Cyclic ADP-ribose increases Ca2+ removal in smooth muscle

Journal of Cell Science - Tập 116 Số 21 - Trang 4291-4306 - 2003
Karen N. Bradley1, Susan Currie1, Debbi MacMillan1, T C Muir1, John G. McCarron1
1Institute of Biomedical and Life Sciences, Neuroscience and Biomedical Systems, West Medical Building, University of Glasgow, Glasgow G12 8QQ, UK.

Tóm tắt

Ca2+ release via ryanodine receptors (RyRs) is vital in cell signalling and regulates diverse activities such as gene expression and excitation-contraction coupling. Cyclic ADP ribose (cADPR), a proposed modulator of RyR activity, releases Ca2+ from the intracellular store in sea urchin eggs but its mechanism of action in other cell types is controversial. In this study, caged cADPR was used to examine the effect of cADPR on Ca2+ signalling in single voltage-clamped smooth muscle cells that have RyR but lack FKBP12.6, a proposed target for cADPR. Although cADPR released Ca2+ in sea urchin eggs (a positive control), it failed to alter global or subsarcolemma [Ca2+]c, to cause Ca2+-induced Ca2+ release or to enhance caffeine responses in colonic myocytes. By contrast, caffeine (an accepted modulator of RyR) was effective in these respects. The lack of cADPR activity on Ca2+ release was unaffected by the introduction of recombinant FKBP12.6 into the myocytes. Indeed in western blots, using brain membrane preparations as a source of FKBP12.6, cADPR did not bind to FKBPs, although FK506 was effective. However, cADPR increased and its antagonist 8-bromo-cADPR slowed the rate of Ca2+ removal from the cytoplasm. The evidence indicates that cADPR modulates [Ca2+]c but not via RyR; the mechanism may involve the sarcolemma Ca2+ pump.

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Tài liệu tham khảo

Aarhus, R., Gee, K. and Lee. H. C. (1995). Caged cyclic ADP-ribose synthesis and use. J. Biol. Chem.270, 7745-7749.

Baughman, G., Wiederrecht, G. J., Chang, F., Martin, M. M. and Bourgeois, S. (1997). Tissue distribution and abundance of human FKBP51, an FK506-binding protein that can mediate calcineurin inhibition. Biochem. Biophys. Res. Comm.232, 437-443.

Benham, C. D. and Bolton, T. B. (1986). Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J. Physiol.381, 385-406.

Bielefeldt, K., Sharma, R. V., Whiteis, C., Yedidag, E. and Abboud, F. M. (1997). Tacrolimus (FK506). modulates calcium release and contractility of intestinal smooth muscle. Cell Calcium22, 507-514.

Bolton, T. B., Prestwich, S. A., Zholos, A. V. and Gordienko, D. V. (1999). Excitation-contraction coupling in gastrointestinal and other smooth muscles. Annu. Rev. Physiol.61, 85-115.

Bradley, K. N., Flynn, E. R. M., Muir, T. C. and McCarron, J. G. (2002). Ca2+ regulation in guinea-pig colonic smooth muscle: the role of the Na+-Ca2+ exchanger and the sarcoplasmic reticulum. J. Physiol.538, 465-482.

Brillantes, A. M. B., Ondrias, K., Scott, A., Kobrinsky, E., Ondriasova, E., Moschella, M. C., Jayaraman, T., Landers, M., Ehrlich, B. E. and Marks, A. R. (1994). Stabilization of calcium-release channel (ryanodine receptor) function by FK506-binding protein. Cell77, 513-523.

Bultynck, G., de Smedt, P., Rossi, D., Callewart, G., Missiaen, L., Sorrentino, V., de Smedt, H. and Parys, J. B. (2001a). Characterisation and mapping of the 12 kDa FK506-binding protein (FKBP12)-binding site on different isoforms of the ryanodine receptor and of the inositol 1,4,5-trisphosphate receptor. Biochem. J.354, 413-422.

Bultynck, G., Rossi, D., Callewaert, G., Missiaen, L., Sorrentino, V., Parys, J. B. and DeSmedt, H. (2001b). The conserved sites for the FK506-binding proteins in ryanodine receptors and inositol 1,4,5-trisphosphate receptors are structurally different. J. Biol. Chem.276, 47715-47724.

