Skeletal Muscle and the Effects of Ammonia Toxicity in Fish, Mammalian, and Avian Species: A Comparative Review Based on Molecular Research
Language English Country Switzerland Media electronic
Document type Journal Article, Review
Grant support
NC1084
USDA Regional Project
PubMed
32629824
PubMed Central
PMC7370143
DOI
10.3390/ijms21134641
PII: ijms21134641
Knihovny.cz E-resources
- Keywords
- ammonia, avian, fish, mammal, muscle, myostatin,
- MeSH
- Ammonia pharmacology toxicity MeSH
- Hyperammonemia etiology MeSH
- Liver Cirrhosis etiology MeSH
- Muscle Fibers, Skeletal drug effects MeSH
- Muscle, Skeletal drug effects metabolism MeSH
- Birds MeSH
- Fishes MeSH
- Sarcopenia etiology MeSH
- Mammals MeSH
- Muscular Atrophy metabolism physiopathology MeSH
- Muscle Development drug effects physiology MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Ammonia MeSH
Typically, mammalian and avian models have been used to examine the effects of ammonia on skeletal muscle. Hyperammonemia causes sarcopenia or muscle wasting, in mammals and has been linked to sarcopenia in liver disease patients. Avian models of skeletal muscle have responded positively to hyperammonemia, differing from the mammalian response. Fish skeletal muscle has not been examined as extensively as mammalian and avian muscle. Fish skeletal muscle shares similarities with avian and mammalian muscle but has notable differences in growth, fiber distribution, and response to the environment. The wide array of body sizes and locomotion needs of fish also leads to greater diversity in muscle fiber distribution and growth between different fish species. The response of fish muscle to high levels of ammonia is important for aquaculture and quality food production but has not been extensively studied to date. Understanding the differences between fish, mammalian and avian species' myogenic response to hyperammonemia could lead to new therapies for muscle wasting due to a greater understanding of the mechanisms behind skeletal muscle regulation and how ammonia effects these mechanisms. This paper provides an overview of fish skeletal muscle and ammonia excretion and toxicity in fish, as well as a comparison to avian and mammalian species.
Department of Anatomy Poznan University of Medical Sciences 60 781 Poznan Poland
Department of Histology and Embryology Poznan University of Medical Sciences 60 781 Poznan Poland
Prestage Department of Poultry Science North Carolina State University Raleigh NC 27695 USA
See more in PubMed
Wang W., Walsh W. High ammonia tolerance in fishes of the family Batrachoididae (Toadfish and Midshipmen) Aquat. Toxicol. 2000;50:205–219. doi: 10.1016/S0166-445X(99)00101-0. PubMed DOI
Wee N.L.J., Tng Y.Y.M., Cheng H.T., Lee S.M.L., Chew S.F., Ip Y.K. Ammonia toxicity and tolerance in the brain of the African sharptooth catfish, Clarias gariepinus. Aquat. Toxicol. 2007;82:204–213. doi: 10.1016/j.aquatox.2007.02.015. PubMed DOI
Ip Y.K., Leong M.W.F., Sim M.Y., Goh G.S., Wong W.P., Chew S.F. Chronic and acute ammonia toxicity in mudskippers, Periophthalmodon schlosseri and Boleophthalmus boddaerti: Brain ammonia and glutamine contents, and effects of methionine sulfoximine and MK801. J. Exp. Biol. 2005;208:1993–2004. doi: 10.1242/jeb.01586. PubMed DOI
Sänger A.M., Stoiber W. Muscle Fiber Diversity and Plasticity. Fish Physiol. 2001;18:187–250.
Greer-Walker M. Growth and development of the Skeletal Muscle Fibres of the Cod (Gadus morhua L.) ICES J. Mar. Sci. 1970;33:228–244. doi: 10.1093/icesjms/33.2.228. DOI
Zhang G., Swank D.M., Rome L.C. Quantitative distribution of muscle fiber types in the scup Stenotomus chrysops. J. Morphol. 1996;229:71–81. doi: 10.1002/(SICI)1097-4687(199607)229:1<71::AID-JMOR4>3.0.CO;2-S. PubMed DOI
Rome L.C., Swank D., Corda D. How fish power swimming. Science. 1993;261:340–343. doi: 10.1126/science.8332898. PubMed DOI
Bone Q. Fish Physiology. Elsevier; Amsterdam, The Netherlands: 1978. Locomotor muscle.
