Skip to main content
SpringerLink
Log in

Glycine max (soy) based diet improves antioxidant defenses and prevents cell death in cadmium intoxicated lungs

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Cadmium (Cd) is a toxic metal and an important environmental contaminant. We analyzed its effects on oligoelements, oxidative stress, cell death, Hsp expression and the histoarchitecture of rat lung under different diets, using animal models of subchronic cadmium intoxication. We found that Cd lung content augmented in intoxicated groups: Zn, Mn and Se levels showed modifications among the different diets, while Cu showed no differences. Lipoperoxidation was higher in both intoxicated groups. Expression of Nrf-2 and SOD-2 increased only in SoCd. GPx levels showed a trend to increase in Cd groups. CAT activity was higher in intoxicated groups, and it was higher in Soy groups vs. Casein. LDH activity in BAL increased in CasCd and decreased in both soy-fed groups. BAX/Bcl-2 semiquantitative ratio showed similar results than LDH activity, confirmed by Caspase 3 immunofluorescence. The histological analysis revealed an infiltration process in CasCd lungs, with increased connective tissue, fused alveoli and capillary fragility. Histoarchitectural changes were less severe in soy groups. Hsp27 expression increased in both intoxicated groups, while Hsp70 only augmented in SoCd. This show that a soy-diet has a positive impact upon oxidative unbalance, cell death and morphological changes induced by Cd and it could be a good alternative strategy against Cd exposure.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126

    CAS  Google Scholar 

  • Ahamed M, Akhtar MJ, Alaizeri ZM, Alhadlaq HA (2020) Tio2 nanoparticles potentiated the citotoxicity, oxidative stress and apoptosis response of cadmium in two different human cells. Environ Sci Pollut Res Int 27:10425–10435

    CAS  PubMed  Google Scholar 

  • Al-Gnami SA (2014) Effect of polyphenols which extracted from green tea in reduce toxic effects of cadmium sulfate in rat’s livers. Pharm Biol Sci 9:53–58

    Google Scholar 

  • Alvarez SM, Gomez NN, Scardapane L, Zirulnik F, Martinez D, Gimenez MS (2004) Morphological changes and oxidative stress in rat prostate exposed to a non-carcinogenic dose of cadmium. Toxicol Lett 153:365–376

    CAS  PubMed  Google Scholar 

  • Alvarez S, Gómez N, Scardapane L, Fornés M, Giménez M (2006) Effects of chronic exposure to cadmium on prostate lipids and morphology. Biometals 20:727–741

    PubMed  Google Scholar 

  • ATSDR (Agency for Toxic Substances, Disease Registry) (2008) Toxicological profile for cadmium US Department of Health and Human Service. Public Health Service Agency for Toxic undefinedubundefinedtanceundefined and Diundefinedeaundefinede Regiundefinedtry, Atlanta

    Google Scholar 

  • Bansal N, Parle M (2010) Soybean supplementation helps reverse age- and scopolamine-induced memory deficits in mice. J Med Food 13:1293–1300

    CAS  PubMed  Google Scholar 

  • Barnes S (1998) Evolution of the health benefits of soy isoflavones. Proc Soc Exp Biol Med 217:386–392

    CAS  PubMed  Google Scholar 

  • Beyersmann D, Hechtenberg S (1997) Cadmium, gene regulation, and cellular signaling in mammalian cells. Toxicol Appl Pharmacol 144:247–261

    CAS  PubMed  Google Scholar 

  • Beyersmann D, Hartwig A (2008) Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82:493–512

    CAS  PubMed  Google Scholar 

  • Biaggio VS, Alvarez-Olmedo DG, Perez Chaca MV, Salvetti NR, Valdez SR, Fanelli MA, Ortega HH, Gomez NN, Gimenez MS (2014) Cytoprotective mechanisms in rats lung parenchyma with zinc deprivation. Biometals 27(2):305–315

    CAS  PubMed  Google Scholar 

  • Borie R, Crestani B (2018) Antineutrophil cytoplasmic antibodies-associated lung fibrosis. Semin Respir Crit Care Med 39:465–470

