Role of the SIK2-p35-PJA2 complex in pancreatic β-cell functional compensation

Nature Cell Biology

Volumn 16, Issue 3, 2014, Pages 234-244

  Sakamaki, Jun Ichi ^a   Fu, Accalia ^a   Reeks, Courtney ^a   Baird, Stephen ^a   Depatie, Chantal ^a   Al Azzabi, Mufida ^a   Bardeesy, Nabeel ^b   Gingras, Anne Claude ^c,d   Yee, Siu Pok ^e   Screaton, Robert A ^a,f  

^a CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^f UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PJA2 PROTEIN; PROTEIN P35; SALT INDUCIBLE KINASE 2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM MOBILIZATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; GENE INACTIVATION; GLUCOSE INTOLERANCE; HUMAN; HUMAN CELL; HYPERGLYCEMIA; INSULIN RELEASE; MALE; METABOLIC SYNDROME X; MOUSE; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; UBIQUITINATION;

ANIMALS; CALCIUM SIGNALING; FEMALE; GLUCOSE; GLUCOSE INTOLERANCE; INSULIN; INSULIN-SECRETING CELLS; MALE; MEMBRANE POTENTIALS; METABOLIC SYNDROME X; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTEIN-SERINE-THREONINE KINASES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84895455224     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2919     Document Type: Article

References (54)

