Low-threshold exocytosis induced by cAMP-recruited CaV3.2 (α1H) channels in rat chromaffin cells

Biophysical Journal

Volumn 90, Issue 5, 2006, Pages 1830-1841

  Giancippoli, A ^a   Novara, M ^a   De Luca, A ^a   Baldelli, P ^a,b   Marcantoni, A ^a   Carbone, E ^a,b   Carabelli, V ^a  

^a CNISM Research Unit   (Italy)

^b Dept of Neuroscience ^*  (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL T TYPE; CYCLIC AMP; NICKEL; CA(V)3.2 PROTEIN, RAT; CALCIUM;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CHROMAFFIN CELL; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC POTENTIAL; EXOCYTOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; CELL CULTURE; CHANNEL GATING; DIFFERENTIAL THRESHOLD; DRUG EFFECT; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALIA;

ANIMALS; CALCIUM; CALCIUM CHANNELS, T-TYPE; CELLS, CULTURED; CHROMAFFIN CELLS; CYCLIC AMP; DIFFERENTIAL THRESHOLD; EXOCYTOSIS; ION CHANNEL GATING; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33646145318     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.071647     Document Type: Article

References (60)

1. Albillos, A., A. R. Artalejo, M. G. Lopez, L. Gandía, A. G. García, and E. Carbone. 1994. Calcium channel subtypes in cat chromaffin cells. J. Physiol. 477:197-213.
2. 2+ concentrations. Pflugers Arch. 432:1030-1038.
3. Albillos, A., A. G. García, and L. Gandía. 1993. ω-Agatoxin-IVA-sensitive calcium channels in bovine chromaffin cells. FEBS Lett. 336:259-262.
4. Bossu, J. L., M. De Waard, and A. Feltz. 1991. Two types of calcium channels are expressed in adult bovine chromaffin cells. J. Physiol. 437:621-634.
5. Bossu, J. L., M. De Waard, and A. Feltz. 1991. Inactivation characteristics reveal two calcium currents in adult bovine chromaffin cells. J. Physiol. 437:603-620.
6. Hoshi, T., and S. J. Smith. 1987. Large depolarization induces long openings of voltage-dependent calcium channels in adrenal chromaffin cells. J. Neurosci. 7:571-580.
7. 2+ signals and secretion in chromaffin cell subtypes. Am. J. Physiol. 272:C476-C484.
8. 2+ channels dominate the control of secretion in bovine chromaffin cells. FEBS Lett. 349:331-337.
9. 2+ channels in bovine chromaffin cells. J. Neurochem. 74:1271-1278.
10. 2+ channels are coupled to the rapid component of secretion in mouse adrenal slice chromaffin cells. J. Neurosci. 20:8323-8330.
11. 2+ channel trigger secretion with different efficacies in chromaffin cells. Nature. 367:72-76.
12. 2+ channels are located closer to secretory sites than L-type channels: functional evidence in chromaffin cells. Pflugers Arch. 435:472-478.
13. Carabelli, V., I. Carra, and E. Carbone. 1998. Localized secretion of ATP and opioids revealed through single Ca2+ channel modulation in bovine chromaffin cells. Neuron. 20:1255-1268.
14. Carabelli, V., A. Giancippoli, P. Baldelli, E. Carbone, and A. R. Artalejo. 2003. Distinct potentiation of L-type currents and secretion by cAMP in rat chromaffin cells. Biophys. J. 85:1326-1337.
15. Mansvelder, H. D., and K. S. Kits. 1998. The relation of exocytosis and rapid endocytosis to calcium entry evoked by short repetitive depolarizing pulses in rat melanotropic cells. J. Neurosci. 18:81-92.
16. Kim, S. J., W. Lim, and J. Kim. 1995. Contribution of L- and N-type calcium currents to exocytosis in rat adrenal medullary chromaffin cells. Brain Res. 675:289-296.
17. 2+ diffusion near the membrane: implications for secretion in neuroendocrine cells. Biophys. J. 72:674-690.
18. 2+ channel types in bovine chromaffin cells. Pflugers Arch. 439:304-314.
