Criteria for Searching for Proteins with High Osmotic Activity in the Blood of Albumin-Free Teleost

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The criteria for searching for proteins-substitutes for the osmotic function of serum albumin in the blood of albumin-free fish that have lost albumins during the evolutionary process have been developed: (1) high negative charge of the proteins-substitutes (q–) as a measure of their high osmotic activity and/or (2) the ability to remodel with the formation of particles with high q–. In albumin-free fish, these criteria are met by multiple serum α1-globulins: α1-antitrypsin (AIAT); heat acclimation protein Wap65 or hemopexin Hx; apolipoproteins A in high-density lipoproteins (HDL) content. Their status as factors with high osmotic activity comparable to mammalian albumins is confirmed by experimental data from various authors. Comparison of the organization of serum α1-globulins in albumin-free fish and mammals with analbuminemia allowed us to identify strategies in fish (1) to enhance the negative charge of AIAT and Wap65, which is not typical for AIAT and Hx in humans, and (2) to the dominant content of HDL lipoproteins in the blood of fish, which, during remodeling in the experiment and in vivo, form particles with high q– and high water-binding activity. The results obtained confirm the concept of the stability of the protein system of plasma in Vertebrata, capable of compensating for the functions of individual proteins lost during the evolutionary process and adapting to environmental conditions due to adaptive changes in the organization of own proteins, including by changing their surface charge, which affects osmotic activity.

