Cited by 623Autophagy in Disease and TherapyT-cell and B-cell ImmunologyPhagocytosis and Immune Regulation

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A critical role for the autophagy gene Atg5 in T cell survival and proliferation

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Pua, Heather H., Dzhagalov, Ivan, Chuck, Mariana, Mizushima, Noboru, He, You-Wen·2007·The Journal of Experimental Medicine

DOI 10.1084/jem.20061303PMC PMC2118420

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Abstract

Macroautophagy (hereafter referred to as autophagy) is a well-conserved intracellular degradation process. Recent studies examining cells lacking the autophagy genes Atg5 and Atg7 have demonstrated that autophagy plays essential roles in cell survival during starvation, in innate cell clearance of microbial pathogens, and in neural cell maintenance. However, the role of autophagy in T lymphocyte development and survival is not known. Here, we demonstrate that autophagosomes form in primary mouse T lymphocytes. By generating Atg5−/− chimeric mice, we found that Atg5-deficient T lymphocytes underwent full maturation. However, the numbers of total thymocytes and peripheral T and B lymphocytes were reduced in Atg5 chimeras. In the periphery, Atg5−/− CD8+ T lymphocytes displayed dramatically increased cell death. Furthermore, Atg5−/− CD4+ and CD8+ T cells failed to undergo efficient proliferation after TCR stimulation. These results demonstrate a critical role for Atg5 in multiple aspects of lymphocyte development and function and suggest that autophagy may be essential for both T lymphocyte survival and proliferation.

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Figure 1. Atg5−/− thymocytes are reduced in number but develop normally. (A) Rag-2−/− DN thymocytes, sorted DP, CD4+ SP, CD8+ SP, and peripheral T cell subsets from C57BL/6 mice were analyzed for the expression of autophagy genes by semiquantitative RT-PCR. Both sorted CD4+ and CD8+ peripheral T cells were activated in vitro for 2 d with anti-CD3 and subjected to RT-PCR analysis. (B) Transmission electron microscopy of peripheral T cells. Freshly isolated (F) and anti-CD3–activated (A) CD4+ and CD8+ T cells (n = 50) were cross sectioned and analyzed for the presence of autophagosomes (arrows). Activated cells were cultured in vitro for 2 d with anti-CD3. (C) T cell immunoblot for LC3. Purified T cells from C57BL/6 mice were either immediately lysed or amino acid starved in vitro for 4 h in a balanced salt solution, or stimulated with plate-bound anti-CD3 with or without hIL-2 (100 U/ml) for 16 h. The lysates were probed for LC3 processing. Actin serves as a loading control. (D) Total thymocyte number in Atg5−/− and wild-type chimeras. Circles and squares represent individual mice. P = 0.04. (E) FACS profile of Atg5−/− thymocytes. Total thymocytes were stained with anti-CD4 and anti-CD8. DN thymocytes were pregated on CD3−CD4−CD8− cells. (F) FACS analysis of thymocyte apoptosis. Thymocytes were stained with CD4, CD8, 7-AAD, and annexin V. Numbers indicate the percentage of cells in each region.CC BY-NC-SA · PubMed Central

Figure 2. Defective peripheral lymphocyte compartment in Atg5−/− chimeras. (A) FACS profiles of donor-derived CD4+ and CD8+ T cells in the spleens of Atg5−/− and wild-type chimeric mice 6–10 wk after reconstitution. All cells are pregated on CD45.2+ donor-derived cells. (B) The numbers of T cells, B cells, and neutrophils in the spleen of Atg5−/− and wild-type chimeras. The numbers are derived from multiplying the percentage of CD4+ and CD8+ T cells, B220+, or Gr-1+CD11b+ CD45.2+ cells by the total numbers of splenocytes. p values for comparison between Atg5−/− and wild-type chimeras are: T cells, P = 0.0267; B cells, P = 0.0001; PMN, P = 0.8785. (C) The numbers of CD4+ and CD8+ T lymphocytes in the spleen of Atg5−/− and wild-type chimeras. CD4+ T cells, P = 0.0678; CD8+ T cells, P = 0.002. (D) The CD4+ to CD8+ T cell ratio in Atg5−/− and wild-type chimeras. Shown are data from individual mice. P = 0.0163. All p values are derived from unpaired, two-tailed Student's t test.CC BY-NC-SA · PubMed Central

