Assessment of ATP metabolism to adenosine by ecto-nucleotidases carried by tumor-derived small extracellular vesicles.

Derived High pressure liquid chromatography N6-etheno-ADP N6-etheno-AMP N6-etheno-ATP N6-etheno-adenosine Small extracellular Tumor Vesicles

Journal

Purinergic signalling
ISSN: 1573-9546
Titre abrégé: Purinergic Signal
Pays: Netherlands
ID NLM: 101250499

Informations de publication

Date de publication:
27 Jul 2024
Historique:
received: 18 01 2024
accepted: 04 07 2024
medline: 28 7 2024
pubmed: 28 7 2024
entrez: 27 7 2024
Statut: aheadofprint

Résumé

Immunosuppression is a hallmark of cancer progression. Tumor-derived small extracellular vesicles (sEV), also known as TEX, produce adenosine (ADO) and can mediate tumor-induced immunosuppression.Here, the ATP pathway of ADO production (ATP

Identifiants

pubmed: 39066830
doi: 10.1007/s11302-024-10038-7
pii: 10.1007/s11302-024-10038-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIH HHS
ID : R01-CA 256068
Pays : United States
Organisme : NIH HHS
ID : UO1-DE029759
Pays : United States

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674. https://doi.org/10.1016/j.cell.2011.02.013
doi: 10.1016/j.cell.2011.02.013 pubmed: 21376230
Czystowska-Kuzmicz M, Whiteside TL (2021) The potential role of tumor-derived exosomes in diagnosis, prognosis, and response to therapy in cancer. Expert Opin Biol Ther 21:241–258. https://doi.org/10.1080/14712598.2020.1813276
doi: 10.1080/14712598.2020.1813276 pubmed: 32813990
Olejarz W, Dominiak A, Zolnierzak A, Kubiak-Tomaszewska G, Lorenc T (2020) Tumor-derived exosomes in immunosuppression and immunotherapy. J Immunol Res 2020:6272498. https://doi.org/10.1155/2020/6272498
doi: 10.1155/2020/6272498 pubmed: 32537468 pmcid: 7261328
Whiteside TL (2017) Exosomes in cancer: another mechanism of tumor-induced immune suppression. Adv Exp Med Biol 1036:81–89. https://doi.org/10.1007/978-3-319-67577-0_6
doi: 10.1007/978-3-319-67577-0_6 pubmed: 29275466
Abels ER, Breakefield XO (2016) Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol 36:301–312. https://doi.org/10.1007/s10571-016-0366-z
doi: 10.1007/s10571-016-0366-z pubmed: 27053351 pmcid: 5546313
Kalluri R, LeBleu VS (2020) The biology, function, and biomedical applications of exosomes. 367. https://doi.org/10.1126/science.aau6977
Hurwitz SN (2016) Proteomic profiling of NCI-60 extracellular vesicles uncovers common protein cargo and cancer type-specific biomarkers. Oncotarget 7:86999–87015. https://doi.org/10.18632/oncotarget.13569
doi: 10.18632/oncotarget.13569 pubmed: 27894104 pmcid: 5341331
Maas SLN, Breakefield XO, Weaver AM (2017) Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol 27:172–188. https://doi.org/10.1016/j.tcb.2016.11.003
doi: 10.1016/j.tcb.2016.11.003 pubmed: 27979573
Atay S, Godwin AK (2014) Tumor-derived exosomes: a message delivery system for tumor progression. Commun Integr Biol 7:e28231. https://doi.org/10.4161/cib.28231
doi: 10.4161/cib.28231 pubmed: 24778765 pmcid: 3995727
Ludwig N, Yerneni SS, Razzo BM, Whiteside TL (2018) Exosomes from HNSCC promote angiogenesis through reprogramming of endothelial cells. Mol Cancer Res 16:1798–1808. https://doi.org/10.1158/1541-7786.MCR-18-0358
doi: 10.1158/1541-7786.MCR-18-0358 pubmed: 30042174
Crow J, Samuel G, Godwin AK (2019) Beyond tumor mutational burden: potential and limitations in using exosomes to predict response to immunotherapy. Expert Rev Mol Diagn 19:1079–1088. https://doi.org/10.1080/14737159.2020.1688144
doi: 10.1080/14737159.2020.1688144 pubmed: 31687863
