Early and late G1/S cyclins and cdks act complementarily to enhance authentic human β-Cell proliferation and expansion

Diabetes

Volumn 64, Issue 10, 2015, Pages 3485-3498

  Tiwari, Shiwani ^a   Roel, Chris ^a   Wills, Rachel ^b   Casinelli, Gabriella ^b   Tanwir, Mansoor ^b   Takane, Karen K ^a   Fiaschi Taesch, Nathalie M ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN E; CYCLIN DEPENDENT KINASE; CYCLINE; GLUCOSE; INSULIN; RETINOBLASTOMA PROTEIN;

ADULT; ANIMAL CELL; ARTICLE; CELL COUNT; CELL CYCLE G1 PHASE; CELL DIVISION; CELL EXPANSION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; AGING; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AGING; ANIMALS; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASES; CYCLINS; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RETINOBLASTOMA PROTEIN;

EID: 84953343386     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-1885     Document Type: Article

References (70)

1. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-Cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110
2. Szabat M, Lynn FC, Hoffman BG, Kieffer TJ, Allan DW, Johnson JD. Maintenance of β-cell maturity and plasticity in the adult pancreas: developmental biology concepts in adult physiology. Diabetes 2012;61:1365-1371
3. Cozar-Castellano I, Fiaschi-Taesch N, Bigatel TA, et al. Molecular control of cell cycle progression in the pancreatic beta-cell. Endocr Rev 2006;27:356-370
4. Cozar-Castellano I, Harb G, Selk K, et al. Lessons from the first comprehensive molecular characterization of cell cycle control in rodent insulinoma cell lines. Diabetes 2008;57:3056-3068
5. Fiaschi-Taesch N, Bigatel TA, Sicari B, et al. Survey of the human pancreatic β-cell G1/S proteome reveals a potential therapeutic role for cdk-6 and cyclin D1 in enhancing human β-cell replication and function in vivo. Diabetes 2009;58:882-893
6. Vasavada RC, Gonzalez-Pertusa JA, Fujinaka Y, Fiaschi-Taesch N, Cozar-Castellano I, Garcia-Ocaña A. Growth factors and beta cell replication. Int J Biochem Cell Biol 2006;38:931-950
7. Fiaschi-Taesch NM, Kleinberger JW, Salim FG, et al. Human pancreatic β-cell G1/S molecule cell cycle atlas. Diabetes 2013;62:2450-2459
8. Wang P, Fiaschi-Taesch NM, Vasavada RC, Scott DK, García-Ocaña A, Stewart AF. Diabetes mellitus-advances and challenges in human β-cell proliferation. Nat Rev Endocrinol 2015;11:201-212
9. Perl S, Kushner JA, Buchholz BA, et al. Significant human beta-cell turnover is limited to the first three decades of life as determined by in vivo thymidine analog incorporation and radiocarbon dating. J Clin Endocrinol Metab 2010;95:E234-E239
10. Meier JJ, Butler AE, Saisho Y, et al. β-Cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 2008;57:1584-1594
11. Köhler CU, Olewinski M, Tannapfel A, Schmidt WE, Fritsch H, Meier JJ. Cell cycle control of β-cell replication in the prenatal and postnatal human pancreas. Am J Physiol Endocrinol Metab 2011;300:E221-E230
12. Saisho Y, Butler AE, Manesso E, Elashoff D, Rizza RA, Butler PC. β-cell mass and turnover in humans: effects of obesity and aging. Diabetes Care 2013;36:111-117
13. Gregg BE, Moore PC, Demozay D, et al. Formation of a human β-cell population within pancreatic islets is set early in life. J Clin Endocrinol Metab 2012;97:3197-3206
14. Fiaschi-Taesch NM, Kleinberger JW, Salim FG, et al. Cytoplasmic-nuclear trafficking of G1/S cell cycle molecules and adult human β-cell replication: a revised model of human β-cell G1/S control. Diabetes 2013;62:2460-2470
15. Avrahami D, Li C, Yu M, et al. Targeting the cell cycle inhibitor p57Kip2 promotes adult human © cell replication. J Clin Invest 2014;124:670-674
16. Burke JR, Hura GL, Rubin SM. Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control. Genes Dev 2012;26:1156-1166
17. Rubin SM. Deciphering the retinoblastoma protein phosphorylation code. Trends Biochem Sci 2013;38:12-19
18. Macdonald JI, Dick FA. Posttranslational modifications of the retinoblastoma tumor suppressor protein as determinants of function. Genes Cancer 2012;3:619-633
19. Malumbres M, Barbacid M. Mammalian cyclin-dependent kinases. Trends Biochem Sci 2005;30:630-641
20. Malumbres M, Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 2009;9:153-166