19. Lukyanetz, E. A., and E. Neher. 1999. Different types of calcium channels and secretion from bovine chromaffin cells. Eur. J. Neurosci. 11:2865-2873.
20. 2+ channels of bovine chromaffin cells. J. Physiol. 516:421-432.
21. 2+-channels explains the preferential distribution of exocytotic active zones in neurites emitted by bovine chromaffin cells. Eur. J. Cell Biol. 80:358-365.
22. 2+ channels, derived from mRNA identification studies. FEBS Lett. 481:235-239.
23. Bournaud, R., J. Hidalgo, H. Yu, E. Jaimovich, and T. Shimar. 2001. Low threshold T-type calcium current in rat chromaffin cells. J. Physiol. 537:35-44.
24. Hollins, B., and S. R. Ikeda. 1996. Inward currents underlying action potentials in rat adrenal chromaffin cells. J. Neurophysiol. 76:1195-1211.
25. Novara, M., P. Baldelli, D. Cavallari, V. Carabelli, A. Giancippoli, and E. Carbone. 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.
26. 2+ channels in bovine chromaffin cells. J. Physiol. 532:73-90.
27. Cesetti, T., J. M. Hernandez-Gujio, P. Baldelli, V. Carabelli, and E. Carbone. 2003. Opposite action of β1- and β2-adrenergic receptors on Ca(V)1 L-channel current in rat adrenal chromaffin cells. J. Neurosci. 23:73-83.
28. Schrier, A. D., H. Wang, E. M. Talley, E. Perez-Reyes, and P. Q. Barrett. 2001. Alpha1H T-type Ca2+ channel is the predominant subtype expressed in bovine and rat zona glomerulosa. Am. J. Physiol. Cell Physiol. 280:C265-C272.
29. Bhattacharjee, A., R. M. Whitehurst, M. Zhang, L. Wang, and M. Li. 1997. T-type calcium channels facilitate insulin secretion by enhancing general excitability in the insulin-secreting beta-cell line. Endocrinology. 138:3735-3740.
30. Leuranguer, V., A. Monteil, E. Bourinet, G. Dayanithi, and J. Nargeot. 2000. T-type calcium currents in rat cardiomyocytes during postnatal development: contribution to hormone secretion. Am. J. Physiol. Heart Circ. Physiol. 279:H2540-H2548.
31. Mansvelder, H. D., J. C. Lodder, M. S. Sons, and K. S. Kits. 2002. Dopamine modulates exocytosis independent of Ca(2+) entry in melanotropic cells. J. Neurophysiol. 87:793-801.
32. 2+ channels mediate neurotransmitter release in retinal bipolar cells. Neuron. 32:89-98.
33. Harkins, A. B., A. L. Cahill, J. F. Powers, A. S. Tischler, and A. P. Fox. 2003. Expression of recombinant calcium channels support secretion in a mouse pheochromocytoma cell line. J. Neurophysiol. 90:2325-2333.
34. Rae, J., K. Cooper, P. Gates, and M. Watsky. 1991. Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Methods. 37:15-26.
35. Barry, P. H., and J. W. Lynch. 1991. Liquid junction potentials and small cell effects in patch-clamp analysis. J. Membr. Biol. 121:101-117.
36. 2+ channel gene family. Circ. Res. 83:103-109.
37. Lee, J. H., J. C. Gomora, L. L. Cribbs, and E. Perez-Reyes. 1999. Nickel block of three cloned T-type calcium channels: low concentrations selectively block alpha1H. Biophys. J. 77:3034-3042.
38. Hwang, O., M. L. Kim, and J. D. Lee. 1994. Differential induction of gene expression of catecholamine biosynthetic enzymes and preferential increase in norepinephrine by forskolin. Biochem. Pharmacol. 48:1927-1934.
39. Newcomb, R., B. Szoke, A. Palma, G. Wang, X. Chen, W. Hopkins, R. Cong, J. Miller, L. Urge, K. Tarczy-Hornoch, J. A. Loo, D. J. Dooley, L. Nadasdi, R. W. Tsien, J. Lemos, and G. Miljanich. 1998. Selective peptide antagonist of the class E calcium channel from the venom of the tarantula Hysterocrates gigas. Biochemistry. 37:15353-15362.
40. Horrigan, F. T., and R. J. Bookmann. 1994. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron. 13:1119-1129.
