Abstract
Fish are useful animal models for studying effects of nutrients and environmental factors on gene expression (including epigenetics), toxicology, and carcinogenesis. To optimize the response of the animals to substances of interest (including toxins and carcinogens), water pollution, or climate changes, it is imperative to understand their fundamental biochemical processes. One of these processes concerns energy metabolism for growth, development, and survival. We have recently shown that tissues of hybrid striped bass (HSB), zebrafish, and largemouth bass (LMB) use amino acids (AAs; such as glutamate, glutamine, aspartate, alanine, and leucine) as major energy sources. AAs contribute to about 80% of ATP production in the liver, proximal intestine, kidney, and skeletal muscle tissue of the fish. Thus, as for mammals (including humans), AAs are the primary metabolic fuels in the proximal intestine of fish. In contrast, glucose and fatty acids are only minor metabolic fuels in the fish. Fish tissues have high activities of glutamate dehydrogenase, glutamate–oxaloacetate transaminase, and glutamate-pyruvate transaminase, as well as high rates of glutamate uptake. In contrast, the activities of hexokinase, pyruvate dehydrogenase, and carnitine palmitoyltransferase 1 in all the tissues are relatively low. Furthermore, unlike mammals, the skeletal muscle (the largest tissue) of HSB and LMB has a limited uptake of long-chain fatty acids and barely oxidizes fatty acids. Our findings explain differences in the metabolic patterns of AAs, glucose, and lipids among various tissues in fish. These new findings have important implications for understanding metabolic significance of the tissue-specific oxidation of AAs (particularly glutamate and glutamine) in gene expression (including epigenetics), nutrition, and health, as well as carcinogenesis in fish, mammals (including humans), and other animals.
Sichao Jia, Xinyu Li: Contributed equally to this work.
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- AAs:
-
Amino acids
- BCAT:
-
Branched-chain AA transaminase
- CPT-I:
-
Carnitine palmitoyltransferase 1
- GDH:
-
Glutamate dehydrogenase
- HSB:
-
Hybrid striped bass
- LMB:
-
Largemouth bass
- PDH:
-
Pyruvate dehydrogenase
References
Andersen S, Waagbø R, Espe M (2016) Functional amino acids in fish health and welfare. Front Biosci 8:143–169
Arike L, Seiman A, van der Post S, Rodriguez Piñeiro AM, Ermund A, Schütte A, Bäckhed F, Johansson MEV, Hansson GC (2020) Protein turnover in epithelial cells and mucus along the gastrointestinal tract is coordinated by the spatial location and microbiota. Cell Rep 30:1077–1087
Bailey GS, Williams DE, Hendricks JD (1996) Fish models for environmental carcinogenesis: the rainbow trout. Environ Health Perspec 104:5–21
Ballantyne JS (2001) Amino acid metabolism. Fish Physiol 20:77–107
Baxt LA, Xavier RJ (2015) Role of autophagy in the maintenance of intestinal homeostasis. Gastroenterology 149:553–562
Bazer FW, Burghardt RC, Johnson GA, Spencer TE, Wu G (2018) Mechanisms for the establishment and maintenance of pregnancy: synergies from scientific collaborations. Biol Reprod 99:225–241
Bazer FW, Seo H, Johnson GA, Wu G (2021) One-carbon metabolism and development of the conceptus during pregnancy: lessons from studies with sheep and pigs. Adv Exp Med Biol 1285:1–15
Black JJ, Baumann PC (1991) Carcinogens and cancers in freshwater fishes. Environ Health Perspec 90:27–33
Bunton TE (1996) Experimental chemical carcinogenesis in fish. Toxicol Pathol 24:603–618
Campbell JW, Aster PL, Vorhaben JE (1983) Mitochondrial ammoniagenesis in liver of the channel catfish Ictalurus punctatus. Am J Physiol 244:R709–R717
Cao Y, Yao J, Sun X, Liu S, Martin GB (2021) Amino acids in the nutrition and production of sheep and goats. Adv Exp Med Biol 1285:63–79
Chamberlin ME, Glemet HC, Ballantyne JS (1991) Glutamine metabolism in a holostean (Amia calva) and teleost fish (Salvelinus namaycush). Am J Physiol Integr Comp Physiol 260:R159–R166
Chen JQ, Jin Y, Yang Y, Wu ZL, Wu G (2020) Epithelial dysfunction in lung diseases: effects of amino acids and potential mechanisms. Adv Exp Med Biol 1265:57–70
