Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T08:48:12.415Z Has data issue: false hasContentIssue false

The role of chemokines and their receptors during protist parasite infections

Published online by Cambridge University Press:  06 October 2016

FIONA M. MENZIES*
Affiliation:
Infection and Microbiology Group, Institute of Biomedical and Environmental Health Research, School of Science and Sport, University of the West of Scotland, Paisley PA1 2BE, UK
DAVID MACPHAIL
Affiliation:
Infection and Microbiology Group, Institute of Biomedical and Environmental Health Research, School of Science and Sport, University of the West of Scotland, Paisley PA1 2BE, UK
FIONA L. HENRIQUEZ
Affiliation:
Infection and Microbiology Group, Institute of Biomedical and Environmental Health Research, School of Science and Sport, University of the West of Scotland, Paisley PA1 2BE, UK
*
*Corresponding author: Infection and Microbiology Group, Institute of Biomedical and Environmental Health Research, School of Science and Sport, University of the West of Scotland, Paisley PA1 2BE, UK. E-mail: [email protected]

Summary

Protists are a diverse collection of eukaryotic organisms that account for a significant global infection burden. Often, the immune responses mounted against these parasites cause excessive inflammation and therefore pathology in the host. Elucidating the mechanisms of both protective and harmful immune responses is complex, and often relies of the use of animal models. In any immune response, leucocyte trafficking to the site of infection, or inflammation, is paramount, and this involves the production of chemokines, small chemotactic cytokines of approximately 8–10 kDa in size, which bind to specific chemokine receptors to induce leucocyte movement. Herein, the scientific literature investigating the role of chemokines in the propagation of immune responses against key protist infections will be reviewed, focussing on Plasmodium species, Toxoplasma gondii, Leishmania species and Cryptosporidium species. Interestingly, many studies find that chemokines can in fact, promote parasite survival in the host, by drawing in leucocytes for spread and further replication. Recent developments in drug targeting against chemokine receptors highlights the need for further understanding of the role played by these proteins and their receptors in many different diseases.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2016 

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

Alexander, J., Satoskar, A. R. and Russell, D. G. (1999). Leishmania species: models of intracellular parasitism. Journal of Cell Science 112, 29933002.Google Scholar
Aliberti, J., Valenzuela, J. G., Carruthers, V. B., Hieny, S., Andersen, J., Charest, H., Reis e Sousa, C., Fairlamb, A., Ribeiro, J. M. and Sher, A. (2003). Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nature Immunology 4, 485490.CrossRefGoogle ScholarPubMed
Armah, H. B., Wilson, N. O., Sarfo, B. Y., Powell, M. D., Bond, V. C., Anderson, W., Adjei, A. A., Gyasi, R. K., Tettey, Y., Wiredu, E. K., Tongren, J. E., Udhayakumar, V. and Stiles, J. K. (2007). Cerebrospinal fluid and serum biomarkers of cerebral malaria mortality in Ghanaian children. Malaria Journal 6, 147.Google Scholar
Artavanis-Tsakonas, K. and Riley, E. M. (2002). Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. Journal of Immunology 169, 29562963.Google Scholar
Auray, G., Lacroix-Lamandé, S., Mancassola, R., Dimier-Poisson, I. and Laurent, F. (2007). Involvement of intestinal epithelial cells in dendritic cell recruitment during C. parvum infection. Microbes Infect 9, 574582.Google Scholar
Bachelerie, F., Ben-Baruch, A., Burkhardt, A. M., Combadiere, C., Farber, J. M., Graham, G. J., Horuk, R., Sparre-Ulrich, A. H., Locati, M., Luster, A. D., Mantovani, A., Matsushima, K., Murphy, P. M., Nibbs, R., Nomiyama, H., Power, C. A., Proudfoot, A. E., Rosenkilde, M. M., Rot, A., Sozzani, S., Thelen, M., Yoshie, O. and Zlotnik, A. (2014). International Union of Pharmacology. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacological Reviews 66, 179.Google Scholar
Badolato, R., Sacks, D. L., Savoia, D. and Musso, T. (1996). Leishmania major: infection of human monocytes induces expression of IL-8 and MCAF. Experimental Parasitology 82, 2126.CrossRefGoogle ScholarPubMed
Barragan, A. and Sibley, L. D. (2002). Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. Journal of Experimental Medicine 195, 16251633.CrossRefGoogle ScholarPubMed
Bates, P. A. (2007). Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. International Journal for Parasitology 37, 10971106.Google Scholar
