Identification of neurogenic intestinal motility patterns in silver perch (Bidyanus bidyanus) that persist over wide temperature ranges.


Journal

Neurogastroenterology and motility
ISSN: 1365-2982
Titre abrégé: Neurogastroenterol Motil
Pays: England
ID NLM: 9432572

Informations de publication

Date de publication:
05 2021
Historique:
revised: 28 10 2020
received: 02 07 2020
accepted: 30 10 2020
pubmed: 20 12 2020
medline: 1 1 2022
entrez: 19 12 2020
Statut: ppublish

Résumé

Fish are increasingly being utilized as a model species for genetic manipulation studies related to gastrointestinal (GI) motility. Our aim was to identify whether patterns of GI motility in fish and the mechanisms underlying their generation are similar to those recorded from mammals (including humans). The entire intestine was removed from euthanized adult Silver Perch (n = 11) and lesioned at the midway point to obtain two equal lengths. Proximal and distal segments were studied separately in organ baths with oxygenated Krebs solution, maintained at either 15°C (n = 5) or 25°C (n = 6). Motility was analyzed during rest, after oral infusion of Krebs solution, and after application of hexamethonium (100 µM) and tetrodotoxin (TTX) (0.6 µM). Antegrade and retrograde propagating contractions (PC) were recorded in all preparations. In the proximal intestine, at 15 and 25°C, retrograde PCs occurred at 2.7 [1.7-4.5] and 3.1 [1.6-6.5] times the frequency of antegrade PCs, respectively. Colder temperatures did not inhibit PC frequency. Hexamethonium did not inhibit PC, and however, TTX abolished all contractile activity. Both neurogenic antegrade and retrograde propagating contractions occur throughout the intestine of Silver Perch. However, unlike the mammalian colon, these motor patterns do not require enteric nicotinic transmission and they are not inhibited by cold temperatures (15°C). Therefore, while the GI motility patterns in Silver Perch resemble those recorded from the colon of mammals, there may be differences in the mechanisms that underlying their generation.

Sections du résumé

BACKGROUND
Fish are increasingly being utilized as a model species for genetic manipulation studies related to gastrointestinal (GI) motility. Our aim was to identify whether patterns of GI motility in fish and the mechanisms underlying their generation are similar to those recorded from mammals (including humans).
METHODS
The entire intestine was removed from euthanized adult Silver Perch (n = 11) and lesioned at the midway point to obtain two equal lengths. Proximal and distal segments were studied separately in organ baths with oxygenated Krebs solution, maintained at either 15°C (n = 5) or 25°C (n = 6). Motility was analyzed during rest, after oral infusion of Krebs solution, and after application of hexamethonium (100 µM) and tetrodotoxin (TTX) (0.6 µM).
KEY RESULTS
Antegrade and retrograde propagating contractions (PC) were recorded in all preparations. In the proximal intestine, at 15 and 25°C, retrograde PCs occurred at 2.7 [1.7-4.5] and 3.1 [1.6-6.5] times the frequency of antegrade PCs, respectively. Colder temperatures did not inhibit PC frequency. Hexamethonium did not inhibit PC, and however, TTX abolished all contractile activity.
CONCLUSIONS AND INFERENCES
Both neurogenic antegrade and retrograde propagating contractions occur throughout the intestine of Silver Perch. However, unlike the mammalian colon, these motor patterns do not require enteric nicotinic transmission and they are not inhibited by cold temperatures (15°C). Therefore, while the GI motility patterns in Silver Perch resemble those recorded from the colon of mammals, there may be differences in the mechanisms that underlying their generation.

Identifiants

pubmed: 33340207
doi: 10.1111/nmo.14037
doi:

Substances chimiques

Isotonic Solutions 0
Krebs-Ringer solution 0
Nicotinic Antagonists 0
Sodium Channel Blockers 0
Hexamethonium 3C9PSP36Z2
Tetrodotoxin 4368-28-9

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14037

Informations de copyright

© 2020 John Wiley & Sons Ltd.

