Claudin-3 and claudin-4 regulate sensitivity to cisplatin by controlling expression of the copper and cisplatin influx transporter CTR1

Molecular Pharmacology

Volumn 83, Issue 1, 2013, Pages 85-94

  Shang, Xiying ^b   Lin, Xinjian ^b   Manorek, Gerald ^b   Howell, Stephen B ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; CLAUDIN 3; CLAUDIN 4; DOXORUBICIN; ETOPOSIDE; MONOPHENOL MONOOXYGENASE; PACLITAXEL; VINCRISTINE;

ARTICLE; CANCER CELL; CONTROLLED STUDY; CYTOTOXICITY; DNA ADDUCT; DRUG ACCUMULATION; DRUG MECHANISM; DRUG SENSITIVITY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; OVARY CARCINOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; TIGHT JUNCTION; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CATION TRANSPORT PROTEINS; CELL LINE, TUMOR; CISPLATIN; CLAUDIN-3; CLAUDIN-4; COPPER; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; MONOPHENOL MONOOXYGENASE; NEOPLASM TRANSPLANTATION; OVARIAN NEOPLASMS; RNA, MESSENGER; TIGHT JUNCTIONS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84871572370     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.079798     Document Type: Article

References (59)

1. Balda MS, Garrett MD, and Matter K (2003) The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density. J Cell Biol 160:423-432. (Pubitemid 36182732)
2. Balda MS and Matter K (2000) The tight junction protein ZO-1 and an interacting transcription factor regulate ErbB-2 expression. EMBO J 19:2024-2033. (Pubitemid 30237578)
3. Blair BG, Larson CA, Adams PL, Abada PB, Safaei R, and Howell SB (2010) Regulation of copper transporter 2 expression by copper and cisplatin in human ovarian carcinoma cells. Mol Pharmacol 77:912-921.
4. Bouchard B, Fuller BB, Vijayasaradhi S, and Houghton AN (1989) Induction of pigmentation in mouse fibroblasts by expression of human tyrosinase cDNA. J Exp Med 169:2029-2042. (Pubitemid 19162964)
5. Ersoz S, Mungan S, Cobanoglu U, Turgutalp H, and Ozoran Y (2011) Prognostic importance of claudin-1 and claudin-4 expression in colon carcinomas. Pathol Res Pract 207:285-289.
6. Finch A, Shaw P, Rosen B, Murphy J, Narod SA, and Colgan TJ (2006) Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers. Gynecol Oncol 100:58-64. (Pubitemid 41815050)
7. Fink D, Nebel S, Norris PS, Baergen RN, Wilczynski SP, Costa MJ, Haas M, Cannistra SA, and Howell SB (1998) Enrichment for DNA mismatch repair-deficient cells during treatment with cisplatin. Int J Cancer 77:741-746. (Pubitemid 28341392)
8. Fink D, Zheng H, Nebel S, Norris PS, Aebi S, Lin TP, Nehmé A, Christen RD, Haas M, MacLeod CL, and Howell SB (1997) In vitro and in vivo resistance to cisplatin in cells that have lost DNA mismatch repair. Cancer Res 57:1841-1845. (Pubitemid 27209707)
9. Heinzelmann-Schwarz VA, Gardiner-Garden M, Henshall SM, Scurry J, Scolyer RA, Davies MJ, Heinzelmann M, Kalish LH, Bali A, and Kench JG et al. (2004) Overexpression of the cell adhesion molecules DDR1, Claudin 3, and Ep-CAM in metaplastic ovarian epithelium and ovarian cancer. Clin Cancer Res 10:4427-4436. (Pubitemid 38878885)
10. Hewitt KJ, Agarwal R, and Morin PJ (2006) The claudin gene family: expression in normal and neoplastic tissues. BMC Cancer 6:186.
