Ukr.Biochem.J. 2019; Volume 91, Issue 4, Jul-Aug, pp. 58-69

doi: https://doi.org/10.15407/ubj91.04.058

Carassius auratus as a novel model for the hyperglycemia study

12.06.2019   Uncategorized   No comments

H. I. Falfushynska1, O. I. Horyn1, L. L. Gnatyshyna1,2,
B. B. Buyak1, N. I. Rusnak1, O. O. Fedoruk1, O. B. Stoliar1

1Ternopil Volodymyr Hnatiuk National Pedagogical University, Ukraine;
e-mail: falfushynska@tnpu.edu.ua;
2I. Horbachevsky Ternopil State Medical University, Ukraine

Received: 21 August 2018; Accepted: 13 December 2018

The aim of the present study was to create a suitable model of the glucose toxicity and elucidate the ability of zinc-binding proteins metallothioneins in the crucian carp Carassius auratus to reflect it. For that, fish was loaded by three waterborne concentrations of glucose (low (5.55 mM, LC), middle (55.5 mM, MC) or high (111 mM, HC)) for 21 days. The level of blood glucose, responses of metallothioneins, oxidative stress, DNA instability in the liver, as well as erythrocytes indices, cholinesterase activity in the brain and morphometric variables were evaluated. An increase in blood glucose levels (up to 3–5 times), glycated hemoglobin (HbA1c, only by the HC, by 55%), methemoglobin (by two times), oxyradicals (16-57%) and TBARS levels (up to 57%), frequency of the micronucleated erythrocytes, DNA fragmentation in hepatocytes, body mass and hepatosomatic indices and a decrease in metallothioneins concentration (40-74%), cholinesterase activity (~70%), total hemoglobin (by 18%) and red blood cells count (only after HC-treatment, by 47%) were detected. The lysosomal membrane stability, evaluated by the neutral red retention time, was affected by all studied concentrations of glucose (decreased by 58%). The most prominent changes were observed after the HC of glucose. CART analysis revealed the significant splitting parameters for studied group differentiation including HbA1c, lysosomal membrane stability and lipid peroxidation. We could consider the crucian carp is a useful model organism to perform DM studies and in the future, this fish model can help in mechanistic investigations and testing therapeutic interventions under glycemic states.

Keywords: , , , , , ,

References:

