Ectonucleotidase CD39 is highly expressed on ATLL cells and is responsible for their immunosuppressive function.


Journal

Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895

Informations de publication

Date de publication:
01 2021
Historique:
received: 15 12 2019
accepted: 24 02 2020
revised: 09 02 2020
pubmed: 24 3 2020
medline: 14 1 2021
entrez: 24 3 2020
Statut: ppublish

Résumé

Adult T-cell leukemia/lymphoma (ATLL) patients have an extremely poor prognosis, partly due to their immunosuppressive state. The majority of ATLL patients have leukemic cells with phenotype similar to Tregs, prompting suggestions that ATLL cells themselves have immunosuppressive functions. In this study, we detected CD39 expression on ATLL cells, particularly frequent on aggressive subtypes. CD39 and CD73 convert extracellular adenosine triphosphate (ATP) into adenosine, a key player in Tregs' immunosuppression. In vitro culture, both CD39

Identifiants

pubmed: 32203145
doi: 10.1038/s41375-020-0788-y
pii: 10.1038/s41375-020-0788-y
pmc: PMC7787980
doi:

Substances chimiques

Antigens, CD 0
Biomarkers 0
Adenosine Triphosphate 8L70Q75FXE
Apyrase EC 3.6.1.5
CD39 antigen EC 3.6.1.5

