Deletion of retinoic acid receptor β (RARβ) impairs pancreatic endocrine differentiation

Experimental Cell Research

Volumn 319, Issue 14, 2013, Pages 2196-2204

  Pérez, Ronald J ^a   Benoit, Yannick D ^a   Gudas, Lorraine J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Endocrine; Islet cells; Pancreas; RAR ; Retinoic acid; Stem cell

Indexed keywords

ACTIVIN A; CYTOCHROME P450 26A1; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; NEUROGENIN 3; NICOTINAMIDE; RETINOIC ACID RECEPTOR BETA; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; EMBRYONIC STEM CELL; GENE DELETION; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; MOUSE; NONHUMAN; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STABLE EXPRESSION;

EID: 84880738579     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.05.032     Document Type: Article

References (60)

1. Guariguata L., Whiting D., Weil C., Unwin N. The International Diabetes Federation diabetes atlas methodology for estimating global and national prevalence of diabetes in adults. Diabetes Res. Clin. Pract. 2011, 94:322-332.
2. Whiting D.R., Guariguata L., Weil C., Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res. Clin. Pract. 2011, 94:311-321.
3. Huang E.S., Basu A., O'Grady M., Capretta J.C. Projecting the future diabetes population size and related costs for the U.S. Diabetes Care 2009, 32:2225-2229.
4. Oliver-Krasinski J.M., Stoffers D.A. On the origin of the beta cell. Genes Dev. 2008, 22:1998-2021.
5. Waldron-Lynch F., Herold K.C. Immunomodulatory therapy to preserve pancreatic beta-cell function in type 1 diabetes. Nat. Rev. Drug Discov. 2011, 10:439-452.
6. Waldron-Lynch F., von Herrath M., Herold K.C. Towards a curative therapy in type 1 diabetes: remission of autoimmunity, maintenance and augmentation of beta cell mass. Novartis Found. Symp. 2008, 292:146-155. (discussion 155-148, 202-143).
7. Charbonnel B., Penfornis A., Varroud-Vial M., Kusnik-Joinville O., Detournay B. Insulin therapy for diabetes mellitus: treatment regimens and associated costs. Diabetes Metab. 2011.
8. Zaret K.S., Grompe M. Generation and regeneration of cells of the liver and pancreas. Science 2008, 322:1490-1494.
9. Weir G.C., Cavelti-Weder C., Bonner-Weir S. Stem cell approaches for diabetes: towards beta cell replacement. Genome Med. 2011, 3:61.
10. Sui J., Mehta M., Shi B., Morahan G., Jiang F.X. Directed differentiation of embryonic stem cells allows exploration of novel transcription factor genes for pancreas development. Stem Cell Rev. 2012, 1:1-10.
11. Ben-Yehudah A., White C., Navara C.S., Castro C.A., Ize-Ludlow D., Shaffer B., Sukhwani M., Mathews C.E., Chaillet J.R., Witchel S.F. Evaluating protocols for embryonic stem cell differentiation into insulin-secreting beta-cells using insulin II-GFP as a specific and noninvasive reporter. Cloning Stem Cells 2009, 11:245-257.
12. Blyszczuk P., Czyz J., Kania G., Wagner M., Roll U., St-Onge L., Wobus A.M. Expression of Pax4 in embryonic stem cells promotes differentiation of nestin-positive progenitor and insulin-producing cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:998-1003.
13. Borowiak M., Maehr R., Chen S., Chen A.E., Tang W., Fox J.L., Schreiber S.L., Melton D.A. Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 2009, 4:348-358.
14. D'Amour K.A., Bang A.G., Eliazer S., Kelly O.G., Agulnick A.D., Smart N.G., Moorman M.A., Kroon E., Carpenter M.K., Baetge E.E. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 2006, 24:1392-1401.
15. Kroon E., Martinson L.A., Kadoya K., Bang A.G., Kelly O.G., Eliazer S., Young H., Richardson M., Smart N.G., Cunningham J., Agulnick A.D., D'Amour K.A., Carpenter M.K., Baetge E.E. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 2008, 26:443-452.
16. Micallef S.J., Janes M.E., Knezevic K., Davis R.P., Elefanty A.G., Stanley E.G. Retinoic acid induces Pdx1-positive endoderm in differentiating mouse embryonic stem cells. Diabetes 2005, 54:301-305.
17. Mongan N.P., Gudas L.J. Diverse actions of retinoid receptors in cancer prevention and treatment. Differentiation 2007, 75:853-870.
18. Niederreither K., Dollé P. Retinoic acid in development: towards an integrated view. Nat. Rev. Genet. 2008, 9:541-553.
