Intracellular delivery of short interfering RNA in rat organ of corti using a cell-penetrating peptide PepFect6

Molecular Therapy Nucleic Acids

Volumn 1, Issue DEC, 2012, Pages

  Dash Wagh, Suvarna ^a   Jacob, Stefan ^a   Lindberg, Staffan ^b   Fridberger, Anders ^a   Langel, Ülo ^b   Ulfendahl, Mats ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Cell penetrating peptide (CPP); Cochlea; Connexin; FRAP; Gap junctions; Gene therapy; Inner ear; Nanoparticles; siRNA

Indexed keywords

CALCEIN; CELL PENETRATING PEPTIDE; CONNEXIN 26; MESSENGER RNA; PEPFECT6; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CELL PENETRATING PEPTIDE PEPFECT6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CORTI ORGAN; CYTOTOXICITY; GENE VECTOR; HAIR CELL; HEARING IMPAIRMENT; HOUSEKEEPING GENE; INNER EAR; INTERNALIZATION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PRIORITY JOURNAL; RAT; RNA INTERFERENCE; TISSUE CULTURE; CELL CULTURE; COCHLEA; CONTROLLED STUDY; ENDOSOME; GENE SILENCING; RNA TRANSPORT;

EID: 85015397679     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2012.50     Document Type: Article

References (49)

