191
Views
0
CrossRef citations to date
0
Altmetric
Review

Adenosine pathway inhibitors: novel investigational agents for the treatment of metastatic breast cancer

, , , , , , , , , , , & show all
Pages 707-713 | Received 03 Feb 2022, Accepted 12 May 2022, Published online: 18 May 2022

References

  • Bergin ART, Loi S. Triple-negative breast cancer: recent treatment advances. F1000Res. 2019 Aug 2;8:F1000. Faculty Rev-1342. PMID: 31448088; PMCID: PMC6681627
  • da Silva Jl, Cardoso Nunes NC, Izetti P, et al. Triple negative breast cancer: a thorough review of biomarkers. Crit Rev Oncol Hematol. 2020Jan;145:102855. Epub 2019 Dec 20. PMID: 31927455
  • Gong J, Chehrazi-Raffle A, Reddi S, et al. Development of PD-1 and PD-L1 inhibitors as a form of cancer immunotherapy: a comprehensive review of registration trials and future considerations. J Immunother Cancer. 2018 Jan 23;6(1):8. PMID: 29357948; PMCID: PMC5778665.
  • Yang Y. Cancer immunotherapy: harnessing the immune system to battle cancer. J Clin Invest. 2015 Sep;125(9):3335–3337. Epub 2015 Sep 1. PMID: 26325031; PMCID: PMC4588312.
  • Kwapisz D. Pembrolizumab and atezolizumab in triple-negative breast cancer. Cancer Immunol Immunother. 2021 Mar;70(3):607–617. Epub 2020 Oct 5. PMID: 33015734.
  • Badve SS, Penault-Llorca F, Reis-Filho JS, et al. Determining PD-L1 status in patients with triple-negative breast cancer: lessons learned from impassion130. J Natl Cancer Inst. 2021 Jul 20;113(4):390–399. djab121. Epub ahead of print. PMID: 34286340.
  • Rozenblit M, Huang R, Danziger N, et al. Comparison of PD-L1 protein expression between primary tumors and metastatic lesions in triple negative breast cancers. J Immunother Cancer. 2020 Nov;8(2):e001558. PMID: 33239417; PMCID: PMC7689582.
  • Keenan TE, Tolaney SM. Role of immunotherapy in triple-negative breast cancer. J Natl Compr Canc Netw. 2020 Apr;18(4):479–489. PMID: 32259782.
  • Zong Y, Pegram M. Research advances and new challenges in overcoming triple-negative breast cancer. Cancer Drug Resist. 2021;4(3):517–542. Epub 2021 Apr 8. PMID: 34888495; PMCID: PMC8654168.
  • Rizzo A, Ricci AD, Lanotte L, et al. Immune-based combinations for metastatic triple negative breast cancer in clinical trials: current knowledge and therapeutic prospects. Expert Opin Investig Drugs. 2021 Dec; 13:1–9 Epub ahead of print. PMID: 34802383
  • Adams E, Wildiers H, Neven P, et al. Sacituzumab govitecan and trastuzumab deruxtecan: two new antibody-drug conjugates in the breast cancer treatment landscape. ESMO Open. 2021 Aug;6(4):100204. Epub 2021 Jul 2. PMID: 34225076; PMCID: PMC8259232.
  • Vijayan D, Young A, Teng MWL, et al. Targeting immunosuppressive adenosine in cancer. Nat Rev Cancer. 2017 Dec 17; 12: 709–724. Epub 2017 Oct 23. Erratum in: Nat Rev Cancer. 2017 Nov 22;17 (12):765. PMID: 29059149.
  • Ferrante CJ, Pinhal-Enfield G, Elson G, et al. The adenosine-dependent angiogenic switch of macrophages to an M2-like phenotype is independent of interleukin-4 receptor alpha (IL-4Rα) signaling. Inflammation. 2013 Aug;36(4):921–931. PMID: 23504259; PMCID: PMC3710311.
  • Sidders B, Zhang P, Goodwin K, et al. Adenosine signaling is prognostic for cancer outcome and has predictive utility for immunotherapeutic response. Clin Cancer Res. 2020 May 1;26(9):2176–2187. Epub 2020 Jan 17. PMID: 31953314.
  • Ghalamfarsa G, Kazemi MH, Raoofi Mohseni S, et al. CD73 as a potential opportunity for cancer immunotherapy. Expert Opin Ther Targets. 2019 Feb;23(2):127–142. Epub 2018 Dec 26. PMID: 30556751.
