Characterization of the interaction between Actinin-Associated LIM Protein (ALP) and the rod domain of α-actinin
Tóm tắt
The PDZ-LIM proteins are a family of signalling adaptors that interact with the actin cross-linking protein, α-actinin, via their PDZ domains or via internal regions between the PDZ and LIM domains. Three of the PDZ-LIM proteins have a conserved 26-residue ZM motif in the internal region, but the structure of the internal region is unknown. In this study, using circular dichroism and nuclear magnetic resonance (NMR), we showed that the ALP internal region (residues 107–273) was largely unfolded in solution, but was able to interact with the α-actinin rod domain in vitro, and to co-localize with α-actinin on stress fibres in vivo. NMR analysis revealed that the titration of ALP with the α-actinin rod domain induces stabilization of ALP. A synthetic peptide (residues 175–196) that contained the N-terminal half of the ZM motif was found to interact directly with the α-actinin rod domain in surface plasmon resonance (SPR) measurements. Short deletions at or before the ZM motif abrogated the localization of ALP to actin stress fibres. The internal region of ALP appeared to be largely unstructured but functional. The ZM motif defined part of the interaction surface between ALP and the α-actinin rod domain.
Tài liệu tham khảo
Frank D, Kuhn C, Katus HA, Frey N: The sarcomeric Z-disc: a nodal point in signalling and disease. J Mol Med. 2006, 84 (6): 446-468. 10.1007/s00109-005-0033-1.
Blanchard A, Ohanian V, Critchley D: The structure and function of alpha-actinin. J Muscle Res Cell Motil. 1989, 10 (4): 280-289. 10.1007/BF01758424.
Broderick MJ, Winder SJ: Towards a complete atomic structure of spectrin family proteins. J Struct Biol. 2002, 137 (1–2): 184-193. 10.1006/jsbi.2002.4465.
McKeown CR, Han HF, Beckerle MC: Molecular characterization of the Caenorhabditis elegans ALP/Enigma gene alp-1. Dev Dyn. 2006, 235 (2): 530-538. 10.1002/dvdy.20633.
Xia H, Winokur ST, Kuo WL, Altherr MR, Bredt DS: Actinin-associated LIM protein: identification of a domain interaction between PDZ and spectrin-like repeat motifs. J Cell Biol. 1997, 139 (2): 507-515. 10.1083/jcb.139.2.507.
Faulkner G, Pallavicini A, Formentin E, Comelli A, Ievolella C, Trevisan S, Bortoletto G, Scannapieco P, Salamon M, Mouly V: ZASP: a new Z-band alternatively spliced PDZ-motif protein. J Cell Biol. 1999, 146 (2): 465-475. 10.1083/jcb.146.2.465.
Guy PM, Kenny DA, Gill GN: The PDZ domain of the LIM protein enigma binds to beta-tropomyosin. Mol Biol Cell. 1999, 10 (6): 1973-1984.
Pomies P, Macalma T, Beckerle MC: Purification and characterization of an alpha-actinin-binding PDZ-LIM protein that is Up-regulated during muscle differentiation. J Biol Chem. 1999, 274 (41): 29242-29250. 10.1074/jbc.274.41.29242.
Zhou Q, Ruiz-Lozano P, Martone ME, Chen J: Cypher, a striated muscle-restricted PDZ and LIM domain-containing protein, binds to alpha-actinin-2 and protein kinase C. J Biol Chem. 1999, 274 (28): 19807-19813. 10.1074/jbc.274.28.19807.
Nakagawa N, Hoshijima M, Oyasu M, Saito N, Tanizawa K, Kuroda S: ENH, containing PDZ and LIM domains, heart/skeletal muscle-specific protein, associates with cytoskeletal proteins through the PDZ domain. Biochem Biophys Res Commun. 2000, 272 (2): 505-512. 10.1006/bbrc.2000.2787.
Passier R, Richardson JA, Olson EN: Oracle, a novel PDZ-LIM domain protein expressed in heart and skeletal muscle. Mech Dev. 2000, 92 (2): 277-284. 10.1016/S0925-4773(99)00330-5.
Niederlander N, Fayein NA, Auffray C, Pomies P: Characterization of a new human isoform of the enigma homolog family specifically expressed in skeletal muscle. Biochem Biophys Res Commun. 2004, 325 (4): 1304-1311. 10.1016/j.bbrc.2004.10.178.
Wang H, Harrison-Shostak DC, Lemasters JJ, Herman B: Cloning of a rat cDNA encoding a novel LIM domain protein with high homology to rat RIL. Gene. 1995, 165 (2): 267-271. 10.1016/0378-1119(95)00542-E.
