Abstract
Aldehyde reductase (AKR1A1) is a carbonyl detoxification protein in toxic aldehyde removal. In the present study, the full-length cDNA of yellow catfish AKR1A1 (TfAKR1A1) was cloned. As expected, yellow catfish AKR1A1 showed similarities with that of other species. Subsequently, prokaryotic expression vector was constructed and recombinant TfAKR1A1 (rTfAKR1A1) was successfully induced and purified. rTfAKR1A1 exhibited reductive activity to many aldehydes and ketones. To determine whether TfAKR1A1 could confer stress tolerance in vitro, the viability of control and TfAKR1A1 expression E. coli under abiotic stress was compared by spot assay. Results showed that the recombinant strain had better stress resistance under cadmium, hydrogen peroxide, and DL-glyceraldehyde stress. Then, effects of an intraperitoneal injection of rTfAKR1A1 protein on cadmium-induced oxidative stress were evaluated. Results displayed that TfAKR1A1 and Nrf2 expression levels were significantly decreased, CAT and SOD expression levels were significantly increased, BCL-2 and IL-10 expression levels were significantly increased, and caspase3a, NF-κB, and IL-1β expression levels were significantly decreased in protein-injection group. Furthermore, oxidative stress indexes in livers under different protein injection doses were examined by ELISA. Results showed that CAT, SOD, and GSH-Px activities were upregulated, ROS and T-AOC contents were also improved, while MDA content was significantly decreased both in lower and middle dose injection groups. Finally, liver pathological section analysis was performed. Results displayed that liver injury degree in protein-injected groups was lower than that of PBS group under cadmium stress. These results suggested that TfAKR1A1 played important roles in response to cadmium stress in yellow catfish.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Ahmed MK, Parvin E, Islam MM, Akter MS, Khan S, Al-Mamun MH (2014) Lead- and cadmium-induced histopathological changes in gill, kidney and liver tissue of freshwater climbing perch Anabas testudineus (Bloch, 1792). Chem Ecol 30(6):532–540. https://doi.org/10.1080/02757540.2014.889123
Aon MA, Cortassa S, O’rourke B (2010) Redox-optimized ROS balance: a unifying hypothesis. Biochim Biophys Acta Bioenerg 1797(6–7):865–877. https://doi.org/10.1016/j.bbabio.2010.02.016
Ax W, Soldan M, Koch L, Maser E (2000) Development of daunorubicin resistance in tumour cells by induction of carbonyl reduction. Biochem Pharmacol 59(3):293–300. https://doi.org/10.1016/S0006-2952(99)00322-6
Barrera G, Pizzimenti S, Ciamporcero ES, Daga M, Ullio C, Arcaro A, Gentile F (2015) Role of 4-hydroxynonenal-protein adducts in human diseases. Antioxid Redox Signal 22(18):1681–1702. https://doi.org/10.1089/ars.2014.6166
Barski OA, Papusha VZ, Ivanova MM, Rudman DM, Finegold MJ (2005) Developmental expression and function of aldehyde reductase in proximal tubules of the kidney. Am J Physiol Ren Physiol 289(1):200–207. https://doi.org/10.1152/ajprenal.00411.2004
Chatterjee S, Kundu S, Bhattacharyya A (2008) Mechanism of cadmium induced apoptosis in the immunocyte. Toxicol Lett 177(2):83–89. https://doi.org/10.1016/j.toxlet.2007.12.010
Chen J, Xu Y, Han Q, Yao Y, Xing H, Teng X (2019) Immunosuppression, oxidative stress, and glycometabolism disorder caused by cadmium in common carp (Cyprinus carpio L.): application of transcriptome analysis in risk assessment of environmental contaminant cadmium. J Hazard Mater 366:386–394. https://doi.org/10.1016/j.jhazmat.2018.12.014
Cortassa S, O’Rourke B (1837) Aon MA (2014) Redox-optimized ROS balance and the relationship between mitochondrial respiration and ROS. Biochim Biophys Acta Bioenerg 2:287–295. https://doi.org/10.1016/j.bbabio.2013.11.007
