Behavioural and neurological symptoms accompanied by cellular neuroinflammation in IL-10-deficient mice infected with Plasmodium chabaudi

Malaria Journal

Volumn 15, Issue 1, 2016, Pages

  Wilson, Kyle D ^a   Stutz, Sonja J ^a   Ochoa, Lorenzo F ^b   Valbuena, Gustavo A ^a,b   Cravens, Petra D ^a   Dineley, Kelly T ^a   Vargas, Gracie ^a,b   Stephens, Robin ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Brain; Malaria; Monocyte; Mouse; Neuroinflammation; T cell

Indexed keywords

CD45 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; TUMOR NECROSIS FACTOR; IL10 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BRAIN EDEMA; BRAIN HEMORRHAGE; CELL POPULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FLOW CYTOMETRY; GENE MUTATION; GRIP STRENGTH; HEREDITY; IMMUNOCOMPETENT CELL; MACROPHAGE; MONOCYTE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NOCICEPTION; NONHUMAN; PLASMODIUM CHABAUDI; PLASMODIUM CHABAUDI INFECTION; VASCULAR ENDOTHELIUM; WILD TYPE; ANIMAL; ANIMAL BEHAVIOR; BRAIN; C57BL MOUSE; CEREBRAL MALARIA; COMPLICATION; DEFICIENCY; DISEASE MODEL; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INFLAMMATION; LEUKOCYTE; MALE; MENTAL DISORDERS; PARASITOLOGY; PATHOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; HUMANS; INFLAMMATION; INTERLEUKIN-10; LEUKOCYTES; MALARIA, CEREBRAL; MALE; MENTAL DISORDERS; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; PLASMODIUM CHABAUDI;

EID: 84983541128     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/s12936-016-1477-1     Document Type: Article

References (48)

