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Published in: European Journal of Nutrition 4/2017

01-06-2017 | Original Contribution

Dietary fatty acids specifically modulate phospholipid pattern in colon cells with distinct differentiation capacities

Authors: Jiřina Hofmanová, Josef Slavík, Petra Ovesná, Zuzana Tylichová, Jan Vondráček, Nicol Straková, Alena Hyršlová Vaculová, Miroslav Ciganek, Alois Kozubík, Lucie Knopfová, Jan Šmarda, Miroslav Machala

Published in: European Journal of Nutrition | Issue 4/2017

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Abstract

Purpose

Although beneficial effects of the dietary n-3 docosahexaenoic acid (DHA) or butyrate in colon carcinogenesis have been implicated, the mechanisms of their action are not fully clear. Here, we investigated modulations of composition of individual phospholipid (PL) classes, with a particular emphasis on cardiolipins (CLs), in colon cells treated with DHA, sodium butyrate (NaBt), or their combination (DHA/NaBt), and we evaluated possible associations between lipid changes and cell fate after fatty acid treatment.

Methods

In two distinct human colon cell models, foetal colon (FHC) and adenocarcinoma (HCT-116) cells, we compared patterns and composition of individual PL classes following the fatty acid treatment by HPLC-MS/MS. In parallel, we measured the parameters reflecting cell proliferation, differentiation and death.

Results

In FHC cells, NaBt induced primarily differentiation, while co-treatment with DHA shifted their response towards cell death. In contrast, NaBt induced apoptosis in HCT-116 cells, which was not further affected by DHA. DHA was incorporated in all main PL types, increasing their unsaturation, while NaBt did not additionally modulate these effects in either cell model. Nevertheless, we identified an unusually wide range of CL species to be highly increased by NaBt and particularly by DHA/NaBt, and these effects were more pronounced in HCT-116 cells. DHA and DHA/NaBt enhanced levels of high molecular weight and more unsaturated CL species, containing DHA, which was specific for either differentiation or apoptotic responses.

Conclusions

We identified a wide range of CL species in the colon cells which composition was significantly modified after DHA and NaBt treatment. These specific CL modulations might contribute to distinct cellular differentiation or apoptotic responses.
Appendix
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Literature
1.
go back to reference Augenlicht LH, Mariadason JM, Wilson A, Arango D, Yang W, Heerdt BG, Velcich A (2002) Short chain fatty acids and colon cancer. J Nutr 132:3804S–3808S Augenlicht LH, Mariadason JM, Wilson A, Arango D, Yang W, Heerdt BG, Velcich A (2002) Short chain fatty acids and colon cancer. J Nutr 132:3804S–3808S
2.
go back to reference Baracos VE, Mazurak VC, Ma DW (2004) n-3 polyunsaturated fatty acids throughout the cancer trajectory: influence on disease incidence, progression, response to therapy and cancer-associated cachexia. Nutr Res Rev 17:177–192CrossRef Baracos VE, Mazurak VC, Ma DW (2004) n-3 polyunsaturated fatty acids throughout the cancer trajectory: influence on disease incidence, progression, response to therapy and cancer-associated cachexia. Nutr Res Rev 17:177–192CrossRef
3.
go back to reference Calder PC (2008) Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res 52:885–897CrossRef Calder PC (2008) Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res 52:885–897CrossRef
4.
go back to reference Ambrožová G, Pekarová M, Lojek A (2010) Effect of polyunsaturated fatty acids on the reactive oxygen and nitrogen species production by raw 264.7 macrophages. Eur J Nutr 49:133–139CrossRef Ambrožová G, Pekarová M, Lojek A (2010) Effect of polyunsaturated fatty acids on the reactive oxygen and nitrogen species production by raw 264.7 macrophages. Eur J Nutr 49:133–139CrossRef
5.
go back to reference Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ (2008) Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27:104–119CrossRef Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ (2008) Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27:104–119CrossRef
6.
go back to reference Dupertuis YM, Meguid MM, Pichard C (2007) Colon cancer therapy: new perspectives of nutritional manipulations using polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care 10:427–432CrossRef Dupertuis YM, Meguid MM, Pichard C (2007) Colon cancer therapy: new perspectives of nutritional manipulations using polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care 10:427–432CrossRef
7.
