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Costimulatory receptors in the channel catfish: CD28 family members and their ligands

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Abstract

The CD28-B7 interaction is required to deliver a second signal necessary for T-cell activation. Additional membrane receptors of the CD28 and B7 families are also involved in immune checkpoints that positively or negatively regulate leukocyte activation, in particular T lymphocytes. BTLA is an inhibitory receptor that belongs to a third receptor family. Fish orthologs exist only for some of these genes, and the potential interactions between the corresponding ligands remain mostly unclear. In this work, we focused on the channel catfish (Ictalurus punctatus), a long-standing model for fish immunology, to analyze these co-stimulatory and co-inhibitory receptors. We identified one copy of cd28, ctla4, cd80/86, b7h1/dc, b7h3, b7h4, b7h5, two btla, and four b7h7 genes. Catfish CD28 contains the highly conserved mammalian cytoplasmic motif for PI3K and GRB2 recruitment, however this motif is absent in cyprinids. Fish CTLA4 share a C-terminal putative GRB2-binding site but lacks the mammalian PI3K/GRB2-binding motif. While critical V-domain residues for human CD80 or CD86 binding to CD28/CTLA4 show low conservation in fish CD80/86, C-domain residues are highly conserved, underscoring their significance. Catfish B7H1/DC had a long intracytoplasmic domain with a P-loop-NTPase domain that is absent in mammalian sequences, while the lack of NLS motif in fish B7H4 suggests this protein may not regulate cell growth when expressed intracellularly. Finally, there is a notable expansion of fish B7H7s, which likely play diverse roles in leukocyte regulation. Overall, our work contributes to a better understanding of fish leukocyte co-stimulatory and co-inhibitory receptors.

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References

  • August A, Gibson S, Kawakami Y, Kawakami T, Mills GB, Dupont B (1994) CD28 is associated with and induces the immediate tyrosine phosphorylation and activation of the Tec family kinase ITK/EMT in the human Jurkat leukemic T-cell line. Proc Natl Acad Sci USA 91:9347–9351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernard D, Riteau B, Hansen JD, Phillips RB, Michel F, Boudinot P, Benmansour A (2006) Costimulatory receptors in a teleost fish: typical CD28, elusive CTLA4. J Immunol 176:4191–4200

    Article  CAS  PubMed  Google Scholar 

  • Bernard D, Hansen JD, Du Pasquier L, Lefranc MP, Benmansour A, Boudinot P (2007) Costimulatory receptors in jawed vertebrates: conserved CD28, odd CTLA4 and multiple BTLAs. Dev Comp Immunol 31:255–271

    Article  CAS  PubMed  Google Scholar 

  • Bhatt RS, Berjis A, Konge JC, Mahoney KM, Klee AN, Freeman SS, Chen CH, Jegede OA, Catalano PJ, Pignon JC, Sticco-Ivins M, Zhu B, Hua P, Soden J, Zhu J, McDermott DF, Arulanandam AR, Signoretti S, Freeman GJ (2021) KIR3DL3 Is an Inhibitory Receptor for HHLA2 that Mediates an Alternative Immunoinhibitory Pathway to PD1. Cancer Immunol Res 9:156–169

    Article  CAS  PubMed  Google Scholar 

  • Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ (2007) Programmed death-1 ligand 1 interacts specifically with the B7–1 costimulatory molecule to inhibit T cell responses. Immunity 27:111–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen W, Qie C, Hu X, Wang L, Jiang J, Liu W, Liu J (2022) A small molecule inhibitor of VSIG-8 prevents its binding to VISTA. Invest New Drugs 40:690–699

    Article  PubMed  Google Scholar 

  • Chuang E, Fisher TS, Morgan RW, Robbins MD, Duerr JM, Vander Heiden MG, Gardner JP, Hambor JE, Neveu MJ, Thompson CB (2000) The CD28 and CTLA-4 receptors associate with the serine/threonine phosphatase PP2A. Immunity 13:313–322

    Article  CAS  PubMed  Google Scholar 

  • Ciprut S, Berberich A, Knoll M, Pusch S, Hoffmann D, Furkel J, Ward Gahlawat A, Kahlert-Konzelamnn L, Sahm F, Warnken U, Winter M, Schnolzer M, Pusch S, von Deimling A, Abdollahi A, Wick W, Lemke D (2022) AAMP is a binding partner of costimulatory human B7-H3. Neurooncol Adv 4:vdac098

