ReviewNeuronal primary cilia: a review
Section snippets
The long history of the discovery of neuronal cilia
Most neuroscientists would be surprised—if not downright skeptical—to hear that primary cilia are a consistent feature of neurons in the mammalian central nervous system. Over a century ago, the preeminent neuroanatomist Ramón y Cajal (Ramón y Cajal, 1995) drew and described in meticulous detail a myriad of neurons without including primary cilia, so how could neurons have them? To this day, cilia are rarely catalogued among the organelles of neurons, despite several demonstrations of their
Not all neuronal cilia are alike: regional variations in function?
We observed that for nearly all regions of the rat CNS, each neuron appears to have a solitary cilium(Fig. 1) as visualized by distinctive staining with an antibody raised to an N-terminal peptide from subunit of mouse G11 (Santa Cruz Biotechnology, Santa Cruz, CA, USA) (Fuchs et al., 2000; Hughes et al., 2002), which is the α-subunit of G11, a G protein that couples many neurotransmitter receptors to their second messenger responses. Staining in cilia was completely abolished by preabsorption
Information from sensory cilia
Specialized sensory cilia convey a large portion of the stream of information to the vertebrate brain. These cilia are typically nonmotile and are thought to be derived from primary cilia (Dubruille et al., 2002; Menco and Farbman, 1985a). Olfactory cilia are endowed with a sensory transduction kit complete with olfactory receptors, G proteins, adenylyl cyclase, and ion channels that initiate depolarization of the ciliated olfactory neuron. Sensory neurons in acoustico-vestibular systems have
Primary cilia as responders
Sensing in cilia is useful insofar as the end result is an adaptive response. The cilia of sensory cells transduce stimulus energy into changes in ion permeability, which in turn translates as changes in membrane potential. But how can a tiny cilium get the attention of a large neuron? Based on the information that olfactory cilia—an average of 11 per neuron in rat (Menco and Farbman, 1985b)—can trigger action potentials in an olfactory receptor neuron, it seems likely that a single primary
Cilia in development
The relationship between cilia and cell proliferation is a topic of long-standing interest (Fonte et al., 1971; Ho and Tucker, 1989). Cilia emerge from basal bodies, which originate as centrosomes, which in turn organize the mitotic spindle. Precursor cells resorb cilia just before mitosis and regrow them afterwards. It is tempting to consider that cilia may mediate influences from the extracellular milieu on cell proliferation and differentiation. Ca2+levels are implicated in mediating many
Neuronal cilia depend on intraflagellar transport; clinical implications
We recently found that most neuronal cilia appeared to be absent in mutant Tg737orpkmice, suggesting that the intraflagellar transport protein polaris (IFT88), which is necessary for ciliogenesis in various cell types (Pazour et al., 2000; Yoder et al., 2002), is also important for neuronal cilia. Again, heterogeneity is evidenced by the observation that while many brain regions in IFT88-deficient mice lacked sst3-immunoreactive cilia, some brain regions retained shortened cilia, including much
Acknowledgements
We thank our students who participated in the research, particularly Rhome Hughes for his morphometric study of neuronal cilia. Those currently working on the Tg737orpkmouse brains include Ankur Patel, Rajin Shahriar, Suman Pasapuleti, and Weilan Zuo. We are grateful to Dr Gregory Pazour for providing the Tg737orpkbrains. This research was supported by NIMH MH41865 (JLF), NIH NS41891 (HDS), and grants from the University of North Texas.
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Molecular control of the development of hypothalamic neurons involved in metabolic regulation
2022, Journal of Chemical NeuroanatomyPatterns of cilia gene dysregulations in major psychiatric disorders
2021, Progress in Neuro-Psychopharmacology and Biological PsychiatryCitation Excerpt :Primary cilia are microtubule-based organelles that protrude from the surface of almost all cell types including neurons (Fuchs and Schwark, 2004; Baudoin et al., 2012; Gerdes et al., 2009).
Primary cilia in the Syrian hamster biliary tract: Bile flow antennae and outlooks about signaling on the hepato-biliary-pancreatic stem cells
2020, Translational Research in AnatomyCitation Excerpt :If motility is the primary function for a cilium, the primary cilia are immotile and are only involved in sensory function(s), as shown long ago by the photoreceptors of the retinal epithelium [57,79,80]. A plethora of reviews about the primary cilia that have appeared in several biomedical journals [e.g. 29–48,59,60,71–81,84–88,90,93,97–107] are certainly informative about the diverse tissue's occurrence, but some of those, published with a few weeks apart, often make information redundant and have not brought new morphological information. In fact, there are reviews that make the topic hard to be understood by the unprepared readers because did not distinguish between the typical, motile ‘cilium’ and ‘flagellum’ from ‘primary cilium’ or even classified them as one ‘immotile cilium’ even if this cilium has never been motile… because it does not have central microtubules as reviewed in Ref. [57] and recently brilliantly shown in 3-D views [59].
Primary cilia formation is diminished in schizophrenia and bipolar disorder: A possible marker for these psychiatric diseases
2018, Schizophrenia ResearchCitation Excerpt :The primary cilium (PC) is a non-motile organelle composed of nine pairs of peripheral microtubules with no central pair of singlet microtubules (9 + 0), in contrast with the ciliary axoneme, which can be found in motile cilia (9 + 2) (Satir and Christensen, 2007). This organelle protrudes from the plasma membrane in almost every single cell type, including brain neurons (Fuchs and Schwark, 2004), and use the mother centriole as a cytosolic template, known as the basal body (Sorokin, 1962). Primary cilia are formed during the G0 or G1 phase of the cell cycle (Kim and Tsiokas, 2011) and its membrane is a selectively enriched center of GPCRs (Schou et al., 2015), which are carried along the axoneme by intraflagellar transport (IFT) (Kozminski et al., 1993; Rosenbaum and Witman, 2002).
Cilia loss on distinct neuron populations differentially alters cocaine-induced locomotion and reward
2024, Journal of Psychopharmacology