Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-06-12T10:23:49.440Z Has data issue: false hasContentIssue false
  • English
  • Français

Digestive flexibility in a euryhaline crab from a SW Atlantic coastal lagoon: alkaline phosphatase activity sensitive to salinity in the hepatopancreas

Published online by Cambridge University Press:  11 May 2015

Silvina Andrea Pinoni ,
Eugenia Méndez  and
Alejandra Antonia López Mañanes
Silvina Andrea Pinoni
Affiliation:
Instituto de Investigaciones Marinas y Costeras (IIMyC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)-Universidad Nacional de Mar del Plata, Funes 3250 (7600) Mar del Plata, Argentina
Eugenia Méndez
Affiliation:
Instituto de Investigaciones Marinas y Costeras (IIMyC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)-Universidad Nacional de Mar del Plata, Funes 3250 (7600) Mar del Plata, Argentina
Alejandra Antonia López Mañanes*
Affiliation:
Instituto de Investigaciones Marinas y Costeras (IIMyC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)-Universidad Nacional de Mar del Plata, Funes 3250 (7600) Mar del Plata, Argentina
*
Correspondence should be addressed to: A.A. López Mañanes, Instituto de Investigaciones Marinas y Costeras (IIMyC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)-Universidad Nacional de Mar del Plata, Funes 3250 (7600) Mar del Plata, Argentina email: mananes@mdp.edu.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

We studied biochemical characteristics and the response to low salinity at short and long-term after feeding of alkaline phosphatase (AP) activity in hepatopancreas of the osmoregulator crab Neohelice granulata from Mar Chiquita coastal lagoon (Buenos Aires Province, Argentina) (37°32′–37°45′S 57°19′–57°26′W). The hepatopancreas exhibited a levamisole-insensitive and a levamisole-sensitive AP activity with distinct characteristics. Levamisole-insensitive activity was similar within the range of pH 7.4–9.0 and exhibited a Michaelis–Menten kinetics. Levamisole-sensitive AP activity appeared to be maximal at pH 8.5 and appeared to exhibit an allosteric kinetics. In crabs acclimated to 10 psu (hyper-regulation conditions) levamisole-insensitive and levamisole-sensitive AP activity increased (about 16-fold) over time from short term (2–4 h) to long term (120 h) after feeding while no changes occurred in crabs acclimated to 35 psu (osmoconforming conditions). The changes of AP activity along with the higher values at 120 h after feeding in 10 psu compared with those in 35 psu, and the concomitant changes in proteolytic activity, suggest a role of AP in digestive and metabolic adjustments at the biochemical level upon hyper-regulatory conditions.

Keywords

digestive flexibilityalkaline phosphatasehepatopancreascrabs
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 6 , September 2015 , pp. 1133 - 1140
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ali, A.T., Ferris, W.F., Penny, C.B., Van der Merwe, M.-T., Jacobson, B.F., Paiker, J.E. and Crowther, N.J. (2013) Lipid accumulation and alkaline phosphatase activity in human preadipocytes isolated from different body fat depots. Journal of Endocrinology, Metabolism and Diabetes South Africa 18, 58–64.CrossRefGoogle Scholar
Asaro, A., del Valle, J.C. and López Mañanes, A.A. (2009) Sucrase and maltase activities in hepatopancreas of Neohelice granulata: post-ingesta response. Biocell 33, A197.Google Scholar
Asaro, A., del Valle, J.C. and López Mañanes, A. (2011) Amylase, maltase and sucrase activities in hepatopancreas of the euryhaline crab Neohelice granulata (Decapoda: Brachyura: Varunidae): partial characterization and response to low environmental salinity. Scientia Marina 75, 517–524.Google Scholar
