Morphophysiological changes in the splenic extracellular matrix of Leishmania infantum-naturally infected dogs is associated with alterations in lymphoid niches and the CD4+ T cell frequency in spleens

The spleen is one of the main affected organs in canine visceral leishmaniasis (CVL). Disorganization of the splenic white pulp (SWP) has been associated with immunosuppression and disease progression. This study aims to assess structural and cellular changes in the splenic extracellular matrix of d...

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Veröffentlicht in:PLoS neglected tropical diseases 2018-04, Vol.12 (4), p.e0006445-e0006445
Hauptverfasser: da Silva, Aurea Virginia Andrade, Figueiredo, Fabiano Borges, Menezes, Rodrigo Caldas, Mendes-Junior, Arthur Augusto, de Miranda, Luisa Helena Monteiro, Cupolillo, Elisa, Porrozzi, Renato, Morgado, Fernanda Nazaré
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container_title PLoS neglected tropical diseases
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creator da Silva, Aurea Virginia Andrade
Figueiredo, Fabiano Borges
Menezes, Rodrigo Caldas
Mendes-Junior, Arthur Augusto
de Miranda, Luisa Helena Monteiro
Cupolillo, Elisa
Porrozzi, Renato
Morgado, Fernanda Nazaré
description The spleen is one of the main affected organs in canine visceral leishmaniasis (CVL). Disorganization of the splenic white pulp (SWP) has been associated with immunosuppression and disease progression. This study aims to assess structural and cellular changes in the splenic extracellular matrix of dogs with CVL, correlating these changes with the parasite load and clinical signs. Splenic fragments were collected from 41 naturally infected animals for parasite load quantification by quantitative PCR, histopathological analysis and immunohistochemistry for CD3+, CD4+, and CD8+ T cells; CD21+ B cells; Ki-67+, IFN-γ+, and IL-10+ cells; and the MMP-9 and ADAM-10 enzymes. Laminin, collagen and fibronectin deposition were also evaluated. The animals were grouped according to the level of SWP organization. SWP disorganization was accompanied by a reduction in the quantity of lymphoid follicles/mm2 (p > 0.0001). Animals with moderate to intense SWP disorganization showed more clinical signs (p = 0.021), higher laminin (p = 0.045) and collagen deposition (p = 0.036), higher MMP-9 expression (p = 0.035) and lower numbers of CD4+ T cells (p = 0.027) in the spleen than the animals with organized SWP. These data suggest that splenic structure and function are drastically altered and compromised during CVL.
doi_str_mv 10.1371/journal.pntd.0006445
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Disorganization of the splenic white pulp (SWP) has been associated with immunosuppression and disease progression. This study aims to assess structural and cellular changes in the splenic extracellular matrix of dogs with CVL, correlating these changes with the parasite load and clinical signs. Splenic fragments were collected from 41 naturally infected animals for parasite load quantification by quantitative PCR, histopathological analysis and immunohistochemistry for CD3+, CD4+, and CD8+ T cells; CD21+ B cells; Ki-67+, IFN-γ+, and IL-10+ cells; and the MMP-9 and ADAM-10 enzymes. Laminin, collagen and fibronectin deposition were also evaluated. The animals were grouped according to the level of SWP organization. SWP disorganization was accompanied by a reduction in the quantity of lymphoid follicles/mm2 (p &gt; 0.0001). 