19. Boylan J.F., Lohnes D., Taneja R., Chambon P., Gudas L.J. Loss of retinoic acid receptor gamma function in F9 cells by gene disruption results in aberrant Hoxa-1 expression and differentiation upon retinoic acid treatment. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:9601-9605.
20. Means A.L., Gudas L.J. The roles of retinoids in vertebrate development. Annu. Rev. Biochem. 1995, 64:201-233.
21. Kashyap V., Gudas L.J., Brenet F., Funk P., Viale A., Scandura J.M. Epigenomic reorganization of the clustered Hox genes in embryonic stem cells induced by retinoic acid. J. Biol. Chem. 2011, 286:3250-3260.
22. Chen Y., Pan F.C., Brandes N., Afelik S., Solter M., Pieler T. Retinoic acid signaling is essential for pancreas development and promotes endocrine at the expense of exocrine cell differentiation in Xenopus. Dev. Biol. 2004, 271:144-160.
23. Ostrom M., Loffler K.A., Edfalk S., Selander L., Dahl U., Ricordi C., Jeon J., Correa-Medina M., Diez J., Edlund H. Retinoic acid promotes the generation of pancreatic endocrine progenitor cells and their further differentiation into beta-cells. PLoS One 2008, 3:e2841.
24. Matthews K.A., Rhoten W.B., Driscoll H.K., Chertow B.S. Vitamin A deficiency impairs fetal islet development and causes subsequent glucose intolerance in adult rats. J. Nutr. 2004, 134:1958-1963.
25. Chertow B.S., Blaner W.S., Baranetsky N.G., Sivitz W.I., Cordle M.B., Thompson D., Meda P. Effects of vitamin A deficiency and repletion on rat insulin secretion in vivo and in vitro from isolated islets. J. Clin. Invest. 1987, 79:163-169.
26. Dolle P., Ruberte E., Leroy P., Morriss-Kay G., Chambon P. Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 1990, 110:1133-1151.
27. Ghyselinck N.B., Dupé V., Dierich A., Messaddeq N., Garnier J.M., Rochette-Egly C., Chambon P., Mark M. Role of the retinoic acid receptor beta (RARbeta) during mouse development. Int. J. Dev. Biol. 1997, 41:425-447.
28. Ueki T., Toyota M., Sohn T., Yeo C.J., Issa J.P., Hruban R.H., Goggins M. Hypermethylation of multiple genes in pancreatic adenocarcinoma. Cancer Res. 2000, 60:1835-1839.
29. Martinez-Ceballos E., Chambon P., Gudas L.J. Differences in gene expression between wild type and Hoxa1 knockout embryonic stem cells after retinoic acid treatment or leukemia inhibitory factor (LIF) removal. J. Biol. Chem. 2005, 280:16484-16498.
30. Laursen K.B., Wong P.M., Gudas L.J. Epigenetic regulation by RARalpha maintains ligand-independent transcriptional activity. Nucleic Acids Res. 2012, 40:102-115.
31. Benoit Y.D., Lussier C., Ducharme P.A., Sivret S., Schnapp L.M., Basora N., Beaulieu J.F. Integrin alpha8beta1 regulates adhesion, migration and proliferation of human intestinal crypt cells via a predominant RhoA/ROCK-dependent mechanism. Biol. Cell 2009, 101:695-708.
32. Spokoini R., Kfir-Erenfeld S., Yefenof E., Sionov R.V. Glycogen synthase kinase-3 plays a central role in mediating glucocorticoid-induced apoptosis. Mol. Endocrinol. 2010, 24:1136-1150.
33. Yamaguchi T.P., Takada S., Yoshikawa Y., Wu N., McMahon A.P. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 1999, 13:3185-3190.
34. Otonkoski T., Beattie G.M., Mally M.I., Ricordi C., Hayek A. Nicotinamide is a potent inducer of endocrine differentiation in cultured human fetal pancreatic cells. J. Clin. Invest. 1993, 92:1459-1466.
35. Lumelsky N., Blondel O., Laeng P., Velasco I., Ravin R., McKay R. Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 2001, 292:1389-1394.
36. Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003, 113:643-655.
37. Hosler B.A., LaRosa G.J., Grippo J.F., Gudas L.J. Expression of REX-1, a gene containing zinc finger motifs, is rapidly reduced by retinoic acid in F9 teratocarcinoma cells. Mol. Cell. Biol. 1989, 9:5623-5629.
38. Marchand M., Schroeder I.S., Markossian S., Skoudy A., Negre D., Cosset F.L., Real P., Kaiser C., Wobus A.M., Savatier P. Mouse ES cells over-expressing the transcription factor NeuroD1 show increased differentiation towards endocrine lineages and insulin-expressing cells. Int. J. Dev. Biol. 2009, 53:569-578.
