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Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells
Abstract
A major unanswered question is what distinguishes the majority of activated CD8 T cells that die after an acute viral infection from the small fraction (5-10%) that survive to become long-lived memory cells. In this study we show that increased expression of the interleukin 7 receptor alpha-chain (IL-7Ralpha) identifies the effector CD8 T cells that will differentiate into memory cells. IL-7R(hi) effector cells contained increased amounts of antiapoptotic molecules, and adoptive transfer of IL-7R(hi) and IL-7R(lo) effector cells showed that IL-7R(hi) cells preferentially gave rise to memory cells that could persist and confer protective immunity. Thus, selective expression of IL-7R identifies memory cell precursors, and this marker may be useful in predicting the number of memory T cells generated after infection or immunization.
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“Ag-specific CD8 T cells derived from the effector phase of a response can express various combinations of CD127 and KLRG1, which define either more short-lived effector cells (SLECs; CD127−KLRG1+), which are lost during the contraction phase of the immune response, or memory precursor effector cells (MPECs; CD127+KLRG1−), which are more likely to persist and contribute to memory populations [224,”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [224]
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DNA Methylation and Immune Memory Response
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“associated with T cell engraftment after in vivo adoptive transfer experiments, and therefore is a marker for T cell fitness and persistence (27).”
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“In the linear model of Tmem development, transitioning CD8 Teff can elect one of two fates delineated by the distinct expression of the killer-lectin–like receptor G-1 (KLRG-1) and the IL-7 Ra-chain (CD127), which denote KLRG-1CD127 short-lived effector cells (SLECs) and KLRG1CD127 memory precursor effector cells (MPE…”
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“cells (33, 34) also implicated in the arrest of proliferation, and”
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“TSLE cells can be identified by high expression of the lectinlike receptor, KLRG1, and low expression of IL-7R (KLRG1IL7R), whereas TMP cells can be identified by reciprocally high expression of IL-7R and low expression of KLRG1 (KLRG1IL7R) (38).”
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“Expression of the IL-7R α-chain (CD127) on CD8+ T cells during the acute phase of the response is also essential, although not sufficient on its own, for identifying the memory precursors at the acute time of infection (Kaech et al., 2003; Huster et al., 2004; Hand et al., 2007; Croom et al., 2011).”
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E2A-regulated epigenetic landscape promotes memory CD8 T cell differentiation
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Divergent metabolic programmes control two populations of MAIT cells that protect the lung
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Regulation of T cell-dendritic cell interactions by IL-7 governs T-cell activation and homeostasis
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IL-7 as a potential therapy for HIV-1-infected individuals
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“These cells are the precursors of the memory CD8+ T cell pool that confers protective immunity, and their survival was shown to depend on IL-7 [48].”
BackgroundCellerai, C., Harari, A., Vallelian, F., Boyman, O., & Pantaleo, G. (2007) · European Journal of Immunology · doi:10.1002/eji.200636885 · Cited by 41
Histone Methyltransferase and Histone Methylation in Inflammatory T-Cell Responses
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“Cytokine receptor expression has previously been used to identify the precursors of memory T cells: Following an acute systemic viral infection, the transition from CD8+ effector cells into a long-lived memory cell has been associated with differential expression of the IL-7 receptor (29), and a similar argument has r…”
MethodAllie, S. R., Zhang, W., Tsai, C.-Y., Noelle, R. J., & Usherwood, E. J. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1201945 · Cited by 40
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Common gamma chain cytokines and CD8 T cells in cancer
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Depletion of T Cells by Type I Interferon: Differences between Young and Aged Mice
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“Assessed by intracellular staining with anti-active caspase-3 Ab as described (26), the intracellular expression of active caspase-3 in CD8 T cells was significantly increased 24 h after poly(I:C) in young mice, while only minimal up-regulation of active caspase-3 was observed in aged mice (Fig.”
The contribution of epigenetic memory to immunologic memory
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Self-citationRecombinant IL-7 enhances the potency of GM-CSF-secreting tumor cell immunotherapy
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Origin of CD8+ effector and memory T cell subsets.
