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*
Schistosomiasis Immunology and Pathology Unit and
Max Planck Institut für Immunbiologie, Freiburg, Germany;
Department of Microbiology/Immunology, Cornell University, Ithaca, NY 14853;
Immunobiology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892;
¶ Department of Biochemistry, University of Extremadura, Caceres, Spain; and
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Biomedical Research Institute, Rockville, MD 20852
Type 2 cytokines regulate fibrotic liver pathology in mice infected
with Schistosoma mansoni. Switching the immune response
to a type 1-dominant reaction has proven highly effective at reducing
the pathologic response. Activation of NOS-2 is critical, because type
1-deviated/NO synthase 2 (NOS-2)-deficient mice completely fail to
control their response. Here, we demonstrate the differential
regulation of NOS-2 and arginase type 1 (Arg-1) by type 1/type 2
cytokines in vivo and for the first time show a critical role for
arginase in the pathogenesis of schistosomiasis. Using
cytokine-deficient mice and two granuloma models, we show that
induction of Arg-1 is type 2 cytokine dependent. Schistosome eggs
induce Arg-1, while Mycobacterium avium-infected mice
develop a dominant NOS-2 response. IFN-
suppresses Arg-1 activity,
because type 1 polarized IL-4/IL-10-deficient, IL-4/IL-13-deficient,
and egg/IL-12-sensitized animals fail to up-regulate Arg-1 following
egg exposure. Notably, granuloma size decreases in these
type-1-deviated/Arg-1-unresponsive mice, suggesting an important
regulatory role for Arg-1 in schistosome egg-induced pathology. To test
this hypothesis, we administered difluoromethylornithine to block
ornithine-aminodecarboxylase, which uses the product of arginine
metabolism, L-ornithine, to generate polyamines.
Strikingly, granuloma size and hepatic fibrosis increased in the
ornithine-aminodecarboxylase-inhibited mice. Furthermore, we show that
type 2 cytokine-stimulated macrophages produce proline under strict
arginase control. Together, these data reveal an important regulatory
role for the arginase biosynthetic pathway in the regulation of
inflammation and demonstrate that differential activation of
Arg-1/NOS-2 is a critical determinant in the pathogenesis of granuloma
formation.
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J. A. Van Ginderachter, S. Meerschaut, Y. Liu, L. Brys, K. De Groeve, G. Hassanzadeh Ghassabeh, G. Raes, and P. De Baetselier Peroxisome proliferator-activated receptor {gamma} (PPAR{gamma}) ligands reverse CTL suppression by alternatively activated (M2) macrophages in cancer Blood, July 15, 2006; 108(2): 525 - 535. [Abstract] [Full Text] [PDF]
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G. Hassanzadeh Ghassabeh, P. De Baetselier, L. Brys, W. Noel, J. A. Van Ginderachter, S. Meerschaut, A. Beschin, F. Brombacher, and G. Raes Identification of a common gene signature for type II cytokine-associated myeloid cells elicited in vivo in different pathologic conditions Blood, July 15, 2006; 108(2): 575 - 583. [Abstract] [Full Text] [PDF]
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 T. Nakano, H. Inoue, S. Fukuyama, K. Matsumoto, M. Matsumura, M. Tsuda, T. Matsumoto, H. Aizawa, and Y. Nakanishi Niflumic Acid Suppresses Interleukin-13-induced Asthma Phenotypes Am. J. Respir. Crit. Care Med., June 1, 2006; 173(11): 1216 - 1221. [Abstract] [Full Text] [PDF]
