Circulating inflammatory monocytes contribute to impaired influenza vaccine responses in HIV-infected participants

Varghese K. George, Suresh Pallikkuth, Rajendra Pahwa, Lesley R. De Armas, Stefano Rinaldi, Li Pan, Savita G Pahwa

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Objective: Antibody responses are often impaired in old age and in HIV-positive (HIV+) infection despite virologic control with antiretroviral therapy but innate immunologic determinants are not well understood. Design: Monocytes and natural killer cells were examined for relationships to age, HIV infection and influenza vaccine responses. Methods: Virologically suppressed HIV+ (n = 139) and HIV-negative (HIV-) (n = 137) participants classified by age as young (18-39 years), middle-Aged (40-59 years) and old (≥60 years) were evaluated preinfluenza and postinfluenza vaccination. Results: Prevaccination frequencies of inflammatory monocytes were highest in old HIV+ and HIV-, with old HIV+ exhibiting higher frequency of integrin CD11b on inflammatory monocytes that was correlated with age, expression of C-C chemokine receptor-2 (CCR2) and plasma soluble tumor necrosis factor receptor-1 (sTNFR1), with inverse correlation with postvaccination influenza H1N1 antibody titers. Higher frequencies of CD11b + inflammatory monocytes (CD11b hi, >48.4%) compared with low frequencies of CD11b + inflammatory monocytes (<15.8%) was associated with higher prevaccination frequencies of total and inflammatory monocytes and higher CCR2 MFI, higher plasma sTNFR1 and CXCL-10 with higher lipopolysaccharide stimulated expression of TNFα and IL-6, concomitant with lower postvaccination influenza antibody titers. In HIV+ CD11b hi expressers, the depletion of inflammatory monocytes from peripheral blood mononuclear cells resulted in enhanced antigen-specific CD4+ T-cell proliferation. Immature CD56 hi natural killer cells were lower in young HIV+ compared with young HIV-participants. Conclusion: Perturbations of innate immunity and inflammation signified by high CD11b on inflammatory monocytes are exacerbated with aging in HIV+ and negatively impact immune function involved in Ab response to influenza vaccination.

Original languageEnglish (US)
Pages (from-to)1219-1228
Number of pages10
JournalAIDS
Volume32
Issue number10
DOIs
StatePublished - Jun 19 2018

Fingerprint

Influenza Vaccines
Monocytes
HIV
Human Influenza
CC Chemokines
Tumor Necrosis Factor Receptors
Chemokine Receptors
Natural Killer Cells
HIV Infections
Vaccination
AIDS Vaccines
CD4 Antigens
Antibodies
Innate Immunity
Integrins
Antibody Formation
Lipopolysaccharides
Interleukin-6
Blood Cells
Cell Proliferation

Keywords

  • aging
  • CD11b
  • HIV infection
  • inflammation
  • inflammatory monocytes
  • seasonal influenza vaccination
  • vaccine responses

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology
  • Infectious Diseases

Cite this

Circulating inflammatory monocytes contribute to impaired influenza vaccine responses in HIV-infected participants. / George, Varghese K.; Pallikkuth, Suresh; Pahwa, Rajendra; De Armas, Lesley R.; Rinaldi, Stefano; Pan, Li; Pahwa, Savita G.

In: AIDS, Vol. 32, No. 10, 19.06.2018, p. 1219-1228.

Research output: Contribution to journalArticle

George, Varghese K. ; Pallikkuth, Suresh ; Pahwa, Rajendra ; De Armas, Lesley R. ; Rinaldi, Stefano ; Pan, Li ; Pahwa, Savita G. / Circulating inflammatory monocytes contribute to impaired influenza vaccine responses in HIV-infected participants. In: AIDS. 2018 ; Vol. 32, No. 10. pp. 1219-1228.
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abstract = "Objective: Antibody responses are often impaired in old age and in HIV-positive (HIV+) infection despite virologic control with antiretroviral therapy but innate immunologic determinants are not well understood. Design: Monocytes and natural killer cells were examined for relationships to age, HIV infection and influenza vaccine responses. Methods: Virologically suppressed HIV+ (n = 139) and HIV-negative (HIV-) (n = 137) participants classified by age as young (18-39 years), middle-Aged (40-59 years) and old (≥60 years) were evaluated preinfluenza and postinfluenza vaccination. Results: Prevaccination frequencies of inflammatory monocytes were highest in old HIV+ and HIV-, with old HIV+ exhibiting higher frequency of integrin CD11b on inflammatory monocytes that was correlated with age, expression of C-C chemokine receptor-2 (CCR2) and plasma soluble tumor necrosis factor receptor-1 (sTNFR1), with inverse correlation with postvaccination influenza H1N1 antibody titers. Higher frequencies of CD11b + inflammatory monocytes (CD11b hi, >48.4{\%}) compared with low frequencies of CD11b + inflammatory monocytes (<15.8{\%}) was associated with higher prevaccination frequencies of total and inflammatory monocytes and higher CCR2 MFI, higher plasma sTNFR1 and CXCL-10 with higher lipopolysaccharide stimulated expression of TNFα and IL-6, concomitant with lower postvaccination influenza antibody titers. In HIV+ CD11b hi expressers, the depletion of inflammatory monocytes from peripheral blood mononuclear cells resulted in enhanced antigen-specific CD4+ T-cell proliferation. Immature CD56 hi natural killer cells were lower in young HIV+ compared with young HIV-participants. Conclusion: Perturbations of innate immunity and inflammation signified by high CD11b on inflammatory monocytes are exacerbated with aging in HIV+ and negatively impact immune function involved in Ab response to influenza vaccination.",
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T1 - Circulating inflammatory monocytes contribute to impaired influenza vaccine responses in HIV-infected participants

