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07.05.2024 | Original Article

Organization of enkephalinergic neuronal system in the central nervous system of the gecko Hemidactylus frenatus

verfasst von: Ananya Ganeyan, C. B. Ganesh

Erschienen in: Brain Structure and Function

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Abstract

Enkephalins are endogenous opioid pentapeptides that play a role in neurotransmission and pain modulation in vertebrates. However, the distribution pattern of enkephalinergic neurons in the brains of reptiles has been understudied. This study reports the organization of the methionine-enkephalin (M-ENK) and leucine-enkephalin (L-ENK) neuronal systems in the central nervous system of the gecko Hemidactylus frenatus using an immunofluorescence labeling method. Although M-ENK and L-ENK-immunoreactive (ir) fibers extended throughout the pallial and subpallial subdivisions, including the olfactory bulbs, M-ENK and L-ENK-ir cells were found only in the dorsal septal nucleus. Enkephalinergic perikarya and fibers were highly concentrated in the periventricular and lateral preoptic areas, as well as in the anterior and lateral subdivisions of the hypothalamus, while enkephalinergic innervation was observed in the hypothalamic periventricular nucleus, infundibular recess nucleus and median eminence. The dense accumulation of enkephalinergic content was noticed in the pars distalis of the hypophysis. In the thalamus, the nucleus rotundus and the dorsolateral, medial, and medial posterior thalamic nuclei contained M-ENK and L-ENK-ir fibers, whereas clusters of M-ENK and L-ENK-ir neurons were observed in the pretectum, mesencephalon, and rhombencephalon. The enkephalinergic fibers were also seen in the area X around the central canal, as well as the dorsal and ventral horns. The widespread distribution of enkephalin-containing neurons within the central nervous system implies that enkephalins regulate a variety of functions in the gecko, including sensory, behavioral, hypophysiotropic, and neuroendocrine functions.

Báez-Mendoza R, Schultz W (2013) The role of the striatum in social behavior. Front Neurosci 7:233. https://doi.org/10.3389/fnins.2013.00233CrossRefPubMedPubMedCentral

Batten TFC, Moons L, Cambre M, Vandesande F (1990) Anatomical distribution of galanin-like immunoreactivity in the brain and pituitary of teleost fishes. Neurosci Lett 111:12–17. https://doi.org/10.1016/0304-3940(90)90336-8CrossRefPubMed

Benton MJ (2005) Vertebrate Palaeontology. 3rd Edition, Blackwell Publishing Company, Hoboken 229–231

Bodnar RJ (2018) Endogenous opiates and behavior. Peptides 101:167–212. https://doi.org/10.1016/j.peptides.2018.01.011CrossRefPubMed

Bodnar RJ, Klein GE (2005) Endogenous opiates and behavior: 2004. Peptides 26(12):2629–2711. https://doi.org/10.1016/j.peptides.2005.06.010CrossRefPubMed

Brauth SE (1984) Enkephalin-like immunoreactivity within the telencephalon of the reptile Caiman crocodilus. Neuroscience 11(2):345–358. https://doi.org/10.1016/0306-4522(84)90028-9CrossRefPubMed

Code RA, Carr CE (1995) Enkephalin-like immunoreactivity in the chick brainstem: possible relation to the cochlear efferent system. Hear Res 87(1–2):69–83. https://doi.org/10.1016/0378-5955(95)00080-nCrossRefPubMed

Cruce JA (1975) An autoradiographic study of the projections of the mammillothalamic tract in the rat. Brain Res 85(2):211–219. https://doi.org/10.1016/0006-8993CrossRefPubMed

de Lanerolle NC, Elde RP, Sparber SB, Frick M (1981) Distribution of methionine-enkephalin immunoreactivity in the chick brain: an immunohistochemical study. J Comp Neurol 10(4):513–533. https://doi.org/10.1002/cne.901990406CrossRef

Domínguez L, Morona R, Joven A, González A, López JM (2010) Immunohistochemical localization of orexins (hypocretins) in the brain of reptiles and its relation to monoaminergic systems. J Chem Neuroanat 39(1):20–34. https://doi.org/10.1016/j.jchemneu.2009.07.007CrossRefPubMed

Dores RM, Finger TE, Gold MR (1984) Immunohistochemical localization of enkephalin and ACTH-related substances in the pituitary of the lamprey. Cell Tissue Res 235:107–115CrossRefPubMed

