Cis-9,trans-11-conjugated linoleic acid affects lipid raft composition and sensitizes human colorectal adenocarcinoma HT-29 cells to X-radiation

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 1, 2013, Pages 2233-2242

  Gra̧dzka, Iwona ^a   Sochanowicz, Barbara ^a   Brzóska, Kamil ^a   Wójciuk, Grzegorz ^a   Sommer, Sylwester ^a   Wojewódzka, Maria ^a   Gasińska, Anna ^b   Degen, Christian ^c   Jahreis, Gerhard ^c   Szumiel, Irena ^a  

^a INSTITUTE OF NUCLEAR CHEMISTRY AND TECHNOLOGY   (Poland)

^b INSTITUTE OF ONCOLOGY   (Poland)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Cis 9,trans 11 conjugated linoleic acid; DNA double strand break; EGF receptor; HT 29 cells; Lipid raft; Radiosensitization

Indexed keywords

CAVEOLIN 1; CHOLESTEROL; CONJUGATED LINOLEIC ACID; EPIDERMAL GROWTH FACTOR RECEPTOR; HISTONE H2AX; PROTEIN KINASE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOACCUMULATION; CANCER CELL CULTURE; CELL CYCLE PROGRESSION; CELL NUCLEUS; CELL SURVIVAL; CELLULAR DISTRIBUTION; CELLULAR STRESS RESPONSE; CHROMATID ABERRATION; CHROMATID FRAGMENTATION; CHROMOSOME ABERRATION; CIS TRANS ISOMERISM; COLORECTAL CARCINOMA; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; FRAGMENTATION REACTION; GAS CHROMATOGRAPHY; GENE EXPRESSION; GENE FREQUENCY; HUMAN; HUMAN CELL; LIPID COMPOSITION; LIPID RAFT; MEMBRANE STRUCTURE; MOLECULAR CLONING; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PULSED FIELD GEL ELECTROPHORESIS; RADIOSENSITIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; X IRRADIATION; X RAY;

ADENOCARCINOMA; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DNA BREAKS, DOUBLE-STRANDED; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LINOLEIC ACIDS, CONJUGATED; MEMBRANE MICRODOMAINS; RADIATION TOLERANCE; RADIATION-SENSITIZING AGENTS; X-RAYS;

EID: 84868586293     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.10.015     Document Type: Article

References (86)

