Asialoglycoprotein receptor and its application in liver-targeted drug delivery

Progress in Biochemistry and Biophysics

Volumn 42, Issue 6, 2015, Pages 501-510

  Huang, Yuan Yu ^a   Liang, Zi Cai ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

Antisense oligonucleotides; ASGPR; Drug delivery; GalNAc; Liver targeting; SiRNA

Indexed keywords

EID: 84938056583     PISSN: 10003282     EISSN: None     Source Type: Journal    
DOI: 10.16476/j.pibb.2015.0028     Document Type: Article

References (68)

1. Franssen E J, Jansen R W, Vaalburg M, et al. Hepatic and intrahepatic targeting of an anti-inflammatory agent with human serumalbumin and neoglycoproteins as carrier molecules. Biochem Pharmacol, 1993, 45(6): 1215-1226
2. Morell A G, Irvine R A, Sternlieb I, et al. Physical and chemical studies on ceruloplasmin. V. Metabolic studies on sialic acid-free ceruloplasmin in vivo. J Biol Chem, 1968, 243(1): 155-159
3. Meier M, Bider MD, Malashkevich V N, et al. Crystal structure of the carbohydrate recognition domain of the H1 subunit of the asialoglycoprotein receptor. J Mol Biol, 2000, 300(4): 857-865.
4. Tozawa R, Ishibashi S, Osuga J, et al. Asialoglycoprotein receptor deficiency in mice lacking the major receptor subunit. Its obligate requirement for the stable expression of oligomeric receptor. J Biol Chem, 2001, 276(16): 12624-12628
5. Treichel U, Meyer Zum Buschenfelde K H, Dienes H P, et al. Receptor-mediated entry of hepatitis B virus particles into liver cells. Arch Virol, 1997, 142(3): 493-498
6. Becker S, Spiess M, Klenk H D. The asialoglycoprotein receptor is a potential liver-specific receptor for Marburg virus. J Gen Virol, 1995, 76( Pt 2): 393-399
7. Porat N, Apicella M A, Blake M S. Neisseria gonorrhoeae utilizes and enhances the biosynthesis of the asialoglycoprotein receptor expressed on the surface of the hepatic HepG2 cell line. Infect Immun, 1995, 63(4): 1498-1506
8. Harvey H A, Jennings M P, Campbell C A, et al. Receptormediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor. Mol Microbiol, 2001, 42(3): 659-672
9. Hilgard P, Schreiter T, Stockert R J, et al. Asialoglycoprotein receptor facilitates hemolysis in patients with alcoholic liver cirrhosis. Hepatology, 2004, 39(5): 1398-1407
10. Schwartz A L, Fridovich S E, Lodish H F. Kinetics of internalization and recycling of the asialoglycoprotein receptor in a hepatoma cell line. J Biol Chem, 1982, 257(8): 4230-4237
11. Schwartz A L, Rup D, Lodish H F. Difficulties in the quantification of asialoglycoprotein receptors on the rat hepatocyte. J Biol Chem, 1980, 255(19): 9033-9036
12. Yoshida S, Furuhashi M, Suganuma N. Expression of asialoglycoprotein receptor in human fetal liver. Endocr J, 1999, 46(1): 67-73
13. Tolleshaug H, Berg T, Frolich W, et al. Intracellular localization and degradation of asialofetuin in isolated rat hepatocytes. Biochim Biophys Acta, 1979, 585(1): 71-84
14. Schwartz A L, Fridovich S E, Knowles B B, et al. Characterization of the asialoglycoprotein receptor in a continuous hepatoma line. J Biol Chem, 1981, 256(17): 8878-8881
15. Bareford LM, Swaan PW. Endocytic mechanisms for targeted drug delivery. Adv Drug Deliv Rev, 2007, 59(8): 748-758
