PDX-1/VP16 fusion protein, together with neurod or Ngn3, markedly induces insulin gene transcription and ameliorates glucose tolerance

Diabetes

Volumn 54, Issue 4, 2005, Pages 1009-1022

  Kaneto, Hideaki ^a   Nakatani, Yoshihisa ^a   Miyatsuka, Takeshi ^a   Matsuoka, Taka Aki ^a   Matsuhisa, Munehide ^a   Hori, Masatsugu ^a   Yamasaki, Yoshimitsu ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CYCLOPHILIN; HELIX LOOP HELIX PROTEIN; HYBRID PROTEIN; INSULIN; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; NEUROGENIC DIFFERENTIATION FACTOR; NEUROGENIN 3; STREPTOZOCIN; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL STRAIN HEPG2; CONTROLLED STUDY; DIABETES MELLITUS; ELECTRON MICROSCOPY; ENHANCER REGION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INSULIN SYNTHESIS; MALE; MATURITY ONSET DIABETES MELLITUS; MOUSE; NONHUMAN; NORTHERN BLOTTING; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOZOCIN DIABETES; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE; WESTERN BLOTTING; WILD TYPE;

ADENOVIRIDAE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOOD GLUCOSE; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DIABETES MELLITUS, EXPERIMENTAL; HERPES SIMPLEX VIRUS PROTEIN VMW65; HOMEODOMAIN PROTEINS; INSULIN; MALE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; RECOMBINANT FUSION PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 15944417831     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.54.4.1009     Document Type: Article

References (80)

1. Ohlsson H, Karlsson K, Edlund T: IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J 12:4251-4259, 1993
2. Miller CP, McGehee RE, Habener JF: IDX-1: a new homeodomain transcription factor expressed in rat pancreatic islets and duodenum that transactivates the somatostatin gene. EMBO J 13:1145-1156, 1994
3. Leonard J, Peers B, Johnson T, Ferreri K, Lee S, Montminy MR: Characterization of somatostatin transactivating factor-1, a novel homeobox factor that stimulates somatostatin expression in pancreatic islet cells. Mol Endocrinol 7:1275-1283, 1993
4. Jonsson J, Carlsson L, Edlund T, Edlund H: Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 37:606-609, 1994
5. Guz Y, Montminy MR, Stein R, Leonard J, Gamer LW, Wright CV, Teitelman G: Expression of murine STF-1, a putative insulin gene transcription factor, in beta cells of pancreas, duodenal epithelium and pancreatic exocrine and endocrine progenitors during ontogeny. Development 121:11-18, 1995
6. Slack JMW: Developmental biology of the pancreas. Development 121: 1569-1580, 1995
7. Offield MF, Jetton TL, Labosky P, Ray M, Stein R, Magnuson M, Hogan BLM, Wright CVE: PDX-1 is required for pancreas outgrowth and differentiation of the rostral duodenum. Development 122:983-985, 1996
8. Ahlgren U, Jonsson J, Edlund H: The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 122:1409-1416, 1996
9. Stoffers DA, Zinkin NT, Stanojevic V, Clarke WL, Habener JF: Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet 15:106-110, 1997
10. Kaneto H, Miyagawa J, Kajimoto Y, Yamamoto K, Watada H, Umayahara Y, Hanafusa T, Matsuzawa Y, Yamasaki Y, Higashiyama S, Taniguchi N: Expression of heparin-binding epidermal growth factor-like growth factor during pancreas development: a potential role of PDX-1 in transcriptional activation. J Biol Chem 272:29137-29143, 1997
