Coordination of calcium signals by pituitary endocrine cells in situ

Cell Calcium

Volumn 51, Issue 3-4, 2012, Pages 222-230

  Hodson, David J ^a,b   Romanò, Nicola ^a,b   Schaeffer, Marie ^a,b,c   Fontanaud, Pierre ^a,b   Lafont, Chrystel ^a,b   Fiordelisio, Tatiana ^a,b,d   Mollard, Patrice ^a,b  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b UNIV MONTPELLIER   (France)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Calcium; Endocrinology; Gap junction; Imaging; Network; Pituitary; Systems biology

Indexed keywords

CALCIUM ION; G PROTEIN COUPLED RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE; VOLTAGE GATED CALCIUM CHANNEL;

ACTH SECRETING CELL; ACTION POTENTIAL; ARTICLE; BLOOD FLOW; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL COMMUNICATION; CELL POPULATION; ENDOCRINE CELL; EXOCYTOSIS; EXTRACELLULAR MATRIX; GAP JUNCTION; GONADOTROPIN SECRETING CELL; GROWTH HORMONE SECRETING CELL; HORMONE RELEASE; HYPOPHYSIS CELL; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROLACTIN SECRETING CELL; TSH SECRETING CELL;

MAMMALIA;

EID: 84858282498     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2011.11.007     Document Type: Article

References (124)

1. Robinson I.C.A.F., Hindmarsh P.C. The importance of the secretory pattern of growth hormone for statural growth. Handbook of Physiology 1999, 329-395. Oxford University Press, New York. J.L. Kostyo (Ed.).
2. Bonnefont X., Lacampagne A., Sanchez-Hormigo A., Fino E., Creff A., Mathieu M.N., Smallwood S., Carmignac D., Fontanaud P., Travo P., Alonso G., Courtois-Coutry N., Pincus S.M., Robinson I.C., Mollard P. Revealing the large-scale network organization of growth hormone-secreting cells. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:16880-16885.
3. Chauvet N., El-Yandouzi T., Mathieu M.N., Schlernitzauer A., Galibert E., Lafont C., Le Tissier P., Robinson I.C., Mollard P., Coutry N. Characterization of adherens junction protein expression and localization in pituitary cell networks. J. Endocrinol. 2009, 202:375-387.
4. Sanchez-Cardenas C., Fontanaud P., He Z., Lafont C., Meunier A.C., Schaeffer M., Carmignac D., Molino F., Coutry N., Bonnefont X., Gouty-Colomer L.A., Gavois E., Hodson D.J., Le Tissier P., Robinson I.C., Mollard P. Pituitary growth hormone network responses are sexually dimorphic and regulated by gonadal steroids in adulthood. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:21878-21883.
5. Hodson D.J., Molino F., Fontanaud P., Bonnefont X., Mollard P. Investigating and modelling pituitary endocrine network function. J. Neuroendocrinol. 2010, 22:1217-1225.
6. Budry L., Lafont C., El Yandouzi T., Chauvet N., Conejero G., Drouin J., Mollard P. Related pituitary cell lineages develop into interdigitated 3D cell networks. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:12515-12520.
7. Schaeffer M., Hodson D.J., Meunier A.C., Lafont C., Birkenstock J., Carmignac D., Murray J.F., Gavois E., Robinson I.C., Le Tissier P., Mollard P. Influence of estrogens on GH-cell network dynamics in females: a live in situ imaging approach. Endocrinology 2011, 152:4789-4799.
8. Tannenbaum G.S., Martin J.B., Colle E. Ultradian growth hormone rhythm in the rat: effects of feeding, hyperglycemia, and insulin-induced hypoglycemia. Endocrinology 1976, 99:720-727.
9. Sartor O., Bowers C.Y., Chang D. Parallel studies of His-DTrp-Ala-Trp-DPhe-Lys-NH2 and human pancreatic growth hormone-releasing factor-44-NH2 in rat primary pituitary cell monolayer culture. Endocrinology 1985, 116:952-957.
10. Mollard P., Schlegel W. Why are endocrine pituitary cells excitable?. Trends Endocrinol. Metab. 1996, 7:361-365.
11. Bonnefont X., Fiekers J., Creff A., Mollard P. Rhythmic bursts of calcium transients in acute anterior pituitary slices. Endocrinology 2000, 141:868-875.