Creagh EM, Conroy H, Martin SJ (2003) Caspase-activation pathways in apoptosis and immunity. Immunol Rev 193(1):10–21. https://doi.org/10.1034/j.1600-065X.2003.00048.x
Dai Z, Cheng J, Bao L, Zhu X, Li H, Chen X, Huang H (2020) Exposure to waterborne cadmium induce oxidative stress, autophagy and mitochondrial dysfunction in the liver of Procypris merus. Ecotoxicol Environ Saf 204:111051. https://doi.org/10.1016/j.ecoenv.2020.111051
Ewa DK, Dorota PG, Katarzyna G, Magdalena S, Grzegorz G, Ewa Ł, Bogdan S, Włodzimierz P (2019). Cadmium-induced oxidative stress in Prussian carp (Carassius gibelio Bloch) hepatopancreas: ameliorating effect of melatonin. Environ Sci Pollut Res. 26: 12264–12279.https://doi.org/10.1007/s11356-019-04595-3
Fujii J, Hamaoka R, Matsumoto A, Fujii T, Yamaguchi Y, Egashira M, Taniguchi N (1999) The structural organization of the human aldehyde reductase gene, AKR1A1, and mapping to chromosome 1p33→p32. Cytogenet Genome Res 84(3–4):230–232. https://doi.org/10.1159/000015265
Gajewska J, Azzahra NA, Bingöl ÖA, Izbiańska-Jankowska K, Jelonek T, Deckert J, Arasimowicz-Jelonek M (2020) Cadmium stress reprograms ROS/RNS homeostasis in Phytophthora infestans (Mont.) de Bary. Int J Mol Sci 21(21):8375. https://doi.org/10.3390/ijms21218375
Ge J, Guo K, Zhang C, Talukder M, Lv MW, Li JY, Li JL (2021) Comparison of nanoparticle-selenium, selenium-enriched yeast and sodium selenite on the alleviation of cadmium-induced inflammation via NF-kB/IκB pathway in heart. Sci Total Environ 773:145442. https://doi.org/10.1016/j.scitotenv.2021.145442
Genchi G, Sinicropi MS, Lauria G, Carocci A, Catalano A (2020) The effects of cadmium toxicity. Int J Environ Res Public Health 17(11):3782. https://doi.org/10.3390/ijerph17113782
Guardiola FA, Cuesta A, Meseguer J, Martínez S, Martínez-Sánchez MJ, Pérez-Sirvent C, Esteban MA (2013) Accumulation, histopathology and immunotoxicological effects of waterborne cadmium on gilthead seabream (Sparus aurata). Fish Shellfish Immunol 35(3):792–800. https://doi.org/10.1016/j.fsi.2013.06.011
Hassanin A, Kaminishi Y, Itakura T (2017) Characterization of Tilapia (Oreochromis niloticus) aldehyde reductase (AKR1A1) gene, promoter and expression pattern in benzo-a-pyrene exposed fish. Toxicol Mech Methods 27(1):36–44. https://doi.org/10.1080/15376516.2016.1238529
Hegedüs A, Erdei S, Janda T, Tóth E, Horváth G, Dudits D (2004) Transgenic tobacco plants overproducing alfalfa aldose/aldehyde reductase show higher tolerance to low temperature and cadmium stress. Plant Sci 166(5):1329–1333. https://doi.org/10.1016/j.plantsci.2004.01.013
Huang CX, Lv B, Wang Y (2015) Protein phosphatase 2A mediates oxidative stress induced apoptosis in osteoblasts. Mediators Inflamm 2015:1–8. https://doi.org/10.1155/2015/804260
Jia B, St-Hilaire S, Singh K, Gardner IA (2017) Biosecurity knowledge, attitudes and practices of farmers culturing yellow catfish (Pelteobagrus fulvidraco) in Guangdong and Zhejiang provinces, China. Aquaculture 471:146–156. https://doi.org/10.1016/j.aquaculture.2017.01.016
Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283(2–3):65–87. https://doi.org/10.1016/j.tox.2011.03.001
Jung KA, Choi BH, Nam CW, Song M, Kim ST, Lee JY, Kwak MK (2013) Identification of aldo-keto reductases as NRF2-target marker genes in human cells. Toxicol Lett 218(1):39–49. https://doi.org/10.1016/j.toxlet.2012.12.026
Kan CA, Meijer GAL (2007) The risk of contamination of food with toxic substances present in animal feed. Anim Feed Sci Technol 133(1–2):84–108. https://doi.org/10.1016/j.anifeedsci.2006.08.005
Kassner N, Huse K, Martin HJ, Gödtel-Armbrust U, Metzger A, Meineke I, Wojnowski L (2008) Carbonyl reductase 1 is a predominant doxorubicin reductase in the human liver. Drug Metab Dispos 36(10):2113–2120. https://doi.org/10.1124/dmd.108.022251
