Dual modes of motility at the leading edge of migrating epithelial cell sheets

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 39, 2012, Pages 15799-15804

  Klarlund, Jes K ^a  

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

Author keywords

Cell extrusion; Cell migration; Cell motility; Corneal epithelium; Wound healing

Indexed keywords

ACTIN; AGAROSE; EPIDERMAL GROWTH FACTOR RECEPTOR; MYOSIN IIA;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DAMAGE; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CELL SHEET; CELL STRUCTURE; CONTROLLED STUDY; DIGESTION; EPITHELIUM CELL; FINGER; GROWTH INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STIMULUS;

CELL MOVEMENT; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; RECEPTOR, EPIDERMAL GROWTH FACTOR; WOUND HEALING;

EID: 84866885006     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1210992109     Document Type: Article

References (62)

1. Fini ME, Stramer BM (2005) How the cornea heals: Cornea-specific repair mechanisms affecting surgical outcomes. Cornea 24(8 Suppl):S2-S11. (Pubitemid 41688549)
2. Gurtner GC, Werner S, Barrandon Y, Longaker MT (2008) Wound repair and regeneration. Nature 453:314-321. (Pubitemid 351693137)
3. Farooqui R, 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. (Pubitemid 40277104)
4. Bugyi B, Carlier MF (2010) Control of actin filament treadmilling in cell motility. Annu Rev Biophys 39:449-470.
5. Ridley AJ (2011) Life at the leading edge. Cell 145:1012-1022.
6. Martin P, Lewis J (1992) Actin cables and epidermal movement in embryonic wound healing. Nature 360:179-183.
7. Bement WM, Forscher P, Mooseker MS (1993) A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J Cell Biol 121:565-578. (Pubitemid 23131268)
8. Garcia-Fernandez B, Campos I, Geiger J, Santos AC, Jacinto A (2009) Epithelial resealing. Int J Dev Biol 53:1549-1556.
9. Danjo Y, Gipson IK (1998) Actin 'purse string' filaments are anchored by E-cadherin-mediated adherens junctions at the leading edge of the epithelial wound, providing coordinated cell movement. J Cell Sci 111:3323-3332. (Pubitemid 28563035)
10. Redd MJ, Cooper L, Wood W, Stramer B, Martin P (2004) Wound healing and inflammation: Embryos reveal the way to perfect repair. Philos Trans R Soc Lond B Biol Sci 359:777-784. (Pubitemid 38673745)
11. Bullen TF, et al. (2006) Characterization of epithelial cell shedding from human small intestine. Lab Invest 86:1052-1063. (Pubitemid 44423069)
12. Hantash BM, Zhao L, Knowles JA, Lorenz HP (2008) Adult and fetal wound healing. Front Biosci 13:51-61. (Pubitemid 351594762)
13. Buchanan EP, Longaker MT, Lorenz HP (2009) Fetal skin wound healing. Adv Clin Chem 48:137-161.
14. Rosenblatt J, Raff MC, Cramer LP (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11:1847-1857. (Pubitemid 33136524)
15. Russo JM, et al. (2005) Distinct temporal-spatial roles for rho kinase and myosin light chain kinase in epithelial purse-string wound closure. Gastroenterology 128: 987-1001. (Pubitemid 40523549)
16. Tamada M, Perez TD, Nelson WJ, Sheetz MP (2007) Two distinct modes of myosin assembly and dynamics during epithelial wound closure. J Cell Biol 176:27-33. (Pubitemid 46041677)
17. Puddicombe SM, et al. (2000) Involvement of the epidermal growth factor receptor in epithelial repair in asthma. FASEB J 14:1362-1374. (Pubitemid 30439745)
18. Tokumaru S, et al. (2000) Ectodomain shedding of epidermal growth factor receptor ligands is required for keratinocyte migration in cutaneous wound healing. J Cell Biol 151:209-220.
