Abstract
This review is an update of information recently obtained about the physiological, cellular, and molecular mechanisms used by crustacean organ systems to regulate and detoxify environmental heavy metals. It uses the American lobster, Homarus americanus, and other decapod crustaceans as model organisms whose cellular detoxification processes may be widespread among both invertebrates and vertebrates alike. The focus of this review is the decapod hepatopancreas and its complement of metallothioneins, membrane metal transport proteins, and vacuolar sequestration mechanisms, although comparative remarks about potential detoxifying roles of gills, integument, and kidneys are included. Information is presented about the individual roles of hepatopancreatic mitochondria, lysosomes, and endoplasmic reticula in metal sequestration and detoxification. Current working models for the involvement of mitochondrial and endoplasmic reticulum calcium-transport proteins in metal removal from the cytoplasm and the inhibitory interactions between the metals and calcium are included. In addition, copper transport proteins and V-ATPases associated with lysosomal membranes are suggested as possible sequestration processes in these organelles. Together with several possible cytoplasmic divalent and trivalent anions such as sulfate, oxalate, or phosphate, accumulations of metals in lysosomes and their complexation into detoxifying precipitation granules may be regulated by variations in lysosomal pH brought about by bafilomycin-sensitive proton ATPases. Efflux processes for metal transport from hepatopancreatic epithelial cells to the hemolymph are described, as are the possible roles of hemocytes as metal sinks. While some of the cellular processes for isolating heavy metals from general circulation occur in the hepatopancreas and are beginning to be understood, very little is currently known about the roles of the gills, integument, and kidneys in metal regulation. Therefore, much remains to be clarified about the organs and mechanisms involved in metal homeostasis in decapod crustaceans.
Similar content being viewed by others
Abbreviations
- ER :
-
endoplasmic reticulum
- SERCA :
-
sarco/endoplasmic reticulum calcium ATPase
- V-ATPase:
-
vacuolar ATPase
- PMCA :
-
plasma membrane calcium ATPase
References
Ahearn GA (1980) Intestinal electrophysiology and transmural ion transport in freshwater prawns. Am J Physiol 239:C1–C10
Ahearn GA (1982) Water and solute transport in crustacean gastrointestinal trace. In: Podesta RB (ed) Membrane physiology of invertebrates. Marcel Dekker, New York, pp 261–339
Ahearn GA (1984) Sigmoid kinetics of sodium chloride transport in crustacean intestine. In: Gerencser GA (ed) Chloride transport coupling in biological membranes and epithelia. Elsevier/North Holland Press, Amsterdam, pp 121–149
Ahearn GA (1996) The invertebrate electrogenic 2Na+/1H+ exchanger: polyfunctional epithelial workstation. News Physiol Sci 11:31–35
Ahearn GA, Clay LP (1989) Kinetic analysis of electrogenic 2Na/1H antiport in crustacean hepatopancreas. Am J Physiol 257:R484–R493
Ahearn GA, Franco P (1990) Na and Ca share the electrogenic 2Na/1H antiporter in crustacean antennal glands. Am J Physiol 259:F758–F767
Ahearn GA, Franco P (1991) Electrogenic 2Na/1H antiport in echinoderm gastrointestinal epithelium. J Exp Biol 158:495–507
Ahearn GA, Franco P (1993) Ca transport pathways in brush border membrane vesicles of crustacean antennal glands. Am J Physiol 264:R1206–R1213
Ahearn GA, Zhuang Z (1996) Cellular mechanisms of calcium transport in crustaceans. Physiol Zool 69:383–402
