DHA-mediated enhancement of TRAIL-induced apoptosis in colon cancer cells is associated with engagement of mitochondria and specific alterations in sphingolipid metabolism

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 9, 2014, Pages 1308-1317

  Skender, Belma ^a,b   Hofmanová, Jiřina ^a,b   Slavík, Josef ^c   Jelínková, Iva ^a,b   Machala, Miroslav ^c   Moyer, Mary Pat ^d   Kozubík, Alois ^a,b   Hyrslova Vaculova, Alena ^a  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

^b MASARYK UNIVERSITY   (Czech Republic)

^c VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^d INCELL Corporation LLC ^*  (United States)

Author keywords

Apoptosis; Colon cancer; Docosahexaenoic acid; Lipid metabolism; TRAIL

Indexed keywords

CERAMIDE; CYTOCHROME C; DOCOSAHEXAENOIC ACID; INHIBITOR OF APOPTOSIS PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL XL; PROTEIN MCL 1; SPHINGOLIPID; SPHINGOMYELIN; SPHINGOSINE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ADHERENT CELL; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL LINE; CELL CYCLE S PHASE; CELL DEATH; CELL LEVEL; COLON CANCER; CONTROLLED STUDY; CYTOTOXICITY; DNA CONTENT; G1 PHASE CELL CYCLE CHECKPOINT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LIPID METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY;

APOPTOSIS; COLON CANCER; DOCOSAHEXAENOIC ACID; LIPID METABOLISM; TRAIL;

ADENOCARCINOMA; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; COLONIC NEOPLASMS; CYTOCHROMES C; DOCOSAHEXAENOIC ACIDS; DRUG SYNERGISM; EIF-2 KINASE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSCRIPTION FACTOR CHOP; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84903828689     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.06.005     Document Type: Article

References (59)

