The Potential of Liposomes with Carbonic Anhydrase IX to Deliver Anticancer Ingredients to Cancer Cells in Vivo
Abstract
:1. Introduction
2. The Development of Liposomal Therapeutics
3. Key Challenges of Liposomes for in Vivo Delivery of Anticancer Ingredients
4. The Rising of CA-IX as a Targeted Anticancer Drug Delivery System
4.1. Biochemical Structure of CA-ΙΧ
4.2. Functions of CA-ΙΧ in Tumour Tissue
4.3. Protein Expression of CA-ΙΧ
Carcinoma | HER2 Expression | CA-IX Expression |
---|---|---|
Bladder micropapillary carcinomas typical urothelial carcinoma | 15% of 61 [132] 9% of 100 [132] | N.D. 71% of 340 cases [133] |
Brain | N.D. | 97% of 112 cases [120] |
Breast | 18% of 1134 cases [129] | 30% of 740 cases [130] |
Cervix | 14% of 50 cases [134] | 82% of 221 cases [112] |
Colorectal | 4% of 51 cases [135] | 49% of 80 cases [113] |
Endometrial | 12% of 286 cases [136] | 89% of 92 cases [137] |
Gastric | 12% of 131 cases [138] | 48% of 42 cases [139] |
Gastroesophageal | 24% of 100 cases [138] | 49% of 39 cases [139] |
Head and neck | 7% f 57 cases [140] | 26% of 72 cases [141] |
Kidney clear cell renal cell carcinoma | Detected in normal tissue Rare [142] | 99% of 186 cases [143] |
Liver | N.D. | 30% of 69 cases [108] |
Lung | 13% of 563 cases [144] | 82% of 175 cases [103] |
Oral cavity | 1% of 196 cases [145] | 43% of 80 cases [122] |
Ovarian | 29% of 50 cases [146] | 18% of 205 cases [114] |
Prostate | 14% of 216 cases [147] | 0% of 59 cases [148] |
4.4. CA-ΙΧ-Targeted Therapeutic Approaches
4.5. Optimization of Antibody-Targeted Immunoliposomes
5. Immunoliposome
5.1. CA-ΙΧ-Targeted Immunoliposomes
5.2. Limitations of CA-IX-Targeted Immunoliposomes
6. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- GLOBOCAN 2012: Estimated cancer incidence, mortality and prevalence worldwide in 2012. Available online: http://globocan.iarc.fr/Default.aspx (accessed on 18 December 2014).
- Celia, C.; Trapasso, E.; Locatelli, M.; Navarra, M.; Ventura, C.A.; Wolfram, J.; Carafa, M.; Morittu, V.M.; Britti, D. Anticancer activity of liposomal bergamot essential oil (BEO) on human neuroblastoma cells. Colloids Surf. B Biointerfaces 2013, 112, 548–553. [Google Scholar] [CrossRef] [PubMed]
- Wolfram, J.; Suri, K.; Huang, Y.; Molinaro, R.; Borsoi, C.; Scott, B.; Boom, K.; Paolino, P.; Fresta, M.; Wan, J.; et al. Evaluation of anticancer activity of celastrol liposomes in prostate cancer cells. J. Microencapsul. 2014, 31, 501–507. [Google Scholar] [CrossRef]
- Cosco, D.; Bulotta, A.; Ventura, M.; Celia, C.; Calimeri, T.; Perri, G.; Paolino, D.; Costa, N.; Neri, P.; Tagliaferri, P.; et al. In vivo activity of gemcitabine-loaded PEGylated small unilamellar liposomes against pancreatic cancer. Cancer Chemother. Pharmacol. 2009, 64, 1009–1020. [Google Scholar] [CrossRef]
- Paolino, D.; Cosco, D.; Celano, M.; Moretti, S.; Puxeddu, E.; Russo, D.; Fresta, M. Gemcitabine-loaded biocompatible nanocapsules for the effective treatment of human cancer. Nanomedicine (Lond.) 2013, 8, 193–201. [Google Scholar] [CrossRef]
- Davis, M.E.; Chen, Z.G.; Shin, D.M. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat. Rev. Drug Discov. 2008, 7, 771–782. [Google Scholar] [CrossRef] [PubMed]
- Janoff, A.S. Liposomes: Rational Design; Marcel Dekker, Inc.: New York, NY, USA, 1999. [Google Scholar]
- Bangham, A.D.; Horne, R.W.; Glauert, A.M.; Dingle, J.T.; Lucy, J.A. Action of saponin on biological cell membranes. Nature 1962, 196, 952–955. [Google Scholar] [CrossRef] [PubMed]
- Horne, R.W.; Bangham, A.D.; Whittaker, V.P. Negatively stained lipoprotein membranes. Nature 1963, 200, 1340. [Google Scholar] [CrossRef] [PubMed]
- Bangham, A.D.; Horne, R.W. Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope. J. Mol. Biol. 1964, 8, 660–668. [Google Scholar] [CrossRef] [PubMed]
- Bangham, A.D.; Standish, M.M.; Weissmann, G. The action of steroids and streptolysin S on the permeability of phospholipid structures to cations. J. Mol. Biol. 1965, 13, 253–259. [Google Scholar] [CrossRef] [PubMed]
- Yashroy, R.C. Lamellar dispersion and phase separation of chloroplast membrane lipids by negative staining electron microscopy. J. Biosci. 1990, 15, 93–98. [Google Scholar] [CrossRef]
- MacNaught, A.D.; Wilkinson, A.R. Compendium of Chemical Terminology: IUPAC Recommendations, 2nd ed.; Blackwell Science: Oxford, UK, 1997. [Google Scholar]
- Feigenson, G. Phase behavior of lipid mixtures. Nat. Chem. Biol. 2006, 2, 560–563. [Google Scholar] [CrossRef] [PubMed]
- Wiggins, P. Role of water in some biological processes. Microbiol. Rev. 1990, 54, 432–449. [Google Scholar] [PubMed]
- Van Meer, G.; Voelker, D.R.; Feigenson, G.W. Membrane lipids: Where they are and how they behave. Nat. Rev. Mol. Cell Biol. 2008, 9, 112–124. [Google Scholar] [CrossRef] [PubMed]
- Hauser, H.; Gains, N. Spontaneous vesiculation of phospholipids: A simple and quick method of forming unilamellar vesicles. Proc. Natl. Acad. Sci. USA 1982, 79, 1683–1687. [Google Scholar] [CrossRef] [PubMed]
- Cullis, P.R. Liposomes by accident: Commentary. J. Liposome Res. 2000, 10, ix–xxiv. [Google Scholar] [CrossRef]
- Mayer, L.D.; Bally, M.B.; Cullis, P.R. Uptake of adriamycin into large unilamellar vesicles in response to a pH gradient. Biochim. Biophys. Acta Biomembr. 1986, 857, 123–126. [Google Scholar] [CrossRef]
- Barenholz, Y. Doxil®—The first FDA-approved nano-drug: Lessons learned. J. Control. Release 2012, 160, 117–134. [Google Scholar] [CrossRef] [PubMed]
- Celano, M.; Calvagno, M.G.; Bulotta, S.; Paolino, D.; Arturi, F.; Rotiroti, D.; Filetti, S.; Fresta, M.; Russo, D. Cytotoxic effects of Gemcitabine-loaded liposomes in human anaplastic thyroid carcinoma cells. BMC Cancer 2004, 4. [Google Scholar] [CrossRef] [Green Version]
- Calvagno, M.G.; Celia, C.; Paolino, D.; Cosco, D.; Iannone, M.; Castelli, F.; Filetti, S.; Fresta, M.; Russo, D. Effects of lipid composition and preparation conditions on physical-chemical properties, technological parameters and in vitro biological activity of gemcitabine-loaded liposomes. Curr. Drug Deliv. 2007, 4, 89–101. [Google Scholar] [CrossRef] [PubMed]
