Differential Expression of Chemokines and Their Receptors in Adult and Neonatal Macrophages Infected with Human or Avian Influenza Viruses

Abstract In 1997, avian influenza virus H5N1 was transmitted directly from chicken to human and resulted in a severe disease that had a higher mortality rate in adults than in children. The characteristic mononuclear leukocyte infiltration in the lung and the high inflammatory response in H5N1 infection prompted us to compare the chemokine responses between influenza virus–infected adult and neonatal monocyte-derived macrophages (MDMs). The effects of avian influenza virus A/Hong Kong/483/97 (H5N1) (H5N1/97), its precursor A/Quail/Hong Kong/G1/97 (H9N2) (H9N2/G1), and human influenza virus A/Hong Kong/54/98 (H1N1) (H1N1/98) were compared. Significantly higher expression of CCL2, CCL3, CCL5, and CXCL10 was induced by avian influenza viruses than by human influenza virus. Moreover, the increase in CCL3 expression in H5N1/97-infected adult MDMs was significantly higher than that in neonatal MDMs. Enhanced expression of CCR1 and CCR5 was found in avian virus–infected adult MDMs. The strong induction of chemokines and their receptors by avian influenza viruses, particularly in adult MDMs, may account for the severity of H5N1 disease

[1]  J. Peiris,et al.  Functional Tumor Necrosis Factor–Related Apoptosis-Inducing Ligand Production by Avian Influenza Virus–Infected Macrophages , 2006, The Journal of infectious diseases.

[2]  Z. Brown,et al.  Chemokine Receptors , 2006, Treatments in respiratory medicine.

[3]  David E. Swayne,et al.  Pathogenicity of Influenza Viruses with Genes from the 1918 Pandemic Virus: Functional Roles of Alveolar Macrophages and Neutrophils in Limiting Virus Replication and Mortality in Mice , 2005, Journal of Virology.

[4]  N. Kajiwara,et al.  CCL5-CCR5 interaction provides antiapoptotic signals for macrophage survival during viral infection , 2005, Nature Medicine.

[5]  Jeffery K. Taubenberger,et al.  Characterization of the 1918 influenza virus polymerase genes , 2005, Nature.

[6]  Y. Lau,et al.  Chemokine up-regulation in SARS-coronavirus–infected, monocyte-derived human dendritic cells , 2005, Blood.

[7]  Angus Nicoll,et al.  Avian influenza A (H5N1) infection in humans. , 2005, The New England journal of medicine.

[8]  R. Webster,et al.  Pathogenesis of Hong Kong H5N1 influenza virus NS gene reassortants in mice: the role of cytokines and B- and T-cell responses. , 2005, The Journal of general virology.

[9]  R. Garofalo,et al.  A comparison of epidemiologic and immunologic features of bronchiolitis caused by influenza virus and respiratory syncytial virus , 2005, Journal of medical virology.

[10]  Silvano Sozzani,et al.  The chemokine system in diverse forms of macrophage activation and polarization. , 2004, Trends in immunology.

[11]  J. Nattermann,et al.  Semiquantitative analysis of intrahepatic CC-chemokine mRNas in chronic hepatitis C. , 2004, Mediators of inflammation.

[12]  T. Mizutani,et al.  Different chemokine expression in lethal and non‐lethal murine west nile virus infection , 2004, Journal of medical virology.

[13]  Hidekazu Nishimura,et al.  Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus , 2004, Nature.

[14]  Bao Lu,et al.  Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice , 2004, Journal of leukocyte biology.

[15]  H. Rosenberg,et al.  Functional Antagonism of Chemokine Receptor CCR1 Reduces Mortality in Acute Pneumovirus Infection In Vivo , 2004, Journal of Virology.

[16]  Y. Lau,et al.  Tolerance associated with cord blood transplantation may depend on the state of host dendritic cells , 2004, British journal of haematology.

[17]  W. Ip,et al.  Distinct Maturation of, but Not Migration between, Human Monocyte-Derived Dendritic Cells upon Ingestion of Apoptotic Cells of Early or Late Phases 1 , 2004, The Journal of Immunology.

[18]  J. Peiris,et al.  Re-emergence of fatal human influenza A subtype H5N1 disease , 2004, The Lancet.

[19]  G. Gray,et al.  Age-Related Changes in Expression of CXCR4 and CCR5 on Peripheral Blood Leukocytes from Uninfected Infants Born to Human Immunodeficiency Virus Type 1-Infected Mothers , 2004, Clinical Diagnostic Laboratory Immunology.

[20]  K. Yuen,et al.  Peiris, J.S.M. et al. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 363, 617−619 , 2004 .

[21]  H. Rosenberg,et al.  Chemokine regulation of inflammation during acute viral infection , 2003, Current opinion in allergy and clinical immunology.

[22]  M. Heise,et al.  Chemokines and viruses: friends or foes? , 2003, Trends in microbiology.

[23]  D. Gemsa,et al.  Chemokine receptor expression and chemotactic responsiveness of human monocytes after influenza A virus infection , 2003, Journal of leukocyte biology.

[24]  N. Lukacs,et al.  Respiratory syncytial virus‐induced CCL5/RANTES contributes to exacerbation of allergic airway inflammation , 2003, European journal of immunology.

[25]  W. Ho,et al.  CCR5 Expression and β-Chemokine Production During Placental Neonatal Monocyte Differentiation , 2003, Pediatric Research.

[26]  Y. Guan,et al.  Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? , 2002, The Lancet.

[27]  Y. Guan,et al.  Molecular Evolution of H6 Influenza Viruses from Poultry in Southeastern China: Prevalence of H6N1 Influenza Viruses Possessing Seven A/Hong Kong/156/97 (H5N1)-Like Genes in Poultry , 2002, Journal of Virology.

[28]  K. Melén,et al.  Survey Molecular pathogenesis of influenza A virus infection and virus-induced regulation of cytokine gene expression , 1998 .

[29]  Y. Lau,et al.  Decreased yield, phenotypic expression and function of immature monocyte‐derived dendritic cells in cord blood , 2001, British journal of haematology.

[30]  D. Gemsa,et al.  Increase of CCR1 and CCR5 expression and enhanced functional response to MIP‐1α during differentiation of human monocytes to macrophages , 2001, Journal of leukocyte biology.

[31]  H. Rosenberg,et al.  The Chemokine Macrophage-Inflammatory Protein-1α and Its Receptor CCR1 Control Pulmonary Inflammation and Antiviral Host Defense in Paramyxovirus Infection , 2000, The Journal of Immunology.

[32]  N. Maeda,et al.  Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. , 2000, The American journal of pathology.

[33]  A. Maghazachi Chemokines, G proteins and natural killer cells. , 2000, Archivum immunologiae et therapiae experimentalis.

[34]  G. Karupiah,et al.  Chemokines and chemokine receptors in infectious diseases , 1999, Immunology and cell biology.

[35]  E. Jaffe,et al.  MIP-1alpha expression in tissues from patients with hemophagocytic syndrome. , 1999, Laboratory investigation; a journal of technical methods and pathology.

[36]  Y. Lau,et al.  IGF-I Increases Interferon-γ and IL-6 mRNA Expression and Protein Production in Neonatal Mononuclear Cells , 1999, Pediatric Research.

[37]  M. Peiris,et al.  Human infection with influenza H9N2 , 1999, The Lancet.

[38]  Y. Lau,et al.  Effect of insulin‐like growth factor 1 on PHA‐stimulated cord blood mononuclear cell telomerase activity , 1999, British journal of haematology.

[39]  M. Peiris,et al.  Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus , 1998, The Lancet.

[40]  A. Luster,et al.  Chemokines--chemotactic cytokines that mediate inflammation. , 1998, The New England journal of medicine.

[41]  I. Campbell,et al.  Chemokine gene expression in the brains of mice with lymphocytic choriomeningitis , 1997, Journal of virology.

[42]  T. Sauerbruch,et al.  Semiquantitative analysis of intrahepatic cytokine mRNAs in chronic hepatitis C. , 1997, The Journal of infectious diseases.

[43]  K. Matsushima,et al.  Preparation of specific polyclonal antibodies to a C-C chemokine receptor , CCR 1 , and determination of CCR 1 expression on various types of leukocytes , 2005 .

[44]  J. Sheridan,et al.  Requirement of MIP-1 alpha for an inflammatory response to viral infection. , 1995, Science.

[45]  P. Payment,et al.  Methods and techniques in virology , 1993 .

[46]  K. Frei,et al.  A kinetic study of immune mediators in the lungs of mice infected with influenza A virus. , 1992, Journal of immunology.

[47]  K. Nomoto,et al.  Protective mechanisms against pulmonary infection with influenza virus. I. Relative contribution of polymorphonuclear leukocytes and of alveolar macrophages to protection during the early phase of intranasal infection. , 1987, The Journal of general virology.

[48]  G. K. Hirst ADSORPTION OF INFLUENZA HEMAGGLUTININS AND VIRUS BY RED BLOOD CELLS , 1942, The Journal of experimental medicine.