Register      Login
Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
Shopping Cart: ( empty )
You are here: Home > Journals > CH > CH14304
RESEARCH FRONT
Contents Vol 67(12)

The Relevance of Structural Biology in Studying Molecules Involved in Parasite–Host Interactions: Potential for Designing New Interventions

Lyndel Mason A , Parisa Amani B , Megan Cross A , Joshua Baker A , Ulla-Maja Bailey A , Malcolm K. Jones C D , Robin B. Gasser E and Andreas Hofmann A E F G
+ Author Affiliations
- Author Affiliations

A Eskitis Institute, Griffith University, Nathan, Qld 4111, Australia.

B Department of Chemistry, K. N. Toosi University of Technology, Tehran, 19697, Iran.

C School of Veterinary Science, The University of Queensland, Gatton, Qld 4072, Australia.

D QIMR Berghofer Medical Research Institute, Herston, Qld 4029, Australia.

E Faculty of Veterinary Science, The University of Melbourne, Parkville, Vic. 3010, Australia.

F Queensland Tropical Health Alliance, Smithfield, Qld 4878, Australia.

G Corresponding author. Email: a.hofmann@griffith.edu.au




Andreas Hofmann obtained his doctoral degree for studies at the Max Planck Institute for Biochemistry (Munich, Germany) in the laboratory of Robert Huber. After a post-doctoral term at the National Cancer Institute in Maryland (USA) with Alex Wlodawer, Andreas established his own laboratory at The University of Edinburgh. Since 2006, he has lead the Structural Chemistry Program at Griffith University's Eskitis Institute. Andreas holds a Fellowship of the Higher Education Academy (UK), as well as an Honorary Senior Research Fellowship in the Faculty of Veterinary Science at the University of Melbourne. His research interests are in structure–function relationships of proteins involved in infectious and neurological diseases.

Australian Journal of Chemistry 67(12) 1732-1740 https://doi.org/10.1071/CH14304
Submitted: 15 May 2014  Accepted: 10 June 2014   Published: 1 August 2014

Abstract

New interventions against infectious diseases require a detailed knowledge and understanding of pathogen–host interactions and pathogeneses at the molecular level. The combination of the considerable advances in systems biology research with methods to explore the structural biology of molecules is poised to provide new insights into these areas. Importantly, exploring three-dimensional structures of proteins is central to understanding disease processes, and establishing structure–function relationships assists in identification and assessment of new drug and vaccine targets. Frequently, the molecular arsenal deployed by invading pathogens, and in particular parasites, reveals a common theme whereby families of proteins with conserved three-dimensional folds play crucial roles in infectious processes, but individual members of such families show high levels of specialisation, which is often achieved through grafting particular structural features onto the shared overall fold. Accordingly, the applicability of predictive methodologies based on the primary structure of proteins or genome annotations is limited, particularly when thorough knowledge of molecular-level mechanisms is required. Such instances exemplify the need for experimental three-dimensional structures provided by protein crystallography, which remain an essential component of this area of research. In the present article, we review two examples of key protein families recently investigated in our laboratories, which could represent intervention targets in the metabolome or secretome of parasites.


References

[1]  S. Kutz, A. Dobson, E. Hoberg, Science 2009, 326, 1187.
         | Crossref | GoogleScholarGoogle Scholar | 19965449PubMed |

[2]  J. N. Mills, K. L. Gage, A. S. Khan, Environ. Health Perspect. 2010, 118, 1507.
         | Crossref | GoogleScholarGoogle Scholar | 20576580PubMed |

[3]  C. E. Barry, Curr. Top. Med. Chem. 2011, 11, 1216.
         | Crossref | GoogleScholarGoogle Scholar | 21401509PubMed |

[4]  C. Arama, M. Troye-Blomberg, J. Intern. Med. 2014, 275, 456.
         | Crossref | GoogleScholarGoogle Scholar | 24635625PubMed |

[5]  K. J. Evans, L. Kedzierski, J. Trop. Med. 2012, 2012, 892817.
         | Crossref | GoogleScholarGoogle Scholar | 21912561PubMed |

[6]  C. Y. Leow, C. Willis, A. Osman, L. Mason, A. Simon, B. J. Smith, R. B. Gasser, M. K. Jones, A. Hofmann, FEBS J. 2014, 281, 1209.
         | Crossref | GoogleScholarGoogle Scholar |

