Coordinating epidermal growth factor-induced motility promotes efficient wound closure

American Journal of Physiology - Cell Physiology

Volumn 288, Issue 1 57-1, 2005, Pages

  Kurten, Richard C ^a,b   Chowdhury, Parag ^a   Sanders Jr , Ronald C ^c   Pittman, Laura M ^a   Sessions, Laura W ^a   Chambers, Timothy C ^a   Lyle, Christopher S ^a   Schnackenberg, Bradley J ^a,b   Jones, Stacie M ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b ARKANSAS CHILDREN S HOSPITAL RESEARCH INSTITUTE   (United States)

^c University of Florida and UF Health Shands Children s Hospital   (United States)

Author keywords

Cell motility; Wound healing

Indexed keywords

EPIDERMAL GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MOTILITY; CONTROLLED STUDY; EPITHELIUM CELL; FIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SERUM FACTOR; TISSUE CULTURE; TISSUE INJURY; WOUND HEALING;

ANIMALS; BLOOD PROTEINS; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; FIBROBLASTS; KIDNEY; WOUND HEALING;

ANIMALIA;

EID: 10644294753     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00024.2003     Document Type: Article

References (53)

1. Balkovetz DF. Hepatocyte growth factor and Madin-Darby canine kidney cells: in vitro models of epithelial cell movement and morphogenesis. Microsc Res Tech 43: 456-463, 1998.
2. Behrens J, Vakaet L, Friis R, Winterhager E, Van Roy F, Mareel MM, and Birchmeier W. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/beta-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J Cell Biol 120: 757-766, 1993.
3. Carlin CR, Phillips PD, Knowles BB, and Cristofalo VJ. Diminished in vitro tyrosine kinase activity of the EGF receptor of senescent human fibroblasts. Nature 306: 617-620, 1983.
4. Cerutis DR, Dreyer A, Cordini F, McVaney TP, Mattson JS, Parrish LC, Romito L, Huebner GR, and Jabro M. Lysophosphatidic acid modulates the regenerative responses of human gingival fibroblasts and enhances the actions of platelet-derived growth factor. J Periodontol 75: 297-305, 2004.
5. Cerutis DR, Nogami M, Anderson JL, Churchill JD, Hornberger DJ, Rennard SI, and Toews ML. Lysophosphatidic acid and EGF stimulate mitogenesis in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 273: L10-L15, 1997.
6. Chen P, Gupta K, and Wells A. Cell movement elicited by epidermal growth factor receptor requires kinase and autophosphorylation but is separable from mitogenesis. J Cell Biol 124: 547-555, 1994.
7. Chen P, Xie H, Sekar MC, Gupta K, and Wells A. Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J Cell Biol 127: 847-857, 1994.
8. Chou J, Burke NA, Iwabu A, Watkins SC, and Wells A. Directional motility induced by epidermal growth factor requires Cdc42. Exp Cell Res 287: 47-56, 2003.
9. Cohen S, Fava RA, and Sawyer ST. Purification and characterization of epidermal growth factor receptor/protein kinase from normal mouse liver. Proc Natl Acad Sci USA 79: 6237-6241, 1982.
10. Cohen S, Ushiro H, Stoscheck C, and Chinkers M. A native 170,000 epidermal growth factor receptor-kinase complex from shed plasma membrane vesicles. J Biol Chem 257: 1523-1531, 1982.
11. Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, and Gruenert DC. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 10: 38-47, 1994.
12. Davies DE, Polosa R, Puddicombe SM, Richter A, and Holgate ST. The epidermal growth factor receptor and its ligand family: their potential role in repair and remodelling in asthma. Allergy 54: 771-783, 1999.
13. Fenteany G, Janmey PA, and Stossel TP. Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr Biol 10: 831-838, 2000.
