Characterization of a monoclonal antibody capable of reliably quantifying expression of human copper transporter 1 (hCTR1)

Journal of Trace Elements in Medicine and Biology

Volumn 28, Issue 2, 2014, Pages 151-159

  Quail, Jacob F ^a   Tsai, Cheng Yu ^a   Howell, Stephen B ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Copper; Copper transporter 1; Monoclonal antibody; Transporter; Western blot

Indexed keywords

CARRIER PROTEIN; CISPLATIN; COPPER SULFATE; EPITOPE; HUMAN COPPER TRANSPORTER 1; HUMAN COPPER TRANSPORTER 1 MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; MYC PROTEIN; PROTEIN TAG; UNCLASSIFIED DRUG; CARRIER PROTEINS AND BINDING PROTEINS; MEMBRANE PROTEIN; MONOMER; CATION TRANSPORT PROTEIN; CELL EXTRACT; COPPER TRANSPORTER 1;

ANTIBODY SCREENING; ARTICLE; BIOTINYLATION; CANCER CELL CULTURE; CELL LYSATE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; DEGLYCOSYLATION; DOWN REGULATION; DRUG DETERMINATION; DRUG EFFECT; DRUG MECHANISM; DRUG SENSITIVITY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IC 50; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; WESTERN BLOTTING; AMINO TERMINAL SEQUENCE; ANTIGEN ANTIBODY REACTION; CROSS REACTION; PROTEIN ANALYSIS; CELL MEMBRANE; DRUG EFFECTS; GENE SILENCING; GENETIC ENGINEERING; GLYCOSYLATION; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; TUMOR CELL LINE;

MAMMALIA; ORYCTOLAGUS CUNICULUS;

ANTIBODIES, MONOCLONAL; BIOTINYLATION; BLOTTING, WESTERN; CATION TRANSPORT PROTEINS; CELL EXTRACTS; CELL LINE, TUMOR; CELL MEMBRANE; CISPLATIN; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; GENETIC ENGINEERING; GLYCOSYLATION; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION;

EID: 84898022542     PISSN: 0946672X     EISSN: 18783252     Source Type: Journal    
DOI: 10.1016/j.jtemb.2013.12.003     Document Type: Article

References (41)

