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Nano-copper Enhances Gene Regulation of Non-specific Immunity and Antioxidative Status of Fish Reared Under Multiple Stresses

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Abstract

Arsenic pollution, water temperature, and pH are the major concern for aquaculture. Moreover, the aim of the present investigation was to delineate the role of nano-copper (Cu-NPs) in the mitigation of arsenic toxicity, high temperature (34 °C) and low pH (6.5) stress on Pangasianodon hypophthalmus. Four isonitrogenous and isocaloric experimental diets of Cu-NPs at 0, 1.0, 1.5 and 2.0 mg kg−1 were formulated and prepared. Arsenic pollution, low pH and high temperature stress significantly reduced the anti-oxidative status (super oxide dismutase, catalase, glutathione peroxidase and glutathione-s-transferase), lipid peroxidation, total anti-oxidative capacity and lipid profiling (cholesterol, total lipid, phospholipid, very low-density lipoprotein and triglyceride). Further, the supplementation of Cu-NPs at 1.5 and 1.0 mg kg−1 diets noticeably improve the anti-oxidant status and capacity. The stressors groups (As + pH + T, As + T and As) significantly reduced fish immunity viz. albumin, globulin, total protein, albumin globulin ratio (A:G ratio), myeloperoxidase, respiratory burst activities, tumor necrosis factor, total immunoglobulin, and interleukin. Whereas supplementation of Cu-NPs at 1.5 and 1.0 mg kg−1 diets improved the immunity of the fish reared under multiple stresses (As + pH + T). Tail DNA %, DNA damage-inducible protein (DDIP) and inducible nitric oxide (iNOS) synthase gene expression were significantly enhanced with exposure to arsenic, low pH and high temperature but supplementation of Cu-NPs protects the tissues against DNA damage and improved the gene expression of iNOS and DDIP. Cu-NPs at 1.5 and 1.0 mg kg−1 diets significantly enhanced the body weight gain %, protein efficiency ratio, specific growth rate, daily growth index, relative feed intake and reduced the feed conversion ratio. Whereas, the growth-related gene expression such as myostatin (MYST), somatostatin (SMT) was downregulated by Cu supplementation and upregulated the gene expression of growth hormone regulator 1 and β (GHR1 and GHR β) and growth hormone (GH) gene in fish. Dietary Cu-NPs supplementation protects the fish against bacterial infection and enhances arsenic detoxification in different tissues. The present investigation revealed that supplementation of Cu-NPs at 1.5 and 1.0 mg kg−1 diet has the potential to mitigate multiple stress (As + pH + T) in fish.

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Availability of data and materials

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  1. Kumar N, Singh DK, Bhushan S, Jamwal A (2021) Mitigating multiple stresses in Pangasianodon hypophthalmus with a novel dietary mixture of selenium nanoparticles and Omega-3-fatty acid. Sci Rep 11:19429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Isaak DJ, Wollrab S, Horan D, Chandler G (2012) Climate change effects on stream and river temperatures across the northwest U. S. from 1980–2009 and implications for salmonid fishes. Clim Chang 113:499–524. https://doi.org/10.1007/s10584-011-0326-z

    Article  Google Scholar 

  3. Kumar N, Bhushan S, Patole P, Gite A (2022) Multi-biomarker approach to assess chromium, pH and temperature toxicity in fish. Comp Biochem Physiol C 254:109264

    CAS  Google Scholar 

  4. Kumar N (2021) Dietary riboflavin enhances immunity and anti-oxidative status against arsenic and high temperature in Pangasianodon hypophthalmus. Aquaculture 533:736209

    Article  CAS  Google Scholar 

  5. Kumar K, Gupta SK, Chandan NK, Bhushan S, Singh DK, Kumar P, Kumar P, Wakchaure GC, Singh NP (2020) Mitigation potential of selenium nanoparticles and riboflavin against arsenic and elevated temperature stress in Pangasianodon hypophthalmus. Sci Rep 10:17883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wang J, Zhao X (2009) On the potential of biological treatment for arsenic contaminated soils and groundwater. J Environ Manag 90:2367–2376

    Article  CAS  Google Scholar 

  7. Abdul KSM, Jayasinghe SS, Chandana EPS, Jayasumana C, De Silva PMCS (2015) Arsenic and human health effects: a review. Environ Toxicol Pharmacol 40(3):828–846

