Deletion of the homeobox gene PRX-2 affects fetal but not adult fibroblast wound healing responses

Journal of Investigative Dermatology

Volumn 120, Issue 1, 2003, Pages 135-144

  White, Philip ^a   Thomas, David W ^a   Fong, Steven ^b   Stelnicki, Eric ^e   Meijlink, Fritz ^c   Largman, Corey ^b   Stephens, Phil ^a,d  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HUBRECHT INSTITUTE   (Netherlands)

^d CARDIFF UNIVERSITY   (United Kingdom)

^e NONE

Author keywords

Fibroblast; Homeobox gene; Prx 2; Wound healing

Indexed keywords

GELATINASE A; HYALURONIC ACID; MUTANT PROTEIN; TRANSCRIPTION FACTOR;

ADOLESCENT; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FETUS; FIBROBLAST; GENE DELETION; GENE EXPRESSION; GENETIC STRAIN; HOMEOBOX; HOMOZYGOSITY; IN VITRO STUDY; IN VIVO STUDY; LEG ULCER; MESENCHYME CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SKIN SCAR; WILD TYPE; WOUND HEALING;

EID: 0037243526     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.2003.12015.x     Document Type: Article

References (65)

1. Adzick NS, Lorenz HP: Cells, matrix, growth-factors, and the surgeon - the biology of scarless fetal wound repair. Ann Surg 220:10-18, 1994
2. Ahlgren T, Jarstrand C: Hyaluronic acid enhanced phagocytosis of human monocytes in vitro. J Clin Immunol 4:246-249, 1984
3. Al-Khateeb T, Stephens P, Shepherd JP, Thomas DW: An investigation of preferential fibroblast wound repopulation using a novel in vitro wound model. J Periodontol 68:1063-1069, 1997
4. Aumailley M, Mann K, von der Mark H, Timpl R: Cell attachment properties of collagen type VI and arg-gly-asp dependent binding to its α2(VI) and α3(VI) chains. Exp Cell Res 181:463-474, 1989
5. Azzam HS, Thompson EW: Collagen-induced activation of the Mr 72,000 type-IV collagenase in normal and malignant human fibroblastoid cells. Cancer Res 52:4540-4544, 1992
6. Bell E, Ivarsson B, Merrill C: Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vi-tro. Proc Natl Acad Sci USA 76:1274-1278, 1979
7. ten Berge D, Brouwer A, Korving J, Martin J, Meijlink F: Prx1 and Prx2 in skeletogenesis: roles in the craniofacial region, inner ear and limbs. Development 125:3831-3842, 1998
8. Bieberich CJ, Ruddle FH, Stenn KS: Differential expression of the hox 3.1 gene in adult-mouse skin. Ann N Y Acad Sci 642:346-354, 1991
9. Boudreau N, Andrews C, Srebrow A, Ravanpay A, Cheresh DA: Induction of the angiogenic phenotype by Hox D3. J Cell Biol 139:257-264, 1997
10. Burd DAR, Longaker MT, Rittenberg T, Adzick NS, Harrison MR, Ehrlich HP: In vitro fetal wound contraction - the effect of amniotic-fluid. Br J Plast Surg 44:302-305, 1991
11. Care A, Silvani A, Meccia E, et al: HOXB7 constitutively activates basic fibroblast growth factor in melanomas. Mol Cell Biol 16:4842-4851, 1996
12. Chapman SC, Ayala JE, Streeper RS, et al: Multiple promoter elements are required for the stimulatory effect of insulin on human collagenase-1 gene transcription - selective effects on activator protein-1 expression may explain the quantitative difference in insulin and phorbol ester action. J Biol Chem 274:18625-18634, 1999
13. Cillo C, Faiella A, Cantile M, Boncinelli E: Homeobox genes and cancer. Exp Cell Res 248:1-9, 1999
14. Clark EA, Brugge JS: Integrins and signal-transduction pathways - the road taken. Science 268:233-239, 1995
15. Cook H, Stephens P, Davies KJ, Harding KG, Thomas DW: Defective extracellular matrix reorganisation by chronic wound fibroblasts is associated with alterations in TIMP-1, TIMP-2 and MMP-2 activity. J Invest Dermatol 115:225-233, 2000
16. Coughlan AR, Robertson DHL, Burke R, Beynon RJ, Carter SD: Isolation and identification of canine matrix metalloproteinase-2 (MMP-2). Vet J 155:231-237, 1998
17. De Jong R, Meijlink F: The homeobox gene S8: mesoderm-specific expression in presomite embryos and in cells cultured in vitro and modulation in differentiating pluripotent cells. Dev Biol 157:133-146, 1993
18. Deryugina EI, Bourdon MA, Reisfeld RA, Strongin A: Remodelling of collagen matrix by human tumor cells requires activation and cell surface association of matrix metalloproteinase-2. Cancer Res 58:3737-3750, 1998