Références

Spencer NJ, Hu H. Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility. Nat Rev Gastroenterol Hepatol. 2020;17(6):338-351.
Davenport HW. Gastrointestinal physiology, 1895-1975: motility. Compr Physiol. 2011:1-101.
Jacobj C. Pharmakologische Untersuchung über das Colchicumgift (Pharmacological study of colchicum toxin). Archiv für experimentelle Pathologie und Pharmakologie. 1890;27(1-2):119-157.
Cannon WB. The movements of the intestines studied by means of the Rontgen rays. Am J Physiol. 1902;6:251-277.
Ehrlein HJ, Reich H, Schwinger M. Physiological significance of the contractions of the rabbit proximal colon. Q J Exp Physiol. 1982;67(3):407-417.
Dinning PG, Costa M, Brookes SJ, Spencer NJ. Neurogenic and myogenic motor patterns of rabbit proximal, mid, and distal colon. Am J Physiol Gastrointest Liver Physiol. 2012;303(1):G83-G92.
Hipper K, Ehrlein HJ. Motility of the large intestine and flow of digesta in pigs. Res Vet Sci. 2001;71(2):93-100.
Bedrich M, Ehrlein H. Motor function of the large intestine and flow of digesta in sheep. Small Ruminant Res. 2001;42:141-155.
Adler HF, Atkinson AJ, Ivy AC. A study of the motility of the human colon: an explanation of dysynergia of the colon, or of the “unstable colon”. Am J Dig Dis. 1941;8(6):197-202.
Bassotti G, Clementi M, Antonelli E, Pelli MA, Tonini M. Low-amplitude propagated contractile waves: a relevant propulsive mechanism of human colon. Dig Liver Dis. 2001;33(1):36-40.
Dinning PG, Wiklendt L, Maslen L, et al. Quantification of in vivo colonic motor patterns in healthy humans before and after a meal revealed by high-resolution fiber-optic manometry. Neurogastroenterol Motil. 2014;26(10):1443-1457.
Brijs J, Hennig GW, Grans A, Dekens E, Axelsson M, Olsson C. Exposure to seawater increases intestinal motility in euryhaline rainbow trout (Oncorhynchus mykiss). J Exp Biol. 2017;220(Pt 13):2397-2408.
Fujii K, Nakajo K, Egashira Y, et al. Gastrointestinal neurons expressing HCN4 regulate retrograde peristalsis. Cell Rep. 2020;30(9):2879-2888 e2873.
Ganz J, Baker RP, Hamilton MK, et al. Image velocimetry and spectral analysis enable quantitative characterization of larval zebrafish gut motility. Neurogastroenterol Motil. 2018;30(9):e13351.
Brijs J, Hennig GW, Axelsson M, Olsson C. Effects of feeding on in vivo motility patterns in the proximal intestine of shorthorn sculpin (Myoxocephalus scorpius). J Exp Biol. 2014;217(17):3015-3027.
Miegel R, Pain S, Van Wettere W, Howarth G, Stone D. Effect of water temperature on gut transit time, digestive enzyme activity and nutrient digestibility in yellowtail kingfish (Seriola lalandi). Aquaculture. 2010;308(3-4):145-151.
Burnstock G. Reversible inactivation of nervous activity in a fish gut. J Physiol. 1958;141(1):35.
Al-Hussaini A. On the functional morphology of the alimentary tract of some fish in relation to differences in their feeding habits: anatomy and histology. J Cell Sci. 1949;3(10):109-139.
Barlow C, McLoughlin R, Bock K. Complementary feeding habits of golden perch Macquaria ambigua (Richardson)(Percichthyidae) and silver perch Bidyanus bidyanus (Mitchell)(Teraponidae) in farm dams. Proc Linnean Soc NSW. 1987;109(3):143-152.
Mallen-Cooper M, Stuart I. Age, growth and non-flood recruitment of two potamodromous fishes in a large semi-arid/temperate river system. River Res Appl. 2003;19(7):697-719.
Hakim Y, Rowland SJ, Guy JA, Mifsud C, Uni Z, Harpaz S. Effects of genetic strain and holding facility on the characteristics of alkaline phosphatase and brush border enzymes in silver perch (Bidyanus bidyanus). Aquac Res. 2007;38(4):361-372.
Rowland SJ, Landos M, Callinan RB, et al.Development of a health management strategy for the silver perch aquaculture industry. NSW Department of Primary Industries - Fisheries Final Report Series. 2007;93.
de Abreu MS, Giacomini A, Sysoev M, et al. Modeling gut-brain interactions in zebrafish. Brain Res Bull. 2019;148:55-62.
Costa M, Dodds KN, Wiklendt L, Spencer NJ, Brookes SJ, Dinning PG. Neurogenic and myogenic motor activity in the colon of the guinea pig, mouse, rabbit, and rat. Am J Physiol Gastrointest Liver Physiol. 2013;305(10):G749-G759.
Froese R. Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. J Appl Ichthyol. 2006;22(4):241-253.
