A mouse model for dominant collagen VI disorders Heterozygous Deletion of Col6a3 EXON 16

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10293-10307

  Pan, Te Cheng ^a   Zhang, Rui Zhu ^a   Arita, Machiko ^a   Bogdanovich, Sasha ^b   Adams, Sheila M ^c   Gara, Sudheer Kumar ^d   Wagener, Raimund ^d,e   Khurana, Tejvior S ^b   Birk, David E ^c   Chu, Mon Li ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d UNIVERSITY OF COLOGNE   (Germany)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS; MUSCULOSKELETAL SYSTEM;

ANIMAL MODEL; CONNECTIVE TISSUES; GENE MUTATIONS; MOLECULAR DEFECTS; MOUSE MODELS; MUSCULAR DYSTROPHY; MUTANT MICE;

COLLAGEN;

COLLAGEN TYPE 6; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BETHLEM MYOPATHY; CELL DAMAGE; CELL ULTRASTRUCTURE; COL6A3 GENE; COLLAGEN DISEASE; CONTROLLED STUDY; EXON SKIPPING; FEMALE; GENE; GENE DELETION; GENE MUTATION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC CODE; HETEROZYGOSITY; HISTOLOGY; MITOCHONDRION; MOUSE; MUSCULAR DYSTROPHY; MYOPATHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SARCOPLASMIC RETICULUM; ULLRICH CONGENITAL MUSCULAR DYSTROPHY;

CONNECTIVE TISSUE; EXTRACELLULAR MATRIX; FIBROBLAST; MUSCLE; TENDON;

ALLELES; ANIMALS; COLLAGEN TYPE VI; DISEASE MODELS, ANIMAL; EXONS; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; GENES, DOMINANT; HETEROZYGOTE; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MUSCLE CONTRACTION; MUSCLES; MUSCULAR DISEASES; MUSCULAR DYSTROPHIES; PHENOTYPE; SARCOPLASMIC RETICULUM; SEQUENCE DELETION; TENDONS;

EID: 84898627367     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.549311     Document Type: Article

References (50)

