Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-13T13:26:27.928Z Has data issue: false hasContentIssue false

Functional group/guild modelling of inter-specific pathogen interactions: A potential tool for predicting the consequences of co-infection

Published online by Cambridge University Press:  14 May 2008

J. LELLO*
Affiliation:
School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff, CF10 3US
T. HUSSELL
Affiliation:
Kennedy Institute, Imperial College London, ARC Building, Charing Cross Campus, 1 Aspenlea Road, London, W6 8LH
*
Corresponding author: Dr Joanne Lello, School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff, CF10 3US; Tel: 02920 875885; Fax: 02920 874562; E-Mail: lelloj@cardiff.ac.uk.

Summary

Although co-infection is the norm in most human and animal populations, clinicians currently have no practical tool to assist them in choosing the best treatment strategy for such patients. Given the vast range of potential pathogens which may co-infect the host, obtaining such a practical tool may seem an intractable problem. In ecology the joint concepts of functional groups and guilds have been used to conceptually simplify complex ecosystems, in order to understand how their component parts interact and may be manipulated. Here we propose a mechanism by which to apply these concepts to pathogen co-infection systems. Further, we describe how these groups could be incorporated into a mathematical modelling framework which, after validation, could be used as a clinical tool to predict the outcome of any particular combination of pathogens co-infecting a host.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

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

REFERENCES

Abbassi, H., Dambrine, G., Cherel, Y., Coudert, F. and Naciri, M. (2000). Interaction of Marek's disease virus and Cryptosporidium baileyi in experimentally infected chickens. Avian Diseases 44, 776789.CrossRefGoogle ScholarPubMed
Abolhassani, M. and Darabi, H. (2006). Immunosuppressive activity of Leishmania major culture supernatant. Iranian Journal of Public Health 35, 2227.Google Scholar
Abu-Raddad, L. J., Patnaik, P. and Kublin, J. G. (2006). Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa. Science 314, 16031606.CrossRefGoogle ScholarPubMed
Allard, J. B., Poynter, M. E., Marr, K. A., Cohn, L., Rincon, M. and Whittaker, L. A. (2006). Aspergillus fumigatus generates an enhanced th2-biased immune response in mice with defective cystic fibrosis transmembrane conductance regulator. Journal of Immunology 177, 51865194.CrossRefGoogle ScholarPubMed
Azevedo, M. S. P., Yuan, L., Pouly, S., Gonzales, A. M., Jeong, K. I., Nguyen, T. V. and Saif, L. J. (2006). Cytokine responses in gnotobiotic pigs after infection with virulent or attenuated human rotavirus. Journal of Virology 80, 372382.CrossRefGoogle ScholarPubMed
Baumgart, M., Tompkins, F., Leng, J. and Hesse, M. (2006). Naturally occurring CD4(+)Foxp3(+) regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation. Journal of Immunology 176, 53745387.CrossRefGoogle ScholarPubMed
Bayraktar, M. R., Mehmet, N. and Durmaz, R. (2005). Serum cytokine changes in Turkish children infected with Giardia lamblia with and without allergy: Effect of metronidazole treatment. Acta Tropica 95, 116122.CrossRefGoogle ScholarPubMed
Becker, Y. (2006). Respiratory syncytial virus (RSV) evades the human adaptive immune system by skewing the Th1/Th2 cytokine balance toward increased levels of Th2 cytokines and IgE, markers of allergy – a review. Virus Genes 33, 235252.CrossRefGoogle ScholarPubMed
Biber, P. D., Harwell, M. A. and Cropper, W. P. (2004). Modeling the dynamics of three functional groups of macroalgae in tropical seagrass habitats. Ecological Modelling 175, 2554.CrossRefGoogle Scholar
Bilenko, N., Levy, A., Dagan, R., Deckelbaum, R. J., El-on, Y. and Fraser, D. (2004). Does co-infection with Giardia lamblia modulate the clinical characteristics of enteric infections in young children? European Journal of Epidemiology 19, 877883.CrossRefGoogle ScholarPubMed