go back to reference Pot GK, Geelen A, van Heijningen EM, Siezen CL, van Kranen HJ, Kampman E (2008) Opposing associations of serum n-3 and n-6 polyunsaturated fatty acids with colorectal adenoma risk: an endoscopy-based case–control study. Int J Cancer 123:1974–1977CrossRef Pot GK, Geelen A, van Heijningen EM, Siezen CL, van Kranen HJ, Kampman E (2008) Opposing associations of serum n-3 and n-6 polyunsaturated fatty acids with colorectal adenoma risk: an endoscopy-based case–control study. Int J Cancer 123:1974–1977CrossRef
8.
go back to reference Calviello G, Serini S, Piccioni E (2007) n-3 polyunsaturated fatty acids and the prevention of colorectal cancer: molecular mechanisms involved. Curr Med Chem 14:3059–3069CrossRef Calviello G, Serini S, Piccioni E (2007) n-3 polyunsaturated fatty acids and the prevention of colorectal cancer: molecular mechanisms involved. Curr Med Chem 14:3059–3069CrossRef
9.
go back to reference Sauer J, Richter KK, Pool-Zobel BL (2007) Physiological concentrations of butyrate favorably modulate genes of oxidative and metabolic stress in primary human colon cells. J Nutr Biochem 18:736–745CrossRef Sauer J, Richter KK, Pool-Zobel BL (2007) Physiological concentrations of butyrate favorably modulate genes of oxidative and metabolic stress in primary human colon cells. J Nutr Biochem 18:736–745CrossRef
10.
go back to reference Wächtershäuser A, Stein J (2000) Rationale for the luminal provision of butyrate in intestinal diseases. Eur J Nutr 39:164–171CrossRef Wächtershäuser A, Stein J (2000) Rationale for the luminal provision of butyrate in intestinal diseases. Eur J Nutr 39:164–171CrossRef
11.
go back to reference Chapkin RS, Seo J, McMurray DN, Lupton JR (2008) Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine. Chem Phys Lipids 153:14–23CrossRef Chapkin RS, Seo J, McMurray DN, Lupton JR (2008) Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine. Chem Phys Lipids 153:14–23CrossRef
12.
go back to reference Comba A, Lin YH, Eynard AR, Valentich MA, Fernandez-Zapico ME, Pasqualini ME (2011) Basic aspects of tumor cell fatty acid-regulated signaling and transcription factors. Cancer Metastasis Rev 30:325–342CrossRef Comba A, Lin YH, Eynard AR, Valentich MA, Fernandez-Zapico ME, Pasqualini ME (2011) Basic aspects of tumor cell fatty acid-regulated signaling and transcription factors. Cancer Metastasis Rev 30:325–342CrossRef
13.
go back to reference Skender B, Hyršlová Vaculová A, Hofmanová J (2012) 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 156:186–199CrossRef Skender B, Hyršlová Vaculová A, Hofmanová J (2012) 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 156:186–199CrossRef
14.
go back to reference Hofmanová J, Hyršlová Vaculová A, Kozubík A (2013) Regulation of the metabolism of polyunsaturated fatty acids and butyrate in colon cancer cells. Curr Pharm Biotechnol 14:274–288CrossRef Hofmanová J, Hyršlová Vaculová A, Kozubík A (2013) Regulation of the metabolism of polyunsaturated fatty acids and butyrate in colon cancer cells. Curr Pharm Biotechnol 14:274–288CrossRef
15.
go back to reference Pool-Zobel BL, Selvaraju V, Sauer J, Kautenburger T, Kiefer J, Richter KK, Soom M, Wolfl S (2005) Butyrate may enhance toxicological defence in primary, adenoma and tumor human colon cells by favourably modulating expression of glutathione S-transferases genes, an approach in nutrigenomics. Carcinogenesis 26:1064–1076CrossRef Pool-Zobel BL, Selvaraju V, Sauer J, Kautenburger T, Kiefer J, Richter KK, Soom M, Wolfl S (2005) Butyrate may enhance toxicological defence in primary, adenoma and tumor human colon cells by favourably modulating expression of glutathione S-transferases genes, an approach in nutrigenomics. Carcinogenesis 26:1064–1076CrossRef
16.
