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Roles of connexins and pannexins in (neuro)endocrine physiology

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Abstract

To ensure appropriate secretion in response to demand, (neuro)endocrine tissues liberate massive quantities of hormones, which act to coordinate and synchronize biological signals in distant secretory and nonsecretory cell populations. Intercellular communication plays a central role in this control. With regard to molecular identity, junctional cell–cell communication is supported by connexin-based gap junctions. In addition, connexin hemichannels, the structural precursors of gap junctions, as well as pannexin channels have recently emerged as possible modulators of the secretory process. This review focuses on the expression of connexins and pannexins in various (neuro)endocrine tissues, including the adrenal cortex and medulla, the anterior pituitary, the endocrine hypothalamus and the pineal, thyroid and parathyroid glands. Upon a physiological or pathological stimulus, junctional intercellular coupling can be acutely modulated or persistently remodeled, thus offering multiple regulatory possibilities. The functional roles of gap junction-mediated intercellular communication in endocrine physiology as well as the involvement of connexin/pannexin-related hemichannels are also discussed.

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Abbreviations

ACTH:

Adrenocorticotropic hormone

ATP:

Adenosine triphosphate

ARC:

Arcuate

cAMP:

Cyclic adenosine monophosphate

CRH:

Corticotropin-releasing hormone

Cx:

Connexin

FS:

Folliculostellate

FSH:

Follicle-stimulating hormone

GH:

Growth hormone

GHRH:

Growth hormone-releasing hormone

GnRH:

Gonadotropin-releasing hormone

LH:

Luteinizing hormone

PACAP:

Pituitary adenylate cyclase-activating peptide

Panx:

Pannexin

PRL:

Prolactin

PV:

Parvocellular

PVN:

Paraventricular nucleus

SON:

Supraoptic nucleus

T3:

Triiodothyronine

T4:

Thyroxine

TRH:

Thyrotropin-releasing hormone

TSH:

Thyroid-stimulating hormone

ZF:

Zona fasciculata

ZG:

Zona glomerulosa

ZR:

Zona reticularis

References

  1. South J, Blass B (2012) Handbook of neuroendocrinology. Elsevier, London

    Google Scholar 

  2. Veldhuis JD, Keenan DM, Pincus SM (2010) Regulation of complex pulsatile and rhythmic neuroendocrine systems: the male gonadal axis as a prototype. Prog Brain Res 181:79–110. doi:10.1016/S0079-6123(08)81006-0

    CAS  PubMed  Google Scholar 

  3. Bosco D, Haefliger JA, Meda P (2011) Connexins: key mediators of endocrine function. Physiol Rev 91(4):1393–1445. doi:10.1152/physrev.00027.2010

    CAS  PubMed  Google Scholar 

  4. 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 neuro-hormonal systems. Biochim Biophys Acta 1818 (8):1919–1936. doi:10.1016/j.bbamem.2011.09.022

  5. Ehrhart-Bornstein M, Hilbers U (1998) Neuroendocrine properties of adrenocortical cells. Horm Metab Res 30(6–7):436–439. doi:10.1055/s-2007-978911

    CAS  PubMed  Google Scholar 

  6. Friend DS, Gilula NB (1972) A distinctive cell contact in the rat adrenal cortex. J Cell Biol 53(1):148–163

    CAS  PubMed Central  PubMed  Google Scholar 

  7. Willenberg HS, Schott M, Saeger W, Tries A, Scherbaum WA, Bornstein SR (2006) Expression of connexins in chromaffin cells of normal human adrenals and in benign and malignant pheochromocytomas. Ann N Y Acad Sci 1073:578–583. doi:10.1196/annals.1353.060

    CAS  PubMed  Google Scholar 

  8. Meda P, Pepper MS, Traub O, Willecke K, Gros D, Beyer E, Nicholson B, Paul D, Orci L (1993) Differential expression of gap junction connexins in endocrine and exocrine glands. Endocrinology 133(5):2371–2378

    CAS  PubMed  Google Scholar 

  9. Murray SA, Pharrams SY (1997) Comparison of gap junction expression in the adrenal gland. Microsc Res Tech 36(6):510–519. doi:10.1002/(SICI)1097-0029(19970315)36:6<510:AID-JEMT8>3.0.CO;2-L

    CAS  PubMed  Google Scholar 

  10. Oyoyo UA, Shah US, Murray SA (1997) The role of alpha1 (connexin-43) gap junction expression in adrenal cortical cell function. Endocrinology 138(12):5385–5397. doi:10.1210/endo.138.12.5617

    CAS  PubMed  Google Scholar 

  11. Murray SA, Davis K, Fishman LM, Bornstein SR (2000) Alpha1 connexin 43 gap junctions are decreased in human adrenocortical tumors. J Clin Endocrinol Metab 85(2):890–895

    CAS  PubMed  Google Scholar 

  12. Desarmenien MG, Jourdan C, Toutain B, Vessieres E, Hormuzdi SG, Guerineau NC (2013) Gap junction signalling is a stress-regulated component of adrenal neuroendocrine stimulus-secretion coupling in vivo. Nat Commun 4:2938. doi:10.1038/ncomms3938

    PubMed  Google Scholar 

  13. Murray SA, Oyoyo UA, Pharrams SY, Kumar NM, Gilula NB (1995) Characterization of gap junction expression in the adrenal gland. Endocr Res 21(1–2):221–229

    CAS  PubMed  Google Scholar 

  14. Davis KT, Prentice N, Gay VL, Murray SA (2002) Gap junction proteins and cell–cell communication in the three functional zones of the adrenal gland. J Endocrinol 173(1):13–21

    CAS  PubMed  Google Scholar 

  15. Martin AO, Mathieu MN, Chevillard C, Guerineau NC (2001) Gap junctions mediate electrical signaling and ensuing cytosolic Ca2+ increases between chromaffin cells in adrenal slices: a role in catecholamine release. J Neurosci 21(15):5397–5405

    CAS  PubMed  Google Scholar 

  16. Palacios G (1979) Cell junctions in the adrenal cortex of the postnatal rat. J Anat 129(Pt 4):695–701

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Dahl E, Winterhager E, Traub O, Willecke K (1995) Expression of gap junction genes, connexin40 and connexin43, during fetal mouse development. Anat Embryol (Berl) 191(3):267–278

    CAS  Google Scholar 

  18. Joseph T, Slack C, Gould RP (1973) Gap junctions and electrotonic coupling in foetal rabbit adrenal cortical cells. J Embryol Exp Morphol 29(3):681–696

