IL-12p40 Deficiency Leads to Uncontrolled Trypanosoma cruzi Dissemination in the Spinal Cord Resulting in Neuronal Death and Motor Dysfunction

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Bombeiro, André Luis ^a   Gonçalves, Lígia Antunes ^b   Penha Gonçalves, Carlos ^b   Marinho, Claudio Romero Farias ^a   D'Império Lima, Maria Regina ^a   Chadi, Gerson ^a   Álvarez, José Maria ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; CD3 ANTIGEN; GAMMA INTERFERON; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12P40; MESSENGER RNA; RNA 18S; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DENSITY; CHAGAS DISEASE; CONTROLLED STUDY; DEMYELINATION; DISEASE MODEL; FEMALE; FORELIMB; KNOCKOUT MOUSE; MACROPHAGE; MICROGLIA; MOTOR DYSFUNCTION; MOUSE; MYELITIS; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPATHOLOGY; NITROSYLATION; NONHUMAN; PARALYSIS; PARASITE CLEARANCE; PARASITE LOAD; PARASITE TRANSMISSION; PROTEIN DEFICIENCY; QUANTITATIVE ANALYSIS; SPINAL CORD; TRYPANOSOMA CRUZI; WILD TYPE;

ANIMALS; CELL DEATH; CHAGAS DISEASE; DISEASE MODELS, ANIMAL; FEMALE; GLIOSIS; HUMANS; INTERLEUKIN-12 SUBUNIT P40; MACROPHAGES; MICE; MICE, KNOCKOUT; MICROGLIA; MOTOR ACTIVITY; MYELITIS; NERVE DEGENERATION; SPINAL CORD; TRYPANOSOMA CRUZI;

MUS; TRYPANOSOMA CRUZI;

EID: 84869049629     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049022     Document Type: Article

References (53)

