A molecular mechanism for the requirement of PAT-4 (Integrin-linked Kinase (ILK)) for the localization of UNC-112 (kindlin) to integrin adhesion sites

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 28537-28551

  Qadota, Hiroshi ^a,b   Moerman, Donald G ^b   Benian, Guy M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION SITES; ADHESION STRUCTURES; CAENORHABDITIS ELEGANS; CYTOPLASMIC TAIL; GENETIC ANALYSIS; INTEGRIN-LINKED KINASE; INTEGRINS; MOLECULAR BASIS; MOLECULAR MECHANISM; MUSCLE CELL; MUTATION RESULTS; N-TERMINALS;

ENZYMES;

ADHESION;

CARRIER PROTEIN; INTEGRIN; INTEGRIN LINKED KINASE; PROTEIN UNC 112; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME BINDING; ENZYME LOCALIZATION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION;

AMINO ACID SUBSTITUTION; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; MODELS, BIOLOGICAL; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES;

EID: 84865257028     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.354852     Document Type: Article

References (47)

1. Waterston, R. H. (1988) Muscle. in The Nematode Caenorhabditis elegans. (Wood, W. B., ed) pp. 281-335, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
2. Moerman, D. G., and Fire, A. (1997) Muscle. Structure, function, and development. in C. elegans II (Riddle, D. L., T. Blumenthal, T., Meyer, B. J., and Priess, J. R., eds) pp. 417-470, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
3. Moerman, D. G., and Williams, B. D. (2006) Sarcomere assembly in C. elegans muscle. in WormBook: The Online Review of C. elegans Biology, doi/10.1895/wormbook.1.81.1
4. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94
5. Waterston, R. H., Thomson, J. N., and Brenner, S. (1980) Mutants with altered muscle structure of Caenorhabditis elegans. Dev. Biol. 77, 271-302 (Pubitemid 10011378)
6. Zengel, J. M., and Epstein, H. F. (1980) Identification of genetic elements associated with muscle structure in the nematode Caenorhabditis elegans. Cell Motil. 1, 73-97 (Pubitemid 12233335)
7. Williams, B. D., and Waterston, R. H. (1994) Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J. Cell Biol. 124, 475-490 (Pubitemid 24064460)
8. Meissner, B., Warner, A., Wong, K., Dube, N., Lorch, A., McKay, S. J., Khattra, J., Rogalski, T., Somasiri, A., Chaudhry, I., Fox, R. M., Miller, D. M., 3rd, Baillie, D. L., Holt, R. A., Jones, S. J., Marra, M. A., and Moerman, D. G. (2009) An integrated strategy to study muscle development and myofilament structure in Caenorhabditis elegans. PLoS Genet. 5, e1000537
9. Rogalski, T. M., Mullen, G. P., Gilbert, M. M., Williams, B. D., and Moerman, D. G. (2000) The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J. Cell Biol. 150, 253-264 (Pubitemid 30480998)
10. Mackinnon, A. C., Qadota, H., Norman, K. R., Moerman, D. G., and Williams, B. D. (2002) C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr. Biol. 12, 787-797 (Pubitemid 34514364)
11. Lin, X., Qadota, H., Moerman, D. G., and Williams, B. D. (2003) C. elegans PAT-6/actopaxin plays a critical role in the assembly of integrin adhesion complexes in vivo. Curr. Biol. 13, 922-932 (Pubitemid 36632141)
12. Norman, K. R., Cordes, S., Qadota, H., Rahmani, P., and Moerman, D. G. (2007) UNC-97/PINCH is involved in the assembly of integrin cell adhesion complexes in Caenorhabditis elegans body wall muscle. Dev. Biol. 309, 45-55 (Pubitemid 47302444)
13. Mercer, K. B., Flaherty, D. B., Miller, R. K., Qadota, H., Tinley, T. L., Moerman, D. G., and Benian, G. M. (2003) Caenorhabditis elegans UNC- 98, a C2H2 zinc finger protein, is a novel partner of UNC-97/PINCH in muscle adhesion complexes. Mol. Biol. Cell 14, 2492-2507 (Pubitemid 36724337)
14. Miller, R. K., Qadota, H., Landsverk, M. L., Mercer, K. B., Epstein, H. F., and Benian, G. M. (2006) UNC-98 links an integrin-associated complex to thick filaments in Caenorhabditis elegans muscle. J. Cell Biol. 175, 853-859 (Pubitemid 44969191)
15. Qadota, H., Mercer, K. B., Miller, R. K., Kaibuchi, K., and Benian, G. M. (2007) Two LIM domain proteins and UNC-96 link UNC-97/pinch to myosin thick filaments in Caenorhabditis elegans muscle. Mol. Biol. Cell 18, 4317-4326 (Pubitemid 350060161)
