 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, September 15, 1999, 19(18):7711-7720
Neuronal Expression of Neural Nitric Oxide Synthase (nNOS) Protein Is Suppressed by an Antisense RNA Transcribed from an NOS Pseudogene
Sergei A. Korneev, Ji-Ho Park, and Michael O'Shea Sussex Centre for Neuroscience, School of Biological Sciences, University of Sussex, Brighton, East Sussex, BN1 9QG, United Kingdom
Here, we show that a nitric oxide synthase (NOS) pseudogene is expressed in the CNS of the snail Lymnaea stagnalis. The pseudo-NOS transcript includes a region of significant antisense homology to a previously reported neuronal NOS (nNOS)-encoding mRNA. This suggested that the pseudo-NOS transcript acts as a natural antisense regulator of nNOS protein synthesis. In support of this, we show that both the nNOS-encoding and the pseudo-NOS transcripts are coexpressed in giant identified neurons (the cerebral giant cells) in the cerebral ganglion. Moreover, reverse transcription-PCR experiments on RNA isolated from the CNS establish that stable RNA-RNA duplex molecules do form between the two transcripts in vivo. Using an in vitro translation assay, we further demonstrate that the antisense region of the pseudogene transcript prevents the translation of nNOS protein from the nNOS-encoding mRNA. By analyzing NOS RNA and nNOS protein expression in two different identified neurons, we find that when both the nNOS-encoding and the pseudo-NOS transcripts are present in the same neuron, nNOS enzyme activity is substantially suppressed. Importantly, these results show that a natural antisense mechanism can mediate the translational control of nNOS expression in the Lymnaea CNS. Our findings also suggest that transcribed pseudogenes are not entirely without purpose and are a potential source of a new class of regulatory gene in the nervous system.
Key words: nNOS; antisense; pseudogene; translational regulation; dsRNA; RNA interface
Copyright © 1999 Society for Neuroscience 0270-6474/99/19187711-10$05.00/0
This article has been cited by other articles:
J.-T. Li, Y. Zhang, L. Kong, Q.-R. Liu, and L. Wei
Trans-natural antisense transcripts including noncoding RNAs in 10 species: implications for expression regulation
Nucleic Acids Res., September 1, 2008; 36(15): 4833 - 4844.
[Abstract] [Full Text] [PDF]
K. Rull, P. Hallast, L. Uuskula, J. Jackson, M. Punab, A. Salumets, R.K. Campbell, and M. Laan
Fine-scale quantification of HCG beta gene transcription in human trophoblastic and non-malignant non-trophoblastic tissues
Mol. Hum. Reprod., January 1, 2008; 14(1): 23 - 31.
[Abstract] [Full Text] [PDF]
D. V. Babushok, K. Ohshima, E. M. Ostertag, X. Chen, Y. Wang, P. K. Mandal, N. Okada, C. S. Abrams, and H. H. Kazazian Jr.
A novel testis ubiquitin-binding protein gene arose by exon shuffling in hominoids
Genome Res., August 1, 2007; 17(8): 1129 - 1138.
[Abstract] [Full Text] [PDF]
J. P. Rinehart, A. Li, G. D. Yocum, R. M. Robich, S. A. L. Hayward, and D. L. Denlinger
Inaugural Article: Up-regulation of heat shock proteins is essential for cold survival during insect diapause
PNAS, July 3, 2007; 104(27): 11130 - 11137.
[Abstract] [Full Text] [PDF]
M. F. Mehler and J. S. Mattick
Noncoding RNAs and RNA Editing in Brain Development, Functional Diversification, and Neurological Disease
Physiol Rev, July 1, 2007; 87(3): 799 - 823.
[Abstract] [Full Text] [PDF]
M. B. Gerstein, C. Bruce, J. S. Rozowsky, D. Zheng, J. Du, J. O. Korbel, O. Emanuelsson, Z. D. Zhang, S. Weissman, and M. Snyder
What is a gene, post-ENCODE? History and updated definition
Genome Res., June 1, 2007; 17(6): 669 - 681.
[Abstract] [Full Text] [PDF]
Y. Ruan, H. S. Ooi, S. W. Choo, K. P. Chiu, X. D. Zhao, K.G. Srinivasan, F. Yao, C. Y. Choo, J. Liu, P. Ariyaratne, et al.
Fusion transcripts and transcribed retrotransposed loci discovered through comprehensive transcriptome analysis using Paired-End diTags (PETs)
Genome Res., June 1, 2007; 17(6): 828 - 838.
