Mice lacking neutral amino acid transporter B0AT1 (Slc6a19) have elevated levels of FGF21 and GLP-1 and improved glycaemic control

Molecular Metabolism

Volumn 4, Issue 5, 2015, Pages 406-417

  Jiang, Yang ^a   Rose, Adam J ^b   Sijmonsma, Tjeerd P ^b   Bröer, Angelika ^a   Pfenninger, Anja ^c   Herzig, Stephan ^b   Schmoll, Dieter ^c   Bröer, Stefan ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c SANOFI AVENTIS DEUTSCHLAND GMBH   (Germany)

Author keywords

Amino acid metabolism; Epithelial transport; Type 2 diabetes

Indexed keywords

3 METHYLHISTIDINE; AMINO ACID TRANSPORTER; CHOLESTEROL; CREATININE; FATTY ACID; FIBROBLAST GROWTH FACTOR 21; GLUCAGON LIKE PEPTIDE 1; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; KETONE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN S6; PROTEIN SLC6A19; PYRUVIC ACID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1;

ABDOMINAL SUBCUTANEOUS FAT; AMINO ACID ANALYSIS; AMINO ACID METABOLISM; AMINO ACID TRANSPORT; AMINO ACID URINE LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; ENERGY EXPENDITURE; FEMALE; GLUCOSE TOLERANCE; GLUCOSE TRANSPORT; GLYCEMIC CONTROL; INSULIN RELEASE; INSULIN SENSITIVITY; INTESTINE ABSORPTION; INTRACELLULAR SIGNALING; LIVER LEVEL; LIVER WEIGHT; MALE; METABOLIC REGULATION; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; UPREGULATION; WHITE ADIPOSE TISSUE;

MUS;

EID: 84933677558     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2015.02.003     Document Type: Article

References (64)

