Recombinant MG53 protein modulates therapeutic cell membrane repair in treatment of muscular dystrophy

Science Translational Medicine

Volumn 4, Issue 139, 2012, Pages

  Weisleder, Noah ^a,b   Takizawa, Norio ^b   Lin, Peihui ^a   Wang, Xianhua ^c   Cao, Chunmei ^c   Zhang, Yan ^c   Tan, Tao ^b   Ferrante, Christopher ^b   Zhu, Hua ^a   Chen, Pin Jung ^b   Yan, Rosalie ^b   Sterling, Matthew ^a   Zhao, Xiaoli ^a   Hwang, Moonsun ^a   Takeshima, Miyuki ^d   Cai, Chuanxi ^a   Cheng, Heping ^c   Takeshima, Hiroshi ^d   Xiao, Rui Ping ^c   Ma, Jianjie ^a,b  

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

^b TRIM edicine Inc   (United States)

^c PEKING UNIVERSITY   (China)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; LACTATE DEHYDROGENASE; MITSUGUMIN 53; PHOSPHATIDYLSERINE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; MITSUGUMIN 53, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE MARKER; DRUG EFFECT; DRUG MECHANISM; DRUG PROTEIN BINDING; DUCHENNE MUSCULAR DYSTROPHY; ENZYME ASSAY; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MEMBRANE DAMAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN TARGETING; REGENERATIVE MEDICINE; SIGNAL TRANSDUCTION; TISSUE REPAIR; TRANSLATION INITIATION; ANIMAL; CELL LINE; CELL MEMBRANE; CHO CELL; HAMSTER; METABOLISM; MUSCULAR DYSTROPHY; SKELETAL MUSCLE; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CHO CELLS; CRICETINAE; HUMANS; MALE; MICE; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES;

EID: 84862907349     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3003921     Document Type: Article

References (56)