go back to reference Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA (2002) The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 132:1012–1017 Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA (2002) The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 132:1012–1017
17.
go back to reference Wilson AJ, Byun DS, Popova N, Murray LB, L’Italien K, Sowa Y, Arango D, Velcich A, Augenlicht LH, Mariadason JM (2006) Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 281:13548–13558CrossRef Wilson AJ, Byun DS, Popova N, Murray LB, L’Italien K, Sowa Y, Arango D, Velcich A, Augenlicht LH, Mariadason JM (2006) Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 281:13548–13558CrossRef
18.
go back to reference Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ (2012) The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell 48:612–626CrossRef Donohoe DR, Collins LB, Wali A, Bigler R, Sun W, Bultman SJ (2012) The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol Cell 48:612–626CrossRef
19.
go back to reference Habermann N, Christian B, Luckas B, Pool-Zobel BL, Lund EK, Glei M (2009) Effects of fatty acids on metabolism and cell growth of human colon cell lines of different transformation state. BioFactors 35:460–467CrossRef Habermann N, Christian B, Luckas B, Pool-Zobel BL, Lund EK, Glei M (2009) Effects of fatty acids on metabolism and cell growth of human colon cell lines of different transformation state. BioFactors 35:460–467CrossRef
20.
go back to reference Hofmanová J, Straková N, Vaculová AH, Tylichová Z, Šafaříková B, Skender B, Kozubík A (2014) Interaction of dietary fatty acids with tumour necrosis factor family cytokines during colon inflammation and cancer. Mediators Inflamm 2014:848632CrossRef Hofmanová J, Straková N, Vaculová AH, Tylichová Z, Šafaříková B, Skender B, Kozubík A (2014) Interaction of dietary fatty acids with tumour necrosis factor family cytokines during colon inflammation and cancer. Mediators Inflamm 2014:848632CrossRef
21.
go back to reference Ma DW, Seo J, Switzer KC, Fan YY, McMurray DN, Lupton JR, Chapkin RS (2004) n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research. J Nutr Biochem 15:700–706CrossRef Ma DW, Seo J, Switzer KC, Fan YY, McMurray DN, Lupton JR, Chapkin RS (2004) n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research. J Nutr Biochem 15:700–706CrossRef
22.
go back to reference Khairallah RJ, Sparagna GC, Khanna N, O’Shea KM, Hecker PA, Kristian T, Fiskum G, Des Rosiers C, Polster BM, Stanley WC (2010) Dietary supplementation with docosahexaenoic acid, but not eicosapentaenoic acid, dramatically alters cardiac mitochondrial phospholipid fatty acid composition and prevents permeability transition. Biochim Biophys Acta 1797:1555–1562CrossRef Khairallah RJ, Sparagna GC, Khanna N, O’Shea KM, Hecker PA, Kristian T, Fiskum G, Des Rosiers C, Polster BM, Stanley WC (2010) Dietary supplementation with docosahexaenoic acid, but not eicosapentaenoic acid, dramatically alters cardiac mitochondrial phospholipid fatty acid composition and prevents permeability transition. Biochim Biophys Acta 1797:1555–1562CrossRef
23.
go back to reference Kagan VE, Tyurina YY, Bayir H, Chu CT, Kapralov AA, Vlasova II, Belikova NA, Tyurin VA, Amoscato A, Epperly M, Greenberger J, Dekosky S, Shvedova AA, Jiang J (2006) The “pro-apoptotic genies” get out of mitochondria: oxidative lipidomics and redox activity of cytochrome c/cardiolipin complexes. Chem Biol Interact 163:15–28CrossRef Kagan VE, Tyurina YY, Bayir H, Chu CT, Kapralov AA, Vlasova II, Belikova NA, Tyurin VA, Amoscato A, Epperly M, Greenberger J, Dekosky S, Shvedova AA, Jiang J (2006) The “pro-apoptotic genies” get out of mitochondria: oxidative lipidomics and redox activity of cytochrome c/cardiolipin complexes. Chem Biol Interact 163:15–28CrossRef
24.
go back to reference Schug ZT, Gottlieb E (2009) Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis. Biochim Biophys Acta 1788:2022–2031CrossRef Schug ZT, Gottlieb E (2009) Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis. Biochim Biophys Acta 1788:2022–2031CrossRef
25.
