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Parasites and the neuroendocrine control of fish intestinal function: an ancient struggle between pathogens and host

Published online by Cambridge University Press:  16 August 2022

Giampaolo Bosi
Affiliation:
Department of Veterinary Medicine and Animal Science, University of Milan, St. dell'Università 6, 26900 Lodi, Italy
Barbara J. Maynard
Affiliation:
The Institute for Learning and Teaching, Colorado State University, Fort Collins, CO 80523, USA
Flavio Pironi
Affiliation:
Department of Life Sciences and Biotechnology, University of Ferrara, St. Borsari 46, 44121 Ferrara, Italy
Bahram Sayyaf Dezfuli*
Affiliation:
Department of Life Sciences and Biotechnology, University of Ferrara, St. Borsari 46, 44121 Ferrara, Italy
*
Author for correspondence: Bahram Sayyaf Dezfuli, E-mail: dzb@unife.it

Abstract

Most individual fish in wild and farmed populations can be infected with parasites. Fish intestines can harbour protozoans, myxozoans and helminths, which include several species of digeneans, cestodes, nematodes and acanthocephalans. Enteric parasites often induce inflammation of the intestine; the pathogen provokes changes in the host physiology, which will be genetically selected for if they benefit the parasite. The host response to intestinal parasites involves neural, endocrine and immune systems and interaction among these systems is coordinated by hormones, chemokines, cytokines and neurotransmitters including peptides. Intestinal fish parasites have effects on the components of the enteric nervous and endocrine systems; mechanical/chemical changes impair the activity of these systems, including gut motility and digestion. Investigations on the role of the neuroendocrine system in response to fish intestinal parasites are very few. This paper provides immunohistochemical and ultrastructural data on effects of parasites on the enteric nervous system and the enteric endocrine system in several fish–parasite systems. Emphasis is on the occurrence of 21 molecules including cholecystokinin-8, neuropeptide Y, enkephalins, galanin, vasoactive intestinal peptide and serotonin in infected tissues.

Type
Review Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Adamo, SA (2002) Modulating the modulators: parasites, neuromodulators and host behavioural change. Brain Behavior and Evolution 60, 370377.CrossRefGoogle Scholar
Ahlman, H and Nilsson, O (2001) The gut as the largest endocrine organ in the body. Annals of Oncology 12, S63S68.CrossRefGoogle Scholar
Aldegunde, M and Mancebo, M (2006) Effects of neuropeptide Y on food intake and brain biogenic amines in the rainbow trout (Oncorhynchus mykiss). Peptides 27, 719727.CrossRefGoogle ScholarPubMed
Aldman, G and Holmgren, S (1995) Intraduodenal fat and amino acids activate gallbladder motility in the rainbow trout, Oncorhynchus mykiss. General and Comparative Endocrinology 100, 2732.CrossRefGoogle ScholarPubMed
Anderson, RC (2000) Nematode Parasites of Vertebrates: Their Development and Transmission. Wallingford, UK: CABI Publishing.CrossRefGoogle Scholar
Anderson, C and Campbell, G (1988) Immunohistochemical study of 5-HT-containing neurons in the teleost intestine: relationship to the presence of enterochromaffin cells. Cell and Tissue Research 254, 553599.CrossRefGoogle Scholar
Bahlool, QZM, Skovgaard, A, Kania, P, Haarder, S and Buchmann, K (2012) Microhabitat preference of Anisakis simplex in three salmonid species: immunological implications. Veterinary Parasitology 190, 489495.CrossRefGoogle ScholarPubMed
Bahlool, QZM, Skovgaard, A, Kania, PW and Buchmann, K (2013) Effects of excretory/secretory products from Anisakis simplex (Nematoda) on immune gene expression in rainbow trout (Oncorhynchus mykiss). Fish & Shellfish Immunology 35, 734739.CrossRefGoogle ScholarPubMed
Bakke, AM, Glover, C and Krogdahl, Å (2010) Feeding, digestion and absorption of nutrients. Fish Physiology 30, 57110.CrossRefGoogle Scholar
Barber, I and Huntingford, FA (1995) The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 132, 12231240.CrossRefGoogle Scholar
Barber, I and Wright, HA (2005) Effects of parasites on fish behaviour: interactions with host physiology. Fish Physiology 24, 110149.Google Scholar
Barber, I, Mora, AB, Payne, EM, Weinersmith, KL and Sih, A (2017) Parasitism, personality and cognition in fish. Behavioural Processes 141, 205219.CrossRefGoogle ScholarPubMed
Barry, J, McLeish, J, Dodd, JA, Turnbull, JF, Boylan, P and Adams, CE (2014) Introduced parasite Anguillicola crassus infection significantly impedes swim bladder function in the European eel Anguilla anguilla (L). Journal of Fish Diseases 37, 921924.CrossRefGoogle ScholarPubMed
Beach, MA, McVean, A, Roberts, MG and Thorndyke, MC (1988) The effects of bombesin on the feeding of fish. Neuroscience Letters 32, S46.Google Scholar
Bermúdez, R, Vigliano, F, Quiroga, MI, Nieto, JM, Bosi, G and Domeneghini, C (2007) Immunohistochemical study on the neuroendocrine system of the digestive tract of turbot, Scophthalmus maximus (L.), infected by Enteromyxum scophthalmi (Myxozoa). Fish & Shellfish Immunology 22, 252263.CrossRefGoogle Scholar
Blanco, AM, Bertucci, JI, Valenciano, AI, Delgado, MJ and Unniappan, S (2017) Ghrelin suppresses cholecystokinin (CCK), peptide YY (PYY) and glucagon-like peptide-1 (GLP-1) in the intestine, and attenuates the anorectic effects of CCK, PYY and GLP-1 in goldfish (Carassius auratus). Hormones and Behavior 93, 6271.CrossRefGoogle ScholarPubMed
Blanco, AM, Calo, J and Soengas, JL (2021) The gut–brain axis in vertebrates: implications for food intake regulation. Journal of Experimental Biology 224, jeb231571.CrossRefGoogle ScholarPubMed
Bohórquez, DV and Liddle, RA (2015) Gastrointestinal hormones and neurotransmitters. In Feldman, M, Friedman, LS and Brandt, LJ (eds), Sleisenger and Fortran's Gastrointestinal and Liver Disease. Philadelphia, PA, USA: Saunders/Elsevier, pp. 3654.Google Scholar
