Induction of apoptosis by the medium-chain length fatty acid lauric acid in colon cancer cells due to induction of oxidative stress

Chemotherapy

Volumn 59, Issue 3, 2014, Pages 214-224

  Fauser, J K ^a,b   Matthews, G M ^c,d   Cummins, A G ^b   Howarth, G S ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b QUEEN ELIZABETH HOSPITAL   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

Apoptosis; Caco 2; Cell cycle; Colorectal cancer; Glutathione; IEC 6; Medium chain fatty acid; Reactive oxygen species; Redox; Short chain fatty acid

Indexed keywords

BUTYRIC ACID; GLUTATHIONE; LAURIC ACID; REACTIVE OXYGEN METABOLITE; ANTINEOPLASTIC AGENT; SODIUM LAURIC ACID; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL DEATH; CELL LINE; CELL STRAIN CACO 2; CELL VIABILITY; COLON CANCER; FLOW CYTOMETRY; INTESTINE CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; ANTINEOPLASTIC ACTIVITY; CACO 2 CELL LINE; CANCER INHIBITION; CELL COUNT; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYMOLOGY; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; INCUBATION TIME; M PHASE CELL CYCLE CHECKPOINT; PROTEIN ANALYSIS;

APOPTOSIS; BUTYRATES; CACO-2 CELLS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; COLONIC NEOPLASMS; HUMANS; LAURIC ACIDS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84890464769     PISSN: 00093157     EISSN: 14219794     Source Type: Journal    
DOI: 10.1159/000356067     Document Type: Article

References (45)

