Targeting Strategies for Glucose Metabolic Pathways and T Cells in Colorectal Cancer

Author(s): Gang Wang, Jun-Jie Wang, Rui Guan, Yan Sun, Feng Shi, Jing Gao*, Xing-Li Fu*.

Journal Name: Current Cancer Drug Targets

Volume 19 , Issue 7 , 2019

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Colorectal cancer is a heterogeneous group of diseases that result from the accumulation of different sets of genomic alterations, together with epigenomic alterations, and it is influenced by tumor–host interactions, leading to tumor cell growth and glycolytic imbalances. This review summarizes recent findings that involve multiple signaling molecules and downstream genes in the dysregulated glycolytic pathway. This paper further discusses the role of the dysregulated glycolytic pathway in the tumor initiation, progression and the concomitant systemic immunosuppression commonly observed in colorectal cancer patients. Moreover, the relationship between colorectal cancer cells and T cells, especially CD8+ T cells, is discussed, while different aspects of metabolic pathway regulation in cancer cell proliferation are comprehensively defined. Furthermore, this study elaborates on metabolism in colorectal cancer, specifically key metabolic modulators together with regulators, glycolytic enzymes, and glucose deprivation induced by tumor cells and how they inhibit T-cell glycolysis and immunogenic functions. Moreover, metabolic pathways that are integral to T cell function, differentiation, and activation are described. Selective metabolic inhibitors or immunemodulation agents targeting these pathways may be clinically useful to increase effector T cell responses for colorectal cancer treatment. However, there is a need to identify specific antigens using a cancer patient-personalized approach and combination strategies with other therapeutic agents to effectively target tumor metabolic pathways.

Keywords: Colorectal cancers, glucose metabolism, T cells, immune microenvironment, therapy, genomic alterations.

[1]
Song, L.L.; Li, Y.M. Current noninvasive tests for colorectal cancer screening: An overview of colorectal cancer screening tests. World J. Gastrointest. Oncol., 2016, 8(11), 793-800.
[2]
Siegel, R.; Naishadham, D.; Jemal, A. Cancer statistics, 2013. CA Cancer J. Clin., 2013, 63(1), 11-30.
[3]
Fearon, E.R.; Vogelstein, B. A genetic model for colorectal tumorigenesis. Cell, 1990, 61(5), 759-767.
[4]
Cunningham, D.; Atkin, W.; Lenz, H.J.; Lynch, H.T.; Minsky, B.; Nordlinger, B.; Starling, N. Colorectal cancer. Lancet, 2010, 375(9719), 1030-1047.
[5]
Sameer, A.S. Colorectal cancer: molecular mutations and polymorphisms. Front. Oncol., 2013, 3, 114.
[6]
Jiménez, B.; Mirnezami, R.; Kinross, J.; Cloarec, O.; Keun, H.C.; Holmes, E.; Goldin, R.D.; Ziprin, P.; Darzi, A.; Nicholson, J.K. 1H HR-MAS NMR spectroscopy of tumor-induced local metabolic “field-effects” enables colorectal cancer staging and prognostication. J. Proteome Res., 2013, 12(2), 959-968.
[7]
Williams, M.D.; Zhang, X.; Park, J.J.; Siems, W.F.; Gang, D.R.; Resar, L.M.; Reeves, R.; Hill, H.H., Jr Characterizing metabolic changes in human colorectal cancer. Anal. Bioanal. Chem., 2015, 407(16), 4581-4595.
[8]
Graziano, F.; Ruzzo, A.; Giacomini, E.; Ricciardi, T.; Aprile, G.; Loupakis, F.; Lorenzini, P.; Ongaro, E.; Zoratto, F.; Catalano, V.; Sarti, D.; Rulli, E.; Cremolini, C.; De Nictolis, M.; De Maglio, G.; Falcone, A.; Fiorentini, G.; Magnani, M. Glycolysis gene expression analysis and selective metabolic advantage in the clinical progression of colorectal cancer. Pharmacogenomics J., 2017, 17(3), 258.
[9]
Yeh, C.S.; Wang, J.Y.; Chung, F.Y.; Lee, S.C.; Huang, M.Y.; Kuo, C.W.; Yang, M.J.; Lin, S.R. Significance of the glycolytic pathway and glycolysis related-genes in tumorigenesis of human colorectal cancers. Oncol. Rep., 2008, 19(1), 81-91.
[10]
Bi, X.; Lin, Q.; Foo, T.W.; Joshi, S.; You, T.; Shen, H.M.; Ong, C.N.; Cheah, P.Y.; Eu, K.W.; Hew, C.L. Proteomic analysis of colorectal cancer reveals alterations in metabolic pathways: mechanism of tumorigenesis. Mol. Cell. Proteomics, 2006, 5(6), 1119-1130.
[11]
Brown, D.G.; Rao, S.; Weir, T.L.; O’Malia, J.; Bazan, M.; Brown, R.J.; Ryan, E.P. Metabolomics and metabolic pathway networks from human colorectal cancers, adjacent mucosa, and stool. Cancer Metab., 2016, 4, 11.
[12]
Nam, S.O.; Yotsumoto, F.; Miyata, K.; Fukagawa, S.; Yamada, H.; Kuroki, M.; Miyamoto, S. Warburg effect regulated by amphiregulin in the development of colorectal cancer. Cancer Med., 2015, 4(4), 575-587.
[13]
Wang, G.; Fu, X.L.; Wang, J.J.; Guan, R.; Tang, X.J. Novel strategies to discover effective drug targets in metabolic and immune therapy for glioblastoma. Curr. Cancer Drug Targets, 2016. [Epub ahead of print].
[14]
Ottensmeier, C.H.; Perry, K.L.; Harden, E.L.; Stasakova, J.; Jenei, V.; Fleming, J.; Wood, O.; Woo, J.; Woelk, C.H.; Thomas, G.J.; Thirdborough, S.M. Upregulated Glucose Metabolism Correlates Inversely with CD8+ T-cell Infiltration and Survival in Squamous Cell Carcinoma. Cancer Res., 2016, 76(14), 4136-4148.
[15]
Eleftheriadis, T.; Pissas, G.; Antoniadi, G.; Liakopoulos, V.; Stefanidis, I. Malate dehydrogenase-2 inhibitor LW6 promotes metabolic adaptations and reduces proliferation and apoptosis in activated human T-cells. Exp. Ther. Med., 2015, 10(5), 1959-1966.
[16]
McIntyre, A.; Harris, A.L. Metabolic and hypoxic adaptation to anti-angiogenic therapy: a target for induced essentiality. EMBO Mol. Med., 2015, 7(4), 368-379.
[17]
Quintieri, L.; Selmy, M.; Indraccolo, S. Metabolic effects of antiangiogenic drugs in tumors: therapeutic implications. Biochem. Pharmacol., 2014, 89(2), 162-170.