1. Tremblay F., Lavigne C., Jacques H., Marette A. Role of dietary proteins and amino acids in the pathogenesis of insulin resistance. Annual Review of Nutrition 2007, 27:293-310.
2. Krebs M., Krssak M., Bernroider E., Anderwald C., Brehm A., Meyerspeer M., et al. Mechanism of amino acid-induced skeletal muscle insulin resistance in humans. Diabetes 2002, 51:599-605.
3. Tessari P., Inchiostro S., Biolo G., Duner E., Nosadini R., Tiengo A., et al. Hyperaminoacidaemia reduces insulin-mediated glucose disposal in healthy man. Diabetologia 1985, 28:870-872.
4. Shah O.J., Wang Z., Hunter T. Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Current Biology 2004, 14:1650-1656.
5. Copps K.D., White M.F. Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia 2012, 55:2565-2582.
6. Macotela Y., Emanuelli B., Bang A.M., Espinoza D.O., Boucher J., Beebe K., et al. Dietary leucine-an environmental modifier of insulin resistance acting on multiple levels of metabolism. PLoS One 2011, 6:e21187.
7. Zhang Y., Guo K., LeBlanc R.E., Loh D., Schwartz G.J., Yu Y.H. Increasing dietary leucine intake reduces diet-induced obesity and improves glucose and cholesterol metabolism in mice via multimechanisms. Diabetes 2007, 56:1647-1654.
8. Bernard J.R., Liao Y.H., Hara D., Ding Z., Chen C.Y., Nelson J.L., et al. An amino acid mixture improves glucose tolerance and insulin signaling in Sprague-Dawley rats. American Journal of Physiology. Endocrinology and Metabolism 2011, 300:E752-E760.
9. Xiao F., Huang Z., Li H., Yu J., Wang C., Chen S., et al. Leucine deprivation increases hepatic insulin sensitivity via GCN2/mTOR/S6K1 and AMPK pathways. Diabetes 2011, 60:746-756.
10. Lu J., Xie G., Jia W. Insulin resistance and the metabolism of branched-chain amino acids. Frontier Medical 2013, 7:53-59.
11. Solon-Biet S.M., McMahon A.C., Ballard J.W., Ruohonen K., Wu L.E., Cogger V.C., et al. The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metabolism 2014, 19:418-430.
12. Newgard C.B., An J., Bain J.R., Muehlbauer M.J., Stevens R.D., Lien L.F., et al. Abranched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metabolism 2009, 9:311-326.
13. Wang T.J., Larson M.G., Vasan R.S., Cheng S., Rhee E.P., McCabe E., et al. Metabolite profiles and the risk of developing diabetes. Nature Medicine 2011, 17:448-453.
14. Newgard C.B. Interplay between lipids and branched-chain amino acids in development of insulin resistance. Cell Metabolism 2012, 15:606-614.
15. Kilberg M.S., Shan J., Su N. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends in Endocrinology & Metabolism 2009, 20:436-443.
16. Krokowski D., Han J., Saikia M., Majumder M., Yuan C.L., Guan B.J., et al. Aself-defeating anabolic program leads to beta-cell apoptosis in endoplasmic reticulum stress-induced diabetes via regulation of amino acid flux. The Journal of Biological Chemistry 2013, 288:17202-17213.
17. Laeger T., Henagan T.M., Albarado D.C., Redman L.M., Bray G.A., Noland R.C., et al. FGF21 is an endocrine signal of protein restriction. The Journal of Clinical Investigation 2014, 124:3913-3922.
18. De Sousa-Coelho A.L., Marrero P.F., Haro D. Activating transcription factor 4-dependent induction of FGF21 during amino acid deprivation. The Biochemical Journal 2012, 443:165-171.
19. Kharitonenkov A., Adams A.C. Inventing new medicines: the FGF21 story. Molecular Metabolism 2014, 3:221-229.
20. Owen B.M., Mangelsdorf D.J., Kliewer S.A. Tissue-specific actions of the metabolic hormones FGF15/19 and FGF21. Trends in Endocrinology and Metabolism: TEM 2015, 26:22-29.
21. Adams A.C., Yang C., Coskun T., Cheng C.C., Gimeno R.E., Luo Y., et al. The breadth of FGF21's metabolic actions are governed by FGFR1 in adipose tissue. Molecular Metabolism 2012, 2:31-37.
22. Holland W.L., Adams A.C., Brozinick J.T., Bui H.H., Miyauchi Y., Kusminski C.M., et al. An FGF21-adiponectin-ceramide axis controls energy expenditure and insulin action in mice. Cell Metabolism 2013, 17:790-797.
23. Reimann F., Williams L., da Silva Xavier G., Rutter G.A., Gribble F.M. Glutamine potently stimulates glucagon-like peptide-1 secretion from GLUTag cells. Diabetologia 2004, 47:1592-1601.
