Dietary polyunsaturated fatty acids as inducers of apoptosis: Implications for cancer

Apoptosis

Volumn 14, Issue 2, 2009, Pages 135-152

  Serini, Simona ^a   Piccioni, Elisabetta ^a   Merendino, Nicolò ^b   Calviello, Gabriella ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b UNIVERSITY OF TUSCIA   (Italy)

Author keywords

LNA; Apoptosis; CLA; DHA; EPA; ER stress

Indexed keywords

ARACHIDONIC ACID; AZOXYMETHANE; CASPASE 9; CELECOXIB; CLIOQUINOL; CONJUGATED LINOLEIC ACID; DOCOSAHEXAENOIC ACID; FLUOROURACIL; FUMAGILLOL CHLOROACETYLCARBAMATE; GAMMA LINOLENIC ACID; GENISTEIN; GLUCOSE REGULATED PROTEIN 78; ICOSAPENTAENOIC ACID; IMATINIB; METHYLNITROSOUREA; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; POLYUNSATURATED FATTY ACID; PROPOFOL; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN P53; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VEGETABLE OIL;

ALZHEIMER DISEASE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BLADDER CARCINOMA; BREAST CANCER; BREAST CARCINOGENESIS; CANCER GROWTH; CANCER INHIBITION; CANCER REGRESSION; CELL PROLIFERATION; CELL STRAIN HL 60; CELLULAR STRESS RESPONSE; CHEMICAL CARCINOGENESIS; CHRONIC DISEASE; COCULTURE; COLON CANCER; DAIRY PRODUCT; DNA BINDING; ENDOPLASMIC RETICULUM STRESS; FAT INTAKE; FISH; GENE OVEREXPRESSION; GLIOBLASTOMA; GLIOMA; HEART PROTECTION; HUMAN; IN VIVO STUDY; LIPID PEROXIDATION; LIVER CELL CARCINOMA; LIVER PROTECTION; MEAT; NERVE CELL CULTURE; NEUROBLASTOMA; NONHUMAN; OSTEOSARCOMA CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROSTATE CARCINOMA; RETINA MACULA AGE RELATED DEGENERATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VASCULAR SMOOTH MUSCLE; VEGETABLE;

ANIMALS; APOPTOSIS; DIETARY FATS, UNSATURATED; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; FATTY ACIDS, UNSATURATED; HUMANS; NEOPLASMS;

EID: 58849110405     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-008-0298-2     Document Type: Article

References (193)

1. G Calviello S Serini P Palozza 2006 n-3 Polyunsaturated fatty acids as signal transduction modulators and therapeutical agents in cancer Curr Signal Transduct Ther 1 255 271
2. MP Mattson 2000 Apoptosis in neurodegenerative disorders Nat Rev Mol Cell Biol 1 120 129
3. RW Johnstone AJ Frew MJ Smyth 2008 The TRAIL apoptotic pathway in cancer onset, progression and therapy Nat Rev Cancer 8 782 798
4. PC Calder 2008 Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases Mol Nutr Food Res 52 885 897
5. PC Calder 1997 n-3 polyunsaturated fatty acids and cytokine production in health and disease Ann Nutr Metab 41 203 234
6. G Calviello S Serini E Piccioni 2007 n-3 polyunsaturated fatty acids and the prevention of colorectal cancer: molecular mechanisms involved Curr Med Chem 14 3059 3069
7. AP Simopoulos 2003 Essential fatty acids in health and chronic diseases Forum Nutr 56 67 70
8. R Kapoor YS Huang 2006 Gamma linolenic acid: an antiinflammatory omega-6 fatty acid Curr Pharm Biotechnol 7 531 534
9. A Bhattacharya J Banu M Rahman J Causey G Fernandes 2006 Biological effects of conjugated linoleic acids in health and disease J Nutr Biochem 17 789 810
10. Y Cao AT Pearman GA Zimmerman TM McIntyre SM Prescott 2000 Intracellular unesterified arachidonic acid signals apoptosis Proc Natl Acad Sci USA 97 11280 11285
11. RS Chapkin J Seo DN McMurray JR Lupton 2008 Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine Chem Phys Lipids 153 14 23
12. S Serini S Trombino F Oliva E Piccioni G Monego F Resci 2008 Docosahexaenoic acid induces apoptosis in lung cancer cells by increasing MKP-1 and down-regulating p-ERK1/2 and p-p38 expression Apoptosis 13 1172 1183
13. G Calviello F Resci S Serini E Piccioni A Toesca A Boninsegna 2007 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 1202 1209
14. G Calviello F Di Nicuolo S Serini E Piccioni A Boninsegna N Maggiano 2005 Docosahexaenoic acid enhances the susceptibility of human colorectal cancer cells to 5-fluorouracil Cancer Chemother Pharmacol 55 12 20
15. G Calviello F Di Nicuolo S Gragnoli E Piccioni S Serini N Maggiano 2004 n-3 PUFAs reduce VEGF expression in human colon cancer cells modulating the COX-2/PGE2 induced ERK-1 and -2 and HIF-1 alpha induction pathway Carcinogenesis 25 2303 2310
16. G Calviello P Palozza N Maggiano E Piccioni P Franceschelli A Frattucci 1999 Cell proliferation, differentiation, and apoptosis are modified by n-3 polyunsaturated fatty acids in normal colonic mucosa Lipids 34 599 604
17. P Borgeat M Hamberg B Samuelsson 1976 Transformation of arachidonic acid and homo-gamma-linolenic acid by rabbit polymorphonuclear leukocytes. Monohydroxy acids from novel lipoxygenases J Biol Chem 251 7816 7820