1. Scherr, M, Morgan, MA and Eder, M (2003). Gene silencing mediated by small interfering RNAs in mammalian cells. Curr Med Chem 10: 245-256. (Pubitemid 36131657)
2. Elbashir, SM, Harborth, J, Lendeckel, W, Yalcin, A, Weber, K and Tuschl, T (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498. (Pubitemid 32494397)
3. Dykxhoorn, DM and Lieberman, J (2006). Knocking down disease with siRNAs. Cell 126: 231-235. (Pubitemid 44092975)
4. Lares, MR, Rossi, JJ and Ouellet, DL (2010). RNAi and small interfering RNAs in human disease therapeutic applications. Trends Biotechnol 28: 570-579.
5. Shim, MS and Kwon, YJ (2010). Efficient and targeted delivery of siRNA in vivo. FEBS J 277: 4814-4827.
6. Andaloussi, SE, Lehto, T, Mäger, I, Rosenthal-Aizman, K, Oprea, II, Simonson, OE et al. (2011). Design of a peptide-based vector, PepFect6, for efficient delivery of siRNA in cell culture and systemically in vivo. Nucleic Acids Res 39: 3972-3987.
7. Crombez, L, Morris, MC, Dufort, S, Aldrian-Herrada, G, Nguyen, Q, Mc Master, G et al. (2009). Targeting cyclin B1 through peptide-based delivery of siRNA prevents tumour growth. Nucleic Acids Res 37: 4559-4569.
8. Kim, WJ, Christensen, LV, Jo, S, Yockman, JW, Jeong, JH, Kim, YH et al. (2006). Cholesteryl oligoarginine delivering vascular endothelial growth factor siRNA effectively inhibits tumor growth in colon adenocarcinoma. Mol Ther 14: 343-350. (Pubitemid 44184964)
9. Crombez, L, Aldrian-Herrada, G, Konate, K, Nguyen, QN, McMaster, GK, Brasseur, R et al (2009). A new potent secondary amphipathic cell-penetrating peptide for siRNA delivery into mammalian cells. Mol Ther 17: 95-103.
10. El-Andaloussi, S, Holm, T and Langel, U (2005). Cell-penetrating peptides: mechanisms and applications. Curr Pharm Des 11: 3597-3611. (Pubitemid 41630987)
11. Heitz, F, Morris, MC and Divita, G (2009). Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics. Br J Pharmacol 157: 195-206.
12. Foged, C and Nielsen, HM (2008). Cell-penetrating peptides for drug delivery across membrane barriers. Expert Opin Drug Deliv 5: 105-117. (Pubitemid 351234112)
13. Stewart, KM, Horton, KL and Kelley, SO (2008). Cell-penetrating peptides as delivery vehicles for biology and medicine. Org Biomol Chem 6: 2242-2255. (Pubitemid 351863664)
14. Youngblood, DS, Hatlevig, SA, Hassinger, JN, Iversen, PL and Moulton, HM (2007). Stability of cell-penetrating peptide-morpholino oligomer conjugates in human serum and in cells. Bioconjug Chem 18: 50-60. (Pubitemid 46145994)
15. Mäe, M, Andaloussi, SE, Lehto, T and Langel, U (2009). Chemically modified cell-penetrating peptides for the delivery of nucleic acids. Expert Opin Drug Deliv 6: 1195-1205.
16. El-Sayed, A, Futaki, S and Harashima, H (2009). Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment. AAPS J 11: 13-22.
17. Mäe, M, El Andaloussi, S, Lundin, P, Oskolkov, N, Johansson, HJ, Guterstam, P et al. (2009). A stearylated CPP for delivery of splice correcting oligonucleotides using a noncovalent co-incubation strategy. J Control Release 134: 221-227.
18. Lustig, LR and Akil, O (2012). Cochlear gene therapy. Curr Opin Neurol 25: 57-60.
19. Van Camp, G, Snoeckx, RL, Hilgert, N, van den Ende, J, Fukuoka, H, Wagatsuma, M et al. (2006). A new autosomal recessive form of Stickler syndrome is caused by a mutation in the COL9A1 gene. Am J Hum Genet 79: 449-457. (Pubitemid 44384254)
20. Rabionet, R, Gasparini, P and Estivill, X (2000). Molecular genetics of hearing impairment due to mutations in gap junction genes encoding beta connexins. Hum Mutat 16: 190-202.
21. Nickel, R and Forge, A (2008). Gap junctions and connexins in the inner ear: their roles in homeostasis and deafness. Curr Opin Otolaryngol Head Neck Surg 16: 452-457.
22. Denoyelle, F, Lina-Granade, G, Plauchu, H, Bruzzone, R, Chaib, H, Levi-Acobas, F et al. (1998). Connexin 26 gene linked to a dominant deafness. Nature 393: 319-320. (Pubitemid 28269696)
23. Majumder, P, Crispino, G, Rodriguez, L, Ciubotaru, CD, Anselmi, F, Piazza, V et al. (2010). ATP-mediated cell-cell signaling in the organ of Corti: the role of connexin channels. Purinergic Signal 6: 167-187.
24. Anselmi, F, Hernandez, VH, Crispino, G, Seydel, A, Ortolano, S, Roper, SD et al. (2008). ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc Natl Acad Sci USA 105: 18770-18775.
25. Ortolano, S, Di Pasquale, G, Crispino, G, Anselmi, F, Mammano, F and Chiorini, JA (2008). Coordinated control of connexin 26 and connexin 30 at the regulatory and functional level in the inner ear. Proc Natl Acad Sci USA 105: 18776-18781.