Jayne B.C., Lauder G.V. How swimming fish use slow and fast muscle fibers: Implications for models of vertebrate muscle recruitment. J. Comp. Physiol. A. 1994;175:123–131. doi: 10.1007/BF00217443. PubMed DOI
Driedzic W.R., Hochachka P.W. Control of Energy Metabolism in Fish White Muscle. Am. J. Physiol. 1976;230:579–582. doi: 10.1152/ajplegacy.1976.230.3.579. PubMed DOI
McKenzie D.J. Encyclopedia of Fish Physiology. Elsevier; Amsterdam, The Netherlands: 2011. Energetics of Fish Swimming.
Videler J.J. Fish Swimming. Springer; Dordrecht, Netherlands: 1993.
Rowlerson A., Mascarello F., Radaelli G., Veggetti A. Differentiation and growth of muscle in the fish Sparus aurata (L): II. Hyperplastic and hypertrophic growth of lateral muscle from hatching to adult. J. Muscle Res. Cell Motil. 1995;16:223–236. doi: 10.1007/BF00121131. PubMed DOI
Johnston I.A., Davison W., Goldspink G. Energy metabolism of carp swimming muscles. J. Comp. Physiol. B. 1977;114:203–216. doi: 10.1007/BF00688970. DOI
Johnston I.A., Patterson S., Ward P., Goldspink G. The histochemical demonstration of myofibrillar adenosine triphosphatase activity in fish muscle. Can. J. Zool. 1974;52:871–877. doi: 10.1139/z74-118. PubMed DOI
Schiaffino S., Reggiani C. Fiber types in mammalian skeletal muscles. Physiol. Rev. 2011;91:1447–1531. doi: 10.1152/physrev.00031.2010. PubMed DOI
Gerrard D.E., Grant A.L. Principles of Animal Growth and Development. Kendall Hunt; Dubuque, IA, USA: 2003.
Sawatari E., Seki R., Adachi T., Hashimoto H., Uji S., Wakamatsu Y., Nakata T., Kinoshita M. Overexpression of the dominant-negative form of myostatin results in doubling of muscle-fiber number in transgenic medaka (Oryzias latipes) Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2010;155:183–189. doi: 10.1016/j.cbpa.2009.10.030. PubMed DOI
Wiskus K.J., Addis P.B., Ma R.-I. Distribution of βR, αR and αW Fibers in Turkey Muscles. Poult. Sci. 1976;55:562–572. doi: 10.3382/ps.0550562. DOI
Pette D., Staron R. Myosin Isoforms, Muscle Fiber Types, and Transitions. Microsc. Res. Tech. 2000;50:500–509. doi: 10.1002/1097-0029(20000915)50:6<500::AID-JEMT7>3.0.CO;2-7. PubMed DOI
Vélez E.J., Lutfi E., Azizi S., Perelló M., Salmerón C., Riera-Codina M., Ibarz A., Fernández-Borràs J., Blasco J., Capilla E., et al. Understanding fish muscle growth regulation to optimize aquaculture production. Aquaculture. 2017;467:28–40. doi: 10.1016/j.aquaculture.2016.07.004. DOI
Mommsen T.P. Paradigms of Growth in Fish. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001;129:207–219. doi: 10.1016/S1096-4959(01)00312-8. PubMed DOI
Bodine S.C., Stitt T.N., Gonzalez M., Kline W.O., Stover G.L., Bauerlein R., Zlotchenko E., Scrimgeour A., Lawrence J.C., Glass D.J., et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 2001;3:1014–1019. doi: 10.1038/ncb1101-1014. PubMed DOI
Wigmore P.M., Strickland N.C. DNA, RNA and Protein in Skeletal Muscle of Large and Small Pig Fetuses. Growth. 1983;47:67–76. doi: 10.1371/journal.pone.0072418. PubMed DOI
Koumans J.T.M., Akster H.A., Booms G.H.R., Osse J.W.M. Growth of carp (Cyprinus carpio) white axial muscle; hyperplasia and hypertrophy in relation to the myonucleus/sarcoplasm ratio and the occurrence of different subclasses of myogenic cells. J. Fish Biol. 1993;43:69–80. doi: 10.1111/j.1095-8649.1993.tb00411.x. DOI
Koumans J.T.M., Akster H.A., Witkam A., Osse J.W.M. Numbers of muscle nuclei and myosatellite cell nuclei in red and white axial muscle during growth of the carp (Cyprinus carpio) J. Fish Biol. 1994;44:391–408. doi: 10.1111/j.1095-8649.1994.tb01220.x. DOI
