Modulation of synaptic transmission by the BCL-2 family protein BCL-xL

Elizabeth A. Jonas, Daniel Hoit, John A. Hickman, Teresa A. Brandt, Brian M. Polster, Yihru Fannjiang, Erin McCarthy, Marlena K. Montanez, J Marie Hardwick, Leonard K. Kaczmarek

Research output: Contribution to journalArticle

Abstract

BCL-2 family proteins are known to regulate cell death during development by influencing the permeability of mitochondrial membranes. The anti-apoptotic BCL-2 family protein BCL-xL is highly expressed in the adult brain and localizes to mitochondria in the presynaptic terminal of the adult squid stellate ganglion. Application of recombinant BCL-xL through a patch pipette to mitochondria inside the giant presynaptic terminal triggered multiconductance channel activity in mitochondrial membranes. Furthermore, injection of full-length BCL-xL protein into the presynaptic terminal enhanced postsynaptic responses and enhanced the rate of recovery from synaptic depression, whereas a recombinant pro-apoptotic cleavage product of BCL-xL attenuated postsynaptic responses. The effect of BCL-xL on synaptic responses persisted in the presence of a blocker of mitochondrial calcium uptake and was mimicked by injection of ATP into the terminal. These studies indicate that the permeability of outer mitochondrial membranes influences synaptic transmission, and they raise the possibility that modulation of mitochondrial conductance by BCL-2 family proteins affects synaptic stability.

Original languageEnglish (US)
Pages (from-to)8423-8431
Number of pages9
JournalJournal of Neuroscience
Volume23
Issue number23
StatePublished - Sep 10 2003

Fingerprint

Synaptic Transmission
Presynaptic Terminals
Mitochondrial Membranes
Permeability
Mitochondria
Proteins
Stellate Ganglion
Decapodiformes
Injections
Cell Death
Adenosine Triphosphate
Calcium
Brain

Keywords

  • ATP
  • BCL-2
  • BCL-xL
  • Mitochondria
  • Neurotransmitter release
  • Squid

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Jonas, E. A., Hoit, D., Hickman, J. A., Brandt, T. A., Polster, B. M., Fannjiang, Y., ... Kaczmarek, L. K. (2003). Modulation of synaptic transmission by the BCL-2 family protein BCL-xL. Journal of Neuroscience, 23(23), 8423-8431.

Modulation of synaptic transmission by the BCL-2 family protein BCL-xL. / Jonas, Elizabeth A.; Hoit, Daniel; Hickman, John A.; Brandt, Teresa A.; Polster, Brian M.; Fannjiang, Yihru; McCarthy, Erin; Montanez, Marlena K.; Hardwick, J Marie; Kaczmarek, Leonard K.

In: Journal of Neuroscience, Vol. 23, No. 23, 10.09.2003, p. 8423-8431.

Research output: Contribution to journalArticle

Jonas, EA, Hoit, D, Hickman, JA, Brandt, TA, Polster, BM, Fannjiang, Y, McCarthy, E, Montanez, MK, Hardwick, JM & Kaczmarek, LK 2003, 'Modulation of synaptic transmission by the BCL-2 family protein BCL-xL', Journal of Neuroscience, vol. 23, no. 23, pp. 8423-8431.
Jonas EA, Hoit D, Hickman JA, Brandt TA, Polster BM, Fannjiang Y et al. Modulation of synaptic transmission by the BCL-2 family protein BCL-xL. Journal of Neuroscience. 2003 Sep 10;23(23):8423-8431.
Jonas, Elizabeth A. ; Hoit, Daniel ; Hickman, John A. ; Brandt, Teresa A. ; Polster, Brian M. ; Fannjiang, Yihru ; McCarthy, Erin ; Montanez, Marlena K. ; Hardwick, J Marie ; Kaczmarek, Leonard K. / Modulation of synaptic transmission by the BCL-2 family protein BCL-xL. In: Journal of Neuroscience. 2003 ; Vol. 23, No. 23. pp. 8423-8431.
@article{84638559c30e403cb66c70b9aa1760be,
title = "Modulation of synaptic transmission by the BCL-2 family protein BCL-xL",
abstract = "BCL-2 family proteins are known to regulate cell death during development by influencing the permeability of mitochondrial membranes. The anti-apoptotic BCL-2 family protein BCL-xL is highly expressed in the adult brain and localizes to mitochondria in the presynaptic terminal of the adult squid stellate ganglion. Application of recombinant BCL-xL through a patch pipette to mitochondria inside the giant presynaptic terminal triggered multiconductance channel activity in mitochondrial membranes. Furthermore, injection of full-length BCL-xL protein into the presynaptic terminal enhanced postsynaptic responses and enhanced the rate of recovery from synaptic depression, whereas a recombinant pro-apoptotic cleavage product of BCL-xL attenuated postsynaptic responses. The effect of BCL-xL on synaptic responses persisted in the presence of a blocker of mitochondrial calcium uptake and was mimicked by injection of ATP into the terminal. These studies indicate that the permeability of outer mitochondrial membranes influences synaptic transmission, and they raise the possibility that modulation of mitochondrial conductance by BCL-2 family proteins affects synaptic stability.",
keywords = "ATP, BCL-2, BCL-xL, Mitochondria, Neurotransmitter release, Squid",
author = "Jonas, {Elizabeth A.} and Daniel Hoit and Hickman, {John A.} and Brandt, {Teresa A.} and Polster, {Brian M.} and Yihru Fannjiang and Erin McCarthy and Montanez, {Marlena K.} and Hardwick, {J Marie} and Kaczmarek, {Leonard K.}",
year = "2003",
month = "9",
day = "10",
language = "English (US)",
volume = "23",
pages = "8423--8431",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "23",