Blondel, J. (2003). Guilds or functional groups: does it matter? Oikos 100, 223231.CrossRefGoogle Scholar
Brown, M., Mawa, P. A., Joseph, S., Bukusuba, J., Watera, C., Whitworth, J. A. G., Dunne, D. W. and Elliott, A. M. (2005). Treatment of Schistosoma mansoni infection increases helminth-specific type 2 cytokine responses and HIV-1 loads in coinfected Ugandan adults. Journal of Infectious Diseases 191, 16481657.CrossRefGoogle ScholarPubMed
Cardoso, L. S., Oliveira, S. C., Pacifico, L. G. G., Goes, A. M., Oliveira, R. R., Fonseca, C. T., De Carvalho, E. M. and Araujo, M. I. (2006). Schistosoma mansoni antigen-driven interleukin-10 production in infected asthmatic individuals. Memorias do Instituto Oswaldo Cruz 101, 339343.CrossRefGoogle ScholarPubMed
Carlyon, J. A. and Fikrig, E. (2003). Invasion and survival strategies of Anaplasma phagocytophilum. Cellular Microbiology 5, 743754.CrossRefGoogle ScholarPubMed
Catovsky, S. (1998). Functional groups: clarifying our use of the term. Bulletin of the Ecological Society of America 79, 126127.Google Scholar
Christensen, N. O., Nansen, P., Fagbemi, B. O. and Monrad, J. (1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental-infection of mammalian hosts. Zeitschrift fűr Parasitenkunde-Parasitology Research 73, 387410.CrossRefGoogle ScholarPubMed
Cooper, A. M., Dalton, D. K., Stewart, T. A., Griffin, J. P., Russell, D. G. and Orme, I. M. (1993). Disseminated tuberculosis in interferon-gamma gene-disrupted mice. Journal of Experimental Medicine 178, 22432247.CrossRefGoogle ScholarPubMed
Coutinho, H. M., Leenstra, T., Acosta, L. P., Su, L., Jarilla, B., Jiz, M. A., Langdon, G. C., Olveda, R. M., Mcgarvey, S. T., Kurtis, J. D. and Friedman, J. F. (2006). Pro-inflammatory cytokines and C-reactive protein are associated with undernutrition in the context of Schistosoma japonicum infection. American Journal of Tropical Medicine and Hygiene 75, 720726.CrossRefGoogle ScholarPubMed
D'orazio, S. E. F., Troese, M. J. and Starnbach, M. N. (2006). Cytosolic localization of Listeria monocytogenes triggers an early IFN-gamma response by CD8(+) T cells that correlates with innate resistance to infection. Journal of Immunology 177, 71467154.CrossRefGoogle ScholarPubMed
Davic, R. D. (2003). Linking keystone species and functional groups: A new operational defintion of the keystone species concept. Conservation Ecology 7, r11 (online).CrossRefGoogle Scholar
Davis, A. J., Liu, W. C., Perner, J. and Voigt, W. (2004). Reliability characteristics of natural functional group interaction webs. Evolutionary Ecology Research 6, 11451166.Google Scholar
Dawson, H. D., Beshah, E., Nishi, S., Solano-Aguilar, G., Morimoto, M., Zhao, A. P., Madden, K. B., Ledbetter, T. K., Dubey, J. P., Shea-Donohue, T., Lunney, J. K. and Urban, J. F. (2005). Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infection and Immunity 73, 11161128.CrossRefGoogle ScholarPubMed
De Bernardis, F., Lucciarini, R., Boccanera, M., Amantini, C., Arancia, S., Morrone, S., Mosca, M., Cassone, A. and Santoni, G. (2006). Phenotypic and functional characterization of vaginal dendritic cells in a rat model of Candida albicans vaginitis. Infection and Immunity 74, 42824294.CrossRefGoogle Scholar
Deehan, M. R., Goodridge, H. S., Blair, D., Lochnit, G., Dennis, R. D., Geyer, R., Harnett, M. M. and Harnett, W. (2002). Immunomodulatory properties of Ascaris suum glycosphingolipids – phosphorylcholine and non-phosphorylcholine-dependent effects. Parasite Immunology 24, 463469.CrossRefGoogle ScholarPubMed
Deka, S., Vanover, J., Dessus-Babus, S., Whittimore, J., Howett, M. K., Wyrick, P. B. and Schoborg, R. V. (2006). Chlamydia trachomatis enters a viable but non-cultivable (persistent) state within herpes simplex virus type 2 (HSV-2) co-infected host cells. Cellular Microbiology 8, 149162.CrossRefGoogle ScholarPubMed
Dekossodo, S. and Grau, G. E. (1993). Profiles of cytokine production in relation with susceptibility to cerebral malaria. Journal of Immunology 151, 48114820.CrossRefGoogle Scholar