Ahearn GA, Maginniss LA, Song YK, Tornquist A (1977) Intestinal water and ion transport in freshwater malacostracan prawns (Crustacea). In: Jungreis AM, Hodges T, Kleinzeller A, Schultz S (eds) Water relations in membrane transport in plants and animals. Academic Press, New York, pp 129–142
Ahearn GA, Grover ML, Tsuji RT, Clay LP (1987) Proton-stimulated Cl/HCO3 antiport by purified lobster hepatopancreatic basolateral membrane vesicles. Am J Physiol 252:R859–R870
Ahearn GA, Franco P, Clay LP (1990) Electrogenic 2Na/1H exchange in crustaceans. J Membr Biol 116:215–226
Ahearn GA, Zhuang Z, Duerr J, Pennington V (1994) Role of the invertebrate electrogenic 2Na+/1H+ antiporter in monovalent and divalent cation transport. J Exp Biol 196:319–335
Ahearn HRH, Ahearn GA, Gomme J (2000) Effects of cadmium on integumentary uptake of 3H-l-histidine in the marine polychaete worm, Nereis succinea. J Exp Biol 203:2877–2885
Al-Mohanna SY, Nott JA (1985) The accumulation of metals in the hepatopancreas of the shrimp, Penaeus semisulcatus de Haan (Crustacea: Decapoda) during the moult cycle. Proc Conf Mar Environ Pollut, pp 195–209
Al-Mohanna SY, Nott JA (1987) R-cells and the digestive cycle in Penaeus semisulcatus de Haan (Crustacea: Decapoda). Mar Biol 95:129–137
Becker GL, Chen C, Greenawalt JW, Lehninger AL (1974) Calcium phosphate granules in the hepatopancreas of the blue crab Callinectes sapidus. J Cell Biol 61:316–326
Becker GL, Termine JD, Eanes ED (1976) Comparative studies of intra- and extramitochondrial calcium phosphates from the hepatopancreas of the blue crab (Callinectes sapidus). Calcif Tissue Res 21:105–113
Behnke RD, Wong RK, Huse SM, Reshkin SJ, Ahearn GA (1990) Proline transport by brush border membrane vesicles of lobster antennal glands. Am J Physiol 258:F311–F320
Behnke RD, Busquets-Turner L, Ahearn GA (1998) Epithelial glucose transport by lobster antennal gland. J Exp Biol 201:3385–3393
Brouwer M, Winge DR, Gray WR (1989) Structural and functional diversity of copper-metallothioneins from the American lobster Homarus americanus. J Inorg Biochem 35:289–303
Brouwer M, Schlenk D, Ringwood AH, Brouwer-Hoexum T (1992) Metal-specific induction of metallothionein isoforms in the blue crab Callinectes sapidus in response to single- and mixed-metal exposure. Arch Biochem Physiol 294:461–468
Brouwer M, Enghild J, Hoexum-Brouwer T, Thogersen I, Truncali A (1995) Primary structure and tissue-specific expression of blue crab (Callinectes sapidus) metallothionein isoforms. Biochem J 311:617–622
Brouwer M, Syring R, Brouwer TH (2002) Role of a copper-specific metallothionein of the blue crab, Callinectes sapidus, in copper metabolism associated with degradation and synthesis of hemocyanin. J Inorg Biochem 88:228–239
Brown BE (1982) The form and function of metal-containing “granules” in invertebrate tissues. Biol Rev 57:621–667
Bull PC, Thomas GR, Rommens JM, Forbes JR, Cox DW (1993) The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat Genet 5:327–337
Bury NR, Grosell M, Grover AK, Wood CM (1999) ATP-dependent silver transport across the basolateral membrane of rainbow trout gills. Toxicol Appl Pharmacol 159:1–8
Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206:11–23
Capo JA, Mandal PK, Eyyunni S, Ahearn GA (2004) 65Zn2+ transport by lobster hepatopancreatic basolateral membrane vesicles. (submitted)
Cattey MA, Gerencser GA, Ahearn GA (1992) Electrogenic H-regulated sulfate-chloride exchange in lobster hepatopancreatic brush border membrane vesicles. Am J Physiol 262:R255–R262
