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α-Transducin and α-gustducin immunoreactive cells in the stomach of common sole (Solea solea) fed with mussel meal

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Abstract

Vertebrates perceive a variety of exogenous substances using two main chemosensory systems, taste and olfaction. The taste perception occurs through the interaction of taste receptors associated with specific G protein subunits such as α-transducin (Gαtran) and α-gustducin (Gαgust). Aquatic vertebrates are also provided with a chemosensory system consisting of solitary chemosensory cells distributed to the oropharynx and skin. In this study, we identified Gαtran and Gαgust-immunoreactive cells intermingled with non-labeled epithelial cells in the gastric mucosa of the common sole. A long-term diet with increasing concentrations of mussel meal in the protein component of a conventional fish meal-based diet induced a dose-dependent increase in the gastric epithelial area and density of Gαtran and Gαgust immunoreactive cells. These findings suggest that taste-related molecules are regulated by changes in diet formulation in common sole aquaculture.

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References

  • Anagnostidis A, Michailidou M, Vatsos JN, Tsopelakos A, Miliou H, Angelidis P (2013) Use of frozen mussel (Mytilus galloprovincialis) and mussel meal in the diet of sea bass (Dicentrarchus labrax Linnaeus, 1758) and sea bream (Sparus aurata Linnaeus, 1758) fingerlings a preliminary study. Aquacult Res 2013:1–5. doi:10.1111/are.12174

    Google Scholar 

  • Appelbaum S, Schemmel C (1983) Dermal sense organs and their significance in the feeding behaviour of the common sole Solea vulgaris. Mar Ecol Prog Ser 13:29–36

    Article  Google Scholar 

  • Behrens M, Meyerhof W (2011) Gustatory and extragustatory functions of mammalian taste receptors. Physiol Behav 105:4–13. doi:10.1016/j.physbeh.2011.02.010

    Article  CAS  PubMed  Google Scholar 

  • Berge GM, Austreng E (1989) Blue mussel in feed for rainbow trout. Aquaculture 81:79–90

    Article  Google Scholar 

  • Bonaldo A, Parma L, Badiani A, Serratore P, Gatta PP (2011) Very early weaning of common sole (Solea solea L.) larvae by means of different feeding regimes and three commercial microdiets: influence on performances, metamorphosis development and tank hygiene. Aquaculture 321(3):237–244. doi:10.1016/j.aquaculture.2011.09.007

    Article  Google Scholar 

  • Braun CB (1998) Schreiner organs: a new craniate chemosensory modality in hagfishes. J Comp Neurol 392(2):135–163. doi:10.1002/(sici)1096-9861(19980309)392:2<135:aid-cne1>3.0.co;2-3

    Article  CAS  PubMed  Google Scholar 

  • Cabral HN (2000) Comparative feeding ecology of sympatric Solea solea and S. senegalensis, within the nursery areas of the Tagus estuary Portugal. J Fish Biol 57:1550–1562. doi:10.1006/jfbi.2000.1408

    Article  Google Scholar 

  • Caicedo A, Pereira E, Margolskee RF, Roper SD (2003) Role of the G-protein subunit alpha-gustducin in taste cell responses to bitter stimuli. J Neurosci 23(30):9947–9952

    CAS  PubMed  Google Scholar 

  • Cheled-Shoval SL, Behrens M, Meyerhof W, Niv MY, Uni Z (2014) Perinatal administration of a bitter tastant influences gene expression in chicken palate and duodenum. J Agric Food Chem 62(52):12512–12520. doi:10.1021/jf502219a

    Article  CAS  PubMed  Google Scholar 

  • Daly K, Al-Rammahi M, Arora DK, Moran AW, Proudman CJ, Ninomiya Y, Shirazi-Beechey SP (2012) Expression of sweet receptor components in equine small intestine: relevance to intestinal glucose transport. Am J Physiol Regul Integr Comp Physiol 303(2):R199–R208. doi:10.1152/ajpregu.00031.2012

