ZFIN ID: ZDB-PERS-960805-427
Panula, Pertti
Email: pertti.panula@helsinki.fi
URL: http://www.helsinki.fi/neurosci/groups/panula.html
Affiliation: Panula Lab
Address: Department of Anatomy and Neuroscience Center University of Helsinki, Biomedicum Institute of Biomedicine/Anatomy POB 63 00014 Univ Helsinki Finland
Country: Finland
Phone: 358-40-5922323

The group is interested in elucidating how the modulatory aminergic and peptidergic systems regulate important behaviors in vertebrates. Defects in these systems are responsble symptoms in major neurological and psychiatric diseases, e.g. Parkinson's disease, schizophrenia and depression. New neuropeptides and their receptors can be important regulators of aminergic (e.g. noradrenergic, dopaminergic and histaminergic) systems.
To elucidate the role of histamine in development and brain functions, a multidisciplinary study was initiated in zebrafish. In adult fish, histamine is highly concentrated in the brain, as evidenced by specific immunocytochemical methods and HPLC. During development, histamine is first detected in the brain at about 85 h post fertilization, and at 90 h, immunoreactive fibers can be seen in the telencephalon. One of the prominent target areas of hypothalamic histamine neurons in zebrafish is optic tectum. Mutations affecting optic pathfinding may thus be useful in determining the role of histamine in development and regeneration.

We are interested in brain neuronal systems at the time when the zebrafish behavior is already possible to analyze using automated systems rather than the very early larval systems. The pathways of all major aminergic cell groups were mapped using double-staining confocal and 2-photon imaging of wholemounts and thick slices of zf brain, and a 3D imaging system was developed for fruther use of mutants. Automated behavioral assays were also developed to evaluate the usefulness of the zf model in studies on degenerative diseases. These systems are currently used to analyze the significance of newly identified genes.

Sundvik, M., Puttonen, H., Semenova, S., Panula, P. (2021) The bullies are the leaders of the next generation: inherited aminergic neurotransmitter system changes in socially dominant zebrafish, Danio rerio. Behavioural brain research. 409:113309
Chen, Y.C., Baronio, D., Semenova, S., Abdurakhmanova, S., Panula, P. (2020) Cerebral Dopamine Neurotrophic Factor regulates multiple neuronal subtypes and behavior. The Journal of neuroscience : the official journal of the Society for Neuroscience. 40(32):6146-6164
Leinonen, J.T., Chen, Y.C., Pennonen, J., Lehtonen, L., Junna, N., Tukiainen, T., Panula, P., Widén, E. (2019) LIN28B affects gene expression at the hypothalamic-pituitary axis and serum testosterone levels. Scientific Reports. 9:18060
Caldwell, L.J., Davies, N.O., Cavone, L., Mysiak, K.S., Semenova, S.A., Panula, P., Armstrong, J.D., Becker, C.G., Becker, T. (2019) Regeneration of dopaminergic neurons in adult zebrafish depends on immune system activation and differs for distinct populations. The Journal of neuroscience : the official journal of the Society for Neuroscience. 39(24):4694-4713
Leinonen, J.T., Chen, Y.C., Tukiainen, T., Panula, P., Widén, E. (2018) Transient modification of lin28b expression - Permanent effects on zebrafish growth. Molecular and Cellular Endocrinology. 479:61-70
Semenova, S., Rozov, S., Panula, P. (2017) Distribution, properties, and inhibitor sensitivity of zebrafish catechol-O-methyl transferases (COMT). Biochemical pharmacology. 145:147-157
Stainier, D.Y.R., Raz, E., Lawson, N.D., Ekker, S.C., Burdine, R.D., Eisen, J.S., Ingham, P.W., Schulte-Merker, S., Yelon, D., Weinstein, B.M., Mullins, M.C., Wilson, S.W., Ramakrishnan, L., Amacher, S.L., Neuhauss, S.C.F., Meng, A., Mochizuki, N., Panula, P., Moens, C.B. (2017) Guidelines for morpholino use in zebrafish. PLoS Genetics. 13:e1007000