Cossins AR, Crawford DL (2005) Fish models for environmental genomics. Nat Rev Genet 6:324–333
Couch JA, Harshbarger JC (1985) Effects of carcinogenic agents on aquatic animals: an environmental and experimental overview. Environ Carcinogen Revs 3:63–105
Ebeling JM, Timmons MB (2012) Recirculating aquaculture systems. In: Aquaculture production systems
Enes P, Panserat S, Kaushik S, Oliva-Teles A (2006) Effect of normal and waxy maize starch on growth, food utilization and hepatic glucose metabolism in European sea bass (Dicentrarchus labrax) juveniles. Comp Biochem Physiol A 143:89–96
Fontana L, Partridge L (2015) Promoting health and longevity through diet: from model organisms to humans. Cell 161:106–118
French CJ, Mommsen TP, Hochachka PW (1981) Amino acid utilisation in isolated hepatocytes from rainbow trout. Eur J Biochem 113:311–317
Gatlin DM, Barrows FT, Brown P et al (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579
Gaylord TG, Rawles SD (2007) The modification of poultry by-product meal for use in hybrid striped bass Morone chrysops×M. saxatilis diets. J World Aquac Soc 36:363–374
Gilbreath KR, Bazer FW, Satterfield MC, Wu G (2021) Amino acid nutrition and reproductive performance in ruminants. Adv Exp Med Biol 1285:43–61
Hawkins WE, Overstreet RM, Fournie JW, Walker WW (1985) Development of aquarium fish models for environmental carcinogenesis: tumor induction in seven species. J Appl Toxicol 5:261–264
Haynes TE, Li P, Li XL, Shimotori K, Sato H, Flynn NE et al (2009) L-Glutamine or L-alanyl-L-glutamine prevents oxidant- or endotoxin-induced death of neonatal enterocytes. Amino Acids 37:131–142
He WL, Li P, Wu G (2021) Amino acid nutrition and metabolism in chickens. Adv Exp Med Biol 1285:109–131
Hou Y, Wu G (2018) L-Glutamate nutrition and metabolism in swine. Amino Acids 50:1497–1510
Hou Y, Yin Y, Wu G (2015) Dietary essentiality of “nutritionally non-essential amino acids” for animals and humans. Exp Biol Med 240:997–1007
Hou YQ, He WL, Hu SD, Wu G (2019) Composition of polyamines and amino acids in plant-source foods for human consumption. Amino Acids 51:1153–1165
Hou YQ, Hu SD, Li XY, He WL, Wu G (2020) Amino acid metabolism in the liver: nutritional and physiological significance. Adv Exp Med Biol 1265:21–37
Ip YK, Chew SF (2010) Ammonia production, excretion, toxicity, and defense in fish: a review. Front Physiol 1:134
Ishak Gabra MB, Yang Y, Li H et al (2020) Dietary glutamine supplementation suppresses epigenetically-activated oncogenic pathways to inhibit melanoma tumour growth. Nat Commun 11:3326
Ji Y, Wu ZL, Dai ZL, Wang XL, Li J, Wang BG, Wu G (2017) Fetal and neonatal programming of postnatal growth and feed efficiency in swine. J Anim Sci Biotechnol 8:42
Jia S (2019) Nutritional roles of glutamate and glutamine in the growth of juvenile hybrid striped bass. M.S. Thesis. Texas A&M University, College Station, TX, USA
Jia S, Li X, Zheng S, Wu G (2017) Amino acids are major energy substrates for tissues of hybrid striped bass and zebrafish. Amino Acids 49:2053–2063
Jobgen WS, Fried SK, Fu WJ et al (2006) Regulatory role for the arginine–nitric oxide pathway in metabolism of energy substrates. J Nutr Biochem 17:571–588
Johnson GA, Bazer FW, Burghardt RC, Wu G, Seo H, Kramer AC, McLendon BA (2018) Cellular events during ovine implantation and impact for gestation. Anim Reprod 15(Suppl 1):843–855
Jürss K, Bastrop R (1995) Amino acid metabolism in fish. In: Biochemistry and molecular biology of fishes. vol 4. Elsevier, New York, NY. pp 159–189
Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquac Res 41:322–332
Kovacevic Z, J D McGivan JD (1983) Mitochondrial metabolism of glutamine and glutamate and its physiological significance. Physiol Rev 63:547–605
Lei J, Feng D, Zhang Y et al (2012) Regulation of leucine catabolism by metabolic fuels in mammary epithelial cells. Amino Acids 43:2179–2189
Leone RD, Zhao L, Englert JM, Sun I-M, Oh M-H, Im-Hong Sun I-H, Arwood ML, Bettencourt IA, Patel CH, Wen J, Tam A, Blosser RL, Prchalova E, Alt J, Rais R, Slusher BS, Powell JD (2019) Glutamine blockade induces divergent metabolic programs to overcome tumor immune evasion. Science 366:1013–1021
