Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 36, pp 36462–36473 | Cite as

Attenuation of utero-toxicity, metabolic dysfunction and inflammation by soy protein concentrate in rats exposed to fluoridated water: consequence of hyperlipidemia in parallel with hypohomocysteinemia

  • Lipirani Jana
  • Pikash Pratim Maity
  • Hasina Perveen
  • Moumita Dash
  • Suryashis Jana
  • Arindam Dey
  • Subrata Kumar De
  • Sandip Chattopadhyay
Research Article
  • 26 Downloads

Abstract

Lipid peroxidation and ROS generation are the pathogenesis of chronic fluoride toxicity, and its detrimental effects on human reproduction are noted drastically. The aim of the present study was to elucidate the defensive effects of soy protein concentrate (SPC) against sodium fluoride (NaF)-induced uterine dysfunction at biochemical and histological level. Rats were randomly distributed into four groups as control, NaF-treated (200 ppm), and SPC co-administered groups (20 mg and 40 mg/ 100 g body weight) for 16 days. SPC reversed the toxic effects of NaF. SPC significantly ameliorated the NaF-induced alterations of the antioxidant system in the uterus by decreasing lipid peroxidation products and by increasing antioxidant activities. SPC significantly counteracted the adverse effects of NaF on serum level of lactate dehydrogenase (LDH) and inflammatory markers Interleukin-6 (IL-6), tumor necrosis factor alpha (TNF-α) and nuclear factor kappa-B (NF-κB). Our results also explored that lipid profile was meaningfully altered due to NaF and also focused a diminution of circulating homocysteine (Hcy) and altered lipid profiles along with a diminished quantity of serum B12 and B9. However, both the doses of SPC reverted back serum levels of B12, B9, and Hcy status in similar fashion along with its corrective action on lipid profile. NaF-treated group exhibited a marked degree of reduction in the weights of ovary and uterus with an alteration of normal tissue histology and significant diminution in serum estradiol (ES) levels without fluctuating uterine estradiol receptor-α (ER-α). However, SPC restored the normal tissue histoarchitecture and also increased the functional efficiency and expression of the ER-α receptor by overturning the ES levels in NaF-treated rats. Moreover, both the doses of SPC were effective against NaF-induced alterations, although 40 mg SPC/100 g body weight had better efficacy in ameliorating the NaF-induced adverse effects on the uterus and ovary.

Keywords

Soy protein concentrate Antioxidant system Estradiol Homocysteine and lipid profile Vitamins Uterus and ovary 

Abbreviations

CAT

Catalase

CD

Conjugated dienes

ES

Estradiol

ER-α

Estradiol receptor-α

GPx

Glutathione peroxidase

Hcy

Homocysteine

HDL

High density lipoprotein

IL-6

Interleukin-6

LDH

Lactate dehydrogenase

LDL

Low density lipoprotein

MDA

Malondialdehyde

NaF

Sodium fluoride

NF-κB

Nuclear factor kappa B

NPSH

Non-protein soluble thiol

ROS

Reactive oxygen species

SGOT

Serum glutamic oxaloacetic transaminase

SGPT

Serum glutamic pyruvic transaminase

SOD

Superoxide dismutase

SPC

Soy protein concentrate

TNF-α

Tumor necrosis factor alpha

Notes

Funding information

This research was partially supported by a grant from UGC NET-JRF (Award Letter No. F.15-9(JULY 2016)/2016(NET) and UGC Ref. No.: 1111/(NET-JULY 2016).

Compliance with ethical standards

This study was performed following the guidelines of the Institutional Ethical Committee.

