Type 1 Diabetes Is Associated With Enterovirus Infection in Gut Mucosa
Enterovirus infections have been linked to type 1 diabetes in several studies. Enteroviruses also have tropism to pancreatic islets and can cause β-cell damage in experimental models. Viral persistence has been suspected to be an important pathogenetic factor. This study evaluates whether gut mucosa...
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| Veröffentlicht in: | Diabetes (New York, N.Y.) N.Y.), 2012-03, Vol.61 (3), p.687-691 |
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| creator | OIKARINEN, Maarit TAURIAINEN, Sisko OIKARINEN, Sami HONKANEN, Teemu COLLIN, Pekka RANTALA, Immo MÄKI, Markku KAUKINEN, Katri HYÖTY, Heikki |
| description | Enterovirus infections have been linked to type 1 diabetes in several studies. Enteroviruses also have tropism to pancreatic islets and can cause β-cell damage in experimental models. Viral persistence has been suspected to be an important pathogenetic factor. This study evaluates whether gut mucosa is a reservoir for enterovirus persistence in type 1 diabetic patients. Small-bowel mucosal biopsy samples from 39 type 1 diabetic patients, 41 control subjects, and 40 celiac disease patients were analyzed for the presence of enterovirus using in situ hybridization (ISH), RT-PCR, and immunohistochemistry. The presence of virus was compared with inflammatory markers such as infiltrating T cells, HLA-DR expression, and transglutaminase 2-targeted IgA deposits. Enterovirus RNA was found in diabetic patients more frequently than in control subjects and was associated with a clear inflammation response in the gut mucosa. Viral RNA was often detected in the absence of viral protein, suggesting defective replication of the virus. Patients remained virus positive in follow-up samples taken after 12 months' observation. The results suggest that a large proportion of type 1 diabetic patients have prolonged/persistent enterovirus infection associated with an inflammation process in gut mucosa. This finding opens new opportunities for studying the viral etiology of type 1 diabetes. |
| doi_str_mv | 10.2337/db11-1157 |
| format | Article |
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Enteroviruses also have tropism to pancreatic islets and can cause β-cell damage in experimental models. Viral persistence has been suspected to be an important pathogenetic factor. This study evaluates whether gut mucosa is a reservoir for enterovirus persistence in type 1 diabetic patients. Small-bowel mucosal biopsy samples from 39 type 1 diabetic patients, 41 control subjects, and 40 celiac disease patients were analyzed for the presence of enterovirus using in situ hybridization (ISH), RT-PCR, and immunohistochemistry. The presence of virus was compared with inflammatory markers such as infiltrating T cells, HLA-DR expression, and transglutaminase 2-targeted IgA deposits. Enterovirus RNA was found in diabetic patients more frequently than in control subjects and was associated with a clear inflammation response in the gut mucosa. Viral RNA was often detected in the absence of viral protein, suggesting defective replication of the virus. Patients remained virus positive in follow-up samples taken after 12 months' observation. The results suggest that a large proportion of type 1 diabetic patients have prolonged/persistent enterovirus infection associated with an inflammation process in gut mucosa. This finding opens new opportunities for studying the viral etiology of type 1 diabetes.</description><identifier>ISSN: 0012-1797</identifier><identifier>EISSN: 1939-327X</identifier><identifier>DOI: 10.2337/db11-1157</identifier><identifier>PMID: 22315304</identifier><identifier>CODEN: DIAEAZ</identifier><language>eng</language><publisher>Alexandria, VA: American Diabetes Association</publisher><subject>Adolescent ; Adult ; Aged ; Antibodies ; Biological and medical sciences ; Biopsy ; Celiac disease ; Diabetes ; Diabetes Mellitus, Type 1 - etiology ; Diabetes Mellitus, Type 1 - virology ; Diabetes. Impaired glucose tolerance ; Endocrine pancreas. Apud cells (diseases) ; Endocrinopathies ; Enterovirus ; Enterovirus - isolation & purification ; Enterovirus diseases ; Enterovirus infections ; Enterovirus Infections - complications ; Etiopathogenesis. Screening. Investigations. Target tissue resistance ; Female ; Health aspects ; HLA-DR Antigens - analysis ; Humans ; Hybridization ; Immune system ; In Situ Hybridization ; Infections ; Inflammation ; Inflammatory bowel disease ; Intestinal Mucosa - virology ; Male ; Medical sciences ; Pancreas ; Pathophysiology ; Polymerase Chain Reaction ; Risk factors ; RNA, Viral - analysis ; Type 1 diabetes</subject><ispartof>Diabetes (New York, N.Y.), 2012-03, Vol.61 (3), p.687-691</ispartof><rights>2015 INIST-CNRS</rights><rights>COPYRIGHT 2012 American Diabetes Association</rights><rights>COPYRIGHT 2012 American Diabetes Association</rights><rights>Copyright American Diabetes Association Mar 2012</rights><rights>2012 by the American Diabetes Association. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c640t-2dbb4e81de34b3b0684a2e275a02f1d6774595df1983bbcb8e863f0966dc8fdf3</citedby><cites>FETCH-LOGICAL-c640t-2dbb4e81de34b3b0684a2e275a02f1d6774595df1983bbcb8e863f0966dc8fdf3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3282798/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3282798/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25565295$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22315304$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>OIKARINEN, Maarit</creatorcontrib><creatorcontrib>TAURIAINEN, Sisko</creatorcontrib><creatorcontrib>OIKARINEN, Sami</creatorcontrib><creatorcontrib>HONKANEN, Teemu</creatorcontrib><creatorcontrib>COLLIN, Pekka</creatorcontrib><creatorcontrib>RANTALA, Immo</creatorcontrib><creatorcontrib>MÄKI, Markku</creatorcontrib><creatorcontrib>KAUKINEN, Katri</creatorcontrib><creatorcontrib>HYÖTY, Heikki</creatorcontrib><title>Type 1 Diabetes Is Associated With Enterovirus Infection in Gut Mucosa</title><title>Diabetes (New York, N.Y.)</title><addtitle>Diabetes</addtitle><description>Enterovirus infections have been linked to type 1 diabetes in several studies. Enteroviruses also have tropism to pancreatic islets and can cause β-cell damage in experimental models. Viral persistence has been suspected to be an important pathogenetic factor. This study evaluates whether gut mucosa is a reservoir for enterovirus persistence in type 1 diabetic patients. Small-bowel mucosal biopsy samples from 39 type 1 diabetic patients, 41 control subjects, and 40 celiac disease patients were analyzed for the presence of enterovirus using in situ hybridization (ISH), RT-PCR, and immunohistochemistry. The presence of virus was compared with inflammatory markers such as infiltrating T cells, HLA-DR expression, and transglutaminase 2-targeted IgA deposits. Enterovirus RNA was found in diabetic patients more frequently than in control subjects and was associated with a clear inflammation response in the gut mucosa. Viral RNA was often detected in the absence of viral protein, suggesting defective replication of the virus. Patients remained virus positive in follow-up samples taken after 12 months' observation. The results suggest that a large proportion of type 1 diabetic patients have prolonged/persistent enterovirus infection associated with an inflammation process in gut mucosa. This finding opens new opportunities for studying the viral etiology of type 1 diabetes.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Aged</subject><subject>Antibodies</subject><subject>Biological and medical sciences</subject><subject>Biopsy</subject><subject>Celiac disease</subject><subject>Diabetes</subject><subject>Diabetes Mellitus, Type 1 - etiology</subject><subject>Diabetes Mellitus, Type 1 - virology</subject><subject>Diabetes. Impaired glucose tolerance</subject><subject>Endocrine pancreas. Apud cells (diseases)</subject><subject>Endocrinopathies</subject><subject>Enterovirus</subject><subject>Enterovirus - isolation & purification</subject><subject>Enterovirus diseases</subject><subject>Enterovirus infections</subject><subject>Enterovirus Infections - complications</subject><subject>Etiopathogenesis. Screening. Investigations. Target tissue resistance</subject><subject>Female</subject><subject>Health aspects</subject><subject>HLA-DR Antigens - analysis</subject><subject>Humans</subject><subject>Hybridization</subject><subject>Immune system</subject><subject>In Situ Hybridization</subject><subject>Infections</subject><subject>Inflammation</subject><subject>Inflammatory bowel disease</subject><subject>Intestinal Mucosa - virology</subject><subject>Male</subject><subject>Medical sciences</subject><subject>Pancreas</subject><subject>Pathophysiology</subject><subject>Polymerase Chain Reaction</subject><subject>Risk factors</subject><subject>RNA, Viral - analysis</subject><subject>Type 1 diabetes</subject><issn>0012-1797</issn><issn>1939-327X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqNkl1rFDEUhoModrt64R-QQRHxYmo-Jh9zIyxruxZWelPRu5DJnGxTZpPtZKbYf98sXasri0guAjnPeTk574vQK4JPKGPyY9sQUhLC5RM0ITWrS0blj6dogjGhJZG1PELHKV1jjEU-z9ERpYxwhqsJOru820BBis_eNDBAKs5TMUspWm8GaIvvfrgqTsMAfbz1_ZjLwYEdfAyFD8ViHIqvo43JvEDPnOkSvNzdU_Tt7PRy_qVcXizO57NlaUWFh5K2TVOBIi2wqmENFqoyFKjkBlNHWiFlxWveOlIr1jS2UaAEc7gWorXKtY5N0acH3c3YrKG1EIbedHrT-7Xp73Q0Xu9Xgr_Sq3irGVVUZtUper8T6OPNCGnQa58sdJ0JEMeka16JSuL_IfMOVa0Ez-Sbv8jrOPYh7yFDopa0yqZM0dsHaGU60D64mOezW0k9o4pIVQteZao8QK0gQP5MDOB8ft7jTw7w-bSw9vZgw4e9hswM8HNYmTElrRbLfw2zY23sOliBzsbOLw5q2z6m1IN79IVgvQ2q3gZVb4Oa2dd_GvlI_kpmBt7tAJOs6VxvgvXpN8e54LTm7B7KnusV</recordid><startdate>20120301</startdate><enddate>20120301</enddate><creator>OIKARINEN, Maarit</creator><creator>TAURIAINEN, Sisko</creator><creator>OIKARINEN, Sami</creator><creator>HONKANEN, Teemu</creator><creator>COLLIN, Pekka</creator><creator>RANTALA, Immo</creator><creator>MÄKI, Markku</creator><creator>KAUKINEN, Katri</creator><creator>HYÖTY, Heikki</creator><general>American Diabetes Association</general><scope>IQODW</scope><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>8GL</scope><scope>3V.</scope><scope>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8AF</scope><scope>8AO</scope><scope>8C1</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BEC</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7P</scope><scope>MBDVC</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>S0X</scope><scope>7X8</scope><scope>7U9</scope><scope>H94</scope><scope>5PM</scope></search><sort><creationdate>20120301</creationdate><title>Type 1 Diabetes Is Associated With Enterovirus Infection in Gut Mucosa</title><author>OIKARINEN, Maarit ; TAURIAINEN, Sisko ; OIKARINEN, Sami ; HONKANEN, Teemu ; COLLIN, Pekka ; RANTALA, Immo ; MÄKI, Markku ; KAUKINEN, Katri ; HYÖTY, Heikki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c640t-2dbb4e81de34b3b0684a2e275a02f1d6774595df1983bbcb8e863f0966dc8fdf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Adolescent</topic><topic>Adult</topic><topic>Aged</topic><topic>Antibodies</topic><topic>Biological and medical sciences</topic><topic>Biopsy</topic><topic>Celiac disease</topic><topic>Diabetes</topic><topic>Diabetes Mellitus, Type 1 - etiology</topic><topic>Diabetes Mellitus, Type 1 - virology</topic><topic>Diabetes. Impaired glucose tolerance</topic><topic>Endocrine pancreas. Apud cells (diseases)</topic><topic>Endocrinopathies</topic><topic>Enterovirus</topic><topic>Enterovirus - isolation & purification</topic><topic>Enterovirus diseases</topic><topic>Enterovirus infections</topic><topic>Enterovirus Infections - complications</topic><topic>Etiopathogenesis. Screening. Investigations. Target tissue resistance</topic><topic>Female</topic><topic>Health aspects</topic><topic>HLA-DR Antigens - analysis</topic><topic>Humans</topic><topic>Hybridization</topic><topic>Immune system</topic><topic>In Situ Hybridization</topic><topic>Infections</topic><topic>Inflammation</topic><topic>Inflammatory bowel disease</topic><topic>Intestinal Mucosa - virology</topic><topic>Male</topic><topic>Medical sciences</topic><topic>Pancreas</topic><topic>Pathophysiology</topic><topic>Polymerase Chain Reaction</topic><topic>Risk factors</topic><topic>RNA, Viral - analysis</topic><topic>Type 1 diabetes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>OIKARINEN, Maarit</creatorcontrib><creatorcontrib>TAURIAINEN, Sisko</creatorcontrib><creatorcontrib>OIKARINEN, Sami</creatorcontrib><creatorcontrib>HONKANEN, Teemu</creatorcontrib><creatorcontrib>COLLIN, Pekka</creatorcontrib><creatorcontrib>RANTALA, Immo</creatorcontrib><creatorcontrib>MÄKI, Markku</creatorcontrib><creatorcontrib>KAUKINEN, Katri</creatorcontrib><creatorcontrib>HYÖTY, Heikki</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: High School</collection><collection>ProQuest Central (Corporate)</collection><collection>Nursing & Allied Health Database</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>eLibrary</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>SciTech Premium Collection</collection><collection>Consumer Health Database (Alumni Edition)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>ProQuest Biological Science Collection</collection><collection>Consumer Health Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>SIRS Editorial</collection><collection>MEDLINE - Academic</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Diabetes (New York, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>OIKARINEN, Maarit</au><au>TAURIAINEN, Sisko</au><au>OIKARINEN, Sami</au><au>HONKANEN, Teemu</au><au>COLLIN, Pekka</au><au>RANTALA, Immo</au><au>MÄKI, Markku</au><au>KAUKINEN, Katri</au><au>HYÖTY, Heikki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Type 1 Diabetes Is Associated With Enterovirus Infection in Gut Mucosa</atitle><jtitle>Diabetes (New York, N.Y.)</jtitle><addtitle>Diabetes</addtitle><date>2012-03-01</date><risdate>2012</risdate><volume>61</volume><issue>3</issue><spage>687</spage><epage>691</epage><pages>687-691</pages><issn>0012-1797</issn><eissn>1939-327X</eissn><coden>DIAEAZ</coden><abstract>Enterovirus infections have been linked to type 1 diabetes in several studies. Enteroviruses also have tropism to pancreatic islets and can cause β-cell damage in experimental models. Viral persistence has been suspected to be an important pathogenetic factor. This study evaluates whether gut mucosa is a reservoir for enterovirus persistence in type 1 diabetic patients. Small-bowel mucosal biopsy samples from 39 type 1 diabetic patients, 41 control subjects, and 40 celiac disease patients were analyzed for the presence of enterovirus using in situ hybridization (ISH), RT-PCR, and immunohistochemistry. The presence of virus was compared with inflammatory markers such as infiltrating T cells, HLA-DR expression, and transglutaminase 2-targeted IgA deposits. Enterovirus RNA was found in diabetic patients more frequently than in control subjects and was associated with a clear inflammation response in the gut mucosa. Viral RNA was often detected in the absence of viral protein, suggesting defective replication of the virus. Patients remained virus positive in follow-up samples taken after 12 months' observation. The results suggest that a large proportion of type 1 diabetic patients have prolonged/persistent enterovirus infection associated with an inflammation process in gut mucosa. This finding opens new opportunities for studying the viral etiology of type 1 diabetes.</abstract><cop>Alexandria, VA</cop><pub>American Diabetes Association</pub><pmid>22315304</pmid><doi>10.2337/db11-1157</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Diabetes (New York, N.Y.), 2012-03, Vol.61 (3), p.687-691 |
| issn | 0012-1797 1939-327X |
| language | eng |
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| source | MEDLINE; Journals@Ovid Complete; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Adolescent Adult Aged Antibodies Biological and medical sciences Biopsy Celiac disease Diabetes Diabetes Mellitus, Type 1 - etiology Diabetes Mellitus, Type 1 - virology Diabetes. Impaired glucose tolerance Endocrine pancreas. Apud cells (diseases) Endocrinopathies Enterovirus Enterovirus - isolation & purification Enterovirus diseases Enterovirus infections Enterovirus Infections - complications Etiopathogenesis. Screening. Investigations. Target tissue resistance Female Health aspects HLA-DR Antigens - analysis Humans Hybridization Immune system In Situ Hybridization Infections Inflammation Inflammatory bowel disease Intestinal Mucosa - virology Male Medical sciences Pancreas Pathophysiology Polymerase Chain Reaction Risk factors RNA, Viral - analysis Type 1 diabetes |
| title | Type 1 Diabetes Is Associated With Enterovirus Infection in Gut Mucosa |
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