  • Daeron M, Jaeger S, Du Pasquier L, Vivier E (2008) Immunoreceptor tyrosine-based inhibition motifs : a quest in the past and future. Immunol Rev 224:11–43

    Article  CAS  PubMed  Google Scholar 

  • FAO (2023) Global Aquatic Processed Production Statistics. Fisheries and Aquaculture Division Rome

  • Fargeas CA, Truneh A, Reddy M, Hurle M, Sweet R, Sekaly RP (1995) Identification of residues in the V domain of CD80 (B7–1) implicated in functional interactions with CD28 and CTLA4. J Exp Med 182:667–675

    Article  CAS  PubMed  Google Scholar 

  • Flajnik MF, Tlapakova T, Criscitiello MF, Krylov V, Ohta Y (2012) Evolution of the B7 family: co-evolution of B7H6 and NKp30, identification of a new B7 family member, B7H7, and of B7’s historical relationship with the MHC. Immunogenetics 64:571–590

  • Flies DB, Han X, Higuchi T, Zheng L, Sun J, Ye J, Chen L (2014) Coinhibitory receptor PD-1H preferentially suppresses CD4 T cell-mediated immunity. J Clin Inv 124:1966–1975

    Article  CAS  Google Scholar 

  • Francisco LM, Sage PT, Sharpe AH (2010) The PD-1 pathway in tolerance and autoimmunity. Immunol Rev 236:219–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Getu AA, Tigabu A, Zhou M, Lu J, Fodstad O, Tan M (2023) New frontiers in immune checkpoint B7–H3 (CD276) research and drug development. Mol Cancer 22:43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenwald RJ, Freeman GJ, Sharpe AH (2005) The B7 family revisited. Annu Rev Immunol 23:515–548

    Article  PubMed  Google Scholar 

  • Hansen JD, Du Pasquier L, Lefranc MP, Lopez V, Benmansour A, Boudinot P (2009) The B7 family of immunoregulatory receptors: a comparative and evolutionary perspective. Mol Immunol 46:457–472

    Article  CAS  PubMed  Google Scholar 

  • Harada Y, Tanabe E, Watanabe R, Weiss BD, Matsumoto A, Ariga H, Koiwai O, Fukui Y, Kubo M, June CH, Abe R (2001) Novel role of phosphatidylinositol 3-kinase in CD28-mediated costimulation. J Biol Chem 276:9003–9008

    Article  CAS  PubMed  Google Scholar 

  • Harada Y, Ohgai D, Watanabe R, Okano K, Koiwai O, Tanabe K, Toma H, Altman A, Abe R (2003) A single amino acid alteration in cytoplasmic domain determines IL-2 promoter activation by ligation of CD28 but not inducible costimulator (ICOS). J Exp Med 197:257–262

    Article  PubMed  PubMed Central  Google Scholar 

  • Hashiguchi M, Kobori H, Ritprajak P, Kamimura Y, Kozono H, Azuma M (2008) Triggering receptor expressed on myeloid cell-like transcript 2 (TLT-2) is a counter-receptor for B7–H3 and enhances T cell responses. Proc Natl Acad Sci USA 105:10495–10500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higo K, Oda M, Morii H, Takahashi J, Harada Y, Ogawa S, Abe R (2014) Quantitative analysis by surface plasmon resonance of CD28 interaction with cytoplasmic adaptor molecules Grb2, Gads and p85 PI3K. Immunol Invest 43:278–291

    Article  CAS  PubMed  Google Scholar 

  • Holdorf AD, Green JM, Levin SD, Denny MF, Straus DB, Link V, Changelian PS, Allen PM, Shaw AS (1999) Proline residues in CD28 and the Src homology (SH)3 domain of Lck are required for T cell costimulation. J Exp Med 190:375–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu CB, Huang C, Wang J, Hong Y, Fan DD, Chen Y, Lin AF, Xiang LX, Shao JZ (2023) PD-L1/BTLA Checkpoint Axis Exploited for Bacterial Immune Escape by Restraining CD8+ T Cell-Initiated Adaptive Immunity in Zebrafish. J Immunol 211:816–835

