HOXA3 induces cell migration in endothelial and epithelial cells promoting angiogenesis and wound repair

Journal of Cell Science

Volumn 118, Issue 12, 2005, Pages 2567-2577

  Mace, Kimberly A ^a   Hansen, Scott L ^a   Myers, Connie ^a   Young, David M ^a   Boudreau, Nancy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Angiogenesis; Cell migration; HOXA3; uPAR; Wound repair

Indexed keywords

MATRIX METALLOPROTEINASE 14; PROTEIN HOXA3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXA3; UNCLASSIFIED DRUG; UROKINASE RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DAMAGE; CELL FUNCTION; CELL MIGRATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIUM CELL; EPITHELIUM CELL; GENE EXPRESSION; GENE TRANSFER; HUMAN; HUMAN CELL; IN VIVO STUDY; KERATINOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; TISSUE REPAIR; UPREGULATION; WOUND CLOSURE; WOUND HEALING;

ANGIOGENIC PROTEINS; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIAL CELLS; EPITHELIAL CELLS; HOMEODOMAIN PROTEINS; HUMANS; KERATINOCYTES; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; METALLOENDOPEPTIDASES; MICE; MICE, INBRED NOD; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CELL SURFACE; SKIN; TRANS-ACTIVATION (GENETICS); UP-REGULATION; WOUND HEALING;

ANIMALIA;

EID: 21644472188     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02399     Document Type: Article

References (46)

