Dynamic molecular changes during the first week of human life follow a robust developmental trajectory

Amy H. Lee; Casey P. Shannon; Nelly Amenyogbe; Tue B. Bennike; Joann Diray-Arce; Olubukola T. Idoko; Erin E. Gill; Rym Ben-Othman; William S. Pomat; Simon D. van Haren; Kim Anh Lê Cao; Momoudou Cox; Alansana Darboe; Reza Falsafi; Davide Ferrari; Daniel J. Harbeson; Daniel He; Cai Bing; Samuel J. Hinshaw; Jorjoh Ndure; Jainaba Njie-Jobe; Matthew A. Pettengill; Peter C. Richmond; Rebecca Ford; Gerard Saleu; Geraldine Masiria; John Paul Matlam; Wendy Kirarock; Elishia Roberts; Mehrnoush Malek; Guzmán Sanchez-Schmitz; Amrit Singh; Asimenia Angelidou; Kinga K. Smolen; The EPIC Consortium; Ryan R. Brinkman; Al Ozonoff; Robert E.W. Hancock; Anita H.J. van den Biggelaar; Hanno Steen; Scott J. Tebbutt; Beate Kampmann; Ofer Levy; Tobias R. Kollmann

doi:10.1038/s41467-019-08794-x

Dynamic molecular changes during the first week of human life follow a robust developmental trajectory

Amy H. Lee, Casey P. Shannon, Nelly Amenyogbe, Tue B. Bennike, Joann Diray-Arce, Olubukola T. Idoko, Erin E. Gill, Rym Ben-Othman, William S. Pomat, Simon D. van Haren, Kim Anh Lê Cao, Momoudou Cox, Alansana Darboe, Reza Falsafi, Davide Ferrari, Daniel J. Harbeson, Daniel He, Cai Bing, Samuel J. Hinshaw, Jorjoh NdureJainaba Njie-Jobe, Matthew A. Pettengill, Peter C. Richmond, Rebecca Ford, Gerard Saleu, Geraldine Masiria, John Paul Matlam, Wendy Kirarock, Elishia Roberts, Mehrnoush Malek, Guzmán Sanchez-Schmitz, Amrit Singh, Asimenia Angelidou, Kinga K. Smolen, The EPIC Consortium, Ryan R. Brinkman, Al Ozonoff, Robert E.W. Hancock, Anita H.J. van den Biggelaar, Hanno Steen, Scott J. Tebbutt, Beate Kampmann, Ofer Levy, Tobias R. Kollmann^*

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › Research › peer-review

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Abstract

Systems biology can unravel complex biology but has not been extensively applied to human newborns, a group highly vulnerable to a wide range of diseases. We optimized methods to extract transcriptomic, proteomic, metabolomic, cytokine/chemokine, and single cell immune phenotyping data from <1 ml of blood, a volume readily obtained from newborns. Indexing to baseline and applying innovative integrative computational methods reveals dramatic changes along a remarkably stable developmental trajectory over the first week of life. This is most evident in changes of interferon and complement pathways, as well as neutrophil-associated signaling. Validated across two independent cohorts of newborns from West Africa and Australasia, a robust and common trajectory emerges, suggesting a purposeful rather than random developmental path. Systems biology and innovative data integration can provide fresh insights into the molecular ontogeny of the first week of life, a dynamic developmental phase that is key for health and disease.

Original language	English
Article number	1092
Journal	Nature Communications
Volume	10
Issue number	1
Number of pages	14
ISSN	2041-1723
DOIs	https://doi.org/10.1038/s41467-019-08794-x
Publication status	Published - 12 Mar 2019

Keywords

Chemokines/blood
Child Development/physiology
Cohort Studies
Cytokines/blood
Gambia
Gene Expression Profiling
Humans
Immunophenotyping
Infant, Newborn/blood
Metabolomics
Papua New Guinea
Proteomics
Systems Biology

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10.1038/s41467-019-08794-x

Open Access ArticleFinal published version, 4.26 MBLicence: CC BY 4.0

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Lee, A. H., Shannon, C. P., Amenyogbe, N., Bennike, T. B., Diray-Arce, J., Idoko, O. T., Gill, E. E., Ben-Othman, R., Pomat, W. S., van Haren, S. D., Cao, K. A. L., Cox, M., Darboe, A., Falsafi, R., Ferrari, D., Harbeson, D. J., He, D., Bing, C., Hinshaw, S. J., ... Kollmann, T. R. (2019). Dynamic molecular changes during the first week of human life follow a robust developmental trajectory. Nature Communications, 10(1), Article 1092. https://doi.org/10.1038/s41467-019-08794-x

