ROCK1 functions as a suppressor of inflammatory cell migration by regulating PTEN phosphorylation and stability

Blood

Volumn 115, Issue 9, 2010, Pages 1785-1796

  Vemula, Sasidhar ^b   Shi, Jianjian ^a   Hanneman, Philip ^a   Wei, Lei ^a   Kapur, Reuben ^b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; F ACTIN; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; ROCK1 PROTEIN; UNCLASSIFIED DRUG; ACTIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PTEN PROTEIN, MOUSE; RHO KINASE; ROCK1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PERITONITIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; WOUND HEALING; ANIMAL; BIOLOGICAL MODEL; CELL MOTION; CHEMISTRY; DISEASE MODEL; GENETICS; INFLAMMATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY;

ACTINS; ANIMALS; CELL ADHESION; CELL MOVEMENT; DISEASE MODELS, ANIMAL; GLYCOGEN SYNTHASE KINASE 3; INFLAMMATION; MACROPHAGES; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEUTROPHILS; PERITONITIS; PHOSPHORYLATION; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RHO-ASSOCIATED KINASES; WOUND HEALING;

EID: 77950365395     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-08-237222     Document Type: Article

References (62)

1. Baggiolini M. Chemokines in pathology and medicine. J Intern Med. 2001;250(2):91-104.
2. Davis C, Fischer J, Ley K, Sarembock IJ. The role of inflammation in vascular injury and repair. J Thromb Haemost. 2003;1(8):1699-1709.
3. Wipke BT, Allen PM. Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol. 2001;167(3):1601-1608.
4. Chuluyan HE, Osborn L, Lobb R, Issekutz AC. Domains 1 and 4 of vascular cell adhesion molecule-1 (CD106) both support very late activation antigen-4 (CD49d/CD29)-dependent monocyte transendothelial migration. J Immunol. 1995;155(6):3135-13134
5. Meerschaert J, Furie MB. The adhesion molecules used by monocytes for migration across endothelium include CD11a/CD18, CD11b/CD18, and VLA-4 on monocytes and ICAM-1, VCAM-1, and other ligands on endothelium. J Immunol. 1995;154(8):4099-4112.
6. Vanhaesebroeck B, Leevers SJ, Ahmadi K, et al. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem. 2001;70:535-602. (Pubitemid 32662219)
7. Hawkins PT, Anderson KE, Davidson K, Stephens LR. Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans. 2006;34(5):647-662.
8. Cully M, You H, Levine AJ, Mak TW. Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat Rev Cancer. 2006;6(3):184-192. (Pubitemid 43292562)
9. Maehama T, Dixon JE. PTEN: a tumour suppressor that functions as a phospholipid phosphatase. Trends Cell Biol. 1999;9(4):125-128. (Pubitemid 29161437)
10. Salmena L, Carracedo A, Pandolfi PP. Tenets of PTEN tumor suppression. Cell. 2008;133(3):403-414.
11. Stemke-Hale K, Gonzalez-Angulo AM, Lluch A, et al. An integrative genomic and proteomic analysis of PIK3CA, PTEN, and AKT mutations in breast cancer. Cancer Res. 2008;68(15):6084-6091.
12. Funamoto S, Meili R, Lee S, Parry L, Firtel RA. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell. 2002;109(5):611-623. (Pubitemid 34628724)
13. Li Z, Hannigan M, Mo Z, et al. Directional sensing requires G beta gamma-mediated PAK1 and PIX alpha-dependent activation of Cdc42. Cell. 2003;114(2):215-227. (Pubitemid 36936915)
14. Li Z, Dong X, Wang Z, et al. Regulation of PTEN by Rho small GTPases. Nat Cell Biol. 2005;7(4):399-404. (Pubitemid 40533130)
15. Iijima M, Huang YE, Devreotes P. Temporal and spatial regulation of chemotaxis. Dev Cell. 2002;3(4):469-478.
16. Ridley A. Rac and Rho. Curr Biol. 1999;9(5):R156.
17. Ridley AJ. Rho proteins, PI 3-kinases, and monocyte/macrophage motility. FEBS Lett. 2001;498(2):168-171.
18. Ridley A. Rho GTPases: integrating integrin signaling. J Cell Biol. 2000;150(4):F107-F109.
19. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature. 2002;420(6916):629-635.
20. Ridley AJ. The GTP-binding protein Rho. Int J Biochem Cell Biol. 1997;29(11):1225-1229.
21. Ishizaki T, Naito M, Fujisawa K, et al. p160ROCK, a Rho-associated coiled-coil forming protein kinase, works downstream of Rho and induces focal adhesions. FEBS Lett. 1997;404(2):118-124. (Pubitemid 27113436)
22. Riento K, Ridley AJ. Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol. 2003;4(6):446-456. (Pubitemid 36648590)
23. Matsui T, Amano M, Yamamoto T, et al. Rhoassociated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J. 1996;15(9):2208-2216. (Pubitemid 26141137)
24. Nakagawa O, Fujisawa K, Ishizaki T, Saito Y, Nakao K, Narumiya S. ROCK-I and ROCK-II, two isoforms of Rho-associated coiled-coil forming protein serine/threonine kinase in mice. FEBS Lett. 1996;392(2):189-193. (Pubitemid 26276745)
25. Amano M, Ito M, Kimura K, et al. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem. 1996;271(34):20246-20249. (Pubitemid 26281788)
26. Kawano Y, Fukata Y, Oshiro N, et al. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J Cell Biol. 1999;147(5):1023-1038.
27. Kureishi Y, Kobayashi S, Amano M, et al. Rhoassociated kinase directly induces smooth muscle contraction through myosin light chain phosphorylation. J Biol Chem. 1997;272(19):12257-12260. (Pubitemid 27203307)
28. Amano M, Chihara K, Kimura K, et al. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science. 1997;275(5304):1308-1311. (Pubitemid 27114159)
29. Arber S, Barbayannis FA, Hanser H, et al. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature. 1998;393(6687):805- 809. (Pubitemid 28299494)
30. Maekawa M, Ishizaki T, Boku S, et al. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science. 1999;285(5429):895-898. (Pubitemid 29381991)
31. Zhang YM, Bo J, Taffet GE, et al. Targeted deletion of ROCK1 protects the heart against pressure overload by inhibiting reactive fibrosis. FASEB J. 2006;20(7):916-925.
32. Meng F, Lowell CA. A beta 1 integrin signaling pathway involving Src-family kinases, Cbl and PI-3 kinase is required for macrophage spreading and migration. EMBO J. 1998;17(15):4391-4403. (Pubitemid 28362629)
33. Lowell CA, Berton G. Resistance to endotoxic shock and reduced neutrophil migration in mice deficient for the Src-family kinases Hck and Fgr. Proc Natl Acad Sci U S A. 1998;95(13):7580-7584. (Pubitemid 28293295)
34. Munugalavadla V, Borneo J, Ingram DA, Kapur R. p85alpha subunit of class IA PI-3 kinase is crucial for macrophage growth and migration. Blood. 2005;106(1):103-109. (Pubitemid 40967180)
35. Lowell CA, Berton G. Integrin signal transduction in myeloid leukocytes. J Leukoc Biol. 1999;65(3):313-320. (Pubitemid 29109702)
36. Suen PW, Ilic D, Caveggion E, Berton G, Damsky CH, Lowell CA. Impaired integrin-mediated signal transduction, altered cytoskeletal structure and reduced motility in Hck/Fgr deficient macrophages. J Cell Sci. 1999;112(22):4067-4078. (Pubitemid 30119775)
37. Roberts AW, Kim C, Zhen L, et al. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity. 1999;10(2):183-196. (Pubitemid 29115624)
38. Pradip D, Peng X, Durden DL. Rac2 specificity in macrophage integrin signaling: potential role for Syk kinase. J Biol Chem. 2003;278(43):41661-41669. (Pubitemid 37310423)
39. Yin J, Yu FS. Rho kinases regulate corneal epithelial wound healing. Am J Physiol Cell Physiol. 2008;295(2):C378-C387. (Pubitemid 352755785)
40. Sun H, Lesche R, Li DM, et al. PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway. Proc Natl Acad Sci U S A. 1999;96(11):6199-6204. (Pubitemid 29256643)