    PubMed  Google Scholar 

  • Byun J, Han Y, Lee S (2010) The effects of yellow soybean, black soybean, and sword bean on lipid levels and oxidative stress in ovariectomized rats. Int J Vitam Nutr Res 80:97–106

    CAS  PubMed  Google Scholar 

  • Caisova´ D, Eybl V (1997) The influence of repeated administration of cadmium and lead on the activity of glutathione peroxidase and lipid peroxidation in mice. Biomarkers Environ 2:57–60

    Google Scholar 

  • Casalino E, Calzaretti G, Sblano C, Landriscina C (2002) Molecular inhibitory mechanisms of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology 179:37–50

    CAS  PubMed  Google Scholar 

  • Charab M, Abouzeinab N, Moustafa M (2016) The protective effect of selenium on oxidative stress induced by waterpipe (narghile) smoke in lungs and liver of mice. Biol Trace Elem Res 174:392–401

    CAS  PubMed  Google Scholar 

  • Chen G, Zhao L, Bao S, Cong T (2006) Effects of different proteins on the metabolism of Zn, Cu, Fe and Mn in rats. Biol Trace Elem Res 113:165–175

    CAS  PubMed  Google Scholar 

  • Ckless K, van der Vliet A, Janssen-Heininger Y (2007) Oxidative-nitrosative stress and post-translational protein modifications: implications to lung structure-function relations. Arginase modulates NF-kappaB activity via nitric oxide-dependent mechanism. Am J Respir Cell Mol Biol 36:645–653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Della Latta V, Cecchettini A, del Ry S, Morales M (2015) Bleomycin in the setting of lung fibrosis induction: from biological mechanisms to counteractions. Pharmacol Res 97:122–130

    CAS  PubMed  Google Scholar 

  • Draper H, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431

    CAS  PubMed  Google Scholar 

  • Drent M, Cobben N, Henderson R, Jacobs J, Wouters E, van Dieijen-Visser M (1996) BAL fluid LDH activity and LDH isoenzyme pattern in lipoid pneumonia caused by an intravenous injection of lamp oil. Eur Respir J 9:2416–2418

    CAS  PubMed  Google Scholar 

  • Dua K, Malyla V, Singhvi G, Wadhwa R, Krishna R, Shukla S, Shastri M, Chellappan D, Maurya P, Satija S, Mehta M, Gulati M, Hansbro N, Collet T, Awasthi R, Gupta G, Hsu A, Hansbro P (2019) Increasing complexity and interactions of oxidative stress in chronic respiratory diseases: an emerging need for novel drugs delivery systems. Chem Biol Interact 299:168–178

    CAS  PubMed  Google Scholar 

  • Dwivedi VK, Bhatanagar A, Chaudhary M (2012) Protective role of ceftriaxone plus sulbactam with VRP1034 on oxidative stress, hematological and enzymatic parameters in cadmium toxicity induced rat model. Interdiscip Toxicol 5(4):192–200

    CAS  PubMed  PubMed Central  Google Scholar 

  • El-Demerdash FM, Yousef MI, Kedwany FS, Baghdadi HH (2004) Cadmium-induced changes in lipid peroxidation, blood hematology, biochemical parameters and semen quality of male rats: protective role of vitamin E and β-carotene. Food Chem Toxicol 42:1563–1571

    CAS  PubMed  Google Scholar 

  • Erbas D, Soncul H, Turkozkan N, Arioioglu A, Muftugoglu S, Ersoz A (1995) Effect of selenium in ischemic and reperfusion injury in isolated guinea pig lungs. Gen Pharmacol 26:1669–1672

    CAS  PubMed  Google Scholar 

  • Erikson K, Aschner M (2019) Manganese: its role in disease and health. Met Ions Life Sci 19:253–266