Kensler TW, Wakabayashi N, Biswal S (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47:89–116. https://doi.org/10.1146/annurev.pharmtox.46.120604.141046
Kim MS, Kim BJ, Woo HN, Kim KW, Kim KB, Kim IK, Jung YK (2000) Cadmium induces caspase-mediated cell death: suppression by Bcl-2. Toxicology 145(1):27–37. https://doi.org/10.1016/S0300-483X(99)00176-6
Kondoh M, Araragi S, Sato K, Higashimoto M, Takiguchi M, Sato M (2002) Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170(1–2):111–117. https://doi.org/10.1016/S0300-483X(01)00536-4
Lai CW, Chen HL, Tu MY, Lin WY, Röhrig T, Yang SH, Chen CM (2017) A novel osteoporosis model with ascorbic acid deficiency in Akr1A1 gene knockout mice. Oncotarget 8(5):7357. https://doi.org/10.18632/oncotarget.14458
Li X, Li J, Wang Y, Fu L, Fu Y, Li B, Jiao B (2011) Aquaculture industry in China: current state, challenges, and outlook. Rev Fish Sci 19(3):187–200. https://doi.org/10.1080/10641262.2011.573597
Li W, Wang Q, Li S, Jiang A, Sun WX (2017) Molecular cloning, genomic structure, polymorphism analysis and recombinant expression of a α1-antitrypsin like gene from swamp eel, Monopterus albus. Fish Shellfish Immunol 62:124–138. https://doi.org/10.1016/j.fsi.2017.01.021
Li D, Gu Z, Zhang J, Ma S (2019) Protective effect of inducible aldo-keto reductases on 4-hydroxynonenal-induced hepatotoxicity. Chem Biol Interact 304:124–130. https://doi.org/10.1016/j.cbi.2019.02.012
Li X, Schmöhl F, Qi H, Bennewitz K, Tabler CT, Poschet G, Kroll J (2020) Regulation of gluconeogenesis by aldo-keto-reductase 1a1b in Zebrafish. Iscience 23(12):101763. https://doi.org/10.1016/j.isci.2020.10176
Li Y, Wu YC, Zhang JY, Peng J, Liao HL, Zhang YF (2009) A P2P based distributed services network for next generation mobile internet communications. In: Proceedings of the 18th international conference on World wide web 2009: 1177–1178. https://doi.org/10.1145/1526709.1526916
Loboda A, Damulewicz M, Pyza E, Jozkowicz A, Dulak J (2016) Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell Mol Life Sci 73(17):3221–3247. https://doi.org/10.1007/s00018-016-2223-0
MacLeod AK, Acosta-Jimenez L, Coates PJ, McMahon M, Carey FA, Honda T, Wolf CR (2016) Aldo-keto reductases are biomarkers of NRF2 activity and are coordinately overexpressed in non-small cell lung cancer. Br J Cancer 115(12):1530–1539. https://doi.org/10.1038/bjc.2016.363
Matsunaga T, Haga M, Watanabe G, Shinoda Y, Endo S, Kajiwara Y, Hara A (2012) 9, 10-Phenanthrenequinone promotes secretion of pulmonary aldo-keto reductases with surfactant. Cell Tissue Res 347(2):407–417. https://doi.org/10.1007/s00441-011-1304-5
Mitsuishi Y, Motohashi H, Yamamoto M (2012) The Keap1–Nrf2 system in cancers: stress response and anabolic metabolism. Front Oncol 2:200. https://doi.org/10.3389/fonc.2012.00200
Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB (2014) Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 20(7):1126–1167. https://doi.org/10.1089/ars.2012.5149
Mittler R (2017) ROS are good. Trends Plant Sci 22(1):11–19. https://doi.org/10.1016/j.tplants.2016.08.002
O’Connor T, Ireland LS, Harrison DJ, Hayes JD (1999) Major differences exist in the function and tissue-specific expression of human aflatoxin B1 aldehyde reductase and the principal human aldo-keto reductase AKR1 family members. Biochem J 343(2):487–504. https://doi.org/10.1042/bj3430487
Osorio-Yáñez C, García-Tavera JL, Pérez-Núñez MT, Poblete-Naredo I, Muñoz B, Barron-Vivanco BS, Albores A (2012) Benzo[a]pyrene induces hepatic AKR1A1 mRNA expression in tilapia fish (Oreochromis niloticus). Toxicol Mech Methods 22(6):438–444. https://doi.org/10.3109/15376516.2012.666684
