Development and distribution of neuronal cilia in mouse neocortex.
Neuronal primary cilia are not generally recognized, but they are considered to extend from most, if not all, neurons in the neocortex. However, when and how cilia develop in neurons are not known. This study used immunohistochemistry for adenylyl cyclase III (ACIII), a marker of primary cilia, and electron microscopic analysis to describe the development and maturation of cilia in mouse neocortical neurons. Our results indicate that ciliogenesis is initiated in late fetal stages after neuroblast migration, when the mother centriole docks with the plasma membrane, becomes a basal body, and grows a cilia bud that we call a procilium. This procilium consists of a membranous protrusion extending from the basal body but lacking axonemal structure and remains undifferentiated until development of the axoneme and cilia elongation starts at about postnatal day 4. Neuronal cilia elongation and final cilia length depend on layer position, and the process extends for a long time, lasting 8-12 weeks. We show that, in addition to pyramidal neurons, inhibitory interneurons also grow cilia of comparable length, suggesting that cilia are indeed present in all neocortical neuron subtypes. Furthermore, the study of mice with defective ciliogenesis suggested that failed elongation of cilia is not essential for proper neuronal migration and laminar organization or establishment of neuronal polarity. Thus, the function of this organelle in neocortical neurons remains elusive.
Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510, USA. jon.arellano@yale.edu
Jon I
JI
Arellano
Sarah M
SM
Guadiana
Joshua J
JJ
Breunig
Pasko
P
Rakic
Matthew R
MR
Sarkisian
D000199:Actins / Q000276:immunology; D000262:Adenylyl Cyclases / Q000276:immunology; D000818:Animals; D000906:Antibodies / Q000032:analysis / Q000276:immunology; D000941:Antigens / Q000276:immunology / Q000378:metabolism; D001369:Axons / Q000378:metabolism / Q000648:ultrastructure; D015153:Blotting, Western; D064032:Calbindin 2; D064026:Calbindins; D016764:Cell Polarity / Q000502:physiology; D002645:Chickens / Q000276:immunology; D002923:Cilia / Q000502:physiology* / Q000648:ultrastructure; D004268:DNA-Binding Proteins; D018274:Electroporation; D047108:Embryonic Development; D005260:Female; D049452:Green Fluorescent Proteins / Q000276:immunology; D007150:Immunohistochemistry; D051379:Mice; D008854:Microscopy, Electron; D016253:Microscopy, Immunoelectron; D019579:Neocortex / Q000166:cytology* / Q000254:growth & development* / Q000648:ultrastructure; D009419:Nerve Tissue Proteins / Q000276:immunology; D009474:Neurons / Q000502:physiology* / Q000648:ultrastructure; D009687:Nuclear Proteins / Q000276:immunology; D010320:Parvalbumins / Q000276:immunology; D011247:Pregnancy; D064030:S100 Calcium Binding Protein G / Q000276:immunology
D000199:Actins; D000906:Antibodies; D000941:Antigens; D064032:Calbindin 2; D064026:Calbindins; D004268:DNA-Binding Proteins; D009419:Nerve Tissue Proteins; C492380:NeuN protein, mouse; D009687:Nuclear Proteins; D010320:Parvalbumins; D064030:S100 Calcium Binding Protein G; C086178:pericentrin; D049452:Green Fluorescent Proteins; D000262:Adenylyl Cyclases; C421784:adenylate cyclase 3