The Neurotoxic Effect of Environmental Temperature Variation in Adult Zebrafish (Danio rerio)
Abstract
:1. Introduction
2. Results
2.1. Common Protein Networks Involved in the Neurotoxicity Induced by Thermal Stress and the Alteration of BDNF Expression
2.2. Common Proteins Involved in Temperature-Induced Neurotoxicity
2.3. Neurotoxicity Associated with Anxiety-like or Boldness Behaviour
2.4. Upstream Regulators’ Analysis
3. Discussion
3.1. Common Proteins Involved in Temperature-Induced Neurotoxicity
3.2. Analysis of Upstream Regulators
3.3. Neurotoxicity Associated with Anxiety-like or Boldness Behaviour
4. Materials and Methods
4.1. Thermal Treatment and Behavioural Analysis Performed in Previous Studies
4.2. IPA Tox Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Tox Functions Related to Neurotoxicity (p Value ≤ 0.05) (From Table S9) | |||||||||
---|---|---|---|---|---|---|---|---|---|
18 °C vs. 26 °C (A) | 18 °C vs. 26 °C (C) | 34 °C vs. 26 °C (A) | 34 °C vs. 26 °C (C) | KO26 °C vs. WT26 °C | HT26 °C vs. WT26 °C | KO34 °C vs. WT34 °C | HT34 °C vs. WT34 °C | ||
Neurological Disease | X | X | X | X | X | X | X | X | |
Nervous System Development and Function | X | X | X | X | X | X | X | X | |
Psychological Disorders | X | X | |||||||
Functions related to neurological disease and nervous system development with a significant activation, Z score (From Table S10) | |||||||||
Movement disorders | Generalized seizures, environmental induced seizure, tonic-clonic seizure | ↑ | ↑ | ↑ | ↑ | ↑ | |||
Coordination | ↓ | ↓ | ↓ | ↓ | |||||
Movement Disorders, ataxia, convulsion | ↑ | ↑ | ↑ | ||||||
Myoclonus | ↑ | ||||||||
Alteration of nervous system development | MorphoGenesis of nervous tissue, synapse formation | ↓ | ↓ | ↓ | |||||
NeuritoGenesis, growth of neurites, neuronal cells proliferation | ↓ | ↓ | ↓ | ||||||
Transport of synaptic vesicles | ↑ | ||||||||
Endocytosis of synaptic vesicles | ↑ | ↓ | |||||||
Degeneration of neurons, encephalopathy | ↑ | ↑ | |||||||
Brain tumour | ↓ | ||||||||
Brain lesion | ↓ | ||||||||
Common hallmarks of neurotoxicity induced by thermal stress and alteration of BDNF expression | |||||||||
Alteration of synapse formation and neuronal projections | X | X | X | X | X | X | X | X | |
Alteration of calcium homeostasis | X | X | X | X | X | X | X | X | |
Alteration of mitochondria and energy metabolism | X | X | X | X | X | X | X | X |
Gene (Human) | Gene Symbol (Danio rerio) | Ensembl Gene ID (Danio rerio) | Protein Name | Occurrence in 377 Terms/Categories | % Occurrence |
---|---|---|---|---|---|
PPP3CA | ppp3cb | ENSDARG00000025106 | protein phosphatase 3 catalytic subunit alpha | 169 | 45 |
ppp3ca | ENSDARG00000004988 | ||||