24. Thomas F.B., Mazzaferri E.L., Crockett S.E., Mekhjian H.S., Gruemer H.D., Cataland S. Stimulation of secretion of gastric inhibitory polypeptide and insulin by intraduodenal amino acid perfusion. Gastroenterology 1976, 70:523-527.
25. Westerterp-Plantenga M.S., Lemmens S.G., Westerterp K.R. Dietary protein - its role in satiety, energetics, weight loss and health. The British Journal of Nutrition 2012, 108(Suppl 2):S105-S112.
26. Simpson S.J., Raubenheimer D. Obesity: the protein leverage hypothesis. Obesity Reviews 2005, 6:133-142.
27. Journel M., Chaumontet C., Darcel N., Fromentin G., Tome D. Brain responses to high-protein diets. Advances in Nutrition 2012, 3:322-329.
28. Houde V.P., Brule S., Festuccia W.T., Blanchard P.G., Bellmann K., Deshaies Y., et al. Chronic rapamycin treatment causes glucose intolerance and hyperlipidemia by upregulating hepatic gluconeogenesis and impairing lipid deposition in adipose tissue. Diabetes 2010, 59:1338-1348.
29. Felig P. Amino acid metabolism in man. The Annual Review of Biochemistry 1975, 44:933-955.
30. Broer S. Amino acid transport across mammalian intestinal and renal epithelia. Physiological Reviews 2008, 88:249-286.
31. Broer A., Klingel K., Kowalczuk S., Rasko J.E., Cavanaugh J., Broer S. Molecular cloning of mouse amino acid transport system B0, a neutral amino acid transporter related to Hartnup disorder. The Journal of Biological Chemistry 2004, 279:24467-24476.
32. Broer A., Juelich T., Vanslambrouck J.M., Tietze N., Solomon P.S., Holst J., et al. Impaired nutrient signaling and body weight control in a Na+ neutral amino acid cotransporter (Slc6a19)-deficient mouse. The Journal of Biological Chemistry 2011, 286:26638-26651.
33. Nassl A.M., Rubio-Aliaga I., Fenselau H., Marth M.K., Kottra G., Daniel H. Amino acid absorption and homeostasis in mice lacking the intestinal peptide transporter PEPT1. The American Journal of Physiology-Gastrointestinal and Liver Physiology 2011, 301:G128-G137.
34. Broer S. The role of the neutral amino acid transporter B0AT1 (SLC6A19) in Hartnup disorder and protein nutrition. IUBMB Life 2009, 61:591-599.
35. Seow H.F., Broer S., Broer A., Bailey C.G., Potter S.J., Cavanaugh J.A., et al. Hartnup disorder is caused by mutations in the gene encoding the neutral amino acid transporter SLC6A19. Nature Genetics 2004, 36:1003-1007.
36. Kleta R., Romeo E., Ristic Z., Ohura T., Stuart C., Arcos-Burgos M., et al. Mutations in SLC6A19, encoding B0AT1, cause Hartnup disorder. Nature Genetics 2004, 36:999-1002.
37. Danilczyk U., Sarao R., Remy C., Benabbas C., Stange G., Richter A., et al. Essential role for collectrin in renal amino acid transport. Nature 2006, 444:1088-1091.
38. Kowalczuk S., Broer A., Tietze N., Vanslambrouck J.M., Rasko J.E., Broer S. Aprotein complex in the brush-border membrane explains a Hartnup disorder allele. Faseb Journal 2008, 22:2880-2887.
39. Tschop M.H., Speakman J.R., Arch J.R., Auwerx J., Bruning J.C., Chan L., et al. Aguide to analysis of mouse energy metabolism. Nature Methods 2012, 9:57-63.
40. Speakman J.R., Fletcher Q., Vaanholt L. The '39 steps': an algorithm for performing statistical analysis of data on energy intake and expenditure. Disease Models & Mechanisms 2013, 6:293-301.
41. Carpenter A.E., Jones T.R., Lamprecht M.R., Clarke C., Kang I.H., Friman O., et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biology 2006, 7:R100.
42. Levy L.L. Hartnup disorder. The metabolic & molecular bases of inherited diseases 2001, 4957-4969. McGraw-Hill, New York. C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle (Eds.).
43. Speakman J.R. Measuring energy metabolism in the mouse - theoretical, practical, and analytical considerations. Frontiers in Physiology 2013, 4:34.
44. Kharitonenkov A., Shiyanova T.L., Koester A., Ford A.M., Micanovic R., Galbreath E.J., et al. FGF-21 as a novel metabolic regulator. The Journal of Clinical Investigation 2005, 115:1627-1635.
45. Coskun T., Bina H.A., Schneider M.A., Dunbar J.D., Hu C.C., Chen Y., et al. Fibroblast growth factor 21 corrects obesity in mice. Endocrinology 2008, 149:6018-6027.