Barker, P.L. and Gibson, R. (1977) Observations on the feeding mechanism, structure of the gut, and digestive physiology of the European lobster Homarus gammarus (L.) (Decapoda: Nephropidae). Journal of Experimental Marine Biology and Ecology 26, 297–324.CrossRefGoogle Scholar
Bortolus, A. and Iribarne, O. (1999) Effects of the burrowing crab Chasmagnathus granulata on a Spartina salt marsh. Marine Ecology Progress Series 178, 79–88.CrossRefGoogle Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Buchet, R., Millán, J.M. and Magne, D. (2013) Multisystemic functions of alkaline phosphatases. Methods in Molecular Biology 1053, 27–51.CrossRefGoogle ScholarPubMed
Carter, C.G. and Mente, E. (2014) Protein synthesis in crustaceans: a review focused on feeding and nutrition. Central European Journal of Biology 9, 1–10.Google Scholar
Ceccaldi, H.J. (1989) Anatomy and physiology of digestive tract of Crustaceans Decapods reared in aquaculture. Advances In Tropical Aquaculture Tahiti; Aquacop. Ifremer. Actes de Colloque 9, 243–259.Google Scholar
Chan, J. and Stinson, R. (1986) Dephosphorylation of phosphoproteins of human liver plasma membranes by endogenous and purified liver alkaline phosphatases. Journal of Biological Chemistry 261, 7635–7639.CrossRefGoogle ScholarPubMed
Chen, Q.-X., Zheng, W.-Z., Lin, J.-Y., Cai, Z.-T. and Zhou, H.-M. (2000) Kinetic of inhibition of green crab (Scylla serrata) alkaline phosphatase by vanadate. Biochemistry (Moscow) 65, 1105–1110.Google ScholarPubMed
Chen, Q.X. and Zhou, H.M. (1998) An essential lysine residue of green crab (Scylla serrata) alkaline phosphatase. Biochemistry and Molecular Biology International 46, 225–231.Google ScholarPubMed
Díez-Zaera, M., Díaz-Hernández, J.I., Hernández-Álvarez, E., Zimmermann, H., Díaz-Hernández, M. and Miras-Portugal, M.T. (2011) Tissue-nonspecific alkaline phosphatase promotes axonal growth of hippocampal neurons. Molecular Biology of the Cell 22, 1014–1024.CrossRefGoogle ScholarPubMed
Fanjul, E., Grela, M.A., Canepuccia, A. and Iribarne, O. (2008) The Southwest Atlantic intertidal burrowing crab Neohelice granulata modifies nutrient loads of phreatic waters entering coastal area. Estuaries and Coastal Shelf Sciences 79, 300–306.CrossRefGoogle Scholar
Freire, C.A., Onken, H. and McNamara, J.C. (2008) A structure function analysis of ion transport in crustacean gills and excretory organs. Comparative Biochemistry and Physiology A 151, 272–304.CrossRefGoogle ScholarPubMed
Geddes, K. and Philpott, D.J. (2008) A new role for intestinal alkaline phosphatase in gut barrier maintenance. Gastroenterology 135, 8–12.CrossRefGoogle ScholarPubMed
Gibson, R. and Barker, P.L. (1979) The decapod hepatopancreas. Oceanography and Marine Biology: An Annual Review 17, 285–346.Google Scholar
Gomori, G. (1955) Preparation of buffers for use in enzyme studies. Methods in Enzymology 1, 138–146.CrossRefGoogle Scholar
Iribarne, O., Bortolus, A. and Botto, F. (1997) Between-habitats differences in burrow characteristics and trophic modes in the southwestern Atlantic burrowing crab Chasmagnathus granulata. Marine Ecology Progress Series 155, 132–145.CrossRefGoogle Scholar
Iribarne, O., Martinetto, P., Schwindt, E., Botto, F., Bortolus, A. and García Borboroglu, P. (2003) Evidence of habitat displacement between two common soft-bottom SW Atlantic intertidal crabs. Journal of Experimental Marine Biology and Ecology 296, 167–182.CrossRefGoogle Scholar
