Definition of a consensus integrin adhesome and its dynamics during adhesion complex assembly and disassembly

Nature Cell Biology

Volumn 17, Issue 12, 2015, Pages 1577-1587

  Horton, Edward R ^a   Byron, Adam ^a,b   Askari, Janet A ^a   Ng, Daniel H J ^a   Millon Frémillon, Angélique ^a   Robertson, Joseph ^a   Koper, Ewa J ^a   Paul, Nikki R ^a   Warwood, Stacey ^c   Knight, David ^c   Humphries, Jonathan D ^a   Humphries, Martin J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; CALDESMON; FIBRONECTIN; FOCAL ADHESION KINASE; INTEGRIN; INTEGRIN ADHESION COMPLEX; INTEGRIN LINKED KINASE; KINDLIN; META ADHESOME; MULTIPROTEIN COMPLEX; MYOSIN II; PAXILLIN; PINCH PROTEIN; PROTEOME; TALIN; UNCLASSIFIED DRUG; VASP PROTEIN; VINCULIN; ZYXIN; ACTININ; NOCODAZOLE; TUBULIN MODULATOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEOMICS; ANIMAL; CELL CULTURE; CLASSIFICATION; CLUSTER ANALYSIS; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; FOCAL ADHESION; IMMUNOBLOTTING; K-562 CELL LINE; KINETICS; MASS SPECTROMETRY; METABOLISM; PROCEDURES; TUMOR CELL LINE;

ACTININ; ANIMALS; CELL ADHESION; CELL LINE, TUMOR; CELLS, CULTURED; CLUSTER ANALYSIS; FOCAL ADHESIONS; HUMANS; IMMUNOBLOTTING; INTEGRINS; K562 CELLS; KINETICS; MASS SPECTROMETRY; MICE; MICROSCOPY, FLUORESCENCE; NOCODAZOLE; PAXILLIN; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; TALIN; TUBULIN MODULATORS; VINCULIN; ZYXIN;

EID: 84948718179     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3257     Document Type: Article

References (70)

