Caspase-12 dampens the immune response to malaria independently of the inflammasome by targeting NF-κB signaling

Journal of Immunology

Volumn 185, Issue 9, 2010, Pages 5495-5502

  Labbé, Katherine ^a   Miu, Jenny ^a   Yeretssian, Garabet ^a   Serghides, Lena ^b,c   Tam, Mifong ^a   Finney, Constance A ^b,c   Erdman, Laura K ^b,c   Goulet, Marie Line ^a   Kain, Kevin C ^b,c   Stevenson, Mary M ^a   Saleh, Maya ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 12; I KAPPA B ALPHA; I KAPPA B BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; CASP12 PROTEIN, MOUSE; CYTOKINE;

ANIMAL CELL; ARTICLE; BRAIN MALARIA; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME INHIBITION; FEMALE; IMMUNE RESPONSE; INFECTION SENSITIVITY; MOUSE; NONHUMAN; PARASITE CLEARANCE; PATHOGENESIS; PLASMODIUM CHABAUDI INFECTION; PRIORITY JOURNAL; PROTEIN TARGETING; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC PREDISPOSITION; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATION; MALARIA; METABOLISM; MOUSE MUTANT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CASPASE 12; CYTOKINES; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFLAMMATION; MALARIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 78149487761     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002517     Document Type: Article

References (33)