1. Matthews GM, Howarth GS, Butler RN: Short-chain fatty acids induce apoptosis in colon cancer cells associated with changes to intracellular redox state and glucose metabolism. Chemotherapy 2012; 58: 102-109.
2. 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; 132:1012-1017. (Pubitemid 34493567)
3. Fauser JK, Prisciandaro LD, Cummins AG, Howarth GS: Fatty acids as potential adjunc-tive colorectal chemotherapeutic agents. Cancer Biol Ther 2011; 11:724-731.
4. Matthews GM, Butler RN: Cellular mucosal defense during Helicobacter pylori infection: a review of the role of glutathione and the oxi-dative pentose pathway. Helicobacter 2005; 10:298-306. (Pubitemid 41104968)
5. Young GP, Hu Y, Le Leu RK, Nyskohus L: Dietary fibre and colorectal cancer: a model for environment-gene interactions. Mol Nutr Food Res 2005; 49:571-584. (Pubitemid 40853703)
6. Beermann C, Jelinek J, Reinecker T, Hauen-schild A, Boehm G, Klor HU: Short-term effects of dietary medium-chain fatty acids and n-3 long-chain polyunsaturated fatty acids on the fat metabolism of healthy volunteers. Lip-ids Health Dis 2003; 2:1-10. (Pubitemid 38809228)
7. Bocca C, Bozzo F, Gabriel L, Miglietta A: Conjugated linoleic acid inhibits Caco-2 cell growth via ERK-MAPK signaling pathway. J Nutr Biochem 2007; 18:332-340. (Pubitemid 46590715)
8. Lima TM, Kanunfre CC, Pompeia C, Verlen-gia R, Curi R: Ranking the toxicity of fatty acids on Jurkat and Raji cells by flow cytometric analysis. Toxicol In Vitro 2002; 16:741-747. (Pubitemid 35356282)
9. Pajak B, Gajkowska B, Orzechowski A: Sodium butyrate sensitizes human colon adeno-carcinoma COLO 205 cells to both intrinsic and TNF-alpha-dependent extrinsic apopto-sis. Apoptosis 2009; 14:203-217.
10. Hyzd'alova M, Hofmanova J, Pachernik J, Vac-ulova A, Kozubik A: The interaction of butyr-ate with TNF-alpha during differentiation and apoptosis of colon epithelial cells: role of NF-kappaB activation. Cytokine 2008; 44: 33-43.
11. Buda A, Qualtrough D, Jepson MA, Martines D, Paraskeva C, Pignatelli M: Butyrate down-regulates alpha2beta1 integrin: a possible role in the induction of apoptosis in colorectal cancer cell lines. Gut 2003; 52:729-734. (Pubitemid 36528877)
12. Ruemmele FM, Schwartz S, Seidman EG, Di-onne S, Levy E, Lentze MJ: Butyrate induced Caco-2 cell apoptosis is mediated via the mi-tochondrial pathway. Gut 2003; 52:94-100. (Pubitemid 36020773)
13. Engelbrecht AM, Toit-Kohn JL, Ellis B, Thomas M, Nell T, Smith R: Differential induction of apoptosis and inhibition of the PI3-kinase pathway by saturated, monounsaturated and polyunsaturated fatty acids in a colon cancer cell model. Apoptosis 2008; 13:1368-1377.
14. Nano JL, Nobili C, Girard-Pipau F, Rampal P: Effects of fatty acids on the growth of Caco-2 cells. Prostaglandins Leukot Essent Fatty Acids 2003; 69:207-215. (Pubitemid 37463800)
15. Kato T, Kolenic N, Pardini RS: Docosahexae-noic acid (DHA), a primary tumor suppres-sive omega-3 fatty acid, inhibits growth of colorectal cancer independent of p53 muta-tional status. Nutr Cancer 2007; 58:178-187. (Pubitemid 47328769)
16. Lee SH, Yamaguchi K, Kim JS, Eling TE, Safe S, Park Y, et al: Conjugated linoleic acid stimulates an anti-tumorigenic protein NAG-1 in an isomer specific manner. Carcinogenesis 2006; 27:972-981.
17. Toit-Kohn JL, Louw L, Engelbrecht AM: Doc-osahexaenoic acid induces apoptosis in colorectal carcinoma cells by modulating the PI3 kinase and p38 MAPK pathways. J Nutr Biochem 2009; 20:106-114.
18. Sun Y, Huang L, Mackenzie GG, Rigas B: Ox-idative stress mediates through apoptosis the anticancer effect of phospho-nonsteroidal anti-inflammatory drugs: implications for the role of oxidative stress in the action of anti-cancer agents. J Pharmacol Exp Ther 2011; 338:775-783.
19. Aw TY: Molecular and cellular responses to oxidative stress and changes in oxidation-reduction imbalance in the intestine. Am J Clin Nutr 1999; 70:557-565. (Pubitemid 29463451)
20. Rigas B, Sun Y: Induction of oxidative stress as a mechanism of action of chemopreventive agents against cancer. Br J Cancer 2008; 98: 1157-1160. (Pubitemid 351481667)
21. Conklin KA: Chemotherapy-associated oxida-tive stress: impact on chemotherapeutic effectiveness. Integr Cancer Ther 2004; 3: 284-300.
22. Circu ML, Aw TY: Glutathione and apopto-sis. Free Radic Res 2008; 42:689-706.
23. Balendiran GK, Dabur R, Fraser D: The role of glutathione in cancer. Cell Biochem Funct 2004; 22:343-352. (Pubitemid 39518098)