21. Kushner JA, Ciemerych MA, Sicinska E, et al. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 2005;25:3752-3762
22. Rane SG, Dubus P, Mettus RV, et al. Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia. Nat Genet 1999;22:44-52
23. Alonso LC, Yokoe T, Zhang P, et al. Glucose infusion in mice: a new model to induce β-cell replication. Diabetes 2007;56:1792-1801
24. Salpeter SJ, Klein AM, Huangfu D, Grimsby J, Dor Y. Glucose and aging control the quiescence period that follows pancreatic beta cell replication. Development 2010;137:3205-3213
25. Salpeter SJ, Klochendler A, Weinberg-Corem N, et al. Glucose regulates cyclin D2 expression in quiescent and replicating pancreatic β-cells through glycolysis and calcium channels. Endocrinology 2011;152:2589-2598
26. Karslioglu E, Kleinberger JW, Salim FG, et al. cMyc is a principal upstream driver of beta-cell proliferation in rat insulinoma cell lines and is an effective mediator of human beta-cell replication. Mol Endocrinol 2011;25:1760-1772
27. Song WJ, Schreiber WE, Zhong E, et al. Exendin-4 stimulation of cyclin A2 in β-cell proliferation. Diabetes 2008;57:2371-2381
28. Guthalu Kondegowda N, Joshi-Gokhale S, Harb G, et al. Parathyroid hormone-related protein enhances human β-cell proliferation and function with associated induction of cyclin-dependent kinase 2 and cyclin E expression. Diabetes 2010;59:3131-3138
29. Schisler JC, Fueger PT, Babu DA, et al. Stimulation of human and rat islet beta-cell proliferation with retention of function by the homeodomain transcription factor Nkx6.1. Mol Cell Biol 2008;28:3465-3476
30. Fiaschi-Taesch NM, Berman DM, Sicari BM, et al. Hepatocyte growth factor enhances engraftment and function of nonhuman primate islets. Diabetes 2008;57:2745-2754
31. Fiaschi-Taesch NM, Salim F, Kleinberger J, et al. Induction of human β-cell proliferation and engraftment using a single G1/S regulatory molecule, cdk6. Diabetes 2010;59:1926-1936
32. Parnaud G, Bosco D, Berney T, et al. Proliferation of sorted human and rat beta cells. Diabetologia 2008;51:91-100
33. Liu H, Remedi MS, Pappan KL, et al. Glycogen synthase kinase-3 and mammalian target of rapamycin pathways contribute to DNA synthesis, cell cycle progression, and proliferation in human islets. Diabetes 2009;58:663-672
34. Tyrberg B, Eizirik DL, Hellerström C, Pipeleers DG, Andersson A. Human pancreatic beta-cell deoxyribonucleic acid-synthesis in islet grafts decreases with increasing organ donor age but increases in response to glucose stimulation in vitro. Endocrinology 1996;137:5694-5699
35. Davalli AM, Ogawa Y, Ricordi C, Scharp DW, Bonner-Weir S, Weir GC. A selective decrease in the beta cell mass of human islets transplanted into diabetic nude mice. Transplantation 1995;59:817-820
36. Menge BA, Tannapfel A, Belyaev O, et al. Partial pancreatectomy in adult humans does not provoke β-cell regeneration. Diabetes 2008;57:142-149
37. Rao P, Roccisana J, Takane KK, et al. Gene transfer of constitutively active Akt markedly improves human islet transplant outcomes in diabetic severe combined immunodeficient mice. Diabetes 2005;54:1664-1675
38. Levitt HE, Cyphert TJ, Pascoe JL, et al. Glucose stimulates human beta cell replication in vivo in islets transplanted into NOD-severe combined immunodeficiency (SCID) mice. Diabetologia 2011;54:572-582
39. Metukuri MR, Zhang P, Basantani MK, et al. ChREBP mediates glucosestimulated pancreatic β-cell proliferation. Diabetes 2012;61:2004-2015
40. Wang P, Alvarez-Perez JC, Felsenfeld DP, et al. A high-throughput chemical screen reveals that harmine-mediated inhibition of DYRK1A increases human pancreatic beta cell replication. Nat Med 2015;21:383-388
41. Vasavada RC, Wang L, Fujinaka Y, et al. Protein kinase C-ξ activation markedly enhances β-cell proliferation: an essential role in growth factor mediated β-cell mitogenesis. Diabetes 2007;56:2732-2743
42. Malumbres M, Barbacid M. Cell cycle kinases in cancer. Curr Opin Genet Dev 2007;17:60-65
43. Rieck S, Zhang J, Li Z, et al. Overexpression of hepatocyte nuclear factor-4α initiates cell cycle entry, but is not sufficient to promote β-cell expansion in human islets. Mol Endocrinol 2012;26:1590-1602
44. Brissova M, Fowler MJ, Nicholson WE, et al. Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy. J Histochem Cytochem 2005;53:1087-1097.