  • Csóka B, Selmeczy Z, Koscsó B, et al. Adenosine promotes alternative macrophage activation via A2A and A2B receptors. FASEB J. 2012 Jan;26(1):376–386. Epub 2011 Sep 16. PMID: 21926236; PMCID: PMC3250237.
  • Whiteside TL. Targeting adenosine in cancer immunotherapy: a review of recent progress. Expert Rev Anticancer Ther. 2017 Jun;17(6):527–535. Epub 2017 Apr 27. PMID: 28399672; PMCID: PMC6702668.
  • Magagna I, Gourdin N, Kieffer Y, et al. CD73-Mediated immunosuppression is linked to a specific fibroblast population that paves the way for new therapy in breast cancer. Cancers (Basel). 2021 Nov 23;13(23):5878. PMID: 34884993; PMCID: PMC8657241.
  • Nikas IP, Paschou SA, Ryu HS. The role of nicotinamide in cancer chemoprevention and therapy. Biomolecules. 2020 Mar 20;10(3):477. PMID: 32245130; PMCID: PMC7175378.
  • Moesta AK, Li XY, Smyth MJ. Targeting CD39 in cancer. Nat Rev Immunol. 2020Dec;20(12):739–755. Epub 2020 Jul 29. PMID: 32728220.
  • Li XY, Moesta AK, Xiao C, et al. Targeting CD39 in cancer reveals an extracellular ATP- and inflammasome-driven tumor immunity. Cancer Discov. 2019Dec;9(12):1754–1773. Epub 2019 Nov 7. PMID: 31699796; PMCID: PMC6891207.
  • Lin X, Chai G, Wu Y, et al. RNA m6A methylation regulates the epithelial mesenchymal transition of cancer cells and translation of Snail. Nat Commun. 2019 May 6;10(1):2065. PMID: 31061416; PMCID: PMC6502834.
  • Beavis PA, Divisekera U, Paget C, et al. Blockade of A2A receptors potently suppresses the metastasis of CD73+ tumors. Proc Natl Acad Sci U S A. 2013 Sep 3;110(36):14711–14716. Epub 2013 Aug 20. PMID: 23964122; PMCID: PMC3767556.
  • Haskó G, Szabó C, Németh ZH, et al. Adenosine receptor agonists differentially regulate IL-10, TNF-alpha, and nitric oxide production in RAW 264.7 macrophages and in endotoxemic mice. J Immunol. 1996 Nov 15;157(10):4634–4640. PMID: 8906843.
  • Haskó G, Kuhel DG, Chen JF, et al. Adenosine inhibits IL-12 and TNF-[alpha] production via adenosine A2a receptor-dependent and independent mechanisms. FASEB J. 2000Oct;14(13):2065–2074. PMID: 11023991.
  • Kraehenbuehl L, Weng CH, Eghbali S, et al. Enhancing immunotherapy in cancer by targeting emerging immunomodulatory pathways. Nat Rev Clin Oncol. 2022Jan;19(1):37–50. Epub 2021 Sep 27. PMID: 34580473.
  • Giannone G, Ghisoni E, Genta S, et al. Immuno-metabolism and microenvironment in cancer: key players for immunotherapy. Int J Mol Sci. 2020 Jun 21;21(12):4414. PMID: 32575899; PMCID: PMC7352562.
  • Vaupel P, Multhoff G. Fatal alliance of hypoxia-/hif-1α-driven microenvironmental traits promoting cancer progression. Adv Exp Med Biol. 2020;1232:169–176. PMID: 31893407.
  • Zhou Z, Lv J, Yu H, et al. Mechanism of RNA modification N6-methyladenosine in human cancer. Mol Cancer. 2020 Jun 8;19(1):104. PMID: 32513173; PMCID: PMC7278081.
  • Allard B, Beavis PA, Darcy PK, et al. Immunosuppressive activities of adenosine in cancer. Curr Opin Pharmacol. 2016 Aug;29:7–16 Epub 2016 May 19. PMID: 27209048
  • Young A, Mittal D, Stagg J, et al. Targeting cancer-derived adenosine: new therapeutic approaches. Cancer Discov. 2014Aug;4(8):879–888. Epub 2014 Jul 17. PMID: 25035124.
  • Thompson EA, Powell JD. Inhibition of the adenosine pathway to potentiate cancer immunotherapy: potential for combinatorial approaches. Annu Rev Med. 2021 Jan 27;72(1):331–348. Epub 2020 Sep 9. PMID: 32903139; PMCID: PMC8074264.
