THE ROLE OF METHYLAMINES IN MAINTENANCE OF THE OSMOTIC HOMEOSTASIS OF CARTILAGINOUS FISHES AND COELACANTHS
Abstract and keywords
Abstract (English):
This article contains the review of existing literature considering roles methylamines in cartilaginous fishes and coelacanths, emphasizing their osmoregulatory role as “compatible osmolytes” — substances preserving biomolecules structure and function under high salinities. Methylamines presented are: trimethylamine oxide (TMAO), betaine, glycerophosphoholine (GPC) and sarcosine. Methylamines are usually used for osmoregulation by fishes accumulating urea in their bodies: those are marine cartilaginous fishes, elasmobranchs and chimaeras, and also latimeria (the only extant coelacanth). The reason is methylamines are most effective in opposing deleterious effect of urea on proteins. The main compatible osmolyte in marine elasmobranchs is TMAO, some of them also use betaine. For latimeria the literature contains data on the use of TMAO as main osmolyte. Freshwater elasmobranchs, Potamotrigonidae, do not accumulate urea or any methylamines in their bodies. Euryhaline elasmobranchs, such as Carcharhinus leucas, Dasyatis sabina, Himantura signifer, accumulate urea and methylamines, mainly TMAO, in seawater, but not in freshwater. GPC plays only minor role as osmolyte in fishes considered, and sarcosine is one of the main osmolythes in some skates and rays. Methylamines such as TMAO also function as depth and heat protectors, promote correct folding of many proteins. The metabolic scheme of methylamines in fish is also presented. Cartilaginous fishes have different capability of synthesizing TMAO from TMA, but all of them can synthesize betaine from choline. Latimeria seem to be capable of synthesizing TMAO. Dipnoan fishes accumulate urea under drought conditions but are not likely to accumulate methylamines as they do need inhibition of protein functions for their dormant state.

Keywords:
osmotic homeostasis, fish, osmolytes, methylamines, TMAO, betaine, sarcosine, glycerophosphoholine
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References

1. Filippova A.E. Rol' svobodnyh aminokislot v podderzhanii osmoticheskogo gomeostaza u ryb // Trudy IBVV im. I.D. Papanina RAN. 2023. vyp. 104(107). S. 30–49. DOI:https://doi.org/10.47021/0320-3557-2024-30-49.

2. An N., Wang H., Li J. et al. The characteristics of trimethylamine N-oxide content in different classes of marine animals over the coastal and offshore areas of China // Mar Pollut Bull. 2023. Vol. 197. P. 115706. DOI:https://doi.org/10.1016/j.marpolbul.2023.115706.

3. Anderson W.G., Nawata C.M., Wood C.M. et al. Body fluid osmolytes and urea and ammonia flux in the colon of two chondrichthyan fishes, the ratfish, Hydrolagus colliei, and spiny dogfish, Squalus acanthias // Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2012. Vol. 161. № 1. P. 27–35. DOI:https://doi.org/10.1016/j.cbpa.2011.08.017.

4. Andreeva A.M. Structural and functional organization of fish blood proteins. New York: Nova Science Publishers, Inc., 2012. 188 p.

5. Arakawa T., Timasheff S.N. Preferential interactions of proteins with solvent components in aqueous amino acid solutions // Arch Biochem Biophys. 1983. Vol. 224. № 1. P. 169–177. DOI:https://doi.org/10.1016/0003-9861(83)90201-1.

6. Arakawa T., Timasheff S.N. The stabilization of proteins by osmolytes // Biophys. J. 1985. Vol. 47. P. 411–414. DOI:https://doi.org/10.1016/S0006-3495(85)83932-1.

7. Athawale M.V., Dordick J.S., Garde S. Osmolyte trimethylamine-N-oxide does not affect the strength of hydrophobic interactions: origin of osmolyte compatibility // Biophys. J. 2005. Vol. 89. № 2. P. 858–866. DOI:https://doi.org/10.1529/biophysj.104.056671.

8. Baker J.R., Struempler A., Chaykin S. A comparative study of trimethylamine-N-oxide biosynthesis // Biochim. Biophys. Acta. 1963. Vol. 71. P. 58–64. DOI:https://doi.org/10.1016/0006-3002(63)90985-5.

9. Ballantyne J.S. Jaws: The inside story. The metabolism of elasmobranch fishes // Comp. Biochem. Physiol. B. 1997. Vol. 118. № 4. P. 703–742. DOI:https://doi.org/10.1016/s0305-0491(97)00272-1.

