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Muscle Cell Membrane Repair and Therapeutic Implications

  • Renzhi HanEmail author
Chapter

Abstract

Plasma membrane forms the physical barrier that separates the cellular interior from the exterior environment, and its integrity is essential for cell survival and function. Mammalian cells have evolved efficient membrane repair mechanisms that are activated to reseal injured plasma membrane and maintain cell viability. Many of the membrane repair proteins have first been identified in skeletal muscle, where defects in the genes encoding these proteins often lead to myopathies. Dysferlin is a muscle-specific protein implicated in mediating Ca2+-activated membrane-membrane fusion to facilitate membrane repair. Genetic mutations in dysferlin gene are linked to several forms of muscular dystrophy. Likewise, anoctamin 5 (Ano5), synaptotagmin VII (Syt7), and TRPML1 have been found to play roles in muscle membrane repair, and their genetic defects have been shown to cause various forms of myopathies. Other proteins such as MG53 and annexins were found to interact with dysferlin and modulate the membrane repair process and other membrane tracking events in muscle. Given the importance of membrane integrity in human health and disease in general, the membrane repair proteins have become promising targets for therapeutic development that are aimed to boost the intrinsic membrane repair function of the cells.

Keywords

Anoctamin 5 Dysferlin Gene therapy Membrane repair MG53 Muscular dystrophy TMEM16E 

Notes

Acknowledgments

R.H. is supported by US National Institutes of Health grants R01-HL116546 and R01-AR064241.

Competing Interests

The authors declare no competing financial interests.

References

  1. 1.
    McNeil PL, Khakee R (1992) Disruptions of muscle fiber plasma membranes. Role in exercise-induced damage. Am J Pathol 140(5):1097–1109PubMedPubMedCentralGoogle Scholar
  2. 2.
    Liu J, Aoki M, Illa I, Wu C, Fardeau M, Angelini C, Serrano C, Urtizberea JA, Hentati F, Hamida MB, Bohlega S, Culper EJ, Amato AA, Bossie K, Oeltjen J, Bejaoui K, McKenna-Yasek D, Hosler BA, Schurr E, Arahata K, de Jong PJ, Brown RH Jr (1998) Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat Genet 20(1):31–36CrossRefGoogle Scholar
  3. 3.
    Bashir R, Britton S, Strachan T, Keers S, Vafiadaki E, Lako M, Richard I, Marchand S, Bourg N, Argov Z, Sadeh M, Mahjneh I, Marconi G, Passos-Bueno MR, Moreira Ede S, Zatz M, Beckmann JS, Bushby K (1998) A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nat Genet 20(1):37–42CrossRefGoogle Scholar
  4. 4.
    Bansal D, Miyake K, Vogel SS, Groh S, Chen CC, Williamson R, McNeil PL, Campbell KP (2003) Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423(6936):168–172CrossRefGoogle Scholar
  5. 5.
    Chakrabarti S, Kobayashi KS, Flavell RA, Marks CB, Miyake K, Liston DR, Fowler KT, Gorelick FS, Andrews NW (2003) Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice. J Cell Biol 162(4):543–549. jcb.200305131 [pii].  https://doi.org/10.1083/jcb.200305131 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Cheng XP, Zhang XL, Gao Q, Samie MA, Azar M, Tsang WL, Dong LB, Sahoo N, Li XR, Zhuo Y, Garrity AG, Wang X, Ferrer M, Dowling J, Xu L, Han RZ, Xu HX (2014) The intracellular Ca2+ channel MCOLN1 is required for sarcolemma repair to prevent muscular dystrophy. Nat Med 20(10):1187–1192.  https://doi.org/10.1038/nm.3611 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Bolduc V, Marlow G, Boycott KM, Saleki K, Inoue H, Kroon J, Itakura M, Robitaille Y, Parent L, Baas F, Mizuta K, Kamata N, Richard I, Linssen WH, Mahjneh I, de Visser M, Bashir R, Brais B (2010) Recessive mutations in the putative calcium-activated chloride channel Anoctamin 5 cause proximal LGMD2L and distal MMD3 muscular dystrophies. Am J Hum Genet 86(2):213–221. S0002-9297(09)00574-6 [pii].  https://doi.org/10.1016/j.ajhg.2009.12.013 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Hicks D, Sarkozy A, Muelas N, Koehler K, Huebner A, Hudson G, Chinnery PF, Barresi R, Eagle M, Polvikoski T, Bailey G, Miller J, Radunovic A, Hughes PJ, Roberts R, Krause S, Walter MC, Laval SH, Straub V, Lochmuller H, Bushby K (2011) A founder mutation in Anoctamin 5 is a major cause of limb-girdle muscular dystrophy. Brain 134:171–182.  https://doi.org/10.1093/Brain/Awq294 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Jaiswal JK, Marlow G, Summerill G, Mahjneh I, Mueller S, Hill M, Miyake K, Haase H, Anderson LV, Richard I, Kiuru-Enari S, McNeil PL, Simon SM, Bashir R (2007) Patients with a non-dysferlin Miyoshi myopathy have a novel membrane repair defect. Traffic 8(1):77–88CrossRefGoogle Scholar
  10. 10.
