Effects of inserting fluorescent proteins into the α1S II-III loop: Insights into excitation-contraction coupling

Journal of General Physiology

Volumn 134, Issue 1, 2009, Pages 35-51

  Bannister, Roger A ^a   Papadopoulos, Symeon ^b,c   Haarmann, Claudia S ^b,d   Beam, Kurt G ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d NANION TECHNOLOGIES GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIHYDROPYRIDINE RECEPTOR; CYAN FLUORESCENT PROTEIN; RYANODINE RECEPTOR 1; YELLOW FLUORESCENT PROTEIN;

ARTICLE; GENE INSERTION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CELLS, CULTURED; LUMINESCENT PROTEINS; MICE; MUSCLE CONTRACTION; MYOFIBRILS; NEUROMUSCULAR JUNCTION; PROTEIN STRUCTURE, TERTIARY; SYNAPTIC TRANSMISSION;

EID: 67649951484     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200910241     Document Type: Article

References (68)

1. Adams, B.A., T. Tanabe, A. Mikami, S. Numa, and K.G. Beam. 1990. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs. Nature. 346:569-572. (Pubitemid 20238809)
2. Ahern, C.A., J. Arikkath, P. Vallejo, C.A. Gurnett, P.A. Powers, K.P. Campbell, and R. Coronado. 2001a. Intramembrane charge movements and excitation-contraction coupling expressed by two-domain fragments of the Ca2+ channel. Proc. Natl. Acad. Sci. USA. 98:6935-6940. (Pubitemid 32538320)
3. Ahern, C.A., D. Bhattacharya, L. Mortenson, and R. Coronado. 2001b. A component of excitation-contraction coupling triggered in the absence of the T671-L690 and L720-Q765 regions of the II-III loop of the dihydropyridine receptor α1S pore subunit. Biophys. J. 81:3294-3307. (Pubitemid 33111477)
4. 2+ current and charge movements in skeletal myotubes promoted by the β-subunit of the dihydropyridine receptor in the absence of ryanodine receptor type 1. Biophys. J. 84:942-959.
5. 2+ channel. J. Gen. Physiol. 115:467-480.
6. 2+ channel expression. J. Biol. Chem. 276:17732-17738.
7. Bannister, R.A. 2007. Bridging the myoplasmic gap: recent developments in skeletal muscle excitation-contraction coupling. J. Muscle Res. Cell Motil. 28:275-283. (Pubitemid 350043630)
8. 1S N-terminus is not essential for bi-directional coupling with RyR1. Biochem. Biophys. Res. Commun. 336:134-141.
9. Bannister, R.A., H.M. Colecraft, and K.G. Beam. 2008a. Rem inhibits skeletal muscle EC coupling by reducing the number of functional L-type Ca2+ channels. Biophys. J. 94:2631-2638.
10. Bannister, R.A., M. Grabner, and K.G. Beam. 2008b. The α1S III-IV loop influences 1,4-dihydropyridine receptor gating but is not directly involved in excitation-contraction coupling interactions with the type 1 ryanodine receptor. J. Biol. Chem. 283:23217-23223.
11. Beam, K.G., and C. Franzini-Armstrong. 1997. Functional and structural approaches to the study of excitation-contraction coupling. Methods Cell Biol. 52:283-306. (Pubitemid 128787399)
12. Beam, K.G., and P. Horowicz. 2004. Excitation-contraction coupling in skeletal muscle. In Myology: Basic and Clinical. A.G. Engel and C. Franzini-Armstrong, editors. Third edition. McGraw Hill, New York. 257-280.
13. 1a subunit in excitation-contraction coupling of skeletal muscle. Biophys. J. 77:2953-2967.
14. Block, B.A., T. Imagawa, K.P. Campbell, and C. Franzini-Armstrong. 1988. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J. Cell Biol. 107:2587-2600. (Pubitemid 19019400)