Bueno L, Ferre J-P, Ruckebusch Y. Effects of anesthesia and surgical procedures on intestinal myoelectric activity in rats. Am J Dig Dis. 1978;23(8):690-695.
Nilsson A, Fänge R. Digestive proteases in the holocephalian fish Chimaera monstrosa (L.). Comp Biochem Physiol. 1969;31(1):147-165.
Burnstock G. The effect of drugs on spontaneous motility and on response to stimulation of the extrinsic nerves of the gut of a teleostean fish. Br J Pharmacol Chemother. 1958;13(3):216-226.
Bürkner P-C. brms: an R package for Bayesian multilevel models using Stan. J Stat Softw. 2017;80(1):28.
Rich A, Gordon S, Brown C, et al. Kit signaling is required for development of coordinated motility patterns in zebrafish gastrointestinal tract. Zebrafish. 2013;10(2):154-160.
Karila P, Holmgren S. Enteric reflexes and nitric oxide in the fish intestine. J Exp Biol. 1995;198(11):2405-2412.
Kikuchi K, Noh H, Numayama-Tsuruta K, Ishikawa T. Mechanical roles of anterograde and retrograde intestinal peristalses after feeding in a larval fish (Danio rerio). Am J Physiol Gastrointest Liver Physiol. 2020;318(6):G1013-G1021.
Rønnestad I, Rojas-Garcia C, Skadal J. Retrograde peristalsis; a possible mechanism for filling the pyloric caeca? J Fish Biol. 2000;56(1):216-218.
Huizinga JD, Martz S, Gil V, Wang XY, Jimenez M, Parsons S. Two independent networks of interstitial cells of Cajal work cooperatively with the enteric nervous system to create colonic motor patterns. Front Neurosci. 2011;5:93.
Spencer NJ, Bywater RA. Enteric nerve stimulation evokes a premature colonic migrating motor complex in mouse. Neurogastroenterol Motil. 2002;14(6):657-665.
Nicholas S, Spencer NJ. Peristalsis and fecal pellet propulsion do not require nicotinic, purinergic, 5-HT3, or NK3 receptors in isolated guinea pig distal colon. Am J Physiol Gastrointest Liver Physiol. 2010;298(6):G952-G961.
Sia TC, Brookes SJ, Dinning PG, Wattchow DA, Spencer NJ. Peristalsis and propulsion of colonic content can occur after blockade of major neuroneuronal and neuromuscular transmitters in isolated guinea pig colon. Am J Physiol Gastrointest Liver Physiol. 2013;305(12):G933-G939.
Kuizenga MH, Sia TC, Dodds KN, et al. Neurally mediated propagating discrete clustered contractions superimposed on myogenic ripples in ex vivo segments of human ileum. Am J Physiol Gastrointest Liver Physiol. 2015;308(1):G1-G11.
Chen JH, Zhang Q, Yu Y, et al. Neurogenic and myogenic properties of pan-colonic motor patterns and their spatiotemporal organization in rats. PLoS One. 2013;8(4):e60474.
Mane N, Jimenez M. Interplay between myogenic pacemakers and enteric neurons determine distinct motor patterns in the rat colon. Neurogastroenterol Motil. 2014;26(10):1508-1512.
Singh S, Sharma J, Ahmad T, Chakrabarti R. Effect of water temperature on the physiological responses of Asian catfish Clarias batrachus (Linnaeus 1758). Asian Fisheries Sci. 2013;26(1):26-38.
Handeland SO, Imsland AK, Stefansson SO. The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts. Aquaculture. 2008;283(1-4):36-42.
Gräns A, Seth H, Axelsson M, et al. Effects of acute temperature changes on gut physiology in two species of sculpin from the west coast of Greenland. Polar Biol. 2013;36(6):775-785.
Rowland SJ, Allan GL, Hollis M, Pontifex T. Production of the Australian freshwater silver perch, Bidyanus bidyanus (Mitchell), at two densities in earthen ponds. Aquaculture. 1995;130(4):317-328.

Auteurs

Bradley S Jones (BS)

College of Science & Engineering, Flinders University, Adelaide, SA, Australia.

Lauren J Keightley (LJ)

College of Medicine & Public Health, Flinders University, Adelaide, SA, Australia.

James O Harris (JO)

College of Science & Engineering, Flinders University, Adelaide, SA, Australia.

Lukasz Wiklendt (L)

College of Medicine & Public Health, Flinders University, Adelaide, SA, Australia.

Nick J Spencer (NJ)

College of Medicine & Public Health, Flinders University, Adelaide, SA, Australia.

Phil G Dinning (PG)

College of Medicine & Public Health, Flinders University, Adelaide, SA, Australia.
Department of Surgery and Gastroenterology, Flinders Medical Centre, Bedford Park, SA, Australia.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH