Differential activity of transcription factors and neuronal effectors during the development of pikeperch brain

. 2025 Nov 15 ; 14 (11) : . [epub] 20251120

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid41140115

Grantová podpora
LM2023055 ELIXIR CZ
MEYS CR ELIXIR CZ
RVO 67985807 Akademie Věd České Republiky

Juvenile pikeperch (Sander lucioperca) undergo several ontogenetic shifts, the timing of which determines the survival of their first winter. The shift from planktivory to a more active piscivorous phenotype involves moving from pelagic to demersal habitat with more stimuli and hence potential brain functional reorganizations. During two consecutive years, we collected planktivores and piscivores with different body sizes between the years, recording distinct stages relative to the shift, and analyzed their whole-brain transcriptomes in an ecological context. We identified a distinct non-overlapping group of transcription factors (TFs) significantly upregulated in each phenotype: TFs upregulated in planktivores correspond to initial establishment of brain regions and overall architecture; TFs upregulated in piscivores correspond to the refinement of neurons and the formation of specific neuronal circuits. The planktivores independently of body size were characterized by interconnected activity of two TFs, fosab and junba. Gene set enrichment revealed extracellular matrix and collagen-related transcripts in piscivores from both years. A high activity of solute carrier (Slc) transporters was identified in the smaller-bodied piscivores. The neurotranscriptomics results reflected differences in body size and matched with ecological data and survival rates. The brain regulome indicated that body size differences translate into the specific gene activity of juvenile pikeperch.

Zobrazit více v PubMed

Alberini, C. M. (2009). Transcription factors in long-term memory and synaptic plasticity. PubMed DOI PMC

Argyrousi, E. K., Heckman, P. R. A. and Prickaerts, J. (2020). Role of cyclic nucleotides and their downstream signaling cascades in memory function: Being at the right time at the right spot. PubMed DOI

Ashburner, M., Ball, C., Blake, J., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000). Gene ontology: tool for the unification of biology. PubMed DOI PMC

Ayka, A. and Şehirli, A. Ö. (2020). The role of the SLC transporters protein in the neurodegenerative disorders. PubMed DOI PMC

Bhattarai, S., Sochacka-Marlowe, A., Crutchfield, G., Khan, R., Londraville, R. and Liu, Q. (2016). Krüpple-like factors 7 and 6a mRNA expression in adult zebrafish central nervous system. PubMed DOI PMC

Bolger, A. M., Lohse, M. and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. PubMed PMC

Bradford, Y. M., Van Slyke, C. E., Ruzicka, L., Singer, A., Eagle, A., Fashena, D., Howe, D. G., Frazer, K., Martin, R., Paddock, H.et al. (2022). Zebrafish Information Network, the knowledgebase for PubMed DOI PMC

Burge, S., Kelly, E., Lonsdale, D., Mutowo-Muellenet, P., McAnulla, C., Mitchell, A., Sangrador-Vegas, A., Yong, S. Y., Mulder, N. and Hunter, S. (2012). Manual GO annotation of predictive protein signatures: the InterPro approach to GO curation. PubMed DOI PMC

Calvo, R. and Schluessel, V. (2021). Neural substrates involved in the cognitive information processing in teleost fish. PubMed DOI PMC

Chan, G. N., Hoque, M. T. and Bendayan, R. (2013). Role of nuclear receptors in the regulation of drug transporters in the brain. PubMed DOI

Chen, L., Huang, R., Li, Y., Li, Y., Li, Y., Liao, L., He, L., Zhu, Z. and Wang, Y. (2021). Genome-wide identification, evolution of Krüppel-like factors (klfs) and their expressions during GCRV challenge in grass carp ( PubMed DOI

Chu, P. L., Gigliotti, J. C., Cechova, S., Bodonyi-Kovacs, G., Wang, Y. T., Chen, L., Wassertheil-Smoller, S., Cai, J., Isakson, B. E., Franceschini, N.et al. (2023). Collectrin ( PubMed DOI PMC

Colchen, T., Gisbert, E., Krauss, D., Ledoré, Y., Pasquet, A. and Fontaine, P. (2020). Improving pikeperch larviculture by combining environmental, feeding and populational factors. DOI

Conde-Sieira, M. and Soengas, J. L. (2017). Nutrient sensing systems in fish: impact on food intake regulation and energy homeostasis. PubMed DOI PMC

