Cx36 is a target of Beta2/NeuroD1, which associates with prenatal differentiation of insulin-producing β cells

Journal of Membrane Biology

Volumn 245, Issue 5-6, 2012, Pages 263-273

  Nlend, Rachel Nlend ^a   Aït Lounis, Aouatef ^b   Allagnat, Florent ^c   Cigliola, Valentina ^a   Charollais, Anne ^a   Reith, Walter ^a   Haefliger, Jacques Antoine ^c   Meda, Paolo ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Benyoucef Benkhedda   (Algeria)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Beta2 neurod1; Connexin; Gap junctions; Gene regulation; Pancreas; Promoter; Transcription factor

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CONNEXIN 36; INSULIN; NEUROGENIC DIFFERENTIATION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; E BOX ELEMENT; EMBRYO; FEMALE; GENE; GJD2 GENE; MALE; MOUSE; NONHUMAN; ORGANOGENESIS; PANCREAS; PANCREAS ISLET BETA CELL; PRENATAL DEVELOPMENT; PRENATAL PERIOD; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; COMPUTATIONAL BIOLOGY; CONNEXINS; GAP JUNCTIONS; HELA CELLS; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84864361989     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-012-9447-1     Document Type: Article

References (55)

1. Aramata S, Han SI, Yasuda K, Kataoka K (2005) Synergistic activation of the insulin gene promoter by the beta-cell enriched transcription factors MafA, Beta2, and Pdx1. Biochim Biophys Acta 1730:41-46 (Pubitemid 41008611)
2. Berthoud VM, Singh R, Minogue PJ, Ragsdale CW, Beyer EC (2004) Highly restricted pattern of connexin36 expression in chick somite development. Anat Embryol 209:11-18 (Pubitemid 40064368)
3. Bosco D, Haefliger JA, Meda P (2011) Connexins: key mediators of endocrine function. Physiol Rev 91:1393-1445
4. Carvalho CP, Barbosa HC, Britan A, Santos-Silva JC, Boschero AC, Meda P, Collares-Buzato CB (2010) Beta cell coupling and connexin expression change during the functional maturation of rat pancreatic islets. Diabetologia 53:1428-1437
5. Carvalho CP, Oliveira RB, Britan A, Silva-Santos JC, Boschero AC, Meda P, Collares-Buzato CB (2012) Impaired beta-to-beta cell coupling mediated by Cx36 gap junctions in pre-diabetic mice. Am J Physiol Endocrinol Metab 302 (in press)
6. Cho JH, Tsai MJ (2004) The role of BETA2/NeuroD1 in the development of the nervous system. Mol Neurobiol 30:35-47
7. Cina C, Bechberger JF, Ozog MA, Naus CC (2007) Expression of connexins in embryonic mouse neocortical development. J Comp Neurol 504:298-313 (Pubitemid 350012216)
8. Cummings DM, Yamazaki I, Cepeda C, Paul DL, Levine MS (2008) Neuronal coupling via connexin36 contributes to spontaneous synaptic currents of striatal medium-sized spiny neurons. J Neurosci Res 86:2147-2158
9. Degen J, Meier C, Van Der Giessen RS, Sohl G, Petrasch-Parwez E, Urschel S, Dermietzel R, Schilling K, De Zeeuw CI, Willecke K (2004) Expression pattern of lacZ reporter gene representing connexin36 in transgenic mice. J Comp Neurol 473:511-525 (Pubitemid 38580447)
10. Docherty HM, Hay CW, Ferguson LA, Barrow J, Durward E, Docherty K (2005) Relative contribution of PDX-1, MafA and E47/beta2 to the regulation of the human insulin promoter. Biochem J 389:813-820 (Pubitemid 41117341)
11. Gulisano M, Parenti R, Spinella F, Cicirata F (2000) Cx36 is dynamically expressed during early development of mouse brain and nervous system. Neuroreport 11:3823-3828
12. Habener JF, Kemp DM, Thomas MK (2005) Minireview: transcriptional regulation in pancreatic development. Endocrinology 146:1025-1034 (Pubitemid 40289291)
13. Head WS, Orseth ML, Nunemaker CS, Satin LS, Piston DW, Benninger RK (2012) Connexin-36 gap junctions regulate in vivo first- and second-phase insulin secretion dynamics and glucose tolerance in the conscious mouse. Diabetes 61 (in press)
14. Henderson E, Stein R (1994) c-jun inhibits transcriptional activation by the insulin enhancer, and the insulin control element is the target of control. Mol Cell Biol 14:655-662
15. Herrera PL (2000) Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 127:2317-2322 (Pubitemid 30386571)
16. Hohl M, Thiel G (2005) Cell type-specific regulation of RE-1 silencing transcription factor (REST) target genes. Eur J Neurosci 22:2216-2230 (Pubitemid 41653535)
