Sox9-haploinsufficiency causes glucose intolerance in mice

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Dubois, Claire L ^a   Shih, Hung Ping ^a   Seymour, Philip A ^a   Patel, Nisha A ^a   Behrmann, James M ^a   Ngo, Victoria ^a   Sander, Maike ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HEPATOCYTE NUCLEAR FACTOR 3BETA; HEPATOCYTE NUCLEAR FACTOR 6; INSULIN; PROTEIN TCF2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEIN; NERVE PROTEIN; NEUROG3 PROTEIN, MOUSE; PANCREATIC AND DUODENAL HOMEOBOX 1 PROTEIN; PRIMER DNA; SOX9 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENZYME INACTIVATION; GENE DOSAGE; GENE REGULATORY NETWORK; GENETIC MODEL; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; HAPLOINSUFFICIENCY; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS CELL; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; STEM CELL; TRANSCRIPTION REGULATION; ANIMAL; C57BL MOUSE; FAT INTAKE; GENETICS; GLUCOSE TOLERANCE TEST; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

MUS;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; DIETARY FATS; DNA PRIMERS; GLUCOSE TOLERANCE TEST; HAPLOINSUFFICIENCY; HOMEODOMAIN PROTEINS; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; POLYMERASE CHAIN REACTION; SOX9 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS;

EID: 79960982596     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023131     Document Type: Article

References (47)

