Ukr.Biochem.J. 2017; Volume 89, Issue 4, Jul-Aug, pp. 56-67
doi: https://doi.org/10.15407/ubj89.04.056
Role of peripheral dopaminergic system in the pathogenesis of experimental colitis in rats
A. I. Prysiazhniuk, M. P. Rudyk, T. M. Chervinska, T. V. Dovbynchuk,
I. V. Opeida, L. M. Skivka, G. M. Tolstanova
Taras Shevchenko National University of Kyiv, Ukraine;
e-mail: gtolstanova@gmail.com
Dopamine (DA) is produced and released by immune cells. Recent data pointed to DA as a key mediator between the nervous and immune systems. In the present study we tested the hypothesis that peripheral dopaminergic system plays a negative role in ulcerative colitis pathogenesis via the effect on activity of peripheral blood phagocytes. The study was conducted on male Wistar rats (170-200 g). The peripheral dopaminergic system was destroyed by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) injection (20 mg/kg, s.c., 4 times every 2 h). Colitis was induced by 0.1 ml 6% iodoacetamide enema. Rats were subjected to autopsy on the 18th day. We found that MPTP-treated rats had decreased levels of tyrosine hydroxylase, rate-limiting enzyme of DA synthesis, in colon but not in brain. The number and activity of colonic and peripheral blood granulocytes did not significantly differ in saline- and MPTP-treated rats with colitis. The decreased ROS production by monocytes; increased 1.8-fold the number of CD69 (an early activation marker) positive monocytes and 6-fold intensity of CD69 surface expression were observed in MPTP-treated rats vs. saline-treated rats during colitis. The CD14 (the endotoxin coreceptor of phagocytes) surface expression was 2-fold increased in MPTP-treated rats without colitis, but significantly decreased in both saline- and MPTP-treated rats with colitis. We showed for the first time that the destruction of peripheral dopaminergic neurons leads to the improvement of morphological signs of experimental colitis, which might be through the regulatory effect of dopaminergic system on monocytes phenotype and their respiratory burst activity.
Keywords: CD14, CD69, dopaminergic system, granulocytes, monocytes, ulcerative colitis in rats
References:
- Pacheco R, Contreras F, Zouali M. The dopaminergic system in autoimmune diseases. Proceedings of ICI Milan. 2013; 2014: 132.
- Eisenhofer G, Aneman A, Friberg P, Hooper D, Fåndriks L, Lonroth H, Hunyady B, Mezey E. Substantial production of dopamine in the human gastrointestinal tract. J Clin Endocrinol Metab. 1997 Nov;82(11):3864-71. PubMed, CrossRef
- Eaker EY, Bixler GB, Dunn AJ, Moreshead WV, Mathias JR. Dopamine and norepinephrine in the gastrointestinal tract of mice and the effects of neurotoxins. J Pharmacol Exp Ther. 1988 Feb;244(2):438-42. PubMed
- Eldrup E, Richter EA, Christensen NJ. DOPA, norepinephrine, and dopamine in rat tissues: no effect of sympathectomy on muscle DOPA. Am J Physiol. 1989 Feb;256(2 Pt 1):E284-7. PubMed
- Li ZS, Schmauss C, Cuenca A, Ratcliffe E, Gershon MD. Physiological modulation of intestinal motility by enteric dopaminergic neurons and the D2 receptor: analysis of dopamine receptor expression, location, development, and function in wild-type and knock-out mice. J Neurosci. 2006 Mar 8;26(10):2798-807. PubMed, CrossRef
- Seol IW, Kuo NY, Kim KM. Effects of dopaminergic drugs on the mast cell degranulation and nitric oxide generation in RAW 264.7 cells. Arch Pharm Res. 2004 Jan;27(1):94-8. PubMed, CrossRef
- Basu S, Nagy JA, Pal S, Vasile E, Eckelhoefer IA, Bliss VS, Manseau EJ, Dasgupta PS, Dvorak HF, Mukhopadhyay D. The neurotransmitter dopamine inhibits angiogenesis induced by vascular permeability factor/vascular endothelial growth factor. Nat Med. 2001 May;7(5):569-74. PubMed, CrossRef
