Matrix metalloproteinase inhibition negatively affects muscle stem cell behavior

International Journal of Clinical and Experimental Pathology

Volumn 6, Issue 2, 2013, Pages 124-141

  Bellayr, Ian ^a   Holden, Kyle ^b   Mu, Xiaodong ^c   Pan, Haiying ^d   Li, Yong ^d,e  

^a University of Pittsburgh   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS   (United States)

^e UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Cell migration; Differentiation; MMPs; Skeletal muscle stem cells

Indexed keywords

DIPEPTIDE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE INHIBITOR; N (2(R) 2 (HYDROXAMIDOCARBONYLMETHYL) 4 METHYLPENTANOYL) L TRYPTOPHAN METHYLAMIDE; N-(2(R)-2-(HYDROXAMIDOCARBONYLMETHYL)-4-METHYLPENTANOYL)-L-TRYPTOPHAN METHYLAMIDE;

ADIPOGENESIS; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BONE DEVELOPMENT; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELL MIGRATION; CELL MOTION; CYTOLOGY; DIFFERENTIATION; DRUG EFFECT; ENZYMOLOGY; FEMALE; INJURY; METABOLISM; MMPS; MOUSE; PHYSIOLOGY; SKELETAL MUSCLE; SKELETAL MUSCLE STEM CELLS; STEM CELL; WOUND HEALING;

CELL MIGRATION; DIFFERENTIATION; MMPS; SKELETAL MUSCLE STEM CELLS;

ADIPOGENESIS; ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELL MOVEMENT; CELLS, CULTURED; DIPEPTIDES; FEMALE; MATRIX METALLOPROTEINASE INHIBITORS; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; OSTEOGENESIS; STEM CELLS; WOUND HEALING;

MLCS; MLOWN;

EID: 84879811394     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (73)

1. Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004; 84: 209-38.
2. Grefte S, Kuijpers-Jagtman AM, Torensma R, Von den Hoff JW. Skeletal muscle development and regeneration. Stem Cells Dev 2007; 16: 857-68.
3. Huard J, Li Y, Fu FH. Muscle injuries and repair: current trends in research. J Bone Joint Surg Am 2002; 84-A: 822-32.
4. Nozaki M, Li Y, Zhu J, Ambrosio F, Uehara K, Fu FH, Huard J. Improved muscle healing after contusion injury by the inhibitory effect of suramin on myostatin, a negative regulator of muscle growth. Am J Sports Med 2008; 36: 2354-62.
5. Ritenour AE, Christy RJ, Roe JL, Baer DG, Dubick MA, Wade CE, Holcomb JB, Walters TJ. The Effect of a Hypobaric, Hypoxic Environment on Acute Skeletal Muscle Edema after Ischemia-Reperfusion Injury in Rats. Journal of Surgical Research 2010; 160: 253-259.
6. Wu X, Wolf SE, Walters TJ. Muscle contractile properties in severely burned rats. Burns 2010; 36: 905-11.
7. Bellayr I, Mu X, Li Y. Biochemical insights into the role of matrix metalloproteinases in regeneration: challenges and recent developments. Future Med Chem 2009; 1: 1095-1111.
8. Chazaud B, Brigitte M, Yacoub-Youssef H, Arnold L, Gherardi R, Sonnet C, Lafuste P, Chretien F. Dual and beneficial roles of macrophages during skeletal muscle regeneration. Exerc Sport Sci Rev 2009; 37: 18-22.
9. Chazaud B, Sonnet C, Lafuste P, Bassez G, Rimaniol AC, Poron F, Authier FJ, Dreyfus PA, Gherardi RK. Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J Cell Biol 2003; 163: 1133-43.
10. Chen X, Li Y. Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adh Migr 2009; 3: 337-41.
11. Brunelli S, Rovere-Querini P. The immune system and the repair of skeletal muscle. Pharmacol Res 2008; 58: 117-21.
12. Wang W, Pan H, Murray K, Jefferson BS, Li Y. Matrix metalloproteinase-1 promotes muscle cell migration and differentiation. Am J Pathol 2009; 174: 541-9.
13. Ehrhardt J, Morgan J. Regenerative capacity of skeletal muscle. Curr Opin Neurol 2005; 18: 548-53.
14. Ten Broek RW, Grefte S, Von den Hoff JW. Regulatory factors and cell populations involved in skeletal muscle regeneration. J Cell Physiol 2010; 224: 7-16.
15. Kuang S, Gillespie MA, Rudnicki MA. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2008; 2: 22-31.
16. Boonen KJ, Post MJ. The muscle stem cell niche: regulation of satellite cells during regeneration. Tissue Eng Part B Rev 2008; 14: 419-31.
17. Serrano AL, Munoz-Canoves P. Regulation and dysregulation of fibrosis in skeletal muscle. Exp Cell Res 2010; 316: 3050-8.
18. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003; 92: 827-39.
19. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004; 4: 617-29.
20. Gill SE, Parks WC. Metalloproteinases and their inhibitors: regulators of wound healing. Int J Biochem Cell Biol 2008; 40: 1334-47.
21. Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007; 8: 221-33.
22. 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 2008; 37: 583-92.
23. Fukushima K, Nakamura A, Ueda H, Yuasa K, Yoshida K, Takeda S, Ikeda S. Activation and localization of matrix metalloproteinase-2 and -9 in the skeletal muscle of the muscular dystrophy dog (CXMDJ). BMC Musculoskelet Disord 2007; 8: 54.
24. 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 2008; 52: 307-14.
25. Ohtake Y, Tojo H, Seiki M. Multifunctional roles of MT1-MMP in myofiber formation and morphostatic maintenance of skeletal muscle. J Cell Sci 2006; 119: 3822-32.
26. Soini Y, Satta J, Maatta M, Autio-Harmainen H. Expression of MMP2, MMP9, MT1-MMP, TIMP1, and TIMP2 mRNA in valvular lesions of the heart. J Pathol 2001; 194: 225-31.
27. Toth M, Chvyrkova I, Bernardo MM, Hernandez-Barrantes S, Fridman R. Pro-MMP-9 activation by the MT1-MMP/MMP-2 axis and MMP-3: role of TIMP-2 and plasma membranes. Biochem Biophys Res Commun 2003; 308: 386-95.
28. Bedair H, Liu TT, Kaar JL, Badlani S, Russell AJ, Li Y, Huard J. Matrix metalloproteinase-1 therapy improves muscle healing. J Appl Physiol 2007; 102: 2338-45.
29. Kaar JL, Li Y, Blair HC, Asche G, Koepsel RR, Huard J, Russell AJ. Matrix metalloproteinase-1 treatment of muscle fibrosis. Acta Biomater 2008; 4: 1411-20.
