Connective tissue growth factor (CTGF) inactivation leads to defects in islet cell lineage allocation and β-cell proliferation during embryogenesis

Molecular Endocrinology

Volumn 23, Issue 3, 2009, Pages 324-336

  Crawford, Laura A ^a   Guney, Michelle A ^a   Oh, Young Ah ^a   Deyoung, R Andrea ^b   Valenzuela, David M ^d   Murphy, Andrew J ^d   Yancopoulos, George D ^d   Lyons, Karen M ^b   Brigstock, David R ^c   Economides, Aris ^b,d   Gannon, Maureen ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; BETA GALACTOSIDASE; BONE MORPHOGENETIC PROTEIN; CONNECTIVE TISSUE GROWTH FACTOR; GLUCAGON; INSULIN; PROTEIN P27; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; CTGF GENE; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE EXPRESSION; GENE INACTIVATION; HETEROZYGOTE; MORPHOGENESIS; MOUSE; NONHUMAN; ORGANOGENESIS; PANCREAS DEVELOPMENT; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

ANIMALS; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; CELL SIZE; CELLS, CULTURED; CONNECTIVE TISSUE GROWTH FACTOR; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; GLUCAGON; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

EID: 61449178818     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2008-0045     Document Type: Article

References (66)

1. Meissner HP 1976 Electrophysiological evidence for coupling between β cells of pancreatic islets. Nature 262:502-504
2. Bennett MV, Goodenough DA 1978 Gap junctions, electrotonic coupling, and intercellular communication. Neurosci Res Program Bull 16:1-486
3. Halban PA, Wollheim CB, Blondel B, Meda P, Niesor EN, Mintz DH 1982 The possible importance of contact between pancreatic islet cells for the control of insulin release. Endocrinology 111:86-94
4. Samols E, Stagner JI, Ewart RB, Marks V 1988 The order of islet microvascular cellular perfusion is B-A-D in the perfused rat pancreas. J Clin Invest 82:350-353
5. Bosco D, Orci L, Meda P 1989 Homologous but not heterologous contact increases the insulin secretion of individual pancreatic β-cells. Exp Cell Res 184:72-80
6. Pictet RL, Clark WR, Williams RH, Rutter WJ 1972 An ultrastructural analysis of the developing embryonic pancreas. Dev Biol 29:436-467
7. Teitelman G, Lee J, Reis DJ 1987 Differentiation of prospective mouse pancreatic islet cells during development in vitro and during regeneration. Dev Biol 120:425-433
8. Bonner-Weir S, Baxter LA, Schuppin GT, Smith FE 1993 A second pathway for regeneration of adult exocrine and endocrine pancreas. A possible recapitulation of embryonic development. Diabetes 42:1715-1720
9. Gu D, Sarvetnick N 1993 Epithelial cell proliferation and islet neogenesis in IEN-γ transgenic mice. Development 118:33-46
10. Miralles F, Battelino T, Czernichow P, Scharfmann R 1998 TGF-βj plays a key role in morphogenesis of the pancreatic islets of Langerhans by controlling the activity of the matrix metalloproteinase MMP-2. J Cell Biol 143:827-836
11. Cirulli V, Beattie GM, Klier G, Ellisman M, Ricordi C, Quaranta V, Frasier F, Ishii JK, Hayek A, Salomon DR 2000 Expression and function of α(v) β(3) and α(v) β(5) integrins in the developing pancreas: roles in the adhesion and migration of putative endocrine progenitor cells. J Cell Biol 150:1445-1460
12. Gu G, Brown JR, Melton DA 2003 Direct lineage tracing reveals the ontogeny of pancreatic cell fates during mouse embryogenesis. Mech Dev 120:35-43
