Plasmatic exosomes from prostate cancer patients show increased carbonic anhydrase IX expression and activity and low pH

References

• Warburg O. On the origin of cancer cells. Science 1956;123:309–14.
   PubMed Web of Science ®Google Scholar
• Fais S, Venturi G, Gatenby B. Microenvironmental acidosis in carcinogenesis and metastases: new strategies in prevention and therapy. Cancer Metastas Rev 2014;33:1095–108.
   PubMed Web of Science ®Google Scholar
• Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004;4:891–9.
   PubMed Web of Science ®Google Scholar
• Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029–33.
   PubMed Web of Science ®Google Scholar
• Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer 2011;11:85–95.
   PubMed Web of Science ®Google Scholar
• Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77.
   PubMed Web of Science ®Google Scholar
• Gillies RJ, Brown JS, Anderson ARA, Gatenby RA. Eco-evolutionary causes and consequences of temporal changes in intratumoural blood flow. Nat Rev Cancer 2018;18:576–85.
   PubMed Web of Science ®Google Scholar
• Fais S, Fauvarque M-O. TM9 and cannibalism: how to learn more about cancer by studying amoebae and invertebrates. Trends Mol Med 2012;18:4–5.
   PubMed Web of Science ®Google Scholar
• Fais S. A non-mainstream approach against cancer. J Enzyme Inhib Med Chem 2016;31:882–9.
   PubMed Web of Science ®Google Scholar
• Fais S, Overholtzer M. Cell-in-cell phenomena in cancer. Nat Rev Cancer 2018;18:758–66.
   PubMed Web of Science ®Google Scholar
• Spugnini EP, Sonveaux P, Stock C, et al. Proton channels and exchangers in cancer. Biochim Biophys Acta BBA – Biomembr 2015;1848:2715–26.
   PubMed Web of Science ®Google Scholar
• Iessi E, Logozzi M, Mizzoni D, et al. Rethinking the combination of proton exchanger inhibitors in cancer therapy. Metabolites 2017;8:2.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Winum J-Y. Carbonic anhydrase IX inhibitors in cancer therapy: an update. Future Med Chem 2015;7:1407–14.
   PubMed Web of Science ®Google Scholar
• Federici C, Petrucci F, Caimi S, et al. Exosome release and low pH belong to a framework of resistance of human melanoma cells to cisplatin. PLoS One 2014;9:e88193.
   PubMed Web of Science ®Google Scholar
• Taylor S, Spugnini EP, Assaraf YG, et al. Microenvironment acidity as a major determinant of tumor chemoresistance: proton pump inhibitors (PPIs) as a novel therapeutic approach. Drug Resist Updat 2015;23:69–78.
   PubMed Web of Science ®Google Scholar
• Logozzi M, Angelini DF, Iessi E, et al. Increased PSA expression on prostate cancer exosomes in in vitro condition and in cancer patients. Cancer Lett 2017;403:318–29.
   PubMed Web of Science ®Google Scholar
• Logozzi M, Mizzoni D, Angelini D, et al. Microenvironmental pH and exosome levels interplay in human cancer cell lines of different histotypes. Cancers 2018;10:370.
   PubMed Web of Science ®Google Scholar
• Logozzi M, Spugnini E, Mizzoni D, et al. Extracellular acidity and increased exosome release as key phenotypes of malignant tumors. Cancer Metastasis Rev 2019;38:93–101.
   PubMed Web of Science ®Google Scholar
• Valadi H, Ekström K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654–9.
   PubMed Web of Science ®Google Scholar
• Camussi G, Deregibus M-C, Bruno S, et al. Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am J Cancer Res 2011;1:98–110.
   PubMed Web of Science ®Google Scholar
• Nolte’tHoen ENM, Buermans HPJ, Waasdorp M, et al. Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res 2012;40:9272–85.
   PubMed Web of Science ®Google Scholar
• Canitano A, Venturi G, Borghi M, et al. Exosomes released in vitro from Epstein–Barr virus (EBV)-infected cells contain EBV-encoded latent phase mRNAs. Cancer Lett 2013;337:193–9.
   PubMed Web of Science ®Google Scholar
• Zhao H, Achreja A, Iessi E, et al. The key role of extracellular vesicles in the metastatic process. Biochim Biophys Acta BBA - Rev Cancer 2018;1869:64–77.
   PubMed Web of Science ®Google Scholar
• Spugnini E, Logozzi M, Di Raimo R, et al. A role of tumor-released exosomes in paracrine dissemination and metastasis. Int J Mol Sci 2018;19:3968.
   Web of Science ®Google Scholar
• Iessi E, Logozzi M, Lugini L, et al. Acridine orange/exosomes increase the delivery and the effectiveness of acridine orange in human melanoma cells: a new prototype for theranostics of tumors. J Enzyme Inhib Med Chem 2017;32:648–57.
   PubMed Web of Science ®Google Scholar
• Kusuzaki K, Matsubara T, Murata H, et al. Natural extracellular nanovesicles and photodynamic molecules: is there a future for drug delivery? J Enzyme Inhib Med Chem 2017;32:908–16.
   PubMed Web of Science ®Google Scholar
• Parolini I, Federici C, Raggi C, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 2009;284:34211–22.
   PubMed Web of Science ®Google Scholar
• Logozzi M, De Milito A, Lugini L, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One 2009;4:e5219.