    Article  CAS  PubMed  Google Scholar 

  • Day OJ, Howell BR, Jones DA (1997) The effect of dietary hydrolysed fish protein concentrate on the survival and growth of juvenile Dover sole, Solea solea (L.), during and after weaning. Aquacul Res 28:911–921. doi:10.1046/j.1365-2109.1997.00922.x

    Article  Google Scholar 

  • Depoortere I (2014) Taste receptors of the gut: emerging roles in health and disease. Gut 63(1):179–190. doi:10.1136/gutjnl-2013-305112

    Article  CAS  PubMed  Google Scholar 

  • Dinis MT, Ribeiro L, Soares F, Sarasquete C (1999) A review on the cultivation potential of Solea senegalensis in Spain and in Portugal. Aquaculture 176:27–38. doi:10.1016/S0044-8486(99)00047-2

    Article  Google Scholar 

  • Finger TE (1997) Evolution of taste and solitary chemoreceptor cell systems. Brain Behav Evol 50(4):23443. doi:10.1159/000113337

    Article  Google Scholar 

  • Finger TE, Böttger B, Hansen A, Anderson KT, Alimohammadi H, Silver WL (2003) Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc Natl Acad Sci USA 100(15):8981–8986. doi:10.1073/pnas.1531172100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fonds M, Drinkwaard B, Resink JW, Eysink GGJ, Toet W (1989) Measurements of metabolism, food intake and growth of Solea solea (L.) fed with mussel meat or with dry food. In: De Pauw N, Jaspers E, Ackefors H, Wilkins N (eds) Aquaculture: a biotechnology in progress, vol 2. European Aquaculture Society, Bredene, pp 851–874

    Google Scholar 

  • Hansen A, Finger TE (2009) Solitary chemosensory cells: phylogenyand ontogeny. In: Zaccone G, Cutz E, Adriaensen D, Nurse CA, Mauceri A (eds) Airway chemoreceptors in the vertebrates-structure, evolution and function. Science Publishers, Enfield (NH), pp 377–387

    Chapter  Google Scholar 

  • Hansen A, Reutter K (2004) Chemosensory systems in fish: structural, functional and ecological aspects. In: von derEmde G, Mogdans J, Kapoor BG (eds) The senses of fish: adaptations for the reception of natural stimuli. Narosa Publishing House/Kluwer Academic Publishers, New Delhi/Dordrecht, pp 55–89

    Chapter  Google Scholar 

  • Harvey R, Blaxter JHS, Hoyt RD (1992) Development of superficial and lateral line neuromasts in larvae and juveniles of plaice (Pluronectes platessa) and sole (Solea solea). J Mar Biol Assoc UK 72:651–668. doi:10.1017/S0025315400059427

    Article  Google Scholar 

  • Hashiguchi Y, Furuta Y, Kawahara R, Nishida M (2007) Diversification and adaptive evolution of putative sweet taste receptors in threespine stickleback. Gene 396(1):170–179. doi:10.1016/j.gene.2007.03.015

    Article  CAS  PubMed  Google Scholar 

  • Howell BR (1997) A re-appraisal of the potential of the sole, Solea solea (L.), for commercial cultivation. Aquaculture 155:355–365

    Article  Google Scholar 

  • Imsland AK, Foss A, Conceição LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P (2003) A review of the culture potential of Solea solea and S. senegalensis. Rev Fish Biol Fish 13:379–408. doi:10.1007/s11160-013-9317-7

    Article  Google Scholar 

  • Ishimaru Y, Okada S, Naito H, Nagai T, Yasuoka A, Matsumoto I, Abe K (2005) Two families of candidate taste receptors in fishes. Mech Dev 122:1310–1321. doi:10.1016/j.mod.2005.07.005