Chassard-Bouchaud C (1981) Role des lysosomes dans le phenomene de concentration du cadmium. Microanalyse par spectrographie des rayons X. C R Acad Sci Paris 261–265
Chavez-Crooker P, Garrido N, Ahearn GA (2001) Copper transport by lobster hepatopancreatic epithelial cells separated by centrifugal elutriation: measurements with the fluorescent dye, Phen Green. J Exp Biol 204:1433–1444
Chavez-Crooker P, Garrido N, Ahearn GA (2002) Copper transport by lobster (Homarus americanus) hepatopancreatic mitochondria. J Exp Biol 205:405–413
Chavez-Crooker P, Garrido N, Pozo P, Ahearn GA (2003) Copper transport by lobster (Homarus americanus) hepatopancreatic lysosomes. Comp Biochem Physiol 135C:107–118
Chelly J, Turner Z, Tonnesen T, Patterson A, Ishikawa-Brush Y (1993) Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat Genet 3:14–19
Conrad EM, Ahearn GA (2003) Effect of Zn2+ on transmural transport of 3H-l-histidine across perfused intestine of the American lobster, Homarus americanus. FASEB J 17:A470
Conrad EM, Ahearn GA (2004) Zinc-histidine co-transport by a PEPT-1-like transport system in lobster (Homarus americanus) intestine. FASEB J 18:A706
Coombs T, George SG (1978) Mechanisms of immobilization and detoxification of metals in marine organisms. In: McLusky DS, Berry AJ (eds) Physiology and behaviour of marine organisms. Pergamon Press, New York, pp 179–187
Dancis A, Haile D, Yuan DS, Klausner RD (1994) The Saccharomyces cerevisiae copper transport protein (Ctr1p). Biochemical characterization, regulation by copper, and physiologic role in copper uptake. J Biol Chem 269:25660–25667
Fei Y, Kanai Y, Nussberger S, Ganapathy V, Leibach FH, Romero MF, Singh SK, Boron WF, Hediger MA (1994) Expression cloning of a mammalian proton-coupled oligopeptide transporter. Nature 368:563–566
Gaither LA, Eide DJ (2000) Functional expression of the human hZIP2 zinc transporter. J Biol Chem 275:5560–5564
Gaither, LA Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14:251–270
George SG (1983) Heavy metal detoxification in the mussel Mytilis edulis: composition of Cd-containing kidney granules (tertiary lysosomes). Comp Biochem Physiol 76C:53–57
George SG, Pirie BJS, Cheyne AR, Coombs TL, Grant PT (1978) Detoxification of metals by marine bivalves: an ultrastructural study on the compartmentation of copper and zinc in the oyster Ostrea edulis. Mar Biol 45:147–156
Gerencser GA (1996) The chloride pump: a Cl−-translocating P-type ATPase. Crit Rev Biochem Mol Biol 31:303–337
Gerencser GA, Cattey MA, Ahearn GA (1995) Sulfate-oxalate exchange in lobster hepatopancreatic basolateral membrane vesicles. Am J Physiol 38:R572–R577
Gerencser GA, Ahearn GA, Cattey MA (1999) Sulfate/bicarbonate antiport by lobster hepatopancreatic basolateral membrane vesicles. J Exp Zool 284:158–167
Gerencser GA, Burgin C, Robins F, Ahearn GA (2000a) The oxalate/sulfate antiporter in lobster hepatopancreas: internal and external binding constants. J Exp Biol 203:1497–1502
Gerencser GA, Ahearn GA, Robbins F, Cattey MA (2000b) Chloride transport by lobster hepatopancreas is facilitated by several anion antiport mechanisms. Comp Biochem Physiol 125A:223–228
Gerencser GA, Ahearn GA, Zhang J, Cattey MA (2001) Sulfate transport mechanisms in epithelial systems. J Exp Zool 289:245–253
Grosell M, Wood CM (2002) Copper uptake across rainbow trout gills: mechanisms of apical entry. J Exp Biol 205:1179–1188
Grinstein S (1988) Na/H exchange. CRC Press, Boca Raton
Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1977) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388:482–488
