Wounding sheets of epithelial cells activates the epidermal growth factor receptor through distinct short- and long-range mechanisms

Molecular Biology of the Cell

Volumn 19, Issue 11, 2008, Pages 4909-4917

  Block, Ethan R ^a   Klarlund, Jes K ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; APYRASE; EPIDERMAL GROWTH FACTOR RECEPTOR; PHOSPHOLIPASE D2; ISOENZYME; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE D; PROTEIN TYROSINE KINASE;

ARTICLE; CELL DAMAGE; CELL MOTILITY; CONTROLLED STUDY; EPITHELIUM CELL; GENE ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; BIOLOGICAL MODEL; CELL LINE; CORNEA LIMBUS; CYTOLOGY; ENZYME ACTIVATION; ENZYMOLOGY; EXTRACELLULAR SPACE; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; WOUND HEALING;

ADENOSINE TRIPHOSPHATE; CELL LINE; ENZYME ACTIVATION; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; EXTRACELLULAR SPACE; HUMANS; ISOENZYMES; LIMBUS CORNEAE; MODELS, BIOLOGICAL; PHOSPHOLIPASE D; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRANSCRIPTIONAL ACTIVATION; WOUND HEALING;

EID: 58149303264     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-01-0097     Document Type: Article

References (62)

1. Ahn, B. H., Kim, S. Y., Kim, E. H., Choi, K. S., Kwon, T. K., Lee, Y. H., Chang, J. S., Kim, M. S., Jo, Y. H., and Min, D. S. (2003). Transmodulation between phospholipase D and c-Src enhances cell proliferation. Mol. Cell. Biol. 23, 3103-3115.
2. Allen-Gipson, D. S., Wong, J., Spurzem, J. R., Sisson, J. H., and Wyatt, T. A. (2006). Adenosine A2A receptors promote adenosine-stimulated wound healing in bronchial epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L849-L855.
3. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
4. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C. J., McLauchlan, H., Klevernic, I., Arthur, J. S., Alessi, D. R., and Cohen, P. (2007). The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408, 297-315.
5. Bindschadler, M., and McGrath, J. L. (2007). Sheet migration by wounded monolayers as an emergent property of single-cell dynamics. J. Cell Sci. 120, 876-884.
6. Block, E. R., Matela, A. R., SundarRaj, N., Iszkula, E. R., and Klarlund, J. K. (2004). Wounding induces motility in sheets of corneal epithelial cells through loss of spatial constraints: role of heparin-binding epidermal growth factorlike growth factor signaling. J. Biol. Chem. 279, 24307-24312.
7. Bollag, W. B., Barrett, P. Q., Isales, C. M., Liscovitch, M., and Rasmussen, H. (1990). A potential role for phospholipase-D in the angiotensin-II-induced stimulation of aldosterone secretion from bovine adrenal glomerulosa cells. Endocrinology 127, 1436-1443.
8. Boucher, I., Yang, L., Mayo, C., Klepeis, V., and Trinkaus-Randall, V. (2007). Injury and nucleotides induce phosphorylation of epidermal growth factor receptor: MMP and HB-EGF dependent pathway. Exp. Eye Res. 85, 130-141.
9. Bours, M. J., Swennen, E. L., Di Virgilio, F., Cronstein, B. N., and Dagnelie, P. C. (2006). Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 112, 358-404.
10. Burnstock, G. (2006). Purinergic signalling-an overview. Novartis Found Symp. 276, 26-48 (discussion 48-57, 275-281).
11. Burnstock, G. (2007a). Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 87, 659 -797.
12. Burnstock, G. (2007b). Purine and pyrimidine receptors. Cell Mol. Life Sci. 64, 1471-1483.
13. Cazzolli, R., Shemon, A. N., Fang, M. Q., and Hughes, W. E. (2006). Phospholipid signalling through phospholipase D and phosphatidic acid. IUBMB Life 58, 457-461.
14. de Giorgi, V., Sestini, S., Massi, D., Ghersetich, I., and Lotti, T. (2007). Kera-tinocyte growth factor receptors. Dermatol. Clin. 25, 477-485, vii.
15. Dignass, A. U., Becker, A., Spiegler, S., and Goebell, H. (1998). Adenine nucleotides modulate epithelial wound healing in vitro. Eur. J. Clin. Invest. 28, 554-561.
16. el-Moatassim, C., and Dubyak, G. R. (1992). A novel pathway for the activation of phospholipase D by P2z purinergic receptors in BAC1.2F5 macro-phages. J. Biol. Chem. 267, 23664-23673.
17. Exton, J. H. (2002). Regulation of phospholipase D. FEBS Lett. 531, 58-61.