15. Buck, E., I. Zimanyi, J.J. Abramson, and I.N. Pessah. 1992. Ryanodine stabilizes multiple conformational states of the skeletal muscle calcium release channel. J. Biol. Chem. 267:23560-23567. (Pubitemid 23088155)
16. Carbonneau, L., D. Bhattacharya, D.C. Sheridan, and R. Coronado. 2005. Multiple loops of the dihydropyridine receptor pore subunit are required for full-scale excitation-contraction coupling in skeletal muscle. Biophys. J. 89:243-255. (Pubitemid 41098279)
17. 2+ channel β-subunit and ryanodine receptor type 1 strengthens excitation-contraction coupling. Proc. Natl. Acad. Sci. USA. 102:19225-19230.
18. 1S loop region critical for skeletal muscle contraction is intrinsically unstructured and binds to a SPRY domain of the type 1 ryanodine receptor. Int. J. Biochem. Cell Biol. 41:677-686.
19. El-Hayek, R., and N. Ikemoto. 1998. Identification of the minimum essential region in the II-III loop of the dihydropyridine receptor α1 subunit required for activation of skeletal muscle-type excitation-contraction coupling. Biochemistry. 37:7015-7020. (Pubitemid 28228139)
20. Flucher, B.E., N. Kasielke, and M. Grabner. 2000. The triad targeting signal of the skeletal muscle calcium channel is localized in the COOH terminus of the α1S subunit. J. Cell Biol. 151:467-478. (Pubitemid 30787240)
21. 2+ channel fragments in triad targeting and restoration of excitation-contraction coupling in skeletal muscle. Proc. Natl. Acad. Sci. USA. 99:10167-10172.
22. 2+ currents and alters channel inactivation properties. J. Biol. Chem. 275:14476-14481.
23. 2δ dihydropyridine receptor subunit is a critical element for excitation-coupled calcium entry but not for formation of tetrads in skeletal myotubes. Biophys. J. 94:3023-3034.
24. García, J., and K.G. Beam. 1994. Measurement of calcium transients and slow calcium current in myotubes. J. Gen. Physiol. 103:107-123. (Pubitemid 24051935)
25. García, J., T. Tanabe, and K.G. Beam. 1994. Relationship of calcium transients to calcium currents and charge movements in myotubes expressing skeletal and cardiac dihydropyridine receptors. J. Gen. Physiol. 103:125-147. (Pubitemid 24051936)
26. 1a subunit in adult mouse skeletal muscle. Biophys. J. 89:3976-3984.
27. 1 subunit is involved in extracellular signalling. J. Physiol. 586:727-738.
28. 2+ channels expressed in dysgenic myotubes. Proc. Natl. Acad. Sci. USA. 95:1903-1908.
29. Grabner, M., R.T. Dirksen, N. Suda, and K.G. Beam. 1999. The II-III loop of the skeletal muscle dihydropyridine receptor is responsible for the bi-directional coupling with the ryanodine receptor. J. Biol. Chem. 274:21913-21919. (Pubitemid 129519744)
30. Kugler, G., M. Grabner, J. Platzer, J. Striessnig, and B.E. Flucher. 2004a. The monoclonal antibody mAB 1A binds to the excitation - contraction coupling domain in the II-III loop of the skeletal muscle calcium channel α1S subunit. Arch. Biochem. Biophys. 427:91-100. (Pubitemid 38725917)
31. 1S II-III loop for skeletal-type excitation-contraction coupling. J. Biol. Chem. 279:4721-4728.
32. Leong, P., and D.H. MacLennan. 1998a. A 37-amino acid sequence in the skeletal muscle ryanodine receptor interacts with the cytoplasmic loop between domains II and III in the skeletal muscle dihydropyridine receptor. J. Biol. Chem. 273:7791-7794. (Pubitemid 28168820)
