Butyrate and docosahexaenoic acid interact in alterations of specific lipid classes in differentiating colon cancer cells

被引:13
作者
Tylichova, Zuzana [1 ,2 ]
Slavik, Josef [3 ]
Ciganek, Miroslav [3 ]
Ovesna, Petra [1 ,4 ]
Krcmar, Pavel [3 ]
Strakova, Nicol [1 ]
Machala, Miroslav [3 ]
Kozubik, Alois [1 ,2 ]
Hofmanova, Jirina [1 ,2 ]
Vondracek, Jan [1 ]
机构
[1] Czech Acad Sci, Inst Biophys, Dept Cytokinet, Kralovopolska 135, Brno 61265, Czech Republic
[2] Masaryk Univ, Dept Expt Biol, Fac Sci, Brno, Czech Republic
[3] Vet Res Inst, Brno, Czech Republic
[4] Masaryk Univ, Inst Biostat & Anal, Brno, Czech Republic
关键词
butyrate; ceramides; colon cancer; docosahexaenoic acid; lipid analyses; phospholipids; POLYUNSATURATED FATTY-ACIDS; STEAROYL-COA DESATURASE; COLORECTAL-CANCER; SODIUM-BUTYRATE; GENE-EXPRESSION; APOPTOSIS; METABOLISM; ACTIVATION; TISSUE; OMEGA-3-FATTY-ACIDS;
D O I
10.1002/jcb.26641
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Docosahexaenoic acid (DHA) and sodium butyrate (NaBt) exhibit a number of interactive effects on colon cancer cell growth, differentiation, or apoptosis; however, the molecular mechanisms responsible for these interactions and their impact on cellular lipidome are still not fully clear. Here, we show that both dietary agents together induce dynamic alterations of lipid metabolism, specific cellular lipid classes, and fatty acid composition. In HT-29 cell line, a model of differentiating colon carcinoma cells, NaBt supported incorporation of free DHA into non-polar lipids and their accumulation in cytoplasmic lipid droplets. DHA itself was not incorporated into sphingolipids; however, it significantly altered representation of individual ceramide (Cer) classes, in particular in combination with NaBt (DHA/NaBt). We observed altered expression of enzymes involved in Cer metabolism in cells treated with NaBt or DHA/NaBt, and exogenous Cer 16:0 was found to promote induction of apoptosis in differentiating HT-29 cells. NaBt, together with DHA, increased n-3 fatty acid synthesis and attenuated metabolism of monounsaturated fatty acids. Finally, DHA and/or NaBt altered expression of proteins involved in synthesis of fatty acids, including elongase 5, stearoyl CoA desaturase 1, or fatty acid synthase, with NaBt increasing expression of caveolin-1 and CD36 transporter, which may further promote DHA incorporation and its impact on cellular lipidome. In conclusion, our results indicate that interactions of DHA and NaBt exert complex changes in cellular lipidome, which may contribute to the alterations of colon cancer cell differentiation/apoptotic responses. The present data extend our knowledge about the nature of interactive effects of dietary fatty acids.
引用
收藏
页码:4664 / 4679
页数:16
相关论文
共 50 条
[1]   Lipid bodies are reservoirs of cyclooxygenase-2 and sites of prostaglandin-E2 synthesis in colon cancer cells [J].
Accioly, Maria T. ;
Pacheco, Patricia ;
Maya-Monteiro, Clarissa M. ;
Carrossini, Nina ;
Robbs, Bruno K. ;
Oliveira, Silvia S. ;
Kaufmann, Cristiane ;
Morgado-Diaz, Jose A. ;
Bozza, Patricia T. ;
Viola, Joao P. B. .
CANCER RESEARCH, 2008, 68 (06) :1732-1740
[2]   Short-Chain Fatty Acids Stimulate Angiopoietin-Like 4 Synthesis in Human Colon Adenocarcinoma Cells by Activating Peroxisome Proliferator-Activated Receptor γ [J].
Alex, Sheril ;
Lange, Katja ;
Amolo, Tom ;
Grinstead, Jeffrey S. ;
Haakonsson, Anders K. ;
Szalowska, Ewa ;
Koppen, Arjen ;
Mudde, Karin ;
Haenen, Danielle ;
Al-Lahham, Sa'ad ;
Roelofsen, Han ;
Houtman, Rene ;
van der Burg, Bart ;
Mandrup, Susanne ;
Bonvin, Alexandre M. J. J. ;
Kalkhoven, Eric ;
Muller, Michael ;
Hooiveld, Guido J. ;
Kersten, Sander .
MOLECULAR AND CELLULAR BIOLOGY, 2013, 33 (07) :1303-1316
[3]  
BLIGH EG, 1959, CAN J BIOCHEM PHYS, V37, P911
[4]   Immunomodulation by omega-3 fatty acids [J].
Calder, Philip C. .
PROSTAGLANDINS LEUKOTRIENES AND ESSENTIAL FATTY ACIDS, 2007, 77 (5-6) :327-335
[5]   Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine [J].
Chapkin, Robert S. ;
Seo, Jeongmin ;
McMurray, David N. ;
Lupton, Joanne R. .
CHEMISTRY AND PHYSICS OF LIPIDS, 2008, 153 (01) :14-23
[6]   Nuclear receptors and lipid physiology: Opening the X-files [J].
Chawla, A ;
Repa, JJ ;
Evans, RM ;
Mangelsdorf, DJ .
SCIENCE, 2001, 294 (5548) :1866-1870
[7]   Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation [J].
Cohen, AW ;
Razani, B ;
Schubert, W ;
Williams, TM ;
Wang, XB ;
Iyengar, P ;
Brasaemle, DL ;
Scherer, PE ;
Lisanti, MP .
DIABETES, 2004, 53 (05) :1261-1270
[8]   Basic aspects of tumor cell fatty acid-regulated signaling and transcription factors [J].
Comba, Andrea ;
Lin, Yi-Hui ;
Renato Eynard, Aldo ;
Ana Valentich, Mirta ;
Fernandez-Zapico, Martin Ernesto ;
Eugenia Pasqualini, Maria .
CANCER AND METASTASIS REVIEWS, 2011, 30 (3-4) :325-342
[9]   Caveolin-1 is transcribed from a hypermethylated promoter to mediate colonocyte differentiation and apoptosis [J].
Dasgupta, Nirmalya ;
Thakur, Bhupesh Kumar ;
Ta, Atri ;
Das, Santasabuj .
EXPERIMENTAL CELL RESEARCH, 2015, 334 (02) :323-336
[10]   Protective action of n-3 fatty acids on benzo[a]pyrene-induced apoptosis through the plasma membrane remodeling-dependent NHE1 pathway [J].
Dendele, Beatrice ;
Tekpli, Xavier ;
Hardonniere, Kevin ;
Holme, Jorn A. ;
Debure, Laure ;
Catheline, Daniel ;
Arlt, Volker M. ;
Nagy, Eszter ;
Phillips, David H. ;
Ovrebo, Steinar ;
Mollerup, Steen ;
Poet, Mallory ;
Chevanne, Martine ;
Rioux, Vincent ;
Dimanche-Boitrel, Marie-Therese ;
Sergent, Odile ;
Lagadic-Gossmann, Dominique .
CHEMICO-BIOLOGICAL INTERACTIONS, 2014, 207 :41-51