Acyclic Cucurbit[n]uril-Type Molecular Container Enables Systemic Delivery of Effective Doses of Albendazole for Treatment of SK-OV-3 Xenograft Tumors

Molecular Pharmaceutics

Volumn 13, Issue 3, 2016, Pages 809-818

  Hettiarachchi, Gaya ^a   Samanta, Soumen K ^a   Falcinelli, Shane ^a   Zhang, Ben ^a   Moncelet, Damien ^a   Isaacs, Lyle ^a   Briken, Volker ^a  

^a University of Maryland   (United States)

Author keywords

albendazole; cancer; cucurbit n uril; drug delivery; excipient; molecular container; solubility

Indexed keywords

ALBENDAZOLE; ALBENDAZOLE SULFOXIDE; ANTINEOPLASTIC AGENT; DRUG METABOLITE; POTASSIUM CHANNEL HERG; ANTHELMINTIC AGENT; BRIDGED COMPOUND; CUCURBIT(7)URIL; EXCIPIENT; IMIDAZOLE DERIVATIVE;

ACYCLIC CUCURBIT[N]URIL TYPE MOLECULAR CONTAINER; AMES TEST; AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG DELIVERY DEVICE; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG SOLUBILITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FRAMESHIFT MUTATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAXIMUM TOLERATED DOSE; MISSENSE MUTATION; MOUSE; NONHUMAN; PATCH CLAMP TECHNIQUE; PERITONEAL CAVITY; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TUMOR GROWTH; TUMOR VOLUME; TUMOR XENOGRAFT; ANIMAL; BIOAVAILABILITY; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; DRUG FORMULATION; DRUG SCREENING; FEMALE; METABOLISM; OVARIAN NEOPLASMS; PATHOLOGY;

ALBENDAZOLE; ANIMALS; ANTHELMINTICS; BIOLOGICAL AVAILABILITY; BRIDGED-RING COMPOUNDS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMPOUNDING; DRUG DELIVERY SYSTEMS; ETHER-A-GO-GO POTASSIUM CHANNELS; EXCIPIENTS; FEMALE; HUMANS; IMIDAZOLES; MAXIMUM TOLERATED DOSE; MICE; OVARIAN NEOPLASMS; SALMONELLA TYPHIMURIUM; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84960192552     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/acs.molpharmaceut.5b00723     Document Type: Article

References (64)