    Cai C, Masumiya H, Weisleder N, Matsuda N, Nishi M, Hwang M, Ko JK, Lin P, Thornton A, Zhao X, Pan Z, Komazaki S, Brotto M, Takeshima H, Ma J (2009) MG53 nucleates assembly of cell membrane repair machinery. Nat Cell Biol 11(1):56–64. ncb1812 [pii].  https://doi.org/10.1038/ncb1812 CrossRefPubMedGoogle Scholar
  11. 11.
    McNeil AK, Rescher U, Gerke V, McNeil PL (2006) Requirement for annexin A1 in plasma membrane repair. J Biol Chem 281(46):35202–35207. M606406200 [pii].  https://doi.org/10.1074/jbc.M606406200 CrossRefPubMedGoogle Scholar
  12. 12.
    Lennon NJ, Kho A, Bacskai BJ, Perlmutter SL, Hyman BT, Brown RH Jr (2003) Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing. J Biol Chem 278(50):50466–50473CrossRefGoogle Scholar
  13. 13.
    Bouter A, Gounou C, Berat R, Tan S, Gallois B, Granier T, d'Estaintot BL, Poschl E, Brachvogel B, Brisson AR (2011) Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat Commun 2:270. ncomms1270 [pii].  https://doi.org/10.1038/ncomms1270 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Swaggart KA, Demonbreun AR, Vo AH, Swanson KE, Kim EY, Fahrenbach JP, Holley-Cuthrell J, Eskin A, Chen ZG, Squire K, Heydemann A, Palmer AA, Nelson SF, McNally EM (2014) Annexin A6 modifies muscular dystrophy by mediating sarcolemmal repair. Proc Natl Acad Sci U S A 111(16):6004–6009.  https://doi.org/10.1073/pnas.1324242111 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Demonbreun AR, Quattrocelli M, Barefield DY, Allen MV, Swanson KE, McNally EM (2016) An actin-dependent annexin complex mediates plasma membrane repair in muscle. J Cell Biol 213(6):705–718.  https://doi.org/10.1083/jcb.201512022 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Potez S, Luginbuhl M, Monastyrskaya K, Hostettler A, Draeger A, Babiychuk EB (2011) Tailored protection against plasmalemmal injury by annexins with different Ca2+ sensitivities. J Biol Chem 286(20):17982–17991.  https://doi.org/10.1074/jbc.M110.187625 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Mellgren RL, Miyake K, Kramerova I, Spencer MJ, Bourg N, Bartoli M, Richard I, Greer PA, McNeil PL (2009) Calcium-dependent plasma membrane repair requires m- or mu-calpain, but not calpain-3, the proteasome, or caspases. Biochim Biophys Acta 1793(12):1886–1893. S0167-4889(09)00238-9 [pii].  https://doi.org/10.1016/j.bbamcr.2009.09.013 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Mellgren RL, Huang X (2007) Fetuin A stabilizes m-calpain and facilitates plasma membrane repair. J Biol Chem 282(49):35868–35877CrossRefGoogle Scholar
  19. 19.