Pan YX, Luo Z, Zhuo MQ, Wei CC, Chen GH, Song YF (2018) Oxidative stress and mitochondrial dysfunction mediated Cd-induced hepatic lipid accumulation in zebrafish Danio rerio. Aquat Toxicol 199:12–20. https://doi.org/10.1016/j.aquatox.2018.03.017
Pavlaki MD, Araújo MJ, Cardoso DN, Silva ARR, Cruz A, Mendo S, Loureiro S (2016) Ecotoxicity and genotoxicity of cadmium in different marine trophic levels. Environ Pollut 215:203–212. https://doi.org/10.1016/j.envpol.2016.05.010
Rochette L, Zeller M, Cottin Y, Vergely C (2018) Redox functions of heme oxygenase-1 and biliverdin reductase in diabetes. Trends Endocrinol Metab 29(2):74–85. https://doi.org/10.1016/j.tem.2017.11.005
Ruangsomboon S, Wongrat L (2006) Bioaccumulation of cadmium in an experimental aquatic food chain involving phytoplankton (Chlorella vulgaris), zooplankton (Moina macrocopa), and the predatory catfish Clarias macrocephalus × C. gariepinus. Aquat Toxicol 78(1):15–20. https://doi.org/10.1016/j.aquatox.2006.01.015
Shi H, Sui Y, Wang X, Luo Y, Ji L (2005) Hydroxyl radical production and oxidative damage induced by cadmium and naphthalene in liver of Carassius auratus. Comp Biochem Physiol C Toxicol Pharmacol 140(1):115–121. https://doi.org/10.1016/j.cca.2005.01.009
Stomberski CT, Anand P, Venetos NM, Hausladen A, Zhou HL, Premont RT, Stamler JS (2019) AKR1A1 is a novel mammalian S-nitroso-glutathione reductase. J Biol Chem 294(48):18285–18293. https://doi.org/10.1074/jbc.RA119.011067
Sun Y, Li Y, An J, Liu Z, Chen Q (2019) Antioxidative and inflammatory responses in spleen and head kidney of yellow catfish (Pelteobagrus fulvidraco) induced by waterborne cadmium exposure. Turk J Fish Aquat Sci 20(2):87–96. https://doi.org/10.4194/1303-2712-v20_02_01
Sun JX, Wang SC, Cao YR, Wang ST, Li S (2020) Cadmium exposure induces apoptosis, inflammation and immunosuppression through CYPs activation and antioxidant dysfunction in common carp neutrophils. Fish Shellfish Immunol 99:284–290. https://doi.org/10.1016/j.fsi.2020.02.015
Taguchi K, Motohashi H, Yamamoto M (2011) Molecular mechanisms of the Keap1–Nrf2 pathway in stress response and cancer evolution. Genes Cells 16(2):123–140. https://doi.org/10.1111/j.1365-2443.2010.01473.x
Thophon S, Kruatrachue M, Upatham ES, Pokethitiyook P, Sahaphong S, Jaritkhuan S (2003) Histopathological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environ Pollut 121(3):307–320. https://doi.org/10.1016/S0269-7491(02)00270-1
Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12(10):1161–1208. https://doi.org/10.2174/0929867053764635
Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192(2–3):95–117. https://doi.org/10.1016/S0300-483X(03)00305-6
Wang D, Malo D, Hekimi S (2010) Elevated mitochondrial reactive oxygen species generation affects the immune response via hypoxia-inducible factor-1α in long-lived Mclk1+/− mouse mutants. J Immunol 184(2):582–590. https://doi.org/10.4049/jimmunol.0902352
Wang HY, Xiao DF, Zhou C, Wang LL, Wu L, Lu YT, Ma MG (2017) YLL056C from Saccharomyces cerevisiae encodes a novel protein with aldehyde reductase activity. Appl Microbiol Biotechnol 101(11):4507–4520. https://doi.org/10.1007/s00253-017-8209-5
Wei K, Yang J, Song C (2020) The responses of prophenoloxidase and MAPK/Nrf2 pathway to cadmium stress in red swamp crayfish Procambarus clarkii. Mar Freshw Behav Physiol 53(2):59–72. https://doi.org/10.1080/10236244.2020.1764189
West AP, Shadel GS, Ghosh S (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11(6):389–402. https://doi.org/10.1038/nri2975
Wu YH, Li ZH, Zhong LQ, Chen DQ (2016) Tissue-specific stress and hepatic DNA damage in Pelteobagrus fulvidraco caused by low concentrations of cadmium. Toxicol Environ Chem 98(1):90–100. https://doi.org/10.1080/02772248.2015.1105227