16. Lehrman M A, Hill R L. The binding of fucose-containing glycoproteins by hepatic lectins. Purification of a fucose-binding lectin fromrat liver. J Biol Chem, 1986, 261(16): 7419-7425
17. Iobst S T, Drickamer K. Selective sugar binding to the carbohydrate recognition domains of the rat hepatic and macrophage asialoglycoprotein receptors. J Biol Chem, 1996, 271 (12): 6686-6693
18. Rensen P C, Sliedregt L A, Ferns M, et al. Determination of the upper size limit for uptake and processing of ligands by the asialoglycoprotein receptor on hepatocytes in vitro and in vivo. J Biol Chem, 2001, 276(40): 37577-37584
19. Lee Y C, Townsend R R, Hardy M R, et al. Binding of synthetic oligosaccharides to the hepatic Gal/GalNAc lectin. Dependence on fine structural features. J Biol Chem, 1983, 258(1): 199-202
20. Lee R T, Lin P, Lee Y C. New synthetic cluster ligands for galactose/N-acetylgalactosamine-specific lectin of mammalian liver. Biochemistry, 1984, 23(18): 4255-4261
21. Baenziger J U, Maynard Y. Human hepatic lectin. Physiochemical properties and specificity. J Biol Chem, 1980, 255(10): 4607-4613
22. Biessen E A, Beuting D M, Roelen H C, et al. Synthesis of cluster galactosides with high affinity for the hepatic asialoglycoprotein receptor. J Med Chem, 1995, 38(9): 1538-1546
23. Bergen J M, Von Recum H A, Goodman T T, et al. Gold nanoparticles as a versatile platformfor optimizing physicochemical parameters for targeted drug delivery. Macromol Biosci, 2006, 6(7): 506-516
24. Wang H X, Xiong M H, Wang Y C, et al. N-acetylgalactosamine functionalized mixed micellar nanoparticles for targeted delivery of siRNA to liver. J Control Release, 2013, 166(2): 106-114
25. Akinc A, Querbes W, De S, et al. Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms. Mol Ther, 2010, 18(7): 1357-1364
26. Chen S, Tam Y Y, Lin P J, et al. Development of lipid nanoparticle formulations of siRNA for hepatocyte gene silencing following subcutaneous administration. J Control Release, 2014, 196: 106-112
27. Wu G Y, Wu C H. Receptor-mediated in vitro gene transformation by a soluble DNA carrier system. J Biol Chem, 1987, 262 (10): 4429-4432
28. Wu G Y, Wu C H. Receptor-mediated gene delivery and expression in vivo. J Biol Chem, 1988, 263(29): 14621-14624
29. Wu G Y, Wu C H. Specific inhibition of hepatitis B viral gene expression in vitro by targeted antisense oligonucleotides. J Biol Chem, 1992, 267(18): 12436-12439
30. Plank C, Zatloukal K, Cotten M, et al. Gene transfer into hepatocytes using asialoglycoprotein receptor mediated endocytosis of DNA complexed with an artificial tetra-antennary galactose ligand. Bioconjug Chem, 1992, 3(6): 533-539
31. Rohlff C, Watson S A, Morris T M, et al. A novel, orally administered nucleoside analogue, OGT 719, inhibits the liver invasive growth of a human colorectal tumor, C170HM2. Cancer Res, 1999, 59(6): 1268-1272
32. Seymour L W, Ferry D R, Anderson D, et al. Hepatic drug targeting: phase I evaluation of polymer-bound doxorubicin. J Clin Oncol, 2002, 20(6): 1668-1676
33. Fiume L, Di Stefano G. Lactosaminated human albumin, a hepatotropic carrier of drugs. Eur J Pharm Sci, 2010, 40 (4): 253-262
34. Merwin J R, Noell G S, Thomas W L, et al. Targeted delivery of DNA using YEE(GalNAcAH)3, a synthetic glycopeptide ligand for the asialoglycoprotein receptor. Bioconjug Chem, 1994, 5 (6): 612-620
