Skip to main content

Advertisement

SpringerLink
Log in

Effect of Tungstate Administration on the Lipid Peroxidation and Antioxidant Parameters in Salivary Glands of STZ-Induced Diabetic Rats

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Sodium tungstate is an alternative to reduce hyperglycemia for the treatment of diabetes. In previous work, we showed that the administration of sodium tungstate increased the specific activity of salivary amylase in the parotid gland. Here, we investigated the effect of the administration of sodium tungstate on the lipid peroxidation and some antioxidant parameters in the submandibular (SM) and parotid (PA) salivary glands of streptozotocin (STZ)-induced diabetic rats. Thirty-two male Wistar rats were divided into four groups (n = 8, each): control (C), control treated with sodium tungstate (CT), diabetic (D), and diabetic treated with sodium tungstate (CT). Sodium tungstate (2 mg/ml) was administered to the STZ-induced diabetic rats for 15 days. Malondialdehyde (MDA), reduced (GSH) and oxidized (GSSG) glutathione, and blood glucose concentrations were quantified. In addition, superoxide dismutase (SOD) and catalase (CAT) activities were assessed. Results revealed that diabetes caused an increase in MDA concentration in both glands, a reduction in the SOD activity in SM, and an increase in catalase activity in PA glands. Administration of sodium tungstate reduced the blood glucose levels and normalized the SOD activity in the SM and MDA levels in both glands of the STZ-induced diabetic rats. Catalase activity was increased in PA glands of diabetic and tungstate-treated animals (p < 0.05). The GSH/GSSG ratio was increased in SM glands of tungstate-treated animals (p < 0.05). Overall, the reduction of hyperglycemia by sodium tungstate reduced lipid peroxidation and caused alterations in the antioxidant system in the salivary glands of STZ-induced diabetic rats.

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
Fig. 3

Similar content being viewed by others

References

  1. Classification and diagnosis of diabetes (2015). Diabetes Care 38 Suppl:S8-s16. https://doi.org/10.2337/dc15-S005

  2. Sies H (2015) Oxidative stress: a concept in redox biology and medicine. Redox Biol 4:180–183. https://doi.org/10.1016/j.redox.2015.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Sies H, Cadenas E (1985) Oxidative stress: damage to intact cells and organs. Philos T Roy Soc B 311(1152):617–631. https://doi.org/10.1098/rstb.1985.0168

    Article  CAS  Google Scholar 

  4. Ighodaro OM (2018) Molecular pathways associated with oxidative stress in diabetes mellitus. Biomed Pharmacother 108:656–662. https://doi.org/10.1016/j.biopha.2018.09.058

    Article  CAS  PubMed  Google Scholar 

  5. Williamson JR, Chang K, Frangos M, Hasan KS, Ido Y, Kawamura T, Nyengaard JR, van den Enden M, Kilo C, Tilton RG (1993) Hyperglycemic pseudohypoxia and diabetic complications. Diabetes 42(6):801–813. https://doi.org/10.2337/diab.42.6.801

    Article  CAS  PubMed  Google Scholar 

  6. Pedersen AML, Sorensen CE, Proctor GB, Carpenter GH, Ekstrom J (2018) Salivary secretion in health and disease. J Oral Rehabil 45(9):730–746. https://doi.org/10.1111/joor.12664

    Article  CAS  PubMed  Google Scholar 

  7. Alfadda AA, Sallam RM (2012) Reactive oxygen species in health and disease. J Biomed Biotechnol 2012:936486–936414. https://doi.org/10.1155/2012/936486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ibuki FK, Simoes A, Nogueira FN (2010) Antioxidant enzymatic defense in salivary glands of streptozotocin-induced diabetic rats: a temporal study. Cell Biochem Funct 28(6):503–508. https://doi.org/10.1002/cbf.1683

    Article  CAS  PubMed  Google Scholar 

  9. Nogueira FN, Carvalho AM, Yamaguti PM, Nicolau J (2005) Antioxidant parameters and lipid peroxidation in salivary glands of streptozotocin-induced diabetic rats. Clin Chim Acta 353(1–2):133–139