Stickland N.C. Growth and development of muscle fibres in the rainbow trout (Salmo gairdneri) J. Anat. 1983;137:323–333. PubMed PMC
Rowlerson A., Veggetti A. Cellular Mechanisms of Post-Embryonic Muscle Growth in Aquaculture Species. Fish Physiol. 2001;18:103–140. doi: 10.1016/S1546-5098(01)18006-4. DOI
Veggetti A., Mascarello F., Scapolo P.A., Rowlerson A., Carnevali C. Muscle growth and myosin isoform transitions during development of a small teleost fish, Poecilia reticulata (Peters) (Atheriniformes, Poeciliidae): A histochemical, immunohistochemical, ultrastructural and morphometric study. Anat. Embryol. 1993;187:353–361. doi: 10.1007/BF00185893. PubMed DOI
Carpenè E., Veggetti A. Increase in muscle fibres in the lateralis muscle (white portion) of Mugilidae (Pisces, Teleostei) Experientia. 1981;37:191–193. doi: 10.1007/BF01963227. PubMed DOI
Romanello M.G., Scapolo P.A., Luprano S., Mascarello F. Post-larval growth in the lateral white muscle of the eel, Anguilla anguilla. J. Fish Biol. 1987;30:161–172. doi: 10.1111/j.1095-8649.1987.tb05742.x. DOI
Patterson S.E., Mook L.B., Devoto S.H. Growth in the Larval Zebrafish Pectoral Fin and Trunk Musculature. Dev. Dyn. 2008;237:307–315. doi: 10.1002/dvdy.21400. PubMed DOI
Ahammad A.K.S., Asaduzzaman M., Asakawa S., Watabe S., Kinoshita S. Regulation of gene expression mediating indeterminate muscle growth in teleosts. Mech. Dev. 2015;137:53–65. doi: 10.1016/j.mod.2015.02.006. PubMed DOI
Froehlich J.M., Fowler Z.G., Galt N.J., Smith D.L., Biga P.R. Sarcopenia and piscines: The case for indeterminate-growing fish as unique genetic model organisms in aging and longevity research. Front. Genet. 2013;4:159. doi: 10.3389/fgene.2013.00159. PubMed DOI PMC
Seale P., Sabourin L.A., Girgis-Gabardo A., Mansouri A., Gruss P., Rudnicki M.A. Pax7 is required for the specification of myogenic satellite cells. Cell. 2000;102:777–786. doi: 10.1016/S0092-8674(00)00066-0. PubMed DOI
Wang Y.X., Rudnicki M.A. Satellite Cells, the Engines of Muscle Repair. Nat. Rev. Mol. Cell Biol. 2011;13:127–133. doi: 10.1038/nrm3265. PubMed DOI
Kablar B., Krastel K., Ying C., Asakura A., Tapscott S.J., Rudnicki M.A. MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development. 1997;124:4729–4738. PubMed
Rudnicki M.A., Schnegelsberg P.N., Stead R.H., Braun T., Arnold H.H., Jaenisch R. MyoD or Myf-5 Is Required for the Formation of Skeletal Muscle. Cell. 1993;75:1351–1359. doi: 10.1016/0092-8674(93)90621-V. PubMed DOI
Tajbakhsh S., Cossu G. Establishing myogenic identity during somitogenesis. Curr. Opin. Genet. Dev. 1997;7:634–641. doi: 10.1016/S0959-437X(97)80011-1. PubMed DOI
Hasty P., Bradley A., Morris J.H., Edmondson D.G., Venuti J.M., Olson E.N., Klein W.H. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature. 1993;364:501–506. doi: 10.1038/364501a0. PubMed DOI
Hinits Y., Osborn D.P.S., Carvajal J.J., Rigby P.W.J., Hughes S.M. Mrf4 (myf6) is dynamically expressed in differentiated zebrafish skeletal muscle. Gene Expr. Patterns. 2007;7:738–745. doi: 10.1016/j.modgep.2007.06.003. PubMed DOI PMC
Nabeshima Y., Hanaoka K., Hayasaka M., Esuml E., Li S., Nonaka I., Nabeshima Y. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature. 1993;364:532–535. doi: 10.1038/364532a0. PubMed DOI
Weinberg E.S., Allende M.L., Kelly C.S., Abdelhamid A., Murakami T., Andermann P., Doerre O.G., Grunwald D.J., Riggleman B. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development. 1996;122:271–280. PubMed
Cole N.J., Hall T.E., Martin C.I., Chapman M.A., Kobiyama A., Nihei Y., Watabe S., Johnston I.A. Temperature and the expression of myogenic regulatory factors (MRFs) and myosin heavy chain isoforms during embryogenesis in the common carp Cyprinus carpio L. J. Exp. Biol. 2004;207:2111–2120. doi: 10.1242/jeb.01263. PubMed DOI