    CAS  PubMed  Google Scholar 

  19. McDonald TJ, Li C, Massmann GA, Figueroa JP (2003) Connexin 43 ontogeny in fetal sheep adrenal glands. Steroids 68(7–8):613–620

    CAS  PubMed  Google Scholar 

  20. McNutt NS, Jones AL (1970) Observations on the ultrastructure of cytodifferentiation in the human fetal adrenal cortex. Lab Invest 22(6):513–527

    CAS  PubMed  Google Scholar 

  21. Murray SA, Fletcher WH (1984) Hormone-induced intercellular signal transfer dissociates cyclic AMP-dependent protein kinase. J Cell Biol 98(5):1710–1719

    CAS  PubMed  Google Scholar 

  22. Munari-Silem Y, Rousset B (1996) Gap junction-mediated cell-to-cell communication in endocrine glands–molecular and functional aspects: a review. Eur J Endocrinol 135(3):251–264

    CAS  PubMed  Google Scholar 

  23. Murray SA, Davis K, Gay V (2003) ACTH and adrenocortical gap junctions. Microsc Res Tech 61(3):240–246. doi:10.1002/jemt.10332

    CAS  PubMed  Google Scholar 

  24. Murray SA, Nickel BM, Gay VL (2009) Gap junctions as modulators of adrenal cortical cell proliferation and steroidogenesis. Mol Cell Endocrinol 300(1–2):51–56. doi:10.1016/j.mce.2008.09.027

    CAS  PubMed  Google Scholar 

  25. Murray SA, Shah US (1998) Modulation of adrenal gap junction expression. Horm Metab Res 30(6–7):426–431. doi:10.1055/s-2007-978909

    CAS  PubMed  Google Scholar 

  26. Shah US, Murray SA (2001) Bimodal inhibition of connexin 43 gap junctions decreases ACTH-induced steroidogenesis and increases bovine adrenal cell population growth. J Endocrinol 171(1):199–208

    CAS  PubMed  Google Scholar 

  27. Davis KT, McDuffie I, Mawhinney LA, Murray SA (2000) Hypophysectomy results in a loss of connexin gap junction protein from the adrenal cortex. Endocr Res 26(4):561–570

    CAS  PubMed  Google Scholar 

  28. Munari-Silem Y, Lebrethon MC, Morand I, Rousset B, Saez JM (1995) Gap junction-mediated cell-to-cell communication in bovine and human adrenal cells. A process whereby cells increase their responsiveness to physiological corticotropin concentrations. J Clin Invest 95(4):1429–1439. doi:10.1172/JCI117813

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Defranco BH, Nickel BM, Baty CJ, Martinez JS, Gay VL, Sandulache VC, Hackam DJ, Murray SA (2008) Migrating cells retain gap junction plaque structure and function. Cell Commun Adhes 15(3):273–288. doi:10.1080/15419060802198298

    CAS  PubMed  Google Scholar 

  30. Grynszpan-Wynograd O, Nicolas G (1980) Intercellular junctions in the adrenal medulla: a comparative freeze-fracture study. Tissue Cell 12(4):661–672

    CAS  PubMed  Google Scholar 

  31. Anderson DJ (1997) Cellular and molecular biology of neural crest cell lineage determination. Trends Genet 13(7):276–280

    CAS  PubMed  Google Scholar 

  32. Massey SC, O’Brien JJ, Trexler EB, Li W, Keung JW, Mills SL, O’Brien J (2003) Multiple neuronal connexins in the mammalian retina. Cell Commun Adhes 10(4–6):425–430

    CAS  PubMed  Google Scholar 

  33. Eiberger J, Kibschull M, Strenzke N, Schober A, Bussow H, Wessig C, Djahed S, Reucher H, Koch DA, Lautermann J, Moser T, Winterhager E, Willecke K (2006) Expression pattern and functional characterization of connexin29 in transgenic mice. Glia 53(6):601–611. doi:10.1002/glia.20315

    PubMed  Google Scholar 

  34. Colomer C, Olivos Ore LA, Coutry N, Mathieu MN, Arthaud S, Fontanaud P, Iankova I, Macari F, Thouennon E, Yon L, Anouar Y, Guerineau NC (2008) Functional remodeling of gap junction-mediated electrical communication between adrenal chromaffin cells in stressed rats. J Neurosci 28(26):6616–6626. doi:10.1523/JNEUROSCI.5597-07.2008

    CAS  PubMed  Google Scholar 

  35. Hill J, Lee SK, Samasilp P, Smith C (2012) Pituitary adenylate cyclase-activating peptide enhances electrical coupling in the mouse adrenal medulla. Am J Physiol Cell Physiol 303(3):C257–C266. doi:10.1152/ajpcell.00119.2012

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Cena V, Nicolas GP, Sanchez-Garcia P, Kirpekar SM, Garcia AG (1983) Pharmacological dissection of receptor-associated and voltage-sensitive ionic channels involved in catecholamine release. Neuroscience 10(4):1455–1462

    CAS  PubMed  Google Scholar 

  37. Colomer C, Martin AO, Desarmenien MG, Guerineau NC (2012) Gap junction-mediated intercellular communication in the adrenal medulla: An additional ingredient of stimulus-secretion coupling regulation. Biochim Biophys Acta 1818 (8):1937–1951. doi:10.1016/j.bbamem.2011.07.034

  38. Martin AO, Mathieu MN, Guerineau NC (2003) Evidence for long-lasting cholinergic control of gap junctional communication between adrenal chromaffin cells. J Neurosci 23(9):3669–3678

    CAS  PubMed  Google Scholar 

  39. Martin AO, Alonso G, Guerineau NC (2005) Agrin mediates a rapid switch from electrical coupling to chemical neurotransmission during synaptogenesis. J Cell Biol 169(3):503–514. doi:10.1083/jcb.200411054

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Colomer C, Desarmenien MG, Guerineau NC (2009) Revisiting the stimulus-secretion coupling in the adrenal medulla: role of gap junction-mediated intercellular communication. Mol Neurobiol 40(1):87–100. doi:10.1007/s12035-009-8073-0

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Colomer C, Lafont C, Guerineau NC (2008) Stress-induced intercellular communication remodeling in the rat adrenal medulla. Ann N Y Acad Sci 1148:106–111. doi:10.1196/annals.1410.040