[18]
Stacker, S.A.; Achen, M.G. The VEGF signaling pathway in cancer: the road ahead. Chin. J. Cancer, 2013, 32(6), 297-302.
[19]
Jia, Y.; Guo, M. Epigenetic changes in colorectal cancer. Chin. J. Cancer, 2013, 32(1), 21-30.
[20]
Harris, A.L. Hypoxia--a key regulatory factor in tumour growth. Nat. Rev. Cancer, 2002, 2(1), 38-47.
[21]
Chen, C.; Pore, N.; Behrooz, A.; Ismail-Beigi, F.; Maity, A. Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J. Biol. Chem., 2001, 276(12), 9519-9525.
[22]
Mazurek, S.; Boschek, C.B.; Eigenbrodt, E. The role of phosphometabolites in cell proliferation, energy metabolism, and tumor therapy. J. Bioenerg. Biomembr., 1997, 29(4), 315-330.
[23]
Hu, J.; Yan, W.Y.; Xie, L.; Cheng, L.; Yang, M.; Li, L.; Shi, J.; Liu, B.R.; Qian, X.P. Coexistence of MSI with KRAS mutation is associated with worse prognosis in colorectal cancer. Medicine (Baltimore), 2016, 95(50), e5649.
[24]
Iwamoto, M.; Kawada, K.; Nakamoto, Y.; Itatani, Y.; Inamoto, S.; Toda, K.; Kimura, H.; Sasazuki, T.; Shirasawa, S.; Okuyama, H.; Inoue, M.; Hasegawa, S.; Togashi, K.; Sakai, Y. Regulation of 18F-FDG accumulation in colorectal cancer cells with mutated KRAS. J. Nucl. Med., 2014, 55(12), 2038-2044.
[25]
Yun, J.; Rago, C.; Cheong, I.; Pagliarini, R.; Angenendt, P.; Rajagopalan, H.; Schmidt, K.; Willson, J.K.; Markowitz, S.; Zhou, S.; Diaz, L.A., Jr; Velculescu, V.E.; Lengauer, C.; Kinzler, K.W.; Vogelstein, B.; Papadopoulos, N. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science, 2009, 325(5947), 1555-1559.
[26]
Jadvar, H.; Alavi, A.; Gambhir, S.S. 18F-FDG uptake in lung, breast, and colon cancers: molecular biology correlates and disease characterization. J. Nucl. Med., 2009, 50(11), 1820-1827.
[27]
Maddalena, F.; Lettini, G.; Gallicchio, R.; Sisinni, L.; Simeon, V.; Nardelli, A.; Venetucci, A.A.; Storto, G.; Landriscina, M. Evaluation of Glucose Uptake in Normal and Cancer Cell Lines by Positron Emission Tomography. Mol. Imaging, 2015, 14, 490-498.
[28]
Levine, A.J.; Puzio-Kuter, A.M. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science, 2010, 330(6009), 1340-1344.
[29]
Semenza, G.L. HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations. J. Clin. Invest., 2013, 123(9), 3664-3671.
[30]
Lee-Kong, S.A.; Ruby, J.A.; Chessin, D.B.; Pucciarelli, S.; Shia, J.; Riedel, E.R.; Nitti, D.; Guillem, J.G. Hypoxia-related proteins in patients with rectal cancer undergoing neoadjuvant combined modality therapy. Dis. Colon Rectum, 2012, 55(9), 990-995.
[31]
Zeng, M.; Kikuchi, H.; Pino, M.S.; Chung, D.C. Hypoxia activates the K-ras proto-oncogene to stimulate angiogenesis and inhibit apoptosis in colon cancer cells. PLoS One, 2010, 5(6), e10966.
[32]
Kikuchi, H.; Pino, M.S.; Zeng, M.; Shirasawa, S.; Chung, D.C. Oncogenic KRAS and BRAF differentially regulate hypoxia-inducible factor-1alpha and -2alpha in colon cancer. Cancer Res., 2009, 69(21), 8499-8506.
[33]
Wieman, H.L.; Wofford, J.A.; Rathmell, J.C. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol. Biol. Cell, 2007, 18(4), 1437-1446.
[34]
Toda, K.; Kawada, K.; Iwamoto, M.; Inamoto, S.; Sasazuki, T.; Shirasawa, S.; Hasegawa, S.; Sakai, Y. Metabolic Alterations Caused by KRAS Mutations in Colorectal Cancer Contribute to Cell Adaptation to Glutamine Depletion by Upregulation of Asparagine Synthetase. Neoplasia, 2016, 18(11), 654-665.
[35]
Iwamoto, M.; Kawada, K.; Nakamoto, Y.; Itatani, Y.; Inamoto, S.; Toda, K.; Kimura, H.; Sasazuki, T.; Shirasawa, S.; Okuyama, H.; Inoue, M.; Hasegawa, S.; Togashi, K.; Sakai, Y. Regulation of 18F-FDG accumulation in colorectal cancer cells with mutated KRAS. J. Nucl. Med., 2014, 55(12), 2038-2044.
[36]
Yun, J.; Mullarky, E.; Lu, C.; Bosch, K.N.; Kavalier, A.; Rivera, K.; Roper, J.; Chio, I.I.; Giannopoulou, E.G.; Rago, C.; Muley, A.; Asara, J.M.; Paik, J.; Elemento, O.; Chen, Z.; Pappin, D.J.; Dow, L.E.; Papadopoulos, N.; Gross, S.S.; Cantley, L.C. Vitamin C selectively kills KRAS and BRAF mutant colorectal cancer cells by targeting GAPDH. Science, 2015, 350(6266), 1391-1396.
[37]
Wang, H.J.; Hsieh, Y.J.; Cheng, W.C.; Lin, C.P.; Lin, Y.S.; Yang, S.F.; Chen, C.C.; Izumiya, Y.; Yu, J.S.; Kung, H.J.; Wang, W.C. JMJD5 regulates PKM2 nuclear translocation and reprograms HIF-1α-mediated glucose metabolism. Proc. Natl. Acad. Sci. USA, 2014, 111(1), 279-284.
[38]
Koss, K.; Maxton, D.; Jankowski, J.A. Faecal dimeric M2 pyruvate kinase in colorectal cancer and polyps correlates with tumour staging and surgical intervention. Colorectal Dis., 2008, 10(3), 244-248.
[39]
Huang, J.X.; Zhou, Y.; Wang, C.H.; Yuan, W.W.; Zhang, Z.D.; Zhang, X.F. Tumor M2-pyruvate kinase in stool as a biomarker for diagnosis of colorectal cancer: A meta-analysis. J. Cancer Res. Ther., 2014, 10(Suppl.), C225-C228.
[40]
Zhang, B.; Chen, J.Y.; Chen, D.D.; Wang, G.B.; Shen, P. Tumor type M2 pyruvate kinase expression in gastric cancer, colorectal cancer and controls. World J. Gastroenterol., 2004, 10(11), 1643-1646.
