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Approaches for the identification of potential excreted/secreted proteins of Leishmania major parasites

  • M. CHENIK (a1), S. LAKHAL (a1), N. BEN KHALEF (a1), L. ZRIBI (a1), H. LOUZIR (a1) and K. DELLAGI (a1)...
Abstract

Leishmania parasites are able to survive in host macrophages despite the harsh phagolysosomal vacuoles conditions. This could reflect, in part, their capacity to secrete proteins that may play an essential role in the establishment of infection and serve as targets for cellular immune responses. To characterize Leishmania major proteins excreted/secreted early after promastigote entry into the host macrophage, we have generated antibodies against culture supernatants of stationary-phase promastigotes collected 6 h after incubation in conditions that partially reproduce those prevailing in the parasitophorous vacuole. The screening of an L. major cDNA library with these antibodies led us to isolate 33 different cDNA clones that we report here. Sequence analysis revealed that the corresponding proteins could be classified in 3 groups: 9 proteins have been previously described as excreted/secreted in Leishmania and/or other species; 11 correspond to known proteins already characterized in Leishmania and/or other species although it is unknown whether they are excreted/secreted and 13 code for unknown proteins. Interestingly, the latter are transcribed as shown by RT-PCR and some of them are stage regulated. The L. major excreted/secreted proteins may constitute putative virulence factors, vaccine candidates and/or new drug targets.

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Tel: +216 1 1783022. Fax: +216 11 791833. E-mail: mehdi.chenik@pasteur.rns.tn
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Akopyants, N. S., Matlib, R. S., Bukanova, E. N., Smeds, M. R., Brownstein, B. H., Stormo, G. D. and Beverley, S. M. ( 2004). Expression profiling using random genomic DNA microarrays identifies differentially expressed genes associated with three major developmental stages of the protozoan parasite Leishmania major. Molecular and Biochemical Parasitology136, 7186.

Alexander, J. and Russell, D. G. ( 1992). The interaction of Leishmania species with macrophages. Advances in Parasitology31, 175254.

Amer, A. O. and Swanson, M. S. ( 2002). A phagosome of one's own: a microbial guide to life in the macrophage. Current Opinion in Microbiology5, 5661.

Bates, P. A., Gottlieb, M. and Dwyer, D. M. ( 1988). Leishmania donovani: identification of glycoproteins released by promastigotes during growth in vitro. Experimental Parasitology67, 199209.

Ben Achour, Y., Chenik, M., Louzir, H. and Dellagi, K. ( 2002). Identification of a disulfide isomerase protein of Leishmania major as a putative virulence factor. Infection and Immunity70, 35763585.

Bendtsen, J. D., Jensen, L. J., Blom, N., Von Heijne, G. and Brunak, S. ( 2004). Feature-based prediction of non-classical and leaderless protein secretion. Protein Engineering, Design and Selection17, 349356.

Berberich, C., Ramirez-Pineda, J. R., Hambrecht, C., Alber, G., Skeiky, Y. A. and Moll, H. ( 2003). Dendritic cell (DC)-based protection against an intracellular pathogen is dependent upon DC-derived IL-12 and can be induced by molecularly defined antigens. Journal of Immunology170, 31713179.

Bousoffara, T., Louzir, H., Ben Salah, A. and Dellagi, K. ( 2004). Analysis of granzyme B activity as a surrogate marker of Leishmania-specific cell-mediated cytotoxicity in zoonotic cutaneous leishmaniasis. Journal of Infectious Diseases189, 12651273.

Browne, G. J. and Proud, C. G. ( 2002). Regulation of peptide-chain elongation in mammalian cells. European Journal of Biochemistry269, 53605368.

Buxbaum, L. U., Denise, H., Coombs, G. H., Alexander, J., Mottram, J. C. and Scott, P. ( 2003). Cysteine protease B of Leishmania mexicana inhibits host Th1 responses and protective immunity. Journal of Immunology171, 37113717.

Campbell, K., Diao, H., Ji, J. and Soong, L. ( 2003). DNA immunization with the gene encoding P4 nuclease of Leishmania amazonensis protects mice against cutaneous Leishmaniasis. Infection and Immunity71, 62706278.

Cao, Y., Matsumoto, T., Motomura, K., Ohtsuru, A., Yamashita, S. and Kosaka, M. ( 1998). Impaired induction of heat shock protein implicated in decreased thermotolerance in a temperature-sensitive multinucleated cell line. Pflügers Archiv437, 1520.