16. Qadota, H., and Benian, G. M. (2010) Molecular structure of sarcomere-to- membrane attachment at M-Lines in C. elegans muscle. J. Biomed. Biotechnol. 2010, 864749
17. Wick, M., Bürger, C., Brüsselbach, S., Lucibello, F. C., and Müller, R. (1994) A novel member of human tissue inhibitor of metalloproteinases (TIMP) gene family is regulated during G1 progression, mitogenic stimulation, differentiation, and senescence. J. Biol. Chem. 269, 18953-18960
18. Meves, A., Stremmel, C., Gottschalk, K., and Fässler, R. (2009) The Kindlin protein family. New members to the club of focal adhesion proteins. Trends Cell Biol. 19, 504-513
19. Siegel, D. H., Ashton, G. H., Penagos, H. G., Lee, J. V., Feiler, H. S., Wilhelmsen, K. C., South, A. P., Smith, F. J., Prescott, A. R., Wessagowit, V., Oyama, N., Akiyama, M., Al Aboud, D., Al Aboud, K., Al Githami, A., Al Hawsawi, K., Al Ismaily, A., Al-Suwaid, R., Atherton, D. J., Caputo, R., Fine, J. D., Frieden, I. J., Fuchs, E., Haber, R. M., Harada, T., Kitajima, Y., Mallory, S. B., Ogawa, H., Sahin, S., Shimizu, H., Suga, Y., Tadini, G., Tsuchiya, K., Wiebe, C. B., Wojnarowska, F., Zaghloul, A. B., Hamada, T., Mallipeddi, R., Eady, R. A., McLean, W. H., McGrath, J. A., and Epstein, E. H. (2003) Loss of kindlin-1, a human homolog of the Caenorhabditis elegans actin-extracellular- matrix linker protein UNC-112, causes Kindler syndrome. Am. J. Hum. Genet. 73, 174-187 (Pubitemid 36793789)
20. Sadler, E., Klausegger, A., Muss, W., Deinsberger, U., Pohla-Gubo, G., Laimer, M., Lanschuetzer, C., Bauer, J. W., and Hintner, H. (2006) Novel KIND1 gene mutation in Kindler syndrome with severe gastrointestinal tract involvement. Arch. Dermatol. 142, 1619-1624 (Pubitemid 44969219)
21. Moser, M., Bauer, M., Schmid, S., Ruppert, R., Schmidt, S., Sixt, M., Wang, H. V., Sperandio, M., and Fassler, R. (2009) Kindlin-3 is required for -2 integrin-mediated leukocyte adhesion to endothelial cells. Nat. Med. 15, 300-305
22. Svensson, L., Howarth, K., McDowall, A., Patzak, I., Evans, R., Ussar, S., Moser, M., Metin, A., Fried, M., Tomlinson, I., and Hogg, N. (2009) Leukocyte adhesion deficiency-III is caused by mutations in KINDLIN3 affecting integrin activation. Nat. Med. 15, 306-312
23. Dowling, J. J., Gibbs, E., Russell, M., Goldman, D., Minarcik, J., Golden, J. A., and Feldman, E. L. (2008) Kindlin-2 is an essential component of intercalated discs and is required for vertebrate cardiac structure and function. Circ. Res. 102, 423-431 (Pubitemid 351651103)
24. Weinstein, E. J., Bourner, M., Head, R., Zakeri, H., Bauer, C., and Mazzarella, R. (2003) URP1. A member of a novel family of PH and FERM do-main- containing membrane-associated proteins is significantly overexpressed in lung and colon carcinomas. Biochim. Biophys. Acta 1637, 207-216 (Pubitemid 36407771)
25. Boyd, R. S., Adam, P. J., Patel, S., Loader, J. A., Berry, J., Redpath, N. T., Poyser, H. R., Fletcher, G. C., Burgess, N. A., Stamps, A. C., Hudson, L., Smith, P., Griffiths, M., Willis, T. G., Karran, E. L., Oscier, D. G., Catovsky, D., Terrett, J. A., and Dyer, M. J. (2003) Proteomic analysis of the cellsurface membrane in chronic lymphocytic leukemia. Identification of two novel proteins, BCNP1 and MIG2B. Leukemia 17, 1605-1612 (Pubitemid 36986964)
26. James, P., Halladay, J., and Craig, E. A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436
27. Mercer, K. B., Miller, R. K., Tinley, T. L., Sheth, S., Qadota, H., and Benian, G. M. (2006) Caenorhabditis elegans UNC-96 is a new component of M-lines that interacts with UNC-98 and paramyosin and is required in adult muscle for assembly and/or maintenance of thick filaments. Mol. Biol. Cell 17, 3832-3847 (Pubitemid 44330869)
28. Hikita, T., Qadota, H., Tsuboi, D., Taya, S., Moerman, D. G., and Kaibuchi, K. (2005) Identification of a novel Cdc42 GEF that is localized to the PAT-3-mediated adhesive structure. Biochem. Biophys. Res. Commun. 335, 139-145 (Pubitemid 41350773)
