuthu, A.; Perumal, S-K.; Srinivasan, U.; Ramasamy, R.; Palaniappan, R.; Govindan, M. A gist of gastrointestinal stromal tumors: A review. World J. Gastrointest. Oncol., 2013, 5(6), 102-112.
[http://dx.doi.org/10.4251/wjgo.v5.i6.102] [PMID: 23847717]
[57]
Xue, F.; Liu, Z.; Xu, J.; Xu, X.; Chen, X.; Tian, F. Neferine inhibits growth and migration of gastrointestinal stromal tumor cell line GIST-T1 by up-regulation of miR-449a. Biomed. Pharmacother., 2019, 109, 1951-1959.
[http://dx.doi.org/10.1016/j.biopha.2018.11.029] [PMID: 30551450]
[58]
Liu, Z.; Zhu, J.; Cao, H.; Ren, H.; Fang, X. miR-10b promotes cell invasion through RhoC-AKT signaling pathway by targeting HOXD10 in gastric cancer. Int. J. Oncol., 2012, 40(5), 1553-1560.
[PMID: 22293682]
[59]
Hardell, L.; Carlberg, M.; Hansson Mild, K. Pooled analysis of case-control studies on malignant brain tumours and the use of mobile and cordless phones including living and deceased subjects. Int. J. Oncol., 2011, 38(5), 1465-1474.
[http://dx.doi.org/10.3892/ijo.2011.947] [PMID: 21331446]
[60]
Davis, F.; Il’yasova, D.; Rankin, K.; McCarthy, B.; Bigner, D.D. Medical diagnostic radiation exposures and risk of gliomas. Radiat. Res., 2011, 175(6), 790-796.
[http://dx.doi.org/10.1667/RR2186.1] [PMID: 21466382]
[61]
Reuss, D.; von Deimling, A. Hereditary tumor syndromes and gliomas. Gliomas, 2009, 171, 83-102.
[62]
Liang, H-X.; Sun, L-B.; Liu, N-J. Neferine inhibits proliferation, migration and invasion of U251 glioma cells by down-regulation of miR-10b. Biomed. Pharmacother., 2019, 109, 1032-1040.
[http://dx.doi.org/10.1016/j.biopha.2018.10.122] [PMID: 30551353]
[63]
Rocha, C.R.R.; Silva, M.M.; Quinet, A.; Cabral-Neto, J.B.; Menck, C.F.M. DNA repair pathways and cisplatin resistance: an intimate relationship. Clinics (São Paulo), 2018, 73(Suppl. 1) e478s
[http://dx.doi.org/10.6061/clinics/2018/e478s] [PMID: 30208165]
[64]
Dasari, S.; Tchounwou, P.B. Cisplatin in cancer therapy: molecular mechanisms of action. Eur. J. Pharmacol., 2014, 740, 364-378.
[http://dx.doi.org/10.1016/j.ejphar.2014.07.025] [PMID: 25058905]
[65]
Galluzzi, L.; Vitale, I.; Michels, J.; Brenner, C.; Szabadkai, G.; Harel-Bellan, A.; Castedo, M.; Kroemer, G. Systems biology of cisplatin resistance: past, present and future. Cell Death Dis., 2014, 5(5) e1257
[http://dx.doi.org/10.1038/cddis.2013.428] [PMID: 24874729]
[66]
Huang, C.; Cao, P.; Xie, Z.; Zhu, H. Effect of different heating methods combined with neferine on the expressions of γH2AX and mdr-1/P-gp in MCF-7/Adr breast cancer cells. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 2011, 36(4), 317-322.
[PMID: 21566283]
[67]
Cao, J-G.; Tang, X-Q.; Shi, S-H. Multidrug resistance reversal in human gastric carcinoma cells by neferine. World J. Gastroenterol., 2004, 10(20), 3062-3064.
[PMID: 15378795]
[68]
Kadioglu, O.; Law, B.Y.K.; Mok, S.W.F.; Xu, S-W.; Efferth, T.; Wong, V.K.W. Mode of action analyses of neferine, a bisbenzylisoquinoline alkaloid of lotus (Nelumbo nucifera) against multidrug-resistant tumor cells. Front. Pharmacol., 2017, 8, 238.
[http://dx.doi.org/10.3389/fphar.2017.00238] [PMID: 28529482]
[69]
Lin, X.; Xie, Z.; Qin, Q. Influence of neferine and erythromycin on cellular GSH concentration in K562/A02 cell line. Zhong nan da xue xue bao. J. Cent South Uni. Med. Sci., 2004, 29(3), 284-286.
[70]
Qin, Q.; Xiao, X.; Xie, Z. Effect of neferine combined with mdr-1shRNA on the expression of mdr-1/P-gp in K562/A02 cell line. Zhong nan da xue xue bao. J. Cent South Uni. Med. Sci., 2010, 35(5), 445-450.
[71]
Koosha, S.; Alshawsh, M.A.; Looi, C.Y.; Seyedan, A.; Mohamed, Z. An association map on the effect of flavonoids on the signaling pathways in colorectal cancer. Int. J. Med. Sci., 2016, 13(5), 374-385.