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L. Martin, M. Comalada, L. Marti, E. I. Closs, C. L. MacLeod, R. Martin del Rio, A. Zorzano, M. Modolell, A. Celada, M. Palacin, et al. Granulocyte-macrophage colony-stimulating factor increases L-arginine transport through the induction of CAT2 in bone marrow-derived macrophages Am J Physiol Cell Physiol, May 1, 2006; 290(5): C1364 - C1372. [Abstract] [Full Text] [PDF]
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A. Prasse, D. V. Pechkovsky, G. B. Toews, W. Jungraithmayr, F. Kollert, T. Goldmann, E. Vollmer, J. Muller-Quernheim, and G. Zissel A Vicious Circle of Alveolar Macrophages and Fibroblasts Perpetuates Pulmonary Fibrosis via CCL18 Am. J. Respir. Crit. Care Med., April 1, 2006; 173(7): 781 - 792. [Abstract] [Full Text] [PDF]
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S. Donnelly, S. M. O'Neill, M. Sekiya, G. Mulcahy, and J. P. Dalton Thioredoxin Peroxidase Secreted by Fasciola hepatica Induces the Alternative Activation of Macrophages Infect. Immun., January 1, 2005; 73(1): 166 - 173. [Abstract] [Full Text] [PDF]
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K. Kwong, R. A. Vaishnav, Y. Liu, N. Subhedar, A. J. Stromberg, M. L. Getchell, and T. V. Getchell Target ablation-induced regulation of macrophage recruitment into the olfactory epithelium of Mip-1{alpha}-/- mice and restoration of function by exogenous MIP-1{alpha} Physiol Genomics, December 15, 2004; 20(1): 73 - 86. [Abstract] [Full Text] [PDF]
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P. Misson, S. van den Brule, V. Barbarin, D. Lison, and F. Huaux Markers of macrophage differentiation in experimental silicosis J. Leukoc. Biol., November 1, 2004; 76(5): 926 - 932. [Abstract] [Full Text] [PDF]
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M. Kaviratne, M. Hesse, M. Leusink, A. W. Cheever, S. J. Davies, J. H. McKerrow, L. M. Wakefield, J. J. Letterio, and T. A. Wynn IL-13 Activates a Mechanism of Tissue Fibrosis That Is Completely TGF-{beta} Independent J. Immunol., September 15, 2004; 173(6): 4020 - 4029. [Abstract] [Full Text] [PDF]
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D. P. Beiting, S. K. Bliss, D. H. Schlafer, V. L. Roberts, and J. A. Appleton Interleukin-10 Limits Local and Body Cavity Inflammation during Infection with Muscle-Stage Trichinella spiralis Infect. Immun., June 1, 2004; 72(6): 3129 - 3137. [Abstract] [Full Text] [PDF]
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S. Duleu, P. Vincendeau, P. Courtois, S. Semballa, I. Lagroye, S. Daulouede, J.-L. Boucher, K. T. Wilson, B. Veyret, and A. P. Gobert Mouse Strain Susceptibility to Trypanosome Infection: An Arginase-Dependent Effect J. Immunol., May 15, 2004; 172(10): 6298 - 6303. [Abstract] [Full Text] [PDF]
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P. Kropf, M. A. Freudenberg, M. Modolell, H. P. Price, S. Herath, S. Antoniazi, C. Galanos, D. F. Smith, and I. Muller Toll-Like Receptor 4 Contributes to Efficient Control of Infection with the Protozoan Parasite Leishmania major Infect. Immun., April 1, 2004; 72(4): 1920 - 1928. [Abstract] [Full Text] [PDF]
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L. C. Gavrilescu, B. A. Butcher, L. Del Rio, G. A. Taylor, and E. Y. Denkers STAT1 Is Essential for Antimicrobial Effector Function but Dispensable for Gamma Interferon Production during Toxoplasma gondii Infection Infect. Immun., March 1, 2004; 72(3): 1257 - 1264. [Abstract] [Full Text] [PDF]