[7]  A. Winter, A. M. Yusof, E. Gao, H. L. Yan, A. Hofmann, FEBS J. 2006, 273, 3238.
         | Crossref | GoogleScholarGoogle Scholar | 16857011PubMed |

[8]  S. K. Weeratunga, A. Osman, N. J. Hu, C. K. Wang, L. Mason, S. Svärd, G. Hope, M. K. Jones, A. Hofmann, J. Mol. Biol. 2012, 423, 169.
         | Crossref | GoogleScholarGoogle Scholar | 22796298PubMed |

[9]  A. Hofmann, A. Osman, C. Y. Leow, P. Driguez, D. P. McManus, M. K. Jones, Bioessays 2010, 32, 967.
         | Crossref | GoogleScholarGoogle Scholar | 21105292PubMed |

[10]  C. Y. Leow, C. Willis, R. B. Gasser, A. Hofmann, M. K. Jones, Br. J. Pharmacol. 2014, in press.

[11]  L. Schulte, E. Lovas, K. Green, G. N. Gobert, J. Mulvenna, G. Morgan, M. K. Jones, Int. J. Parasitol. 2013, 43, 785.
         | Crossref | GoogleScholarGoogle Scholar | 23702130PubMed |

[12]  E. Hanssen, C. Dekiwadia, D. T. Riglar, M. Rug, L. Lemgruber, A. F. Cowman, M. Cyrklaff, M. Kudryashev, F. Frischknecht, J. Baum, S. A. Ralph, Cell. Microbiol. 2013, 15, 1457.
         | Crossref | GoogleScholarGoogle Scholar | 23461734PubMed |

[13]  C. Cantacessi, A. Hofmann, B. E. Campbell, R. B. Gasser, in Molecular Diagnostics and High-Throughput Strategies (Eds M. V. Cunha, J. Inácio) 2014, Ch. 29 (Springer: New York, NY), in press.

[14]  A. Hofmann, C. K. Wang, A. Osman, D. Camp, Struct. Chem. 2010, 21, 1117.
         | Crossref | GoogleScholarGoogle Scholar |

[15]  K. Sandhoff, T. Kolter, Trends Cell Biol. 1996, 6, 98.
         | Crossref | GoogleScholarGoogle Scholar | 15157485PubMed |

[16]  T. Linke, G. Wilkening, F. Sadeghlar, H. Mozcall, K. Bernardo, E. Schuchman, K. Sandhoff, J. Biol. Chem. 2001, 276, 5760.
         | Crossref | GoogleScholarGoogle Scholar | 11104761PubMed |

[17]  W. Yuan, X. Qi, P. Tsang, S. Kang, P. A. Illarionov, G. S. Besra, J. Gumperz, P. Cresswell, Proc. Natl. Acad. Sci. USA 2007, 104, 5551.
         | Crossref | GoogleScholarGoogle Scholar | 17372201PubMed |

[18]  F. Ciaffoni, R. Salvioli, M. Tatti, G. Arancia, P. Crateri, A. M. Vaccaro, J. Biol. Chem. 2001, 276, 31583.
         | Crossref | GoogleScholarGoogle Scholar | 11406625PubMed |

[19]  T. A. Don, Y. Oksov, S. Lustigman, A. Loukas, Parasitology 2007, 134, 427.
         | Crossref | GoogleScholarGoogle Scholar | 17109779PubMed |

[20]  S. Nawaratna, D. McManus, L. Moertel, G. Gobert, M. Jones, PLoS Negl. Trop. Dis. 2011, 5, e1043.
         | Crossref | GoogleScholarGoogle Scholar | 21541360PubMed |

[21]  J. Chen, T. Zhang, C. Ju, B. Xu, Y. Lu, X. Mo, S. Chen, Y. Fan, W. Hu, X. Zhou, J. Proteomics 2014, 98, 289.
         | Crossref | GoogleScholarGoogle Scholar | 24448400PubMed |

[22]  G. Wilkening, T. Linke, K. Sandhoff, J. Biol. Chem. 1998, 273, 30271.
         | Crossref | GoogleScholarGoogle Scholar | 9804787PubMed |

[23]  T. Roeder, M. Stanisak, C. Gelhaus, I. Bruchhaus, J. Grötzinger, M. Leippe, Dev. Comp. Immunol. 2010, 34, 203.
         | Crossref | GoogleScholarGoogle Scholar | 19818806PubMed |