About the authors

A. M Andreeva

Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences

Email: aam@ibiw.ru
Borok, Russia

References

  1. Андреева А.М., Рябцева И.П., Федоров Р.А. 2015. Организация белковых комплексов плазмы у костистых рыб // Тр. ИБВВ РАН. Вып. 72(75). С. 5.
  2. Кирпичников В.С. 1987. Генетика и селекция рыб. Л.: Наука.
  3. Черний В.И. 2017. Роль и место альбумина в современной инфузионно-трансфузионной терапии // Медицина неотложных состояний. Вып. 1(80). С. 23. https://doi.org/10.22141/2224-0586.1.80.2017.94448
  4. Adamson R.H., Lenz J.F., Zhang X. et al. 2004. Oncotic pressures opposing filtration across non-fenestrated rat microvessels // J. Physiol. V. 557(3). P. 889. https://doi.org/10.1113/jphysiol.2003.058255
  5. Ahlqvist J. 2004. Equation for osmotic pressure of serum protein (fractions) // J. Appl. Physiol. V. 96. P. 762. https://doi.org/10.1152/japplphysiol.00880.2003
  6. Anguizola J., Matsuda R., Barnaby O.S. et al. 2013. Review: Glycation of human serum albumin // Clin. Chim. Acta. V. 425. P. 64.
  7. Andreeva A.M. 2010. The role of structural organization of blood plasma proteins in the stabilization of water metabolism in bony fish (Teleostei) // J. Ichthyol. V. 5(7). P. 552. https://doi.org/10.1134/S0032945210070076
  8. Аndreeva A.M., Lamash N.E., Serebryakova M.V. et al. 2015. Reorganization of low-molecular-weight fraction of plasma proteins in the annual cycle of Cyprinidae // Biochemistry (Moscow). V. 80. P. 208. https://doi.org/10.1134/S0006297915020078
  9. Andreeva A.M., Serebryakova M.V., Lamash N.E. 2017. Oligomeric protein complexes of apolipoproteins stabilize the internal fluid environment of organism in redfins of the Tribolodon genus (Pisces; Cypriniformes, Cyprinidae) // Comp. Biochem. Physiol., D: Genomics Proteomics. V. 22. P. 90. https://doi.org/10.1016/j.cbd.2017.02.007
  10. Andreeva A.M. 2019. The strategies of organization of the fish plasma proteome: with and without albumin // Russ. J. Mar. Biol. V. 45(4). P. 263. https://doi.org/10.1134/S1063074019040023
  11. Andreeva A.M., Vasiliev A.S., Toropygin I.Yu. et al. 2019. Involvement of apolipoprotein A in maintaining tissue fluid balance in goldfish Carassius auratus // Fish Physiol. Biochem. V. 45(5). P. 1717. https://doi.org/10.1007/s10695-019-00662-1
  12. Andreeva A.M. 2020. Structural organization of plasma proteins as a factor of capillary filtration in pisces // Inland Water Biol. V. 13(4). P. 664. https://doi.org/10.1134/S1995082920060036
  13. Andreeva А.M., Toropygin I.Yu., Garina D.V. et al. 2020. The Role of high_density lipoproteins in maintaining osmotic homeostasis in the goldfish Carassius auratus L. (Cyprinidae) // J. Evol. Biochem. Physiol. V. 56. № 2. Р. 102. https://doi.org/ 10.1134/S0022093020020027
  14. Andreeva A.M. 2022. Evolutionary transformations of albumin using the example of model species of jawless agnatha and bony jawed fish (Review) // Inland Water Biol. V. 15. P. 641. https://doi.org/10.1134/S1995082922050029
  15. Andreeva A.M., Bazarova Z.M., Toropygin I.Yu. et al. 2023. Serum osmotically active proteins in the atlantic cod Gadus morhua // J. Evol. Biochem. Physiol. V. 59(2). P. 325. https://doi.org/10.1134/S0022093023020023
  16. Andreeva A.M., Lamash N., Martemyanov V.I. et al. 2024. High-density lipoprotein remodeling affects the osmotic properties of plasma in goldfish under critical salinity // J. Fish Biol. V. 104(3). P. 564. https://doi.org/10.1111/jfb.15607
  17. Babaei F., Ramalingam R., Tavendale A. et al. 2013. Novel blood collection method allows plasma proteome analysis from single zebrafish // J. Proteome Res. V. 12(4). P. 1580.
  18. Babin P.J., Vernier J.M. 1989. Plasma lipoproteins in fish // J. Lipid Res. V. 30. P. 467. http://www.jlr.org/content/30/4/467.long
  19. Braasch I., Gehrke A.R., Smith J.J. et al. 2016. The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons // Nature Genetics. V. 48. P. 427.
  20. Braasch I., Guiguen Y., Loker R. et al. 2014. Connectivity of vertebrate genomes: Paired-related homeobox (Prrx) genes in spotted gar, basal teleosts, and tetrapods // Comp. Biochem. Physiol. Toxicol. & Pharmacol. V. 163. P. 24.
  21. Chappell D., Jacob M. 2014. Role of the glycocalyx in fluid management: small things matter // Best Pract. Res. Clin. Anaesthesiol. V. 28. P. 227. https://doi.org/10.1016/j.bpa.2014.06.003
  22. Chen J., Shi H., Hu H.Q. et al. 2009. Apolipoprotein A-I, a hyperosmotic adaptation-related protein in ayu (Plecoglossus altivelis) // Comp. Biochem. Physiol. Part B: Biochem. Mol. Biol. V. 152. P. 196.
  23. Curry F.E., Adamson R.H. 2012. Endothelial glycocalyx: permeability barrier and mechanosensory // Ann. Biomed. Eng. V. 40. P. 828. https://doi.org/10.1007/s10439-011-0429-8
