From the membrane to the nucleus and back again: bifunctional focal adhesion proteins

Current Opinion in Cell Biology

Volumn 18, Issue 5, 2006, Pages 524-532

  Hervy, Martial ^a   Hoffman, Laura ^a   Beckerle, Mary C ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; CELL PROTEIN; CYSTEINE RICH PROTEIN 61; INTEGRIN; LIM PROTEIN; PAXILLIN; PROTEIN FHL1; PROTEIN FHL2; PROTEIN FHL3; PROTEIN FHL4; PROTEIN ICAP 1ALPHA; UNCLASSIFIED DRUG; ZYXIN;

CELL ADHESION; CELL COMMUNICATION; CELL MEMBRANE; CELL MOTILITY; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; FOCAL ADHESION; GENE EXPRESSION REGULATION; HUMAN; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW;

ANIMALS; CELL MEMBRANE; CELL NUCLEUS; CELL-MATRIX JUNCTIONS; GENE EXPRESSION REGULATION; HUMANS; INTEGRINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; METALLOPROTEINS; MUSCLE PROTEINS; NUCLEAR PROTEINS; PAXILLIN; PROTO-ONCOGENE PROTEINS C-ABL;

EID: 33748291515     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2006.08.006     Document Type: Review

References (65)

1. Schwartz M.A., and Assoian R.K. Integrins and cell proliferation: regulation of cyclin-dependent kinases via cytoplasmic signaling pathways. J Cell Sci 114 (2001) 2553-2560
2. Schmidhauser C., Casperson G.F., Myers C.A., Sanzo K.T., Bolten S., and Bissell M.J. A novel transcriptional enhancer is involved in the prolactin- and extracellular matrix-dependent regulation of β-casein gene expression. Mol Biol Cell 3 (1992) 699-709
3. Martin-Bermudo M.D., and Brown N.H. Uncoupling integrin adhesion and signaling: the betaPS cytoplasmic domain is sufficient to regulate gene expression in the Drosophila embryo. Genes Dev 13 (1999) 729-739
4. Pabla R., Weyrich A.S., Dixon D.A., Bray P.F., McIntyre T.M., Prescott S.M., and Zimmerman G.A. Integrin-dependent control of translation: engagement of integrin alphaIIbbeta3 regulates synthesis of proteins in activated human platelets. J Cell Biol 144 (1999) 175-184
5. Denis M.M., Tolley N.D., Bunting M., Schwertz H., Jiang H., Lindemann S., Yost C.C., Rubner F.J., Albertine K.H., Swoboda K.J., et al. Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell 122 (2005) 379-391. This paper provides evidence that integrin engagement influences pre-mRNA splicing in platelets.
6. Chicurel M.E., Singer R.H., Meyer C.J., and Ingber D.E. Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature 392 (1998) 730-733
7. Miralles F., Posern G., Zaromytidou A.I., and Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113 (2003) 329-342
8. Yoshigi M., Hoffman L.M., Jensen C.C., Yost H.J., and Beckerle M.C. Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J Cell Biol 171 (2005) 209-215
9. Somogyi K., and Rorth P. Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. Dev Cell 7 (2004) 85-93
10. Zamir E., and Geiger B. Molecular complexity and dynamics of cell-matrix adhesions. J Cell Sci 114 (2001) 3583-3590
11. Kadrmas J.L., and Beckerle M.C. The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol 5 (2004) 920-931. This review of LIM domain proteins describes their roles in communication between the nucleus and cytoplasm.
12. Nix D.A., and Beckerle M.C. Nuclear-cytoplasmic shuttling of the focal contact protein, zyxin: a potential mechanism for communication between sites of cell adhesion and the nucleus. J Cell Biol 138 (1997) 1139-1147
13. Fradelizi J., Noireaux V., Plastino J., Menichi B., Louvard D., Sykes C., Golsteyn R.M., and Friederich E. ActA and human zyxin harbour Arp2/3-independent actin-polymerization activity. Nat Cell Biol 3 (2001) 699-707
14. Hoffman L.M., Jensen C.C., Kloeker S., Wang C.L., Yoshigi M., and Beckerle M.C. Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling. J Cell Biol 172 (2006) 771-782