1. Morel CM, Lazdins J, (2003) Chagas disease. Nat Rev Microbiol 1: 14-15.
2. Rassi A Jr, Rassi A, Marin-Neto JA, (2010) Chagas disease. Lancet 375: 1388-1402.
3. Junqueira C, Caetano B, Bartholomeu DC, Melo MB, Ropert C, et al. (2010) The endless race between Trypanosoma cruzi and host immunity: lessons for and beyond Chagas disease. Expert Rev Mol Med 12: e29.
4. Benitez-Hernandez I, Mendez-Enriquez E, Ostoa P, Fortoul T, Ramirez JA, et al. (2010) Proteolytic cleavage of chemokines by Trypanosoma cruzi's cruzipain inhibits chemokine functions by promoting the generation of antagonists. Immunobiology 215: 413-426.
5. Erdmann H, Steeg C, Koch-Nolte F, Fleischer B, Jacobs T (2009) Sialylated ligands on pathogenic Trypanosoma cruzi interact with Siglec-E (sialic acid-binding Ig-like lectin-E). Cell Microbiol 11.
6. Hoff R, Teixeira RS, Carvalho JS, Mott KE, (1978) Trypanosoma cruzi in the cerebrospinal fluid during the acute stage of Chagas' disease. N Engl J Med 298: 604-606.
7. Marchiori PE, Alexandre PL, Britto N, Patzina RA, Fiorelli AA, et al. (2007) Late reactivation of Chagas' disease presenting in a recipient as an expansive mass lesion in the brain after heart transplantation of chagasic myocardiopathy. J Heart Lung Transplant 26: 1091-1096.
8. Rocha A, de Meneses AC, da Silva AM, Ferreira MS, Nishioka SA, et al. (1994) Pathology of patients with Chagas' disease and acquired immunodeficiency syndrome. Am J Trop Med Hyg 50: 261-268.
9. Michailowsky V, Silva NM, Rocha CD, Vieira LQ, Lannes-Vieira J, et al. (2001) Pivotal role of interleukin-12 and interferon-gamma axis in controlling tissue parasitism and inflammation in the heart and central nervous system during Trypanosoma cruzi infection. Am J Pathol 159: 1723-1733.
10. Marinho CR, Nunez-Apaza LN, Martins-Santos R, Bastos KR, Bombeiro AL, et al. (2007) IFN-gamma, but not nitric oxide or specific IgG, is essential for the in vivo control of low-virulence Sylvio X10/4 Trypanosoma cruzi parasites. Scand J Immunol 66: 297-308.
11. Bombeiro AL, D'Imperio Lima MR, Chadi G, Alvarez JM, (2010) Neurodegeneration and increased production of nitrotyrosine, nitric oxide synthase, IFN-gamma and S100beta protein in the spinal cord of IL-12p40-deficient mice infected with Trypanosoma cruzi. Neuroimmunomodulation 17: 67-78.
12. Aloisi F, (2001) Immune function of microglia. Glia 36: 165-179.
13. Dong Y, Benveniste EN, (2001) Immune function of astrocytes. Glia 36: 180-190.
14. Hendriks JJ, Teunissen CE, de Vries HE, Dijkstra CD, (2005) Macrophages and neurodegeneration. Brain Res Brain Res Rev 48: 185-195.
15. Brown GC, (2007) Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem Soc Trans 35: 1119-1121.
16. Foran E, Trotti D (2009) Glutamate Transporters and the Excitotoxic Path to Motor Neuron Degeneration in Amyotrophic Lateral Sclerosis. Antioxid Redox Signal.
17. Cooper AM, Magram J, Ferrante J, Orme IM, (1997) Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with mycobacterium tuberculosis. J Exp Med 186: 39-45.
18. Miles MA, (1974) Letter: Cloning Trypanosoma cruzi. Trans R Soc Trop Med Hyg 68: 256.
19. Becher B, Durell BG, Noelle RJ, (2002) Experimental autoimmune encephalitis and inflammation in the absence of interleukin-12. J Clin Invest 110: 493-497.
20. Rivlin AS, Tator CH, (1977) Objective clinical assessment of motor function after experimental spinal cord injury in the rat. J Neurosurg 47: 577-581.
21. West MJ, Gundersen HJ, (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296: 1-22.
22. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, et al. (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis 96: 379-394.
23. Chadi G, Gomide VC, (2004) FGF-2 and S100beta immunoreactivities increase in reactive astrocytes, but not in microglia, in ascending dopamine pathways following a striatal 6-OHDA-induced partial lesion of the nigrostriatal system. Cell Biol Int 28: 849-861.
24. Postan M, McDaniel JP, Dvorak JA, (1987) Comparative studies of the infection of Lewis rats with four Trypanosoma cruzi clones. Trans R Soc Trop Med Hyg 81: 415-419.
25. Petray P, Castanos-Velez E, Grinstein S, Orn A, Rottenberg ME, (1995) Role of nitric oxide in resistance and histopathology during experimental infection with Trypanosoma cruzi. Immunol Lett 47: 121-126.
26. Chagas C, (1909) Nova tripanozomiase humana: Estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Memorias do Instituto Oswaldo Cruz 1: 159-218.
27. Cordova E, Boschi A, Ambrosioni J, Cudos C, Corti M (2008) Reactivation of Chagas disease with central nervous system involvement in HIV-infected patients in Argentina, 1992-2007. Int J Infect Dis.