    CAS  Google Scholar 

  • Ferramola M, Anton R, Anzulovich A, Gimenez M (2011) Myocardial oxidative stress following sub-chronic and chronic oral cadmium exposure in rats. Environ Toxicol Pharmacol 32:17–26

    CAS  PubMed  Google Scholar 

  • Ferramola M, Perez Diaz M, Honore S, Sanchez S, Anton R, Anzulovich A, Gimenez M (2012) Cadmium-induced oxidative stress and histological damage in myocardium Effects of a soy-based diet. Toxicol Appl Pharmcol 265:380–389

    CAS  Google Scholar 

  • Fulda S, Meyer E, Friesen C, Susin SA, Kroemer G, Debatin KM (2001) Cell type specific involvement of death receptor and mitochondrial pathways in drug-induced apoptosis. Oncogene 20:1063–1075

    CAS  PubMed  Google Scholar 

  • Genchi G, Sinicropi MS, Lauria G, Carocci A, Catalano A (2020) The effects of cadmium toxicity. Int J Environ Res Public Health 26(11):3782

    Google Scholar 

  • Gomez N, Fernandez M, Zirulnik F, Gil E, Scardapane L, Ojeda M, Gimenez M (2003) Chronic zinc deficiency induces an antioxidant adaptive response in rat lung. Exp Lung Res 29:485–502

    CAS  PubMed  Google Scholar 

  • Grose E, Richads J, Jaskot R, Menache M, Graham J, Dauterman W (1987) A comparative study of the effects of inhaled cadmium chloride and cadmium oxide: pulmonary response. J Toxicol Environ Health 21:219–232

    CAS  PubMed  Google Scholar 

  • Guilleminault L, Williams EJ, Scott HA, Berthon BS, Jensen M, Wood LG (2017) Diet and asthma: is it time to adapt our message? Nutrients 9(11):1227

    PubMed Central  Google Scholar 

  • Gulati S, Thannickal V (2019) The aging lung and idiopathic pulmonary fibrosis. Am J Med Sci 357:384–389

    PubMed  Google Scholar 

  • Hamada T, Tanimoto A, Sasaguri Y (1997) Apoptosis induced by cadmium. Apoptosis 2:359–367

    CAS  PubMed  Google Scholar 

  • Han S, Castranova V, Vallyathan V (2007) Comparative cytotoxicity of cadmium and mercury in a human bronchial epithelial cell line (BEAS-2B) and its role in oxidative stress and induction of heat shock protein 70. J Toxicol Environ Health A 70:852–860

    CAS  PubMed  Google Scholar 

  • Han YL, Sheng Z, Liu GD, Long LL, Wang YF, Yang WX, Zhu JQ (2015) Cloning, characterization and cadmium inducibility of metallothionein in the testes of the mudskipper Boleophthalmus pectinirostris. Ecotoxicol Environ Saf 119:1–8

    CAS  PubMed  Google Scholar 

  • Hassoun EA, Stohs SJ (1996) Cadmium-induced production of superoxide anion and nitric oxide, DNA single strand breaks and lactate dehydrogenase leakage in J774A.1 cell cultures. Toxicology 112(3):219–226

    CAS  PubMed  Google Scholar 

  • Hu R, Xu C, Shen G, Jain M, Khor T, Gopalkrishnan A, Lin W, Reddy B, Chan J, Kong A (2006) Gene expression profiles induced by cancer chemopreventive isothiocyanate sulforaphane in the liver of C57BL/6J mice and C57BL/6J/Nrf2 (–/–) mice. Cancer Lett 243:170–192

    CAS  PubMed  Google Scholar 

  • Hu X, Fernandes J, Jones D, Go Y (2017) Cadmium stimulates myofibroblast differentiation and mouse lung fibrosis. Toxicology 383:50–56

    CAS  PubMed  Google Scholar 

  • IARC Monographs on the Evaluation of the Carcinogenic Risks to Humans (1993) Beryllium, cadmium, mercury, and exposures in the glass manufacturing industry. International Agency for Research on Cancer, Lyon, France, No.  58, pp 119–238

