Skip to main content

Advertisement

SpringerLink
Log in

Biosynthetic Capacity of Rainbow Trout (Oncorhynchus mykiss) Interrenal Tissue After Cadmium Exposure

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

The disruption of endocrine system function in wildlife species, including teleosts, by contaminants such as metals is presently of major environmental concern. Recently, it has been shown that cadmium (Cd) exposure results in significant reductions in corticosteroid secretion by fish interrenal steroidogenic cells, likely through an inhibition of intracellular cortisol synthesis. In the present study, the effects of CdCl2 on unstimulated and stimulated interrenal steroidogenesis in rainbow trout were examined with the intention of furthering an understanding of the site(s) of Cd toxic action. CdCl2 alone reduced cortisol secretion in minced interrenal tissues to 59% and 55% of control values when exposed to 10 and 100 μM, respectively. Incubation of interrenal tissues with 0.01 IU/mL adrenocorticotropic hormone (ACTH), which activates rate-limiting steps in steroid synthesis, resulted in significant stimulation of steroidogenesis in controls. However, ACTH-stimulated steroidogenesis was reduced when tissues were previously incubated with Cd. Maximal rates of unstimulated cortisol secretion were achieved by augmentation using 5 μM 25-hydroxycholesterol (25-OHC) or 0.8 μL/mL synthetic cholesterol [SyntheChol®(SC)]. Steroidogenesis augmentation by 25-OHC was significantly reduced in tissues incubated with Cd. Interestingly, cortisol secretion was significantly higher in SC-augmented tissue exposed to 1 and 10 μM Cd when compared to augmented control tissues. The results of this study show that Cd affects both stimulated and unstimulated steroidogenesis in rainbow trout, and that one major site(s) of action of Cd in the cortisol synthesis pathway is likely prior to cytochrome P450 side chain cleavage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

References

  • Almeida JA, Diniz YS, Marques SFG, Faine LA, Ribas BO, Burneiko RC, Novelli ELB (2002) The use of oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environ Int 27:673–679

    Article  CAS  Google Scholar 

  • Azhar S, Leers-Sucheta S, Reaven E (2003) Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and ‘selective’ pathway connection. Front Biosci 8:998–1029

    Google Scholar 

  • Bauer MP, Bridgham JT, Langenau DM, Johnson AL, Goetz FW (2000) Conservation of steroidogenic acute regulatory (StAR) protein structure and expression in vertebrates. Mol Cell Endocrinol 168:119–125

    Article  CAS  Google Scholar 

  • Brodeur JC, Daniel C, Ricard AC, Hontela A (1998) In vitro response to ACTH of interrenal tissue of rainbow trout (Oncorhynchus mykiss) exposed to cadmium. Aquat Toxicol 42:103–113

    Article  CAS  Google Scholar 

  • Brodeur JC, Sherwood G, Rasmussen JB, Hontela A (1997) Impaired cortisol secretion in yellow perch (Perca flavescens) from lakes contaminated by heavy metals: in vivo and in vitro assessment. Can J Fish Aquat Sci 54:2752–2758

    Article  CAS  Google Scholar 

  • Calogero AE, Bagdy G, Moncada ML, D’Agata R (1993) Effect of selective serotonin agonists on basal, corticotrophin-releasing hormone- and vasopressin-induced ACTH release in vitro from rat pituitary cells. J Endocrinol 136:381–387

    CAS  Google Scholar 

  • Canadian Environmental Protection Act (1994) Cadmium and its compounds (Priority substances list assessment report). Government of Canada, p 15

  • Fu H, Steinebach OM, van den Hamer CJA, Balm PHM, Lock RAC (1990) Involvement of cortisol and metallothionein-like proteins in the physiological responses of tilapia (Oreochromis mossambicus) to sublethal cadmium stress. Aquat Toxicol 16:257–270

    Article  CAS  Google Scholar 

  • Grahame-Smith D, Butcher R, Ney R, Sutherland ER (1967) Adenosine 3′, 5′-monophosphate as the intracellular mediator of the action of adrenocorticotropic hormone on the adrenal cortex. J Biol Chem 242:5535–5541

    CAS  Google Scholar 

  • Hansen JA, Welsh PG, Lipton J, Cacela D, Dailey AD (2002) Relative sensibility of bull trout (Salvelinus confluentus) and rainbow trout (Oncorhynchus mykiss) to acute exposures of cadmium and zinc. Environ Toxicol Chem 21:67–75

    Article  CAS  Google Scholar 

  • Henson MC, Chedrese PJ (2004) Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp Biol Med 229:383–392

    CAS  Google Scholar 

  • Hill CW, Fromm PO (1968) Response of the interrenal gland of rainbow trout (Salmo gairdneri) to stress. Gen Comp Endocr 1:69–77

