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. 2019 Jun 18;14(6):e0216679.
doi: 10.1371/journal.pone.0216679. eCollection 2019.

Seasonal adaptations of the hypothalamo-neurohypophyseal system of the dromedary camel

Fatma Zohra Djazouli Alim  1   2 , Elena V Romanova  3 , Yea-Ling Tay  4 , Ahmad Yamin Bin Abdul Rahman  4 , Kok-Gan Chan  5   6 , Kar-Wai Hong  6 , Mark Rogers  7 , Bruce R Southey  8 , Michael P Greenwood  9 , Andre Souza Mecawi  10   11   12 , Mohammad Rais Mustafa  13 , Nicole Mahy  14 , Colin Campbell  7 , José Antunes-Rodrigues  12 , Jonathan V Sweedler  3 , David Murphy  9   11 , Charles C T Hindmarch  9   11   15
Affiliations

Seasonal adaptations of the hypothalamo-neurohypophyseal system of the dromedary camel

Fatma Zohra Djazouli Alim et al. PLoS One. .

Abstract

The "ship" of the Arabian and North African deserts, the one-humped dromedary camel (Camelus dromedarius) has a remarkable capacity to survive in conditions of extreme heat without needing to drink water. One of the ways that this is achieved is through the actions of the antidiuretic hormone arginine vasopressin (AVP), which is made in a specialised part of the brain called the hypothalamo-neurohypophyseal system (HNS), but exerts its effects at the level of the kidney to provoke water conservation. Interestingly, our electron microscopy studies have shown that the ultrastructure of the dromedary HNS changes according to season, suggesting that in the arid conditions of summer the HNS is in an activated state, in preparation for the likely prospect of water deprivation. Based on our dromedary genome sequence, we have carried out an RNAseq analysis of the dromedary HNS in summer and winter. Amongst the 171 transcripts found to be significantly differentially regulated (>2 fold change, p value <0.05) there is a significant over-representation of neuropeptide encoding genes, including that encoding AVP, the expression of which appeared to increase in summer. Identification of neuropeptides in the HNS and analysis of neuropeptide profiles in extracts from individual camels using mass spectrometry indicates that overall AVP peptide levels decreased in the HNS during summer compared to winter, perhaps due to increased release during periods of dehydration in the dry season.

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Conflict of interest statement

This research was funded in part by the Leverhulme Trust. Additionally, BioEasy Sdn Phd provided support in the form of salaries for authors Y-L.t. and AYbAR. There are no patents or products in development related to this manuscript. This does not alter our adherence to PLOS ONE policies on data and materials sharing.