Deschoolmeester, M. L., Manku, H. and Else, K. J. (2006). The innate immune responses of colonic epithelial cells to Trichuris muris are similar in mouse strains that develop a type 1 or type 2 adaptive immune response. Infection and Immunity 74, 62806286.CrossRefGoogle ScholarPubMed
Deshpande, P. and Shastry, P. (2004). Modulation of cytokine profiles by malaria pigment – hemozoin: role of IL-10 in suppression of proliferative repsonses of mitogen stimulated human PBMC. Cytokine 28, 205213.CrossRefGoogle Scholar
Diehl, S. and Rincon, M. (2002). The two faces of IL-6 on Th1/Th2 differentiation. Molecular Immunology 39, 531536.CrossRefGoogle ScholarPubMed
Dumay, O., Tari, P. S., Tomasini, J. A. and Mouillot, D. (2004). Functional groups of lagoon fish species in Languedoc Roussillon, southern France. Journal of Fish Biology 64, 970983.CrossRefGoogle Scholar
Dunne, D. W., Vennervald, B. J., Booth, M., Joseph, S., Fitzsimmons, C. M., Cahen, P., Sturrock, R. F., Ouma, J. H., Mwatha, J. K., Kimani, G., Kariuki, H. C., Kazibwe, F., Tukahebwa, E. and Kabatereine, N. B. (2006). Applied and basic research on the epidemiology, morbidity, and immunology of schistosomiasis in fishing communities on Lake Albert, Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 216223.CrossRefGoogle ScholarPubMed
Egusa, H., Nikawa, H., Makihira, S., Yatani, H. and Hamada, T. (2006). In vitro mechanisms of interleukin-8-mediated responses of human gingival epithelial cells to Candida albicans infection. International Journal of Medical Microbiology 296, 301311.CrossRefGoogle ScholarPubMed
Farouk, S. E., Dolo, A., Bereczky, S., Kouriba, B., Maiga, B., Farnert, A., Perlmann, H., Hayano, M., Montgomery, S. M., Doumbo, O. K. and Troye-Blomberg, M. (2005). Different antibody- and cytokine-mediated responses to Plasmodium falciparum parasite in two sympatric ethnic tribes living in Mali. Microbes and Infection 7, 110117.CrossRefGoogle ScholarPubMed
Feng, C. G., Kaviratne, M., Rothfuchs, A. G., Cheever, A., Hieny, S., Young, H. A., Wynn, T. A. and Sher, A. (2006). NK cell-derived IFN-gamma differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis. Journal of Immunology 177, 70867093.CrossRefGoogle Scholar
Ferrari, T. C. A., Moreira, P. R. R., Sampaio, M. J., Da Cunha, A. S., De Oliveira, J. T., Gazzinelli, G. and Correa-Oliveira, R. (2006). Intrathecal cytokines in spinal cord schistosomiasis. Journal of Neuroimmunology 177, 136141.CrossRefGoogle ScholarPubMed
Foster, T. E. and Brooks, J. R. (2005). Functional groups based on leaf physiology: are they spatially and temporally robust? Oecologia 144, 337352.CrossRefGoogle ScholarPubMed
Foulds, K. E., Rotte, M. J. and Seder, R. A. (2006). IL-10 is required for optimal CD8 T cell memory following Listeria monocytogenes infection. Journal of Immunology 177, 25652574.CrossRefGoogle ScholarPubMed
Fowler, M. I., Yin, K., Humphries, H. E., Heckels, J. E. and Christodoulides, M. (2006). Comparison of the inflammatory responses of human meningeal cells following challenge with Neisseria lactamica and with Neisseria meningitidis. Infection and Immunity 74, 64676478.CrossRefGoogle ScholarPubMed
Fulton, E. A., Parslow, J. S., Smith, A. D. M. and Johnson, C. R. (2004). Biogeochemical marine ecosystem models II: the effect of physiological detail on model performance. Ecological Modelling 173, 371406.CrossRefGoogle Scholar
Furuta, T., Kikuchi, T., Iwakura, Y. and Watanabe, N. (2006). Protective roles of mast cells and mast cell-derived TNF in murine malaria. Journal of Immunology 177, 32943302.CrossRefGoogle ScholarPubMed
Furze, R. C., Hussell, T. and Selkirk, M. E. (2006). Amelioration of influenza-induced pathology in mice by coinfection with Trichinella spiralis. Infection and Immunity 74, 19241932.CrossRefGoogle ScholarPubMed
Gbakima, A. A. (1993). The effect of dietary-protein on Trichinella spiralis infection and inflammatory reactions in the tongue in CD1 mice. Nutrition Research 13, 787800.CrossRefGoogle Scholar
