Increasing oral absorption of polar neuraminidase inhibitors: A prodrug transporter approach applied to oseltamivir analogue

Molecular Pharmaceutics

Volumn 10, Issue 2, 2013, Pages 512-522

  Gupta, Deepak ^a,d   Varghese Gupta, Sheeba ^b   Dahan, Arik ^e   Tsume, Yasuhiro ^a   Hilfinger, John ^c   Lee, Kyung Dall ^a   Amidon, Gordon L ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c TSRL INC   (United States)

^d LAKE ERIE COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

^e BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

antiviral; Caco 2 permeability; Gly Sar; influenza; intestinal permeability; neuraminidase; oral absorption; oseltamivir; PEPT1; prodrugs; rat perfusion; stability; transporter; valacyclovirase

Indexed keywords

AMINO ACID DERIVATIVE; CARBOXYLIC ACID DERIVATIVE; GUANIDINE DERIVATIVE; GUANIDINE OSELTAMIVIR CARBOXYLATE; GUANIDINE OSELTAMIVIR CARBOXYLATE ISOLEUCINE; GUANIDINE OSELTAMIVIR CARBOXYLATE LEUCINE; GUANIDINE OSELTAMIVIR CARBOXYLATE VALINE; METOPROLOL; OSELTAMIVIR; PEPTIDE TRANSPORTER 1; PRODRUG; SIALIDASE INHIBITOR; UNCLASSIFIED DRUG; VALACICLOVIR;

ANIMAL CELL; APICAL MEMBRANE; AREA UNDER THE CURVE; ARTICLE; BINDING AFFINITY; BRUSH BORDER; CELL ACTIVATION; CELL FREE SYSTEM; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE TRANSPORT; CELL TRANSPORT; CONTROLLED STUDY; DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG COMPETITION; DRUG HALF LIFE; DRUG HYDROLYSIS; DRUG PENETRATION; DRUG STABILITY; DRUG TARGETING; DRUG TRANSPORT; DRUG UPTAKE; ENZYME STABILITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTESTINE PERFUSION; JEJUNUM; MAXIMUM PLASMA CONCENTRATION; NONHUMAN; ORAL DRUG ADMINISTRATION; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TIME TO MAXIMUM PLASMA CONCENTRATION;

ANIMALS; ANTIVIRAL AGENTS; CACO-2 CELLS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEURAMINIDASE; OSELTAMIVIR; PRODRUGS; RATS;

EID: 84873325984     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300564v     Document Type: Article

References (43)