Crean, A. J. and Marshall, D. J. (2009). Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. PubMed DOI PMC

Czeglédi, I., Specziár, A. and Erös, T. (2021). Temporal dynamics of freshwater fish assemblages, their background and methods of quantifications—A synthesis. DOI

Deal, C. K. and Volkoff, H. (2020). The role of the thyroid axis in fish. PubMed DOI PMC

Degen, P. M. and Medo, M. (2025). Replicability of bulk RNA-Seq differential expression and enrichment analysis results for small cohort sizes. PubMed DOI PMC

Derbyshire, E. R. and Marletta, M. A. (2012). Structure and regulation of soluble guanylate cyclase. PubMed DOI

Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M. and Gingeras, T. R. (2013). STAR: ultrafast universal RNA-seq aligner. PubMed PMC

Dörner, H., Wagner, A. and Benndorf, J. (1999). Predation by piscivorous fish on age-0 fish: spatial and temporal variability in a biomanipulated lake (Bautzen Reservoir, Germany). DOI

Eirín-López, J. M., Lewis, J. D., Howe, L. A. and Ausió, J. (2006). Common phylogenetic origin of protamine-like (PL) proteins and histone H1: evidence from bivalve PL genes. PubMed DOI

Feng, Y., Ye, H., Deng, Y., Zhao, Z., Zhao, H., Liu, S., Zhang, L., Duan, Y., Huang, Z., Du, J.et al. (2025). Early brain gene network alterations and growth disruptions in juvenile Chinese longsnout catfish ( PubMed DOI

Garza-Lombó, C., Schroder, A., Reyes-Reyes, E. M. and Franco, R. (2018). mTOR/AMPK signaling in the brain: Cell metabolism, proteostasis and survival. PubMed DOI PMC

Gillespie, M., Jassal, B., Stephan, R., Milacic, M., Rothfels, K., Senff-Ribeiro, A., Griss, J., Sevilla, C., Matthews, L., Gong, C.et al. (2022). The reactome pathway knowledgebase 2022. PubMed DOI PMC

Ginter, K., Kangur, K., Kangur, A. and Haldna, M. (2011). Diet patterns and ontogenetic diet shift of pikeperch, DOI

Glasauer, S. M. and Neuhauss, S. C. (2014). Whole-genome duplication in teleost fishes and its evolutionary consequences. PubMed DOI

Goodrich, H. R. and Clark, T. D. (2023). Why do some fish grow faster than others? DOI

Hai, T. and Hartman, M. G. (2001). The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. PubMed DOI

Hatta, M., Miyake, Y., Uchida, K. and Yamazaki, J. (2018). Keratin 13 gene is epigenetically suppressed during transforming growth factor-β1-induced epithelial-mesenchymal transition in a human keratinocyte cell line. PubMed DOI

Hediger, M. A., Romero, M. F., Peng, J. B., Rolfs, A., Takanaga, H. and Bruford, E. A. (2004). The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteins. PubMed DOI

Herdegen, T. and Leah, J. D. (1998). Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. PubMed DOI

Hobert, O. (2011). Regulation of terminal differentiation programs in the nervous system. PubMed DOI

Hu, C., Tao, L., Cao, X. and Chen, L. (2020). The solute carrier transporters and the brain: Physiological and pharmacological implications. PubMed DOI PMC

Hussain, G., Wang, J., Rasul, A., Anwar, H., Imran, A., Qasim, M., Zafar, S., Kamran, S. K. S., Razzaq, A., Aziz, N.et al. (2019). Role of cholesterol and sphingolipids in brain development and neurological diseases. PubMed DOI PMC

Johnston, C. U. and Kennedy, C. J. (2024). A review of P-glycoprotein function and regulation in fish. DOI

Jůza, T., Vašek, M., Kratochvíl, M., Blabolil, P., Čech, M., Draštík, V., Frouzová, J., Muška, M., Peterka, J., Prchalová, M.et al. (2014). Chaos and stability of age-0 fish assemblages in a temperate deep reservoir: Unpredictable success and stable habitat use. DOI

Kamali-Zare, P. and Nicholson, C. (2013). Brain extracellular space: geometry, matrix and physiological importance. PubMed PMC