1. P. L. McNeil, R. A. Steinhardt, Plasma membrane disruption: Repair, prevention, adaptation. Annu. Rev. Cell Dev. Biol. 19, 697-731 (2003).
2. P. L. McNeil, T. Kirchhausen, An emergency response team for membrane repair. Nat. Rev. Mol. Cell Biol. 6, 499-505 (2005).
3. R. A. Steinhardt, G. Bi, J. M. Alderton, Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science 263, 390-393 (1994).
4. P. L. McNeil, S. Ito, Gastrointestinal cell plasma membrane wounding and resealing in vivo. Gastroenterology 96, 1238-1248 (1989).
5. P. L. McNeil, R. Khakee, Disruptions of muscle fiber plasma membranes. Role in exercise-induced damage. Am. J. Pathol. 140, 1097-1109 (1992).
6. M. S. Clarke, R. W. Caldwell, H. Chiao, K. Miyake, P. L. McNeil, Contraction-induced cell wounding and release of fibroblast growth factor in heart. Circ. Res. 76, 927-934 (1995).
7. K. Miyake, P. L. McNeil, Vesicle accumulation and exocytosis at sites of plasma membrane disruption. J. Cell Biol. 131, 1737-1745 (1995).
8. T. Togo, T. B. Krasieva, R. A. Steinhardt, A decrease in membrane tension precedes successful cell-membrane repair. Mol. Biol. Cell 11, 4339-4346 (2000).
9. D. Bansal, K. Miyake, S. S. Vogel, S. Groh, C. C. Chen, R. Williamson, P. L. McNeil, K. P. Campbell, Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423, 168-172 (2003).
10. A. J. van der Kooi, W. S. Frankhuizen, P. G. Barth, C. J. Howeler, G. W. Padberg, F. Spaans, A. R. Wintzen, J. H. Wokke, G. J. van Ommen, M. de Visser, E. Bakker, H. B. Ginjaar, Limbgirdle muscular dystrophy in the Netherlands: Gene defect identified in half the families. Neurology 68, 2125-2128 (2007).
11. J. K. Jaiswal, G. Marlow, G. Summerill, I. Mahjneh, S. Mueller, M. Hill, K. Miyake, H. Haase, L. V. Anderson, I. Richard, S. Kiuru-Enari, P. L. McNeil, S. M. Simon, R. Bashir, Patients with a non-dysferlin Miyoshi myopathy have a novel membrane repair defect. Traffic 8, 77-88 (2007).
12. S. T. Cooper, E. Kizana, J. D. Yates, H. P. Lo, N. Yang, Z. H. Wu, I. E. Alexander, K. N. North, Dystrophinopathy carrier determination and detection of protein deficiencies in muscular dystrophy using lentiviral MyoD-forced myogenesis. Neuromuscul. Disord. 17, 276-284 (2007).
13. K.Wenzel, C. Geier, F. Qadri, N. Hubner, H. Schulz, B. Erdmann, V. Gross, D. Bauer, R. Dechend, R. Dietz, K. J. Osterziel, S. Spuler, C. Ozcelik, Dysfunction of dysferlin-deficient hearts. J. Mol. Med. 85, 1203-1214 (2007).
14. T. H. Chase, G. A. Cox, L. Burzenski, O. Foreman, L. D. Shultz, Dysferlin deficiency and the development of cardiomyopathy in a mouse model of limb-girdle muscular dystrophy 2B. Am. J. Pathol. 175, 2299-2308 (2009).
15. N. G. Bazan, V. L. Marcheselli, K. Cole-Edwards, Brain response to injury and neurodegeneration: Endogenous neuroprotective signaling. Ann. N. Y. Acad. Sci. 1053, 137-147 (2005).
16. O. Gajic, J. Lee, C. H. Doerr, J. C. Berrios, J. L. Myers, R. D. Hubmayr, Ventilator-induced cell wounding and repair in the intact lung. Am. J. Respir. Crit. Care Med. 167, 1057-1063 (2003).
17. K. R. Doherty, E. M. McNally, Repairing the tears: Dysferlin in muscle membrane repair. Trends Mol. Med. 9, 327-330 (2003).
18. X. Wang, W. Xie, Y. Zhang, P. Lin, L. Han, P. Han, Y.Wang, Z. Chen, G. Ji, M. Zheng, N. Weisleder, R. P. Xiao, H. Takeshima, J. Ma, H. Cheng, Cardioprotection of ischemia/reperfusion injury by cholesterol-dependent MG53-mediated membrane repair. Circ. Res. 107, 76-83 (2010).
19. C. Cai, H. Masumiya, N. Weisleder, N. Matsuda, M.Nishi, M.Hwang, J. K. Ko, P. Lin, A. Thornton, X. Zhao, Z. Pan, S. Komazaki, M. Brotto, H. Takeshima, J. Ma, MG53 nucleates assembly of cell membrane repair machinery. Nat. Cell Biol. 11, 56-64 (2009).
