A dual role of lipasin (betatrophin) in lipid metabolism and glucose homeostasis: Consensus and controversy

Cardiovascular Diabetology

Volumn 13, Issue 1, 2014, Pages

  Zhang, Ren ^a   Abou Samra, Abdul B ^a,b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HAMAD MEDICAL CORPORATION   (Qatar)

Author keywords

Angptl8; Betatrophin; C19orf80; Lipasin; RIFL

Indexed keywords

ANGIOPOIETIN; ANGIOPOIETIN LIKE 3 PROTEIN; ANGIOPOIETIN LIKE 4 PROTEIN; BETATROPHIN; GLUCOSE; LIPASIN; LIPID; RIFL PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; LIPASIN PROTEIN, HUMAN; PEPTIDE HORMONE;

ADIPOGENESIS; AUTOPHAGY; C19ORF80 GENE; CELL PROLIFERATION; CELLULAR PARAMETERS; CONSENSUS; GENE; GENETIC ASSOCIATION; GLUCOSE HOMEOSTASIS; GM6484 GENE; HUMAN; LIPID METABOLISM; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET BETA CELL MASS; PROTEIN FAMILY; REGULATORY MECHANISM; REVIEW; TRANSCRIPTION REGULATION; ANIMAL; GENOME-WIDE ASSOCIATION STUDY; HOMEOSTASIS; METABOLISM; PHYSIOLOGY;

ANIMALS; GENOME-WIDE ASSOCIATION STUDY; GLUCOSE; HOMEOSTASIS; HUMANS; LIPID METABOLISM; PEPTIDE HORMONES;

EID: 84908120785     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/s12933-014-0133-8     Document Type: Review

References (52)

1. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet 2005, 365:1415-1428. 10.1016/S0140-6736(05)66378-7, 15836891.
2. Grundy SM, Benjamin IJ, Burke GL, Chait A, Eckel RH, Howard BV, Mitch W, Smith SC, Sowers JR. Diabetes and cardiovascular disease: a statement for healthcare professionals from the American Heart Association. Circulation 1999, 100:1134-1146. 10.1161/01.CIR.100.10.1134, 10477542.
3. Klein S, Burke LE, Bray GA, Blair S, Allison DB, Pi-Sunyer X, Hong Y, Eckel RH. Clinical implications of obesity with specific focus on cardiovascular disease: a statement for professionals from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism: endorsed by the American College of Cardiology Foundation. Circulation 2004, 110:2952-2967. 10.1161/01.CIR.0000145546.97738.1E, 15509809.
4. Miller M, Stone NJ, Ballantyne C, Bittner V, Criqui MH, Ginsberg HN, Goldberg AC, Howard WJ, Jacobson MS, Kris-Etherton PM, Lennie TA, Levi M, Mazzone T, Pennathur S. Triglycerides and cardiovascular disease: a scientific statement from the American Heart Association. Circulation 2011, 123:2292-2333. 10.1161/CIR.0b013e3182160726, 21502576.
5. Haffner SM. Management of dyslipidemia in adults with diabetes. Diabetes Care 2003, 26(Suppl 1):S83-S86. 12502625.
6. Mooradian AD. Dyslipidemia in type 2 diabetes mellitus. Nat Clin Pract Endocrinol Metab 2009, 5:150-159. 10.1038/ncpendmet1066, 19229235.
7. Patsch JR, Miesenbock G, Hopferwieser T, Muhlberger V, Knapp E, Dunn JK, Gotto AM, Patsch W. Relation of triglyceride metabolism and coronary artery disease. Studies in the postprandial state. Arterioscler Thromb 1992, 12:1336-1345. 10.1161/01.ATV.12.11.1336, 1420093.
8. Kersten S. Physiological regulation of lipoprotein lipase. Biochim Biophys Acta 1841, 2014:919-933.
9. Santamarina-Fojo S, Brewer HB. The familial hyperchylomicronemia syndrome. New insights into underlying genetic defects. JAMA 1991, 265:904-908. 10.1001/jama.1991.03460070086049, 1992190.
10. Coleman T, Seip RL, Gimble JM, Lee D, Maeda N, Semenkovich CF. COOH-terminal disruption of lipoprotein lipase in mice is lethal in homozygotes, but heterozygotes have elevated triglycerides and impaired enzyme activity. J Biol Chem 1995, 270:12518-12525. 10.1074/jbc.270.21.12518, 7759497.
11. Weinstock PH, Bisgaier CL, Aalto-Setala K, Radner H, Ramakrishnan R, Levak-Frank S, Essenburg AD, Zechner R, Breslow JL. Severe hypertriglyceridemia, reduced high density lipoprotein, and neonatal death in lipoprotein lipase knockout mice. Mild hypertriglyceridemia with impaired very low density lipoprotein clearance in heterozygotes. J Clin Invest 1995, 96:2555-2568. 10.1172/JCI118319, 8675619.
12. Beigneux AP, Davies BS, Gin P, Weinstein MM, Farber E, Qiao X, Peale F, Bunting S, Walzem RL, Wong JS, Blaner WS, Ding ZM, Melford K, Wongsiriroj N, Shu X, de Sauvage F, Ryan RO, Fong LG, Bensadoun A, Young SG. Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons. Cell Metab 2007, 5:279-291. 10.1016/j.cmet.2007.02.002, 17403372.
13. Beigneux AP, Franssen R, Bensadoun A, Gin P, Melford K, Peter J, Walzem RL, Weinstein MM, Davies BS, Kuivenhoven JA, Kastelein JJ, Fong LG, Dallinga-Thie GM, Young SG. Chylomicronemia with a mutant GPIHBP1 (Q115P) that cannot bind lipoprotein lipase. Arterioscler Thromb Vasc Biol 2009, 29:956-962. 10.1161/ATVBAHA.109.186577, 19304573.
14. Gray KA, Daugherty LC, Gordon SM, Seal RL, Wright MW, Bruford EA. Genenames.org: the HGNC resources in 2013. Nucleic Acids Res 2013, 41:D545-D552. 10.1093/nar/gks1066, 23161694.
15. Ren G, Kim JY, Smas CM. Identification of RIFL, a novel adipocyte-enriched insulin target gene with a role in lipid metabolism. Am J Physiol Endocrinol Metab 2012, 303:E334-E351. 10.1152/ajpendo.00084.2012, 22569073.
16. Fu Z, Yao F, Abou-Samra AB, Zhang R. Lipasin, thermoregulated in brown fat, is a novel but atypical member of the angiopoietin-like protein family. Biochem Biophys Res Commun 2013, 430:1126-1131. 10.1016/j.bbrc.2012.12.025, 23261442.
17. Zhang R. Lipasin, a novel nutritionally-regulated liver-enriched factor that regulates serum triglyceride levels. Biochem Biophys Res Commun 2012, 424:786-792. 10.1016/j.bbrc.2012.07.038, 22809513.
18. Fu Z, Berhane F, Fite A, Seyoum B, Abou-Samra AB, Zhang R. Elevated circulating lipasin/betatrophin in human type 2 diabetes and obesity. Sci Rep 2014, 4:5013. 24852694.
