Identification of two distinct populations of WT1-specific cytotoxic T lymphocytes in co-vaccination of WT1 killer and helper peptides.

Antigens, Neoplasm / immunology CD5 Antigens / immunology Cancer Vaccines / immunology Cell Death / immunology Cell Proliferation / physiology Cells, Cultured Humans Leukocytes, Mononuclear / immunology Neoplasm Recurrence, Local / immunology Peptides / immunology T-Lymphocytes, Cytotoxic / immunology T-Lymphocytes, Helper-Inducer / immunology Vaccination / methods Vaccines, Subunit / immunology WT1 Proteins / immunology
CD5 Helper peptide Peptide vaccine Tetramerhigh WT1

Journal

Cancer immunology, immunotherapy : CII
ISSN: 1432-0851
Titre abrégé: Cancer Immunol Immunother
Pays: Germany
ID NLM: 8605732

Informations de publication

Date de publication:
Jan 2021
Historique:
received: 31 03 2020
accepted: 16 07 2020
pubmed: 23 7 2020
medline: 30 1 2021
entrez: 23 7 2020
Statut: ppublish

Résumé

Simultaneous induction of tumor antigen-specific cytotoxic T lymphocytes (CTLs) and helper T lymphocytes (HTLs) is required for an optimal anti-tumor immune response. WT1

Identifiants

DOI: 10.1007/s00262-020-02675-9 PMID: 32696072
pubmed: 32696072
doi: 10.1007/s00262-020-02675-9
pii: 10.1007/s00262-020-02675-9
doi:

Substances chimiques

Antigens, Neoplasm 0
CD5 Antigens 0
Cancer Vaccines 0
Peptides 0
Vaccines, Subunit 0
WT1 Proteins 0
WT1 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