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“, 2000) and the interleukin-7 receptor a chain CD127 (Kaech et al., 2003).”
BackgroundLentiviral vector induces high-quality memory T cells via dendritic cells transduction
Ku, M., Authié, P., Névo, F., Souque, P., Bourgine, M., Romano, M., Charneau, P., & Majlessi, L. (2021) · Communications Biology · doi:10.1038/s42003-021-02251-6 · Cited by 38
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Protective immunity towards intracellular pathogens
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“MPCs proliferate less than TECs but go on to survive and undergo homeostatic proliferation alter the infection is eliminated (6, 7).”
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Ly49E separates liver ILC1s into embryo-derived and postnatal subsets with different functions
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“focussed on antigen-specific CD8+ effector cells during acute viral infection, where precursors for memory T cells are enriched in the IL7Ra chain+ (CD127+) subset [37], while CD127-cells are short-term effector cells after the initial expansion [38].”
BackgroundExpression and function of interleukin-7 in secondary and tertiary lymphoid organs
Huang, H.-Y., & Luther, S. A. (2012) · Seminars in Immunology · doi:10.1016/j.smim.2012.02.008 · Cited by 39
IL-6 Receptor α Defines Effector Memory CD8+ T Cells Producing Th2 Cytokines and Expanding in Asthma
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“Thus, following Ag clearance and re-expression of the IL-7Rα receptor on some of the effector CD8 T cells ([61,62] and Hammerbeck and Mescher, manuscript submitted), the low levels of IL-7 present in vivo may stimulate slow proliferation of the effectors and reversal of AINR over one to two weeks.”
BackgroundThe regulatory T cells in anti-influenza antibody response post influenza vaccination
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“Similar observations were made with regard to level of memory CD8 T cells that remained in wt mice with other infections (54, 57).”
BackgroundResultEvery Breath You Take: The Impact of Environment on Resident Memory CD8 T Cells in the Lung
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“Teffs largely fall into one of three categories: terminally differentiated short-lived effector cells (SLECs, KLRG1hi/CD127lo), early effector cells (EECs, KLRG1lo/CD127lo) or memory precursor effector cells (MPECs, KLRG1lo, CD127hi).”
BackgroundInfluentialRegulation of effector and memory CD8+ T cell function by inflammatory cytokines
Valbon, S. F., Condotta, S. A., & Richer, M. J. (2015) · Cytokine · doi:10.1016/j.cyto.2015.11.013 · Cited by 36
Identification of Nascent Memory CD8 T Cells and Modeling of Their Ontogeny.
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“Indeed, transfer experiments can only assess the pres- ence of precursors within a given population without quantification (Hand et al., 2007; Kaech et al., 2003; Kedzierska et al., 2007).”
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“This enables segregation of effector CD8 T cells into short-lived effector cells (SLECs [KLRG1 CD127 ]) and memory precursor effector cells (MPECs [KLRG1 CD127 ]) (33, 39, 40).”
BackgroundBromodomain protein BRD4 directs and sustains CD8 T cell differentiation during infection
Milner, J. J., Toma, C., Quon, S., Omilusik, K. D., Scharping, N. E., Dey, A., Reina‐Campos, M., Nguyen, H., Getzler, A. J., Diao, H., et al. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20202512 · Cited by 38
“Differential expression levels of KLRG1 and CD127 delineate effector populations with distinct fates during acute infections (Chang et al., 2014; Joshi et al., 2007; Kaech et al., 2003).”
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“In mice, compared with cells with low levels of IL-7Ra expression, effector CD8 T cells with high levels of IL-7Ra expression survived better and became memory CD8 T cells during microbial infections (10, 11).”
BackgroundMemory Generation and Maintenance of CD8+ T Cell Function during Viral Persistence
Cush, S. S., Anderson, K. M., Ravneberg, D. H., Weslow-Schmidt, J. L., & Flaño, E. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.1.141 · Cited by 37
“Selective expression of IL-7R identifies CD8 T cells that generate memory cells (78, 79).”
