Structures of SdrD from Staphylococcus aureusreveal the molecular mechanism of how the cell surface receptors recognize their ligands

Xiao Wang1, Jingpeng Ge1, Bao Liu2, Yulin Hu3, Maojun Yang1()

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Protein Cell ›› 2013, Vol. 4 ›› Issue (4) : 277-285. DOI: 10.1007/s13238-013-3009-x
RESEARCH ARTICLE
RESEARCH ARTICLE

Structures of SdrD from Staphylococcus aureusreveal the molecular mechanism of how the cell surface receptors recognize their ligands

  • Xiao Wang1, Jingpeng Ge1, Bao Liu2, Yulin Hu3, Maojun Yang1()
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Abstract

Staphylococcus aureus is the most important Gram-positive colonizer of human skin and nasal passage, causing high morbidity and mortality. SD-repeat containing protein D (SdrD), an MSCRAMM (Microbial Surface Components Recognizing Adhesive Matrix Molecules) family surface protein, plays an important role in S. aureus adhesion and pathogenesis, while its binding target and molecular mechanism remain largely unknown. Here we solved the crystal structures of SdrD N2-N3 domain and N2-N3-B1 domain. Through structural analysis and comparisons, we characterized the ligand binding site of SdrD, and proposed a featured sequence motif of its potential ligands. In addition, the structures revealed for the fi rst time the interactions between B1 domain and N2-N3 domain among B domain-containing MSCRAMMs. Our results may help in understanding the roles SdrD plays in S. aureus adhesion and shed light on the development of novel antibiotics.

Keywords

SdrD / adhesin / MSCRAMM / Staphylococcus aureus

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Xiao Wang, Jingpeng Ge, Bao Liu, Yulin Hu, Maojun Yang. Structures of SdrD from Staphylococcus aureusreveal the molecular mechanism of how the cell surface receptors recognize their ligands. Prot Cell, 2013, 4(4): 277‒285 https://doi.org/10.1007/s13238-013-3009-x