    Article  CAS  PubMed  Google Scholar 

  • Husain B, Ramani SR, Chiang E, Lehoux I, Paduchuri S, Arena TA, Patel A, Wilson B, Chan P, Franke Y, Wong AW, Lill JR, Turley SJ, Gonzalez LC, Grogan JL, Martinez-Martin N (2019) A Platform for Extracellular Interactome Discovery Identifies Novel Functional Binding Partners for the Immune Receptors B7–H3/CD276 and PVR/CD155. Mol Cell Proteomics 18:2310–2323

    Article  PubMed  PubMed Central  Google Scholar 

  • Hutloff A, Dittrich AM, Beier KC, Eljaschewitsch B, Kraft R, Anagnostopoulos I, Kroczek RA (1999) ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 397:263–266

    Article  CAS  PubMed  Google Scholar 

  • Ikemizu S, Gilbert RJ, Fennelly JA, Collins AV, Harlos K, Jones EY, Stuart DI, Davis SJ (2000) Structure and dimerization of a soluble form of B7–1. Immunity 12:51–60

    Article  CAS  PubMed  Google Scholar 

  • Ishida Y, Agata Y, Shibahara K, Honjo T (1992) Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J 11:3887–3895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biémont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigó R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quétier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957

  • Johnston RJ, Su LJ, Pinckney J, Critton D, Boyer E, Krishnakumar A, Corbett M, Rankin AL, Dibella R, Campbell L, Martin GH, Lemar H, Cayton T, Huang RY, Deng X, Nayeem A, Chen H, Ergel B, Rizzo JM, Yamniuk AP, Dutta S, Ngo J, Shorts AO, Ramakrishnan R, Kozhich A, Holloway J, Fang H, Wang YK, Yang Z, Thiam K, Rakestraw G, Rajpal A, Sheppard P, Quigley M, Bahjat KS, Korman AJ (2019) VISTA is an acidic pH-selective ligand for PSGL-1. Nature 574:565–570

  • Kaur S, Qureshi OS, Sansom DM (2013) Comparison of the Intracellular Trafficking Itinerary of CTLA-4 Orthologues. PLoS ONE 8:e60903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keir ME, Butte MJ, Freeman GJ, Sharpe AH (2008) PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 26:677–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kortum AN, Rodriguez-Nunez I, Yang J, Shim J, Runft D, O’Driscoll ML, Haire RN, Cannon JP, Turner PM, Litman RT, Kim CH, Neely MN, Litman GW, Yoder JA (2014) Differential expression and ligand binding indicate alternative functions for zebrafish polymeric immunoglobulin receptor (pIgR) and a family of pIgR-like (PIGRL) proteins. Immunogenetics 66:267–279

  • Leddon SA, Fettis MM, Abramo K, Kelly R, Oleksyn D, Miller J (2020) The CD28 Transmembrane Domain Contains an Essential Dimerization Motif. Front Immunol 11:1519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leipe DD, Koonin EV, Aravind L (2004) STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 343:1–28

    Article  CAS  PubMed  Google Scholar 

  • Leitner J, Klauser C, Pickl WF, Stockl J, Majdic O, Bardet AF, Kreil DP, Dong C, Yamazaki T, Zlabinger G, Pfistershammer K, Steinberger P (2009) B7–H3 is a potent inhibitor of human T-cell activation: No evidence for B7–H3 and TREML2 interaction. Eur J Immunol 39:1754–1764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin YF, He J, Zeng RY, Li ZM, Luo ZY, Pan WQ, Weng SP, Guo CJ, He JG (2019) Deletion of the Infectious spleen and kidney necrosis virus ORF069L reduces virulence to mandarin fish Siniperca chuatsi. Fish Shellfish Immunol 95:328–335

    Article  CAS  PubMed  Google Scholar 

  • Lindsten T, Lee KP, Harris ES, Petryniak B, Craighead N, Reynolds PJ, Lombard DB, Freeman GJ, Nadler LM, Gray GS et al (1993) Characterization of CTLA-4 structure and expression on human T cells. J Immunol 151:3489–3499

    Article  CAS  PubMed  Google Scholar 

  • Marengere LE, Waterhouse P, Duncan GS, Mittrucker HW, Feng GS, Mak TW (1996) Regulation of T cell receptor signaling by tyrosine phosphatase SYP association with CTLA-4. Science 272:1170–1173

