High glucose exposure promotes activation of protein phosphatase 2A in rodent islets and INS-1 832/13 β-cells by increasing the posttranslational carboxylmethylation of its catalytic subunit

Endocrinology

Volumn 155, Issue 2, 2014, Pages 380-391

  Arora, Daleep K ^a   Machhadieh, Baker ^b   Matti, Andrea ^c   Wadzinski, Brian E ^d   Ramanadham, Sasanka ^e   Kowluru, Anjaneyulu ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF DETROIT MERCY   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLGLUCOSE; GLUCOSE; LEUCINE; LEUCINE CARBOXYMETHYL TRANSFERASE 1; MANNITOL; PHOSPHOPROTEIN PHOSPHATASE 2A; SMALL INTERFERING RNA; THAPSIGARGIN; TRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENE SILENCING; HYPERGLYCEMIA; MALE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; PROTEIN PROCESSING; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CATALYTIC DOMAIN; GLUCOSE; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; OXIDATIVE STRESS; PROTEIN PHOSPHATASE 2; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84893187581     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1773     Document Type: Article

References (48)

1. Prentki M, Matschinsky FM. Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol Rev. 1987;67: 1185-1248.
2. JonesPM,Persaud SJ. Protein kinases, protein phosphorylation, and the regulation of insulin secretion from pancreatic β-cells. Endocr Rev. 1998;19: 429-461.
3. Kowluru A, Seavey SE, Rabaglia ME, Nesher R, Metz SA. Carboxylmethylation of the catalytic subunit of protein phosphatase 2A in insulin-secreting cells: evidence for functional consequences on enzyme activity and insulin secretion. Endocrinology. 1996;137: 2315-2323.
4. Kowluru A. Novel regulatory roles for protein phosphatase-2A in the islet β cell. Biochem Pharmacol. 2005;69: 1681-1691.
5. Leulliot N, Quevillon-Cheruel S, Sorel I, et al. Structure of protein phosphatase methyltransferase 1 (PPM1), a leucine carboxyl methyltransferase involved in the regulation of protein phosphatase 2A activity. J Biol Chem. 2004;279: 8351-8358.
6. Janssens V, Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J. 2001;353: 417-439.
7. Favre B, Zolnierowicz S, Turowski P, Hemmings BA. The catalytic subunit of protein phosphatase 2A is carboxyl-methylated in vivo. J Biol Chem. 1994;269: 16311-16317.
8. Sents W, Ivanova E, Lambrecht C, Haesen D, Janssens V. The biogenesis of active protein phosphatase 2A holoenzymes: a tightly regulated process creating phosphatase specificity. FEBS J. 2013; 280: 644-661.
9. Chen J, Martin BL, Brautigan DL. Regulation of protein serinethreonine phosphatase type-2A by tyrosine phosphorylation. Science. 1992;257: 1261-1264.
10. BegumN, Ragolia L.cAMPcounter-regulates insulin-mediated protein phosphatase-2A inactivation in rat skeletal muscle cells. J Biol Chem. 1996;271: 31166-31171.
11. Poitout V, Robertson RP. Glucolipotoxicity: fuel excess and β-cell dysfunction. Endocr Rev. 2008;29: 351-366.
12. Olson LK, Qian J, Poitout V. Glucose rapidly and reversibly decreases INS-1 cell gene transcription via decrements in STF-1 andC1 activator transcription factor activity. Mol Endocrinol. 1998;12: 207-219.
13. Lupi R, Dotta F, Marselli L, et al. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that β-cell death is caspase mediated, partially de-pendent on ceramide pathway, and Bcl-2 regulated. Diabetes. 2002; 51: 1437-1442.
14. Fonseca SG, Urano F, Burcin M, Gromada J. Stress hyperactivation in the β-cell. Islets. 2010;2: 1-9.
15. Longin S, Zwaenepoel K, Martens E, et al. Spatial control of protein phosphatase 2A (de)methylation. Exp Cell Res. 2008;314: 68-81.
16. Kowluru A, Veluthakal R. Rho guanosine diphosphate-dissociation inhibitor plays a negative modulatory role in glucose-stimulated insulin secretion. Diabetes. 2005;54: 3523-3529.
17. Kowluru A, Veluthakal R, Rhodes CJ, Kamath V, Syed I, Koch BJ. Protein farnesylation-dependent Raf/extracellular signal-related kinase signaling links to cytoskeletal remodeling to facilitate glucoseinduced insulin secretion in pancreatic β-cells. Diabetes. 2010;59: 967-977.
18. Kowluru A, Metz SA. Stimulation by PGE2 of a high-affinity GTPase in the secretory granules of normal rat and human pancreatic islets. Biochem J. 1994;297: 399-406.
19. Kowluru A, Rabaglia ME, Muse KE, Metz SA. Subcellular localization and kinetic characterization of guanine nucleotide binding proteins in normal rat and human pancreatic islets and transformed β-cells. Biochim Biophys Acta. 1994;1222: 348-359.
20. Li G, Kowluru A, Metz SA. Characterization of prenylcysteine methyltransferase in insulin-secreting cells. Biochem J. 1996;316: 345-351.
21. Du Y, Kowluru A, Kern TS. PP2A contributes to endothelial death in high glucose: inhibition by benfotiamine. Am J Physiol Regul Integr Comp Physiol. 2010;299:R1610-R1617.
22. Bryant JC, Westphal RS, Wadzinski BE. Methylated C-terminal leucine residue of PP2A catalytic subunit is important for binding of regulatory Bα subunit. Biochem J. 1999;339: 241-246.