Bosi, G, Di Giancamillo, A, Arrighi, S and Domeneghini, C (2004) An immunohistochemical study on the neuroendocrine system in the alimentary canal of the brown trout, Salmo trutta, L., 1758. General and Comparative Endocrinology 138, 166181.CrossRefGoogle Scholar
Bosi, G, Shinn, AP, Giari, L, Simoni, E, Pironi, F and Dezfuli, BS (2005a) Changes in the neuromodulators of the diffuse endocrine system of the alimentary canal of farmed rainbow trout, Oncorhynchus mykiss (Walbaum), naturally infected with Eubothrium crassum (Cestoda). Journal of Fish Diseases 28, 703711.CrossRefGoogle ScholarPubMed
Bosi, G, Domeneghini, C, Arrighi, S, Giari, L, Simoni, E and Dezfuli, BS (2005b) Response of the gut neuroendocrine system of Leuciscus cephalus (L.) to the presence of Pomphorhynchus laevis Müller, 1776 (Acanthocephala). Histology and Histopathology 20, 509518.Google Scholar
Bosi, G, Shinn, AP, Simoni, E, Arrighi, S and Domeneghini, C (2006) A comparative immunohistochemical study on a galanin-like peptide in the neuroendocrine system of the alimentary canal of three species of siluriform catfishes. Journal of Fish Biology 68, 86100.CrossRefGoogle Scholar
Bosi, G, Bermùdez, R and Domeneghini, C (2007) The galaninergic enteric nervous system of pleuronectiformes (Pisces, Osteichthyes): an immunohistochemical and confocal laser scanning immunofuorescence study. General and Comparative Endocrinology 152, 2229.CrossRefGoogle Scholar
Bosi, G, Shinn, AP, Giari, L and Sayyaf Dezfuli, B (2015) Enteric neuromodulators and mucus discharge in a fish infected with the intestinal helminth Pomphorhynchus laevis. Parasites & Vectors 8, 359.CrossRefGoogle Scholar
Bosi, G, Giari, L, DePasquale, JA, Carosi, A, Lorenzoni, M and Dezfuli, BS (2017) Protective responses of intestinal mucous cells in a range of fish–helminth systems. Journal of Fish Diseases 40, 10011014.CrossRefGoogle Scholar
Bosi, G, Lorenzoni, M, Carosi, A and Sayyaf Dezfuli, B (2020) Mucosal hallmarks in the alimentary canal of Northern pike Esox lucius (Linnaeus). Animals 10, 1479.CrossRefGoogle ScholarPubMed
Branson, E, Riaza, A and Alvarez-Pellitero, P (1999) Myxosporean infection causing intestinal disease in farmed turbot, Scophthalmus maximus (L.), (Teleostei: Scophthalmidae). Journal of Fish Diseases 22, 395e9.CrossRefGoogle Scholar
Buchmann, K (2012) Fish immune responses against endoparasitic nematodes – experimental models. Journal of Fish Diseases 35, 623635.CrossRefGoogle ScholarPubMed
Buchmann, K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Frontiers in Immunology 5, 459.CrossRefGoogle Scholar
Buchmann, K (2022a) The ontogeny of the fish immune system. In Buchmann, K and Secombes, CH (eds), Principles of Fish Immunology. Berlin: Springer, pp. 495510.CrossRefGoogle Scholar
Buchmann, K (2022b) Antiparasitic immune responses. In Buchmann, K and Secombes, CH (eds), Principles of Fish Immunology. Berlin: Springer, pp. 535563.CrossRefGoogle Scholar
Ceccotti, C, Giaroni, C, Bistoletti, M, Viola, M, Crema, F and Terova, G (2018) Neurochemical characterization of myenteric neurons in the juvenile gilthead sea bream (Sparus aurata) intestine. PLoS ONE 13, e0201760.CrossRefGoogle ScholarPubMed
Chu, S and Schubert, ML (2013) Gastric secretion. Current Opinion in Gastroenterology 29, 636641.CrossRefGoogle ScholarPubMed
Dawson, LHJ, Pike, AW, Houlihan, DF and McVicar, AH (1999) Changes in physiological parameters and feeding behaviour of Atlantic salmon Salmo salar infected with sea lice Lepeophtheirus salmonis. Diseases of Aquatic Organisms 35, 8999.CrossRefGoogle ScholarPubMed
Day, R and Salzet, M (2002) The neuroendocrine phenotype, cellular plasticity, and the search for genetic switches: redefining the diffuse neuroendocrine system. Neuroendocrinology Letters 23, 447451.Google ScholarPubMed
de Matos, LV, de Oliveira, MIB, Gomes, ALS and da Silva, GS (2017) Morphological and histochemical changes associated with massive infection by Neoechinorhynchus buttnerae (Acanthocephala: Neoechinorhynchidae) in the farmed freshwater fish Colossoma macropomum Cuvier, 1818 from the Amazon State, Brazil. Parasitology Research 116, 10291037.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Arrighi, S, Domeneghini, C and Bosi, G (2000) Immunohistochemical detection of neuromodulators in the intestine of Salmo trutta Linnaeus naturally infected with Cyathocephalus truncatus Pallas (Cestoda). Journal of Fish Diseases 23, 265273.CrossRefGoogle Scholar
Dezfuli, BS, Pironi, F, Giari, L, Domeneghini, C and Bosi, G (2002) Effect of Pomphorhynchus laevis (Acanthocephala) on putative neuromodulators in the intestine of naturally infected Salmo trutta. Diseases of Aquatic Organisms 51, 2735.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Giari, L, Arrighi, S, Domeneghini, C and Bosi, G (2003) Influence of enteric helminths on the distribution of intestinal endocrine cells belonging to the diffuse endocrine system in brown trout, Salmo trutta L. Journal of Fish Diseases 26, 155166.CrossRefGoogle Scholar
Dezfuli, BS, Giari, L, Simoni, E, Shinn, AP and Bosi, G (2004) Immunohistochemistry, histopathology and ultrastructure of Gasterosteus aculeatus (L.) tissues infected with Glugea anomala (Moniez 1887). Diseases of Aquatic Organisms 58, 193202.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Pironi, F, Shinn, AP, Manera, M and Giari, L (2007a) Histopathology and ultrastructure of Platichthys flesus naturally infected with Anisakis simplex s.l. larvae (Nematoda: Anisakidae). Journal of Parasitology 93, 14161423.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Pironi, F, Simoni, E, Shinn, AP and Giari, L (2007b) Selected pathological, immunohistochemical and ultrastructural changes associated with an infection by Diphyllobothrium dendriticum (Nitzsch, 1824) (Cestoda) plerocercoids in Coregonus lavaretus (L.) (Coregonidae). Journal of Fish Diseases 30, 471482.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Giovinazzo, G, Lui, A and Giari, L (2008) Inflammatory response to Dentitruncus truttae (Acanthocephala) in the intestine of brown trout. Fish & Shellfish Immunology 24, 726733.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Lui, A, Giovinazzo, G, Boldrini, P and Giari, L (2009) Intestinal inflammatory response of powan Coregonus lavaretus (Pisces) to the presence of acanthocephalan infections. Parasitology 136, 929937.CrossRefGoogle Scholar
