Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-24T08:16:57.913Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative genomics and proteomics to study tissue-specific response and function in natural Mycobacterium bovis infections

Published online by Cambridge University Press:  13 August 2007

Victoria Naranjo ,
Christian Gortazar ,
Margarita Villar  and
José de la Fuente
Victoria Naranjo
Affiliation:
Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain
Christian Gortazar
Affiliation:
Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain
Margarita Villar
Affiliation:
Instituto de Tecnologías Química y Medioambiental ITQUIMA, University of Castilla La Mancha, Campus Universitario s/n, 13071 Ciudad Real, Spain
José de la Fuente*
Affiliation:
Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain Center for Veterinary Health Sciences, Department of Veterinary Pathobiology, Oklahoma State University, Stillwater, OK 74078, USA
*
*Corresponding author. E-mail: [email protected] or [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Bovine tuberculosis (bTB) is an established zoonotic disease which affects cattle and wildlife worldwide and new strategies are required to control and eradicate the disease. The European wild boar (Sus scrofa) is a major reservoir of bTB in Spain. The objective of this paper was to review tissue-specific response and function of mandibular lymph nodes (MLN) and oropharyngeal tonsils (OT) in European wild boar naturally infected with Mycobacterium bovis. Genomics and proteomics data were used to compare differential gene expression and global protein patterns in OT and MLN of M. bovis-infected and uninfected European wild boar and the results were analyzed considering previous reports of experimental infections in laboratory and domestic animals. The results showed tissue-specific differences in OT and MLN in response to M. bovis infection. Tissue-specific differences in gene expression and protein profiles suggested different functions for OT and MLN during mycobacterial infection and provided information to characterize the pathobiology of M. bovis infection in European wild boar with important implications for the control of bTB in Spain. The characterization of molecular events in tissues that play different roles during mycobacterial infection in naturally infected individuals may be relevant to understand the pathobiology of M. bovis infection and to design effective strategies for the control of bTB in wildlife reservoirs.

Keywords

bovine tuberculosiswild boarmycobacteriaIberian red deervaccine
Type
Review Article
Information
Animal Health Research Reviews , Volume 8 , Issue 1 , June 2007 , pp. 81 - 88
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acevedo-Whitehouse, K, Vicente, J, Gortazar, C, Höfle, U, Fernández de Mera, IG and Amos, W (2005). Genetic resistance to bovine tuberculosis in the Iberian wild boar. Molecular Ecology 14: 3209–3217.CrossRefGoogle ScholarPubMed
Aggeli, C, Pitsavos, C, Brili, S, Hasapis, D, Frogoudaki, A, Stefanadis, C and Toutouzas, P (2000). Relevance of adenosine deaminase and lysozyme measurements in the diagnosis of tuberculous pericarditis. Cardiology 94: 81–85.CrossRefGoogle ScholarPubMed
Ballesteros, C, Pérez de la Lastra, JM and de la Fuente, J (2007). Recent developments in oral bait vaccines for wildlife. Recent Patents on Drug Delivery and Formulation: in press.CrossRefGoogle ScholarPubMed
Blumenthal, A, Lauber, J, Hoffmann, R, Ernst, M, Keller, C, Buer, J, Ehlers, S and Reiling, N (2005). Common and unique gene expression signatures of human macrophages in response to four strains of Mycobacterium avium that differ in their growth and persistence characteristics. Infection and Immunity 73: 3330–3341.CrossRefGoogle ScholarPubMed
Buddle, BM, Wedlock, DN, Denis, M and Skinner, MA (2005). Identification of immune response correlates for protection against bovine tuberculosis. Veterinary Immunology and Immunopathology 108: 45–51.CrossRefGoogle ScholarPubMed
Buddle, BM, Wedlock, DN and Denis, M (2006). Progress in the development of tuberculosis vaccines for cattle and wildlife. Veterinary Microbiology 112: 191–200.CrossRefGoogle ScholarPubMed
Chaussabel, D, Semnani, RT, McDowell, MA, Sacks, D, Sher, A and Nutman, TB (2003). Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood 102: 672–681.CrossRefGoogle ScholarPubMed
Clemens, DL and Horwitz, MA (1995). Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. Journal of Experimental Medicine 181: 257–270.CrossRefGoogle ScholarPubMed
