Switch from ER-mitochondrial to SR-mitochondrial calcium coupling during muscle differentiation

Cell Calcium

Volumn 52, Issue 5, 2012, Pages 355-365

  Yi, Muqing ^a   Weaver, David ^a   Eisner, Verónica ^a   Várnai, Péter ^b   Hunyady, László ^b   Ma, Jianjie ^c   Csordás, György ^a   Hajnóczky, György ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Calcium signaling; Development; Mitochondria; Mitochondria associated membranes (Mam); Ryanodine receptor; Sarcoplasmic reticulum

Indexed keywords

CAFFEINE; CALCIUM ION; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; RYANODINE RECEPTOR 1; VASOPRESSIN;

ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL COUNT; CELL DIFFERENTIATION; CELL ELONGATION; CELL INTERACTION; CELL STIMULATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; INTRACELLULAR SIGNALING; MITOCHONDRION; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SARCOPLASMIC RETICULUM;

EID: 84866759005     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2012.05.012     Document Type: Article

References (62)

1. Shore G.C., Tata J.R. Two fractions of rough endoplasmic reticulum from rat liver. I: recovery of rapidly sedimenting endoplasmic reticulum in association with mitochondria. Journal of Cell Biology 1977, 72:714-725.
2. Rusinol A.E., Cui Z., Chen M.H., Vance J.E. A unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins. Journal of Biological Chemistry 1994, 269:27494-27502.
3. 2+ responses. Science 1998, 280:1763-1766.
4. Csordas G., Renken C., Varnai P., Walter L., Weaver D., Buttle K.F., Balla T., Mannella C.A., Hajnoczky G. Structural and functional features and significance of the physical linkage between ER and mitochondria. Journal of Cell Biology 2006, 174:915-921.
5. de Brito O.M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456:605-610.
6. Kornmann B., Currie E., Collins S.R., Schuldiner M., Nunnari J., Weissman J.S., Walter P. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 2009, 325:477-481.
7. 2+ channels. Journal of Cell Biology 2006, 175:901-911.
8. Hayashi T., Su T.P. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 2007, 131:596-610.
9. Wang H.J., Guay G., Pogan L., Sauve R., Nabi I.R. Calcium regulates the association between mitochondria and a smooth subdomain of the endoplasmic reticulum. Journal of Cell Biology 2000, 150:1489-1498.
10. Simmen T., Aslan J.E., Blagoveshchenskaya A.D., Thomas L., Wan L., Xiang Y., Feliciangeli S.F., Hung C.H., Crump C.M., Thomas G. PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO Journal 2005, 24:717-729.
11. Wang B., Nguyen M., Chang N.C., Shore G.C. Fis1, Bap31 and the kiss of death between mitochondria and endoplasmic reticulum. EMBO Journal 2011, 30:451-452.
12. Friedman J.R., Lackner L.L., West M., DiBenedetto J.R., Nunnari J., Voeltz G.K. ER tubules mark sites of mitochondrial division. Science 2011, 334:358-362.
13. Csordas G., Thomas A.P., Hajnoczky G. Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO Journal 1999, 18:96-108.
14. 2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 1993, 262:744-747.
15. Hajnoczky G., Robb-Gaspers L.D., Seitz M.B., Thomas A.P. Decoding of cytosolic calcium oscillations in the mitochondria. Cell 1995, 82:415-424.
16. 2+ channels. Molecular Cell 2010, 38:280-290.
17. Csordas G., Varnai P., Golenar T., Roy S., Purkins G., Schneider T.G., Balla T., Hajnoczky G. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Molecular Cell 2010, 39:121-132.
18. Franzini-Armstrong C. ER-mitochondria communication. How privileged?. Physiology (Bethesda) 2007, 22:261-268.