10. Ballantyne J.S. Some of the most interesting things we know, and don't know, about the biochemistry and physiology of elasmobranch fishes (sharks, skates and rays) // Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 2016. Vol. 199. P. 21–28. DOI:https://doi.org/10.1016/j.cbpb.2016.03.005.

11. Ballantyne J.S., Fraser D.I. 4 — Euryhaline Elasmobranchs // Fish Physiol. 2012. Vol. 32. P. 125–198. DOI:https://doi.org/10.1016/B978-0-12-396951-4.00004-9.

12. Ballantyne J.S., Moon T.W. Solute effects on mitochondria from an elasmobranch (Raja erinacea) and a teleost (Pseudopleuronectes americanus) // J. Exp. Zool. 1986a. Vol. 239. № 3. P. 319–328. DOI:https://doi.org/10.1002/jez.1402390303.

13. Ballantyne J.S., Moon T.W. The effects of urea, trimethylamine oxide and ionic strength on the oxidation of acyl carnitines by mitochondria isolated from the liver of the Little Skate Raja erinacea // J. Comp. Physiol. B. 1986b. Vol. 156. P. 845–851. DOI:https://doi.org/10.1007/BF00694260.

14. Ballantyne J.S., Moyes C., Moon T.W. Osmolarity affects oxidation of sarcosine by isolated hepatocytes and mitochondria from a euryhaline elasmobranch // J. Exp. Zool. 1986. Vol. 238. P. 267–271. DOI:https://doi.org/10.1002/jez.1402380217.

15. Barton K.N., Buhr M.M., Ballantyne J.S. Effects of urea and trimethylamine N-oxide on fluidity of liposomes and membranes of an elasmobranch // Am. J. Physiol. 1999. Vol. 276. № 2. P. R397–R406. DOI:https://doi.org/10.1152/ajpregu.1999.276.2.R397.

16. Bedford J.J. The composition of the fluid compartments of two condrichthyans, Callorhyncus milli and Squalus acanthias // Comp. Biochem. Physiol. A. 1983. Vol. 76. P. 75–80. DOI:https://doi.org/10.1016/0300-9629(83)90295-5.

17. Bedford J.J., Harper J.L., Leader J.P. et al. Betaine is the principal counteracting osmolyte in tissues of the elephant fish, Callorhincus millii (Elasmobranchii, Holocephali) // Comp. Biochem. Physiol. B. 1998a. Vol. 119. P. 521–526.

18. Bedford J., Harper J., Leader J., Smith R.A.J. Identification and measurement of methylamines in elasmobranch tissues using proton nuclear magnetic resonance (1H-NMR) spectroscopy // J. Comp. Physiol. B. 1998b. Vol. 168. P. 123–131. DOI:https://doi.org/10.1007/s003600050128.

19. Bockus A.B. A study of the regulatory and environmental factors affecting trimethylamine oxide accumulation in marine organisms // Open Access Dissertations. University of Rhode Island. 2016. Paper 513. 158 p. DOI:https://doi.org/10.23860/diss-bockus-abigail-2016.

20. Bockus A.B., Seibel B.A. Trimethylamine oxide accumulation as a function of depth in Hawaiian mid-water fishes // Deep Sea Res. Part I. 2016. Vol. 112. P. 37–44. DOI:https://doi.org/10.1016/j.dsr.2016.03.005.

21. Bockus A.B., Seibel B.A. Synthetic capacity does not predict elasmobranchs' ability to maintain trimethylamine oxide without a dietary contribution // Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2018. Vol. 217. P. 35–42. DOI:https://doi.org/10.1016/j.cbpa.2017.12.008.

22. Bolen D.W. Protein stabilization by naturally occurring osmolytes // Methods Mol. Biol. 2001. Vol. 168. P. 17–36. DOI:https://doi.org/10.1385/1-59259-193-0:017.

23. Bolen D.W., Rose G.D. Structure and energetics of the hydrogen-bonded backbone in protein folding // Annu. Rev. Biochem. 2008. Vol. 77. P. 339–362. DOI:https://doi.org/10.1146/annurev.biochem.77.061306.131357.

24. Boyd T.A., Cha C.J., Forster R.P., Goldstein L. Free amino acids in tissues of the skate Raja erinacea and the stingray Dasyatis sabina: effects of environmental dilution // J. Exp. Zool. 1977. Vol. 199. № 3. P. 435–442. DOI:https://doi.org/10.1002/jez.1401990318.

