Immunohistochemical characterization of the jugular (superior vagal) ganglion in the pig

• Autorzy: Sienkiewicz W. , Dudek A. , Zacharko-Siembida A. , Marszalek M.
• Języki publikacji: EN

Abstrakty

EN

The study was carried out on three 4-month old female pigs. All the animals were deeply anesthetized and transcardially perfused with 4% buffered paraformaldehyde (pH 7.4). Left and right superior vagal ganglia (SVG) were collected and processed for immunofluorescence labeling method. The preparations were examined under a Zeiss LSM 710 confocal microscope equipped with adequate filter block. Neurons forming SVG were round or oval in shape with a round nucleus in the center. The majority of them (52%) were medium (M) (31-50 μm in diameter) while 7% and 41% were small (S) (up to 30μm in diameter) or large (L) (above 50 μm in diameter) in size, respectively. Double-labeling immunofluorescence revealed that SVG neurons stained for CGRP (approx. 57%; among them 37%, 9% and 54% were M, S and L in size, respectively), SP (14.5%; 72.4% M, 3.4% S, 24.2% L), VACHT (26%; 63% M, 24% S and 13% L ), GAL (14%; 57% M, 29% S, 14% L), NPY (12%; 53% M, 12% S, 35% L), Met-Enk (5%; 40% M, 6% S and 54% L), PACAP (15%; 52% M, 24% S and 24% L),VIP (6.3%; 67% M, 8% S and 25% L), and NOS-positive (6%; 31% M and 69% L). The most abundant populations of intraganglionic nerve fibers were those which stained for CGRP or GAL, whereas only single SP-, PACAP- or Met-ENK-positive nerve terminals were observed.

• Wydawca: -
• Czasopismo: Polish Journal of Veterinary Sciences
• Rocznik: 2017
• Tom: 20
• Numer: 2
• Opis fizyczny: p.377-385,fig.,ref.

Twórcy

autor

Sienkiewicz W.

• Department of Animal Anatomy, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Oczapowskiego 13 Bldg. 105J, 10-719 Olsztyn, Poland

autor

Dudek A.

• Department of Animal Anatomy, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Oczapowskiego 13 Bldg. 105J, 10-719 Olsztyn, Poland

autor

Zacharko-Siembida A.

• Department of Animal Anatomy and Histology, Faculty of Veterinary Medicine, University of Life Sciences, Akademicka 12, 20-033, Lublin, Poland

autor

Marszalek M.

• Department of Animal Anatomy, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Oczapowskiego 13 Bldg. 105J, 10-719 Olsztyn, Poland

