A short-chain fatty acid, propionate, enhances the cytotoxic effect of cisplatin by modulating GPR41 signaling pathways in HepG2 cells

Oncotarget

Volumn 9, Issue 59, 2018, Pages 31342-31354

  Kobayashi, Mamiko ^a   Mikami, Daisuke ^a   Uwada, Junsuke ^b   Yazawa, Takashi ^b   Kamiyama, Kazuko ^a   Kimura, Hideki ^c   Taniguchi, Takanobu ^b   Iwano, Masayuki ^a  

^a UNIVERSITY OF FUKUI   (Japan)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

^c UNIVERSITY OF FUKUI HOSPITAL   (Japan)

Author keywords

Cleaved caspase 3; GPR41; GPR43; Histone deacetylase; SCFA

Indexed keywords

CASPASE 3; CISPLATIN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 41; G PROTEIN COUPLED RECEPTOR 43; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE 8; HISTONE H3; PROPIONATE SODIUM; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; HEP-G2 CELL LINE; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INFANT; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 85050959602     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.25809     Document Type: Article

References (45)

1. Bruix J, Reig M, Sherman M. Evidence-based diagnosis, staging, and treatment of patients with hepatocellular carcinoma. Gastroenterol. 2016; 150:836-53
2. Buecher B, Bleiberg H. Non-systemic chemotherapy in the treatment of colorectal cancer-Portal vein, hepatic arterial and intraperitoneal approaches. Aliment Pharmacol Ther. 2001; 15:1527-41
3. Guarner F, Malagelada JR. Gut flora in health and disease. Lancet. 2003; 360:512-9
4. Donohoe DR, Garge N, Zhang X, Sun W, O'Connell TM, Bunger MK, Bultman SJ. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011; 13:517-26
5. Harig JM, Soergel KH, Komorowski RA, Wood CM. Treatment of diversion colitis with short-chain-fatty acid irrigation. N Engl J Med. 1989; 320:23-8
6. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, Tobe T, Clarke JM, Topping DL, Suzuki T, Taylor TD, Itoh K, Kikuchi J, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011; 469:543-7
7. Bindels LB, Porporato P, Dewulf EM, Verrax J, Neyrinck AM, Martin JC, Scott KP, Buc Calderon P, Feron O, Muccioli GG, Sonveaux P, Cani PD, Delzenne NM. Gut microbiota-derived propionate reduces cancer cell proliferation in the liver. Br J Cancer. 2012; 107:1337-44
8. Tang Y, Chen Y, Jiang H, Robbins GT, Nie D. G-proteincoupled receptor for short-chain fatty acids suppresses colon cancer. Int J Cancer. 2011; 128:847-56
9. Thirunavukkarasan M, Wang C, Rao A, Hind T, Teo YR, Siddiquee AAM, Goghari MAI, Kumar AP, Herr DR. Shortchain fatty acid receptors inhibit invasive phenotypes in breast cancer cells. PLoS One. 2017; 12:e0186334
10. Candido EPM, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell. 1978; 14:105-13
11. Sealy L, Chalkley R. The effect of sodium butyrate on histone modification. Cell. 1978; 14:115-21
12. Vidali G, Boffa LC, Bradbury EM, Allfrey VG. Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc Natl Acad Sci USA. 1978; 75:2239-43
13. Boffa IC, Vidali G, Mann RS, Allfrey VG. Suppression of histone deacetylation in vivo and in vitro by sodium butyrate. J Biol Chem. 1978; 253:3364-6
14. Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA. The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr. 2002; 132:1012-7
15. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, Pike NB, Strum JC, Steplewski KM, et al. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem. 2003; 278:11312-9
16. Hong YH, Nishimura Y, Hishikawa D, Tsuzuki H, Miyahara H, Gotoh C, Choi KC, Feng DD, Chen C, Lee HG, Katoh K, Roh SG, Sasaki S. Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology. 2005; 146:5092-9
17. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, MacKay F, Artis D, Xavier RJ, Teixeira MM, MacKay CR. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009; 461:1282-6
18. Koprinarova M, Markovska P, Iliev I, Anachkova B, Russev G. Sodium butyrate enhances the cytotoxic effect of cisplatin by abrogating the cisplatin imposed cell cycle arrest. BMC Mol Biol. 2010; 11:49
19. Buurman R, Grlevik E, Schffer V, Eilers M, Sandbothe M, Kreipe H, Wilkens L, Schlegelberger B, Khnel F, Skawran B. Histone deacetylases activate hepatocyte growth factor signaling by repressing microRNA-449 in hepatocellular carcinoma cells. Gastroenterology. 2012; 143:811-820.e15
20. Shin S, Kim M, Lee SJ, Park KS, Lee CH. Trichostatin a sensitizes hepatocellular carcinoma cells to enhanced NK cell-mediated killing by regulating immune-related genes. Cancer Genomics Proteomics. 2017; 14:349-62
21. Rivera S, Leteur C, Mégnin F, Law F, Martins I, Kloos I, Depil S, Modjtahedi N, Perfettini JL, Hennequin C, Deutsch E. Time dependent modulation of tumor radiosensitivity by a pan HDAC inhibitor: abexinostat. Oncotarget. 2017; 8:56210-27. https://doi.org/10.18632/oncotarget.14813
22. Kim MS, Blake M, Baek JH, Kohlhagen G, Pommier Y, Carrier F. Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Res. 2003; 63:7291-300
23. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007; 35:495-516
24. Powers SK, Hudson MB, Nelson WB, Talbert EE, Min K, Szeto HH, Kavazis AN, Smuder AJ. Mitochondria-targeted antioxidants protect against mechanical ventilation-induced diaphragm weakness. Crit Care Med. 2011; 39:1749-59
25. Mangmool S, Kurose H. Gi/o protein-dependent and-independent actions of pertussis toxin (ptx). Toxins (Basel). 2011; 3:884-99
26. Park JS, Lee EJ, Lee JC, Kim WK, Kim HS. Antiinflammatory effects of short chain fatty acids in IFNgamma-stimulated RAW 264.7 murine macrophage cells: involvement of NF-kappaB and ERK signaling pathways. Int Immunopharmacol. 2007; 7:70-7
27. Vinolo MAR, Rodrigues HG, Hatanaka E, Sato FT, Sampaio SC, Curi R. Suppressive effect of short-chain fatty acids on production of proinflammatory mediators by neutrophils. J Nutr Biochem. 2011; 22:849-55
28. Tedelind S, Westberg F, Kjerrulf M, Vidal A. Antiinflammatory properties of the short-chain fatty acids acetate and propionate: A study with relevance to inflammatory bowel disease. World J Gastroenterol. 2007; 13:2826-32
29. Kobayashi M, Mikami D, Kimura H, Kamiyama K, Morikawa Y, Yokoi S, Kasuno K, Takahashi N, Taniguchi T, Iwano M. Short-chain fatty acids, GPR41 and GPR43 ligands, inhibit TNF-α-induced MCP-1 expression by modulating p38 and JNK signaling pathways in human renal cortical epithelial cells. Biochem Biophys Res Commun. 2017; 486:499-505
30. Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, Sitaraman SV, Knight R, Ley RE, Gewirtz AT. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science. 2010; 328:228-31
31. Ang Z, Er JZ, Tan NS, Lu J, Liou YC, Grosse J, Ding JL. Human and mouse monocytes display distinct signalling and cytokine profiles upon stimulation with FFAR2/FFAR3 short-chain fatty acid receptor agonists. Sci Rep. 2016; 6:34145
32. Andrade-Oliveira V, Amano MT, Correa-Costa M, Castoldi A, Felizardo RJF, de Almeida DC, Bassi EJ, Moraes-Vieira PM, Hiyane MI, Rodas ACD, Peron JPS, Aguiar CF, Reis MA, et al. Gut bacteria products prevent aki induced by ischemia-reperfusion. J Am Soc Nephrol. 2015; 26:1877-88
33. Aoyama M, Kotani J, Usami M. Butyrate and propionate induced activated or non-activated neutrophil apoptosis via HDAC inhibitor activity but without activating GPR-41/GPR-43 pathways. Nutrition. 2010; 26:653-61
34. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic treg cell homeostasis. Science. 2013; 341:569-73
35. Benedetti G, Fredriksson L, Herpers B, Meerman J, Van De Water B, De Graauw M. TNF-α-mediated NF-κB survival signaling impairment by cisplatin enhances JNK activation allowing synergistic apoptosis of renal proximal tubular cells. Biochem Pharmacol. 2013; 85:274-86
36. Pabla N, Dong Z. Cisplatin nephrotoxicity: Mechanisms and renoprotective strategies. Kidney Int. 2008; 73:994-1007
37. van Horssen R, Ten Hagen TLM, Eggermont AMM. TNFalpha in cancer treatment: molecular insights, antitumor effects, and clinical utility. Oncologist. 2006; 11:397-408
38. Sun H, Zhong YJ, Zheng XL, Wang Q, Yang L, Shi F, Yan JQ, He F, Liao LC, Lin Y, Zhang L, Wang X. Critical role of CD40-mediated autocrine tumor necrosis factoralpha in potentiation of cisplatin-induced cytotoxicity in cancer cells. Cancer Sci. 2012; 103:197-202
39. Liu J, Li G, Wang X, Wang L, Zhao R, Wang J, Kong Y, Ding J, Li J, Zhang L. Droxinostat, a histone deacetylase inhibitor, induces apoptosis in hepatocellular carcinoma cell lines via activation of the mitochondrial pathway and downregulation of FLIP. Transl Oncol. 2016; 9:70-8
40. Fan J, Lou B, Chen W, Zhang J, Lin S, Lv FF, Chen Y. Down-regulation of HDAC5 inhibits growth of human hepatocellular carcinoma by induction of apoptosis and cell cycle arrest. Tumour Biol. 2014; 35:11523-32
41. Kanno K, Kanno S, Nitta H, Uesugi N, Sugai T, Masuda T, Wakabayashi G, Maesawa C. Overexpression of histone deacetylase 6 contributes to accelerated migration and invasion activity of hepatocellular carcinoma cells. Oncol Rep. 2012; 28:867-73
42. Wu J, Du C, Lv Z, Ding C, Cheng J, Xie H, Zhou L, Zheng S. The up-regulation of histone deacetylase 8 promotes proliferation and inhibits apoptosis in hepatocellular carcinoma. Dig Dis Sci. 2013; 58:3545-53
43. Finnin MS, Donigian JR, Cohen A, Richon VM, Rifkind RA, Marks PA, Breslow R, Pavletich NP. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature. 1999; 401:188-93
44. Gururaja TL, Yung S, Ding R, Huang J, Zhou X, McLaughlin J, Daniel-Issakani S, Singh R, Cooper RDG, Payan DG, Masuda ES, Kinoshita T. A class of small molecules that inhibit TNFα-induced survival and death pathways via prevention of interactions between TNFαRI, TRADD, and RIP1. Chem Biol. 2007; 14:1105-18
45. Mikami D, Kimura H, Kamiyama K, Torii K, Kasuno K, Takahashi N, Yoshida H, Iwano M. Telmisartan activates endogenous peroxisome proliferator-activated receptor-d and may have anti-fibrotic effects in human mesangial cells. Hypertens Res. 2014; 37:422-31