Prostaglandin E2-dependent blockade of actomyosin and stress fibre formation is mediated through S1379 phosphorylation of ROCK2

Journal of Cellular Biochemistry

Volumn 115, Issue 9, 2014, Pages 1516-1527

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

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

FIBROBLASTS; FIBROSIS; MYOFIBROBLASTS; MYOSIN LIGHT CHAIN; ROCK2; STRESS FIBRES

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOKINE; FILAMIN A; G PROTEIN COUPLED RECEPTOR; GUANOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 20; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; PAXILLIN; PHOSPHOPROTEIN; PROSTAGLANDIN E2; RHO ASSOCIATED COILED COIL CONTAINING KINASE 2; UNCLASSIFIED DRUG; CARDIAC MYOSIN; MYOSIN LIGHT CHAIN 2; RHO KINASE; ROCK2 PROTEIN, HUMAN;

ARTICLE; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FOCAL ADHESION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; MYOFIBROBLAST; PRIORITY JOURNAL; STRESS FIBER; WESTERN BLOTTING; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; GENETICS; METABOLISM; MUTATION; PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; SYNOVIAL FLUID;

ACTOMYOSIN; CARDIAC MYOSINS; CELLS, CULTURED; DINOPROSTONE; FIBROBLASTS; HUMANS; MUTATION; MYOSIN LIGHT CHAINS; PHOSPHORYLATION; PROTEOMICS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; STRESS FIBERS; SYNOVIAL FLUID;

EID: 84904409287     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24806     Document Type: Article

References (50)

