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Cadmium exposure affects growth performance, energy metabolism, and neuropeptide expression in Carassius auratus gibelio

Abstract

Cadmium (Cd) is the most abundant heavy metal in aquatic environments and is easily detected on a global scale. Carassius auratus gibelio is a common aquaculture species. The aim of this study was to explore the toxic effects of 1, 2, and 4 mg/L Cd on the energy metabolism, growth performance, and neurological responses of C. gibelio. After 30 days of exposure, Cd concentrations in the liver and brain were significantly increased in Cd-exposed groups. Low-level Cd exposure (1 mg/L) increased weight and length gains, as well as food intake, in the fish. Acetylcholinesterase activity decreased significantly in the Cd-exposed groups. Energy metabolism levels (as reflected by oxygen consumption, ammonia excretion rate, and swimming activity), as well as serum T3 and T4 levels, increased significantly in the fish exposed to 1 mg/L Cd. However, energy metabolism and serum T3/T4 levels decreased significantly in the 4-mg/L Cd group. Neuropeptide gene expression levels in brain were consistent with the observed changes in food intake. In the Cd-exposed groups, the expression levels of neuropeptide Y (NPY), apelin, and metallothionein (MT) increased significantly, while those of pro-opinmelanocortin (POMC), ghrelin, and corticotrophin-releasing factor (CRF) decreased significantly. Our data suggested that in fish, low doses of Cd might increase food intake, as well as weight and length gains, but high doses of Cd might have the opposite effect. These effects might be a result of neurohumoral regulation. Long-term exposure to low doses of Cd might cause weight gain and affect food intake.

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References

  1. Abrantes N, Pereira R, Gonçalves F (2010) Occurrence of pesticides in water, sediments, and fish tissues in a lake surrounded by agricultural lands: concerning risks to humans and ecological receptors. Water Air Soil Pollut 212:77–88

  2. Barbieri E, Paes ET (2011) The use of oxygen consumption and ammonium excretion to evaluate the toxicity of cadmium on Farfantepenaeus paulensis with respect to salinity. Chemosphere 84:9–16

  3. Boeck GD et al (1995) The effect of sublethal levels of copper on oxygen consumption and ammonia excretion in the common carp, Cyprinus carpio. Aquat Toxicol 32:127–141

  4. Branka IO et al (2006) Combined effects of coenzyme Q and vitamin E in cadmium induced alterations of antioxidant defense system in the rat heart. Environ Toxicol Pharmacol 22:219–224

  5. Chen XM, Guo GL, Sun L, Yang QS, Wang GQ, Qin GX, Zhang DM (2016) Effects of Ala-Gln feeding strategies on growth, metabolism, and crowding stress resistance of juvenile Cyprinus carpio var. Jian. Fish Shellfish Immunol 51:365–372

  6. Chow ESH, Hui MNY, Lin CC, Cheng SH (2008) Cadmium inhibits neurogenesis in zebrafish embryonic brain development. Aquat Toxicol 87:157–169

  7. Cicik B et al (2004) Effects of lead and cadmium interactions on the metal accumulation in tissue and organs of the Nile tilapia (Oreochromis niloticus). Bull Environ Contam Toxicol 72:141

  8. Dray C, Knauf C, Daviaud D, Waget A, Boucher J, Buléon M, Cani PD, Attané C, Guigné C, Carpéné C, Burcelin R, Castan-Laurell I, Valet P (2008) Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab 8:437–445

  9. Fabrice B, Thierry R (2006) The melanocortin system during fasting. Peptides 27:291–300

  10. Favorito R, Chiarelli G, Grimaldi MC, de Bonis S, Lancieri M, Ferrandino I (2011) Bioaccumulation of cadmium and its cytotoxic effect on zebrafish brain. Chem Ecol 27:39–46

  11. Fox BK, Breves JP, Hirano T, Grau EG (2009) Effects of short- and long-term fasting on plasma and stomach ghrelin, and the growth hormone/insulin-like growth factor I axis in the tilapia, Oreochromis mossambicus. Domest Anim Endocrinol 37:1–11

  12. Gülüzar A et al (2015) Alterations in the serum biomarkers belonging to different metabolicsystems of fish (Oreochromis niloticus) after Cd and Pb exposures. Environ Toxicol Pharmacol 40:508–515

  13. Heydarnejad et al (2013) Effects of cadmium at sub-lethal concentration on growth and biochemical parameters in rainbow trout (Oncorhynchus mykiss). Ir Vet J 66:11–11

  14. Jie L et al (2011) Heavy metal contamination and risk assessment in water, paddy soil, and rice around an electroplating plant. Environ Sci Pollut Res Int 18:1623–1632

  15. Johnson KM, Lema SC (2011) Tissue-specific thyroid hormone regulation of gene transcripts encoding iodothyronine deiodinases and thyroid hormone receptors in striped parrotfish (Scarus iseri ). Gen Comp Endocrinol 172:505–517

  16. Jönsson E (2013) The role of ghrelin in energy balance regulation in fish. Gen Comp Endocrinol 187:79–85

  17. Kim JH, Kang JC (2017a) Effects of sub-chronic exposure to lead (Pb) and ascorbic acid in juvenile rockfish: antioxidant responses, MT gene expression, and neurotransmitters. Chemosphere. 171:520–527

  18. Kim JH, Kang JC (2017b) Toxic effects on bioaccumulation and hematological parameters of juvenile rockfish Sebastes schlegelii exposed to dietary lead (Pb) and ascorbic acid. Chemosphere 176:131–140

