Two mRNA-Binding Proteins Regulate the Distribution of Syntaxin mRNA in<i>Aplysia</i>Sensory Neurons

Hu, Jiang-Yuan; Wu, Fang; Schwartz, James H.; Schacher, Samuel

doi:10.1523/jneurosci.4917-05.2006

Cited by 26 publications

(25 citation statements)

References 69 publications

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“…For example, in both the mammalian nervous system and the developing Drosophila embryo, the dsRBP Staufen binds to the 39 UTR of certain mRNAs to promote their localization (Roegiers and Jan 2000). Of particular relevance to our studies, in the sensory neurons of Aplysia, Staufen is involved in localizing syntaxin mRNA via its 39 UTR (Liu et al 2006).…”

Section: Do Inosine-containing Mrnas Have Different Fates?mentioning

confidence: 88%

C. elegans and H. sapiens mRNAs with edited 3′ UTRs are present on polysomes

Hundley¹,

Krauchuk²,

Bass³

2008

RNA

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Adenosine deaminases that act on RNA (ADARs) are editing enzymes that convert adenosine to inosine in double-stranded RNA (dsRNA). ADARs sometimes target codons so that a single mRNA yields multiple protein isoforms. However, ADARs most often target noncoding regions of mRNAs, such as untranslated regions (UTRs). To understand the function of extensive doublestranded 39 UTR structures, and the inosines within them, we monitored the fate of reporter and endogenous mRNAs that include structured 39 UTRs in wild-type Caenorhabditis elegans and in strains with mutations in the ADAR genes. In general, we saw little effect of editing on stability or translatability of mRNA, although in one case an ADR-1 dependent effect was observed. Importantly, whereas previous studies indicate that inosine-containing RNAs are retained in the nucleus, we show that both C. elegans and Homo sapiens mRNAs with edited, structured 39 UTRs are present on translating ribosomes.

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Section: Do Inosine-containing Mrnas Have Different Fates?mentioning

confidence: 88%

C. elegans and H. sapiens mRNAs with edited 3′ UTRs are present on polysomes

Hundley¹,

Krauchuk²,

Bass³

2008

RNA

View full text Add to dashboard Cite

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“…To localize stau2 and FMRP to DRG axons by IHC we focused on nociceptive, TRPV1-positive axons because they are readily labeled with an anti-TRPV1 antibody and their functional role (Liu et al, 2006). Rat DRG neurons also express CPEB (Price and Cervero, unpublished observations), hence, it is tempting to speculate that trafficking of stau or FMRP might be altered in pathophysiologies that lead to nociceptive plasticity, especially in the direction of the central projection.…”

Section: Stau2 and Fmrp Proteins Localize To Drg Axons: Implications mentioning

confidence: 99%

“…These findings suggest that both stau2 and FMRP are differentially trafficked into the peripheral or central branches of nociceptors such that the peripheral direction is preferred in the normal animal. In aplysia sensory neurons stau and cytoplasmic polyadenylation element binding protein (CPEB) cooperate to modify the distribution of syntaxin mRNA to different regions of sensory neurons upon 5-HT stimulation (Liu et al, 2006). Rat DRG neurons also express CPEB (Price and Cervero, unpublished observations), hence, it is tempting to speculate that trafficking of stau or FMRP might be altered in pathophysiologies that lead to nociceptive plasticity, especially in the direction of the central projection.…”

Section: Stau2 and Fmrp Proteins Localize To Drg Axons: Implications mentioning

confidence: 99%

“…To the extent that FMRP mRNA and protein were found in the dorsal roots, we cannot exclude the possibility that its source is intrinsic (i.e. extraneuronal); however, the finding that FMRP immunoreactivity localizes to peripherally and centrally projecting sensory axons by IHC suggests that at least a portion of this protein band represents axonal FMRP.To localize stau2 and FMRP to DRG axons by IHC we focused on nociceptive, TRPV1-positive axons because they are readily labeled with an anti-TRPV1 antibody and their functional role (Liu et al, 2006). Rat DRG neurons also express CPEB (Price and Cervero, unpublished observations), hence, it is tempting to speculate that trafficking of stau or FMRP might be altered in pathophysiologies that lead to nociceptive plasticity, especially in the direction of the central projection.…”