  1. Olokoba AB, Obateru OA, Olokoba LB. Type 2 diabetes mellitus: a review of current trends. Oman Med J. 2012 Jul;27(4):269-73. PubMed, PubMedCentral, CrossRef
  2. Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, Cavan D, Shaw JE, Makaroff LE. IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract. 2017 Jun;128:40-50. PubMed, CrossRef
  3. Capiotti KM, Antonioli R Jr, Kist LW, Bogo MR, Bonan CD, Da Silva RS. Persistent impaired glucose metabolism in a zebrafish hyperglycemia model. Comp Biochem Physiol B Biochem Mol Biol. 2014 May;171:58-65.  PubMed, CrossRef
  4. Capiotti KM, De Moraes DA, Menezes FP, Kist LW, Bogo MR, Da Silva RS. Hyperglycemia induces memory impairment linked to increased acetylcholinesterase activity in zebrafish (Danio rerio). Behav Brain Res. 2014 Nov 1;274:319-25. PubMed, CrossRef
  5. Carnovali M, Luzi L, Banfi G, Mariotti M. Chronic hyperglycemia affects bone metabolism in adult zebrafish scale model. Endocrine. 2016 Dec;54(3):808-817. PubMed, CrossRef
  6. Kawahito S, Kitahata H, Oshita S. Problems associated with glucose toxicity: role of hyperglycemia-induced oxidative stress. World J Gastroenterol. 2009 Sep 7;15(33):4137-42. PubMed, PubMedCentral, CrossRef
  7. Viskupicova J, Blaskovic D, Galiniak S, Soszyński M, Bartosz G, Horakova L, Sadowska-Bartosz I. Effect of high glucose concentrations on human erythrocytes in vitro. Redox Biol. 2015 Aug;5:381-7. PubMed, PubMedCentral, CrossRef
  8. Palmer TN, Ryman BE. Studies on oral glucose intolerance in fish. J Fish Biol. 1972;4(2):311-319.  CrossRef
  9. Kamalam BS, Medale F, Panserat S. Utilisation of dietary carbohydrates in farmed fishes: New insights on influencing factors, biological limitations and future strategies. Aquaculture. 2017;467(20):3-27. CrossRef
  10. Takahashi S. Positive and negative regulators of the metallothionein gene (review). Mol Med Rep. 2015 Jul;12(1):795-9.  PubMed, CrossRef
  11. Krężel A, Maret W. The Functions of Metamorphic Metallothioneins in Zinc and Copper Metabolism. Int J Mol Sci. 2017 Jun 9;18(6). pii: E1237. PubMed, PubMedCentral, CrossRef
  12. Bellomo E, Hogstrand C, Maret W.  Redox and zinc signalling pathways converging on protein tyrosine phosphatases. Free Radic Biol Med. 2014 Oct;75(Suppl 1):S9. PubMed, CrossRef
  13. Lowell BB, Shulman GI. Mitochondrial dysfunction and type 2 diabetes. Science. 2005 Jan 21;307(5708):384-7. PubMed, CrossRef
  14. Chabosseau P, Rutter GA. Zinc and diabetes. Arch Biochem Biophys. 2016 Dec 1;611:79-85. PubMed, CrossRef
  15. Cai L. Metallothionein as an adaptive protein prevents diabetes and its toxicity. Nonlinearity Biol Toxicol Med. 2004 Apr;2(2):89-103. PubMed, PubMedCentral, CrossRef
  16. Moon TW, Foster GD. Tissue carbohydrate metabolism, gluconeogenesis and hormonal and environmental influences. Biochem Mol Biol Fish. 1995;4:65-100.  CrossRef
  17. Falfushynska HI, Gnatyshyna LL, Stoliar OB, Nam YK. Various responses to copper and manganese exposure of Carassius auratus gibelio from two populations. Comp Biochem Physiol C Toxicol Pharmacol. 2011 Sep;154(3):242-53. PubMed, CrossRef
  18. Falfushynska H, Gnatyshyna L, Turta O, Stoliar O, Mitina N, Zaichenko A, Stoika R. Responses of hepatic metallothioneins and apoptotic activity in Carassius auratus gibelio witness a release of cobalt and zinc from waterborne nanoscale composites. Comp Biochem Physiol C Toxicol Pharmacol. 2014 Mar;160:66-74. PubMed, CrossRef
  19. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265-75. PubMed
  20. Viarengo A, Ponzano E, Dondero F, Fabbri R. A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar Environ Res. 1997;44(1):69-84.  CrossRef
  21.  Viarengo A, Burlando B, Cavaletto M, Marchi B, Ponzano E, Blasco J. Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am J Physiol. 1999 Dec;277(6):R1612-9. PubMed, CrossRef
  22.  Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979 Jun;95(2):351-8. PubMed, CrossRef
  23. Olive PL. DNA precipitation assay: a rapid and simple method for detecting DNA damage in mammalian cells. Environ Mol Mutagen. 1988;11(4):487-95. PubMed, CrossRef
  24. Falfushynska HI, Gnatyshyna LL, Stoliar OB. Population-related molecular responses on the effect of pesticides in Carassius auratus gibelio. Comp Biochem Physiol C Toxicol Pharmacol. 2012 Mar;155(2):396-406. PubMed, CrossRef
  25. Moore MN, Lowe D, Köhler A. Biological effects of contaminants: measurement of lysosomal membrane stability. ICES Tech. Mar. Environ. Sci. 2004;36:31.
  26. Nazar ML, Rodrigues LEA, Nascimento I. The lysosomal stability as a biomarker for the determination of pollution in aquatic environments. Braz Arch Biol Technol. 2008;51(5):1071-1077.  CrossRef
  27. Ellman GL, Courtney KD, Andres VJr, Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961 Jul;7(2):88-95. PubMed, CrossRef
  28. Graham JJ, Ryall RG, Wise PH. Glycosylated haemoglobin and relative polycythaemia in diabetes mellitus. Diabetologia. 1980 Mar;18(3):205-7. PubMed, CrossRef
  29. Agrawal R, Bhatnagar R, Smart T, Richards C, Pavesio CE, Shima DT, Jones P. Assessment of red blood cell deformability by optical tweezers in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2015;56(7):5183.