1. Puig S., Thiele D.J. Molecular mechanisms of copper uptake and distribution. Curr Opin Chem Biol 2002, 6:171-180.
2. Tsai C.Y., Finley J.C., Ali S.S., Patel H.H., Howell S.B. Copper influx transporter 1 is required for FGF, PDGF and EGF-induced MAPK signaling. Biochem Pharmacol 2012, 84:1007.
3. Wee N.K., Weinstein D.C., Fraser S.T., Assinder S.J. The mammalian copper transporters CTR1 and CTR2 and their roles in development and disease. Int J Biochem Cell Biol 2013, 45:960-963.
4. Holzer A.K., Howell S.B. The internalization and degradation of human copper transporter 1 following cisplatin exposure. Cancer Res 2006, 66:10944-10952.
5. Howell S.B., Safaei R., Larson C.A., Sailor M.J. Copper transporters and the cellular pharmacology of the platinum-containing cancer drugs. Mol Pharmacol 2010, 77:887-894.
6. Abada P., Howell S.B. Regulation of cisplatin cytotoxicity by Cu influx transporters. Met Based Drugs 2010, 2010:317581.
7. Lee Y.Y., Choi C.H., Do I.G., Song S.Y., Lee W., Park H.S., et al. Prognostic value of the copper transporters, CTR1 and CTR2, in patients with ovarian carcinoma receiving platinum-based chemotherapy. Gynecol Oncol 2011, 122:361-365.
8. Chen H.H., Yan J.J., Chen W.C., Kuo M.T., Lai Y.H., Lai W.W., et al. Predictive and prognostic value of human copper transporter 1 (hCtr1) in patients with stage III non-small-cell lung cancer receiving first-line platinum-based doublet chemotherapy. Lung Cancer 2012, 75:228-234.
9. Kuo M.T., Fu S., Savarak N., Chen H.H.W. Role of the high-affinity copper transporter (hCTR1) in cisplatin sensitivity in cancer chemotherapy. Cancer Res 2012, 72:4616-4621.
10. Liang Z.D., Long Y., Tsai W.B., Fu S., Kurzrock R., Gagea-Iurascu M., et al. Mechanistic basis for overcoming platinum resistance using copper chelating agents. Mol Cancer Ther 2012, 11:2483-2494.
11. Fu S., Naing A., Fu C., Kuo M.T., Kurzrock R. Overcoming platinum resistance through the use of a copper-lowering agent. Overcoming platinum resistance using a copper-lowering agent. Mol Cancer Ther 2011, 11:1221-1225.
12. Ishida S., McCormick F., Smith-McCune K., Hanahan D. Enhancing tumor-specific uptake of the anticancer drug cisplatin with a copper chelator. Cancer Cell 2010, 17:574-583.
13. Maryon E.B., Zhang J., Jellison J.W., Kaplan J.H. Human copper transporter 1 lacking o-linked glycosylation is proteolytically cleaved in a rab-9 positive endosomal compartment. J Biol Chem 2009, 284:28104-28114.
14. Maryon E.B., Molloy S.A., Kaplan J.H. O-linked glycosylation at threonine 27 protects the copper transporter hCTR1 from proteolytic cleavage in mammalian cells. J Biol Chem 2007, 282:20376-20387.
15. Nose Y., Wood L.K., Kim B.E., Prohaska J.R., Fry R.S., Spears J.W., et al. Ctr1 is an apical copper transporter in mammalian intestinal epithelial cells in vivo that is controlled at the level of protein stability. J Biol Chem 2010, 285:32385-32392.
16. Klomp A.E., Tops B.B., Van Denberg I.E., Berger R., Klomp L.W. Biochemical characterization and subcellular localization of human copper transporter 1 (hCTR1). Biochem J 2002, 364:497-505.
17. De Feo C.J., Aller S.G., Siluvai G.S., Blackburn N.J., Unger V.M. Three-dimensional structure of the human copper transporter hCTR1. Proc Natl Acad Sci 2009, 106:4237-4242.
18. Yoshida H., Teramae M., Yamauchi M., Fukuda T., Yasui T., Sumi T., et al. Association of copper transporter expression with platinum resistance in epithelial ovarian cancer. Anticancer Res 2013, 33:1409-1414.
19. Ogane N., Yasuda M., Kameda Y., Yokose T., Kato H., Itoh A., et al. Prognostic value of organic anion transporting polypeptide 1B3 and copper transporter 1 expression in endometrial cancer patients treated with paclitaxel and carboplatin. Biomed Res 2013, 34:143-151.
20. Narayanan G.R.B.S., Vuyyuru H., Muthuvel B., Konerirajapuram Natrajan S. CTR1 silencing inhibits angiogenesis by limiting copper entry into endothelial cells. PLoS ONE 2013, 8:e71982.
21. De Benedetto M.L., Capo C.R., Ferri A., Valle C., Polimanti R., Carri M.T., et al. Glutaredoxin 1 is a major player in copper metabolism in neuroblastoma cells. Biochim Biophys Acta 2013, 1840:255-261.