    Redpath GM, Woolger N, Piper AK, Lemckert FA, Lek A, Greer PA, North KN, Cooper ST (2014) Calpain cleavage within dysferlin exon 40a releases a synaptotagmin-like module for membrane repair. Mol Biol Cell 25(19):3037–3048.  https://doi.org/10.1091/mbc.E14-04-0947 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Lek A, Evesson FJ, Lemckert FA, Redpath GM, Lueders AK, Turnbull L, Whitchurch CB, North KN, Cooper ST (2013) Calpains, cleaved mini-dysferlinC72, and L-type channels underpin calcium-dependent muscle membrane repair. J Neurosci 33(12):5085–5094.  https://doi.org/10.1523/JNEUROSCI.3560-12.2013 CrossRefPubMedGoogle Scholar
  21. 21.
    Scheffer LL, Sreetama SC, Sharma N, Medikayala S, Brown KJ, Defour A, Jaiswal JK (2014) Mechanism of Ca(2)(+)-triggered ESCRT assembly and regulation of cell membrane repair. Nat Commun 5:5646.  https://doi.org/10.1038/ncomms6646 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Jimenez AJ, Maiuri P, Lafaurie-Janvore J, Divoux S, Piel M, Perez F (2014) ESCRT machinery is required for plasma membrane repair. Science 343(6174):986. ARTN 1247136.  https://doi.org/10.1126/science.1247136 CrossRefGoogle Scholar
  23. 23.
    Illa I, Serrano-Munuera C, Gallardo E, Lasa A, Rojas-Garcia R, Palmer J, Gallano P, Baiget M, Matsuda C, Brown RH (2001) Distal anterior compartment myopathy: a dysferlin mutation causing a new muscular dystrophy phenotype. Ann Neurol 49(1):130–134CrossRefGoogle Scholar
  24. 24.
    Bansal D, Campbell KP (2004) Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol 14(4):206–213. S0962892404000546 [pii].  https://doi.org/10.1016/j.tcb.2004.03.001 CrossRefPubMedGoogle Scholar
  25. 25.
    Han R, Campbell KP (2007) Dysferlin and muscle membrane repair. Curr Opin Cell Biol 19(4):409–416. S0955-0674(07)00099-3 [pii].  https://doi.org/10.1016/j.ceb.2007.07.001 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Davis DB, Doherty KR, Delmonte AJ, McNally EM (2002) Calcium-sensitive phospholipid binding properties of normal and mutant ferlin C2 domains. J Biol Chem 277(25):22883–22888CrossRefGoogle Scholar
  27. 27.
    Xu L, Pallikkuth S, Hou Z, Mignery GA, Robia SL, Han R (2011) Dysferlin forms a dimer mediated by the C2 domains and the transmembrane domain in vitro and in living cells. PLoS One 6(11):e27884. PONE-D-11-07224 [pii].  https://doi.org/10.1371/journal.pone.0027884 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Martens S, Kozlov MM, McMahon HT (2007) How synaptotagmin promotes membrane fusion. Science 316(5828):1205–1208CrossRefGoogle Scholar
  29. 29.
    Therrien C, Di Fulvio S, Pickles S, Sinnreich M (2009) Characterization of lipid binding specificities of dysferlin C2 domains reveals novel interactions with phosphoinositides. Biochemistry 48(11):2377–2384.  https://doi.org/10.1021/bi802242r CrossRefPubMedGoogle Scholar
  30. 30.
    Han R, Bansal D, Miyake K, Muniz VP, Weiss RM, McNeil PL, Campbell KP (2007) Dysferlin-mediated membrane repair protects the heart from stress-induced left ventricular injury. J Clin Invest 117(7):1805–1813CrossRefGoogle Scholar
  31. 31.
    Mellgren RL, Zhang W, Miyake K, McNeil PL (2007) Calpain is required for the rapid, calcium-dependent repair of wounded plasma membrane. J Biol Chem 282(4):2567–2575CrossRefGoogle Scholar
  32. 32.