Xie S.Q., Mason P.S., Wilkes D., Goldspink G., Fauconneau B., Stickland N.C. Lower environmental temperature delays and prolongs myogenic regulatory factor expression and muscle differentiation in rainbow trout (Onchrhynchus mykiss) embryos. Differentiation. 2001;68:106–114. doi: 10.1046/j.1432-0436.2001.680204.x. PubMed DOI
Steinbacher P., Haslett J.R., Obermayer A., Marschallinger J., Bauer H.C., Sänger A.M., Stoiber W. MyoD and Myogenin expression during myogenic phases in brown trout: A precocious onset of mosaic hyperplasia is a prerequisite for fast somatic growth. Dev. Dyn. 2007;236:1106–1114. doi: 10.1002/dvdy.21103. PubMed DOI
Schiaffino S., Dyar K.A., Ciciliot S., Blaauw B., Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 2013;280:4294–4314. doi: 10.1111/febs.12253. PubMed DOI
Barclay R.D., Burd N.A., Tyler C., Tillin N.A., Mackenzie R.W. The Role of the IGF-1 Signaling Cascade in Muscle Protein Synthesis and Anabolic Resistance in Aging Skeletal Muscle. Front. Nutr. 2019;6:146. doi: 10.3389/fnut.2019.00146. PubMed DOI PMC
Tortorella L.L., Milasincic D.J., Pilch P.F. Critical proliferation-independent window for basic fibroblast growth factor repression of myogenesis via the p42/p44 MAPK signaling pathway. J. Biol. Chem. 2001;276:13709–13717. doi: 10.1074/jbc.M100091200. PubMed DOI
Ju L., Johnson S.E. ERK2 Is Required for Efficient Terminal Differentiation of Skeletal Myoblasts. Biochem. Biophys. Res. Commun. 2006;345:1425–1433. doi: 10.1016/J.BBRC.2006.05.051. PubMed DOI
Beckman B.R., Larsen D.A., Moriyama S., Lee-Pawlak B., Dickhoff W.W. Insulin-like Growth factor-I and Environmental Modulation of Growth During Smoltification of Spring Chinook Salmon (Oncorhynchus Tshawystscha) Gen. Comp. Endocrinol. 1998;109:325–335. doi: 10.1006/gcen.1997.7036. PubMed DOI
Pérez-Sánchez J., Martí-Palanca H., Kaushik S.J. Ration size and protein intake affect circulating growth hormone concentration, hepatic growth hormone binding and plasma insulin-like growth factor-I immunoreactivity in a marine teleost, the gilthead sea bream (Sparus aurata) J. Nutr. 1995;125:546–552. doi: 10.1093/jn/125.3.546. PubMed DOI
McCormick S.D., Kelley K.M., Young G., Nishioka R.S., Bern H.A. Stimulation of coho salmon growth by insulin-like growth factor I. Gen. Comp. Endocrinol. 1992;86:398–406. doi: 10.1016/0016-6480(92)90064-Q. PubMed DOI
McPherron A.C., Lawler A.M., Lee S.-J. Regulation of skeletal muscle mass in mice by a new TGF-p superfamily member. Nature. 1997;387:83–90. doi: 10.1038/387083a0. PubMed DOI
Thomas M., Langley B., Berry C., Sharma M., Kirk S., Bass J., Kambadur R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J. Biol. Chem. 2000;275:40235–40243. doi: 10.1074/jbc.M004356200. PubMed DOI
Zhu X., Topouzis S., Liang L.F., Stotish R.L. Myostatin Signaling Through Smad2, Smad3 and Smad4 Is Regulated by the Inhibitory Smad7 by a Negative Feedback Mechanism. Cytokine. 2004;26:262–272. doi: 10.1016/j.cyto.2004.03.007. PubMed DOI
McFarlane C., Plummer E., Thomas M., Hennebry A., Ashby M., Ling N., Smith H., Sharma M., Kambadur R. Myostatin Induces Cachexia by Activating the Ubiquitin Proteolytic System Through an NF-kappaB-independent, FoxO1-dependent Mechanism. J. Cell. Physiol. 2006;209:501–514. doi: 10.1002/jcp.20757. PubMed DOI
Trendelenburg A.U., Meyer A., Rohner D., Boyle J., Hatakeyama S., Glass D.J. Myostatin Reduces Akt/TORC1/p70S6K Signaling, Inhibiting Myoblast Differentiation and Myotube Size. Am. J. Physiol. Cell Physiol. 2009;296:1258–1270. doi: 10.1152/ajpcell.00105.2009. PubMed DOI
