Clonal evolution and antigen recognition of anti-nuclear antibodies in acute systemic lupus erythematosus

The evolutional process of disease-associated autoantibodies in systemic lupus erythematosus (SLE) remains to be established. Here we show intraclonal diversification and affinity maturation of anti-nuclear antibody (ANA)-producing B cells in SLE. We identified a panel of monoclonal ANAs recognizing...

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Published inScientific reports Vol. 7; no. 1; pp. 16428 - 14
Main Authors Sakakibara, Shuhei, Arimori, Takao, Yamashita, Kazuo, Jinzai, Hideyuki, Motooka, Daisuke, Nakamura, Shota, Li, Songling, Takeda, Kazuya, Katayama, Jun, El Hussien, Marwa Ali, Narazaki, Masashi, Tanaka, Toshio, Standley, Daron M., Takagi, Junichi, Kikutani, Hitoshi
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 27.11.2017
Nature Publishing Group
Subjects
101/1
631/250/38
631/45/535/1266
Acute Disease
Affinity
Amino Acid Sequence
Anti-DNA antibodies
Antibodies, Antinuclear - chemistry
Antibodies, Antinuclear - immunology
Antigens
Antigens - chemistry
Antigens - immunology
Autoantibodies
Autoantibodies - blood
Autoimmune diseases
Biochemical analysis
Clonal Evolution - immunology
Crystal structure
Deoxyribonucleic acid
DNA
DNA - immunology
HEK293 Cells
Humanities and Social Sciences
Humans
Immunoglobulins
Lupus
Lupus Erythematosus, Systemic - blood
Lupus Erythematosus, Systemic - immunology
Lymphocytes
Lymphocytes B
multidisciplinary
Mutation
Mutation - genetics
Mutation Rate
Phylogeny
Ribonucleoproteins
Science
Science (multidisciplinary)
Syndecan-1 - metabolism
Systemic lupus erythematosus
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Abstract The evolutional process of disease-associated autoantibodies in systemic lupus erythematosus (SLE) remains to be established. Here we show intraclonal diversification and affinity maturation of anti-nuclear antibody (ANA)-producing B cells in SLE. We identified a panel of monoclonal ANAs recognizing nuclear antigens, such as double-stranded DNA (dsDNA) and ribonucleoproteins (RNPs) from acute SLE subjects. These ANAs had relatively few, but nonetheless critical mutations. High-throughput immunoglobulin sequencing of blood lymphocytes disclosed the existence of sizable ANA lineages shearing critical mutations intraclonally. We further focused on anti-DNA antibodies, which are capable to bind to both single-stranded (ss) and dsDNA at high affinity. Crystal structure and biochemical analysis confirmed a direct role of the mutations in the acquisition of DNA reactivity and also revealed that these anti-DNA antibodies recognized an unpaired region within DNA duplex. Our study unveils the unique properties of high-affinity anti-DNA antibodies that are generated through antigen-driven affinity maturation in acute phase of SLE.
AbstractList The evolutional process of disease-associated autoantibodies in systemic lupus erythematosus (SLE) remains to be established. Here we show intraclonal diversification and affinity maturation of anti-nuclear antibody (ANA)-producing B cells in SLE. We identified a panel of monoclonal ANAs recognizing nuclear antigens, such as double-stranded DNA (dsDNA) and ribonucleoproteins (RNPs) from acute SLE subjects. These ANAs had relatively few, but nonetheless critical mutations. High-throughput immunoglobulin sequencing of blood lymphocytes disclosed the existence of sizable ANA lineages shearing critical mutations intraclonally. We further focused on anti-DNA antibodies, which are capable to bind to both single-stranded (ss) and dsDNA at high affinity. Crystal structure and biochemical analysis confirmed a direct role of the mutations in the acquisition of DNA reactivity and also revealed that these anti-DNA antibodies recognized an unpaired region within DNA duplex. Our study unveils the unique properties of high-affinity anti-DNA antibodies that are generated through antigen-driven affinity maturation in acute phase of SLE.The evolutional process of disease-associated autoantibodies in systemic lupus erythematosus (SLE) remains to be established. Here we show intraclonal diversification and affinity maturation of anti-nuclear antibody (ANA)-producing B cells in SLE. We identified a panel of monoclonal ANAs recognizing nuclear antigens, such as double-stranded DNA (dsDNA) and ribonucleoproteins (RNPs) from acute SLE subjects. These ANAs had relatively few, but nonetheless critical mutations. High-throughput immunoglobulin sequencing of blood lymphocytes disclosed the existence of sizable ANA lineages shearing critical mutations intraclonally. We further focused on anti-DNA antibodies, which are capable to bind to both single-stranded (ss) and dsDNA at high affinity. Crystal structure and biochemical analysis confirmed a direct role of the mutations in the acquisition of DNA reactivity and also revealed that these anti-DNA antibodies recognized an unpaired region within DNA duplex. Our study unveils the unique properties of high-affinity anti-DNA antibodies that are generated through antigen-driven affinity maturation in acute phase of SLE.