- Lasic, D.; Martin, F. Stealth Liposomes; CRC Press: Boca Raton, FL, USA, 1995. [Google Scholar]
- Parr, M.J.; Masin, D.; Cullis, P.R.; Bally, M.B. Accumulation of liposomal lipid and encapsulated doxorubicin in murine Lewis lung carcinoma: the lack of beneficial effects by coating liposomes with poly(ethylene glycol). J. Pharmacol. Exp. Ther. 1997, 280, 1319–1327. [Google Scholar] [PubMed]
- Nag, O.K.; Awasthi, V. Surface engineering of liposomes for stealth behavior. Pharmaceutics 2013, 5, 542–569. [Google Scholar] [CrossRef] [PubMed]
- Wong, B.C.; Zhang, H.; Qin, L.; Chen, H.; Fang, C.; Lu, A.; Yang, Z. Carbonic anhydrase IX-directed immunoliposomes for targeted drug delivery to human lung cancer cells in vitro. Drug Des. Dev. Ther. 2014, 8, 993–1001. [Google Scholar]
- Kirpotin, D.; Park, J.W.; Hong, K.; Zalipsky, S.; Li, W.L.; Carter, P.; Benz, C.C.; Papahadjopoulos, D. Sterically stabilized Anti-HER2 immunoliposomes: Design and targeting to human breast cancer cells in vitro. Biochemistry 1997, 36, 66–75. [Google Scholar] [CrossRef] [PubMed]
- Park, J.W.; Hong, K.L.; Kirpotin, D.B.; Colbern, G.; Shalaby, R.; Baselga, J.; Shao, Y.; Nielsen, U.B.; Marks, J.D.; Moore, D.; et al. Anti-HER2 immunoliposomes: Enhanced efficacy attributable to targeted delivery. Clin. Cancer Res. 2002, 8, 1172–1181. [Google Scholar]
- Brown, B.S.; Patanam, T.; Mobli, K.; Celia, C.; Zage, P.E.; Bean, A.J.; Tasciotti, E. Etoposide-loaded immunoliposomes as active targeting agents for GD2-positive malignancies. Cancer Biol. Ther. 2014, 15, 851–861. [Google Scholar] [CrossRef] [PubMed]
- Raju, A.; Muthu, M.S.; Feng, S.S. Trastuzumab-conjugated vitamin E TPGS liposomes for sustained and targeted delivery of docetaxel. Expert Opin. Drug Deliv. 2013, 10, 747–760. [Google Scholar] [CrossRef] [PubMed]
- Turk, M.J.; Waters, D.J.; Low, P.S. Folate-conjugated liposomes preferentially target macrophages associated with ovarian carcinoma. Cancer Lett. 2004, 213, 165–172. [Google Scholar] [CrossRef] [PubMed]
- Paolino, D.; Licciardi, M.; Celia, C.; Giammona, G.; Fresta, M.; Cavallaro, G. Folate-targeted supramolecular vesicular aggregates as a new frontier for effective anticancer treatment in in vivo model. Eur. J. Pharm. Biopharm. 2012, 82, 94–102. [Google Scholar] [CrossRef]
- Chen, C.W.; Lu, D.W.; Yeh, M.K.; Shiau, C.Y.; Chiang, C.H. Novel RGD-lipid conjugate-modified liposomes for enhancing siRNA delivery in human retinal pigment epithelial cells. Int. J. Nanomed. 2011, 6, 2567–2580. [Google Scholar] [CrossRef]
- Li, W.; Su, B.; Meng, S.Y.; Ju, L.X.; Yan, L.H.; Ding, Y.M.; Song, Y.; Zhou, W.; Li, H.Y.; Tang, L.; et al. RGD-targeted paramagnetic liposomes for early detection of tumor: In vitro and in vivo studies. Eur. J. Radiol. 2011, 80, 598–606. [Google Scholar] [CrossRef]
- Arias, J.L. Liposomes in drug delivery: A patent review (2007‒present). Expert Opin. Ther. Pat. 2013, 23, 1399–1414. [Google Scholar] [CrossRef]
- Kim, C.K.; Lim, S.J. Recent progress in drug delivery systems for anticancer agents. Arch. Pharm. Res. 2002, 25, 229–239. [Google Scholar] [PubMed]
- Zou, Y.Y.; Ling, Y.H.; Reddy, S.; Priebe, W.; Perezsoler, R. Effect of vesicle size and lipid composition on the in vivo tumor selectivity and toxicity of the non-cross-resistant anthracycline annamycin incorporated in liposomes. Int. J. Cancer 1995, 61, 666–671. [Google Scholar] [CrossRef] [PubMed]
- Harrington, K.J.; Rowlinson-Busza, G.; Uster, P.S.; Stewart, J.S. Pegylated liposome-encapsulated doxorubicin and cisplatin in the treatment of head and neck xenograft tumours. Cancer Chemother. Pharm. 2000, 46, 10–18. [Google Scholar] [CrossRef]
- Koller-Lucae, S.K.M.; Schott, H.; Schwendener, R.A. Low density lipoprotein and liposome mediated uptake and cytotoxic effect of N-4-octadecyl-1-β-D-arabinofuranosylcytosine in Daudi lymphoma cells. Br. J. Cancer 1999, 80, 1542–1549. [Google Scholar] [CrossRef]
- Forssen, E.A. The design and development of DaunoXome(R) for solid tumor targeting in vivo. Adv. Drug Deliv. Rev. 1997, 24, 133–150. [Google Scholar]
- Hong, R.L.; Tseng, Y.L. Phase I and pharmacokinetic study of a stable, polyethylene-glycolated liposomal doxorubicin in patients with solid tumors—The relation between pharmacokinetic property and toxicity. Cancer 2001, 91, 1826–1833. [Google Scholar] [CrossRef] [PubMed]
- Kim, C.K.; Han, J.H. Lymphatic delivery and pharmacokinetics of methotrexate after intramuscular injection of differently charged liposome-entrapped methotrexate to rats. J. Microencapsul. 1995, 12, 437–446. [Google Scholar] [CrossRef] [PubMed]
- Ceruti, M.; Crosasso, P.; Brusa, P.; Arpicco, S.; Dosio, F.; Cattel, L. Preparation, characterization, cytotoxicity and pharmacokinetics of liposomes containing water-soluble prodrugs of paclitaxel. J. Control. Release 2000, 63, 141–153. [Google Scholar] [CrossRef] [PubMed]
- Paolino, D.; Cosco, D.; Racanicchi, L.; Trapasso, E.; Celia, C.; Iannon, M.; Puxeddu, E.; Costante, G.; Filetti, S.; Russo, D.; et al. Gemcitabine-loaded PEGylated unilamellar liposomes vs GEMZAR: biodistribution, pharmacokinetic features and in vivo antitumor activity. J. Control. Release 2010, 144, 144–50. [Google Scholar] [PubMed]
- Dalla Pozza, E.; Lerda, C.; Costanzo, C.; Donadelli, M.; Dando, I.; Zoratti, E.; Scupoli, M.T.; Beghelli, S.; Scarpa, A.; Fattal, R.; et al. Targeting gemcitabine containing liposomes to CD44 expressing pancreatic adenocarcinoma cells causes an increase in the antitumoral activity. Biochim. Biophys. Acta Biomembr. 2013, 1828, 1396–1404. [Google Scholar] [CrossRef]
- Kanter, P.M.; Klaich, G.M.; Bullard, G.A.; King, J.M.; Bally, M.B.; Mayer, L.D. Liposome-encapsulated vincristine: Preclinical toxicologic and pharmacologic comparison with free vincristine and empty liposomes in mice, rats and dogs. AntiCancer Drugs 1994, 5, 579–590. [Google Scholar] [CrossRef]