Graham, A. L., Lamb, T. J., Read, A. F. and Allen, J. E. (2005). Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. Journal of Infectious Diseases 191, 410421.CrossRefGoogle ScholarPubMed
Gurish, M. F., Bryce, P. J., Tao, H., Kisselgof, A. B., Thornton, E. M., Miller, H. R., Friend, D. S. and Oettgen, H. C. (2004). IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. Journal of Immunology 172, 11391145.CrossRefGoogle ScholarPubMed
Harms, G. and Feldmeier, H. (2002). Review: HIV infection and tropical parasitic diseases – deleterious interactions in both directions? Tropical Medicine & International Health 7, 479488.CrossRefGoogle ScholarPubMed
Helmby, H. and Grencis, R. K. (2002). IL-18 regulates intestinal mastocytosis and Th2 cytokine production independently of IFN-gamma during Trichinella spiralis infection. Journal of Immunology 169, 25532560.CrossRefGoogle ScholarPubMed
Hood, R. R., Laws, E. A., Armstrong, R. A., Bates, N. R., Brown, C. W., Carlson, C. A., Chai, F., Doney, S. C., Falkowski, P. G., Feely, R. A., Friedrichs, M. A. M., Landry, M. R., Moore, J. K., Nelson, D. M., Richardson, T. L., Salihoglu, B., Schartau, M., Toole, D. A. and Wiggert, J. D. (2006). Pelagic functional group modeling: Progress, challenges and prospects. Deep-Sea Research Part II-Topical Studies in Oceanography 53, 459512.CrossRefGoogle Scholar
Hsu, C. C. (2006). Generalizing self-organizing map for categorical data. Ieee Transactions on Neural Networks 17, 294304.CrossRefGoogle ScholarPubMed
Hughes, C. A. and Shafran, S. D. (2006). Treatment of hepatitis C in HIV-coinfected patients. Annals of Pharmacotherapy 40, 479489.CrossRefGoogle ScholarPubMed
Jiang, B., Snipes-Magaldi, L., Dennehy, P., Keyserling, H., Holman, R. C., Bresee, J., Gentsch, J. and Glass, R. I. (2003). Cytokines as mediators for or effectors against rotavirus disease in children. Clinical and Diagnostic Laboratory Immunology 10, 9951001.Google ScholarPubMed
John, C. C., Opika-Opoka, R., Byarugaba, J., Idro, R. and Boivin, M. J. (2006). Low levels of RANTES are associated with mortality in children with cerebral malaria. Journal of Infectious Diseases 194, 837845.CrossRefGoogle ScholarPubMed
Karosi, T., Jokay, I., Konya, J., Szabo, L. Z., Pytel, J., Jori, J., Szalmas, A. and Sziklai, I. (2006). Detection of osteoprotegerin and TNF-alpha mRNA in ankylotic staples footplates in connection with measles virus positivity. Laryngoscope 116, 14271433.CrossRefGoogle Scholar
Khan, W. I., Vallance, B. A., Blennerhasset, P. A., Deng, Y., Verdu, E. F., Matthaei, K. I. and Collins, S. M. (2001). Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infection and Immunity 69, 838844.CrossRefGoogle ScholarPubMed
King, J. R., Andersen, A. N. and Cutter, A. D. (1998). Ants as bioindicators of habitat disturbance: validation of the functional group model for Australia's humid tropics. Biodiversity and Conservation 7, 16271638.CrossRefGoogle Scholar
Kontorinis, N., Agarwal, K. and Dieterich, D. T. (2005). Treatment of hepatitis C virus in HIV patients: a review. Aids 19, S166S173.CrossRefGoogle ScholarPubMed
Kosonen, J., Rantala, A., Little, C. H., Lintu, P., Harjamaki, P. R., Georgiou, G. M., Cone, R. E. and Savolainen, J. (2006). Increased levels of Candida albicans mannan-specific T-cell-derived antigen binding molecules in patients with invasive candidiasis. Clinical and Vaccine Immunology 13, 467474.CrossRefGoogle ScholarPubMed
Kringel, H., Iburg, T., Dawson, H., Aasted, B. and Roepstorff, A. (2006). A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of a local type 2 response associated with worm burden. International Journal for Parasitology 36, 915924.CrossRefGoogle ScholarPubMed
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. (2004). Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840844.CrossRefGoogle ScholarPubMed
Li, E. Q., Zhou, P. and Singer, S. M. (2006). Neuronal nitric oxide synthase is necessary for elimination of Giardia lamblia infections in mice. Journal of Immunology 176, 516521.CrossRefGoogle ScholarPubMed
