Bacterial monocultures, propionate, butyrate and H2O2 modulate the expression, secretion and structure of the fasting-induced adipose factor in gut epithelial cell lines

Environmental Microbiology

Volumn 13, Issue 7, 2011, Pages 1778-1789

  Grootaert, Charlotte ^a   Van de Wiele, Tom ^a   Van Roosbroeck, Ilse ^a   Possemiers, Sam ^a   Vercoutter Edouart, Anne Sophie ^b   Verstraete, Willy ^a   Bracke, Marc ^c   Vanhoecke, Barbara ^c  

^a GHENT UNIVERSITY   (Belgium)

^b UNIV LILLE   (France)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN; ANGPTL4 PROTEIN, HUMAN; BUTYRIC ACID DERIVATIVE; HYDROGEN PEROXIDE; ISOPROTEIN; PROPIONIC ACID DERIVATIVE;

ARTICLE; BACTERIUM; BACTERIUM ADHERENCE; CELL STRAIN CACO 2; CELL STRAIN HCT116; DIET RESTRICTION; EPITHELIUM CELL; GLYCOSYLATION; HUMAN; METABOLISM; SECRETION;

ANGIOPOIETINS; BACTERIA; BACTERIAL ADHESION; BUTYRATES; CACO-2 CELLS; EPITHELIAL CELLS; FASTING; GLYCOSYLATION; HCT116 CELLS; HUMANS; HYDROGEN PEROXIDE; PROPIONATES; PROTEIN ISOFORMS;

BACTERIA (MICROORGANISMS); BACTEROIDES THETAIOTAOMICRON; CLOSTRIDIUM PERFRINGENS; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI;

EID: 79959829730     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02482.x     Document Type: Article

References (54)

