Plasmodium berghei histamine-releasing factor favours liver-stage development via inhibition of IL-6 production and associates with a severe outcome of disease

Cellular Microbiology

Volumn 17, Issue 4, 2015, Pages 542-558

  Mathieu, Cédric ^a,b   Demarta Gatsi, Claudia ^a,b   Porcherie, Adeline ^a,b   Brega, Sara ^a   Thiberge, Sabine ^a   Ronce, Karine ^a,b   Smith, Leanna ^a,b   Peronet, Roger ^a,b   Amino, Rogerio ^a   Ménard, Robert ^a   Mécheri, Salaheddine ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTAMINE RELEASING FACTOR; INTERLEUKIN 6; TUMOR PROTEIN; UNCLASSIFIED DRUG; TUMOR MARKER; TUMOR PROTEIN, TRANSLATIONALLY-CONTROLLED 1;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; APICOMPLEXAN LIFE CYCLE STAGE; ARTICLE; BLOOD; BRAIN MALARIA; CLONE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DOWN REGULATION; ERYTHROCYTE; FEMALE; HOST CELL; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LIVER; MOUSE; NEUROPATHOLOGY; NEUTROPHIL; NONHUMAN; PARASITEMIA; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RODENT MODEL; SPOROZOITE; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; KNOCKOUT MOUSE; MALARIA; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; TREATMENT OUTCOME;

MAMMALIA; MUS; PLASMODIUM BERGHEI; RODENTIA;

ANIMALS; BIOMARKERS, TUMOR; DISEASE MODELS, ANIMAL; HOST-PATHOGEN INTERACTIONS; INTERLEUKIN-6; LIVER; MALARIA; MICE; MICE, KNOCKOUT; PLASMODIUM BERGHEI; TREATMENT OUTCOME;

EID: 84924292749     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12382     Document Type: Article

References (48)