253-263

Subventions

Organisme : Japan Society for the Promotion of Science
ID : JP17K07215

Références

Schoenberger SP, Toes RE, van der Voort EI, Offringa R, Melief CJ (1998) T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393:480–483. https://doi.org/10.1038/31002
doi: 10.1038/31002 pubmed: 9624005
Joffre OP, Segura E, Savina A, Amigorena S (2012) Cross-presentation by dendritic cells. Nat Rev Immunol 12:557–569. https://doi.org/10.1038/nri3254
doi: 10.1038/nri3254 pubmed: 22790179
Bos R, Sherman LA (2010) CD4 + T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8 + T lymphocytes. Cancer Res 70:8368–8377. https://doi.org/10.1158/0008-5472.CAN-10-1322
doi: 10.1158/0008-5472.CAN-10-1322 pubmed: 20940398 pmcid: 2970736
Nakata J, Nakajima H, Hayashibara H, Imafuku K, Morimoto S, Fujiki F, Motooka D, Okuzaki D, Hasegawa K, Hosen N, Tsuboi A, Oka Y, Kumanogoh A, Oji Y, Sugiyama H (2018) Extremely strong infiltration of WT1-specific CTLs into mouse tumor by the combination vaccine with WT1-specific CTL and helper peptides. Oncotarget. 9:36029–36038. https://doi.org/10.18632/oncotarget.26338
doi: 10.18632/oncotarget.26338 pubmed: 30542516 pmcid: 6267595
Ahrends T, Spanjaard A, Pilzecker B, Babala N, Bovens A, Xiao Y, Jacobs H, Borst J (2017) CD4(+) T cell help confers a cytotoxic T cell effector program including coinhibitory receptor downregulation and increased tissue invasiveness. Immunity 47(848–61):e5. https://doi.org/10.1016/j.immuni.2017.10.009
doi: 10.1016/j.immuni.2017.10.009
Aubert RD, Kamphorst AO, Sarkar S, Vezys V, Ha SJ, Barber DL, Ye L, Sharpe AH, Freeman GJ, Ahmed R (2011) Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection. Proc Natl Acad Sci USA 108:21182–21187. https://doi.org/10.1073/pnas.1118450109
doi: 10.1073/pnas.1118450109 pubmed: 22160724
Sun JC, Bevan MJ (2003) Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300:339–342. https://doi.org/10.1126/science.1083317
doi: 10.1126/science.1083317 pubmed: 12690202 pmcid: 2778341
Sconocchia G, Eppenberger-Castori S, Zlobec I, Karamitopoulou E, Arriga R, Coppola A, Caratelli S, Spagnoli GC, Lauro D, Lugli A, Han J, Iezzi G, Ferrone C, Ferlosio A, Tornillo L, Droeser R, Rossi P, Attanasio A, Ferrone S, Terracciano L (2014) HLA class II antigen expression in colorectal carcinoma tumors as a favorable prognostic marker. Neoplasia. 16:31–42. https://doi.org/10.1593/neo.131568
doi: 10.1593/neo.131568 pubmed: 24563618 pmcid: 3924546
Nasman A, Andersson E, Marklund L, Tertipis N, Hammarstedt-Nordenvall L, Attner P, Nyberg T, Masucci GV, Munck-Wikland E, Ramqvist T, Dalianis T (2013) HLA class I and II expression in oropharyngeal squamous cell carcinoma in relation to tumor HPV status and clinical outcome. PLoS ONE 8:e77025. https://doi.org/10.1371/journal.pone.0077025
doi: 10.1371/journal.pone.0077025 pubmed: 24130830 pmcid: 3794938
Esteban F, Ruiz-Cabello F, Concha A, Perez-Ayala M, Sanchez-Rozas JA, Garrido F (1990) HLA-DR expression is associated with excellent prognosis in squamous cell carcinoma of the larynx. Clin Exp Metastasis 8:319–328
doi: 10.1007/BF01810678
Cheever MA, Allison JP, Ferris AS, Finn OJ, Hastings BM, Hecht TT, Mellman I, Prindiville SA, Viner JL, Weiner LM, Matrisian LM (2009) The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res. 15:5323–5337
doi: 10.1158/1078-0432.CCR-09-0737
Fujiki F, Oka Y, Tsuboi A, Kawakami M, Kawakatsu M, Nakajima H, Elisseeva OA, Harada Y, Ito K, Li Z, Tatsumi N, Sakaguchi N, Fujioka T, Masuda T, Yasukawa M, Udaka K, Kawase I, Oji Y, Sugiyama H (2007) Identification and characterization of a WT1 (Wilms Tumor Gene) protein-derived HLA-DRB1*0405-restricted 16-mer helper peptide that promotes the induction and activation of WT1-specific cytotoxic T lymphocytes. J Immunother 30:282–293. https://doi.org/10.1097/01.cji.0000211337.91513.94