1. WHO. World Malaria Report 2015. Geneva: World Health Organization; 2015. http://www.who.int/malaria/publications/world-malaria-report-2015/en/. Accessed 07 Apr 2016.
2. Amante FH, Haque A, Stanley AC, de Rivera F, Randall LM, Wilson YA, et al. Immune-mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria. J Immunol. 2010;185:3632-42.
3. Seydel KB, Kampondeni SD, Valim C, Potchen MJ, Milner DA, Muwalo FW, et al. Brain swelling and death in children with cerebral malaria. N Engl J Med. 2015;372:1126-37.
4. Taylor TE, Fu WJ, Carr RA, Whitten RO, Mueller JG, Fosiko NG, et al. Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat Med. 2004;10:143-5.
5. Ouma C, Davenport GC, Were T, Otieno MF, Hittner JB, Vulule JM, et al. Haplotypes of IL-10 promoter variants are associated with susceptibility to severe malarial anemia and functional changes in IL-10 production. Hum Genet. 2008;124:515-24.
6. May J, Lell B, Luty AJ, Meyer CG, Kremsner PG. Plasma interleukin-10: tumor necrosis factor (TNF)-alpha ratio is associated with TNF promoter variants and predicts malarial complications. J Infect Dis. 2000;182:1570-3.
7. Sanni LA, Jarra W, Li C, Langhorne J. Cerebral edema and cerebral hemorrhages in interleukin-10-deficient mice infected with Plasmodium chabaudi. Infect Immun. 2004;72:3054-8.
8. Brugat T, Cunningham D, Sodenkamp J, Coomes S, Wilson M, Spence PJ, et al. Sequestration and histopathology in Plasmodium chabaudi malaria are influenced by the immune response in an organ-specific manner. Cell Microbiol. 2014;16:687-700.
9. Mota MM, Jarra W, Hirst E, Patnaik PK, Holder AA. Plasmodium chabaudi-infected erythrocytes adhere to CD36 and bind to microvascular endothelial cells in an organ-specific way. Infect Immun. 2000;68:4135-44.
10. Li C, Sanni LA, Omer F, Riley E, Langhorne J. Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor beta antibodies. Infect Immun. 2003;71:4850-6.
11. Clark IA, Chaudhri G. Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis. Br J Haematol. 1988;70:99-103.
12. Mastelic B, do Rosario AP, Veldhoen M, Renauld JC, Jarra W, Sponaas AM, et al. IL-22 protects against liver pathology and lethality of an experimental blood-stage malaria infection. Front Immunol. 2012;3:85.
13. Findlay EG, Greig R, Stumhofer JS, Hafalla JCR, de Souza JB, Saris CJ, et al. Essential role for IL-27 receptor signaling in prevention of Th1-mediated immunopathology during malaria infection. J Immunol. 2010;185:2482-92.
14. Luty AJ, Lell B, Schmidt-Ott R, Lehman LG, Luckner D, Greve B, et al. Parasite antigen-specific interleukin-10 and antibody reponses predict accelerated parasite clearance in Plasmodium falciparum malaria. Eur Cytokine Netw. 1998;9:639-46.
15. Milner DA Jr, Whitten RO, Kamiza S, Carr R, Liomba G, Dzamalala C, et al. The systemic pathology of cerebral malaria in African children. Front Cell Infect Microbiol. 2014;4:104.
16. Manning L, Rosanas-Urgell A, Laman M, Edoni H, McLean C, Mueller I, et al. A histopathologic study of fatal paediatric cerebral malaria caused by mixed Plasmodium falciparum/Plasmodium vivax infections. Malar J. 2012;11:107.
17. Dorovini-Zis K, Schmidt K, Huynh H, Fu W, Whitten RO, Milner D, et al. The neuropathology of fatal cerebral malaria in malawian children. Am J Pathol. 2011;178:2146-58.
18. Berendt A, Tumer G, Newbold C. Cerebral malaria: the sequestration hypothesis. Parasitol Today. 1994;10:412-4.
19. Campanella GS, Tager AM, El Khoury JK, Thomas SY, Abrazinski TA, Manice LA, et al. Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria. Proc Natl Acad Sci USA. 2008;105:4814-9.
20. Rudin W, Eugster HP, Bordmann G, Bonato J, Müller M, Yamage M, et al. Resistance to cerebral malaria in tumor necrosis factor-alpha/beta-deficient mice is associated with a reduction of intercellular adhesion molecule-1 up-regulation and T helper type 1 response. Am J Pathol. 1997;150:257-66.
21. Belnoue E, Kayibanda M, Vigario AM, Deschemin J-C, Nv Rooijen, Viguier M, et al. On the pathogenic role of brain-sequestered αβ CD8 + T cells in experimental cerebral malaria. J Immunol. 2002;169:6369-75.
22. Nitcheu J, Bonduelle O, Combadiere C, Tefit M, Seilhean D, Mazier D, et al. Perforin-dependent brain-infiltrating cytotoxic CD8 + T lymphocytes mediate experimental cerebral malaria pathogenesis. J Immunol. 2003;170:2221-8.
23. Potter S, Chan-Ling T, Ball HJ, Mansour H, Mitchell A, Maluish L, et al. Perforin mediated apoptosis of cerebral microvascular endothelial cells during experimental cerebral malaria. Int J Parasitol. 2006;36:485-96.
24. Belnoue E, Potter SM, Rosa DS, Mauduit M, Grüner AC, Kayibanda M, et al. Control of pathogenic CD8 + T cell migration to the brain by IFN-γ during experimental cerebral malaria. Parasite Immunol. 2008;30:544-53.
