Vimentin is sufficient and required for wound repair and remodeling in alveolar epithelial cells

FASEB Journal

Volumn 25, Issue 11, 2011, Pages 3873-3883

  Rogel, Micah R ^a,b   Soni, Pritin N ^b   Troken, James R ^b   Sitikov, Albert ^b   Trejo, Humberto E ^b   Ridge, Karen M ^b,c,d  

^a Northwestern University   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

Intermediate filaments; Lung injury; Migration; Scratch wound assay; TGF 1

Indexed keywords

ADENOVIRUS VECTOR; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INTERMEDIATE FILAMENT PROTEIN; LUCIFERASE; MESSENGER RNA; SHORT HAIRPIN RNA; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VIMENTIN;

5' UNTRANSLATED REGION; ACUTE LUNG INJURY; ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE RELEASE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; MALE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; WOUND CLOSURE; WOUND HEALING;

ANIMALS; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; MALE; PULMONARY ALVEOLI; RATS; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA1; VIMENTIN; WOUND HEALING;

EID: 80355129706     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-170795     Document Type: Article

References (52)

1. Uhal, B. D. (1997) Cell cycle kinetics in the alveolar epithelium. Am. J. Physiol. Lung Cell. Mol. Physiol. 272, L1031-L1045
2. Zahm, J. M., Chevillard, M., and Puchelle, E. (1991) Wound repair of human surface respiratory epithelium. Am. J. Respir. Cell Mol. Biol. 5, 242-248
3. Adamson, I. Y., Hedgecock, C., and Bowden, D. H. (1990) Epithelial cell-fibroblast interactions in lung injury and repair. Am. J. Pathol. 137, 385-392 (Pubitemid 20232999)
4. Lesur, O., Arsalane, K., and Lane, D. (1996) Lung alveolar epithelial cell migration in vitro: modulators and regulation processes. Am. J. Physiol. Lung Cell. Mol. Physiol. 270, L311-L319
5. Kheradmand, F., Folkesson, H. G., Shum, L., Derynk, R., Pytela, R., and Matthay, M. A. (1994) Transforming growth factor-alpha enhances alveolar epithelial cell repair in a new in vitro model. Am. J. Physiol. Lung Cell. Mol. Physiol. 267, L728-L738
6. Buisson, A. C., Gilles, C., Polette, M., Zahm, J. M., Birembaut, P., and Tournier, J. M. (1996) Wound repair-induced expression of a stromelysins is associated with the acquisition of a mesenchymal phenotype in human respiratory epithelial cells. Lab. Invest. 74, 658-669 (Pubitemid 26105728)
7. Gilles, C., Polette, M., Zahm, J. M., Tournier, J. M., Volders, L., Foidart, J. M., and Birembaut, P. (1999) Vimentin contributes to human mammary epithelial cell migration. J. Cell Sci. 112, 4615-4625 (Pubitemid 30034810)
8. SundarRaj, N., Rizzo, J. D., Anderson, S. C., and Gesiotto, J. P. (1992) Expression of vimentin by rabbit corneal epithelial cells during wound repair. Cell Tissue Res. 267, 347-356
9. Willis, B. C., Liebler, J. M., Luby-Phelps, K., Nicholson, A. G., Crandall, E. D., du Bois, R. M., and Borok, Z. (2005) Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am. J. Pathol. 166, 1321-1332 (Pubitemid 40586504)
10. Boyer, B., Valles, A. M., and Edme, N. (2000) Induction and regulation of epithelial-mesenchymal transitions. Biochem. Pharmacol. 60, 1091-1099
11. Dennler, S., Goumans, M. J., and ten Dijke, P. (2002) Transforming growth factor beta signal transduction. J. Leukoc. Biol. 71, 731-740
