Connective tissue growth factor modulates adult β-cell maturity and proliferation to promote β-cell regeneration in mice

Diabetes

Volumn 64, Issue 4, 2015, Pages 1284-1298

  Riley, Kimberly G ^a   Pasek, Raymond C ^b   Maulis, Matthew F ^b   Peek, Jennifer ^b   Thorel, Fabrizio ^c   Brigstock, David R ^d   Herrera, Pedro L ^c   Gannon, Maureen ^a,b,e  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d OHIO STATE UNIVERSITY   (United States)

^e DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BETA1 INTEGRIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CONNECTIVE TISSUE GROWTH FACTOR; CYCLIN B1; CYCLIN D1; CYCLIN D2; CYCLIN D3; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; GELATINASE A; GLUCOSE; KI 67 ANTIGEN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OSTEOGENIC PROTEIN 1; PROTEIN P16; SCATTER FACTOR; SEROTONIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TRYPTOPHAN HYDROXYLASE; UVOMORULIN; CADHERIN;

ADULT; ANIMAL CELL; ARTICLE; CELL CONTACT; CELL COUNT; CELL CYCLE REGULATION; CELL DENSITY; CELL DESTRUCTION; CELL DIVISION; CELL MATURATION; CELL PROLIFERATION; CELL REGENERATION; CELL SELF-RENEWAL; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; IN VIVO STUDY; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; UPREGULATION; ANIMAL; CELL CYCLE; CELL DEATH; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; REGENERATION;

ANIMALS; ANTIGENS, CD29; CADHERINS; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CONNECTIVE TISSUE GROWTH FACTOR; HEPATOCYTE GROWTH FACTOR; INSULIN-SECRETING CELLS; MICE; REGENERATION;

EID: 84962013306     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-1195     Document Type: Article

References (51)