    Article  CAS  PubMed  Google Scholar 

  • Janssen S, Laermans J, Iwakura H, Tack J, Depoortere I (2012) Sensing of fatty acids for octanoylation of ghrelin involves a gustatory G-protein. PLoS One 7(6):e40168. doi:10.1371/journal.pone.0040168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Janssen S, Laermans J, Verhulst PJ, Thijs T, Tack J, Depoortere I (2011) Bitter taste receptors and a-gustducin regulate the secretion of ghrelin with functional effects on food intake and gastric emptying. Proc Natl Acad Sci USA 108:2094–2099. doi:10.1073/pnas.1011508108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kikuchi K (1999) Use of defatted soybean meal as a substitute for fish meal in diets of Japanese flounder (Paralichthys olivaceus). Aquaculture 179:3–11. doi:10.1016/S0044-8486(99)00147-7

    Article  Google Scholar 

  • Kikuchi K, Furuta T (2009a) Inclusion of blue mussel extract in diets based on fish and soybean meals for tiger puffer Takifugu rubripes. Fish Sci 75:183–189. doi:10.1007/s12562-008-0012-x

    Article  CAS  Google Scholar 

  • Kikuchi K, Furuta T (2009b) Use of defatted soybean meal and blue mussel meat as substitute for fish meal in the diet of tiger puffer, Takifugu rubripes. J World Aquac Soc 40:472–482. doi:10.1111/j.1749-7345.2009.00265.x

    Article  Google Scholar 

  • Kikuchi K, Ueda A, Sugita H, Takeda S (2002) Effect of dietary inclusion of blue mussel extract on growth and body composition of Japanese flounder Paralichthys olivaceus. J World Aquac Soc 33:4–47

    Article  Google Scholar 

  • Kirino M, Parnes J, Hansen A, Kiyohara S, Finger TE (2013) Evolutionary origins of taste buds: phylogenetic analysis of purinergic neurotransmission in epithelial chemosensors. Open Biol 3(3):130015. doi:10.1098/rsob.130015

    Article  PubMed Central  PubMed  Google Scholar 

  • Kuciel M, Lauriano ER, Silvestri G, Zuwała K, Pergolizzi S, Zaccone D (2013) The structural organization and immunohistochemistry of G-protein alpha subunits in the olfactory system of the air-breathing mudskipper, Periophthalmus barbarus (Linnaeus, 1766) (Gobiidae, Oxudercinae). Acta Histochem 116(1):70–78. doi:10.1016/j.acthis.2013.05.005

    Article  PubMed  Google Scholar 

  • Laberge F, Hara TJ (2001) Neurobiology of fish olfaction: a review. Brain Res Brain Res Rev 36(1):46–59. doi:10.1016/S0165-0173(01)00064-9

    Article  CAS  PubMed  Google Scholar 

  • Lagardère JP, Favre L, Mosneron Duplin J, Sureau D (1992) Orientation by olfactory perception in the common sole (Solea solea) evaluated using ultrasonic telemetry. In: Priede IG, Swift SM (eds) Wildlife telemetry remote monitoring and tracking of animals. Ellis Horwood, Chichester, pp 367–375

    Google Scholar 

  • Latorre R, Mazzoni M, De Giorgio R, Vallorani C, Bonaldo A, Gatta PP, Corinaldesi R, Ruggeri E, Bernardini C, Chiocchetti R, Sternini C, Clavenzani P (2013) Enteroendocrine profile of α-transducin immunoreactive cells in the gastrointestinal tract of the European sea bass (Dicentrarchus labrax). Fish Physiol Biochem 39(6):1555–1565. doi:10.1007/s10695-013-9808-4

    Article  CAS  PubMed  Google Scholar 

  • Mackie AM, Adron JW, Grant PT (1980) Chemical nature of feeding stimulants for the juvenile Dover sole, Solea solea (L.). J Fish Biol 16:701–708