Belnoue, E., Costa, F. T., Vigario, A. M., Voza, T., Gonnet, F., Landau, I., Van Rooijen, N., Mack, M., Kuziel, W. A. and Renia, L. (2003 a). Chemokine receptor CCR2 is not essential for the development of experimental cerebral malaria. Infection and Immunity 71, 36483651.CrossRefGoogle Scholar
Belnoue, E., Kayibanda, M., Deschemin, J. C., Viguier, M., Mack, M., Kuziel, W. A. and Renia, L. (2003 b). CCR5 deficiency decreases susceptibility to experimental cerebral malaria. Blood 101, 42534259.Google Scholar
Benevides, L., Milanezi, C. M., Yamauchi, L. M., Benjamim, C. F., Silva, J. S. and Silva, N. M. (2008). CCR2 receptor is essential to activate microbicidal mechanisms to control Toxoplasma gondii infection in the central nervous system. American Journal of Pathology 173, 741751.Google Scholar
Bliss, S. K., Marshall, A. J., Zhang, Y. and Denkers, E. Y. (1999). Human polymorphonuclear leukocytes produce IL-12, TNF-alpha, and the chemokines macrophage-inflammatory protein-1 alpha and -1 beta in response to Toxoplasma gondii antigens. Journal of Immunology 162, 73697375.Google Scholar
Borad, A. and Ward, H. (2010). Human immune responses in cryptosporidiosis. Future Microbiology 5, 507519.Google Scholar
Braun, L., Brenier-Pinchart, M.-P., Yogavel, M., Curt-Varesano, A., Curt-Bertini, R.-L., Hussain, T., Kieffer-Jaquinod, S., Coute, Y., Pelloux, H., Tardieux, I., Sharma, A., Belrhali, H., Bougdour, A. and Hakimi, M.-A. (2013). A Toxoplasma dense granule protein, GRA24, modulates the early immune response to infection by promoting a direct and sustained host p38 MAPK activation. Journal of Experimental Medicine 210, 20712086.CrossRefGoogle ScholarPubMed
Brenier-Pinchart, M.-P., Villena, I., Mercier, C., Durand, F., Simon, J., Cesbron-Delauw, M.-F. and Pelloux, H. (2006). The Toxoplasma surface protein SAG1 triggers efficient in vitro secretion of chemokine ligand 2 (CCL2) from human fibroblasts. Microbes and Infection 8, 254261.CrossRefGoogle ScholarPubMed
Campanella, G. S., Tager, A. M., El Khoury, J. K., Thomas, S. Y., Abrazinski, T. A., Manice, L. A., Colvin, R. A. and Luster, A. D. (2008). Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria. Proceedings of the National Academy of Sciences of the United States of America 105, 48144819.Google Scholar
Campbell, L. D., Stewart, J. N. and Mead, J. R. (2002). Susceptibility to Cryptosporidium parvum infections in cytokine- and chemokine-receptor knockout mice. Journal of Parasitology 88, 10141016.CrossRefGoogle ScholarPubMed
Carvalho, L. P., Petritus, P. M., Trochtenberg, A. L., Zaph, C., Hill, D. A., Artis, D. and Scott, P. (2012). Lymph node hypertrophy following Leishmania major infection is dependent on TLR9. Journal of Immunology 188, 13941401.CrossRefGoogle ScholarPubMed
Castellani, M. L., Bhattacharya, K., Tagen, M., Kempuraj, D., Perrella, A., De Lutiis, M., Boucher, W., Conti, P., Theoharides, T. C., Cerulli, G., Salini, V. and Neri, G. (2007). Anti-chemokine therapy for inflammatory diseases. International Journal of Immunopathology and Pharmacology 20, 447453.CrossRefGoogle ScholarPubMed
Cohen, S. B., Maurer, K. J., Egan, C. E., Oghumu, S., Satoskar, A. R. and Denkers, E. Y. (2013). CXCR3-dependent CD4(+) T cells are required to activate inflammatory monocytes for defense against intestinal infection. PLoS Pathogens 9, e1003706.Google Scholar
Combadiere, C., Ahuja, S. K., Tiffany, H. L. and Murphy, P. M. (1996). Cloning and functional expression of CC CKR5, a human monocyte CC chemokine receptor selective for MIP-1(alpha), MIP-1(beta), and RANTES. Journal of Leukocyte Biology 60, 147152.CrossRefGoogle Scholar
Comerford, I. and McColl, S. R. (2011). Mini-review series: focus on chemokines. Immunology and Cell Biology 89, 183184.CrossRefGoogle ScholarPubMed
Coombes, J. L. and Hunter, C. A. (2015). Immunity to Toxoplasma gondii–into the 21st century. Parasite Immunology 37, 105107.Google Scholar
Coombes, J. L., Charsar, B. A., Han, S. J., Halkias, J., Chan, S. W., Koshy, A. A., Striepen, B., and Robey, E. A. (2013). Motile invaded neutrophils in the small intestine of Toxoplasma gondii-infected mice reveal a potential mechanism for parasite spread. Proceedings of the National Academy of Sciences of the United States of America 110, E1913E1922.Google ScholarPubMed
Cotterell, S. E., Engwerda, C. R. and Kaye, P. M. (1999). Leishmania donovani infection initiates T cell-independent chemokine responses, which are subsequently amplified in a T cell-dependent manner. European Journal of Immunology 29, 203214.Google Scholar