1. Amzallag, A., Passer, B.J., Allanic, D., Segura, E., Théry, C., Goud, B., etal. (2004) TSAP6 facilitates the secretion of translationally controlled tumour protein/histamine-releasing factor via a nonclassical pathway. J Biol Chem 279: 46104-46122.
2. Arcuri, F., Papa, S., Carducci, A., Romagnoli, R., Liberatori, S., Riparbelli, M.G., etal. (2004) Translationally controlled tumor protein (TCTP) in the human prostate and prostate cancer cells: expression, distribution, and calcium binding activity. Prostate 60: 130-140.
3. Augustijn, K.D., Kleemann, R., Thompson, J., Kooistra, T., Crawford, C.E., Reece, S.E., etal. (2007) Functional characterization of the Plasmodium falciparum and P.berghei homologues of macrophage migration inhibitory factor. Infect Immun 75: 1116-1128.
4. Beghdadi, W., Porcherie, A., Schneider, B.S., Dubayle, D., Peronet, R., Huerre, M., etal. (2008) Inhibition of histamine-mediated signaling confers significant protection against severe malaria in mouse models of disease. J Exp Med 205: 395-408.
5. Bhattacharya, U., Roy, S., Kar, P.K., Sarangi, B., and Lahiri, S.C. (1988) Histamine & kinin system in experimental malaria. Indian J Med Res 88: 558-563.
6. Bheekha-Escura, R., MacGlashan, D.W., Langdon, J.M., and MacDonald, S.M. (2000) Human recombinant histamine-releasing factor activates human eosinophils and the eosinophilic cell line, AML14-3D10. Blood 96: 2191-2198.
7. Bhisutthibhan, J., Philbert, M.A., Fujioka, H., Aikawa, M., and Meshnick, S.R. (1999) The Plasmodium falciparum translationally controlled tumor protein: subcellular localization and calcium binding. Eur J Cell Biol 78: 665-670.
8. Butler, N.S., Schmidt, N.W., Vaughan, A.M., Aly, A.S., Kappe, S.H., and Harty, J.T. (2011) Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell Host Microbe 9: 451-462.
9. Chitpatima, S.T., Makrides, S., Bandyopadhyay, R., and Brawerman, G. (1988) Nucleotide sequence of a major messenger RNA for a 21 kilodalton polypeptide that is under translational control in mouse tumour cells. Nucleic Acids Res 16: 2350.
10. Chung, S., Kim, M., Choi, W., Chung, J., and Lee, K. (2000) Expression of translationally controlled tumor protein mRNA in human colon cancer. Cancer Lett 156: 185-190.
11. van Dijk, M.R., Douradinha, B., Franke-Fayard, B., Heussler, V., van Dooren, M.W., van Schaijk, B., etal. (2005) Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proc Natl Acad Sci USA 102: 12194-12199.
12. Enwonwu, C.O., Afolabi, B.M., Salako, L.O., Idigbe, E.O., and Bashirelah, N. (2000) Increased plasma levels of histidine and histamine in falciparum malaria: relevance to severity of infection. J Neural Transm 107: 1273-1287.
13. Fenner, B.J., Scannell, M., and Prehn, J.H. (2010) Expanding the substantial interactome of NEMO using protein microarrays. PLoS ONE 5: e8799.
14. Gachet, Y., Tournier, S., Lee, M., Lazaris-Karatzas, A., Poulton, T., and Bommer, U.A. (1999) The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J Cell Sci 112 (Part 8): 1257-1271.
15. Gross, B., Gaestel, M., Boehm, H., and Bielka, H. (1989) cDNA sequence coding for a translationally controlled human tumour protein. Nucleic Acids Res 17: 8367.
16. Haussig, J.M., Matuschewski, K., and Kooij, T.W. (2011) Inactivation of a Plasmodium apicoplast protein attenuates formation of liver merozoites. Mol Microbiol 81: 1511-1525.
17. Heppner, D.G., Jr, Kester, K.E., Ockenhouse, C.F., Tornieporth, N., Ofori, O., Lyon, J.A., etal. (2005) Towards an RTS, S-based, multi-stage, multi-antigen vaccine against falciparum malaria: progress at the Walter Reed Army Institute of Research. Vaccine 23: 2243-2250.
18. Ishino, T., Chinzei, Y., and Yuda, M. (2005) Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Mol Microbiol 58: 1264-1275.
19. Ishino, T., Orito, Y., Chinzei, Y., and Yuda, M. (2006) A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol Microbiol 59: 1175-1184.
20. Kashiwakura, J.C., Ando, T., Matsumoto, K., Kimura, M., Kitaura, J., Matho, M.H., etal. (2012) Histamine-releasing factor has a proinflammatory role in mouse models of asthma and allergy. J Clin Invest 122: 218-228.
21. Labaied, M., Harupa, A., Dumpit, R.F., Coppens, I., Mikolajczak, S.A., and Kappe, S.H. (2007) Plasmodium yoelii sporozoites with simultaneous deletion of P52 and P36 are completely attenuated and confer sterile immunity against infection. Infect Immun 75: 3758-3768.
22. Macdonald, S.M. (2012) Potential role of histamine releasing factor (HRF) as a therapeutic target for treating asthma and allergy. J Asthma Allergy 5: 51-59.
23. MacDonald, S.M., Rafnar, T., Langdon, J., and Lichtenstein, L.M. (1995) Molecular identification of an IgE-dependent histamine-releasing factor. Science 269: 688-690.
24. MacDonald, S.M., Bhisutthibhan, J., Shapiro, T.A., Rogerson, S.J., Taylor, T.E., Tembo, M., etal. (2001) Immune mimicry in malaria: Plasmodium falciparum secretes a functional histamine-releasing factor homolog in vitro and in vivo. Proc Natl Acad Sci USA 98: 10829-10832.