    Article  PubMed  Google Scholar 

  8. Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60–72

    Article  PubMed  PubMed Central  Google Scholar 

  9. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Exp Suppl 101:133–164

    PubMed  Google Scholar 

  10. Kumar N, Gupta SK, Bhushan S, Singh NP (2019) Impacts of acute toxicity of arsenic (III) alone and with high temperature on stress biomarkers, immunological status and cellular metabolism in fish. Aquat Toxicol 4(214):105233

    Article  Google Scholar 

  11. Lizama AK, Fletcher TD, Sun G (2011) Removal processes for arsenic in constructed wetlands. Chemosphere 84:1032–1043

    Article  Google Scholar 

  12. Majewski M, Ognik K, Juśkiewicz J (2019) Copper nanoparticles modify the blood plasma antioxidant status and modulate the vascular mechanisms with nitric oxide and prostanoids involved in Wistar rats. Pharmacol Rep 71(3):509–516

    Article  CAS  PubMed  Google Scholar 

  13. El Basuini MF, El-Hais AM, Dawood MA et al (2016) Effect of different levels of dietary copper nanoparticles and copper sulfate on growth performance, blood biochemical profiles, antioxidant status and immune response of red sea bream (Pagrus major). Aquaculture 455:32–40

    Article  Google Scholar 

  14. Mohseni M, Pourkazemi M, Baim SC (2014) Effects of dietary inorganic copper on growth performance and immune response of juvenile beluga, Huso huso. Aquacult Nutr 20:547–556

    Article  CAS  Google Scholar 

  15. Vivoli G, Bergomi M, Rovesti S, Pinotti M, Caselgrandi E (1995) Zinc, copper, and zinc- or copper-dependent enzymes in human hypertension. Biol Trace Elem Res 49(2–3):97–106

    Article  CAS  PubMed  Google Scholar 

  16. Majewski M, Kozlowska A, Thoene M, Lepiarczyk E, Grzegorzewski WJ (2016) Overview of the role of vitamins and minerals on the kynurenine pathway in health and disease. J Physiol Pharmacol 67(1):3–19

    CAS  PubMed  Google Scholar 

  17. Majewski M, Jurgonski A, Fotschki B, Juskiewicz J (2018) The toxic effects of monosodium glutamate (MSG) - the involvement of nitric oxide, prostanoids and potassium channels in the reactivity of thoracic arteries in MSG-obese rats. Toxicol Appl Pharmacol 359:62–69

    Article  CAS  PubMed  Google Scholar 

  18. Tan XY, Luo Z, Liu X, Xie CX (2011) Dietary copper (Cu) requirement for juvenile yellow catfish Pelteobagrus fulvidraco. Aquacult Nutr 17:170–176

    Article  CAS  Google Scholar 

  19. Feng M, Wang ZS, Zhou AG, Ai DW (2009) The effects of different sizes of nanometer zinc oxide on the proliferation and cell integrity of mice duodenum–epithelial cells in primary culture. Pak J Nutr 8:1164–1166

    Article  CAS  Google Scholar 

  20. Gatlin DM III, Wilson RP (1986) Dietary copper requirement of fingerling channel catfish. Aquaculture 54:277–285

    Article  CAS  Google Scholar 

  21. Huang S, Wang L, Liu L, Hou Y, Li L (2015) Nanotechnology in agriculture, livestock, and aquaculture in China, A review. Agron Sustain Dev 35(2):369–400

    Article  Google Scholar 

  22. Lall SP (2002) The minerals. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, New York, pp 260–308

    Google Scholar 

  23. Kumar N et al (2014) Lipotropes protect against pathogen-aggravated stress and mortality in low dose pesticide-exposed fish. PLoS ONE 9(4):93499

    Article  Google Scholar 

  24. Okado-Matsumoto A, Fridovich I (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 276:38388–38393

    Article  CAS  PubMed  Google Scholar 

  25. Uriu-Adams JY, Keen CL (2005) Copper, oxidative stress, and human health. Mol Aspects Med 26(2005):268–298

    Article  CAS  PubMed  Google Scholar 

  26. Lukasewycz OA, Prohaska JR (1990) The immune response in copper deficiency. Ann N Y Acad Sci 587:147–159

    Article  CAS  PubMed  Google Scholar 

  27. Koller LD, Mulhern SA, Frankel NC, Steven MG, Williams JR (1987) Immune dysfunction in rats fed a diet deficient in copper. Am J Clin Nutr 45:997–1006

