Higher PIK3C2B gene expression of H1N1+ specific B-cells is associated with lower H1N1 immunogenicity after trivalent influenza vaccination in HIV infected children

Nicola Cotugno; Sonia Zicari; Elena Morrocchi; Lesley R. de Armas; Suresh Pallikkuth; Stefano Rinaldi; Alessandra Ruggiero; Emma Concetta Manno; Paola Zangari; Maria Chiriaco; Stefania Bernardi; Sarah F. Andrews; Alberto Cagigi; Paolo Rossi; Adrian B. McDermott; Savita Pahwa; Paolo Palma

doi:10.1016/j.clim.2020.108440

Higher PIK3C2B gene expression of H1N1+ specific B-cells is associated with lower H1N1 immunogenicity after trivalent influenza vaccination in HIV infected children

Nicola Cotugno, Sonia Zicari, Elena Morrocchi, Lesley R. de Armas, Suresh Pallikkuth, Stefano Rinaldi, Alessandra Ruggiero, Emma Concetta Manno, Paola Zangari, Maria Chiriaco, Stefania Bernardi, Sarah F. Andrews, Alberto Cagigi, Paolo Rossi, Adrian B. McDermott, Savita Pahwa, Paolo Palma

Microbiology & Immunology

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Perinatally HIV-infected children (PHIV), despite successful antiretroviral therapy, present suboptimal responses to vaccinations compared to healthy-controls (HC). Here we investigated phenotypic and transcriptional signatures of H1N1-specific B-cells (H1N1-Sp) in PHIV, differentially responding to trivalent-influenza-vaccine (TIV), and HC. Patients were categorized in responders (R) and non-responders (NR) according to hemagglutination-inhibition-assay at baseline and 21 days after TIV. No differences in H1N1-Sp frequencies were found between groups. H1N1-Sp transcriptional analysis revealed a distinct signature between PHIV and HC. NR presented higher PIK3C2B and NOD2 expression compared to R, confirmed by downregulation of PIK3C2B in resting-memory of R after H1N1 in-vitro stimulation. In conclusion this study confirms that qualitative rather than quantitative analyses are needed to characterize immune responses in PHIV. These results further suggest that higher PIK3C2B in H1N1-Sp of NR is associated with lower H1N1 immunogenicity and may be targeted by future modulating strategies to improve TIV responses in PHIV.

Original language	English (US)
Article number	108440
Journal	Clinical Immunology
Volume	215
DOIs	https://doi.org/10.1016/j.clim.2020.108440
State	Published - Jun 2020

Keywords

Antigen specific B cells
Gene expression
H1N1
Influenza vaccination
PIK3C2B
Perinatally HIV infected children

ASJC Scopus subject areas

Immunology and Allergy
Immunology

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Cotugno, N., Zicari, S., Morrocchi, E., de Armas, L. R., Pallikkuth, S., Rinaldi, S., Ruggiero, A., Manno, E. C., Zangari, P., Chiriaco, M., Bernardi, S., Andrews, S. F., Cagigi, A., Rossi, P., McDermott, A. B., Pahwa, S., & Palma, P. (2020). Higher PIK3C2B gene expression of H1N1+ specific B-cells is associated with lower H1N1 immunogenicity after trivalent influenza vaccination in HIV infected children. Clinical Immunology, 215, [108440]. https://doi.org/10.1016/j.clim.2020.108440

Higher PIK3C2B gene expression of H1N1+ specific B-cells is associated with lower H1N1 immunogenicity after trivalent influenza vaccination in HIV infected children. / Cotugno, Nicola; Zicari, Sonia; Morrocchi, Elena; de Armas, Lesley R.; Pallikkuth, Suresh; Rinaldi, Stefano; Ruggiero, Alessandra; Manno, Emma Concetta; Zangari, Paola; Chiriaco, Maria; Bernardi, Stefania; Andrews, Sarah F.; Cagigi, Alberto; Rossi, Paolo; McDermott, Adrian B.; Pahwa, Savita; Palma, Paolo.

In: Clinical Immunology, Vol. 215, 108440, 06.2020.