L1CAM | l1camb | ENSDARG00000015025 | cell adhesion molecule L1 Like | 132 | 35 |
l1cama | ENSDARG00000007149 | ||||
CAMK2A | camk2a | ENSDARG00000053617 | calcium/calmodulin dependent protein kinase II alpha | 128 | 34 |
CACNA2D2 | cacna2d2a | ENSDARG00000103390 | calcium voltage-gated channel auxiliary subunit alpha 2 delta 2 | 127 | 34 |
DNM1L | dnm1l | ENSDARG00000015006 | dynamin 1 Like | 126 | 33 |
SLC2A1 | slc2a1b | ENSDARG00000007412 | solute carrier family 2 member 1 | 120 | 32 |
slc2a1a | ENSDARG00000001437 | ||||
CDK5 | cdk5 | ENSDARG00000056683 | cyclin dependent kinase 5 | 119 | 32 |
TBC1D24 | tbc1d24 | ENSDARG00000069339 | TBC1 domain family member 24 | 119 | 32 |
GABBR2 | gabbr2 | ENSDARG00000061042 | Gamma-aminobutyric acid Type B Receptor | 112 | 30 |
MECP2 | mecp2 | ENSDARG00000014218 | methyl-CpG binding protein 2 | 111 | 29 |
MAPK10 | mapk10 | ENSDARG00000102730 | mitogen-activated protein kinase 10 | 110 | 29 |
GSK3B | gsk3ba | ENSDARG00000017803 | glycogen synthase kinase-3 beta | 109 | 29 |
C3 | c3a.1 | ENSDARG00000012694 | complement component 3 | 108 | 29 |
c3a.2 | ENSDARG00000087359 | ||||
GNAD1 | G protein alpha stimulating activity polypeptide 1 | 108 | 29 | ||
STXBP1 | stxbp1a | ENSDARG00000001994 | syntaxin binding protein 1 | 107 | 28 |
MAG | Mag | ENSDARG00000104023 | myelin associated glycoprotein | 105 | 28 |
PAK1 | pak1 | ENSDARG00000103959 | serine/threonine-protein kinase PAK 1 | 104 | 28 |
CYFIP2 | cyfip2 | ENSDARG00000036375 | cytoplasmic FMR1 interacting protein 2 | 99 | 26 |
GRN | Grna | ENSDARG00000004954 | granulin precursor | 97 | 26 |
LGI1 | lgi1a | ENSDARG00000020493 | leucine rich glioma inactivated 1 | 97 | 26 |
EPHA4 | epha4a | ENSDARG00000054454 | EPH Receptor A4) | 91 | 24 |
GIT1 | git1 | ENSDARG00000039489 | ARF GTPase-activating protein | 91 | 24 |
RYR2 | ryr2a | ENSDARG00000098856 | ryanodine receptor 2 | 90 | 24 |
ryr1a | ENSDARG00000011422 | ||||
ryr1b | ENSDARG00000023797 | ||||
TUBA1A | tuba1a | ENSDARG00000001889 | tubulin Alpha 1a | 89 | 24 |
CTSD | Ctsd | ENSDARG00000057698 | cathepsin D | 88 | 23 |
LAMC1 | lamc1 | ENSDARG00000036279 | laminin subunit gamma 1 | 87 | 23 |
SLC17A7 | slc17a7a | ENSDARG00000016480 | solute carrier family 17 member 7 | 87 | 23 |
FAM107A | si:ch211-236d3.4 | ENSDARG00000086300 | family with sequence similarity 107 member A | 85 | 23 |
CAMK4 | camk4 | ENSDARG00000005372 | calcium/calmodulin-dependent protein kinase type IV | 84 | 22 |
GAP43 | gap43 | ENSDARG00000099744 | growth associated protein 43 | 84 | 22 |
SYN1 | syn1 | ENSDARG00000060368 | synapsin 1 | 84 | 22 |
FMR1 | fmr1 | ENSDARG00000037433 | fragile X messenger ribonucleoprotein 1 | 83 | 22 |
NRP1 | nrp1a | ENSDARG00000102153 | neuropilin 1 | 82 | 22 |
