Bioimaging for targeted delivery of hyaluronic acid derivatives to the livers in cirrhotic mice using quantum dots

ACS Nano

Volumn 4, Issue 6, 2010, Pages 3005-3014

  Kim, Ki Su ^a   Hur, Wonhee ^b   Park, Sang Jun ^a   Hong, Sung Woo ^b   Choi, Jung Eun ^b   Goh, Eun Ji ^a   Yoon, Seung Kew ^b   Hahn, Sei Kwang ^a  

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

^b The Catholic University of Korea   (South Korea)

Author keywords

Bioimaging; Hyaluronic acid; Liver cirrhosis; Quantum dots; Targeted delivery

Indexed keywords

BIO-IMAGING; HYALURONIC ACIDS; LIVER CIRRHOSIS; QUANTUM DOT; TARGETED DELIVERY;

AMIDES; CELL CULTURE; DISEASES; DRUG DELIVERY; ENDOTHELIAL CELLS; ORGANIC ACIDS; SEMICONDUCTOR QUANTUM DOTS; TUMORS;

LIVER;

DRUG CARRIER; HYALURONIC ACID; QUANTUM DOT;

ANIMAL; ARTICLE; CHEMISTRY; FLUORESCENCE MICROSCOPY; LIVER CIRRHOSIS; MATERIALS TESTING; METHODOLOGY; MOUSE; PATHOLOGY;

ANIMALS; DRUG CARRIERS; HYALURONIC ACID; LIVER CIRRHOSIS; MATERIALS TESTING; MICE; MICROSCOPY, FLUORESCENCE; QUANTUM DOTS;

EID: 77955868542     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn100589y     Document Type: Article

References (44)