1. 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.
2. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, et al. (2002) The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 32: 128-134.
3. Kopp JL, Dubois CL, Schaffer AE, Hao E, Shih HP, et al. (2011) Sox9+ ductal cells are multipotent progenitors throughout development but do not produce new endocrine cells in the normal or injured adult pancreas. Development 138: 653-665.
4. Solar M, Cardalda C, Houbracken I, Martin M, Maestro MA, et al. (2009) Pancreatic exocrine duct cells give rise to insulin-producing beta cells during embryogenesis but not after birth. Dev Cell 17: 849-860.
5. 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: 1607-1611.
6. Hani EH, Stoffers DA, Chèvre JC, Durand E, Stanojevic V, et al. (1999) Defective mutations in the insulin promoter factor-1 (IPF-1) gene in late-onset type 2 diabetes mellitus. J Clin Invest 104: R41-48.
7. Stoffers DA, Ferrer J, Clarke WL, Habener JF, (1997) Early-onset type-II diabetes mellitus (MODY4) linked to IPF1. Nat Genet 17: 138-139.
8. Stoffers DA, Zinkin NT, Stanojevic V, Clarke WL, Habener JF, (1997) Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet 15: 106-110.
9. Ahlgren U, Jonsson J, Jonsson L, Simu K, Edlund H, (1998) beta-cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the beta-cell phenotype and maturity onset diabetes. Genes & Development 12: 1763-1768.
10. Gittes GK, (2009) Developmental biology of the pancreas: a comprehensive review. Dev Biol 326: 4-35.
11. Ohlsson H, Karlsson K, Edlund T, (1993) IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J 12: 4251-4259.
12. Oliver-Krasinski JM, Kasner MT, Yang J, Crutchlow MF, Rustgi AK, et al. (2009) The diabetes gene Pdx1 regulates the transcriptional network of pancreatic endocrine progenitor cells in mice. J Clin Invest 119: 1888-1898.
13. Seymour PA, Freude KK, Tran MN, Mayes EE, Jensen J, et al. (2007) SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc Natl Acad Sci USA 104: 1865-1870.
14. Seymour PA, Freude KK, Dubois CL, Shih HP, Patel NA, et al. (2008) A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev Biol 323: 19-30.
15. Lynn FC, Smith SB, Wilson ME, Yang KY, Nekrep N, et al. (2007) Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc Natl Acad Sci USA 104: 10500-10505.
16. Yamagata K, Oda N, Kaisaki PJ, Menzel S, Furuta H, et al. (1996) Mutations in the hepatocyte nuclear factor-1alpha gene in maturity-onset diabetes of the young (MODY3). Nature 384: 455-458.
17. Pontoglio M, Sreenan S, Roe M, Pugh W, Ostrega D, et al. (1998) Defective insulin secretion in hepatocyte nuclear factor 1alpha-deficient mice. J Clin Invest 101: 2215-2222.
18. Bali D, Svetlanov A, Lee HW, Fusco-DeMane D, Leiser M, et al. (1995) Animal model for maturity-onset diabetes of the young generated by disruption of the mouse glucokinase gene. J Biol Chem 270: 21464-21467.
19. Maestro MA, Boj SF, Luco RF, Pierreux CE, Cabedo J, et al. (2003) Hnf6 and Tcf2 (MODY5) are linked in a gene network operating in a precursor cell domain of the embryonic pancreas. Hum Mol Genet 12: 3307-3314.
20. Badea TC, Wang Y, Nathans J, (2003) A noninvasive genetic/pharmacologic strategy for visualizing cell morphology and clonal relationships in the mouse. J Neurosci 23: 2314-2322.
21. Robinson SP, Langan-Fahey SM, Johnson DA, Jordan VC, (1991) Metabolites, pharmacodynamics, and pharmacokinetics of tamoxifen in rats and mice compared to the breast cancer patient. Drug Metab Dispos 19: 36-43.
22. Hayashi S, McMahon AP, (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
23. Nyqvist D, Mattsson G, Köhler M, Lev-Ram V, Andersson A, et al. (2005) Pancreatic islet function in a transgenic mouse expressing fluorescent protein. J Endocrinol 186: 333-341.
24. Gu C, Stein GH, Pan N, Goebbels S, Hornberg H, et al. (2010) Pancreatic beta cells require NeuroD to achieve and maintain functional maturity. Cell Metab 11: 298-310.
25. Kilic G, Wang J, Sosa-Pineda B, (2006) Osteopontin is a novel marker of pancreatic ductal tissues and of undifferentiated pancreatic precursors in mice. Dev Dyn 235: 1659-1667.
26. Guz Y, Montminy MR, Stein R, Leonard J, Gamer LW, et al. (1995) 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.
27. Stoffers DA, Thomas MK, Habener JF, (1997) Homeodomain protein IDX-1: a master regulator of pancreas development and insulin gene expression. Trends Endocrinol Metab 8: 145-151.
28. Lee J-Y, Ristow M, Lin X, White MF, Magnuson MA, et al. (2006) RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function. J Biol Chem 281: 2649-2653.
29. Trudeau JD, Dutz JP, Arany E, Hill DJ, Fieldus WE, et al. (2000) Neonatal beta-cell apoptosis: a trigger for autoimmune diabetes? Diabetes 49: 1-7.
30. Scaglia L, Cahill CJ, Finegood DT, Bonner-Weir S, (1997) Apoptosis participates in the remodeling of the endocrine pancreas in the neonatal rat. Endocrinology 138: 1736-1741.
31. Pan FC, Wright C, (2011) Pancreas organogenesis: from bud to plexus to gland. Dev Dyn 240: 530-565.
32. Gerrish K, Gannon M, Shih D, Henderson E, Stoffel M, et al. (2000) Pancreatic beta cell-specific transcription of the pdx-1 gene. The role of conserved upstream control regions and their hepatic nuclear factor 3beta sites. J Biol Chem 275: 3485-3492.
33. Jacquemin P, Lemaigre FP, Rousseau GG, (2003) The Onecut transcription factor HNF-6 (OC-1) is required for timely specification of the pancreas and acts upstream of Pdx-1 in the specification cascade. Dev Biol 258: 105-116.
34. Jacquemin P, Durviaux SM, Jensen J, Godfraind C, Gradwohl G, et al. (2000) Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Molecular and Cellular Biology 20: 4445-4454.
35. Haumaitre C, Barbacci E, Jenny M, Ott MO, Gradwohl G, et al. (2005) Lack of TCF2/vHNF1 in mice leads to pancreas agenesis. Proc Natl Acad Sci USA 102: 1490-1495.
36. Wang S, Yan J, Anderson DA, Xu Y, Kanal MC, et al. (2010) Neurog3 gene dosage regulates allocation of endocrine and exocrine cell fates in the developing mouse pancreas. Dev Biol 339: 26-37.
37. Piper K, Ball SG, Keeling JW, Mansoor S, Wilson DI, et al. (2002) Novel SOX9 expression during human pancreas development correlates to abnormalities in Campomelic dysplasia. Mech Dev 116: 223-226.
38. Bagheri-Fam S, Barrionuevo F, Dohrmann U, Günther T, Schüle R, et al. (2006) Long-range upstream and downstream enhancers control distinct subsets of the complex spatiotemporal Sox9 expression pattern. Dev Biol 291: 382-397.
39. Brissova M, Shiota M, Nicholson WE, Gannon M, Knobel SM, et al. (2002) Reduction in pancreatic transcription factor PDX-1 impairs glucose-stimulated insulin secretion. J Biol Chem 277: 11225-11232.
40. García-Herrero CM, Galán M, Vincent O, Flández B, Gargallo M, et al. (2007) Functional analysis of human glucokinase gene mutations causing MODY2: exploring the regulatory mechanisms of glucokinase activity. Diabetologia 50: 325-333.
41. Edghill EL, Bingham C, Slingerland AS, Minton JAL, Noordam C, et al. (2006) Hepatocyte nuclear factor-1 beta mutations cause neonatal diabetes and intrauterine growth retardation: support for a critical role of HNF-1beta in human pancreatic development. Diabet Med 23: 1301-1306.
42. Mayer C, Böttcher Y, Kovacs P, Halbritter J, Stumvoll M, (2008) Phenotype of a patient with a de novo mutation in the hepatocyte nuclear factor 1beta/maturity-onset diabetes of the young type 5 gene. Metab Clin Exp 57: 416-420.
43. Haumaitre C, Fabre M, Cormier S, Baumann C, Delezoide A-L, et al. (2006) Severe pancreas hypoplasia and multicystic renal dysplasia in two human fetuses carrying novel HNF1beta/MODY5 mutations. Hum Mol Genet 15: 2363-2375.
44. Barbacci E, Chalkiadaki A, Masdeu C, Haumaitre C, Lokmane L, et al. (2004) HNF1beta/TCF2 mutations impair transactivation potential through altered co-regulator recruitment. Hum Mol Genet 13: 3139-3149.
45. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, et al. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52: 102-110.
46. Manolio TA, (2009) Collaborative genome-wide association studies of diverse diseases: programs of the NHGRI's office of population genomics. Pharmacogenomics 10: 235-241.
47. Gao N, Lelay J, Vatamaniuk MZ, Rieck S, Friedman JR, et al. (2008) Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development. Genes & Development 22: 3435-3448.