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

107-118

Références

Uchiyama T, Yodoi J, Sagawa K, Takatsuki K, Uchino H. Adult T-cell leukemia: clinical and hematologic features of 16 cases. Blood. 1977;50:481–92.
pubmed: 301762 doi: 10.1182/blood.V50.3.481.481
Takatsuki K. Discovery of adult T-cell leukemia. Retrovirology. 2005;2:16.
pubmed: 15743528 pmcid: 555581 doi: 10.1186/1742-4690-2-16
Kawano N, Yoshida S, Kuriyama T, Tahara Y, Yamashita K, Nagahiro Y, et al. Clinical features and treatment outcomes of 81 patients with aggressive type adult T-cell leukemia-lymphoma at a single institution over a 7-year period (2006–12). Intern Med. 2015;54:1489–98.
pubmed: 26073237 doi: 10.2169/internalmedicine.54.1953
Shimoyama M. Diagnostic criteria and classification of clinical subtypes of adult T‐cell leukaemia‐lymphoma: a report from the Lymphoma Study Group (1984–87). Br J Haematol. 1991;79:428–37.
pubmed: 1751370 doi: 10.1111/j.1365-2141.1991.tb08051.x
Nasr R, Marçais A, Hermine O, Bazarbachi A. Overview of targeted therapies for adult T-cell leukemia/lymphoma. Methods Mol Biol. 2017;1582:197–216.
pubmed: 28357672 doi: 10.1007/978-1-4939-6872-5_15
Ogata M, Satou T, Kawano R, Yoshikawa T, Ikewaki J, Kohno K, et al. High incidence of cytomegalovirus, human herpesvirus-6, and Epstein-Barr virus reactivation in patients receiving cytotoxic chemotherapy for Adult T cell leukemia. J Med Virol. 2011;83:702–9.
pubmed: 21328386 doi: 10.1002/jmv.22013
Satou Y, Utsunomiya A, Tanabe J, Nakagawa M, Nosaka K, Matsuoka M. HTLV-1 modulates the frequency and phenotype of FoxP3+CD4+ T cells in virus-infected individuals. Retrovirology. 2012;9:46.
pubmed: 22647666 pmcid: 3403885 doi: 10.1186/1742-4690-9-46
Karube K, Ohshima K, Tsuchiya T, Yamaguchi T, Kawano R, Suzumiya J, et al. Expression of FoxP3, a key molecule in CD4+CD25+ regulatory T cells, in adult T-cell leukaemia/lymphoma cells. Br J Haematol. 2004;126:81–84.
pubmed: 15198736 doi: 10.1111/j.1365-2141.2004.04999.x
Chen S, Ishii N, Ine S, Ikeda S, Fujimura T, Ndhlovu LC, et al. Regulatory T cell-like activity of Foxp3+ adult T cell leukemia cells. Int Immunol. 2005;18:269–77.
pubmed: 16361311 doi: 10.1093/intimm/dxh366
Yano H, Ishida T, Inagaki A, Ishii T, Kusumoto S, Komatsu H, et al. Regulatory T-cell function of adult T-cell leukemia/lymphoma cells. Int J Cancer. 2007;120:2052–7.
pubmed: 17278106 doi: 10.1002/ijc.22536
Shimauchi T, Kabashima K, Tokura Y. Adult T-cell leukemia/lymphoma cells from blood and skin tumors express cytotoxic T lymphocyte-associated antigen-4 and Foxp3 but lack suppressor activity toward autologous CD8
pubmed: 17970785
Toulza F, Nosaka K, Takiguchi M, Pagliuca T, Mitsuya H, Tanaka Y, et al. FoxP3
pubmed: 19544530 doi: 10.1002/ijc.24664
Miyara M, Yoshioka Y, Kitoh A, Shima T, Wing K, Niwa A, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity. 2009;30:899–911.
pubmed: 19464196 doi: 10.1016/j.immuni.2009.03.019
Karube K, Aoki R, Sugita Y, Yoshida S, Nomura Y, Shimizu K, et al. The relationship of FOXP3 expression and clinicopathological characteristics in adult T-cell leukemia/lymphoma. Mod Pathol. 2008;21:617–25.
pubmed: 18246047 doi: 10.1038/modpathol.2008.25
Ghezeldasht SA, Sadeghian H, Azarpazhooh MR, Shamsian SAA, Rafatpanah H, Mahmoodi M, et al. Evaluation of T regulatory lymphocytes transcription factors in HTLV-1-associated myelopathy/tropical spastic paraparesis (HAM/TSP) patients. Appl Biochem Biotechnol. 2017;182:1403–14.
pubmed: 28101786 doi: 10.1007/s12010-017-2406-7
Pulte D, Furman RR, Broekman MJ, Drosopoulos JHF, Ballard HS, Olson KE, et al. CD39 expression on T lymphocytes correlates with severity of disease in patients with chronic lymphocytic leukemia. Clin Lymphoma Myeloma Leuk. 2011;11:367–72.
pubmed: 21816376 pmcid: 3590911 doi: 10.1016/j.clml.2011.06.005
Cai XY, Wang XF, Li J, Dong JN, Liu JQ, Li NP, et al. High expression of CD39 in gastric cancer reduces patient outcome following radical resection. Oncol Lett. 2016;12:4080–6.
pubmed: 27895775 pmcid: 5104239 doi: 10.3892/ol.2016.5189
Sitkovsky M, Lukashev D, Deaglio S, Dwyer K, Robson SC, Ohta A. Adenosine A2A receptor antagonists: Blockade of adenosinergic effects and T regulatory cells. Br J Pharmacol. 2008;153:S457–464.
pubmed: 18311159 pmcid: 2268051 doi: 10.1038/bjp.2008.23
Mandapathil M, Hilldorfer B, Szczepanski MJ, Czystowska M, Szajnik M, Ren J, et al. Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+regulatory T Cells. J Biol Chem. 2010;285:7176–86.
pubmed: 19858205 doi: 10.1074/jbc.M109.047423
Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med. 2007;204:1257–65.
pubmed: 17502665 pmcid: 2118603 doi: 10.1084/jem.20062512
Kobie JJ, Shah PR, Yang L, Rebhahn JA, Fowell DJ, Mosmann TRT. Regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5’-adenosine monophosphate to adenosine. J Immunol. 2006;177:6780–6.
pubmed: 17082591 doi: 10.4049/jimmunol.177.10.6780
Borsellino G, Kleinewietfeld M, Di Mitri D, Sternjak A, Diamantini A, Giometto R, et al. Expression of ectonucleotidase CD39 by Foxp3+Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood. 2007;110:1225–32.
pubmed: 17449799 doi: 10.1182/blood-2006-12-064527
Doi Y, Yokota T, Satoh Y, Okuzaki D, Tokunaga M, Ishibashi T, et al. Variable SATB1 levels regulate hematopoietic stem cell heterogeneity with distinct lineage fate. Cell Rep. 2018;23:3223–35.
pubmed: 29898394 doi: 10.1016/j.celrep.2018.05.042
Kobayashi S, Nakano K, Watanabe E, Ishigaki T, Ohno N, Yuji K, et al. CADM1 expression and stepwise downregulation of CD7 are closely associated with clonal expansion of HTLV-I-infected cells in adult T-cell leukemia/lymphoma. Clin Cancer Res. 2014;20:2851–61.
pubmed: 24727323 doi: 10.1158/1078-0432.CCR-13-3169
Antonioli L, Blandizzi C, Pacher P, Haskó G. Immunity, inflammation and cancer: a leading role for adenosine. Nat Rev Cancer. 2013;13:842–57.
pubmed: 24226193 doi: 10.1038/nrc3613
Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 2004;10:942–9.
pubmed: 15322536 pmcid: 15322536 doi: 10.1038/nm1093
Yamaguchi T, Hirota K, Nagahama K, Ohkawa K, Takahashi T, Nomura T, et al. Control of immune responses by antigen-specific regulatory T cells expressing the folate receptor. Immunity. 2007;27:145–59.
pubmed: 17613255 doi: 10.1016/j.immuni.2007.04.017
Sugiyama D, Nishikawa H, Maeda Y, Nishioka M, Tanemura A, Katayama I, et al. Anti-CCR4 mAb selectively depletes effector-type FoxP3+CD4+ regulatory T cells, evoking antitumor immune responses in humans. Proc Natl Acad Sci. 2013;110:17945–51790.
pubmed: 24127572 doi: 10.1073/pnas.1316796110
Nishikawa H, Sakaguchi S. Regulatory T cells in tumor immunity. Int J Cancer. 2010;127:759–67.
pubmed: 20518016
Yasunaga JI, Sakai T, Nosaka K, Etoh KI, Tamiya S, Koga S, et al. Impaired production of naive T lymphocytes in human T-cell leukemia virus type I-infected individuals: its implications in the immunodeficient state. Blood. 2001;97:3177–83.
doi: 10.1182/blood.V97.10.3177
Uchiyama T. Human T cell leukemia virus type 1 (HTLV-1) and human diseases. Annu Rev Immunol. 1997;15:15–37.
pubmed: 9143680 doi: 10.1146/annurev.immunol.15.1.15
Watanabe T. Adult T-cell leukemia: molecular basis for clonal expansion and transformation of HTLV-1-infected T cells. Blood 2017;129:1071–81.
pubmed: 28115366 pmcid: 5374731 doi: 10.1182/blood-2016-09-692574
Tsukasaki K. Genetic instability of adult T-cell leukemia/lymphoma by comparative genomic hybridization analysis. J Clin Immunol. 2002;22:57–63.
pubmed: 11998893 doi: 10.1023/A:1014471500757
Airas L, Jalkanen S. CD73 mediates adhesion of B cells to follicular dendritic cells. Blood. 1996;88:1755–64.
pubmed: 8781432 doi: 10.1182/blood.V88.5.1755.1755
Schuler PJ, Saze Z, Hong CS, Muller L, Gillespie DG, Cheng D, et al. Human CD4+CD39+ regulatory T cells produce adenosine upon co-expression of surface CD73 or contact with CD73+ exosomes or CD73+ cells. Clin Exp Immunol. 2014;177:531–43.
pubmed: 24749746 pmcid: 4226604 doi: 10.1111/cei.12354
Abousamra NK, Salah El-Din M, Hamza Elzahaf E, Esmael ME. Ectonucleoside triphosphate diphosphohydrolase-1 (E-NTPDase1/CD39) as a new prognostic marker in chronic lymphocytic leukemia. Leuk Lymphoma. 2015;56:113–9.
pubmed: 24684231 doi: 10.3109/10428194.2014.907893
Dwyer KM, Hanidziar D, Putheti P, Hill PA, Pommey S, McRae JL, et al. Expression of CD39 by human peripheral blood CD4+CD25+T cells denotes a regulatory memory phenotype. Am J Transpl. 2010;10:2410–20.
doi: 10.1111/j.1600-6143.2010.03291.x
Zhang Y, Li L, Wang L, Li J, Fan Z, Yang L, et al. Metformin-induced reduction of CD39 and CD73 blocks myeloid-derived suppressor cell activity in patients with ovarian cancer. Cancer Res. 2018;78:1779–81.
pubmed: 29374065 pmcid: 5882589 doi: 10.1158/0008-5472.CAN-17-2460
Ogura M, Ishida T, Taniwaki M, Ando K, Tobinai K, Fujimoto K, et al. Multicenter phase II study of mogamulizumab (KW-0761), a defucosylated anti-CCR4 antibody, in patients with relapsed peripheral and cutaneous T-cell lymphoma and cutaneous T-cell lymphoma. J Clin Oncol. 2014;32:1157–63.
pubmed: 24616310 doi: 10.1200/JCO.2013.52.0924
Yamamoto K, Utsunomiya A, Tobinai K, Tsukasaki K, Uike N, Uozumi K, et al. Phase I study of KW-0761, a defucosylated humanized anti-CCR4 antibody, in relapsed patients with adult T-cell leukemia-lymphoma and peripheral T-cell lymphoma. J Clin Oncol. 2010;28:1591–8.
pubmed: 20177026 doi: 10.1200/JCO.2009.25.3575