1. Fontana, R. J.; Goodman, Z. D.; Dienstag, J. L.; Bonkovsky, H. L.; Naishadham, D.; Sterling, R. K.; Su, G. L.; Ghosh, M.; Wright, E. C. HALT-C Trial Group, Relationship of Serum Fibrosis Markers with Liver Fibrosis Stage and Collagen Content in Patients with Advanced Chronic Hepatitis C. Hepatology 2008, 47, 789-798.
2. Engström-Laurent, A.; Lööf, L.; Nyberg, A.; Schröder, T. Increased Serum Levels of Hyaluronate in Liver Disease. Hepatology 1985, 5, 638-642.
3. Gabrielli, G. B.; Capra, F.; Casaril, M.; Squarzoni, S.; Tognella, P.; Dagradi, R.; De Maria, E.; Colombari, R.; Corrocher, R.; De Sandre, G. Serum Laminin and Type III Procollagen in Chronic Hepatitis C. Diagnostic Value in the Assessment of Disease Activity and Fibrosis. Clin. Chim. Acta 1997, 265, 21-31.
4. Ryhanen, L.; Stenback, F.; Ala-Kokko, L.; Savolainen, E. R. The Effect of Malotilate on Type III and Type IV Collagen, Laminin and Fibronectin Metabolism in Dimethylnitrosamine-Induced Liver Fibrosis in the Rat. J. Hepatol. 1996, 24, 238-245.
5. Friedman, S. L. Seminars in Medicine of the Beth Israel Hospital, Boston. The Cellular Basis of Hepatic Fibrosis. Mechanisms and Treatment Strategies. N. Engl. J. Med. 1993, 328, 1828-1835.
6. Hui, A. Y.; Friedman, S. L. Molecular Basis of Hepatic Fibrosis. Expert Rev. Mol. Med. 2003, 5, 1-23.
7. Schuppan, D.; Popov, Y. Hepatic Fibrosis: From Bench to Bedside. J. Gastroenterol. Hepatol. 2002, 17 (Suppl 3), S300-305.
8. Kuo, J. W. Practical Aspects of Hyaluronan Based Medical Products; Taylor & Francis: New York, 2006.
9. Prevo, R.; Banerji, S.; Ferguson, D. J.; Clasper, S.; Jackson, D. G. Mouse LYVE-1 is an Endocytic Receptor for Hyaluronan in Lymphatic Endothelium. J. Biol. Chem. 2001, 276, 19420-19430.
10. Stern, R.; Asari, A. A.; Sugahara, K. N. Hyaluronan Fragments: An Information-Rich System. Eur. J. Cell Biol. 2006, 85, 699-715.
11. Aruffo, A.; Stamenkovic, I.; Melnick, M.; Underhill, C. B.; Seed, B. CD44 is the Principal Cell Surface Receptor for Hyaluronate. Cell 1990, 61, 1303-1313.
12. Entwistle, J.; Hall, C. L.; Turley, E. A. HA Receptors: Regulators of Signalling to the Cytoskeleton. J. Cell. Biochem. 1996, 61, 569-577.
13. Toole, B. P. Hyaluronan-Cell Interactions in Morphogenesis; Portland Press: London, 1998.
14. Asayama, S.; Nogawa, M.; Takei, Y.; Akaike, T.; Maruyama, A. Synthesis of Novel Polyampholyte Comb-Type Copolymers Consisting of a Poly (L-lysine) Backbone and Hyaluronic Acid Side Chains for a DNA Carrier. Bioconjugate Chem. 1998, 9, 476-481.
15. Takei, Y.; Maruyama, A.; Ferdous, A.; Nishimura, Y.; Kawano, S.; Ikejima, K.; Okumura, S.; Asayama, S.; Nogawa, M.; Hashimoto, M.; Makino, Y.; Kinoshita, M.; Watanabe, S.; Akaike, T.; Lemasters, J. J.; Sato, N. Targeted Gene Delivery to Sinusoidal Endothelial Cells: DNA Nanoassociate Bearing Hyaluronan- Glycocalyx. FASEB J. 2004, 18, 699-701.
16. Schledzewski, K.; Falkowski, M.; Moldenhauer, G.; Metharom, P.; Kzhyshkowska, J.; Ganss, R.; Demory, A.; Falkowska-Hansen, B.; Kurzen, H.; Ugurel, S.; Geginat, G.; Arnold, B.; Goerdt, S. Lymphatic Endothelium-Specific Hyaluronan Receptor LYVE-1 is Expressed by Stabilin-1 +, F4/80+, CD11b+ Macrophages in Malignant Tumours and Wound Healing Tissue. In Vivo and in Bone Marrow Cultures In Vitro: Implications for the Assessment of Lymphangiogenesis. J. Pathol. 2006, 209, 67-77.
17. Eriksson, S.; Fraser, J. R.; Laurent, T. C.; Pertoft, H.; Smedsrod, B. Endothelial Cells are a Site of Uptake and Degradation of Hyaluronic Acid in the Liver. Exp. Cell Res. 1983, 144, 223-228.
18. Guechot, J.; Loria, A.; Serfaty, L.; Giral, P.; Giboudeau, J.; Poupon, R. Serum Hyaluronan as a Marker of Liver Fibrosis in Chronic Viral Hepatitis C: Effect of α-Interferon Therapy. J. Hepatol. 1995, 22, 22-26.
19. Oberti, F.; Valsesia, E.; Pilette, C.; Rousselet, M. C.; Bedossa, P.; Aube, C.; Gallois, Y.; Rifflet, H.; Maiga, M. Y.; Penneau-Fontbonne, D.; Cales, P. Noninvasive Diagnosis of Hepatic Fibrosis or Cirrhosis. Gastroenterology 1997, 113, 1609-1616.
20. Urashima, S.; Tsutsumi, M.; Ozaki, K.; Tsuchishima, M.; Shimanaka, K.; Ueshima, Y.; Takase, S. Immunohistochemical Study of Hyaluronate Receptor (CD44) in Alcoholic Liver Disease. Alcohol.: Clin. Exp. Res. 2000, 24, 34S-38S.
21. Satoh, T.; Ichida, T.; Matsuda, Y.; Sugiyama, M.; Yonekura, K.; Ishikawa, T.; Asakura, H. Interaction between Hyaluronan and CD44 in the Development of Dimethylnitrosamine-Induced Liver Cirrhosis. J. Gastroenterol. Hepatol. 2000, 15, 402-411.