Kotaka M, Ngai SM, Garcia-Barcelo M, Tsui SK, Fung KP, Lee CY, Waye MM: Characterization of the human 36-kDa carboxyl terminal LIM domain protein (hCLIM1). J Cell Biochem. 1999, 72 (2): 279-285. 10.1002/(SICI)1097-4644(19990201)72:2<279::AID-JCB12>3.0.CO;2-7.
Kotaka M, Kostin S, Ngai S, Chan K, Lau Y, Lee SM, Li H, Ng EK, Schaper J, Tsui SK: Interaction of hCLIM1, an enigma family protein, with alpha-actinin 2. J Cell Biochem. 2000, 78 (4): 558-565. 10.1002/1097-4644(20000915)78:4<558::AID-JCB5>3.0.CO;2-I.
Vallenius T, Mäkelä TP: Clik1: a novel kinase targeted to actin stress fibers by the CLP-36 PDZ-LIM protein. J Cell Sci. 2002, 115 (Pt 10): 2067-2073.
Vallenius T, Scharm B, Vesikansa A, Luukko K, Schafer R, Mäkelä TP: The PDZ-LIM protein RIL modulates actin stress fiber turnover and enhances the association of alpha-actinin with F-actin. Exp Cell Res. 2004, 293 (1): 117-128. 10.1016/j.yexcr.2003.09.004.
Kiess M, Scharm B, Aguzzi A, Hajnal A, Klemenz R, Schwarte-Waldhoff I, Schafer R: Expression of ril, a novel LIM domain gene, is down-regulated in Hras-transformed cells and restored in phenotypic revertants. Oncogene. 1995, 10 (1): 61-68.
Bashirova AA, Markelov ML, Shlykova TV, Levshenkova EV, Alibaeva RA, Frolova EI: The human RIL gene: mapping to human chromosome 5q31.1, genomic organization and alternative transcripts. Gene. 1998, 210 (2): 239-245. 10.1016/S0378-1119(98)00080-8.
Torrado M, Senatorov VV, Trivedi R, Fariss RN, Tomarev SI: Pdlim2, a novel PDZ-LIM domain protein, interacts with alpha-actinins and filamin A. Invest Ophthalmol Vis Sci. 2004, 45 (11): 3955-3963. 10.1167/iovs.04-0721.
Loughran G, Healy NC, Kiely PA, Huigsloot M, Kedersha NL, O'Connor R: Mystique is a new insulin-like growth factor-I-regulated PDZ-LIM domain protein that promotes cell attachment and migration and suppresses Anchorage-independent growth. Mol Biol Cell. 2005, 16 (4): 1811-1822. 10.1091/mbc.E04-12-1052.
Pashmforoush M, Pomies P, Peterson KL, Kubalak S, Ross J, Hefti A, Aebi U, Beckerle MC, Chien KR: Adult mice deficient in actinin-associated LIM-domain protein reveal a developmental pathway for right ventricular cardiomyopathy. Nat Med. 2001, 7 (5): 591-597. 10.1038/87920.
Zhou Q, Chu PH, Huang C, Cheng CF, Martone ME, Knoll G, Shelton GD, Evans S, Chen J: Ablation of Cypher, a PDZ-LIM domain Z-line protein, causes a severe form of congenital myopathy. J Cell Biol. 2001, 155 (4): 605-612. 10.1083/jcb.200107092.
Jani K, Schöck F: Zasp is required for the assembly of functional integrin adhesion sites. J Cell Biol. 2007, 179 (7): 1583-1597. 10.1083/jcb.200707045.
Schulz TW, Nakagawa T, Licznerski P, Pawlak V, Kolleker A, Rozov A, Kim J, Dittgen T, Kohr G, Sheng M: Actin/alpha-actinin-dependent transport of AMPA receptors in dendritic spines: role of the PDZ-LIM protein RIL. J Neurosci. 2004, 24 (39): 8584-8594. 10.1523/JNEUROSCI.2100-04.2004.
Au Y, Atkinson RA, Guerrini R, Kelly G, Joseph C, Martin SR, Muskett FW, Pallavicini A, Faulkner G, Pastore A: Solution structure of ZASP PDZ domain; implications for sarcomere ultrastructure and enigma family redundancy. Structure (Camb). 2004, 12 (4): 611-622. 10.1016/j.str.2004.02.019.
Klaavuniemi T, Kelloniemi A, Ylänne J: The ZASP-like motif in actinin-associated LIM protein is required for interaction with the alpha-actinin rod and for targeting to the muscle Z-line. J Biol Chem. 2004, 279 (25): 26402-26410. 10.1074/jbc.M401871200.
Bauer K, Kratzer M, Otte M, de Quintana KL, Hagmann J, Arnold GJ, Eckerskorn C, Lottspeich F, Siess W: Human CLP36, a PDZ-domain and LIM-domain protein, binds to alpha-actinin-1 and associates with actin filaments and stress fibers in activated platelets and endothelial cells. Blood. 2000, 96 (13): 4236-4245.