RTN4 | rtn4a | ENSDARG00000112237 | reticulon 4 | 81 | 21 |
CPLX1 | cplx2 | ENSDARG00000111920 | complexin 1 | 80 | 21 |
Calcium Homeostasis | |||
---|---|---|---|
Gene (Human) | Gene Symbol (Danio rerio) | Ensembl Gene ID (Danio rerio) | Protein Name |
PPP3CA | ppp3cb | ENSDARG00000025106 | protein phosphatase 3 catalytic subunit alpha |
ppp3ca | ENSDARG00000004988 | ||
CACNA2D2 | cacna2d2a | ENSDARG00000103390 | calcium voltage-gated channel auxiliary subunit alpha 2 delta 2 |
RYR2 | ryr2a | ENSDARG00000098856 | ryanodine receptor 2 |
ryr1a | ENSDARG00000011422 | ||
ryr1b | ENSDARG00000023797 | ||
SYN1 | syn1 | ENSDARG00000060368 | synapsin 1 |
CAMK2A | camk2a | ENSDARG00000053617 | calcium/calmodulin dependent protein kinase II alpha |
CAMK4 | camk4 | ENSDARG00000005372 | calcium/calmodulin dependent protein kinase IV |
Mitochondria and energy metabolism | |||
PPP3CA | ppp3cb | ENSDARG00000025106 | protein phosphatase 3 catalytic subunit alpha |
ppp3ca | ENSDARG00000004988 | ||
DNM1L | dnm1l | ENSDARG00000015006 | dynamin 1 Like |
CAMK2A | camk2a | ENSDARG00000053617 | calcium/calmodulin dependent protein kinase II alpha |
GSK3B | gsk3ba | ENSDARG00000017803 | glycogen synthase kinase-3 beta |
SLC2A1 | slc17a7a | ENSDARG00000016480 | solute carrier family 2 member 1 |
Synapses alteration | |||
GABBR2 | gabbr2 | ENSDARG00000061042 | Gamma-aminobutyric acid Type B Receptor |
STXBP1 | stxbp1a | ENSDARG00000001994 | syntaxin binding protein 1 |
RTN4 | rtn4a | ENSDARG00000112237 | reticulon 4 |
CPLX1 | cplx2 | ENSDARG00000111920 | complexin 1 |
SLC17A7 | slc17a7a | ENSDARG00000016480 | solute carrier family 17 member 7 |
L1CAM (CHL1) | l1camb | ENSDARG00000015025 | cell adhesion molecule L1 Like |
l1cama | ENSDARG00000007149 | ||
CTSD | ctsd | ENSDARG00000057698 | cathepsin D |
18 °C vs. 26 °C | |
---|---|
Networks | Molecules |
Neuron projections | adam22 ↑, prkcbb ↓, mapk10 ↓, gap43 ↓, snap25a ↓, slc17a7 ↑, htt ↓, cplx1 ↓, camk2a ↑, rasgrf1 ↓ |
Synapsis formation | adam22 ↑, mapk10 ↓, gsk3b ↑, slc6a1b ↑, ache ↑, snap25a ↓, slc17a7 ↑, htt ↓, cplx1 ↓, syn1 ↓, camk2a ↑ |
Abnormal locomotory behaviour process quality | dyrk1aa ↓, stxbp1a ↑, cyfip2 ↑, ache ↑ |
IL3 signalling | prkcbb ↓, stat3 ↑, pak1 ↑, sgk3b ↑, slc2a1a ↓ |
psychological disorder: calcium signalling and adaptive immune system network | snc2b ↓, ppp3ca ↓ ↑, cacna1c ↓, camk2a ↑ |
34 °C vs. 26 °C | |
Networks | Molecules |
Synapsis | gabbr2 ↓, gabrg2 ↓, tbc1d24 ↓, stxbp1a ↑, cplx1 ↓, syn1 ↓, git1 ↓, ppp3ca ↑, ppp1r9a ↓, map1b ↑, mapk10 ↓ |
Regulation of cytoskeleton organization | spns2 ↓, gfap ↑, htt ↓, hsp90aa1.1 ↑, dpysl3 ↑, dync1h1 ↑, ppp1r9a ↓, map1b ↑, tuba1l2 ↓ |
Establishment of cell polarity | cdh2 ↑, map1b ↑ |
KO BDNF and HT BDNF at 26 °C and 34 °C vs. WT | |
