Functional chromaffin cell plasticity in response to stress: Focus on nicotinic, gap junction, and voltage-gated Ca2+ channels

Journal of Molecular Neuroscience

Volumn 48, Issue 2, 2012, Pages 368-386

  Guérineau, Nathalie C ^a   Desarménien, Michel G ^b   Carabelli, Valentina ^c   Carbone, Emilio ^c  

^a Universite d'Angers   (France)

^b INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

Adrenal stimulus secretion coupling; Chromaffin cells; Gap junctions; Nicotinic receptors; Stress; Voltagegated calcium channels

Indexed keywords

CATECHOLAMINE; CONNEXIN 26; CONNEXIN 32; CONNEXIN 36; CONNEXIN 43; NICOTINIC RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

ADRENAL MEDULLA; CATECHOLAMINE RELEASE; CHROMAFFIN CELL; CONFERENCE PAPER; DENERVATION; GAP JUNCTION; HUMAN; INTRACELLULAR SIGNALING; NONHUMAN; PLASTICITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RECEPTOR UPREGULATION; SPLANCHNIC NERVE; STRESS;

CALCIUM CHANNELS; CATECHOLAMINES; CHROMAFFIN CELLS; GAP JUNCTIONS; HUMANS; RECEPTORS, NICOTINIC; STRESS, PHYSIOLOGICAL;

EID: 84868208834     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-012-9707-7     Document Type: Conference Paper

References (157)