    Article  CAS  PubMed  Google Scholar 

  28. Kumar N, Singh AK, Kumar S, Kumar T, Kochewad SA, Thorat ST, Patole PB, Gite A (2023) Nano-copper enhances thermal efficiency and stimulates gene expression in response to multiple stresses in Pangasianodon hypophthalmus (Striped catfish). Aquaculture 564:739059

    Article  CAS  Google Scholar 

  29. Kumar N, Kumar S, Singh AK, Gite A, Patole PB, Thorat ST (2022) Exploring mitigating role of zinc nanoparticles on arsenic, ammonia and temperature stress using molecular signature in fish. J Trace Elem Med Biol 74:127076

    Article  CAS  PubMed  Google Scholar 

  30. Kumar N, Krishnani KK, Kumar P, Singh NP (2017) Zinc nanoparticles potentiates thermal tolerance and cellular stress protection of Pangasius hypophthalmus reared under multiple stressors. J Therm Biol 70:61–68

    Article  CAS  PubMed  Google Scholar 

  31. Kumar N, Krishnani KK, Singh NP (2018) Comparative study of selenium and selenium nanoparticles with reference to acute toxicity, biochemical attributes, and histopathological response in fish. Environ Sci Pollut Res Int 25(9):8914–8927

    Article  CAS  PubMed  Google Scholar 

  32. APHA-AWWA-WEF (1998) In: Clesceri LS, Greenberg AE, Eaton AD (Eds) Standard methods for the estimation of water and waste water, twentieth ed., American Public Health Association, American Water Works Association, Water Environment Federation, Washington DC

  33. Halver JE (1976) The nutritional requirements of cultivated warm water and cold water fish species. In: Report of the FAO Technical Conference on Aquaculture, Kyoto, Japan, 26 May–2 June 1976, 9. FAO Fisheries Report No. 188 FI/ R188 (En)

  34. AOAC (1995) In: Cunnif, P.A. (Ed.), Official methods of analysis of the Association of Official Analytical Chemists, 16th ed.1. AOAC International, Arlington, pp. 31–65

  35. Lowry OH, Ronebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  PubMed  Google Scholar 

  36. Pfaf MW (2001) A new mathematical model for relative quantifcation in real-time RT-PCR. Nucl Acids Res 29(9):e45

    Article  Google Scholar 

  37. Takahara S, Hamilton BH, Nell JV, Kobra TY, Ogura Y, Nishimura ET (1960) Hypocatalesemia, a new generis Carrier state. J Clin Invest 29(1960):610–619

    Article  Google Scholar 

  38. Habing WH, Pabst MN, Bjacoby W, Glutathion S (1974) Glutathione S-transferases. Transferase, the first enzymatic step in mercatpopunc acid formation. J Biol Chem 249:7130–7139

    Google Scholar 

  39. Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169

    CAS  PubMed  Google Scholar 

  40. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    Article  CAS  PubMed  Google Scholar 

  41. Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278

    Article  CAS  PubMed  Google Scholar 

  42. Hestrin S (1949) The reaction of acetyl choline and other carboxylic acid derivatives with hydroxylamine and its analytical application. J Biol Chem 180:249–261

    Article  CAS  PubMed  Google Scholar 

  43. Roe JH, Keuther CA (1943) The determinations of ascorbic acid in whole blood and urine through the 2,4-dinitrophenylhydrazine (DNPH) derivative of dehydroascorbic acid. J Biol Chem 147:399–407

    Article  CAS  Google Scholar 

  44. Doumas BT, Watson W, Biggs HG (1971) Albumin standards and measurement of serum albumin with bromocresol green. Clin Chim Acta 31:87–96

    Article  CAS  PubMed  Google Scholar 

  45. Secombes CJ (1990) Isolation of Salmonid macrophage and analysis of their killing activity. In: Stolen JSTC, Fletcher DP, Anderson BS, Van Muiswinkel WB (eds) Techniques in fish immunology. SOS Publication, Fair Haven (NJ), pp 137–152

    Google Scholar 

  46. Stasiack AS, Bauman CP (1996) Neutrophil activity as a potent indicator concomitant analysis. Fish Shellfish Immunol 37:539

    Google Scholar 

  47. Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153:375–380

    Article  CAS  Google Scholar 

  48. Somoyogi M (1945) A new reagent for the determination of sugars. J Biol Chem 160:61–68

    Article  Google Scholar 

  49. Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58:239–248

    Article  CAS  PubMed  Google Scholar 

  50. Sahoo PK, Kumari J, Mishra BK (2005) Non-specific immune responses in juveniles of Indian major carps. J Appl Ichthyol 21:151–155