[Abstract] [Full Text] [PDF]
D. Zheng, A. Frankish, R. Baertsch, P. Kapranov, A. Reymond, S. W. Choo, Y. Lu, F. Denoeud, S. E. Antonarakis, M. Snyder, et al.
Pseudogenes in the ENCODE regions: Consensus annotation, analysis of transcription, and evolution
Genome Res., June 1, 2007; 17(6): 839 - 851.
[Abstract] [Full Text] [PDF]
N. Osato, Y. Suzuki, K. Ikeo, and T. Gojobori
Transcriptional Interferences in cis Natural Antisense Transcripts of Humans and Mice
Genetics, June 1, 2007; 176(2): 1299 - 1306.
[Abstract] [Full Text] [PDF]
H. Rompler, C. Staubert, D. Thor, A. Schulz, M. Hofreiter, and T. Schoneberg
G Protein-Coupled Time Travel: Evolutionary Aspects of GPCR Research
Mol. Interv., February 1, 2007; 7(1): 17 - 25.
[Abstract] [Full Text] [PDF]
V. A. Straub, J. Grant, M. O'Shea, and P. R. Benjamin
Modulation of Serotonergic Neurotransmission by Nitric Oxide
J Neurophysiol, February 1, 2007; 97(2): 1088 - 1099.
[Abstract] [Full Text] [PDF]
K. V. Prasanth and D. L. Spector
Eukaryotic regulatory RNAs: an answer to the 'genome complexity' conundrum
Genes & Dev., January 1, 2007; 21(1): 11 - 42.
[Abstract] [Full Text] [PDF]
A. Yao, R. Charlab, and P. Li
Systematic identification of pseudogenes through whole genome expression evidence profiling
Nucleic Acids Res., September 11, 2006; 34(16): 4477 - 4485.
[Abstract] [Full Text] [PDF]
S. Kaneko, I. Aki, K. Tsuda, K. Mekada, K. Moriwaki, N. Takahata, and Y. Satta
Origin and Evolution of Processed Pseudogenes That Stabilize Functional Makorin1 mRNAs in Mice, Primates and Other Mammals
Genetics, April 1, 2006; 172(4): 2421 - 2429.
[Abstract] [Full Text] [PDF]
S. J. Elliman, I. Wu, and D. M. Kemp
Adult Tissue-specific Expression of a Dppa3-derived Retrogene Represents a Postnatal Transcript of Pluripotent Cell Origin
J. Biol. Chem., January 6, 2006; 281(1): 16 - 19.
[Abstract] [Full Text] [PDF]
R. E. van Kesteren, C. Carter, H. M. G. Dissel, J. van Minnen, Y. Gouwenberg, N. I. Syed, G. E. Spencer, and A. B. Smit
Local Synthesis of Actin-Binding Protein {beta}-Thymosin Regulates Neurite Outgrowth
J. Neurosci., January 4, 2006; 26(1): 152 - 157.
[Abstract] [Full Text] [PDF]
M. Nei
Selectionism and Neutralism in Molecular Evolution
Mol. Biol. Evol., December 1, 2005; 22(12): 2318 - 2342.
[Abstract] [Full Text] [PDF]
G. C. Chan, J. E. Fish, I. A. Mawji, D. D. Leung, A. C. Rachlis, and P. A. Marsden
Epigenetic Basis for the Transcriptional Hyporesponsiveness of the Human Inducible Nitric Oxide Synthase Gene in Vascular Endothelial Cells
J. Immunol., September 15, 2005; 175(6): 3846 - 3861.
[Abstract] [Full Text] [PDF]
S. Steigele and K. Nieselt
Open reading frames provide a rich pool of potential natural antisense transcripts in fungal genomes
Nucleic Acids Res., September 7, 2005; 33(16): 5034 - 5044.
[Abstract] [Full Text] [PDF]
N. Juretic, D. R. Hoen, M. L. Huynh, P. M. Harrison, and T. E. Bureau
The evolutionary fate of MULE-mediated duplications of host gene fragments in rice
Genome Res., September 1, 2005; 15(9): 1292 - 1297.
[Abstract] [Full Text] [PDF]
P. M. Harrison, D. Zheng, Z. Zhang, N. Carriero, and M. Gerstein
Transcribed processed pseudogenes in the human genome: an intermediate form of expressed retrosequence lacking protein-coding ability
Nucleic Acids Res., April 28, 2005; 33(8): 2374 - 2383.