[41]
Demır, A.S.; Erdenen, F.; Müderrısoğlu, C.; Toros, A.B.; Bektaş, H.; Gelışgen, R.; Tabak, Ö.; Altunoğlu, E.; Uzun, H.; Erdem Huq, G.E.; Aral, H. Diagnostic and prognostic value of tumor M2-pyruvate kinase levels in patients with colorectal canhcer. Turk. J. Gastroenterol., 2013, 24(1), 36-42.
[42]
Wang, J.; Wang, H.; Liu, A.; Fang, C.; Hao, J.; Wang, Z. Lactate dehydrogenase A negatively regulated by miRNAs promotes aerobic glycolysis and is increased in colorectal cancer. Oncotarget, 2015, 6(23), 19456-19468.
[43]
Vander Heiden, M.G.; Cantley, L.C.; Thompson, C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science, 2009, 324(5930), 1029-1033.
[44]
Cantor, J.R.; Sabatini, D.M. Cancer cell metabolism: one hallmark, many faces. Cancer Discov., 2012, 2(10), 881-898.
[45]
Zhao, D.; Zou, S.W.; Liu, Y.; Zhou, X.; Mo, Y.; Wang, P.; Xu, Y.H.; Dong, B.; Xiong, Y.; Lei, Q.Y.; Guan, K.L. Lysine-5 acetylation negatively regulates lactate dehydrogenase A and is decreased in pancreatic cancer. Cancer Cell, 2013, 23(4), 464-476.
[46]
Bui, T.; Thompson, C.B. Cancer’s sweet tooth. Cancer Cell, 2006, 9(6), 419-420.
[47]
Loupakis, F.; Yang, D.; Yau, L.; Feng, S.; Cremolini, C.; Zhang, W.; Maus, M.K.; Antoniotti, C.; Langer, C.; Scherer, S.J.; Müller, T.; Hurwitz, H.I.; Saltz, L.; Falcone, A.; Lenz, H.J. Primary tumor location as a prognostic factor in metastatic colorectal cancer. J. Natl. Cancer Inst., 2015, 107(3), dju427.
[48]
Herling, A.; König, M.; Bulik, S.; Holzhütter, H.G. Enzymatic features of the glucose metabolism in tumor cells. FEBS J., 2011, 278(14), 2436-2459.
[49]
Mathupala, S.P.; Ko, Y.H.; Pedersen, P.L. Hexokinase-2 bound to mitochondria: cancer’s stygian link to the “Warburg Effect” and a pivotal target for effective therapy. Semin. Cancer Biol., 2009, 19(1), 17-24.
[50]
Draoui, N.; Schicke, O.; Seront, E.; Bouzin, C.; Sonveaux, P.; Riant, O.; Feron, O. Antitumor activity of 7-aminocarboxycoumarin derivatives, a new class of potent inhibitors of lactate influx but not efflux. Mol. Cancer Ther., 2014, 13(6), 1410-1418.
[51]
Sun, Q.; Chen, X.; Ma, J.; Peng, H.; Wang, F.; Zha, X.; Wang, Y.; Jing, Y.; Yang, H.; Chen, R.; Chang, L.; Zhang, Y.; Goto, J.; Onda, H.; Chen, T.; Wang, M.R.; Lu, Y.; You, H.; Kwiatkowski, D.; Zhang, H. Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth. Proc. Natl. Acad. Sci. USA, 2011, 108(10), 4129-4134.
[52]
Düvel, K.; Yecies, J.L.; Menon, S.; Raman, P.; Lipovsky, A.I.; Souza, A.L.; Triantafellow, E.; Ma, Q.; Gorski, R.; Cleaver, S.; Vander Heiden, M.G.; MacKeigan, J.P.; Finan, P.M.; Clish, C.B.; Murphy, L.O.; Manning, B.D. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol. Cell, 2010, 39(2), 171-183.
[53]
Maiese, K.; Chong, Z.Z.; Shang, Y.C.; Wang, S. mTOR: on target for novel therapeutic strategies in the nervous system. Trends Mol. Med., 2013, 19(1), 51-60.
[54]
Kim, D.D.; Eng, C. The promise of mTOR inhibitors in the treatment of colorectal cancer. Expert Opin. Investig. Drugs, 2012, 21(12), 1775-1788.
[55]
Mitsuishi, Y.; Taguchi, K.; Kawatani, Y.; Shibata, T.; Nukiwa, T.; Aburatani, H.; Yamamoto, M.; Motohashi, H. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell, 2012, 22(1), 66-79.
[56]
Du, W.; Jiang, P.; Mancuso, A.; Stonestrom, A.; Brewer, M.D.; Minn, A.J.; Mak, T.W.; Wu, M.; Yang, X. TAp73 enhances the pentose phosphate pathway and supports cell proliferation. Nat. Cell Biol., 2013, 15(8), 991-1000.
[57]
Zhou, C.F.; Li, X.B.; Sun, H.; Zhang, B.; Han, Y.S.; Jiang, Y.; Zhuang, Q.L.; Fang, J.; Wu, G.H. Pyruvate kinase type M2 is upregulated in colorectal cancer and promotes proliferation and migration of colon cancer cells. IUBMB Life, 2012, 64(9), 775-782.
[58]
Sun, Q.; Chen, X.; Ma, J.; Peng, H.; Wang, F.; Zha, X.; Wang, Y.; Jing, Y.; Yang, H.; Chen, R.; Chang, L.; Zhang, Y.; Goto, J.; Onda, H.; Chen, T.; Wang, M.R.; Lu, Y.; You, H.; Kwiatkowski, D.; Zhang, H. Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth. Proc. Natl. Acad. Sci. USA, 2011, 108(10), 4129-4134.
[59]
Kato, H.; Nakajima, S.; Saito, Y.; Takahashi, S.; Katoh, R.; Kitamura, M. mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1-JNK pathway. Cell Death Differ., 2012, 19(2), 310-320.
[60]
Polak, P.; Hall, M.N. mTOR and the control of whole body metabolism. Curr. Opin. Cell Biol., 2009, 21(2), 209-218.
[61]
Iurlaro, R.; León-Annicchiarico, C.L.; Muñoz-Pinedo, C. Regulation of cancer metabolism by oncogenes and tumor suppressors. Methods Enzymol., 2014, 542, 59-80.
[62]
He, T.L.; Zhang, Y.J.; Jiang, H.; Li, X.H.; Zhu, H.; Zheng, K.L. The c-Myc-LDHA axis positively regulates aerobic glycolysis and promotes tumor progression in pancreatic cancer. Med. Oncol., 2015, 32(7), 187.
[63]
Zalata, K.R.; Elshal, M.F.; Foda, A.A.; Shoma, A. Genetic dissimilarity between primary colorectal carcinomas and their lymph node metastases: ploidy, p53, bcl-2, and c-myc expression--a pilot study. Tumour Biol., 2015, 36(8), 6579-6584.
[64]
Dang, CV; Le, A A; Gao, P MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clinical cancer research: an official journal of the American Association for Cancer Research, 2009, 15, 6479-6483.
[65]
Guertin, D.A.; Sabatini, D.M. Defining the role of mTOR in cancer. Cancer Cell, 2007, 12(1), 9-22.
[66]
Golestan, A. MSc, Mojtahedi Z PhD, Ghalamfarsa G PhD, Hamidinia M MSc, Takhshid MA PhD. The Effects of NDRG2 Overexpression on Cell Proliferation and Invasiveness of SW48 ColorectalCancer Cell Line. Iran. J. Med. Sci., 2015, 40(5), 430-439.
[67]
Lorentzen, A.; Mitchelmore, C. NDRG2 gene copy number is not altered in colorectal carcinoma. World J. Clin. Oncol., 2017, 8(1), 67-74.
[68]
Clevers, H. Wnt/beta-catenin signaling in development and disease. Cell, 2006, 127(3), 469-480.
[69]
Jen, K.Y.; Cheung, V.G. Identification of novel p53 target genes in ionizing radiation response. Cancer Res., 2005, 65(17), 7666-7673.
[70]
Kimata, M.; Matoba, S.; Iwai-Kanai, E.; Nakamura, H.; Hoshino, A.; Nakaoka, M.; Katamura, M.; Okawa, Y.; Mita, Y.; Okigaki, M.; Ikeda, K.; Tatsumi, T.; Matsubara, H. p53 and TIGAR regulate cardiac myocyte energy homeostasis under hypoxic stress. Am. J. Physiol. Heart Circ. Physiol., 2010, 299(6), H1908-H1916.
[71]
Peña-Rico, M.A.; Calvo-Vidal, M.N.; Villalonga-Planells, R.; Martínez-Soler, F.; Giménez-Bonafé, P.; Navarro-Sabaté, À.; Tortosa, A.; Bartrons, R.; Manzano, A. TP53 induced glycolysis and apoptosis regulator (TIGAR) knockdown results in radiosensitization of glioma cells. Radiother. Oncol., 2011, 101(1), 132-139.
[72]
Yin, L.; Kosugi, M.; Kufe, D. Inhibition of the MUC1-C oncoprotein induces multiple myeloma cell death by down-regulating TIGAR expression and depleting NADPH. Blood, 2012, 119(3), 810-816.
[73]
Lui, V.W.; Lau, C.P.; Cheung, C.S.; Ho, K.; Ng, M.H.; Cheng, S.H.; Hong, B.; Tsao, S.W.; Tsang, C.M.; Lei, K.I.; Yamasaki, Y.; Mita, A.; Chan, A.T. An RNA-directed nucleoside anti-metabolite, 1-(3-C-ethynyl-beta-d-ribo-pentofuranosyl)cytosine (ECyd), elicits antitumor effect via TP53-induced Glycolysis and Apoptosis Regulator (TIGAR) downregulation. Biochem. Pharmacol., 2010, 79(12), 1772-1780.
[74]
Wanka, C.; Steinbach, J.P.; Rieger, J. Tp53-induced glycolysis and apoptosis regulator (TIGAR) protects glioma cells from starvation-induced cell death by up-regulating respiration and improving cellular redox homeostasis. J. Biol. Chem., 2012, 287(40), 33436-33446.
[75]
Ye, L.; Zhao, X.; Lu, J.; Qian, G.; Zheng, J.C.; Ge, S. Knockdown of TIGAR by RNA interference induces apoptosis and autophagy in HepG2 hepatocellular carcinoma cells. Biochem. Biophys. Res. Commun., 2013, 437(2), 300-306.
[76]
Cheung, E.C.; Athineos, D.; Lee, P.; Ridgway, R.A.; Lambie, W.; Nixon, C.; Strathdee, D.; Blyth, K.; Sansom, O.J.; Vousden, K.H. TIGAR is required for efficient intestinal regeneration and tumorigenesis. Dev. Cell, 2013, 25(5), 463-477.
[77]
Cooper, H.S.; Murthy, S.N.; Shah, R.S.; Sedergran, D.J. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab. Invest., 1993, 69(2), 238-249.
[78]
Won, K.Y.; Lim, S.J.; Kim, G.Y.; Kim, Y.W.; Han, S.A.; Song, J.Y.; Lee, D.K. Regulatory role of p53 in cancer metabolism via SCO2 and TIGAR in human breast cancer. Hum. Pathol., 2012, 43(2), 221-228.
[79]
Sinha, S.; Ghildiyal, R.; Mehta, V.S.; Sen, E. ATM-NFκB axis-driven TIGAR regulates sensitivity of glioma cells to radiomimetics in the presence of TNFαCell Death Dis., 2013. 4e615
[80]
Kroemer, G.; Pouyssegur, J. Tumor cell metabolism: cancer’s Achilles’ heel. Cancer Cell, 2008, 13(6), 472-482.
[81]
Massari, F.; Ciccarese, C.; Santoni, M.; Iacovelli, R.; Mazzucchelli, R.; Piva, F.; Scarpelli, M.; Berardi, R.; Tortora, G.; Lopez-Beltran, A.; Cheng, L.; Montironi, R. Metabolic phenotype of bladder cancer. Cancer Treat. Rev., 2016, 45, 46-57.
[82]
Vander Heiden, M.G.; Cantley, L.C.; Thompson, C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science, 2009, 324(5930), 1029-1033.
[83]
Landis, J.; Shaw, L.M. Insulin receptor substrate 2-mediated phosphatidylinositol 3-kinase signaling selectively inhibits glycogen synthase kinase 3β to regulate aerobic glycolysis. J. Biol. Chem., 2014, 289(26), 18603-18613.
[84]
Taubes, G. Cancer research. Unraveling the obesity-cancer connection. Science, 2012, 335(6064), 28-30-32.
[85]
Zha, X.; Hu, Z.; Ji, S.; Jin, F.; Jiang, K.; Li, C.; Zhao, P.; Tu, Z.; Chen, X.; Di, L.; Zhou, H.; Zhang, H. NFκB up-regulation of glucose transporter 3 is essential for hyperactive mammalian target of rapamycin-induced aerobic glycolysis and tumor growth. Cancer Lett., 2015, 359(1), 97-106.
[86]
Sandulache, V.C.; Myers, J.N. Altered metabolism in head and neck squamous cell carcinoma: an opportunity for identification of novel biomarkers and drug targets. Head Neck, 2012, 34(2), 282-290.
[87]
Ward, P.S.; Thompson, C.B. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell, 2012, 21(3), 297-308.
[88]
Donohoe, D.R.; Garge, N.; Zhang, X.; Sun, W.; O’Connell, T.M.; Bunger, M.K.; Bultman, S.J. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab., 2011, 13(5), 517-526.
