Matrix metalloproteinase 13 is a new contributor to skeletal muscle regeneration and critical for myoblast migration

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 5, 2013, Pages

  Lei, Hanqin ^a   Leong, Dephne ^a   Smith, Lucas R ^a,b   Barton, Elisabeth R ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Collagenase; Matrix metalloproteinase; Muscle repair; Myoblast maturation

Indexed keywords

CARDIOTOXIN; COLLAGENASE 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL FUSION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; MALE; MOUSE; MUSCLE INJURY; MUSCLE REGENERATION; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE;

COLLAGENASE; MATRIX METALLOPROTEINASE; MUSCLE REPAIR; MYOBLAST MATURATION;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; COBRA CARDIOTOXIN PROTEINS; GENE EXPRESSION; MALE; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE INHIBITORS; MICE; MICE, INBRED C57BL; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYOBLASTS; REGENERATION;

EID: 84883392475     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00051.2013     Document Type: Article

References (35)

1. Bani C, Lagrota-Candido J, Pinheiro DF, Leite PE, Salimena MC, Henriques-Pons A, Quirico-Santos T. Pattern of metalloprotease activity and myofiber regeneration in skeletal muscles of mdx mice. Muscle Nerve 37: 583-592, 2008.
2. Barton ER, DeMeo J, Lei H. The insulin-like growth factor (IGF)-I E-peptides are required for isoform-specific gene expression and muscle hypertrophy after local IGF-I production. J Appl Physiol 108: 1069-1076, 2010.
3. Bellayr I, Holden K, Mu X, Pan H, Li Y. Matrix metalloproteinase inhibition negatively affects muscle stem cell behavior. Int J Clin Exp Pathol 6: 124-141, 2013.
4. Brisson BK, Barton ER. Insulin-like growth factor-I E-peptide activity is dependent on the IGF-I receptor. PLos One 7: e45588, 2012.
5. Brown MD, Hudlicka O. Modulation of physiological angiogenesis in skeletal muscle by mechanical forces: involvement of VEGF and metalloproteinases. Angiogenesis 6: 1-14, 2003.
6. Caron NJ, Asselin I, Morel G, Tremblay JP. Increased myogenic potential and fusion of matrilysin-expressing myoblasts transplanted in mice. Cell Transplant 8: 465-476, 1999.
7. Cheng XW, Kuzuya M, Nakamura K, Maeda K, Tsuzuki M, Kim W, Sasaki T, Liu Z, Inoue N, Kondo T, Jin H, Numaguchi Y, Okumura K, Yokota M, Iguchi A, Murohara T. Mechanisms underlying the impairment of ischemia-induced neovascularization in matrix metalloproteinase 2-deficient mice. Circ Res 100: 904-913, 2007.
8. Engel CK, Pirard B, Schimanski S, Kirsch R, Habermann J, Klingler O, Schlotte V, Weithmann KU, Wendt KU. Structural basis for the highly selective inhibition of MMP-13. Chem Biol 12: 181-189, 2005.
9. Fowlkes JL, Thrailkill KM, Serra DM, Suzuki K, Nagase H. Matrix metalloproteinases as insulin-like growth factor binding protein-degrading proteinases. Prog Growth Factor Res 6: 255-263, 1995.
10. Freije JM, Diez-Itza I, Balbin M, Sanchez LM, Blasco R, Tolivia J, Lopez-Otin C. Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 269: 16766-16773, 1994.
11. Gill SE, Parks WC. Metalloproteinases and their inhibitors: regulators of wound healing. Int J Biochem Cell Biol 40: 1334-1347, 2008.
12. Goetsch SC, Hawke TJ, Gallardo TD, Richardson JA, Garry DJ. Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol Genomics 14: 261-271, 2003.
13. Gogly B, Groult N, Hornebeck W, Godeau G, Pellat B. Collagen zymography as a sensitive and specific technique for the determination of subpicogram levels of interstitial collagenase. Anal Biochem 255: 211-216, 1998.
14. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, Lopez-Otin C, Krane SM. Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci USA 101: 17192-17197, 2004.
15. Kherif S, Lafuma C, Dehaupas M, Lachkar S, Fournier JG, Verdiere-Sahuque M, Fardeau M, Alameddine HS. Expression of matrix metalloproteinases 2 and 9 in regenerating skeletal muscle: a study in experimentally injured and mdx muscles. Dev Biol 205: 158-170, 1999.