11. Hofmann I, Schnölzer M, Kaufmann I, and Franke WW (2002) Symplekin, a constitutive protein of karyo- and cytoplasmic particles involved in mRNA biogenesis in Xenopus laevis oocytes. Mol Biol Cell 13:1665-1676. (Pubitemid 34522647)
12. Holzer AK, Katano K, Klomp LW, and Howell SB (2004a) Cisplatin rapidly downregulates its own influx transporter hCTR1 in cultured human ovarian carcinoma cells. Clin Cancer Res 10:6744-6749. (Pubitemid 39346572)
13. Holzer AK, Samimi G, Katano K, Naerdemann W, Lin X, Safaei R, and Howell SB (2004b) The copper influx transporter human copper transport protein 1 regulates the uptake of cisplatin in human ovarian carcinoma cells. Mol Pharmacol 66:817-823. (Pubitemid 39319453)
14. Hough CD, Sherman-Baust CA, Pizer ES, Montz FJ, Im DD, Rosenshein NB, Cho KR, Riggins GJ, and Morin PJ (2000) Large-scale serial analysis of gene expression reveals genes differentially expressed in ovarian cancer. Cancer Res 60:6281-6287.
15. Howell SB, Safaei R, Larson CA, and Sailor MJ (2010) Copper transporters and the cellular pharmacology of the platinum-containing cancer drugs. Mol Pharmacol 77:887-894.
16. Hurd TW, Gao L, Roh MH, Macara IG, and Margolis B (2003) Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat Cell Biol 5:137-142. (Pubitemid 36210848)
17. Ishida S, Lee J, Thiele DJ, and Herskowitz I (2002) Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals. Proc Natl Acad Sci USA 99:14298-14302. (Pubitemid 35257666)
18. Itoh M and Bissell MJ (2003) The organization of tight junctions in epithelia: implications for mammary gland biology and breast tumorigenesis. J Mammary Gland Biol Neoplasia 8:449-462. (Pubitemid 39137506)
19. Karst AM, Levanon K, and Drapkin R (2011) Modeling high-grade serous ovarian carcinogenesis from the fallopian tube. Proc Natl Acad Sci USA 108:7547-7552.
20. Katahira J, Sugiyama H, Inoue N, Horiguchi Y, Matsuda M, and Sugimoto N (1997) Clostridium perfringens enterotoxin utilizes two structurally related membrane proteins as functional receptors in vivo. J Biol Chem 272:26652-26658. (Pubitemid 27458889)
21. Katano K, Safaei R, Samimi G, Holzer A, Rochdi M, and Howell SB (2003) The copper export pump ATP7B modulates the cellular pharmacology of carboplatin in ovarian carcinoma cells. Mol Pharmacol 64:466-473. (Pubitemid 36910011)
22. Köhler K and Zahraoui A (2005) Tight junction: a co-ordinator of cell signalling and membrane trafficking. Biol Cell 97:659-665. (Pubitemid 41079038)
23. Kominsky SL (2006) Claudins: emerging targets for cancer therapy. Expert Rev Mol Med 8:1-11.
24. Kominsky SL, Tyler B, Sosnowski J, Brady K, Doucet M, Nell D, Smedley JG, 3rd, McClane B, Brem H, and Sukumar S (2007) Clostridium perfringens enterotoxin as a novel-targeted therapeutic for brain metastasis. Cancer Res 67:7977-7982. (Pubitemid 47395128)
25. Larson CA, Adams PL, Blair BG, Safaei R, and Howell SB (2010) The role of the methionines and histidines in the transmembrane domain of mammalian copper transporter 1 in the cellular accumulation of cisplatin. Mol Pharmacol 78:333-339.
26. Larson CA, Blair BG, Safaei R, and Howell SB (2009) The role of the mammalian copper transporter 1 in the cellular accumulation of platinum-based drugs. Mol Pharmacol 75:324-330.
27. Lee KW, Lee NK, Kim JH, Kang MS, Yoo HY, Kim HH, Um SH, and Kim SH (2012) Twist1 causes the transcriptional repression of claudin-4 with prognostic significance in esophageal cancer. Biochem Biophys Res Commun 423:454-460.
