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SIPA1L2 controls trafficking and local signaling of TrkB-containing amphisomes at presynaptic terminals

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SIPA1L2 controls trafficking and local signaling of TrkB-containing amphisomes at presynaptic terminals. / Andres-Alonso, Maria; Ammar, Mohamed Raafet; Butnaru, Ioana; Gomes, Guilherme M; Acuña Sanhueza, Gustavo; Raman, Rajeev; Yuanxiang, PingAn; Borgmeyer, Maximilian; Lopez-Rojas, Jeffrey; Raza, Syed Ahsan; Brice, Nicola; Hausrat, Torben J; Macharadze, Tamar; Diaz-Gonzalez, Silvia; Carlton, Mark; Failla, Antonio Virgilio; Stork, Oliver; Schweizer, Michaela; Gundelfinger, Eckart D; Kneussel, Matthias; Spilker, Christina; Karpova, Anna; Kreutz, Michael R.

In: NAT COMMUN, Vol. 10, No. 1, 29.11.2019, p. 5448.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Andres-Alonso, M, Ammar, MR, Butnaru, I, Gomes, GM, Acuña Sanhueza, G, Raman, R, Yuanxiang, P, Borgmeyer, M, Lopez-Rojas, J, Raza, SA, Brice, N, Hausrat, TJ, Macharadze, T, Diaz-Gonzalez, S, Carlton, M, Failla, AV, Stork, O, Schweizer, M, Gundelfinger, ED, Kneussel, M, Spilker, C, Karpova, A & Kreutz, MR 2019, 'SIPA1L2 controls trafficking and local signaling of TrkB-containing amphisomes at presynaptic terminals', NAT COMMUN, vol. 10, no. 1, pp. 5448. https://doi.org/10.1038/s41467-019-13224-z

APA

Andres-Alonso, M., Ammar, M. R., Butnaru, I., Gomes, G. M., Acuña Sanhueza, G., Raman, R., Yuanxiang, P., Borgmeyer, M., Lopez-Rojas, J., Raza, S. A., Brice, N., Hausrat, T. J., Macharadze, T., Diaz-Gonzalez, S., Carlton, M., Failla, A. V., Stork, O., Schweizer, M., Gundelfinger, E. D., ... Kreutz, M. R. (2019). SIPA1L2 controls trafficking and local signaling of TrkB-containing amphisomes at presynaptic terminals. NAT COMMUN, 10(1), 5448. https://doi.org/10.1038/s41467-019-13224-z

Vancouver

Andres-Alonso M, Ammar MR, Butnaru I, Gomes GM, Acuña Sanhueza G, Raman R et al. SIPA1L2 controls trafficking and local signaling of TrkB-containing amphisomes at presynaptic terminals. NAT COMMUN. 2019 Nov 29;10(1):5448. https://doi.org/10.1038/s41467-019-13224-z

Bibtex

@article{a35f43171fc44b03bc943d339ed9447d,
title = "SIPA1L2 controls trafficking and local signaling of TrkB-containing amphisomes at presynaptic terminals",
abstract = "Amphisomes are organelles of the autophagy pathway that result from the fusion of autophagosomes with late endosomes. While biogenesis of autophagosomes and late endosomes occurs continuously at axon terminals, non-degradative roles of autophagy at boutons are barely described. Here, we show that in neurons BDNF/TrkB traffick in amphisomes that signal locally at presynaptic boutons during retrograde transport to the soma. This is orchestrated by the Rap GTPase-activating (RapGAP) protein SIPA1L2, which connects TrkB amphisomes to a dynein motor. The autophagosomal protein LC3 regulates RapGAP activity of SIPA1L2 and controls retrograde trafficking and local signaling of TrkB. Following induction of presynaptic plasticity, amphisomes dissociate from dynein at boutons enabling local signaling and promoting transmitter release. Accordingly, sipa1l2 knockout mice show impaired BDNF-dependent presynaptic plasticity. Taken together, the data suggest that in hippocampal neurons, TrkB-signaling endosomes are in fact amphisomes that during retrograde transport have local signaling capacity in the context of presynaptic plasticity.",
author = "Maria Andres-Alonso and Ammar, {Mohamed Raafet} and Ioana Butnaru and Gomes, {Guilherme M} and {Acu{\~n}a Sanhueza}, Gustavo and Rajeev Raman and PingAn Yuanxiang and Maximilian Borgmeyer and Jeffrey Lopez-Rojas and Raza, {Syed Ahsan} and Nicola Brice and Hausrat, {Torben J} and Tamar Macharadze and Silvia Diaz-Gonzalez and Mark Carlton and Failla, {Antonio Virgilio} and Oliver Stork and Michaela Schweizer and Gundelfinger, {Eckart D} and Matthias Kneussel and Christina Spilker and Anna Karpova and Kreutz, {Michael R}",
year = "2019",
month = nov,
day = "29",
doi = "10.1038/s41467-019-13224-z",
language = "English",
volume = "10",
pages = "5448",
journal = "NAT COMMUN",
issn = "2041-1723",
publisher = "NATURE PUBLISHING GROUP",
number = "1",

