STAT6-/- mice exhibit decreased cells with alternatively activated macrophage phenotypes and enhanced disease severity in murine neurocysticercosis

Journal of Neuroimmunology

Volumn 232, Issue 1-2, 2011, Pages 26-34

  Mishra, Bibhuti B ^a   Gundra, Uma Mahesh ^a   Teale, Judy M ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

Alternatively activated macrophages; CNS; Helminth; Neurocysticercosis; STAT6

Indexed keywords

ARGINASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; STAT6 PROTEIN; STAT6 PROTEIN, MOUSE;

ALTERNATIVELY ACTIVATED MACROPHAGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN LEVEL; CELL ACTIVATION; CELL ACTIVITY; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HISTOLOGY; IMMUNOFLUORESCENCE TEST; INFECTION CONTROL; INFECTION SENSITIVITY; MESOCESTOIDEA; MOUSE; NEUROCYSTICERCOSIS; NEUROPATHOLOGY; NONHUMAN; PARASITE LOAD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; RNA ISOLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BRAIN DISEASE; C57BL MOUSE; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOLOGY; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE MUTANT; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BRAIN DISEASES; DISEASE MODELS, ANIMAL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROCYSTICERCOSIS; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAT6 TRANSCRIPTION FACTOR;

EID: 79952247491     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2010.09.029     Document Type: Article

References (69)