17. Itkin-Ansari P, Marcora E, Geron I, Tyrberg B, Demeterco C, Hao E, Padilla C, Ratineau C, Leiter A, Lee JE, Levine F (2005) NeuroD1 in the endocrine pancreas: localization and dual function as an activator and repressor. Dev Dyn 233:946-953 (Pubitemid 40853470)
18. Iwata I, Nagafuchi S, Nakashima H, Kondo S, Koga T, Yokogawa Y, Akashi T, Shibuya T, Umeno Y, Okeda T, Shibata S, Kono S, Yasunami M, Ohkubo H, Niho Y (1999) Association of polymorphism in the NeuroD/BETA2 gene with type 1 diabetes in the Japanese. Diabetes 48:416-419 (Pubitemid 29061119)
19. Jonsson J, Carlsson L, Edlund T, Edlund H (1994) Insulin-promoterfactor 1 is required for pancreas development in mice. Nature 371:606-609 (Pubitemid 24315741)
20. Kim SK, MacDonald RJ (2002) Signaling and transcriptional control of pancreatic organogenesis. Curr Opin Genet Dev 12:540-547 (Pubitemid 35013536)
21. Kim JW, Seghers V, Cho JH, Kang Y, Kim S, Ryu Y, Baek K, Aguilar-Bryan L, Lee YD, Bryan J, Suh-Kim H (2002) Transactivation of the mouse sulfonylurea receptor I gene by BETA2/NeuroD. Mol Endocrinol 16:1097-1107 (Pubitemid 34478546)
22. Klee P, Allagnat F, Pontes H, Cederroth M, Charollais A, Caille D, Britan A, Haefliger JA, Meda P (2011) Connexins protect mouse pancreatic b cells against apoptosis. J Clin Invest 121: 4870-4879
23. Le Gurun S, Martin D, Formenton A, Maechler P, Caille D, Waeber G, Meda P, Haefliger JA (2003) Connexin-36 contributes to control function of insulin-producing cells. J Biol Chem 278: 37690-37697 (Pubitemid 37175293)
24. Lee JE (1997) NeuroD and neurogenesis. Dev Neurosci 19:27-32 (Pubitemid 27095951)
25. Lee JE, Hollenberg SM, Snider L, Turner DL, Lipnick N, Weintraub H (1995) Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268:836-884
26. Liu M, Pereira FA, Price SD, Chu MJ, Shope C, Himes D, Eatock RA, Brownell WE, Lysakowski A, Tsai MJ (2000) Essential role of Beta2/NeuroD1 in development of the vestibular and auditory systems. Genes Dev 14:2839-2854
27. MacDonald MJ (2007) Synergistic potent insulin release by combinations of weak secretagogues in pancreatic islets and INS-1 cells. J Biol Chem 282:6043-6052 (Pubitemid 47100859)
28. MacDonald PE, Rorsman P (2007) The ins and outs of secretion from pancreatic beta-cells: control of single-vesicle exo- and endocytosis. Physiology (Bethesda) 22:113-121
29. Malecki MT, Jhala US, Antonellis A, Fields L, Doria A, Orban T, Saad M, Warram JH, Montminy M, Krolewski AS (1999) Mutations in NEUROD1 are associated with the development of type 2 diabetes mellitus. Nat Genet 23:323-328 (Pubitemid 29526431)
30. Malecki MT, Cyganek K, Klupa T, Sieradzki J (2003) The Ala45Thr polymorphism of Beta2/NeuroD1 gene and susceptibility to type 2 diabetes mellitus in a Polish population. Acta Diabetol 40: 109-111 (Pubitemid 36850929)
31. Martin D, Tawadros T, Meylan L, Abderrahmani A, Condorelli DF, Waeber G, Haefliger JA (2003) Critical role of the transcriptional repressor neuron-restrictive silencer factor in the specific control of connexin36 in insulin-producing cell lines. J Biol Chem 278:53082-53089 (Pubitemid 38035911)
32. Masternak K, Peyraud N, Krawczyk M, Barras E, Reith W (2003) Chromatin remodeling and extragenic transcription at the MHC class II locus control region. Nat Immunol 4:132-137 (Pubitemid 36193014)
33. Meda P (2012) The in vivo b-to-b-cell chat room: connexin connections matter. Diabetes 61 (in press)
34. Mirasierra M, Vallejo M (2006) The homeoprotein Alx3 expressed in pancreatic beta-cells regulates insulin gene transcription by interacting with the basic helix-loop-helix protein E47. Mol Endocrinol 20:2876-2889 (Pubitemid 44833542)
35. Miyata T, Maeda T, Lee JE (1999) NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev 13:1647-1652 (Pubitemid 29325870)
36. Murtaugh LC (2007) Pancreas and beta-cell development: from the actual to the possible. Development 134:427-438 (Pubitemid 46332480)
37. Naya FJ, Stellrecht CM, Tsai MJ (1994) Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev 9:1009-1919
