Genome-wide analysis of host-plasmodium yoelii interactions reveals regulators of the type i interferon response

Cell Reports

Volumn 12, Issue 4, 2015, Pages 661-672

  Wu, Jian ^a   Cai, Baowei ^b,c   Sun, Wenxiang ^a   Huang, Ruili ^d   Liu, Xueqiao ^a   Lin, Meng ^c   Pattaradilokrat, Sittiporn ^a,e   Martin, Scott ^d   Qi, Yanwei ^a,b   Nair, Sethu C ^a   Bolland, Silvia ^a   Cohen, Jeffrey I ^a   Austin, Christopher P ^d   Long, Carole A ^a   Myers, Timothy G ^a   Wang, Rong Fu ^c   Su, Xin zhuan ^a,b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b XIAMEN UNIVERSITY   (China)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e CHULALONGKORN UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE PHOSPHORIBOSYLTRANSFERASE; ADENOSINE DEAMINASE; ADENOSINE TRIPHOSPHATE; BETA INTERFERON; FC RECEPTOR; GLUTATHIONE PEROXIDASE; INTERFERON; INTERLEUKIN 1BETA; MESSENGER RNA;

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME 10; CHROMOSOME 13; CHROMOSOME 14; CHROMOSOME 3; CHROMOSOME 4; CHROMOSOME 8; CHROMOSOME 9; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENE INTERACTION; GENE LOCUS; GENE ONTOLOGY; GENETIC ASSOCIATION; GENOTYPE; HEMATOPOIESIS; HOST PATHOGEN INTERACTION; LIMIT OF DETECTION; MICROSATELLITE MARKER; MOUSE; NONHUMAN; PARASITOSIS; PHENOTYPE; PLASMODIUM YOELII; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; UPREGULATION; VESICULAR STOMATITIS; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; GENETICS; GENOME; GENOME-WIDE ASSOCIATION STUDY; HOST PARASITE INTERACTION; MALARIA; METABOLISM; PARASITOLOGY; PATHOGENICITY;

ANIMALS; GENOME, PROTOZOAN; GENOME-WIDE ASSOCIATION STUDY; HOST-PARASITE INTERACTIONS; INTERFERON TYPE I; MALARIA; MICE; MICE, INBRED C57BL; PLASMODIUM YOELII; QUANTITATIVE TRAIT LOCI;

EID: 84947040852     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.06.058     Document Type: Article

References (42)