45. Rieck S, Kaestner KH. Expansion of beta-cell mass in response to pregnancy. Trends Endocrinol Metab 2010;21:151-158
46. Dor Y, Melton DA. Facultative endocrine progenitor cells in the adult pancreas. Cell 2008;132:183-184
47. Scharfmann R, Pechberty S, Hazhouz Y, et al. Development of a conditionally immortalized human pancreatic b cell line. J Clin Invest 2014;124:2087-2098
48. Carlier G, Maugein A, Cordier C, et al. Human fucci pancreatic beta cell lines: new tools to study beta cell cycle and terminal differentiation. PLoS One 2014;9:e108202
49. Gorges LL, Lents NH, Baldassare JJ. The extreme COOH terminus of the retinoblastoma tumor suppressor protein pRb is required for phosphorylation on Thr-373 and activation of E2F. Am J Physiol Cell Physiol 2008;295:C1151-C1160
50. Lents NH, Gorges LL, Baldassare JJ. Reverse mutational analysis reveals threonine-373 as a potentially sufficient phosphorylation site for inactivation of the retinoblastoma tumor suppressor protein (pRB). Cell Cycle 2006;5:1699-1707
51. Kozar K, Ciemerych MA, Rebel VI, et al. Mouse development and cell proliferation in the absence of D-cyclins. Cell 2004;118:477-491
52. Kozar K, Sicinski P. Cell cycle progression without cyclin D-CDK4 and cyclin D-CDK6 complexes. Cell Cycle 2005;4:388-391
53. Keenan SM, Lents NH, Baldassare JJ. Expression of cyclin E renders cyclin D-CDK4 dispensable for inactivation of the retinoblastoma tumor suppressor protein, activation of E2F, and G1-S phase progression. J Biol Chem 2004;279:5387-5396
54. Korzelius J, The I, Ruijtenberg S, et al. Caenorhabditis elegans cyclin D/CDK4 and cyclin E/CDK2 induce distinct cell cycle re-entry programs in differentiated muscle cells. PLoS Genet 2011;7:e1002362
55. Lukas J, Herzinger T, Hansen K, et al. Cyclin E-induced S phase without activation of the pRb/E2F pathway. Genes Dev 1997;11:1479-1492
56. Johnson N, Shapiro GI. Cyclin-dependent kinases (cdks) and the DNA damage response: rationale for cdk inhibitor-chemotherapy combinations as an anticancer strategy for solid tumors. Expert Opin Ther Targets 2010;14:1199-1212
57. Yata K, Esashi F. Dual role of CDKs in DNA repair: to be, or not to be. DNA Repair (Amst) 2009;8:6-18
58. Thorel F, Népote V, Avril I, et al. Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 2010;464:1149-1154
59. Ye L, Robertson MA, Hesselson D, Stainier DY, Anderson RM. Glucagon is essential for alpha cell transdifferentiation and beta cell neogenesis. Development 2015;142:1407-1417
60. Malumbres M. Physiological relevance of cell cycle kinases. Physiol Rev 2011;91:973-1007
61. Moore JD, Yang J, Truant R, Kornbluth S. Nuclear import of Cdk/cyclin complexes: identification of distinct mechanisms for import of Cdk2/cyclin E and Cdc2/cyclin B1. J Cell Biol 1999;144:213-224
62. Jackman M, Kubota Y, den Elzen N, Hagting A, Pines J. Cyclin A- and cyclin E-Cdk complexes shuttle between the nucleus and the cytoplasm. Mol Biol Cell 2002;13:1030-1045
63. Tschen SI, Dhawan S, Gurlo T, Bhushan A. Age-dependent decline in betacell proliferation restricts the capacity of β-cell regeneration in mice. Diabetes 2009;58:1312-1320
64. Chen X, Zhang X, Chen F, Larson CS, Wang LJ, Kaufman DB. Comparative study of regenerative potential of beta cells from young and aged donor mice using a novel islet transplantation model. Transplantation 2009;88:496-503
65. Chen H, Gu X, Su IH, et al. Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev 2009;23:975-985
66. Hinault C, Hu J, Maier BF, Mirmira RG, Kulkarni RN. Differential expression of cell cycle proteins during ageing of pancreatic islet cells. Diabetes Obes Metab 2008;10(Suppl. 4):136-146
67. Rankin MM, Kushner JA. Aging induces a distinct gene expression program in mouse islets. Islets 2010;2:345-352
68. Maedler K, Schumann DM, Schulthess F, et al. Aging correlates with decreased β-cell proliferative capacity and enhanced sensitivity to apoptosis: a potential role for Fas and pancreatic duodenal homeobox-1. Diabetes 2006;55:2455-2462
69. Krishnamurthy J, Ramsey MR, Ligon KL, et al. p16INK4a induces an agedependent decline in islet regenerative potential. Nature 2006;443:453-457
70. Kushner JA. The role of aging upon β cell turnover. J Clin Invest 2013;123:990-995