Research output: Contribution to journal › Article › peer-review

Cotugno, N, Zicari, S, Morrocchi, E, de Armas, LR, Pallikkuth, S, Rinaldi, S, Ruggiero, A, Manno, EC, Zangari, P, Chiriaco, M, Bernardi, S, Andrews, SF, Cagigi, A, Rossi, P, McDermott, AB, Pahwa, S & Palma, P 2020, 'Higher PIK3C2B gene expression of H1N1+ specific B-cells is associated with lower H1N1 immunogenicity after trivalent influenza vaccination in HIV infected children', Clinical Immunology, vol. 215, 108440. https://doi.org/10.1016/j.clim.2020.108440

Cotugno, Nicola ; Zicari, Sonia ; Morrocchi, Elena ; de Armas, Lesley R. ; Pallikkuth, Suresh ; Rinaldi, Stefano ; Ruggiero, Alessandra ; Manno, Emma Concetta ; Zangari, Paola ; Chiriaco, Maria ; Bernardi, Stefania ; Andrews, Sarah F. ; Cagigi, Alberto ; Rossi, Paolo ; McDermott, Adrian B. ; Pahwa, Savita ; Palma, Paolo. / Higher PIK3C2B gene expression of H1N1+ specific B-cells is associated with lower H1N1 immunogenicity after trivalent influenza vaccination in HIV infected children. In: Clinical Immunology. 2020 ; Vol. 215.

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title = "Higher PIK3C2B gene expression of H1N1+ specific B-cells is associated with lower H1N1 immunogenicity after trivalent influenza vaccination in HIV infected children",

abstract = "Perinatally HIV-infected children (PHIV), despite successful antiretroviral therapy, present suboptimal responses to vaccinations compared to healthy-controls (HC). Here we investigated phenotypic and transcriptional signatures of H1N1-specific B-cells (H1N1-Sp) in PHIV, differentially responding to trivalent-influenza-vaccine (TIV), and HC. Patients were categorized in responders (R) and non-responders (NR) according to hemagglutination-inhibition-assay at baseline and 21 days after TIV. No differences in H1N1-Sp frequencies were found between groups. H1N1-Sp transcriptional analysis revealed a distinct signature between PHIV and HC. NR presented higher PIK3C2B and NOD2 expression compared to R, confirmed by downregulation of PIK3C2B in resting-memory of R after H1N1 in-vitro stimulation. In conclusion this study confirms that qualitative rather than quantitative analyses are needed to characterize immune responses in PHIV. These results further suggest that higher PIK3C2B in H1N1-Sp of NR is associated with lower H1N1 immunogenicity and may be targeted by future modulating strategies to improve TIV responses in PHIV.",

keywords = "Antigen specific B cells, Gene expression, H1N1, Influenza vaccination, PIK3C2B, Perinatally HIV infected children",

author = "Nicola Cotugno and Sonia Zicari and Elena Morrocchi and {de Armas}, {Lesley R.} and Suresh Pallikkuth and Stefano Rinaldi and Alessandra Ruggiero and Manno, {Emma Concetta} and Paola Zangari and Maria Chiriaco and Stefania Bernardi and Andrews, {Sarah F.} and Alberto Cagigi and Paolo Rossi and McDermott, {Adrian B.} and Savita Pahwa and Paolo Palma",

note = "Funding Information: This work was made possible by the support from a pilot award to NC from Miami Center for AIDS Research (CFAR), grants obtained by Bambino Ges? Children's Hospital (Ricerca corrente 2020 to NC), Associazione Volontari Bambino Ges?, Ricerca Finalizzata 2010, Ministero della Salute (RF_2010_2310438), and grants AI108472 and AI127347 to SP and the Laboratory Sciences Core of the Miami CFAR (P30AI073961) from the National Institutes of Health (NIH), which is supported by the following NIH Co-Funding and Participating Institutes and Centers: NIAID, NCI, NICHD, NHLBI, NIDA, NIMH, NIA, NIDDK, NIGMS, FIC, and OAR. Funding Information: This work was made possible by the support from a pilot award to NC from Miami Center for AIDS Research (CFAR), grants obtained by Bambino Ges{\'u} Children's Hospital (Ricerca corrente 2020 to NC), Associazione Volontari Bambino Ges{\`u} , Ricerca Finalizzata 2010, Ministero della Salute (RF_2010_2310438), and grants AI108472 and AI127347 to SP and the Laboratory Sciences Core of the Miami CFAR (P30AI073961) from the National Institutes of Health (NIH), which is supported by the following NIH Co-Funding and Participating Institutes and Centers: NIAID , NCI , NICHD , NHLBI , NIDA , NIMH , NIA , NIDDK , NIGMS , FIC , and OAR . ",

year = "2020",

month = jun,

doi = "10.1016/j.clim.2020.108440",

language = "English (US)",

volume = "215",

journal = "Clinical Immunology",

issn = "1521-6616",

publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Higher PIK3C2B gene expression of H1N1+ specific B-cells is associated with lower H1N1 immunogenicity after trivalent influenza vaccination in HIV infected children

AU - Cotugno, Nicola

AU - Zicari, Sonia

AU - Morrocchi, Elena

AU - de Armas, Lesley R.

