The relevance of the migration inhibitory factor (MIF) for peripheral tissue response in murine sublethal systemic Aspergillus fumigatus infection

References

• Romani L. Immunity to fungal infections. Nat Rev Immunol 2011; 11: 275–288.
   PubMed Web of Science ®Google Scholar
• Carneiro-Sampaio M, Coutinho A. Immunity to microbes: lessons from primary immunodeficiencies. Infect Immun 2007; 75: 1545–1555.
   PubMed Web of Science ®Google Scholar
• Mircescu MM, Lipuma L, van Rooijen N, Pamer EG, Hohl TM. Essential role for neutrophils but not alveolar macrophages at early time points following Aspergillus fumigatus infection. J Infect Dis 2009; 200: 647–656.
   PubMed Web of Science ®Google Scholar
• Mirkov I, Stojanovic I, Stosic-Grujicic S, . Splenic and lung response to nonlethal systemic Aspergillus fumigatus infection in C57BL/6 mice. Med Mycol 2010; 48: 735–743.
   PubMed Web of Science ®Google Scholar
• Cenci E, Mencacci A, d'Ostiani CF, . Cytokine- and T helper-dependent lung mucosal immunity in mice with invasive pulmonary aspergillosis. J Infect Dis 1998; 178: 1750–1760.
   PubMed Web of Science ®Google Scholar
• Hebart H, Bollinger C, Fisch P, . Analysis of T-cell responses to Aspergillus fumigatus antigens in healthy individuals and patients with hematologic malignancies. Blood 2002; 100: 4521–4528.
   PubMed Web of Science ®Google Scholar
• Curtis MM, Way SS. Interleukin-17 in host defense against bacterial, mycobacterial and fungal pathogens. Immunology 2009; 126: 177–185.
   PubMed Web of Science ®Google Scholar
• Bloom BR, Bennett B. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 1966; 153: 80–82.
   PubMed Web of Science ®Google Scholar
• David JR. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci USA 1966; 56: 72–77.
   PubMed Web of Science ®Google Scholar
• Rocklin RE, Meyers OL, David JR. An in vitro assay for cellular hypersensitivity in man. J Immunol 1970; 104: 95–102.
   PubMed Web of Science ®Google Scholar
• Rocklin RE, MacDermott RP, Chess L, Schlossman SF, David JR. Studies on mediator production by highly purified human T and B lymphocytes. J Exp Med 1974; 140: 1303–1316.
   PubMed Web of Science ®Google Scholar
• Weiser WY, Pozzi LM, David JR. Human recombinant migration inhibitory factor activates human macrophages to kill Leishmania donovani. J Immunol 1991; 147: 2006–2011.
   PubMed Web of Science ®Google Scholar
• Lue H, Kleemann R, Calandra T, Roger T, Bernhagen J. Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect 2002; 4: 449–460.
   PubMed Web of Science ®Google Scholar
• Calandra T, Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 2003; 3: 791–800.
   PubMed Web of Science ®Google Scholar
• Bacher M, Meinhardt A, Lan HY, . Migration inhibitory factor expression in experimentally induced endotoxemia. Am J Pathol 1997; 150: 235–246.
   PubMed Web of Science ®Google Scholar
• Cvetkovic I, Stosic-Grujicic S. Neutralization of macrophage migration inhibitory factor – novel approach for the treatment of immunoinflammatory disorders. Int Immunopharmac 2006; 6: 1527–1534.
   PubMed Web of Science ®Google Scholar
• Cooke G, Armstrong ME, Donnelly SC. Macrophage migration inhibitory factor (MIF), enzymatic activity and the inflammatory response. Biofactors 2009; 35: 165–168.
   PubMed Web of Science ®Google Scholar
• Calandra T, Bucala R. Macrophage migration inhibitory factor (MIF). A glucocorticoid counter-regulator within the immune system. Crit Rev Immunol 1997; 17: 77–88.
   PubMed Web of Science ®Google Scholar
• Stojanovic I, Cvjeticanin T, Lazaroski S, Stosic-Grujicic S, Miljkovic DJ. Macrophage migration inhibitory factor stimulates interleukin-17 expression and production in lymph node cells. Immunology 2009; 126: 74–83.
   PubMed Web of Science ®Google Scholar
• Leng L, Metz CN, Fang Y, . MIF signal transduction initiated by binding to CD74. J Exp Med 2003; 197:1467–1476.
   PubMed Web of Science ®Google Scholar
• Bernhagen J, Krohn R, Lue H, . MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 2007; 13: 587–596.
   PubMed Web of Science ®Google Scholar
• Tarnowski M, Grymula K, Liu R, . Macrophage migration inhibitory factor is secreted by rhabdomyosarcoma cells, modulates tumor metastasis by binding to CXCR4 and CXCR7 receptors and inhibits recruitment of cancer-associated fibroblasts. Mol Cancer Res 2010; 8: 1328–1343.