[89]
Kim, J.W.; Zeller, K.I.; Wang, Y.; Jegga, A.G.; Aronow, B.J.; O’Donnell, K.A.; Dang, C.V. Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Mol. Cell. Biol., 2004, 24(13), 5923-5936.
[90]
Ellis, B.C.; Graham, L.D.; Molloy, P.L. CRNDE, a long non-coding RNA responsive to insulin/IGF signaling, regulates genes involved in central metabolism. Biochim. Biophys. Acta, 2014, 1843(2), 372-386.
[91]
Wei, Z.; Cui, L.; Mei, Z.; Liu, M.; Zhang, D. miR-181a mediates metabolic shift in colon cancer cells via the PTEN/AKT pathway. FEBS Lett., 2014, 588(9), 1773-1779.
[92]
Gerweck, L.E.; Seetharaman, K. Cellular pH gradient in tumor versus normal tissue: potential exploitation for the treatment of cancer. Cancer Res., 1996, 56(6), 1194-1198.
[93]
Helmlinger, G.; Yuan, F.; Dellian, M.; Jain, R.K. Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat. Med., 1997, 3(2), 177-182.
[94]
Quail, D.F.; Joyce, J.A. Microenvironmental regulation of tumor progression and metastasis. Nat. Med., 2013, 19(11), 1423-1437.
[95]
Amend, S.R.; Pienta, K.J. Ecology meets cancer biology: the cancer swamp promotes the lethal cancer phenotype. Oncotarget, 2015, 6(12), 9669-9678.
[96]
Seo, Y.; Kinsella, T.J. Essential role of DNA base excision repair on survival in an acidic tumor microenvironment. Cancer Res., 2009, 69(18), 7285-7293.
[97]
Gorrini, C.; Harris, I.S.; Mak, T.W. Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discov., 2013, 12(12), 931-947.
[98]
Harris, I.S.; Treloar, A.E.; Inoue, S.; Sasaki, M.; Gorrini, C.; Lee, K.C.; Yung, K.Y.; Brenner, D.; Knobbe-Thomsen, C.B.; Cox, M.A.; Elia, A.; Berger, T.; Cescon, D.W.; Adeoye, A.; Brüstle, A.; Molyneux, S.D.; Mason, J.M.; Li, W.Y.; Yamamoto, K.; Wakeham, A.; Berman, H.K.; Khokha, R.; Done, S.J.; Kavanagh, T.J.; Lam, C.W.; Mak, T.W. Glutathione and thioredoxin antioxidant pathways synergize to drive cancer initiation and progression. Cancer Cell, 2015, 27(2), 211-222.
[99]
Lamonte, G.; Tang, X.; Chen, J.L.; Wu, J.; Ding, C.K.; Keenan, M.M.; Sangokoya, C.; Kung, H.N.; Ilkayeva, O.; Boros, L.G.; Newgard, C.B.; Chi, J.T. Acidosis induces reprogramming of cellular metabolism to mitigate oxidative stress. Cancer Metab., 2013, 1(1), 23.
[100]
Zhao, M.; Liu, Q.; Gong, Y.; Xu, X.; Zhang, C.; Liu, X.; Zhang, C.; Guo, H.; Zhang, X.; Gong, Y.; Shao, C. GSH-dependent antioxidant defense contributes to the acclimation of colon cancer cells to acidic microenvironment. Cell Cycle, 2016, 15(8), 1125-1133.
[101]
Maulucci, G.; Daniel, B.; Cohen, O.; Avrahami, Y.; Sasson, S. Hormetic and regulatory effects of lipid peroxidation mediators in pancreatic beta cells. Mol. Aspects Med., 2016, 49, 49-77.
[102]
Ladell, K.; Hashimoto, M.; Iglesias, M.C.; Wilmann, P.G.; McLaren, J.E.; Gras, S.; Chikata, T.; Kuse, N.; Fastenackels, S.; Gostick, E.; Bridgeman, J.S.; Venturi, V.; Arkoub, Z.A.; Agut, H.; van Bockel, D.J.; Almeida, J.R.; Douek, D.C.; Meyer, L.; Venet, A.; Takiguchi, M.; Rossjohn, J.; Price, D.A.; Appay, V. A molecular basis for the control of preimmune escape variants by HIV-specific CD8+ T cells. Immunity, 2013, 38(3), 425-436.
[103]
Gubser, P.M.; Bantug, G.R.; Razik, L.; Fischer, M.; Dimeloe, S.; Hoenger, G.; Durovic, B.; Jauch, A.; Hess, C. Rapid effector function of memory CD8+ T cells requires an immediate-early glycolytic switch. Nat. Immunol., 2013, 14(10), 1064-1072.
[104]
Chang, C.H.; Curtis, J.D.; Maggi, L.B., Jr; Faubert, B.; Villarino, A.V.; O’Sullivan, D.; Huang, S.C.; van der Windt, G.J.; Blagih, J.; Qiu, J.; Weber, J.D.; Pearce, E.J.; Jones, R.G.; Pearce, E.L. Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell, 2013, 153(6), 1239-1251.
[105]
Pagès, F.; Berger, A.; Camus, M.; Sanchez-Cabo, F.; Costes, A.; Molidor, R.; Mlecnik, B.; Kirilovsky, A.; Nilsson, M.; Damotte, D.; Meatchi, T.; Bruneval, P.; Cugnenc, P.H.; Trajanoski, Z.; Fridman, W.H.; Galon, J. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med., 2005, 353(25), 2654-2666.
[106]
Kryczek, I.; Banerjee, M.; Cheng, P.; Vatan, L.; Szeliga, W.; Wei, S.; Huang, E.; Finlayson, E.; Simeone, D.; Welling, T.H.; Chang, A.; Coukos, G.; Liu, R.; Zou, W. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood, 2009, 114(6), 1141-1149.
[107]
Powell, D.J., Jr; Dudley, M.E.; Robbins, P.F.; Rosenberg, S.A. Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood, 2005, 105(1), 241-250.
[108]
Wei, S.; Zhao, E.; Kryczek, I.; Zou, W. Th17 cells have stem cell-like features and promote long-term immunity. OncoImmunology, 2012, 1(4), 516-519.
[109]
Chang, C.H.; Qiu, J.; O’Sullivan, D.; Buck, M.D.; Noguchi, T.; Curtis, J.D.; Chen, Q.; Gindin, M.; Gubin, M.M.; van der Windt, G.J.; Tonc, E.; Schreiber, R.D.; Pearce, E.J.; Pearce, E.L. Metabolic Competition in the Tumor Microenvironment Is a Driver of Cancer Progression. Cell, 2015, 162(6), 1229-1241.
[110]
Ho, P.C.; Bihuniak, J.D.; Macintyre, A.N.; Staron, M.; Liu, X.; Amezquita, R.; Tsui, Y.C.; Cui, G.; Micevic, G.; Perales, J.C.; Kleinstein, S.H.; Abel, E.D.; Insogna, K.L.; Feske, S.; Locasale, J.W.; Bosenberg, M.W.; Rathmell, J.C.; Kaech, S.M. Phosphoenolpyruvate Is a Metabolic Checkpoint of Anti-tumor T Cell Responses. Cell, 2015, 162(6), 1217-1228.