Networks | Molecules |
Synapsis | rapgef2 ↓, nptnb ↓, git1 ↓, dcc ↓, pak1 ↑, dnm1 ↓, ctnnd2a ↑, cdk5 ↓ ↑, gsk3b ↓, mapk10 ↓, ppp3ca ↓ ↑, dnm1b ↓, grid2 ↓, map2 ↓ ↑, slc17a7 ↓ ↑, sptbn1 ↓, tbc1d24 ↓, stxbp1a ↓, shank2 ↑, camk2a ↓, syn2a ↓, slc6a1b ↑, tnr ↓ ↑, vamp2 ↑, gap43 ↑, cplx2 ↓ ↑, rab3aa ↓, cplx1 ↓ ↑, fmr1 ↓, mecp2 ↓ ↑, camk4 ↓, rtn4a ↑, cyfip2 ↓ |
Stress response | sod2 ↓, sod1 ↑, hsp90a1 ↓, capzb ↓, tuba1a ↓, gsk3b ↓, camk2a ↓, mapk1 ↓ |
Response to heat stress | mapk1 ↓, gsk3b ↓, hsp90ab1 ↓, camk2a ↓ |
Gene (Human) | Gene Symbol (Danio rerio) | Ensembl Gene ID (Danio rerio) | Protein Name | p-Value | Predicted Activation | Gene (Human) | Gene Symbol (Danio rerio) | Ensembl Gene ID (Danio rerio) | Protein Name | p-Value | Predicted Activation |
---|---|---|---|---|---|---|---|---|---|---|---|
ACUTE_18 °C | CHRONIC_18 °C | ||||||||||
KDM5A | kdm5a | ENSDARG00000104567 | Lysine Demethylase 5A Transcriptor regulator | 3.80 × 10−12 | TP53 | tp53 | ENSDARG00000035559 | Tumor Protein P53 | 3.88 × 10−22 | ||
RICTOR | rictora | ENSDARG00000100867 | Rapamycin-Insensitive Companion Of MTOR | 4.95 × 10−12 | MAPT | mapta maptb | ENSDARG00000089314; ENSDARG00000087616 | Microtubule associated protein tau | 3.16 × 10−18 | ||
rictorb | ENSDARG00000002020 | ||||||||||
UQCC3 | uqcc3 | ENSDARG00000093382 | Ubiquinol-Cytochrome C Reductase Complex Assembly Factor 3 | 1.30 × 10−11 | APP | appa; appb | ENSDARG00000104279; ENSDARG00000055543 | Amyloid Beta Precursor Protein | 8.61 × 10−15 | ||
HTT | Htt | ENSDARG00000052866 | Huntingtin | 9.49 × 10−11 | NFE2L2 | nfe2l2a | ENSDARG00000042824 | NFE2 Like BZIP Transcription Factor 2 | 1.25 × 10−14 | ||
MAPT | mapta | ENSDARG00000089314 | Microtubule associated protein tau | 2.21 × 10−10 | 1,2-dithiol-3-thione | Chemical Reagent | 1.34 × 10−14 | ||||
maptb | ENSDARG00000087616 | ||||||||||
ACUTE_34 °C | CHRONIC_34 °C | ||||||||||
APP | appa; appb | ENSDARG00000104279; ENSDARG00000055543 | Amyloid Beta Precursor Protein | 9.84 × 10−13 | MAPT | mapta; maptb | ENSDARG00000089314; ENSDARG00000087616 | Microtubule associated protein tau | 2.94 × 10−19 | ||
CD437 | chemical drug | 4.69 × 10−12 | APP | appa; appb | ENSDARG00000104279; ENSDARG00000055543 | Amyloid Beta Precursor Protein | 7.82 × 10−16 | ||||
MAPT | mapta; maptb | ENSDARG00000089314; ENSDARG00000087616 | Microtubule associated protein tau | 1.12 × 10−11 | NFE2L2 | nfe2l2a | ENSDARG00000042824 | NFE2 Like BZIP Transcription Factor 2 | 2.41 × 10−15 | In. | |
ST1926 | chemical drug | 3.58 × 10−10 | TP53 | tp53 | ENSDARG00000035559 | Tumor Protein P53 | 2.56 × 10−15 | ||||
Pln | pln | ENSDARG00000069404 | Phospholamban | 6.80 × 10−10 | 1,2-dithiol-3-thione | Chemical Reagent | 3.33 × 10−14 | In. | |||