12. Van Goor F., Zivadinovic D., Martinez-Fuentes A.J., Stojilkovic S.S. Dependence of pituitary hormone secretion on the pattern of spontaneous voltage-gated calcium influx. Cell type-specific action potential secretion coupling. J. Biol. Chem. 2001, 276:33840-33846.
13. Stojilkovic S.S., Catt K.J. Calcium oscillations in anterior pituitary cells. Endocr. Rev. 1992, 13:256-280.
14. 2+ in pituitary cells due to action potentials. Nature 1987, 329:719-721.
15. Li Y.X., Rinzel J., Vergara L., Stojilkovic S.S. Spontaneous electrical and calcium oscillations in unstimulated pituitary gonadotrophs. Biophys. J. 1995, 69:785-795.
16. Li Y.X., Stojilkovic S.S., Keizer J., Rinzel J. Sensing and refilling calcium stores in an excitable cell. Biophys. J. 1997, 72:1080-1091.
17. Ben-Jonathan N., Hnasko R. Dopamine as a prolactin (PRL) inhibitor. Endocr. Rev. 2001, 22:724-763.
18. 2+ signaling-secretion coupling. Trends Endocrinol. Metab. 2005, 16:152-159.
19. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature 1993, 361:315-325.
20. Stojilkovic S.S., Reinhart J., Catt K.J. Gonadotropin-releasing hormone receptors: structure and signal transduction pathways. Endocr. Rev. 1994, 15:462-499.
21. Kaiser U.B., Conn P.M., Chin W.W. Studies of gonadotropin-releasing hormone (GnRH) action using GnRH receptor-expressing pituitary cell lines. Endocr. Rev. 1997, 18:46-70.
22. Ashworth R., Hinkle P.M. Thyrotropin-releasing hormone-induced intracellular calcium responses in individual rat lactotrophs and thyrotrophs. Endocrinology 1996, 137:5205-5212.
23. Petit A., Bleicher C., Lussier B.T. Intracellular calcium stores are involved in growth hormone-releasing hormone signal transduction in rat somatotrophs. Can. J. Physiol. Pharmacol. 1999, 77:520-528.
24. Yamamori E., Iwasaki Y., Oki Y., Yoshida M., Asai M., Kambayashii M., Oiso Y., Nakashima N. Possible involvement of ryanodine receptor-mediated intracellular calcium release in the effect of corticotropin-releasing factor on adrenocorticotropin secretion. Endocrinology 2004, 145:36-38.
25. Corcuff J.B., Guerineau N.C., Mariot P., Lussier B.T., Mollard P. Multiple cytosolic calcium signals and membrane electrical events evoked in single arginine vasopressin-stimulated corticotrophs. J. Biol. Chem. 1993, 268:22313-22321.
26. Lachowicz A., Van Goor F., Katzur A.C., Bonhomme G., Stojilkovic S.S. Uncoupling of calcium mobilization and entry pathways in endothelin-stimulated pituitary lactotrophs. J. Biol. Chem. 1997, 272:28308-28314.
27. Zhu H., Hille B., Xu T. Sensitization of regulated exocytosis by protein kinase C. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:17055-17059.
28. 2+ currents sensitive to dihydropyridines. J. Biol. Chem. 1994, 269:25158-25164.
29. 2+ oscillations. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:9750-9754.
30. Kaftan E.J., Xu T., Abercrombie R.F., Hille B. Mitochondria shape hormonally induced cytoplasmic calcium oscillations and modulate exocytosis. J. Biol. Chem. 2000, 275:25465-25470.
31. Tse A., Tse F.W., Almers W., Hille B. Rhythmic exocytosis stimulated by GnRH-induced calcium oscillations in rat gonadotropes. Science 1993, 260:82-84.
32. Tse A., Tse F.W., Hille B. Calcium homeostasis in identified rat gonadotrophs. J. Physiol. 1994, 477(Pt 3):511-525.
33. Lledo P.M., Somasundaram B., Morton A.J., Emson P.C., Mason W.T. Stable transfection of calbindin-D28k into the GH3 cell line alters calcium currents and intracellular calcium homeostasis. Neuron 1992, 9:943-954.
