Matrix metalloproteinase activity correlates with blastema formation in the regenerating MRL mouse ear hole model

Developmental Dynamics

Volumn 226, Issue 2, 2003, Pages 377-387

  Gourevitch, Dmitri ^a   Clark, Lise ^a   Chen, Pan ^a   Seitz, Alexander ^a   Samulewicz, Stefan J ^a   Heber Katz, Ellen ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

Collagen type I and IV; MMPs; MRL mice; Regeneration; TIMPs

Indexed keywords

GELATIN; GELATINASE A; GELATINASE B; MATRIX METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BLASTEMA; CARTILAGE; ENZYME ACTIVITY; HAIR FOLLICLE; INFLAMMATION; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SCAR FORMATION; TISSUE REGENERATION; WOUND HEALING; ZYMOGRAPHY;

ANIMALS; EAR; ENDOPEPTIDASES; EXTRACELLULAR MATRIX; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; REGENERATION; RNA; SPECIES SPECIFICITY; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TISSUE INHIBITOR OF METALLOPROTEINASE-3; WOUNDS, PENETRATING;

MAMMALIA;

EID: 0037308876     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.10243     Document Type: Article

References (72)

1. Alleva DG, Kaser SB, Beller DI. 1997. Aberrant cytokine expression and autocrine regulation characterize macrophages from young MRL+/+ and NZB/W F1 lupus-prone mice. J Immunol 159:5610-5619.
2. Armstrong JR, Ferguson MWJ. 1995. Ontogeny of the skin and the transition from scar-free to scarring phenotype during wound healing in the pouch of a young marsupial Monodelphis domestica. Dev Biol 169:242-360.
3. Baker EA, Leaper DJ. 2000. Proteinases, their inhibitors, and cytokine profiles in acute wound fluid. Wound Repair Regen 8:392-398.
4. Blankenhorn EP, Troutman S, Desquenne Clark L, Zhang X-M, Heber-Katz E. 2003. Sexually dimorphic genes regulate healing and regeneration in the MRL/MpJ mouse. Mammalian Genome (in press).
5. Boone TC, Johnson MJ, DeClerk YA, Langeley KE. 1990. cDNA cloning and expression of a metalloproteinase inhibitor related to tissue inhibitor of metalloproteinase. Proc Natl Acad Sci U S A 87:2800-2804.
6. Borgens RB. 1982. Mice regrow the tips of the foretoes. Science 217:747-750.
7. Brockes JP. 1997. Amphibian limb regeneration: rebuilding a complex structure. Science 276:81-87.
8. Brooks PC, Stromblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler-Stevenson WG, Quigley JP, Cheresh DA. 1996. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85:683-693.
9. Butler GS, Butler MJ, Atkinson SJ, Will H, Tamura T, van Westrum SS, Crabbe T, Clements J, d'Ortho MP, Murphy G. 1998. The TIMP2 membrane type 1 metalloproteinase "receptor" regulates the concentration and efficient activation of pro-gelatinase A. A kinetic study. J Biol Chem 273:871-880.
10. Chernoff EAG, O'Hara CM, Bauerle B, Bowling M. 2000. Matrix metalloproteinase production in regenerating axolotl spinal cord. Wound Repair Regen 8:282-291.
11. Chin JR, Werb Z. 1997. Matrix metalloproteinases regulate morphogenesis, migration, and remodeling of epithelium, tongue skeletal muscle and cartilage in the mandibular arch. Development 124:1519-1530.
12. Christensen RN, Weinstein M, Tassava RA. 2002. Expression of fibroblast growth factors 4, 8, and 10 in limbs, flanks, and blastemas of Ambystoma. Dev Dyn 223:193-203.
13. Clark RAF. 1996. Wound repair: overview and general consideration. In: Clark R, editor. The molecular and cellular biology of wound repair. New York: Plenum Press. p 3-35.
