The diabetes-linked transcription factor PAX4 promotes β-cell proliferation and survival in rat and human islets

Journal of Cell Biology

Volumn 167, Issue 6, 2004, Pages 1123-1135

  Brun, Thierry ^a   Franklin, Isobel ^a   St Onge, Luc ^b,d   Biason Lauber, Anna ^c   Schoenle, Eugene J ^c   Wollheim, Claes B ^a   Gauthier, Benoit R ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b DeveloGen AG   (Germany)

^c UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^d NeuroNova AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; ADENOSINE TRIPHOSPHATE; BETACELLULIN; CALCIUM; GLUCOSE; INHIBITOR OF APOPTOSIS PROTEIN; INHIBITOR OF DIFFERENTIATION 2; INSULIN; MESSENGER RNA; MITOGENIC AGENT; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL XL; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX4; UNCLASSIFIED DRUG; WORTMANNIN;

ADENOVIRUS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DIABETES MELLITUS; GENE INDUCTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INSULIN RELEASE; MASS; MITOCHONDRION; MUTANT; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; RAT; SIGNAL TRANSDUCTION; TRANSACTIVATION;

ACTIVINS; ADENOVIRIDAE; ANIMALS; BCL-X PROTEIN; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DIABETES MELLITUS; GENES, MYC; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INHIBIN-BETA SUBUNITS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISLETS OF LANGERHANS; PAIRED BOX TRANSCRIPTION FACTORS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ADENOVIRIDAE; ANIMALIA;

EID: 11244311918     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200405148     Document Type: Article

References (51)

1. Baumann Kubetzko, F.B., C. Di Paolo, C. Maag, R. Meier, B.W. Schafer, D.R. Betts, R.A. Stahel, and A. Himmelmann. 2004. The PAX5 oncogene is expressed in N-type neuroblastoma cells and increases tumorigenicity of a S-type cell line. Carcinogenesis. 25:1839-1846.
2. Bonner-Weir, S. 2000. Life and death of the pancreatic beta cells. Trends Endocrinol. Metab. 11:375-378.
3. Buteau, J., S. Foisy, C.J. Rhodes, L. Carpenter, T.J. Biden, and M. Prentki. 2001. Protein kinase Czeta activation mediates glucagon-like peptide-1-induced pancreatic beta-cell proliferation. Diabetes. 50:2237-2243.
4. Buteau, J., S. Foisy, E. Joly, and M. Prentki. 2003. Glucagon-like peptide I induces pancreatic beta-cell proliferation via transactivation of the epidermal growth factor receptor. Diabetes. 52:124-132.
5. Campbell, S.C., H. Cragg, L.J. Elrick. W.M. Macfarlan, K.I. Shennan, and K. Docherty. 1999. Inhibitory effect of Pax4 on the human insulin and islet amyloid polypeptide (IAPP) promoters. FEBS Lett. 463:53-57.
6. Challet, C., P. Maechler, C.B. Wollheim, and U.T. Ruegg. 2001. Mitochondrial calcium oscillations in C2C12 myotubes. J. Biol. Chem. 276:3791-3797.
7. Cheung, W.C., J.S. Kim, M. Linden, L. Peng, B. Van Ness, R.D. Polakiewicz, and S. Janz. 2004. Novel targeted deregulation of c-Myc cooperates with Bcl-X(L) to cause plasina cell neoplasms in mice. J. Clin. Invest. 113:1763-1773.
8. Collins, C.L., B.P. Bode, W.W. Souba, and S.F. Abcouwer. 1998. Multiwell 14CO2-capture assay for evaluation of substrate oxidation rates of cells in culture. Biotechniques. 24:803-808.
9. Demeterco, C., G.M. Beattie, S.A. Dib, A.D. Lopez, and A. Hayek, 2000. A role for activin A and betacellulin in human fetal pancreatic cell differentiation and growth. J. Clin. Endocrinol. Metab. 85:3892-3896.
10. Detimary, P., J.C. Jonas, and J.C. Henquin. 1995. Possible links between glucose-induced changes in the energy state of pancreatic B cells and insulin release. Unmasking by decreasing a stable pool of adenine nucleotides in mouse islets. J. Clin. Invest. 96:1738-1745.
11. Dor, Y., J. Brown, O.I. Martinez, and D.A. Melton. 2004. Adult pancreatic beta-cells are formed by self-duplication rather than stein-cell differentiation. Nature. 429:41-46.
12. -/- mice. J. Clin. Invest. 113:1288-1295.
13. Finegood, D.T., M.D. McArthur, D. Kojwang, M.J. Thomas, B.G. Topp, T. Leonard, and R.E. Buckingham. 2001. Beta-cell mass dynamics in Zucker diabetic fatty rats. Rosiglitazone prevents the rise in net cell death. Diabetes. 50:1021-1029.
14. Garcia-Ocana, A., R.C. Vasavada, K.K. Takane, A. Cebrian, J.C. Lopez-Talavera, and A.F. Stewart. 2001. Using beta-cell growth factors to enhance human pancreatic Islet transplantation. J. Clin. Endocrinol. Metab. 86:984-988.
15. Gauthier, B., M. Robb, F. Gaudet, G.S. Ginsburg, and R. McPherson. 1999a. Characterization of a cholesterol response element (CRE) in the promoter of the cholesteryl ester transfer protein gene: functional role of the transcription factors SREBP-1a, -2, and YY1. J. Lipid Res. 40:1284-1293.
16. Gauthier, B., M. Robb, and R. McPherson. 1999b. Cholesteryl ester transfer protein gene expression during differentiation of human preadipocytes to adipocytes in primary culture. Atherosclerosis. 142:301-307.
17. Gauthier, B.R., V.M. Schwitzgebel, M. Zaiko, A. Mamin, B. Ritz-Laser, and J. Philippe. 2002. Hepatic nuclear factor-3 (HNF-3 or Foxa2) regulates glucagon gene transcription by binding to the G1 and G2 promoter elements. Mol. Endocrinol. 16:170-183.
18. Gauthier, B.R., T. Brun, E.J. Sarret, H. Ishihara, O. Schaad, P. Descombes, and C.B. Wollheim. 2004. Oligonucleotide microarray analysis reveals PDX1 as an essential regulator of mitochondrial metabolism in rat islets. J. Biol. Chem. 279:31121-31130.
19. Gittes, G.K., and W.J. Rutter. 1992. Onset of cell-specific gene expression in the developing mouse pancreas. Proc. Natl. Acad. Sci. USA. 89:1128-1132.
20. Heremans, Y., M. Van De Casteele, P. in't Veld, G. Gradwohl, P. Serup, O. Madsen, D. Pipeleers, and H. Heimberg. 2002. Recapitulation of embryonic neuroendocrine differentiation in adult human pancreatic duct cells expressing neurogenin 3. J. Cell Biol. 159:303-312.
21. Holm, P., B. Rydlander, H. Luthman, and I. Kockum. 2004. Interaction and association analysis of a type I diabetes susceptibility locus on chromosome 5q11-q13 and the 7q32 chromosomal region in Scandinavian families. Diabetes. 53:1584-1591.
22. Ishihara, H., H. Wang, L.R. Drewes, and C.B. Wollheim. 1999. Overexpression of monocarboxylate transporter and lactate dehydrogenase alters insulin secretory responses to pyruvate and lactate in beta cells. J. Clin. Invest. 104:1621-1629.
23. Ishihara, H., P. Maechler, A. Gjinovci, P.L. Herrera, and C.B. Wollheim. 2003. Islet beta-cell secretion determines glucagon release from neighbouring alpha-cells. Nat. Cell Biol. 5:330-335.
24. Jonas. E.A., D. Hoit, J.A. Hickman, T.A. Brandt, B.M. Polster, Y. Fannjiang, E. McCarthy. M.K. Montanez, J.M. Hardwick, and L.K. Kaczmarek. 2003. Modulation of synaptic transmission by the BCL-2 family protein BCL-xL. J. Neurosci. 23:8423-8431.
25. Kanatsuka, A., Y. Tokuyama, O. Nozaki, K. Matsui, and T. Egashira. 2002. Beta-cell dysfunction in late-onset diabetic subjects carrying homozygous mutation in transcription factors NeuroD1 and Pax4. Metabolism. 51:1161-1165.
26. 2+ in aequorin-expressing INS-1 cells. J. Clin. Invest. 98:2524-2538.