25. Burg M.B., Kwon E.D., Peters E.M. Glycerophosphocholine and betaine counteract the effect of urea on pyruvate kinase // Kidney Int. Suppl. 1996. Vol. 57. P. S100–S104.

26. Burg M.B., Peters E.M. Effects of glycine betaine and glycerophosphocholine on thermal stability of ribonuclease // Am. J. Physiol. 1998. Vol. 274. № 4. P. F762–F765. DOI:https://doi.org/10.1152/ajprenal.1998.274.4.F762.

27. Cohen J.J., Krupp M.A., Chidsey C.A. 3rd. Renal conservation of trimethylamine oxide by the spiny dogfish, Squalus acanthias // Am. J. Physiol. 1958. Vol. 194. № 2. P. 229–235. DOI:https://doi.org/10.1152/ajplegacy.1958.194.2.229.

28. Cooper A., Morris S. Osmotic, ionic and haematological response of the Port Jackson shark Heterodontus portusjacksoni and the common stingaree Trygonoptera testacea upon exposure to diluted seawater // Mar. Biol. 1998. Vol. 132. P. 29–42. DOI:https://doi.org/10.1007/s002270050369.

29. Deck C.A., Bockus A.B., Seibel B.A., Walsh P.J. Effects of short-term hyper- and hypo-osmotic exposure on the osmoregulatory strategy of unfed North Pacific spiny dogfish (Squalus suckleyi) // Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2016. Vol. 193. P. 29–35. DOI:https://doi.org/10.1016/j.cbpa.2015.12.004.

30. Doolittle R.F., Thomas C., Stone W. Jr. Osmotic pressure and aqueous humor formation in dogfish // Science. 1960. Vol. 132. № 3418. P. 36–37. DOI:https://doi.org/10.1126/science.132.3418.36.

31. Dyer W.J. Amines in fish muscle. VI. Trimethylamine oxide content of fish and marine invertebrates // J. Fish. Res. Bd. Can. 1952. Vol. 8. № 5. P. 314–324. DOI:https://doi.org/10.1139/f50-020.

32. Edwards S.L., Marshall W.S. Principles and patterns of osmoregulation and euryhalinity in fishes // Fish Physiol. 2012. Vol. 32. P. 1–44. DOI:https://doi.org/10.1016/B978-0-12-396951-4.00001-3.

33. Evans D.H. Osmotic, ionic and nitrogenous-waste balance | Osmoregulation in Fishes: An Introduction // Encyclopedia of Fish Physiology. 2011. Vol. 2. P. 1348–1353. DOI:https://doi.org/10.1016/B978-0-12-374553-8.00210-0.

34. Fedotova M. Compatible osmolytes-bioprotectants: is there a common link between their hydration and their protective action under abiotic stresses? // J. Mol. Liq. 2019. Vol. 292. P. 111339. DOI:https://doi.org/10.1016/j.molliq.2019.111339.

35. Fedotova M., Kruchinin S. Chuev G. Hydration structure of osmolyte TMAO: concentration/pressure-induced response // New J. Chem. 2017. Vol. 41. P. 1219–1228. DOI:https://doi.org/10.1039/C6NJ03296F.

36. Felitsky D.J., Cannon J.G., Capp M.W. et al. The exclusion of glycine betaine from anionic biopolymer surface: why glycine betaine is an effective osmoprotectant but also a compatible solute // Biochemistry. 2004. Vol. 43. № 46. P. 14732–14743. DOI:https://doi.org/10.1021/bi049115w.

37. Figueroa-Soto C.G., Valenzuela-Soto E.M. Glycine betaine rather than acting only as an osmolyte also plays a role as regulator in cellular metabolism // Biochimie. 2018. Vol. 147. P. 89–97. DOI:https://doi.org/10.1016/j.biochi.2018.01.002.

38. Forster R.P., Goldstein L. Intracellular osmoregulatory role of amino acids and urea in marine elasmobranchs // Am. J. Physiol. 1976. Vol. 230. № 4. P. 925–931. DOI:https://doi.org/10.1152/ajplegacy.1976.230.4.925.

39. Gillett M.B., Suko J.R., Santoso F.O. Yancey P.H. Elevated levels of trimethylamine oxide in muscles of deep‐sea gadiform teleosts // J. Exp. Zool. 1997. Vol. 279. P. 386–391.

40. Goldstein L., Dewitt-Harley S. Trimethylamine oxidase of nurse shark liver and its relation to mammalian mixed function amine oxidase // Comp. Biochem. Physiol B. 1973. Vol. 45. № 4. P. 895–903. DOI:https://doi.org/10.1016/0305-0491(73)90150-8.

