Cell cycle control of β-cell replication in the prenatal and postnatal human pancreas

American Journal of Physiology - Endocrinology and Metabolism

Volumn 300, Issue 1, 2011, Pages

  Köhler, Christina U ^a   Olewinski, Marvin ^a   Tannapfel, Andrea ^b   Schmidt, Wolfgang E ^a   Fritsch, Helga ^c   Meier, Juris J ^a  

^a ST JOSEF HOSPITAL   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Cyclin D3; Development; p16; p27

Indexed keywords

CELL CYCLE PROTEIN; CYCLIN D3; INSULIN; KI 67 ANTIGEN; PROTEIN P16; PROTEIN P27;

ADULT; ARTICLE; CELL CYCLE REGULATION; CELL DIVISION; EMBRYO; FEMALE; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; PANCREAS ISLET BETA CELL; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADULT; AGED; AGED, 80 AND OVER; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIVISION; CYCLIN D3; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FEMALE; GESTATIONAL AGE; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN-SECRETING CELLS; KI-67 ANTIGEN; MALE; MIDDLE AGED; PANCREAS;

EID: 78650778644     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00496.2010     Document Type: Article

References (52)

1. Agarwal SK, Mateo CM, Marx SJ. Rare germline mutations in cyclin-dependent kinase inhibitor genes in multiple endocrine neoplasia type 1 and related states. J Clin Endocrinol Metab 94: 1826-1834, 2009.
2. Alonso LC, Yokoe T, Zhang P, Scott DK, Kim SK, O'Donnell CP, Garcia-Ocana A. Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes 56: 1792-1801, 2007. (Pubitemid 47025447)
3. Bartkova J, Zemanova M, Bartek J. Abundance and subcellular localisation of cyclin D3 in human tumours. Int J Cancer 65: 323-327, 1996. (Pubitemid 26059986)
4. Bonner-Weir S, Baxter LA, Schuppin GT, Smith FE. A second pathway for regeneration of adult exocrine and endocrine pancreas. A possible recapitulation of embryonic development. Diabetes 42: 1715-1720, 1993.
5. Broadbent HM, Peden JF, Lorkowski S, Goel A, Ongen H, Green F, Clarke R, Collins R, Franzosi MG, Tognoni G, Seedorf U, Rust S, Eriksson P, Hamsten A, Farrall M, Watkins H. Susceptibility to coronary artery disease and diabetes is encoded by distinct, tightly linked SNPs in the ANRIL locus on chromosome 9p. Hum Mol Genet 17: 806-814, 2008.
6. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52: 102-110, 2003. (Pubitemid 36042113)
7. Canavese G, Azzoni C, Pizzi S, Corleto VD, Pasquali C, Davoli C, Crafa P, Delle Fave G, Bordi C. p27: a potential main inhibitor of cell proliferation in digestive endocrine tumors but not a marker of benign behavior. Hum Pathol 32: 1094-1101, 2001.
8. Chen H, Gu X, Su IH, Bottino R, Contreras JL, Tarakhovsky A, Kim SK. Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev 23: 975-985, 2009.
9. Ciemerych MA, Kenney AM, Sicinska E, Kalaszczynska I, Bronson RT, Rowitch DH, Gardner H, Sicinski P. Development of mice expressing a single D-type cyclin. Genes Dev 16: 3277-3289, 2002. (Pubitemid 36025979)
10. Cozar-Castellano I, Fiaschi-Taesch N, Bigatel TA, Takane KK, Garcia-Ocana A, Vasavada R, Stewart AF. Molecular control of cell cycle progression in the pancreatic beta cell. Endocr Rev 25: 25, 2006.
11. Davalli AM, Perego L, Bertuzzi F, Finzi G, La Rosa S, Blau A, Placidi C, Nano R, Gregorini L, Perego C, Capella C, Folli F. Disproportionate hyperproinsulinemia, beta-cell restricted prohormone convertase 2 deficiency, and cell cycle inhibitors expression by human islets transplanted into athymic nude mice: insights into nonimmune-mediated mechanisms of delayed islet graft failure. Cell Transplant 17: 1323-1336, 2008.
12. Dhawan S, Tschen SI, Bhushan A. Bmi-1 regulates the Ink4a/Arf locus to control pancreatic beta-cell proliferation. Genes Dev 23: 906-911, 2009.
13. Doglioni C, Chiarelli C, Macri E, Dei Tos AP, Meggiolaro E, Dalla Palma P, Barbareschi M. Cyclin D3 expression in normal, reactive and neoplastic tissues. J Pathol 185: 159-166, 1998.
14. Draper N, Bui M, Boulware DC, Lloyd M, Chiappori AA, Pledger WJ, Coppola D. Increased cyclin D3 expression significantly correlates with p27 nuclear positivity in gastrointestinal stromal tumors. Hum Pathol 39: 1784-1791, 2008.