Da Gama, L. M., Ribeiro-Gomes, F. L., Guimaraes, U. Jr. and Arnholdt, A. C. (2004). Reduction in adhesiveness to extracellular matrix components, modulation of adhesion molecules and in vivo migration of murine macrophages infected with Toxoplasma gondii . Microbes and Infection 6, 12871296.Google Scholar
Del Rio, L., Bennouna, S., Salinas, J. and Denkers, E. Y. (2001). CXCR2 deficiency confers impaired neutrophil recruitment and increased susceptibility during Toxoplasma gondii infection. Journal of Immunology 167, 65036509.Google Scholar
Denney, C. F., Eckmann, L. and Reed, S. L. (1999). Chemokine secretion of human cells in response to Toxoplasma gondii infection. Infection and Immunity 67, 15471552.Google Scholar
de Sablet, T., Potiron, L., Marquis, M., Bussière, F. I., Lacroix-Lamandé, S. and Laurent, F. (2016). Cryptosporidium parvum increases intestinal permeability through interaction with epithelial cells and IL-1β and TNFα released by inflammatory monocytes. Cellular Microbiology. doi:10.1111/cmi.12632.CrossRefGoogle ScholarPubMed
Díaz, N. L., Zerpa, O. and Tapia, F. J. (2013). Chemokines and chemokine receptors expression in the lesions of patients with American cutaneous leishmaniasis. Memórias do Instituto Oswaldo Cruz 108, 446452.Google Scholar
Dostálová, A. and Volf, P. (2012). Leishmania development in sand flies: parasite–vector interactions overview. Parasites and Vectors 5, 112.Google Scholar
Dragic, T., Litwin, V., Allaway, G. P., Martin, S. R., Huang, Y., Nagashima, K. A., Cayanan, C., Maddon, P. J., Koup, R. A., Moore, J. P. and Paxton, W. A. (1996). HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381, 667673.CrossRefGoogle ScholarPubMed
Dubey, J. P. (1996). Toxoplasma Gondii . In Medical Microbiology, 4th Edn (ed. S., Baron), University of Texas Medical Branch, Galveston, TX. Chapter 84. Available from: http://www.ncbi.nlm.nih.gov/books/NBK7752/.Google Scholar
Dubey, J. P. (2009). History of the discovery of the life cycle of Toxoplasma gondii . International Journal for Parasitology 39, 877882.Google Scholar
Dubey, J. P., Lindsay, D. S. and Speer, C. A. (1998). Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clinical Microbiology Reviews 11, 267299.Google Scholar
Dunay, I. R., Damatta, R. A., Fux, B., Presti, R., Greco, S., Colonna, M. and Sibley, L. D. (2008). Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii . Immunity 29, 306317.Google Scholar
Dunay, I. R., Fuchs, A. and Sibley, L. D. (2010). Inflammatory monocytes but not neutrophils are necessary to control infection with Toxoplasma gondii in Mice. Infection and Immunity 78, 15641570.Google Scholar
Egan, C. E., Craven, M. D., Leng, J., Mack, M., Simpson, K. W. and Denkers, E. Y. (2009). CCR2-dependent intraepithelial lymphocytes mediate inflammatory gut pathology during Toxoplasma gondii infection. Mucosal Immunology 2, 527535.Google Scholar
Elsheikha, H. M. and Khan, N. A. (2010). Protozoa traversal of the blood–brain barrier to invade the central nervous system. FEMS Microbiology Reviews 34, 532553.CrossRefGoogle ScholarPubMed
Esche, C., Stellato, C. and Beck, L. A. (2005). Chemokines: key players in innate and adaptive immunity. The Journal of Investigative Dermatology 125, 615628.Google Scholar
Franklin, B. S., Parroche, P., Ataide, M. A., Lauw, F., Ropert, C., de Oliveira, R. B., Pereira, D., Tada, M. S., Nogueira, P., da Silva, L. H., Bjorkbacka, H., Golenbock, D. T. and Gazzinelli, R. T. (2009). Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proceedings of the National Academy of Sciences of the United States of America 106, 57895794.Google Scholar
Ghalib, H. W., Whittle, J. A., Kubin, M., Hashim, F. A., el-Hassan, A. M., Grabstein, K. H., Trinchieri, G. and Reed, S. G. (1995). IL-12 enhances Th1-type responses in human Leishmania donovani infections. Journal of Immunology 154, 46234629.Google Scholar
Gilbert, R., Tan, H. K., Cliffe, S., Guy, E. and Stanford, M. (2006). Symptomatic toxoplasma infection due to congenital and postnatally acquired infection. Archives of Disease in Childhood 91, 495498.Google Scholar
Gopal, R., Birdsell, D. and Monroy, F. P. (2011). Regulation of chemokine responses in intestinal epithelial cells by stress and Toxoplasma gondii infection. Parasite Immunology 33, 1224.CrossRefGoogle ScholarPubMed
Graves, D. T. and Jiang, Y. (1995). Chemokines, a family of chemotactic cytokines. Critical Reviews in Oral Biology & Medicine 6, 109118.CrossRefGoogle ScholarPubMed
Guesdon, W., Auray, G., Pezier, T., Bussiere, F. I., Drouet, F., Le Vern, Y., Marquis, M., Potiron, L., Rabot, S., Bruneau, A., Werts, C., Laurent, F. and Lacroix-Lamande, S. (2015). CCL20 displays antimicrobial activity against Cryptosporidium parvum, but its expression is reduced during infection in the intestine of neonatal mice. Journal of Infectious Diseases 212, 13321340.Google Scholar