  30. Stookey JD, Burg M, Sellmeyer DE, Greenleaf JE, Arieff A, Van Hove L, Gardner C, King JC. A proposed method for assessing plasma hypertonicity in vivo. Eur J Clin Nutr. 2007 Jan;61(1):143-6. PubMed, CrossRef
  31. Oyedemi SO, Adewusi EA, Aiyegoro OA, Akinpelu DA. Antidiabetic and haematological effect of aqueous extract of stem bark of Afzelia africana (Smith) on streptozotocin-induced diabetic Wistar rats. Asian Pac J Trop Biomed. 2011 Oct;1(5):353-8. PubMed, PubMedCentral, CrossRef
  32. Tamariz LJ, Young JH, Pankow JS, Yeh HC, Schmidt MI, Astor B, Brancati FL. Blood viscosity and hematocrit as risk factors for type 2 diabetes mellitus: the atherosclerosis risk in communities (ARIC) study. Am J Epidemiol. 2008 Nov 15;168(10):1153-60. PubMed, PubMedCentral, CrossRef
  33. Mahmoud AM. Hematological alterations in diabetic rats – Role of adipocytokines and effect of citrus flavonoids. EXCLI J. 2013 Jul 19;12:647-57. PubMed, PubMedCentral
  34. Bosman DR, Winkler AS, Marsden JT, Macdougall IC, Watkins PJ. Anemia with erythropoietin deficiency occurs early in diabetic nephropathy. Diabetes Care. 2001 Mar;24(3):495-9. PubMed, CrossRef
  35. Richter NA. Percentage of glycosylated hemoglobin and serum concentration of glucose in the blood of Japanese macaques and in three exotic ruminant species. Am J Vet Res. 1986 Aug;47(8):1783-4. PubMed
  36. Alayash AI, el-Hassan AM, Omer R, Bonaventura J. Glycosylated haemoglobin: an indicator of long-term blood glucose in domestic sheep and goats. Comp Biochem Physiol A Comp Physiol. 1988;90(2):229-31. PubMed, CrossRef
  37. Unnikrishnan R, Anjana RM, Jayashri R, Mohan V. Unexpectedly low HbA1c levels in two diabetes patients following dapsone use. Indian J Endocrinol Metab. 2012 Jul;16(4):658-9. PubMed, PubMedCentral, CrossRef
  38. Yamashita T, Hashiramoto A, Haluzik M, Mizukami H, Beck S, Norton A, Kono M, Tsuji S, Daniotti JL, Werth N, Sandhoff R, Sandhoff K, Proia RL. Enhanced insulin sensitivity in mice lacking ganglioside GM3. Proc Natl Acad Sci USA. 2003 Mar 18;100(6):3445-9. PubMed, PubMedCentral, CrossRef
  39. Tiribuzi R, Orlacchio A, Crispoltoni L, Maiotti M, Zampolini M, De Angeliz M, Mecocci P, Cecchetti R, Bernardi G, Datti A, Martino S, Orlacchio A. Lysosomal β-galactosidase and β-hexosaminidase activities correlate with clinical stages of dementia associated with Alzheimer’s disease and type 2 diabetes mellitus. J Alzheimers Dis. 2011;24(4):785-97. PubMed, CrossRef
  40. Sims-Robinson C, Zhao S, Hur J, Feldman EL. Central nervous system endoplasmic reticulum stress in a murine model of type 2 diabetes. Diabetologia. 2012 Aug;55(8):2276-84. PubMed, PubMedCentral, CrossRef
  41. Sims-Robinson C, Bakeman A, Rosko A, Glasser R, Feldman EL. The Role of Oxidized Cholesterol in Diabetes-Induced Lysosomal Dysfunction in the Brain. Mol Neurobiol. 2016 May;53(4):2287-96. PubMed, PubMedCentral, CrossRef
  42. Tachibana H, Ogawa D, Sogawa N, Asanuma M, Miyazaki I, Terami N, Hatanaka T, Horiguchi CS, Nakatsuka A, Eguchi J, Wada J, Yamada H, Takei K, Makino H. Metallothionein deficiency exacerbates diabetic nephropathy in streptozotocin-induced diabetic mice. Am J Physiol Renal Physiol. 2014 Jan 1;306(1):F105-15. PubMed, CrossRef
  43. Bellomo EA, Meur G, Rutter GA. Glucose regulates free cytosolic Zn²⁺ concentration, Slc39 (ZiP), and metallothionein gene expression in primary pancreatic islet β-cells. J Biol Chem. 2011 Jul 22;286(29):25778-89. PubMed, PubMedCentral, CrossRef
  44. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res. 2010 Oct 29;107(9):1058-70. PubMed, PubMedCentral, CrossRef
  45. Fenech M, Kirsch-Volders M, Natarajan AT, Surralles J, Crott JW, Parry J, Norppa H, Eastmond DA, Tucker JD, Thomas P. Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis. 2011 Jan;26(1):125-32. PubMed, CrossRef
  46. Falfushynska HI, Gnatyshyna LL, Stoliar OB. In situ exposure history modulates the molecular responses to carbamate fungicide Tattoo in bivalve mollusk. Ecotoxicology. 2013 Apr;22(3):433-45. PubMed, CrossRef
  47. Falfushynska H, Gnatyshyna L, Horyn O, Shulgai A, Stoliar O. A calcium channel blocker nifedipine distorts the effects of nano-zinc oxide on metal metabolism in the marsh frog Pelophylax ridibundus. Saudi J Biol Sci. 2017;4:67-74.   CrossRef
  48. Salimi M, Broumand B, Mozdarani H. Association of elevated frequency of micronuclei in peripheral blood lymphocytes of type 2 diabetes patients with nephropathy complications. Mutagenesis. 2016 Nov;31(6):627-633. PubMed, CrossRef
  49. Shettigar SK, Shailaja C, Kulkarni RK. Elevated micronuclei frequency in type 2 diabetes with high glycosylated hemoglobin. Diabetes Res Clin Pract. 2012 Feb;95(2):246-50. PubMed, CrossRef
  50. Sherin A, Anu J, Peeyush KT, Smijin S, Anitha M, Roshni BT, Paulose CS. Cholinergic and GABAergic receptor functional deficit in the hippocampus of insulin-induced hypoglycemic and streptozotocin-induced diabetic rats. Neuroscience. 2012 Jan 27;202:69-76. PubMed, CrossRef
  51. Kuhad A, Chopra K. Lycopene ameliorates thermal hyperalgesia and cold allodynia in STZ-induced diabetic rat. Indian J Exp Biol. 2008 Feb;46(2):108-11. PubMed
  52. Tomlinson DR, Gardiner NJ. Glucose neurotoxicity. Nat Rev Neurosci. 2008 Jan;9(1):36-45. PubMed, CrossRef
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