Hagedorn M, Weihrauch D, Towle DW, Ziegler A (2003) Molecular characterization of the smooth endoplasmic reticulum Ca2+-ATPase of Porcellio scaber and its expression in sternal epithelia during the moult cycle. J Exp Biol 206:2167–75
Havelaar AC, de Gast IL, Snijders S, Beerens CEMT, Mancini GMS, Verheijen FW (1998) Characterization of a heavy metal ion transporter in the lysosomal membrane. FEBS Lett 436:223–227
Hopkin SP (1989) Ecophysiology of metals in terrestrial invertebrates. Elsevier Applied Science, London
Horn NM, Thomas AL, Tompkins JD (1995) The effect of histidine and cysteine on zinc influx into rat and human erythrocytes. J Physiol (Lond) 489:73–80
Kampfenkel K, Kushnir S, Babiychuk E, Inze D, Montagu MV (1995) Molecular characterization of a putative Arabidopsis thaliana copper transporter and its yeast homologue. J Biol Chem 270:28479–28486
Klein MJ, Ahearn GA (1999) Calcium transport processes of lobster hepatopancreatic mitochondria. J Exp Zool 283:147–159
Lee J, Prohaska JR, Dagenais SL, Glover TW, Thiele DJ (2000) Isolation of a murine copper transporter gene, tissue specific expression and functional complementation of a yeast copper transport mutant. Gene 254:87–96
Lee J, Prohaska JR, Thiele DJ (2001) Essential role for mammalian copper transporter Ctr1 in copper homeostasis and embryonic development. Proc Natl Acad Sci USA 98:6842–684
Lee J, Petris MJ, Thiele DJ (2002) Characterization of mouse embryonic cells deficient in the Ctr1 high affinity copper transporter: identification of a Ctr1-independent copper transport system. J Biol Chem 277:40253–40259
Liang R, Fei Y, Prasad PD, Ramamoorthy S, Han H, Yang-Feng TL, Hediger MA, Ganapathy V, Leibach FH (1995) Human intestinal H+/peptide cotransporter. J Biol Chem 270:6456–6463
MacLennan DH, Brandl CJ, Korczak B, Green NM (1985) Amino acid sequence of a Ca2+Mg2+-dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence. Nature 316:696–700
Mason AZ, Simkiss K (1982) Sites of mineral deposition in metal-accumulating cells. Exp Cell Res 139:383–391
Mason AZ, Simkiss K, Ryan KP (1984) The ultrastructural localization of metals in specimens of Littorina littorea collected from clean and polluted sites. J Exp Mar Biol UK 64:699–720
Mauri M, Orlando E (1982) Experimental study on renal concretions in the wedge shell Donax trunculus L. J Exp Mar Biol UK 63:47–57
McMahon RJ, Cousins RJ (1998) Mammalian zinc transporters. J Nutr 128:667–670
Menkes JH, Alter M, Steigleder GK, Weakly DR, Sung JH (1962) A sex-linked recessive disorder with retardation of growth, peculiar hair, and focal cerebral and cerebellar degeneration. Pediatrics 29:764–779
Mercer JF, Livingston J, Hall B, Paytner JA, Begy C (1993) Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat Genet 3:20–25
Moore MN (1977) Lysosomal responses to environmental chemicals in some marine invertebrates. In: Giam CS (ed) Pollutant effects on marine organisms. DC Heath, Lexington, MA, pp 143–165
Peppler JE, Ahearn GA (2003) Effect of heavy metals on the uptake of 3H-l-histidine by the polychaete Nereis succinea. Comp Biochem Physiol 136C:181–189
Petrukhin K, Fischer SG, Pirastu M, Tanzi RE, Chernov I (1993) Mapping, cloning and genetic characterization of the region containing the Wilson disease gene. Nat Genet 5:338–343
Pirie B, Liu F, George S (1985) Ultrastructural localization of copper and zinc in the polychaete Nereis diversicolor, from a highly contaminated estuary. Mar Environ Res 17:197–208
Roesijadi G (1992) Metallothioneins in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–114