[24]  J. Matsuda, M. T. Vanier, Y. Saito, J. Tohyama, K. Suzuki, K. Suzuki, Hum. Mol. Genet. 2001, 10, 1191.
         | Crossref | GoogleScholarGoogle Scholar | 11371512PubMed |

[25]  K. A. Kretz, G. S. Carson, S. Morimoto, Y. Kishimoto, A. L. Fluharty, J. S. O’Brien, Proc. Natl. Acad. Sci. USA 1990, 87, 2541.
         | Crossref | GoogleScholarGoogle Scholar | 2320574PubMed |

[26]  Y. Sun, B. Liou, H. Ran, M. R. Skelton, M. T. Williams, C. V. Vorhees, K. Kitatani, Y. A. Hannun, D. P. Witte, Y.-H. Xu, G. A. Grabowski, Hum. Mol. Genet. 2010, 19, 1088.
         | Crossref | GoogleScholarGoogle Scholar | 20047948PubMed |

[27]  O. Hecht, N. A. Van Nuland, K. Schleinkofer, A. J. Dingley, H. Bruhn, M. Leippe, J. Grötzinger, J. Biol. Chem. 2004, 279, 17834.
         | Crossref | GoogleScholarGoogle Scholar | 14970207PubMed |

[28]  J. Lee, P. Cho, T. Y. Kim, S. Kang, K. Song, S. Hong, Biochem. Biophys. Res. Commun. 2002, 296, 1238.
         | Crossref | GoogleScholarGoogle Scholar | 12207906PubMed |

[29]  A. M. Espino, G. V. Hillyer, J. Parasitol. 2004, 90, 876.
         | Crossref | GoogleScholarGoogle Scholar | 15357089PubMed |

[30]  J. Lee, T. Kim, X. Gan, S. Kang, S. Hong, Parasitol. Int. 2003, 52, 175.
         | Crossref | GoogleScholarGoogle Scholar | 12798930PubMed |

[31]  O. Figueroa-Santiago, B. Delgado, A. M. Espino, Diagn. Microbiol. Infect. Dis. 2011, 70, 355.
         | Crossref | GoogleScholarGoogle Scholar | 21683266PubMed |

[32]  A. M. Espino, A. Morales, B. Delgado, F. M. Rivera, O. Figueroa, E. Suárez, Ethn. Dis. 2010, 20, 17.

[33]  C. A. Morrison, T. Colin, J. L. Sexton, F. Bowen, J. Wicker, T. Friedel, T. W. Spithill, Vaccine 1996, 14, 1603.
         | Crossref | GoogleScholarGoogle Scholar | 9032888PubMed |

[34]  J. P. Dalton, S. McGonigle, T. P. Rolph, S. J. Andrews, Infect. Immun. 1996, 64, 5066.
         | 8945548PubMed |

[35]  A. Muro, V. Ramajo, J. López, F. Simón, G. V. Hillyer, Vet. Parasitol. 1997, 69, 219.
         | Crossref | GoogleScholarGoogle Scholar | 9195732PubMed |

[36]  D. Torres, A. M. Espino, Infect. Immun. 2006, 74, 4932.
         | Crossref | GoogleScholarGoogle Scholar | 16861685PubMed |

[37]  D. Andreu, C. Carreño, C. Linde, H. G. Boman, M. Andersson, Biochem. J. 1999, 344, 845.
         | Crossref | GoogleScholarGoogle Scholar | 10585872PubMed |

[38]  Z. Wang, E. Choice, A. Kaspar, D. Hanson, S. Okada, S. C. Lyu, A. M. Krensky, C. Clayberger, J. Immunol. 2000, 165, 1486.
         | Crossref | GoogleScholarGoogle Scholar | 10903754PubMed |

[39]  L. Yang, J. Johansson, R. Ridsdale, H. Willander, M. Fitzen, H. T. Akinbi, T. E. Weaver, J. Immunol. 2010, 184, 975.
         | Crossref | GoogleScholarGoogle Scholar | 20007532PubMed |

[40]  D. H. Anderson, M. R. Sawaya, D. Cascio, W. Ernst, R. Modlin, A. Krensky, D. Eisenberg, J. Mol. Biol. 2003, 325, 355.
         | Crossref | GoogleScholarGoogle Scholar | 12488100PubMed |

[41]  E. Liepinsh, M. Andersson, J. M. Ruysschaert, G. Otting, Nat. Struct. Biol. 1997, 4, 793.
         | Crossref | GoogleScholarGoogle Scholar | 9334742PubMed |