1. Akhmetshina A, Dees C, Pileckyte M, Szucs G, Spriewald BM, Zwerina J, et al. 2008. Rho-associated kinases are crucial for myofibroblast differentiation and production of extracellular matrix in scleroderma fibroblasts. Arthritis Rheum 58: 2553-2564.
2. Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, Christy W, Cooke TD,. 1986. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 29: 1039-1049.
3. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, Kaibuchi K,. 1996. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 271: 20246-20249.
4. Amano M, Chibara K, Nakamura N, Kaneto T, Matsuura Y, Kaibuchi K,. 1999. The COOH terminus of Rho-kinase negatively regulates rho-kinase activity. J Biol Chem 274: 32418-32424.
5. Ballestrem C, Erez N, Kirchner J, Kam Z, Bershadsky A, Geiger B,. 2006. Molecular mapping of tyrosine-phosphorylated proteins in focal adhesions using fluorescence resonance energy transfer. J Cell Sci 119: 866-875.
6. Besser A, Schwarz,. 2007. Coupling biochemistry and mechanics in cell adhesion: a model for inhomogeneous stress fiber contraction. New J. Physics 9: 425.
7. Bond J, Ho TQ, Selim MA, Hunter C, Bowers EV, Levinson H,. 2011. Temporal spatial expression and function of non-muscle myosin II isoforms IIA and IIB in scar remodeling. Lab Invest 91 (4): 499-508.
8. Butcher DT, Alliston T, Weaver VM,. 2009. A tense situation: Forcing tumour progression. Nat Rev Cancer 9: 108-122.
9. Clegg CH, Abrahamsen MS, Degen JL, Morris DR, McKnight,. 1992. Cyclic AMP-dependent protein kinase controls basal gene activity and steroidogenesis in Y1 adrenal tumor cells. Biochemistry 31: 3720-3726.
10. Desmoulière A, Darby IA, Gabbiani G,. 2003. Normal and pathologic soft tissue remodeling: Role of the myofibroblast, with special emphasis on liver and kidney fibrosis. Lab Invest 83: 1689-1707.
11. Doggrell SA,. 2005. Rho-kinase inhibitors show promise in pulmonary hypertension. Expert Opin Invest Drugs 14: 1157-1159.
12. Dong JM, Leung T, Manser E, Lim L,. 1998. CAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKalpha. J Biol Chem 273: 22554-22562.
13. Dreiza CM, Brophy CM, Komalavilas P, Furnish EJ, Joshi L, Pallero MA, et al. 2005. Transducible heat shock protein 20 (HSP20) phosphopeptide alters cytoskeletal dynamics. FASEB J 19: 261-263.
14. Faour WH, Alaaeddine N, Mancini A, He QW, Jovanovic D, Di Battista JA,. 2005. 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 280: 9536-9546.
15. Funk CD,. 2001. Prostaglandins and leukotrienes: Advances in eicosanoid biology. Science 294: 1871-1875.
16. Goeckeler ZM, Wysolmerski RB,. 2005. Myosin phosphatase and cofilin mediate cAMP/cAMP-dependent protein kinase-induced decline in endothelial cell isometric tension and myosin II regulatory light chain phosphorylation. J Biol Chem 280: 33083-33095.
17. Guarino M, Tosoni A, Nebuloni M,. 2009. Direct contribution of epithelium to organ fibrosis: Epithelial-mesenchymal transition. Hum Pathol 40: 1365-1376.
18. Hinz B,. 2007. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 127: 526-537.
19. Hinz B,. 2010. The myofibroblast: Paradigm for a mechanically active cell. J Biomech 43: 146-155.
20. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C,. 2001. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 12: 2730-2741.
21. Hochberg MC, Chang RW, Dwosh I, Lindsey S, Pincus T, Wolfe F,. 1991. The American College of Rheumatology 1991 revised criteria for the classification of global functional status in rheumatoid arthritis. Arthritis Rheum 35: 498-502.
22. Horowitz JC, Thannickal VJ,. 2006. Epithelial-mesenchymal interactions in pulmonary fibrosis. Semin. Respir. Crit Care Med 27: 600-612.
23. Howe AK,. 2004. Regulation of actin-based cell migration by cAMP/PKA. Biochim Biophys Acta 1692: 159-174.
24. Ishizaki T, Maekawa M, Fujisawa K, Okawa K, Iwamatsu A, Fujita A, Watanabe N, Saito Y, Kakizuka A, Morii N, Narumiya,. 1996. The small GTP-binding protein Rho binds to and activates a 160kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J 15: 1885-1893.
25. Jones AT, Sayers EJ,. 2012. Cell entry of cell penetrating peptides: Tales of tails wagging dogs. J Control Release 161 (2): 582-591.
26. Kartberg F, Asp L, Dejgaard SY, Smedh M, Fernandez-Rodriguez J, Nilsson T, Presley JF,. 2010. ARFGAP2 and ARFGAP3 are essential for COPI coat assembly on the Golgi membrane of living cells. J Biol Chem 285: 36709-36720.
27. Kolodsick JE, Peters-Golden M, Larios J, Toews GB, Thannickal VJ, Moore BB,. 2003. Prostaglandin E2 inhibits fibroblast to myofibroblast transition via E. prostanoid receptor 2 signaling and cyclic adenosine monophosphate elevation. Am J Respir Cell Mol Biol 29: 537-544.