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confidence: 99%

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The RNA binding and transport proteins staufen and fragile X mental retardation protein are expressed by rat primary afferent neurons and localize to peripheral and central axons

et al. 2006

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Neuronal proteins have been traditionally viewed as being derived solely from the soma; however, accumulating evidence indicates that dendritic and axonal sites are capable of a more autonomous role in terms of new protein synthesis. Such extra-somal translation allows for more rapid, on-demand regulation of neuronal structure and function than would otherwise be possible. While mechanisms of dendritic RNA transport have been elucidated, it remains unclear how RNA is trafficked into the axon for this purpose. Primary afferent neurons of the dorsal root (DRG) and trigeminal (TG) ganglia have among the longest axons in the neuraxis and such axonal protein synthesis would be advantageous, given the greater time involved for protein trafficking to occur via axonal transport. Therefore, we hypothesized that these primary sensory neurons might express proteins involved in RNA transport. Rat DRG and TG neurons expressed staufen (stau) 1 and 2 (detected at the mRNA level) and stau2 and fragile × mental retardation protein (FMRP; detected at the protein level). Stau2 mRNA was also detected in human TG neurons. Stau2 and FMRP protein were localized to the sciatic nerve and dorsal roots by immunohistochemistry and to dorsal roots by Western blot. Stau2 and FMRP immunoreactivities colocalized with transient receptor potential channel type 1 immunoreactivity in sensory axons of the sciatic nerve and dorsal root, suggesting that these proteins are being transported into the peripheral and central terminals of nociceptive sensory axons. Based on these findings, we propose that stau2 and FMRP proteins are attractive candidates to subserve RNA transport in sensory neurons, linking somal transcriptional events to axonal translation. Keywordsprimary afferent neuron; fragile X mental retardation protein; staufen; RNA binding protein; axonal translation; RNA cargoThe discovery that RNA is transported to synaptic sites by RNA transport proteins, where it can be translated on demand, has provided insight into how neurons handle the rapid synaptic architectural and signaling changes that are known to occur in brain areas associated with learning and memory (Job and Eberwine, 2001;Steward and Worley, 2002;Steward and Schuman, 2003;Martin, 2004;Tiedge, 2005). There is now compelling evidence that translation occurs in axons (Koenig, 1967;Nixon, 1980;Koenig, 1991;Eng et al., 1999;Brittis et al., 2002;Piper and Holt, 2004), as mRNA and translational machinery have been localized to CNS (Tiedge et al., 1993;Aronov et al., 2001;Brittis et al., 2002), sympathetic (Olink-Coux andHollenbeck, 1996;Eng et al., 1999) and sensory (Zheng et al., 2001;Li et al., 2004a;Verma et al., 2005;Willis et al., 2005) axons. Moreover, an emerging physiological role for local translation in axons has been described for growth cone guidance and collapse (Zheng et al., 2001;Li et al., 2004a;Verma et al., 2005;Wu et al., 2005).Primary sensory neurons of the dorsal root ganglion (DRG) and trigeminal ganglion (TG) have among the longest axons of the entire ne...

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“…RNA-binding proteins transport coding and non-coding RNAs to their cellular destinations (Liu et al, 2006;Cao et al, 2006), regulate mRNA stability (Goldstrohm et al, 2006), and control translation in response to environmental cues (Antar et al, 2004). It is also known that most RNA-binding proteins are components of multi-protein complexes which include other RNA-binding proteins and a plethora of RNA targets.…”

Section: Introductionmentioning

confidence: 99%