41. Goldstein L., Forster R.P. Osmoregulation and urea metabolism in the little skate Raja erinacea // Am. J. Physiol. 1971. Vol. 220. № 3. P. 742–746. DOI:https://doi.org/10.1152/ajplegacy.1971.220.3.742.

42. Goldstein L., Funkhouser D. Biosynthesis of trimethylamine oxide in the nurse shark, Ginglymostoma cirratum // Comp. Biochem. Physiol. A. Comp. Physiol. 1972. Vol. 42. № 1. P. 51–57. DOI:https://doi.org/10.1016/0300-9629(72)90365-9.

43. Goldstein L., Harley-DeWitt S., Forster R.P. Activities of ornithine-urea cycle enzymes and of trimethylamine oxidase in the coelacanth, Latimeria chalumnae // Comp. Biochem. Physiol. B. 1973. Vol. 44. № 2. P. 357–362. DOI:https://doi.org/10.1016/0305-0491(73)90008-4.

44. Goldstein L., Hartman S.C., Forster R.P. On the origin of trimethylamine oxide in the spiny dogfish, Squalus acanthias // Comp. Biochem. Physiol. 1967. Vol. 21. № 3. P. 19–22. DOI:https://doi.org/10.1016/0010-406x(67)90467-7.

45. Goldstein L., Kleinzeller A. Cell volume regulation in lower vertebrates // Curr. Top. Membr. Transp. 1987. Vol. 30. P. 181–203.

46. Goldstein L., Oppelt W.W., Maren T.H. Osmotic regulation and urea metabolism in the lemon shark Negaprion brevirostris // Am. J. Physiol.. 1968. Vol. 215. № 6. P. 1493–1497. DOI:https://doi.org/10.1152/ajplegacy.1968.215.6.1493

47. Goldstein L., Palatt P.J. Trimethylamine oxide excretion rates in elasmobranchs // Am. J. Physiol. 1974. Vol. 227. № 6. P. 1268–1272. DOI:https://doi.org/10.1152/ajplegacy.1974.227.6.1268

48. Griffith R.W., Pang P.K.T., Srivastava A.K., Pickford G.E. Serum composition of freshwater stingrays (Potamotrygonidae) adapted to freshwater and dilute seawater // Biol. Bull. 1973. Vol. 144. № 2. P. 304–320. DOI:https://doi.org/10.2307/1540010.

49. Griffith R.W., Umminger B.L., Grant B.F., Pang P.K., Pickford G.E. Serum composition of the coelacanth, Latimeria chalumnae Smith // J. Exp. Zool. 1974. Vol.187. № 1. P. 87–102. DOI:https://doi.org/10.1002/jez.1401870111.

50. Groninger H.S. The occurrence and significance of trimethylamine oxide in marine animals // US Fish and Wildlife Service. 1959. Vol. 569. 22 p.

51. Hammerschlag N. Osmoregulation in elasmobranchs: A review for fish biologists, behaviourists and ecologists // Mar. Freshw. Behav. Physiol. 2006. Vol. 39. P. 209–228. DOI:https://doi.org/10.1080/10236240600815820.

52. Kelly R.H., Yancey P.H. High contents of trimethylamine oxide correlating with depth in deep-sea teleost fishes, skates, and decapod crustaceans // Biol. Bull. 1999. Vol. 196. № 1. P. 18–25. DOI:https://doi.org/10.2307/1543162.

53. Kleinzeller A. Trimethylamine oxide and the maintenance of volume of dogfish shark rectal gland cells // J. Exp. Zool. 1985. Vol. 236. № 1. P. 11–17. DOI:https://doi.org/10.1002/jez.1402360103.

54. Kolhatkar A., Robertson C.E., Thistle M.E. et al. Coordination of chemical (trimethylamine oxide) and molecular (heat shock protein 70) chaperone responses to heat stress in elasmobranch red blood cells // Physiol. Biochem. Zool. 2014. Vol. 87. № 5. P. 652–662. DOI:https://doi.org/10.1086/676831.

55. Koomoa D.L., Musch M.W., MacLean A.V., Goldstein L. Volume-activated trimethylamine oxide efflux in red blood cells of spiny dogfish (Squalus acanthias) // Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001. Vol. 281. № 3. P. R803–R810. DOI:https://doi.org/10.1152/ajpregu.2001.281.3.R803.

