Differential response of olfactory sensory neuron populations to copper ion exposure in zebrafish

Lazzari, Maurizio; Bettini, Simone; Milani, Liliana; Maurizii, Maria Gabriella

doi:10.1016/j.aquatox.2016.12.012

Cited by 26 publications

(40 citation statements)

References 86 publications

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“…In the current study, we used transgenic zebrafish with confocal imaging and phenotypic anchoring of olfactory behavior to better understand cellular mechanisms of Cu olfactory injury and recovery of specific neuron populations. In this regard, previous studies of toxic effects of metals on the olfactory sensory epithelium offish generally relied on histology, immunostaining, scanning electron microscopy (SEM), and behavioral studies (Dew et al, 2014; Haverroth et al, 2015; Heffern et al, 2018; Lazzari et al, 2017; Williams et al, 2016) to distinguish between the various OSN populations. However, imaging of histological and/or immunostained tissue sections can yield low cellular-level resolution and difficulty in distinguishing different cell types that are interspersed within the olfactory sensory epithelium (Lazzari et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…Similar to other vertebrates, zebrafish olfaction is functional at early stages of development (4 days postfertilization, dpf) and mediates behavioral and survival strategies in the developing larvae (Lindsay and Vogt, 2004). These attributes make zebrafish an excellent model system to study Cu olfactory injury (Lazzari et al, 2017; Tilton et al, 2008, 2011) and to investigate the cellular targets and recovery from metal exposures. In the present study, we analyzed Cu-induced injury and recovery of the two major OSN populations using confocal imaging of double-transgenic ( Tg ) zebrafish larvae (Lakhina et al, 2012; Miyasaka et al, 2005; Sato et al, 2005, 2007) that express both red fluorescent protein (RFP) in the ciliated OSNs under the control of the OMP promoter ( OMP:RFP ), and Venus in the microvillous OSNs driven by the TRPC2 promoter ( TRPC2:Venus ) (Lakhina et al, 2012; Miyasaka et al, 2005; Sato et al, 2005, 2007).…”

Section: Introductionmentioning

confidence: 99%

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Differential copper-induced death and regeneration of olfactory sensory neuron populations and neurobehavioral function in larval zebrafish

Heffern

Cheresh

et al. 2018

NeuroToxicology

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Fish rely heavily on their sense of smell to maintain behaviors essential for survival, such as predator detection and avoidance, prey selection, social behavior, imprinting, and homing to natal streams and spawning sites. Due to its direct contact with the outside environment, the peripheral olfactory system of fish is particularly susceptible to dissolved contaminants. In particular, environmental exposures to copper (Cu) can cause a rapid loss of olfactory function. In this study, confocal imaging of double-transgenic zebrafish larvae with differentially labeled ciliated and microvillous olfactory sensory neurons (OSNs) were used to examine cell death and regeneration following Cu exposure. Changes in cell morphologies were observed at varying degrees within both ciliated and microvillous OSNs, including the presence of round dense cell bodies, cell loss and fragmentation, retraction or loss of axons, disorganized cell arrangements, and loss of cells and fluorescence signal intensity, which are all indicators of cell death after Cu exposure. A marked loss of ciliated OSNs relative to microvillous OSNs occurred after exposure to low Cu concentrations for 3 hours, with some regeneration observed after 72 hours. At higher Cu concentrations and 24-h exposures, ciliated and microvillous OSNs were damaged with increased severity of injury with longer Cu exposures. Interestingly, microvillous, but not ciliated OSNs, regenerated rapidly within the 72-h time period of recovery after death from Cu exposure, suggesting that microvillous OSNs may be replaced in lieu of ciliated OSNs. An increase in bromodeoxyuridine labeling was observed 24 h after Cu-induced OSN death, suggesting that increased proliferation of the olfactory stem cells replaced the damaged OSNs. Olfactory behavioral analyses supported our imaging studies and revealed both initial loss and restoration of olfactory function after Cu exposures. In summary, our studies indicate that following zebrafish OSN damage by Cu, regeneration of microvillous OSNs may occur exceeding ciliated OSNs, likely via increased proliferation of the cellular reservoir of neuronal OSC precursors. Transgenic zebrafish are a valuable tool to study metal olfactory injury and recovery and to characterize sensitive olfactory neuron populations in fish exposed to environmental pollutants.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Differential copper-induced death and regeneration of olfactory sensory neuron populations and neurobehavioral function in larval zebrafish

Heffern

Cheresh

et al. 2018

NeuroToxicology

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“…The genotoxic effect of the polluted environment in fishes (e.g., Lazzari et al 2017Lazzari et al , 2019 and bivalves was investigated applying different programs. In bivalve, for example, although a lot of genotoxicity biomarkers were examined in marine mussels, only a limited number were verified on a broad range of laboratory and field conditions (Dixon et al 2002).…”

Section: Introductionmentioning

confidence: 99%

Cell cultures of the Manila clam and their possible use in biomonitoring and species preservation

Attaallah

Marchionni

El-Beltagy

et al. 2020

The European Zoological Journal

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A huge progress has been achieved in mammalian in vitro technique. Instead, of the many trials to develop marine invertebrate cell cultures, only a few have obtained them and only from few tissues. Since in vitro cell culture of invertebrates could be very useful for many aspects of basic and applied science, in this work we investigate and describe the development of a technique for the establishment of cell cultures from gill, mantle and gonadic tissue of the Manila clam (Ruditapes philippinarum). We maintained viable cultures for up to 25 days. Culture viability and proliferation were tested with 3-(4,5-Dimethylthiazol-2-yl)-2,5-Diphenyltetrazolium Bromide (MTT) and with trypan blue, while an antibody against the ATP-dependent RNA helicase VASA, a protein expressed in the germline, and in multipotent stem cells of some animals, was used to verify the presence of these cell types. Following the described protocol: 1) explant resulted the better source to obtain cell cultures, when compared to enzymatic dissociation; 2) cultures of suspended cells were viable for longer period than adherent cells; 3) cell cultures obtained from tissues sampled in September-October performed better compared to other periods of the year, regarding maintenance and growth; 4) the tissue from which we obtained longer-lived cell cultures was gonadic tissue, especially form samples that show more undifferentiated germ cells and more VASA-stained cells. This study describes the challenges concerning the development of in vitro culture techniques for aquatic invertebrates.

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“…These olfactory alterations correlate with a long-term decrease in alarm and avoidance responses [88,114,115,116,117,118,119]. Exposure to Copper (Cu) causes marked OSN death, with a preferential loss of ciliated in comparison to microvillous OSNs; impairs the transcription of a wide variety of genes involved in olfactory processing, such as ORs and ionic channels; and reduces the recognition of bile salts while impairing odor-mediated alarm responses [120,121,122,123,124]. Cobalt (Co) is a naturally occurring and essential metal at low concentrations, but it is an environmental contaminant when found in high concentrations.…”

Section: The Olfactory System Of Zebrafish As a Model Of Neuroplasmentioning

confidence: 99%

“…In control conditions, OSNs present a constant turnover rate and most proliferation occurs in discrete clusters located in the apex of the lamellae [13,38,40,152]. Following damage to the olfactory organ, cellular proliferation is increased and localized in broader regions on the olfactory epithelium, giving rise to a rapid recovery of olfactory organ size and function [18,123,124]. Newly generated OSNs can reinnervate the olfactory bulb in their corresponding glomeruli and make synaptic connections with mitral cells.…”

Section: The Olfactory System Of Zebrafish As a Model Of Neuroplasmentioning

confidence: 99%

The Olfactory System of Zebrafish as a Model for the Study of Neurotoxicity and Injury: Implications for Neuroplasticity and Disease

Calvo-Ochoa

Byrd-Jacobs

2019

IJMS

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The olfactory system, composed of the olfactory organs and the olfactory bulb, allows organisms to interact with their environment and through the detection of odor signals. Olfaction mediates behaviors pivotal for survival, such as feeding, mating, social behavior, and danger assessment. The olfactory organs are directly exposed to the milieu, and thus are particularly vulnerable to damage by environmental pollutants and toxicants, such as heavy metals, pesticides, and surfactants, among others. Given the widespread occurrence of olfactory toxicants, there is a pressing need to understand the effects of these harmful compounds on olfactory function. Zebrafish (Danio rerio) is a valuable model for studying human physiology, disease, and toxicity. Additionally, the anatomical components of the zebrafish olfactory system are similar to those of other vertebrates, and they present a remarkable degree of regeneration and neuroplasticity, making it an ideal model for the study of regeneration, reorganization and repair mechanisms following olfactory toxicant exposure. In this review, we focus on (1) the anatomical, morphological, and functional organization of the olfactory system of zebrafish; (2) the adverse effects of olfactory toxicants and injury to the olfactory organ; and (3) remodeling and repair neuroplasticity mechanisms following injury and degeneration by olfactory toxicant exposure.

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Differential response of olfactory sensory neuron populations to copper ion exposure in zebrafish

Cited by 26 publications

References 86 publications

Differential copper-induced death and regeneration of olfactory sensory neuron populations and neurobehavioral function in larval zebrafish

Differential copper-induced death and regeneration of olfactory sensory neuron populations and neurobehavioral function in larval zebrafish

Cell cultures of the Manila clam and their possible use in biomonitoring and species preservation

The Olfactory System of Zebrafish as a Model for the Study of Neurotoxicity and Injury: Implications for Neuroplasticity and Disease

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