1. Are, A., Aronsson, L., Wang, S., Greicius, G., Lee, Y.K., Gustafsson, J.-Ã., etal. (2008) Enterococcus faecalis from newborn babies regulate endogenous PPARγ activity and IL-10 levels in colonic epithelial cells. Proc Natl Acad Sci USA 105: 1943-1948.
2. Aronsson, L., Huang, Y., Parini, P., Korach-André, M., Hakansson, J., Gustafsson, J.A., etal. (2010) Decreased fat storage by Lactobacillus paracasei is associated with increased levels of angiopoietin-like 4 protein (ANGPTL4). PLoS ONE 5: e13078.
3. Bäckhed, F., Ding, H., Wang, T., Hooper, L.V., Koh, G.Y., Nagy, A., etal. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101: 15718-15723.
4. Bäckhed, F., Manchester, J.K., Semenkovich, C.F., and Gordon, J.I. (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 104: 979-984.
5. Banerjee, D., Jacob, J., Kunjamma, G., Madhusoodanan, U.K., and Ghosh, S. (2004) Measurement of urinary hydrogen peroxide by FOX-1 method in conjunction with catalase in diabetes mellitus: a sensitive and specific approach. Clin Chim Acta 350: 233-236.
6. Belanger, A.J., Lu, H., Date, T., Liu, L.X., Vincent, K.A., Akita, G.Y., etal. (2002) Hypoxia up-regulates expression of peroxisome proliferator-activated receptor γ angiopoietin-related gene (PGAR) in cardiomyocytes: role of hypoxia inducible factor 1α. J Mol Cell Cardiol 34: 765-774.
7. Bernet, M.F., Brassart, D., Neeser, J.R., and Servin, A.L. (1993) Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl Environ Microbiol 59: 4121-4128.
8. Bhattacharjee, R.N., Park, K.S., Uematsu, S., Okada, K., Hoshino, K., Takeda, K., etal. (2005) Escherichia coli verotoxin 1 mediates apoptosis in human HCT116 colon cancer cells by inducing overexpression of the GADD family of genes and S phase arrest. FEBS Lett 579: 6604-6610.
9. Brown, R.E., Imran, A., Belsham, D.D., Ur, E., and Wilkinson, M. (2006) Regulation of brain-derived resistin and FIAF in a novel hypothalamic neuronal cell line. Endocr Abstr 11: 280.
10. Brown, R., Imran, S.A., and Wilkinson, M. (2009) Lipopolysaccharide (LPS) stimulates adipokine and socs3 gene expression in mouse brain and pituitary gland in vivo, and in N-1 hypothalamic neurons in vitro. J Neuroimmunol 209: 96-103.
11. Chantret, I., Barbat, A., Dussaulx, E., Brattain, M.G., and Zweibaum, A. (1988) Epithelial polarity, villin expression, and enterocytic differentiation of cultured human colon carcinoma cells: a survey of twenty cell lines. Cancer Res 48: 1936-1942.
12. Cummings, J.H. (1981) Short chain fatty acids in the human colon. Gut 22: 763-779.
13. Cummings, J.H., Pomare, E.W., Branch, W.J., Naylor, C.P., and Macfarlane, G.T. (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28: 1221-1227.
14. De Boever, P., Deplancke, B., and Verstraete, W. (2000) Fermentation by gut microbiota cultured in a simulator of the human intestinal microbial ecosystem is improved by supplementing a soygerm powder. J Nutr 130: 2599-2606.
15. Dutton, S., and Trayhurn, P. (2008) Regulation of angiopoietin-like protein 4/fasting-induced adipose factor (ANGPTL4/FIAF) expression in mouse white adipose tissue and 3T3-L1 adipocytes. Br J Nutr 100: 18-26.
16. Fleissner, C.K., Huebel, N., Abd El-Bary, M.M., Loh, G., Klaus, S., and Blaut, M. (2010) Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br J Nutr 104: 919-929.
17. Galaup, A., Cazes, A., Le Jan, S., Philippe, J., Connault, E., Le Coz, E., etal. (2006) Angiopoietin-like 4 prevents metastasis through inhibition of vascular permeability and tumor cell motility and invasiveness. Proc Natl Acad Sci USA 103: 18721-18726.
18. Ge, H., Yang, G., Huang, L., Motola, D.L., Pourbahrami, T., and Li, C. (2004) Oligomerization and regulated proteolytic processing of angiopoietin-like protein 4. J Biol Chem 279: 2038-2045.
19. Hamer, H.M., Jonkers, D., Venema, K., Vanhoutvin, S., Troost, F.J., and Brummer, J.R. (2008) Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27: 104-119.
