Interactive effects of fatty acid and butyrate-induced mitochondrial Ca 2+ loading and apoptosis in colonocytes

Cancer

Volumn 117, Issue 23, 2011, Pages 5294-5303

  Kolar, Satya ^a   Barhoumi, Rola ^b   Jones, Chris K ^a   Wesley, Joshua ^a   Lupton, Joanne R ^a   Fan, Yang Yi ^a   Chapkin, Robert S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

chemoprevention; colon cancer; combination chemotherapy; dietary fiber; endoplasmic reticulum stress; fish oil; young adult mouse colon cells

Indexed keywords

ARACHIDONIC ACID; BUTYRIC ACID; CALCIUM ION; DOCOSAHEXAENOIC ACID; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; ICOSAPENTAENOIC ACID; INITIATION FACTOR 2ALPHA; LINOLEIC ACID; OLEIC ACID; POLYUNSATURATED FATTY ACID;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL CULTURE; COLONOCYTE; CONTROLLED STUDY; CYTOSOL; DRUG MECHANISM; DRUG POTENTIATION; ENDOPLASMIC RETICULUM STRESS; GENETIC REGULATION; INTESTINE CELL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; BUTYRATES; CALCIUM; CELLS, CULTURED; COLON; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS, OMEGA-3; FATTY ACIDS, UNSATURATED; MICE; MITOCHONDRIA; RUTHENIUM COMPOUNDS;

EID: 81755184359     PISSN: 0008543X     EISSN: 10970142     Source Type: Journal    
DOI: 10.1002/cncr.26205     Document Type: Article

References (45)