References

  1. Afolabi OK, Oyewo EB, Adekunle AS, Adedosu OT, Adedeji AL (2013) Oxidative indices correlate with dyslipidemia and pro-inflammatory cytokine levels in fluoride-exposed rats. Arch Ind Hyg Toxicol 64:521–529Google Scholar
  2. Ali N, Zhang L, Li L, Chan LH, Li B (2015) Effect of pressurized soy protein isolate upon the growth and antioxidants functions of SD rat. Food Nutri Sci 6:501Google Scholar
  3. Al-Khafaji F, Bowron A, Day AP, Scott J, Stansbie D (1998) Stabilization of blood homocysteine by 3-deazaadenosine. Ann Clin Biochem 35:780–782Google Scholar
  4. Anderson JW, Blake JE, Turner J, Smith BM (1998) Effects of soy protein on renal function and proteinuria in patients with type 2 diabetes. Am J Clin Nutr 68:1347–1353Google Scholar
  5. Appelt LC, Reicks MM (1999) Soy induces phase II enzymes but does not inhibit dimethylbenz [a] anthracene-induced carcinogenesis in female rats. J Nutr 129:1820–1826Google Scholar
  6. Atmaca G (2004) Antioxidant effects of sulfur-containing amino acids. Yonsei Med J 45:776–788Google Scholar
  7. Aukema HM, Housini I (2001) Dietary soy protein effects on disease and IGF-I in male and female Han: SPRD-cy rats. Kidney Int 59:52–61Google Scholar
  8. Bachinskiĭ PP, Gutsalenko OA, Naryzhniuk ND, Sidora VD, Shliakhta AI (1985) Action of the body fluorine of healthy persons and thyroidopathy patients on the function of hypophyseal-thyroid the system. Probl Endokrinol (Mosk) 31:25–29Google Scholar
  9. Barbosa AC, Lajolo FM, Genovese MI (2011) Effect of free or protein-associated soy isoflavones on the antioxidant status in rats. J Sci Food Agri 91:721–731Google Scholar
  10. Baum JA, Teng H, Erdman JW Jr, Weigel RM, Klein BP, Persky VW, Freels S, Surya P, Bakhit RM, Ramos E, Shay NF (1998) Long-term intake of soy protein improves blood lipid profiles and increases mononuclear cell low-density-lipoprotein receptor messenger RNA in hypercholesterolemic, postmenopausal women. Am J Clin Nutr 68:545–551Google Scholar
  11. Bauman WA, Shaw S, Jayatilleke E, Spungen AM, Herbert V (2000) Increased intake of calcium reverses vitamin B12 malabsorption induced by metformin. Diabetes Care 23:1227–1231Google Scholar
  12. Bouaziz H, Fetoui H, Ketata S, Jammoussi K, Ellouze F, Zeghal N (2006a) Effects of sodium fluoride ingested by lactating mice on some haematological parameters in suckling pups and dams. Fluoride 39:211–219Google Scholar
  13. Bouaziz H, Ketata S, Jammoussi K, Boudawara T, Ayedi F, Ellouze F, Zeghal N (2006b) Effects of sodium fluoride on hepatic toxicity in adult mice and their suckling pups. Pestic Biochem Physiol 86:124–130Google Scholar
  14. Brandt RB, Laux JE, Spainhour SE, Kline ES (1987) Lactate dehydrogenase in rat mitochondria. Arch Biochem Biophys 259:412–422Google Scholar
  15. Burris RL, Nag HP, Nagarajan S (2014) Soy protein inhibits inflammation-induced VCAM-1 and inflammatory cytokine induction by inhibiting the NF-κB and AKT signaling pathway in apolipoprotein E–deficient mice. Eur J Nutr 53:135–148Google Scholar
  16. Campbell MF, Kraut CW, Yackel WC, Yang HS (1985) Soy protein concentrate. In: Altschul AM, Wilcke HL (eds) New protein foods: seed storage proteins 5. Academic pressGoogle Scholar
  17. CGWB (2015) Groundwater quality scenario in India. In: Central ground water board. Government of India, New DelhiGoogle Scholar
