Quantitative phosphoproteomic analysis of signaling downstream of the prostaglandin E2/G-protein coupled receptor in human synovial fibroblasts: Potential antifibrotic networks

Journal of Proteome Research

Volumn 13, Issue 11, 2014, Pages 5262-5280

  Gerarduzzi, Casimiro ^a,b   He, Qingwen ^b   Antoniou, John ^c   Di Battista, John A ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b ROYAL VICTORIA HOSPITAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

cell signaling; phosphosubstrate; Prostaglandin E2; synovial fibroblasts

Indexed keywords

CELL PROTEIN; G PROTEIN COUPLED RECEPTOR; ICOSANOID; PHOSPHOPROTEIN; PROSTAGLANDIN E2; PROTEIN KINASE; SERINE; THREONINE; CYCLIC AMP DEPENDENT PROTEIN KINASE;

AMINO ACID SEQUENCE; ARTICLE; CELL MIGRATION; CELL MOTILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA SEQUENCE; DOWN REGULATION; FIBROBLAST; FOCAL ADHESION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; ADULT; CELL MOTION; CYTOLOGY; CYTOSKELETON; DRUG EFFECTS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PROCEDURES; SIGNAL TRANSDUCTION; SYNOVIUM;

ADULT; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL MOVEMENT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSKELETON; DINOPROSTONE; FIBROBLASTS; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOMICS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SYNOVIAL MEMBRANE;

EID: 84908884857     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500495s     Document Type: Article

References (81)