22. Lee, H.; Mok, H.; Lee, S.; Oh, Y. K.; Park, T. G. Target-Specific Intracellular Delivery of siRNA Using Degradable Hyaluronic Acid Nanogels. J. Controlled Release 2007, 119, 245-252.
23. Jiang, G.; Park, K.; Kim, J.; Kim, K. S.; Hahn, S. K. Target Specific Intracellular Delivery of siRNA/PEI-HA Complex by Receptor Mediated Endocytosis. Mol. Pharm. 2009, 6, 727-737.
24. 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.
25. Oh, E. J.; Park, K. T.; Kim, K. S.; Kim, J. S.; 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.
26. Michalet, X.; Pinaud, F. F.; Bentolila, L. A.; Tsay, J. M.; Doose, S.; Li, J. J.; Sundaresan, G.; Wu, A. M.; Gambhir, S. S.; Weiss, S. Quantum Dots for Live Cells, In Vivo Imaging, and Diagnostics. Science 2005, 307, 538-544.
27. Chan, W. C.; Nie, S. Quantum Dot Bioconjugates for Ultrasensitive Nonisotopic Detection. Science 1998, 281, 2016-2018.
28. Weissleder, R.; Tung, C. H.; Mahmood, U.; Bogdanov, A., Jr. In Vivo Imaging of Tumors with Protease-Activated Near-Infrared Fluorescent Probes. Nat. Biotechnol. 1999, 17, 375-378.
29. Luo, Y.; Ziebell, M. R.; Prestwich, G. D. A Hyaluronic Acid-Taxol Antitumor Bioconjugate Targeted to Cancer Cells. Biomacromolecules 2000, 1, 208-218.
30. Luo, Y.; Bernshaw, N. J.; Lu, Z. R.; Kopecek, J.; Prestwich, G. D. Targeted Delivery of Doxorubicin by HPMA Copolymer-Hyaluronan Bioconjugates. Pharm. Res. 2002, 19, 396-402. (Pubitemid 34408935)
31. Oh, E. J.; Kim, J. W.; Kong, J. H.; Ryu, S. H.; Hahn, S. K. Signal Transduction of Hyaluronic Acid-Peptide Conjugate for Formyl Peptide Receptor like 1 Receptor. Bioconjugate Chem. 2008, 19, 2401-2408.
32. Kim, S. J.; Hahn, S. K.; Kim, M. J.; Kim, D. H.; Lee, Y. P. Development of a Novel Sustained Release Formulation of Recombinant Human Growth Hormone Using Sodium Hyaluronate Microparticles. J. Controlled Release 2005, 104, 323-335.
33. Motokawa, K.; Hahn, S. K.; Nakamura, T.; Miyamoto, H.; Shimoboji, T. Selectively Crosslinked Hyaluronic Acid Hydrogels for Sustained Release Formulation of Erythropoietin. J. Biomed. Mater. Res. A 2006, 78, 459-465. (Pubitemid 44253529)
34. Kim, J.; Park, K.; Hahn, S. K. Effect of Hyaluronic Acid Molecular Weight on the Morphology of Quantum Dot-Hyaluronic Acid Conjugates. Int. J. Biol. Macromo. 2008, 42, 41-45.
35. Banerji, S.; Wright, A. J.; Noble, M.; Mahoney, D. J.; Campbell, I. D.; Day, A. J.; Jackson, D. G. Structures of the CD44-Hyaluronan Complex Provide Insight into a Fundamental Carbohydrate-Protein Interaction. Nat. Struct. Mol. Biol. 2007, 14, 234-239.
36. Mochizuki, S.; Kano, A.; Shimada, N.; Maruyama, A. Uptake of Enzymatically Digested Hyaluronan by Liver Endothelial Cells In Vivo and In Vitro. J. Biomater. Sci., Polym. Ed. 2009, 20, 83-97.
37. Edwards, M. J.; Keller, B. J.; Kauffman, F. C.; Thurman, R. G. The Involvement of Kupffer Cells in Carbon Tetrachloride Toxicity. Toxicol. Appl. Pharmacol. 1993, 119, 275-279.
38. Rieder, H.; Armbrust, T.; Meyer zum Buschenfelde, K. H.; Ramadori, G. Contribution of Sinusoidal Endothelial Liver Cells to Liver Fibrosis: Expression of Transforming Growth Factor-β 1 Receptors and Modulation of Plasmin-Generating Enzymes by Transforming Growth Factor-β 1. Hepatology 1993, 18, 937-944.
39. Warren, A.; Bertolino, P.; Benseler, V.; Fraser, R.; McCaughan, G. W.; Le Couteur, D. G. Marked Changes of the Hepatic Sinusoid in a Transgenic Mouse Model of Acute Immune-Mediated Hepatitis. J. Hepatol. 2007, 46, 239-246.
40. Matsumura, Y.; Maeda, H. A New Concept for Macromolecular Therapeutics in Cancer Chemotherapy: Mechanism of Tumoritropic Accumulation of Proteins and the Antitumor Agent Smancs. Cancer Res. 1986, 46, 6387-6392.
41. Vasey, P. A.; Kaye, S. B.; Morrison, R.; Twelves, C.; Wilson, P.; Duncan, R.; Thomson, A. H.; Murray, L. S.; Hilditch, T. E.; Murray, T.; Burtles, S.; Fraier, D.; Frigerio, E.; Cassidy, J. Phase I Clinical and Pharmacokinetic Study of PK1 [N-(2-Hydroxypropyl) methacrylamide Copolymer Doxorubicin]: First Member of a New Class of Chemotherapeutic Agents-Drug-Polymer Conjugates. Cancer Research Campaign Phase I/II Committee. Clin. Cancer Res. 1999, 5, 83-94.
42. Lee, H.; Lee, K.; Kim, I. K.; Park, T. G. Synthesis, Characterization, and In Vivo Diagnostic Applications of Hyaluronic Acid Immobilized Gold Nanoprobes. Biomaterials 2008, 29, 4709-4718.
43. Knablein, J., Ed. In Modern Biopharmaceuticals; Wiley-VCH: Weinheim, Germany, 2005; Supplementary CD-ROM.
44. Friedman, S. Isolation and Culture of Hepatic Nonparenchymal Cells. In In Vitro Biological Systems; Tyson, C., Frazier, J., Eds.; Academic Press: San Diego, CA, 1993; Vol. 1, p 292310.