1jo8 Citations

Unusual binding properties of the SH3 domain of the yeast actin-binding protein Abp1: structural and functional analysis.

Abstract

Abp1p is an actin-binding protein that plays a central role in the organization of Saccharomyces cerevisiae actin cytoskeleton. By a combination of two-hybrid and phage-display approaches, we have identified six new ligands of the Abp1-SH3 domain. None of these SH3-mediated novel interactions was detected in recent all genome high throughput protein interaction projects. Here we show that the SH3-mediated association of Abp1p with the Ser/Thr kinases Prk1p and Ark1p is essential for their localization to actin cortical patches. The Abp1-SH3 domain has a rather unusual binding specificity, because its target peptides contain the tetrapentapeptide +XXXPXXPX+PXXL with positive charges flanking the polyproline core on both sides. Here we present the structure of the Abp1-SH3 domain solved at 1.3-A resolution. The peptide-binding pockets in the SH3 domain are flanked by two acidic residues that are uncommon at those positions in the SH3 domain family. We have shown by site-directed mutagenesis that one of these negatively charged side chains may be the key determinant for the preference for non-classical ligands.

Articles - 1jo8 mentioned but not cited (7)

  1. Targeting AMAP1 and cortactin binding bearing an atypical src homology 3/proline interface for prevention of breast cancer invasion and metastasis. Hashimoto S, Hirose M, Hashimoto A, Morishige M, Yamada A, Hosaka H, Akagi K, Ogawa E, Oneyama C, Agatsuma T, Okada M, Kobayashi H, Wada H, Nakano H, Ikegami T, Nakagawa A, Sabe H. Proc. Natl. Acad. Sci. U.S.A. 103 7036-7041 (2006)
  2. Structural basis of murein peptide specificity of a gamma-D-glutamyl-l-diamino acid endopeptidase. Xu Q, Sudek S, McMullan D, Miller MD, Geierstanger B, Jones DH, Krishna SS, Spraggon G, Bursalay B, Abdubek P, Acosta C, Ambing E, Astakhova T, Axelrod HL, Carlton D, Caruthers J, Chiu HJ, Clayton T, Deller MC, Duan L, Elias Y, Elsliger MA, Feuerhelm J, Grzechnik SK, Hale J, Han GW, Haugen J, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Kumar A, Marciano D, Morse AT, Nigoghossian E, Okach L, Oommachen S, Paulsen J, Reyes R, Rife CL, Trout CV, van den Bedem H, Weekes D, White A, Wolf G, Zubieta C, Hodgson KO, Wooley J, Deacon AM, Godzik A, Lesley SA, Wilson IA. Structure 17 303-313 (2009)
  3. Transplanting supersites of HIV-1 vulnerability. Zhou T, Zhu J, Yang Y, Gorman J, Ofek G, Srivatsan S, Druz A, Lees CR, Lu G, Soto C, Stuckey J, Burton DR, Koff WC, Connors M, Kwong PD. PLoS ONE 9 e99881 (2014)
  4. Structure of the SH3 domain of human osteoclast-stimulating factor at atomic resolution. Chen L, Wang Y, Wells D, Toh D, Harold H, Zhou J, DiGiammarino E, Meehan EJ. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62 844-848 (2006)
  5. SH3 domain-peptide binding energy calculations based on structural ensemble and multiple peptide templates. Hong S, Chung T, Kim D. PLoS ONE 5 e12654 (2010)
  6. Combining Evolutionary Information and an Iterative Sampling Strategy for Accurate Protein Structure Prediction. Braun T, Koehler Leman J, Lange OF. PLoS Comput. Biol. 11 e1004661 (2015)
  7. Fold and flexibility: what can proteins' mechanical properties tell us about their folding nucleus? Sacquin-Mora S. J R Soc Interface 12 (2015)


Reviews citing this publication (10)