[Abstract] [Full Text] [PDF]
S. A. Korneev, V. Straub, I. Kemenes, E. I. Korneeva, S. R. Ott, P. R. Benjamin, and M. O'Shea
Timed and Targeted Differential Regulation of Nitric Oxide Synthase (NOS) and Anti-NOS Genes by Reward Conditioning Leading to Long-Term Memory Formation
J. Neurosci., February 2, 2005; 25(5): 1188 - 1192.
[Abstract] [Full Text] [PDF]
O. Podlaha and J. Zhang
Nonneutral Evolution of the Transcribed Pseudogene Makorin1-p1 in Mice
Mol. Biol. Evol., December 1, 2004; 21(12): 2202 - 2209.
[Abstract] [Full Text] [PDF]
S. Nisole, C. Lynch, J. P. Stoye, and M. W. Yap
A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1
PNAS, September 7, 2004; 101(36): 13324 - 13328.
[Abstract] [Full Text] [PDF]
G. B. Robb, A. R. Carson, S. C. Tai, J. E. Fish, S. Singh, T. Yamada, S. W. Scherer, K. Nakabayashi, and P. A. Marsden
Post-transcriptional Regulation of Endothelial Nitric-oxide Synthase by an Overlapping Antisense mRNA Transcript
J. Biol. Chem., September 3, 2004; 279(36): 37982 - 37996.
[Abstract] [Full Text] [PDF]
H. BARTSCH, S. VOIGTSBERGER, G. BAUMANN, I. MORANO, and H. P. LUTHER
Detection of a novel sense-antisense RNA-hybrid structure by RACE experiments on endogenous troponin I antisense RNA
RNA, August 1, 2004; 10(8): 1215 - 1224.
[Abstract] [Full Text] [PDF]
M. Vallee, F. Guay, D. Beaudry, J. Matte, R. Blouin, J.-P. Laforest, M. Lessard, and M.-F. Palin
Effects of Breed, Parity, and Folic Acid Supplement on the Expression of Folate Metabolism Genes in Endometrial and Embryonic Tissues from Sows in Early Pregnancy
Biol Reprod, October 1, 2002; 67(4): 1259 - 1267.
[Abstract] [Full Text] [PDF]
D.-H. Hyun, M. Lee, N. Hattori, S.-I. Kubo, Y. Mizuno, B. Halliwell, and P. Jenner
Effect of Wild-type or Mutant Parkin on Oxidative Damage, Nitric Oxide, Antioxidant Defenses, and the Proteasome
J. Biol. Chem., August 2, 2002; 277(32): 28572 - 28577.
[Abstract] [Full Text] [PDF]
S. Korneev and M. O'Shea
Evolution of Nitric Oxide Synthase Regulatory Genes by DNA Inversion
Mol. Biol. Evol., August 1, 2002; 19(8): 1228 - 1233.
[Abstract] [Full Text] [PDF]
S. A. Korneev, I. Kemenes, V. Straub, K. Staras, E. I. Korneeva, G. Kemenes, P. R. Benjamin, and M. O'Shea
Suppression of Nitric Oxide (NO)-Dependent Behavior by Double-Stranded RNA-Mediated Silencing of a Neuronal NO Synthase Gene
J. Neurosci., May 30, 2002; (2002) 20026422.
[Abstract] [Full Text] [PDF]
C. J. H. Elliott and A. J. Susswein
Comparative neuroethology of feeding control in molluscs
J. Exp. Biol., April 1, 2002; 205(7): 877 - 896.
[Abstract] [Full Text] [PDF]
H. G. Trapido-Rosenthal, K. H. Sharp, T. S. Galloway, and C. E. Morrall
Nitric Oxide and Cnidarian-Dinoflagellate Symbioses: Pieces of a Puzzle
Integr. Comp. Biol., April 1, 2001; 41(2): 247 - 257.
[Abstract] [Full Text] [PDF]
P. M. Harrison, N. Echols, and M. B. Gerstein
Digging for dead genes: an analysis of the characteristics of the pseudogene population in the Caenorhabditis elegans genome
Nucleic Acids Res., February 1, 2001; 29(3): 818 - 830.
[Abstract] [Full Text] [PDF]
P. R. Benjamin, K. Staras, and G. Kemenes
A Systems Approach to the Cellular Analysis of Associative Learning in the Pond Snail Lymnaea
Learn. Mem., May 1, 2000; 7(3): 124 - 131.
[Abstract] [Full Text]
|
|
|
|
 |
|