12. Bierie, B., and Moses, H. L. (2006) TGF-beta and cancer. Cytokine Growth Factor Rev. 17, 29-40
13. Siegel, P. M., and Massague, J. (2003) Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat. Rev. Cancer 3, 807-821
14. Bergeron, A., Soler, P., Kambouchner, M., Loiseau, P., Milleron, B., Valeyre, D., Hance, A. J., and Tazi, A. (2003) Cytokine profiles in idiopathic pulmonary fibrosis suggest an important role for TGF-β and IL-10. Eur. Respir. J. 22, 69-76 (Pubitemid 36896473)
15. Dhainaut, J. F., Charpentier, J., and Chiche, J. D. (2003) Transforming growth factor-beta: a mediator of cell regulation in acute respiratory distress syndrome. Crit. Care Med. 31, S258-S264 (Pubitemid 36458177)
16. Khalil, N., Corne, S., Whitman, C., and Yacyshyn, H. (1996) Plasmin regulates the activation of cell-associated latent TGFbeta 1 secreted by rat alveolar macrophages after in vivo bleomycin injury. Am. J. Respir. Cell Mol. Biol. 15, 252-259 (Pubitemid 126439878)
17. Khalil, N., O'Connor, R. N., Flanders, K. C., and Unruh, H. (1996) TGF-beta 1, but not TGF-beta 2 or TGF-beta 3, is differentially present in epithelial cells of advanced pulmonary fibrosis: an immunohistochemical study. Am. J. Respir. Cell Mol. Biol. 14, 131-138 (Pubitemid 126441385)
18. Sime, P. J., Xing, Z., Graham, F. L., Csaky, K. G., and Gauldie, J. (1997) Adenovector-mediated gene transfer of active transforming growth factor-beta1 induces prolonged severe fibrosis in rat lung. J. Clin. Invest. 100, 768-776 (Pubitemid 27371693)
19. Pittet, J. F., Griffiths, M. J., Geiser, T., Kaminski, N., Dalton, S. L., Huang, X., Brown, L. A., Gotwals, P. J., Koteliansky, V. E., Matthay, M. A., and Sheppard, D. (2001) TGF-beta is a critical mediator of acute lung injury. J. Clin. Invest. 107, 1537-1544 (Pubitemid 32574640)
20. Bonniaud, P., Kolb, M., Galt, T., Robertson, J., Robbins, C., Stampfli, M., Lavery, C., Margetts, P. J., Roberts, A. B., and Gauldie, J. (2004) Smad3 null mice develop airspace enlargement and are resistant to TGF-beta-mediated pulmonary fibrosis. J. Immunol. 173, 2099-2108 (Pubitemid 38971648)
21. Sivaramakrishnan, S., DeGiulio, J. V., Lorand, L., Goldman, R. D., and Ridge, K. M. (2008) Micromechanical properties of keratin intermediate filament networks. Proc. Natl. Acad. Sci. U. S. A. 105, 889-894 (Pubitemid 351282051)
22. Sivaramakrishnan, S., Schneider, J. L., Sitikov, A., Goldman, R. D., and Ridge, K. M. (2009) Shear stress induced reorganization of the keratin intermediate filament network requires phosphorylation by protein kinase C zeta. Mol. Biol. Cell 20, 2755-2765
23. Ridge, K. M., Linz, L., Flitney, F. W., Kuczmarski, E. R., Chou, Y. H., Omary, M. B., Sznajder, J. I., and Goldman, R. D. (2005) Keratin 8 phosphorylation by protein kinase C delta regulates shear stress-mediated disassembly of keratin intermediate filaments in alveolar epithelial cells. J. Biol. Chem. 280, 30400-30405 (Pubitemid 41216223)
24. Yoon, K. H., Yoon, M., Moir, R. D., Khuon, S., Flitney, F. W., and Goldman, R. D. (2001) Insights into the dynamic properties of keratin intermediate filaments in living epithelial cells. J. Cell Biol. 153, 503-516 (Pubitemid 34280138)