27. Kojima, H., M. Fujimiya, K. Matsumura, P. Younan, H. Imaeda, M. Maeda, and L. Chan. 2003. NeuroD-betacellulin gene therapy induces islet neogenesis in the liver and reverses diabetes in mice. Nat. Med. 9:596-603.
28. Koski, C.L., S. Hila, and G.E. Hoffman. 2004. Regulation of cytokine-induced neuron death by ovarian hormones: involvement of antiapoptotic protein expression and c-JUN N-terminal kinase-mediated proapoptotic signaling. Endocrinology. 145:95-103.
29. Lasorella, A., M. Noseda, M. Beyna, Y. Yokota, and A. Iavarone. 2000. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature. 407:592-598.
30. Laybutt, D.R., H. Kaneto, W. Hasenkamp, S. Grey, J.C. Jonas, D.C. Sgroi, A. Groff, C. Ferran, S. Bonner-Weir, A. Sharma, and G.C. Weir. 2002. Increased expression of antioxidant and antiapoptotic genes in islets that may contribute to beta-cell survival during chronic hyperglycemia. Diabetes. 51:413-423.
31. Liu, Y.Q., J.A. Moibi, and J.L. Leahy. 2004. Chronic high glucose lowers pyruvate dehydrogenase activity in islets through enhanced production of long chain acyl-CoA: prevention of impaired glucose oxidation by enhanced pyruvate recycling through the malate-pyruvate shuttle. J. Biol. Chem. 279:7470-7475.
32. Maechler, P., and C.B. Wollheim. 2001. Mitochondrial function in normal and diabetic beta-cells. Nature. 414:807-812.
33. Margue, C.M., M. Bemasconi, F.G. Barr, and B.W. Schafer. 2000. Transcriptional modulation of the anti-apoptotic protein BCL-XL by the paired box transcription factors PAX3 and PAX3/FKHR. Oncogene. 19:2921-2929.
34. Miyamoto, T., T. Kakizawa, K. Ichikawa, S. Nishio, S. Kajikawa, and K. Hashizume. 2001. Expression of dominant negative form of PAX4 in human insulinoma. Biochem. Biophys. Res. Commun. 282:34-40.
35. Muratovska, A., C. Zhou, S. He, P. Goodyer, and M.R. Eccles. 2003. Paired-Box genes are frequently expressed in cancer and often required for cancer cell survival. Oncogene. 22:7989-7997.
36. Nielsen, J.H., E.D. Galsgaard, A. Moldrup, B.N. Friedrichsen, N. Billestrup, J.A. Hansen, Y.C. Lee, and C. Carlsson. 2001. Regulation of beta-cell mass by hormones and growth factors. Diabetes. 50:S25-S29.
37. Parker, C.J., S.G. Shawcross, H. Li, Q.Y. Wang, C.S. Herrington, S. Kumar, R.M. MacKie, W. Prime, I.G. Rennie, K. Sisley, and P. Kumar. 2004. Expression of PAX 3 alternatively spliced transcripts and identification of two new isoforms in human tumors of neural crest origin. Int. J. Cancer. 108:314-320.
38. Pelengaris, S., M. Khan, and G. Evan. 2002. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell. 109:321-334.
39. Ritz-Laser, B., A. Estreicher, B. Gauthier, A. Mamin, H. Edlund, and J. Philippe. 2002. The pancreatic b-cell-specific transcription factor Pax-4 inhibits glucagon gene expression through Pax-6. Diabetologia. 45:97-107.
40. Salehi, A., D. Chen, R. Hakanson, G. Nordin, and I. Lundquist. 1999. Gastrectomy induces impaired insulin and glucagon secretion: evidence for a gastro-insular axis in mice. J. Physiol. 514:579-591.
41. Schaniel, C., M. Gottar, E. Roosnek, F. Melchers, and A.G. Rolink. 2002. Extensive in vivo self-renewal, long-term reconstitution capacity, and hematopoietic multipotency of Pax5-deficient precursor B-cell clones. Blood. 99:2760-2766.
42. Scharfmann, R., A. Basmaciogullari, and P. Czemichow. 1990. Effect of growth hormone and glucose on rat islet cells replication using 5-bromo-2-deoxyuridine incorporation. Diabetes Res. 15:137-141.
43. Shimajiri, Y., T. Sanke, H. Furuta, T. Hanabusa, T. Nakagawa, Y. Fujitani, Y. Kajimoto, N. Takasu, and K. Nanjo. 2001. A missense mutation of Pax4 gene (R121W) is associated with type 2 diabetes in Japanese. Diabetes. 50:2864-2869.
44. Shimajiri, Y., M. Shimabukuro, T. Tomoyose, H. Yogi, I. Komiya, and N. Takasu. 2003. PAX4 mutation (R121W) as a prodiabetic variant in Okinawans. Biochem. Biophys. Res. Commun. 302:342-344.
45. Sosa-Pineda, B., K. Chowdhury, M. Torres, G. Oliver, and P. Gruss. 1997. The Pax4 gene is essential for differentiation of insulin-producing beta cells in the mammalian pancreas. Nature. 386:399-402.
46. Theis, M., C. Mas, B. Doring, J. Degen, C. Brink, D. Caille, A. Charollais, O. Kruger, A. Plum, V. Nepote, et al. 2004. Replacement by a lacZ reporter gene assigns mouse connexin36, 45 and 43 to distinct cell types in pancreatic islets. Exp. Cell Res. 294:18-29.
47. Ueda, Y. 2000. Activin A increases Pax4 gene expression in pancreatic beta cell lines. FEBS Lett. 480:101-105.
48. Wollheim, C.B., and P. Maechler. 2002. Beta-cell mitochondria and insulin secretion: messenger role of nucleotides and metabolites. Diabetes. 51 Suppl 1:S37-S42.
49. Yamamura, T., H. Otani, Y. Nakao, R. Hattori, M. Osako, and H. Imamura. 2001. IGF-I differentially regulates Bcl-xL and Bax and confers myocardial protection in the rat heart. Am. J. Physiol. Heart Circ. Physiol. 280:H1191-H1200.
50. Zalzman, M., S. Gupta, R.K. Giri, I. Berkovich, B.S. Sappal, O. Kamieli, M.A. Zem, N. Fleischer, and S. Efrat. 2003. Reversal of hyperglycemia in mice by using human expandable insulin-producing cells differentiated from fetal liver progenitor cells. Proc. Natl. Acad. Sci. USA. 100:2426-2431.
51. Zhou, Y.P., J.C. Pena, M.W. Roe, A. Mittal, M. Levisetti, A.C. Baldwin, W. Pugh, D. Ostrega, N. Ahmed, V.P. Bindokas, et al. 2000. Overexpression of Bcl-x(L) in beta-cells prevents cell death but impairs mitochondrial signal for insulin secretion. Am. J. Physiol. Endocrinol. Metab. 278:E340-E351.