Opposite effects of PDGF-BB and prostaglandin E1 on cell-motility related processes are paralleled by modifications of distinct actin-binding proteins

Experimental Cell Research

Volumn 315, Issue 10, 2009, Pages 1745-1758

  van Wieringen, Tijs ^a   Kimani, Stanley G ^a   Hultgård Ekwall, Anna Karin ^a   Forsberg, Jens ^a   Reyhani, Vahid ^a   Engström, Åke ^a   Rubin, Kristofer ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Caldesmon; Collagen gel contraction; Cytoskeleton; ERK; Extracellular matrix; Fibroblast; Interstitial fluid pressure

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; COLLAGEN GEL; DODECYL SULFATE SODIUM; PLATELET DERIVED GROWTH FACTOR BB; PROSTAGLANDIN E1; TRITON X 100;

ANAPHYLAXIS; ARTICLE; CELL KINETICS; CELL MOTILITY; CELL SPREADING; CYTOSKELETON; FIBROBLAST; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; TISSUE PRESSURE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ACTINS; ALPROSTADIL; ANIMALS; CALMODULIN-BINDING PROTEINS; CATTLE; CELL ADHESION; CELL MOVEMENT; COLLAGEN; CYTOSKELETON; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GELS; GENE EXPRESSION PROFILING; HUMANS; MICROFILAMENT PROTEINS; MYOSIN-LIGHT-CHAIN KINASE; PHOSPHORYLATION; PHOSPHOSERINE; PLATELET-DERIVED GROWTH FACTOR; RECEPTORS, PROSTAGLANDIN E; RNA, MESSENGER; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 67349145276     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.02.005     Document Type: Article

References (62)

