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Unbalanced recovery of regulatory and effector T cells after allogeneic stem cell transplantation contributes to chronic GVHD
The development and maintenance of immune tolerance after allogeneic hematopoietic stem cell transplantation (HSCT) requires the balanced reconstitution of donor-derived CD4 regulatory T cells (CD4Tregs) as well as effector CD4 (conventional CD4 T cells [CD4Tcons]) and CD8 T cells. To characterize t...
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| Published in: | Blood 2016-02, Vol.127 (5), p.646-657 |
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| creator | Alho, Ana C. Kim, Haesook T. Chammas, Marie J. Reynolds, Carol G. Matos, Tiago R. Forcade, Edouard Whangbo, Jennifer Nikiforow, Sarah Cutler, Corey S. Koreth, John Ho, Vincent T. Armand, Philippe Antin, Joseph H. Alyea, Edwin P. Lacerda, Joao F. Soiffer, Robert J. Ritz, Jerome |
| description | The development and maintenance of immune tolerance after allogeneic hematopoietic stem cell transplantation (HSCT) requires the balanced reconstitution of donor-derived CD4 regulatory T cells (CD4Tregs) as well as effector CD4 (conventional CD4 T cells [CD4Tcons]) and CD8 T cells. To characterize the complex mechanisms that lead to unbalanced recovery of these distinct T-cell populations, we studied 107 adult patients who received T-replete stem cell grafts after reduced-intensity conditioning. Immune reconstitution of CD4Treg, CD4Tcon, and CD8 T cells was monitored for a 2-year period. CD3 T-cell counts gradually recovered to normal levels during this period but CD8 T cells recovered more rapidly than either CD4Tregs or CD4Tcons. Reconstituting CD4Tregs and CD4Tcons were predominantly central memory (CM) and effector memory (EM) cells and CD8 T cells were predominantly terminal EM cells. Thymic generation of naive CD4Tcon and CD8 T cells was maintained but thymic production of CD4Tregs was markedly decreased with little recovery during the 2-year study. T-cell proliferation was skewed in favor of CM and EM CD4Tcon and CD8 T cells, especially 6 to 12 months after HSCT. Intracellular expression of BCL2 was increased in CD4Tcon and CD8 T cells in the first 3 to 6 months after HSCT. Early recovery of naive and CM fractions within each T-cell population 3 months after transplant was also strongly correlated with the subsequent development of chronic graft-versus-host disease (GVHD). These dynamic imbalances favor the production, expansion, and persistence of effector T cells over CD4Tregs and were associated with the development of chronic GVHD.
•Homeostatic recovery after allogeneic HSCT favors the production, expansion, and survival of effector T cells over CD4Tregs.•Unbalanced reconstitution of regulatory and effector T-cell subsets contributes to the development of chronic graft-versus-host disease. |
| doi_str_mv | 10.1182/blood-2015-10-672345 |
| format | article |
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•Homeostatic recovery after allogeneic HSCT favors the production, expansion, and survival of effector T cells over CD4Tregs.•Unbalanced reconstitution of regulatory and effector T-cell subsets contributes to the development of chronic graft-versus-host disease.