Transcriptomic profiling of microglia reveals signatures of cell activation and immune response, during experimental cerebral malaria

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Capuccini, Barbara ^a   Lin, Jingwen ^a   Talavera López, Carlos ^a   Khan, Shahid M ^b   Sodenkamp, Jan ^a   Spaccapelo, Roberta ^c   Langhorne, Jean ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF PERUGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; BETA INTERFERON; CHEMOKINE; HLA ANTIGEN CLASS 1; INTERFERON; INTERFERON REGULATORY FACTOR 7; IRF7 PROTEIN, MOUSE; OASL1 PROTEIN, MOUSE;

ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CEREBRAL MALARIA; CLUSTER ANALYSIS; CYTOLOGY; DISEASE MODEL; DNA MICROARRAY; ERYTHROCYTE; FEMALE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MICROGLIA; MOUSE; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; PLASMODIUM BERGHEI; PRINCIPAL COMPONENT ANALYSIS; UPREGULATION;

2',5'-OLIGOADENYLATE SYNTHETASE; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINES; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; ERYTHROCYTES; FEMALE; GENE EXPRESSION PROFILING; HISTOCOMPATIBILITY ANTIGENS CLASS I; INTERFERON REGULATORY FACTOR-7; INTERFERON TYPE I; INTERFERON-BETA; MALARIA, CEREBRAL; MICE; MICE, INBRED C57BL; MICROGLIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMODIUM BERGHEI; PRINCIPAL COMPONENT ANALYSIS; UP-REGULATION;

EID: 85006810409     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep39258     Document Type: Article

References (49)