28. Lee Y, Miron A, Drapkin R, NucciMR, Medeiros F, Saleemuddin A, Garber J, Birch C, Mou H, and Gordon RW et al. (2007) A candidate precursor to serous carcinoma that originates in the distal fallopian tube. J Pathol 211:26-35. (Pubitemid 46092026)
29. Lemmers C, Médina E, Delgrossi MH, Michel D, Arsanto JP, and Le Bivic A (2002) hINADl/PATJ, a homolog of discs lost, interacts with crumbs and localizes to tight junctions in human epithelial cells. J Biol Chem 277:25408-25415. (Pubitemid 34951853)
30. Levanon K, Ng V, Piao HY, and Zhang YChang MC, Roh MH, Kindelberger DW, Hirsch MS, Crum CP, Marto JA, and Drapkin R (2010) Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene 29:1103-1113.
31. Lin X, Kim HK, and Howell SB (1999) The role of DNA mismatch repair in cisplatin mutagenicity. J Inorg Biochem 77:89-93. (Pubitemid 30089087)
32. Lin X, Okuda T, Holzer A, and Howell SB (2002) The copper transporter CTR1 regulates cisplatin uptake in Saccharomyces cerevisiae. Mol Pharmacol 62:1154-1159. (Pubitemid 35222507)
33. Litkouhi B, Kwong J, Lo CM, Smedley JG, 3rd, McClane BA, Aponte M, Gao Z, Sarno JL, Hinners J, and Welch WR et al. (2007) Claudin-4 overexpression in epithelial ovarian cancer is associated with hypomethylation and is a potential target for modulation of tight junction barrier function using a C-terminal fragment of Clostridium perfringens enterotoxin. Neoplasia 9:304-314. (Pubitemid 46608297)
34. Martin TA, Watkins G, Mansel RE, and Jiang WG (2004) Loss of tight junction plaque molecules in breast cancer tissues is associated with a poor prognosis in patients with breast cancer. Eur J Cancer 40:2717-2725. (Pubitemid 39574723)
35. Matsuoka T, Mitomi H, Fukui N, Kanazawa H, Saito T, Hayashi T, and Yao T (2011) Cluster analysis of claudin-1 and -4, E-cadherin, and β-catenin expression in colorectal cancers. J Surg Oncol 103:674-686.
36. Møller LB, Petersen C, Lund C, and Horn N (2000) Characterization of the hCTR1 gene: genomic organization, functional expression, and identification of a highly homologous processed gene. Gene 257:13-22.
37. Morin PJ (2005) Claudin proteins in human cancer: promising new targets for diagnosis and therapy. Cancer Res 65:9603-9606.
38. Mullin JM (2004) Epithelial barriers, compartmentation, and cancer. Sci STKE 2004:pe2.
39. Ouban A and Ahmed AA (2010) Claudins in human cancer: a review. Histol Histopathol 25:83-90.
40. Petris MJ, Strausak D, and Mercer JF (2000) The Menkes copper transporter is required for the activation of tyrosinase. Hum Mol Genet 9:2845-2851.
41. Rangel LB, Agarwal R, D'Souza T, Pizer ES, Alò PL, Lancaster WD, Gregoire L, Schwartz DR, Cho KR, and Morin PJ (2003) Tight junction proteins claudin-3 and claudin-4 are frequently overexpressed in ovarian cancer but not in ovarian cystadenomas. Clin Cancer Res 9:2567-2575. (Pubitemid 36842098)
42. Roh MH, Liu CJ, Laurinec S, and Margolis B (2002) The carboxyl terminus of zona occludens-3 binds and recruits a mammalian homologue of discs lost to tight junctions. J Biol Chem 277:27501-27509. (Pubitemid 34951771)
43. Saeki R, Kondoh M, Kakutani H, Matsuhisa K, Takahashi A, Suzuki H, Kakamu Y, Watari A, and Yagi K (2010) A claudin-targeting molecule as an inhibitor of tumor metastasis. J Pharmacol Exp Ther 334:576-582.
44. Safaei R (2006) Role of copper transporters in the uptake and efflux of platinum containing drugs. Cancer Lett 234:34-39.