1. Barber, G.N. (2011). Innate immune DNA sensing pathways: STING, AIMII and the regulation of interferon production and inflammatory responses. Curr. Opin. Immunol. 23, 10-20.
2. Barreiro, L.B., Tailleux, L., Pai, A.A., Gicquel, B., Marioni, J.C., and Gilad, Y. (2012). Deciphering the genetic architecture of variation in the immune response to Mycobacterium tuberculosis infection. Proc. Natl. Acad. Sci. USA 109, 1204-1209.
3. Benjamini, Y., and Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165-1188.
4. Boivin, G.A., Pothlichet, J., Skamene, E., Brown, E.G., Loredo-Osti, J.C., Sladek, R., and Vidal, S.M. (2012). Mapping of clinical and expression quantitative trait loci in a sex-dependent effect of host susceptibility to mouse-adapted influenza H3N2/HK/1/68. J. Immunol. 188, 3949-3960.
5. Bottomly, D., Ferris, M.T., Aicher, L.D., Rosenzweig, E., Whitmore, A., Aylor, D.L., Haagmans, B.L., Gralinski, L.E., Bradel-Tretheway, B.G., Bryan, J.T., et al. (2012). Expression quantitative trait Loci for extreme host response to influenza a in pre-collaborative cross mice. G3 (Bethesda) 2, 213-221.
6. Bü ngener, W. (1979). [Malaria plasmodia in the mouse. Parasitization of mature and immature erythrocytes by Plasmodium berghei, Plasmodium yoelii and Plasmodium chabaudi (author's transl)]. Tropenmed. Parasitol. 30, 198-205.
7. Carlton, J.M., Angiuoli, S.V., Suh, B.B., Kooij, T.W., Pertea, M., Silva, J.C., Ermolaeva, M.D., Allen, J.E., Selengut, J.D., Koo, H.L., et al. (2002). Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419, 512-519.
8. Chapman, M.S., Wu, L., Amatucci, A., Ho, S.N., and Michaelson, J.S. (2013). TWEAK signals through JAK-STAT to induce tumor cell apoptosis. Cytokine 61, 210-217.
9. Degner, J.F., Pai, A.A., Pique-Regi, R., Veyrieras, J.B., Gaffney, D.J., Pickrell, J.K., De Leon, S., Michelini, K., Lewellen, N., Crawford, G.E., et al. (2012).
10. DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482, 390-394.
11. Eskan, M.A., Rose, B.G., Benakanakere, M.R., Lee, M.J., and Kinane, D.F. (2008). Sphingosine 1-phosphate 1 and TLR4 mediate IFN-beta expression in human gingival epithelial cells. J. Immunol. 180, 1818-1825.
12. Fairfax, B.P., Humburg, P., Makino, S., Naranbhai, V., Wong, D., Lau, E., Jostins, L., Plant, K., Andrews, R., McGee, C., and Knight, J.C. (2014). Innate immune activity conditions the effect of regulatory variants upon monocyte gene expression. Science 343, 1246949.
13. Gao, D., Wu, J., Wu, Y.T., Du, F., Aroh, C., Yan, N., Sun, L., and Chen, Z.J. (2013). Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341, 903-906.
14. Gazzinelli, R.T., Kalantari, P., Fitzgerald, K.A., and Golenbock, D.T. (2014). Innate sensing of malaria parasites. Nat. Rev. Immunol. 14, 744-757.
15. George, C.X., Gan, Z., Liu, Y., and Samuel, C.E. (2011). Adenosine deaminases acting on RNA, RNA editing, and interferon action. J. Interferon Cytokine Res. 31, 99-117.
16. Ioan-Facsinay, A., de Kimpe, S.J., Hellwig, S.M., van Lent, P.L., Hofhuis, F.M., van Ojik, H.H., Sedlik, C., da Silveira, S.A., Gerber, J., de Jong, Y.F., et al. (2002). FcgammaRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 16, 391-402.
17. Kohonen, T. (2006). Self-organizing neural projections. Neural Netw. 19, 723-733.
18. Larsson, J., and Karlsson, S. (2005). The role of Smad signaling in hematopoiesis. Oncogene 24, 5676-5692.
19. Lee, M.N., Ye, C., Villani, A.C., Raj, T., Li, W., Eisenhaure, T.M., Imboywa, S.H., Chipendo, P.I., Ran, F.A., Slowikowski, K., et al. (2014). Common genetic variants modulate pathogen-sensing responses in human dendritic cells. Science 343, 1246980.
20. Li, J., Pattaradilokrat, S., Zhu, F., Jiang, H., Liu, S., Hong, L., Fu, Y., Koo, L., Xu, W., Pan, W., et al. (2011). Linkage maps from multiple genetic crosses and loci linked to growth-related virulent phenotype in Plasmodium yoelii. Proc. Natl. Acad. Sci. USA 108, E374-E382.
21. Li, L., Zhang, X., and Zhao, H. (2012). eQTL. Methods Mol. Biol. 871, 265-279.
22. Liehl, P., and Mota, M.M. (2012). Innate recognition of malarial parasites by mammalian hosts. Int. J. Parasitol. 42, 557-566.
