Persisting fetal clonotypes influence the structure and overlap of adult human T cell receptor repertoires

The diversity of T-cell receptors recognizing foreign pathogens is generated through a highly stochastic recombination process, making the independent production of the same sequence rare. Yet unrelated individuals do share receptors, which together constitute a "public" repertoire of abun...

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Published in:PLoS computational biology Vol. 13; no. 7; p. e1005572
Main Authors: Pogorelyy, Mikhail V., Elhanati, Yuval, Marcou, Quentin, Sycheva, Anastasiia L., Komech, Ekaterina A., Nazarov, Vadim I., Britanova, Olga V., Chudakov, Dmitriy M., Mamedov, Ilgar Z., Lebedev, Yury B., Mora, Thierry, Walczak, Aleksandra M.
Format: Journal Article
Language:English
Published: United States Public Library of Science 01.07.2017
PLOS
Public Library of Science (PLoS)
Subjects:
Age
Aging - genetics
Aging - immunology
Base Sequence
Bioinformatics
Biology and Life Sciences
Cells, Cultured
Cloning
Cord blood
Data analysis
Decay rate
Fetuses
Gene Expression Regulation, Developmental - genetics
Gene Expression Regulation, Developmental - immunology
Gene Rearrangement, T-Lymphocyte - genetics
Genetic Variation - genetics
Humans
Immune system
Leukemia
Life Sciences
Lymphocytes
Lymphocytes T
Medical research
Medicine and Health Sciences
Molecular Sequence Data
Nucleotides
Pathogens
Peptides
Physiological aspects
Receptors
Receptors, Antigen, T-Cell - physiology
Recombination
Recombination, Genetic
Research and Analysis Methods
Stochastic processes
Stochasticity
T cell antigen receptors
T cell receptors
T-Cell Antigen Receptor Specificity - genetics
T-cell receptor
Twins
Twins, Monozygotic - genetics
ISSN:1553-7358, 1553-734X, 1553-7358
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Abstract The diversity of T-cell receptors recognizing foreign pathogens is generated through a highly stochastic recombination process, making the independent production of the same sequence rare. Yet unrelated individuals do share receptors, which together constitute a "public" repertoire of abundant clonotypes. The TCR repertoire is initially formed prenatally, when the enzyme inserting random nucleotides is downregulated, producing a limited diversity subset. By statistically analyzing deep sequencing T-cell repertoire data from twins, unrelated individuals of various ages, and cord blood, we show that T-cell clones generated before birth persist and maintain high abundances in adult organisms for decades, slowly decaying with age. Our results suggest that large, low-diversity public clones are created during pre-natal life, and survive over long periods, providing the basis of the public repertoire.
AbstractList The diversity of T-cell receptors recognizing foreign pathogens is generated through a highly stochastic recombination process, making the independent production of the same sequence rare. Yet unrelated individuals do share receptors, which together constitute a " public " repertoire of abundant clonotypes. The TCR repertoire is initially formed prenatally, when the enzyme inserting random nucleotides is downregulated, producing a limited diversity subset. By statistically analyzing deep sequencing T-cell repertoire data from twins, unrelated individuals of various ages, and cord blood, we show that T-cell clones generated before birth persist and maintain high abundances in adult organisms for decades, slowly decaying with age. Our results suggest that large, low-diversity public clones are created during pre-natal life, and survive over long periods, providing the basis of the public repertoire.