- Hoarau, D.; Delmas, P.; David, S.; Roux, E.; Leroux, J.C. Novel long-circulating lipid nanocapsules. Pharm. Res. 2004, 21, 1783–1789. [Google Scholar] [CrossRef]
- Immordino, M.L.; Dosio, F.; Cattel, L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int. J. Nanomed. 2006, 1, 297–315. [Google Scholar] [CrossRef]
- Park, J.W. Liposome-based drug delivery in breast cancer treatment. Breast Cancer Res. 2002, 4, 95–99. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Allen, T.M.; Cullis, P.R. Liposomal drug delivery systems: From concept to clinical applications. Adv. Drug Deliv. Rev. 2013, 65, 36–48. [Google Scholar] [CrossRef] [PubMed]
- Solomon, R.; Gabizon, A.A. Clinical pharmacology of liposomal anthracyclines: Focus on pegylated liposomal doxorubicin. Clin. Lymphoma Myeloma 2008, 8, 21–32. [Google Scholar] [CrossRef] [PubMed]
- Rafiyath, S.M.; Rasul, M.; Lee, B.; Wei, G.; Lamba, G.; Liu, D. Comparison of safety and toxicity of liposomal doxorubicin vs. conventional anthracyclines: A meta-analysis. Exp. Hematol. Oncol. 2012, 1, 10. [Google Scholar] [CrossRef] [PubMed]
- Barrett-Lee, P.J.; Dixon, J.M.; Farrell, C.; Jones, A.; Leonard, R.; Murray, N.; Palmieri, C.; Plummer, C.J.; Stanley, A.; Verrill, M.W. Expert opinion on the use of anthracyclines in patients with advanced breast cancer at cardiac risk. Ann. Oncol. 2009, 20, 816–827. [Google Scholar] [CrossRef] [PubMed]
- Charrois, G.; Allen, T. Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer. Biochim. Biophys. Acta 2004, 1663, 167–177. [Google Scholar] [CrossRef]
- Laginha, K.M.; Verwoert, S.; Charrois, G.J.; Allen, T.M. Determination of doxorubicin levels in whole tumor and tumor nuclei in murine breast cancer tumors. Clin. Cancer Res. 2005, 11, 6944–6949. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.; Lu, A.; Wong, B.C.; Chen, X.; Bian, Z.; Zhao, Z; Huang, W.; Zhang, G.; Chen, H.; Xu, M. Effect of liposomes on the absorption of water-soluble active pharmaceutical ingredients via oral administration. Curr. Pharm. Des. 2013, 19, 6647–6654. [Google Scholar] [CrossRef] [PubMed]
- Patel, H.M. Serum opsonins and liposomes: Their interaction and opsonophagocytosis. Crit. Rev. Ther. Drug Carr. Syst. 1992, 9, 39–90. [Google Scholar]
- Juliano, R.L.; Stamp, D. The effect of particle size and charge on the clearance rates of liposomes and liposome encapsulated drugs. Biochem. Biophys. Res. Commun. 1975, 63, 651–688. [Google Scholar] [CrossRef] [PubMed]
- Ishida, T.; Harashima, H.; Kiwada, H. Liposome clearance. Biosci. Rep. 2002, 22, 197–224. [Google Scholar] [CrossRef] [PubMed]
- Liu, D.X.; Mori, A.; Huang, L. Role of liposome size and RES blockade in controlling biodistribution and tumor uptake of GM1-containing liposomes. Biochim. Biophys. Acta 1992, 1104, 95–101. [Google Scholar] [CrossRef]
- Mora, M.; Sagrista, M.L.; Trombetta, D.; Bonina, F.P.; de Pasquale, A.; Saija, A. Design and characterization of liposomes containing long-chain N-AcylPEs for brain delivery: Penetration of liposomes incorporating GM1 into the rat brain. Pharm. Res. 2002, 19, 1430–1438. [Google Scholar] [CrossRef] [PubMed]
- Caliceti, P.; Veronese, F.M. Pharmacokinetic and biodistribution properties of poly(ethylene glycol)-protein conjugates. Adv. Drug Deliv. Rev. 2003, 55, 1261–1277. [Google Scholar] [CrossRef] [PubMed]
- Monfardini, C.; Veronese, F.M. Stabilization of substances in circulation. Bioconjug. Chem. 1998, 9, 418–450. [Google Scholar]
- Allen, T.M.; Cheng, W.W.; Hare, J.I.; Laginha, K.M. Pharmacokinetics and pharmacodynamics of lipidic nano-particles in cancer. Anticancer Agents Med. Chem. 2006, 6, 513–523. [Google Scholar] [CrossRef] [PubMed]
- Dudley, A.C. Tumor endothelial cells. Cold Spring Harb. Perspect. Med. 2012, 2. [Google Scholar] [CrossRef]
- Chauhan, A.K.; Varma, A. A Textbook of Molecular Biotechnology 2009; I.K. Int. Publishing House Pvt. Ltd.: New Delhi, India, 2009. [Google Scholar]
- Bae, Y.H. Drug targeting and tumor heterogeneity. J. Control. Release 2009, 133, 2–3. [Google Scholar] [CrossRef] [PubMed]
- Sawant, R.R.; Torchilin, V.P. Torchilin, challenges in development of targeted liposomal therapeutics. AAPS J. 2012, 14, 303–315. [Google Scholar] [CrossRef]
- Soldati, T.; Schliwa, M. Powering membrane traffic in endocytosis and recycling. Nat. Rev. Mol. Cell Biol. 2006, 7, 897–908. [Google Scholar] [CrossRef] [PubMed]
- Higashi, N.; Yamauchi, M.; Okumura, Y.; Nakanishi, M.; Sunamoto, J. Fusion between Jurkat cell and PEO-lipid modified liposome. Biochim. Biophys. Acta 1996, 1285, 183–191. [Google Scholar] [CrossRef]
- Koshkaryev, A.; Sawant, R.; Deshpande, M.; Torchilin, V. Immunoconjugates and long circulating systems: Origins, current state of the art and future directions. Adv. Drug Deliv. Rev. 2013, 65, 24–35. [Google Scholar] [CrossRef] [PubMed]
- Murase, Y.; Asai, T.; Katanasaka, Y.; Sugiyama, T.; Shimizu, K.; Maeda, N.; Oku, N. A novel DDS strategy, “dual-targeting”, and its application for antineovascular therapy. Cancer Lett. 2010, 287, 165–171. [Google Scholar] [CrossRef]
- Jayaraman, M.; Ansell, S.M.; Mui, B.L.; Tam, Y.K.; Chen, J.; Du, X.; Butler, D.; Eltepu, L.; Matsuda, S.; Narayanannair, J.K.; et al. Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo. Angew. Chem. Int. Ed. Engl. 2012, 51, 8529–8533. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Nicol, F.; Szoka, F.C., Jr. GALA: A designed synthetic pH-responsive amphipathic peptide with applications in drug and gene delivery. Adv. Drug Deliv. Rev. 2004, 56, 967–985. [Google Scholar] [CrossRef] [PubMed]
- Pagano, R.E.; Weinstein, J.N. Interactions of liposomes with mammalian cells. Annu. Rev. Biophys. Bioeng. 1978, 7, 435–468. [Google Scholar] [CrossRef] [PubMed]
- Noble, G.T.; Stefanick, J.F.; Ashley, J.D.; Kiziltepe, T.; Bilgicer, B. Ligand-targeted liposome design: Challenges and fundamental considerations. Trends Biotechnol. 2014, 32, 32–45. [Google Scholar] [CrossRef]