The evolutional process of disease-associated autoantibodies in systemic lupus erythematosus (SLE) remains to be established. Here we show intraclonal diversification and affinity maturation of anti-nuclear antibody (ANA)-producing B cells in SLE. We identified a panel of monoclonal ANAs recognizing nuclear antigens, such as double-stranded DNA (dsDNA) and ribonucleoproteins (RNPs) from acute SLE subjects. These ANAs had relatively few, but nonetheless critical mutations. High-throughput immunoglobulin sequencing of blood lymphocytes disclosed the existence of sizable ANA lineages shearing critical mutations intraclonally. We further focused on anti-DNA antibodies, which are capable to bind to both single-stranded (ss) and dsDNA at high affinity. Crystal structure and biochemical analysis confirmed a direct role of the mutations in the acquisition of DNA reactivity and also revealed that these anti-DNA antibodies recognized an unpaired region within DNA duplex. Our study unveils the unique properties of high-affinity anti-DNA antibodies that are generated through antigen-driven affinity maturation in acute phase of SLE.
ArticleNumber 16428
Author Jinzai, Hideyuki
El Hussien, Marwa Ali
Arimori, Takao
Katayama, Jun
Tanaka, Toshio
Nakamura, Shota
Standley, Daron M.
Yamashita, Kazuo
Takeda, Kazuya
Narazaki, Masashi
Motooka, Daisuke
Li, Songling
Sakakibara, Shuhei
Takagi, Junichi
Kikutani, Hitoshi
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  fullname: Tanaka, Toshio
  organization: Laboratory of Immunopathology, Immunology Frontier Research Center, Osaka University, Suita, Department of Respiratory Medicine and Clinical Immunology, Graduate School of Medicine, Osaka University, Suita, Department of Clinical Application of Biologics, Graduate School of Medicine, Osaka University, Suita
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  givenname: Daron M.
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Snippet The evolutional process of disease-associated autoantibodies in systemic lupus erythematosus (SLE) remains to be established. Here we show intraclonal...
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SubjectTerms 101/1
631/250/38
631/45/535/1266
Acute Disease
Affinity
Amino Acid Sequence
Anti-DNA antibodies
Antibodies, Antinuclear - chemistry
Antibodies, Antinuclear - immunology
Antigens
Antigens - chemistry
Antigens - immunology
Autoantibodies
Autoantibodies - blood
Autoimmune diseases
Biochemical analysis
Clonal Evolution - immunology
Crystal structure
Deoxyribonucleic acid
DNA
DNA - immunology
HEK293 Cells
Humanities and Social Sciences
Humans
Immunoglobulins
Lupus
Lupus Erythematosus, Systemic - blood
Lupus Erythematosus, Systemic - immunology
Lymphocytes
Lymphocytes B
multidisciplinary
Mutation
Mutation - genetics
Mutation Rate
Phylogeny
Ribonucleoproteins
Science
Science (multidisciplinary)
Syndecan-1 - metabolism
Systemic lupus erythematosus
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Title Clonal evolution and antigen recognition of anti-nuclear antibodies in acute systemic lupus erythematosus
URI https://link.springer.com/article/10.1038/s41598-017-16681-y
https://www.ncbi.nlm.nih.gov/pubmed/29180749
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https://www.proquest.com/docview/1969919575
https://pubmed.ncbi.nlm.nih.gov/PMC5703881
Volume 7
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