Longitudinal profiling of human blood transcriptome in healthy and lupus pregnancy

Seunghee Hong; Romain Banchereau; Bat Sheva L. Maslow; Marta M. Guerra; Jacob Cardenas; Jeanine Baisch; D. Ware Branch; T. Flint Porter; Allen Sawitzke; Carl A. Laskin; Jill P. Buyon; Joan Merrill; Lisa R. Sammaritano; Michelle Petri; Elizabeth Gatewood; Alma Martina Cepika; Marina Ohouo; Gerlinde Obermoser; Esperanza Anguiano; Tae Whan Kim; John Nulsen; Djamel Nehar-Belaid; Derek Blankenship; Jacob Turner; Jacques Banchereau; Jane E. Salmon; Virginia Pascual

doi:10.1084/jem.20190185

Longitudinal profiling of human blood transcriptome in healthy and lupus pregnancy

Seunghee Hong, Romain Banchereau, Bat Sheva L. Maslow, Marta M. Guerra, Jacob Cardenas, Jeanine Baisch, D. Ware Branch, T. Flint Porter, Allen Sawitzke, Carl A. Laskin, Jill P. Buyon, Joan Merrill, Lisa R. Sammaritano, Michelle Petri, Elizabeth Gatewood, Alma Martina Cepika, Marina Ohouo, Gerlinde Obermoser, Esperanza Anguiano, Tae Whan KimJohn Nulsen, Djamel Nehar-Belaid, Derek Blankenship, Jacob Turner, Jacques Banchereau, Jane E. Salmon, Virginia Pascual

Department of Biotechnology

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

35 Citations (Scopus)

Abstract

Systemic lupus erythematosus carries an increased risk of pregnancy complications, including preeclampsia and fetal adverse outcomes. To identify the underlying molecular mechanisms, we longitudinally profiled the blood transcriptome of 92 lupus patients and 43 healthy women during pregnancy and postpartum and performed multicolor flow cytometry in a subset of them. We also profiled 25 healthy women undergoing assisted reproductive technology to monitor transcriptional changes around embryo implantation. Sustained down-regulation of multiple immune signatures, including interferon and plasma cells, was observed during healthy pregnancy. These changes appeared early after embryo implantation and were mirrored in uncomplicated lupus pregnancies. Patients with preeclampsia displayed early up-regulation of neutrophil signatures that correlated with expansion of immature neutrophils. Lupus pregnancies with fetal complications carried the highest interferon and plasma cell signatures as well as activated CD4⁺ T cell counts. Thus, blood immunomonitoring reveals that both healthy and uncomplicated lupus pregnancies exhibit early and sustained transcriptional modulation of lupus-related signatures, and a lack thereof associates with adverse outcomes.

Original language	English
Pages (from-to)	1154-1169
Number of pages	16
Journal	Journal of Experimental Medicine
Volume	216
Issue number	5
DOIs	https://doi.org/10.1084/jem.20190185
Publication status	Published - 2019 May 1

Bibliographical note

Funding Information:
This work was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases/National Institutes of Health awards R01 AR49772 and R01 AR49772-07S2 (J.E. Salmon), R01 AR69572 and AR43727 (M. Petri), National Institute of Allergy and Infectious Diseases/National Institutes of Health award U19 AI082715 (V. Pascual), P50AR070594 (V. Pascual and J. Banchereau), the Morris and Alma Schapiro Fund (J.E. Salmon), the Baylor-Scott & White Health Care Research Foundation, and the Kathryn W. Davis gift to the Jackson Laboratory.

Publisher Copyright:
© 2019 Hong et al.