    Article  CAS  PubMed  Google Scholar 

  10. Reuterving CO (1986) Pilocarpine-stimulated salivary flow rate and salivary glucose concentration in alloxan diabetic rats. Influence of severity and duration of diabetes. Acta Physiol Scand 126(4):511–515. https://doi.org/10.1111/j.1748-1716.1986.tb07849.x

    Article  CAS  PubMed  Google Scholar 

  11. Vatta MS, Hope SI, Prendes GM, Bianciotti LG, Elverdin JC, Fernandez BE (2002) Salivary glands and noradrenergic transmission in diabetic rats. Auton Autacoid Pharmacol 22(2):65–71

    Article  CAS  PubMed  Google Scholar 

  12. Romero AC, Ibuki FK, Nogueira FN (2012) Sialic acid reduction in the saliva of streptozotocin induced diabetic rats. Arch Oral Biol 56(9):1189–1193. https://doi.org/10.1016/j.archoralbio.2012.02.016

    Article  CAS  Google Scholar 

  13. Nicolau J, Rosa R, Fava-de-Moraes F (1969) The effect of alloxan diabetes upon N-acetylneuraminic acid concentration in the submaxillary glands of rats. Pharmacol Ther Dent 19(2):106–110

    CAS  Google Scholar 

  14. Nicolau J, Souza DN, Nogueira FN (2006) Activity, distribution and regulation of phosphofructokinase in salivary gland of rats with streptozotocin-induced diabetes. Braz Oral res 20 (2):108-113. S1806-83242006000200004

  15. Nicolau J, de Matos JA, de Souza DN, Neves LB, Lopes AC (2005) Altered glycogen metabolism in the submandibular and parotid salivary glands of rats with streptozotocin-induced diabetes. J Oral Sci 47(2):111–116

    Article  CAS  PubMed  Google Scholar 

  16. Nogueira FN, Nicolau J (2004) Influence of streptozotocin-induced diabetes on the activity, distribution and isoenzymes of hexokinase of salivary gland of rats. J Physiol Biochem 61(3):421–427. https://doi.org/10.1007/BF03168448

    Article  Google Scholar 

  17. Nogueira FN, Carvalho RA (2017) Metabolic remodeling triggered by salivation and diabetes in major salivary glands. NMR Biomed 30(2). https://doi.org/10.1002/nbm.3683

  18. Manfredi M, McCullough MJ, Vescovi P, Al-Kaarawi ZM, Porter SR (2004) Update on diabetes mellitus and related oral diseases. Oral Dis 10(4):187–200

    Article  CAS  PubMed  Google Scholar 

  19. Halliwell B, Gutteridge JM (1985) Free radicals in biology and medicine

  20. Kosower NS, Kosower EM (1976) The glutathione-glutathione disulfide system. Free radicals in biology, academic press

  21. Bertinat R, Nualart F, Li X, Yanez AJ, Gomis R (2015) Preclinical and clinical studies for sodium tungstate: application in humans. J Clin Cell Immunol 6(1). https://doi.org/10.4172/2155-9899.1000285

  22. Heidari Z, Harati M, Mahmoudzadeh-Sagheb HR, Moudi B (2008) Beta cell protective effects of sodium tungstate in streptozotocin-induced diabetic rats: glycemic control, blockage of oxidative stress and beta cell histochemistry. Iran Biomed J 12(3):143–152

    CAS  PubMed  Google Scholar 

  23. Thompson KH, Chiles J, Yuen VG, Tse J, McNeill JH, Orvig C (2004) Comparison of anti-hyperglycemic effect amongst vanadium, molybdenum and other metal maltol complexes. J Inorg Biochem 98(5):683–690

    Article  CAS  PubMed  Google Scholar 

  24. Barbera A, Gomis RR, Prats N, Rodriguez-Gil JE, Domingo M, Gomis R, Guinovart JJ (2001) Tungstate is an effective antidiabetic agent in streptozotocin-induced diabetic rats: a long-term study. Diabetologia 44(4):507–513. https://doi.org/10.1007/s001250100479

