MMP-13 regulates growth of wound granulation tissue and modulates gene expression signatures involved in inflammation, proteolysis, and cell viability

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Toriseva, Mervi ^a,b   Laato, Matti ^c   Carpén, Olli ^a   Ruohonen, Suvi T ^a   Savontaus, Eriika ^a   Inada, Masaki ^d   Krane, Stephen M ^e   Kähäri, Veli Matti ^a,b  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c TURKU UNIVERSITY HOSPITAL   (Finland)

^d TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGENASE 3;

ADAMTS4 GENE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL DIAMETER; CAPILLARY DENSITY; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GEL; GENE; GENE CONTROL; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC LINKAGE; GRANULATION TISSUE; GROWTH REGULATION; HISTOLOGY; INFLAMMATION; LEUKOCYTE MOTILITY; LL6 GENE; MICROVASCULATURE; MMP13 GENE; MMP2 GENE; MMP9 GENE; MOUSE; MYOFIBROBLAST; NONHUMAN; NPY GENE; NUCLEOTIDE SEQUENCE; PDGFD GENE; PROTEIN DEGRADATION; SKIN FIBROBLAST; TISSUE GROWTH; TISSUE SECTION; UPREGULATION; WILD TYPE; WOUND HEALING;

ADAM PROTEINS; ANIMALS; CELL DIFFERENTIATION; CELL SURVIVAL; COLLAGEN; DOWN-REGULATION; GELS; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GRANULATION TISSUE; INFLAMMATION; MALE; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 2; MICE; MYOFIBROBLASTS; NEOVASCULARIZATION, PATHOLOGIC; NEUROPEPTIDE Y; PROCOLLAGEN N-ENDOPEPTIDASE; PROTEOLYSIS; SKIN; TIME FACTORS; WOUND HEALING;

MUS;

EID: 84864683850     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042596     Document Type: Article

References (65)