Dezfuli, BS, Pironi, F, Campisi, M, Shinn, AP and Giari, L (2010) The response of intestinal mucous cells to the presence of enteric helminths: their distribution, histochemistry and fine structure. Journal of Fish Diseases 33, 481488.CrossRefGoogle Scholar
Dezfuli, BS, Castaldelli, G, Bo, T, Lorenzoni, M and Giari, L (2011a) Intestinal immune response of Silurus glanis and Barbus barbus naturally infected with Pomphorhynchus laevis (Acanthocephala). Parasite Immunology 33, 116123.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Giari, L, Squerzanti, S, Lui, A, Lorenzoni, M, Sakalli, S and Shinn, AP (2011b) Histological damage and inflammatory response elicited by Monobothrium wageneri (Cestoda) in the intestine of Tinca tinca (Cyprinidae). Parasites & Vectors 4, 225.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Lui, A, Giari, L, Castaldelli, G, Shinn, AP and Lorenzoni, M (2012) Innate immune defence mechanisms of tench, Tinca tinca (L.), naturally infected with the tapeworm Monobothrium wageneri. Parasite Immunology 34, 511519.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Bo, T, Lorenzoni, M, Shinn, AP and Giari, L (2015) Fine structure and cellular responses at the host–parasite interface in a range of fish–helminth systems. Veterinary Parasitology 208, 272279.CrossRefGoogle Scholar
Di Giovangiulio, M, Verheijden, S, Bosmans, G, Stakenborg, N, Boeckxstaens, GE and Matteoli, G (2015) The neuromodulation of the intestinal immune system and its relevance in inflammatory bowel disease. Frontiers in Immunology 6, 590.CrossRefGoogle ScholarPubMed
Dumbo, JC and Avenant-Oldewage, A (2019) Histopathological changes induced by the digenean intestinal parasite Masenia nkomatiensis Dumbo, Dos Santos, & Avenant-Oldewage, 2019 of the catfish Clarias gariepinus (Burchell) from Incomati Basin, Mozambique. Journal of Fish Diseases 42, 13411350.CrossRefGoogle Scholar
Esteban, FJ, Jiménez, A, Barroso, JB, Pedrosa, JA, del Moral, ML, Rodrigo, J and Peinado, MA (1998) The innervation of rainbow trout (Oncorhynchus mykiss) liver: protein gene product 9.5 and neuronal nitric oxide synthase immunoreactivities. Journal of Anatomy 193, 241249.CrossRefGoogle ScholarPubMed
Fairweather, I (1997) Peptides: an emerging force in host responses to parasitism. In Beckage, NE (ed.), Parasites and Pathogens: Effects on Host Hormones and Behavior. New York, USA: Chapman & Hall, International Thomson Publishing, pp. 113139.CrossRefGoogle Scholar
Feist, SW and Longshaw, M (2008) Histopathology of fish parasite infections – importance for populations. Journal of Fish Biology 73, 21432160.CrossRefGoogle Scholar
Finney, JL, Robertson, GN, McGee, CAS, Smith, FM and Croll, RP (2006) Structure and autonomic innervation of the swim bladder in the zebrafish (Danio rerio). The Journal of Comparative Neurology 495, 587606.CrossRefGoogle ScholarPubMed
Foster, N and Lee, DL (1996) A vasoactive intestinal polypeptide-like protein excreted/secreted by Nippostrongylus brasiliensis and its effect on contraction of uninfected rat intestine. Parasitology 112, 97104.CrossRefGoogle ScholarPubMed
Franke, F, Rahn, AK, Dittmar, J, Erin, N, Rieger, JK, Haase, D, Samonte-Padilla, IE, Lange, J, Jacobsen, PJ, Hermida, M, Fernández, C, Kurtz, J, Bakker, TCM, Reusch, TBH, Kalbe, M and Scharsack, JP (2014) In vitro leukocyte response of three-spined sticklebacks (Gasterosteus aculeatus) to helminth parasite antigens. Fish & Shellfish Immunology 36, 130140.CrossRefGoogle ScholarPubMed
Fujita, T and Kobayashi, S (1977) Structure and function of gut endocrine cells. International Review of Cytology 6, 187233.Google Scholar
Furness, JB (2000) Types of neurons in the enteric nervous system. Journal of the Autonomic Nervous System 81, 8796.CrossRefGoogle ScholarPubMed
Furness, JB (2006a) Structure of the enteric nervous system. In Furness, (ed.), The Enteric Nervous System. Oxford, UK: Blackwell Publishing, pp. 128.Google Scholar
Furness, JB (2006b) Pharmacology of transmission and sites of drug action in the enteric nervous system. In Furness, (ed.), The Enteric Nervous System. Oxford, UK: Blackwell Publishing, pp. 103131.Google Scholar
Gabanyi, I, Muller, PA, Feighery, L, Oliveira, TY, Costa-Pinto, FA and Mucida, D (2016) Neuro-immune interactions drive tissue programming in intestinal macrophages. Cell 164, 378391.CrossRefGoogle ScholarPubMed
Gay, J, Ressayre, L, Garcia-Villar, R, Bueno, L and Fioramonti, J (2003) Alteration of CCK-induced satiety in post-Nippostrongylus brasiliensis-infected rats. Brain, Behavior, and Immunity 17, 3542.CrossRefGoogle ScholarPubMed
Gräns, A and Olsson, C (2011) Integrated function and control of the gut: gut motility. In Farrell, AP (ed.), Encyclopedia of Fish Physiology. London, UK: Academic Press, pp. 12921300.CrossRefGoogle Scholar
Grove, DJ and Holmgren, S (1992a) Intrinsic mechanisms controlling cardiac stomach volume of the rainbow trout (Oncorhynchus mykiss) following gastric distension. Journal of Experimental Biology 163, 3348.CrossRefGoogle Scholar
Grove, DJ and Holmgren, S (1992b) Mechanisms controlling stomach volume of the Atlantic cod Gadus morhua following gastric distension. Journal of Experimental Biology 163, 4963.CrossRefGoogle Scholar
