Predation threats for a 24-h period activated the extension of axons in the brains of Xenopus tadpoles.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
16 07 2020
16 07 2020
Historique:
received:
26
12
2019
accepted:
24
02
2020
entrez:
18
7
2020
pubmed:
18
7
2020
medline:
15
12
2020
Statut:
epublish
Résumé
The threat of predation is a driving force in the evolution of animals. We have previously reported that Xenopus laevis enhanced their tail muscles and increased their swimming speeds in the presence of Japanese larval salamander predators. Herein, we investigated the induced gene expression changes in the brains of tadpoles under the threat of predation using 3'-tag digital gene expression profiling. We found that many muscle genes were expressed after 24 h of exposure to predation. Ingenuity pathway analysis further showed that after 24 h of a predation threat, various signal transduction genes were stimulated, such as those affecting the actin cytoskeleton and CREB pathways, and that these might increase microtubule dynamics, axonogenesis, cognition, and memory. To verify the increase in microtubule dynamics, DiI was inserted through the tadpole nostrils. Extension of the axons was clearly observed from the nostril to the diencephalon and was significantly increased (P ≤ 0.0001) after 24 h of exposure to predation, compared with that of the control. The dynamic changes in the signal transductions appeared to bring about new connections in the neural networks, as suggested by the microtubule dynamics. These connections may result in improved memory and cognition abilities, and subsequently increase survivability.
Identifiants
pubmed: 32678123
doi: 10.1038/s41598-020-67975-7
pii: 10.1038/s41598-020-67975-7
pmc: PMC7367293
doi:
Substances chimiques
Biomarkers
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11737Références
Spitze, K. Predator-mediated plasticity of prey life history and morphology: Chaoborus americanus predation on Daphnia pulex. Am. Nat. 139, 229–247 (1992).
doi: 10.1086/285325
Schoeppner, N. M. & Relyea, R. A. Damage, digestion, and defence: The roles of alarm cues and kairomones for inducing prey defences. Ecol. Lett. 8, 505–512 (2005).
pubmed: 21352454
doi: 10.1111/j.1461-0248.2005.00744.x
Relyea, R. A. et al. Phylogenetic patterns of trait and trait plasticity evolution: Insights from amphibian embryos. Evolution Int. J. Organic Evolut. 72, 663–678 (2018).
doi: 10.1111/evo.13428
Reger, J., Lind, M. I., Robinson, M. R. & Beckerman, A. P. Predation drives local adaptation of phenotypic plasticity. Nat. Ecol. Evolut. 2, 100–107 (2018).
doi: 10.1038/s41559-017-0373-6
Nunes, A. L., Richter-Boix, A., Laurila, A. & Rebelo, R. Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study. Oecologia 171, 115–127 (2013).
pubmed: 22707039
doi: 10.1007/s00442-012-2389-6
Johnston, C. A., Wilson Rankin, E. E. & Gruner, D. S. Foraging connections: Patterns of prey use linked to invasive predator diel movement. PLoS ONE 13, e0201883 (2018).
pubmed: 30110360
pmcid: 6093679
doi: 10.1371/journal.pone.0201883
Hollander, J. & Bourdeau, P. E. Evidence of weaker phenotypic plasticity by prey to novel cues from non-native predators. Ecol. Evolut. 6, 5358–5365 (2016).
doi: 10.1002/ece3.2271
Relyea, R. A. Trait-mediated indirect effects in larval anurans: Reversing competition with the threat of predation. Ecology 81, 2278–2289 (2000).
doi: 10.1890/0012-9658(2000)081[2278:TMIEIL]2.0.CO;2
Gallie, J. A., Mumme, R. L. & Wissinger, S. A. Experience has no effect on the development of chemosensory recognition of predators by tadpoles of the American toad, Bufo americanus. Herpetologica 57, 376–383 (2001).
McCollum, S. A. & Leimberger, J. D. Predator-induced morphological changes in an amphibian: Predation by dragonflies affects tadpole shape and color. Oecologia 109, 615–621 (1997).
pubmed: 28307347
doi: 10.1007/s004420050124
Relyea, R. A. Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82, 523–540 (2001).
doi: 10.1890/0012-9658(2001)082[0523:MABPOL]2.0.CO;2
Fraker, M. E. The effect of hunger on the strength and duration of the antipredator behavioral response of green frog (Rana clamitans) tadpoles. Behav. Ecol. Sociobiol. 62, 1201–1205 (2008).
doi: 10.1007/s00265-008-0549-9
VanBuskirk, J. & Relyea, R. A. Selection for phenotypic plasticity in Rana sylvatica tadpoles. Biol. J. Linn. Soc. 65, 301–328 (1998).
