Inhibition of megakaryocyte development in the bone marrow underlies dengue virus-induced thrombocytopenia in humanized mice

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11648-11658

  Sridharan, Aishwarya ^a,b   Chen, Qingfeng ^b,c   Tang, Kin Fai ^d   Ooi, Eng Eong ^b,d   Hibberd, Martin L ^a,e   Chenb, Jianzhu ^b,f  

^a SINGAPORE MIT ALLIANCE   (Singapore)

^b SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d DUKE NUS MEDICAL SCHOOL   (Singapore)

^e GENOME INSTITUTE OF SINGAPORE   (Singapore)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

THROMBOPOIETIN;

ADOPTIVE TRANSFER; ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL MATURATION; CLINICAL FEATURE; DENGUE VIRUS INDUCED THROMBOCYTOPENIA; FETUS LIVER; HUMAN; HUMAN CELL; LEUKOPENIA; LIVER CELL; MACROPHAGE; MEGAKARYOCYTE; MONOCYTE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; THROMBOCYTE; THROMBOCYTOPENIA; THROMBOCYTOPOIESIS; VIRUS STRAIN;

ANIMALS; BONE MARROW; DENGUE; DENGUE VIRUS; HUMANS; MEGAKARYOCYTES; MICE; MICE, SCID; THROMBOCYTOPENIA;

EID: 84886897854     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01156-13     Document Type: Article

References (30)