Klaavuniemi T, Ylänne J: Zasp/Cypher internal ZM-motif containing fragments are sufficient to co-localize with alpha-actinin – analysis of patient mutations. Exp Cell Res. 2006, 312 (8): 1299-1311. 10.1016/j.yexcr.2005.12.036.
Vatta M, Mohapatra B, Jimenez S, Sanchez X, Faulkner G, Perles Z, Sinagra G, Lin JH, Vu TM, Zhou Q: Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J Am Coll Cardiol. 2003, 42 (11): 2014-2027. 10.1016/j.jacc.2003.10.021.
Selcen D, Engel AG: Mutations in ZASP define a novel form of muscular dystrophy in humans. Ann Neurol. 2005, 57 (2): 269-276. 10.1002/ana.20376.
Te Velthuis AJ, Isogai T, Gerrits L, Bagowski CP: Insights into the molecular evolution of the PDZ/LIM family and identification of a novel conserved protein motif. PLoS ONE. 2007, 2 (2): e189-10.1371/journal.pone.0000189.
Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O, Beckmann JS, Silman I, Sussman JL: FoldIndex(C): a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics. 2005, 21 (16): 3435-3438. 10.1093/bioinformatics/bti537.
Schultz J, Milpetz F, Bork P, Ponting CP: SMART, a simplemodular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA. 1998, 95 (11): 5857-5864. 10.1073/pnas.95.11.5857.
Linding R, Jensen LJ, Diella F, Bork P, Gibson TJ, Russell RB: Protein disorder prediction: implications for structural proteomics. Structure (Camb). 2003, 11 (11): 1453-1459. 10.1016/j.str.2003.10.002.
Bondos SE, Bicknell A: Detection and prevention of protein aggregation before, during, and after purification. Anal Biochem. 2003, 316 (2): 223-231. 10.1016/S0003-2697(03)00059-9.
Golovanov AP, Hautbergue GM, Wilson SA, Lian LY: A simple method for improving protein solubility and long-term stability. J Am Chem Soc. 2004, 126 (29): 8933-8939. 10.1021/ja049297h.
Alho N, Klaavuniemi T, Ylänne J, Permi P, Mattila S: Backbone NMR assignment of the internal interaction site of ALP. Biomolecular NMR Assignments. 2007, 1 (1): 85-10.1007/s12104-007-9024-1.
Spera S, Bax A: Empirical correlation between protein backbone conformation and Calpha and Cbeta 13-C nuclear magnetic resonance chemical shifts. J Am Chem Soc. 1991, 113: 5490-5492. 10.1021/ja00014a071.
Small JV: Structure-function relationships in smooth muscle: the missing links. BioEssays. 1995, 17 (9): 785-792. 10.1002/bies.950170908.
Vlahos CJ, McDowell SA, Clerk A: Kinases as therapeutic targets for heart failure. Nat Rev Drug Discov. 2003, 2 (2): 99-113. 10.1038/nrd1009.
Wilkins BJ, Molkentin JD: Calcium-calcineurin signaling in the regulation of cardiac hypertrophy. Biochem Biophys Res Commun. 2004, 322 (4): 1178-1191. 10.1016/j.bbrc.2004.07.121.
Vega RB, Bassel-Duby R, Olson EN: Control of cardiac growth and function by calcineurin signaling. J Biol Chem. 2003, 278 (39): 36981-36984. 10.1074/jbc.R300023200.
Kuroda S, Tokunaga C, Kiyohara Y, Higuchi O, Konishi H, Mizuno K, Gill GN, Kikkawa U: Protein-protein interaction of zinc finger LIM domains with protein kinase C. J Biol Chem. 1996, 271 (49): 31029-31032. 10.1074/jbc.271.49.31029.
Frey N, Olson EN: Calsarcin-3, a novel skeletal muscle-specific member of the calsarcin family, interacts with multiple Z-disc proteins. J Biol Chem. 2002, 277 (16): 13998-14004. 10.1074/jbc.M200712200.
Djinovic-Carugo K, Young P, Gautel M, Saraste M: Structure of the alpha-actinin rod: molecular basis for cross-linking of actin filaments. Cell. 1999, 98 (4): 537-546. 10.1016/S0092-8674(00)81981-9.
Ylänne J, Scheffzek K, Young P, Saraste M: Crystal Structure of the alpha-Actinin Rod Reveals an Extensive Torsional Twist. Structure. 2001, 9 (7): 597-604. 10.1016/S0969-2126(01)00619-0.
Hotulainen P, Lappalainen P: Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol. 2006, 173 (3): 383-394. 10.1083/jcb.200511093.
Sambrook J, Russell DW: Molecular Cloning, a laboratory mamual. 2001, New York: Cold Spring Harbor Laboratory Press, 3