Carrero, J. C., Petrossian, P., Acosta, E., Sanchez-Zerpa, M., Ortiz-Ortiz, L. and Laclette, J. P. ( 2000). Cloning and characterization of Entamoeba histolytica antigens recognized by human secretory IgA antibodies. Parasitology Research86, 330334.

Collins, P. R., Stack, C. M., O'Neill, S. M., Doyle, S., Ryan, T., Brennan, G. P., Mousley, A., Stewart, M., Maule, A. G., Dalton, J. P. and Donnelly, S. ( 2004). Cathepsin L1, the major protease involved in liver fluke (Fasciola hepatica) virulence: propeptide cleavage sites and autoactivation of the zymogen secreted from gastrodermal cells. The Journal of Biological Chemistry279, 1703817046.

Condeelis, J. ( 1995). Elongation factor 1 alpha, translation and the cytoskeleton. Trends in Biochemical Sciences20, 169170.

Cornelissen, J. B., Gaasenbeek, C. P., Borgsteede, F. H., Holland, W. G., Harmsen, M. M. and Boersma, W. J. ( 2001). Early immunodiagnosis of fasciolosis in ruminants using recombinant Fasciola hepatica cathepsin L-like protease. International Journal for Parasitology31, 728737.

Cunningham, A. C. ( 2002). Parasitic adaptive mechanisms in infection by Leishmania. Experimental and Molecular Pathology72, 132141.

Dalton, J. P., Neill, S. O., Stack, C., Collins, P., Walshe, A., Sekiya, M., Doyle, S., Mulcahy, G., Hoyle, D., Khaznadji, E., Moire, N., Brennan, G., Mousley, A., Kreshchenko, N., Maule, A. G. and Donnelly, S. M. ( 2003). Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. International Journal for Parasitology33, 11731181.

Daryani, A., Hosseini, A. Z. and Dalimi, A. ( 2003). Immune responses against excreted/secreted antigens of Toxoplasma gondii tachyzoites in the murine model. Veterinary Parasitology113, 123134.

De Carvalho, L. P., Soto, M., Jeronimo, S., Dondji, B., Bacellar, O., Luz, V., Orge Orge, G., Alonso, C., Jesus, A. R. and Carvalho, E. M. ( 2003). Characterization of the immune response to Leishmania infantum recombinant antigens. Microbes and Infection5, 712.

Delgado, G., Parra-Lopez, C. A., Vargas, L. E., Hoya, R., Estupinan, M., Guzman, F., Torres, A., Alonso, C., Velez, I. D., Spinel, C. and Patarroyo, M. E. ( 2003). Characterizing cellular immune response to kinetoplastid membrane protein-11 (KMP-11) during Leishmania (Viannia) panamensis infection using dendritic cells (DCs) as antigen presenting cells (APCs). Parasite Immunology25, 199209.

Denise, H., Mcneil, K., Brooks, D. R., Alexander, J., Coombs, G. H. and Mottram, J. C. ( 2003). Expression of multiple CPB genes encoding cysteine proteases is required for Leishmania mexicana virulence in vivo. Infection and Immunity71, 31903195.

Desjeux, P. ( 1996). Leishmaniasis. Public health aspects and control. Clinics in Dermatology14, 417423.

Dobbin, C. A., Smith, N. C. and Johnson, A. M. ( 2002). Heat shock protein 70 is a potential virulence factor in murine toxoplasma infection via immunomodulation of host NF-kappa B and nitric oxide. Journal of Immunology169, 958965.

Dowd, A. J., Smith, A. M., Mcgonigle, S. and Dalton, J. P. ( 1994). Purification and characterisation of a second cathepsin L proteinase secreted by the parasitic trematode Fasciola hepatica. European Journal of Biochemistry223, 9198.

Duclos, S. and Desjardins, M. ( 2000). Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cellular Microbiology2, 365377.

Ferrari, D. M. and Soling, H. D. ( 1999). The protein disulphide-isomerase family: unravelling a string of folds. The Biochemical Journal339, 110.

Garlapati, S., Dahan, E. and Shapira, M. ( 1999). Effect of acidic pH on heat shock gene expression in Leishmania. Molecular and Biochemical Parasitology100, 95101.

Garrido, C., Schmitt, E., Cande, C., Vahsen, N., Parcellier, A. and Kroemer, G. ( 2003). HSP27 and HSP70: potentially oncogenic apoptosis inhibitors. Cell Cycle2, 579584.

