Convergence of the insulin and serotonin programs in the pancreatic β-cell

Diabetes

Volumn 60, Issue 12, 2011, Pages 3208-3216

  Ohta, Yasuharu ^a,d   Kosaka, Yasuhiro ^a   Kishimoto, Nina ^a   Wang, Juehu ^a   Smith, Stuart B ^a   Honig, Gerard ^a   Kim, Hail ^a   Gasa, Rosa M ^a,e,f   Neubauer, Nicole ^a   Liou, Angela ^a   Tecott, Laurence H ^a   Deneris, Evan S ^b   German, Michael S ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF BARCELONA   (Spain)

^f INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; SEROTONIN; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR PDX 1; TRYPTOPHAN HYDROXYLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GLUCOSE METABOLISM; IMMUNOHISTOCHEMISTRY; IMPAIRED GLUCOSE TOLERANCE; IN SITU HYBRIDIZATION; INSULIN RELEASE; INSULIN TOLERANCE TEST; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; SEROTONINERGIC SYSTEM;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INSULIN; INSULIN-SECRETING CELLS; MICE; NIH 3T3 CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEROTONERGIC NEURONS; SEROTONIN; TRANSCRIPTION FACTORS; TRYPTOPHAN HYDROXYLASE;

EID: 82255185857     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db10-1192     Document Type: Article

References (50)