doi: 10.1097/01.cji.0000211337.91513.94 pubmed: 17414319
Fujiki F, Oka Y, Kawakatsu M, Tsuboi A, Nakajima H, Elisseeva OA, Harada Y, Li Z, Tatsumi N, Kamino E, Shirakata T, Nishida S, Taniguchi Y, Kawase I, Oji Y, Sugiyama H (2008) A WT1 protein-derived, naturally processed 16-mer peptide, WT1(332), is a promiscuous helper peptide for induction of WT1-specific Th1-type CD4(+) T cells. Microbiol Immunol 52:591–600. https://doi.org/10.1111/j.1348-0421.2008.00080.x
doi: 10.1111/j.1348-0421.2008.00080.x pubmed: 19120973
Anguille S, Fujiki F, Smits EL, Oji Y, Lion E, Oka Y, Berneman ZN, Sugiyama H (2013) Identification of a Wilms’ tumor 1-derived immunogenic CD4(+) T-cell epitope that is recognized in the context of common Caucasian HLA-DR haplotypes. Leukemia 27:748–750. https://doi.org/10.1038/leu.2012.248
doi: 10.1038/leu.2012.248 pubmed: 22929521
Kobayashi Y, Sakura T, Miyawaki S, Toga K, Sogo S, Heike Y (2017) A new peptide vaccine OCV-501: in vitro pharmacology and phase 1 study in patients with acute myeloid leukemia. Cancer Immunol Immunother 66:851–863. https://doi.org/10.1007/s00262-017-1981-3
doi: 10.1007/s00262-017-1981-3 pubmed: 28321480 pmcid: 5489634
Lin Y, Fujiki F, Katsuhara A, Oka Y, Tsuboi A, Aoyama N, Tanii S, Nakajima H, Tatsumi N, Morimoto S, Tamanaka T, Tachino S, Hosen N, Nishida S, Oji Y, Kumanogoh A, Sugiyama H (2013) HLA-DPB1*05: 01-restricted WT1332-specific TCR-transduced CD4 + T lymphocytes display a helper activity for WT1-specific CTL induction and a cytotoxicity against leukemia cells. J Immunother 36:159–170. https://doi.org/10.1097/CJI.0b013e3182873581
doi: 10.1097/CJI.0b013e3182873581 pubmed: 23502763
Fujiki F, Oka Y, Kawakatsu M, Tsuboi A, Tanaka-Harada Y, Hosen N, Nishida S, Shirakata T, Nakajima H, Tatsumi N, Hashimoto N, Taguchi T, Ueda S, Nonomura N, Takeda Y, Ito T, Myoui A, Izumoto S, Maruno M, Yoshimine T, Noguchi S, Okuyama A, Kawase I, Oji Y, Sugiyama H (2010) A clear correlation between WT1-specific Th response and clinical response in WT1 CTL epitope vaccination. Anticancer Res. 30:2247–2254
pubmed: 20651376
Tsuboi A, Hashimoto N, Fujiki F, Morimoto S, Kagawa N, Nakajima H, Hosen N, Nishida S, Nakata J, Morita S, Sakamoto J, Oji Y, Oka Y, Sugiyama H (2019) A phase I clinical study of a cocktail vaccine of Wilms’ tumor 1 (WT1) HLA class I and II peptides for recurrent malignant glioma. Cancer Immunol Immunother 68:331–340. https://doi.org/10.1007/s00262-018-2274-1
doi: 10.1007/s00262-018-2274-1 pubmed: 30430205
Phan GQ, Touloukian CE, Yang JC, Restifo NP, Sherry RM, Hwu P, Topalian SL, Schwartzentruber DJ, Seipp CA, Freezer LJ, Morton KE, Mavroukakis SA, White DE, Rosenberg SA (2003) Immunization of patients with metastatic melanoma using both class I- and class II-restricted peptides from melanoma-associated antigens. J Immunother 26:349–356
doi: 10.1097/00002371-200307000-00007
Slingluff CL Jr, Lee S, Zhao F, Chianese-Bullock KA, Olson WC, Butterfield LH, Whiteside TL, Leming PD, Kirkwood JM (2013) A randomized phase II trial of multiepitope vaccination with melanoma peptides for cytotoxic T cells and helper T cells for patients with metastatic melanoma (E1602). Clin Cancer Res 19:4228–4238. https://doi.org/10.1158/1078-0432.CCR-13-0002
doi: 10.1158/1078-0432.CCR-13-0002 pubmed: 23653149
Izumoto S, Tsuboi A, Oka Y, Suzuki T, Hashiba T, Kagawa N, Hashimoto N, Maruno M, Elisseeva OA, Shirakata T, Kawakami M, Oji Y, Nishida S, Ohno S, Kawase I, Hatazawa J, Nakatsuka S, Aozasa K, Morita S, Sakamoto J, Sugiyama H, Yoshimine T (2008) Phase II clinical trial of Wilms tumor 1 peptide vaccination for patients with recurrent glioblastoma multiforme. J Neurosurg 108:963–971. https://doi.org/10.3171/JNS/2008/108/5/0963