18. Farooqui, R., and Fenteany, G. (2005). Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement. J. Cell Sci. 118, 51-63.
19. Fenteany, G., Janmey, P. A., and Stossel, T. P. (2000). Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr. Biol. 10, 831-838.
20. Fini, M. E., and Stramer, B. M. (2005). How the cornea heals: cornea-specific repair mechanisms affecting surgical outcomes. Cornea 24, S2-S11.
21. Fischer, O. M., Hart, S., Gschwind, A., and Ullrich, A. (2003). EGFR signal transactivation in cancer cells. Biochem. Soc. Trans. 31, 1203-1208.
22. Gargett, C. E., Cornish, E. J., and Wiley, J. S. (1996). Phospholipase D activation by P2Z-purinoceptor agonists in human lymphocytes is dependent on bivalent cation influx. Biochem. J. 313(Pt 2), 529-535.
23. Gipson, I. K., Spurr-Michaud, S., Argueso, P., Tisdale, A., Ng, T. F., and Russo, C. L. (2003). Mucin gene expression in immortalized human corneal-limbal and conjunctival epithelial cell lines. Invest. Ophthalmol. Vis. Sci. 44, 2496-2506.
24. Hansen, L. A., Alexander, N., Hogan, M. E., Sundberg, J. P., Dlugosz, A., Threadgill, D. W., Magnuson, T., and Yuspa, S. H. (1997). Genetically null mice reveal a central role for epidermal growth factor receptor in the differentiation of the hair follicle and normal hair development. Am. J. Pathol. 150, 1959-1975.
25. Higashiyama, S., and Nanba, D. (2005). ADAM-mediated ectodomain shedding of HB-EGF in receptor cross-talk. Biochim. Biophys. Acta 1751, 110-117.
26. Jacinto, A., Martinez-Arias, A., and Martin, P. (2001). Mechanisms of epithelial fusion and repair. Nat. Cell Biol. 3, E117-E123.
27. Jane, S. M., Ting, S. B., and Cunningham, J. M. (2005). Epidermal impermeable barriers in mouse and fly. Curr. Opin. Genet. Dev. 15, 447-453.
28. Jang, A. C., Starz-Gaiano, M., and Montell, D. J. (2007). Modeling migration and metastasis in Drosophila. J. Mammary Gland Biol. Neoplasia 12, 103-114.
29. Jenkins, G. M., and Frohman, M. A. (2005). Phospholipase D: a lipid centric review. Cell Mol. Life Sci. 62, 2305-2316.
30. Katz, M., Amit, I., and Yarden, Y. (2007). Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim. Biophys. Acta 1773, 1161-1176.
31. 2+ waves in epithelial cells. J. Cell Sci. 114, 4185-4195.
32. Klepeis, V. E., Weinger, I., Kaczmarek, E., and Trinkaus-Randall, V. (2004). P2Y receptors play a critical role in epithelial cell communication and migration. J. Cell. Biochem. 93, 1115-1133.
33. Kusner, D. J., and Adams, J. (2000). ATP-induced killing of virulent Mycobacterium tuberculosis within human macrophages requires phospholipase D. J. Immunol. 164, 379-388.
34. Le Stunff, H., Auger, R., Kanellopoulos, J., and Raymond, M. N. (2004). The Pro-451 to Leu polymorphism within the C-terminal tail of P2X7 receptor impairs cell death but not phospholipase D activation in murine thymocytes. J. Biol. Chem. 279, 16918-16926.
35. Li, F., and Malik, K. U. (2005). Angiotensin II-induced Akt activation through the epidermal growth factor receptor in vascular smooth muscle cells is mediated by phospholipid metabolites derived by activation of phospho-lipase D. J. Pharmacol. Exp. Ther. 312, 1043-1054.
36. Liu, Y., Geisbuhler, B., and Jones, A. W. (1992). Activation of multiple mechanisms including phospholipase D by endothelin-1 in rat aorta. Am. J. Physiol. 262, C941-C949.
37. Martin, T. W., Feldman, D. R., Goldstein, K. E., and Wagner, J. R. (1989). Long-term phorbol ester treatment dissociates phospholipase D activation from phosphoinositide hydrolysis and prostacyclin synthesis in endothelial cells stimulated with bradykinin. Biochem. Biophys. Res. Commun. 165, 319-326.
38. Mazie, A. R., Spix, J. K., Block, E. R., Achebe, H. B., and Klarlund, J. K. (2006). Epithelial cell motility is triggered by activation of the EGF receptor through phosphatidic acid signaling. J. Cell Sci. 119, 1645-1654.
39. McDermott, M., Wakelam, M. J., and Morris, A. J. (2004). Phospholipase D. Biochem. Cell Biol. 82, 225-253.
40. McKay, M. M., and Morrison, D. K. (2007). Integrating signals from RTKs to ERK/MAPK. Oncogene 26, 3113-3121.
41. Netto, M. V., Mohan, R. R., Ambrosio, R., Jr., Hutcheon, A. E., Zieske, J. D., and Wilson, S. E. (2005). Wound healing in the cornea: a review of refractive surgery complications and new prospects for therapy. Cornea 24, 509-522.