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Disorganization of the splenic white pulp (SWP) has been associated with immunosuppression and disease progression. This study aims to assess structural and cellular changes in the splenic extracellular matrix of dogs with CVL, correlating these changes with the parasite load and clinical signs. Splenic fragments were collected from 41 naturally infected animals for parasite load quantification by quantitative PCR, histopathological analysis and immunohistochemistry for CD3+, CD4+, and CD8+ T cells; CD21+ B cells; Ki-67+, IFN-γ+, and IL-10+ cells; and the MMP-9 and ADAM-10 enzymes. Laminin, collagen and fibronectin deposition were also evaluated. The animals were grouped according to the level of SWP organization. SWP disorganization was accompanied by a reduction in the quantity of lymphoid follicles/mm2 (p &gt; 0.0001). Animals with moderate to intense SWP disorganization showed more clinical signs (p = 0.021), higher laminin (p = 0.045) and collagen deposition (p = 0.036), higher MMP-9 expression (p = 0.035) and lower numbers of CD4+ T cells (p = 0.027) in the spleen than the animals with organized SWP. 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parasitology</subject><subject>Extracellular Matrix - pathology</subject><subject>Fibronectin</subject><subject>Follicles</subject><subject>Funding</subject><subject>Gelatinase B</subject><subject>Genetic aspects</subject><subject>Granulomas</subject><subject>Histopathology</subject><subject>Immunohistochemistry</subject><subject>Immunohistochemistry - veterinary</subject><subject>Immunosuppression</subject><subject>Infections</subject><subject>Interleukin 10</subject><subject>Laminin</subject><subject>Leishmania</subject><subject>Leishmania amazonensis</subject><subject>Leishmania infantum</subject><subject>Leishmania infantum - immunology</subject><subject>Leishmania infantum - physiology</subject><subject>Leishmaniasis</subject><subject>Leishmaniasis, Visceral - immunology</subject><subject>Leishmaniasis, Visceral - parasitology</subject><subject>Leishmaniasis, Visceral - pathology</subject><subject>Leishmaniasis, Visceral - veterinary</subject><subject>Lymphocytes</subject><subject>Lymphocytes - immunology</subject><subject>Lymphocytes - pathology</subject><subject>Lymphocytes B</subject><subject>Lymphocytes T</subject><subject>Medicine and Health Sciences</subject><subject>Niches</subject><subject>Nucleotide sequence</subject><subject>Organizations</subject><subject>Organs</subject><subject>Parasite Load - veterinary</subject><subject>Parasites</subject><subject>Parasitic diseases</subject><subject>PCR</subject><subject>Pulp</subject><subject>Spleen</subject><subject>Spleen - immunology</subject><subject>Spleen - parasitology</subject><subject>Spleen - pathology</subject><subject>Structure-function relationships</subject><subject>Tropical diseases</subject><subject>Vector-borne diseases</subject><subject>Visceral leishmaniasis</subject><subject>White pulp</subject><subject>γ-Interferon</subject><issn>1935-2735</issn><issn>1935-2727</issn><issn>1935-2735</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>DOA</sourceid><recordid>eNptU11v0zAUjRCIjcE_QGAJCSGhFjuJk_gFaSpfk4Z4Gc_WrT8aV45dbAfWn8i_wmm7qUWTH2LdnHvO8f0oipcEz0nVkg9rPwYHdr5xSc4xxk1d00fFOWEVnZVtRR8f3c-KZzGuMaaMduRpcVaypm1J15wXf7_7sOn9pt9G461fGQEWiR7cSkVkHEq9QnFjlTMCqdsUQChrRwsBDZCCuUVeo2tlYj-AM5AzNLg0DjMHaQxg7XYKKZGURNKvMmVEEKMXBqbQH5N6BDapAMl4t1O02yEbMhJlyT6bACd3Lhaf6vfoBk36SAf1a1ROTOw7e8rF58UTDTaqF4fvRfHzy-ebxbfZ9Y-vV4vL65loyjrNJKWkIy0GJklFFWOaMCo6QQnRS4KZoi3DUFO6JK1oMFt2QJYd0RIUK6XW1UXxes-7sT7yQxciL3HF2oaSkmbE1R4hPaz5JpgBwpZ7MHwX8GHFISQjrOJYNoBLUA2p26zZdGSpK02BsbLqWD2pfTyojctBSaFc7oE9IT3940zPV_43p6wiTVdlgncHguBzzWLig4lTEcEpP06-y47Rui1Jhr75D_rw6w6oFeQH5O76aSomUn5Jq6bDrGzqjJo_gMpHqsEI75Q2OX6S8PYooVd5Kvro7bibi1NgvQeK4GMMSt8Xg2A-bcadaz5tBj9sRk57dVzI-6S7Vaj-AQ_SDs4</recordid><startdate>20180420</startdate><enddate>20180420</enddate><creator>da