- Basu S, Sarkar C, Chakroborty D, Nagy J, Mitra RB, Dasgupta PS, Mukhopadhyay D. Ablation of peripheral dopaminergic nerves stimulates malignant tumor growth by inducing vascular permeability factor/vascular endothelial growth factor-mediated angiogenesis. Cancer Res. 2004 Aug 15;64(16):5551-5. PubMed, CrossRef
- Chakroborty D, Sarkar C, Yu H, Wang J, Liu Z, Dasgupta PS, Basu S. Dopamine stabilizes tumor blood vessels by up-regulating angiopoietin 1 expression in pericytes and Kruppel-like factor-2 expression in tumor endothelial cells. Proc Natl Acad Sci USA. 2011 Dec 20;108(51):20730-5. PubMed, PubMedCentral, CrossRef
- Gomez R, Gonzalez-Izquierdo M, Zimmermann RC, Novella-Maestre E, Alonso-Muriel I, Sanchez-Criado J, Remohi J, Simon C, Pellicer A. Low-dose dopamine agonist administration blocks vascular endothelial growth factor (VEGF)-mediated vascular hyperpermeability without altering VEGF receptor 2-dependent luteal angiogenesis in a rat ovarian hyperstimulation model. Endocrinology. 2006 Nov;147(11):5400-11. PubMed, CrossRef
- Magro F, Vieira-Coelho MA, Fraga S, Serrão MP, Veloso FT, Ribeiro T, Soares-da-Silva P. Impaired synthesis or cellular storage of norepinephrine, dopamine, and 5-hydroxytryptamine in human inflammatory bowel disease. Dig Dis Sci. 2002 Jan;47(1):216-24. PubMed
- Magro F, Fraga S, Ribeiro T, Soares-da-Silva P. Decreased availability of intestinal dopamine in transmural colitis may relate to inhibitory effects of interferon-gamma upon L-DOPA uptake. Acta Physiol Scand. 2004 Apr;180(4):379-86. PubMed, CrossRef
- Magro F, Cunha E, Araujo F, Meireles E, Pereira P, Dinis-Ribeiro M, Veloso FT, Medeiros R, Soares-da-Silva P. Dopamine D2 receptor polymorphisms in inflammatory bowel disease and the refractory response to treatment. Dig Dis Sci. 2006 Nov;51(11):2039-44. PubMed, CrossRef
- Tolstanova G, Deng X, Ahluwalia A, Paunovic B, Prysiazhniuk A, Ostapchenko L, Tarnawski A, Sandor Z, Szabo S. Role of Dopamine and D2 Dopamine Receptor in the Pathogenesis of Inflammatory Bowel Disease. Dig Dis Sci. 2015 Oct;60(10):2963-75. PubMed, CrossRef
- Szabo S, Horner HC, Maull H, Schnoor J, Chiueh CC, Palkovits M. Biochemical changes in tissue catecholamines and serotonin in duodenal ulceration caused by cysteamine or propionitrile in the rat. J Pharmacol Exp Ther. 1987 Mar;240(3):871-8. PubMed
- Prysiazhniuk A., Dovbynchuk T., Kopiyak B., Kompanets I., Tolstanova G. The role of central and peripheral D2R receptors in the mechanism of colonic vascular permeability during experimental colitis in rats. Bull Taras Shevchenko Nat Univ Kyiv, Series: Probl Physiol Funct Regul. 2017; 1(22): 44-48.
- Anderson G, Noorian AR, Taylor G, Anitha M, Bernhard D, Srinivasan S, Greene JG. Loss of enteric dopaminergic neurons and associated changes in colon motility in an MPTP mouse model of Parkinson’s disease. Exp Neurol. 2007 Sep;207(1):4-12. PubMed, PubMedCentral, CrossRef
- Beregovyi SM, Chervinska TM, Dranitsina AS, Szabo S, Tolstanova GM. Redox-sensitive transcription factors Egr-1 and Sp1 in the pathogenesis of experimental gastric ulcer. Ukr Biochem J. 2015 Jul-Aug;87(4):70-7. PubMed, CrossRef
- Skivka LM, Fedorchuk OG, Rudyk MP, Pozur VV, Khranovska NM, Grom MY, Nowicky JW. Antineoplastic drug NSC631570 modulates functions of hypoxic macrophages. Tsitol Genet. 2013 Sep-Oct;47(5):70-82. PubMed
- Skivka LM, Fedorchuk OG, Susak YM, Susak MY, Malanchuk OM, Rudyk MP, Nowicky YW. Physical activity interferes with the immunomodulatory effect of the antineoplastic drug NSC631570. Curr Pharm Biotechnol. 2015;16(1):49-59. PubMed, CrossRef
