Structural and functional characterization of ryanodine receptor-natrin toxin interaction

Biophysical Journal

Volumn 95, Issue 9, 2008, Pages 4289-4299

  Zhou, Qiang ^a   Wang, Qiong Ling ^b   Meng, Xing ^c   Shu, Yuyan ^d   Jiang, Tao ^e   Wagenknecht, Terence ^c,f   Yin, Chang Cheng ^b   Sui, Sen Fang ^a   Liu, Zheng ^c  

^a TSINGHUA UNIVERSITY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c WADSWORTH CENTER   (United States)

^d GUANGXI MEDICAL UNIVERSITY   (China)

^e INSTITUTE OF BIOPHYSICS   (China)

^f STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CYSTEINE; NATRIN PROTEIN, NAJA ATRA; RYANODINE; RYANODINE RECEPTOR; SNAKE VENOM; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; CRYOELECTRON MICROSCOPY; DRUG EFFECT; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CATALYTIC DOMAIN; COBRA VENOMS; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RYANODINE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SUBSTRATE SPECIFICITY;

EID: 58149149338     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.137224     Document Type: Article

References (52)

1. Kierszenbaum, A. L., O. Lea, P. Petrusz, F. S. French, and L. L. Tres. 1981. Isolation, culture, and immunocytochemical characterization of epididymal epithelial cells from pubertal and adult rats. Proc. Natl. Acad. Sci. USA. 78:1675-1679.
2. Ellerman, D. A., V. G. Da Ros, D. J. Cohen, D. Busso, M. M. Morgenfeld, and P. S. Cuasnicu. 2002. Expression and structure-function analysis of DE, a sperm cysteine-rich secretory protein that mediates gamete fusion. Biol. Reprod. 67:1225-1231.
3. Kasahara, M., J. Gutknecht, K. Brew, N. Spurr, and P. N. Goodfellow. 1989. Cloning and mapping of a testis-specific gene with sequence similarity to a sperm-coating glycoprotein gene. Genomics. 5:527-534.
4. Maeda, T., J. Nishida, and Y. Nakanishi. 1999. Expression pattern, subcellular localization and structure-function relationship of rat Tpx-1, a spermatogenic cell adhesion molecule responsible for association with Sertoli cells. Dev. Growth Differ. 41:715-722.
5. Kratzschmar, J., B. Haendler, U. Eberspaecher, D. Roosterman, P. Donner, and W. D. Schleuning. 1996. The human cysteine-rich secretory protein (CRISP) family. Primary structure and tissue distribution of CRISP-1, CRISP-2 and CRISP-3. Eur. J. Biochem. 236:827-836.
6. Yamazaki, Y., and T. Morita. 2004. Structure and function of snake venom cysteine-rich secretory proteins. Toxicon. 44:227-231.
7. Jalkanen, J., I. Huhtaniemi, and M. Poutanen. 2005. Mouse cysteine-rich secretory protein 4 (CRISP4): a member of the CRISP family exclusively expressed in the epididymis in an androgen-dependent manner. Biol. Reprod. 72:1268-1274.
8. Franzini-Armstrong, C., and F. Protasi. 1997. Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol. Rev. 77:699-729.
9. Morrissette, J., J. Kratzschmar, B. Haendler, R. el-Hayek, J. Mochca-Morales, B. M. Martin, J. R. Patel, R. L. Moss, W. D. Schleuning, R. Coronado, and L. D. Possani. 1995. Primary structure and properties of helothermine, a peptide toxin that blocks ryanodine receptors. Biophys. J. 68:2280-2288.
10. Nobile, M., V. Magnelli, L. Lagostena, J. Mochca-Morales, L. D. Possani, and G. Prestipino. 1994. The toxin helothermine affects potassium currents in newborn rat cerebellar granule cells. J. Membr. Biol. 139:49-55.
11. Nobile, M., F. Noceti, G. Prestipino, and L. D. Possani. 1996. Helothermine, a lizard venom toxin, inhibits calcium current in cerebellar granules. Exp. Brain Res. 110:15-20.
12. 2+ signaling. J. Biol. Chem. 281:4156-4163.
