Seoul virus-infected rat lung endothelial cells and alveolar macrophages differ in their ability to support virus replication and induce regulatory T cell phenotypes

Journal of Virology

Volumn 86, Issue 21, 2012, Pages 11845-11855

  Li, Wei ^a   Klein, Sabra L ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CELL SURFACE MARKER; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; PROGRAMMED DEATH 1 LIGAND 1; RANTES; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL CONTACT; CELL CULTURE; CELL TYPE; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; HELPER CELL; LUNG ALVEOLUS MACROPHAGE; LUNG ENDOTHELIAL CELL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; MALE; NONHUMAN; PERSISTENT VIRUS INFECTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY T LYMPHOCYTE; SEOUL VIRUS; SEOUL VIRUS INFECTION; T LYMPHOCYTE; VIRUS INFECTION; VIRUS PARTICLE; VIRUS REPLICATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; ENDOTHELIAL CELLS; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; MACROPHAGES, ALVEOLAR; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEOUL VIRUS; T-LYMPHOCYTES, REGULATORY; VIRUS REPLICATION;

HANTAVIRUS; RATTUS; SEOUL VIRUS;

EID: 84869009392     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01233-12     Document Type: Article

References (81)

1. Alard P, Clark SL, Kosiewicz MM. 2004. Mechanisms of tolerance induced by TGF beta-treated APC: CD4 regulatory T cells prevent the induction of the immune response possibly through a mechanism involving TGF beta. Eur. J. Immunol. 34:1021-1030.
2. Au RY, Jedlicka AE, Li W, Pekosz A, Klein SL. 2010. Seoul virus suppresses NF-kappaB-mediated inflammatory responses of antigen presenting cells from Norway rats. Virology 400:115-127.
3. Barber DL, et al. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:682-687.
4. Bas A, Forsberg G, Hammarstrom S, Hammarstrom ML. 2004. Utility of the housekeeping genes 18S rRNA, beta-actin and glyceraldehyde-3-phosphate-dehydrogenase for normalization in real-time quantitative reverse transcriptase-polymerase chain reaction analysis of gene expression in human T lymphocytes. Scand. J. Immunol. 59:566-573
5. Bjorkstrom NK, et al. 2011. Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J. Exp. Med. 208:13-21.
6. Blackburn SD, et al. 2010. Tissue-specific differences in PD-1 and PD-L1 expression during chronic viral infection: implications for CD8 T-cell exhaustion. J. Virol. 84:2078-2089.
7. Blattman JN, Wherry EJ, Ha SJ, van der Most RG, Ahmed R. 2009.Impact of epitope escape on PD-1 expression and CD8 T-cell exhaustion during chronic infection. J. Virol. 83:4386-4394.
8. Boni C, et al. 2007. Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J. Virol. 81:4215- 4225.
9. Borges AA, et al. 2008. Role of mixed Th1 and Th2 serum cytokines on pathogenesis and prognosis of hantavirus pulmonary syndrome. Microbes Infect. 10:1150-1157.
10. Botten J, et al. 2000. Experimental infection model for Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus). Proc. Natl. Acad. Sci. U.S.A. 97:10578-10583.
11. Botten J, et al. 2003. Persistent Sin Nombre virus infection in the deer mouse (Peromyscus maniculatus) model: sites of replication and strandspecific expression. J. Virol. 77:1540-1550.
12. Cabrera R, et al. 2004. An immunomodulatory role for CD4(+)CD25(+) regulatory T lymphocytes in hepatitisCvirus infection. Hepatology 40:1062-1071.
13. Cavanaugh PG, Nicolson GL. 1989. Purification and some properties of a lung-derived growth factor that differentially stimulates the growth of tumor cells metastatic to the lung. Cancer Res. 49:3928-3933.
14. Chen LB, Yang WS. 1990. Abnormalities of T cell immunoregulation in hemorrhagic fever with renal syndrome. J. Infect. Dis. 161:1016-1019.