    PubMed  Google Scholar 

  42. Kuri BA, Chan SA, Smith CB (2009) PACAP regulates immediate catecholamine release from adrenal chromaffin cells in an activity-dependent manner through a protein kinase C-dependent pathway. J Neurochem 110(4):1214–1225. doi:10.1111/j.1471-4159.2009.06206.x

    CAS  PubMed Central  PubMed  Google Scholar 

  43. Stroth N, Kuri BA, Mustafa T, Chan SA, Smith CB, Eiden LE (2013) PACAP controls adrenomedullary catecholamine secretion and expression of catecholamine biosynthetic enzymes at high splanchnic nerve firing rates characteristic of stress transduction in male mice. Endocrinology 154(1):330–339. doi:10.1210/en.2012-1829

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Colomer C, Olivos-Ore LA, Vincent A, McIntosh JM, Artalejo AR, Guerineau NC (2010) Functional characterization of alpha9-containing cholinergic nicotinic receptors in the rat adrenal medulla: implication in stress-induced functional plasticity. J Neurosci 30(19):6732–6742. doi:10.1523/JNEUROSCI.4997-09.2010

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Rodriguez H, Filippa V, Mohamed F, Dominguez S, Scardapane L (2007) Interaction between chromaffin and sustentacular cells in adrenal medulla of viscacha (Lagostomus maximus maximus). Anat Histol Embryol 36(3):182–185. doi:10.1111/j.1439-0264.2006.00732.x

    CAS  PubMed  Google Scholar 

  46. Belliveau DJ, Bani-Yaghoub M, McGirr B, Naus CC, Rushlow WJ (2006) Enhanced neurite outgrowth in PC12 cells mediated by connexin hemichannels and ATP. J Biol Chem 281(30):20920–20931. doi:10.1074/jbc.M600026200

    CAS  PubMed  Google Scholar 

  47. Schock SC, Leblanc D, Hakim AM, Thompson CS (2008) ATP release by way of connexin 36 hemichannels mediates ischemic tolerance in vitro. Biochem Biophys Res Commun 368(1):138–144. doi:10.1016/j.bbrc.2008.01.054

    CAS  PubMed  Google Scholar 

  48. John SA, Kondo R, Wang SY, Goldhaber JI, Weiss JN (1999) Connexin-43 hemichannels opened by metabolic inhibition. J Biol Chem 274(1):236–240

    CAS  PubMed  Google Scholar 

  49. Wang N, De Bock M, Decrock E, Bol M, Gadicherla A, Vinken M, Rogiers V, Bukauskas FF, Bultynck G, Leybaert L (2013) Paracrine signaling through plasma membrane hemichannels. Biochim Biophys Acta 1828(1):35–50. doi:10.1016/j.bbamem.2012.07.002

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Sahu G, Sukumaran S, Bera AK (2014) Pannexins form gap junctions with electrophysiological and pharmacological properties distinct from connexins. Sci Rep 4:4955. doi:10.1038/srep04955

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Momboisse F, Olivares MJ, Baez-Matus X, Guerra MJ, Flores-Munoz C, Saez JC, Martinez AD, Cardenas AM (2014) Pannexin 1 channels: new actors in the regulation of catecholamine release from adrenal chromaffin cells. Front Cell Neurosci 8:270. doi:10.3389/fncel.2014.00270

    PubMed Central  PubMed  Google Scholar 

  52. Vanden Abeele F, Bidaux G, Gordienko D, Beck B, Panchin YV, Baranova AV, Ivanov DV, Skryma R, Prevarskaya N (2006) Functional implications of calcium permeability of the channel formed by pannexin 1. J Cell Biol 174(4):535–546. doi:10.1083/jcb.200601115

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Iglesias R, Dahl G, Qiu F, Spray DC, Scemes E (2009) Pannexin 1: the molecular substrate of astrocyte “hemichannels”. J Neurosci 29(21):7092–7097. doi:10.1523/JNEUROSCI.6062-08.2009

    CAS  PubMed Central  PubMed  Google Scholar 

  54. Le Tissier PR, Hodson DJ, Lafont C, Fontanaud P, Schaeffer M, Mollard P (2012) Anterior pituitary cell networks. Front Neuroendocrinol 33(3):252–266. doi:10.1016/j.yfrne.2012.08.002

    PubMed  Google Scholar 

  55. Nakajima T, Yamaguchi H, Takahashi K (1980) S100 protein in folliculostellate cells of the rat pituitary anterior lobe. Brain Res 191(2):523–531

    CAS  PubMed  Google Scholar 

  56. Fauquier T, Lacampagne A, Travo P, Bauer K, Mollard P (2002) Hidden face of the anterior pituitary. Trends Endocrinol Metab 13(7):304–309

    CAS  PubMed  Google Scholar 

  57. Mollard P, Hodson DJ, Lafont C, Rizzoti K, Drouin J (2012) A tridimensional view of pituitary development and function. Trends Endocrinol Metab 23(6):261–269. doi:10.1016/j.tem.2012.02.004

    CAS  PubMed  Google Scholar 

  58. Hodson DJ, Mollard P (2012) Pituitary endocrine cell networks - 10 years and beyond. Ann Endocrinol (Paris) 73(2):56–58. doi:10.1016/j.ando.2012.03.033

    CAS  Google Scholar 

  59. Hodson DJ, Romano N, Schaeffer M, Fontanaud P, Lafont C, Fiordelisio T, Mollard P (2012) Coordination of calcium signals by pituitary endocrine cells in situ. Cell Calcium 51(3–4):222–230. doi:10.1016/j.ceca.2011.11.007

    CAS  PubMed  Google Scholar 

  60. Hodson DJ, Mollard P (2013) Navigating pituitary structure and function—defining a roadmap for hormone secretion. J Neuroendocrinol 25(7):674–675. doi:10.1111/jne.12041

    CAS  PubMed  Google Scholar 

  61. Fauquier T, Guerineau NC, McKinney RA, Bauer K, Mollard P (2001) Folliculostellate cell network: a route for long-distance communication in the anterior pituitary. Proc Natl Acad Sci USA 98(15):8891–8896. doi:10.1073/pnas.151339598