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M. Hesse, C. A. Piccirillo, Y. Belkaid, J. Prufer, M. Mentink-Kane, M. Leusink, A. W. Cheever, E. M. Shevach, and T. A. Wynn The Pathogenesis of Schistosomiasis Is Controlled by Cooperating IL-10-Producing Innate Effector and Regulatory T Cells J. Immunol., March 1, 2004; 172(5): 3157 - 3166. [Abstract] [Full Text] [PDF]
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S. El-Gayar, H. Thuring-Nahler, J. Pfeilschifter, M. Rollinghoff, and C. Bogdan Translational Control of Inducible Nitric Oxide Synthase by IL-13 and Arginine Availability in Inflammatory Macrophages J. Immunol., November 1, 2003; 171(9): 4561 - 4568. [Abstract] [Full Text] [PDF]
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N. G. Sandler, M. M. Mentink-Kane, A. W. Cheever, and T. A. Wynn Global Gene Expression Profiles During Acute Pathogen-Induced Pulmonary Inflammation Reveal Divergent Roles for Th1 and Th2 Responses in Tissue Repair J. Immunol., October 1, 2003; 171(7): 3655 - 3667. [Abstract] [Full Text] [PDF]
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A. C. La Flamme, K. Ruddenklau, and B. T. Backstrom Schistosomiasis Decreases Central Nervous System Inflammation and Alters the Progression of Experimental Autoimmune Encephalomyelitis Infect. Immun., September 1, 2003; 71(9): 4996 - 5004. [Abstract] [Full Text] [PDF]
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P. C. Rodriguez, A. H. Zea, J. DeSalvo, K. S. Culotta, J. Zabaleta, D. G. Quiceno, J. B. Ochoa, and A. C. Ochoa L-Arginine Consumption by Macrophages Modulates the Expression of CD3{zeta} Chain in T Lymphocytes J. Immunol., August 1, 2003; 171(3): 1232 - 1239. [Abstract] [Full Text] [PDF]
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Y. Liu, J. A. Van Ginderachter, L. Brys, P. De Baetselier, G. Raes, and A. B. Geldhof Nitric Oxide-Independent CTL Suppression during Tumor Progression: Association with Arginase-Producing (M2) Myeloid Cells J. Immunol., May 15, 2003; 170(10): 5064 - 5074. [Abstract] [Full Text] [PDF]
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L. Martinez-Pomares, D. M. Reid, G. D. Brown, P. R. Taylor, R. J. Stillion, S. A. Linehan, S. Zamze, S. Gordon, and S. Y. C. Wong Analysis of mannose receptor regulation by IL-4, IL-10, and proteolytic processing using novel monoclonal antibodies J. Leukoc. Biol., May 1, 2003; 73(5): 604 - 613. [Abstract] [Full Text] [PDF]
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M. G. Chiaramonte, M. Mentink-Kane, B. A. Jacobson, A. W. Cheever, M. J. Whitters, M. E.P. Goad, A. Wong, M. Collins, D. D. Donaldson, M. J. Grusby, et al. Regulation and Function of the Interleukin 13 Receptor {alpha} 2 During a T Helper Cell Type 2-dominant Immune Response J. Exp. Med., March 17, 2003; 197(6): 687 - 701. [Abstract] [Full Text] [PDF]
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D. M. Mosser The many faces of macrophage activation J. Leukoc. Biol., February 1, 2003; 73(2): 209 - 212. [Full Text] [PDF]
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C. Stempin, L. Giordanengo, S. Gea, and F. Cerban Alternative activation and increase of Trypanosoma cruzi survival in murine macrophages stimulated by cruzipain, a parasite antigen J. Leukoc. Biol., October 1, 2002; 72(4): 727 - 734. [Abstract] [Full Text] [PDF]
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A. Mencacci, C. Montagnoli, A. Bacci, E. Cenci, L. Pitzurra, A. Spreca, M. Kopf, A. H. Sharpe, and L. Romani CD80+Gr-1+ Myeloid Cells Inhibit Development of Antifungal Th1 Immunity in Mice with Candidiasis J. Immunol., September 15, 2002; 169(6): 3180 - 3190. [Abstract] [Full Text] [PDF]
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