McPherron A.C., Lee S.J. Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl. Acad. Sci. USA. 1997;94:12457–12461. doi: 10.1073/pnas.94.23.12457. PubMed DOI PMC
Kambadur R., Sharma M., Smith T.P., Bass J.J. Mutations in Myostatin (GDF8) in Double-Muscled Belgian Blue and Piedmontese Cattle. Genome Res. 1997;7:910–915. doi: 10.1101/gr.7.9.910. PubMed DOI
Acosta J., Carpio Y., Borroto I., González O., Estrada M.P. Myostatin gene silenced by RNAi show a zebrafish giant phenotype. J. Biotechnol. 2005;119:324–331. doi: 10.1016/j.jbiotec.2005.04.023. PubMed DOI
Fuentes E.N., Pino K., Navarro C., Delgado I., Valdés J.A., Molina A. Transient inactivation of myostatin induces muscle hypertrophy and overcompensatory growth in zebrafish via inactivation of the SMAD signaling pathway. J. Biotechnol. 2013;168:295–302. doi: 10.1016/j.jbiotec.2013.10.028. PubMed DOI
Lee S.B., Kim Y.S., Oh M.-Y., Jeong I., Seong K.-B., Jin H.-J. Improving rainbow trout (Oncorhynchus mykiss) growth by treatment with a fish (Paralichthys olivaceus) myostatin prodomain expressed in soluble forms in E. coli. Aquaculture. 2010;302:270–278. doi: 10.1016/j.aquaculture.2010.02.027. DOI
Rescan P.-Y., Jutel I., Rallière C. Two myostatin genes are differentially expressed in myotomal muscles of the trout (Oncorhynchus mykiss) J. Exp. Biol. 2001;204:3523–3529. PubMed
Østbye T.K., Galloway T.F., Nielsen C., Gabestad I., Bardal T., Andersen Ø. The two myostatin genes of Atlantic salmon (Salmo salar) are expressed in a variety of tissues. Eur. J. Biochem. 2001;268:5249–5257. doi: 10.1046/j.0014-2956.2001.02456.x. PubMed DOI
Roberts S.B., Goetz F.W. Differential skeletal muscle expression of myostatin across teleost species, and the isolation of multiple myostatin isoforms. FEBS Lett. 2001;491:212–216. doi: 10.1016/S0014-5793(01)02196-2. PubMed DOI
Wang C., Chen Y.L., Bian W.P., Xie S.L., Qi G.L., Liu L., PR S., JX Z., DS P. Deletion of Mstna and Mstnb Impairs the Immune System and Affects Growth Performance in Zebrafish. Fish Shellfish Immunol. 2018;72:572–580. doi: 10.1016/j.fsi.2017.11.040. PubMed DOI
Maccatrozzo L., Bargelloni L., Radaelli G., Mascarello F., Patarnello T. Characterization of the myostatin gene in the gilthead seabream (Sparus aurata): Sequence, genomic structure, and expression pattern. Mar. Biotechnol. 2001;3:224–230. doi: 10.1007/s101260000064. PubMed DOI
Leggatt R.A., Iwama G.K. Occurrence of polyploidy in the fishes. Rev. Fish Biol. Fish. 2003;13:237–246. doi: 10.1023/B:RFBF.0000033049.00668.fe. DOI
Gabillard J.C., Biga P.R., Rescan P.Y., Seiliez I. Revisiting the Paradigm of Myostatin in Vertebrates: Insights from Fishes. Gen. Comp. Endocrinol. 2013;194:45–54. doi: 10.1016/j.ygcen.2013.08.012. PubMed DOI
Ji S., Losinski R.L., Cornelius S.G., Frank G.R., Willis G.M., Gerrard D.E., Depreux F.F., Spurlock M.E. Myostatin expression in porcine tissues: Tissue specificity and developmental and postnatal regulation. Am. J. Physiol. 1998;275:1265–1273. doi: 10.1152/ajpregu.1998.275.4.R1265. PubMed DOI
Sharma M., Kambadur R., Matthews K.G., Somers W.G., Devlin G.P., Conaglen J.V., Fowke P.J., Bass J.J. Myostatin, a Transforming Growth Factor-Beta Superfamily Member, Is Expressed in Heart Muscle and Is Upregulated in Cardiomyocytes After Infarct. J. Cell. Physiol. 1999;180:1–9. doi: 10.1002/(SICI)1097-4652(199907)180:1<1::AID-JCP1>3.0.CO;2-V. PubMed DOI
Rodgers B.D., Weber G.M., Sullivan C.V., Levine M.A. Isolation and Characterization of Myostatin Complementary Deoxyribonucleic Acid Clones from Two Commercially Important Fish: Oreochromis mossambicusand Morone chrysops. Endocrinology. 2001;142:1412–1418. doi: 10.1210/endo.142.4.8097. PubMed DOI