24. Gotoh Y, Noda T, Iwakiri R, Fujimoto K, Rhoads CA, Aw TY: Lipid peroxide-induced redox imbalance differentially mediates Caco-2 cell proliferation and growth arrest. Cell Prolif 2002; 35:221-235. (Pubitemid 34985157)
25. Palomares T, Carames M, Garcia-Alonso I, Alonso-Varona A: Glutathione modulation reverses the growth-promoting effect of growth factors, improving the 5-fluorouracil antitumour response in WiDr colon cancer cells. Anticancer Res 2009; 29:3957-3965.
26. Matthews GM, Howarth GS, Butler RN: Short-chain fatty acid modulation of apopto-sis in the Kato III human gastric carcinoma cell line. Cancer Biol Ther 2007; 6:1051-1057. (Pubitemid 351574956)
27. Trigatti BL, Gerber GE: A direct role for serum albumin in the cellular uptake of long-chain fatty acids. Biochem J 1995; 308: 155-159.
28. Alexandre J, Batteux F, Nicco C, Chereau C, Laurent A, Guillevin L, et al: Accumulation of hydrogen peroxide is an early and crucial step for paclitaxel-induced cancer cell death both in vitro and in vivo. Int J Cancer 2006; 119:41-48.
29. Trayner ID, Rayner AP, Freeman GE, Far-zaneh F: Quantitative multiwell myeloid differentiation assay using dichlorodihydrofluo-rescein diacetate (H2DCF-DA) or dihy-drorhodamine 123 (H2R123). J Immunol Methods 1995; 186:275-284.
30. Attene-Ramos M, Kitiphongspattana K, Ishii-Schrade K, Gaskins HR: Temporal changes of multiple redox couples from proliferation to growth arrest in IEC-6 intestinal epithelial cells. Am J Physiol Cell Physiol 2005; 289:C1220-C1228. (Pubitemid 41456838)
31. Sado-Kamdem SL, Vannini L, Guerzoni ME: Effect of alpha-linolenic, capric and lauric acid on the fatty acid biosynthesis in Staphy-lococcus aureus. Int J Food Microbiol 2009; 129:288-294.
32. Adhikari D, Feroz F, Liefshitz A, Barakat RR, Bertino JR, Banerjee D: Pretreatment of endo-metrial carcinoma cell lines with butyrate results in upregulation of Bax and correlates with potentiation of radiation induced cell kill. In Vivo 2000; 14:603-609. (Pubitemid 34097520)
33. Litvak DA, Evers BM, Hwang KO, Hellmich MR, Ko TC, Townsend CM Jr: Butyrate-in-duced differentiation of Caco-2 cells is associated with apoptosis and early induction of p21Waf1/Cip1 and p27Kip1. Surgery 1998; 124: 161-169, discussion 169-170.
34. Roy MJ, Dionne S, Marx G, Qureshi I, Sarma D, Levy E, et al: In vitro studies on the inhibition of colon cancer by butyrate and carnitine. Nutrition 2009; 25:1193-1201.
35. Takayama C, Mukaizawa F, Fujita T, Oga-wara K, Ogawara K, Kimura T: Amino acids suppress apoptosis induced by sodium lau-rate, an absorption enhancer. J Pharm Sci 2009; 98:4629-4638.
36. Bartolotta S, Garcia CC, Candurra NA, Da-monte EB: Effect of fatty acids on arenavirus replication: inhibition of virus production by lauric acid. Arch Virol 2001; 146:777-790. (Pubitemid 32437312)
37. Hornung B, Amtmann E, Sauer G: Lauric acid inhibits the maturation of vesicular stomatitis virus. J Gen Virol 1994; 75:353-361. (Pubitemid 24050393)
38. Petschow BW, Batema RP, Ford LL: Susceptibility of Helicobacter pylori to bactericidal properties of medium-chain monoglycerides and free fatty acids. Antimicrob Agents Che-mother 1996; 40:302-306. (Pubitemid 26049339)
39. Kirlin WG, Cai J, Thompson SA, Diaz D, Ka-vanagh TJ, Jones DP: Glutathione redox potential in response to differentiation and enzyme inducers. Free Radic Biol Med 1999; 27: 1208-1218. (Pubitemid 30001481)
40. Pias EK, Aw TY: Apoptosis in mitotic competent undifferentiated cells is induced by cellular redox imbalance independent of reactive oxygen species production. FASEB J 2002; 16: 781-790. (Pubitemid 34615126)
41. Noda T, Iwakiri R, Fujimoto K, Aw TY: Induction of mild intracellular redox imbalance inhibits proliferation of Caco-2 cells. FASEB J 2001; 15:2131-2139. (Pubitemid 32927930)
42. Xiang AC, Xie J, Zhang XJ: Acetylcholinester-ase in intestinal cell differentiation involves G2/M cell cycle arrest. Cell Mol Life Sci 2008; 65:1768-1779.
43. Jordan A, Stein J: Effect of an omega-3 fatty acid containing lipid emulsion alone and in combination with 5-fluorouracil (5-FU) on growth of the colon cancer cell line Caco-2. Eur J Nutr 2003; 42:324-331. (Pubitemid 38055612)
44. Circu ML, Aw TY: Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 2010; 48:749-762.
45. Muller RH, Radtke M, Wissing SA: Nano-structured lipid matrices for improved micro-encapsulation of drugs. Int J Pharm 2002; 242: 121-128.