In vivo delivery of cell-permeable antisense hypoxia-inducible factor 1α oligonucleotide to adipose tissue reduces adiposity in obese mice

Journal of Controlled Release

Volumn 161, Issue 1, 2012, Pages 1-9

  Park, Yoon Shin ^a   David, Allan E ^a   Huang, Yongzhuo ^b   Park, Jun Beom ^c   He, Huining ^d   Byun, Youngro ^c   Yang, Victor C ^a,c,d  

^a UNIVERSITY OF MICHIGAN   (United States)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^c Seoul National University   (South Korea)

^d TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Adipogenesis; Angiogenesis; Antisense oligonucleotide; Hypoxia inducible factor 1 ; Low molecular weight protamine; Obesity

Indexed keywords

ADIPOGENESIS; ANGIOGENESIS; ANTISENSE OLIGONUCLEOTIDES; HYPOXIA-INDUCIBLE FACTOR 1; LOW MOLECULAR WEIGHT; OBESITY;

ALUMINUM; MAMMALS; MOLECULAR WEIGHT; NUTRITION; OLIGONUCLEOTIDES; TISSUE;

BLOOD VESSELS;

ALANINE AMINOTRANSFERASE; ANTISENSE OLIGONUCLEOTIDE; ASPARTATE AMINOTRANSFERASE; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTAMINE; TRIACYLGLYCEROL;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTISENSE THERAPY; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BODY WEIGHT; CELL PERMEABILIZATION; CELL SIZE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IN VIVO GENE TRANSFER; LIPID BLOOD LEVEL; LIPID DIET; LIVER TOXICITY; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; UMBILICAL VEIN ENDOTHELIAL CELL; WHITE ADIPOSE TISSUE;

ADIPOGENESIS; ADIPOSE TISSUE; ADIPOSITY; ANGIOGENESIS INHIBITORS; ANIMALS; BLOOD GLUCOSE; CELL LINE; DOWN-REGULATION; DRUG CARRIERS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; OLIGONUCLEOTIDES, ANTISENSE; PROTAMINES;

EID: 84862595727     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.04.026     Document Type: Article

References (46)