  1. Actin and endocytosis in budding yeast. Goode BL, Eskin JA, Wendland B. Genetics 199 315-358 (2015)
  2. SH3 domains: modules of protein-protein interactions. Kurochkina N, Guha U. Biophys Rev 5 29-39 (2013)
  3. The mammalian actin-binding protein 1 (mAbp1): a novel molecular player in leukocyte biology. Schymeinsky J, Sperandio M, Walzog B. Trends Cell Biol. 21 247-255 (2011)
  4. Actin-depolymerizing factor homology domain: a conserved fold performing diverse roles in cytoskeletal dynamics. Poukkula M, Kremneva E, Serlachius M, Lappalainen P. Cytoskeleton (Hoboken) 68 471-490 (2011)
  5. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Moseley JB, Goode BL. Microbiol. Mol. Biol. Rev. 70 605-645 (2006)
  6. Prk1p. Zeng G, Cai M. Int. J. Biochem. Cell Biol. 37 48-53 (2005)
  7. Exploring protein-protein interactions with phage display. Sidhu SS, Fairbrother WJ, Deshayes K. Chembiochem 4 14-25 (2003)
  8. Functional genomics of intracellular peptide recognition domains with combinatorial biology methods. Sidhu SS, Bader GD, Boone C. Curr Opin Chem Biol 7 97-102 (2003)
  9. The Ark1/Prk1 family of protein kinases. Regulators of endocytosis and the actin skeleton. Smythe E, Ayscough KR. EMBO Rep. 4 246-251 (2003)
  10. Phage display of random peptide libraries: applications, limits, and potential. Szardenings M. J. Recept. Signal Transduct. Res. 23 307-349 (2003)

Articles citing this publication (51)

