1. bookVolume 67 (2017): Issue 3 (September 2017)
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eISSN
1820-7448
First Published
25 Mar 2014
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4 times per year
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English
access type Open Access

An Immunohistochemical Study of Cocaine- and Amphetamine-Regulated Transcript (Cart) Expression in the Pterygopalatine Ganglion of the Pig

Published Online: 23 Sep 2017
Volume & Issue: Volume 67 (2017) - Issue 3 (September 2017)
Page range: 397 - 408
Received: 17 Jan 2017
Accepted: 04 May 2017
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
Abstract

Although, a great effort has been made to understand the synthesis, regulation, processing and function of cocaine- and amphetamine-regulated transcript (CART) peptide at the central level, its peripheral function(s) are still obscure. Moreover, scarce studies describing the presence of CART in peripheral autonomic ganglia are mainly limited to laboratory rodents. Thus, the aim of the present study was to immunohistochemically investigate the expression of CART in Hu C/D-positive neurons of the porcine pterygopalatine ganglion (PPG). The distribution pattern of CART-IR nerve elements in PPG has been also assessed. The co-localization of CART with substance P (SP), galanin or somatostatin was studied by means of double immunohistochemical stainings. The presence of Hu C/D-positive/CART-positive neurons was detected both in the left and right PPG (4.7±1.2% and 5.2% ± 1.4%, respectively). The CARTimmunoreactive (IR) neurons were categorized as either middle (ca. 80%) or small (ca. 20%) in size. Moderate numbers of CART-IR boutons were also detected between CART-negative ganglionic neurons. CART-IR basket-like formations around PPG neurons were regularly observed. Virtually all CART-IR neurons additionally co-stored VIP, whereas none of the CART-expressing cells showed the presence of galanin, SP or somatostatin. CART-IR basket-like formations exclusively encircled VIP-IR PPG neurons. Thus, CART-IR nerve cells seem to constitute a relatively small homologous population of the porcine PPG neurons with largely unknown functions. Further functional studies aiming at whether CART-IR neurons could serve as interneurons are necessary.

Keywords

1. ten Tusscher MP, Klooster J, Vrensen GF: The innervation of the rabbit’s anterior eye segment: a retrograde tracing study. Exp Eye Res 1998, 46:717-730.10.1016/S0014-4835(88)80058-7Search in Google Scholar

2. Oyagi S, Ito J, Honjo I: The origin of autonomic nerves of the Eustachian tube as studied by the horseradish peroxidase tracer method. Acta Otolaryngol 1988, 105:266-272.10.3109/00016488809097007Search in Google Scholar

3. Shiotani Y, Yamano M, Shiosaka S, Emson PC, Hillyard CJ, Girgis S, MacIntyre I: Distribution and origins of substance P (SP)-, calcitonin gene-related peptide (CGRP)-, vasoactive intestinal polypeptide (VIP)- and neuropeptide Y (NPY)-containing nerve fibers in the pineal gland of gerbils. Neurosci Lett 1986, 70:187-192.10.1016/0304-3940(86)90461-1Search in Google Scholar

4. Cuthbertson S, LeDoux MS, Jones S, Jones J, Zhou Q, Gong S, Ryan P, Reiner A: Localization of preganglionic neurons that innervate choroidal neurons of pterygopalatine ganglion. Invest Ophthalmol Vis Sci 2003, 44:3713-3724.10.1167/iovs.02-120712939284Search in Google Scholar

5. Beckers HJ, Klooster J, Vrensen GF, Lamers WP: Facial parasympathetic innervation of the rat choroid, lacrimal glands and ciliary ganglion. An ultrastructural pterygopalatine tracing and immunohistochemical study. Ophthalmic Res 1993, 25:319-330.10.1159/0002673328259266Search in Google Scholar

6. Li C, Fitzgerald ME, Del Mar N, Cuthbertson-Coates S, LeDoux MS, Gong S, Ryan JP, Reiner A: The identification and neurochemical characterization of central neurons that target parasympathetic preganglionic neurons involved in the regulation of choroidal blood flow in the rat eye using pseudorabies virus, immunolabeling and conventional pathway tracing methods. Front Neuroanat 2015, 9:65.10.3389/fnana.2015.00065445158126082687Search in Google Scholar

7. Szczurkowski A, Sienkiewicz W, Kuchinka J, Kaleczyc J: Morphology and immunohistochemical characteristics of the pterygopalatine ganglion in the chinchilla (Chinchilla laniger, Molina). Pol J Vet Sci 2013, 16:359-368.10.2478/pjvs-2013-004823971205Search in Google Scholar