1. Williams, H. D.; Trevaskis, N. L.; Charman, S. A.; Shanker, R. M.; Charman, W. N.; Pouton, C. W.; Porter, C. J. H. Strategies to address low drug solubility in discovery and development Pharmacol. Rev. 2013, 65, 315-499 10.1124/pr.112.005660
2. Savjani, K. T.; Gajjar, A. K.; Savjani, J. K. Drug Solubility: Importance and Enhancement Techniques ISRN Pharm. 2012, 2012, 1-10 10.5402/2012/195727
3. Barenholz, Y. Doxil® - the first FDA-approved nano-drug: lessons learned J. Controlled Release 2012, 160, 117-134 10.1016/j.jconrel.2012.03.020
4. Stella, V. J.; He, Q. Cyclodextrins Toxicol. Pathol. 2008, 36, 30-42 10.1177/0192623307310945
5. Ligand Pharmaceuticals, Inc. Captisol + Partnerships &Collaborations, Url. (n.d.). http://www.captisol.com/partnerships-collaborations/ (accessed May 1, 2015).
6. Lee, J. W.; Samal, S.; Selvapalam, N.; Kim, H.-J.; Kim, K. Cucurbituril Homologues and Derivatives: New Opportunities in Supramolecular Chemistry Acc. Chem. Res. 2003, 36, 621-630 10.1021/ar020254k
7. Lagona, J.; Mukhopadhyay, P.; Chakrabarti, S.; Isaacs, L. The cucurbit[n]uril family Angew. Chem., Int. Ed. 2005, 44, 4844-4870 10.1002/anie.200460675
8. Macartney, D. H. Encapsulation of Drug Molecules by Cucurbiturils: Effects on their Chemical Properties in Aqueous Solution Isr. J. Chem. 2011, 51, 600-615 10.1002/ijch.201100040
9. Masson, E.; Ling, X.; Joseph, R.; Kyeremeh-Mensah, L.; Lu, X. Cucurbituril Chemistry: A Tale of Supramolecular Success RSC Adv. 2012, 2, 1213-1247 10.1039/C1RA00768H
10. Nau, W. M.; Florea, M.; Assaf, K. I. Deep Inside Cucurbiturils: Physical Properties and Volumes of their Inner Cavity Determine the Hydrophobic Driving Force for Host-Guest Complexation Isr. J. Chem. 2011, 51, 559-577 10.1002/ijch.201100044
11. Walker, S.; Oun, R.; McInnes, F. J.; Wheate, N. J. The Potential of Cucurbit[n]urils in Drug Delivery Isr. J. Chem. 2011, 51, 616-624 10.1002/ijch.201100033
12. Cao, L.; ͆ekutor, M.; Zavalij, P. Y.; Mlinarić-Majerski, K.; Glaser, R.; Isaacs, L. Cucurbit[7]uril. Guest Pair with an Attomolar Dissociation Constant Angew. Chem., Int. Ed. 2014, 53, 988-993 10.1002/anie.201309635
13. Liu, S.; Ruspic, C.; Mukhopadhyay, P.; Chakrabarti, S.; Zavalij, P. Y.; Isaacs, L. The Cucurbit[n]uril Family: Prime Components for Self-Sorting Systems J. Am. Chem. Soc. 2005, 127, 15959-15967 10.1021/ja055013x
14. Mock, W. L.; Shih, N. Y. Structure and selectivity in host-guest complexes of cucurbituril J. Org. Chem. 1986, 51, 4440-4446 10.1021/jo00373a018
15. Rekharsky, M. V.; Mori, T.; Yang, C.; Ko, Y. H.; Selvapalam, N.; Kim, H.; Sobransingh, D.; Kaifer, A. E.; Liu, S.; Isaacs, L.; Chen, W.; Moghaddam, S.; Gilson, M. K.; Kim, K.; Inoue, Y. A synthetic host-guest system achieves avidin-biotin affinity by overcoming enthalpy-entropy compensation Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 20737-20742 10.1073/pnas.0706407105
16. Biedermann, F.; Uzunova, V. D.; Scherman, O. A.; Nau, W. M.; De Simone, A. Release of high-energy water as an essential driving force for the high-affinity binding of cucurbit[n]urils J. Am. Chem. Soc. 2012, 134, 15318-15323 10.1021/ja303309e
17. Hettiarachchi, G.; Nguyen, D.; Wu, J.; Lucas, D.; Ma, D.; Isaacs, L.; Briken, V. Toxicology and drug delivery by cucurbit[n]uril type molecular containers PLoS One 2010, 5, e10514 10.1371/journal.pone.0010514