Guijarro, AI, Delgado, MJ, Pinillos, ML, López-Patiño, MA, Alonso-Bedate, M and De Pedro, N (1999) Galanin and β-endorphin as feeding regulators in cyprinids: effect of temperature. Aquaculture Research 30, 483489.CrossRefGoogle Scholar
Halliez, MCM and Buret, AG (2015) Gastrointestinal parasites and the neural control of gut functions. Frontiers in Cellular Neuroscience 9, 452.CrossRefGoogle ScholarPubMed
Hammerschmidt, K and Kurtz, J (2005) Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences. International Journal for Parasitology 35, 14991507.CrossRefGoogle ScholarPubMed
Hébert, FO, Phelps, L, Samonte, I, Panchal, M, Grambauer, S, Barber, I, Kalbe, M, Landry, CR and Aubin-Horth, N (2015) Identification of candidate mimicryproteins involved in parasite-driven phenotypic changes. Parasites & Vectors 8, 225.CrossRefGoogle ScholarPubMed
Helland-Riise, SH, Vindas, MA, Johansen, IB, Nadler, LE, Weinersmith, KL, Hechinger, RF and Øverli, Ø (2020) Brain-encysting trematodes (Euhaplorchis californiensis) decrease raphe serotonergic activity in California killifish (Fundulus parvipinnis). Biology Open 9, bio049551.CrossRefGoogle ScholarPubMed
Herbison, REH (2017) Lessons in mind control: trends in research on the molecular mechanisms behind parasite–host behavioral manipulation. Frontiers in Ecology and Evolution 5, 102.CrossRefGoogle Scholar
Hernández-Bello, R, Escobedo, G, Guzmán, C, Ibarra-Coronado, EG, López-Griego, L and Morales-Montor, J (2010) Immunoendocrine host–parasite interactions during helminth infections: from the basic knowledge to its possible therapeutic applications. Parasite Immunology 32, 633643.Google ScholarPubMed
Herr, N, Bode, C and Duerschmied, D (2017) The effects of serotonin in immune cells. Frontiers in Cardiovascular Medicine 4, 48.CrossRefGoogle ScholarPubMed
Himick, BA and Peter, RE (1994a) CCK/gastrin-like immunoreactivity in brain and gut, and CCK suppression of feeding in goldfish. American Journal of Physiology 267, R841R851.Google ScholarPubMed
Himick, BA and Peter, RE (1994b) Bombesin acts to suppress feeding behavior and alter serum growth hormone in goldfish. Physiology and Behavior 55, 6572.CrossRefGoogle ScholarPubMed
Hirabayashi, T, Nakamachi, T and Shioda, S (2018) Discovery of PACAP and its receptors in the brain. The Journal of Headache and Pain 19, 28.CrossRefGoogle ScholarPubMed
Hoai, TD (2020) Reproductive strategies of parasitic flatworms (Platyhelminthes, Monogenea): the impact on parasite management in aquaculture. Aquaculture International 28, 421447.CrossRefGoogle Scholar
Holmgren, S (1985) Neuropeptide functions in the fish gut. Peptides 6, 363368.CrossRefGoogle ScholarPubMed
Holmgren, S and Jönsson, A-C (1988) Occurrence and effects on motility of bombesin related peptides in the gastrointestinal tract of the Atlantic cod, Gadus morhua. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology 89, 249256.CrossRefGoogle ScholarPubMed
Holmgren, S and Olsson, C (2009) The neuronal and endocrine regulation of gut function. In Bernier, NJ, Van Der Kraak, G, Farrell, AP and Brauner, CJ (eds), Fish Physiology. Cambridge: Academic Press, vol. 28, pp. 467512.Google Scholar
Jennings, JB (1968) Nutrition and digestion. In Florkin, M and Scheer, BT (eds), Chemical Zoology, Vol. II. Porifera, Coelenterata and Platyhelminthes. New York & London: Academic Press Inc., pp. 303326.Google Scholar
Johansson, MEV and Hansson, GC (2014) Is the intestinal goblet cell a major immune cell? Cell Host & Microbe 15, 251252.CrossRefGoogle ScholarPubMed
Jönsson, E, Kaiya, H and Björnsson, BT (2010) Ghrelin decreases food intake in juvenile rainbow trout (Oncorhynchus mykiss) through the central anorexigenic corticotropin-releasing factor system. General and Comparative Endocrinology 166, 3946.CrossRefGoogle ScholarPubMed
Kaelberer, MM, Buchanan, KL, Klein, ME, Barth, BB, Montoya, MM, Shen, X and Bohórquez, DV (2018) A gut–brain neural circuit for nutrient sensory transduction. Science (New York, N.Y.) 361, eaat5236.CrossRefGoogle ScholarPubMed
Kågström, J and Holmgren, S (1997) VIP-induced relaxation of small arteries of the rainbow trout, Oncorhynchus mykiss, involves prostaglandin synthesis but not nitric oxide. Journal of the Autonomic Nervous System 63, 6876.CrossRefGoogle Scholar
Kai-Larsen, Y, Bergsson, G, Gudmundsson, GH, Printz, G, Jornvall, H, Marchini, G and Agerberth, B (2007) Antimicrobial components of the neonatal gut affected upon colonization. Pediatric Research 61, 530536.CrossRefGoogle ScholarPubMed
Kiliaan, AJ, Scholten, G and Groot, A (1997) Exocytotic release of vasoactive intestinal polypeptide and serotonin from mucosal nerve fibres and endocrine cells of the intestine of the goldfish (Carassius auratus) and the tilapia (Oreochromis mossambicus): an ultrastructural study. Histochemical Journal 29, 4551.CrossRefGoogle Scholar
Kiris, GA, Kumlu, M and Dikel, S (2007) Stimulatory effects of neuropeptide Y on food intake and growth of Oreochromis niloticus. Aquaculture 264, 383389.CrossRefGoogle Scholar
Klein, SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiology and Behavior 79, 441449.CrossRefGoogle ScholarPubMed
Kulkarni, S, Micci, MA, Leser, J, Shin, C, Tang, SC, Fu, YY, Liu, L, Li, Q, Saha, M, Li, C, Enikolopov, G, Becker, L, Rakhilin, N, Anderson, M, Shen, X, Dong, X, Butte, MJ, Song, H, Southard-Smith, EM, Kapur, RP, Bogunovic, M and Pasricha, PJ (2017) Adult enteric nervous system in health is maintained by a dynamic balance between neuronal apoptosis and neurogenesis. Proceedings of the National Academy of Sciences of the USA 114, E3709E3718.CrossRefGoogle ScholarPubMed
Kulkarni, S, Ganz, J, Bayrer, J, Becker, L, Bogunovic, M and Rao, M (2018) Advances in enteric neurobiology: the ‘brain’ in the gut in health and disease. The Journal of Neuroscience 38, 93469354.CrossRefGoogle ScholarPubMed
Larhammar, DAN, Söderberg, C and Lundell, I (1998) Evolution of the neuropeptide Y family and its receptors. Annals of the New York Academy of Sciences 839, 3540.CrossRefGoogle ScholarPubMed
