Skip to main content
Log in

Content of Methemoglobin in the Blood of Teleost Fish: Effect of Environmental Factors and Natural States of the Organism (Review)

  • ECOLOGICAL PHYSIOLOGY AND BIOCHEMISTRY OF HYDROBIONTS
  • Published:
Inland Water Biology Aims and scope Submit manuscript

Abstract

This paper presents summarized information on the factors determining an increase in content of methemoglobin (MtHb) in the blood of teleost fish. It is shown that the transition of hemoglobin to the ferric form in fish can be caused not only by cases of toxic methemoglobinemia. A significant increase in the concentration of MtHb in fish blood is also observed under the conditions of external hypoxia and hypothermia. This may be due to an increase in the content of the deoxy-form of the pigment (hypoxia) and a decrease in the activity of NADH-diaphorase (hypothermia). In fish, there is also a periodic increase in the content of MtHb in the blood during the annual cycle. This state coincides with the prespawning and spawning periods. It is associated with the monocyclic functioning of the hematopoietic tissue. Active erythropoiesis in fish occurs only in the postspawning period for 2–3 months. At all other times, the destructive processes dominate in the red blood system, which affects both the number of circulating red blood cells and the level of oxidative processes in them. In comparison with mammals, fish hemoglobins prove to be less resistant to oxidative stress, which is probably due to their instability and low efficiency of NADH diaphorase in red blood cells of this systematic group of organisms. At the same time, fish red blood cells are characterized by a high content of glutathione (GSH), especially in terms of hemoglobin (GSH/Hb index). This is due to the high efficiency of the pentose shunt reactions, which allows maintaining a high level of NADPH in the cell. This feature probably compensates for the low activity of NADH diaphorase. A protective effect of Cl and epinephrine on hemoglobin is recorded under nitrite intoxication. They significantly reduce the toxic effect of N\({\text{O}}_{2}^{ - }\). We further discuss the mechanisms responsible for the transition of fish hemoglobin to the oxidized state.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Adragna, N.C., Di Fulvio, M., and Lauf, P.K., Regulation of K-Cl cotransport: from function to genes, J. Membr. Biol., 2004, vol. 201, p. 109. https://doi.org/10.1007/s00232-006-1002-5

    Article  CAS  PubMed  Google Scholar 

  2. Affonso, E.G., Polez, V.L., Correa, 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, p. 375. https://doi.org/10.1016/S1532-0456(02)00127-8

    Article  CAS  Google Scholar 

  3. Alayash, A.I., Brockner-Ryan, B.A., and Fratantoni, J.C., Oxidation reactions of human, opossum (Didelphis virginiana) and spot (Leiostomus xanthurus) hemoglobins: a search for a correlation with some structural-functional properties, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1993, vol. 106, p. 427. https://doi.org/10.1016/0305-0491(93)90324-x

    Article  CAS  Google Scholar 

  4. Andreyeva, 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 

  5. Andreyeva, A.Y., Soldatov, A.A., and Kukhareva, T.A., Black scorpionfish (Scorpaena porcus) hemopoiesis: analysis by flow cytometry and light microscopy, Anat. Rec., 2017a, vol. 300, no. 11, p. 1993. https://doi.org/10.1002/ar.23631/pdf

    Article  CAS  Google Scholar 

  6. Andreyeva, A.Y., Soldatov, A.A., and Mukhanov, V.S., The influence of acute hypoxia on the functional and morphological state of the black scorpionfish red blood cell, In Vitro Cell. Dev. Biol.: Anim., 2017b, vol. 53, p. 312. https://doi.org/10.1002/ar.23631

    Article  CAS  Google Scholar 

  7. Anuradha, S. and Subburam, V., Role of sewage bacteria in methemoglobin formation in Cyprinus carpio exposed to nitrate, J. Environ. Biol., 1995, vol. 16, p. 175.

    Google Scholar 

  8. Bachand, L. and Leray, C., Erythrocyte metabolism in the yellow porch. I. Glycolytic enzymes, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1975, vol. 50, no. 4, p. 567.