25. Linke A, Kühn R, Müller W, Honarvar N, Li C, Langhorne J. Plasmodium chabaudi chabaudi: differential susceptibility of gene-targeted mice deficient in IL-10 to an erythrocytic-stage infection. Exp Parasitol. 1996;84:253-63.
26. Li C, Corraliza I, Langhorne J. A Defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect Immun. 1999;67:4435-42.
27. do Freitas Rosario AP, Lamb T, Spence P, Stephens R, Lang A, Roers A, et al. IL-27 promotes IL-10 production by effector Th1 CD4 + T cells: a critical mechanism for protection from severe immunopathology during malaria infection. J Immunol. 2012;188:1178-90.
28. Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, Martin JE. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome. 1997;8:711-3.
29. Yap GS, Stevenson MM. Plasmodium chabaudi AS: erythropoietic responses during infection in resistant and susceptible mice. Exp Parasitol. 1992;75:340-52.
30. Cross CE, Langhorne J. Plasmodium chabaudi chabaudi (AS): inflammatory cytokines and pathology in an erythrocytic-stage infection in mice. Exp Parasitol. 1998;90:220-9.
31. Lamb TJ, Langhorne J. The severity of malarial anaemia in Plasmodium chabaudi infections of BALB/c mice is determined independently of the number of circulating parasites. Malar J. 2008;7:68.
32. Lackner P, Beer R, Heussler V, Goebel G, Rudzki D, Helbok R, et al. Behavioural and histopathological alterations in mice with cerebral malaria. Neuropathol Appl Neurobiol. 2006;32:177-88.
33. Desruisseaux MS, Gulinello M, Smith DN, Lee SC, Tsuji M, Weiss LM, et al. Cognitive dysfunction in mice infected with Plasmodium berghei strain ANKA. J Infect Dis. 2008;197:1621-7.
34. Hermsen C, Van De Wiel T, Mommers E, Sauerwein R, Eling W. Depletion of CD4+ or CD8 + T-cells prevents Plasmodium berghei induced cerebral malaria in end-stage disease. Parasitology. 1997;114:7-12.
35. Poh CM, Howland SW, Grotenbreg GM, Renia L. Damage to the blood-brain barrier during experimental cerebral malaria results from synergistic effects of CD8 + T cells with different specificities. Infect Immun. 2014;82:4854-64.
36. Villegas-Mendez A, Greig R, Shaw TN, de Souza JB, Gwyer Findlay E, Stumhofer JS, et al. IFN-gamma-producing CD4 + T cells promote experimental cerebral malaria by modulating CD8 + T cell accumulation within the brain. J Immunol. 2012;189:968-79.
37. Lacerda-Queiroz N, Rodrigues DH, Vilela MC, Miranda AS, Amaral DC, Camargos ER, et al. Inflammatory changes in the central nervous system are associated with behavioral impairment in Plasmodium berghei (strain ANKA)-infected mice. Exp Parasitol. 2010;125:271-8.
38. Trang TTM, Phu NH, Vinh H, Hien TT, Cuong BM, Chau TTH, et al. Acute renal failure in patients with severe falciparum malaria. Clin Infect Dis. 1992;15:874-80.
39. Mohan A, Sharma SK, Bollineni S. Acute lung injury and acute respiratory distress syndrome in malaria. J Vector Borne Dis. 2008;45:179-93.
40. Krishnan A, Karnad DR. Severe falciparum malaria: an important cause of multiple organ failure in Indian intensive care unit patients. Crit Care Med. 2003;31:2278-84.
41. Seixas E, Oliveira P, Moura Nunes JF, Coutinho A. An experimental model for fatal malaria due to TNF-α-dependent hepatic damage. Parasitology. 2008;135:683-90.
42. Seixas E, Gozzelino R, Chora Â, Ferreira A, Silva G, Larsen R, et al. Heme oxygenase-1 affords protection against noncerebral forms of severe malaria. Proc Natl Acad Sci USA. 2009;106:15837-42.
43. Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, Epiphanio S, et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med. 2007;13:703-10.
44. Clark IA, Awburn MM, Harper CG, Liomba NG, Molyneux ME. Induction of HO-1 in tissue macrophages and monocytes in fatal falciparum malaria and sepsis. Malar J. 2003;2:41.
45. Neill AL, Hunt NH. Pathology of fatal and resolving Plasmodium berghei cerebral malaria in mice. Parasitology. 1992;105:165-75.
46. Couper KN, Blount DG, Wilson MS, Hafalla JC, Belkaid Y, Kamanaka M, et al. IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog. 2008;4:e1000004.
47. Sponaas A-M, do Freitas Rosario AP, Voisine C, Mastelic B, Thompson J, Koernig S, et al. Migrating monocytes recruited to the spleen play an important role in control of blood stage malaria. Blood. 2009;114:5522-31.
48. Guha SK, Tillu R, Sood A, Patgaonkar M, Nanavaty IN, Sengupta A, et al. Single episode of mild murine malaria induces neuroinflammation, alters microglial profile, impairs adult neurogenesis, and causes deficits in social and anxiety-like behavior. Brain Behav Immun. 2014;42:123-37.