Distribution and immunohistochemical properties of autonomic neurons supplying the ovine hip joint capsule

https://doi.org/10.17221/61/2017-VETMEDCitation:Sienkiewicz W, Dudek A, Chroszcz A, Janeczek M, Kaleczyc J (2018): Distribution and immunohistochemical properties of autonomic neurons supplying the ovine hip joint capsule. Veterinarni Medicina, 63: 261-270.
download PDF

Combined retrograde tracing and double labelling immunohistochemistry were applied to study the distribution and chemical coding of autonomic neurons projecting to the ovine hip joint capsule. As revealed by retrograde tracing, fast blue-positive autonomic neurons supplying the lateral side of the hip joint capsule and the medial side of the hip joint capsule were located within the lumbar and sacral of the ipsilateral sympathetic chain ganglia and within the caudal mesenteric ganglion. Immunohistochemistry revealed that nearly all (sympathetic chain ganglia: 96% and caudal mesenteric ganglion: 98.8%) the neurons were adrenergic in nature (positive for dopamine β-hydroxylase). Many retrogradely labelled neurons also displayed immunoreactivity to neuropeptide Y (approximately 34% of fast blue-positive neurons within caudal mesenteric ganglion and sympathetic chain ganglia). Populations of Met-Enk+ (20%) and Leu-Enk+ (6%) neurons were present only in the sympathetic chain ganglia while within caudal mesenteric ganglion no enkephalinergic-labelled neurons were noted. Only a small population (2.2%) of hip joint capsule-projecting neurons were Gal-IR and they were observed only within the caudal mesenteric ganglion. No cholinergic neurons involved in the innervation of the hip joint capsule were found. However, fast blue-positive nerve cell bodies were surrounded by numerous cholinergic nerve fibres often forming basket-like formations. Single Gal+ nerve fibres were found in the intraganglionic connective tissue. Substance P-positive or calcitonin gene-related peptide-positive intraganglionic nerve terminals were very numerous and formed “baskets” surrounding fast blue-positive perikarya within sympathetic chain ganglias and caudal mesenteric ganglion.

References:
Ackermann Paul W., Li Jian, Finn Anja, Ahmed Mahmood, Kreicbergs Andris (2001): Autonomic innervation of tendons, ligaments and joint capsules. A morphologic and quantitative study in the rat. Journal of Orthopaedic Research, 19, 372-378 https://doi.org/10.1016/S0736-0266(00)90029-9
 
Ahmed M., Bjurholm A., Kreicbergs A., Schultzberg M. (1993): Sensory and Autonomic Innervation of the Facet Joint in the Rat Lumbar Spine. Spine, 18, 2121-2126 https://doi.org/10.1097/00007632-199310001-00032
 
Ahmed Mahmood, Bjurholm Anders, Srinivasan Gopala Rao, Theodorsson Elvar, Kreicbergs Andris (1994): Extraction of neuropeptides from joint tissue for quantitation by radioimmunoassay. A study in the rat. Peptides, 15, 317-322 https://doi.org/10.1016/0196-9781(94)90019-1
 
Ahmed M, Bjurholm A, Theodorsson E, Schultzberg M, Kreicbergs A (1995): Neuropeptide Y- and vasoactive intestinal polypeptide-like immunoreactivity in adjuvant arthritis: Effects of capsaicin treatment. Neuropeptides, 29, 33-43 https://doi.org/10.1016/0143-4179(95)90054-3
 
Bergmann G., Siraky J., Rohlmann A., Koelbel R. (1984): A comparison of hip joint forces in sheep, dog and man. Journal of Biomechanics, 17, 907-921 https://doi.org/10.1016/0021-9290(84)90004-6
 
Bergmann G, Graichen F, Rohlmann A (1999): Hip joint forces in sheep. Journal of Biomechanics, 32, 769-777 https://doi.org/10.1016/S0021-9290(99)00068-8
 
Białecki Jacek, Majchrzycki Marian, Szymczak Antoni, Klimowicz-Bodys Małgorzata Dorota, Wierzchoś Edward, Kołomecki Krzysztof (2014): Hip Joint Replacement Using Monofilament Polypropylene Surgical Mesh: An Animal Model. BioMed Research International, 2014, 1-6 https://doi.org/10.1155/2014/187320
 
Buma Pieter (2009): Innervation of the patella: An immunohistochemical study in mice. Acta Orthopaedica Scandinavica, 65, 80-86 https://doi.org/10.3109/17453679408993724
 
