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Voltage-Operated Calcium Channel Heterogeneity in Pancreatic β Cells: Physiopathological Implications

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Abstract

Voltage-operated calcium channels play crucial roles in stimulus-secretion coupling in pancreatic β cells. A growing body of evidence indicates that these channels in β cells are heterogeneous. In particular, not all the high-threshold calcium channels expressed belong to the best known L-type. In rat insulinoma cells, for example, L, N, and P/Q-type channels are present, while in human β cells L-type and P/Q-type dominate. Where present, N-type and P/Q-type channels participate, alongside with the dominant L-type, in the control of sugar- or depolarization-induced hormone release. Distinct biophysical properties and selective modulation of the channel subtypes are likely to play important physiological roles. T-type channels are involved in beta cell apoptosis, while calcium channel autoantibodies recognizing high-threshold channels in β cells, have been described both in neurological and diabetic patients. Subtype-selective calcium channel drugs have the potential for being beneficial in beta cell pathological states.

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References

  • Abrahamsson, H., Berggren, P. O., and Hellman, B., (1984). Am. J. Physiol. 247, E719–E725. Endocrin. Metab. 10.

    PubMed  Google Scholar 

  • Aicardi, G., Pollo, A., Sher, E., and Carbone, E., (1991). FEBS Lett. 281, 201–204.

    PubMed  Google Scholar 

  • Ashcroft, F. M., Kelly, R. P., and Smith, P. A., (1990). Pflügers Arch. 415, 504–506.

    Google Scholar 

  • Ashcroft, F. M., and Rorsman, P., (1991). Prog. Biophys. Mol. Biol. 54, 87–143.

    Google Scholar 

  • Barnett, D. W., Pressel, D. M., and Misler, S., (1995). Pflügers Arch. 431, 272–282.

    Google Scholar 

  • Bertram, R., and Sherman, A., (2000). J. Biosci. 25, 197–209.

    PubMed  Google Scholar 

  • Bhattacharjee, A., Whitehurst, R. M., Jr., and Zhang, M., (1997). Endocrinology, 138, 3735–3740.

    PubMed  Google Scholar 

  • Bokvist, K., Eliasson, L., Ammala, C., Renstrom, E., and Rorsman, P., (1995). EMBO J. 14, 50–57.

    PubMed  Google Scholar 

  • Boschero, A. C., Tombaccini, D., and Atwater, I., (1988). FEBS Lett. 236, 375–379.

    PubMed  Google Scholar 

  • Boschero, A. C., Tombaccini, D., and Atwater, I., (1988). FEBS Lett. 236, 375–379.

    PubMed  Google Scholar 

  • Bourinet, E., Soong, T. W., Sutton, K., Slaymaker, S., Mathews, E., Monteil, A., Zamponi, G. W., Nargeot, J., and Snutch, T. P., (1999). Nat. Neurosci. 2, 407–415.

    PubMed  Google Scholar 

  • Carbone, E., Sher, E., and Clemanti, F., (1990). Pflügers Arch. 416, 170–179.

    Google Scholar 

  • Carbone, E., and Swandulla, D., (1989). Prog. Biophys. Mol. Biol. 54, 31–58.

    PubMed  Google Scholar 

  • Castellan, A., Wei, X., Birnbaumer, L., and Perez-Reyes, E., (1993). J. Biol. Chem. 268, 3450–3455.

    PubMed  Google Scholar 

  • Codignola, A., Tarroni, P., Clementi, F., Pollo, A., Lovallo, M., Carbone, E., and Sher, E., (1993). J. Biol. Chem. 268, 26240–26247.

    Google Scholar 

  • Cook, D. L., Satin, L. S., and Hopkins, W. F., (1991). Trends Neurosci. 9, 411–414.

    Google Scholar 

  • Davalli, A. M., Biancardi, E., Pollo, A., Socci, C., Pontiroli, A. E., Poza, G., Clementi, F., Sher, E., and Carbone, E., (1996). J. Endocrinol. 150, 195–203.

    PubMed  Google Scholar 

  • Feng, Z. P., Hamid, J., Doering, C., Bosey, G. M., Snutch, T. P., and Zamponi, G. W., (2001). J. Biol. Chem. 276, 15728–15735.

    PubMed  Google Scholar 

  • Findlay, I., and Dunne, M. J., (1985). FEBS. Lett. 189, 281–285.