56. Kültz D., Li J., Paguio D., Pham T., Eidsaa M., Almaas E. Population-specific renal proteomes of marine and freshwater three-spined sticklebacks // J. Proteomics. 2016. Vol. 135. P. 112–131. DOI:https://doi.org/10.1016/j.jprot.2015.10.002.

57. Kumar N., Kishore N. Mechanistic insights into osmolyte action in protein stabilization under harsh conditions: N-methylacetamide in glycine betaine-urea mixture // Chem. Phys. 2014. Vol. 443. P. 133–141. DOI:https://doi.org/10.1016/j.chemphys.2014.09.010.

58. Kumar R. Role of naturally occurring osmolytes in protein folding and stability // Arch. Biochem. Biophys. 2009. Vol. 491. P. 1–6. DOI:https://doi.org/10.1016/j.abb.2009.09.007.

59. Kumar R., Serrette J.M., Khan S.H. et al. Effects of different osmolytes on the induced folding of the N-terminal activation domain (AF1) of the glucocorticoid receptor // Arch. Biochem. Biophys. 2007. Vol. 465. P. 452–460. DOI: 0.1016/j.abb.2007.06.019.

60. Kumar R., Serrette J.M., Thompson E.B. Osmolyte-induced folding enhances tryptic enzyme activity // Arch. Biochem. Biophys. 2005. Vol. 436. № 1. P. 78–82. DOI:https://doi.org/10.1016/j.abb.2005.01.008.

61. Laxson C.J., Condon N.E., Drazen J.C., Yancey P.H. Decreasing urea∶trimethylamine N-oxide ratios with depth in chondrichthyes: a physiological depth limit? // Physiol. Biochem. Zool. 2011. Vol. 84. № 5. P. 494–505. DOI:https://doi.org/10.1086/661774

62. Leech A.R., Goldstein L. β‐Alanine oxidation in the liver of the little skate, Raja erinacea // J. Exp. Zool. 1983. Vol. 225. P. 9–14.

63. Liao Y.T., Manson A.C., DeLyser M.R. et al. Trimethylamine N-oxide stabilizes proteins via a distinct mechanism compared with betaine and glycine // Proc. Natl. Acad. Sci. USA. 2017. Vol. 114. № 10. P. 2479–2484. DOI:https://doi.org/10.1073/pnas.1614609114.

64. Lin T.Y., Timasheff S.N. Why do some organisms use a urea-methylamine mixture as osmolyte? Thermodynamic compensation of urea and trimethylamine N-oxide interactions with protein // Biochemistry. 1994. Vol. 33. № 42. P. 12695–12701. DOI:https://doi.org/10.1021/bi00208a021.

65. Lutz P.L., Robertson J.D. Osmotic constituents of the coelacanth, Latimeria chalumnae Smith // Biol. Bull. 1971. Vol. 141. P. 553–560.

66. MacLellan R.J., Tunnah L., Barnett D. et al. Chaperone roles for TMAO and HSP70 during hyposmotic stress in the spiny dogfish shark (Squalus acanthias) // J. Comp. Physiol. B. 2015. Vol. 185. № 7. P. 729–740. DOI:https://doi.org/10.1007/s00360-015-0916-6.

67. Mandrup-Poulsen J. Changes in selected blood serum constituents, as a function of salinity variations, in the marine elasmobranch, Sphyrna tiburo // Comp. Biochem. Physiol. A. 1981. Vol. 70. P. 127–131.

68. Mashino T., Fridovich I. Effects of urea and trimethylamine-N-oxide on enzyme activity and stability // Arch. Biochem. Biophys. 1987. Vol. 258. № 2. P. 356–360. DOI:https://doi.org/10.1016/0003-9861(87)90355-9.

69. Nasralla M., Laurent H., Alderman O.L.G. et al. Trimethylamine-N-oxide depletes urea in a peptide solvation shell // Proc. Natl. Acad. Sci. USA. 2024. Vol. 121. № 14. P. e2317825121. DOI:https://doi.org/10.1073/pnas.2317825121.

70. Norris E.R., Benoit G.J. Studies on trimethylamine oxide: I. Occurrence of trimethylamine oxide in marine organisms // J. Biol. Chem. 1945. Vol. 158. P. 433–438. DOI:https://doi.org/10.1016/S0021-9258(18)43148-1.

71. Palmer H.R., Bedford J.J., Leader J.P., Smith R.A. 31P and 1H NMR studies of the effect of the counteracting osmolyte trimethylamine-N-oxide on interactions of urea with ribonuclease A // J. Biol. Chem. 2000. Vol. 275. № 36. P. 27708–27711. DOI:https://doi.org/10.1074/jbc.M003550200.