19. Desmouliere A, Gabbiani G: The role of the myofibroblast in wound healing and fibrocontractive diseases. In: Clark RAF, ed. Molecular and Cellular Biology of Wound Repair, 2nd edn. New York: Plenum Press, 1996: pp 391-423
20. Detmer K, Lawrence HJ, Largman C: Expression of class I homeobox genes in fetal and adult murine skin. J Invest Dermatol 101:517-522, 1993
21. Ehrlich HP, Rajaratnam JBM: Cell locomotion forces versus cell contraction forces for collagen lattice contraction - an in vitro model of wound contraction.Tissue Cell 22:407-417, 1990
22. Ellis I, Banyard J, Schor SL: Differential response of fetal and adult fibroblasts to cytokines: cell migration and hyaluronan synthesis. Development 124:1593-1600, 1997
23. Fainsod A, Bogarad LD, Ruusala T, Lubin M, Crothers DM, Ruddle FH: The homeo domain of a murine protein binds 5′ to its own homeo box. Proc Natl Acad Sci USA 83:9532-9536, 1986
24. Farndale RWA, Barrett AJ: Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883:173-177, 1986
25. Grinnell F: Fibroblasts, myofibroblasts, and wound contraction. J Cell Biol 124:401-404, 1994
26. Haas TL, Davis SJ, Madri JA: Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. J Biol Chem 273:3604-3610, 1998
27. Holly SP, Larson MK, Parise LV: Multiple roles of integrins in cell motility. Exp Cell Res 261:69-74, 2000
28. van den Hoogen BM, van Weeren PR, Lopes-Cardozo M, van Golde LM, Barne-veld A, van de Lest CH: A microtiter plate assay for the determination of uronic acids. Anal Biochem 257:107-111, 1998
29. Inagaki Y, Nemoto T, Nakao A, Dijke Part P, Kobayashi K,Takehara K, Greenwel P: Interaction between GC box binding factors and Smad proteins modulates cell lineage-specific α2(I) collagen gene transcription. J Biol Chem 276:16573-16579, 2001
30. Jayaraman G, Srinivas R, Duggan C, et al: p300/cAMP-responsive element- binding protein interactions with Ets-1 and Ets-2 in the transcriptional activation of the human stromelysin promoter. J Biol Chem 274:17342-17352, 1999
31. Jones FS, Prediger EA, Bittner DA, De Robertis EM, Edelman GM: Cell adhesion molecules as targets for Hox genes: neural cell adhesion molecule promoter activity is modulated by cotransfection with Hox-2.5 and -2.4. Proc Natl Acad Sci USA 89:2086-2090, 1992
32. Krumlauf R: Hox genes in vertebrate development. Cell 78:191-201, 1994
33. Lawrence HJ, Sauvageau G, Humphries RK, Largman C: The role of HOX homeo-box genes in normal and leukemic hematopoiesis. Stem Cells 14:281-291, 1996
34. Longaker M, Adzick N: The biology of fetal wound healing. Plast Reconstr Surg 87:788-798, 1991
35. Lorenz HP, Longaker MT, Whitby DJ, Harrison MR, Adzick NS: Scarless fetal skin repair is intrinsic to the fetal fibroblast. Surg Forum 43:694-696, 1992
36. Lorenz H, Lin R, Longaker M, Whitby D, Adzick N: The fetal fibroblast: the effector cell of scarless fetal skin repair. Plast Reconstr Surg 96:1251-1259, 1995
37. Lu M-F, Cheng H-T, Kern M, Potter S, Tran B, Diekwisch T, Martin J: Prx-1 functions cooperatively with another paired-related homeobox gene, Prx-2 , to maintain cell fates within the craniofacial mesenchyme. Development 126:495-504, 1999
38. Mavilio F, Simeone A, Giampaolo A, et al: Differential and stage-related expression in embryonic tissues of a new human homoeobox gene. Nature 324:664-668, 1986
39. Meyer LJM, Stern R: Age-dependent changes of hyaluronan in human skin. J Invest Dermatol 102:385-389, 1994
40. Mosmann T: Rapid colormetric assay for cellular growth and survival - application to proliferation and cytotoxic assays. J Immunol Meth 65:55-63, 1983
41. O'Kane S, Ferguson MWJ: Transforming growth factor βs and wound healing. Int J Biochem Cell Biol 29:63-78, 1997
42. Palecek SP, Schmidt CE, Lauffenburger DA, Horwitz AF: Integrin dynamics on the tail region of migrating fibroblasts. J Cell Sci 109:941-952, 1996
43. Perkins A, Kongsuwan K, Visvader J, Adams JM, Cory S: Homeobox gene expression plus autocrine growth factor production elicits myeloid leukemia. Proc Natl Acad Sci USA 87:8398-8402, 1990