  • Ikediobi C, Badisa V, Ayuk-Takem L, Latinwo L, West J (2004) Response of antioxidant enzymes and redox metabolites to cadmium-induced oxidative stress in CRL-1439 normal rat liver cells. Int J Mol Med 14:87–92

    CAS  PubMed  Google Scholar 

  • Illesca PG, Álvarez SM, Selensciga DA, Ferreira M, Giménez R, Lombardo MS, DAlessandro YB, (2017) Dietary soy protein improves adipose tissue dysfunction by modulating parameters related with oxidative stress in dyslipidemic insulin-resistant rats. Biomed Pharmacother 88:1008–1015

    CAS  PubMed  Google Scholar 

  • Jaiswal A (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 36:1199–1207

    CAS  PubMed  Google Scholar 

  • Javid B, MacAry P, Lehner P (2007) Structure and function: heat shock proteins and adaptative immunity. J Immnol 179:2035–2040

    CAS  Google Scholar 

  • Jiang T, Sun Q, Chen S (2016) Oxidative stress: a major pathogenesis and potential therapeutic target of antioxidant agents in Parkinson’s disease and Alzheimer’s disease. Prog Neurobiol 147:1–19

    CAS  PubMed  Google Scholar 

  • Kameoka S, Leavitt P, Chang C, Kuo S-M (1999) Expression of antioxidant proteins in human intestinal Caco-2 cells treated with dietary flavonoids. Cancer Lett 146:161–167

    CAS  PubMed  Google Scholar 

  • Kim J, Ellwood P, Asher ML (2009) Diet and asthma: looking back, moving forward. Respir Res 10(1):49

    PubMed  PubMed Central  Google Scholar 

  • Kiran Kumar KM, Naveen Kumar M, Patil RH, Nagesh R, Hegde SM, Kavya K, Babu RL, Ramesh GT, Sharma SC (2016) Cadmium induces oxidative stress and apoptosis in lung epithelial cells. Toxicol Mech Methods 26(9):658–666

    CAS  PubMed  Google Scholar 

  • Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH et al (1995) Cytotoxicity-dependent APO-1(Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14:5579–5588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klimova B, Kuca K, Novotny M, Maresova P (2017) Cystic fibrosis revisited—a review study. Med Chem 13:102–109

    CAS  PubMed  Google Scholar 

  • Kun-Young K, Jae-Hwi J, Sun-Young K, Chi-Heum C, Hoon-Kyu O, Sang-Pyo K (2003) Cadmium induced acute lung injury and TUNEL expression of apoptosis in respiratory cells. J Korean Med Sci 18:655–662

    Google Scholar 

  • Kwak M, Wakabayashi N, Itoh K, Motohashi H, Yamamoto M, Kensler T (2003) Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway identification of novel gene clusters for cell survival. J Biol Chem 278:8135–8145

    CAS  PubMed  Google Scholar 

  • Labunskyy V, Hatfield D, Gladyshev V (2014) Selenoproteins: molecular pathways and physiological roles. Physiol Rev 94:739–777

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larregle E, Varas S, Oliveros L, Martinez L, Antón R, Marchevsky E, Giménez M (2008) Lipid metabolism in liver of rat exposed to cadmium. Food Chem Toxicol 46:1786–1792

    CAS  PubMed  Google Scholar 

  • Lei W, Wang L, Liu D, Xu T, Luo J (2011) Histopathological and biochemical alternations of the heart induced by acute cadmium exposure in the freshwater crab Sinopotamon yangtsekiense. Chemosphere 84:689–694

    CAS  PubMed  Google Scholar 

  • Leonard M, Kieran N, Howell K, Burne M, Varadarajan R, Dhakshinamoorthy S, Porter A, O’Farrelly C, Rabb H, Taylor C (2006) Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia–reperfusion injury. FASEB J 20:2624–2626