Ebbesson SOE (1967) Ascending axon degeneration following hemisection of the spinal cord in the tegu lizard (Tupinambis nigropunctatus). Brain Res 5:178–206CrossRefPubMed

Fernández-Espejo E (2000) Cómo Funciona El nucleus accumbens? [How does the nucleus accumbens function?]. Rev Neurol 30(9):845–849PubMed

Fernandez-Llebrez P, Perez J, Nadales AE, Cifuentes M, Grondona JM, Mancera JM, Rodríguez EM (1988) Immunocytochemical study of the hypothalamic magnocellular neurosecretory nuclei of the snake Natrix maura and the turtle Mauremys caspica. Cell Tissue Res 253:435–445. https://doi.org/10.1007/BF00222301CrossRefPubMed

Fonken LK, Nelson RJ (2014) The effects of light at night on circadian clocks and metabolism. Endocr Rev 35(4):648–670. https://doi.org/10.1210/er.2013-1051CrossRefPubMed

Furukawa Y, Kotegawa T, Tsutsui K (1995) Effects of opioid peptides on the electrical activity of preoptic and hypothalamic neurons in the quail brain. J Exp Zool 273(2):96–103. https://doi.org/10.1002/jez.1402730203. PMID: 7595282

Ganesh CB (2021) The stress—reproductive axis in fish: the involvement of functional neuroanatomical systems in the brain. J Chem Neuroanat 112:101904. https://doi.org/10.1016/j.jchemneu.2020.101904CrossRefPubMed

Ganesh CB, Vijayalaxmi (2020) Methionine-enkephalin treatment suppresses the pituitary-ovary axis in the cichlid fish Oreochromis mossambicus. Aquac Rep 17:100311. https://doi.org/10.1016/j.aqrep.2020.100311CrossRef

Ganesh CB, Vijayalaxmi (2021) Neuroanatomical organization of methionine-enkephalinergic system in the brain of the Mozambique tilapia Oreochromis mossambicus. J Chem Neuroanat 115:101963. https://doi.org/10.1016/j.jchemneu.2021.101963CrossRefPubMed

Ganeyan A, Ganesh CB (2023a) The influence of the opioid pentapeptide methionine-enkephalin on seasonal and FSH-induced ovarian recrudescence in the gecko Hemidactylus frenatus. Gen Comp Endocrinol 1(342):114353. https://doi.org/10.1016/j.ygcen.2023

Ganeyan A, Ganesh CB (2023b) The opioid peptide leucine-enkephalin disrupts seasonal and gonadotropin-induced ovarian recrudescence in the gecko Hemidactylus frenatus. Comp Biochem Physiol Mol Integr Physiol 283:111454. https://doi.org/10.1016/j.cbpa.2023.111454

Ganeyan A, Ganesh CB (2023c) Organization of the galaninergic neuronal system in the brain of the gecko Hemidactylus frenatus. Neuropeptides 97:102310. https://doi.org/10.1016/j.npep.2022.102310

Goossens N, Dierickx K, Vandesande F (1979) Immunocytochemical localization of vasotocin and mesotocin in the hypothalamus of lacertilian reptiles. Cell Tissue Res 200(2):223–227. https://doi.org/10.1007/BF00236415CrossRefPubMed

Gopal N, Sudha Devi AR (2019) Effect of leucine enkephalin administration on ovarian maturation in the freshwater crab Travancoriana schirnerae. Int J Aquat Biol 1:14–26. https://doi.org/10.22034/ijab.v7i1.526

Guirado S, Dávila J (2009) Evolution of the Optic Tectum in Amniotes. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of Neuroscience. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-29678-2_3162CrossRef

Hammouche SB, Bennis M (2013) Galanin immunoreactivity in the brain of the desert lizard Uromastyx acanthinura during activity season. Folia Histochem et Cytob 51(1):45–54. https://doi.org/10.5603/fhc.2013.007CrossRef

Hoogland PVIM (1977) Efferent connections of the striatum in Tupinambis nigropunctatus. J MorphoI 152:229–246CrossRef

Hughes J, Smith TW, Kosterlitz HW, Fothergill LA, Morgan BA, Morris HR (1975) Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature 258:577–580CrossRefPubMed

Kaminski T, Siawrys G, Bogacka I, Okrasa S, Przała J (2003) The regulation of steroidogenesis by opioid peptides in porcine theca cells. Anim Reprod Sci 78:71–84CrossRefPubMed