Liew, F. Y., Xu, D. M., Brint, E. K. and O'neill, L. A. J. (2005). Negative regulation of Toll-like receptor-mediated immune responses. Nature Reviews Immunology 5, 446458.CrossRefGoogle ScholarPubMed
Liu, Q., Liu, Z. G., Alem, F., Whitmire, J., Urban, J. and Gause, W. (2005). IL-18 induces IL-4 independent IL-13 mediated host resistance to Trichuris muris. FASEB Journal 19, A938A938.Google Scholar
Loeuillet, C., Martinon, F., Perez, C., Munoz, M., Thome, M. and Meylan, P. R. (2006). Mycobacterium tuberculosis subverts innate immunity to evade specific effectors. Journal of Immunology 177, 62456255.CrossRefGoogle ScholarPubMed
McConchie, B. W., Norris, H. H., Bundoc, V. G., Trivedi, S., Boesen, A., Urban, J. F. and Keane-Myers, A. M. (2006). Ascaris suum-derived products suppress mucosal allergic inflammation in an interleukin-10-independent manner via interference with dendritic cell function. Infection and Immunity 74, 66326641.CrossRefGoogle Scholar
Mikhailova, A. A., Belevskaya, R. G., Kalyuzhnaya, M., Fonina, L. A., Liashenko, V. A. and Petrov, R. V. (2006). Myelopeptide-2 recovers interleukin-2 synthesis and interleukin-2 receptor expression in human T lymphocytes depressed by tumor products or measles virus. Journal of Immunotherapy 29, 306312.CrossRefGoogle ScholarPubMed
Milcu, A., Partsch, S., Langel, R. and Scheu, S. (2006). The response of decomposers (earthworms, springtails and microorganisms) to variations in species and functional group diversity of plants. Oikos 112, 513524.CrossRefGoogle Scholar
Morales, P., Reyes, P., Vargas, M., Rios, M., Imarai, M., Cardenas, H., Croxatto, H., Orihuela, P., Vargas, R., Fuhrer, J., Heckels, J. E., Christodoulides, M. and Velasquez, L. (2006). Infection of human Fallopian tube epithelial cells with Neisseria gonorrhoeae protects cells from tumor necrosis factor alpha-induced apoptosis. Infection and Immunity 74, 36433650.CrossRefGoogle ScholarPubMed
Mukherjee, P., Sen, P. C. and Ghose, A. C. (2006). Lymph node cells from BALB/c mice with chronic visceral leishmaniasis exhibiting cellular anergy and apoptosis: Involvement of Ser/Thr phosphatase. Apoptosis 11, 20132029.CrossRefGoogle ScholarPubMed
Mullen, A. B., Lawrence, C. E., Mcfarlane, E., Wei, X. Q. and Carter, K. C. (2006). Endogenous interleukin-18 is involved in immunity to Leishmania donovani but its absence does not adversely influence the therapeutic activity of sodium stibogluconate. Immunology 119, 348354.CrossRefGoogle Scholar
Onah, D. N. and Wakelin, D. (1999). Trypanosome-induced suppression of responses to Trichinella spiralis in vaccinated mice. International Journal for Parasitology 29, 10171026.CrossRefGoogle ScholarPubMed
Ozoren, N., Masumoto, J., Franchi, L., Kanneganti, T. D., Body-Malapel, M., Erturk, I., Jagirdar, R., Zhu, L., Inohara, N., Bertin, J., Coyle, A., Grant, E. P. and Nunez, G. (2006). Distinct roles of TLR2 and the adaptor ASC in IL-1 beta/IL-18 secretion in response to Listeria monocytogenes. Journal of Immunology 176, 43374342.CrossRefGoogle Scholar
Page, K. R., Scott, A. L. and Manabe, Y. C. (2006). The expanding realm of heterologous immunity: friend or foe? Cellular Microbiology 8, 185196.CrossRefGoogle ScholarPubMed
Parekh, S. B., Bubb, W. A., Hunt, N. H. and Rae, C. (2006). Brain metabolic markers reflect susceptibility status in cytokine gene knockout mice with murine cerebral malaria. International Journal for Parasitology 36, 14091418.CrossRefGoogle ScholarPubMed
Park, Y. S., Chon, T. S., Kwak, I. S. and Lek, S. (2004). Hierarchical community classification and assessment of aquatic ecosystems using artificial neural networks. Science of the Total Environment 327, 105122.CrossRefGoogle ScholarPubMed
Parthasarathy, G. and Mansfield, L. S. (2005). Trichuris suis excretory secretory products (ESP) elicit interleukin-6 (IL-6) and IL-10 secretion from intestinal epithelial cells (IPEC-1). Veterinary Parasitology 131, 317324.CrossRefGoogle ScholarPubMed
