Zebrafish Models of Neurodevelopmental Disorders: Limitations and Benefits of Current Tools and Techniques
Abstract
:1. Introduction
2. Zebrafish Central Nervous System Development and Organization
2.1. CNS Morphogenesis
2.2. Neuronal Subclasses
3. Genetic Tools for Investigating Neuronal Development and Function
3.1. Knockdown Techniques
3.2. Transgene Overexpression
3.3. Stable Mutagenesis
4. Assays
4.1. Cellular Characterization
4.2. Behavior Characterization
4.2.1. Larvae Assays
4.2.2. Adult Assays
Learning Tests
Anxiety/Fear Tests
Social Interaction Tests
5. Zebrafish Models of Human Neurodevelopmental Disorders
6. Therapies
7. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
ADHD | attention deficit hyperactivity disorder |
ASD | autism spectrum disorder |
C | cerebellum |
CAM | cameleon |
CNS | central nervous system |
CNV | copy number variation |
CRISPR | clustered regularly interspaced short palindromic repeats |
D | diencephalon |
DD | developmental delay |
DPF | days post fertilization |
GFP | green fluorescent protein |
GLRA2 | glycine receptor alpha 2 |
GlyR | glycine receptor |
ID | intellectual disability |
M | midbrain |
MHB | midbrain-hindbrain boundary |
MO | morpholino |
MPEP | 2-methyl-6-(phenylethynyl)pyridine |
MPH | methylphenidate |
H: | hindbrain |
HA | habenula |
HPF | hours post fertilization |
HYP | hypothalamus |
OB | olfactory bulb |
ON | optic nerve |
ORR | optic recess region |
OV | otic vesicle |
PAL | pallium |
PB | pineal body |
PFOS | perfluorooctane sulfonate |
PTZ | pentylenetetrazol |
R | retina |
RFP | red fluorescent protein |
r1–r7 | rhombomeres 1 to 7 |
SUB | sub-pallium |
T | telencephalon |
TEG | tegmentum |
UV | ultra violet |
VPA | valproic acid |
YFP | yellow fluorescent protein |
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Line | Promoter | Features | Cells Tagged | References |
---|---|---|---|---|
Tg(alx:Kaede) | alx (human CHX10) | Kaede converts from green to red after UV radiation; cell tracking | In spinal cord: ipsilateral descending neurons, glutamatergic (V2a neurons) | [71] |
Tg(alx:GFP) | GFP expression | |||
Tg(atoh1a:EGFP) | atonal bHLH transcription factor 1a | GFP expression | Cerebellum (glutamatergic neurons) and tegmentum cells (cells connecting to the hypothalamus and optic tectum) | [72] |
Tg(barhl2:GFP) | barh-like homeobox 2 promoter | GFP expression | Neurons at the dorso-lateral edge of the hindbrain and spinal cord | [73] |
Tg(dbx1b:GFP) | developing brain homeobox 1b promoter | GFP expression | Early neuronal marker, expressed in a population of glutamatergic and glycinergic neurons in the hindbrain | [73,74] |
Tg(dbx1b:loxP-DsRed-loxP-GFP) | Conditional system, depending on cre expression | |||
Tg(dbx1b:Cre) | cre recombinase expression | |||
Tg(eng1b:eng-GFP); Tg(hsp70:eng-GFP) | engrailed 1 | Expression of fusion eng-GFP protein, drived by endogenous (eng1b) or heat shock (hsp70) promoter | In spinal cord: ipsilateral gylcinergic interneurons (circumferencial ascending interneurons), V1 neurons | [75] |
Tg(evx1:GFP) | even-skipped homeobox 1 | GFP expression | In spinal cord: commissural interneurons, ventral projections from the spinal cord | [76] |
Tg(gad1b:RFP) | glutamic acid decarboxylase | RFP expression | GABAergic neurons | [74,77] |
Tg(gad1b:loxP-DsRed-loxP-GFP) | Conditional system, depending on cre expression | |||
Tg (gfap:GFP) | glial fibrillary acidic protein | GFP expression | Neural stem cells throughout the brain, retina, hindbrain, and spinal cord | [74,78] |
Tg (gfap:dTomato) | dTomato expression | |||
Tg(glyt2:GFP); Tg(glyt2:RFP) | glycine transporter-2 promoter | GFP or RFP expression | Glycinergic neurons | [74,77,79] |
Tg(glyt2:loxP-DsRed-loxP-GFP) | Conditional system, depending on cre expression | |||
Tg(vglut2a:GFP) | glutamate transporter promoter | GFP expression | Glutamatergic neurons | [37,74] |
Tg(vglut2a:loxP-DsRed-loxP-GFP) | Conditional system, depending on cre expression | |||
Tg(hb9:GFP) | motor neuron and pancreas homeobox 1 (mnx1), previously known as hb9 | GFP expression | In spinal cord: motor neurons and interneurons | [76] |