  19. Landrigan PJ, Boffetta P, Apostoli P (2000) The reproductive toxicity and carcinogenicity of lead: a critical review. Am J Ind Med 38:231–243

  20. Leal RB et al (2012) Cadmium neurotoxicity and its role in brain disorders. Springer, New York

  21. Marchant TA, Peter RE (1986) Seasonal variations in body growth rates and circulating levels of growth hormone in the goldfish, Carassius auratus. J Exp Zool A Ecol Genet Physiol 237:231–239

  22. Matsuda K, Kojima K, Shimakura SI, Wada K, Maruyama K, Uchiyama M, Kikuyama S, Shioda S (2008) Corticotropin-releasing hormone mediates alpha-melanocyte-stimulating hormone-induced anorexigenic action in goldfish. Peptides 29:1930–1936

  23. Modi HR, Katyare SS (2009) Cadmium exposure-induced alterations in the lipid/phospholipids composition of rat brain microsomes and mitochondria. Neurosci Lett 464:108–112

  24. Mohsen N et al (2012) Metal concentrations in tissues of two fish species from Qeshm Island, Iran. Bull Environ Contam Toxicol 89:1004–1008

  25. Olsson PE, Larsson Å, Haux C (1996) Influence of seasonal changes in water temperature on cadmium inducibility of hepatic and renal metallothionein in rainbow trout. Mar Environ Res 42:41–44

  26. Pino JD et al (2016) Cadmium-induced cell death of basal forebrain cholinergic neurons mediated by muscarinic M1 receptor blockade, increase in GSK-3β enzyme, β-amyloid and tau protein levels. Arch Toxicol 90:1081–1092

  27. Pradip KM et al (2019) Bioaccumulation and potential sources of heavy metal contamination in fish species in River Ganga basin: possible human health risks evaluation. Toxicol Rep 6:472–481

  28. 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

  29. Richetti SK, Rosemberg DB, Ventura-Lima J, Monserrat JM, Bogo MR, Bonan CD (2011) Acetylcholinesterase activity and antioxidant capacity of zebrafish brain is altered by heavy metal exposure. Neurotoxicology. 32:116–122

  30. Shaffi SA et al (2001) Influence of protective agents on metal induced respiratory distress in Labeo rohita (Ham). Bull Environ Contam Toxicol 66:611–616

  31. Signa G, Mazzola A, Tramati CD, Vizzini S (2017) Diet and habitat use influence Hg and Cd transfer to fish and consequent biomagnification in a highly contaminated area: Augusta Bay (Mediterranean Sea). Environ Pollut 230:394–404

  32. Straus DL, Chambers JE (1995) Inhibition of acetylcholinesterase and aliesterases of fingerling channel catfish by chlorpyrifos, parathion, and S , S , S -tributyl phosphorotrithioate (DEF). Aquat Toxicol 33:311–324

  33. Tang W, Shan B, Zhang H, Mao Z (2010) Heavy metal sources and associated risk in response to agricultural intensification in the estuarine sediments of Chaohu Lake Valley, East China. J Hazard Mater 176:945–951

  34. Tata JR (2011) Looking for the mechanism of action of thyroid hormone. J Thyroid Res 2011,730630:1–12

  35. Volkoff H, Peter RE (2001) Interactions between orexin A, NPY and galanin in the control of food intake of the goldfish, Carassius auratus. Regul Pept 101:59–72

  36. Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology. 192:95–117

  37. Wei M et al (2008) Heavy metal pollution in Tianjin Bohai Bay, China. J Environ Sci 20:814–819

  38. Witeska M et al (2006) Respiratory and hematological response of tench, Tinca tinca (L.) to a short-term cadmium exposure. Aquac Int 14:141–152

  39. Wu SM et al (1999) Cadmium-inducible metallothionein in tilapia (Oreochromis mossambicus). Bull Environ Contam Toxicol 62:758–768

  40. Yin Y et al (2018) Effect of sub-chronic exposure to lead (Pb) and Bacillus subtilis on Carassius auratus gibelio: bioaccumulation, antioxidant responses and immune responses

  41. Yun RJ et al (2017) Assessment of heavy metals in aquaculture fishes collected from southwest coast of Taiwan and human consumption risk. Int Biodeterior Biodegradation 124:314–325

  42. Zhang J, Sun P, Yang F, Kong T, Zhang R (2016a) Tributyltin disrupts feeding and energy metabolism in the goldfish (Carassius auratus ). Chemosphere. 152:221–228

  43. Zhang J, Zhang C, Sun P, Shao X (2016b) Tributyltin affects shoaling and anxiety behavior in female rare minnow (Gobiocypris rarus ). Aquat Toxicol 178:80–87

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Funding

The work was supported by the National Natural Sciences Foundational of China (No. 30972191), the 948 Program from Ministry of Agriculture of China (No. 2014Z34), and Jilin Agricultural University National College Students Innovation and Entrepreneurship Training Program (No. 201810193047).

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Correspondence to Yuehong Li.

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All experimental and animal-handling protocols were designed following the guidelines approved by the Institutional Animal Care and Use Committee, Jilin Agricultural University.

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Cai, Y., Yin, Y., Li, Y. et al. Cadmium exposure affects growth performance, energy metabolism, and neuropeptide expression in Carassius auratus gibelio. Fish Physiol Biochem 46, 187–197 (2020). https://doi.org/10.1007/s10695-019-00709-3

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Keywords

  • Cadmium
  • Thyroid hormone
  • Neuropeptide
  • Food intake