SOX4 cooperates with neurogenin 3 to regulate endocrine pancreas formation in mouse models

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• 作者：Eric E. Xu (1) (2)
  Nicole A. J. Krentz (1) (2)
  Sara Tan (1)
  Sam Z. Chow (1)
  Mei Tang (1) (2)
  Cuilan Nian (1) (2)
  Francis C. Lynn (1) (2) (3)
  
  1. Diabetes Research Program ; Child and Family Research Institute ; A4-184 ; 950 West 28 Ave ; Vancouver ; BC ; V5Z 4H4 ; Canada
  2. Department of Surgery ; University of British Columbia ; Vancouver ; BC ; Canada
  3. Department of Cellular and Physiological Sciences ; University of British Columbia ; Vancouver ; BC ; Canada
  
• 关键词：Basic science ; Cell lines ; Human ; Islet development ; Islet transplantation ; Islets ; Knockout mice ; Transcription factors
• 刊名：Diabetologia
• 出版年：2015
• 出版时间：May 2015
• 年：2015
• 卷：58
• 期：5
• 页码：1013-1023
• 全文大小：1,808 KB
• 参考文献：1. Seymour, PA, Freude, KK, Tran, MN (2007) SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc Natl Acad Sci U S A 104: pp. 1865-1870 CrossRef
  2. Kawaguchi, Y, Cooper, B, Gannon, M (2002) The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 32: pp. 128-134 CrossRef
  3. Jonsson, J, Carlsson, L, Edlund, T, Edlund, H (1994) Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371: pp. 606-609 CrossRef
  4. Lammert, E, Cleaver, O, Melton, D (2001) Induction of pancreatic differentiation by signals from blood vessels. Science 294: pp. 564-567 CrossRef
  5. Kim, SK, Melton, DA (1998) Pancreas development is promoted by cyclopamine, a hedgehog signaling inhibitor. Proc Natl Acad Sci U S A 95: pp. 13036-13041 CrossRef
  6. Deutsch, G, Jung, J, Zheng, M (2001) A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 128: pp. 871-881
  7. Hebrok, M, Kim, SK, St Jacques, B (2000) Regulation of pancreas development by hedgehog signaling. Development 127: pp. 4905-4913
  8. Kim, SK, Hebrok, M, Li, E (2000) Activin receptor patterning of foregut organogenesis. Genes Dev 14: pp. 1866-1871
  9. Pictet, RL, Clark, WR, Williams, RH, Rutter, WJ (1972) An ultrastructural analysis of the developing embryonic pancreas. Dev Biol 29: pp. 436-467 CrossRef
  10. Shih, HP, Wang, A, Sander, M (2013) Pancreas organogenesis: from lineage determination to morphogenesis. Annu Rev Cell Dev Biol 29: pp. 81-105 CrossRef
  11. Gouzi, M, Kim, YH, Katsumoto, K (2011) Neurogenin3 initiates stepwise delamination of differentiating endocrine cells during pancreas development. Dev Dyn 240: pp. 589-604 CrossRef
  12. Gradwohl, G, Dierich, A, LeMeur, M, Guillemot, F (2000) Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci U S A 97: pp. 1607-1611 CrossRef
  13. Zhou, Q, Law, AC, Rajagopal, J (2007) A multipotent progenitor domain guides pancreatic organogenesis. Dev Cell 13: pp. 103-114 CrossRef
  14. Kopp, JL, Dubois, CL, Hao, E (2011) Progenitor cell domains in the developing and adult pancreas. Cell Cycle 10: pp. 1921-1927 CrossRef
  15. Jensen, J, Pedersen, EE, Galante, P (2000) Control of endodermal endocrine development by Hes-1. Nat Genet 24: pp. 36-44 CrossRef
  16. Murtaugh, LC, Stanger, BZ, Kwan, KM, Melton, DA (2003) Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci U S A 100: pp. 14920-14925 CrossRef
  17. 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: pp. 2447-2457
  18. Miyatsuka, T, Li, Z, German, MS (2009) Chronology of islet differentiation revealed by temporal cell labeling. Diabetes 58: pp. 1863-1868 CrossRef
  19. Ahlgren, U, Pfaff, SL, Jessell, TM (1997) Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 385: pp. 257-260 CrossRef
  20. Naya, FJ, Huang, HP, Qiu, Y (1997) Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroD-deficient mice. Genes Dev 11: pp. 2323-2334 CrossRef
  21. Sander, M, Neub眉ser, A, Kalamaras, J (1997) Genetic analysis reveals that PAX6 is required for normal transcription of pancreatic hormone genes and islet development. Genes Dev 11: pp. 1662-1673 CrossRef
  22. Smith, SB, Qu, H-Q, Taleb, N (2010) Rfx6 directs islet formation and insulin production in mice and humans. Nature 463: pp. 775-780 CrossRef
  23. Sussel, L, Kalamaras, J, Hartigan-O鈥機onnor, DJ (1998) Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 125: pp. 2213-2221
  24. Sosa-Pineda, B, Chowdhury, K, Torres, M (1997) The Pax4 gene is essential for differentiation of insulin-producing beta cells in the mammalian pancreas. Nature 386: pp. 399-402 CrossRef
  25. Matsuoka, T, Zhao, L, Artner, I (2003) Members of the large Maf transcription family regulate insulin gene transcription in islet beta cells. Mol Cell Biol 23: pp. 6049-6062 CrossRef
  26. Wegner, M (2010) All purpose Sox: the many roles of Sox proteins in gene expression. Int J Biochem Cell Biol 42: pp. 381-390 CrossRef
  27. Kamachi, Y, Kondoh, H (2013) Sox proteins: regulators of cell fate specification and differentiation. Development 140: pp. 4129-4144 CrossRef
  28. Lioubinski, O, M眉ller, M, Wegner, M, Sander, M (2003) Expression of Sox transcription factors in the developing mouse pancreas. Dev Dyn 227: pp. 402-408 CrossRef
  29. Mavropoulos, A, Devos, N, Biemar, F (2005) Sox4b is a key player of pancreatic alpha cell differentiation in zebrafish. Dev Biol 285: pp. 211-223 CrossRef
