Loss of epidermal MMP-14 expression interferes with angiogenesis but not with re-epithelialization

European Journal of Cell Biology

Volumn 91, Issue 10, 2012, Pages 748-756

  Zigrino, Paola ^a   Ayachi, Ouissam ^a   Schild, Alexander ^a   Kaltenberg, Jennifer ^a   Zamek, Jan ^a   Nischt, Roswitha ^a   Koch, Manuel ^a   Mauch, Cornelia ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Angiogenesis; Collagen; MMP; Proteases; Wound healing

Indexed keywords

COLLAGEN; MATRIX METALLOPROTEINASE 14;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; DERMIS; EPIDERMIS; EPITHELIZATION; HOMEOSTASIS; KERATINOCYTE; LEUKOCYTE; MACROPHAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WOUND HEALING;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; COLLAGEN; ENDOSTATINS; EPIDERMIS; GENE EXPRESSION; KERATINOCYTES; LEUKOCYTES; MACROPHAGES; MATRIX METALLOPROTEINASE 14; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; NEUTROPHILS; RE-EPITHELIALIZATION;

MUS;

EID: 84866453248     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2012.05.003     Document Type: Article

References (40)

1. Ansell D.M., Kloepper J.E., Thomason H.A., Paus R., Hardman M.J. Exploring the " hair growth-wound healing connection" : anagen phase promotes wound re-epithelialization. J. Invest. Dermatol. 2011, 131:518-528.
2. Aplin A.C., Zhu W.H., Fogel E., Nicosia R.F. Vascular regression and survival are differentially regulated by MT1-MMP and TIMPs in the aortic ring model of angiogenesis. Am. J. Physiol. Cell Physiol. 2009, 297:C471-C480.
3. Arroyo A.G., Iruela-Arispe M.L. Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc. Res. 2010, 86:226-235.
4. Benjamin L.E. The controls of microvascular survival. Cancer Metast. Rev. 2000, 19:75-81.
5. Bloch W., Huggel K., Sasaki T., Grose R., Bugnon P., Addicks K., Timpl R., Werner S. The angiogenesis inhibitor endostatin impairs blood vessel maturation during wound healing. FASEB J. 2000, 14:2373-2376.
6. Brown L.F., Yeo K.T., Berse B., Yeo T.K., Senger D.R., Dvorak H.F., van de Water L. Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. J. Exp. Med. 1992, 176:1375-1379.
7. Chang J.H., Javier J.A., Chang G.Y., Oliveira H.B., Azar D.T. Functional characterization of neostatins, the MMP-derived, enzymatic cleavage products of type XVIII collagen. FEBS Lett. 2005, 579:3601-3606.
8. Chau Y.P., Lin S.Y., Chen J.H., Tai M.H. Endostatin induces autophagic cell death in EAhy926 human endothelial cells. Histol. Histopathol. 2003, 18:715-726.
9. Chun T.H., Sabeh F., Ota I., Murphy H., McDonagh K.T., Holmbeck K., Birkedal-Hansen H., Allen E.D., Weiss S.J. MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J. Cell Biol. 2004, 167:757-767.
10. Clark R.A. Biology of dermal wound repair. Dermatol. Clin. 1993, 11:647-666.
11. Genis L., Galvez B.G., Gonzalo P., Arroyo A.G. MT1-MMP: universal or particular player in angiogenesis?. Cancer Metast. Rev. 2006, 25:77-86.
12. Gill S.E., Parks W.C. Metalloproteinases and their inhibitors: regulators of wound healing. Int. J. Biochem. Cell Biol. 2008, 40:1334-1347.
13. Hafner M., Wenk J., Nenci A., Pasparakis M., Scharffetter-Kochanek K., Smyth N., Peters T., Kess D., Holtkotter O., Shephard P., Kudlow J.E., Smola H., Haase I., Schippers A., Krieg T., Muller W. Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis 2004, 38:176-181.
14. Holmbeck K., Bianco P., Caterina J., Yamada S., Kromer M., Kuznetsov S.A., Mankani M., Robey P.G., Poole A.R., Pidoux I., Ward J.M., Birkedal-Hansen H. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999, 99:81-92.
15. Holmbeck K., Bianco P., Yamada S., Birkedal-Hansen H. MT1-MMP: a tethered collagenase. J. Cell. Physiol. 2004, 200:11-19.
16. Hotary K.B., Yana I., Sabeh F., Li X.Y., Holmbeck K., Birkedal-Hansen H., Allen E.D., Hiraoka N., Weiss S.J. Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes. J. Exp. Med. 2002, 195:295-308.
17. Im E., Kazlauskas A. New insights regarding vessel regression. Cell Cycle 2006, 5:2057-2059.
18. Itoh Y., Seiki M. MT1-MMP: a potent modifier of pericellular microenvironment. J. Cell. Physiol. 2006, 206:1-8.