1. Alvarez J.I., Teale J.M. Differential changes in junctional complex proteins suggest the ependymal lining as the main source of leukocyte infiltration into ventricles in murine neurocysticercosis. J. Neuroimmunol. 2007, 187:102-113.
2. Alvarez J.I., Teale J.M. Evidence for differential changes of junctional complex proteins in murine neurocysticercosis dependent upon CNS vasculature. Brain Res. 2007, 1169:98-111.
3. Alvarez J.I., Rivera J., Teale J.M. Differential release and phagocytosis of tegument glycoconjugates in neurocysticercosis: implications for immune evasion strategies. PLoS Negl. Trop. Dis. 2008, 2:e218.
4. Alvarez J.I., Mishra B.B., Gundra U.M., Mishra P.K., Teale J.M. Mesocestoides corti intracranial infection as a murine model for neurocysticercosis. Parasitology 2010, 137:359-372.
5. Anthony R.M., Urban J.F., Alem F., Hamed H.A., Rozo C.T., Boucher J.L., Van Rooijen N., Gause W.C. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 2006, 12:955-960.
6. Atochina O., Da'dara A.A., Walker M., Harn D.A. The immunomodulatory glycan LNFPIII initiates alternative activation of murine macrophages in vivo. Immunology 2008, 125:111-121.
7. Brosnan C.F., Battistini L., Raine C.S., Dickson D.W., Casadevall A., Lee S.C. Reactive nitrogen intermediates in human neuropathology: an overview. Dev. Neurosci. 1994, 16:152-161.
8. Cardona A.E., Teale J.M. Gamma/delta T cell-deficient mice exhibit reduced disease severity and decreased inflammatory response in the brain in murine neurocysticercosis. J. Immunol. 2002, 169:3163-3171.
9. Cardona A.E., Restrepo B.I., Jaramillo J.M., Teale J.M. Development of an animal model for neurocysticercosis: immune response in the central nervous system is characterized by a predominance of gamma delta T cells. J. Immunol. 1999, 162:995-1002.
10. Cardona A.E., Gonzalez P.A., Teale J.M. CC chemokines mediate leukocyte trafficking into the central nervous system during murine neurocysticercosis: role of gamma delta T cells in amplification of the host immune response. Infect. Immun. 2003, 71:2634-2642.
11. Chao C.C., Hu S., Molitor T.W., Shaskan E.G., Peterson P.K. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Immunol. 1992, 149:2736-2741.
12. Chavarria A., Alcocer-Varela J. Is damage in central nervous system due to inflammation?. Autoimmun. Rev. 2004, 3:251-260.
13. Chomarat P., Banchereau J. Interleukin-4 and interleukin-13: their similarities and discrepancies. Int. Rev. Immunol. 1998, 17:1-52.
14. Correa D., Dalma D., Espinoza B., Plancarte A., Rabiela M.T., Madrazo I., Gorodezky C., Flisser A. Heterogeneity of humoral immune components in human cysticercosis. J. Parasitol. 1985, 71:535-541.
15. Davis L.E., Kornfeld M. Neurocysticercosis: neurologic, pathogenic, diagnostic and therapeutic aspects. Eur. Neurol. 1991, 31:229-240.
16. Finkelman F.D., Shea-Donohue T., Morris S.C., Gildea L., Strait R., Madden K.B., Schopf L., Urban J.F. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 2004, 201:139-155.
17. Gause W.C., Urban J.F., Stadecker M.J. The immune response to parasitic helminths: insights from murine models. Trends Immunol. 2003, 24:269-277.
18. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
19. Grewal J.S., Kaur S., Bhatti G., Ganguly N.K., Mahajan R.C., Malla N. Kinetics of humoral & cellular immune responses in experimental cysticercosis in pigs infected with Taenia solium. Indian J. Med. Res. 2000, 111:43-49.
20. Harn D.A., McDonald J., Atochina O., Da'dara A.A. Modulation of host immune responses by helminth glycans. Immunol. Rev. 2009, 230:247-257.
21. Hesse M., Modolell M., La Flamme A.C., Schito M., Fuentes J.M., Cheever A.W., Pearce E.J., Wynn T.A. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol. 2001, 167:6533-6544.
22. Joshi A.D., Raymond T., Coelho A.L., Kunkel S.L., Hogaboam C.M. A systemic granulomatous response to Schistosoma mansoni eggs alters responsiveness of bone-marrow-derived macrophages to Toll-like receptor agonists. J. Leukoc. Biol. 2008, 83:314-324.
23. Keegan A.D., Johnston J.A., Tortolani P.J., McReynolds L.J., Kinzer C., O'Shea J.J., Paul W.E. Similarities and differences in signal transduction by interleukin 4 and interleukin 13: analysis of Janus kinase activation. Proc. Natl Acad. Sci. USA 1995, 92:7681-7685.
24. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 2009, 29:13435-13444.
25. Kreider T., Anthony R.M., Urban J.F., Gause W.C. Alternatively activated macrophages in helminth infections. Curr. Opin. Immunol. 2007, 19:448-453.
26. Lehnardt S., Henneke P., Lien E., Kasper D.L., Volpe J.J., Bechmann I., Nitsch R., Weber J.R., Golenbock D.T., Vartanian T. A mechanism for neurodegeneration induced by group B streptococci through activation of the TLR2/MyD88 pathway in microglia. J. Immunol. 2006, 177:583-592.
27. Leonard W.J., O'Shea J.J. Jaks and STATs: biological implications. Annu. Rev. Immunol. 1998, 16:293-322.
28. Lumeng C.N., Bodzin J.L., Saltiel A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 2007, 117:175-184.
29. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25:677-686.
30. Mantovani A., Sica A., Locati M. Macrophage polarization comes of age. Immunity 2005, 23:344-346.
31. Mantovani A., Sica A., Locati M. New vistas on macrophage differentiation and activation. Eur. J. Immunol. 2007, 37:14-16.
32. Martin P., Leibovich S.J. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol. 2005, 15:599-607.
33. Martinez F.O., Gordon S., Locati M., Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 2006, 177:7303-7311.
34. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008, 13:453-461.
35. Martinez F.O., Helming L., Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 2009, 27:451-483.
36. Mishra B.B., Mishra P.K., Teale J.M. Expression and distribution of Toll-like receptors in the brain during murine neurocysticercosis. J. Neuroimmunol. 2006, 181:46-56.
