Tumor growth retardation and chemosensitizing action of fatty acid synthase inhibitor orlistat on T cell lymphoma: Implication of reconstituted tumor microenvironment and multidrug resistance phenotype

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 1, 2014, Pages 294-302

  Kant, Shiva ^a   Kumar, Ajay ^a   Singh, Sukh Mahendra ^a  

^a BANARAS HINDU UNIVERSITY   (India)

Author keywords

Apoptosis; Chemosensitization; Fatty acid synthase; Orlistat; T cell lymphoma

Indexed keywords

CISPLATIN; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 6; MULTIDRUG RESISTANCE PROTEIN; TETRAHYDROLIPSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL POPULATION; CELL SURVIVAL; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; FASN GENE; GENE EXPRESSION; MOUSE; NONHUMAN; ONCOGENE; PH; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T CELL LYMPHOMA; TUMOR GROWTH; TUMOR MICROENVIRONMENT; UPREGULATION;

MURINAE; MUS;

APOPTOSIS; CHEMOSENSITIZATION; DALTON'S LYMPHOMA; DCFDA; DICHLORODIHYDROFLUORESCEIN DIACETATE; DL; FASN; FATTY ACID SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INOS; MDR; MRP-1; MULTIDRUG RESISTANT ASSOCIATED PROTEIN-1; MULTIDRUG RESISTANT PROTEIN; NITRIC OXIDE; NO; ORLISTAT; REACTIVE OXYGEN SPECIES; ROS; T CELL LYMPHOMA;

ANIMALS; ANTI-OBESITY AGENTS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CISPLATIN; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, MULTIPLE; DRUG THERAPY, COMBINATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FATTY ACID SYNTHASES; FLOW CYTOMETRY; LACTONES; LYMPHOMA, T-CELL; MICE; MICE, INBRED BALB C; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR MICROENVIRONMENT;

EID: 84885343725     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.09.020     Document Type: Article

References (56)