Casatti C.A., Frigo L., Bauer J.A. (2016): Origin of Sensory and Autonomic Innervation of the Rat Temporomandibular Joint: A Retrograde Axonal Tracing Study with the Fluorescent Dye Fast Blue. Journal of Dental Research, 78, 776-783 https://doi.org/10.1177/00220345990780031001
 
CATRE MEL G., SALO PAUL T. (1999): Quantitative analysis of the sympathetic innervation of the rat knee joint. Journal of Anatomy, 194, 233-239 https://doi.org/10.1046/j.1469-7580.1999.19420233.x
 
Dudek A., Sienkiewicz W., Marczak M., Kaleczyc J. (2011): Immunohistochemical properties of motoneurons supplying the trapezius muscle in the rat. Polish Journal of Veterinary Sciences, 14, - https://doi.org/10.2478/v10181-011-0030-y
 
Dudek A, Sienkiewicz W, Pidsudko Z, Franke-Radowiecka A, Tomaszewska O, Kaleczyc J (2014): The distribution of trapezius muscle-projecting autonomic neurons in the pig. International Conference Current Approaches to Health and Diseases in Animals and Humas. Lublin, Poland. 55 pp.
 
Heppelmann B., Shahbazian Zahra, Hanesch Ulrike (1997): Quantitative examination of calcitonin gene-related peptide immunoreactive nerve fibres in the cat knee joint capsule. Anatomy and Embryology, 195, 525-530 https://doi.org/10.1007/s004290050072
 
Janig W (ed.) (2006): The Integrative Action of the Autonomic Nervous System: Neurobiology of Homeostasis. Cambridge University Press, Cambridge. 620 pp.
 
Jänig Wilfrid, Green Paul G (2014): Acute inflammation in the joint: Its control by the sympathetic nervous system and by neuroendocrine systems. Autonomic Neuroscience, 182, 42-54 https://doi.org/10.1016/j.autneu.2014.01.001
 
Lee SH, Wang SC, Shen CL (1991): Innervation of the knee joint in the rabbit and the Formosan rock-monkey (Macaca cyclopis): a retrograde HRP study. Proceedings of the National Science Council, Republic of China. Part B, Life Sciences 15, 171–177.
 
Lundberg JM, Rudehill A, Sollevi A (1989a): Pharmacological characterization of neuropeptide Y and noradrenaline mechanisms in sympathetic control of pig spleen. European Journal of Pharmacology 163, 103–113.
 
Lundberg JM, Rudehill A, Sollevi A, Fried G, Wallin G (1989b): Co-release of neuropeptide Y and noradrenaline from pig spleen in vivo: importance of subcellular storage, nerve impulse frequency and pattern, feedback regulation and resupply by axonal transport. Neuroscience 28, 475–486.
 
Marshall KW, Theriault E, Homonko DA (1994): Distribution of substance P and calcitonin gene related peptide immunoreactivity in the normal feline knee. The Journal of Rheumatology 21, 883–889.
 
Miozzari H.H., Clark J.M., Jacob H.A.C., von Rechenberg B., Nötzli H.P. (2004): Effects of removal of the acetabular labrum in a sheep hip model. Osteoarthritis and Cartilage, 12, 419-430 https://doi.org/10.1016/j.joca.2004.02.008
 
Muhr G, Stockhusen H, Scartazini R (1974): Biological stabilization of plastic implants in the sheep hip joint. Langenbecks Archiv fur Chirurgie, 221–223.
 
Preston Elaine, McManus Clare D., Jonsson Ann-Cathrine, Courtice Gillian P. (1995): Vasoconstrictor effects of galanin and distribution of galanin containing fibres in three species of elasmobranch fish. Regulatory Peptides, 58, 123-134 https://doi.org/10.1016/0167-0115(95)00060-O
 
Ruth James A., Doerr Alphonse L., Eiden Lee E. (1984): [LEU5]enkephalin inhibits norepinephrine-induced contraction of rat aorta. European Journal of Pharmacology, 105, 189-191 https://doi.org/10.1016/0014-2999(84)90667-8
 
Saxler Guido, Löer Franz, Skumavc Marc, Pförtner Jörg, Hanesch Ulrike (2007): Localization of SP- and CGRP-immunopositive nerve fibers in the hip joint of patients with painful osteoarthritis and of patients with painless failed total hip arthroplasties. European Journal of Pain, 11, 67-67 https://doi.org/10.1016/j.ejpain.2005.12.011
 
