Colloidal structure and proton conductivity of the gel within the electrosensory organs of cartilaginous fishes

Phillips, Molly; Wheeler, Alauna C.; Robinson, Matthew J.; Leppert, Valerie J.; Jia, Manping; Rolandi, Marco; Hirst, Linda S.; Amemiya, Chris T.

doi:10.1016/j.isci.2021.102947

Cited by 3 publications

(3 citation statements)

References 37 publications

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“…Keratan sulfates endow AoL gel with high conductivity [ 3 , 7 , 46 ]. Carbohydrates form globular aggregates in the hydrogel [ 47 ]. We attempted to label Polyodon AO gel with two different polyclonal antibodies to human mucins (Abcam, genes MUC1, MUC2), with negative results (perhaps explained by species differences).…”

Section: Discussionmentioning

confidence: 99%

Lectin binding and gel secretion within Lorenzinian electroreceptors of Polyodon

et al. 2022

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We imaged the carbohydrate-selective spatial binding of 8 lectins in the ampullary organs (AOs) of electroreceptors on the rostrum of freshwater paddlefish (Polyodon spathula), by fluorescence imaging and morphometry of frozen sections. A focus was candidate sites of secretion of the glycoprotein gel filling the lumen of AOs. The rostrum of Polyodon is an electrosensory appendage anterior of the head, covered with >50,000 AOs, each homologous with the ampulla of Lorenzini electroreceptors of marine rays and sharks. A large electrosensory neuroepithelium (EN) lines the basal pole of each AO’s lumen in Polyodon; support cells occupy most (97%) of an EN’s apical area, along with electrosensitive receptor cells. (1) Lectins WGA or SBA labeled the AO gel. High concentrations of the N-acetyl-aminocarbohydrate ligands of these lectins were reported in canal gel of ampullae of Lorenzini, supporting homology of Polyodon AOs. In cross sections of EN, WGA or SBA labeled cytoplasmic vesicles and organelles in support cells, especially apically, apparently secretory. Abundant phalloidin+ microvilli on the apical faces of support cells yielded the brightest label by lectins WGA or SBA. In parallel views of the apical EN surface, WGA labeled only support cells. We concluded that EN support cells massively secrete gel from their apical microvilli (and surface?), containing amino carbohydrate ligands of WGA or SBA, into the AO lumen. (2) Lectins RCA120 or ConA also labeled EN support cells, each differently. RCA120-fluorescein brightly labeled extensive Golgi tubules in the apical halves of EN cells. ConA did not label microvilli, but brightly labeled small vesicles throughout support cells, apparently non-secretory. (3) We demonstrated “sockets” surrounding the basolateral exteriors of EN receptor cells, as candidate glycocalyces. (4) We explored whether additional secretions may arise from non-EN epithelial cells of the interior ampulla wall. (5) Model: Gel is secreted mainly by support cells in the large EN covering each AO’s basal pole. Secreted gel is pushed toward the pore, and out. We modeled gel velocity as increasing ~11x, going distally in AOs (toward the narrowed neck and pore), due to geometrical taper of the ampulla wall. Gel renewal and accelerated expulsion may defend against invasion of the AO lumen by microbes or small parasites. (6) We surveyed lectin labeling of accessory structures, including papilla cells in AO necks, striated ectoderm epidermis, and sheaths on afferent axons or on terminal glia.