14. Clark LD, Clark RK, Heber-Katz, E. 1998. A new murine model for mammalian wound repair and regeneration. Clin Immunol Immunopathol 88:35-45.
15. Damjanovski S, Puzianowska-Kuznicka M, Ishuzuya-Oka A, Shi YB. 2000. Differential regulation of three thyroid hormone-responsive matrix metalloproteinase genes implicates distinct functions during frog embryogenesis. FASEB J 14:503-510.
16. Douglas BS. 1972. Conservative management of guillotine amputations of the fingers of children. Aust Paediatr J 8:86-90.
17. Dresden MH, Gross J. 1970. The collagenolytic enzyme of the regenerating limb of the Newt triturus viridescens. Dev Biol 22:129-137.
18. Fini ME, Girard MT, Matsubara M, Bartlett JD. 1995. Unique regulation of the matrix metalloproteinase, gelatinase B. Invest Opthalmol Vis Sci 36:622-633.
19. Globus M, Vethamany-Globus S, Lee YCI, 1980. Effect of apical epidermal cap on mitotic cycle and cartilage differentiation in regeneration blastemata in the newt. Notophthalmus viridescens. Dev Biol 75:358-372.
20. Goss RJ. 1970. Problems of antlerogenesis. Clin Orthop 69:227-238.
21. Goss RJ, Grimes LN. 1975. Epidermal downgrowths in regenerating rabbit ear holes. J Morphol 146:533-542.
22. Grillo HC, Lapiere CM, Dresden MH, Gross J. 1968. Collagenolytic activity in regenerating forelimbs of the adult newt. Dev Biol 17:571-583.
23. Gross J. 1966. How do tadpoles lose their tails. J Invest Dermatol 47:274-277.
24. Gross J. 1996. Getting to mammalian wound repair and amphibian limb regeneration: a mechanistic link in the early events. Wound Repair Regen 4:190-202.
25. Hamaguchi M, Yamagata S, Thant AA, Xiao H, Iwata H, Mazaki T, Hanafusa H. 1995. Augmentation of metalloproteinase (gelatinase) activity secreted from Rous sarcoma virus-infected cells correlates with transforming activity of src. Oncogene 10:1037-1043.
26. Hakkinen L, Uitto V-J, Larjava H. 2000. Cell biology of gingival wound healing. Periodontology 24:127-152.
27. Hartwell DW, Fenton MJ, Levine JS, Beller DI. 1995. Aberrant cytokine regulation in macrophages from young autoimmune-prone mice: evidence that the intrinsic defect in MRL macrophage IL-1 expression is transcriptionally controlled. Mol Immunol 32:743-751.
28. Hay ED, 1984. Cell-matrix interaction in the embryo: cell shape, cell surface, cell skeletons, and their role in differentiation. In: Trelstad RL, editor. The role of extracellular matrix in development. New York: Alan Liss. p 1-31.
29. Hayakawa T, Yamashita K, Tanzawa K, Uchujima E, Iwata K. 1992. Growth-promoting activity of tissue inhibitor of metalloproteinase-1 (TIMP-1) for a wide range of cells. A possible new growth factor in serum. FEBS Lett 298:29-32.
30. Heber-Katz E. 1999. The regenerating mouse ear. Semin Cell Dev Biol 10:415-420.
31. Hopkinson-Woolley J, Highes D, Gordon S, Martin P. 1994 Macrophage recruitment during limb development and wound healing in the embryonic and fetal mouse. J Cell Sci 107:1159-1167.
32. Howard EW, Bullen EC, Banda MJ. 1991. Regulation of the autoactivation of human 72 kDa progelatinase by tissue inhibitor of metalloproteinases-2. J Biol Chem 266:13064-13069.
33. Illingworth CM. 1974. Trapped fingers and amputated finger tips in children. J Pediatr Surg 9:853-858.
