C-elegans multi-dendritic sensory neurons: Morphology and function

被引:116
作者
Albeg, Adi [1 ]
Smith, Cody J. [2 ,3 ]
Chatzigeorgiou, Marios [4 ]
Feitelson, Dror G. [5 ]
Hall, David H. [6 ]
Schafer, William R. [4 ]
Miller, David M., III [2 ,3 ]
Treinin, Millet [1 ]
机构
[1] Hebrew Univ Hadassah Med Sch, Inst Med Res Israel Canada, Dept Med Neurobiol, IL-91120 Jerusalem, Israel
[2] Vanderbilt Univ, Dept Cell & Dev Biol, Nashville, TN 37232 USA
[3] Vanderbilt Univ, Program Neurosci, Nashville, TN 37232 USA
[4] MRC Lab Mol Biol, Div Cell Biol, Cambridge, England
[5] Hebrew Univ Jerusalem, Dept Comp Sci, IL-91904 Jerusalem, Israel
[6] Albert Einstein Coll Med, Dept Neurosci, Bronx, NY 10467 USA
关键词
C; elegans; Somatosensory system; Nociceptor; Proprioceptor; Behavior; Movement; TOUCH RECEPTOR NEURONS; CAENORHABDITIS-ELEGANS; ACETYLCHOLINE-RECEPTOR; MECHANOSENSORY NEURONS; NERVOUS-SYSTEM; MEC-3; GENE; CELL-TYPES; EXPRESSION; DEGENERATION; CHANNEL;
D O I
10.1016/j.mcn.2010.10.001
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
PVD and FLP sensory neurons envelope the body of the C elegans adult with a highly branched network of thin sensory processes. Both PVD and FLP neurons are mechanosensors. PVD is known to mediate the response to high threshold mechanical stimuli. Thus PVD and FLP neurons are similar in both morphology and function to mammalian nociceptors. To better understand the function of these neurons we generated strains lacking them. Behavioral analysis shows that PVD and FLP regulate movement under normal growth conditions, as animals lacking these neurons demonstrate higher dwelling behavior. In addition, PVD-whose thin branches project across the body-wall muscles-may have a role in proprioception, as ablation of PVD leads to defective posture. Moreover, movement-dependent calcium transients are seen in PVD, a response that requires MEC-10, a subunit of the mechanosensory DEG/ENaC channel that is also required for maintaining wild-type posture. Hence, PVD senses both noxious and innocuous signals to regulate C elegans behavior, and thus combines the functions of multiple mammalian somatosensory neurons. Finally, strong mechanical stimulation leads to inhibition of egg-laying, and this response also depends on PVD and FLP neurons. Based on all these results we suggest that noxious signals perceived by PVD and FLP promote an escape behavior consisting of increased speed, reduced pauses and reversals, and inhibition of egg-laying. (C) 2010 Elsevier Inc. All rights reserved.
引用
收藏
页码:308 / 317
页数:10
相关论文
共 34 条
[1]   Sense and specificity: a molecular identity far nociceptors [J].
Caterina, MJ ;
Julius, D .
CURRENT OPINION IN NEUROBIOLOGY, 1999, 9 (05) :525-530
[2]   DEVELOPMENTAL GENETICS OF THE MECHANOSENSORY NEURONS OF CAENORHABDITIS-ELEGANS [J].
CHALFIE, M ;
SULSTON, J .
DEVELOPMENTAL BIOLOGY, 1981, 82 (02) :358-370
[3]   Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors [J].
Chatzigeorgiou, Marios ;
Yoo, Sungjae ;
Watson, Joseph D. ;
Lee, Wei-Hsiang ;
Spencer, W. Clay ;
Kindt, Katie S. ;
Hwang, Sun Wook ;
Miller, David M., III ;
Treinin, Millet ;
Driscoll, Monica ;
Schafer, William R. .
NATURE NEUROSCIENCE, 2010, 13 (07) :861-U106
[4]   THE MEC-4 GENE IS A MEMBER OF A FAMILY OF CAENORHABDITIS-ELEGANS GENES THAT CAN MUTATE TO INDUCE NEURONAL DEGENERATION [J].
DRISCOLL, M ;
CHALFIE, M .
NATURE, 1991, 349 (6310) :588-593
[5]   PROPER EXPRESSION OF MYOSIN GENES IN TRANSGENIC NEMATODES [J].
FIRE, A ;
WATERSTON, RH .
EMBO JOURNAL, 1989, 8 (11) :3419-3428
[6]   The C-elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors [J].
Halevi, S ;
McKay, J ;
Palfreyman, M ;
Yassin, L ;
Eshel, M ;
Jorgensen, E ;
Treinin, M .
EMBO JOURNAL, 2002, 21 (05) :1012-1020
[7]   THE MEC-7 BETA-TUBULIN GENE OF CAENORHABDITIS-ELEGANS IS EXPRESSED PRIMARILY IN THE TOUCH RECEPTOR NEURONS [J].
HAMELIN, M ;
SCOTT, IM ;
WAY, JC ;
CULOTTI, JG .
EMBO JOURNAL, 1992, 11 (08) :2885-2893
[8]   GENE INTERACTIONS AFFECTING MECHANOSENSORY TRANSDUCTION IN CAENORHABDITIS-ELEGANS [J].
HUANG, MX ;
CHALFIE, M .
NATURE, 1994, 367 (6462) :467-470
[9]   A sensory feedback circuit coordinates muscle activity in Drosophila [J].
Hughes, Cynthia L. ;
Thomas, John B. .
MOLECULAR AND CELLULAR NEUROSCIENCE, 2007, 35 (02) :383-396
[10]   A DUAL MECHANOSENSORY AND CHEMOSENSORY NEURON IN CAENORHABDITIS-ELEGANS [J].
KAPLAN, JM ;
HORVITZ, HR .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1993, 90 (06) :2227-2231