Kishida, O. & Nishimura, K. Multiple inducible defences against multiple predators in the anuran tadpole, Rana pirica. Evolut. Ecol. Res. 7, 619–631 (2005).
Van Buskirk, J., McCollum, S. A. & Werner, E. E. Natural selection for environmentally induced phenotypes in tadpoles. Evolution Int. J. Organic Evolut. 51, 1983–1992 (1997).
doi: 10.2307/2411018
Kishida, O., Trussell, G. C., Mougi, A. & Nishimura, K. Evolutionary ecology of inducible morphological plasticity in predator-prey interaction: Toward the practical links with population ecology. Popul. Ecol. 52, 37–46 (2010).
doi: 10.1007/s10144-009-0182-0
Mori, T. et al. The constant threat from a non-native predator increases tail muscle and fast-start swimming performance in Xenopus tadpoles. Biol. Open 6, 1726–1733 (2017).
pubmed: 29141955
pmcid: 5703619
doi: 10.1242/bio.029926
Middlemis Maher, J., Werner, E. E. & Denver, R. J. Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proc. Biol. Sci. 280, 20123075 (2013).
pubmed: 23466985
pmcid: 3619459
Adamec, R., Kent, P., Anisman, H., Shallow, T. & Merali, Z. Neural plasticity, neuropeptides and anxiety in animals—Implications for understanding and treating affective disorder following traumatic stress in humans. Neurosci. Biobehav. Rev. 23, 301–318 (1998).
pubmed: 9884124
doi: 10.1016/S0149-7634(98)00032-3
Figueiredo, H. F., Bodie, B. L., Tauchi, M., Dolgas, C. M. & Herman, J. P. Stress integration after acute and chronic predator stress: Differential activation of central stress circuitry and sensitization of the hypothalamo-pituitary-adrenocortical axis. Endocrinology 144, 5249–5258 (2003).
pubmed: 12960031
doi: 10.1210/en.2003-0713
Jongren, M., Westander, J., Natt, D. & Jensen, P. Brain gene expression in relation to fearfulness in female red junglefowl (Gallus gallus). Genes Brain Behav. 9, 751–758 (2010).
pubmed: 20597989
doi: 10.1111/j.1601-183X.2010.00612.x
Sanogo, Y. O., Hankison, S., Band, M., Obregon, A. & Bell, A. M. Brain transcriptomic response of threespine sticklebacks to cues of a predator. Brain Behav. Evol. 77, 270–285 (2011).
pubmed: 21677424
pmcid: 3182040
doi: 10.1159/000328221
Fraser, B. A., Weadick, C. J., Janowitz, I., Rodd, F. H. & Hughes, K. A. Sequencing and characterization of the guppy (Poecilia reticulata) transcriptome. BMC Genomics 12, 202 (2011).
pubmed: 21507250
pmcid: 3113783
doi: 10.1186/1471-2164-12-202
Drew, R. E. et al. Brain transcriptome variation among behaviorally distinct strains of zebrafish (Danio rerio). BMC Genomics 13, 323 (2012).
pubmed: 22817472
pmcid: 3434030
doi: 10.1186/1471-2164-13-323
Cinel, S. D. & Taylor, S. J. Prolonged bat call exposure induces a broad transcriptional response in the male fall armyworm (Spodoptera frugiperda; Lepidoptera: Noctuidae) brain. Front. Behav. Neurosci. 13, 36 (2019).
pubmed: 30863292
pmcid: 6399161
doi: 10.3389/fnbeh.2019.00036
Miksys, S. & Tyndale, R. F. The unique regulation of brain cytochrome P450 2 (CYP2) family enzymes by drugs and genetics. Drug Metab. Rev. 36, 313–333 (2004).
pubmed: 15237857
doi: 10.1081/DMR-120034149
Ekins, S. & Wrighton, S. A. The role of CYP2B6 in human xenobiotic metabolism. Drug Metab. Rev. 31, 719–754 (1999).
pubmed: 10461547
doi: 10.1081/DMR-100101942
Hiroi, T. et al. Progesterone oxidation by cytochrome P450 2D isoforms in the brain. Endocrinology 142, 3901–3908 (2001).
pubmed: 11517168
doi: 10.1210/endo.142.9.8363
Seliskar, M. & Rozman, D. Mammalian cytochromes P450–importance of tissue specificity. Biochim. Biophys. Acta 1770, 458–466 (2007).
pubmed: 17097232
doi: 10.1016/j.bbagen.2006.09.016
Borkum, J. M. Migraine triggers and oxidative stress: A narrative review and synthesis. Headache 56, 12–35 (2016).
pubmed: 26639834
doi: 10.1111/head.12725
Brown, D. R., Schulz-Schaeffer, W. J., Schmidt, B. & Kretzschmar, H. A. Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp. Neurol. 146, 104–112 (1997).
