Skip to main content
SpringerLink
Log in

Serum Osmotically Active Proteins in the Atlantic Cod Gadus morhua

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

Osmotically active proteins (OAP) in the anodic blood serum fraction of the Atlantic cod Gadus morhua were identified using polyacrylamide gel electrophoresis and MALDI mass-spectrometry. A total of 17 OAPs were found. According to the Gene Ontology annotations of candidate genes, 13 OAPs were classified as extracellular and 4 as intracellular proteins. Cod serum OAPs accounted for ~50% of the total protein content. Extracellular apolipoproteins (ApoA, within high-density lipoproteins) and hemopexin dominated in the OAP pool, with ApoA-I accounting for ~25% of total serum proteins. Of the intracellular proteins, low molecular weight fragments of the myosin heavy chain dominated on the proteomic map. The obtained results are consistent with the “albumin-free” capillary exchange hypothesis, which considers multiple extracellular and intracellular proteins of different functional classes as osmotically active plasma proteins in albumin-free teleosts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

REFERENCES

  1. Levitt D, Levitt M (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 Gen Med 9: 229–255. https://doi.org/10.2147/IJGM.S102819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Schulz GE, Schirmer RH (1979) Principles of Protein Structure. Springer-Verlag, New York, 314 p.

    Book  Google Scholar 

  3. Dziegielewska KM, Evans CA, Fossan G, et al. (1980) Proteins in cerebrospinal fluid and plasma of fetal sheep during development. J Physiol 300: 441–455. https://doi.org/10.1113/jphysiol.1980.sp013171

  4. Majorek KA, Porebski PJ, Dayal A, et al. (2012) Structural and immunologic characterization of bovine, horse, and rabbit serum albumins. Mol Immunol 52(3–4): 174–182. https://doi.org/10.1016/j.molimm.2012.05.011

  5. Anguizola J, Matsuda R, Barnaby OS, et al. (2013) Review: glycation of human serum albumin. Clin Chim Acta 425: 64–76. https://doi.org/10.1016/j.cca.2013.07.013

  6. Gray JE, Doolittle RF (1992) Characterization, primary structure, and evolution of lamprey plasma albumin. Protein Sci 1(2): 289–302. https://doi.org/10.1002/pro.5560010211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Byrnes L, Gannon F (1990) Atlantic salmon (Salmo salar) serum albumin: cDNA sequence, evolution, and tissue expression. DNA Cell Biol 9(9): 647–655. https://doi.org/10.1089/dna.1990.9.647

    Article  CAS  PubMed  Google Scholar 

  8. Metcalf V, Brennan S, Chambers G, George P (1998) The albumins of Chinook salmon (Oncorhynchus tshawytscha) and brown trout (Salmo trutta) appear to lack a propeptide. Arch Biochem Biophys 350(2): 239–244. https://doi.org/10.1006/abbi.1997.0509

    Article  CAS  PubMed  Google Scholar 

  9. Metcalf VJ, Brennan SO, Chambers GK, George PM (1998) The albumin of the brown trout (Salmo trutta) is a glycoprotein. Biochim Biophys Acta 1386(1): 90–96.

    CAS  PubMed  Google Scholar 

  10. Xu Y, Ding Z (2005) N-terminal sequence and main characteristics of Atlantic salmon (Salmo salar) albumin. Prep Biochem Biotechnol 35(4): 283–290. https://doi.org/10.1080/10826060500218081

    Article  CAS  PubMed  Google Scholar 

  11. Li S, Cao Y, Geng F (2017) Genome-wide identification and comparative analysis of albumin family in vertebrates. Evol Bioinf Online 13: 1. https://doi.org/10.1177/1176934317716089

    Article  CAS  Google Scholar 

  12. Ballantyne JS (2016) 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 199: 21–28. https://doi.org/10.1016/j.cbpb.2016.03.005

    Article  CAS  PubMed  Google Scholar 

  13. Andreeva AM (2022) Evolutionary transformations of albumin using the example of model species of jawless Agnatha and bony jawed fish (review). Inland Water Biology 15(5): 641–658. https://doi.org/10.1134/S1995082922050029

    Article  Google Scholar 

  14. Andreeva AM (2020) Structural organization of plasma proteins as a factor of capillary filtration in Pisces. Inland Water Biology 13(4): 664–673. https://doi.org/10.1134/S1995082920060036

    Article  Google Scholar 

  15. Michelis R, Sela S, Zeitun T, Geron R, Kristal B (2016) Unexpected normal colloid osmotic pressure in clinical states with low serum albumin. PLoS One 11(7): e0159839. https://doi.org/10.1371/journal.pone.0159839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gaal O, Medgyesi GA, Vereczkey L (1980) Electrophoresis in the separation of biological macromolecules. John Wiley and Sons, Chichester, 83–87.