    Article  CAS  Google Scholar 

  9. Bieniarz, K., Szymacha, J., and Epler, P., Gonad development, ovulation and spermiation in carp under highly eutrophicated pond conditions, Aquaculture, 1995, vol. 129, p. 133.

    Article  Google Scholar 

  10. 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, no. 100836. https://doi.org/10.1016/j.mex.2020.100836

  11. Boutilier, R.G. and Ferguson, R.A., Nucleated red cell function: metabolism and pH regulation, Can. J. Zool., 1989, vol. 67, p. 2986. https://doi.org/10.1139/z89-421

    Article  CAS  Google Scholar 

  12. Bowser, P.R., Falls, W.W., Vanzandt, J., et al., Methemoglobinemia in channel catfish: methods of prevention, Prog. Fish Cult., 2011, vol. 45, no. 3, p. 154. https://doi.org/10.1577/1548-8659(1983)45[154:MICC]2.0.CO;2

    Article  Google Scholar 

  13. 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. 1. https://doi.org/10.3389/fphys.2017.00375

    Article  Google Scholar 

  14. Chernikova, V.V., Hematological characteristics of wintering carp underyearlings, Izv. Vses. Inst. Ozern. Rechn. Rybn. Khoz., 1974, vol. 88, p. 109.

    Google Scholar 

  15. Dafre, A.L. and Reischl, E., Asymmetric hemoglobins, their thiol content, and blood glutathione of the scalloped hammerhead shark, Sphyrna lewini, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1997, vol. 116, no. 3, p. 323. https://doi.org/10.1016/S0305-0491(96)00215-5

    Article  CAS  Google Scholar 

  16. Dubinina, E.E., Danilova, L.A., Efimova, L.F., et al., Activity of superoxide dismutase and the content of methemoglobin in human and animal erythrocytes, Zh. Evol. Biokhim. Fiziol., 1988, vol. 24, no. 2, p. 17.

    Google Scholar 

  17. Ferguson, R.A. and Storey, K.B., Glycolytic and associated enzymes of rainbow trout (Oncorhynchus mykiss) red cells: in vitro and in vivo studies, J. Exp. Biol., 1991, vol. 155, p. 469.

    Article  CAS  Google Scholar 

  18. Flerova, E.A., Sendek, D.S., and Yurchenko, V.V., Specific features of the ultrastructure of mesonephros of smolts of the Atlantic salmon Salmo salar L. (Baltic Sea population) and brown trout Salmo trutta L., Inland Water Biol., 2020, vol. 13, no. 4, pp. 445–454. https://doi.org/10.1134/S1995082920030062

    Article  Google Scholar 

  19. Gabryelak, T. and Peres, G., Comparative antioxidant enzyme and lipid peroxidation study in erythrocytes and liver of some freshwater fish, Acta Biol. Hung., 1986, vol. 37, nos. 3–4, p. 219.

    CAS  PubMed  Google Scholar 

  20. Giles, M.A., Strain differences in hemoglobin polymorphism, oxygen consumption, and blood oxygen equilibria in three hatchery broodstocks of Arctic charr, Salvelinus alpinus, Fish. Physiol. Biochem., 1991, vol. 9, no. 4, p. 291.

    Article  CAS  PubMed  Google Scholar 

  21. 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 

  22. Gritsenko, O.F., Kotlyar, A.N., and Kotenev, B.N., Promyslovye ryby Rossii (Commercial Fishes of Russia), Moscow: VNIRO, 2006, vol. 2.

  23. 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.

    Article  Google Scholar 

  24. Hattingh, J. and Du ToitP.J., The haemoglobins of the yellowfish and barbel, S. Afr. J. Med. Sci., 1973, vol. 38, nos. 1–2, p. 37.

    CAS  PubMed  Google Scholar 

  25. Hilmy, A.M., El-Domiaty, N.A., and Wershana, K., Acute and chronic toxicity of nitrite to Clarias lazera, Comp. Biochem. Physiol., Part C: Comp. Pharmacol., 1987, vol. 86, p. 247.

