Insulin demand regulates β cell number via the unfolded protein response

Journal of Clinical Investigation

Volumn 125, Issue 10, 2015, Pages 3831-3846

  Sharma, Rohit B ^a   O'Donnell, Amy C ^b   Stamateris, Rachel E ^a   Ha, Binh ^a   McCloskey, Karen M ^b   Reynolds, Paul R ^c   Arvan, Peter ^d   Alonso, Laura C ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c DEPARTMENT OF MEDICINE   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CASPASE 3; INITIATION FACTOR 2ALPHA; INSULIN; ATF6 PROTEIN, HUMAN; ATF6 PROTEIN, MOUSE; BIOLOGICAL MARKER; HYBRID PROTEIN; LEPTIN RECEPTOR; LEPTIN RECEPTOR, MOUSE; PROINSULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL COUNT; CELL DEATH; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENETIC MODEL; HUMAN; HUMAN CELL; HYPERGLYCEMIA; MALE; MOUSE; NONHUMAN; ORGAN SIZE; PRIORITY JOURNAL; PROTEOMICS; UNFOLDED PROTEIN RESPONSE; ADAPTATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; BIOSYNTHESIS; C57BL MOUSE; CALCIUM SIGNALING; CELL CULTURE; CELL DIVISION; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; METABOLISM; MUTANT MOUSE STRAIN; OBESITY; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN PROCESSING; ROUGH ENDOPLASMIC RETICULUM; ULTRASTRUCTURE;

ACTIVATING TRANSCRIPTION FACTOR 6; ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOMARKERS; CALCIUM SIGNALING; CELL DIVISION; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; ENDOPLASMIC RETICULUM, ROUGH; GENE EXPRESSION REGULATION; GLYCOSYLATION; HUMANS; HYPERGLYCEMIA; INSULIN; INSULIN-SECRETING CELLS; MALE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; OBESITY; PROINSULIN; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, LEPTIN; RECOMBINANT FUSION PROTEINS; UNFOLDED PROTEIN RESPONSE;

EID: 84943253417     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI79264     Document Type: Article

References (66)