The diversity of T-cell receptors recognizing foreign pathogens is generated through a highly stochastic recombination process, making the independent production of the same sequence rare. Yet unrelated individuals do share receptors, which together constitute a “public” repertoire of abundant clonotypes. The TCR repertoire is initially formed prenatally, when the enzyme inserting random nucleotides is downregulated, producing a limited diversity subset. By statistically analyzing deep sequencing T-cell repertoire data from twins, unrelated individuals of various ages, and cord blood, we show that T-cell clones generated before birth persist and maintain high abundances in adult organisms for decades, slowly decaying with age. Our results suggest that large, low-diversity public clones are created during pre-natal life, and survive over long periods, providing the basis of the public repertoire. The enormous diversity of T-cell receptor (TCR) molecules allows our adaptive immune system to recognize and fight infections. TCRs are formed through the stochastic rearrangement of DNA. By analysing human repertoire sequences of identical twins using a statistical model for TCR formation, we identified T-cells that were exchanged between twin embryos during pregnancy. We exploited the slightly different recombination statistics between fetal clonotypes and mature ones to track their relative fractions in adult T-cell repertoires of different ages. We showed that the decay of fetal clonotypes with age is extremely slow, spanning several decades. Our findings suggest that an important part of our adaptive immune system is formed before birth.
The diversity of T-cell receptors recognizing foreign pathogens is generated through a highly stochastic recombination process, making the independent production of the same sequence rare. Yet unrelated individuals do share receptors, which together constitute a "public" repertoire of abundant clonotypes. The TCR repertoire is initially formed prenatally, when the enzyme inserting random nucleotides is downregulated, producing a limited diversity subset. By statistically analyzing deep sequencing T-cell repertoire data from twins, unrelated individuals of various ages, and cord blood, we show that T-cell clones generated before birth persist and maintain high abundances in adult organisms for decades, slowly decaying with age. Our results suggest that large, low-diversity public clones are created during pre-natal life, and survive over long periods, providing the basis of the public repertoire.The diversity of T-cell receptors recognizing foreign pathogens is generated through a highly stochastic recombination process, making the independent production of the same sequence rare. Yet unrelated individuals do share receptors, which together constitute a "public" repertoire of abundant clonotypes. The TCR repertoire is initially formed prenatally, when the enzyme inserting random nucleotides is downregulated, producing a limited diversity subset. By statistically analyzing deep sequencing T-cell repertoire data from twins, unrelated individuals of various ages, and cord blood, we show that T-cell clones generated before birth persist and maintain high abundances in adult organisms for decades, slowly decaying with age. Our results suggest that large, low-diversity public clones are created during pre-natal life, and survive over long periods, providing the basis of the public repertoire.
Audience Academic
Author Chudakov, Dmitriy M.
Walczak, Aleksandra M.
Marcou, Quentin
Lebedev, Yury B.
Elhanati, Yuval
Komech, Ekaterina A.
Mamedov, Ilgar Z.
Sycheva, Anastasiia L.
Mora, Thierry
Pogorelyy, Mikhail V.
Nazarov, Vadim I.
Britanova, Olga V.
AuthorAffiliation 4 Masaryk University, Central European Institute of Technology, Brno, Czech Republic
3 Pirogov Russian National Research Medical University, Moscow, Russian Federation
Fred Hutchinson Cancer Research Center, UNITED STATES
2 Laboratoire de physique théorique, CNRS, UPMC and École normale supérieure, Paris, France
1 Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
5 Laboratoire de physique statistique, CNRS, UPMC and École normale supérieure, Paris, France
AuthorAffiliation_xml – name: 4 Masaryk University, Central European Institute of Technology, Brno, Czech Republic
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– name: Fred Hutchinson Cancer Research Center, UNITED STATES
– name: 1 Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow, Russian Federation
– name: 5 Laboratoire de physique statistique, CNRS, UPMC and École normale supérieure, Paris, France
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  givenname: Mikhail V.
  surname: Pogorelyy
  fullname: Pogorelyy, Mikhail V.
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  surname: Elhanati
  fullname: Elhanati, Yuval
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  orcidid: 0000-0001-7074-2761
  surname: Marcou
  fullname: Marcou, Quentin
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  surname: Sycheva
  fullname: Sycheva, Anastasiia L.
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  surname: Komech
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  orcidid: 0000-0003-0430-790X
  surname: Chudakov
  fullname: Chudakov, Dmitriy M.