18. Plumb, J. A.; Venugopal, B.; Oun, R.; Gomez-Roman, N.; Kawazoe, Y.; Venkataramanan, N. S.; Wheate, N. J. Cucurbit[7]uril encapsulated cisplatin overcomes cisplatin resistance via a pharmacokinetic effect Metallomics 2012, 4, 561-567 10.1039/c2mt20054f
19. Uzunova, V. D.; Cullinane, C.; Brix, K.; Nau, W. M.; Day, A. I. Toxicity of cucurbit[7]uril and cucurbit[8]uril: An exploratory in vitro and in vivo study Org. Biomol. Chem. 2010, 8, 2037-2042 10.1039/b925555a
20. Walker, S.; Kaur, R.; McInnes, F. J.; Wheate, N. J. Synthesis, Processing and Solid State Excipient Interactions of Cucurbit[6]uril and Its Formulation into Tablets for Oral Drug Delivery Mol. Pharmaceutics 2010, 7, 2166-2172 10.1021/mp100191b
21. Dong, N.; Xue, S. F.; Zhu, Q. J.; Tao, Z.; Zhao, Y.; Yang, L. X. Cucurbit[n]urils (n = 7, 8) binding of camptothecin and the effects on solubility and reactivity of the anticancer drug Supramol. Chem. 2008, 20, 659-665 10.1080/10610270701666018
22. Dong, N.; Wang, X.; Pan, J.; Tao, Z. Influence of Cucurbit(n = 7,8-uril on the Solubility and Stability of Chlorambucil. Acta Chim. Sinica. 2011, 69, 1431-1437
23. Zhao, Y.; Buck, D. P.; Morris, D. L.; Pourgholami, M. H.; Day, A. I.; Collins, J. G. Solubilisation and cytotoxicity of albendazole encapsulated in cucurbit[n]uril Org. Biomol. Chem. 2008, 6, 4509 10.1039/b813759e
24. Koner, A. L. K. L.; Ghosh, I.; Saleh, N.; Nau, W. M. N. M. Supramolecular encapsulation of benzimidazole-derived drugs by cucurbit[7]uril Can. J. Chem. 2011, 89, 139-147 10.1139/V10-079
25. Jeon, Y. J.; Kim, S.-Y.; Ko, Y. H.; Sakamoto, S.; Yamaguchi, K.; Kim, K. Novel molecular drug carrier: encapsulation of oxaliplatin in cucurbit[7]uril and its effects on stability and reactivity of the drug Org. Biomol. Chem. 2005, 3, 2122-2125 10.1039/b504487a
26. McInnes, F. J.; Anthony, N. G.; Kennedy, A. R.; Wheate, N. J. Solid state stabilisation of the orally delivered drugs atenolol, glibenclamide, memantine and paracetamol through their complexation with cucurbit[7]uril Org. Biomol. Chem. 2010, 8, 765-773 10.1039/b918372h
27. Miskolczy, Z.; Megyesi, M.; Tárkányi, G.; Mizsei, R.; Biczók, L. Inclusion complex formation of sanguinarine alkaloid with cucurbit[7]uril: inhibition of nucleophilic attack and photooxidation Org. Biomol. Chem. 2011, 9, 1061-1070 10.1039/C0OB00666A
28. Saleh, N.; Koner, A. L.; Nau, W. M. Activation and Stabilization of Drugs by Supramolecular pKa Shifts: Drug-Delivery Applications Tailored for Cucurbiturils Angew. Chem. 2008, 120, 5478-5481 10.1002/ange.200801054
29. Jung, H.; Park, K. M.; Yang, J.-A.; Oh, E. J.; Lee, D.-W.; Park, K.; Ryu, S. H.; Hahn, S. K.; Kim, K. Theranostic systems assembled in situ on demand by host-guest chemistry Biomaterials 2011, 32, 7687-7694 10.1016/j.biomaterials.2011.06.060
30. Kim, E.; Kim, D.; Jung, H.; Lee, J.; Paul, S.; Selvapalam, N.; Yang, Y.; Lim, N.; Park, K.; Kim, C. G. Facile, Template-Free Synthesis of Stimuli-Responsive Polymer Nanocapsules for Targeted Drug Delivery Angew. Chem. 2010, 122, 4507-4510 10.1002/ange.201000818
31. Loh, X. J.; del Barrio, J.; Toh, P. P. C.; Lee, T.-C.; Jiao, D.; Rauwald, U.; Appel, E. A.; Scherman, O. A. Triply Triggered Doxorubicin Release From Supramolecular Nanocontainers Biomacromolecules 2011, 13, 84-91 10.1021/bm201588m
32. Park, K. M.; Suh, K.; Jung, H.; Lee, D.-W.; Ahn, Y.; Kim, J.; Baek, K.; Kim, K. Cucurbituril -based nanoparticles: A new efficient vehicle for targeted intracellular delivery of hydrophobic drugs Chem. Commun. 2009, 0, 71-73 10.1039/B815009E
