Alterations in Exocytosis Induced by Neuronal Ca2+ Sensor-1 in Bovine Chromaffin Cells

Overview

Journal J Neurosci

Specialty Neurology

Date 2002 Mar 30

PMID 11923406

Citations 16

Authors

Chien-Yuan Pan

Andreas Jeromin

Kenneth Lundstrom

Seung Hyun Yoo

John Roder

Aaron P Fox

Affiliations

Soon will be listed here.

Abstract

A variety of Ca2+ binding proteins are known to play an integral role in catecholamine release from synapses as well as secretory cells, such as chromaffin cells. The Drosophila protein frequenin and its mammalian homolog neuronal Ca2+ sensor-1 (NCS-1) belong to a family of Ca2+ sensors with EF hands that bind Ca2+ and then interact with other proteins. Frequenin/NCS-1 has been shown to enhance exocytotic activity in addition to altering Ca2+ channel regulation. To better understand how NCS-1 regulates stimulus-secretion coupling, bovine chromaffin cells were infected with Semliki Forest virus (SFV) vectors containing the rat NCS-1 gene. Cells were studied in the perforated whole-cell patch-clamp configuration. Membrane capacitance was monitored as an indicator of exocytosis-endocytosis. Exocytosis elicited by membrane depolarization was not significantly different between cells infected with SFV expressing green fluorescent protein (GFP) or GFP plus NCS-1, except that the overexpression of NCS-1 resulted in a faster rundown in exocytosis. When cells were stimulated with histamine, NCS-1 overexpression led to higher exocytosis, as well as [Ca2+]i elevation. Immunocytochemistry showed a similar distribution of NCS-1 and phosphatidylinositol 4-kinase beta (PI4Kbeta). NCS-1 and PI4Kbeta coimmunoprecipitate, opening up the possibility that the two proteins directly interact. These results suggest that NCS-1 may regulate cellular activity through the modulation of the phosphatidylinositol signaling pathway.

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References

Finnegan J, Borges R, Wightman R . Comparison of cytosolic Ca2+ and exocytosis responses from single rat and bovine chromaffin cells. Neuroscience. 1996; 71(3):833-43. DOI: 10.1016/0306-4522(95)00459-9. View

Pongs O, Lindemeier J, Zhu X, Theil T, Engelkamp D, Krah-Jentgens I . Frequenin--a novel calcium-binding protein that modulates synaptic efficacy in the Drosophila nervous system. Neuron. 1993; 11(1):15-28. DOI: 10.1016/0896-6273(93)90267-u. View

Harkins A, Dlouhy S, Ghetti B, Cahill A, Won L, Heller B . Evidence of elevated intracellular calcium levels in weaver homozygote mice. J Physiol. 2000; 524 Pt 2:447-55. PMC: 2269872. DOI: 10.1111/j.1469-7793.2000.t01-2-00447.x. View

Knight D . Secretion from bovine chromaffin cells acutely expressing exogenous proteins using a recombinant Semliki Forest virus containing an EGFP reporter. Mol Cell Neurosci. 2000; 14(6):486-505. DOI: 10.1006/mcne.1999.0793. View

Olafsson P, Wang T, Lu B . Molecular cloning and functional characterization of the Xenopus Ca(2+)-binding protein frequenin. Proc Natl Acad Sci U S A. 1995; 92(17):8001-5. PMC: 41274. DOI: 10.1073/pnas.92.17.8001. View

Pan C, Fox A . Rundown of secretion after depletion of intracellular calcium stores in bovine adrenal chromaffin cells. J Neurochem. 2000; 75(3):1132-9. DOI: 10.1046/j.1471-4159.2000.0751132.x. View

Benfenati F, Onofri F, Giovedi S . Protein-protein interactions and protein modules in the control of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci. 1999; 354(1381):243-57. PMC: 1692491. DOI: 10.1098/rstb.1999.0376. View

Lysakowski A, Figueras H, Price S, Peng Y . Dense-cored vesicles, smooth endoplasmic reticulum, and mitochondria are closely associated with non-specialized parts of plasma membrane of nerve terminals: implications for exocytosis and calcium buffering by intraterminal organelles. J Comp Neurol. 1999; 403(3):378-90. DOI: 10.1002/(sici)1096-9861(19990118)403:3<378::aid-cne7>3.0.co;2-x. View

Chen X, Zhong Z, Yokoyama S, BARK C, Meister B, Berggren P . Overexpression of rat neuronal calcium sensor-1 in rodent NG108-15 cells enhances synapse formation and transmission. J Physiol. 2001; 532(Pt 3):649-59. PMC: 2278582. DOI: 10.1111/j.1469-7793.2001.0649e.x. View

10.

Toker A . The synthesis and cellular roles of phosphatidylinositol 4,5-bisphosphate. Curr Opin Cell Biol. 1998; 10(2):254-61. DOI: 10.1016/s0955-0674(98)80148-8. View

11.

Artalejo C, Perlman R, Fox A . Omega-conotoxin GVIA blocks a Ca2+ current in bovine chromaffin cells that is not of the "classic" N type. Neuron. 1992; 8(1):85-95. DOI: 10.1016/0896-6273(92)90110-y. View

12.

Raucher D, Stauffer T, Chen W, Shen K, Guo S, York J . Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell. 2000; 100(2):221-8. DOI: 10.1016/s0092-8674(00)81560-3. View

13.

Braunewell K, Gundelfinger E . Intracellular neuronal calcium sensor proteins: a family of EF-hand calcium-binding proteins in search of a function. Cell Tissue Res. 1999; 295(1):1-12. DOI: 10.1007/s004410051207. View

14.

Tse F, Tse A, Hille B, Horstmann H, Almers W . Local Ca2+ release from internal stores controls exocytosis in pituitary gonadotrophs. Neuron. 1997; 18(1):121-32. DOI: 10.1016/s0896-6273(01)80051-9. View

15.

Rivosecchi R, Pongs O, Theil T, Mallart A . Implication of frequenin in the facilitation of transmitter release in Drosophila. J Physiol. 1994; 474(2):223-32. PMC: 1160311. DOI: 10.1113/jphysiol.1994.sp020015. View

16.

Brini M, Carafoli E . Calcium signalling: a historical account, recent developments and future perspectives. Cell Mol Life Sci. 2000; 57(3):354-70. PMC: 11146899. DOI: 10.1007/PL00000698. View

17.

Zhang X, MAJERUS P . Phosphatidylinositol signalling reactions. Semin Cell Dev Biol. 1998; 9(2):153-60. DOI: 10.1006/scdb.1997.0220. View

18.

Ashery U, Betz A, Xu T, Brose N, RETTIG J . An efficient method for infection of adrenal chromaffin cells using the Semliki Forest virus gene expression system. Eur J Cell Biol. 1999; 78(8):525-32. DOI: 10.1016/s0171-9335(99)80017-x. View

19.

Burgoyne R, Morgan A . Ca2+ and secretory-vesicle dynamics. Trends Neurosci. 1995; 18(4):191-6. DOI: 10.1016/0166-2236(95)93900-i. View

20.

Wiedemann C, Schafer T, Burger M, Sihra T . An essential role for a small synaptic vesicle-associated phosphatidylinositol 4-kinase in neurotransmitter release. J Neurosci. 1998; 18(15):5594-602. PMC: 6793044. View