Up-regulation of CD44 in the development of metastasis, recurrence and drug resistance of ovarian cancer

Oncotarget

Volumn 6, Issue 11, 2015, Pages 9313-9326

  Gao, Yan ^a,b   Foster, Rosemary ^a   Yang, Xiaoqian ^a,b   Feng, Yong ^a   Shen, Jacson K ^a   Mankin, Henry J ^a   Hornicek, Francis J ^a   Amiji, Mansoor M ^c   Duan, Zhenfeng ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b ZHENGZHOU UNIVERSITY   (China)

^c NORTHEASTERN UNIVERSITY   (United States)

Author keywords

CD44; Ovarian cancer; Paclitaxel; Pgp; Tissue microarray

Indexed keywords

HERMES ANTIGEN; PACLITAXEL; ANTINEOPLASTIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CANCER RECURRENCE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG SENSITIVITY; HUMAN; IMMUNOHISTOCHEMISTRY; METASTASIS; NONHUMAN; OVARY CANCER; PRIMARY TUMOR; SPHEROID CELL; TISSUE MICROARRAY; TUMOR XENOGRAFT; UPREGULATION; WOUND HEALING; ANIMAL; BAGG ALBINO MOUSE; DRUG RESISTANCE; DRUG SCREENING; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MORTALITY; MOUSE; NEOPLASMS, GLANDULAR AND EPITHELIAL; NUDE MOUSE; OVARIAN NEOPLASMS; PATHOLOGY; RECURRENT DISEASE; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD44; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; MICE, TRANSGENIC; NEOPLASM METASTASIS; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; PACLITAXEL; RECURRENCE; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84928747380     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3220     Document Type: Article

