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Phagocyte-specific S100 proteins in the local response to the Echinococcus granulosus larva

Published online by Cambridge University Press:  05 January 2012

TATIANA BASIKA
Affiliation:
Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) e Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay
NATALIA MUÑOZ
Affiliation:
Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) e Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay
CECILIA CASARAVILLA
Affiliation:
Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) e Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay
FLORENCIA IRIGOÍN
Affiliation:
Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) e Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay
CARLOS BATTHYÁNY
Affiliation:
Unidad de Bioquímica y Proteómica Analíticas, Instituto Pasteur de Montevideo, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay
MARIANA BONILLA
Affiliation:
Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) e Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay
GUSTAVO SALINAS
Affiliation:
Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) e Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay
JOSÉ PEDRO PACHECO
Affiliation:
Departamento de Patología, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay
JOHANESS ROTH
Affiliation:
Department of Dermatology, University of Münster, Münster, Germany
ROSARIO DURÁN
Affiliation:
Unidad de Bioquímica y Proteómica Analíticas, Instituto Pasteur de Montevideo, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay
ALVARO DÍAZ*
Affiliation:
Cátedra de Inmunología, Departamento de Biociencias (Facultad de Química) e Instituto de Química Biológica (Facultad de Ciencias), Universidad de la República, Montevideo, Uruguay
*
*Corresponding author: Cátedra de Inmunología, Instituto de Higiene, Avenida Alfredo Navarro 3051, Montevideo, CP 11600, Uruguay. Tel/Fax: +59824874320. E-mail: [email protected].

Summary

Infection by larval Echinococcus granulosus is usually characterized by tight inflammatory control. However, various degrees of chronic granulomatous inflammation are also observed, reaching a high point in infection of cattle by the most prevalent parasite strain worldwide, which is not well adapted to this host species. In this context, epithelioid and multinucleated giant macrophages surround the parasite, and the secreted products of these cells often associate with the larval wall. The phagocyte-specific S100 proteins, S100A8, S100A9 and S100A12, are important non-conventionally secreted amplifiers of inflammatory responses. We have analysed by proteomics and immunohistochemistry the presence of these proteins at the E. granulosus larva-host interface. We found that, in the context of inflammatory control as observed in human infections, the S100 proteins are not abundant, but S100A9 and S100A8 can be expressed by eosinophils distal to the parasite. In the granulomatous inflammation context as observed in cattle infections, we found that S100A12 is one of the most abundant host-derived, parasite-associated proteins, while S100A9 and S100A8 are not present at similarly high levels. As expected, S100A12 derives mostly from the epithelioid and multinucleated giant cells. S100A12, as well as cathepsin K and matrix metalloproteinase-9, also expressed by E. granulosus-elicited epithelioid cells, are connected to the Th17 arm of immunity, which may therefore be involved in this granulomatous response.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Aguiar-Passeti, T., Postol, E., Sorg, C. and Mariano, M. (1997). Epithelioid cells from foreign-body granuloma selectively express the calcium-binding protein MRP-14, a novel down-regulatory molecule of macrophage activation. Journal of Leukocyte Biology 62, 852858.CrossRefGoogle ScholarPubMed