1. Anti M, Armelao F, Marra G, et al. Effects of different doses of fish oil on rectal cell proliferation in patients with sporadic colonic adenomas. Gastroenterology. 1994; 107: 1709-1718. (Pubitemid 24357624)
2. 2 release in healthy subjects. Gastroenterology. 1993; 105: 1317-1322. (Pubitemid 23315305)
3. Caygill CP, Charlett A, Hill MJ,. Fat, fish, fish oil and cancer, Br J Cancer. 1996; 74: 159-164. (Pubitemid 26231995)
4. Chang WCL, Chapkin RS, Lupton FR,. Predictive value of proliferation, differentiation and apoptosis as intermediate markers for colon tumorigenesis. Carcinogenesis. 1997; 18: 721-730. (Pubitemid 28132459)
5. Chang WC, Chapkin RS, Lupton JR,. Fish oil blocks azoxymethane-induced tumorigenesis by increased cell differentiation and apoptosis rather than decreased cell proliferation, J Nutr. 1998; 18: 351-357.
6. Cheng J, Ogawa K, Kuriki K, et al. Increased intake of n-3 polyunsaturated fatty acids elevates the level of apoptosis in the normal sigmoid colon of patients polypectomized for adenomas/tumors. Cancer Lett. 2003; 193: 17-24. (Pubitemid 36412075)
7. Reddy BS, Patlolla JM, Simi B, Wang SH, Rao CV,. Prevention of colon cancer by low doses of celecoxib, a cyclooxygenase inhibitor, administered in a diet rich in w-3 polyunsaturated fatty acids. Cancer Res. 2005; 65: 8022-8027. (Pubitemid 41297283)
8. Courtney ED, Matthews S, Finlayson C, et al. Eicosapentaenoic acid (EPA) reduces crypt cell proliferation and increases apoptosis in normal colonic mucosa in subjects with a history of colorectal adenomas. Int J Colorectal Dis. 2007; 22: 765-776. (Pubitemid 46863753)
9. Hall MN, Chavarro JE, Lee IM, Willett WC, Ma J,. A 22-year prospective study of fish, n-3 fatty acid intake, and colorectal cancer risk in men. Cancer Epidemiol Biomarkers Prev. 2008; 17: 1136-1143.
10. West NJ, Clark SK, Phillips RK, et al. Eicosapentaenoic acid reduces rectal polyp number and size in familial adenomatous polyposis. Gut. 2010; 59: 918-925.
11. Verlengia R, Gorjao R, Kanunfre CC, et al. Comparative effects of eicosapentaenoic acid and docosahexaenoic acid on proliferation, cytokine production, and pleiotropic gene expression in Jurkat cells. J Nutr Biochem. 2004; 15: 657-664.
12. Rahman MD, Bhattacharya A, Fernandez G,. Docosahexaenoic acid is more potent inhibitor of osteoclast differentiation in RAW 264.7 cells than eicosapentaenoic acid. J Cell Physiol. 2008; 214: 201-209. (Pubitemid 350225482)
13. Chapkin RS, Seo J, McMurray DN, Lupton JR,. Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine. Chem Phys Lipids. 2008; 153: 14-23.
14. Bedi A, Pasricha PJ, Akhtar AJ, et al. Inhibition of apoptosis during development of colorectal cancer. Cancer Res. 1995; 55: 1811-1816.
15. Siniscrope FA, Ruan SB, Cleary KR, Stephens LC, Lee JJ, Levin B,. Bcl-2 and p53 oncoprotein expression during colorectal tumorigenesis. Cancer Res. 1995; 55: 237-241.
16. Hong MY, Lupton JR, Morris JS, et al. Dietary fish oil reduces DNA adduct levels in rat colon in part by increasing apoptosis during tumor initiation. Cancer Epidemiol Biomarkers Prev. 2000; 9: 819-826. (Pubitemid 30660055)
17. Hong MY, Bancroft LK, Turner NK, et al. Fish oil decreases oxidative DNA damage by enhancing apoptosis in rat colon. Nutr Cancer. 2005; 52: 166-175. (Pubitemid 41579759)
18. Chapkin RS, McMurray DN, Lupton DR,. Colon cancer, fatty acids and anti-inflammatory compounds. Curr Opin Gastroenterol. 2007; 23: 48-54. (Pubitemid 44875910)
19. Ng Y, Barhoumi R, Tjalkens RB, et al. The role of docosahexaenoic acid mediating mitochondrial membrane lipid oxidation and apoptosis in colonocytes. Carcinogenesis. 2005; 26: 1914-1921. (Pubitemid 41631264)
20. Crim KC, Sanders L, Hong MY, et al. Upregulation of p21waf1/cip1 expression in vivo by butyrate administration can be chemoprotective or chemopromotive depending on the lipid component of the diet. Carcinogenesis. 2008; 29: 1415-1420.
21. Smith JG, Yokoyama WH, German JB,. Butyric acid from the diet: actions at the level of gene expression. Crit Rev Food Sci. 1998; 38: 259-297. (Pubitemid 128354931)
22. Fan YY, Zhang J, Barhoumi R, et al. Antagonism of CD95 signaling blocks butyrate induction of apoptosis in young adult mouse colonic cells. Am J Physiol. 1999; 277 (2 pt 1): C310-C319. (Pubitemid 29415046)