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Section: Discussionmentioning

confidence: 99%

Lectin binding and gel secretion within Lorenzinian electroreceptors of Polyodon

et al. 2022

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“…2003 ) is also a component of this complex as is another unidentified GAG binding protein. Subsequent studies showed this electrosensory gel was an ultrasensitive proton binding complex and the most sensitive proton detection system known in nature ( Phillips et al. 2021 ).…”

Section: The Electrosensory Gel Of the Ampoules Of Lorenzinimentioning

confidence: 99%

Keratan sulfate, an electrosensory neurosentient bioresponsive cell instructive glycosaminoglycan

Melrose

2024

Glycobiology

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The roles of keratan sulfate (KS) as a proton detection glycosaminoglycan in neurosensory processes in the central and peripheral nervous systems is reviewed. The functional properties of the KS-proteoglycans aggrecan, phosphacan, podocalyxcin as components of perineuronal nets in neurosensory processes in neuronal plasticity, cognitive learning and memory are also discussed. KS-glycoconjugate neurosensory gels used in electrolocation in elasmobranch fish species and KS substituted mucin like conjugates in some tissue contexts in mammals need to be considered in sensory signalling. Parallels are drawn between KS’s roles in elasmobranch fish neurosensory processes and its roles in mammalian electro mechanical transduction of acoustic liquid displacement signals in the cochlea by the tectorial membrane and stereocilia of sensory inner and outer hair cells into neural signals for sound interpretation. The sophisticated structural and functional proteins which maintain the unique high precision physical properties of stereocilia in the detection, transmittance and interpretation of acoustic signals in the hearing process are important. The maintenance of the material properties of stereocilia are essential in sound transmission processes. Specific, emerging roles for low sulfation KS in sensory bioregulation are contrasted with the properties of high charge density KS isoforms. Some speculations are made on how the molecular and electrical properties of KS may be of potential application in futuristic nanoelectronic, memristor technology in advanced ultrafast computing devices with low energy requirements in nanomachines, nanobots or molecular switches which could be potentially useful in artificial synapse development. Application of KS in such innovative areas in bioregulation are eagerly awaited.

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“…Recently, chitin, long assumed to be absent from vertebrates, has been shown to be endogenously produced in fishes and amphibians [7,8]. Intriguingly, some gastropod mollusk epidermal chitin and vertebrate chitin are present outside of hard skeletal tissues (e.g., as a component of the gel-like substance in ampullae of Lorenzini in skates) [8][9][10], demonstrating that this glycopolymer is utilized in more diverse contexts than previously realized.…”

Section: Introductionmentioning

confidence: 96%

Unexpected Distribution of Chitin and Chitin Synthase across Soft-Bodied Cnidarians

et al. 2023

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Cnidarians are commonly recognized as sea jellies, corals, or complex colonies such as the Portuguese man-of-war. While some cnidarians possess rigid internal calcareous skeletons (e.g., corals), many are soft-bodied. Intriguingly, genes coding for the chitin-biosynthetic enzyme, chitin synthase (CHS), were recently identified in the model anemone Nematostella vectensis, a species lacking hard structures. Here we report the prevalence and diversity of CHS across Cnidaria and show that cnidarian chitin synthase genes display diverse protein domain organizations. We found that CHS is expressed in cnidarian species and/or developmental stages with no reported chitinous or rigid morphological structures. Chitin affinity histochemistry indicates that chitin is present in soft tissues of some scyphozoan and hydrozoan medusae. To further elucidate the biology of chitin in cnidarian soft tissues, we focused on CHS expression in N. vectensis. Spatial expression data show that three CHS orthologs are differentially expressed in Nematostella embryos and larvae during development, suggesting that chitin has an integral role in the biology of this species. Understanding how a non-bilaterian lineage such as Cnidaria employs chitin may provide new insight into hitherto unknown functions of polysaccharides in animals, as well as their role in the evolution of biological novelty.

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Colloidal structure and proton conductivity of the gel within the electrosensory organs of cartilaginous fishes

Cited by 3 publications

References 37 publications

Lectin binding and gel secretion within Lorenzinian electroreceptors of Polyodon

Lectin binding and gel secretion within Lorenzinian electroreceptors of Polyodon

Keratan sulfate, an electrosensory neurosentient bioresponsive cell instructive glycosaminoglycan

Unexpected Distribution of Chitin and Chitin Synthase across Soft-Bodied Cnidarians

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