34. Ito A, Sato T, Mori Y. 1990. Tumor necrosis factor bifunctionally regulated matrix metalloproteinases and tissue inhibitor of metalloproteinases (TIMP) production by human fibroblasts. FEBS Lett 269:93-95.
35. Itoh T, Matsuda H, Tanioka M, Kuwabara K, Itohara S, Suzuki R. 2002. The role of matrix metalloproteinase-2 and matrix metalloproteinase-9 in antibody-induced arthritis. J Immunol 169:2643-2647.
36. Jung JC, Leco KJ, Edwards DR, Fini ME. 2002. Matrix metalloproteinases mediate the dismantling of mesenchymal structures in the tadpole tail during thyroid hormone-induced tail resorption. Dev Dyn 223:402-413.
37. Ladwig GP, Robson MC, Liu R, Kuhn MA, Muir DF, Schultz GS, 2002. Ratios of activated matrix metalloproteinase-9 to tissue inhibitor of matrix metalloproteinase-1 in wound fluids are inversely correlated with healing of pressure ulcers. Wound Repair Regen 10:26-37.
38. Leferovich JM, Bedelbaeva K, Samulewicz S, Xhang X-M, Zwas DR, Lankford EB, Heber-Katz E. 2001. Heart regeneration in adult MRL mice. Proc Natl Acad Sci U S A 98:9830-9835.
39. Mackay AR, Hartzler JL, Pelina MD, Thorgeirsson UP. 1990. Studies on the ability of 65-kDa and 92-kDa tumor cell gelatinases to degrade type IV collagen, J Biol Chem 265:21929-21934.
40. Masinde GL, Li X, Gu W, Davidson H, Mohan S, Baylink DJ. 2001. Identification of wound healing/regeneration quantitative trait loci (QTL) at multiple time points that explain seventy percent of variance in (MRL/MpJ and SJL/J) mice F2 population. Genome Res 11:2027-2033.
41. Matrisan LM. 1992. The matrix-degrading metalloproteinases. Bioassays 14:455-463.
42. Matsubara M, Girard MT, Kublin CL, Cintron C, Fini ME. 1991. Differential roles for two gelatinolytic enzymes of the matrix metalloproteinase family in the remodelling cornea. Dev Biol 147:425-439.
43. McBrearty BA, Desquenne-Clark L, Zhang X-M, Blankenhorn EP, Heber-Katz E. 1998. Genetic analysis of a mammalian wound healing trait. Proc Natl Acad Sci U S A 95:11792-11797.
44. Miyamori H, Takino T, Kobayashi Y, Tokai H, Itoh Y, Seiki M, Sato H. 2001. Claudin promotes activation of pro-matrix metalloproteinase-2 mediated by membrane-type matrix metalloproteinases. J Biol Chem 276:28204-28211.
45. Miyazaki K, Uchiyawa K, Imokawa Y, Yoshizato K. 1996. Cloning and characterization of cDNAs for matrix metalloproteinases of regenerating newt limbs. Proc Natl Acad Sci U S A 93:6819-6824.
46. Murphy G, Gavrilovic J. 1999. Proteolysis and cell migration: creating a path? Curr Opin Cell Biol 11:614-621.
47. Murphy G, Willenbrock F, Crabbe T, O'Shea M, Ward R, Atkinson S, O'Connell J, Docherty A, 1994. Regulation of matrix metalloproteinase activity. Ann N Y Acad Sci 732:31-41.
48. Neufield DA. 1989. Epidermis, basement membrane, and connective-tissue healing after amputation of mouse digits: implications for mammalian appendage regeneration. Anat Rec 223:425-432.
49. Oofusa K, Yoshizato K. 1991. Biochemical and immunological characterization of collagenase in tissues of metamorphosing bullfrog tadpoles. Dev Growth Differ 33:329-339.
50. Okada A, Tomasetto C, Lutz Y, Belloccq JP, Rio MC, Bassett P. 1997. Expression of matrix metalloproteinases during rat skin wound healing: evidence that membrane type-1 matrix metalloproteinase is a stromal activator of progelatinase A. J Cell Biol 137:67-78.
51. Parks WC. 1999. Matrix metalloproteinases in repair. Wound Repair Regen 7:423-432.