Akpek, E. K., Liu, S. H., Thompson, R. and Gottsch, J. D. (2002). Identification of paramyosin as a binding protein for calgranulin C in experimental helminthic keratitis. Investigative Ophthalmology and Visual Science 43, 26772684.Google ScholarPubMed
Arai, K., Mizuno, K., Yamada, T. and Nozawa, R. (1999). Immunohistochemical evaluation of MRP-14 expression in epithelioid granuloma using monoclonal antibody 60B8. Journal of Investigative Allergology and Clinical Immunology 9, 2126.Google ScholarPubMed
Bortoletti, G. and Ferretti, G. (1978). Ultrastructural aspects of fertile and sterile cysts of Echinococcus granulosus developed in hosts of different species. International Journal for Parasitology 8, 421431.CrossRefGoogle ScholarPubMed
Breijo, M., Spinelli, P., Sim, R. B. and Ferreira, A. M. (1998). Echinococcus granulosus: an intraperitoneal diffusion chamber model of secondary infection in mice. Experimental Parasitology 90, 270276.CrossRefGoogle ScholarPubMed
Campo, I., Morbini, P., Zorzetto, M., Tinelli, C., Brunetta, E., Villa, C., Bombieri, C., Cuccia, M., Agostini, C., Bozzi, V., Facoetti, A., Ferrarotti, I., Mazzola, P., Scabini, R., Semenzato, G., Pignatti, P. F., Pozzi, E. and Luisetti, M. (2007). Expression of receptor for advanced glycation end products in sarcoid granulomas. American Journal of Respiratory and Critical Care Medicine 175, 498506.CrossRefGoogle ScholarPubMed
Casaravilla, C., Brearley, C., Soule, S., Fontana, C., Veiga, N., Bessio, M. I., Ferreira, F., Kremer, C. and Diaz, A. (2006). Characterization of myo-inositol hexakisphosphate deposits from larval Echinococcus granulosus. FEBS Journal 273, 31923203.CrossRefGoogle ScholarPubMed
Casaravilla, C. and Díaz, A. (2010). Studies on the structural mucins of the Echinococcus granulosus laminated layer. Molecular and Biochemical Parasitology 174, 132136.CrossRefGoogle ScholarPubMed
Coltorti, E. A. and Varela-Díaz, V. M. (1974). Echinococcus granulosus: Penetration of macromolecules and their localization in the parasite membranes of cysts. Experimental Parasitology 35, 225231.CrossRefGoogle Scholar
Coury, F., Annels, N., Rivollier, A., Olsson, S., Santoro, A., Speziani, C., Azocar, O., Flacher, M., Djebali, S., Tebib, J., Brytting, M., Egeler, R. M., Rabourdin-Combe, C., Henter, J. I., Arico, M. and Delprat, C. (2008). Langerhans cell histiocytosis reveals a new IL-17A-dependent pathway of dendritic cell fusion. Nature, Medicine 14, 8187.CrossRefGoogle ScholarPubMed
Dai, W. J., Waldvogel, A., Siles-Lucas, M. and Gottstein, B. (2004). Echinococcus multilocularis proliferation in mice and respective parasite 14-3-3 gene expression is mainly controlled by an alphabeta CD4 T-cell-mediated immune response. Immunology 112, 481488.CrossRefGoogle ScholarPubMed
Delabie, J., De Wolf-Peeters, C., Van Den Oord, J. J. and Desmet, V. J. (1990). Differential expression of the calcium-binding proteins MRP8 and MRP14 in granulomatous conditions: an immunohistochemical study. Clinical and Experimental Immunology 81, 123126.CrossRefGoogle ScholarPubMed