34. Stojilkovic S.S., Tabak J., Bertram R. Ion channels and signaling in the pituitary gland. Endocr. Rev. 2010, 31:845-915.
35. Neher E., Marty A. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:6712-6716.
36. McGuinness L., Magoulas C., Sesay A.K., Mathers K., Carmignac D., Manneville J.B., Christian H., Phillips J.A., Robinson I.C. Autosomal dominant growth hormone deficiency disrupts secretory vesicles in vitro and in vivo in transgenic mice. Endocrinology 2003, 144:720-731.
37. 2+ signalling: dense core granule exocytosis viewed by total internal reflection fluorescence microscopy. Methods 2008, 46:233-238.
38. Berridge M.J., Bootman M.D., Lipp P. Calcium-a life and death signal. Nature 1998, 395:645-648.
39. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 2000, 1:11-21.
40. Peterlin Z.A., Kozloski J., Mao B.Q., Tsiola A., Yuste R. Optical probing of neuronal circuits with calcium indicators. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:3619-3624.
41. Ikegaya Y., Aaron G., Cossart R., Aronov D., Lampl I., Ferster D., Yuste R. Synfire chains and cortical songs: temporal modules of cortical activity. Science 2004, 304:559-564.
42. Cossart R., Ikegaya Y., Yuste R. Calcium imaging of cortical networks dynamics. Cell Calcium 2005, 37:451-457.
43. Bonifazi P., Goldin M., Picardo M.A., Jorquera I., Cattani A., Bianconi G., Represa A., Ben-Ari Y., Cossart R. GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 2009, 326:1419-1424.
44. Waite E., Lafont C., Carmignac D., Chauvet N., Coutry N., Christian H., Robinson I., Mollard P., Le Tissier P. Different degrees of somatotroph ablation compromise pituitary growth hormone cell network structure and other pituitary endocrine cell types. Endocrinology 2010, 151:234-243.
45. Schwartz J. Intercellular communication in the anterior pituitary. Endocr. Rev. 2000, 21:488-513.
46. Denef C. Paracrinicity: the story of 30 years of cellular pituitary crosstalk. J. Neuroendocrinol. 2008, 20:1-70.
47. Stojilkovic S.S., Merelli F., Iida T., Krsmanovic L.Z., Catt K.J. Endothelin stimulation of cytosolic calcium and gonadotropin secretion in anterior pituitary cells. Science 1990, 248:1663-1666.
48. Kanyicska B., Burris T.P., Freeman M.E. The effects of endothelins on the secretion of prolactin, luteinizing hormone, and follicle-stimulating hormone are mediated by different guanine nucleotide-binding proteins. Endocrinology 1991, 129:2607-2613.
49. Tomic M., Zivadinovic D., Van Goor F., Yuan D., Koshimizu T., Stojilkovic S.S. Expression of Ca(2+)-mobilizing endothelin(A) receptors and their role in the control of Ca(2+) influx and growth hormone secretion in pituitary somatotrophs. J. Neurosci. 1999, 19:7721-7731.
50. Kanyicska B., Lerant A., Freeman M.E. Endothelin-like immunoreactivity in lactotrophs, gonadotrophs, and somatotrophs of rat anterior pituitary gland are affected differentially by ovarian steroid hormones. Endocrine 2001, 14:263-268.
51. Steger R.W, Bartke A., Parkening T.A., Collins T., Buonomo F.C., Tang K.C., Wagner T.E., Yun J.S. Effects of heterologous growth hormones on hypothalamic and pituitary function in transgenic mice. Neuroendocrinology 1991, 53:365-372.
52. Tang K., Bartke A., Gardiner C.S., Wagner T.E., Yun J.S. Gonadotropin secretion, synthesis, and gene expression in two types of bovine growth hormone transgenic mice. Biol. Reprod. 1993, 49:346-353.
53. Mertani H.C., Waters M.J., Jambou R., Gossard F., Morel G. Growth hormone receptor binding protein in rat anterior pituitary. Neuroendocrinology 1994, 59:483-494.
54. Tortonese D.J., Brooks J., Ingleton P.M., McNeilly A.S. Detection of prolactin receptor gene expression in the sheep pituitary gland and visualization of the specific translation of the signal in gonadotrophs. Endocrinology 1998, 139:5215-5223.