42. Ohtsu, H., Dempsey, P. J., and Eguchi, S. (2006). ADAMs as mediators ofEGF receptor transactivation by G protein-coupled receptors. Am J. Physiol. Cell Physiol. 291, C1-C10.
43. Perez-Andres, E. et al. (2002). Activation of phospholipase D-2 by P2X(7) agonists in rat submandibular gland acini. J. Lipid Res. 43, 1244-1255.
44. Pochet, S., Gomez-Munoz, A., Marino, A., and Dehaye, J. P. (2003). Regulation of phospholipase D by P2X7 receptors in submandibular ductal cells. Cell Signal. 15, 927-935.
45. Raja, Sivamani, K., Garcia, M. S., and Isseroff, R. R. (2007). Wound re-epithelialization: modulating keratinocyte migration in wound healing. Front. Biosci. 12, 2849-2868.
46. Repertinger, S. K., Campagnaro, E., Fuhrman, J., El-Abaseri, T., Yuspa, S. H., and Hansen, L. A. (2004). EGFR enhances early healing after cutaneous incisional wounding. J. Invest. Dermatol. 123, 982-989.
47. Roskoski, R., Jr. (2005). Src kinase regulation by phosphorylation and dephos-phorylation. Biochem. Biophys. Res. Commun. 331, 1-14.
48. Rubinfeld, H., and Seger, R. (2005). The ERK cascade: a prototype of MAPK signaling. Mol. Biotechnol. 31, 151-174.
49. Sanderson, M. P., Dempsey, P. J., and Dunbar, A. J. (2006). Control of ErbB signaling through metalloprotease mediated ectodomain shedding of EGF-like factors. Growth Factors 24, 121-136.
50. Schmidt, B. T., Feduska, J. M., Witt, A. M., and Deasy, B. M. (2008). Robotic cell culture system for stem cell assays. Industrial Robot. 35, 116-124.
51. Sherratt, J. A., and Dallon, J. C. (2002). Theoretical models of wound healing: past successes and future challenges. CR Biol. 325, 557-564.
52. Sponsel, H. T., Breckon, R., and Anderson, R. J. (1995). Adenine nucleotide and protein kinase C regulation of renal tubular epithelial cell wound healing. Kidney Int. 48, 85-92.
53. 2+ influx and phospholipase D activities of a rat brain-derived type-2 astrocyte cell line, RBA-2, are mediated through P2X7 receptors. J. Neurochem. 73, 334-343.
54. van der Bend, R. L., de Widt, J., van Corven, E. J., Moolenaar, W. H., and van Blitterswijk, W. J. (1992). The biologically active phospholipid, lysophospha-tidic acid, induces phosphatidylcholine breakdown in fibroblasts via activation of phospholipase D. Comparison with the response to endothelin. Bio-chem. J. 285(Pt 1), 235-240.
55. Wesley, U. V., Bove, P. F., Hristova, M., McCarthy, S., and van der Vliet, A. (2007). Airway epithelial cell migration and wound repair by ATP-mediated activation of dual oxidase 1. J. Biol. Chem. 282, 3213-3220.
56. Xu, K. P., Ding, Y., Ling, J., Dong, Z., and Yu, F. S. (2004). Wound-induced HB-EGF ectodomain shedding and EGFR activation in corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 45, 813-820.
57. Xu, K. P., Yin, J., and Yu, F. S. (2006). SRC-family tyrosine kinases in wound-and ligand-induced epidermal growth factor receptor activation in human corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 47, 2832-2839.
58. Yang, L., Cranson, D., and Trinkaus-Randall, V. (2004). Cellular injury induces activation of MAPK via P2Y receptors. J. Cell. Biochem. 91, 938-950.
59. Yin, J., Xu, K., Zhang, J., Kumar, A., and Yu, F. S. (2007). Wound-induced ATP release and EGF receptor activation in epithelial cells. J. Cell Sci. 120, 815-825.
60. Zhang, Q., Thomas, S. M., Lui, V. W., Xi, S., Siegfried, J. M., Fan, H., Smithgall, T. E., Mills, G. B., and Grandis, J. R. (2006). Phosphorylation of TNF-alpha converting enzyme by gastrin-releasing peptide induces amphiregulin release and EGF receptor activation. Proc. Natl. Acad. Sci. USA 103, 6901-6906.
61. Zhang, Q., Thomas, S. M., Xi, S., Smithgall, T. E., Siegfried, J. M., Kamens, J., Gooding, W. E., and Grandis, J. R. (2004). SRC family kinases mediate epidermal growth factor receptor ligand cleavage, proliferation, and invasion of head and neck cancer cells. Cancer Res. 64, 6166-6173.
62. Zieske, J. D., Takahashi, H., Hutcheon, A. E., and Dalbone, A. C. (2000). Activation of epidermal growth factor receptor during corneal epithelial migration. Invest. Ophthalmol. Vis. Sci. 41, 1346-1355.