    Godell CM, Smyers ME, Eddleman CS, Ballinger ML, Fishman HM, Bittner GD (1997) Calpain activity promotes the sealing of severed giant axons. Proc Natl Acad Sci U S A 94(9):4751–4756CrossRefGoogle Scholar
  33. 33.
    Middel V, Zhou L, Takamiya M, Beil T, Shahid M, Roostalu U, Grabher C, Rastegar S, Reischl M, Nienhaus GU, Strahle U (2016) Dysferlin-mediated phosphatidylserine sorting engages macrophages in sarcolemma repair. Nat Commun 7:12875.  https://doi.org/10.1038/ncomms12875 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Pedemonte N, Galietta LJ (2014) Structure and function of TMEM16 proteins (anoctamins). Physiol Rev 94(2):419–459.  https://doi.org/10.1152/physrev.00039.2011 CrossRefPubMedGoogle Scholar
  35. 35.
    Brunner JD, Lim NK, Schenck S, Duerst A, Dutzler R (2014) X-ray structure of a calcium-activated TMEM16 lipid scramblase. Nature 516(7530):207.  https://doi.org/10.1038/nature13984 CrossRefPubMedGoogle Scholar
  36. 36.
    Tsutsumi S, Kamata N, Vokes TJ, Maruoka Y, Nakakuki K, Enomoto S, Omura K, Amagasa T, Nagayama M, Saito-Ohara F, Inazawa J, Moritani M, Yamaoka T, Inoue H, Itakura M (2004) The novel gene encoding a putative transmembrane protein is mutated in gnathodiaphyseal dysplasia (GDD). Am J Hum Genet 74(6):1255–1261.  https://doi.org/10.1086/421527 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Marconi C, Binello PB, Badiali G, Caci E, Cusano R, Garibaldi J, Pippucci T, Merlini A, Marchetti C, Rhoden KJ, Galietta LJV, Lalatta F, Balbi P, Seri M (2013) A novel missense mutation in ANO5/TMEM16E is causative for gnathodiaphyseal dyplasia in a large Italian pedigree. Eur J Hum Genet 21(6):613–619.  https://doi.org/10.1038/ejhg.2012.224 CrossRefPubMedGoogle Scholar
  38. 38.
    Mizuta K, Tsutsumi S, Inoue H, Sakamoto Y, Miyatake K, Miyawaki K, Noji S, Kamata N, Itakura M (2007) Molecular characterization of GDD1/TMEM16E, the gene product responsible for autosomal dominant gnathodiaphyseal dysplasia. Biochem Biophys Res Commun 357(1):126–132.  https://doi.org/10.1016/j.bbrc.2007.03.108 CrossRefPubMedGoogle Scholar
  39. 39.
    Tsutsumi S, Inoue H, Sakamoto Y, Mizuta K, Kamata N, Itakura M (2005) Molecular cloning and characterization of the murine gnathodiaphyseal dysplasia gene GDD1. Biochem Biophys Res Commun 331(4):1099–1106. S0006-291X(05)00749-7 [pii].  https://doi.org/10.1016/j.bbrc.2005.03.226 CrossRefPubMedGoogle Scholar
  40. 40.
    Xu J, El Refaey M, Xu L, Zhao L, Gao Y, Floyd K, Karaze T, Janssen PML, Han R (2015) Genetic disruption of Ano5 in mice does not recapitulate human ANO5-deficient muscular dystrophy. Skelet Muscle 5:43CrossRefGoogle Scholar
  41. 41.
    Gyobu S, Miyata H, Ikawa M, Yamazaki D, Takeshima H, Suzuki J, Nagata S (2016) A role of TMEM16E carrying a scrambling domain in sperm motility. Mol Cell Biol 36(4):645–659.  https://doi.org/10.1128/Mcb.00919-15 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Griffin DA, Johnson RW, Whitlock JM, Pozsgai ER, Heller KN, Grose WE, Arnold WD, Sahenk Z, Hartzell HC, Rodino-Klapac LR (2016) Defective membrane fusion and repair in Anoctamin5-deficient muscular dystrophy. Hum Mol Genet 25(10):1900–1911.  https://doi.org/10.1093/hmg/ddw063 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Charton K, Suel-Petat L, Monjaret F, Bourg-Alibert N, Roudaut C, Gicquel E, Udd B, Richard I (2013) The phenotype of dysferlin-deficient mice is not rescued by AAV-mediated transfer of Anoctamin 5. Mol Ther 21:S235–S235Google Scholar
  44. 44.
