Loss of angiopoietin-like 4 (ANGPTL4) in mice with diet-induced obesity uncouples visceral obesity from glucose intolerance partly via the gut microbiota

Diabetologia

Volumn 61, Issue 6, 2018, Pages 1447-1458

  Janssen, Aafke W F ^a   Katiraei, Saeed ^b   Bartosinska, Barbara ^c,d   Eberhard, Daniel ^c,d   Willems van Dijk, Ko ^b   Kersten, Sander ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

Author keywords

Angiopoietin like 4; Antibiotics; Glucose tolerance; Gut microbiota; Insulin secretion; White adipose tissue

Indexed keywords

AMPICILLIN; ANGIOPOIETIN RELATED PROTEIN 4; CHOLESTEROL; DRINKING WATER; FRUCTOSE; GLUCOSE; INSULIN; LIPOPROTEIN LIPASE; METRONIDAZOLE; NEOMYCIN; UNSATURATED FATTY ACID; ANGPTL4 PROTEIN, MOUSE; FATTY ACID;

ADLERCREUTZIA; ALLOBACULUM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT GAIN; CLOSTRIDIACEAE; CONTROLLED STUDY; DIET INDUCED OBESITY; ENZYME ACTIVITY; FAT MASS; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; INFLAMMATION; INSULIN LEVEL; INSULIN RELEASE; INTESTINE FLORA; INTRA-ABDOMINAL FAT; LACHNOSPIRACEAE; LACTOBACILLUS; MALE; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; OBESITY; PANCREAS ISLET; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEPLETION; ABDOMINAL OBESITY; ANIMAL; BODY WEIGHT; C57BL MOUSE; GENETICS; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; INSULIN RESISTANCE; LIPID DIET; METABOLISM; PERMEABILITY; PHENOTYPE;

ANGIOPOIETIN-LIKE 4 PROTEIN; ANIMALS; BODY WEIGHT; DIET, HIGH-FAT; FATTY ACIDS; FRUCTOSE; GASTROINTESTINAL MICROBIOME; GLUCOSE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; INSULIN; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; MALE; MICE; MICE, INBRED C57BL; OBESITY; OBESITY, ABDOMINAL; PERMEABILITY; PHENOTYPE; WEIGHT GAIN;

EID: 85044937071     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-018-4583-5     Document Type: Article

References (50)