Radaelli G., Rowlerson A., Mascarello F., Patruno M., Funkenstein B. Myostatin Precursor is Present in Several Tissues in Teleost Fish: A Comparative Immunolocalization Study. Cell Tissue Res. 2003;311:239–250. doi: 10.1007/s00441-002-0668-y. PubMed DOI
Carlson C.J., Booth F.W., Gordon S.E. Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading. Am. J. Physiol. 1999;277:601–606. doi: 10.1152/ajpregu.1999.277.2.R601. PubMed DOI
Campbell J.W., Aster P.L., Vorhaben J.E. Mitochondrial ammoniagenesis in liver of the channel catfish Ictalurus punctatus. Am. J. Physiol. 1983;244:R709–R717. doi: 10.1152/ajpregu.1983.244.5.R709. PubMed DOI
Ip Y.K., Chew S.F. Ammonia production, excretion, toxicity, and defense in fish: A review. Front. Physiol. 2010;1:134. doi: 10.3389/fphys.2010.00134. PubMed DOI PMC
Campbell J.W., Vorhaben J.E. Avian Mitochondrial Glutamine Metabolism. J. Biol. Chem. 1976;251:781–786. PubMed
Aoki T.T., Brennan M.F., Fitzpatrick G.F., Knight D.C. Leucine Meal Increases Glutamine and Total Nitrogen Release from Forearm Muscle. J. Clin. Investig. 1981;68:1522–1528. doi: 10.1172/JCI110406. PubMed DOI PMC
Cooper A.J. 13N as a Tracer for Studying Glutamate Metabolism. Neurochem. Int. 2011;59:456–464. doi: 10.1016/j.neuint.2010.11.011. PubMed DOI PMC
Smith D.D., Campbell J.W. Distribution of glutamine synthetase and carbamoyl-phosphate synthetase I in vertebrate liver. Proc. Natl. Acad. Sci. USA. 1988;85:160–164. doi: 10.1073/pnas.85.1.160. PubMed DOI PMC
Randall D.J., Wood C.M., Perry S.F., Bergman H., Maloiy G.M., Mommsen T.P., Wright P.A. Urea excretion as a strategy for survival in a fish living in a very alkaline environment. Nature. 1989;337:165–166. doi: 10.1038/337165a0. PubMed DOI
Walsh P.J., Danulat E., Mommsen T.P. Variation in urea excretion in the gulf toadfish Opsanus beta. Mar. Biol. 1990;106:323–328. doi: 10.1007/BF01344308. DOI
Walsh P., Milligan C. Effects of feeding and confinement on nitrogen metabolism and excretion in the gulf toadfish Opsanus beta. J. Exp. Biol. 1995;198:1559–1566. PubMed
Ip Y.K., Zubaidah R.M., Liew P.C., Loong A.M., Hiong K.C., Wong W.P., Chew S.F. African sharptooth catfish Clarias gariepinus does not detoxify ammonia to urea or amino acids but actively excretes ammonia during exposure to environmental ammonia. Physiol. Biochem. Zool. 2004;77:242–254. doi: 10.1086/383499. PubMed DOI
Blair S.D., Wilkie M.P., Edwards S.L. Rh glycoprotein immunoreactivity in the skin and its role in extrabranchial ammonia excretion by the sea lamprey (Petromyzon marinus) in fresh water. Can. J. Zool. 2017;95:95–105. doi: 10.1139/cjz-2016-0120. DOI
Evans D.H., Piermarini P.M., Choe K.P. The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol. Rev. 2005;85:97–177. doi: 10.1152/physrev.00050.2003. PubMed DOI
Goldstein L., Claiborne J.B., Evans D.E. Ammonia excretion by the gills of two marine teleost fish: The importance of NH4+ permeance. J. Exp. Zool. 1982;219:395–397. doi: 10.1002/jez.1402190317. PubMed DOI
Danulat E., Kempe S. Nitrogenous waste excretion and accumulation of urea and ammonia inChalcalburnus tarichi (Cyprinidae), endemic to the extremely alkaline Lake Van (Eastern Turkey) Fish Physiol. Biochem. 1992;9:377–386. doi: 10.1007/BF02274218. PubMed DOI
Wright P.A., Wood C.M. A New Paradigm for Ammonia Excretion in Aquatic Animals: Role of Rhesus (Rh) Glycoproteins. J. Exp. Biol. 2009;212:2303–2312. doi: 10.1242/jeb.023085. PubMed DOI
Maetz J. Na+/NH4+, Na+/H+ Exchanges and NH3 Movement Across the Gill of Carassius Auratus. J. Exp. Biol. 1973;58:255–275.
Planelles G. Ammonium Homeostasis and Human Rhesus Glycoproteins. Nephron. Physiol. 2007;105:11–17. doi: 10.1159/000096979. PubMed DOI
Nakada T., Westhoff C.M., Kato A., Hirose S. Ammonia secretion from fish gill depends on a set of Rh glycoproteins. FASEB J. 2007;21:1067–1074. doi: 10.1096/fj.06-6834com. PubMed DOI
Nawata C.M., Wood C.M. mRNA expression analysis of the physiological responses to ammonia infusion in rainbow trout. J. Comp. Physiol. B. 2009;179:799–810. doi: 10.1007/s00360-009-0361-5. PubMed DOI
Egnew N., Renukdas N., Ramena Y., Yadav A.K., Kelly A.M., Lochmann R.T., Sinha A.K. Physiological insights into largemouth bass (Micropterus salmoides) survival during long-term exposure to high environmental ammonia. Aquat. Toxicol. 2019;207:72–82. doi: 10.1016/j.aquatox.2018.11.027. PubMed DOI
Braun M.H., Steele S.L., Perry S.F. The responses of zebrafish (Danio rerio) to high external ammonia and urea transporter inhibition: Nitrogen excretion and expression of rhesus glycoproteins and urea transporter proteins. J. Exp. Biol. 2009;212:3846–3856. doi: 10.1242/jeb.034157. PubMed DOI
Chen X.L., Zhang B., Chng Y.R., Ong J.L.Y., Chew S.F., Wong W.P., Lam S.H., Nakada T., Ip Y.K. Ammonia exposure affects the mRNA and protein expression levels of certain Rhesus glycoproteins in the gills of climbing perch. J. Exp. Biol. 2017;220:2916–2931. doi: 10.1242/jeb.157123. PubMed DOI
Tsui T.K.N., Hung C.Y.C., Nawata C.M., Wilson J.M., Wright P.A., Wood C.M. Ammonia transport in cultured gill epithelium of freshwater rainbow trout: The importance of Rhesus glycoproteins and the presence of an apical Na+/NH4+ exchange complex. J. Exp. Biol. 2009;212:878–892. doi: 10.1242/jeb.021899. PubMed DOI
Iwata K., Deguchi M. Metabolic Fate and Distribution of 15 N-Ammonia in an Ammonotelic Amphibious Fish, Periophthalmus modestus, Following Immersion in 15 N-Ammonium Sulfate: A Long Term Experiment. Zool. Sci. 1995;12:175–184. doi: 10.2108/zsj.12.175. DOI
Wright P.A., Steele S.L., Huitema A., Bernier N.J. Induction of Four Glutamine Synthetase Genes in Brain of Rainbow Trout in Response to Elevated Environmental Ammonia. J. Exp. Biol. 2007;210:2905–2911. doi: 10.1242/jeb.003905. PubMed DOI
Wicks B.J., Randall D.J. The effect of feeding and fasting on ammonia toxicity in juvenile rainbow trout, Oncorhynchus mykiss. Aquat. Toxicol. 2002;59:71–82. doi: 10.1016/S0166-445X(01)00237-5. PubMed DOI
Banerjee B., Koner D., Bhuyan G., Saha N. Differential Expression of Multiple Glutamine Synthetase Genes in Air-Breathing Magur Catfish, Clarias magur and Their Induction Under Hyper-Ammonia Stress. Gene. 2018;671:85–95. doi: 10.1016/j.gene.2018.05.111. PubMed DOI
Veauvy C.M., McDonald M.D., Van Audekerke J., Vanhoutte G., Van Camp N., Van der Linden A., Walsh P.J. Ammonia Affects Brain Nitrogen Metabolism but Not Hydration Status in the Gulf Toadfish (Opsanus Beta) Aquat. Toxicol. 2005;74:32–46. doi: 10.1016/j.aquatox.2005.05.003. PubMed DOI
Takahashi H., Koehler R.C., Brusilow S.W., Traystman R.J. Inhibition of brain glutamine accumulation prevents cerebral edema in hyperammonemic rats. Am. J. Physiol. 1991;261:825–829. doi: 10.1152/ajpheart.1991.261.3.H825. PubMed DOI
Clemmesen J.O., Larsen F.S., Kondrup J., Hansen B.A., Ott P. Cerebral herniation in patients with acute liver failure is correlated with arterial ammonia concentration. Hepatology. 1999;29:648–653. doi: 10.1002/hep.510290309. PubMed DOI
Dasarathy S. Consilience in Sarcopenia of Cirrhosis. J. Cachexia Sarcopenia Muscle. 2012;3:225–237. doi: 10.1007/s13539-012-0069-3. PubMed DOI PMC
Ganda O.P., Ruderman N.B. Muscle nitrogen metabolism in chronic hepatic insufficiency. Metabolism. 1976;25:427–435. doi: 10.1016/0026-0495(76)90075-5. PubMed DOI