Dell'angelica, E. C., Schleicher, C. H. and Santome, J. A. (1994). Primary structure and binding properties of calgranulin C, a novel S100-like calcium-binding protein from pig granulocytes. Journal of Biological Chemistry 269, 2892928936.CrossRefGoogle Scholar
Díaz, A. and Allen, J. E. (2007). Mapping immune response profiles: the emerging scenario from helminth immunology. European Journal of Immunology 37, 33193326.CrossRefGoogle ScholarPubMed
Díaz, A., Casaravilla, C., Allen, J. E., Sim, R. B. and Ferreira, A. M. (2011 a). Understanding the laminated layer of larval Echinococcus II: immunology. Trends in Parasitology 27, 264272.CrossRefGoogle ScholarPubMed
Díaz, A., Casaravilla, C., Irigoín, F., Lin, G., Previato, J. O. and Ferreira, F. (2011 b). Understanding the laminated layer of larval Echinococcus I: structure. Trends in Parasitology 27, 204213.CrossRefGoogle ScholarPubMed
Díaz, A., Ferreira, A. and Sim, R. B. (1997). Complement evasion by Echinococcus granulosus: sequestration of host factor H in the hydatid cyst wall. Journal of Immunology 158, 37793786.CrossRefGoogle ScholarPubMed
Díaz, A., Ibarguren, S., Breijo, M., Willis, A. C. and Sim, R. B. (2000 a). Host-derived annexin II at the host-parasite interface of the Echinococcus granulosus hydatid cyst. Molecular and Biochemical Parasitology 110, 171176.CrossRefGoogle ScholarPubMed
Díaz, A., Willis, A. C. and Sim, R. B. (2000 b). Expression of the proteinase specialized in bone resorption, cathepsin K, in granulomatous inflammation. Molecular Medicine 6, 648659.CrossRefGoogle ScholarPubMed
Edgeworth, J. D., Abiose, A. and Jones, B. R. (1993). An immunohistochemical analysis of onchocercal nodules: evidence for an interaction between macrophage MRP8/MRP14 and adult Onchocerca volvulus. Clinical and Experimental Immunology 92, 8492.CrossRefGoogle ScholarPubMed
Ehrchen, J. M., Sunderkotter, C., Foell, D., Vogl, T. and Roth, J. (2009). The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. Journal of Leukocyte Biology 86, 557566.CrossRefGoogle ScholarPubMed
Gottsch, J. D., Eisinger, S. W., Liu, S. H. and Scott, A. L. (1999). Calgranulin C has filariacidal and filariastatic activity. Infection and Immunity 67, 66316636.CrossRefGoogle ScholarPubMed
Gottstein, B. and Hemphill, A. (1997). Immunopathology of Echinococcosis. Chemical Immunology 66, 177208.Google ScholarPubMed
Haider, A. S., Lowes, M. A., Suarez-Farinas, M., Zaba, L. C., Cardinale, I., Khatcherian, A., Novitskaya, I., Wittkowski, K. M. and Krueger, J. G. (2008). Identification of cellular pathways of “type 1,” Th17 T cells, and TNF- and inducible nitric oxide synthase-producing dendritic cells in autoimmune inflammation through pharmacogenomic study of cyclosporine A in psoriasis. Journal of Immunology 180, 19131920.CrossRefGoogle ScholarPubMed
Hamazaki, H. (1987). Ca2+-mediated association of human serum amyloid P component with heparan sulfate and dermatan sulfate. Journal of Biological Chemistry 262, 14561460.CrossRefGoogle ScholarPubMed
Heegaard, N. H., He, X. and Blomberg, L. G. (2006). Binding of Ca2+, Mg2+, and heparin by human serum amyloid P component in affinity capillary electrophoresis. Electrophoresis 27, 26092615.CrossRefGoogle ScholarPubMed
Hitomi, J., Yamaguchi, K., Kikuchi, Y., Kimura, T., Maruyama, K. and Nagasaki, K. (1996). A novel calcium-binding protein in amniotic fluid, CAAF1: its molecular cloning and tissue distribution. Journal of Cell Science 109, 805815.CrossRefGoogle ScholarPubMed
