Journal of fish pathology (한국어병학회지)

The Korean Society of Fish Pathology (한국어병학회)
권호 표지
DOI QR코드

DOI QR Code

Changes in hematoserological profiles and leukocyte redistribution in rainbow trout (Oncorhynchus mykiss) under progressive hypoxia

  • Roh, HyeongJin (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University) ;
  • Kim, Bo Seong (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University) ;
  • Kim, Ahran (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University) ;
  • Kim, Nameun (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University) ;
  • Lee, Mu Kun (Korean Aquatic Organism Disease Inspector Association) ;
  • Park, Chan-Il (Department of Marine Biology & Aquaculture, College of Marine Science, Gyeongsang National University) ;
  • Kim, Do-Hyung (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University)
  • Received : 2020.04.13
  • Accepted : 2020.05.01
  • Published : 2020.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

In recent years, global warming is causing dramatic environmental changes and deterioration, such as hypoxia, leading to reduced survival rate and growth performance of farmed aquatic animals. Hence, understanding systemic immuno-physiological changes in fish under environmental stress might be important to maximize aquaculture production. In this study, we investigated physiological changes in rainbow trout exposed to hypoxic stress by monitoring changes in blood chemistry, leukocyte population, and expression levels of related cytokine genes. Hematological and serological factors were evaluated in blood obtained from rainbow trout sampled at a dissolved level of 4.6 mg O2 L-1 and 2.1 mg O2 L-1. Blood and head kidney tissue obtained at each sampling time point were used to determine erythrocyte size, leukocyte population, and cytokine gene expression. The level of LDH and GPT in fish under progressive hypoxia were significantly increased in plasma. Likewise, the (Granulocyte + Macrophage)/lymphocyte ratio (%) of fish exposed to hypoxia was significantly lower than that in fish in the control group. Such changes might be due to the rapid movement of lymphocytes in fish exposed to acute hypoxia. In this study, significant up-regulation in expression levels of IL-1β and IL-6 gene appeared to be involved in the redistribution of leukocytes in rainbow trout. This is the first study to demonstrate the involvement of cytokines in leukocyte trafficking in fish exposed to hypoxia. It will help us understand systemic physiological changes and mechanisms involved in teleost under hypoxic stress.

