Melanocytes from patients affected by Ullrich congenital muscular dystrophy and Bethlem myopathy have dysfunctional mitochondria that can be rescued with cyclophilin inhibitors

Frontiers in Aging Neuroscience

Volumn 6, Issue NOV, 2014, Pages

  Zulian, Alessandra ^a,b   Tagliavini, Francesca ^b,c   Rizzo, Erika ^a,b   Pellegrini, Camilla ^c   Sardone, Francesca ^b,c   Zini, Nicoletta ^b,c   Maraldi, Nadir Mario ^b   Santi, Spartaco ^b,c   Faldini, Cesare ^d   Merlini, Luciano ^c   Petronilli, Valeria ^a,b   Bernardi, Paolo ^a,b   Sabatelli, Patrizia ^b,c  

^a UNIVERSITY OF PADOVA   (Italy)

^b CNR   (Italy)

^c RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Collagen VI; Cyclophilin inhibitors; Melanocytes; Mitochondria; Muscular dystrophy; Permeability transition

Indexed keywords

COLLAGEN TYPE 4; CYCLOSPORIN A [4 N METHYLISOLEUCINE]; OLIGOMYCIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; BETHLEM MYOPATHY; CLINICAL ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; DRUG EFFICACY; DUCHENNE MUSCULAR DYSTROPHY; HUMAN; HUMAN CELL; MELANOCYTE; MITOCHONDRION; MUSCULAR DYSTROPHY; MYOPATHY; ULLRICH CONGENITAL MUSCULAR DYSTROPHY;

EID: 84921417882     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00324     Document Type: Article

References (58)

