Scarless skin wound healing in FOXN1 deficient (nude) mice is associated with distinctive matrix metalloproteinase expression

Matrix Biology

Volumn 30, Issue 4, 2011, Pages 290-300

  Gawronska Kozak, Barbara ^a,b  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b INSTITUTE OF ANIMAL REPRODUCTION AND FOOD RESEARCH   (Poland)

Author keywords

FOXN1; Matrix metalloproteinases; Nude mice; Regeneration; Wound healing

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGENASE 3; GELATINASE A; GELATINASE B; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MESSENGER RNA; NEUTROPHIL COLLAGENASE; STROMELYSIN; STROMELYSIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EPIDERMIS; FEMALE; GRANULATION TISSUE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCARLESS SKIN WOUND HEALING; SKIN FIBROBLAST; SKIN INCISION; SKIN INJURY; TISSUE REGENERATION; UPREGULATION; WESTERN BLOTTING; WILD TYPE; WOUND HEALING; ZYMOGRAPHY;

ANIMALS; CELLS, CULTURED; CICATRIX; COLLAGEN; ENZYME ASSAYS; FEMALE; FIBROBLASTS; FORKHEAD TRANSCRIPTION FACTORS; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, NUDE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKIN; TISSUE INHIBITOR OF METALLOPROTEINASES; TRANSCRIPTION, GENETIC; UP-REGULATION;

MAMMALIA; MUS; MUS MUSCULUS;

EID: 79958161535     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2011.04.004     Document Type: Article

References (49)