1. Gurtner GC, Werner S, Barrandon Y, Longaker MT, (2008) Wound repair and regeneration. Nature 453: 314-321.
2. Shaw TJ, Martin P, (2009) Wound repair at a glance. J Cell Sci 122: 3209-3213.
3. Page-McCaw A, Ewald AJ, Werb Z, (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8: 221-233.
4. Toriseva M, Kähäri VM, (2009) Proteinases in cutaneous wound healing. Cell Mol Life Sci 66: 203-224.
5. Lee NV, Sato M, Annis DS, Loo JA, Wu L, et al. (2006) ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. Embo J 25: 5270-5283.
6. Mauch C, Zamek J, Abety AN, Grimberg G, Fox JW, et al. (2010) Accelerated wound repair in ADAM-9 knockout animals. J Invest Dermatol 130: 2120-2130.
7. Lund LR, Rømer J, Bugge TH, Nielsen BS, Frandsen TL, et al. (1999) Functional overlap between two classes of matrix-degrading proteases in wound healing. Embo J 18: 4645-4656.
8. Mirastschijski U, Schnabel R, Claes J, Schneider W, Ågren MS, et al. (2010) Matrix metalloproteinase inhibition delays wound healing and blocks the latent transforming growth factor-β1-promoted myofibroblast formation and function. Wound Repair Regen 18: 223-234.
9. Inoue M, Kratz G, Haegerstrand A, Ståhle-Bäckdahl M, (1995) Collagenase expression is rapidly induced in wound-edge keratinocytes after acute injury in human skin, persists during healing, and stops at re-epithelialization. J Invest Dermatol 104: 479-483.
10. Nwomeh BC, Liang HX, Cohen IK, Yager DR, (1999) MMP-8 is the predominant collagenase in healing wounds and nonhealing ulcers. J Surg Res 81: 189-195.
11. Mirastschijski U, Impola U, Jahkola T, Karlsmark T, S. Ågren MS, et al. (2002) Ectopic localization of matrix metalloproteinase-9 in chronic cutaneous wounds. Hum Pathol 33: 355-364.
12. Vaalamo M, Weckroth M, Puolakkainen P, Kere J, Saarinen P, et al. (1996) Patterns of matrix metalloproteinase and TIMP-1 expression in chronic and normally healing human cutaneous wounds. Br J Dermatol 135: 52-59.
13. Hieta N, Impola U, Lopez-Otin C, Saarialho-Kere U, Kähäri VM, (2003) Matrix metalloproteinase-19 expression in dermal wounds and by fibroblasts in culture. J Invest Dermatol 121: 997-1004.
14. Ahokas K, Skoog T, Suomela S, Jeskanen L, Impola U, et al. (2005) Matrilysin-2 (matrix metalloproteinase-26) is upregulated in keratinocytes during wound repair and early skin carcinogenesis. J Invest Dermatol 124: 849-856.
15. Lohi J, Wilson CL, Roby JD, Parks WC, (2001) Epilysin, a novel human matrix metalloproteinase (MMP-28) expressed in testis and keratinocytes and in response to injury. J Biol Chem 276: 10134-10144.
16. Pilcher BK, Dumin JA, Sudbeck BD, Krane SM, Welgus HG, et al. (1997) The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J Cell Biol 137: 1445-1457.
17. Pins GD, Collins-Pavao ME, Van De Water L, Yarmush ML, Morgan JR, (2000) Plasmin triggers rapid contraction and degradation of fibroblast-populated collagen lattices. J Invest Dermatol 114: 647-653.
18. Freije JM, Diéz-Itza I, Balbín M, Sánchez LM, Blasco R, et al. (1994) Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 269: 16766-16773.
19. Gack S, Vallon R, Schmidt J, Grigoriadis A, Tuckermann J, et al. (1995) Expression of interstitial collagenase during skeletal development of the mouse is restricted to osteoblast-like cells and hypertrophic chondrocytes. Cell Growth Differ 6: 759-767.
20. Johansson N, Saarialho-Kere U, Airola K, Herva R, Nissinen L, et al. (1997) Collagenase-3 (MMP-13) is expressed by hypertrophic chondrocytes, periosteal cells, and osteoblasts during human fetal bone development. Dev Dyn 208: 387-395.
21. Madlener M, Parks WC, Werner S, (1998) Matrix metalloproteinases (MMPs) and their physiological inhibitors (TIMPs) are differentially expressed during excisional skin wound repair. Exp Cell Res 242: 201-210.
22. Wu N, Jansen ED, Davidson JM, (2003) Comparison of mouse matrix metalloproteinase 13 expression in free-electron laser and scalpel incisions during wound healing. J Invest Dermatol 121: 926-932.
23. Vaalamo M, Mattila L, Johansson N, Kariniemi A-L, Karjalainen-Lindsberg M-L, et al. (1997) Distinct populations of stromal cells express collagenase-3 (MMP-13) and collagenase-1 (MMP-1) in chronic ulcers but not in normally healing wounds. J Invest Dermatol 109: 96-101.
