Endocytic pathway and resistance to cholesterol depletion of cholesterol derived cationic lipids for gene delivery

Molecular Pharmaceutics

Volumn 9, Issue 12, 2012, Pages 3579-3585

  Bae, Yun Ui ^a   Kim, Bieong Kil ^b   Park, Jong Won ^a   Seu, Young Bae ^b   Doh, Kyung Oh ^a  

^a Yeungnam University   (South Korea)

^b Kyungpook National University   (South Korea)

Author keywords

cholesterol; endocytic pathway; gene delivery; nonviral vector

Indexed keywords

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; CATION; CHOL E LIPOPLEX; CHOLESTEROL; CLATHRIN; GENISTEIN; LIPID; LIPOPLEX; LIPOSOME; LUCIFERASE; MEVINOLIN; PLASMID DNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOCOMPATIBILITY; CAVEOLA; CELL MEMBRANE; CELL VIABILITY; CELLULAR DISTRIBUTION; CHOLESTEROL DEPLETION; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DEPLETION; ENDOCYTOSIS; ENDOSOME; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSFECTION; INTERNALIZATION; LYSOSOME; NONHUMAN; PARTICLE SIZE; PINOCYTOSIS; PRIORITY JOURNAL;

ANIMALS; BETA-CYCLODEXTRINS; CATIONS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CHOLESTEROL; COS CELLS; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; FATTY ACIDS, MONOUNSATURATED; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; MEMBRANE LIPIDS; QUATERNARY AMMONIUM COMPOUNDS;

EID: 84870506800     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300458h     Document Type: Article

References (45)