[42]  J. Kervinen, G. J. Tobin, J. Costa, D. S. Waugh, A. Wlodawer, A. Zdanov, EMBO J. 1999, 18, 3947.
         | Crossref | GoogleScholarGoogle Scholar | 10406799PubMed |

[43]  B. C. Bornhauser, P. Olsson, D. Lindholm, J. Biol. Chem. 2003, 278, 35412.
         | Crossref | GoogleScholarGoogle Scholar | 12826659PubMed |

[44]  C. Willis, C. Wang, A. Osman, A. Simon, D. Pickering, J. Mulvenna, A. Riboldi-Tunicliffe, M. Jones, A. Loukas, A. Hofmann, PLoS ONE 2011, 6, e25369.
         | Crossref | GoogleScholarGoogle Scholar | 21991310PubMed |

[45]  M. Miteva, M. Andersson, A. Karshikoff, G. Otting, FEBS Lett. 1999, 462, 155.
         | Crossref | GoogleScholarGoogle Scholar | 10580110PubMed |

[46]  M. Rossmann, R. Shultz-Heienbrok, J. Behlke, N. Remmel, C. Alings, K. Sandhoff, W. Saenger, T. Maier, Structure 2008, 16, 809.
         | Crossref | GoogleScholarGoogle Scholar | 18462685PubMed |

[47]  Y. Wang, G. A. Grabowski, X. Qi, Arch. Biochem. Biophys. 2003, 415, 43.
         | Crossref | GoogleScholarGoogle Scholar | 12801511PubMed |

[48]  T. Gutsmann, B. Riekens, H. Bruhn, A. Wiese, U. Seydel, M. Leippe, Biochemistry 2003, 42, 9804.
         | Crossref | GoogleScholarGoogle Scholar | 12911324PubMed |

[49]  V. Ahn, K. Faull, J. Whitelegge, A. Fluharty, G. Prive, Proc. Natl. Acad. Sci. USA 2003, 100, 38.
         | Crossref | GoogleScholarGoogle Scholar | 12518053PubMed |

[50]  J. P. Hewitson, J. R. Grainger, R. M. Maizels, Mol. Biochem. Parasitol. 2009, 167, 1.
         | Crossref | GoogleScholarGoogle Scholar | 19406170PubMed |

[51]  D. C. Koboldt, K. M. Steinberg, D. E. Larson, R. K. Wilson, E. R. Mardis, Cell 2013, 155, 27.
         | Crossref | GoogleScholarGoogle Scholar | 24074859PubMed |

[52]  J. Mulvenna, B. Hamilton, S. H. Nagaraj, D. Smyth, A. Loukas, J. J. Gorman, Mol. Cell. Proteomics 2009, 8, 109.
         | Crossref | GoogleScholarGoogle Scholar | 18753127PubMed |

[53]  C. Cantacessi, B. E. Campbell, A. Visser, P. Geldhof, M. J. Nolan, A. J. Nisbet, J. B. Matthews, A. Loukas, A. Hofmann, D. Otranto, P. W. Sternberg, R. B. Gasser, Biotechnol. Adv. 2009, 27, 376.
         | Crossref | GoogleScholarGoogle Scholar | 19239923PubMed |

[54]  B. J. D. Datu, R. B. Gasser, S. H. Nagaraj, E. K. Ong, P. O’Donoghue, R. McInnes, S. Ranganathan, A. Loukas, PLoS Negl. Trop. Dis. 2008, 2, e130.
         | Crossref | GoogleScholarGoogle Scholar |

[55]  A. Loukas, J. Bethony, S. Brooker, P. Hotez, Lancet Infect. Dis. 2006, 6, 733.
         | Crossref | GoogleScholarGoogle Scholar | 17067922PubMed |

[56]  L. P. Farias, D. Rodrigues, V. Cunna, H. K. Rofatto, E. L. Faquim-Mauro, L. C. C. Leite, PLoS Negl. Trop. Dis. 2012, 6, e1510.
         | Crossref | GoogleScholarGoogle Scholar | 22347513PubMed |

[57]  C. K. Wang, U. Broder, S. K. Weeratunga, R. B. Gasser, A. Loukas, A. Hofmann, Bioinformatics 2012, 28, 1026.
         | Crossref | GoogleScholarGoogle Scholar | 22332239PubMed |

[58]  A. Osman, C. K. Wang, A. Winter, A. Loukas, L. Tribolet, R. B. Gasser, A. Hofmann, Biotechnol. Adv. 2012, 30, 652.
         | Crossref | GoogleScholarGoogle Scholar | 22120067PubMed |