24. Ravanti L, Häkkinen L, Larjava H, Saarialho-Kere U, Foschi M, et al. (1999) Transforming growth factor-β induces collagenase-3 expression by human gingival fibroblasts via p38 mitogen-activated protein kinase. J Biol Chem 274: 37292-37300.
25. Ravanti L, Toriseva M, Penttinen R, Crombleholme T, Foschi M, et al. (2001) Expression of human collagenase-3 (MMP-13) by fetal skin fibroblasts is induced by transforming growth factor β via p38 mitogen-activated protein kinase. FASEB J 15: 1098-1100.
26. Toriseva MJ, Ala-aho R, Karvinen J, Baker AH, Marjomäki VS, et al. (2007) Collagenase-3 (MMP-13) enhances remodeling of three-dimensional collagen and promotes survival of human skin fibroblasts. J Invest Dermatol 127: 49-59.
27. Hartenstein B, Dittrich BT, Stickens D, Heyer B, Vu TH, et al. (2006) Epidermal development and wound healing in matrix metalloproteinase 13-deficient mice. J Invest Dermatol 126: 486-496.
28. Hattori N, Mochizuki S, Kishi K, Nakajima T, Takaishi H, et al. (2009) MMP-13 plays a role in keratinocyte migration, angiogenesis, and contraction in mouse skin wound healing. Am J Pathol 175: 533-546.
29. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, et al. (2004) Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci U S A 101: 17192-17197.
30. Inkinen K, Turakainen H, Wolff H, Ravanti L, Kähäri VM, et al. (2000) Expression and activity of matrix metalloproteinase-2 and-9 in experimental granulation tissue. Apmis 108: 318-328.
31. Laato M, Kähäri VM, Niinikoski J, Vuorio E, (1987) Epidermal growth factor increases collagen production in granulation tissue by stimulation of fibroblast proliferation and not by activation of procollagen genes. Biochem J 247: 385-388.
32. Farshchian M, Kivisaari A, Ala-aho R, Riihilä P, Kallajoki M, et al. (2011) Serpin peptidase inhibitor clade A member 1 (SerpinA1): a novel biomarker for progression of cutaneous squamous cell carcinoma. Am J Pathol 179: 1110-9.
33. Stokes A, Joutsa J, Ala-aho R, Pitchers M, Pennington CJ, et al. (2010) Expression profiles and clinical correlations of degradome components in the tumor microenvironment of head and neck squamous cell carcinoma. Clin Cancer Res 16: 2022-2035.
34. Ala-aho R, Johansson N, Grénman R, Fusenig NE, López-Otín C, et al. (2000) Inhibition of collagenase-3 (MMP-13) expression in transformed human keratinocytes by interferon-γ is associated with activation of extracellular signal-regulated kinase-1,2 and STAT1. Oncogene 19: 248-257.
35. Hinz B, (2010) The myofibroblast: paradigm for a mechanically active cell. J Biomech 43: 146-155.
36. Grinnell F, Petroll WM, (2010) Cell motility and mechanics in three-dimensional collagen matrices. Annu Rev Cell Dev Biol 26: 335-361.
37. Nowacki S, Skowron M, Oberthuer A, Fagin A, Voth H, et al. (2008) Expression of the tumour suppressor gene CADM1 is associated with favourable outcome and inhibits cell survival in neuroblastoma. Oncogene 27: 3329-3338.
38. Xin H, Pramanik R, Choubey D, (2003) Retinoblastoma (Rb) protein upregulates expression of the Ifi202 gene encoding an interferon-inducible negative regulator of cell growth. Oncogene 22: 4775-4785.
39. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Müller-Newen G, et al. (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 374: 1-20.
40. Ekstrand AJ, Cao R, Bjorndahl M, Nystrom S, Jonsson-Rylander AC, et al. (2003) Deletion of neuropeptide Y (NPY) 2 receptor in mice results in blockage of NPY-induced angiogenesis and delayed wound healing. Proc Natl Acad Sci U S A 100: 6033-6038.
41. Koulu M, Movafagh S, Tuohimaa J, Jaakkola U, Kallio J, et al. (2004) Neuropeptide Y and Y2-receptor are involved in development of diabetic retinopathy and retinal neovascularization. Ann Med 36: 232-240.
42. Movafagh S, Hobson JP, Spiegel S, Kleinman HK, Zukowska Z, (2006) Neuropeptide Y induces migration, proliferation, and tube formation of endothelial cells bimodally via Y1, Y2, and Y5 receptors. Faseb J 20: 1924-1926.
43. Tommila M, Stark C, Jokilammi A, Peltonen V, Penttinen R, et al. (2011) Hemoglobin expression in rat experimental granulation tissue. J Mol Cell Biol 3: 190-196.
44. Uutela M, Wirzenius M, Paavonen K, Rajantie I, He Y, et al. (2004) PDGF-D induces macrophage recruitment, increased interstitial pressure, and blood vessel maturation during angiogenesis. Blood 104: 3198-3204.