- Heath, T.D.; Fraley, R.T.; Papahadjopoulos, D. Antibody targeting of liposomes: Cell specificity obtained by conjugation of F(ab')2 to vesicle surface. Science 1980, 210, 539–541. [Google Scholar] [CrossRef] [PubMed]
- Leserman, L.D.; Barbet, J.; Kourilsky, F.; Weinstein, J.N. Targeting to cells of fluorescent liposomes covalently coupled with monoclonal antibody or protein A. Nature 1980, 288, 602–604. [Google Scholar] [CrossRef] [PubMed]
- Liao, S.Y.; Lerman, M.I.; Stanbridge, E.J. Expression of transmembrane carbonic anhydrases, CAIX and CAXII, in human development. BMC Dev. Biol. 2009, 9. [Google Scholar] [CrossRef]
- Kondo, E.; Saito, K.; Tashiro, Y.; Kamide, K.; Uno, S.; Furuya, T.; Mashita, M.; Nakajima, K.; Tsumuraya, T.; Kobayashi, N.; et al. Tumour lineage-homing cell-penetrating peptides as anticancer molecular delivery systems. Nat. Commun. 2012. [Google Scholar] [CrossRef]
- McDonald, P.C.; Winum, J-Y.; Supuran, C.T.; Dedhar, S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 2012, 3, 84–97. [Google Scholar] [PubMed]
- Supuran, C.T. Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators. Nat. Rev. Drug Discov. 2008, 7, 168–181. [Google Scholar] [CrossRef] [PubMed]
- Chiche, J.; Ilc, K.; Laferriere, J.; Trottier, E.; Dayan, F.; Mazure, N.M.; Brahimi-Horn, M.C.; Pouysségur, J. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res. 2009, 69, 358–368. [Google Scholar] [CrossRef] [PubMed]
- Shin, H-J.; Rho, S.B.; Jung, D.C.; Han, I-O.; Oh, E-S.; Kim, J-Y. Carbonic anhydrase IX (CA9) modulates tumor-associated cell migration and invasion. J. Cell Sci. 2011, 124, 1077–1087. [Google Scholar] [CrossRef] [PubMed]
- Neri, D.; Supuran, C.T. Interfering with pH regulation in tumours as a therapeutic strategy. Nat. Rev. Drug Discov. 2011, 10, 767–777. [Google Scholar] [CrossRef] [PubMed]
- Olive, P.L.; Aquino-Parsons, C.; MacPhail, S.H.; Liao, S.Y.; Raleigh, J.A.; Lerman, M.I.; Stanbridge, E.G. Carbonic anhydrase 9 as an endogenous marker for hypoxic cells in cervical cancer. Cancer Res. 2001, 61, 8924–8929. [Google Scholar] [PubMed]
- Tureci, O.; Sahin, U.; Vollmar, E.; Siemer, S.; Gottert, E.; Seitz, G.; Parkkilal, A.K.; Shah, G.N.; Grubb, J.H.; Pfreundschuh, M. Human carbonic anhydrase XII: cDNA cloning, expression, and chromosomal localization of a carbonic anhydrase gene that is overexpressed in some renal cell cancers. Proc. Natl. Acad. Sci. USA 1998, 95, 7608–7613. [Google Scholar] [CrossRef] [PubMed]
- Pastorekova, S.; Zatovicova, M.; Pastorek, J. Cancer-associated carbonic anhydrases and their inhibition. Curr. Pharm. Des. 2008, 14, 685–698. [Google Scholar] [CrossRef] [PubMed]
- Opavsky, R.; Pastorekova, S.; Zelnik, V.; Gibadulinova, A.; Stanbridge, E.J.; Zavada, J.; Kettmannd, R.; Pastorek, J. HumanMN/CA9 gene, a novel member of the carbonic anhydrase family: Structure and exon to protein domain relationships. Genomics 1996, 33, 480–487. [Google Scholar] [CrossRef]
- De Simone, G.; Supuran, C.T. Carbonic anhydrase IX: Biochemical and crystallographic characterization of a novel antitumor target. Biochim. Biophy. Acta Proteins Proteomics 2010, 1804, 404–409. [Google Scholar] [CrossRef]
- Innocenti, A.; Pastorekova, S.; Pastorek, J.; Scozzafava, A.; de Simone, G.; Supuran, C.T. 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, 5825–5828. [Google Scholar] [CrossRef] [PubMed]
- Supuran, C.T. Carbonic anhydrase IX: A new drug target for designing diagnostic tools and antitumor agents. Hacettepe J. Biol. Chem. 2009, 37, 259–270. [Google Scholar]
- Swietach, P.; Hulikova, A.; Vaughan-Jones, R.D.; Harris, A.L. New insights into the physiological role of carbonic anhydrase IX in tumour pH regulation. Oncogene 2010, 29, 6509–6521. [Google Scholar] [CrossRef] [PubMed]
- Swietach, P.; Patiar, S.; Supuran, C.T.; Harris, A.L.; Vaughan-Jones, R.D. The role of carbonic anhydrase 9 in regulating extracellular and intracellular pH in three-dimensional tumor cell growths. J. Biol. Chem. 2009, 284, 20299–20310. [Google Scholar] [CrossRef] [PubMed]
- Saarnio, J.; Parkkila, S.; Parkkila, A.K.; Haukipuro, K.; Pastorekova, S.; Pastorek, J.; Kairaluoma, M.I.; Karttunen, T.J. Immunohistochemical study of colorectal tumors for expression of a novel transmembrane carbonic anhydrase, MN/CA IX, with potential value as a marker of cell proliferation. Am. J. Pathol. 1998, 153, 279–285. [Google Scholar] [CrossRef] [PubMed]
- Saarnio, J.; Parkkila, S.; Parkkila, A.K.; Waheed, A.; Casey, M.C.; Zhou, X.Y.; Kairaluoma, M.I.; Karttunen, T.T. Immunohistochemistry of carbonic anhydrase isozyme IX (MN/CA IX) in human gut reveals polarized expression in the epithelial cells with the highest proliferative capacity. J. Histochem. Cytochem. 1998, 46, 497–504. [Google Scholar] [CrossRef] [PubMed]
- Svastova, E.; Zilka, N.; Zat’ovicova, M.; Gibadulinova, A.; Ciampor, F.; Pastorek, J.; Pastoreková, S. Carbonic anhydrase IX reduces E-cadherin-mediated adhesion of MDCK cells via interaction with β-catenin. Exp. Cell Res. 2003, 290, 332–345. [Google Scholar] [CrossRef] [PubMed]
- Cianchi, F.; Vinci, M.C.; Supuran, C.T.; Peruzzi, B.; de Giuli, P.; Fasolis, G.; Perigli, G.; Pastorekova, S.; Papucci, L.; Pini, A.; et al. Selective inhibition of carbonic anhydrase IX decreases cell proliferation and induces ceramide-mediated apoptosis in human cancer cells. J. Pharmacol. Exp. Ther. 2010, 334, 710–719. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Rocken, C.; Hoffmann, J.; Kruger, S.; Lendecke, U.; Rocco, A.; Pastorekova, S.; Malfertheiner, P.; Ebert, M.P.A. Expression of carbonic anhydrase 9 at the invasion front of gastric cancers. Gut 2005, 54, 920–927. [Google Scholar] [CrossRef] [PubMed]
- Turner, J.R.; Odze, R.D.; Crum, C.P.; Resnick, M.B. MN antigen expression in normal, preneoplastic, and neoplastic esophagus: A clinicopathological study of a new cancer-associated biomarker. Hum. Pathol. 1997, 28, 740–744. [Google Scholar] [CrossRef] [PubMed]