Silva, Aurea Virginia Andrade</creator><creator>Figueiredo, Fabiano Borges</creator><creator>Menezes, Rodrigo Caldas</creator><creator>Mendes-Junior, Arthur Augusto</creator><creator>de Miranda, Luisa Helena Monteiro</creator><creator>Cupolillo, Elisa</creator><creator>Porrozzi, Renato</creator><creator>Morgado, Fernanda Nazaré</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7SS</scope><scope>7T2</scope><scope>7T7</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8C1</scope><scope>8FD</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>F1W</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>K9.</scope><scope>L.G</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-7188-251X</orcidid></search><sort><creationdate>20180420</creationdate><title>Morphophysiological changes in the splenic extracellular matrix of Leishmania infantum-naturally infected dogs is associated with alterations in lymphoid niches and the CD4+ T cell frequency in spleens</title><author>da Silva, Aurea Virginia Andrade ; Figueiredo, Fabiano Borges ; Menezes, Rodrigo Caldas ; Mendes-Junior, Arthur Augusto ; de Miranda, Luisa Helena Monteiro ; Cupolillo, Elisa ; Porrozzi, Renato ; Morgado, Fernanda Nazaré</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c624t-d5518170a9d135e99f195c8c511fb109e5790a455b17c609b8a1b81fdae92dff3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Body organs</topic><topic>CD3 antigen</topic><topic>CD4 antigen</topic><topic>CD4-Positive T-Lymphocytes - immunology</topic><topic>CD4-Positive T-Lymphocytes - pathology</topic><topic>CD8 antigen</topic><topic>Cells</topic><topic>Cellular structure</topic><topic>Chemokines</topic><topic>Collagen</topic><topic>Cytokines</topic><topic>Deposition</topic><topic>Development and progression</topic><topic>Diseases and pests</topic><topic>DNA</topic><topic>Dog Diseases - immunology</topic><topic>Dog Diseases - parasitology</topic><topic>Dog Diseases - pathology</topic><topic>Dogs</topic><topic>Extracellular</topic><topic>Extracellular matrix</topic><topic>Extracellular Matrix - immunology</topic><topic>Extracellular Matrix - parasitology</topic><topic>Extracellular Matrix - pathology</topic><topic>Fibronectin</topic><topic>Follicles</topic><topic>Funding</topic><topic>Gelatinase B</topic><topic>Genetic aspects</topic><topic>Granulomas</topic><topic>Histopathology</topic><topic>Immunohistochemistry</topic><topic>Immunohistochemistry - veterinary</topic><topic>Immunosuppression</topic><topic>Infections</topic><topic>Interleukin 10</topic><topic>Laminin</topic><topic>Leishmania</topic><topic>Leishmania amazonensis</topic><topic>Leishmania infantum</topic><topic>Leishmania infantum - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PLoS neglected tropical diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>da Silva, Aurea Virginia Andrade</au><au>Figueiredo, Fabiano Borges</au><au>Menezes, Rodrigo Caldas</au><au>Mendes-Junior, Arthur Augusto</au><au>de Miranda, Luisa Helena Monteiro</au><au>Cupolillo, Elisa</au><au>Porrozzi, Renato</au><au>Morgado, Fernanda Nazaré</au><au>Descoteaux, Albert</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Morphophysiological changes in the splenic extracellular matrix of Leishmania infantum-naturally infected dogs is associated with alterations in lymphoid niches and the CD4+ T cell frequency in spleens</atitle><jtitle>PLoS neglected tropical diseases</jtitle><addtitle>PLoS Negl Trop