The ability of hyaluronan fragments to reverse the resistance of C6 rat glioma cell line to temozolomide and carmustine

Wspolczesna Onkologia

Volumn 18, Issue 5, 2014, Pages 323-328

  Karbownik, Michal Seweryn ^a   Pietras, Tadeusz ^a   Szemraj, Janusz ^a   Kowalczyk, Edward ^a   Nowak, Jerzy Zygmunt ^a,b,c  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

^b INSTITUTE OF PHARMACOLOGY   (Poland)

^c Medical Center MEDYCEUSZ in Lodz   (Poland)

Author keywords

Carmustine; CD44; Drug resistance; Glioma; Hyaluronan oligomers; Temozolomide

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CARMUSTINE; DISACCHARIDE; HYALURONAN OLIGOMER 2; HYALURONAN OLIGOMER 5; HYALURONAN POLYMER 68 KDA; HYALURONIC ACID; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; CELL VIABILITY ASSAY; CONTROLLED STUDY; CYTOTOXICITY; FOLLOW UP; GLIOMA CELL; GLIOMA CELL LINE; MTT ASSAY; NONHUMAN; RAT;

EID: 84918841656     PISSN: 14282526     EISSN: None     Source Type: Journal    
DOI: 10.5114/wo.2014.43493     Document Type: Article

References (73)