- Ilie, M.; Mazure, N.M.; Hofman, V.; Ammadi, R.E.; Ortholan, C.; Bonnetaud, C.; Mouroux, J.; Pouysségur, J.; Hofman, P. High levels of carbonic anhydrase IX in tumour tissue and plasma are biomarkers of poor prognostic in patients with non-small cell lung cancer. Br. J. Cancer 2010, 102, 1627–1635. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.J.; Rabbani, Z.N.; Dewhirst, M.W.; Vujaskovic, Z.; Vollmer, R.T.; Schreiber, E.G.; Oosterwijk, E.; Kelley, M.J. Expression of HIF-1α, CA IX, VEGF, and MMP-9 in surgically resected non-small cell lung cancer. Lung Cancer 2005, 49, 325–335. [Google Scholar] [CrossRef] [PubMed]
- Swinson, D.E.B.; Jones, J.L.; Richardson, D.; Wykoff, C.; Turley, H.; Pastorek, J.; Taub, N.; Harris, A.L.; O’Byrne, K.J. Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-small-cell lung cancer. J. Clin. Oncol. 2003, 21, 473–482. [Google Scholar] [CrossRef] [PubMed]
- Chia, S.K.; Wykoff, C.C.; Watson, P.H.; Han, C.; Leek, R.D.; Pastorek, J.; Gatter, K.C.; Ratcliffe, P.; Harris, A.L. Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma. J. Clin. Oncol. 2001, 19, 3660–3668. [Google Scholar] [PubMed]
- Tan, E.Y.; Yan, M.; Campo, L.; Han, C.; Takano, E.; Turley, H.; Candiloro, I.; Pezzella, F.; Gatter, K.C.; Millar, E.K.A.; et al. The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy. Br. J. Cancer 2009, 100, 405–411. [Google Scholar] [CrossRef] [PubMed]
- Trastour, C.; Benizri, E.; Ettore, F.; Ramaioli, A.; Chamorey, E.; Pouyssegur, J.; Berra, E. HIF-1α and CA IX staining in invasive breast carcinomas: Prognosis and treatment outcome. Int. J. Cancer 2007, 120, 1451–1458. [Google Scholar] [CrossRef] [PubMed]
- Kockar, F.; Yildrim, H.; Sagkan, R.I.; Hagemann, C.; Soysal, Y.; Anacker, J.; Hamza, A.A.; Vordermark, D.; Flentje, A.; Said, H.M. Hypoxia and cytokines regulate carbonic anhydrase 9 expression in hepatocellular carcinoma cells in vitro. World J. Clin. Oncol. 2012, 3, 82–91. [Google Scholar] [CrossRef] [PubMed]
- Yu, S.-J.; Yoon, J.-H.; Lee, J.-H.; Myung, S.-J.; Jang, E.-S.; Kwak, M.-S.; Cho, E.-J.; Jang, J.-J.; Kim, Y.-J.; Lee, H.-S. Inhibition of hypoxia-inducible carbonic anhydrase-IX enhances hexokinase II inhibitor-induced hepatocellular carcinoma cell apoptosis. Acta Pharmacol. Sin. 2011, 32, 912–920. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.Y.; Shin, H.J.; Kim, T.H.; Cho, K.H.; Shin, K.H.; Kim, B.K.; Roh, J.W.; Lee, S.; Park, S.Y.; Hwang, Y.J.; et al. Tumor-associated carbonic anhydrases are linked to metastases in primary cervical cancer. J. Cancer Res. Clin. Oncol. 2006, 132, 302–308. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.; Shin, H.J.; Han, I.O.; Hong, E.K.; Park, S.Y.; Roh, J.W.; Shin, K.H.; Kim, T.H.; Kim, J.Y. Tumor carbonic anhydrase 9 expression is associated with the presence of lymph node metastases in uterine cervical cancer. Cancer Sci. 2007, 98, 329–333. [Google Scholar] [CrossRef] [PubMed]
- Loncaster, J.A.; Harris, A.L.; Davidson, S.E.; Logue, J.P.; Hunter, R.D.; Wycoff, C.C.; Pastorek, J.; Ratcliffe, P.J.; Stratford, I.J.; West, C.M.L. Carbonic anhydrase (CA IX) expression, a potential new intrinsic marker of hypoxia: Correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res. 2001, 61, 6394–6399. [Google Scholar] [PubMed]
- Woelber, L.; Kress, K.; Kersten, J.F.; Choschzick, M.; Kilic, E.; Herwig, U.; Lindner, C.; Schwarz, J.; Jaenicke; Mahner, F.S.; et al. Carbonic anhydrase IX in tumor tissue and sera of patients with primary cervical cancer. BMA Cancer 2011, 11. [Google Scholar] [CrossRef]
- Korkeila, E.; Talvinen, K.; Jaakkola, P.M.; Minn, H.; Syrjanen, K.; Sundstrom, J.; Pyrhönen, S. Expression of carbonic anhydrase IX suggests poor outcome in rectal cancer. Br. J. Cancer 2009, 100, 874–880. [Google Scholar] [CrossRef] [PubMed]
- Choschzick, M.; Oosterwijk, E.; Muller, V.; Woelber, L.; Simon, R.; Moch, H.; Tennstedt, P. Overexpression of carbonic anhydrase IX (CAIX) is an independent unfavorable prognostic marker in endometrioid ovarian cancer. Virchows Arch. 2011, 459, 193–200. [Google Scholar] [CrossRef] [PubMed]
- Hoskin, P.J.; Sibtain, A.; Daley, F.M.; Wilson, G.D. GLUTI and CAIX as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome of ARCON. Br. J. Cancer 2003, 89, 1290–1297. [Google Scholar] [CrossRef] [PubMed]
- De Schutter, H.; Landuyt, W.; Verbeken, E.; Goethals, L.; Hermans, R.; Nuyts, S. The prognostic value of the hypoxia markers CA IX and GLUT I and the cytokines VEGF and IL 6 in head and neck squamous cell carcinoma treated by radiotherapy chemotherapy. BMC Cancer 2005, 5. [Google Scholar] [CrossRef] [PubMed]
- Hoogsteen, I.J.; Marres, H.A.M.; Wijffels, K.; Rijken, P.; Peters, J.P.W.; van den Hoogen, F.J.A.; Oosterwijk, E.; van der Kogel, A.J.; Kaanders, J.H.A.M. Colocalization of carbonic anhydrase 9 expression and cell proliferation in human head and neck squamous cell carcinoma. Clin. Cancer Res. 2005, 11, 97–106. [Google Scholar] [PubMed]
- Koukourakis, M.I.; Bentzen, S.M.; Giatromanolaki, A.; Wilson, G.D.; Daley, F.M.; Saunders, M.I.; Dische, S.; Sivridis, E.; Harris, A.L. Endogenous markers of two separate, hypoxia response pathways (hypoxia inducible factor 2 α and carbonic anhydrase 9) are associated with radiotherapy failure in head and neck cancer patients recruited in the CHART randomized trial. J. Clin. Oncol. 2006, 24, 727–735. [Google Scholar] [CrossRef] [PubMed]
- Nordfors, K.; Haapasalo, J.; Korja, M.; Niemela, A.; Laine, J.; Parkkila, A.K.; Pastorekova, S.; Pastorek, J.; Waheed, A.; Sly, W.S.; et al. The tumour-associated carbonic anhydrases CA II, CA IX and CA XII in a group of medulloblastomas and supratentorial primitive neuroectodermal tumours: an association of CA IX with poor prognosis. BMC Cancer 2010, 10. [Google Scholar] [CrossRef]
- Proescholdt, M.A.; Mayer, C.; Kubitza, M.; Schubert, T.; Liao, S.Y.; Stanbridge, E.J.; Ivanov, S.; Oldfield, E.H.; Brawanski, A.; Merrill, M.J. Expression of hypoxia-inducible carbonic anhydrases in brain tumors. Neuro Oncol. 2005, 7, 465–475. [Google Scholar]
