Nahir Guadalupe Gazal, Maria Jose Castellanos-Montiel, Guillermina Bruno, Anna Kristina Franco-Flores, Sarah Lépine, Lale Gursu, Ghazal Haghi, Gilles Maussion, Wolfgang E Reintsch, Fernando D Stefani, Agustín Anastasía, Mariano Bisbal, Ezequiel Axel Gorostiza, Thomas M Durcan, Nicolás Unsain
The actin/spectrin membrane-associated periodic skeleton (MPS) is a cytoskeletal structure that supports axonal integrity and function. Lower spinal motor neurons (MNs) are characterized by exceptionally long axons and are particularly susceptible to degeneration in a wide range of hereditary neuromuscular disorders, including amyotrophic lateral sclerosis. Using confocal and super-resolution imaging, we characterized the spatial distribution of βII-spectrin and the assembly pattern of the MPS in human MN axons derived from induced pluripotent stem cells. We discovered a striking gap-and-patch pattern in the medial axon, where sharply demarcated βII-spectrin gaps alternate with patches containing a well-organized MPS. The pattern is acutely induced by the kinase inhibitor staurosporine and pharmacological inhibition of actin polymerization prevents patch formation, indicating a requirement for actin nucleation in MPS assembly. Our data supports a model in which spectrin incorporation into nascent MPS patches depletes neighboring regions, producing long-range gaps-and-patches patterns.