go back to reference Chicco AJ, Sparagna GC (2007) Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 292:C33–C44CrossRef Chicco AJ, Sparagna GC (2007) Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 292:C33–C44CrossRef
26.
go back to reference Monteiro JP, Oliveira PJ, Jurado AS (2013) Mitochondrial membrane lipid remodeling in pathophysiology: a new target for diet and therapeutic interventions. Prog Lipid Res 52:513–528CrossRef Monteiro JP, Oliveira PJ, Jurado AS (2013) Mitochondrial membrane lipid remodeling in pathophysiology: a new target for diet and therapeutic interventions. Prog Lipid Res 52:513–528CrossRef
27.
go back to reference Hofmanová J, Vaculová A, Lojek A, Kozubík A (2005) Interaction of polyunsaturated fatty acids and sodium butyrate during apoptosis in HT-29 human colon adenocarcinoma cells. Eur J Nutr 44:40–51CrossRef Hofmanová J, Vaculová A, Lojek A, Kozubík A (2005) Interaction of polyunsaturated fatty acids and sodium butyrate during apoptosis in HT-29 human colon adenocarcinoma cells. Eur J Nutr 44:40–51CrossRef
28.
go back to reference Hofmanová J, Vaculová A, Koubková Z, Hýžd’alová M, Kozubík A (2009) Human fetal colon cells and colon cancer cells respond differently to butyrate and PUFAs. Mol Nutr Food Res 53(Suppl 1):S102–S113CrossRef Hofmanová J, Vaculová A, Koubková Z, Hýžd’alová M, Kozubík A (2009) Human fetal colon cells and colon cancer cells respond differently to butyrate and PUFAs. Mol Nutr Food Res 53(Suppl 1):S102–S113CrossRef
29.
go back to reference Kolar SS, Barhoumi R, Lupton JR, Chapkin RS (2007) Docosahexaenoic acid and butyrate synergistically induce colonocyte apoptosis by enhancing mitochondrial Ca2+ accumulation. Cancer Res 67:5561–5568CrossRef Kolar SS, Barhoumi R, Lupton JR, Chapkin RS (2007) Docosahexaenoic acid and butyrate synergistically induce colonocyte apoptosis by enhancing mitochondrial Ca2+ accumulation. Cancer Res 67:5561–5568CrossRef
30.
go back to reference Lee DY, Lupton JR, Aukema HM, Chapkin RS (1993) Dietary fat and fiber alter rat colonic mucosal lipid mediators and cell proliferation. J Nutr 123:1808–1817 Lee DY, Lupton JR, Aukema HM, Chapkin RS (1993) Dietary fat and fiber alter rat colonic mucosal lipid mediators and cell proliferation. J Nutr 123:1808–1817
31.
go back to reference Sanders LM, Henderson CE, Hong MY, Barhoumi R, Burghardt RC, Wang N, Spinka CM, Carroll RJ, Turner ND, Chapkin RS, Lupton JR (2004) An increase in reactive oxygen species by dietary fish oil coupled with the attenuation of antioxidant defenses by dietary pectin enhances rat colonocyte apoptosis. J Nutr 134:3233–3238 Sanders LM, Henderson CE, Hong MY, Barhoumi R, Burghardt RC, Wang N, Spinka CM, Carroll RJ, Turner ND, Chapkin RS, Lupton JR (2004) An increase in reactive oxygen species by dietary fish oil coupled with the attenuation of antioxidant defenses by dietary pectin enhances rat colonocyte apoptosis. J Nutr 134:3233–3238
32.
go back to reference Hofmanová J, Ciganek M, Slavík J, Kozubík A, Stixová L, Vaculová A, Dušek L, Machala M (2012) Lipid alterations in human colon epithelial cells induced to differentiation and/or apoptosis by butyrate and polyunsaturated fatty acids. J Nutr Biochem 23:539–548CrossRef Hofmanová J, Ciganek M, Slavík J, Kozubík A, Stixová L, Vaculová A, Dušek L, Machala M (2012) Lipid alterations in human colon epithelial cells induced to differentiation and/or apoptosis by butyrate and polyunsaturated fatty acids. J Nutr Biochem 23:539–548CrossRef
33.
go back to reference Vištejnová L, Dvořáková J, Hasová M, Muthny T, Velebný V, Souček K, Kubala L (2009) The comparison of impedance-based method of cell proliferation monitoring with commonly used metabolic-based techniques. Neuro Endocrinol Lett 30(Suppl 1):121–127 Vištejnová L, Dvořáková J, Hasová M, Muthny T, Velebný V, Souček K, Kubala L (2009) The comparison of impedance-based method of cell proliferation monitoring with commonly used metabolic-based techniques. Neuro Endocrinol Lett 30(Suppl 1):121–127
34.
go back to reference Kovaříková M, Pacherník J, Hofmanová J, Zadák Z, Kozubík A (2000) TNF-alpha modulates the differentiation induced by butyrate in the HT-29 human colon adenocarcinoma cell line. Eur J Cancer 36:1844–1852CrossRef Kovaříková M, Pacherník J, Hofmanová J, Zadák Z, Kozubík A (2000) TNF-alpha modulates the differentiation induced by butyrate in the HT-29 human colon adenocarcinoma cell line. Eur J Cancer 36:1844–1852CrossRef
35.
go back to reference Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRef Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRef
36.
go back to reference Kang JX, Wang J (2005) A simplified method for analysis of polyunsaturated fatty acids. BMC Biochem 6:5CrossRef Kang JX, Wang J (2005) A simplified method for analysis of polyunsaturated fatty acids. BMC Biochem 6:5CrossRef
37.
go back to reference Taguchi R, Houjou T, Nakanishi H, Yamazaki T, Ishida M, Imagawa M, Shimizu T (2005) Focused lipidomics by tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 823:26–36CrossRef Taguchi R, Houjou T, Nakanishi H, Yamazaki T, Ishida M, Imagawa M, Shimizu T (2005) Focused lipidomics by tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 823:26–36CrossRef
38.
go back to reference Grupp K, Jedrzejewska K, Tsourlakis MC, Koop C, Wilczak W, Adam M, Quaas A, Sauter G, Simon R, Izbicki JR, Graefen M, Huland H, Schlomm T, Minner S, Steurer S (2013) High mitochondria content is associated with prostate cancer disease progression. Mol Cancer 12:145CrossRef Grupp K, Jedrzejewska K, Tsourlakis MC, Koop C, Wilczak W, Adam M, Quaas A, Sauter G, Simon R, Izbicki JR, Graefen M, Huland H, Schlomm T, Minner S, Steurer S (2013) High mitochondria content is associated with prostate cancer disease progression. Mol Cancer 12:145CrossRef
39.
go back to reference Schønberg SA, Lundemo AG, Fladvad T, Holmgren K, Bremseth H, Nilsen A, Gederaas O, Tvedt KE, Egeberg KW, Krokan HE (2006) Closely related colon cancer cell lines display different sensitivity to polyunsaturated fatty acids, accumulate different lipid classes and downregulate sterol regulatory element-binding protein 1. FEBS J 273:2749–2765CrossRef Schønberg SA, Lundemo AG, Fladvad T, Holmgren K, Bremseth H, Nilsen A, Gederaas O, Tvedt KE, Egeberg KW, Krokan HE (2006) Closely related colon cancer cell lines display different sensitivity to polyunsaturated fatty acids, accumulate different lipid classes and downregulate sterol regulatory element-binding protein 1. FEBS J 273:2749–2765CrossRef
40.
go back to reference Seo J, Barhoumi R, Johnson AE, Lupton JR, Chapkin RS (2006) Docosahexaenoic acid selectively inhibits plasma membrane targeting of lipidated proteins. FASEB J 20:770–772 Seo J, Barhoumi R, Johnson AE, Lupton JR, Chapkin RS (2006) Docosahexaenoic acid selectively inhibits plasma membrane targeting of lipidated proteins. FASEB J 20:770–772
41.
go back to reference Stillwell W, Shaikh SR, Zerouga M, Siddiqui R, Wassall SR (2005) Docosahexaenoic acid affects cell signaling by altering lipid rafts. Reprod Nutr Dev 45:559–579CrossRef Stillwell W, Shaikh SR, Zerouga M, Siddiqui R, Wassall SR (2005) Docosahexaenoic acid affects cell signaling by altering lipid rafts. Reprod Nutr Dev 45:559–579CrossRef
42.