1. S.C. Mills, A.C. Windsor, and S.C. Knight The potential interactions between polyunsaturated fatty acids and colonic inflammatory processes Clin. Exp. Immunol. 142 2005 216 228 (Pubitemid 41565236)
2. C.G. Candela, L.M.B. Lopez, and V.L. Kohen Importance of a balanced omega 6/omega 3 ratio for the maintenance of health. Nutritional recommendations Nutr. Hosp. 26 2011 323 329
3. I.M. Berquin, I.J. Edwards, and Y.Q. Chen Multi-targeted therapy of cancer by omega-3 fatty acids Cancer Lett. 269 2008 363 377
4. R.S. Chapkin, M.Y. Hong, Y.Y. Fan, L.A. Davidson, L.M. Sanders, C.E. Henderson, R. Barhoumi, R.C. Burghardt, N.D. Turner, and J.R. Lupton Dietary n-3 PUFA alter colonocyte mitochondrial membrane composition and function Lipids 37 2002 193 199 (Pubitemid 34213986)
5. S. Gabriella Calviello Serini, Dietary Omega-3 Polyunsaturated Fatty Acids and Cancer 2010 Springer Netherlands Netherlands
6. S. Kim, D.P. Sandler, J. Galanko, C. Martin, and R.S. Sandler Intake of polyunsaturated fatty acids and distal large bowel cancer risk in whites and African Americans Am. J. Epidemiol. 171 2010 969 979
7. L.C. Chiu, E.Y. Wong, and V.E. Ooi Docosahexaenoic acid from a cultured microalga inhibits cell growth and induces apoptosis by upregulating Bax/Bcl-2 ratio in human breast carcinoma MCF-7 cells Ann. N. Y. Acad. Sci. 1030 2004 361 368 (Pubitemid 40378934)
8. N. Habermann, A. Schon, E.K. Lund, and M. Glei Fish fatty acids alter markers of apoptosis in colorectal adenoma and adenocarcinoma cell lines but fish consumption has no impact on apoptosis-induction ex vivo Apoptosis 15 2010 621 630
9. J.E. Slagsvold, C.H. Pettersen, G.L. Storvold, T. Follestad, H.E. Krokan, and S.A. Schonberg DHA alters expression of target proteins of cancer therapy in chemotherapy resistant SW620 colon cancer cells Nutr. Cancer 62 2010 611 621
10. G. Calviello, F. Resci, S. Serini, E. Piccioni, A. Toesca, A. Boninsegna, G. Monego, F.O. Ranelletti, and P. Palozza Docosahexaenoic acid induces proteasome-dependent degradation of beta-catenin, down-regulation of survivin and apoptosis in human colorectal cancer cells not expressing COX-2 Carcinogenesis 28 2007 1202 1209 (Pubitemid 47062678)
11. A. Giros, M. Grzybowski, V.R. Sohn, E. Pons, J. Fernandez-Morales, R.M. Xicola, P. Sethi, J. Grzybowski, A. Goel, C.R. Boland, M.A. Gassull, and X. Llor Regulation of colorectal cancer cell apoptosis by the n-3 polyunsaturated fatty acids Docosahexaenoic and Eicosapentaenoic Cancer Prev. Res. (Phila) 2 2009 732 742
12. J. Hofmanová, A. Vaculová, Z. Koubková, M. Hyžďalová, and A. Kozubík Human fetal colon cells and colon cancer cells respond differently to butyrate and PUFAs Mol. Nutr. Food Res. 53 Suppl. 1 2009 S102 S113
13. Y. Ng, R. Barhoumi, R.B. Tjalkens, Y.Y. Fan, S. Kolar, N. Wang, J.R. Lupton, and R.S. Chapkin The role of docosahexaenoic acid in mediating mitochondrial membrane lipid oxidation and apoptosis in colonocytes Carcinogenesis 26 2005 1914 1921 (Pubitemid 41631264)
14. S. Oyadomari, and M. Mori Roles of CHOP/GADD153 in endoplasmic reticulum stress Cell Death Differ. 11 2004 381 389 (Pubitemid 38489416)
15. C.H. Jakobsen, G.L. Storvold, H. Bremseth, T. Follestad, K. Sand, M. Mack, K.S. Olsen, A.G. Lundemo, J.G. Iversen, H.E. Krokan, and S.A. Schonberg DHA induces ER stress and growth arrest in human colon cancer cells: associations with cholesterol and calcium homeostasis J. Lipid Res. 49 2008 2089 2100
16. J.L. Toit-Kohn, L. Louw, and A.M. Engelbrecht Docosahexaenoic acid induces apoptosis in colorectal carcinoma cells by modulating the PI3 kinase and p38 MAPK pathways J. Nutr. Biochem. 20 2009 106 114
17. A.J. Cockbain, G.J. Toogood, and M.A. Hull Omega-3 polyunsaturated fatty acids for the treatment and prevention of colorectal cancer Gut 61 2012 135 149
18. B. Skender, A.H. Vaculová, and J. Hofmanová Docosahexaenoic fatty acid (DHA) in the regulation of colon cell growth and cell death: a review Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 156 2012 186 199
19. W.E. Hardman, M.P. Moyer, and I.L. Cameron Consumption of an omega-3 fatty acids product, INCELL AAFA, reduced side-effects of CPT-11 (irinotecan) in mice Br. J. Cancer 86 2002 983 988 (Pubitemid 34271037)
20. J. Hofmanová, A. Vaculová, and A. Kozubík Polyunsaturated fatty acids sensitize human colon adenocarcinoma HT-29 cells to death receptor-mediated apoptosis Cancer Lett. 218 2005 33 41 (Pubitemid 40082699)