    Article  Google Scholar 

  • Hines GA, Azziz R (1999) Impact of architectural disruption on adrenocortical steroidogenesis in vitro. JCE & M 84:1017–1021

    CAS  Google Scholar 

  • Hontela A, Daniel C, Rasmussen JB (1997) Structural and functional impairment of the hypothalamo-pituitary-interrenal axis in fish exposed to bleached kraft mill effluent in the St Maurice River, Québec. Ecotoxicology 6:1–12

    Article  CAS  Google Scholar 

  • Jefcoate CR, Simpson ER, Boyd GS (1974) Spectral properties of rat adrenal-mitochondrial cytochrome P-450. Eur J Biochem 42:539–551

    Article  CAS  Google Scholar 

  • Kakuta I (2002) Interrenal stress responsiveness of marbled sole, Pleuronectes yokohamae, inhabiting Tokyo Bay. Envir Toxicol 17:1–6

    Article  CAS  Google Scholar 

  • Kallen CB, Arakane F, Christenson LK, Watari H, Devoto L, Strauss JF III (1998) Unveiling the mechanism of action and regulation of the steroidogenic acute regulatory protein. Mol Cell Endocrinol 145:39–45

    Article  CAS  Google Scholar 

  • King SR, Matassa AA, White EK, Walsh LP, Jo Y, Rao RM, Stocco DM, Reyland ME (2004) Oxysterols regulate expression of the steroidogenic acute regulatory protein. J Mol Endocrinol 32:507–517

    Article  CAS  Google Scholar 

  • Kloas W, Reinecke M, Hanke W (1994) Role of atrial natriuretic peptide for adrenal regulation in the teleost fish Cyprinus carpio. Am J Physiol 267:R1034–R1042

    CAS  Google Scholar 

  • Kusakabe M, Todo T, McQuillan HJ, Goetz FW, Young G (2002) Characterization and expression of steroidogenic acute regulatory protein and MLN64 cDNAs in trout. Endocrinology 143:2062–2070

    Article  CAS  Google Scholar 

  • Lacroix A, Hontela A (2004) A comparative assessment of the adrenotoxic effects of cadmium in two teleost species, rainbow trout, Oncorhynchus mykiss, and yellow perch, Perca flavescens. Aquat Toxicol 67:13–21

    Article  CAS  Google Scholar 

  • Lacroix M, Hontela A (2001) Regulation of acute cortisol synthesis by cAMP-dependent protein kinase and protein kinase C in a teleost species, the rainbow trout (Oncorhynchus mykiss). J Endocrinol 169:71–78

    Article  CAS  Google Scholar 

  • Laflamme JS, Couillard Y, Campbell PGC, Hontela A (2000) Interrenal metallothionein and cortisol secretion in relation to Cd, Cu and zinc exposure in yellow perch, Perca flavescens, from Abitibi lakes. Can J Fish Aquat Sci 57:1692–1700

    Article  CAS  Google Scholar 

  • Lappivaara J (2001) Effects of acute handling stress on whitefish Coregonus lavaretus after prolonged exposure to biologically treated and untreated bleached kraft mill effluent. Arch Environ Contam Toxicol 41:55–64

    Article  CAS  Google Scholar 

  • Leblond VS, Hontela A (1999) Effects of in vitro exposures to cadmium, mercury, zinc, and 1-(2-chlorophenyl)-1-(4-chlorophenyl)-2,2-dichloroethane on steroidogenesis by dispersed interrenal cells of rainbow trout (Oncorhynchus mykiss). Toxicol Appl Pharmacol 157:16–22

    Article  CAS  Google Scholar 

  • Lyndersen E, Löfgren S, Arnese RT (2002) Metals in Scandinavian surface waters: effects of acidification, liming, and potential reacidification. Crit Rev Env Sci Technol 32:73–295

    Google Scholar 

  • Mason JI, Arthur JR, Boyd GS (1978) Control of sterol metabolism in rat adrenal mitochondria. Biochem J 173:1045–1051

    Google Scholar 

  • May TW, Wiedmeyer RR, Gober J, Larson S (2001) Influence of mining-related activities on concentration of metals in water and sediment from streams of the Black Hills, South Dakota. Arch Environ Contam Toxicol 40:1–9

    Article  CAS  Google Scholar 

  • McGeer JC, Szebedinszky C, McDonald DG, Wood CM (2000) Effect of chronic sublethal exposure to waterborne Cu, Cd or Zn in rainbow trout. 1: Iono-regulatory disturbance and metabolic costs. Aquat Toxicol 50:231–243

    Article  CAS  Google Scholar 

  • Mgbonyebi OP, Smothers CT, Mrotek JJ (1994) Modulation of adrenal cell functions by cadmium salts: 2. Sites affected by CdCl2 during unstimulated steroid synthesis. Cell Biol Toxicol 10:23–33