    CAS  PubMed  Google Scholar 

  • Li X, Gilmour P, Donaldson K, MacNee W (1996) Free radical activity and pro-inflammatory effects of particulate air polution (PM10) in vivo and in vitro. Thorax 51:1216–1222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Kondo T, Zhao QL, Li FJ, Tanabe K, Arai Y, Zhou ZC, Kasuya M (2000) Apoptosis induced by cadmium in human lymphoma U937 cells through Ca2+-calpain and caspase-mitochondria-dependent pathways. J Biol Chem 275:39702–39709

    CAS  PubMed  Google Scholar 

  • Liu T, Gonzalez de los Santos F, Phan S (2017) The bleomycin model of pulmonary fibrosis. Method Mol Biol 1627:27–42

    CAS  Google Scholar 

  • Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurement with Folin phenol reagent. J BiolChem 193:265–275

    CAS  Google Scholar 

  • Lu CF, Yuan XY, Li LZ, Zhou W, Zhao J, Wang YM, Peng SQ (2015) Combined exposure of nano-silica and lead induced potentiation of oxidative stress and DNA damage in human lung epithelial cells. Ecotoxicol Environ Saf 122:537–544

    CAS  PubMed  Google Scholar 

  • Luchese C, Brandão R, Oliveira R, Nogueira C, Santos F (2007) Efficacy of diphenil diselenide against cerebral and pulmonary damage induced by cadmium in mice. Toxicol Lett 173:181–190

    CAS  PubMed  Google Scholar 

  • Manca D, Ricard A, Trottier B, Chevalier G (1991) Studies of lipid peroxidation in rat tissues following administration of low and moderate doses of cadmium chloride. Toxicology 67:303–323

    CAS  PubMed  Google Scholar 

  • Manca D, Ricard A, Tra H, Chevalier G (1994) Relation between lipid peroxidation and inflammation in the pulmonary toxicity of cadmium. Arch Toxicol 68:364–369

    CAS  PubMed  Google Scholar 

  • Manna P, Sinha M, Sil P (2008) Amelioration of cadmium-induced cardiac impairment by taurine. Chem Biol Interact 174:88–97

    CAS  PubMed  Google Scholar 

  • Meyer K (2017) Pulmonary fibrosis, part I: epidemiology, pathogenesis and diagnosis. Expert Rev Respir Med 11:343–359

    CAS  PubMed  Google Scholar 

  • Min K, Fujita Y, Onosaka S, Tanaka K (1991) Role of intestinal metallothionein in absorption and distribution of orally administered cadmium. Toxicol Appl Pharmacol 109:7–16

    CAS  PubMed  Google Scholar 

  • Mohammadi F, Nezafat N, Negahdaripour M, Dabbagh F, Haghghi A, Kianpour S, Banihashemi M, Ghasemi Y (2018) Neuroprotective effects of heat shock protein 70. CNS Neurol Disord Drug Targets 17:736–742

    CAS  PubMed  Google Scholar 

  • Morel I, Lescoat G, Cogrel P, Sergent O, Pasdeloup N, Brissot P, Cillard P, Cillar J (1993) Antioxidant and iron-chelating activities of the flavonoids catechin, quercetin, and diosmetin on iron-loaded rat hepatocyte cultures. Biochem Pharmacol 45:13–19

    CAS  PubMed  Google Scholar 

  • Nemmiche S, Chabane-Sari D, Guiraud P (2007) Role of alpha-tocopherol in cadmium-induced oxidative stress in Wistar rat’s blood, liver and brain. Chem Biol Interact 170:221–230

    CAS  PubMed  Google Scholar 

  • Niewoehner D, Hoidal J (1982) Lung fibrosis and emphysema: divergent responses to a common injury? Science 217:359–360

    CAS  PubMed  Google Scholar 

  • Nordberg G (1972) Cadmium metabolism and toxicity. Environ Physiol Biochem 2:7–36

    CAS  Google Scholar 

  • Ofman G, Tipple T (2019) Antioxidants and bronchopulmonary dysplasia: beating the system or beating a dead horse? Free Radic Biol Med 142:138–145

