Comparative Distribution and In Vitro Activities of the Urotensin II-Related Peptides URP1 and URP2 in Zebrafish: Evidence for Their Colocalization in Spinal Cerebrospinal Fluid-Contacting Neurons

Quan, Feng B.; Dubessy, Christophe; Galant, Sonya; Кенигфест, Н. Б.; Djenoune, Lydia; Leprince, Jérôme; Wyart, Claire; Lihrmann, Isabelle; Tostivint, Hervé

doi:10.1371/journal.pone.0119290

Cited by 54 publications

(72 citation statements)

References 72 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The mechanisms underlying the contribution of Pkd2l1 in CSF-cNs to body axis maintenance are unknown. CSF-cNs in the spinal cord express neuropeptides and monoamines and modulate excitability of motor circuits via GABAergic synapses [36][37][38] . CSF-cNs synapse onto premotor and motor neurons 22,39,40 ; decreased CSF-cN activity throughout life may lead to changes in swimming output.…”

Section: Discussionmentioning

confidence: 99%

Pkd2l1 is required for mechanoception in cerebrospinal fluid-contacting neurons and maintenance of spine curvature

Sternberg

Prendergast

Brosse

et al. 2018

Preprint

Self Cite

View full text Add to dashboard Cite

Flow of cerebrospinal fluid (CSF) may contribute to spine morphogenesis, as mutations affecting both cilia motility and CSF flow lead to scoliosis 1 . However, the mechanisms underlying detection of the CSF flow in the central canal of the spinal cord remain elusive. Here we used full-field optical coherence tomography (FF-OCT) and bead tracking to demonstrate that CSF flows bidirectionally along the antero-posterior axis in the central canal of zebrafish embryos. In the zebrafish mutant cfap298 tm304 , previously known as kurly, reduction of cilia motility slows transport down the length of central canal. To investigate downstream mechanisms that could transduce CSF flow, we performed calcium imaging in sensory neurons contacting the CSF (CSF-cNs) and found that disruption in cilia motility impaired the activity of CSF-cNs. CSF-cNs across species express the transient receptor potential channel PKD2L1, also known as TRPP3, which contributes to CSF-cN chemosensory properties. Using calcium imaging and whole-cell patch clamp recordings, we found that the loss of the Pkd2l1 channel in pkd2l1 mutant embryos also abolished CSF-cN activity. Whole-cell recordings further demonstrated that opening of a single channel is sufficient to trigger action potentials in wild type CSF-cNs. Recording from isolated cells in vitro, we showed that CSF-cNs are mechanosensory cells that respond to pressure in a Pkd2l1-dependent manner. Interestingly, adult pkd2l1 mutant zebrafish develop an exaggerated spine curvature, reminiscent of kyphosis in humans. Our study indicates that CSF-cNs are mechanosensory cells whose spontaneous activity reflects CSF flow in vivo. Furthermore, Pkd2l1 in CSF-cNs contributes to the maintenance of the natural curvature of the spine.

show abstract

Section: Discussionmentioning

confidence: 99%

Pkd2l1 is required for mechanoception in cerebrospinal fluid-contacting neurons and maintenance of spine curvature

Sternberg

Prendergast

Brosse

et al. 2018

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Several genes encoding regulators of embryonic axis curvature were also upregulated in rpgrip1l ∆/∆ fish, among which pkd1b [21], urp1 and upr2 [4] and scospondin [3]. urp1 and urp2 encode peptides of the Urotensin II family and are expressed in ventral spinal CSF-cNs [22,23].…”

Section: Upregulation Of Urp Signaling Participates In Scoliosis Onsementioning

confidence: 99%

“…To investigate the tissue specificity of this up-regulation, we performed immunofluorescence with an antibody to a conserved domain of the Urotensin II peptide family [24,25]. In the zebrafish spinal cord, urp1 and urp2 are expressed in ventral CSF-cNs while other genes of the family are expressed in the caudal neurosecretory system [23,25,26].…”

Section: Upregulation Of Urp Signaling Participates In Scoliosis Onsementioning

confidence: 99%

Loss of the Reissner Fiber and increased URP neuropeptide signaling underlie scoliosis in a zebrafish ciliopathy mutant