28. Rosemberg S, Chaves CJ, Higuchi ML, Lopes MB, Castro LH, et al. (1992) Fatal meningoencephalitis caused by reactivation of Trypanosoma cruzi infection in a patient with AIDS. Neurology 42: 640-642.
29. Leiguarda R, Roncoroni A, Taratuto AL, Jost L, Berthier M, et al. (1990) Acute CNS infection by Trypanosoma cruzi (Chagas' disease) in immunosuppressed patients. Neurology 40: 850-851.
30. Jardim E, Takayanagui OM, (1994) Chagasic meningoencephalitis with detection of Trypanosoma cruzi in the cerebrospinal fluid of an immunodepressed patient. J Trop Med Hyg 97: 367-370.
31. Marinho CR, Nunez-Apaza LN, Bortoluci KR, Bombeiro AL, Bucci DZ, et al. (2009) Infection by the Sylvio X10/4 clone of Trypanosoma cruzi: relevance of a low-virulence model of Chagas' disease. Microbes Infect 11: 1037-1045.
32. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, et al. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
33. da Matta Guedes PM, Gutierrez FR, Maia FL, Milanezi CM, Silva GK, et al. (2010) IL-17 produced during Trypanosoma cruzi infection plays a central role in regulating parasite-induced myocarditis. PLoS Negl Trop Dis 4: e604.
34. Miyazaki Y, Hamano S, Wang S, Shimanoe Y, Iwakura Y, et al. (2010) IL-17 is necessary for host protection against acute-phase Trypanosoma cruzi infection. J Immunol 185: 1150-1157.
35. Andrade MS, Hanania FR, Daci K, Leme RJ, Chadi G, (2008) Contuse lesion of the rat spinal cord of moderate intensity leads to a higher time-dependent secondary neurodegeneration than severe one. An open-window for experimental neuroprotective interventions. Tissue Cell 40: 143-156.
36. Chadi G, Andrade MS, Leme RJ, Gomide VC, (2001) Experimental models of partial lesion of rat spinal cord to investigate neurodegeneration, glial activation, and behavior impairments. Int J Neurosci 111: 137-165.
37. Thery C, Chamak B, Mallat M, (1991) Cytotoxic Effect of Brain Macrophages on Developing. Eur J Neurosci 3: 1155-1164.
38. Carpentier PA, Begolka WS, Olson JK, Elhofy A, Karpus WJ, et al. (2005) Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 49: 360-374.
39. Bal-Price A, Moneer Z, Brown GC, (2002) Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes. Glia 40: 312-323.
40. Chao CC, Hu S, (1994) Tumor necrosis factor-alpha potentiates glutamate neurotoxicity in human fetal brain cell cultures. Dev Neurosci 16: 172-179.
41. Merrill JE, Scolding NJ, (1999) Mechanisms of damage to myelin and oligodendrocytes and their relevance to disease. Neuropathol Appl Neurobiol 25: 435-458.
42. Dewar D, Underhill SM, Goldberg MP, (2003) Oligodendrocytes and ischemic brain injury. J Cereb Blood Flow Metab 23: 263-274.
43. Domercq M, Sanchez-Gomez MV, Sherwin C, Etxebarria E, Fern R, et al. (2007) System xc- and glutamate transporter inhibition mediates microglial toxicity to oligodendrocytes. J Immunol 178: 6549-6556.
44. Matute C, Sanchez-Gomez MV, Martinez-Millan L, Miledi R, (1997) Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc Natl Acad Sci U S A 94: 8830-8835.
45. Sica A, Mantovani A, (2012) Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122: 787-795.
46. Franklin BS, Parroche P, Ataide MA, Lauw F, Ropert C, et al. (2009) Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc Natl Acad Sci U S A 106: 5789-5794.
47. Tessema TS, Schwamb B, Lochner M, Forster I, Jakobi V, et al. (2009) Dynamics of gut mucosal and systemic Th1/Th2 cytokine responses in interferon-gamma and interleukin-12p40 knock out mice during primary and challenge Cryptosporidium parvum infection. Immunobiology 214: 454-466.
48. Bastos KR, Alvarez JM, Marinho CR, Rizzo LV, Lima MR, (2002) Macrophages from IL-12p40-deficient mice have a bias toward the M2 activation profile. J Leukoc Biol 71: 271-278.
49. Abrahamsohn IA, Coffman RL, (1996) Trypanosoma cruzi: IL-10, TNF, IFN-gamma, and IL-12 regulate innate and acquired immunity to infection. Exp Parasitol 84: 231-244.
50. Dinarello CA, (1999) IL-18: A TH1-inducing, proinflammatory cytokine and new member of the IL-1 family. J Allergy Clin Immunol 103: 11-24.
51. Muller U, Kohler G, Mossmann H, Schaub GA, Alber G, et al. (2001) IL-12-independent IFN-gamma production by T cells in experimental Chagas' disease is mediated by IL-18. J Immunol 167: 3346-3353.
52. Conti B, Park LC, Calingasan NY, Kim Y, Kim H, et al. (1999) Cultures of astrocytes and microglia express interleukin 18. Brain Res Mol Brain Res 67: 46-52.
53. Prinz M, Hanisch UK, (1999) Murine microglial cells produce and respond to interleukin-18. J Neurochem 72: 2215-2218.