Paterson, J. C. M., Garside, P., Kennedy, M. W. and Lawrence, C. E. (2002). Modulation of a heterologous immune response by the products of Ascaris suum. Infection and Immunity 70, 60586067.CrossRefGoogle ScholarPubMed
Pedersen, A. B. and Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22, 133139.CrossRefGoogle ScholarPubMed
Pepe, M., Altamura, M., Spinelli, R., Calvello, R., Saccia, M., Cavallo, P., Covelli, V., Jirillo, E. and Brandonisio, O. (2006). Toll-like receptor-positive cells and recognition of pathogens: How human myeloid dendritic cells respond to in vitro infection with Leishmania infantum. Current Pharmaceutical Design 12, 42554262.CrossRefGoogle ScholarPubMed
Perona-Wright, G., Jenkins, S. J. and Macdonald, A. S. (2006). Dendritic cell activation and function in response to Schistosoma mansoni. International Journal for Parasitology 36, 711721.CrossRefGoogle ScholarPubMed
Petchey, O. L. and Gaston, K. J. (2006). Functional diversity: back to basics and looking forward. Ecology Letters 9, 741758.CrossRefGoogle ScholarPubMed
Poorter, L., Bongers, L. and Bongers, F. (2006). Architecture of 54 moist-forest tree species: Traits, trade-offs, and functional groups. Ecology 87, 12891301.CrossRefGoogle ScholarPubMed
Popov, A., Abdullah, Z., Wickenhauser, C., Saric, T., Driesen, J., Hanisch, F. G., Domann, E., Raven, E. L., Dehus, O., Hermann, C., Eggle, D., Debey, S., Chakraborty, T., Kronke, M., Utermohlen, O. and Schultze, J. L. (2006). Indoleamine 2,3-dioxygenase-expressing dendritic cells form suppurative granulomas following Listeria monocytogenes infection. Journal of Clinical Investigation 116, 31603170.CrossRefGoogle ScholarPubMed
Ramharter, M., Kremsner, P. G., Willheim, M., Winkler, H., Graninger, W. and Winkler, S. (2004). Plasmodium falciparum-specific interleukin-2 and tumor necrosis factor-alpha expressing-T cells are associated with resistance to reinfection and severe malaria in healthy African children. European Cytokine Network 15, 189196.Google ScholarPubMed
Reimert, C. A., Fitzsimmons, C. M., Joseph, S., Mwatha, J. K., Jones, F. M., Kimani, G., Hoffmann, K. F., Booth, M., Kabatereine, N. B., Dunne, D. W. and Vennervald, B. J. (2006). Eosinophil activity in Schistosoma mansoni infections in vivo and in vitro in relation to plasma cytokine profile pre- and posttreatment with praziquantel. Clinical and Vaccine Immunology 13, 584593.CrossRefGoogle ScholarPubMed
Riffault, S., Dubuquoy, C., Castagne, N., Baranowski, E., Charley, B. and Eleouet, J. F. (2006). Replication of Bovine respiratory syncytial virus in murine cells depends on type I interferon-receptor functionality. Journal of General Virology 87, 21452148.CrossRefGoogle ScholarPubMed
Roberts, M. T. M. (2005). Current understandings on the immunology of leishmaniasis and recent developments in prevention and treatment. British Medical Bulletin 75–76, 115130.CrossRefGoogle ScholarPubMed
Roberts-Thomson, I. C., Grove, D. I., Stevens, D. P. and Warren, K. S. (1976). Suppression of giardiasis during intestinal phase of trichinosis in mouse. Gut 17, 953958.CrossRefGoogle Scholar
Rockstroh, J. K. (2006). Management of hepatitis C/HIV coinfection. Current Opinion in Infectious Diseases 19, 813.CrossRefGoogle ScholarPubMed
Rousseau, D., Lefichoux, Y., Stien, X., Suffia, I., Ferrua, B. and Kubar, J. (1997). Progression of visceral leishmaniasis due to Leishmania infantum in BALB/c mice is markedly slowed by prior infection with Trichinella spiralis. Infection and Immunity 65, 49784983.CrossRefGoogle ScholarPubMed
Santiago, H. C., Pires, M. F. B., Souza, D. G., Roffe, E., Cortes, D. F., Tafuri, W. L., Teixeira, M. M. and Vieira, L. Q. (2006). Platelet activating factor receptor-deficient mice present delayed interferon-gamma upregulation and high susceptibility to Leishmania amazonensis infection. Microbes and Infection 8, 25692577.CrossRefGoogle ScholarPubMed