Hoffmann, F., Muller, W., Schutz, D., Penfold, M. E., Wong, Y. H., Schulz, S. and Stumm, R. (2012). Rapid uptake and degradation of CXCL12 depend on CXCR7 carboxyl-terminal serine/threonine residues. Journal of Biological Chemistry 287, 2836228377.Google Scholar
Hora, R., Kapoor, P., Thind, K. K. and Mishra, P. C. (2016). Cerebral malaria–clinical manifestations and pathogenesis. Metabolic Brain Disease 31, 225237.Google Scholar
Ibrahim, H. M., Bannai, H., Xuan, X. and Nishikawa, Y. (2009). Toxoplasma gondii cyclophilin 18-mediated production of nitric oxide induces Bradyzoite conversion in a CCR5-dependent manner. Infection and Immunity 77, 36863695.Google Scholar
Ibrahim, H. M., Xuan, X. and Nishikawa, Y. (2010). Toxoplasma gondii cyclophilin 18 regulates the proliferation and migration of murine macrophages and spleen cells. Clinical and Vaccine Immunology 17, 13221329.Google Scholar
Ibrahim, H. M., Nishimura, M., Tanaka, S., Awadin, W., Furuoka, H., Xuan, X. and Nishikawa, Y. (2014). Overproduction of Toxoplasma gondii cyclophilin-18 regulates host cell migration and enhances parasite dissemination in a CCR5-independent manner. BMC Microbiology 14, 76.Google Scholar
Jain, V., Armah, H. B., Tongren, J. E., Ned, R. M., Wilson, N. O., Crawford, S., Joel, P. K., Singh, M. P., Nagpal, A. C., Dash, A. P., Udhayakumar, V., Singh, N. and Stiles, J. K. (2008). Plasma IP-10, apoptotic and angiogenic factors associated with fatal cerebral malaria in India. Malaria Journal 7, 83.Google Scholar
Jia, T., Serbina, N. V., Brandl, K., Zhong, M. X., Leiner, I. M., Charo, I. F. and Pamer, E. G. (2008). Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. Journal of Immunology 180, 68466853.Google Scholar
Jiang, P. J., Zhao, A. M., Bao, S. M., Xiao, S. J. and Xiong, M. (2009). Expression of chemokine receptors CCR3, CCR5 and CXCR3 on CD4(+) T cells in CBA/JxDBA/2 mouse model, selectively induced by IL-4 and IL-10, regulates the embryo resorption rate. Chinese Medical Journal (Engl) 122, 19171921.Google Scholar
Jones, J. L. and Dubey, J. P. (2010). Waterborne toxoplasmosis–recent developments. Experimental Parasitology 124, 1025.Google Scholar
Jones, J. L., Kruszon-Moran, D., Wilson, M., McQuillan, G., Navin, T. and McAuley, J. B. (2001). Toxoplasma gondii infection in the United States: seroprevalence and risk factors. American Journal of Epidemiology 154, 357365.Google Scholar
Kantele, A. and Jokiranta, T. S. (2011). Review of cases with the emerging fifth human malaria parasite, Plasmodium knowlesi . Clinical Infectious Diseases 52, 13561362.CrossRefGoogle ScholarPubMed
Kaushansky, A. and Kappe, S. H. (2015). Selection and refinement: the malaria parasite's infection and exploitation of host hepatocytes. Current Opinion in Microbiology 26, 7178.Google Scholar
Kawai, T., Seki, M., Hiromatsu, K., Eastcott, J. W., Watts, G. F., Sugai, M., Smith, D. J., Porcelli, S. A. and Taubman, M. A. (1999). Selective diapedesis of Th1 cells induced by endothelial cell RANTES. Journal of Immunology 163, 32693278.Google Scholar
Kemp, M., Hey, A. S., Kurtzhals, J. A., Christensen, C. B., Gaafar, A., Mustafa, M. D., Kordofani, A. A., Ismail, A., Kharazmi, A. and Theander, T. G. (1994). Dichotomy of the human T cell response to Leishmania antigens. I. Th1-like response to Leishmania major promastigote antigens in individuals recovered from cutaneous leishmaniasis. Clinical and Experimental Immunology 96, 410415.Google Scholar
Khan, I. A., Murphy, P. M., Casciotti, L., Schwartzman, J. D., Collins, J., Gao, J. L. and Yeaman, G. R. (2001). Mice lacking the chemokine receptor CCR1 show increased susceptibility to Toxoplasma gondii infection. Journal of Immunology 166, 19301937.Google Scholar
Khan, I. A., Thomas, S. Y., Moretto, M. M., Lee, F. S., Islam, S. A., Combe, C., Schwartzman, J. D. and Luster, A. D. (2006). CCR5 is essential for NK cell trafficking and host survival following Toxoplasma gondii infection. PLoS Pathogens 2, e49.Google Scholar
Korich, D. G., Mead, J. R., Madore, M. S., Sinclair, N. A. and Sterling, C. R. (1990). Effects of ozone, chlorine dioxide, chlorine, and monochloramine on Cryptosporidium parvum oocyst viability. Applied and Environmental Microbiology 56, 14231428.Google Scholar
Kurtzhals, J. A., Hey, A. S., Jardim, A., Kemp, M., Schaefer, K. U., Odera, E. O., Christensen, C. B., Githure, J. I., Olafson, R. W., Theander, T. G. and et al. (1994). Dichotomy of the human T cell response to Leishmania antigens. II. Absent or Th2-like response to gp63 and Th1-like response to lipophosphoglycan-associated protein in cells from cured visceral leishmaniasis patients. Clinical and Experimental Immunology 96, 416421.Google Scholar
