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Cases of a Spontaneous Increase in Methemoglobin Concentration in Fish Blood during the Annual Cycle

  • ECOLOGICAL PHYSIOLOGY AND BIOCHEMISTRY OF HYDROBIONTS
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Abstract

The dynamics of the content of erythrocyte number and concentration of methemoglobin in the blood of the thermophilic mullet (Chelon auratus Risso, 1810) and the cold-loving flounder (Platichthys flesus L., 1758) during the annual cycle has been studied. The degree of maturity of the circulating erythrocyte mass is judged on the basis of construction of acid erythrograms. A pronounced negative relationship is found between the number of red blood cells and the concentration of methemoglobin in the blood of both types (r = –0.681; –0.778). It has been shown that the youngest generation of red blood cells appears in the peripheral bed of both species in the postspawning period (1.5–2.0 months), which reflects the active production of erythrocytes by hematopoietic tissue. The rest of the time, there is a gradual aging of the circulating erythrocyte mass. This leads to a decrease in the number of red blood cells in the blood and is accompanied by an increase in the concentration of methemoglobin. The latter, apparently, determines the production of erythropoietins in the kidneys and activates the processes of erythropoiesis in hematopoietic tissue (prespawning period).

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REFERENCES

  1. Affonso, E.G., Polez, V.L., Corrêa, C.F., et al., Blood parameters and metabolites in the teleost fish Colossoma macropomum exposed to sulfide or hypoxia, Comp. Biochem. Physiol., Part C: Comp. Pharmacol., 2002, vol. 133, no. 3, p. 375. https://doi.org/10.1016/s1532-0456(02)00127-8

    Article  CAS  Google Scholar 

  2. Andreeva, A.M. and Ryabtseva, I., Adaptation mechanisms of respiratory blood function in Teleostei, J. Ichthyol., 2011, vol. 51, no. 9, p. 799. https://doi.org/10.1134/S0032945211050018

    Article  Google Scholar 

  3. Andreeva, A.Y., Soldatov, A.A., and Kukhareva, T.A., Black scorpionfish (Scorpaena porcus) hemopoiesis: Analysis by flow cytometry and light microscopy, Anatom. Rec., 2017, vol. 300, no. 11, p. 1993. https://doi.org/10.1002/ar.23631

    Article  CAS  Google Scholar 

  4. Blair, B., Barlow, C., Martin, E., et al., Methemoglobin determination by multi-component analysis in coho salmon (Oncorhynchus kisutch) possessing unstable hemoglobin, Methods, 2020, vol. 7, p. 100836. https://doi.org/10.1016/j.mex.2020.100836

    Article  CAS  Google Scholar 

  5. Chen, N., Wu, M., Tang, G.-P., et al., Effects of acute hypoxia and reoxygenation on physiological and immune responses and redox balance of wuchang bream (Megalobrama amblycephala Yih, 1955), Front. Physiol., 2017, vol. 8, p. 375. https://doi.org/10.3389/fphys.2017.00375

    Article  PubMed  PubMed Central  Google Scholar 

  6. Chou, C.-F., Tohari, S., Brenner, S., and Venkatesh, B., Erythropoietin gene from a teleost fish, Fugu rubripes, Blood, 2004, vol. 104, p. 1498. https://doi.org/10.1182/blood-2003-10-3404

    Article  CAS  PubMed  Google Scholar 

  7. Fischer, U., Ototake, M., and Nakanishi, T., Life span of circulating blood cells in ginbuna crucian carp (Carassius auratus langsdorfii), Fish Shellfish Immunol., 1998, vol. 8, p. 339. https://doi.org/10.1006/fsim.1998.0144

    Article  Google Scholar 

  8. Graham, M.S. and Fletcher, G.L., High concentrations of methemoglobin in five species of temperate marine teleosts, J. Exp. Zool., 1986, vol. 239, p. 139. https://doi.org/10.1002/jez.1402390117

    Article  CAS  PubMed  Google Scholar 

  9. Hammer, Ø. and Harper, D.A.T., Paleontological Data Analysis, Blackwell, 2006. https://doi.org/10.1002/jqs.1107

  10. Hardig, J. and Hoglund, L.B., Seasonal and ontogenetic effects on methaemoglobin and reduced glutathione contents in the blood of reared baltic salmon, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 1983, vol. 76, no. 1, p. 27. https://doi.org/10.1016/0300-9629(83)90039-7

    Article  Google Scholar 

  11. Houston, A.H., Roberts, W.C., and Kennington, J.A., Hematological response in fish: pronephric and splenic involvements in the goldfish, Carassius auratus L., Fish Physiol. Biochem., 1996, vol. 15, no. 6, p. 481. https://doi.org/10.1007/BF01874922

    Article  CAS  PubMed  Google Scholar 

  12. Kokkidis, M.J., Goubier, V., Martin, M., et al., Haematological changes in the blood of cultured black-bass (Micropterus salmoides) during an annual sexual reproductive cycle, Ichtyologie, 2000, vol. 24, no. 3S, p. 113.

