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The exploration of a new environment leads to the modulation of gene expression for prolonged times in the rat
Abstract
In the present study we performed a transcriptional analysis in order to evaluate changes in gene expression induced by exploration in prolonged times. The analysis was carried out 3, 10 and 20 days after exploration. We analyzed the modulation of the expression levels of Pfn2, Casp3, Pdrg1, Pea15, Ywhaz genes which previously were found not modulated 2 days after exploration. Our data show that the expression of Pfn2, Casp3, Pdrg1, Pea15, Ywhaz genes was modulated at 10 or 20 days. The transcript, whose expression had been evaluated with the qRT-PCR, code for proteins which belong to the following functional categories: synaptic modulation, apoptosis, signal transduction.
It is interesting to note that the modulation of the expression of these genes was evident some days after environmental exploration, and not previously at 2 days after conditioning as occurred after contextual fear conditioning (CFC). Hence it is possible to hypothesize that the spatial memory processes require a longer period of elaboration than the emotional ones, fundamental for the survival of the species.
Keywords
References
Aitken A. 14-3-3 proteins: a historic overview. Semin Cancer Biol. 16(3):162-72, 2006.
Archer J. Tests for emotionality in rats and mice: a review. Anim Behav. 21(2):205-35, 1973.
Augustsson H., Meyerson B.J. Exploration and risk assessment: a comparative study of male house mice (Mus musculus musculus) and two laboratory strains. Physiol Behav. 81(4):685-98, 2004.
Augustsson H., Dahlborn K., Meyerson B.J. Exploration and risk assessment in female wild house mice (Mus musculus musculus) and two laboratory strains. Physiol Behav. 84(2):265-77, 2005.
Barnes C.A. Spatial learning and memory processes: the search for their neurobiological mechanisms in the rat. Trends Neurosci. 11(4):163-9, 1988.
Belzung C. Measuring rodent exploratory behavior.Techniques in the Behavioral and Neural Sciences. Chapter 4.11.Volume 13, Pages 738-749, 1999.
Belzung C., Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res. 125(1-2):141-9, 2001.
Campbell D.S., and Holt C.E. “Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones”. Neuron 37: 939-952, 2003.
Carlier M.F., Pernier J., Montaville P., Shekhar S., Kühn S. Control of polarized assembly of actin filaments in cell motility Cytoskeleton Dynamics and Motility group. Cell Mol Life Sci. 72(16): 3051–3067, 2015.
Da Silva J.S., Medina M., Zuliani C., Di Nardo A., Witke W., Dotti C.G. RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability. J Cell Biol. 162(7):1267-79, 2003
Federighi G., Traina G., Macchi M., Ciampini C., Bernardi R., Baldi E., Bucherelli C., Brunelli M., Scuri R. Modulation of gene expression in contextual fear conditioning in the rat. PLoS One., 8(11):e80037, 2013.
Federighi G., Traina G., Bernardi R., Baldi E., Bucherelli C., Scuri R. Contextual fear conditioning modulates the gene expression over time. Archives Ital. Biol. 156 (1-2):40-47, 2018
Fu H., Subramanian R., Masters S.C. 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxico. 40:617-47, 2000.
Gilman C.P., and Mattson M.P. “Do apoptotic mechanisms regulate synaptic plasticity and growth-cone motility?” Neuromolecular Med. 2: 197-214, 2002.
Hermeking H., Benzinger A. 14-3-3 proteins in cell cycle regulation. Semin Cancer Biol. 16 (3):183-92, 2006.
Hejblum B. P. , Skinner J. , Thiébaut R . Time-Course Gene Set Analysis for Longitudinal Gene Expression Data. PLoS Comput Biol. 11(6): e1004310, 2015.
Huesmann G. R., Clayton D. F. Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song response habituation. Neuron. 52(6): 1061–1072, 2006.