Stern R.A., Dasarathy S., Mozdziak P.E. Ammonia elicits a different myogenic response in avian and murine myotubes. In Vitro Cell Dev. Biol. Anim. 2017;53:99–110. doi: 10.1007/s11626-016-0088-z. PubMed DOI
Dasarathy S., Hatzoglou M. Hyperammonemia and Proteostasis in Cirrhosis. Curr. Opin. Clin. Nutr. Metab. Care. 2018;21:30–36. doi: 10.1097/MCO.0000000000000426. PubMed DOI PMC
Beker A., Vanhooser S.L., Swartzlander J.H., Teeter R.G. Atmospheric Ammonia Concentration Effects on Broiler Growth and Performance. J. Appl. Poult. Res. 2004;13:5–9. doi: 10.1093/japr/13.1.5. DOI
Zhang J., Li C., Tang X., Lu Q., Sa R., Zhang H. High Concentrations of Atmospheric Ammonia Induce Alterations in the Hepatic Proteome of Broilers (Gallus gallus): An iTRAQ-Based Quantitative Proteomic Analysis. PLoS ONE. 2015;10:e0123596. doi: 10.1371/journal.pone.0123596. PubMed DOI PMC
Smart G.R. Investigations of the toxic mechanisms of ammonia to fish-gas exchange in rainbow trout (Salmo gairdneri) exposed to acutely lethal concentrations. J. Fish Biol. 1978;12:93–104. doi: 10.1111/j.1095-8649.1978.tb04155.x. DOI
Randall D.J., Tsui T.K. Ammonia Toxicity in Fish. Mar. Pollut. Bull. 2002;45:17–23. doi: 10.1016/S0025-326X(02)00227-8. PubMed DOI
Suski C.D., Kieffer J.D., Killen S.S., Tufts B.L. Sub-lethal ammonia toxicity in largemouth bass. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2007;146:381–389. doi: 10.1016/j.cbpa.2006.11.005. PubMed DOI
Robinette H.R. Effect of Selected Sublethal Levels of Ammonia on the Growth of Channel Catfish (Ictalurus punctatus) Progress. Fish Cult. 1976;38:26–29. doi: 10.1577/1548-8659(1976)38[26:EOSSLO]2.0.CO;2. DOI
Smart G. The effect of ammonia exposure on gill structure of the rainbow trout (Salmo gairdneri) J. Fish Biol. 1976;8:471–475. doi: 10.1111/j.1095-8649.1976.tb03990.x. DOI
Daoust P.Y., Ferguson H.W. The pathology of chronic ammonia toxicity in rainbow trout, Salmo gairdneri Richardson. J. Fish Dis. 1984;7:199–205. doi: 10.1111/j.1365-2761.1984.tb00924.x. DOI
Ferguson R.I., Ashmore P.E., Ashworth P.J., Paola C., Prestegaard K.L. Measurements in a Braided River chute and lobe: 1. Flow pattern, sediment transport, and channel change. Water Resour. Res. 1992;28:1877–1886. doi: 10.1029/92WR00700. DOI
Tng Y.Y.M., Chew S.F., Wee N.L.J., Wong F.K., Wong W.P., Tok C.Y., Ip Y.K. Acute ammonia toxicity and the protective effects of methionine sulfoximine on the swamp eel, Monopterus albus. J. Exp. Zool. A Ecol. Genet. Physiol. 2009;311:676–688. doi: 10.1002/jez.555. PubMed DOI
Binstock L., Lecar H. Ammonium Ion Currents in the Squid Giant Axon. J. Gen. Physiol. 1969;53:342–361. doi: 10.1085/jgp.53.3.342. PubMed DOI PMC
Cooper A.J., Plum F. Biochemistry and Physiology of Brain Ammonia. Physiol. Rev. 1987;67:440–519. doi: 10.1152/physrev.1987.67.2.440. PubMed DOI
Stern R.A., Ashwell C.M., Dasarathy S., Mozdziak P.E. The effect of hyperammonemia on myostatin and myogenic regulatory factor gene expression in broiler embryos. Animal. 2015;9:992–999. doi: 10.1017/S1751731115000117. PubMed DOI PMC
McKenzie D.J., Shingles A., Taylor E.W. Sub-lethal plasma ammonia accumulation and the exercise performance of salmonids. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2003;135:515–526. doi: 10.1016/S1095-6433(03)00116-8. PubMed DOI
Dosdat A., Person-Le Ruyet J., Covès D., Dutto G., Gasset E., Le Roux A., Lemarié G. Effect of chronic exposure to ammonia on growth, food utilisation and metabolism of the European sea bass (Dicentrarchus labrax) Aquat. Living Resour. 2003;16:509–520. doi: 10.1016/j.aquliv.2003.08.001. DOI