Geldhof, P., Vercauteren, I., Knox, D., Demaere, V., Van Zeveren, A., Berx, G., Vercruysse, J. and Claerebout, E. ( 2003). Protein disulphide isomerase of Ostertagia ostertagi: an excretory-secretory product of L4 and adult worms? International Journal for Parasitology33, 129136.

Handman, E. ( 1999). Cell biology of Leishmania. Advances in Parasitology44, 139.

Handman, E., Osborn, A. H., Symons, F., Van Driel, R. and Cappai, R. ( 1995a). The Leishmania promastigote surface antigen 2 complex is differentially expressed during the parasite life cycle. Molecular and Biochemical Parasitology74, 189200.

Harmsen, M. M., Cornelissen, J. B., Buijs, H. E., Boersma, W. J., Jeurissen, S. H. and Van Milligen, F. J. ( 2004). Identification of a novel Fasciola hepatica cathepsin L protease containing protective epitopes within the propeptide. International Journal for Parasitology34, 675682.

Heid, C. A., Stevens, J., Livak, K. J. and Williams, P. M. ( 1996). Real time quantitative PCR. Genome Research6, 986994.

Houde, M., Bertholet, S., Gagnon, E., Brunet, S., Goyette, G., Laplante, A., Princiotta, M. F., Thibault, P., Sacks, D. and Desjardins, M. ( 2003). Phagosomes are competent organelles for antigen cross-presentation. Nature425, 402406.

Huang, J., Huang, Q., Zhou, X., Shen, M. M., Yen, A., Yu, S. X., Dong, G., Qu, K., Huang, P., Anderson, E. M., Daniel-Issakani, S., Buller, R. M., Payan, D. G. and Lu, H. H. ( 2004). The poxvirus p28 virulence factor is an E3 ubiquitin ligase. The Journal of Biological Chemistry279, 5411054116.

Hunter-Lavin, C., Davies, E. L., Bacelar, M. M., Marshall, M. J., Andrew, S. M. and Williams, J. H. ( 2004). Hsp70 release from peripheral blood mononuclear cells. Biochemical and Biophysical Research Communications324, 511517.

Imai, A., Matsuyama, T., Hanzawa, Y., Akiyama, T., Tamaoki, M., Saji, H., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., Tabata, S., Komeda, Y. and Takahashi, T. ( 2004). Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiology135, 15651573.

Jardim, A., Funk, V., Caprioli, R. M. and Olafson, R. W. ( 1995). Isolation and structural characterization of the Leishmania donovani kinetoplastid membrane protein-11, a major immunoreactive membrane glycoprotein. The Biochemical Journal305, 307313.

Jensen, A. T., Gasim, S., Ismail, A., Gaafar, A., Kurtzhals, J. A., Kemp, M., El Hassan, A. M., Kharazmi, A. and Theander, T. G. ( 1998). Humoral and cellular immune responses to synthetic peptides of the Leishmania donovani kinetoplastid membrane protein-11. Scandinavian Journal of Immunology48, 103109.

Jimenez-Ruiz, A., Boceta, C., Bonay, P., Requena, J. M. and Alonso, C. ( 1998). Cloning, sequencing, and expression of the PSA genes from Leishmania infantum. European Journal of Biochemistry251, 389397.

Kaiser, A. E., Gottwald, A. M., Wiersch, C. S., Maier, W. A. and Seitz, H. M. ( 2003). Spermidine metabolism in parasitic protozoa – a comparison to the situation in prokaryotes, viruses, plants and fungi. Folia Parasitologica50, 318.

Kebaier, C., Louzir, H., Chenik, M., Ben Salah, A. and Dellagi, K. ( 2001). Heterogeneity of wild Leishmania major isolates in experimental murine pathogenicity and specific immune response. Infection and Immunity69, 49064915.

Kedzierski, L., Montgomery, J., Bullen, D., Curtis, J., Gardiner, E., Jimenez-Ruiz, A. and Handman, E. ( 2004). A leucine-rich repeat motif of Leishmania parasite surface antigen 2 binds to macrophages through the complement receptor 3. Journal of Immunology172, 49024906.

Kemp, M., Handman, E., Kemp, K., Ismail, A., Mustafa, M. D., Kordofani, A. Y., Bendtzen, K., Kharazmi, A. and Theander, T. G. ( 1998). The Leishmania promastigote surface antigen-2 (PSA-2) is specifically recognised by Th1 cells in humans with naturally acquired immunity to L. major. FEMS Immunology and Medical Microbiology20, 209218.