22. Davies K.M., Hare D.J., Cottam V., Chen N., Hilgers L., Halliday G., et al. Localization of copper and copper transporters in the human brain. Metallomics 2013, 5:43-51.
23. Larson C.A., Adams P.L., Jandial D.D., Blair B.G., Safaei R., Howell S.B. The role of the N-terminus of mammalian copper transporter 1 in the cellular accumulation of cisplatin. Biochem Pharmacol 2010, 80:448-454.
24. Shang X., Lin X., Manorek G., Howell S.B. Claudin-3 and claudin-4 regulate sensitivity to cisplatin by controlling expression of the copper and cisplatin influx Rransporter CTR1. Mol Pharmacol 2013, 83:84-94.
25. Yuan X., Lin X., Manorek G., Howell S.B. Challenges associated with the targeted delivery of gelonin to claudin-expressing cancer cells with the use of activatable cell penetrating peptides to enhance potency. BMC Cancer 2011, 11:61.
26. Kalayda G.V., Wagner C.H., Jaehde U. Relevance of copper transporter 1 for cisplatin resistance in human ovarian carcinoma cells. J Inorg Biochem 2012, 116C:1-10.
27. Holzer A.K., Katano K., Klomp L.W., Howell S.B. Cisplatin rapidly down-regulates its own influx transporter hCTR1 in cultured human ovarian carcinoma cells. Clin Cancer Res 2004, 10:6744-6749.
28. Holzer A.K., Samimi G., Katano K., Naerdemann W., Lin X., Safaei R., et al. The copper influx transporter human copper transport protein 1 regulates the uptake of cisplatin in human ovarian carcinoma cells. Mol Pharmacol 2004, 66:817-823.
29. Pabla N., Murphy R.F., Liu K., Dong Z. The copper transporter Ctr1 contributes to cisplatin uptake by renal tubular cells during cisplatin nephrotoxicity. Am J Physiol Renal Physiol 2009, 296:F505-F511.
30. Ivy K.D., Kaplan J.H. A re-evaluation of the role of hCTR1, the human high-affinity copper transporter, in platinum-drug entry into human cells. Mol Pharmacol 2013, 83:1237-1246.
31. Molloy S.A., Kaplan J.H. Copper-dependent recycling of hCTR1, the human high affinity copper transporter. J Biol Chem 2009, 284:29704-29713.
32. Ciarimboli G., Deuster D., Knief A., Sperling M., Holtkamp M., Edemir B., et al. Organic cation transporter 2 mediates cisplatin-induced oto- and nephrotoxicity and is a target for protective interventions. Am J Pathol 2010, 176:1169-1180.
33. Yonezawa A., Masuda S., Yokoo S., Katsura T., Inui K. Cisplatin and oxaliplatin, but not carboplatin and nedaplatin, are substrates for human organic cation transporters (SLC22A1-3 and multidrug and toxin extrusion family). J Pharmacol Exp Ther 2006, 319:879-886.
34. Song I., Savaraj N., Siddik Z., Liu P., Wei Y., Wu C., et al. Role of copper transporter Ctr1 in the transport of platinum-based antitumor agents in cisplatin-sensitive and resistant cells. Mol Cancer Ther 2004, 3:1543-1549.
35. Kuo Y.M., Gybina A.A., Pyatskowit J.W., Gitschier J., Prohaska J.R. Copper transport protein (Ctr1) levels in mice are tissue specific and dependent on copper status. J Nutr 2006, 136:21-26.
36. Eisses J.F., Kaplan J.H. Molecular characterization of hCTR1, the human copper uptake protein. J Biol Chem 2002, 277:29162-29171.
37. Haas K.L., Putterman A.B., White D.R., Thiele D.J., Franz K.J. Model peptides provide new insights into the role of histidine residues as potential ligands in human cellular copper acquisition via Ctr1. JACS 2011, 133:4427-4437.
38. Lee J., Pena M.M., Nose Y., Thiele D.J. Biochemical characterization of the human copper transporter Ctr1. J Biol Chem 2002, 277:4380-4387.
39. Safaei R., Maktabi M.H., Blair B.G., Larson C.A., Howell S.B. Effects of the loss of Atox1 on the cellular pharmacology of cisplatin. J Inorg Biochem 2009, 103:333-341.
40. Jandial D.D., Farshchi-Heydari S., Larson C.A., Elliot G.I., Wrasidlo W.J., Howell S.B. Enhanced delivery of cisplatin to intraperitoneal ovarian carcinomas mediated by the effects of bortezomib on the human copper transporter 1. Clin Cancer Res 2009, 15:553-560.
41. Abada P.B., Larson C.A., Manorek G., Adams P., Howell S.B. Sec61beta controls sensitivity to platinum-containing chemotherapeutic agents through modulation of the copper-transporting ATPase ATP7A. Mol Pharmacol 2012, 82:510-520.