Neuronal SH2B1 is essential for controlling energy and glucose homeostasis

Journal of Clinical Investigation

Volumn 117, Issue 2, 2007, Pages 397-406

  Ren, Decheng ^a   Zhou, Yingjiang ^a   Morris, David ^a   Li, Minghua ^a   Li, Zhiqin ^a   Rui, Liangyou ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; JANUS KINASE 2; LEPTIN; NEUROPEPTIDE; PROTEIN SH2; PROTEIN SH2B1; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APPETITE; ARTICLE; BODY WEIGHT; BRAIN; CONTROLLED STUDY; ENERGY BALANCE; GENE DELETION; GENE OVEREXPRESSION; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; HEART; HYPERGLYCEMIA; HYPERLIPIDEMIA; HYPERPHAGIA; HYPOTHALAMUS; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIVER; METABOLIC DISORDER; MUSCLE; NERVE CELL; NERVOUS SYSTEM; NONHUMAN; OBESITY; PANCREAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TRANSGENIC MOUSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADIPOSE TISSUE; ANIMALS; BASE SEQUENCE; BODY WEIGHT; DNA PRIMERS; ENERGY METABOLISM; GLUCOSE; HOMEOSTASIS; HYPERLIPIDEMIAS; HYPOTHALAMUS; INSULIN RESISTANCE; LEPTIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; OBESITY;

EID: 33846822094     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI29417     Document Type: Article

References (66)