Kanehisa, M., Furumichi, M., Tanabe, M., Sato, Y. and Morishima, K. (2017). KEGG: new perspectives on genomes, pathways, diseases and drugs. PubMed DOI PMC

Keppeler, F. W., Montaña, C. G. and Winemiller, K. O. (2020). The relationship between trophic level and body size in fishes depends on functional traits. DOI

Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development in zebrafish. PubMed DOI

Kubra, K., Gaddu, G. K., Liongue, C., Heidary, S., Ward, A. C., Dhillon, A. S. and Basheer, F. (2022). Phylogenetic and expression analysis of PubMed DOI PMC

Kuleshov, M. V., Jones, M. R., Rouillard, A. D., Fernandez, N. F., Duan, Q., Wang, Z., Koplev, S., Jenkins, S. L., Jagodnik, K. M., Lachmann, A.et al. (2016). Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. PubMed DOI PMC

Kuleshov, M. V., Diaz, J. E. L., Flamholz, Z. N., Keenan, A. B., Lachmann, A., Wojciechowicz, M. L., Cagan, R. L. and Ma'ayan, A. (2019). modEnrichr: a suite of gene set enrichment analysis tools for model organisms. PubMed DOI PMC

Laplante, M. and Sabatini, D. M. (2013). Regulation of mTORC1 and its impact on gene expression at a glance. PubMed DOI PMC

Lehner, B., Crombie, C., Tischler, J., Fortunato, A. and Fraser, A. G. (2006). Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. PubMed DOI

Leung, R. F., George, A. M., Roussel, E. M., Faux, M. C., Wigle, J. T. and Eisenstat, D. D. (2022). Genetic regulation of vertebrate forebrain development by homeobox genes. PubMed DOI PMC

Liao, Y., Smyth, G. K. and Shi, W. (2019). The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. PubMed DOI PMC

Lipton, J. O. and Sahin, M. (2014). The neurology of mTOR. PubMed DOI PMC

Love, M. I., Huber, W. and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. PubMed DOI PMC

Madison, B. N., Tavakoli, S., Kramer, S. and Bernier, N. J. (2015). Chronic cortisol and the regulation of food intake and the endocrine growth axis in rainbow trout. PubMed DOI

Merico, D., Isserlin, R., Stueker, O., Emili, A. and Bader, G. D. (2010). Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PubMed DOI PMC

Metcalfe, N. B., Van Leeuwen, T. E. and Killen, S. S. (2016). Does individual variation in metabolic phenotype predict fish behaviour and performance? PubMed DOI PMC

Moore, D. L. and Goldberg, J. L. (2011). Multiple transcription factor families regulate axon growth and regeneration. PubMed DOI PMC

Moore, D. L., Apara, A. and Goldberg, J. L. (2011). Krüppel-like transcription factors in the nervous system: novel players in neurite outgrowth and axon regeneration. PubMed DOI PMC

Nguinkal, J. A., Brunner, R. M., Verleih, M., Rebl, A., de Los Ríos-Pérez, L., Schäfer, N., Hadlich, F., Stüeken, M., Wittenburg, D. and Goldammer, T. (2019). The first highly contiguous genome assembly of pikeperch ( PubMed DOI PMC

Nguyen, Y. T. K., Ha, H. T. T., Nguyen, T. H. and Nguyen, L. N. (2021). The role of SLC transporters for brain health and disease. PubMed DOI PMC

Nicholson, C. and Hrabětová, S. (2017). Brain extracellular space: the final frontier of neuroscience. PubMed DOI PMC

Nolan, E. T., Hindes, A. M., Bolland, J. D., Davies, P., Roberts, C. G., Tarkan, A. S. and Britton, J. R. (2024). Movements and habitat use of native and invasive piscivorous fishes in a temperate and channelized lowland river. DOI

Otteson, D. C., Liu, Y., Lai, H., Wang, C., Gray, S., Jain, M. K. and Zack, D. J. (2004). Kruppel-like factor 15, a zinc-finger transcriptional regulator, represses the rhodopsin and interphotoreceptor retinoid-binding protein promoters. PubMed DOI PMC

Pavličević, J., Glamuzina, L., Conides, A., Savić, N., Rozić, I., Klaoudatos, D., Kazić, A. and Glamuzina, B. (2016). Pikeperch, DOI