    CAS  PubMed Central  PubMed  Google Scholar 

  62. Bonnefont X, Lacampagne A, Sanchez-Hormigo A, Fino E, Creff A, Mathieu MN, Smallwood S, Carmignac D, Fontanaud P, Travo P, Alonso G, Courtois-Coutry N, Pincus SM, Robinson IC, Mollard P (2005) Revealing the large-scale network organization of growth hormone-secreting cells. Proc Natl Acad Sci USA 102(46):16880–16885. doi:10.1073/pnas.0508202102

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Sanchez-Cardenas C, Fontanaud P, He Z, Lafont C, Meunier AC, Schaeffer M, Carmignac D, Molino F, Coutry N, Bonnefont X, Gouty-Colomer LA, Gavois E, Hodson DJ, Le Tissier P, Robinson IC, Mollard P (2010) Pituitary growth hormone network responses are sexually dimorphic and regulated by gonadal steroids in adulthood. Proc Natl Acad Sci USA 107(50):21878–21883. doi:10.1073/pnas.1010849107

    CAS  PubMed Central  PubMed  Google Scholar 

  64. Budry L, Lafont C, El Yandouzi T, Chauvet N, Conejero G, Drouin J, Mollard P (2011) Related pituitary cell lineages develop into interdigitated 3D cell networks. Proc Natl Acad Sci USA 108(30):12515–12520. doi:10.1073/pnas.1105929108

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Hodson DJ, Schaeffer M, Romano N, Fontanaud P, Lafont C, Birkenstock J, Molino F, Christian H, Lockey J, Carmignac D, Fernandez-Fuente M, Le Tissier P, Mollard P (2012) Existence of long-lasting experience-dependent plasticity in endocrine cell networks. Nat Commun 3:605. doi:10.1038/ncomms1612

    PubMed Central  PubMed  Google Scholar 

  66. Featherstone K, Harper CV, McNamara A, Semprini S, Spiller DG, McNeilly J, McNeilly AS, Mullins JJ, White MR, Davis JR (2011) Pulsatile patterns of pituitary hormone gene expression change during development. J Cell Sci 124(Pt 20):3484–3491. doi:10.1242/jcs.088500

    CAS  PubMed Central  PubMed  Google Scholar 

  67. Sanchez-Cardenas C, Hernandez-Cruz A (2010) GnRH-Induced [Ca2+]i-signalling patterns in mouse gonadotrophs recorded from acute pituitary slices in vitro. Neuroendocrinology 91(3):239–255. doi:10.1159/000274493

    CAS  PubMed  Google Scholar 

  68. Schlegel W, Winiger BP, Mollard P, Vacher P, Wuarin F, Zahnd GR, Wollheim CB, Dufy B (1987) Oscillations of cytosolic Ca2+ in pituitary cells due to action potentials. Nature 329(6141):719–721. doi:10.1038/329719a0

    CAS  PubMed  Google Scholar 

  69. Mollard P, Schlegel W (1996) Why are endocrine pituitary cells excitable? Trends Endocrinol Metab 7(10):361–365

    CAS  PubMed  Google Scholar 

  70. Stojilkovic SS, Tabak J, Bertram R (2010) Ion channels and signaling in the pituitary gland. Endocr Rev 31(6):845–915. doi:10.1210/er.2010-0005

    CAS  PubMed Central  PubMed  Google Scholar 

  71. Fletcher WH, Anderson NC, Jr., Everett JW (1975) Intercellular communication in the rat anterior pituitary gland. An in vivo and in vitro study. J Cell Biol 67 (2PT.1):469–476

  72. Horvath E, Kovacs K, Ezrin C (1977) Junctional contract between lactotrophs and gonadotrophs in the rat pituitary. IRCS Med Sci 5:511

    Google Scholar 

  73. Soji T, Herbert DC (1989) Intercellular communication between rat anterior pituitary cells. Anat Rec 224(4):523–533. doi:10.1002/ar.1092240410

    CAS  PubMed  Google Scholar 

  74. Guerineau NC, McKinney RA, Debanne D, Mollard P, Gahwiler BH (1997) Organotypic cultures of the rat anterior pituitary: morphology, physiology and cell-to-cell communication. J Neurosci Methods 73(2):169–176

    CAS  PubMed  Google Scholar 

  75. Yamamoto T, Hossain MZ, Hertzberg EL, Uemura H, Murphy LJ, Nagy JI (1993) Connexin43 in rat pituitary: localization at pituicyte and stellate cell gap junctions and within gonadotrophs. Histochemistry 100(1):53–64

    CAS  PubMed  Google Scholar 

  76. Belluardo N, Mudo G, Trovato-Salinaro A, Le Gurun S, Charollais A, Serre-Beinier V, Amato G, Haefliger JA, Meda P, Condorelli DF (2000) Expression of connexin36 in the adult and developing rat brain. Brain Res 865(1):121–138

    CAS  PubMed  Google Scholar 

  77. Morand I, Fonlupt P, Guerrier A, Trouillas J, Calle A, Remy C, Rousset B, Munari-Silem Y (1996) Cell-to-cell communication in the anterior pituitary: evidence for gap junction-mediated exchanges between endocrine cells and folliculostellate cells. Endocrinology 137(8):3356–3367

    CAS  PubMed  Google Scholar 

  78. Guerineau NC, Bonnefont X, Stoeckel L, Mollard P (1998) Synchronized spontaneous Ca2+ transients in acute anterior pituitary slices. J Biol Chem 273(17):10389–10395

    CAS  PubMed  Google Scholar 

  79. Horiguchi K, Fujiwara K, Kouki T, Kikuchi M, Yashiro T (2008) Immunohistochemistry of connexin 43 throughout anterior pituitary gland in a transgenic rat with green fluorescent protein-expressing folliculo-stellate cells. Anat Sci Int 83(4):256–260. doi:10.1111/j.1447-073X.2008.00239.x

    CAS  PubMed  Google Scholar 

  80. Vitale ML, Cardin J, Gilula NB, Carbajal ME, Pelletier RM (2001) Dynamics of connexin 43 levels and distribution in the mink (Mustela vison) anterior pituitary are associated with seasonal changes in anterior pituitary prolactin content. Biol Reprod 64(2):625–633

    CAS  PubMed  Google Scholar 

  81. Stojilkovic SS (2001) A novel view of the function of pituitary folliculo-stellate cell network. Trends Endocrinol Metab 12(9):378–380

    CAS  PubMed  Google Scholar 

  82. Lewis BM, Pexa A, Francis K, Verma V, McNicol AM, Scanlon M, Deussen A, Evans WH, Rees DA, Ham J (2006) Adenosine stimulates connexin 43 expression and gap junctional communication in pituitary folliculostellate cells. FASEB J 20(14):2585–2587. doi:10.1096/fj.06-6121fje

