Bioimaging of hyaluronate-interferon α conjugates using a non-interfering zwitterionic fluorophore

Biomacromolecules

Volumn 16, Issue 9, 2015, Pages 3054-3061

  Kim, Ki Su ^a   Hyun, Hoon ^c,d   Yang, Jeong A ^b   Lee, Min Young ^b   Kim, Hyemin ^b   Yun, Seok Hyun ^a   Choi, Hak Soo ^c   Hahn, Sei Kwang ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Pohang University of Science and Technology (POSTECH)   (South Korea)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Chonnam National University Medical School   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BIOACTIVITY; FLUOROPHORES; GLYCOPROTEINS; VIRUSES;

ANTIVIRAL ACTIVITIES; BIODISTRIBUTIONS; BIOLOGICAL BEHAVIOR; BIOLOGICALLY INERT; ENZYME LINKED IMMUNOSORBENT ASSAY; HEPATITIS C VIRUS; INTERFERON ALPHAS; PHARMACOKINETIC ANALYSIS;

HYALURONIC ACID;

2',5' OLIGOADENYLATE SYNTHETASE; ALPHA INTERFERON DERIVATIVE; ANTIVIRUS AGENT; FLUORESCENT DYE; HYALURONATE INTERFERON ALPHA CONJUGATE; HYALURONIC ACID DERIVATIVE; MESSENGER RNA; PEGINTERFERON ALPHA; UNCLASSIFIED DRUG; ZW 800 1; ALPHA INTERFERON; HYALURONIC ACID; QUATERNARY AMMONIUM DERIVATIVE; SULFONIC ACID DERIVATIVE; ZW800-1 COMPOUND;

ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CONFOCAL MICROSCOPY; CONJUGATION; CONTROLLED STUDY; DAUDI CELL LINE; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG LIVER LEVEL; DRUG SYNTHESIS; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FLUORESCENCE IMAGING; GENE EXPRESSION; HEPATITIS C; HEPATITIS C VIRUS; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MEAN RESIDENCE TIME; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; RAT; CHEMISTRY; FLUORESCENCE MICROSCOPY; HEP-G2 CELL LINE; HEPACIVIRUS; PATHOLOGY;

HEP G2 CELLS; HEPACIVIRUS; HEPATITIS C; HUMANS; HYALURONIC ACID; INTERFERON-ALPHA; MICROSCOPY, FLUORESCENCE; QUATERNARY AMMONIUM COMPOUNDS; SULFONIC ACIDS;

EID: 84941695677     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/acs.biomac.5b00933     Document Type: Article

References (36)

