Silencing of choline acetyltransferase expression by lentivirus-mediated RNA interference in cultured cells and in the adult rodent brain

Journal of Neuroscience Research

Volumn 87, Issue 2, 2009, Pages 532-544

  Santamaria, Julie ^a   Khalfallah, Olfa ^a,b   Sauty, Claire ^a   Brunet, Isabelle ^a   Sibieude, Mathieu ^a   Mallet, Jacques ^a   Berrard, Sylvie ^a   Lecomte, Maria José ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b CNRS   (France)

Author keywords

Cholinergic function; Knockdown; Lentiviral vector; Medial septum; NG108 15 cells

Indexed keywords

ACETYLCHOLINE; CHOLINE ACETYLTRANSFERASE; ENHANCED GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; MESSENGER RNA; SHORT HAIRPIN RNA; VESICULAR ACETYLCHOLINE TRANSPORTER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL LINE; CHOLINERGIC NERVE CELL; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPORTER GENE; RNA INTERFERENCE; RODENT; ANIMAL; BRAIN; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENE VECTOR; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; GENETICS; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; LENTIVIRINAE; METHODOLOGY; MOUSE; NERVE CELL; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN; CELLS, CULTURED; CHOLINE O-ACETYLTRANSFERASE; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC VECTORS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; LENTIVIRUS; MALE; MICE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; TRANSDUCTION, GENETIC; TRANSFECTION;

EID: 62849092335     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21866     Document Type: Article

References (48)