Bibliografia

• Arimura A (1992) Pituitary adenylate cyclase activating polypeptide (PACAP): discovery and current status of research. Regul Pept 37: 287-303.
• Bäurle J, Brüning G, Schemann M, Nishiike S, Guldin WO (1999) Co-localization of glutamate, choline acetyltransferase and glycine in the mammalian vestibular ganglion and periphery. Neuroreport 10: 3517-3521.
• Bellier JP, Kimura H (2007) Acetylcholine synthesis by choline acetyltransferase of a peripheral type as demonstrated in adult rat dorsal root ganglion. J Neurochem 101: 1607-1618.
• Bulc M, Nidzgorska A, Całka J (2013) Immunohistochemical characterization of the porcine nodose ganglion. Acta Histochem 115: 440-446.
• Castrignano F, De Stefano ME, Leone F, Mulatero B, Tata AM, Fasolo A, Augusti-Tocco G (1990) Ontogeny of acetylcholinesterase, substance P and calcitonin gene-related peptide-like immunoreactivity in chick dorsal root ganglia. Neuroscience 34: 499-510.
• Chang HM, Berde CB, Holz GG 4th, Steward GF, Kream RM (1989) Sufentanil, morphine, met-enkephalin, and kappa-agonist (U-50,488H) inhibit substance P release from primary sensory neurons: a model for presynaptic spinal opioid actions. Anesthesiology 70: 672-677.
• Czyzyk-Krzeska MF, Bayliss DA, Lawson EE, Millhorn DE (1991a) Expression of messenger RNAs for peptides and tyrosine hydroxylase in primary sensory neurons that innervate arterial baroreceptors and chemoreceptors. Neurosci Lett 129: 98-102.
• Czyzyk-Krzeska MF, Bayliss DA, Seroogy KB, Millhorn DE (1991b) Gene expression for peptides in neurons of the petrosal and nodose ganglia in rat. Exp Brain Res 83: 411-418.
• Decressac M, Barker RA (2012) Neuropeptide Y and its role in CNS disease and repair. Exp Neurol 238: 265-272.
• DeLeon M, Covenas R, Chadi G, Narvaez JA, Fuxe K, Cintra A (1994) Subpopulations of primary sensory neurons show coexistence of neuropeptides and glucocorticoid receptors in the rat spinal and trigeminal ganglia. Brain Res 636: 338-342.
• Ding YQ, Li JL, Lu BZ, Wang D, Zhang ML, Li JS (1998) Co-localization of mu-opioid receptor-like immunoreactivity with substance P-LI, calcitonin gene-related peptide-LI and nitric oxide synthase-LI in vagal and glossopharyngeal afferent neurons of the rat. Brain Res 792: 149-153.
• Dinh QT, Groneberg DA, Peiser C, Joachim RA, Frossard N, Arck PC, Klapp BF, Fischer A (2005a) Expression of substance P and nitric oxide synthase in vagal sensory neurons innervating the mouse airways. Regul Pept 126: 189-194.
• Dinh QT, Mingomataj E, Quarcoo D, Groneberg DA, Witt C, Klapp BF, Braun A, Fischer A (2005b) Allergic airway inflammation induces tachykinin peptides expression in vagal sensory neurons innervating mouse airways. Clin Exp Allergy 35: 820-825.
• Dudek A, Sienkiewicz W, Kaleczyc J (2012) Immunohistochemical characterization of neurons in the vestibular ganglion (Scarpa’s ganglion) of the pig. Pol J Vet Sci 15: 499-507.
• Finley JC, Polak J, Katz DM (1992) Transmitter diversity in carotid body afferent neurons: dopaminergic and peptidergic phenotypes. Neuroscience 51: 973-987.
• Fischer A, Hoffmann B (1996) Nitric oxide synthase in neurons and nerve fibers of lower airways and in vagal sensory ganglia of man. Correlation with neuropeptides. Am J Respir Crit Care Med 154: 209-216.
• Forstermann U, Sessa WC (2012) Nitric oxide synthases: regulation and function. Eur Heart J 33: 829-837.
• Funakoshi K, Kusakabe T, Kadota T, Goris RC, Kishida R (1989) Substance P immunoreactivity in the vagal nerve of mice. Neurosci Res 7: 235-248.
• Gauda EB, Cooper R, Johnson SM, McLemore GL, Marshall C (2004) Autonomic microganglion cells: a source of acetylcholine in the rat carotid body. J Appl Physiol 96: 384-391.
• Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M (2011) Projections of calcitonin gene-related peptide immunoreactive neurons in the vagal ganglia of the rat. J Chem Neuroanat 41: 55-62.
• Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M (2012) Localization in the vagal ganglia of calcitonin gene-related peptide- and calretinin-immunoreactive neurons that innervate the cervical and the subdiaphragmatic esophagus of the rat. J Chem Neuroanat 43: 34-42.
• Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M (2014a) Brain-derived neurotrophic factor immunoreactive vagal sensory neurons innervating the gastrointestinal tract of the rat. J Chem Neuroanat 61-62: 83-87.
• Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M (2014b) Calcitonin gene-related peptide immunoreactive sensory neurons in the vagal and glossopharyngeal ganglia innervating the larynx of the rat. J Chem Neuroanat 55: 18-23.
• Helke CJ, Hill KM (1988) Immunohistochemical study of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat. Neuroscience 26: 539-551.
• Helke CJ, Niederer AJ (1990) Studies on the coexistence of substance P with other putative transmitters in the nodose and petrosal ganglia. Synapse 5: 144-151.
• Helke CJ, Rabchevsky A (1991) Axotomy alters putative neurotransmitters in visceral sensory neurons of the nodose and petrosal ganglia. Brain Res 551: 44-51.
• 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: 577-580.
• Ichikawa H, Helke CJ (1993) Distribution, origin and plasticity of galanin-immunoreactivity in the rat carotid body. Neuroscience 52: 757-767.
• Ichikawa H, Jacobowitz DM, Winsky L, Helke CJ (1991) Calretinin-immunoreactivity in vagal and glossopharyngeal sensory neurons of the rat: distribution and coexistence with putative transmitter agents. Brain Res 557: 316-321.
• Ichikawa H, Terayama R, Yamaai T, Yan Z, Sugimoto T (2007) Brain-derived neurotrophic factor-immunoreactive neurons in the rat vagal and glossopharyngeal sensory ganglia; co-expression with other neurochemical substances. Brain Res 1155: 93-99.
• Joachim RA, Cifuentes LB, Sagach V, Quarcoo D, Hagen E, Arck PC, Fischer A, Klapp BF, Dinh QT (2006) Stress induces substance P in vagal sensory neurons innervating the mouse airways. Clin Exp Allergy 36: 1001-1010.
• Kaleczyc J, Juranek J, Calka J, Lakomy M (2005) Immunohistochemical characterization of neurons in the porcine ciliary ganglion. Pol J Vet Sci 8: 65-72.
• Kang TC, Lee HS, Lee S, Lee CH (2001) Localization and coexistence of calcium-binding proteins and neuropeptides in the vagal ganglia of the goat. Anat Histol Embryol 30: 281-288.
• Katz DM, Karten HJ (1980) Substance P in the vagal sensory ganglia: localization in cell bodies and pericellular arborizations. J Comp Neurol 193: 549-564.
• Kummer W, Fischer A, Kurkowski R, Heym C (1992) The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry. Neuroscience 49: 715-737.
• Kummer W, Gibbins IL, Stefan P, Kapoor V (1990) Catecholamines and catecholamine-synthesizing enzymes in guinea-pig sensory ganglia. Cell Tissue Res 261: 595-606.
• Lakomy M, Kaleczyc J, Wasowicz K, Czaja K (2002) Immunohistochemical study of the otic ganglion in the pig. Pol J Vet Sci 5: 257-262.
• Lang R, Gundlach AL, Holmes FE, Hobson SA, Wynick D, Hokfelt T, Kofler B (2015) Physiology, signaling, and pharmacology of galanin peptides and receptors: three decades of emerging diversity. Pharmacol Rev 67: 118-175.
• Lundberg JM, Hökfelt T, Nilsson G, Terenius L, Rehfeld J, Elde R, Said S (1978) Peptide neurons in the vagus, splanchnic and sciatic nerves. Acta Physiol Scand 104: 499-501.
• Mulder H, Uddman R, Moller K, Elsas T, Ekblad E, Alumets J, Sundler F (1995) Pituitary adenylate cyclase activating polypeptide is expressed in autonomic neurons. Regul Pept 59: 121-128.
• Nazeri M, Razavinasab M, Abareghi F, Shabani M (2014) Role of nitric oxide in altered nociception and memory following chronic stress. Physiol Behav 129: 214-220.
• Pedrazzini T, Pralong F, Grouzmann E (2003) Neuropeptide Y: the universal soldier. Cell Mol Life Sci 60: 350-377.
• Podlasz P, Wąsowicz K, Kaleczyc J, Lakomy M, Bukowski R (2003) Localization of immunoreactivities for neuropeptides and neurotransmitter-synthesizing enzymes in the pterygopalatine ganglion of the pig. Vet Med-Czech 48: 99-107.
• Przewłocki R, Przewłocka B (2001) Opioids in chronic pain. Eur J Pharmacol 429: 79-91.