1. Angelin, A., Bonaldo, P., and Bernardi, P. (2008). Altered threshold of the mitochondrial permeability transition pore in Ullrich congenital muscular dystrophy. Biochim. Biophys. Acta 1777, 893-896. doi: 10.1016/j.bbabio.2008.03.026
2. Angelin, A., Tiepolo, T., Sabatelli, P., Grumati, P., Bergamin, N., Golfieri, C., et al. (2007). Mitochondrial dysfunction in the pathogenesis of Ullrich congenital muscular dystrophy and prospective therapy with cyclosporins. Proc. Natl. Acad. Sci. U.S.A. 104, 991-996. doi:10.1073/pnas.0610270104
3. Bernardi, P. (2013). The mitochondrial permeability transition pore: a mystery solved? Front. Physiol. 4:95. doi:10.3389/fphys.2013.00095
4. Bernardi, P., Scorrano, L., Colonna, R., Petronilli, V., and Di Lisa, F. (1999). Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur. J. Biochem. 264, 687-701. doi:10.1046/j.1432-1327.1999.00725.x
5. Bertini, E., and Pepe, G. (2002). Collagen type VI and related disorders: Bethlem myopathy and Ullrich scleroatonic muscular dystrophy. Eur. J. Paediatr. Neurol. 6, 193-198. doi:10.1053/ejpn.2002.0593
6. Bethlem, J., and Wijngaarden, G. K. (1976). Benign myopathy, with autosomal dominant inheritance. A report on three pedigrees. Brain 99, 91-100. doi:10.1093/brain/99.1.91
7. Camacho Vanegas, O., Bertini, E., Zhang, R. Z., Petrini, S., Minosse, C., Sabatelli, P., et al. (2001). Ullrich scleroatonic muscular dystrophy is caused by recessive mutations in collagen type VI. Proc. Natl. Acad. Sci. U.S.A. 98, 7516-7521. doi:10.1073/pnas.121027598
8. Campoli, M., Ferrone, S., and Wang, X. (2010). Functional and clinical relevance of chondroitin sulfate proteoglycan 4. Adv. Cancer Res. 109, 73-121. doi:10.1016/B978-0-12-380890-5.00003-X
9. Clerc, P., Carey, G. B., Mehrabian, Z., Wei, M., Hwang, H., Girnun, G. D., et al. (2012). Rapid detection of an ABT-737-sensitive primed for death state in cells using microplate-based respirometry. PLoS ONE 7:e42487. doi:10.1371/journal.pone.0042487
10. Colombatti, A., and Bonaldo, P. (1987). Biosynthesis of chick type VI collagen. II. Processing and secretion in fibroblasts and smooth muscle cells. J. Biol. Chem. 262, 14461-14466.
11. Daum, S., Schumann, M., Mathea, S., Aumuller, T., Balsley, M. A., Constant, S. L., et al. (2009). Isoform-specific inhibition of cyclophilins. Biochemistry 48, 6268-6277. doi:10.1021/bi9007287
12. Di Lisa, F., Menabò, R., Canton, M., Barile, M., and Bernardi, P. (2001). Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J. Biol. Chem. 276, 2571-2575. doi:10.1074/jbc. M006825200
13. Gao, F. L., Jin, R., Zhang, L., and Zhang, Y. G. (2013). The contribution of melanocytes to pathological scar formation during wound healing. Int. J. Clin. Exp. Med. 6, 609-613.
14. Gara, S. K., Grumati, P., Urciuolo, A., Bonaldo, P., Kobbe, B., Koch, M., et al. (2008). Three novel collagen VI chains with high homology to the alpha3 chain. J. Biol. Chem. 283, 10658-10670. doi:10.1074/jbc. M709540200
15. Giorgio, V., von Stockum, S., Antoniel, M., Fabbro, A., Fogolari, F., Forte, M., et al. (2013). Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl. Acad. Sci. U.S.A. 110, 5887-5892. doi:10.1073/pnas.1217823110
16. Grumati, P., Coletto, L., Sabatelli, P., Cescon, M., Angelin, A., Bertaggia, E., et al. (2010). Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat. Med. 16, 1313-1320. doi:10.1038/nm.2247
17. Herzog, C., Has, C., Franzke, C. W., Echtermeyer, F. G., Schlötzer-Schrehardt, U., Kröger, S., et al. (2004). Dystroglycan in skin and cutaneous cells: beta-subunit is shed from the cell surface. J. Invest. Dermatol. 122, 1372-1380. doi:10.1111/j.0022-202X.2004.22605.x
18. Hüser, J., and Blatter, L. A. (1999). Fluctuations in mitochondrial membrane potential caused by repetitive gating of the permeability transition pore. Biochem. J. 343(Pt 2), 311-317. doi:10.1042/0264-6021:3430311
19. Hüser, J., Rechenmacher, C. E., and Blatter, L. A. (1998). Imaging the permeability pore transition in single mitochondria. Biophys. J. 74, 2129-2137. doi:10.1016/S0006-3495(98)77920-2
20. Irwin, W. A., Bergamin, N., Sabatelli, P., Reggiani, C., Megighian, A., Merlini, L., et al. (2003). Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat. Genet. 35, 267-271. doi:10.1038/ng1270
21. Jöbsis, G. J., Boers, J. M., Barth, P. G., and de Visser, M. (1999). Bethlem myopathy: a slowly progressive congenital muscular dystrophy with contractures. Brain 122(Pt 4), 649-655. doi:10.1093/brain/122.4.649