}

RIS

TY - JOUR

T1 - SIPA1L2 controls trafficking and local signaling of TrkB-containing amphisomes at presynaptic terminals

AU - Andres-Alonso, Maria

AU - Ammar, Mohamed Raafet

AU - Butnaru, Ioana

AU - Gomes, Guilherme M

AU - Acuña Sanhueza, Gustavo

AU - Raman, Rajeev

AU - Yuanxiang, PingAn

AU - Borgmeyer, Maximilian

AU - Lopez-Rojas, Jeffrey

AU - Raza, Syed Ahsan

AU - Brice, Nicola

AU - Hausrat, Torben J

AU - Macharadze, Tamar

AU - Diaz-Gonzalez, Silvia

AU - Carlton, Mark

AU - Failla, Antonio Virgilio

AU - Stork, Oliver

AU - Schweizer, Michaela

AU - Gundelfinger, Eckart D

AU - Kneussel, Matthias

AU - Spilker, Christina

AU - Karpova, Anna

AU - Kreutz, Michael R

PY - 2019/11/29

Y1 - 2019/11/29

N2 - Amphisomes are organelles of the autophagy pathway that result from the fusion of autophagosomes with late endosomes. While biogenesis of autophagosomes and late endosomes occurs continuously at axon terminals, non-degradative roles of autophagy at boutons are barely described. Here, we show that in neurons BDNF/TrkB traffick in amphisomes that signal locally at presynaptic boutons during retrograde transport to the soma. This is orchestrated by the Rap GTPase-activating (RapGAP) protein SIPA1L2, which connects TrkB amphisomes to a dynein motor. The autophagosomal protein LC3 regulates RapGAP activity of SIPA1L2 and controls retrograde trafficking and local signaling of TrkB. Following induction of presynaptic plasticity, amphisomes dissociate from dynein at boutons enabling local signaling and promoting transmitter release. Accordingly, sipa1l2 knockout mice show impaired BDNF-dependent presynaptic plasticity. Taken together, the data suggest that in hippocampal neurons, TrkB-signaling endosomes are in fact amphisomes that during retrograde transport have local signaling capacity in the context of presynaptic plasticity.

AB - Amphisomes are organelles of the autophagy pathway that result from the fusion of autophagosomes with late endosomes. While biogenesis of autophagosomes and late endosomes occurs continuously at axon terminals, non-degradative roles of autophagy at boutons are barely described. Here, we show that in neurons BDNF/TrkB traffick in amphisomes that signal locally at presynaptic boutons during retrograde transport to the soma. This is orchestrated by the Rap GTPase-activating (RapGAP) protein SIPA1L2, which connects TrkB amphisomes to a dynein motor. The autophagosomal protein LC3 regulates RapGAP activity of SIPA1L2 and controls retrograde trafficking and local signaling of TrkB. Following induction of presynaptic plasticity, amphisomes dissociate from dynein at boutons enabling local signaling and promoting transmitter release. Accordingly, sipa1l2 knockout mice show impaired BDNF-dependent presynaptic plasticity. Taken together, the data suggest that in hippocampal neurons, TrkB-signaling endosomes are in fact amphisomes that during retrograde transport have local signaling capacity in the context of presynaptic plasticity.

U2 - 10.1038/s41467-019-13224-z

DO - 10.1038/s41467-019-13224-z

M3 - SCORING: Journal article

C2 - 31784514

VL - 10

SP - 5448

JO - NAT COMMUN

JF - NAT COMMUN

SN - 2041-1723

IS - 1

ER -