1. Anwer, K.; Barnes, M. N.; Fewell, J.; Lewis, D. H.; Alvarez, R. D. Phase-I clinical trial of IL-12 plasmid/lipopolymer complexes for the treatment of recurrent ovarian cancer Gene Ther. 2010, 17 (3) 360-9
2. Kawase, Y.; Ladage, D.; Hajjar, R. J. Rescuing the failing heart by targeted gene transfer J. Am. College Cardiol. 2011, 57 (10) 1169-80
3. El-Aneed, A. An overview of current delivery systems in cancer gene therapy J. Controlled Release 2004, 94 (1) 1-14 (Pubitemid 37542373)
4. Garcia, L.; Bunuales, M.; Duzgunes, N.; Tros de Ilarduya, C. Serum-resistant lipopolyplexes for gene delivery to liver tumour cells Eur. J. Pharm. Biopharm. 2007, 67 (1) 58-66 (Pubitemid 46991330)
5. Zhi, D.; Zhang, S.; Wang, B.; Zhao, Y.; Yang, B.; Yu, S. Transfection efficiency of cationic lipids with different hydrophobic domains in gene delivery Bioconjugate Chem. 2010, 21 (4) 563-77
6. Xu, L.; Anchordoquy, T. J. Cholesterol domains in cationic lipid/DNA complexes improve transfection Biochim. Biophys. Acta 2008, 1778 (10) 2177-81
7. Medvedeva, D. A.; Maslov, M. A.; Serikov, R. N.; Morozova, N. G.; Serebrenikova, G. A.; Sheglov, D. V.; Latyshev, A. V.; Vlassov, V. V.; Zenkova, M. A. Novel cholesterol-based cationic lipids for gene delivery J. Med. Chem. 2009, 52 (21) 6558-68
8. Tagami, T.; Barichello, J. M.; Kikuchi, H.; Ishida, T.; Kiwada, H. The gene-silencing effect of siRNA in cationic lipoplexes is enhanced by incorporating pDNA in the complex Int. J. Pharm. 2007, 333 (1-2) 62-9 (Pubitemid 46283268)
9. Spagnou, S.; Miller, A. D.; Keller, M. Lipidic carriers of siRNA: differences in the formulation, cellular uptake, and delivery with plasmid DNA Biochemistry 2004, 43 (42) 13348-56 (Pubitemid 39391135)
10. Han, S. E.; Kang, H.; Shim, G. Y.; Suh, M. S.; Kim, S. J.; Kim, J. S.; Oh, Y. K. Novel cationic cholesterol derivative-based liposomes for serum-enhanced delivery of siRNA Int. J. Pharm. 2008, 353 (1-2) 260-9
11. Zhang, Y.; Bradshaw-Pierce, E. L.; Delille, A.; Gustafson, D. L.; Anchordoquy, T. J. In vivo comparative study of lipid/DNA complexes with different in vitro serum stability: effects on biodistribution and tumor accumulation J. Pharm. Sci. 2008, 97 (1) 237-50
12. Xu, L.; Anchordoquy, T. J. Effect of cholesterol nanodomains on the targeting of lipid-based gene delivery in cultured cells Mol. Pharm. 2010, 7 (4) 1311-7
13. Marchini, C.; Montani, M.; Amici, A.; Amenitsch, H.; Marianecci, C.; Pozzi, D.; Caracciolo, G. Structural stability and increase in size rationalize the efficiency of lipoplexes in serum Langmuir 2009, 25 (5) 3013-21
14. Kim, B. K.; Doh, K. O.; Nam, J. H.; Kang, H.; Park, J. G.; Moon, I. J.; Seu, Y. B. Synthesis of novel cholesterol-based cationic lipids for gene delivery Bioorg. Med. Chem. Lett. 2009, 19 (11) 2986-9
15. Rejman, J.; Bragonzi, A.; Conese, M. Role of clathrin- and caveolae-mediated endocytosis in gene transfer mediated by lipo- and polyplexes Mol. Ther. 2005, 12 (3) 468-74 (Pubitemid 41150132)
16. Wong, A. W.; Scales, S. J.; Reilly, D. E. DNA internalized via caveolae requires microtubule-dependent, Rab7-independent transport to the late endocytic pathway for delivery to the nucleus J. Biol. Chem. 2007, 282 (31) 22953-63 (Pubitemid 47267352)
17. van der Aa, M. A.; Huth, U. S.; Hafele, S. Y.; Schubert, R.; Oosting, R. S.; Mastrobattista, E.; Hennink, W. E.; Peschka-Suss, R.; Koning, G. A.; Crommelin, D. J. Cellular uptake of cationic polymer-DNA complexes via caveolae plays a pivotal role in gene transfection in COS-7 cells Pharm. Res. 2007, 24 (8) 1590-8 (Pubitemid 46988225)
18. Caracciolo, G.; Callipo, L.; De Sanctis, S. C.; Cavaliere, C.; Pozzi, D.; Lagana, A. Surface adsorption of protein corona controls the cell internalization mechanism of DC-Chol-DOPE/DNA lipoplexes in serum Biochim. Biophys. Acta 2010, 1798 (3) 536-43
19. Irie, T.; Fukunaga, K.; Pitha, J. Hydroxypropylcyclodextrins in parenteral use. I: Lipid dissolution and effects on lipid transfers in vitro J. Pharm. Sci. 1992, 81 (6) 521-3
20. Rodal, S. K.; Skretting, G.; Garred, O.; Vilhardt, F.; van Deurs, B.; Sandvig, K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles Mol. Biol. Cell 1999, 10 (4) 961-74 (Pubitemid 29193724)
21. Lee, C. J.; Lin, H. R.; Liao, C. L.; Lin, Y. L. Cholesterol effectively blocks entry of flavivirus J. Virol. 2008, 82 (13) 6470-80
22. Khalil, I. A.; Kogure, K.; Akita, H.; Harashima, H. Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery Pharmacol. Rev. 2006, 58 (1) 32-45
23. von Gersdorff, K.; Sanders, N. N.; Vandenbroucke, R.; De Smedt, S. C.; Wagner, E.; Ogris, M. The internalization route resulting in successful gene expression depends on both cell line and polyethylenimine polyplex type Mol. Ther. 2006, 14 (5) 745-53 (Pubitemid 44480760)