AU - Pallikkuth, Suresh

AU - Rinaldi, Stefano

AU - Ruggiero, Alessandra

AU - Manno, Emma Concetta

AU - Zangari, Paola

AU - Chiriaco, Maria

AU - Bernardi, Stefania

AU - Andrews, Sarah F.

AU - Cagigi, Alberto

AU - Rossi, Paolo

AU - McDermott, Adrian B.

AU - Pahwa, Savita

AU - Palma, Paolo

N1 - Funding Information: This work was made possible by the support from a pilot award to NC from Miami Center for AIDS Research (CFAR), grants obtained by Bambino Ges? Children's Hospital (Ricerca corrente 2020 to NC), Associazione Volontari Bambino Ges?, Ricerca Finalizzata 2010, Ministero della Salute (RF_2010_2310438), and grants AI108472 and AI127347 to SP and the Laboratory Sciences Core of the Miami CFAR (P30AI073961) from the National Institutes of Health (NIH), which is supported by the following NIH Co-Funding and Participating Institutes and Centers: NIAID, NCI, NICHD, NHLBI, NIDA, NIMH, NIA, NIDDK, NIGMS, FIC, and OAR. Funding Information: This work was made possible by the support from a pilot award to NC from Miami Center for AIDS Research (CFAR), grants obtained by Bambino Gesú Children's Hospital (Ricerca corrente 2020 to NC), Associazione Volontari Bambino Gesù , Ricerca Finalizzata 2010, Ministero della Salute (RF_2010_2310438), and grants AI108472 and AI127347 to SP and the Laboratory Sciences Core of the Miami CFAR (P30AI073961) from the National Institutes of Health (NIH), which is supported by the following NIH Co-Funding and Participating Institutes and Centers: NIAID , NCI , NICHD , NHLBI , NIDA , NIMH , NIA , NIDDK , NIGMS , FIC , and OAR .

PY - 2020/6

Y1 - 2020/6

N2 - Perinatally HIV-infected children (PHIV), despite successful antiretroviral therapy, present suboptimal responses to vaccinations compared to healthy-controls (HC). Here we investigated phenotypic and transcriptional signatures of H1N1-specific B-cells (H1N1-Sp) in PHIV, differentially responding to trivalent-influenza-vaccine (TIV), and HC. Patients were categorized in responders (R) and non-responders (NR) according to hemagglutination-inhibition-assay at baseline and 21 days after TIV. No differences in H1N1-Sp frequencies were found between groups. H1N1-Sp transcriptional analysis revealed a distinct signature between PHIV and HC. NR presented higher PIK3C2B and NOD2 expression compared to R, confirmed by downregulation of PIK3C2B in resting-memory of R after H1N1 in-vitro stimulation. In conclusion this study confirms that qualitative rather than quantitative analyses are needed to characterize immune responses in PHIV. These results further suggest that higher PIK3C2B in H1N1-Sp of NR is associated with lower H1N1 immunogenicity and may be targeted by future modulating strategies to improve TIV responses in PHIV.

AB - Perinatally HIV-infected children (PHIV), despite successful antiretroviral therapy, present suboptimal responses to vaccinations compared to healthy-controls (HC). Here we investigated phenotypic and transcriptional signatures of H1N1-specific B-cells (H1N1-Sp) in PHIV, differentially responding to trivalent-influenza-vaccine (TIV), and HC. Patients were categorized in responders (R) and non-responders (NR) according to hemagglutination-inhibition-assay at baseline and 21 days after TIV. No differences in H1N1-Sp frequencies were found between groups. H1N1-Sp transcriptional analysis revealed a distinct signature between PHIV and HC. NR presented higher PIK3C2B and NOD2 expression compared to R, confirmed by downregulation of PIK3C2B in resting-memory of R after H1N1 in-vitro stimulation. In conclusion this study confirms that qualitative rather than quantitative analyses are needed to characterize immune responses in PHIV. These results further suggest that higher PIK3C2B in H1N1-Sp of NR is associated with lower H1N1 immunogenicity and may be targeted by future modulating strategies to improve TIV responses in PHIV.

KW - Antigen specific B cells

KW - Gene expression

KW - H1N1

KW - Influenza vaccination

KW - PIK3C2B

KW - Perinatally HIV infected children

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