15. Zeile W.L., Condit R.C., Lewis J.I., Purich D.L., and Southwick F.S. Vaccinia locomotion in host cells: evidence for the universal involvement of actin-based motility sequences ABM-1 and ABM-2. Proc Natl Acad Sci U S A 95 (1998) 13917-13922
16. Degenhardt Y.Y., and Silverstein S. Interaction of zyxin, a focal adhesion protein, with the e6 protein from human papillomavirus type 6 results in its nuclear translocation. J Virol 75 (2001) 11791-11802
17. Kato T., Muraski J., Chen Y., Tsujita Y., Wall J., Glembotski C.C., Schaefer E., Beckerle M., and Sussman M.A. Atrial natriuretic peptide promotes cardiomyocyte survival by cGMP-dependent nuclear accumulation of zyxin and Akt. J Clin Invest 115 (2005) 2716-2730. This paper provides evidence that nuclear targeting of zyxin influences cell survival.
18. Cattaruzza M., Lattrich C., and Hecker M. Focal adhesion protein zyxin is a mechanosensitive modulator of gene expression in vascular smooth muscle cells. Hypertension 43 (2004) 726-730. This paper reports a role for zyxin in the transcriptional response to mechanical stress in vascular smooth muscle cells.
19. Morinobu M., Nakamoto T., Hino K., Tsuji K., Shen Z.J., Nakashima K., Nifuji A., Yamamoto H., Hirai H., and Noda M. The nucleocytoplasmic shuttling protein CIZ reduces adult bone mass by inhibiting bone morphogenetic protein-induced bone formation. J Exp Med 201 (2005) 961-970
20. Janssen H., and Marynen P. Interaction partners for human ZNF384/CIZ/NMP4-zyxin as a mediator for p130CAS signaling?. Exp Cell Res (2006)
21. Yi J., Kloeker S., Jensen C.C., Bockholt S., Honda H., Hirai H., and Beckerle M.C. Members of the Zyxin family of LIM proteins interact with members of the p130Cas family of signal transducers. J Biol Chem 277 (2002) 9580-9589
22. Guo B., Sallis R.E., Greenall A., Petit M.M., Jansen E., Young L., Van de Ven W.J., and Sharrocks A.D. The LIM domain protein LPP is a coactivator for the ETS domain transcription factor PEA3. Mol Cell Biol 26 (2006) 4529-4538. This paper provides the first evidence of a nuclear function for LPP, showing how the protein can modulate gene transcription.
23. Lee J.W., Choi H.S., Gyuris J., Brent R., and Moore D.D. Two classes of proteins dependent on either the presence or absence of thyroid hormone for interaction with the thyroid hormone receptor. Mol Endocrinol 9 (1995) 243-254
24. Kassel O., Schneider S., Heilbock C., Litfin M., Gottlicher M., and Herrlich P. A nuclear isoform of the focal adhesion LIM-domain protein Trip6 integrates activating and repressing signals at AP-1- and NF-kappaB-regulated promoters. Genes Dev 18 (2004) 2518-2528. This paper provides compelling evidence for a transcriptional role of a TRIP6 isoform and illustrates how a LIM scaffolding protein can contribute to the switch from activation to repression.
25. Brown M.C., and Turner C.E. Paxillin: adapting to change. Physiol Rev 84 (2004) 1315-1339
26. Gustavsson A., Yuan M., and Fallman M. Temporal dissection of β1-integrin signaling indicates a role for p130Cas-Crk in filopodia formation. J Biol Chem 279 (2004) 22893-22901
27. Woods A.J., Kantidakis T., Sabe H., Critchley D.R., and Norman J.C. Interaction of paxillin with poly(A)-binding protein 1 and its role in focal adhesion turnover and cell migration. Mol Cell Biol 25 (2005) 3763-3773. This paper provides an elegant demonstration of paxillin's role in chaperoning mRNA-protein complexes from the nucleus to particular subcellular domains within the cytoplasm.
28. de Hoog C.L., Foster L.J., and Mann M. RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell 117 (2004) 649-662. The authors use an innovative approach to identify ribonucleoprotein complexes assembled upon cell-matrix adhesion.
29. Mingle L.A., Okuhama N.N., Shi J., Singer R.H., Condeelis J., and Liu G. Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J Cell Sci 118 (2005) 2425-2433