1. Su, Z., and M. M. Stevenson. 2002. IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J. Immunol. 168:1348-1355.
2. Miu, J., A. J. Mitchell, M. Müller, S. L. Carter, P. M. Manders, J. A. McQuillan, B. M. Saunders, H. J. Ball, B. Lu, I. L. Campbell, and N. H. Hunt. 2008. Chemokine gene expression during fatal murine cerebral malaria and protection due to CXCR3 deficiency. J. Immunol. 180:1217-1230.
3. Hunt, N. H., and G. E. Grau. 2003. Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol. 24:491-499.
4. Dostert, C., G. Guarda, J. F. Romero, P. Menu, O. Gross, A. Tardivel, M. L. Suva, J. C. Stehle, M. Kopf, I. Stamenkovic, et al. 2009. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS ONE 4: e6510.
5. Shio, M. T., M. Tiemi Shio, S. C. Eisenbarth, M. Savaria, A. F. Vinet, M. J. Bellemare, K. W. Harder, F. S. Sutterwala, D. S. Bohle, A. Descoteaux, et al. 2009. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 5: e1000559.
6. Roy, S., J. R. Sharom, C. Houde, T. P. Loisel, J. P. Vaillancourt, W. Shao, M. Saleh, and D. W. Nicholson. 2008. Confinement of caspase-12 proteolytic activity to autoprocessing. Proc. Natl. Acad. Sci. USA 105:4133-4138.
7. Saleh, M., J. C. Mathison, M. K. Wolinski, S. J. Bensinger, P. Fitzgerald, N. Droin, R. J. Ulevitch, D. R. Green, and D. W. Nicholson. 2006. Enhanced bacterial clearance and sepsis resistance in caspase-12-deficient mice. Nature 440:1064-1068.
8. Saleh, M., J. P. Vaillancourt, R. K. Graham, M. Huyck, S. M. Srinivasula, E. S. Alnemri, M. H. Steinberg, V. Nolan, C. T. Baldwin, R. S. Hotchkiss, et al. 2004. Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms. Nature 429:75-79.
9. Yeretssian, G., K. Doiron, W. Shao, B. R. Leavitt, M. R. Hayden, D. W. Nicholson, and M. Saleh. 2009. Gender differences in expression of the human caspase-12 long variant determines susceptibility to Listeria monocytogenes infection. Proc. Natl. Acad. Sci. USA 106:9016-9020.
10. Labbé, K., and M. Saleh. 2008. Cell death in the host response to infection. Cell Death Differ. 15:1339-1349.
11. Kuida, K., J. A. Lippke, G. Ku, M. W. Harding, D. J. Livingston, M. S. Su, and R. A. Flavell. 1995. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267:2000-2003.
12. Podoba, J. E., and M. M. Stevenson. 1991. CD4+ and CD8+ T lymphocytes both contribute to acquired immunity to blood-stage Plasmodium chabaudi AS. Infect. Immun. 59:51-58.
13. Bertrand, M. J., K. Doiron, K. Labbé, R. G. Korneluk, P. A. Barker, and M. Saleh. 2009. Cellular inhibitors of apoptosis cIAP1 and cIAP2 are required for innate immunity signaling by the pattern recognition receptors NOD1 and NOD2. Immunity 30:789-801.
14. Trager, W., and J. B. Jensen. 1976. Human malaria parasites in continuous culture. Science 193:673-675.
15. Yap, G. S., P. Jacobs, and M. M. Stevenson. 1994. Th cell regulation of host resistance to blood-stage Plasmodium chabaudi AS. Res. Immunol. 145:419-422.
16. Stevenson, M. M., M. F. Tam, M. Belosevic, P. H. van der Meide, and J. E. Podoba. 1990. Role of endogenous gamma interferon in host response to infection with blood-stage Plasmodium chabaudi AS. Infect. Immun. 58:3225-3232.
17. LeBlanc, P. M., G. Yeretssian, N. Rutherford, K. Doiron, A. Nadiri, L. Zhu, D. R. Green, S. Gruenheid, and M. Saleh. 2008. Caspase-12 modulates NOD signaling and regulates antimicrobial peptide production and mucosal immunity. Cell Host Microbe 3:146-157.
18. Hunt, N. H., J. Golenser, T. Chan-Ling, S. Parekh, C. Rae, S. Potter, I. M. Medana, J. Miu, and H. J. Ball. 2006. Immunopathogenesis of cerebral malaria. Int. J. Parasitol. 36:569-582.
19. Stevenson, M. M., and E. M. Riley. 2004. Innate immunity to malaria. Nat. Rev. Immunol. 4:169-180.
20. de Souza, J. B., and E. M. Riley. 2002. Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes Infect. 4:291-300.
21. Reimer, T., M. H. Shaw, L. Franchi, C. Coban, K. J. Ishii, S. Akira, T. Horii, A. Rodriguez, and G. Nunez. 2009. Experimental cerebral malaria progresses independently of the Nlrp3 inflammasome. Eur. J. Immunol. 40:764-769.
22. Griffith, J. W., T. Sun, M. T. McIntosh, and R. Bucala. 2009. Pure hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J. Immunol. 183:5208-5220.
23. Krishnegowda, G., A. M. Hajjar, J. Zhu, E. J. Douglass, S. Uematsu, S. Akira, A. S. Woods, and D. C. Gowda. 2005. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem. 280:8606-8616.
24. Seixas, E., J. F. Moura Nunes, I. Matos, and A. Coutinho. 2009. The interaction between DC and Plasmodium berghei/chabaudi-infected erythrocytes in mice involves direct cell-to-cell contact, internalization and TLR. Eur. J. Immunol. 39:1850-1863.
25. Gowda, D. C. 2007. TLR-mediated cell signaling by malaria GPIs. Trends Parasitol. 23:596-604.
26. Su, Z., and M. M. Stevenson. 2000. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 68:4399-4406.
27. Jaramillo, M., D. C. Gowda, D. Radzioch, and M. Olivier. 2003. Hemozoin increases IFN-gamma-inducible macrophage nitric oxide generation through extracellular signal-regulated kinase-and NF-kappa B-dependent pathways. J. Immunol. 171:4243-4253.
28. Coban, C., K. J. Ishii, S. Uematsu, N. Arisue, S. Sato, M. Yamamoto, T. Kawai, O. Takeuchi, H. Hisaeda, T. Horii, and S. Akira. 2007. Pathological role of Tolllike receptor signaling in cerebral malaria. Int. Immunol. 19:67-79.
29. Cui, J., L. Zhu, X. Xia, H. Y. Wang, X. Legras, J. Hong, J. Ji, P. Shen, S. Zheng, Z. J. Chen, and R. F. Wang. 2010. NLRC5 negatively regulates the NF-kappaB and type I interferon signaling pathways. Cell 141:483-496.
30. Miu, J., N. H. Hunt, and H. J. Ball. 2008. Predominance of interferon-related responses in the brain during murine malaria, as identified by microarray analysis. Infect. Immun. 76:1812-1824.
31. Griffith, J. W., C. O'Connor, K. Bernard, T. Town, D. R. Goldstein, and R. Bucala. 2007. Toll-like receptor modulation of murine cerebral malaria is dependent on the genetic background of the host. J. Infect. Dis. 196:1553-1564.
32. Xue, Y., A. Daly, B. Yngvadottir, M. Liu, G. Coop, Y. Kim, P. Sabeti, Y. Chen, J. Stalker, E. Huckle, et al. 2006. Spread of an inactive form of caspase-12 in humans is due to recent positive selection. Am. J. Hum. Genet. 78:659-670.
33. McCall, M. B., B. Ferwerda, J. Hopman, I. Ploemen, B. Maiga, M. Daou, A. Dolo, C. C. Hermsen, O. K. Doumbo, G. Bedu-Addo, et al. 2010. Persistence of full-length caspase-12 and its relation to malaria in West and Central African populations. Eur. Cytokine Netw. 21:77-83.