- Choi, S.W.; Kim, J.Y.; Park, J.Y.; Cha, I.H.; Kim, J.; Lee, S. Expression of carbonic anhydrase IX is associated with postoperative recurrence and poor prognosis in surgically treated oral squamous cell carcinomas. Hum. Pathol. 2008, 39, 1317–1322. [Google Scholar] [CrossRef]
- Eckert, A.W.; Lautner, M.H.W.; Schutze, A.; Bolte, K.; Bache, M.; Kappler, M.; Schubert, J.; Taubert, H.; Bilkenroth, U. Co-expression of Hif1 α and CAIX is associated with poor prognosis in oral squamous cell carcinoma patients. J. Oral Pathol. Med. 2010, 39, 313–317. [Google Scholar]
- Pastorekova, S.; Parkkila, S.; Parkkila, A.K.; Opavsky, R.; Zelnik, V.; Saarnio, J.; Pastorek, J. Carbonic anhydrase IX, MN/CA IX: Analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts. Gastroenterology 1997, 112, 398–408. [Google Scholar] [CrossRef] [PubMed]
- Gut, M.O.; Parkkila, S.; Vernerova, Z.; Rohde, E.; Zavada, J.; Hocker, M.; Pastorek, J.; Karttunen, T.; Gibadulinová, A.; Závadová, Z.; et al. Gastric hyperplasia in mice with targeted disruption of the carbonic anhydrase gene Car9. Gastroenterology 2002, 123, 1889–1903. [Google Scholar] [CrossRef] [PubMed]
- Leppilampi, M.; Karttunen, T.J.; Kivela, J.; Gut, M.O.; Pastorekova, S.; Pastorek, J.; Parkkila, S. Gastric pit cell hyperplasia and glandular atrophy in carbonic anhydrase IX knockout mice: studies on two strains C57/BL6 and BALB/C. Transgenic Res. 2005, 14, 655–663. [Google Scholar] [CrossRef] [PubMed]
- Wykoff, C.C.; Beasley, N.J.P.; Watson, P.H.; Turner, K.J.; Pastorek, J.; Sibtain, A.; Wilson, G.D.; Turley, H.; Talks, K.L.; Maxwell, P.H.; et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 2000, 60, 7075–7083. [Google Scholar]
- Helmlinger, G.; Yuan, F.; Dellian, M.; Jain, R.K. Interstitial pH and pO2 gradients in solid tumors in vivo: High-resolution measurements reveal a lack of correlation. Nat. Med. 1997, 3, 177–182. [Google Scholar] [CrossRef] [PubMed]
- Lendahl, U.; Lee, K.L.; Yang, H.; Poellinger, L. Generating specificity and diversity in the transcriptional response to hypoxia. Nat. Rev. Genet. 2009, 10, 821–832. [Google Scholar] [CrossRef]
- Triple-Negative Breast Cancer, 2014; National Cancer Institute: Rockville, MD, USA, 2014.
- Choi, J.; Kim, D.H.; Jung, W.H.; Koo, J.S. Metabolic interaction between cancer cells and stromal cells according to breast cancer molecular subtype. Breast Cancer Res. 2013, 15. [Google Scholar] [CrossRef]
- Ivanova, L.; Zandberga, E.; Silina, K.; Kalnina, Z.; Abols, A.; Endzelins, E.; Vendina, I.; Romanchikova, N.; Hegmane, A.; Trapencieris, P.; et al. Prognostic relevance of carbonic anhydrase IX expression is distinct in various subtypes of breast cancer and its silencing suppresses self-renewal capacity of breast cancer cells. Cancer Chemother. Pharmacol. 2014. [Google Scholar] [CrossRef]
- Schneider, S.A.; Sukov, W.R.; Frank, I.; Boorjian, S.A.; Costello, B.A.; Tarrell, R.F.; Thapa, P.; Thompson, R.H.; Tollefson, M.K.; Karnes, R.J.; et al. Outcome of patients with micropapillary urothelial carcinoma following radical cystectomy: ERBB2 (HER2) amplification identifies patients with poor outcome. Mod. Pathol. 2014, 27, 758–764. [Google Scholar] [CrossRef] [PubMed]
- Klatte, T.; Seligson, D.B.; Rao, J.Y.; Yu, H.; de Martino, M.; Kawaoka, K.; Wong, S.G.; Belldegrun, A.S.; Pantuck, A.J. Carbonic anhydrase IX in bladder cancer: A diagnostic, prognostic, and therapeutic molecular marker. Cancer 2009, 115, 1448–1458. [Google Scholar] [CrossRef] [PubMed]
- Mitra, A.B.; Murty, V.V.; Pratap, M.; Sodhani, P.; Chaganti, R.S. ERBB2 (HER2/neu) oncogene is frequently amplified in squamous cell carcinoma of the uterine cervix. Cancer Res. 1994, 54, 637–639. [Google Scholar] [PubMed]
- Pappas, A.; Lagoudianakis, E.; Seretis, C.; Tsiambas, E.; Koronakis, N.; Toutouzas, K.; Katergiannakis, V.; Manouras, A. Clinical role of HER-2/neu expression in colorectal cancer. J. BUON 2013, 18, 98–104. [Google Scholar] [PubMed]
- Fleming, G.F.; Sill, M.W.; Darcy, K.M.; McMeekin, D.S.; Thigpen, J.T.; Adler, L.M.; Berekg, J.S.; Chapmanh, J.A.; DiSilvestroi, P.A.; Horowitz, I.R.; et al. Phase II trial of trastuzumab in women with advanced or recurrent, HER2-positive endometrial carcinoma: A Gynecologic Oncology Group study. Gynecol. Oncol. 2010, 116, 15–20. [Google Scholar] [CrossRef] [PubMed]
- Sadlecki, P.; Bodnar, M.; Grabiec, M.; Marszalek, A.; Walentowicz, P. The role of Hypoxia-inducible factor-1α, glucose transporter-1, (GLUT-1) and carbon anhydrase IX in endometrial cancer patients. Biomed. Res. Int. 2014, 2014. doi:org/10.1155/2014/616850. [Google Scholar]
- Tanner, M.; Hollmen, M.; Junttila, T.T.; Kapanen, A.I.; Tommola, S.; Soini, Y.; Helin, H.; Salo, J.; Joensuu, H.; Sihvo, S.; et al. Amplification of HER-2 in gastric carcinoma: association with Topoisomerase IIα gene amplification, intestinal type, poor prognosis and sensitivity to trastuzumab. Ann. Oncol. 2005, 16, 273–278. [Google Scholar] [CrossRef] [PubMed]
- Driessen, A.; Landuyt, W.; Pastorekova, S.; Moons, J.; Goethals, L.; Haustermans, K.; Nafteux, P.; Penninckx, F.; Geboes, K.; Lerut, T.; et al. Expression of carbonic anhydrase IX (CA IX), a hypoxia-related protein, rather than ascular-endothelial growth factor (VEGF), a pro-angiogenic factor, correlates with an extremely poor prognosis in esophageal and gastric adenocarcinomas. Ann. Surg. 2006, 243, 334–340. [Google Scholar] [CrossRef] [PubMed]
- Ali, M.A.; Gunduz, M.; Gunduz, E.; Tamamura, R.; Beder, L.B.; Katase, N.; Hatipoglu, O.F.; Fukushima, K.; Yamanaka, N.; Shimizu, K. Expression and mutation analysis of her2 in head and neck squamous cell carcinoma. Cancer Investig. 2010, 28, 495–500. [Google Scholar] [CrossRef]
- Koukourakis, M.I.; Giatromanolaki, A.; Sivridis, E.; Simopoulos, K.; Pastorek, J.; Wykoff, C.C.; Gatter, K.C.; Harris, A.L. Hypoxia-regulated carbonic anhydrase-9 (CA9) relates to poor vascularization and resistance of squamous cell head and neck cancer to chemoradiotherapy. Clin. Cancer Res. 2001, 7, 3399–3403. [Google Scholar] [PubMed]