  1. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. McLellan JS, Pancera M, Carrico C, Gorman J, Julien JP, Khayat R, Louder R, Pejchal R, Sastry M, Dai K, O'Dell S, Patel N, Shahzad-ul-Hussan S, Yang Y, Zhang B, Zhou T, Zhu J, Boyington JC, Chuang GY, Diwanji D, Georgiev I, Kwon YD, Lee D, Louder MK, Moquin S, Schmidt SD, Yang ZY, Bonsignori M, Crump JA, Kapiga SH, Sam NE, Haynes BF, Burton DR, Koff WC, Walker LM, Phogat S, Wyatt R, Orwenyo J, Wang LX, Arthos J, Bewley CA, Mascola JR, Nabel GJ, Schief WR, Ward AB, Wilson IA, Kwong PD. Nature 480 336-343 (2011)
  2. A modular design for the clathrin- and actin-mediated endocytosis machinery. Kaksonen M, Toret CP, Drubin DG. Cell 123 305-320 (2005)
  3. Optimization of specificity in a cellular protein interaction network by negative selection. Zarrinpar A, Park SH, Lim WA. Nature 426 676-680 (2003)
  4. Protein interaction networks by proteome peptide scanning. Landgraf C, Panni S, Montecchi-Palazzi L, Castagnoli L, Schneider-Mergener J, Volkmer-Engert R, Cesareni G. PLoS Biol. 2 E14 (2004)
  5. Vaccine-induced IgG antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infection. Zolla-Pazner S, deCamp A, Gilbert PB, Williams C, Yates NL, Williams WT, Howington R, Fong Y, Morris DE, Soderberg KA, Irene C, Reichman C, Pinter A, Parks R, Pitisuttithum P, Kaewkungwal J, Rerks-Ngarm S, Nitayaphan S, Andrews C, O'Connell RJ, Yang ZY, Nabel GJ, Kim JH, Michael NL, Montefiori DC, Liao HX, Haynes BF, Tomaras GD. PLoS ONE 9 e87572 (2014)
  6. Negative regulation of yeast WASp by two SH3 domain-containing proteins. Rodal AA, Manning AL, Goode BL, Drubin DG. Curr. Biol. 13 1000-1008 (2003)
  7. Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Araujo-Bazán L, Peñalva MA, Espeso EA. Mol. Microbiol. 67 891-905 (2008)
  8. Structures of invisible, excited protein states by relaxation dispersion NMR spectroscopy. Vallurupalli P, Hansen DF, Kay LE. Proc. Natl. Acad. Sci. U.S.A. 105 11766-11771 (2008)
  9. PtdIns(4,5)P2 turnover is required for multiple stages during clathrin- and actin-dependent endocytic internalization. Sun Y, Carroll S, Kaksonen M, Toshima JY, Drubin DG. J. Cell Biol. 177 355-367 (2007)
  10. Using NMR chemical shifts as structural restraints in molecular dynamics simulations of proteins. Robustelli P, Kohlhoff K, Cavalli A, Vendruscolo M. Structure 18 923-933 (2010)
  11. The phosphoinositide phosphatase Sjl2 is recruited to cortical actin patches in the control of vesicle formation and fission during endocytosis. Stefan CJ, Padilla SM, Audhya A, Emr SD. Mol. Cell. Biol. 25 2910-2923 (2005)
  12. A complex-based reconstruction of the Saccharomyces cerevisiae interactome. Wang H, Kakaradov B, Collins SR, Karotki L, Fiedler D, Shales M, Shokat KM, Walther TC, Krogan NJ, Koller D. Mol. Cell Proteomics 8 1361-1381 (2009)
  13. Displacement of formins from growing barbed ends by bud14 is critical for actin cable architecture and function. Chesarone M, Gould CJ, Moseley JB, Goode BL. Dev. Cell 16 292-302 (2009)
  14. Multiple pathways regulate endocytic coat disassembly in Saccharomyces cerevisiae for optimal downstream trafficking. Toret CP, Lee L, Sekiya-Kawasaki M, Drubin DG. Traffic 9 848-859 (2008)
  15. Structures of HIV-1 Env V1V2 with broadly neutralizing antibodies reveal commonalities that enable vaccine design. Gorman J, Soto C, Yang MM, Davenport TM, Guttman M, Bailer RT, Chambers M, Chuang GY, DeKosky BJ, Doria-Rose NA, Druz A, Ernandes MJ, Georgiev IS, Jarosinski MC, Joyce MG, Lemmin TM, Leung S, Louder MK, McDaniel JR, Narpala S, Pancera M, Stuckey J, Wu X, Yang Y, Zhang B, Zhou T, NISC Comparative Sequencing Program, Mullikin JC, Baxa U, Georgiou G, McDermott AB, Bonsignori M, Haynes BF, Moore PL, Morris L, Lee KK, Shapiro L, Mascola JR, Kwong PD. Nat. Struct. Mol. Biol. 23 81-90 (2016)