15. Childs JE, Glass GE, Korch GW, LeDuc JW. 1989. Effects of hantaviral infection on survival, growth and fertility in wild rat (Rattus norvegicus) populations of Baltimore, Maryland. J. Wildl. Dis. 25:469-476.
16. du Bois RM. 1985. The alveolar macrophage. Thorax 40:321-327.
17. Easterbrook JD, Klein SL. 2008. Immunological mechanisms mediating hantavirus persistence in rodent reservoirs. PLoS Pathog. 4:e1000172. doi: 10.1371/journal.ppat.1000172.
18. Easterbrook JD, Klein SL. 2008. Seoul virus enhances regulatory and reduces proinflammatory responses in male Norway rats. J. Med. Virol.80:1308-1318.
19. Easterbrook JD, Zink MC, Klein SL. 2007. Regulatory T cells enhance persistence of the zoonotic pathogen Seoul virus in its reservoir host. Proc. Natl. Acad. Sci. U.S.A. 104:15502-15507.
20. Elliott LH, et al. 1994. Isolation of the causative agent of hantavirus pulmonary syndrome. Am. J. Trop. Med. Hyg. 51:102-108.
21. Fels AO, Cohn ZA. 1986. The alveolar macrophage. J. Appl. Physiol. 60:353-369.
22. Francisco LM, et al. 2009. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J. Exp. Med. 206:3015-3029.
23. Freeman GJ, et al. 2000. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192:1027-1034.
24. Gavrilovskaya IN, Gorbunova EE, Mackow ER. 2010. Pathogenic hantaviruses direct the adherence of quiescent platelets to infected endothelial cells. J. Virol. 84:4832-4839.
25. Gavrilovskaya IN, Gorbunova EE, Mackow NA, Mackow ER. 2008. Hantaviruses direct endothelial cell permeability by sensitizing cells to the vascular permeability factor VEGF, while angiopoietin 1 and sphingosine 1-phosphate inhibit hantavirus-directed permeability. J. Virol. 82:57975806.
26. Hall CH, Kassel R, Tacke RS, Hahn YS. 2010. HCV+ hepatocytes induce human regulatory CD4+ T cells through the production of TGF-beta.PLoS One 5:e12154. doi:10.1371/journal.pone.0012154.
27. Hannah MF, Bajic VB, Klein SL. 2008. Sex differences in the recognition of and innate antiviral responses to Seoul virus in Norway rats. Brain Behav. Immun. 22:503-516.
28. Hoshino Y, et al. 2007. Mechanisms of polymorphonuclear neutrophilmediated induction of HIV-1 replication in macrophages during pulmonary tuberculosis. J. Infect. Dis. 195:1303-1310.
29. Hutchinson KL, Rollin PE, Peters CJ. 1998. Pathogenesis of a North American hantavirus, Black Creek Canal virus, in experimentally infected Sigmodon hispidus. Am. J. Trop. Med. Hyg. 59:58-65.
30. Jiang H, et al. 2008. Hantaan virus induces toll-like receptor 4 expression, leading to enhanced production of beta interferon, interleukin-6 and tumor necrosis factor-alpha. Virology 380:52-59.
31. Kariwa H, et al. 1996. Modes of Seoul virus infections: persistency in newborn rats and transiency in adult rats. Arch. Virol. 141:2327-2338.
32. Keir ME, et al. 2006. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J. Exp. Med. 203:883-895.
33. Khaiboullina SF, Netski DM, Krumpe P, St Jeor SC. 2000. Effects of tumor necrosis factor alpha on sin nombre virus infection in vitro. J. Virol. 74:11966-11971.
34. Khaiboullina SF, St Jeor SC. 2002. Hantavirus immunology. Viral Immunol. 15:609-625.
35. Kilpatrick ED, et al. 2004. Role of specific CD8+ T cells in the severity of a fulminant zoonotic viral hemorrhagic fever, hantavirus pulmonary syndrome. J. Immunol. 172:3297-3304.
36. Kitamura T, et al. 1983. Isolation of virus causing hemorrhagic fever with renal syndrome (HFRS) through a cell culture system. Jpn. J. Med. Sci. Biol. 36:17-25.
37. Klein SL, et al. 2004. Differential expression of immunoregulatory genes in male and female Norway rats following infection with Seoul virus. J. Med. Virol. 74:180-190.
38. Kosiewicz MM, Alard P. 2004. Tolerogenic antigen-presenting cells: regulation of the immune response by TGF-beta-treated antigen-presenting cells. Immunol. Res. 30:155-170.
39. Kraus AA, Priemer C, Heider H, Kruger DH, Ulrich R. 2005. Inactivation of Hantaan virus-containing samples for subsequent investigations outside biosafety level 3 facilities. Intervirology 48:255-261.
40. Kraus AA, et al. 2004. Differential antiviral response of endothelial cells after infection with pathogenic and nonpathogenic hantaviruses. J. Virol. 78:6143-6150.
41. Krupnick AS, et al. 2005. Murine vascular endothelium activates and induces the generation of allogeneic CD4+25+Foxp3+ regulatory T cells. J. Immunol. 175:6265-6270.
42. Lambrecht BN. 2006. Alveolar macrophage in the driver's seat. Immunity 24:366-368.
43. Lee PW, Yanagihara R, Gibbs CJ, Jr, Gajdusek DC. 1986. Pathogenesis of experimental Hantaan virus infection in laboratory rats. Arch. Virol. 88:57-66.
44. Linderholm M, Ahlm C, Settergren B, Waage A, Tarnvik A. 1996. Elevated plasma levels of tumor necrosis factor (TNF)-alpha, soluble TNF receptors, interleukin (IL)-6, and IL-10 in patients with hemorrhagic fever with renal syndrome. J. Infect. Dis. 173:38-43.
45. Maes P, Clement J, Gavrilovskaya I, Van Ranst M. 2004. Hantaviruses:immunology, treatment, and prevention. Viral Immunol. 17:481-497.
46. Maier H, Isogawa M, Freeman GJ, Chisari FV. 2007. PD-1:PD-L1 interactions contribute to the functional suppression of virus-specific CD8+ T lymphocytes in the liver. J. Immunol. 178:2714-2720.
47. Markotic A, et al. 1999. Role of peripheral blood mononuclear cell (PBMC) phenotype changes in the pathogenesis of haemorrhagic fever with renal syndrome (HFRS). Clin. Exp. Immunol. 115:329-334.
48. Marsac D, et al. 2011. Infection of human monocyte-derived dendritic cells by ANDES Hantavirus enhances pro-inflammatory state, the secretion of active MMP-9 and indirectly enhances endothelial permeability. Virol. J. 8:223.
49. Mori M, et al. 1999. High levels of cytokine-producing cells in the lung tissues of patients with fatal hantavirus pulmonary syndrome. J. Infect. Dis. 179:295-302.
50. Mueller SN, et al. 2010. PD-L1 has distinct functions in hematopoietic and nonhematopoietic cells in regulating T cell responses during chronic infection in mice. J. Clin. Invest. 120:2508-2515.
51. Muhlbauer M, et al. 2006. PD-L1 is induced in hepatocytes by viral infection and by interferon-alpha and-gamma and mediates T cell apoptosis. J. Hepatol. 45:520-528.
52. Murphy J, Summer R, Wilson AA, Kotton DN, Fine A. 2008. The prolonged life-span of alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 38:380-385.
53. Nagai T, et al. 1985. Isolation of haemorrhagic fever with renal syndrome virus from leukocytes of rats and virus replication in cultures of rat and human macrophages. J. Gen. Virol. 66:1271-1278.
54. Nakata K, et al. 1997. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. Am. J. Respir. Crit. Care Med. 155:996-1003.
55. Noone CM, et al. 2008. Natural killer cells regulate T-cell proliferation during human parainfluenza virus type 3 infection. J. Virol. 82:9299-9302.
56. Oh S, McCaffery JM, Eichelberger MC. 2000. Dose-dependent changes in influenza virus-infected dendritic cells result in increased allogeneic T-cell proliferation at low, but not high, doses of virus. J. Virol. 74:5460-5469.
57. Peng G, et al. 2008. PD-1 upregulation is associated with HBV-specific T cell dysfunction in chronic hepatitis B patients. Mol. Immunol. 45:963-970.
58. Pensiero MN, Sharefkin JB, Dieffenbach CW, Hay J. 1992. Hantaan virus infection of human endothelial cells. J. Virol. 66:5929-5936.
59. Plekhova NG, et al. 2005. Metabolic activity of macrophages infected with hantavirus, an agent of hemorrhagic fever with renal syndrome. Biochemistry 70:990-997.
60. Prescott J, et al. 2010. New World hantaviruses activate IFNlambda production in type I IFN-deficient vero E6 cells. PLoS One 5:e11159. doi:10.1371/journal.pone.0011159.
61. Quigley M, et al. 2010. Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat. Med. 16:1147-1151.
62. Raftery MJ, Kraus AA, Ulrich R, Kruger DH, Schonrich G. 2002. Hantavirus infection of dendritic cells. J. Virol. 76:10724-10733.
63. Rehn B, Bruch J, Zou T, Hobusch G. 1992. Recovery of rat alveolar macrophages by bronchoalveolar lavage under normal and activated conditions. Environ. Health Perspect. 97:11-16.
64. Rowe RK, Suszko JW, Pekosz A. 2008. Roles for the recycling endosome,Rab8, and Rab11 in hantavirus release from epithelial cells. Virology 382:239-249.
65. Safronetz D, et al. 2011. Pathogenesis and host response in Syrian hamsters following intranasal infection with Andes virus. PLoS Pathog. 7:e1002426. doi:10.1371/journal.ppat.1002426.
66. Sanduzzi A, Fraziano M, Mariani F. 2001. Monocytes/macrophages in HIV infection and tuberculosis. J. Biol. Regul. Homeost. Agents 15:294-298.
67. Schonrich G, et al. 2008. Hantavirus-induced immunity in rodent reservoirs and humans. Immunol. Rev. 225:163-189.
68. Schountz T, et al. 2007. Regulatory T cell-like responses in deer mice persistently infected with Sin Nombre virus. Proc. Natl. Acad. Sci. U.S.A. 104:15496-15501.
69. Shrivastava-Ranjan P, Rollin PE, Spiropoulou CF. 2010. Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J. Virol. 84:11227-11234.
70. Stoltz M, et al. 2011. A model system for in vitro studies of bank vole borne viruses. PLoS One 6:e28992. doi:10.1371/journal.pone.0028992.
71. Sundstrom JB, et al. 2001. Hantavirus infection induces the expression of RANTES and IP-10 without causing increased permeability in human lung microvascular endothelial cells. J. Virol. 75:6070-6085.
72. Taflin C, et al. 2011. Human endothelial cells generate Th17 and regulatory T cells under inflammatory conditions. Proc. Natl. Acad. Sci. U.S.A. 108:2891-2896.
73. Temonen M, et al. 1993. Susceptibility of human cells to Puumala virus infection. J. Gen. Virol. 74:515-518.
74. Terajima M, Hayasaka D, Maeda K, Ennis FA. 2007. Immunopathogenesis of hantavirus pulmonary syndrome and hemorrhagic fever with renal syndrome: do CD8+T cells trigger capillary leakage in viral hemorrhagic fevers? Immunol. Lett. 113:117-120.
75. Urbani S, et al. 2006. PD-1 expression in acute hepatitis C virus (HCV) infection is associated with HCV-specific CD8 exhaustion. J. Virol. 80:11398-11403.
76. Walker JD, Maier CL, Pober JS. 2009. Cytomegalovirus-infected human endothelial cells can stimulate allogeneic CD4+memory T cells by releasing antigenic exosomes. J. Immunol. 182:1548-1559.
77. Wewers MD, Rennard SI, Hance AJ, Bitterman PB, Crystal RG. 1984. Normal human alveolar macrophages obtained by bronchoalveolar lavage have a limited capacity to release interleukin-1. J. Clin. Invest. 74:2208-2218.
78. Yanagihara R, Amyx HL, Gajdusek DC. 1985. Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). J. Virol. 55:34-38.
79. Yang G, et al. 2007. Association of CD4+CD25+Foxp3+ regulatory T cells with chronic activity and viral clearance in patients with hepatitis B. Int. Immunol. 19:133-140.
80. Yoshizawa K, et al. 2010. Expansion of CD4(+)CD25(+)FoxP3(+) regulatory T cells in hepatitis C virus-related chronic hepatitis, cirrhosis and hepatocellular carcinoma. Hepatol Res. 40:179-187.
81. Zhu LY, Chi LJ, Wang X, Zhou H. 2009. Reduced circulating CD4+CD25+ cell populations in haemorrhagic fever with renal syndrome. Clin. Exp. Immunol. 156:88-96.