Whiteside TL (2023) Evaluating tumor cell- and T cell-derived extracellular vesicles as potential biomarkers of cancer and immune cell competence. Expert Rev Mol Diagn 23:109–122. https://doi.org/10.1080/14737159.2023.2178902
doi: 10.1080/14737159.2023.2178902 pubmed: 36787282 pmcid: 9998373
Peinado H (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18:883–891. https://doi.org/10.1038/nm.2753
doi: 10.1038/nm.2753 pubmed: 22635005 pmcid: 3645291
Razzo BM (2020) Tumor-derived exosomes promote carcinogenesis of murine oral squamous cell carcinoma. Carcinogenesis 41:625–633. https://doi.org/10.1093/carcin/bgz124
doi: 10.1093/carcin/bgz124 pubmed: 31245809
Whiteside TL, Diergaarde B, Hong CS (2021) Tumor-derived exosomes (TEX) and their role in immuno-oncology. Int J Mol Sci 22:6234. https://doi.org/10.3390/ijms22126234
doi: 10.3390/ijms22126234 pubmed: 34207762 pmcid: 8229953
Azambuja JH, Ludwig N, Yerneni SS, Braganhol E, Whiteside TL (2020) Arginase-1+ exosomes from reprogrammed macrophages promote glioblastoma progression. Int J Mol Sci 21:3990. https://doi.org/10.3390/ijms21113990
doi: 10.3390/ijms21113990 pubmed: 32498400 pmcid: 7312363
Whiteside TL (2018) Exosome and mesenchymal stem cell cross-talk in the tumor microenvironment. Semin Immunol 35:69–79. https://doi.org/10.1016/j.smim.2017.12.003
doi: 10.1016/j.smim.2017.12.003 pubmed: 29289420
Barbato S, Solaini G, Fabbri M (2017) MicroRNAs in oncogenesis and tumor suppression. Int Rev Cell Mol Biol 333:229–268. https://doi.org/10.1016/bs.ircmb.2017.05.001
doi: 10.1016/bs.ircmb.2017.05.001 pubmed: 28729026
Zebrowska A, Widlak P, Whiteside T, Pietrowska M (2020) Signaling of tumor-derived sEV impacts melanoma progression. Int J Mol Sci 21:5066. https://doi.org/10.3390/ijms21145066
doi: 10.3390/ijms21145066 pubmed: 32709086 pmcid: 7404104
Clayton A, Al-Taei S, Webber J, Mason MD, Tabi Z (2011) Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J Immunol 187:676–683. https://doi.org/10.4049/jimmunol.1003884
doi: 10.4049/jimmunol.1003884 pubmed: 21677139
Schuler PJ (2014) 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 177:531–543. https://doi.org/10.1111/cei.12354
doi: 10.1111/cei.12354 pubmed: 24749746 pmcid: 4226604
Ludwig N (2020) Tumor-derived exosomes promote angiogenesis via adenosine A(2B) receptor signaling. Angiogenesis 23:599–610. https://doi.org/10.1007/s10456-020-09728-8
doi: 10.1007/s10456-020-09728-8 pubmed: 32419057 pmcid: 7529853
Ludwig N, Gillespie DG, Reichert TE, Jackson EK, Whiteside TL (2020) Purine metabolites in tumor-derived Exosomes may facilitate immune escape of head and neck squamous cell carcinoma. Cancers 12:1602. https://doi.org/10.3390/cancers12061602
doi: 10.3390/cancers12061602 pubmed: 32560461 pmcid: 7352909
Ohta A (2006) A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad. Sci 103:13132–13137. https://doi.org/10.1073/pnas.0605251103
doi: 10.1073/pnas.0605251103 pubmed: 16916931 pmcid: 1559765
Jackson EK, Gillespie DG, Cheng D, Mi Z, Menshikova EV (2020) Characterization of the N(6)-etheno-bridge method to assess extracellular metabolism of adenine nucleotides: detection of a possible role for purine nucleoside phosphorylase in adenosine metabolism. Purinergic Signalling 16:187–211. https://doi.org/10.1007/s11302-020-09699-x
doi: 10.1007/s11302-020-09699-x pubmed: 32367441 pmcid: 7367995
Ludwig N (2019) Isolation and analysis of tumor-derived exosomes. Curr Protoc Immunol 127:e91. https://doi.org/10.1002/cpim.91
doi: 10.1002/cpim.91 pubmed: 31763776 pmcid: 6880756
