Zhang Gang, Bogdanova Nataliia, Gao Tong, Song Julia J, Cragg Mark S, Glennie Martin J, Sheikh Kazim A
Department of Neurology, University of Texas Medical School at Houston, Houston, Texas, United States of America.
Antibody and Vaccine Group, Cancer Sciences Division, Faculty of Medicine, University of Southampton, Southampton, United Kingdom.
PLoS One. 2014 Feb 11;9(2):e88703. doi: 10.1371/journal.pone.0088703. eCollection 2014.
Anti-glycan/ganglioside antibodies are the most common immune effectors found in patients with Guillain-Barré Syndrome, which is a peripheral autoimmune neuropathy. We previously reported that disease-relevant anti-glycan autoantibodies inhibited axon regeneration, which echo the clinical association of these antibodies and poor recovery in Guillain-Barré Syndrome. However, the specific molecular and cellular elements involved in this antibody-mediated inhibition of axon regeneration are not previously defined. This study examined the role of Fcγ receptors and macrophages in the antibody-mediated inhibition of axon regeneration. A well characterized antibody passive transfer sciatic nerve crush and transplant models were used to study the anti-ganglioside antibody-mediated inhibition of axon regeneration in wild type and various mutant and transgenic mice with altered expression of specific Fcγ receptors and macrophage/microglia populations. Outcome measures included behavior, electrophysiology, morphometry, immunocytochemistry, quantitative real-time PCR, and western blotting. We demonstrate that the presence of autoantibodies, directed against neuronal/axonal cell surface gangliosides, in the injured mammalian peripheral nerves switch the proregenerative inflammatory environment to growth inhibitory milieu by engaging specific activating Fcγ receptors on recruited monocyte-derived macrophages to cause severe inhibition of axon regeneration. Our data demonstrate that the antibody orchestrated Fcγ receptor-mediated switch in inflammation is one mechanism underlying inhibition of axon regeneration. These findings have clinical implications for nerve repair and recovery in antibody-mediated immune neuropathies. Our results add to the complexity of axon regeneration in injured peripheral and central nervous systems as adverse effects of B cells and autoantibodies on neural injury and repair are increasingly recognized.
抗聚糖/神经节苷脂抗体是格林-巴利综合征患者中最常见的免疫效应物,格林-巴利综合征是一种周围性自身免疫性神经病变。我们之前报道过,与疾病相关的抗聚糖自身抗体抑制轴突再生,这与这些抗体和格林-巴利综合征恢复不良的临床关联相呼应。然而,此前尚未明确参与这种抗体介导的轴突再生抑制的具体分子和细胞成分。本研究探讨了Fcγ受体和巨噬细胞在抗体介导的轴突再生抑制中的作用。利用一个特征明确的抗体被动转移坐骨神经挤压和移植模型,研究抗神经节苷脂抗体介导的野生型以及特定Fcγ受体和巨噬细胞/小胶质细胞群体表达改变的各种突变和转基因小鼠的轴突再生抑制情况。结果指标包括行为、电生理学、形态学、免疫细胞化学、定量实时PCR和蛋白质印迹法。我们证明,在受伤的哺乳动物周围神经中,针对神经元/轴突细胞表面神经节苷脂的自身抗体通过与募集的单核细胞衍生巨噬细胞上的特定激活Fcγ受体结合,将促再生的炎症环境转变为生长抑制性环境,从而严重抑制轴突再生。我们的数据表明,抗体精心策划的Fcγ受体介导的炎症转变是轴突再生抑制的一种潜在机制。这些发现对抗体介导的免疫性神经病变中的神经修复和恢复具有临床意义。我们的结果增加了受伤的周围和中枢神经系统中轴突再生的复杂性,因为B细胞和自身抗体对神经损伤和修复的不利影响越来越受到认可。