13. Chang C, Holtzman DA, Chau S, Chickering T, Woolf EA, Holmgren LM, Bodorova J, Gearing DP, Holmes WE, Brivanlou AH 2001 Twisted gastrulation can function as a BMP antagonist. Nature 410:483-487
14. Oelgeschlager M, Larrain J, Geissert D, De Robertis EM 2000 The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling. Nature 405:757-763
15. Hunt LT, Barker WC 1987 von Willebrand factor shares a distinctive cysteine-rich domain with thrombospondin and procollagen. Biochem Biophys Res Commun 144:876-882
16. Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, De Robertis EM 1994 Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79:779-790
17. Abreu JG, Ketpura NI, Reversade B, De Robertis EM 2002 Connective-tissue growth factor(CTGE) modulatescell signalling by BMP and TGE-β. Nat Cell Biol 4:599-604
18. Adams JC 2001 Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol 17:25-51
19. Rothberg JM, Jacobs JR, Goodman CS, Artavanis-Tsakonas S 1990 slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGE and LRR domains. Genes Dev 4:2169-2187
20. Brose K, Tessier-Lavigne M 2000 Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr Opin Neurobiol 10:95-102
21. Moussad EE, Brigstock DR 2000 Connective tissue growth factor: what's in a name? Mol Genet Metab 71:276-292
22. Kireeva ML, Latinkic BV, Kolesnikova TV, Chen CC, Yang GP, Abler AS, Lau LF 1997 Cyr61 and Eisp12 are both ECM-associated signaling molecules: activities, metabolism, and localization during development. Exp Cell Res 233:63-77
23. Igarashi A, Okochi H, Bradham DM, Grotendorst GR 1993 Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol Biol Cell 4:637-645
24. Blom IE, Goldschmeding R, Leask A 2002 Gene regulation of connective tissue growth factor: new targets for antifibrotic therapy? Matrix Biol 21:473-482
25. Mercurio S, Latinkic B, Itasaki N, Krumlauf R, Smith JC 2004 Connectivetissue growth factor modulates WNT signalling and interacts with the WNT receptor complex. Development 131:2137-2147
26. Babic AM, Chen CC, Lau LF 1999 Fisp12/mouse connective tissue growth factor mediates endothelial cell adhesion and migration through integrin αvβ3, promotes endothelial cell survival, and induces angiogenesis in vivo. Mol Cell Biol 19:2958-2966
27. Chen CC, Chen N, Lau LF 2001 The angiogenic factors Cyr61 and connective tissue growth factor induce adhesive signaling in primary human skin fibroblasts. J Biol Chem 276:10443-10452
28. Fan WH, Karnovsky MJ 2002 Increased MMP-2 expression in connective tissue growth factor over-expression vascular smooth muscle cells. J Biol Chem 277:9800-9805
29. di Mola FF, Friess H, Martignoni ME, Di Sebastiano P, Zimmermann A, Innocenti P, Graber H, Gold LI, Korc M, Buchler MW 1999 Connective tissue growth factor is a regulator for fibrosis in human chronic pancreatitis. Ann Surg 230:63-71
30. Dornhofer N, Spong S, Bennewith K, Salim A, Klaus S, Kambham N, Wong C, Kaper F, Sutphin P, Nacalumi R, Hockel M, Le Q, Longaker M, Yang G, Koong A, Giaccia A 2006 Connective tissue growth factor-specific monoclonal antibody therapy inhibits pancreatic tumor growth and metastasis. Cancer Res 66:5816-5827
31. Ivkovic S, Yoon BS, Popoff SN, Safadi FF, Libuda DE, Stephenson RC, Daluiski A, Lyons KM 2003 Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 130:2779-2791
32. Wilding Crawford L, Tweedie Ables E, Oh YA, Boone B, Levy S, Gannon M 2008 Gene expression profiling of a mouse model of pancreatic islet dysmor- phogenesis. PLoS One 3:e1611