15. Eshkoor SA, Ismail P, Rahman SA, Oshkour SA. p16 gene expression in basal cell carcinoma. Arch Med Res 39: 668-673, 2008.
16. Fiaschi-Taesch N, Bigatel TA, Sicari B, Takane KK, Salim F, Velazquez-Garcia S, Harb G, Selk K, Cozar-Castellano I, Stewart AF. Survey of the human pancreatic beta-cell G1/S proteome reveals a potential therapeutic role for cdk-6 and cyclin D1 in enhancing human beta-cell replication and function in vivo. Diabetes 58: 882-893, 2009.
17. Fiaschi-Taesch NM, Salim F, Kleinberger J, Troxell R, Cozar-Castellano I, Selk K, Cherok E, Takane KK, Scott DK, Stewart AF. Induction of human beta-cell proliferation and engraftment using a single G1/S regulatory molecule, cdk6. Diabetes 59: 1926-1936.
18. Florenes VA, Faye RS, Maelandsmo GM, Nesland JM, Holm R. Levels of cyclin D1 and D3 in malignant melanoma: deregulated cyclin D3 expression is associated with poor clinical outcome in superficial melanoma. Clin Cancer Res 6: 3614-3620, 2000.
19. Friedrichsen BN, Neubauer N, Lee YC, Gram VK, Blume N, Petersen JS, Nielsen JH, Moldrup A. Stimulation of pancreatic beta-cell replication by incretins involves transcriptional induction of cyclin D1 via multiple signalling pathways. J Endocrinol 188: 481-492, 2006.
20. Georgia S, Bhushan A. p27 Regulates the transition of beta-cells from quiescence to proliferation. Diabetes 55: 2950-2956, 2006. (Pubitemid 44923631)
21. Georgitsi M, Raitila A, Karhu A, van der Luijt RB, Aalfs CM, Sane T, Vierimaa O, Makinen MJ, Tuppurainen K, Paschke R, Gimm O, Koch CA, Gundogdu S, Lucassen A, Tischkowitz M, Izatt L, Aylwin S, Bano G, Hodgson S, De Menis E, Launonen V, Vahteristo P, Aaltonen LA. Germline CDKN1B/p27Kip1 mutation in multiple endocrine neoplasia. J Clin Endocrinol Metab 92: 3321-3325, 2007.
22. Gordon KE, Ireland H, Roberts M, Steeghs K, McCaul JA, Mac-Donald DG, Parkinson EK. High levels of telomere dysfunction bestow a selective disadvantage during the progression of human oral squamous cell carcinoma. Cancer Res 63: 458-467, 2003.
23. Harb G, Vasavada RC, Cobrinik D, Stewart AF. The retinoblastoma protein and its homolog p130 regulate the G1/S transition in pancreatic beta-cells. Diabetes 58: 1852-1862, 2009.
24. Kassem SA, Ariel I, Thornton PS, Scheimberg I, Glaser B. Beta-cell proliferation and apoptosis in the developing normal human pancreas and in hyperinsulinism of infancy. Diabetes 49: 1325-1333, 2000.
25. Korbonits M, Chahal HS, Kaltsas G, Jordan S, Urmanova Y, Khalimova Z, Harris PE, Farrell WE, Claret FX, Grossman AB. Expression of phosphorylated p27(Kip1) protein and Jun activation domain-binding protein 1 in human pituitary tumors. J Clin Endocrinol Metab 87: 2635-2643, 2002.
26. Krishnamurthy J, Ramsey MR, Ligon KL, Torrice C, Koh A, Bonner-Weir S, Sharpless NE. p16INK4a induces an age-dependent decline in islet regenerative potential. Nature 443: 453-457, 2006. (Pubitemid 44477281)
27. Krishnamurthy J, Torrice C, Ramsey MR, Kovalev GI, Al-Regaiey K, Su L, Sharpless NE. Ink4a/Arf expression is a biomarker of aging. J Clin Invest 114: 1299-1307, 2004.
28. Kushner JA, Ciemerych MA, Sicinska E, Wartschow LM, Teta M, Long SY, Sicinski P, White MF. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 25: 3752-3762, 2005.
29. Meier JJ. Beta cell mass in diabetes: a realistic therapeutic target? Diabetologia 4: 4, 2008.
30. Meier JJ, Bhushan A, Butler AE, Rizza RA, Butler PC. Sustained beta-cell apoptosis in patients with long-standing type 1 diabetes: Indirect evidence for islet regeneration? Diabetologia 48: 2221-2228, 2005.
31. Meier JJ, Bhushan A, Butler PC. The Potential for Stem Cell Therapy in Diabetes. Pediatr Res 59: 65R-73R, 2006.
32. Meier JJ, Butler AE, Saisho Y, Monchamp T, Galasso R, Bhushan A, Rizza RA, Butler PC. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 57: 1584-1594, 2008.
33. Meier JJ, Butler PC. Insulin secretion. In: Endocrinology (5th ed.), edited by DeGroot LJ and Jameson JL. Philadelphia, PA: Elsevier Saunders, 2005, p. 961-973.