1. Albillos A, Garcia AG, Gandia L (1993) omega-Agatoxin-IVA-sensitive calcium channels in bovine chromaffin cells. FEBS Lett 336:259-262
2. 2+ channel subtypes in bovine chromaffin cells: selectivity of action and voltage-dependence. Eur J Neurosci 8:1561-1570
3. Albillos A, Gandia L, Michelena P et al (1996b) The mechanism of calcium channel facilitation in bovine chromaffin cells. J Physiol 494(Pt 3):687-695
4. 2+ channels are coupled to the rapid component of secretion in mouse adrenal slice chromaffin cells. J Neurosci 20:8323-8330
5. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73-120
6. 2+ release in chromaffin cells seen from inside the ER with targeted aequorin. J Cell Biol 144:241-254
7. Arnaiz-Cot JJ, de Diego AM, Hernandez-Guijo JM, Gandia L, Garcia AG (2008) A two-step model for acetylcholine control of exocytosis via nicotinic receptors. Biochem Biophys Res Commun 365:413-419
8. 2+ currents are found in bovine chromaffin cells: facilitation is due to the recruitment of one type. J Physiol 432:681-707
9. Axelrod J (1971) Noradrenaline: fate and control of its biosynthesis. Science 173:598-606
10. Baldelli P, Hernandez-Guijo JM, Carabelli V et al (2004) Direct and remote modulation of L-channels in chromaffin cells: distinct actions on alpha1C and alpha1D subunits? Mol Neurobiol 29:73-96
11. Barbara JG, Takeda K (1995) Voltage-dependent currents and modulation of calcium channel expression in zona fasciculata cells from rat adrenal gland. J Physiol 488:609-622
12. Barbara JG, Lemos VS, Takeda K (1998) Pre- and post-synaptic muscarinic receptors in thin slices of rat adrenal gland. Eur J Neurosci 10:3535-3545
13. Bean BP (1989) Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340:153-156
14. Benavides A, Calvo S, Tornero D, Gonzalez-Garcia C, Ceña V (2004) Adrenal medulla calcium channel population is not conserved in bovine chromaffin cells in culture. Neuroscience 128:99-109
15. Borland G, Smith BO, Yarwood SJ (2009) EPAC proteins transduce diverse cellular actions of cAMP. Br J Pharmacol 158:70-86
16. Bosco D, Haefliger JA, Meda P (2011) Connexins: key mediators of endocrine function. Physiol Rev 91:1393-1445
17. Bournaud R, Hidalgo J, Yu H, Jaimovich E, Shimahara T (2001) Low threshold T-type calcium current in rat embryonic chromaffin cells. J Physiol 537:35-44
18. Buttigieg J, Brown S, Holloway AC, Nurse CA (2009) Chronic nicotine blunts hypoxic sensitivity in perinatal rat adrenal chromaffin cells via upregulation of KATP channels: role of alpha7 nicotinic acetylcholine receptor and hypoxia-inducible factor-2alpha. J Neurosci 29:7137-7147
19. Campanucci V, Krishnaswamy A, Cooper E (2010) Diabetes depresses synaptic transmission in sympathetic ganglia by inactivating nAChRs through a conserved intracellular cysteine residue. Neuron 66:827-834
20. Campos-Caro A, Smillie FI, Dominguez del Toro E et al (1997) Neuronal nicotinic acetylcholine receptors on bovine chromaffin cells: cloning, expression, and genomic organization of receptor subunits. J Neurochem 68:488-497
21. Campos-Caro A, Carrasco-Serrano C, Valor LM, Viniegra S, Ballesta JJ, Criado M (1999) Multiple functional Sp1 domains in the minimal promoter region of the neuronal nicotinic receptor alpha5 subunit gene. J Biol Chem 274:4693-4701
22. 2+ channel kinetics by receptor agonists in IMR32 cells. Biophys J 70:2144-2154
23. 2+ channel modulation in bovine chromaffin cells. Neuron 20:1255-1268
24. 2+ channels in bovine chromaffin cells. J Physiol 532:73-90
25. Carabelli V, D'Ascenzo M, Carbone E, Grassi C (2002) Nitric oxide inhibits neuroendocrine Ca(V)1 L-channel gating via cGMP dependent protein kinase in cell-attached patches of bovine chromaffin cells. J Physiol 541:351-366
26. Carabelli V, Giancippoli A, Baldelli P, Carbone E, Artalejo AR (2003) Distinct potentiation of L-type currents and secretion by cAMP in rat chromaffin cells. Biophys J 85:1326-1337
27. 2+-dependence. Eur Biophys J 36:753-762
28. Carabelli V, Marcantoni A, Comunanza V et al (2007b) Chronic hypoxia up-regulates alpha1H T-type channels and lowthreshold catecholamine secretion in rat chromaffin cells. J Physiol 584:149-165
29. Carbone E, Lux HD (1987) Kinetics and selectivity of a low-voltageactivated calcium current in chick and rat sensory neurones. J Physiol 386:547-570
