Efficient CPP-mediated Cre protein delivery to developing and adult CNS tissues

BMC Biotechnology

Volumn 9, Issue , 2009, Pages

  Gitton, Yorick ^a,b   Tibaldi, Lorenzo ^b   Dupont, Edmond ^b   Levi, Giovanni ^a   Joliot, Alain ^b,c  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c l'alimentation et l'Environnement   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT BRAINS; APPLIED RESEARCHES; BIOLOGICAL ACTIVITIES; CELL TARGETING; CELL-PENETRATING PEPTIDES; CENTRAL NERVOUS SYSTEM TISSUES; CRE RECOMBINASE; CULTURED CELLS; ENZYMATIC ACTIVITIES; GENE DELIVERIES; GENE FUNCTIONS; GENETIC MODIFICATIONS; NEURAL CELLS; NEURAL TISSUES; NEURODEGENERATIVE; NON-VIRAL; ORGANOTYPIC CULTURES; PHYSIOLOGICAL CONDITIONS; PROOF OF CONCEPTS; PROTEIN CONJUGATES; PROTEIN DELIVERIES; REPORTER-GENE EXPRESSIONS; SPINAL CORDS;

AMINES; BIOACTIVITY; CELL MEMBRANES; GENE EXPRESSION; GENE TRANSFER; HISTOLOGY; PROTEINS; TISSUE;

CELL CULTURE;

CRE RECOMBINASE; HYBRID PROTEIN; INTEGRASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONJUGATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE FUSION; GENE TARGETING; GENETIC RECOMBINATION; GENETIC TRANSDUCTION; IMMUNODETECTION; MOUSE; NERVE CELL CULTURE; NERVOUS TISSUE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CYTOLOGY; GENE TRANSFER; GENE VECTOR; INNERVATION; METABOLISM; NERVE CELL; PLASMID; PRENATAL DEVELOPMENT; TRANSGENIC MOUSE;

MUS;

ANIMALS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; EMBRYO, MAMMALIAN; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; INTEGRASES; MICE; MICE, TRANSGENIC; NEURONS; PLASMIDS; RECOMBINANT FUSION PROTEINS; RECOMBINATION, GENETIC; TRANSDUCTION, GENETIC;

EID: 65649131227     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/1472-6750-9-40     Document Type: Article

References (53)