39. Langton S., Gudas L.J. CYP26A1 knockout embryonic stem cells exhibit reduced differentiation and growth arrest in response to retinoic acid. Dev. Biol. 2008, 315:331-354.
40. Bernardo A.S., Hay C.W., Docherty K. Pancreatic transcription factors and their role in the birth, life and survival of the pancreatic beta cell. Mol. Cell Endocrinol. 2008, 294:1-9.
41. Kashyap V., Rezende N.C., Scotland K.B., Shaffer S.M., Persson J.L., Gudas L.J., Mongan N.P. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev. 2009, 18:1093-1108.
42. Rukstalis J.M., Habener J.F. Neurogenin3: a master regulator of pancreatic islet differentiation and regeneration. Islets 2009, 1:177-184.
43. Soria B. In-vitro differentiation of pancreatic beta-cells. Differentiation 2001, 68:205-219.
44. Van Hoof D., D'Amour K.A., German M.S. Derivation of insulin-producing cells from human embryonic stem cells. Stem Cell Res. 2009, 3:73-87.
45. Gosmain Y., Katz L.S., Masson M.H., Cheyssac C., Poisson C., Philippe J. Pax6 is crucial for beta-cell function, insulin biosynthesis, and glucose-induced insulin secretion. Mol. Endocrinol. 2012, 26:696-709.
46. Ahlgren U., Pfaff S.L., Jessell T.M., Edlund T., Edlund H. Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 1997, 385:257-260.
47. Naujok O., Francini F., Picton S., Bailey C.J., Lenzen S., Jorns A. Changes in gene expression and morphology of mouse embryonic stem cells on differentiation into insulin-producing cells in vitro and in vivo. Diabetes Metab. Res. Rev. 2009, 25:464-476.
48. Gasa R., Mrejen C., Leachman N., Otten M., Barnes M., Wang J., Chakrabarti S., Mirmira R., German M. Proendocrine genes coordinate the pancreatic islet differentiation program in vitro. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13245-13250.
49. Cai J., Yu C., Liu Y., Chen S., Guo Y., Yong J., Lu W., Ding M., Deng H. Generation of homogeneous PDX1(+) pancreatic progenitors from human ES cell-derived endoderm cells. J. Mol. Cell. Biol. 2010, 2:50-60.
50. Jonsson J., Carlsson L., Edlund T., Edlund H. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 1994, 371:606-609.
51. Fujimoto K., Polonsky K.S. Pdx1 and other factors that regulate pancreatic beta-cell survival. Diabetes Obes. Metab. 2009, 11(Suppl. 4):30-37.
52. Dalgin G., Ward A.B., Hao le T., Beattie C.E., Nechiporuk A., Prince V.E. Zebrafish mnx1 controls cell fate choice in the developing endocrine pancreas. Development 2011, 138:4597-4608.
53. Vetere A., Marsich E., Di Piazza M., Koncan R., Micali F., Paoletti S. Neurogenin3 triggers beta-cell differentiation of retinoic acid-derived endoderm cells. Biochem. J. 2003, 371:831-841.
54. Dohrmann C., Gruss P., Lemaire L. Pax genes and the differentiation of hormone-producing endocrine cells in the pancreas. Mech. Dev. 2000, 92:47-54.
55. Chen C., Zhang Y., Sheng X., Huang C., Zang Y.Q. Differentiation of embryonic stem cells towards pancreatic progenitor cells and their transplantation into streptozotocin-induced diabetic mice. Cell. Biol. Int. 2008, 32:456-461.
56. Sirchia S.M., Ren M., Pili R., Sironi E., Somenzi G., Ghidoni R., Toma S., Nicolo G., Sacchi N. Endogenous reactivation of the RARbeta2 tumor suppressor gene epigenetically silenced in breast cancer. Cancer Res. 2002, 62:2455-2461.
57. Youssef E.M., Estecio M.R., Issa J.P. Methylation and regulation of expression of different retinoic acid receptor beta isoforms in human colon cancer. Cancer Biol. Ther. 2004, 3:82-86.
58. House M.G., Herman J.G., Guo M.Z., Hooker C.M., Schulick R.D., Lillemoe K.D., Cameron J.L., Hruban R.H., Maitra A., Yeo C.J. Aberrant hypermethylation of tumor suppressor genes in pancreatic endocrine neoplasms. Ann. Surg. 2003, 238:423-431. (discussion 431-422).
59. Sato N., Fukushima N., Hruban R.H., Goggins M. CpG island methylation profile of pancreatic intraepithelial neoplasia. Mod. Pathol. 2008, 21:238-244.
60. Volkmar M., Dedeurwaerder S., Cunha D.A., Ndlovu M.N., Defrance M., Deplus R., Calonne E., Volkmar U., Igoillo-Esteve M., Naamane N., Del Guerra S., Masini M., Bugliani M., Marchetti P., Cnop M., Eizirik D.L., Fuks F. DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from type 2 diabetic patients. EMBO J. 2012, 31:1405-1426.