Figures

Fig 1
Fig 1. Fine structure of magnocellular neurones.
(A, A') Electron microscopic observations of the dromedary SON revealed the presence of two distinct MN phenotypes—light (lMN) and dark (dMN). Light profiles are more abundant than dark. Other important elements found in the SON are myelinated axons (arrowheads). Glial cells (Gl) are observed in different levels of the HNS, and parenchymal glial cells are seen (A').
Fig 2
Fig 2. Ultrastructural description of SON magnocellular neurons and their subcellular elements in the somatic zone.
Light (lMN) and dark (dMN) magnocellular neurones are morphologically distinct. The nuclei of lMN (A) and dMN (A') are different in shape, respectively rounded and indented. However, both contain dense fibillary condensed (dfc) and granular chromatin (gc). The cytoplasm of the IMN is less loaded (asterisks in A) than that of the dMN. (B-B') Both lMN and dMN showed high activity as reflected by the presence of a well developed machinery of neurosecretion and recycling. Rough endoplasmic reticulum (RER), Golgi apparatus (G), mitochondrion (M), polyvesicular body (pv), lysosomes (ly) and dense core secretory granules (arrowheads; 195.71 nm ± 4.02 and 157.5nm ±3.65) are the main membranous structures found at the subcellular level of MNs. The rough endoplasmic reticulum (RER) was abundant and was present in different degree of dilation (B,C). The rectangle in panel (B) identifies several phagosomes (polyvesicular bodies) with vesicles of heterogeneous size. The Golgi apparatus is scattered as discontinuous (B) or well developed continuous (C). (D) Cluster of mitochondria (M) observed close to plasma membrane. (E) Lysosomes (ly) and autophagosomes (white asterisks), internalizing cytoplasmic membranous structures (black asterisks). (F) Polyvesicular bodies containing heterogeneous vesicles.
Fig 3
Fig 3. Cell populations and vasculature of supraoptic nucleus at the somatic zone.
(A, A') Parenchymal glial cells are distinguished as two groups: cells having smooth rounded nuclei and vesicles similar to lipid droplets (asterisk) (A) and cells with polylobed nuclei containing lipid droplets or endosomes in the cytoplasm (asterisk) (A'). (B)The supraoptic nucleus is richly vascularized. Capillaries (asterisks) are abundant and sometimes close to MNs. (B') Endothelial cells (light asterisks) and pericyte (dark asterisk) of capillaries. bl: basal lamina.
Fig 4
Fig 4. Electron micrographs illustrating the complex organisation of the supraoptic nucleus dendritic zone.
(A, B) Dendrites of magnocellular neurones are found with glial cells (Gl) and their processes (light asterisk in B). From these dendrites derive spines (dark arrowheads) that make synaptic contact with axons terminals (ax). Degenerating elements also are observed (dark asterisks in B). (C) A cluster of spines (square) near large dendrites (d). One appears with an apparent neck (asterisk) and head (S) making synaptic contact (arrowheads) with axon terminals (ax). (D) Two clusters of dendritic spines (s and s') organised in bundles and connected to presynaptic elements (arrowheads).
Fig 5
Fig 5. Structural membrane contacts of somatic zone magnocellular perikaryons.
Magnocellular neurones establish different types of membrane contact with other supraoptic nucleus elements. (A) Soma-somatic membrane apposition of two adjacent magnocelluar neurones (MN1 and MN2) without intervening neuropil elements; MN1 and MN2 membranes in close contact (arrows in magnified rectangle). Note the presence of active synapses on both MNs (dark arrows). Direct contact of magnocellular neurone membrane with the basal lamina (bl) of a capillary (light arrow). (B) Two adjacent magnocellular neurones (MN1 and MN2) membranes separated by neuropil elements (arrow in the square magnified). (C) Adjacent magnocellular neurones (MN1, MN2 and MN3) with direct soma-soma membrane apposition (white arrowheads between MN1 and MN2) and separated by neuropil elements in several places (dark arrowheads). (D) Direct contact of MN soma membrane with capillary basal lamina (bl) (arrow). (E) Blood barrier in the supraoptic nucleus demonstrating endothelial cells (asterisk) tightly linked (arrowhead) and magnocelluar neurone membrane separated from capillary basal lamina by glial process (Gl).
Fig 6
Fig 6. Common synaptic innervations types found in the supraoptic nucleus.
(A) Axo-somatic active synapses (arrowheads) were in contact with magnocellular neurones in an active functional stage, according to the cytoplasmic subcellular appearance, especially the dilated rough reticulum endoplasmic. (B) Axo-axonic synapse (arrowhead) (asterisk represents an magnocellular neurone axon). (C) Axo-dendritic synapse (arrowhead) (square magnified in the right) (asterisks represent a dendrite from a magnocellular neurone). (D) In the dendritic zone, multiple axo-dendritic synapses (arrowheads) (asterisk represents a dendrite from a magnocellular neurone) are seen. Note the dilation stage of rough reticulum endoplasmic reticulum (RER).
