The small GTPase N-Ras regulates extracellular matrix synthesis, proliferation and migration in fibroblasts

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 2734-2744

  Fuentes Calvo, Isabel ^a,b   Crespo, Piero ^c   Santos, Eugenio ^a   López Novoa, José M ^a,b   Martínez Salgado, Carlos ^a,b,d  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b INSTITUTO DE INVESTIGACIÓN BIOMÉDICA DE SALAMANCA IBSAL   (Spain)

^c UNIVERSITY OF CANTABRIA   (Spain)

^d HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

Author keywords

MEK ERK 1 2; PI3K Akt; Ras proteins; Renal fibrosis; Transforming growth factor 1

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; FIBROBLAST; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 84882784817     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.07.008     Document Type: Article

References (73)

1. Barbacid M. Ras genes. Annu. Rev. Biochem. 1987, 56:779-827.
2. Dhanasekaran N., Premkumar Reddy E. Signaling by dual specificity kinases. Oncogene 1998, 17:1447-1455.
3. Kerkhoff E., Rapp U.R. Cell cycle targets of Ras/Raf signalling. Oncogene 1998, 17:1457-1462.
4. Barbacid M. Ras oncogenes: their role in neoplasia. Eur. J. Clin. Investig. 1990, 20:225-235.
5. Santos E., Tronick S.R., Aaronson S.A., Pulciani S., Barbacid M. T24 human bladder carcinoma oncogene is an activated form of the normal human homologue of BALB- and Harvey-MSV transforming genes. Nature 1982, 298:343-347.
6. Leon J., Guerrero I., Pellicer A. Differential expression of the ras gene family in mice. Mol. Cell. Biol. 1987, 7:1535-1540.
7. Furth M.E., Aldrich T.H., Cordon-Cardo C. Expression of ras proto-oncogene proteins in normal human tissues. Oncogene 1987, 1:47-58.
8. Prior I.A., Hancock J.F. Compartmentalization of Ras proteins. J. Cell Sci. 2001, 114:1603-1608.
9. Hancock J.F., Cadwallader K., Paterson H., Marshall C.J. A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO J. 1991, 10:4033-4039.
10. Roy S., Luetterforst R., Harding A., Apolloni A., Etheridge M., Stang E., Rolls B., Hancock J.F., Parton R.G. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1999, 1:98-105.
11. Roy S., Plowman S., Rotblat B., Prior I.A., Muncke C., Grainger S., Parton R.G., Henis Y.I., Kloog Y., Hancock J.F. Individual palmitoyl residues serve distinct roles in H-ras trafficking, microlocalization, and signaling. Mol. Cell. Biol. 2005, 25:6722-6733.
12. Castellano E., Santos E. Functional specificity of ras isoforms: so similar but so different. Genes Cancer 2011, 2:216-231.
13. Calvo F., Agudo-Ibanez L., Crespo P. The Ras-ERK pathway: understanding site-specific signaling provides hope of new anti-tumor therapies. Bioessays 2010, 32:412-421.
14. Arozarena I., Calvo F., Crespo P. Ras, an actor on many stages: posttranslational modifications, localization, and site-specified events. Genes Cancer 2011, 2:182-194.
15. Takai Y., Sasaki T., Matozaki T. Small GTP-binding proteins. Physiol. Rev. 2001, 81:153-208.
16. Wellbrock C., Karasarides M., Marais R. The RAF proteins take centre stage. Nat. Rev. 2004, 5:875-885.
17. Cantley L.C. The phosphoinositide 3-kinase pathway. Science (New York, N.Y.) 2002, 296:1655-1657.
18. Blobe G.C., Schiemann W.P., Lodish H.F. Role of transforming growth factor beta in human disease. N. Engl. J. Med. 2000, 342:1350-1358.
19. Branton M.H., Kopp J.B. TGF-beta and fibrosis. Microbes Infect. 1999, 1:1349-1365.
