Melanin-concentrating hormone regulates beat frequency of ependymal cilia and ventricular volume

Conductier, Grégory; Brau, Frédéric; Viola, Angèle; Langlet, Fanny; Ramkumar, Navean; Dehouck, Bénédicte; Lemaire, T.; Chapot, Raphaël; Lucas, Laurianne; Rovère, Carole; Maitre, Priscilla; Hosseiny, Salma; Petit-Paitel, Agnès; Adamantidis, Antoine; Lakaye, Bernard; Risold, Pierre‐Yves; Prévot, Vincent; Meste, Olivier; Nahon, Jean‐Louis; Guyon, Alice

doi:10.1038/nn.3401

Cited by 74 publications

(80 citation statements)

References 19 publications

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“…When applied to real data, the MLE method was successfully used to determine the CBF of ependymal cells boarding the mouse third ventricle in brain slices [2]. In this study, we have shown that the CBF varies from slice to slice between 2 and 16 Hz with an average of 11.18 ± 0.72 Hz (N = 55 slices in 14 mice) and that it is positively modulated by the neurotransmitter serotonin, by ATP and by the hypothalamic peptide melanin-concentrating hormone (MCH).…”

Section: Resultsmentioning

confidence: 99%

“…7e illustrates that it is possible to record higher CBFs. It shows the effects on CBFs recorded at 34 • C (thus with a faster baseline CBF) of increasing concentrations of an orexigenic hypothalamic peptide known to be released during fasting, melanin-concentrating hormone (MCH), which has previously been shown to modulate the CBFs in the third ventricle [2].…”

Section: Resultsmentioning

confidence: 99%

“…First, cilia are densely packed on all naturally occurring ciliated surfaces (Figs. 1,2). Since this density is Abstract The estimation of the cilia beating frequency (CBF) is of great interest in understanding how the CBF modulates liquid fluxes and how it is controlled by the ciliated cell intra-and/or extracellular medium composition in physiological processes.…”

Section: Introductionmentioning

confidence: 99%

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Robust estimation of the motile cilia beating frequency

Meste

Brau

Guyon

2015

Med Biol Eng Comput

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The estimation of the cilia beating frequency (CBF) is of great interest in understanding how the CBF modulates liquid fluxes and how it is controlled by the ciliated cell intra- and/or extracellular medium composition in physiological processes. Motion artifacts and camera defaults may hinder the computation of the frequency variations during long-lasting experiments. We have developed a new analysis approach consisting of a preliminary corrective step (removal of a grid pattern on the image sequence and shift compensation), followed by a harmonic model of the observed cilia using a maximum likelihood estimator framework. It is shown that a more accurate estimation of the frequency can be obtained by averaging the squared Fourier transform of individual pixels followed by a particular summation over the different frequencies, namely the compressed spectrum. Robustness of the proposed method over traditional approaches is shown by several examples and simulations. The method is then applied to images of samples containing ciliated ependymal cells located in the third cerebral ventricle of mouse brains, showing that even small variations in CBF in response to changes in the amount of oxygenation, pH or glucose were clearly visible in the computed frequencies. As a conclusion, this method reveals a fine metabolic tuning of the cilia beating in ependimocytes lining the third cerebral ventricle. Such regulations are likely to participate in homeostatic mechanisms regulating CSF movements and brain energy supply.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Robust estimation of the motile cilia beating frequency

Meste

Brau

Guyon

2015

Med Biol Eng Comput

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“…Neuropeptides regulate ciliary beating and influence larval swimming behavior in marine annelids (Conzelmann et al, 2011) and melanin-concentrating hormone regulates ciliary beat frequency in the ependymal cells that move cerebrospinal fluid in the ventricles (Conductier et al, 2013). In addition, the G-proteincoupled receptors for neuropeptide Y, somatostatin and kisspeptin localize to neuronal cilia (Loktev and Jackson, 2013).…”

Section: Introductionmentioning

confidence: 99%

Early eukaryotic origins for cilia-associated bioactive peptide-amidating activity

Kumar

Blaby‐Haas

Merchant

et al. 2016

Journal of Cell Science

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Ciliary axonemes and basal bodies were present in the last eukaryotic common ancestor and play crucial roles in sensing and responding to environmental cues. Peptidergic signaling, generally considered a metazoan innovation, is essential for organismal development and homeostasis. Peptidylglycine α-amidating monooxygenase (PAM) is crucial for the last step of bioactive peptide biosynthesis. However, identification of a complete PAM-like gene in green algal genomes suggests ancient evolutionary roots for bioactive peptide signaling. We demonstrate that the Chlamydomonas reinhardtii PAM gene encodes an active peptide-amidating enzyme (CrPAM) that shares key structural and functional features with the mammalian enzyme, indicating that components of the peptide biosynthetic pathway predate multicellularity. In addition to its secretory pathway localization, CrPAM localizes to cilia and tightly associates with the axonemal superstructure, revealing a new axonemal enzyme activity. This localization pattern is conserved in mammals, with PAM present in both motile and immotile sensory cilia. The conserved ciliary localization of PAM adds to the known signaling capabilities of the eukaryotic cilium and provides a potential mechanistic link between peptidergic signaling and endocrine abnormalities commonly observed in ciliopathies.