</description><identifier>ISSN: 0006-4971</identifier><identifier>EISSN: 1528-0020</identifier><identifier>DOI: 10.1182/blood-2015-10-672345</identifier><identifier>PMID: 26670634</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adult ; Aged ; CD4-Positive T-Lymphocytes - immunology ; CD4-Positive T-Lymphocytes - pathology ; CD8-Positive T-Lymphocytes - immunology ; CD8-Positive T-Lymphocytes - pathology ; Chronic Disease ; Female ; Graft vs Host Disease - etiology ; Graft vs Host Disease - immunology ; Graft vs Host Disease - pathology ; Hematopoietic Stem Cell Transplantation - adverse effects ; Humans ; Male ; Middle Aged ; T-Lymphocytes, Regulatory - immunology ; T-Lymphocytes, Regulatory - pathology ; Transplantation ; Transplantation, Homologous - adverse effects ; Young Adult</subject><ispartof>Blood, 2016-02, Vol.127 (5), p.646-657</ispartof><rights>2016 American Society of Hematology</rights><rights>2016 by The American Society of Hematology.</rights><rights>2016 by The American Society of Hematology 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c463t-9b9bac450fd120f09fc1b4120be900d7cb220bb22390ea639558776afee2fbf63</citedby><cites>FETCH-LOGICAL-c463t-9b9bac450fd120f09fc1b4120be900d7cb220bb22390ea639558776afee2fbf63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0006497120305012$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,315,786,790,891,3568,27957,27958,45815</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26670634$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Alho, Ana C.</creatorcontrib><creatorcontrib>Kim, Haesook T.</creatorcontrib><creatorcontrib>Chammas, Marie J.</creatorcontrib><creatorcontrib>Reynolds, Carol G.</creatorcontrib><creatorcontrib>Matos, Tiago R.</creatorcontrib><creatorcontrib>Forcade, Edouard</creatorcontrib><creatorcontrib>Whangbo, Jennifer</creatorcontrib><creatorcontrib>Nikiforow, Sarah</creatorcontrib><creatorcontrib>Cutler, Corey S.</creatorcontrib><creatorcontrib>Koreth, John</creatorcontrib><creatorcontrib>Ho, Vincent T.</creatorcontrib><creatorcontrib>Armand, Philippe</creatorcontrib><creatorcontrib>Antin, Joseph H.</creatorcontrib><creatorcontrib>Alyea, Edwin P.</creatorcontrib><creatorcontrib>Lacerda, Joao F.</creatorcontrib><creatorcontrib>Soiffer, Robert J.</creatorcontrib><creatorcontrib>Ritz, Jerome</creatorcontrib><title>Unbalanced recovery of regulatory and effector T cells after allogeneic stem cell transplantation contributes to chronic GVHD</title><title>Blood</title><addtitle>Blood</addtitle><description>The development and maintenance of immune tolerance after allogeneic hematopoietic stem cell transplantation (HSCT) requires the balanced reconstitution of donor-derived CD4 regulatory T cells (CD4Tregs) as well as effector CD4 (conventional CD4 T cells [CD4Tcons]) and CD8 T cells. To characterize the complex mechanisms that lead to unbalanced recovery of these distinct T-cell populations, we studied 107 adult patients who received T-replete stem cell grafts after reduced-intensity conditioning. Immune reconstitution of CD4Treg, CD4Tcon, and CD8 T cells was monitored for a 2-year period. CD3 T-cell counts gradually recovered to normal levels during this period but CD8 T cells recovered more rapidly than either CD4Tregs or CD4Tcons. Reconstituting CD4Tregs and CD4Tcons were predominantly central memory (CM) and effector memory (EM) cells and CD8 T cells were predominantly terminal EM cells. Thymic generation of naive CD4Tcon and CD8 T cells was maintained but thymic production of CD4Tregs was markedly decreased with little recovery during the 2-year study. T-cell proliferation was skewed in favor of CM and EM CD4Tcon and CD8 T cells, especially 6 to 12 months after HSCT. Intracellular expression of BCL2 was increased in CD4Tcon and CD8 T cells in the first 3 to 6 months after HSCT. Early recovery of naive and CM fractions within each T-cell population 3 months after transplant was also strongly correlated with the subsequent development of chronic graft-versus-host disease (GVHD). These dynamic imbalances favor the production, expansion, and persistence of effector T cells over CD4Tregs and were associated with the development of chronic GVHD.