– sequence: 9
  givenname: Ilgar Z.
  surname: Mamedov
  fullname: Mamedov, Ilgar Z.
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  surname: Mora
  fullname: Mora, Thierry
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  givenname: Aleksandra M.
  surname: Walczak
  fullname: Walczak, Aleksandra M.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28683116$$D View this record in MEDLINE/PubMed
https://hal.sorbonne-universite.fr/hal-01579464$$DView record in HAL
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ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Pogorelyy MV, Elhanati Y, Marcou Q, Sycheva AL, Komech EA, Nazarov VI, et al. (2017) Persisting fetal clonotypes influence the structure and overlap of adult human T cell receptor repertoires. PLoS Comput Biol 13(7): e1005572. https://doi.org/10.1371/journal.pcbi.1005572
Attribution
2017 Pogorelyy et al 2017 Pogorelyy et al
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Pogorelyy MV, Elhanati Y, Marcou Q, Sycheva AL, Komech EA, Nazarov VI, et al. (2017) Persisting fetal clonotypes influence the structure and overlap of adult human T cell receptor repertoires. PLoS Comput Biol 13(7): e1005572. https://doi.org/10.1371/journal.pcbi.1005572
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Pogorelyy MV, Elhanati Y, Marcou Q, Sycheva AL, Komech EA, Nazarov VI, et al. (2017) Persisting fetal clonotypes influence the structure and overlap of adult human T cell receptor repertoires. PLoS Comput Biol 13(7): e1005572. https://doi.org/10.1371/journal.pcbi.1005572
– notice: Attribution
– notice: 2017 Pogorelyy et al 2017 Pogorelyy et al
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Pogorelyy MV, Elhanati Y, Marcou Q, Sycheva AL, Komech EA, Nazarov VI, et al. (2017) Persisting fetal clonotypes influence the structure and overlap of adult human T cell receptor repertoires. PLoS Comput Biol 13(7): e1005572. https://doi.org/10.1371/journal.pcbi.1005572
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Conceptualization: DMC IZM YBL TM AMW.Data curation: MVP.Formal analysis: MVP YE QM TM AMW.Funding acquisition: DMC IZM YBL TM AMW.Investigation: MVP ALS EAK OVB.Methodology: MVP YE QM TM AMW.Project administration: DMC IZM YBL TM AMW.Resources: MVP ALS EAK OVB.Software: MVP YE QM VIN.Supervision: DMC IZM YBL TM AMW.Writing – original draft: TM AMW MVP.Writing – review & editing: TM AMW MVP.
The authors have declared that no competing interests exist.
ORCID 0000-0002-5456-9361
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Snippet The diversity of T-cell receptors recognizing foreign pathogens is generated through a highly stochastic recombination process, making the independent...
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SubjectTerms Age
Aging - genetics
Aging - immunology
Base Sequence
Bioinformatics
Biology and Life Sciences
Cells, Cultured
Cloning
Cord blood
Data analysis
Decay rate
Fetuses
Gene Expression Regulation, Developmental - genetics
Gene Expression Regulation, Developmental - immunology
Gene Rearrangement, T-Lymphocyte - genetics
Genetic Variation - genetics
Humans
Immune system
Leukemia
Life Sciences
Lymphocytes
Lymphocytes T
Medical research
Medicine and Health Sciences
Molecular Sequence Data
Nucleotides
Pathogens
Peptides
Physiological aspects
Receptors
Receptors, Antigen, T-Cell - physiology
Recombination
Recombination, Genetic
Research and Analysis Methods
Stochastic processes
Stochasticity
T cell antigen receptors
T cell receptors
T-Cell Antigen Receptor Specificity - genetics
T-cell receptor
Twins
Twins, Monozygotic - genetics
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Title Persisting fetal clonotypes influence the structure and overlap of adult human T cell receptor repertoires
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