1. Wynn, T. A. Cellular and molecular mechanisms of fibrosis J. Pathol. 2008, 214 (2) 199-210
2. Desmoulière, A.; Chaponnier, C.; Gabbiani, G. Tissue repair, contraction, and the myofibroblast Wound Repair Regen. 2005, 13 (1) 7-12
3. Narumiya, S.; Sugimoto, Y.; Ushikubi, F. Prostanoid receptors: structures, properties, and functions Physiol. Rev. 1999, 79 (4) 1193-1226
4. Funk, C. D. Prostaglandins and leukotrienes: advances in eicosanoid biology Science 2001, 294 (5548) 1871-1875
5. Wilborn, J.; Crofford, L. J.; Burdick, M. D.; Kunkel, S. L.; Strieter, R. M.; Peters-Golden, M. Cultured lung fibroblasts isolated from patients with idiopathic pulmonary fibrosis have a diminished capacity to synthesize prostaglandin E2 and to express cyclooxygenase-2 J. Clin. Invest. 1995, 95 (4) 1861-1868
6. Vancheri, C.; Sortino, M. A.; Tomaselli, V.; Mastruzzo, C.; Condorelli, F.; Bellistrí, G.; Pistorio, M. P.; Canonico, P. L.; Crimi, N. Different expression of TNF-alpha receptors and prostaglandin E(2) Production in normal and fibrotic lung fibroblasts: potential implications for the evolution of the inflammatory process Am. J. Respir. Cell Mol. Biol. 2000, 22 (5) 628-634
7. Keerthisingam, C. B.; Jenkins, R. G.; Harrison, N. K.; Hernandez-Rodriguez, N. A.; Booth, H.; Laurent, G. J.; Hart, S. L.; Foster, M. L.; McAnulty, R. J. Cyclooxygenase-2 deficiency results in a loss of the anti-proliferative response to transforming growth factor-beta in human fibrotic lung fibroblasts and promotes bleomycin-induced pulmonary fibrosis in mice Am. J. Pathol. 2001, 158 (4) 1411-1422
8. Charbeneau, R. P.; Christensen, P. J.; Chrisman, C. J.; Paine, R.; Toews, G. B.; Peters-Golden, M.; Moore, B. B. Impaired synthesis of prostaglandin E2 by lung fibroblasts and alveolar epithelial cells from GM-CSF-/-mice: implications for fibroproliferation Am. J. Physiol.: Lung Cell. Mol. Physiol. 2003, 284 (6) L1103-L1111
9. Hodges, R. J.; Jenkins, R. G.; Wheeler-Jones, C. P.; Copeman, D. M.; Bottoms, S. E.; Bellingan, G. J.; Nanthakumar, C. B.; Laurent, G. J.; Hart, S. L.; Foster, M. L.; McAnulty, R. J. Severity of lung injury in cyclooxygenase-2-deficient mice is dependent on reduced prostaglandin E(2) production Am. J. Pathol. 2004, 165 (5) 1663-1676
10. Peters-Golden, M.; Bailie, M.; Marshall, T.; Wilke, C.; Phan, S. H.; Toews, G. B.; Moore, B. B. Protection from pulmonary fibrosis in leukotriene-deficient mice Am. J. Respir. Crit. Care Med. 2002, 165 (2) 229-235
11. White, E. S.; Atrasz, R. G.; Dickie, E. G.; Aronoff, D. M.; Stambolic, V.; Mak, T. W.; Moore, B. B.; Peters-Golden, M. Prostaglandin E(2) inhibits fibroblast migration by E-prostanoid 2 receptor-mediated increase in PTEN activity Am. J. Respir. Cell Mol. Biol. 2005, 32 (2) 135-141
12. Kolodsick, J. E.; Peters-Golden, M.; Larios, J.; Toews, G. B.; Thannickal, V. J.; Moore, B. B. Prostaglandin E2 inhibits fibroblast to myofibroblast transition via E. prostanoid receptor 2 signaling and cyclic adenosine monophosphate elevation Am. J. Respir. Cell Mol. Biol. 2003, 29 (5) 537-544
13. Moore, B. B.; Ballinger, M. N.; White, E. S.; Green, M. E.; Herrygers, A. B.; Wilke, C. A.; Toews, G. B.; Peters-Golden, M. Bleomycin-induced E prostanoid receptor changes alter fibroblast responses to prostaglandin E2 J. Immunol. 2005, 174 (9) 5644-5649
14. Borok, Z.; Gillissen, A.; Buhl, R.; Hoyt, R. F.; Hubbard, R. C.; Ozaki, T.; Rennard, S. I.; Crystal, R. G. Augmentation of functional prostaglandin E levels on the respiratory epithelial surface by aerosol administration of prostaglandin E Am. Rev. Respir. Dis. 1991, 144 (5) 1080-1084