19. Franzini-Armstrong C., Protasi F., Ramesh V. Shape, size, and distribution of Ca(2+) release units and couplons in skeletal and cardiac muscles. Biophysical Journal 1999, 77:1528-1539.
20. Boncompagni S., Rossi A.E., Micaroni M., Beznoussenko G.V., Polishchuk R.S., Dirksen R.T., Protasi F. Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures. Molecular Biology of the Cell 2009, 20:1058-1067.
21. 2+ signaling in the heart. Journal of Cell Science 2009, 122:1005-1013.
22. Franzini-Armstrong C., Boncompagni S. The evolution of the mitochondria-to-calcium release units relationship in vertebrate skeletal muscles. Journal of Biomedicine and Biotechnology 2011, 2011:830573.
23. 2+ from sarcoplasmic reticulum to mitochondria in skeletal muscle. Journal of Biological Chemistry 2006, 281:1547-1554.
24. 2+ from sarcoplasmic reticulum to mitochondria in rat ventricular myocytes. Journal of Bioenergetics and Biomembranes 2000, 32:97-104.
25. Yi J., Ma C., Li Y., Weisleder N., Rios E., Ma J., Zhou J. Mitochondrial calcium uptake regulates rapid calcium transients in skeletal muscle during excitation-contraction (E-C) coupling. Journal of Biological Chemistry 2011, 286:32436-32443.
26. Eisner V., Parra V., Lavandero S., Hidalgo C., Jaimovich E. Mitochondria fine-tune the slow Ca(2+) transients induced by electrical stimulation of skeletal myotubes. Cell Calcium 2010, 48:358-370.
27. 2+ homeostasis in primary cultures of skeletal muscle myotubes. Molecular Biology of the Cell 1997, 8:129-143.
28. 2+ transfer between sarcoplasmic reticulum subdomains and the mitochondria in heart muscle. Journal of Biological Chemistry 2008, 283:32771-32780.
29. 2+ spark suppression in skeletal muscle. American Journal of Physiology. Cell Physiology 2011, 301(5):c1128-c1139.
30. 2+] in cardiac cells. EMBO Journal 2001, 20:4998-5007.
31. 2+-mediated cell death by the transcriptional coactivator PGC-1alpha. Cell Death and Differentiation 2006, 13:586-596.
32. Szalai G., Csordas G., Hantash B.M., Thomas A.P., Hajnoczky G. Calcium signal transmission between ryanodine receptors and mitochondria. Journal of Biological Chemistry 2000, 275:15305-15313.
33. Brillantes A.M., Bezprozvannaya S., Marks A.R. Developmental and tissue-specific regulation of rabbit skeletal and cardiac muscle calcium channels involved in excitation-contraction coupling. Circulation Research 1994, 75:503-510.
34. Takeshima H., Iino M., Takekura H., Nishi M., Kuno J., Minowa O., Takano H., Noda T. Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene. Nature 1994, 369:556-559.
35. Flucher B.E., Andrews S.B., Daniels M.P. Molecular organization of transverse tubule/sarcoplasmic reticulum junctions during development of excitation-contraction coupling in skeletal muscle. Molecular Biology of the Cell 1994, 5:1105-1118.
36. Takekura H., Flucher B.E., Franzini-Armstrong C. Sequential docking, molecular differentiation, and positioning of T-tubule/SR junctions in developing mouse skeletal muscle. Developmental Biology 2001, 239:204-214.
37. Nakayama H., Bodi I., Maillet M., DeSantiago J., Domeier T.L., Mikoshiba K., Lorenz J.N., Blatter L.A., Bers D.M., Molkentin J.D. The IP3 receptor regulates cardiac hypertrophy in response to select stimuli. Circulation Research 2010, 107:659-666.
38. 2+ transients and arrhythmias associated with cardiac hypertrophy. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:11406-11411.
39. 2+ signalling in the mammalian heart. Journal of Physiology 2007, 584:601-611.
40. Powell J.A., Carrasco M.A., Adams D.S., Drouet B., Rios J., Muller M., Estrada M., Jaimovich E. IP(3) receptor function and localization in myotubes: an unexplored Ca(2+) signaling pathway in skeletal muscle. Journal of Cell Science 2001, 114:3673-3683.