Dis</addtitle><date>2018-04-20</date><risdate>2018</risdate><volume>12</volume><issue>4</issue><spage>e0006445</spage><epage>e0006445</epage><pages>e0006445-e0006445</pages><issn>1935-2735</issn><issn>1935-2727</issn><eissn>1935-2735</eissn><abstract>The spleen is one of the main affected organs in canine visceral leishmaniasis (CVL). Disorganization of the splenic white pulp (SWP) has been associated with immunosuppression and disease progression. This study aims to assess structural and cellular changes in the splenic extracellular matrix of dogs with CVL, correlating these changes with the parasite load and clinical signs. Splenic fragments were collected from 41 naturally infected animals for parasite load quantification by quantitative PCR, histopathological analysis and immunohistochemistry for CD3+, CD4+, and CD8+ T cells; CD21+ B cells; Ki-67+, IFN-γ+, and IL-10+ cells; and the MMP-9 and ADAM-10 enzymes. Laminin, collagen and fibronectin deposition were also evaluated. The animals were grouped according to the level of SWP organization. SWP disorganization was accompanied by a reduction in the quantity of lymphoid follicles/mm2 (p &gt; 0.0001). Animals with moderate to intense SWP disorganization showed more clinical signs (p = 0.021), higher laminin (p = 0.045) and collagen deposition (p = 0.036), higher MMP-9 expression (p = 0.035) and lower numbers of CD4+ T cells (p = 0.027) in the spleen than the animals with organized SWP. These data suggest that splenic structure and function are drastically altered and compromised during CVL.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29677186</pmid><doi>10.1371/journal.pntd.0006445</doi><orcidid>https://orcid.org/0000-0002-7188-251X</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1935-2735
ispartof PLoS neglected tropical diseases, 2018-04, Vol.12 (4), p.e0006445-e0006445
issn 1935-2735
1935-2727
1935-2735
language eng
recordid cdi_plos_journals_2039765125
source MEDLINE; Directory of Open Access Journals; PubMed Central Open Access; Public Library of Science website; Free E-Journal (出版社公開部分のみ); PubMed Central
subjects Analysis
Animals
Biology and Life Sciences
Body organs
CD3 antigen
CD4 antigen
CD4-Positive T-Lymphocytes - immunology
CD4-Positive T-Lymphocytes - pathology
CD8 antigen
Cells
Cellular structure
Chemokines
Collagen
Cytokines
Deposition
Development and progression
Diseases and pests
DNA
Dog Diseases - immunology
Dog Diseases - parasitology
Dog Diseases - pathology
Dogs
Extracellular
Extracellular matrix
Extracellular Matrix - immunology
Extracellular Matrix - parasitology
Extracellular Matrix - pathology
Fibronectin
Follicles
Funding
Gelatinase B
Genetic aspects
Granulomas
Histopathology
Immunohistochemistry
Immunohistochemistry - veterinary
Immunosuppression
Infections
Interleukin 10
Laminin
Leishmania
Leishmania amazonensis
Leishmania infantum
Leishmania infantum - immunology
Leishmania infantum - physiology
Leishmaniasis
Leishmaniasis, Visceral - immunology
Leishmaniasis, Visceral - parasitology
Leishmaniasis, Visceral - pathology
Leishmaniasis, Visceral - veterinary
Lymphocytes
Lymphocytes - immunology
Lymphocytes - pathology
Lymphocytes B
Lymphocytes T
Medicine and Health Sciences
Niches
Nucleotide sequence
Organizations
Organs
Parasite Load - veterinary
Parasites
Parasitic diseases
PCR
Pulp
Spleen
Spleen - immunology
Spleen - parasitology
Spleen - pathology
Structure-function relationships
Tropical diseases
Vector-borne diseases
Visceral leishmaniasis
White pulp
γ-Interferon
title Morphophysiological changes in the splenic extracellular matrix of Leishmania infantum-naturally infected dogs is associated with alterations in lymphoid niches and the CD4+ T cell frequency in spleens
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