Perland, E. and Fredriksson, R. (2017). Classification systems of secondary active transporters. PubMed DOI

Piecha, D., Wiberg, C., Mörgelin, M., Reinhardt, D. P., Deák, F., Maurer, P. and Paulsson, M. (2002). Matrilin-2 interacts with itself and with other extracellular matrix proteins. PubMed DOI PMC

Policar, T., Schaefer, F. J., Panana, E., Meyer, S., Teerlinck, D. T. and Żarski, D. (2019). Recent progress in european percid fish culture production technology-tackling bottlenecks. DOI

Ribeiro, D., Gkenas, C., Gago, J. and Ribeiro, F. (2021). Variation in diet patterns of the invasive top predator DOI

Rønnestad, I., Gomes, A. S., Murashita, K., Angotzi, R., Jönsson, E. and Volkoff, H. (2017). Appetite-controlling endocrine systems in teleosts. PubMed DOI PMC

Rosati, D., Palmieri, M., Brunelli, G., Morrione, A., Iannelli, F., Frullanti, E. and Giordano, A. (2024). Differential gene expression analysis pipelines and bioinformatic tools for the identification of specific biomarkers: a review. PubMed DOI PMC

Ru, X., Huang, Y., Zhou, T., Yang, T., Chen, P., Yang, J., Zhu, C. and Shi, H. (2025). Brain transcriptome profiles of greater amberjack ( DOI

Russo, A. F. (2017). Overview of neuropeptides: awakening the senses? PubMed DOI PMC

Sánchez-Hernández, J., Nunn, A. D., Adams, C. E. and Amundsen, P.-A. (2019). Causes and consequences of ontogenetic dietary shifts: a global synthesis using fish models. PubMed DOI

Saperas, N., Chiva, M., Casas, M. T., Campos, J. L., Eirín-López, J. M., Frehlick, L. J., Prieto, C., Subirana, J. A. and Ausió, J. (2006). A unique vertebrate histone H1-related protamine-like protein results in an unusual sperm chromatin organization. PubMed DOI

Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B. and Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. PubMed DOI PMC

Shaulian, E. and Karin, M. (2002). AP-1 as a regulator of cell life and death. PubMed DOI

Soengas, J. L., Cerdá-Reverter, J. M. and Delgado, M. J. (2018). Central regulation of food intake in fish: an evolutionary perspective. PubMed DOI

Sousa, W. and Flames, N. (2022). Transcriptional regulation of neuronal identity. PubMed DOI PMC

Stakėnas, S., Gregory, S. D., Britton, J. R., Marsh, J. E., Tarkan, A. S., Zięba, G., Wesley, K. J. and Copp, G. H. (2024). Tracking the invasive and euryhaline pikeperch PubMed DOI

Symonová, R., Jůza, T., Tesfaye, M., Brabec, M., Bartoň, D., Blabolil, P., Draštík, V., Kočvara, L., Muška, M., Prchalová, M.et al. (2025). Transition to piscivory seen through brain transcriptomics in a juvenile percid fish: complex interplay of differential gene transcription, alternative splicing, and ncrna activity. PubMed DOI PMC

Szklarczyk, D., Kirsch, R., Koutrouli, M., Nastou, K., Mehryary, F., Hachilif, R., Gable, A. L., Fang, T., Doncheva, N. T., Pyysalo, S.et al. (2023). The STRING database in 2023: protein-protein association networks and functional enrichment analyses for any sequenced genome of interest. PubMed DOI PMC

Tang, H., Finn, R. D. and Thomas, P. D. (2019). TreeGrafter: phylogenetic tree-based annotation of proteins with Gene Ontology terms and other annotations. PubMed DOI PMC

Tesfaye, M., (2025). Environmental drivers of pikeperch (Sander lucioperca) population dynamics in a changing climate.