22. Kawahara, G., Ogawa, M., Okada, M., Malicdan, M. C., Goto, Y., Hayashi, Y. K., et al. (2008). Diminished binding of mutated collagen VI to the extracellular matrix surrounding myocytes. Muscle Nerve 38, 1192-1195. doi:10.1002/mus.21030
23. Kuo, H. J., Maslen, C. L., Keene, D. R., and Glanville, R. W. (1997). Type VI collagen anchors endothelial basement membranes by interacting with type IV collagen. J. Biol. Chem. 272, 26522-26529. doi:10.1074/jbc.272.42.26522
24. Lampe, A. K., and Bushby, K. M. (2005). Collagen VI related muscle disorders. J. Med. Genet. 42, 673-685. doi:10.1136/jmg.2002.002311
25. Menazza, S., Blaauw, B., Tiepolo, T., Toniolo, L., Braghetta, P., Spolaore, B., et al. (2010). Oxidative stress by monoamine oxidases is causally involved in myofiber damage in muscular dystrophy. Hum. Mol. Genet. 19, 4207-4215. doi:10.1093/hmg/ddq339
26. Merlini, L., Angelin, A., Tiepolo, T., Braghetta, P., Sabatelli, P., Zamparelli, A., et al. (2008a). Cyclosporin A corrects mitochondrial dysfunction and muscle apoptosis in patients with collagen VI myopathies. Proc. Natl. Acad. Sci. U.S.A. 105, 5225-5229. doi:10.1073/pnas.0800962105
27. Merlini, L., Martoni, E., Grumati, P., Sabatelli, P., Squarzoni, S., Urciuolo, A., et al. (2008b). Autosomal recessive myosclerosis myopathy is a collagen VI disorder. Neurology 71, 1245-1253. doi:10.1212/01.wnl.0000327611.01687.5e
28. Merlini, L., and Bernardi, P. (2008). Therapy of collagen VI-related myopathies (Bethlem and Ullrich). Neurotherapeutics 5, 613-618. doi:10.1016/j.nurt.2008.08.004
29. Merlini, L., Morandi, L., Granata, C., and Ballestrazzi, A. (1994). Bethlem myopathy: early-onset benign autosomal dominant myopathy with contractures. Description of two new families. Neuromuscul. Disord. 4, 503-511. doi:10.1016/0960-8966(94)90091-4
30. Millay, D. P., Sargent, M. A., Osinska, H., Baines, C. P., Barton, E. R., Vuagniaux, G., et al. (2008). Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat. Med. 14, 442-447. doi:10.1038/nm1736
31. Nicolli, A., Basso, E., Petronilli, V., Wenger, R. M., and Bernardi, P. (1996). Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, a cyclosporin A-sensitive channel. J. Biol. Chem. 271, 2185-2192. doi:10.1074/jbc.271.4.2185
32. Pellegrini, C., Zulian, A., Gualandi, F., Manzati, E., Merlini, L., Michelini, M. E., et al. (2013). Melanocytes-A novel tool to study mitochondrial dysfunction in Duchenne muscular dystrophy. J. Cell Physiol. 228, 1323-1331. doi:10.1002/jcp.24290
33. Penzo, D., Petronilli, V., Angelin, A., Cusan, C., Colonna, R., Scorrano, L., et al. (2004). Arachidonic acid released by phospholipase A2 activation triggers Ca2+-dependent apoptosis through the mitochondrial pathway. J. Biol. Chem. 279, 25219-25225. doi:10.1074/jbc. M310381200
34. Pepe, G., Bertini, E., Bonaldo, P., Bushby, K., Giusti, B., de Visser, M., et al. (2002). Bethlem myopathy (BETHLEM) and Ullrich scleroatonic muscular dystrophy: 100th ENMC international workshop, 23-24 November 2001, Naarden, The Netherlands. Neuromuscul. Disord. 12, 984-993. doi:10.1016/S0960-8966(02)00139-6
35. Petronilli, V., Miotto, G., Canton, M., Brini, M., Colonna, R., Bernardi, P., et al. (1999). Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 76, 725-734. doi:10.1016/S0006-3495(99)77239-5
36. Petronilli, V., Penzo, D., Scorrano, L., Bernardi, P., and Di Lisa, F. (2001). The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J. Biol. Chem. 276, 12030-12034. doi:10.1074/jbc. M010604200
37. Pfaff, M., Aumailley, M., Specks, U., Knolle, J., Zerwes, H. G., and Timpl, R. (1993). Integrin and Arg-Gly-Asp dependence of cell adhesion to the native and unfolded triple helix of collagen type VI. Exp. Cell Res. 206, 167-176. doi:10.1006/excr.1993.1134
38. Pinon, P., and Wehrle-Haller, B. (2011). Integrins: versatile receptors controlling melanocyte adhesion, migration and proliferation. Pigment Cell Melanoma Res. 24, 282-294. doi:10.1111/j.1755-148X.2010.00806.x
39. Reutenauer, J., Dorchies, O. M., Patthey-Vuadens, O., Vuagniaux, G., and Ruegg, U. T. (2008). Investigation of Debio 025, a cyclophilin inhibitor, in the dystrophic mdx mouse, a model for Duchenne muscular dystrophy. Br. J. Pharmacol 155, 574-584. doi:10.1038/bjp.2008.285
40. Sabatelli, P., Gara, S. K., Grumati, P., Urciuolo, A., Gualandi, F., Curci, R., et al. (2011). Expression of the collagen VI alpha5 and alpha6 chains in normal human skin and in skin of patients with collagen VI-related myopathies. J. Invest. Dermatol. 131, 99-107. doi:10.1038/jid.2010.284