1. Lippert TH, Ruoff HJ, Volm M. Current status of methods to assess cancer drug resistance. Int J Med Sci 2011; 8: 245-53.
2. Liu FS. Mechanisms of chemotherapeutic drug resistance in cancer therapy - a quick review. Taiwan J Obstet Gynecol 2009; 48: 239-44.
3. Gottesman MM. Mechanisms of cancer drug resistance. Annu Rev Med 2002; 53: 615-27.
4. Huang Y. Pharmacogenetics/genomics of membrane transporters in cancer chemotherapy. Cancer Metastasis Rev 2007; 26: 183-201.
5. Damaraju VL, Damaraju S, Young JD, Baldwin SA, Mackey J, Sawyer MB, Cass CE. Nucleoside anticancer drugs: the role of nucleoside transporters in resistance to cancer chemotherapy. Oncogene 2003; 22: 7524-36.
6. Sun YL, Patel A, Kumar P, Chen ZS. Role of ABC transporters in cancer chemotherapy. Chin J Cancer 2012; 31: 51-7.
7. Nobili S, Landini I, Mazzei T, Mini E. Overcoming tumor multidrug resistance using drugs able to evade P-glycoprotein or to exploit its expression. Med Res Rev 2012; 32: 1220-62.
8. Bardenheuer W, Lehmberg K, Rattmann I, et al. Resistance to cytarabine and gemcitabine and in vitro selection of transduced cells after retroviral expression of cytidine deaminase in human hematopoietic progenitor cells. Leukemia 2005;19: 2281-8.
9. Kasahara K, Fujiwara Y, Nishio K, Ohmori T, Sugimoto Y, Komiya K, Matsuda T, Saijo N. Metallothionein content correlates with the sensitivity of human small cell lung cancer cell lines to cisplatin. Cancer Res 1991; 51: 3237-42.
10. Rochat B. Role of cytochrome P450 activity in the fate of anticancer agents and in drug resistance: focus on tamoxifen, paclitaxel and imatinib metabolism. Clin Pharmacokinet 2005; 44: 349-66.
11. Bean J, Riely GJ, Balak M, Marks JL, Ladanyi M, Miller VA, Pao W. Acquired resistance to epidermal growth factor receptor kinase inhibitors associated with a novel T854A mutation in a patient with EGFR-mutant lung adenocarcinoma. Clin Cancer Res 2008; 14: 7519-25.
12. Apperley JF. Part I: mechanisms of resistance to imatinib in chronic myeloid leukaemia. Lancet Oncol 2007; 8: 1018-29.
13. Engelman JA, Zejnullahu K, Mitsudomi T, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-43.
14. Jiang G, Li LT, Xin Y, Zhang L, Liu YQ, Zheng JN. Strategies to improve the killing of tumors using temozolomide: targeting the DNA repair protein MGMT. Curr Med Chem 2012; 19: 3886-92.
15. Wilson TR, Johnston PG, Longley DB. Anti-apoptotic mechanisms of drug resistance in cancer. Curr Cancer Drug Targets 2009; 9: 307-19.
16. Reed JC. Apoptosis mechanisms: implications for cancer drug discovery. Oncology (Williston Park) 2004; 18: 11-20.
17. Wysocki PJ, Korski K, Lamperska K, Zaluski J, Mackiewicz A. Primary resistance to docetaxel-based chemotherapy in metastatic breast cancer patients correlates with a high frequency of BRCA1 mutations. Med Sci Monit 2008; 14: SC7-10.
18. Zahreddine H, Borden KL. Mechanisms and insights into drug resistance in cancer. Front Pharmacol 2013; 4: 28.
19. Meads MB, Gatenby RA, Dalton WS. Environment-mediated drug resistance: a major contributor to minimal residual disease. Nat Rev Cancer 2009; 9: 665-74.
20. Correia AL, Bissell MJ. The tumor microenvironment is a dominant force in multidrug resistance. Drug Resist Updat 2012; 15: 39-49.
21. Frassanito MA, Cusmai A, Iodice G, Dammacco F. Autocrine interleukin- 6 production and highly malignant multiple myeloma: relation with resistance to drug-induced apoptosis. Blood 2001; 97: 483-9.
22. Voorhees PM, Chen Q, Kuhn DJ, et al. Inhibition of interleukin-6 signaling with CNTO 328 enhances the activity of bortezomib in preclinical models of multiple myeloma. Clin Cancer Res 2007; 13: 6469-78.
23. Hazlehurst LA, Argilagos RF, Dalton WS. Beta1 integrin mediated adhesion increases Bim protein degradation and contributes to drug resistance in leukaemia cells. Br J Haematol 2007; 136: 269-75.
24. Toole BP, Slomiany MG. Hyaluronan: a constitutive regulator of chemoresistance and malignancy in cancer cells. Semin Cancer Biol 2008; 18: 244-50.