24. Duan, Y.; Zhang, S.; Wang, B.; Yang, B.; Zhi, D. The biological routes of gene delivery mediated by lipid-based non-viral vectors Expert O pin. Drug Delivery 2009, 6 (12) 1351-61
25. Conner, S. D.; Schmid, S. L. Regulated portals of entry into the cell Nature 2003, 422 (6927) 37-44 (Pubitemid 36323287)
26. Vercauteren, D.; Vandenbroucke, R. E.; Jones, A. T.; Rejman, J.; Demeester, J.; De Smedt, S. C.; Sanders, N. N.; Braeckmans, K. The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls Mol. Ther. 2010, 18 (3) 561-9
27. Cardarelli, F.; Pozzi, D.; Bifone, A.; Marchini, C.; Caracciolo, G. Cholesterol-dependent macropinocytosis and endosomal escape control the transfection efficiency of lipoplexes in CHO living cells Mol. Pharm. 2012, 9 (2) 334-40
28. Zhang, X. X.; Allen, P. G.; Grinstaff, M. Macropinocytosis is the major pathway responsible for DNA transfection in CHO cells by a charge-reversal amphiphile Mol. Pharm. 2011, 8 (3) 758-66
29. Douglas, K. L.; Piccirillo, C. A.; Tabrizian, M. Cell line-dependent internalization pathways and intracellular trafficking determine transfection efficiency of nanoparticle vectors Eur. J. Pharm. Biopharm. 2008, 68 (3) 676-87 (Pubitemid 351318216)
30. Izumisawa, T.; Hattori, Y.; Date, M.; Toma, K.; Maitani, Y. Cell line-dependent internalization pathways determine DNA transfection efficiency of decaarginine-PEG-lipid Int. J. Pharm. 2011, 404 (1-2) 264-70
31. Serikawa, T.; Kikuchi, H.; Oite, T.; Tanaka, K. Enhancement of gene expression efficiency using cationic liposomes on ovarian cancer cells Drug Delivery 2008, 15 (8) 523-9
32. Zuhorn, I. S.; Kalicharan, R.; Hoekstra, D. Lipoplex-mediated transfection of mammalian cells occurs through the cholesterol-dependent clathrin-mediated pathway of endocytosis J. Biol. Chem. 2002, 277 (20) 18021-8 (Pubitemid 34967614)
33. Marchini, C.; Pozzi, D.; Montani, M.; Alfonsi, C.; Amici, A.; Candeloro De Sanctis, S.; Digman, M. A.; Sanchez, S.; Gratton, E.; Amenitsch, H.; Fabbretti, A.; Gualerzi, C. O.; Caracciolo, G. Role of temperature-independent lipoplex-cell membrane interactions in the efficiency boost of multicomponent lipoplexes Cancer Gene Ther. 2011, 18 (8) 543-52
34. Pozzi, D.; Marchini, C.; Cardarelli, F.; Amenitsch, H.; Garulli, C.; Bifone, A.; Caracciolo, G. Transfection efficiency boost of cholesterol- containing lipoplexes Biochim. Biophys. Acta 2012, 1818 (9) 2335-43
35. Walczyk, D.; Bombelli, F. B.; Monopoli, M. P.; Lynch, I.; Dawson, K. A. What the cell "sees" in bionanoscience J. Am. Chem. Soc. 2010, 132 (16) 5761-8
36. Capriotti, A. L.; Caracciolo, G.; Caruso, G.; Foglia, P.; Pozzi, D.; Samperi, R.; Lagana, A. Differential analysis of protein corona profile adsorbed onto different nonviral gene delivery systems Anal. Biochem. 2011, 419 (2) 180-9
37. Caracciolo, G.; Pozzi, D.; Capriotti, A. L.; Cavaliere, C.; Foglia, P.; Amenitsch, H.; Lagana, A. Evolution of the protein corona of lipid gene vectors as a function of plasma concentration Langmuir 2011, 27 (24) 15048-53
38. Gref, R.; Minamitake, Y.; Peracchia, M. T.; Trubetskoy, V.; Torchilin, V.; Langer, R. Biodegradable long-circulating polymeric nanospheres Science (New York, N.Y.) 1994, 263 (5153) 1600-3 (Pubitemid 24128361)
39. Illum, L.; Davis, S. S. The organ uptake of intravenously administered colloidal particles can be altered using a non-ionic surfactant (Poloxamer 338) FEBS Lett. 1984, 167 (1) 79-82 (Pubitemid 14198834)
40. Kaul, G.; Amiji, M. Long-circulating poly(ethylene glycol)-modified gelatin nanoparticles for intracellular delivery Pharm. Res. 2002, 19 (7) 1061-7 (Pubitemid 34804251)
41. Zelphati, O.; Uyechi, L. S.; Barron, L. G.; Szoka, F. C., Jr. Effect of serum components on the physico-chemical properties of cationic lipid/oligonucleotide complexes and on their interactions with cells Biochim. Biophys. Acta 1998, 1390 (2) 119-33 (Pubitemid 28122331)
42. Almofti, M. R.; Harashima, H.; Shinohara, Y.; Almofti, A.; Li, W.; Kiwada, H. Lipoplex size determines lipofection efficiency with or without serum Mol. Membr. Biol. 2003, 20 (1) 35-43 (Pubitemid 36460644)
43. Rejman, J.; Oberle, V.; Zuhorn, I. S.; Hoekstra, D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis Biochem. J. 2004, 377 (Pt 1) 159-69 (Pubitemid 38114443)
44. Rejman, J.; Conese, M.; Hoekstra, D. Gene transfer by means of lipo- and polyplexes: role of clathrin and caveolae-mediated endocytosis J. Liposome Res. 2006, 16 (3) 237-47 (Pubitemid 44358997)
45. Hoekstra, D.; Rejman, J.; Wasungu, L.; Shi, F.; Zuhorn, I. Gene delivery by cationic lipids: in and out of an endosome Biochem. Soc. Trans. 2007, 35 (Pt 1) 68-71