  18. Collins TF, Sprando RL, Shackelford ME, Black TN, Ames MJ, Welsh JJ, Balmer MF, Olejnik N, Ruggles DI (1995) Developmental toxicity of sodium fluoride in rats. Food Chem Toxicol 33:951–960Google Scholar
  19. Despres JP (2006) Abdominal obesity: the most prevalent cause of the metabolic syndrome and related cardiometabolic risk. Eur Heart J 8(1):B4–B12Google Scholar
  20. Devasagayam TP, Boloor KK, Ramasarma T (2003) Methods for estimating lipid peroxidation: an analysis of merits and demerits. Ind J Biochem Biophys 40:300–308Google Scholar
  21. Dhurvey V, Thakare M (2016) The effect of sodium fluoride intoxication on the estrous cycle and ovarian hormones in rats. Fluoride 49:223Google Scholar
  22. Dhurvey V, Patil V, Thakare M (2017) Effect of sodium fluoride on the structure and function of the thyroid and ovary in albino rats (rattus norvegicus). Fluoroide 50:235–246Google Scholar
  23. Drent M, Cobben NA, Henderson RF, Wouters EF, van Dieijen-Visser M (1996) Usefulness of lactate dehydrogenase and its isoenzymes as indicators of lung damage or inflammation. Eur Respir J 9:1736–1742Google Scholar
  24. Emsley J, Jones DJ, Miller JM, Overill RE, Waddilove RA (1981) An unexpectedly strong hydrogen bond: ab initio calculations and spectroscopic studies of amide-fluoride systems. J Am Chem Soc 103:24–28Google Scholar
  25. FAO/WHO (1989) Protein quality evaluation: report of the joint FAO/WHO expert consultation. Food and Agriculture Organization of the United Nations (Food and Nutrition Paper), Bethesda, p 51Google Scholar
  26. Food and Drug Administration (1999) Food labeling health claims; soy protein and coronary heart disease. Fed Regist 64:57699–57733Google Scholar
  27. Galvez AF, Chen N, Macasieb J, Ben O (2001) Chemopreventive property of a soybean peptide (lunasin) that binds to deacetylated histones and inhibits acetylation. Cancer Res 61:7473–7478Google Scholar
  28. Gawel S, Wardas M, Niedworok E, Wardas P (2004) Malondialdehyde (MDA) as a lipid peroxidation marker. Wiadomoscilekarskie 57:453–455Google Scholar
  29. Ghosh D, Das S, Maiti R, Jana D, Das UB (2002) Testicular toxicity in sodium fluoride treated rats: association with oxidative stress. ReprodToxicol 16:385–390Google Scholar
  30. Ghosh S, Willard B, Comhair SA, Dibello P, Xu W, Shiva S, Aulak KS, Kinter M, Erzurum SC (2013) Disulfide bond as a switch for copper-zinc superoxide dismutase activity in asthma. Antioxid Redox Signal 18(4):412–423Google Scholar
  31. Gudbrandsen OA, Wergedahl H, Mørk S, Liaset B, Espe M, Berge RK (2006) Dietary soya protein concentrate enriched with isoflavones reduced fatty liver, increased hepatic fatty acid oxidation and decreased the hepatic mRNA level of VLDL receptor in obese Zucker rats. Br J Nutr 96:249–257Google Scholar
  32. Hadwan MH (2016) New method for assessment of serum catalase activity. Indian J Sci Technol 9:1–5Google Scholar
  33. Hanson LN, Engelman HM, Alekel DL, Schalinske KL, Kohut ML, Reddy MB (2006) Effects of soy isoflavones and phytate on homocysteine, C-reactive protein, and iron status in postmenopausal women. Am J Clin Nutr 84:774–780Google Scholar
  34. Helmy SA, Emarah HA, Abdelrazek HM (2014) Estrogenic effect of soy phytoestrogens on the uterus of ovariectomized female rats. Clin Pharmacol Biopharmaceut 2:1–7Google Scholar