1. Couch, R. B. Advances in influenza virus vaccine research Ann. N.Y. Acad. Sci. 1993, 685, 803-12 (Pubitemid 23238566)
2. Belshe, R. B.; Burk, B.; Newman, F.; Cerruti, R. L.; Sim, I. S. Resistance of influenza A virus to amantadine and rimantadine: results of one decade of surveillance J. Infect. Dis. 1989, 159 (3) 430-5 (Pubitemid 19065888)
3. Hayden, F. G.; Hay, A. J. Emergence and transmission of influenza A viruses resistant to amantadine and rimantadine Curr. Top. Microbiol. Immunol. 1992, 176, 119-30
4. Palese, P.; Tobita, K.; Ueda, M.; Compans, R. W. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase Virology 1974, 61 (2) 397-410
5. Burnet, F. M. Mucins and mucoids in relation to influenza virus action. IV. Inhibition by purified mucoid of infection and hemagglutination with the virus strain WSE Aust. J. Exp. Biol. Med. Sci. 1948, 26, 381-387
6. Klenk, H.-D. R., R. The molecular biology of influenza virus pathogenicity Adv. Virus Res. 1988, 34, 247-280
7. McKimm-Breschkin, J. L. Resistance of influenza viruses to neuraminidase inhibitors-a review Antiviral Res. 2000, 47 (1) 1-17 (Pubitemid 30621392)
8. McKimm-Breschkin, J. L.; Selleck, P. W.; Usman, T. B.; Johnson, M. A. Reduced sensitivity of influenza A (H5N1) to oseltamivir Emerging Infect. Dis. 2007, 13 (9) 1354-7 (Pubitemid 47510297)
9. Rameix-Welti, M.-A.; van der Werf, S.; Naffakh, N. Sensitivity of H5N1 influenza viruses to oseltamivir: an update Future Virol. 2008, 3 (2) 157-165 (Pubitemid 351385980)
10. de Jong, M. D.; Thanh, T. T.; Khanh, T. H.; Hien, V. M.; Smith, G. J. D.; Chau, N. V.; Cam, B. V.; Qui, P. T.; Ha, D. Q.; Guan, Y.; Peiris, J. S. M.; Hien, T. T.; Farrar, J. Oseltamivir Resistance during Treatment of Influenza A (H5N1) Infection N. Engl. J. Med. 2005, 353, 2667-72 (Pubitemid 41817715)
11. Moscona, A. Oseltamivir Resistance-Disabling Our Influenza Defenses N. Engl. J. Med. 2005, 353, 2633-6 (Pubitemid 41817709)
12. Gubareva, L. V.; Webster, R. G.; Hayden, F. G. Comparison of the activities of zanamivir, oseltamivir, and RWJ-270201 against clinical isolates of influenza virus and neuraminidase inhibitor-resistant variants Antimicrob. Agents Chemother. 2001, 45 (12) 3403-8 (Pubitemid 33107853)
13. Collins, P. J.; Haire, L. F.; Lin, Y. P.; Liu, J.; Russell, R. J.; Walker, P. A.; Skehel, J. J.; Martin, S. R.; Hay, A. J.; Gamblin, S. J. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants Nature 2008, 453 (7199) 1258-61 (Pubitemid 351913590)
14. Woods, J. M.; Bethell, R. C.; Coates, J. A.; Healy, N.; Hiscox, S. A.; Pearson, B. A.; Ryan, D. M.; Ticehurst, J.; Tilling, J.; Walcott, S. M. 4-Guanidino-2,4-dideoxy-2,3-dehydro-N-acetylneuraminic acid is a highly effective inhibitor both of the sialidase (neuraminidase) and of growth of a wide range of influenza A and B viruses in vitro Antimicrob. Agents Chemother. 1993, 37 (7) 1473-9 (Pubitemid 23202375)
15. von Itzstein, M.; Wu, W.-Y.; Kok, G. B.; Pegg, M. S.; Dyason, J. C.; Jin, B.; Phan, T. V.; Smythe, M. L.; White, H. F.; Oliver, S. W.; Colman, P. M.; Varghese, J. N.; Ryan, D. M.; Woods, J. M.; Bethell, R. C.; Hotham, V. J.; Cameron, J. M.; Penn, C. R. Rational design of potent sialidase-based inhibitors of influenza virus replication Nature 1993, 363 (6428) 418-23 (Pubitemid 23179386)