1. Flier, J.S. 2004. Obesity wars: molecular progress confronts an expanding epidemic. Cell. 116:337-350.
2. Friedman, J.M., and Halaas, J.L. 1998. Leptin and the regulation of body weight in mammals. Nature. 395:763-770.
3. Schwartz, M.W., and Porte, D., Jr. 2005. Diabetes, obesity, and the brain. Science. 307:375-379.
4. Zhang, Y., et al. 1994. Positional cloning of the mouse obese gene and its human homologue. Nature. 372:425-432.
5. Chua, S.C., Jr., et al. 1996. Phenotypes of mouse diabetes and rat fatty due to mutations in the OB (leptin) receptor. Science. 271:994-996.
6. Chen, H., et al. 1996. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell. 84:491-495.
7. Lee, G.H., et al. 1996. Abnormal splicing of the leptin receptor in diabetic mice. Nature. 379:632-635.
8. Vaisse, C., et al. 1996. Leptin activation of Stat3 in the hypothalamus of wild-type and ob/ob mice but not db/db mice. Nat. Genet. 14:95-97.
9. Bjorbaek, C., Uotani, S., da Silva, B., and Flier, J.S. 1997. Divergent signaling capacities of the long and short isoforms of the leptin receptor. J. Biol. Chem. 272:32686-32695.
10. Baumann, H., et al. 1996. The full-length leptin receptor has signaling capabilities of interleukin 6-type cytokine receptors. Proc. Natl. Acad. Sci. U. S. A. 93:8374-8378.
11. Zhao, A.Z., Huan, J.N., Gupta, S., Pal, R., and Sahu, A. 2002. A phosphatidylinositol 3-kinase phosphodiesterase 3B-cyclic AMP pathway in hypothalamic action of leptin on feeding. Nat. Neurosci. 5:727-728.
12. Niswender, K.D., et al. 2001. Intracellular signalling. Key enzyme in leptin-induced anorexia. Nature. 413:794-795.
13. Bates, S.H., et al. 2003. STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature. 421:856-859.
14. Cui, Y., et al. 2004. Essential role of STAT3 in body weight and glucose homeostasis. Mol. Cell. Biol. 24:258-269.
15. Gao, Q., et al. 2004. Disruption of neural signal transducer and activator of transcription 3 causes obesity, diabetes, infertility, and thermal dysregulation. Proc. Natl. Acad. Sci. U. S. A. 101:4661-4666.
16. Suzuki, R., et al. 2004. Both insulin signaling defects in the liver and obesity contribute to insulin resistance and cause diabetes in Irs2(-/-) mice. J. Biol. Chem. 279:25039-25049.
17. Lin, X., et al. 2004. Dysregulation of insulin receptor substrate 2 in β cells and brain causes obesity and diabetes. J. Clin. Invest. 114:908-916. doi:10.1172/JCI200422217.
18. Banks, A.S., Davis, S.M., Bates, S.H., and Myers, M.G., Jr. 2000. Activation of downstream signals by the long form of the leptin receptor. J. Biol. Chem. 275:14563-14572.
19. Bjorbaek, C., and Kahn, B.B. 2004. Leptin signaling in the central nervous system and the periphery. Recent Prog. Horm. Res. 59:305-331.
20. Myers, M.P., et al. 2001. TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J. Biol. Chem. 276:47771-47774.
21. Cheng, A., et al. 2002. Attenuation of leptin action and regulation of obesity by protein tyrosine phosphatase 1B. Dev. Cell. 2:497-503.
22. Zabolotny, J.M., et al. 2002. PTP1B regulates leptin signal transduction in vivo. Dev. Cell. 2:489-495.
23. Bjorbaek, C., Elmquist, J.K., Frantz, J.D., Shoelson, S.E., and Flier, J.S. 1998. Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol. Cell. 1:619-625.
24. Ungureanu, D., Saharinen, P., Junttila, I., Hilton, D.J., and Silvennoinen, O. 2002. Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS-1. Mol. Cell. Biol. 22:3316-3326.
25. Howard, J.K., et al. 2004. Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nat. Med. 10:734-738.
26. Mori, H., et al. 2004. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat. Med. 10:739-743.
27. Rui, L., and Carter-Su, C. 1999. Identification of SH2-bbeta as a potent cytoplasmic activator of the tyrosine kinase Janus kinase 2. Proc. Natl. Acad. Sci. U. S. A. 96:7172-7177.
28. Osborne, M.A., Dalton, S., and Kochan, J.P. 1995. The yeast tribrid system - genetic detection of trans-phosphorylated ITAM-SH2-interactions. Biotechnology (N. Y.). 13:1474-1478.
29. Rui, L., Mathews, L.S., Hotta, K., Gustafson, T.A., and Carter-Su, C. 1997. Identification of SH2-Bbeta as a substrate of the tyrosine kinase JAK2 involved in growth hormone signaling. Mol. Cell. Biol. 17:6633-6644.
30. Yokouchi, M., et al. 1997. Cloning and characterization of APS, an adaptor molecule containing PH and SH2 domains that is tyrosine phosphorylated upon B-cell receptor stimulation. Oncogene. 15:7-15.
31. Yousaf, N., Deng, Y., Kang, Y., and Riedel, H. 2001. Four PSM/SH2-B alternative splice variants and their differential roles in mitogenesis. J. Biol. Chem. 276:40940-40948.
32. Kotani, K., Wilden, P., and Pillay, T.S. 1998. SH2-Balpha is an insulin-receptor adapter protein and substrate that interacts with the activation loop of the insulin-receptor kinase. Biochem. J. 335:103-109.
33. Nelms, K., et al. 1999. Alternative splicing, gene localization, and binding of SH2-B to the insulin receptor kinase domain. Mamm. Genome. 10:1160-1167.
34. Qian, X., Riccio, A., Zhang, Y., and Ginty, D.D. 1998. Identification and characterization of novel substrates of Trk receptors in developing neurons. Neuron. 21:1017-1029.
35. Riedel, H., Wang, J., Hansen, H., and Yousaf, N. 1997. PSM, an insulin-dependent, pro-rich, PH, SH2 domain containing partner of the insulin receptor. J. Biochem. (Tokyo). 122:1105-1113.