Auteurs

Yasuhiro Nagate (Y)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Sachiko Ezoe (S)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan. sezoe@bldon.med.osaka-u.ac.jp.
Department of Environmental Space Infection Control, Osaka University Graduate School of Medicine, Suita, Japan. sezoe@bldon.med.osaka-u.ac.jp.

Jiro Fujita (J)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Daisuke Okuzaki (D)

Genome Information Research Center, Research Institute for Microbial Diseases, Osaka University, Suita, Japan.

Daisuke Motooka (D)

Genome Information Research Center, Research Institute for Microbial Diseases, Osaka University, Suita, Japan.

Tomohiko Ishibashi (T)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.
Department of Vascular Physiology, National Cerebral and Cardiovascular Center Research Institute, Suita, Japan.

Michiko Ichii (M)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Akira Tanimura (A)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Masako Kurashige (M)

Department of Pathology, Osaka University Graduate School of Medicine, Osaka University, Suita, Japan.

Eiichi Morii (E)

Department of Pathology, Osaka University Graduate School of Medicine, Osaka University, Suita, Japan.

Takuya Fukushima (T)

Laboratory of Hematoimmunology, School of Health Sciences, Faculty of Medicine, University of the Ryukyus, Nishihara, Japan.

Youko Suehiro (Y)

Department of Hematology, National Kyushu Cancer, Fukuoka, Japan.

Takafumi Yokota (T)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Hirohiko Shibayama (H)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Kenji Oritani (K)

Department of Hematology, Graduate School of Medical Sciences, International University of Health and Welfare Hospital, Narita, Japan.

Yuzuru Kanakura (Y)

Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C

Classifications MeSH