1. J.P. Gillet, T. Efferth, and J. Remacle Chemotherapy-induced resistance by ATP-binding cassette transporter genes Biochim. Biophys. Acta 1775 2007 237 262 (Pubitemid 46899341)
2. G. Szakacs, J.K. Paterson, J.A. Ludwig, C. Booth-Genthe, and M.M. Gottesman Targeting multidrug resistance in cancer Nat. Rev. Drug Discov. 5 2006 219 234 (Pubitemid 43336035)
3. D. Neri, and C.T. Supuran Interfering with pH regulation in tumours as a therapeutic strategy Nat. Rev. Drug Discov. 10 2011 767 777
4. K.M. Bailey, J.W. Wojtkowiak, A.I. Hashim, and R.J. Gillies Targeting the metabolic microenvironment of tumors Adv. Pharmacol. 65 2012 63 107
5. M.A. Swartz, N. Iida, E.W. Roberts, S. Sangaletti, M.H. Wong, F.E. Yull, L.M. Coussens, and Y.A. DeClerck Tumor microenvironment complexity: emerging roles in cancer therapy Cancer Res. 72 2012 2473 2480
6. J.A. Menendez Fine-tuning the lipogenic/lipolytic balance to optimize the metabolic requirements of cancer cell growth: molecular mechanisms and therapeutic perspectives Biochim. Biophys. Acta 1801 2010 381 391
7. H. Liu, J.Y. Liu, X. Wu, and J.T. Zhang Biochemistry, molecular biology, and pharmacology of fatty acid synthase, an emerging therapeutic target and diagnosis/prognosis marker Int. J. Biochem. Mol. Biol. 1 2010 69 89
8. T. Mashima, H. Seimiya, and T. Tsuruo De novo fatty-acid synthesis and related pathways as molecular targets for cancer therapy Br. J. Cancer 100 2009 1369 1372
9. J.A. Menendez, and R. Lupu Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis Nat. Rev. Cancer 7 2007 763 777 (Pubitemid 47469806)
10. R. Flavin, S. Peluso, P.L. Nguyen, and M. Loda Fatty acid synthase as a potential therapeutic target in cancer Future Oncol. 6 2010 551 562
11. J.V. Swinnen, K. Brusselmans, and G. Verhoeven Increased lipogenesis in cancer cells: new players, novel targets Curr. Opin. Clin. Nutr. Metab. Care 9 2006 358 365 (Pubitemid 44101970)
12. S.S. Chirala, A. Jayakumar, Z.W. Gu, and S.J. Wakil Human fatty acid synthase: role of interdomain in the formation of catalytically active synthase dimer Proc. Natl. Acad. Sci. U. S. A. 98 2001 3104 3108 (Pubitemid 32220806)
13. J. Fujiwara, Y. Sowa, M. Horinaka, M. Koyama, M. Wakada, T. Miki, and T. Sakai The anti-obesity drug orlistat promotes sensitivity to TRAIL by two different pathways in hormone-refractory prostate cancer cells Int. J. Oncol. 40 2012 1483 1491
14. S. Kant, A. Kumar, and S.M. Singh Fatty acid synthase inhibitor orlistat induces apoptosis in T cell lymphoma: role of cell survival regulatory molecules Biochim. Biophys. Acta 1820 2012 1764 1773
15. J. Ross, A.M. Najjar, M. Sankaranarayanapillai, W.P. Tong, K. Kaluarachchi, and S.M. Ronen Fatty acid synthase inhibition results in a magnetic resonance-detectable drop in phosphocholine Mol. Cancer Ther. 7 2008 2556 2565
16. S.A. Zaitone, and S. Essawy Addition of a low dose of rimonabant to orlistat therapy decreases weight gain and reduces adiposity in dietary obese rats Clin. Exp. Pharmacol. Physiol. 39 2012 551 559
17. J.S. Fang, R.D. Gillies, and R.A. Gatenby Adaptation to hypoxia and acidosis in carcinogenesis and tumor progression Semin. Cancer Biol. 18 2008 330 337
18. H. Izumi, T. Torigoe, H. Ishiguchi, H. Uramoto, Y. Yoshida, M. Tanabe, T. Ise, T. Murakami, T. Yoshida, M. Nomoto, and K. Kohno Cellular pH regulators: potentially promising molecular targets for cancer chemotherapy Cancer Treat. Rev. 29 2003 541 549 (Pubitemid 37428326)
19. L.E. Gerweck, S. Vijayappa, and S. Kozin Tumor pH controls the in vivo efficacy of weak acid and base chemotherapeutics Mol. Cancer Ther. 5 2006 1275 1279 (Pubitemid 43881320)
20. A. Kumar, A.C. Bharti, and S.M. Singh Effect of aspirin administration on reversal of tumor-induced suppression of myelopoiesis in T-cell lymphoma bearing host Blood Cells Mol. Dis. 48 2012 238 246