18. LS Harbige 2003 Fatty acids, the immune response, and autoimmunity: a question of n-6 essentiality and the balance between n-6 and n-3 Lipids 38 323 341
19. WP Leary KM Robinson J Booyens N Dippenaar 1982 Some effects of gamma-linolenic acid on cultured human oesophageal carcinoma cells S Afr Med J 62 681 683
20. ME Bégin UN Das G Ells DF Horrobin 1985 Selective killing of human cancer cells by polyunsaturated fatty acids Prostaglandins Leukot Med 19 177 186
21. PS Sagar UN Das 1995 Cytotoxic action of cis-unsaturated fatty acids on human cervical carcinoma (HeLa) cells in vitro Prostaglandins Leukot Essent Fat Acids 53 287 299
22. UN Das 2006 Tumoricidal and anti-angiogenic actions of gamma-linolenic acid and its derivatives Curr Pharm Biotechnol 7 457 466
23. UN Das 1991 Tumoricidal action of cis-unsaturated fatty acids and their relationship to free radicals and lipid peroxidation Cancer Lett 56 235 243
24. X Kong H Ge L Hou L Shi Z Liu 2006 Induction of apoptosis in K562/ADM cells by gamma-linolenic acid involves lipid peroxidation and activation of caspase-3 Chem Biol Interact 162 140 148
25. FL Chung J Pan S Choudhury R Roy W Hu MS Tang 2003 Formation of trans-4-hydroxy-2-nonenal- and other enal-derived cyclic DNA adducts from omega-3 and omega-6 polyunsaturated fatty acids and their roles in DNA repair and human p53 gene mutation Mutat Res 531 25 36
26. JA Menendez L Vellon R Colomer R Lupu 2005 Effect of γ-linolenic acid on the transcriptional activity of the Her-2/neu (erbB-2) oncogene J Natl Cancer Inst 97 1611 1615
27. JA Menendez M del Mar Barbacid S Montero E Sevilla E Escrich M Solanas 2001 Effects of gamma-linolenic acid and oleic acid on paclitaxel cytotoxicity in human breast cancer cells Eur J Cancer 37 402 413
28. A Colquhoun 1998 Induction of apoptosis by polyunsaturated fatty acids and its relationship to fatty acid inhibition of carnitine palmitoyltransferase I activity in Hep2 cells Biochem Mol Biol Int 45 331 336
29. PS Sagar UN Das R Koratkar G Ramesh M Padma GS Kumar 1992 Cytotoxic action of cis-unsaturated fatty acids on human cervical carcinoma (HeLa) cells: relationship to free radicals, and lipid peroxidation and its modulation by calmodulin antagonists Cancer Lett 63 189 198
30. JC Seegers M de Kock ML Lottering CJ Grobler DH van Papendorp Y Shou 1997 Effects of gamma-linolenic acid and arachidonic acid on cell cycle progression and apoptosis induction in normal and transformed cells Prostaglandins Leukot Essent Fat Acids 56 271 280
31. T Mainou-Fowler SJ Proctor AM Dickinson 2001 Gamma-linolenic acid induces apoptosis in B-chronic lymphocytic leukaemia cells in vitro Leuk Lymphoma 40 393 403
32. RC Gillis BJ Daley BL Enderson MD Karlstad 2004 Inhibition of 5-lipoxygenase induces cell death in anti-inflammatory fatty acid-treated HL-60 cells JPEN J Parenter Enter Nutr 28 308 314
33. KC Jung CH Park YH Hwang HS Rhee JH Lee HK Kim 2006 Fatty acids, inhibitors for the DNA binding of c-Myc/Max dimer, suppress proliferation and induce apoptosis of differentiated HL-60 human leukemia cell Leukemia 20 122 127
34. RC Maia CA Culver SM Laster 2006 Evidence against calcium as a mediator of mitochondrial dysfunction during apoptosis induced by arachidonic acid and other free fatty acids J Immunol 177 6398 6404
35. M Artwohl M Roden W Waldhäusl A Freudenthaler SM Baumgartner-Parzer 2004 Free fatty acids trigger apoptosis and inhibit cell cycle progression in human vascular endothelial cells FASEB J 18 146 148
36. ME Surette IL Koumenis MB Edens KM Tramposch FH Chilton 2003 Inhibition of leukotriene synthesis, pharmacokinetics, and tolerability of a novel dietary fatty acid formulation in healthy adult subjects Clin Ther 25 948 971
37. HA Leaver SB Wharton HS Bell IM Leaver-Yap IR Whittle 2002 Highly unsaturated fatty acid induced tumour regression in glioma pharmacodynamics and bioavailability of gamma linolenic acid in an implantation glioma model: effects on tumour biomass, apoptosis and neuronal tissue histology Prostaglandins Leukot Essent Fat Acids 67 283 292
38. HA Leaver HS Bell MT Rizzo JW Ironside A Gregor SB Wharton 2002 Antitumour and pro-apoptotic actions of highly unsaturated fatty acids in glioma Prostaglandins Leukot Essent Fat Acids 66 19 29
39. KL Ramos A Colquhoun 2003 Protective role of glucose-6-phosphate dehydrogenase activity in the metabolic response of C6 rat glioma cells to polyunsaturated fatty acid exposure Glia 43 149 166
40. A Colquhoun RI Schumacher 2001 Modifications in mitochondrial metabolism and ultrastructure and their relationship to tumour growth inhibition by gamma-linolenic acid Mol Cell Biochem 218 13 20