Khachaturian H, Lewis ME, Watson SJ (1983) Enkephalin systems in diencephalon and brainstem of the rat. J Comp Neurol. 1;220(3):310 – 20. https://doi.org/10.1002/cne.902200305

Kishori B, Reddy PS (2003) Influence of leucine-enkephalin on moulting and vitellogenesis in the freshwater crab, Oziotelphusa senex senex (Fabricius, 1791) (Decapoda, Brachyura). Crustaceana 76:1281–1290

Kotegawa T, Abe T, Tsutsui K (1997) Inhibitory role of opioid peptides in the regulation of aggressive and sexual behaviors in male Japanese quails. J Exp Zool 277(2):146–154. https://doi.org/10.1002/(sici)1097-010x(19970201)277:2<146::aid-jez6>3.0.co;2-p

Kozicz T, Lázár G (2001) Colocalization of GABA, enkephalin and neuropeptide Y in the tectum of the green frog Rana esculenta. Peptides 22(7):1071–1077. https://doi.org/10.1016/s0196-9781(01)00430-2CrossRefPubMed

Kumar S, Nagaraju GP, Song H, von Kalm L, Borst DW (2012) Exposure to exogenous enkephalins disrupts reproductive development in the Eastern Lubber Grasshopper, Romalea microptera (Insecta: orthoptera). PLoS ONE 7:e51126. https://doi.org/10.1371/journal.pone.0051126CrossRefPubMedPubMedCentral

Kusuma A (1979) The organization of the spinal cord in reptiles with different locomotor patterns. Thesis, University of Nijmegen, Netherlands.

Lewis JW, Baldrighi G, Akil H (1987) A possible interface between autonomic function and pain control: opioid analgesia and the nucleus tractus solitarius. Brain Res 424(1):65–70. https://doi.org/10.1016/0006-8993(87)91193-0CrossRefPubMed

Linster C, Wyble B, Hasselmo ME (1999) Electrical stimulation of the horizontal limb of the diagonal band of Broca modulates population EPSPs in piriform cortex. J Neurophysiol 81(6):2737–2742. https://doi.org/10.1152/jn.1999.81.6.2737CrossRefPubMed

Merchenthaler I, Lázár G, Maderdrut JL (1989) Distribution of proenkephalin-derived peptides in the brain of Rana esculenta. J Comp Neurol 281(1):23–39. https://doi.org/10.1002/cne.902810104CrossRefPubMed

Miselis RR (1981) The efferent projections of the subfornical organ of the rat: a circumventricular organ within a neural network subserving water balance. Brain Res 230:1–23. https://doi.org/10.1016/0006-8993(81)90388-7CrossRefPubMed

Naik DR, Sar M, Stumpf WE (1981) Immunohistochemical localization of enkephalin in the central nervous system and pituitary of the lizard, Anolis carolinensis. J Comp Neurol 198. https://doi.org/10.1002/cne.901980404CrossRef

Northcutt RG, Pritz MB (1978) A spinothalamic pathway to the dorsal ventricular ridge in the speckled caiman, Caiman crocodilus. Anat Rec 190:618

Pestarino M, Vallarino M, Polzonetti-Magni A, Carnevali O, Mosconi G, Facchinetti F (1992) Occurrence of immunoreactive met- and Leu-Enkephalin-like peptides in the ovary of the green frog, Rana esculenta. Gen Comp Endocrinol 85(1):118–123. https://doi.org/10.1016/0016-6480(92)90179-nCrossRefPubMed

Peter R, Paulencu CR (1980) Involvement of the preoptic region in gonadotropin release-inhibition in goldfish, Carassius auratus. J Neuroendocrinol 31(2):133–141. https://doi.org/10.1159/000123064CrossRef

Piñuela C, Northcutt RG (2007) Immunohistochemical organization of the forebrain in the white sturgeon, Acipenser transmontanus. Brain Behav Evol 69(4):229–253. https://doi.org/10.1159/000099612CrossRefPubMed

Pritz M (1995) The thalamus of reptiles and mammals: similarities and differences. Brain Behav Evol 46:197–208. https://doi.org/10.1159/000113274CrossRefPubMed

Reddy PS (2000) Involvement of opioid peptides in the regulation of reproduction in the prawn Penaeus indicus. Naturwissenschaften 87:535–538CrossRefPubMed