1. Tan, S.-L.; Pause, A.; Shi, Y.; Sonenberg, N. Hepatitis C therapeutics: current status and emerging strategies Nat. Rev. Drug Discovery 2002, 1, 867-881 10.1038/nrd937
2. Gravitz, L. Introduction: A smouldering public-health crisis Nature 2011, 474, S2-S4 10.1038/474S2a
3. Perz, J. F.; Armstrong, G. L.; Farrington, L. A.; Hutin, Y. J. F.; Bell, B. P. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide J. Hepatol. 2006, 45, 529-538 10.1016/j.jhep.2006.05.013
4. Fellay, J.; Thompson, A. J.; Ge, D.; Gumbs, C. E.; Urban, T. J.; Shianna, K. V.; Little, L. D.; Qiu, P.; Bertelsen, A. H.; Watson, M.; Warner, A.; Muir, A. J.; Brass, C.; Albrecht, J.; Sulkowski, M.; McHutchison, J. G.; Goldstein, D. B. ITPA gene variants protect against anaemia in patients treated for chronic hepatitis C Nature 2010, 464, 405-408 10.1038/nature08825
5. Thomas, D. L.; Thio, C. L.; Martin, M. P.; Qi, Y.; Ge, D.; O'hUigin, C.; Kidd, J.; Kidd, K.; Khakoo, S. I.; Alexander, G.; Goedert, J. J.; Kirk, G. D.; Donfield, S. M.; Rosen, H. R.; Tobler, L. H.; Busch, M. P.; McHutchison, J. G.; Goldstein, D. B.; Carrington, M. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus Nature 2009, 461, 798-801 10.1038/nature08463
6. Schlutter, J. Therapeutics: New drugs hit the target Nature 2011, 474, S5-S7 10.1038/474S5a
7. Wang, Y.-S.; Youngster, S.; Grace, M.; Bausch, J.; Bordens, R.; Wyss, D. F. Structural and biological characterization of pegylated recombinant interferon alpha-2b and its therapeutic implications Adv. Drug Delivery Rev. 2002, 54, 547-570 10.1016/S0169-409X(02)00027-3
8. Bailon, P.; Palleroni, A.; Schaffer, C. A.; Spence, C. L.; Fung, W.-J.; Porter, J. E.; Ehrlich, G. K.; Pan, W.; Xu, Z.-X.; Modi, M. W.; Farid, A.; Berthold, W.; Graves, M. Rational Design of a Potent, Long-Lasting Form of Interferon: A 40 kDa Branched Polyethylene Glycol-Conjugated Interferon α-2a for the Treatment of Hepatitis C Bioconjugate Chem. 2001, 12, 195-202 10.1021/bc000082g
9. Foser, S.; Schacher, A.; Weyer, K. A.; Brugger, D.; Dietel, E.; Marti, S.; Schreitmuller, T. Isolation, structural characterization, and antiviral activity of positional isomers of monopegylated interferon alpha-2a (PEGASYS) Protein Expression Purif. 2003, 30, 78-87 10.1016/S1046-5928(03)00055-X
10. Yang, J.-A.; Park, K.; Jung, H.; Kim, H.; Hong, S. W.; Yoon, S. K.; Hahn, S. K. Target specific hyaluronic acid-interferon alpha conjugate for the treatment of hepatitis C virus infection Biomaterials 2011, 32, 8722-8729 10.1016/j.biomaterials.2011.07.088
11. Oh, E. J.; Park, K.; Kim, K. S.; Kim, J.; Yang, J.-A.; Kong, J.-H.; Lee, M. Y.; Hoffman, A. S.; Hahn, S. K. Target specific and long-acting delivery of protein, peptide, and nucleotide therapeutics using hyaluronic acid derivatives J. Controlled Release 2010, 141, 2-12 10.1016/j.jconrel.2009.09.010
12. Stern, R. Hyaluronan catabolism: a new metabolic pathway Eur. J. Cell Biol. 2004, 83, 317-325 10.1078/0171-9335-00392
13. Goh, E. J.; Kim, K. S.; Kim, Y. R.; Jung, H. S.; Beack, S.; Kong, W. H.; Scarcelli, G.; Yun, S. H.; Hahn, S. K. Bioimaging of Hyaluronic Acid Derivatives Using Nanosized Carbon Dots Biomacromolecules 2012, 13, 2554-2561 10.1021/bm300796q
14. Kim, J.; Kim, K. S.; Jiang, G.; Kang, H.; Kim, S.; Kim, B.-S.; Park, M. H.; Hahn, S. K. In vivo real-time bioimaging of hyaluronic acid derivatives using quantum dots Biopolymers 2008, 89, 1144-1153 10.1002/bip.21066
15. Kim, K. S.; Hur, W.; Park, S.-J.; Hong, S. W.; Choi, J. E.; Goh, E. J.; Yoon, S. K.; Hahn, S. K. Bioimaging for Targeted Delivery of Hyaluronic Acid Derivatives to the Livers in Cirrhotic Mice Using Quantum Dots ACS Nano 2010, 4, 3005-3014 10.1021/nn100589y
16. Kim, K. S.; Kim, S.; Beack, S.; Yang, J.-A.; Yun, S. H.; Hahn, S. K. In vivo real-time confocal microscopy for target-specific delivery of hyaluronic acid-quantum dot conjugates Nanomedicine 2012, 8, 1070-1073 10.1016/j.nano.2012.05.014
17. Choi, H. S.; Ipe, B. I.; Misra, P.; Lee, J. H.; Bawendi, M. G.; Frangioni, J. V. Tissue- and Organ-Selective Biodistribution of NIR Fluorescent Quantum Dots Nano Lett. 2009, 9, 2354-2359 10.1021/nl900872r
18. Soo Choi, H.; Liu, W.; Misra, P.; Tanaka, E.; Zimmer, J. P.; Itty Ipe, B.; Bawendi, M. G.; Frangioni, J. V. Renal clearance of quantum dots Nat. Biotechnol. 2007, 25, 1165-1170 10.1038/nbt1340