41. JM Griinari BA Corl SH Lacy PY Chouinard KV Nurmela DE Bauman 2000 Conjugated linoleic acid is synthesized endogenously in lactating dairy cows by Delta(9)-desaturase J Nutr 130 2285 2291
42. SF Chin W Liu JM Storkson YL Ha MW Pariza 1992 Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens J Food Compon Anal 5 185 197
43. B Majumder KW Wahle S Moir A Schofield SN Choe A Farquharson 2002 Conjugated linoleic acids (CLAs) regulate the expression of key apoptotic genes in human breast cancer cells FASEB J 16 1447 1449
44. A Miglietta F Bozzo C Bocca L Gabriel A Trombetta S Belotti 2006 Conjugated linoleic acid induces apoptosis in MDA-MB-231 breast cancer cells through ERK/MAPK signalling and mitochondrial pathway Cancer Lett 234 149 157
45. A Miller C Stanton R Devery 2002 Cis 9, trans 11- and trans 10, cis 12-conjugated linoleic acid isomers induce apoptosis in cultured SW480 cells Anticancer Res 22 3879 3887
46. F Beppu M Hosokawa L Tanaka H Kohno T Tanaka K Miyashita 2006 Potent inhibitory effect of trans9, trans11 isomer of conjugated linoleic acid on the growth of human colon cancer cells J Nutr Biochem 17 830 836
47. A Cimini L Cristiano S Colafarina E Benedetti S Di Loreto C Festuccia 2005 PPARgamma-dependent effects of conjugated linoleic acid on the human glioblastoma cell line (ADF) Int J Cancer 117 923 933
48. M Yamasaki Y Miyamoto H Chujo K Nishiyama H Tachibana K Yamada 2005 Trans10, cis12-conjugated linoleic acid induces mitochondria-related apoptosis and lysosomal destabilization in rat hepatoma cells Biochim Biophys Acta 1735 176 184
49. JJ Ochoa AJ Farquharson I Grant LE Moffat SD Heys KW Wahle 2004 Conjugated linoleic acids (CLAs) decrease prostate cancer cell proliferation: different molecular mechanisms for cis-9, trans-11 and trans-10, cis-12 isomers Carcinogenesis 25 1185 1191
50. JR Liu BQ Chen YM Yang XL Wang YB Xue YM Zheng 2002 Effect of apoptosis on gastric adenocarcinoma cell line SGC-7901 induced by cis-9, trans-11-conjugated linoleic acid World J Gastroenterol 8 999 1004
51. YS Kim RM Cerbo CK Hah KN Bahn JO Kim YL Ha 2008 Growth inhibition of osteosarcoma cell MG-63 by a mixture of trans, trans conjugated linoleic acid isomers: possible mechanistic actions J Food Sci 73 T7 T15
52. G Muzio M Maggiora M Oraldi A Trombetta RA Canuto 2007 PPARalpha and PP2A are involved in the proapoptotic effect of conjugated linoleic acid on human hepatoma cell line SK-HEP-1 Int J Cancer 121 2395 2401
53. L Ou Y Wu C Ip X Meng YC Hsu MM Ip 2008 Apoptosis induced by t10,c12-conjugated linoleic acid is mediated by an atypical endoplasmic reticulum stress response J Lipid Res 49 985 994
54. E Szegezdi SE Logue AM Gorman A Samali 2006 Mediators of endoplasmic reticulum stress-induced apoptosis EMBO Rep 7 880 885
55. C Xu B Bailly-Maitre JC Reed 2005 Endoplasmic reticulum stress: cell life and death decisions J Clin Invest 115 2656 2664
56. M Boyce J Yuan 2006 Cellular response to endoplasmic reticulum stress: a matter of life or death Cell Death Differ 13 363 373
57. DG Breckenridge M Germain JP Mathai M Nguyen GC Shore 2003 Regulation of apoptosis by endoplasmic reticulum pathways Oncogene 22 8608 8618
58. HP Harding Y Zhang H Zeng I Novoa PD Lu M Calfon 2003 An integrated stress response regulates amino acid metabolism and resistance to oxidative stress Mol Cell 11 619 633
59. H Zinszner M Kuroda X Wang N Batchvarova RT Lightfoot H Remotti 1998 CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum Genes Dev 12 982 995
60. NN Iwakoshi AH Lee LH Glimcher 2003 The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response Immunol Rev 194 29 38
61. H Nishitoh M Saitoh Y Mochida K Takeda H Nakano M Rothe 1998 ASK1 is essential for JNK/SAPK activation by TRAF2 Mol Cell 2 389 395
62. M Matsumoto M Minami K Takeda Y Sakao S Akira 1996 Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells FEBS Lett 395 143 147
63. E Szegezdi U Fitzgerald A Samali 2003 Caspase-12 and ER-stress-mediated apoptosis: the story so far Ann NY Acad Sci 1010 186 194
64. L Romero-Ramirez H Cao D Nelson E Hammond AH Lee H Yoshida 2004 XBP1 is essential for survival under hypoxic conditions and is required for tumor growth Cancer Res 64 5943 5947
65. DR Fels C Koumenis 2006 The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth Cancer Biol Ther 5 723 728
66. H Chujo M Yamasaki S Nou N Koyanagi H Tachibana K Yamada 2003 Effect of conjugated linoleic acid isomers on growth factor-induced proliferation of human breast cancer cells Cancer Lett 202 81 87
67. EJ Kim PE Holthuizen HS Park YL Ha KC Jung JH Park 2002 Trans-10, cis-12-conjugated linoleic acid inhibits Caco-2 colon cancer cell growth Am J Physiol Gastrointest Liver Physiol 283 G357 G367