30. Carbone E, Carabelli V, Cesetti T, Baldelli P, Hernandez-Guijo JM, Giusta L (2001) G-protein- and cAMP-dependent L-channel gating modulation: a manyfold system to control calcium entry in neurosecretory cells. Pflugers Arch 442:801-813
31. Carbone E, Marcantoni A, Giancippoli A, Guido D, Carabelli V (2006) T-type channels-secretion coupling: evidence for a fast lowthreshold exocytosis. Pflugers Arch 453:373-383
32. Carrasco-Serrano C, Criado M (2004) Glucocorticoid activation of the neuronal nicotinic acetylcholine receptor alpha7 subunit gene: involvement of transcription factor Egr-1. FEBS Lett 566:247-250
33. Caton D, Calabrese A, Mas C, Serre-Beinier V, Wonkam A, Meda P (2002) Beta-cell crosstalk: a further dimension in the stimulus-secretion coupling of glucose-induced insulin release. Diabetes Metab 28:3S45-3S53, discussion 43S108-112
34. Catterall WA (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3:a003947
35. Ceña 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 10:1455-1462
36. Cesetti T, Hernandez-Guijo JM, Baldelli P, Carabelli V, Carbone E (2003) Opposite action of beta1- and beta2-adrenergic receptors on Ca(V)1 L-channel current in rat adrenal chromaffin cells. J Neurosci 23:73-83
37. Chan SA, Smith C (2001) Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells. J Physiol 537:871-885
38. Chow RH, von Ruden L, Neher E (1992) Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356:60-63
39. Chung MK, Guler AD, Caterina MJ (2008) TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 11:555-564
40. Cocchia D, Michetti F (1981) S-100 antigen in satellite cells of the adrenal medulla and the superior cervical ganglion of the rat. An immunochemical and immunocytochemical study. Cell Tissue Res 215:103-112
41. Colomer C, Lafont C, Guerineau NC (2008a) Stress-induced intercellular communication remodeling in the rat adrenal medulla. Ann N Y Acad Sci 1148:106-111
42. Colomer C, Olivos Ore LA, Coutry N et al (2008b) Functional remodeling of gap junction-mediated electrical communication between adrenal chromaffin cells in stressed rats. J Neurosci 28:6616-6626
43. 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 40:87-100
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 30:6732-6742
45. Colomer C, Martin AO, Desarmenien MG, Guerineau NC (2011) Gap junction-mediated intercellular communication in the adrenal medulla: an additional ingredient of stimulus-secretion coupling regulation. Biochim Biophys Acta. doi:10.1016/j.bbamem.2011.07.034 [Epub ahead of print]
46. Comunanza V, Carbone E, Marcantoni A, Sher E, Ursu D (2011) Calciumdependent inhibition of T-type calcium channels by TRPV1 activation in rat sensory neurons. Pflugers Arch 462:709-722
47. Criado M, Alamo L, Navarro A (1992) Primary structure of an agonist binding subunit of the nicotinic acetylcholine receptor from bovine adrenal chromaffin cells. Neurochem Res 17:281-287
48. 2+ channel currents in cultured bovine adrenal chromaffin cells. Neuron 16:1027-1036
49. Currie KP, Fox AP (2002) Differential facilitation of N- and P/Q-type calcium channels during trains of action potential-like waveforms. J Physiol 539:419-431
50. Degen J, Meier C, Van Der Giessen RS et al (2004) Expression pattern of lacZ reporter gene representing connexin36 in transgenic mice. J Comp Neurol 473:511-525
51. Del Toro R, Levitsky KL, Lopez-Barneo J, Chiara MD (2003) Induction of T-type calcium channel gene expression by chronic hypoxia. J Biol Chem 278:22316-22324
52. Di Angelantonio S, Matteoni C, Fabbretti E, Nistri A (2003) Molecular biology and electrophysiology of neuronal nicotinic receptors of rat chromaffin cells. Eur J Neurosci 17:2313-2322
53. Diverse-Pierluissi M, Dunlap K,Westhead EW (1991) Multiple actions of extracellular ATP on calcium currents in cultured bovine chromaffin cells. Proc Natl Acad Sci USA 88:1261-1265
54. Douglas WW (1968) Stimulus-secretion coupling: the concept and clues from chromaffin and other cells. Br J Pharmacol 34:451-474
55. Douglas WW(1975) Secretomotor control of adrenal medullary secretion: synaptic, membrane and ionic events in stimulus-secretion coupling. In: Blaschko H, Sayers G, Smith AD (eds) Handbook of physiology. American Physiological Society, Baltimore, pp 367-388