30. Han YP, Yan C, Zhou L, Qin L, Tsukamoto H. A matrix metalloproteinase-9 activation cascade by hepatic stellate cells in trans-differentiation in the three-dimensional extracellular matrix. J Biol Chem 2007; 282: 12928-39.
31. Stetler-Stevenson WG. Tissue inhibitors of metalloproteinases in cell signaling: metalloproteinase- independent biological activities. Sci Signal 2008; 1: re6.
32. Melendez-Zajgla J, Del Pozo L, Ceballos G, Maldonado V. Tissue inhibitor of metalloproteinases- 4. The road less traveled. Mol Cancer 2008; 7: 85.
33. Gharaibeh B, Lu A, Tebbets J, Zheng B, Feduska J, Crisan M, Peault B, Cummins J, Huard J. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc 2008; 3: 1501-9.
34. Li Y, Pan H, Huard J. Isolating stem cells from soft musculoskeletal tissues. J Vis Exp 2010.
35. Bae YH, Ding Z, Zou L, Wells A, Gertler F, Roy P. Loss of profilin-1 expression enhances breast cancer cell motility by Ena/VASP proteins. J Cell Physiol 2009; 219: 354-64.
36. Nishita M, Tomizawa C, Yamamoto M, Horita Y, Ohashi K, Mizuno K. Spatial and temporal regulation of cofilin activity by LIM kinase and Slingshot is critical for directional cell migration. J Cell Biol 2005; 171: 349-59.
37. Deasy BM, Gharaibeh BM, Pollett JB, Jones MM, Lucas MA, Kanda Y, Huard J. Long-term self-renewal of postnatal muscle-derived stem cells. Mol Biol Cell 2005; 16: 3323-33.
38. Urish KL, Vella JB, Okada M, Deasy BM, Tobita K, Keller BB, Cao B, Piganelli JD, Huard J. Antioxidant levels represent a major determinant in the regenerative capacity of muscle stem cells. Mol Biol Cell 2009; 20: 509-20.
39. Zheng B, Cao B, Li G, Huard J. Mouse adiposederived stem cells undergo multilineage differentiation in vitro but primarily osteogenic and chondrogenic differentiation in vivo. Tissue Eng 2006; 12: 1891-901.
40. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006; 7: R100.
41. Jankowski RJ, Deasy BM, Huard J. Muscle-derived stem cells. Gene Ther 2002; 9: 642-7.
42. Jankowski RJ, Haluszczak C, Trucco M, Huard J. Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: potential for rapid isolation of musclederived stem cells. Hum Gene Ther 2001; 12: 619-28.
43. Lee JY, Qu-Petersen Z, Cao B, Kimura S, Jankowski R, Cummins J, Usas A, Gates C, Robbins P, Wernig A, Huard J. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol 2000; 150: 1085-100.
44. Corsi KA, Pollett JB, Phillippi JA, Usas A, Li G, Huard J. Osteogenic potential of postnatal skeletal muscle-derived stem cells is influenced by donor sex. J Bone Miner Res 2007; 22: 1592-602.
45. Kim KS, Lee JH, Ahn HH, Lee JY, Khang G, Lee B, Lee HB, Kim MS. The osteogenic differentiation of rat muscle-derived stem cells in vivo within in situ-forming chitosan scaffolds. Biomaterials 2008; 29: 4420-8.
46. Payne KA, Meszaros LB, Phillippi JA, Huard J. Effect of phosphatidyl inositol 3-kinase, extracellular signal-regulated kinases 1/2, and p38 mitogen-activated protein kinase inhibition on osteogenic differentiation of muscle-derived stem cells. Tissue Eng Part A 2010; 16: 3647-55.
47. Bonewald LF, Harris SE, Rosser J, Dallas MR, Dallas SL, Camacho NP, Boyan B, Boskey A. von Kossa staining alone is not sufficient to confirm that mineralization in vitro represents bone formation. Calcif Tissue Int 2003; 72: 537-47.
48. Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, Partridge T, Gussoni E, Kunkel LM, Huard J. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 2007; 15: 867-77.
49. Pawlikowski B, Lee L, Zuo J, Kramer RH. Analysis of human muscle stem cells reveals a differentiation-resistant progenitor cell population expressing Pax7 capable of self-renewal. Dev Dyn 2009; 238: 138-49.
50. Hurme T, Kalimo H, Lehto M, Jarvinen M. Healing of skeletal muscle injury: an ultrastructural and immunohistochemical study. Med Sci Sports Exerc 1991; 23: 801-10.
51. Huard J, Gharaibeh B, Usas A. Regenerative Medicine Based on Muscle-Derived Stem Cells. Oper Tech Orthop 2010; 20: 119-126.