    Cheng XP, Zhang XL, Yu L, Xu HX (2015) Calcium signaling in membrane repair. Semin Cell Dev Biol 45:24–31.  https://doi.org/10.1016/j.semcdb.2015.10.031 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Cheng XP, Shen DB, Samie M, Xu HX (2010) Mucolipins: intracellular TRPML1-3 channels. FEBS Lett 584(10):2013–2021.  https://doi.org/10.1016/j.febslet.2009.12.056 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Abe K, Puertollano R (2011) Role of TRP channels in the regulation of the endosomal pathway. Physiology 26(1):14–22.  https://doi.org/10.1152/physiol.00048.2010 CrossRefPubMedGoogle Scholar
  47. 47.
    Sun M, Goldin E, Stahl S, Falardeau JL, Kennedy JC, Acierno JS, Bove C, Kaneski CR, Nagle J, Bromley MC, Colman M, Schiffmann R, Slaugenhaupt SA (2000) Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum Mol Genet 9(17):2471–2478.  https://doi.org/10.1093/hmg/9.17.2471 CrossRefPubMedGoogle Scholar
  48. 48.
    Bassi MT, Manzoni M, Monti E, Pizzo MT, Ballabio A, Borsani G (2000) Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV. Am J Hum Genet 67(5):1110–1120.  https://doi.org/10.1016/S0002-9297(07)62941-3 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Bargal R, Avidan N, Ben-Asher E, Olender Z, Zeigler M, Frumkin A, Raas-Rothschild A, Glusman G, Lancet D, Bach G (2000) Identification of the gene causing mucolipidosis type IV. Nat Genet 26(1):118–123.  https://doi.org/10.1038/79095 CrossRefPubMedGoogle Scholar
  50. 50.
    Dong XP, Shen D, Wang X, Dawson T, Li X, Zhang Q, Cheng X, Zhang Y, Weisman LS, Delling M, Xu H (2010) PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun 1:38.  https://doi.org/10.1038/ncomms1037 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Shen D, Wang X, Li X, Zhang X, Yao Z, Dibble S, Dong XP, Yu T, Lieberman AP, Showalter HD, Xu H (2012) Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat Commun 3:731.  https://doi.org/10.1038/ncomms1735 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Zhang X, Li X, Xu H (2012) Phosphoinositide isoforms determine compartment-specific ion channel activity. Proc Natl Acad Sci U S A 109(28):11384–11389.  https://doi.org/10.1073/pnas.1202194109 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Venugopal B, Browning MF, Curcio-Morelli C, Varro A, Michaud N, Nanthakumar N, Walkley SU, Pickel J, Slaugenhaupt SA (2007) Neurologic, gastric, and opthalmologic pathologies in a murine model of mucolipidosis type IV. Am J Hum Genet 81(5):1070–1083.  https://doi.org/10.1086/521954 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Dong XP, Wang X, Shen D, Chen S, Liu M, Wang Y, Mills E, Cheng X, Delling M, Xu H (2009) Activating mutations of the TRPML1 channel revealed by proline-scanning mutagenesis. J Biol Chem 284(46):32040–32052.  https://doi.org/10.1074/jbc.M109.037184 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Samie M, Wang X, Zhang X, Goschka A, Li X, Cheng X, Gregg E, Azar M, Zhuo Y, Garrity AG, Gao Q, Slaugenhaupt S, Pickel J, Zolov SN, Weisman LS, Lenk GM, Titus S, Bryant-Genevier M, Southall N, Juan M, Ferrer M, Xu H (2013) A TRP channel in the lysosome regulates large particle phagocytosis via focal exocytosis. Dev Cell 26(5):511–524.  https://doi.org/10.1016/j.devcel.2013.08.003 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Kozai D, Ogawa N, Mori Y (2014) Redox regulation of transient receptor potential channels. Antioxid Redox Signal 21(6):971–986.  https://doi.org/10.1089/ars.2013.5616 CrossRefPubMedGoogle Scholar
  57. 57.