20. Alcock R.A., Dey S., Chendil D., Inayat M.S., Mohiuddin M., Hartman G., Chatfield L.K., Gallicchio V.S., Ahmed M.M. Farnesyltransferase inhibitor (L-744,832) restores TGF-beta type II receptor expression and enhances radiation sensitivity in K-ras mutant pancreatic cancer cell line MIA PaCa-2. Oncogene 2002, 21:7883-7890.
21. Iglesias M., Frontelo P., Gamallo C., Quintanilla M. Blockade of Smad4 in transformed keratinocytes containing a Ras oncogene leads to hyperactivation of the Ras-dependent Erk signalling pathway associated with progression to undifferentiated carcinomas. Oncogene 2000, 19:4134-4145.
22. Kretzschmar M., Doody J., Timokhina I., Massague J. A mechanism of repression of TGFbeta/Smad signaling by oncogenic Ras. Genes Dev. 1999, 13:804-816.
23. Haberstroh U., Zahner G., Disser M., Thaiss F., Wolf G., Stahl R.A. TGF-beta stimulates rat mesangial cell proliferation in culture: role of PDGF beta-receptor expression. Am. J. Physiol. 1993, 264:F199-F205.
24. Matsuzaki K. Modulation of TGF-beta signaling during progression of chronic liver diseases. Front. Biosci. 2009, 14:2923-2934.
25. Colicelli J. Human RAS superfamily proteins and related GTPases. Sci. STKE 2004, 2004:RE13.
26. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 2003, 3:11-22.
27. Rojas A., Padidam M., Cress D., Grady W.M. TGF-beta receptor levels regulate the specificity of signaling pathway activation and biological effects of TGF-beta. Biochim. Biophys. Acta 2009, 1793:1165-1173.
28. Castellano E., Downward J. RAS interaction with PI3K: more than just another effector pathway. Genes Cancer 2011, 2:261-274.
29. Castellano E., Downward J. Role of RAS in the regulation of PI 3-kinase. Curr. Top. Microbiol. Immunol. 2010, 346:143-169.
30. Grande M.T., Lopez-Novoa J.M. Fibroblast activation and myofibroblast generation in obstructive nephropathy. Nat. Rev. Nephrol. 2009, 5:319-328.
31. Hutchison N., Fligny C., Duffield J.S. Resident mesenchymal cells and fibrosis. Biochim. Biophys. Acta 2013, 1832:962-971.
32. Fuentes-Calvo I., Blazquez-Medela A.M., Eleno N., Santos E., Lopez-Novoa J.M., Martinez-Salgado C. H-Ras isoform modulates extracellular matrix synthesis, proliferation, and migration in fibroblasts. Am. J. Physiol. 2011, 302:C686-C697.
33. Martinez-Salgado C., Fuentes-Calvo I., Garcia-Cenador B., Santos E., Lopez-Novoa J.M. Involvement of H- and N-Ras isoforms in transforming growth factor-beta1-induced proliferation and in collagen and fibronectin synthesis. Exp. Cell Res. 2006, 312:2093-2106.
34. Fotiadou P.P., Takahashi C., Rajabi H.N., Ewen M.E. Wild-type NRas and KRas perform distinct functions during transformation. Mol. Cell. Biol. 2007, 27:6742-6755.
35. Grande M.T., Fuentes-Calvo I., Arevalo M., Heredia F., Santos E., Martinez-Salgado C., Rodriguez-Puyol D., Nieto M.A., Lopez-Novoa J.M. Deletion of H-Ras decreases renal fibrosis and myofibroblast activation following ureteral obstruction in mice. Kidney Int. 2010, 77:509-518.
36. Esteban L.M., Vicario-Abejon C., Fernandez-Salguero P., Fernandez-Medarde A., Swaminathan N., Yienger K., Lopez E., Malumbres M., McKay R., Ward J.M., Pellicer A., Santos E. Targeted genomic disruption of H-ras and N-ras, individually or in combination, reveals the dispensability of both loci for mouse growth and development. Mol. Cell. Biol. 2001, 21:1444-1452.