Cross, ML, Buddle, BM and Aldwell, FE (2007). The potential of oral vaccines for disease control in wildlife species. Veterinary Journal: in press (doi: 10.1016/j.tvjl.2006.10.005).CrossRefGoogle ScholarPubMed
Danelishvili, L, McGarvey, J, Li, Y-J and Bermudez, LE (2003). Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cellular Microbiology 5: 649–660.CrossRefGoogle ScholarPubMed
Fernández de Mera, IG, Pérez de la Lastra, JM, Ayoubi, P, Naranjo, V, Kocan, KM, Gortazar, C and de la Fuente, J (2007). Differential expression of inflammatory and immune response genes in mesenteric lymph nodes of Iberian red deer (Cervus elaphus hispanicus) naturally infected with Mycobacterium bovis. Developmental and Comparative Immunology, in press.Google Scholar
Gortazar, C, Vicente, J and Gavier-Widén, D (2003). Pathology of bovine tuberculosis in the European wild boar (Sus scrofa). Veterinary Record 152: 779–790.CrossRefGoogle ScholarPubMed
Gortazar, C, Vicente, J, Samper, S, Garrido, J, Fernández-De-Mera, IG, Gavín, P, Juste, RA, Martín, C, Acevedo, P, De La Puente, M and Höfle, U (2005). Molecular characterization of Mycobacterium tuberculosis complex isolates from wild ungulates in South-Central Spain. Veterinary Research 36: 43–52.CrossRefGoogle ScholarPubMed
Keller, C, Lauber, J, Blumenthal, A, Buer, J and Ehlers, S (2004). Resistance and susceptibility to tuberculosis analyzed at the transcriptome level: lessons from mouse macrophages. Tuberculosis 84: 144–158.CrossRefGoogle Scholar
Keller, C, Hoffmann, R, Lang, R, Brandau, S, Hermann, C and Ehlers, S (2006). Genetically determined susceptibility to tuberculosis in mice causally involves accelerated and enhanced recruitment of granulocytes. Infection and Immunity 74: 4295–4309.CrossRefGoogle ScholarPubMed
Kim, DK, Park, GM, Hwang, YI, Kim, HJ, Han, SK, Shim, Y-S and Yim, J-J (2006). Microarray analysis of gene expression associated with extrapulmonary dissemination of tuberculosis. Respirology 11: 557–565.CrossRefGoogle ScholarPubMed
Koguchi, Y, Kawakami, K, Uezu, K, Fukushima, K, Kon, S, Maeda, M, Nakamoto, A, Owan, I, Kuba, M, Kudeken, N, Azuma, M, Yara, S, Shinzato, T, Higa, F, Tateyama, M, Kadota, J, Mukae, H, Kohno, S, Uede, T and Saito, A (2003). High plasma osteopontin level and its relationship with interleukin-12-mediated type 1 T helper cell response in tuberculosis. American Journal of Respiratory Critical Care Medicine 167: 1355–1359.CrossRefGoogle ScholarPubMed
Koul, A, Herget, T, Klebl, B and Ullrich, A (2004). Interplay between mycobacteria and host signalling pathways. Nature Review Microbiology 2: 189–202.CrossRefGoogle ScholarPubMed
Lyashchenko, KP, Greenwald, R, Esfandiari, J, Olsen, JH, Ball, R, Dumonceaux, G, Dunker, F, Buckley, C, Richard, M, Murray, S, Payeur, JB, Andersen, P, Pollock, JM, Mikota, S, Miller, M, Sofranko, D and Waters, WR (2006). Tuberculosis in elephants: antibody responses to defined antigens of Mycobacterium tuberculosis, potential for early diagnosis, and monitoring of treatment. Clinical and Vaccine Immunology 13: 722–732.CrossRefGoogle ScholarPubMed
Martín-Hernando, MP, Höfle, U, Vicente, J, Ruiz-Fons, F, Vidal, D, Barral, M, Garrido, JA, de la Fuente, J and Gortazar, C (2007). Lesions associated with Mycobacterium tuberculosis complex infection in the European wild boar. Tuberculosis: in press (doi: 10.1016/j.tube.2007.02.003).CrossRefGoogle ScholarPubMed
Meade, KG, Gormley, E, Park, SDE, Fitzsimons, T, Rosa, GJM, Costello, E, Keane, J, Coussens, PM and MacHugh, DE (2006). Gene expression profiling of peripheral blood mononuclear cells (PBMC) from Mycobacterium bovis infected cattle after in vitro antigenic stimulation with purified protein derivative of tuberculin (PPD). Veterinary Immunology and Immunopathology 113: 73–89.CrossRefGoogle ScholarPubMed
Meijer, AH, Verbeek, FJ, Salas-Vidal, E, Corredor-Adamez, M, Bussmana, J, van der Sarc, AM, Ottod, GW, Geislerd, R and Spaink, HP (2005). Transcriptome profiling of adult zebrafish at the late stage of chronic tuberculosis due to Mycobacterium marinum infection. Molecular Immunology 42: 1185–1203.CrossRefGoogle ScholarPubMed
Mishra, OP, Yusuf, S, Ali, Z and Nath, G (2000). Lysozyme levels for the diagnosis of tuberculous effusions in children. Journal of Tropical Pediatrics 46: 296–300.CrossRefGoogle ScholarPubMed
Naranjo, V, Höfle, U, Vicente, J, Martín, MP, Ruiz-Fons, F, Gortazar, C, Kocan, KM and de la Fuente, J (2006a). Genes differentially expressed in oropharyngeal tonsils and mandibular lymph nodes of tuberculous and non-tuberculous European wild boars naturally exposed to Mycobacterium bovis. FEMS Immunology and Medical Microbiology 46: 298–312.CrossRefGoogle ScholarPubMed