KO BDNF_26 °C | HT BDNF_26 °C | ||||||||||
MAPT | mapta; maptb | ENSDARG00000089314; ENSDARG00000087616 | Microtubule associated protein tau | 2.92 × 10−52 | MAPT | mapta; maptb | ENSDARG00000089314; ENSDARG00000087616 | Microtubule associated protein tau | 1.75 × 10−19 | ||
APP | appa; appb | ENSDARG00000104279; ENSDARG00000055543 | Amyloid Beta Precursor Protein | 2.32 × 10−37 | ST1926 | chemical drug | 5.68 × 10−15 | ||||
CD 437 | chemical drug | 2.58 × 10−33 | Ac. | CD437 | chemical drug | 5.11 × 10−14 | |||||
PSEN1 | psen1 | ENSDARG00000004870 | Presenilina 1 | 4.90 × 10−32 | UQCC3 | uqcc3 | ENSDARG00000093382 | Ubiquinol-Cytochrome C Reductase Complex Assembly Factor 3 | 1.07 × 10−13 | ||
TP53 | tp53 | ENSDARG00000035559 | Tumor Protein P53 | 2.04 × 10−31 | beta-estradiol | Chemical-endogenous | 2.65 × 10−12 | In. | |||
KO BDNF_34 °C | HT BDNF_34 °C | ||||||||||
MAPT | mapta; maptb | ENSDARG00000089314; ENSDARG00000087616 | Microtubule associated protein tau | 4.50 × 10−80 | CD437 | Chemical drug | 6.84 × 10−14 | ||||
CLPP | clpp | ENSDARG00000020679 | Caseinolytic Mitochondrial Matrix Peptidase Proteolytic Subunit | 2.98 × 10−49 | Activated | MAPT | mapta; maptb | ENSDARG00000089314; ENSDARG00000087616 | Microtubule associated protein tau | 1.30 × 10−13 | |
APP | appa; appb | ENSDARG00000104279; ENSDARG00000055543 | Amyloid Beta Precursor Protein | 1.81 × 10−48 | RICTOR | rictora; rictorb | ENSDARG00000100867; ENSDARG00000002020 | Rapamycin-Insensitive Companion Of MTOR | 7.45 × 10−13 | ||
PSEN1 | psen1 | ENSDARG00000004870 | Presenilina 1 | 5.79 × 10−44 | Sirolimus | Chemical drug | 9.20 × 10−12 | ||||
UQCC3 | uqcc3 | ENSDARG00000093382 | Ubiquinol-Cytochrome C Reductase Complex Assembly Factor 3 | 4.60 × 10−43 | TP53 | tp53 | ENSDARG00000035559 | Tumor protein P53 | 7.17 × 10−11 | Ac. |
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Maffioli, E.; Nonnis, S.; Grassi Scalvini, F.; Negri, A.; Tedeschi, G.; Toni, M. The Neurotoxic Effect of Environmental Temperature Variation in Adult Zebrafish (Danio rerio). Int. J. Mol. Sci. 2023, 24, 15735. https://doi.org/10.3390/ijms242115735
Maffioli E, Nonnis S, Grassi Scalvini F, Negri A, Tedeschi G, Toni M. The Neurotoxic Effect of Environmental Temperature Variation in Adult Zebrafish (Danio rerio). International Journal of Molecular Sciences. 2023; 24(21):15735. https://doi.org/10.3390/ijms242115735
Chicago/Turabian StyleMaffioli, Elisa, Simona Nonnis, Francesca Grassi Scalvini, Armando Negri, Gabriella Tedeschi, and Mattia Toni. 2023. "The Neurotoxic Effect of Environmental Temperature Variation in Adult Zebrafish (Danio rerio)" International Journal of Molecular Sciences 24, no. 21: 15735. https://doi.org/10.3390/ijms242115735