The interplay between G protein-coupled receptor kinase 2 (GRK2) and histone deacetylase 6 (HDAC6) at the crossroads of epithelial cell motility

Cell Adhesion and Migration

Volumn 6, Issue 6, 2012, Pages 495-501

  Lafarga, Vanesa ^a,b   Mayor, Federico ^a,b   Penela, Petronila ^a,b  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas   (Spain)

Author keywords

Cell migration; GRK2; HDAC6; Microtubules; Polarity; Tubulin acetylation

Indexed keywords

ALPHA TUBULIN; G PROTEIN COUPLED RECEPTOR KINASE 2; HISTONE DEACETYLASE 6;

ACUTE GRANULOCYTIC LEUKEMIA; BREAST TUMOR; CANCER CELL; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELLULAR DISTRIBUTION; CHRONIC INFLAMMATION; DEACETYLATION; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; GENE OVEREXPRESSION; METASTASIS; MICROTUBULE ASSEMBLY; MOUTH CARCINOMA; NEOPLASM; NOTE; ORAL SQUAMOUS CARCINOMA; OVARY CARCINOMA; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

EID: 84872066649     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.21585     Document Type: Note

References (52)

1. Raman D, Sobolik-Delmaire T, Richmond A. Chemokines in health and disease. Exp Cell Res 2011; 317:575-89; PMID:21223965; http://dx.doi.org/10. 1016/j.yexcr.2011.01.005
2. Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011; 147:992-1009; PMID:22118458; http://dx.doi.org/10.1016/j.cell.2011.11.016
3. Kay RR, Langridge P, Traynor D, Hoeller O. Changing directions in the study of chemotaxis. Nat Rev Mol Cell Biol 2008; 9:455-63; PMID:18500256
4. Berzat A, Hall A. Cellular responses to extracellular guidance cues. EMBO J 2010; 29:2734-45; PMID: 20717143; http://dx.doi.org/10.1038/emboj.2010.170
5. Ritter SL, Hall RA. Fine-tuning of GPCR activity by receptor-interacting proteins. Nat Rev Mol Cell Biol 2009; 10:819-30; PMID:19935667; http://dx.doi.org/10.1038/nrm2803
6. Cotton M, Claing A. G protein-coupled receptors stimulation and the control of cell migration. Cell Signal 2009; 21:1045-53; PMID:19249352; http://dx.doi.org/10.1016/j.cellsig.2009.02.008
7. Moore CA, Milano SK, Benovic JL. Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 2007; 69:451-82; PMID:17037978; http://dx.doi.org/10.1146/annurev.physiol.69.022405.154712
8. Gurevich EV, Tesmer JJ, Mushegian A, Gurevich VV. G protein-coupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol Ther 2012; 133:40-69; PMID:21903131; http://dx.doi.org/10.1016/j.pharmthera.2011.08. 001
9. Liu X, Ma B, Malik AB, Tang H, Yang T, Sun B, et al. Bidirectional regulation of neutrophil migration by mitogen-activated protein kinases. Nat Immunol 2012; 13:457-64; PMID:22447027; http://dx.doi.org/10.1038/ni.2258
10. Penela P, Ribas C, Aymerich I, Mayor F, Jr. New roles of G protein-coupled receptor kinase 2 (GRK2) in cell migration. Cell Adh Migr 2009; 3:19-23; PMID: 19372742; http://dx.doi.org/10.4161/cam.3.1.7149
11. Arnon TI, Xu Y, Lo C, Pham T, An J, Coughlin S, et al. GRK2-dependent S1PR1 desensitization is required for lymphocytes to overcome their attraction to blood. Science 2011; 333:1898-903; PMID: 21960637; http://dx.doi.org/10.1126/ science.1208248
12. Penela P, Ribas C, Aymerich I, Eijkelkamp N, Barreiro O, Heijnen CJ, et al. G protein-coupled receptor kinase 2 positively regulates epithelial cell migration. EMBO J 2008; 27:1206-18; PMID:18369319; http://dx.doi.org/10.1038/ emboj.2008.55
13. Entschladen F, Gunzer M, Scheuffele CM, Niggemann B, Zänker KS. T lymphocytes and neutrophil granulocytes differ in regulatory signaling and migratory dynamics with regard to spontaneous locomotion and chemotaxis. Cell Immunol 2000; 199:104-14; PMID: 10698620; http://dx.doi.org/10.1006/cimm.1999. 1605
14. Niggemann B, Drell TL, 4th, Joseph J, Weidt C, Lang K, Zaenker KS, et al. Tumor cell locomotion: differential dynamics of spontaneous and induced migration in a 3D collagen matrix. Exp Cell Res 2004; 298:178-87; PMID:15242772; http://dx.doi.org/10.1016/j.yexcr.2004.04.001
15. Penela P, Murga C, Ribas C, Lafarga V, Mayor F, Jr. The complex G protein-coupled receptor kinase 2 (GRK2) interactome unveils new physiopathological targets. Br J Pharmacol 2010; 160:821-32; PMID: 20590581; http://dx.doi.org/10.1111/j.1476-5381.2010.00727.x