- Shapiro H, Lutaty A, Ariel A. Macrophages, meta-inflammation, and immuno-metabolism. Sci World J. 2011;11:2509-29. PubMed, PubMedCentral, CrossRef
- Beaulieu JM, Gainetdinov RR. The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol Rev. 2011 Mar;63(1):182-217. PubMed, CrossRef
- Mezey E, Eisenhofer G, Hansson S, Harta G, Hoffman BJ, Gallatz K, Palkovits M, Hunyady B. Non-neuronal dopamine in the gastrointestinal system. Clin Exp Pharmacol Physiol Suppl. 1999 Apr;26:S14-22. PubMed
- Yamamoto C, Kawana E. Immunohistochemical detection of GABA in rat striatum by intraperitoneal injection of MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine). Okajimas Folia Anat Jpn. 1991 Dec;68(5):271-82. PubMed, CrossRef
- Natale G, Kastsiushenka O, Fulceri F, Ruggieri S, Paparelli A, Fornai F. MPTP-induced parkinsonism extends to a subclass of TH-positive neurons in the gut. Brain Res. 2010 Oct 8;1355:195-206. PubMed, CrossRef
- Ampe B, Anissa EA, Michotte Y, Sarre S. Dopaminergic Control of the Neurotransmitter Release in the Subthalamic Nucleus: Implications for Parkinson’s Disease Treatment Strategies. Etiology and Pathophysiology of Parkinson’s Disease. Ed. Prof. Abdul Qqyyum Rana. InTech, 2011. P. 421-433. CrossRef
- Kmieć Z, Cyman M, Ślebioda TJ. Cells of the innate and adaptive immunity and their interactions in inflammatory bowel disease. Adv Med Sci. 2017 Mar;62(1):1-16. PubMed, CrossRef
- de Lange KM, Barrett JC. Understanding inflammatory bowel disease via immunogenetics. J Autoimmun. 2015 Nov;64:91-100. PubMed, CrossRef
- Katsanos KH, Papadakis KA. Inflammatory Bowel Disease: Updates on Molecular Targets for Biologics. Gut Liver. 2017 Jul 15;11(4):455-463. PubMed, CrossRef
- Pinoli M, Marino F, Cosentino M. Dopaminergic Regulation of Innate Immunity: a Review. J Neuroimmune Pharmacol. 2017 Jun 3: 1-22. PubMed, CrossRef
- Sarkar C, Basu B, Chakroborty D, Dasgupta PS, Basu S. The immunoregulatory role of dopamine: an update. Brain Behav Immun. 2010 May;24(4):525-8. PubMed, PubMedCentral, CrossRef
- Kumar V, Sharma A. Neutrophils: Cinderella of innate immune system. Int Immunopharmacol. 2010 Nov;10(11):1325-34. PubMed, CrossRef
- Yamazaki M, Matsuoka T, Yasui K, Komiyama A, Akabane T. Dopamine inhibition of superoxide anion production by polymorphonuclear leukocytes. J Allergy Clin Immunol. 1989 May;83(5):967-72. PubMed, CrossRef
- Trabold B, Gruber M, Fröhlich D. Functional and phenotypic changes in polymorphonuclear neutrophils induced by catecholamines. Scand Cardiovasc J. 2007 Jan;41(1):59-64. PubMed, CrossRef
- Radulovic K, Niess JH. CD69 is the crucial regulator of intestinal inflammation: a new target molecule for IBD treatment? J Immunol Res. 2015;2015:497056. PubMed, PubMedCentral, CrossRef
- Yamauchi K, Kasuya Y, Kuroda F, Tanaka K, Tsuyusaki J, Ishizaki S, Matsunaga H, Iwamura C, Nakayama T, Tatsumi K. Attenuation of lung inflammation and fibrosis in CD69-deficient mice after intratracheal bleomycin. Respir Res. 2011 Oct 5;12:131. PubMed, PubMedCentral, CrossRef
- Bergquist J, Ohlsson B, Tarkowski A. Nuclear factor-kappa B is involved in the catecholaminergic suppression of immunocompetent cells. Ann N Y Acad Sci. 2000;917:281-9. PubMed, CrossRef
- Yan Y, Jiang W, Liu L, Wang X, Ding C, Tian Z, Zhou R. Dopamine controls systemic inflammation through inhibition of NLRP3 inflammasome. Cell. 2015 Jan 15;160(1-2):62-73. PubMed, CrossRef
This work is licensed under a Creative Commons Attribution 4.0 International License.