35. Hangeland J J, Levis J T, Lee Y C, et al. Cell-type specific and ligand specific enhancement of cellular uptake of oligodeoxynucleoside methylphosphonates covalently linked with a neoglycopeptide, YEE(ah-GalNAc)3. Bioconjug Chem, 1995, 6(6): 695-701.
36. Biessen E A, Sliedregt-Bol K, Pa T H, et al. Design of a targeted peptide nucleic acid prodrug to inhibit hepatic human microsomal triglyceride transfer protein expression in hepatocytes. Bioconjug Chem, 2002, 13(2): 295-302
37. Rensen P C, Van Leeuwen S H, Sliedregt L A, et al. Design and synthesis of novel N-acetylgalactosamine-terminated glycolipids for targeting of lipoproteins to the hepatic asialoglycoprotein receptor. J Med Chem, 2004, 47(23): 5798-5808
38. Akinc A, Goldberg M, Qin J, et al. Development of lipidoid-siRNA formulations for systemic delivery to the liver. Mol Ther, 2009, 17(5): 872-879
39. Semple S C, Akinc A, Chen J, et al. Rational design of cationic lipids for siRNAdelivery. Nat Biotechnol, 2010, 28(2): 172-176
40. Nair J K, Willoughby J L, Chan A, et al. Multivalent N-Acetylgalactosamine-Conjugated siRNA localizes in hepatocytes and elicits robust RNAi-Mediated gene silencing. J Am Chem Soc, 2014, 136(49): 16958-16961
41. Rajeev K G, Nair J K, Jayaraman M, et al. Hepatocyte-specific delivery of siRNAs conjugated to novel non-nucleosidic trivalent N-Acetylgalactosamine elicits robust gene silencing in vivo. Chembiochem, 2015, 16(6): 903-908
42. Abstracts 8th Annual Meeting of the Oligonucleotide Therapeutics Society, Boston, Massachusetts, USA, October 28-31, 2012 Abstracts. Nucleic Acid Ther, 2012, 22(6): A2-A2
43. Matsuda S, Keiser K, Nair J K, et al. siRNA conjugates carrying sequentially assembled trivalent N-Acetylgalactosamine linked through nucleosides elicit robust gene silencing in vivo in hepatocytes. ACS Chem Biol, 2015, 10 (5): 1181-1187(DOI: 10. 1021/cb501028c)
44. Kanasty R, Dorkin J R, Vegas A, et al. Delivery materials for siRNA therapeutics. Nat Mater, 2013, 12(11): 967-977
45. Monia B P. Board of the Oligonucleotide Therapeutics S. 9th annual meeting of the Oligonucleotide Therapeutics Society Naples, Italy October 6-8, 2013. Session summaries. Nucleic Acid Ther, 2013, 23(6): 450-458
46. Zimmermann T, Karsten V, Harrop J, et al. Phase I first-in-humans trial of ALN-TTRsc, a novel RNA interference therapeutic for the treatment of familial amyloidotic cardiomyopathy (FAC). Journal of Cardiac Failure, 2013, 19(8): S66-S66
47. Castano A, Drachman B M, Judge D, et al. Natural history and therapy of TTR-cardiac amyloidosis: emerging disease-modifying therapies fromorgan transplantation to stabilizer and silencer drugs. Heart Fail Rev, 2015, 20(2): 163-178
48. Lorenzer C, Dirin M, Winkler A M, et al. Going beyond the liver: Progress and challenges of targeted delivery of siRNA therapeutics. J Control Release, 2015, 203: 1-15
49. Sehgal A, Barros S, Ivanciu L, et al. An RNAi therapeutic targeting antithrombin to rebalance the coagulation system and promote hemostasis in hemophilia. Nat Med, 2015, 21 (5): 492-497(DOI: 10.1038/nm.3847)
50. Borodovsky A, Yucius K, Sprague A, et al. Aln-CC5, an investigational RNAi therapeutic targeting C5 for complement inhibition. Blood, 2014, 124(21)