19. Quagliarini F, Wang Y, Kozlitina J, Grishin NV, Hyde R, Boerwinkle E, Valenzuela DM, Murphy AJ, Cohen JC, Hobbs HH. Atypical angiopoietin-like protein that regulates ANGPTL3. Proc Natl Acad Sci U S A 2012, 109:19751-19756. 10.1073/pnas.1217552109, 23150577.
20. Wang Y, Quagliarini F, Gusarova V, Gromada J, Valenzuela DM, Cohen JC, Hobbs HH. Mice lacking ANGPTL8 (Betatrophin) manifest disrupted triglyceride metabolism without impaired glucose homeostasis. Proc Natl Acad Sci U S A 2013, 110:16109-16114. 10.1073/pnas.1315292110, 24043787.
21. Yi P, Park JS, Melton DA. Betatrophin: a hormone that controls pancreatic beta cell proliferation. Cell 2013, 153:747-758. 10.1016/j.cell.2013.04.008, 23623304.
22. Espes D, Lau J, Carlsson PO. Increased circulating levels of betatrophin in individuals with long-standing type 1 diabetes. Diabetologia 2014, 57:50-53. 10.1007/s00125-013-3071-1, 24078058.
23. Espes D, Martinell M, Carlsson PO. Increased circulating betatrophin concentrations in patients with type 2 diabetes. Int J Endocrinol 2014, 2014:323407. 10.1155/2014/323407, 24963292.
24. Fenzl A, Itariu BK, Kosi L, Fritzer-Szekeres M, Kautzky-Willer A, Stulnig TM, Kiefer FW. Circulating betatrophin correlates with atherogenic lipid profiles but not with glucose and insulin levels in insulin-resistant individuals. Diabetologia 2014, 57:1204-1208. 10.1007/s00125-014-3208-x, 24623100.
25. Tseng YH, Ke PY, Liao CJ, Wu SM, Chi HC, Tsai CY, Chen CY, Lin YH, Lin KH. Chromosome 19 open reading frame 80 is upregulated by thyroid hormone and modulates autophagy and lipid metabolism. Autophagy 2014, 10:20-31. 10.4161/auto.26126, 24262987.
26. Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, Handsaker RE, Kang HM, Marth GT, McVean GA. An integrated map of genetic variation from 1,092 human genomes. Nature 2012, 491:56-65. 10.1038/nature11632, 23128226.
27. Peloso GM, Auer PL, Bis JC, Voorman A, Morrison AC, Stitziel NO, Brody JA, Khetarpal SA, Crosby JR, Fornage M, Isaacs A, Jakobsdottir J, Feitosa MF, Davies G, Huffman JE, Manichaikul A, Davis B, Lohman K, Joon AY, Smith AV, Grove ML, Zanoni P, Redon V, Demissie S, Lawson K, Peters U, Carlson C, Jackson RD, Ryckman KK, Mackey RH, et al. Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks. Am J Hum Genet 2014, 94:223-232. 10.1016/j.ajhg.2014.01.009, 24507774.
28. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, Koseki M, Pirruccello JP, Ripatti S, Chasman DI, Willer CJ, Johansen CT, Fouchier SW, Isaacs A, Peloso GM, Barbalic M, Ricketts SL, Bis JC, Aulchenko YS, Thorleifsson G, Feitosa MF, Chambers J, Orho-Melander M, Melander O, Johnson T, Li X, Guo X, Li M, Shin Cho Y, Jin Go M, Jin Kim Y, et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 2010, 466:707-713. 10.1038/nature09270, 20686565.
29. Weissglas-Volkov D, Aguilar-Salinas CA, Nikkola E, Deere KA, Cruz-Bautista I, Arellano-Campos O, Munoz-Hernandez LL, Gomez-Munguia L, Ordonez-Sanchez ML, Reddy PM, Lusis AJ, Matikainen N, Taskinen MR, Riba L, Cantor RM, Sinsheimer JS, Tusie-Luna T, Pajukanta P. Genomic study in Mexicans identifies a new locus for triglycerides and refines European lipid loci. J Med Genet 2013, 50:298-308. 10.1136/jmedgenet-2012-101461, 23505323.
30. Tang T, Li L, Tang J, Li Y, Lin WY, Martin F, Grant D, Solloway M, Parker L, Ye W, Forrest W, Ghilardi N, Oravecz T, Platt KA, Rice DS, Hansen GM, Abuin A, Eberhart DE, Godowski P, Holt KH, Peterson A, Zambrowicz BP, de Sauvage FJ. A mouse knockout library for secreted and transmembrane proteins. Nat Biotechnol 2010, 28:749-755. 10.1038/nbt.1644, 20562862.
31. Mattijssen F, Kersten S. Regulation of triglyceride metabolism by Angiopoietin-like proteins. Biochim Biophys Acta 1821, 2012:782-789.
32. Ono M, Shimizugawa T, Shimamura M, Yoshida K, Noji-Sakikawa C, Ando Y, Koishi R, Furukawa H. Protein region important for regulation of lipid metabolism in angiopoietin-like 3 (ANGPTL3): ANGPTL3 is cleaved and activated in vivo. J Biol Chem 2003, 278:41804-41809. 10.1074/jbc.M302861200, 12909640.
33. Camenisch G, Pisabarro MT, Sherman D, Kowalski J, Nagel M, Hass P, Xie MH, Gurney A, Bodary S, Liang XH, Clark K, Beresini M, Ferrara N, Gerber HP. ANGPTL3 stimulates endothelial cell adhesion and migration via integrin alpha vbeta 3 and induces blood vessel formation in vivo. J Biol Chem 2002, 277:17281-17290. 10.1074/jbc.M109768200, 11877390.