    Google Scholar 

  13. Krishna, M.S. and Venkataramana, G., Status of lipid peroxidation, glutathione, ascorbic acid, vitamin E and antioxidant enzymes in patients with pregnancy-induced hypertension, Indian J. Physiol. Pharmacol., 2007, vol. 51, p. 284.

    Google Scholar 

  14. Kushakovskii, M.S., Methemoglobinemia, Spravochnik po funktsional’noi diagnostike (Reference Book on Functional Diagnostics), Moscow: Meditsina, 1970.

    Google Scholar 

  15. Lai, J.C.C., Kakuta, I., Mok, H.O.L., et al., Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen, J. Exp. Biol., 2006, vol. 209, p. 2734. https://doi.org/10.1242/jeb.02279

    Article  CAS  PubMed  Google Scholar 

  16. Maestre, R., Pazos, M., and Medina, I., Involvement of methemoglobin (MetHb) formation and hemin loss in the pro-oxidant activity of fish hemoglobins, J. Agric. Food Chem., 2009, vol. 57, no. 15, p. 7013. https://doi.org/10.1021/jf9006664

    Article  CAS  PubMed  Google Scholar 

  17. Maslova, M.N. and Tavrovskaya, T.V., The dynamics of seasonal changes in the erythrocyte systems of lower vertebrates: Seasonal dynamics of erythropoiesis in the trout Salmo gairdneri, Zh. Evol. Biokhim. Fiziol., 1991, vol. 27, p. 796.

    CAS  Google Scholar 

  18. Maslova, M.N., Soldatov, A.A., and Tavrovskaya, T.V., Seasonal dynamics in the state of the red blood system of several Black Sea fish, J. Evol. Biochem. Physiol., 1988, vol. 24, no. 4, p. 398.

    Google Scholar 

  19. Moritz, K.M., Lim, G.B., and Wintour, E.M., Developmental regulation of erythropoietin and erythropoiesis, Am. J. Physiol., 1997, vol. 273, p. R1829. https://doi.org/10.1152/ajpregu.1997.273.6.R1829

  20. Percy, M.J. and Lappin, T.R., Recessive congenital methaemoglobinaemia: cytochrome b 5 reductase deficiency, Br. J. Haematol., 2008, vol. 141, no. 3, p. 298. https://doi.org/10.1111/j.1365-2141.2008.07017.x

    Article  CAS  PubMed  Google Scholar 

  21. Phillips, M.C.L., Moyes, C.D., and Tufts, B.L., The effects of cell ageing on metabolism in rainbow trout (Oncorhynchus mykiss) red blood cells, J. Exp. Biol., 2000, vol. 203, no. 6, p. 1039. https://doi.org/10.1242/jeb.203.6.1039

    Article  CAS  PubMed  Google Scholar 

  22. Pottinger, T.G. and Pickering, A.D., Androgen levels and erythrocytosis in maturing brown trout, Salmo trutta L., Fish Physiol. Biochem., 1987, vol. 3, no. 3, p. 121. https://doi.org/10.1007/BF02180413

    Article  CAS  PubMed  Google Scholar 

  23. Powell, M.D. and Perry, S.F., Respiratory and acid-base pathophysiology of hydrogen peroxide in rainbow trout (Oncorhynchus mykiss), Aquat. Toxicol., 1997, vol. 37, p. 99. https://doi.org/10.1016/S0166-445X(96)00826-0

    Article  CAS  Google Scholar 

  24. Rothmann, C., Levinshal, T., Timan, B., et al., Spectral imaging of red blood cells in experimental anemia of Cyprinus carpio, Comp. Biochem. Physiol., 2000, vol. 125A, p. 75. https://doi.org/10.1016/s1095-6433(99)00157-9

    Article  CAS  Google Scholar 

  25. Sajiki, J. and Takahashi, K., In vitro formation of methemoglobin by lipophilic fractions in fishes and the causative substance, Eisei Kagaku, 1991, vol. 37, no. 6, p. 467. https://doi.org/10.1248/JHS1956.37.467

    Article  CAS  Google Scholar 

  26. Saleh, M.C. and McConkey, S., NADH-dependent cytochrome b5 reductase and NADPH methemoglobin reductase activity in the erythrocytes of Oncorhynchus mykiss, Fish Physiol. Biochem., 2012, vol. 38, p. 1807. https://doi.org/10.1007/s10695-012-9677-2

    Article  CAS  PubMed  Google Scholar 

  27. Schechter, A.N., Hemoglobin research and the origins of molecular medicine, Blood, 2008, vol. 112, no. 10, p. 3927. https://doi.org/10.1182/blood-2008-04-078188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Schoore, E.J., Simco, B.A., and Davis, K.B., Responses of blue catfish and channel catfish to environmental nitrite, J. Aquat. Anim. Health, 1995, vol. 7, p. 304. https://doi.org/10.1577/1548-8667(1995)007<0304:ROBCAC>2.3.CO;2

    Article  Google Scholar 

  29. Shedpure, M. and Pati, A.K., Do thyroid and testis modulate the effects of pineal and melatonin on haemopoietic variables in Clarias batrachus?, J. Biosci., 1996, vol. 21, no. 6, p. 797. https://doi.org/10.1007/BF02704721

    Article  CAS  Google Scholar 

  30. Soldatov, A.A., Peculiarities of organization and functioning of the fish red blood system, J. Evol. Biochem. Physiol., 2005, vol. 41, p. 272.

