Abstract
The study of the diversity of metabolic pathways is an important aspect for understanding the evolutionary relationships between metabolic pathways and their biochemical precursors. Recently, researchers described a sulfolactate dehydrogenase-like protein encoded in eukaryotes by the AqE gene, which remains highly conserved in teleosts. However, the metabolic role of this enzyme is still unknown. In the present work, we studied the transcriptional activity of the AqE gene, as well as other genes associated with energy exchange in the large yellow croaker Larimichthys crocea. The quantitative analysis of expression showed the tissue specificity of the AqE gene activity in the yellow croaker. The gene is active in the liver, skin, and gills. The analysis of gene expression in various organs and under the influence of stressful conditions suggests that the enzyme encoded by the AqE gene is involved in the malate-aspartate shuttle or in the excretion of the final metabolites (sulfolactate) from the organism.
Similar content being viewed by others
REFERENCES
Hochachka, P.W. and Somero, G.N., Biochemical Adaptation: Mechanisms and Process of Physiological Evolution, New York: Oxford University Press, 2002.
Madern, D., Molecular evolution within the L-malate and L-lactate dehydrogenase super-family, J. Mol. Evol., 2002, vol. 54, no. 6, pp. 825—840. https://doi.org/10.1007/s00239-001-0088-8
Honka, E., Fabry, S., Niermann, T., et al., Properties and primary structure of the L-malate dehydrogenase from the extremely thermophilic archaebacterium Methanothermus fervidus, Eur. J. Biochem., 1990, vol. 188, no. 3, pp. 623—632. https://doi.org/10.1111/j.1432-1033.1990.tb15443.x
Jendrossek, D., Kratzin, H.D., and Steinbüchel, A., The Alcaligenes eutrophus ldh structural gene encodes a novel type of lactate dehydrogenase, FEMS Microbiol. Lett., 1993, vol. 112, no. 2, pp. 229—235. https://doi.org/10.1111/j.1574-6968.1993.tb06453.x
Muramatsu, H., Mihara, H., Goto, M., et al., A new family of NAD(P)H-dependent oxidoreductases distinct from conventional Rossmann-fold proteins, J. Biosci. Bioeng., 2005, vol. 99, no. 6, pp. 541—547. https://doi.org/10.1263/jbb.99.541
Irimia, A., Madern, D., Zaccaï, G., and Vellieux, F.M., Methanoarchaeal sulfolactate dehydrogenase: prototype of a new family of NADH-dependent enzymes, EMBO J., 2004, vol. 23, no. 6, pp. 1234—1244. https://doi.org/10.1038/sj.emboj.7600147
Denger, K. and Cook, A.M., Racemase activity effected by two dehydrogenases in sulfolactate degradation by Chromohalobacter salexigens: purification of (S)-sulfolactate dehydrogenase, Microbiology (Reading), 2010, vol. 156, no. 3, pp. 967—974. https://doi.org/10.1099/mic.0.034736-0
Zhang, Y., Schofield, L.R., Sang, C., et al., Expression, purification, and characterization of (R)-sulfolactate dehydrogenase (ComC) from the rumen methanogen Methanobrevibacter millerae SM9, Archaea, 2017, article 5793620. https://doi.org/10.1155/2017/5793620
Puzakova, L.V., Puzakov, M.V., and Soldatov, A.A., Gene encoding a novel enzyme of LDH2/MDH2 family is lost in plant and animal genomes during transition to land, J. Mol. Evol., 2019, vol. 87, no. 1, pp. 52—59. https://doi.org/10.1007/s00239-018-9884-2
Puzakova, L.V., Puzakov, M.V., and Gostyukhina, O.L., Newly discovered AqE gene is highly conserved in non-tetrapod vertebrates, J. Mol. Evol., 2021, vol. 89, nos. 4—5, pp. 214—224. https://doi.org/10.1007/s00239-021-09997-x
Weinstein, C.L. and Griffith, O.W., Cysteine sulfonate and beta-sulfopyruvate metabolism: partitioning between decarboxylation, transamination, and reduction pathways, J. Biol. Chem., 1988, vol. 263, no. 8, pp. 3735—3743.
Borst, P., The malate—aspartate shuttle (Borst cycle): how it started and developed into a major metabolic pathway, IUBMB Life, 2020, vol. 72, no. 11, pp. 2241—2259. https://doi.org/10.1002/iub.2367
Wu, C., Zhang, D., Kan, M., et al., The draft genome of the large yellow croaker reveals well-developed innate immunity, Nat. Commun., 2014, vol. 5, article 5227. https://doi.org/10.1038/ncomms6227
Bray, N.L., Pimentel, H., Melsted, P., and Pachter, L., Near-optimal probabilistic RNA-seq quantification, Nat. Biotechnol., 2016, vol. 34, no. 5, pp. 525—527. https://doi.org/10.1038/nbt.3519
Pimentel, H., Bray, N.L., Puente, S., et al., Differential analysis of RNA-seq incorporating quantification uncertainty, Nat. Methods, 2017, vol. 14, no. 7, pp. 687—690. https://doi.org/10.1038/nmeth.4324
Kessler, Y., Helfer-Hungerbuehler, A.K., Cattori, V., et al., Quantitative TaqMan real-time PCR assays for gene expression normalisation in feline tissues, BMC Mol. Biol., 2009, vol. 10, p.106. https://doi.org/10.1186/1471-2199-10-106
Leal, M.F., Astur, D.C., Debieux, P., et al., Identification of suitable reference genes for investigating gene expression in anterior cruciate ligament injury by using reverse transcription-quantitative PCR, PLoS One, 2015, vol. 10, no. 7, р. e0133323. https://doi.org/10.1371/journal.pone.0133323
Minárik, P., Tomásková, N., Kollárová, M., and Antalík, M., Malate dehydrogenases—structure and function, Gen. Physiol. Biophys., 2002, vol. 21, no. 3, pp. 257—265.