    Google Scholar 

  17. Andreeva AM (2021) Organization and function of osmotically active fraction of fish (Pisces) plasma proteome. Inland Water Biology 14(4): 449–460. https://doi.org/10.1134/S1995082921040039

    Article  Google Scholar 

  18. Michel CC (1997) Starling: the formulation of his hypothesis of microvascular fluid exchange and its significance after 100 years. Exp Physiol 82: 1–30. https://doi.org/10.1113/expphysiol.1997.sp004000

    Article  CAS  PubMed  Google Scholar 

  19. Weinbaum S (1998) Whitaker distinguished lecture: model tosolve mysteries in biomechanics at the cellular level; a new view of fiber matrix layers. Ann Biomed Eng 26: 627–643. https://doi.org/10.1114/1.134

    Article  CAS  PubMed  Google Scholar 

  20. Adamson RH, Lenz JF, Zhang X, et al. (2004) Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol 557(3): 889–907. https://doi.org/10.1113/jphysiol.2003.058255

  21. Rosengren BI, Carlsson O, Venturoli D, Rayyes O, Rippe B (2004) Transvascular passage of macromolecules into the peritoneal cavity of normo- and hypothermic rats in vivo: active or passive transport? J Vasc Res 41: 123–130. https://doi.org/10.1159/000077131

    Article  CAS  PubMed  Google Scholar 

  22. Curry FE, Adamson RH (2012) Endothelial glycocalyx: permeability barrier and mechanosensor. Ann Biomed Eng 40: 828–839. https://doi.org/10.1007/s10439-011-0429-8

    Article  CAS  PubMed  Google Scholar 

  23. Chappell D, Jacob M (2014) Role of the glycocalyx in fluid management: small things matter. Best Pract Res Clin Anaesthesiol 28: 227–234. https://doi.org/10.1016/j.bpa.2014.06.003

    Article  PubMed  Google Scholar 

  24. Itzhaki RF, Gill DM (1964) A micro-biuret method for estimating proteins. Anal Biochem 9: 401–410.

    Article  CAS  PubMed  Google Scholar 

  25. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259): 680–685. https://doi.org/10.1038/227680a0

    Article  CAS  PubMed  Google Scholar 

  26. Kirpichnikov VS (1987) Genetics and selectics of fish. Nauka, Leningrad, 520 p. (In Russ).

    Google Scholar 

  27. Andreeva AM, Lamash NE, Serebryakova MV, Ryabtseva IP, Bolshakov VV (2015) Reorganization of low-molecular-weight fraction of plasma proteins in the annual cycle of Cyprinidae. Biochemistry (Mosc) 80(2): 208–218. https://doi.org/10.1134/S0006297915020078

  28. Andreeva AM, Serebryakova MV, Lamash N (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 22: 90–97. https://doi.org/10.1016/j.cbd.2017.02.007

    Article  CAS  Google Scholar 

  29. Andreeva AM, Vasiliev AS, Toropygin IY, Garina DV, Lamash N, Filippova A (2019) Involvement of apolipoprotein A in maintaining tissue fluid balance in goldfish Carassius auratus. Fish Physiol Biochem 45(5): 1717–1730. https://doi.org/10.1007/s10695-019-00662-1

    Article  CAS  PubMed  Google Scholar 

  30. Andreeva AM, Toropygin IYu, Garina DV, Lamash NE, Vasiliev AS (2020) The Role of High-Density Lipoproteins in Maintaining Osmotic Homeostasis in the Goldfish Carassius auratus L. (Cyprinidae). J Evol Biochem Physiol 56: 102–112. https://doi.org/10.1134/S0022093020020027

    Article  CAS  Google Scholar 

  31. Choudhury M, Yamada S, Komatsu M, Kishimura H, Ando S (2009) Homologue of mammalian apolipoprotein A-II in non-mammalian vertebrates. Acta Biochim Biophys Sin (Shanghai) 41(5): 370–378. https://doi.org/10.1093/abbs/gmp015