Lacroix-Lamandé, S., Mancassola, R., Auray, G., Bernardet, N. and Laurent, F. (2008). CCR5 is involved in controlling the early stage of Cryptosporidium parvum infection in neonates but is dispensable for parasite elimination. Microbes and Infection 10, 390395.Google Scholar
Lambert, H., Vutova, P. P., Adams, W. C., Lore, K. and Barragan, A. (2009). The Toxoplasma gondii-shuttling function of dendritic cells is linked to the parasite genotype. Infection and Immunity 77, 16791688.Google Scholar
Lantier, L., Lacroix-Lamandé, S., Potiron, L., Metton, C., Drouet, F., Guesdon, W., Gnahoui-David, A., Le Vern, Y., Deriaud, E., Fenis, A., Rabot, S., Descamps, A., Werts, C. and Laurent, F. (2013). Intestinal CD103+ dendritic cells are key players in the innate immune control of Cryptosporidium parvum infection in neonatal mice. PLoS Pathogens 9, e1003801.Google Scholar
Laskay, T., van Zandbergen, G. and Solbach, W. (2003). Neutrophil granulocytes–Trojan horses for Leishmania major and other intracellular microbes? Trends in Microbiology 11, 210214.Google Scholar
Laurent, F., Eckmann, L., Savidge, T. C., Morgan, G., Theodos, C., Naciri, M. and Kagnoff, M. F. (1997). Cryptosporidium parvum infection of human intestinal epithelial cells induces the polarized secretion of C-X-C chemokines. Infection and Immunity 65, 50675073.Google Scholar
Lee, B., Sharron, M., Montaner, L. J., Weissman, D. and Doms, R. W. (1999). Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proceedings of the National Academy of Sciences of the United States of America 96, 52155220.Google Scholar
Liu, M., Guo, S., Hibbert, J. M., Jain, V., Singh, N., Wilson, N. O. and Stiles, J. K. (2011). CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cytokine and Growth Factor Reviews 22, 121130.Google ScholarPubMed
Loetscher, M., Gerber, B., Loetscher, P., Jones, S. A., Piali, L., Clark-Lewis, I., Baggiolini, M. and Moser, B. (1996). Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. Journal of Experimental Medicine 184, 963969.Google Scholar
Luangsay, S., Kasper, L. H., Rachinel, N., Minns, L. A., Mennechet, F. J., Vandewalle, A. and Buzoni-Gatel, D. (2003). CCR5 mediates specific migration of Toxoplasma gondii-primed CD8 lymphocytes to inflammatory intestinal epithelial cells. Gastroenterology 125, 491500.Google Scholar
Lucchi, N. W., Jain, V., Wilson, N. O., Singh, N., Udhayakumar, V. and Stiles, J. K. (2011). Potential serological biomarkers of cerebral malaria. Disease Markers 31, 327335.Google Scholar
Luker, K. E., Steele, J. M., Mihalko, L. A., Ray, P. and Luker, G. D. (2010). Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene 29, 45994610.CrossRefGoogle ScholarPubMed
Maillot, C., Gargala, G., Delaunay, A., Ducrotte, P., Brasseur, P., Ballet, J. J. and Favennec, L. (2000). Cryptosporidium parvum infection stimulates the secretion of TGF-beta, IL-8 and RANTES by Caco-2 cell line. Parasitology Research 86, 947949.Google Scholar
Mammari, N., Vignoles, P., Halabi, M. A., Darde, M. L. and Courtioux, B. (2014). In vitro infection of human nervous cells by two strains of Toxoplasma gondii: a kinetic analysis of immune mediators and parasite multiplication. PLoS ONE 9, e98491.Google Scholar
McCall, M. B. and Sauerwein, R. W. (2010). Interferon-gamma–central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. Journal of Leukocyte Biology 88, 11311143.Google Scholar
McColl, S. R. (2002). Chemokines and dendritic cells: a crucial alliance. Immunology and Cell Biology 80, 489496.Google Scholar
McDonald, V., Korbel, D. S., Barakat, F. M., Choudhry, N. and Petry, F. (2013). Innate immune responses against Cryptosporidium parvum infection. Parasite Immunology 35, 5564.Google Scholar
McGovern, K. E. and Wilson, E. H. (2013). Role of chemokines and trafficking of immune cells in parasitic infections. Current Immunology Reviews 9, 157168.Google Scholar
Melo, G. D., Silva, J. E., Grano, F. G., Souza, M. S. and Machado, G. F. (2015). Leishmania infection and neuroinflammation: specific chemokine profile and absence of parasites in the brain of naturally-infected dogs. Journal of Neuroimmunology 289, 2129.Google Scholar
Miller, C. M., Boulter, N. R., Ikin, R. J. and Smith, N. C. (2009). The immunobiology of the innate response to Toxoplasma gondii . International Journal for Parasitology 39, 2339.Google Scholar
Mohit, E. and Rafati, S. (2012). Chemokine-based immunotherapy: delivery systems and combination therapies. Immunotherapy 4, 807840.Google Scholar