  35. Hernández-Ledesma B, Hsieh CC, Ben O (2009) Antioxidant and anti-inflammatory properties of cancer preventive peptide lunasin in RAW 2647 macrophages. Biochem Biophys Res Commun 390:803–808Google Scholar
  36. Herrmann W, Obeid R, Hübner U, Jouma M, Geisel J (2004) Homocysteine in relation to C-reactive protein and low-density lipoprotein cholesterol in assessment of cardiovascular risk. Cell Mol Biol 50:895–901Google Scholar
  37. Hirano T, Takahashi T, Saito S, Tajima H, Ebara T, Adachi M (2001) Apoprotein C-III deficiency markedly stimulates triglyceride secretion in vivo: comparison with apoprotein E. Am J Physiol Endocrinol Metab 281:665–669Google Scholar
  38. Hofmann MA, Lalla E, Lu Y, Gleason MR, Wolf BM, Tanji N, Ferran LJ, Kohl B, Rao V, Kisiel W, Stern DM (2001) Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model. J Clin Invest 107:675–683Google Scholar
  39. Hubert J, Berger M, Dayde J (2005) Use of simplified HPLC-UV analysis for soya saponin B determination: study of saponin and isoflavones variability in soybean cultivars and soy-based health food products. J Agric Food Chem 53:3923–3930Google Scholar
  40. Jaric I, ZivanoviC J, Miler M, Ajdzanovic V, Blagojevic D, Ristic N, Milosevic V, Nestorovic N (2018) Genistein and daidzein treatments differently affect uterine homeostasis in the ovary-intact middle-aged rats. Toxicol Appl Pharmacol 339:73–84Google Scholar
  41. Jhala DD, Nair SB, Chinoy NJ (2004) Reversible toxicity of fluoride and arsenic in ovary of mice. Fluoride 37:71–79Google Scholar
  42. Kamata H, Honda SI, Maeda S, Chang L, Hirata H, Karin M (2005) Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120:649–661Google Scholar
  43. Kamble N, Velhal V (2010) Cytopathological assessment of uterine cells in rattus norvegicus due to induced sodium fluoride. Bioscan 27:301–303Google Scholar
  44. Kojima M, Sekikawa K, Nemoto K, Degawa M (2005) Tumor necrosis factor-alpha independent downregulation of hepatic cholesterol 7alpha hydroxylase gene in mice treated with lead nitrate. Toxicol Sci 87:537–542Google Scholar
  45. Kumar A (2012) Effect of simuastation on paraxonase 1 (PON1) activity and oxidation stress in: Kumar a (ed) significance of lipid profile assay as diagnostic and prognostic tool. CreateSpace Independent Publishing Platform, California, pp 105–109Google Scholar
  46. Lawson PB, Yu MH (2003) Fluoride inhibition of superoxide dismutase (SOD) from the earthworm Eisenia fetida. Fluoride 36:143–151Google Scholar
  47. Liu J, Du J, Zhang Y, Sun W, Smith BJ, Oberley LW, Cullen JJ (2006) Suppression of the malignant phenotype in pancreatic cancer by overexpression of phospholipid hydroperoxide glutathione peroxidase. Hum Gene Ther 17:105–116Google Scholar
  48. Lohakare JD, Pattanaik AK (2013) Effects of addition of fluorine in diets differing in protein content on urinary fluoride excretion, clinical chemistry and thyroid hormones in calves. Rev Bras Zootec 42:751–758Google Scholar
  49. Lu Y, Luo Q, Cui H, Deng H, Kuang P, Liu H, Fang J, Zuo Z, Deng J, Li Y, Wang X (2017) Sodium fluoride causes oxidative stress and apoptosis in the mouse liver. Aging (Albany NY) 9:1623–1639Google Scholar
  50. Luo Q, Cui H, Deng H, Kuang P, Liu H, Lu Y, Fang J, Zuo Z, Deng J, Li Y, Wang X (2017) Sodium fluoride induces renal inflammatory responses by activating NF-κB signaling pathway and reducing anti-inflammatory cytokine expression in mice. Oncotarget 8:80192–80207Google Scholar