    CAS  Google Scholar 

  26. Hofer, R. and Gatumu, E., Necrosis of trout retina (Oncorhynchus mykiss) after sublethal exposure to nitrite, Arch. Environ. Contam. Toxicol., 1994, vol. 26, p. 119.

    Article  CAS  Google Scholar 

  27. Holk, K., Effects of isotonic swelling on the intracellular bohr factor and the oxygen affinity of trout and carp blood, Fish Physiol. Biochem., 1996, vol. 15, p. 371. https://doi.org/10.1007/BF01875579

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  29. Huey, D.W. and Beitingh, T.L., A methemoglobin reductase system in channel catfish, Ictalurus punctatus, Can. J. Zool., 1982, vol. 60, no. 6, p. 1511.

    Article  CAS  Google Scholar 

  30. Imsland, A.K., Brix, O., Naevdal, G., and Samuelsen, E.N., Hemoglobin genotypes in turbot (Scophthalmus maximum R.), their oxygen affinity properties and relation with growth, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 1997, vol. 116, no. 2, p. 157.

    Article  Google Scholar 

  31. Jensen, F.B., Nitrite and red cell function in carp: control factors for nitrite entry, membrane potassium ion permeation, oxygen affinity and methemoglobin formation, J. Exp. Biol., 1990, vol. 152, p. 149.

    Article  Google Scholar 

  32. Jensen, F.B. and Nielsen, K., Methemoglobin reductase activity in intact fish red blood cells, Comp. Biochem. Physiol. A Mol. Integr. Physiol., 2018, vol. 216, p. 14. https://doi.org/10.1016/j.cbpa.2017.11.004

    Article  CAS  PubMed  Google Scholar 

  33. Jensen, F.B., Fago, A., and Weber, R.E., Hemoglobin structure and function, in Fish Physiology, San Diego: Academic, 1998, vol. 17, p. 1.

    Google Scholar 

  34. Kawatsu, Y., Nakanishi, Y., and Takeda, H., Methemoglobin determination in eel blood, Bull. Jpn. Soc. Sci. Fish., 1987, vol. 53, no. 1, p. 9. https://doi.org/10.2331/suisan.53.9

    Article  CAS  Google Scholar 

  35. Kawatsu, H., Yamazaki, T., and Miyamori, E., In vitro hemolysis and methemoglobin formation in common carp erythrocytes induced by hydrogen peroxide and hypoxanthine-xanthine oxidase, Bull. Jpn. Soc. Sci. Fish., 1991, vol. 57, no. 12, p. 2299. https://doi.org/10.2331/suisan.57.2299

    Article  CAS  Google Scholar 

  36. 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, Ichthyologie, 2000, vol. 24, no. 3S, p. 113.

    Google Scholar 

  37. Koudela, K. and Zitkova, V., Chronostabilita a termostabilita methemoglobinu y erytrocytech karpa obecneno, Sb. VSZ. Praze, 1991, p. 35.

    Google Scholar 

  38. 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. https://doi.org/10.4103/0019-5359.29592

    Article  Google Scholar 

  39. Lane, H.C., Weaver, J.W., Benson, J.A., and Nichols, H.A., Some age-related changes of adult rainbow trout, Salmo gairdneri R., peripheral erythrocytes separated by velocity sedimentation at unit gravity, J. Fish. Biol., 1982, vol. 21, no. 1, p. 1. https://doi.org/10.1111/j.1095-8649.1982.tb02818.x

    Article  Google Scholar 

  40. Lund, S.G., Phillips, M.C.L., Moyes, C.D., and Tufts, B.L., The effects of cell ageing on protein synthesis in rainbow trout (Oncorhynchus mykiss) red blood cells, J. Exp. Biol., 2000, vol. 203, p. 2219.