doi: 10.3171/JNS/2008/108/5/0963 pubmed: 18447714
Tsuboi A, Oka Y, Udaka K, Murakami M, Masuda T, Nakano A, Nakajima H, Yasukawa M, Hiraki A, Oji Y, Kawakami M, Hosen N, Fujioka T, Wu F, Taniguchi Y, Nishida S, Asada M, Ogawa H, Kawase I, Sugiyama H (2002) Enhanced induction of human WT1-specific cytotoxic T lymphocytes with a 9-mer WT1 peptide modified at HLA-A*2402-binding residues. Cancer Immunol Immunother 51:614–620. https://doi.org/10.1007/s00262-002-0328-9
doi: 10.1007/s00262-002-0328-9 pubmed: 12439606
Nishida S, Ishikawa T, Egawa S, Koido S, Yanagimoto H, Ishii J, Kanno Y, Kokura S, Yasuda H, Oba MS, Sato M, Morimoto S, Fujiki F, Eguchi H, Nagano H, Kumanogoh A, Unno M, Kon M, Shimada H, Ito K, Homma S, Oka Y, Morita S, Sugiyama H (2018) Combination gemcitabine and WT1 peptide vaccination improves progression-free survival in advanced pancreatic ductal adenocarcinoma: a phase II randomized study. Cancer Immunol Res. https://doi.org/10.1158/2326-6066.CIR-17-0386
doi: 10.1158/2326-6066.CIR-17-0386 pubmed: 29653982
Hashimoto N, Tsuboi A, Kagawa N, Chiba Y, Izumoto S, Kinoshita M, Kijima N, Oka Y, Morimoto S, Nakajima H, Morita S, Sakamoto J, Nishida S, Hosen N, Oji Y, Arita N, Yoshimine T, Sugiyama H (2015) Wilms tumor 1 peptide vaccination combined with temozolomide against newly diagnosed glioblastoma: safety and impact on immunological response. Cancer Immunol Immunother 64:707–716. https://doi.org/10.1007/s00262-015-1674-8
doi: 10.1007/s00262-015-1674-8 pubmed: 25772149
Friedlein G, El Hage F, Vergnon I, Richon C, Saulnier P, Lecluse Y, Caignard A, Boumsell L, Bismuth G, Chouaib S, Mami-Chouaib F (2007) Human CD5 protects circulating tumor antigen-specific CTL from tumor-mediated activation-induced cell death. J Immunol. 178:6821–6827. https://doi.org/10.4049/jimmunol.178.11.6821
doi: 10.4049/jimmunol.178.11.6821 pubmed: 17513730
Tabbekh M, Franciszkiewicz K, Haouas H, Lecluse Y, Benihoud K, Raman C, Mami-Chouaib F (2011) Rescue of tumor-infiltrating lymphocytes from activation-induced cell death enhances the antitumor CTL response in CD5-deficient mice. J Immunol. 187:102–109. https://doi.org/10.4049/jimmunol.1004145
doi: 10.4049/jimmunol.1004145 pubmed: 21622855
Fulton RB, Hamilton SE, Xing Y, Best JA, Goldrath AW, Hogquist KA, Jameson SC (2015) The TCR’s sensitivity to self peptide-MHC dictates the ability of naive CD8(+) T cells to respond to foreign antigens. Nat Immunol 16:107–117. https://doi.org/10.1038/ni.3043
doi: 10.1038/ni.3043 pubmed: 25419629
Slingluff CL Jr, Petroni GR, Chianese-Bullock KA, Smolkin ME, Ross MI, Haas NB, von Mehren M, Grosh WW (2011) Randomized multicenter trial of the effects of melanoma-associated helper peptides and cyclophosphamide on the immunogenicity of a multipeptide melanoma vaccine. J Clin Oncol 29:2924–2932. https://doi.org/10.1200/JCO.2010.33.8053
doi: 10.1200/JCO.2010.33.8053 pubmed: 21690475 pmcid: 3138719
Lazarski CA, Chaves FA, Jenks SA, Wu S, Richards KA, Weaver JM, Sant AJ (2005) The kinetic stability of MHC class II:peptide complexes is a key parameter that dictates immunodominance. Immunity 23:29–40. https://doi.org/10.1016/j.immuni.2005.05.009
doi: 10.1016/j.immuni.2005.05.009 pubmed: 16039577
Borst J, Ahrends T, Babala N, Melief CJM, Kastenmuller W (2018) CD4(+) T cell help in cancer immunology and immunotherapy. Nat Rev Immunol 18:635–647. https://doi.org/10.1038/s41577-018-0044-0
doi: 10.1038/s41577-018-0044-0 pubmed: 30057419
Zanetti M (2015) Tapping CD4 T cells for cancer immunotherapy: the choice of personalized genomics. J Immunol. 194:2049–2056. https://doi.org/10.4049/jimmunol.1402669