  32. Babin PJ, Vernier JM (1989) Plasma lipoproteins in fish. J Lipid Res 30: 467.

    Article  CAS  PubMed  Google Scholar 

  33. Stoletov K, Fang L, Soo-Ho Choin, Hartvigsen K, Hansen LF, Hall C, Pattison J, Juliano J, Miller ER, Almazan F, Crosier Ph, Witztum J, Klemke R, Miller Yu (2009) Vascular lipid accumulation, lipoprotein oxidation, and macrophage lipid uptake in hypercholesterolemic zebrafish. Circul Res 104: 952–960. https://doi.org/10.1161/CIRCRESAHA.108.189803

    Article  CAS  Google Scholar 

  34. Andreeva AM (2019) The strategies of organization of the fish plasma proteome: with and without albumin. Russ J Mar Biol 45(4): 263–274. https://doi.org/10.1134/S1063074019040023

    Article  CAS  Google Scholar 

  35. Saito H, Lund-Katz S, Phillips M (2004) Contributions of domain structure and lipid interaction to the functionality of exchangeable human apolipoproteins. Progress in Lipid Research 43(4): 350–380. https://doi.org/10.1016/j.plipres.2004.05.002

    Article  CAS  PubMed  Google Scholar 

  36. Diaz-Rosales P, Pereiro P, Figueras A, Novoa B, Dios S (2014) The warm temperature acclimation protein (Wap65) has an important role in the inflammatory response of turbot (Scophthalmus maximus). Fish Shellfish Immunol 41(1): 80–92. https://doi.org/10.1016/j.fsi.2014.04.012

    Article  CAS  PubMed  Google Scholar 

  37. Sha Z, Peng Xu, Tomokazu T, Hong Liu, Terhune J (2008) The warm temperature acclimation protein Wap65 as an immune response gene: its duplicates are differentially regulated by temperature and bacterial infections. Mol Immunol 45(5): 1458–1469. https://doi.org/10.1016/j.molimm.2007.08.012

    Article  CAS  PubMed  Google Scholar 

  38. Sarropoulou E, Fernandes J M O, Mitter K, Magoulas A, Mulero V, Sepulcre M, Figueras A, Novoa B (2010) Evolution of a multifunctional gene: the warm temperature acclimation protein Wap65 in the European seabass Dicentrarchus labrax. Molecular Phylogenetics and Evolution 55(2): 640–649. https://doi.org/10.1016/j.ympev.2009.10.001

    Article  CAS  PubMed  Google Scholar 

  39. Cho YS, Kim BS, Kim DS, Nam YK (2012) Modulation of warm-temperature acclimation- associated 65-kDa protein genes (Wap65-1 and Wap65-2) in mud loach (Misgurnus mizolepis, Cypriniformes) liver in response to different stimulatory treatments. Fish Shellfish Immunol 32(5): 662–669. https://doi.org/10.1016/j.fsi.2012.01.009

    Article  CAS  PubMed  Google Scholar 

  40. Li Ch, Gao Ch, Fu Q, Su B, Chen J (2017) Identification and expression analysis of fetuin B (FETUB) in turbot (Scophthalmus maximus L.) mucosal barriers following bacterial challenge. Fish and Shellfish Immunol 68: 386–394. https://doi.org/10.1016/j.fsi.2017.07.032

    Article  CAS  Google Scholar 

  41. Janciauskiene S (2001) Conformational properties of serineproteinase inhibitors (serpins) confer multiple pathophysiological roles. Biochim Biophys Acta 1535(3): 221. https://doi.org/10.1016/s0925-4439(01)00025-4

    Article  CAS  PubMed  Google Scholar 

  42. Odronitz F, Kollmar M (2007) Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol 8(9): R196. https://doi.org/10.1186/gb-2007-8-9-r196.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Poukkula M, Kremneva E, Serlachius M, Lappalainen P (2011) Actin-depolymerizing factor homology domain: a conserved fold performing diverse roles in cytoskeletal dynamics. Cytoskeleton (Hoboken) 68(9): 471–490. https://doi.org/10.1002/cm.20530.

  44. Otis J, Zeituni EM, Thierer JH, Anderson JL, Brown AC, Boehm ED, Cerchione DM, Ceasrine AM, Avraham-David I, Tempelhof H, Yaniv K, Farber SA (2015) Zebrafish as a model for apolipoprotein biology: comprehensive expression analysis and a role for ApoA-IV in regulating food intake. Dis Model Mech 8(3): 295–309. https://doi.org/10.1242/dmm.018754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Anderson NL, Polanski M, Pieper R, Gatlin T, Tirumalai R, Conrads TP, Veenstra TD, Adkins JN, Pounds JG, Fagan R, Lobley A (2004) The human plasma proteome: a nonredundant list developedby combination of four separate sources. Mol Cell Proteomics 3: 311–326. https://doi.org/10.1074/mcp.M300127-MCP200