11. Sander M, German MS: The beta cell transcription factors and development of the pancreas. J Mol Med 75:327-340, 1997
12. Dutta S, Bonner-Weir S, Montminy M, Wright C: Regulatory factor linked to late-onset diabetes? Nature 392:560, 1998
13. Stoffers DA, Heller RS, Miller CP, Habener JF: Developmental expression of the homeodomain protein IDX-1 mice transgenic for an IDX-1 promoter/LacZ transcriptional reporter. Endocrinology 140:5374-5381, 1999
14. Holland AM, Hale MA, Kagami H, Hammer RE, MacDonald RJ: Experimental control of pancreatic development and maintenance. Proc Natl Acad Sci U S A 99:12236-12241, 2002
15. Bonner-Weir S, Taneja M, Weir GC, Tatarkiewicz K, Song K-H, Sharma A, O'Neil JJ: In vitro cultivation of human islets expanded ductal tissue. Proc Natl Acad Sci U S A 97:7999-8004, 2000
16. Ferber S, Halkin A, Cohen H, Ber I, Einav Y, Goldberg I, Barshack I, Seijffers R, Kopolovic J, Kaiser N, Karasik A: Pancreatic and duodenal homeobox gene 1 induces expression of insulin genes in liver and ameliorates streptozotocin-induced hyperglycemia. Nat Med 6:568-572, 2000
17. Kojima H, Nakamura T, Fujita Y, Kishi A, Fujimiya M, Yamada S, Kudo M, Nishio Y, Maegawa H, Haneda M, Yasuda H, Kojima I, Seno M, Wong NCW, Kikkawa R, Kashiwagi A: Combined expression of pancreatic duodenal homeobox 1 and islet factor 1 induces immature enterocytes to produce insulin. Diabetes 51:1398-1408, 2002
18. Yoshida S, Kajimoto Y, Yasuda T, Watada H, Fujitani Y, Kosaka H, Gotow T, Miyatsuka T, Umayahara Y, Yamasaki Y, Hori M: PDX-1 induces differentiation of intestinal epithelioid IEC-6 into insulin-producing cells. Diabetes 51:2505-2513, 2002
19. Ber I, Shternhall K, Perl S, Ohanuna Z, Goldberg I, Barshack I, Benvenisti-Zarum L, Meivar-Levy I, Ferber S: Functional, persistent, and extended liver to pancreas transdifferentiation. J Biol Chem 22:31950-31957, 2003
20. Noguchi H, Kaneto H, Weir GC, Bonner-Weir S: PDX-1 protein containing its own Antennapedia-like protein transduction domain can transduce pancreatic duct and islet cells. Diabetes 52:1732-1737, 2003
21. Moritoh Y, Yamato E, Yasui Y, Miyazaki S, Miyazaki J: Analysis of insulin-producing cells during in vitro differentiation from feeder-free embryonic stem cells. Diabetes 52:1163-1168, 2003
22. Taniguchi H, Yamato E, Tashiro F, Ikegami H, Ogihara T, Miyazaki J: β-Cell neogenesis induced by adenovirus-mediated gene delivery of transcription factor PDX-1 into mouse pancreas. Gene Ther 10:15-23, 2003
23. Tang D-Q, Cao L-Z, Burkhardt BR, Xia C-Q, Litherland SA, Atkinson MA, Yang L-J: In vivo and in vitro characterization of insulin-producing cells obtained from murine bone marrow. Diabetes 53:1721-1732, 2004
24. Leon-Quinto T, Jones J, Skoudy A, Burcin M, Soria B: In vitro directed differentiation of mouse embryonic stem cells into insulin-producing cells. Diabetologia 47:1442-1451, 2004
25. Miyazaki S, Yamato E, Miyazaki J: Regulated expression of pdx-1 promotes in vitro differentiation of insulin-producing cells from embryonic stem cells. Diabetes 53:1030-1037, 2004
26. Koizumi M, Doi R, Toyoda E, Tulachan SS, Kami K, Mori T, Ito D, Kawaguchi Y, Fujimoto K, Gittes GK, Imamura M: Hepatic regeneration and enforced PDX-1 expression accelerate transdifferentiation in liver. Surgery 136:449-457, 2004
27. Petersen HV, Serup P, Leonard J, Michelsen BK, Madsen OD: Transcriptional regulation of the human insulin gene is dependent on the homeodomain protein STF1/IPF1 acting through the CT boxes. Proc Natl Acad Sci U S A 91:10465-10469, 1994