1. Redinger RN (2007) The pathophysiology of obesity and its clinical manifestations. Gastroenterol Hepatol 3:856–863
2. Voshol PJ, Rensen PCN, van Dijk KW et al (2009) Effect of plasma triglyceride metabolism on lipid storage in adipose tissue: studies using genetically engineered mouse models. Biochim Biophys Acta 1791:479–485
3. Kersten S (2014) Physiological regulation of lipoprotein lipase. Biochim Biophys Acta 1841:919–933
4. Davies BSJ, Beigneux AP, Barnes RH et al (2010) GPIHBP1 is responsible for the entry of lipoprotein lipase into capillaries. Cell Metab 12:42–52
5. Beigneux AP, Davies BSJ, Gin P et al (2007) Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons. Cell Metab 5:279–291
6. Dijk W, Kersten S (2016) Regulation of lipid metabolism by angiopoietin-like proteins. Curr Opin Lipidol 27:249–256
7. Dijk W, Heine M, Vergnes L et al (2015) ANGPTL4 mediates shuttling of lipid fuel to brown adipose tissue during sustained cold exposure. elife 4:e08428
8. Catoire M, Alex S, Paraskevopulos N et al (2014) Fatty acid-inducible ANGPTL4 governs lipid metabolic response to exercise. Proc Natl Acad Sci U S A 111:E1043–E1052
9. Kroupa O, Vorrsjö E, Stienstra R et al (2012) Linking nutritional regulation of Angptl4, Gpihbp1, and Lmf1 to lipoprotein lipase activity in rodent adipose tissue. BMC Physiol 12:13
10. Mattijssen F, Alex S, Swarts HJ et al (2014) Angptl4 serves as an endogenous inhibitor of intestinal lipid digestion. Mol Metab 3:135–144
11. Köster A, Chao YB, Mosior M et al (2005) Transgenic angiopoietin-like (angptl)4 overexpression and targeted disruption of angptl4 and angptl3: regulation of triglyceride metabolism. Endocrinology 146:4943–4950
12. Xu A, Lam MC, Chan KW et al (2005) Angiopoietin-like protein 4 decreases blood glucose and improves glucose tolerance but induces hyperlipidemia and hepatic steatosis in mice. Proc Natl Acad Sci U S A 102:6086–6091
13. Wang Y, Liu LM, Wei L et al (2016) Angiopoietin-like protein 4 improves glucose tolerance and insulin resistance but induces liver steatosis in high-fat-diet mice. Mol Med Rep 14:3293–3300
14. Mandard S, Zandbergen F, van Straten E et al (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
15. Lichtenstein L, Berbée JFP, van Dijk SJ et al (2007) Angptl4 upregulates cholesterol synthesis in liver via inhibition of LPL- and HL-dependent hepatic cholesterol uptake. Arterioscler Thromb Vasc Biol 27:2420–2427
16. Lichtenstein L, Mattijssen F, de Wit NJ et al (2010) Angptl4 protects against severe proinflammatory effects of saturated fat by inhibiting fatty acid uptake into mesenteric lymph node macrophages. Cell Metab 12:580–592
17. −/− mice trans fat promotes foam cell formation in mesenteric lymph nodes without leading to ascites. J Lipid Res 58:1100–1113
18. Janssen AWF, Houben T, Katiraei S et al (2017) Modulation of the gut microbiota impacts non-alcoholic fatty liver disease: a potential role for bile acids. J Lipid Res 58:1399–1416
19. Basciano H, Federico L, Adeli K (2005) Fructose, insulin resistance, and metabolic dyslipidemia. Nutr Metab 2:5
20. Chung S, Parks JS (2015) Dietary cholesterol effects on adipose tissue inflammation. Curr Opin Lipidol 27:19–25
21. Janssen AWF, Dijk W, Boekhorst J et al (2017) ANGPTL4 promotes bile acid absorption during taurocholic acid supplementation via a mechanism dependent on the gut microbiota. Biochim Biophys Acta Mol Cell Biol Lipids 1862:1056–1067
22. Ijssennagger N, Belzer C, Hooiveld GJ et al (2015) Gut microbiota facilitates dietary heme-induced epithelial hyperproliferation by opening the mucus barrier in colon. Proc Natl Acad Sci 112:10038–10043
23. Cruz WS, Kwon G, Marshall CA et al (2001) Glucose and insulin stimulate heparin-releasable lipoprotein lipase activity in mouse islets and INS-1 cells. A potential link between insulin resistance and beta-cell dysfunction. J Biol Chem 276:12162–12168
24. Pappan KL, Pan Z, Kwon G et al (2005) Pancreatic β-cell lipoprotein lipase independently regulates islet glucose metabolism and normal insulin secretion. J Biol Chem 280:9023–9029