  16. Structural characterization of Lyn-SH3 domain in complex with a herpesviral protein reveals an extended recognition motif that enhances binding affinity. Bauer F, Schweimer K, Meiselbach H, Hoffmann S, Rösch P, Sticht H. Protein Sci. 14 2487-2498 (2005)
  17. GMF is an evolutionarily developed Adf/cofilin-super family protein involved in the Arp2/3 complex-mediated organization of the actin cytoskeleton. Nakano K, Kuwayama H, Kawasaki M, Numata O, Takaine M. Cytoskeleton (Hoboken) 67 373-382 (2010)
  18. Protein stabilization by specific binding of guanidinium to a functional arginine-binding surface on an SH3 domain. Zarrine-Afsar A, Mittermaier A, Kay LE, Davidson AR. Protein Sci. 15 162-170 (2006)
  19. The Saccharomyces cerevisiae actin patch protein App1p is a phosphatidate phosphatase enzyme. Chae M, Han GS, Carman GM. J. Biol. Chem. 287 40186-40196 (2012)
  20. Structural and functional dissection of the Abp1 ADFH actin-binding domain reveals versatile in vivo adapter functions. Quintero-Monzon O, Rodal AA, Strokopytov B, Almo SC, Goode BL. Mol. Biol. Cell 16 3128-3139 (2005)
  21. Structure-based prediction of the Saccharomyces cerevisiae SH3-ligand interactions. Fernandez-Ballester G, Beltrao P, Gonzalez JM, Song YH, Wilmanns M, Valencia A, Serrano L. J. Mol. Biol. 388 902-916 (2009)
  22. The biologically relevant targets and binding affinity requirements for the function of the yeast actin-binding protein 1 Src-homology 3 domain vary with genetic context. Haynes J, Garcia B, Stollar EJ, Rath A, Andrews BJ, Davidson AR. Genetics 176 193-208 (2007)
  23. Solution structure of a Hck SH3 domain ligand complex reveals novel interaction modes. Schmidt H, Hoffmann S, Tran T, Stoldt M, Stangler T, Wiesehan K, Willbold D. J. Mol. Biol. 365 1517-1532 (2007)
  24. Scd5p mediates phosphoregulation of actin and endocytosis by the type 1 phosphatase Glc7p in yeast. Zeng G, Huang B, Neo SP, Wang J, Cai M. Mol. Biol. Cell 18 4885-4898 (2007)
  25. A myosin IK-Abp1-PakB circuit acts as a switch to regulate phagocytosis efficiency. Dieckmann R, von Heyden Y, Kistler C, Gopaldass N, Hausherr S, Crawley SW, Schwarz EC, Diensthuber RP, Côté GP, Tsiavaliaris G, Soldati T. Mol. Biol. Cell 21 1505-1518 (2010)
  26. Paxillin and ponsin interact in nascent costameres of muscle cells. Gehmlich K, Pinotsis N, Hayess K, van der Ven PF, Milting H, El Banayosy A, Körfer R, Wilmanns M, Ehler E, Fürst DO. J. Mol. Biol. 369 665-682 (2007)
  27. PAH1-encoded phosphatidate phosphatase plays a role in the growth phase- and inositol-mediated regulation of lipid synthesis in Saccharomyces cerevisiae. Pascual F, Soto-Cardalda A, Carman GM. J. Biol. Chem. 288 35781-35792 (2013)
  28. Identification of Gal80p-interacting proteins by Saccharomyces cerevisiae whole genome phage display. Hertveldt K, Dechassa ML, Robben J, Volckaert G. Gene 307 141-149 (2003)
  29. Differential dynamic engagement within 24 SH3 domain: peptide complexes revealed by co-linear chemical shift perturbation analysis. Stollar EJ, Lin H, Davidson AR, Forman-Kay JD. PLoS ONE 7 e51282 (2012)
  30. Structural, functional, and bioinformatic studies demonstrate the crucial role of an extended peptide binding site for the SH3 domain of yeast Abp1p. Stollar EJ, Garcia B, Chong PA, Rath A, Lin H, Forman-Kay JD, Davidson AR. J. Biol. Chem. 284 26918-26927 (2009)
  31. Abl-SH3 binding protein 2, 3BP2, interacts with CIN85 and HIP-55. Le Bras S, Moon C, Foucault I, Breittmayer JP, Deckert M. FEBS Lett. 581 967-974 (2007)