1. Rakic P Hashimoto-Torii K Sarkisian MR Genetic determinants of neuronal migration in the cerebral cortex Novartis Foundation Symposium 2007, 288:45-53. 18494251
2. Lemkine GF Goula D Becker N Paleari L Levi G Demeneix BA Optimisation of polyethylenimine-based gene delivery to mouse brain J Drug Target 1999, 7(4):305-312. 10682909
3. Goula D Remy JS Erbacher P Wasowicz M Levi G Abdallah B Demeneix BA Size, diffusibility and transfection performance of linear PEI/DNA complexes in the mouse central nervous system Gene Ther 1998, 5(5):712-717. 9797878
4. Lemkine GF Mantero S Migne C Raji A Goula D Normandie P Levi G Demeneix BA Preferential transfection of adult mouse neural stem cells and their immediate progeny in vivo with polyethylenimine Mol Cell Neurosci 2002, 19(2):165-174. 11860270
5. Prochiantz A Getting hydrophilic compounds into cells: Lessons from homeopeptides Curr Opin Neurobiol 1996, 6(5):629-634. 8937827
6. Lindgren M Hallbrink M Prochiantz A Langel U Cell-penetrating peptides Trends Pharmacol Sci 2000, 21(3):99-103. 10689363
7. Prochiantz A Messenger proteins: Homeoproteins, TAT and others Curr Opin Cell Biol 2000, 12(4):400-406. 10873818
8. Joliot A Prochiantz A Transduction peptides: From technology to physiology Nat Cell Biol 2004, 6(3):189-196. 15039791
9. Stewart KM Horton KL Kelley SO Cell-penetrating peptides as delivery vehicles for biology and medicine Org Biomol Chem 2008, 6(13):2242-2255. 18563254
10. Schwarze SR Ho A Vocero-Akbani A Dowdy SF In vivo protein transduction: delivery of a biologically active protein into the mouse Science 1999, 285(5433):1569-1572. 10477521
11. Joliot A Prochiantz A Homeoproteins as natural Penetratin cargoes with signaling properties Adv Drug Deliv Rev 2008, 60(4-5):608-613. 18037528
12. Cai SR Xu G Becker-Hapak M Ma M Dowdy SF McLeod HL The kinetics and tissue distribution of protein transduction in mice Eur J Pharm Sci 2006, 27(4):311-319. 16376528
13. Peitz M Pfannkuche K Rajewsky K Edenhofer F Ability of the hydrophobic FGF and basic TAT peptides to promote cellular uptake of recombinant Cre recombinase: A tool for efficient genetic engineering of mammalian genomes Proc Natl Acad Sci USA 2002, 99(7):4489-4494. 123675 11904364
14. Jo D Nashabi A Doxsee C Lin Q Unutmaz D Chen J Ruley HE Epigenetic regulation of gene structure and function with a cell-permeable Cre recombinase Nat Biotechnol 2001, 19(10):929-933. 11581657
15. Nolden L Edenhofer F Peitz M Brustle O Stem cell engineering using transducible Cre recombinase Methods Mol Med 2007, 140:17-32. 18085201
16. Xu Y Liu S Yu G Chen J Chen J Xu X Wu Y Zhang A Dowdy SF Cheng G Excision of selectable genes from transgenic goat cells by a protein transducible TAT-Cre recombinase Gene 2008, 419(1):70-74. 18547746
17. Hashimoto M Taniguchi M Yoshino S Arai S Sato K S Phase-preferential Cre-recombination in mammalian cells revealed by HIV-TAT-PTD-mediated protein transduction Journal of Biochemistry 2008, 143(1):87-95. 17965427
18. Yu BD Becker-Hapak M Snyder EL Vooijs M Denicourt C Dowdy SF Distinct and nonoverlapping roles for pRB and cyclin D: cyclin-dependent kinases 4/6 activity in melanocyte survival Proc Natl Acad Sci USA 2003, 100(25):14881-14886. 299840 14630948
19. Sauer B Henderson N Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1 Proc Natl Acad Sci USA 1988, 85(14):5166-5170. 281709 2839833
20. Melan MA Sluder G Redistribution and differential extraction of soluble proteins in permeabilized cultured cells. Implications for immunofluorescence microscopy J Cell Sci 1992, 101(Pt 4):731-743. 1527176
21. Holm T Johansson H Lundberg P Pooga M Lindgren M Langel U Studying the uptake of cell-penetrating peptides Nat Protoc 2006, 1(2):1001-1005. 17406337
22. Lundberg M Wikstrom S Johansson M Cell surface adherence and endocytosis of protein transduction domains Mol Ther 2003, 8(1):143-150. 12842437
23. Lundberg M Johansson M Positively charged DNA-binding proteins cause apparent cell membrane translocation Biochem Biophys Res Commun 2002, 291(2):367-371. 11846414
24. Lundberg M Johansson M Is VP22 nuclear homing an artifact? Nat Biotechnol 2001, 19(8):713-714. 11479552
25. Ross MF Filipovska A Smith RA Gait MJ Murphy MP Cell-penetrating peptides do not cross mitochondrial membranes even when conjugated to a lipophilic cation: Evidence against direct passage through phospholipid bilayers Biochem J 2004, 383(Pt 3):457-468. 1133738 15270716
26. Sauer B Identification of cryptic lox sites in the yeast genome by selection for Cre-mediated chromosome translocations that confer multiple drug resistance J Mol Biol 1992, 223(4):911-928. 1554399
