Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-19T07:19:11.842Z Has data issue: false hasContentIssue false
  • English
  • Français

Plasma membrane localization and function of TRPC1 is dependent on its interaction with β-tubulin in retinal epithelium cells

Published online by Cambridge University Press:  02 June 2005

SUNITHA BOLLIMUNTHA ,
ERIC CORNATZER  and
BRIJ B SINGH
SUNITHA BOLLIMUNTHA
Affiliation:
Department of Biochemistry and Molecular Biology, School of Medicine & Health Sciences, University of North Dakota, Grand Forks
ERIC CORNATZER
Affiliation:
Department of Biochemistry and Molecular Biology, School of Medicine & Health Sciences, University of North Dakota, Grand Forks
BRIJ B SINGH
Affiliation:
Department of Biochemistry and Molecular Biology, School of Medicine & Health Sciences, University of North Dakota, Grand Forks
Get access Rights & Permissions [Opens in a new window]

Abstract

Mammalian homologues of the Drosophila canonical Transient Receptor Potential (TRPC) protein have been proposed to encode the store-operated Ca2+ influx (SOC) channel(s). This study examines the role of TRPC1 in the SOC mechanism of retinal cells. htrpc1 transcript was detected in bovine retinal and in human adult retinal pigment epithelial (ARPE) cells. Western blot analysis also confirmed the expression of TRPC1 protein in neuronal cells including retina and ARPE cells. To determine the role of TRPC1 protein in retinal cells, TRPC1 was recombinantly expressed in ARPE cells and changes in intracellular Ca2+ were analyzed. ARPE cells stably transfected with htrp1 cDNA displayed 2-fold higher Ca2+ influx with no significant increase in the basal influx. Consistent with this the overexpressed TRPC1 protein was localized in the plasma membrane region of ARPE cells. Interestingly, both bovine retinal tissues and ARPE cells showed that TRPC1 protein co-localizes and could be co-immunoprecipitated with β-tubulin. Disruption of tubulin by colchicine significantly decreased both plasma membrane staining of the TRPC1 protein and Ca2+ influx in ARPE cells. These results suggest that TRPC1 channel protein is expressed in retinal cells, further, targeting/retention of the TRPC1 protein to the plasma membrane in retinal cells is mediated via its interaction with β-tubulin.