30. Condeelis J., and Singer R.H. How and why does β-actin mRNA target?. Biol Cell 97 (2005) 97-110
31. Yang L., Guerrero J., Hong H., DeFranco D.B., and Stallcup M.R. Interaction of the tau2 transcriptional activation domain of glucocorticoid receptor with a novel steroid receptor coactivator, Hic-5, which localizes to both focal adhesions and the nuclear matrix. Mol Biol Cell 11 (2000) 2007-2018
32. Kasai M., Guerrero-Santoro J., Friedman R., Leman E.S., Getzenberg R.H., and DeFranco D.B. The Group 3 LIM domain protein paxillin potentiates androgen receptor transactivation in prostate cancer cell lines. Cancer Res 63 (2003) 4927-4935
33. Saelzler MP, Spackman CC, Liu Y, Martinez LC, Harris JP, Abe MK: ERK8 down-regulates transactivation of the glucocorticoid receptor through Hic-5. J Biol Chem 2006. in press.
34. Ghogomu S.M., van Venrooy S., Ritthaler M., Wedlich D., and Gradl D. HIC-5 is a novel repressor of lymphoid enhancer factor/T-cell factor-driven transcription. J Biol Chem 281 (2006) 1755-1764
35. Shibanuma M., Kim-Kaneyama J.R., Sato S., and Nose K. A LIM protein, Hic-5, functions as a potential coactivator for Sp1. J Cell Biochem 91 (2004) 633-645
36. Kim-Kaneyama J.R., Suzuki W., Ichikawa K., Ohki T., Kohno Y., Sata M., Nose K., and Shibanuma M. Uni-axial stretching regulates intracellular localization of Hic-5 expressed in smooth-muscle cells in vivo. J Cell Sci 118 (2005) 937-949
37. Shibanuma M., Kim-Kaneyama J.R., Ishino K., Sakamoto N., Hishiki T., Yamaguchi K., Mori K., Mashimo J., and Nose K. Hic-5 communicates between focal adhesions and the nucleus through oxidant-sensitive nuclear export signal. Mol Biol Cell 14 (2003) 1158-1171
38. Wu R.F., Xu Y.C., Ma Z., Nwariaku F.E., Sarosi Jr. G.A., and Terada L.S. Subcellular targeting of oxidants during endothelial cell migration. J Cell Biol 171 (2005) 893-904. This paper reports on the interaction of Hic-5 with TRAF4, suggesting a function for Hic-5 in the regulation of reactive oxygen species at focal adhesions.
39. Louis H.A., Pino J.D., Schmeichel K.L., Pomies P., and Beckerle M.C. Comparison of three members of the cysteine-rich protein family reveals functional conservation and divergent patterns of gene expression. J Biol Chem 272 (1997) 27484-27491
40. Sadler I., Crawford A.W., Michelsen J.W., and Beckerle M.C. Zyxin and cCRP: two interactive LIM domain proteins associated with the cytoskeleton. J Cell Biol 119 (1992) 1573-1587
41. Knoll R., Hoshijima M., and Chien K. Cardiac mechanotransduction and implications for heart disease. J Mol Med 81 (2003) 750-756
42. Chang D.F., Belaguli N.S., Iyer D., Roberts W.B., Wu S.P., Dong X.R., Marx J.G., Moore M.S., Beckerle M.C., Majesky M.W., et al. Cysteine-rich LIM-only proteins CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev Cell 4 (2003) 107-118
43. Kong Y., Shelton J.M., Rothermel B., Li X., Richardson J.A., Bassel-Duby R., and Williams R.S. Cardiac-specific LIM protein FHL2 modifies the hypertrophic response to beta-adrenergic stimulation. Circulation 103 (2001) 2731-2738
44. Gunther T., Poli C., Muller J.M., Catala-Lehnen P., Schinke T., Yin N., Vomstein S., Amling M., and Schule R. Fhl2 deficiency results in osteopenia due to decreased activity of osteoblasts. Embo J 24 (2005) 3049-3056
45. Morlon A., and Sassone-Corsi P. The LIM-only protein FHL2 is a serum-inducible transcriptional coactivator of AP-1. Proc Natl Acad Sci U S A 100 (2003) 3977-3982
46. Coghill I.D., Brown S., Cottle D.L., McGrath M.J., Robinson P.A., Nandurkar H.H., Dyson J.M., and Mitchell C.A. FHL3 is an actin-binding protein that regulates alpha-actinin-mediated actin bundling: FHL3 localizes to actin stress fibers and enhances cell spreading and stress fiber disassembly. J Biol Chem 278 (2003) 24139-24152