16. Ryan, D. M.; Ticehurst, J.; Dempsey, M. H.; Penn, C. R. Inhibition of influenza virus replication in mice by GG167 (4-guanidino-2,4-dideoxy-2,3- dehydro-N-acetylneuraminic acid) is consistent with extracellular activity of viral neuraminidase (sialidase) Antimicrob. Agents Chemother. 1994, 38 (10) 2270-5 (Pubitemid 24304215)
17. Hayden, F. G.; Treanor, J. J.; Betts, R. F.; Lobo, M.; Esinhart, J. D.; Hussey, E. K. Safety and efficacy of the neuraminidase inhibitor GG167 in experimental human influenza JAMA 1996, 275 (4) 295-9 (Pubitemid 26028588)
18. Li, W.; Escarpe, P. A.; Eisenberg, E. J.; Cundy, K. C.; Sweet, C.; Jakeman, K. J.; Merson, J.; Lew, W.; Williams, M.; Zhang, L.; Kim, C. U.; Bischofberger, N.; Chen, M. S.; Mendel, D. B. Identification of GS 4104 as an orally bioavailable prodrug of the influenza virus neuraminidase inhibitor GS 4071 Antimicrob. Agents Chemother. 1998, 42 (3) 647-53 (Pubitemid 28114822)
19. Li, F.; Maag, H.; Alfredson, T. Prodrugs of nucleoside analogues for improved oral absorption and tissue targeting J. Pharm. Sci. 2008, 97 (3) 1109-34
20. Han, H.; de Vrueh, R. L.; Rhie, J. K.; Covitz, K. M.; Smith, P. L.; Lee, C. P.; Oh, D. M.; Sadee, W.; Amidon, G. L. 5′-Amino acid esters of antiviral nucleosides, acyclovir, and AZT are absorbed by the intestinal PEPT1 peptide transporter Pharm. Res. 1998, 15 (8) 1154-9 (Pubitemid 28401703)
21. Sugawara, M.; Huang, W.; Fei, Y. J.; Leibach, F. H.; Ganapathy, V.; Ganapathy, M. E. Transport of valganciclovir, a ganciclovir prodrug, via peptide transporters PEPT1 and PEPT2 J. Pharm. Sci. 2000, 89 (6) 781-9
22. Varghese Gupta, S.; Gupta, D.; Sun, J.; Dahan, A.; Tsume, Y.; Hilfinger, J.; Lee, K.-D.; Amidon, G. L. Enhancing the Intestinal Membrane Permeability of Zanamivir: A Carrier Mediated Prodrug Approach Mol. Pharmaceutics 2011, 8 (6) 2358-67
23. Shitara, E.; Nishimura, Y.; Nerome, K.; Hiramoto, Y.; Takeuchi, T. Synthesis of 6-acetamido-5-amino- and -5-guanidino-3,4-dehydro-N-(2- ethylbutyryl)-3-piperidinecarboxylic acids related to zanamivir and oseltamivir, inhibitors of influenza virus neuraminidases Org. Lett. 2000, 2 (24) 3837-40
24. Gomes, P.; Santos, M. I.; Trigo, M. J.; Castanheiro, R.; Moreira, R. Improved Synthesis of Amino Acid and Dipeptide Chloromethyl Esters Using Bromochloromethane Synth. Commun. 2003, 33 (10) 1683-93 (Pubitemid 36597561)
25. Masuda, T.; Yoshida, S.; Arai, M.; Kaneko, S.; Yamashita, M.; Honda, T. Synthesis and anti-influenza evaluation of polyvalent sialidase inhibitors bearing 4-guanidino-Neu5Ac2en derivatives Chem. Pharm. Bull. (Tokyo) 2003, 51 (12) 1386-98 (Pubitemid 41694755)
26. Nudelman, A.; Gnizi, E.; Katz, Y.; Azulai, R.; Cohen-Ohana, M.; Zhuk, R.; Sampson, S. R.; Langzam, L.; Fibach, E.; Prus, E.; Pugach, V.; Rephaeli, A. Prodrugs of butyric acid. Novel derivatives possessing increased aqueous solubility and potential for treating cancer and blood diseases Eur. J. Med. Chem. 2001, 36 (1) 63-74 (Pubitemid 32174854)
27. Gupta, D.; Gupta, S. V.; Lee, K.-D.; Amidon, G. L. Chemical and Enzymatic Stability of Amino Acid Prodrugs Containing Methoxy, Ethoxy and Propylene Glycol Linkers Mol. Pharmaceutics 2009, 6 (5) 1604-11
28. Kim, I.; Chu, X.-y.; Kim, S.; Provoda, C. J.; Lee, K.-D.; Amidon, G. L. Identification of a Human Valacyclovirase. Biphenyl Hydrolase-like Protein as Valacyclovir Hydrolase J. Biol. Chem. 2003, 278 (28) 25348-56 (Pubitemid 36835284)