1. Hynes, R. O. Integrins: bidirectional, allosteric signaling machines. Cell. 110, 673-687 (2002).
2. Liu, S., Calderwood, D. A., & Ginsberg, M. H. Integrin cytoplasmic domain-binding proteins. J. Cell Sci. 113, 3563-3571 (2000).
3. Morse, E. M., Brahme, N. N., & Calderwood, D. A. Integrin cytoplasmic tail interactions. Biochemistry (Mosc.) 53, 810-820 (2014).
4. Winograd-Katz, S. E., Fässler, R., Geiger, B., & Legate, K. R. The integrin adhesome: from genes and proteins to human disease. Nat. Rev. Mol. Cell Biol. 15, 273-288 (2014).
5. Zaidel-Bar, R., & Geiger, B. The switchable integrin adhesome. J. Cell Sci. 123, 1385-1388 (2010).
6. Zaidel-Bar, R., Itzkovitz, S., Maayan, A., Iyengar, R., & Geiger, B. Functional atlas of the integrin adhesome. Nat. Cell Biol. 9, 858-867 (2007).
7. Byron, A., Humphries, J. D., Bass, M. D., Knight, D., & Humphries, M. J. Proteomic analysis of integrin adhesion complexes. Sci. Signal. 4, pt2 (2011).
8. Byron, A., Humphries, J. D., Craig, S. E., Knight, D., & Humphries, M. J. Proteomic analysis of 4 1 integrin adhesion complexes reveals-subunit-dependent protein recruitment. Proteomics. 12, 2107-2114 (2012).
9. Byron, A., et al. A proteomic approach reveals integrin activation state-dependent control of microtubule cortical targeting. Nat. Commun. 6, 6135 (2015).
10. Huang, I.-H., et al. GEF-H1 controls focal adhesion signaling that regulates mesenchymal stem cell lineage commitment. J. Cell Sci. 127, 4186-4200 (2014).
11. Humphries, J. D., et al. Proteomic analysis of integrin-Associated complexes identifies RCC2 as a dual regulator of Rac1 and Arf6. Sci. Signal. 2, ra51 (2009).
12. Kuo, J.-C., Han, X., Hsiao, C.-T., Yates, J. R., & Waterman, C. M. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 13, 383-393 (2011).
13. Ng, D. H. J., Humphries, J. D., Byron, A., Millon-Frémillon, A., & Humphries, M. J. Microtubule-dependent modulation of adhesion complex composition. PLoS ONE. 9, e115213 (2014).
14. Robertson, J., et al. Defining the phospho-Adhesome through the phosphoproteomic analysis of integrin signalling. Nat. Commun. 6, 6265 (2015).
15. Schiller, H. B., Friedel, C. C., Boulegue, C., & Fässler, R. Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep. 12, 259-266 (2011).
16. Schiller, H. B., et al. 1- And v-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat. Cell Biol. 15, 625-636 (2013).
17. Yue, J., et al. Microtubules regulate focal adhesion dynamics through MAP4K4. Dev. Cell. 31, 572-585 (2014).
18. Jones, M. C., et al. Isolation of integrin-based adhesion complexes. Curr. Protoc. Cell Biol. 66, 9.8.1-9.8.15 (2015).
19. Kuo, J.-C., Han, X., Yates, J. R., & Waterman, C. M. Isolation of focal adhesion proteins for biochemical and proteomic analysis. Methods Mol. Biol. 757, 297-323 (2012).
20. Humphries, J. D., Paul, N. R., Humphries, M. J., & Morgan, M. R. Emerging properties of adhesion complexes: what are they and what do they do?. Trends Cell Biol. 25, 388-397 (2015).
21. Geiger, T., & Zaidel-Bar, R. Opening the floodgates: proteomics and the integrin adhesome. Curr. Opin. Cell Biol. 25, 562-568 (2012).
22. Smith, M. A., Hoffman, L. M., & Beckerle, M. C. LIM proteins in actin cytoskeleton mechanoresponse. Trends Cell Biol. 24, 575-583 (2014).
23. Uemura, A., Nguyen, T.-N., Steele, A. N., & Yamada, S. The LIM domain of zyxin is sufficient for force-induced accumulation of zyxin during cell migration. Biophys. J. 101, 1069-1075 (2011).
24. Schiller, H. B., & Fässler, R. Mechanosensitivity and compositional dynamics of cellmatrix adhesions. EMBO Rep. 14, 509-519 (2013).
25. Rolland, T., et al. A proteome-scale map of the human interactome network. Cell. 159, 1212-1226 (2014).
26. Janovick, J. A., Natarajan, K., Longo, F., & Conn, P. M. Caldesmon: a bifunctional (calmodulin and actin) binding protein which regulates stimulated gonadotropin release. Endocrinology. 129, 68-74 (1991).
27. Manders, E. M. M., Verbeek, F. J., & Aten, J. A. Measurement of co-localization of objects in dual-colour confocal images. J. Microsc. 169, 375-382 (1993).
28. Dougherty, G. W., Jose, C., Gimona, M., & Cutler, M. L. The Rsu-1-PINCH1-ILK complex is regulated by Ras activation in tumor cells. Eur. J. Cell Biol. 87, 721-734 (2008).
29. Attanasio, F., et al. Novel invadopodia components revealed by differential proteomics analysis. Eur. J. Cell Biol. 90, 115-127 (2011).
30. Cervero, P., Himmel, M., Krüger, M., & Linder, S. Proteomic analysis of podosome fractions from macrophages reveals similarities to spreading initiation centres. Eur. J. Cell Biol. 91, 908-922 (2012).
31. de Hoog, C. L., Foster, L. J., & Mann, M. RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell. 117, 649-662 (2004).
32. Ezratty, E. J., Partridge, M. A., & Gundersen, G. G. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7, 581-590 (2005).
33. Beggs, A. H., et al. Cloning and characterization of two human skeletal muscle-Actinin genes located on chromosomes 1 and 11. J. Biol. Chem. 267, 9281-9288 (1992).
34. Bialkowska, K., et al. The integrin co-Activator Kindlin-3 is expressed and functional in a non-hematopoietic cell, the endothelial cell. J. Biol. Chem. 285, 18640-18649 (2010).