Tg(HuC:CAM) | HuC (or elav3, ELAV like neuron-specific RNA binding protein 3) | cameleon expression (calcium indicator derivative from GFP) | Early neuronal marker; spinal cord: glycinergic interneurons | [74,75,80,81,82,83] |
Tg(HuC:Ckaede) | Kaede converts from green to red after radiation with UV; cell tracking | |||
Tg(HuC:GFP) Tg(HuC:RFP) | GFP or RFP expression | |||
Tg(HuC:loxP-DsRed-loxP-GFP) | Conditional system, depending on cre expression | |||
Tg(hox9a:Cre) | homeobox 9 | cre recombinase expression | Spinal cord neurons | [74] |
Tg(isl1:GFP) | LIM/homeobox 1 | GFP expression | Ubiquitous motor neurons | [76,84] |
Tg(lhx2a:GFP) | LIM Homeobox 2a | GFP expression | Olfactory bulb neurons | [14] |
Tg(lhx2a:gap:YFP) | gap: membrane signal, YFP will be found in the cell membrane | |||
Tg(NBT:GCaMP3) | neural beta-tubulin | GCaMP3: calcium reporter, allows live imaging of neuronal activity | Ubiquitous neuronal cells | [85] |
Tg(nestin:GFP) | nestin | GFP expression | Ubiquitous neural stem cells | [86] |
Tg(ngn1:GFP); Tg(neurog1:RFP) | neurogenin1 | GFP or RFP expression | In spinal cord: Rohon Beard and dorsal root ganglia neurons | [76,77] |
Tg(olig2:EGFP) | oligodendrocyte lineage transcription factor 2 | GFP expression | Oligodendrocytes, spinal cord motor neurons, and cerebellum cells | [37,87] |
Tg(ptf1a:EGFP) | pancreas associated transcription factor 1a | GFP expression | Purkinje cells and telencephalon’s ventricular zone | [72] |
Tg(tub:CAM) | golfish neural tubulin | CAM: cameleon expression (calcium indicator derivative from GFP) | In spinal cord: ipsilateral glycinergic interneurons (circumferential ascending interneurons) | [75] |
GFP/tRFP-ki | otx2 | knock-in of fluorescent tag | Retina, midbrain, MHB expression | [88] |
venus/tRFP-ki | pax2a | knock-in of fluorescent tag | MHB and otic vesicle expression |
Gene | Human Disorder | Technique | Observations | Reference |
---|---|---|---|---|
16p11.2 CNV; kctd13 | ASD, ID | Splice block and translation MO, RNA overexpression | Overexpression of kctd13: microcephaly caused by decreased proliferation and increased apoptosis; kockdown of kctd13: macrocephaly caused by increased proliferation; knockdown several genes in 16p11.2 region results in neural tube and axon morphogenesis defects | [155,156] |
auts2 (autism susceptibility candidate 2) | ASD, ADHD, DD, epilepsy | Translation and splice block MO | Smaller body size; severe decrease in the number of neurons in the brain, retina, and spinal cord. Touch evoked response assay showed decreased response from MO-injected larvae | [145] |
chd8 (chromodomain helicase DNA binding protein 8) | ASD, DD | Splice block MO | Increased head size, with increased number of midbrain and forebrain progenitors | [149,150] |
cntnap2 (contactin associated protein-like 2) | ASD | Zinc fingers | Decrease in GABAergic cells in the pallium and cerebellum, increased seizures when exposed to PTZ; increased nighttime activity | [153] |
ctnnd2 (delta catenin) | ASD, ID | Splice block MO | Gastrulation defects; co-injection with wt or mutant ctnnd2 fully (wt) or partially (mutant) rescues phenotype; abnormal neuronal patterning, with ectopic Isl1-positive cells in the optic recess region | [157,158] |
c8orf37 (chromosome 8 open reading frame 37) | Bardet Biedl syndrome, ASD | Translation and splice block MO | Abnormal response to visual motor response test; co-injection with wt mRNA rescues phenotype, co-injection with mutant mRNA not able to rescue the phenotype | [159] |
dyrk1a (dual-specificity tyrosine-(Y)-phosphorylation regulated kinase 1A) | Down syndrome, ASD, ID | TALENs | Adult mutants present with microcephaly, possibly due to cell death, and reduced neuronal activation (c-fos expression) in the hypothalamus, and reduced expression of chr (corticotrophin-releasing hormone) in the preoptic region; novel tank test revealed shorter freezing time and increased exploration; social interaction test showed mutant specimen spending less time close to interaction fish | [148] |