20. C. Cai, N. Weisleder, J. K. Ko, S. Komazaki, Y. Sunada, M. Nishi, H. Takeshima, J. Ma, Membrane repair defects in muscular dystrophy are linked to altered interaction between MG53, caveolin-3, and dysferlin. J. Biol. Chem. 284, 15894-15902 (2009).
21. C. M. Cao, Y. Zhang, N. Weisleder, C. Ferrante, X. Wang, F. Lv, Y. Zhang, R. Song, M. Hwang, L. Jin, J. Guo, W. Peng, G. Li, M. Nishi, H. Takeshima, J. Ma, R. P. Xiao, MG53 constitutes a primary determinant of cardiac ischemic preconditioning. Circulation 121, 2565-2574 (2010).
22. H. Moser, Duchenne muscular dystrophy: Pathogenetic aspects and genetic prevention. Hum. Genet. 66, 17-40 (1984).
23. P. N. Ray, B. Belfall, C. Duff, C. Logan, V. Kean, M. W. Thompson, J. E. Sylvester, J. L. Gorski, R. D. Schmickel, R. G. Worton, Cloning of the breakpoint of an X;21 translocation associated with Duchenne muscular dystrophy. Nature 318, 672-675 (1985).
24. K. P. Campbell, Three muscular dystrophies: Loss of cytoskeleton- extracellular matrix linkage. Cell 80, 675-679 (1995).
25. T. A. Partridge, Impending therapies for Duchenne muscular dystrophy. Curr. Opin. Neurol. 24, 415-422 (2011).
26. J. Watchko, T. O'Day, B. Wang, L. Zhou, Y. Tang, J. Li, X. Xiao, Adeno-associated virus vector-mediated minidystrophin gene therapy improves dystrophic muscle contractile function in mdx mice. Hum. Gene Ther. 13, 1451-1460 (2002).
27. I. Yanagihara, K. Inui, G. Dickson, G. Turner, T. Piper, Y. Kaneda, S. Okada, Expression of full-length human dystrophin cDNA in mdx mouse muscle by HVJ-liposome injection. Gene Ther. 3, 549-553 (1996).
28. P. R. Clemens, S. Kochanek, Y. Sunada, S. Chan, H. H. Chen, K. P. Campbell, C. T. Caskey, In vivo muscle gene transfer of full-length dystrophin with an adenoviral vector that lacks all viral genes. Gene Ther. 3, 965-972 (1996).
29. E. Gussoni, G. K. Pavlath, A. M. Lanctot, K. R. Sharma, R. G. Miller, L. Steinman, H. M. Blau, Normal dystrophin transcripts detected in Duchenne muscular dystrophy patients after myoblast transplantation. Nature 356, 435-438 (1992).
30. E. Gussoni, Y. Soneoka, C. D. Strickland, E. A. Buzney, M. K. Khan, A. F. Flint, L. M. Kunkel, R. C. Mulligan, Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390-394 (1999).
31. M. Sampaolesi, S. Blot, G. D'Antona, N. Granger, R. Tonlorenzi, A. Innocenzi, P. Mognol, J. L. Thibaud, B. G. Galvez, I. Barthélémy, L. Perani, S. Mantero, M. Guttinger, O. Pansarasa, C. Rinaldi, M. G. Cusella De Angelis, Y. Torrente, C. Bordignon, R. Bottinelli, G. Cossu, Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444, 574-579 (2006).
32. I. Nonaka, Animal models of muscular dystrophies. Lab. Anim. Sci. 48, 8-17 (1998).
33. H. Zhu, P. Lin, G. De, K. H. Choi, H. Takeshima, N. Weisleder, J. Ma, Polymerase transcriptase release factor (PTRF) anchors MG53 protein to cell injury site for initiation of membrane repair. J. Biol. Chem. 286, 12820-12824 (2011).
34. P. Lin, H. Zhu, C. Cai, X. Wang, C. Cao, R. Xiao, Z. Pan, N. Weisleder, H. Takeshima, J. Ma, Nonmuscle myosin IIA facilitates vesicle trafficking for MG53-mediated cell membrane repair. FASEB J. 26, 1875-1883 (2012).
35. R. Ng, J. M. Metzger, D. R. Claflin, J. A. Faulkner, Poloxamer 188 reduces the contraction-induced force decline in lumbrical muscles from mdx mice. Am. J. Physiol. Cell Physiol. 295, C146-C150 (2008).
36. B. Greenebaum, K. Blossfield, J. Hannig, C. S. Carrillo, M. A. Beckett, R. R. Weichselbaum, R. C. Lee, Poloxamer 188 prevents acute necrosis of adult skeletal muscle cells following high-dose irradiation. Burns 30, 539-547 (2004).
37. R. C. Lee, L. P. River, F. S. Pan, L. Ji, R. L. Wollmann, Surfactant-induced sealing of electropermeabilized skeletal muscle membranes in vivo. Proc. Natl. Acad. Sci. U.S.A. 89, 4524-4528 (1992).