1. Falck B, Torp A. A fluorescence method for histochemical demonstration of noradrenalin in the adrenal medulla. Med Exp Int J Exp Med 1961;5:428-432
2. Pearse AG, Polak JM. Neural crest origin of the endocrine polypeptide (APUD) cells of the gastrointestinal tract and pancreas. Gut 1971;12:783-788
3. Pictet RL, Rall LB, Phelps P, Rutter WJ. The neural crest and the origin of the insulin-producing and other gastrointestinal hormone-producing cells. Science 1976;191:191-192
4. Le Douarin NM. On the origin of pancreatic endocrine cells. Cell 1988;53:169-171
5. Wilson ME, Scheel D, German MS. Gene expression cascades in pancreatic development. Mech Dev 2003;120:65-80 (Pubitemid 35469131)
6. Falkmer S. Phylogeny and ontogeny of the neuroendocrine cells of the gastrointestinal tract. Endocrinol Metab Clin North Am 1993;22:731-752 (Pubitemid 24017270)
7. Devaskar SU, Giddings SJ, Rajakumar PA, Carnaghi LR, Menon RK, Zahm DS. Insulin gene expression and insulin synthesis in mammalian neuronal cells. J Biol Chem 1994;269:8445-8454 (Pubitemid 24200266)
8. Gelling RW, Morton GJ, Morrison CD, et al. Insulin action in the brain contributes to glucose lowering during insulin treatment of diabetes. Cell Metab 2006;3:67-73
9. Ahrén B. Autonomic regulation of islet hormone secretion - implications for health and disease. Diabetologia 2000;43:393-410 (Pubitemid 30237947)
10. Cordes SP. Molecular genetics of the early development of hindbrain serotonergic neurons. Clin Genet 2005;68:487-494 (Pubitemid 41748847)
11. Sander M, Sussel L, Conners J, et al. Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of beta-cell formation in the pancreas. Development 2000;127:5533-5540 (Pubitemid 32049205)
12. Craven SE, Lim KC, Ye W, Engel JD, de Sauvage F, Rosenthal A. Gata2 specifies serotonergic neurons downstream of sonic hedgehog. Development 2004;131:1165-1173 (Pubitemid 38380469)
13. Tecott LH. Serotonin and the orchestration of energy balance. Cell Metab 2007;6:352-361 (Pubitemid 350012001)
14. Maekawa F, Toyoda Y, Torii N, et al. Localization of glucokinase-like immunoreactivity in the rat lower brain stem: for possible location of brain glucose-sensing mechanisms. Endocrinology 2000;141:375-384 (Pubitemid 32260380)
15. Moriyama R, Tsukamura H, Kinoshita M, Okazaki H, Kato Y, Maeda K. In vitro increase in intracellular calcium concentrations induced by low or high extracellular glucose levels in ependymocytes and serotonergic neurons of the rat lower brainstem. Endocrinology 2004;145:2507-2515 (Pubitemid 38535078)
16. Xu AW, Kaelin CB, Takeda K, Akira S, Schwartz MW, Barsh GS. PI3K integrates the action of insulin and leptin on hypothalamic neurons. J Clin Invest 2005;115:951-958 (Pubitemid 40489399)
17. Lam DD, Przydzial MJ, Ridley SH, et al. Serotonin 5-HT2C receptor agonist promotes hypophagia via downstream activation of melanocortin 4 receptors. Endocrinology 2008;149:1323-1328 (Pubitemid 351397929)
18. Xu Y, Jones JE, Kohno D, et al. 5-HT2CRs expressed by pro-opiomelanocortin neurons regulate energy homeostasis. Neuron 2008;60:582-589
19. Kaplan DD, Zimmermann G, Suyama K, Meyer T, Scott MP. A nucleostemin family GTPase, NS3, acts in serotonergic neurons to regulate insulin signaling and control body size. Genes Dev 2008;22:1877-1893 (Pubitemid 352008637)
20. Murakami H, Murakami S. Serotonin receptors antagonistically modulate Caenorhabditis elegans longevity. Aging Cell 2007;6:483-488 (Pubitemid 47087053)
21. Wade JM, Juneja P, MacKay AW, et al. Synergistic impairment of glucose homeostasis in ob/ob mice lacking functional serotonin 2C receptors. Endocrinology 2008;149:955-961 (Pubitemid 351397943)
22. Hendricks TJ, Fyodorov DV, Wegman LJ, et al. Pet-1 ETS gene plays a critical role in 5-HT neuron development and is required for normal anxiety-like and aggressive behavior. Neuron 2003;37:233-247 (Pubitemid 36143819)
23. Lee CS, Perreault N, Brestelli JE, Kaestner KH. Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev 2002;16:1488-1497 (Pubitemid 34686330)
24. Sussel L, Kalamaras J, Hartigan-O'Connor DJ, et al. Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 1998;125:2213-2221 (Pubitemid 28336383)
25. Scott MM, Wylie CJ, Lerch JK, et al. A genetic approach to access serotonin neurons for in vivo and in vitro studies. Proc Natl Acad Sci USA 2005;102:16472-16477 (Pubitemid 41688938)
26. Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002;129:2447-2457 (Pubitemid 34863851)
27. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999;21:70-71 (Pubitemid 29036285)
28. Novak A, Guo C, Yang W, Nagy A, Lobe CG. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 2000;28:147-155
29. Lynn FC, Smith SB, Wilson ME, Yang KY, Nekrep N, German MS. Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc Natl Acad Sci USA 2007;104:10500-10505 (Pubitemid 47185694)
30. Szot GL, Koudria P, Bluestone JA. Murine pancreatic islet isolation. J Vis Exp 2007;7:255
31. Schwitzgebel VM, Scheel DW, Conners JR, et al. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 2000;127:3533-3542
32. Miyatsuka T, Li Z, German MS. Chronology of islet differentiation revealed by temporal cell labeling. Diabetes 2009;58:1863-1868
33. Walther DJ, Peter JU, Bashammakh S, et al. Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 2003;299:76 (Pubitemid 36042402)
34. Sakowski SA, Geddes TJ, Thomas DM, Levi E, Hatfield JS, Kuhn DM. Differential tissue distribution of tryptophan hydroxylase isoforms 1 and 2 as revealed with monospecific antibodies. Brain Res 2006;1085:11-18 (Pubitemid 43728204)
35. Ebihara S, Marks T, Hudson DJ, Menaker M. Genetic control of melatonin synthesis in the pineal gland of the mouse. Science 1986;231:491-493 (Pubitemid 16163738)
36. Hendricks T, Francis N, Fyodorov D, Deneris ES. The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J Neurosci 1999;19:10348-10356 (Pubitemid 30228042)
37. Wang YC, Zuraek MB, Kosaka Y, et al. The ETS oncogene family transcription factor FEV identifies serotonin-producing cells in normal and neoplastic small intestine. Endocr Relat Cancer 2010;17:283-291
38. Wicksteed B, Brissova M, Yan W, et al. Conditional gene targeting in mouse pancreatic ß-Cells: analysis of ectopic Cre transgene expression in the brain. Diabetes 2010;59:3090-3098
39. Honig G, Liou A, Berger M, German MS, Tecott LH. Precise pattern of recombination in serotonergic and hypothalamic neurons in a Pdx1-cre transgenic mouse line. J Biomed Sci 2010;17:82
40. Fyodorov D, Nelson T, Deneris E. Pet-1, a novel ETS domain factor that can activate neuronal nAchR gene transcription. J Neurobiol 1998;34:151-163 (Pubitemid 28067143)
41. Boam DS, Clark AR, Docherty K. Positive and negative regulation of the human insulin gene by multiple trans-acting factors. J Biol Chem 1990;265:8285-8296
42. Smith PA, Duchen MR, Ashcroft FM. A fluorimetric and amperometric study of calcium and secretion in isolated mouse pancreatic beta-cells. Pflugers Arch 1995;430:808-818
43. Harris PE, Ferrara C, Barba P, Polito T, Freeby M, Maffei A. VMAT2 gene expression and function as it applies to imaging beta-cell mass. J Mol Med (Berl) 2008;86:5-16
44. Rieck S, White P, Schug J, et al. The transcriptional response of the islet to pregnancy in mice. Mol Endocrinol 2009;23:1702-1712
45. Schraenen A, Lemaire K, de Faudeur G, et al. Placental lactogens induce serotonin biosynthesis in a subset of mouse beta cells during pregnancy. Diabetologia 2010;53:2589-2599
46. Kim H, Toyofuku Y, Lynn FC, et al. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 2010;16:804-808
47. Matsuda M, Imaoka T, Vomachka AJ, et al. Serotonin regulates mammary gland development via an autocrine-paracrine loop. Dev Cell 2004;6:193-203 (Pubitemid 38195217)
48. Finegood DT, Scaglia L, Bonner-Weir S. Dynamics of beta-cell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes 1995;44:249-256
49. Meier JJ, Butler AE, Saisho Y, et al. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 2008;57:1584-1594
50. Mezuk B, Eaton WW, Albrecht S, Golden SH. Depression and type 2 diabetes over the lifespan: a meta-analysis. Diabetes Care 2008;31:2383-2390