Compressive stress induces dephosphorylation of the myosin regulatory light chain via RhoA phosphorylation by the adenylyl cyclase/protein kinase a signaling pathway

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Takemoto, Kenji ^a   Ishihara, Seiichiro ^a,b   Mizutani, Takeomi ^a   Kawabata, Kazushige ^a   Haga, Hisashi ^a,b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; MYOSIN REGULATORY LIGHT CHAIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; CALYCULIN A; MYOSIN LIGHT CHAIN KINASE; OXAZOLE DERIVATIVE; PPP1R12A PROTEIN, MOUSE; SMALL INTERFERING RNA;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; COMPRESSION; CONTROLLED STUDY; MECHANICAL STRESS; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; COMPRESSIVE STRENGTH; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; RNA INTERFERENCE;

ACTIN CYTOSKELETON; ADENYLYL CYCLASES; ANIMALS; CELL LINE; COMPRESSIVE STRENGTH; CYCLIC AMP-DEPENDENT PROTEIN KINASES; MICE; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN KINASE; MYOSIN-LIGHT-CHAIN PHOSPHATASE; OXAZOLES; PHOSPHORYLATION; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84923886578     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117937     Document Type: Article

References (58)

1. Kuo L, Arko F, Chilian WM, Davis MJ (1993) Coronary venular responses to flow and pressure. Circ Res 72: 607-615 PMID: 8431988
2. Osol G, Brekke JF, McElroy-Yaggy K, Gokina NI (2002) Myogenic tone, reactivity, and forced dilatation: a three-phase model of in vitro arterial myogenic behavior. Am J Physiol Heart Circ Physiol 283: H2260-2267. PMID: 12388265
3. Izzard AS, Graham D, Burnham MP, Heerkens EH, Dominiczak AF, et al. (2003) Myogenic and structural properties of cerebral arteries from the stroke-prone spontaneously hypertensive rat. Am J Physiol Heart Circ Physiol 285: H1489-1494. PMID: 12816753
4. Gschwend S, Henning RH, Pinto YM, de Zeeuw D, van Gilst WH, et al. (2003) Myogenic constriction is increased in mesenteric resistance arteries from rats with chronic heart failure: instantaneous counteraction by acute AT1 receptor blockade. Br J Pharmacol 139: 1317-1325. PMID: 12890711
5. Masumoto A, Mohri M, Shimokawa H, Urakami L, Usui M, et al. (2002) Suppression of coronary artery spasm by the Rho-kinase inhibitor fasudil in patients with vasospastic angina. Circulation 105: 1545-1547. PMID: 11927519
6. Miyamoto S, Teramoto H, Coso OA, Gutkind JS, Burbelo PD, et al. (1995) Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol 131: 791-805. PMID: 7593197
7. Coste B, Mathur J, Schmidt M, Earley TJ, Ranade S, et al. (2010) Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330: 55-60. doi: 10.1126/science.1193270 PMID: 20813920
8. Hara F, Fukuda K, Asada S, Matsukawa M, Hamanishi C (2001) Cyclic tensile stretch inhibition of nitric oxide release from osteoblast-like cells is both G protein and actin-dependent. J Orthop Res 19: 126-131. PMID: 11332608
9. Dennerll TJ, Joshi HC, Steel VL, Buxbaum RE, Heidemann SR (1988) Tension and compression in the cytoskeleton of PC-12 neurites. II: Quantitative measurements. J. Cell Biol 107: 665-674 PMID: 3417767
10. Riser BL, Cortes P, Zhao X, Bernstein J, Dumler F, et al. (1992) Intraglomerular pressure and mesangial stretching stimulate extracellular matrix formation in the rat. J Clin Invest 90: 1932-1943. PMID: 1430216
11. Yoshikawa T, Peel SA, Gladstone JR, Davies JE (1997) Biochemical analysis of the response in rat bone marrow cell cultures to mechanical stimulation. Biomed Mater Eng 7: 369-377. PMID: 9622104
12. Mizutani T, Haga H, Kawabata K (2004) Cellular stiffness response to external deformation: tensional homeostasis in a single fibroblast. Cell Motil Cytoskeleton 59: 242-248. PMID: 15493061
13. Ikebe M, Hartshorne DJ (1985) Phosphorylation of smooth muscle myosin at two distinct sites by myosin light chain kinase. J Biol Chem 260: 10027-10031. PMID: 3839510