  30. McDonald, E, Li, J, Krishnamurthy, M (2012) SOX9 regulates endocrine cell differentiation during human fetal pancreas development. Int J Biochem Cell Biol 44: pp. 72-83 CrossRef
  31. Wilson, ME, Yang, KY, Kalousova, A (2005) The HMG box transcription factor Sox4 contributes to the development of the endocrine pancreas. Diabetes 54: pp. 3402-3409 CrossRef
  32. Muzumdar, MD, Tasic, B, Miyamichi, K (2007) A global double-fluorescent Cre reporter mouse. Genesis 45: pp. 593-605 CrossRef
  33. Schonhoff, SE, Giel-Moloney, M, Leiter, AB (2004) Neurogenin 3-expressing progenitor cells in the gastrointestinal tract differentiate into both endocrine and non-endocrine cell types. Dev Biol 270: pp. 443-454 CrossRef
  34. Penzo-M茅ndez A, Dy P, Pallavi B, Lefebvre V (2007) Generation of mice harboring a Sox4 conditional null allele. 780:776鈥?80
  35. Sabatini, PV, Krentz, NAJ, Zarrouki, B (2013) Npas4 is a novel activity-regulated cytoprotective factor in pancreatic 尾-cells. Diabetes 62: pp. 2808-2820 CrossRef
  36. Carpenter, AE, Jones, TR, Lamprecht, MR (2006) Cell profiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7: pp. R100 CrossRef
  37. Luo, J, Deng, Z-L, Luo, X (2007) A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2: pp. 1236-1247 CrossRef
  38. Seymour, PA, Freude, KK, Dubois, CL (2008) A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev Biol 323: pp. 19-30 CrossRef
  39. Schaffer, AE, Freude, KK, Nelson, SB, Sander, M (2010) Nkx6 transcription factors and Ptf1a function as antagonistic lineage determinants in multipotent pancreatic progenitors. Dev Cell 18: pp. 1022-1029 CrossRef
  40. Yoshida, T, Hanahan, D (1994) Murine pancreatic ductal adenocarcinoma produced by in vitro transduction of polyoma middle T oncogene into the islets of Langerhans. Am J Pathol 145: pp. 671-684
  41. Gasa, R, Mrejen, C, Leachman, N (2004) Proendocrine genes coordinate the pancreatic islet differentiation program in vitro. Proc Natl Acad Sci U S A 101: pp. 13245-13250 CrossRef
  42. Lynn, FC, Smith, SB, Wilson, ME (2007) Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc Natl Acad Sci U S A 104: pp. 10500-10505 CrossRef
  43. Lee, JC, Smith, SB, Watada, H (2001) Regulation of the pancreatic pro-endocrine gene neurogenin3. Diabetes 50: pp. 928-936 CrossRef
  44. Rukstalis, JM, Habener, JF (2009) Neurogenin3: a master regulator of pancreatic islet differentiation and regeneration. Islets 1: pp. 177-184 CrossRef
  45. Bhattaram, P, Penzo-M茅ndez, A, Sock, E (2010) Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat Commun 1: pp. 9 CrossRef
  46. Talchai, C, Xuan, S, Kitamura, T (2012) Generation of functional insulin-producing cells in the gut by Foxo1 ablation. Nat Genet 44: pp. 406-412 CrossRef
  47. Anderson, KR, Torres, CA, Solomon, K (2009) Cooperative transcriptional regulation of the essential pancreatic islet gene NeuroD1 (beta2) by Nkx2.2 and neurogenin 3. J Biol Chem 284: pp. 31236-31248 CrossRef
  48. Xiao, X, Chen, Z, Shiota, C (2013) No evidence for 尾 cell neogenesis in murine adult pancreas. J Clin Invest 123: pp. 2207-2217 CrossRef
  49. Boyer, LA, Lee, TI, Cole, MF (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: pp. 947-956 CrossRef
  50. Aksoy, I, Jauch, R, Chen, J (2013) Oct4 switches partnering from Sox2 to Sox17 to reinterpret the enhancer code and specify endoderm. EMBO J 32: pp. 938-953 CrossRef
  51. Choi, E, Kraus, MRC, Lemaire, LA (2012) Dual lineage-specific expression of Sox17 during mouse embryogenesis. Stem Cells 30: pp. 2297-2308 CrossRef
  52. Lynn, FC, Skewes-Cox, P, Kosaka, Y (2007) MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes 56: pp. 2938-2945 CrossRef
  53. Goldsworthy, M, Hugill, A, Freeman, H, Horner, E (2008) Role of the transcription factor sox4 in insulin secretion and impaired glucose tolerance. Diabetes 57: pp. 2234-2244 CrossRef
  54. Apelqvist, A, Li, H, Sommer, L (1999) Notch signalling controls pancreatic cell differentiation. Nature 400: pp. 877-881 CrossRef
  55. Qu X, Afelik S, Jensen JN et al (2013) Notch-mediated post-translational control of Ngn3 protein stability regulates pancreatic patterning and cell fate commitment. Dev Biol 1鈥?2
  56. Schwitzgebel, VM, Scheel, DW, Conners, JR (2000) Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127: pp. 3533-3542
  57. Wang, S, Jensen, JN, Seymour, PA (2009) Sustained Neurog3 expression in hormone-expressing islet cells is required for endocrine maturation and function. Proc Natl Acad Sci U S A 106: pp. 9715-9720 CrossRef
  58. Lee, C, Sund, N, Vatamaniuk, M (2002) Foxa2 controls Pdx1 gene expression in pancreatic beta cells in vivo. Diabetes 51: pp. 2546-2551 CrossRef
  59. Smith, SB, Gasa, R, Watada, H (2003) Neurogenin3 and hepatic nuclear factor 1 cooperate in activating pancreatic expression of Pax4. J Biol Chem 278: pp. 38254-38259 CrossRef
  60. Prado, CL, Pugh-Bernard, AE, Elghazi, L (2004) Ghrelin cells replace insulin-producing beta cells in two mouse models of pancreas development. Proc Natl Acad Sci U S A 101: pp. 2924-2929 CrossRef
  61. Wang, Q, Elghazi, L, Martin, S (2008) Ghrelin is a novel target of Pax4 in endocrine progenitors of the pancreas and duodenum. Dev Dyn 237: pp. 51-61 CrossRef
  