35. Karaköse, E., Schiller, H. B., & Fässler, R. The kindlins at a glance. J. Cell Sci. 123, 2353-2356 (2010).
36. Zhang, Y., et al. Nuclear SIPA1 activates integrin 1 promoter and promotes invasion of breast cancer cells. Oncogene. 34, 1451-1462 (2015).
37. Bai, S. W., et al. Identification and characterization of a set of conserved and new regulators of cytoskeletal organization, cell morphology and migration. BMC Biol. 9, 54 (2011).
38. Buxbaum, A. R., Wu, B., & Singer, R. H. Single-Actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science. 343, 419-422 (2014).
39. Chicurel, M. E., Singer, R. H., Meyer, C. J., & Ingber, D. E. Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature. 392, 730-733 (1998).
40. Katz, Z. B., et al.-Actin mRNA compartmentalization enhances focal adhesion stability and directs cell migration. Genes Dev. 26, 1885-1890 (2012).
41. Willett, M., Pollard, H. J., Vlasak, M., & Morley, S. J. Localization of ribosomes and translation initiation factors to talin/ 3-integrin-enriched adhesion complexes in spreading and migrating mammalian cells. Biol. Cell. 102, 265-276 (2010).
42. Willett, M., Brocard, M., Davide, A., & Morley, S. J. Translation initiation factors and active sites of protein synthesis co-localize at the leading edge of migrating fibroblasts. Biochem. J. 438, 217-227 (2011).
43. Mellacheruvu, D., et al. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat. Methods. 10, 730-736 (2013).
44. Bachir, A. I., et al. Integrin-Associated complexes form hierarchically with variable stoichiometry in nascent adhesions. Curr. Biol. 24, 1845-1853 (2014).
45. Etheridge, T., et al. The integrin-Adhesome is required to maintain muscle structure, mitochondrial ATP production, and movement forces in Caenorhabditis elegans. FASEB J. 29, 1235-1246 (2015).
46. Bulgakova, N. A., Klapholz, B., & Brown, N. H. Cell adhesion in Drosophila: versatility of cadherin and integrin complexes during development. Curr. Opin. Cell Biol. 24, 702-712 (2012).
47. Wickström, S. A., Lange, A., Montanez, E., & Fässler, R. The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase! EMBO J. 29, 281-291 (2010).
48. Sebé-Pedrós, 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).
49. Meller, J., et al. Emergence and subsequent functional specialization of kindlins during evolution of cell adhesiveness. Mol. Biol. Cell. 26, 786-796 (2015).
50. Kanchanawong, P., et al. Nanoscale architecture of integrin-based cell adhesions. Nature. 468, 580-584 (2010).
51. Kelly, D. F., & Taylor, K. A. Identification of the 1-integrin binding site on-Actinin by cryoelectron microscopy. J. Struct. Biol. 149, 290-302 (2005).
52. Otey, C. A., Pavalko, F. M., & Burridge, K. An interaction between-Actinin and the 1 integrin subunit in vitro. J. Cell Biol. 111, 721-729 (1990).
53. Choi, C. K., et al. Actin and-Actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat. Cell Biol. 10, 1039-1050 (2008).
54. Rossier, O., et al. Integrins 1 and 3 exhibit distinct dynamic nanoscale organizations inside focal adhesions. Nat. Cell Biol. 14, 1057-1067 (2012).
55. Zaidel-Bar, R., Cohen, M., Addadi, L., & Geiger, B. Hierarchical assembly of cellmatrix adhesion complexes. Biochem. Soc. Trans. 32, 416-420 (2004).
56. Zaidel-Bar, R., Ballestrem, C., Kam, Z., & Geiger, B. Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 116, 4605-4613 (2003).
57. Bass, M. D., et al. Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J. Cell Biol. 117, 527-538 (2007).
58. Shevchenko, A., Wilm, M., Vorm, O., & Mann, M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996).
59. Perkins, D. N., Pappin, D. J., Creasy, D. M., & Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis. 20, 3551-3567 (1999).
60. Gray, K. A., Yates, B., Seal, R. L., Wright, M. W., & Bruford, E. A. Genenames.org: the HGNC resources in 2015. Nucleic Acids Res. 43, D1079-D1085 (2015).
61. Mitchell, A., et al. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 43, D213-D221 (2015).
62. de Hoon, M. J. L., Imoto, S., Nolan, J., & Miyano, S. Open source clustering software. Bioinformatics. 20, 1453-1454 (2004).
63. Saldanha, A. J. Java Treeview-extensible visualization of microarray data. Bioinformatics. 20, 3246-3248 (2004).
64. Saeed, A. I., et al. TM4: a free, open-source system for microarray data management and analysis. BioTechniques. 34, 374-378 (2003).
65. Cline, M. S., et al. Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2, 2366-2382 (2007).
66. Assenov, Y., Ramírez, F., Schelhorn, S.-E., Lengauer, T., & Albrecht, M. Computing topological parameters of biological networks. Bioinformatics. 24, 282-284 (2008).
67. Huang, D. W., Sherman, B. T., & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
68. Zeeberg, B. R., et al. High-Throughput GoMiner, an industrial-strength integrative gene ontology tool for interpretation of multiple-microarray experiments, with application to studies of Common Variable Immune Deficiency (CVID). BMC Bioinformatics. 6, 168 (2005).
69. Schindelin, J., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 9, 676-682 (2012).
70. Vizcaíno, J. A., et al. The Proteomics Identifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41, D1063-D1069 (2013).