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“One of these markers is the -chain of the IL-7 receptor (CD127), which is downregulated by effector T cells but is expressed by naive and memory cells (26, 34, 35).”
BackgroundThe Privacy of T Cell Memory to Viruses
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Influenza Virus-Specific Immunological Memory Is Enhanced by Repeated Social Defeat
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“It is a candidate phenotypic marker for memory CD8 T cells (40, 41).”
InfluentialSepsis-induced changes in differentiation, maintenance, and function of memory CD8 T cell subsets
Heidarian, M., Griffith, T. S., & Badovinac, V. P. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1130009 · Cited by 41
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“However, TET2 KO P14 cells did not acquire surface characteristics of classical T EFF and T MEM that arise during acute resolving infections ( 28 , 29 ).”
Self-citationTransfer of CD8+ T Cell Memory Using Bcl-2 as a Marker
Dunkle, A. D., Dzhagalov, I. L., Gordy, C. L., & He, Y.-W. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103481 · Cited by 37
“sistent with the evidence that IL-7 is important for memory cell survival (2, 3).”
BackgroundD’Cruz, L. M., Lind, K. C., Wu, B. B., Fujimoto, J., & Goldrath, A. W. (2012) · European Journal of Immunology · doi:10.1002/eji.201242497 · Cited by 37
Uhrlaub, J. L., Brien, J. D., Widman, D. G., Mason, P. W., & Nikolich‐Žugich, J. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002799 · Cited by 37
“1E), a phenotype that corresponds to fully mature effector CD8 T cells (31, 32).”
BackgroundNew insights into IL-7 signaling pathways during early and late T cell development
Niu, N., & Qin, X. (2013) · Cellular and Molecular Immunology · doi:10.1038/cmi.2013.11 · Cited by 37
T Cell Memory in the Context of Persistent Herpes Viral Infections
Torti, N., & Oxenius, A. (2012) · Viruses · doi:10.3390/v4071116 · Cited by 38
“This finding confirmed a superiority of memory precursor cells to survive and undergo homeostatic proliferation, but also highlighted a not-so-short-lived behavior of effector cells, as about 40 days after transfer a considerable number of remaining transferred cells was still present [19].”
BackgroundAdenovirus vector and mRNA vaccines: Mechanisms regulating their immunogenicity
Provine, N. M., & Klenerman, P. (2022) · European Journal of Immunology · doi:10.1002/eji.202250022 · Cited by 37
PI3Kδ Regulates the Magnitude of CD8+ T Cell Responses after Challenge with Listeria monocytogenes
Pearce, V. Q., Bouabe, H., MacQueen, A. R., Carbonaro, V., & Okkenhaug, K. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1501227 · Cited by 36
“These data indicate that p110dD910A cells produce near normal numbers of Tmem, but that the p110dD910A Tmem, similar to their naive precursors, produce an effector T cell (Teff) response of reduced magnitude upon acute challenge with Lm-OVA. p110dD910A mice generate normal numbers of memory precursor effector cells in…”
BackgroundInfluentialBhadra, R., Guan, H., & Khan, I. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010842 · Cited by 37
“To determine if lower Bcl-2 levels observed in the activated phenotype (CD44) CD8 T cells from anti IL-7 treated KO mice (Figure 2) is due to reduced frequency of antigen-specific cells in these animals, BrdU labeled cells were assayed for Bcl-2 and CD127, hallmarks of effector cells destined to be long-lived memory c…”
BackgroundNolz, J. C., Rai, D., Badovinac, V. P., & Harty, J. T. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118868109 · Cited by 36
Xu, X., Sun, Q., Mei, Y., Liu, Y., & Zhao, L. (2017) · Cancer Science · doi:10.1111/cas.13468 · Cited by 36
“IL7 contributes to survival of na€ıve and memory CD8 T cells.(24) IL15 induces proliferation of na€ıve and memory CD8 T cells, and contributes to the maintenance of long-lasting memory CD8 T cells.”