- Wang, H.; Liu, C.; Han, J.; Zhen, L.; Zhang, T.; He, X.; Xu, E.; Li, M. HER2 expression in renal cell carcinoma is rare and negatively correlated with that in normal renal tissue. Oncol. Lett. 2012, 4, 194–198. [Google Scholar] [PubMed]
- Genega, E.M. Carbonic anhydrase IX expression in renal neoplasms: Correlation with tumor type and grade. Am. J. Clin. Pathol. 2010, 134, 873–879. [Google Scholar] [CrossRef] [PubMed]
- Heinmoller, P.; Gross, C.; Beyser, K.; Schmidtgen, C.; Maass, G.; Rüschoff, J. Pedrocchi M HER2 status in non-small cell lung cancer: Results from patient screening for enrollment to a phase II study of herceptin. Clin. Cancer Res. 2003, 9, 5238–5243. [Google Scholar] [PubMed]
- Hanken, H.; Gaudin, R.; Grobe, A.; Fraederich, M.; Eichhorn, W.; Smeets, R.; Simon, R.; Sauter, G.; Grupp, H.; Izbicki, J.R. Her2 expression and gene amplification is rarely detectable in patients with oral squamous cell carcinomas. J. Oral Pathol. Med. 2014, 43, 304–308. [Google Scholar] [CrossRef] [PubMed]
- Lanitis, E.; Dangaj, D.; Hagemann, I.S.; Song, D.G.; Best, A.; Sandaltzopoulos, R.; George, C.; Daniel, J.P., Jr. Primary human ovarian epithelial cancer cells broadly express HER2 at immunologically-detectable levels. PLoS One 2012, 7, e49829. [Google Scholar] [CrossRef] [PubMed]
- Jorda, M.; Morales, A.; Ghorab, Z.; Fernandez, G.; Nadji, M.; Block, N. Her2 expression in prostatic cancer: A comparison with mammary carcinoma. J. Urol. 2002, 168, 1412–1414. [Google Scholar] [CrossRef] [PubMed]
- Smyth, L.G.; O’Hurley, G.; O’Grady, A.; Fitzpatrick, J.M.; Kay, E.; Watson, R.W.G. Carbonic anhydrase IX expression in prostate cancer. Prostate Cancer Prostatic. Dis. 2010, 13, 178–181. [Google Scholar] [CrossRef] [PubMed]
- Oosterwijk, E.; Ruiter, D.J.; Hoedemaeker, P.J.; Pauwels, E.K.J.; Jonas, U.; Zwartendijk, J.; Warnaar, S.O. Monoclonal antibody G 250 recognizes a determinant present in renal-cell carcinoma and absent from normal kidney. Int. J. Cancer 1986, 38, 489–494. [Google Scholar] [CrossRef] [PubMed]
- Pastorek, J.; Pastorekova, S.; Callebaut, I.; Mornon, J.P.; Zelnik, V.; Opavsky, R.; Zat’ovicová, M.; Liao, S.; Portetelle, D.; Stanbridge, E.J. Cloning and characterization of MN, a human tumor-associated protein with a domain homologous to carbonic anhydrase and a putative helix-loop-helix DNA binding segment. Oncogene 1994, 9, 2877–2888. [Google Scholar] [PubMed]
- Grabmaier, K.; Vissers, J.L.M.; de Weijert, M.C.A.; Oosterwijk-Wakka, J.C.; van Bokhoven, A.; Brakenhoff, R.H.; Noessner, E.; Mulders, P.A.; Merkx, G.; Figdor, C.G. Molecular cloning and immunogenicity of renal cell carcinoma-associated antigen G250. Int. J. Cancer 2000, 85, 865–870. [Google Scholar] [CrossRef] [PubMed]
- Surfus, J.E.; Hank, J.A.; Oosterwijk, E.; Welt, S.; Lindstrom, M.J.; Albertini, M.R.; Schiller, J.H.; Sondel, P.M. Anti-renal-cell carcinoma chimeric antibody G250 facilitates antibody-dependent cellular cytotoxicity with in vitro and in vivo interleukin-2-activated effectors. J. Immunother. 1996, 19, 184–191. [Google Scholar] [CrossRef]
- Liu, Z.Q.; Smyth, F.E.; Renner, C.; Lee, F.T.; Oosterwijk, E.; Scott, A.M. Anti-renal cell carcinoma chimeric antibody G250: Cytokine enhancement of in vitro anti body-dependent cellular cytotoxicity. Cancer Immunol. Immunother. 2002, 51, 171–177. [Google Scholar] [CrossRef] [PubMed]
- Belldegrun, A.S.; Chamie, K.; Kloepfer, P.; Fall, B.; Bevan, P.; Stoerkel, S.; Wilhelm, O.; Pantuck, A.J. ARISER: A randomized double blind phase III study to evaluate adjuvant cG250 treatment versus placebo in patients with high-risk ccRCC-Results and implications for adjuvant clinical trials. In Proceedings of 2013 ASCO Annual Meeting, Chicago, IL, USA, 31 May−4 June, 2013. Abstract Number 4507.
- Bleumer, I.; Knuth, A.; Oosterwijk, E.; Hofmann, R.; Varga, Z.; Lamers, C.; Kruit, W.; Melchior, S.; Mala, C.; Ullrich, S.; et al. A phase II trial of chimeric monoclonal antibody G250 for advanced renal cell carcinoma patients. Br. J. Cancer 2004, 90, 985–990. [Google Scholar] [CrossRef] [PubMed]
- Davis, I.D.; Wiseman, G.A.; Lee, F-T.; Gansen, D.N.; Hopkins, W.; Papenfuss, A.T.; Liu, L.; Moynihan, T.J.; Croghan, G.A.; Adjei, A.A. A phase I multiple dose, dose escalation study of cG250 monoclonal antibody in patients with advanced renal cell carcinoma. Cancer Immun. 2007, 7, 13–13. [Google Scholar]
- Bleumer, I.; Oosterwijk, E.; Oosterwijk-Wakka, J.C.; Voller, M.C.W.; Melchior, S.; Warnaar, S.O.; Mala, C.; Beck, J.; Mulders, P.F.A. A clinical trial with chimeric monoclonal antibody WX-G250 and low dose interleukin-2 pulsing scheme for advanced renal cell carcinoma. J. Urol. 2006, 175, 57–62. [Google Scholar] [CrossRef] [PubMed]
- Davis, I.D.; Liu, Z.; Saunders, W.; Lee, F-T.; Spirkoska, V.; Hopkins, W.; Smyth, F.E.; Chong, G.; Papenfuss, A.T.; Chappell, B.; et al. A pilot study of monoclonal antibody cG250 and low dose subcutaneous IL-2 in patients with advanced renal cell carcinoma. Cancer Immun. 2007, 7, 14–14. [Google Scholar] [PubMed]
- Siebels, M.; Rohrmann, K.; Oberneder, R.; Stahler, M.; Haseke, N.; Beck, J.; Hofmann, R.; Kindler, M.; Kloepfer, P.; Stief, C. A clinical phase I/II trial with the monoclonal antibody cG250 (RENCAREX®) and interferon-α-2a in metastatic renal cell carcinoma patients. World J. Urol. 2011, 29, 121–126. [Google Scholar] [CrossRef] [PubMed]
- Zatovicova, M.; Jelenska, L.; Hulikova, A.; Csaderova, L.; Ditte, Z.; Ditte, P.; Goliasova, T.; Pastorek, J.; Pastorekova, S. Carbonic anhydrase IX as an anticancer therapy target: Preclinical evaluation of internalizing monoclonal antibody directed to catalytic domain. Curr. Pharm. Des. 2010, 16, 3255–3263. [Google Scholar] [CrossRef] [PubMed]
- Petrul, H.M.; Schatz, C.A.; Kopitz, C.C.; Adnane, L.; McCabe, T.J.; Trail, P.; Ha, S.; Chang, Y.S.; Voznesensky, A.; Ranges, G.; et al. Therapeutic mechanism and efficacy of the antibody-drug conjugate BAY 79–4620 targeting human carbonic anhydrase 9. Mol. Cancer Ther. 2012, 11, 340–349. [Google Scholar] [PubMed]