1. Weir GC, Bonner-Weir S. Islet β cell mass in diabetes and how it relates to function, birth, and death. Ann N Y Acad Sci. 2013;1281:92-105.
2. Costes S, Langen R, Gurlo T, Matveyenko AV, Butler PC. β-Cell failure in type 2 diabetes: a case of asking too much of too few? Diabetes. 2013;62(2):327-335.
3. Back SH, Kaufman RJ. Endoplasmic reticulum stress and type 2 diabetes. Annu Rev Biochem. 2012;81:767-793.
4. Papa FR. Endoplasmic reticulum stress, pancreatic β-cell degeneration, and diabetes. Cold Spring Harb Perspect Med. 2012;2(9):a007666.
5. Mirmira RG. Saturated free fatty acids: islet β cell "stressERs". Endocrine. 2012;42(1):1-2.
6. Eizirik DL, Cnop M. ER stress in pancreatic beta cells: the thin red line between adaptation and failure. Sci Signal. 2010;3(110):pe7.
7. Ron D, Harding HP. Protein-folding homeostasis in the endoplasmic reticulum and nutritional regulation. Cold Spring Harb Perspect Biol. 2012;4(12):a013177.
8. Sachdeva MM, Stoffers DA. Minireview: Meeting the demand for insulin: molecular mechanisms of adaptive postnatal beta-cell mass expansion. Mol Endocrinol. 2009;23(6):747-758.
9. Butler AE, et al. Hematopoietic stem cells derived from adult donors are not a source of pancreatic β-cells in adult nondiabetic humans. Diabetes. 2007;56(7):1810-1816.
10. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation. Nature. 2004;429(6987):41-46.
11. Georgia S, Bhushan A. Beta cell replication is the primary mechanism for maintaining postnatal β cell mass. J Clin Invest. 2004;114(7):963-968.
12. Teta M, Rankin MM, Long SY, Stein GM, Kushner JA. Growth and regeneration of adult β cells does not involve specialized progenitors. Dev Cell. 2007;12(5):817-826.
13. Brennand K, Huangfu D, Melton D. All β cells contribute equally to islet growth and maintenance. PLoS Biol. 2007;5(7):e163.
14. Fontés G, et al. Glucolipotoxicity age-dependently impairs beta cell function in rats despite a marked increase in β cell mass. Diabetologia. 2010;53(11):2369-2379.
15. Alonso LC, et al. Glucose infusion in mice: a new model to induce β-cell replication. Diabetes. 2007;56(7):1792-1801.
16. Bonner-Weir S, Deery D, Leahy JL, Weir GC. Compensatory growth of pancreatic β-cells in adult rats after short-term glucose infusion. Diabetes. 1989;38(1):49-53.
17. Flier SN, Kulkarni RN, Kahn CR. Evidence for a circulating islet cell growth factor in insulin-resistant states. Proc Natl Acad Sci U S A. 2001;98(13):7475-7480.
18. Salpeter SJ, Khalaileh A, Weinberg-Corem N, Ziv O, Glaser B, Dor Y. Systemic regulation of the age-related decline of pancreatic β-cell replication. Diabetes. 2013;62(8):2843-2848.
19. Porat S, et al. Control of pancreatic β cell regeneration by glucose metabolism. Cell Metab. 2011;13(4):440-449.
20. Metukuri MR, et al. ChREBP mediates glucosestimulated pancreatic β-cell proliferation. Diabetes. 2012;61(8):2004-2015.
21. El Ouaamari A, et al. Liver-derived systemic factors drive βcell hyperplasia in insulin-resistant states. Cell Rep. 2013;3(2):401-410.
22. Demirci C, et al. Loss of HGF/c-Met signaling in pancreatic β-cells leads to incomplete maternal β-cell adaptation and gestational diabetes mellitus. Diabetes. 2012;61(5):1143-1152.
23. Zarrouki B, et al. Epidermal growth factor receptor signaling promotes pancreatic β-cell proliferation in response to nutrient excess in rats through mTOR and FOXM1. Diabetes. 2014;63(3):982-993.
24. Pascoe J, et al. Free fatty acids block glucoseinduced β-cell proliferation in mice by inducing cell cycle inhibitors p16 and p18. Diabetes. 2012;61(3):632-641.
25. Yokoe T, et al. Intermittent hypoxia reverses the diurnal glucose rhythm and causes pancreatic β-cell replication in mice. J Physiol. 2008;586(3):899-911.
26. Chang SC, et al. Rat gene encoding the 78-kDa glucose-regulated protein GRP78: its regulatory sequences and the effect of protein glycosylation on its expression. Proc Natl Acad Sci U S A. 1987;84(3):680-684.
27. Hetz C, et al. The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J Neurosci. 2005;25(11):2793-2802.
28. Stamateris RE, Sharma RB, Hollern DA, Alonso LC. Adaptive β-cell proliferation increases early in high-fat feeding in mice, concurrent with metabolic changes, with induction of islet cyclin D2 expression. Am J Physiol Endocrinol Metab. 2013;305(1):E149-E159.
29. Chan JY, Luzuriaga J, Bensellam M, Biden TJ, Laybutt DR. Failure of the adaptive unfolded protein response in islets of obese mice is linked with abnormalities in β-cell gene expression and progression to diabetes. Diabetes. 2013;62(5):1557-1568.
30. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest. 2008;118(10):3378-3389.
31. Laybutt DR, et al. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia. 2007;50(4):752-763.
32. Matsuda T, et al. Ablation of C/EBPβ alleviates ER stress and pancreatic β cell failure through the GRP78 chaperone in mice. J Clin Invest. 2010;120(1):115-126.
33. Oyadomari S, et al. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest. 2002;109(4):525-532.
34. Yoshioka M, Kayo T, Ikeda T, Koizuni A. A novel locus, Mody4, distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6 (Akita) mutant mice. Diabetes. 1997;46(5):887-894.
35. Kayo T, Koizumi A. Mapping of murine diabetogenic gene mody on chromosome 7 at D7Mit258 and its involvement in pancreatic islet and β cell development during the perinatal period. J Clin Invest. 1998;101(10):2112-2118.