BackgroundMukherjee, S., Sengupta, R., Mukhopadhyay, D., Braun, C., Mitra, S., Roy, S., Das, N. K., Chatterjee, U., von Stebut, E., & Chatterjee, M. (2019) · Scientific Reports · doi:10.1038/s41598-018-37144-y · Cited by 36
The Potential of Tissue-Resident Memory T Cells for Adoptive Immunotherapy against Cancer
Beumer‐Chuwonpad, A., Taggenbrock, R. L. R. E., Ngo, T. A., & van Gisbergen, K. P. J. M. (2021) · Cells · doi:10.3390/cells10092234 · Cited by 40
T cell responses to control fungal infection in an immunological memory lens
Sharma, J., Mudalagiriyappa, S., & Nanjappa, S. G. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.905867 · Cited by 39
Lin, Y., Jones-Mason, M. E., Inoue, M., Lasorella, A., Iavarone, A., Li, Q.-J., Shinohara, M. L., & Zhuang, Y. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200491 · Cited by 34
“Altered expression of both antiapoptotic and proapoptotic genes, such as Bcl-2 and Bim, has been observed in Id2-deficient CD8 T cells (7).”
InfluentialSaito, H., Okita, K., Chang, A. E., & Ito, F. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-1742 · Cited by 38
Generating long‐lived CD8+ T‐cell memory: Insights from epigenetic programs
Dogra, P., Ghoneim, H. E., Abdelsamed, H. A., & Youngblood, B. (2016) · European Journal of Immunology · doi:10.1002/eji.201545550 · Cited by 38
CD4+ t-cell depletion in hiv infection: Killed by friendly fire?
Moanna, A., Dunham, R. M., Paiardini, M., & Silvestri, G. (2005) · Current HIV/AIDS Reports · doi:10.1007/s11904-996-0004-3 · Cited by 36
Sleep enhances serum interleukin-7 concentrations in humans
Benedict, C., Dimitrov, S., Marshall, L., & Born, J. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.04.004 · Cited by 40
“The IL-7 signal and the ability to express IL-7Ra are essential during the contraction phase after the acute immune response, in which more than 95% of antigen-specific effector T cells become eliminated due to apoptosis, and for the development of CD8+ effector T cells to CD8+ memory T cells (Kaech et al., 2003).”
BackgroundContracting the ‘mus cells’– does down‐sizing suit us for diving into the memory pool?
Kurtuluş, S., Tripathi, P., Opferman, J. T., & Hildeman, D. A. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00920.x · Cited by 35
“During viral infection, it was first found that effector CD8 T cells having increased expression of CD127 were enriched as the response contracted (79).”
BackgroundHernandez, M. G. H., Shen, L., & Rock, K. L. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.7.4382 · Cited by 35
Heterogeneity within T Cell Memory: Implications for Transplant Tolerance
Krummey, S. M., & Ford, M. L. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00036 · Cited by 36
“Memory precursor cells upregulate CD127 and remain KLRG-1 low, although several studies have shown that CD127 is permissive but not instructive or even required for memory cell formation (Lacombe et al., 2005; Wojciechowski et al., 2006; Hand et al., 2007).”
BackgroundInfluentialShi, M., Hao, S., Chan, T., & Xiang, J. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0506321 · Cited by 36
“After priming, 5% to 10% of the effector CD8 T cells give rise to long-lived CD8 Tm cells [1].”