25. Laurent TC. Biochemistry of hyaluronan. Acta Otolaryngol Suppl 1987; 442: 7-24.
26. Laurent TC, Fraser JR. Hyaluronan. FASEB J 1992; 6: 2397-404.
27. Fraser JR, Laurent TC, Laurent UB. Hyaluronan: its nature, distribution, functions and turnover. J Intern Med 1997; 242: 27-33.
28. Provenzano PP, Hingorani SR. Hyaluronan, fluid pressure, and stromal resistance in pancreas cancer. Br J Cancer 2013; 108: 1-8.
29. Jacobetz MA, Chan DS, Neesse A, et al. Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer. Gut 2013; 62: 112-20.
30. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 2004; 4: 528-39.
31. Vabres P. Hyaluronan, embryogenesis and morphogenesis. Ann Dermatol Venereol 2010; 137 Suppl 1: S9-S14.
32. Bollyky PL, Bogdani M, Bollyky JB, Hull RL, Wight TN. The role of hyaluronan and the extracellular matrix in islet inflammation and immune regulation. Curr Diab Rep 2012; 12: 471-80.
33. Olczyk P, Komosiska-Vassev K, Winsz-Szczotka K, Kunik-Trocha K, Olczyk K. Hyaluronan: structure, metabolism, functions, and role in wound healing. Postepy Hig Med Dosw (Online) 2008; 62: 651-9.
34. Karbownik MS, Nowak JZ. Hyaluronan in cancer - pathophysiology and pharmacotherapy perspectives. J Oncol 2011; 61: 380-95.
35. Negi LM, Talegaonkar S, Jaggi M, Ahmad FJ, Iqbal Z, Khar RK. Role of CD44 in tumour progression and strategies for targeting. J Drug Target 2012; 20: 561-73.
36. Misra S, Heldin P, Hascall VC, Karamanos NK, Skandalis SS, Markwald RR, Ghatak S. Hyaluronan-CD44 interactions as potential targets for cancer therapy. FEBS J 2011; 278: 1429-43.
37. Karbownik MS, Nowak JZ. Hyaluronan: towards novel anti-cancer therapeutics. Pharmacol Rep 2013; 65: 1056-74.
38. Xu Y, Stamenkovic I, Yu Q. CD44 attenuates activation of the hippo signaling pathway and is a prime therapeutic target for glioblastoma. Cancer Res 2010; 70: 2455-64.
39. da Cunha CB, Oliveira C, Wen X, et al. De novo expression of CD44 variants in sporadic and hereditary gastric cancer. Lab Invest 2010; 90: 1604-14.
40. Desai B, Ma T, Zhu J, Chellaiah MA. Characterization of the expression of variant and standard CD44 in prostate cancer cells: identification of the possible molecular mechanism of CD44/MMP9 complex formation on the cell surface. J Cell Biochem 2009; 108: 272-84.
41. Wang SJ, Wong G, de Heer AM, Xia W, Bourguignon LY. CD44 variant isoforms in head and neck squamous cell carcinoma progression. Laryngoscope 2009; 119: 1518-30.
42. Liu CM, Chang CH, Yu CH, Hsu CC, Huang LL. Hyaluronan substratum induces multidrug resistance in human mesenchymal stem cells via CD44 signaling. Cell Tissue Res 2009; 336: 465-75.
43. Torre C, Wang SJ, Xia W, Bourguignon LY. Reduction of hyaluronan- CD44-mediated growth, migration, and cisplatin resistance in head and neck cancer due to inhibition of Rho kinase and PI-3 kinase signaling. Arch Otolaryngol Head Neck Surg 2010; 136: 493-501.
44. Wang SJ, Bourguignon LY. Role of hyaluronan-mediated CD44 signaling in head and neck squamous cell carcinoma progression and chemoresistance. Am J Pathol 2011; 178: 956-63.
45. Bourguignon LY, Earle C, Wong G, Spevak CC, Krueger K. Stem cell marker (Nanog) and Stat-3 signaling promote MicroRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells. Oncogene 2012; 31: 149-60.
46. Misra S, Ghatak S, Zoltan-Jones A, Toole BP. Regulation of multidrug resistance in cancer cells by hyaluronan. J Biol Chem 2003; 278: 25285-8.
47. Ghatak S, Misra S, Toole BP. Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J Biol Chem 2002; 277: 38013-20.
48. Misra S, Ghatak S, Toole BP. Regulation of MDR1 expression and drug resistance by a positive feedback loop involving hyaluronan, phosphoinositide 3-kinase, and ErbB2. J Biol Chem 2005; 280: 20310-5.
49. Ohashi R, Takahashi F, Cui R, et al. Interaction between CD44 and hyaluronate induces chemoresistance in non-small cell lung cancer cell. Cancer Lett 2007; 252: 225-34.