1. Ades, E. W., Candal, F. J., Swerlick, R. A., George, V. G., Summers, S., Bosse, D. C. and Lawley, T. J. (1992). HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J. Invest. Dermatol. 99, 683-690.
2. Belotti, D., Clausse, N., Flagiello, D., Alami, Y., Daukandt, M., Deroanne, C., Malfoy, B., Boncinelli, E., Faiella, A. and Castronovo, V. (1998). Expression and modulation of homeobox genes from cluster B in endothelial cells. Lab. Invest. 78, 1291-1299.
3. Blasi, F. and Carmeliet, P. (2002). uPAR: a versatile signalling orchestrator. Nat. Rev. Mol. Cell Biol. 3, 932-943.
4. Boudreau, N. J. and Varner, J. A. (2004). The homeobox transcription factor Hox D3 promotes integrin alpha5beta1 expression and function during angiogenesis. J. Biol. Chem. 279, 4862-4868.
5. Boudreau, N., Andrews, C., Srebrow, A., Ravanpay, A. and Cheresh, D. A. (1997). Induction of the angiogenic phenotype by Hox D3. J. Cell Biol. 139, 257-264.
6. Bruhl, T., Urbich, C., Aicher, D., Acker-Palmer, A., Zeiher, A. M. and Dimmeler, S. (2004). Homeobox A9 transcriptionally regulates the EphB4 receptor to modulate endothelial cell migration and tube formation. Circ. Res. 94, 743-751.
7. Cantile, M., Pettinato, G., Procino, A., Feliciello, I., Cindolo, L. and Cillo, C. (2003). In vivo expression of the whole HOX gene network in human breast cancer. Eur. J. Cancer 39, 257-264.
8. Chen, F. and Capecchi, M. R. (1999). Paralogous mouse Hox genes, Hoxa9, Hoxb9, and Hoxd9, function together to control development of the mammary gland in response to pregnancy. Proc. Natl. Acad. Sci. USA 96, 541-546.
9. Chen, J. and Ruley, H. E. (1998). An enhancer element in the EphA2 (Eck) gene sufficient for rhombomere-specific expression is activated by HOXA1 and HOXB1 homeobox proteins. J. Biol. Chem. 273, 24670-24675.
10. Chun, T. H., Sabeh, F., Ota, I., Murphy, H., McDonagh, K. T., Holmbeck, K., Birkedal-Hansen, H., Allen, E. D. and Weiss, S. J. (2004). MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J. Cell Biol. 167, 757-767.
11. Cillo, C., Cantile, M., Mortarini, R., Barba, P., Parmiani, G. and Anichini, A. (1996). Differential patterns of HOX gene expression are associated with specific integrin and ICAM profiles in clonal populations isolated from a single human melanoma metastasis. Int. J. Cancer 66, 692-697.
12. Cillo, C., Faiella, A., Cantile, M. and Boncinelli, E. (1999). Homeobox genes and cancer. Exp. Cell Res. 248, 1-9.
13. Collen, A., Hanemaaijer, R., Lupu, F., Quax, P. H., van Lent, N., Grimbergen, J., Peters, E., Koolwijk, P. and van Hinsbergh, V. W. (2003). Membrane-type matrix metalloproteinase-mediated angiogenesis in a fibrin-collagen matrix. Blood 101, 1810-1817.
14. Condie, B. G. and Capecchi, M. R. (1994). Mice with targeted disruptions in the paralogous genes hoxa-3 and hoxd-3 reveal synergistic interactions. Nature 370, 304-307.
15. Coussens, L. M. and Werb, Z. (2002). Inflammation and cancer. Nature 420, 860-867.
16. Coussens, L. M., Tinkle, C. L., Hanahan, D. and Werb, Z. (2000). MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103, 481-490.
17. Daniel, R. J. and Groves, R. W. (2002). Increased migration of murine keratinocytes under hypoxia is mediated by induction of urokinase plasminogen activator. J. Invest. Dermatol. 119, 1304-1309.
18. Fibbi, G., Caldini, R., Chevanne, M., Pucci, M., Schiavone, N., Morbidelli, L., Parenti, A., Granger, H. J., Del Rosso, M. and Ziche, M. (1998). Urokinase-dependent angiogenesis in vitro and diacylglycerol production are blocked by antisense oligonucleotides against the urokinase receptor. Lab. Invest. 78, 1109-1119.
19. Gaufo, G. O., Thomas, K. R. and Capecchi, M. R. (2003). Hox3 genes coordinate mechanisms of genetic suppression and activation in the generation of branchial and somatic motoneurons. Development 130, 5191-5201.
20. Greenhalgh, D. G., Sprugel, K. H., Murray, M. J. and Ross, R. (1990). PDGF and FGF stimulate wound healing in the genetically diabetic mouse. Am. J. Pathol. 136, 1235-1246.
21. Greer, J. M., Puetz, J., Thomas, K. R. and Capecchi, M. R. (2000). Maintenance of functional equivalence during paralogous Hox gene evolution. Nature 403, 661-665.
22. Gruss, C. J., Satyamoorthy, K., Berking, C., Lininger, J., Nesbit, M., Schaider, H., Liu, Z. J., Oka, M., Hsu, M. Y., Shirakawa, T. et al. (2003). Stroma formation and angiogenesis by overexpression of growth factors, cytokines, and proteolytic enzymes in human skin grafted to SCID mice. J. Invest. Dermatol. 120, 683-692.
23. Haas, T. L., Stitelman, D., Davis, S. J., Apte, S. S. and Madri, J. A. (1999). Egr-1 mediates extracellular matrix-driven transcription of membrane type 1 matrix metalloproteinase in endothelium. J. Biol. Chem. 274, 22679-22685.
24. Hansen, S. L., Myers, C. A., Charboneau, A., Young, D. M. and Boudreau, N. (2003a). HoxD3 accelerates wound healing in diabetic mice. Am. J. Pathol. 163, 2421-2431.