15. Faour, W. H.; Alaaeddine, N.; Mancini, A.; He, Q. W.; Jovanovic, D.; Di Battista, J. A. Early growth response factor-1 mediates prostaglandin E2-dependent transcriptional suppression of cytokine-induced tumor necrosis factor-alpha gene expression in human macrophages and rheumatoid arthritis-affected synovial fibroblasts J. Biol. Chem. 2005, 280, 9536-9546
16. Zhai, B.; Yang, H.; Mancini, A.; He, Q. W.; Antoniou, J.; Di Battista, J. A. Leukotriene B(4) BLT receptor signaling regulates the level and stability of cyclooxygenase-2 (COX-2) mRNA through restricted activation of Ras/Raf/ERK/p42 AUF1 pathway J. Biol. Chem. 2010, 285, 23568-23580
17. 2 inhibits human lung fibroblast chemotaxis through disparate actions on different E-prostanoid receptors Am. J. Respir. Cell Mol. Biol. 2011, 44 (1) 99-107
18. Buckley, C. D.; Pilling, D.; Lord, J. M.; Akbar, A. N.; Scheel-Toellner, D.; Salmon, M. Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation Trends Immunol. 2001, 22 (4) 199-204
19. Strutz, F.; Okada, H.; Lo, C. W.; Danoff, T.; Carone, R. L.; Tomaszewski, J. E.; Neilson, E. G. Identification and characterization of a fibroblast marker: FSP1 J. Cell Biol. 1995, 130 (2) 393-405
20. Zimmermann, T.; Kunisch, E.; Pfeiffer, R.; Hirth, A.; Stahl, H. D.; Sack, U.; Laube, A.; Liesaus, E.; Roth, A.; Palombo-Kinne, E.; Emmrich, F.; Kinne, R. W. Isolation and characterization of rheumatoid arthritis synovial fibroblasts from primary culture-primary culture cells markedly differ from fourth-passage cells Arthritis Res. 2001, 3 (1) 72-76
21. Rush, J.; Moritz, A.; Lee, K. A.; Guo, A.; Goss, V. L.; Spek, E. J.; Zhang, H.; Zha, X. M.; Polakiewicz, R. D.; Comb, M. J. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells Nat. Biotechnol. 2004, 23 (1) 94-101
22. Stokes, M. P.; Rush, J.; Macneill, J.; Ren, J. M.; Sprott, K.; Nardone, J.; Yang, V.; Beausoleil, S. A.; Gygi, S. P.; Livingstone, M.; Zhang, H.; Polakiewicz, R. D.; Comb, M. J. Profiling of UV-induced ATM/ATR signaling pathways Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (50) 19855-19860
23. Rikova, K.; Guo, A.; Zeng, Q.; Possemato, A.; Yu, J.; Haack, H.; Nardone, J.; Lee, K.; Reeves, C.; Li, Y.; Hu, Y.; Tan, Z.; Stokes, M.; Sullivan, L.; Mitchell, J.; Wetzel, R.; Macneill, J.; Ren, J. M.; Yuan, J.; Bakalarski, C. E.; Villen, J.; Kornhauser, J. M.; Smith, B.; Li, D.; Zhou, X.; Gygi, S. P.; Gu, T. L.; Polakiewicz, R. D.; Rush, J.; Comb, M. J. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer Cell 2007, 131 (6) 1190-1203
24. Moritz, A.; Li, Y.; Guo, A.; Villén, J.; Wang, Y.; MacNeill, J.; Kornhauser, J.; Sprott, K.; Zhou, J.; Possemato, A.; Ren, J. M.; Hornbeck, P.; Cantley, L. C.; Gygi, S. P.; Rush, J.; Comb, M. J. Akt-RSK-S6 kinase signaling networks activated by oncogenic receptor tyrosine kinases Sci. Signal. 2010, 3 (136) ra64
25. Gnad, F.; Young, A.; Zhou, W.; Lyle, K.; Ong, C. C.; Stokes, M. P.; Silva, J. C.; Belvin, M.; Friedman, L. S.; Koeppen, H.; Minden, A.; Hoeflich, K. P. Systems-wide analysis of K-Ras, Cdc42, and PAK4 signaling by quantitative phosphoproteomics Mol. Cell. Proteomics 2013, 12 (8) 2070-2080
26. Bonnette, P. C.; Robinson, B. S.; Silva, J. C.; Stokes, M. P.; Brosius, A. D.; Baumann, A.; Buckbinder, L. Phosphoproteomic characterization of PYK2 signaling pathways involved in osteogenesis J. Proteomics 2010, 73 (7) 1306-1320
27. Brave, S. R.; Ratcliffe, K.; Wilson, Z.; James, N. H.; Ashton, S.; Wainwright, A.; Kendrew, J.; Dudley, P.; Broadbent, N.; Sproat, G.; Taylor, S.; Barnes, C.; Silva, J. C.; Farnsworth, C. L.; Hennequin, L.; Ogilvie, D. J.; Jürgensmeier, J. M.; Shibuya, M.; Wedge, S. R.; Barry, S. T. Assessing the activity of cediranib, a VEGFR-2/3 tyrosine kinase inhibitor, against VEGFR-1 and members of the structurally related PDGFR family Mol. Cancer Ther. 2011, 10 (5) 861-873