Keywords

References

  1. Angelidis P, Baudin-Laurencin F and Youinou P.: Stress in rainbow trout, Salmo gairdneri: effects upon phagocyte chemiluminescence, circulating leucocytes and susceptibility to Aeromonas salmonicida. J Fish Biol 31, 113-122, 1987.
  2. Barange M and Perry RI. Physical and ecological impacts of climate change relevant to marine and inland capture fisheries and aquaculture. Climate change implications for fisheries and aquaculture 7, 2009.
  3. Bianchini K and Wright PA.: Hypoxia delays hematopoiesis: retention of embryonic hemoglobin and erythrocytes in larval rainbow trout, Oncorhynchus mykiss, during chronic hypoxia exposure. J Exp Biol 216, 4415-4425, 2013. https://doi.org/10.1242/jeb.083337
  4. Breitburg DL, Hondorp D, Audemard C, Carnegie RB, Burrell RB, Trice M and Clark V.: Landscape-level variation in disease susceptibility related to shallow-water hypoxia. PLoS One 10, e0116223, 2015. https://doi.org/10.1371/journal.pone.0116223
  5. Castro R, Abos B, Pignatelli J, von Gersdorff Jorgensen L, Gonzalez Granja A, Buchmann K and Tafalla C.: Early immune responses in rainbow trout liver upon viral hemorrhagic septicemia virus (VHSV) infection. PLoS One 9, e111084, 2014. https://doi.org/10.1371/journal.pone.0111084
  6. Davis A, Maney D and Maerz J.: The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22, 760-772, 2008. https://doi.org/10.1111/j.1365-2435.2008.01467.x
  7. DEBLASI A, MAISEL AS, FELDMAN RD, ZIEGLER MG, FRATELLI M, DILALLO M, SMITH DA, LAI CC and MOTULSKY HJ.: In Vivo Regulation $ofI^2$-Adrenergic Receptors on Human Mononuclear Leukocytes: Assessment of Receptor Number, Location, and Function after Posture Change, Exercise, and Isoproterenol Infusion. The Journal of Clinical Endocrinology & Metabolism 63, 847-853, 1986. https://doi.org/10.1210/jcem-63-4-847
  8. Dhabhar FS.: Stress-induced augmentation of immune function-The role of stress hormones, leukocyte trafficking, and cytokines. Brain Behav Immun 16, 785-798, 2002. https://doi.org/10.1016/S0889-1591(02)00036-3
  9. Diaz RJ and Rosenberg R.: Spreading dead zones and consequences for marine ecosystems. Science 321, 926-929, 2008. https://doi.org/10.1126/science.1156401
  10. Diaz-Rosales P, Bird S, Wang T, Fujiki K, Davidson W, Zou J and Secombes C.: Rainbow trout interleukin-2: cloning, expression and bioactivity analysis. Fish Shellfish Immunol 27, 414-422, 2009. https://doi.org/10.1016/j.fsi.2009.06.008
  11. Eliason EJ and Farrell AP.: Effect of hypoxia on specific dynamic action and postprandial cardiovascular physiology in rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 171, 44-50, 2014. https://doi.org/10.1016/j.cbpa.2014.01.021
  12. Girasole M, Dinarelli S and Boumis G.: Structure and function in native and pathological erythrocytes: a quantitative view from the nanoscale. Micron 43, 1273-1286, 2012. https://doi.org/10.1016/j.micron.2012.03.019
  13. Goldberg ED.: Emerging problems in the coastal zone for the twenty-first century. Mar Pollut Bull 31, 152-158, 1995. https://doi.org/10.1016/0025-326X(95)00102-S
  14. Grayfer L, Hodgkinson JW, Hitchen SJ, Belosevic M. Characterization and functional analysis of goldfish (Carassius auratus L.) interleukin-10. Mol. Immunol 48: 563-571. 2011. https://doi.org/10.1016/j.molimm.2010.10.013
  15. Hirano T, Yasukawa K, Harada H, Taga T, Watanabe Y, Matsuda T, Kashiwamura S, Nakajima K, Koyama K and Iwamatsu A.: Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 324, 73-76, 1986. https://doi.org/10.1038/324073a0
  16. Holeton GF and Randall DJ.: Changes in blood pressure in the rainbow trout during hypoxia. J Exp Biol 46, 297-305, 1967. https://doi.org/10.1242/jeb.46.2.297
  17. Hunninghake GW, Glazier AJ, Monick MM and Dinarello CA.: Interleukin-1 is a chemotactic factor for human T-lymphocytes. Am Rev Respir Dis 135, 66-71, 1987.
  18. Kim D and Austin B.: Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immunol 21, 513- 524, 2006. https://doi.org/10.1016/j.fsi.2006.02.007
  19. Kim WR, Flamm SL, Di Bisceglie AM and Bodenheimer HC.: Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology 47, 1363-1370, 2008. https://doi.org/10.1002/hep.22109