    CAS  PubMed  Google Scholar 

  83. Castrique E, Fernandez-Fuente M, Le Tissier P, Herman A, Levy A (2012) Use of a prolactin-Cre/ROSA-YFP transgenic mouse provides no evidence for lactotroph transdifferentiation after weaning, or increase in lactotroph/somatotroph proportion in lactation. J Endocrinol 205(1):49–60. doi:10.1677/JOE-09-0414

    Google Scholar 

  84. Christian HC, Imirtziadis L, Tortonese D (2015) Ultrastructural changes in lactotrophs and folliculo-stellate cells in the ovine pituitary during the annual reproductive cycle. J Neuroendocrinol. doi:10.1111/jne.12261

    PubMed  Google Scholar 

  85. Winterhager E, Pielensticker N, Freyer J, Ghanem A, Schrickel JW, Kim JS, Behr R, Grummer R, Maass K, Urschel S, Lewalter T, Tiemann K, Simoni M, Willecke K (2007) Replacement of connexin43 by connexin26 in transgenic mice leads to dysfunctional reproductive organs and slowed ventricular conduction in the heart. BMC Dev Biol 7:26. doi:10.1186/1471-213X-7-26

    PubMed Central  PubMed  Google Scholar 

  86. Robinson ICAF, Hindmarsh PC (1999) The importance of the secretory pattern of growth hormone for statural growth. In: Kostyo JL (ed) Handbook of physiology. Section 7: The endocrine system, vol 5. Hormonal control of growth. Oxford University Press, New York, pp 329-395

  87. Raisman G, Field PM (1973) Sexual dimorphism in the neuropil of the preoptic area of the rat and its dependence on neonatal androgen. Brain Res 54:1–29

  88. McArthur S, Robinson IC, Gillies GE (2011) Novel ontogenetic patterns of sexual differentiation in arcuate nucleus GHRH neurons revealed in GHRH-enhanced green fluorescent protein transgenic mice. Endocrinology 152(2):607–617. doi:10.1210/en.2010-0798

    CAS  PubMed  Google Scholar 

  89. Waite E, Lafont C, Carmignac D, Chauvet N, Coutry N, Christian H, Robinson I, Mollard P, Le Tissier P (2010) Different degrees of somatotroph ablation compromise pituitary growth hormone cell network structure and other pituitary endocrine cell types. Endocrinology 151(1):234–243. doi:10.1210/en.2009-0539

    CAS  PubMed  Google Scholar 

  90. Li S, Bjelobaba I, Yan Z, Kucka M, Tomic M, Stojilkovic SS (2011) Expression and roles of pannexins in ATP release in the pituitary gland. Endocrinology 152(6):2342–2352. doi:10.1210/en.2010-1216

    CAS  PubMed Central  PubMed  Google Scholar 

  91. Sandilos JK, Bayliss DA (2012) Physiological mechanisms for the modulation of pannexin 1 channel activity. J Physiol 590(Pt 24):6257–6266. doi:10.1113/jphysiol.2012.240911

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Li S, Tomic M, Stojilkovic SS (2011) Characterization of novel Pannexin 1 isoforms from rat pituitary cells and their association with ATP-gated P2X channels. Gen Comp Endocrinol 174(2):202–210. doi:10.1016/j.ygcen.2011.08.019

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Tomic M, Jobin RM, Vergara LA, Stojilkovic SS (1996) Expression of purinergic receptor channels and their role in calcium signaling and hormone release in pituitary gonadotrophs. Integration of P2 channels in plasma membrane- and endoplasmic reticulum-derived calcium oscillations. J Biol Chem 271(35):21200–21208

    CAS  PubMed  Google Scholar 

  94. Koshimizu T, Tomic M, Van Goor F, Stojilkovic SS (1998) Functional role of alternative splicing in pituitary P2X2 receptor-channel activation and desensitization. Mol Endocrinol 12(7):901–913. doi:10.1210/mend.12.7.0129

    CAS  PubMed  Google Scholar 

  95. He ML, Gonzalez-Iglesias AE, Stojilkovic SS (2003) Role of nucleotide P2 receptors in calcium signaling and prolactin release in pituitary lactotrophs. J Biol Chem 278(47):46270–46277. doi:10.1074/jbc.M309005200

    CAS  PubMed  Google Scholar 

  96. Stojilkovic SS, Zemkova H (2013) P2X receptor channels in endocrine glands. Wiley Interdiscip Rev Membr Transp Signal 2(4):173–180. doi:10.1002/wmts.89

    CAS  PubMed Central  PubMed  Google Scholar 

  97. Daniel PM (1976) Anatomy of the hypothalamus and pituitary gland. J Clin Pathol Suppl (Assoc Clin Pathol) 7:1–7

    CAS  Google Scholar 

  98. Leng G, Brown CH, Russell JA (1999) Physiological pathways regulating the activity of magnocellular neurosecretory cells. Prog Neurobiol 57(6):625–655

    CAS  PubMed  Google Scholar 

  99. Brown CH, Bains JS, Ludwig M, Stern JE (2013) Physiological regulation of magnocellular neurosecretory cell activity: integration of intrinsic, local and afferent mechanisms. J Neuroendocrinol 25(8):678–710. doi:10.1111/jne.12051

    CAS  PubMed  Google Scholar 

  100. Hatton GI (1988) Pituicytes, glia and control of terminal secretion. J Exp Biol 139:67–79

    CAS  PubMed  Google Scholar 

  101. Arumugam H, Liu X, Colombo PJ, Corriveau RA, Belousov AB (2005) NMDA receptors regulate developmental gap junction uncoupling via CREB signaling. Nat Neurosci 8(12):1720–1726. doi:10.1038/nn1588

    CAS  PubMed  Google Scholar 

  102. Andrew RD, MacVicar BA, Dudek FE, Hatton GI (1981) Dye transfer through gap junctions between neuroendocrine cells of rat hypothalamus. Science 211(4487):1187–1189

    CAS  PubMed  Google Scholar 

  103. Yang QZ, Hatton GI (1988) Direct evidence for electrical coupling among rat supraoptic nucleus neurons. Brain Res 463(1):47–56

    CAS  PubMed  Google Scholar 

  104. Hatton GI, Yang QZ, Smithson KG (1988) Synaptic inputs and electrical coupling among magnocellular neuroendocrine cells. Brain Res Bull 20(6):751–755