Reiner A (1987) The distribution of proenkephalin-derived peptides in the central nervous system of turtles. J Comp Neurol 259(1):65–91. https://doi.org/10.1002/cne.902590106CrossRefPubMed

Reiner A, Karten HJ, Brecha NC (1982) Enkephalin-mediated basal ganglia influences over the optic tectum: immunohistochemistry of the tectum and the lateral spiriform nucleus in pigeon. J Comp Neurol 208(1):37–53. https://doi.org/10.1002/cne.902080104CrossRefPubMed

Reiner A, Brauth SE, Karten HJ (1984) Evolution of the amniote basal ganglia. Trends Neurosci 7:320–325CrossRef

Rodríguez Díaz MA, Candal E, Santos-Duran GN, Adrio F, Rodríguez -Moldes I (2011) Comparative analysis of Met-enkephalin, galanin and GABA immunoreactivity in the developing trout preoptic–hypophyseal system. Gen Comp Endocrinol 173:148–158. https://doi.org/10.1016/j.ygcen.2011.05.012CrossRefPubMed

Roy S, Wang JH, Balasubramanian S, Sumandeep, Charboneau R, Barke R, Loh HH (2001) Role of hypothalamic-pituitary axis in morphine-induced alteration in thymic cell distribution using mu-opioid receptor knockout mice. J Neuroimmunol 1;116(2):147 – 55. https://doi.org/10.1016/s0165-5728(01)00299-5

Russchen FT, Smeets WJAJ, Hoogland PV (1987) Histochemical identification of pallidal and striatal structures in the Lizard Gekko gecko: evidence for compartmentalization. J Comp Neurol 256(3):329–341. https://doi.org/10.1002/cne.902560303CrossRefPubMed

Sanchez VA, Segura L, Pradhan AA (2016) The delta opioid receptor tool box. Neuroscience 338:145–159CrossRef

Sar M, Stump WE, Miller RJ (1978) Immunohistochemical localization of enkephalin in rat brain and spinal cord. J Comp Neurol 182:46–482CrossRef

Sarojini R, Nagabhushanam R, Fingerman M (1995) Evidence for opioid involvement in the regulation of ovarian maturation of the fiddler crab, Uca pugilator. Comp Biochem Physiol 111A:279–282CrossRef

Schwarz I, Muller M, Pavlova I, Schweihoff J, Musacchio F, Mittag M, Fuhrmann M, Schwarz MK (2020) The diagonal band of broca regulates olfactory-mediated behaviors by modulating odor-evoked responses within the olfactory bulb. bioRxiv 372649. https://doi.org/10.1101/2020.11.07.372649.

Sha A, Sun H, Wang Y (2012) Leucine-enkephalin immunoreactivity is also present in the nervous and digestive systems of the octopus, Octopus ocellatus. Mar Freshw Behav Physiol 45:155–160CrossRef

Silla A, Calatayud N, Trudeau V (2021) Amphibian reproductive technologies: approaches and welfare considerations. Conserv Physiol 9(1). https://doi.org/10.1093/conphys/coab011

Simantov R, Snyder SH (1976) Morphine-like peptides in mammalian brain: isolation, structure elucidation, and interaction with the opiate receptor. Proc Natl Acad Sci USA 73:2515–2519CrossRefPubMedPubMedCentral

Smeets WJ, Hoogland PV, Lohman AH (1986) A forebrain atlas of the Lizard Gekko gecko. J Comp Neurol 254(1):1–19. https://doi.org/10.1002/cne.902540102CrossRefPubMed

Stuesse SL, Adli DSH, Cruce WLR (2001) Immunohistochemical distribution of enkephalin, substance P, and somatostatin in the brainstem of the leopard frog, Rana pipiens. Microsc Res Tech 54:229–245CrossRefPubMed

Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21(8):323–331. https://doi.org/10.1016/s0166-2236(98)01265-xCrossRefPubMed

Takahashi A (2021) Enkephalin. Ando H, Ukena K, Nagata S (Eds.), Handbook of Hormones 91–94. https://doi.org/10.1016/b978-0-12-820649-2.00023-1

Tanaka J, Saito H, Seto K (1988) Involvement of the septum in the regulation of paraventricular vasopressin neurons by the subfornical organ in the rat. Neurosci Lett 92:187–191. https://doi.org/10.1016/0304-3940(88)90058-4CrossRefPubMed

ten Donkelaar HJ, Bangma GC, Barbas-Henry HA, de Boer-van Huizen R, Wolters JG (1987) The brain stem in a lizard, Varanus exanthematicus. Adv Anat Embryol Cell Biol 107:1–168. https://doi.org/10.1007/978-3-642-72763-4CrossRefPubMed

ten Donkelaar HJ, Kusuma A, de Boer-van Huizen R (1980) Cells of origin of pathways descending to the spinal cord in some quadrupedal reptiles. J Comp Neurol 192(4):827–851. https://doi.org/10.1002/cne.901920413.