    Article  CAS  PubMed  Google Scholar 

  • Morales-Lange B, Ramirez-Cepeda F, Schmitt P, Guzman F, Lagos L, Overland M, Wong-Benito V, Imarai M, Fuentes D, Boltana S, Alcaino J, Soto C, Mercado L (2021) Interferon Gamma Induces the Increase of Cell-Surface Markers (CD80/86, CD83 and MHC-II) in Splenocytes From Atlantic Salmon. Front Immunol 12:666356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peach RJ, Bajorath J, Brady W, Leytze G, Greene J, Naemura J, Linsley PS (1994) Complementarity determining region 1 (CDR1)- and CDR3-analogous regions in CTLA-4 and CD28 determine the binding to B7–1. J Exp Med 180:2049–2058

    Article  CAS  PubMed  Google Scholar 

  • Peach RJ, Bajorath J, Naemura J, Leytze G, Greene J, Aruffo A, Linsley PS (1995) Both extracellular immunoglobin-like domains of CD80 contain residues critical for binding T cell surface receptors CTLA-4 and CD28. J Biol Chem 270:21181–21187

    Article  CAS  PubMed  Google Scholar 

  • Qureshi OS, Zheng Y, Nakamura K, Attridge K, Manzotti C, Schmidt EM, Baker J, Jeffery LE, Kaur S, Briggs Z, Hou TZ, Futter CE, Anderson G, Walker LS, Sansom DM (2011) Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 332:600–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rombout JH, van der Tuin SJ, Yang G, Schopman N, Mroczek A, Hermsen T, Taverne-Thiele JJ (2008) Expression of the polymeric Immunoglobulin Receptor (pIgR) in mucosal tissues of common carp (Cyprinus carpio L.). Fish Shellfish Immunol 24:620–628

    Article  CAS  PubMed  Google Scholar 

  • Rudd CE, Schneider H (2003) Unifying concepts in CD28, ICOS and CTLA4 co-receptor signaling. Nat Rev Immunol 3:544–556

    Article  CAS  PubMed  Google Scholar 

  • Schneider H, Rudd CE (2008) CD28 and Grb-2, relative to Gads or Grap, preferentially co-operate with Vav1 in the activation of NFAT/AP-1 transcription. Biochem Biophys Res Commun 369:616–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sedy JR, Gavrieli M, Potter KG, Hurchla MA, Lindsley RC, Hildner K, Scheu S, Pfeffer K, Ware CF, Murphy TL, Murphy KM (2005) B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat Immunol 6:90–98

    Article  CAS  PubMed  Google Scholar 

  • Stamper CC, Zhang Y, Tobin JF, Erbe DV, Ikemizu S, Davis SJ, Stahl ML, Seehra J, Somers WS, Mosyak L (2001) Crystal structure of the B7–1/CTLA-4 complex that inhibits human immune responses. Nature 410:608–611

    Article  CAS  PubMed  Google Scholar 

  • Stet RJ, Hermsen T, Westphal AH, Jukes J, Engelsma M, Lidy Verburg-van Kemenade BM, Dortmans J, Aveiro J, Savelkoul HF (2005) Novel immunoglobulin-like transcripts in teleost fish encode polymorphic receptors with cytoplasmic ITAM or ITIM and a new structural Ig domain similar to the natural cytotoxicity receptor NKp44. Immunogenetics 57:77–89

    Article  CAS  PubMed  Google Scholar 

  • Sugamata R, Suetake H, Kikuchi K, Suzuki Y (2009) Teleost B7 expressed on monocytes regulates T cell responses. J Immunol 182:6799–6806

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Rubinstein R, Lines JL, Wasiuk A, Ahonen C, Guo Y, Lu LF, Gondek D, Wang Y, Fava RA, Fiser A, Almo S, Noelle RJ (2011) VISTA, a novel mouse Ig superfamily ligand that negatively regulates T cell responses. J Exp Med 208:577–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Wu G, Manick B, Hernandez V, Renelt M, Erickson C, Guan J, Singh R, Rollins S, Solorz A, Bi M, Li J, Grabowski D, Dirkx J, Tracy C, Stuart T, Ellinghuysen C, Desmond D, Foster C, Kalabokis V (2019) VSIG-3 as a ligand of VISTA inhibits human T-cell function. Immunology 156:74–85