References

[1] Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., Mc-Coy, A.J., Moriarty, N.W., Read, R.J., Sacchettini, J.C., Sauter, N.K., and Terwilliger, T.C. (2002). PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. Sect. D-Biol. Crystallogr . 58, 1948-1954 .10.1107/S0907444902016657
[2] Barbu, E.M., Ganesh, V.K., Gurusiddappa, S., Mackenzie, R.C., Foster, T.J., Sudhof, T.C., and Hook, M. (2010). beta-Neurexin is a ligand for the Staphylococcus aureus MSCRAMM SdrC. PLoS Pathog . 6, 11.10.1371/journal.ppat.1000726
[3] Costerton, J.W., Stewart, P.S., and Greenberg, E.P. (1999). Bacterial biofi lms: A common cause of persistent infections. Science 284, 1318-1322 .10.1126/science.284.5418.1318
[4] Deivanayagam, C.C.S., Rich, R.L., Carson, M., Owens, R.T., Danthuluri, S., Bice, T., Hook, M., and Narayana, S.V.L. (2000). Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Struct Fold Des 8, 67-78 .10.1016/S0969-2126(00)00081-2
[5] Deivanayagam, C.C.S., Wann, E.R., Chen, W., Carson, M., Rajashankar, K.R., Hook, M., and Narayana, S.V.L. (2002). A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fi brinogen-binding MSCRAMM, clumping factor A. EMBO J 21, 6660-6672 .10.1093/emboj/cdf619
[6] Diekema, D.J., Pfaller, M.A., Schmitz, F.J., Smayevsky, J., Bell, J., Jones, R.N., Beach, M., and Grp, S.P. (2001). Survey of infections due to Staphylococcus species: Frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacifi c region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin Infect Dis 32, S114-132 .10.1086/320184
[7] Downer, R., Roche, F., Park, P.W., Mecham, R.P., and Foster, T.J. (2002). The elastin-binding protein of Staphylococcus aureus (EbpS) is expressed at the cell surface as an integral membrane protein and not as a cell wall-associated protein. J Biol Chem 277, 243-250 .10.1074/jbc.M107621200
[8] Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D-Biol Crystallogr 60, 2126-2132 .10.1107/S0907444904019158
[9] Foster, T.J., and Hook, M. (1998). Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6, 484-488 .10.1016/S0966-842X(98)01400-0
[10] Ganesh, V.K., Barbu, E.M., Deivanayagam, C.C.S., Le, B., Anderson, A.S., Matsuka, Y.V., Lin, S.L., Foster, T.J., Narayana, S.V.L., and Hook, M. (2011). Structural and biochemical characterization of Staphylococcus aureus clumping factor B/ligand interactions. J Biol Chem 286, 25963-25972 .10.1074/jbc.M110.217414
[11] Ganesh, V.K., Rivera, J.J., Smeds, E., Ko, Y.P., Bowden, M.G., Wann, E.R., Gurusiddappa, S., Fitzgerald, J.R., and Hook, M. (2008). A structural model of the Staphylococcus aureus ClfA-fi brinogen interaction opens new avenues for the design of anti-Staphylococcal therapeutics. PLoS Pathog . 4, 10.10.1371/journal.ppat.1000226
[12] Gordon, R.J., and Lowy, F.D. (2008). Pathogenesis of methicillinresistant Staphylococcus aureus infection. Clin Infect Dis 46, S350-359 .10.1086/533591
[13] Hartford, O.M., Wann, E.R., Hook, M., and Foster, T.J. (2001). Identification of residues in the Staphylococcus aureus fi brinogen-binding MSCRAMM clumping factor A (ClfA) that are important for ligand binding. J. Biol. Chem . 276, 2466-2473 .10.1074/jbc.M007979200
[14] Jancarik, J., Scott, W.G., Milligan, D.L., Koshland, D.E., and Kim, S.H. (1991). Crystallization and preliminary-x-ray diffraction study of the ligand-binding domain of the bacterial chemotaxis-mediating aspartate receptor of salmonella-typhimurium. J Mol Biol 221, 31-34 .10.1016/0022-2836(91)80198-4
[15] Josefsson, E., O’Connell, D., Foster, T.J., Durussel, I., and Cox, J.A. (1998). The binding of calcium to the B-repeat segment of SdrD, a cell surface protein of Staphylococcus aureus. J Biol Chem 273, 31145-31152 .10.1074/jbc.273.47.31145
[16] Kluytmans, J., vanBelkum, A., and Verbrugh, H. (1997). Nasal carriage of Staphylococcus aureus: Epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10, 505-520 .
[17] Lowy, F.D. (2003). Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Invest 111, 1265-1273 .
[18] Maltezou, H.C., and Giamarellou, H. (2006). Community-acquired methicillin-resistant Staphylococcus aureus infections. Int J Antimicrob Agents 27, 87-96 .10.1016/j.ijantimicag.2005.11.004
[19] McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007). Phaser crystallographic software. J Appl Crystallogr 40, 658-674 .10.1107/S0021889807021206
[20] McCrea, K.W., Hartford, O., Davis, S., Eidhin, D.N., Lina, G., Speziale, P., Foster, T.J., and Hook, M. (2000). The serine-aspartate repeat (Sdr) protein family in Staphylococcus epidermidis. Microbiology (UK) 146, 1535-1546 .
[21] Mongkolrattanothai, K., Boyle, S., Kahana, M.D., and Daum, R.S. (2003). Severe Staphylococcus aureus infections caused by clonally related community-acquired methicillin-susceptible and methicillin- resistant isolates. Clin Infect Dis 37, 1050-1058 .10.1086/378277
[22] Moran, G.J., Krishnadasan, A., Gorwitz, R.J., Fosheim, G.E., McDougal, L.K., Carey, R.B., Talan, D.A., and Grp, E.M.I.N.S. (2006). Methicillin-resistant S-aureus infections among patients in the emergency department. N Engl J Med 355, 666-674 .10.1056/NEJMoa055356
[23] O’Riordan, K., and Lee, J.C. (2004). Staphylococcus aureus capsular polysaccharides. Clin Microbiol Rev 17, 218-234 .10.1128/CMR.17.1.218-234.2004
[24] Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276, 307-326 .10.1016/S0076-6879(97)76066-X
[25] Patti, J.M., and Hook, M. (1994). Microbial adhesins recognizing extracellular-matrix macromolecules. Curr Opin Cell Biol 6, 752-758 .10.1016/0955-0674(94)90104-X
[26] Ponnuraj, K., Bowden, M.G., Davis, S., Gurusiddappa, S., Moore, D., Choe, D., Xu, Y., Hook, M., and Narayana, S.V.L. (2003). A “dock, lock, and latch” structural model for a staphylococcal adhesin binding to fi brinogen. Cell 115, 217-228 .10.1016/S0092-8674(03)00809-2
[27] Schito, G.C. (2006). The importance of the development of antibiotic resistance in Staphylococcus aureus. Clin Microbiol Infect 12, 3-8 .10.1111/j.1469-0691.2006.01343.x
[28] Schneider, T.R., and Sheldrick, G.M. (2002). Substructure solution with SHELXD. Acta Crystallogr Sect D-Biol Crystallogr 58, 1772-1779 .10.1107/S0907444902011678
[29] Trad, S., Allignet, J., Frangeul, L., Davi, M., Vergassola, M., Couve, E., Morvan, A., Kechrid, A., Buchrieser, C., Glaser, P., . (2004). DNA macroarray for identification and typing of Staphylococcus aureus isolates. J Clin Microbiol 42, 2054-2064 .10.1128/JCM.42.5.2054-2064.2004
[30] Tung, H.S., Guss, B., Hellman, U., Persson, L., Rubin, K., and Ryden, C. (2000). A bone sialoprotein-binding protein from Staphylococcus aureus: a member of the staphylococcal Sdr family. Biochem J 345, 611-619 .10.1042/0264-6021:3450611
[31] Weber, J.T. (2005). Community-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis 41, S269-272 .10.1086/430788
[32] Xiang, H., Feng, Y., Wang, J.W., Liu, B., Chen, Y.G., Liu, L., Deng, X.M., and Yang, M.J. (2012). Crystal structures reveal the multi-ligand binding mechanism of Staphylococcus aureus ClfB. Plos Pathogens 8, 2751-2751 .10.1371/journal.ppat.1002751
[33] Zhang, L.Q., Xiang, H., Gao, J.L., Hu, J., Miao, S.Y., Wang, L.F., Deng, X.M., and Li, S.T. (2010). Purifi cation, characterization, and crystallization of the adhesive domain of SdrD from Staphylococcus aureus. Protein Expr Purif 69, 204-208 .10.1016/j.pep.2009.09.007
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