    CAS  PubMed  Google Scholar 

  105. Westberg L, Sawa E, Wang AY, Gunaydin LA, Ribeiro AC, Pfaff DW (2009) Colocalization of connexin 36 and corticotropin-releasing hormone in the mouse brain. BMC Neurosci 10:41. doi:10.1186/1471-2202-10-41

    PubMed Central  PubMed  Google Scholar 

  106. Hosny S, Jennes L (1998) Identification of gap junctional connexin-32 mRNA and protein in gonadotropin-releasing hormone neurons of the female rat. Neuroendocrinology 67(2):101–108

    CAS  PubMed  Google Scholar 

  107. Tsukahara S, Maekawa F, Tsukamura H, Hirunagi K, Maeda K (1999) Morphological characterization of relationship between gap junctions and gonadotropin releasing hormone nerve terminals in the rat median eminence. Neurosci Lett 261(1–2):105–108

    CAS  PubMed  Google Scholar 

  108. Campbell RE, Ducret E, Porteous R, Liu X, Herde MK, Wellerhaus K, Sonntag S, Willecke K, Herbison AE (2011) Gap junctions between neuronal inputs but not gonadotropin-releasing hormone neurons control estrous cycles in the mouse. Endocrinology 152(6):2290–2301. doi:10.1210/en.2010-1311

    CAS  PubMed  Google Scholar 

  109. Allard C, Carneiro L, Grall S, Cline BH, Fioramonti X, Chretien C, Baba-Aissa F, Giaume C, Penicaud L, Leloup C (2014) Hypothalamic astroglial connexins are required for brain glucose sensing-induced insulin secretion. J Cereb Blood Flow Metab 34(2):339–346. doi:10.1038/jcbfm.2013.206

    CAS  PubMed Central  PubMed  Google Scholar 

  110. Duan L, Yuan H, Su CJ, Liu YY, Rao ZR (2004) Ultrastructure of junction areas between neurons and astrocytes in rat supraoptic nuclei. World J Gastroenterol 10(1):117–121

    PubMed  Google Scholar 

  111. Sohl G, Maxeiner S, Willecke K (2005) Expression and functions of neuronal gap junctions. Nat Rev Neurosci 6(3):191–200. doi:10.1038/nrn1627

    PubMed  Google Scholar 

  112. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247(4941):470–473

    CAS  PubMed  Google Scholar 

  113. Cobbett P, Hatton GI (1984) Dye coupling in hypothalamic slices: dependence on in vivo hydration state and osmolality of incubation medium. J Neurosci 4(12):3034–3038

    CAS  PubMed  Google Scholar 

  114. Micevych PE, Popper P, Hatton GI (1996) Connexin 32 mRNA levels in the rat supraoptic nucleus: up-regulation prior to parturition and during lactation. Neuroendocrinology 63(1):39–45

    CAS  PubMed  Google Scholar 

  115. Hatton GI, Yang QZ, Cobbett P (1987) Dye coupling among immunocytochemically identified neurons in the supraoptic nucleus: increased incidence in lactating rats. Neuroscience 21(3):923–930

    CAS  PubMed  Google Scholar 

  116. Hatton GI, Yang QZ (1994) Incidence of neuronal coupling in supraoptic nuclei of virgin and lactating rats: estimation by neurobiotin and lucifer yellow. Brain Res 650(1):63–69

    CAS  PubMed  Google Scholar 

  117. Cobbett P, Yang QZ, Hatton GI (1987) Incidence of dye coupling among magnocellular paraventricular nucleus neurons in male rats is testosterone dependent. Brain Res Bull 18(3):365–370

    CAS  PubMed  Google Scholar 

  118. Hatton GI, Yang QZ, Koran LE (1992) Effects of ovariectomy and estrogen replacement on dye coupling among rat supraoptic nucleus neurons. Brain Res 572(1–2):291–295

    CAS  PubMed  Google Scholar 

  119. Orellana JA, Saez PJ, Cortes-Campos C, Elizondo RJ, Shoji KF, Contreras-Duarte S, Figueroa V, Velarde V, Jiang JX, Nualart F, Saez JC, Garcia MA (2012) Glucose increases intracellular free Ca(2 +) in tanycytes via ATP released through connexin 43 hemichannels. Glia 60(1):53–68. doi:10.1002/glia.21246

    PubMed Central  PubMed  Google Scholar 

  120. Giaume C, Leybaert L, Naus CC, Saez JC (2013) Connexin and pannexin hemichannels in brain glial cells: properties, pharmacology, and roles. Front Pharmacol 4:88. doi:10.3389/fphar.2013.00088

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Langlet F, Levin BE, Luquet S, Mazzone M, Messina A, Dunn-Meynell AA, Balland E, Lacombe A, Mazur D, Carmeliet P, Bouret SG, Prevot V, Dehouck B (2013) Tanycytic VEGF-A boosts blood-hypothalamus barrier plasticity and access of metabolic signals to the arcuate nucleus in response to fasting. Cell Metab 17(4):607–617. doi:10.1016/j.cmet.2013.03.004

    CAS  PubMed Central  PubMed  Google Scholar 

  122. Jiang S, Yuan H, Duan L, Cao R, Gao B, Xiong YF, Rao ZR (2011) Glutamate release through connexin 43 by cultured astrocytes in a stimulated hypertonicity model. Brain Res 1392:8–15. doi:10.1016/j.brainres.2011.03.056

    CAS  PubMed  Google Scholar 

  123. Ye ZC, Wyeth MS, Baltan-Tekkok S, Ransom BR (2003) Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci 23(9):3588–3596

    CAS  PubMed  Google Scholar 

  124. Yuan H, Duan L, Qiu Y, Gao LZ, Zhang P, Cao R, Rao ZR (2004) Response of son astrocytes and neurons to hyperosmotic stimulation after carbenoxolone injection into the lateral ventricle. Acta Anatomica Sinica 35:127–131

    CAS  Google Scholar 

  125. Ray A, Zoidl G, Weickert S, Wahle P, Dermietzel R (2005) Site-specific and developmental expression of pannexin1 in the mouse nervous system. Eur J Neurosci 21(12):3277–3290. doi:10.1111/j.1460-9568.2005.04139.x