16. Kosaki N, Takaishi H, Kamekura S, Kimura T, Okada Y, Minqi L, Amizuka N, Chung UI, Nakamura K, Kawaguchi H, Toyama Y, D'Armiento J. Impaired bone fracture healing in matrix metalloproteinase-13 deficient mice. Biochem Biophys Res Commun 354: 846-851, 2007.
17. Leeman MF, Curran S, Murray GI. The structure, regulation, and function of human matrix metalloproteinase-13. Crit Rev Biochem Mol Biol 37: 149-166, 2002.
18. Li H, Mittal A, Makonchuk DY, Bhatnagar S, Kumar A. Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum Mol Genet 18: 2584-2598, 2009.
19. Mariani TJ, Sandefur S, Roby JD, Pierce RA. Collagenase-3 induction in rat lung fibroblasts requires the combined effects of tumor necrosis factor-α and 12-lipoxygenase metabolites: a model of macrophage-induced, fibroblast-driven extracellular matrix remodeling during inflammatory lung injury. Mol Biol Cell 9: 1411-1424, 1998.
20. Mazor R, Alsaigh T, Shaked H, Altshuler AE, Pocock ES, Kistler EB, Karin M, Schmid-Schonbein GW. Matrix metalloproteinase-1-mediated up-regulation of vascular endothelial growth factor-2 in endothelial cells. J Biol Chem 288: 598-607, 2013.
21. Miller MC, Manning HB, Jain A, Troeberg L, Dudhia J, Essex D, Sandison A, Seiki M, Nanchahal J, Nagase H, Itoh Y. Membrane type 1 matrix metalloproteinase is a crucial promoter of synovial invasion in human rheumatoid arthritis. Arthritis Rheum 60: 686-697, 2009.
22. Mills P, Lafreniere JF, Benabdallah BF, El Fahime M, Tremblay JP. A new pro-migratory activity on human myogenic precursor cells for a synthetic peptide within the E domain of the mechano growth factor. Exp Cell Res 313: 527-537, 2007.
23. Miyazaki D, Nakamura A, Fukushima K, Yoshida K, Takeda S, Ikeda S. Matrix metalloproteinase-2 ablation in dystrophin-deficient mdx muscles reduces angiogenesis resulting in impaired growth of regenerated muscle fibers. Hum Mol Genet 20: 1787-1799, 2011.
24. Nistico P, Bissell MJ, Radisky DC. Epithelial-mesenchymal transition: general principles and pathological relevance with special emphasis on the role of matrix metalloproteinases. Cold Spring Harbor Perspect Biol 4: a011908, 2012.
25. Percival JM, Whitehead NP, Adams ME, Adamo CM, Beavo JA, Froehner SC. Sildenafil reduces respiratory muscle weakness and fibrosis in the mdx mouse model of Duchenne muscular dystrophy. J Pathol 228: 77-87, 2012.
26. Pfeffer LA, Brisson BK, Lei H, Barton ER. The insulin-like growth factor-I E-peptides modulate cell entry of the mature IGF-I protein. Mol Biol Cell 20: 3810-3817, 2009.
27. Siefert SA, Sarkar R. Matrix metalloproteinases in vascular physiology and disease. Vascular 20: 210-216, 2012.
28. Torrente Y, El Fahime E, Caron NJ, Bresolin N, Tremblay JP. Intramuscular migration of myoblasts transplanted after muscle pretreatment with metalloproteinases. Cell Transplant 9: 539-549, 2000.
29. Vihinen P, Kahari VM. Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets. Int J Cancer 99: 157-166, 2002.
30. Wang W, Pan H, Murray K, Jefferson BS, Li Y. Matrix metalloproteinase-1 promotes muscle cell migration and differentiation. Am J Pathol 174: 541-549, 2009.
31. Wu N, Opalenik S, Liu J, Jansen ED, Giro MG, Davidson JM. Real-time visualization of MMP-13 promoter activity in transgenic mice. Matrix Biol 21: 149-161, 2002.
32. Zhang B, Cao X, Liu Y, Cao W, Zhang F, Zhang S, Li H, Ning L, Fu L, Niu Y, Niu R, Sun B, Hao X. Tumor-derived matrix metalloproteinase-13 (MMP-13) correlates with poor prognoses of invasive breast cancer. BMC Cancer 8: 83, 2008.
33. Zhang D, Samani AA, Brodt P. The role of the IGF-I receptor in the regulation of matrix metalloproteinases, tumor invasion and metastasis. Horm Metab Res 35: 802-808, 2003.
34. Zheng Z, Leng Y, Zhou C, Ma Z, Zhong Z, Shi XM, Zhang W. Effects of matrix metalloproteinase-1 on the myogenic differentiation of bone marrow-derived mesenchymal stem cells in vitro. Biochem Biophys Res Commun 428: 309-314, 2012.
35. Zimowska M, Brzoska E, Swierczynska M, Streminska W, Moraczewski J. Distinct patterns of MMP-9 and MMP-2 activity in slow and fast twitch skeletal muscle regeneration in vivo. Int J Dev Biol 52: 307-314, 2008.