go back to reference Wright MM, Howe AG, Zaremberg V (2004) Cell membranes and apoptosis: role of cardiolipin, phosphatidylcholine, and anticancer lipid analogues. Biochem Cell Biol 82:18–26CrossRef Wright MM, Howe AG, Zaremberg V (2004) Cell membranes and apoptosis: role of cardiolipin, phosphatidylcholine, and anticancer lipid analogues. Biochem Cell Biol 82:18–26CrossRef
43.
go back to reference Shaikh SR, Kinnun JJ, Leng X, Williams JA, Wassall SR (2015) How polyunsaturated fatty acids modify molecular organization in membranes: insight from NMR studies of model systems. Biochim Biophys Acta 1848:211–219CrossRef Shaikh SR, Kinnun JJ, Leng X, Williams JA, Wassall SR (2015) How polyunsaturated fatty acids modify molecular organization in membranes: insight from NMR studies of model systems. Biochim Biophys Acta 1848:211–219CrossRef
44.
go back to reference Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9:139–150CrossRef Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9:139–150CrossRef
45.
go back to reference Skender B, Hofmanová J, Slavík J, Jelínková I, Machala M, Moyer MP, Kozubík A, Hyršlová Vaculová A (2014) DHA-mediated enhancement of TRAIL-induced apoptosis in colon cancer cells is associated with engagement of mitochondria and specific alterations in sphingolipid metabolism. Biochim Biophys Acta 1841:1308–1317CrossRef Skender B, Hofmanová J, Slavík J, Jelínková I, Machala M, Moyer MP, Kozubík A, Hyršlová Vaculová A (2014) DHA-mediated enhancement of TRAIL-induced apoptosis in colon cancer cells is associated with engagement of mitochondria and specific alterations in sphingolipid metabolism. Biochim Biophys Acta 1841:1308–1317CrossRef
46.
go back to reference Zeczycki TN, Whelan J, Hayden WT, Brown DA, Shaikh SR (2014) Increasing levels of cardiolipin differentially influence packing of phospholipids found in the mitochondrial inner membrane. Biochem Biophys Res Commun 450:366–371CrossRef Zeczycki TN, Whelan J, Hayden WT, Brown DA, Shaikh SR (2014) Increasing levels of cardiolipin differentially influence packing of phospholipids found in the mitochondrial inner membrane. Biochem Biophys Res Commun 450:366–371CrossRef
47.
go back to reference Kiebish MA, Han X, Cheng H, Chuang JH, Seyfried TN (2008) Cardiolipin and electron transport chain abnormalities in mouse brain tumor mitochondria: lipidomic evidence supporting the Warburg theory of cancer. J Lipid Res 49:2545–2556CrossRef Kiebish MA, Han X, Cheng H, Chuang JH, Seyfried TN (2008) Cardiolipin and electron transport chain abnormalities in mouse brain tumor mitochondria: lipidomic evidence supporting the Warburg theory of cancer. J Lipid Res 49:2545–2556CrossRef
48.
go back to reference Aoun M, Fouret G, Michel F, Bonafos B, Ramos J, Cristol JP, Carbonneau MA, Coudray C, Feillet-Coudray C (2012) Dietary fatty acids modulate liver mitochondrial cardiolipin content and its fatty acid composition in rats with non alcoholic fatty liver disease. J Bioenerg Biomembr 44:439–452CrossRef Aoun M, Fouret G, Michel F, Bonafos B, Ramos J, Cristol JP, Carbonneau MA, Coudray C, Feillet-Coudray C (2012) Dietary fatty acids modulate liver mitochondrial cardiolipin content and its fatty acid composition in rats with non alcoholic fatty liver disease. J Bioenerg Biomembr 44:439–452CrossRef
49.
go back to reference Feillet-Coudray C, Fouret G, Casas F, Coudray C (2014) Impact of high dietary lipid intake and related metabolic disorders on the abundance and acyl composition of the unique mitochondrial phospholipid, cardiolipin. J Bioenerg Biomembr 46:447–457CrossRef Feillet-Coudray C, Fouret G, Casas F, Coudray C (2014) Impact of high dietary lipid intake and related metabolic disorders on the abundance and acyl composition of the unique mitochondrial phospholipid, cardiolipin. J Bioenerg Biomembr 46:447–457CrossRef
50.
