Non-neural tyrosine hydroxylase, via modulation of endocrine pancreatic precursors, is required for normal development of beta cells in the mouse pancreas

Diabetologia

Volumn 57, Issue 11, 2014, Pages 2339-2347

  Vázquez, Patricia ^a,b   Robles, Ana M ^a   de Pablo, Flora ^a,b   Hernández Sánchez, Catalina ^a,b  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Beta cells; Catecholamines; Dopamine; Glucagon; Insulin; Islet development; Neurogenin 3; Tyrosine hydroxylase

Indexed keywords

DOPAMINE; GLUCAGON; THORIUM; TYROSINE 3 MONOOXYGENASE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HES1 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN;

ADULT; ARTICLE; CELL MATURATION; CELLS; DEVELOPMENT; EXPLANT; FEMALE; HOMEOBOX; HUMAN; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MOUSE; NEURAL CREST CELL; NEUROMODULATION; PANCREAS; PANCREAS ISLET; STEM CELL; WILD TYPE; ANIMAL; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IMMUNOBLOTTING; METABOLISM; PANCREAS ISLET BETA CELL; REAL TIME POLYMERASE CHAIN REACTION; TUNEL ASSAY;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DOPAMINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; HOMEODOMAIN PROTEINS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; PANCREAS; REAL-TIME POLYMERASE CHAIN REACTION; TYROSINE 3-MONOOXYGENASE;

EID: 84919971625     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-014-3341-6     Document Type: Article

References (50)