68. HJ Cho WK Kim JI Jung EJ Kim SS Lim DY Kwon 2005 Trans-10, cis-12, not cis-9, trans-11, conjugated linoleic acid decreases ErbB3 expression in HT-29 human colon cancer cells World J Gastroenterol 11 5142 5150
69. L Ou C Ip B Lisafeld MM Ip 2007 Conjugated linoleic acid induces apoptosis of murine mammary tumor cells via Bcl-2 loss Biochem Biophys Res Commun 356 1044 1049
70. LS Wang YW Huang S Liu P Yan YC Lin 2008 Conjugated linoleic acid induces apoptosis through estrogen receptor alpha in human breast tissue BMC Cancer 8 208 221
71. SH Lee K Yamaguchi JS Kim TE Eling S Safe Y Park 2006 Conjugated linoleic acid stimulates an anti-tumorigenic protein NAG-1 in an isomer specific manner Carcinogenesis 27 972 981
72. NS Kelley NE Hubbard KL Erickson 2007 Conjugated linoleic acid isomers and cancer J Nutr 137 2599 2607
73. M Maggiora M Bologna MP Cerù L Possati A Angelucci A Cimini 2004 An overview of the effect of linoleic and conjugated-linoleic acids on the growth of several human tumor cell lines Int J Cancer 112 909 919
74. AP Nugent HM Roche EJ Noone A Long DK Kelleher MJ Gibney 2005 The effects of conjugated linoleic acid supplementation on immune function in healthy volunteers Eur J Clin Nutr 59 742 750
75. V Mougios A Matsakas A Petridou S Ring A Sagredos A Melissopoulou 2001 Effect of supplementation with conjugated linoleic acid on human serum lipids and body fat J Nutr Biochem 12 585 594
76. HS Park JH Ryu YL Ha JH Park 2001 Dietary conjugated linoleic acid (CLA) induces apoptosis of colonic mucosa in 1,2-dimethylhydrazine-treated rats: a possible mechanism of the anticarcinogenic effect by CLA Br J Nutr 86 549 555
77. HS Park CS Chun S Kim YL Ha JH Park 2006 Dietary trans-10, cis-12 and cis-9, trans-11 conjugated linoleic acids induce apoptosis in the colonic mucosa of rats treated with 1,2-dimethylhydrazine J Med Food 9 22 27
78. J Rajakangas S Basu I Salminen M Mutanen 2003 Adenoma growth stimulation by the trans-10, cis-12 isomer of conjugated linoleic acid (CLA) is associated with changes in mucosal NF-kappaB and cyclin D1 protein levels in the Min mouse J Nutr 133 1943 1948
79. C Ip Y Dong MM Ip S Banni G Carta E Angioni 2002 Conjugated linoleic acid isomers and mammary cancer prevention Nutr Cancer 43 52 58
80. NE Hubbard D Lim KL Erickson 2003 Effect of separate conjugated linoleic acid isomers on murine mammary tumorigenesis Cancer Lett 190 13 19
81. MM Ip SO McGee PA Masso-Welch C Ip X Meng L Ou 2007 The t10,c12 isomer of conjugated linoleic acid stimulates mammary tumorigenesis in transgenic mice over-expressing erbB2 in the mammary epithelium Carcinogenesis 28 1269 1276
82. DJ Slamon GM Clark SG Wong WJ Levin A Ullrich WL McGuire 1987 Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene Science 235 177 182
83. X Meng SF Shoemaker SO McGee MM Ip 2008 t10,c12-Conjugated linoleic acid stimulates mammary tumor progression in Her2/ErbB2 mice through activation of both proliferative and survival pathways Carcinogenesis 29 1013 1021
84. Y Yasui R Suzuki H Kohno S Miyamoto F Beppu M Hosokawa 2007 9trans, 11trans conjugated linoleic acid inhibits the development of azoxymethane-induced colonic aberrant crypt foci in rats Nutr Cancer 59 82 91
85. N Tsuboyama-Kasaoka M Takahashi K Tanemura HJ Kim T Tange H Okuyama 2000 Conjugated linoleic acid supplementation reduces adipose tissue by apoptosis and develops lipodystrophy in mice Diabetes 49 1534 1542
86. HS Yun SH Do WI Jeong HJ Yang DW Yuan IH Hong 2008 Cytotoxic effects of the conjugated linoleic acid isomers t10c12, c9t11-CLA and mixed form on rat hepatic stellate cells and CCl4-induced hepatic fibrosis J Nutr Biochem 19 175 183
87. S Toomey B Harhen HM Roche D Fitzgerald O Belton 2006 Profound resolution of early atherosclerosis with conjugated linoleic acid Atherosclerosis 187 40 49
88. MW Pariza Y Park ME Cook 2000 Mechanisms of action of conjugated linoleic acid: evidence and speculation Proc Soc Exp Biol Med 223 8 13
89. Y Park JM Storkson KJ Albright W Liu MW Pariza 1999 Evidence that trans10, cis12 isomer of conjugated linoleic acid induces body composition changes in mice Lipids 34 235 241
90. JL Miner CA Cederberg MK Nielsen X Chen CA Baile 2001 Conjugated linoleic acid (CLA), body fat, and apoptosis Obes Res 9 129 134
91. M Evans C Geigerman J Cook L Curtis B Kuebler M McIntosh 2000 Conjugated linoleic acid suppresses triglyceride accumulation and induces apoptosis in 3T3-L1 preadipocytes Lipids 35 899 910
92. KM Hargrave BJ Meyer C Li MJ Azain CA Baile JL Miner 2004 Influence of dietary conjugated linoleic acid and fat source on body fat and apoptosis in mice Obes Res 12 1435 1444