1. R.E. Lawson, A.R. Moss, and D.I. Givens The role of dairy products in supplying conjugated linoleic acid to man's diet: a review Nutr. Res. Rev. 14 2001 153 172
2. W.W. Christie, G. Dobson, and R.O. Adlof A practical guide to the isolation, analysis and identification of conjugated linoleic acid Lipids 42 2007 1073 1084
3. K.L. Houseknecht, J.P. VandenHeuvel, S.Y. Moya-Camarena, C.P. Portocarrero, L.W. Peck, K.P. Nickel, and M.A. Belury Dietary conjugated linoleic acid normalizes impaired glucose tolerance in the Zucker diabetic fatty fa/fa rat Biochem. Biophys. Res. Commun. 244 1998 678 682
4. H.J. Cho, W.K. Kim, E.J. Kim, K.C. Jung, S. Park, H.S. Lee, A.L. Tyner, and J.H. Park Conjugated linoleic acid inhibits cell proliferation and ErB3 signaling in HT-29 human colon cell line Am. J. Physiol. Gastrointest. Liver Physiol. 284 2003 G996 G1005
5. M.A. Zulet, A. Marti, M.D. Parra, and J.A. Martinez Inflammation and conjugated linoleic acid: mechanisms of action and implication for human health J. Physiol. Biochem. 61 2005 483 494
6. N.S. Kelley, N.E. Hubbard, and K.L. Erickson Conjugated linoleic acid isomers and cancer J. Nutr. 137 2007 2599 2607
7. R. Ringseis Influence of conjugated linoleic acids on functional properties of vascular cells Br. J. Nutr. 102 2009 1099 1116
8. K. Eder, and R. Ringseis Metabolism and actions of conjugated linoleic acids on atherosclerosis-related events in vascular endothelial cells and smooth muscle cells Mol. Nutr. Food Res. 54 2010 17 36
9. K. Nagao, and T. Yanagita Conjugated fatty acids in food and their health benefits J. Biosci. Bioeng. 100 2005 152 157
10. I. Churruca, A. Fernandez-Quintela, and M.P. Portillo Conjugated linoleic acid isomers: differences in metabolism and biological effects Biofactors 35 2009 105 111
11. E.F. Murphy, G.J. Hooived, M. Muller, R.A. Calogero, and K.D. Cashman Conjugated linoleic acid alters global gene expression in human intestinal-like Caco-2 cells in an isomer-specific manner J. Nutr. 137 2007 2359 2365
12. J. Herrmann, D. Rubin, R. Hasler, U. Helwig, M. Pfeuffer, A. Auinger, C. Laue, P. Winkler, S. Schreiber, D. Bell, and J. Schrezenmeir Isomer-specific effects of CLA on gene expression in human adipose tissue depending on PPARgamma2 P12A polymorphism: a double blind, randomized, controlled cross-over study Lipids Health Dis. 8 2009 35
13. M.W. Pariza, Y. Park, and M.E. Cook Mechanisms of action of conjugated linoleic acid: evidence and speculation Proc. Soc. Exp. Biol. Med. 223 2000 8 13
14. S.P. Jackson Sensing and repairing DNA-double strand breaks Carcinogenesis 23 2002 687 696
15. I. Szumiel Intrinsic radiation sensitivity: cellular signalling is the key Radiat. Res. 169 2008 249 258
16. J.F. Hancock Lipid rafts: contentious only from simplistic standpoints Nat. Rev. Mol. Cell Biol. 7 2006 456 462
17. K. Jacobson, O.G. Mouritsen, and R.G. Anderson Lipid rafts: at a crossroad between cell biology and physics Nat. Cell Biol. 9 2007 7 14
18. L.J. Pike The challenge of lipid rafts J. Lipid Res. 50 2009 S323 S328 (Suppl.)
19. I. Levental, M. Grzybek, and K. Simons Greasing their way: lipid modifications determine protein association with membrane rafts Biochemistry 49 2010 6305 6316
20. J.C. Lawrence, D.E. Saslowsky, J.M. Edwardson, and R.M. Henderson Real-time analysis of the effects of cholesterol on lipid raft behavior using atomic force microscopy Biophys. J. 84 2003 1827 1832
21. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124
22. P. Yaqoob The nutritional significance of lipid rafts Annu. Rev. Nutr. 29 2009 257 282
23. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
24. G. Agatha, A. Voight, E. Kauf, and F. Zintl Conjugated linoleic acid modulation of cell membrane in leukemia cells Cancer Lett. 209 2004 87 103