19. Xu KP, Ding Y, Ling J, Dong Z, Yu FS (2004) Wound-induced HB-EGF ectodomain shedding and EGFR activation in corneal epithelial cells. Invest Ophthalmol Vis Sci 45: 813-820. (Pubitemid 38868376)
20. Block ER, Matela AR, SundarRaj N, Iszkula ER, Klarlund JK (2004) Wounding induces motility in sheets of corneal epithelial cells through loss of spatial constraints: Role of heparin-binding epidermal growth factor-like growth factor signaling. J Biol Chem 279:24307-24312. (Pubitemid 38725293)
21. Myhre GM, Toruner M, Abraham S, Egan LJ (2004) Metalloprotease disintegrin-mediated ectodomain shedding of EGFR ligands promotes intestinal epithelial restitution. Am J Physiol Gastrointest Liver Physiol 287:G1213-G1219. (Pubitemid 39551852)
22. Boucher I, Yang L, Mayo C, Klepeis V, 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. (Pubitemid 47017273)
23. Block ER, et al. (2010) Free edges in epithelial cell sheets stimulate epidermal growth factor receptor signaling. Mol Biol Cell 21:2172-2181.
24. Omelchenko T, Vasiliev JM, Gelfand IM, Feder HH, Bonder EM (2003) Rho-dependent formation of epithelial "leader" cells during wound healing. Proc Natl Acad Sci USA 100:10788-10793. (Pubitemid 37140106)
25. Poujade M, et al. (2007) Collective migration of an epithelial monolayer in response to a model wound. Proc Natl Acad Sci USA 104:15988-15993. (Pubitemid 350099346)
26. Gipson IK, et al. (2003) Mucin gene expression in immortalized human corneal-limbal and conjunctival epithelial cell lines. Invest Ophthalmol Vis Sci 44:2496-2506. (Pubitemid 36618406)
27. Aktories K, Wilde C, Vogelsgesang M (2004) Rho-modifying C3-like ADP-ribosyltransferases. Rev Physiol Biochem Pharmacol 152:1-22. (Pubitemid 44417934)
28. Kovács M, Tóth J, Hetényi C, Málnási- Csizmadia A, Sellers JR (2004) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279:35557-35563. (Pubitemid 39100557)
29. Brock J, Midwinter K, Lewis J, Martin P (1996) Healing of incisional wounds in the embryonic chick wing bud: Characterization of the actin purse-string and demonstration of a requirement for Rho activation. J Cell Biol 135:1097-1107. (Pubitemid 26403781)
30. Danjo Y, Gipson IK (2002) Specific transduction of the leading edge cells of migrating epithelia demonstrates that they are replaced during healing. Exp Eye Res 74: 199-204. (Pubitemid 34948395)
31. Ellis AG, et al. (2006) Preclinical analysis of the analinoquinazoline AG1478, a specific small molecule inhibitor of EGF receptor tyrosine kinase. Biochem Pharmacol 71: 1422-1434.
32. Block ER, Klarlund JK (2008) Wounding sheets of epithelial cells activates the epidermal growth factor receptor through distinct short- and long-range mechanisms. Mol Biol Cell 19:4909-4917.
33. Favata MF, et al. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273:18623-18632. (Pubitemid 28334795)
34. Bain J, et al. (2007) The selectivity of protein kinase inhibitors: A further update. Biochem J 408:297-315.
35. Curran T, Bravo R, Müller R (1985) Transient induction of c-fos and c-myc in an immediate consequence of growth factor stimulation. Cancer Surv 4:655-681.
36. Rollins BJ, Stiles CD (1988) Regulation of c-myc and c-fos proto-oncogene expression by animal cell growth factors. In Vitro Cell Dev Biol 24:81-84. (Pubitemid 18098045)