21. A. Kumar, S. Kant, and S.M. Singh Novel molecular mechanisms of antitumor action of dichloroacetate against T cell lymphoma: implication of altered glucose metabolism, pH homeostasis and cell survival regulation Chem. Biol. Interact. 199 2012 29 37
22. A. Kumar, S. Kant, and S.M. Singh Alpha-Cyano-4-hydroxycinnamate induces apoptosis in Dalton's lymphoma cells: role of altered cell survival-regulatory mechanisms Anticancer Drugs 24 2013 158 171
23. M.A. Carvalho, K.G. Zecchin, F. Seguin, D.C. Bastos, M. Agostini, A.L. Rangel, S.S. Veiga, H.F. Raposo, H.C. Oliveira, M. Loda, R.D. Coletta, and E. Graner Fatty acid synthase inhibition with Orlistat promotes apoptosis and reduces cell growth and lymph node metastasis in a mouse melanoma model Int. J. Cancer 123 2008 2557 2565
24. N.K. Vishvakarma, and S.M. Singh Augmentation of myelopoiesis in a murine host bearing a T cell lymphoma following in vivo administration of proton pump inhibitor pantoprazole Biochimie 93 2011 1786 1796
25. N.K. Vishvakarma, and S.M. Singh Mechanisms of tumor growth retardation by modulation of pH regulation in the tumor-microenvironment of a murine T cell lymphoma Biomed. Pharmacother. 65 2011 27 39
26. E. Furuta, S.K. Pai, R. Zhan, S. Bandyopadhyay, M. Watabe, Y.Y. Mo, S. Hirota, S. Hosobe, T. Tsukada, K. Miura, S. Kamada, K. Saito, M. Iiizumi, W. Liu, J. Ericsson, and K. Watabe Fatty acid synthase gene is up-regulated by hypoxia via activation of Akt and sterol regulatory element binding protein-1 Cancer Res. 68 2008 1003 1011 (Pubitemid 351278386)
27. W. Rosenau, G.C. Burke, and R. Anderson Effects of lymphotoxin on target-cell plasma-membrane lipids Cell. Immunol. 60 1981 144 154 (Pubitemid 11102723)
28. J.P. Gillet, and M.M. Gottesman Advances in the molecular detection of ABC transporters involved in multidrug resistance in cancer Curr. Pharm. Biotechnol. 12 2011 686 692
29. F. Seguin, M.A. Carvalho, D.C. Bastos, M. Agostini, K.G. Zecchin, M.P. Alvarez-Flores, A.M. Chudzinski-Tavassi, R.D. Coletta, and E. Graner The fatty acid synthase inhibitor orlistat reduces experimental metastases and angiogenesis in B16-F10 melanomas Br. J. Cancer 107 2012 977 987
30. J.M. Tirado-Velez, I. Joumady, A. Saez-Benito, I. Cozar-Castellano, and G. Perdomo Inhibition of fatty acid metabolism reduces human myeloma cells proliferation PLoS One 7 2012 e46484
31. C. Sautes-Fridman, J. Cherfils-Vicini, D. Damotte, S. Fisson, W.H. Fridman, I. Cremer, and M.C. Dieu-Nosjean Tumor microenvironment is multifaceted Cancer Metastasis Rev. 30 2011 13 25
32. S.L. Shiao, A.P. Ganesan, H.S. Rugo, and L.M. Coussens Immune microenvironments in solid tumors: new targets for therapy Genes Dev. 25 2011 2559 2572
33. S. Huerta-Yepez, M. Vega, S.E. Escoto-Chavez, B. Murdock, T. Sakai, S. Baritaki, and B. Bonavida Nitric oxide sensitizes tumor cells to TRAIL-induced apoptosis via inhibition of the DR5 transcription repressor Yin Yang 1 Nitric Oxide 20 2009 39 52
34. X. Peng, and V. Gandhi ROS-activated anticancer prodrugs: a new strategy for tumor-specific damage Ther. Deliv. 3 2012 823 833
35. F. Rothweiler, M. Michaelis, P. Brauer, J. Otte, K. Weber, B. Fehse, H.W. Doerr, M. Wiese, J. Kreuter, Y. Al-Abed, F. Nicoletti, and J. Cinatl Jr. Anticancer effects of the nitric oxide-modified saquinavir derivative saquinavir-NO against multidrug-resistant cancer cells Neoplasia 12 2010 1023 1030
36. W.M. Xu, L.Z. Liu, M. Loizidou, M. Ahmed, and I.G. Charles The role of nitric oxide in cancer Cell Res. 12 2002 311 320 (Pubitemid 135708343)
37. J. Yang, L.J. Wu, S.I. Tashino, S. Onodera, and T. Ikejima Reactive oxygen species and nitric oxide regulate mitochondria-dependent apoptosis and autophagy in evodiamine-treated human cervix carcinoma HeLa cells Free Radic. Res. 42 2008 492 504 (Pubitemid 351935163)