    CAS  PubMed  Google Scholar 

  • Ognjanović B, Marković S, Pavlović S, Žikić R, Štajn A, Saičić Z (2008) Effect of chronic cadmium exposure on antioxidant defense system in some tissues of rats: effect of selenium. Physiol Res 57:403–411

    PubMed  Google Scholar 

  • Oh SH, Lee BH, Lim SC (2004) Cadmium induces apoptotic cell death in WI 38 cells via caspase-dependent Bid cleavage and calpain-mediated mitochondrial Bax cleavage by Bcl-2-independent pathway. Biochem Pharmacol 68(9):1845–1855

    CAS  PubMed  Google Scholar 

  • Ortega H, Lorente J, Mira G, Baravalle C, Salvetti N (2004) Constant light exposure cause dissociation in gonadotropins secretion and inhibits partially neuroendocrine differentiation of Leydig cells in adult rats. Reprod Domest Anim 39:417–423

    CAS  PubMed  Google Scholar 

  • Perez Diaz M, Acosta M, Mohamed F, Ferramola M, Oliveros L, Gimenez M (2013) Protective effects of soybeans as protein source in the diet against cadmium-aorta redox and morphological alterations. Toxicol Appl Pharmacol 272:806–815

    CAS  PubMed  Google Scholar 

  • Plateo Pignatari MG, Della Vedova MC, Perez Diaz MF, Navigatore L, Gimenez MS, Ramirez D (2019) Effects of a subchronic intoxication with cadmium in the hippocampus of rats fed with a soybean-based diet. Appl Cell Biol 6:18–33

    Google Scholar 

  • Prabu SM, Shagirtha K (2019) Cadmium and apoptosis: a molecular approach. Res Rev J Toxicol 6:8–17

    Google Scholar 

  • Raymond F, Burk M (2008) Selenium, an antioxidant nutrient. Nutr Clin Care 5(2):75–79

    Google Scholar 

  • Reeves P, Inc (1996) ISBN: 0-8493-9611-5

  • Renugadevi J, Prabu S (2008) Naringenin protects against cadmium-induced oxidative renal dysfunction in rats. Toxicology 256:128–134

    PubMed  Google Scholar 

  • Richeldi L, Collard H, Jones M (2017) Idiopathic pulmonary fibrosis. Lancet 389:1941–1952

    PubMed  Google Scholar 

  • Rodriguez-Casado A, Alvarez I, Toledano A, de Miguel E, Carmona P (2007) Amphetamine effects on brain protein structure and oxidative stress as revealed by FTIR microspectroscopy. Biopolymers 86:437–446

    CAS  PubMed  Google Scholar 

  • Salvetti N, Gimeno E, Lorente J, Ortega H (2004) Expression of cytoskeletal proteins in the follicular wall of induced ovarian cysts. Cells Tissues Organs 178:117–125

    CAS  PubMed  Google Scholar 

  • Saturnino C, Iacopetta D, Sinicropi MS, Rosano C, Caruso A, Caporale A, Marra N, Marengo B, Pronzato MA, Parisi OI et al (2014) N-Alkyl carbazole derivatives as new tools for Alzheimer’s disease: preliminary studies. Molecules 19:9307–9317

    PubMed  PubMed Central  Google Scholar 

  • Scherer G, Barkemeyer H (1983) Cadmium concentrations in tobacco and tobacco smoke. Ecotoxicol Environ Saf 7(1):8

    Google Scholar 

  • Selim M, Rashed E, Aleisa N, Daghestani M (2012) The protection role of heat shock protein 70 (HSP-70) in the testes of cadmium-exposed rats. Bioinformation 8:58–64

    PubMed  PubMed Central  Google Scholar 

  • Sichel G, Corsaro C, Scalia M, Di Bilio A, Bonomo R (1991) In vitro scavenger activity of some flavonoids and melanins against O2–. Free Radic Biol Med 11:1–8

    CAS  PubMed  Google Scholar 

  • Sinha M, Manna P, Sil P (2008) Taurine protects the antioxidant defense system in the erythrocytes of cadmium treated mice. BMB Rep 41:657–663