Moradin, N. and Descoteaux, A. (2012). Leishmania promastigotes: building a safe niche within macrophages. Frontiers in Cellular and Infection Microbiology 2, 121.Google Scholar
Munoz, M., Liesenfeld, O. and Heimesaat, M. M. (2011). Immunology of Toxoplasma gondii . Immunological Reviews 240, 269285.Google Scholar
Newton, C. R., Hien, T. T. and White, N. (2000). Cerebral malaria. Journal of Neurology Neurosurgery & Psychiatry 69, 433441.Google Scholar
Nibbs, R. J. and Graham, G. J. (2013). Immune regulation by atypical chemokine receptors. Nature Reviews. Immunology 13, 815829.Google Scholar
Nie, C. Q., Bernard, N. J., Norman, M. U., Amante, F. H., Lundie, R. J., Crabb, B. S., Heath, W. R., Engwerda, C. R., Hickey, M. J., Schofield, L. and Hansen, D. S. (2009). IP-10-mediated T cell homing promotes cerebral inflammation over splenic immunity to malaria infection. PLoS Pathogens 5, e1000369.Google Scholar
Nitcheu, J., Bonduelle, O., Combadiere, C., Tefit, M., Seilhean, D., Mazier, D. and Combadiere, B. (2003). Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. Journal of Immunology 170, 22212228.Google Scholar
Niu, X., Wang, H. and Fu, Z. F. (2011). Role of chemokines in rabies pathogenesis and protection. Advances in Virus Research 79, 7389.Google Scholar
Noor, S., Habashy, A. S., Nance, J. P., Clark, R. T., Nemati, K., Carson, M. J. and Wilson, E. H. (2010). CCR7-dependent immunity during acute Toxoplasma gondii infection. Infection and Immunity 78, 22572263.Google Scholar
Nylen, S. and Gautam, S. (2010). Immunological perspectives of leishmaniasis. Journal of Global Infectious Diseases 2, 135146.Google Scholar
Oghumu, S., Lezama-Davila, C. M., Isaac-Marquez, A. P. and Satoskar, A. R. (2010). Role of chemokines in regulation of immunity against leishmaniasis. Experimental Parasitology 126, 389396.Google Scholar
Oliveira, W. N., Ribeiro, L. E., Schrieffer, A., Machado, P., Carvalho, E. M. and Bacellar, O. (2014). The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of human tegumentary leishmaniasis. Cytokine 66, 127132.Google Scholar
Paspalaki, P. K., Mihailidou, E. P., Bitsori, M., Tsagkaraki, D. and Mantzouranis, E. (2001). Polyomyositis and myocarditis associated with acquired toxoplasmosis in an immunocompetent girl. BMC Musculoskeletal Disorders 2, 8.Google Scholar
Pattaradilokrat, S., Li, J., Wu, J., Qi, Y., Eastman, R. T., Zilversmit, M., Nair, S. C., Huaman, M. C., Quinones, M., Jiang, H., Li, N., Zhu, J., Zhao, K., Kaneko, O., Long, C. A. and Su, X.-Z. (2014). Plasmodium genetic loci linked to host cytokine and chemokine responses. Genes and Immunity 15, 145152.Google Scholar
Perez-Mazliah, D. and Langhorne, J. (2014). CD4T-cell subsets in malaria: TH1/TH2 revisited. Frontiers in Immunology 5, 671.Google Scholar
Petry, F., Jakobi, V. and Tessema, T. S. (2010). Host immune response to Cryptosporidium parvum infection. Experimental Parasitology 126, 304309.Google Scholar
Pinard, J. A., Leslie, N. S. and Irvine, P. J. (2003). Maternal serologic screening for toxoplasmosis. Journal of Midwifery & Women's Health 48, 308316; quiz 386.Google Scholar
Rachinel, N., Buzoni-Gatel, D., Dutta, C., Mennechet, F. J., Luangsay, S., Minns, L. A., Grigg, M. E., Tomavo, S., Boothroyd, J. C. and Kasper, L. H. (2004). The induction of acute ileitis by a single microbial antigen of Toxoplasma gondii . Journal of Immunology 173, 27252735.Google Scholar
Racoosin, E. L. and Beverley, S. M. (1997). Leishmania major: promastigotes induce expression of a subset of chemokine genes in murine macrophages. Experimental Parasitology 85, 283295.Google Scholar
Rajagopalan, L. and Rajarathnam, K. (2006). Structural basis of chemokine receptor function–a model for binding affinity and ligand selectivity. Bioscience Reports 26, 325339.Google Scholar
Raz, E. and Mahabaleshwar, H. (2009). Chemokine signaling in embryonic cell migration: a fisheye view. Development 136, 12231229.Google Scholar
Ritter, U., Moll, H., Laskay, T., Brocker, E., Velazco, O., Becker, I. and Gillitzer, R. (1996). Differential expression of chemokines in patients with localized and diffuse cutaneous American leishmaniasis. Journal of Infectious Diseases 173, 699709.CrossRefGoogle ScholarPubMed
Rodrigues, I. A., Mazotto, A. M., Cardoso, V., Alves, R. L., Amaral, A. C., Silva, J. R., Pinheiro, A. S. and Vermelho, A. B. (2015). Natural products: insights into leishmaniasis inflammatory response. Mediators of Inflammation 2015, 835910.Google Scholar