Cancela, J. M., Mogami, H., Tepikin, A. V. and Petersen, O. H. (1998). Intracellular glucose switches between cyclic ADP-ribose and inositol trisphosphate triggering of cytosolic Ca2+ spiking. Curr. Biol.8, 865-868.

Cannell, M. B., Cheng, H. and Lederer, W. J. (1994). Spatial non-uniformities in [Ca2+]i during excitation-contraction coupling in cardiac myocytes. Biophys. J.67, 1942-1956.

Carmody, M., Mackrill, J. J., Sorrentino, V. and O'Neill, C. (2001). FKBP12 associates tightly with the skeletal muscle type 1 ryanodine receptor, but not with other intracellular calcium release channels. FEBS Lett.505, 97-102.

Copello, J. A., Jeyakumar, L. and Fleischer, S. (1999). FK binding proteins (FKBP12 and FKBP12.6) do not modulate channel activity of ryanodine receptor isoform 3 (RyR3) from bovine diaphragm muscle (BDM). Biophys. J.76, A469.

Copello, J. A., Qi, Y., Jeyakumar, L. H., Ogunbunmi, E. and Fleischer, S. (2001). Lack of effect of cADP-ribose and NAADP on the activity of skeletal muscle and heart ryanodine receptors. Cell Calcium30, 269-284.

Cui, Y., Galione, A. and Terrar, D. A. (1999). Effects of photoreleased cADP-ribose on calcium transients and calcium sparks in myocytes isolated from guinea-pig and rat ventricle. Biochem. J.342, 269-273.

Currie, S. and Smith, G. L. (1999). Enhanced phosphorylation of phospholamban and downregulation of sarco/endoplasmic reticulum Ca2+ ATPase type 2 (SERCA 2) in cardiac sarcoplasmic reticulum from rabbits with heart failure. Cardiovasc. Res.41, 135-146.

Endo, M., Tanaka, M. and Ogawa, I. (1970). Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature228, 34-36.

Fabiato, A. (1983). Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am. J. Physiol.245, C1-C14.

Flynn, E. R. M., Bradley, K. N., Muir, T. C. and McCarron, J. G. (2001). Functionally-separate intracellular Ca2+ stores in smooth muscle. J. Biol. Chem.276, 36411-36418.

Fruen, B. R., Mickelson, J. R., Shomer, N. H., Velez, P. and Louis, C. F. (1994). Cyclic ADP-ribose does not affect cardiac or skeletal-muscle ryanodine receptors. FEBS Lett.352, 123-126.

Fukushi, Y., Kato, I., Takasawa, S., Sasaki, T., Ong, B. H., Sato, M., Ohsaga, A., Sato, K., Shirato, K., Okamoto, H. and Maruyama, Y. (2001). Identification of cyclic ADP-ribose-dependent mechanisms in pancreatic muscarinic Ca2+ signaling using CD38 knockout mice. J. Biol. Chem.276, 649-655.

Galione, A. and Sethi, J. (1996). Cyclic ADP-ribose and calcium signalling. In Biochemistry of Smooth Muscle Contraction (ed. M. Barany). pp. 295-305. Academic Press.

Galione, A., Lee, H. C. and Busa, W. B. (1991). Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science.253, 1143-1146.

Gillot, I. and Whitaker, M. (1994). Calcium signals in and around the nucleus in sea urchin eggs. Cell Calcium16, 269-278.

Guerrero-Hernandez, A., Gomez-Viquez, L., Guerrero-Serna, G. and Rueda, A. (2002). Ryanodine receptors in smooth muscle. Frontiers Biosci.7, D1676-D1688.

Guo, X. Q., Laflamme, M. A. and Becker, P. L. (1996). Cyclic ADP-ribose does not regulate sarcoplasmic reticulum Ca2+ release in intact cardiac myocytes. Circ. Res.79, 147-151.

Iino, S., Cui, Y., Galione, A. and Terrar, D. (1997). Actions of cADP-ribose and its antagonists on contraction in guinea pig isolated ventricular myocytes – influence of temperature. Circ. Res.81, 879-884.

Iizuka, K., Yoshii, A., Dobashi, K., Horie, T., Mori, M. and Nakazawa, T. (1998). InsP3, but not novel Ca2+ releasers, contributes to agonist-initiated contraction in rabbit airway smooth muscle. J. Physiol.511, 915-933.