    Article  CAS  PubMed  Google Scholar 

  25. Donmez BO, Ozturk N, Sarikanat M, Oguz N, Sari R, Ozdemir S (2014) Sodium tungstate alleviates biomechanical properties of diabetic rat femur via modulation of oxidative stress. Gen Physiol Biophys 33(4):443–452. https://doi.org/10.4149/gpb_2014020

    Article  CAS  PubMed  Google Scholar 

  26. Leite MF, Nicolau J (2009) Sodium tungstate on some biochemical parameters of the parotid salivary gland of streptozotocin-induced diabetic rats: a short-term study. Biol Trace Elem Res 127(2):154–163. https://doi.org/10.1007/s12011-008-8233-5

    Article  CAS  PubMed  Google Scholar 

  27. Bergmeyer H, Bernt E (1974) D-glucose determination with GOD and POD, rapid assay. Methods of enzymatic analysis 3:1211–1212

    Google Scholar 

  28. Paoletti F, Mocali A (1990) Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation. Methods Enzymol 186:209–220. https://doi.org/10.1016/0076-6879(90)86110-h

    Article  CAS  PubMed  Google Scholar 

  29. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  30. Esterbauer H, Cheeseman KH (1990) Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 186:407–421. https://doi.org/10.1016/0076-6879(90)86134-h

    Article  CAS  PubMed  Google Scholar 

  31. Lowry OH, Rosebrough NS, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  PubMed  Google Scholar 

  32. Nakhaee A, Bokaeian M, Akbarzadeh A, Hashemi M (2010) Sodium tungstate attenuate oxidative stress in brain tissue of streptozotocin-induced diabetic rats. Biol Trace Elem Res 136(2):221–231. https://doi.org/10.1007/s12011-009-8537-0

    Article  CAS  PubMed  Google Scholar 

  33. Akabarzadeh A, Norouzian M, Jamshidi S, Farhangi A, Allahverdi A, Mofidian S (2007) Lamerad B (2007) induction of diabetes by streptozotocine in rats. Indian J Clin Biochem 22(2):60–64. https://doi.org/10.1007/BF02913315

    Article  Google Scholar 

  34. Barbera A, Rodríguez-Gil JE, Guinovart JJ (1994) Insulin-like actions of tungstate in diabetic rats. Normalization of hepatic glucose metabolism. J Biol Chem 269(31):20047–20053

    Article  CAS  PubMed  Google Scholar 

  35. Muñoz MC, Barberà A, Domínguez J, Fernàndez-Alvarez J, Gomis R, Guinovart JJ (2001) Effects of tungstate, a new potential oral antidiabetic agent, in Zucker diabetic fatty rats. Diabetes 50(1):131–138

    Article  PubMed  Google Scholar 

  36. Rodriguez-Hernandez CJ, Guinovart JJ, Murguia JR (2012) Anti-diabetic and anti-obesity agent sodium tungstate enhances GCN pathway activation through Glc7p inhibition. FEBS Lett 586(3):270–276. https://doi.org/10.1016/j.febslet.2011.12.035

    Article  CAS  PubMed  Google Scholar 

  37. Canals I, Carmona MC, Amigo M, Barbera A, Bortolozzi A, Artigas F, Gomis R (2009) A functional leptin system is essential for sodium tungstate antiobesity action. Endocrinology 150(2):642–650. https://doi.org/10.1210/en.2008-0881

    Article  CAS  PubMed  Google Scholar 

  38. Amigó-Correig M, Barceló-Batllori S, Piquer S, Soty M, Pujadas G, Gasa R, Bortolozzi A, Carmona M, Gomis R (2011) Sodium tungstate regulates food intake and body weight through activation of the hypothalamic leptin pathway. Diabetes Obes Metab 13(3):235–242. https://doi.org/10.1111/j.1463-1326.2010.01339.x