25. Hansen, S. L., Young, D. M. and Boudreau, N. B. (2003b). HoxD3 expression and collagen synthesis in diabetic fibroblasts. Wound Repair Regen. 11, 474-480.
26. Hiraoka, N., Allen, E., Apel, I. J., Gyetko, M. R. and Weiss, S. J. (1998). Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell 95, 365-377.
27. Jones, F. S., Chalepakis, G., Gruss, P. and Edelman, G. M. (1992). Activation of the cytotactin promoter by the homeobox-containing gene Evx-1. Proc. Natl. Acad. Sci. USA 89, 2091-2095.
28. Krampert, M., Bloch, W., Sasaki, T., Bugnon, P., Rulicke, T., Wolf, E., Aumailley, M., Parks, W. C. and Werner, S. (2004). Activities of the matrix metalloproteinase Stromelysin-2 (MMP-10) in matrix degradation and keratinocyte organization in wounded skin. Mol. Biol. Cell 15, 5242-5254.
29. Kroon, M. E., Koolwijk, P., van Goor, H., Weidle, U. H., Collen, A., van der Pluijm, G. and van Hinsbergh, V. W. (1999). Role and localization of urokinase receptor in the formation of new microvascular structures in fibrin matrices. Am. J. Pathol. 154, 1731-1742.
30. Lafleur, M. A., Handsley, M. M., Knauper, V., Murphy, G. and Edwards, D. R. (2002). Endothelial tubulogenesis within fibrin gels specifically requires the activity of membrane-type-matrix metalloproteinases (MT-MMPs). J. Cell Sci. 115, 3427-3438.
31. Lakka, S. S., Gondi, C. S., Yanamandra, N., Dinh, D. H., Olivero, W. C., Gujrati, M. and Rao, J. S. (2003). Synergistic down-regulation of urokinase plasminogen activator receptor and matrix metalloproteinase-9 in SNB19 glioblastoma cells efficiently inhibits glioma cell invasion, angiogenesis, and tumor growth. Cancer Res. 63, 2454-2461.
32. Li, F., Goncalves, J., Faughnan, K., Steiner, M. G., Pagan-Charry, L, Esposito, D., Chin, B., Providence, K. M., Higgins, P. J. and Staiano-Coico, L. (2000). Targeted inhibition of wound-induced PAI-1 expression alters migration and differentiation in human epidermal keratinocytes. Exp. Cell Res. 258, 245-253.
33. Lorentz, O., Duluc, I., Arcangelis, A. D., Simon-Assmann, P., Kedinger, M. and Freund, J. N. (1997). Key role of the Cdx2 homeobox gene in extracellular matrix-mediated intestinal cell differentiation. J. Cell Biol. 139, 1553-1565.
34. Manley, N. R. and Capecchi, M. R. (1997). Hox group 3 paralogous genes act synergistically in the formation of somitic and neural crest-derived structures. Dev. Biol. 192, 274-288.
35. Martin, P. and Parkhurst, S. M. (2004). Parallels between tissue repair and embryo morphogenesis. Development 131, 3021-3034.
36. Myers, C., Charboneau, A. and Boudreau, N. (2000). Homeobox B3 promotes capillary morphogenesis and angiogenesis. J. Cell Biol. 148, 343-351.
37. Nehls, V. and Drenckhahn, D. (1995). A microcarrier-based cocultivation system for the investigation of factors and cells involved in angiogenesis in three-dimensional fibrin matrices in vitro. Histochem. Cell Biol. 104, 459-466.
38. Patel, C. V., Sharangpani, R., Bandyopadhyay, S. and DiCorleto, P. E. (1999). Endothelial cells express a novel, tumor necrosis factor-alpha-regulated variant of HOXA9. J. Biol. Chem. 274, 1415-1422.
39. Penkov, D., Tanaka, S., Di, Rocco, G., Berthelsen, J., Blasi, F. and Ramirez, F. (2000). Cooperative interactions between PBX, PREP, and HOX proteins modulate the activity of the alpha 2(V) collagen (COL5A2) promoter. J. Biol. Chem. 275, 16681-16689.
40. Raman, V., Martensen, S. A., Reisman, D., Evron, E., Odenwald, W. F., Jaffee, E., Marks, J. and Sukumar, S. (2000). Compromised HOXA5 function can limit p53 expression in human breast tumours. Nature 405, 974-978.
41. Stelnicki, E. J., Arbeit, J., Cass, D. L., Saner, C., Harrison, M. and Largman, C. (1998). Modulation of the human homeobox genes PRX-2 and HOXB13 in scarless fetal wounds. J. Invest. Dermatol. 111, 57-63.
42. Uyeno, L. A., Newman-Keagle, J. A., Cheung, I., Hunt, T. K., Young, D. M. and Boudreau, N. (2001). Hox D3 expression in normal and impaired wound healing. J. Surg. Res. 100, 46-56.
43. Vasir, B., Reitz, P., Xu, G., Sharma, A., Bonner-Weir, S. and Weir, G. C. (2000). Effects of diabetes and hypoxia on gene markers of angiogenesis (HGF, cMET, uPA and uPAR, TGF-alpha, TGF-beta, bFGF and Vimentin) in cultured and transplanted rat islets. Diabetologia 43, 763-772.
44. Wang, Z., Troilo, P. J., Wang, X., Griffiths, T. G., Pacchione, S. J., Barnum, A. B., Harper, L. B., Pauley, C. J., Niu, Z., Denisova, L. et al. (2004). Detection of integration of plasmid DNA into host genomic DNA following intramuscular injection and electroporation. Gene Ther. 11, 711-721.
45. Xu, Y., Swerlick, R. A., Sepp, N., Bosse, D., Ades, E. W. and Lawley, T. J. (1994). Characterization of expression and modulation of cell adhesion molecules on an immortalized human dermal microvascular endothelial cell line (HMEC-1). J. Invest. Dermatol. 102, 833-837.
46. Zhou, H. M., Nichols, A., Meda, P. and Vassalli, J. D. (2000). Urokinase-type plasminogen activator and its receptor synergize to promote pathogenic proteolysis. EMBO J. 19, 4817-4826.