Seixas, E. and Ostler, D. (2005). Plasmodium chabaudi chabaudi (AS): Differential cellular responses to infection in resistant and susceptible mice. Experimental Parasitology 110, 394405.CrossRefGoogle ScholarPubMed
Seoh, J. Y., Khan, M., Park, S. H., Park, H. K., Shin, M. H., Ha, E. H., Lee, B. E., Yoo, K., Han, H. S., Oh, S., Wi, J. H., Hong, C. K., Oh, C. H., Kim, Y. A. and Park, J. W. (2003). Serum cytokine profiles in patients with Plasmodium vivax malaria: A comparison between those who presented with and without hyperpyrexia. American Journal of Tropical Medicine and Hygiene 68, 102106.CrossRefGoogle ScholarPubMed
Sharma, S. K., Farah, D., Misra-Bhattacharya, S., Bajpai, P., Agarwal, A. and Mohammad, O. (2006). Escheriosome entrapped soluble blood stage antigens impart protective immunity against a multi-drug resistant isolate of Plasmodium yoelii nigeriensis in BALB/c mice. Vaccine 24, 948956.CrossRefGoogle ScholarPubMed
Shumilla, J. A., Lacaille, V., Hornell, T. M. C., Huang, J., Narasimhan, S., Relman, D. A. and Mellins, E. D. (2004). Bordetella pertussis infection of primary human monocytes alters HLA-DR expression. Infection and Immunity 72, 14501462.CrossRefGoogle ScholarPubMed
Singer, S. M. and Nash, T. E. (2000). T-cell-dependent control of acute Giardia lamblia infections in mice. Infection and Immunity 68, 170175.CrossRefGoogle ScholarPubMed
Sousa-Pereira, S. R., Teixeira, A. L., Silva, L. C. S., Souza, A. L. S., Antunes, C. M., Teixeira, M. M. and Lambertucci, J. R. (2006). Serum and cerebral spinal fluid levels of chemokines and Th2 cytokines in Schistosoma mansoni myeloradiculopathy. Parasite Immunology 28, 473478.CrossRefGoogle ScholarPubMed
Souza, V. M. O., Jacysyn, J. F. and Macedo, M. S. (2004). IL-4 and IL-10 are essential for immunosuppression induced by high molecular weight proteins from Ascaris suum. Cytokine 28, 92100.CrossRefGoogle ScholarPubMed
Stadecker, M. J., Asahi, H., Finger, E., Hernandez, H. J., Rutitzky, L. I. and Sun, J. (2004). The immunobiology of Th1 polarization in high-pathology schistosomiasis. Immunological Reviews 201, 168179.CrossRefGoogle ScholarPubMed
Stebbing, J., Waters, L., Mandalia, S., Bower, M., Nelson, M. and Gazzard, B. (2005). Hepatitis C virus infection in HIV type 1-infected individuals does not accelerate a decrease in the CD4(+) cell count but does increase the likelihood of AIDS-defining events. Clinical Infectious Diseases 41, 906911.CrossRefGoogle Scholar
Stevens, D. A. (2006). Th1/Th2 in aspergillosis. Medical Mycology 44, S229S235.CrossRefGoogle ScholarPubMed
Stewart, M. J., Kulkarni, S. B., Meusel, T. R. and Imani, F. (2006). c-Jun N-terminal kinase negatively regulates dsRNA and RSV induction of tumor necrosis factor-alpha transcription in human epithelial cells. Journal of Interferon and Cytokine Research 26, 521533.CrossRefGoogle ScholarPubMed
Storkey, J. (2006). A functional group approach to the management of UK arable weeds to support biological diversity. Weed Research 46, 513522.CrossRefGoogle Scholar
Sullivan, P. S., Hanson, D. L., Teshale, E. H., Wotring, L. L. and Brooks, J. T. (2006). Effect of hepatitis C infection on progression of HIV disease and early response to initial antiretroviral therapy. Aids 20, 11711179.CrossRefGoogle ScholarPubMed
Taylor, M. D., Betts, C. J. and Else, K. J. (2000). Peripheral cytokine responses to Trichuris muris reflect those occurring locally at the site of infection. Infection and Immunity 68, 18151819.CrossRefGoogle ScholarPubMed
Thom, M. L., Hope, J. C., Mcaulay, M., Villarreal-Ramos, B., Coffey, T. J., Stephens, S., Vordermeier, H. M. and Howard, C. J. (2006). The effect of tuberculin testing on the development of cell-mediated immune responses during mycobacterium bovis infection. Veterinary Immunology and Immunopathology 114, 2536.CrossRefGoogle ScholarPubMed
Tishon, A., Lewicki, H., Andaya, A., Mcgavern, D., Martin, L. and Oldstone, M. B. A. (2006). CD4 T cell control primary measles virus infection of the CNS: Regulation is dependent on combined activity with either CD8 T cells or with B cells: CD4, CD8 or B cells alone are ineffective. Virology 347, 234245.CrossRefGoogle ScholarPubMed
