Characterization of ryanodine receptor type 1 single channel activity using "on-nucleus" patch clamp

Cell Calcium

Volumn 56, Issue 2, 2014, Pages 96-107

  Wagner, Larry E ^a   Groom, Linda A ^a   Dirksen, Robert T ^a   Yule, David I ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Inositol 1,4,5 trisphosphate receptor; Ryanodine receptor; Single channel measurement

Indexed keywords

CAFFEINE; CALCIUM ION; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; DANTROLENE; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; RYANODINE RECEPTOR 1; CALCIUM; CALCIUM CHANNEL STIMULATING AGENT; CESIUM; CESIUM CHLORIDE; CHLORIDE; POTASSIUM CHLORIDE; RYANODINE; RYANODINE RECEPTOR;

ARTICLE; CALCIUM TRANSPORT; CELL NUCLEUS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOPLASMIC RETICULUM; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; INTRACELLULAR MEMBRANE; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; CHEMISTRY; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; RABBIT; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ORYCTOLAGUS CUNICULUS;

ANIMALS; CAFFEINE; CALCIUM; CALCIUM CHANNEL AGONISTS; CELL NUCLEUS; CESIUM; CHLORIDES; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHLORIDE; RABBITS; RYANODINE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS;

EID: 84904563392     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.05.004     Document Type: Article

References (57)

1. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 2000, 1:11-21.
2. Serysheva I. Structure and Function of Calcium Release Channels 2010, Academic Press.
3. Capes E.M., Loaiza R., Valdivia H.H. Ryanodine receptors. Skeletal Muscle 2011, 1:18.
4. Lanner J.T., Georgiou D.K., Joshi A.D., Hamilton S.L. Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harbor Perspectives in Biology 2010, 2:a003996.
5. Fill M., Copello J.A. Ryanodine receptor calcium release channels. Physiol. Rev. 2002, 82:893-922.
6. Foskett J.K., White C., Cheung K.H., Mak D.O. Inositol trisphosphate receptor Ca2+ release channels. Physiol. Rev. 2007, 87:593-658.
7. Bosanac I., Alattia J.R., Mal T.K., Chan J., Talarico S., Tong F.K., Tong K.I., Yoshikawa F., Furuichi T., Iwai M., Michikawa T., Mikoshiba K., Ikura M. Structure of the inositol 1,4,5-trisphosphate receptor binding core in complex with its ligand. Nature 2002, 420:696-700.
8. Bosanac I., Michikawa T., Mikoshiba K., Ikura M. Structural insights into the regulatory mechanism of IP3 receptor. Biochim. Biophys. Acta 2004, 1742:89-102.
9. Lobo P.A., Van Petegem F. Crystal structures of the N-terminal domains of cardiac and skeletal muscle ryanodine receptors: insights into disease mutations. Structure 2009, 17:1505-1514.
10. Van Petegem F. Ryanodine receptors: structure and function. J. Biol. Chem. 2012, 287:31624-31632.
11. Seo M.D., Velamakanni S., Ishiyama N., Stathopulos P.B., Rossi A.M., Khan S.A., Dale P., Li C., Ames J.B., Ikura M., Taylor C.W. Structural and functional conservation of key domains in InsP3 and ryanodine receptors. Nature 2012, 483:108-112.
12. Bezprozvanny I. The inositol 1,4,5-trisphosphate receptors. Cell Calcium 2005, 38:261-272.
13. Yule D.I., Betzenhauser M.J., Joseph S.K. Linking structure to function: recent lessons from inositol 1,4,5-trisphosphate receptor mutagenesis. Cell Calcium 2010, 47:469-479.
14. Ivanova H., Vervliet T., Missiaen L., Parys J.B., De Smedt H., Bultynck G. Inositol 1,4,5-trisphosphate receptor-isoform diversity in cell death and survival. Biochim. Biophys. Acta 2014.
15. Clapham D.E. Calcium signaling. Cell 1995, 80:259-268.
16. Bootman M.D., Rietdorf K., Collins T., Walker S., Sanderson M. Ca2+-sensitive fluorescent dyes and intracellular Ca2+ imaging. Cold Spring Harbor Protocols 2013, 2013:83-99.
17. Bezprozvanny I. Bilayer measurement of endoplasmic reticulum Ca2+ channels. Cold Spring Harbor Protocols 2013, 2013.
18. Smith J.S., Coronado R., Meissner G. Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels. Nature 1985, 316:446-449.
19. Bezprozvanny I., Watras J., Ehrlich B.E. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 1991, 351:751-754.
20. Dellis O., Dedos S.G., Tovey S.C., Taufiq Ur R., Dubel S.J., Taylor C.W. Ca2+ entry through plasma membrane IP3 receptors. Science 2006, 313:229-233.
21. Wagner L.E., Joseph S.K., Yule D.I. Regulation of single inositol 1,4,5-trisphosphate receptor channel activity by protein kinase A phosphorylation. J. Physiol. 2008, 586:3577-3596.
22. Rosker C., Meur G., Taylor E.J., Taylor C.W. Functional ryanodine receptors in the plasma membrane of RINm5F pancreatic beta-cells. J. Biol. Chem. 2009, 284:5186-5194.
23. Stehno-Bittel L., Luckhoff A., Clapham D.E. Calcium release from the nucleus by InsP3 receptor channels. Neuron 1995, 14:163-167.
24. Mak D.O., Foskett J.K. Single-channel inositol 1,4,5-trisphosphate receptor currents revealed by patch clamp of isolated Xenopus oocyte nuclei. J. Biol. Chem. 1994, 269:29375-29378.
25. Mak D.O., McBride S., Foskett J.K. Inositol 1,4,5-trisphosphate [correction of tris-phosphate] activation of inositol trisphosphate [correction of tris-phosphate] receptor Ca2+ channel by ligand tuning of Ca2+ inhibition. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15821-15825.
26. Mak D.O., McBride S., Raghuram V., Yue Y., Joseph S.K., Foskett J.K. Single-channel properties in endoplasmic reticulum membrane of recombinant type 3 inositol trisphosphate receptor. J. Gen. Physiol. 2000, 115:241-256.
27. Wagner L.E., Yule D.I. Differential regulation of the InsP(3) receptor type-1 and -2 single channel properties by InsP(3), Ca(2)(+) and ATP. J. Physiol. 2012, 590:3245-3259.
28. Alzayady K.J., Wagner L.E., Chandrasekhar R., Monteagudo A., Godiska R., Tall G.G., Joseph S.K., Yule D.I. Functional inositol 1,4,5-trisphosphate receptors assembled from concatenated homo- and heteromeric subunits. J. Biol. Chem. 2013, 288:29772-29784.
29. Mak D.O., Vais H., Cheung K.H., Foskett J.K. Patch-clamp electrophysiology of intracellular Ca2+ channels. Cold Spring Harbor Protocols 2013, 2013:787-797.