Hong CS, Funk S, Muller L, Boyiadzis M, Whiteside TL (2016) Isolation of biologically active and morphologically intact exosomes from plasma of patients with cancer. J Extracell Vesicles 5:29289. https://doi.org/10.3402/jev.v5.29289
doi: 10.3402/jev.v5.29289 pubmed: 27018366
Sharma P, Diergaarde B, Ferrone S, Kirkwood JM, Whiteside TL (2020) Melanoma cell-derived exosomes in plasma of melanoma patients suppress functions of immune effector cells. Sci Rep 10:92. https://doi.org/10.1038/s41598-019-56542-4
doi: 10.1038/s41598-019-56542-4 pubmed: 31919420 pmcid: 6952363
Theodoraki MN, Hong CS, Donnenberg VS, Donnenberg AD, Whiteside TL (2021) Evaluation of exosome proteins by on-bead flow cytometry. Cytometry A 99:372–381. https://doi.org/10.1002/cyto.a.24193
doi: 10.1002/cyto.a.24193 pubmed: 33448645
Witwer KW (2021) Updating MISEV: Evolving the minimal requirements for studies of extracellular vesicles. J. Extracell. Vesicles 10:e12182. https://doi.org/10.1002/jev2.12182
doi: 10.1002/jev2.12182 pubmed: 34953156 pmcid: 8710080
Bhattarai S (2015) alpha, beta-Methylene-ADP (AOPCP) derivatives and analogues: development of potent and selective ecto-5’-nucleotidase (CD73) inhibitors. J Med Chem 58:6248–6263. https://doi.org/10.1021/acs.jmedchem.5b00802
doi: 10.1021/acs.jmedchem.5b00802 pubmed: 26147331
Lee SY (2015) Polyoxometalates–potent and selective ecto-nucleotidase inhibitors. Biochem Pharmacol 93:171–181. https://doi.org/10.1016/j.bcp.2014.11.002
doi: 10.1016/j.bcp.2014.11.002 pubmed: 25449596
Hajjar DP (1986) Regulation of neutral cholesteryl esterase in arterial smooth muscle cells: stimulation by agonists of adenylate cyclase and cyclic AMP-dependent protein kinase. Arch Biochem Biophys 247:49–56. https://doi.org/10.1016/0003-9861(86)90531-x
doi: 10.1016/0003-9861(86)90531-x pubmed: 3010880
Lazarowski ER (2004) Nucleotide release provides a mechanism for airway surface liquid homeostasis. J Biol Chem 279:36855–36864. https://doi.org/10.1074/jbc.M405367200
doi: 10.1074/jbc.M405367200 pubmed: 15210701
Levitt B, Head RJ, Westfall DP (1984) High-pressure liquid chromatographic-fluorometric detection of adenosine and adenine nucleotides: application to endogenous content and electrically induced release of adenyl purines in guinea pig vas deferens. Anal Biochem 137:93–100. https://doi.org/10.1016/0003-2697(84)90352-x
doi: 10.1016/0003-2697(84)90352-x pubmed: 6731811
Todorov LD (1997) Neuronal release of soluble nucleotidases and their role in neurotransmitter inactivation. Nature 387:76–79. https://doi.org/10.1038/387076a0
doi: 10.1038/387076a0 pubmed: 9139824
Yegutkin GG, Boison D (2022) ATP and adenosine metabolism in cancer: exploitation for therapeutic gain. Pharmacol Rev 74:797–822. https://doi.org/10.1124/pharmrev.121.000528
doi: 10.1124/pharmrev.121.000528 pubmed: 35738682

Auteurs

Chang-Sook Hong (CS)

Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15213, USA.
UPMC Hillman Cancer Center, UPCI Research Pavilion, Suite 1.27, 5117 Centre Avenue, Pittsburgh, PA, 15213, USA.

Elizabeth V Menshikova (EV)

Department of Pharmacology and Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Theresa L Whiteside (TL)

Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15213, USA. whitesidetl@upmc.edu.
UPMC Hillman Cancer Center, UPCI Research Pavilion, Suite 1.27, 5117 Centre Avenue, Pittsburgh, PA, 15213, USA. whitesidetl@upmc.edu.
Departments of Immunology and Otolaryngology, Pittsburgh, PA, 15213, USA. whitesidetl@upmc.edu.

Edwin K Jackson (EK)

Department of Pharmacology and Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Classifications MeSH