[http://dx.doi.org/10.7150/ijms.14485] [PMID: 27226778]
[72]
Manogaran, P.; Beeraka, N.M.; Huang, C-Y.; Vijaya Padma, V. Neferine and isoliensinine enhance ‘intracellular uptake of cisplatin’ and induce ‘ROS-mediated apoptosis’ in colorectal cancer cells - A comparative study. Food Chem. Toxicol., 2019, 132 110652
[http://dx.doi.org/10.1016/j.fct.2019.110652] [PMID: 31255669]
[73]
Sivalingam, K.S.; Paramasivan, P.; Weng, C.F.; Viswanadha, V.P. Neferine potentiates the antitumor effect of cisplatin in human lung adenocarcinoma cells via a mitochondria-mediated apoptosis Pathway. J. Cell. Biochem., 2017, 118(9), 2865-2876.
[http://dx.doi.org/10.1002/jcb.25937] [PMID: 28214344]
[74]
Kalai Selvi, S.; Vinoth, A.; Varadharajan, T.; Weng, C.F.; Vijaya Padma, V. Neferine augments therapeutic efficacy of cisplatin through ROS- mediated non-canonical autophagy in human lung adenocarcinoma (A549 cells). Food Chem. Toxicol., 2017, 103, 28-40.
[http://dx.doi.org/10.1016/j.fct.2017.02.020] [PMID: 28223119]
[75]
Deng, G.; Zeng, S.; Ma, J.; Zhang, Y.; Qu, Y.; Han, Y.; Yin, L.; Cai, C.; Guo, C.; Shen, H. The anti-tumor activities of Neferine on cell invasion and oxaliplatin sensitivity regulated by EMT via Snail signaling in hepatocellular carcinoma. Sci. Rep., 2017, 7, 41616.
[http://dx.doi.org/10.1038/srep41616] [PMID: 28134289]
[76]
Yang, D.; Zou, X.; Yi, R.; Liu, W.; Peng, D.; Zhao, X. Neferine increase in vitro anticancer effect of dehydroepiandrosterone on MCF-7 human breast cancer cells. App. Biol. Chem., 2016, 59(4), 585-596.
[http://dx.doi.org/10.1007/s13765-016-0199-y]
[77]
Zhang, X.; Wang, X.; Wu, T.; Li, B.; Liu, T.; Wang, R.; Liu, Q.; Liu, Z.; Gong, Y.; Shao, C. Isoliensinine induces apoptosis in triple-negative human breast cancer cells through ROS generation and p38 MAPK/JNK activation. Sci. Rep., 2015, 5, 12579.
[http://dx.doi.org/10.1038/srep12579] [PMID: 26219228]
[78]
Shu, G.; Yue, L.; Zhao, W.; Xu, C.; Yang, J.; Wang, S.; Yang, X. Isoliensinine, a bioactive alkaloid derived from embryos of nelumbo nucifera, induces hepatocellular carcinoma cell apoptosis through suppression of NF-κB signaling. J. Agric. Food Chem., 2015, 63(40), 8793-8803.
[http://dx.doi.org/10.1021/acs.jafc.5b02993] [PMID: 26389520]
[79]
Law, B.Y.K.; Chan, W.K.; Xu, S.W.; Wang, J.R.; Bai, L.P.; Liu, L.; Wong, V.K.W. Natural small-molecule enhancers of autophagy induce autophagic cell death in apoptosis-defective cells. Sci. Rep., 2014, 4, 5510.
[http://dx.doi.org/10.1038/srep05510] [PMID: 24981420]
[80]
Yang, X.; Huang, M.; Yang, J.; Wang, J.; Zheng, S.; Ma, X.; Cai, J.; Deng, S.; Shu, G.; Yang, G. Activity of isoliensinine in improving the symptoms of type 2 diabetic mice via activation of AMP-activated kinase and regulation of PPARγ. J. Agric. Food Chem., 2017, 65(33), 7168-7178.
[http://dx.doi.org/10.1021/acs.jafc.7b01964] [PMID: 28745497]
[81]
Xiao, J-H.; Zhang, Y-L.; Feng, X-L.; Wang, J-L.; Qian, J-Q. Effects of isoliensinine on angiotensin II-induced proliferation of porcine coronary arterial smooth muscle cells. J. Asian Nat. Prod. Res., 2006, 8(3), 209-216.
[http://dx.doi.org/10.1080/1028602042000325609] [PMID: 16864426]
[82]
Meng, X-L.; Zheng, L-C.; Liu, J.; Gao, C-C.; Qiu, M-C.; Liu, Y-Y.; Lu, J.; Wang, D.; Chen, C-L. Inhibitory effects of three bisbenzylisoquinoline alkaloids on lipopolysaccharide-induced microglial activation. RSC Advances, 2017, 7(30), 18347-18357.
[http://dx.doi.org/10.1039/C7RA01882G]
[83]
Wilson, M.S.; Wynn, T.A. Pulmonary fibrosis: pathogenesis, etiology and regulation. Mucosal Immunol., 2009, 2(2), 103-121.