    PubMed  Google Scholar 

  126. Ohbuchi T, Yokoyama T, Saito T, Ohkubo J, Suzuki H, Ishikura T, Katoh A, Fujihara H, Hashimoto H, Ueta Y (2011) Possible contribution of pannexin channel to ATP-induced currents in vitro in vasopressin neurons isolated from the rat supraoptic nucleus. Brain Res 1394:71–78. doi:10.1016/j.brainres.2011.04.017

    CAS  PubMed  Google Scholar 

  127. Maronde E, Stehle JH (2007) The mammalian pineal gland: known facts, unknown facets. Trends Endocrinol Metab 18(4):142–149. doi:10.1016/j.tem.2007.03.001

    CAS  PubMed  Google Scholar 

  128. Berthoud VM, Hall DH, Strahsburger E, Beyer EC, Saez JC (2000) Gap junctions in the chicken pineal gland. Brain Res 861(2):257–270

    CAS  PubMed  Google Scholar 

  129. Krstic R (1974) Ultrastructure of rat pineal gland after preparation by freeze-etching technique. Cell Tissue Res 148(3):371–379

    CAS  PubMed  Google Scholar 

  130. Taugner R, Schiller A, Rix E (1981) Gap junctions between pinealocytes. A freeze-fracture study of the pineal gland in rats. Cell Tissue Res 218(2):303–314

    CAS  PubMed  Google Scholar 

  131. Condorelli DF, Belluardo N, Trovato-Salinaro A, Mudo G (2000) Expression of Cx36 in mammalian neurons. Brain Res Brain Res Rev 32(1):72–85

    CAS  PubMed  Google Scholar 

  132. Huang SK, Taugner R (1984) Gap junctions between guinea-pig pinealocytes. Cell Tissue Res 235(1):137–141

    CAS  PubMed  Google Scholar 

  133. Ichimura T (1992) The ultrastructure of neuronal-pinealocytic interconnections in the monkey pineal. Microsc Res Tech 21(2):124–135. doi:10.1002/jemt.1070210205

    CAS  PubMed  Google Scholar 

  134. Moller M (1976) The ultrastructure of the human fetal pineal gland. II. Innervation and cell junctions. Cell Tissue Res 169(1):7–21

    CAS  PubMed  Google Scholar 

  135. Cieciura L, Krakowski G (1991) Junctional systems in the pineal gland of the Wistar rat (Ratus ratus). A freeze-fracture and thin section study. J Submicrosc Cytol Pathol 23(2):327–330

    CAS  PubMed  Google Scholar 

  136. Berthoud VM, Saez JC (1993) Changes in connexin43, the gap junction protein of astrocytes, during development of the rat pineal gland. J Pineal Res 14(2):67–72

    CAS  PubMed  Google Scholar 

  137. Saez JC, Berthoud VM, Kadle R, Traub O, Nicholson BJ, Bennett MV, Dermietzel R (1991) Pinealocytes in rats: connexin identification and increase in coupling caused by norepinephrine. Brain Res 568(1–2):265–275

    CAS  PubMed  Google Scholar 

  138. Schenda J, Vollrath L (1999) An intrinsic neuronal-like network in the rat pineal gland. Brain Res 823(1–2):231–233

    CAS  PubMed  Google Scholar 

  139. Giaume C, Tabernero A, Medina JM (1997) Metabolic trafficking through astrocytic gap junctions. Glia 21(1):114–123

    CAS  PubMed  Google Scholar 

  140. Benarroch EE (2005) Neuron-astrocyte interactions: partnership for normal function and disease in the central nervous system. Mayo Clin Proc 80(10):1326–1338. doi:10.4065/80.10.1326

    CAS  PubMed  Google Scholar 

  141. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322(5907):1551–1555. doi:10.1126/science.1164022

    CAS  PubMed  Google Scholar 

  142. Lin H, Mitasikova M, Dlugosova K, Okruhlicova L, Imanaga I, Ogawa K, Weismann P, Tribulova N (2008) Thyroid hormones suppress epsilon-PKC signalling, down-regulate connexin-43 and increase lethal arrhythmia susceptibility in non-diabetic and diabetic rat hearts. J Physiol Pharmacol 59(2):271–285

    CAS  PubMed  Google Scholar 

  143. Almeida NA, Cordeiro A, Machado DS, Souza LL, Ortiga-Carvalho TM, Campos-de-Carvalho AC, Wondisford FE, Pazos-Moura CC (2009) Connexin40 messenger ribonucleic acid is positively regulated by thyroid hormone (TH) acting in cardiac atria via the TH receptor. Endocrinology 150(1):546–554. doi:10.1210/en.2008-0451

    CAS  PubMed  Google Scholar 

  144. Mitasikova M, Lin H, Soukup T, Imanaga I, Tribulova N (2009) Diabetes and thyroid hormones affect connexin-43 and PKC-epsilon expression in rat heart atria. Physiol Res 58(2):211–217

    CAS  PubMed  Google Scholar 

  145. Potter E, Schoenermark M, Bock O, Hoang-Vu C, Munari-Silem Y, Rousset B, Brabant G (1996) Cell adhesion receptors and gap junctions in normal and neoplastic transformed thyrocytes. Exp Clin Endocrinol Diabetes 104(Suppl 4):24–28. doi:10.1055/s-0029-1211695

    PubMed  Google Scholar 

  146. Darr EA, Patel AD, Yu G, Komorowski Z, McCormick S, Tiwari R, Schantz SP, Geliebter J (2011) Reduced Cx43 gap junction plaque expression differentiates thyroid carcinomas from benign disease. Arch Otolaryngol Head Neck Surg 137(11):1161–1165. doi:10.1001/archoto.2011.186

    PubMed  Google Scholar 

  147. Dominguez C, Karayan-Tapon L, Desurmont T, Gibelin H, Crespin S, Fromont G, Levillain P, Bouche G, Cantereau A, Mesnil M, Kraimps JL (2011) Altered expression of the gap junction protein connexin43 is associated with papillary thyroid carcinomas when compared with other noncancer pathologies of the thyroid. Thyroid 21(10):1057–1066. doi:10.1089/thy.2011.0041

    CAS  PubMed  Google Scholar 

  148. Guerrier A, Fonlupt P, Morand I, Rabilloud R, Audebet C, Krutovskikh V, Gros D, Rousset B, Munari-Silem Y (1995) Gap junctions and cell polarity: connexin32 and connexin43 expressed in polarized thyroid epithelial cells assemble into separate gap junctions, which are located in distinct regions of the lateral plasma membrane domain. J Cell Sci 108(Pt 7):2609–2617