14. Mabuchi Y, Mabuchi K, Stafford WF, Grabarek Z (2010) Modular structure of smooth muscle Myosin light chain kinase: hydrodynamic modeling and functional implications. Biochemistry 49: 2903-2917. doi: 10.1021/bi901963e PMID: 20196616
15. Alessi D, MacDougall LK, Sola MM, Ikebe M, Cohen P (1992) The control of protein phosphatase-1 by targetting subunits. The major myosin phosphatase in avian smooth muscle is a novel form of protein phosphatase-1. Eur J Biochem 210: 1023-1035. PMID: 1336455
16. Shirazi A, Iizuka K, Fadden P, Mosse C, Somlyo AP, et al. (1994) Purification and characterization of the mammalian myosin light chain phosphatase holoenzyme. The differential effects of the holoenzyme and its subunits on smooth muscle. J Biol Chem 269: 31598-31606. PMID: 7989330
17. Kimura K, Fukata Y, Matsuoka Y, Bennett V, Matsuura Y, et al. (1998) Regulation of the association of adducin with actin filaments by Rho-associated kinase (Rho-kinase) and myosin phosphatase. J Biol Chem 273: 5542-5548. PMID: 9488679
18. Mizutani T, Kawabata K, Koyama Y, Takahashi M, Haga H (2009) Regulation of cellular contractile force in response to mechanical stretch by diphosphorylation of myosin regulatory light chain via RhoA signaling cascade. Cell Motil Cytoskeleton 66: 389-397. doi: 10.1002/cm.20378 PMID: 19444895
19. Nusser N, Gosmanova E, Makarova N, Fujiwara Y, Yang L, et al (2006) Serine phosphorylation differentially affects RhoA binding to effectors: implications to NGF-induced neurite outgrowth. Cell Signal 18: 704-714. PMID: 16109481
20. Kawamoto T, Haga H, Tamura K, Mizutani T, Kawabata K (2008) Mechanical Response to Isotropic Shrinkage of Fibroblasts Measured by Scanning Probe Microscopy. Jpn J Appl Phys 47: 6173-6176
21. Tamura K, Haga H, Mizutani T, Kawabata K (2011) Active fluctuation in the cortical cytoskeleton observed by high-speed live-cell scanning probe microscopy. Acta Biomater 7: 3766-3772. doi: 10.1016/j.actbio.2011.06.013 PMID: 21704197
22. Yoshigi M, Hoffman LM, Jensen CC, Yost HJ, Beckerle MC (2005) Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J Cell Biol 171: 209-215. PMID: 16247023
23. Mehta D, Gunst SJ (1999) Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J Physiol 519: 829-840. PMID: 10457094
24. Ichikawa K, Hirano K, Ito M, Tanaka J, Nakano T, Hartshorne DJ (1996) Interactions and properties of smooth muscle myosin phosphatase. Biochemistry 35: 6313-6320. PMID: 8639575
25. Hirano K, Phan BC, Hartshorne DJ (1997) Interactions of the subunits of smooth muscle myosin phosphatase. J Biol Chem 272: 3683-3688. PMID: 9013623
26. Hudson CA, Heesom KJ, Lopez Bernal A (2012) Phasic contractions of isolated human myometrium are associated with Rho-kinase (ROCK)-dependent phosphorylation of myosin phosphatase-targeting subunit (MYPT1). Mol Hum Reprod 18: 265-279. doi: 10.1093/molehr/gar078 PMID: 22155728
27. Kiss E, Muranyi A, Csortos C, Gergely P, Ito M, et al (2002) Integrin-linked kinase phosphorylates the myosin phosphatase target subunit at the inhibitory site in platelet cytoskeleton. Biochemical Journal 365: 79-87. PMID: 11931630
28. Takizawa N, Koga Y, Ikebe M (2002) Phosphorylation of CPI17 and myosin binding subunit of type 1 protein phosphatase by p21-activated kinase. Biochem Biophys Res Commun 297: 773-778. PMID: 12359219
29. Velasco G, Armstrong C, Morrice N, Frame S, Cohen P (2002) Phosphorylation of the regulatory subunit of smooth muscle protein phosphatase 1M at Thr850 induces its dissociation from myosin. FEBS Lett 527: 101-104. PMID: 12220642
30. Khromov A, Choudhury N, Stevenson AS, Somlyo AV, Eto M (2009) Phosphorylation-dependent autoinhibition of myosin light chain phosphatase accounts for Ca2+ sensitization force of smooth muscle contraction. J Biol Chem 284: 21569-21579. doi: 10.1074/jbc.M109.019729 PMID: 19531490
31. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, et al (1996) Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J 15: 510-519. PMID: 8599934
32. Meinkoth JL, Alberts AS, Went W, Fantozzi D, Taylor SS, et al (1993) Signal transduction through the cAMP-dependent protein kinase. Mol Cell Biochem 127-128: 179-186.
