SAD-A Potentiates Glucose-Stimulated Insulin Secretion as a Mediator of Glucagon-Like Peptide 1 Response in Pancreatic β Cells

Molecular and Cellular Biology

Volumn 33, Issue 13, 2013, Pages 2527-2534

  Nie, Jia ^a,b   Lilley, Brendan N ^c   Pan, Y Albert ^c   Faruque, Omar ^b   Liu, Xiaolei ^b   Zhang, Weiping ^d   Sanes, Joshua R ^c   Han, Xiao ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c HARVARD UNIVERSITY   (United States)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INCRETIN; PROTEIN; SAD A PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; GLUCOSE INTOLERANCE; GLUCOSE STIMULATED INSULIN SECRETION; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; CALCIUM; CELL LINE; CYCLIC AMP; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; GLUCOSE INTOLERANCE; INCRETINS; INSULIN; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICE, TRANSGENIC; PANCREAS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; THREONINE;

EID: 84880783742     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00285-13     Document Type: Article

References (41)

1. Newgard CB, Lu D, Jensen MV, Schissler J, Boucher A, Burgess S, Sherry AD. 2002. Stimulus/secretion coupling factors in glucosestimulated insulin secretion: insights gained from a multidisciplinary approach. Diabetes 51(Suppl 3):S389-S393.
2. Drucker DJ. 2006. The biology of incretin hormones. Cell Metab. 3:153-165.
3. Dyachok O, Idevall-Hagren O, Sagetorp J, Tian G, Wuttke A, Arrieumerlou C, Akusjarvi G, Gylfe E, Tengholm A. 2008. Glucose-induced cyclic AMP oscillations regulate pulsatile insulin secretion. Cell Metab. 8:26-37.
4. 't Hart LM, Simonis-Bik AM, Nijpels G, van Haeften TW, Schafer SA, Houwing-Duistermaat JJ, Boomsma DI, Groenewoud MJ, Reiling E, van Hove EC, Diamant M, Kramer MH, Heine RJ, Maassen JA, KirchhoffK, Machicao F, Haring HU, Slagboom PE, Willemsen G, Eekhoff EM, de Geus EJ, Dekker JM, Fritsche A. 2010. Combined risk allele score of eight type 2 diabetes genes is associated with reduced first-phase glucose-stimulated insulin secretion during hyperglycemic clamps. Diabetes 59:287-292.
5. Fehse F, Trautmann M, Holst JJ, Halseth AE, Nanayakkara N, Nielsen LL, Fineman MS, Kim DD, Nauck MA. 2005. Exenatide augments first and second-phase insulin secretion in response to intravenous glucose in subjects with type 2 diabetes. J. Clin. Endocrinol. Metab. 90:5991-5997.
6. Rubino F, R'Bibo LS, del Genio F, Mazumdar M, McGraw TE. 2010. Metabolic surgery: the role of the gastrointestinal tract in diabetes mellitus. Nat. Rev. Endocrinol. 6:102-109.
7. Dupre J, Beck JC. 1966. Stimulation of release of insulin by an extract of intestinal mucosa. Diabetes 15:555-559.
8. MacDonald PE, El-Kholy W, Riedel MJ, Salapatek AM, Light PE, Wheeler MB. 2002. The multiple actions of GLP-1 on the process of glucose-stimulated insulin secretion. Diabetes 51(Suppl 3):S434-S442.
9. Ozaki N, Shibasaki T, Kashima Y, Miki T, Takahashi K, Ueno H, Sunaga Y, Yano H, Matsuura Y, Iwanaga T, Takai Y, Seino S. 2000. cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat. Cell Biol. 2:805-811.
10. Seino S, Shibasaki T, Minami K. 2011. Dynamics of insulin secretion and the clinical implications for obesity and diabetes. J. Clin. Invest. 121:2118-2125.