25. G.C. Burdge, B. Lupoli, J.J. Russell, S. Tricon, S. Kew, T. Baneriee, K.J. Shingfield, D.E. Beever, R.F. Grimble, C.M. Williams, P. Yacob, and P.C. Calder Incorporation of cis-9, trans11 or trans-10, cis-12 conjugated linoleic acid into plasma and cellular lipids in healthy men J. Lipid Res. 45 2004 736 741
26. P.D. Biondo, D.N. Brindley, M.B. Sawyer, and C.J. Field The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy J. Nutr. Biochem. 19 2008 787 796
27. P.S.P. Huot, B. Sarkar, and D.W.L. Ma Conjugated linoleic acid alters caveolae phospholipid fatty acid composition and decreases caveolin-1 expression in MCF-7 breast cancer cells Nutr. Res. 30 2010 179 185
28. P.V. Subbaiah, I.G. Gould, S. Lal, and B. Aizezi Incorporation profiles of conjugated linoleic acid isomers in cell membranes and their positional distribution in phospholipids Biochim. Biophys. Acta 1811 2011 17 24
29. S.R. Wassall, and W. Stillwell Docosahexaenoic acid domains: the ultimate non-raft membrane domain Chem. Phys. Lipids 153 2008 57 63
30. A. Drouin, P. Douillette, and B. Lacasse Paquette, Radiosensitizing effect of conjugated linoleic acid on tumor cells MCF-7 and MDA-MB-231 Can. J. Physiol. Pharmacol. 82 2004 94 102
31. C. Degen, J. Ecker, S. Piegholdt, G. Liebisch, G. Schmitz, and G. Jahreis Metabolic and growth inhibitory effects of conjugated fatty acids in the cell line HT-29 with special regard to the conversion of t11, t13-CLA Biochim. Biophys. Acta 1811 2011 1070 1080
32. I. Gra̧dzka, and T. Iwaneńko A non-radioactive, PFGE-based assay for low levels of DNA double-strand breaks in mammalian cells DNA Repair 4 2005 1129 1139
33. E. Gotoh Drug-induced premature chromosome condensation (PCC) protocols: cytogenetic approaches in mitotic chromosome and interphase chromatin Methods Mol. Biol. 523 2009 83 92
34. T. Kawata, H. Ito, K. George, H. Wu, and F.A. Cucinotta Chromosome aberrations induced by high-LET radiations Biol. Sci. Space 18 2004 216 223
35. C. Liu, T. Kawata, N. Shigematsu, F.A. Cucinotta, K. George, M. Saito, T. Uno, K. Isobe, and H. Ito A comparison of chromosome repair kinetics in G(0) and G(1) reveals that enhanced repair fidelity under noncycling conditions accounts for increased potentially lethal damage repair Radiat. Res. 174 2010 566 573
36. A. Jucha, A. Wegierek-Ciuk, Z. Koza, H. Lisowska, A. Wójcik, M. Wojewódzka, and A. Lankoff FociCounter: a freely available PC programme for quantitative and qualitative analysis of gamma-H2AX foci Mutat. Res. 696 2010 16 20
37. B.B. Olsen, O.-G. Issinger, and B. Guerra Regulation of DNA-dependent protein kinase by protein kinase CK2 in human glioblastoma cells Oncogene 29 2010 6016 6026 Supplementary Materials and Methods available at http://www.nature.com/onc/journal/v29/n45/suppinfo/onc2010337s1.html
38. S.J. Veuger, N.J. Curtin, and G.-C. Smith Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1 Cancer Res. 63 2003 6008 6015
39. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
40. A. Jaudszus, M. Krokowski, P. Möckel, Y. Darcan, A. Avagyan, P. Matricardi, G. Jahreis, and E. Hamelmann Cis-9, trans-11-conjugated linoleic acid inhibits allergic sensitization and airway inflammation via a PPARgamma-related mechanism in mice J. Nutr. 138 2008 1336 1342
41. J.L. Macdonald, and L.J. Pike A simplified method for the preparation of detergent-free lipid rafts J. Lipid Res. 46 2005 1061 1067
42. F. Beppu, M. Hosokawa, L. Tanaka, H. Kohno, T. Tanaka, and K. Miyashita Potent inhibitory effect of trans9, trans11 isomer of conjugated linoleic acid on the growth of human colon cancer cells J. Nutr. Biochem. 17 2006 830 836
43. A. Petridou, V. Mougios, and A. Sagredos Supplementation with CLA: isomer incorporation into serum lipids and effect on body fat of women Lipids 38 2003 805 811
44. K. Sato, N. Shinohara, T. Honma, J. Ito, T. Arai, N. Nosaka, T. Aoyama, T. Tsuduki, and I. Ikeda The change in conjugated linoleic acid concentration in blood of Japanese fed a conjugated linoleic acid diet J. Nutr. Sci. Vitaminol. 57 2011 164 171