1. Akaneya Y, Jiang B, Tsumoto T. 2005. RNAi-induced gene silencing by local electroporation in targeting brain region. J Neurophysiol 93:594-602.
2. Amar L, Desclaux M, Faucon-Biguet N, Mallet J, Vogel R. 2006. Control of small inhibitory RNA levels and RNA interference by doxycycline induced activation of a minimal RNA polymerase III promoter. Nucleic Acids Res 34:e37.
3. An DS, Xie Y, Mao SH, Morizono K, Kung SK, Chen IS. 2003. Efficient lentiviral vectors for short hairpin RNA delivery into human cells. Hum Gene Ther 14:1207-1212.
4. Bäckman C, Zhang Y, Hoffer BJ, Tomac AC. 2003. Short interfering RNAs (siRNAs) for reducing dopaminergic phenotypic markers. J Neurosci Methods 131:51-56.
5. Brerer LM, Haroutunian V, Gabriel S, Knott PJ, Carlin LS, Purohit DP, Perl DP, Schmeidler J, Kanof P, Davis KL. 1995. Neurochemical correlates of dementia severity in Alzheimer's disease: relative importance of the cholinergic deficits. J Neurochem 64:749-760.
6. Blömer U, Naldini L, Kafri T, Trono D, Verma IM, Gage FH. 1997. Highly efficient and sustained gene transfer in adult neurons with-a lentivirus vector. J Virol 71:6641-6649.
7. Bot I, Guo J, Van Eck M, Van Santbrink PJ, Groot PH, Hildebrand RB, Seppen J, Van Berkel TJ, Biessen EA. 2005. Lentiviral shRNA silencing of murine bone marrow cell CCR2 leads to persistent knockdown of CCR2 function in vivo. Blood 106:1147-1153.
8. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
9. Brandon EP, Lin W, D'Amour KA, Pizzo DP, Dominguez B, Sugiura Y, Thode S, Ko CP, Thal LJ, Gage FH, Lee KF. 2003. Aberrant patterning of neuromuscular synapses in choline acetyltransferase-deficient mice. J Neurosci 23:539-549.
10. Brice A, Berrard S, Raynaud B, Ansieau S, Coppola T, Weber MJ, Mallet J. 1989. Complete sequence of a cDNA encoding an active rat choline acetyltransferase: a tool to investigate the plasticity of cholinergic phenotype expression. J Neurosci Res 23:266-273.
11. Brummelkamp TR, Bernards R, Agami R. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553.
12. Chen Y, Lin MC, Yao H, Wang H, Zhang AQ, Yu J, Hai CK, Lau GK, He ML, Sung J, Kung HF. 2007. Lentivirus-mediated RNA interference targeting enhancer of zeste homolog 2 inhibits hepatocellular carcinoma growth through down-regulation of stathmin. Hepatology 46:200-208.
13. De Gois S, Houhou L, Oda Y, Corbex M, Pajak F, Thevenot E, Vodjdani G, Mallet J, Berrard S. 2000. Is RE1/NRSE a common cis-regulatory sequence for ChAT and VAChT genes?. J Biol Chem 275: 36683-36690.
14. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
15. Fonnum F. 1975. A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem 24:407-409.
16. Friedman A, Behrens CJ, Heinemann U. 2007. Cholinergic dysfunction in temporal lobe epilepsy. Epilepsia 48(Suppl 5):126-130.
17. Hamprecht B. 1977. Structural, electrophysiological, biochemical, and pharmacological properties of neuroblastoma-glioma cell hybrids in cell culture. Int Rev Cytol 49:99-170.
18. Harborth J, Elbashir SM, Vandenburgh K, Manninga H, Scaringe SA, Weber K, Tuschl T. 2003. Sequence, chemical, and structural variation of small interfering RNAs and short hairpin RNAs and the effect on mammalian gene silencing. Antisense Nucleic Acid Drug Dev 13:83-105.
19. Heckers S, Ohtake T, Wiley RG, Lappi DA, Geula C, Mesulam MM. 1994. Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J Neurosci 14:1271-1289.
20. Hersh LB. 1992. Induction of choline acetyltransferase in the neuroblastoma X glioma cell line NG108-15. Neurochem Res 17:1063-1067.
21. Holen T, Amarzguioui M, Wiiger MT, Babaie E, Prydz H. 2002. Positional effects of short interfering RNAs targeting the human coagulation trigger tissue factor. Nucleic Acids Res 30:1757-1766.
22. Holt DJ, Herman MM, Hyde TM, Kleinman JE, Sinton CM, German DC, Hersh LB, Graybiel AM, Saper CB. 1999. Evidence for a deficit in cholinergic interneurons in the striatum in schizophrenia. Neuroscience 94:21-31.
23. Isacson R, Kull B, Salmi P, Wahlestedt C. 2003. Lack of efficacy of "naked" small interfering RNA applied directly to rat brain. Acta Physiol Scand 179:173-177.
24. Kengaku M, Misawa H, Deguchi T. 1993. Multiple mRNA species of choline acetyltransferase from rat spinal cord. Brain Res Mol Brain Res 18:71-76.
25. Khvorova A, Reynolds A, Jayasena SD. 2003. Functional siRNAs and miRNAs exhibit strand bias. Cell 115:209-216.
26. Komai S, Licznerski P, Cetin A, Waters J, Denk W, Brecht M, Osten P. 2006. Postsynaptic excitability is necessary for strengthening of cortical sensory responses during experience-dependent development. Nat Neurosci 9:1125-1133.