All Science Journal Classification (ASJC) codes

Immunology and Allergy
Immunology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1084/jem.20190185

Cite this

Hong, S., Banchereau, R., Maslow, B. S. L., Guerra, M. M., Cardenas, J., Baisch, J., Ware Branch, D., Flint Porter, T., Sawitzke, A., Laskin, C. A., Buyon, J. P., Merrill, J., Sammaritano, L. R., Petri, M., Gatewood, E., Cepika, A. M., Ohouo, M., Obermoser, G., Anguiano, E., ... Pascual, V. (2019). Longitudinal profiling of human blood transcriptome in healthy and lupus pregnancy. Journal of Experimental Medicine, 216(5), 1154-1169. https://doi.org/10.1084/jem.20190185

@article{43e034ace2bc4530a074960e6c90955a,

title = "Longitudinal profiling of human blood transcriptome in healthy and lupus pregnancy",

abstract = "Systemic lupus erythematosus carries an increased risk of pregnancy complications, including preeclampsia and fetal adverse outcomes. To identify the underlying molecular mechanisms, we longitudinally profiled the blood transcriptome of 92 lupus patients and 43 healthy women during pregnancy and postpartum and performed multicolor flow cytometry in a subset of them. We also profiled 25 healthy women undergoing assisted reproductive technology to monitor transcriptional changes around embryo implantation. Sustained down-regulation of multiple immune signatures, including interferon and plasma cells, was observed during healthy pregnancy. These changes appeared early after embryo implantation and were mirrored in uncomplicated lupus pregnancies. Patients with preeclampsia displayed early up-regulation of neutrophil signatures that correlated with expansion of immature neutrophils. Lupus pregnancies with fetal complications carried the highest interferon and plasma cell signatures as well as activated CD4+ T cell counts. Thus, blood immunomonitoring reveals that both healthy and uncomplicated lupus pregnancies exhibit early and sustained transcriptional modulation of lupus-related signatures, and a lack thereof associates with adverse outcomes.",

author = "Seunghee Hong and Romain Banchereau and Maslow, {Bat Sheva L.} and Guerra, {Marta M.} and Jacob Cardenas and Jeanine Baisch and {Ware Branch}, D. and {Flint Porter}, T. and Allen Sawitzke and Laskin, {Carl A.} and Buyon, {Jill P.} and Joan Merrill and Sammaritano, {Lisa R.} and Michelle Petri and Elizabeth Gatewood and Cepika, {Alma Martina} and Marina Ohouo and Gerlinde Obermoser and Esperanza Anguiano and Kim, {Tae Whan} and John Nulsen and Djamel Nehar-Belaid and Derek Blankenship and Jacob Turner and Jacques Banchereau and Salmon, {Jane E.} and Virginia Pascual",

note = "Funding Information: This work was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases/National Institutes of Health awards R01 AR49772 and R01 AR49772-07S2 (J.E. Salmon), R01 AR69572 and AR43727 (M. Petri), National Institute of Allergy and Infectious Diseases/National Institutes of Health award U19 AI082715 (V. Pascual), P50AR070594 (V. Pascual and J. Banchereau), the Morris and Alma Schapiro Fund (J.E. Salmon), the Baylor-Scott & White Health Care Research Foundation, and the Kathryn W. Davis gift to the Jackson Laboratory. Publisher Copyright: {\textcopyright} 2019 Hong et al.",

year = "2019",

month = may,

day = "1",

doi = "10.1084/jem.20190185",

language = "English",

volume = "216",

pages = "1154--1169",

journal = "Journal of Experimental Medicine",

issn = "0022-1007",

publisher = "Rockefeller University Press",

number = "5",

}

Hong, S, Banchereau, R, Maslow, BSL, Guerra, MM, Cardenas, J, Baisch, J, Ware Branch, D, Flint Porter, T, Sawitzke, A, Laskin, CA, Buyon, JP, Merrill, J, Sammaritano, LR, Petri, M, Gatewood, E, Cepika, AM, Ohouo, M, Obermoser, G, Anguiano, E, Kim, TW, Nulsen, J, Nehar-Belaid, D, Blankenship, D, Turner, J, Banchereau, J, Salmon, JE & Pascual, V 2019, 'Longitudinal profiling of human blood transcriptome in healthy and lupus pregnancy', Journal of Experimental Medicine, vol. 216, no. 5, pp. 1154-1169. https://doi.org/10.1084/jem.20190185

TY - JOUR

T1 - Longitudinal profiling of human blood transcriptome in healthy and lupus pregnancy

AU - Hong, Seunghee

AU - Banchereau, Romain

AU - Maslow, Bat Sheva L.

AU - Guerra, Marta M.

AU - Cardenas, Jacob

AU - Baisch, Jeanine

AU - Ware Branch, D.

AU - Flint Porter, T.