Keywords

Transient receptor potential proteinStore-operated calcium entryβ-tubulinTraffickingRetina
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 2 , March 2005 , pp. 163 - 170
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Berridge, M.D. (1998). Neuronal calcium signaling. Neuron 21, 13–26.CrossRefGoogle Scholar
Bollimuntha, S., Singh, B.B., Shavali, S., Sharma, S.K., & Ebadi, M. (2005). TRPC1-mediated inhibition of MPP+ neurotoxicity in human SH-SY5Y neuroblastoma cells. Journal of Biological Chemistry 280, 2132–2140.CrossRefGoogle Scholar
Catsicas, M. & Mobbs, P. (2001). The GABAB receptors regulate chick retinal calcium waves. Journal of Neuroscience 21, 897–910.Google Scholar
Clapham, D.E. (2003). TRP channels as cellular sensors. Nature 426, 517–524.CrossRefGoogle Scholar
Crousillac, S., LeRouge, M., Rankin, M., & Gleason, E. (2003). Immunolocalization of the TRPC channel subunits 1 and 4 in the chiken retina. Visual Neuroscience 20, 453–463.CrossRefGoogle Scholar
Downing, K.H. & Nogales, E. (1999). Crystallographic structure of tubulin: Implications for dynamics and drug binding. Cell Structure and Function 24, 269–275.CrossRefGoogle Scholar
Dunn, K.C., Aotaki-Keen, A.E., Putkey, F.R., & Hjelmeland, L.M. (1996). ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Experimental Eye Research 62, 155–169.CrossRefGoogle Scholar
Himpens, B. & Vereecke, J. (2000). Intra- and intercellular Ca2+-signal transduction. ScienceSTKE 62, 501–563.Google Scholar
Hong, Y.S., Park, S., Geng, C., Baek, K., Bowman, J.D., Yoon, J., & Pak, W.L. (2002). Single amino acid change in the fifth transmembrane segment of the TRP Ca2+ channel causes massive degeneration of photoreceptors. Journal of Biological Chemistry 277, 33884–33889.CrossRefGoogle Scholar
Ilia, M. & Jeffery, G. (2000). Retinal cell addition and rod production depend on early stages of ocular melanin synthesis. Journal of Comparative Neurology 420, 437–444.3.0.CO;2-1>CrossRefGoogle Scholar
Liu, X., Wang, W., Singh, B.B., Lockwich, T., Jadlowiec, J., O'Connell, B., Wellner, R., Zhu, M.X., & Ambudkar, I.S. (2000). TRPC1 a candidate protein for the store-operated Ca2+ influx mechanism in salivary gland cells. Journal of Biological Chemistry 275, 3403–3411.CrossRefGoogle Scholar
Lockwich, T., Singh, B.B., Liu, X., & Ambudkar, I.S. (2001). Stabilization of cortical actin induces internalization of transient receptor potential 3 (Trp3)-associated caveolar Ca2+ signaling complex and loss of Ca2+ influx without disruption of Trp3-inositol trisphosphate receptor association. Journal of Biological Chemistry 276, 42401–42408.CrossRefGoogle Scholar
Mery, L., Strauss, B., Dufour, J.F., Krause, K.H., & Hoth, M. (2002). The PDZ-interacting domain of TRPC4 controls its localization and surface expression in HEK293 cells. Journal of Cell Science 115, 3497–3508.Google Scholar
Micci, M.A. & Christensen, B.N. (1998). Exchange in catfish retina horizontal cells: Regulation of intracellular Ca2+ store function. American Journal of Physiology 274, 1625–1633.Google Scholar
Minke, B. (2002). The TRP calcium channel and retinal degradation. Advances in Experimental Medicine and Biology 514, 601–622.CrossRefGoogle Scholar
Minke, B. & Cook, B. (2002). TRP channel proteins and signal transduction. Physiological Review 82, 429–452.CrossRefGoogle Scholar
Montell, C. (2001). Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Science STKE. 90, REI.Google Scholar
Ohmasa, M. & Saito, T. (2004). GABAA-receptor-mediated increase in intracellular Ca2+ concentration in the regenerating retina of adult newt. Neuroscience Research 49, 219–227.CrossRefGoogle Scholar
Owens, D.F. & Kriegstein, A.R. (1998). Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone. Journal of Neuroscience 18, 5374–5388.Google Scholar
Putney, J.W., Jr. (1991). The capacitative model for receptor-activated calcium entry. Advances in Pharmacology 22, 251–269.CrossRefGoogle Scholar
Putney, J.W., Jr. (2003). Capacitative calcium entry in the nervous system. Cell Calcium 34, 339–344.CrossRefGoogle Scholar
Raymond, S.M. & Jackson, I.J. (1995). The retinal pigmented epithelium is required for development and maintenance of the mouse neural retina. Current Biology 5, 1286–1295.CrossRefGoogle Scholar
Rosenthal, R. & Strauss, O. (2002). Ca2+-channels in the RPE. Advances in Experimental Medicine and Biology 514, 225–235.CrossRefGoogle Scholar
Rothermel, A., Willbold, E., Degrip, W.J., & Layer, P.G. (1997). Pigmented epithelium induces complete retinal reconstitution from dispersed embryonic chick retinae in reaggregation culture. Proceedings of the Royal Society (London) 264, 1293–1302.CrossRefGoogle Scholar
Ryan, J.S., Baldridge, W.H., & Kell, M.E. (1999). Purinergic regulation of cation conductances and intracellular Ca2+ in cultured rat retinal pigment epithelial cells. Journal of Physiology 520, 745–759.CrossRefGoogle Scholar
Sato, M., Ohguro, H., Ohguro, I., Mamiya, K., Takano, Y., Yamazaki, H., Metoki, T., Miyagawa, K., Ishikawa, F., & Nakazawa, M. (2003). Study of pharmacological effects of nilvadipine on RCS rat retinal degradation by micro array analysis. Biochemistry and Biophysical Research Communication 306, 826–831.CrossRefGoogle Scholar
Sosa, R., Hoffpauir, B., Rankin, M.L., Bruch, R.C., & Gleason, E.L. (2002). Metabotropic glutamate receptor 5 and calcium signaling in retinal amacrine cells. Journal of Neurochemistry 81, 973–983CrossRefGoogle Scholar
Singh, B.B., Lockwich, T., Bandyopadhyay, B., Liu, X., Bollimuntha, S., Brazer, S.C., Combs, C., Das, S., Leenders, M., Sheng, Z., Knepper, M., Ambudkar, S.V., & Ambudkar, I.S. (2004). VAMP-2-dependent exocytosis is involved in plasma membrane insertion of TRPC3 channels and contributes to agonist-stimulated Ca2+ influx. Molecular Cell 15, 635–646.CrossRefGoogle Scholar
Singh, B.B., Liu, X., Tang, J., Zhu, M.X., & Ambudkar, I.S. (2002). Calmodulin regulates Ca2+-dependent feedback inhibition of store-operated Ca2+ influx by interaction with a site in the C-terminus of TrpC1. Molecular Cell 9, 739–750.CrossRefGoogle Scholar
Singh, B.B., Zheng, C., Liu, X., Lockwich, T., Liao, D., Zhu, M., Birnbaumer, L., & Ambudkar, I.S. (2001). TRPC1 dependent enhancement of salivary gland fluid secretion: Role of store-operated calcium entry. FASEB Journal 15, 1652–1654.Google Scholar
Topp, K.S., Bisla, K., Saks, N.D., & Lavail. J.H. (1996). Centripetal transport of herpes simplex virus in human retinal pigment epithelial cells in vitro. Neuroscience 71, 1133–1144.CrossRefGoogle Scholar
Vollmer, G. & Layer, P.G. (1986). An in vitro model of proliferation and differentiation of the chick retina: Coaggregates of retinal and pigment epithelial cells. Journal of Neuroscience 6, 1885–1896.Google Scholar