BackgroundWells, A. C., Hioki, K. A., Angelou, C. C., Lynch, A. C., Liang, X., Ryan, D. J., Thesmar, I., Zhanybekova, S., Žuklys, S., Ullom, J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40959-7 · Cited by 35
The Expansion and Maintenance of Antigen‐Selected CD8+ T Cell Clones
Fearon, D. T. (2007) · Advances in immunology · doi:10.1016/s0065-2776(07)96003-4 · Cited by 35
“…with a TCM phenotype survive better than do those with TEM and TEFF phenotypes, perhaps because they maintain expression of CD127, the IL-7Ra chain (Kaech et al., 2003; Schluns et al., 2000), and the gradual increase in the TCM/TEM ratio during the memory phase could also have been caused by the…”
Immunization with SARS-CoV S DNA vaccine generates memory CD4+ and CD8+ T cell immune responses
Huang, J., Ma, R., & Wu, C. Y. (2006) · Vaccine · doi:10.1016/j.vaccine.2006.03.058 · Cited by 35
“CD4 + and CD8 + T cells from lymph nodes, spleens and lungs were divided into IL-7R␣ (CD127) + and CD62L + subpopulations which have been shown in mice to distinguish naïve and memory T cells [13, 14] .”
BackgroundIL-7-dependent STAT-5 activation and CD8+ T cell proliferation are impaired in HIV infection
Vranjkovic, A., Crawley, A. M., Patey, A. M., & Angel, J. B. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.0710430 · Cited by 35
“[15] demonstrated the dependence of memory CD8 T cell genesis on IL-7 and that CD127 expression distinguishes effector cells (mostly CD127), which successfully develop from activated CD127 naı̈ve cells into mem-”
BackgroundKarwot, R., Maxeiner, J., Schmitt, S., Scholtes, P., Hausding, M., Lehr, H. A., Glimcher, L. H., & Finotto, S. (2008) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2007.12.1172 · Cited by 35
Albuquerque, A. S., Cortesão, C. S., Foxall, R. B., Soares, R. S., Victorino, R. M. M., & Sousa, A. E. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.5.3252 · Cited by 36
“tiated effector T cells have been shown to be IL-7R , a phenotype associated with decreased survival and proliferation in response to IL-7 (21, 22).”
BackgroundFunctional heterogeneity of human skin‐resident memory T cells in health and disease
Strobl, J., & Haniffa, M. A. (2023) · Immunological Reviews · doi:10.1111/imr.13213 · Cited by 34
Gerlach, C., van Heijst, J. V., & Schumacher, T. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05830.x · Cited by 41
Functional Heterogeneity in the CD4+ T Cell Response to Murine γ-Herpesvirus 68
Hu, Z., Blackman, M. A., Kaye, K. M., & Usherwood, E. J. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1401928 · Cited by 35
“CD127 (IL-7Ra) is a marker to identify memory cell precursors (42).”
Background
Metadata
- Authors
- Kaech, S. M., Tan, J. T., Wherry, E. J., Konieczny, B. T., Surh, C. D., & Ahmed, R.
- Affiliations
- Emory University (US)
- Scripps Research Institute (US)
- Corresponding author
- Ahmed, Rafi
- Venue
- Nature Immunology
- Published
- 2003-11-16
- Volume
- 4
- Issue
- 12
- Pages
- 1191-1198
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- OpenAlex
- W1974842026
- Cited by
- 1,830
- References
- 48
- Citations by year
- 2026: 41 · 2025: 57 · 2024: 42 · 2023: 63 · 2022: 67 · 2021: 69 · 2020: 67 · 2019: 70 · 2018: 56 · 2017: 59 · 2016: 77 · 2015: 73 · 2014: 73 · 2013: 96 · 2012: 91
- FWCI
- 30.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Keywords
- CD127, CD8+ T cells, effector T cells, memory T cells, apoptosis, adoptive transfer, viral infection, protective immunity, memory T cell generation
- MeSH terms
- Animals, Antigens, Surface, Cell Differentiation, Immunologic Memory, Lymphocyte Activation, Lymphocytic Choriomeningitis, Lymphocytic choriomeningitis virus, Mice, Transgenic, Signal Transduction, Gene Expression, T-Lymphocyte Subsets, CD8-Positive T-Lymphocytes, Cell Lineage, Adoptive Transfer, Receptors, Interleukin-7, Oligonucleotide Array Sequence Analysis, Mice
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