20. Henriksson, A., Szewzyk, R., and Conway, P.L. (1991) Characteristics of the adhesive determinants of Lactobacillus fermentum 104. Appl Environ Microbiol 57: 499-502.
21. Huycke, M.M., Abrams, V., and Moore, D.R. (2002) Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis 23: 529-536.
22. Ishizu, K., Sunose, N., Yamazaki, K., Tsuruo, T., Sadahiro, S., Makuuchi, H., and Yamori, T. (2007) Development and characterization of a model of liver metastasis using human colon cancer HCT-116 cells. Biol Pharm Bull 30: 1779-1783.
23. Kersten, S., Mandard, S., Tan, N.S., Escher, P., Metzger, D., Chambon, P., etal. (2000) Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J Biol Chem 275: 28488-28493.
24. Kersten, S., Lichtenstein, L., Steenbergen, E., Mudde, K., Hendriks, H.F., Hesselink, M.K., etal. (2009) Caloric restriction and exercise increase plasma ANGPTL4 levels in humans via elevated free fatty acids. Arterioscler Thromb Vasc Biol 29: 969-974.
25. Kim, Y., Lee, D., Kim, D., Cho, J., Yang, J., Chung, M., etal. (2008) Inhibition of proliferation in colon cancer cell lines and harmful enzyme activity of colon bacteria by Bifidobacterium adolescentis SPM0212. Arch Pharm Res 31: 468-473.
26. Koliwad, S.K., Kuo, T., Shipp, L.E., Gray, N.E., Bäckhed, F., So, A.Y., etal. (2009) Angiopoietin-like 4 (ANGPTL4/FIAF) is a direct glucocorticoid receptor target and participates in glucocorticoid-regulated triglyceride metabolism. J Biol Chem 284: 25593-25601.
27. Le Jan, S., Amy, C., Cazes, A., Monnot, C., Lamande, N., Favier, J., etal. (2003) Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am J Pathol 162: 1521-1528.
28. Lee, Y.-K., and Puong, K.Y. (2002) Competition for adhesion between probiotics and human gastrointestinal pathogens in the presence of carbohydrate. Br J Nutr 88: S101-S108.
29. Lee, E.C., Desai, U., Gololobov, G., Hong, S., Feng, X., Yu, X.C., etal. (2009) Identification of a new functional domain in angiopoietin-like 3 (ANGPTL3) and angiopoietin-like 4 (ANGPTL4) involved in binding and inhibition of lipoprotein lipase (LPL). J Biol Chem 284: 13735-13745.
30. Lichtenstein, L., and Kersten, S. (2010) Modulation of plasma TG lipolysis by angiopoietin-like proteins and GPIHBP1. Biochim Biophys Acta Mol Cell Biol Lipids 1801: 415-420.
31. Lichtenstein, L., Berbee, J.F., van Dijk, S.J., van Dijk, K.W., Bensadoun, A., Kema, I.P., etal. (2007) ANGPTL4 upregulates cholesterol synthesis in liver via inhibition of LPL- and HL-dependent hepatic cholesterol uptake. Arterioscler Thromb Vasc Biol 27: 2420-2427.
32. Lu, B., Moser, A., Shigenaga, J.K., Grunfeld, C., and Feingold, K.R. (2010) The acute phase response stimulates the expression of angiopoietin like protein 4. Biochem Biophys Res Commun 391: 1737-1741.
33. Mandard, S., Zandbergen, F., Tan, N.S., Escher, P., Patsouris, D., Koenig, W., etal. (2004) The direct peroxisome proliferator-activated receptor target fasting-induced adipose factor (FIAF/PGAR/ANGPTL4) is present in blood plasma as a truncated protein that is increased by fenofibrate treatment. J Biol Chem 279: 34411-34420.
34. Mandard, S., Zandbergen, F., van Straten, E., Wahli, W., Kuipers, F., Muller, M., and Kersten, S. (2006) The fasting-induced adipose factor/angiopoietin-like protein 4 is physically associated with lipoproteins and governs plasma lipid levels and adiposity. J Biol Chem 281: 934-944.
35. Masco, L., Huys, G., De Brandt, E., Temmerman, R., and Swings, J. (2005) Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. Int J Food Microbiol 102: 221-230.
36. Murata, M., Yudo, K., Nakamura, H., Chiba, J., Okamoto, K., Suematsu, N., etal. (2009) Hypoxia upregulates the expression of angiopoietin-like-4 in human articular chondrocytes: role of angiopoietin-like-4 in the expression of matrix metalloproteinases and cartilage degradation. J Orthop Res 27: 50-57.