    Meroni G, Diez-Roux G (2005) TRIM/RBCC, a novel class of ‘single protein RING finger’ E3 ubiquitin ligases. BioEssays 27(11):1147–1157.  https://doi.org/10.1002/bies.20304 CrossRefPubMedGoogle Scholar
  58. 58.
    Duann P, Li H, Lin P, Tan T, Wang Z, Chen K, Zhou X, Gumpper K, Zhu H, Ludwig T, Mohler PJ, Rovin B, Abraham WT, Zeng C, Ma J (2015) MG53-mediated cell membrane repair protects against acute kidney injury. Sci Transl Med 7(279):279–236.  https://doi.org/10.1126/scitranslmed.3010755 CrossRefGoogle Scholar
  59. 59.
    Jia Y, Chen K, Lin P, Lieber G, Nishi M, Yan R, Wang Z, Yao Y, Li Y, Whitson BA, Duann P, Li H, Zhou X, Zhu H, Takeshima H, Hunter JC, McLeod RL, Weisleder N, Zeng C, Ma J (2014) Treatment of acute lung injury by targeting MG53-mediated cell membrane repair. Nat Commun 5:4387.  https://doi.org/10.1038/ncomms5387 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Kim S, Seo J, Ko YG, Huh YD, Park H (2012) Lipid-binding properties of TRIM72. BMB Rep 45(1):26–31CrossRefGoogle Scholar
  61. 61.
    Hwang M, Ko JK, Weisleder N, Takeshima H, Ma JJ (2011) Redox-dependent oligomerization through a leucine zipper motif is essential for MG53-mediated cell membrane repair. Am J Physiol Cell Physiol 301(1):C106–C114.  https://doi.org/10.1152/ajpcell.00382.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Cai C, Lin P, Zhu H, Ko JK, Hwang M, Tan T, Pan Z, Korichneva I, Ma J (2015) Zinc binding to MG53 protein facilitates repair of injury to cell membranes. J Biol Chem 290(22):13830–13839.  https://doi.org/10.1074/jbc.M114.620690 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Li H, Duann P, Lin PH, Zhao L, Fan Z, Tan T, Zhou X, Sun M, Fu M, Orange M, Sermersheim M, Ma H, He D, Steinberg SM, Higgins R, Zhu H, John E, Zeng C, Guan J, Ma J (2015) Modulation of wound healing and scar formation by MG53 protein-mediated cell membrane repair. J Biol Chem 290(40):24592–24603.  https://doi.org/10.1074/jbc.M115.680074 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Flix B, de la Torre C, Castillo J, Casal C, Illa I, Gallardo E (2013) Dysferlin interacts with calsequestrin-1, myomesin-2 and dynein in human skeletal muscle. Int J Biochem Cell Biol 45(8):1927–1938.  https://doi.org/10.1016/j.biocel.2013.06.007 CrossRefPubMedGoogle Scholar
  65. 65.
    Matsuda C, Miyake K, Kameyama K, Keduka E, Takeshima H, Imamura T, Araki N, Nishino I, Hayashi Y (2012) The C2A domain in dysferlin is important for association with MG53 (TRIM72). PLoS Curr 4:e5035add5038caff5034.  https://doi.org/10.1371/5035add8caff4 CrossRefGoogle Scholar
  66. 66.
    Gerke V, Creutz CE, Moss SE (2005) Annexins: linking Ca2+ signalling to membrane dynamics. Nat Rev Mol Cell Biol 6(6):449–461. nrm1661 [pii].  https://doi.org/10.1038/nrm1661 CrossRefPubMedGoogle Scholar
  67. 67.
    Blackwood RA, Ernst JD (1990) Characterization of Ca2(+)-dependent phospholipid binding, vesicle aggregation and membrane fusion by annexins. Biochem J 266(1):195–200CrossRefGoogle Scholar
  68. 68.