  24. Curry S., Mandelkow H., Brick P., Franks N. 1998. Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites // Nat. Struct. Biol. V. 5(9). P. 827.
  25. De Smet H., Blust R., Moens L. 1998. Absence of albumin in the plasma of the common carp Cyprinus carpio: binding of fatty acids to high density lipoprotein // Fish Physiol. Biochem. V. 19(1). P. 71.
  26. Deutsch H.F., McShan W.H. 1949. Biophysical studies of blood plasma proteins; electrophoretic studies of the blood serum proteins of some lower animals // J. Biol. Chem. V. 180(1). P. 219.
  27. Esumi H., Sugimura T. 2007. Phenotypic reversion in analbuminemic rats due to an altered splicing mechanism // Proc. Jpn. Acad. Ser B Phys. Biol. Sci. V. 83(4). P. 101. https://doi.org/10.2183/pjab.83.101
  28. Fanali G., di Masi A., Trezza V. et al. 2012. Human serum albumin: from bench to bedside // Mol. Aspects Med. V. 33(3). P. 209. https://doi.org/10.1016/j.mam.2011.12.002
  29. Gaal O., Medgyesi G.A., Vereczkey L. 1980. Electrophoresis in the separation of biological macromolecules. Chichester: Wiley.
  30. Gabel J.C., Drake R.E. 1984. Plasma proteins and protein osmotic pressure // Edema, edited by Staub NC and Taylor AE. New York: Raven. P. 371.
  31. Grandison M.K., Boudinot F.D. 2000. Age-related changes in protein binding of drugs: implications for therapy // Clin. Pharmacokinet. V. 38(3). P. 271. https://doi.org/10.2165/00003088-200038030-00005
  32. Helvaci M.R., Lesley Pocock A.A. 2020. The safest values of high density lipoproteins in the plasma // World Family Medicine Journal // Middle East J. Family Medicine. V. 18(5). P. 38. https://doi.org/10.5742/MEWFM.2020.93807
  33. Kornmueller K., Vidakovic I., Prassl R. 2019. Artificial high density lipoprotein nanoparticles in cardiovascular research // Molecules. V. 24(15). P. 2829 (1–28). https://doi.org/10.3390/molecules24152829
  34. Kontush A., Lindahl M., Lhomme M. et al. 2015. Structure of HDL: particle subclasses and molecular components // Handb. Exp. Pharmacol. V. 224. P. 3. https://doi.org/10.1007/978-3-319-09665-0_1
  35. Kuz'min E.V., Kuz'mina O.Iu. 2005. Population analysis of electrophoretic variation in blood serum albumins of European (Acipencer ruthensis L.) and Siberian (A. ruthensis marsiglii Brandt) sterlet // Genetika. V. 41(2). P. 246. In Russian.
  36. Kueppers F. 1971. Alpha-1-antitrypsin: physiology, genetics and pathology // Humangenetik. V. 11(3). P. 177. https://doi.org/10.1007/BF00274738
  37. Lahlou B., Henderson I.W., Sawyer W.H. 1969. Sodium exchanges in goldfish (Carassius auratus L.) adapted to a hypertonic saline solution // Comp. Biochem. Physiol. V. 28(3). P. 1427.
  38. Larsson M., Pettersson T., Carlstrom A. 1985. Thyroid hormone binding in serum of 15 vertebrate species: isolation of thyroxine-binding globulin and prealbumin analogs // Gen. Comp. Endocrinol. V. 58(3). P. 360.
  39. Levitt D.G., Levitt M.D. 2016. Human serum albumin homeostasis: a new look at the roles of synthesis, catabolism, renal and gastrointestinal excretion, and the clinical value of serum albumin measurements // Int. J. General Med. V. 9. P. 229.
  40. Martemyanov V.I., Poddubnaya N.Y. 2019. Volume regulation of muscle cells in the carp Cyprinus carpio in response to hypernatremia // Bratisl. Med. J. V. 120(1). P. 52.
  41. Metcalf V.J., Brennan S.O., George P.M. 1999. The Antarctic toothfish (Dissostichus mawsoni) lacks plasma albumin and utilises high density lipoprotein as its major palmitate binding protein // Comp. Biochem. Physiol. Part B: Biochem. Mol. Biol. V. 124(2). P. 147.
  42. Michel C.C. 1997. Starling: the formulation of his hypothesis of microvascular fluid exchange and its significance after 100 years // Exp. Physiol. V. 82. P. 1. https://doi.org/10.1113/expphysiol.1997.sp004000
  43. Michelis R., Sela S., Zeitun T. et al. 2016. Unexpected normal colloid osmotic pressure in clinical states with low serum albumin // PLoS ONE. V. 11(7). e0159839.
  44. Minchiotti L., Caridi G., Campagnoli M. et al. 2019. Diagnosis, phenotype, and molecular genetics of congenital analbuminemia // Frontiers in Genetic. V. 10. P. 1. https://doi.org/10.3389/fgene.2019.00336
  45. Moore D.H. 1945. Species differences in serum protein patterns // J. Biol. Chem. V. 161. P. 21.
  46. Nagase S., Shimamune K., Shumiya S. 1980. Albumin-deficient rat mutant: an animal model for analbuminemia // Jikken Dobutsu. V. 29(1). P. 33. https://doi.org/10.1538/expanim1978.29.1_33
  47. Nelson J.S. 2006. Fishes of the World. New Jersey: John Wiley & Sons, Inc.