    Article  CAS  PubMed  Google Scholar 

  41. Lushchak, V.I. and Bagnyukova, T.V., Effects of different environmental oxygen levels on free radical processes in fish, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2006, vol. 144, p. 283. https://doi.org/10.1016/j.cbpb.2006.02.014

    Article  CAS  Google Scholar 

  42. Mansouri, A., Methemoglobin formation and reduction in relation to hemoglobin oxygen affinity, Experientia, 1981, vol. 37, p. 95. https://doi.org/10.1007/bf01965591

    Article  CAS  PubMed  Google Scholar 

  43. Marinsky, C.A., Houston, A.H., and Murad, A., Effect of hypoxia on hemoglobin isomorph abundance in rainbow trout, Salmo gairdneri, Can. J. Zool., 1990, vol. 68, no. 5, p. 884. https://doi.org/10.1139/z90-128

    Article  Google Scholar 

  44. Maslova, M.N. and Tavrovskaya, T.V., Dynamics of seasonal changes in the red blood system of lower vertebrates: seasonal dynamics of erythropoiesis in the trout Salmo gairdneri, Zh. Evol. Biokhim. Fiziol., 1991, vol. 27, p. 796.

    CAS  Google Scholar 

  45. 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 

  46. Mather-Mihaich, E. and Di-Giulio, R.T., Oxidant, mixed-function oxidase and peroxisomal responses in channel catfish exposed to a bleached kraft mill effluent, Arch. Environ. Contam. Toxicol., 1991, vol. 20, no. 3, p. 391. https://doi.org/10.1007/bf01064409

    Article  CAS  PubMed  Google Scholar 

  47. Mathies, T. and Mauldin, R.E., Lethal methemoglobinemia in the invasive brown treesnake after acetaminophen ingestion, Sci. Rep., 2020, vol. 10, no. 845. https://doi.org/10.1038/s41598-019-56216-1

  48. Miyauchi, M., Takagi, M., and Uematsu, T., Studies on toxicities of biphenyl ether herbicides and their analogues to fish. I. The methemoglobin-formation by the nitroso-derivatives in white spotted char, Salvelinus leucomaenis, erythrocytes, Bull. Jpn. Soc. Sci. Fish., 1979, vol. 45, no. 12, p. 1563.

    Article  CAS  Google Scholar 

  49. Murad, A., Houston, A.H., and Samson, L., Haematological response to reduced oxygen-carrying capacity, increased temperature and hypoxia in goldfish, J. Fish. Biol., 1990, vol. 36, no. 3, p. 289. https://doi.org/10.1111/j.1095-8649.1990.tb05610.x

    Article  Google Scholar 

  50. Nobrega, F.G., Maia, J.C.C., Colli, W., and Saldanha, P.H., Heterogeneity of erythrocyte glucose-6-phosphate dehydrogenase activity and electrophoretic patterns among representatives of different classes of vertebrates, Comp. Biochem. Physiol., 1970, vol. 33, no. 1, p. 191. https://doi.org/10.1016/0010-406x(70)90494-9

    Article  CAS  PubMed  Google Scholar 

  51. Paajaste, M.N. and Nikinmaa, M., Effect of noradrenaline on the methemoglobin concentration of rainbow trout red cells, J. Exp. Zool., 1991, vol. 260, no. 1, p. 28. https://doi.org/10.1002/JEZ.1402600104

    Article  CAS  PubMed  Google Scholar 

  52. 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 

  53. Perutz, M.F., Mechanisms regulating the reactions of human haemoglobin with oxygen and carbon monoxide, Annu. Rev. Physiol., 1990, vol. 52, p. 1. https://doi.org/10.1146/annurev.ph.52.030190.000245

    Article  CAS  PubMed  Google Scholar 

  54. 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, p. 1039.

    Article  CAS  PubMed  Google Scholar 

  55. Planus, J., Albi, J.L., Pesquero, J., and Sanchez, J., Glucose metabolism in brown trout erythrocytes, Arch. Int. Physiol. Biochim., 1989, vol. 97, no. 5, p. 41.

    Google Scholar 

  56. Pottinger, T.G. and Pickering, A.D., Androgen levels and erythrocytosis in maturing brown trout, Salmo trutta L., Fish Physiol. Biochem., 1987, vol. 3, p. 121.

