Ras activated ERK and PI3K pathways differentially affect directional movement of cultured fibroblasts

Cellular Physiology and Biochemistry

Volumn 31, Issue 1, 2013, Pages 123-142

  Sepe, Leandra ^a,b   Ferrari, Maria Carla ^a,b   Cantarella, Concita ^c   Fioretti, Francesca ^a   Paolella, Giovanni ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^c UNIVERSITY OF SALERNO   (Italy)

Author keywords

Directional migration; ERK; Ras; Wound healing

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN; RASV12 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL STRAIN 3T3; CONTROLLED STUDY; DIRECTIONAL CELL MIGRATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FIBROBLAST; FIBROBLAST CULTURE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING; VELOCITY; WOUND HEALING; CELL ASSAY; CELL TRACKING; EMBRYO; ENZYME INHIBITION; IMMUNOFLUORESCENCE; MICROSCOPY; MOUSE; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; WESTERN BLOTTING;

EID: 84873034877     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000343355     Document Type: Article

References (60)

1. Wennerberg K, Rossman KL, Der CJ: The ras superfamily at a glance. J Cell Sci 2005;118:843-846.
2. Rajalingam K, Schreck R, Rapp UR, Albert S: Ras oncogenes and their downstream targets. Biochim Biophys Acta 2007;1773:1177-1195.
3. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D: Ras oncogenes: Weaving a tumorigenic web. Nat Rev Cancer 2011;11:761-774.
4. Jemal A, Siegel R, Xu J, Ward E: Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
5. Schubbert S, Shannon K, Bollag G: Hyperactive ras in developmental disorders and cancer. Nat Rev Cancer 2007;7:295-308.
6. Muschel RJ, Williams JE, Lowy DR, Liotta LA: Harvey ras induction of metastatic potential depends upon oncogene activation and the type of recipient cell. Am J Pathol 1985;121:1-8.
7. Bondy GP, Wilson S, Chambers AF: Experimental metastatic ability of h-ras-transformed nih3t3 cells. Cancer Res 1985;45:6005-6009.
8. Greig RG, Koestler TP, Trainer DL, Corwin SP, Miles L, Kline T, Sweet R, Yokoyama S, Poste G: Tumorigenic and metastatic properties of "Normal" And ras-transfected nih/3t3 cells. Proc Natl Acad Sci U S A 1985;82:3698-3701.
9. Fujimoto K, Sheng H, Shao J, Beauchamp RD: Transforming growth factor-beta1 promotes invasiveness after cellular transformation with activated ras in intestinal epithelial cells. Exp Cell Res 2001;266:239-249.
10. Gildea JJ, Harding MA, Gulding KM, Theodorescu D: Transmembrane motility assay of transiently transfected cells by fluorescent cell counting and luciferase measurement. Biotechniques 2000;29:81-86.
11. Ueoka Y, Kato K, Kuriaki Y, Horiuchi S, Terao Y, Nishida J, Ueno H, Wake N: Hepatocyte growth factor modulates motility and invasiveness of ovarian carcinomas via ras-mediated pathway. Br J Cancer 2000;82:891-899.
12. Nguyen DH, Catling AD, Webb DJ, Sankovic M, Walker LA, Somlyo AV, Weber MJ, Gonias SL: Myosin light chain kinase functions downstream of ras/erk to promote migration of urokinase-type plasminogen activator-stimulated cells in an integrin-selective manner. J Cell Biol 1999;146:149-164.
13. Yip SC, El-Sibai M, Coniglio SJ, Mouneimne G, Eddy RJ, Drees BE, Neilsen PO, Goswami S, Symons M, Condeelis JS, Backer JM: The distinct roles of ras and rac in pi 3-kinase-dependent protrusion during egf-stimulated cell migration. J Cell Sci 2007;120:3138-3146.
14. Petrie RJ, Doyle AD, Yamada KM: Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 2009;10:538-549.
15. Jaeger S, Song Q, Chen SS: Dynamik: A software environment for cell dynamics, motility, and information tracking, with an application to ras pathways. Bioinformatics 2009;25:2383-2388.
16. Martens L, Monsieur G, Ampe C, Gevaert K, Vandekerckhove J: Cell-motility: A cross-platform, open source application for the study of cell motion paths. BMC Bioinformatics 2006;7:289.