Figure 3. Selective survival defect in Atg5−/− CD8+ T cells. (A) FACS analysis of CD8+ T cell apoptosis. Donor-derived CD8+ T cells in Atg5−/− and wild-type chimeras were stained with 7-AAD and PE–annexin V. Numbers indicate the percentage of cells in each region. (B). Apoptotic rates of various cell populations in Atg5−/− and wild-type chimeras. Donor-derived cells (CD45.2+) were stained using the indicated lineage markers plus PE–annexin V and analyzed by FACS. CD8+ T cells, P = 0.0118; CD4+, P = 0.0544; B220+, P = 0.0826; Gr1+ cells, P = 0.6605. n = 3. (C) Apoptotic rates of donor-derived and host long-term surviving CD4+ and CD8+ T cells. p values for donor versus host T cells in Atg5−/− chimeras: CD4+ T cells, P = 0.72; CD8+ T cells, P = 0.004.CC BY-NC-SA · PubMed Central

Figure 4. Impaired proliferation of Atg5−/− T cells upon anti-CD3 stimulation. (A) Proliferation of Atg5−/− and wild-type CD4+ T cells upon TCR stimulation. Splenocytes from control and Atg5−/− chimeras were labeled with CFSE and stimulated under the following conditions for 3 d: 5 μg/ml of plate-bound anti-CD3, or plus 1 μg/ml plate-bound anti-CD28, or plus 100 U/ml of recombinant IL-2, or 10 ng/ml PMA plus 300 ng/ml of ionomycin. Shown are the percentage of cells with diluted CFSE staining and the mean fluorescence intensity of the proliferating population. (B) Up-regulation of CD25 and CD69 on Atg5−/− and wild-type T cells after overnight stimulation with plate-bound anti-CD3. (C) Apoptosis rates of Atg5−/− and wild-type T cells after TCR stimulation. Total splenocytes were cultured either in media alone or with 5 μg/ml of plate bound anti-CD3 for the indicated times. Apoptosis was measured by annexin V staining. Data are representative of two experiments.CC BY-NC-SA · PubMed Central