28. Stokes, M. P.; Farnsworth, C. L.; Moritz, A.; Silva, J. C.; Jia, X.; Lee, K. A.; Guo, A.; Polakiewicz, R. D.; Comb, M. J. PTMScan direct: identification and quantification of peptides from critical signaling proteins by immunoaffinity enrichment coupled with LC-MS/MS Mol. Cell. Proteomics 2012, 11 (5) 187-201
29. Guo, A.; Gu, H.; Zhou, J.; Mulhern, D.; Wang, Y.; Lee, K. A.; Yang, V.; Aguiar, M.; Kornhauser, J.; Jia, X.; Ren, J.; Beausoleil, S. A.; Silva, J. C.; Vemulapalli, V.; Bedford, M. T.; Comb, M. J. Immunoaffinity enrichment and mass spectrometry analysis of protein methylation Mol. Cell. Proteomics 2014, 13 (1) 372-387
30. Kartberg, F.; Asp, L.; Dejgaard, S. Y.; Smedh, M.; Fernandez-Rodriguez, J.; Nilsson, T.; Presley, J. F. ARFGAP2 and ARFGAP3 are essential for COPI coat assembly on the Golgi membrane of living cells J. Biol. Chem. 2010, 285 (47) 36709-36720
31. Huang, S. Y.; Tsai, M. L.; Chen, G. Y.; Wu, C. J.; Chen, S. H. A systematic MS-based approach for identifying in vitro substrates of PKA and PKG in rat uteri J. Proteome Res. 2007, 6, 2674-2684
32. Michl, P.; Knobel, B.; Downward, J. CUTL1 is phosphorylated by protein kinase A, modulating its effects on cell proliferation and motility J. Biol. Chem. 2006, 281, 15138-15144
33. Jay, D.; García, E. J.; de la Luz Ibarra, M. In situ determination of a PKA phosphorylation site in the C-terminal region of filamin Mol. Cell. Biochem. 2004, 260, 49-53
34. Edwards, H. V.; Scott, J. D.; Baillie, G. S. The A-kinase-anchoring protein AKAP-Lbc facilitates cardioprotective PKA phosphorylation of Hsp20 on Ser16 Biochem. J. 2012, 446, 437-443
35. Palmer, D.; Jimmo, S. L.; Raymond, D. R.; Wilson, L. S.; Carter, R. L.; Maurice, D. H. Protein kinase A phosphorylation of human phosphodiesterase 3B promotes 14-3-3 protein binding and inhibits phosphatase-catalyzed inactivation J. Biol. Chem. 2007, 282, 9411-9419
36. Terunuma, M.; Jang, I. S.; Ha, S. H.; Kittler, J. T.; Kanematsu, T.; Jovanovic, J. N.; Nakayama, K. I.; Akaike, N.; Ryu, S. H.; Moss, S. J.; Hirata, M. GABAA receptor phospho-dependent modulation is regulated by phospholipase C-related inactive protein type 1, a novel protein phosphatase 1 anchoring protein J. Neurosci. 2004, 24, 7074-7084
37. Aboulaich, N.; Chui, P. C.; Asara, J. M.; Flier, J. S.; Maratos-Flier, E. Polymerase I and Transcript Release Factor Regulates Lipolysis via a Phosphorylation-Dependent Mechanism Diabetes 2011, 60, 757-765
38. Smith, F. D.; Samelson, B. K.; Scott, J. D. Discovery of cellular substrates for protein kinase A using a peptide array screening protocol Biochem. J. 2011, 438, 103-110
39. Yang, L.; Qiao, G.; Ying, H.; Zhang, J.; Yin, F. TCR-induced Akt serine 473 phosphorylation is regulated by protein kinase C-alpha Biochem. Biophys. Res. Commun. 2010, 400, 16-20
40. Flotow, H.; Thomas, G. Substrate recognition determinants of the mitogen-activated 70K S6 kinase from rat liver J. Biol. Chem. 1992, 267, 3074-3078
41. Gerarduzzi, C.; He, Q. W.; Antoniou, J.; Di Battista, J. A. Prostaglandin E2-Dependent Blockade of Actomyosin and Stress Fiber Formation Is Mediated Through S1379 Phosphorylation of ROCK2 J. Cell Biochem. 2014, 115 (9) 1516-1527
42. Howe, A. K. Regulation of actin-based cell migration by cAMP/PKA Biochim. Biophys. Acta 2004, 1692 (2-3) 159-174
43. Grønborg, M.; Kristiansen, T. Z.; Stensballe, A.; Andersen, J. S.; Ohara, O.; Mann, M.; Jensen, O. N.; Pandey, A. A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies: identification of a novel protein, Frigg, as a protein kinase A substrate Mol. Cell. Proteomics 2002, 1 (7) 517-527
44. Antoine-Bertrand, J.; Ghogha, A.; Luangrath, V.; Bedford, F. K.; Lamarche-Vane, N. The activation of ezrin-radixin-moesin proteins is regulated by netrin-1 through Src kinase and RhoA/Rho kinase activities and mediates netrin-1-induced axon outgrowth Mol. Biol. Cell 2011, 19, 3734-3746