38. H.U. Simon, A. Haj-Yehia, and F. Levi-Schaffer Role of reactive oxygen species (ROS) in apoptosis induction Apoptosis 5 2000 415 418 (Pubitemid 32162623)
39. H.T. Chung, H.O. Pae, B.M. Choi, T.R. Billiar, and Y.M. Kim Nitric oxide as a bioregulator of apoptosis Biochem. Biophys. Res. Commun. 282 2001 1075 1079
40. E. Itakura, R.R. Huang, D.R. Wen, E. Paul, P.H. Wunsch, and A.J. Cochran IL-10 expression by primary tumor cells correlates with melanoma progression from radial to vertical growth phase and development of metastatic competence Mod. Pathol. 24 2011 801 809
41. A.M. O'Farrell, Y. Liu, K.W. Moore, and A.L.F. Mui IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for Stat3-dependent and -independent pathways EMBO J. 17 1998 1006 1018 (Pubitemid 28077655)
42. R. Sabat, G. Grutz, K. Warszawska, S. Kirsch, E. Witte, K. Wolk, and J. Geginat Biology of interleukin-10 Cytokine Growth Factor Rev. 21 2010 331 344
43. R. Perez-Rodriguez, C. Roncero, A.M. Olivan, M.P. Gonzalez, and M.J. Oset-Gasque Signaling mechanisms of interferon gamma induced apoptosis in chromaffin cells: involvement of nNOS, iNOS, and NFkappaB J. Neurochem. 108 2009 1083 1096
44. E.Y. Ahn, G. Pan, S.M. Vickers, and J.M. McDonald IFN-gammaupregulates apoptosis-related molecules and enhances Fas-mediated apoptosis in human cholangiocarcinoma Int. J. Cancer 100 2002 445 451
45. L. Wall, F. Burke, C. Barton, J. Smyth, and F. Balkwill IFN-gamma induces apoptosis in ovarian cancer cells in vivo and in vitro Clin. Cancer Res. 9 2003 2487 2496 (Pubitemid 36842088)
46. W. Doerrler, K.R. Feingold, and C. Grunfeld Cytokines induce catabolic effects in cultured adipocytes by multiple mechanisms Cytokine 6 1994 478 484 (Pubitemid 24306961)
47. F.C. McGillicuddy, E.H. Chiquoine, C.C. Hinkle, R.J. Kim, R. Shah, H.M. Roche, E.M. Smyth, and M.P. Reilly Interferon gamma attenuates insulin signaling, lipid storage, and differentiation in human adipocytes via activation of the JAK/STAT pathway J. Biol. Chem. 284 2009 31936 31944
48. W.J. Wang, X.X. Shi, Y.W. Liu, Y.Q. He, Y.Z. Wang, C.X. Yang, and F. Gao The mechanism underlying the effects of the cell surface ATP synthase on the regulation of intracellular acidification during acidosis J. Cell. Biochem. 114 2013 1695 1703
49. B. Marquez, and F. Van Bambeke ABC multidrug transporters: target for modulation of drug pharmacokinetics and drug-drug interactions Curr. Drug Targets 12 2011 600 620
50. J.T. Zhang Use of arrays to investigate the contribution of ATP-binding cassette transporters to drug resistance in cancer chemotherapy and prediction of chemosensitivity Cell Res. 17 2007 311 323
51. U. Stein, and W. Walther Cytokine-mediated reversal of multidrug resistance Cytotechnology 27 1998 271 282 (Pubitemid 29025475)
52. D. Szabo, H. Keyzer, H.E. Kaiser, and J. Molnar Reversal of multidrug resistance of tumor cells Anticancer. Res. 20 2000 4261 4274 (Pubitemid 32141771)
53. S.M. Simon, and M. Schindler Cell biological mechanisms of multidrug resistance in tumors Proc. Natl. Acad. Sci. U. S. A. 91 1994 3497 3504 (Pubitemid 24139457)
54. +-ATPase in drug-resistant human breast carcinoma cell lines Biochem. Pharmacol. 57 1999 1037 1046 (Pubitemid 29168552)
55. M. Wartenberg, E. Hoffmann, H. Schwindt, F. Grunheck, J. Petros, J.R.S. Arnold, R. Hescheler, and H. Sauer Reactive oxygen species-linked regulation of the multidrug resistance transporter P-glycoprotein in Nox-1 overexpressing prostate tumor spheroids FEBS Lett. 579 2005 4541 4549 (Pubitemid 41116394)
56. C. Riganti, E. Miraglia, D. Viarisio, C. Costamagna, G. Pescarmona, D. Ghigo, and A. Bosia Nitric oxide reverts the resistance to doxorubicin in human colon cancer cells by inhibiting the drug efflux Cancer Res. 65 2005 516 525 and Technology