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The “Intermediate” CD14 + CD16 + monocyte subpopulation plays a role in IVIG responsiveness of children with Kawasaki disease
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Autophagy, a Novel Pathway to Regulate Calcium Mobilization in T Lymphocytes
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“Many Atgs, such as Atg5, Beclin 1 and LC3, are expressed in thymocytes, most highly during double negative (DN) thymocyte development, but also expressed in mature CD4+ and CD8+ T cell sub-populations.”
BackgroundMethodInfluentialSelf-citation
Autophagy-dependent danger signaling and adaptive immunity to poorly immunogenic tumors
Kroemer, G., & Galluzzi, L. (2016) · Oncotarget · doi:10.18632/oncotarget.13892 · Cited by 15
“Similarly, the spontaneous CD3+CD4+ and CD3+CD8+ T-cell infiltrates isolated from autophagyproficient versus -deficient B16 and 4T1 tumors growing in immunocompetent syngeneic mice did not differ with respect to an panel of activation/exhaustion markers encompassing CD44, interferon gamma (IFNG), tumor necrosis factor…”
Background
ATG5-Dependent Autophagy Uncouples T-cell Proliferative and Effector Functions and Separates Graft-versus-Host Disease from Graft-versus-Leukemia
Oravecz-Wilson, K. I., Rossi, C., Zajac, C. K., Sun, Y., Li, L., Decoville, T., Fujiwara, H., Kim, S. H., Peltier, D., & Reddy, P. R. (2020) · Cancer Research · doi:10.1158/0008-5472.can-20-1346 · Cited by 13
“Furthermore, consistent with previous reports (13, 20), no differences were observed in expression levels of CD69 upon activation (Supplementary Fig.”
MethodResult
A Spontaneous H2-Aa Point Mutation Impairs MHC II Synthesis and CD4+ T-Cell Development in Mice
Zhao, Y. F., Xiong, J., Chen, H., Zhang, M., Zhou, L., Wu, Y., Li, W.-J., Fei, X., Li, F., Zhu, C., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.810824 · Cited by 13
“Although autophagy was shown to play an essential role in T-cell proliferation, survival, and activation (11), knockout of autophagy-related protein ATG5 displayed no influence on T-cell development in the thymus (12).”
Background
Redox status regulates autophagy in thymic stromal cells and promotes T cell tolerance
Semwal, M. K., Hester, A. K., Xiao, Y., Udeaja, C., Cepeda, S., Verschelde, J., Jones, N., Wedemeyer, S. A., Emtage, S., Wimberly, K., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204296119 · Cited by 13
“Since stimulation of T cells is known to induce autophagy (28), we first evaluated whether we could measure increased autophagosome formation using a cytometric approach in GFP-LC3 Tg mice.”
Method
Autophagy and T-cell education in the thymus: Eat yourself to know yourself
Nedjic, J., Aichinger, M., & Klein, L. (2008) · Cell Cycle · doi:10.4161/cc.7.23.7121 · Cited by 18
Autophagy of pathogens alarms the immune system and participates in its effector functions
Romão, S., & Münz, C. (2011) · Swiss Medical Weekly · doi:10.4414/smw.2011.13198 · Cited by 14
Autophagy: Shedding Light on the Mechanisms and Multifaceted Roles in Cancers
You, H., Wang, L., Meng, H., Li, J., & Fang, G.-Y. (2025) · Biomolecules · doi:10.3390/biom15070915 · Cited by 14
Endoplasmic reticulum stress in T cell‐mediated diseases
Chen, S., Wang, Q., Wang, H., & Xia, S. (2023) · Scandinavian Journal of Immunology · doi:10.1111/sji.13307 · Cited by 13
Autophagy-enhancing ATG16L1 polymorphism is associated with improved clinical outcome and T-cell immunity in chronic HIV-1 infection
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“Autophagy is an example of autophagy’s dual nature because of the critical function ATG5 (Pua et al. 2007).”
Influential
Autophagy-related IFNG is a prognostic and immunochemotherapeutic biomarker of COAD patients
Yue, T., Cai, Y., Zhu, J., Liu, Y., Chen, S., Wang, P., & Rong, L. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1064704 · Cited by 12
“Besides, autophagy participated in innate immunity, inflammatory response (3) and adaptive immune response by processing antigens (4) and regulating the development and function of lymphocytes (5).”
Background
The effect of gamma keratose on cell viability in vitro after thermal stress and the regulation of cell death pathway-specific gene expression
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Macroautophagy during Innate Immune Activation
Münz, C. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00072 · Cited by 13
“…both innate and adaptive immunity (Münz, 2009) and macroautophagy clearly assists T cell development and T cell mediated immune responses in vivo (Pua et al., 2007; Nedjic et al., 2008; Lee et al., 2010), the contributions of innate and adaptive pathogen restriction mechanisms via macroautophagy…”
Background
Histone Methylation Keeps the Brakes on Autophagy
Collins, P. L., & Oltz, E. M. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01033-13 · Cited by 12
“Indeed, mice rendered incapable of inducing autophagy in this lineage exhibit impaired T cell proliferation and survival (12).”
Background
Increased Thymic Cell Turnover under Boron Stress May Bypass TLR3/4 Pathway in African Ostrich
Huang, H., Xiao, K., Lu, S., Yang, K., Ansari, A. R., Khaliq, H., Song, H., Zhong, J., Liu, H., & Peng, K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129596 · Cited by 12
“Recent studies also showed that autophagy played a critical role for T cell development [4], thus we evaluated the expression of LC3A/B, the classic index for autophagy [3], in ostrich thymus.”
Background
T cell intrinsic roles of autophagy in promoting adaptive immunity
Walsh, C. M., & Bell, B. D. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.03.005 · Cited by 12
Hypoxia and Serum deprivation protected MiaPaCa-2 cells from KAI1-induced proliferation inhibition through autophagy pathway activation in solid tumors
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Role of canonical and noncanonical autophagy pathways in shaping the life journey of B cells
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Sphingosine-1-phosphate alleviates Sjögren’s syndrome-like symptoms via inducing autophagy and regulating status of Treg cells in NOD mice
Jin, Y., Wang, Y., Feng, M., Ni, X., Qiang, L., Xue, J., Sun, L., Gao, C., & Luo, J. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.113514 · Cited by 11