45. Wang, Y.; Waldron, R. T.; Dhaka, A.; Patel, A.; Riley, M. M.; Rozengurt, E.; Colicelli, J. The RAS effector RIN1 directly competes with RAF and is regulated by 14-3-3 proteins Mol. Cell. Biol. 2002, 22 (3) 916-926
46. Kim, M. S.; Lee, E. J.; Kim, H. R.; Moon, A. p38 Kinase is a key signaling molecule for H-Ras-induced cell motility and invasive phenotype in human breast epithelial cells Cancer Res. 2003, 63, 5454-5461
47. Tscharntke, M.; Pofahl, R.; Krieg, T.; Haase, I. Ras-induced spreading and wound closure in human epidermal keratinocytes FASEB J. 2005, 19 (13) 1836-1838
48. Kim, E. S.; Kim, M. S.; Moon, A. Transforming growth factor (TGF)-beta in conjunction with H-ras activation promotes malignant progression of MCF10A breast epithelial cells Cytokine 2005, 29 (2) 84-91
49. Derynck, R.; Akhurst, R. J.; Balmain, A. TGF-beta signaling in tumor suppression and cancer progression Nat. Genet. 2001, 29, 117-129
50. Ziegler, S.; Eiseler, T.; Scholz, R. P.; Beck, A.; Link, G.; Hausser, A. A novel protein kinase D phosphorylation site in the tumor suppressor Rab interactor 1 is critical for coordination of cell migration Mol. Biol. Cell 2011, 22 (5) 570-580
51. Oberprieler, N. G.; Lemeer, S.; Kalland, M. E.; Torgersen, K. M.; Heck, A. J.; Taskén, K. High-resolution mapping of prostaglandin E2-dependent signaling networks identifies a constitutively active PKA signaling node in CD8+CD45RO+ T cells Blood 2010, 116 (13) 2253-2265
52. Xu, X.; Jin, T. A shortcut from GPCR signaling to Rac-mediated actin cytoskeleton through an ELMO/DOCK complex Small GTPases 2012, 3 (3) 183-5
53. Dong, J. M.; Leung, T.; Manser, E.; Lim, L. cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKalpha J. Biol. Chem. 1998, 273 (35) 22554-22562
54. Edwards, J. G.; Campbell, G.; Carr, M.; Edwards, C. C. Shapes of cells spreading on fibronectin: measurement of the stellation of BHK21 cells induced by raising cyclic AMP, and of its reversal by serum and lysophosphatidic acid J. Cell Sci. 1993, 104 (Pt 2) 399-407
55. Ramakers, G. J.; Moolenaar, W. H. Regulation of astrocyte morphology by RhoA and lysophosphatidic acid Exp. Cell Res. 1998, 245 (2) 252-62
56. Pelletier, S.; Julien, C.; Popoff, M. R.; Lamarche-Vane, N.; Meloche, S. Cyclic AMP induces morphological changes of vascular smooth muscle cells by inhibiting a Rac-dependent signaling pathway J. Cell. Physiol. 2005, 204 (2) 412-422
57. Bulin, C.; Albrecht, U.; Bode, J. G.; Weber, A. A.; Schrör, K.; Levkau, B.; Fischer, J. W. Differential effects of vasodilatory prostaglandins on focal adhesions, cytoskeletal architecture, and migration in human aortic smooth muscle cells Arterioscler., Thromb., Vasc. Biol. 2004, 25 (1) 84-89
58. Shabb, J. B. Physiological substrates of cAMP-dependent protein kinase Chem. Rev. 2001, 101 (8) 2381-2411
59. Thomas, P. E.; Peters-Golden, M.; White, E. S.; Thannickal, V. J.; Moore, B. B. PGE(2) inhibition of TGF-beta1-induced myofibroblast differentiation is Smad-independent but involves cell shape and adhesion-dependent signaling Am. J. Physiol.: Lung Cell. Mol. Physiol. 2007, 293 (2) L417-L428
60. Gabbiani, G. The myofibroblast in wound healing and fibrocontractive diseases J. Pathol. 2003, 200 (4) 500-503
61. Burridge, K.; Chrzanowska-Wodnicka, M. Focal adhesions, contractility, and signaling Annu. Rev. Cell Dev Biol. 1996, 12, 463-518
62. Kreis, T. E.; Birchmeier, W. Stress fiber sarcomeres of fibroblasts are contractile Cell 1980, 22 (2 Pt 2) 555-561
63. Hinz, B.; Dugina, V.; Ballestrem, C.; Wehrle-Haller, B.; Chaponnier, C. Alpha-smooth muscle actin is crucial for focal adhesion maturation in myofibroblasts Mol. Biol. Cell 2003, 14 (6) 2508-2519