41. Mueller BK, Mack H, Teusch N. Rho kinase, a promising drug target for neurological disorders. Nat Rev Drug Discov. 2005;4(5):387-398. (Pubitemid 40704122)
42. Darenfed H, Dayanandan B, Zhang T, Hsieh SH, Fournier AE, Mandato CA. Molecular characterization of the effects of Y-27632. Cell Motil Cytoskeleton. 2007;64(2):97-109.
43. Subramanian KK, Jia Y, Zhu D, et al. Tumor suppressor PTEN is a physiologic suppressor of chemoattractant-mediated neutrophil functions. Blood. 2007;109(9):4028-4037. (Pubitemid 46641758)
44. Vazquez F, Ramaswamy S, Nakamura N, Sellers WR. Phosphorylation of the PTEN tail regulates protein stability and function. Mol Cell Biol. 2000;20(14):5010-5018. (Pubitemid 30431555)
45. Hall A, Paterson HF, Adamson P, Ridley AJ. Cellular responses regulated by rho-related small GTP-binding proteins. Philos Trans R Soc Lond B Biol Sci. 1993;340(1293):267-271.
46. Ridley AJ. Rho family proteins: coordinating cell responses. Trends Cell Biol. 2001;11(12):471-477.
47. Ridley AJ. Rho GTPases and cell migration. J Cell Sci. 2001;114(15):2713-2722.
48. 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 caspase-independent manner. J Exp Med. 2005;201(3):465-471. (Pubitemid 40229420)
49. Sebbagh M, Renvoize C, Hamelin J, Riche N, Bertoglio J, Breard J. Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat Cell Biol. 2001;3(4):346-352. (Pubitemid 32288441)
50. Mong PY, Wang Q. Activation of Rho kinase isoforms in lung endothelial cells during inflammation. J Immunol. 2009;182(4):2385-2394.
51. Yoneda A, Multhaupt HA, Couchman JR. The Rho kinases I and II regulate different aspects of myosin II activity. J Cell Biol. 2005;170(3):443-453. (Pubitemid 41126943)
52. Yoneda A, Ushakov D, Multhaupt HA, Couchman JR. Fibronectin matrix assembly requires distinct contributions from Rho kinases I and -II. Mol Biol Cell. 2007;18(1):66-75. (Pubitemid 46066711)
53. Riento K, Totty N, Villalonga P, Garg R, Guasch R, Ridley AJ. RhoE function is regulated by ROCK I-mediated phosphorylation. EMBO J. 2005;24(6):1170-1180. (Pubitemid 40516600)
54. Papakonstanti EA, Ridley AJ, Vanhaesebroeck B. The p110delta isoform of PI 3-kinase negatively controls RhoAand PTEN. EMBO J. 2007;26(13):3050-3061. (Pubitemid 47057501)
55. Suzuki A, Kaisho T, Ohishi M, et al. Critical roles of Pten in B cell homeostasis and immunoglobulin class switch recombination. J Exp Med. 2003;197(5):657-667. (Pubitemid 36314660)
56. Liliental J, Moon SY, Lesche R, et al. Genetic deletion of the Pten tumor suppressor gene promotes cell motility by activation of Rac1 and Cdc42 GTPases. Curr Biol. 2000;10(7):401-404. (Pubitemid 30213387)
57. Iijima M, Devreotes P. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell. 2002;109(5):599-610. (Pubitemid 34628723)
58. Lacalle RA, Gomez-Mouton C, Barber DF, et al. PTEN regulates motility but not directionality during leukocyte chemotaxis. J Cell Sci. 2004;117(25):6207-6215. (Pubitemid 40123984)
59. Kapoor M, Liu S, Shi-wen X, et al. GSK-3beta in mouse fibroblasts controls wound healing and fibrosis through an endothelin-1-dependent mechanism. J Clin Invest. 2008;118(10):3279-3290.
60. Neumeister P, Pixley FJ, Xiong Y, et al. Cyclin D1 governs adhesion and motility of macrophages. Mol Biol Cell. 2003;14(5):2005-2015. (Pubitemid 36583549)
61. Noma K, Rikitake Y, Oyama N, et al. ROCK1 mediates leukocyte recruitment and neointima formation following vascular injury. J Clin Invest. 2008;118(5):1632-1644.
62. Leenen PJ, de Bruijn MF, Voerman JS, Campbell PA, van Ewijk W. Markers of mouse macrophage development detected by monoclonal antibodies. J Immunol Methods. 1994;174(1):5-19.