56. Douglas WW, Kanno T, Sampson SR (1967) Effects of acetylcholine and other medullary secretagogues and antagonists on the membrane potential of adrenal chromaffin cells: an analysis employing techniques of tissue culture. J Physiol 188:107-120
57. Ducsay CA, Hyatt K, Mlynarczyk M, Root BK, Kaushal KM, Myers DA (2007) Long-term hypoxia modulates expression of key genes regulating adrenomedullary function in the late gestation ovine fetus. Am J Physiol Regul Integr Comp Physiol 293: R1997-R2005
58. Eiberger J, Kibschull M, Strenzke N et al (2006) Expression pattern and functional characterization of connexin29 in transgenic mice. Glia 53:601-611
59. Elmslie KS, Zhou W, Jones SW (1990) LHRH and GTP-gamma-S modify calcium current activation in bullfrog sympathetic neurons. Neuron 5:75-80
60. 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 98:8891-8896
61. 2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 35:1-8
62. 2+ permeability through rat cloned alpha9-containing nicotinic acetylcholine receptors. Cell Calcium 39:349-355
63. Fulop T, Smith C (2007) Matching native electrical stimulation by graded chemical stimulation in isolated mouse adrenal chromaffin cells. J Neurosci Methods 166:195-202
64. Gandia L, Garcia AG, Morad M (1993) ATP modulation of calcium channels in chromaffin cells. J Physiol 470:55-72
65. Garcia AG, Garcia-De-Diego AM, Gandia L, Borges R, Garcia-Sancho J (2006) Calcium signaling and exocytosis in adrenal chromaffin cells. Physiol Rev 86:1093-1131
66. Garcia-Fernandez M, Mejias R, Lopez-Barneo J (2007) Developmental changes of chromaffin cell secretory response to hypoxia studied in thin adrenal slices. Pflugers Arch 454:93-100
67. Garcia-Guzman M, Sala F, Sala S et al (1995) alpha-Bungarotoxinsensitive nicotinic receptors on bovine chromaffin cells: molecular cloning, functional expression and alternative splicing of the alpha 7 subunit. Eur J Neurosci 7:647-655
68. 2+ channels, derived from mRNA identification studies. FEBS Lett 481:235-239
69. Garcia-Palomero E, Renart J, Andres-Mateos E et al (2001) Differential expression of calcium channel subtypes in the bovine adrenal medulla. Neuroendocrinology 74:251-261
70. Giancippoli A, Novara M, de Luca A et al (2006) Low-threshold exocytosis induced by cAMP-recruited CaV3.2 (alpha1H) channels in rat chromaffin cells. Biophys J 90:1830-1841
71. Giordanetto F, Knerr L, Wallberg A (2011) T-type calcium channels inhibitors: a patent review. Expert Opin Ther Pat 21:85-101
72. Gosso S, Gavello D, Giachello CN, Franchino C, Carbone E, Carabelli V (2011) The effect of CdSe-ZnS quantum dots on calcium currents and catecholamine secretion in mouse chromaffin cells. Biomaterials 32:9040-9050
73. Gotti C, Zoli M, Clementi F (2006) Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol Sci 27:482-491
74. Grynszpan-Wynograd O, Nicolas G (1980) Intercellular junctions in the adrenal medulla: a comparative freeze-fracture study. Tissue Cell 12:661-672
75. Guerineau NC, Desarmenien MG (2010) Developmental and stressinduced remodeling of cell-cell communication in the adrenal medullary tissue. Cell Mol Neurobiol 30:1425-1431
76. Herlitze S, Hockerman GH, Scheuer T, Catterall WA (1997) Molecular determinants of inactivation and G protein modulation in the intracellular loop connecting domains I and II of the calcium channel alpha1A subunit. Proc Natl Acad Sci USA 94:1512-1516
77. Hernandez A, Segura-Chama P, Jimenez N, Garcia AG, Hernandez-Guijo JM, Hernandez-Cruz A (2011) Modulation by endogenously released ATP and opioids of chromaffin cell calcium channels in mouse adrenal slices. Am J Physiol Cell Physiol 300:C610-C623
78. Hernandez-Guijo JM, de Pascual R, Garcia AG, Gandia L (1998a) Separation of calcium channel current components in mouse chromaffin cells superfused with low- and high-barium solutions. Pflugers Arch 436:75-82
79. Hernandez-Guijo JM, Gandia L, Lara B, Garcia AG (1998b) Autocrine/paracrine modulation of calcium channels in bovine chromaffin cells. Pflugers Arch 437:104-113
80. Hernandez-Guijo JM, Carabelli V, Gandia L, Garcia AG, Carbone E (1999) Voltage-independent autocrine modulation of L-type channels mediated by ATP, opioids and catecholamines in rat chromaffin cells. Eur J Neurosci 11:3574-3584