14. Fukata M, Nakagawa M, and Kaibuchi K. Roles of Rho-family GTPases in cell polarisation and directional migration. Curr Opin Cell Biol 15: 590-597, 2003.
15. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 200: 500-503, 2003.
16. Gatlin J, Melkus MW, Padgett A, Petroll WM, Cavanagh HD, Garcia JV, and Jester JV. In vivo fluorescent labeling of corneal wound healing fibroblasts. Exp Eye Res 76: 361-371, 2003.
17. Huttenlocher A, Palecek SP, Lu Q, Zhang W, Mellgren RL, Lauffenburger BA, Ginsberg MH, and Horwitz AF. Regulation of cell migration by the calcium-dependent protease calpain. J Biol Chem 272: 32719-32722, 1997.
18. Jensen FC, Girardi AJ, Gilden RV, and Koprowski H. Infection of human and simian tissue cultures with Rous Sarcoma Virus. Proc Natl Acad Sci USA 52: 53-59, 1964.
19. Jester JV, Petroll WM, Barry PA, and Cavanagh HD. Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing. Invest Ophthalmol Vis Sci 36: 809-819, 1995.
20. Jones SM, Foreman SK, Shank BB, and Kurten RC. EGF receptor downregulation depends on a trafficking motif in the distal tyrosine kinase domain. Am J Physiol Cell Physiol 282: C420-C433, 2002.
21. Kheradmand F, Folkesson HG, Shum L, Derynk R, Pytela R, and Matthay MA. Transforming growth factor-α enhances alveolar epithelial cell repair in a new in vitro model. Am J Physiol Lung Cell Mol Physiol 267: L728-L738, 1994.
22. Kiehart DP. Wound healing: the power of the purse string. Curr Biol 9: R602-R605, 1999.
23. Kim JS, McKinnis VS, Nawrocki A, and White SR. Stimulation of migration and wound repair of guinea-pig airway epithelial cells in response to epidermal growth factor. Am J Respir Cell Mol Biol 18: 66-74, 1998.
24. Lai WH, Cameron PH, Wada I, Doherty JJ II, Kay DG, Posner BI, and Bergeron JJ. Ligand-mediated internalization, recycling, and down-regulation of the epidermal growth factor receptor in vivo. J Cell Biol 109: 2741-2749, 1989. [Corrigenda. J Cell Biol 110: January 1990, following p. 227.]
25. Lee H, Goetzl EJ, and An S. Lysophosphatidic acid and sphingosine 1-phosphate stimulate endothelial cell wound healing. Am J Physiol Cell Physiol 278: C612-C618, 2000.
26. Lotz MM, Rabinovitz I, and Mercurio AM. Intestinal restitution: progression of actin cytoskeleton rearrangements and integrin function in a model of epithelial wound healing. Am J Pathol 156: 985-996, 2000.
27. Maheshwari G, Wells A, Griffith LG, and Lauffenburger DA. Biophysical integration of effects of epidermal growth factor and fibronectin on fibroblast migration. Biophys J 76: 2814-2823, 1999.
28. Martin P. Wound healing - aiming for perfect skin regeneration. Science 276: 75-81, 1997.
29. Matthay MA, Thiery JP, Lafont F, Stampfer F, and Boyer B. Transient effect of epidermal growth factor on the motility of an immortalized mammary epithelial cell line. J Cell Sci 106: 869-878, 1993.
30. McCawley LJ, O'Brien P, and Hudson LG. Overexpression of the epidermal growth factor receptor contributes to enhanced ligand-mediated motility in keratinocyte cell lines. Endocrinology 138: 121-127, 1997.
31. McCormack SA, Viar MJ, and Johnson LR. Migration of IEC-6 cells: a model for mucosal healing. Am J Physiol Gastrointest Liver Physiol 263: G426-G435, 1992.
32. Nanney LB, Paulsen S, Davidson MK, Cardwell NL, Whitsitt JS, and Davidson JM. Boosting epidermal growth factor receptor expression by gene gun transfection stimulates epidermal growth in vivo. Wound Repair Regen 8: 117-127, 2000.
33. Nawrocki-Raby B, Gilles C, Polette M, Bruyneel E, Laronze JY, Bonnet N, Foidart JM, Mareel M, and Birembaut P. Upregulation of MMPs by soluble E-cadherin in human lung tumor cells. Int J Cancer 105: 790-795, 2003.