11. Dolz M, Movassat J, Bailbe D, Le StunffH, Giroix MH, Fradet M, Kergoat M, Portha B. 2011. cAMP-secretion coupling is impaired in diabetic GK/Par rat beta-cells: a defect counteracted by GLP-1. Am. J. Physiol. Endocrinol. Metab. 301:E797-E806.
12. Fujimoto T, Yurimoto S, Hatano N, Nozaki N, Sueyoshi N, Kameshita I, Mizutani A, Mikoshiba K, Kobayashi R, Tokumitsu H. 2008. Activation of SAD kinase by Ca2+/calmodulin-dependent protein kinase kinase. Biochemistry 47:4151-4159.
13. Guo Z, Tang W, Yuan J, Chen X, Wan B, Gu X, Luo K, Wang Y, Yu L. 2006. BRSK2 is activated by cyclic AMP-dependent protein kinase A through phosphorylation at Thr260. Biochem. Biophys. Res. Commun. 347:867-871.
14. Alessi DR, Sakamoto K, Bayascas JR. 2006. LKB1-dependent signaling pathways. Annu. Rev. Biochem. 75:137-163.
15. Fu A, Ng AC, Depatie C, Wijesekara N, He Y, Wang GS, Bardeesy N, Scott FW, Touyz RM, Wheeler MB, Screaton RA. 2009. Loss of Lkb1 in adult beta cells increases beta cell mass and enhances glucose tolerance in mice. Cell Metab. 10:285-295.
16. Granot Z, Swisa A, Magenheim J, Stolovich-Rain M, Fujimoto W, Manduchi E, Miki T, Lennerz JK, Stoeckert CJ, Jr, Meyuhas O, Seino S, Permutt MA, Piwnica-Worms H, Bardeesy N, Dor Y. 2009. LKB1 regulates pancreatic beta cell size, polarity, and function. Cell Metab. 10: 296-308.
17. Sun G, Tarasov AI, McGinty JA, French PM, McDonald A, Leclerc I, Rutter GA. 2010. LKB1 deletion with the RIP2.Cre transgene modifies pancreatic beta-cell morphology and enhances insulin secretion in vivo. Am. J. Physiol. Endocrinol. Metab. 298:E1261-E1273.
18. Alvarado-Kristensson M, Rodriguez MJ, Silio V, Valpuesta JM, Carrera AC. 2009. SADB phosphorylation of gamma-tubulin regulates centrosome duplication. Nat. Cell Biol. 11:1081-1092.
19. Barnes AP, Lilley BN, Pan YA, Plummer LJ, Powell AW, Raines AN, Sanes JR, Polleux F. 2007. LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129:549-563.
20. Inoue E, Mochida S, Takagi H, Higa S, Deguchi-Tawarada M, Takao-Rikitsu E, Inoue M, Yao I, Takeuchi K, Kitajima I, Setou M, Ohtsuka T, Takai Y. 2006. SAD: a presynaptic kinase associated with synaptic vesicles and the active zone cytomatrix that regulates neurotransmitter release. Neuron 50:261-275.
21. Kishi M, Pan YA, Crump JG, Sanes JR. 2005. Mammalian SAD kinases are required for neuronal polarization. Science 307:929-932.
22. Muller M, Lutter D, Puschel AW. 2010. Persistence of the cell-cycle checkpoint kinase Wee1 in SadA- and SadB-deficient neurons disrupts neuronal polarity. J. Cell Sci. 123:286-294.
23. Nie J, Sun C, Faruque O, Ye G, Li J, Liang Q, Chang Z, Yang W, Han X, Shi Y. 2012. Synapses of amphids defective (SAD-A) kinase promotes glucose-stimulated insulin secretion through activation of p21-activated kinase (PAK1) in pancreatic beta-cells. J. Biol. Chem. 287:26435-26444.
24. Morioka T, Asilmaz E, Hu J, Dishinger JF, Kurpad AJ, Elias CF, Li H, Elmquist JK, Kennedy RT, Kulkarni RN. 2007. Disruption of leptin receptor expression in the pancreas directly affects beta cell growth and function in mice. J. Clin. Invest. 117:2860-2868.
25. National Institutes of Health. 1985. Guide for the care and use of laboratory animals. NIH publication no. 86-23. National Institutes of Health, Bethesda, MD.