1. Engel, J., Furthmayr, H., Odermatt, E., von der Mark, H., Aumailley, M., Fleischmajer, R., and Timpl, R. (1985) Structure and macromolecular organization of type VI collagen. Ann. N.Y. Acad. Sci. 460, 25-37
2. Chu, M. L., Conway, D., Pan, T. C., Baldwin, C., Mann, K., Deutzmann, R., and Timpl, R. (1988) Amino acid sequence of the triple-helical domain of human collagen type VI. J. Biol. Chem. 263, 18601-18606
3. Chu, M. L., Zhang, R. Z., Pan, T. C., Stokes, D., Conway, D., Kuo, H. J., Glanville, R., Mayer, U., Mann, K., and Deutzmann, R. (1990) Mosaic structure of globular domains in the human type VI collagenα3 chain. Similarity to von Willebrand factor, fibronectin, actin, salivary proteins, and aprotinin type protease inhibitors. EMBO J. 9, 385-393
4. Chu, M. L., Pan, T. C., Conway, D., Kuo, H. J., Glanville, R. W., Timpl, R., Mann, K., and Deutzmann, R. (1989) Sequence analysis of α1(VI) and α2(VI) chains of human type VI collagen reveals internal triplication of globular domains similar to the A domains of von Willebrand factor and two α2(VI) chain variants that differ in the carboxy terminus. EMBO J. 8, 1939-1946
5. Gara, S. K., Grumati, P., Urciuolo, A., Bonaldo, P., Kobbe, B., Koch, M., Paulsson, M., and Wagener, R. (2008) Three novel collagen VI chains with high homology to the α3 chain. J. Biol. Chem. 283, 10658-10670
6. Fitzgerald, J., Rich, C., Zhou, F. H., and Hansen, U. (2008) Three novel collagen VI chains,α4(VI),α5(VI), andα6(VI). J. Biol. Chem. 283, 20170-20180
7. Gara, S. K., Grumati, P., Squarzoni, S., Sabatelli, P., Urciuolo, A., Bonaldo, P., Paulsson, M., and Wagener, R. (2011) Differential and restricted expression of novel collagen VI chains in mouse. Matrix Biol. 30, 248-257
8. Bönnemann, C. G. (2011) The collagen VI-related myopathies. Muscle meets its matrix. Nat. Rev. Neurol. 7, 379-390
9. Allamand, V., Briñas, L., Richard, P., Stojkovic, T., Quijano-Roy, S., and Bonne, G. (2011) ColVI myopathies. Where do we stand, where do we go? Skelet. Muscle 1, 30
10. Norwood, F. L., Harling, C., Chinnery, P. F., Eagle, M., Bushby, K., and Straub, V. (2009) Prevalence of genetic muscle disease in Northern England. In-depth analysis of a muscle clinic population. Brain 132, 3175-3186
11. Okada, M., Kawahara, G., Noguchi, S., Sugie, K., Murayama, K., Nonaka, I., Hayashi, Y. K., and Nishino, I. (2007) Primary collagen VI deficiency is the second most common congenital muscular dystrophy in Japan. Neurology 69, 1035-1042
12. Mercuri, E., and Muntoni, F. (2012) The ever-expanding spectrum of congenital muscular dystrophies. Ann. Neurol. 72, 9-17
13. Briñas, L., Richard, P., Quijano-Roy, S., Gartioux, C., Ledeuil, C., Lacène, E., Makri, S., Ferreiro, A., Maugenre, S., Topaloglu, H., Haliloglu, G., Pénisson-Besnier, I., Jeannet, P. Y., Merlini, L., Navarro, C., Toutain, A., Chaigne, D., Desguerre, I., de Die-Smulders, C., Dunand, M., Echenne, B., Eymard, B., Kuntzer, T., Maincent, K., Mayer, M., Plessis, G., Rivier, F., Roelens, F., Stojkovic, T., Taratuto, A. L., Lubieniecki, F., Monges, S., Tranchant, C., Viollet, L., Romero, N. B., Estournet, B., Guicheney, P., and Allamand, V. (2010) Early onset collagen VI myopathies. Genetic and clinical correlations. Ann. Neurol. 68, 511-520
14. 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, 649-655
15. Merlini, L., Martoni, E., Grumati, P., Sabatelli, P., Squarzoni, S., Urciuolo, A., Ferlini, A., Gualandi, F., and Bonaldo, P. (2008) Autosomal recessive myosclerosis myopathy is a collagen VI disorder. Neurology 71, 1245-1253
16. Scacheri, P. C., Gillanders, E. M., Subramony, S. H., Vedanarayanan, V., Crowe, C. A., Thakore, N., Bingler, M., and Hoffman, E. P. (2002) Novel mutations in collagen VI genes. Expansion of the Bethlem myopathy phenotype. Neurology 58, 593-602
17. Camacho Vanegas, O., Bertini, E., Zhang, R. Z., Petrini, S., Minosse, C., Sabatelli, P., Giusti, B., Chu, M. L., and Pepe, G. (2001) Ullrich scleroatonic muscular dystrophy is caused by recessive mutations in collagen type VI. Proc. Natl. Acad. Sci. U.S.A. 98, 7516-7521