  • Stagg J, Divisekera U, McLaughlin N, et al. Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci U S A. 2010 Jan 26;107(4):1547–1552. Epub 2010 Jan 4. PMID: 20080644; PMCID: PMC2824381.
  • Arab S, Alizadeh A, Asgharzade S. Tumor-resident adenosine-producing mesenchymal stem cells as a potential target for cancer treatment. Clin Exp Med. 2021 May;21(2):205–213. Epub 2021 Jan 23. PMID: 33484380.
  • Churov A, Zhulai G. Targeting adenosine and regulatory T cells in cancer immunotherapy. Hum Immunol. 2021 Apr;82(4):270–278. Epub 2021 Feb 18. PMID: 33610376.
  • Martinez-Marti A, Majem M, Barlesi F, et al. COAST: an open-label, randomised, phase II platform study of durvalumab alone or in combination with novel agents in patients with locally advanced, unresectable, stage III NSCLC. Ann Oncol. 2021;32(suppl_5):S1283–S1346.
  • Fong L, Hotson A, Powderly JD, et al. Adenosine 2A receptor blockade as an immunotherapy for treatment-refractory renal cell cancer. Cancer Discov. 2020 Jan;10 1:40–53. Epub 2019 Nov 15. PMID: 31732494; PMCID: PMC6954326
  • Sato H, Okonogi N, Nakano T. Rationale of combination of anti-PD-1/PD-L1 antibody therapy and radiotherapy for cancer treatment. Int J Clin Oncol. 2020 May;25(5):801–809. Epub 2020 Apr 3. PMID: 32246277; PMCID: PMC7192886.
  • Hatfield SM, Sitkovsky MV. Antihypoxic oxygenation agents with respiratory hyperoxia to improve cancer immunotherapy. J Clin Invest. 2020 Nov 2;130(11):5629–5637. PMID: 32870821; PMCID: PMC7598059.
  • Wilkins AC, Patin EC, Harrington KJ, et al. The immunological consequences of radiation-induced DNA damage. J Pathol. 2019 Apr;247(5):606–614. Epub 2019 Feb 15. PMID: 30632153.
  • Wennerberg E, Spada S, Rudqvist NP, et al. CD73 blockade promotes dendritic cell infiltration of irradiated tumors and tumor rejection. Cancer Immunol Res. 2020 Apr;8(4):465–478. Epub 2020 Feb 11. PMID: 32047024; PMCID: PMC7125001.
  • Caluwé A D, Buisseret L, Poortmans P, et al. Neo-CheckRay: radiation therapy and adenosine pathway blockade to increase benefit of immuno-chemotherapy in early stage luminal B breast cancer, a randomized phase II trial. BMC Cancer. 2021 Aug 6;21(1):899. PMID: 34362344; PMCID: PMC8343924.
  • Gao ZW, Dong K, Zhang HZ. The roles of CD73 in cancer. Biomed Res Int. 2014;2014:460654. Epub 2014 Jul 14. PMID: 25126561; PMCID: PMC4121992.
  • Allard D, Chrobak P, Allard B, et al. Targeting the CD73-adenosine axis in immuno-oncology. Immunol Lett. 2019 Jan; 205: 31–39 Epub 2018 May 24. PMID: 29758241
  • Allard B, Allard D, Buisseret L, et al. The adenosine pathway in immuno-oncology. Nat Rev Clin Oncol. 2020 Oct;17(10): 611–629. Epub 2020 Jun 8. Erratum in: Nat Rev Clin Oncol 2020 Jul 17. PMID: 32514148
  • de Araújo JB, Kerkhoff VV, de Oliveira Maciel SFV, et al. Targeting the purinergic pathway in breast cancer and its therapeutic applications. Purinergic Signal. 2021 Jun;17(2):179–200. Epub 2021 Feb 12. PMID: 33576905; PMCID: PMC7879595.
  • Eiger D, Maurer C, Brandao M, et al. First findings from SYNERGY, a phase I/II trial testing the addition of the anti-CD73 oleclumab (O) to the anti-PD-L1 durvalumab (D) and chemotherapy (ChT) as first line therapy for patients (pts) with metastatic triple-negative breast cancer (mTNBC). Ann Oncol. 2020;31(4):S386–S387.