  48. Nguyen M.K., Kurtz I. 2006. Quantitative interrelationship between Gibbs–Donnan equilibrium, osmolality of body fluid compartments, and plasma water sodium concentration // J. Appl. Physiol. V. 100. P. 1293. https://doi.org/10.1152/japplphysiol.01274.2005
  49. Noel E.S., Reis M.D., Arain Z., Ober E.A. 2010. Analysis of the Albumin/alpha-Fetoprotein/Afamin/Group specific component gene family in the context of zebrafish liver differentiation // Gene expression patterns. V. 10. P. 237.
  50. Nynca J., Arnold G., Frohlich T., Ciereszko A. 2017. Proteomic identification of rainbow trout blood plasma proteins and their relationship to seminal plasma proteins // Proteomics. V. 17(11). P. 1. https://doi.org/10.1002/pmic.201600460
  51. Ohno S. 1970. Evolution by gene duplication. Berlin: Springer.
  52. Olson K.R. 1992. Blood and extracellular fluid volume regulation: role of the renin-angiotensin system, kallikrein–kinin system, and atrial natriuretic peptides // Fish Physiol. V. 12. P. 136. https://doi.org/10.1016/S1546-5098(08)60010-2
  53. Olson K.R., Kinney D.W., Dombrowski R.A., Duff D.W. 2003. Transvascular and intravascular fluid transport in the rainbow trout: revisiting Starling’s forces, the secondary circulation and interstitial compliance // J. Exp. Biol. V. 206. P. 457. https://doi.org/10.1242/jeb.00123
  54. Olson K.R. 2011. Design and physiology of capillaries and secondary circulation. Circulatory fluid balance and transcapillary exchange // Encyclopedia of Fish Physiology from Genome to Environment. P. 1154. https://doi.org/10.1016/B978-0-12-374553-8.00050-2
  55. Otis J., Zeituni E.M., Thierer J.H. et al. 2015. Zebrafish as a model for apolipoprotein biology: comprehensive expression analysis and a role for ApoA-IV in regulating food intake // Dis. Model. Mech. V. 8(3). P. 295. https://doi.org/10.1242/dmm.018754
  56. Ott H. 1956. Die Errechnung des kolloidosmotischen Serumdruckes aus dem Eiweiss-Spektrum und das mittlere Molekulargewicht der Serumeiweiss-fraktionen // Klin Wochenschr. V. 34. P. 1079.
  57. Park Y.J., Kim Y.C., Kim M.O., Ruy J.H., Han S.W., Kim H.J. 2000. Successful treatment in the patient with serum sodium level greater than 200 mEq/L // J Korean Med Sci. V. 15 (6). P. 701. https://doi.org/10.3346/jkms.2000.15.6.701
  58. Pasquier J., Cabau C., Nguyen T. et al. 2016. Gene evolution and gene expression after whole genome duplication in fish: the PhyloFish database // BMC Genomics. V. 17. № 368. P. 1. https://doi.org/10.1186/s12864-016-2709-z
  59. Peters T. 1970. Serum albumin // Adv. Clin. Chem. V. 13. P. 37. https://doi.org/10.1016/s0065-2423(08)60385-6
  60. Power D.M., Elias N.P., Richardson S.J. et al. 2000. Evolution of the thyroid hormone-binding protein, transthyretin // Gen. Comp. Endocrynol. V. 119. P. 241.
  61. Qiu L.L., Levinson S.S., Keeling K.L., Elin R.J. 2003. Convenient and effective method for removing fibrinogen from serum specimens before protein electrophoresis // Clin. Chem. V. 49(6/1). P. 868. https://doi.org/10.1373/49.6.868
  62. Rosengren B.I., Carlsson O., Venturoli D. et al. 2004. Transvascular passage of macromolecules into the peritoneal cavity of normo- and hypothermic rats in vivo: active or passive transport? // J. Vasc. Res. V. 41. P. 123. https://doi.org/10.1159/000077131
  63. Sarin H. 2010. Physiologic upper limits of pore size of different blood capillary types and another perspective on the dual pore theory of microvascular permeability // J. Angiog. Res. V. 2. P. 1. https://doi.org/10.1186/2040-2384-2-14
  64. Schulz G.E., Schirmer R.H. 1979. Principles of Protein Structure. New York: Springer.
  65. Stoletov K., Fang L., Soo-Ho Choin et al. 2009. Vascular lipid accumulation, lipoprotein oxidation, and macrophage lipid uptake in hypercholesterolemic zebrafish // Circul. Res. V. 104. P. 952. https://doi.org/10.1161/CIRCRESAHA.108.189803
  66. Tiselius A. 1937. Electrophoresis of serum globulin: Electrophoretic analysis of normal and immune sera // Biochem. J. V. 31(9). P. 1464.
  67. Weinbaum S. 1998. Whitaker distinguished lecture: model to solve mysteries in biomechanics at the cellular level; a new view of fiber matrix layers // Ann. Biomed. Eng. V. 26. P. 627. https://doi.org/10.1114/1.134
  68. Wicher K.B., Fries E. 2006. Haptoglobin, a hemoglobinbinding plasma protein, is present in bony fish and mammals but not in frog and chicken // Proc. Natl. Acad. Sci. U.S.A. V. 103(11). P. 4168.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2025 Russian Academy of Sciences

Согласие на обработку персональных данных

 

Используя сайт https://journals.rcsi.science, я (далее – «Пользователь» или «Субъект персональных данных») даю согласие на обработку персональных данных на этом сайте (текст Согласия) и на обработку персональных данных с помощью сервиса «Яндекс.Метрика» (текст Согласия).