    PubMed  Google Scholar 

  • Gilon, P., Yakel, J., Gromada, J., Zhu, Y., Henquin, J. C., and Rorsman, P., (1997). J. Physiol. 499, 65–76.

    PubMed  Google Scholar 

  • Grabsch, H., Pereverzev, A., Weiergraber, M., Schramm, M., Henry, M., Vajna, R., Beattie, R. E., Volsen, S. G., Klockner, U., Hescheler, J., and Schneider, T., (1999). J. Histochem. Cytochem. 47, 981–994.

    PubMed  Google Scholar 

  • Gromada, J., Bokvist, K., Ding, W. G., Barg, S., Buschard, K., Renstrom, E., and Rorsman, P., (1997). J. Gen. Physiol. 110, 217–228.

    PubMed  Google Scholar 

  • Henquin, J. C., Schmeer, W., Nenquin, M., and Meissner, H. P., (1985). Biochem. Biophys. Res. Commun. 131, 980–986.

    PubMed  Google Scholar 

  • Hopkins, W. F., Satin, L. S., and Cook, D. L., (1991). J. Membr. Biol. 119, 229–239.

    PubMed  Google Scholar 

  • Horwath, A., Szabadkai, G., Varnai, P., Aranyi, T., Wollheim, C. B., Spat, A., and Enyedi, P., (1998). Cell Calcium, 23, 33–42.

    PubMed  Google Scholar 

  • Ihara, Y., Yamada, Y., Fujii, Y., Gonoi, T., Yano, H., Yasuda, K., and Inagaki, N., Seino S., (1995). Mol. Endocrinol. 9, 121–130.

    PubMed  Google Scholar 

  • Iwashima, Y., Pugh, W., Depaoli, A. M., Takeda, J., Seino, S., Bell, G. I., Polonsky, K. S., (1993). Diabetes, 42, 948–955.

    PubMed  Google Scholar 

  • Juntii-Berggren, L., Larsson, O., Rorsman, P., Ammala, C., Bokvist, K., Wahlander, K., Nicotera, P., Dypbukt, J., Orrenius, S., Hallberg, A., and Berggren, P. O., (1993). Science, 261, 86–90.

    PubMed  Google Scholar 

  • Kato, S., Ishida, H., Tsuura, Y., Okamoto, Y., Tsuji, K., Horie, M., Okada, H., and Seino, Y., (1994). Metabolism, 43, 1395–1400.

    PubMed  Google Scholar 

  • Kato, S., Ishida, H., Tsuura, Y., Tsuji, K., Nishimura, M., Horie, M., Taminato, T., Ikehara, S., Okada, H., Ikeda, H., Okada, Y., and Seino, Y., (1996). J. Clin. Invest. 97, 2417–2425.

    PubMed  Google Scholar 

  • Kelly, R. P., Sutton, R., and Ashcroft, F. M., (1991). J. Physiol. 443, 175–192.

    PubMed  Google Scholar 

  • Kim, S. J., Sung, J. J., and Park, Y. S., (1998). Biophy. Res. Commun. 243, 874–884.

    Google Scholar 

  • Komatsu, M., Yokokawa, N., Takeda, T., Nagasawa, Y., Aizawa, T., and Yamada, Y., (1989). Endocrinology, 125, 2008–2014.

    PubMed  Google Scholar 

  • Ligon, B., Boyd, A. E. III., and Dunlap, K., (1998). J. Biol. Chem. 273, 13905–13911.

    PubMed  Google Scholar 

  • Llinas, R., Sugimori, M., and Silver, R. B., (1995). Neuropharmacology, 34, 1443–1451.

    PubMed  Google Scholar 

  • Magnelli, V., Grassi, C., Parlatore, E., Sher, E., and Crabone, E., (1996). FEBS Lett. 387, 47–52.

    PubMed  Google Scholar 

  • Magnelli, V., Pollo, A., Sher, E., and Carbone, E., (1995). Pflügers Arch. 429, 762–771.

    Google Scholar 

  • Malaisse-Lagae, F., Mathias, P. C. F., and Malaisse, W. J., (1984). Biochem. Biophys. Res. Commun. 123, 1062–1068.

    PubMed  Google Scholar 

  • Mansvelder, H. D., and Kits, K. S., (2000). Prog. Neurobiol. 62, 427–441.