•Homeostatic recovery after allogeneic HSCT favors the production, expansion, and survival of effector T cells over CD4Tregs.•Unbalanced reconstitution of regulatory and effector T-cell subsets contributes to the development of chronic graft-versus-host disease.</description><subject>Adult</subject><subject>Aged</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>CD4-Positive T-Lymphocytes - pathology</subject><subject>CD8-Positive T-Lymphocytes - immunology</subject><subject>CD8-Positive T-Lymphocytes - pathology</subject><subject>Chronic Disease</subject><subject>Female</subject><subject>Graft vs Host Disease - etiology</subject><subject>Graft vs Host Disease - immunology</subject><subject>Graft vs Host Disease - pathology</subject><subject>Hematopoietic Stem Cell Transplantation - adverse effects</subject><subject>Humans</subject><subject>Male</subject><subject>Middle Aged</subject><subject>T-Lymphocytes, Regulatory - immunology</subject><subject>T-Lymphocytes, Regulatory - pathology</subject><subject>Transplantation</subject><subject>Transplantation, Homologous - adverse effects</subject><subject>Young Adult</subject><issn>0006-4971</issn><issn>1528-0020</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNp9kUFvVCEQx4nR2LX6DYzh6OXpwAPevouJabU1aeKl9UqAN2wxb2EFdpMe_O7yurXqxQvMMDP_meFHyGsG7xhb8_d2TmnqODDZMejUwHshn5AVk3zdAXB4SlYAoDoxDuyEvCjlOwATPZfPyQlXagDVixX5eROtmU10ONGMLh0w39Hkm73Zz6am5pk4UfQeXfPoNXU4z4UaXzFTM89pgxGDo6Xi9j5Gazax7JpmNTWkSF2KNQe7r1hoTdTd5hRbwcW3y_OX5Jk3c8FXD_cpufn86frssrv6evHl7ONV54Tqazfa0RonJPiJcfAwesesaKbFEWAanOXNbkc_AhrVj1Kuh0EZj8i99ao_JR-Ouru93eLksE1kZr3LYWvynU4m6H8jMdzqTTpoMQguJW8Cbx8Ecvqxx1L1NpRlWxMx7Ytmg-KjHPt-aKnimOpyKiWjf2zDQC_k9D05vZBbno7kWtmbv0d8LPqN6s8O2D7qEDDr4gIu4EIDV_WUwv87_ALIt65R</recordid><startdate>20160204</startdate><enddate>20160204</enddate><creator>Alho, Ana C.</creator><creator>Kim, Haesook T.</creator><creator>Chammas, Marie J.</creator><creator>Reynolds, Carol G.</creator><creator>Matos, Tiago R.</creator><creator>Forcade, Edouard</creator><creator>Whangbo, Jennifer</creator><creator>Nikiforow, Sarah</creator><creator>Cutler, Corey S.</creator><creator>Koreth, John</creator><creator>Ho, Vincent T.</creator><creator>Armand, Philippe</creator><creator>Antin, Joseph H.</creator><creator>Alyea, Edwin P.</creator><creator>Lacerda, Joao F.</creator><creator>Soiffer, Robert J.</creator><creator>Ritz, Jerome</creator><general>Elsevier Inc</general><general>American Society of Hematology</general><scope>6I.</scope><scope>AAFTH</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20160204</creationdate><title>Unbalanced recovery of regulatory and effector T cells after allogeneic stem cell transplantation contributes to chronic GVHD</title><author>Alho, Ana C. ; Kim, Haesook T. ; Chammas, Marie J. ; Reynolds, Carol G. ; Matos, Tiago R. ; Forcade, Edouard ; Whangbo, Jennifer ; Nikiforow, Sarah ; Cutler, Corey S. ; Koreth, John ; Ho, Vincent T. ; Armand, Philippe ; Antin, Joseph H. ; Alyea, Edwin P. ; Lacerda, Joao F. ; Soiffer, Robert J. ; Ritz, Jerome</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-9b9bac450fd120f09fc1b4120be900d7cb220bb22390ea639558776afee2fbf63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adult</topic><topic>Aged</topic><topic>CD4-Positive T-Lymphocytes - immunology</topic><topic>CD4-Positive T-Lymphocytes - pathology</topic><topic>CD8-Positive T-Lymphocytes - immunology</topic><topic>CD8-Positive T-Lymphocytes - pathology</topic><topic>Chronic Disease</topic><topic>Female</topic><topic>Graft vs Host Disease - etiology</topic><topic>Graft vs Host Disease - immunology</topic><topic>Graft vs Host Disease - pathology</topic><topic>Hematopoietic Stem Cell Transplantation - adverse effects</topic><topic>Humans</topic><topic>Male</topic><topic>Middle Aged</topic><topic>T-Lymphocytes, Regulatory - immunology</topic><topic>T-Lymphocytes, Regulatory - pathology</topic><topic>Transplantation</topic><topic>Transplantation, Homologous - adverse effects</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Alho, Ana C.</creatorcontrib><creatorcontrib>Kim, Haesook T.</creatorcontrib><creatorcontrib>Chammas, Marie J.</creatorcontrib><creatorcontrib>Reynolds, Carol G.</creatorcontrib><creatorcontrib>Matos, Tiago R.