Hofmann, M. A., Drury, S., Fu, C., Qu, W., Taguchi, A., Lu, Y., Avila, C., Kambham, N., Bierhaus, A., Nawroth, P., Neurath, M. F., Slattery, T., Beach, D., McClary, J., Nagashima, M., Morser, J., Stern, D. and Schmidt, A. M. (1999). RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 97, 889901.CrossRefGoogle Scholar
Ilg, E. C., Troxler, H., Burgisser, D. M., Kuster, T., Markert, M., Guignard, F., Hunziker, P., Birchler, N. and Heizmann, C. W. (1996). Amino acid sequence determination of human S100A12 (P6, calgranulin C, CGRP, CAAF1) by tandem mass spectrometry. Biochemical and Biophysical Research Communications 225, 146150.CrossRefGoogle ScholarPubMed
Irigoín, F., Casaravilla, C., Iborra, F., Sim, R. B., Ferreira, F. and Díaz, A. (2004). Unique precipitation and exocytosis of a calcium salt of myo-inositol hexakisphosphate in larval Echinococcus granulosus. Journal of Cellular Biochemistry 93, 12721281.CrossRefGoogle ScholarPubMed
Irigoín, F., Ferreira, F., Fernández, C., Sim, R. B. and Díaz, A. (2002). myo-Inositol hexakisphosphate is a major component of an extracellular structure in the parasitic cestode Echinococcus granulosus. The Biochemical Journal 362, 297304.CrossRefGoogle Scholar
Irigoín, F., Laich, A., Ferreira, A. M., Fernández, C., Sim, R. B. and Díaz, A. (2008). Resistance of the Echinococcus granulosus cyst wall to complement activation: analysis of the role of InsP 6 deposits. Parasite Immunology 30, 354364.CrossRefGoogle ScholarPubMed
Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J. and Mann, M. (2005). Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Molecular and Cellular Proteomics 4, 12651272.CrossRefGoogle ScholarPubMed
Ivanov, S., Bozinovski, S., Bossios, A., Valadi, H., Vlahos, R., Malmhall, C., Sjostrand, M., Kolls, J. K., Anderson, G. P. and Linden, A. (2007). Functional relevance of the IL-23-IL-17 axis in lungs in vivo. American Journal of Respiratory Cell and Molecular Biology 36, 442451.CrossRefGoogle ScholarPubMed
Jenkins, D. J., Romig, T. and Thompson, R. C. (2005). Emergence/re-emergence of Echinococcus spp. – a global update. International Journal for Parasitology 35, 12051219.CrossRefGoogle ScholarPubMed
Kim, M. H., Choi, Y. W., Choi, H. Y., Myung, K. B. and Cho, S. N. (2006). The expression of RAGE and EN-RAGE in leprosy. British Journal of Dermatology 154, 594601.CrossRefGoogle ScholarPubMed
Koenders, M. I., Kolls, J. K., Oppers-Walgreen, B., Van Den Bersselaar, L., Joosten, L. A., Schurr, J. R., Schwarzenberger, P., Van Den Berg, W. B. and Lubberts, E. (2005 a). Interleukin-17 receptor deficiency results in impaired synovial expression of interleukin-1 and matrix metalloproteinases 3, 9, and 13 and prevents cartilage destruction during chronic reactivated streptococcal cell wall-induced arthritis. Arthritis and Rheumatism 52, 32393247.CrossRefGoogle ScholarPubMed
Koenders, M. I., Lubberts, E., Oppers-Walgreen, B., Van Den Bersselaar, L., Helsen, M. M., Di Padova, F. E., Boots, A. M., Gram, H., Joosten, L. A. and Van Den Berg, W. B. (2005 b). Blocking of interleukin-17 during reactivation of experimental arthritis prevents joint inflammation and bone erosion by decreasing RANKL and interleukin-1. American Journal of Pathology 167, 141149.CrossRefGoogle ScholarPubMed
Krensky, A. M. and Clayberger, C. (2009). Biology and clinical relevance of granulysin. Tissue Antigens 73, 193198.CrossRefGoogle ScholarPubMed
Kurata, A., Terado, Y., Schulz, A., Fujioka, Y. and Franke, F. E. (2005). Inflammatory cells in the formation of tumor-related sarcoid reactions. Human Pathology 36, 546554.CrossRefGoogle ScholarPubMed