    PubMed  Google Scholar 

  • Mansvelder, H. D., Stoof, J. C., and Kits, K. S., (1996). Eur. J. Pharmacol. 311, 293–304.

    PubMed  Google Scholar 

  • Marchetti, C., Amico, C., Podesta, D., and Robello, M., (1994). Eur. Biophys. J. 23, 51–58.

    PubMed  Google Scholar 

  • Mintz, I. M., Venema V. J., Swiderk, K. M., Lee, T. D., Bean, B. P., and Adams, M. E., (1992). Nature, 355, 827–829.

    PubMed  Google Scholar 

  • Misler, S., Barnett, D. W., Pressel, D. M., Gillis, K. D., Scharp, D. W., and Falke, L. C., (1992). Diabetes 41, 662–670.

    PubMed  Google Scholar 

  • Namkung, Y., Skrypnyk, N., Jeong, M. J., Lee, T., Lee, M. S., Kim, H. L., Chin, H., Suh, P. G., Kim, S. S., and Shin, H. S., (2001). J. Clin. Invest. 108, 1015–1022.

    PubMed  Google Scholar 

  • Olivera, B. M., Rivier, J., Clark, G., Ramilo, C. A., Corpuz, G. P., Abbogadie, F. C., Mena, E. E., Woodward, S. R., Hillyard, D. R., and Cruz, L. J., (1990). Science, 249, 257–263.

    PubMed  Google Scholar 

  • Passafaro, M., Codignola, A., Rogers, M., Cooke, L., and Sher, E., (2000). Pharmacol. Res. 41, 325–334.

    PubMed  Google Scholar 

  • Perez-Reyes, E., Castellano, A., Kim, H. S., Bertrand, P., Baggstrom, E., Lacerda, A. E., Wei, X., and Birnbaumer, L., (1992). J. Biol. Chem. 267, 1792–1797.

    PubMed  Google Scholar 

  • Perez-Reyes, E., Cribbs, L. L., Daud, A., Lacerda, A. E., Barclay, J., Williamson, M. P., Fox, M., Rees, M., and Lee, L.-H., (1998). Nature, 391, 896–900.

    PubMed  Google Scholar 

  • Petersen, O. H., and Findlay, I., (1987). Physiol. Rev. 67, 1054–1116.

    PubMed  Google Scholar 

  • Piedras-Renteira, E. S., and Tsien, R. W., (1998). Proc. Natl. Acad. Sci. U.S.A. 95, 7760–7765.

    PubMed  Google Scholar 

  • Plant, T. D., (1988). J. Physiol. 404, 731–747.

    PubMed  Google Scholar 

  • Pollo, A., Lovallo, M., Biancardi, E., Sher, E., Socci, C., and Carbone, E., (1993). Pflügers Arch. 423, 462–471.

    Google Scholar 

  • Prentki, M., and Matschinsky, F. M., (1987). Physiol. Rev. 67, 1185–1248.

    PubMed  Google Scholar 

  • Pressel, D. M., and Misler, S., (1991). J. Member. Biol. 124, 239–253.

    Google Scholar 

  • Qian, W. J., and Kennedy, R. T., (2001). Biochem. Biophys. Res. Commun. 286, 315–321.

    PubMed  Google Scholar 

  • Ramanadham, S., and Turk, J., (1994). Cell Calcium, 15, 259–264.

    PubMed  Google Scholar 

  • Rojas, E., Hidalgo, J., Carrol, P. B., Li, M. X., and Atwater, I., (1990). FEBS Lett. 261, 265–270.

    PubMed  Google Scholar 

  • Rorsman, P., and Trube, G., (1986). J. Physiol. 374, 531–550.

    PubMed  Google Scholar 

  • Safayhi, H., Haase, H., Kramer, U., Bihlmayer, A., Roenfeldt, M., Ammon, H. P. T., Froschmayr, M., Cassidy, T. N., Morano, I., Ahlijanian, M. K., and Striessnig, J., (1997). Mol. Endocrinol. 11, 619–629.

    PubMed  Google Scholar 

  • Sala, S., and Matteson, D. R., (1990). Biophys. J. 58, 567–571.

    PubMed  Google Scholar 

  • Satin, L. S., (2000). Endocrine, 13, 251–262.

    PubMed  Google Scholar 

  • Satin, L. S., and Cook, D. L., (1988). Pflügers Arch. 411, 401–409.