Latorre, R, Sternini, C, De Giorgio, R and Greenwood-Van Meerveld, B (2016) Enteroendocrine cells: a review of their role in brain-gut communication. Neurogastroenterology & Motility 28, 620630.CrossRefGoogle ScholarPubMed
Le Bail, PY and Boeuf, G (1997) What hormones may regulate food intake in fish. Aquatic Living Resources 10, 371379.CrossRefGoogle Scholar
Lefebvre, F, Wielgoss, S, Nagasawa, K and Moravec, F (2012) On the origin of Anguillicoloides crassus, the invasive nematode of Anguillid eels. Aquatic Invasions 7, 443453.CrossRefGoogle Scholar
Levsen, A, Svanevik, CS, Cipriani, P, Mattiucci, S, Gay, M, Hastie, LC, Bušelić, I, Mladineo, I, Karl, H, Ostermeyer, U, Buchmann, K, Højgaard, DP, González, ÁF, Pascual, S and Pierce, GJ (2018) A survey of zoonotic nematodes of commercial key fish species from major European fishing grounds – introducing the FP7 parasite exposure assessment study. Fisheries Research 202, 421.CrossRefGoogle Scholar
Li, C, Zhang, Y, Wang, R, Lu, J, Nandi, S, Mohanty, S, Terhune, J, Liu, Z and Peatman, E (2012) RNA-seq analysis of mucosal immune responses reveals signatures of intestinal barrier disruption and pathogen entry following Edwardsiella ictaluri infection in channel catfish, Ictalurus punctatus. Fish & Shellfish Immunology 32, 816827.CrossRefGoogle ScholarPubMed
Li, S, Han, L, Bai, J, Ma, D, Quan, Y, Fan, J, Jiang, P and Yu, L (2015) Cloning, tissue distribution and effects of fasting on pituitary adenylate cyclase-activating polypeptide in largemouth bass. Chinese Journal of Oceanology and Limnology 33, 328338.CrossRefGoogle Scholar
Lomax, AE, Linden, DR, Mawe, GM and Sharkey, KA (2006) Effects of gastrointestinal inflammation on enteroendocrine cells and enteric neural reflex circuits. Autonomic Neuroscience 126–127, 250257.CrossRefGoogle ScholarPubMed
Losada, AP, Bermúdez, R, Faílde, LD, Di Giancamillo, A, Domeneghini, C and Quiroga, MI (2014) Effects of Enteromyxum scophthalmi experimental infection on the neuroendocrine system of turbot, Scophthalmus maximus (L.). Fish & Shellfish Immunology 40, 577583.CrossRefGoogle ScholarPubMed
Lowe-Jinde, L and Zimmerman, AM (1991) Influence of Cryptobia salmositica on feeding, body composition and growth in rainbow trout. Canadian Journal of Zoology 69, 13971401.CrossRefGoogle Scholar
Lundin, K and Holmgren, S (1984) Vasoactive intestinal polypeptide-like immunoreactivity and effects of VIP in the swimbladder of the cod, Gadus morhua. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 154, 627633.CrossRefGoogle Scholar
Maeda, Y, Palomares-Rius, JE, Hino, A, Afrin, T, Mondal, SI, Nakatake, A, Maruyama, H and Kikuchi, T (2019) Secretome analysis of Strongyloides venezuelensis parasitic stages reveals that soluble and insoluble proteins are involved in its parasitism. Parasites & Vectors 12, 21.CrossRefGoogle ScholarPubMed
Maggi, CA (1997) The effects of tachykinins on inflammatory and immune cells. Regulatory Peptides 70, 7590.CrossRefGoogle ScholarPubMed
Margolis, KG and Gershon, MD (2016) Enteric neuronal regulation of intestinal inflammation. Trends in Neurosciences 39, 614624.CrossRefGoogle ScholarPubMed
Martínez-Álvarez, RM, Volkoff, H, Muñoz-Cueto, JA and Delgado, MJ (2009) Effect of calcitonin gene-related peptide (CGRP), adrenomedullin and adrenomedullin-2/intermedin on food intake in goldfish (Carassius auratus). Peptides 30, 803807.CrossRefGoogle ScholarPubMed
Matsuda, K, Kashimoto, K, Higuchi, T, Yoshida, T, Uchiyama, M, Shioda, S, Arimura, A and Okamura, T (2000) Presence of pituitary adenylate cyclase-activating polypeptide (PACAP) and its relaxant activity in the rectum of a teleost, the stargazer, Uranoscopus japonicus. Peptides 21, 821827.CrossRefGoogle Scholar
Matsuda, K, Maruyama, K, Nakamachi, T, Miura, T, Uchiyama, M and Shioda, S (2005) Inhibitory effects of pituitary adenylate cyclase-activating polypeptide (PACAP) and vasoactive intestinal peptide (VIP) on food intake in the goldfish, Carassius auratus. Peptides 26, 16111616.CrossRefGoogle ScholarPubMed
Mehrdana, F and Buchmann, K (2017) Excretory/secretory products of anisakid nematodes: biological and pathological roles. Acta Veterinaria Scandinavica 59, 112.CrossRefGoogle ScholarPubMed
Merali, Z, McIntosh, J and Anisman, H (1999) Role of bombesin related peptides in the control of food intake. Neuropeptides 33, 376386.CrossRefGoogle ScholarPubMed
Mercer, JG and Chappell, LH (2000) Appetite and parasite. Biologist (Columbus, Ohio) 47, 3540.Google ScholarPubMed
Mercer, JG, Mitchell, PI, Moar, KM, Bissett, A, Geissler, S, Bruce, K and Chappell, LH (2000) Anorexia in rats infected with the nematode, Nippostrongylus brasiliensis: experimental manipulations. Parasitology 120, 641647.CrossRefGoogle ScholarPubMed
Mola, L, Bertacchi, I, Gambarelli, A and Pederzoli, A (2004) Occurrence of ACTH- and enkephalin-like peptides in the developing gut of Dicentrarchus labrax L. General and Comparative Endocrinology 136, 2329.CrossRefGoogle ScholarPubMed
Moon, TW (1998) Glucagon: from hepatic binding to metabolism in teleost fish. Comparative Biochemistry and Physiology, Part B: Biochemistry and Molecular Biology 121, 2734.CrossRefGoogle Scholar
Moravec, F and Justine, J-L (2020) New records of spirurid nematodes (Nematoda, Spirurida, Guyanemidae, Philometridae & Cystidicolidae) from marine fishes of New Caledonia, with redescriptions of two species and erection of Ichthyofilaroides n. gen. Parasite 27, 5.CrossRefGoogle ScholarPubMed
Nakamachi, T, Tanigawa, A, Konno, N, Shioda, S and Matsuda, K (2019) Expression patterns of PACAP and PAC1R genes and anorexigenic action of PACAP1 and PACAP2 in zebrafish. Frontiers in Endocrinology 10, 227.CrossRefGoogle ScholarPubMed