Lee, C., Bongcam-Rudloff, E., Sollner, C., Jahnen-Dechent, W. and Claesson-Welsh, L. (2009). Type 3 cystatins; fetuins, kininogen and histidine-rich glycoprotein. Frontiers in Bioscience 14, 29112922.CrossRefGoogle ScholarPubMed
Liu, R., Mori, S., Wake, H., Zhang, J., Liu, K., Izushi, Y., Takahashi, H. K., Peng, B. and Nishibori, M. (2009). Establishment of in vitro binding assay of high mobility group box-1 and S100A12 to receptor for advanced glycation endproducts: heparin's effect on binding. Acta Medica Okayama 63, 203211.Google ScholarPubMed
Liu, S. H. and Gottsch, J. D. (1996). Amino acid sequence of an immunogenic corneal stromal protein. Invest Ophthalmol Vis Sci 37, 944948.Google ScholarPubMed
Loser, K., Vogl, T., Voskort, M., Lueken, A., Kupas, V., Nacken, W., Klenner, L., Kuhn, A., Foell, D., Sorokin, L., Luger, T. A., Roth, J. and Beissert, S. (2010). The Toll-like receptor 4 ligands Mrp8 and Mrp14 are crucial in the development of autoreactive CD8+ T cells. Nature Medicine 16, 713717.CrossRefGoogle ScholarPubMed
Marco, M., Baz, A., Fernández, C., Gonzalez, G., Hellman, U., Salinas, G. and Nieto, A. (2006). A relevant enzyme in granulomatous reaction, active matrix metalloproteinase-9, found in bovine Echinococcus granulosus hydatid cyst wall and fluid. Parasitology Research 100, 131139.CrossRefGoogle Scholar
Marti, T., Erttmann, K. D. and Gallin, M. Y. (1996). Host-parasite interaction in human onchocerciasis: identification and sequence analysis of a novel human calgranulin. Biochemical and Biophysical Research Communications 221, 454458.CrossRefGoogle ScholarPubMed
McMorran, B. J., Patat, S. A., Carlin, J. B., Grimwood, K., Jones, A., Armstrong, D. S., Galati, J. C., Cooper, P. J., Byrnes, C. A., Francis, P. W., Robertson, C. F., Hume, D. A., Borchers, C. H., Wainwright, C. E. and Wainwright, B. J. (2007). Novel neutrophil-derived proteins in bronchoalveolar lavage fluid indicate an exaggerated inflammatory response in pediatric cystic fibrosis patients. Clinical Chemistry 53, 17821791.CrossRefGoogle ScholarPubMed
Monteiro, K. M., De Carvalho, M. O., Zaha, A. and Ferreira, H. B. (2010). Proteomic analysis of the Echinococcus granulosus metacestode during infection of its intermediate host. Proteomics 10, 19851999.CrossRefGoogle ScholarPubMed
Morbini, P., Villa, C., Campo, I., Zorzetto, M., Inghilleri, S. and Luisetti, M. (2006). The receptor for advanced glycation end products and its ligands: a new inflammatory pathway in lung disease? Modern Pathology 19, 14371445.CrossRefGoogle ScholarPubMed
Mufarrij, A. A., Arnaut, A., Meshefedjian, G. and Matossian, R. M. (1990). Comparative histopathological study in the hepatic and pulmonary human hydatidosis. Helminthologia 27, 279290.Google Scholar
Muhlschlegel, F., Sygulla, L., Frosch, P., Massetti, P. and Frosch, M. (1993). Paramyosin of Echinococcus granulosus: cDNA sequence and characterization of a tegumental antigen. Parasitol Research 79, 660666.CrossRefGoogle ScholarPubMed
Nieberle, K. and Cohrs, P. (1967). Textbook of the Special Pathological Anatomy of Domestic Animals. Pergamon Press, Oxford, UK.Google Scholar
Okamoto Yoshida, Y., Umemura, M., Yahagi, A., O'brien, R. L., Ikuta, K., Kishihara, K., Hara, H., Nakae, S., Iwakura, Y. and Matsuzaki, G. (2010). Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung. Journal of Immunology 184, 44144422.CrossRefGoogle ScholarPubMed