Kurar, E. and Splitter, G. A. ( 1997). Nucleic acid vaccination of Brucella abortus ribosomal L7/L12 gene elicits immune response. Vaccine15, 18511857.

Lalmanach, G., Boulange, A., Serveau, C., Lecaille, F., Scharfstein, J., Gauthier, F. and Authie, E. ( 2002). Congopain from Trypanosoma congolense: drug target and vaccine candidate. Biological Chemistry383, 739749.

Landfear, S. M. and Ignatushchenko, M. ( 2001). The flagellum and flagellar pocket of trypanosomatids. Molecular and Biochemical Parasitology115, 117.

Lei, B., Mackie, S., Lukomski, S. and Musser, J. M. ( 2000). Identification and immunogenicity of group A Streptococcus culture supernatant proteins. Infection and Immunity68, 68076818.

Lemesre, J. L., Holzmuller, P., Cavaleyra, M., Goncalves, R. B., Hottin, G. and Papierok, G. ( 2005). Protection against experimental visceral leishmaniasis infection in dogs immunized with purified excreted secreted antigens of Leishmania infantum promastigotes. Vaccine23, 28252840.

Len, A. C., Cordwell, S. J., Harty, D. W. and Jacques, N. A. ( 2003). Cellular and extracellular proteome analysis of Streptococcus mutans grown in a chemostat. Proteomics3, 627646.

Liao, X., Ying, T., Wang, H., Wang, J., Shi, Z., Feng, E., Wei, K., Wang, Y., Zhang, X., Huang, L., Su, G. and Huang, P. ( 2003). A two-dimensional proteome map of Shigella flexneri. Electrophoresis24, 28642882.

Louzir, H., Melby, P. C., Ben Salah, A., Marrakchi, H., Aoun, K., Ben Ismail, R. and Dellagi, K. ( 1998). Immunologic determinants of disease evolution in localized cutaneous leishmaniasis due to Leishmania major. Journal of Infectious Diseases177, 16871695.

Matlashewski, G. ( 2001). Leishmania infection and virulence. Medical Microbiology and Immunology190, 3742.

Mattow, J., Schaible, U. E., Schmidt, F., Hagens, K., Siejak, F., Brestrich, G., Haeselbarth, G., Muller, E. C., Jungblut, P. R. and Kaufmann, S. H. ( 2003). Comparative proteome analysis of culture supernatant proteins from virulent Mycobacterium tuberculosis H37Rv and attenuated M. bovis BCG Copenhagen. Electrophoresis24, 34053420.

Mayer, M. P. and Bukau, B. ( 2005). Hsp70 chaperones: cellular functions and molecular mechanism. Cellular and Molecular Life Sciences62, 670684.

Mendez, S., Belkaid, Y., Seder, R. A. and Sacks, D. ( 2002). Optimization of DNA vaccination against cutaneous leishmaniasis. Vaccine20, 37023708.

Mottram, J. C., Coombs, G. H. and Alexander, J. ( 2004). Cysteine peptidases as virulence factors of Leishmania. Current Opinion in Microbiology7, 375381.

Mottram, J. C., Souza, A. E., Hutchison, J. E., Carter, R., Frame, M. J. and Coombs, G. H. ( 1996). Evidence from disruption of the Imcpb gene array of Leishmania mexicana that cysteine proteinases are virulence factors. Proceedings of the National Academy of Sciences, USA93, 60086013.

Mukhopadhyay, S., Sen, P., Majumder, H. K. and Roy, S. ( 1998). Reduced expression of lipophosphoglycan (LPG) and kinetoplastid membrane protein (KMP)-11 in Leishmania donovani promastigotes in axenic culture. The Journal of Parasitology84, 644647.

Mustafa, A. S. ( 2002). Development of new vaccines and diagnostic reagents against tuberculosis. Molecular Immunology39, 113119.

Nandan, D., Cherkasov, A., Sabouti, R., Yi, T. and Reiner, N. E. ( 2003). Molecular cloning, biochemical and structural analysis of elongation factor-1 alpha from Leishmania donovani: comparison with the mammalian homologue. Biochemical and Biophysical Research Communications302, 646652.

Nandan, D. and Reiner, N. E. ( 2005). Leishmania donovani engages in regulatory interference by targeting macrophage protein tyrosine phosphatase SHP-1. Clinical Immunology114, 266277.