References (49)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA: a cancer journal for clinicians. 2014; 64:9-29.
2. Armstrong DK, Bundy B, Wenzel L, Huang HQ, Baergen R, Lele S, Copeland LJ, Walker JL, Burger RA. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. The New England journal of medicine. 2006; 354:34-43.
3. Bookman MA, Brady MF, McGuire WP, Harper PG, Alberts DS, Friedlander M, Colombo N, Fowler JM, Argenta PA, De Geest K, Mutch DG, Burger RA, Swart AM, Trimble EL, Accario-Winslow C, Roth LM. Evaluation of new platinum-based treatment regimens in advanced-stage ovarian cancer: a Phase III Trial of the Gynecologic Cancer Intergroup. Journal of clinical oncology:official journal of the American Society of Clinical Oncology. 2009; 27:1419-1425.
4. Vaughan S, Coward JI, Bast RC Jr., Berchuck A, Berek JS, Brenton JD, Coukos G, Crum CC, Drapkin R, Etemadmoghadam D, Friedlander M, Gabra H, Kaye SB, Lord CJ, Lengyel E, Levine DA, et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nature reviews Cancer. 2011; 11:719-725.
5. Screaton GR, Bell MV, Jackson DG, Cornelis FB, Gerth U, Bell JI. Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proceedings of the National Academy of Sciences of the United States of America. 1992; 89:12160-12164.
6. Naor D, Wallach-Dayan SB, Zahalka MA, Sionov RV. Involvement of CD44, a molecule with a thousand faces, in cancer dissemination. Seminars in cancer biology. 2008; 18:260-267.
7. Ruiz P, Schwarzler C, Gunthert U. CD44 isoforms during differentiation and development. BioEssays: news and reviews in molecular, cellular and developmental biology. 1995; 17:17-24.
8. Ross JS, Sheehan CE, Williams SS, Malfetano JH, Szyfelbein WM, Kallakury BV. Decreased CD44 standard form expression correlates with prognostic variables in ovarian carcinomas. American journal of clinical pathology. 2001; 116:122-128.
9. Cho EY, Choi Y, Chae SW, Sohn JH, Ahn GH. Immunohistochemical study of the expression of adhesion molecules in ovarian serous neoplasms. Pathology international. 2006; 56:62-70.
10. Zagorianakou N, Stefanou D, Makrydimas G, Zagorianakou P, Briasoulis E, Karavasilis B, Agnantis NJ. CD44s expression, in benign, borderline and malignant tumors of ovarian surface epithelium. Correlation with p53, steroid receptor status, proliferative indices (PCNA, MIB1) and survival. Anticancer research. 2004; 24:1665-1670.
11. Berner HS, Davidson B, Berner A, Risberg B, Kristensen GB, Trope CG, Van de Putte G, Nesland JM. Expression of CD44 in effusions of patients diagnosed with serous ovarian carcinoma-diagnostic and prognostic implications. Clinical & experimental metastasis. 2000; 18:197-202.
12. Quattrocchi L, Sisson M, Green A, Martin SG, Durrant L, Deen S. Expression of angiogenic chemokines in ovarian clear cell carcinoma. The journal of obstetrics and gynaecology research. 2013; 39:297-304.
13. Ren H, Tan ZP, Zhu X, Crosby K, Haack H, Ren JM, Beausoleil S, Moritz A, Innocenti G, Rush J, Zhang Y, Zhou XM, Gu TL, Yang YF, Comb MJ. Identification of anaplastic lymphoma kinase as a potential therapeutic target in ovarian cancer. Cancer research. 2012; 72:3312-3323.
14. Wittinger M, Vanhara P, El-Gazzar A, Savarese-Brenner B, Pils D, Anees M, Grunt TW, Sibilia M, Holcmann M, Horvat R, Schemper M, Zeillinger R, Schofer C, Dolznig H, Horak P, Krainer M. hVps37A Status affects prognosis and cetuximab sensitivity in ovarian cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2011; 17:7816-7827.
15. Downie D, McFadyen MC, Rooney PH, Cruickshank ME, Parkin DE, Miller ID, Telfer C, Melvin WT, Murray GI. Profiling cytochrome P450 expression in ovarian cancer:identification of prognostic markers. Clinical cancer research: an official journal of the American Association for Cancer Research. 2005; 11:7369-7375.
16. Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi OP. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nature medicine. 1998; 4:844-847.
17. Chiaffarino F, Parazzini F, Bosetti C, Franceschi S, Talamini R, Canzonieri V, Montella M, Ramazzotti V, La Vecchia C. Risk factors for ovarian cancer histotypes. European journal of cancer (Oxford, England: 1990). 2007; 43:1208-1213.
18. Kurian AW, Balise RR, McGuire V, Whittemore AS. Histologic types of epithelial ovarian cancer: have they different risk factors? Gynecologic oncology. 2005; 96:520-530.
19. Duan Z, Foster R, Bell DA, Mahoney J, Wolak K, Vaidya A, Hampel C, Lee H, Seiden MV. Signal transducers and activators of transcription 3 pathway activation in drug-resistant ovarian cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2006; 12:5055-5063.
20. Gallatin WM, Weissman IL, Butcher EC. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature. 1983; 304:30-34.
21. Sherman L, Sleeman J, Dall P, Hekele A, Moll J, Ponta H, Herrlich P. The CD44 proteins in embryonic development and in cancer. Current topics in microbiology and immunology. 1996; 213:249-269.
22. Pure E, Cuff CA. A crucial role for CD44 in inflammation. Trends in molecular medicine. 2001; 7:213-221.
23. Schmits R, Filmus J, Gerwin N, Senaldi G, Kiefer F, Kundig T, Wakeham A, Shahinian A, Catzavelos C, Rak J, Furlonger C, Zakarian A, Simard JJ, Ohashi PS, Paige CJ, Gutierrez-Ramos JC, et al. CD44 regulates hematopoietic progenitor distribution, granuloma formation, and tumorigenicity. Blood. 1997; 90:2217-2233.
24. Shah V, Taratula O, Garbuzenko OB, Taratula OR, Rodriguez-Rodriguez L, Minko T. Targeted nanomedicine for suppression of CD44 and simultaneous cell death induction in ovarian cancer: an optimal delivery of siRNA and anticancer drug. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19:6193-6204.