21. A. Vaculová, J. Hofmanová, L. Anděra, and A. Kozubík TRAIL and docosahexaenoic acid cooperate to induce HT-29 colon cancer cell death Cancer Lett. 229 2005 43 48 (Pubitemid 41262538)
22. S.R. Wiley, K. Schooley, P.J. Smolak, W.S. Din, C.P. Huang, J.K. Nicholl, G.R. Sutherland, T.D. Smith, C. Rauch, and C.A. Smith Identification and characterization of a new member of the TNF family that induces apoptosis Immunity 3 1995 673 682 (Pubitemid 26091143)
23. R.M. Pitti, S.A. Marsters, S. Ruppert, C.J. Donahue, A. Moore, and A. Ashkenazi Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family J. Biol. Chem. 271 1996 12687 12690 (Pubitemid 26175834)
24. L.Y. Dimberg, C.K. Anderson, R. Camidge, K. Behbakht, A. Thorburn, and H.L. Ford On the TRAIL to successful cancer therapy? Predicting and counteracting resistance against TRAIL-based therapeutics Oncogene 32 2013 1341 1350
25. L. Galligan, D.B. Longley, M. McEwan, T.R. Wilson, K. McLaughlin, and P.G. Johnston Chemotherapy and TRAIL-mediated colon cancer cell death: the roles of p53, TRAIL receptors, and c-FLIP Mol. Cancer Ther. 4 2005 2026 2036 (Pubitemid 43056986)
26. S. Fulda, E. Meyer, and K.M. Debatin Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression Oncogene 21 2002 2283 2294 (Pubitemid 34407288)
27. A. Vaculová, J. Hofmanová, J. Zatloukalová, and A. Kozubík Differences in TRAIL-induced changes of Mcl-1 expression among distinct human colon epithelial cell lines Exp. Cell Res. 315 2009 3259 3266
28. M.S. Lippa, L.D. Strockbine, T.T. Le, D.G. Branstetter, C.A. Strathdee, and P.M. Holland Expression of anti-apoptotic factors modulates Apo2L/TRAIL resistance in colon carcinoma cells Apoptosis 12 2007 1465 1478 (Pubitemid 46988283)
29. H. LeBlanc, D. Lawrence, E. Varfolomeev, K. Totpal, J. Morlan, P. Schow, S. Fong, R. Schwall, D. Sinicropi, and A. Ashkenazi Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax Nat. Med. 8 2002 274 281 (Pubitemid 34250106)
30. T.E. Fandy, S. Shankar, and R.K. Srivastava Smac/DIABLO enhances the therapeutic potential of chemotherapeutic drugs and irradiation, and sensitizes TRAIL-resistant breast cancer cells Mol. Cancer 7 2008 60
31. C. Voelkel-Johnson, Y.A. Hannun, and A. El-Zawahry Resistance to TRAIL is associated with defects in ceramide signaling that can be overcome by exogenous C6-ceramide without requiring down-regulation of cellular FLICE inhibitory protein Mol. Cancer Ther. 4 2005 1320 1327
32. M.P. Moyer, L.A. Manzano, R.L. Merriman, J.S. Stauffer, and L.R. Tanzer NCM460, a normal human colon mucosal epithelial cell line In Vitro Cell. Dev. Biol. Anim. 32 1996 315 317
33. O. Vondalová Blanářová, I. Jelínková, A. Szoor, B. Skender, K. Souček, V. Horváth, A. Vaculová, L. Anděra, P. Sova, J. Szollosi, J. Hofmanová, G. Vereb, and A. Kozubík Cisplatin and a potent platinum(IV) complex-mediated enhancement of TRAIL-induced cancer cells killing is associated with modulation of upstream events in the extrinsic apoptotic pathway Carcinogenesis 32 2011 42 51
34. S. Huerta, J.H. Heinzerling, Y.M. Anguiano-Hernandez, S. Huerta-Yepez, J. Lin, D. Chen, B. Bonavida, and E.H. Livingston Modification of gene products involved in resistance to apoptosis in metastatic colon cancer cells: roles of Fas, Apaf-1, NFkappaB, IAPs, Smac/DIABLO, and AIF J. Surg. Res. 142 2007 184 194 (Pubitemid 47277413)
35. M. Hornle, N. Peters, B. Thayaparasingham, H. Vorsmann, H. Kashkar, and D. Kulms Caspase-3 cleaves XIAP in a positive feedback loop to sensitize melanoma cells to TRAIL-induced apoptosis Oncogene 30 2011 575 587
36. V.E. Kagan, H.A. Bayir, N.A. Belikova, O. Kapralov, Y.Y. Tyurina, V.A. Tyurin, J. Jiang, D.A. Stoyanovsky, P. Wipf, P.M. Kochanek, J.S. Greenberger, B. Pitt, A.A. Shvedova, and G. Borisenko Cytochrome c/cardiolipin relations in mitochondria: a kiss of death Free Radic. Biol. Med. 46 2009 1439 1453
37. S.M. Watkins, L.C. Carter, and J.B. German Docosahexaenoic acid accumulates in cardiolipin and enhances HT-29 cell oxidant production J. Lipid Res. 39 1998 1583 1588 (Pubitemid 28377921)
38. S.N. Sun, W.D. Jia, H. Chen, J.L. Ma, Y.S. Ge, J.H. Yu, and J.S. Li Docosahexaenoic acid (DHA) induces apoptosis in human hepatocellular carcinoma cells Int. J. Clin. Exp. Pathol. 6 2013 281 289
39. Z.Y. Chen, and N.W. Istfan Docosahexaenoic acid is a potent inducer of apoptosis in HT-29 colon cancer cells Prostaglandins Leukot. Essent. Fatty Acids 63 2000 301 308