    CAS  PubMed  Google Scholar 

  • Soares S, Martins H, Gutiérrez-Merino C, Aureliano M (2007) Vanadium and cadmium in vivo effects in teleost cardiac muscle: metal accumulation and oxidative stress markers. Comp Biochem Physiol C Toxicol Pharmacol 141:168–178

    Google Scholar 

  • Song XB, Liu G, Wang ZY, Wang L (2016) Puerarin protects against cadmium-induced proximal tubular cell apoptosis by restoring mitochondrial function. Chem Biol Interact 260:219–231

    CAS  PubMed  Google Scholar 

  • Soo E, Yip G, Lwin Z, Kumar S, Bay B (2008) Heat shock proteins as novel therapeutic targets in cancer. In Vivo 22:311–315

    CAS  PubMed  Google Scholar 

  • Soodaeva S, Kubysheva N, Klimanov I, Nikitina L, Batyrshin I (2019) Features of oxidative and nitrosative metabolism in lung diseases. Oxid Med Cell Longev. https://doi.org/10.1155/2019/1689861

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamás MJ, Fauvet B, Christen P, Goloubinoff P (2018) Misfolding and aggregation of nascent proteins: a novel mode of toxic cadmium action in vivo. Curr Genet 64:177–181

    PubMed  Google Scholar 

  • Tan S, Yang S, Chen M, Wang Y, Zhu L, Sun Z, Chen S (2020) Lipopolysaccharides promote pulmonary fibrosis in silicosis through the aggravation of apoptosis and inflammation in alveolar macrophages. Open Life Sci. Aug 18;15(1):598-605. doi: https://doi.org/10.1515/biol-2020-0061

  • Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S (2002) Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 62:5196–5203

    CAS  PubMed  Google Scholar 

  • US Public Health Service (2011) Guide for the care and use of laboratory animals. 8th Edition. National Research Council of the National Academies. The National Academies Press, Washington DC

  • Vasconsuelo A, Milanesi L, Boland R (2010) Participation of HSP27 in the antiapoptotic action of 17 beta-estradiol in skeletal muscle cells. Cell Stress Chaperones 15:183–192

    CAS  PubMed  Google Scholar 

  • Vencataraman T, Coleman C, Frieman M (2017) Overactive epidermal growth factor receptor signaling leads to increased fibrosis after severe acute respiratory syndrome coronavirus infection. J Virol 91:182–117

    Google Scholar 

  • Verlecar X, Jena K, Chainy G (2007) Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature. Chem Biol Interact 167:219–226

    CAS  PubMed  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117

    CAS  PubMed  Google Scholar 

  • Wang J, Zhu H, Liu X, Liu Z (2014) Oxidative stress and Ca2+ signals involved on cadmium-induced apoptosis in rat hepatocyte. Biol Trace Elem Res 161:180–189

    CAS  PubMed  Google Scholar 

  • Wirth D, Christians E, Li X, Benjamin I, Gustin P (2003) Use of Hsf1 (–/–) mice reveals an essential role for HSF1 to protect lung against cadmium-induced injury. Toxicol Appl Pharmacol 192:12–20

    CAS  PubMed  Google Scholar 

  • Wu C, Zhang W, Mai K, Xu W, Zhong X (2011) Effects of dietary Zn on gene expression of antioxidant enzymes and heat shock proteins in hepatopancreas of abalone Haliotis discus hannai. Comp Biochem Physiol Part C 154:1–6

    Google Scholar 

  • Xiangyu C, Mingyang F, Ruochen B, Xiaomei Z, Baorong F, Siqi T, Chengying L, Qijiu L, Jianli L (2021) Cadmium induced BEAS-2B cells apoptosis and mitochondria damage via MAPK signaling pathway. Chemosphere 263:128346