37. Mishra B.B., Gundra U.M., Teale J.M. Expression and distribution of Toll-like receptors 11-13 in the brain during murine neurocysticercosis. J. Neuroinflammation 2008, 5:53.
38. Mishra B.B., Gundra U.M., Wong K., Teale J.M. MyD88-deficient mice exhibit decreased parasite induced immune responses but reduced disease severity in a murine model of neurocysticercosis. Infect. Immun. 2009, 77(12):5369-5379.
39. Modolell M., Corraliza I.M., Link F., Soler G., Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur. J. Immunol. 1995, 25:1101-1104.
40. Mosser D.M. The many faces of macrophage activation. J. Leukoc. Biol. 2003, 73:209-212.
41. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8:958-969.
42. Moy F.J., Diblasio E., Wilhelm J., Powers R. Solution structure of human IL-13 and implication for receptor binding. J. Mol. Biol. 2001, 310:219-230.
43. Munder M., Eichmann K., Modolell M. Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype. J. Immunol. 1998, 160:5347-5354.
44. Nash T.E., Singh G., White A.C., Rajshekhar V., Loeb J.A., Proano J.V., Takayanagui O.M., Gonzalez A.E., Butman J.A., DeGiorgio C., Del Brutto O.H., Delgado-Escueta A., Evans C.A., Gilman R.H., Martinez S.M., Medina M.T., Pretell E.J., Teale J., Garcia H.H. Treatment of neurocysticercosis: current status and future research needs. Neurology 2006, 67:1120-1127.
45. Nathan C., Shiloh M.U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl Acad. Sci. USA 2000, 97:8841-8848.
46. Nauta A.J., Raaschou-Jensen N., Roos A., Daha M.R., Madsen H.O., Borrias-Essers M.C., Ryder L.P., Koch C., Garred P. Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur. J. Immunol. 2003, 33:2853-2863.
47. Nelms K., Keegan A.D., Zamorano J., Ryan J.J., Paul W.E. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 1999, 17:701-738.
48. Noel W., Raes G., Hassanzadeh Ghassabeh G., De Baetselier P., Beschin A. Alternatively activated macrophages during parasite infections. Trends Parasitol. 2004, 20:126-133.
49. Obiri N.I., Debinski W., Leonard W.J., Puri R.K. Receptor for interleukin 13. Interaction with interleukin 4 by a mechanism that does not involve the common gamma chain shared by receptors for interleukins 2, 4, 7, 9, and 15. J. Biol. Chem. 1995, 270:8797-8804.
50. Obiri N.I., Murata T., Debinski W., Puri R.K. Modulation of interleukin (IL)-13 binding and signaling by the gammac chain of the IL-2 receptor. J. Biol. Chem. 1997, 272:20251-20258.
51. O'Connell A.E., Kerepesi L.A., Vandergrift G.L., Herbert D.R., TJ V.A.N.W., Hooper D.C., Pearce E.J., Abraham D. IL-4(-/-) mice with lethal Mesocestoides corti infections-reduced Th2 cytokines and alternatively activated macrophages. Parasite Immunol. 2009, 31:741-749.
52. Pauleau A.L., Rutschman R., Lang R., Pernis A., Watowich S.S., Murray P.J. Enhancer-mediated control of macrophage-specific arginase I expression. J. Immunol. 2004, 172:7565-7573.
53. Pesce J.T., Ramalingam T.R., Mentink-Kane M.M., Wilson M.S., El Kasmi K.C., Smith A.M., Thompson R.W., Cheever A.W., Murray P.J., Wynn T.A. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 2009, 5:e1000371.
54. Pesce J.T., Ramalingam T.R., Wilson M.S., Mentink-Kane M.M., Thompson R.W., Cheever A.W., Urban J.F., Wynn T.A. Retnla (relmalpha/fizz1) suppresses helminth-induced Th2-type immunity. PLoS Pathog. 2009, 5:e1000393.
55. Raes G., Brys L., Dahal B.K., Brandt J., Grooten J., Brombacher F., Vanham G., Noel W., Bogaert P., Boonefaes T., Kindt A., Van den Bergh R., Leenen P.J., De Baetselier P., Ghassabeh G.H. Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J. Leukoc. Biol. 2005, 77:321-327.
56. Reece J.J., Siracusa M.C., Scott A.L. Innate immune responses to lung-stage helminth infection induce alternatively activated alveolar macrophages. Infect. Immun. 2006, 74:4970-4981.
57. Restrepo B.I., Llaguno P., Sandoval M.A., Enciso J.A., Teale J.M. Analysis of immune lesions in neurocysticercosis patients: central nervous system response to helminth appears Th1-like instead of Th2. J. Neuroimmunol. 1998, 89:64-72.
58. Restrepo B.I., Alvarez J.I., Castano J.A., Arias L.F., Restrepo M., Trujillo J., Colegial C.H., Teale J.M. Brain granulomas in neurocysticercosis patients are associated with a Th1 and Th2 profile. Infect. Immun. 2001, 69:4554-4560.
59. Reyes J.L., Terrazas L.I. The divergent roles of alternatively activated macrophages in helminthic infections. Parasite Immunol. 2007, 29:609-619.
60. Saba K., Denda-Nagai K., Irimura T. A C-type lectin MGL1/CD301a plays an anti-inflammatory role in murine experimental colitis. Am. J. Pathol. 2009, 174:144-152.
61. Sato K., Imai Y., Higashi N., Kumamoto Y., Onami T.M., Hedrick S.M., Irimura T. Lack of antigen-specific tissue remodeling in mice deficient in the macrophage galactose-type calcium-type lectin 1/CD301a. Blood 2005, 106:207-215.
62. Sciutto E., Chavarria A., Fragoso G., Fleury A., Larralde C. The immune response in Taenia solium cysticercosis: protection and injury. Parasite Immunol. 2007, 29:621-636.
63. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 1992, 176:287-292.
64. Terrazas L.I. The complex role of pro- and anti-inflammatory cytokines in cysticercosis: immunological lessons from experimental and natural hosts. Curr. Top. Med. Chem. 2008, 8:383-392.
65. Umemura N., Saio M., Suwa T., Kitoh Y., Bai J., Nonaka K., Ouyang G.F., Okada M., Balazs M., Adany R., Shibata T., Takami T. Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics. J. Leukoc. Biol. 2008, 83:1136-1144.
66. Urban J.F., Noben-Trauth N., Donaldson D.D., Madden K.B., Morris S.C., Collins M., Finkelman F.D. IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 1998, 8:255-264.
67. van Riet E., Hartgers F.C., Yazdanbakhsh M. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 2007, 212:475-490.
68. Voehringer D., van Rooijen N., Locksley R.M. Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J. Leukoc. Biol. 2007, 81:1434-1444.
69. White A.C. Neurocysticercosis: updates on epidemiology, pathogenesis, diagnosis, and management. Annu. Rev. Med. 2000, 51:187-206.