93. M Pinzani P Gentilini 1999 Biology of hepatic stellate cells and their possible relevance in the pathogenesis of portal hypertension in cirrhosis Semin Liver Dis 19 397 410
94. E Stachowska M Baśkiewicz-Masiuk V Dziedziejko I Gutowska I Baranowska-Bosiacka M Marchlewicz 2008 Conjugated linoleic acid increases intracellular ROS synthesis and oxygenation of arachidonic acid in macrophages Nutrition 24 187 199
95. Y Yu PH Correll JP Vanden Heuvel 2002 Conjugated linoleic acid decreases production of pro-inflammatory products in macrophages: evidence for a PPAR gamma-dependent mechanism Biochim Biophys Acta 15 89 99
96. TG Brock M Peters-Golden 2007 Activation and regulation of cellular eicosanoid biosynthesis Sci World J 7 1273 1284
97. SP Khanapure DS Garvey DR Janero LG Letts 2007 Eicosanoids in inflammation: biosynthesis, pharmacology, and therapeutic frontiers Curr Top Med Chem 7 311 340
98. D Wang RN Dubois 2006 Prostaglandins and cancer Gut 55 115 122
99. DP Rose JM Connolly 2000 Regulation of tumor angiogenesis by dietary fatty acids and eicosanoids Nutr Cancer 37 119 127
100. A González-Périz J Clària 2007 New approaches to the modulation of the cyclooxygenase-2 and 5-lipoxygenase pathways Curr Top Med Chem 7 297 309
101. AM Monjazeb KP High A Connoy LS Hart C Koumenis FH Chilton 2006 Arachidonic acid-induced gene expression in colon cancer cells Carcinogenesis 27 1950 1960
102. W Dempke C Rie A Grothey HJ Schmoll 2001 Cyclooxygenase-2: a novel target for cancer chemotherapy? J Cancer Res Clin Oncol 127 411 417
103. S Gupta M Srivastava N Ahmad K Sakamoto DG Bostwick H Mukhtar 2001 Lipoxygenase-5 is overexpressed in prostate adenocarcinoma Cancer 91 737 743
104. R Pérez X Matabosch A Llebaria MA Balboa J Balsinde 2006 Blockade of arachidonic acid incorporation into phospholipids induces apoptosis in U937 promonocytic cells J Lipid Res 47 484 491
105. KM Fang WL Chang SM Wang MJ Su ML Wu 2008 Arachidonic acid induces both Na+ and Ca2+ entry resulting in apoptosis J Neurochem 104 1177 1189
106. L Scorrano D Penzo V Petronilli F Pagano P Bernardi 2001 Arachidonic acid causes cell death through the mitochondrial permeability transition. Implications for tumor necrosis factor-alpha apoptotic signaling J Biol Chem 276 12035 12040
107. D Dymkowska J Szczepanowska MR Wieckowski L Wojtczak 2006 Short-term and long-term effects of fatty acids in rat hepatoma AS-30D cells: the way to apoptosis Biochim Biophys Acta 1763 152 163
108. S Jayadev CM Linardic YA Hannun 1994 Identification of arachidonic acid as a mediator of sphingomyelin hydrolysis in response to tumor necrosis factor alpha J Biol Chem 269 5757 5763
109. R Vento N D'Alessandro M Giuliano M Lauricella M Carabillò G Tesoriere 2000 Induction of apoptosis by arachidonic acid in human retinoblastoma Y79 cells: involvement of oxidative stress Exp Eye Res 70 503 517
110. PC Calder 2004 n-3 Fatty acids and cardiovascular disease: evidence explained and mechanisms explored Clin Sci (Lond) 107 1 11
111. JM Alessandri P Guesnet S Vancassel P Astorg I Denis B Langelier 2004 Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life Reprod Nutr Dev 44 509 538
112. JW Sijben PC Calder 2007 Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease Proc Nutr Soc 66 237 259
113. PC Calder 2006 n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases Am J Clin Nutr 83 1505S 1519S
114. KC Switzer DN McMurray RS Chapkin 2004 Effects of dietary n-3 polyunsaturated fatty acids on T-cell membrane composition and function Lipids 39 1163 1170
115. M Hirafuji T Machida N Hamaue M Minami 2003 Cardiovascular protective effects of n-3 polyunsaturated fatty acids with special emphasis on docosahexaenoic acid J Pharmacol Sci 92 308 316
116. C Boudrault RP Bazinet DW Ma 2009 Experimental models and mechanisms underlying the protective effects of n-3 polyunsaturated fatty acids in Alzheimer's disease J Nutr Biochem 20 1 10
117. CA Pfrommer W Erl PC Weber 2006 Docosahexaenoic acid induces ciap1 mRNA and protects human endothelial cells from stress-induced apoptosis Am J Physiol Heart Circ Physiol 290 H2178 H2186
118. H Heimli C Giske S Naderi CA Drevon K Hollung 2002 Eicosapentaenoic acid promotes apoptosis in Ramos cells via activation of caspase-3 and -9 Lipids 37 797 802
119. N Danbara T Yuri M Tsujita-Kyutoku M Sato H Senzaki H Takada 2004 Conjugated docosahexaenoic acid is a potent inducer of cell cycle arrest and apoptosis and inhibits growth of colo 201 human colon cancer cells Nutr Cancer 50 71 79
120. X Llor E Pons A Roca M Alvarez J Mañé F Fernández- Bañares 2003 The effects of fish oil, olive oil, oleic acid and linoleic acid on colorectal neoplastic processes Clin Nutr 22 71 79
