Treloar Helen B, Ray Arundhati, Dinglasan Lu Anne, Schachner Melitta, Greer Charles A
Department of Neurosurgery, Yale University School of Medicine, New Haven, Connecticut 06520-8082, USA.
J Neurosci. 2009 Jul 29;29(30):9405-16. doi: 10.1523/JNEUROSCI.2356-09.2009.
We recently described the boundary-like expression pattern of the extracellular matrix molecule tenascin-C (Tnc) in the developing mouse olfactory bulb (OB) (Shay et al., 2008). In the present study, we test the hypothesis that Tnc inhibits olfactory sensory neuron (OSN) axon growth in the developing OB before glomerulogenesis. The period of time before glomerular formation begins, when axons remain restricted to the developing olfactory nerve layer (ONL), is crucial for axon sorting. Here, we show with in vitro analyses that OSN neurite outgrowth is inhibited by Tnc in a dose-dependent manner and that, in stripe assays, axons preferentially avoid Tnc. Using Tnc-null mice, we also show that that glomerular development is delayed in the absence of Tnc. In wild-type mice, OSN axons coalesce into immature or protoglomeruli, which further differentiate and segregate into glomeruli. Glomeruli are first identifiable as discrete structures at birth. In null mice, glomeruli appear immature at birth, remain fused to the ONL, and have a significantly larger diameter compared with wild-type controls. By postnatal day 4, null glomeruli are indistinguishable from controls. Thus, OSN axons appear delayed in their coalescence into glomerular structures. These data correlate with behavioral reports of Tnc-null mice, which are delayed by 24 h in their acquisition of an olfactory behavior (de Chevigny et al., 2006). Collectively, these data demonstrate that Tnc is an inhibitory boundary molecule in the developing OB during a key period of development.
我们最近描述了细胞外基质分子腱生蛋白-C(Tnc)在发育中的小鼠嗅球(OB)中的边界样表达模式(Shay等人,2008年)。在本研究中,我们检验了Tnc在肾小球形成之前抑制发育中的OB中嗅觉感觉神经元(OSN)轴突生长的假说。在轴突仍局限于发育中的嗅神经层(ONL)时,肾小球形成开始之前的这段时间对于轴突分选至关重要。在这里,我们通过体外分析表明,Tnc以剂量依赖性方式抑制OSN神经突生长,并且在条带分析中,轴突优先避开Tnc。使用Tnc基因敲除小鼠,我们还表明在没有Tnc的情况下肾小球发育延迟。在野生型小鼠中,OSN轴突聚集成不成熟的或原肾小球,其进一步分化并分离成肾小球。肾小球在出生时首先可被识别为离散结构。在基因敲除小鼠中,肾小球在出生时显得不成熟,仍与ONL融合,并且与野生型对照相比直径明显更大。到出生后第4天,基因敲除小鼠的肾小球与对照无法区分。因此,OSN轴突聚集成肾小球结构的过程似乎延迟了。这些数据与Tnc基因敲除小鼠的行为报告相关,其在获得嗅觉行为方面延迟了24小时(de Chevigny等人,2006年)。总体而言,这些数据表明Tnc在发育的关键时期是发育中的OB中的一种抑制性边界分子。