1. Ashcroft G.S., Horan M.A., Ferguson M.W. Aging is associated with reduced deposition of specific extracellular matrix components, an upregulation of angiogenesis, and an altered inflammatory response in a murine incisional wound healing model. J. Invest. Dermatol. 1997, 108:430-437.
2. Ashcroft G.S., Horan M.A., Herrick S.E., Tarnuzzer R.W., Schultz G.S., Ferguson M.W. Age-related differences in the temporal and spatial regulation of matrix metalloproteinases (MMPs) in normal skin and acute cutaneous wounds of healthy humans. Cell Tissue Res. 1997, 290:581-591.
3. Ashcroft G.S., Mills S.J., Ashworth J.J. Ageing and wound healing. Biogerontology 2002, 3:337-345.
4. Barrick B., Campbell E.J., Owen C.A. Leukocyte proteinases in wound healing: roles in physiologic and pathologic processes. Wound Repair Regen. 1999, 7:410-422.
5. Bryant S.V., Endo T., Gardiner D.M. Vertebrate limb regeneration and the origin of limb stem cells. Int. J. Dev. Biol. 2002, 46:887-896.
6. Clark R. The Molecular and Cellular Biology of Wound Repair 1996, Plenum Press, New York.
7. Clark L.D., Clark R.K., Heber-Katz E. A new murine model for mammalian wound repair and regeneration. Clin. Immunol. Immunopathol. 1998, 88:35-45.
8. Colwell A.S., Longaker M.T., Lorenz H.P. Mammalian fetal organ regeneration. Adv. Biochem. Eng. Biotechnol. 2005, 93:83-100.
9. Dang C., Ting K., Soo C., Longaker M.T., Lorenz H.P. Fetal wound healing current perspectives. Clin. Plast. Surg. 2003, 30:13-23.
10. Dang C.M., Beanes S.R., Lee H., Zhang X., Soo C., Ting K. Scarless fetal wounds are associated with an increased matrix metalloproteinase-to-tissue-derived inhibitor of metalloproteinase ratio. Plast. Reconstr. Surg. 2003, 111:2273-2285.
11. Ferguson M.W., O'Kane S. Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. Philos Trans R Soc Lond B Biol Sci. 2004, 359:839-850.
12. Fujiwara M., Muragaki Y., Ooshima A. Keloid-derived fibroblasts show increased secretion of factors involved in collagen turnover and depend on matrix metalloproteinase for migration. Br. J. Dermatol. 2005, 153:295-300.
13. Gawronska-Kozak B. Regeneration in the ears of immunodeficient mice: identification and lineage analysis of mesenchymal stem cells. Tissue Eng. 2004, 10:1251-1265.
14. Gawronska-Kozak B., Bogacki M., Rim J.S., Monroe W.T., Manuel J.A. Scarless skin repair in immunodeficient mice. Wound Repair Regen. 2006, 14:265-276.
15. Gill S.E., Parks W.C. Metalloproteinases and their inhibitors: regulators of wound healing. Int. J. Biochem. Cell Biol. 2008, 40:1334-1347.
16. Gurtner G.C., Werner S., Barrandon Y., Longaker M.T. Wound repair and regeneration. Nature 2008, 453:314-321.
17. Han Y.P., Tuan T.L., Hughes M., Wu H., Garner W.L. Transforming growth factor-beta - and tumor necrosis factor-alpha-mediated induction and proteolytic activation of MMP-9 in human skin. J. Biol. Chem. 2001, 276:22341-22350.
18. Han M., Yang X., Lee J., Allan C.H., Muneoka K. Development and regeneration of the neonatal digit tip in mice. Dev. Biol. 2008, 315:125-135.
19. Hartenstein B., Dittrich B.T., Stickens D., Heyer B., Vu T.H., Teurich S., Schorpp-Kistner M., Werb Z., Angel P. Epidermal development and wound healing in matrix metalloproteinase 13-deficient mice. J. Invest. Dermatol. 2006, 126:486-496.
20. Hattori N., Mochizuki S., Kishi K., Nakajima T., Takaishi H., D'Armiento J., Okada Y. MMP-13 plays a role in keratinocyte migration, angiogenesis, and contraction in mouse skin wound healing. Am. J. Pathol. 2009, 175:533-546.
21. Kobayashi T., Hattori S., Shinkai H. Matrix metalloproteinases-2 and -9 are secreted from human fibroblasts. Acta Derm. Venereol. 2003, 83:105-107.
22. Kyriakides T.R., Wulsin D., Skokos E.A., Fleckman P., Pirrone A., Shipley J.M., Senior R.M., Bornstein P. Mice that lack matrix metalloproteinase-9 display delayed wound healing associated with delayed reepithelization and disordered collagen fibrillogenesis. Matrix Biol. 2009, 28:65-73.
23. Legrand C., Gilles C., Zahm J.M., Polette M., Buisson A.C., Kaplan H., Birembaut P., Tournier J.M. Airway epithelial cell migration dynamics. MMP-9 role in cell-extracellular matrix remodeling. J. Cell Biol. 1999, 146:517-529.
24. Longaker M.T., Whitby D.J., Adzick N.S., Crombleholme T.M., Langer J.C., Duncan B.W., Bradley S.M., Stern R., Ferguson M.W., Harrison M.R. Studies in fetal wound healing, VI. Second and early third trimester fetal wounds demonstrate rapid collagen deposition without scar formation. J. Pediatr. Surg. 1990, 25:63-68. discussion 68-9.
25. Lorenz H.P., Lin R.Y., Longaker M.T., Whitby D.J., Adzick N.S. The fetal fibroblast: the effector cell of scarless fetal skin repair. Plast. Reconstr. Surg. 1995, 96:1251-1259. discussion 1260-1.