Rodriguez-Sosa, M., Rosas, L. E., Terrazas, L. I., Lu, B., Gerard, C. and Satoskar, A. R. (2003). CC chemokine receptor 1 enhances susceptibility to Leishmania major during early phase of infection. Immunology and Cell Biology 81, 114120.CrossRefGoogle ScholarPubMed
Rostene, W., Kitabgi, P. and Parsadaniantz, S. M. (2007). Chemokines: a new class of neuromodulator? Nature Reviews Neuroscience 8, 895903.CrossRefGoogle ScholarPubMed
Rot, A. (2005). Contribution of Duffy antigen to chemokine function. Cytokine & Growth Factor Reviews 16, 687694.Google Scholar
Rothenberg, M. E. (2000). Chemokine knockout mice. Methods in Molecular Biology 138, 253257.Google Scholar
Ruffini, P. A., Morandi, P., Cabioglu, N., Altundag, K. and Cristofanilli, M. (2007). Manipulating the chemokine-chemokine receptor network to treat cancer. Cancer 109, 23922404.Google Scholar
Sallusto, F., Lenig, D., Mackay, C. R. and Lanzavecchia, A. (1998). Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. Journal of Experimental Medicine 187, 875883.Google Scholar
Sallusto, F., Palermo, B., Lenig, D., Miettinen, M., Matikainen, S., Julkunen, I., Forster, R., Burgstahler, R., Lipp, M. and Lanzavecchia, A. (1999). Distinct patterns and kinetics of chemokine production regulate dendritic cell function. European Journal of Immunology 29, 16171625.Google Scholar
Sanecka, A. and Frickel, E. M. (2012). Use and abuse of dendritic cells by Toxoplasma gondii . Virulence 3, 678689.Google Scholar
Sato, N., Kuziel, W. A., Melby, P. C., Reddick, R. L., Kostecki, V., Zhao, W., Maeda, N., Ahuja, S. K. and Ahuja, S. S. (1999). Defects in the generation of IFN-gamma are overcome to control infection with Leishmania donovani in CC chemokine receptor (CCR) 5-, macrophage inflammatory protein-1 alpha-, or CCR2-deficient mice. Journal of Immunology 163, 55195525.Google Scholar
Sato, N., Ahuja, S. K., Quinones, M., Kostecki, V., Reddick, R. L., Melby, P. C., Kuziel, W. A. and Ahuja, S. S. (2000). CC chemokine receptor (CCR)2 is required for langerhans cell migration and localization of T helper cell type 1 (Th1)-inducing dendritic cells. Absence of CCR2 shifts the Leishmania major-resistant phenotype to a susceptible state dominated by Th2 cytokines, b cell outgrowth, and sustained neutrophilic inflammation. Journal of Experimental Medicine 192, 205218.Google Scholar
Schall, T. J., Bacon, K., Toy, K. J. and Goeddel, D. V. (1990). Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347, 669671.Google Scholar
Schofield, L., Villaquiran, J., Ferreira, A., Schellekens, H., Nussenzweig, R. and Nussenzweig, V. (1987). Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330, 664666.Google Scholar
Schulthess, J., Meresse, B., Ramiro-Puig, E., Montcuquet, N., Darche, S., Bègue, B., Ruemmele, F., Combadière, C., Di Santo, J. P., Buzoni-Gatel, D. and Cerf-Bensussan, N. (2012). Interleukin-15-dependent NKp46+ innate lymphoid cells control intestinal inflammation by recruiting inflammatory monocytes. Immunity 37, 108121.Google Scholar
Serbina, N. V. and Pamer, E. G. (2006). Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nature Immunology 7, 311317.Google Scholar
Shapira, M. and Zinoviev, A. (2011). Leishmania parasites act as a Trojan horse that paralyzes the translation system of host macrophages. Cell Host & Microbe 9, 257259.Google Scholar
Shi, C. and Pamer, E. G. (2011). Monocyte recruitment during infection and inflammation. Nature Reviews. Immunology 11, 762774.Google Scholar
Shi, C., Jia, T., Mendez-Ferrer, S., Hohl, T. M., Serbina, N. V., Lipuma, L., Leiner, I., Li, M. O., Frenette, P. S. and Pamer, E. G. (2011). Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands. Immunity 34, 590601.Google Scholar
Speer, C. A. and Dubey, J. P. (1998). Ultrastructure of early stages of infections in mice fed Toxoplasma gondii oocysts. Parasitology 116(Pt 1), 3542.Google Scholar
Sponaas, A. M., Freitas do Rosario, A. P., Voisine, C., Mastelic, B., Thompson, J., Koernig, S., Jarra, W., Renia, L., Mauduit, M., Potocnik, A. J. and Langhorne, J. (2009). Migrating monocytes recruited to the spleen play an important role in control of blood stage malaria. Blood 114, 55225531.CrossRefGoogle Scholar
Srivastava, K., Cockburn, I. A., Swaim, A., Thompson, L. E., Tripathi, A., Fletcher, C. A., Shirk, E. M., Sun, H., Kowalska, M. A., Fox-Talbot, K., Sullivan, D., Zavala, F. and Morrell, C. N. (2008). Platelet factor 4 mediates inflammation in experimental cerebral malaria. Cell Host & Microbe 4, 179187.Google Scholar
Steege, J. C., Buurman, W. A. and Forget, P. P. (1997). The neonatal development of intraepithelial and lamina propria lymphocytes in the murine small intestine. Developmental Immunology 5, 121128.Google Scholar