Nam, BH, Moon, JY, Kim, YO, Kong, HJ, Kim, WJ, Kim, DG, Jee, YJ and Lee, SJ (2013) Structural and functional characterization of pituitary adenylyl cyclase-activating polypeptide (PACAP)/PACAP-related peptide (PRP) and its receptor in olive flounder (Paralichthys olivaceus). Comparative Biochemistry and Physiology, Part B: Biochemistry and Molecular Biology 164, 1828.CrossRefGoogle ScholarPubMed
Nardocci, G, Navarro, C, Cortés, PP, Imarai, M, Montoya, M, Valenzuela, B, Jara, P, Acuña-Castillo, C and Fernández, R (2014) Neuroendocrine mechanisms for immune system regulation during stress in fish. Fish & Shellfish Immunology 40, 531538.CrossRefGoogle ScholarPubMed
Navarro, I, Carneiro, MN, Parrizas, M, Maestro, JL, Planas, J and Gutierrez, J (1993) Post-feeding levels of insulin and glucagon in trout (Salmo trutta fario). Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology 104, 389393.CrossRefGoogle Scholar
Nilsson, S (2009) Nervous control of fish swimbladders. Acta Histochemica 111, 176184.CrossRefGoogle ScholarPubMed
O'Dorisio, MS and Panerai, A (1990) Neuropeptides and immunopeptides: messengers in a neuroimmune axis. Annals of the New York Academy of Sciences 594, 1503.Google Scholar
Olsson, C and Holmgren, S (1997) Nitric oxide in the fish gut. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology 118, 959964.CrossRefGoogle ScholarPubMed
Olsson, C and Holmgren, S (2000) PACAP and nitric oxide inhibit contractions in the proximal intestine of the Atlantic cod, Gadus morhua. Journal of Experimental Biology 203, 575583.CrossRefGoogle ScholarPubMed
Olsson, C and Holmgren, S (2001) The control of gut motility. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology 128, 481503.CrossRefGoogle ScholarPubMed
Olsson, C, Aldman, G, Larsson, A and Holmgren, S (1999) Cholecystokinin affects gastric emptying and stomach motility in the rainbow trout Oncorhynchus mykiss. Journal of Experimental Biology 202, 161170.CrossRefGoogle ScholarPubMed
Olsson, C, Holbrook, JD, Bompadre, G, Jönsson, E, Hoyle, CH, Sanger, GJ, Holmgren, S and Andrews, PL (2008a) Identification of genes for the ghrelin and motilin receptors and a novel related gene in fish, and stimulation of intestinal motility in zebrafish (Danio rerio) by ghrelin and motilin. General and Comparative Endocrinology 155, 217226.CrossRefGoogle Scholar
Olsson, C, Holmberg, A and Holmgren, S (2008b) Development of the enteric and vagal innervation of the zebrafish (Danio rerio) gut. The Journal of Comparative Neurology 508, 756770.CrossRefGoogle ScholarPubMed
On, JS and Chow, BK (2016) Molecular evolution of pituitary adenylate cyclase-activating polypeptide subfamily and cognate receptor subfamily. In Reglodi, D and Tamas, A (eds), Current Topics in Neurotoxicity. Pituitary Adenylate Cyclase Activating Polypeptide – PACAP. Berlin, D: Springer Nature, pp. 317.CrossRefGoogle Scholar
Øverli, Ø, Páll, M, Borg, B, Jobling, M and Winberg, S (2001) Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus. Proceedings of the Royal Society B: Biological Sciences 268, 14111415.CrossRefGoogle ScholarPubMed
Palmer, JM and Greenwood-Van Meerveld, B (2001) Integrative neuroimmunomodulation of gastrointestinal function during enteric parasitism. Journal of Parasitology 87, 483504.CrossRefGoogle ScholarPubMed
Peinado, MA, del Moral, ML, Jiménez, A, Rodrigo, J and Esteban, FJ (2002) The nitrergic autonomic innervation of the liver. Autonomic Neuroscience 99, 6769.CrossRefGoogle ScholarPubMed
Pelster, B, Schneebauer, G and Dirks, RP (2016) Anguillicola crassus infection significantly affects the silvering related modifications in steady state mRNA levels in gas gland tissue of the European eel. Frontiers in Physiology 7, 175.CrossRefGoogle ScholarPubMed
Penney, CC and Volkoff, H (2014) Peripheral injections of cholecystokinin, apelin, ghrelin and orexin in cavefish (Astyanax fasciatus mexicanus): effects on feeding and on the brain expression levels of tyrosine hydroxylase, mechanistic target of rapamycin and appetite-related hormones. General and Comparative Endocrinology 196, 3440.CrossRefGoogle ScholarPubMed
Polakof, S, Míguez, JM and Soengas, JL (2011) Evidence for a gut–brain axis used by glucagon-like peptide-1 to elicit hyperglycaemia in fish. Journal of Neuroendocrinology 23, 508518.CrossRefGoogle ScholarPubMed
Poulin, R (1998) Evolutionary Ecology of Parasites: From Individuals to Communities. London, UK: Chapman and Hall.Google Scholar
Poulin, R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. In Brockmann, HJ (ed.), Advances in the Study of Behavior. Burlington, MA: Academic Press, pp. 151186.Google Scholar
Powell, MD, Wright, GM and Burka, JF (1991) Degranulation of eosinophilic granule cells induced by capsaicin and substance P in the intestine of the rainbow trout (Oncorhynchus mykiss Walbaum). Cell & Tissue Research 266, 469474.CrossRefGoogle ScholarPubMed
Power, C, Nowak, BF, Cribb, TH and Bott, NJ (2020) Bloody flukes: a review of aporocotylids as parasites of cultured marine fishes. International Journal for Parasitology 50, 743753.CrossRefGoogle ScholarPubMed
Ranta, E (1995) Schistocephalus infestation improves prey-size selection by three-spined sticklebacks, Gasterosteus aculeatus. Journal of Fish Biology 46, 156158.CrossRefGoogle Scholar
Redondo, MJ, Palenzuela, O and Álvarez-Pellitero, P (2004) Studies on transmission and life cycle of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. Folia Parasitologica 51, 188198.CrossRefGoogle ScholarPubMed
Robledo, D, Ronza, P and Harrison, PW (2014) RNA-seq analysis reveals significant transcriptome changes in turbot (Scophthalmus maximus) suffering severe enteromyxosis. BMC Genomics 15, 1149.CrossRefGoogle ScholarPubMed
Roch, GJ, Wu, S and Sherwood, NM (2009) Hormones and receptors in fish: do duplicate matter? General and Comparative Endocrinology 161, 312.CrossRefGoogle ScholarPubMed
Rønnestad, I, Kamisaka, Y, Conceição, LEC, Morais, S and Tonheim, SK (2007) Digestive physiology of marine fish larvae: hormonal control and processing capacity for proteins, peptides and amino acids. Aquaculture 268, 8297.CrossRefGoogle Scholar