17. DeNicola GM, Tuveson DA: Ras in cellular transformation and senescence. Eur J Cancer 2009;45:211-216.
18. Vial E, Sahai E, Marshall CJ: Erk-mapk signaling coordinately regulates activity of rac1 and rhoa for tumor cell motility. Cancer Cell 2003;4:67-79.
19. Cantarella C, Sepe L, Fioretti F, Ferrari MC, Paolella G: Analysis and modelling of motility of cell populations with motocell. BMC Bioinformatics 2009;10:S12.
20. Batschelet: Circular stastistics in biology. Academic Press, London UK, 1981
21. Mardia: Statistics of directional data. Academic Press, New York 1972
22. Kurten RC, Chowdhury P, Sanders RC Jr, Pittman LM, Sessions LW, Chambers TC, Lyle CS, Schnackenberg BJ, Jones SM: Coordinating epidermal growth factor-induced motility promotes efficient wound closure. Am J Physiol Cell Physiol 2005;288:C109-121.
23. Matsubayashi Y, Ebisuya M, Honjoh S, Nishida E: Erk activation propagates in epithelial cell sheets and regulates their migration during wound healing. Curr Biol 2004;14:731-735.
24. Bentley: Modelling circular data using a mixture of von mises and uniform distribution. Simon Fraser University 2006
25. Watson G: Goodness-of-fit tests on a circle. Biometrika 1961:109-114.
26. Tscharntke M, Pofahl R, Krieg T, Haase I: Ras-induced spreading and wound closure in human epidermal keratinocytes. FASEB J 2005;19:1836-1838.
27. Turchi L, Chassot AA, Rezzonico R, Yeow K, Loubat A, Ferrua B, Lenegrate G, Ortonne JP, Ponzio G: Dynamic characterization of the molecular events during in vitro epidermal wound healing. J Invest Dermatol 2002;119:56-63.
28. Tarnawski AS: Cellular and molecular mechanisms of gastrointestinal ulcer healing. Dig Dis Sci 2005;50:S24-33.
29. Behm B, Babilas P, Landthaler M, Schreml S: Cytokines, chemokines and growth factors in wound healing. J Eur Acad Dermatol Venereol 2012;26:812-820.
30. Nikolic DL, Boettiger AN, Bar-Sagi D, Carbeck JD, Shvartsman SY: Role of boundary conditions in an experimental model of epithelial wound healing. Am J Physiol Cell Physiol 2006;291:C68-75.
31. Giehl K: Oncogenic ras in tumour progression and metastasis. Biol Chem 2005;386:193-205.
32. Shima Y, Okamoto T, Aoyama T, Yasura K, Ishibe T, Nishijo K, Shibata KR, Kohno Y, Fukiage K, Otsuka S, Uejima D, Nakayama T, Nakamura T, Kiyono T, Toguchida J: In vitro transformation of mesenchymal stem cells by oncogenic h-rasval12. Biochem Biophys Res Commun 2007;353:60-66.
33. Sasaki AT, Chun C, Takeda K, Firtel RA: Localized ras signaling at the leading edge regulates pi3k, cell polarity and directional cell movement. J Cell Biol 2004;167:505-518.
34. Fitsialos G, Chassot AA, Turchi L, Dayem MA, LeBrigand K, Moreilhon C, Meneguzzi G, Busca R, Mari B, Barbry P, Ponzio G: Transcriptional signature of epidermal keratinocytes subjected to in vitro scratch wounding reveals selective roles for erk1/2, p38, and phosphatidylinositol 3-kinase signaling pathways. J Biol Chem 2007;282:15090-15102.
35. Tetreault MP, Chailler P, Beaulieu JF, Rivard N, Menard D: Epidermal growth factor receptor-dependent pi3k-activation promotes restitution of wounded human gastric epithelial monolayers. J Cell Physiol 2008;214:545-557.
36. Al-Shanti N, Faulkner SH, Saini A, Loram I, Stewart CE: A semi-automated programme for tracking myoblast migration following mechanical damage: Manipulation by chemical inhibitors. Cell Physiol Biochem 2011;27:625-636.
37. Krueger JS, Keshamouni VG, Atanaskova N, Reddy KB: Temporal and quantitative regulation of mitogen-activated protein kinase (mapk) modulates cell motility and invasion. Oncogene 2001;20:4209-4218.
38. McCawley LJ, Li S, Wattenberg EV, Hudson LG: Sustained activation of the mitogen-activated protein kinase pathway. A mechanism underlying receptor tyrosine kinase specificity for matrix metalloproteinase-9 induction and cell migration. J Biol Chem 1999;274:4347-4353.