1. D.W. Haslam, W.P. James, Obesity, Lancet 366 (9492) (2005) 1197-1209. (Pubitemid 41393598)
2. M.C. Carr, J.D. Brunzell, Abdominal obesity and dyslipidemia in the metabolic syndrome: importance of type 2 diabetes and familial combined hyperlipidemia in coronary artery disease risk, J. Clin. Endocrinol. Metab. 89 (6) (2004) 2601-2607. (Pubitemid 38766338)
3. R. Padwal, A. Kezouh, M. Levine, M. Etminan, Long-term persistence with orlistat and sibutramine in a population-based cohort, Int. J. Obes. (Lond) 31 (10) (2007) 1567-1570. (Pubitemid 47482652)
4. R. Sari, M.K. Balci, M. Cakir, H. Altunbas, U. Karayalcin, Comparison of efficacy of sibutramine or orlistat versus their combination in obese women, Endocr. Res. 30 (2) (2004) 159-167. (Pubitemid 39243118)
5. C.G. Brook, Relation between age of onset of obesity and size and number of adipose cells, Br. Med. J. 2 (5804) (1972) 25-27.
6. Y. Cao, Adipose tissue angiogenesis as a therapeutic target for obesity and metabolic diseases, Nat. Rev. Drug Discov. 9 (2) (2010) 107-115.
7. H.R. Lijnen, Angiogenesis and obesity, Cardiovasc. Res. 78 (2) (2008) 286-293. (Pubitemid 351556088)
8. G. Helmlinger, F. Yuan, M. Dellian, R.K. Jain, Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation, Nat. Med. 3 (2) (1997) 177-182. (Pubitemid 27064702)
9. M.S. O'Reilly, L. Holmgren, Y. Shing, C. Chen, R.A. Rosenthal, M. Moses, W.S. Lane, Y. Cao, E.H. Sage, J. Folkman, Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma, Cell 79 (2) (1994) 315-328. (Pubitemid 24324921)
10. M.S. O'Reilly, T. Boehm, Y. Shing, N. Fukai, G. Vasios, W.S. Lane, E. Flynn, J.R. Birkhead, B.R. Olsen, J. Folkman, Endostatin: an endogenous inhibitor of angiogenesis and tumor growth, Cell 88 (2) (1997) 277-285. (Pubitemid 28015876)
11. M.A. Rupnick, D. Panigrahy, C.Y. Zhang, S.M. Dallabrida, B.B. Lowell, R. Langer, M.J. Folkman, Adipose tissue mass can be regulated through the vasculature, Proc. Natl. Acad. Sci. U. S. A. 99 (16) (2002) 10730-10735.
12. R. Cao, E. Brakenhielm, C. Wahlestedt, J. Thyberg, Y. Cao, Leptin induces vascular permeability and synergistically stimulates angiogenesis with FGF-2 and VEGF, Proc. Natl. Acad. Sci. U. S. A. 98 (11) (2001) 6390-6395. (Pubitemid 32488247)
13. P. Hnik, D.S. Boyer, L.R. Grillone, J.G. Clement, S.P. Henry, E.A. Green, Antisense oligonucleotide therapy in diabetic retinopathy, J. Diabetes Sci. Technol. 3 (4) (2009) 924-930.
14. L. Xu, T. Anchordoquy, Drug delivery trends in clinical trials and translational medicine: challenges and opportunities in the delivery of nucleic acid-based therapeutics, J. Pharm. Sci. 100 (1) (2011) 38-52.
15. E.R. Rayburn, R. Zhang, Antisense, RNAi, and gene silencing strategies for therapy: mission possible or impossible? Drug Discov. Today 13 (11-12) (2008) 513-521.
16. B. Yu, X. Zhao, L.J. Lee, R.J. Lee, Targeted delivery systems for oligonucleotide therapeutics, AAPS J. 11 (1) (2009) 195-203.
17. C. Leonetti, G. Zupi, Targeting different signaling pathways with antisense oligonucleotides combination for cancer therapy, Curr. Pharm. Des. 13 (5) (2007) 463-470. (Pubitemid 46477751)
18. E.R. Rayburn, H. Wang, R. Zhang, Antisense-based cancer therapeutics: are we there yet? Expert Opin. Emerg. Drugs 11 (2) (2006) 337-352. (Pubitemid 43723312)
19. J.Q. Gao, Y. Eto, Y. Yoshioka, F. Sekiguchi, S. Kurachi, T. Morishige, X. Yao, H. Watanabe, R. Asavatanabodee, F. Sakurai, H. Mizuguchi, Y. Okada, Y. Mukai, Y. Tsutsumi, T.Mayumi, N. Okada, S. Nakagawa, Effective tumor targeted gene transfer using PEGylated adenovirus vector via systemic administration, J. Control. Release 122 (1) (2007) 102-110. (Pubitemid 47284554)
20. Y.T. Ko, R. Bhattacharya, U. Bickel, Liposome encapsulated polyethylenimine/ODN polyplexes for brain targeting, J. Control. Release 133 (3) (2009) 230-237.
21. Y. Kim, M. Tewari, J.D. Pajerowski, S. Cai, S. Sen, J.H. Williams, S.R. Sirsi, G.J. Lutz, D.E. Discher, Polymersome delivery of siRNA and antisense oligonucleotides, J. Control. Release 134 (2) (2009) 132-140.
22. M.S. Wadhwa, W.T. Collard, R.C. Adami, D.L. McKenzie, K.G. Rice, Peptide-mediated gene delivery: influence of peptide structure on gene expression, Bioconjug. Chem. 8 (1) (1997) 81-88. (Pubitemid 27064227)
23. L. Dong, S. Xia, Y. Luo, H. Diao, J. Zhang, J. Chen, J. Zhang, Targeting delivery oligonucleotide into macrophages by cationic polysaccharide from Bletilla striata successfully inhibited the expression of TNF-alpha, J. Control. Release 134 (3) (2009) 214-220.
24. D.G. Miller, M.A. Adam, A.D. Miller, Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection, Mol. Cell. Biol. 10 (8) (1990) 4239-4242.
25. M. Junghans, J. Kreuter, A. Zimmer, Antisense delivery using protamine- oligonucleotide particles, Nucleic Acids Res. 28 (10) (2000) E45.