36. Rui, L., and Carter-Su, C. 1998. Platelet-derived growth factor (PDGF) stimulates the association of SH2-Bbeta with PDGF receptor and phosphorylation of SH2-Bbeta. J. Biol. Chem. 273:21239-21245.
37. Rui, L., Herrington, J., and Carter-Su, C. 1999. SH2-B, a membrane-associated adapter, is phosphorylated on multiple serines/threonines in response to nerve growth factor by kinases within the MEK/ERK cascade. J. Biol. Chem. 274:26485-26492.
38. Rui, L., Herrington, J., and Carter-Su, C. 1999. SH2-B is required for nerve growth factor-induced neuronal differentiation. J. Biol. Chem. 274:10590-10594.
39. Suzuki, K., et al. 2002. Association of SH2-B to phosphorylated tyrosine residues in the activation loop of TrkB. Res. Commun. Mol. Pathol. Pharmacol. 111:27-39.
40. Wang, J., and Riedel, H. 1998. Insulin-like growth factor-I receptor and insulin receptor association with a Src homology-2 domain-containing putative adapter. J. Biol. Chem. 273:3136-3139.
41. Zhang, Y., et al. 2006. Interaction of SH2-Bbeta with RET is involved in signaling of GDNF-induced neurite outgrowth. J. Cell Sci. 119:1666-1676.
42. Kong, M., Wang, C.S., and Donoghue, D.J. 2002. Interaction of fibroblast growth factor receptor 3 and the adapter protein SH2-B. A role in STAT5 activation. J. Biol. Chem. 277:15962-15970.
43. O'Brien, K.B., O'Shea, J.J., and Carter-Su, C. 2002. SH2-B family members differentially regulate JAK family tyrosine kinases. J. Biol. Chem. 277:8673-8681.
44. Duan, C., Yang, H., White, M.F., and Rui, L. 2004. Disruption of the SH2-B gene causes age-dependent insulin resistance and glucose intolerance. Mol. Cell. Biol. 24:7435-7443.
45. Ren, D., Li, M., Duan, C., and Rui, L. 2005. Identification of SH2-B as a key regulator of leptin sensitivity, energy balance, and body weight in mice. Cell Metab. 2:95-104.
46. Li, M., Ren, D., Iseki, M., Takaki, S., and Rui, L. 2006. Differential role of SH2-B and APS in regulating energy and glucose homeostasis. Endocrinology. 147:2163-2170.
47. Ohtsuka, S., et al. 2002. SH2-B is required for both male and female reproduction. Mol. Cell. Biol. 22:3066-3077.
48. Kowalski, T.J., Liu, S.-M., Leibel, R.L., and Chua, S.C., Jr. 2001. Transgenic complementation of leptin-receptor deficiency. I. Rescue of the obesity/diabetes phenotype of LEPR-null mice expressing a LEPR-B transgene. Diabetes. 50:425-435.
49. Mizuno, T.M., Kelley, K.A., Pasinetti, G.M., Roberts, J.L., and Mobbs, C.V. 2003. Transgenic neuronal expression of proopiomelanocortin attenuates hyperphagic response to fasting and reverses metabolic impairments in leptin-deficient obese mice. Diabetes. 52:2675-2683.
50. Cone, R.D. 2005. Anatomy and regulation of the central melanocortin system. Nat. Neurosci. 8:571-578.
51. Seeley, R.J., Drazen, D.L., and Clegg, D.J. 2004. The critical role of the melanocortin system in the control of energy balance. Annu. Rev. Nutr. 24:133-149.
52. Ahmed, Z., and Pillay, T.S. 2003. Adapter protein with a pleckstrin homology (PH) and an Src homology 2 (SH2) domain (APS) and SH2-B enhance insulin-receptor autophosphorylation, extracellular-signal-regulated kinase and phosphoinositide 3-kinase-dependent signalling. Biochem. J. 371:405-412.
53. Bruning, J.C., et al. 2000. Role of brain insulin receptor in control of body weight and reproduction. Science. 289:2122-2125.
54. Benoit, S.C., Clegg, D.J., Seeley, R.J., and Woods, S.C. 2004. Insulin and leptin as adiposity signals. Recent Prog. Horm. Res. 59:267-285.
55. Hu, J., and Hubbard, S.R. 2006. Structural basis for phosphotyrosine recognition by the Src homology-2 domains of the adapter proteins SH2-B and APS. J. Mol. Biol. 361:69-79.
56. Kurzer, J.H., et al. 2004. Tyrosine 813 is a site of JAK2 autophosphorylation critical for activation of JAK2 by SH2-B beta. Mol. Cell. Biol. 24:4557-4570.
57. Nishi, M., et al. 2005. Kinase activation through dimerization by human SH2-B. Mol. Cell. Biol. 25:2607-2621.
58. Duan, C., Li, M., and Rui, L. 2004. SH2-B promotes insulin receptor substrate 1 (IRS1)- and IRS2-mediated activation of the phosphatidylinositol 3-kinase pathway in response to leptin. J. Biol. Chem. 279:43684-43691.
59. White, M.F. 2002. IRS proteins and the common path to diabetes. Am. J. Physiol. Endocrinol. Metab. 283:E413-E422.
60. Balthasar, N., et al. 2005. Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell. 123:493-505.
61. Pocai, A., et al. 2005. Central leptin acutely reverses diet-induced hepatic insulin resistance. Diabetes. 54:3182-3189.
62. Morton, G.J., et al. 2005. Leptin regulates insulin sensitivity via phosphatidylinositol-3-OH kinase signaling in mediobasal hypothalamic neurons. Cell Metab. 2:411-420.
63. Inoue, H., et al. 2006. Role of hepatic STAT3 in brain-insulin action on hepatic glucose production. Cell Metab. 3:267-275.
64. Gelling, R.W., et al. 2006. Insulin action in the brain contributes to glucose lowering during insulin treatment of diabetes. Cell Metab. 3:67-73.
65. Obici, S., Feng, Z., Karkanias, G., Baskin, D.G., and Rossetti, L. 2002. Decreasing hypothalamic insulin receptors causes hyperphagia and insulin resistance in rats. Nat. Neurosci. 5:566-572.
66. Obici, S., Zhang, B.B., Karkanias, G., and Rossetti, L. 2002. Hypothalamic insulin signaling is required for inhibition of glucose production. Nat. Med. 8:1376-1382.