41. Zamponi, G. W., E. Bourinet, and T. P. Snutch. 1996. Nickel block of a family of neuronal calcium channels: subtype- and subunit-dependent action at multiple sites. J. Membr. Biol. 151:77-90.
42. Gillis, K. D., R. Mossner, and E. Neher. 1996. Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron. 16:1209-1220.
43. 2+ channels. Eur. J. Neurosci. 11:4171-4178.
44. Moser, T., and E. Neher. 1997. Rapid exocytosis in single chromaffin cells recorder from mouse adrenal slices. J. Neurosci. 17:2314-2323.
45. Thiagarajan, R., T. Tewolde, Y. Li, P. L. Becker, M. M. Rich, and K. L. Engisch. 2004. Rab3A negatively regulates activity-dependent modulation of exocytosis in bovine adrenal chromaffin cells. J. Physiol. 555:439-457.
46. Kits, K. S., and H. D. Mansvelder. 2000. Regulation of exocytosis in neuroendocrine cells: spatial organization of channels and vesicles, stimulus-secretion coupling, calcium buffers and modulation. Brain Res. Brain Res. Rev. 33:78-94.
47. Moser, T., and E. Neher. 1997. Estimation of mean exocytic vesicle capacitance in mouse adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA. 94:6735-6740.
48. 2+ channels. Annu. Rev. Cell Dev. Biol. 16:521-555.
49. Baldelli, P., J. M. Hernandez-Guijo, V. Carabelli, M. Novara, T. Cesetti, E. Andres-Mateos, C. Montiel, and E. Carbone. 2004. Direct and remote modulation of L-channels in chromaffin cells: distinct actions on alpha1C and alpha1D subunits? Mol. Neurobiol. 29:73-96.
50. Lim, W., S. J. Kim, H. D. Yan, and J. Kim. 1997. Ca2+-channel-dependent and -independent inhibition of exocytosis by extracellular ATP in voltage-clamped rat adrenal chromaffin cells. Pflugers Arch. 435:34-42.
51. Barg, S., X. Ma, L. Eliasson, J. Galvanovskis, S. O. Gopel, S. Obermuller, J. Platzer, E. Renstrom, M. Trus, D. Atlas, J. Striessnig, and P. Rorsman. 2001. Fast exocytosis with few Ca(2+) channels in insulin-secreting mouse pancreatic B cells. Biophys. J. 81:3308-3323.
52. Hsu, S. F., and M. B. Jackson. 1996. Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. J. Physiol. 494:539-553.
53. Seward, E. P., N. I. Chernevskaya, and M. C. Nowycky. 1995. Exocytosis in peptidergic nerve terminals exhibits two calciumsensitive phases during pulsatile calcium entry. J. Neurosci. 15:3390-3399.
54. Peng, Y. Y., and R. S. Zucker. 1993. Release of LHRH is linearly related to the time integral of presynaptic Ca2+ elevation above a threshold level in bullfrog sympathetic ganglia. Neuron. 10:465-473.
55. Fomina, A. F., and M. C. Nowycky. 1999. A current activated on depletion of intracellular Ca2+ stores can regulate exocytosis in adrenal chromaffin cells. J. Neurosci. 19:3711-3722.
56. Yizhar, O., U. Matti, R. Melamed, Y. Hagalili, D. Bruns, J. Rettig, and U. Ashery. 2004. Tomosyn inhibits priming of large dense-core vesicles in a calcium-dependent manner. Proc. Natl. Acad. Sci. USA. 101:2578-2583.
57. Voets, T., E. Neher, and T. Moser. 1999. Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron. 23:607-615.
58. Carbone, E., and H. D. Lux. 1987. Single low-voltage-activated calcium channels in chick and rat sensory neurons. J. Physiol. 386:571-601.
59. Tang, K. S., A. Tse, and F. W. Tse. 2005. Differential regulation of multiple populations of granules in rat adrenal chromaffin cells by culture duration and cyclic AMP. J. Neurochem. 92:1126-1139.
60. Duan, K., X. Yu, C. Zhang, and Z. Zhou. 2003. Control of secretion by temporal patterns of action potentials in adrenal chromaffin cells. J. Neurosci. 23:11235-11243.