Wu SM, Shu LH, Liu JH, Chen CH (2017) Anti-oxidative responses on hepatic tissue of zebrafish (Danio rerio) in a short duration of sub-lethal concentrations of cadmium exposure. Bull Environ Contam Toxicol 98(5):612–618. https://doi.org/10.1007/s00128-017-2063-0
Xie D, Li Y, Liu Z, Chen Q (2019) Inhibitory effect of cadmium exposure on digestive activity, antioxidant capacity and immune defense in the intestine of yellow catfish (Pelteobagrus fulvidraco). Comp Biochem Physiol C Toxicol Pharmacol 222:65–73. https://doi.org/10.1016/j.cbpc.2019.04.012
Younis EM, Abdel-Warith AA, Al-Asgah NA, Ebaid H, Mubarak M (2013) Histological changes in the liver and intestine of Nile tilapia, Oreochromis niloticus, exposed to sublethal concentrations of cadmium. Pak J Zool 45(3):833–841. https://doi.org/10.1080/11250003.2013.783631
Yuan SS, Lv ZM, Zhu AY, Zheng JL, Wu CW (2017) Negative effect of chronic cadmium exposure on growth, histology, ultrastructure, antioxidant and innate immune responses in the liver of zebrafish: preventive role of blue light emitting diodes. Ecotoxicol Environ Saf 139:18–26. https://doi.org/10.1016/j.ecoenv.2017.01.021
Zang YW, Zheng ST, Tang F, Yang L, Wei XP, Kong D, Sun WX, Li W (2020) Heme oxygenase 1 plays a crucial role in swamp eel response to oxidative stress induced by cadmium exposure or Aeromonas hydrophila infection. Fish Physiol Biochem 46(6):1947–1963. https://doi.org/10.1007/s10695-020-00846-0
Zhang Z, Zheng Z, Cai J, Liu Q, Yang J, Gong Y, Xu S (2017) Effect of cadmium on oxidative stress and immune function of common carp (Cyprinus carpio L.) by transcriptome analysis. Aquat Toxicol 192:171–177. https://doi.org/10.1016/j.aquatox.2017.09.022
Zhang J, Zheng S, Wang S, Liu Q, Xu S (2020) Cadmium-induced oxidative stress promotes apoptosis and necrosis through the regulation of the miR-216a-PI3K/AKT axis in common carp lymphocytes and antagonized by selenium. Chemosphere 258:127341. https://doi.org/10.1016/j.chemosphere.2020.127341
Zheng JL, Yuan SS, Wu CW, Lv ZM (2016) Acute exposure to waterborne cadmium induced oxidative stress and immunotoxicity in the brain, ovary and liver of zebrafish (Danio rerio). Aquat Toxicol 180:36–44. https://doi.org/10.1016/j.aquatox.2016.09.012
Zhu QL, Guo SN, Yuan SS, Lv ZM, Zheng JL, Xia H (2017) Heat indicators of oxidative stress, inflammation and metal transport show dependence of cadmium pollution history in the liver of female zebrafish. Aquat Toxicol 191:1–9. https://doi.org/10.1016/j.aquatox.2017.07.010
Ziltener P, Reinheckel T, Oxenius A (2016) Neutrophil and alveolar macrophage-mediated innate immune control of Legionella pneumophila lung infection via TNF and ROS. PLoS Pathog 12(4):e1005591. https://doi.org/10.1371/journal.ppat.1005591
Funding
This study was supported in part by grants the Yangtze Youth Talent Fund (2015cqr18) and Open Fund of Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education, Yangtze University (KF2015016).
Author information
Authors and Affiliations
Contributions
WL conceived and designed the experiments. LY performed the experiments and wrote the paper. SZ, DK, SX, JW, and NW performed part of experiments. WS analyzed and interpreted the data.
Corresponding author
Ethics declarations
Ethics declarations
All procedures are carried out in accordance with the Laboratory Animal Care and Use Guidelines and approved by the Yangtze University Institutional Animal Care and Use Committee.
Consent for publication
All authors agree the contents of the final manuscript and approved the publication.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yang, L., Zheng, S., Kong, D. et al. Characterization, expression, and function analysis of AKR1A1 gene from yellow catfish (Tachysurus fulvidraco). Fish Physiol Biochem 48, 285–302 (2022). https://doi.org/10.1007/s10695-022-01048-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-022-01048-6