44. Rieger E, Bijl JJ, van Oostveen JW, et al: Expression of the homeobox gene HOXC4 in keratinocytes of normal skin and epithelial skin tumors is correlated with differentiation. J Invest Dermatol 103:341-346, 1994
45. Rooney P, Kumar S: Inverse relationship between hyaluronan and collagens in development and angiogenesis. Differentiation 54:1-9, 1993
46. Rowling PJE, Raxworthy MJ, Wood EJ, Kearney JN: Fabrication and reorganization of dermal equivalents suitable for skin grafting after major cutaneous injury. Biomaterials 11:181-185, 1990
47. Sander G, Bawden CS, Hynd PI, Nesci A, Rogers G, Powell BC: Expression of the homeobox gene, Barx2, in wool follicle development. J Invest Dermatol 115:753-756, 2000
48. Schor SL, Ellis I, Irwin CR, et al: Subpopulations of fetal-like gingival fibroblasts: characterisation and potential significance for wound healing and the progression of periodontal disease. Oral Dis 2:155-166, 1996
49. Scott GA, Goldsmith LA: Homeobox genes and skin development: a review. J Invest Dermatol 101:3-8, 1993
50. Seltzer JL, Lee AY, Akers KT, Sudbeck B, Southon EA, Wayner EA, Eisen AZ: Activation of 72-kDa type-IV collagenase/gelatinase by normal fibroblasts in collagen lattices is mediated by integrin receptors but is not related to lattice contraction. Exp Cell Res 213:365-374, 1994
51. Shah M, Foreman DM, Ferguson MWJ: Neutralizing antibodies to TGFβ1,2 reduces cutaneous scarring in adult rodents. J Cell Sci 107:1137-1157, 1994
52. Shah M, Foreman OM, Ferguson MWJ: Neutralization of TGFβ1 and TGFβ2 or exogenous addition of TGFβ3 to cutaneous wounds reduces scarring. J Cell Sci 108:983-1002, 1995
53. Siebert J, Burd D, McCarthy J,Weinzweig J, Ehrlich H: Fetal wound healing: a biochemical study of scarless healing. Plast Reconstr Surg 85:495-502, 1990
54. Stelnicki E, Arbeit J, Cass DL, Saner C, Harrison M, Largman C.: Modulation of the human homeobox genes PRX-2 and HOXB13 in scarless fetal wounds. J Invest Dermatol 111:57-63, 1998
55. Stephens P, Davies KJ, Al-Khateeb T, Shepherd JP, Thomas DW: A comparison of the ability of intra oral and extra oral fibroblasts to stimulate extracellular matrix reorganization in a model of wound contraction. J Dent Res 75:1358-1364, 1996
56. Stephens P, Davies KJ, Occleston N, et al: Skin and oral fibroblasts exhibit phenotypic differences in extracellular matrix reorganization and matrix metalloproteinase activity. Br J Dermatol 144:229-237, 2001
57. Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI: Mechanism of cell surface activation of the 72-kDa type IV collagenase. J Biol Chem 270:5331-5338, 1995
58. Taniguchi Y, Komatsu N, Moriuchi T: Overexpression of the HOX4A (HOXD3) homeobox gene in human erythroleukemia HEL cells results in altered adhesive properties. Blood 85:2786-2794, 1995
59. Thali M, Muller MM, DeLorenzi M, Matthias P, Bienz M: Drosophila homoeotic genes encode transcriptional activators similar to mammalian OTF-2. Nature 336:598-601, 1988
60. Thomas DW, O'Neill ID, Harding KG, Shepherd JP: Cutaneous wound-healing - a current perspective. J Oral Maxillofac Surg 53:442-447, 1995
61. Tomasek JJ, Halliday NL, Updike DL, Ahern Moore JS,Vu TKH, Liu RW, Howard EW: Gelatinase A activation is regulated by the organization of the polymerized actin cytoskeleton. J Biol Chem 272:7482-7487, 1997
62. Verrecchia F, Mauviel A: Transforming growth factor-β signalling through the Smad pathway: role in extracellular matrix gene expression and regulation. J Invest Dermatol 118:211-215, 2002
63. West DC, Shaw DM, Lorenz P, Adzick NS, Longaker MT: Fibrotic healing of adult and late gestation fetal wounds correlates with increased hyaluronidase activity and removal of hyaluronan. Int J Biochem Cell Biol 29:201-210, 1997
64. Westermarck J, Kahari VM: Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J 13:781-792, 1999
65. Xu JH, Zutter MM, Santoro SA, Clark RAF: A three-dimensional collagen lattice activates NF-κB in human fibroblasts. Role in integrin alpha (2) gene expression and tissue remodeling. J Cell Biol 140:709-719, 1998