45. Safaei R, Maktabi MH, Blair BG, Larson CA, and Howell SB (2009) Effects of the loss of Atox1 on the cellular pharmacology of cisplatin. J Inorg Biochem 103:333-341.
46. Samimi G, Safaei R, Katano K, Holzer AK, Rochdi M, Tomioka M, Goodman M, and Howell SB (2004) Increased expression of the copper efflux transporter ATP7A mediates resistance to cisplatin, carboplatin, and oxaliplatin in ovarian cancer cells. Clin Cancer Res 10:4661-4669. (Pubitemid 38955516)
47. Santin AD, Cané S, Bellone S, PalmieriM, Siegel ER, Thomas M, Roman JJ, Burnett A, Cannon MJ, and Pecorelli S (2005) Treatment of chemotherapy-resistant human ovarian cancer xenografts in C.B-17/SCID mice by intraperitoneal administration of Clostridium perfringens enterotoxin. Cancer Res 65:4334-4342. (Pubitemid 40775672)
48. Santin AD, Zhan F, Bellone S, Palmieri M, Cane S, Bignotti E, Anfossi S, Gokden M, Dunn D, and Roman JJ et al. (2004) Gene expression profiles in primary ovarian serous papillary tumors and normal ovarian epithelium: identification of candidate molecularmarkers for ovarian cancer diagnosis and therapy. Int J Cancer 112:14-25. (Pubitemid 39249487)
49. Sasaki H, Matsui C, Furuse K, Mimori-Kiyosue Y, Furuse M, and Tsukita S (2003) Dynamic behavior of paired claudin strands within apposing plasma membranes. Proc Natl Acad Sci USA 100:3971-3976. (Pubitemid 36418141)
50. Stewart DJ (2007) Mechanisms of resistance to cisplatin and carboplatin. Crit Rev Oncol Hematol 63:12-31.
51. Szasz AM, Nemeth Z, Gyorffy B, Micsinai M, Krenacs T, Baranyai Z, Harsanyi L, Kiss A, Schaff Z, Tokes AM, and Kulka J (2011) Identification of a claudin-4 and E-cadherin score to predict prognosis in breast cancer. Cancer Sci 102:2248-2254.
52. Thiery JP, Acloque H, Huang RY, and Nieto MA (2009) Epithelial- mesenchymal transitions in development and disease. Cell 139:871-890.
53. Tisato F, Marzano C, Porchia M, Pellei M, and Santini C (2010) Copper in diseases and treatments, and copper-based anticancer strategies. Med Res Rev 30:708-749.
54. Toyofuku K, Wada I, Hirosaki K, Park JS, Hori Y, and Jimbow K (1999) Promotion of tyrosinase folding in COS 7 cells by calnexin. J Biochem 125:82-89. (Pubitemid 29085966)
55. Tsutsumi K, Sato N, Tanabe R, Mizumoto K, Morimatsu K, Kayashima T, Fujita H, Ohuchida K, Ohtsuka T, and Takahata S et al. (2012) Claudin-4 expression predicts survival in pancreatic ductal adenocarcinoma. Ann Surg Oncol 19(Suppl 3):S491-S499.
56. Yoshida H, Sumi T, Zhi X, Yasui T, Honda K, and Ishiko O (2011) Claudin-4: a potential therapeutic target in chemotherapy-resistant ovarian cancer. Anticancer Res 31:1271-1277.
57. Yoshihara K, Tajima A, Yahata T, and Kodama SFujiwara H, Suzuki M, Onishi Y, Hatae M, Sueyoshi K, and Fujiwara H et al. (2010) Gene expression profile for predicting survival in advanced-stage serous ovarian cancer across two independent datasets. PLoS ONE 5:e9615.
58. Yuan X, Lin X, Manorek G, and Howell SB (2011) 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 11:61.
59. Yuan X, Lin X, Manorek G, Kanatani I, Cheung LH, Rosenblum MG, and Howell SB (2009) Recombinant CPE fused to tumor necrosis factor targets human ovarian cancer cells expressing the claudin-3 and claudin-4 receptors. Mol Cancer Ther 8:1906-1915.