Pietzsch, J. and Hoppmann, S. (2009). Human S100A12: a novel key player in inflammation? Amino Acids 36, 381389.CrossRefGoogle ScholarPubMed
Prause, O., Bozinovski, S., Anderson, G. P. and Linden, A. (2004). Increased matrix metalloproteinase-9 concentration and activity after stimulation with interleukin-17 in mouse airways. Thorax 59, 313317.CrossRefGoogle ScholarPubMed
Rabinovich, G. A. and Ilarregui, J. M. (2009). Conveying glycan information into T-cell homeostatic programs: a challenging role for galectin-1 in inflammatory and tumor microenvironments. Immunological Reviews 230, 144159.CrossRefGoogle ScholarPubMed
Rao, D. G. and Mohiyuddin, S. (1974). Incidence of hydatid cysts in bovines and histopathological changes of pulmonary tissue in hydatidosis. Indian Journal of Animal Science 44, 437440.Google Scholar
Richards, K. S., Arme, C. and Bridges, J. F. (1983). Echinococcus granulosus equinus: an ultrastructural study of murine tissue response to hydatid cysts. Parasitology 86, 407417.CrossRefGoogle ScholarPubMed
Ritter, M., Gross, O., Kays, S., Ruland, J., Nimmerjahn, F., Saijo, S., Tschopp, J., Layland, L. E. and Prazeres Da Costa, C. (2010). Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proceedings of the National Academy of Sciences, USA 107, 2045920464.CrossRefGoogle ScholarPubMed
Robinson, M. J., Tessier, P., Poulsom, R. and Hogg, N. (2002). The S100 family heterodimer, MRP-8/14, binds with high affinity to heparin and heparan sulfate glycosaminoglycans on endothelial cells. Journal of Biological Chemistry 277, 36583665.CrossRefGoogle ScholarPubMed
Roth, J., Burwinkel, F., Van Den Bos, C., Goebeler, M., Vollmer, E. and Sorg, C. (1993). MRP8 and MRP14, S-100-like proteins associated with myeloid differentiation, are translocated to plasma membrane and intermediate filaments in a calcium-dependent manner. Blood 82, 18751883.CrossRefGoogle Scholar
Rutitzky, L. I., Smith, P. M. and Stadecker, M. J. (2009). T-bet protects against exacerbation of schistosome egg-induced immunopathology by regulating Th17-mediated inflammation. European Journal of Immunology 39, 24702481.CrossRefGoogle ScholarPubMed
Sakamoto, T. and Cabrera, P. A. (2003). Immunohistochemical observations on cellular response in unilocular hydatid lesions and lymph nodes of cattle. Acta Tropica 85, 271279.CrossRefGoogle ScholarPubMed
Slais, J. and Vanek, M. (1980). Tissue reaction to spherical and lobular hydatid cysts of Echinococcus granulosus (Batsch, 1786). Folia Parasitologica (Praha) 27, 135143.Google ScholarPubMed
Sonnenberg, G. F., Fouser, L. A. and Artis, D. (2010). Functional biology of the IL-22-IL-22R pathway in regulating immunity and inflammation at barrier surfaces. Advances in Immunology 107, 129.CrossRefGoogle ScholarPubMed
Stadelmann, B., Spiliotis, M., Muller, J., Scholl, S., Muller, N., Gottstein, B. and Hemphill, A. (2010). Echinococcus multilocularis phosphoglucose isomerase (EmPGI): A glycolytic enzyme involved in metacestode growth and parasite-host cell interactions. International Journal for Parasitology 40, 15631574.CrossRefGoogle ScholarPubMed
Struyf, S., Proost, P., Lenaerts, J. P., Stoops, G., Wuyts, A. and Van Damme, J. (2001). Identification of a blood-derived chemoattractant for neutrophils and lymphocytes as a novel CC chemokine, Regakine-1. Blood 97, 21972204.CrossRefGoogle ScholarPubMed
Sunderkotter, C. H., Tomimori-Yamashita, J., Nix, V., Maeda, S. M., Sindrilaru, A., Mariano, M., Sorg, C. and Roth, J. (2004). High expression of myeloid-related proteins 8 and 14 characterizes an inflammatorily active but ineffective response of macrophages during leprosy. Immunology 111, 472480.CrossRefGoogle ScholarPubMed