26. Oshima, A, Doi, T, Mitsuoka, K, Maeda, S and Fujiyoshi, Y (2003). Roles of Met-34, Cys-64, and Arg-75 in the assembly of human connexin 26. Implication for key amino acid residues for channel formation and function. J Biol Chem 278: 1807-1816. (Pubitemid 36801417)
27. Deng, Y, Chen, Y, Reuss, L and Altenberg, GA (2006). Mutations of connexin 26 at position 75 and dominant deafness: essential role of arginine for the generation of functional gap-junctional channels. Hear Res 220: 87-94. (Pubitemid 44332009)
28. Kelsell, DP, Dunlop, J, Stevens, HP, Lench, NJ, Liang, JN, Parry, G et al. (1997). Connexin 26 mutations in hereditary non-syndromic sensorineural deafness. Nature 387: 80-83. (Pubitemid 27202653)
29. Maeda, Y, Fukushima, K, Nishizaki, K and Smith, RJ (2005). In vitro and in vivo suppression of GJB2 expression by RNA interference. Hum Mol Genet 14: 1641-1650. (Pubitemid 40895516)
30. Maeda, Y, Sheffield, AM and Smith, RJ (2009). Therapeutic regulation of gene expression in the inner ear using RNA interference. Adv Otorhinolaryngol 66: 13-36.
31. Gross, J, Stute, K, Moller, R, Fuchs, J, Amarjargal, N, Pohl, EE et al. (2010). Expression of prestin and Gata-3,-2,-1 mRNA in the rat organ of Corti during the postnatal period and in culture. Hear Res 261: 9-21.
32. Russell, IJ and Richardson, GP (1987). The morphology and physiology of hair cells in organotypic cultures of the mouse cochlea. Hear Res 31: 9-24. (Pubitemid 18016333)
33. Forge, A and Schacht, J (2000). Aminoglycoside antibiotics. Audiol Neurootol 5: 3-22. (Pubitemid 30093591)
34. Jagger, DJ and Forge, A (2006). Compartmentalized and signal-selective gap junctional coupling in the hearing cochlea. J Neurosci 26: 1260-1268. (Pubitemid 43237058)
35. Zorko, M and Langel, U (2005). Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv Drug Deliv Rev 57: 529-545. (Pubitemid 40255559)
36. Futaki, S, Nakase, I, Tadokoro, A, Takeuchi, T and Jones, AT (2007). Arginine-rich peptides and their internalization mechanisms. Biochem Soc Trans 35(Pt 4): 784-787. (Pubitemid 47310368)
37. Kaneko, T, Harasztosi, C, Mack, AF and Gummer, AW (2006). Membrane traffic in outer hair cells of the adult mammalian cochlea. Eur J Neurosci 23: 2712-2722. (Pubitemid 43801463)
38. Miwa, T, Minoda, R, Kaitsuka, T, Ise, M, Tomizawa, K and Yumoto, E (2011). Protein transduction into the mouse otocyst using arginine-rich cell-penetrating peptides. Neuroreport 22: 994-999.
39. Matsushita, M, Noguchi, H, Lu, YF, Tomizawa, K, Michiue, H, Li, ST et al. (2004). Photo-acceleration of protein release from endosome in the protein transduction system. FEBS Lett 572: 221-226. (Pubitemid 39092539)
40. Kilk, K, Mahlapuu, R, Soomets, U and Langel, U (2009). Analysis of in vitro toxicity of five cell-penetrating peptides by metabolic profiling. Toxicology 265: 87-95.
41. Kaur, T, Mukherjea, D, Sheehan, K, Jajoo, S, Rybak, LP and Ramkumar, V (2011). Short interfering RNA against STAT1 attenuates cisplatin-induced ototoxicity in the rat by suppressing inflammation. Cell Death Dis 2: e180.
42. Mukherjea, D, Jajoo, S, Kaur, T, Sheehan, KE, Ramkumar, V and Rybak, LP (2010). Transtympanic administration of short interfering (si)RNA for the NOX3 isoform of NADPH oxidase protects against cisplatin-induced hearing loss in the rat. Antioxid Redox Signal 13: 589-598.
43. Meyer, J, Mack, AF and Gummer, AW (2001). Pronounced infracuticular endocytosis in mammalian outer hair cells. HearRes 161: 10-22. (Pubitemid 34017160)
44. de Monvel, JB, Brownell, WE and Ulfendahl, M (2006). Lateral diffusion anisotropy and membrane lipid/skeleton interaction in outer hair cells. Biophys J 91: 364-381. (Pubitemid 44015333)
45. Griesinger, CB, Richards, CD and Ashmore, JF (2004). Apical endocytosis in outer hair cells of the mammalian cochlea. Eur J Neurosci 20: 41-50. (Pubitemid 38932125)
46. Hornung, V, Guenthner-Biller, M, Bourquin, C, Ablasser, A, Schlee, M, Uematsu, S et al. (2005). Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat Med 11: 263-270. (Pubitemid 40460553)
47. Forge, A, Marziano, NK, Casalotti, SO, Becker, DL and Jagger, D (2003). The inner ear contains heteromeric channels composed of cx26 and cx30 and deafness-related mutations in cx26 have a dominant negative effect on cx30. Cell Commun Adhes 10: 341-346. (Pubitemid 38081395)
48. Sun, J, Ahmad, S, Chen, S, Tang, W, Zhang, Y, Chen, P et al. (2005). Cochlear gap junctions coassembled from Cx26 and 30 show faster intercellular Ca2+ signaling than homomeric counterparts. Am J Physiol, Cell Physiol 288: C613-C623. (Pubitemid 40229490)
49. Andaloussi, SE, Lehto, T, Lundin, P and Langel, U (2011). Application of PepFect peptides for the delivery of splice-correcting oligonucleotides. Methods Mol Biol 683: 361-373.