45. B. Nevaldine, J.A. Longo, and P.J. Hahn The scid defect results in much slower repair of DNA double-strand breaks but not high levels of residual breaks Radiat. Res. 147 1997 535 540
46. H. Utsumi, and M.M. Elkind Requirement for repair of DNA double-strand breaks by homologous recombination in split-dose recovery Radiat. Res. 155 2001 680 686
47. S. Meike, T. Yamamori, H. Yatsui, M. Eitaki, A. Matsuda, M. Morimatsu, M. Fukushima, Y. Yamasaki, and O. Inanamio A nucleoside anticancer drug, 1-(3-C-ethynyl-β-d-ribo-pentofuranosyl) cytosine (TAS106), sensitizes cells to radiation by suppressing BRCA2 expression Mol. Cancer 10 2011 92 100
48. N.C. Estabrook, H. Chin-Sinex, A.J. Borgmann, R.M. Dhaemers, R.H. Shapiro, D. Gilley, N. Huda, P. Crooks, C. Sweeney, and M.S. Mendonca Inhibition of NF-κB and DNA double-strand break repair by DNAPT sensitizes non-small lung cancers to X-rays Free Radic. Biol. Med. 51 2011 2249 2258
49. K. Dittmann, C. Mayer, B. Fahrenbacher, M. Schaller, U. Raju, L. Milas, D.J. Chen, R. Kehlbach, and H.P. Rodemann Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase J. Biol. Chem. 280 2005 31182 31189
50. E.M. Khan, J.M. Heidinger, M. Levy, M.P. Lisanti, T. Ravid, and T. Goldkorn Epidermal growth factor receptor exposed to oxidative stress undergoes Src- and caveolin-1 dependent perinuclear trafficking J. Biol. Chem. 281 2006 14486 14493
51. K. Dittmann, C. Mayer, and H.P. Rodemann Nuclear EGFR as novel therapeutic target. Insights into nuclear translocation and function Strahlenther. Onkol. 186 2009 1 6
52. K. Dittmann, C. Mayer, B. Fehrenbacher, M. Schaller, R. Kehlbach, and H.P. Rodemann Nuclear epidermal growth factor receptor modulates cellular radio-sensitivity by regulation of chromatin access Radiother. Oncol. 99 2011 317 322
53. C. Ip, and J.A. Scimeca Conjugated linoleic acid and linoleic acid are distinctive modulators of mammary carcinogenesis Nutr. Cancer 27 1997 131 135
54. N. Shikazono, M. Noguchi, K. Fujii, A. Urushibara, and A. Yokoya The yield, processing, and biological consequences of clustered DNA damage induced by ionizing radiation J. Radiat. Res. (Tokyo) 50 2009 27 36
55. L.J. Eccles, P. O'Neill, and M.E. Lomax Delayed repair or radiation induced clustered DNA damage: friend or foe? Mutat. Res. 711 2011 134 141
56. S.K. Singh, M. Wang, C. Staudt, and G. Iliakis Post-irradiation chemical processing of DNA damage generates double-strand breaks in cells already engaged in repair Nucleic Acids Res. 39 2011 8416 8429
57. S. Vispé, E.L. Ho, T.M. Yung, and M.S. Satoh Double-strand DNA break formation mediated by flap endonuclease-1 J. Biol. Chem. 278 2003 35279 35285
58. N. Yang, H. Galick, and S.S. Wallace Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks DNA Repair (Amst.) 3 2004 1323 1334
59. M. Gulston, C. de Lara, T. Jenner, E. Davis, and P. O'Neil Processing of clustered DNA damage generates additional double-strand breaks in mammalian cells post-irradiation Nucleic Acids Res. 32 2004 1602 1609
60. S. Vispé, and M.S. Satoh DNA repair patch-mediated double strand DNA break formation in human cells J. Biol. Chem. 275 2000 27386 27392
61. S. Biade, C.C. Stobbe, and J.D. Chapman The intrinsic radiosensitivity of some human tumor cells throughout their cell cycles Radiat. Res. 147 1997 416 421
62. E. Mladenov, and G. Iliakis Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways Mutat. Res. 711 2011 61 72
63. S.J. DiBiase, Z.-C. Zeng, R. Chen, T. Hyslop, W.J. Curran Jr., and G. Iliakis DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus Cancer Res. 60 2000 1245 1253
64. J. Tremp Chromosome aberrations and cell survival in irradiated mammalian cells Radiat. Res. 85 1981 554 566