1. World Health Organization. 2009. Dengue guidelines for diagnosis treatment prevention and control. World Health Organization, Geneva, Switzerland.
2. Thon JN, Italiano JE. 2012. Platelets: production, morphology and ultrastructure. Handb. Exp. Pharmacol. 210:3-22.
3. Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, Jin DK, Dias S, Zhang F, Hartman TE, Hackett NR, Crystal RG, Witte L, Hicklin DJ, Bohlen P, Eaton D, Lyden D, de Sauvage F, Rafii S. 2004.Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat. Med. 10:64-71.
4. Tomer A. 2004. Human marrow megakaryocyte differentiation: multiparameter correlative analysis identifies von Willebrand factor as a sensitive and distinctive marker for early (2N and 4N) megakaryocytes. Blood 104: 2722-2727.
5. Kaushansky K. 2006. Lineage-specific hematopoietic growth factors. N. Engl. J. Med. 354:2034-2045.
6. Wolber EM, Jelkmann W. 2002. Thrombopoietin: the novel hepatic hormone. News Physiol. Sci. 17:6-10.
7. Wang S, He R, Patarapotikul J, Innis BL, Anderson R. 1995. Antibodyenhanced binding of dengue-2 virus to human platelets. Virology 213: 254-257.
8. Saito M, Oishi K, Inoue S, Dimaano EM, Alera MTP, Robles AMP, Estrella BD, Kumatori A, Moji K, Alonzo MT, Buerano CC, Matias RR, Morita K, Natividad FF, Nagatake T. 2004. Association of increased platelet-associated immunoglobulins with thrombocytopenia and the severity of disease in secondary dengue virus infections. Clin. Exp. Immunol. 138:299-303.
9. Lin CF, Lei HY, Liu CC, Liu HS, Yeh TM, Wang ST, Yang TI, Sheu FC, Kuo CF, Lin YS. 2001. Generation of IgM anti-platelet autoantibody in dengue patients. J. Med. Virol. 63:143-149.
10. Sun DS, King CC, Huang HS, Shih YL, Lee CC, Tsai WJ, Yu CC, Chang HH. 2007. Antiplatelet autoantibodies elicited by dengue virus nonstructural protein 1 cause thrombocytopenia and mortality in mice. J. Thromb Haemost. 5:2291-2299.
11. Nelson ER, Bierman HR, Chulajata R. 1964. Hematologic findings in the 1960 hemorrhagic fever epidemic (dengue) in Thailand. Am. J. Trop. Med. Hyg. 13:642-649.
12. La Russa VF, Innis BL. 1995. Mechanisms of dengue virus-induced bone marrow suppression. Baillieres Clin. Haematol. 8:249-270.
13. Noisakran S, Onlamoon N, Hsiao HM, Clark KB, Villinger F, Ansari AA, Perng GC. 2012. Infection of bone marrow cells by dengue virus in vivo. Exp. Hematol. 40:250-259.e4.
14. Ishikawa F, Yasukawa M, Lyons B, Yoshida S, Miyamoto T, Yoshimoto G, Watanabe T, Akashi K, Shultz LD, Harada M. 2005. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood 106:1565-1573.
15. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, ChaleffS, Kotb M, Gillies SD, King M, Mangada J, Greiner DL, Handgretinger R. 2005. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174:6477-6489.
16. Mota J, Rico-Hesse R. 2009. Humanized mice show clinical signs of dengue fever according to infecting virus genotype. J. Virol. 83:8638-8645.
17. Mota J, Rico-Hesse R. 2011. Dengue virus tropism in humanized mice recapitulates human dengue fever. PLoS One 6:e20762.
18. Jaiswal S, Pearson T, Friberg H, Shultz LD, Greiner DL, Rothman AL, Mathew A. 2009. Dengue virus infection and virus-specific HLA-A2 restricted immune responses in humanized NOD-scid IL2rgammanull mice. PLoS One 4:e7251.
19. Chen Q, Khoury M, Limmon G, Choolani M, Chan JK, Chen J. 2013. Human fetal hepatic progenitor cells are distinct from, but closely related to, hematopoietic stem/progenitor cells. Stem Cells. [Epub ahead of print.]
20. Ito M, Hiramatsu H, Kobayashi K, Suzue K, Kawahata M, Hioki K, Ueyama Y, Koyanagi Y, Sugamura K, Tsuji K, Heike T, Nakahata T. 2002. NOD/SCID/gamma(c) (null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 100:3175-3182.
21. Lepus CM, Gibson TF, Gerber SA, Kawikova I, Szczepanik M, Hossain J, Ablamunits V, Kirkiles-Smith N, Herold KC, Donis RO, Bothwell AL, Pober JS, Harding MJ. 2009. Comparison of human fetal liver, umbilical cord blood, and adult blood hematopoietic stem cell engraftment in NOD-scid/gammac-/-, Balb/c-Rag1-/-gammac-/-, and C.B-17-scid/bg immunodeficient mice. Hum. Immunol. 70:790-802.
22. Low JGH, Ooi EE, Tolfvenstam T, Leo YS, Hibberd ML, Ng LC, Lai YL, Yap GSL, Li CSC, Vasudevan SG, Ong A. 2006. Early dengue infection and outcome study (EDEN)-study design and preliminary findings. Ann. Acad. Med. Singapore 35:783-789.
23. Chen Q, He F, Kwang J, Chan JKY, Chen J. 2012. GM-CSF and IL-4 stimulate antibody responses in humanized mice by promoting T, B, and dendritic cell maturation. J. Immunol. 189:5223-5229.
24. Sabin AB, Schlesinger RW. 1945. Production of immunity to dengue with virus modified by propagation in mice. Science 101:640-642.
25. Wolber EM, Dame C, Fahnenstich H, Hofmann D, Bartmann P, Jelkmann W, Fandrey J. 1999. Expression of the thrombopoietin gene in human fetal and neonatal tissues. Blood 94:97-105.
26. Sung JM, Lee CK, Wu-Hsieh BA. 2012. Intrahepatic infiltrating NK and CD8 T cells cause liver cell death in different phases of dengue virus infection. PLoS One 7:e46292.
27. Liu CC, Huang KJ, Lin YS, Yeh TM, Liu HS, Lei HY. 2002. Transient CD4/CD8 ratio inversion and aberrant immune activation during dengue virus infection. J. Med. Virol. 68:241-252.
28. Carballido JM, Namikawa R, Carballido-Perrig N, Antonenko S, Roncarolo MG, de Vries JE. 2000. Generation of primary antigen-specific human T- and B-cell responses in immunocompetent SCID-hu mice. Nat. Med. 6:103-106.
29. Legrand N, Weijer K, Spits H. 2006. Experimental models to study development and function of the human immune system in vivo. J. Immunol. 176:2053-2058.
30. Shultz LD, Ishikawa F, Greiner DL. 2007. Humanized mice in translational biomedical research. Nat. Rev. Immunol. 7:118-130.