26. Wicksteed B, Brissova M, Yan W, Opland DM, Plank JL, Reinert RB, Dickson LM, Tamarina NA, Philipson LH, Shostak A, Bernal-Mizrachi E, Elghazi L, Roe MW, Labosky PA, Myers MG, Jr, Gannon M, Powers AC, Dempsey PJ. 2010. Conditional gene targeting in mouse pancreatic ss-cells: analysis of ectopic Cre transgene expression in the brain. Diabetes 59:3090-3098.
27. Zenke FT, King CC, Bohl BP, Bokoch GM. 1999. Identification of a central phosphorylation site in p21-activated kinase regulating autoinhibition and kinase activity. J. Biol. Chem. 274:32565-32573.
28. Prentki M, Nolan CJ. 2006. Islet beta cell failure in type 2 diabetes. J. Clin. Invest. 116:1802-1812.
29. Doria A, Lee J, Warram JH, Krolewski AS. 1996. Diabetes susceptibility at IDDM2 cannot be positively mapped to the VNTR locus of the insulin gene. Diabetologia 39:594-599.
30. Liu H, Remedi MS, Pappan KL, Kwon G, Rohatgi N, Marshall CA, McDaniel ML. 2009. Glycogen synthase kinase-3 and mammalian target of rapamycin pathways contribute to DNA synthesis, cell cycle progression, and proliferation in human islets. Diabetes 58:663-672.
31. Van de Velde S, Hogan MF, Montminy M. 2011. mTOR links incretin signaling to HIF induction in pancreatic beta cells. Proc. Natl. Acad. Sci. U. S. A. 108:16876-16882.
32. Inoki K, Kim J, Guan KL. 2012. AMPK and mTOR in cellular energy homeostasis and drug targets. Annu. Rev. Pharmacol. Toxicol. 52:381-400.
33. Cai F, Gyulkhandanyan AV, Wheeler MB, Belsham DD. 2007. Glucose regulates AMP-activated protein kinase activity and gene expression in clonal, hypothalamic neurons expressing proopiomelanocortin: additive effects of leptin or insulin. J. Endocrinol. 192:605-614.
34. Gleason CE, Lu D, Witters LA, Newgard CB, Birnbaum MJ. 2007. The role of AMPK and mTOR in nutrient sensing in pancreatic beta-cells. J. Biol. Chem. 282:10341-10351.
35. Hurov JB, Huang M, White LS, Lennerz J, Choi CS, Cho YR, Kim HJ, Prior JL, Piwnica-Worms D, Cantley LC, Kim JK, Shulman GI, Piwnica-Worms H. 2007. Loss of the Par-1b/MARK2 polarity kinase leads to increased metabolic rate, decreased adiposity, and insulin hypersensitivity in vivo. Proc. Natl. Acad. Sci. U. S. A. 104:5680-5685.
36. Lennerz JK, Hurov JB, White LS, Lewandowski KT, Prior JL, Planer GJ, Gereau RW, IV, Piwnica-Worms D, Schmidt RE, Piwnica-Worms H. 2010. Loss of Par-1a/MARK3/C-TAK1 kinase leads to reduced adiposity, resistance to hepatic steatosis, and defective gluconeogenesis. Mol. Cell. Biol. 30:5043-5056.
37. Sun C, Tian L, Nie J, Zhang H, Han X, Shi Y. 2012. Inactivation of MARK4, an AMP-activated protein kinase (AMPK)-related kinase, leads to insulin hypersensitivity and resistance to diet-induced obesity. J. Biol. Chem. 287:38305-38315.
38. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, Yamanaka M, Zhang C, Tamamoto A, Satoh T, Miyazaki J, Seino S. 2007. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc. Natl. Acad. Sci. U. S. A. 104:19333-19338.
39. Nesher R, Anteby E, Yedovizky M, Warwar N, Kaiser N, Cerasi E. 2002. Beta-cell protein kinases and the dynamics of the insulin response to glucose. Diabetes 51(Suppl 1):S68-S73.
40. Ahn JH, McAvoy T, Rakhilin SV, Nishi A, Greengard P, Nairn AC. 2007. Protein kinase A activates protein phosphatase 2A by phosphorylation of the B56delta subunit. Proc. Natl. Acad. Sci. U. S. A. 104:2979-2984.
41. Nikolic M, Chou MM, Lu W, Mayer BJ, Tsai LH. 1998. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395:194-198.