[http://dx.doi.org/10.1038/mi.2008.85] [PMID: 19129758]
[84]
Hu, Y.; Li, M.; Zhang, M.; Jin, Y. Inhalation treatment of idiopathic pulmonary fibrosis with curcumin large porous microparticles. Int. J. Pharm., 2018, 551(1-2), 212-222.
[http://dx.doi.org/10.1016/j.ijpharm.2018.09.031] [PMID: 30227240]
[85]
Allen, J.T.; Spiteri, M.A. Growth factors in idiopathic pulmonary fibrosis: relative roles. Respir. Res., 2002, 3(1), 13.
[http://dx.doi.org/10.1186/rr162] [PMID: 11806848]
[86]
Xiao, J-H.; Zhang, J-H.; Chen, H-L.; Feng, X-L.; Wang, J-L. Inhibitory effects of isoliensinine on bleomycin-induced pulmonary fibrosis in mice. Planta Med., 2005, 71(3), 225-230.
[http://dx.doi.org/10.1055/s-2005-837821] [PMID: 15770542]
[87]
Hu, X.; Liou, A.K.; Leak, R.K.; Xu, M.; An, C.; Suenaga, J.; Shi, Y.; Gao, Y.; Zheng, P.; Chen, J. Neurobiology of microglial action in CNS injuries: receptor-mediated signaling mechanisms and functional roles. Prog. Neurobiol., 2014, 119-120, 60-84.
[http://dx.doi.org/10.1016/j.pneurobio.2014.06.002] [PMID: 24923657]
[88]
Perry, V.H.; Holmes, C. Microglial priming in neurodegenerative disease. Nat. Rev. Neurol., 2014, 10(4), 217-224.
[http://dx.doi.org/10.1038/nrneurol.2014.38] [PMID: 24638131]
[89]
Zhang, F.; Ren, X.; Zhao, M.; Zhou, B.; Han, Y. Angiotensin-(1-7) abrogates angiotensin II-induced proliferation, migration and inflammation in VSMCs through inactivation of ROS-mediated PI3K/Akt and MAPK/ERK signaling pathways. Sci. Rep., 2016, 6, 34621.
[http://dx.doi.org/10.1038/srep34621] [PMID: 27687768]
[90]
Olokoba, A.B.; Obateru, O.A.; Olokoba, L.B. Type 2 diabetes mellitus: a review of current trends. Oman Med. J., 2012, 27(4), 269-273.
[http://dx.doi.org/10.5001/omj.2012.68] [PMID: 23071876]
[91]
Garvey, W.T.; Maianu, L.; Zhu, J-H.; Brechtel-Hook, G.; Wallace, P.; Baron, A.D. Evidence for defects in the trafficking and translocation of GLUT4 glucose transporters in skeletal muscle as a cause of human insulin resistance. J. Clin. Invest., 1998, 101(11), 2377-2386.
[http://dx.doi.org/10.1172/JCI1557] [PMID: 9616209]
[92]
Leguisamo, N.M.; Lehnen, A.M.; Machado, U.F.; Okamoto, M.M.; Markoski, M.M.; Pinto, G.H.; Schaan, B.D. GLUT4 content decreases along with insulin resistance and high levels of inflammatory markers in rats with metabolic syndrome. Cardiovasc. Diabetol., 2012, 11(1), 100.
[http://dx.doi.org/10.1186/1475-2840-11-100] [PMID: 22897936]
[93]
Shu, G.; Zhang, L.; Jiang, S.; Cheng, Z.; Wang, G.; Huang, X.; Yang, X. Isoliensinine induces dephosphorylation of NF-kB p65 subunit at Ser536 via a PP2A-dependent mechanism in hepatocellular carcinoma cells: roles of impairing PP2A/I2PP2A interaction. Oncotarget, 2016, 7(26), 40285-40296.
[http://dx.doi.org/10.18632/oncotarget.9603] [PMID: 27244888]
[94]
Li, W.; Qiu, Y.; Hao, J.; Zhao, C.; Deng, X.; Shu, G. Dauricine upregulates the chemosensitivity of hepatocellular carcinoma cells: Role of repressing glycolysis via miR-199a:HK2/PKM2 modulation. Food Chem. Toxicol., 2018, 121, 156-165.
[http://dx.doi.org/10.1016/j.fct.2018.08.030] [PMID: 30171973]
[95]
Manogaran, P.; Beeraka, N.M.; Huang, C-Y.; Padma, V.V. Neferine and isoliensinine from Nelumbo nucifera induced reactive oxygen species (ROS)-mediated apoptosis in colorectal cancer HCT-15 cells. Afr. J. Pharm. Pharmacol., 2019, 13, 90-99.
[http://dx.doi.org/10.5897/AJPP2019.5036]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 32
Year: 2019
Published on: 08 January, 2020
Page: [2940 - 2957]
Pages: 18
DOI: 10.2174/1568026619666191116160908
Price: $65

Article Metrics

PDF: 24
HTML: 6



Related Article(s)

Most Downloaded Article(s)