13. Yamazaki, Y., F. Hyodo, and T. Morita. 2003. Wide distribution of cysteine-rich secretory proteins in snake venoms: isolation and cloning of novel snake venom cysteine-rich secretory proteins. Arch. Biochem. Biophys. 412:133-141.
14. Chang, T.-Y., S.-H. Mao, and Y.-W. Guo. 1997. Cloning and expression of a cysteine-rich venom protein from Trimeresurus mucrosquamatus (Taiwan habu). Toxicon. 35:879-888.
15. Jin, Y., Q. Lu, X. Zhou, S. Zhu, R. Li, W. Wang, and Y. Xiong. 2003. Purification and cloning of cysteine-rich proteins from Trimeresurus jerdonii and Naja atra venoms. Toxicon. 42:539-547.
16. Yamazaki, Y., H. Koike, Y. Sugiyama, K. Motoyoshi, T. Wada, S. Hishinuma, M. Mita, and T. Morita. 2002. Cloning and characterization of novel snake venom proteins that block smooth muscle contraction. Eur. J. Biochem. 269:2708-2715.
17. Wang, J., B. Shen, M. Guo, X. Lou, Y. Duan, X. P. Cheng, M. Teng, L. Niu, Q. Liu, Q. Huang, and Q. Hao. 2005. Blocking effect and crystal structure of natrin toxin, a cysteine-rich secretory protein from Naja atra venom that targets the BKCa channel. Biochemistry. 44:10145-10152.
18. Wang, F., H. Li, M. Liu, H. Song, H. Han, Q. Wang, C. Yin, Y. Zhou, Z. Qi, Y. Shu, Z. Lin, and T. Jiang. 2006. Structural and functional analysis of natrin, a venom protein that targets various ion channels. Biochem. Biophys. Res. Commun. 351:443-448.
19. + channel inhibitor-like fold. J. Biol. Chem. 280:12405-12412.
20. 2+-channel blocker derived from snake venom. J. Mol. Biol. 350:735-743.
21. Saito, A., S. Seiler, A. Chu, and S. Fleischer. 1984. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. J. Cell Biol. 99:875-885.
22. Inui, M., A. Saito, and S. Fleischer. 1987. Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J. Biol. Chem. 262:1740-1747.
23. Yin, C. C., and F. A. Lai. 2000. Intrinsic lattice formation by the ryanodine receptor calcium-release channel. Nat. Cell Biol. 2:669-671.
24. 687 and FKBP12. Biophys. J. 77:189-203.
25. Liu, Z., J. Zhang, M. Sharma, P. Li, S. R. W. Chen, and T. Wagenknecht. 2001. Three-dimensional reconstruction of the recombinant type 3 ryanodine receptor and localization of its amino terminus. Proc. Natl. Acad. Sci. USA. 98:6104-6109.
26. Frank, J., M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith. 1996. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116:190-199.
27. Malhotra, A., P. Penczek, R. K. Agrawal, I. S. Gabashvilli, R. A. Grassucci, R. Jünemann, M. Burkhardt, K. H. Nierhaus, and J. Frank. 1998. Escherichia coli 70S ribosome at 15 Å resolution by cryoelectron microscopy: localization of fMet-tRNAfMet and fitting of L1 protein. J. Mol. Biol. 280:103-116.
28. Agrawal, R. K., P. Penczek, R. A. Grassucci, and J. Frank. 1998. Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc. Natl. Acad. Sci. USA. 95:6134-6138.
29. 3H]ryanodine binding assay. J. Biol. Chem. 273:33259-33266.
30. Chu, A., M. Diaz-Munoz, M. J. Hawkes, K. Brush, and S. L. Hamilton. 1990. Ryanodine as a probe for the functional state of the skeletal muscle sarcoplasmic reticulum calcium release channel. Mol. Pharmacol. 37:735-741.
31. Radermacher, M., V. Rao, R. Grassucci, J. Frank, A. P. Timerman, S. Fleischer, and T. Wagenknecht. 1994. Cryo-electron microscopy and three-dimensional reconstruction of the calciumrelease channel/ryanodine receptor from skeletal muscle. J. Cell Biol. 127:411-423.
32. Frank, J. 2006. Multivariate data analysis and classification of images. In Three-Dimensional Electron Microscopy of Macromolecular Assemblies. J. Frank, editor. Oxford University Press, New York. 145-192.