  32. Protein structure protection commits gene expression patterns. Chen J, Liang H, Fernández A. Genome Biol. 9 R107 (2008)
  33. Characterization of the yeast actin patch protein App1p phosphatidate phosphatase. Chae M, Carman GM. J. Biol. Chem. 288 6427-6437 (2013)
  34. Clathrin- and Arp2/3-independent endocytosis in the fungal pathogen Candida albicans. Epp E, Nazarova E, Regan H, Douglas LM, Konopka JB, Vogel J, Whiteway M. MBio 4 e00476-13 (2013)
  35. A novel function of Arp2p in mediating Prk1p-specific regulation of actin and endocytosis in yeast. Jin M, Cai M. Mol. Biol. Cell 19 297-307 (2008)
  36. Directed discovery of bivalent peptide ligands to an SH3 domain. Ferguson MR, Fan X, Mukherjee M, Luo J, Khan R, Ferreon JC, Hilser VJ, Shope RE, Fox RO. Protein Sci. 13 626-632 (2004)
  37. Targeted Isolation of Antibodies Directed against Major Sites of SIV Env Vulnerability. Mason RD, Welles HC, Adams C, Chakrabarti BK, Gorman J, Zhou T, Nguyen R, O'Dell S, Lusvarghi S, Bewley CA, Li H, Shaw GM, Sheng Z, Shapiro L, Wyatt R, Kwong PD, Mascola JR, Roederer M. PLoS Pathog. 12 e1005537 (2016)
  38. Ultrastructural imaging of endocytic sites in Saccharomyces cerevisiae by transmission electron microscopy and immunolabeling. Buser C, Drubin DG. Microsc. Microanal. 19 381-392 (2013)
  39. A Conserved residue in the yeast Bem1p SH3 domain maintains the high level of binding specificity required for function. Gorelik M, Stanger K, Davidson AR. J. Biol. Chem. 286 19470-19477 (2011)
  40. Discovering protein-protein interactions. Ng SK, Tan SH. J Bioinform Comput Biol 1 711-741 (2004)
  41. The proline-rich region of 18.5 kDa myelin basic protein binds to the SH3-domain of Fyn tyrosine kinase with the aid of an upstream segment to form a dynamic complex in vitro. De Avila M, Vassall KA, Smith GS, Bamm VV, Harauz G. Biosci. Rep. 34 e00157 (2014)
  42. Negative regulation of the actin-regulating kinase Prk1p by patch localization-induced autophosphorylation. Huang B, Chua LL, Bose N, Cai M. Traffic 10 35-41 (2009)
  43. Whole genome phage display selects for proline-rich Boi polypeptides against Bem1p. Hertveldt K, Robben J, Volckaert G. Biotechnol. Lett. 28 1233-1239 (2006)
  44. A semi-automated method for purification of milligram quantities of proteins on the QIAcube. McGraw J, Tatipelli VK, Feyijinmi O, Traore MC, Eangoor P, Lane S, Stollar EJ. Protein Expr. Purif. 96 48-53 (2014)
  45. The importance of conserved features of yeast actin-binding protein 1 (Abp1p): the conditional nature of essentiality. Garcia B, Stollar EJ, Davidson AR. Genetics 191 1199-1211 (2012)
  46. Yeast dynamin implicated in endocytic scission and the disassembly of endocytic components. Wang D, Sletto J, Tenay B, Kim K. Commun Integr Biol 4 178-181 (2011)
  47. PakB binds to the SH3 domain of Dictyostelium Abp1 and regulates its effects on cell polarity and early development. Yang Y, de la Roche M, Crawley SW, Li Z, Furmaniak-Kazmierczak E, Côté GP. Mol. Biol. Cell 24 2216-2227 (2013)
  48. Evolution of domain-peptide interactions to coadapt specificity and affinity to functional diversity. Kelil A, Levy ED, Michnick SW. Proc. Natl. Acad. Sci. U.S.A. 113 E3862-71 (2016)
  49. What is the shape of the distribution of protein conformations at equilibrium? Cruzeiro L, Degrève L. J. Biomol. Struct. Dyn. 33 1539-1546 (2015)
  50. Exploring the Levinthal limit in protein folding. Cruzeiro L, Degrève L. J Biol Phys 43 15-30 (2017)
  51. Exhaustive search of linear information encoding protein-peptide recognition. Kelil A, Dubreuil B, Levy ED, Michnick SW. PLoS Comput. Biol. 13 e1005499 (2017)