25. Li CZ, Liu B, Wen ZQ, Li HY. Inhibition of CD44 expression by small interfering RNA to suppress the growth and metastasis of ovarian cancer cells in vitro and in vivo. Folia biologica. 2008; 54:180-186.
26. Kim Y, Kumar S. CD44-Mediated Adhesion to Hyaluronic Acid Contributes to Mechanosensing and Invasive Motility. Molecular cancer research: MCR. 2014; 12:1416-1429.
27. Cheng W, Liu T, Wan X, Gao Y, Wang H. MicroRNA-199a targets CD44 to suppress the tumorigenicity and multidrug resistance of ovarian cancer-initiating cells. The FEBS journal. 2012; 279:2047-2059.
28. Ashkar S, Weber GF, Panoutsakopoulou V, Sanchirico ME, Jansson M, Zawaideh S, Rittling SR, Denhardt DT, Glimcher MJ, Cantor H. Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science (New York, NY). 2000; 287:860-864.
29. Dimitroff CJ, Lee JY, Fuhlbrigge RC, Sackstein R. A distinct glycoform of CD44 is an L-selectin ligand on human hematopoietic cells. Proceedings of the National Academy of Sciences of the United States of America. 2000; 97:13841-13846.
30. Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R. CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. The Journal of cell biology. 2001; 153:1277-1286.
31. Naor D, Sionov RV, Ish-Shalom D. CD44: structure, function, and association with the malignant process. Advances in cancer research. 1997; 71:241-319.
32. Bourguignon LY, Gilad E, Rothman K, Peyrollier K. Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling, leading to actin binding, Elk-1/ estrogen receptor transcriptional activation, and ovarian cancer progression. The Journal of biological chemistry. 2005; 280:11961-11972.
33. Carpenter PM, Dao AV. The role of hyaluronan in mesothelium- induced motility of ovarian carcinoma cells. Anticancer research. 2003; 23:3985-3990.
34. Napier SL, Healy ZR, Schnaar RL, Konstantopoulos K. Selectin ligand expression regulates the initial vascular interactions of colon carcinoma cells: the roles of CD44v and alternative sialofucosylated selectin ligands. The Journal of biological chemistry. 2007; 282:3433-3441.
35. Van Phuc P, Nhan PL, Nhung TH, Tam NT, Hoang NM, Tue VG, Thuy DT, Ngoc PK. Downregulation of CD44 reduces doxorubicin resistance of CD44CD24 breast cancer cells. OncoTargets and therapy. 2011; 4:71-78.
36. Higgins CF. Multiple molecular mechanisms for multidrug resistance transporters. Nature. 2007; 446:749-757.
37. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nature reviews Cancer. 2002; 2:48-58.
38. Yoon C, Park do J, Schmidt B, Thomas NJ, Lee HJ, Kim TS, Janjigian YY, Cohen DJ, Yoon SS. CD44 expression denotes a subpopulation of gastric cancer cells in which Hedgehog signaling promotes chemotherapy resistance. Clinical cancer research: an official journal of the American Association for Cancer Research. 2014; 20:3974-3988.
39. Lakshman M, Subramaniam V, Rubenthiran U, Jothy S. CD44 promotes resistance to apoptosis in human colon cancer cells. Experimental and molecular pathology. 2004; 77:18-25.
40. Fedorchenko O, Stiefelhagen M, Peer-Zada AA, Barthel R, Mayer P, Eckei L, Breuer A, Crispatzu G, Rosen N, Landwehr T, Lilienthal N, Mollmann M, Montesinos-Rongen M, Heukamp L, Durig J, Hallek M, et al. CD44 regulates the apoptotic response and promotes disease development in chronic lymphocytic leukemia. Blood. 2013; 121:4126-4136.
41. Cain JW, Hauptschein RS, Stewart JK, Bagci T, Sahagian GG, Jay DG. Identification of CD44 as a surface biomarker for drug resistance by surface proteome signature technology. Molecular cancer research: MCR. 2011; 9:637-647.
42. Scully RE. World Health Organization classification and nomenclature of ovarian cancer. National Cancer Institute monograph. 1975; 42:5-7.
43. Shepherd JH. Revised FIGO staging for gynaecological cancer. British journal of obstetrics and gynaecology. 1989; 96:889-892.
44. Denny L, Quinn M, Hacker N. FIGO Cancer Report 2012. International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics. 2012; 119:S89.
45. Duan Z, Feller AJ, Penson RT, Chabner BA, Seiden MV. Discovery of differentially expressed genes associated with paclitaxel resistance using cDNA array technology: analysis of interleukin (IL) 6, IL-8, and monocyte chemotactic protein 1 in the paclitaxel-resistant phenotype. Clinical cancer research: an official journal of the American Association for Cancer Research. 1999; 5:3445-3453.
46. Halder J, Landen CN Jr., Lutgendorf SK, Li Y, Jennings NB, Fan D, Nelkin GM, Schmandt R, Schaller MD, Sood AK. Focal adhesion kinase silencing augments docetaxelmediated apoptosis in ovarian cancer cells. Clinical cancer research: an official journal of the American Association for Cancer Research. 2005; 11:8829-8836.
47. Duan Z, Brakora KA, Seiden MV. Inhibition of ABCB1 (MDR1) and ABCB4 (MDR) expression by small interfering RNA and reversal of paclitaxel resistance in human ovarian cancer cells. Molecular cancer therapeutics. 2004; 3:833-838.
48. Lamendola DE, Duan Z, Yusuf RZ, Seiden MV. Molecular description of evolving paclitaxel resistance in the SKOV-3 human ovarian carcinoma cell line. Cancer research. 2003; 63:2200-2205.
49. Kittler R, Surendranath V, Heninger AK, Slabicki M, Theis M, Putz G, Franke K, Caldarelli A, Grabner H, Kozak K, Wagner J, Rees E, Korn B, Frenzel C, Sachse C, Sonnichsen B, et al. Genome-wide resources of endoribonuclease- prepared short interfering RNAs for specific loss-of-function studies. Nature methods. 2007; 4:337-344.