T Cell Lineage Determination Precedes the Initiation of TCR β Gene Rearrangement
Open accessAbstract
Loss of dendritic cell potential is one of the major events in intrathymic T cell development, during which the progenitors become determined to the T cell lineage. However, it remains unclear whether this event occurs in synchrony with another important event, TCRβ chain gene rearrangement, which has been considered the definitive sign of irreversible T cell lineage commitment. To address this issue, we used transgenic mice in which GFP expression is controlled by the lck proximal promoter. We found that the double-negative (DN) 2 stage can be subdivided into GFP− and GFP+ populations, representing functionally different developmental stages in that the GFP−DN2, but not GFP+DN2, cells retain dendritic cell potential. The GFP+DN2 cells were found to undergo several rounds of proliferation before the initiation of TCRβ rearrangement as evidenced by the diversity of D-Jβ rearrangements seen in T cells derived from a single GFP+DN2 progenitor. These results indicated that the determination step of progenitors to the T cell lineage is a separable event from TCRβ rearrangement.
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In mouse, natural loss of access to dendritic cell and granulocyte programs agrees with the timing of PU.1 downregulation.
“there is good agreement between the cells' natural loss of access to the dendritic cell and granulocyte programs, on the one hand, and the timing of PU.1 downregulation, on the other hand (33, 39–42).”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [39]
The section on PU.1 downregulation reports that PU.1 becomes undetectable at the GFP-positive DN2 stage, when dendritic-cell potential is completely lost; the Discussion also describes the events as coincident (page numbers unavailable). The paper does not establish the timing of a loss of granulocyte potential, so that part of the claim is unsupported by this source. (LLM, conf=0.88)
Experimental — accuracy not yet measuredPopulation dynamic models imply that the stages when PU.1 is expressed occupy a minimum of 7-10 intrathymic cell divisions of pro-T cells.
“Population dynamic models imply that the stages when PU.1 is expressed occupy a minimum of 7–10 intrathymic cell divisions of pro-T cells (39, 66, 67).”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [39]
The PU.1 expression section reports expression through GFP-negative DN2 and loss at GFP-positive DN2. The Discussion reports more than 10 DN1–DN2 divisions, while the proliferation results estimate about four divisions after the transition; together these imply more than six divisions before PU.1 becomes undetectable. The paper does not establish the full stated 7–10-division range for PU.1-expressing stages. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThese stages span multiple cell cycles in vivo and in vitro.
“These stages span multiple cell cycles in vivo and in vitro (33, 39, 67, 124).”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [39]
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Otsuka, R., Wada, H., Sasaki, A., Tsuji, H., Murata, T., Hasegawa, Y., Kaitani, A., Kitaura, J., & Seino, K. (2026) · Transplantation · doi:10.1097/tp.0000000000005795 · Cited by 1 · see citing works
Developmental stages and pathways of NK cell maturation
Grzywacz, B. J., Miller, J. S., & Verneris, M. R. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-370454-2.00001-6 · Cited by 1 · see citing works
Understanding immune system development: An epigenetic perspective
Madhok, A., deSouza, A., & Galande, S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-817964-2.00003-4 · Cited by 1 · see citing works
Molecular Pathogenesis of T Lymphoblastic Lymphomas in an Atm-deficient Mouse Model
Wong, P. P. C. (2013) · TSpace (University of Toronto)
Transcriptional Regulation of T Cell Lineage Commitment
Rothenberg, E. V. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-374279-7.04006-6
Generation and Regeneration of T Cells
Kawamoto, H., Ikawa, T., Maeda, T., & Masuda, K. (2016) · Springer eBooks · doi:10.1007/978-4-431-56027-2_2
Self-citationREGULATION OF EARLY T-CELL DEVELOPMENT AND COMMITMENT BY HEB
Braunstein, M. (2011) · TSpace (University of Toronto)
The Heart of the Machine: Construction of T Cell Identity, Made Accessible
Rothenberg, E. V. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2200264
Transcriptional Regulation of T-Cell Lineage Commitment
Rothenberg, E. V. (2024) · Elsevier eBooks · doi:10.1016/b978-0-128-24465-4.00018-1
Control of Migration During Intrathymic T Cell Development
Tipan, P. G., & Ehrlich, L. I. R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-128-24465-4.00030-2
Étude de la migration thymique : vers une reconstitution optimale du compartiment T
Lopez, V. M. (2017) · theses.fr (ABES) · doi:10.70675/8b7063c6z09bcz4785zba10z0ea2d20623a7
- Authors
- Masuda, K., Kakugawa, K., Nakayama, T., Minato, N., Katsura, Y., & Kawamoto, H.
- Affiliations
- Kyoto University (JP)
- RIKEN (JP)
- Chiba University (JP)
- Nihon University (JP)
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-09
- Volume
- 179
- Issue
- 6
- Pages
- 3699-3706
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W1538274751
- Cited by
- 77
- References
- 33
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 4 · 2018: 3 · 2017: 4 · 2016: 7 · 2015: 3 · 2014: 5 · 2013: 6 · 2012: 4
- FWCI
- 2.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Keywords
- TCR beta gene rearrangement, double-negative thymocytes, GFP reporter mice, thymocyte proliferation, transgenic mice
- MeSH terms
- Proto-Oncogene Protein Spi-1, Animals, Cell Differentiation, Cell Division, Cells, Cultured, Dendritic Cells, Mice, Inbred C57BL, Mice, Transgenic, Organ Culture Techniques, Proto-Oncogene Proteins, Stem Cells, Thymus Gland, Gene Rearrangement, beta-Chain T-Cell Antigen Receptor, Trans-Activators, Down-Regulation, T-Lymphocyte Subsets, Receptors, Antigen, T-Cell, alpha-beta, Cell Lineage, Green Fluorescent Proteins, Mice
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