    Google Scholar 

  • Yan-Ming X, Dan-Dan W, Wei Z, Fei-Yuan Y, Feng Y, Yue Y, Yuan Z, Yick-Pang C, Andy T (2016) Proteome profiling of cadmium-induced apoptosis by antibody array analyses in human bronchial epithelial cells. Oncotarget 7:6146–6158

    Google Scholar 

  • Yenari M, Liu J, Zheng Z, Vexler Z, Lee J, Giffard R (2005) Antiapoptotic and antiinflammatory mechanisms of heat-shock protein protection. Ann N Y Acad Sci 1053:74–83

    CAS  PubMed  Google Scholar 

  • Yesildag K, Gur C, Ileriturk M, Kandemir F (2021) Evaluation of oxidative stress, inflammation, apoptosis, oxidative DNA damage and metalloproteinases in the lungs of rats treated with cadmium and carvacrol. Mol Biol Rep. https://doi.org/10.1007/s11033-021-06948-z

    Article  PubMed  Google Scholar 

  • Yoon GA, Park S (2014) Antioxidant action of soy isoflavones on oxidative stress and antioxidant enzyme activities in exercised rats. Nutr Res Pract 8(6):618–624

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu MK, Li HY, Bai LH, Wang LS, Zou XT (2020) Histological changes, lipid metabolism, and oxidative and endoplasmic reticulum stress in the liver of laying hens exposed to cadmium concentrations. Poult Sci 99(6):3215–3228

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Ricedal Alimentos S.A., Santa Fe, Argentina, for providing the soybean flour.

Funding

The present study was supported by grants from Consejo Nacional de Investigaciones Cientificas y Tecnicas(CONICET) and Universidad Nacional de San Luis (UNSL), Argentina (Nos. PROICO 2-418 and PROICO 2-2318).

Author information

Authors and Affiliations

  1. Laboratory of Nutrition and Environment, Faculty of Chemistry, Biochemistry and Pharmacy, National University of San Luis, San Luis, Argentina

    Gabriel Giezi Boldrini, Glenda Martín Molinero & Silvina Mónica Álvarez

  2. IMIBIO-SL CONICET, San Luis, Argentina

    Gabriel Giezi Boldrini, Glenda Martín Molinero, Silvina Mónica Álvarez & Nidia Noemí Gómez

  3. Laboratory of Morphophysiology, Faculty of Chemistry, Biochemistry and Pharmacy, National University of San Luis, San Luis, Argentina

    María Verónica Pérez Chaca, María Eugenia Ciminari & Nidia Noemí Gómez

  4. INQUISAL CONICET, San Luis, Argentina

    Franco Moyano

  5. Laboratory of Oncology, IMBECU (CCT), CONICET, Mendoza, Argentina

    Maria Evelyn Córdoba, Gisela Pennacchio & Mariel Fanelli

Authors
  1. Gabriel Giezi Boldrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Glenda Martín Molinero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. María Verónica Pérez Chaca
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María Eugenia Ciminari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Franco Moyano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Evelyn Córdoba
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gisela Pennacchio
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mariel Fanelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Silvina Mónica Álvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nidia Noemí Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GGB conducted most of the experiments, developed and maintained the animal models and wrote the initial manuscript draft. GMM developed and maintained the animal models and collaborated with molecular biology determinations. MVPC conducted the histology determinations and assisted in the enzymatic determinations. MEC collaborated in BAL collection and animal handling. FM run the trace elements determinations. MF conceptualized the immunohistochemistry experiments, oversaw data collections and analyzed the results. SMA and NNG conceptualized and designed the study, oversaw the data collection, reviewed and revised the manuscript.

Corresponding authors

Correspondence to Silvina Mónica Álvarez or Nidia Noemí Gómez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict 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

Boldrini, G.G., Martín Molinero, G., Pérez Chaca, M.V. et al. Glycine max (soy) based diet improves antioxidant defenses and prevents cell death in cadmium intoxicated lungs. Biometals 35, 229–244 (2022). https://doi.org/10.1007/s10534-022-00361-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-022-00361-0

Keywords

Search

Navigation