38. Naya FJ, Stellrecht CM, Tsai MJ (1995) Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev 9:1009-1019
39. Naya FJ, Huang HP, Qiu Y, Mutoh H, DeMayo FJ, Leiter AB, Tsai MJ (1997) Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroDdeficient mice. Genes Dev 11:2323-2334 (Pubitemid 27408530)
40. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, Hogan BL, Wright CV (1996) PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122:983-995 (Pubitemid 26096002)
41. Pérez-Armendariz EM, Cruz-Miguel L, Coronel-Cruz C, Esparza- Aguilar M, Pinzon-Estrada E, Rancaño-Camacho E, Zacarias- Climaco G, Olivares PF, Espinosa AM, Becker I, Sáez JC, Berumen J, Pérez-Palacios G (2012) Connexin 36 is expressed in beta and connexins 26 and 32 in acinar cells at the end of the secondary transition of mouse pancreatic development and increase during fetal and perinatal life. Anat Rec 295:980-990
42. Pictet RL, Clark WR, Williams RH, Rutter WJ (1972) An ultrastructural analysis of the developing embryonic pancreas. Dev Biol 29:436-467
43. Potolicchio I, Cigliola V, Velazquez-Garcia S, Klee P, Valjevac A, Kapic D, Cosovic E, Lepara O, Hadzovic-Dzuvo A, Mornjacovic Z, Meda P (2012) Connexin-dependent signaling in neurohormonal systems. Biochim Biophys Acta 1818:1919-1936
44. Poulin G, Turgeon B, Drouin J (1997) NeuroD1/beta2 contributes to cell-specific transcription of the proopiomelanocortin gene. Mol Cell Biol 17:6673-6682 (Pubitemid 27451214)
45. Qiu Y, Guo M, Huang S, Stein R (2002) Insulin gene transcription is mediated by interactions between the p300 coactivator and PDX- 1, BETA2, and E47. Mol Cell Biol 22:412-420 (Pubitemid 34027487)
46. Ravier MA, Guldenagel M, Charollais A, Gjinovci A, Caille D, Sohl G, Wollheim CB, Willecke K, Henquin JC, Meda P (2005) Loss of connexin36 channels alters beta-cell coupling, islet synchronization of glucose-induced Ca2? and insulin oscillations, and basal insulin release. Diabetes 54:1798-1807 (Pubitemid 40770770)
47. Robinson KA, Koepke JI, Kharodawala M, Lopes JM (2000) A network of yeast basic helix-loop-helix interactions. Nucleic Acids Res 28:4460-4466
48. Serre-Beinier V, Le Gurun S, Belluardo N, Trovato-Salinaro A, Charollais A, Haefliger JA, Condorelli DF, Meda P (2000) Cx36 preferentially connects beta-cells within pancreatic islets. Diabetes 49:727-734 (Pubitemid 30339987)
49. Serre-Beinier V, Bosco D, Zulianello L, Charollais A, Caille D, Charpantier E, Gauthier BR, Diaferia GR, Giepmans BN, Lupi R, Marchetti P, Deng S, Buhler L, Berney T, Cirulli V, Meda P (2009) Cx36 makes channels coupling human pancreatic betacells, and correlates with insulin expression. Hum Mol Genet 18:428-439
50. Sommer L, Ma Q, Anderson DJ (1996) Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol Cell Neurosci 8:221-241 (Pubitemid 27057148)
51. Speier S, Gjinovci A, Charollais A, Meda P, Rupnik M (2007) Cx36- mediated coupling reduces beta-cell heterogeneity, confines the stimulating glucose concentration range, and affects insulin release kinetics. Diabetes 56:1078-1086 (Pubitemid 46525063)
52. Theis M, Mas C, Doring B, Degen J, Brink C, Caille D, Charollais A, Kruger O, Plum A, Nepote V, Herrera P, Meda P, Willecke K (2004) Replacement by a lacZ reporter gene assigns mouse connexin36, 45 and 43 to distinct cell types in pancreatic islets. Exp Cell Res 294:18-29 (Pubitemid 38229776)
53. Wellershaus K, Degen J, Deuchars J, Theis M, Charollais A, Caille D, Gauthier B, Janssen-Bienhold U, Sonntag S, Herrera P, Meda P, Willecke K (2008) A new conditional mouse mutant reveals specific expression and functions of connexin36 in neurons and pancreatic beta-cells. Exp Cell Res 314:997-1012
54. Yamada S, Motohashi Y, Yanagawa T, Maruyama T, Kasuga A, Hirose H, Matsubara K, Shimada A, Saruta T (2001) NeuroD/ beta2 gene G→A polymorphism may affect onset pattern of type 1 diabetes in Japanese. Diabetes Care 24:1438-1441 (Pubitemid 33716434)
55. Zhang C, Moriguchi T, Kajihara M, Esaki R, Harada A, Shimohata H, Oishi H, Hamada M, Morito N, Hasegawa K, Kudo T, Engel JD, Yamamoto M, Takahashi S (2005) MafA is a key regulator of glucose-stimulated insulin secretion. Mol Cell Biol 25: 4969-4976 (Pubitemid 40781098)