18. Pan, T. C., Zhang, R. Z., Sudano, D. G., Marie, S. K., Bönnemann, C. G., and Chu, M. L. (2003) New molecular mechanism for Ullrich congenital muscular dystrophy. A heterozygous in-frame deletion in the COL6A1 gene causes a severe phenotype. Am. J. Hum. Genet. 73, 355-369
19. Zhang, R. Z., Sabatelli, P., Pan, T. C., Squarzoni, S., Mattioli, E., Bertini, E., Pepe, G., and Chu, M. L. (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
20. Peat, R. A., Baker, N. L., Jones, K. J., North, K. N., and Lamandé, S. R. (2007) Variable penetrance of COL6A1 null mutations. Implications for prenatal diagnosis and genetic counselling in Ullrich congenital muscular dystrophy families. Neuromuscul. Disord. 17, 547-557
21. Bonaldo, P., Braghetta, P., Zanetti, M., Piccolo, S., Volpin, D., and Bressan, G. M. (1998) Collagen VI deficiency induces early onset myopathy in the mouse. An animal model for Bethlem myopathy. Hum. Mol. Genet. 7, 2135-2140
22. Pan, T. C., Zhang, R. Z., Markova, D., Arita, M., Zhang, Y., Bogdanovich, S., Khurana, T. S., Bönnemann, C. G., Birk, D. E., and Chu, M. L. (2013) COL6A3 protein deficiency in mice leads to muscle and tendon defects similar to human collagen VI congenital muscular dystrophy. J. Biol. Chem. 288, 14320-14331
23. Lampe, A. K., Zou, Y., Sudano, D., O'Brien, K. K., Hicks, D., Laval, S. H., Charlton, R., Jimenez-Mallebrera, C., Zhang, R. Z., Finkel, R. S., Tennekoon, G., Schreiber, G., van der Knaap, M. S., Marks, H., Straub, V., Flanigan, K. M., Chu, M. L., Muntoni, F., Bushby, K. M., and Bönnemann, C. G. (2008) Exon skipping mutations in collagen VI are common and are predictive for severity and inheritance. Hum. Mutat. 29, 809-822
24. Giusti, B., Lucarini, L., Pietroni, V., Lucioli, S., Bandinelli, B., Sabatelli, P., Squarzoni, S., Petrini, S., Gartioux, C., Talim, B., Roelens, F., Merlini, L., Topaloglu, H., Bertini, E., Guicheney, P., and Pepe, G. (2005) Dominant and recessive COL6A1 mutations in Ullrich scleroatonic muscular dystrophy. Ann. Neurol. 58, 400-410
25. Baker, N. L., Mörgelin, M., Peat, R., Goemans, N., North, K. N., Bateman, J. F., and Lamandé, S. R. (2005) Dominant collagen VI mutations are a common cause of Ullrich congenital muscular dystrophy. Hum. Mol. Genet. 14, 279-293
26. Tillet, E., Wiedemann, H., Golbik, R., Pan, T. C., Zhang, R. Z., Mann, K., Chu, M. L., and Timpl, R. (1994) Recombinant expression and structural and binding properties of α1(VI) and α2(VI) chains of human collagen type VI. Eur. J. Biochem. 221, 177-185
27. Specks, U., Mayer, U., Nischt, R., Spissinger, T., Mann, K., Timpl, R., Engel, J., and Chu, M. L. (1992) Structure of recombinant N-terminal globule of type VI collagen α3 chain and its binding to heparin and hyaluronan. EMBO J. 11, 4281-4290
28. Bogdanovich, S., Krag, T. O., Barton, E. R., Morris, L. D., Whittemore, L. A., Ahima, R. S., and Khurana, T. S. (2002) Functional improvement of dystrophic muscle by myostatin blockade. Nature 420, 418-421
29. Bogdanovich, S., McNally, E. M., and Khurana, T. S. (2008) Myostatin blockade improves function but not histopathology in a murine model of limb-girdle muscular dystrophy 2C. Muscle Nerve 37, 308-316
30. Brooks, S. V., and Faulkner, J. A. (1990) Contraction-induced injury. Recovery of skeletal muscles in young and old mice. Am. J. Physiol. 258, C436-C442
31. u, Y., Ansorge, H. L., Zhang, G., Soslowsky, L. J., Bonaldo, P., Chu, M. L., and Birk, D. E. (2011) Dysfunctional tendon collagen fibrillogenesis in collagen VI null mice. Matrix Biol. 30, 53-61
32. Norris, R. A., Damon, B., Mironov, V., Kasyanov, V., Ramamurthi, A., Moreno-Rodriguez, R., Trusk, T., Potts, J. D., Goodwin, R. L., Davis, J., Hoffman, S., Wen, X., Sugi, Y., Kern, C. B., Mjaatvedt, C. H., Turner, D. K., Oka, T., Conway, S. J., Molkentin, J. D., Forgacs, G., and Markwald, R. R. (2007) Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J. Cell Biochem. 101, 695-711
33. Irwin, W. A., Bergamin, N., Sabatelli, P., Reggiani, C., Megighian, A., Merlini, L., Braghetta, P., Columbaro, M., Volpin, D., Bressan, G. M., Bernardi, P., and Bonaldo, P. (2003) Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat. Genet. 35, 367-371
