Neurotrophin-Induced Transport of a β-Actin mRNP Complex Increases β-Actin Levels and Stimulates Growth Cone Motility

Zhang, H.L.; Eom, Taesun; Oleynikov, Yuri; Shenoy, Shailesh M.; Liebelt, David A.; Dictenberg, Jason B.; Singer, Robert H.; Bassell, Gary J.

doi:10.1016/s0896-6273(01)00357-9

Cited by 350 publications

(385 citation statements)

References 56 publications

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“…To date, a number of RNA binding and transport proteins have been localized to dendrites, but only one, ZBP1, has been conclusively localized to axons (Zhang et al, 2001). This scarcity of data on candidate proteins for RNA transport to axons presents an obstacle for understanding the role of intra-axonal protein synthesis, because, aside from ZBP1, many of the proteins thought to be involved in RNA localization have not been demonstrated there.…”

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

confidence: 99%

“…To this end, various components of the translational machinery have been identified in the axons of DRG neurons (Koenig, 1991;Pannese and Ledda, 1991;Verma et al, 2005), and translation itself has been shown to occur in these axons (Koenig, 1991;Zheng et al, 2001;Verma et al, 2005;Willis et al, 2005). However, with the exception of zipcode binding protein 1 (ZBP1), which transports β-actin mRNA to growth cones (Zhang et al, 2001), RNA binding and transport molecules have not been shown to be present in axons, and none, to our knowledge, have been localized to the axons of DRG afferents.In this study, we tested the hypothesis that two of the best characterized RNA binding and transport proteins, staufen (stau) and fragile X mental retardation protein (FMRP), localize to extra-somal sites in sensory neurons, consistent with a role in RNA transport. Here, we provide evidence that DRG and TG neurons express a number of RNA binding and transport proteins.…”

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confidence: 99%

“…On the other hand, a recent study indicates that FMRP is found in the axons of hippocampal neurons (Antar et al, 2006). Thus, it remains to be seen if the axonal localization of stau2 and FMRP occurs on a more general basis or if this is largely limited to sensory axons and exceptional cases in the CNS.To date, a number of RNA binding and transport proteins have been localized to dendrites, but only one, ZBP1, has been conclusively localized to axons (Zhang et al, 2001). This scarcity of data on candidate proteins for RNA transport to axons presents an obstacle for understanding the role of intra-axonal protein synthesis, because, aside from ZBP1, many of the proteins thought to be involved in RNA localization have not been demonstrated there.…”

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

confidence: 99%

mentioning

confidence: 99%

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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

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“…This localization can be induced by NT-3 signaling, or by cAMP elevation and subsequent PKA activation (Zhang et al 1999). This axonal distribution can be inhibited with antisense oligonucleotides that disrupt the binding of the actin mRNA to Zipcode Binding Protein (ZBP-1), which also blocked the NT-3-induced protein localization at the growth cone and decreased growth cone motility (Zhang et al 2001). Therefore trophic stimulation of axon growth may involve the stimulation of localized mRNA transport and protein synthesis as a mechanism of quickly localizing needed proteins.…”

Section: How Do Extracellular Signals Induce Axon Elongation?mentioning

confidence: 99%

How does an axon grow?

Goldberg¹

2003

Genes Dev.

203

138

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How do axons grow during development, and why do they fail to regrow when injured? In the complicated mesh of our nervous system, the axon is the information superhighway, carrying all of the data we use to sense our environment and carry out behaviors. To wire up our nervous system properly, neurons must elongate their axons during development to reach their targets. This is no simple task, however. The complex morphology of axons and dendrites puts neurons among the most intricate and beautiful cells in the body. Knowledge of how neurons extend axons and dendrites, elongate at a particular rate, and stop growing at the proper time is critical to understanding the development of our nervous system, yet the regulation of these processes is poorly understood. Considerable attention in recent years has focused on understanding how growth cones are guided and steered through complicated pathways (for review, see Schmidt and Hall 1998;Mueller 1999), and even how neurons initiate new processes (for review, see Da Silva and Dotti 2002), but what mechanisms are involved in elongation itself? Are environmental signals needed to drive axon growth and, if so, what are the intracellular molecular mechanisms by which they induce elongation? What controls the rate of axon growth? How do CNS neurons know whether to extend axons or dendrites? Is the signaling of axon versus dendrite growth attributable to different extracellular signals, different neuronal states, or both? All of these questions bear critically on our understanding of axon growth and here I review recent answers and approaches to the above questions, and highlight their relevance during development, injury, and disease.

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“…De manière surprenante, ZPB1 se lie à la fois aux microfilaments et aux microtubules, et est capable de former des granules qui montrent des mouvements motorisés sur les deux types de structures [31]. ZBP1 peut ainsi utiliser les deux types de supports pour transporter l'ARNm de l'actine β, avec cependant des préférences cellulaires : les microfilaments dans les fibroblastes [31], et les microtubules dans les neurones [32]. Le bloquage de la localisation de l'ARNm de l'actine β à l'aide d'oligonucléotides antisens du zipcode entraîne la délocalisation de ZBP1, ce qui suggère que l'interaction ARN-protéine est essentielle au transport du complexe ribonucléoprotéique.…”

Section: Fondements Moléculaires Du Transport Des Arnm De L'actine βunclassified

Polarité cellulaire et localisation intracellulaire des ARNm de l’actine

Lavoie

Basyuk²,

Bordonne³

et al. 2004

Med Sci (Paris)

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Neurotrophin-Induced Transport of a β-Actin mRNP Complex Increases β-Actin Levels and Stimulates Growth Cone Motility

Cited by 350 publications

References 56 publications

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

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

How does an axon grow?

Polarité cellulaire et localisation intracellulaire des ARNm de l’actine

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