45. Wang Z, Kong D, Banerjee S, Li Y, Adsay NV, et al. (2007) Down-regulation of platelet-derived growth factor-D inhibits cell growth and angiogenesis through inactivation of Notch-1 and nuclear factor-kappaB signaling. Cancer Res 67: 11377-11385.
46. Giangreco A, Jensen KB, Takai Y, Miyoshi J, Watt FM, (2009) Necl2 regulates epidermal adhesion and wound repair. Development 136: 3505-3514.
47. Ding S, Merkulova-Rainon T, Han ZC, Tobelem G, (2003) HGF receptor up-regulation contributes to the angiogenic phenotype of human endothelial cells and promotes angiogenesis in vitro. Blood 101: 4816-4822.
48. Grzeszkiewicz TM, Lindner V, Chen N, Lam SC, Lau LF, (2002) The angiogenic factor cysteine-rich 61 (CYR61, CCN1) supports vascular smooth muscle cell adhesion and stimulates chemotaxis through integrin α6β1 and cell surface heparan sulfate proteoglycans. Endocrinology 143: 1441-1450.
49. Mohan R, Sivak J, Ashton P, Russo LA, Pham BQ, et al. (2000) Curcuminoids inhibit the angiogenic response stimulated by fibroblast growth factor-2, including expression of matrix metalloproteinase gelatinase B. J Biol Chem 275: 10405-10412.
50. Veit G, Zwolanek D, Eckes B, Niland S, Käpylä J, et al. (2011) Collagen XXIII, novel ligand for integrin α2β1 in the epidermis. J Biol Chem 286: 27804-27813.
51. Kahn J, Mehraban F, Ingle G, Xin X, Bryant JE, et al. (2000) Gene expression profiling in an in vitro model of angiogenesis. Am J Pathol 156: 1887-1900.
52. Lederle W, Hartenstein B, Meides A, Kunzelmann H, Werb Z, et al. (2010) MMP13 as a stromal mediator in controlling persistent angiogenesis in skin carcinoma. Carcinogenesis 31: 1175-1184.
53. Zigrino P, Kuhn I, Bauerle T, Zamek J, Fox JW, et al. (2009) Stromal expression of MMP-13 is required for melanoma invasion and metastasis. J Invest Dermatol 129: 2686-2693.
54. Lecomte J, Louis K, Detry B, Blacher S, Lambert V, et al. (2011) Bone marrow-derived mesenchymal cells and MMP13 contribute to experimental choroidal neovascularization. Cell Mol Life Sci 68: 677-686.
55. Chen L, Arbieva ZH, Guo S, Marucha PT, Mustoe TA, et al. (2010) Positional differences in the wound transcriptome of skin and oral mucosa. BMC Genomics 11: 471.
56. Cole J, Tsou R, Wallace K, Gibran N, Isik F, (2001) Early gene expression profile of human skin to injury using high-density cDNA microarrays. Wound Repair Regen 9: 360-370.
57. Roy S, Khanna S, Rink C, Biswas S, Sen CK, (2008) Characterization of the acute temporal changes in excisional murine cutaneous wound inflammation by screening of the wound-edge transcriptome. Physiol Genomics 34: 162-184.
58. Ågren MS, (1994) Gelatinase activity during wound healing. Br J Dermatol 131: 634-640.
59. Kato T, Kure T, Chang JH, Gabison EE, Itoh T, et al. (2001) Diminished corneal angiogenesis in gelatinase A-deficient mice. FEBS Lett 508: 187-190.
60. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, et al. (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93: 411-422.
61. Endo H, Niioka M, Sugioka Y, Itoh J, Kameyama K, et al. (2011) Matrix metalloproteinase-13 promotes recovery from experimental liver cirrhosis in rats. Pathobiology 78: 239-252.
62. Jeon SH, Chae BC, Kim HA, Seo GY, Seo DW, et al. (2007) Mechanisms underlying TGF-β1-induced expression of VEGF and Flk-1 in mouse macrophages and their implications for angiogenesis. J Leukoc Biol 81: 557-566.
63. Salter RC, Arnaoutakis K, Michael DR, Singh NN, Ashlin TG, et al. (2011) The expression of a disintegrin and metalloproteinase with thrombospondin motifs 4 in human macrophages is inhibited by the anti-atherogenic cytokine transforming growth factor-β and requires Smads, p38 mitogen-activated protein kinase and c-Jun. Int J Biochem Cell Biol 43: 805-811.
64. Johansson N, Airola K, Grénman R, Kariniemi A-L, Saarialho-Kere U, et al. (1997) Expression of collagenase-3 (matrix metalloproteinase-13) in squamous cell carcinomas of the head and neck. Am J Pathol 151: 499-508.
65. Nikkola J, Vihinen P, Vlaykova T, Hahka-Kemppinen M, Kähäri VM, et al. (2002) High expression levels of collagenase-1 and stromelysin-1 correlate with shorter disease-free survival in human metastatic melanoma. Int J Cancer 97: 432-438.