    Article  CAS  Google Scholar 

  • Margolskee RF (2002) Molecular mechanisms of bitter and sweet taste transduction. J Biol Chem 277:1–4. doi:10.1074/jbc.R100054200

    Article  CAS  PubMed  Google Scholar 

  • Mas-Muñoz J, Komen H, Schneider O, Visch SW, Schrama JW (2011) Feeding behaviour, swimming activity and boldness explain variation in feed intake and growth of sole (Solea solea) reared in captivity. PLoS One 6(6):e21393. doi:10.1371/journal.pone.0021393

    Article  PubMed Central  PubMed  Google Scholar 

  • Mazzoni M, De Giorgio R, Latorre R, Vallorani C, Bosi P, Trevisi P, Barbara G, Stanghellini V, Corinaldesi R, Forni M, Faussone Pellegrini MS, Sternini C, Clavenzani P (2013) Expression and regulation of α-transducin in the pig gastrointestinal tract. J Cell Mol Med 17:466–474. doi:10.1111/jcmm.12026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ming D, Ninomiya Y, Margolskee RF (1999) Blocking taste receptor activation of gustducin inhibits gustatory responses to bitter compounds. Proc Natl Acad Sci USA 96:9903–9908. doi:10.1073/pnas.96.17.9903

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nagel F, von Danwitz A, Schlachter M, Kroeckel S, Wagner C, Schulz C (2013) Blue mussel meal as feed attractant in rapeseed protein-based diets for turbot (Psetta maxima L.). Aquac Res 45:1964–1978. doi:10.1111/are.12140

    Article  Google Scholar 

  • Newell RIE (1989) Special profiles: life histories and environmental requirement of coastal fishes and invertebrates (Mid and North Atlantic) blue mussel. U.S. Fish and Wildlife Service Biological Report 82(11.102), pp 1–25

  • Oike H, Nagai T, Furuyama A, Okada S, Aihara Y, Ishimaru Y, Marui T, Matsumoto I, Misaka T, Abe K (2007) Characterization of ligands for fish taste receptors. J Neurosci 27:5584–5592. doi:10.1523/jneurosci.0651-07.2007

    Article  CAS  PubMed  Google Scholar 

  • Parisi G, Terova G, Gasco L, Piccolo G, Roncarati A, Moretti VM, Centoducati G, Gatta PP, Pais A (2014) Current status and future perspectives of Italian finfish aquaculture. Rev Fish Biol Fish 24:1573. doi:10.1007/s11160-013-9317-7

    Article  Google Scholar 

  • Parma L, Bonaldo A (2013) Larval fish weaning. In: Qin JG (ed) Larval fish aquaculture. Nova Science Publishers, New York, pp 201–222

    Google Scholar 

  • Polakof S, Soengas JL (2013) Evidence of sugar sensitive genes in the gut of a carnivorous fish species. Comp Biochem Physiol B Biochem Mol Biol 166(1):58–64. doi:10.1016/j.cbpb.2013.07.003

    Article  CAS  PubMed  Google Scholar 

  • Reig L, Ginovart M, Flos R (2003) Modification of the feeding behavior of sole (Solea solea) through the additions of a commercial flavor as an alternative to betaine. Aquat Living Resour 16:370–379. doi:10.1016/S0990-7440(03)00062-7

    Article  Google Scholar 

  • Rozengurt E, Sternini C (2007) Taste receptor signaling in the mammalian gut. Curr Opin Pharmacol 7(6):557–562. doi:10.1016/j.coph.2007.10.002

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rozengurt N, Wu SV, Chen MC, Huang C, Sternini C, Rozengurt E (2006) Colocalization of the alpha-subunit of gustducin with PYY and GLP-1 in L cells of human colon. Am J Physiol Gastrointest Liver Physiol 291:G792–G802. doi:10.1152/ajpgi.00074.2006

    Article  CAS  PubMed  Google Scholar 

  • Sbarbati A, Osculati F (2005) The taste cell-related diffuse chemosensory system. Prog Neurobiol 5(4):295–307. doi:10.1016/j.pneurobio.2005.03.001