  • Rizzo A, Ricci AD. Biomarkers for breast cancer immunotherapy: PD-L1, TILs, and beyond. Expert Opin Investig Drugs. 2021 Nov; 25: 1–7 Epub ahead of print. PMID: 34793275
  • Blackley EF, Loi S. Targeting immune pathways in breast cancer: review of the prognostic utility of TILs in early stage triple negative breast cancer (TNBC). Breast. 2019 Nov;48(1):S44–S48. PMID: 31839159.
  • Bou-Dargham MJ, Draughon S, Cantrell V, et al. Advancements in human breast cancer targeted therapy and immunotherapy. J Cancer. 2021 Oct 11;12(23):6949–6963. PMID: 34729098; PMCID: PMC8558657.
  • Beavis PA, Hatfield SM. Editorial overview: cancer 2020 current mechanistic insights into the hypoxia-adenosine-A2A adenosinergic immunosuppressive axis in cancer immunotherapies. Curr Opin Pharmacol. 2020 Aug;53:iii–v. PMID: 33183677
  • Allard D, Allard B, Gaudreau PO, et al. CD73-adenosine: a next-generation target in immuno-oncology. Immunotherapy. 2016 Feb;8(2):145–163. Epub 2016 Jan 25. PMID: 26808918.
  • Chen S, Wainwright DA, Wu JD, et al. CD73: an emerging checkpoint for cancer immunotherapy. Immunotherapy. 2019Aug;11(11):983–997. Epub 2019 Jun 21. PMID: 31223045; PMCID: PMC6609898.
  • Allard B, Pommey S, Smyth MJ, et al. Targeting CD73 enhances the antitumor activity of anti-PD-1 and anti-CTLA-4 mAbs. Clin Cancer Res. 2013 Oct 15;19(20):5626–5635. Epub 2013 Aug 27. PMID: 23983257.
  • Deng WW, Li YC, Ma SR, et al. Specific blockade CD73 alters the “exhausted” phenotype of T cells in head and neck squamous cell carcinoma. Int J Cancer. 2018 Sep 15;143(6):1494–1504. PMID: 29663369.
  • Németh ZH, Lutz CS, Csóka B, et al. Adenosine augments IL-10 production by macrophages through an A2B receptor-mediated posttranscriptional mechanism. J Immunol. 2005 Dec 15;175(12):8260–8270. PMID: 16339566; PMCID: PMC2000336.
  • Alsaab HO, Sau S, Alzhrani R, et al. PD-1 and PD-L1 checkpoint signaling inhibition for cancer immunotherapy: mechanism, combinations, and clinical outcome. Front Pharmacol. 2017;8:561.
  • Sugie T. Immunotherapy for metastatic breast cancer. Chin Clin Oncol. 2018 Jun;7(3):28. PMID: 30056730.
  • Paver EC, Cooper WA, Colebatch AJ, et al. Programmed death ligand-1 (PD-L1) as a predictive marker for immunotherapy in solid tumours: a guide to immunohistochemistry implementation and interpretation. Pathology. 2021 Feb;53(2):141–156. Epub 2020 Dec 30. PMID: 33388161.
  • Rugo HS, Loi S, Adams S, et al. PD-L1 immunohistochemistry assay comparison in atezolizumab plus nab -paclitaxel–treated advanced triple-negative breast cancer. J Natl Cancer Inst. 2021 Jun 7;113(12):1733–1743. djab108. Epub ahead of print. PMID: 34097070
  • Winer EP, Lipatov O, Im SA, et al. KEYNOTE-119 investigators. pembrolizumab versus investigator-choice chemotherapy for metastatic triple-negative breast cancer (KEYNOTE-119): a randomised, open-label, phase 3 trial. Lancet Oncol. 2021 Apr;22(4):499–511. Epub 2021 Mar 4. PMID: 33676601.
  • Petruk N, Tuominen S, Åkerfelt M, et al. CD73 facilitates EMT progression and promotes lung metastases in triple-negative breast cancer. Sci Rep. 2021 Mar 16;11(1):6035. PMID: 33727591; PMCID: PMC7966763.
  • Boison D, Yegutkin GG. Adenosine metabolism: emerging concepts for cancer therapy. Cancer Cell. 2019 Dec 9;36(6):582–596. PMID: 31821783; PMCID: PMC7224341.
  • Antonioli L, Yegutkin GG, Pacher P, et al. Anti-CD73 in cancer immunotherapy: awakening new opportunities. Trends Cancer. 2016 Feb 1;2(2):95–109. PMID: 27014745; PMCID: PMC4800751.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.