Rothstein A (1989) The Na/H exchange system in cell pH and volume control. Rev Physiol Biochem Pharmacol 112:235–257
Shetlar RE, Towle DW (1989) Electrogenic sodium-proton exchange in membrane vesicles from crab (Carcinus maenas) gill. Am J Physiol 257:R924–R931
Tanzi RE, Petrukhin K, Chernov I, Pellequer JL, Ross B (1993) The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nat Genet 5:344–350
Thamotharan M, Ahearn GA (1996) Dipeptide transport by crustacean hepatopancreatic brush border membrane vesicles. J Exp Biol 199:635–641
Verbost PM, Van Rooij J, Flik G, Lock RAC, Bonga SEW (1989) The movement of cadmium through freshwater trout branchial epithelium and its interference with calcium transport. J Exp Biol 145:185–197
Verri T, Kottra G, Romano A, Tiso N, Peric M, Maffia M, Boll M, Argenton F, Daniel H, Storelli C (2003) Molecular and functional characterization of the zebrafish (Danio rerio) PEPT1-type peptide transporter. FEBS Lett 549:115–122
Viarengo A (1989) Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. Rev Aquat Sci 1:295–317
Virarengo A, Nott JA (1993) Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp Biochem Physiol 404C:355–372
Viarengo A, Moore MN, Pertica M, Mancinelli G, Zanicchi G, Pipe RK (1985) Detoxification of copper in the cells of the digestive gland of mussel: the role of lysosomes and thioneins. Sci Total Environ 44:135–145
Viarengo A, Moore MN, Mancinelli G, Mazzucotelli A, Pipe RK, Farrar SV (1987) Metallothioneins and lysosomes in metal toxicity and homeostasis in marine mussels: the effect of cadmium in the presence and absence of phenanthrene. Mar Biol 94:251–257
Vulpe CD, Packman S (1995) Cellular copper transport. Annu Rev Nutr 15:293–322
Vulpe C, Levinson B, Whitney S, Packman S, Gilschier J (1993) Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet 3:7–13
Weinman EJ, Reuss L (1982) Na/H exchange at the apical membrane of Necturus gallbladder. J Gen Physiol 80:299–321
Wheatly M, Gao Y, Freire N, Zanotto FP (2001) Subcellular calcium homeostasis during transepithelial calcium flux associated with crustacean molting: what role do SERCAs and PMCAs play? In: Gay CV, Dacke CG, Danks JA, Cox PA (eds) Proceedings of the 3rd international satellite symposium on the comparative endocrinology of calcium regulation http://www.sci.port.ac.uk/~cecr
Wilson SAK (1912) Brain 34:295–509
Zhang Z, Chen D, Wheatly MG (2000) Cloning and characterization of sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) from crayfish axial muscle. J Exp Biol 203:3411–3423
Zhou B, Gitschier J (1997) hCTR1: a human gene for copper uptake identified by complementation in yeast. Proc Natl Acad Sci USA 94:7481–7486
Zhuang Z, Ahearn GA (1995) Ca2+ and Zn2+ are transported by the electrogenic 2 Na+/1H+ antiporter in echinoderm gastrointestinal epithelium. J Exp Biol 198:1207–1217
Zhuang Z, Ahearn GA (1996) Calcium transport process of lobster hepatopancreatic brush border membrane vesicles. J Exp Biol 119:1195–1208
Zhuang Z, Ahearn GA (1998) Energized Ca2+ transport by hepatopancreatic basolateral membranes of Homarus americanus. J Exp Biol 201:211–220
Acknowledgements
Much of the work reported in this review on the American lobster, Homarus americanus, was supported by National Science Foundation grant IBN99-74569.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume
Rights and permissions
About this article
Cite this article
Ahearn, G.A., Mandal, P.K. & Mandal, A. Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review. J Comp Physiol B 174, 439–452 (2004). https://doi.org/10.1007/s00360-004-0438-0
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-004-0438-0