    Article  CAS  PubMed  Google Scholar 

  • Watanabe N, Gavrieli M, Sedy JR, Yang J, Fallarino F, Loftin SK, Hurchla MA, Zimmerman N, Sim J, Zang X, Murphy TL, Russell JH, Allison JP, Murphy KM (2003) BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat Immunol 4:670–679

    Article  CAS  PubMed  Google Scholar 

  • Wcisel DJ, Dornburg A, McConnell SC, Hernandez KM, Andrade J, de Jong JLO, Litman GW, Yoder JA (2023) A highly diverse set of novel immunoglobulin-like transcript (NILT) genes in zebrafish indicates a wide range of functions with complex relationships to mammalian receptors. Immunogenetics 75:53–69

    Article  CAS  PubMed  Google Scholar 

  • Xie X, Chen C, Chen W, Jiang J, Wang L, Li T, Sun H, Liu J (2021) Structural Basis of VSIG3: The Ligand for VISTA. Front Immunol 12:625808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan R, Yang S, Gu A, Zhan F, He C, Qin C, Zhang X, Feng P (2013) Murine b7–h3 is a co-stimulatory molecule for T cell activation. Monoclon Antib Immunodiagn Immunother 32:395–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang WC, Ghiotto M, Castellano R, Collette Y, Auphan N, Nunes JA, Olive D (2000) Role of Tec kinase in nuclear factor of activated T cells signaling. Int Immunol 12:1547–1552

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Schwartz JC, Almo SC, Nathenson SG (2003) Crystal structure of the receptor-binding domain of human B7–2: insights into organization and signaling. Proc Natl Acad Sci USA 100:2586–2591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YA, Hikima J, Li J, LaPatra SE, Luo YP, Sunyer JO (2009) Conservation of structural and functional features in a primordial CD80/86 molecule from rainbow trout (Oncorhynchus mykiss), a primitive teleost fish. J Immunol 183:83–96

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Wu H, Lu D, Li G, Sun C, Song H, Li J, Zhai T, Huang L, Hou C, Wang W, Zhou B, Chen S, Lu B, Zhang X (2013) The costimulatory molecule B7–H4 promote tumor progression and cell proliferation through translocating into nucleus. Oncogene 32:5347–5358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XJ, Zhang XY, Wang P, Zhang YA (2018) Identification of another primordial CD80/86 molecule in rainbow trout: Insights into the origin and evolution of CD80 and CD86 in vertebrates. Dev Comp Immunol 89:73–82

    Article  PubMed  Google Scholar 

  • Zhu Y, Yao S, Iliopoulou BP, Han X, Augustine MM, Xu H, Phennicie RT, Flies SJ, Broadwater M, Ruff W, Taube JM, Zheng L, Luo L, Zhu G, Chen J, Chen L (2013) B7–H5 costimulates human T cells via CD28H. Nat Commun 4:2043

    Article  PubMed  Google Scholar 

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Funding

SQ was funded by US Department of Agriculture, Agricultural Research Service Project 6066-31000-016-00D. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture (USDA). USDA is an equal opportunity provider and employer. PB was funded by Agence Nationale de la Recherche (ANR-21-CE35-0019, LipofishVac) and by institutional grants from INRAE.

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  1. USDA-ARS-WARU, 141 Experiment Station Rd, 38776, Stoneville, MS, USA

    Sylvie M. A. Quiniou

  2. Center for Immunology and Microbial Research, University of Mississippi Medical Center, 39216, Jackson, MS, USA

    Eva Bengtén

  3. Department of Cell and Molecular Biology, University of Mississippi Medical Center, 39216, Jackson, MS, USA

    Eva Bengtén

  4. Université Paris-Saclay, INRAE, UVSQ, VIM, Jouy-en-Josas, 78350, France

    Pierre Boudinot

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Quiniou, S.M.A., Bengtén, E. & Boudinot, P. Costimulatory receptors in the channel catfish: CD28 family members and their ligands. Immunogenetics 76, 51–67 (2024). https://doi.org/10.1007/s00251-023-01327-3

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