Sayyaf Dezfuli, B and Giari, L (2022) Acanthocephala. In Schierwater, B and DeSalle, R (eds), Invertebrate Zoology: A Tree of Life Approach. New York, USA: CRC Taylor & Francis Group, pp. 369378.Google Scholar
Sayyaf Dezfuli, B, Fernandes, CE, Galindo, GM, Castaldelli, G, Manera, M, DePasquale, JA, Lorenzoni, M, Bertin, S and Giari, L (2016) Nematode infection in liver of the fish Gymnotus inaequilabiatus (Gymnotiformes: Gymnotidae) from the Pantanal Region in Brazil: pathobiology and inflammatory response. Parasites & Vectors 9, 473.CrossRefGoogle ScholarPubMed
Sayyaf Dezfuli, B, DePasquale, JA, Castaldelli, G, Giari, L and Bosi, G (2017) A fish model for the study of the relationship between neuroendocrine and immune cells in the intestinal epithelium: Silurus glanis infected with a tapeworm. Fish & Shellfish Immunology 64, 243250.CrossRefGoogle Scholar
Sayyaf Dezfuli, B, Castaldelli, G and Giari, L (2018a) Histopathological and ultrastructural assessment of two mugilid species infected with myxozoans and helminths. Journal of Fish Diseases 41, 299307.CrossRefGoogle ScholarPubMed
Sayyaf Dezfuli, B, Giari, L, Lorenzoni, M, Carosi, A, Manera, M and Bosi, G (2018b) Pike intestinal reaction to Acanthocephalus lucii (Acanthocephala): immunohistochemical and ultrastructural surveys. Parasites & Vectors 11, 424.CrossRefGoogle ScholarPubMed
Sayyaf Dezfuli, B, Giari, L and Bosi, G (2021a) Survival of metazoan parasites in fish: putting into context the protective immune responses of teleost fish. Advances in Parasitology 112, 77132.CrossRefGoogle ScholarPubMed
Sayyaf Dezfuli, B, Maestri, C, Lorenzoni, M, Carosi, A, Maynard, BJ and Bosi, G (2021b) The impact of Anguillicoloides crassus (Nematoda) on European eel swimbladder: histopathology and relationship between neuroendocrine and immune cells. Parasitology 148, 612622.CrossRefGoogle Scholar
Sayyaf Dezfuli, B, Simoni, E, Bosi, G, Palomba, M, Mattiucci, S, Giulietti, L, Bao, M, Levsen, A and Cipriani, P (2021c) Immunohistopathological response against anisakid nematode larvae and a coccidian in Micromesistius poutassou from NE Atlantic waters. Journal of Helminthology 95, e14.CrossRefGoogle Scholar
Sayyaf Dezfuli, B, Pironi, F, Maynard, BJ, Simoni, E and Bosi, G (2022) Rodlet cells, fish immune cells and a sentinel of parasitic harm in teleost organs. Fish & Shellfish Immunology 121, 516534.CrossRefGoogle Scholar
Scharsack, JP, Kalbe, M, Derner, R, Kurtz, J and Milinski, M (2004) Modulation of granulocyte responses in three spined sticklebacks (Gasterosteus aculeatus L.) infected with the tapeworm (Schistocephalus solidus, Muller 1776). Diseases of Aquatic Organisms 59, 141150.CrossRefGoogle ScholarPubMed
Scharsack, JP, Koch, K and Hammerschmidt, K (2007) Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proceedings of the Royal Society B: Biological Sciences 274, 31513158.CrossRefGoogle ScholarPubMed
Scharsack, JP, Gossens, A, Franke, F and Kurtz, J (2013) Excretory products of the cestode, Schistocephalus solidus, modulate in vitro responses of leukocytes from its specific host, the three-spined stickleback (Gasterosteus aculeatus). Fish & Shellfish Immunology 35, 17791787.CrossRefGoogle ScholarPubMed
Schroeter, JC, Fenn, CM and Small, BC (2015) Elucidating the roles of gut neuropeptides on channel catfish feed intake, glycemia, and hypothalamic NPY and POMC expression. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology 188, 168174.CrossRefGoogle ScholarPubMed
Sekar, R, Wang, L and Chow, BKC (2017) Central control of feeding behavior by the secretin, PACAP, and glucagon family of peptides. Frontiers in Endocrinology 8, 18.CrossRefGoogle ScholarPubMed
Serna-Duque, JA and Esteban, MA (2020) Effects of inflammation and/or infection on the neuroendocrine control of fish intestinal motility: a review. Fish & Shellfish Immunology 103, 342356.CrossRefGoogle ScholarPubMed
Shahbazi, F, Karila, P, Olsson, C, Holmgren, S, Conlon, JM and Jensen, J (1998) Primary structure, distribution, and effects on motility of CGRP in the intestine of the cod Gadus morhua. American Journal of Physiology 275, R19R28.Google ScholarPubMed
Shaw, JC and Øverli, Ø (2012) Brain-encysting trematodes and altered monoamine activity in naturally infected killifish Fundulus parvipinnis. Journal of Fish Biology 81, 22132222.CrossRefGoogle ScholarPubMed
Shinn, AJ, Pratoomyot, J, Bron, J, Paladini, G, Brooker, E and Brooker, A (2015) Economic impacts of aquatic parasites on global finfish production. Global Aquaculture Advocate. September/October 2015, Global Aquaculture Alliance, pp. 8284.Google Scholar
Silva-Gomes, AL, Gomes Coelho-Filho, J, Viana-Silva, W, Braga-Oliveira, MI, Bernardino, G and Costa, JI (2017) The impact of Neoechinorhynchus buttnerae (Golvan, 1956) (Eoacanthocephala: Neochinorhynchidae) outbreaks on productive and economic performance of the tambaqui Colossoma macropomum (Cuvier, 1818), reared in ponds. Latin American Journal of Aquatic Research 45, 496500.CrossRefGoogle Scholar
Smales, LR (2015) Acanthocephala. In Schmidt-Rhaesa, A (ed.), Handbook of Zoology. Cycloneuralia Gastrotricha and Gnathifera. Berlin, D: De Gruyter, pp. 317336.Google Scholar
Smyth, JD (1969) The Physiology of Cestodes. Edinburgh, UK: Oliver & Boyd.Google Scholar
Stakenborg, N, Viola, MF and Boeckxstaens, GE (2020) Intestinal neuro-immune interactions: focus on macrophages, mast cells and innate lymphoid cells. Current Opinion in Neurobiology 62, 6875.CrossRefGoogle ScholarPubMed
Stefano, GB, Scharrer, B, Smith, EM, Hughes, TK Jr, Magazine, HI, Bilfinger, TV, Hartman, AR, Fricchione, GL, Liu, Y and Makman, MH (2017) Opioid and opiate immunoregulatory processes. Critical Reviews in Immunology 37, 213248.CrossRefGoogle ScholarPubMed
Sternini, C, Anselmi, L and Rozengurt, E (2008) Enteroendocrine cells: a site of ‘taste’ in gastrointestinal chemosensing. Current Opinion in Endocrinology 15, 7378.Google ScholarPubMed