40. R. Qadhi, N. Alsaleh, V. Samokhvalov, H. El-Sikhry, J. Bellenger, and J.M. Seubert Differential responses to docosahexaenoic acid in primary and immortalized cardiac cells Toxicol. Lett. 219 2013 288 297
41. L. Walter, and G. Hajnoczky Mitochondria and endoplasmic reticulum: the lethal interorganelle cross-talk J. Bioenerg. Biomembr. 37 2005 191 206 (Pubitemid 41420474)
42. A. Xiong, W. Yu, R. Tiwary, B.G. Sanders, and K. Kline Distinct roles of different forms of vitamin E in DHA-induced apoptosis in triple-negative breast cancer cells Mol. Nutr. Food Res. 56 2012 923 934
43. X.J. Zou, L. Yang, and S.L. Yao Endoplasmic reticulum stress and C/EBP homologous protein-induced Bax translocation are involved in angiotensin II-induced apoptosis in cultured neonatal rat cardiomyocytes Exp. Biol. Med. (Maywood) 237 2012 1341 1349
44. K.D. McCullough, J.L. Martindale, L.O. Klotz, T.Y. Aw, and N.J. Holbrook Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state Mol. Cell. Biol. 21 2001 1249 1259 (Pubitemid 32114973)
45. C. Horbinski, and C.T. Chu Kinase signaling cascades in the mitochondrion: a matter of life or death Free Radic. Biol. Med. 38 2005 2 11 (Pubitemid 39626903)
46. X.Z. Wang, and D. Ron Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase Science 272 1996 1347 1349 (Pubitemid 26199977)
47. M. Wu, K.A. Harvey, N. Ruzmetov, Z.R. Welch, L. Sech, K. Jackson, W. Stillwell, G.P. Zaloga, and R.A. Siddiqui Omega-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway Int. J. Cancer 117 2005 340 348 (Pubitemid 41429556)
48. S. Nemoto, M. Nakamura, Y. Osawa, S. Kono, Y. Itoh, Y. Okano, T. Murate, A. Hara, H. Ueda, Y. Nozawa, and Y. Banno Sphingosine kinase isoforms regulate oxaliplatin sensitivity of human colon cancer cells through ceramide accumulation and Akt activation J. Biol. Chem. 284 2009 10422 10432
49. D.A. Litvak, A.J. Bilchik, and M.C. Cabot Modulators of ceramide metabolism sensitize colorectal cancer cells to chemotherapy: a novel treatment strategy J. Gastrointest. Surg. 7 2003 140 148 (discussion 148) (Pubitemid 36875811)
50. S.A. Morad, M. Schmid, B. Buchele, H.U. Siehl, M. El Gafaary, O. Lunov, T. Syrovets, and T. Simmet A novel semisynthetic inhibitor of the FRB domain of mammalian target of rapamycin blocks proliferation and triggers apoptosis in chemoresistant prostate cancer cells Mol. Pharmacol. 83 2013 531 541
51. T.S. Tirodkar, and C. Voelkel-Johnson Sphingolipids in apoptosis Exp. Oncol. 34 2012 231 242
52. C. von Haefen, T. Wieder, B. Gillissen, L. Storck, V. Graupner, B. Dorken, and P.T. Daniel Ceramide induces mitochondrial activation and apoptosis via a Bax-dependent pathway in human carcinoma cells Oncogene 21 2002 4009 4019 (Pubitemid 34679242)
53. S.A. Novgorodov, Z.M. Szulc, C. Luberto, J.A. Jones, J. Bielawski, A. Bielawska, Y.A. Hannun, and L.M. Obeid Positively charged ceramide is a potent inducer of mitochondrial permeabilization J. Biol. Chem. 280 2005 16096 16105 (Pubitemid 40616734)
54. D. Hartmann, J. Lucks, S. Fuchs, S. Schiffmann, Y. Schreiber, N. Ferreiras, J. Merkens, R. Marschalek, G. Geisslinger, and S. Grosch Long chain ceramides and very long chain ceramides have opposite effects on human breast and colon cancer cell growth Int. J. Biochem. Cell Biol. 44 2012 620 628
55. S. Schiffmann, S. Ziebell, J. Sandner, K. Birod, K. Deckmann, D. Hartmann, S. Rode, H. Schmidt, C. Angioni, G. Geisslinger, and S. Grosch Activation of ceramide synthase 6 by celecoxib leads to a selective induction of C16:0-ceramide Biochem. Pharmacol. 80 2010 1632 1640
56. A.F. Renert, P. Leprince, M. Dieu, J. Renaut, M. Raes, V. Bours, J.P. Chapelle, J. Piette, M.P. Merville, and M. Fillet The proapoptotic C16-ceramide-dependent pathway requires the death-promoting factor Btf in colon adenocarcinoma cells J. Proteome Res. 8 2009 4810 4822
57. N. Marchesini, W. Osta, J. Bielawski, C. Luberto, L.M. Obeid, and Y.A. Hannun Role for mammalian neutral sphingomyelinase 2 in confluence-induced growth arrest of MCF7 cells J. Biol. Chem. 279 2004 25101 25111 (Pubitemid 38756759)
58. T. Sassa, S. Suto, Y. Okayasu, and A. Kihara A shift in sphingolipid composition from C24 to C16 increases susceptibility to apoptosis in HeLa cells Biochim. Biophys. Acta 1821 2012 1031 1037
59. S. White-Gilbertson, T. Mullen, C. Senkal, P. Lu, B. Ogretmen, L. Obeid, and C. Voelkel-Johnson Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells Oncogene 28 2009 1132 1141