33. Gu G, Dubauskaite J, Melton DA 2002 Direct evidence for the pancreatic lineage: NGN3 + cells are islet progenitors and are distinct from duct progenitors. Development 129:2447-2457
34. Gannon M, Tweedie Ables E, Crawford L, Lowe D, Offield MF, Magnuson MA, Wright CV 2008 pdx-1 function is specifically required in embryonic β cells to generate appropriate numbers of endocrine cell types and maintain glucose homeostasis. Dev Biol 314:406-417
35. Rhodes CJ 2005 Type 2 diabetes-a matter of β-cell life and death? Science 307:380-384
36. Uchida T, Nakamura T, Hashimoto N, Matsuda T, Kotani K, Sakaue H, Kido Y, Hayashi Y, Nakayama KI, White MF, Kasuga M 2005 Deletion of Cdkn 1b ameliorates hyperglycemia by maintaining compensatory hyperinsulinemia in diabetic mice. Nat Med 11:175-182
37. Wu SH, Wu XH, Lu C, Dong L, Chen ZQ 2006 Lipoxin A4 inhibits proliferation of human lung fibroblasts induced by connective tissue growth factor. Am J Respir Cell Mol Biol 34:65-72
38. Zhang H, Ackermann AM, Gusarova GA, Lowe D, Feng X, Kopsombut UG, Costa RH, Gannon M 2006 The Eoxm1 transcription factor is required to maintain pancreatic β cell mass. Mol Endocrinol 20:1853-1866
39. Wenger C, Ellenrieder V, Alber B, Lacher U, Menke A, Hameister H, Wilda M, Iwamura T, Beger HG, Adler G, Gress TM 1999 Expression and differential regulation of connective tissue growth factor in pancreatic cancer cells. Oncogene 18:1073-1080
40. Gannon M, Ray MK, Van Zee K, Rausa F, Costa RH, Wright CV 2000 Persistent expression of HNE6 in islet endocrine cells causes disrupted islet architecture and loss of β cell function. Development 127:2883-2895
41. Tweedie E, Artner I, Crawford L, Poffenberger G, Thorens B, Stein R, Powers AC, Gannon M 2006 Maintenance of hepatic nuclear factor 6 in postnatal islets impairs terminal differentiation and function of β-cells. Diabetes 55: 3264-3270
42. Kapasa M, Serafimidis I, Gavalas A, Kossida S 2008 Identification of phylogenetically conserved enhancer elements implicated in pancreas development in the WISP1 and CTGF orthologs. Genomics 92:301-308
43. Murtaugh L, Melton DA 2003 Genes, signals, and lineages in pancreas development. Annu Rev Cell Dev Biol 19:71-89
44. Lammert E, Cleaver O, Melton D 2001 Induction of pancreatic differentiation by signals from blood vessels. Science 294:564-567
45. Cleaver O, Melton DA 2003 Endothelial signaling during development. Nat Med 9:661-668
46. Smart NG, Apelqvist AA, Gu X, Harmon EB, Topper JN, MacDonald RJ, Kim SK 2006 Conditional expression of Smad7 in pancreatic β cells disrupts TGF-β signaling and induces reversible diabetes mellitus. PLoS Biol 4:e39
47. Nakanishi T, Nishida T, Shimo T, Kobayashi K, Kubo T, Tamatani T, Tezuka K, Takigawa M 2000 Effects of CTGF/Hcs24, a product of a hypertrophic chondrocyte-specific gene, on the proliferation and differentiation of chondrocytes in culture. Endocrinology 141:264-273
48. Safadi FF, Xu J, Smock SL, Kanaan RA, Selim AH, Odgren PR, Marks Jr SC, Owen TA, Popoff SN 2003 Expression of connective tissue growth factor in bone: its role in osteoblast proliferation and differentiation in vitro and bone formation in vivo. J Cell Physiol 196:51-62
49. Pi L, Oh SH, Shupe T, Petersen BE 2005 Role of connective tissue growth factor in oval cell response during liver regeneration after 2-AAF/PHx in rats. Gastroenterology 128:2077-2088