25. Kreznar JH, Keller MP, Traeger LL et al (2017) Host genotype and gut microbiome modulate insulin secretion and diet-induced metabolic phenotypes. Cell Rep 18:1739–1750
26. Simon MC, Strassburger K, Nowotny B et al (2015) Intake of Lactobacillus reuteri improves incretin and insulin secretion in glucose-tolerant humans: a proof of concept. Diabetes Care 38:1827–1834
27. Bäckhed F, Ding H, Wang T et al (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101:15718–15723
28. Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A 104:979–984
29. Sukonina V, Lookene A, Olivecrona T, Olivecrona G (2006) Angiopoietin-like protein 4 converts lipoprotein lipase to inactive monomers and modulates lipase activity in adipose tissue. Proc Natl Acad Sci U S A 103:17450–17455
30. Lee E-C, Landes GM, Chung K, et al; Lexicon Pharmaceuticals, Inc, Monoclonal antibodies against ANGPTL4. US Patent 2006/0222645 A1. 6 Jan 2006
31. Mulder H, Yang S, So M et al (2004) Inhibition of lipase activity and lipolysis in rat islets reduces insulin secretion. Diabetes 53:122–128
32. Koyama K, Chen G, Wang MY et al (1997) Beta-cell function in normal rats made chronically hyperleptinemic by adenovirus-leptin gene therapy. Diabetes 46:1276–1280
33. Nyrén R, Chang CL, Lindström P et al (2012) Localization of lipoprotein lipase and GPIHBP1 in mouse pancreas: effects of diet and leptin deficiency. BMC Physiol 12:14
34. Kim H-K, Kwon O, Park K-H et al (2017) Angiopoietin-like peptide 4 regulates insulin secretion and islet morphology. Biochem Biophys Res Commun 485:113–118
35. Mehta N, Qamar A, Qu L et al (2014) Differential association of plasma angiopoietin-like proteins 3 and 4 with lipid and metabolic traits. Arterioscler Thromb Vasc Biol 34:1057–1063
36. Lotta LA, Gulati P, Day FR et al (2017) Integrative genomic analysis implicates limited peripheral adipose storage capacity in the pathogenesis of human insulin resistance. Nat Genet 49:17–26
37. Liu DJ, Peloso GM, Yu H et al (2017) Exome-wide association study of plasma lipids in >300,000 individuals. Nat Genet 49:1758–1766
38. Caesar R, Reigstad CS, Bäckhed HK et al (2012) Gut-derived lipopolysaccharide augments adipose macrophage accumulation but is not essential for impaired glucose or insulin tolerance in mice. Gut 61:1701–1707
39. Rabot S, Membrez M, Bruneau A et al (2010) Germ-free C57BL/6J mice are resistant to high-fat-diet-induced insulin resistance and have altered cholesterol metabolism. FASEB J 24:4948–4959
40. Hwang I, Park YJ, Kim YR et al (2015) Alteration of gut microbiota by vancomycin and bacitracin improves insulin resistance via glucagon-like peptide 1 in diet-induced obesity. FASEB J 29:2397–2411
41. Vrieze A, Van Nood E, Holleman F et al (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143:913–916
42. Ussar S, Griffin NW, Bezy O et al (2015) Interactions between gut microbiota, host genetics and diet modulate the predisposition to obesity and metabolic syndrome. Cell Metab 22:1–15
43. Karlsson FH, Tremaroli V, Nookaew I et al (2013) Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498:99–103
44. Priyadarshini M, Wicksteed B, Schiltz GE et al (2016) SCFA receptors in pancreatic β cells: novel diabetes targets? Trends Endocrinol Metab 27:653–664
45. Priyadarshini M, Villa SR, Fuller M et al (2015) An acetate-specific GPCR, FFAR2, regulates insulin secretion. Mol Endocrinol 29:1055–1066
46. Perry RJ, Peng L, Barry NA et al (2016) Acetate mediates a microbiome–brain–β-cell axis to promote metabolic syndrome. Nature 534:213–217
47. Amyot J, Semache M, Ferdaoussi M et al (2012) Lipopolysaccharides impair insulin gene expression in isolated islets of langerhans via toll-like receptor-4 and NF-kB signalling. PLoS One 7:e36200
48. Nguyen AT, Mandard S, Dray C et al (2014) Lipopolysaccharides-mediated increase in glucose-stimulated insulin secretion: involvement of the GLP-1 pathway. Diabetes 63:471–482
49. Setchell KDR, Clerici C (2010) Equol: history, chemistry, and formation. J Nutr 3:1355–1362
50. Cheong SH, Furuhashi K, Ito K et al (2014) Antihyperglycemic effect of equol, a daidzein derivative, in cultured L6 myocytes and ob/ob mice. Mol Nutr Food Res 58:267–277