29. Nonet, M. L., Grundahl, K., Meyer, B. J., and Rand, J. B. (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73, 1291-1305 (Pubitemid 23201144)
30. Qadota, H., Blangy, A., Xiong, G., and Benian, G. M. (2008) The DH-PH region of the giant protein UNC-89 activates RHO-1 GTPase in Caenorhabditis elegans body wall muscle. J. Mol. Biol. 383, 747-752
31. Cadwell, R. C., and Joyce, G. F. (1992) Randomization of genes by PCR mutagenesis. PCR Methods Appl. 2, 28-33
32. Takita, Y., Takahara, M., Nogami, S., Anraku, Y., and Ohya, Y. (1997) Applications of the long and accurate polymerase chain reaction method in yeast molecular biology. Direct sequencing of the amplified DNA and its introduction into yeast. Yeast 13, 763-768 (Pubitemid 27287856)
33. Qadota, H., McGaha, L. A., Mercer, K. B., Stark, T. J., Ferrara, T. M., and Benian, G. M. (2008) A novel protein phosphatase is a binding partner for the protein kinase domains of UNC-89 (Obscurin) in Caenorhabditis elegans. Mol. Biol. Cell 19, 2424-2432
34. Yochem, J., Gu, T., and Han, M. (1998) A new marker for mosaic analysis in Caenorhabditis elegans indicates a fusion between hyp6 and hyp7, two major components of the hypodermis. Genetics 149, 1323-1334 (Pubitemid 28334526)
35. Mitani, S. (1995) Genetic regulation of mec-3 gene expression implicated in the specification of the mechanosensory neuron cell types in Caenorhabditis elegans. Dev. Growth Differ. 37, 551-557
36. Miller, D. M., 3rd, Ortiz, I., Berliner, G. C., and Epstein, H. F. (1983) Differential localization of two myosins within nematode thick filaments. Cell 34, 477-490
37. Zervas, C. G., Gregory, S. L., and Brown, N. H. (2001) Drosophila integrinlinked kinase is required at sites of integrin adhesion to link the cytoskeleton to the plasma membrane. J. Cell Biol. 152, 1007-1018 (Pubitemid 34286076)
38. Montanez, E., Ussar, S., Schifferer, M., Bösl, M., Zent, R., Moser, M., and Fässler, R. (2008) Kindlin-2 controls bidirectional signaling of integrins. Genes Dev. 22, 1325-1330 (Pubitemid 351717522)
39. Dowling, J. J., Vreede, A. P., Kim, S., Golden, J., and Feldman, E. L. (2008) Kindlin-2 is required for myocyte elongation and is essential for myogenesis. BMC Cell Biol. 9, 36
40. Persad, S., Attwell, S., Gray, V., Mawji, N., Deng, J. T., Leung, D., Yan, J., Sanghera, J., Walsh, M. P., and Dedhar, S. (2001) Regulation of protein kinase B/Akt-serine 473 phosphorylation by integrin-linked kinase. Critical roles for kinase activity and amino acids arginine 211 and serine 343. J. Biol. Chem. 276, 27462-27469
41. Laub, M. T., and Goulian, M. (2007) Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 41, 121-145
42. Reczek, D., and Bretscher, A. (1998) The carboxyl-terminal region of EBP50 binds to a site in the amino-terminal domain of ezrin that is masked in the dormant molecule. J. Biol. Chem. 273, 18452-18458 (Pubitemid 28334773)
43. Pietromonaco, S. F., Simons, P. C., Altman, A., and Elias, L. (1998) Protein kinase C-θ phosphorylation of moesin in the actin-binding sequence. J. Biol. Chem. 273, 7594-7603 (Pubitemid 28153699)
44. Matsui, T., Yonemura, S., and Tsukita, S. (1999) Activation of ERM proteins in vivo by Rho involves phosphatidylinositol 4-phosphate 5-kinase and not ROCK kinases. Curr. Biol. 9, 1259-1262 (Pubitemid 29527153)
45. Goult, B. T., Bouaouina, M., Harburger, D. S., Bate, N., Patel, B., Anthis, N. J., Campbell, I. D., Calderwood, D. A., Barsukov, I. L., Roberts, G. C., and Critchley, D. R. (2009) The structure of the N terminus of kindlin-1. A domain important for αiibβ3 integrin activation. J. Mol. Biol. 394, 944-956
46. Liu, J., Fukuda, K., Xu, Z., Ma, Y. Q., Hirbawi, J., Mao, X., Wu, C., Plow, E. F., and Qin, J. (2011) Structural basis of phosphoinositide binding to kindlin-2 protein pleckstrin homology domain in regulating integrin activation. J. Biol. Chem. 286, 43334-43342
47. Wilson, K. J., Qadota, H., Mains, P. E., and Benian, G. M. (2012) UNC-89 (obscurin) binds to MEL-26, a BTB domain protein, and affects the function of MEI-1 (katanin) in striated muscle of C. elegans. Mol. Biol. Cell 23, 2623-2634