Puttonen, H.A.J., Sundvik, M., Semenova, S., Shirai, Y., Chen, Y.C., Panula, P. (2017) Knock-out of histamine receptor H3 alters adaptation to sudden darkness and monoamine levels in the zebrafish. Acta physiologica (Oxford, England). 222(3)
Puttonen, H.A.J., Semenova, S., Sundvik, M., Panula, P. (2017) Storage of neural histamine and histaminergic neurotransmission is VMAT2 dependent in the zebrafish. Scientific Reports. 7:3060
Aho, V., Vainikka, M., Puttonen, H.A., Ikonen, H.M., Salminen, T., Panula, P., Porkka-Heiskanen, T., Wigren, H.K. (2017) Homeostatic response to sleep/rest deprivation by constant water flow in larval zebrafish in both dark and light conditions. Journal of sleep research. 26(3):394-400
Chen, Y.C., Semenova, S., Rozov, S., Sundvik, M., Bonkowsky, J.L., Panula, P. (2016) A novel developmental role for dopaminergic signaling to specify hypothalamic neurotransmitter identity. The Journal of biological chemistry. 291(42):21880-21892
Ruokonen, S.K., Sanwald, C., Sundvik, M., Polnick, S., Vyavaharkar, K., Duša, F., Holding, A.J., King, A.W., Kilpeläinen, I.A., Lämmerhofer, M., Panula, P., Wiedmer, S.K. (2016) Effect of ionic liquids on zebrafish (Danio rerio) viability, behavior, and histology; correlation between toxicity and ionic liquid aggregation. Environmental science & technology. 50(13):7116-25
Keatinge, M., Bui, H., Menke, A., Chen, Y.C., Sokol, A.M., Bai, Q., Ellett, F., Da Costa, M., Burke, D., Gegg, M., Trollope, L., Payne, T., McTighe, A., Mortiboys, H., de Jager, S., Nuthhall, H., Kuo, M.S., Fleming, A., Schapira, A.H., Renshaw, S.A., Highley, J.R., Chacinska, A., Panula, P., Burton, E.A., O'Neill, M.J., Bandmann, O. (2015) Glucocerebrosidase 1 deficient Danio rerio mirror key pathological aspects of human Gaucher disease and provide evidence of early microglial activation preceding alpha-synuclein-independent neuronal cell death. Human molecular genetics. 24(23):6640-52
Wang, H., Semenova, S., Kuusela, S., Panula, P., Lehtonen, S. (2015) Tankyrases regulate glucoregulatory mechanisms and somatic growth via the central melanocortin system in zebrafish larvae. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 29(11):4435-48
Sundvik, M., Nieminen, H.J., Salmi, A., Panula, P., Hæggström, E. (2015) Effects of acoustic levitation on the development of zebrafish, Danio rerio, embryos. Scientific Reports. 5:13596
Chen, Y.C., Harrison, P.W., Kotrschal, A., Kolm, N., Mank, J.E., Panula, P. (2015) Expression change in Angiopoietin-1 underlies change in relative brain size in fish. Proceedings. Biological sciences. 282(1810)
Sundvik, M., Panula, P. (2015) "Interactions of the orexin/hypocretin neurons and the histaminergic system". Acta physiologica (Oxford, England). 213(2):321-33
Semenova, S.A., Chen, Y.C., Zhao, X., Rauvala, H., Panula, P. (2014) The tyrosine hydroxylase 2 (TH2) system in zebrafish brain and stress activation of hypothalamic cells. Histochemistry and cell biology. 142(6):619-33
Zhao, X., Kuja-Panula, J., Sundvik, M., Chen, Y.C., Aho, V., Peltola, M., Porkka-Heiskanen, T., Panula, P., Rauvala, H. (2014) Amigo Adhesion Protein Regulates Development of Neural Circuits in Zebrafish Brain. The Journal of biological chemistry. 289(29):19958-19975
Dash, S.N., Lehtonen, E., Wasik, A.A., Schepis, A., Paavola, J., Panula, P., Nelson, W.J., and Lehtonen, S. (2014) sept7b is essential for pronephric function and development of left-right asymmetry in zebrafish embryogenesis. Journal of Cell Science. 127(Pt 7):1476-1486
Panula, P., Sundvik, M., and Karlstedt, K. (2014) Developmental roles of brain histamine. Trends in neurosciences. 37(3):159-168
Decker, A.R., McNeill, M.S., Lambert, A.M., Overton, J.D., Chen, Y.C., Lorca, R.A., Johnson, N.A., Brockerhoff, S.E., Mohapatra, D.P., Macarthur, H., Panula, P., Masino, M.A., Runnels, L.W., and Cornell, R.A. (2014) Abnormal differentiation of dopaminergic neurons in zebrafish trpm7 mutant larvae impairs development of the motor pattern. Developmental Biology. 386(2):428-39