37. Montero A., Rodriguez-Barbero A., Lopez-Novoa J.M. A role for platelet-activating factor in endothelin-1-induced rat mesangial cell proliferation. Eur. J. Pharmacol. 1993, 243:235-240.
38. Bryant R.J., Banks P.M., O'Malley D.P. Ki67 staining pattern as a diagnostic tool in the evaluation of lymphoproliferative disorders. Histopathology 2006, 48:505-515.
39. Cortes P., Riser B.L., Asano K., Rodriguez-Barbero A., Narins R.G., Yee J. Effects of oral antihyperglycemic agents on extracellular matrix synthesis by mesangial cells. Kidney Int. 1998, 54:1985-1998.
40. Matallanas D., Arozarena I., Berciano M.T., Aaronson D.S., Pellicer A., Lafarga M., Crespo P. Differences on the inhibitory specificities of H-Ras, K-Ras, and N-Ras (N17) dominant negative mutants are related to their membrane microlocalization. J. Biol. Chem. 2003, 278:4572-4581.
41. Gerdes J., Lemke H., Baisch H., Wacker H.H., Schwab U., Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 1984, 133:1710-1715.
42. Kelman Z. PCNA: structure, functions and interactions. Oncogene 1997, 14:629-640.
43. Rajalingam K., Schreck R., Rapp U.R., Albert S. Ras oncogenes and their downstream targets. Biochim. Biophys. Acta 2007, 1773:1177-1195.
44. Stites E.C., Ravichandran K.S. A systems perspective of ras signaling in cancer. Clin. Cancer Res. 2009, 15:1510-1513.
45. Rodriguez-Pena A.B., Grande M.T., Eleno N., Arevalo M., Guerrero C., Santos E., Lopez-Novoa J.M. Activation of Erk1/2 and Akt following unilateral ureteral obstruction. Kidney Int. 2008, 74:196-209.
46. Rodriguez-Pena A.B., Santos E., Arevalo M., Lopez-Novoa J.M. Activation of small GTPase Ras and renal fibrosis. J. Nephrol. 2005, 18:341-349.
47. Eddy A.A. Progression in chronic kidney disease. Adv. Chronic Kidney Dis. 2005, 12:353-365.
48. Liu Y. Cellular and molecular mechanisms of renal fibrosis. Nat. Rev. Nephrol. 2011, 7:684-696.
49. Slack J.L., Parker M.I., Robinson V.R., Bornstein P. Regulation of collagen I gene expression by ras. Mol. Cell. Biol. 1992, 12:4714-4723.
50. Hall A., Marshall C.J., Spurr N.K., Weiss R.A. Identification of transforming gene in two human sarcoma cell lines as a new member of the ras gene family located on chromosome 1. Nature 1983, 303:396-400.
51. Rasheed S., Nelson-Rees W.A., Toth E.M., Arnstein P., Gardner M.B. Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 1974, 33:1027-1033.
52. Brenner K.A., Corbett S.A., Schwarzbauer J.E. Regulation of fibronectin matrix assembly by activated Ras in transformed cells. Oncogene 2000, 19:3156-3163.
53. Chandler L.A., Bourgeois S. Posttranscriptional down-regulation of fibronectin in N-ras-transformed cells. Cell Growth Differ. 1991, 2:379-384.
54. Ivarsson M., McWhirter A., Borg T.K., Rubin K. Type I collagen synthesis in cultured human fibroblasts: regulation by cell spreading, platelet-derived growth factor and interactions with collagen fibers. Matrix Biol. 1998, 16:409-425.
55. Reddy V.S., Harskamp R.E., van Ginkel M.W., Calhoon J., Baisden C.E., Kim I.S., Valente A.J., Chandrasekar B. Interleukin-18 stimulates fibronectin expression in primary human cardiac fibroblasts via PI3K-Akt-dependent NF-kappaB activation. J. Cell. Physiol. 2008, 215:697-707.
56. Ricupero D.A., Poliks C.F., Rishikof D.C., Cuttle K.A., Kuang P.P., Goldstein R.H. Phosphatidylinositol 3-kinase-dependent stabilization of alpha1(I) collagen mRNA in human lung fibroblasts. Am. J. Physiol. 2001, 281:C99-C105.