47. Muller J.M., Metzger E., Greschik H., Bosserhoff A.K., Mercep L., Buettner R., and Schule R. The transcriptional coactivator FHL2 transmits Rho signals from the cell membrane into the nucleus. Embo J 21 (2002) 736-748
48. Johannessen M., Moller S., Hansen T., Moens U., and Van Ghelue M. The multifunctional roles of the four-and-a-half-LIM only protein FHL2. Cell Mol Life Sci 63 (2006) 268-284
49. Bouvard D., Vignoud L., Dupe-Manet S., Abed N., Fournier H.N., Vincent-Monegat C., Retta S.F., Fassler R., and Block M.R. Disruption of focal adhesions by integrin cytoplasmic domain-associated protein-1 α. J Biol Chem 278 (2003) 6567-6574
50. Degani S., Balzac F., Brancaccio M., Guazzone S., Retta S.F., Silengo L., Eva A., and Tarone G. The integrin cytoplasmic domain-associated protein ICAP-1 binds and regulates Rho family GTPases during cell spreading. J Cell Biol 156 (2002) 377-387
51. Fournier H.N., Dupe-Manet S., Bouvard D., Luton F., Degani S., Block M.R., Retta S.F., and Albiges-Rizo C. Nuclear translocation of integrin cytoplasmic domain-associated protein 1 stimulates cellular proliferation. Mol Biol Cell 16 (2005) 1859-1871. This paper shows that the integrin partner ICAP-1α shuttles to the nucleus where it can influence gene expression.
52. Hernandez S.E., Krishnaswami M., Miller A.L., and Koleske A.J. How do Abl family kinases regulate cell shape and movement?. Trends Cell Biol 14 (2004) 36-44
53. Lewis J.M., Baskaran R., Taagepera S., Schwartz M.A., and Wang J.Y. Integrin regulation of c-Abl tyrosine kinase activity and cytoplasmic-nuclear transport. Proc Natl Acad Sci U S A 93 (1996) 15174-15179
54. Lewis J.M., and Schwartz M.A. Integrins regulate the association and phosphorylation of paxillin by c-Abl. J Biol Chem 273 (1998) 14225-14230
55. Leng Y., Zhang J., Badour K., Arpaia E., Freeman S., Cheung P., Siu M., and Siminovitch K. Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc Natl Acad Sci U S A 102 (2005) 1098-1103
56. Kain K.H., Gooch S., and Klemke R.L. Cytoplasmic c-Abl provides a molecular 'Rheostat' controlling carcinoma cell survival and invasion. Oncogene 22 (2003) 6071-6080
57. Wang J.Y. Nucleo-cytoplasmic communication in apoptotic response to genotoxic and inflammatory stress. Cell Res 15 (2005) 43-48
58. Vigneri P., and Wang J.Y. Induction of apoptosis in chronic myelogenous leukemia cells through nuclear entrapment of BCR-ABL tyrosine kinase. Nat Med 7 (2001) 228-234
59. Bai J., Uehara Y., and Montell D.J. Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103 (2000) 1047-1058
60. Nix D.A., Fradelizi J., Bockholt S., Menichi B., Louvard D., Friederich E., and Beckerle M.C. Targeting of zyxin to sites of actin membrane interaction and to the nucleus. J Biol Chem 276 (2001) 34759-34767
61. Petit M.M., Fradelizi J., Golsteyn R.M., Ayoubi T.A., Menichi B., Louvard D., Van de Ven W.J., and Friederich E. LPP, an actin cytoskeleton protein related to zyxin, harbors a nuclear export signal and transcriptional activation capacity. Mol Biol Cell 11 (2000) 117-129
62. Wang Y., and Gilmore T.D. LIM domain protein Trip6 has a conserved nuclear export signal, nuclear targeting sequences, and multiple transactivation domains. Biochim Biophys Acta 1538 (2001) 260-272
63. Woods A.J., Roberts M.S., Choudhary J., Barry S.T., Mazaki Y., Sabe H., Morley S.J., Critchley D.R., and Norman J.C. Paxillin associates with poly(A)-binding protein 1 at the dense endoplasmic reticulum and the leading edge of migrating cells. J Biol Chem 277 (2002) 6428-6437
64. Taagepera S., McDonald D., Loeb J.E., Whitaker L.L., McElroy A.K., Wang J.Y., and Hope T.J. Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc Natl Acad Sci U S A 95 (1998) 7457-7462
65. Yoshida K., and Miki Y. Enabling death by the Abl tyrosine kinase: mechanisms for nuclear shuttling of c-Abl in response to DNA damage. Cell Cycle 4 (2005) 777-779