41. Sabatelli, P., Gualandi, F., Gara, S. K., Grumati, P., Zamparelli, A., Martoni, E., et al. (2012a). Expression of collagen VI alpha5 and alpha6 chains in human muscle and in Duchenne muscular dystrophy-related muscle fibrosis. Matrix Biol. 31, 187-196. doi:10.1016/j.matbio.2011.12.003
42. Sabatelli, P., Palma, E., Angelin, A., Squarzoni, S., Urciuolo, A., Pellegrini, C., et al. (2012b). Critical evaluation of the use of cell cultures for inclusion in clinical trials of patients affected by collagen VI myopathies. J. Cell. Physiol. 227, 2927-2935. doi:10.1002/jcp.23039
43. Santiago-Walker, A., Li, L., Haass, N. K., and Herlyn, M. (2009). Melanocytes: from morphology to application. Skin Pharmacol. Physiol. 22, 114-121. doi:10.1159/000178870
44. Scorrano, L., Penzo, D., Petronilli, V., Pagano, F., and Bernardi, P. (2001). Arachidonic acid causes cell death through the mitochondrial permeability transition. Implications for tumor necrosis factor-a apoptotic signaling. J. Biol. Chem. 276, 12035-12040. doi:10.1074/jbc. M010603200
45. Sewry, C. A., Philpot, J., Sorokin, L. M., Wilson, L. A., Naom, I., Goodwin, F., et al. (1996). Diagnosis of merosin (laminin-2) deficient congenital muscular dystrophy by skin biopsy. Lancet 347, 582-584. doi:10.1016/S0140-6736(96)91274-X
46. Sorato, E., Menazza, S., Zulian, A., Sabatelli, P., Gualandi, F., Merlini, L., et al. (2014). Monoamine oxidase inhibition prevents mitochondrial dysfunction and apoptosis in myoblasts from patients with collagen VI myopathies. Free Radic. Biol. Med. 75C, 40-47. doi:10.1016/j.freeradbiomed.2014.07.006
47. Tagliavini, F., Pellegrini, C., Sardone, F., Squarzoni, S., Paulsson, M., Wagener, R., et al. (2014). Defective collagen VI alpha6 chain expression in the skeletal muscle of patients with collagen VI-related myopathies. Biochim. Biophys. Acta 1842, 1604-1612. doi:10.1016/j.bbadis.2014.05.033
48. Telfer, W. R., Busta, A. S., Bonnemann, C. G., Feldman, E. L., and Dowling, J. J. (2010). Zebrafish models of collagen VI-related myopathies. Hum. Mol. Genet. 19, 2433-2444. doi:10.1093/hmg/ddq126
49. Tiepolo, T., Angelin, A., Palma, E., Sabatelli, P., Merlini, L., Nicolosi, L., et al. (2009). The cyclophilin inhibitor Debio 025 normalizes mitochondrial function, muscle apoptosis and ultrastructural defects in Col6a1-/- myopathic mice. Br. J. Pharmacol. 157, 1045-1052. doi:10.1111/j.1476-5381.2009.00316.x
50. Ullrich, O. (1930). Kongenitale, atonisch-sklerotische Muskeldystrophie, ein weiterer Typus der heredodegenerativen Erkrankungen des neuromuskulaeren Systems. Z. Ges. Neurol. Psychiatr. 126, 171-201. doi:10.1007/BF02864097
51. Vinogradov, A., Scarpa, A., and Chance, B. (1972). Calcium and pyridine nucleotide interaction in mitochondrial membranes. Arch. Biochem. Biophys. 152, 646-654. doi:10.1016/0003-9861(72)90261-5
52. Wiberg, C., Heinegård, D., Wenglén, C., Timpl, R., and Mörgelin, M. (2002). Biglycan organizes collagen VI into hexagonal-like networks resembling tissue structures. J. Biol. Chem. 277, 49120-49126. doi:10.1074/jbc. M206891200
53. Wissing, E. R., Millay, D. P., Vuagniaux, G., and Molkentin, J. D. (2010). Debio-025 is more effective than prednisone in reducing muscular pathology in mdx mice. Neuromuscul. Disord. 20, 753-760. doi:10.1016/j.nmd.2010.06.016
54. Wu, M., Neilson, A., Swift, A. L., Moran, R., Tamagnine, J., Parslow, D., et al. (2007). Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292, C125-C136. doi:10.1152/ajpcell.00247.2006
55. Zambruno, G., Marchisio, P. C., Melchiori, A., Bondanza, S., Cancedda, R., and De Luca, M. (1993). Expression of integrin receptors and their role in adhesion, spreading and migration of normal human melanocytes. J. Cell Sci. 105(Pt 1), 179-190.
56. Zhang, R. Z., Sabatelli, P., Pan, T. C., Squarzoni, S., Mattioli, E., Bertini, E., et al. (2002). Effects on collagen VI mRNA stability and microfibrillar assembly of three COL6A2 mutations in two families with Ullrich congenital muscular dystrophy. J. Biol. Chem. 277, 43557-43564. doi:10.1074/jbc. M207696200
57. Zou, Y., Zhang, R. Z., Sabatelli, P., Chu, M. L., and Bonnemann, C. G. (2008). Muscle interstitial fibroblasts are the main source of collagen VI synthesis in skeletal muscle: implications for congenital muscular dystrophy types Ullrich and Bethlem. J. Neuropathol. Exp. Neurol. 67, 144-154. doi:10.1097/nen.0b013e3181634ef7
58. Zulian, A., Rizzo, E., Schiavone, M., Palma, E., Tagliavini, F., Blaauw, B., et al. (2014). NIM811, a cyclophilin inhibitor without immunosuppressive activity, is beneficial in collagen VI congenital muscular dystrophy models. Hum. Mol. Genet. 23, 5353-5363. doi:10.1093/hmg/ddu254