Kannan, M. S., Fenton, A. M., Prakash, Y. S. and Sieck, G. C. (1996). Cyclic ADP-ribose stimulates sarcoplasmic reticulum in porcine coronary smooth muscle. Am. J. Physiol.270, H801-H806.

Kuemmerle, J. F. and Makhlouf, G. M. (1995). Agonist-stimulated cyclic ADP ribose. Endogenous modulator of Ca(2+)-induced Ca2+ release in intestinal longitudinal muscle. J. Biol. Chem.270, 25488-25494.

Lahouratate, P., Guibert, J. and Faivre, J. F. (1997). cADP-ribose releases Ca2+ from cardiac sarcoplasmic reticulum independently of ryanodine receptor. Am. J. Physiol.273, H1082-H1089.

Lee, H. C. (2001). Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Annu. Rev. Pharmacol. Toxicol.41, 317-345.

Lee, H. C., Aarhus, R. and Walseth, T. F. (1993). Calcium mobilisation by dual receptors during fertilisation of sea urchin eggs. Science261, 352-355.

Lee, H. C., Aarhus, R., Graeff, R., Gurnack, M. E. and Walseth, T. F. (1994). Cyclic ADP ribose activation of the ryanodine receptor is mediated by calmodulin. Nature370, 307-309.

Leite, M. F., Burgstahler, A. D. and Nathanson, M. H. (2002). Ca2+ waves require sequential activation of inositol trisphosphate receptors and ryanodine receptors in pancreatic acini. Gastroenterology122, 415-427.

Li, N., Teggatz, E. G., Li, P.-L., Allaire, R. and Zuo, A.-P. (2000). Formation and actions of cyclic ADP-ribose in renal microvessels. Microvasc. Res.60, 149-159.

Li, P., Tang, W.-X., Valdivia, H. H., Zou, A. P. and Campbell, W. B. (2001). cADP-ribose activates reconstituted ryanodine receptors from coronary arterial smooth muscle. Am. J. Physiol.280, H208-H215.

Lukyanenko, V., Gyorke, I., Wiesner, T. F. and Gyorke, S. (2001). Potentiation of Ca2+ release by cADPR-ribose in the heart is mediated by enhanced SR Ca2+ uptake into the sarcoplasmic reticulum. Circ. Res.89, 614-622.

Marks, A. R. (1996). Cellular functions of immunophilins. Physiol. Rev.76, 631-649.

Marx, S. O., Reiken, S., Hisamatsu, Y., Jayaraman, T., Burkhoff, D., Rosemblit, N. and Marks, A. R. (2000). PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell101, 365-376.

McCarron, J. G. and Muir, T. C. (1999). Mitochondrial regulation of the cytosolic Ca2+ concentration and the InsP3-sensitive Ca2+ store in guinea-pig colonic smooth muscle. J. Physiol.516, 149-161.

McCarron, J. G., Flynn, E. R. M., Bradley, K. N. and Muir, T. C. (2000). Two pathways mediate InsP3-sensitive store refilling in guinea-pig colonic smooth muscle. J. Physiol.525, 113-124.

McCarron, J. G., Craig, J. W., Bradley, K. N. and Muir, T. C. (2002). Agonist-induced phasic and tonic responses in smooth muscle are mediated by InsP3. J. Cell Sci.115, 2207-2218.

Missiaen, L., Parys, J. B., DeSmedt, H., Sienaert, I., Sipma, H., Valingen, S., Maes, K., Kunzelmann, K. and Casteels, R. (1998). Inhibition of inositol trisphosphate-induced calcium release by cyclic ADP-ribose in A7r5 smooth muscle cells and in 16HBE14o-bronchial mucosal cells. Biochem. J.329, 489-495.

Moore, E. D. W., Becker, P. L., Fogarty, K. E., Williams, D. A. and Fay, F. S. (1990). Ca2+ imaging in single living cells: theoretical and practical issues. Cell Calcium11, 157-179.

Morrissette, J., Heisermann, G., Cleary, J., Ruoho, A. and Coronado, R. (1993). Cyclic ADP-ribose induced Ca2+ release in rabbit skeletal-muscle sarcoplasmic-reticulum. FEBS Lett.330, 270-274.