    Article  Google Scholar 

  • Sutherland K, Young RL, Cooper NJ, Horowitz M, Blackshaw LA (2007) Phenotypic characterization of taste cells of the mouse small intestine. Am J Physiol Gastrointest Liver Physiol 292:G1420–G1428. doi:10.1152/ajpgi.00504.2006

    Article  CAS  PubMed  Google Scholar 

  • Swartz TD, Duca FA, de Wouters T, Sakar Y, Covasa M (2012) Up-regulation of intestinal type 1 taste receptor 3 and sodium glucose luminal transporter-1 expression and increased sucrose intake in mice lacking gut microbiota. Br J Nutr 107(5):621–630. doi:10.1017/S0007114511003412

    Article  CAS  PubMed  Google Scholar 

  • Teixeira CM, Cabral HN (2010) Comparative analysis of the diet, growth and reproduction of the soles, Solea solea and Solea senegalensis, occurring in sympatry along the Portuguese coast. J Mar Biol Assoc UK 90:995–1003. doi:10.1017/S0025315410000238

    Article  Google Scholar 

  • Vegezzi G, Anselmi L, Huynh J, Barocelli E, Rozengurt E, Raybould H, Sternini C (2014) Diet-reduced regulation of bitter taste receptor subtypes in the mouse gastrointestinal tract. PLoS One 9(9):e107732. doi:10.1371/journal.pone.0107732

    Article  PubMed Central  PubMed  Google Scholar 

  • Whitear M (1992) Solitary chemoreceptor cells. In: Hara TJ (ed) Chemoreception in fishes. Chapman and Hall, London, pp 103–125

    Chapter  Google Scholar 

  • Widmayer P, Küper M, Kramer M, Königsrainer A, Breer H (2012) Altered expression of gustatory-signaling elements in gastric tissue of morbidly obese patients. Int J Obes (Lond) 36(10):1353–1359. doi:10.1038/ijo.2011.216

    Article  CAS  Google Scholar 

  • Yasuoka A, Abe K (2009) Gustation in fish: search for prototype of taste perception. Results Probl Cell Differ 47:239–255. doi:10.1007/400_2008_6

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Deng S, Zhang H, Li H, Li L (2006) Distribution of different taste buds and expression of alpha gustducin in the barbles of yellow catfish (Pelteobagrus fulvidraco). Fish Physiol Biochem 32:55–62. doi:10.1007/s10695-006-6937-z

    Article  CAS  PubMed  Google Scholar 

  • Zhang XJ, Zhou LH, Ban X, Liu DX, Jiang W, Liu XM (2011) Decreased expression of CD36 in circumvallate taste buds of high-fat diet induced obese rats. Acta Histochem 113(6):663–667. doi:10.1016/j.acthis.2010.09.007

    Article  CAS  PubMed  Google Scholar 

  • Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS (2003) The receptors for mammalian sweet and umami taste. Cell 115:255–266. doi:10.1016/S0092-8674(03)00844-4

    Article  CAS  PubMed  Google Scholar 

  • Zielinski BS, Hara TJ (2006) Olfaction. In: Hara TJ, Zielinski BS (eds) Sensory systems neuroscience. Elsevier, New York, pp 1–43

    Chapter  Google Scholar 

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Acknowledgments

This study was financed by the Department of Veterinary Medical Science, University of Bologna. The authors thank Drs. Roberto De Giorgio (University of Bologna, Italy) and Catia Sternini (University of California at Los Angeles) for their comments on the manuscript.

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Mazzoni, M., Bonaldo, A., Gatta, P.P. et al. α-Transducin and α-gustducin immunoreactive cells in the stomach of common sole (Solea solea) fed with mussel meal. Fish Physiol Biochem 41, 603–612 (2015). https://doi.org/10.1007/s10695-015-0031-3

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