33. Leong, P., and D.H. MacLennan. 1998b. The cytoplasmic loops between domains II and III and domains III and IV in the skeletal muscle dihydropyridine receptor bind to a contiguous site in the skeletal muscle ryanodine receptor. J. Biol. Chem. 273:29958-29964. (Pubitemid 28510013)
34. Lorenzon, N.M., and K.G. Beam. 2007. Accessibility of targeted DHPR sites to streptavidin and functional effects of binding on EC coupling. J. Gen. Physiol. 130:379-388. (Pubitemid 47481601)
35. Lorenzon, N.M., C.S. Haarmann, E.E. Norris, S. Papadopoulos, and K.G. Beam. 2004. Metabolic biotinylation as a probe of supramolecular structure of the triad junction in skeletal muscle. J. Biol. Chem. 279:44057-44064. (Pubitemid 39390715)
36. Nakai, J., R.T. Dirksen, H.T. Nguyen, I.N. Pessah, K.G. Beam, and P.D. Allen. 1996. Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature. 380:72-75. (Pubitemid 26076239)
37. 2+ channels. J. Biol. Chem. 273:13403-13406.
38. Nakai, J., T. Tanabe, T. Konno, B.A. Adams, and K.G. Beam. 1998b. Localization in the II-III loop of the dihydropyridine receptor of a sequence critical for excitation-contraction coupling. J. Biol. Chem. 273:24983-24986. (Pubitemid 28443252)
39. 1S or excitation-contraction coupling. J. Biol. Chem. 280:2229-2237.
40. 2+ channel subunits: lessons learned from muscle. Curr. Opin. Pharmacol. 8:311-318.
41. Paolini, C., J.D. Fessenden, I.N. Pessah, and C. Franzini-Armstrong. 2004. Evidence for conformational coupling between two calcium channels. Proc. Natl. Acad. Sci. USA. 101:12748-12752. (Pubitemid 39122094)
42. Papadopoulos, S., V. Leuranguer, R.A. Bannister, and K.G. Beam. 2004. Mapping sites of potential proximity between the dihydropyridine receptor and RyR1 in muscle using a cyan fluorescent protein-yellow fluorescent protein tandem as a fluorescence resonance energy transfer probe. J. Biol. Chem. 279:44046-44056. (Pubitemid 39390714)
43. Proenza, C., C. Wilkens, N.M. Lorenzon, and K.G. Beam. 2000a. A carboxyl-terminal region important for the expression and targeting of the skeletal muscle dihydropyridine receptor. J. Biol. Chem. 275:23169-23174. (Pubitemid 30646211)
44. Proenza, C., C.M. Wilkens, and K.G. Beam. 2000b. Excitation-contraction coupling is not affected by scrambled sequence in residues 681-690 of the dihydropyridine receptor II-III loop. J. Biol. Chem. 275:29935-29937. (Pubitemid 30751295)
45. 1S (CaV1.1) II-III loop. J. Biol. Chem. 277:6530-6535.
46. Protasi, F., C. Franzini-Armstrong, and P.D. Allen. 1998. Role of ryanodine receptors in the assembly of calcium release units in skeletal muscle. J. Cell Biol. 140:831-842. (Pubitemid 28141221)
47. Protasi, F., H. Takekura, Y. Wang, S.R.W. Chen, G. Meissner, P.D. Allen, and C. Franzini-Armstrong. 2000. RYR1 and RYR3 have different roles in the assembly of calcium release units of skeletal muscle. Biophys. J. 79:2494-2508. (Pubitemid 30847850)
48. 1S-dihydropyridine receptors in skeletal muscle. Biophys. J. 83:3230-3244.
49. 1a subunit is essential for the assembly of dihydropyridine-receptor arrays in skeletal muscle. Proc. Natl. Acad. Sci. USA. 102:17219-17224.
50. 1-null zebrafish relaxed is an exclusive function of the β1a subunit. J. Biol. Chem. 284:1242-1251.
51. Sencer, S., R.V. Papineni, D.B. Halling, P. Pate, J. Krol, J.Z. Zhang, and S.L. Hamilton. 2001. Coupling of RYR1 and L-type calcium channels via calmodulin binding domains. J. Biol. Chem. 276:38237-38241. (Pubitemid 37384081)