1. Riley, E. M. & Stewart, V. A. Immune mechanisms in malaria: new insights in vaccine development. Nat Med 19, 168-178 (2013).
2. WHO. World malaria report 2014, 1-20 (2014).
3. White, N. J., Turner, G. D. H., Day, N. P. J. & Dondorp, A. M. Lethal malaria: Marchiafava and Bignami were right. J. Infect. Dis. 208, 192-198 (2013).
4. Clark, I. A. & Rockett, K. A. The cytokine theory of human cerebral malaria. Parasitol. Today (Regul. Ed.) 10, 410-412 (1994).
5. Grau, G. E. R. & Craig, A. G. Cerebral malaria pathogenesis: revisiting parasite and host contributions. Future Microbiol 7, 291-302 (2012).
6. Hoeffel, G. et al. C-Myb(+ ) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42, 665-678 (2015).
7. Prinz, M. & Priller, J. Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat. Rev. Neurosci. 15, 300-312 (2014).
8. Salter, M. W. & Beggs, S. Sublime microglia: expanding roles for the guardians of the CNS. Cell 158, 15-24 (2014).
9. Masuda, T. & Prinz, M. Microglia: A Unique Versatile Cell in the Central Nervous System. ACS Chem. Neurosci. 7, 428-434 (2016).
10. Goldmann, T. & Prinz, M. Role of Microglia in CNS Autoimmunity. Clinical and Developmental Immunology 2013, 1-8 (2013).
11. Idro, R., Marsh, K., John, C. C. & Newton, C. R. J. Cerebral Malaria: Mechanisms of Brain Injury and Strategies for Improved Neurocognitive Outcome. Pediatr Res 68, 267-274 (2010).
12. Medana, I. M. & Turner, G. D. H. Human cerebral malaria and the blood-brain barrier. International Journal for Parasitology 36, 555-568 (2006).
13. Szklarczyk, A. et al. Glial activation and matrix metalloproteinase release in cerebral malaria. J. Neurovirol. 13, 2-10 (2007).
14. Shaw, T. N. et al. Perivascular Arrest of CD8+ T Cells Is a Signature of Experimental Cerebral Malaria. PLoS Pathog 11, e1005210 (2015).
15. Lennington, J. B. et al. Transcriptome Analysis of the Human Striatum in Tourette Syndrome. Biol Psychiatry 79, 372-382 (2016).
16. Chiu, I. M. et al. A neurodegeneration-specific gene-expression signature of acutely isolated microglia from an amyotrophic lateral sclerosis mouse model. Cell Rep 4, 385-401 (2013).
17. Delahaye, N. F. et al. Gene expression analysis reveals early changes in several molecular pathways in cerebral malaria-susceptible mice versus cerebral malaria-resistant mice. BMC Genomics 8, 452 (2007).
18. Berghout, J. et al. Irf8-regulated genomic responses drive pathological inflammation during cerebral malaria. PLoS Pathog 9, e1003491 (2013).
19. Nacer, A. et al. Neuroimmunological Blood Brain Barrier Opening in Experimental Cerebral Malaria. PLoS Pathog 8, e1002982 (2012).
20. Goldmann, T. et al. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci 16, 1618-1626 (2013).
21. Larson, S. R. et al. Ly6C|[plus]| monocyte efferocytosis and cross-presentation of cell-Associated antigens. Cell Death & Differentiation 23, 997-1003 (2016).
22. Antonelli, A. et al. Interferon-α ,-βand-γinduce CXCL11 secretion in human thyrocytes: modulation by peroxisome proliferatoractivated receptor γagonists. Immunobiology 218, 690-695 (2013).
23. Kroetz, D. N. et al. Type I Interferon Induced Epigenetic Regulation of Macrophages Suppresses Innate and Adaptive Immunity in Acute Respiratory Viral Infection. PLoS Pathog 11, e1005338 (2015).
24. Sjöstrand, M. et al. The Expression of BAFF Is Controlled by IRF Transcription Factors. The Journal of Immunology 196, 91-96 (2016).
25. Lindahl, P., Gresser, I., Leary, P. & Tovey, M. Interferon treatment of mice: enhanced expression of histocompatibility antigens on lymphoid cells. Proc Natl Acad Sci USA 73, 1284-1287 (1976).
26. Bai, X. et al. Mycobacterium tuberculosis increases IP-10 and MIG protein despite inhibition of IP-10 and MIG transcription. Tuberculosis (Edinb) 91, 26-35 (2011).
27. Bouazzaoui, A. et al. Chemokine and chemokine receptor expression analysis in target organs of acute graft-versus-host disease. Genes Immun. 10, 687-701 (2009).
28. Lin, J.-W. et al. Replication of Plasmodium in reticulocytes can occur without hemozoin formation, resulting in chloroquine resistance. Journal of Experimental Medicine 212, 893-903 (2015).
29. Blasi, E., Barluzzi, R., Bocchini, V., Mazzolla, R. & Bistoni, F. Immortalization of murine microglial cells by a v-raf/v-myccarrying retrovirus. Journal of Neuroimmunology 27, 229-237 (1990).
30. Ding, Z. et al. Antiviral drug ganciclovir is a potent inhibitor of microglial proliferation and neuroinflammation. Journal of Experimental Medicine 211, 189-198 (2014).
31. Medana, I. M., Hunt, N. H. & Chan-Ling, T. Early activation of microglia in the pathogenesis of fatal murine cerebral malaria. Glia 19, 91-103 (1997).
32. Hoffmann, A. et al. Experimental Cerebral Malaria Spreads along the Rostral Migratory Stream. PLoS Pathog 12, e1005470-e1005470 (2016).
33. Hansen, D. S. Inflammatory responses associated with the induction of cerebral malaria: lessons from experimental murine models. PLoS Pathog 8, e1003045 (2012).
34. Howland, S. W., Poh, C. M. & Rénia, L. Activated Brain Endothelial Cells Cross-Present Malaria Antigen. PLoS Pathog 11, e1004963 (2015).
35. deWalick, S. et al. Cutting Edge: Conventional Dendritic Cells Are the Critical APC Required for the Induction of Experimental Cerebral Malaria. J. Immunol. 178, 6033-6037 (2007).
36. Haque, A. et al. Type I IFN signaling in CD8-DCs impairs Th1-dependent malaria immunity. J. Clin. Invest. 124, 2483-2496 (2014).
37. Rocha, B. C. et al. Type I Interferon Transcriptional Signature in Neutrophils and Low-Density Granulocytes Are Associated with Tissue Damage in Malaria. Cell Rep 13, 2829-2841 (2015).
38. Zanon, R. G. et al. Interferon (IFN) beta treatment induces major histocompatibility complex (MHC) class I expression in the spinal cord and enhances axonal growth and motor function recovery following sciatic nerve crush in mice. Neuropathol. Appl. Neurobiol. 36, 515-534 (2010).
39. Palomo, J. et al. Type I interferons contribute to experimental cerebral malaria development in response to sporozoite or blood-stage Plasmodium berghei ANKA. Eur. J. Immunol. 43, 2683-2695 (2013).
40. Rauch, I., Möller, M. & Decker, T. The regulation of inflammation by interferons and their STATs. JAKSTAT 2, e23820-e23820 (2013).
41. Wilson, N. O. et al. Pharmacologic inhibition of CXCL10 in combination with anti-malarial therapy eliminates mortality associated with murine model of cerebral malaria. PLoS ONE 8, e60898 (2013).
42. Dalko, E. et al. Heme dampens T-cell sequestration by modulating glial cell responses during rodent cerebral malaria. Brain Behav. Immun., doi: 10.1016/j.bbi07157(2016) (2016).
43. Ivashkiv, L. B. & Donlin, L. T. Regulation of type I interferon responses. Nature Reviews Immunology 14, 36-49 (2014).
44. González-Navajas, J. M., Lee, J., David, M. & Raz, E. Immunomodulatory functions of type I interferons. Nature Reviews Immunology 1-23 (2012), doi: 10.1038/nri3133 (2012).
45. Gough, D. J., Messina, N. L., Clarke, C. J. P., Johnstone, R. W. & Levy, D. E. Constitutive Type I Interferon Modulates Homeostatic Balance through Tonic Signaling. Immunity 36, 166-174 (2012).
46. Waknine-Grinberg, J. H. et al. Artemisone effective against murine cerebral malaria. Malar J 9, 227-227 (2010).
47. Spaccapelo, R. et al. Disruption of plasmepsin-4 and merozoites surface protein-7 genes in Plasmodium berghei induces combined virulence-Attenuated phenotype. Sci Rep 1, 39 (2011).
48. Cardona, A. E. et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9, 917-924 (2006).
49. Livak, K. J. & Schmittgen, T. D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-δ δ CT Method. Methods 25, 402-408 (2001).