50. Asano M, Kubota S, Nakanishi T, Nishida T, Yamaai T, Yosimichi G, Ohyama K, Sugimoto T, Murayama Y, Takigawa M 2005 Effect of connective tissue growth factor (CCN2/CTGF) on proliferation and differentiation of mouse periodontal ligament-derived cells. Cell Commun Signal 3:11
51. Dor Y, Brown J, Martinez OI, Melton DA 2004 Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429:41-46
52. Teta M, Long SY, Wartschow LM, Rankin MM, Kushner JA 2005 Very slow turnover of β-cells in aged adult mice. Diabetes 54:2557-2567
53. Ackermann AM, Gannon M 2007 Molecular regulation of pancreatic β-cell mass development, maintenance, and expansion. J Mol Endocrinol 38:193-206
54. Jiang Y, Nishimura W, Devor-Henneman D, Kusewitt D, Wang H, Holloway MP, Dohi T, Sabo E, Robinson ML, Altieri DC, Sharma A, Altura RA 2008 Postnatal expansion of the pancreatic β-cell mass is dependent on survivin. Diabetes 57:2718-2727
55. Zhang FD, Li Y, Iida K, McGrath B, Cavener DR 2006 PERK EIF2AK3 control of pancreatic β cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab 4:491-497
56. Valenzuela DM, Murphy AJ, Frendewey D, Gale NW, Economides AN, Auerbach W, Poueymirou WT, Adams NC, Rojas J, Yasenchak J, Chernomorsky R, Boucher M, Elsasser AL, Esau L, Zheng J, Griffiths JA, Wang X, Su H, Xue Y, Dominguez MG, Noguera I, Torres R, Macdonald LE, Stewart AF, DeChiara TM, Yancopoulos GD 2003 High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat Biotechnol 21:652-659
57. Yang XW, Model P, Heintz N 1997 Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat Biotechnol 15:859-865
58. Zhang Y, Buchholz F, Muyrers JP, Stewart AF 1998 A new logic for DNA engineering using recombination in Escherichia coli. Nat Genet 20:123-128
59. Liu YT, Chao DC, Lee F, Chen CG, Ji DD 1998 Molecular characterization of Gluconobacter oxydans recA gene and its inhibitory effect on the function of the host wild-type recA gene. Can J Microbiol 44:149-156
60. Narayanan K, Williamson R, Zhang Y, Stewart AF, Ioannou PA 1999 Efficient and precise engineering of a 200 kb β-globin human/bacterial artificial chromosome in E. coli DH10B using an inducible homologous recombination system. Gene Ther 6:442-447
61. Sauer B, Henderson N 1988 Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc Natl Acad Sci USA 85:5166-5170
62. Wu KL, Gannon M, Peshavaria M, Offield MF, Henderson E, Ray M, Marks A, Gamer LW, Wright CV, Stein R 1997 Hepatocyte nuclear factor 3β is involved in pancreatic β-cell-specific transcription of the pdx-1 gene. Mol Cell Biol 17:6002-6013
63. Steffen CL, Ball-Mirth DK, Harding PA, Bhattacharyya N, Pillai S, Brigstock DR 1998 Characterization of cell-associated and soluble forms of connective tissue growth factor (CTGF) produced by fibroblast cells in vitro. Growth Factors 15:199-213
64. Brissova M, Shiota M, Nicholson WE, Gannon M, Knobel SM, Piston DW, Wright CV, Powers AC 2002 Reduction in pancreatic transcription factor PDX-1 impairs glucose-stimulated insulin secretion. J Biol Chem 277:11225-11232
65. Thimmappaya B, Zain BS, Dhar R, Weissman SM 1978 Nucleotide sequence of DNA template for the 3′ ends of SV40 mRNA. II. The sequence of the DNA fragment EcorII-F and a part of EcorII-H. J Biol Chem 253:1613-1618
66. Adra CN, Boer PH, McBurney MW 1987 Cloning and expression of the mouse pgk-1 gene and the nucleotide sequence of its promoter. Gene 60:65-74