Terasaki, F., Fujita, M., Shimomura, H., Tsukada, B., Otsuka, K., Otsuka, K., Katashima, T., Ikemoto, M. and Kitaura, Y. (2007). Enhanced expression of myeloid-related protein complex (MRP8/14) in macrophages and multinucleated giant cells in granulomas of patients with active cardiac sarcoidosis. Circulation Journal 71, 15451550.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. (1995). Biology and systematics of Echinococcus. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.), pp. 150. CAB International, Wallingford, UK.Google Scholar
Turk, V., Stoka, V. and Turk, D. (2008). Cystatins: biochemical and structural properties, and medical relevance. Front Biosci 13, 54065420.CrossRefGoogle ScholarPubMed
Vogl, T., Propper, C., Hartmann, M., Strey, A., Strupat, K., Van Den Bos, C., Sorg, C. and Roth, J. (1999 a). S100A12 is expressed exclusively by granulocytes and acts independently from MRP8 and MRP14. Journal of Biological Chemistry 274, 2529125296.CrossRefGoogle ScholarPubMed
Vogl, T., Roth, J., Sorg, C., Hillenkamp, F. and Strupat, K. (1999 b). Calcium-induced noncovalently linked tetramers of MRP8 and MRP14 detected by ultraviolet matrix-assisted laser desorption/ionization mass spectrometry. Journal of the American Society of Mass Spectrometry 10, 11241130.Google ScholarPubMed
Vogl, T., Tenbrock, K., Ludwig, S., Leukert, N., Ehrhardt, C., Van Zoelen, M. A., Nacken, W., Foell, D., Van Der Poll, T., Sorg, C. and Roth, J. (2007). Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nature Medicine 13, 10421049.CrossRefGoogle ScholarPubMed
Vuitton, D. A. and Gottstein, B. (2010). Echinococcus multilocularis and its intermediate host: a model of parasite-host interplay. Journal of Biomedicine and Biotechnology 2010, 923193.CrossRefGoogle Scholar
Wolk, K., Witte, E., Wallace, E., Docke, W. D., Kunz, S., Asadullah, K., Volk, H. D., Sterry, W. and Sabat, R. (2006). IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis. European Journal of Immunology 36, 13091323.CrossRefGoogle ScholarPubMed
Yamashita, J., Ohbayashi, M. and Sakamoto, T. (1961). Studies on echinococcosis XII. Ovine experimental cases of unilocular echinococcosis. Japanese Journal of Veterinary Research 9, 2330.Google Scholar
Yang, T. H., Tzeng, S., Cheng, I., Burnett, M. G., Yoshizawa, Y., Fukuyama, K., Lee, S. C. and Epstein, W. L. (1997). Identification of the mouse calcium-binding proteins, MRP 8 and MRP 14, in Schistosoma mansoni-induced granulomas: biochemical and functional characterization. Journal of Leukocyte Biology 61, 258266.CrossRefGoogle ScholarPubMed
Yang, Z., Yan, W. X., Cai, H., Tedla, N., Armishaw, C., Di Girolamo, N., Wang, H. W., Hampartzoumian, T., Simpson, J. L., Gibson, P. G., Hunt, J., Hart, P., Hughes, J. M., Perry, M. A., Alewood, P. F. and Geczy, C. L. (2007). S100A12 provokes mast cell activation: a potential amplification pathway in asthma and innate immunity. Journal of Allergy and Clinical Immunology 119, 106114.CrossRefGoogle ScholarPubMed
Zwadlo, G., Bruggen, J., Gerhards, G., Schlegel, R. and Sorg, C. (1988). Two calcium-binding proteins associated with specific stages of myeloid cell differentiation are expressed by subsets of macrophages in inflammatory tissues. Clinical and Experimental Immunology 72, 510515.Google ScholarPubMed
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