Differential Cytokine Utilization and Tissue Tropism Results in Distinct Repopulation Kinetics of Naïve vs. Memory T Cells in Mice
Naïve and memory T cells co-exist in the peripheral T cell pool, but the cellular mechanisms that maintain the balance and homeostasis of these two populations remain mostly unclear. To address this question, here, we assessed homeostatic proliferation and repopulation kinetics of adoptively transfe...
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Published in | Frontiers in immunology Vol. 10; p. 355 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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04.03.2019
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Abstract | Naïve and memory T cells co-exist in the peripheral T cell pool, but the cellular mechanisms that maintain the balance and homeostasis of these two populations remain mostly unclear. To address this question, here, we assessed homeostatic proliferation and repopulation kinetics of adoptively transferred naïve and memory T cells in lymphopenic host mice. We identified distinct kinetics of proliferation and tissue-distribution between naïve and memory donor T cells, which resulted in the occupancy of the peripheral T cell pool by mostly naïve-origin T cells in short term (<1 week), but, in a dramatic reversal, by mostly memory-origin T cells in long term (>4 weeks). To explain this finding, we assessed utilization of the homeostatic cytokines IL-7 and IL-15 by naïve and memory T cells. We found different efficiencies of IL-7 signaling between naïve and memory T cells, where memory T cells expressed larger amounts of IL-7Rα but were significantly less potent in activation of STAT5 that is downstream of IL-7 signaling. Nonetheless, memory T cells were superior in long-term repopulation of the peripheral T cell pool, presumably, because they preferentially migrated into non-lymphoid tissues upon adoptive transfer and additionally utilized tissue IL-15 for rapid expansion. Consequently, co-utilization of IL-7 and IL-15 provides memory T cells a long-term survival advantage. We consider this mechanism important, as it permits the memory T cell population to be maintained in face of constant influx of naïve T cells to the peripheral T cell pool and under competing conditions for survival cytokines. |
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AbstractList | Naïve and memory T cells co-exist in the peripheral T cell pool, but the cellular mechanisms that maintain the balance and homeostasis of these two populations remain mostly unclear. To address this question, here, we assessed homeostatic proliferation and repopulation kinetics of adoptively transferred naïve and memory T cells in lymphopenic host mice. We identified distinct kinetics of proliferation and tissue-distribution between naïve and memory donor T cells, which resulted in the occupancy of the peripheral T cell pool by mostly naïve-origin T cells in short term (<1 week), but, in a dramatic reversal, by mostly memory-origin T cells in long term (>4 weeks). To explain this finding, we assessed utilization of the homeostatic cytokines IL-7 and IL-15 by naïve and memory T cells. We found different efficiencies of IL-7 signaling between naïve and memory T cells, where memory T cells expressed larger amounts of IL-7Rα but were significantly less potent in activation of STAT5 that is downstream of IL-7 signaling. Nonetheless, memory T cells were superior in long-term repopulation of the peripheral T cell pool, presumably, because they preferentially migrated into non-lymphoid tissues upon adoptive transfer and additionally utilized tissue IL-15 for rapid expansion. Consequently, co-utilization of IL-7 and IL-15 provides memory T cells a long-term survival advantage. We consider this mechanism important, as it permits the memory T cell population to be maintained in face of constant influx of naïve T cells to the peripheral T cell pool and under competing conditions for survival cytokines. |
Author | Hawk, Nga V Hwang, SuJin Gress, Ronald E Kwon, Juntae Johns, Christopher Park, Jung-Hyun Chung, Hyunsoo Kim, Hye Kyung Castro, Ehydel |
AuthorAffiliation | 2 Experimental Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health , Bethesda, MD , United States 1 Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health , Bethesda, MD , United States |
AuthorAffiliation_xml | – name: 1 Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health , Bethesda, MD , United States – name: 2 Experimental Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health , Bethesda, MD , United States |