50. Gilg AG, Tye SL, Tolliver LB, et al. Targeting hyaluronan interactions in malignant gliomas and their drug-resistant multipotent progenitors. Clin Cancer Res 2008; 14: 1804-13.
51. Bacso Z, Nagy H, Goda K, Bene L, Fenyvesi F, Matko J, Szabo G. Raft and cytoskeleton associations of an ABC transporter: P-glycoprotein. Cytometry A 2004; 61: 105-16.
52. Coley HM. Overcoming multidrug resistance in cancer: clinical studies of p-glycoprotein inhibitors. Methods Mol Biol 2010; 596: 341-58.
53. Baird RD, Kaye SB. Drug resistance reversal - are we getting closer? Eur J Cancer 2003; 39: 2450-61.
54. Lompardia SL, Papademetrio DL, Mascaro M, Alvarez EM, Hajos SE. Human leukaemic cell lines synthesize hyaluronan to avoid senescence and resist chemotherapy. Glycobiology 2013; 12: 1463-76.
55. Qin Z, Dai L, Bratoeva M, Slomiany MG, Toole BP, Parsons C. Cooperative roles for emmprin and LYVE-1 in the regulation of chemoresistance for primary effusion lymphoma. Leukemia 2011; 25: 1598-609.
56. Slomiany MG, Dai L, Bomar PA, Knackstedt TJ, Kranc DA, Tolliver L, Maria BL, Toole BP. Abrogating drug resistance in malignant peripheral nerve sheath tumors by disrupting hyaluronan-CD44 interactions with small hyaluronan oligosaccharides. Cancer Res 2009; 69: 4992-8.
57. Cui X, Zhou S, Xu H, Zhao T, Liu A, Guo X, Wang F. Reversal effects of hyaluronan oligosaccharides on adriamycin resistance of K562/A02 cells. Anticancer Drugs. 2009; 20: 800-6.
58. Toole BP, Ghatak S, Misra S. Hyaluronan oligosaccharides as a potential anticancer therapeutic. Curr Pharm Biotechnol 2008; 9: 249-52.
59. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352: 987-96.
60. Brandes AA, Tosoni A, Franceschi E, Reni M, Gatta G, Vecht C. Glioblastoma in adults. Crit Rev Oncol Hematol 2008; 67: 139-52.
61. Murat A, Migliavacca E, Gorlia T, et al. Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol 2008; 26: 3015-24.
62. Brandes AA, Fiorentino MV. The role of chemotherapy in recurrent malignant gliomas: an overview. Cancer Invest 1996; 14: 551-9.
63. Sarkaria JN, Kitange GJ, James CD, Plummer R, Calvert H, Weller M, Wick W. Mechanisms of chemoresistance to alkylating agents in malignant glioma. Clin Cancer Res 2008; 14: 2900-8.
64. Peignan L, Garrido W, Segura R, Melo R, Rojas D, Carcamo JG, San Martin R, Quezada C. Combined use of anticancer drugs and an inhibitor of multiple drug resistance-associated protein-1 increases sensitivity and decreases survival of glioblastoma multiforme cells in vitro. Neurochem Res 2011; 36: 1397-406.
65. Lesley J, Hascall VC, Tammi M, Hyman R. Hyaluronan binding by cell surface CD44. J Biol Chem 2000; 275: 26967-75.
66. Ostermann S, Csajka C, Buclin T, Leyvraz S, Lejeune F, Decosterd LA, Stupp R. Plasma and cerebrospinal fluid population pharmacokinetics of temozolomide in malignant glioma patients. Clin Cancer Res 2004; 10: 3728-36.
67. Portnow J, Badie B, Chen M, Liu A, Blanchard S, Synold TW. The neuropharmacokinetics of temozolomide in patients with resectable brain tumors: potential implications for the current approach to chemoradiation. Clin Cancer Res 2009; 15: 7092-8.
68. Henner WD, Peters WP, Eder JP, Antman K, Schnipper L, Frei E 3rd. Pharmacokinetics and immediate effects of high-dose carmustine in man. Cancer Treat Rep 1986; 70: 877-80.
69. Lin SH, Kleinberg LR. Carmustine wafers: localized delivery of chemotherapeutic agents in CNS malignancies. Expert Rev Anticancer Ther 2008; 8: 343-59.
70. Knupfer MM, Poppenborg H, Hotfilder M, Domula M, Wolff JE. Hyaluronic acid binding capacity of malignant glioma cells. Anticancer Res 1998; 18: 353-6.
71. Zhou XD, Wang XY, Qu FJ, et al. Detection of cancer stem cells from the C6 glioma cell line. J Int Med Res 2009; 37: 503-10.
72. Shen G, Shen F, Shi Z, Liu W, Hu W, Zheng X, Wen L, Yang X. Identification of cancer stem-like cells in the C6 glioma cell line and the limitation of current identification methods. In Vitro Cell Dev Biol Anim 2008; 44: 280-9.
73. Gillet JP, Varma S, Gottesman MM. The clinical relevance of cancer cell lines. J Natl Cancer Inst 2013; 105: 452-8.