1. Stolovich-Rain M, Hija A, Grimsby J, Glaser B, Dor Y. Pancreatic beta cells in very old mice retain capacity for compensatory proliferation. J Biol Chem 2012; 287: 27407-27414
2. Rankin MM, Kushner JA. Adaptive beta-cell proliferation is severely restricted with advanced age. Diabetes 2009;58: 1365-1372
3. Chen H, Gu X, Liu Y, et al. PDGF signalling controls age-dependent proliferation in pancreatic β-cells. Nature 2011;478: 349-355
4. Teta M, Long SY, Wartschow LM, Rankin MM, Kushner JA. Very slow turnover of beta-cells in aged adult mice. Diabetes 2005;54: 2557-2567
5. Krishnamurthy J, Ramsey MR, Ligon KL, et al. p16INK4a induces an agedependent decline in islet regenerative potential. Nature 2006;443: 453-457
6. Migliorini A, Bader E, Lickert H. Islet cell plasticity and regeneration. Mol Metab 2014;3: 268-274
7. Katsube K, Sakamoto K, Tamamura Y, Yamaguchi A. Role of CCN, a vertebrate specific gene family, in development. Dev Growth Differ 2009;51: 55-67
8. de Winter P, Leoni P, Abraham D. Connective tissue growth factor: Structure-function relationships of a mosaic, multifunctional protein. Growth Factors 2008;26: 80-91
9. Nguyen TQ, Roestenberg P, van Nieuwenhoven FA, et al. CTGF inhibits BMP-7 signaling in diabetic nephropathy. J Am Soc Nephrol 2008;19: 2098-2107
10. Mercurio S, Latinkic B, Itasaki N, Krumlauf R, Smith JC. Connective-tissue growth factor modulates WNT signalling and interacts with the WNT receptor complex. Development 2004;131: 2137-2147
11. Lau LF, Lam SC. The CCN family of angiogenic regulators: The integrin connection. Exp Cell Res 1999;248: 44-57
12. Charrier A, Brigstock DR. Regulation of pancreatic function by connective tissue growth factor (CTGF, CCN2). Cytokine Growth Factor Rev 2013;24: 59-68
13. Crawford LA, Guney MA, Oh YA, et al. Connective tissue growth factor (CTGF) inactivation leads to defects in islet cell lineage allocation and beta-cell proliferation during embryogenesis. Mol Endocrinol 2009;23: 324-336
14. Guney MA, Petersen CP, Boustani A, et al. Connective tissue growth factor acts within both endothelial cells and beta cells to promote proliferation of developing beta cells. Proc Natl Acad Sci USA 2011;108: 15242-15247
15. Gunasekaran U, Hudgens CW, Wright BT, Maulis MF, Gannon M. Differential regulation of embryonic and adult β cell replication. Cell Cycle 2012;11: 2431-2442
16. Milo-Landesman D, Surana M, Berkovich I, et al. Correction of hyperglycemia in diabetic mice transplanted with reversibly immortalized pancreatic beta cells controlled by the tet-on regulatory system. Cell Transplant 2001;10: 645-650
17. 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
18. Henley KD, Gooding KA, Economides AN, Gannon M. Inactivation of the dual Bmp/Wnt inhibitor Sostdc1 enhances pancreatic islet function. Am J Physiol Endocrinol Metab 2012;303: E752-E761
19. Golson ML, Maulis MF, Dunn JC, et al. Activated FoxM1 attenuates streptozotocin-mediated β-cell death. Mol Endocrinol 2014;28: 1435-1447
20. Teta M, Rankin MM, Long SY, Stein GM, Kushner JA. Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev Cell 2007; 12: 817-826
21. Golson ML, Bush WS, Brissova M. Automated quantification of pancreatic β-cell mass. Am J Physiol Endocrinol Metab 2014;306: E1460-E1467
22. 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
23. Mosser RE, Gannon M. An assay for small scale screening of candidate β cell proliferative factors using intact islets. Biotechniques 2013;55: 310-312
24. di Mola FF, Friess H, Martignoni ME, et al. Connective tissue growth factor is a regulator for fibrosis in human chronic pancreatitis. Ann Surg 1999;230: 63-71
25. Criscimanna A, Speicher JA, Houshmand G, et al. Duct cells contribute to regeneration of endocrine and acinar cells following pancreatic damage in adult mice. Gastroenterology 2011; 141: 1451-1462
26. Lammert E, Gu G, McLaughlin M, et al. Role of VEGF-A in vascularization of pancreatic islets. Curr Biol 2003;13: 1070-1074
27. Alvarez-Perez JC, Ernst S, Demirci C, et al. Hepatocyte growth factor/c-Met signaling is required for β-cell regeneration. Diabetes 2014;63: 216-223
28. Brigstock DR. Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis 2002;5: 153-165
29. Wakae-Takada N, Xuan S, Watanabe K, Meda P, Leibel RL. Molecular basis for the regulation of islet beta cell mass in mice: The role of E-cadherin. Diabetologia 2013;56: 856-866
30. Guo S, Dai C, Guo M, et al. Inactivation of specific β cell transcription factors in type 2 diabetes. J Clin Invest 2013;123: 3305-3316
31. Weinberg N, Ouziel-Yahalom L, Knoller S, Efrat S, Dor Y. Lineage tracing evidence for in vitro dedifferentiation but rare proliferation of mouse pancreatic beta-cells. Diabetes 2007;56: 1299-1304
32. Talchai C, Xuan S, Lin HV, Sussel L, Accili D. Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure. Cell 2012;150: 1223-1234
33. Artner I, Hang Y, Mazur M, et al. MafA and MafB regulate genes critical to beta-cells in a unique temporal manner. Diabetes 2010;59: 2530-2539
34. Nishimura W, Kondo T, Salameh T, et al. A switch from MafB to MafA expression accompanies differentiation to pancreatic beta-cells. Dev Biol 2006; 293: 526-539
35. Zhang H, Ackermann AM, Gusarova GA, et al. The FoxM1 transcription factor is required to maintain pancreatic beta-cell mass. Mol Endocrinol 2006;20: 1853-1866
36. Ackermann AM, Gannon M. Molecular regulation of pancreatic beta-cell mass development, maintenance, and expansion. J Mol Endocrinol 2007;38: 193-206
37. Zhang H, Zhang J, Pope CF, et al. Gestational diabetes mellitus resulting from impaired beta-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen. Diabetes 2010;59: 143-152
38. Golson ML, Misfeldt AA, Kopsombut UG, Petersen CP, Gannon M. High Fat Diet Regulation of β-Cell Proliferation and β-Cell Mass. Open Endocrinol J 2010;4: 66-77
39. Arnott JA, Nuglozeh E, Rico MC, et al. Connective tissue growth factor (CTGF/CCN2) is a downstream mediator for TGF-beta1-induced extracellular matrix production in osteoblasts. J Cell Physiol 2007;210: 843-852
40. Leask A, Holmes A, Black CM, Abraham DJ. Connective tissue growth factor gene regulation. Requirements for its induction by transforming growth factorbeta 2 in fibroblasts. J Biol Chem 2003;278: 13008-13015
41. Phanish MK, Wahab NA, Hendry BM, Dockrell ME. TGF-beta1-induced connective tissue growth factor (CCN2) expression in human renal proximal tubule epithelial cells requires Ras/MEK/ERK and Smad signalling. Nephron, Exp Nephrol 2005;100: E156-e165
42. Pannu J, Nakerakanti S, Smith E, ten Dijke P, Trojanowska M. Transforming growth factor-beta receptor type I-dependent fibrogenic gene program is mediated via activation of Smad1 and ERK1/2 pathways. J Biol Chem 2007;282: 10405-10413
43. Ren W, Sun X, Wang K, et al. BMP9 inhibits the bone metastasis of breast cancer cells by downregulating CCN2 (connective tissue growth factor, CTGF) expression. Mol Biol Rep 2014;41: 1373-1383
44. Saleem S, Li J, Yee SP, Fellows GF, Goodyer CG, Wang R. beta1 integrin/ FAK/ERK signalling pathway is essential for human fetal islet cell differentiation and survival. J Pathol 2009;219: 182-192
45. Diaferia GR, Jimenez-Caliani AJ, Ranjitkar P, et al. b1 integrin is a crucial regulator of pancreatic β-cell expansion. Development 2013;140: 3360-3372
46. Terauchi Y, Takamoto I, Kubota N, et al. Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat diet-induced insulin resistance. J Clin Invest 2007;117: 246-257
47. Luo Q, Kang Q, Si W, et al. Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J Biol Chem 2004;279: 55958-55968
48. El-Gohary Y, Tulachan S, Wiersch J, et al. A smad signaling network regulates islet cell proliferation. Diabetes 2014;63: 224-236
49. Liu Z, Habener JF. Glucagon-like peptide-1 activation of TCF7L2-dependent Wnt signaling enhances pancreatic beta cell proliferation. J Biol Chem 2008;283: 8723-8735
50. Kim H, Toyofuku Y, Lynn FC, et al. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 2010;16: 804-808
51. Ohara-Imaizumi M, Kim H, Yoshida M, et al. Serotonin regulates glucosestimulated insulin secretion from pancreatic β cells during pregnancy. Proc Natl Acad Sci USA 2013;110: 19420-19425