  20. King AJ, Tonkin Z and Lieshcke J.: Short-term effects of a prolonged blackwater event on aquatic fauna in the Murray River, Australia: considerations for future events. Marine and Freshwater Research 63, 576-586, 2012. https://doi.org/10.1071/MF11275
  21. Kishimoto T, Akira S, Narazaki M and Taga T.: Interleukin-6 family of cytokines and gp130. Blood 86, 1243-1254, 1995. https://doi.org/10.1182/blood.V86.4.1243.bloodjournal8641243
  22. Kruger K, Lechtermann A, Fobker M, Volker K and Mooren F.: Exercise-induced redistribution of T lymphocytes is regulated by adrenergic mechanisms. Brain Behav Immun 22, 324-338, 2008. https://doi.org/10.1016/j.bbi.2007.08.008
  23. Kruse M, Meinl E, Henning G, Kuhnt C, Berchtold S, Berger T, Schuler G and Steinkasserer A.: Signaling lymphocytic activation molecule is expressed on mature CD83+ dendritic cells and is up-regulated by IL-1 beta. J Immunol 167, 1989-1995, 2001. https://doi.org/10.4049/jimmunol.167.4.1989
  24. Lai JC, Kakuta I, Mok HO, Rummer JL and Randall D.: Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen. J Exp Biol 209, 2734-2738, 2006. https://doi.org/10.1242/jeb.02279
  25. Levin L, Ekau W, Gooday A, Jorissen F, Middelburg J, Naqvi S, Neira C, Rabalais N and Zhang J.: Effects of natural and human-induced hypoxia on coastal benthos, 2009.
  26. Li TL and Gleeson M.: The effect of single and repeated bouts of prolonged cycling and circadian variation on saliva flow rate, immunoglobulin A and alpha-amylase responses. J Sports Sci 22, 1015-1024, 2004. https://doi.org/10.1080/02640410410001716733
  27. Liu J, Plagnes-Juan E, Geurden I, Panserat S and Marandel L.: Exposure to an acute hypoxic stimulus during early life affects the expression of glucose metabolism-related genes at first-feeding in trout. Scientific reports 7, 1-12, 2017. https://doi.org/10.1038/s41598-016-0028-x
  28. Lott J, Wolf P. Alanine and aspartate aminotransferase (ALT and AST). Clinical enzymology: a case-oriented approach 111-138. 1986.
  29. Lutticken C, Kruttgen A, Moller C, Heinrich PC and Rose-John S.: Evidence for the importance of a positive charge and an ${\alpha}$-helical structure of the C-terminus for biological activity of human IL-6. FEBS Lett 282, 265-267, 1991. https://doi.org/10.1016/0014-5793(91)80491-K
  30. Marques-Rocha JL, Samblas M, Milagro FI, Bressan J, Martinez JA, Marti A. Noncoding RNAs, cytokines, and inflammation-related diseases. The FASEB Journal 29: 3595-3611. 2015. https://doi.org/10.1096/fj.14-260323
  31. Maule AG and Schreck CB.: Changes in numbers of leukocytes in immune organs of juvenile coho salmon after acute stress or cortisol treatment. J Aquat Anim Health 2, 298-304, 1990. https://doi.org/10.1577/1548-8667(1990)002<0298:CINOLI>2.3.CO;2
  32. McLoughlin RM, Jenkins BJ, Grail D, Williams AS, Fielding CA, Parker CR, Ernst M, Topley N and Jones SA.: IL-6 trans-signaling via STAT3 directs T cell infiltration in acute inflammation. Proc Natl Acad Sci U S A 102, 9589-9594, 2005. https://doi.org/10.1073/pnas.0501794102
  33. Milligan CL and Girard SS.: Lactate metabolism in rainbow trout. J Exp Biol 180, 175-193, 1993. https://doi.org/10.1242/jeb.180.1.175
  34. MIT License, 2015. Norman Will, U of MN Natural Resources Research Institute. Retrieved from http://www.waterontheweb.org/under/waterquality/DOSatCalc.html.
  35. Ni M, Wen H, Li J, Chi M, Bu Y, Ren Y, Zhang M, Song Z and Ding H.: The physiological performance and immune responses of juvenile Amur sturgeon (Acipenser schrenckii) to stocking density and hypoxia stress. Fish Shellfish Immunol 36, 325-335, 2014. https://doi.org/10.1016/j.fsi.2013.12.002
  36. Nishizawa H, Kono Y, Arai N, Shoji J and Mitamura H.: Ventilatory and behavioural responses of the marbled sole Pseudopleuronectes yokohamae to progressive hypoxia. J Fish Biol 90, 2363-2374, 2017. https://doi.org/10.1111/jfb.13319
  37. O'Connor E, Pottinger T and Sneddon L.: The effects of acute and chronic hypoxia on cortisol, glucose and lactate concentrations in different populations of three-spined stickleback. Fish Physiol Biochem 37, 461-469, 2011. https://doi.org/10.1007/s10695-010-9447-y