27. Lasek AW, Janak PH, He L, Whistler JL, Heberlein U. 2007. Downregulation of mu opioid receptor by RNA interference in the ventral teg-mental area reduces ethanol consumption in mice. Genes Brain Behav 6:728-735.
28. Makimura H, Mizuno TM, Mastaitis JW, Agami R, Mobbs CV. 2002. Reducing hypothalamic AGRP by RNA interference increases metabolic rate and decreases body weight without influencing food intake. BMC Neurosci 3:18.
29. Misawa H, Ishii K, Deguchi T. 1992. Gene expression of mouse choline acetyltransferase. Alternative splicing and identification of a highly active promoter region. J Biol Chem 267:20392-20399.
30. Misgeld T, Burgess RW, Lewis RM, Cunningham JM, Lichtman JW, Sanes JR. 2002. Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36:635-648.
31. Paxinos G, Watson C. 1982. The rat brain in stereotaxic coordinates. Sydney: Academic Press.
32. Pfeifer A, Eigenbrod S, Al-Khadra S, Hofmann A, Mitteregger G, Moser M, Bertsch U, Kretzschmar H. 2006. Lentivector-mediated RNAi efficiently suppresses prion protein and prolongs survival of scrapie-infected mice. J Clin Invest 116:3204-3210.
33. Pluta K, Diehl W, Zhang XY, Kutner R, Bialkowska A, Reiser J. 2007. Lentiviral vectors encoding tetracycline-dependent repressors and transactivators for reversible knockdown of gene expression: a comparative study. BMC Biotechnol 7:41.
34. Rosenberg RN, Vance CK, Morrison M, Prashad N, Meyne J, Baskin F. 1978. Differentiation of neuroblastoma, glioma, and hybrid cells in culture as measured by the synthesis of specific protein species: evidence for neuroblast-glioblast reciprocal genetic regulation. J Neurochem 30:1343-1355.
35. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, Rooney DL, Zhang M, Ihrig MM, McManus MT, Gertler FB, Scott ML, Van Parijs L. 2003. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 33:401-406.
36. Sapru MK, Yates JW, Hogan S, Jiang L, Halter J, Bohn MC. 2006. Silencing of human alpha-synuclein in vitro and in rat brain using lentiviral-mediated RNAi. Exp Neurol 198:382-390.
37. Tandon A, Bachoo M, Weldon P, Polosa C, Collier B. 1996. Effects of colchicine application to preganglionic axons on choline acetyltransferase activity and acetylcholine content and release in the superior cervical ganglion. J Neurochem 66:1033-1041.
38. Thakker DR, Natt F, Husken D, Maier R, Muller M, van der Putten H, Hoyer D, Cryan JF. 2004. Neurochemical and behavioral consequences of widespread gene knockdown in the adult mouse brain by using nonviral RNA interference. Proc Natl Acad Sci U S A 101: 17270-17275.
39. Thakker DR, Natt F, Husken D, van der Putten H, Maier R, Hoyer D, Cryan JF. 2005. siRNA-mediated knockdown of the serotonin transporter in the adult mouse brain. Mol Psychiatry 10:782-789, 714.
40. Tiscornia G, Singer O, Ikawa M, Verma IM. 2003. A general method for gene knockdown in mice by using lentiviral vectors expressing small interfering RNA. Proc Natl Acad Sci U S A 100:1844-1848.
41. Van den Haute C, Eggermont K, Nuttin B, Debyser Z, Baekelandt V. 2003. Lentiviral vector-mediated delivery of short hairpin RNA results in persistent knockdown of gene expression in mouse brain. Hum Gene Ther 14:1799-1807.
42. Waite JJ, Thal LJ. 1996. Lesions of the cholinergic nuclei in the rat basal forebrain: excitotoxins vs. an immunotoxin. Life Sci 58:1947-1953.
43. Walsh TJ, Kelly RM, Dougherty KD, Stackman RW, Wiley RG, Kutscher CL. 1995. Behavioral and neurobiological alterations induced by the immunotoxin 192-IgG-saporin: cholinergic and noncholinergic effects following i.c.v. injection. Brain Res 702:233-245.
44. Wenthold RJ, Mahler HR. 1975. Purification of rat brain choline acetyltransferase and an estimation of its half-life. J Neurochem 24:963-967.
45. Wiley RG, Oeltmann TN, Lappi DA. 1991. Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res 562:149-153.
46. Wiznerowicz M, Szulc J, Trono D. 2006. Tuning silence: conditional systems for RNA interference. Nat Methods 3:682-688.
47. Wrenn CC, Lappi DA, Wiley RG. 1999. Threshold relationship between lesion extent of the cholinergic basal forebrain in the rat and working memory impairment in the radial maze. Brain Res 847:284-298.
48. Zennou V, Serguera C, Sarkis C, Colin P, Perret E, Mallet J, Chameau P. 2001. The HIV-1 DNA flap stimulates HIV vector-mediated cell transduction in the brain. Nat Biotechnol 19:446-450.