29. Hidalgo, I. J.; Li, J. Carrier-mediated transport and efflux mechanisms in Caco-2 cells Adv. Drug Delivery Rev. 1996, 22 (1-2) 53-66 (Pubitemid 26423597)
30. Liang, R.; Fei, Y. J.; Prasad, P. D.; Ramamoorthy, S.; Han, H.; Yang-Feng, T. L.; Hediger, M. A.; Ganapathy, V.; Leibach, F. H. Human intestinal H+/peptide cotransporter. Cloning, functional expression, and chromosomal localization J. Biol. Chem. 1995, 270 (12) 6456-63
31. Artursson, P.; Karlsson, J. Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells Biochem. Biophys. Res. Commun. 1991, 175 (3) 880-5
32. Croyle, M. A.; Roessler, B. J.; Hsu, C.-P.; Sun, R.; Amidon, G. L. Beta Cyclodextrins Enhance Adenoviral-Mediated Gene Delivery to the Intestine Pharm. Res. 1998, 15 (9) 1348-55 (Pubitemid 28427920)
33. Hsu, C. P.; Hilfinger, J. M.; Walter, E.; Merkle, H. P.; Roessler, B. J.; Amidon, G. L. Overexpression of human intestinal oligopeptide transporter in mammalian cells via adenoviral transduction Pharm. Res. 1998, 15 (9) 1376-81 (Pubitemid 28427924)
34. Amidon, G. L.; Sinko, P. J.; Fleisher, D. Estimating human oral fraction dose absorbed: a correlation using rat intestinal membrane permeability for passive and carrier-mediated compounds Pharm. Res. 1988, 5 (10) 651-4 (Pubitemid 18263612)
35. Kim, J. S.; Mitchell, S.; Kijek, P.; Tsume, Y.; Hilfinger, J.; Amidon, G. L. The suitability of an in situ perfusion model for permeability determinations: utility for BCS class I biowaiver requests Mol. Pharmaceutics 2006, 3 (6) 686-94 (Pubitemid 46087485)
36. Dahan, A.; West, B. T.; Amidon, G. L. Segmental-dependent membrane permeability along the intestine following oral drug administration: Evaluation of a triple single-pass intestinal perfusion (TSPIP) approach in the rat Eur. J. Pharm. Sci. 2009, 36 (2-3) 320-9
37. Fagerholm, U.; Johansson, M.; Lennernas, H. Comparison between permeability coefficients in rat and human jejunum Pharm. Res. 1996, 13 (9) 1336-42 (Pubitemid 26344978)
38. Tsume, Y.; Hilfinger, J. M.; Amidon, G. L. Enhanced cancer cell growth inhibition by dipeptide prodrugs of floxuridine: increased transporter affinity and metabolic stability Mol. Pharmaceutics 2008, 5 (5) 717-27
39. Landowski, C. P.; Lorenzi, P. L.; Song, X.; Amidon, G. L. Nucleoside ester prodrug substrate specificity of liver carboxylesterase J. Pharmacol. Exp. Ther. 2006, 316 (2) 572-80 (Pubitemid 43130983)
40. Song, X.; Lorenzi, P. L.; Landowski, C. P.; Vig, B. S.; Hilfinger, J. M.; Amidon, G. L. Amino acid ester prodrugs of the anticancer agent gemcitabine: synthesis, bioconversion, metabolic bioevasion, and hPEPT1-mediated transport Mol. Pharmaceutics 2005, 2 (2) 157-67 (Pubitemid 41295363)
41. Perry, C. M.; Brogden, R. N. Cefuroxime axetil. A review of its antibacterial activity, pharmacokinetic properties and therapeutic efficacy Drugs 1996, 52 (1) 125-58
42. Frampton, J. E.; Brogden, R. N.; Langtry, H. D.; Buckley, M. M. Cefpodoxime proxetil. A review of its antibacterial activity, pharmacokinetic properties and therapeutic potential Drugs 1992, 44 (5) 889-917
43. Bender, D. M.; Peterson, J. A.; McCarthy, J. R.; Gunaydin, H.; Takano, Y.; Houk, K. N. Cyclopropanecarboxylic acid esters as potential prodrugs with enhanced hydrolytic stability Org. Lett. 2008, 10 (3) 509-11