The regulation of microglia by aging and autophagy in multiple sclerosis
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The role of autophagy in initiation, progression, TME modification, diagnosis, and treatment of esophageal cancers
Zhou, S., Sun, X., Jin, Z., Yang, H., & Ye, W. (2022) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2022.103702 · Cited by 11
Autophagy Regulation of Mammalian Immune Cells
He, W., Xiong, W., & Xia, X. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-0606-2_2 · Cited by 11
Autophagy and senescence: Insights from normal and cancer stem cells
Talukdar, S., Das, S. K., Emdad, L., & Fisher, P. B. (2021) · Advances in cancer research · doi:10.1016/bs.acr.2021.01.005 · Cited by 12
CD8+ T cell survival in lethal fungal sepsis was ameliorated by T-cell-specific mTOR deletion
Wang, H., Han, W., Guo, R., Bai, G., Chen, J., & Cui, N. (2021) · International Journal of Medical Sciences · doi:10.7150/ijms.55592 · Cited by 9
“The mTOR signaling pathway is closely related to T-cell death-survival balancing in infection or stress [11-12].”
Background
Radiotherapy modulates autophagy to reshape the tumor immune microenvironment to enhance anti-tumor immunity in esophageal cancer
Zhou, S., & Yang, H. (2025) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2025.189302 · Cited by 9
Perspectives of Targeting Autophagy as an Adjuvant to Anti-PD-1/PD-L1 Therapy for Colorectal Cancer Treatment
ALKhemeiri, N., Eljack, S., & Saber-Ayad, M. M. (2025) · Cells · doi:10.3390/cells14100745 · Cited by 9
“Collectively, these studies elucidated that ablation of the core autophagy proteins resulted in a significant reduction in thymocytes and peripheral T-cells (lymphocyte survival) [119,120].”
L’autophagie et l’homéostasie des lymphocytes T et B - Bien recycler pour un développement durable
Arnold, J., Murera, D., Arbogast, F., Muller, S., & Gros, F. (2016) · médecine/sciences · doi:10.1051/medsci/20163203013 · Cited by 6
“La première étude s’intéressant au rôle de l’autophagie dans les lymphocytes a été publiée par Heather Pua [10], à partir de modèles murins de délétion du gène Atg5.”
BackgroundInfluential
Overexpression of ATG5 Gene Makes Granulocyte-Like HL-60 Susceptible to Release Reactive Oxygen Species
Mroczek, A., Cieloch, A., Manda‐Handzlik, A., Kuźmicka, W., Muchowicz, A., & Wachowska, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155194 · Cited by 9
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Background
Autophagic flux restoration enhances the antitumor efficacy of tumor infiltrating lymphocytes
Zhang, C., Sun, Y., Li, S., Shen, L., Teng, X., Xiao, Y., Wu, N., & Lu, Z. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-004868 · Cited by 9
Autophagy modulation in cancer
Guilbaud, E., Ryan, K. M., Green, D. R., & Galluzzi, L. (2026) · Nature Reviews Drug Discovery · doi:10.1038/s41573-026-01449-9 · Cited by 11
“Similarly, ATG5 is fundamental for T cell survival and proliferation 273,274 , as well as for the establishment of immunological memory upon antigenic challenges 274 .”
Redox balance of mouse medullary CD4 single‐positive thymocytes
Jin, R., Teng, F., Xu, X., Yao, Y., Zhang, S., Sun, X., Zhang, Y., & Ge, Q. (2013) · Immunology and Cell Biology · doi:10.1038/icb.2013.57 · Cited by 8
Toxoplasma gondii profilin and tachyzoites RH strain may manipulate autophagy via downregulating Atg5 and Atg12 and upregulating Atg7
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Crosstalk between autophagy and metabolic regulation of (CAR) T cells: therapeutic implications
Meymandi, A. R. P., Akbari, B., Soltantoyeh, T., Hadjati, J., Klionsky, D. J., Badie, B., & Mirzaei, H. R. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1212695 · Cited by 9
“Autophagy has been shown to enhance T cell survival by preventing cell death (19, 23).”
BackgroundInfluential
Mechanisms and regulation of autophagy in mammalian cells
Mehrpour, M., Botti, J., & Codogno, P. (2012) · Atlas of Genetics and Cytogenetics in Oncology and Haematology · doi:10.4267/2042/46951 · Cited by 8
Targeting Autophagy Facilitates T Lymphocyte Migration by Inducing the Expression of CXCL10 in Gastric Cancer Cell Lines
Meng, Q., Zhang, Y., & Hu, L. G. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00886 · Cited by 8
CD8+ T cell metabolic changes in breast cancer
Castoldi, Â., Lee, J., Carvalho, D. D. S., & Souto, F. O. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2022.166565 · Cited by 9
Autophagy
Hsu, C. (2019) · The Chinese Journal of Physiology · doi:10.4103/cjp.cjp_25_19 · Cited by 8
“The progression of sepsis into immunosuppression also can be explained by the role of autophagy in maintaining survival and proliferation of T-lymphocytes.[65] A recent study further finds that restoring impaired autophagic flux by genipin and sinomenine protects against septic liver injury.”
Background
Molecular Mechanisms Underpinning Immunometabolic Reprogramming: How the Wind Changes during Cancer Progression
Flati, I., Nolfi, M. D. V., Dall’Aglio, F., Vecchiotti, D., Verzella, D., Alesse, E., Capece, D., & Zazzeroni, F. (2023) · Genes · doi:10.3390/genes14101953 · Cited by 7
Molecular and temporal control of restimulation-induced cell death (RICD) in T lymphocytes
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“TCR-induced selective autophagy and macroautophagy have been shown to help to regulate NF-κ B activation and enable clonal expansion, respectively, in part by promoting T cell survival (Pua et al., 2007; Paul et al., 2012).”
Research progress of T cell autophagy in autoimmune diseases
Zhao, X., Ma, D., Yang, B., Wang, Y., & Zhang, L. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1425443 · Cited by 8
Deciphering the dual role of autophagy in gastric cancer and gastroesophageal junction cancer: from tumor suppression to cancer progression
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The role of autophagy protein Atg5 in multiple sclerosis
Baeva, M.-E., & Camara-Lemarroy, C. R. (2023) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2023.105029 · Cited by 7
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CD30 plays a role in T‐dependent immune response and T cell proliferation
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Background

