Transient overexpression of cyclin D2/CDK4/GLP1 genes induces proliferation and differentiation of adult pancreatic progenitors and mediates islet regeneration

Cell Cycle

Volumn 11, Issue 4, 2012, Pages 695-705

  Chen, Shuyuan ^a   Shimoda, Masyuki ^a   Chen, Jiaxi ^a   Matsumodo, Shinichi ^a   Grayburn, Paul A ^b  

^a BAYLOR RESEARCH INSTITUTE   (United States)

^b BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adult pancreatic progenitor cells; Cell cycle regulation; Diabetes; Differentiation; Islets regeneration; Proliferation

Indexed keywords

CYCLIN D2; CYCLIN DEPENDENT KINASE 4; GLUCAGON LIKE PEPTIDE 1;

ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL REGENERATION; CELLULAR PARAMETERS; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE THERAPY; HYPOTHESIS; MALE; NONHUMAN; PANCREAS CELL; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; PLASMID; RAT; ULTRASOUND TARGETED MICROBUBBLE DESTRUCTION;

RATTUS;

EID: 84863116820     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.11.4.19120     Document Type: Article

References (40)

1. Huang ES, Basu A, O'Grady M, Capretta JC. Projecting the future diabetes population size and related costs for the US Diabetes Care 2009; 32:2225-9; PMID:19940225; http://dx.doi.org/10.2337/dc09-0459.
2. Butler PC, Meier JJ, Butler AE, Bhushan A. The replication of β cells in normal physiology, in disease and for therapy. Nat Clin Pract Endocrinol Metab 2007; 3:758-68; PMID:17955017; http://dx.doi. org/10.1038/ncpendmet0647.
3. Meier JJ. Beta cell mass in diabetes: a realistic therapeutic target? Diabetologia 2008; 51:703-13; PMID:18317728; http://dx.doi.org/10.1007/s00125- 008-0936-9.
4. 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 2005; 48:2221-8; PMID:16205882; http://dx.doi.org/10.1007/s00125-005-1949-2.
5. 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 2003; 52:102-10; PMID:12502499; http://dx.doi. org/10.2337/diabetes.52.1.102.
6. Bonner-Weir S, Weir GC. New sources of pancreatic beta-cells. Nat Biotechnol 2005; 23:857-61; PMID:16003374; http://dx.doi.org/10.1038/nbt1115.
7. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004; 429:41-6; PMID:15129273; http://dx.doi.org/10.1038/nature02520.
8. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008; 455:627-32; PMID:18754011; http://dx.doi.org/10.1038/nature07314.
9. Levine F, Itkin-Ansari P. β-cell Regeneration: neogenesis, replication or both? J Mol Med (Berl) 2008; 86:247-58; PMID:17922102; http://dx.doi. org/10.1007/s00109-007-0259-1.
10. Cozar-Castellano I, Fiaschi-Taesch N, Bigatel TA, Takane KK, Garcia-Ocaña A, Vasavada R, et al. Molecular control of cell cycle progression in the pancreatic beta-cell. Endocr Rev 2006; 27:356-70; PMID:16638909; http://dx.doi.org/10.1210/er.2006-0004.
11. Kushner JA, Ciemerych MA, Sicinska E, Wartschow LM, Teta M, Long SY, et al. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 2005; 25:3752-62; PMID:15831479; http://dx.doi.org/10.1128/MCB.25. 9.3752-62.2005.
12. Georgia S, Bhushan A. p27 Regulates the transition of β-cells from quiescence to proliferation. Diabetes 2006; 55:2950-6; PMID:17065330; http://dx.doi. org/10.2337/db06-0249.
13. Teta M, Long SY, Wartschow LM, Rankin MM, Kushner JA. Very slow turnover of beta-cells in aged adult mice. Diabetes 2005; 54:2557-67; PMID:16123343; http://dx.doi.org/10.2337/diabetes. 54.9.2557.
14. 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; 38:931-50; PMID:16168703; http://dx.doi.org/10.1016/j.biocel.2005.08.003.
15. Kushner JA. Beta-cell growth: an unusual paradigm of organogenesis that is cyclin D2/Cdk4 dependent. Cell Cycle 2006; 5:234-7; PMID:16410729; http://dx.doi. org/10.4161/cc.5.3.2399.
16. He LM, Sartori DJ, Teta M, Opare-Addo LM, Rankin MM, Long SY, et al. Cyclin D2 protein stability is regulated in pancreatic beta-cells. Mol Endocrinol 2009; 23:1865-75; PMID:19628581; http://dx.doi. org/10.1210/me.2009- 0057.
17. Cozar-Castellano I, Takane KK, Bottino R, Balamurugan AN, Stewart AF. Induction of beta-cell proliferation and retinoblastoma protein phosphorylation in rat and human islets using adenovirus-mediated transfer of cyclin-dependent kinase-4 and cyclin D1. Diabetes 2004; 53:149-59; PMID:14693709; http://dx.doi.org/10.2337/diabetes.53.1.149.
18. Fiaschi-Taesch N, Bigatel TA, Sicari B, Takane KK, Salim F, Velazquez-Garcia S, et al. 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 2009; 58:882-93; PMID:19136653; http://dx.doi.org/10.2337/db08-0631.
19. Georgia S, Bhushan A. Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J Clin Invest 2004; 114:963-8; PMID:15467835.