    Article  CAS  Google Scholar 

  31. Soldatov, A.A., Physiological aspects of effects of urethane anesthesia on the organism of marine fishes, Hydrobiol. J., 2005, vol. 41, no. 1, p. 113. https://doi.org/10.1615/HydrobJ.v41.i1.130

    Article  Google Scholar 

  32. Soldatov, A.A., Content of methemoglobin in the blood of teleost fish: effect of environmental factors and natural states of the organism (review), Inland Water Biol., 2021, vol. 14, no. 6, p. 747. https://doi.org/10.1134/S1995082921060122

    Article  Google Scholar 

  33. Soldatov, A.A. and Maslova, M.N., Concentration of methemoglobin in blood of fish in the course of the annual cycle, J. Evol. Biochem. Physiol., 1989, vol. 25, no. 4, p. 317.

    Google Scholar 

  34. Soldatov, A.A., Andreeva, A.Y., Kukhareva, T.A., and Andreyenko, T.I., Methemoglobin and the activities of catalase and superoxide dismutase in nucleated erythrocytes of Scorpaena porcus (Linnaeus, 1758) under experimental hypoxia (in vitro), Biophysics, 2020, vol. 65, p. 452. https://doi.org/10.1134/S0006350920030197

    Article  CAS  Google Scholar 

  35. Sorvachev, K.F., Osnovy biokhimii pitaniya ryb (Fundamentals of Biochemistry of Fish Nutrition), Moscow: Legk. Pishch. Prom-st., 1982.

  36. Stenko, M.I., Blood, in Spravochnik po klinicheskim laboratornym metodam issledovaniya (Handbook of Clinical Laboratory Research Methods), Moscow: Meditsina, 1975.

  37. Tilak, K.S., Veeraiah, K., and Milton, J., Effects of ammonia, nitrite and nitrate on hemoglobin content and oxygen consumption of freshwater fish, Cyprinus carpio (Linnaeus), J. Environ. Biol., 2007, vol. 28, no. 1, p. 45.

    CAS  PubMed  Google Scholar 

  38. Wdzieczak, J., Zalesna, G., Bartkowiak, A., et al., Comparative studies on superoxide dismutase, catalase and peroxidase level in erythrocytes and livers of different fresh water and marine fish species, Comp. Biochem. Physiol., 1982, vol. 73B, no. 2, p. 361. https://doi.org/10.1016/0305-0491(82)90298-X

    Article  CAS  Google Scholar 

  39. Wickramasinghe, S.N., Erythropoietin and the human kidney: evidence for an evolutionary link from studies of Salmo gairdneri, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 1993, vol. 104A, p. 63. https://doi.org/10.1016/0300-9629(93)90009-s

    Article  CAS  Google Scholar 

  40. Woo, S.P.S., Liu, W., Au, D.W.T., et al., Antioxidant responses and lipid peroxidation in gills and erythrocytes of fish (Rhabdosarga sarba) upon exposure to Chattonella marina and hydrogen peroxide: Implications on the cause of fish kills, J. Exp. Mar. Biol. Ecol., 2006, vol. 336, p. 230. https://doi.org/10.1016/j.jembe.2006.05.013

    Article  CAS  Google Scholar 

  41. Žikić, R.V., Štajn, A., and Petrović, V.M., Effect of dexamethasone on the activity of superoxide dismutase and catalase in the tissue and erythrocytes of goldfish, Carassius auratus gibelio (Bloch), Iugosl. Physiol. Pharmacol. Acta, 1991, vol. 27, no. 1, p. 45.

    Google Scholar 

  42. Zolotova, T.E., Experimental study of hematopoiesis in fish, Extended Abstract of Cand. Sci. Dissertation, Moscow: Moscow State Univ., 1987.

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Funding

This work was carried out within the framework of the Russian Science Foundation, project 23-24-00061.

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  1. Kovalevsky Institute of Biology of the South Seas, Russian Academy of Sciences, Sevastopol, Russia

    A. A. Soldatov

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Correspondence to A. A. Soldatov.

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Translated by P. Kuchina

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Soldatov, A.A. Cases of a Spontaneous Increase in Methemoglobin Concentration in Fish Blood during the Annual Cycle. Inland Water Biol 16, 769–775 (2023). https://doi.org/10.1134/S1995082923040181

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