81. Hill J, Chan SA, Kuri B, Smith C (2011) PACAP recruits a low voltage activated T-type calcium influx under acute sympathetic stimulation in mouse adrenal chromaffin cells. J Biol Chem 286:42459-42469
82. Hollins B, Ikeda SR (1996) Inward currents underlying action potentials in rat adrenal chromaffin cells. J Neurophysiol 76:1195-1211
83. Horrigan FT, Bookman RJ (1994) Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13:1119-1129
84. Hunter RG, Bloss EB, McCarthy KJ, McEwen BS (2010) Regulation of the nicotinic receptor alpha7 subunit by chronic stress and corticosteroids. Brain Res 1325:141-146
85. Ikeda SR (1996) Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature 380:255-258
86. Ikeda SR, Dunlap K (1999) Voltage-dependent modulation of N-type calcium channels: role of G protein subunits. Adv Second Messenger Phosphoprotein Res 33:131-151
87. 2+ stores in rat adrenal chromaffin cells. Cell Calcium 33:19-26
88. Jagger DJ, Griesinger CB, Rivolta MN, Holley MC, Ashmore JF (2000) Calcium signalling mediated by the 9 acetylcholine receptor in a cochlear cell line from the Immortomouse. J Physiol 527:49-54
89. Jagodic MM, Pathirathna S, Nelson MT et al (2007) Cell-specific alterations of T-type calcium current in painful diabetic neuropathy enhance excitability of sensory neurons. J Neurosci 27:3305-3316
90. Jain R, Lammert E (2009) Cell-cell interactions in the endocrine pancreas. Diabetes Obes Metab 11(Suppl 4):159-167
91. Kidokoro Y, Ritchie AK (1980) Chromaffin cell action potentials and their possible role in adrenaline secretion from rat adrenal medulla. J Physiol 307:199-216
92. Kilpatrick DL, Slepetis R, Kirshner N (1981) Ion channels and membrane potential in stimulus-secretion coupling in adrenal medulla cells. J Neurochem 36:1245-1255
93. Kilpatrick DL, Slepetis RJ, Corcoran JJ, Kirshner N (1982) Calcium uptake and catecholamine secretion by cultured bovine adrenal medulla cells. J Neurochem 38:427-435
94. Kim SJ, Lim W, Kim J (1995) Contribution of L- and N-type calcium currents to exocytosis in rat adrenal medullary chromaffin cells. Brain Res 675:289-296
95. 2+ diffusion near the membrane: implications for secretion in neuroendocrine cells. Biophys J 72:674-690
96. 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 110:1214-1225
97. Lalevee N, Rebsamen MC, Barrere-Lemaire S et al (2005) Aldosterone increases T-type calcium channel expression and in vitro beating frequency in neonatal rat cardiomyocytes. Cardiovasc Res 67:216-224
98. Lesouhaitier O, Chiappe A, Rossier MF (2001) Aldosterone increases T-type calcium currents in human adrenocarcinoma (H295R) cells by inducing channel expression. Endocrinology 142:4320-4330
99. 2+ channel expression and its role in rat chromaffin cell responsiveness to acute hypoxia. J Physiol 587:1917-1929
100. 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 122:485-498
101. Lipscombe D, Helton TD, Xu W (2004) L-type calcium channels: the low down. J Neurophysiol 92:2633-2641
102. Liu H, Enyeart JA, Enyeart JJ (2010) ACTH induces Cav3.2 current and mRNA by cAMP-dependent and cAMP-independent mechanisms. J Biol Chem 285:20040-20050
103. Lloyd RV, Blaivas M, Wilson BS (1985) Distribution of chromogranin and S100 protein in normal and abnormal adrenal medullary tissues. Arch Pathol Lab Med 109:633-635
104. Lopez MG, Shukla R, Garcia AG,Wakade AR (1992) A dihydropyridineresistant component in the rat adrenal secretory response to splanchnic nerve stimulation. J Neurochem 58:2139-2144
105. Lopez MG, Albillos A, de la Fuente MT et al (1994) Localized L-type calcium channels control exocytosis in cat chromaffin cells. Pflugers Arch 427:348-354
106. Lopez MG, Montiel C, Herrero CJ et al (1998) Unmasking the functions of the chromaffin cell alpha7 nicotinic receptor by using short pulses of acetylcholine and selective blockers. Proc Natl Acad Sci USA 95:14184-14189
107. Lu SJ, Li H, Zhou FH, Zhang JJ, Wang LX (2007) Connexin 36 is expressed and associated with zonula occludens-1 protein in PC-12 cells. Gen Physiol Biophys 26:33-39