51. Yasuda M, Gan L, Chen B, et al. RNAi-mediated silencing of hepatic Alas1 effectively prevents and treats the induced acute attacks in acute intermittent porphyria mice. Proc Natl Acad Sci USA, 2014, 111(21): 7777-7782
52. Fitzgerald K, Frank-Kamenetsky M, Shulga-Morskaya S, et al. Effect of an RNA interference drug on the synthesis of proprotein convertase subtilisin/kexin type 9 (PCSK9) and the concentration of serum LDL cholesterol in healthy volunteers: a randomised, single-blind, placebo-controlled, phase 1 trial. Lancet, 2014, 383(9911): 60-68
53. Stock J. Improving the care of high-risk patients: the potential of PCSK9. Atherosclerosis, 2014, 232(2): 420-422
54. Sepp-Lorenzino L, Abrams M, Carayannopoulos L, et al. ALN-HBV, a GalNAc-siRNA enhanced stabilization chemistry RNAi therapeutic for the treatment of chronic hepatitis B virus infection. Hepatology, 2014, 60(Supplement S1): 1091A-1091A
55. Alabi C, Vegas A, Anderson D. Attacking the genome: emerging siRNA nanocarriers from concept to clinic. Curr Opin Pharmacol, 2012, 12(4): 427-433
56. Rozema D B, Lewis D L, Wakefield D H, et al. Dynamic PolyConjugates for targeted in vivo delivery of siRNA to hepatocytes. Proc Natl Acad Sci USA, 2007, 104 (32): 12982-12987
57. Wong S C, Klein J J, Hamilton H L, et al. Co-injection of a targeted, reversibly masked endosomolytic polymer dramatically improves the efficacy of cholesterol-conjugated small interfering RNAs in vivo. Nucleic Acid Ther, 2012, 22(6): 380-390
58. Sebestyen M G, Wong S C, Trubetskoy V, et al. Targeted in vivo delivery of siRNA and an endosome-releasing agent to hepatocytes. MethodsMol Biol, 2015, 1218: 163-186
59. Soutschek J, Akinc A, Bramlage B, et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature, 2004, 432(7014): 173-178
60. Wooddell C I, Rozema D B, Hossbach M, et al. Hepatocytetargeted RNAi therapeutics for the treatment of chronic hepatitis B virus infection. Mol Ther, 2013, 21(5): 973-985
61. Steinbach O C. Industry update. Therapeutic Delivery, 2015, 6(3): 277-381
62. Schneider B, Grote M, John M, et al. Targeted siRNA delivery and mRNA knockdown mediated by bispecific digoxigenin-binding antibodies. Mol Ther Nucleic Acids, 2012, 1: e46
63. Prakash T P, Graham M J, Yu J, et al. Targeted delivery of antisense oligonucleotides to hepatocytes using triantennary N-acetyl galactosamine improves potency 10-fold in mice. Nucleic Acids Res, 2014, 42(13): 8796-8807
64. Baek J, Kang S, Min H. MicroRNA-targeting therapeutics for hepatitis C. Arch PharmRes, 2014, 37(3): 299-305
65. Baumann V, Winkler J. MiRNA-based therapies: strategies and delivery platforms for oligonucleotide and non-oligonucleotide agents. Future Med Chem, 2014, 6(17): 1967-1984
66. Zangi L, Lui K O, Von Gise A, et al. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat Biotechnol, 2013, 31(10): 898-907
67. Rejman J, Tavernier G, Bavarsad N, et al. mRNA transfection of cervical carcinoma and mesenchymal stem cells mediated by cationic carriers. J Control Release, 2010, 147(3): 385-391
68. Tachibana R, Harashima H, Shinohara Y, et al. Quantitative studies on the nuclear transport of plasmid DNA and gene expression employing nonviral vectors. Adv Drug Deliv Rev, 2001, 52 (3): 219-226