[111]
Pollizzi, K.N.; Sun, I.H.; Patel, C.H.; Lo, Y.C.; Oh, M.H.; Waickman, A.T.; Tam, A.J.; Blosser, R.L.; Wen, J.; Delgoffe, G.M.; Powell, J.D. Asymmetric inheritance of mTORC1 kinase activity during division dictates CD8(+) T cell differentiation. Nat. Immunol., 2016, 17(6), 704-711.
[112]
Fox, C.J.; Hammerman, P.S.; Thompson, C.B. Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol., 2005, 5(11), 844-852.
[113]
Patsoukis, N.; Bardhan, K.; Chatterjee, P.; Sari, D.; Liu, B.; Bell, L.N.; Karoly, E.D.; Freeman, G.J.; Petkova, V.; Seth, P.; Li, L.; Boussiotis, V.A. PD-1 alters T-cell metabolic reprogramming by inhibiting glycolysis and promoting lipolysis and fatty acid oxidation. Nat. Commun., 2015, 6, 6692.
[114]
Gubser, P.M.; Bantug, G.R.; Razik, L.; Fischer, M.; Dimeloe, S.; Hoenger, G.; Durovic, B.; Jauch, A.; Hess, C. Rapid effector function of memory CD8+ T cells requires an immediate-early glycolytic switch. Nat. Immunol., 2013, 14(10), 1064-1072.
[115]
Greiner, E.F.; Guppy, M.; Brand, K. Glucose is essential for proliferation and the glycolytic enzyme induction that provokes a transition to glycolytic energy production. J. Biol. Chem., 1994, 269(50), 31484-31490.
[116]
Macintyre, A.N.; Gerriets, V.A.; Nichols, A.G.; Michalek, R.D.; Rudolph, M.C.; Deoliveira, D.; Anderson, S.M.; Abel, E.D.; Chen, B.J.; Hale, L.P.; Rathmell, J.C. The glucose transporter Glut1 is selectively essential for CD4 T cell activation and effector function. Cell Metab., 2014, 20(1), 61-72.
[117]
van der Windt, G.J.; Everts, B.; Chang, C.H.; Curtis, J.D.; Freitas, T.C.; Amiel, E.; Pearce, E.J.; Pearce, E.L. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity, 2012, 36(1), 68-78.
[118]
van der Windt, G.J.; O’Sullivan, D.; Everts, B.; Huang, S.C.; Buck, M.D.; Curtis, J.D.; Chang, C.H.; Smith, A.M.; Ai, T.; Faubert, B.; Jones, R.G.; Pearce, E.J.; Pearce, E.L. CD8 memory T cells have a bioenergetic advantage that underlies their rapid recall ability. Proc. Natl. Acad. Sci. USA, 2013, 110(35), 14336-14341.
[119]
Ganapathy-Kanniappan, S.; Geschwind, J.F. Tumor glycolysis as a target for cancer therapy: progress and prospects. Mol. Cancer, 2013, 12, 152.
[120]
Jang, M.; Kim, S.S.; Lee, J. Cancer cell metabolism: implications for therapeutic targets.Exp. Mol. Med., 2013. 45e45
[121]
Zhou, M.; Zhao, Y.; Ding, Y.; Liu, H.; Liu, Z.; Fodstad, O.; Riker, A.I.; Kamarajugadda, S.; Lu, J.; Owen, L.B.; Ledoux, S.P.; Tan, M. Warburg effect in chemosensitivity: targeting lactate dehydrogenase-A re-sensitizes taxol-resistant cancer cells to taxol. Mol. Cancer, 2010, 9, 33.
[122]
Tong, J.; Xie, G.; He, J.; Li, J.; Pan, F.; Liang, H. Synergistic antitumor effect of dichloroacetate in combination with 5-fluorouracil in colorectal cancer. J. Biomed. Biotechnol., 2011, •••, 2011740564.
[123]
Ho, N.; Coomber, B.L. Pyruvate dehydrogenase kinase expression and metabolic changes following dichloroacetate exposure in anoxic human colorectal cancer cells. Exp. Cell Res., 2015, 331(1), 73-81.
[124]
Bandukwala, H.S.; Gagnon, J.; Togher, S.; Greenbaum, J.A.; Lamperti, E.D.; Parr, N.J.; Molesworth, A.M.; Smithers, N.; Lee, K.; Witherington, J.; Tough, D.F.; Prinjha, R.K.; Peters, B.; Rao, A. Selective inhibition of CD4+ T-cell cytokine production and autoimmunity by BET protein and c-Myc inhibitors. Proc. Natl. Acad. Sci. USA, 2012, 109(36), 14532-14537.
[125]
Powell, J.D.; Zheng, Y. Dissecting the mechanism of T-cell anergy with immunophilin ligands. Curr. Opin. Investig. Drugs, 2006, 7(11), 1002-1007.
[126]
Touzot, M.; Soulillou, J.P.; Dantal, J. Mechanistic target of rapamycin inhibitors in solid organ transplantation: from benchside to clinical use. Curr. Opin. Organ Transplant., 2012, 17(6), 626-633.
[127]
Waickman, A.T.; Powell, J.D. mTOR, metabolism, and the regulation of T-cell differentiation and function. Immunol. Rev., 2012, 249(1), 43-58.
[128]
Jin, M.L.; Park, S.Y.; Kim, Y.H.; Park, G.; Lee, S.J. Halofuginone induces the apoptosis of breast cancer cells and inhibits migration via downregulation of matrix metalloproteinase-9. Int. J. Oncol., 2014, 44(1), 309-318.
[129]
de Figueiredo-Pontes, L.L.; Assis, P.A.; Santana-Lemos, B.A.; Jácomo, R.H.; Lima, A.S.; Garcia, A.B.; Thomé, C.H.; Araújo, A.G.; Panepucci, R.A.; Zago, M.A.; Nagler, A.; Falcão, R.P.; Rego, E.M. Halofuginone has anti-proliferative effects in acute promyelocytic leukemia by modulating the transforming growth factor beta signaling pathway. PLoS One, 2011, 6(10), e26713.
[130]
Ellis, B.C.; Graham, L.D.; Molloy, P.L. CRNDE, a long non-coding RNA responsive to insulin/IGF signaling, regulates genes involved in central metabolism. Biochim. Biophys. Acta, 2014, 1843(2), 372-386.
[131]
Wei, Z.; Cui, L.; Mei, Z.; Liu, M.; Zhang, D. miR-181a mediates metabolic shift in colon cancer cells via the PTEN/AKT pathway. FEBS Lett., 2014, 588(9), 1773-1779.