Nixon, G. F., Mignery, G. A. and Somylo, A. V. (1994). Immunogold localization of inositol 1,4,5-trisphosphate receptors and characterization of ultrastructural features of the sarcoplasmic reticulum in phasic and tonic smooth muscle. J. Muscle Res. Cell Motil.15, 682-700.

Noguchi, N., Takasawa, S., Nata, K., Tohgo, A., Kato, I., Ikehata, F., Yonekura, H. and Okamoto, H. (1997). Cyclic ADP-ribose binds to FK506-binding protein 12.6 to release Ca2+ from islet microsomes. J. Biol. Chem.272, 3133-3136.

Petersen, O. H. and Cancela, J. M. (1999). New Ca2+-releasing messengers: are they important in the nervous system. Trends Neurol. Sci.22, 488-494.

Prakash, Y. S., Kannan, M. S., Walseth, T. F. and Sieck, G. C. (1998). Role of cyclic ADP-ribose in the regulation of [Ca2+]c in porcine tracheal smooth muscle. Am. J. Physiol.274, C1653-C1660.

Prakash, Y. S., Kannan, M. S., Walseth, T. F. and Sieck, G. C. (2000). cADP ribose and [Ca2+]i regulation in rat cardiac myocytes. Am. J. Physiol.279, H1482-H1489.

Prestle, J., Janssen, P. M. L., Janssen, A. P., Zeitz, O., Lehnart, S. E., Bruce, L., Smith, G. L. and Hasenfuss, G. (2001). Overexpression of FK506-binding protein FKBP12.6 in cardiomyocytes reduces ryanodine receptor-mediated Ca2+ leak from the sarcoplasmic reticulum and increases contractility. Circ. Res.88, 188-194.

Sanders, K. M. (2001). Invited review: mechanisms of calcium handling in smooth muscles. J. Appl. Physiol.91, 1438-1449.

Schatzmann, H. J. (1989). The calcium pump of the surface membrane and of the sarcoplasmic reticulum. Annu. Rev. Physiol.51, 473-485.

Sitsapesan, R., McGarry, S. J. and Williams, A. J. (1994). Cyclic ADP-ribose competes with ATP for the adenine nucleotide binding site on the cardiac ryanodine receptor Ca2+ release channel. Circ. Res.75, 596-600.

Stull, J. T., Kamm, K. E. and Taylor, D. A. (1988). Calcium control of smooth muscle contractility. Am. J. Med. Sci.296, 241-245.

Tang, W.-X., Chen, Y.-F., Zou, A.-P., Campbell, W. and Li, P.-L. (2002). Role of FKBP12.6 in cADPR-induced activation of reconstituted ryanodine receptors from arterial smooth muscle. Am. J. Physiol.282, H1304-H1310.

Thorn, P., Gerasimenko, O. and Petersen, O. H. (1994). Cyclic ADP-ribose regulation of ryanodine receptors involved in agonist-evoked cytosolic Ca2+ oscillations in pancreatic acinar-cells. EMBO J.13, 2038-2043.

Timerman, A. P., Onoue, H., Xin, H. B., Barg, S., Copello, J., Wiederrecht, G. and Fleischer, S. (1996). Selective binding of FKBP12.6 by the cardiac ryanodine receptor. J. Biol. Chem.271, 20385-20391.

Vanlingen, S., Sipma, H., de Smet, P., Callewaert, G., Missiaen, L., de Smedt, H. and Parys, J. B. (2001). Modulation of inositol 1,4,5-trisphosphate binding to the various inositol 1,4,5-trisphosphate receptor isoforms by thimerosal and cyclic ADP-ribose. Biochem. Pharmacol.61, 803-809.

Walseth, T. F. and Lee, H.-C. (1993). Synthesis and characterisation of antagonists of cyclic-ADP-ribose-induced Ca2+ release. Biochem. Biophys. Acta1178, 235-242.

Walseth, T. F., Aarhus, R., Kerr, J. A. and Lee, H. C. (1993). Identification of cyclic ADP-ribose-binding proteins by photoaffinity-labeling. J. Biol. Chem.268, 26686-26691.

Xin, H. B., Senbonmatsu, T., Cheng, D. S., Wang, X. Y., Copello, J. A., Collier, M. L., Deng, K. Y., Jeyakumar, L. H., Magnuson, M. A., Inagami, T. et al. (2002). Oestrogen protects FKBP12.6 null mice from cardiac hypertrophy. Nature416, 334-338.