@article{a883a18f26304edfa9b4aa008fca0d0c,

title = "Dynamic molecular changes during the first week of human life follow a robust developmental trajectory",

abstract = "Systems biology can unravel complex biology but has not been extensively applied to human newborns, a group highly vulnerable to a wide range of diseases. We optimized methods to extract transcriptomic, proteomic, metabolomic, cytokine/chemokine, and single cell immune phenotyping data from <1 ml of blood, a volume readily obtained from newborns. Indexing to baseline and applying innovative integrative computational methods reveals dramatic changes along a remarkably stable developmental trajectory over the first week of life. This is most evident in changes of interferon and complement pathways, as well as neutrophil-associated signaling. Validated across two independent cohorts of newborns from West Africa and Australasia, a robust and common trajectory emerges, suggesting a purposeful rather than random developmental path. Systems biology and innovative data integration can provide fresh insights into the molecular ontogeny of the first week of life, a dynamic developmental phase that is key for health and disease.",

keywords = "Chemokines/blood, Child Development/physiology, Cohort Studies, Cytokines/blood, Gambia, Gene Expression Profiling, Humans, Immunophenotyping, Infant, Newborn/blood, Metabolomics, Papua New Guinea, Proteomics, Systems Biology",

author = "Lee, {Amy H.} and Shannon, {Casey P.} and Nelly Amenyogbe and Bennike, {Tue B.} and Joann Diray-Arce and Idoko, {Olubukola T.} and Gill, {Erin E.} and Rym Ben-Othman and Pomat, {William S.} and {van Haren}, {Simon D.} and Cao, {Kim Anh L{\^e}} and Momoudou Cox and Alansana Darboe and Reza Falsafi and Davide Ferrari and Harbeson, {Daniel J.} and Daniel He and Cai Bing and Hinshaw, {Samuel J.} and Jorjoh Ndure and Jainaba Njie-Jobe and Pettengill, {Matthew A.} and Richmond, {Peter C.} and Rebecca Ford and Gerard Saleu and Geraldine Masiria and Matlam, {John Paul} and Wendy Kirarock and Elishia Roberts and Mehrnoush Malek and Guzm{\'a}n Sanchez-Schmitz and Amrit Singh and Asimenia Angelidou and Smolen, {Kinga K.} and {The EPIC Consortium} and Diana Vo and Ken Kraft and Kerry McEnaney and Sofia Vignolo and Arnaud Marchant and Brinkman, {Ryan R.} and Al Ozonoff and Hancock, {Robert E.W.} and {van den Biggelaar}, {Anita H.J.} and Hanno Steen and Tebbutt, {Scott J.} and Beate Kampmann and Ofer Levy and Kollmann, {Tobias R.}",

year = "2019",

month = mar,

day = "12",

doi = "10.1038/s41467-019-08794-x",

language = "English",

volume = "10",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

}

Lee, AH, Shannon, CP, Amenyogbe, N, Bennike, TB, Diray-Arce, J, Idoko, OT, Gill, EE, Ben-Othman, R, Pomat, WS, van Haren, SD, Cao, KAL, Cox, M, Darboe, A, Falsafi, R, Ferrari, D, Harbeson, DJ, He, D, Bing, C, Hinshaw, SJ, Ndure, J, Njie-Jobe, J, Pettengill, MA, Richmond, PC, Ford, R, Saleu, G, Masiria, G, Matlam, JP, Kirarock, W, Roberts, E, Malek, M, Sanchez-Schmitz, G, Singh, A, Angelidou, A, Smolen, KK, The EPIC Consortium, Brinkman, RR, Ozonoff, A, Hancock, REW, van den Biggelaar, AHJ, Steen, H, Tebbutt, SJ, Kampmann, B, Levy, O & Kollmann, TR 2019, 'Dynamic molecular changes during the first week of human life follow a robust developmental trajectory', Nature Communications, vol. 10, no. 1, 1092. https://doi.org/10.1038/s41467-019-08794-x

TY - JOUR

T1 - Dynamic molecular changes during the first week of human life follow a robust developmental trajectory

AU - Lee, Amy H.

AU - Shannon, Casey P.

AU - Amenyogbe, Nelly

AU - Bennike, Tue B.

AU - Diray-Arce, Joann

AU - Idoko, Olubukola T.

AU - Gill, Erin E.

AU - Ben-Othman, Rym

AU - Pomat, William S.

AU - van Haren, Simon D.