16. Cant SH, Pitcher JA. G protein-coupled receptor kinase 2-mediated phosphorylation of ezrin is required for G protein-coupled receptor-dependent reorganization of the actin cytoskeleton. Mol Biol Cell 2005; 16:3088-99; PMID:15843435; http://dx.doi.org/10.1091/mbc.E04-10-0877
17. Kahsai AW, Zhu S, Fenteany G. G protein-coupled receptor kinase 2 activates radixin, regulating membrane protrusion and motility in epithelial cells. Biochim Biophys Acta 2010; 1803:300-10; PMID: 19913059; http://dx.doi.org/10.1016/j.bbamcr.2009.11.002
18. Siegrist SE, Doe CQ. Microtubule-induced cortical cell polarity. Genes Dev 2007; 21:483-96; PMID: 17344411; http://dx.doi.org/10.1101/gad.1511207
19. Etienne-Manneville S. From signaling pathways to microtubule dynamics: the key players. Curr Opin Cell Biol 2010; 22:104-11; PMID:20031384; http://dx.doi.org/10.1016/j.ceb.2009.11.008
20. Watanabe T, Noritake J, Kaibuchi K. Regulation of microtubules in cell migration. Trends Cell Biol 2005; 15:76-83; PMID:15695094; http://dx.doi.org/10. 1016/j.tcb.2004.12.006
21. Wadsworth P. Regional regulation of microtubule dynamics in polarized, motile cells. Cell Motil Cytoskeleton 1999; 42:48-59; PMID:9915584; http://dx.doi.org/10.1002/(SICI)1097-0169(1999)42:1〈48::AID-CM5〉3.0. CO;2-8
22. Zilberman Y, Ballestrem C, Carramusa L, Mazitschek R, Khochbin S, Bershadsky A. Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6. J Cell Sci 2009; 122:3531-41; PMID: 19737819; http://dx.doi.org/10.1242/jcs.046813
23. Valenzuela-Fernández A, Cabrero JR, Serrador JM, Sánchez-Madrid F. HDAC6: a key regulator of cytoskeleton, cell migration and cell-cell interactions. Trends Cell Biol 2008; 18:291-7; PMID:18472263; http://dx.doi.org/10.1016/j.tcb.2008.04.003
24. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, et al. HDAC6 is a microtubule-associated deacetylase. Nature 2002; 417:455-8; PMID: 12024216; http://dx.doi.org/10.1038/417455a
25. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci U S A 2003; 100:4389-94; PMID:12677000; http://dx.doi.org/10.1073/pnas.0430973100
26. Lafarga V, Aymerich I, Tapia O, Mayor F, Jr., Penela P. A novel GRK2/HDAC6 interaction modulates cell spreading and motility. EMBO J 2012; 31:856-69; PMID:22193721; http://dx.doi.org/10.1038/emboj.2011.466
27. Zhang X, Yuan Z, Zhang Y, Yong S, Salas-Burgos A, Koomen J, et al. HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol Cell 2007; 27:197-213; PMID:17643370; http://dx.doi.org/10.1016/j.molcel.2007.05.033
28. Gao YS, Hubbert CC, Lu J, Lee YS, Lee JY, Yao TP. Histone deacetylase 6 regulates growth factor-induced actin remodeling and endocytosis. Mol Cell Biol 2007; 27:8637-47; PMID:17938201; http://dx.doi.org/10.1128/MCB.00393-07
29. Luo J, Benovic JL. G protein-coupled receptor kinase interaction with Hsp90 mediates kinase maturation. J Biol Chem 2003; 278:50908-14; PMID:14557268; http://dx.doi.org/10.1074/jbc.M307637200
30. Cabrero JR, Serrador JM, Barreiro O, Mittelbrunn M, Naranjo-Suárez S, Martín-Cófreces N, et al. Lymphocyte chemotaxis is regulated by histone deacetylase 6, independently of its deacetylase activity. Mol Biol Cell 2006; 17:3435-45; PMID:16738306; http://dx.doi.org/10.1091/mbc.E06-01-0008
31. Boyault C, Zhang Y, Fritah S, Caron C, Gilquin B, Kwon SH, et al. HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes Dev 2007; 21:2172-81; PMID: 17785525; http://dx.doi.org/10. 1101/gad.436407
32. Kaluza D, Kroll J, Gesierich S, Yao TP, Boon RA, Hergenreider E, et al. Class IIb HDAC6 regulates endothelial cell migration and angiogenesis by deacetylation of cortactin. EMBO J 2011; 30:4142-56; PMID:21847094; http://dx.doi.org/10.1038/emboj.2011.298
33. Aldana-Masangkay GI, Sakamoto KM. The role of HDAC6 in cancer. J Biomed Biotech 2011; 2011: 875824; http://dx.doi.org/10.1155/2011/875824
34. Métayé T, Gibelin H, Perdrisot R, Kraimps JL. Pathophysiological roles of G-protein-coupled receptor kinases. Cell Signal 2005; 17:917-28; PMID:15894165; http://dx.doi.org/10.1016/j.cellsig.2005.01.002