26. N. Dinauer, D. Lochmann, I. Demirhan, A. Bouazzaoui, A. Zimmer, A. Chandra, J. Kreuter, H. von Briesen, Intracellular tracking of protamine/antisense oligonucleotide nanoparticles and their inhibitory effect on HIV-1 transactivation, J. Control. Release 96 (3) (2004) 497-507. (Pubitemid 38553927)
27. Y.S. Park, Y. Huang, Y.J. Park, A.E. David, L.White, H. He, H.S. Chung, V.C. Yang, Specific down regulation of 3T3-L1 adipocyte differentiation by cell-permeable antisense HIF1alpha-oligonucleotide, J. Control. Release 144 (1) (2010) 82-90.
28. Y.J. Park, L.C. Chang, J.F. Liang, C. Moon, C.P. Chung, V.C. Yang, Nontoxic membrane translocation peptide from protamine, low molecular weight protamine (LMWP), for enhanced intracellular protein delivery: in vitro and in vivo study, FASEB J. 19 (11) (2005) 1555-1557. (Pubitemid 41279029)
29. Y.Huang, Y.S. Park, C.Moon,A.E.David,H.S. Chung,V.C. Yang, Synthetic skin-permeable proteins enabling needleless immunization, Angew. Chem. Int. Ed Engl. 49 (15) (2010) 2724-2727.
30. W. Lv, C. Zhang, D.H. Zhou, J. Hao, J.G. Sun, T. Liu, Y.X. Hao, P.W. Yu, RNAi-mediated gene silencing of vascular endothelial growth factor inhibits growth of colorectal cancer, Cancer Biother. Radiopharm. 22 (6) (2007) 841-852.
31. V.T. Samuel, C.S. Choi, T.G. Phillips, A.J. Romanelli, J.G. Geisler, S. Bhanot, R. McKay, B. Monia, J.R. Shutter, R.A. Lindberg, G.I. Shulman, M.M. Veniant, Targeting foxo1 in mice using antisense oligonucleotide improves hepatic and peripheral insulin action, Diabetes 55 (7) (2006) 2042-2050. (Pubitemid 44509978)
32. H.S. Younis, B. Hirakawa, W. Scott, P. Tran, G. Bhat, T. Affolter, J. Chapman, J. Heyen, K. Chakravarty, G. Alton, Antisense inhibition of S6 kinase 1 produces improved glucose tolerance and is well tolerated for 4 weeks of treatment in rats, Pharmacology 87 (1-2) (2011) 11-23.
33. X.X. Yu, S.F. Murray, L. Watts, S.L. Booten, J. Tokorcheck, B.P. Monia, S. Bhanot, Reduction of JNK1 expression with antisense oligonucleotide improves adiposity in obese mice, Am. J. Physiol. Endocrinol. Metab. 295 (2) (2008) E436-E445.
34. S. Reitman, S. Frankel, A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases, Am. J. Clin. Pathol. 28 (1) (1957) 56-63.
35. J. Folch, M. Lees, G.H. Sloane Stanley, A simple method for the isolation and purification of total lipides from animal tissues, J. Biol. Chem. 226 (1) (1957) 497-509.
36. N. Hosogai, A. Fukuhara, K. Oshima, Y. Miyata, S. Tanaka, K. Segawa, S. Furukawa, Y. Tochino, R. Komuro, M. Matsuda, I. Shimomura, Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation, Diabetes 56 (4) (2007) 901-911. (Pubitemid 46525054)
37. X. Zhang, K.S. Lam, H. Ye, S.K. Chung, M. Zhou, Y. Wang, A. Xu, Adipose tissue-specific inhibition of hypoxia-inducible factor 1{alpha} induces obesity and glucose intolerance by impeding energy expenditure in mice, J. Biol. Chem. 285 (43) (2010) 32869-32877.
38. D.R. Sorensen, M. Leirdal, M. Sioud, Gene silencing by systemic delivery of synthetic siRNAs in adult mice, J. Mol. Biol. 327 (4) (2003) 761-766. (Pubitemid 36315917)
39. D.M. Wilcox, R. Yang, S.J. Morgan, P.T. Nguyen, M.J. Voorbach, P.M. Jung, D.L. Haasch, E. Lin, E.N. Bush, T.J. Opgenorth, P.B. Jacobson, C.A. Collins, C.M. Rondinone, T. Surowy, K.T. Landschulz, Delivery of RNAi reagents in murine models of obesity and diabetes, J. RNAi Gene Silencing 3 (1) (2006) 225-236.
40. M.R. Alam, V. Dixit, H. Kang, Z.B. Li, X. Chen, J. Trejo, M. Fisher, R.L. Juliano, Intracellular delivery of an anionic antisense oligonucleotide via receptor-mediated endocytosis, Nucleic Acids Res. 36 (8) (2008) 2764-2776. (Pubitemid 351659588)
41. G. Voros, E. Maquoi, D. Demeulemeester, N. Clerx, D. Collen, H.R. Lijnen, Modulation of angiogenesis during adipose tissue development in murine models of obesity, Endocrinology 146 (10) (2005) 4545-4554. (Pubitemid 41324053)
42. N. Pandya, N. Dhalla, D. Santani, Angiogenesis - a new target for future therapy, Vascul. Pharmacol. 44 (5) (2006) 265-274.
43. S. Nishimura, I. Manabe, M. Nagasaki, Y. Hosoya, H. Yamashita, H. Fujita, M. Ohsugi, K. Tobe, T. Kadowaki, R. Nagai, S. Sugiura, Adipogenesis in obesity requires close interplay between differentiating adipocytes, stromal cells, and blood vessels, Diabetes 56 (6) (2007) 1517-1526. (Pubitemid 46842598)
44. I.M. Kaplan, J.S. Wadia, S.F. Dowdy, Cationic TAT peptide transduction domain enters cells by macropinocytosis, J. Control. Release 102 (1) (2005) 247-253. (Pubitemid 40093789)
45. B. Gupta, T.S. Levchenko, V.P. Torchilin, Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides, Adv. Drug Deliv. Rev. 57 (4) (2005) 637-651. (Pubitemid 40255564)
46. P. Midoux, M. Monsigny, Efficient gene transfer by histidylated polylysine/pDNA complexes, Bioconjug. Chem. 10 (3) (1999) 406-411. (Pubitemid 29243322)