    Article  CAS  Google Scholar 

  • Miller WL (1988) Molecular biology of steroid hormone synthesis. Endocrinol Rev 9:295–318

    Article  CAS  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268

    Article  Google Scholar 

  • Page GW (1981) Comparison of groundwater and surface water for patterns and levels of contamination by toxic substances. Environ Sci Technol 15:1475–1481

    Article  CAS  Google Scholar 

  • Pratap HB, Wendelaar Bonga SE (1990) Effects of water-borne cadmium on plasma cortisol, and glucose in the cichlid fish Oreochromis mossambicus. Comp Biochem Physiol 95C:313–317

    CAS  Google Scholar 

  • Pratap HB, Wendelaar Bonga SE (1993) Effects of ambient and dietary cadmium on pavement cells, chloride cells, and Na+/K+ -ATPase activity in the gills of the freshwater teleost Oreochromis mossambicus at normal and high calcium levels in the ambient water. Aquat Toxicol 26:133–149

    Article  CAS  Google Scholar 

  • Ricard AC, Daniel C, Anderson P, Hontela A (1998) Effects of subchronic exposure to cadmium chloride on endocrine and metabolic functions in rainbow trout (Oncorhynchus mykiss). Arch Environ Contam Toxicol 34:377–381

    Article  CAS  Google Scholar 

  • Schreck CB (1990) Physiological, behavioral, and performance indicators of stress. In: Adams SM (eds) Biological indicators of stress in fish. American Fisheries Society, Maryland, p 29–37

    Google Scholar 

  • Schreck CB, Bradford CS, Fitzpatrick MS, Patiño R (1989) Regulation of the interrenal of fishes: non-classical control mechanisms. Fish Physiol Biochem 7:259–265

    Article  CAS  Google Scholar 

  • Scott GR, Sloman KA, Rouleau C, Wood CM (2003) Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 206:1779–1790

    Article  CAS  Google Scholar 

  • Sloman KA, Scott GR, Diao Z, Rouleau C, Wood CM, McDonald DG (2003) Cadmium affects the social behavior of rainbow trout, Oncorhychus mykiss. Aquat Toxicol 65:171–185

    Article  CAS  Google Scholar 

  • Talley D, Cutak B, Rathbone E, Al-Kolla T, Allison D, Blasberg J, Kao K, Caple M (2003) SyntheCholTM synthetic cholesterol for cholesterol dependent cell culture—development of non-animal derived chemically defined NSO medium. 18th Meeting of European Society for Animal Cell Technology. Granada, Spain (Poster Presented)

  • Taylor HE, Garbarino JR, Brinton TI (1990) The occurrence and distribution of trace metals in the Mississippi river and its tributaries. Sci Total Environ 97–98:369–384

    Article  Google Scholar 

  • Thomas P (1989) Effects of Aroclor 1254 and Cadmium on reproductive endocrine function and ovarian growth in atlantic croaker. Mar Environ Res 28:499–503

    Article  CAS  Google Scholar 

  • Thorton I (1992) Sources and pathways of cadmium in the environment, Vol. 118. IARC Science Publication, p 149–162

  • Tilton SC, Foran CM, Benson WH (2003) Effects of cadmium on the reproductive axis of Japanese medaka (Oryzias latipes). Comp Biochem Physiol C 136:265–276

    Google Scholar 

  • Vaglio A, Landriscina C (1999) Changes in liver enzyme activity in the teleost Sparus aurata in response to cadmium intoxication. Ecotoxicol Environ Saf 43:111–116

    Article  CAS  Google Scholar 

  • Wilson JM, Vijayan MM, Kennedy CJ, Iwama GK, Moon TW (1998) β-Napthoflavone abolishes interrenal sensitivity to ACTH stimulation in rainbow trout. J Endocrinol 157:63–70

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by an NSERC individual research grant to C.J.K. The authors wish to thank Mr. B. Leighton animal care and Mr. W. Leung for research assistance.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6

    H. M. Lizardo-Daudt, Onkar S. Bains, Christopher R. Singh & Christopher J. Kennedy

  2. Universidade do Vale do Rio dos Sinos, Sao Leopoldo, RS, Brazil

    H. M. Lizardo-Daudt

Authors
  1. H. M. Lizardo-Daudt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Onkar S. Bains
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher R. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher J. Kennedy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher J. Kennedy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lizardo-Daudt, H.M., Bains, O.S., Singh, C.R. et al. Biosynthetic Capacity of Rainbow Trout (Oncorhynchus mykiss) Interrenal Tissue After Cadmium Exposure. Arch Environ Contam Toxicol 52, 90–96 (2007). https://doi.org/10.1007/s00244-005-0155-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-005-0155-z

Keywords

Search

Navigation