8. Shimizu T, Morris JL, Gibbins IL: Expression of immunoreactivity to neurokinin-1 receptor by subsets of cranial parasympathetic neurons: correlation with neuropeptides, nitric oxide synthase, and pathways. Exp Neurol 2001, 172:293-306.10.1006/exnr.2001.779911716554Search in Google Scholar

9. Motosugi H: Immunohistochemical observation of neurotransmitters in rat and human pterygopalatine ganglia. Nihon Jibiinkoka Gakkai Kaiho 1993, 96:936-945.10.3950/jibiinkoka.96.9368102178Search in Google Scholar

10. Liu J, Evans MS, Brewer GJ, Lee TJ: N-type Ca2+ channels in cultured rat sphenopalatine ganglion neurons: an immunohistochemical and electrophysiological study. J Cereb Blood Flow Metab 2000, 1:183-191.10.1097/00004647-200001000-0002310616807Search in Google Scholar

11. Podlasz P, Wąsowicz K, Kaleczyc J, Łakomy M, Bukowski R: Localization of immunoreactivities for neuropeptides and neurotransmitter-synthesizing enzymes in the pterygopalatine ganglion of the pig. Vet Med - Czech 2003, 48:99-107.10.17221/5756-VETMEDSearch in Google Scholar

12. Ivanusic JJ, Goulding KE, Kwok MM, Jennings EA: Neurochemical classifi cation and projection targets of CART peptide immunoreactive neurons in sensory and parasympathetic ganglia of the head. Neuropeptides 2012, 46:55-60.10.1016/j.npep.2011.09.00222005173Search in Google Scholar

13. Radzimirska M, Bogus-Nowakowska K, Kuder T, Robak A: Distribution of cocaine- and amphetamine-regulated transcript (CART), neuropeptide Y (NPY) and galanin (GAL) in the pterygopalatine ganglion of the domestic duck (Anas platyrhynchos f. domestica). Folia Histochem Cytobiol 2016, 54:25-31.10.5603/FHC.a2016.000227044589Search in Google Scholar

14. Rogge G, Jones D, Hubert GW, Lin Y, Kuhar MJ: CART peptides: regulators of body weight, reward and other functions. Nat Rev Neurosci 2008, 9:747-758.10.1038/nrn2493441845618802445Search in Google Scholar

15. Arciszewski MB, Zacharko-Siembida A: A co-localization study on the ovine pancreas innervation. Ann Anat 2007,189:157-67.10.1016/j.aanat.2006.09.00217419548Search in Google Scholar

16. Richardson RJ, Grkovic I, Anderson CR: Cocaine- and amphetamine-related transcript peptide and somatostatin in rat intracardiac ganglia. Cell Tissue Res 2006, 324:17-24.10.1007/s00441-005-0087-y16374620Search in Google Scholar

17. Równiak M, Robak A, Bogus-Nowakowska K, Wasilewska B, Najdzion J, Majewski M: The cocaine- and amphetamine-regulated transcript (CART) immunoreactivity in the amygdala of the pig. Anat Histol Embryol 2010, 39:385-397.10.1111/j.1439-0264.2010.01006.x20594191Search in Google Scholar

18. Kolenkiewicz M, Robak A, Równiak M, Bogus-Nowakowska K, Całka J, Majewski M: Distribution of cocaine- and amphetamine-regulated transcript in the hippocampal formation of the guinea pig and domestic pig. Folia Morphol (Warsz) 2009, 68:23-31.Search in Google Scholar

19. Bogus-Nowakowska K, Robak A, Równiak M, Wasilewska B, Najdzion J, Kolenkiewicz M, Zakowski W, Majewski M: Distribution and chemical coding pattern of the cocaine- and amphetamine-regulated transcript (CART) immunoreactivity in the preoptic area of the pig. Folia Histochem Cytobiol 2011, 49:604-614.10.5603/FHC.2011.008322252754Search in Google Scholar

20. Fenwick NM, Martin CL, Llewellyn-Smith IJ: Immunoreactivity for cocaine- and amphetamine-regulated transcript in rat sympathetic preganglionic neurons projecting to sympathetic ganglia and the adrenal medulla. J Comp Neurol 2006, 495:422-433.10.1002/cne.2087016485287Search in Google Scholar

21. Kozsurek M, Lukácsi E, Fekete C, Wittmann G, Réthelyi M, Puskár Z: Cocaine- and amphetamine-regulated transcript peptide (CART) is present in peptidergic C primary afferents and axons of excitatory interneurons with a possible role in nociception in the superficial laminae of the rat spinal cord. Eur J Neurosci 2007, 26:1624-1631.10.1111/j.1460-9568.2007.05789.x17880396Search in Google Scholar

22. Ellis LM, Mawe GM: Distribution and chemical coding of cocaine- and amphetamineregulated transcript peptide (CART)-immunoreactive neurons in the guinea pig bowel. Cell Tissue Res 2003, 312:265-274.10.1007/s00441-002-0678-9Search in Google Scholar