AU - Sawitzke, Allen

AU - Laskin, Carl A.

AU - Buyon, Jill P.

AU - Merrill, Joan

AU - Sammaritano, Lisa R.

AU - Petri, Michelle

AU - Gatewood, Elizabeth

AU - Cepika, Alma Martina

AU - Ohouo, Marina

AU - Obermoser, Gerlinde

AU - Anguiano, Esperanza

AU - Kim, Tae Whan

AU - Nulsen, John

AU - Nehar-Belaid, Djamel

AU - Blankenship, Derek

AU - Turner, Jacob

AU - Banchereau, Jacques

AU - Salmon, Jane E.

AU - Pascual, Virginia

N1 - Funding Information: This work was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases/National Institutes of Health awards R01 AR49772 and R01 AR49772-07S2 (J.E. Salmon), R01 AR69572 and AR43727 (M. Petri), National Institute of Allergy and Infectious Diseases/National Institutes of Health award U19 AI082715 (V. Pascual), P50AR070594 (V. Pascual and J. Banchereau), the Morris and Alma Schapiro Fund (J.E. Salmon), the Baylor-Scott & White Health Care Research Foundation, and the Kathryn W. Davis gift to the Jackson Laboratory. Publisher Copyright: © 2019 Hong et al.

PY - 2019/5/1

Y1 - 2019/5/1

N2 - Systemic lupus erythematosus carries an increased risk of pregnancy complications, including preeclampsia and fetal adverse outcomes. To identify the underlying molecular mechanisms, we longitudinally profiled the blood transcriptome of 92 lupus patients and 43 healthy women during pregnancy and postpartum and performed multicolor flow cytometry in a subset of them. We also profiled 25 healthy women undergoing assisted reproductive technology to monitor transcriptional changes around embryo implantation. Sustained down-regulation of multiple immune signatures, including interferon and plasma cells, was observed during healthy pregnancy. These changes appeared early after embryo implantation and were mirrored in uncomplicated lupus pregnancies. Patients with preeclampsia displayed early up-regulation of neutrophil signatures that correlated with expansion of immature neutrophils. Lupus pregnancies with fetal complications carried the highest interferon and plasma cell signatures as well as activated CD4+ T cell counts. Thus, blood immunomonitoring reveals that both healthy and uncomplicated lupus pregnancies exhibit early and sustained transcriptional modulation of lupus-related signatures, and a lack thereof associates with adverse outcomes.

AB - Systemic lupus erythematosus carries an increased risk of pregnancy complications, including preeclampsia and fetal adverse outcomes. To identify the underlying molecular mechanisms, we longitudinally profiled the blood transcriptome of 92 lupus patients and 43 healthy women during pregnancy and postpartum and performed multicolor flow cytometry in a subset of them. We also profiled 25 healthy women undergoing assisted reproductive technology to monitor transcriptional changes around embryo implantation. Sustained down-regulation of multiple immune signatures, including interferon and plasma cells, was observed during healthy pregnancy. These changes appeared early after embryo implantation and were mirrored in uncomplicated lupus pregnancies. Patients with preeclampsia displayed early up-regulation of neutrophil signatures that correlated with expansion of immature neutrophils. Lupus pregnancies with fetal complications carried the highest interferon and plasma cell signatures as well as activated CD4+ T cell counts. Thus, blood immunomonitoring reveals that both healthy and uncomplicated lupus pregnancies exhibit early and sustained transcriptional modulation of lupus-related signatures, and a lack thereof associates with adverse outcomes.

UR - http://www.scopus.com/inward/record.url?scp=85065550012&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85065550012&partnerID=8YFLogxK

U2 - 10.1084/jem.20190185

DO - 10.1084/jem.20190185

M3 - Article

C2 - 30962246

AN - SCOPUS:85065550012

SN - 0022-1007

VL - 216

SP - 1154

EP - 1169

JO - Journal of Experimental Medicine

JF - Journal of Experimental Medicine

IS - 5

ER -

Longitudinal profiling of human blood transcriptome in healthy and lupus pregnancy

Abstract

Bibliographical note

All Science Journal Classification (ASJC) codes

UN SDGs

Access to Document

Other files and links

Fingerprint

Cite this