34. Meier JJ, Kohler CU, Alkhatib B, Sergi C, Junker T, Klein HH, Schmidt WE, Fritsch H. Beta-cell development and turnover during prenatal life in humans. Eur J Endocrinol 162: 559-568.
35. Meier JJ, Menge BA, Breuer TG, Muller CA, Tannapfel A, Uhl W, Schmidt WE, Schrader H. Functional assessment of pancreatic beta-cell area in humans. Diabetes 58: 1595-1603, 2009.
36. Nielsen GP, Stemmer-Rachamimov AO, Shaw J, Roy JE, Koh J, Louis DN. Immunohistochemical survey of p16INK4A expression in normal human adult and infant tissues. Lab Invest 79: 1137-1143, 1999.
37. Ogino S, Shima K, Nosho K, Irahara N, Baba Y, Wolpin BM, Giovannucci EL, Meyerhardt JA, Fuchs CS. A cohort study of p27 localization in colon cancer, body mass index, and patient survival. Cancer Epidemiol Biomarkers Prev 18: 1849-1858, 2009.
38. Parry D, Mahony D, Wills K, Lees E. Cyclin D-CDK subunit arrangement is dependent on the availability of competing INK4 and p21 class inhibitors. Mol Cell Biol 19: 1775-1783, 1999.
39. Pei XH, Xiong Y. Biochemical and cellular mechanisms of mammalian CDK inhibitors: a few unresolved issues. Oncogene 24: 2787-2795, 2005.
40. Pellegata NS, Quintanilla-Martinez L, Siggelkow H, Samson E, Bink K, Hofler H, Fend F, Graw J, Atkinson MJ. Germ-line mutations in p27Kip1 cause a multiple endocrine neoplasia syndrome in rats and humans. Proc Natl Acad Sci USA 103: 15558-15563, 2006.
41. Rachdi L, Balcazar N, Elghazi L, Barker DJ, Krits I, Kiyokawa H, Bernal-Mizrachi E. Differential effects of p27 in regulation of beta-cell mass during development, neonatal period, and adult life. Diabetes 55: 3520-3528, 2006. (Pubitemid 44923613)
42. Rivard N, L'Allemain G, Bartek J, Pouyssegur J. Abrogation of p27Kip1 by cDNA antisense suppresses quiescence (G0 state) in fibroblasts. J Biol Chem 271: 18337-18341, 1996.
43. Russo AA, Tong L, Lee JO, Jeffrey PD, Pavletich NP. Structural basis for inhibition of the cyclin-dependent kinase Cdk6 by the tumour suppressor p16INK4a. Nature 395: 237-243, 1998.
44. Sanchez-Beato M, Camacho FI, Martinez-Montero JC, Saez AI, Villuendas R, Sanchez-Verde L, Garcia JF, Piris MA. Anomalous high p27/KIP1 expression in a subset of aggressive B-cell lymphomas is associated with cyclin D3 overexpression. p27/KIP1-cyclin D3 colocalization in tumor cells. Blood 94: 765-772, 1999.
45. Sanki A, Li W, Colman M, Karim RZ, Thompson JF, Scolyer RA. Reduced expression of p16 and p27 is correlated with tumour progression in cutaneous melanoma. Pathology 39: 551-557, 2007.
46. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512, 1999.
47. Troncone G, Martinez JC, Iaccarino A, Zeppa P, Caleo A, Russo M, Migliaccio I, Motti ML, Califano D, Palmieri EA, Palombini L. p27Kip1 is expressed in proliferating cells in its form phosphorylated on threonine 187. BMC Clin Pathol 5: 3, 2005.
48. Tschen SI, Dhawan S, Gurlo T, Bhushan A. Age-dependent decline in beta-cell proliferation restricts the capacity of beta-cell regeneration in mice. Diabetes 58: 1312-1320, 2009.
49. Uchida T, Nakamura T, Hashimoto N, Matsuda T, Kotani K, Sakaue H, Kido Y, Hayashi Y, Nakayama KI, White MF, Kasuga M. Deletion of Cdkn1b ameliorates hyperglycemia by maintaining compensatory hyperinsulinemia in diabetic mice. Nat Med 11: 175-182, 2005.
50. Zeggini E, Weedon MN, Lindgren CM, Frayling TM, Elliott KS, Lango H, Timpson NJ, Perry JR, Rayner NW, Freathy RM, Barrett JC, Shields B, Morris AP, Ellard S, Groves CJ, Harries LW, Marchini JL, Owen KR, Knight B, Cardon LR, Walker M, Hitman GA, Morris AD, Doney AS, McCarthy MI, Hattersley AT. Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science 316: 1336-1341, 2007.
51. Zhang X, Gaspard JP, Mizukami Y, Li J, Graeme-Cook F, Chung DC. Overexpression of cyclin D1 in pancreatic beta-cells in vivo results in islet hyperplasia without hypoglycemia. Diabetes 54: 712-719, 2005. (Pubitemid 40322073)
52. Zhong L, Georgia S, Tschen SI, Nakayama K, Bhushan A. Essential role of Skp2-mediated p27 degradation in growth and adaptive expansion of pancreatic beta cells. J Clin Invest 117: 2869-2876, 2007.