Neurons differentiate magnitude and location of mechanical stimuli

被引:69
作者
Gaub, Benjamin M. [1 ]
Kasuba, Krishna Chaitanya [1 ]
Mace, Emilie [2 ]
Strittmatter, Tobias [1 ]
Laskowski, Pawel R. [1 ]
Geissler, Sydney A. [1 ]
Hierlemann, Andreas [1 ]
Fussenegger, Martin [1 ]
Roska, Botond [2 ]
Mueller, Daniel J. [1 ]
机构
[1] Eidgenossische Tech Hsch Zurich, Dept Biosyst Sci & Engn, CH-4058 Basel, Switzerland
[2] Friedrich Miescher Inst Biomed Res, Neural Circuit Labs, CH-4058 Basel, Switzerland
关键词
atomic force microscopy; calcium response; mechanobiology; mechanosensitivity; cortex neurons; CALCIUM-CHANNELS; CATION CHANNEL; BRAIN; TRPV1; THRESHOLD; STRETCH; PIEZO1; FORM;
D O I
10.1073/pnas.1909933117
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Neuronal activity can be modulated by mechanical stimuli. To study this phenomenon quantitatively, we mechanically stimulated rat cortical neurons by shear stress and local indentation. Neurons show 2 distinct responses, classified as transient and sustained. Transient responses display fast kinetics, similar to spontaneous neuronal activity, whereas sustained responses last several minutes before returning to baseline. Local soma stimulations with micrometersized beads evoke transient responses at low forces of similar to 220 nN and pressures of similar to 5.6 kPa and sustained responses at higher forces of similar to 360 nN and pressures of similar to 9.2 kPa. Among the neuronal compartments, axons are highly susceptible to mechanical stimulation and predominantly show sustained responses, whereas the less susceptible dendrites predominantly respond transiently. Chemical perturbation experiments suggest that mechanically evoked responses require the influx of extracellular calcium through ion channels. We propose that subtraumatic forces/pressures applied to neurons evoke neuronal responses via nonspecific gating of ion channels.
引用
收藏
页码:848 / 856
页数:9
相关论文
共 44 条
[1]   Atomic force microscopy-based characterization and design of biointerfaces [J].
Alsteens, David ;
Gaub, Hermann E. ;
Newton, Richard ;
Pfreundschuh, Moritz ;
Gerber, Christoph ;
Muller, Daniel J. .
NATURE REVIEWS MATERIALS, 2017, 2 (05)
[2]   Neurosensory mechanotransduction [J].
Chalfie, Martin .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2009, 10 (01) :44-52
[3]  
Colton C. K., 2007, V179, P173
[4]   STED Nanoscopy Reveals the Ubiquity of Subcortical Cytoskeleton Periodicity in Living Neurons [J].
D'Este, Elisa ;
Kamin, Dirk ;
Goettfert, Fabian ;
El-Hady, Ahmed ;
Hell, Stefan W. .
CELL REPORTS, 2015, 10 (08) :1246-1251
[5]   Capsazepine block of voltage-activated calcium channels in adult rat dorsal root ganglion neurones in culture [J].
Docherty, RJ ;
Yeats, JC ;
Piper, AS .
BRITISH JOURNAL OF PHARMACOLOGY, 1997, 121 (07) :1461-1467
[6]   Neurite Branch Retraction Is Caused by a Threshold-Dependent Mechanical Impact [J].
Franze, Kristian ;
Gerdelmann, Jens ;
Weick, Michael ;
Betz, Timo ;
Pawlizak, Steve ;
Lakadamyali, Melike ;
Bayer, Johannes ;
Rillich, Katja ;
Goegler, Michael ;
Lu, Yun-Bi ;
Reichenbach, Andreas ;
Janmey, Paul ;
Kaes, Josef .
BIOPHYSICAL JOURNAL, 2009, 97 (07) :1883-1890
[7]   AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3-dihydrobenzo[b][1,4]dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties [J].
Gavva, NR ;
Tamir, R ;
Qu, YS ;
Klionsky, L ;
Zhang, TJ ;
Immke, D ;
Wang, J ;
Zhu, D ;
Vanderah, TW ;
Porreca, F ;
Doherty, EM ;
Norman, MH ;
Wild, KD ;
Bannon, AW ;
Louis, JC ;
Treanor, JJS .
JOURNAL OF PHARMACOLOGY AND EXPERIMENTAL THERAPEUTICS, 2005, 313 (01) :474-484
[8]   Mechanical stretch to neurons results in a strain rate and magnitude-dependent increase in plasma membrane permeability [J].
Geddes, DM ;
Cargill, RS ;
LaPlaca, MC .
JOURNAL OF NEUROTRAUMA, 2003, 20 (10) :1039-1049
[9]   An in vitro model of neural trauma:: Devise characterization and calcium response to mechanical stretch [J].
Geddes, DM ;
Cargill, RS .
JOURNAL OF BIOMECHANICAL ENGINEERING-TRANSACTIONS OF THE ASME, 2001, 123 (03) :247-255
[10]   Chronic Traumatic Encephalopathy in Blast-Exposed Military Veterans and a Blast Neurotrauma Mouse Model [J].
Goldstein, Lee E. ;
Fisher, Andrew M. ;
Tagge, Chad A. ;
Zhang, Xiao-Lei ;
Velisek, Libor ;
Sullivan, John A. ;
Upreti, Chirag ;
Kracht, Jonathan M. ;
Ericsson, Maria ;
Wojnarowicz, Mark W. ;
Goletiani, Cezar J. ;
Maglakelidze, Giorgi M. ;
Casey, Noel ;
Moncaster, Juliet A. ;
Minaeva, Olga ;
Moir, Robert D. ;
Nowinski, Christopher J. ;
Stern, Robert A. ;
Cantu, Robert C. ;
Geiling, James ;
Blusztajn, Jan K. ;
Wolozin, Benjamin L. ;
Ikezu, Tsuneya ;
Stein, Thor D. ;
Budson, Andrew E. ;
Kowall, Neil W. ;
Chargin, David ;
Sharon, Andre ;
Saman, Sudad ;
Hall, Garth F. ;
Moss, William C. ;
Cleveland, Robin O. ;
Tanzi, Rudolph E. ;
Stanton, Patric K. ;
McKee, Ann C. .
SCIENCE TRANSLATIONAL MEDICINE, 2012, 4 (134)