37. Padua, D., Zhang, X.H., Wang, Q., Nadal, C., Gerald, W.L., Gomis, R.R., and Massague, J. (2008) TGFβ primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133: 66-77.
38. Rajput, A., Dominguez San Martin, I., Rose, R., Beko, A., Levea, C., Sharratt, E., etal. (2008) Characterization of HCT116 human colon cancer cells in an orthotopic model. J Surg Res 147: 276-281.
39. Schwab, M., Reynders, V., Ulrich, S., Zahn, N., Stein, J., and Schröder, O. (2006) PPARγ is a key target of butyrate-induced caspase-3 activation in the colorectal cancer cell line Caco-2. Apoptosis 11: 1801-1811.
40. Shan, L., Yu, X.C., Liu, Z., Hu, Y., Sturgis, L.T., Miranda, M.L., and Liu, Q. (2009) The angiopoietin-like proteins ANGPTL3 and ANGPTL4 inhibit lipoprotein lipase activity through distinct mechanisms. J Biol Chem 284: 1419-1424.
41. Simiantonaki, N., Taxeidis, M., Jayasinghe, C., Kurzik-Dumke, U., and Kirkpatrick, C. (2008) Hypoxia-inducible factor 1 α expression increases during colorectal carcinogenesis and tumor progression. BMC Cancer 8: 320.
42. Stapleton, C.M., Joo, J.H., Kim, Y.-S., Liao, G., Panettieri, R.A., Jr, and Jetten, A.M. (2010) Induction of ANGPTL4 expression in human airway smooth muscle cells by PMA through activation of PKC and MAPK pathways. Exp Cell Res 316: 507-516.
43. Takahashi, K., Sugi, Y., Hosono, A., and Kaminogawa, S. (2009) Epigenetic regulation of TLR4 gene expression in intestinal epithelial cells for the maintenance of intestinal homeostasis. J Immunol 183: 6522-6529.
44. Verine, J., Lehmann-Che, J., Soliman, H., Feugeas, J.P., Vidal, J.S., Mongiat-Artus, P., etal. (2010) Determination of angptl4 mRNA as a diagnostic marker of primary and metastatic clear cell renal-cell carcinoma. PLoS ONE 5: e10421.
45. Voltan, S., Martines, D., Elli, M., Brun, P., Longo, S., Porzionato, A., etal. (2008) Lactobacillus crispatus M247-derived H2O2 acts as a signal transducing molecule activating peroxisome proliferator activated receptor γ in the intestinal mucosa. Gastroenterology 135: 1216-1227.
46. Wächtershäuser, A., and Stein, J. (2000) Rationale for the luminal provision of butyrate in intestinal diseases. Eur J Nutr 39: 164-171.
47. Xu, A., Lam, M.C., Chan, K.W., Wang, Y., Zhang, J., Hoo, R.L., etal. (2005) Angiopoietin-like protein 4 decreases blood glucose and improves glucose tolerance but induces hyperlipidemia and hepatic steatosis in mice. Proc Natl Acad Sci USA 102: 6086-6091.
48. Yang, Y.-H., Wang, Y., Lam, K.S.L., Yau, M.-H., Cheng, K.K.Y., Zhang, J., etal. (2008) Suppression of the Raf/MEK/ERK signaling cascade and inhibition of angiogenesis by the carboxyl terminus of angiopoietin-like protein 4. Arterioscler Thromb Vasc Biol 28: 835-840.
49. Yoon, J.C., Chickering, T.W., Rosen, E.D., Dussault, B., Qin, Y., Soukas, A., etal. (2000) Peroxisome proliferator-activated receptor γ target gene encoding a novel angiopoietin-related protein associated with adipose differentiation. Mol Cell Biol 20: 5343-5349.
50. Yu, H.-B., Li, D.-Y., Zhang, H.-F., Xue, H.-Z., Pan, C.-E., Zhao, S.-H., and Wang, L. (2010) Resveratrol inhibits invasion and metastasis of hepatocellular carcinoma cells. J Anim Vet Adv 9: 3117-3124.
51. Zandbergen, F., van Dijk, S., and Kersten, S. (2006) Fasting-induced adipose factor/angiopoietin-like protein 4: a potential target for dyslipidemia? Future Lipidol 1: 227-236.
52. Zgouras, D., Wächtershäuser, A., Frings, D., and Stein, J. (2003) Butyrate impairs intestinal tumor cell-induced angiogenesis by inhibiting HIF-1α nuclear translocation. Biochem Biophys Res Commun 300: 832-838.
53. Zhao, L., Kwon, M.J., Huang, S., Lee, J.Y., Fukase, K., Inohara, N., and Hwang, D.H. (2007) Differential modulation of Nods signaling pathways by fatty acids in human colonic epithelial HCT116 cells. J Biol Chem 282: 11618-11628.
54. Zweibaum, A., Pinto, M., Chevalier, G., Dussaulx, E., Triadou, N., Lacroix, B., etal. (1985) Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose. J Cell Physiol 122: 21-29.