27. Thyagarajan B Guimaraes MJ Groth AC Calos MP Mammalian genomes contain active recombinase recognition sites Gene 2000, 244(1-2):47-54. 10689186
28. Loonstra A Vooijs M Beverloo HB Allak BA van Drunen E Kanaar R Berns A Jonkers J Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells Proc Natl Acad Sci USA 2001, 98(16):9209-9214. 55399 11481484
29. Takayama K Torashima T Horiuchi H Hirai H Purkinje-cell-preferential transduction by lentiviral vectors with the murine stem cell virus promoter Neurosci Lett 2008, 443(1):7-11. 18675313
30. Will E Klump H Heffner N Schwieger M Schiedlmeier B Ostertag W Baum C Stocking C Unmodified Cre recombinase crosses the membrane Nucleic Acids Res 2002, 30(12):e59. 117301 12060697
31. Lin Q Jo D Gebre-Amlak KD Ruley HE Enhanced cell-permeant Cre protein for site-specific recombination in cultured cells BMC Biotechnol 2004, 4:25. 529453 15500682
32. Kellendonk C Tronche F Monaghan AP Angrand PO Stewart F Schutz G Regulation of Cre recombinase activity by the synthetic steroid RU 486 Nucleic Acids Res 1996, 24(8):1404-1411. 145830 8628671
33. Dupont E Prochiantz A Joliot A Identification of a signal peptide for unconventional secretion J Biol Chem 2007, 282(12):8994-9000. 17242404
34. Gitton Y Cohen-Tannoudji M Wassef M Role of thalamic axons in the expression of H-2Z1, a mouse somatosensory cortex specific marker Cereb Cortex 1999, 9(6):611-620. 10498279
35. Gitton Y Cohen-Tannoudji M Wassef M Specification of somatosensory area identity in cortical explants J Neurosci 1999, 19(12):4889-4898. 10366623
36. Dahmane N Sanchez P Gitton Y Palma V Sun T Beyna M Weiner H Ruiz i Altaba A The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumorigenesis Development 2001, 128:24-5201-5212. 11748155
37. Joliot AH Triller A Volovitch M Pernelle C Prochiantz A alpha-2,8-Polysialic acid is the neuronal surface receptor of antennapedia homeobox peptide New Biol 1991, 3(11):1121-1134. 1777485
38. Bielle F Griveau A Narboux-Neme N Vigneau S Sigrist M Arber S Wassef M Pierani A Multiple origins of Cajal-Retzius cells at the borders of the developing pallium Nat Neurosci 2005, 8(8):1002-1012. 16041369
39. Raineteau O Hugel S Ozen I Rietschin L Sigrist M Arber S Gahwiler BH Conditional labeling of newborn granule cells to visualize their integration into established circuits in hippocampal slice cultures Mol Cell Neurosci 2006, 32(4):344-355. 16828306
40. Cao G Pei W Ge H Liang Q Luo Y Sharp FR Lu A Ran R Graham SH Chen J In Vivo Delivery of a Bcl-xL Fusion Protein Containing the TAT Protein Transduction Domain Protects against Ischemic Brain Injury and Neuronal Apoptosis J Neurosci 2002, 22(13):5423-5431. 12097494
41. Asoh S Ohsawa I Mori T Katsura K Hiraide T Katayama Y Kimura M Ozaki D Yamagata K Ohta S Protection against ischemic brain injury by protein therapeutics Proc Natl Acad Sci USA 2002, 99(26):17107-17112. 139277 12475933
42. Silver DP Livingston DM Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity Mol Cell 2001, 8(1):233-243. 11511376
43. Baba Y Nakano M Yamada Y Saito I Kanegae Y Practical range of effective dose for Cre recombinase-expressing recombinant adenovirus without cell toxicity in mammalian cells Microbiol Immunol 2005, 49(6):559-570. 15965304
44. Rakic P Specification of cerebral cortical areas Science 1988, 241(4862):170-176. 3291116
45. Bystron I Blakemore C Rakic P Development of the human cerebral cortex: Boulder Committee revisited Nature Review Neuroscience 2008, 9(2):110-122.
46. Ruiz i Altaba A Gitton Y Dahmane N Embryonic regionalization of the neocortex Mech Dev 2001, 107(1-2):3-11. 11520659
47. Cantor EJ Chong S Intein-mediated rapid purification of Cre recombinase Protein Expr Purif 2001, 22(1):135-140. 11388811
48. Soriano P Generalized lacZ expression with the ROSA26 Cre reporter strain Nat Genet 1999, 21(1):70-71. 9916792
49. Srinivas S Watanabe T Lin CS William CM Tanabe Y Jessell TM Costantini F Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus BMC Dev Biol 2001, 1:4. 31338 11299042
50. Lobe CG Koop KE Kreppner W Lomeli H Gertsenstein M Nagy A Z/AP, a double reporter for cre-mediated recombination Dev Biol 1999, 208(2):281-292. 10191045
51. Hippenmeyer S Vrieseling E Sigrist M Portmann T Laengle C Ladle DR Arber S A developmental switch in the response of DRG neurons to ETS transcription factor signaling PLoS Biol 2005, 3(5):e159. 1084331 15836427
52. De Paola V Arber S Caroni P AMPA receptors regulate dynamic equilibrium of presynaptic terminals in mature hippocampal networks Nat Neurosci 2003, 6(5):491-500. 12692557
53. Benouaiche L Gitton Y Vincent C Couly G Levi G Sonic hedgehog signalling from foregut endoderm patterns the avian nasal capsule Development 2008, 135(13):2221-2225. 18539922