  51. Malanovic N, Streith I, Wolinski H, Rechberger G, Kohlwein SD, Tehlivets O (2008) S-adenosyl-L-homocysteine hydrolase, key enzyme of methylation metabolism, regulates phosphatidylcholine synthesis and triacylglycerol homeostasis in yeast implications for homocysteine as a risk factor of atherosclerosis. J Biol Chem 283:23989–23999Google Scholar
  52. Mehdi S, Jarvi ET, Koehl JR, McCarthy JR, Bey P (1990) The mechanism of inhibition of S-adenosyl-L-homocysteine hydrolase by fluorine-containing adenosine analogs. J Enzyme Inhib 4:1–13Google Scholar
  53. Menoyo I, Rigalli A, Puche RC (2005) Effect of fluoride on the secretion of insulin in the rat. Arzneimittelforschung 55:455–460Google Scholar
  54. Michelfelder AJ (2009) Soy: a complete source of protein. Am Fam Physician 79:43–47Google Scholar
  55. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, Shelton MD (2008) Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Rignal 10:1941–1988Google Scholar
  56. Milman N (2012) Intestinal absorption of folic acid-new physiologic & molecular aspects. Indian J Med Res 136:725Google Scholar
  57. Minaei M, Fazelipour S, Tootian Z, Minaei M (2017) The effect of cost effective and useful diets on blood parameters in female mice. Food Nutr Sci 8:474–484Google Scholar
  58. Mohammed IA, Al-Okaily BN (2017) Effect of sodium fluoride on liver functions of rats and amelioration by CoQ10. J Entomol Zool Stud 5:887–893Google Scholar
  59. Nagata C, Shimizu H, Takami R, Hayashi M, Takeda N, Yasuda K (2003) Soy product intake is inversely associated with serum homocysteine level in premenopausal Japanese women. J Nutr 133:797–800Google Scholar
  60. Obeid R, Herrmann W (2009) Homocysteine and lipids: S-adenosyl methionine as a key intermediate. FEBS Lett 58:1215–1225Google Scholar
  61. Paglia DE, Valentine WN (1967) Studies on quantitative and qualitative characterization of erythrocyte glutathione peroxidise. J Lab Clin Med 70:158–169Google Scholar
  62. Pattichis K, Louca LL, Glover V (1994) Quantitation of soluble superoxide dismutase in rat Striata, based on the inhibition of nitrite formation from hydroxylammonium chloride. Anal Biochem 221:428–431Google Scholar
  63. Potter SM (1995) Overview of proposed mechanisms for the hypocholesterolemic effect of soy. J Nutr 125:606–611Google Scholar
  64. Reddy KS, Reddy NV, Niharika P, Reddy MA, Reddy H, Daneswari V (2017) Defluoridation of water using natural adsorbents. Int J Pedod Rehabil 2:51–54Google Scholar
  65. Sauerheber R (2013) Physiologic conditions affect toxicity of ingested industrial fluoride. J Environ Public Health 2013:13Google Scholar
  66. Sharma JD, Solanki M, Solanki D (2007) Sodium fluoride toxicity on reproductive organs of female albino rats. Asian J Exp Sci 21:359–364Google Scholar
  67. Shin DS, DiDonato M, Barondeau DP, Hura GL, Hitomi C, Berglund JA, Getzoff ED, Cary SC, Tainer JA (2009) Superoxide dismutase from the eukaryotic thermophile Alvinella pompejana: structures, stability, mechanism, and insights into amyotrophic lateral sclerosis. J Mol Biol 385:1534–1555Google Scholar
  68. Sorescu D, Weiss D, Lassègue B, Clempus RE, Szöcs K, Sorescu GP, Valppu L, Quinn MT, Lambeth JD, Vega JD, Taylor WR (2002) Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 105:1429–1435Google Scholar