28. Peers B, Leonard J, Sharma S, Teitelman G, Montminy MR: Insulin expression in pancreatic islet cells relies on cooperative interactions between the helix loop helix factor E47 and the homeobox factor STF-1. Mol Endocrinol 8:1798-1806, 1994
29. Waeber G, Thompson N, Nicod P, Bonny C: Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Mol Endocrinol 10:1327-1334, 1996
30. Watada H, Kajimoto Y, Umayahara Y, Matsuoka T, Kaneto H, Fujitani Y, Kamada T, Kawamori R, Yamasaki Y: The human glucokinase gene β-cell-type promoter: an essential role of insulin promoter factor 1 (IPF1)/PDX-1 in its activation in HIT-T15 cells. Diabetes 45:1478-1488, 1996
31. Ahlgren U, Jonsson J, Jonsson L, Simu K, Edlund H: β-Cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the β-cell phenotype and maturity onset diabetes. Genes Dev 12:1763-1768, 1998
32. Wang H, Maechler P, Ritz-Laser B, Hagenfeldt KA, Ishihara H, Philippe J, Wollheim CB: PDX1 level defines pancreatic gene expression pattern and cell lineage differentiation. J Biol Chem 276:25279-25286, 2001
33. Leibowitz G, Ferber S, Apelqvist A, Edlund H, Gross DJ, Cerasi E, Melloul D, Kaiser N: IPF1/PDX1 deficiency and β-cell dysfunction in psammomys obesus, an animal with type 2 diabetes. Diabetes 50:1799-1806, 2001
34. McKinnon CM, Docherty K: Pancreatic duodenal homeobox-1, PDX-1, a major regulator of beta cell identity and function. Diabetologia 44:1203-1214, 2001
35. Brissova M, Shiota M, Nicholson WE, Gannon M, Knobel SM, Piston DW, Wright CV, Powers AC: Reduction in pancreatic transcription factor PDX-1 impairs glucose-stimulated insulin secretion. J Biol Chem 277:11225-11232, 2002
36. Chakrabarti SK, James JC, Mirmira RG: Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic transcription factor, PDX1: importance of chromatin structure in directing promoter binding. J Biol Chem 277:13286-13293, 2002
37. Kulkarni RN, Jhala US, Winnay JN, Krajewski S, Montminy M, Kahn CR: PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J Clin Invest 114:828-836, 2004
38. Stoffers DA, Ferrer J, Clarke WL, Habener JF: Early-onset type-II diabetes mellitus (MODY4) linked to IPF1. Nat Genet 17:138-139, 1997
39. Naya FJ, Stellrecht CMM, Tsai M-J: Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev 9:1009-1019, 1995
40. Naya FJ, Huang H, Qiu Y, Mutoh H, DeMayo F, Leiter AB, Tsai M-J: Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroD-deficient mice. Genes Dev 11:2323-2334, 1997
41. Kojima H, Fujimiya M, Matsumura K, Younan P, Imaeda H, Maeda M, Chan L: NeuroD-betacellulin gene therapy induces islet neogenesis in the liver and reverses diabetes in mice. Nat Med 9:595-603, 2003
42. Sharma A, Stein R: Glucose-induced transcription of the insulin gene is mediated by factors required for β-cell-type-specific expression. Mol Cell Biol 14:871-879, 1994
43. German MS, Wang J: The insulin gene contains multiple transcriptional elements that respond to glucose. Mol Cell Biol 14:4067-4075, 1994
44. Malecki MT, Jhala US, Antonellis A, Fields L, Doris A, Orban T, Saad M, Warram JH, Montiminy M, Krolewski AS: Mutations in NeuroD1 are associated with the development of type 2 diabetes mellitus. Nat Genet 23:323-328, 1999
45. Grapin-Botton A, Majithia AR, Melton DA: Key events of pancreas formation are triggered in gut endoderm by ectopic expression of pancreatic regulatory genes. Genes Dev 15:444-454, 2001