55. Hodson D.J., Townsend J., Gregory S.J., Walters C., Tortonese D.J. Role of prolactin in the gonadotroph responsiveness to gonadotrophin-releasing hormone during the equine annual reproductive cycle. J. Neuroendocrinol. 2010, 22:509-517.
56. Hodson D.J., Townsend J., Tortonese D.J. Characterization of the effects of prolactin in gonadotroph target cells. Biol. Reprod. 2010, 83:1046-1055.
57. Andric S.A., Kostic T.S., Tomic M., Koshimizu T., Stojilkovic S.S. Dependence of soluble guanylyl cyclase activity on calcium signaling in pituitary cells. J. Biol. Chem. 2001, 276:844-849.
58. Tsumori M., Murakami Y., Koshimura K., Kato Y. Growth hormone-releasing hormone and gonadotropin-releasing hormone stimulate nitric oxide production in 17beta-estradiol-primed rat anterior pituitary cells. Endocrine 2002, 17:215-218.
59. Hokfelt T., Ceccatelli S., Gustafsson L., Hulting A.L., Verge V., Villar M., Xu X.J., Xu Z.Q., Wiesenfeld-Hallin Z., Zhang X. Plasticity of NO synthase expression in the nervous and endocrine systems. Neuropharmacology 1994, 33:1221-1227.
60. Duvilanski B.H., Zambruno C., Seilicovich A., Pisera D., Lasaga M., Diaz M.C., Belova N., Rettori V., McCann S.M. Role of nitric oxide in control of prolactin release by the adenohypophysis. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:170-174.
61. Kostic T.S., Andric S.A., Stojilkovic S.S. Spontaneous and receptor-controlled soluble guanylyl cyclase activity in anterior pituitary cells. Mol. Endocrinol. 2001, 15:1010-1022.
62. Brown E., McKee T., diTomaso E., Pluen A., Seed B., Boucher Y., Jain R.K. Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat. Med. 2003, 9:796-800.
63. Perentes J.Y., McKee T.D., Ley C.D., Mathiew H., Dawson M., Padera T.P., Munn L.L., Jain R.K., Boucher Y. In vivo imaging of extracellular matrix remodeling by tumor-associated fibroblasts. Nat. Methods 2009, 6:143-145.
64. Chapman L., Nishimura A., Buckingham J.C., Morris J.F., Christian H.C. Externalization of annexin I from a folliculo-stellate-like cell line. Endocrinology 2002, 143:4330-4338.
65. Tierney T., Christian H.C., Morris J.F., Solito E., Buckingham J.C. Evidence from studies on co-cultures of TtT/GF and AtT20 cells that annexin 1 acts as a paracrine or juxtacrine mediator of the early inhibitory effects of glucocorticoids on ACTH release. J. Neuroendocrinol. 2003, 15:1134-1143.
66. Christian H.C., Flower R.J., Morris J.F., Buckingham J.C. Localisation and semi-quantitative measurement of lipocortin 1 in rat anterior pituitary cells by fluorescence-activated cell analysis/sorting and electron microscopy. J. Neuroendocrinol. 1999, 11:707-714.
67. Christian H.C., Taylor A.D., Flower R.J., Morris J.F., Buckingham J.C. Characterization and localization of lipocortin 1-binding sites on rat anterior pituitary cells by fluorescence-activated cell analysis/sorting and electron microscopy. Endocrinology 1997, 138:5341-5351.
68. Taylor A.D., Philip J.G., John C.D., Cover P.O., Morris J.F., Flower R.J., Buckingham J.C. Annexin 1 (lipocortin 1) mediates the glucocorticoid inhibition of cyclic adenosine 3',5'-monophosphate-stimulated prolactin secretion. Endocrinology 2000, 141:2209-2219.
69. Taylor A.D., Christian H.C., Morris J.F., Flower R.J., Buckingham J.C. Evidence from immunoneutralization and antisense studies that the inhibitory actions of glucocorticoids on growth hormone release in vitro require annexin 1, lipocortin 1. Br. J. Pharmacol. 2000, 131:1309-1316.
70. John C.D., Christian H.C., Morris J.F., Flower R.J., Solito E., Buckingham J.C. Annexin 1 and the regulation of endocrine function. Trends Endocrinol. Metab. 2004, 15:103-109.