[59]  C. Cantacessi, A. Hofmann, N. D. Young, R. S. Hall, A. Loukas, R. B. Gasser, PLoS ONE 2012, 7, e31164.
         | Crossref | GoogleScholarGoogle Scholar | 22384000PubMed |

[60]  C. Cantacessi, J. Mulvenna, N. D. Young, M. Kasny, P. Horak, A. Aziz, A. Hofmann, A. Loukas, R. B. Gasser, Mol. Cell. Proteomics 2012, 11, 1340.
         | Crossref | GoogleScholarGoogle Scholar | 22899770PubMed |

[61]  E. M. Schwarz, P. K. Korhonen, B. E. Campbell, N. D. Young, A. R. Jex, A. Jabbar, R. S. Hall, A. Mondal, A. C. Howe, J. Pell, A. Hofmann, P. R. Boag, X.-Q. Zhu, T. Gregory, A. Loukas, B. A. Williams, I. Antoshechkin, C. Brown, P. W. Sternberg, R. B. Gasser, Genome Biol. 2013, 14, R89.
         | Crossref | GoogleScholarGoogle Scholar | 23985341PubMed |

[62]  G. M. Gibbs, K. Roelants, M. K. O’Bryan, Endocr. Rev. 2008, 29, 865.
         | Crossref | GoogleScholarGoogle Scholar | 18824526PubMed |

[63]  O. A. Asojo, G. Goud, K. Dhar, A. Loukas, B. Zhan, V. Deumic, S. Liu, G. E. O. Borgstahl, P. J. Hotez, J. Mol. Biol. 2005, 346, 801.
         | Crossref | GoogleScholarGoogle Scholar | 15713464PubMed |

[64]  L. Mason, L. Tribolet, A. Simon, N. von Gnielinski, L. Nienaber, P. Taylor, C. Willis, M. K. Jones, P. W. Sternberg, R. B. Gasser, A. Loukas, A. Hofmann, Int. J. Biochem. Cell Biol. 2014, 50, 146.
         | Crossref | GoogleScholarGoogle Scholar | 24631931PubMed |

[65]  A. J. Fay, X. Qian, Y. N. Jan, L. Y. Jan, Proc. Natl. Acad. Sci. USA 2006, 103, 17548.
         | Crossref | GoogleScholarGoogle Scholar | 17085590PubMed |

[66]  P. J. Muchowski, L. Zhang, E. R. Chang, H. R. Soule, E. F. Plow, M. Moyle, J. Biol. Chem. 1994, 269, 26419.
         | 7929363PubMed |

[67]  A. A. Veenstra, J. Tang, T. S. Kern, PLoS ONE 2013, 8, e78405.
         | Crossref | GoogleScholarGoogle Scholar | 24205223PubMed |

[68]  A. Del Valle, B. F. Jones, L. M. Harrison, R. C. Chadderdon, M. Cappello, Mol. Biochem. Parasitol. 2003, 129, 167.
         | Crossref | GoogleScholarGoogle Scholar | 12850261PubMed |

[69]  R. O. Hynes, Cell 2002, 110, 673.
         | Crossref | GoogleScholarGoogle Scholar | 12297042PubMed |

[70]  P. L. Stewart, G. R. Nemerow, Trends Microbiol. 2007, 15, 500.
         | Crossref | GoogleScholarGoogle Scholar | 17988871PubMed |

[71]  S. Stefanic, J. Dvorak, M. Horn, S. Braschi, D. Sojka, D. S. Ruelas, B. Suzuki, K. Lim, S. D. Hopkins, J. H. McKerrow, C. R. Caffrey, PLoS Negl. Trop. Dis. 2010, 4, e850.
         | Crossref | GoogleScholarGoogle Scholar | 20976050PubMed |

[72]  A. G. Maule, P. McVeigh, J. J. Dalzell, L. Atkinson, A. Mousley, N. J. Marks, Trends Parasitol. 2011, 27, 505.
         | Crossref | GoogleScholarGoogle Scholar | 21885343PubMed |

[73]  M. Moyle, D. L. Foster, D. E. McGrath, S. M. Brown, Y. Laroche, J. De Meutter, P. Stanssens, C. A. Bogowitz, V. A. Fried, J. A. Ely, H. R. Soule, G. P. Vlasuk, J. Biol. Chem. 1994, 269, 10008.
         | 7908286PubMed |