23. Evans DR, Hemmings BA. Mutation of the C-terminal leucine residue of PP2Ac inhibits PR55/B subunit binding and confers supersensitivity to microtubule destabilization in saccharomyces cerevisiae. Mol Gen Genet. 2000;264: 425-432.
24. Reddy AB, Ramana KV, Srivastava S, Bhatnagar A, Srivastava SK. Aldose reductase regulates high glucose-induced ectodomain shedding of tumor necrosis factor (TNF)-α via protein kinase c-δ and TNF-α converting enzyme in vascular smooth muscle cells. Endocrinology. 2009;150: 63-74.
25. Kowluru A, Seavey SE, Li G, et al. Glucose- and GTP-dependent stimulation of the carboxyl methylation of Cdc42 in rodent and human pancreatic islets and pure β cell. J Clin Invest. 1996;98: 540-555.
26. Jangati GR, Veluthakal R, Kowluru A. siRNA-mediated depletion of endogenous protein phosphatase 2Acα markedly attenuates ceramide- activated protein phosphatase activity in insulin-secreting INS-832/13 cells. Biochem Biophys Res Commun. 2006;348: 649-652.
27. Tersey SA, Nishiki Y, Templin AT, et al. Islet β-cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes. 2012;61: 818-827.
28. Back SH, Kaufman RJ. Endoplasmic reticulum stress and type 2 diabetes. Annu Rev Biochem. 2012;81: 767-793.
29. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev. 2008;29: 42-61.
30. Yan L, Guo S, Brault M, et al. The B55α-containing PP2A holoenzyme dephosphorylates FOXO1 in islet β-cells under oxidative stress. Biochem J. 2012;444: 239-247.
31. Kowluru A. Small G proteins in islet β-cell function. Endocr Rev. 2010;31: 52-78.
32. Kowluru A, Matti A. Hyperactivation of protein phosphatase 2A in models of glucolipotoxicity and diabetes: potential mechanisms and functional consequences. Biochem Pharmacol. 2012;84: 591-597.
33. Rastogi S, Sentex E, Elimban V, Dhalla NS, Netticadan T. Elevated levels of protein phosphatase 1 and phosphatase 2A may contribute to cardiac dysfunction in diabetes. Biochem Biophys Acta. 2003; 1638: 273-277.
34. Galbo T, Olsen GS, Quistorff B, Nishimura E. Free fatty acid-induced PP2A hyperactivity selectively impairs hepatic insulin action on glucose metabolism. PLoS One. 2011;6:e27424.
35. Wu Y, Song P, Xu J, Zhang M, Zou MH. Activation of protein phosphatase 2A by palmitate inhibits AMP-activated protein kinase. J Biol Chem. 2007;282: 9777-9788.
36. Højlund K, Poulsen M, Staehr P, Brusgaard K, Beck-Nielsen H. Effect of insulin on protein phosphatase 2A expression in muscle in type 2 diabetes. Eur J Clin Invest. 2002;32: 918-923.
37. Li Q, Li J, Ren J. UCF-101 mitigates streptozotocin-induced cardiomyocyte dysfunction: role of AMPK. Am J Physiol Endocrinol Metab. 2009;297:E965-E973.
38. Araki E, Oyadomari S, Mori M. Endoplasmic reticulum stress and diabetes mellitus. Intern Med. 2003;42: 7-14.
39. Meares GP, Hughes KJ, Naatz A, et al. IRE1-dependent activation of AMPK in response to nitric oxide. Mol Cell Biol. 2011;31: 4286-4297.
40. Baldwin AC, Green CD, Olson LK, Moxley MA, Corbett JA. A role for aberrant protein palmitoylation in FFA-induced ER stress and β-cell death. Am J Physiol Endocrinol Metab. 2012;302:E1390-E1398.
41. Hou ZQ, Li HL, Gao L, Pan L, Zhao JJ, Li GW. Involvement of chronic stresses in rat islets and INS-1 cell glucotoxicity induced by intermittent high glucose. Mol Cell Endocrinol. 2008;291: 71-78.
42. Syed I, Jayaram B, Subasinghe W, Kowluru A. Tiam1/Rac1 signaling pathway mediates palmitate-induced, ceramide-sensitive generation of superoxides and lipid peroxides and loss of mitochondrial membrane potential in pancreatic β-cells. Biochem Pharmacol. 2010;80: 874-883.
43. Subasinghe W, Syed I, Kowluru A. Phagocyte-like NADPH oxidase promotes cytokine-induced mitochondrial dysfunction in pancreatic β-cells: evidence for regulation by Rac1. Am J Physiol Regul Integr Comp Physiol. 2011;300:R12-R20.
44. Kowluru A. Friendly, and not so friendly, roles of Rac1 in isletβ-cell function: lessons learnt from pharmacological and molecular biological approaches. Biochem Pharmacol. 2011;81: 965-975.
45. Syed I, KyathanahalliCN,Jayaram B, et al. Increased phagocyte-like NADPHoxidase andROSgeneration in type 2 diabeticZDFrat and human islets: role of Rac1-JNK1/2 signaling pathway in mitochondrial dysregulation in the diabetic islet. Diabetes. 2011;60: 2843-2852.
46. Mohammed AM, Syeda K, Hadden T, Kowluru A. Upregulation of phagocyte-like NADPH oxidase by cytokines in pancreatic β-cells: attenuation of oxidative and nitrosative stress by 2-bromopalmitate. Biochem Pharmacol. 2013;85: 109-114.
47. Syeda K, Mohammed AM, Arora DK, Kowluru A. Glucotoxic conditions induce endoplasmic stress to cause caspase 3 mediated lamin B degradation in pancreatic β-cells: protection by nifedipine. Biochem Pharmacol. 2013;86: 1338-1346.
48. Castermans D, Somers I, Kriel J, et al. Glucose-induced posttranslational activation of protein phosphatases PP2A and PP1 in yeast. Cell Res. 2012;22: 1058-1077.