    Google Scholar 

  • Satin, L. S., Tavalin, S. J., Kinard, T. A., and Teague, J., (1995). Endocrinology, 136, 4589–4601.

    PubMed  Google Scholar 

  • Seino, S., Chen, L., Seino, M., Blondel, O., Takeda, J., Johnson, J. H., and Bell, G. I., (1992). Proc. Natl. Acad. Sci. U.S.A. 89, 584–588.

    PubMed  Google Scholar 

  • Sher, E., (1997). Cell Biol. Int. 12, 779–781.

    Google Scholar 

  • Sher, E., Biancardi, E., Pollo, A., Carbone, E., Li, g., Wollheim, C. B., and Clementi, F., (1992). Eur. J. Pharmacol. 216, 407–414.

    PubMed  Google Scholar 

  • Sher, E., and Clementi, F., (1991). Neuroscience, 42, 301–307.

    PubMed  Google Scholar 

  • Sher, E., Codignola, A., Rogers, M., and Richmond, J., (1996). FEBS Lett. 385, 176–180.

    PubMed  Google Scholar 

  • Sher, E., Giovannini, F., Boot, J., and Lang, B., (2000). Biochimie. 82, 927–936.

    PubMed  Google Scholar 

  • Stanley, E. F., (1997). Trends Neurosci. 20, 404–409.

    PubMed  Google Scholar 

  • Tsien, R. W., Lipscombe, D., Madison, D. V., Bley, K. R., and Fox, A. P., (1988). Trends Neurosci. 11, 431–436.

    PubMed  Google Scholar 

  • Vajna, R., Klockner, U., Pereverzev, A., Weiergraber, M., Chen, X., Miljanich, G., Klugbauer, N., Hescheler, J., Perez-Reyes, E., and Schneider, T., (2001). Eur. J. Biochem. 268, 1066–1075.

    PubMed  Google Scholar 

  • Volsen, S. G., Day, N. C., McCormack, A. L., Smith, W., Craig, P. J., Beattie, R., Ince, P. G., Shaw, P. J., Ellis, S. B., Gillespie, A., Harpold, M. M., and Lodge, D., (1995). Mol. Brain Res. 34, 271–282.

    PubMed  Google Scholar 

  • Wang, L., Bhattacharjee, A., Fu, J., and Li, M., (1996). Diabetes, 45, 1678–1683.

    PubMed  Google Scholar 

  • Wang, L., Bhattacharjee, A., Zuo, Z., Hu, F., Honkanen, R. E., Berggren, P. O., and Li, M., (1999). Endocrinology, 140, 1200–1204.

    PubMed  Google Scholar 

  • Wiser, O., Trus, M., Hernandez, A., Renstrom, E., Barg, S., Rorsman, P., and Atlas, D., (1999). Proc. Natl. Acad. Sci. U.S.A. 96, 248–253.

    PubMed  Google Scholar 

  • Wollheim, C. B., and Pozzan, T., (1984). J. Biol. Chem. 259, 2262–2267.

    PubMed  Google Scholar 

  • Wollheim, C. B., and Sharp, G. W. G., (1981). Physiol. Rev. 61, 914–973.

    PubMed  Google Scholar 

  • Yaney, G. C., Wheeler, M. B., Wei, X., Perez-Reyes, E., Birnbaumer, L., Boyd, A. E. III., and Moss, L. G., (1992). Mol. Cell Endocrinol. 6, 2143–2152.

    Google Scholar 

  • Yang, S. N., Larsson, O., Branstrom, R., Bertorello, A. M., Leibiger, B., Leibiger, I. B., Moede, T., Kohler, M., Meister, B., and Berggren, P. O., (1999). Proc. Natl. Acad. Sci. U.S.A. 96, 10164–10169.

    PubMed  Google Scholar 

  • Zhuang, H., Bhattacharjee, A., Hu, F., Zhang, M., Goswami, T., Wang, L., Wu, S., Berggren, P. O., and Li, M., (2000). Diabetes, 49, 59–64.

    PubMed  Google Scholar 

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Sher, E., Giovannini, F., Codignola, A. et al. Voltage-Operated Calcium Channel Heterogeneity in Pancreatic β Cells: Physiopathological Implications. J Bioenerg Biomembr 35, 687–696 (2003). https://doi.org/10.1023/B:JOBB.0000008032.49504.48

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