pubmed: 9225743
doi: 10.1006/exnr.1997.6505
Paitel, E., Fahraeus, R. & Checler, F. Cellular prion protein sensitizes neurons to apoptotic stimuli through Mdm2-regulated and p53-dependent caspase 3-like activation. J. Biol. Chem. 278, 10061–10066 (2003).
pubmed: 12529324
doi: 10.1074/jbc.M211580200
Kannan, K. & Jain, S. K. Oxidative stress and apoptosis. Pathophysiology 7, 153–163 (2000).
pubmed: 10996508
doi: 10.1016/S0928-4680(00)00053-5
Klingenberg, M. The ADP and ATP transport in mitochondria and its carrier. Biochim. Biophys. Acta 1778, 1978–2021 (2008).
pubmed: 18510943
doi: 10.1016/j.bbamem.2008.04.011
Klumpe, I. et al. Transgenic overexpression of adenine nucleotide translocase 1 protects ischemic hearts against oxidative stress. J. Mol. Med. (Berlin, Germany) 94, 645–653 (2016).
doi: 10.1007/s00109-016-1413-4
Avila, D. V. et al. Phosphodiesterase 4b expression plays a major role in alcohol-induced neuro-inflammation. Neuropharmacology 125, 376–385 (2017).
pubmed: 28807677
pmcid: 5797427
doi: 10.1016/j.neuropharm.2017.08.011
You, T. et al. Roflupram, a phosphodiesterase 4 inhibitor, suppresses inflammasome activation through autophagy in microglial cells. ACS Chem. Neurosci. 8, 2381–2392 (2017).
pubmed: 28605578
doi: 10.1021/acschemneuro.7b00065
Glover, E. M., Ressler, K. J. & Davis, M. Differing effects of systemically administered rapamycin on consolidation and reconsolidation of context vs cued fear memories. Learn. Mem. (Cold Spring Harbor, N.Y.) 17, 577–581 (2010).
doi: 10.1101/lm.1908310
Parsons, R. G., Gafford, G. M. & Helmstetter, F. J. Translational control via the mammalian target of rapamycin pathway is critical for the formation and stability of long-term fear memory in amygdala neurons. J. Neurosci. 26, 12977–12983 (2006).
pubmed: 17167087
pmcid: 6674972
doi: 10.1523/JNEUROSCI.4209-06.2006
Slipczuk, L. et al. BDNF activates mTOR to regulate GluR1 expression required for memory formation. PLoS ONE 4, e6007 (2009).
pubmed: 19547753
pmcid: 2695538
doi: 10.1371/journal.pone.0006007
Fifield, K. et al. Time-dependent effects of rapamycin on consolidation of predator stress-induced hyperarousal. Behav. Brain Res. 286, 104–111 (2015).
pubmed: 25746515
doi: 10.1016/j.bbr.2015.02.045
Sidrauski, C. et al. Pharmacological brake-release of mRNA translation enhances cognitive memory. eLife 2, e00498 (2013).
pubmed: 23741617
pmcid: 3667625
doi: 10.7554/eLife.00498
Dubey, J., Ratnakaran, N. & Koushika, S. P. Neurodegeneration and microtubule dynamics: Death by a thousand cuts. Front. Cell. Neurosci. 9, 343 (2015).
pubmed: 26441521
pmcid: 4563776
doi: 10.3389/fncel.2015.00343
Penazzi, L., Bakota, L. & Brandt, R. Microtubule dynamics in neuronal development, plasticity, and neurodegeneration. Int. Rev. Cell Mol. Biol. 321, 89–169 (2016).
pubmed: 26811287
doi: 10.1016/bs.ircmb.2015.09.004
Govek, E. E., Newey, S. E. & Van Aelst, L. The role of the Rho GTPases in neuronal development. Genes Dev. 19, 1–49 (2005).
pubmed: 15630019
doi: 10.1101/gad.1256405
Hoogenraad, C. C. & Bradke, F. Control of neuronal polarity and plasticity—A renaissance for microtubules?. Trends Cell Biol. 19, 669–676 (2009).
pubmed: 19801190
doi: 10.1016/j.tcb.2009.08.006
Heasman, S. J. & Ridley, A. J. Mammalian Rho GTPases: New insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690–701 (2008).
pubmed: 18719708
doi: 10.1038/nrm2476
Vargas, J. P., Lopez, J. C. & Portavella, M. What are the functions of fish brain pallium?. Brain Res. Bull. 79, 436–440 (2009).
pubmed: 19463910
doi: 10.1016/j.brainresbull.2009.05.008
Portavella, M. & Vargas, J. P. Emotional and spatial learning in goldfish is dependent on different telencephalic pallial systems. Eur. J. Neurosci. 21, 2800–2806 (2005).