Tesfaye, M., Souza, A. T., Soukalová, K., Šmejkal, M., Hejzlar, J., Prchalová, M., Říha, M., Muška, M., Vašek, M., Frouzová, J.et al. (2023). Somatic growth of pikeperch ( DOI

Tesfaye, M., Jůza, T., Šmejkal, M., Hejzlar, J., Čech, M., Prchalová, M., Muška, M., Tušer, M., Kočvara, L., Sajdlová, Z.et al. (2024). The impact of climatic conditions and food availability on bimodality size structure and density of YOY pikeperch ( DOI

Tesfaye, M., Souza, A. T., Šmejkal, M., Jůza, T., Sajdlová, Z., Draštík, V., Kočvara, L., Symonová, R., Meador, T. B., Vašek, M.et al. (2025). Distinct intra-cohort resource utilization in young-of-the-year pikeperch ( PubMed DOI PMC

Tesfaye, M., Jůza, T., Šmejkal, M., Soukalová, K., Bartoň, D., Blabolil, P., Čech, M., Hejzlar, J.et al. (in press). Disentangling the drivers of a piscivorous intra-annual cohort and the contributions of three cohorts to early-year class strength in pikeperch (

The Gene Ontology Consortium (2023). The Gene Ontology knowledgebase in 2023. PubMed DOI PMC

The UniProt Consortium (2017). UniProt: the universal protein knowledgebase. PubMed DOI PMC

Tönißen, K., Franz, G. P., Rebl, A., Lutze, P. and Grunow, B. (2024). Does size matter? Small and large larvae of pikeperch ( DOI

Tregub, P. P., Komleva, Y. K., Kukla, M. V., Averchuk, A. S., Vetchinova, A. S., Rozanova, N. A., Illarioshkin, S. N., Salmina, A. B., et al. (2025). Brain plasticity and cell competition: immediate early genes are the focus. PubMed DOI PMC

Veldman, M. B., Bemben, M. A., Thompson, R. C. and Goldman, D. (2007). Gene expression analysis of zebrafish retinal ganglion cells during optic nerve regeneration identifies KLF6a and KLF7a as important regulators of axon regeneration. PubMed DOI

Vinnicombe, K. R. T. and Volkoff, H. (2022). Possible role of transcription factors (BSX, NKX2.1, IRX3 and SIRT1) in the regulation of appetite in goldfish ( PubMed DOI

Vinsland, E. and Linnarsson, S. (2022). Single-cell RNA-sequencing of mammalian brain development: insights and future directions. PubMed DOI

Wang, J., Chitsaz, F., Derbyshire, M. K., Gonzales, N. R., Gwadz, M., Lu, S., Marchler, G. H., Song, J. S., Thanki, N., Yamashita, R. A.et al. (2023). The conserved domain database in 2023. PubMed DOI PMC

Wang, Q., Zhang, L., Zhu, C., Lu, K., Wu, J. and Liang, X. F. (2025). PubMed DOI PMC

West, A. E. and Greenberg, M. E. (2011). Neuronal activity-regulated gene transcription in synapse development and cognitive function. PubMed DOI PMC

Wingender, E., Schoeps, T., Haubrock, M., Krull, M. and Dönitz, J. (2018). TFClass: expanding the classification of human transcription factors to their mammalian orthologs. PubMed DOI PMC

Wysujack, K., Kasprzak, P., Laude, U. and Mehner, T. (2002). Management of a pikeperch stock in a long-term biomanipulated stratified lake: efficient predation vs. low recruitment. DOI

Xiang, T., Yang, C., Deng, Z., Sun, D., Luo, F. and Chen, Y. (2024). Krüppel-like factors family in health and disease. PubMed DOI PMC

Yuce, K. and Okzan, A. I. (2024). The kruppel-like factor (KLF) family, diseases, and physiological events. PubMed DOI

Závorka, L., Blanco, A., Chaguaceda, F., Cucherousset, J., Killen, S. S., Liénart, C., Mathieu-Resuge, M., Němec, P., Pilecky, M., Scharnweber, K.et al. (2023). The role of vital dietary biomolecules in eco-evo-devo dynamics. PubMed DOI

Zhang, H., Wang, H., Shen, X., Jia, X., Yu, S., Qiu, X., Wang, Y., Du, J., Yan, J. and He, J. (2021). The landscape of regulatory genes in brain-wide neuronal phenotypes of a vertebrate brain. PubMed DOI PMC

Zhao, Y., Duan, M., Lin, X., Li, W., Liu, H., Meng, K., Liu, F., Hu, W. and Luo, D. (2024). Molecular underpinnings underlying behaviors changes in the brain of juvenile common carp ( PubMed DOI PMC

Zhou, S. and Shu, Y. (2022). Transcriptional regulation of solute carrier (SLC) drug transporters. PubMed DOI PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...