   PubMed Web of Science ®Google Scholar
• Rodríguez Zorrilla S, Pérez-Sayans M, Fais S, et al. A pilot clinical study on the prognostic relevance of plasmatic exosomes levels in oral squamous cell carcinoma patients. Cancers 2019;11:429.
   Web of Science ®Google Scholar
• Logozzi M, Capasso C, Di Raimo R, et al. Prostate cancer cells and exosomes in acidic condition show increased carbonic anhydrase IX expression and activity. J Enzyme Inhib Med Chem 2019;34:272–8.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:48.
   PubMed Web of Science ®Google Scholar
• Li Y, Dong M, Sheng W, Huang L. Roles of carbonic anhydrase IX in development of pancreatic cancer. Pathol Oncol Res 2016;22:277–86.
   PubMed Web of Science ®Google Scholar
• Ambrosio MR, Di Serio C, Danza G, et al. Carbonic anhydrase IX is a marker of hypoxia and correlates with higher Gleason scores and ISUP grading in prostate cancer. Diagn Pathol 2016;11:45.
   PubMed Web of Science ®Google Scholar
• Mahon BP, Bhatt A, Socorro L, et al. The structure of carbonic anhydrase IX is adapted for low-pH catalysis. Biochemistry 2016;55:4642–53.
   PubMed Web of Science ®Google Scholar
• Rosenberg V, Pastorekova S, Zatovicova M, et al. High serum carbonic anhydrase IX predicts shorter survival in head and neck cancer. Bratisl Lek Listy 2016;117:201–4.
   PubMed Web of Science ®Google Scholar
• Horie K, Kawakami K, Fujita Y, et al. Exosomes expressing carbonic anhydrase 9 promote angiogenesis. Biochem Biophys Res Commun 2017;492:356–61.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Alterio V, Di Fiore A, et al. Inhibition of carbonic anhydrase IX targets primary tumors, metastases, and cancer stem cells: three for the price of one. Med Res Rev 2018;38:1799–836.
   PubMed Web of Science ®Google Scholar
• Lucarini L, Magnelli L, Schiavone N, et al. Plasmatic carbonic anhydrase IX as a diagnostic marker for clear cell renal cell carcinoma. J Enzyme Inhib Med Chem 2018;33:234–40.
   PubMed Web of Science ®Google Scholar
• Cetin B, Gonul II, Gumusay O, et al. Carbonic anhydrase IX is a prognostic biomarker in glioblastoma multiforme: carbonic anhydrase IX and glioblastoma multiforme. Neuropathology 2018;38:457–62.
   PubMed Web of Science ®Google Scholar
• Lin C, Wong BCK, Chen H, et al. Pulmonary delivery of triptolide-loaded liposomes decorated with anti-carbonic anhydrase IX antibody for lung cancer therapy. Sci Rep 2017;7:2019–23.
   PubMed Web of Science ®Google Scholar
• Riemann A, Güttler A, Haupt V, et al. Inhibition of carbonic anhydrase IX by ureidosulfonamide inhibitor U104 reduces prostate cancer cell growth, but does not modulate daunorubicin or cisplatin cytotoxicity. Oncol Res Featur Preclin Clin Cancer Ther 2018;26:191–200.
   Google Scholar
• Hedlund EE, McDonald PC, Nemirovsky O, et al. Harnessing induced essentiality: targeting carbonic anhydrase IX and angiogenesis reduces lung metastasis of triple negative breast cancer xenografts. Cancers 2019;11:1002.
   PubMed Web of Science ®Google Scholar
• Benej M, Pastorekova S, Pastorek J, Carbonic anhydrase IX: regulation and role in cancer. In: Frost SC, McKenna R, editors. Carbonic anhydrase: mechanism, regulation, links to disease, and industrial applications. Vol. 75. Dordrecht: Springer Netherlands; 2014. p. 199–219.
   Google Scholar
• Andreucci E, Peppicelli S, Carta F, et al. Carbonic anhydrase IX inhibition affects viability of cancer cells adapted to extracellular acidosis. J Mol Med 2017;95:1341–53.
   PubMed Web of Science ®Google Scholar
• Caby M-P, Lankar D, Vincendeau-Scherrer C, et al. Exosomal-like vesicles are present in human blood plasma. Int Immunol 2005;17:879–87.
   PubMed Web of Science ®Google Scholar
• Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles 2018;7:1535750.
   PubMed Web of Science ®Google Scholar
• Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006;30:3.22.1–3.22.29.
   Google Scholar
• Pastoreková S, Závadová Z, Košťál M, et al. A novel quasi-viral agent, MaTu, is a two-component system. Virology 1992;187:620–6.
   PubMed Web of Science ®Google Scholar
• Logozzi M, Mizzoni D, Di Raimo R, et al. Oral administration of fermented papaya (FPP®) controls the growth of a murine melanoma through the in vivo induction of a natural antioxidant response. Cancers 2019;11:118.
   Web of Science ®Google Scholar
• Innocenti A, Pastorekova S, Pastorek J, et al. The proteoglycan region of the tumor-associated carbonic anhydrase isoform IX acts as anintrinsic buffer optimizing CO2 hydration at acidic pH values characteristic of solid tumors. Bioorg Med Chem Lett 2009;19:5825–8.
   PubMed Web of Science ®Google Scholar