pubmed: 15926927
doi: 10.1111/j.1460-9568.2005.04114.x
Fletcher, M. L. Olfactory aversive conditioning alters olfactory bulb mitral/tufted cell glomerular odor responses. Front. Syst. Neurosci. 6, 16 (2012).
pubmed: 22461771
pmcid: 3309973
doi: 10.3389/fnsys.2012.00016
Kass, M. D., Rosenthal, M. C., Pottackal, J. & McGann, J. P. Fear learning enhances neural responses to threat-predictive sensory stimuli. Science 342, 1389–1392 (2013).
pubmed: 24337299
pmcid: 4011636
doi: 10.1126/science.1244916
Laberge, F. & Roth, G. Organization of the sensory input to the telencephalon in the fire-bellied toad, Bombina orientalis. J. Comp. Neurol. 502, 55–74 (2007).
pubmed: 17335050
doi: 10.1002/cne.21297
Laberge, F., Muhlenbrock-Lenter, S., Dicke, U. & Roth, G. Thalamo-telencephalic pathways in the fire-bellied toad Bombina orientalis. J. Comp. Neurol. 508, 806–823 (2008).
pubmed: 18395828
doi: 10.1002/cne.21720
54Nieuwenhuys, R., Donkelaar, H. J. t. & Nicholson, C. The Central Nervous System of Vertebrates. Vol. 3 (Springer, New York, 1998).
Grossman, E. N., Giurumescu, C. A. & Chisholm, A. D. Mechanisms of ephrin receptor protein kinase-independent signaling in amphid axon guidance in Caenorhabditis elegans. Genetics 195, 899–913 (2013).
pubmed: 23979582
pmcid: 3813872
doi: 10.1534/genetics.113.154393
Borasio, G. D. et al. ras p21 protein promotes survival and fiber outgrowth of cultured embryonic neurons. Neuron 2, 1087–1096 (1989).
pubmed: 2696501
doi: 10.1016/0896-6273(89)90233-X
Sloniowski, S. & Ethell, I. M. Looking forward to EphB signaling in synapses. Semin. Cell Dev. Biol. 23, 75–82 (2012).
pubmed: 22040917
doi: 10.1016/j.semcdb.2011.10.020
Cruz, E. et al. Infralimbic EphB2 modulates fear extinction in adolescent rats. J. Neurosci. 35, 12394–12403 (2015).
pubmed: 26354908
pmcid: 4563033
doi: 10.1523/JNEUROSCI.4254-14.2015
Mayr, B. & Montminy, M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599–609 (2001).
pubmed: 11483993
doi: 10.1038/35085068
Watkins, J. C. & Evans, R. H. Excitatory amino acid transmitters. Annu. Rev. Pharmacol. Toxicol. 21, 165–204 (1981).
pubmed: 6112965
doi: 10.1146/annurev.pa.21.040181.001121
61Garcia-Nafria, J., Herguedas, B., Watson, J. F. & Greger, I. H. The dynamic AMPA receptor extracellular region: A platform for synaptic protein interactions. J. Physiol. (2016).
Semenza, G. L. & Wang, G. L. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell Biol. 12, 5447–5454 (1992).
pubmed: 1448077
pmcid: 360482
Barrett, T. D. et al. Pharmacological characterization of 1-(5-chloro-6-(trifluoromethoxy)- 1H-benzoimidazol-2-yl)-1H-pyrazole-4-carboxylic acid (JNJ-42041935), a potent and selective hypoxia-inducible factor prolyl hydroxylase inhibitor. Mol. Pharmacol. 79, 910–920 (2011).
pubmed: 21372172
doi: 10.1124/mol.110.070508
Sugiyama, M. et al. Homozygous and heterozygous GH transgenesis alters fatty acid composition and content in the liver of Amago salmon (Oncorhynchus masou ishikawae). Biol. Open 1, 1035–1042 (2012).
pubmed: 23213381
pmcid: 3507178
doi: 10.1242/bio.20121263
Kawamoto, T. Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch. Histol. Cytol. 66, 123–143 (2003).
pubmed: 12846553
doi: 10.1679/aohc.66.123
Komatsu, Y., Kishigami, S. & Mishina, Y. In situ hybridization methods for mouse whole mounts and tissue sections with and without additional beta-galactosidase staining. Methods Mol. Biol. (Clifton, N.Y.) 1092, 1–15 (2014).
doi: 10.1007/978-1-60327-292-6_1
Mori, T. et al. Genetic basis of phenotypic plasticity for predator-induced morphological defenses in anuran tadpole, Rana pirica, using cDNA subtraction and microarray analysis. Biochem. Biophys. Res. Commun. 330, 1138–1145 (2005).
pubmed: 15823562
doi: 10.1016/j.bbrc.2005.03.091