    Article  PubMed  Google Scholar 

  39. Amigó-Correig M, Barceló-Batllori S, Soria G, Krezymon A, Benani A, Pénicaud L, Tudela R, Planas AM, Fernández E, del Carmen CM (2012) Anti-obesity sodium tungstate treatment triggers axonal and glial plasticity in hypothalamic feeding centers. PLoS One 7(7):e39087. https://doi.org/10.1371/journal.pone.0039087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Baynes JW, Thorpe SR (1999) Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48(1):1–9. https://doi.org/10.2337/diabetes.48.1.1

    Article  CAS  PubMed  Google Scholar 

  41. Nakhaee A, Shahabizadeh F, Erfani M (2013) Protein and lipid oxidative damage in healthy students during and after exam stress. Physiol Behav 118:118–121. https://doi.org/10.1016/j.physbeh.2013.05.028

    Article  CAS  PubMed  Google Scholar 

  42. Rellier N, Ruggiero-Lopez D, Lecomte M, Lagarde M, Wiernsperger N (1999) In vitro and in vivo alterations of enzymatic glycosylation in diabetes. Life Sci 64(17):1571–1583. https://doi.org/10.1016/s0024-3205(99)00094-6

    Article  CAS  PubMed  Google Scholar 

  43. Sachdeva S, Flora SJS (2014) Efficacy of some antioxidants supplementation in reducing oxidative stress post sodium tungstate exposure in male Wistar rats. J Trace Elem Med Biol 28(2):233–239. https://doi.org/10.1016/j.jtemb.2014.01.004

    Article  CAS  PubMed  Google Scholar 

  44. Fridovich I (1997) Superoxide anion radical (O2-.), superoxide dismutases, and related matters. J Biol Chem 272(30):18515–18517. https://doi.org/10.1074/jbc.272.30.18515

    Article  CAS  PubMed  Google Scholar 

  45. Rathore N, John S, Kale M, Bhatnagar D (1998) Lipid peroxidation and antioxidant enzymes in isoproterenol induced oxidative stress in rat tissues. Pharmacol Res 38(4):297–303. https://doi.org/10.1006/phrs.1998.0365

    Article  CAS  PubMed  Google Scholar 

  46. Gunawardena HP, Silva R (2019) Poor Glycaemic control is associated with increased lipid peroxidation and glutathione peroxidase activity in type 2 diabetes patients. Oxid med cell Longev 5;2019:9471697. https://doi.org/10.1155/2019/9471697

  47. Weksler-Zangen S, Yaffe P (2003) Ornoy a (2003) reduced SOD activity and increased neural tube defects in embryos of the sensitive but not of the resistant Cohen diabetic rats cultured under diabetic conditions. Birth Defects Res A Clin Mol Teratol 67(6):429–437. https://doi.org/10.1002/bdra.10043

    Article  CAS  PubMed  Google Scholar 

  48. Ibuki FK, Bergamaschi CT, da Silva PM, Nogueira FN (2020) Effect of vitamin C and E on oxidative stress and antioxidant system in the salivary glands of STZ-induced diabetic rats. Arch Oral Biol 116:104765. https://doi.org/10.1016/j.archoralbio.2020.104765

    Article  CAS  PubMed  Google Scholar 

  49. Nissanka N, Moraes CT (2018) Mitochondrial DNA damage and reactive oxygen species in neurodegenerative disease. FEBS Lett 592(5):728–742. https://doi.org/10.1002/1873-3468.12956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Krylatov AV, Maslov LN, Voronkov NS, Boshchenko AA, Popov SV, Gomez L, Wang H, Jaggi AS, Downey JM (2018) Reactive oxygen species as intracellular signaling molecules in the cardiovascular system. Curr Cardiol Rev 14(4):290–300. https://doi.org/10.2174/1573403x14666180702152436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Volpe CMO, Villar-Delfino PH, Dos Anjos PMF, Nogueira-Machado JA (2018) Cellular death, reactive oxygen species (ROS) and diabetic complications. Cell Death Dis 9(2):119. https://doi.org/10.1038/s41419-017-0135-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Liao Z, Chua D, Tan NS (2019) Reactive oxygen species: a volatile driver of field cancerization and metastasis. Mol Cancer 30 18(1):65. https://doi.org/10.1186/s12943-019-0961-y