Jahn, M.P., Cavagni, G.M., Kaiser, D. and Kucharski, L.C. (2006) Osmotic effect of choline and glycine betaine on the gills and hepatopancreas of the Chasmagnathus granulata crab submitted to hyperosmotic stress. Journal of Experimental Marine Biology and Ecology 334, 1–9.CrossRefGoogle Scholar
Lallès, J.P. (2014) Luminal ATP: the missing link between intestinal alkaline phosphatase, the gut microbiota, and inflammation? American Journal of Physiology. Gastrointestinal and Liver Physiology 306, 824–825.CrossRefGoogle ScholarPubMed
Larsen, E.H., Deaton, L.E., Onken, H., O'Donnell, M., Grosell, M., Dantzler, W.H. and Weihrauch, D. (2014) Osmoregulation and excretion. Comprehensive Physiology 4, 2–12.Google ScholarPubMed
Li, E., Chen, L., Zeng, C., Yu, N., Xiong, Z., Chen, X. and Qin, J.G. (2008) Comparison of digestive and antioxidant enzymes activities, haemolymph oxyhemocyanin contents and hepatopancreas histology of white shrimp, Litopenaeus vannamei, at various salinities. Aquaculture 274, 80–86.CrossRefGoogle Scholar
Linder, C.H., Englund, U.H., Narisawa, S., Millán, J.L. and Magnusson, P. (2013) Isozyme profile and tissue-origin of alkaline phosphatases in mouse serum. Bone 53, 399–408.CrossRefGoogle Scholar
Linton, S.M., Saborowski, R., Shirley, A.J. and Penny, J.A. (2014) Digestive enzymes of two brachyuran and two anomuran land crabs from Christmas Island, Indian Ocean. Journal of Comparative Physiology B 184. doi: 10.1007/s00360-014-0815-2.CrossRefGoogle ScholarPubMed
Ljungström, M., Norberg, L., Olaisson, H., Wernstedt, C., Vega, F.V., Arvidson, G. and Mårdh, S. (1984) Characterization of proton-transporting membranes from resting pig gastric mucosa. Biochimica et Biophysica Acta 769, 209–219.CrossRefGoogle ScholarPubMed
López Mañanes, A.A., Magnoni, L.J. and Goldemberg, A.L. (2000) Branchial carbonic anhydrase (CA) of gills of Chasmagnathus granulata (Crustacea Decapoda). Comparative and Biochemical Physiology B 127, 85–95.CrossRefGoogle ScholarPubMed
Lovett, D., Towle, D. and Faris, J. (1994) Salinity-sensitive alkaline phosphatase activity in gills of the blue crab, Callinectes sapidus Rathbun. Comparative and Biochemical Physiology B 109, 163–173.CrossRefGoogle Scholar
Luppi, T., Bas, C., Méndez Casariego, A., Albano, M., Lancia, J., Kittlein, M., Rosenthal, A., Farías, N., Spivak, E. and Iribarne, O. (2013) The influence of habitat, season and tidal regime in the activity of the intertidal crab Neohelice (=Chasmagnathus) granulata. Helgoland Marine Research 67, 1–15.CrossRefGoogle Scholar
Martins, T.L., Chittó, A.L.F., Rossetti, C.R., Brondani, C.K., Kucharski, L.C. and Da Silva, R.S.M. (2011) Effects of hypo- or hyperosmotic stress on lipid synthesis and gluconeogenic activity in tissues of the crab Neohelice granulata. Comparative Biochemistry and Physiology A 158, 400–405.CrossRefGoogle ScholarPubMed
Mazorra, M.T., Rubio, J.A. and Blasco, J. (2002) Acid and alkaline phosphatase activities in the clam Scrobicularia plana: kinetic characteristics and effects of heavy metals. Comparative Biochemistry and Physiology B 131, 241–249.CrossRefGoogle ScholarPubMed
McGaw, I. and Curtis, D. (2013) A review of gastric processing in decapod crustaceans. Journal of Comparative Physiology B 183, 443–465.CrossRefGoogle ScholarPubMed
McNamara, J.C. and Faria, S.C. (2012) Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. Journal of Comparative Physiology B 182, 997–1014.CrossRefGoogle ScholarPubMed
Méndez, E., López Mañanes, A.A. and Pinoni, S.A. (2011) Lipase activity in the hepatopancreas of the euryhaline crab Neohelice granulata: short and long term postfeeding response. Biocell 35, A142–A164.Google Scholar