Irle E. Combined lesions of septum, amygdala, hippocampus, anterior thalamus, mamillary bodies and cingulate and subicular cortex fail to impair the acquisition of complex learning tasks. Exp Brain Res. 58(2):346-61, 1985.
Jazvinšćak J.M, Vlainić J., Čadež V., Šegota S. Correction: Atomic force microscopy reveals new biophysical markers for monitoring subcellular changes in oxidative injury: Neuroprotective effects of quercetin at the nanoscale. PLoS One. 14(2):e0212150, 2019.
Kasinski A., Dong X., Khuri F.R., Boss J., Fu H. Transcriptional Regulation of YWHAZ, the Gene Encoding 14-3-3ζ. PLoS One. 9(4): e93480. 2014.
Ko L.J., and Prives C. “p53: puzzle and paradigm” Genes Dev. 10: 1054-1072, 1996.
Kuo C.T., Zhu S., Younger S., Jan L.Y., Jan Y.N. “Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning” Neuron 51: 283-290, 2006.
Lee Y.Y., Ryu M.S., Kim H.S., Suganuma M., Song K.Y., Lim I.K. Regulations of Reversal of Senescence by PKC Isozymes in Response to 12-O Tetradecanoylphorbol-13-Acetate via Nuclear Translocation of pErk1/2. Mol Cells. 39(3): 266–279, 2016.
Li Z., Jo J., Jia J.M., Lo.SC., Whitcomb DJ., Jiao S., Cho K., Sheng M. “Caspase-3 Activation via Mitochondria Is Required for Long-Term Depression and AMPA Receptor Internalization” Cell 141: 859-871, 2010.
Lieberwirth C., Pan Y., Liu Y., Zhang Z., Wang Z. Hippocampal adult neurogenesis: Its regulation and potential role in spatial learning and memory. Brain Res. 1; 1644:127-40, 2016.
Lister R.G. Ethologically-based animal models of anxiety disorders. Pharmacol Ther. 46(3):321-40, 1990.
Livak KJ., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods.;25(4):402-8, 2001.
Marques J.M., Olsson I.A., Ogren S.O., Dahlborn K. Evaluation of exploration and risk assessment in pre-weaning mice using the novel cage test. Physiol Behav. 93(1-2):139-47, 2008.
Matsumoto J., Makino Y., Miura H., Yano M. A computational model of the hippocampus that represents environmental structure and goal location, and guides movement. Biol Cybern. 105(2):139-52, 2011.
Mendez M., Arias N., Uceda S., Arias J.L. c-Fos expression correlates with performance on novel object and novel place recognition tests. Brain Res Bull. 117:16-23, 2015.
Montgomery K.C. The relation between fear induced by novel stimulation and exploratory behavior. J Comp Physiol Psychol. 48(4):254-60, 1955.
Mundy W.R., Tilson H.A. Behavioral impairment in the rat after colchicine lesions of the hippocampus and nucleus basalis. Neurotoxicology. 9(3):511-9, 1988.
O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34(1):171-5, 1971.
Pernier J., Shekhar S., Jegou A., Guichard B., Carlier M.F. Profilin Interaction with Actin Filament Barbed End Controls Dynamic Instability, Capping, Branching, and Motility. Dev Cell. 36(2): 201–214, 2016.
Poltz R., Naumann M. Dynamics of p53 and NF-κB regulation in response to DNA damage and identification of target proteins suitable for therapeutic intervention. BMC Syst Biol. 6: 125. 2012.
Ramírez-Amaya V., Vazdarjanova A., Mikhael D., Rosi S., Worley P.F., Barnes C.A. Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci. 16;25(7):1761-8, 2005.
Ramos J.W., Townsend D.A., Piarulli D., Kolata S., Light K., Hale G., Matzel L.D. Deletion of PEA-15 in mice is associated with specific impairments of spatial learning abilities Neuroscience 10:134, 2009.