25. Prahlad, V., Yoon, M., Moir, R. D., Vale, R. D., and Goldman, R. D. (1998) Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J. Cell Biol. 143, 159-170 (Pubitemid 28480525)
26. Yoon, M., Moir, R. D., Prahlad, V., and Goldman, R. D. (1998) Motile properties of vimentin intermediate filament networks in living cells. J. Cell Biol. 143, 147-157 (Pubitemid 28480524)
27. Eriksson, J. E., He, T., Trejo-Skalli, A. V., Harmala-Brasken, A. S., Hellman, J., Chou, Y. H., and Goldman, R. D. (2004) Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J. Cell Sci. 117, 919-932 (Pubitemid 38386949)
28. Liang, C. C., Park, A. Y., and Guan, J. L. (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat. Protoc. 2, 329-333 (Pubitemid 47040047)
29. Wu, Y., Zhang, X., Salmon, M., Lin, X., and Zehner, Z. E. (2007) TGFbeta1 regulation of vimentin gene expression during differentiation of the C2C12 skeletal myogenic cell line requires Smads, AP-1 and Sp1 family members. Biochim. Biophys. Acta 1773, 427-439 (Pubitemid 46275072)
30. Eckes, B., Colucci-Guyon, E., Smola, H., Nodder, S., Babinet, C., Krieg, T., and Martin, P. (2000) Impaired wound healing in embryonic and adult mice lacking vimentin. J. Cell Sci. 113, 2455-2462 (Pubitemid 30601362)
31. Eckes, B., Dogic, D., Colucci-Guyon, E., Wang, N., Maniotis, A., Ingber, D., Merckling, A., Langa, F., Aumailley, M., Delouvee, A., Koteliansky, V., Babinet, C., and Krieg, T. (1998) Impaired mechanical stability, migration and contractile capacity in vimentin- deficient fibroblasts. J. Cell Sci. 111, 1897-1907 (Pubitemid 28370534)
32. Brown, M. J., Hallam, J. A., Colucci-Guyon, E., and Shaw, S. (2001) Rigidity of circulating lymphocytes is primarily conferred by vimentin intermediate filaments. J. Immunol. 166, 6640-6646 (Pubitemid 32467205)
33. Mendez, M. G., Kojima, S., and Goldman, R. D. (2009) Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition. FASEB J. 24, 1838-1851
34. Godsel, L. M., Hsieh, S. N., Amargo, E. V., Bass, A. E., Pascoe- McGillicuddy, L. T., Huen, A. C., Thorne, M. E., Gaudry, C. A., Park, J. K., Myung, K., Goldman, R. D., Chew, T. L., and Green, K. J. (2005) Desmoplakin assembly dynamics in four dimensions: multiple phases differentially regulated by intermediate filaments and actin. J. Cell Biol. 171, 1045-1059 (Pubitemid 41815836)
35. Bhattacharya, R., Gonzalez, A. M., Debiase, P. J., Trejo, H. E., Goldman, R. D., Flitney, F. W., and Jones, J. C. (2009) Recruitment of vimentin to the cell surface by beta3 integrin and plectin mediates adhesion strength. J. Cell Sci. 122, 1390-1400
36. Barberis, L., Pasquali, C., Bertschy-Meier, D., Cuccurullo, A., Costa, C., Ambrogio, C., Vilbois, F., Chiarle, R., Wymann, M., Altruda, F., Rommel, C., and Hirsch, E. (2009) Leukocyte transmigration is modulated by chemokine-mediated PI3Kgamma-dependent phosphorylation of vimentin. Eur. J. Immunol. 39, 1136-1146
37. Goto, H., Tanabe, K., Manser, E., Lim, L., Yasui, Y., and Inagaki, M. (2002) Phosphorylation and reorganization of vimentin by p21-activated kinase (PAK). Genes Cells 7, 91-97 (Pubitemid 34213355)
38. Li, Q. F., Spinelli, A. M., Wang, R., Anfinogenova, Y., Singer, H. A., and Tang, D. D. (2006) Critical role of vimentin phosphorylation at Ser-56 by p21-activated kinase in vimentin cytoskeleton signaling. J. Biol. Chem. 281, 34716-34724 (Pubitemid 46036677)