34. Lamandé, S. R., Mörgelin, M., Selan, C., Jöbsis, G. J., Baas, F., and Bateman, J. F. (2002) Kinked collagen VI tetramers and reduced microfibril formation as a result of Bethlem myopathy and introduced triple helical glycine mutations. J. Biol. Chem. 277, 1949-1956
35. Persikov, A. V., Ramshaw, J. A., Kirkpatrick, A., and Brodsky, B. (2000) Amino acid propensities for the collagen triple-helix. Biochemistry 39, 14960-14967
36. Sabatelli, P., Gualandi, F., Gara, S. K., Grumati, P., Zamparelli, A., Martoni, E., Pellegrini, C., Merlini, L., Ferlini, A., Bonaldo, P., Maraldi, N. M., Paulsson, M., Squarzoni, S., and Wagener, R. (2012) Expression of collagen VI α5 and α6 chains in human muscle and in Duchenne muscular dystrophy-related muscle fibrosis. Matrix Biol. 31, 187-196
37. Sacco, A., Mourkioti, F., Tran, R., Choi, J., Llewellyn, M., Kraft, P., Shkreli, M., Delp, S., Pomerantz, J. H., Artandi, S. E., and Blau, H. M. (2010) Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143, 1059-1071
38. Angelin, A., Tiepolo, T., Sabatelli, P., Grumati, P., Bergamin, N., Golfieri, C., Mattioli, E., Gualandi, F., Ferlini, A., Merlini, L., Maraldi, N. M., Bonaldo, P., and Bernardi, P. (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
39. Merlini, L., Angelin, A., Tiepolo, T., Braghetta, P., Sabatelli, P., Zamparelli, A., Ferlini, A., Maraldi, N. M., Bonaldo, P., and Bernardi, P. (2008) Cyclosporin A corrects mitochondrial dysfunction and muscle apoptosis in patients with collagen VI myopathies. Proc. Natl. Acad. Sci. U.S.A. 105, 5225-5229
40. Gualandi, F., Manzati, E., Sabatelli, P., Passarelli, C., Bovolenta, M., Pellegrini, C., Perrone, D., Squarzoni, S., Pegoraro, E., Bonaldo, P., and Ferlini, A. (2012) Antisense-induced messenger depletion corrects a COL6A2 dominant mutation in Ullrich myopathy. Hum. Gene Ther. 23, 1313-1318
41. Minamitani, T., Ikuta, T., Saito, Y., Takebe, G., Sato, M., Sawa, H., Nishimura, T., Nakamura, F., Takahashi, K., Ariga, H., and Matsumoto, K. (2004) Modulation of collagen fibrillogenesis by tenascin-X and type VI collagen. Exp. Cell Res. 298, 305-315
42. Urciuolo, A., Quarta, M., Morbidoni, V., Gattazzo, F., Molon, S., Grumati, P., Montemurro, F., Tedesco, F. S., Blaauw, B., Cossu, G., Vozzi, G., Rando, T. A., and Bonaldo, P. (2013) Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nat. Commun. 4, 1964
43. Schalkwijk, J., Zweers, M. C., Steijlen, P. M., Dean, W. B., Taylor, G., van Vlijmen, I. M., van Haren, B., Miller, W. L., and Bristow, J. (2001) A recessive form of the Ehlers-Danlos syndrome caused by tenascin-X deficiency. N. Engl. J. Med. 345, 1167-1175
44. Kirschner, J., Hausser, I., Zou, Y., Schreiber, G., Christen, H. J., Brown, S. C., Anton-Lamprecht, I., Muntoni, F., Hanefeld, F., and Bönnemann, C. G. (2005) Ullrich congenital muscular dystrophy. Connective tissue abnormalities in the skin support overlap with Ehlers-Danlos syndromes. Am. J. Med. Genet. A 132A, 296-301
45. Minamitani, T., Ariga, H., and Matsumoto, K. (2004) Deficiency of tenascin-X causes a decrease in the level of expression of type VI collagen. Exp. Cell Res. 297, 49-60
46. Voermans, N. C., Verrijp, K., Eshuis, L., Balemans, M. C., Egging, D., Sterrenburg, E., van Rooij, I. A., van der Laak, J. A., Schalkwijk, J., van der Maarel, S. M., Lammens, M., and van Engelen, B. G. (2011) Mild muscular features in tenascin-X knockout mice, a model of Ehlers-danlos syndrome. Connect. Tissue Res. 52, 422-432
47. Lorts, A., Schwanekamp, J. A., Baudino, T. A., McNally, E. M., and Molkentin, J. D. (2012) Deletion of periostin reduces muscular dystrophy and fibrosis in mice by modulating the transforming growth factor-β pathway. Proc. Natl. Acad. Sci. U.S.A. 109, 10978-10983
48. Ritty, T. M., Roth, R., and Heuser, J. E. (2003) Tendon cell array isolation reveals a previously unknown fibrillin-2-containing macromolecular assembly. Structure 11, 1179-1188
49. Wiberg, C., Hedbom, E., Khairullina, A., Lamandé, S. R., Oldberg, A., Timpl, R., Mörgelin, M., and Heinegard, D. (2001) Biglycan and decorin bind close to the N-terminal region of the collagen VI triple helix. J. Biol. Chem. 276, 18947-18952
50. Chen, S., and Birk, D. E. (2013) The regulatory roles of small leucine-rich proteoglycans in extracellular matrix assembly. FEBS J. 280, 2120-2137