25. Maegraith, B., and Fletcher, A. (1972) The pathogenesis of mammalian malaria. Adv Parasitol 10: 49-75.
26. Maheshwari, R.K. (1990) The role of cytokines in malaria infection. Bull World Health Organ 68 (Suppl.): 138-144.
27. Miller, J.L., Harupa, A., Kappe, S.H., and Mikolajczak, S.A. (2012) Plasmodium yoelii macrophage migration inhibitory factor is necessary for efficient liver-stage development. Infect Immun 80: 1399-1407.
28. Nemeth, E., Rivera, S., Gabayan, V., Keller, C., Taudorf, S., Pedersen, B.K., and Ganz, T. (2004) IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest 113: 1271-1276.
29. Nussler, A., Drapier, J.C., Renia, L., Pied, S., Miltgen, F., Gentilini, M., and Mazier, D. (1991) L-arginine-dependent destruction of intrahepatic malaria parasites in response to tumor necrosis factor and/or interleukin 6 stimulation. Eur J Immunol 21: 227-230.
30. Pelleau, S., Diop, S., Dia Badiane, M., Vitte, J., Beguin, P., Nato, F., etal. (2012) Enhanced basophil reactivities during severe malaria and their relationship with the Plasmodium falciparum histamine-releasing factor translationally controlled tumor protein. Infect Immun 80: 2963-2970.
31. Pied, S., Civas, A., Berlot-Picard, F., Renia, L., Miltgen, F., Gentilini, M., etal. (1992) IL-6 induced by IL-1 inhibits malaria pre-erythrocytic stages but its secretion is down-regulated by the parasite. J Immunol 148: 197-201.
32. Portugal, S., Drakesmith, H., and Mota, M.M. (2011) Superinfection in malaria: plasmodium shows its iron will. EMBO Rep 12: 1233-1242.
33. Puga, I., Cols, M., Barra, C.M., He, B., Cassis, L., Gentile, M., etal. (2012) B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat Immunol 13: 170-180.
34. Rho, S.B., Lee, J.H., Park, M.S., Byun, H.J., Kang, S., Seo, S.S., etal. (2011) Anti-apoptotic protein TCTP controls the stability of the tumor suppressor p53. FEBS Lett 585: 29-35.
35. Rid, R., Onder, K., Trost, A., Bauer, J., Hintner, H., Ritter, M., etal. (2010) H2O2-dependent translocation of TCTP into the nucleus enables its interaction with VDR in human keratinocytes: TCTP as a further module in calcitriol signalling. J Steroid Biochem Mol Biol 118: 29-40.
36. Schofield, L., Ferreira, A., Altszuler, R., Nussenzweig, V., and Nussenzweig, R.S. (1987) Interferon-gamma inhibits the intrahepatocytic development of malaria parasites in vitro. J Immunol 139: 2020-2025.
37. Schroeder, J.T., Lichtenstein, L.M., and MacDonald, S.M. (1997) Recombinant histamine-releasing factor enhances IgE-dependent IL-4 and IL-13 secretion by human basophils. J Immunol 159: 447-452.
38. Srichaikul, T., Archararit, N., Siriasawakul, T., and Viriyapanich, T. (1976) Histamine changes in Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 70: 36-38.
39. Sun, T., Holowka, T., Song, Y., Zierow, S., Leng, L., Chen, Y., etal. (2012) A Plasmodium-encoded cytokine suppresses T-cell immunity during malaria. Proc Natl Acad Sci USA 109: E2117-E2126.
40. Susini, L., Besse, S., Duflaut, D., Lespagnol, A., Beekman, C., Fiucci, G., etal. (2008) TCTP protects from apoptotic cell death by antagonizing bax function. Cell Death Differ 15: 1211-1220.
41. Terebuh, P.D., Otterness, I.G., Strieter, R.M., Lincoln, P.M., Danforth, J.M., Kunkel, S.L., and Chensue, S.W. (1992) Biologic and immunohistochemical analysis of interleukin-6 expression in vivo. Constitutive and induced expression in murine polymorphonuclear and mononuclear phagocytes. Am J Pathol 140: 649-657.
42. Vercoutter-Edouart, A.S., Czeszak, X., Crepin, M., Lemoine, J., Boilly, B., Le Bourhis, X., etal. (2001) Proteomic detection of changes in protein synthesis induced by fibroblast growth factor-2 in MCF-7 human breast cancer cells. Exp Cell Res 262: 59-68.
43. Vonakis, B.M., Sora, R., Langdon, J.M., Casolaro, V., and MacDonald, S.M. (2003) Inhibition of cytokine gene transcription by the human recombinant histamine-releasing factor in human T lymphocytes. J Immunol 171: 3742-3750.
44. Vreden, S.G., van den Broek, M.F., Oettinger, M.C., Verhave, J.P., Meuwissen, J.H., and Sauerwein, R.W. (1992) Cytokines inhibit the development of liver schizonts of the malaria parasite Plasmodium berghei in vivo. Eur J Immunol 22: 2271-2275.
45. Wykes, M.N., Zhou, Y.H., Liu, X.Q., and Good, M.F. (2005) Plasmodium yoelii can ablate vaccine-induced long-term protection in mice. J Immunol 175: 2510-2516.
46. Xu, A., Bellamy, A.R., and Taylor, J.A. (1999) Expression of translationally controlled tumour protein is regulated by calcium at both the transcriptional and translational level. Biochem J 342: 683-689.
47. Yang, Y., Yang, F., Xiong, Z., Yan, Y., Wang, X., Nishino, M., etal. (2005) An N-terminal region of translationally controlled tumor protein is required for its antiapoptotic activity. Oncogene 24: 4778-4788.
48. Zhang, D., Li, F., Weidner, D., Mnjoyan, Z.H., and Fujise, K. (2002) Physical and functional interaction between myeloid cell leukemia 1 protein (MCL1) and Fortilin. The potential role of MCL1 as a fortilin chaperone. J Biol Chem 277: 37430-37438.