37. Johnson GR, Kannan B, Shoyab M, Stromberg K (1993) Amphiregulin induces tyrosine phosphorylation of the epidermal growth factor receptor and p185erbB2. Evidence that amphiregulin acts exclusively through the epidermal growth factor receptor at the surface of human epithelial cells. J Biol Chem 268:2924-2931. (Pubitemid 23057930)
38. Chrisman CA (2010) Care of chronic wounds in palliative care and end-of-life patients. Int Wound J 7:214-235.
39. Markova A, Mostow EN (2012) US skin disease assessment: Ulcer and wound care. Dermatol Clin 30:107-111, ix.
40. Jaalouk DE, Lammerding J (2009) Mechanotransduction gone awry. Nat Rev Mol Cell Biol 10:63-73.
41. Mammoto A, Ingber DE (2009) Cytoskeletal control of growth and cell fate switching. Curr Opin Cell Biol 21:864-870.
42. Wang N, Tytell JD, Ingber DE (2009) Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10:75-82.
43. Vogel V, Sheetz MP (2009) Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways. Curr Opin Cell Biol 21:38-46.
44. Kolahi KS, Mofrad MR (2010) Mechanotransduction: A major regulator of homeostasis and development. Wiley Interdiscip Rev Syst Biol Med 2:625- 639.
45. Cai Y, Sheetz MP (2009) Force propagation across cells: Mechanical coherence of dynamic cytoskeletons. Curr Opin Cell Biol 21:47-50.
46. Howard J (2009) Mechanical signaling in networks of motor and cytoskeletal proteins. Annu Rev Biophys 38:217-234.
47. Schwartz MA (2010) Integrins and extracellular matrix in mechanotransduction. Cold Spring Harb Perspect Biol 2:a005066.
48. Moore SW, Roca-Cusachs P, Sheetz MP (2010) Stretchy proteins on stretchy substrates: The important elements of integrin-mediated rigidity sensing. Dev Cell 19:194-206.
49. Sachs F (2010) Stretch-activated ion channels: What are they? Physiology (Bethesda) 25:50-56.
50. Gu Y, Forostyan T, Sabbadini R, Rosenblatt J (2011) Epithelial cell extrusion requires the sphingosine-1-phosphate receptor 2 pathway. J Cell Biol 193:667-676.
51. Belacortu Y, Paricio N (2011) Drosophila as a model of wound healing and tissue regeneration in vertebrates. Dev Dyn 240:2379-2404.
52. Gorfinkiel N, Schamberg S, Blanchard GB (2011) Integrative approaches to morphogenesis: Lessons from dorsal closure. Genesis 49:522-533.
53. Fenteany G, Janmey PA, Stossel TP (2000) Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr Biol 10:831-838. (Pubitemid 30597202)
54. Tambe DT, et al. (2011) Collective cell guidance by cooperative intercellular forces. Nat Mater 10:469-475.
55. Trepat X, Fredberg JJ (2011) Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol 21:638-646.
56. Singh AB, Harris RC (2005) Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal 17:1183- 1193.
57. Yoshioka J, et al. (2005) Cardiomyocyte hypertrophy and degradation of connexin43 through spatially restricted autocrine/paracrine heparin-binding EGF. Proc Natl Acad Sci USA 102:10622-10627. (Pubitemid 41061604)
58. Higashiyama S, et al. (2008) Membrane-anchored growth factors, the epidermal growth factor family: Beyond receptor ligands. Cancer Sci 99:214-220. (Pubitemid 351228472)
59. Bindschadler M, McGrath JL (2007) Sheet migration by wounded monolayers as an emergent property of single-cell dynamics. J Cell Sci 120:876-884. (Pubitemid 46523489)
60. Ouaknin GY, Bar-Yoseph PZ (2009) Stochastic collective movement of cells and fingering morphology: No maverick cells. Biophys J 97:1811-1821.
61. Mark S, et al. (2010) Physical model of the dynamic instability in an expanding cell culture. Biophys J 98:361-370.
62. Angelini TE, et al. (2011) Glass-like dynamics of collective cell migration. Proc Natl Acad Sci USA 108:4714-4719.