108. Mahapatra S, Marcantoni A, Vandael DH, Striessnig J, Carbone E (2011) Are Ca(v)1.3 pacemaker channels in chromaffin cells? Possible bias from resting cell conditions and DHP blockers usage. Channels (Austin) 5:219-224
109. Marcantoni A, Baldelli P, Hernandez-Guijo JM, Comunanza V, Carabelli V, Carbone E (2007) L-type calcium channels in adrenal chromaffin cells: role in pace-making and secretion. Cell Calcium 42:397-408
110. Marcantoni A, Carabelli V, Comunanza V, Hoddah H, Carbone E (2008) Calcium channels in chromaffin cells: focus on L and T types. Acta Physiol (Oxf) 192:233-246
111. Marcantoni A, Carabelli V, Vandael DH, Comunanza V, Carbone E (2009) PDE type-4 inhibition increases L-type Ca(2+) currents, action potential firing, and quantal size of exocytosis in mouse chromaffin cells. Pflugers Arch 457:1093-1110
112. Marcantoni A, Vandael DH, Mahapatra S et al (2010) Loss of Cav1.3 channels reveals the critical role of L-type and BK channel coupling in pacemaking mouse adrenal chromaffin cells. J Neurosci 30:491-504
113. Marchetti C, Carbone E, Lux HD (1986) Effects of dopamine and noradrenaline on Ca channels of cultured sensory and sympathetic neurons of chick. Pflugers Arch 406:104-111
114. Marger F, Gelot A, Alloui A et al (2011) T-type calcium channels contribute to colonic hypersensitivity in a rat model of irritable bowel syndrome. Proc Natl Acad Sci USA 108:11268-11273
115. Mariot P, Vanoverberghe K, Lalevee N, Rossier MF, Prevarskaya N (2002) Overexpression of an alpha 1H (Cav3.2) T-type calcium channel during neuroendocrine differentiation of human prostate cancer cells. J Biol Chem 277:10824-10833
116. 2+ increases between chromaffin cells in adrenal slices: a role in catecholamine release. J Neurosci 21:5397-5405
117. Martin AO, Mathieu MN, Guerineau NC (2003) Evidence for longlasting cholinergic control of gap junctional communication between adrenal chromaffin cells. J Neurosci 23:3669-3678
118. Martin AO, Alonso G, Guerineau NC (2005) Agrin mediates a rapid switch from electrical coupling to chemical neurotransmission during synaptogenesis. J Cell Biol 169:503-514
119. Meda P, Pepper MS, Traub O et al (1993) Differential expression of gap junction connexins in endocrine and exocrine glands. Endocrinology 133:2371-2378
120. Mollard P, Seward EP, Nowycky MC (1995) Activation of nicotinic receptors triggers exocytosis from bovine chromaffin cells in the absence of membrane depolarization. Proc Natl Acad Sci USA 92:3065-3069
121. Morand I, Fonlupt P, Guerrier A et al (1996) Cell-to-cell communication in the anterior pituitary: evidence for gap junction-mediated exchanges between endocrine cells and folliculostellate cells. Endocrinology 137:3356-3367
122. Moser T (1998) Low-conductance intercellular coupling between mouse chromaffin cells in situ. J Physiol 506(Pt 1):195-205
123. Murray SA, Pharrams SY (1997) Comparison of gap junction expression in the adrenal gland. Microsc Res Tech 36:510-519
124. Neher E (2006) A comparison between exocytic control mechanisms in adrenal chromaffin cells and a glutamatergic synapse. Pflugers Arch 453:261-268
125. Novara M, Baldelli P, Cavallari D, Carabelli V, Giancippoli A, Carbone E (2004) Exposure to cAMP and beta-adrenergic stimulation recruits Ca(V)3 T-type channels in rat chromaffin cells through Epac cAMP receptor proteins. J Physiol 558:433-449
126. Nurse CA, Buttigieg J, Brown S, Holloway AC (2009) Regulation of oxygen sensitivity in adrenal chromaffin cells. Ann N YAcad Sci 1177:132-139
127. 2+ current is expressed in hypertrophied adult feline left ventricular myocytes. Circ Res 73:777-782
128. Olivos L, Artalejo AR (2008) Muscarinic excitation-secretion coupling in chromaffin cells. Acta Physiol (Oxf) 192:213-220
129. Panner A, Wurster RD (2006) T-type calcium channels and tumor proliferation. Cell Calcium 40:253-259
130. Parker TL, Kesse WK, Tomlinson A, Coupland RE (1988) Ontogenesis of preganglionic sympathetic innervation of rat adrenal chromaffin cells. In: Dahlström A, Belmaker RH, Sandler M (eds) Progress in catecholamine research, part A: basic aspects and peripheral mechanisms. Liss, New York, pp 227-232
131. Perez-Alvarez A, Hernandez-Vivanco A, Caba-Gonzalez JC, Albillos A (2011a) Different roles attributed to Cav1 channel subtypes in spontaneous action potential firing and fine tuning of exocytosis in mouse chromaffin cells. J Neurochem 116:105-121