    Wang W, Creutz CE (1994) Role of the amino-terminal domain in regulating interactions of annexin I with membranes: effects of amino-terminal truncation and mutagenesis of the phosphorylation sites. Biochemistry 33(1):275–282CrossRefGoogle Scholar
  69. 69.
    Roostalu U, Strahle U (2012) In vivo imaging of molecular interactions at damaged sarcolemma. Dev Cell 22(3):515–529. S1534-5807(11)00574-0 [pii].  https://doi.org/10.1016/j.devcel.2011.12.008 CrossRefPubMedGoogle Scholar
  70. 70.
    Benz J, Bergner A, Hofmann A, Demange P, Gottig P, Liemann S, Huber R, Voges D (1996) The structure of recombinant human annexin VI in crystals and membrane-bound. J Mol Biol 260(5):638–643.  https://doi.org/10.1006/jmbi.1996.0426 CrossRefPubMedGoogle Scholar
  71. 71.
    Buzhynskyy N, Golczak M, Lai-Kee-Him J, Lambert O, Tessier B, Gounou C, Berat R, Simon A, Granier T, Chevalier JM, Mazeres S, Bandorowicz-Pikula J, Pikula S, Brisson AR (2009) Annexin-A6 presents two modes of association with phospholipid membranes. A combined QCM-D, AFM and cryo-TEM study. J Struct Biol 168(1):107–116.  https://doi.org/10.1016/j.jsb.2009.03.007 CrossRefPubMedGoogle Scholar
  72. 72.
    Hawkins TE, Roes J, Rees D, Monkhouse J, Moss SE (1999) Immunological development and cardiovascular function are normal in annexin VI null mutant mice. Mol Cell Biol 19(12):8028–8032CrossRefGoogle Scholar
  73. 73.
    Marg A, Schoewel V, Timmel T, Schulze A, Shah C, Daumke O, Spuler S (2012) Sarcolemmal repair is a slow process and includes EHD2. Traffic 13(9):1286–1294.  https://doi.org/10.1111/j.1600-0854.2012.01386.x CrossRefPubMedGoogle Scholar
  74. 74.
    Jaiswal JK, Lauritzen SP, Scheffer L, Sakaguchi M, Bunkenborg J, Simon SM, Kallunki T, Jaattela M, Nylandsted J (2014) S100A11 is required for efficient plasma membrane repair and survival of invasive cancer cells. Nat Commun 5:3795. ARTN 3795.  https://doi.org/10.1038/ncomms4795 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Mosser G, Ravanat C, Freyssinet JM, Brisson A (1991) Sub-domain structure of lipid-bound annexin-V resolved by electron image analysis. J Mol Biol 217(2):241–245CrossRefGoogle Scholar
  76. 76.
    Skrahina T, Piljic A, Schultz C (2008) Heterogeneity and timing of translocation and membrane-mediated assembly of different annexins. Exp Cell Res 314(5):1039–1047.  https://doi.org/10.1016/j.yexcr.2007.11.015 CrossRefPubMedGoogle Scholar
  77. 77.
    Weisleder N, Takizawa N, Lin P, Wang X, Cao C, Zhang Y, Tan T, Ferrante C, Zhu H, Chen PJ, Yan R, Sterling M, Zhao X, Hwang M, Takeshima M, Cai C, Cheng H, Takeshima H, Xiao RP, Ma J (2012) Recombinant MG53 protein modulates therapeutic cell membrane repair in treatment of muscular dystrophy. Sci Transl Med 4(139):139–185.  https://doi.org/10.1126/scitranslmed.3003921 CrossRefGoogle Scholar
  78. 78.