71. Laird D.W., Puranam K.L., Revel J.P. Turnover and phosphorylation dynamics of connexin43 gap junction protein in cultured cardiac myocytes. Biochem. J. 1991, 273(Pt 1):67-72.
72. Beardslee M.A., Laing J.G., Beyer E.C., Saffitz J.E. Rapid turnover of connexin43 in the adult rat heart. Circ. Res. 1998, 83:629-635.
73. Lampe P.D., Lau A.F. The effects of connexin phosphorylation on gap junctional communication. Int. J. Biochem. Cell Biol. 2004, 36:1171-1186.
74. Verselis V.K., Bennett M.V., Bargiello T.A. A voltage-dependent gap junction in Drosophila melanogaster. Biophys. J. 1991, 59:114-126.
75. Moreno A.P., Saez J.C., Fishman G.I., Spray D.C. Human connexin43 gap junction channels. Regulation of unitary conductances by phosphorylation. Circ. Res. 1994, 74:1050-1057.
76. 2+ influx inhibits cell coupling. Nat. Methods 2005, 2:55-62.
77. Meda P., Pepper M.S., Traub O., Willecke K., Gros D., Beyer E., Nicholson B., Paul D., Orci L. Differential expression of gap junction connexins in endocrine and exocrine glands. Endocrinology 1993, 133:2371-2378.
78. Yamamoto T., Hossain M.Z., Hertzberg E.L., Uemura H., Murphy L.J., Nagy J.I. Connexin43 in rat pituitary: localization at pituicyte and stellate cell gap junctions and within gonadotrophs. Histochemistry 1993, 100:53-64.
79. Belluardo N., Mudo G., Trovato-Salinaro A., Le Gurun S., Charollais A., Serre-Beinier V., Amato G., Haefliger J.A., Meda P., Condorelli D.F. Expression of connexin36 in the adult and developing rat brain. Brain Res. 2000, 865:121-138.
80. Vitale M.L., Cardin J., Gilula N.B., Carbajal M.E., Pelletier R.M. 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. 2001, 64:625-633.
81. Shirasawa N., Mabuchi Y., Sakuma E., Horiuchi O., Yashiro T., Kikuchi M., Hashimoto Y., Tsuruo Y., Herbert D.C., Soji T. Intercellular communication within the rat anterior pituitary gland: X. Immunohistocytochemistry of S-100 and connexin 43 of folliculo-stellate cells in the rat anterior pituitary gland. Anat. Rec. 2004, 278A:462-473.
82. Fortin M.E., Pelletier R.M., Meilleur M.A., Vitale M.L. Modulation of GJA1 turnover and intercellular communication by proinflammatory cytokines in the anterior pituitary folliculostellate cell line TtT/GF. Biol. Reprod. 2006, 74:2-12.
83. Serre-Beinier V., Mas C., Calabrese A., Caton D., Bauquis J., Caille D., Charollais A., Cirulli V., Meda P. Connexins and secretion. Biol. Cell. 2002, 94:477-492.
84. Yamasaki S., Sakata-Sogawa K., Hasegawa A., Suzuki T., Kabu K., Sato E., Kurosaki T., Yamashita S., Tokunaga M., Nishida K., Hirano T. Zinc is a novel intracellular second messenger. J. Cell Biol. 2007, 177:637-645.
85. Nicolson T.J., Bellomo E.A., Wijesekara N., Loder M.K., Baldwin J.M., Gyulkhandanyan A.V., Koshkin V., Tarasov A.I., Carzaniga R., Kronenberger K., Taneja T.K., da Silva Xavier G., Libert S., Froguel P., Scharfmann R., Stetsyuk V., Ravassard P., Parker H., Gribble F.M., Reimann F., Sladek R., Hughes S.J., Johnson P.R., Masseboeuf M., Burcelin R., Baldwin S.A., Liu M., Lara-Lemus R., Arvan P., Schuit F.C., Wheeler M.B., Chimienti F., Rutter G.A. Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 2009, 58:2070-2083.
86. Lemaire K., Ravier M.A., Schraenen A., Creemers J.W., Van de Plas R., Granvik M., Van Lommel L., Waelkens E., Chimienti F., Rutter G.A., Gilon P., in't Veld P.A., Schuit F.C. Insulin crystallization depends on zinc transporter ZnT8 expression, but is not required for normal glucose homeostasis in mice. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14872-14877.