132. Perez-Alvarez A, Hernandez-Vivanco A, McIntosh JM, Albillos A (2011b) Native {alpha}6{beta}4* nicotinic receptors control exocytosis in human chromaffin cells of the adrenal gland. FASEB J. doi:10.1096/fj.11-190223 [Epub ahead of print]
133. Perez-Alvarez A, Hernandez-Vivanco A, Gregorio SA, Tabernero A, McIntosh JM, Albillos A (2011c) Pharmacological characterization of native alpha7 nAChRs and their contribution to depolarizationelicited exocytosis in human chromaffin cells. Br J Pharmacol. doi:10.1111/j.1476-5381.2011.01596.x [Epub ahead of print]
134. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83:117-161
135. Pluteanu F, Cribbs LL (2009) T-type calcium channels are regulated by hypoxia/reoxygenation in ventricular myocytes. Am J Physiol Heart Circ Physiol 297:H1304-H1313
136. Rosa JM, de Diego AM, Gandia L, Garcia AG (2007) L-type calcium channels are preferentially coupled to endocytosis in bovine chromaffin cells. Biochem Biophys Res Commun 357:834-839
137. Rosa JM, Gandia L, Garcia AG (2010) Permissive role of sphingosine on calcium-dependent endocytosis in chromaffin cells. Pflugers Arch 460:901-914
138. Rosa JM, Torregrosa-Hetland CJ, Colmena I, Gutierrez LM, Garcia AG, Gandia L (2011) Calcium entry through slow-inactivating Ltype calcium channels preferentially triggers endocytosis rather than exocytosis in bovine chromaffin cells. Am J Physiol Cell Physiol 301:C86-C98
139. Sala F, Nistri A, Criado M (2008) Nicotinic acetylcholine receptors of adrenal chromaffin cells. Acta Physiol (Oxf) 192:203-212
140. 2+ channel. Am J Physiol Heart Circ Physiol. doi:10.1152/ ajpheart.00849.2011 [Epub ahead of print]
141. Seidler FJ, Slotkin TA (1985) Adrenomedullary function in the neonatal rat: responses to acute hypoxia. J Physiol 358:1-16
142. 2+ channels are abnormal in genetically determined cardiomyopathic hamster hearts. Circ Res 75:149-155
143. 2+-dependent gating of CaV1.3 L-type calcium channels by alternative splicing of a C-terminal regulatory domain. J Biol Chem 283:20733-20744
144. Slotkin TA (1986) Development of the sympathoadrenal axis. In: Gootman PM (ed) Developmental neurobiology of the autonomic nervous system. Humana, Totowa, pp 69-96
145. 2+ channels and ryanodine receptors mediate the augmented exocytosis of catecholamines from intermittent hypoxia-treated neonatal rat chromaffin cells. J Neurosci 30:10763-10772
146. Stojilkovic SS, Tabak J, Bertram R (2010) Ion channels and signaling in the pituitary gland. Endocr Rev 31:845-915
147. Takebayashi S, Li Y, Kaku T et al (2006) Remodeling excitation- contraction coupling of hypertrophied ventricular myocytes is dependent on T-type calcium channels expression. Biochem Biophys Res Commun 345:766-773
148. Thiagarajan R, Tewolde T, Li Y, Becker PL, Rich MM, Engisch KL (2004) Rab3A negatively regulates activity-dependent modulation of exocytosis in bovine adrenal chromaffin cells. J Physiol 555:439-457
149. Thompson RJ, Jackson A, Nurse CA (1997) Developmental loss of hypoxic chemosensitivity in rat adrenomedullary chromaffin cells. J Physiol 498(Pt 2):503-510
150. Tyagi E, Agrawal R, Nath C, Shukla R (2010) Inhibitory role of cholinergic system mediated via alpha7 nicotinic acetylcholine receptor in LPS-induced neuro-inflammation. Innate Immun 16:3-13
151. Vandael DH, Marcantoni A, Mahapatra S et al (2010) Ca(v)1.3 and BK channels for timing and regulating cell firing. Mol Neurobiol 42:185-198
152. Wakade AR (1981) Studies on secretion of catecholamines evoked by acetylcholine or transmural stimulation of the rat adrenal gland. J Physiol 313:463-480
153. 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
154. Wu MM, Llobet A, Lagnado L (2009) Loose coupling between calcium channels and sites of exocytosis in chromaffin cells. J Physiol 587:5377-5391
155. 2+ signaling pathways in mouse adrenal medullary chromaffin cells. J Neurochem 112:1210-1222
156. 2+ signaling, prolyl hydroxylases, and mTOR. J Cell Physiol 217:674-685
157. Zamponi GW, Bourinet E, Nelson D, Nargeot J, Snutch TP (1997) Crosstalk between G proteins and protein kinase C mediated by the calcium channel alpha1 subunit. Nature 385:442-446