72. Pillans R.D., Anderson W.G., Good J.P. et al. Plasma and erythrocyte solute properties of juvenile bull sharks, Carcharhinus leucas, acutely exposed to increasing environmental salinity // J. Exp. Mar. Biol. Ecol. 2006. Vol. 331. P. 145–157. DOI:https://doi.org/10.1016/j.jembe.2005.10.013.

73. Pillans R.D., Good J.P., Anderson W.G. et al. Freshwater to seawater acclimation of juvenile bull sharks (Carcharhinus leucas): plasma osmolytes and Na+/K+-ATPase activity in gill, rectal gland, kidney and intestine // J. Comp. Physiol. B. 2005. Vol. 175. № 1. P. 37–44. DOI:https://doi.org/10.1007/s00360-004-0460-2.

74. Pollard A., Wyn Jones R.G. Enzyme activities in concentrated solutions of glycinebetaine and other solutes // Planta. 1979. Vol. 144. № 3. P. 291–298. DOI:https://doi.org/10.1007/BF00388772.

75. Read L.J. Urea and trimethylamine oxide levels in elasmobranch embryos // Biol. Bull. 1968. Vol. 135. № 3. P. 537–547. DOI:https://doi.org/10.2307/1539716.

76. Robertson J.D. Osmotic constitutents of the blood plasma and parietal muscle of Squalus acanthias L. // Biol. Bull. 1975. Vol. 148. № 2. P. 303–319. DOI:https://doi.org/10.2307/1540549.

77. Robertson J.D. Osmotic constituents of the blood-plasma and parietal muscle of Scyliorhinus canicula (L) // Comp. Biochem. Physiol. A. 1989. Vol. 93. P. 799–880. DOI:https://doi.org/10.1016/0300-9629(89)90504-5.

78. Rudolph A.S., Crowe J.H., Crowe L.M. Effects of three stabilizing agents — proline, betaine, and trehalose — on membrane phospholipids // Arch. Biochem. Biophys. 1986. Vol. 245. № 1. P. 134–143. DOI:https://doi.org/10.1016/0003-9861(86)90197-9.

79. Samerotte A.L., Drazen J.C., Brand G.L. et al. Correlation of trimethylamine oxide and habitat depth within and among species of teleost fish: an analysis of causation // Physiol. Biochem. Zool. 2007. Vol. 80. № 2. P. 197–208. DOI:https://doi.org/10.1086/510566

80. Samuelsson L.M., Bedford J.J., Smith R.A., Leader J.P. A comparison of the counteracting effects of glycine betaine and TMAO on the activity of RNase A in aqueous urea solution // Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2005. Vol. 141. № 1. P. 22–28. DOI:https://doi.org/10.1016/j.cbpb.2005.03.004.

81. Santoro M.M., Liu Y., Khan S.M. et al. Increased thermal stability of proteins in the presence of naturally occurring osmolytes // Biochemistry. 1992. Vol. 31. № 23. P. 5278–5283. DOI:https://doi.org/10.1021/bi00138a006.

82. Seibel B.A., Walsh P.J. Trimethylamine oxide accumulation in marine animals: relationship to acylglycerol storage // J. Exp. Biol. 2002. Vol. 205 (Pt 3). P. 297–306. DOI:https://doi.org/10.1242/jeb.205.3.297.

83. Shakhman Y., Shumilin I., Harries D. Urea counteracts trimethylamine N-oxide (TMAO) compaction of lipid membranes by modifying van der Waals interactions // J. Colloid Interface Sci. 2023. Vol. 629 (Pt A). P. 165–172. DOI:https://doi.org/10.1016/j.jcis.2022.08.123.

84. Schlenk D. Occurrence of flavin-containing monooxygenases in non-mammalian eukaryotic organisms // Comp. Biochem. Physiol. C. Pharmacol. Toxicol. Endocrinol. 1998. Vol. 121. P. 185–195. DOI:https://doi.org/10.1016/s0742-8413(98)10060-9.

85. Schlenk D., Li-Schlenk R. Characterization of liver flavin-containing monooxygenase of the dogfish shark (Squalus acanthias) and partial purification of liver flavin-containing monooxygenase of the silky shark (Carcharhinus falciformis) // Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 1994. Vol. 109. № 4. P. 655–664. DOI:https://doi.org/10.1016/0305-0491(94)90128-7.