go back to reference Cortie CH, Else PL (2012) Dietary docosahexaenoic Acid (22:6) incorporates into cardiolipin at the expense of linoleic Acid (18:2): analysis and potential implications. Int J Mol Sci 13:15447–15463CrossRef Cortie CH, Else PL (2012) Dietary docosahexaenoic Acid (22:6) incorporates into cardiolipin at the expense of linoleic Acid (18:2): analysis and potential implications. Int J Mol Sci 13:15447–15463CrossRef
51.
go back to reference Stanley WC, Khairallah RJ, Dabkowski ER (2012) Update on lipids and mitochondrial function: impact of dietary n-3 polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care 15:122–126CrossRef Stanley WC, Khairallah RJ, Dabkowski ER (2012) Update on lipids and mitochondrial function: impact of dietary n-3 polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care 15:122–126CrossRef
52.
go back to reference Gonzalvez F, Gottlieb E (2007) Cardiolipin: setting the beat of apoptosis. Apoptosis 12:877–885CrossRef Gonzalvez F, Gottlieb E (2007) Cardiolipin: setting the beat of apoptosis. Apoptosis 12:877–885CrossRef
53.
go back to reference Rohrbach S (2009) Effects of dietary polyunsaturated fatty acids on mitochondria. Curr Pharm Des 15:4103–4116CrossRef Rohrbach S (2009) Effects of dietary polyunsaturated fatty acids on mitochondria. Curr Pharm Des 15:4103–4116CrossRef
54.
go back to reference Planas-Iglesias J, Dwarakanath H, Mohammadyani D, Yanamala N, Kagan VE, Klein-Seetharaman J (2015) Cardiolipin interactions with proteins. Biophys J 109:1282–1294CrossRef Planas-Iglesias J, Dwarakanath H, Mohammadyani D, Yanamala N, Kagan VE, Klein-Seetharaman J (2015) Cardiolipin interactions with proteins. Biophys J 109:1282–1294CrossRef
55.
go back to reference Heerdt BG, Houston MA, Wilson AJ, Augenlicht LH (2003) The intrinsic mitochondrial membrane potential (Deltapsim) is associated with steady-state mitochondrial activity and the extent to which colonic epithelial cells undergo butyrate-mediated growth arrest and apoptosis. Cancer Res 63:6311–6319 Heerdt BG, Houston MA, Wilson AJ, Augenlicht LH (2003) The intrinsic mitochondrial membrane potential (Deltapsim) is associated with steady-state mitochondrial activity and the extent to which colonic epithelial cells undergo butyrate-mediated growth arrest and apoptosis. Cancer Res 63:6311–6319
56.
go back to reference Marcil V, Delvin E, Seidman E, Poitras L, Zoltowska M, Garofalo C, Levy E (2002) Modulation of lipid synthesis, apolipoprotein biogenesis, and lipoprotein assembly by butyrate. Am J Physiol Gastrointest Liver Physiol 283:G340–G346CrossRef Marcil V, Delvin E, Seidman E, Poitras L, Zoltowska M, Garofalo C, Levy E (2002) Modulation of lipid synthesis, apolipoprotein biogenesis, and lipoprotein assembly by butyrate. Am J Physiol Gastrointest Liver Physiol 283:G340–G346CrossRef
57.
go back to reference Kamitani H, Ikawa H, Hsi LC, Watanabe T, DuBois RN, Eling TE (1999) Regulation of 12-lipoxygenase in rat intestinal epithelial cells during differentiation and apoptosis induced by sodium butyrate. Arch Biochem Biophys 368:45–55CrossRef Kamitani H, Ikawa H, Hsi LC, Watanabe T, DuBois RN, Eling TE (1999) Regulation of 12-lipoxygenase in rat intestinal epithelial cells during differentiation and apoptosis induced by sodium butyrate. Arch Biochem Biophys 368:45–55CrossRef
58.