[132]
Chen, G.Q.; Tang, C.F.; Shi, X.K.; Lin, C.Y.; Fatima, S.; Pan, X.H.; Yang, D.J.; Zhang, G.; Lu, A.P.; Lin, S.H.; Bian, Z.X. Halofuginone inhibits colorectal cancer growth through suppression of Akt/mTORC1 signaling and glucose metabolism. Oncotarget, 2015, 6(27), 24148-24162.
[133]
Chen, G.Q.; Gong, R.H.; Yang, D.J.; Zhang, G.; Lu, A.P.; Yan, S.C.; Lin, S.H.; Bian, Z.X. Halofuginone dually regulates autophagic flux through nutrient-sensing pathways in colorectal cancer. Cell Death Dis., 2017, 8(5), e2789.
[134]
Thoreen, C.C.; Kang, S.A.; Chang, J.W.; Liu, Q.; Zhang, J.; Gao, Y.; Reichling, L.J.; Sim, T.; Sabatini, D.M.; Gray, N.S. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem., 2009, 284(12), 8023-8032.
[135]
Wang, L.; Xiong, H.; Wu, F.; Zhang, Y.; Wang, J.; Zhao, L.; Guo, X.; Chang, L.J.; Zhang, Y.; You, M.J.; Koochekpour, S.; Saleem, M.; Huang, H.; Lu, J.; Deng, Y. Hexokinase 2-mediated Warburg effect is required for PTEN- and p53-deficiency-driven prostate cancer growth. Cell Reports, 2014, 8(5), 1461-1474.
[136]
Cao, Y.; Rathmell, J.C.; Macintyre, A.N. Metabolic reprogramming towards aerobic glycolysis correlates with greater proliferative ability and resistance to metabolic inhibition in CD8 versus CD4 T cells. PLoS One, 2014, 9(8), e104104.
[137]
Roberts, D.J.; Miyamoto, S. Hexokinase II integrates energy metabolism and cellular protection: Akting on mitochondria and TORCing to autophagy. Cell Death Differ., 2015, 22(2), 248-257.
[138]
Arafa, S.A.; Abdelazeem, A.H.; Arab, H.H.; Omar, H.A. OSU-CG5, a novel energy restriction mimetic agent, targets human colorectal cancer cells in vitro. Acta Pharmacol. Sin., 2014, 35(3), 394-400.
[139]
Zwicker, F.; Kirsner, A.; Peschke, P.; Roeder, F.; Debus, J.; Huber, P.E.; Weber, K.J. Dichloroacetate induces tumor-specific radiosensitivity in vitro but attenuates radiation-induced tumor growth delay in vivo. Strahlenther. Onkol., 2013, 189(8), 684-692.
[140]
Fath, M.A.; Diers, A.R.; Aykin-Burns, N.; Simons, A.L.; Hua, L.; Spitz, D.R. Mitochondrial electron transport chain blockers enhance 2-deoxy-D-glucose induced oxidative stress and cell killing in human colon carcinoma cells. Cancer Biol. Ther., 2009, 8(13), 1228-1236.
[141]
Ying, Q.; Ansong, E.; Diamond, A.M.; Lu, Z.; Yang, W.; Bie, X. Quantitative proteomic analysis reveals that anti-cancer effects of selenium-binding protein 1 in vivo are associated with metabolic pathways. PLoS One, 2015, 10(5), e0126285.
[142]
Gattinoni, L.; Zhong, X.S.; Palmer, D.C.; Ji, Y.; Hinrichs, C.S.; Yu, Z.; Wrzesinski, C.; Boni, A.; Cassard, L.; Garvin, L.M.; Paulos, C.M.; Muranski, P.; Restifo, N.P. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat. Med., 2009, 15(7), 808-813.
[143]
Sukumar, M.; Liu, J.; Ji, Y.; Subramanian, M.; Crompton, J.G.; Yu, Z.; Roychoudhuri, R.; Palmer, D.C.; Muranski, P.; Karoly, E.D.; Mohney, R.P.; Klebanoff, C.A.; Lal, A.; Finkel, T.; Restifo, N.P.; Gattinoni, L. Inhibiting glycolytic metabolism enhances CD8+ T cell memory and antitumor function. J. Clin. Invest., 2013, 123(10), 4479-4488.
[144]
Topalian, S.L.; Drake, C.G.; Pardoll, D.M. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell, 2015, 27(4), 450-461.
[145]
Pardoll, D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer, 2012, 12(4), 252-264.
[146]
Patsoukis, N.; Bardhan, K.; Chatterjee, P.; Sari, D.; Liu, B.; Bell, L.N.; Karoly, E.D.; Freeman, G.J.; Petkova, V.; Seth, P.; Li, L.; Boussiotis, V.A. PD-1 alters T-cell metabolic reprogramming by inhibiting glycolysis and promoting lipolysis and fatty acid oxidation. Nat. Commun., 2015, 6, 6692.
[147]
Barañano, K.W.; Hartman, A.L. The ketogenic diet: uses in epilepsy and other neurologic illnesses. Curr. Treat. Options Neurol., 2008, 10(6), 410-419.
[148]
Turati, F.; Edefonti, V.; Bravi, F.; Ferraroni, M.; Talamini, R.; Giacosa, A.; Montella, M.; Parpinel, M.; La Vecchia, C.; Decarli, A. Adherence to the European food safety authority’s dietary recommendations and colorectal cancer risk. Eur. J. Clin. Nutr., 2012, 66(4), 517-522.
[149]
Wiktorowska-Owczarek, A.; Berezińska, M.; Nowak, J.Z. PUFAs: structures, metabolism and functions. Adv. Clin. Exp. Med., 2015, 24(6), 931-941.
[150]
Ferreri, C.; Chatgilialoglu, C. Membrane Lipidomics for Personalized Health; Wiley & Sons Ltd.: Chichester, 2015.
[151]
Das, U.N. Essential Fatty acids - a review. Curr. Pharm. Biotechnol., 2006, 7(6), 467-482.
[152]
Wang, S.; Xie, J.; Li, H.; Yang, K. Differences of polyunsaturated fatty acid in patients with colorectal cancer and healthy people. J. Cancer Res. Ther., 2015, 11(2), 459-463.
[153]
Yang, K.; Li, H.; Dong, J.; Dong, Y.; Wang, C.Z. Expression profile of polyunsaturated fatty acids in colorectal cancer. World J. Gastroenterol., 2015, 21(8), 2405-2412.
[154]
Lee, J.Y.; Zhao, L.; Hwang, D.H. Modulation of pattern recognition receptor-mediated inflammation and risk of chronic diseases by dietary fatty acids. Nutr. Rev., 2010, 68(1), 38-61.
[155]
Eleftheriadis, T.; Pissas, G.; Antoniadi, G.; Liakopoulos, V.; Stefanidis, I. Malate dehydrogenase-2 inhibitor LW6 promotes metabolic adaptations and reduces proliferation and apoptosis in activated human T-cells. Exp. Ther. Med., 2015, 10(5), 1959-1966.