65. 2 redox stress Am. J. Respir. Cell Mol. Biol. 19 1998 786 798
66. T. Ravid, C. Sweeney, P. Gee, K.L. Carraway III, and T. Goldkorn Epidermal growth factor receptor activation under oxidative stress fails to promote c-Cbl mediated down-regulation J. Biol. Chem. 277 2002 31214 31219
67. K. Dittmann, C. Mayer, R. Kehlbah, M.-C. Rothmund, and H.P. Rodemann Radiation-induced lipid peroxidation activates src kinase and triggers nuclear EGFR transport Radiother. Oncol. 92 2009 379 382
68. A. de Laurentiis, L. Donovan, and A. Arcaro Lipid rafts and caveolae in signaling by growth factor receptors Open Biochem. J. 1 2007 12 32
69. R.S. Chapkin, D.N. McMurray, L.A. Davidson, B.S. Patil, Y.Y. Fan, and J.R. Lupton Bioactive dietary long-chain fatty acids: emerging mechanisms of action Br. J. Nutr. 100 2008 1152 1157
70. A.F. Quest, L. Leyton, and M. Paragga Caveolins, caveolae, and lipid rafts in cellular transport, signaling, and disease Biochem. Cell Biol. 82 2004 129 144
71. K. Simons, and W.L. Vaz Model systems, lipid rafts, and cell membranes Annu. Rev. Biophys. Biomol. Struct. 33 2004 269 295
72. K. Simons, and M.J. Gerl Revitalizing membrane rafts: new tools and insights Nat. Rev. Mol. Cell Biol. 11 2010 688 699
73. K.L. Ritzenthaler, A.M. Suahin, T.D. Shultz, N. Dasguta, M.A. McGuire, and M.K. McGuire Dietary intake of c9,t11 conjugated linoleic acid correlates with its concentration in plasma lipid fractions in men but not in women J. Nutr. 142 2012 1645 1651
74. J. Ecker, G. Liebisch, M. Scherer, and G. Schmitz Differential effects of conjugated linoleic acid isomers on macrophage glycerophospholipid metabolism J. Lipid Res. 51 2010 2686 2694
75. A. Catalá Lipid peroxidation of membrane phospholipids generates hydroxyl-alkenals and oxidized phospholipids active in physiological and/or pathological conditions Chem. Phys. Lipids 157 2009 1 11
76. N. Zarkovic 4-Hydroxynonenal as a bioactive marker of pathophysiological processes Mol. Aspects Med. 24 2003 281 291
77. M. Stahlhut, and B. van Deurs Identification of filamin as a novel ligand for caveolin-1: evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton Mol. Biol. Cell 11 2000 325 337
78. W.S. Bush, G. Ihrke, J.M. Robinson, and A.K. Kenworthy Antibody-specific detection of caveolin-1 in subapical compartments of MDCK cells Histochem. Cell Biol. 126 2006 27 34
79. H. Robenek, G. Weissen-Plenz, and N.J. Severs Freeze-fracture replica immunolabelling reveals caveolin-1 in the human cardiomyocyte plasma membrane J. Cell Mol. Med. 12 2008 2519 2521
80. H. Demová, and R. Komers Determination of caveolin-1 in renal caveolar and non-caveolar fractions in experimental type 1 diabetes Physiol. Res. 58 2009 563 568
81. Y. Yao, S. Hong, H. Zhou, T. Yuan, R. Zeng, and K. Liao The differential protein and lipid compositions of noncaveolar lipid microdomains and caveolae Cell Res. 19 2009 497 506
82. M.G. Waugh, D. Lawson, and J.J. Hsuan Epidermal growth factor activation is localized within low-buoyant density, non-caveolar membrane domains Biochem. J. 337 1999 591 597
83. T. Ringerike, F.D. Blystad, F.O. Levy, I.H. Madshus, and E. Stang Cholesterol is important in control of EGF receptor kinase activity but EGF receptors are not concentrated in caveolae J. Cell Sci. 115 2002 1331 1340
84. P. Lajoie, L.D. Kojic, S. Nim, L. Li, J.W. Dennis, and I.R. Nabi Caveolin-1 regulation of dynamin-dependent, raft-mediated endocytosis of cholera toxin-B subunit occurs independently of caveolae J. Cell Mol. Med. 13 2009 3218 3225
85. W. Zundel, L.M. Swiersz, and A. Giacca Caveolin 1-mediated regulation of receptor tyrosine kinase-associated phosphatidylinositol 3-kinase activity by ceramide Mol. Cell. Biol. 20 2000 1507 1514
86. W. Elyassaki, and S. Wu Lipid rafts mediate ultraviolet light-induced Fas aggregation in M624 melanoma cells Photochem. Photobiol. 82 2006 787 792