}

TY - JOUR

T1 - Modulation of synaptic transmission by the BCL-2 family protein BCL-xL

AU - Jonas, Elizabeth A.

AU - Hoit, Daniel

AU - Hickman, John A.

AU - Brandt, Teresa A.

AU - Polster, Brian M.

AU - Fannjiang, Yihru

AU - McCarthy, Erin

AU - Montanez, Marlena K.

AU - Hardwick, J Marie

AU - Kaczmarek, Leonard K.

PY - 2003/9/10

Y1 - 2003/9/10

N2 - BCL-2 family proteins are known to regulate cell death during development by influencing the permeability of mitochondrial membranes. The anti-apoptotic BCL-2 family protein BCL-xL is highly expressed in the adult brain and localizes to mitochondria in the presynaptic terminal of the adult squid stellate ganglion. Application of recombinant BCL-xL through a patch pipette to mitochondria inside the giant presynaptic terminal triggered multiconductance channel activity in mitochondrial membranes. Furthermore, injection of full-length BCL-xL protein into the presynaptic terminal enhanced postsynaptic responses and enhanced the rate of recovery from synaptic depression, whereas a recombinant pro-apoptotic cleavage product of BCL-xL attenuated postsynaptic responses. The effect of BCL-xL on synaptic responses persisted in the presence of a blocker of mitochondrial calcium uptake and was mimicked by injection of ATP into the terminal. These studies indicate that the permeability of outer mitochondrial membranes influences synaptic transmission, and they raise the possibility that modulation of mitochondrial conductance by BCL-2 family proteins affects synaptic stability.

AB - BCL-2 family proteins are known to regulate cell death during development by influencing the permeability of mitochondrial membranes. The anti-apoptotic BCL-2 family protein BCL-xL is highly expressed in the adult brain and localizes to mitochondria in the presynaptic terminal of the adult squid stellate ganglion. Application of recombinant BCL-xL through a patch pipette to mitochondria inside the giant presynaptic terminal triggered multiconductance channel activity in mitochondrial membranes. Furthermore, injection of full-length BCL-xL protein into the presynaptic terminal enhanced postsynaptic responses and enhanced the rate of recovery from synaptic depression, whereas a recombinant pro-apoptotic cleavage product of BCL-xL attenuated postsynaptic responses. The effect of BCL-xL on synaptic responses persisted in the presence of a blocker of mitochondrial calcium uptake and was mimicked by injection of ATP into the terminal. These studies indicate that the permeability of outer mitochondrial membranes influences synaptic transmission, and they raise the possibility that modulation of mitochondrial conductance by BCL-2 family proteins affects synaptic stability.

KW - ATP

KW - BCL-2

KW - BCL-xL

KW - Mitochondria

KW - Neurotransmitter release

KW - Squid

UR - http://www.scopus.com/inward/record.url?scp=0141856430&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0141856430&partnerID=8YFLogxK

M3 - Article

VL - 23

SP - 8423

EP - 8431

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 23

ER -