33. Cao, L.; Hettiarachchi, G.; Briken, V.; Isaacs, L. Cucurbit[7]uril Containers for Targeted Delivery of Oxaliplatin to Cancer Cells Angew. Chem., Int. Ed. 2013, 52, 12033-12037 10.1002/anie.201305061
34. MA, W. J.; Chen, J. M.; Jiang, L.; Yao, J.; Lu, T. B. The Delivery of Triamterene by Cucurbit[7]uril: Synthesis, Structures and Pharmacokinetics Study Mol. Pharmaceutics 2013, 10, 4698-705 10.1021/mp400529m
35. Lee, J. W.; Samal, S.; Selvapalam, N.; Kim, H. J.; Kim, K. Cucurbituril homologues and derivatives: new opportunities in supramolecular chemistry Acc. Chem. Res. 2003, 36, 621-30 10.1021/ar020254k
36. Ma, D.; Hettiarachchi, G.; Nguyen, D.; Zhang, B.; Wittenberg, J. B.; Zavalij, P. Y.; Briken, V.; Isaacs, L. Acyclic cucurbit[n]uril molecular containers enhance the solubility and bioactivity of poorly soluble pharmaceuticals Nat. Chem. 2012, 4, 503-510 10.1038/nchem.1326
37. Zhang, B.; Isaacs, L. Acyclic cucurbit[n]uril-type molecular containers: influence of aromatic walls on their function as solubilizing excipients for insoluble drugs J. Med. Chem. 2014, 57, 9554-9563 10.1021/jm501276u
38. Zhang, B.; Zavalij, P. Y.; Isaacs, L. Acyclic CB[n]-type molecular containers: effect of solubilizing group on their function as solubilizing excipients Org. Biomol. Chem. 2014, 12, 2413-2422 10.1039/C3OB42603C
39. Gilberg, L.; Zhang, B.; Zavalij, P. Y.; Sindelar, V.; Isaacs, L. Acyclic cucurbit[n]uril-type molecular containers: influence of glycoluril oligomer length on their function as solubilizing agents Org. Biomol. Chem. 2015, 13, 4041-4050 10.1039/C5OB00184F
40. Bernard, W. S.; Christopher, P. W. World Cancer Report 2014; International Agency for Research on Cancer, World Health Organization, 2014.
41. Lacey, E. Mode of action of benzimidazoles Parasitol. Today 1990, 6, 112-115 10.1016/0169-4758(90)90227-U
42. Barrowman, M. M.; Marriner, S. E.; Bogan, J. A. The binding and subsequent inhibition of tubulin polymerization in Ascaris suum (in vitro) by benzimidazole anthelmintics Biochem. Pharmacol. 1984, 33, 3037-3040 10.1016/0006-2952(84)90605-1
43. Morris, D. L.; Jourdan, J. L.; Pourgholami, M. H. Pilot study of albendazole in patients with advanced malignancy. Effect on serum tumor markers/high incidence of neutropenia Oncology 2001, 61, 42-46 10.1159/000055351
44. Pourgholami, M. H.; Szwajcer, M.; Chin, M.; Liauw, W.; Seef, J.; Galettis, P.; Morris, D. L.; Links, M. Cancer Chemother. Pharmacol. 2010, 65, 597-605 10.1007/s00280-009-1157-8
45. Marriner, S. E.; Morris, D. L.; Dickson, B.; Bogan, J. A. Pharmacokinetics of albendazole in man Eur. J. Clin. Pharmacol. 1986, 30, 705-708 10.1007/BF00608219
46. Connors, K. A. Binding Constants; John Wiley and Sons: New York, 1987; pp 261-281.
47. Higuchi, T.; Connors, K. A. Phase-Solubility Techniques Adv. Anal. Chem. Instrum. 1965, 4, 117-212
48. Hoffmann, U.; Grosse-Sundrup, M.; Eikermann-Haerter, K.; Zaremba, S.; Ayata, C.; Zhang, B.; Ma, D.; Isaacs, L.; Eikermann, M. Calabadion: A new agent to reverse the effects of benzylisoquinoline and steroidal neuromuscular-blocking agents Anesthesiology 2013, 119, 317-325 10.1097/ALN.0b013e3182910213
49. Mortelmans, K.; Zeiger, E. The Ames Salmonella/microsome mutagenicity assay Mutat. Res., Fundam. Mol. Mech. Mutagen. 2000, 455, 29-60 10.1016/S0027-5107(00)00064-6
50. Gintant, G. A.; Su, Z.; Martin, R. L.; Cox, B. F. Utility of hERG assays as surrogate markers of delayed cardiac repolarization and QT safety Toxicol. Pathol. 2006, 34, 81-90 10.1080/01926230500431376