34. Eckel RH. Lipoprotein lipase. A multifunctional enzyme relevant to common metabolic diseases. N Engl J Med 1989, 320:1060-1068. 10.1056/NEJM198904203201607, 2648155.
35. Zhang R, Abou-Samra AB. Emerging roles of Lipasin as a critical lipid regulator. Biochem Biophys Res Commun 2013, 432:401-405. 10.1016/j.bbrc.2013.01.129, 23415864.
36. Leanca CC, Nunes VS, Panzoldo NB, Zago VS, Parra ES, Cazita PM, Jauhiainen M, Passarelli M, Nakandakare ER, de Faria EC, Quintao EC. Metabolism of plasma cholesterol and lipoprotein parameters are related to a higher degree of insulin sensitivity in high HDL-C healthy normal weight subjects. Cardiovasc Diabetol 2013, 12:173. 10.1186/1475-2840-12-173, 24267726.
37. Huang Y, Li X, Wang M, Ning H, Li Y, Sun C. Lipoprotein lipase links vitamin D, insulin resistance, and type 2 diabetes: a cross-sectional epidemiological study. Cardiovasc Diabetol 2013, 12:17. 10.1186/1475-2840-12-17, 23320821.
38. Hu H, Sun W, Yu S, Hong X, Qian W, Tang B, Wang D, Yang L, Wang J, Mao C, Zhou L, Yuan G: Increased circulating levels of betatrophin in newly diagnosed type 2 diabetic patients.Diabetes Care 2014. in press..
39. Parsons JA, Brelje TC, Sorenson RL. Adaptation of islets of Langerhans to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology 1992, 130:1459-1466. 1537300.
40. Alonso LC, Yokoe T, Zhang P, Scott DK, Kim SK, O'Donnell CP, Garcia-Ocana A. Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes 2007, 56:1792-1801. 10.2337/db06-1513, 17400928.
41. Bruning JC, Winnay J, Bonner-Weir S, Taylor SI, Accili D, Kahn CR. Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell 1997, 88:561-572. 10.1016/S0092-8674(00)81896-6, 9038347.
42. Kulkarni RN, Jhala US, Winnay JN, Krajewski S, Montminy M, Kahn CR. PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J Clin Invest 2004, 114:828-836. 10.1172/JCI21845, 15372107.
43. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA, Kahn CR. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell 2000, 6:87-97. 10.1016/S1097-2765(00)00010-1, 10949030.
44. El Ouaamari A, Kawamori D, Dirice E, Liew CW, Shadrach JL, Hu J, Katsuta H, Hollister-Lock J, Qian WJ, Wagers AJ, Kulkarni RN. Liver-derived systemic factors drive beta cell hyperplasia in insulin-resistant states. Cell Rep 2013, 3:401-410. 10.1016/j.celrep.2013.01.007, 23375376.
45. Jiao Y, Le Lay J, Yu M, Naji A, Kaestner KH. Elevated mouse hepatic betatrophin expression does not increase human beta-cell replication in the transplant setting. Diabetes 2014, 63:1283-1288. 10.2337/db13-1435, 24353178.
46. Stewart AF. Betatrophin versus bitter-trophin and the elephant in the room: time for a new normal in beta-cell regeneration research. Diabetes 2014, 63:1198-1199. 10.2337/db14-0009, 24651805.
47. Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Bostrom EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Hojlund K, Gygi SP, Spiegelman BM. A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 2012, 481:463-468. 10.1038/nature10777, 22237023.
48. Zhang Y, Li R, Meng Y, Li S, Donelan W, Zhao Y, Qi L, Zhang M, Wang X, Cui T, Yang LJ, Tang D. Irisin stimulates browning of white adipocytes through mitogen-activated protein kinase p38 MAP kinase and ERK MAP kinase signaling. Diabetes 2014, 63:514-525. 10.2337/db13-1106, 24150604.
49. Sanchis-Gomar F, Perez-Quilis C. The p38-PGC-1alpha-irisin-betatrophin axis: Exploring new pathways in insulin resistance. Adipocyte 2014, 3:67-68. 10.4161/adip.27370, 24575373.
50. Gomez-Ambrosi J, Pascual E, Catalan V, Rodriguez A, Ramirez B, Silva C, Gil MJ, Salvador J, Fruhbeck G: Circulating betatrophin concentrations are decreased in human obesity and type 2 diabetes.J Clin Endocrinol Metab 2014. in press..
51. Fu Z, Abou-Samra AB, Zhang R. An explanation for recent discrepancies in levels of human circulating betatrophin. Diabetologia 2014, 57:2232-2234. 10.1007/s00125-014-3346-1, 25099942.
52. Chang JK, Lyu RM, Chen XQ, Tian Q, Sabirov A, Dun SL, Dun NJ. Detection of C-terminal betatrophin peptides in human plasma and rodent liver. Detection of C-terminal betatrophin peptides in human plasma and rodent liver. The 4th Asia-Pacific International Peptide Symposium. Peptide Science, Japan 2013, 243-246. Nishiuchi Y, Teshima T.