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“…Collectively, our data revealed a dynamic control of MCH neurons on spontaneous CBF of MCH-R1-expressing ependymal cells and on cerebrospinal fluid flow in brain ventricles. 40,41 MCH-R2 STRUCTURE AND SIGNALLING The second MCH receptor, named here MCH-R2, was identified in the human genome by use of in silico data mining, and its complementary DNA was subsequently isolated from human brain complementary DNA libraries. 18--19 In contrast to the MCH-R1 gene, which is intronless in its coding region, the MCH-R2 gene encompasses five coding and one noncoding exon and may produce receptor variants by alternative splicing that would lead to a truncated version of MCH-R2.…”

Section: Mch-r1 Structure and Signallingmentioning

confidence: 99%

The melanin-concentrating hormone receptors: neuronal and non-neuronal functions

et al. 2014

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Melanin-concentrating hormone (MCH) is a cyclic peptide highly conserved in vertebrates and was originally identified as a skin-paling factor in Teleosts. In fishes, MCH also participates in the regulation of the stress-response and feeding behaviour. Mammalian MCH is a hypothalamic neuropeptide that displays multiple functions, mostly controlling feeding behaviour and energy homeostasis. Transgenic mouse models and pharmacological studies have shown the importance of the MCH system as a potential target in the treatment of appetite disorders and obesity as well as anxiety and psychiatric diseases. Two G-proteincoupled receptors (GPCRs) binding MCH have been characterized so far. The first, named MCH-R1 and also called SLC1, was identified through reverse pharmacology strategies by several groups as a cognate receptor of MCH. This receptor is expressed at high levels in many brain areas of rodents and primates and is also expressed in peripheral organs, albeit at a lower rate. A second receptor, designated MCH-R2, exhibited 38% identity to MCH-R1 and was identified by sequence analysis of the human genome. Interestingly, although MCH-R2 orthologues were also found in fishes, dogs, ferrets and non-human primates, this MCH receptor gene appeared either lacking or non-functional in rodents and lagomorphs. Both receptors are class I GPCRs, whose main roles are to mediate the actions of peptides and neurotransmitters in the central nervous system. However, examples of action of MCH on neuronal and non-neuronal cells are emerging that illustrate novel MCH functions. In particular, the functionality of endogenously expressed MCH-R1 has been explored in human neuroblastoma cells, SK-N-SH and SH-SY5Y cells, and in non-neuronal cell types such as the ependymocytes. Indeed, we have identified mitogen-activated protein kinase (MAPK)-dependent or calcium-dependent signalling cascades that ultimately contributed to neurite outgrowth in neuroblastoma cells or to modulation of ciliary beating in ependymal cells. The putative role of MCH on cellular shaping and plasticity on one side and volume transmission on the other must be now considered.International Journal of Obesity Supplements (2014) 4, S31--S36; doi:10.1038/ijosup.2014.9Keywords: AROM gene; energy balance; feeding behaviour; melanin-concentrating hormone; MCH receptors; primate-specific PMCHL genes Melanin-concentrating hormone (MCH) is a cyclic peptide that was first isolated from salmon pituitary glands 1 and subsequently characterized in the rat hypothalamus.2 Brain and peripheral expression of MCH was then established in many mammalian species including humans (reviewed in Nahon et al.3 ). In the central nervous system, MCH mRNA and peptide syntheses were found predominantly in neurons of the lateral hypothalamus and zona incerta that projected throughout the brain 4,5 (Figure 1 12). The first receptor, named here MCH-R1, also called SLC1, was simultaneously identified through reverse pharmacology strategies by several groups as a cognate receptor of MCH. 13--16 ...

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Melanin-concentrating hormone regulates beat frequency of ependymal cilia and ventricular volume

Cited by 74 publications

References 19 publications

Robust estimation of the motile cilia beating frequency

Robust estimation of the motile cilia beating frequency

Early eukaryotic origins for cilia-associated bioactive peptide-amidating activity

The melanin-concentrating hormone receptors: neuronal and non-neuronal functions

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