fmr (fragil x mental retardation) | Fragile X syndrome, learningand cognitive deficits, ADHD, ASD | Translation block MO, ENU mutagenesis | MO injection: patterning defects of the forebrain and MHB; hindbrain oedema; spinal cord neurites with increased branching; co-injection with fmr1 mRNA or MPEP rescues the phenotypes. Knock-out studies: embryos show no phenotypes (possible compensation mechanism?); open field test on adult zebrafish showed decreased freezing | [131,152,160,161] |
glra2 (glycine receptor alpha 2) | ASD | Translation block MO | Hyperbranching of spinal motor neuron axons; co-injection with wt GLRA2 rescues phenotype, while co-injection with mutant RNA fails to rescue | [6] |
lphn3.1 (latrophilin 3) | ADHD | Splice block MO | MO-injected embryos swim longer distances in an un-evoked swimming assay; neuron quantification showed a reduction in the number and a general disorganization of the dopaminergic neurons; behavioral phenotype can be rescued by exposure to ADHD treatment drugs methylphenidate and atomoxetine | [162] |
mecp2 (methyl-CpG-binding protein 2) | ASD, Rett syndrome | Translation and splice block MOs; ENU mutagenesis | MO studies: abnormal neuronal branching and growth of motor neurons; touch-evoked response assay showed a slower response. Mutant studies: touch-evoked response assay showed that mutant larvae have a prolonged coiling response and swimming behavior at later stages shows a reduced in spontaneous activity | [163,164] |
met (tyrosine kinase receptor) | ASD | Translation block MO | Reduction of the cerebellum size by reduced proliferation, impairs migration of hindbrain facial motor neurons | [165] |
nbea (neurobeachin) | ASD | ENU mutagenesis | Loss of GlyR in both hindbrain and spinal cord, reduced dendritic complexity, and defects in glycinergic synaptogenesis; startle response test shows that mutant larvae respond in only 50% of the trials | [154] |
shank3b (sh3 and multiple ankyrin repeat protein 3) | ASD and ID | Splice block MO; CRISPR/Cas9 | MO studies: affected brain patterning; reduction of GABAergic and glutamatergic neurons in the mid and hindbrain; touch-evoked response is impaired. Stable mutant studies: swimming behavior and visual motor response test showed a decrease in response in larvae and adults; embryonic brain shows a decrease in the huc-positive cells, this difference becomes smaller throughout development | [83,166,167] |
syngap1 (synaptic ras GTPase activating protein) | ASD and ID | Splice block MO | Brain patterning affected; reduction of GABAergic and glutamatergic neurons in the mid and hindbrain; touch-evoked response is impaired in morphant larvae, with reduced swim speed | [167] |
trappc6b (trafficking protein particle complex 6b) | Microcephaly, epilepsy, ASD | Translation and splice block MO | Decreased head size due to increased apoptosis, increased spontaneous neuron firing and activity | [151] |
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Vaz, R.; Hofmeister, W.; Lindstrand, A. Zebrafish Models of Neurodevelopmental Disorders: Limitations and Benefits of Current Tools and Techniques. Int. J. Mol. Sci. 2019, 20, 1296. https://doi.org/10.3390/ijms20061296
Vaz R, Hofmeister W, Lindstrand A. Zebrafish Models of Neurodevelopmental Disorders: Limitations and Benefits of Current Tools and Techniques. International Journal of Molecular Sciences. 2019; 20(6):1296. https://doi.org/10.3390/ijms20061296
Chicago/Turabian StyleVaz, Raquel, Wolfgang Hofmeister, and Anna Lindstrand. 2019. "Zebrafish Models of Neurodevelopmental Disorders: Limitations and Benefits of Current Tools and Techniques" International Journal of Molecular Sciences 20, no. 6: 1296. https://doi.org/10.3390/ijms20061296
APA StyleVaz, R., Hofmeister, W., & Lindstrand, A. (2019). Zebrafish Models of Neurodevelopmental Disorders: Limitations and Benefits of Current Tools and Techniques. International Journal of Molecular Sciences, 20(6), 1296. https://doi.org/10.3390/ijms20061296