    Article  CAS  PubMed  Google Scholar 

  46. Nguyen MK, Kurtz I (2006) Quantitative interrelationship between Gibbs-Donnan equilibrium, osmolality of body fluid compartments, and plasma water sodium concentration. J Appl Physiol 100: 1293–1300. https://doi.org/10.1152/japplphysiol.01274.2005

    Article  CAS  PubMed  Google Scholar 

  47. Olson KR (1992) Blood and extracellular fluid volume regulation: role of the renin-angiotensin system, kallikrein-kinin system, and atrial natriuretic peptides. Fish Physiology 12(B):135–234. https://doi.org/10.1016/S1546-5098(08)60010-2

    Article  Google Scholar 

  48. Olson KR, Kinney DW, Dombrowski RA, Duff DW (2003) Transvascular and intravascular fluid transport in the rainbow trout: revisiting Starling’s forces, the secondary circulation and interstitial compliance. J Exp Biol 206(3): 457–467. https://doi.org/10.1242/jeb.00123

    Article  PubMed  Google Scholar 

  49. Sarin H (2010) Physiologic upper limits of pore size of different blood capillary types and another perspective on the dualpore theory of microvascular permeability. J Angiog Res 2(1): 14. https://doi.org/10.1186/2040-2384-2-14

    Article  CAS  Google Scholar 

  50. 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 19(1): 71–81.

    Article  Google Scholar 

  51. Chen J, Shi YuH, Hu HQ, Niu He, Li MiY (2009) Apolipoprotein A-I, a hyperosmoic adaptation-related protein in ayu (Plecoglossus altivelis). Comp Biochem Physiol B 152: 196–201. https://doi.org/10.1016/j.cbpb.2008.11.005

    Article  CAS  PubMed  Google Scholar 

  52. Andreeva AM, Martemyanov V, Vasiliev AS, Toropygin IYu, Lamash N, Garina DV, Pavlov D (2022) Goldfish as a model for studying the effect of hypernatremia on blood plasma lipoproteins. Bratisl Med J 123(3): 172–177. https://doi.org/10.4149/BLL_2022_028

    Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to I.P. Ryabtseva (IBIW RAS) for her partake in collecting research material.

Funding

This work was implemented under the governmental assignment to the Papanin Institute for Biology of Inland Waters of the Russian Academy of Sciences (IBIW RAS) No. 121050500046-8.

Author information

Authors and Affiliations

  1. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Yaroslavskaya Oblast, Russia

    A. M. Andreeva, Z. M. Bazarova, I. Yu. Toropygin, A. S. Vasiliev, R. A. Fedorov & D. V. Garina

  2. V.N. Orekhovich Institute of Biomedical Chemistry, Russian Academy of Sciences, Moscow, Russia

    I. Yu. Toropygin

  3. St. Petersburg State University, St. Petersburg, Russia

    P. A. Pavlova

Authors
  1. A. M. Andreeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Z. M. Bazarova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. Yu. Toropygin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. S. Vasiliev
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. A. Fedorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. A. Pavlova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. D. V. Garina
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, experimental design, data analysis, writing the manuscript (A.M.A.); fish capturing, blood sampling, serum preparation (А.S.V.); electrophoresis (А.S.V., R.A.F.); protein trypsinolysis, MALDI mass-spectrometry, searching for candidate proteins (Z.M.B., I.Yu.T.); Gene Ontology annotation analysis of candidate proteins (А.М.А., Z.M.B., P.А.P.); electrophoregram densitometry, manuscript formatting (D.V.G.).

Corresponding author

Correspondence to A. M. Andreeva.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

All experimental procedures that involved model animals (fish) complied with ethical standards approved by the legal acts of the Russian Federation, as well as with the principles of the Basel Declaration and the recommendations of the Bioethics Committee at the IBIW RAS (Minutes No. 2 of 19.01.2021).

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

Additional information

Translated by A. Polyanovsky

Russian Text © The Author(s), 2023, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2023, Vol. 59, No. 2, pp. 90–99https://doi.org/10.31857/S004445292302002X.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andreeva, A.M., Bazarova, Z.M., Toropygin, I.Y. et al. Serum Osmotically Active Proteins in the Atlantic Cod Gadus morhua. J Evol Biochem Phys 59, 325–336 (2023). https://doi.org/10.1134/S0022093023020023

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093023020023

Keywords:

Search

Navigation