121. BA Narayanan NK Narayanan BS Reddy 2001 Docosahexaenoic acid regulated genes and transcription factors inducing apoptosis in human colon cancer cells Int J Oncol 19 1255 1262
122. K Arita H Kobuchi T Utsumi Y Takehara J Akiyama AA Horton 2001 Mechanism of apoptosis in HL-60 cells induced by n-3 and n-6 polyunsaturated fatty acids Biochem Pharmacol 62 821 828
123. J Hofmanová A Vaculová A Kozubík 2005 (DHA and AA) Polyunsaturated fatty acids sensitize human colon adenocarcinoma HT-29 cells to death receptor-mediated apoptosis Cancer Lett 218 33 41
124. M Yano E Kishida M Iwasaki S Kojo Y Masuzawa 2000 Docosahexaenoic acid and vitamin E can reduce human monocytic U937 cell apoptosis induced by tumor necrosis factor J Nutr 130 1095 1101
125. M Wu KA Harvey N Ruzmetov ZR Welch L Sech K Jackson 2005 Omega-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway Int J Cancer 117 340 348
126. RA Siddiqui LJ Jenski KA Harvey JD Wiesehan W Stillwell GP Zaloga 2003 Cell-cycle arrest in Jurkat leukaemic cells: a possible role for docosahexaenoic acid Biochem J 371 621 629
127. CA Jolly YH Jiang RS Chapkin DN McMurray 1997 Dietary [n-3] polyunsaturated fatty acids suppress murine lymphoproliferation, interleukin-2 secretion, and the formation of diacylglycerol and ceramide J Nutr 127 37 43
128. DN McMurray CA Jolly RS Chapkin 2000 Effects of dietary n-3 fatty acids on T-cell activation and T-cell receptor-mediated signalling in a murine model J Infect Dis 182 S103 S107
129. PD Schley HB Jijon LE Robinson CJ Field 2005 Mechanisms of omega-3 fatty acid-induced growth inhibition in MDA-MB-231 human breast cancer cells Breast Cancer Res Treat 92 187 195
130. PD Schley DN Brindley CJ Field 2007 (n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells J Nutr 137 548 553
131. H Sun IM Berquin RT Owens JT O'Flaherty IJ Edwards 2008 Peroxisome proliferator-activated receptor gamma-mediated up-regulation of syndecan-1 by n-3 fatty acids promotes apoptosis of human breast cancer cells Cancer Res 68 2912 2919
132. ZY Chen NW Istfan 2000 Docosahexaenoic acid is a potent inducer of apoptosis in HT-29 colon cancer cells Prostaglandins Leukot Essent Fat Acids 63 301 308
133. MY Hong RS Chapkin R Barhoumi RC Burghardt ND Turner CE Henderson 2002 Fish oil increases mitochondrial phospholipid unsaturation, upregulating reactive oxygen species and apoptosis in rat colonocytes Carcinogenesis 23 1919 1925
134. BA Narayanan NK Narayanan D Desai B Pittman BS Reddy 2004 Effects of a combination of docosahexaenoic acid and 1,4-phenylene bis(methylene) selenocyanate on cyclooxygenase 2, inducible nitric oxide synthase and beta-catenin pathways in colon cancer cells Carcinogenesis 25 2443 2449
135. OC Trifan T Hla 2003 Cyclooxygenase-2 modulates cellular growth and promotes tumorigenesis J Cell Mol Med 7 207 222
136. G Hawcroft M D'Amico C Albanese AF Markham RG Pestell MA Hull 2002 Indomethacin induces differential expression of beta-catenin, gamma-catenin and T-cell factor target genes in human colorectal cancer cells Carcinogenesis 23 107 114
137. H Li L Liu ML David CM Whitehead M Chen JR Fetter 2002 Pro-apoptotic actions of exisulind and CP461 in SW480 colon tumor cells involve beta-catenin and cyclin D1 down-regulation Biochem Pharmacol 64 1325 1336
138. CH Jakobsen GL Størvold H Bremseth T Follestad K Sand M Mack 2008 DHA induces ER stress and growth arrest in human colon cancer cells: associations with cholesterol and calcium homeostasis J Lipid Res 49 2089 2100
139. E Diakogiannaki NG Morgan 2008 Differential regulation of the ER stress response by long-chain fatty acids in the pancreatic beta-cell Biochem Soc Trans 36 959 962
140. E Karaskov C Scott L Zhang T Teodoro M Ravazzola A Volchuk 2006 Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis Endocrinology 147 3398 3407
141. T Ota C Gayet HN Ginsberg 2008 Inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress in rodents J Clin Invest 118 316 332
142. HS Finstad MC Myhrstad H Heimli J Lømo HK Blomhoff SO Kolset 1998 Multiplication and death-type of leukemia cell lines exposed to very long-chain polyunsaturated fatty acids Leukemia 12 921 929
143. HS Finstad H Dyrendal MC Myhrstad H Heimli CA Drevon 2000 Uptake and activation of eicosapentaenoic acid are related to accumulation of triacylglycerol in Ramos cells dying from apoptosis J Lipid Res 41 554 563
144. Y Tanaka K Goto Y Matsumoto R Ueoka 2008 Remarkably high inhibitory effects of docosahexaenoic acid incorporated into hybrid liposomes on the growth of tumor cells along with apoptosis Int J Pharm 359 264 271
145. N Merendino B Loppi M D'Aquino R Molinari G Pessina C Romano 2005 Docosahexaenoic acid induces apoptosis in the human PaCa-44 pancreatic cancer cell line by active reduced glutathione extrusion and lipid peroxidation Nutr Cancer 52 225 233