51. Roche, O.; Trube, G.; Zuegge, J.; Pflimlin, P.; Alanine, A.; Schneider, G. A virtual screening method for prediction of the HERG potassium channel liability of compound libraries ChemBioChem 2002, 3, 455-459 10.1002/1439-7633(20020503)3:5<455::AID-CBIC455>3.0.CO;2-L
52. Pourgholami, M. H.; Wangoo, K. T.; Morris, D. L. Albendazole-Cyclodextrin Complex: Enhanced Cytotoxicity in Ovarian Cancer Cells Anticancer Res. 2008, 28, 2775-2779
53. Pourgholami, M. H.; Cai, Z. Y.; CHU, S. W. L.; Galettis, P.; Morris, D. L. The Influence of Ovarian Cancer Induced Peritoneal Carcinomatosis on the Pharmacokinetics of Albendazole in Nude Mice Anticancer Res. 2010, 30, 423-428
54. Food and Drug Administration. HHS, International Conference onHarmonisation; guidance on S7Asafety pharmacology studies for human pharmaceuticals; availability.Notice. Fed Regist. (2001, 66, 36791-36792.
55. Carr, D. B.; McDonnell Moorehead, T.; Bouchard, A.; Sprenger, C. R.; Hamilton, D. A.; Lang, E.; Madden, D.; Lacouture, P. G.; Wright, C., IV Effects of injectable HPβCD-diclofenac on the human delayed rectifier potassium channel current in vitro and on proarrhythmic QTc in vivo Clin. Ther. 2013, 35, 646-658 10.1016/j.clinthera.2013.03.014
56. Mikhail, A.; Fischer, C.; Patel, A.; Long, M. A.; Limberis, J. T.; Martin, R. L.; Cox, B. F.; Gintant, G. A.; Su, Z. Hydroxypropyl beta-cyclodextrins: A misleading vehicle for the in vitro hERG current assay J. Cardiovasc. Pharmacol. 2007, 49, 269-274 10.1097/FJC.0b013e318036dd05
57. de Kam, P.-J.; van Kuijk, J.; Smeets, J.; Thomsen, T.; Peeters, P. Sugammadex is not associated with QT/QTc prolongation: methodology aspects of an intravenous moxifloxacin-controlled thorough QT study Int. J. Clin. Pharmacol. Ther. 2012, 50, 595-604 10.5414/CP201693
58. Ehteda, A.; Galettis, P.; CHU, S. W. L.; Pillai, K.; Morris, D. L. Complexation of Albendazole with Hydroxypropyl-β-Cyclodextrin Significantly Improves its Pharmacokinetic Profile, Cell Cytotoxicity and Antitumor Efficacy in Nude Mice Anticancer Res. 2012, 32, 3659-3666
59. Cai, Z.-Y.; Galettis, P.; Lu, Y.; Morris, D. L.; Pourgholami, M. H. Pharmacokinetics of albendazole in New Zealand white rabbits: Oral versus intraperitoneal administration Anticancer Res. 2007, 27, 417-422
60. Hossein Pourgholami, M. Albendazole: A Potent Inhibitor of Vascular Endothelial Growth Factor and Malignant Ascites Formation in OVCAR-3 Tumor-Bearing Nude Mice Clin. Cancer Res. 2006, 12, 1928-1935 10.1158/1078-0432.CCR-05-1181
61. Dayan, A. D. Albendazole, mebendazole and praziquantel. Review of non-clinical toxicity and pharmacokinetics Acta Trop. 2003, 86, 141-159 10.1016/S0001-706X(03)00031-7
62. Pourgholami, M. H.; Akhter, J.; Wang, L.; Lu, Y.; Morris, D. L. Antitumor activity of albendazole against the human colorectal cancer cell line HT-29: in vitro and in a xenograft model of peritoneal carcinomatosis Cancer Chemother. Pharmacol. 2005, 55, 425-432 10.1007/s00280-004-0927-6
63. Bai, R.-Y; Staedtke, V.; Aprhys, C. M.; Gallia, G. L.; Riggins, G. J. Antiparasitic mebendazole shows survival benefit in 2 preclinical models of glioblastoma multiforme Neuro-Oncology 2011, 13, 974-982 10.1093/neuonc/nor077
64. Pourgholami, M. H.; Woon, L.; Almajd, R.; Akhter, J.; Bowery, P.; Morris, D. L. In vitro and in vivo suppression of growth of hepatocellular carcinoma cells by albendazole Cancer Lett. 2001, 165, 43-49 10.1016/S0304-3835(01)00382-2