Fig 7
Fig 7
Debris and degenerating material in somatic zone of the supraoptic nucleus observed in summer (A, B and C) and winter (D) seasons. (A, B) Debris bodies are found in somatic zone (arrows) localised inside glial cells (arrows in B, and asterisk in rectangle magnified in the top left of B). (C, D) Large degenerative bodies (asterisks) observed between magnocellular neurones close to their membrane.
Fig 8
Fig 8. Debris material in supraoptic nucleus dendritic zone observed in summer and winter seasons.
(A) Degenerative elements (asterisks) are observed near magnocellular neurone spines and dendrites in both seasons. (B, C) These elements (asterisks) are generally abutted by glial processes (Gl) and engulfed (C). It seems that glial cells (Gl) are attracted to debris zones, and possibly remove them from the neuropil by phagocytosis. Note in B and C that glial cells are engulfing debris (asterisks).
Fig 9
Fig 9. Debris material in perivascular zones of the supraoptic nucleus observed in summer and winter seasons.
A-B) Cytoplasmic recycling material is observed in perivascular cells of the somatic zone. (C-E) Debris bodies (asterisks) are also found close to capillaries, engulfed or inside glial cells (Gl). bl: basal lamina; MN: magnocellular neurone.
Fig 10
Fig 10. Quantitative analysis of dromedary SON parameters comparing winter and summer.
(A) Statistical analysis of capillary parameters (18 capillaries from 3 slices from 3 animals for each season). Ca: area of lumen; BLt: thickness of basal lamina (dashed line); Fn: number of fenestrations (in pink); Fa area of fenestrations. ** Significant seasonal variations (p < 1%). (B) Statistical analysis of synapse parameters (32 synapses from 3 slices from 3 animal for each season). SMAl: synaptic membrane apposition length (dashed lines in pink); PSDl: post-synaptic density length (dashed lines in white); PSDa: post-synaptic density-area (dense area at the side of magnocellular (MN) cell body membrane). * Significant seasonal variations (p < 5%). (C) Statistical analysis of number and kind of debris: DBn: number of degenerating bodies; DAn: number of degenerating axons. ***High significant seasonal variations (p < 0.01%). DA: degenerating body; DA: degenerating axon. F: fenestration; bl: basal lamina; MN: magnocellular neurone; L: lumen.
Fig 11
Fig 11
Electron micrographs showing ultrastructural differences in capillary (cp) basal lamina (bl) between winter (A) and summer (B). Note the differences in thickness and fenestration (outlined in pink). Note differences between seasons in cytoplasmic expansions (arrowheads) and thickness of endothelial cells (EC).
Fig 12
Fig 12. Characterization of a dromedary camel POMC prohormone.
(A) Translated protein sequence, predicted signal peptide shown in lowercase letters, confirmed cleavage sites shown in green, confirmed amidation sites shown in blue, peptides detected by MALDI TOF MS underlined. (B) Phylogenetic tree for POMC prohormones from human (P01189), cow (P01190), ship (P01191) and a novel camel sequence that all share 75% identity. This tree was produced using CLUSTALO pairwise alignments and neighbor joining method. Camel POMC shares 89.4% identity with sheep, 88.3% with cow, and 79.3% with human POMC prohormones. Representative MALDI TOF mass spectra of individual camel pituitary extracts. (C) Full mass range spectrum from a summer sample, peaks matching the masses of predicted peptides are labelled (Table 1); (D) Zoom-in view showing differential detection of neurotensin, melanotropin alpha, α-MSH, and its post-translationally modified forms depending on the season. Labels: W, winter; S, summer.
Fig 13
Fig 13. Seasonal peptide level change in camel supraoptic nucleus and neurointermediate lobe.
(A) Signal intensity changes of select peptide ions in camel supraoptic nucleus at different seasons. Labels: AVP, arginine vasopressin; OT, oxytocin. (B) Principal component analysis plot for the first three principal components (PC) allows discrimination between seasonal supraoptic nucleus samples based on peptide profile change, S1-S3, summer samples; W1-W4, winter samples, W3 samples is an incorrectly isolated sample. (C) Signal intensity changes of AVP ions in camel neurointermediate lobe at different seasons. Labels: AVP, arginine vasopressin. (D) Principal component analysis plot for the first three principal components (PCs) allows discrimination between seasonal neurointermediate lobe samples based on peptide profile change. S1-S3, summer samples; W1-W4, winter samples.
Fig 14
Fig 14. Circulating plasma AVP and OT levels are unchanged with season in hydrated males dromedary camels as determined by radioimmunoassay.
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