57. Winbanks C.E., Grimwood L., Gasser A., Darby I.A., Hewitson T.D., Becker G.J. Role of the phosphatidylinositol 3-kinase and mTOR pathways in the regulation of renal fibroblast function and differentiation. Int. J. Biochem. Cell Biol. 2007, 39:206-219.
58. Weber K.S., Ostermann G., Zernecke A., Schroder A., Klickstein L.B., Weber C. Dual role of H-Ras in regulation of lymphocyte function antigen-1 activity by stromal cell-derived factor-1alpha: implications for leukocyte transmigration. Mol. Biol. Cell 2001, 12:3074-3086.
59. Cunliffe I.A., Rees R.C., Rennie I.G. The effect of TGF-beta 1 and TGF-beta 2 on the proliferation of human Tenon's capsule fibroblasts in tissue culture. Acta Ophthalmol. Scand. 1996, 74:31-35.
60. Kay E.P., Lee M.S., Seong G.J., Lee Y.G. TGF-beta s stimulate cell proliferation via an autocrine production of FGF-2 in corneal stromal fibroblasts. Curr. Eye Res. 1998, 17:286-293.
61. Kay E.P., Lee H.K., Park K.S., Lee S.C. Indirect mitogenic effect of transforming growth factor-beta on cell proliferation of subconjunctival fibroblasts. Investig. Ophthalmol. Vis. Sci. 1998, 39:481-486.
62. Werner H., Roberts C.T. The IGFI receptor gene: a molecular target for disrupted transcription factors. Genes Chromosomes Cancer 2003, 36:113-120.
63. Valluru M., Staton C.A., Reed M.W., Brown N.J. Transforming growth factor-beta and endoglin signaling orchestrate wound healing. Front. Physiol. 2011, 2:89.
64. Grande M.T., Arevalo M., Nunez A., Cannata-Andia J.B., Santos E., Lopez-Novoa J.M. Targeted genomic disruption of H-ras and N-ras has no effect on early renal changes after unilateral ureteral ligation. World J. Urol. 2009, 27:787-797.
65. Ishida T., Haneda M., Maeda S., Koya D., Kikkawa R. Stretch-induced overproduction of fibronectin in mesangial cells is mediated by the activation of mitogen-activated protein kinase. Diabetes 1999, 48:595-602.
66. Jiang M.D., Zheng S.M., Xu H., Zeng W.Z., Zhang Y., Sun H.P., Wang Y.X., Qin J.P., Wu X.L. An experimental study of extracellular signal-regulated kinase and its interventional treatments in hepatic fibrosis. Hepatobiliary Pancreat. Dis. Int. 2008, 7:51-57.
67. Matthiesen S., Bahulayan A., Holz O., Racke K. MAPK pathway mediates muscarinic receptor-induced human lung fibroblast proliferation. Life Sci. 2007, 80:2259-2262.
68. Kahan C., Seuwen K., Meloche S., Pouyssegur J. Coordinate, biphasic activation of p44 mitogen-activated protein kinase and S6 kinase by growth factors in hamster fibroblasts. Evidence for thrombin-induced signals different from phosphoinositide turnover and adenylylcyclase inhibition. J. Biol. Chem. 1992, 267:13369-13375.
69. Pumiglia K.M., Decker S.J. Cell cycle arrest mediated by the MEK/mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:448-452.
70. Qui M.S., Green S.H. PC12 cell neuronal differentiation is associated with prolonged p21ras activity and consequent prolonged ERK activity. Neuron 1992, 9:705-717.
71. Roovers K., Assoian R.K. Integrating the MAP kinase signal into the G1 phase cell cycle machinery. Bioessays 2000, 22:818-826.
72. Kim S.E., Lee W.J., Choi K.Y. The PI3 kinase-Akt pathway mediates Wnt3a-induced proliferation. Cell. Signal. 2007, 19:511-518.
73. Kim C.S., Kim J.K., Nam S.Y., Yang K.H., Jeong M., Kim H.S., Kim C.S., Jin Y.W., Kim J. Low-dose radiation stimulates the proliferation of normal human lung fibroblasts via a transient activation of Raf and Akt. Mol. Cells 2007, 24:424-430.