Stoyanova, II and Gulubova, MV (2002) Mast cells and inflammatory mediators in chronic ulcerative colitis. Acta Histochemica 104, 185192.CrossRefGoogle ScholarPubMed
Sundstrom, G, Larsson, TA, Brenner, S, Venkatesh, B and Larhammar, D (2008) Evolution of the neuropeptide Y family: new genes by chromosome duplications in early vertebrates and in teleost fishes. General and Comparative Endocrinology 155, 705716.CrossRefGoogle ScholarPubMed
Szabó, A, Nemcsók, J, Kása, P and Budai, D (1991) Comparative study of acetylcholine synthesis in organs of freshwater teleosts. Fish Physiology and Biochemistry 9, 9399.CrossRefGoogle ScholarPubMed
Takei, Y and Loretz, CA (2011) The gastrointestinal tract as an endocrine/neuroendocrine/paracrine organ: organization, chemical messenger and physiological targets. In Grosell, M, Farrel, AP and Brauner, CJ (eds), The Multifunctional Gut of Fish. Amsterdam, NL: Elsevier, pp. 261317.Google Scholar
Taraschewski, H (2000) Host–parasite interactions in Acanthocephala: a morphological approach. Advances in Parasitology 46, 1179.CrossRefGoogle ScholarPubMed
Tavares-Dias, M and Martins, ML (2017) An overall estimation of losses caused by diseases in the Brazilian fish farms. Journal of Parasitic Diseases 41, 913918.CrossRefGoogle ScholarPubMed
Thomas, F, Adamo, S and Moore, J (2005) Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185199.CrossRefGoogle ScholarPubMed
Unniappan, S, Canosa, LF and Peter, RE (2004) Orexigenic actions of ghrelin in goldfish: feeding-induced changes in brain and gut mRNA expression and serum levels, and responses to central and peripheral injections. Neuroendocrinology 79, 100108.CrossRefGoogle ScholarPubMed
Volkoff, H (2006) The role of neuropeptide Y, orexins, cocaine and amphetamine related transcript, cholecystokinin, amylin and leptin in the regulation of feeding in fish. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology 144, 325331.CrossRefGoogle ScholarPubMed
Volkoff, H (2016) The neuroendocrine regulation of food intake in fish: a review of current knowledge. Frontiers in Neuroscience 10, 540.CrossRefGoogle Scholar
Volkoff, H and Peter, RE (2001) Interactions between orexin A, NPY and galanin in the control of food intake of the goldfish, Carassius auratus. Regulatory Peptides 101, 5972.CrossRefGoogle ScholarPubMed
Volkoff, H, Eykelbosh, AJ and Peter, RE (2003) Role of leptin in the control of feeding of goldfish Carassius auratus: interactions with cholecystokinin, neuropeptide Y and orexin A, and modulation by fasting. Brain Research 972, 90109.CrossRefGoogle ScholarPubMed
Volkoff, H, Canosa, LF, Unniappan, S, Cerda-Reverter, JM, Bernier, NJ, Kelly, SP and Peter, RE (2005) Neuropeptides and the control of food intake in fish. General and Comparative Endocrinology 142, 319.CrossRefGoogle ScholarPubMed
Volkoff, H, Unniappan, S and Kelly, SP (2009) The endocrine regulation of food intake. In Bernier, NJ, Van der Kraak, G, Farrel, AP and Brauner, CJ (eds), Fish Physiology. Cambridge: Academic Press, vol. 28, pp. 421465. doi: 10.1016/S1546-5098(09)28009-5Google Scholar
Wang, SJ, Sharkey, KA and McKay, D (2018) Modulation of the immune response by helminths: a role for serotonin? Bioscience Reports 38, BSR20180027.CrossRefGoogle ScholarPubMed
Weinersmith, KL, Hanninen, AF, Sih, A, Mcelreath, R and Earley, RL (2016) The relationship between handling time and cortisol release rates changes as a function of brain parasite densities in California killifish Fundulus parvipinnis. Journal of Fish Biology 88, 11251142.CrossRefGoogle ScholarPubMed
Whitmore, TE, Holloway, JL, Lofton-Day, CE, Maurer, MF, Chen, L, Quinton, TJ, Vincent, JB, Scherer, SW and Lok, S (2000) Human secretin (SCT): gene structure, chromosome location, and distribution of mRNA. Cytogenetics and Cell Genetics 90, 4752.CrossRefGoogle ScholarPubMed
Würtz, J and Taraschewski, H (2000) Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Diseases of Aquatic Organisms 39, 121134.CrossRefGoogle ScholarPubMed
Yan, P, Jia, J, Yang, G, Wang, D, Sun, C and Li, W (2017) Duplication of neuropeptide Y and peptide YY in Nile tilapia Oreochromis niloticus and their roles in food intake regulation. Peptides 88, 97105.CrossRefGoogle ScholarPubMed
Ye, L and Rawls, JF (2021) Microbial influences on gut development and gut–brain communication. Development (Cambridge, England) 148, dev194936.CrossRefGoogle ScholarPubMed
Ye, L, Bae, M, Cassilly, CD, Jabba, SV, Thorpe, DW, Martin, AM, Lu, H-L, Wang, J, Thompson, JD, Lickwar, CR, Poss, KD, Keating, DJ, Jordt, S-E, Clardy, J, Liddle, RA and Rawls, JF (2021) Enteroendocrine cells sense bacterial tryptophan catabolites to activate enteric and vagal neuronal pathways. Cell Host & Microbe 29, 179196.CrossRefGoogle ScholarPubMed
Yokobori, E, Azuma, M, Nishiguchi, R, Kang, KS, Kamijo, M, Uchiyama, M and Matsuda, K (2012) Neuropeptide Y stimulates food intake in the zebrafish, Danio rerio. Journal of Neuroendocrinology 24, 766773.CrossRefGoogle ScholarPubMed
Zhang, X, Tang, N, Qi, J, Wang, S, Hao, J, Wu, Y, Chen, H, Tian, Z, Wang, B, Chen, D and Li, Z (2017) CCK reduces the food intake mainly through CCK1R in Siberian sturgeon (Acipenser baerii Brandt). Scientific Reports 7, 12413.CrossRefGoogle ScholarPubMed
Zhou, Y, Liang, XF, Yuan, X, Li, J, He, Y, Fang, L, Guo, X, Liu, L, Li, B and Shen, D (2013) Neuropeptide Y stimulates food intake and regulates metabolism in grass carp, Ctenopharyngodon idellus. Aquaculture 380, 5261.CrossRefGoogle Scholar
Zoghbi, S, Trompette, A, Claustre, J, Homsi, ME, Garzón, J, Jourdan, G, Scoazec, J-Y and Plaisancié, P (2006) β-Casomorphin-7 regulates the secretion and expression of gastrointestinal mucins through a μ-opioid pathway. American Journal of Physiology: Gastrointestinal and Liver Physiology 290, G1105G1113.Google ScholarPubMed