AU - George, Varghese K.

AU - Pallikkuth, Suresh

AU - Pahwa, Rajendra

AU - De Armas, Lesley R.

AU - Rinaldi, Stefano

AU - Pan, Li

AU - Pahwa, Savita G

PY - 2018/6/19

Y1 - 2018/6/19

N2 - Objective: Antibody responses are often impaired in old age and in HIV-positive (HIV+) infection despite virologic control with antiretroviral therapy but innate immunologic determinants are not well understood. Design: Monocytes and natural killer cells were examined for relationships to age, HIV infection and influenza vaccine responses. Methods: Virologically suppressed HIV+ (n = 139) and HIV-negative (HIV-) (n = 137) participants classified by age as young (18-39 years), middle-Aged (40-59 years) and old (≥60 years) were evaluated preinfluenza and postinfluenza vaccination. Results: Prevaccination frequencies of inflammatory monocytes were highest in old HIV+ and HIV-, with old HIV+ exhibiting higher frequency of integrin CD11b on inflammatory monocytes that was correlated with age, expression of C-C chemokine receptor-2 (CCR2) and plasma soluble tumor necrosis factor receptor-1 (sTNFR1), with inverse correlation with postvaccination influenza H1N1 antibody titers. Higher frequencies of CD11b + inflammatory monocytes (CD11b hi, >48.4%) compared with low frequencies of CD11b + inflammatory monocytes (<15.8%) was associated with higher prevaccination frequencies of total and inflammatory monocytes and higher CCR2 MFI, higher plasma sTNFR1 and CXCL-10 with higher lipopolysaccharide stimulated expression of TNFα and IL-6, concomitant with lower postvaccination influenza antibody titers. In HIV+ CD11b hi expressers, the depletion of inflammatory monocytes from peripheral blood mononuclear cells resulted in enhanced antigen-specific CD4+ T-cell proliferation. Immature CD56 hi natural killer cells were lower in young HIV+ compared with young HIV-participants. Conclusion: Perturbations of innate immunity and inflammation signified by high CD11b on inflammatory monocytes are exacerbated with aging in HIV+ and negatively impact immune function involved in Ab response to influenza vaccination.

AB - Objective: Antibody responses are often impaired in old age and in HIV-positive (HIV+) infection despite virologic control with antiretroviral therapy but innate immunologic determinants are not well understood. Design: Monocytes and natural killer cells were examined for relationships to age, HIV infection and influenza vaccine responses. Methods: Virologically suppressed HIV+ (n = 139) and HIV-negative (HIV-) (n = 137) participants classified by age as young (18-39 years), middle-Aged (40-59 years) and old (≥60 years) were evaluated preinfluenza and postinfluenza vaccination. Results: Prevaccination frequencies of inflammatory monocytes were highest in old HIV+ and HIV-, with old HIV+ exhibiting higher frequency of integrin CD11b on inflammatory monocytes that was correlated with age, expression of C-C chemokine receptor-2 (CCR2) and plasma soluble tumor necrosis factor receptor-1 (sTNFR1), with inverse correlation with postvaccination influenza H1N1 antibody titers. Higher frequencies of CD11b + inflammatory monocytes (CD11b hi, >48.4%) compared with low frequencies of CD11b + inflammatory monocytes (<15.8%) was associated with higher prevaccination frequencies of total and inflammatory monocytes and higher CCR2 MFI, higher plasma sTNFR1 and CXCL-10 with higher lipopolysaccharide stimulated expression of TNFα and IL-6, concomitant with lower postvaccination influenza antibody titers. In HIV+ CD11b hi expressers, the depletion of inflammatory monocytes from peripheral blood mononuclear cells resulted in enhanced antigen-specific CD4+ T-cell proliferation. Immature CD56 hi natural killer cells were lower in young HIV+ compared with young HIV-participants. Conclusion: Perturbations of innate immunity and inflammation signified by high CD11b on inflammatory monocytes are exacerbated with aging in HIV+ and negatively impact immune function involved in Ab response to influenza vaccination.

KW - aging

KW - CD11b

KW - HIV infection

KW - inflammation

KW - inflammatory monocytes

KW - seasonal influenza vaccination

KW - vaccine responses

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