    Idone V, Tam C, Goss JW, Toomre D, Pypaert M, Andrews NW (2008) Repair of injured plasma membrane by rapid Ca2+−dependent endocytosis. J Cell Biol 180(5):905–914. jcb.200708010 [pii].  https://doi.org/10.1083/jcb.200708010 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Tam C, Idone V, Devlin C, Fernandes MC, Flannery A, He X, Schuchman E, Tabas I, Andrews NW (2010) Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. J Cell Biol 189(6):1027–1038.  https://doi.org/10.1083/jcb.201003053 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Gulbins E (2003) Regulation of death receptor signaling and apoptosis by ceramide. Pharmacol Res 47(5):393–399CrossRefGoogle Scholar
  81. 81.
    van Blitterswijk WJ, van der Luit AH, Veldman RJ, Verheij M, Borst J (2003) Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem J 369(Pt 2):199–211.  https://doi.org/10.1042/BJ20021528 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Babiychuk EB, Monastyrskaya K, Draeger A (2008) Fluorescent annexin A1 reveals dynamics of ceramide platforms in living cells. Traffic 9(10):1757–1775.  https://doi.org/10.1111/j.1600-0854.2008.00800.x CrossRefPubMedGoogle Scholar
  83. 83.
    He B, Tang RH, Weisleder N, Xiao B, Yuan Z, Cai C, Zhu H, Lin P, Qiao C, Li J, Mayer C, Li J, Ma J, Xiao X (2012) Enhancing muscle membrane repair by gene delivery of MG53 ameliorates muscular dystrophy and heart failure in delta-Sarcoglycan-deficient hamsters. Mol Ther 20(4):727–735.  https://doi.org/10.1038/mt.2012.5 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Liu J, Zhu H, Zheng Y, Xu Z, Li L, Tan T, Park KH, Hou J, Zhang C, Li D, Li R, Liu Z, Weisleder N, Zhu D, Lin P, Ma J (2015) Cardioprotection of recombinant human MG53 protein in a porcine model of ischemia and reperfusion injury. J Mol Cell Cardiol 80:10–19.  https://doi.org/10.1016/j.yjmcc.2014.12.010 CrossRefPubMedGoogle Scholar
  85. 85.
    Song R, Peng W, Zhang Y, Lv F, Wu HK, Guo J, Cao Y, Pi Y, Zhang X, Jin L, Zhang M, Jiang P, Liu F, Meng S, Zhang X, Jiang P, Cao CM, Xiao RP (2013) Central role of E3 ubiquitin ligase MG53 in insulin resistance and metabolic disorders. Nature 494(7437):375–379.  https://doi.org/10.1038/nature11834 CrossRefPubMedGoogle Scholar
  86. 86.
    Yi JS, Park JS, Ham YM, Nguyen N, Lee NR, Hong J, Kim BW, Lee H, Lee CS, Jeong BC, Song HK, Cho H, Kim YK, Lee JS, Park KS, Shin H, Choi I, Lee SH, Park WJ, Park SY, Choi CS, Lin P, Karunasiri M, Tan T, Duann P, Zhu H, Ma J, Ko YG (2013) MG53-induced IRS-1 ubiquitination negatively regulates skeletal myogenesis and insulin signalling. Nat Commun 4:2354.  https://doi.org/10.1038/ncomms3354 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Liu F, Song R, Feng Y, Guo J, Chen Y, Zhang Y, Chen T, Wang Y, Huang Y, Li CY, Cao C, Zhang Y, Hu X, Xiao RP (2015) Upregulation of MG53 induces diabetic cardiomyopathy through transcriptional activation of peroxisome proliferation-activated receptor alpha. Circulation 131(9):795–804.  https://doi.org/10.1161/CIRCULATIONAHA.114.012285 CrossRefPubMedGoogle Scholar
  88. 88.
    Lee CS, Yi JS, Jung SY, Kim BW, Lee NR, Choo HJ, Jang SY, Han J, Chi SG, Park M, Lee JH, Ko YG (2010) TRIM72 negatively regulates myogenesis via targeting insulin receptor substrate-1. Cell Death Differ 17(8):1254–1265.  https://doi.org/10.1038/cdd.2010.1 CrossRefPubMedGoogle Scholar
  89. 89.
    Nguyen N, Yi JS, Park H, Lee JS, Ko YG (2014) Mitsugumin 53 (MG53) ligase ubiquitinates focal adhesion kinase during skeletal myogenesis. J Biol Chem 289(6):3209–3216.  https://doi.org/10.1074/jbc.M113.525154 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Surgery, Davis Heart and Lung Research InstituteThe Ohio State University Wexner Medical CenterColumbusUSA

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