23. Fan YY, Tian Y, Davidson LA, et al. Proapoptotic effects of n-3 fatty acids are enhanced in SOD2 knockout mouse colon. J Nutr. 2009; 139: 1328-1332.
24. Berridge MJ, Lipp P, Bootman MD,. The versatility and universality of calcium signaling. Nat Rev Mol Cell Biol. 2000; 1: 11-21.
25. Orrenius S, Gogvadze V, Zhivotovsky B,. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol. 2007; 47: 143-183.
26. 2+ accumulation. Cancer Res. 2007; 67: 5561-5568. (Pubitemid 46997299)
27. Hong MY, Chapkin RS, Barhoumi R, et al. Fish oil increases mitochondrial phospholipid unsaturation, upregulating reactive oxygen species and apoptosis in rat colonocytes. Carcinogenesis. 2002; 23: 1919-1925. (Pubitemid 35355941)
28. 2+ accumulation in human colon cancer cells and primary cultures of rat colonic crypts. Am J Physiol GI Liver Physiol. 2007; 293: G935-G943. (Pubitemid 350106557)
29. Diakogiannaki E, Morgan NG,. Differential regulation of the ER stress response by long-chain fatty acids in the pancreatic B-cell. Biochem Soc Trans. 2008; 36: 959-962.
30. Jacobsen CH, Storvold GL, Bremseth H, et al. DHA induces ER stress and growth arrest in human colon cancer cells: associations with cholesterol and calcium homeostasis. J Lipid Res. 2008; 49: 2089-2100.
31. Whitehead RH, VanEeden PE, Noble MD, Ataliotis P, Jat PS,. Establishment of conditionally immortalized epithelial cell lines from both colon and small intestine of adult H-2Kb-tsA58 transgenic mice. Proc Natl Acad Sci U S A. 1993; 90: 587-591. (Pubitemid 23028908)
32. Davidson LA, Lupton JR, Jiang YH, Chapkin RS,. Carcinogen and dietary lipid regulate ras expression and localization in rat colon without affecting farnesylation kinetics. Carcinogenesis. 1999; 20: 785-791. (Pubitemid 29191859)
33. Zoran DL, Turner ND, Taddeo SS, Chapkin RS, Lupton JR,. Wheat bran reduces tumor incidence in a rodent model of colon cancer independent of effects on distal luminal butyrate concentrations. J Nutr. 1997; 127: 2217-2225. (Pubitemid 27481768)
34. Conquer JA, Holub BJ,. Effect of supplementation with different doses of DHA on the levels of circulating DHA as non-esterified fatty acid in subjects of Asian Indian background. J Lipid Res. 1998; 39: 286-292. (Pubitemid 28100666)
35. Turk HF, Kolar SS, Fan YY, Cozby CA, Lupton JR, Chapkin RS,. Linoleic acid and butyrate synergize to increase bcl-2 in colonocytes. Int J Cancer. 2011; 128: 63-71.
36. Chami M, Oules B, Szabadkai G, Tacine R, Rizzuto R, Paterlini-Brechot P,. Role of SERCA1 truncated isoform in the proapoptotic calcium transfer from ER to mitochondria during ER stress. Mol Cell. 2008; 32: 641-651.
37. Zhao P, Xiao X, Kim AS, et al. c-Jun inhibits thapsigargin-induced ER stress through up-regulation of DSCR1/Adapt78. Exp Biol Med. 2008; 233: 1289-1300.
38. Sanders LM, Henderson CE, Hong MY, et al. Enhancement of reactive oxygen species by dietary fish oil and attenuation of antioxidant defenses by dietary pectin coordinately heightens apoptosis in rat. J Nutr. 2004; 134: 3233-3238. (Pubitemid 39602991)
39. Davidson LA, Nguyen DV, Hokanson RM, et al. Chemopreventive n-3 polyunsaturated fatty acids reprogram genetic signatures during colon cancer initiation and progression in the rat. Cancer Res. 2004; 64: 6797-6804. (Pubitemid 39297944)
40. Kim W, McMurray DN, Chapkin RS,. N-3 polyunsaturated fatty acids-physiological relevance and dose. Prostaglandins Leukot Essent Fatty Acids. 2010; 82: 155-158.
41. Lopez de Silanes N,., Olmo J, Turnay G, et al. Acquisition of resistance to butyrate enhances survival after stress and induces malignancy of human colon carcinoma cells. Cancer Res. 2004; 64: 4593-4600.
42. Graham DJ,. Cox-2 inhibitors, other NSAIDs, and cardiovascular risk. JAMA. 2006; 296: 1653-1656.
43. Bresalier RS,. Chemoprevention of colorectal neoplasia: advances and controversies (the COX-2 story). Curr Opin Gastroenterol. 2007; 23: 44-47. (Pubitemid 44875909)
44. Bingham SA, Day NE, Luben R, et al. European Prospective Investigation into Cancer and Nutrition. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet. 2003; 361: 1496-1501. (Pubitemid 36566339)
45. Gupta N, Martin PM, Prasad PD, Ganapathy V,. SLC5A8 (SMCT1)-mediated transport of butyrate forms the basis for the tumor suppressive function of the transporter. Life Sci. 2006; 78: 2419-2425.