A molecular ruler regulates cytoskeletal remodelling by the Rho kinases

Nature Communications

Volumn 6, Issue , 2015, Pages

  Truebestein, Linda ^a   Elsner, Daniel J ^a   Fuchs, Elisabeth ^a   Leonard, Thomas A ^a,b  

^a MAX F PERUTZ LABORATORIES   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ACTIN; ROCK2 PROTEIN, HUMAN;

ELECTRON MICROSCOPY; ENZYME ACTIVITY; GENE EXPRESSION; MEMBRANE; MOLECULAR ANALYSIS; PLASMA; PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HUMAN; MEMBRANE BINDING; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; CHEMISTRY; DIMERIZATION; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ACTINS; CYTOSKELETON; DIMERIZATION; HUMANS; PROTEIN STRUCTURE, TERTIARY; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN;

EID: 84948807337     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10029     Document Type: Article

References (61)

1. Vicente-Manzanares, M., Ma, X., Adelstein, R. S., Horwitz, A. R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10, 778-790 (2009).
2. Amano, M. et al. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249 (1996).
3. Kawabata, S. et al. Interaction of Rho-kinase with myosin II at stress fibres. Genes Cells 9, 653-660 (2004).
4. Kimura, K. et al. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248 (1996).
5. Winter, C. G. et al. Drosophila Rho-associated kinase (Drok) links Frizzledmediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-91 (2001).
6. Feng, J. et al. Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J .Biol. Chem. 274, 37385-37390 (1999).
7. Amano, M. et al. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275, 1308-1311 (1997).
8. Thumkeo, D. et al. Targeted disruption of the mouse rho-associated kinase 2 gene results in intrauterine growth retardation and fetal death. Mol. Cell Biol. 23, 5043-5055 (2003).
9. Shimizu, Y. et al. ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles. J. Cell Biol. 168, 941-953 (2005).
10. Thumkeo, D., Shimizu, Y., Sakamoto, S., Yamada, S., Narumiya, S. ROCK-I and ROCK-II cooperatively regulate closure of eyelid and ventral body wall in mouse embryo. Genes Cells 10, 825-834 (2005).
11. Jacobs, M. et al. The structure of dimeric ROCK I reveals the mechanism for ligand selectivity. J. Biol. Chem. 281, 260-268 (2006).
12. Yamaguchi, H., Kasa, M., Amano, M., Kaibuchi, K., Hakoshima, T. Molecular mechanism for the regulation of rho-kinase by dimerization and its inhibition by fasudil. Structure 14, 589-600 (2006).
13. Wen, W., Liu, W., Yan, J., Zhang, M. Structure basis and unconventional lipid membrane binding properties of the PH-C1 tandem of rho kinases. J. Biol. Chem. 283, 26263-26273 (2008).
14. Tu, D. et al. Crystal structure of a coiled-coil domain from human ROCK I. PLoS ONE 6, e18080 (2011).
15. Shimizu, T. et al. Parallel coiled-coil association of the RhoA-binding domain in Rho-kinase. J. Biol. Chem. 278, 46046-46051 (2003).
16. Dvorsky, R., Blumenstein, L., Vetter, I. R., Ahmadian, M. R. Structural insights into the interaction of ROCKI with the switch regions of RhoA. J. Biol. Chem. 279, 7098-7104 (2004).
17. Mohan, S. et al. Structure of a highly conserved domain of rock1 required for shroom-mediated regulation of cell morphology. PLoS ONE 8, e81075 (2013).
18. Fujisawa, K., Fujita, A., Ishizaki, T., Saito, Y., Narumiya, S. Identification of the Rho-binding domain of p160ROCK, a Rho-associated coiled-coil containing protein kinase. J. Biol. Chem. 271, 23022-23028 (1996).
19. Feng, J. et al. Rho-associated kinase of chicken gizzard smooth muscle. J. Biol. Chem. 274, 3744-3752 (1999).
20. Matsui, T. et al. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J. 15, 2208-2216 (1996).
21. Ishizaki, T. et al. The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J. 15, 1885-1893 (1996).
22. Sebbagh, M. et al. Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat. Cell Biol. 3, 346-352 (2001).
23. Coleman, M. L. et al. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3, 339-345 (2001).
24. Sebbagh, M., Hamelin, J., Bertoglio, J., Solary, E., Breard, J. Direct cleavage of ROCK II by granzyme B induces target cell membrane blebbing in a caspaseindependent manner. J. Exp. Med. 201, 465-471 (2005).
25. Leonard, T. A., Rozycki, B., Saidi, L. F., Hummer, G., Hurley, J. H. Crystal structure and allosteric activation of protein kinase C betaII. Cell 144, 55-66 (2011).
26. Amano, M. et al. The COOH terminus of Rho-kinase negatively regulates rhokinase activity. J. Biol. Chem. 274, 32418-32424 (1999).
27. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
28. Leung, T., Chen, X. Q., Manser, E., Lim, L. The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell Biol. 16, 5313-5327 (1996).