30. Mak D.O., McBride S., Foskett J.K. ATP regulation of type 1 inositol 1,4,5-trisphosphate receptor channel gating by allosteric tuning of Ca(2+) activation. J. Biol. Chem. 1999, 274:22231-22237.
31. Mak D.O., McBride S., Foskett J.K. Regulation by Ca2+ and inositol 1,4,5-trisphosphate (InsP3) of single recombinant type 3 InsP3 receptor channels. Ca2+ activation uniquely distinguishes types 1 and 3 insp3 receptors. J. Gen. Physiol. 2001, 117:435-446.
32. Wagner L.E., Yule D.I. Differential regulation of the InsP3 receptor type-1 and -2 single channel properties by InsP3, Ca2+ and ATP. J. Physiol. 2012, 590:3245-3259.
33. Graves T.K., Hinkle P.M. Ca(2+)-induced Ca(2+) release in the pancreatic beta-cell: direct evidence of endoplasmic reticulum Ca(2+) release. Endocrinology 2003, 144:3565-3574.
34. Jacobson A.R., Moe S.T., Allen P.D., Fessenden J.D. Structural determinants of 4-chloro-m-cresol required for activation of ryanodine receptor type 1. Mol. Pharmacol. 2006, 70:259-266.
35. Fessenden J.D., Wang Y., Moore R.A., Chen S.R., Allen P.D., Pessah I.N. Divergent functional properties of ryanodine receptor types 1 and 3 expressed in a myogenic cell line. Biophys. J. 2000, 79:2509-2525.
36. Liu Q.Y., Lai F.A., Rousseau E., Jones R.V., Meissner G. Multiple conductance states of the purified calcium release channel complex from skeletal sarcoplasmic reticulum. Biophys. J. 1989, 55:415-424.
37. Smith J.S., Imagawa T., Ma J., Fill M., Campbell K.P., Coronado R. Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum. J. Gen. Physiol. 1988, 92:1-26.
38. Marx S.O., Ondrias K., Marks A.R. Coupled gating between individual skeletal muscle Ca2+ release channels (ryanodine receptors). Science 1998, 281:818-821.
39. Meissner G. Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 1994, 56:485-508.
40. Lindsay A.R., Manning S.D., Williams A.J. Monovalent cation conductance in the ryanodine receptor-channel of sheep cardiac muscle sarcoplasmic reticulum. J. Physiol. 1991, 439:463-480.
41. Chen D.P., Xu L., Tripathy A., Meissner G., Eisenberg B. Selectivity and permeation in calcium release channel of cardiac muscle: alkali metal ions. Biophys. J. 1999, 76:1346-1366.
42. Rousseau E., Meissner G. Single cardiac sarcoplasmic reticulum Ca2+-release channel: activation by caffeine. Am. J. Physiol. 1989, 256:H328-H333.
43. Sitsapesan R., Williams A.J. Mechanisms of caffeine activation of single calcium-release channels of sheep cardiac sarcoplasmic reticulum. J. Physiol. 1990, 423:425-439.
44. Rousseau E., Smith J.S., Meissner G. Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am. J. Physiol. 1987, 253:C364-C368.
45. Guse A.H. Linking NAADP to ion channel activity: a unifying hypothesis. Sci. Signal. 2012, 5. pe18.
46. Galione A., Evans A.M., Ma J., Parrington J., Arredouani A., Cheng X., Zhu M.X. The acid test: the discovery of two-pore channels (TPCs) as NAADP-gated endolysosomal Ca(2+) release channels. Pflugers Arch 2009, 458:869-876.
47. Galione A., Petersen O.H. The NAADP receptor: new receptors or new regulation?. Mol. Interventions 2005, 5:73-79.
48. Lee H.C. Cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate (NAADP) as messengers for calcium mobilization. J. Biol. Chem. 2012, 287:31633-31640.
49. Szentesi P., Collet C., Sarkozi S., Szegedi C., Jona I., Jacquemond V., Kovacs L., Csernoch L. Effects of dantrolene on steps of excitation-contraction coupling in mammalian skeletal muscle fibers. J. Gen. Physiol. 2001, 118:355-375.
50. Cherednichenko G., Ward C.W., Feng W., Cabrales E., Michaelson L., Samso M., Lopez J.R., Allen P.D., Pessah I.N. Enhanced excitation-coupled calcium entry in myotubes expressing malignant hyperthermia mutation R163C is attenuated by dantrolene. Mol. Pharmacol. 2008, 73:1203-1212.
51. Ashley R.H., Williams A.J. Divalent cation activation and inhibition of single calcium release channels from sheep cardiac sarcoplasmic reticulum. J. Gen. Physiol. 1990, 95:981-1005.
52. 2+. J. Gen. Physiol. 1986, 88:573-588.
53. Ionescu L., White C., Cheung K.H., Shuai J., Parker I., Pearson J.E., Foskett J.K., Mak D.O. Mode switching is the major mechanism of ligand regulation of InsP3 receptor calcium release channels. J. Gen. Physiol. 2007, 130:631-645.
54. Siekmann I., Wagner L.E., Yule D., Crampin E.J., Sneyd J. A kinetic model for type I and II IP3R accounting for mode changes. Biophys. J. 2012, 103:658-668.
55. Brillantes A.B., Ondrias K., Scott A., Kobrinsky E., Ondriasova E., Moschella M.C., Jayaraman T., Landers M., Ehrlich B.E., Marks A.R. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 1994, 77:513-523.
56. Wei L., Dirksen R.T. Ryanodinopathies: RyR-linked muscle diseases. Curr. Top. Membr. 2010, 66C:139-167.
57. Betzenhauser M.J., Marks A.R. Ryanodine receptor channelopathies. Pflugers Arch. 2010, 460:467-480.