146. IJ Edwards H Sun Y Hu IM Berquin JT O'Flaherty JM Cline 2008 In vivo and in vitro regulation of syndecan 1 in prostate cells by n-3 polyunsaturated fatty acids J Biol Chem 283 18441 18449
147. ED Courtney S Matthews C Finlayson D Di Pierro A Belluzzi E Roda 2007 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 22 765 776
148. CR Harper MJ Edwards AP De Filippis TA Jacobson 2006 Flaxseed oil increases the plasma concentrations of cardioprotective (n-3) fatty acids in humans J Nutr 136 83 87
149. J Cao KA Schwichtenberg NQ Hanson MY Tsai 2006 Incorporation and clearance of omega-3 fatty acids in erythrocyte membranes and plasma phospholipids Clin Chem 52 2265 2272
150. EO Elvevoll H Barstad ES Breimo J Brox KE Eilertsen T Lund 2006 Enhanced incorporation of n-3 fatty acids from fish compared with fish oils Lipids 41 1109 1114
151. DC Cremonezzi MP Díaz MA Valentich AR Eynard 2004 Neoplastic and preneoplastic lesions induced by melamine in rat urothelium are modulated by dietary polyunsaturated fatty acids Food Chem Toxicol 42 1999 2007
152. P Latham EK Lund IT Johnson 1999 Dietary n-3 PUFA increases the apoptotic response to 1,2-dimethylhydrazine, reduces mitosis and suppresses the induction of carcinogenesis in the rat colon Carcinogenesis 20 645 650
153. WL Chang RS Chapkin JR Lupton 1998 Fish oil blocks azoxymethane-induced rat colon tumorigenesis by increasing cell differentiation and apoptosis rather than decreasing cell proliferation J Nutr 128 491 497
154. G Calviello P Palozza E Piccioni N Maggiano A Frattucci P Franceschelli 1998 Dietary supplementation with eicosapentaenoic and docosahexaenoic acid inhibits growth of Morris hepatocarcinoma 3924A in rats: effects on proliferation and apoptosis Int J Cancer 75 699 705
155. A Vecchini V Ceccarelli F Susta P Caligiana P Orvietani L Binaglia 2004 Dietary alpha-linolenic acid reduces COX-2 expression and induces apoptosis of hepatoma cells J Lipid Res 45 308 316
156. G Calviello P Palozza F Di Nicuolo N Maggiano GM Bartoli 2000 n-3 PUFA dietary supplementation inhibits proliferation and store-operated calcium influx in thymoma cells growing in Balb/c mice J Lipid Res 41 182 189
157. JM Connolly EM Gilhooly DP Rose 1999 Effects of reduced dietary linoleic acid intake, alone or combined with an algal source of docosahexaenoic acid, on MDA-MB-231 breast cancer cell growth and apoptosis in nude mice Nutr Cancer 35 44 49
158. CP Avula AK Zaman R Lawrence G Fernandes 1999 Induction of apoptosis and apoptotic mediators in Balb/C splenic lymphocytes by dietary n-3 and n-6 fatty acids Lipids 34 921 927
159. MY Hong JR Lupton JS Morris N Wang RJ Carroll LA Davidson 2000 Dietary fish oil reduces O6-methylguanine DNA adduct levels in rat colon in part by increasing apoptosis during tumor initiation Cancer Epidemiol Biomarkers Prev 9 819 826
160. LK Bancroft JR Lupton LA Davidson SS Taddeo ME Murphy RJ Carroll 2003 Dietary fish oil reduces oxidative DNA damage in rat colonocytes Free Radic Biol Med 35 149 159
161. LA Davidson DV Nguyen RM Hokanson ES Callaway RB Isett ND Turner 2004 Chemopreventive n-3 polyunsaturated fatty acids reprogram genetic signatures during colon cancer initiation and progression in the rat Cancer Res 64 6797 6804
162. J Cheng K Ogawa K Kuriki Y Yokoyama T Kamiya K Seno 2003 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 193 17 24
163. RS Chapkin MY Hong YY Fan LA Davidson LM Sanders CE Henderson 2002 Dietary n-3 PUFA alter colonocyte mitochondrial membrane composition and function Lipids 37 193 199
164. J Vanamala A Glagolenko P Yang RJ Carroll ME Murphy RA Newman 2008 Dietary fish oil and pectin enhance colonocyte apoptosis in part through suppression of PPARdelta/PGE2 and elevation of PGE3 Carcinogenesis 29 790 796
165. A Jordan J Stein 2003 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 42 324 331
166. A Vaculová J Hofmanová L Andera A Kozubík 2005 TRAIL and docosahexaenoic acid cooperate to induce HT-29 colon cancer cell death Cancer Lett 229 43 48
167. RA Siddiqui M Zerouga M Wu A Castillo K Harvey GP Zaloga 2005 Anticancer properties of propofol-docosahexaenoate and propofol eicosapentaenoate on breast cancer cells Breast Cancer Res 7 R645 R654
168. NK Narayanan BA Narayanan BS Reddy 2005 A combination of docosahexaenoic acid and celecoxib prevents prostate cancer cell growth in vitro and is associated with modulation of nuclear factor-kappaB, and steroid hormone receptors Int J Oncol 26 785 792
169. S Sturlan M Baumgartner E Roth T Bachleitner-Hofmann 2003 Docosahexaenoic acid enhances arsenic trioxide-mediated apoptosis in arsenic trioxide-resistant HL-60 cells Blood 101 4990 4997