46. Apelqvist A, Li H, Sommer L, Beatus P, Anderson DJ, Honjo T, de Angelis MH, Lendahl U, Edlund H: Notch signaling controls pancreatic cell differentiation. Nature 400:877-881, 1999
47. Schwitzgebel VM, Scheel DW, Conners JR, Kalamaras J, Lee JE, Anderson DJ, Sussel L, Johnson JD, German MS: Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127:3533-3542, 2000
48. Gradwohl G, Dierich A, LeMeur M, Guillemot F: neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci U S A 97:1607-1611, 2000
49. Gu G, Dubauskaite J, Melton DA: Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and distinct from duct progenitors. Development 129:2447-2457, 2002
50. Heremans Y, Casteele MVD, Veld P, Gradwohl G, Serup P, Madsen O, Pipeleers D, Heimberg H: Recapitulation of embryonic neuroendocrine differentiation in adult human pancreatic duct cells expressing neurogenin3. J Cell Biol 159:303-311, 2002
51. Leibiger IB, Leibiger B, Moede T, Berggren PO: Exocytosis of insulin promotes insulin gene transcription via the insulin receptor/PI-3 kinase/p70s6 kinase and CaM kinase pathways. Mol Cell 1:933-938, 1998
52. Kulkarni RN, Bruning JC, Winnay JN, Postic C, Magnuson MA, Kahn CR: Tissue-specific knockout of the insulin receptor in pancreatic β cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell 96:329-339, 1999
53. Kulkarni RN, Winnay JN, Daniels M, Bruning JC, Flier SN, Hanahan D, Kahn CR: Altered function of insulin receptor substrate-1-deficient mouse islets and cultured β-cell lines. J Clin Invest 104:R69-R75, 1999
54. Leibiger B, Leibiger IB, Moede T, Kemper S, Kulkarni RN, Kahn CR, de Vargas LM, Berggren PO: Selective insulin signaling through A and B insulin receptors regulates transcription of insulin and glucokinase genes in pancreatic beta cells. Mol Cell 7:559-570, 2001
55. Robertson RP, Zhang H-J, Pyzdrowski KL, Walseth TF: Preservation of insulin mRNA levels and insulin secretion in HIT cells by avoidance of chronic exposure to high glucose concentrations. J Clin Invest 90:320-325, 1992
56. Olson KO, Redmon JB, Towle HC, Robertson RP: Chronic exposure of HIT cells to high glucose concentrations paradoxically decreases insulin gene transcription and alters binding of insulin gene regulatory protein. J Clin Invest 92:514-519, 1993
57. Moran A, Zhang H-J, Olson LK, Harmon JS, Poitout V, Robertson RP: Differentiation of glucose toxicity from beta cell exhaustion during the evolution of defective insulin gene expression in the pancreatic islet cell line, HIT-T15. J Clin Invest 99:534-539, 1997
58. Jonas J-C, Sharma A, Hasenkamp W, Iikova H, Patane G, Laybutt R, Bonner-Weir S, Weir GC: Chronic hyperglycemia triggers loss of pancreatic β cell differentiation in an animal model of diabetes. J Biol Chem 274:14112-14121, 1999
59. Weir GC, Laybutt DR, Kaneto H, Bonner-Weir S, Sharma A: β-Cell adaptation and decompensation during the progression of diabetes. Diabetes 50:S154-S159, 2001
60. Poitout V, Robertson RP: Minireview. Secondary beta-cell failure in type 2 diabetes: a convergence of glucotoxicity and lipotoxicity. Endocrinology 143:339-342, 2002
61. Tanaka Y, Gleason CE, Tran POT, Harmon JS, Robertson RP: Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. Proc Natl Acad Sci U S A 96:10857-10862, 1999
