Mechanism of Axonal Contractility in Embryonic Drosophila Motor Neurons In Vivo

Alireza Tofangchi, Anthony Fan, M Taher A Saif

Research output: Contribution to journalArticle

Abstract

Several in vitro and limited in vivo experiments have shown that neurons maintain a rest tension along their axons intrinsically. They grow in response to stretch but contract in response to loss of tension. This contraction eventually leads to the restoration of the rest tension in axons. However, the mechanism by which axons maintain tension in vivo remains elusive. The objective of this work is to elucidate the key cytoskeletal components responsible for generating tension in axons. Toward this goal, in vivo experiments were conducted on single axons of embryonic Drosophila motor neurons in the presence of various drugs. Each axon was slackened mechanically by bringing the neuromuscular junction toward the central nervous system multiple times. In the absence of any drug, axons shortened and restored the straight configuration within 2–4 min of slackening. The total shortening was ∼40% of the original length. The recovery rate in each cycle, but not the recovery magnitude, was dependent on the axon's prior contraction history. For example, the contraction time of a previously slackened axon may be twice its first-time contraction. This recovery was significantly hampered with the depletion of ATP, inhibition of myosin motors, and disruption of actin filaments. The disruption of microtubules did not affect the recovery magnitude, but, on the contrary, led to an enhanced recovery rate compared to control cases. These results suggest that the actomyosin machinery is the major active element in axonal contraction, whereas microtubules contribute as resistive/dissipative elements.

Original languageEnglish (US)
Pages (from-to)1519-1527
Number of pages9
JournalBiophysical journal
Volume111
Issue number7
DOIs
StatePublished - Oct 4 2016

Fingerprint

Motor Neurons
Drosophila
Axons
Microtubules
Actomyosin
Neuromuscular Junction
Myosins
Contracts
Actin Cytoskeleton
Pharmaceutical Preparations
Central Nervous System
Adenosine Triphosphate
History
Neurons

ASJC Scopus subject areas

  • Biophysics

Cite this

Mechanism of Axonal Contractility in Embryonic Drosophila Motor Neurons In Vivo. / Tofangchi, Alireza; Fan, Anthony; Saif, M Taher A.

In: Biophysical journal, Vol. 111, No. 7, 04.10.2016, p. 1519-1527.

Research output: Contribution to journalArticle

Tofangchi, Alireza ; Fan, Anthony ; Saif, M Taher A. / Mechanism of Axonal Contractility in Embryonic Drosophila Motor Neurons In Vivo. In: Biophysical journal. 2016 ; Vol. 111, No. 7. pp. 1519-1527.
@article{d10851eac66a4d7392a88eb15eb22988,
title = "Mechanism of Axonal Contractility in Embryonic Drosophila Motor Neurons In Vivo",
abstract = "Several in vitro and limited in vivo experiments have shown that neurons maintain a rest tension along their axons intrinsically. They grow in response to stretch but contract in response to loss of tension. This contraction eventually leads to the restoration of the rest tension in axons. However, the mechanism by which axons maintain tension in vivo remains elusive. The objective of this work is to elucidate the key cytoskeletal components responsible for generating tension in axons. Toward this goal, in vivo experiments were conducted on single axons of embryonic Drosophila motor neurons in the presence of various drugs. Each axon was slackened mechanically by bringing the neuromuscular junction toward the central nervous system multiple times. In the absence of any drug, axons shortened and restored the straight configuration within 2–4 min of slackening. The total shortening was ∼40{\%} of the original length. The recovery rate in each cycle, but not the recovery magnitude, was dependent on the axon's prior contraction history. For example, the contraction time of a previously slackened axon may be twice its first-time contraction. This recovery was significantly hampered with the depletion of ATP, inhibition of myosin motors, and disruption of actin filaments. The disruption of microtubules did not affect the recovery magnitude, but, on the contrary, led to an enhanced recovery rate compared to control cases. These results suggest that the actomyosin machinery is the major active element in axonal contraction, whereas microtubules contribute as resistive/dissipative elements.",
author = "Alireza Tofangchi and Anthony Fan and Saif, {M Taher A}",
year = "2016",
month = "10",
day = "4",
doi = "10.1016/j.bpj.2016.08.024",
language = "English (US)",
volume = "111",
pages = "1519--1527",
journal = "Biophysical Journal",
issn = "0006-3495",
publisher = "Biophysical Society",
number = "7",

}

TY - JOUR

T1 - Mechanism of Axonal Contractility in Embryonic Drosophila Motor Neurons In Vivo

AU - Tofangchi, Alireza

AU - Fan, Anthony

AU - Saif, M Taher A

PY - 2016/10/4

Y1 - 2016/10/4

N2 - Several in vitro and limited in vivo experiments have shown that neurons maintain a rest tension along their axons intrinsically. They grow in response to stretch but contract in response to loss of tension. This contraction eventually leads to the restoration of the rest tension in axons. However, the mechanism by which axons maintain tension in vivo remains elusive. The objective of this work is to elucidate the key cytoskeletal components responsible for generating tension in axons. Toward this goal, in vivo experiments were conducted on single axons of embryonic Drosophila motor neurons in the presence of various drugs. Each axon was slackened mechanically by bringing the neuromuscular junction toward the central nervous system multiple times. In the absence of any drug, axons shortened and restored the straight configuration within 2–4 min of slackening. The total shortening was ∼40% of the original length. The recovery rate in each cycle, but not the recovery magnitude, was dependent on the axon's prior contraction history. For example, the contraction time of a previously slackened axon may be twice its first-time contraction. This recovery was significantly hampered with the depletion of ATP, inhibition of myosin motors, and disruption of actin filaments. The disruption of microtubules did not affect the recovery magnitude, but, on the contrary, led to an enhanced recovery rate compared to control cases. These results suggest that the actomyosin machinery is the major active element in axonal contraction, whereas microtubules contribute as resistive/dissipative elements.

AB - Several in vitro and limited in vivo experiments have shown that neurons maintain a rest tension along their axons intrinsically. They grow in response to stretch but contract in response to loss of tension. This contraction eventually leads to the restoration of the rest tension in axons. However, the mechanism by which axons maintain tension in vivo remains elusive. The objective of this work is to elucidate the key cytoskeletal components responsible for generating tension in axons. Toward this goal, in vivo experiments were conducted on single axons of embryonic Drosophila motor neurons in the presence of various drugs. Each axon was slackened mechanically by bringing the neuromuscular junction toward the central nervous system multiple times. In the absence of any drug, axons shortened and restored the straight configuration within 2–4 min of slackening. The total shortening was ∼40% of the original length. The recovery rate in each cycle, but not the recovery magnitude, was dependent on the axon's prior contraction history. For example, the contraction time of a previously slackened axon may be twice its first-time contraction. This recovery was significantly hampered with the depletion of ATP, inhibition of myosin motors, and disruption of actin filaments. The disruption of microtubules did not affect the recovery magnitude, but, on the contrary, led to an enhanced recovery rate compared to control cases. These results suggest that the actomyosin machinery is the major active element in axonal contraction, whereas microtubules contribute as resistive/dissipative elements.

UR - http://www.scopus.com/inward/record.url?scp=85002706095&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85002706095&partnerID=8YFLogxK

U2 - 10.1016/j.bpj.2016.08.024

DO - 10.1016/j.bpj.2016.08.024

M3 - Article

C2 - 27705774

AN - SCOPUS:85002706095

VL - 111

SP - 1519

EP - 1527

JO - Biophysical Journal

JF - Biophysical Journal

SN - 0006-3495

IS - 7

ER -