Neurotrophin-induced transport of a β-actin mRNP complex increases β-actin levels and stimulates growth cone motility

H. L. Zhang; T. Eom; Y. Oleynikov; S. M. Shenoy; D. A. Liebelt; J. B. Dictenberg; R. H. Singer; G. J. Bassell

doi:10.1016/S0896-6273(01)00357-9

Neurotrophin-induced transport of a β-actin mRNP complex increases β-actin levels and stimulates growth cone motility

H. L. Zhang, T. Eom, Y. Oleynikov, S. M. Shenoy, D. A. Liebelt, J. B. Dictenberg, R. H. Singer, G. J. Bassell

Cell Biology

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322 Scopus citations

Abstract

Neurotrophin regulation of actin-dependent changes in growth cone motility may depend on the signaling of β-actin mRNA transport. Formation of an RNP complex between the β-actin mRNA zipcode sequence and Zipcode Binding Protein 1 (ZBP1) was required for its localization to growth cones. Antisense oligonucleotides to the zipcode inhibited formation of this RNP complex in vitro and the neurotrophin-induced localization of β-actin mRNA and ZBP1 granules. Live cell imaging of neurons transfected with EGFP-ZBP1 revealed fast, bidirectional movements of granules in neurites that were inhibited by antisense treatment, as visualized by FRAP analysis. NT-3 stimulation of β-actin protein localization was dependent on the 3′UTR and inhibited by antisense treatment. Growth cones exhibited impaired motility in the presense of antisense. These results suggest a novel mechanism to influence growth cone dynamics involving the regulated transport of mRNA.

Original language	English (US)
Pages (from-to)	261-275
Number of pages	15
Journal	Neuron
Volume	31
Issue number	2
DOIs	https://doi.org/10.1016/S0896-6273(01)00357-9
State	Published - Aug 2 2001

ASJC Scopus subject areas

General Neuroscience

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10.1016/S0896-6273(01)00357-9

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title = "Neurotrophin-induced transport of a β-actin mRNP complex increases β-actin levels and stimulates growth cone motility",

abstract = "Neurotrophin regulation of actin-dependent changes in growth cone motility may depend on the signaling of β-actin mRNA transport. Formation of an RNP complex between the β-actin mRNA zipcode sequence and Zipcode Binding Protein 1 (ZBP1) was required for its localization to growth cones. Antisense oligonucleotides to the zipcode inhibited formation of this RNP complex in vitro and the neurotrophin-induced localization of β-actin mRNA and ZBP1 granules. Live cell imaging of neurons transfected with EGFP-ZBP1 revealed fast, bidirectional movements of granules in neurites that were inhibited by antisense treatment, as visualized by FRAP analysis. NT-3 stimulation of β-actin protein localization was dependent on the 3′UTR and inhibited by antisense treatment. Growth cones exhibited impaired motility in the presense of antisense. These results suggest a novel mechanism to influence growth cone dynamics involving the regulated transport of mRNA.",

author = "Zhang, {H. L.} and T. Eom and Y. Oleynikov and Shenoy, {S. M.} and Liebelt, {D. A.} and Dictenberg, {J. B.} and Singer, {R. H.} and Bassell, {G. J.}",

note = "Funding Information: We thank Suzanne Zukin for helpful discussions and suggestions on this manuscript. We thank Kim Farina, Nancy Standart, and Eng Tan for providing antibodies to ZBP, VgRBP, and HCC. We thank Adam Hartley for assistance with figure preparation and Jeff Levsky for assistance with computer programming. This work was supported by the National Science Foundation grant IBN9811384 and National Institutes of Health (NIH) RO1 grants GM55599 and NS39641 to G.J.B. and AR41480 to R.H.S. This work was also supported by the Muscular Dystrophy Foundation awards to H.L.Z. and G.J.B. H.L.Z. was supported by NIH training grant (T32 NS07439). J.B.D. was supported by NIH training grant (CA09475-13) and is the recipient of the Albert Einstein Scholar Award.",

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doi = "10.1016/S0896-6273(01)00357-9",

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T1 - Neurotrophin-induced transport of a β-actin mRNP complex increases β-actin levels and stimulates growth cone motility

AU - Zhang, H. L.

AU - Eom, T.

AU - Oleynikov, Y.

AU - Shenoy, S. M.

AU - Liebelt, D. A.

AU - Dictenberg, J. B.

AU - Singer, R. H.

AU - Bassell, G. J.

N1 - Funding Information: We thank Suzanne Zukin for helpful discussions and suggestions on this manuscript. We thank Kim Farina, Nancy Standart, and Eng Tan for providing antibodies to ZBP, VgRBP, and HCC. We thank Adam Hartley for assistance with figure preparation and Jeff Levsky for assistance with computer programming. This work was supported by the National Science Foundation grant IBN9811384 and National Institutes of Health (NIH) RO1 grants GM55599 and NS39641 to G.J.B. and AR41480 to R.H.S. This work was also supported by the Muscular Dystrophy Foundation awards to H.L.Z. and G.J.B. H.L.Z. was supported by NIH training grant (T32 NS07439). J.B.D. was supported by NIH training grant (CA09475-13) and is the recipient of the Albert Einstein Scholar Award.

PY - 2001/8/2

Y1 - 2001/8/2

N2 - Neurotrophin regulation of actin-dependent changes in growth cone motility may depend on the signaling of β-actin mRNA transport. Formation of an RNP complex between the β-actin mRNA zipcode sequence and Zipcode Binding Protein 1 (ZBP1) was required for its localization to growth cones. Antisense oligonucleotides to the zipcode inhibited formation of this RNP complex in vitro and the neurotrophin-induced localization of β-actin mRNA and ZBP1 granules. Live cell imaging of neurons transfected with EGFP-ZBP1 revealed fast, bidirectional movements of granules in neurites that were inhibited by antisense treatment, as visualized by FRAP analysis. NT-3 stimulation of β-actin protein localization was dependent on the 3′UTR and inhibited by antisense treatment. Growth cones exhibited impaired motility in the presense of antisense. These results suggest a novel mechanism to influence growth cone dynamics involving the regulated transport of mRNA.

AB - Neurotrophin regulation of actin-dependent changes in growth cone motility may depend on the signaling of β-actin mRNA transport. Formation of an RNP complex between the β-actin mRNA zipcode sequence and Zipcode Binding Protein 1 (ZBP1) was required for its localization to growth cones. Antisense oligonucleotides to the zipcode inhibited formation of this RNP complex in vitro and the neurotrophin-induced localization of β-actin mRNA and ZBP1 granules. Live cell imaging of neurons transfected with EGFP-ZBP1 revealed fast, bidirectional movements of granules in neurites that were inhibited by antisense treatment, as visualized by FRAP analysis. NT-3 stimulation of β-actin protein localization was dependent on the 3′UTR and inhibited by antisense treatment. Growth cones exhibited impaired motility in the presense of antisense. These results suggest a novel mechanism to influence growth cone dynamics involving the regulated transport of mRNA.

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Neurotrophin-induced transport of a β-actin mRNP complex increases β-actin levels and stimulates growth cone motility

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