33. Samso, M., T. Wagenknecht, and P. D. Allen. 2005. Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat. Struct. Mol. Biol. 12:539-544.
34. Liu, Z., R. Wang, J. Zhang, S. R. W. Chen, and T. Wagenknecht. 2005. Localization of a disease-associated mutation site on the three-dimensional structure of cardiac ryanodine receptor. J. Biol. Chem. 280:37941-37947.
35. 2-terminal disease-causing mutation hotspot to the "clamp" region in the three-dimensional structure of the cardiac ryanodine receptor. J. Biol. Chem. 282:17785-17793.
36. McCarty, T. V., K. A. Quane, and P. J. Lynch. 2000. Ryanodine receptor mutations in malignant hyperthermia and central core disease. Hum. Mutat. 15:410-417.
37. Ikemoto, N., and T. Yamamoto. 2002. Regulation of calcium release by interdomain interaction within ryanodine receptors. Front. Biosci. 7:d671-d683.
38. 2+ channel regulation. J. Biol. Chem. 275:11618-11625.
39. Yamamoto, T., and N. Ikemoto. 2002. T-tubule depolarization-induced local events in the ryanodine receptor, as monitored with the fluorescent conformational probe incorporated by mediation of peptide A. J. Biol. Chem. 277:984-992.
40. 2+ release in skinned skeletal muscle fibers. Am. J. Physiol. Cell Physiol. 281:C207-C214.
41. 2+ spark frequency in skeletal muscle. J. Gen. Physiol. 119:15-32.
42. 2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 265:2244-2256.
43. 2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J. Biol. Chem. 265:13472-13483.
44. Sharma, M., P. Penczek, R. Grassucci, H. B. Xin, S. Fleischer, and T. Wagenknecht. 1998. Cryoelectron microscopy and image analysis of the cardiac ryanodine receptor. J. Biol. Chem. 273:18429-18434.
45. Ward, A., M. O. Chaffman, and E. M. Sorkin. 1986. Dantrolene: a review of its pharmacodynamic and pharmacokinetic properties and therapeutic use in malignant hyperthermia, the neurolept malignant syndrome, and an update of its use in muscle spasticity. Drugs. 32:130-168.
46. Oda, T., M. Yano, T. Yamamoto, T. Tokuhisa, S. Okuda, M. Doi, T. Ohkusa, Y. Ikeda, S. Kobayashi, N. Ikemoto, and M. Matsuzaki. 2005. Defective regulation of interdomain interactions within the ryanodine receptor plays a key role in the pathogenesis of heart failure. Circulation. 111:3400-3410.
47. Kobayashi, S., M. L. Bannister, J. P. Gangopadhyay, T. Hamada, J. Parness, and N. Ikemoto. 2005. Dantrolene stabilizes domain interactions within the ryanodine receptor. J. Biol. Chem. 280:6580-6587.
48. Bellinger, A. M., S. Reiken, M. Dura, P. W. Murphy, S. X. Deng, D. W. Landry, D. Nieman, S. E. Lehnart, M. Samaru, A. LaCampagne, and A. R. Marks. 2008. Remodeling of ryanodine receptor complex causes "leaky" channels: a molecular mechanism for decreased exercise capacity. Proc. Natl. Acad. Sci. USA. 105:2198-2202.
49. Tudor, J. E., P. K. Pallaghy, M. W. Pennington, and R. S. Norton. 1996. Solution structure of ShK toxin, a novel potassium channel inhibitor from a sea anemone. Nat. Struct. Biol. 3:317-320.
50. Dauplais, M., A. Lecoq, J. Song, J. Cotton, N. Jamin, B. Gilquin, C. Roumestand, C. Vita, C. L. C. de Medeiros, E. G. Rowan, A. L. Harvey, and A. Menez. 1997. On the convergent evolution of animal toxins. Conservation of a diad of functional residues in potassium channel-blocking toxins with unrelated structures. J. Biol. Chem. 272:4302-4309.
51. Brown, R. L., T. L. Haley, K. A. West, and J. W. Crabb. 1999. Pseudechetoxin: a peptide blocker of cyclic nucleotide-gated ion channels. Proc. Natl. Acad. Sci. USA. 96:754-759.
52. Yamazaki, Y., R. L. Brown, and T. Morita. 2002. Purification and cloning of toxins from elapid venoms that target cyclic nucleotide-gated ion channels. Biochemistry. 41:11331-11337.