    Article  Google Scholar 

  51. Anderson DP, Siwicki AK (1995) Basic haematology and serology for fish health programmes. In: Shhariff JR, Subasinghe RP (eds) Diseases in Asian Aquaculture II, Fish Health Section. Asian Fisheries society, Manila, Philippines, pp 185–202

    Google Scholar 

  52. Arnao M, Cano A, Acosta M (1998) Total antioxidant activity in plant material and its interest in food technology. Recent Res Dev Agric Food Chem 2:893–905

    CAS  Google Scholar 

  53. Campos C et al (2009) Evaluation of the copper (II) reduction assay using bathocuproinedisulfonic acid disodium salt for the total antioxidant capacity assessment: The CUPRAC–BCS assay. Anal Biochem 392(1):37–44

    Article  CAS  PubMed  Google Scholar 

  54. Benzie IFF, Strain JJJ (1996) The Ferric Reducing Ability of Plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76

    Article  CAS  PubMed  Google Scholar 

  55. Ferreira M, Caetano M, Antunes P, Costa J, Gil O, Bandarra N, Pousao-Ferreira P, Carlos Vale C, Reis-Henriques MA (2010) Assessment of contaminants and biomarkers of exposure in wild and farmed seabass. Ecotoxicol Environ Saf 73:579–588

    Article  CAS  PubMed  Google Scholar 

  56. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  57. Bartlett GR (1959) Phosphorus assay in column chromatography. J Biol Chern 234:466–468

    Article  CAS  Google Scholar 

  58. Marinetti GV (1962) Chromatographic separation, identification and analysis of phosphatides. J Lipid Res 3:1–20

    Article  CAS  Google Scholar 

  59. Henly AA (1957) Determination of serum cholesterol. Analyst 82:286–287

    CAS  Google Scholar 

  60. Ali D, Nagpure NS, Kumar S, Kumar R, Kushwaha B (2008) Genotoxicity assessment of acute exposure of chlorpyrifos to freshwater fish Channa punctatus (Bloch) using micronucleus assay and alkaline single-cell gel electrophoresis. Chemosphere 71:1823–1831

    Article  CAS  PubMed  Google Scholar 

  61. Kumar N, Krishnani KK, Meena KK, Gupta SK, Singh NP (2017) Oxidative and cellular metabolic stress of Oreochromis mossambicus as biomarkers indicators of trace element contaminants. Chemosphere 171:265–274

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  63. Donaldson EM (1981) The pituitary-interrenal axis as indicator of stress in fish. In: Pickering AD (ed) Stress and fish. Academic Press, London, pp 11–47

    Google Scholar 

  64. Qian D, Xua C, Chena C, Qind JG, Chenc L, Lia E (2020) Toxic effect of chronic waterborne copper exposure on growth, immunity, anti-oxidative capacity and gut microbiota of Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 100:445–455

    Article  CAS  PubMed  Google Scholar 

  65. Kumar N, Krishnani KK, Gupta SK, Singh NP (2018) Effects of silver nanoparticles on stress biomarkers of Channa striatus: immuno-protective or toxic? Environ Sci Pollut Res 25(15):14813–14826

    Article  CAS  Google Scholar 

  66. Kumar N, Krishnani KK, Gupta SK, Singh NP (2017) Selenium nanoparticles enhanced thermal tolerance and maintain cellular stress protection of Pangasius hypophthalmus reared under lead and high temperature. Respir Physiol Neurobiol 246:107–116

    Article  CAS  PubMed  Google Scholar 

  67. Huesca M, Goodwin A, Bhagwansingh A, Hoffman P, Lingwood CA (1998) Characterization of an acidic-pH-inducible stress protein (hsp70), a putative sulfatide binding adhesin, from Helicobacter pylori. Infect Immunol 66:4061–4067

    Article  CAS  Google Scholar 

  68. Richter-Landsberg C, Bauer NG (2004) Tau-inclusion body formation in oligodendroglia: the role of stress proteins and proteasome inhibition. Int J Dev Neurosci 22(7):443–451

    Article  CAS  PubMed  Google Scholar 

  69. Prohaska JR, Bailey WR, Gross AM, Korte JJ (1990) Effect of dietary copper deficiency on the distribution of dopamine and norepinephrine in mice and rats. J Nutr Biochem 1:149–154

    Article  CAS  PubMed  Google Scholar 

  70. Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97(6):1634–1658

    Article  CAS  PubMed  Google Scholar 

  71. Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  CAS  PubMed  Google Scholar 