34. Nichols WW, Murphy DG, Cristofalo VJ, Toji LH, Greene AE, and Dwight SA. Characterization of a new human diploid cell strain, IMR-90. Science 196: 60-63, 1977.
35. Noguchi S, Ohba Y, and Oka T. Effect of salivary epidermal growth factor on wound healing of tongue in mice. Am J Physiol Endocrinol Metab 260: E620-E625, 1991.
36. Oertel M, Graness A, Thim L, Buhling F, Kalbacher H, and Hoffmann W. Trefoil factor family-peptides promote migration of human bronchial epithelial cells: synergistic effect with epidermal growth factor. Am J Respir Cell Mol Biol 25: 418-424, 2001.
37. Okada H, Danoff TM, Kalluri R, and Neilson EG. Early role of Fsp1 in epithelial-mesenchymal transformation. Am J Physiol Renal Physiol 273: F563-F574, 1997.
38. Palecek SP, Huttenlocher A, Horwitz AF, and Lauffenburger DA. Physical and biochemical regulation of integrin release during rear detachment of migrating cells. J Cell Sci 111: 929-940, 1998.
39. Puddicombe SM, Polosa R, Richter A, Krishna MT, Howarth PH, Holgate ST, and Davies DE. Involvement of the epidermal growth factor receptor in epithelial repair in asthma. FASEB J 14: 1362-1374, 2000.
40. Reenstra WR, Yaar M, and Gilchrest BA. Effect of donor age on epidermal growth factor processing in man. Exp Cell Res 209: 118-122, 1993.
41. Shiraha H, Glading A, Gupta K, and Wells A. IP-10 inhibits epidermal growth factor-induced motility by decreasing epidermal growth factor receptor-mediated calpain activity. J Cell Biol 146: 243-254, 1999.
42. Stolz DB and Michalopoulos GK. Synergistic enhancement of EGF, but not HGF, stimulated hepatocyte motility by TGF-β1 in vitro. J Cell Physiol 170: 57-68, 1997.
43. Sturm A, Sudermann T, Schulte KM, Goebell H, and Dignass AU. Modulation of intestinal epithelial wound healing in vitro and in vivo by lysophosphatidic acid. Gastroenterology 117: 368-377, 1999.
44. Sunada H, Magun BE, Mendelsohn J, and MacCleod CL. Monoclonal antibody against EGF receptor is internalized without stimulating receptor phosphorylation. Proc Natl Acad Sci USA 83: 3825-3829, 1986.
45. Tsutsumi Q, Kurachi H, and Oka T. A physiological role of epidermal growth factor in male reproductive function. Science 233: 975-977, 1986.
46. Ullrich A, Cousens L, Hayflick JS, Dull TJ, Gray A, Tam AW, Lee J, Yarden Y, Libermann TA, Schlessinger J, Downward J, Mayes ELV, Whittle N, Waterfield MD, and Seeburg PH. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309: 418-425, 1984.
47. Vermeer PD, Einwalter LA, Moninger TO, Rokhlina T, Kern JA, Zabner J, and Welsh MJ. Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 422: 322-326, 2003.
48. Vleminckx K, Vakaet L Jr, Mareel M, Fiers W, and van Roy F. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66: 107-119, 1991.
49. Wells A, Gupta K, Chang P, Swindle S, Glading A, and Shiraha H. Epidermal growth factor receptor-mediated motility in fibroblasts. Microsc Res Tech 43: 395-411, 1998.
50. Welsh JB, Gill GN, Rosenfeld MG, and Wells A. A negative feedback loop attenuates EGF-induced morphological changes. J Cell Biol 114: 533-543, 1991.
51. Werner S and Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 83: 835-870, 2003.
52. Wood W, Jacinto A, Grose R, Woolner S, Gale J, Wilson C, and Martin P. Wound healing recapitulates morphogenesis in Drosophila embryos. Nat Cell Biol 4: 907-912, 2002.
53. Xie H, Pallero MA, Gupta K, Chang P, Ware MF, Witke W, Kwiatkowski DJ, Lauffenburger DA, Murphy-Ullrich JE, and Wells A. EGF receptor regulation of cell motility: EGF induces disassembly of focal adhesions independently of the motility-associated PLCgamma signaling pathway. J Cell Sci 111: 615-624, 1998.