  38. Omlin T and Weber JM.: Hypoxia stimulates lactate disposal in rainbow trout. J Exp Biol 213, 3802-3809, 2010. https://doi.org/10.1242/jeb.048512
  39. Petersen L and Gamperl AK.: Cod (Gadus morhua) cardiorespiratory physiology and hypoxia tolerance following acclimation to low-oxygen conditions. Physiological and Biochemical Zoology 84, 18-31, 2011. https://doi.org/10.1086/657286
  40. Poulsen SB, Jensen LF, Nielsen KS, Malte H, Aarestrup K and Svendsen JC.: Behaviour of rainbow trout Oncorhynchus mykiss presented with a choice of normoxia and stepwise progressive hypoxia. J Fish Biol 79, 969-979, 2011. https://doi.org/10.1111/j.1095-8649.2011.03069.x
  41. Randall D, Holeton G and Stevens ED.: The exchange of oxygen and carbon dioxide across the gills of rainbow trout. J Exp Biol 46, 339-348, 1967. https://doi.org/10.1242/jeb.46.2.339
  42. Remen M, Oppedal F, Imsland AK, Olsen RE and Torgersen T.: Hypoxia tolerance thresholds for post-smolt Atlantic salmon: dependency of temperature and hypoxia acclimation. Aquaculture 416, 41-47, 2013. https://doi.org/10.1016/j.aquaculture.2013.08.024
  43. Richards JG, Farrell AP and Brauner CJ.: Fish physiology: hypoxia. Academic Press, 2009.
  44. Rytkonen KT, Vuori KA, Primmer CR and Nikinmaa M.: Comparison of hypoxia-inducible factor-1 alpha in hypoxia-sensitive and hypoxia-tolerant fish species. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 2, 177-186, 2007. https://doi.org/10.1016/j.cbd.2007.03.001
  45. Saint-Paul U.: Physiological adaptation to hypoxia of a neotropical characoid fish Colossoma macropomum, Serrasalmidae. Environ Biol Fishes 11, 53-62, 1984. https://doi.org/10.1007/BF00001845
  46. Somero GN.: The physiology of global change: linking patterns to mechanisms. Annual Review of Marine Science 4, 39-61, 2012. https://doi.org/10.1146/annurev-marine-120710-100935
  47. Takase H, Yu C, Ham D, Chan C, Chen J, Vistica BP, Wawrousek EF, Durum SK, Egwuagu CE and Gery I.: Inflammatory processes triggered by TCR engagement or by local cytokine expression: differences in profiles of gene expression and infiltrating cell populations. J Leukoc Biol 80, 538-545, 2006. https://doi.org/10.1189/jlb.1205719
  48. Talas ZS and Gulhan MF.: Effects of various propolis concentrations on biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss). Ecotoxicol Environ Saf 72, 1994-1998, 2009. https://doi.org/10.1016/j.ecoenv.2009.04.011
  49. Thorarensen H, Gustavsson A, Mallya Y, Gunnarsson S, Arnason J, Arnarson I, Jonsson AF, Smaradottir H, Zoega GT, Imsland AK. The effect of oxygen saturation on the growth and feed conversion of Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 309, 96-102. 2010. https://doi.org/10.1016/j.aquaculture.2010.08.019
  50. van Raaij MT, Pit DS, Balm PH, Steffens AB and van den Thillart, Guido EEJM.: Behavioral strategy and the physiological stress response in rainbow trout exposed to severe hypoxia. Horm Behav 30, 85-92, 1996. https://doi.org/10.1006/hbeh.1996.0012
  51. Vaquer-Sunyer R and Duarte CM.: Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci U S A 105, 15452-15457, 2008. https://doi.org/10.1073/pnas.0803833105
  52. Vijayan MM, Pereira C, Grau EG and Iwama GK.: Metabolic responses associated with confinement stress in tilapia: the role of cortisol. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 116, 89-95, 1997. https://doi.org/10.1016/S0742-8413(96)00124-7
  53. Welker TL, Mcnulty ST and Klesius PH.: Effect of sublethal hypoxia on the immune response and susceptibility of channel catfish, Ictalurus punctatus, to enteric septicemia. J World Aquacult Soc 38, 12-23, 2007. https://doi.org/10.1111/j.1749-7345.2006.00069.x
  54. Wolf PL. Biochemical diagnosis of liver disease. Indian Journal of Clinical Biochemistry 14, 59-90. 1999. https://doi.org/10.1007/BF02869152
  55. Yang J and Chen H.: Effects of gallium on common carp (Cyprinus carpio): acute test, serum biochemistry, and erythrocyte morphology. Chemosphere 53, 877-882, 2003. https://doi.org/10.1016/S0045-6535(03)00657-X