Schaible Hans-Georg, Straub Rainer H. (2014): Function of the sympathetic supply in acute and chronic experimental joint inflammation. Autonomic Neuroscience, 182, 55-64 https://doi.org/10.1016/j.autneu.2013.12.004
 
Sienkiewicz W, Majewski M, Kaleczyc J, Lakomy M (1995): Immunohistochemical study of the existence and coexistence of catecholamine synthesizing enzymes and some neuropeptides in perivascular nerve fibres of the main thoraco-cranial arteries in the pig. Folia Histochemica et Cytobiologica 33, 59–67.
 
Sienkiewicz W., Chrószcz A., Dudek A., Janeczek M., Kaleczyc J. (2015): Caudal mesenteric ganglion in the sheep – macroanatomical and immunohistochemical study. Polish Journal of Veterinary Sciences, 18, - https://doi.org/10.1515/pjvs-2015-0049
 
Tamura Ryoko, Hanesch Ulrike, Schmidt Robert F, Kumazawa Takao, Mizumura Kazue (1998): Examination of colocalization of calcitonin gene-related peptide- and substance P-like immunoreactivity in the knee joint of the dog. Neuroscience Letters, 254, 53-56 https://doi.org/10.1016/S0304-3940(98)00660-0
 
Uddman R., Grunditz Torsten, Kato Joji, Sundler Frank (1998): Distribution and origin of nerve fibers in the rat temporomandibular joint capsule. Anatomy and Embryology, 197, 273-282 https://doi.org/10.1007/s004290050137
 
Wiberg Mikael, Widenfalk Bertil (1991): An anatomical study of the origin of sympathetic and sensory innervation of the elbow and knee joint in the monkey. Neuroscience Letters, 127, 185-188 https://doi.org/10.1016/0304-3940(91)90790-Z
 
Widenfalk Bertil, Wiberg Mikael (1989): Origin of sympathetic and sensory innervation of the knee joint. Anatomy and Embryology, 180, 317-323 https://doi.org/10.1007/BF00311164
 
Widenfalk Bertil, Wiberg Mikael (1990): Origin of sympathetic and sensory innervation of the temporo-mandibular joint. A retrograde axonal tracing study in the rat. Neuroscience Letters, 109, 30-35 https://doi.org/10.1016/0304-3940(90)90533-F
 
Widenfalk B., Elfvin L.-G., Wiberg M. (1988): Origin of sympathetic and sensory innervation of the elbow joint in the rat: A retrograde axonal tracing study with wheat germ agglutinin conjugated horseradish peroxidase. The Journal of Comparative Neurology, 271, 313-318 https://doi.org/10.1002/cne.902710302
 
Witoński D., Wągrowska-Danielewicz Małgorzata (1999): Distribution of substance-P nerve fibers in the knee joint in patients with anterior knee pain syndrome. Knee Surgery, Sports Traumatology, Arthroscopy, 7, 177-183 https://doi.org/10.1007/s001670050144
 
Wojtys Edward M., Beaman Douglas N., Glover Roy A., Janda David (1990): Innervation of the human knee joint by substance-P fibers. Arthroscopy: The Journal of Arthroscopic & Related Surgery, 6, 254-263 https://doi.org/10.1016/0749-8063(90)90054-H
 
Yoshida Niro, Nishiyama Keiji, Tonosaki Yoshikazu, Kikuchi Shinichi, Sugiura Yasuo (1995): Sympathetic and sensory innervation of the rat shoulder joint: a WGA-HRP tracing and CGRP immunohistochemical study. Anatomy and Embryology, 191, 465-469 https://doi.org/10.1007/BF00304431
 
Yoshida H., Fujita S., Nishida M., Iizuka T. (1999): The expression of substance P in human temporomandibular joint samples: an immunohistochemical study. Journal of Oral Rehabilitation, 26, 338-344 https://doi.org/10.1046/j.1365-2842.1999.00400.x
 
Yuan XP, Lin SX, Yuan SL, Qin BZ, Ma D (1994): Distribution, content and action site of leucine-enkephalin in pulmonary artery wall of rat and rabbit. Sheng Li Xue Bao 46, 381–389.
 
download PDF

© 2018 Czech Academy of Agricultural Sciences