</creatorcontrib><creatorcontrib>Forcade, Edouard</creatorcontrib><creatorcontrib>Whangbo, Jennifer</creatorcontrib><creatorcontrib>Nikiforow, Sarah</creatorcontrib><creatorcontrib>Cutler, Corey S.</creatorcontrib><creatorcontrib>Koreth, John</creatorcontrib><creatorcontrib>Ho, Vincent T.</creatorcontrib><creatorcontrib>Armand, Philippe</creatorcontrib><creatorcontrib>Antin, Joseph H.</creatorcontrib><creatorcontrib>Alyea, Edwin P.</creatorcontrib><creatorcontrib>Lacerda, Joao F.</creatorcontrib><creatorcontrib>Soiffer, Robert J.</creatorcontrib><creatorcontrib>Ritz, Jerome</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Blood</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Alho, Ana C.</au><au>Kim, Haesook T.</au><au>Chammas, Marie J.</au><au>Reynolds, Carol G.</au><au>Matos, Tiago R.</au><au>Forcade, Edouard</au><au>Whangbo, Jennifer</au><au>Nikiforow, Sarah</au><au>Cutler, Corey S.</au><au>Koreth, John</au><au>Ho, Vincent T.</au><au>Armand, Philippe</au><au>Antin, Joseph H.</au><au>Alyea, Edwin P.</au><au>Lacerda, Joao F.</au><au>Soiffer, Robert J.</au><au>Ritz, Jerome</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Unbalanced recovery of regulatory and effector T cells after allogeneic stem cell transplantation contributes to chronic GVHD</atitle><jtitle>Blood</jtitle><addtitle>Blood</addtitle><date>2016-02-04</date><risdate>2016</risdate><volume>127</volume><issue>5</issue><spage>646</spage><epage>657</epage><pages>646-657</pages><issn>0006-4971</issn><eissn>1528-0020</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>The development and maintenance of immune tolerance after allogeneic hematopoietic stem cell transplantation (HSCT) requires the balanced reconstitution of donor-derived CD4 regulatory T cells (CD4Tregs) as well as effector CD4 (conventional CD4 T cells [CD4Tcons]) and CD8 T cells. To characterize the complex mechanisms that lead to unbalanced recovery of these distinct T-cell populations, we studied 107 adult patients who received T-replete stem cell grafts after reduced-intensity conditioning. Immune reconstitution of CD4Treg, CD4Tcon, and CD8 T cells was monitored for a 2-year period. CD3 T-cell counts gradually recovered to normal levels during this period but CD8 T cells recovered more rapidly than either CD4Tregs or CD4Tcons. Reconstituting CD4Tregs and CD4Tcons were predominantly central memory (CM) and effector memory (EM) cells and CD8 T cells were predominantly terminal EM cells. Thymic generation of naive CD4Tcon and CD8 T cells was maintained but thymic production of CD4Tregs was markedly decreased with little recovery during the 2-year study. T-cell proliferation was skewed in favor of CM and EM CD4Tcon and CD8 T cells, especially 6 to 12 months after HSCT. Intracellular expression of BCL2 was increased in CD4Tcon and CD8 T cells in the first 3 to 6 months after HSCT. Early recovery of naive and CM fractions within each T-cell population 3 months after transplant was also strongly correlated with the subsequent development of chronic graft-versus-host disease (GVHD). These dynamic imbalances favor the production, expansion, and persistence of effector T cells over CD4Tregs and were associated with the development of chronic GVHD.
•Homeostatic recovery after allogeneic HSCT favors the production, expansion, and survival of effector T cells over CD4Tregs.•Unbalanced reconstitution of regulatory and effector T-cell subsets contributes to the development of chronic graft-versus-host disease.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>26670634</pmid><doi>10.1182/blood-2015-10-672345</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Adult Aged CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - pathology CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - pathology Chronic Disease Female Graft vs Host Disease - etiology Graft vs Host Disease - immunology Graft vs Host Disease - pathology Hematopoietic Stem Cell Transplantation - adverse effects Humans Male Middle Aged T-Lymphocytes, Regulatory - immunology T-Lymphocytes, Regulatory - pathology Transplantation Transplantation, Homologous - adverse effects Young Adult |
| title | Unbalanced recovery of regulatory and effector T cells after allogeneic stem cell transplantation contributes to chronic GVHD |
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