    CAS  PubMed  Google Scholar 

  149. Munari-Silem Y, Guerrier A, Fromaget C, Rabilloud R, Gros D, Rousset B (1994) Differential control of connexin-32 and connexin-43 expression in thyroid epithelial cells: evidence for a direct relationship between connexin-32 expression and histiotypic morphogenesis. Endocrinology 135(2):724–734. doi:10.1210/endo.135.2.8033821

    CAS  PubMed  Google Scholar 

  150. Kostrouch Z, Bernier-Valentin F, Munari-Silem Y, Rajas F, Rabilloud R, Rousset B (1993) Thyroglobulin molecules internalized by thyrocytes are sorted in early endosomes and partially recycled back to the follicular lumen. Endocrinology 132(6):2645–2653. doi:10.1210/endo.132.6.8504765

    CAS  PubMed  Google Scholar 

  151. Setoguti T, Inoue Y, Suematsu T (1982) Intercellular junctions of the hen parathyroid gland. A freeze-fracture study. J Anat 135(Pt 2):395–406

    CAS  PubMed Central  PubMed  Google Scholar 

  152. Green ST (1988) The electrophysiological properties of the parathyroid cell: results of a study employing Sprague-Dawley rats and a review of the literature. Biomed Pharmacother 42(1):61–64

    CAS  PubMed  Google Scholar 

  153. Tonoli H, Flachon V, Audebet C, Calle A, Jarry-Guichard T, Statuto M, Rousset B, Munari-Silem Y (2000) Formation of three-dimensional thyroid follicle-like structures by polarized FRT cells made communication competent by transfection and stable expression of the connexin-32 gene. Endocrinology 141(4):1403–1413. doi:10.1210/endo.141.4.7400

    CAS  PubMed  Google Scholar 

  154. Statuto M, Audebet C, Tonoli H, Selmi-Ruby S, Rousset B, Munari-Silem Y (1997) Restoration of cell-to-cell communication in thyroid cell lines by transfection with and stable expression of the connexin-32 gene. Impact on cell proliferation and tissue-specific gene expression. J Biol Chem 272(39):24710–24716

    CAS  PubMed  Google Scholar 

  155. Flachon V, Tonoli H, Selmi-Ruby S, Durand C, Rabilloud R, Rousset B, Munari-Silem Y (2002) Thyroid cell proliferation in response to forced expression of gap junction proteins. Eur J Cell Biol 81(5):243–252. doi:10.1078/0171-9335-00245

    CAS  PubMed  Google Scholar 

  156. Prost G, Bernier-Valentin F, Munari-Silem Y, Selmi-Ruby S, Rousset B (2008) Connexin-32 acts as a downregulator of growth of thyroid gland. Am J Physiol Endocrinol Metab 294(2):E291–E299. doi:10.1152/ajpendo.00281.2007

    CAS  PubMed  Google Scholar 

  157. Cigliola V, Chellakudam V, Arabieter W, Meda P (2013) Connexins and beta-cell functions. Diabetes Res Clin Pract 99(3):250–259. doi:10.1016/j.diabres.2012.10.016

    CAS  PubMed  Google Scholar 

  158. 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(7):1700–1707. doi:10.2337/db11-1312

    CAS  PubMed Central  PubMed  Google Scholar 

  159. Pointis G, Fiorini C, Gilleron J, Carette D, Segretain D (2007) Connexins as precocious markers and molecular targets for chemical and pharmacological agents in carcinogenesis. Curr Med Chem 14(21):2288–2303

    CAS  PubMed  Google Scholar 

  160. DeVries SH, Schwartz EA (1992) Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. J Physiol 445:201–230

    CAS  PubMed Central  PubMed  Google Scholar 

  161. Bruzzone R, Hormuzdi SG, Barbe MT, Herb A, Monyer H (2003) Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci USA 100(23):13644–13649. doi:10.1073/pnas.2233464100

    CAS  PubMed Central  PubMed  Google Scholar 

  162. 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(4):511–525. doi:10.1002/cne.20085

    CAS  PubMed  Google Scholar 

  163. Li X, Olson C, Lu S, Nagy JI (2004) Association of connexin36 with zonula occludens-1 in HeLa cells, betaTC-3 cells, pancreas, and adrenal gland. Histochem Cell Biol 122(5):485–498. doi:10.1007/s00418-004-0718-5

    CAS  PubMed  Google Scholar 

  164. Nassar-Gentina V, Pollard HB, Rojas E (1988) Electrical activity in chromaffin cells of intact mouse adrenal gland. Am J Physiol 254(5 Pt 1):C675–C683

    CAS  PubMed  Google Scholar 

  165. Moser T (1998) Low-conductance intercellular coupling between mouse chromaffin cells in situ. J Physiol 506(Pt 1):195–205

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We apologize to the many authors whose excellent papers could not be cited in this review because of space limitations. D.J.H. was supported by a Diabetes UK R.D. Lawrence Research Fellowship (12/0004431).

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationship that could be construed as a potential conflict of interest.

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Authors and Affiliations

  1. Section of Cell Biology and Functional Genomics, Department of Medicine, Imperial College London, London, W12 0NN, UK

    David J. Hodson

  2. Department of Integrated Neurovascular and Mitochondrial Biology, Angers, France

    Christian Legros

  3. CNRS UMR6214, Angers, France

    Christian Legros

  4. INSERM U1083, Angers, France

    Christian Legros

  5. University of Angers, Angers, France

    Christian Legros

  6. CNRS, UMR5203, Institut de Génomique Fonctionnelle, 141 rue de la Cardonille, 34094, Montpellier Cedex 5, France

    Michel G. Desarménien & Nathalie C. Guérineau

  7. INSERM, U1191, 34094, Montpellier, France

    Michel G. Desarménien & Nathalie C. Guérineau

  8. University of Montpellier, 34094, Montpellier, France

    Michel G. Desarménien & Nathalie C. Guérineau

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  1. David J. Hodson
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  2. Christian Legros
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  4. Nathalie C. Guérineau
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Correspondence to Nathalie C. Guérineau.

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Hodson, D.J., Legros, C., Desarménien, M.G. et al. Roles of connexins and pannexins in (neuro)endocrine physiology. Cell. Mol. Life Sci. 72, 2911–2928 (2015). https://doi.org/10.1007/s00018-015-1967-2

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