- Manjappa, A.S.; Chaudhari, K.R.; Venkataraju, M.P.; Dantuluri, P.; Nanda, B.; Sidda, C.; Krutika, S.K.; Murthy, R.S.R. Antibody derivatization and conjugation strategies: Application in preparation of stealth immunoliposome to target chemotherapeutics to tumor. J. Control. Release 2011, 150, 2–22. [Google Scholar] [CrossRef]
- Braden, B.C.; Goldman, E.R.; Mariuzza, R.A.; Poljak, R.J. Anatomy of an antibody molecule: Structure, kinetics, thermodynamics and mutational studies of the antilysozyme antibody D1.3. Immunol. Rev. 1998, 163, 45–57. [Google Scholar] [CrossRef] [PubMed]
- Goding, J.W. Monoclonal Antibodies: Principles and Practice; Acadmic Press Inc.: San Dirgo, CA, USA, 1986. [Google Scholar]
- Ravdin, P.M.; Chamness, G.C. The c-erbB-2 proto-oncogene as a prognostic and predictive marker in breast cancer: a paradigm for the development of other macromolecular markers—A review. Gene 1995, 159, 19–27. [Google Scholar] [CrossRef] [PubMed]
- Slamon, D.J.; Clark, G.M.; Wong, S.G.; Levin, W.J.; Ullrich, A.; McGuire, W.L. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987, 235, 177–182. [Google Scholar] [CrossRef] [PubMed]
- Kirpotin, D.B.; Drummond, D.C.; Shao, Y.; Shalaby, M.R.; Hong, K.L.; Nielsen, U.B.; Marks, J.D.; Benz, C.C.; Park, J.W. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res. 2006, 66, 6732–6740. [Google Scholar] [CrossRef] [PubMed]
- Stefanick, J.F.; Ashley, J.D.; Kiziltepe, T.; Bilgicer, B. A systematic analysis of peptide linker length and liposomal polyethylene glycol coating on cellular uptake of peptide-targeted liposomes. ACS Nano 2013, 7, 2935–2947. [Google Scholar] [PubMed]
- Goren, D.; Horowitz, A.T.; Zalipsky, S.; Woodle, M.C.; Yarden, Y.; Gabizon, A. Targeting of stealth liposomes to erbB-2 (Her/2) receptor: In vitro and in vivo studies. Br. J. Cancer 1996, 74, 1749–1756. [Google Scholar] [CrossRef]
- Tuscano, J.M.; Martin, S.M.; Ma, Y.; Zamboni, W.; O’Donnell, R.T. Efficacy, biodistribution, and pharmacokinetics of CD22-targeted pegylated liposomal doxorubicin in a B-cell non-hodgkin’s lymphoma xenograft mouse model. Clin. Cancer Res. 2010, 16, 2760–2768. [Google Scholar] [CrossRef]
- Sapra, P.; Moase, E.H.; Ma, J.; Allen, T.M. Improved therapeutic responses in a xenograft model of human B lymphoma (Namalwa) for liposomal vincristine versus liposomal doxorubicin targeted via anti-CD19 IgG2a or Fab’ fragments. Clin. Cancer Res. 2004, 10, 1100–1111. [Google Scholar] [CrossRef] [PubMed]
- Alshaer, W.; Hillaireau, H.; Vergnaud, J.; Ismail, S.; Fattal, E. Functionalizing liposomes with anti-CD44 aptamer for selective targeting of cancer cells. Bioconjug. Chem. 2014. [Google Scholar] [CrossRef]
- Hatakeyama, H.; Akita, H.; Ishida, E.; Hashimoto, K.; Kobayashi, H.; Aoki, T.; Yasuda, J.; Obata, K.; Kikuchi, H.; Ishid, T.; et al. Tumor targeting of doxorubicin by anti-MT1-MMP antibody-modified PEG liposomes. Int. J. Pharm. 2007, 342, 194–200. [Google Scholar] [CrossRef] [PubMed]
- Mamot, C.; Ritschard, R.; Wicki, A.; Stehle, G.; Dieterle, T.; Bubendorf, L.; Hilker, C.; Deuster, S.; Herrmann, R.; Rochlitz, C. Tolerability, safety, pharmacokinetics, and efficacy of doxorubicin-loaded anti-EGFR immunoliposomes in advanced solid tumours: A phase 1 dose-escalation study. Lancet Oncol. 2012, 13, 1234–1241. [Google Scholar] [CrossRef] [PubMed]
- Matsumura, Y.; Gotoh, M.; Muro, K.; Yamada, Y.; Shirao, K.; Shimada, Y.; Okuwa, M.; Matsumoto, S.; Miyata, Y.; Ohkura, H. Phase I and pharmacokinetic study of MCC-465, a doxorubicin (DXR) encapsulated in PEG immunoliposome, in patients with metastatic stomach cancer. Ann. Oncol. 2004, 15, 517–525. [Google Scholar] [CrossRef] [PubMed]
- Tiwari, G.; Tiwari, R.; Sriwastawa, B.; Bhati, L.; Pandey, S.; Pandey, P.; Bannerjee, S.K. Drug delivery systems: An updated review. Int. J. Pharm. Investig. 2012, 2, 2–11. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.-I.; Yeh, M.-K. Clinical development of liposome-based drugs: Formulation, characterization, and therapeutic efficacy. Int. J. Nanomed. 2012, 7, 49–60. [Google Scholar]
- Shinkai, M.; Le, B.; Honda, H.; Yoshikawa, K.; Shimizu, K.; Saga, S.; Wakabayashi, T.; Yoshida, J.; Kobayashi, T. Targeting hyperthermia for renal cell carcinoma using human MN antigen-specific magnetoliposomes. JNP J. Cancer Res. 2001, 92, 1138–1145. [Google Scholar] [CrossRef]
- Askoxylakis, V.; Ehemann, V.; Rana, S.; Krämer, S.; Rahbari, N.N.; Debus, J.; Haberkorn, U. Binding of the phage display derived peptide CaIX-P1 on human colorectal carcinoma cells correlates with the expression of carbonic anhydrase IX. Int. J. Mol. Sci. 2012, 13, 13030–13048. [Google Scholar] [CrossRef] [PubMed]
- Askoxylakis, V.; Garcia-Boy, R.; Rana, S.; Krämer, S.; Hebling, U.; Mier, W.; Altmann, A.; Markert, A.; Debus, J.; Haberkorn, U. A new peptide ligand for targeting human carbonic anhydrase IX, identified through the phage display technology. PLoS One 2010, 5, e15962. [Google Scholar] [CrossRef] [PubMed]
© 2014 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ng, H.L.H.; Lu, A.; Lin, G.; Qin, L.; Yang, Z. The Potential of Liposomes with Carbonic Anhydrase IX to Deliver Anticancer Ingredients to Cancer Cells in Vivo. Int. J. Mol. Sci. 2015, 16, 230-255. https://doi.org/10.3390/ijms16010230
Ng HLH, Lu A, Lin G, Qin L, Yang Z. The Potential of Liposomes with Carbonic Anhydrase IX to Deliver Anticancer Ingredients to Cancer Cells in Vivo. International Journal of Molecular Sciences. 2015; 16(1):230-255. https://doi.org/10.3390/ijms16010230
Chicago/Turabian StyleNg, Huei Leng Helena, Aiping Lu, Ge Lin, Ling Qin, and Zhijun Yang. 2015. "The Potential of Liposomes with Carbonic Anhydrase IX to Deliver Anticancer Ingredients to Cancer Cells in Vivo" International Journal of Molecular Sciences 16, no. 1: 230-255. https://doi.org/10.3390/ijms16010230