1. Aukland K., and Reed R.K. Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol. Rev. 73 (1993) 1-78
2. Wiig H., Rubin K., and Reed R.K. New and active role of the interstitium in control of interstitial fluid pressure: potential therapeutic consequences. Acta Anaesthesiol. Scand. 47 (2003) 111-121
3. 2α-analogs on collagen gel compaction in vitro and interstitial pressure in vivo. Am. J. Physiol. 274 (1998) H663-H671
4. Rodt S.A., Åhlén K., Berg A., Rubin K., and Reed R.K. A novel physiological function for platelet-derived growth factor-BB in rat dermis. J. Physiol. 495 (1996) 193-200
5. Heuchel R., Berg A., Tallquist M., Åhlen K., Reed R.K., Rubin K., Claesson-Welsh L., Heldin C.H., and Soriano P. Platelet-derived growth factor beta receptor regulates interstitial fluid homeostasis through phosphatidylinositol-3′ kinase signaling. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 11410-11415
6. 1 integrins. Circ. Res. (2006)
7. Åhlén K., Berg A., Stiger F., Tengholm A., Siegbahn A., Gylfe E., Reed R.K., and Rubin K. Cell interactions with collagen matrices in vivo and in vitro depend on phosphatidylinositol 3-kinase and free cytoplasmic calcium. Cell Adhes. Commun. 5 (1998) 461-473
8. Rhee S., and Grinnell F. P21-activated kinase 1: convergence point in PDGF- and LPA-stimulated collagen matrix contraction by human fibroblasts. J. Cell Biol. 172 (2006) 423-432
9. Rönnstrand L., and Heldin C.-H. Mechanisms of platelet-derived growth factor-induced chemotaxis. Int. J. Cancer 91 (2001) 757-762
10. Mellström K., Heldin C.-H., and Westermark B. Induction of circular membrane ruffling on human fibroblasts by platelet-derived growth factor. Exp. Cell Res. 177 (1988) 347-359
11. Baumgartner M., Sillman A.L., Blackwood E.M., Srivastava J., Madson N., Schilling J.W., Wright J.H., and Barber D.L. The Nck-interacting kinase phosphorylates ERM proteins for formation of lamellipodium by growth factors. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 13391-13396
12. Herman B., and Pledger W.J. Platelet-derived growth factor-induced alterations in vinculin and actin distribution in BALB/c-3T3 cells. J. Cell Biol. 100 (1985) 1031-1040
13. Tidball J.G., and Spencer M.J. PDGF stimulation induces phosphorylation of talin and cytoskeletal reorganization in skeletal muscle. J. Cell Biol. 123 (1993) 627-635
14. Åhlén K., Ring P., Tomasini-Johansson B., Holmqvist K., Magnusson K.E., and Rubin K. Platelet-derived growth factor-BB modulates membrane mobility of β1 integrins. Biochem. Biophys. Res. Commun. 314 (2004) 89-96
15. Rhee S., and Grinnell F. Fibroblast mechanics in 3D collagen matrices. Adv. Drug Dil. Rev. 59 (2007) 1299-1305
16. Tingström A., Heldin C.-H., and Rubin K. Regulation of fibroblast-mediated collagen gel contraction by platelet-derived growth factor, interleukin-1α and transforming growth factor-β1. J. Cell. Sci. 102 (1992) 315-322
17. 2 and NO acting through separate parallel pathways. Am. J. Resp. Cell Mol. Biol. 25 (2001) 245-253
18. Ehrlich H.P., and Wyler D.J. Fibroblast contraction of collagen lattices in vitro: inhibition by chronic inflammatory cell mediators. J. Cell. Physiol. 116 (1983) 345-351
19. Ehrlich H.P., Rockwell W.B., Cornwell T.L., and Rajaratnam J.B. Demonstration of a direct role for myosin light chain kinase in fibroblast-populated collagen lattice contraction. J. Cell. Physiol. 146 (1991) 1-7
20. Chen J.D., Kim J.P., Zhang K., Sarret Y., Wynn K.C., Kramer R.H., and Woodley D.T. Epidermal growth factor (EGF) promotes human keratinocyte locomotion on collagen by increasing the α2 integrin subunit. Exp. Cell Res. 209 (1993) 216-223
21. 1 integrin function. Circ. Res. 75 (1994) 942-948
22. Miekka S.I., Ingham K.C., and Menache D. Rapid methods for isolation of human plasma fibronectin. Thromb. Res. 27 (1982) 1-14
23. Schlötzer-Schrehardt U., Zenkel M., and Nusing R.M. Expression and localization of FP and EP prostanoid receptor subtypes in human ocular tissues. Invest. Ophthalmol. Vis. Sci. 43 (2002) 1475-1487
24. Kyveris A., Maruscak E., and Senchyna M. Optimization of RNA isolation from human ocular tissues and analysis of prostanoid receptor mRNA expression using RT-PCR. Mol. Vis. 8 (2002) 51-58
25. 1 integrin-mediated collagen gel contraction is stimulated by PDGF. Exp. Cell Res. 186 (1990) 264-272
26. Shevchenko A., Jensen O.N., Podtelejnikov A.V., Sagliocco F., Wilm M., Vorm O., Mortensen P., Shevchenko A., Boucherie H., and Mann M. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 14440-14445
27. Perkins D.N., Pappin D.J., Creasy D.M., and Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20 (1999) 3551-3567
28. Landegren U. Measurement of cell numbers by means of the endogenous enzyme hexosaminidase, applications to detection of lymphokines and cell surface antigens. J. Immnol. Methods 67 (1984) 379-388
29. Skuta G., Ho C.H., and Grinnell F. Increased myosin light chain phosphorylation is not required for growth factor stimulation of collagen matrix contraction. J. Biol. Chem. 274 (1999) 30163-30168
30. Posewitz M.C., and Tempst P. Immobilized Gallium(III) affinity chromatography of phosphopeptides. Anal. Chem. 71 (1999) 2883-2892
31. Tsukita S., and Yonemura S. Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J. Biol. Chem. 274 (1999) 34507-34510
32. Yamagata A., Kristensen D.B., Takeda Y., Miyamoto Y., Okada K., Inamatsu M., and Yoshizato K. Mapping of phosphorylated proteins on two-dimensional polyacrylamide gels using protein phosphatase. Proteomics 2 (2002) 1267-1276