33. Hanoune J, Defer N (2001) Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol 41: 145-174. PMID: 11264454
34. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, et al (2011) Role of YAP/TAZ in mechanotransduction. Nature 474: 179-183. doi: 10.1038/nature10137 PMID: 21654799
35. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276: 1425-1428. PMID: 9162012
36. Eisenhoffer GT, Loftus PD, Yoshigi M, Otsuna H, Chien CB, et al (2012) Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 484: 546-549. doi: 10.1038/nature10999 PMID: 22504183
37. Norman LL, Brugues J, Sengupta K, Sens P, Aranda-Espinoza H (2010) Cell blebbing and membrane area homeostasis in spreading and retracting cells. Biophys J 99: 1726-1733. doi: 10.1016/j.bpj.2010.07.031 PMID: 20858416
38. Dubin-Thaler BJ, Hofman JM, Cai Y, Xenias H, Spielman I, et al (2008) Quantification of cell edge velocities and traction forces reveals distinct motility modules during cell spreading. PLoS One 3: e3735. doi: 10.1371/journal.pone.0003735 PMID: 19011687
39. Steffen A, Ladwein M, Dimchev GA, Hein A, Schwenkmezger L, et al (2013) Rac function is crucial for cell migration but is not required for spreading and focal adhesion formation. J Cell Sci 126: 4572-4588. doi: 10.1242/jcs.118232 PMID: 23902686
40. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, et al (2009) Coordination of Rho GTPase activities during cell protrusion. Nature 461: 99-103. doi: 10.1038/nature08242 PMID: 19693013
41. Hayakawa K, Tatsumi H, Sokabe M (2011) Actin filaments function as a tension sensor by tensiondependent binding of cofilin to the filament. J Cell Biol 195: 721-727. doi: 10.1083/jcb.201102039 PMID: 22123860
42. Moseley JB, Maiti S, Goode BL (2006) Formin proteins: purification and measurement of effects on actin assembly. Methods Enzymol 406: 215-234. PMID: 16472660
43. Kovar DR, Harris ES, Mahaffy R, Higgs HN, Pollard TD (2006) Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124: 423-435. PMID: 16439214
44. Salisbury JL, Condeelis JS, Satir P (1980) Role of coated vesicles, microfilaments, and calmodulin in receptor-mediated endocytosis by cultured B lymphoblastoid cells. J Cell Biol 87: 132-141. PMID: 6968316
45. Le Clainche C, Pauly BS, Zhang CX, Engqvist-Goldstein AE, Cunningham K, et al (2007) A Hip1R-cortactin complex negatively regulates actin assembly associated with endocytosis. EMBO J 26: 1199-1210. PMID: 17318189
46. Merrifield CJ, Qualmann B, Kessels MM, Almers W (2004) Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts. Eur J Cell Biol 83: 13-18. PMID: 15085951
47. Guilluy C, Swaminathan V, Garcia-Mata R, O 'Brien ET, Superfine R, et al (2011) The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat Cell Biol 13: 722-727. doi: 10.1038/ncb2254 PMID: 21572419
48. Liu Y, Collins C, Kiosses WB, Murray AM, Joshi M, et al (2013) A novel pathway spatiotemporally activates Rac1 and redox signaling in response to fluid shear stress. J Cell Biol 201: 863-873. doi: 10. 1083/jcb.201207115 PMID: 23733346
49. Hobert O, Schilling JW, Beckerle MC, Ullrich A, Jallal B (1996) SH3 domain-dependent interaction of the proto-oncogene product Vav with the focal contact protein zyxin. Oncogene 12: 1577-1581. PMID: 8622875
50. Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, et al (2008) PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J Cell Biol 180: 187-203. doi: 10.1083/jcb.200708194 PMID: 18195107
51. Iwanicki MP, Vomastek T, Tilghman RW, Martin KH, Banerjee J, et al (2008) FAK, PDZ-RhoGEF and ROCKII cooperate to regulate adhesion movement and trailing-edge retraction in fibroblasts. J Cell Sci 121: 895-905. doi: 10.1242/jcs.020941 PMID: 18303050
52. Pinto C, Papa D, Hubner M, Mou TC, Lushington GH, et al (2008) Activation and inhibition of adenylyl cyclase isoforms by forskolin analogs. J Pharmacol Exp Ther 325: 27-36. doi: 10.1124/jpet.107.131904 PMID: 18184830
53. Tian Y, Laychock SG (2001) Protein kinase C and calcium regulation of adenylyl cyclase in isolated rat pancreatic islets. Diabetes 50: 2505-2513. PMID: 11679428
54. Halls ML, Cooper DM (2011) Regulation by Ca2+-signaling pathways of adenylyl cyclases. Cold Spring Harb Perspect Biol 3: a004143. doi: 10.1101/cshperspect.a004143 PMID: 21123395
55. Grunspan-Swirsky A, Pick E (1978) Enhancement of macrophage adenylate cyclase by microtubule disrupting drugs. Immunopharmacology 1: 71-82. PMID: 45791
56. Kwon RY, Temiyasathit S, Tummala P, Quah CC, Jacobs CR (2010) Primary cilium-dependent mechanosensing is mediated by adenylyl cyclase 6 and cyclic AMP in bone cells. FASEB J 24: 2859-2868. doi: 10.1096/fj.09-148007 PMID: 20371630
57. Davies SP, Reddy H, Caivano M, Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105. PMID: 10998351
58. Aburima A, Wraith KS, Raslan Z, Law R, Magwenzi S, et al (2013) cAMP signaling regulates platelet myosin light chain (MLC) phosphorylation and shape change through targeting the RhoA-Rho kinase-MLC phosphatase signaling pathway. Blood 122: 3533-3545. doi: 10.1182/blood-2013-03-487850 PMID: 24100445