20. Zhong L, Georgia S, Tschen SI, Nakayama K, Nakayama K, Bhushan A. Essential role of Skp2-mediated p27 degradation in growth and adaptive expansion of pancreatic beta cells. J Clin Invest 2007; 117:2869-76; PMID:17823659; http://dx.doi. org/10.1172/JCI32198.
21. Chen S, Ding JH, Bekeredjian R, Yang BZ, Shohet RV, Johnston SA, et al. Efficient gene delivery to pancreatic islets with ultrasonic microbubble destruction technology. Proc Natl Acad Sci USA 2006; 103:8469-74; PMID:16709667; http://dx.doi.org/10.1073/pnas.0602921103.
22. Chen S, Ding J, Yu C, Yang B, Wood DR, Grayburn PA. Reversal of streptozotocin-induced diabetes in rats by gene therapy with betacellulin and pancreatic duodenal homeobox-1. Gene Ther 2007; 14:1102-10; PMID:17460716; http://dx.doi.org/10.1038/sj.gt.3302963.
23. Chai RJ, Chen S, Ding J, Grayburn PA. Efficient, glucose responsive and islet-specific transgene expression by a modified rat insulin promoter. Gene Ther 2009; 16:1202-9; PMID:19727136; http://dx.doi. org/10.1038/gt.2009.114.
24. Chen S, Shimoda M, Wang MY, Ding J, Noguchi H, Matsumoto S, et al. Regeneration of pancreatic islets in vivo by ultrasound-targeted gene therapy. Gene Ther 2010; 17:1411-20; PMID:20508600; http://dx.doi. org/10.1038/gt.2010. 85.
25. Ku HT. Minireview: pancreatic progenitor cells-recent studies. Endocrinology 2008; 149:4312-6; PMID:18535096; http://dx.doi.org/10.1210/en. 2008-0546.
26. Schwitzgebel VM, Scheel DW, Conners JR, Kalamaras J, Lee JE, Anderson DJ, et al. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 2000; 127:3533-42; PMID:10903178.
27. Fiaschi-Taesch NM, Salim F, Kleinberger J, Troxell R, Cozar-Castellano I, Selk K, et al. Induction of human beta-cell proliferation and engraftment using a single G1/S regulatory molecule, cdk6. Diabetes 2010; 59:1926-36; PMID:20668294; http://dx.doi. org/10.2337/db09-1776.
28. 2+ channel-dependent exocytosis. Cell Metab 2010; 11:543-53; PMID:20519125; http://dx.doi.org/10.1016/j. cmet.2010.04.007.
29. Gershengorn MC, Hardikar AA, Wei C, Geras-Raaka E, Marcus-Samuels B, Raaka BM. Epithelial-to-mesenchymal transition generates proliferative human islet precursor cells. Science 2004; 306:2261-4; PMID:15564314; http://dx.doi.org/10.1126/science. 1101968.
30. Davani B, Ariely S, Ikonomou L, Oron Y, Gershengorn MC. Human islet-derived precursor cells can cycle between epithelial clusters and mesenchymal phenotypes. J Cell Mol Med 2009; 13:2570-81; PMID:19175683; http://dx.doi.org/10.1111/j.1582-4934.2008.00570.x.
31. Smukler SR, Arntfield ME, Razavi R, Bikopoulos G, Karpowicz P, Seaberg R, et al. The adult mouse and human pancreas contain rare multipotent stem cells that express insulin. Cell Stem Cell 2011; 8:281-93; PMID:21362568; http://dx.doi.org/10.1016/j. stem.2011.01.015.
32. Seaberg RM, Smukler SR, Kieffer TJ, Enikolopov G, Asghar Z, Wheeler MB, et al. Clonal identification of multipotent precursors from adult mouse pancreas that generate neural and pancreatic lineages. Nat Biotechnol 2004; 22:1115-24; PMID:15322557; http://dx.doi. org/10.1038/nbt1004.
33. Tavana O, Zhu C. Too many breaks (brakes): pancreatic β-cell senescence leads to diabetes. Cell Cycle 2011; 10:2471-84; PMID:21750406; http://dx.doi. org/10.4161/cc.10.15.16741.
34. Gunasekaran U, Gannon M. Type 2 diabetes and the aging pancreatic beta cell. Aging (Albany NY) 2011; 3:565-75; PMID:21765202.
35. Kuhlow D, Florian S, von Figura G, Weimer S, Schulz N, Petzke KJ, et al. Telomerase deficiency impairs glucose metabolism and insulin secretion. Aging (Albany NY) 2010; 2:650-8; PMID:20876939.
36. Joglekar MV, Hardikar AA. Epithelial-to-mesenchymal transition in pancreatic islet beta cells. Cell Cycle 2010; 9:4077-9; PMID:20948307; http://dx.doi. org/10.4161/cc.9.20.13590.
37. Baker GL, Landis MW, Hinds PW. Multiple functions of D-type cyclins can antagonize pRb-mediated suppression of proliferation. Cell Cycle 2005; 4:330-8; PMID:15684604; http://dx.doi.org/10.4161/cc.4.2.1485.
38. van den Heuvel S, Harlow E. Distinct roles for cyclin-dependent kinases in cell cycle control. Science 1993; 262:2050-4; PMID:8266103; http://dx.doi. org/10.1126/science.8266103.
39. Choi S, Oh S, Lee M, Kim SW. Glucagon-like peptide-1 plasmid construction and delivery for the treatment of type 2 diabetes. Mol Ther 2005; 12:885-91; PMID:16039908; http://dx.doi.org/10.1016/j. ymthe.2005.03.039.
40. Terauchi Y, Takamoto I, Kubota N, Matsui J, Suzuki R, Komeda K, et al. Glucokinase and IRS-2 are required for compensatory β cell hyperplasia in response to high-fat diet-induced insulin resistance. J Clin Invest 2007; 117:246-57; PMID:17200721; http://dx.doi. org/10.1172/JCI17645.