28. Komalavilas P, Penn RB, Flynn CR, Thresher J, Lopes LB, Furnish EJ, et al. 2008. The small heat shock-related protein, HSP20, is a cAMP-dependent protein kinase substrate that is involved in airway smooth muscle relaxation. Am J Physiol Lung Cell Mol Physiol 294: L69-L78.
29. Liu M, et al. 2009. Therapeutic effect of Y-27632 on chronic allograft nephropathy in rats. J Surg Res 157: 117-127.
30. Moritz A, Li Y, Guo A, Villén J, Wang Y, MacNeill J, Kornhauser J, Sprott K, Zhou J, Possemato A, Min Ren J, Hornbeck P, Cantley LC, Gygi SP, Rush J, Comb MJ,. 2010. Akt-RSK-S6 kinase signaling networks activated by oncogenic receptor tyrosine kinases. Sci Signal 3 (136): ra64.1-ra64.11.
31. Murthy KS, Zhou H, Grider JR, Maklouf GM,. 2003. Inhibition of sustained smooth muscle contraction by PKA and PKG preferentially mediated by phosphorylation of RhoA. Am J Physiol Gastrointest Liver Physiol 284: G1006-G1016.
32. Pasapera AM, Schneider IC, Rericha E, Schlaepfer DD, Waterman CM,. 2010. Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J Cell Biol 188: 877-890.
33. Patel NM, Lederer DJ, Borczuk AC, Kawut SM,. 2007. Pulmonary hypertension in idiopathic pulmonary fibrosis. Chest 132: 998-1006.
34. Ramachandran C, Patil RV, Combrink K, Sharif NA, Srinivas SP,. 2011. 2011. Rho-Rho kinase pathway in the actomyosin contraction and cell-matrix adhesion in immortalized human trabecular meshwork cells. Mol Vis 17: 1877-1890.
35. Sandulache VC, Parekh A, Li-Korotky H, Dohar JE, Hebda PA,. 2007. Prostaglandin E2 inhibition of keloid fibroblast migration, contraction, and transforming growth factor (TGF)-beta1-induced collagen synthesis. Wound Repair Regen 15: 122-133.
36. Schneider IC, Hays CK, Waterman,. 2009. Epidermal growth factor-induced contraction regulates paxillin phosphorylation to temporally separate traction generation from de-adhesion. Mol Biol Cell 20: 3155-3167.
37. Song HY1, Kim MY, Kim KH, Lee IH, Shin SH, Lee JS, Kim JH,. 2010. Synovial fluid of patients with rheumatoid arthritis induces alpha-smooth muscle actin in human adipose tissue-derived mesenchymal stem cells through a TGF-beta1-dependent mechanism. Exp Mol Med 42 (8): 565-573.
38. Steenvoorden, Tolboom TC, van der Pluijm G, Löwik C, Visser CP, DeGroot J, Gittenberger-DeGroot AC, DeRuiter MC, Wisse BJ, Huizinga TW, Toes RE,. 2006. Transition of healthy to diseased synovial tissue in rheumatoid arthritis is associated with gain of mesenchymal/fibrotic characteristics. Arthritis Res Ther 8 (6): R165.
39. Stossel TP, Condeelis J, Cooley L, Hartwig JH, Noegel A, Schleicher M, Shapiro SS,. 2001. Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2: 138-145.
40. Strutz F, Okada H, Lo CW, Danoff T, Carone RL, Tomaszewski JE, Neilson EG,. 1995. Identification and characterization of a fibroblast marker: FSP1. J Cell Biol 130: 393-405.
41. Thomas PE, Peters-Golden M, White ES, Thannickal VJ, Moore BB,. 2007. PGE(2) inhibition of TGF-beta1-induced myofibroblast differentiation is Smad-independent but involves cell shape and adhesion-dependent signalling. Am J Physiol Lung Cell Mol Physiol 293: L417-L428.
42. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA,. 2002. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3: 349-363.
43. Tomasek JJ, Vaughan MB, Kropp BP, Gabbiani G, Martin MD, Haaksma CJ, Hinz B,. 2006. Contraction of myofibroblasts in granulation tissue is dependent on Rho/Rho kinase/myosin light chain phosphatase activity. Wound Repair Regen. 14: 313-320.
44. Turner CE,. 2000. Paxillin and focal adhesion signalling. Nat Cell Biol 2: E231-E236.
45. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR,. 2009. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10: 778-790.
46. Washida N, Wakino S, Tonozuka Y, Homma K, Tokuyama H, Hara Y, Haseqawa K, et al. 2011. Rho-kinase inhibition ameliorates peritoneal fibrosis and angiogenesis in a rat model of peritoneal sclerosis. Nephrol Dial Transplant 26: 2770-2779.
47. Woo MS, Ohta Y, Rabinovitz I, Stossel TP, Blenis J,. 2004. Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol Cell Biol 24: 3025-3035.
48. Wozniak MA, Modzelewska K, Kwong L, Keely PJ,. 2004. Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692: 103-119.
49. Zhai B, Yang H, Mancini A, He QW, Antoniou J, Di Battista,. 2010. 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 285: 23568-23580.
50. Zimmermann T, Kunisch E, Pfeiffer R, Hirth A, Hans-Detlev Stahl H-D, Sack U, Laube A, Liesaus E, Roth A, Palombo-Kinne E, Emmrich F,. 2001. Isolation and characterization of rheumatoid arthritis synovial fibroblasts from primary culture-Primary culture cells markedly differ from fourth-passage cells. Arthritis Res 3: 72-76.