[156]
Hirata, F.; Nomiyama, S.; Hayaishi, O. Indoleamine 2,3-dioxygenase. Note I. Catalytic and molecular properties. Acta Vitaminol. Enzymol., 1975, 29(1-6), 288-290.
[157]
Fallarino, F.; Grohmann, U.; Vacca, C.; Orabona, C.; Spreca, A.; Fioretti, M.C.; Puccetti, P. T cell apoptosis by kynurenines. Adv. Exp. Med. Biol., 2003, 527, 183-190.
[158]
Munn, D.H.; Shafizadeh, E.; Attwood, J.T.; Bondarev, I.; Pashine, A.; Mellor, A.L. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med., 1999, 189(9), 1363-1372.
[159]
Uyttenhove, C.; Pilotte, L.; Théate, I.; Stroobant, V.; Colau, D.; Parmentier, N.; Boon, T.; Van den Eynde, B.J. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med., 2003, 9(10), 1269-1274.
[160]
Ferdinande, L.; Decaestecker, C.; Verset, L.; Mathieu, A.; Moles Lopez, X.; Negulescu, A.M.; Van Maerken, T.; Salmon, I.; Cuvelier, C.A.; Demetter, P. Clinicopathological significance of indoleamine 2,3-dioxygenase 1 expression in colorectal cancer. Br. J. Cancer, 2012, 106(1), 141-147.
[161]
Ghanipour, A.; Jirström, K.; Pontén, F.; Glimelius, B.; Påhlman, L.; Birgisson, H. The prognostic significance of tryptophanyl-tRNA synthetase in colorectal cancer. Cancer Epidemiol. Biomarkers Prev., 2009, 18(11), 2949-2956.
[162]
Uyttenhove, C.; Pilotte, L.; Théate, I.; Stroobant, V.; Colau, D.; Parmentier, N.; Boon, T.; Van den Eynde, B.J. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med., 2003, 9(10), 1269-1274.
[163]
Friberg, M.; Jennings, R.; Alsarraj, M.; Dessureault, S.; Cantor, A.; Extermann, M.; Mellor, A.L.; Munn, D.H.; Antonia, S.J. Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection. Int. J. Cancer, 2002, 101(2), 151-155.
[164]
Hwu, P.; Du, M.X.; Lapointe, R.; Do, M.; Taylor, M.W.; Young, H.A. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J. Immunol., 2000, 164(7), 3596-3599.
[165]
Jürgens, B.; Hainz, U.; Fuchs, D.; Felzmann, T.; Heitger, A. Interferon-gamma-triggered indoleamine 2,3-dioxygenase competence in human monocyte-derived dendritic cells induces regulatory activity in allogeneic T cells. Blood, 2009, 114(15), 3235-3243.
[166]
Sioud, M.; Saebøe-Larssen, S.; Hetland, T.E.; Kaern, J.; Mobergslien, A.; Kvalheim, G. Silencing of indoleamine 2,3-dioxygenase enhances dendritic cell immunogenicity and antitumour immunity in cancer patients. Int. J. Oncol., 2013, 43(1), 280-288.
[167]
Sørensen, R.B.; Hadrup, S.R.; Svane, I.M.; Hjortsø, M.C.; Thor Straten, P.; Andersen, M.H. Indoleamine 2,3-dioxygenase specific, cytotoxic T cells as immune regulators. Blood, 2011, 117(7), 2200-2210.
[168]
Balachandran, V.P.; Cavnar, M.J.; Zeng, S.; Bamboat, Z.M.; Ocuin, L.M.; Obaid, H.; Sorenson, E.C.; Popow, R.; Ariyan, C.; Rossi, F.; Besmer, P.; Guo, T.; Antonescu, C.R.; Taguchi, T.; Yuan, J.; Wolchok, J.D.; Allison, J.P.; DeMatteo, R.P. Imatinib potentiates antitumor T cell responses in gastrointestinal stromal tumor through the inhibition of Ido. Nat. Med., 2011, 17(9), 1094-1100.
[169]
Nayak, A.; Hao, Z.; Sadek, R. A Phase I study of NLG919 for adult patients with recurrent advanced solid tumors. J. Immunother. Cancer, 2014, 2(Suppl. 3), 250.
[170]
Deiab, S.; Mazzio, E.; Eyunni, S.; McTier, O.; Mateeva, N.; Elshami, F.; Soliman, K.F. 1,2,3,4,6-Penta-O-galloylglucose within Galla Chinensis Inhibits Human LDH-A and Attenuates Cell Proliferation in MDA-MB-231 Breast Cancer Cells. Evid. Based Complement. Alternat. Med., 2015, 2015, 276946.
[171]
Estrella, V.; Chen, T.; Lloyd, M.; Wojtkowiak, J.; Cornnell, H.H.; Ibrahim-Hashim, A.; Bailey, K.; Balagurunathan, Y.; Rothberg, J.M.; Sloane, B.F.; Johnson, J.; Gatenby, R.A.; Gillies, R.J. Acidity generated by the tumor microenvironment drives local invasion. Cancer Res., 2013, 73(5), 1524-1535.
[172]
Kareva, I.; Hahnfeldt, P. The emerging “hallmarks” of metabolic reprogramming and immune evasion: distinct or linked? Cancer Res., 2013, 73(9), 2737-2742.
[173]
Da Silva, S.L. Chaar, Jda.S.; Yano, T. Chemotherapeutic potential of two gallic acid derivative compounds from leaves of Casearia sylvestris Sw (Flacourtiaceae). Eur. J. Pharmacol., 2009, 608(1-3), 76-83.
[174]
Fiuza, S.M.; Gomes, C.; Teixeira, L.J.; Girão da Cruz, M.T.; Cordeiro, M.N.; Milhazes, N.; Borges, F.; Marques, M.P. Phenolic acid derivatives with potential anticancer properties--a structure-activity relationship study. Part 1: methyl, propyl and octyl esters of caffeic and gallic acids. Bioorg. Med. Chem., 2004, 12(13), 3581-3589.
[175]
Lee, H.; Lee, H.; Kwon, Y.; Lee, J.H.; Kim, J.; Shin, M.K.; Kim, S.H.; Bae, H. Methyl gallate exhibits potent antitumor activities by inhibiting tumor infiltration of CD4+CD25+ regulatory T cells. J. Immunol., 2010, 185(11), 6698-6705.
[176]
Toda, A.; Piccirillo, C.A. Development and function of naturally occurring CD4+CD25+ regulatory T cells. J. Leukoc. Biol., 2006, 80(3), 458-470.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 7
Year: 2019
Page: [534 - 550]
Pages: 17
DOI: 10.2174/1568009618666181015150138
Price: $58

Article Metrics

PDF: 36
HTML: 2
EPUB: 1
PRC: 1