87. Wijesekara N., Dai F.F., Hardy A.B., Giglou P.R., Bhattacharjee A., Koshkin V., Chimienti F., Gaisano H.Y., Rutter G.A., Wheeler M.B. Beta cell-specific Znt8 deletion in mice causes marked defects in insulin processing, crystallisation and secretion. Diabetologia 2010, 53:1656-1668.
88. Hojyo S., Fukada T., Shimoda S., Ohashi W., Bin B.H., Koseki H., Hirano T. The zinc transporter SLC39A14/ZIP14 controls G-protein coupled receptor-mediated signaling required for systemic growth. PLoS One 2011, 6:e18059.
89. Chen Z.P., Kratzmeier M., Levy A., McArdle C.A., Poch A., Day A., Mukhopadhyay A.K., Lightman S.L. Evidence for a role of pituitary ATP receptors in the regulation of pituitary function. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:5219-5223.
90. Stojilkovic S.S., He M.L., Koshimizu T.A., Balik A., Zemkova H. Signaling by purinergic receptors and channels in the pituitary gland. Mol. Cell. Endocrinol. 2010, 314:184-191.
91. Li S., Bjelobaba I., Yan Z., Kucka M., Tomic M., Stojilkovic S.S. Expression and roles of pannexins in ATP release in the pituitary gland. Endocrinology 2011, 152:2342-2352.
92. Meilleur M.A., Akpovi C.D., Pelletier R.M., Vitale M.L. Tumor necrosis factor-alpha-induced anterior pituitary folliculostellate TtT/GF cell uncoupling is mediated by connexin 43 dephosphorylation. Endocrinology 2007, 148:5913-5924.
93. Reaume A.G., de Sousa P.A., Kulkarni S., Langille B.L., Zhu D., Davies T.C., Juneja S.C., Kidder G.M., Rossant J. Cardiac malformation in neonatal mice lacking connexin43. Science 1995, 267:1831-1834.
94. Lecanda F., Warlow P.M., Sheikh S., Furlan F., Steinberg T.H., Civitelli R. Connexin43 deficiency causes delayed ossification, craniofacial abnormalities, and osteoblast dysfunction. J. Cell Biol. 2000, 151:931-944.
95. Luque R.M., Amargo G., Ishii S., Lobe C., Franks R., Kiyokawa H., Kineman R.D. Reporter expression, induced by a growth hormone promoter-driven Cre recombinase (rGHp-Cre) transgene, questions the developmental relationship between somatotropes and lactotropes in the adult mouse pituitary gland. Endocrinology 2007, 148:1946-1953.
96. Parton L.E, Ye C.P., Coppari R., Enriori P.J., Choi B., Zhang C.Y., Xu C., Vianna C.R., Balthasar N., Lee C.E., Elmquist J.K., Cowley M.A., Lowell B.B. Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature 2007, 449:228-232.
97. Wen S., Schwarz J.R., Niculescu D., Dinu C., Bauer C.K., Hirdes W., Boehm U. Functional characterization of genetically labeled gonadotropes. Endocrinology 2008, 149:2701-2711.
98. 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. A new conditional mouse mutant reveals specific expression and functions of connexin36 in neurons and pancreatic beta-cells. Exp. Cell Res. 2008, 314:997-1012.
99. Nasonkin I.O., Potok M.A., Camper S.A. Cre-mediated recombination in pituitary somatotropes. Genesis 2009, 47:55-60.
100. Campbell R.E., Ducret E., Porteous R., Liu X., Herde M.K., Wellerhaus K., Sonntag S., Willecke K., Herbison A.E. Gap junctions between neuronal inputs but not gonadotropin-releasing hormone neurons control estrous cycles in the mouse. Endocrinology 2011, 152:2290-2301.
101. Rinehart J.F., Farquhar M.G. Electron microscopic studies of the anterior pituitary gland. J. Histochem. Cytochem. 1953, 1:93-113.
102. Ishikawa H., Nogami H., Shirasawa N. Novel clonal strains from adult rat anterior pituitary producing S-100 protein. Nature 1983, 303:711-713.
103. Otto C., tom Dieck S., Bauer K. Dipeptide uptake by adenohypophysial folliculostellate cells. Am. J. Physiol. 1996, 271:C210-C217.