Rivas-Arancibia S., Guevara-Guzman R., Lopez-Vidal Y., Rodriguez-Martinez E., Zanardo-Gomes M., Angoa-Perez M., Raisman-Vozari R. “Oxidative Stress Caused by Ozone Exposure Induces Loss of Brain Repair in the Hippocampus of Adult Rats” Toxilogical Sciences 113(1): 187-197, 2010.
Robinson L., McKillop-Smith S., Ross N.L., Pertwee R.G., Hampson R.E., Platt B., Riedel G. Hippocampal endocannabinoids inhibit spatial learning and limit spatial memory in rats. Psychopharmacology. 198(4):551-63, 2008.
Robles Y., Vivas-Mejía P.E., Ortiz-Zuazaga H.G., Félix J., Ramos X.., Peña de Ortiz S. Hippocampal gene expression profiling in spatial discrimination learning. Neurobiol Learn Mem. 80(1):80-95, 2003.
Rodgers R.J., Haller J., Holmes A., Halasz J., Walton T.J., Brain P.F. Corticosterone response to the plus-maze: high correlation with risk assessment in rats and mice. Physiol Behav. 68(1-2):47-53, 1999.
Roy V., Chapillon P. Further evidences that risk assessment and object exploration behaviours are useful to evaluate emotional reactivity in rodents. Behav Brain Res. 154(2):439-48, 2004.
Sacchetti B., Lorenzini C.A., Baldi E., Bucherelli C., Roberto M., Tassoni G., Brunelli M. Long-lasting hippocampal potentiation and contextual memory consolidation. Eur. J. Neurosci. 13 (12): 2291-8, 2001
Sutherland R.J, Kolb B., Whishaw I.Q. Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neurosci Lett. 31(3):271-6, 1982.
Twomey E.C., Cordasco D.F., Kozuch S. D., Wei Y. Substantial Conformational Change Mediated by Charge-Triad Residues of the Death Effector Domain in Protein-Protein Interactions. PLoS One.; 8(12): e83421, 2013.
Treit D. Animal models for the study of anti-anxiety agents: a review. Neurosci Biobehav Rev. 9(2):203-22, 1985.
Vazdarjanova A., Ramirez-Amaya V., Insel N., Plummer T.K., Rosi S., Chowdhury S., Mikhael D., Worley P.F., Guzowski J.F., Barnes C.A. Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J Comp Neurol. 498(3):317-29, 2006.
Wetzel M.K., Naska S., Laliberte´ C.L, Rymar V.V., Fujitani M., Biernaskie J.A., Cole C.J., Lerch J.P., Spring S., Wang S.H., Frankland P.W., Henkelman R.M., Josselyn S.A., Sadikot A.F., Miller F.D., Kaplan D.R. “p73 Regulates Neurodegeneration and Phospho-Tau Accumulation during Aging and Alzheimer’s Disease” Neuron 59: 708-721, 2008.
Williams D.W., Kondo S., Krzyzanowska A., Hiromi Y., Truman J.W. Local caspase activity directs engulfment of dendrites during pruning Nat. Neurosci. 9:1234–1236, 2006.
Witke W, Podtelejnikov AV, Di Nardo A, Sutherland JD, Gurniak CB, Dotti C, Mann M. In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J. 1998 Feb 16;17(4):967-76.
Woodruff E. R., Chun L. E., Hinds L. R., Spencer R. L. Diurnal Corticosterone Presence and Phase Modulate Clock Gene Expression in the Male Rat Prefrontal Cortex. Endocrinology. 157(4): 1522–1534, 2016.
Yuan J. Divergence from a dedicated cellular suicide mechanism: exploring the evolution of cell death Mol. Cell 23:1–12, 2006.
Zalcman G., Federman N., Fiszbein A., De la Fuente V., Ameneiro L., Schor I., Romano A. Sustained CaMKII Delta Gene Expression Is Specifically Required for Long-Lasting Memories in Mice. Mol. Neurob. 56:1437–1450, 2019.
DOI: https://doi.org/10.12871/aib.v158i3-4.4733
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