doi: 10.4049/jimmunol.1402669 pubmed: 25710958
Southwood S, Sidney J, Kondo A, del Guercio MF, Appella E, Hoffman S, Kubo RT, Chesnut RW, Grey HM, Sette A (1998) Several common HLA-DR types share largely overlapping peptide binding repertoires. J Immunol. 160:3363–3373
pubmed: 9531296
Kobayashi H, Wood M, Song Y, Appella E, Celis E (2000) Defining promiscuous MHC class II helper T-cell epitopes for the HER2/neu tumor antigen. Cancer Res 60:5228–5236
pubmed: 11016652
Aarntzen EH, De Vries IJ, Lesterhuis WJ, Schuurhuis D, Jacobs JF, Bol K, Schreibelt G, Mus R, De Wilt JH, Haanen JB, Schadendorf D, Croockewit A, Blokx WA, Van Rossum MM, Kwok WW, Adema GJ, Punt CJ, Figdor CG (2013) Targeting CD4(+) T-helper cells improves the induction of antitumor responses in dendritic cell-based vaccination. Cancer Res 73:19–29. https://doi.org/10.1158/0008-5472.CAN-12-1127
doi: 10.1158/0008-5472.CAN-12-1127 pubmed: 23087058
Koido S, Homma S, Okamoto M, Takakura K, Mori M, Yoshizaki S, Tsukinaga S, Odahara S, Koyama S, Imazu H, Uchiyama K, Kajihara M, Arakawa H, Misawa T, Toyama Y, Yanagisawa S, Ikegami M, Kan S, Hayashi K, Komita H, Kamata Y, Ito M, Ishidao T, Yusa S, Shimodaira S, Gong J, Sugiyama H, Ohkusa T, Tajiri H (2014) Treatment with chemotherapy and dendritic cells pulsed with multiple Wilms’ tumor 1 (WT1)-specific MHC class I/II-restricted epitopes for pancreatic cancer. Clin Cancer Res 20:4228–4239. https://doi.org/10.1158/1078-0432.CCR-14-0314
doi: 10.1158/1078-0432.CCR-14-0314 pubmed: 25056373
Aloysius MM, Mc Kechnie AJ, Robins RA, Verma C, Eremin JM, Farzaneh F, Habib NA, Bhalla J, Hardwick NR, Satthaporn S, Sreenivasan T, El-Sheemy M, Eremin O (2009) Generation in vivo of peptide-specific cytotoxic T cells and presence of regulatory T cells during vaccination with hTERT (class I and II) peptide-pulsed DCs. J Transl Med. 7:18. https://doi.org/10.1186/1479-5876-7-18
doi: 10.1186/1479-5876-7-18 pubmed: 19298672 pmcid: 2674878
Sanchez PJ, McWilliams JA, Haluszczak C, Yagita H, Kedl RM (2007) Combined TLR/CD40 stimulation mediates potent cellular immunity by regulating dendritic cell expression of CD70 in vivo. J Immunol. 178:1564–1572. https://doi.org/10.4049/jimmunol.178.3.1564
doi: 10.4049/jimmunol.178.3.1564 pubmed: 17237405
Klebanoff CA, Gattinoni L, Torabi-Parizi P, Kerstann K, Cardones AR, Finkelstein SE, Palmer DC, Antony PA, Hwang ST, Rosenberg SA, Waldmann TA, Restifo NP (2005) Central memory self/tumor-reactive CD8 + T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci USA 102:9571–9576. https://doi.org/10.1073/pnas.0503726102
doi: 10.1073/pnas.0503726102 pubmed: 15980149
Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, Citrin DE, Restifo NP, Robbins PF, Wunderlich JR, Morton KE, Laurencot CM, Steinberg SM, White DE, Dudley ME (2011) Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17:4550–4557. https://doi.org/10.1158/1078-0432.CCR-11-0116
doi: 10.1158/1078-0432.CCR-11-0116 pubmed: 21498393 pmcid: 3131487
Mandl JN, Monteiro JP, Vrisekoop N, Germain RN (2013) T cell-positive selection uses self-ligand binding strength to optimize repertoire recognition of foreign antigens. Immunity 38:263–274. https://doi.org/10.1016/j.immuni.2012.09.011
doi: 10.1016/j.immuni.2012.09.011 pubmed: 23290521 pmcid: 3785078
Katsuhara A, Fujiki F, Aoyama N, Tanii S, Morimoto S, Oka Y, Tsuboi A, Nakajima H, Kondo K, Tatsumi N, Nakata J, Nakae Y, Takashima S, Nishida S, Hosen N, Sogo S, Oji Y, Sugiyama H (2015) Transduction of a novel HLA-DRB1*04:05-restricted, WT1-specific TCR gene into human CD4 + T cells confers killing activity against human leukemia cells. Anticancer Res 35:1251–1261
pubmed: 25750272