AU - Cao, Kim Anh Lê

AU - Cox, Momoudou

AU - Darboe, Alansana

AU - Falsafi, Reza

AU - Ferrari, Davide

AU - Harbeson, Daniel J.

AU - He, Daniel

AU - Bing, Cai

AU - Hinshaw, Samuel J.

AU - Ndure, Jorjoh

AU - Njie-Jobe, Jainaba

AU - Pettengill, Matthew A.

AU - Richmond, Peter C.

AU - Ford, Rebecca

AU - Saleu, Gerard

AU - Masiria, Geraldine

AU - Matlam, John Paul

AU - Kirarock, Wendy

AU - Roberts, Elishia

AU - Malek, Mehrnoush

AU - Sanchez-Schmitz, Guzmán

AU - Singh, Amrit

AU - Angelidou, Asimenia

AU - Smolen, Kinga K.

AU - The EPIC Consortium

AU - Vo, Diana

AU - Kraft, Ken

AU - McEnaney, Kerry

AU - Vignolo, Sofia

AU - Marchant, Arnaud

AU - Brinkman, Ryan R.

AU - Ozonoff, Al

AU - Hancock, Robert E.W.

AU - van den Biggelaar, Anita H.J.

AU - Steen, Hanno

AU - Tebbutt, Scott J.

AU - Kampmann, Beate

AU - Levy, Ofer

AU - Kollmann, Tobias R.

PY - 2019/3/12

Y1 - 2019/3/12

N2 - Systems biology can unravel complex biology but has not been extensively applied to human newborns, a group highly vulnerable to a wide range of diseases. We optimized methods to extract transcriptomic, proteomic, metabolomic, cytokine/chemokine, and single cell immune phenotyping data from <1 ml of blood, a volume readily obtained from newborns. Indexing to baseline and applying innovative integrative computational methods reveals dramatic changes along a remarkably stable developmental trajectory over the first week of life. This is most evident in changes of interferon and complement pathways, as well as neutrophil-associated signaling. Validated across two independent cohorts of newborns from West Africa and Australasia, a robust and common trajectory emerges, suggesting a purposeful rather than random developmental path. Systems biology and innovative data integration can provide fresh insights into the molecular ontogeny of the first week of life, a dynamic developmental phase that is key for health and disease.

AB - Systems biology can unravel complex biology but has not been extensively applied to human newborns, a group highly vulnerable to a wide range of diseases. We optimized methods to extract transcriptomic, proteomic, metabolomic, cytokine/chemokine, and single cell immune phenotyping data from <1 ml of blood, a volume readily obtained from newborns. Indexing to baseline and applying innovative integrative computational methods reveals dramatic changes along a remarkably stable developmental trajectory over the first week of life. This is most evident in changes of interferon and complement pathways, as well as neutrophil-associated signaling. Validated across two independent cohorts of newborns from West Africa and Australasia, a robust and common trajectory emerges, suggesting a purposeful rather than random developmental path. Systems biology and innovative data integration can provide fresh insights into the molecular ontogeny of the first week of life, a dynamic developmental phase that is key for health and disease.

KW - Chemokines/blood

KW - Child Development/physiology

KW - Cohort Studies

KW - Cytokines/blood

KW - Gambia

KW - Gene Expression Profiling

KW - Humans

KW - Immunophenotyping

KW - Infant, Newborn/blood

KW - Metabolomics

KW - Papua New Guinea

KW - Proteomics

KW - Systems Biology

UR - http://www.scopus.com/inward/record.url?scp=85062844417&partnerID=8YFLogxK

U2 - 10.1038/s41467-019-08794-x

DO - 10.1038/s41467-019-08794-x

M3 - Journal article

C2 - 30862783

AN - SCOPUS:85062844417

SN - 2041-1723

VL - 10

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 1092

ER -

Dynamic molecular changes during the first week of human life follow a robust developmental trajectory

Abstract

Keywords

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The innate immune system: Ontogeny and role in inflammatory diseases

Development of the humoral innate immune system the first week after birth

Preparing for life: Plasma proteome changes and immune system development during the first week of human life

Ontogeny of the plasma proteome across the first week of human life

Cite this

Dynamic molecular changes during the first week of human life follow a robust developmental trajectory

Abstract

Keywords

Access to Document

AUB Link

Other files and links

Fingerprint

Projects

The innate immune system: Ontogeny and role in inflammatory diseases

Activities

Development of the humoral innate immune system the first week after birth

Preparing for life: Plasma proteome changes and immune system development during the first week of human life

Ontogeny of the plasma proteome across the first week of human life

Cite this