23. Iliff JJ, Alkayed NJ, Gloshani KJ, Traystman RJ, West GA: Cocaine- and amphetamineregulated transcript (CART) peptide: a vasoactive role in the cerebral circulation. J Cereb Blood Flow Metab 2005, 25:1376-1385.10.1038/sj.jcbfm.9600136Search in Google Scholar

24. Banke E, Riva M, Shcherbina L, Wierup N, Degerman E: Cocaine- and amphetamineregulated transcript is expressed in adipocytes and regulate lipid- and glucose homeostasis. Regul Pept 2013, 182:35-40.10.1016/j.regpep.2012.12.011Search in Google Scholar

25. Wierup N, Gunnarsdóttir A, Ekblad E, Sundler F: Characterisation of CART-containing neurons and cells in the porcine pancreas, gastro-intestinal tract, adrenal and thyroid glands. BMC Neurosci 2007, 8:51.10.1186/1471-2202-8-51Search in Google Scholar

26. Arciszewski MB, Barabasz S, Skobowiat C, Maksymowicz W, Majewski M: Immunodetection of cocaine- and amphetamine-regulated transcript in the rumen, reticulum, omasum and abomasum of the sheep. Anat Histol Embryol 2009, 38:62-67.10.1111/j.1439-0264.2008.00893.xSearch in Google Scholar

27. Wojtkiewicz J, Gonkowski S, Bladowski M, Majewski M: Characterisation of cocaine- and amphetamine- regulated transcript-like immunoreactive (CART-LI) enteric neurons in the porcine small intestine. Acta Vet Hung 2012, 60:371-381.10.1556/avet.2012.032Search in Google Scholar

28. Bulc M, Gonkowski S, Landowski P, Kamińska B, Całka J: Immunohistochemical evidence of the co-localisation of cocaine and amphetamine regulatory peptide with neuronal isoform of nitric oxide synthase, vasoactive intestinal peptide and galanin within the circular muscle layer of the human caecum. Folia Morphol (Warsz) 2015, 74:176-182.10.5603/FM.2015.0028Search in Google Scholar

29. Dartt DA, Baker AK, Vaillant C, Rose PE: Vasoactive intestinal polypeptide stimulation of protein secretion from rat lacrimal gland acini. Am J Physiol 1984, 247:G502-G509.10.1152/ajpgi.1984.247.5.G502Search in Google Scholar

30. Grimes PA, McGlinn AM, Koeberlein B, Stone RA: Galanin immunoreactivity in autonomic innervation of the cat eye. J Comp Neurol 1994, 348:234-243.10.1002/cne.903480206Search in Google Scholar

31. Adeghate E, Singh J: Immunohistochemical identifi cation of galanin and leucin-enkephalin in the porcine lacrimal gland. Neuropeptides 1994, 27:285-289.10.1016/0143-4179(94)90109-0Search in Google Scholar

32. Nishimura T, Akasu T: Galanin causes presynaptic inhibition of cholinergic transmission in rabbit parasympathetic ganglia. Kurume Med J 1995, 42:45-48.10.2739/kurumemedj.42.45Search in Google Scholar

33. Parsons RL, Mulvaney JM, Merriam LA: Galanin activates an inwardly rectifying potassium conductance and inhibits a voltage-dependent calcium conductance in mudpuppy parasympathetic neurons. Ann N Y Acad Sci 1998, 863:156-169.10.1111/j.1749-6632.1998.tb10692.xSearch in Google Scholar

34. Beckers HJ, Klooster J, Vrensen GF, Lamers WP: Ultrastructural identifi cation of trigeminal nerve terminals in the pterygopalatine ganglion of rats: an anterograde tracing and immunohistochemical study. Brain Res 1991, 557:22-30.10.1016/0006-8993(91)90111-8Search in Google Scholar

35. Pidsudko Z, Kaleczyc J, Wasowicz K, Sienkiewicz W, Majewski M, Zajac W, Lakomy M: Distribution and chemical coding of intramural neurons in the porcine ileum during proliferative enteropathy. J Comp Pathol 2008, 138:23-31.10.1016/j.jcpa.2007.09.00318061202Search in Google Scholar

36. Pidsudko Z: Immunohistochemical characteristics and distribution of sensory dorsal root Ganglia neurons supplying the urinary bladder in the male pig. J Mol Neurosci 2014, 52:71-81.10.1007/s12031-013-0117-224048739Search in Google Scholar

37. Zacharko-Siembida A, Arciszewski MB: Cocaine- and amphetamine-regulated transcriptlike immunoreactivity (CART-LI) in intramural ganglia of porcine urinary bladder trigone. Med Weter 2014, 70:594-598.Search in Google Scholar

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