35. Salcedo A, Mayor F, Jr., Penela P. Mdm2 is involved in the ubiquitination and degradation of G-protein-coupled receptor kinase 2. EMBO J 2006; 25:4752-62; PMID:17006543; http://dx.doi.org/10.1038/sj.emboj.7601351
36. Bookout AL, Finney AE, Guo R, Peppel K, Koch WJ, Daaka Y. Targeting Gbetagamma signaling to inhibit prostate tumor formation and growth. J Biol Chem 2003; 278:37569-73; PMID:12869546; http://dx.doi.org/10.1074/jbc.M306276200
37. Kirui JK, Xie Y, Wolff DW, Jiang H, Abel PW, Tu Y. Gbetagamma signaling promotes breast cancer cell migration and invasion. J Pharmacol Exp Ther 2010; 333:393-403; PMID:20110378; http://dx.doi.org/10.1124/jpet.109.164814
38. Dickinson M, Johnstone RW, Prince HM. Histone deacetylase inhibitors: potential targets responsible for their anti-cancer effect. Invest New Drugs 2010; 28 (Suppl 1):S3-20; PMID:21161327; http://dx.doi.org/10.1007/s10637-010- 9596-y
39. Butler KV, Kalin J, Brochier C, Vistoli G, Langley B, Kozikowski AP. Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J Am Chem Soc 2010; 132:10842-6; PMID:20614936; http://dx.doi.org/10.1021/ja102758v
40. Inks ES, Josey BJ, Jesinkey SR, Chou CJ. A novel class of small molecule inhibitors of HDAC6. ACS Chem Biol 2012; 7:331-9; PMID:22047054; http://dx.doi.org/10.1021/cb200134p
41. Bali P, Pranpat M, Bradner J, Balasis M, Fiskus W, Guo F, et al. Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis for antileukemia activity of histone deacetylase inhibitors. J Biol Chem 2005; 280:26729-34; PMID:15937340; http://dx.doi.org/10.1074/jbc.C500186200
42. Lodowski DT, Pitcher JA, Capel WD, Lefkowitz RJ, Tesmer JJ. Keeping G proteins at bay: a complex between G protein-coupled receptor kinase 2 and Gbetagamma. Science 2003; 300:1256-62; PMID: 12764189; http://dx.doi.org/10. 1126/science.1082348
43. Tesmer JJ, Tesmer VM, Lodowski DT, Steinhagen H, Huber J. Structure of human G protein-coupled receptor kinase 2 in complex with the kinase inhibitor balanol. J Med Chem 2010; 53:1867-70; PMID: 20128603; http://dx.doi.org/10.1021/ jm9017515
44. Thal DM, Yeow RY, Schoenau C, Huber J, Tesmer JJ. Molecular mechanism of selectivity among G protein-coupled receptor kinase 2 inhibitors. Mol Pharmacol 2011; 80:294-303; PMID:21596927; http://dx.doi.org/10.1124/mol.111.071522
45. Vroon A, Heijnen CJ, Kavelaars A. GRKs and arrestins: regulators of migration and inflammation. J Leukoc Biol 2006; 80:1214-21; PMID:16943386; http://dx.doi.org/10.1189/jlb.0606373
46. Fan J, Malik AB. Toll-like receptor-4 (TLR4) signaling augments chemokine-induced neutrophil migration by modulating cell surface expression of chemokine receptors. Nat Med 2003; 9:315-21; PMID: 12592402; http://dx.doi.org/10.1038/nm832
47. Peppel K, Zhang L, Huynh TT, Huang X, Jacobson A, Brian L, et al. Overexpression of G protein-coupled receptor kinase-2 in smooth muscle cells reduces neointimal hyperplasia. J Mol Cell Cardiol 2002; 34: 1399-409; PMID:12393000; http://dx.doi.org/10.1006/jmcc.2002.2092
48. Guo J, Chen H, Ho J, Mancini J, Sontag T, Laporte SA, et al. TGFbeta-induced GRK2 expression attenuates AngII-regulated vascular smooth muscle cell proliferation and migration. Cell Signal 2009; 21:899-905; PMID: 19385060; http://dx.doi.org/10.1016/j.cellsig.2009.01.037
49. Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, et al. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 2002; 109:873-85; PMID:12110184; http://dx.doi.org/10.1016/S0092-8674(02)00800-0
50. Kaverina I, Krylyshkina O, Small JV. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol 1999; 146:1033-44; PMID:10477757; http://dx.doi.org/10.1083/jcb.146.5.1033
51. Tesmer VM, Lennarz S, Mayer G, Tesmer JJG. Molecular mechanisms for inhibition of G protein-coupled receptor kinase 2 by a selective RNA aptamer. Structure 2012; 20:1300-9; PMID:22727813; http://dx.doi.org/10.1016/j.str.2012. 05.002
52. Iino M, Furugori T, Mori T, Moriyama S, Fukuzawa A, Shibano T. Rational design and evaluation of new lead compound structures for selective betaARK1 inhibitors. J Med Chem 2002; 45:2150-9; PMID: 12014953; http://dx.doi.org/10. 1021/jm010093a