36. Özcan U, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science. 2006;313(5790):1137-1140.
37. Axten JM, et al. Discovery of 7-methyl-5-(1-{[3-(trifluoromethyl)phenyl]acetyl}-2,3-dihydro-1Hindol-5-yl)-7H-pyrrolo[2,3-d]pyrimidin-4-amine (GSK2606414), a potent and selective first-inclass inhibitor of protein kinase R (PKR)-like endoplasmic reticulum kinase (PERK). J Med Chem. 2012;55(16):7193-7207.
38. Cross BC, et al. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule. Proc Natl Acad Sci U S A. 2012;109(15):E869-E878.
39. Okada T, et al. A serine protease inhibitor prevents endoplasmic reticulum stressinduced cleavage but not transport of the membrane-bound transcription factor ATF6. J Biol Chem. 2003;278(33):31024-31032.
40. Bernal-Mizrachi E, et al. Human β-cell proliferation and intracellular signaling part 2: still driving in the dark without a road map. Diabetes. 2014;63(3):819-831.
41. Kulkarni RN, Mizrachi EB, Ocana AG, Stewart AF. Human β-cell proliferation and intracellular signaling: driving in the dark without a road map. Diabetes. 2012;61(9):2205-2213.
42. Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013;32(7):805-818.
43. Scheuner D, et al. Control of mRNA translation preserves endoplasmic reticulum function in β cells and maintains glucose homeostasis. Nat Med. 2005;11(7):757-764.
44. Longuet C, et al. Liver-specific disruption of the murine glucagon receptor produces α-cell hyperplasia: evidence for a circulating α-cell growth factor. Diabetes. 2013;62(4):1196-1205.
45. Fukagawa M, Nakanishi S, Kazama JJ. Basic and clinical aspects of parathyroid hyperplasia in chronic kidney disease. Kidney Int Suppl. 2006;(102):S3-S7.
46. Mittag J, Friedrichsen S, Strube A, Heuer H, Bauer K. Analysis of hypertrophic thyrotrophs in pituitaries of athyroid Pax8-/-mice. Endocrinology. 2009;150(9):4443-4449.
47. Horvath E, Kovacs K, Scheithauer BW. Pituitary hyperplasia. Pituitary. 1999;1(3-4):169-179.
48. Barber TM, Adams E, Ansorge O, Byrne JV, Karavitaki N, Wass JA. Nelson's syndrome. Eur J Endocrinol. 2010;163(4):495-507.
49. Hodish I, et al. In vivo misfolding of proinsulin below the threshold of frank diabetes. Diabetes. 2011;60(8):2092-2101.
50. Matveyenko AV, Gurlo T, Daval M, Butler AE, Butler PC. Successful versus failed adaptation to high-fat diet-induced insulin resistance: the role of IAPP-induced β-cell endoplasmic reticulum stress. Diabetes. 2009;58(4):906-916.
51. Cunha DA, et al. Death protein 5 and p53-upregulated modulator of apoptosis mediate the endoplasmic reticulum stress-mitochondrial dialog triggering lipotoxic rodent and human β-cell apoptosis. Diabetes. 2012;61(11):2763-2775.
52. Wang R, Munoz EE, Zhu S, McGrath BC, Cavener DR. Perk gene dosage regulates glucose homeostasis by modulating pancreatic β-cell functions. PLoS One. 2014;9(6):e99684.
53. Gao Y, et al. PERK is required in the adult pancreas and is essential for maintenance of glucose homeostasis. Mol Cell Biol. 2012;32(24):5129-5139.
54. Lee AH, Heidtman K, Hotamisligil GS, Glimcher LH. Dual and opposing roles of the unfolded protein response regulated by IRE1α and XBP1 in proinsulin processing and insulin secretion. Proc Natl Acad Sci U S A. 2011;108(21):8885-8890.
55. Thorpe JA, Schwarze SR. IRE1α controls cyclin A1 expression and promotes cell proliferation through XBP-1. Cell Stress Chaperones. 2010;15(5):497-508.
56. Usui M, et al. Atf6α-null mice are glucose intolerant due to pancreatic β-cell failure on a high-fat diet but partially resistant to diet-induced insulin resistance. Metabolism. 2012;61(8):1118-1128.
57. Engin F, et al. Restoration of the unfolded protein response in pancreatic β cells protects mice against type 1 diabetes. Sci Transl Med. 2013;5(211):211ra156.
58. Elouil H, et al. Acute nutrient regulation of the unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia. 2007;50(7):1442-1452.
59. Vander Mierde D, et al. Glucose activates a protein phosphatase-1-mediated signaling pathway to enhance overall translation in pancreatic β-cells. Endocrinology. 2007;148(2):609-617.
60. Greenman IC, Gomez E, Moore CE, Herbert TP. Distinct glucose-dependent stress responses revealed by translational profiling in pancreatic β-cells. J Endocrinol. 2007;192(1):179-187.
61. Sidrauski C, McGeachy AM, Ingolia NT, Walter P. The small molecule ISRIB reverses the effects of eIF2α phosphorylation on translation and stress granule assembly. eLife. 2015;4:e05033.
62. Blandino-Rosano M, et al. mTORC1 signaling and regulation of pancreatic β-cell mass. Cell Cycle. 2012;11(10):1892-1902.
63. Tersey SA, et al. Islet β-cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes. 2012;61(4):818-827.
64. Marhfour I, et al. Expression of endoplasmic reticulum stress markers in the islets of patients with type 1 diabetes. Diabetologia. 2012;55(9):2417-2420.
65. Yang C, Diiorio P, Jurczyk A, O'Sullivan-Murphy B, Urano F, Bortell R. Pathological endoplasmic reticulum stress mediated by the IRE1 pathway contributes to pre-insulitic beta cell apoptosis in a virus-induced rat model of type 1 diabetes. Diabetologia. 2013;56(12):2638-2646.
66. Unlü M, Morgan ME, Minden JS. Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis. 1997;18(11):2071-2077.