38. D. Townsend, I. Turner, S. Yasuda, J. Martindale, J. Davis, M. Shillingford, J. N. Kornegay, J. M. Metzger, Chronic administration of membrane sealant prevents severe cardiac injury and ventricular dilatation in dystrophic dogs. J. Clin. Invest. 120, 1140-1150 (2010).
39. S. Yasuda, D. Townsend, D. E. Michele, E. G. Favre, S. M. Day, J. M. Metzger, Dystrophic heart failure blocked by membrane sealant poloxamer. Nature 436, 1025-1029 (2005).
40. F. Follis, B. Jenson, K. Blisard, E. Hall, R. Wong, R. Kessler, T. Temes, J. Wernly, Role of poloxamer 188 during recovery from ischemic spinal cord injury: A preliminary study. J. Invest. Surg. 9, 149-156 (1996).
41. D. M. Frim, D. A. Wright, D. J. Curry, W. Cromie, R. Lee, U. J. Kang, The surfactant poloxamer-188 protects against glutamate toxicity in the rat brain. Neuroreport 15, 171-174 (2004).
42. D. Kilinc, G. Gallo, K. Barbee, Poloxamer 188 reduces axonal beading following mechanical trauma to cultured neurons. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2007, 5395-5398 (2007).
43. T. Gulik-Krzywicki, M. Balerna, J. P. Vincent, M. Lazdunski, Freeze-fracture study of cardiotoxin action on axonal membrane and axonal membrane lipid vesicles. Biochim. Biophys. Acta 643, 101-114 (1981).
44. E. A. Rivas, M. Le Maire, T. Gulik-Krzywicki, Isolation of rhodopsin by the combined action of cardiotoxin and phospholipase A2 on rod outer segment membranes. Biochim. Biophys. Acta 644, 127-133 (1981).
45. V. Dressler, K. Schwister, C. W. Haest, B. Deuticke, Dielectric breakdown of the erythrocyte membrane enhances transbilayer mobility of phospholipids. Biochim. Biophys. Acta 732, 304-307 (1983).
46. T. Fujiwara, K. Ritchie, H. Murakoshi, K. Jacobson, A. Kusumi, Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157, 1071-1081 (2002).
47. A. Sonnleitner, G. J. Schütz, T. Schmidt, Free Brownian motion of individual lipid molecules in biomembranes. Biophys. J. 77, 2638-2642 (1999).
48. D. Bansal, K. P. Campbell, Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol. 14, 206-213 (2004).
49. P. Y. Fong, P. R. Turner, W. F. Denetclaw, R. A. Steinhardt, Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250, 673-676 (1990).
50. N. Deconinck, B. Dan, Pathophysiology of duchenne muscular dystrophy: Current hypotheses. Pediatr. Neurol. 36, 1-7 (2007).
51. C. Pasternak, S. Wong, E. L. Elson, Mechanical function of dystrophin in muscle cells. J. Cell Biol. 128, 355-361 (1995).
52. T. Yokota, Q. L. Lu, T. Partridge, M. Kobayashi, A. Nakamura, S. Takeda, E. Hoffman, Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann. Neurol. 65, 667-676 (2009).
53. E. M. Welch, E. R. Barton, J. Zhuo, Y. Tomizawa, W. J. Friesen, P. Trifillis, S. Paushkin, M. Patel, C. R. Trotta, S. Hwang, R. G. Wilde, G. Karp, J. Takasugi, G. Chen, S. Jones, H. Ren, Y. C. Moon, D. Corson, A. A. Turpoff, J. A. Campbell, M. M. Conn, A. Khan, N. G. Almstead, J. Hedrick, A. Mollin, N. Risher, M. Weetall, S. Yeh, A. A. Branstrom, J. M. Colacino, J. Babiak, W. D. Ju, S. Hirawat, V. J. Northcutt, L. L. Miller, P. Spatrick, F. He, M. Kawana, H. Feng, A. Jacobson, S. W. Peltz, H. L. Sweeney, PTC124 targets genetic disorders caused by nonsense mutations. Nature 447, 87-91 (2007).
54. D. G. Allen, N. P. Whitehead, Duchenne muscular dystrophy-What causes the increased membrane permeability in skeletal muscle? Int. J. Biochem. Cell Biol. 43, 290-294 (2011).
55. J. E. Rooney, P. B. Gurpur, D. J. Burkin, Laminin-111 protein therapy prevents muscle disease in the mdx mouse model for Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. U.S.A. 106, 7991-7996 (2009).
56. K. J. Sonnemann, H. Heun-Johnson, A. J. Turner, K. A. Baltgalvis, D. A. Lowe, J. M. Ervasti, Functional substitution by TAT-utrophin in dystrophin-deficient mice. PLoS Med. 6, e1000083 (2009).