Vesque

Anselme

Pézeron³

et al. 2019

Preprint

View full text Add to dashboard Cite

Cilia-driven movements of the cerebrospinal fluid (CSF) are involved in zebrafish axis straightness, both in embryos and juveniles [1,2]. In embryos, axis straightness requires ciliadependent assembly of the Reissner fiber (RF), a SCO-spondin polymer running down the brain and spinal cord CSF-filled cavities [3]. Reduced expression levels of the urp1 and urp2 genes encoding neuropeptides of the Urotensin II family in CSF-contacting neurons (CSF-cNs) also underlie embryonic ventral curvature of several cilia motility mutants [4]. Moreover, mutants for scospondin and uts2r3 (a Urotensin II peptide family receptor gene) develop scoliosis at juvenile stages [3,4]. However, whether RF maintenance and URP signaling are perturbed in juvenile scoliotic ciliary mutants and how these perturbations are linked to scoliosis is unknown. Here we produced mutants in the zebrafish ortholog of the human RPGRIP1L ciliopathy gene encoding a transition zone protein [5][6][7]. rpgrip1l -/zebrafish had normal embryogenesis and developed 3D spine torsions in juveniles. Cilia lining the CNS cavities were normal in rpgrip1l -/embryos but sparse and malformed in juveniles and adults.Hindbrain ventricle dilations were present at scoliosis onset, suggesting defects in CSF flow.Immunostaining showed a secondary loss of RF correlating with juvenile scoliosis.Surprisingly, transcriptome analysis of rgprip1l mutants at scoliosis onset uncovered increased levels of urp1 and urp2 expression. Overexpressing urp2 in foxj1-expressing cells triggered scoliosis in rpgrip1l heterozygotes. Thus, our results demonstrate that increased URP signaling drives scoliosis onset in a ciliopathy mutant. We propose that imbalanced levels of URP neuropeptides in CSF-cNs may be an initial trigger of scoliosis.

show abstract

“…(H-Val-Phe-Cys-Asn-Ser-Tyr-Gly-Gly-Cys-Lys-Ser-Phe-OH; LV-5348), and SoCCAP3 (H-Val-Phe-Cys-Asn-Ser-Phe-Gly-Gly-Cys-Gln-Asn-OH; LV-5346) were synthesized (0.1 mmol scale) on Fmoc-Ile-PEG-PS, Fmoc-Phe-PEG-PS or Fmoc-Asn(Trt)-PEG-PS resins, respectively, using an Applied Biosystems model 433A automatic peptide synthesizer and the standard procedures, as previously described (Chatenet et al, 2006;Quan et al, 2015). All Fmoc-amino acids (1 mmol, 10 eq.)…”

Section: Soccap2mentioning

confidence: 99%

Crustacean cardioactive peptides: Expression, localization, structure, and a possible involvement in regulation of egg-laying in the cuttlefish Sepia officinalis

Endress

Zatylny-Gaudin

Corre

et al. 2018

General and Comparative Endocrinology

Self Cite

View full text Add to dashboard Cite

The cuttlefish (Sepia officinalis) is a cephalopod mollusk distributed on the western European coast, in the West African Ocean and in the Mediterranean Sea. On the Normandy coast (France), cuttlefish is a target species of professional fishermen, so its reproduction strategy is of particular interest in the context of stock management. Egg-laying, which is coastal, is controlled by several types of regulators among which neuropeptides. The cuttlefish neuropeptidome was recently identified by Zatylny-Gaudin et al. (2016). Among the 38 neuropeptide families identified, some were significantly overexpressed in egg-laying females as compared to mature males. This study is focused on crustacean cardioactive peptides (CCAPs), a highly expressed neuropeptide family strongly suspected of being involved in the control of egg-laying. We investigated the functional and structural characterization and tissue mapping of CCAPs, as well as the expression patterns of their receptors. CCAPs appeared to be involved in oocyte transport through the oviduct and in mechanical secretion of capsular products. Immunocytochemistry revealed that the neuropeptides were localized throughout the central nervous system (CNS) and in the nerve endings of the glands involved in egg-capsule synthesis and secretion, i.e. the oviduct gland and the main nidamental glands. The CCAP receptor was expressed in these glands and in the subesophageal mass of the CNS. Multiple sequence alignments revealed a high level of conservation of CCAP protein precursors in Sepia officinalis and Loligo pealei, two cephalopod decapods. Primary sequences of CCAPs from the two species were fully conserved, and cryptic peptides detected in the nerve endings were also partially conserved, suggesting biological activity that remains unknown for the time being.

show abstract

Comparative Distribution and In Vitro Activities of the Urotensin II-Related Peptides URP1 and URP2 in Zebrafish: Evidence for Their Colocalization in Spinal Cerebrospinal Fluid-Contacting Neurons

Cited by 54 publications

References 72 publications

Pkd2l1 is required for mechanoception in cerebrospinal fluid-contacting neurons and maintenance of spine curvature

Pkd2l1 is required for mechanoception in cerebrospinal fluid-contacting neurons and maintenance of spine curvature

Loss of the Reissner Fiber and increased URP neuropeptide signaling underlie scoliosis in a zebrafish ciliopathy mutant

Crustacean cardioactive peptides: Expression, localization, structure, and a possible involvement in regulation of egg-laying in the cuttlefish Sepia officinalis

Contact Info

Product

Resources

About