29. Ishizaki, T. et al. p160ROCK, a Rho-associated coiled-coil forming protein kinase, works downstream of Rho and induces focal adhesions. FEBS Lett. 404, 118-124 (1997).
30. Rossman, K. L. et al. Functional analysis of cdc42 residues required for Guanine nucleotide exchange. J. Biol. Chem. 277, 50893-50898 (2002).
31. Endicott, J. A., Noble, M. E., Johnson, L. N. The structural basis for control of eukaryotic protein kinases. Annu. Rev. Biochem. 81, 587-613 (2012).
32. Heikkila, T. et al. Co-crystal structures of inhibitors with MRCKbeta, a key regulator of tumor cell invasion. PLoS ONE 6, e24825 (2011).
33. Chen, X. Q. et al. Characterization of RhoA-binding kinase ROKalpha implication of the pleckstrin homology domain in ROKalpha function using region-specific antibodies. J. Biol. Chem. 277, 12680-12688 (2002).
34. Sebe-Pedros, A., Roger, A. J., Lang, F. B., King, N., Ruiz-Trillo, I. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc. Natl Acad. Sci. USA 107, 10142-10147 (2010).
35. Blumenstein, L., Ahmadian, M. R. Models of the cooperative mechanism for Rho effector recognition: implications for RhoA-mediated effector activation. J. Biol. Chem. 279, 53419-53426 (2004).
36. Sahai, E., Alberts, A. S., Treisman, R. RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation. EMBO J. 17, 1350-1361 (1998).
37. Pearce, L. R., Komander, D., Alessi, D. R. The nuts and bolts of AGC protein kinases. Nat. Rev. Mol. Cell Biol. 11, 9-22 (2010).
38. Yang, J. et al. Crystal structure of an activated Akt/protein kinase B ternary complex with GSK3-peptide and AMP-PNP. Nat. Struct. Biol. 9, 940-944 (2002).
39. Gurevich, E. V., Tesmer, J. J., Mushegian, A., Gurevich, V. V. G proteincoupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol. Ther. 133, 40-69 (2012).
40. Couzens, A. L., Saridakis, V., Scheid, M. P. The hydrophobic motif of ROCK2 requires association with the N-terminal extension for kinase activity. Biochem. J. 419, 141-148 (2009).
41. Jeffrey, P. D. et al. Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376, 313-320 (1995).
42. Komander, D., Garg, R., Wan, P. T., Ridley, A. J., Barford, D. Mechanism of multi-site phosphorylation from a ROCK-I:RhoE complex structure. EMBO J. 27, 3175-3185 (2008).
43. Kim, C., Cheng, C. Y., Saldanha, S. A., Taylor, S. S. PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation. Cell 130, 1032-1043 (2007).
44. House, C., Kemp, B. E. Protein kinase C contains a pseudosubstrate prototope in its regulatory domain. Science 238, 1726-1728 (1987).
45. Lietha, D. et al. Structural basis for the autoinhibition of focal adhesion kinase. Cell 129, 1177-1187 (2007).
46. Hildebrand, J. D., Soriano, P. Shroom, a PDZ domain-containing actinbinding protein, is required for neural tube morphogenesis in mice. Cell 99, 485-497 (1999).
47. Nishimura, T., Takeichi, M. Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 135, 1493-1502 (2008).
48. Mohan, S. et al. Structure of Shroom domain 2 reveals a three-segmented coiled-coil required for dimerization, Rock binding, and apical constriction. Mol. Biol. Cell 23, 2131-2142 (2012).
49. Clark, A. G., Dierkes, K., Paluch, E. K. Monitoring actin cortex thickness in live cells. Biophys. J. 105, 570-580 (2013).
50. Kanchanawong, P. et al. Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584 (2010).
51. Hu, K., Ji, L., Applegate, K. T., Danuser, G., Waterman-Storer, C. M. Differential transmission of actin motion within focal adhesions. Science 315, 111-115 (2007).
52. Jiang, G., Giannone, G., Critchley, D. R., Fukumoto, E., Sheetz, M. P. Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424, 334-337 (2003).
53. del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641 (2009).
54. Rauskolb, C., Sun, S., Sun, G., Pan, Y., Irvine, K. D. Cytoskeletal tension inhibits Hippo signaling through an Ajuba-Warts complex. Cell 158, 143-156 (2014).
55. Butcher, D. T., Alliston, T., Weaver, V. M. A tense situation: forcing tumour progression. Nat. Rev. Cancer 9, 108-122 (2009).
56. Wong, C. C., Wong, C. M., Tung, E. K., Man, K., Ng, I. O. Rho-kinase 2 is frequently overexpressed in hepatocellular carcinoma and involved in tumor invasion. Hepatology 49, 1583-1594 (2009).
57. Strohalm, M. et al. mMass 3: a cross-platform software environment for precise analysis of mass spectrometric data. Anal. Chem. 82, 4648-4651 (2010).
58. Rappsilber, J. et al. Protocol for micro-purification, enrichment, prefractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906 (2007).
59. Cox, J., Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372 (2008).
60. Sanjana, N. E., Shalem, O., Zhang, F. Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods 11, 783-784 (2014).
61. Versteeg, G. A. et al. The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors. Immunity 38, 384-398 (2013).