  72. Wang W, Zhou J, Wang P, Tian T, Zheng Y, Liu Y, Mai W, Wang A (2009) Oxidative stress, DNA damage and antioxidant enzyme gene expression in the Pacific white shrimp, Litopenaeus vannamei when exposed to acute pH stress. Comp Biochem Physiol C 150(2009):428–435

    Google Scholar 

  73. Zhou J, Wang WN, Ma GZ, Wang AL, He WY, Wang P, Liu Y, Liu JJ, Sun RY (2008) Gene expression of ferritin in tissues of the Pacific white shrimp, Litopenaeus vannamei after exposure to pH stress. Aquaculture 275:356–360

    Article  CAS  Google Scholar 

  74. Uriu-Adams J (2005) Keen C., Copper, oxidative stress, and human health. Mol Aspects Med 26:268–298

    Article  CAS  PubMed  Google Scholar 

  75. Strain J, Lorenz CR, Bode J, Garland S, Smolen GA, Ta DT, Vickery LE, Culotta VC (1998) Suppressors of superoxide dismutase (SOD1) deficiency in Saccharomyces cerevisiae. Identification of proteins predicted to mediate iron-sulfur cluster assembly. J Biol Chem 273(47):31138–44

    Article  CAS  PubMed  Google Scholar 

  76. Minganti V, Drava G, De Pellegrini R, Siccardi C (2010) Trace elements in farmed and wild gilthead seabream, Sparus aurata. Mar Pollut Bull 60(11):2022–2025

    Article  CAS  PubMed  Google Scholar 

  77. Wang C, Lovell RT (1997) Organic seleniumsources, selenomethionine and selenoyeast, have higher bioavailability than an inorganic selenium source, sodium selenite, in diets for channel catfish (Ictalurus punctatus). Aquaculture 152:223–234

    Article  CAS  Google Scholar 

  78. Coeurdacier JL, Dutto G, Gasset E, Blancheton JP (2011) Is total serum protein a good indicator for welfare in reared sea bass (Dicentrarchus labrax)? Aquat Living Resour 24:121–127

    Article  Google Scholar 

  79. Kumar N et al (2017) Dietary zinc promotes immuno-biochemical plasticity and protects fish against multiple stresses. Fish Shellf Immunol 17(62):184–194

    Article  Google Scholar 

  80. Sharp GJE, Secombes CJ (1993) The role of reactive oxygen species in the killing of the bacterial fish pathogen Aeromonas salmonicida by rainbow trout macrophages. Fish Shellf Immunol 3(2):119–129

    Article  Google Scholar 

  81. Beutler B (2004) Innate immunity: an overview. Mol Immunol 40:845–859

    Article  CAS  PubMed  Google Scholar 

  82. Bonham M, O’Connor JM, Hannigan BM, Strain JJ (2002) The immune system as a physiological indicator of marginal copper status? Br J Nutr 87(5):393–403

    Article  CAS  PubMed  Google Scholar 

  83. Varfolomeev EE, Ashkenazi A (2004) Tumor necrosis factor. Cell 116:491–497

    Article  CAS  PubMed  Google Scholar 

  84. Djurhuus CB et al (2002) Effects of cortisol on lipolysis and regional interstitial glycerol levels in humans. Environ Sci 283(1):E172–E177

    CAS  Google Scholar 

  85. Mroczek-Sosnowska N, Batorska M, Lukasiewicz M, Wnuk A, Sawosz E, Jaworski S, Niemiec J (2013) Effect of nanoparticles of copper and copper sulfate administered in ovo on hematological and biochemical blood markers of broiler chickens. Annals of Warsaw University of Life Sciences-SGGW. Anim Sci 52:141–149

    CAS  Google Scholar 

  86. Bakalli RI, Pesti GM, Ragland WL, Konjufca V (1995) Dietary copper in excess of nutritional requirement reduces plasma and breast muscle cholesterol in chickens. Poult Sci 74:360–365

    Article  CAS  PubMed  Google Scholar 

  87. Kim S, Chao PY, Allen KGD (1992) Inhibition of elevated hepatic glutathione abolishes copper deficiency cholesterolemia. FASEB J 6:2467–2471

    Article  CAS  PubMed  Google Scholar 

  88. Vural H, Demirin H, Kara Y, Eren I, Delibas N (2010) Alterations of plasma magnesium, copper, zinc, iron and selenium concentrations and some related erythrocyte antioxidant enzyme activities in patients with Alzheimer’s disease. J Trace Elem Med Biol 24:169–173