26. Madlener M., Parks W.C., Werner S. Matrix metalloproteinases (MMPs) and their physiological inhibitors (TIMPs) are differentially expressed during excisional skin wound repair. Exp. Cell Res. 1998, 242:201-210.
27. Manuel, J. A., Gawronska-Kozak, B., 2006. Matrix metalloproteinase 9 (MMP-9) is upregulated during scarless wound healing in athymic nude mice. Matrix Biol.
28. Martin P. Wound healing-aiming for perfect skin regeneration. Science. 1997, 276:75-81.
29. Mohan R., Chintala S.K., Jung J.C., Villar W.V., McCabe F., Russo L.A., Lee Y., McCarthy B.E., Wollenberg K.R., Jester J.V., Wang M., Welgus H.G., Shipley J.M., Senior R.M., Fini M.E. Matrix metalloproteinase gelatinase B (MMP-9) coordinates and effects epithelial regeneration. J. Biol. Chem. 2002, 277:2065-2072.
30. Occleston N.L., Laverty H.G., O'Kane S., Ferguson M.W. Prevention and reduction of scarring in the skin by transforming growth factor beta 3 (TGFbeta3): from laboratory discovery to clinical pharmaceutical. J. Biomater. Sci. Polym. Ed. 2008, 19:1047-1063.
31. Occleston N.L., O'Kane S., Goldspink N., Ferguson M.W. New therapeutics for the prevention and reduction of scarring. Drug Discov. Today 2008, 13:973-981.
32. Owen C.A., Hu Z., Barrick B., Shapiro S.D. Inducible expression of tissue inhibitor of metalloproteinases-resistant matrix metalloproteinase-9 on the cell surface of neutrophils. Am. J. Respir. Cell Mol. Biol. 2003, 29:283-294.
33. Page-McCaw A., Ewald A.J., Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 2007, 8:221-233.
34. Park I.S., Kim W.S. Modulation of gelatinase activity correlates with the dedifferentiation profile of regenerating salamander limbs. Mol. Cells 1999, 9:119-126.
35. Parks W.C. Matrix metalloproteinases in repair. Wound Repair Regen. 1999, 7:423-432.
36. Peled Z.M., Phelps E.D., Updike D.L., Chang J., Krummel T.M., Howard E.W., Longaker M.T. Matrix metalloproteinases and the ontogeny of scarless repair: the other side of the wound healing balance. Plast. Reconstr. Surg. 2002, 110:801-811.
37. Ravanti L., Hakkinen L., Larjava H., Saarialho-Kere U., Foschi M., Han J., Kahari V.M. Transforming growth factor-beta induces collagenase-3 expression by human gingival fibroblasts via p38 mitogen-activated protein kinase. J. Biol. Chem. 1999, 274:37292-37300.
38. Ravanti L., Toriseva M., Penttinen R., Crombleholme T., Foschi M., Han J., Kahari V.M. Expression of human collagenase-3 (MMP-13) by fetal skin fibroblasts is induced by transforming growth factor beta via p38 mitogen-activated protein kinase. FASEB J. 2001, 15:1098-1100.
39. Redd M.J., Cooper L., Wood W., Stramer B., Martin P. Wound healing and inflammation: embryos reveal the way to perfect repair. Philos Trans R Soc Lond B Biol Sci. 2004, 359:777-784.
40. Soo C., Shaw W.W., Zhang X., Longaker M.T., Howard E.W., Ting K. Differential expression of matrix metalloproteinases and their tissue-derived inhibitors in cutaneous wound repair. Plast. Reconstr. Surg. 2000, 105:638-647.
41. Steffensen B., Hakkinen L., Larjava H. Proteolytic events of wound-healing - coordinated interactions among matrix metalloproteinases (MMPs), integrins, and extracellular matrix molecules. Crit. Rev. Oral Biol. Med. 2001, 12:373-398.
42. Szpaderska A.M., Zuckerman J.D., DiPietro L.A. Differential injury responses in oral mucosal and cutaneous wounds. J. Dent. Res. 2003, 82:621-626.
43. Toriseva M., Kahari V.M. Proteinases in cutaneous wound healing. Cell. Mol. Life Sci. 2009, 66:203-224.
44. Toriseva M.J., Ala-aho R., Karvinen J., Baker A.H., Marjomaki V.S., Heino J., Kahari V.M. Collagenase-3 (MMP-13) enhances remodeling of three-dimensional collagen and promotes survival of human skin fibroblasts. J. Invest. Dermatol. 2007, 127:49-59.
45. Vaalamo M., Leivo T., Saarialho-Kere U. Differential expression of tissue inhibitors of metalloproteinases (TIMP-1, -2, -3, and -4) in normal and aberrant wound healing. Hum. Pathol. 1999, 30:795-802.
46. Vinarsky V., Atkinson D.L., Stevenson T.J., Keating M.T., Odelberg S.J. Normal newt limb regeneration requires matrix metalloproteinase function. Dev. Biol. 2005, 279:86-98.
47. Wu N., Jansen E.D., Davidson J.M. Comparison of mouse matrix metalloproteinase 13 expression in free-electron laser and scalpel incisions during wound healing. J. Invest. Dermatol. 2003, 121:926-932.
48. Wysocki A.B., Staiano-Coico L., Grinnell F. Wound fluid from chronic leg ulcers contains elevated levels of metalloproteinases MMP-2 and MMP-9. J. Invest. Dermatol. 1993, 101:64-68.
49. Yang E.V., Gardiner D.M., Carlson M.R., Nugas C.A., Bryant S.V. Expression of Mmp-9 and related matrix metalloproteinase genes during axolotl limb regeneration. Dev. Dyn. 1999, 216:2-9.