  53. Halliwell B, Gutteridge JM (1986) Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch Biochem Biophys 246(2):501–514. https://doi.org/10.1016/0003-9861(86)90305-x

    Article  CAS  PubMed  Google Scholar 

  54. Halliwell B (2012) Free radicals and antioxidants: updating a personal view. Nutr Rev 70(5):257–265. https://doi.org/10.1111/j.1753-4887.2012.00476.x

    Article  PubMed  Google Scholar 

  55. Stvolinskii S, Fedorova T, Yuneva M (2003) Boldyrev a (2003) protective effect of carnosine on cu, Zn-superoxide dismutase during impaired oxidative metabolism in the brain in vivo. Bull Exp Biol Med 135(2):130–132. https://doi.org/10.1023/a:1023855428130

    Article  CAS  PubMed  Google Scholar 

  56. Salo DC, Pacifici RE, Lin SW, Giulivi C, Davies K (1990) Superoxide dismutase undergoes proteolysis and fragmentation following oxidative modification and inactivation. J Biol Chem 265(20):11919–11927

    Article  CAS  PubMed  Google Scholar 

  57. He M, Siow RC, Sugden D, Gao L, Cheng X, Mann GE (2011) Induction of HO-1 and redox signaling in endothelial cells by advanced glycation end products: a role for Nrf2 in vascular protection in diabetes. Nutr Metab Cardiovasc Dis 21(4):277–285. https://doi.org/10.1016/j.numecd.2009.12.008

    Article  CAS  PubMed  Google Scholar 

  58. Negi G, Kumar A, Joshi RP, Sharma SS (2011) Oxidative stress and Nrf2 in the pathophysiology of diabetic neuropathy: old perspective with a new angle. Biochem Biophys Res Commun 29 408(1):1–5. https://doi.org/10.1016/j.bbrc.2011.03.087

    Article  CAS  Google Scholar 

  59. Jiménez-Osorio AS, Picazo A, González-Reyes S, Barrera-Oviedo D, Rodríguez-Arellano ME, Pedraza-Chaverri J (2014) Nrf2 and redox status in prediabetic and diabetic patients. Int J Mol Sci 15(11):20290–20305. https://doi.org/10.3390/ijms151120290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Aragno M, Tamagno E, Gatto V, Brignardello E, Parola S, Danni O, Boccuzzi G (1999) Dehydroepiandrosterone protects tissues of streptozotocin-treated rats against oxidative stress. Free Rad Biol Med 26(11–12):1467–1474. https://doi.org/10.1016/s0891-5849(99)00012-x

    Article  CAS  PubMed  Google Scholar 

  61. Maritim AC, Moore BH, Sanders RA, Watkins JB III (1999) Effects of melatonin on oxidative stress in streptozotocin-induced diabetic rats. Int J Toxicol 18(3):161–166. https://doi.org/10.1080/109158199225440

    Article  CAS  Google Scholar 

  62. Townsend DM, Tew KD, Tapiero H (2003) The importance of glutathione in human disease. Biomed Pharmacother 57(3–4):145–155. https://doi.org/10.1016/s0753-3322(03)00043-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Maritim AC, Sanders RA, Watkins JB 3rd (2003) Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol 17(1):24–38. https://doi.org/10.1002/jbt.10058

    Article  CAS  PubMed  Google Scholar 

  64. Lutchmansingh FK, Hsu JW (2018) Glutathione metabolism in type 2 diabetes and its relationship with microvascular complications and glycemia. PLoS One 13(6):e0198626. https://doi.org/10.1371/journal.pone.0198626 eCollection 2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Sekhar RV, McKay SV, Patel SG, Guthikonda AP, Reddy VT, Balasubramanyam A, Jahoor F (2011) Glutathione synthesis is diminished in patients with uncontrolled diabetes and restored by dietary supplementation with cysteine and glycine. Diabetes Care 34(1):162–167. https://doi.org/10.2337/dc10-1006