Author_xml | – sequence: 1 givenname: Hye Kyung surname: Kim fullname: Kim, Hye Kyung organization: Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States – sequence: 2 givenname: Hyunsoo surname: Chung fullname: Chung, Hyunsoo organization: Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States – sequence: 3 givenname: Juntae surname: Kwon fullname: Kwon, Juntae organization: Experimental Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States – sequence: 4 givenname: Ehydel surname: Castro fullname: Castro, Ehydel organization: Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States – sequence: 5 givenname: Christopher surname: Johns fullname: Johns, Christopher organization: Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States – sequence: 6 givenname: Nga V surname: Hawk fullname: Hawk, Nga V organization: Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States – sequence: 7 givenname: SuJin surname: Hwang fullname: Hwang, SuJin organization: Experimental Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States – sequence: 8 givenname: Jung-Hyun surname: Park fullname: Park, Jung-Hyun organization: Experimental Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States – sequence: 9 givenname: Ronald E surname: Gress fullname: Gress, Ronald E organization: Experimental Transplantation and Immunology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, United States |
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Copyright | Copyright © 2019 Kim, Chung, Kwon, Castro, Johns, Hawk, Hwang, Park and Gress. 2019 Kim, Chung, Kwon, Castro, Johns, Hawk, Hwang, Park and Gress |
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Keywords | migration apoptosis cytokines proliferation lymphopenia |
Language | English |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors share senior authorship Edited by: Raghvendra Mohan Srivastava, Memorial Sloan Kettering Cancer Center, United States Reviewed by: Sid P. Kerkar, Boehringer Ingelheim, United States; Fernando Concha-Benavente, University of Pittsburgh, United States This article was submitted to T Cell Biology, a section of the journal Frontiers in Immunology |
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References | Cho (B51) 2010 B24 Guimond (B31) 2009 Moutuou (B23) 2018 Wu (B59) 2013 Mackall (B4) 2011 Parretta (B55) 2005 Berard (B39) 2003 Kieper (B26) 2005 Park (B45) 2018 Jiang (B8) 2005 Baaten (B28) 2010 Schaerli (B54) 2005 Park (B15) 2004 den Braber (B5) 2012 Park (B69) 2018 Wells (B33) 1997 Peschon (B11) 1994 Kim (B13) 2011 Becker (B56) 2005 Park (B68) 2007 Hinrichs (B61) 2009 Fry (B14) 2001 Kaech (B20) 2003 Tan (B36) 2001 Gordy (B40) 2011 Mackall (B65) 2000 Rosen (B47) 2004 Surh (B32) 2000 Sportes (B66) 2008 Gamper (B37) 2012 Kim (B7) 2016 Nolz (B53) 2015 Seddon (B27) 2002 Waickman (B16) 2016 Barber (B35) 2006 Giri (B50) 1994 Liao (B62) 2015 Osborne (B49) 2010 Carrette (B2) 2012 Wherry (B34) 2015 Rochman (B17) 2009 Mazzucchelli (B18) 2007 Gebhardt (B46) 2012 Tan (B67) 2002 Huster (B19) 2004 Diaz-Montero (B63) 2013 Ilangumaran (B41) 2003 Opferman (B9) 2003 Jacobs (B10) 2010 Ku (B44) 2000 Yu (B29) 1999 Boyman (B48) 2009 Klebanoff (B22) 2012 Waldmann (B43) 1998 Geiselhart (B30) 2001 Busch (B58) 2016 Klonowski (B21) 2005 Nolz (B52) 2011 Gossel (B6) 2017 Bradley (B1) 2005 Chu (B3) 2004 von (B12) 1995 Nicholson (B38) 1995 Appelbaum (B57) 2001 Crompton (B60) 2014 Bosco (B25) 2005 Hakim (B64) 1997 Ilangumaran (B42) 2003 |
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SubjectTerms | Adoptive Transfer - methods Animals apoptosis Cell Survival - immunology cytokines Cytokines - immunology Homeostasis - immunology Immunologic Memory - immunology Immunology Interleukin-15 - immunology Kinetics Lymphocyte Activation - immunology lymphopenia Lymphopenia - immunology Mice Mice, Inbred C57BL migration proliferation Receptors, Interleukin-7 - immunology Signal Transduction - immunology STAT5 Transcription Factor - immunology |
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Title | Differential Cytokine Utilization and Tissue Tropism Results in Distinct Repopulation Kinetics of Naïve vs. Memory T Cells in Mice |
URI | https://www.ncbi.nlm.nih.gov/pubmed/30886618 https://search.proquest.com/docview/2194143041 https://pubmed.ncbi.nlm.nih.gov/PMC6409349 https://doaj.org/article/cb45940f914b4b66b4e278b7b32af00d |
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