Li P, Wu G (2020) Composition of amino acids and related nitrogenous nutrients in feedstuffs for animal diets. Amino Acids 52:523–542
Li P, Yin YL, Li DF, Kim SW, Wu G (2007) Amino acids and immune function. Br J Nutr 98:237–252
Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53
Li XY, Zheng SX, Wu G (2020a) Amino acid metabolism in the kidneys: nutritional and physiological significance. Adv Exp Med Biol 1265:71–95
Li XY, Zheng SX, Jia SC, Song F, Zhou CP, Wu G (2020b) Oxidation of energy substrates in tissues of largemouth bass (Micropterus salmoides). Amino Acids 52:1017–1032
Li XY, Zheng SX, Ma XK, Cheng KM, Wu G (2020c) Effects of dietary starch and lipid levels on the protein retention and growth of largemouth bass (Micropterus salmoides). Amino Acids 52:999–1016
Li XY, Zheng SX, Ma XK, Cheng KM, Wu G (2020d) Effects of dietary protein and lipid levels on growth performance, feed utilization, and liver histology of largemouth bass (Micropterus salmoides). Amino Acids 52:1043–1061
Li XY, Zheng SX, Han T, Song F, Wu G (2020e) Effects of dietary protein intake on the oxidation of glutamate, glutamine, glucose and palmitate in tissues of largemouth bass (Micropterus salmoides) Amino Acids 52:1491–1503
Li XL, Zheng SX, Wu G (2020f) Nutrition and metabolism of glutamate and glutamine in fish. Amino Acids 52:671–691
Li XY, Zheng SX, Ma XK, Cheng KM, Wu G (2021a) Use of alternative protein sources for fishmeal replacement in the diet of largemouth bass (Micropterus salmoides). Part I: effects of poultry by-product meal and soybean meal on growth, feed utilization, and health. Amino Acids 53:33-47
Li XY, Zheng SX, Cheng KM, Ma XK, Wu G (2021b) Use of alternative protein sources for fishmeal replacement in the diet of largemouth bass (Micropterus salmoides). Part II: Effects of supplementation with methionine or taurine on growth, feed utilization, and health. Amino Acids 53:49–62
Li XY, Zheng SX, Wu G (2021c) Nutrition and functions of amino acids in fish. Adv Exp Med Biol 1285:133–168
Li XY, Han T, Zheng SX, Wu G (2021d) Nutrition and functions of amino acids in aquatic crustaceans. Adv Exp Med Biol 1285:169–197
Lieu EL, Nguyen T, Rhyne S, Kim J (2020) Amino acids in cancer. Exp Mol Med 52:15–30
Malins DC, Krahn MM, Myers MS (1985b) Toxic chemicals in sediments and biota from a creosote-polluted harbor: Relationships with hepatic neoplasms and other hepatic lesions in English sole (Parophrys vetulus). Carcinogenesis 6:1463–1469
Malins DC, Krahn MM, Brown DW, Rhodes LD, Myers MS, McCain BB, Chan S-L (1985a) Toxic chemicals in marine sediment and biota from Mukilteo, Washington: relationships with hepatic neoplasms and other hepatic lesions in English sole (Parophrys vetulus). J Natl Cancer Inst 74:487–494
Pan SY, Morrison H (2011) Epidemiology of cancer of the small intestine. World J Gastrointest Oncol 3:33–42
Patankar JV, Becker C (2020) Cell death in the gut epithelium and implications for chronic inflammation. Nat Rev Gastroenterol Hepatol 17:543–556
Roberts RJ (1989) Neoplasia of Teleosts. In: Roberts RJ (ed) Fish pathology. Bailliere Tindall, London, pp 153–171
Rønnestad I, Fyhn HJ (1993) Metabolic aspects of free amino acids in developing marine fish eggs and larvae. Rev Fish Sci 1:239–259
Rønnestad I, Thorsen A, Finn RN (1999) Fish larval nutrition: a review of recent advances in the roles of amino acids. Aquaculture 177:201–216
Schartl M (2014) Beyond the zebrafish: diverse fish species for modeling human disease. Dis Model Mech 7:181–192
Schlumberger HG, Lucké B (1948) Tumors of fishes, amphibians, and reptiles. Cancer Res 8:657–753
Seo H, Johnson GA, Bazer FW, Wu G, McLendon BA, Kramer AC (2020) Cell-specific expression of enzymes for serine biosynthesis and glutaminolysis in farm animals. Adv Exp Med Biol 1285:17–28
Simpson NE, Tryndyak VP, Pogribna M, Beland FA, Pogribny IP (2012) Modifying metabolically sensitive histone marks by inhibiting glutamine metabolism affects gene expression and alters cancer cell phenotype. Epigenetics 7:1413–1420