39. Tian YC, Chen YC, Chang CT, Hung CC, Wu MS, Phillips A, Yang CW: Epidermal growth factor and transforming growth factor-beta1 enhance hk-2 cell migration through a synergistic increase of matrix metalloproteinase and sustained activation of erk signaling pathway. Exp Cell Res 2007;313:2367-2377.
40. Chen WL, Lin CT, Li JW, Hu FR, Chen CC: Erk1/2 activation regulates the wound healing process of rabbit corneal endothelial cells. Curr Eye Res 2009;34:103-111.
41. Teranishi S, Kimura K, Nishida T: Role of formation of an erk-fak-paxillin complex in migration of human corneal epithelial cells during wound closure in vitro. Invest Ophthalmol Vis Sci 2009;50:5646-5652.
42. Huang C, Jacobson K, Schaller MD: Map kinases and cell migration. J Cell Sci 2004;117:4619-4628.
43. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, Cheresh DA: Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 1997;137:481-492.
44. Wu WS, Wu JR, Hu CT: Signal cross talks for sustained mapk activation and cell migration: The potential role of reactive oxygen species. Cancer Metastasis Rev 2008;27:303-314.
45. Barros JC, Marshall CJ: Activation of either erk1/2 or erk5 map kinase pathways can lead to disruption of the actin cytoskeleton. J Cell Sci 2005;118:1663-1671.
46. Fincham VJ, James M, Frame MC, Winder SJ: Active erk/map kinase is targeted to newly forming cell-matrix adhesions by integrin engagement and v-src. EMBO J 2000;19:2911-2923.
47. Glading A, Bodnar RJ, Reynolds IJ, Shiraha H, Satish L, Potter DA, Blair HC, Wells A: Epidermal growth factor activates m-calpain (calpain ii), at least in part, by extracellular signal-regulated kinase-mediated phosphorylation. Mol Cell Biol 2004;24:2499-2512.
48. Gialeli C, Theocharis AD, Karamanos NK: Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J 2011;278:16-27.
49. Wilkins A, Insall RH: Small gtpases in dictyostelium: Lessons from a social amoeba. Trends Genet 2001;17:41-48.
50. Sasaki AT, Firtel RA: Finding the way: Directional sensing and cell polarization through ras signalling. Novartis Found Symp 2005;269:73-87; discussion 87-91, 223-230.
51. Zhang S, Charest PG, Firtel RA: Spatiotemporal regulation of ras activity provides directional sensing. Curr Biol 2008;18:1587-1593.
52. Cai H, Devreotes PN: Moving in the right direction: How eukaryotic cells migrate along chemical gradients. Semin Cell Dev Biol 2011;22:834-841.
53. Ferguson GJ, Milne L, Kulkarni S, Sasaki T, Walker S, Andrews S, Crabbe T, Finan P, Jones G, Jackson S, Camps M, Rommel C, Wymann M, Hirsch E, Hawkins P, Stephens L: Pi(3)kgamma has an important context-dependent role in neutrophil chemokinesis. Nat Cell Biol 2007;9:86-91.
54. Hoeller O, Kay RR: Chemotaxis in the absence of pip3 gradients. Curr Biol 2007;17:813-817.
55. Wessels D, Lusche DF, Kuhl S, Heid P, Soll DR: Pten plays a role in the suppression of lateral pseudopod formation during dictyostelium motility and chemotaxis. J Cell Sci 2007;120:2517-2531.
56. Bosgraaf L, Keizer-Gunnink I, Van Haastert PJ: Pi3-kinase signaling contributes to orientation in shallow gradients and enhances speed in steep chemoattractant gradients. J Cell Sci 2008;121:3589-3597.
57. Laird DJ, von Andrian UH, Wagers AJ: Stem cell trafficking in tissue development, growth, and disease. Cell 2008;132:612-630.
58. Wang F: The signaling mechanisms underlying cell polarity and chemotaxis. Cold Spring Harb Perspect Biol 2009;1:a002980.
59. Jin T, Xu X, Hereld D: Chemotaxis, chemokine receptors and human disease. Cytokine 2008;44:1-8.
60. Condeelis J, Singer RH, Segall JE: The great escape: When cancer cells hijack the genes for chemotaxis and motility. Annu Rev Cell Dev Biol 2005;21:695-718.