62. Kaneto H, Kajimoto Y, Miyagawa J, Matsuoka T, Fujitani Y, Umayahara Y, Hanafusa T, Matsuzawa Y, Yamasaki Y, Hori M: Beneficial effects of antioxidants for diabetes: possible protection of pancreatic β-cells against glucose toxicity. Diabetes 48:2398-2406, 1999
63. Kaneto H, Xu G, Fujii N, Kim S, Bonner-Weir S, Weir GC: Involvement of c-Jun N-terminal kinase in oxidative stress-mediated suppression of insulin gene expression. J Biol Chem 277:30010-30018, 2002
64. Robertson RP, Harmon J, Tran PO, Tanaka Y, Takahashi H: Glucose toxicity in β-cells: type 2 diabetes, good radicals gone bad, and glutathione connection. Diabetes 52:581-587, 2003
65. Robertson RP, Harmon J, Tran PO, Poitout V: β-Cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 53:S119-S124, 2004
66. Weir GC, Bonner-Weir S: Scientific and political impediments to successful islet transplantation. Diabetes 46:1247-1256, 1997
67. Robertson RP: Islet transplantation as a treatment for diabetes: a work in progress. N Engl J Med 350:694-705, 2004
68. Kolodka TM, Finegood M, Moss L, Woo SLC: Gene therapy for diabetes mellitus in rats by hepatic expression of insulin. Proc Natl Acad Sci U S A 92:3293-3297, 1995
69. Yang L, Li S, Hatch H, Ahrens K, Cornelius JG, Petersen BE, Peck AB: In vitro trans-differentiation of adult hepatic stem cells into pancreatic endocrine hormone-producing cells. Proc Natl Acad Sci U S A 99:8078-8083, 2002
70. Zalzman M, Gupta S, Giri RK, Berkovich I, Sappal BS, Karnieli O, Zern MA, Fleischer N, Efrat S: Reversal of hyperglycemia in mice by using human expandable insulin-producing cells differentiated from fetal liver progenitor cells. Proc Natl Acad Sci U S A 100:7253-7258, 2003
71. Kojima H, Fujimiya M, Matsumura K, Nakahara T, Hara M, Chan L: Extrapancreatic insulin-producing cells in multiple organs in diabetes. Proc Natl Acad Sci U S A 101:2458-2463, 2004
72. Horb ME, Shen C-N, Tosh D, Slack JMW: Experimental conversion of liver to pancreas. Curr Biol 13:105-115, 2003
73. McLin VA, Zorn AM: Organogenesis: making pancreas from liver. Curr Biol 13:R96-R98, 2003
74. Robinson GLWG, Peshavaria M, Henderson E, Shieh S-Y, Tsai M-J, Teitelman G, Stein R: Expression of the trans-active factors that stimulate insulin control element-mediated activity appear to precede insulin gene transcription. J Biol Chem 269:2452-2460, 1994
75. He T-C, Zhou S, DaCosta LT, Yu J, Kinzler KW, Vogelstein B: A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 95:2509-2514, 1998
76. Ohneda K, Mirmira RG, Wang J, Johnson JD, German MS: The homeodomain of PDX-1 mediates multiple protein-protein interactions in the formation of a transcriptional activation complex on the insulin promoter. Mol Cell Biol 20:900-911, 2000
77. Glick E, Leshkowitz D, Walker MD: Transcription factor BETA2 acts cooperatively with E2A and PDX1 to activate the insulin gene promoter. J Biol Chem 275:2199-2204, 2000
78. Asahara H, Dutta S, Kao H-Y, Evans RM, Montminy M: Pbx-Hox heterodimers recruit coactivator-corepressor complexes in an isoform-specific manner. Mol Cell Biol 19:8219-8225, 1999
79. Dutta S, Gannon M, Peers B, Wright C, Bonner-Weir S, Montminy M: PDX: PBX complexes are required for normal proliferation of pancreatic cells during development. Proc Natl Acad Sci U S A 98:1065-1070, 2001
80. Kim SK, Selleri L, Lee JS, Zhang AY, Gu X, Jacobs Y, Cleary ML: pbx1 inactivation disrupts pancreas development and in ipf1-deficient mice promotes diabetes mellitus. Nat Genet 30:430-435, 2002