Real-time tracking of cell cycle progression during CD8+ effector and memory T-cell differentiation

Ichiko Kinjyo, Jim Qin, Sioh-Yang Tan, Cameron J. Wellard, Paulus Mrass, William Ritchie, Atsushi Doi, Lois L. Cavanagh, Michio Tomura, Asako Sakaue-Sawano, Osami Kanagawa, Atsushi Miyawaki, Philip D. Hodgkin and Wolfgang Weninger ()
Additional contact information
Ichiko Kinjyo: Immune Imaging Program, Centenary Institute for Cancer Medicine and Cell Biology
Jim Qin: Immune Imaging Program, Centenary Institute for Cancer Medicine and Cell Biology
Sioh-Yang Tan: Immune Imaging Program, Centenary Institute for Cancer Medicine and Cell Biology
Cameron J. Wellard: Walter and Eliza Hall Institute of Medical Research
Paulus Mrass: Immune Imaging Program, Centenary Institute for Cancer Medicine and Cell Biology
William Ritchie: Immune Imaging Program, Centenary Institute for Cancer Medicine and Cell Biology
Atsushi Doi: Cell Innovator Co., Ltd.
Lois L. Cavanagh: Immune Imaging Program, Centenary Institute for Cancer Medicine and Cell Biology
Michio Tomura: Laboratory for Autoimmune Regulation, RIKEN Research Center for Allergy and Immunology
Asako Sakaue-Sawano: Laboratory for Cell Function and Dynamics, Brain Science Institute, RIKEN
Osami Kanagawa: Laboratory for Autoimmune Regulation, RIKEN Research Center for Allergy and Immunology
Atsushi Miyawaki: Laboratory for Cell Function and Dynamics, Brain Science Institute, RIKEN
Philip D. Hodgkin: Walter and Eliza Hall Institute of Medical Research
Wolfgang Weninger: Immune Imaging Program, Centenary Institute for Cancer Medicine and Cell Biology

Nature Communications, 2015, vol. 6, issue 1, 1-13

Abstract: Abstract The precise pathways of memory T-cell differentiation are incompletely understood. Here we exploit transgenic mice expressing fluorescent cell cycle indicators to longitudinally track the division dynamics of individual CD8+ T cells. During influenza virus infection in vivo, naive T cells enter a CD62Lintermediate state of fast proliferation, which continues for at least nine generations. At the peak of the anti-viral immune response, a subpopulation of these cells markedly reduces their cycling speed and acquires a CD62Lhi central memory cell phenotype. Construction of T-cell family division trees in vitro reveals two patterns of proliferation dynamics. While cells initially divide rapidly with moderate stochastic variations of cycling times after each generation, a slow-cycling subpopulation displaying a CD62Lhi memory phenotype appears after eight divisions. Phenotype and cell cycle duration are inherited by the progeny of slow cyclers. We propose that memory precursors cell-intrinsically modulate their proliferative activity to diversify differentiation pathways.

Date: 2015
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DOI: 10.1038/ncomms7301

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