Stoletov K, Klemke R (2008) Catch of the day: zebrafish as a human cancer model. Oncogene 27:4509–4520
Tng YYM, Wee NLJ, Ip YK, Chew SF (2008) Postprandial nitrogen metabolism and excretion in juvenile marble goby, oxyeleotris marmorata (Bleeker, 1852). Aquaculture 284:260–267
Trushenski J, Gause B (2013) Comparative value of fish meal alternatives as protein sources in feeds for hybrid striped bass. N Am J Aquac 75:329–341
Van Veld P, Vogelbein W, Cochran M, Goksoyr A, Stegeman J (1997) Route-specific cellular expression of cytochrome P4501A (CYP1A) in fish (Fundulus heteroclitus) following exposure to aqueous and dietary benzo[a]pyrene. Toxicol Appl Pharmacol 142:348–359
Van Waarde A (1983) Review aerobic and anaerobic ammonia production by fish. Comp Biochem Physiol 74b:675–684
Vettore L, Westbrook RL, Tennant DA (2020) New aspects of amino acid metabolism in cancer. Br J Cancer 122:150–156
Wang JJ, Chen LX, Li P, Li XL, Zhou HJ, Wang FL et al (2008) Gene expression is altered in piglet small intestine by weaning and dietary glutamine supplementation. J Nutr 138:1025–1032
Wang JJ, Wu ZL, Li DF, Li N, Dindot SV, Satterfield MC, Bazer FW, Wu G (2012) Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal 17:282–301
Weber JM, Haman F (1996) Pathways for metabolic fuels and oxygen in high performance fish. Comp Biochem Physiol A 113:33–38
Wilson RP (2002) Amino acids and proteins. In: Fish Nutrition (Halver JE, Hardy RW eds). Academic Press, New York. pp 143–179
Williams DE, Lech JJ, Buhler DR (1998) Xenobiotics and xenoestrogens in fish: modulation of cytochrome P450 and carcinogenesis. Mutation Res 399:179–192
Wong C, Qian Y, Yu J (2017) Interplay between epigenetics and metabolism in oncogenesis: mechanisms and therapeutic approaches. Oncogene 36:3359–3374
Wu G (1998) Intestinal mucosal amino acid catabolism. J Nutr 128:1249–1252
Wu G (2013) Amino acids: biochemistry and nutrition. CRC Press, Boca Raton
Wu G (2014) Dietary requirements of synthesizable amino acids by animals: a paradigm shift in protein nutrition. J Anim Sci Biotechnol 5:34
Wu G (2018) Principles of Animal Nutrition. CRC Press, Boca Raton
Wu G (2020) Important roles of dietary taurine, creatine, carnosine, anserine and 4-hydroxyproline in human nutrition and health. Amino Acids 52:329–360
Wu G (2021) Amino Acids: Biochemistry and Nutrition, 2nd edition. CRC Press, Boca Raton
Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Intrauterine growth retardation: Implications for the animal sciences. J Anim Sci 84:2316–2337
Yang Y, He Y, Jin YH, Wu G, and Wu ZL (2021) Amino acids in endoplasmic reticulum stress and redox signaling. Adv Exp Med Biol
Yoshida C, Maekawa M, Bannai M, Yamamoto T (2016) Glutamate promotes nucleotide synthesis in the gut and improves availability of soybean meal feed in rainbow trout. Springerplus 5:1021
Zhang JM, He WL, Yi D, Zhao D, Song Z, Hou YQ, Wu G (2019) Regulation of protein synthesis in porcine mammary epithelial cells by L-valine. Amino Acids 51:717–726
Zhang J, Pavlova NN, Craig B Thompson CB (2020) Cancer cell metabolism: the essential role of the nonessential amino acid, glutamine. EMBO J 36:1302–1315
Zhang Q, Hou YQ, Bazer FW, He WL, Posey EA, Wu G (2021) Amino acids in swine nutrition and production. Adv Exp Med Biol 1285:81–107
Zhu YH, Li TT, Huang SM, Wang W, Dai ZL, Feng CP, Wu G, Wang JJ (2018) Maternal L-glutamine supplementation during late-gestation improves intrauterine growth restriction-induced intestinal dysfunction in piglets. Amino Acids 50:1289–1299
Acknowledgements
This work was supported by Texas A&M AgriLife Research (H-8200). We thank graduate students and research assistants in our laboratory for helpful discussions.
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Jia, S., Li, X., He, W., Wu, G. (2021). Oxidation of Energy Substrates in Tissues of Fish: Metabolic Significance and Implications for Gene Expression and Carcinogenesis. In: Wu, G. (eds) Amino Acids in Nutrition and Health. Advances in Experimental Medicine and Biology, vol 1332. Springer, Cham. https://doi.org/10.1007/978-3-030-74180-8_5
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