170. M Brown M Bellon C Nicot 2007 Emodin and DHA potently increase arsenic trioxide interferon-alpha-induced cell death of HTLV-I-transformed cells by generation of reactive oxygen species and inhibition of Akt and AP-1 Blood 109 1653 1659
171. TM de Lima GP Amarante-Mendes R Curi 2007 Docosahexaenoic acid enhances the toxic effect of imatinib on Bcr-Abl expressing HL-60 cells Toxicol In Vitro 21 1678 1685
172. M Lindskog H Gleissman F Ponthan J Castro P Kogner JI Johnsen 2006 Neuroblastoma cell death in response to docosahexaenoic acid: sensitization to chemotherapy and arsenic-induced oxidative stress Int J Cancer 118 2584 2593
173. M Baumgartner S Sturlan E Roth B Wessner T Bachleitner-Hofmann 2004 Enhancement of arsenic trioxide-mediated apoptosis using docosahexaenoic acid in arsenic trioxide-resistant solid tumor cells Int J Cancer 112 707 712
174. WQ Ding B Liu JL Vaught RD Palmiter SE Lind 2006 Clioquinol and docosahexaenoic acid act synergistically to kill tumor cells Mol Cancer Ther 5 1864 1872
175. PD Biondo DN Brindley MB Sawyer CJ Field 2008 The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy J Nutr Biochem 19 787 796
176. H Nakagawa D Yamamoto Y Kiyozuka K Tsuta Y Uemura K Hioki 2000 Effects of genistein and synergistic action in combination with eicosapentaenoic acid on the growth of breast cancer cell lines J Cancer Res Clin Oncol 126 448 454
177. D Yamamoto Y Kiyozuka Y Adachi H Takada K Hioki A Tsubura 1999 Synergistic action of apoptosis induced by eicosapentaenoic acid and TNP-470 on human breast cancer cells Breast Cancer Res Treat 55 149 160
178. HJ Kim CA Vosseler PC Weber W Erl 2005 Docosahexaenoic acid induces apoptosis in proliferating human endothelial cells J Cell Physiol 204 881 888
179. QN Diep RM Touyz EL Schiffrin 2000 Docosahexaenoic acid, a peroxisome proliferator-activated receptor-alpha ligand, induces apoptosis in vascular smooth muscle cells by stimulation of p38 mitogen-activated protein kinase Hypertension 36 851 855
180. Y Wu M Tada K Takahata K Tomizawa H Matsui 2007 Inhibitory effect of polyunsaturated fatty acids on apoptosis induced by etoposide, okadaic acid and AraC in Neuro2a cells Acta Med Okayama 61 147 152
181. M Hashimoto S Hossain T Shimada K Sugioka H Yamasaki Y Fujii 2002 Docosahexaenoic acid provides protection from impairment of learning ability in Alzheimer's disease model rats J Neurochem 81 1084 1091
182. M Sarsilmaz A Songur H Özyurt I Kus OA Özen B Özyurt 2003 Potential role of dietary ω-3 essential fatty acids on some oxidant/antioxidant parameters in rats' corpus striatum Prostaglandins Leukot Essent Fat Acids 69 253 259
183. F Calon GP Lim T Morihara F Yang O Ubeda N Salem Jr 2005 Dietary n-3 polyunsaturated fatty acid depletion activates caspases and decreases NMDA receptors in the brain of a transgenic mouse model of Alzheimer's disease Eur J Neurosci 22 617 626
184. F Calon GP Lim F Yang T Morihara B Teter O Ubeda 2004 Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model Neuron 43 633 645
185. M Akbar F Calderon Z Wen HY Kim 2005 Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival Proc Natl Acad Sci USA 102 10858 10863
186. HY Kim 2008 Biochemical and biological functions of docosahexaenoic acid in the nervous system: modulation by ethanol Chem Phys Lipids 153 34 46
187. WJ Lukiw JG Cui VL Marcheselli M Bodker A Botkjaer K Gotlinger 2005 A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease J Clin Invest 115 2774 2783
188. NG Bazan 2006 The onset of brain injury and neurodegeneration triggers the synthesis of docosanoid neuroprotective signaling Cell Mol Neurobiol 26 901 913
189. PK Mukherjee VL Marcheselli S Barreiro J Hu D Bok NG Bazan 2007 Neurotrophins enhance retinal pigment epithelial cell survival through neuroprotectin D1 signaling Proc Natl Acad Sci USA 104 13152 13157
190. JR Sparrow HR Vollmer-Snarr J Zhou YP Jang S Jockusch Y Itagaki 2003 A2E-epoxides damage DNA in retinal pigment epithelial cells. Vitamin E and other antioxidants inhibit A2E-epoxide formation Biol Chem 278 18207 18213
191. RA Radu NL Mata A Bagla GH Travis 2004 Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt's macular degeneration Proc Natl Acad Sci USA 101 5928 5933
192. TV Bui Y Han RA Radu GH Travis NL Mata 2006 Characterization of native retinal fluorophores involved in biosynthesis of A2E and lipofuscin-associated retinopathies J Biol Chem 281 18112 18119
193. AV Cideciyan TS Aleman M Swider SB Schwartz JD Steinberg AJ Brucker 2004 Mutations in ABCA4 result in accumulation of lipofuscin before slowing of the retinoid cycle: a reappraisal of the human disease sequence Hum Mol Genet 13 525 534