23. Liehl, P., Zuzarte-Lui{dotless}s, V., Chan, J., Zillinger, T., Baptista, F., Carapau, D., Konert, M., Hanson, K.K., Carret, C., Lassnig, C., et al. (2014). Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection. Nat. Med. 20, 47-53.
24. Linkermann, A., Stockwell, B.R., Krautwald, S., and Anders, H.J. (2014). Regulated cell death and inflammation: an auto-amplification loop causes organ failure. Nat. Rev. Immunol. 14, 759-767.
25. Ma, Z., Moore, R., Xu, X., and Barber, G.N. (2013). DDX24 negatively regulates cytosolic RNA-mediated innate immune signaling. PLoS Pathog. 9, e1003721.
26. Miller, J.L., Sack, B.K., Baldwin, M., Vaughan, A.M., and Kappe, S.H. (2014). Interferon-mediated innate immune responses against malaria parasite liver stages. Cell Rep. 7, 436-447.
27. Mogensen, T.H. (2009). Pathogen recognition and inflammatory signaling in innate immune defenses. Clin. Microbiol. Rev. 22, 240-273.
28. Nair, S.C., Pattaradilokrat, S., Zilversmit, M.M., Dommer, J., Nagarajan, V., Stephens, M.T., Xiao, W., Tan, J.C., and Su, X.Z. (2014). Genome-wide polymorphisms and development of a microarray platform to detect genetic variations in Plasmodium yoelii. Mol. Biochem. Parasitol. 194, 9-15.
29. Pan, Y., Li, R., Meng, J.L., Mao, H.T., Zhang, Y., and Zhang, J. (2014). Smurf2 negatively modulates RIG-I-dependent antiviral response by targeting VISA/ MAVS for ubiquitination and degradation. J. Immunol. 192, 4758-4764.
30. Pattaradilokrat, S., Li, J., Wu, J., Qi, Y., Eastman, R.T., Zilversmit, M., Nair, S.C., Huaman, M.C., Quinones, M., Jiang, H., et al. (2014). Plasmodium genetic loci linked to host cytokine and chemokine responses. Genes Immun. 15, 145-152.
31. Peng, Y., Xu, R., and Zheng, X. (2014). HSCARG negatively regulates the cellular antiviral RIG-I like receptor signaling pathway by inhibiting TRAF3 ubiquitination via recruiting OTUB1. PLoS Pathog. 10, e1004041
32. Rajput, A., Kovalenko, A., Bogdanov, K., Yang, S.H., Kang, T.B., Kim, J.C., Du, J., and Wallach, D. (2011). RIG-I RNA helicase activation of IRF3 transcription factor is negatively regulated by caspase-8-mediated cleavage of the RIP1 protein. Immunity 34, 340-351.
33. Reilly Ayala, H.B., Wacker, M.A., Siwo, G., and Ferdig, M.T. (2010). Quantitative trait loci mapping reveals candidate pathways regulating cell cycle duration in Plasmodium falciparum. BMC Genomics 11, 577.
34. Rusinova, I., Forster, S., Yu, S., Kannan, A., Masse, M., Cumming, H., Chapman, R., and Hertzog, P.J. (2013). Interferome v2.0: an updated database of annotated interferon-regulated genes. Nucleic Acids Res. 41, D1040-D1046.
35. Sakaguchi, S., Yamaguchi, T., Nomura, T., and Ono, M. (2008). Regulatory T cells and immune tolerance. Cell 133, 775-787.
36. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504.
37. Sharma, S., DeOliveira, R.B., Kalantari, P., Parroche, P., Goutagny, N., Jiang, Z., Chan, J., Bartholomeu, D.C., Lauw, F., Hall, J.P., et al. (2011). Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity 35, 194-207.
38. Sun, L., Wu, J., Du, F., Chen, X., and Chen, Z.J. (2013). Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339, 786-791
39. van der Harst, P., Zhang, W., Mateo Leach, I., Rendon, A., Verweij, N., Sehmi, J., Paul, D.S., Elling, U., Allayee, H., Li, X., et al. (2012). Seventy-five genetic loci influencing the human red blood cell. Nature 492, 369-375.
40. Wang, Z., Choi, M.K., Ban, T., Yanai, H., Negishi, H., Lu, Y., Tamura, T., Takaoka, A., Nishikura, K., and Taniguchi, T. (2008). Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc. Natl. Acad. Sci. USA 105, 5477-5482.
41. Wu, J., Tian, L., Yu, X., Pattaradilokrat, S., Li, J., Wang, M., Yu, W., Qi, Y., Zeituni, A.E., Nair, S.C., et al. (2014). Strain-specific innate immune signaling pathways determine malaria parasitemia dynamics and host mortality. Proc. Natl. Acad. Sci. USA 111, E511-E520.
42. Yuan, J., Cheng, K.C., Johnson, R.L., Huang, R., Pattaradilokrat, S., Liu, A., Guha, R., Fidock, D.A., Inglese, J., Wellems, T.E., et al. (2011). Chemical genomic profiling for antimalarial therapies, response signatures, and molecular targets. Science 333, 724-729.