• 刊物类别：Medicine
• 刊物主题：Medicine & Public Health
  Internal Medicine
  Metabolic Diseases
  Human Physiology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0428

文摘

Aims/hypothesis The sex-determining region Y (SRY)-related high mobility group (HMG) box (SOX) family of transcription factors is essential for normal organismal development. Despite the longstanding knowledge that many SOX family members are expressed during pancreas development, a role for many of these factors in the establishment of insulin-producing beta cell fate remains to be determined. The aim of this study is to elucidate the role of SOX4 during beta cell development. Methods We used pancreas and endocrine progenitor mouse knockouts of Sox4 to uncover the roles of SOX4 during pancreas development. Lineage tracing and in vitro models were used to determine how SOX4 regulates beta cell formation and understand the fate of Sox4-null endocrine lineage cells. Results This study demonstrates a progenitor cell-autonomous role for SOX4 in regulating the genesis of beta cells and shows that it is required at multiple stages of the process. SOX4 deletion in the multipotent pancreatic progenitors resulted in impaired endocrine progenitor cell differentiation. Deletion of SOX4 later in the Neurog3-expressing cells also caused reductions in beta cells. Lineage studies showed loss of Sox4 in endocrine progenitors resulted in a block in terminal islet cell differentiation that was attributed to reduction in the production of key beta cell specification factors. Conclusions/interpretation These results demonstrate that SOX4 is essential for normal endocrine pancreas development both concomitant with, and downstream of, the endocrine fate decision. In conclusion, these studies position Sox4 temporally in the endocrine differentiation programme and provide a new target for improving in vitro differentiation of glucose-responsive pancreatic beta cells.