Nandan, D., Yi, T., Lopez, M., Lai, C. and Reiner, N. E. ( 2002). Leishmania EF-1 alpha activates the Src homology 2 domain containing tyrosine phosphatase SHP-1 leading to macrophage deactivation. The Journal of Biological Chemistry277, 5019050197.

Nishisaka, M., Yokoyama, N., Xnan, X., Inoue, N., Nagasawa, H., Fujisaki, K., Mikami, T. and Igarashi, I. ( 2001). Characterisation of the gene encoding a protective antigen from Babesia microti identified it as eta subunit of chaperonin containing T-complex protein 1. International Journal for Parasitology31, 16731679.

Ouaissi, A., Ouaissi, M., Tavares, J. and Cordeiro-Da-Silva, A. ( 2004). Host Cell Phenotypic Variability Induced by Trypanosomatid-Parasite-Released Immunomodulatory Factors: Physiopathological Implications. Journal of Biomedicine and Biotechnology2004, 167174.

Planelles, L., Thomas, M. C., Alonso, C. and Lopez, M. C. ( 2001). DNA immunization with Trypanosoma cruzi HSP70 fused to the KMP11 protein elicits a cytotoxic and humoral immune response against the antigen and leads to protection. Infection and Immunity69, 65586563.

Pockley, A. G., Shepherd, J. and Corton, J. M. ( 1998). Detection of heat shock protein 70 (Hsp70) and anti-Hsp70 antibodies in the serum of normal individuals. Immunological Investigations27, 367377.

Pontes, D. S., Dorella, F. A., Ribeiro, L. A., Miyoshi, A., Le Loir, Y., Gruss, A., Oliveira, S. C., Langella, P. and Azevedo, V. ( 2003). Induction of partial protection in mice after oral administration of Lactococcus lactis producing Brucella abortus L7/L12 antigen. Journal of Drug Targeting11, 489493.

Probst, P., Stromberg, E., Ghalib, H. W., Mozel, M., Badaro, R., Reed, S. G. and Webb, J. R. ( 2001). Identification and characterization of T cell-stimulating antigens from Leishmania by CD4 T cell expression cloning. Journal of Immunology166, 498505.

Pym, A. S., Brodin, P., Majlessi, L., Brosch, R., Demangel, C., Williams, A., Griffiths, K. E., Marchal, G., Leclerc, C. and Cole, S. T. ( 2003). Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nature, Medicine9, 533539.

Rafati, S., Salmanian, A. H., Hashemi, K., Schaff, C., Belli, S. and Fasel, N. ( 2001a). Identification of Leishmania major cysteine proteinases as targets of the immune response in humans. Molecular and Biochemical Parasitology113, 3543.

Rafati, S., Salmanian, A. H., Taheri, T., Vafa, M. and Fasel, N. ( 2001b). A protective cocktail vaccine against murine cutaneous leishmaniasis with DNA encoding cysteine proteinases of Leishmania major. Vaccine19, 33693375.

Ramirez, J. R., Gilchrist, K., Robledo, S., Sepulveda, J. C., Moll, H., Soldati, D. and Berberich, C. ( 2001). Attenuated Toxoplasma gondii ts-4 mutants engineered to express the Leishmania antigen KMP-11 elicit a specific immune response in BALB/c mice. Vaccine20, 455461.

Requena, J. M., Soto, M., Doria, M. D. and Alonso, C. ( 2000). Immune and clinical parameters associated with Leishmania infantum infection in the golden hamster model. Veterinary Immunology and Immunopathology76, 269281.

Rico, A. I., Angel, S. O., Alonso, C. and Requena, J. M. ( 1999). Immunostimulatory properties of the Leishmania infantum heat shock proteins HSP70 and HSP83. Molecular Immunology36, 11311139.

Roberts, S. C., Jiang, Y., Jardim, A., Carter, N. S., Heby, O. and Ullman, B. ( 2001). Genetic analysis of spermidine synthase from Leishmania donovani. Molecular and Biochemical Parasitology115, 217226.

Robinson, P. A. and Ardley, H. C. ( 2004). Ubiquitin-protein ligases–novel therapeutic targets? Current Protein and Peptide Science5, 163176.

Rosa, R., Rodrigues, O. R., Marques, C. and Santos-Gomes, G. M. ( 2005). Leishmania infantum: soluble proteins released by the parasite exert differential effects on host immune response. Experimental Parasitology109, 106114.

Ryazanov, A. G., Rudkin, B. B. and Spirin, A. S. ( 1991). Regulation of protein synthesis at the elongation stage. New insights into the control of gene expression in eukaryotes. FEBS Letters285, 170175.

Sacks, D. L. ( 2001). Abstract Leishmania-sand fly interactions controlling species-specific vector competence. Cellular Microbiology3, 189196.

Sereno, D., Vanhille, L., Vergnes, B., Monte-Allegre, A. and Ouaissi, A. ( 2005). Experimental study of the function of the excreted/secreted Leishmania LmSIR2 protein by heterologous expression in eukaryotic cell line. Kinetoplastid Biology and Disease4, 1.

Shams, H., Klucar, P., Weis, S. E., Lalvani, A., Moonan, P. K., Safi, H., Wizel, B., Ewer, K., Nepom, G. T., Lewinsohn, D. M., Andersen, P. and Barnes, P. F. ( 2004). Characterization of a Mycobacterium tuberculosis peptide that is recognized by human CD4+ and CD8+ T cells in the context of multiple HLA alleles. Journal of Immunology173, 19661977.

Shin, Y. S., Lee, E. G., Shin, G. W., Kim, Y. R., Lee, E. Y., Kim, J. H., Jang, H., Gershwin, L. J., Kim, D. Y., Kim, Y. H., Kim, G. S., Suh, M. D. and Jung, T. S. ( 2004). Identification of antigenic proteins from Neospora caninum recognized by bovine immunoglobulins M, E, A and G using immunoproteomics. Proteomics4, 36003609.

Smith, A. M., Dowd, A. J., Mcgonigle, S., Keegan, P. S., Brennan, G., Trudgett, A. and Dalton, J. P. ( 1993). Purification of a cathepsin L-like proteinase secreted by adult Fasciola hepatica. Molecular and Biochemical Parasitology62, 18.

Spath, G. F. and Beverley, S. M. ( 2001). A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Experimental Parasitology99, 97103.

Symons, F. M., Murray, P. J., Ji, H., Simpson, R J., Osborn, A. H., Cappai, R. and Handman, E. ( 1994). Characterization of a polymorphic family of integral membrane proteins in promastigotes of different Leishmania species. Molecular and Biochemical Parasitology67, 103113.

Tanudji, M., Hevi, S. and Chuck, S. L. ( 2002). Improperly folded green fluorescent protein is secreted via a non-classical pathway. Journal of Cell Science115, 38493857.

Tonui, W. K., Mejia, J. S., Hochberg, L., Mbow, M. L., Ryan, J. R., Chan, A. S., Martin, S. K. and Titus, R. G. ( 2004). Immunization with Leishmania major exogenous antigens protects susceptible BALB/c mice against challenge infection with L. major. Infection and Immunity72, 56545661.

Turano, C., Coppari, S., Altieri, F. and Ferraro, A. ( 2002). Proteins of the PDI family: unpredicted non-ER locations and functions. Journal of Cellular Physiology193, 154163.

Vercauteren, I., Geldhof, P., Peelaers, I., Claerebout, E., Berx, G. and Vercruysse, J. ( 2003). Identification of excretory-secretory products of larval and adult Ostertagia ostertagi by immunoscreening of cDNA libraries. Molecular and Biochemical Parastiology126, 201208.

Voland, P., Weeks, D. L., Vaira, D., Prinz, C. and Sachs, G. ( 2002). Specific identification of three low molecular weight membrane-associated antigens of Helicobacter pylori. Aliment Pharmacology and Therapeutics16, 533544.

Watt, S. A., Wilke, A., Patschkowski, T. and Niehaus, K. ( 2005). Comprehensive analysis of the extracellular proteins from Xanthomonas campestris pv. campestris B100. Proteomics5, 153167.

Wilkinson, B. and Gilbert, H. F. ( 2004). Protein disulfide isomerase. Biochimica et Biophysica Acta1699, 3544.

Yahiaoui, B., Taibi, A. and Ouaissi, A. ( 1996). A Leishmania major protein with extensive homology to silent information regulator 2 of Saccharomyces cerevisiae. Gene169, 115118.

Zadeh-Vakili, A., Taheri, T., Taslimi, Y., Doustdari, F., Salmanian, A. H. and Rafati, S. ( 2004). Immunization with the hybrid protein vaccine, consisting of Leishmania major cysteine proteinases Type I (CPB) and Type II (CPA), partially protects against leishmaniasis. Vaccine22, 19301940.

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