   PubMed Web of Science ®Google Scholar
• Fan H, Hall P, Santos LL, . Macrophage migration inhibitory factor and CD74 regulate macrophage chemotactic responses via MAPK and Rho GTPase. J Immunol 2011; 186: 4915–4924.
   PubMed Web of Science ®Google Scholar
• Leng L, Chen L, Fan J, . A small-molecule macrophage migration inhibitory factor antagonist protects against glomerulonephritis in lupus-prone NZB/NZW F1 and MRL/lpr mice. J Immunol 2011; 186: 527–538.
   PubMed Web of Science ®Google Scholar
• Lue H, Dewor M, Leng L, Bucala R, Bernhagen J. Activation of the JNK signaling pathway by macrophage migration inhibitory factor (MIF) and dependence on CXCR4 and CD74. Cell Signal 2011; 23: 135–144.
   PubMed Web of Science ®Google Scholar
• Calandra T. Macrophage migration inhibitory factor and host innate immune responses to microbes. Scand J Infect Dis 2003; 35: 573–576.
   PubMed Web of Science ®Google Scholar
• Wiersinga WJ, Calandra T, Kager LM, . Expression and function of macrophage migration inhibitory factor (MIF) in melioidosis. PLoS Negl Trop Dis 2010; 4: e605.
   Google Scholar
• Chuang CC, Chuang YC, Chang WT, . Macrophage migration inhibitory factor regulates interleukin-6 production by facilitating nuclear factor-kappa B activation during Vibrio vulnificus infection. BMC Immunol 2010; 11: 50.
   PubMed Web of Science ®Google Scholar
• Terrazas CA, Juarez I, Terrazas LI, . Toxoplasma gondii: impaired maturation and pro-inflammatory response of dendritic cells in MIF-deficient mice favors susceptibility to infection. Exp Parasitol 2010; 126: 348–358.
   PubMed Web of Science ®Google Scholar
• Malu DT, Bélanger B, Desautels F, . Macrophage migration inhibitory factor: a downregulator of early T cell-dependent IFN-γ responses in Plasmodium chabaudi adami (556 KA)-infected mice. J Immunol 2011; 186: 6271–6279.
   PubMed Web of Science ®Google Scholar
• Assuncao-Miranda I, Amaral FA, Bozza FA, . Contribution of macrophage migration inhibitory factor to the pathogenesis of dengue virus infection. FASEB J 2010; 24: 218–228.
   PubMed Web of Science ®Google Scholar
• Chuang YC, Lei HY, Liu HS, . Macrophage migration inhibitory factor induced by dengue virus infection increases vascular permeability. Cytokine 2011; 54: 222–223.
   PubMed Web of Science ®Google Scholar
• Hou XQ, Gao YW, Yang ST, . Role of macrophage migration inhibitory factor in influenza H5N1 virus pneumonia. Acta Virol 2009; 53: 225–231.
   PubMed Web of Science ®Google Scholar
• Defaveri J, Rezkallah-Iwasso MT, Franco MF. Pulmonary paracoccidioidomycosis in immunized mice. Mycopathologia 1992; 119: 1–9.
   PubMed Web of Science ®Google Scholar
• Tewari RP, Von Behren LA. Immune responses in histoplasmosis, a prototype of respiratory mycoses. Indian J Chest Dis Allied Sci 2000; 42: 265–269.
   PubMedGoogle Scholar
• Tanuma H, Asai T, Abe M, Nishiyama S, Katsuoka K. Case report. Lymphatic vessel-type sporotrichosis: immunohistochemical evaluation and cytokine expression pattern. Mycoses 2001; 44: 316–320.
   PubMed Web of Science ®Google Scholar
• Graybill JR, Ahrens J, Nealon T, Paque R. Pulmonary cryptococcosis in the rat. Am Rev Respir Dis 1983; 127: 636–640.
   PubMedGoogle Scholar
• Singh S, Kochhar R, Duta U. Severe duodenal candidiasis in a patient with IgA deficiency and T cell defects. Indian J Gastroenterol 1990; 9: 95–96.
   PubMedGoogle Scholar
• Nicolo C, Le Roy D, Reymond MK, Roger T, Calandra T. Macrophage migration inhibitory factor plays an important role in the host innate immune defenses against Candida infection. Int J Infect Dis 2006; 10: S46–47.
   Web of Science ®Google Scholar
• Krysińska-Traczyk E, Dutkiewicz J. Aspergillus candidus: a respiratory hazard associated with grain dust. Ann Agric Environ Med 2000; 7: 101–109.
   PubMed Web of Science ®Google Scholar
• Stojanovic I, Mirkov I, Kataranovski M, Glamoclija J, Stosic-Grujicic S. A role for macrophage migration inhibitory factor in protective immunity against Aspergillus fumigatus. Immunobiology 2011; 216: 1018–1027.