    Article  CAS  PubMed  Google Scholar 

  66. Ahmad M, Khan MA, Khan AS (2003) Naturally occurring antioxidant vitamin levels in patients with type-II diabetes mellitus. J Ayub Med Coll Abbottabad 15(1):54–57

    PubMed  Google Scholar 

  67. Pazdro R, Burgess JR (2010) The role of vitamin E and oxidative stress in diabetes complications. Mech Ageing Dev 131(4):276–286. https://doi.org/10.1016/j.mad.2010.03.005

    Article  CAS  PubMed  Google Scholar 

  68. van Haaften RI, Haenen GR, Evelo CT, Bast A (2003) Effect of vitamin E on glutathione-dependent enzymes. Drug Metab Rev 35(2–3):215–253. https://doi.org/10.1081/dmr-120024086

    Article  PubMed  Google Scholar 

  69. Meister A (1994) Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem 269(13):9397–9400

    Article  CAS  PubMed  Google Scholar 

  70. Bravi MC, Armiento A, Laurenti O, Cassone-Faldetta M, De Luca O, Moretti A, De Mattia G (2006) Insulin decreases intracellular oxidative stress in patients with type 2 diabetes mellitus. Metabolism 55(5):691–695. https://doi.org/10.1016/j.metabol.2006.01.003

    Article  CAS  PubMed  Google Scholar 

  71. Nicolau J, Sassaki KT (1976) Metabolism of carbohydrate in the major salivary glands of rats. Arch Oral Biol 21(11):659–661. https://doi.org/10.1016/0003-9969(76)90140-0

    Article  CAS  PubMed  Google Scholar 

  72. Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria J Med 54(4):287–293. https://doi.org/10.1016/j.ajme.2017.09.001

    Article  Google Scholar 

  73. Jo S-H, Son M-K, Koh H-J, Lee S-M, Song I-H, Kim Y-O, Lee Y-S, Jeong K-S, Kim WB, Park J-W (2001) Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J Biol Chem 276(19):16168–16176. https://doi.org/10.1074/jbc.M010120200

    Article  CAS  PubMed  Google Scholar 

  74. Schowen RL (1993) Principles of biochemistry 2nd ed.(Lehninger, Albert L.; Nelson, David L.; cox, Michael M.). ACS publications

  75. Leite MF (2006) Estudo temporal do efeito da administração de tungstato de sódio sobre alguns parâmetros de glândulas salivares e saliva de ratas diabéticas. Universidade de São Paulo

  76. Pastore A, Federici G, Bertini E, Piemonte F (2003) Analysis of glutathione: implication in redox and detoxification. Clin Chim Acta 333(1):19–39. https://doi.org/10.1016/s0009-8981(03)00200-6

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by CAPES (Projects 001 and 88881.062183/2014-01) and FAPESP (2013/18609-1).

Author information

Authors and Affiliations

  1. Department of Biomaterials and Oral Biology, School of Dentistry, University of São Paulo, São Paulo, Brazil

    Douglas Nesadal de Souza, Eugen Mendes Nesadal de Souza, Marlus da Silva Pedrosa, Fernando Neves Nogueira, Alyne Simões & José Nicolau

Authors
  1. Douglas Nesadal de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eugen Mendes Nesadal de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marlus da Silva Pedrosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fernando Neves Nogueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alyne Simões
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. José Nicolau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marlus da Silva Pedrosa.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Souza, D.N., de Souza, E.M.N., da Silva Pedrosa, M. et al. Effect of Tungstate Administration on the Lipid Peroxidation and Antioxidant Parameters in Salivary Glands of STZ-Induced Diabetic Rats. Biol Trace Elem Res 199, 1525–1533 (2021). https://doi.org/10.1007/s12011-020-02273-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-020-02273-x

Keywords

Search

Navigation