46. Iglesias P., Selgas R., Romero S., Diez J.J. Biological role, clinical significance, and therapeutic possibilities of the recently discovered metabolic hormone fibroblastic growth factor 21. European Journal of Endocrinology 2012, 167:301-309.
47. McMullen P.D., Bhattacharya S., Woods C.G., Sun B., Yarborough K., Ross S.M., et al. Amap of the PPARalpha transcription regulatory network for primary human hepatocytes. Chemico-Biological Interactions 2014, 209:14-24.
48. Mashili F.L., Austin R.L., Deshmukh A.S., Fritz T., Caidahl K., Bergdahl K., et al. Direct effects of FGF21 on glucose uptake in human skeletal muscle: implications for type 2 diabetes and obesity. Diabetes/Metabolism Research and Reviews 2011, 27:286-297.
49. Markan K.R., Naber M.C., Ameka M.K., Anderegg M.D., Mangelsdorf D.J., Kliewer S.A., et al. Circulating FGF21 is liver derived and enhances glucose uptake during refeeding and overfeeding. Diabetes 2014, 6:4057-4063.
50. Aguirre V., Werner E.D., Giraud J., Lee Y.H., Shoelson S.E., White M.F. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. The Journal of Biological Chemistry 2002, 277:1531-1537.
51. Hancer N.J., Qiu W., Cherella C., Li Y., Copps K.D., White M.F. Insulin and metabolic stress stimulate multisite serine/threonine phosphorylation of insulin receptor substrate 1 and inhibit tyrosine phosphorylation. The Journal of Biological Chemistry 2014, 289:12467-12484.
52. Rajan M.R., Fagerholm S., Jonsson C., Kjolhede P., Turkina M.V., Stralfors P. Phosphorylation of IRS1 at serine 307 in response to insulin in human adipocytes is not likely to be catalyzed by p70 ribosomal S6 kinase. PLoS One 2013, 8:e59725.
53. Nikolaidis L.A., Elahi D., Shen Y.T., Shannon R.P. Active metabolite of GLP-1 mediates myocardial glucose uptake and improves left ventricular performance in conscious dogs with dilated cardiomyopathy. American Journal of Physiology - Heart and Circulatory Physiology 2005, 289:H2401-H2408.
54. Giannocco G., Oliveira K.C., Crajoinas R.O., Venturini G., Salles T.A., Fonseca-Alaniz M.H., et al. Dipeptidyl peptidase IV inhibition upregulates GLUT4 translocation and expression in heart and skeletal muscle of spontaneously hypertensive rats. European Journal of Pharmacology 2013, 698:74-86.
55. Singer D., Camargo S.M., Ramadan T., Schafer M., Mariotta L., Herzog B., et al. Defective intestinal amino acid absorption in Ace2 null mice. The American Journal of Physiology-Gastrointestinal and Liver Physiology 2012, 303:G686-G695.
56. Young S.H., Rey O., Sternini C., Rozengurt E. Amino acid sensing by enteroendocrine STC-1 cells: role of the Na+-coupled neutral amino acid transporter 2. American Journal of Physiology. Cell Physiology 2010, 298:C1401-C1413.
57. Lindgren O., Pacini G., Tura A., Holst J.J., Deacon C.F., Ahren B. Incretin effect after oral amino acid ingestion in humans. The Journal of Clinical Endocrinology and Metabolism 2014, jc20143865 [epub ahead of print].
58. Lin Z., Tian H., Lam K.S., Lin S., Hoo R.C., Konishi M., et al. Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice. Cell Metabolism 2013, 17:779-789.
59. Badman M.K., Pissios P., Kennedy A.R., Koukos G., Flier J.S., Maratos-Flier E. Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metabolism 2007, 5:426-437.
60. Niu M.J., Yang J.K., Lin S.S., Ji X.J., Guo L.M. Loss of angiotensin-converting enzyme 2 leads to impaired glucose homeostasis in mice. Endocrine 2008, 34:56-61.
61. Bernardi S., Tikellis C., Candido R., Tsorotes D., Pickering R.J., Bossi F., et al. ACE2 deficiency shifts energy metabolism towards glucose utilization. Metabolism 2015, 64:406-415.
62. Biden T.J., Boslem E., Chu K.Y., Sue N. Lipotoxic endoplasmic reticulum stress, beta cell failure, and type 2 diabetes mellitus. Trends in Endocrinology and Metabolism: TEM 2014, 25:389-398.
63. Malakauskas S.M., Kourany W.M., Zhang X.Y., Lu D., Stevens R.D., Koves T.R., et al. Increased insulin sensitivity in mice lacking collectrin, a downstream target of HNF-1alpha. Molecular Endocrinology 2009, 23:881-892.
64. She P., Reid T.M., Bronson S.K., Vary T.C., Hajnal A., Lynch C.J., et al. Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metabolism 2007, 6:181-194.