19. Kim M.H., Kitson R.P., Albertsson P., Nannmark U., Basse P.H., Kuppen P.J., Hokland M.E., Goldfarb R.H. Secreted and membrane-associated matrix metalloproteinases of IL-2-activated NK cells and their inhibitors. J. Immunol. 2000, 164:5883-5889.
20. Koch M., Murrell J.R., Hunter D.D., Olson P.F., Jin W., Keene D.R., Brunken W.J., Burgeson R.E. A novel member of the netrin family, beta-netrin, shares homology with the beta chain of laminin: identification, expression, and functional characterization. J. Cell Biol. 2000, 151:221-234.
21. Lederle W., Hartenstein B., Meides A., Kunzelmann H., Werb Z., Angel P., Mueller M.M. MMP13 as a stromal mediator in controlling persistent angiogenesis in skin carcinoma. Carcinogenesis 2010, 31:1175-1184.
22. Lehti K., Lohi J., Juntunen M.M., Pei D., Keski-Oja J. Oligomerization through hemopexin and cytoplasmic domains regulates the activity and turnover of membrane-type 1 matrix metalloproteinase. J. Biol. Chem. 2002, 277:8440-8448.
23. Lin H.C., Chang J.H., Jain S., Gabison E.E., Kure T., Kato T., Fukai N., Azar D.T. Matrilysin cleavage of corneal collagen type XVIII NC1 domain and generation of a 28-kDa fragment. Invest. Ophthalmol. Vis. Sci. 2001, 42:2517-2524.
24. Martin P. Wound healing-aiming for perfect skin regeneration. Science 1997, 276:75-81.
25. Mauch C., Zamek J., Abety A.N., Grimberg G., Fox J.W., Zigrino P. Accelerated wound repair in ADAM-9 knockout animals. J. Invest. Dermatol. 2010, 130:2120-2130.
26. Milner Y., Sudnik J., Filippi M., Kizoulis M., Kashgarian M., Stenn K. Exogen, shedding phase of the hair growth cycle: characterization of a mouse model. J. Invest. Dermatol. 2002, 119:639-644.
27. Mirastschijski U., Zhou Z., Rollman O., Tryggvason K., Agren M.S. Wound healing in membrane-type-1 matrix metalloproteinase-deficient mice. J. Invest. Dermatol. 2004, 123:600-602.
28. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 2006, 69:562-573.
29. Nagavarapu U., Relloma K., Herron G.S. Membrane type 1 matrix metalloproteinase regulates cellular invasiveness and survival in cutaneous epidermal cells. J. Invest. Dermatol. 2002, 118:573-581.
30. Nguyen T.M., Subramanian I.V., Xiao X., Ghosh G., Nguyen P., Kelekar A., Ramakrishnan S. Endostatin induces autophagy in endothelial cells by modulating Beclin 1 and beta-catenin levels. J. Cell. Mol. Med. 2009, 13:3687-3698.
31. O'Reilly M.S., Wiederschain D., Stetler-Stevenson W.G., Folkman J., Moses M.A. Regulation of angiostatin production by matrix metalloproteinase-2 in a model of concomitant resistance. J. Biol. Chem. 1999, 274:29568-29571.
32. Okada A., Tomasetto C., Lutz Y., Bellocq J.P., Rio M.C., Basset P. Expression of matrix metalloproteinases during rat skin wound healing: evidence that membrane type-1 matrix metalloproteinase is a stromal activator of pro-gelatinase A. J. Cell Biol. 1997, 137:67-77.
33. Rodriguez C.I., Buchholz F., Galloway J., Sequerra R., Kasper J., Ayala R., Stewart A.F., Dymecki S.M. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 2000, 25:139-140.
34. Sabeh F., Li X.Y., Saunders T.L., Rowe R.G., Weiss S.J. Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J. Biol. Chem. 2009, 284:23001-23011.
35. Sasaki T., Fukai N., Mann K., Gohring W., Olsen B.R., Timpl R. Structure, function and tissue forms of the C-terminal globular domain of collagen XVIII containing the angiogenesis inhibitor endostatin. EMBO J. 1998, 17:4249-4256.
36. Seppinen L., Sormunen R., Soini Y., Elamaa H., Heljasvaara R., Pihlajaniemi T. Lack of collagen XVIII accelerates cutaneous wound healing, while overexpression of its endostatin domain leads to delayed healing. Matrix Biol. 2008, 27:535-546.
37. Shichiri M., Hirata Y. Antiangiogenesis signals by endostatin. FASEB J. 2001, 15:1044-1053.
38. Wagner W., Wehrmann M. Differential cytokine activity and morphology during wound healing in the neonatal and adult rat skin. J. Cell. Mol. Med. 2007, 11:1342-1351.
39. Wu N., Opalenik S., Liu J., Jansen E.D., Giro M.G., Davidson J.M. Real-time visualization of MMP-13 promoter activity in transgenic mice. Matrix Biol. 2002, 21:149-161.
40. Zhou Z., Apte S.S., Soininen R., Cao R., Baaklini G.Y., Rauser R.W., Wang J., Cao Y., Tryggvason K. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. USA 2000, 97:4052-4057.