[74]  L. Zhang, E. F. Plow, J. Biol. Chem. 1997, 272, 17558.
         | Crossref | GoogleScholarGoogle Scholar | 9211902PubMed |

[75]  B. Mahalingam, K. Ajroud, J. L. Alonso, S. Anand, B. D. Adair, A. L. Horenstein, F. Malavasi, J. Xiong, M. A. Arnaout, J. Immunol. 2011, 187, 6393.
         | Crossref | GoogleScholarGoogle Scholar | 22095715PubMed |

[76]  S. L. Goodman, M. Picard, Trends Pharmacol. Sci. 2012, 33, 405.
         | Crossref | GoogleScholarGoogle Scholar | 22633092PubMed |

[77]  J. Vazquez-Prado, I. Meza, Arch. Med. Res. 1992, 23, 125.
         | 1340273PubMed |

[78]  P. Talamas-Rohana, J. L. Rosales-Encina, M. C. Gutierrez, V. Hernandez, Arch. Med. Res. 1992, 23, 119.
         | 1340272PubMed |

[79]  G. N. Sarma, V. A. Manning, L. M. Ciuffetti, P. A. Karplus, Plant Cell 2005, 17, 3190.
         | Crossref | GoogleScholarGoogle Scholar | 16214901PubMed |

[80]  J. M. Harper, E. F. Hoff, V. B. Carruthers, Mol. Biochem. Parasitol. 2004, 134, 201.
         | Crossref | GoogleScholarGoogle Scholar | 15003840PubMed |

[81]  S. Gantt, C. Persson, K. Rose, A. J. Birkett, R. Abagyan, V. Nussenzweig, Infect. Immun. 2000, 68, 3667.
         | Crossref | GoogleScholarGoogle Scholar | 10816526PubMed |

[82]  K. J. Robson, S. Naitza, G. Barker, R. E. Sinden, A. Crisanti, Mol. Biochem. Parasitol. 1997, 84, 1.
         | Crossref | GoogleScholarGoogle Scholar | 9041516PubMed |

[83]  R. R. Akhouri, A. Sharma, P. Malhotra, A. Sharma, Malar. J. 2008, 7, 63.
         | Crossref | GoogleScholarGoogle Scholar | 18426606PubMed |

[84]  Y. Cho, B. F. Jones, J. J. Vermeire, L. Leng, L. DiFedele, L. Harrisson, H. Xiong, Y.-K. A. Kwong, Y. Chen, R. Bucala, E. Lolis, M. Cappello, J. Biol. Chem. 2007, 282, 23447.
         | Crossref | GoogleScholarGoogle Scholar | 17567581PubMed |

[85]  Y. Cho, J. J. Vermeire, J. S. Merkel, L. Leng, X. Du, R. Bucala, M. Cappello, E. Lolis, Chem. Biol. 2011, 18, 1089.
         | Crossref | GoogleScholarGoogle Scholar | 21944748PubMed |

[86]  B. Zhan, H. Santiago, B. Keegan, P. Gillespie, J. Xue, J. Bethony, L. M. de Oliveira, D. Jiang, D. Diemert, S.-H. Xiao, K. Jones, X. Feng, P. J. Hotez, M. E. Bottazzi, Parasite Immunol. 2012, 34, 404.
         | Crossref | GoogleScholarGoogle Scholar | 22651670PubMed |

[87]  L. Kedzierski, J. Montgomery, D. Bullen, J. Curtis, E. Gardiner, A. Jimenez-Ruiz, E. Handman, J. Immunol. 2004, 172, 4902.
         | Crossref | GoogleScholarGoogle Scholar | 15067069PubMed |

[88]  M. Kelleher, S. F. Moody, P. Mirabile, A. H. Osborn, A. Bacic, E. Handman, Infect. Immun. 1995, 63, 43.
         | 7806383PubMed |

[89]  L. Chen, K. V. N. Rao, Y. He, K. Ramaswamy, J. Biol. Chem. 2002, 277, 34329.
         | Crossref | GoogleScholarGoogle Scholar | 12107158PubMed |

[90]  F. Trottein, S. Nutten, J. P. Papin, C. Leportier, O. Poulain-Godefroy, A. Capron, M. Capron, J. Immunol. 1997, 159, 804.
         | 9218598PubMed |

[91]  W. DeLano, PyMOL 2002 (Schrodinger: New York, NY).