19. Choi, H. S.; Gibbs, S. L.; Lee, J. H.; Kim, S. H.; Ashitate, Y.; Liu, F.; Hyun, H.; Park, G.; Xie, Y.; Bae, S.; Henary, M.; Frangioni, J. V. Targeted zwitterionic near-infrared fluorophores for improved optical imaging Nat. Biotechnol. 2013, 31, 148-153 10.1038/nbt.2468
20. Choi, H. S.; Nasr, K.; Alyabyev, S.; Feith, D.; Lee, J. H.; Kim, S. H.; Ashitate, Y.; Hyun, H.; Patonay, G.; Strekowski, L.; Henary, M.; Frangioni, J. V. Synthesis and In Vivo Fate of Zwitterionic Near-Infrared Fluorophores Angew. Chem., Int. Ed. 2011, 50, 6258-6263 10.1002/anie.201102459
21. Tanaka, E.; Choi, H. S.; Humblet, V.; Ohnishi, S.; Laurence, R. G.; Frangioni, J. V. Real-time intraoperative assessment of the extrahepatic bile ducts in rats and pigs using invisible near-infrared fluorescent light Surgery 2008, 144, 39-48 10.1016/j.surg.2008.03.017
22. Ballou, B.; Fisher, G. W.; Deng, J. S.; Hakala, T. R.; Srivastava, M.; Farkas, D. L. Cyanine fluorochrome-labeled antibodies in vivo: assessment of tumor imaging using Cy3, Cy5, Cy5.5, and Cy7 Cancer Detect. Prev. 1998, 22, 251-257 10.1046/j.1525-1500.1998.0OA25.x
23. Warren, A.; Le Couteur, D. G.; Fraser, R.; Bowen, D. G.; McCaughan, G. W.; Bertolino, P. T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells Hepatology 2006, 44, 1182-1190 10.1002/hep.21378
24. Gaumet, M.; Vargas, A.; Gurny, R.; Delie, F. Nanoparticles for drug delivery: The need for precision in reporting particle size parameters Eur. J. Pharm. Biopharm. 2008, 69, 1-9 10.1016/j.ejpb.2007.08.001
25. Damdinsuren, B.; Nagano, H.; Wada, H.; Noda, T.; Natsag, J.; Marubashi, S.; Miyamoto, A.; Takeda, Y.; Umeshita, K.; Doki, Y.; Dono, K.; Monden, M. Interferon alpha receptors are important for antiproliferative effect of interferon-α against human hepatocellular carcinoma cells Hepatol. Res. 2007, 37, 77-83 10.1111/j.1872-034X.2007.00007.x
26. Melén, K.; Keskinen, P.; Lehtonen, A.; Julkunen, I. Interferon-induced gene expression and signaling in human hepatoma cell lines J. Hepatol. 2000, 33, 764-772 10.1016/S0168-8278(00)80308-6
27. Gisslinger, H.; Kurzrock, R.; Gisslinger, B.; Jiang, S.; Li, S.; Virgolini, I.; Woloszczuk, W.; Andreeff, M.; Talpaz, M. Autocrine cell suicide in a Burkitt lymphoma cell line (Daudi) induced by interferon α: involvement of tumor necrosis factor as ligand for the CD95 receptor Blood 2001, 97, 2791-2797 10.1182/blood.V97.9.2791
28. Bell, S. J.; Fam, C. M.; Chlipala, E. A.; Carlson, S. J.; Lee, J. I.; Rosendahl, M. S.; Doherty, D. H.; Cox, G. N. Enhanced Circulating Half-Life and Antitumor Activity of a Site-Specific Pegylated Interferon-α Protein Therapeutic Bioconjugate Chem. 2008, 19, 299-305 10.1021/bc070131q
29. Glue, P.; Fang, J. W. S.; Rouzier-Panis, R.; Raffanel, C.; Sabo, R.; Gupta, S. K.; Salfi, M.; Jacobs, S. Pegylated interferon-[alpha]2b: Pharmacokinetics, pharmacodynamics, safety, and preliminary efficacy data[ast] Clin. Pharmacol. Ther. 2000, 68, 556-567 10.1067/mcp.2000.110973
30. Yang, J. A.; Park, K.; Jung, H.; Kim, H.; Hong, S. W.; Yoon, S. K.; Hahn, S. K. Target specific hyaluronic acid-interferon alpha conjugate for the treatment of hepatitis C virus infection Biomaterials 2011, 32, 8722-9 10.1016/j.biomaterials.2011.07.088
31. Wüthrich, R. P. The proinflammatory role of hyaluronan-CD44 interactions in renal injury Nephrol. Dial. Transpl. 1999, 14, 2554-2556 10.1093/ndt/14.11.2554
32. Oliver, G. Lymphatic vasculature development Nat. Rev. Immunol. 2004, 4, 35-45 10.1038/nri1258
33. Dusheiko, G. Side effects of α interferon in chronic hepatitis C Hepatology 1997, 26, 112S-121S 10.1002/hep.510260720
34. Lechner, J.; Krall, M.; Netzer, A.; Radmayr, C.; Ryan, M. P.; Pfaller, W. Effects of interferon [agr]-2b on barrier function and junctional complexes of renal proximal tubular LLC-PK1 cells Kidney Int. 1999, 55, 2178-2191 10.1046/j.1523-1755.1999.00487.x
35. Yuan, L.; Wang, J.; Shen, W.-C. Lipidization of human interferon-alpha: A new approach toward improving the delivery of protein drugs J. Controlled Release 2008, 129, 11-17 10.1016/j.jconrel.2008.03.014
36. Shrivastava, S.; Raychoudhuri, A.; Steele, R.; Ray, R.; Ray, R. B. Knockdown of autophagy enhances the innate immune response in hepatitis C virus-infected hepatocytes Hepatology 2011, 53, 406-414 10.1002/hep.24073