Naranjo, V, Ayoubi, P, Vicente, J, Ruiz-Fons, F, Gortazar, C, Kocan, KM and de la Fuente, J (2006b). Characterization of selected genes upregulated in non-tuberculous European wild boar as possible correlates of resistance to Mycobacterium bovis infection. Veterinary Microbiology 116: 224–231.CrossRefGoogle ScholarPubMed
Naranjo, V, Villar, M, Martín-Hernando, MP, Vidal, D, Höfle, U, Gortazar, C, Kocan, KM, Vázquez, J and de la Fuente, J (2007). Proteomic and transcriptomic analyses of differential stress/inflammatory responses in mandibular lymph nodes and oropharyngeal tonsils of European wild boars naturally infected with Mycobacterium bovis. Proteomics 7: 220–231.CrossRefGoogle ScholarPubMed
Nau, GJ, Liaw, L, Chupp, GL, Berman, JS, Hogan, BL and Young, RA (1999). Attenuated host resistance against Mycobacterium bovis BCG infection in mice lacking osteopontin. Infection and Immunity 67: 4223–4230.CrossRefGoogle ScholarPubMed
Orlova, MO, Majorov, KB, Lyadova, IV, Eruslanov, EB, M'lan, CE, Greenwood, CM, Schurr, E and Apt, AS (2006). Constitutive differences in gene expression profiles parallel genetic patterns of susceptibility to tuberculosis in mice. Infection and Immunity 74: 3668–3672.CrossRefGoogle ScholarPubMed
Ragno, S, Romano, M, Howell, S, Pappin, DJ, Jenner, PJ and Colston, MJ (2001). Changes in gene expression in macrophages infected with Mycobacterium tuberculosis: a combined transcriptomic and proteomic approach. Immunology 104: 99–108.CrossRefGoogle ScholarPubMed
Selvaraj, P, Chandra, G, Jawahar, MS, Rani, MV, Rajeshwari, DN and Narayanan, PR (2004). Regulatory role of vitamin D receptor gene variants of Bsm I, Apa I, Taq I, and Fok I polymorphisms on macrophage phagocytosis and lymphoproliferative response to Mycobacterium tuberculosis antigen in pulmonary tuberculosis. Journal of Clinical Immunology 24: 523–532.CrossRefGoogle Scholar
Shalekoff, S, Pendle, S, Johnson, D, Martin, DJ and Tiemessen, CT (2001). Distribution of the human immunodeficiency virus coreceptors CXCR4 and CCR5 on leukocytes of persons with human immunodeficiency virus type 1 infection and pulmonary tuberculosis: implications for pathogenesis. Journal of Clinical Immunology 21: 390–401.CrossRefGoogle ScholarPubMed
Thacker, TC, Palmer, MV and Waters, WR (2006). Correlation of cytokine gene expression with pathology in white-tailed deer (Odocoileus virginianus) infected with Mycobacterium bovis. Clinical and Vaccine Immunology 13: 640–647.CrossRefGoogle ScholarPubMed
Velasco-Velazquez, MA, Barrera, D, Gonzalez-Arenas, A, Rosales, C and Agramonte-Hevia, J (2003). Macrophage–Mycobacterium tuberculosis interactions: role of complement receptor 3. Microbial Pathogenesis 35: 125–131.CrossRefGoogle ScholarPubMed
Vicente, J, Höfle, U, Garrido, JM, Fernandez-de-Mera, IG, Juste, R, Barral, M and Gortazar, C (2006). Wild boar and red deer display high prevalences of tuberculosis-like lesions in Spain. Veterinary Research 37: 107–119.CrossRefGoogle Scholar
Vidal, D, Naranjo, V, Mateo, R, Gortazar, C and de la Fuente, J (2006). Analysis of serum biochemical parameters in relation to Mycobacterium bovis infection of European wild boar (Sus scrofa) in Spain. European Journal of Wildlife Research 52: 301–304.CrossRefGoogle Scholar
Wang, JP, Rought, SE, Corbeil, J and Guiney, DG (2003). Gene expression profiling detects patterns of human macrophage responses following Mycobacterium tuberculosis infection. FEMS Immunology and Medical Microbiology 39: 163–172.CrossRefGoogle ScholarPubMed
Waters, WR, Palmer, MV, Thacker, TC, Bannantine, JP, Vordermeier, HM, Hewinson, RG, Greenwald, R, Esfandiari, J, McNair, J, Pollock, JM, Andersen, P and Lyashchenko, KP (2006). Early antibody responses to experimental Mycobacterium bovis infection of cattle. Clinical and Vaccine Immunology 13: 648–654.CrossRefGoogle ScholarPubMed
Wedlock, DN, Kawakami, RP, Koach, J, Buddle, BM and Collins, DM (2006). Differences of gene expression in bovine alveolar macrophages infected with virulent and attenuated isogenic strains of Mycobacterium bovis. International Immunopharmacology 6: 957–961.CrossRefGoogle ScholarPubMed
Weiss, DJ, Evanson, OA, Deng, M and Abrahamsen, MS (2004). Sequential patterns of gene expression by bovine monocyte-derived macrophages associated with ingestion of mycobacterial organisms. Microbial Pathogenesis 37: 215–224.CrossRefGoogle ScholarPubMed