Priyadarshini, M., Orosco, L.A., and Panula, P.J. (2013) Oxidative stress and regulation of Pink1 in zebrafish (Danio rerio). PLoS One. 8(11):e81851
Reimer, M.M., Norris, A., Ohnmacht, J., Patani, R., Zhong, Z., Dias, T.B., Kuscha, V., Scott, A.L., Chen, Y.C., Rozov, S., Frazer, S.L., Wyatt, C., Higashijima, S., Patton, E.E., Panula, P., Chandran, S., Becker, T., and Becker, C.G. (2013) Dopamine from the Brain Promotes Spinal Motor Neuron Generation during Development and Adult Regeneration. Developmental Cell. 25(5):478-491
Priyadarshini, M., Tuimala, J., Chen, Y.C., and Panula, P. (2013) A zebrafish model of PINK1 deficiency reveals key pathway dysfunction including HIF signaling. Neurobiology of disease. 54:127-38
Puttonen, H.A., Sundvik, M., Rozov, S., Chen, Y.C., and Panula, P. (2013) Acute ethanol treatment upregulates th1, th2, and hdc in larval zebrafish in stable networks. Frontiers in neural circuits. 7:102
Sundvik, M., Chen, Y.C., and Panula, P. (2013) Presenilin1 Regulates Histamine Neuron Development and Behavior in Zebrafish, Danio rerio. The Journal of neuroscience : the official journal of the Society for Neuroscience. 33(4):1589-1597
Podlasz, P., Sallinen, V., Chen, Y.C., Kudo, H., Fedorowska, N., and Panula, P. (2012) Galanin gene expression and effects of its knock-down on the development of the nervous system in larval zebrafish. The Journal of comparative neurology. 520(17):3846-3862
Sundvik, M., and Panula, P. (2012) The organization of the histaminergic system in adult zebrafish (Danio rerio) brain: neuron number, location and co-transmitters. The Journal of comparative neurology. 520(17):3827-3845
Chen, Y.C., Sundvik, M., Rozov, S., Priyadarshini, M., and Panula, P. (2012) MANF regulates dopaminergic neuron development in larval zebrafish. Developmental Biology. 370(2):237-249
Wang, H., Lehtonen, S., Chen, Y.C., Heikkilä, E., Panula, P., and Holthöfer, H. (2012) Neph3 associates with regulation of glomerular and neural development in zebrafish. Differentiation; research in biological diversity. 83(1):38-46
Pavlidis, M., Sundvik, M., Chen, Y.C., and Panula, P. (2011) Adaptive changes in zebrafish brain in dominant-subordinate behavioral context. Behavioural brain research. 225(2):529-37
Sundvik, M., Kudo, H., Toivonen, P., Rozov, S., Chen, Y.C., and Panula, P. (2011) The histaminergic system regulates wakefulness and orexin/hypocretin neuron development via histamine receptor H1 in zebrafish. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 25(12):4338-47
Zhao, X., Kuja-Panula, J., Rouhiainen, A., Chen, Y.C., Panula, P., and Rauvala, H. (2011) High mobility group box-1 (HMGB1; amphoterin) is required for zebrafish brain development. The Journal of biological chemistry. 286(26):23200-13
Panula, P., Chen, Y.C., Priyadarshini, M., Kudo, S., Semenova, S., Sundvik, M., and Sallinen, V. (2010) The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases. Neurobiology of disease. 40(1):46-57
Perälä, N., Peitsaro, N., Sundvik, M., Koivula, H., Sainio, K., Sariola, H., Panula, P., and Immonen, T. (2010) Conservation, expression, and knockdown of zebrafish plxnb2a and plxnb2b. Developmental dynamics : an official publication of the American Association of Anatomists. 239(10):2722-2734
Sallinen, V., Kolehmainen, J., Priyadarshini, M., Toleikyt, G., Chen, Y.C., and Panula, P. (2010) Dopaminergic cell damage and vulnerability to MPTP in Pink1 knockdown zebrafish. Neurobiology of disease. 40(1):93-101
Hölttä-Vuori, M., Salo, V.T., Nyberg, L., Brackmann, C., Enejder, A., Panula, P., and Ikonen, E. (2010) Zebrafish: gaining popularity in lipid research. The Biochemical journal. 429(2):235-242
Panula, P. (2010) Hypocretin/orexin in fish physiology with emphasis on zebrafish. Acta physiologica (Oxford, England). 198(3):381-386
Chen, Y.C., Priyadarshini, M., and Panula, P. (2009) Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochemistry and cell biology. 132(4):375-381