Uliuski PS (1978) Organization of anterior dorsal ventricular ridge in snakes. J Comp Neurol 178:411–450CrossRef

Vallarino M, Bucharles C, Facchinetti F, Vaudry H (1994) Immunocytochemical evidence for the presence of Met-enkephalin and leu-enkephalin distinct neurons in the brain of the elasmobranch fish Scyliorhinus canicula. J Comp Neurol 347:585–597. https://doi.org/10.1002/cne.903470409CrossRefPubMed

Vallarino M, Thoumas JL, Masini MA, Trabucchi M, Chartrel N, Vaudry H (1998) Immunocytochemical localization of enkephalins in the brain of the African lungfish, Protopterus annectens, provides evidence for differential distribution of Met-Enkephalin and Leu-enkephalin. J Comp Neurol 396:275–287CrossRefPubMed

Vecino E, Ekström P (1990) Distribution of Met-enkephalin, Leu-enkephalin, substance P, neuropeptide Y, FMRFamide, and serotonin immunoreactivities in the optic tectum of the Atlantic salmon (Salmo salar L). J Comp Neurol 299(2):229–241. https://doi.org/10.1002/cne.902990207CrossRefPubMed

Vecino E, Perez MTR, Ekstrom P (1995) Localization of enkephalinergic neurons in the central nervous system of the salmon (Salmo salar L.) by in situ hybridization and immunocytochemistry. J Chem Neuroanat 9(2):81–97. https://doi.org/10.1016/0891-0618(95)00068-ICrossRefPubMed

Vijayalaxmi, Ganesh CB (2017) Influence of leucine-enkephalin on pituitary-ovary axis of the cichlid fish Oreochromis mossambicus. Fish Physiol Biochem 43:1253–1264. https://doi.org/10.1007/s10695-017-0369-9

Vijayalaxmi, Sakharkar AJ, Ganesh CB (2020) Leucine-enkephalin-immunoreactive neurons in the brain of the cichlid fish Oreochromis mossambicus. Neuropeptides 81:101999. https://doi.org/10.1016/j.npep.2019.101999CrossRefPubMed

Voneida TJ, Sligar CM (1979) Efferent projections of the dorsal ventricular ridge and the striatum in the Tegu lizard. Tupinambis nigropunctatus. J Comp Neurol 186(1):43–64. https://doi.org/10.1002/cne.901860104CrossRefPubMed

Wang X, Wang W, Tang Y, Dai Z (2021) Subdivisions of the mesencephalon and isthmus in the Lizard Gekko gecko as revealed by ChAT immunohistochemistry. Anat Rec 304(9):2014–2031. https://doi.org/10.1002/ar.24595CrossRef

Wolters JG, Ten Donkelaar HJ, Verhofstand AAJ (1986) Distribution of some peptides (substance P, [Leu] enkephalin, [met] enkephalin) in the brain stem and spinal cord of a lizard, Varanus exanthematicus. Neuroscience 18:917–946CrossRefPubMed

Xu XJ, Hokfelt T, Bartfai T, Wiesenfeld-Hallin Z (2000) Galanin and spinal nociceptive mechanisms: recent advances and therapeutic implications. Neuropeptides 34(3–4):137–147. https://doi.org/10.1054/npep.2000.0820CrossRefPubMed

Yin W, Gore AC (2010) The hypothalamic median eminence and its role in reproductive aging. Ann N Y Acad Sci 1204:113–122. https://doi.org/10.1111/j.1749-6632.2010.05518.xCrossRefPubMedPubMedCentral

Titel: Organization of enkephalinergic neuronal system in the central nervous system of the gecko Hemidactylus frenatus
verfasst von: Ananya Ganeyan
C. B. Ganesh
Publikationsdatum: 07.05.2024
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-024-02805-4

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