go back to reference Zambell KL, Fitch MD, Fleming SE (2003) Acetate and butyrate are the major substrates for de novo lipogenesis in rat colonic epithelial cells. J Nutr 133:3509–3515 Zambell KL, Fitch MD, Fleming SE (2003) Acetate and butyrate are the major substrates for de novo lipogenesis in rat colonic epithelial cells. J Nutr 133:3509–3515
59.
go back to reference Leschelle X, Delpal S, Goubern M, Blottiere HM, Blachier F (2000) Butyrate metabolism upstream and downstream acetyl-CoA synthesis and growth control of human colon carcinoma cells. Eur J Biochem 267:6435–6442CrossRef Leschelle X, Delpal S, Goubern M, Blottiere HM, Blachier F (2000) Butyrate metabolism upstream and downstream acetyl-CoA synthesis and growth control of human colon carcinoma cells. Eur J Biochem 267:6435–6442CrossRef
60.
go back to reference Tailor D, Hahm ER, Kale RK, Singh SV, Singh RP (2014) Sodium butyrate induces DRP1-mediated mitochondrial fusion and apoptosis in human colorectal cancer cells. Mitochondrion 16:55–64CrossRef Tailor D, Hahm ER, Kale RK, Singh SV, Singh RP (2014) Sodium butyrate induces DRP1-mediated mitochondrial fusion and apoptosis in human colorectal cancer cells. Mitochondrion 16:55–64CrossRef
61.
go back to reference Ishihara T, Kohno H, Ishihara N (2015) Physiological roles of mitochondrial fission in cultured cells and mouse development. Ann N Y Acad Sci 1350:77–81CrossRef Ishihara T, Kohno H, Ishihara N (2015) Physiological roles of mitochondrial fission in cultured cells and mouse development. Ann N Y Acad Sci 1350:77–81CrossRef
62.
go back to reference Pajak B, Orzechowski A, Gajkowska B (2007) Molecular basis of sodium butyrate-dependent proapoptotic activity in cancer cells. Adv Med Sci 52:83–88 Pajak B, Orzechowski A, Gajkowska B (2007) Molecular basis of sodium butyrate-dependent proapoptotic activity in cancer cells. Adv Med Sci 52:83–88
63.
go back to reference Murphy EJ, Horrocks LA (1993) Effects of differentiation on the phospholipid and phospholipid fatty acid composition of N1E−115 neuroblastoma cells. Biochim Biophys Acta 1167:131–136CrossRef Murphy EJ, Horrocks LA (1993) Effects of differentiation on the phospholipid and phospholipid fatty acid composition of N1E−115 neuroblastoma cells. Biochim Biophys Acta 1167:131–136CrossRef
64.
go back to reference Sampaio JL, Gerl MJ, Klose C, Ejsing CS, Beug H, Simons K, Shevchenko A (2011) Membrane lipidome of an epithelial cell line. Proc Natl Acad Sci USA 108:1903–1907CrossRef Sampaio JL, Gerl MJ, Klose C, Ejsing CS, Beug H, Simons K, Shevchenko A (2011) Membrane lipidome of an epithelial cell line. Proc Natl Acad Sci USA 108:1903–1907CrossRef
65.
go back to reference Dória ML, Ribeiro AS, Wang J, Cotrim CZ, Domingues P, Williams C, Domingues MR, Helguero LA (2014) Fatty acid and phospholipid biosynthetic pathways are regulated throughout mammary epithelial cell differentiation and correlate to breast cancer survival. FASEB J 28:4247–4264CrossRef Dória ML, Ribeiro AS, Wang J, Cotrim CZ, Domingues P, Williams C, Domingues MR, Helguero LA (2014) Fatty acid and phospholipid biosynthetic pathways are regulated throughout mammary epithelial cell differentiation and correlate to breast cancer survival. FASEB J 28:4247–4264CrossRef
Metadata
Title
Dietary fatty acids specifically modulate phospholipid pattern in colon cells with distinct differentiation capacities
Authors
Jiřina Hofmanová
Josef Slavík
Petra Ovesná
Zuzana Tylichová
Jan Vondráček
Nicol Straková
Alena Hyršlová Vaculová
Miroslav Ciganek
Alois Kozubík
Lucie Knopfová
Jan Šmarda
Miroslav Machala
Publication date
01-06-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 4/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-016-1196-y

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