1. Nolan, C. J., Damm, P. & Prentki, M. Type 2 diabetes across generations: from pathophysiology to prevention and management. Lancet 378, 169-181 (2011).
2. Florez, J. C. Newly identified loci highlight β cell dysfunction as a key cause of type 2 diabetes: where are the insulin resistance genes?. Diabetologia 51, 1100-1110 (2008).
3. Nolan, C. J. Failure of islet beta-cell compensation for insulin resistance causes type 2 diabetes: what causes non-alcoholic fatty liver disease and non-alcoholic steatohepatitis?. Journal of gastroenterology and hepatology 25, 1594-1597 (2010).
4. Kahn, S. E. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes. Diabetologia 46, 3-19 (2003).
5. Prentki, M. & Nolan, C. J. Islet β cell failure in type 2 diabetes. J. Clin. Invest. 116, 1802-1812 (2006).
6. Mari, A. et al. Impaired β cell glucose sensitivity rather than inadequate compensation for insulin resistance is the dominant defect in glucose intolerance. Diabetologia 53, 749-756 (2010).
7. Fu, A. et al. Loss of Lkb1 in adult β cells increases β cell mass and enhances glucose tolerance in mice. Cell Metab 10, 285-295 (2009).
8. Granot, Z. et al. LKB1 regulates pancreatic β cell size, polarity, and function. Cell Metab 10, 296-308 (2009).
9. Sun, G. et al. LKB1 deletion with the RIP2.Cre transgene modifies pancreatic betacell morphology and enhances insulin secretion in vivo. Am. J. Physiol. Endocrinol. Metab 298, E1261-1273 (2010).
10. Wang, Z., Takemori, H., Halder, S. K., Nonaka, Y. & Okamoto, M. Cloning of a novel kinase (SIK) of the SNF1/AMPK family from high salt diet-treated rat adrenal. FEBS Lett. 453, 135-139 (1999).
11. Bricambert, J. et al. Salt-inducible kinase 2 links transcriptional coactivator p300 phosphorylation to the prevention of ChREBP-dependent hepatic steatosis in mice. J. Clin. Invest. 120, 4316-4331 (2010).
12. Horike, N. et al. Downregulation of SIK2 expression promotes the melanogenic program in mice. Pigment. Cell Melanoma Res. 23, 809-819 (2010).
13. Ahmed, A. A. et al. SIK2 is a centrosome kinase required for bipolar mitotic spindle formation that provides a potential target for therapy in ovarian cancer.. Cancer Cell 18, 109-121 (2010).
14. Liu, Y. et al. Salt-inducible kinase is involved in the regulation of corticotropinreleasing hormone transcription in hypothalamic neurons in rats. Endocrinology 153, 223-233 (2012).
15. Muraoka, M. et al. Involvement of SIK2/TORC2 signaling cascade in the regulation of insulin-induced PGC-1alpha and UCP-1 gene expression in brown adipocytes. Am. J. Physiol. Endocrinol. Metab 296, E1430-1439 (2009).
16. Dentin, R. et al. Insulin modulates gluconeogenesis by inhibition of the coactivator TORC2. Nature 449, 366-369 (2007).
17. Nagel, S. et al. Amplification at 11q23 targets protein kinase SIK2 in diffuse large B-cell lymphoma. Leuk Lymphoma 51, 881-891 (2010).
18. Imielinski, M. et al. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 150, 1107-1120 (2012).
19. Sasaki, T. et al. SIK2 is a key regulator for neuronal survival after ischemia via TORC1-CREB. Neuron 69, 106-119 (2011).
20. Screaton, R. A. et al. The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 119, 61-74 (2004).
21. Jhala, U. S. et al. cAMP promotes pancreatic beta-cell survival via CREB-mediated induction of IRS2. Genes Dev. 17, 1575-1580 (2003).
22. Eberhard, C. E., Fu, A., Reeks, C. & Screaton, R. A. CRTC2 Is Required for beta-Cell Function and Proliferation. Endocrinology 154, 2308-2317 (2013).
23. Newgard, C. B. & McGarry, J. D. Metabolic coupling factors in pancreatic beta-cell signal transduction. Annu. Rev. Biochem. 64, 689-719 (1995).
24. MacDonald, P. E., Joseph, J. W. & Rorsman, P. Glucose-sensing mechanisms in pancreatic beta-cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 2211-2225 (2005).
25. Newsholme, P., Bender, K., Kiely, A. & Brennan, L. Amino acid metabolism, insulin secretion and diabetes. Biochem. Soc. Trans. 35, 1180-1186 (2007).
26. Wei, F. Y. et al. Cdk5-dependent regulation of glucose-stimulated insulin secretion. Nat. Med. 11, 1104-1108 (2005).
27. Lew, J. et al. A brain-specific activator of cyclin-dependent kinase 5. Nature 371, 423-426 (1994).
28. Tsai, L. H., Delalle, I., Caviness, V. S. Jr., Chae, T. & Harlow, E. p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371, 419-423 (1994).
29. Cheung, Z. H. & Ip, N. Y. Cdk5: a multifaceted kinase in neurodegenerative diseases. Trends Cell Biol. 22, 169-175 (2012).
30. Patrick, G. N., Zhou, P., Kwon, Y. T., Howley, P. M. & Tsai, L. H. p35, the neuronalspecific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitinproteasome pathway. J. Biol. Chem. 273, 24057-24064 (1998).
31. Nakayama, M., Miyake, T., Gahara, Y., Ohara, O. & Kitamura, T. A novel RINGH2 motif protein downregulated by axotomy: its characteristic localization at the postsynaptic density of axosomatic synapse. J. Neurosci. 15, 5238-5248 (1995).
32. Zhang, Y. et al. Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425-432 (1994).
33. Lignitto, L. et al. Control of PKA stability and signalling by the RING ligase praja2. Nat. Cell Biol. 13, 412-422 (2011).
34. Holz, G. G. & Habener, J. F. Signal transduction crosstalk in the endocrine system: pancreatic beta-cells and the glucose competence concept. Trends Biochem. Sci. 17, 388-393 (1992).
35. Manning, G., Whyte, D. B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912-1934 (2002).
36. Fu, A., Eberhard, C. E. & Screaton, R. A. Role of AMPK in pancreatic β cell function. Molecular and Cellular Endocrinology 366, 127-134 (2013).
37. Nie, J. et al. SAD-A kinase controls islet beta-cell size and function as a mediator of mTORC1 signaling. Proc. Natl Acad. Sci. USA 110, 13857-13862 (2013).
38. Wehr, M. C. et al. Salt-inducible kinases regulate growth through the Hippo signalling pathway in Drosophila. Nat. Cell Biol. 15, 61-71 (2013).
39. Wang, B. et al. A hormone-dependent module regulating energy balance. Cell 145, 596-606 (2011).
40. Wang, B. et al. The insulin-regulated CREB coactivator TORC promotes stress resistance in Drosophila. Cell Metab 7, 434-444 (2008).
41. Choi, S., Kim, W. & Chung, J. Drosophila salt-inducible kinase (SIK) regulates starvation resistance through cAMP-response element-binding protein (CREB)- regulated transcription coactivator (CRTC). J. Biol. Chem. 286, 2658-2664 (2011).
42. Polonsky, K. S. et al. Abnormal patterns of insulin secretion in non-insulin-dependent diabetes mellitus. N. Engl. J. Med. 318, 1231-1239 (1988).
43. O'Rahilly, S., Turner, R. C. & Matthews, D. R. Impaired pulsatile secretion of insulin in relatives of patients with non-insulin-dependent diabetes. N. Engl. J. Med. 318, 1225-1230 (1988).
44. Seino, S., Shibasaki, T. & Minami, K. Dynamics of insulin secretion and the clinical implications for obesity and diabetes. J. Clin. Invest. 121, 2118-2125 (2011).
45. Byrne, M. M., Sturis, J., Sobel, R. J. & Polonsky, K. S. Elevated plasma glucose 2 h postchallenge predicts defects in beta-cell function. The American Journal of Physiology 270, E572-E579 (1996).
46. Weyer, C., Bogardus, C., Mott, D. M. & Pratley, R. E. The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J. Clin. Invest. 104, 787-794 (1999).
47. Mitrakou, A. et al. Role of reduced suppression of glucose production and diminished early insulin release in impaired glucose tolerance. N. Engl. J. Med. 326, 22-29 (1992).
48. Rulifson, E. J., Kim, S. K. & Nusse, R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296, 1118-1120 (2002).
49. Su, S. C. & Tsai, L. H. Cyclin-dependent kinases in brain development and disease. Annu. Rev. Cell Dev. Biol. 27, 465-491 (2011).
50. Lalioti, V. et al. The atypical kinase Cdk5 is activated by insulin, regulates the association between GLUT4 and E-Syt1, and modulates glucose transport in 3T3- L1 adipocytes. Proc. Natl Acad. Sci. USA 106, 4249-4253 (2009).
51. Choi, J. H. et al. Antidiabetic actions of a non-agonist PPAR ligand blocking Cdk5- mediated phosphorylation. Nature 477, 477-481 (2011).
52. Jansson, D. et al. Glucose controls CREB activity in islet cells via regulated phosphorylation of TORC2. Proc. Natl. Acad. Sci. USA 105, 10161-10166 (2008).
53. Kean, M. J., Couzens, A. L. & Gingras, A. C. Mass spectrometry approaches to study mammalian kinase and phosphatase associated proteins. Methods 57, 400-408 (2012).
54. Liu, G. et al. ProHits: integrated software for mass spectrometry-based interaction proteomics. Nat. Biotechnol. 28, 1015-1017 (2010).