39. Dumont, N., Bakin, A. V., and Arteaga, C. L. (2003) Autocrine transforming growth factor-beta signaling mediates Smad-independent motility in human cancer cells. J. Biol. Chem. 278, 3275-3285 (Pubitemid 36801240)
40. Tian, F., Byfield, S. D., Parks, W. T., Stuelten, C. H., Nemani, D., Zhang, Y. E., and Roberts, A. B. (2004) Smad-binding defective mutant of transforming growth factor beta type I receptor enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res. 64, 4523-4530 (Pubitemid 38856924)
41. Liu, I. M., Schilling, S. H., Knouse, K. A., Choy, L., Derynck, R., and Wang, X. F. (2009) TGFbeta-stimulated Smad1/5 phosphorylation requires the ALK5 L45 loop and mediates the pro-migratory TGFbeta switch. EMBO J. 28, 88-98
42. Berthiaume, Y., Lesur, O., and Dagenais, A. (1999) Treatment of adult respiratory distress syndrome: plea for rescue therapy of the alveolar epithelium. Thorax 54, 150-160 (Pubitemid 29101361)
43. Geiser, T., Jarreau, P. H., Atabai, K., and Matthay, M. A. (2000) Interleukin-1beta augments in vitro alveolar epithelial repair. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, L1184-L1190 (Pubitemid 32009504)
44. Howat, W. J., Holgate, S. T., and Lackie, P. M. (2002) TGF-beta isoform release and activation during in vitro bronchial epithelial wound repair. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L115-L123 (Pubitemid 34654188)
45. 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 (Pubitemid 40277104)
46. Savla, U., Olson, L. E., and Waters, C. M. (2004) Mathematical modeling of airway epithelial wound closure during cyclic mechanical strain. J. Appl. Physiol. 96, 566-574 (Pubitemid 38140158)
47. Draper, B. K., Komurasaki, T., Davidson, M. K., and Nanney, L. B. (2003) Epiregulin is more potent than EGF or TGFalpha in promoting in vitro wound closure due to enhanced ERK/ MAPK activation. J. Cell. Biochem. 89, 1126-1137 (Pubitemid 36959380)
48. Ware, L. B., and Matthay, M. A. (2000) The acute respiratory distress syndrome. N. Engl. J. Med. 342, 1334-1349 (Pubitemid 30408719)
49. Singh, A., Greninger, P., Rhodes, D., Koopman, L., Violette, S., Bardeesy, N., and Settleman, J. (2009) A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 15, 489-500
50. Thaiparambil, J. T., Bender, L., Ganesh, T., Kline, E., Patel, P., Liu, Y., Tighiouart, M., Vertino, P. M., Harvey, R. D., Garcia, A., and Marcus, A. I. (2011) Withaferin A inhibits breast cancer invasion and metastasis at sub-cytotoxic doses by inducing vimentin disassembly and serine 56 phosphorylation. [E-pub ahead of print] Int. J. Cancer doi: 10.1002/ijc.25938
51. Bargagna-Mohan, P., Paranthan, R. R., Hamza, A., Dimova, N., Trucchi, B., Srinivasan, C., Elliott, G. I., Zhan, C. G., Lau, D. L., Zhu, H., Kasahara, K., Inagaki, M., Cambi, F., and Mohan, R. Withaferin A targets intermediate filaments glial fibrillary acidic protein and vimentin in a model of retinal gliosis. J. Biol. Chem. 285, 7657-7669
52. Bargagna-Mohan, P., Hamza, A., Kim, Y. E., Khuan Abby Ho, Y., Mor-Vaknin, N., Wendschlag, N., Liu, J., Evans, R. M., Markovitz, D. M., Zhan, C. G., Kim, K. B., and Mohan, R. (2007) The tumor inhibitor and antiangiogenic agent withaferin A targets the intermediate filament protein vimentin. Chem. Biol. 14, 623-634 (Pubitemid 46920982)