Méndez, E., López Mañanes, A.A. and Pinoni, S.A. (2012) Proteolytic activity in hepatopancreas of the euryhaline crab Neohelice granulata: response to hyper-regulation and feeding. Biocell 36, A32–A61.Google Scholar
Michiels, M.S., del Valle, J.C. and López Mañanes, A.A. (2013) Effect of environmental salinity and dopamine injections on key digestive enzymes in hepatopancreas of the euryhaline crab Cyrtograpsus angulatus (Decapoda: Brachyura: Varunidae). Scientia Marina 77, 129–136.Google Scholar
Michiels, M.S., del Valle, J.C. and López Mañanes, A.A. (2015a) Biochemical characteristics and modulation by external and internal factors of aminopeptidase-N activity in the hepatopancreas of a euryhaline burrowing crab. Journal of Comparative Physiology – B. doi: 10.1007/s00360-015-0899-3.CrossRefGoogle ScholarPubMed
Michiels, M.S., del Valle, J.C. and López Mañanes, A.A. (2015b) Lipase activity sensitive to dopamine, glucagon and cyclic AMP in hepatopancreas of the euryhaline burrowing crab Neohelice granulata. Crustaceana 88, 51–65.CrossRefGoogle Scholar
Millán, J.L. (2006) Alkaline phosphatases: structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal 2, 335–341.CrossRefGoogle ScholarPubMed
Monin, M. and Rangneker, P.V. (1974) Histochemical localization of acid and alkaline phosphatases and glucose-6-phosphatase of the hepatopancreas of the crab, Scylla serrata (Forskål). Journal of Experimental Marine Biology and Ecology 14, 1–16.CrossRefGoogle Scholar
Mota, A., Silva, P., Neves, D., Lemos, C., Calhau, C., Torres, D., Martel, F., Fraga, H., Ribeiro, L., Alçada, M.N., Pinho, M.J., Negrão, M.R., Pedrosa, R., Guerreiro, S., Guimarães, J.T., Azevedo, I. and Martins, M.J. (2008) Characterization of rat heart alkaline phosphatase isoenzymes and modulation of activity. Brazilian Journal of Medical and Biological Research 41, 600–609.CrossRefGoogle ScholarPubMed
Muhlia-Almazán, A. and Garcia-Carreño, F.L. (2003) Digestion physiology and proteolytic enzymes of crustacean species of the Mexican Pacific Ocean. In Henrickx, M.E. (ed.) Contributions to the Study of the East Pacific Crustaceans, Volume 2. Instituto de Ciencias del Mar y Limnologia, UNAM, Mexico, pp. 77–91.Google Scholar
Ohkubo, A., Langerman, N. and Kaplan, M.M. (1974) Rat liver alkaline phosphatase. Purification and properties. Journal of Biological Chemistry 249, 7174–7180.CrossRefGoogle Scholar
Olsen, R.L., Øverbo, K. and Myrnes, B. (1991) Alkaline phosphatase from the hepatopancreas of shrimp (Pandalus borealis): a dimeric enzyme with catalytically active subunits. Comparative Biochemistry and Physiology B 99, 755–761.CrossRefGoogle Scholar
Pinoni, S.A. (2009) Mecanismos de mantenimiento del medio interno en respuesta a estrés ambiental en crustáceos decápodos de interés regional. PhD thesis, Universidad Nacional de Mar del Plata, Argentina, 168 pp.Google Scholar
Pinoni, S.A., Goldemberg, A.L. and López Mañanes, A.A. (2005) Alkaline phosphatase activities in muscle of the euryhaline crab Chasmagnathus granulatus: response to environmental salinity. Journal of Experimental Marine Biology and Ecology 326, 217–226.CrossRefGoogle Scholar
Pinoni, S.A., Iribarne, O. and López Mañanes, A. (2011) Between-habitat comparison of digestive enzymes activities and energy reserves in the SW Atlantic euryhaline burrowing crab Neohelice granulata. Comparative Biochemistry and Physiology A 158, 552–559.CrossRefGoogle ScholarPubMed