104. Fauquier T., Guerineau N.C., McKinney R.A., Bauer K., Mollard P. Folliculostellate cell network: a route for long-distance communication in the anterior pituitary. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:8891-8896.
105. Fauquier T., Lacampagne A., Travo P., Bauer K., Mollard P. Hidden face of the anterior pituitary. Trends Endocrinol. Metab. 2002, 13:304-309.
106. Lewis B.M., Pexa A., Francis K., Verma V., McNicol A.M., Scanlon M., Deussen A., Evans W.H., Rees D.A., Ham J. Adenosine stimulates connexin 43 expression and gap junctional communication in pituitary folliculostellate cells. FASEB J. 2006, 20:2585-2587.
107. Kennett J.E., Poletini M.O., Fitch C.A., Freeman M.E. Antagonism of oxytocin prevents suckling- and estradiol-induced, but not progesterone-induced, secretion of prolactin. Endocrinology 2009, 150:2292-2299.
108. Morand I., Fonlupt P., Guerrier A., Trouillas J., Calle A., Remy C., Rousset B., Munari-Silem Y. Cell-to-cell communication in the anterior pituitary: evidence for gap junction-mediated exchanges between endocrine cells and folliculostellate cells. Endocrinology 1996, 137:3356-3367.
109. Renner U., Gloddek J., Pereda M.P., Arzt E., Stalla G.K. Regulation and role of intrapituitary IL-6 production by folliculostellate cells. Domest. Anim. Endocrinol. 1998, 15:353-362.
110. Bonnefont X., Mollard P. Electrical activity in endocrine pituitary cells in situ: a support for a multiple-function coding. FEBS Lett. 2003, 548:49-52.
111. Charles A.C., Naus C.C., Zhu D., Kidder G.M., Dirksen E.R., Sanderson M.J. Intercellular calcium signaling via gap junctions in glioma cells. J. Cell Biol. 1992, 118:195-201.
112. Nedergaard M. Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 1994, 263:1768-1771.
113. 2+ waves in the intact liver. J. Biol. Chem. 1995, 270:8102-8107.
114. 2+ waves in the blowfly salivary gland. EMBO J. 1999, 18:3222-3231.
115. Wussling M.H., Krannich K., Drygalla V., Podhaisky H. Calcium waves in agarose gel with cell organelles: implications of the velocity curvature relationship. Biophys. J. 2001, 80:2658-2666.
116. Straub S.V., Giovannucci D.R., Yule D.I. Calcium wave propagation in pancreatic acinar cells: functional interaction of inositol 1,4,5-trisphosphate receptors, ryanodine receptors, and mitochondria. J. Gen. Physiol. 2000, 116:547-560.
117. 2+ release channels. Physiol. Rev. 2007, 87:593-658.
118. Wagner K.A., Yacono P.W., Golan D.E., Tashjian A.H. Mechanism of spontaneous intracellular calcium fluctuations in single GH4C1 rat pituitary cells. Biochem. J. 1993, 292(Pt 1):175-182.
119. Lafont C., Desarmenien M.G., Cassou M., Molino F., Lecoq J., Hodson D., Lacampagne A., Mennessier G., El Yandouzi T., Carmignac D., Fontanaud P., Christian H., Coutry N., Fernandez-Fuente M., Charpak S., Le Tissier P., Robinson I.C., Mollard P. Cellular in vivo imaging reveals coordinated regulation of pituitary microcirculation and GH cell network function. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4465-4470.
120. Schaeffer M., Hodson D.J., Lafont C., Mollard P. Functional importance of blood flow dynamics and partial oxygen pressure in the anterior pituitary. Eur. J. Neurosci. 2010, 32:2087-2095.
121. Schaeffer M., Hodson D.J., Lafont C., Mollard P. Endocrine cells and blood vessels work in tandem to generate hormone pulses. J. Mol. Endocrinol. 2011, 47:R59-R66.
122. Boger R.H. Nitric oxide and the mediation of the hemodynamic effects of growth hormone in humans. J. Endocrinol. Invest. 1999, 22:75-81.
123. 2 tension. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:5510-5514.
124. Lahiri S., Roy A., Baby S.M., Hoshi T., Semenza G.L., Prabhakar N.R. Oxygen sensing in the body. Prog. Biophys. Mol. Biol. 2006, 91:249-286.