52. Parks WC, Mecham RP. 1998. Matrix metalloproteinases. San Diego: Academic Press.
53. Repesh LA, Oberpriller JC. 1978. Scanning electron microscopy of epidermal cell migration in wound healing during limb regeneration in the adult newt, Notophthalmus viridescens. Am J Anat 151:539-555.
54. Repesh LA, Oberpriller JC. 1980. Ultrastructural studies on migrating epidermal cells during the wound healing stage of regeneration in the adult newt, Notophthalmus viridescens. Am J Anat 159:187-208.
55. Samulewicz SJ, Clark L, Seitz A, Heber-Katz E. 2002. Expression of pref-1, a delta-like protein, in healing mouse ears. Wound Repair Regen 10:215-221.
56. Sawada T, Oofusa K, Yoshizato K. 1999. Characterization of a collagenolytic enzyme released from wounded planarians Dugesia japonica. Wound Repair Regen 7:458-466.
57. Schwartz JD, Monea S, Marcus SG, Patel S, Eng K, Galloway AC, Mignati P, Shamamian P. 1998. Soluble factors released from neutrophils activates endothelial cell matrix metalloproteinase-2. J Surg Res 76:79-85.
58. Seitz A, Aglow E, Heber-Katz E. 2002. Recovery from spinal cord injury: a new transection model in the C57B1/6 mouse. J Neurosci Res 67:337-345.
59. Steffensen B, Bigg HF, Overall CM. 1998. The involvement of the fibronectin type II-like modules of human gelatinase A in cell surface localization and activation. J Biol Chem 273:20622-20628.
60. Steffensen B, Hakkinen L, Larjava H. 2001. Proteolytic events of wound-healing-coordinated interactions among matrix metalloproteinases (MMPs), integrins, and extracellular matrix molecules. Crit Rev Oral Biol Med 12:373-398.
61. Stocum DL. 1995. Wound repair, regeneration and artificial tissue. Austin: R.G. Landes Co.
62. Stocum DL. 1996. Tissue restoration: approaches and prospects. Wound Repair Regen 4:3-15.
63. Stocum DL, Crawford K. 1987. Use of retinoids to analyze the cellular basis of positional memory in regenerating amphibian limbs. Biochem Cell Biol 65:750-761.
64. Stocum DL, Dearlove GE. 1972. Epidermal-mesodermal interaction during morphogenesis of the limb regeneration blastema in larval salamanders. J Exp Zool 181:49-62.
65. Sun X, Mariani FV, Martin GR. 2002. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418:501-508.
66. Suomela S, Kariniemi A-L, Snellman E, Saarialho-Kere U. 2001. Metalloelastase (MMP-12) and 92-kDa gelatinase (MMP-9) as well as their inhibitors, TIMP-1 and -3, are expressed in psoriatic lesions. Exp Dermatol 10:175-183.
67. Trengove NJ, Stacey MC, MacAuley S, Bennett N, Gibson J, Burslem F, Murphy G, Schultz G, 1999. Analysis of the acute and chronic wound environments: the role of proteases and their inhibitors. Wound Repair Regen 7:442-452.
68. Werb Z. 1997. ECM and cell surface proteolysis: regulating cellular ecology. Cell 91:439-442.
69. Wittwer CT, Ririe KM, Andrew RV, David DA, Gundry RA, Balis UJ. 1997. The LightCycler: a microvolume multisample fluorimeter with rapid temperature control. Biotechniques 22:176-181.
70. Woessner JF. 1991. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 5:2145-2154.
71. Yang EV, Bryant SV. 1994. Developmental regulation of a matrix metalloproteinase during regeneration of axolotl appendages. Dev Biol 166:696-703.
72. Yong VW, Forsyth PA, Bell R, Krekoski CA, Edwards DR. 1998. Matrix metalloproteinases and diseases of the CNS. Trends Neurosci 21:75-80.