   PubMed Web of Science ®Google Scholar
• Cenci E, Perito S, Enssle KH, . Th1 and Th2 cytokines in mice with invasive aspergillosis. Infect Immun 1997; 65: 564–570.
   PubMed Web of Science ®Google Scholar
• Mirkov I, Zolotarevski L, Glamoclija J, Kataranovski D, Kataranovski M. Experimental disseminated aspergillosis in mice: histopathological study. J Mycol Med 2008; 18: 75–82.
   Web of Science ®Google Scholar
• Marr KA, Patterson T, Denning D. Aspergillosis. Pathogenesis, clinical manifestations, and therapy. Infect Dis Clin North Am 2002; 16: 875–894.
   PubMed Web of Science ®Google Scholar
• Armstrong-James DPH, Turnbull SA, Teo I, . Impaired interferon-γ responses, increased interleukin-17 expression, and a tumor necrosis factor-α transcriptional program in invasive aspergillosis. J Infect Dis 2009; 200: 1341–1351.
   PubMed Web of Science ®Google Scholar
• Fingerle-Rowson G, Petrenko O, Metz CN, . The p53-dependent effects of macrophage migration inhibitory factor revealed by gene targeting. Proc Natl Acad Sci USA 2003; 100: 9354–9359.
   PubMed Web of Science ®Google Scholar
• Kataranovski M, Mirkov I, Belij S, . Lungs: remote inflammatory target of systemic cadmium administration in rats. Environ Toxicol Pharmacol 2009; 28: 225–231.
   PubMed Web of Science ®Google Scholar
• Orciuolo E, Stanzani M, Canestraro M, . Effects of Aspergillus fumigatus gliotoxin and methylprednisolone on human neutrophils: implications for the pathogenesis of invasive aspergillosis. J Leukoc Biol 2007; 82: 839–848.
   PubMed Web of Science ®Google Scholar
• Crispe IN. The liver as a lymphoid organ. Annu Rev Immunol 2009; 27: 143–163.
   Web of Science ®Google Scholar
• Bernhagen J, Krohn R, Lue H, . MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 2007; 13: 587–59.
   PubMed Web of Science ®Google Scholar
• Santos LL, Fan H, Hall P, . Macrophage migration inhibitory factor regulates neutrophil chemotactic responses in inflammatory arthritis in mice. Arthritis Rheum 2011; 63: 960–970.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Koga K, Linge HM, . Macrophage CD74 contributes to MIF-induced pulmonary inflammation. Respir Res 2009; 10: 33.
   PubMed Web of Science ®Google Scholar
• Ulich TR, Del Castillo J, Keys M, . Kinetics and mechanisms of recombinant human interleukin-1 and tumor necrosis factor-α-induced changes in circulating numbers of neutrophils and lymphocytes. JImmunol 1987; 139: 3406–3415.
   PubMed Web of Science ®Google Scholar
• Ulich TR, Del Castillo J, Guo K. In vivo hematologic efects of recombinant interleukin-6 on hematopoiesis and circulating numbers of RBCs and WBCs. Blood 1989; 73: 108–110.
   PubMed Web of Science ®Google Scholar
• Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 2006; 6: 173-182.
   PubMed Web of Science ®Google Scholar
• Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol 2003; 15: 247–254.
   PubMed Web of Science ®Google Scholar
• Segal BH. Aspergillosis. N Engl J Med 2009; 360: 1870–1884.
   PubMed Web of Science ®Google Scholar
• Brown GD. Innate antifungal immunity: the key role of phagocytes. Annu Rev Immunol 2011; 29: 1–21.
   Google Scholar
• Cramer RA, Rivera A, Hohl TM. Immune responses against Aspergillus fumigatus: what have we learned? Curr Opin Infect Dis 2011; 24: 315–322.
   Google Scholar
• Onodera S, Suzuki K, Matsuno T, . Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion. Immunology 1997; 92: 131–137.
   PubMed Web of Science ®Google Scholar
• Park SJ, Hughes MA, Burdick M, Strieter RM, Mehrad B. Early NK cell-derived IFN-γ is essential to host defense in neutropenic invasive aspergillosis. J Immunol 2009; 182: 4306–4312.
   PubMed Web of Science ®Google Scholar
• Bouzani M, Ok M, McKormick A, . Human NK cells display important antifungal activity against Aspergillus fumigatus, which is directly mediated by IFN-γ release. J Immunol 2011; 187: 1369–1376.
   PubMed Web of Science ®Google Scholar
• Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M. Interleukin-17-producing γδ T cells selectively expand in response to pathogen products and environmental signals. Immunity 2009; 31: 321–330.
   PubMed Web of Science ®Google Scholar
• Xu S, Cao X. Interleukin-17 and its expanding biological functions. Cell Mol Immunol 2010; 7: 164–174.
   PubMed Web of Science ®Google Scholar
• Lin AM, Rubin CJ, Khandpur R, . Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol 2011; 187: 490–500.
   PubMed Web of Science ®Google Scholar