Steigerwald, M. and Moll, H. (2005). Leishmania major modulates chemokine and chemokine receptor expression by dendritic cells and affects their migratory capacity. Infection and Immunity 73, 25642567.Google Scholar
Teixeira, M. J., Teixeira, C. R., Andrade, B. B., Barral-Netto, M. and Barral, A. (2006). Chemokines in host–parasite interactions in leishmaniasis. Trends in Parasitology 22, 3240.Google Scholar
Torre, D., Speranza, F., Giola, M., Matteelli, A., Tambini, R. and Biondi, G. (2002). Role of Th1 and Th2 cytokines in immune response to uncomplicated Plasmodium falciparum malaria. Clinical and Diagnostic Laboratory Immunology 9, 348351.Google Scholar
Tsou, C. L., Peters, W., Si, Y., Slaymaker, S., Aslanian, A. M., Weisberg, S. P., Mack, M. and Charo, I. F. (2007). Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. The Journal of Clinical Investigation 117, 902909.Google Scholar
Tuteja, R. (2007). Malaria – an overview. The FEBS Journal 274, 46704679.Google Scholar
Tzipori, S. and Ward, H. (2002). Cryptosporidiosis: biology, pathogenesis and disease. Microbes and Infection 4, 10471058.Google Scholar
Ubogu, E. E., Callahan, M. K., Tucky, B. H. and Ransohoff, R. M. (2006). CCR5 expression on monocytes and T cells: modulation by transmigration across the blood-brain barrier in vitro . Cellular Immunology 243, 1929.Google Scholar
Ulvmar, M. H., Hub, E. and Rot, A. (2011). Atypical chemokine receptors. Experimental Cell Research 317, 556568.Google Scholar
van Zandbergen, G., Klinger, M., Mueller, A., Dannenberg, S., Gebert, A., Solbach, W. and Laskay, T. (2004). Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. Journal of Immunology 173, 65216525.Google Scholar
Wang, H.-C., Dann, S. M., Okhuysen, P. C., Lewis, D. E., Chappell, C. L., Adler, D. G. and White, A. C. (2007). High levels of CXCL10 are produced by intestinal epithelial cells in AIDS patients with active cryptosporidiosis but not after reconstitution of immunity. Infection and Immunity 75, 481487.Google Scholar
Watts, A. O., Verkaar, F., van der Lee, M. M., Timmerman, C. A., Kuijer, M., van Offenbeek, J., van Lith, L. H., Smit, M. J., Leurs, R., Zaman, G. J. and Vischer, H. F. (2013). beta-Arrestin recruitment and G protein signaling by the atypical human chemokine decoy receptor CCX-CKR. Journal of Biological Chemistry 288, 71697181.Google Scholar
Weidanz, W. P., LaFleur, G., Brown, A., Burns, J. M. Jr., Gramaglia, I. and van der Heyde, H. C. (2010). Gammadelta T cells but not NK cells are essential for cell-mediated immunity against Plasmodium chabaudi malaria. Infection and Immunity 78, 43314340.Google Scholar
Wheeler, R. J., Gluenz, E. and Gull, K. (2011). The cell cycle of Leishmania: morphogenetic events and their implications for parasite biology. Molecular Microbiology 79, 647662.Google Scholar
Wilson, N. O., Jain, V., Roberts, C. E., Lucchi, N., Joel, P. K., Singh, M. P., Nagpal, A. C., Dash, A. P., Udhayakumar, V., Singh, N. and Stiles, J. K. (2011). CXCL4 and CXCL10 predict risk of fatal cerebral malaria. Disease Markers 30, 3949.Google Scholar
Wong, M. M. and Fish, E. N. (2003). Chemokines: attractive mediators of the immune response. Seminars in Immunology 15, 514.Google Scholar
Wu, X., Lee, V. C., Chevalier, E. and Hwang, S. T. (2009). Chemokine receptors as targets for cancer therapy. Current Pharmaceutical Design 15, 742757.Google Scholar
Wykes, M. N. and Horne-Debets, J. (2012). Dendritic cells: the Trojan horse of malaria? International Journal for Parasitology 42, 583587.Google Scholar
Wykes, M. N., Kay, J. G., Manderson, A., Liu, X. Q., Brown, D. L., Richard, D. J., Wipasa, J., Jiang, S. H., Jones, M. K., Janse, C. J., Waters, A. P., Pierce, S. K., Miller, L. H., Stow, J. L. and Good, M. F. (2011). Rodent blood-stage Plasmodium survive in dendritic cells that infect naive mice. Proceedings of the National Academy of Sciences of the United States of America 108, 1120511210.CrossRefGoogle ScholarPubMed
Yang, D., Chen, Q., Hoover, D. M., Staley, P., Tucker, K. D., Lubkowski, J. and Oppenheim, J. J. (2003). Many chemokines including CCL20/MIP-3 alpha display antimicrobial activity. Journal of Leukocyte Biology 74, 448455.Google Scholar
Yung, S. C. and Murphy, P. M. (2012). Antimicrobial chemokines. Frontiers in Immunology 3, 276.CrossRefGoogle ScholarPubMed
Zhao, Y., Mangalmurti, N. S., Xiong, Z., Prakash, B., Guo, F., Stolz, D. B. and Lee, J. S. (2011). Duffy antigen receptor for chemokines mediates chemokine endocytosis through a macropinocytosis-like process in endothelial cells. PLoS ONE 6, e29624.Google Scholar
Zlotnik, A. and Yoshie, O. (2012). The chemokine superfamily revisited. Immunity 36, 705716.Google Scholar