52. 2asubunit in skeletal myotubes. Biophys. J. 85:3739-3757.
53. 2+ dependent excitation-contraction coupling in skeletal myotubes. Biophys. J. 84:220-237.
54. Sheridan, D.C., W. Cheng, L. Carbonneau, C.A. Ahern, and R. Coronado. 2004. Involvement of a heptad repeat in the carboxyl terminus of the dihydropyridine receptor β1a subunit in the mechanism of excitation-contraction coupling in skeletal muscle. Biophys. J. 87:929-942. (Pubitemid 39095074)
55. Sheridan, D.C., H. Takekura, C. Franzini-Armstrong, K.G. Beam, P.D. Allen, and C.F. Perez. 2006. Bidirectional signaling between calcium channels of skeletal muscle requires multiple direct and indirect interactions. Proc. Natl. Acad. Sci. USA. 103:19760-19765. (Pubitemid 46037504)
56. 2+-release channels. Am. J. Physiol. 272:C1475-C1481.
57. Tae, H.S., N.C. Norris, Y. Cui, Y. Karunasekara, P.G. Board, A.F. Dulhunty, and M.G. Casarotto. 2009. Molecular recognition of the disordered dihydropyridine receptor II-III loop by a conserved spry domain of the type 1 ryanodine receptor. Clin. Exp. Pharmacol. Physiol. 36:346-349.
58. Takekura, H., L. Bennett, T. Tanabe, K.G. Beam, and C. Franzini-Armstrong. 1994. Restoration of junctional tetrads in dysgenic myotubes by dihydropyridine receptor cDNA. Biophys. J. 67:793-803. (Pubitemid 24235408)
59. Takekura, H., C. Paolini, C. Franzini-Armstrong, G. Kugler, M. Grabner, and B.E. Flucher. 2004. Differential contribution of skeletal and cardiac II-III loop sequences to the assembly of dihydropyridine-receptor arrays in skeletal muscle. Mol. Biol. Cell. 15:5408-5419. (Pubitemid 39564734)
60. Tanabe, T., H. Takeshima, A. Mikami, V. Flockerzi, H. Takahashi, K. Kangawa, M. Kojima, H. Matsuo, T. Hirose, and S. Numa. 1987. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 328:313-318. (Pubitemid 17097652)
61. Tanabe, T., K.G. Beam, J.A. Powell, and S. Numa. 1988. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature. 336:134-139. (Pubitemid 18266138)
62. Tanabe, T., K.G. Beam, B.A. Adams, T. Niidome, and S. Numa. 1990. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature. 346:567-569. (Pubitemid 20238808)
63. 2+ channel splice variant with high conductance and voltage-sensitivity alters EC coupling in developing skeletal muscle. Biophys. J. 96:35-44.
64. Ursu, D., S. Sebille, B. Dietze, D. Freise, V. Flockerzi, and W. Melzer. 2001. Excitation-contraction coupling in skeletal muscle of a mouse lacking the dihydropyridine receptor subunit γ1. J. Physiol. 533:367-377. (Pubitemid 32519994)
65. Weiss, R.G., K.M.S. O'Connell, B.E. Flucher, P.D. Allen, M. Grabner, and R.T. Dirksen. 2004. Functional analysis of the R1086H malignant hyperthermia mutation in the DHPR reveals an unexpected influence of the III-IV loop on skeletal muscle EC coupling. Am. J. Physiol. Cell Physiol. 287:C1094-C1102. (Pubitemid 39238334)
66. 1S II-III loop and C terminal sequences into α1H fails to restore excitation-contraction coupling in dysgenic myotubes. J. Muscle Res. Cell Motil. 24:99-109.
67. Wilkens, C.M., N. Kasielke, B.E. Flucher, K.G. Beam, and M. Grabner. 2001. Excitation-contraction coupling is unaffected by drastic alteration of the sequence surrounding residues L720-L764 of the α1S II-III loop. Proc. Natl. Acad. Sci. USA. 98:5892-5897. (Pubitemid 32435738)
68. 2+ release channel from skeletal muscle sarcoplasmic reticulum. Mol. Pharmacol. 42:1049-1057.