41. Pacher P., Csordas P., Schneider T., Hajnoczky G. Quantification of calcium signal transmission from sarco-endoplasmic reticulum to the mitochondria. Journal of Physiology 2000, 529(Pt 3):553-564.
42. 2+ marks: miniature calcium signals in single mitochondria driven by ryanodine receptors. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:2380-2385.
43. Comelli M., Domenis R., Bisetto E., Contin M., Marchini M., Ortolani F., Tomasetig L., Mavelli I. Cardiac differentiation promotes mitochondria development and ameliorates oxidative capacity in H9c2 cardiomyoblasts. Mitochondrion 2011, 11:315-326.
44. 2+. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:3197-3202.
45. 2+ release channels. Journal of General Physiology 1997, 110:749-762.
46. Yi M., Weaver D., Hajnoczky G. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. Journal of Cell Biology 2004, 167:661-672.
47. Pacher P., Hajnoczky G. Propagation of the apoptotic signal by mitochondrial waves. EMBO Journal 2001, 20:4107-4121.
48. Beutner G., Sharma V.K., Giovannucci D.R., Yule D.I., Sheu S.S. Identification of a ryanodine receptor in rat heart mitochondria. Journal of Biological Chemistry 2001, 276:21482-21488.
49. Vendelin M., Beraud N., Guerrero K., Andrienko T., Kuznetsov A.V., Olivares J., Kay L., Saks V.A. Mitochondrial regular arrangement in muscle cells: a " crystal-like" pattern. American Journal of Physiology. Cell Physiology 2005, 288:C757-C767.
50. Birkedal R., Shiels H.A., Vendelin M. Three-dimensional mitochondrial arrangement in ventricular myocytes: from chaos to order. American Journal of Physiology. Cell Physiology 2006, 291:C1148-C1158.
51. De Palma C., Falcone S., Pisoni S., Cipolat S., Panzeri C., Pambianco S., Pisconti A., Allevi R., Bassi M.T., Cossu G., Pozzan T., Moncada S., Scorrano L., Brunelli S., Clementi E. Nitric oxide inhibition of Drp1-mediated mitochondrial fission is critical for myogenic differentiation. Cell Death and Differentiation 2010, 17:1684-1696.
52. Chen H., Vermulst M., Wang Y.E., Chomyn A., Prolla T.A., McCaffery J.M., Chan D.C. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010, 141:280-289.
53. Porter G.A., Makuck R.F., Rivkees S.A. Reduction in intracellular calcium levels inhibits myoblast differentiation. Journal of Biological Chemistry 2002, 277:28942-28947.
54. 2+-stimulated mitochondrial biogenesis in muscle fibres of cold-acclimated mice. Journal of Physiology 2010, 588:4275-4288.
55. Cereghetti G.M., Stangherlin A., Martins de Brito O., Chang C.R., Blackstone C., Bernardi P., Scorrano L. Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:15803-15808.
56. Protasi F., Franzini-Armstrong C., Allen P.D. Role of ryanodine receptors in the assembly of calcium release units in skeletal muscle. Journal of Cell Biology 1998, 140:831-842.
57. Park M.Y., Park W.J., Kim D.H. Expression of excitation-contraction coupling proteins during muscle differentiation. Molecules and Cells 1998, 8:513-517.
58. 2+ signaling. Biochimica et Biophysica Acta 2006, 1763:442-449.
59. 2+ signals into mitochondria. Journal of Biological Chemistry 2005, 280(49):40892-40900.
60. 2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:20728-20733.
61. 2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 2009, 136:163-174.
62. Macaskill A.F., Rinholm J.E., Twelvetrees A.E., Arancibia-Carcamo I.L., Muir J., Fransson A., Aspenstrom P., Attwell D., Kittler J.T. Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 2009, 61:541-555.