    Article  CAS  PubMed  Google Scholar 

  57. 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.

    Article  CAS  Google Scholar 

  58. Rabie, F., Magid, A.M., Abdel, G.K., and Karrar, O., Evolution of catalase in fish, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 1972, vol. 43, no. 4, p. 1053. https://doi.org/10.1016/0300-9629(72)90177-6

    Article  CAS  Google Scholar 

  59. Raizada, M.N. and Singh, C.P., Seasonal variations in the erythrocyte counts and haemoglobin content of Cirrhinus mrigala (Ham.), Proc. Indian Nat. Sci. Acad., 1981, vol. 47, no. 5, p. 656.

    Google Scholar 

  60. Ranzani-Paiva, M.J.T., Hematological characteristics of the mullet, Mugil platanus G. from Cananeia lagoon-estuarine region, Bol. Inst. Pesca-Sao-Paulo, 1995, vol. 22, p. 1.

    Google Scholar 

  61. Reagan, R.E. and Drennan, D.G., Enzymatic reduction of methemoglobin to hemoglobin in blue catfish, Ictalurus furcatus, and channel catfish, I. punctatus, [male] x blue catfish [female] hybrids, J. Appl. Aquacult., 1993, vol. 3, nos. 3–4, p. 223.

    Article  Google Scholar 

  62. Rodriguez-Moreno, P.A. and Tarazona, J.V., Nitrite-induced methemoglobin formation and recovery in rainbow trout (Oncorhynchus mykiss) at high chloride concentrations, Bull. Environ. Contam. Toxicol., 1994, vol. 53, no. 1, p. 113.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  64. 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 

  65. Salama, A. and Nikinmaa, M., Effect of oxygen tension on catecholamine-induced formation of camp and on swelling of carp red blood cells, Am. J. Physiol. Cell Physiol., 1990, vol. 259, no. 5, p. C723. https://doi.org/10.1152/ajpcell.1990.259.5.C723

    Article  CAS  Google Scholar 

  66. Saoud, P.I., Naamani, S., Ghanawi, J., and Nasser, N., Effects of acute and chronic nitrite exposure on rabbitfish Siganus rivulatus growth, hematological parameters, and gill histology, J. Aquac. Res., 2014, vol. 5, no. 6, p. 275. https://doi.org/10.4172/2155-9546.1000263

    Article  CAS  Google Scholar 

  67. 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 

  68. 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, no. 4, p. 304. https://doi.org/10.1577/1548-8667(1995)007<0304:ROBCAC>2.3.CO;2

    Article  Google Scholar 

  69. Sephton, D.H., Macphee, W.L., and Driedzic, W.R., Metabolic enzyme activities, oxygen consumption and glucose utilization in sea raven (Hemitripterus americanus) erythrocytes, J. Exp. Biol., 1991, vol. 159, p. 407.

    Article  CAS  Google Scholar 

  70. Smith, C.E. and Russo, R.C., Nitrite-induced methemoglobinemia in rainbow trout, Progr. Fish-Cilt., 1975, vol. 37, no. 3, p. 150.

    Article  CAS  Google Scholar 

  71. Soldatov, A.A., Activity of NADH-dependent methemoglobin reductase in erythrocytes of the round goby Neogobius melanostomus P. during adaptation to low temperatures, Zh. Evol. Biokhim. Fiziol., 1989, vol. 25, no. 6, p. 772.

    CAS  Google Scholar 

  72. Soldatov, A.A., Erythropoiesis and the concentration of methemoglobin in the blood of the singular mullet (Liza aurata Risso) during the annual cycle, in Sovremennye problemy fiziologii i biokhimii vodnykh organizmov (Modern Problems of Physiology and Biochemistry of Aquatic Organisms.), Petrozavodsk: Inst. Biol. Karel. Nauchn. Tsentra Ross. Akad. Nauk, 2005, p. 182.