64. Dugina, V.; Fontao, L.; Chaponnier, C.; Vasiliev, J.; Gabbiani, G. Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors J. Cell Sci. 2001, 114 (18) 3285-3296
65. Huang, S.; Wettlaufer, S. H.; Hogaboam, C.; Aronoff, D. M.; Peters-Golden, M. Prostaglandin E(2) inhibits collagen expression and proliferation in patient-derived normal lung fibroblasts via E prostanoid 2 receptor and cAMP signaling Am. J. Physiol.: Lung Cell. Mol. Physiol. 2007, 292 (2) L405-L413
66. Huang, S. K.; Wettlaufer, S. H.; Chung, J.; Peters-Golden, M. Prostaglandin E2 inhibits specific lung fibroblast functions via selective actions of PKA and Epac-1 Am. J. Respir. Cell Mol. Biol. 2008, 39 (4) 482-489
67. Baud, L.; Perez, J.; Denis, M.; Ardaillou, R. Modulation of fibroblast proliferation by sulfidopeptide leukotrienes: effect of indomethacin J. Immunol. 1987, 138 (4) 1190-1195
68. Kohyama, T.; Ertl, R. F.; Valenti, V.; Spurzem, J.; Kawamoto, M.; Nakamura, Y.; Veys, T.; Allegra, L.; Romberger, D.; Rennard, S. I. Prostaglandin E(2) inhibits fibroblast chemotaxis Am. J. Physiol.: Lung Cell. Mol. Physiol. 2001, 281 (5) L1257-L1263
69. Walker, N. M.; Badri, L. N.; Wadhwa, A.; Wettlaufer, S.; Peters-Golden, M.; Lama, V. N. Prostaglandin E2 as an inhibitory modulator of fibrogenesis in human lung allografts Am. J. Respir Crit Care Med. 2012, 185 (1) 77-84
70. Riento, K.; Ridley, A. J. Rocks: multifunctional kinases in cell behaviour Nat. Rev. Mol. Cell Biol. 2003, 4 (6) 446-456
71. Ishizaki, T.; Maekawa, M.; Fujisawa, K.; Okawa, K.; Iwamatsu, A.; Fujita, A.; Watanabe, N.; Saito, Y.; Kakizuka, A.; Morii, N.; Narumiya, S. The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase EMBO J. 1996, 15 (8) 1885-1893
72. Ziegler, S.; Eiseler, T.; Scholz, R. P.; Beck, A.; Link, G.; Hausser, A. A novel protein kinase D phosphorylation site in the tumor suppressor Rab interactor 1 is critical for coordination of cell migration Mol. Biol. Cell 2011, 22 (5) 570-580
73. Carthy, J. M.; Garmaroudi, F. S.; Luo, Z.; McManus, B. M. Wnt3a induces myofibroblast differentiation by upregulating TGF-beta signaling through SMAD2 in a beta-catenin-dependent manner PloS One 2011, 6 (5) e19809
74. Stossel, T. P.; Condeelis, J.; Cooley, L.; Hartwig, J. H.; Noegel, A.; Schleicher, M.; Shapiro, S. S. Filamins as integrators of cell mechanics and signaling Nat. Rev. Mol. Cell Biol. 2001, 2, 138-145
75. Dong, F.; Feldmesser, M.; Casadevall, A.; Rubin, C. S. Molecular characterization of a cDNA that encodes six isoforms of a novel murine A kinase anchor protein J. Biol. Chem. 1998, 273 (11) 6533-6541
76. Miyamoto, Y.; Yamauchi, J.; Mizuno, N.; Itoh, H. The adaptor protein Nck1 mediates endothelin A receptor-regulated cell migration through the Cdc42-dependent c-Jun N-terminal kinase pathway J. Biol. Chem. 2004, 279 (33) 34336-34342
77. Chen, H.; Lo, S. H. Regulation of tensin-promoted cell migration by its focal adhesion binding and Src homology domain 2 Biochem. J. 2003, 370 (3) 1039-1045
78. Chen, H.; Duncan, I. C.; Bozorgchami, H.; Lo, S. H. Tensin1 and a previously undocumented family member, tensin2, positively regulate cell migration Proc. Natl. Acad. Sci. U. S. A. 2002, 99 (2) 733-738
79. Lo, S. H.; Janmey, P. A.; Hartwig, J. H.; Chen, L. B. Interactions of tensin with actin and identification of its three distinct actin-binding domains J. Cell Biol. 1994, 125 (5) 1067-1075
80. Tada, S.; Iwamoto, H.; Nakamuta, M.; Sugimoto, R.; Enjoji, M.; Nakashima, Y.; Nawata, H. A selective ROCK inhibitor, Y27632, prevents dimethylnitrosamine-induced hepatic fibrosis in rats J. Hepatol. 2001, 34 (4) 529-536
81. Bond, J. E.; Kokosis, G.; Ren, L.; Selim, M. A.; Bergeron, A.; Levinson, H. Wound contraction is attenuated by fasudil inhibition of Rho-associated kinase Plast. Reconstr. Surg. 2011, 128 (5) 438e-450e