1. Collombat P, Xu X, Heimberg H, Mansouri A (2010) Pancreatic beta-cells: from generation to regeneration. Semin Cell Dev Biol 21:838–844
2. Kroon E, Martinson LA, Kadoya K et al (2008) Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 26:443–452
3. Arda HE, Benitez CM, Kim SK (2013) Gene regulatory networks governing pancreas development. Dev Cell 25:5–13
4. Oliver-Krasinski JM, Stoffers DA (2008) On the origin of the beta cell. Genes Dev 22:1998–2021
5. Gittes GK (2009) Developmental biology of the pancreas: a comprehensive review. Dev Biol 326:4–35
6. Heinis M, Simon MT, Duvillie B (2010) New insights into endocrine pancreatic development: the role of environmental factors. Horm Res Paediatr 74:77–82
7. Kim SK, Hebrok M (2001) Intercellular signals regulating pancreas development and function. Genes Dev 15:111–127
8. Ahlgren U, Jonsson J, Edlund H (1996) The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 122:1409–1416
9. Guz Y, Montminy MR, Stein R 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
10. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV (2002) The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 32:128–134
11. Pan FC, Wright C (2011) Pancreas organogenesis: from bud to plexus to gland. Dev Dyn 240:530–565
12. Attali M, Stetsyuk V, Basmaciogullari A et al (2007) Control of beta-cell differentiation by the pancreatic mesenchyme. Diabetes 56:1248–1258
13. Jorgensen MC, Ahnfelt-Ronne J, Hald J, Madsen OD, Serup P, Hecksher-Sorensen J (2007) An illustrated review of early pancreas development in the mouse. Endocr Rev 28:685–705
14. Cano DA, Soria B, Martin F, Rojas A (2014) Transcriptional control of mammalian pancreas organogenesis. Cell Mol Life Sci 71:2383–2402
15. 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
16. + cells are islet progenitors and are distinct from duct progenitors. Development 129:2447–2457
17. Sussel L, Kalamaras J, Hartigan-O’Connor DJ et al (1998) Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 125:2213–2221
18. Apelqvist A, Li H, Sommer L et al (1999) Notch signalling controls pancreatic cell differentiation. Nature 400:877–881
19. Jensen J, Heller RS, Funder-Nielsen T et al (2000) Independent development of pancreatic alpha- and beta-cells from neurogenin3-expressing precursors: a role for the notch pathway in repression of premature differentiation. Diabetes 49:163–176
20. Jensen J, Pedersen EE, Galante P et al (2000) Control of endodermal endocrine development by Hes-1. Nat Genet 24:36–44
21. Lee JC, Smith SB, Watada H et al (2001) Regulation of the pancreatic pro-endocrine gene neurogenin3. Diabetes 50:928–936
22. Teitelman G, Lee JK (1987) Cell lineage analysis of pancreatic islet development: glucagon and insulin cells arise from catecholaminergic precursors present in the pancreatic duct. Dev Biol 121:454–466
23. O’Keeffe GC, Barker RA, Caldwell MA (2009) Dopaminergic modulation of neurogenesis in the subventricular zone of the adult brain. Cell Cycle 8:2888–2894
24. Fitch SR, Kimber GM, Wilson NK et al (2012) Signaling from the sympathetic nervous system regulates hematopoietic stem cell emergence during embryogenesis. Cell Stem Cell 11:554–566
25. Lopez-Sanchez C, Bartulos O, Martinez-Campos E et al (2010) Tyrosine hydroxylase is expressed during early heart development and is required for cardiac chamber formation. Cardiovasc Res 88:111–120
26. Zhou QY, Quaife CJ, Palmiter RD (1995) Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374:640–643
27. Gouzi M, Kim YH, Katsumoto K, Johansson K, Grapin-Botton A (2011) Neurogenin3 initiates stepwise delamination of differentiating endocrine cells during pancreas development. Dev Dyn 240:589–604
28. Herrera PL (2000) Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 127:2317–2322
29. Herrera PL, Huarte J, Zufferey R et al (1994) Ablation of islet endocrine cells by targeted expression of hormone-promoter-driven toxigenes. Proc Natl Acad Sci U S A 91:12999–13003
30. Desgraz R, Herrera PL (2009) Pancreatic neurogenin 3-expressing cells are unipotent islet precursors. Development 136:3567–3574
31. Watada H, Scheel DW, Leung J, German MS (2003) Distinct gene expression programs function in progenitor and mature islet cells. J Biol Chem 278:17130–17140
32. Teitelman G, Joh TH, Reis DJ (1981) Linkage of the brain-skin-gut axis: islet cells originate from dopaminergic precursors. Peptides 2(Suppl 2):157–168
33. Teitelman G, Joh TH, Reis DJ (1981) Transformation of catecholaminergic precursors into glucagon (A) cells in mouse embryonic pancreas. Proc Natl Acad Sci U S A 78:5225–5229
34. Teitelman G, Alpert S, Polak JM, Martinez A, Hanahan D (1993) Precursor cells of mouse endocrine pancreas coexpress insulin, glucagon and the neuronal proteins tyrosine hydroxylase and neuropeptide Y, but not pancreatic polypeptide. Development 118:1031–1039
35. Wilson ME, Kalamaras JA, German MS (2002) Expression pattern of IAPP and prohormone convertase 1/3 reveals a distinctive set of endocrine cells in the embryonic pancreas. Mech Dev 115:171–176
36. Baetge G, Gershon MD (1989) Transient catecholaminergic (TC) cells in the vagus nerves and bowel of fetal mice: relationship to the development of enteric neurons. Dev Biol 132:189–211
37. Jonakait GM, Markey KA, Goldstein M, Black IB (1984) Transient expression of selected catecholaminergic traits in cranial sensory and dorsal root ganglia of the embryonic rat. Dev Biol 101:51–60
38. Bramswig NC, Kaestner KH (2011) Transcriptional regulation of alpha-cell differentiation. Diabetes Obes Metab 13(Suppl 1):13–20
39. Filippi A, Jainok C, Driever W (2012) Analysis of transcriptional codes for zebrafish dopaminergic neurons reveals essential functions of Arx and Isl1 in prethalamic dopaminergic neuron development. Dev Biol 369:133–149
40. Stott SR, Metzakopian E, Lin W, Kaestner KH, Hen R, Ang SL (2013) Foxa1 and foxa2 are required for the maintenance of dopaminergic properties in ventral midbrain neurons at late embryonic stages. J Neurosci 33:8022–8034
41. Ohta Y, Kosaka Y, Kishimoto N et al (2011) Convergence of the insulin and serotonin programs in the pancreatic beta-cell. Diabetes 60:3208–3216
42. Rukstalis JM, Habener JF (2009) Neurogenin3: a master regulator of pancreatic islet differentiation and regeneration. Islets 1:177–184
43. Nekrep N, Wang J, Miyatsuka T, German MS (2008) Signals from the neural crest regulate beta-cell mass in the pancreas. Development 135:2151–2160
44. Ostrom M, Loffler KA, Edfalk S et al (2008) Retinoic acid promotes the generation of pancreatic endocrine progenitor cells and their further differentiation into beta-cells. PLoS One 3:e2841
45. Johansson KA, Dursun U, Jordan N et al (2007) Temporal control of neurogenin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types. Dev Cell 12:457–465
46. Shih HP, Kopp JL, Sandhu M et al (2012) A Notch-dependent molecular circuitry initiates pancreatic endocrine and ductal cell differentiation. Development 139:2488–2499
47. Afelik S, Qu X, Hasrouni E et al (2012) Notch-mediated patterning and cell fate allocation of pancreatic progenitor cells. Development 139:1744–1753
48. Ahren B (2000) Autonomic regulation of islet hormone secretion—implications for health and disease. Diabetologia 43:393–410
49. Costes S, Langen R, Gurlo T, Matveyenko AV, Butler PC (2013) β-Cell failure in type 2 diabetes: a case of asking too much of too few? Diabetes 62:327–335
50. Hernandez-Sanchez C, Mansilla A, de la Rosa EJ, de Pablo F (2006) Proinsulin in development: new roles for an ancient prohormone. Diabetologia 49:1142–1150