  73. 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 

  74. Soldatov, A.A. and Parfenova, I.A., The methemoglobin blood level and stability of circulating erythrocytes of the rockfish Scorpaena porcus to osmotic shock under conditions of experimental hypoxia, J. Evol. Biochem. Physiol., 2001, vol. 37, p. 622. https://doi.org/10.1023/A:1014470311122

    Article  CAS  Google Scholar 

  75. Soldatov, A.A., Parfyonova, I.A., and Konoshenko, S.V., Haemoglobin system of Black Sea round goby under experimental hypoxia conditions, Ukr. Biokhim. Zh., 2004, vol. 76, no. 3, p. 85.

    CAS  Google Scholar 

  76. Soldatov, A.A., Andreyeva, 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 (Moscow), 2020, vol. 65, no. 3, p. 452. https://doi.org/10.31857/S0006302920030138

    Article  CAS  Google Scholar 

  77. Solov’ev, A.L., Dubinina, E.E., Danilova, L.A., et al., Sostav gemoglobina i aktivnost' superoksiddismutazy u ryb, obitayushchikh v ozere Baikal (Hemoglobin Composition and Superoxide Dismutase Activity in Fish Inhabiting Lake Baikal), Available from VINITI, 1988, Leningrad: Leningrad. Pediatr. Med. Inst.

  78. Stara, A., Machova, J., and Velisek, J., Effect of chronic exposure to prometryn on oxidative stress and antioxidant response in early life stages of common carp (Cyprinus carpio L.), Neuro Endocrinol. Lett., 2012, vol. 33, p. 130. https://doi.org//10.1016/j.etap.2011.12.019

    CAS  PubMed  Google Scholar 

  79. Stokes, E.E. and Firkin, B.G., Studies of the peripheral blood of the Port Jackson shark (Heterodontus portusjacksoni) with particular reference to the thrombocyte, Br. J. Haematol., 1971, vol. 20, no. 4, p. 427.

    Article  CAS  PubMed  Google Scholar 

  80. Tiihonen, K. and Nikinmaa, M., Substrate utilization by carp (Cyprinus carpio) erythrocytes, J. Exp. Biol., vol. 161, p. 509.

  81. Tomasso, J.R., Comparative inhibition of nitrite toxicity by chloride in temperate freshwater and euryhaline fishes, in Int. Fish Physiol. Symp., Vancouver, BC (Canada), July 16—21, 1994, p. 239.

  82. Tomasso, J.R., Simco, B.L., and Davis, K.B., Chloride inhibition of nitrite-induced methemoglobinemia in channel catfish (Ictalurus punctatus), J. Fish. Res. Board Can., 1979, vol. 36, no. 9, p. 1141. https://doi.org/10.1139/f79-160

    Article  CAS  Google Scholar 

  83. Tucker, C.S. and Macmillan, J.R., Effect of short-term starvation on methemoglobin levels in nitrite-exposed channel catfish, J. Appl. Aquacult., 1992, vol. 1, no. 4, p. 21. https://doi.org/10.1300/J028v01n04_03

    Article  Google Scholar 

  84. Tufts, B., In vitro evidence for sodium-dependent ph regulation in sea lamprey (Petromyzon marinus) red blood cells, Can. J. Zool., 1992, vol. 70, p. 411.

    Article  CAS  Google Scholar 

  85. Urrutia, M.L. and Tomasso, J.R., Acclimation of channel catfish to environmental nitrite, J. World-Aquacult. Soc., 1987, vol. 18, no. 3, p. 175.

    Article  CAS  Google Scholar 

  86. Val, A.L., De Menezes, G.C., and Wood, C.M., Red blood cell adrenergic responses in Amazonian teleosts, J. Fish. Biol., 1997, vol. 52, p. 83.

    Article  Google Scholar 

  87. Veldre, I.A. and Rooma, M.Ya., Toxic effects of nitrites on fish, Ekologiya, 1990, no. 1, p. 71.

  88. Wang, H. and Hu, D., Toxicity of nitrite to grass carp (Ctenopharyngodon idellus) in ponds and its way of prevention, J. Fish. China Shuichan Xuebao, 1989, vol. 13, p. 207.

