Bimodal Expansion of the Lymphatic Vessels Is Regulated by the Sequential Expression of IL-7 and Lymphotoxin α1β2 in Newly Formed Tertiary Lymphoid Structures

Lymphangiogenesis associated with tertiary lymphoid structure (TLS) has been reported in numerous studies. However, the kinetics and dynamic changes occurring to the lymphatic vascular network during TLS development have not been studied. Using a viral-induced, resolving model of TLS formation in th...

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Published inThe Journal of immunology (1950) Vol. 197; no. 5; pp. 1957 - 1967
Main Authors Nayar, Saba, Campos, Joana, Chung, Ming May, Navarro-Núñez, Leyre, Chachlani, Menka, Steinthal, Nathalie, Gardner, David H, Rankin, Philip, Cloake, Thomas, Caamaño, Jorge H, McGettrick, Helen M, Watson, Steve P, Luther, Sanjiv, Buckley, Christopher D, Barone, Francesca
Format Journal Article
LanguageEnglish
Published United States AAI 01.09.2016
Subjects
Animals
Gene Expression Regulation
Inflammation
Interleukin-7 - genetics
Interleukin-7 - immunology
Interleukin-7 - metabolism
Lymphangiogenesis
Lymphatic Vessels - immunology
Lymphatic Vessels - metabolism
Lymphotoxin alpha1, beta2 Heterotrimer - genetics
Lymphotoxin alpha1, beta2 Heterotrimer - immunology
Lymphotoxin alpha1, beta2 Heterotrimer - metabolism
Mice
Mucosal Immunology
Salivary Glands - immunology
Signal Transduction - genetics
Signal Transduction - immunology
Tertiary Lymphoid Structures - immunology
Tertiary Lymphoid Structures - pathology
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Abstract Lymphangiogenesis associated with tertiary lymphoid structure (TLS) has been reported in numerous studies. However, the kinetics and dynamic changes occurring to the lymphatic vascular network during TLS development have not been studied. Using a viral-induced, resolving model of TLS formation in the salivary glands of adult mice we demonstrate that the expansion of the lymphatic vascular network is tightly regulated. Lymphatic vessel expansion occurs in two distinct phases. The first wave of expansion is dependent on IL-7. The second phase, responsible for leukocyte exit from the glands, is regulated by lymphotoxin (LT)βR signaling. These findings, while highlighting the tight regulation of the lymphatic response to inflammation, suggest that targeting the LTα1β2/LTβR pathway in TLS-associated pathologies might impair a natural proresolving mechanism for lymphocyte exit from the tissues and account for the failure of therapeutic strategies that target these molecules in diseases such as rheumatoid arthritis.
AbstractList Lymphangiogenesis associated with tertiary lymphoid structure (TLS) has been reported in numerous studies. However, the kinetics and dynamic changes occurring to the lymphatic vascular network during TLS development have not been studied. Using a viral-induced, resolving model of TLS formation in the salivary glands of adult mice we demonstrate that the expansion of the lymphatic vascular network is tightly regulated. Lymphatic vessel expansion occurs in two distinct phases. The first wave of expansion is dependent on IL-7. The second phase, responsible for leukocyte exit from the glands, is regulated by lymphotoxin (LT)βR signaling. These findings, while highlighting the tight regulation of the lymphatic response to inflammation, suggest that targeting the LTα1β2/LTβR pathway in TLS-associated pathologies might impair a natural proresolving mechanism for lymphocyte exit from the tissues and account for the failure of therapeutic strategies that target these molecules in diseases such as rheumatoid arthritis.
Lymphangiogenesis associated with tertiary lymphoid structure (TLS) has been reported in numerous studies. However, the kinetics and dynamic changes occurring to the lymphatic vascular network during TLS development have not been studied. Using a viral-induced, resolving model of TLS formation in the salivary glands of adult mice we demonstrate that the expansion of the lymphatic vascular network is tightly regulated. Lymphatic vessel expansion occurs in two distinct phases. The first wave of expansion is dependent on IL-7. The second phase, responsible for leukocyte exit from the glands, is regulated by lymphotoxin (LT)βR signaling. These findings, while highlighting the tight regulation of the lymphatic response to inflammation, suggest that targeting the LTα 1 β 2 /LTβR pathway in TLS-associated pathologies might impair a natural proresolving mechanism for lymphocyte exit from the tissues and account for the failure of therapeutic strategies that target these molecules in diseases such as rheumatoid arthritis.
Author Watson, Steve P
Caamaño, Jorge H
McGettrick, Helen M
Luther, Sanjiv
Nayar, Saba
Navarro-Núñez, Leyre
Rankin, Philip
Gardner, David H
Buckley, Christopher D
Barone, Francesca
Campos, Joana
Steinthal, Nathalie
Chachlani, Menka
Chung, Ming May
Cloake, Thomas
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  organization: Rheumatology Research Group, Centre for Translational Inflammation Research, Institute of Inflammation and Ageing, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, Birmingham B15 2WD, United Kingdom
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  givenname: Ming May
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  givenname: Leyre
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  givenname: David H
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– sequence: 8
  givenname: Philip
  orcidid: 0000-0003-1633-7313
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– sequence: 9
  givenname: Thomas
  surname: Cloake
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– sequence: 10
  givenname: Jorge H
  orcidid: 0000-0003-3530-7056
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  orcidid: 0000-0001-6924-6402
  surname: Buckley
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  givenname: Francesca
  orcidid: 0000-0002-5287-9614
  surname: Barone
  fullname: Barone, Francesca
  email: f.barone@bham.ac.uk
  organization: Rheumatology Research Group, Centre for Translational Inflammation Research, Institute of Inflammation and Ageing, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, Birmingham B15 2WD, United Kingdom; f.barone@bham.ac.uk
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Snippet Lymphangiogenesis associated with tertiary lymphoid structure (TLS) has been reported in numerous studies. However, the kinetics and dynamic changes occurring...
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StartPage 1957
SubjectTerms Animals
Gene Expression Regulation
Inflammation
Interleukin-7 - genetics
Interleukin-7 - immunology
Interleukin-7 - metabolism
Lymphangiogenesis
Lymphatic Vessels - immunology
Lymphatic Vessels - metabolism
Lymphotoxin alpha1, beta2 Heterotrimer - genetics
Lymphotoxin alpha1, beta2 Heterotrimer - immunology
Lymphotoxin alpha1, beta2 Heterotrimer - metabolism
Mice
Mucosal Immunology
Salivary Glands - immunology
Signal Transduction - genetics
Signal Transduction - immunology
Tertiary Lymphoid Structures - immunology
Tertiary Lymphoid Structures - pathology
Title Bimodal Expansion of the Lymphatic Vessels Is Regulated by the Sequential Expression of IL-7 and Lymphotoxin α1β2 in Newly Formed Tertiary Lymphoid Structures
URI https://www.ncbi.nlm.nih.gov/pubmed/27474071
https://search.proquest.com/docview/1812886455
https://pubmed.ncbi.nlm.nih.gov/PMC4991245
Volume 197
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