• Quartu M, Floris A, Del Fiacco M (1990) Substance P- and calcitonin gene-related peptide-like immunoreactive pericellular baskets in human trigeminal ganglion. Basic Appl Histochem 34: 177-181.
• Rytel L, Palus K, Całka J (2015) Co-expression of PACAP with VIP, SP and CGRP in the porcine nodose ganglion sensory neurons. Anat Histol Embryol 44: 86-91.
• Said SI, Mutt V (1970) Polypeptide with broad biological activity: isolation from small intestine. Science 169: 1217-1218.
• Schytz HW, Holst H, Arendt-Nielsen L, Olesen J, Ashina M (2010) Cutaneous nociception and neurogenic inflammation evoked by PACAP38 and VIP. J Headache Pain 11: 309-316.
• Sienkiewicz W (2010) Sources of the porcine testis innervation. Andrologia 42: 395-403.
• Sienkiewicz W, Dudek A (2009) Morphological examination of the proximal ganglion of the vagus nerve in the pig. Pol J Vet Sci 12: 567-569.
• Sienkiewicz W, Kaleczyc J, Majewski M, Lakomy M (1995) NADPH-diaphorase-containing cerebrovascular nerve fibres and their possible origin in the pig. J Hirnforsch (J Brain Res) 36: 353-363.
• Silverman JD, Kruger L (1989) Calcitonin-gene-related-peptide-immunoreactive innervation of the rat head with emphasis on specialized sensory structures. J Comp Neurol 280: 303-330.
• Springall DR, Cadieux A, Oliveira H, Su H, Royston D, Polak JM (1987) Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J Auton Nerv Syst 0: 155-166.
• Strobbia E, Corvetti G, Sisto Daneo L (1988) Distribution of substance P immunoreactive cell bodies and fibers in cranial sensory and autonomic ganglia of the chick. Basic Appl Histochem 32: 161-167.
• Tajti J, Tuka B, Botz B, Helyes Z, Vecsei L (2015) Role of pituitary adenylate cyclase-activating polypeptide in nociception and migraine. CNS Neurol Disord Drug Targets 14: 540-553.
• Tata AM, De Stefano ME, Tomassy GS, Vilaró MT, Levey AI, Biagioni S (2004) Subpopulations of rat dorsal root ganglion neurons express active vesicular acetylcholine transporter. J Neurosci Res 75: 194-202.
• Tata AM, Plateroti M, Cibati M, Biagioni S, Augusti-Tocco G (1994) Cholinergic markers are expressed in developing and mature neurons of chick dorsal root ganglia. J Neurosci Res 37: 247-255.
• Tatemoto K, Rökaeus A, Jörnvall H, McDonald TJ, Mutt V (1983) Galanin – a novel biologically active peptide from porcine intestine. FEBS Lett 164: 124-128.
• Uddman R, Edvinsson L (1989) Neuropeptides in the cerebral circulation. Cerebrovasc Brain Metab Rev 1: 230-252.
• Uddman R, Hara H, Edvinsson L (1989) Neuronal pathways to the rat middle meningeal artery revealed by retrograde tracing and immunocytochemistry. J Auton Nerv Syst 26: 69-75.
• V Euler US, Gaddun JH (1931) An unidentified depressor substance in certain tissue extracts. J Physiol 72: 74-87.
• Yalamuri SM, Brennan TJ, Spofford CM (2013) Neuropeptide Y is analgesic in rats after plantar incision. Eur J Pharmacol 698: 206-212.
• Yamamoto Y, Henrich M, Snipes RL, Kummer W (2003) Altered production of nitric oxide and reactive oxygen species in rat nodose ganglion neurons during acute hypoxia. Brain Res 961: 1-9.
• Yasuhara O, Aimi Y, Shibano A, Matsuo A, Bellier JP, Park M, Tooyama I, Kimura H (2004) Innervation of rat iris by trigeminal and ciliary neurons expressing pChAT, a novel splice variant of choline acetyltransferase. J Comp Neurol 472: 232-245.
• Yeomans DC, Onyüksel H, Dagar S, Ikezaki H, Lu Y, Rubinstein I (2003) Conformation-dependent effects of VIP on nociception in rats. Peptides 24: 617-622.
• Zalecki M (2014) Extrinsic primary afferent neurons projecting to the pylorus in the domestic pig-localization and neurochemical characteristics. J Mol Neurosci 52: 82-89.
• Zhuo H, Ichikawa H, Helke CJ (1997) Neurochemistry of the nodose ganglion. Prog Neurobiol 52: 79-107.
• Zhuo H, Lewin AC, Phillips ET, Sinclair CM, Helke CJ (1995) Inhibition of axoplasmic transport in the rat vagus nerve alters the numbers of neuropeptide and tyrosine hydroxylase messenger RNA-containing and immunoreactive visceral afferent neurons of the nodose ganglion. Neuroscience 66: 175-187.

Identyfikatory

DOI

10.1515/pjvs-2017-0046