  69. Soulsby ME, Phillips B, Chowdhury P (2004) Effects of soy-protein diet on elevated brain lipid peroxide levels induced by simulated weightlessness. Ann Clin Lab Sci 34:103–106Google Scholar
  70. Stubbe J, Nocera DG, Yee CS, Chang MC (2003) Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer. Chem Rev 103:2167–2202Google Scholar
  71. Sumona B, Sheetal S, Anil M, Suvarna P (2011) Comparative evaluation of serum folic acid levels in smokers and non-smokers with chronic periodontitis. Bangladesh J Med Sci 10:83–90Google Scholar
  72. Thakare MT, Dhurvey VT (2014) Histopathological changes in the uterus of rats after an administration of sodium fluoride. Int J Scienti Res 3:63–65Google Scholar
  73. Tolba EA (2013) Dietary phytoestrogens reduce the leptin level in ovariectomized female rats. Int J Chem Environ Biol Sci 1:496–500Google Scholar
  74. Vacek J, Klejdus B, Lojková L, Kubán V (2008) Current trends in isolation, separation, determination and identification of isoflavones: a review. J Sep Sci 31:2054–2067Google Scholar
  75. Wang J, Niu R, Sun Z, Lv LH, Smith GW, Wang JD (2008) Effects of protein and calcium supplementation on bone metabolism and thyroid function in protein and calcium deficient rabbits exposed to fluoride. Fluoride 41:283–291Google Scholar
  76. Weydert CJ, Cullen JJ (2010) Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat Protoc 5:51–66Google Scholar
  77. WHO (2004) Guidelines for drinking-water quality: recommendations. World Health OrganizationGoogle Scholar
  78. Winarsi H, Purwanto A, Dwiyanti H (2010) Protein and isoflavone content in soybean and soy germ. J Biota 15:186–193Google Scholar
  79. Yamaguti PM, Simões A, Ganzerla E, Souza DN, Nogueira FN, Nicolau J (2013) Effects of single exposure of sodium fluoride on lipid peroxidation and antioxidant enzymes in salivary glands of rats. Oxidative Med Cell Longev 2013:1–7Google Scholar
  80. Zhan S, Ho SC (2005) Meta-analysis of the effects of soy protein containing isoflavones on the lipid profile. Am J Clin Nutr 81:397–408Google Scholar
  81. Zhan XA, Wang M, Xu ZR, Li JX, Li JX (2006) Toxic effects of fluoride on kidney function and histological structure in young pigs. Fluoride 39:22–26Google Scholar
  82. Zhou Y, Zhang H, He J, Chen X, Ding Y, Wang Y, Liu X (2013) Effects of sodium fluoride on reproductive function in female rats. Food Chem Toxicol 56:297–303Google Scholar
  83. Zhou Y, Qiu Y, He J, Chen X, Ding Y, Wang Y, Liu X (2013a) The toxicity mechanism of sodium fluoride on fertlity in female rats. Food Chem Toxicol 56:297–303Google Scholar
  84. Zhuo XG, Melby MK, Watanabe S (2004) Soy isoflavones intake lowers serum LDL cholesterol: a metaanalysis of 8 randomized controlled trials in humans. J Nutr 134:2395–2400Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Lipirani Jana
    • 1
  • Pikash Pratim Maity
    • 1
  • Hasina Perveen
    • 1
  • Moumita Dash
    • 1
  • Suryashis Jana
    • 1
  • Arindam Dey
    • 1
  • Subrata Kumar De
    • 2
  • Sandip Chattopadhyay
    • 1
  1. 1.Department of Biomedical Laboratory Science and Management, and Clinical Nutrition and Dietetics division (UGC Innovative Department)Vidyasagar UniversityMidnaporeIndia
  2. 2.Department of ZoologyVidyasagar UniversityMidnaporeIndia

Personalised recommendations