High-resolution live imaging reveals axon-glia interactions during peripheral nerve injury and repair in zebrafish

被引:36
作者
Xiao, Yan [1 ]
Faucherre, Adele [2 ]
Pola-Morell, Laura [2 ]
Heddleston, John M. [3 ]
Liu, Tsung-Li [3 ]
Chew, Teng-Leong [3 ]
Sato, Fuminori [4 ]
Sehara-Fujisawa, Atsuko [4 ]
Kawakami, Koichi [5 ,6 ]
Lopez-Schier, Hernan [1 ,2 ]
机构
[1] Helmholtz Zentrum Munchen, Res Unit Sensory Biol Organogenesis, D-85764 Munich, Germany
[2] Ctr Genom Regulat, Cell & Dev Biol, Barcelona 08003, Spain
[3] Howard Hughes Med Inst, Ashburn, VA 20147 USA
[4] Kyoto Univ, Inst Frontier Med Sci, Sakyo Ku, Kyoto 6068507, Japan
[5] Grad Univ Adv Studies Sokendai, Natl Inst Genet, Div Mol & Dev Biol, Mishima, Shizuoka 4118540, Japan
[6] Grad Univ Adv Studies Sokendai, Dept Genet, Mishima, Shizuoka 4118540, Japan
关键词
High-resolution imaging; Neurotrauma; Regeneration; Schwann cells; Haptotaxis; SCHWANN-CELL DENERVATION; TARGETED GENE-EXPRESSION; BEAM PLANE ILLUMINATION; LATERAL-LINE; MYELINATED AXONS; EXPERIMENTAL STRATEGIES; FUNCTIONAL RECOVERY; REGENERATION; GROWTH; ADULT;
D O I
10.1242/dmm.018184
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Neural damage is a devastating outcome of physical trauma. The glia are one of the main effectors of neuronal repair in the nervous system, but the dynamic interactions between peripheral neurons and Schwann cells during injury and regeneration remain incompletely characterized. Here, we combine laser microsurgery, genetic analysis, high-resolution intravital imaging and lattice light-sheet microscopy to study the interaction between Schwann cells and sensory neurons in a zebrafish model of neurotrauma. We found that chronic denervation by neuronal ablation leads to Schwann-cell death, whereas acute denervation by axonal severing does not affect the overall complexity and architecture of the glia. Neuronal-circuit regeneration begins when Schwann cells extend bridging processes to close the injury gap. Regenerating axons grow faster and directionally after the physiological clearing of distal debris by the Schwann cells. This might facilitate circuit repair by ensuring that axons are guided through unoccupied spaces within bands of Bungner towards their original peripheral target. Accordingly, in the absence of Schwann cells, regenerating axons are misrouted, impairing the re-innervation of sensory organs. Our results indicate that regenerating axons use haptotaxis as a directional cue during the reconstitution of a neural circuit. These findings have implications for therapies aimed at neurorepair, which will benefit from preserving the architecture of the peripheral glia during periods of denervation.
引用
收藏
页码:553 / 564
页数:12
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