Sallinen, V., Sundvik, M., Reenilä, I., Peitsaro, N., Khrustalyov, D., Anichtchik, O., Toleikyte, G., Kaslin, J., and Panula, P. (2009) Hyperserotonergic phenotype after monoamine oxidase inhibition in larval zebrafish. Journal of neurochemistry. 109(2):403-415
Kudo, H., Liu, J., Jansen, E.J., Ozawa, A., Panula, P., Martens, G.J., and Lindberg, I. (2009) Identification of proSAAS homologs in lower vertebrates: conservation of hydrophobic helices and convertase-inhibiting sequences. Endocrinology. 150(3):1393-1399
Sallinen, V., Torkko, V., Sundvik, M., Reenilä, I., Khrustalyov, D., Kaslin, J., and Panula, P. (2009) MPTP and MPP+ target specific aminergic cell populations in larval zebrafish. Journal of neurochemistry. 108(3):719-731
Hölttä-Vuori, M., Uronen, R.L., Repakova, J., Salonen, E., Vattulainen, I., Panula, P., Li, Z., Bittman, R., and Ikonen, E. (2008) BODIPY-cholesterol: A new tool to visualize sterol trafficking in living cells and organisms. Traffic (Copenhagen, Denmark). 9(11):1839-1849
Peitsaro, N., Sundvik, M., Anichtchik, O.V., Kaslin, J., and Panula, P. (2007) Identification of zebrafish histamine H(1), H(2) and H(3) receptors and effects of histaminergic ligands on behavior. Biochemical pharmacology. 73(8):1205-1214
Anichtchik, O., Sallinen, V., Peitsaro, N., and Panula, P. (2006) Distinct structure and activity of monoamine oxidase in the brain of zebrafish (Danio rerio). The Journal of comparative neurology. 498(5):593-610
Panula, P., Sallinen, V., Sundvik, M., Kolehmainen, J., Torkko, V., Tiittula, A., Moshnyakov, M., and Podlasz, P. (2006) Modulatory Neurotransmitter Systems and Behavior: Towards Zebrafish Models of Neurodegenerative Diseases. Zebrafish. 3(2):235-247
Ruuskanen, J.O., Peitsaro, N., Kaslin, J.V., Panula, P., and Scheinin, M. (2005) Expression and function of alpha-adrenoceptors in zebrafish: drug effects, mRNA and receptor distributions. Journal of neurochemistry. 94(6):1559-1569
Kaslin, J., Nystedt, J.M., Ostergard, M., Peitsaro, N., and Panula, P. (2004) The orexin/hypocretin system in zebrafish is connected to the aminergic and cholinergic systems. The Journal of neuroscience : the official journal of the Society for Neuroscience. 24(11):2678-2689
Anichtchik, O.V., Kaslin, J., Peitsaro, N., Scheinin, M., and Panula, P. (2004) Neurochemical and behavioural changes in zebrafish Danio rerio after systemic administration of 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Journal of neurochemistry. 88(2):443-453
Peitsaro, N., Kaslin, J., Anichtchik, O.V., and Panula, P. (2003) Modulation of the histaminergic system and behaviour by alpha-fluoromethylhistidine in zebrafish. Journal of neurochemistry. 86(2):432-441
Kaslin, J. and Panula, P. (2001) Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). The Journal of comparative neurology. 440(4):342-377
Peitsaro, N., Anichtchik, O.V., and Panula, P. (2000) Identification of a histamine H3-like receptor in the zebrafish (Danio rerio) brain. Journal of neurochemistry. 75(2):718-724
Panula, P., Karlstedt, K., Sallmen, T., Peitsaro, N., Kaslin, J., Michelsen, K.A., Anichtchik, O., Kukko-Lukjanov, T., and Lintunen, M. (2000) The histaminergic system in the brain: structural characteristics and changes in hibernation. Journal of chemical neuroanatomy. 18(1-2):65-74
Eriksson, K.S., Peitsaro, N., Karlstedt, K., Kaslin, J., and Panula, P. (1998) Development of the histaminergic neurons and expression of histidine decarboxylase mRNA in the zebrafish brain in the absence of all peripheral histaminergic systems. The European journal of neuroscience. 10:3799-3812
Eriksson, K.S., Kaslin, J., and Panula, P. (1996) Development of the histaminergic nervous system in the zebrafish brain. International journal of developmental neuroscience : the official journal of the International Society for Developmental Neuroscience. 51:99

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