Centre for Discovery Brain Sciences, University of Edinburgh, 49 Little France Crescent, Edinburgh EH16 4SB, UK.
Department of Neurology and Program in Neuroscience, University of California, San Francisco, 675 Nelson Rising Lane, San Francisco, CA 94143, USA.
Curr Biol. 2018 Apr 23;28(8):1296-1305.e5. doi: 10.1016/j.cub.2018.02.068. Epub 2018 Apr 5.
The correct targeting of myelin is essential for nervous system formation and function. Oligodendrocytes in the CNS myelinate some axons, but not others, and do not myelinate structures including cell bodies and dendrites [1]. Recent studies indicate that extrinsic signals, such as neuronal activity [2, 3] and cell adhesion molecules [4], can bias myelination toward some axons and away from cell bodies and dendrites, indicating that, in vivo, neuronal and axonal cues regulate myelin targeting. In vitro, however, oligodendrocytes have an intrinsic propensity to myelinate [5-7] and can promiscuously wrap inert synthetic structures resembling neuronal processes [8, 9] or cell bodies [4]. A current therapeutic goal for the treatment of demyelinating diseases is to greatly promote oligodendrogenesis [10-13]; thus, it is important to test how accurately extrinsic signals regulate the oligodendrocyte's intrinsic program of myelination in vivo. Here, we test the hypothesis that neurons regulate myelination with sufficient stringency to always ensure correct targeting. Surprisingly, however, we find that myelin targeting in vivo is not very stringent and that mistargeting occurs readily when oligodendrocyte and myelin supply exceed axonal demand. We find that myelin is mistargeted to neuronal cell bodies in zebrafish mutants with fewer axons and independently in drug-treated zebrafish with increased oligodendrogenesis. Additionally, by increasing myelin production of oligodendrocytes in zebrafish and mice, we find that excess myelin is also inappropriately targeted to cell bodies. Our results suggest that balancing oligodendrocyte-intrinsic programs of myelin supply with axonal demand is essential for correct myelin targeting in vivo and highlight potential liabilities of strongly promoting oligodendrogenesis.
正确的髓鞘靶向对于神经系统的形成和功能至关重要。中枢神经系统中的少突胶质细胞对一些轴突进行髓鞘化,但对其他轴突不进行髓鞘化,并且不会对包括细胞体和树突在内的结构进行髓鞘化[1]。最近的研究表明,外在信号,如神经元活动[2,3]和细胞粘附分子[4],可以使髓鞘化偏向某些轴突,而远离细胞体和树突,表明在体内,神经元和轴突线索调节髓鞘靶向。然而,在体外,少突胶质细胞具有内在的髓鞘化倾向[5-7],并且可以混杂地包裹类似于神经元过程的惰性合成结构[8,9]或细胞体[4]。治疗脱髓鞘疾病的当前治疗目标是极大地促进少突胶质细胞发生[10-13];因此,测试外在信号在体内如何准确调节少突胶质细胞的内在髓鞘化程序非常重要。在这里,我们检验了神经元以足够的严格性调节髓鞘化以始终确保正确靶向的假设。然而,令人惊讶的是,我们发现体内的髓鞘化靶向并不十分严格,并且当少突胶质细胞和髓鞘供应超过轴突需求时,很容易发生靶向错误。我们发现,在少突胶质细胞数量减少的斑马鱼突变体中和在药物处理的增加少突胶质细胞形成的斑马鱼中,髓鞘会错误地靶向神经元细胞体。此外,通过增加斑马鱼和小鼠中少突胶质细胞的髓鞘生成,我们发现过量的髓鞘也会被错误地靶向到细胞体。我们的结果表明,平衡少突胶质细胞内在的髓鞘供应程序与轴突需求对于体内正确的髓鞘化靶向至关重要,并突出了强烈促进少突胶质细胞发生的潜在风险。