52. Wang XX, Li YC, Ma XP, Han ZC. [Effects of electroacupuncture at Jiaji (EX-B 2) on extracellular matrix MMP-1, MMP-3 and TIMP-1 levels in the degenerated cervical intervertebral disc in rats]. Zhen Ci Yan Jiu 2009; 34: 248-51.
53. Mu X, Urso ML, Murray K, Fu F, Li Y. Relaxin regulates MMP expression and promotes satellite cell mobilization during muscle healing in both young and aged mice. Am J Pathol 2010; 177: 2399-410.
54. Bellayr IH, Mu X, Li Y. Biochemical insights into the role of matrix metalloproteinases in regeneration: challenges and recent developments. Future Med Chem 2009; 1: 1095-1111.
55. Nishimura T, Nakamura K, Kishioka Y, Kato-Mori Y, Wakamatsu J, Hattori A. Inhibition of matrix metalloproteinases suppresses the migration of skeletal muscle cells. J Muscle Res Cell Motil 2008; 29: 37-44.
56. Allen DL, Teitelbaum DH, Kurachi K. Growth factor stimulation of matrix metalloproteinase expression and myoblast migration and invasion in vitro. Am J Physiol Cell Physiol 2003; 284: C805-15.
57. Barnes BR, Szelenyi ER, Warren GL, Urso ML. Alterations in mRNA and protein levels of metalloproteinases- 2, -9, and -14 and tissue inhibitor of metalloproteinase-2 responses to traumatic skeletal muscle injury. Am J Physiol Cell Physiol 2009; 297: C1501-8.
58. El Fahime E, Torrente Y, Caron NJ, Bresolin MD, Tremblay JP. In vivo migration of transplanted myoblasts requires matrix metalloproteinase activity. Exp Cell Res 2000; 258: 279-87.
59. Bellayr IH, Gharaibeh B, Huard J, Li Y. Skeletal muscle-derived stem cells differentiate into hepatocyte-like cells and aid in liver regeneration. Int J Clin Exp Pathol 2010; 3: 681-90.
60. Cao B, Zheng B, Jankowski RJ, Kimura S, Ikezawa M, Deasy B, Cummins J, Epperly M, Qu-Petersen Z, Huard J. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol 2003; 5: 640-6.
61. Kubo S, Cooper GM, Matsumoto T, Phillippi JA, Corsi KA, Usas A, Li G, Fu FH, Huard J. Blocking vascular endothelial growth factor with soluble Flt-1 improves the chondrogenic potential of mouse skeletal muscle-derived stem cells. Arthritis Rheum 2009; 60: 155-65.
62. Lavasani M, Lu A, Peng H, Cummins J, Huard J. Nerve growth factor improves the muscle regeneration capacity of muscle stem cells in dystrophic muscle. Hum Gene Ther 2006; 17: 80-92.
63. Li G, Corsi-Payne K, Zheng B, Usas A, Peng H, Huard J. The dose of growth factors influences the synergistic effect of vascular endothelial growth factor on bone morphogenetic protein 4-induced ectopic bone formation. Tissue Eng Part A 2009; 15: 2123-33.
64. Matsumoto T, Kubo S, Meszaros LB, Corsi KA, Cooper GM, Li G, Usas A, Osawa A, Fu FH, Huard J. The influence of sex on the chondrogenic potential of muscle-derived stem cells: implications for cartilage regeneration and repair. Arthritis Rheum 2008; 58: 3809-19.
65. Romero-Ramos M, Vourc'h P, Young HE, Lucas PA, Wu Y, Chivatakarn O, Zaman R, Dunkelman N, el-Kalay MA, Chesselet MF. Neuronal differentiation of stem cells isolated from adult muscle. J Neurosci Res 2002; 69: 894-907.
66. Smaldone MC, Chancellor MB. Muscle derived stem cell therapy for stress urinary incontinence. World J Urol 2008; 26: 327-32.
67. Bouloumie A, Sengenes C, Portolan G, Galitzky J, Lafontan M. Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes 2001; 50: 2080-6.
68. Chavey C, Mari B, Monthouel MN, Bonnafous S, Anglard P, Van Obberghen E, Tartare-Deckert S. Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation. J Biol Chem 2003; 278: 11888-96.
69. Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2008; 2: 50-9.
70. Luo D, Renault VM, Rando TA. The regulation of Notch signaling in muscle stem cell activation and postnatal myogenesis. Semin Cell Dev Biol 2005; 16: 612-22.
71. Lai EC. Notch signaling: control of cell communication and cell fate. Development 2004; 131: 965-73.
72. Li Y, Foster W, Deasy BM, Chan Y, Prisk V, Tang Y, Cummins J, Huard J. Transforming growth factor-beta1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis. Am J Pathol 2004; 164: 1007-19.
73. Overall CM, Kleifeld O. Tumour microenvironment - opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat Rev Cancer 2006; 6: 227-39.