86. Singh L.R., Poddar N.K., Dar T.A., Kumar R., Ahmad F. Protein and DNA destabilization by osmolytes: the other side of the coin // Life Sci. 2011. Vol. 88. P. 117–125. DOI:https://doi.org/10.1016/j.lfs.2010.10.020.

87. Somero G.N. Protons, osmolytes, and fitness of internal milieu for protein function // Am. J. Physiol. 1986. Vol. 251 (Pt 2). P. R197–R.213. DOI:https://doi.org/10.1152/ajpregu.1986.251.2.R197.

88. Stasiulewicz M., Panuszko A., Smiechowski M. et al. Effect of urea and glycine betaine on the hydration sphere of model molecules for the surface features of proteins // J. Mol. Liq. 2020. Vol. 324. P. 115090. DOI:https://doi.org/10.1016/j.molliq.2020.115090.

89. Steele S.L., Yancey P.H., Wright P.A. Dogmas and controversies in the handling of nitrogenous wastes: osmoregulation during early embryonic development in the marine little skate Raja erinacea; response to changes in external salinity // J. Exp. Biol. 2004. Vol. 207 (Pt 12). P. 2021–2031. DOI:https://doi.org/10.1242/jeb.00959.

90. Steele S.L., Yancey P.H., Wright P.A. The little skate Raja erinacea exhibits an extrahepatic ornithine urea cycle in the muscle and modulates nitrogen metabolism during low-salinity challenge // Physiol. Biochem. Zool. 2005. Vol. 78. № 2. P. 216–226. DOI:https://doi.org/10.1086/427052.

91. Street T.O., Bolen D.W., Rose G.D. A molecular mechanism for osmolyte-induced protein stability // Proc. Natl. Acad. Sci. USA. 2006. Vol. 103. № 38. P. 13997–14002. DOI:https://doi.org/10.1073/pnas.0606236103.

92. Su Z., Dias C. Individual and combined effects of urea and trimethylamine N-oxide (TMAO) on protein structures // J. Mol. Liq. 2019. Vol. 293. P. 111443. DOI:https://doi.org/10.1016/j.molliq.2019.111443.

93. Sulikowski J.A., Treberg J.R., Howell W.H. Fluid regulation and physiological adjustments in the winter skate, Leucoraja ocellata, following exposure to reduced environmental salinities // Environ. Biol. Fish. 2003. Vol. 66. № 4. P. 339–348. DOI:https://doi.org/10.1023/A:1023918231020.

94. Tam W.L., Wong W.P., Loong A.M. et al. The osmotic response of the Asian freshwater stingray (Himantura signifer) to increased salinity: a comparison with marine (Taeniura lymma) and Amazonian freshwater (Potamotrygon motoro) stingrays // J. Exp. Biol. 2003. Vol. 206 (Pt 17). P. 2931–2940. DOI:https://doi.org/10.1242/jeb.00510.

95. Thorson T.B. Freshwater stingrays, Potamotrygon spp.: failure to concentrate urea when exposed to saline medium // Life Sci. II. 1970. Vol. 9. № 15. P. 893–900. DOI:https://doi.org/10.1016/0024-3205(70)90059-7.

96. Thorson T.B., Cowan C.M., Watson D.E. Potamotrygon spp.: elasmobranchs with low urea content // Science. 1967. Vol. 158. № 3799. P. 375–377. DOI:https://doi.org/10.1126/science.158.3799.375.

97. Thorson T.B., Cowan C.M., Watson D.E. Body fluid solutes of juveniles and adults of the euryhaline bullshark Carcharinus leucas from freshwater and saline environments // Physiol. Zool. 1973. Vol. 46. № 1. P. 29–42. DOI:https://doi.org/10.1086/physzool.46.1.30152514.

98. Treberg J.R., Driedzic W.R. Elevated levels of trimethylamine oxide in deep-sea fish: evidence for synthesis and intertissue physiological importance // J. Exp. Zool. 2002. Vol. 293. № 1. P. 39–45. DOI:https://doi.org/10.1002/jez.10109.

99. Treberg J.R., Driedzic W.R. Maintenance and accumulation of trimethylamine oxide by winter skate (Leucoraja ocellata): reliance on low whole animal losses rather than synthesis // Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006. Vol. 291. № 6. P. R1790–R1798. DOI:https://doi.org/10.1152/ajpregu.00150.2006.

100. Treberg J.R., Driedzic W.R. The accumulation and synthesis of betaine in winter skate (Leucoraja ocellata) // Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2007. Vol. 147. № 2. P. 475–483. DOI:https://doi.org/10.1016/j.cbpa.2007.01.028.