    Google Scholar 

  89. 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., Part B: Biochem. Mol. Biol., 1982, vol. 73, no. 2, p. 361. https://doi.org/10.1016/0305-0491(82)90298-X

    Article  Google Scholar 

  90. Weinberg, S.R., Lobue, J., Siegel, C.D., and Gordon, A.S., Hematopoiesis of the kissinggourami. Effects of starvation, bleeding and plasma-stimulating factors and its erythropoiesis, Can. J. Zool., 1976, vol. 54, p. 1115. https://doi.org/10.1139/z76-127

    Article  CAS  PubMed  Google Scholar 

  91. White, A., Handler, Ph., Smith, E.L., Hill, R., and Lehman, R., Principles of Biochemistry, Columbus: McGraw-Hill, 1978, vol. 3.

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

    Article  CAS  Google Scholar 

  93. Williams, E.M. and Eddy, F.B., Regulation of blood haemoglobin and electrolytes in rainbow trout, Salmo gairdneri R., Aquat. Toxicol., 1988a, vol. 13, no. 1, p. 13. https://doi.org/10.1016/0166-445X(88)90069-0

    Article  CAS  Google Scholar 

  94. Williams, E.M. and Eddy, F.B., Anion transport, chloride cell number and nitrite-induced methemoglobinaemia in rainbow trout (Salmo gairdneri) and carp (Cyprinus carpio), Aquat. Toxicol., 1988b, vol. 13, no. 1, p. 29. https://doi.org/10.1016/0166-445X(88)90070-7

    Article  CAS  Google Scholar 

  95. Willmore, W.G. and Storey, K.B., Antioxidant systems and anoxia tolerance in a freshwater turtle, Trachemys scripta elegans, Mol. Cell. Biochem., 1997, vol. 170, p. 177. https://doi.org/10.1023/a:1006817806010

    Article  CAS  PubMed  Google Scholar 

  96. Wise, D.J. and Tomasso, J.R., Ascorbic acid inhibition of nitrite-induced methemoglobinemia in channel catfish, Prog. Fish Cult., 1988, vol. 50, no. 2, p. 77. https://doi.org/10.1577/1548-8640(1988)050<0077:AAIONI>2.3.CO;2

    Article  CAS  Google Scholar 

  97. Yavuzcan, H., Koksal, G., Borazan, G., and Gunal, A.C., Nitrite-induced methemoglobinemia in Nile tilapia, Oreochromis niloticus, J. Appl. Ichthyol., 2006, vol. 22, no. 5, p. 427.

    Article  Google Scholar 

  98. Zapata, A. and Carrato, A., Ultrastructure of elasmobranch and teleost erythrocytes, Acta Zool., 1981, vol. 62, no. 2, p. 129. https://doi.org/10.1111/j.1463-6395.1981.tb00621.x

    Article  Google Scholar 

  99. Zikic, R.V., Stajn, A., and Petrovic, V.M., Effect of dexamethasone on the activity of superoxide dismutase and catalase in the tissue and erythrocytes of goldfish, Acta Biol. Jugosl. C, 1991, vol. 27, no. 1, p. 45.

    CAS  Google Scholar 

  100. Zolotova, T.E., Experimental study of hematopoiesis in fish, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: Moscow State Univ., 1989.

Download references

Funding

This work was carried out as a part of State Task no. АААА-А18-118021490093-4 and supported by the Russian Foundation for Basic Research, project no. 20-04-00037.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. A. Soldatov.

Ethics declarations

Conflict of interests. The author declares that he has no conflicts of interest.

Statement on the welfare of animals. This article does not contain any studies involving animals performed by any of the authors.

Additional information

Translated by E. Kuznetsova

Abbreviations: GSН, glutathione; МtНb, methemoglobin; CAT, catalase (EC 1.11.1.6); SOD, superoxide dismutase.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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 14, 747–757 (2021). https://doi.org/10.1134/S1995082921060122

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1995082921060122

Keywords:

Navigation