Authors: Pua, H. H., Dzhagalov, I., Chuck, M., Mizushima, N., & He, Y.-W.
Affiliations: Duke Medical Center (US)
Japan Science and Technology Agency (JP)
ORCID: Pua, Heather H.
Dzhagalov, Ivan
Mizushima, Noboru
He, You-Wen
Venue: The Journal of Experimental Medicine
Publisher: Rockefeller University Press
Published: 2006-12-26
Volume: 204
Issue: 1
Pages: 25-31
ISSN: 0022-1007 (ISSN-L)
1540-9538
DOI: 10.1084/jem.20061303
PMC: PMC2118420
OpenAlex: W2154663531
Cited by: 622
References: 29
Citations by year: 2026: 10 · 2025: 23 · 2024: 17 · 2023: 23 · 2022: 25 · 2021: 31 · 2020: 34 · 2019: 35 · 2018: 34 · 2017: 39 · 2016: 45 · 2015: 35 · 2014: 34 · 2013: 42 · 2012: 55
FWCI: 19.36
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: The Journal of Experimental Medicine (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Cancer Institute (R01CA092123, CA92123)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK040561)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Keywords: autophagy, ATG5, ATG7, T cell proliferation, T cell development, autophagosomes, CD8+ T cells, CD4+ T cells, T cell receptor stimulation, lymphocyte apoptosis, chimeric mice
MeSH terms: Autophagy-Related Protein 5, Animals, Autophagy, Base Sequence, Cell Differentiation, Cell Survival, Female, Mice, Inbred C57BL, Microtubule-Associated Proteins, Pregnancy, Receptors, Antigen, T-Cell, T-Lymphocytes, Fetal Tissue Transplantation, DNA Primers, Transplantation Chimera, Mice, Knockout, Hematopoietic Stem Cell Transplantation, CD8-Positive T-Lymphocytes, Cell Proliferation, Mice

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A critical role for the autophagy gene Atg5 in T cell survival and proliferation

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