101. Treberg J.R., Speers-Roesch B., Piermarini P.M., Ip Y.K., Ballantyne J.S., Driedzic W.R. The accumulation of methylamine counteracting solutes in elasmobranchs with differing levels of urea: a comparison of marine and freshwater species // J. Exp. Biol. 2006. Vol. 209 (Pt 5). P. 860–870. DOI:https://doi.org/10.1242/jeb.02055.

102. Velankar N.K., Govindan T.K. A preliminary study of the distribution of non-protein nitrogen in some marine fishes and invertebrates // Proc. Indian Acad. Sci. 1958. Vol. 47. P. 202–209. DOI:https://doi.org/10.1007/BF03051563.

103. Wilson E.D., McGuinn M.R., Goldstein L. Trimethylamine oxide transport across plasma membranes of elasmobranch erythrocytes // J. Exp. Zool. 1999. Vol. 284. № 6. P. 605–609. DOI:https://doi.org/10.1002/(sici)1097-010x(19991101)284:6<605::aid-jez1>3.0.co;2-7.

104. Yancey. P.H. Nitrogen compounds as osmolytes // Fish Physiol. 2001. Vol. 20. P. 309–341. DOI:https://doi.org/10.1016/S1546-5098(01)20010-7.

105. Yancey P.H. Organic osmotic effectors in cartilaginous fishes // Transport processes, iono- and osmoregulation (ed. by R. Gilles and M. Gilles-Baillien) Proceedings in Life Sciences. Berlin, Heidelberg: Springer, 1985. P. 424–436. DOI:https://doi.org/10.1007/978-3-642-70613-4_36.

106. Yancey P.H. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses // J. Exp. Biol. 2005. Vol. 208. P. 2819–2830. DOI:https://doi.org/10.1242/jeb.01730.

107. Yancey P.H., Blake W.R., Conley J. Unusual organic osmolytes in deep-sea animals: adaptations to hydrostatic pressure and other perturbants // Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2002. Vol. 133. № 3. P. 667–676. DOI:https://doi.org/10.1016/s1095-6433(02)00182-4.

108. Yancey P.H., Clark M.E., Hand S.C., Bowlus R.D., Somero G.N. Living with water stress: evolution of osmolyte systems // Science. 1982. Vol. 217. № 24. P. 1214–1222. DOI:https://doi.org/10.1126/science.7112124.

109. Yancey P.H., Gerringer M.E., Drazen J.C., Rowden A.A., Jamieson A. Marine fish may be biochemically constrained from inhabiting the deepest ocean depths // Proc. Natl. Acad. Sci. USA. 2014. Vol. 111. № 12. P. 4461–4465. DOI:https://doi.org/10.1073/pnas.1322003111.

110. Yancey P.H., Rhea M.D., Kemp K.M., Bailey D.M. Trimethylamine oxide, betaine and other osmolytes in deep-sea animals: depth trends and effects on enzymes under hydrostatic pressure // Cell. Mol. Biol. 2004. Vol. 50. № 4. P. 371–376.

111. Yancey P.H., Siebenaller J.F. Trimethylamine oxide stabilizes teleost and mammalian lactate dehydrogenases against inactivation by hydrostatic pressure and trypsinolysis // J. Exp. Biol. 1999. Vol. 202 (Pt 24). P. 3597–3603. DOI:https://doi.org/10.1242/jeb.202.24.3597.

112. Yancey P.H., Somero G.N. Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes // Biochem. J. 1979. Vol. 183. P. 317–323. DOI:https://doi.org/10.1042/bj1830317.

113. Yancey P.H., Somero G.N. Methylamine osmoregulatory solutes of elasmobranch fishes counteract urea inhibition of enzymes // J. Exp. Zool. 1980. Vol. 212. P. 205–213.

114. Yancey P.H., Speers-Roesch B., Atchinson S. et al. Osmolyte Adjustments as a Pressure Adaptation in Deep-Sea Chondrichthyan Fishes: An Intraspecific Test in Arctic Skates (Amblyraja hyperborea) along a Depth Gradient // Physiol. Biochem. Zool. 2018. Vol. 91. № 2. P. 788–796. DOI:https://doi.org/10.1086/696157.

115. Zou Q., Bennion B.J., Daggett V., Murphy K.P. The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea // J. Am. Chem. Soc. 2002. Vol. 124. № 7. P. 1192–1202. DOI:https://doi.org/10.1021/ja004206b.

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