    Article  CAS  PubMed  Google Scholar 

  89. Exley C, House E, Polwart A, Esiri MM (2012) Brain burdens of aluminum, iron, and copper and their relationships with amyloid-β pathology in 60 human brains. J Alzheimers Dis 31:725–730

    Article  CAS  PubMed  Google Scholar 

  90. Squitti R, Siotto M, Cassetta E, Ghafir EI, Idrissi I, Colabufo NA (2017) Measurements of serum non-ceruloplasmin copper by a direct fluorescent method specific for Cu (II). Clin Chem Lab Med 55:1360–1367

    Article  CAS  PubMed  Google Scholar 

  91. Nam E, Nam G, Lim MH (2020) Synaptic copper, amyloid-β, and neurotransmitters in Alzheimer’s disease. Biochemistry 59:15–17

    Article  CAS  PubMed  Google Scholar 

  92. Webster RP, Gawde MD, Bhayfacharya RIC (1996) Modulation by dietary copper of aflatoxin B1 activity of DNA repair enzymes poly(ADP-ribose) polymerase, DNA polymerase B and DNA ligase. In Vivo 10:533–536

    CAS  PubMed  Google Scholar 

  93. Damasceno FM, Fleuri LF, Sartori MMP, Amorim RL, Pezzato LE, da Silva RL, Das PC, Ayyappan S, Jena J (2006) Haematological changes in the three Indian major carps, Catla catla (Hamilton), Labeo rohita (Hamilton) and Cirrhinus mrigala (Hamilton) exposed to acidic and alkaline water pH. Aquaculture 235(1–4):633–644

    Google Scholar 

  94. Sabatini SE, Juarez AB, Eppis MR, Bianchi L, Luquet CM, Rios de Molinaa MC (2009) Oxidative stress and antioxidant defences in two green microalgae exposed to copper. Ecotoxicol Environ Saf 72:1200–1206

    Article  CAS  PubMed  Google Scholar 

  95. Klein SE, Sheridan MA (2008) Somatostatin signaling and the regulation of growth and metabolism in fish. Mol Cell Endocrinol 286:148–154

    Article  CAS  PubMed  Google Scholar 

  96. Deane EE, Woo NYS (2009) Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fish 19:97–120

    Article  Google Scholar 

  97. Pickering AD (1993) Growth and stress in fish production. Aquaculture 111:51–63

    Article  Google Scholar 

  98. Barton BA, Iwama GK (1991) Physiological change in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann Rev Fish Dis 1:3–26

    Article  Google Scholar 

  99. Nakano T, Afonso LOB, Beckman BR, Iwama GK, Devlin RH (2013) Acute physiological stress down-regulates mRNA expressions of growth-related genes in Coho Salmon. PLoS ONE 8(8):e71421

    Article  PubMed  PubMed Central  Google Scholar 

  100. Bass J, Oldham J, Sharma M, Kambadur R (1999) Growth factors controlling muscle development. Domest Anim Endocrinol 17:191–197

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The present research was supported by Science and Engineering Research Board, New Delhi, India. as an external project (OXX5467). Authors also thankful to the Director, ICAR-National Institute of Abiotic Stress Management, Baramati, Pune for providing all the facilities for this study.

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External project (OXX5467): Science and Engineering Research Board, New Delhi, India.

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  1. ICAR-National Institute of Abiotic Stress Management, Malegaon, Baramati, Pune, 413115, India

    Neeraj Kumar, Supriya Tukaram Thorat, Archana Gite & Pooja Bapurao Patole

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  1. Neeraj Kumar
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Contributions

Neeraj Kumar, Conceived and designed the experiments; performed the experiments; analysed the data; contributed reagents/materials/analysis tools; wrote the paper. Supriya Tukaram Thorat, Support in sampling and molecular analysis. Archana Gite, Support in sampling and perform analysis. Pooja Bapurao Patole, Analysis and data validation.

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Correspondence to Neeraj Kumar.

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The study protocol and the end-points of the experiments were approved by the Research Advisory Committee of ICAR-NIASM. All the methods were carried out in accordance with relevant national and international guidelines and regulations and strictly followed the animal research (ARRIVE) guidelines.

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Kumar, N., Thorat, S.T., Gite, A. et al. Nano-copper Enhances Gene Regulation of Non-specific Immunity and Antioxidative Status of Fish Reared Under Multiple Stresses. Biol Trace Elem Res 201, 4926–4950 (2023). https://doi.org/10.1007/s12011-023-03575-6

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