Auteurs

Fumihiro Fujiki (F)

Department of Cancer Immunology, Osaka University Graduate School of Medicine, 1-7 Yamada-oka, Suita, Osaka, 565-0871, Japan. fu-fuji@sahs.med.osaka-u.ac.jp.
ORCID: 0000-0002-2433-510X

Akihiro Tsuboi (A)

Department of Cancer Immunotherapy, Osaka University Graduate School of Medicine, Osaka, Japan.

Soyoko Morimoto (S)

Department of Cancer Immunotherapy, Osaka University Graduate School of Medicine, Osaka, Japan.

Naoya Hashimoto (N)

Department of Neurosurgery, Kyoto Prefectural University of Medicine, Graduate School of Medical Science, Kyoto, Japan.

Miki Inatome (M)

Department of Clinical Laboratory and Biomedical Sciences, Osaka University Graduate School of Medicine, Osaka, Japan.

Hiroko Nakajima (H)

Department of Cancer Immunology, Osaka University Graduate School of Medicine, 1-7 Yamada-oka, Suita, Osaka, 565-0871, Japan.

Jun Nakata (J)

Department of Clinical Laboratory and Biomedical Sciences, Osaka University Graduate School of Medicine, Osaka, Japan.

Sumiyuki Nishida (S)

Department of Respiratory Medicine and Clinical Immunology, Osaka University Graduate School of Medicine, Osaka, Japan.

Kana Hasegawa (K)

Department of Cancer Immunology, Osaka University Graduate School of Medicine, 1-7 Yamada-oka, Suita, Osaka, 565-0871, Japan.

Naoki Hosen (N)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Osaka, Japan.
Department of Cancer Stem Cell Biology, Osaka University Graduate School of Medicine, Osaka, Japan.

Yoshihiro Oka (Y)

Department of Respiratory Medicine and Clinical Immunology, Osaka University Graduate School of Medicine, Osaka, Japan.
Department of Cancer Stem Cell Biology, Osaka University Graduate School of Medicine, Osaka, Japan.
Department of Immunopathology, WPI Immunology Frontier Research Center, Osaka University, Osaka, Japan.

Yusuke Oji (Y)

Department of Clinical Laboratory and Biomedical Sciences, Osaka University Graduate School of Medicine, Osaka, Japan.

Shinji Sogo (S)

Department of Cancer Immunology, Osaka University Graduate School of Medicine, 1-7 Yamada-oka, Suita, Osaka, 565-0871, Japan.
Immunology Research Unit, Department of Medical Innovations, Otsuka Pharmaceutical Co., Ltd., Tokushima, Japan.

Haruo Sugiyama (H)

Department of Cancer Immunology, Osaka University Graduate School of Medicine, 1-7 Yamada-oka, Suita, Osaka, 565-0871, Japan.

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questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Leucocytes › Agranulocytes › Lymphocytes › Lymphocytes T › Sous-populations de lymphocytes T › Lymphocytes T auxiliaires › Identification of two distinct populations of...
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questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines tumorales › Protéines suppresseurs de tumeurs › Protéines WT1 › Identification of two distinct populations of...