Otto-Ślusarczyk, D., Graboń, W., and Mielczarek-Puta, M., Aminotransferaza asparaginianowa—kluczowy enzym w metabolizmie ogólnoustrojowym człowieka, Postepy Hig. Med. Dosw., 2016, vol. 70, pp. 219—230. https://doi.org/10.5604/17322693.1197373
Laganá, G., Barreca, D., Calderaro, A., and Bellocco, E., Lactate dehydrogenase inhibition: biochemical relevance and therapeutical potential, Curr. Med. Chem., 2019, vol. 26, no. 18, pp. 3242—3252. https://doi.org/10.2174/0929867324666170209103444
Steenweg, M.E., Jakobs, C., Errami, A., et al., An overview of L-2-hydroxyglutarate dehydrogenase gene (L2HGDH) variants: a genotype—phenotype study, Hum. Mutat., 2010, vol. 31, no. 4, pp. 380—390. https://doi.org/10.1002/humu.21197
Musrati, R.A., Kollárová, M., Mernik, N., and Mikulásová, D., Malate dehydrogenase: distribution, function and properties, Gen. Physiol. Biophys., 1998, vol. 17, no. 3, pp. 193—210.
Mitrakou, A., Kidney: its impact on glucose homeostasis and hormonal regulation, Diabetes Res. Clin. Pract., 2011, vol. 93, suppl. 1, pp. S66—S72. https://doi.org/10.1016/S0168-8227(11)70016-X
Walsh, K. and Koshland, D.E., Jr., Determination of flux through the branch point of two metabolic cycles: the tricarboxylic acid cycle and the glyoxylate shunt, J. Biol. Chem., 1984, vol. 259, no. 15, pp. 9646—9654.
Pan, Y., Chen, H., Siu, F., and Kilberg, M.S., Amino acid deprivation and endoplasmic reticulum stress induce expression of multiple activating transcription factor-3 mRNA species that, when overexpressed in HepG2 cells, modulate transcription by the human asparagine synthetase promoter, J. Biol. Chem., 2003, vol. 278, no. 40, pp. 38402—38412. https://doi.org/10.1074/jbc.M304574200
Bever, K., Chenoweth, M., and Dunn, A., Amino acid gluconeogenesis and glucose turnover in kelp bass (Paralabrax sp.), Am. J. Physiol., 1981, vol. 240, no. 3, pp. 246—252. https://doi.org/10.1152/ajpregu.1981.240.3.R246
Kumar, V., Sahu, N.P., and Pal, A.K., Modulation of key enzymes of glycolysis, gluconeogenesis, amino acid catabolism, and TCA cycle of the tropical freshwater fish Labeo rohita fed gelatinized and non-gelatinized starch diet, Fish Physiol., Biochem., 2010, vol. 36, no. 3, pp. 491—499. https://doi.org/10.1007/s10695-009-9319-5
Artsimovich, N.G., Nastoyashchaya, N.N., Kazanskii, D.B., and Lomakin, M.S., The liver as an organ of immunobiological system of homeostasis, Usp. Sovrem. Biol., 1992, vol. 112, no. 1, pp. 116—124.
Zemkov, G.V. and Zhuravleva, G.F., The kinetics of pathological changes in cumulative toxicosis as the tolerance criterium of the fish population, Usp. Sovrem. Estestvozn., 2004, no. 1, pp. 41—47.
Funding
The work was supported by the state assignment of the Federal Research Center Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences, “Functional, Metabolic, and Toxicological Aspects of the Existence of Hydrobionts and Their Populations in Biotopes with Different Physicochemical Regimes,” state registration number 121041400077-1, and by the Russian Foundation for Basic Research and the city of Sevastopol, scientific project no. 20-44-920006.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest. The authors declare they have no conflicts of interest.
Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals have been followed.
Additional information
Translated by A. Lisenkova
Rights and permissions
About this article
Cite this article
Puzakova, L.V., Puzakov, M.V. Tissue Specificity of the AqE Gene Activity in the Yellow Croaker Larimichthys crocea. Russ J Genet 58, 538–546 (2022). https://doi.org/10.1134/S1022795422050076
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1022795422050076