33. Kordowska J., Huang R., and Wang C.L. Phosphorylation of caldesmon during smooth muscle contraction and cell migration or proliferation. J. Biomed. Sci. 13 (2006) 159-172
34. Hettasch J.M., and Sellers J.R. Caldesmon phosphorylation in intact human platelets by cAMP-dependent protein kinase and protein kinase C. J. Biol. Chem. 266 (1991) 11876-11881
35. Melton A.C., and Yee H.F. Hepatic stellate cell protrusions couple platelet-derived growth factor-BB to chemotaxis. Hepatology 45 (2007) 1446-1453
36. Clark R.A., Folkvord J.M., Hart C.E., Murray M.J., and McPherson J.M. Platelet isoforms of platelet-derived growth factor stimulate fibroblasts to contract collagen matrices. J. Clin. Invest. 84 (1989) 1036-1040
37. Berg A., Rubin K., and Reed R.K. Cytochalasin D induces edema formation and lowering of interstitial fluid pressure in rat dermis. Am. J. Physiol. Heart Circ. Physiol. 281 (2001) H7-13
38. Lidén Å., van Wieringen T., Lannergård J., Kassner A., Heinegård D., Reed R.K., Guss B., and Rubin K. A secreted collagen- and fibronectin-binding streptococcal protein modulates cell-mediated collagen gel contraction and interstitial fluid pressure. J. Biol. Chem. 283 (2008) 1234-1242
39. Kamio K., Liu X., Sugiura H., Togo S., Kobayashi T., Kawasaki S., Wang X., Mao L., Ahn Y., Hogaboam C., Toews M.L., and Rennard S.I. Prostacyclin analogs inhibit fibroblast contraction of collagen gels through the cAMP-PKA pathway. Am. J. Resp. Cell Mol. Biol. 37 (2007) 113-120
40. 2 mediated by an EP2/cAMP-dependent mechanism. Wound Repair Regen. 15 (2007) 390-398
41. Bastien L., Sawyer N., Grygorczyk R., Metters K.M., and Adam M. Cloning, functional expression, and characterization of the human prostaglandin E2 receptor EP2 subtype. J. Biol. Chem. 269 (1994) 11873-11877
42. 1 and its inhibition by L-epinephrine: mechanistic effects. J. Cycl. Nucl. Res. 8 (1982) 309-322
43. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83 (2003) 1325-1358
44. Murthy K.S. Signaling for contraction and relaxation in smooth muscle of the gut. Ann. Rev. Physiol. 68 (2006) 345-374
45. Halligan B.D., Ruotti V., Jin W., Laffoon S., Twigger S.N., and Dratz E.A. ProMoST (Protein Modification Screening Tool): a web-based tool for mapping protein modifications on two-dimensional gels. Nucleic Acids Res. 32 (2004) W638-644
46. Zhu K., Zhao J., Lubman D.M., Miller F.R., and Barder T.J. Protein pI shifts due to posttranslational modifications in the separation and characterization of proteins. Anal. Chem. 77 (2005) 2745-2755
47. Helfman D.M., Levy E.T., Berthier C., Shtutman M., Riveline D., Grosheva I., Lachish-Zalait A., Elbaum M., and Bershadsky A.D. Caldesmon inhibits nonmuscle cell contractility and interferes with the formation of focal adhesions. Mol. Biol. Cell 10 (1999) 3097-3112
48. Dabrowska R., Kulikova N., and Gagola M. Nonmuscle caldesmon: its distribution and involvement in various cellular processes. Protoplasma 224 (2004) 1-13
49. Marston S.B., Fraser I.D., and Huber P.A. Smooth muscle caldesmon controls the strong binding interaction between actin-tropomyosin and myosin. J. Biol. Chem. 269 (1994) 32104-32109
50. Yamboliev I.A., and Gerthoffer W.T. Modulatory role of ERK MAPK-caldesmon pathway in PDGF-stimulated migration of cultured pulmonary artery SMCs. Am. J. Physiol. 280 (2001) C1680-C1688
51. Foster D.B., Huang R., Hatch V., Craig R., Graceffa P., Lehman W., and Wang C.L. Modes of caldesmon binding to actin: sites of caldesmon contact and modulation of interactions by phosphorylation. J. Biol. Chem. 279 (2004) 53387-53394
52. Howe A.K. Regulation of actin-based cell migration by cAMP/PKA. Biochim. Biophys. Acta 1692 (2004) 159-174
53. Dykes A.C., and Wright G.L. Down-regulation of calponin destabilizes actin cytoskeletal structure in A7r5 cells. Can. J. Physiol. Pharm. 85 (2007) 225-232
54. Bretscher A., Reczek D., and Berryman M. Ezrin: a protein requiring conformational activation to link microfilaments to the plasma membrane in the assembly of cell surface structures. J. Cell. Sci. 110 (1997) 3011-3018
55. Bretscher A. Regulation of cortical structure by the ezrin-radixin-moesin protein family. Curr. Op Cell Biol. 11 (1999) 109-116
56. Auvinen E., Kivi N., and Vaheri A. Regulation of ezrin localization by Rac1 and PIPK in human epithelial cells. Exp. Cell Res. 313 (2007) 824-833
57. Urushidani T., Hanzel D.K., and Forte J.G. Protein phosphorylation associated with stimulation of rabbit gastric glands. Biochim. Biophys. Acta 930 (1987) 209-219
58. Chen J., Cohn J.A., and Mandel L.J. Dephosphorylation of ezrin as an early event in renal microvillar breakdown and anoxic injury. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 7495-7499
59. Ghosh M., Song X., Mouneimne G., Sidani M., Lawrence D.S., and Condeelis J.S. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304 (2004) 743-746
60. Hirayama A., Adachi R., Otani S., Kasahara T., and Suzuki K. Cofilin plays a critical role in IL-8-dependent chemotaxis of neutrophilic HL-60 cells through changes in phosphorylation. J. Leukoc. Biol. 81 (2007) 720-728
61. Huang T.Y., DerMardirossian C., and Bokoch G.M. Cofilin phosphatases and regulation of actin dynamics. Curr. Op Cell Biol. 18 (2006) 26-31
62. Nebl G., Fischer S., Penzel R., and Samstag Y. Dephosphorylation of cofilin is regulated through Ras and requires the combined activities of the Ras-effectors MEK and PI3K. Cell Signal. 16 (2004) 235-243