Pinoni, S.A. and López Mañanes, A.A. (2004) Alkaline phosphatase activity sensitive to environmental salinity and dopamine in muscle of the euryhaline crab Cyrtograpsus angulatus. Journal of Experimental Marine Biology and Ecology 307, 35–46.CrossRefGoogle Scholar
Pinoni, S.A. and López Mañanes, A.A. (2008) Partial characterization and response under hyper-regulating conditions of Na+/K+-ATPase and levamisole-sensitive alkaline phosphatase activities in chela muscle of the euryhaline crab Cyrtograpsus angulatus. Scientia Marina 72, 15–24.Google Scholar
Pinoni, S.A. and López Mañanes, A.A. (2009) Na+ATPase activities in chela muscle of the euryhaline crab Neohelice granulata: differential response to environmental salinity. Journal of Experimental Marine Biology and Ecology 372, 91–97.CrossRefGoogle Scholar
Pinoni, S.A. and López Mañanes, A.A. (2014) Lipase and proteolytic activities in hepatopancreas of Neohelice granulata: biogenic amines effect. Biocell 38, A54.Google Scholar
Pinoni, S.A., Michiels, M.S. and López Mañanes, A.A. (2013) Phenotypic flexibility in response to environmental salinity in the euryhaline crab Neohelice granulata from the mudflat and the saltmarsh of a SW coastal lagoon. Marine Biology 160, 2647–2661.CrossRefGoogle Scholar
Romano, N. and Zeng, C. (2012) Osmoregulation in decapod crustaceans: implications to aquaculture productivity, methods for potential improvement and interactions with elevated ammonia exposure. Aquaculture 334–337, 12–23.CrossRefGoogle Scholar
Sánchez-Paz, A., García-Carreño, F., Muhlia-Almazan, A., Peregrino-Uriarte, A. and Yepiz-Plascencia, J.Y.G. (2006) Usage of energy reserves in crustaceans during starvation: status and future directions. Insect Biochemical and Molecular Biology 36, 241–249.CrossRefGoogle ScholarPubMed
Schleich, C.E., Goldemberg, A.L. and López Mañanes, A.A. (2001) Salinity dependent Na+/K+-ATPase activity in gills of euryhaline crab Chasmagnathus granulatus. General Physiology and Biophysics 20, 255–266.Google Scholar
Simao, A.M.S., Marcio, M., Beloti, A.L., de Oliveira, P.T., Granjeiro, J.M., Pizauro, J.M. and Ciancaglini, P. (2007) Culture of osteogenic cells from human alveolar bone: a useful source of alkaline phosphatase. Cell Biology International 31, 1405–1413.CrossRefGoogle Scholar
Spivak, E. (1997) Cangrejos estuariales del Atlántico sudoccidental (25°–41°S) (Crustacea: Decapoda: Brachyura). Investigaciones Marinas Valparaíso 25, 105–120.Google Scholar
Spivak, E.D. (2010) The crab Neohelice (=Chasmagnathus) granulata: an emergent animal model from emergent countries. Helgoland Marine Research 64, 149–154.CrossRefGoogle Scholar
Spivak, E., Anger, K., Luppi, T., Bas, C. and Ismael, D. (1994) Distribution and habitat preferences of two grapsid crab species in Mar Chiquita lagoon (Pcia. Bs As. Argentina). Helgoland Meeresunters 48, 59–78.CrossRefGoogle Scholar
Verri, T., Mandal, A., Zilli, L., Bossa, D., Mandal, P.K., Ingrosso, L., Zonno, V., Viella, S., Aheam, G.A. and Storelli, C. (2001) D-Glucose transport in decapod crustacean hepatopancreas. Comparative Biochemistry and Physiology A 130, 585–606.CrossRefGoogle ScholarPubMed
Wang, Z.-J., Lee, J., Sia, Y.X., Wanga, W., Yangd, J.M., Yina, S.J., Qiana, G.Y. and Parka, Y.D. (2014) A folding study of Antarctic krill (Euphausia superba) alkaline phosphatase using denaturants. International Journal of Biological Macromolecules 70, 266–274.CrossRefGoogle ScholarPubMed
Zeng, H., Ye, H., Li, S., Wang, G. and Huang, J. (2010) Hepatopancreas cell cultures from mud crab, Scylla paramamosain. In Vitro Cellular & Developmental Biology—Animal 46, 431–437.CrossRefGoogle ScholarPubMed