Torres, D., Janot, L., Quesniaux, V. F. J., Grivennikov, S. I., Maillet, I., Sedgwick, J. D., Ryffel, B. and Erard, F. (2005). Membrane tumor necrosis factor confers partial protection to Listeria infection. American Journal of Pathology 167, 16771687.CrossRefGoogle ScholarPubMed
Turner, J. D., Faulkner, H., Kamgno, J., Cormont, F., Van Snick, J., Else, K. J., Grencis, R. K., Behnke, J. M., Boussinesq, M. and Bradley, J. E. (2003). Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. Journal of Infectious Diseases 188, 17681775.CrossRefGoogle Scholar
Vallance, B. A., Matthaei, K. I., Sanovic, S., Young, I. G. and Collins, S. M. (2000). Interleukin-5 deficient mice exhibit impaired host defence against challenge Trichinella spiralis infections. Parasite Immunology 22, 487492.CrossRefGoogle ScholarPubMed
Vancott, J. L., Prada, A. E., Mcneal, M. M., Stone, S. C., Basu, M., Huffer, B., Smiley, K. L., Shao, M. Y., Bean, J. A., Clements, J. D., Choi, A. H. C. and Ward, R. L. (2006). Mice develop effective but delayed protective immune responses when immunized as neonates either intranasally with nonliving VP6/LT(R192G) or orally with live rhesus rotavirus vaccine candidates. Journal of Virology 80, 49494961.CrossRefGoogle ScholarPubMed
von Allmen, N., Christen, S., Forster, U., Gottstein, B., Welle, M. and Muller, N. (2006). Acute trichinellosis increases susceptibility to Giardia lamblia infection in the mouse model. Parasitology 133, 139149.CrossRefGoogle ScholarPubMed
Walzl, G., Tafuro, S., Moss, P., Openshaw, P. J. M. and Hussell, T. (2000). Influenza virus lung infection protects from respiratory syncytial virus-induced immunopathology. Journal of Experimental Medicine 192, 13171326.CrossRefGoogle ScholarPubMed
Wang, H. W., Peters, N. and Schwarze, J. (2006). Plasmacytoid dendritic cells limit viral replication, pulmonary inflammation, and airway hyperresponsiveness in respiratory syncytial virus infection. Journal of Immunology 177, 62636270.CrossRefGoogle ScholarPubMed
Wardle, D. A. and Zackrisson, O. (2005). Effects of species and functional group loss on island ecosystem properties. Nature 435, 806810.CrossRefGoogle ScholarPubMed
Warrender, C., Forrest, S. and Koster, F. (2006). Modeling intercellular interactions in early Mycobacterium infection. Bulletin of Mathematical Biology 68, 22332261.CrossRefGoogle ScholarPubMed
Weller, A. F., Harris, A. J. and Ware, J. A. (2006). Artificial neural networks as potential classification tools for dinoflagellate cyst images: A case using the self-organizing map clustering algorithm. Review of Palaeobotany and Palynology 141, 287302.CrossRefGoogle Scholar
Werling, D., Howard, C. J., Niederer, E., Straub, O. C., Saalmuller, A. and Langhans, W. (1998). Analysis of the phenotype and phagocytic activity of monocytes/macrophages from cattle infected with the bovine leukaemia virus. Veterinary Immunology and Immunopathology 62, 185195.CrossRefGoogle ScholarPubMed
Wieland, C. W., Florquin, S., Pater, J. M., Weijer, S. and Van Der Poll, T. (2006). Interleukin-1 contributes to an effective clearance of Mycobacterium kansasii from the respiratory tract. Microbes and Infection 8, 24092413.CrossRefGoogle Scholar
Xu, J., Yang, Y., Sun, J., Ding, Y., Su, L., Shao, C. and Jiang, B. (2006). Expression of Toll-like receptors and their association with cytokine responses in peripheral blood mononuclear cells of children with acute rotavirus diarrhoea. Clinical and Experimental Immunology 144, 376381.CrossRefGoogle ScholarPubMed
Yanagi, Y., Takeda, M. and Ohno, S. (2006). Measles virus: cellular receptors, tropism and pathogenesis. Journal of General Virology 87, 27672779.CrossRefGoogle ScholarPubMed
Zarantonelli, M. L., Huerre, M., Taha, M. K. and Alonso, J. M. (2006). Differential role of lipooligosaccharide of Neisseria meningitidis in virulence and inflammatory response during respiratory infection in mice. Infection and Immunity 74, 55065512.CrossRefGoogle ScholarPubMed