Skip to main content

Advertisement

Log in

Bio-indicators in cadmium toxicity: Role of HSP27 and HSP70

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Heat shock proteins (HSPs) are a family of proteins that are expressed by cells in reply to stressors. The changes in concentration of HSPs could be utilized as a bio-indicator of oxidative stress caused by heavy metal. Exposure to the different heavy metals may induce or reduce the expression of different HSPs. The exposure to cadmium ion (Cd2+) could increase HSP70 and HSP27 over 2- to 10-fold or even more. The in vitro and in vivo models indicate that the HSP70 family is more sensitive to Cd intoxication than other HSPs. The analyses of other HSPs along with HSP70, especially HSP27, could also be useful to obtain more accurate results. In this regard, this review focuses on examining the literature to bold the futuristic uses of HSPs as bio-indicators in the initial assessment of Cd exposure risks in defined environments.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Not applicable.

References

  • Abdeen A et al (2019) Cadmium overload modulates piroxicam-regulated oxidative damage and apoptotic pathways. Environ Sci Pollut Res 26:25167–25177

    Article  CAS  Google Scholar 

  • Abe T, Konishi T, Katoh T, Hirano H, Matsukuma K, Kashimura M, Higashi K (1994) Induction of heat shock 70 mRNA by cadmium is mediated by glutathione suppressive and non-suppressive triggers. Biochim Biophys Acta Gen Subj 1201:29–36. https://doi.org/10.1016/0304-4165(94)90147-3

    Article  CAS  Google Scholar 

  • Abe T, Yamamura K, Gotoh S, Kashimura M, Higashi K (1998a) Concentration-dependent differential effects of N-acetyl-l-cysteine on the expression of HSP70 and metallothionein genes induced by cadmium in human amniotic cells. Biochim Biophys Acta Gen Subj 1380:123–132. https://doi.org/10.1016/S0304-4165(97)00144-X

    Article  CAS  Google Scholar 

  • Abe T, Yamamura K, Gotoh S, Kashimura M, Higashi K (1998b) Concentration-dependent differential effects of N-acetyl-L-cysteine on the expression of HSP70 and metallothionein genes induced by cadmium in human amniotic cells. Biochim Biophys Acta Gen Subj 1380:123–132

    Article  CAS  Google Scholar 

  • Abiko Y, Yoshida E, Ishii I, Fukuto JM, Akaike T, Kumagai Y (2015) Involvement of reactive persulfides in biological bismethylmercury sulfide formation. Chem Res Toxicol 28:1301–1306

    Article  CAS  Google Scholar 

  • Akbar MT et al (2003) The neuroprotective effects of heat shock protein 27 overexpression in transgenic animals against kainate-induced seizures and hippocampal cell death. J Biol Chem 278:19956–19965

    Article  CAS  Google Scholar 

  • Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11:545–555. https://doi.org/10.1038/nrm2938

  • Akiyama M, Shinkai Y, Unoki T, Shim I, Ishii I, Kumagai Y (2017) The capture of cadmium by reactive polysulfides attenuates cadmium-induced adaptive responses and hepatotoxicity. Chem Res Toxicol 30:2209–2217

    Article  CAS  Google Scholar 

  • Akpor OB, Muchie M (2010) Remediation of heavy metals in drinking water and wastewater treatment systems: processes and applications. Int J Phys Sci

  • Akpor OB, Ohiobor GO, Olaolu DT (2014) Heavy metal pollutants in wastewater effluents: sources, effects and remediation. Adv Biosci Bioeng 2:37–43. https://doi.org/10.11648/j.abb.20140204.11

  • Alkharashi NAO, Periasamy VS, Athinarayanan J, Alshatwi AA (2017) Cadmium triggers mitochondrial oxidative stress in human peripheral blood lymphocytes and monocytes: Analysis using in vitro and system toxicology approaches. J Trace Elem Med Biol 42:117–128

    Article  CAS  Google Scholar 

  • Alnahdi HS, Sharaf IA (2019) Possible prophylactic effect of omega-3 fatty acids on cadmium-induced neurotoxicity in rats’ brains. Environ Sci Pollut Res 26:31254–31262

    Article  CAS  Google Scholar 

  • Alvarez-Olmedo DG et al (2017) Recombinant heat shock protein 27 (HSP27/HSPB1) protects against cadmium-induced oxidative stress and toxicity in human cervical cancer cells. Cell Stress Chaperones 22:357–369. https://doi.org/10.1007/s12192-017-0768-y

    Article  CAS  Google Scholar 

  • Arrigo AP (2001) Hsp27: novel regulator of intracellular redox state. IUBMB Life 52:303–307

    Article  CAS  Google Scholar 

  • Arrigo A-P (2007) The cellular “networking” of mammalian Hsp27 and its functions in the control of protein folding, redox state and apoptosis. https://doi.org/10.1007/978-0-387-39975-1_2

  • Arroyo VS, Flores KM, Ortiz LB, Gómez-Quiroz LE, Gutiérrez-Ruiz MC (2012) Liver and cadmium toxicity. J Drug Metab Toxicol S 5:001. https://doi.org/10.4172/2157-7609.S5-001

  • Awual MR, Eldesoky GE, Yaita T, Naushad M, Shiwaku H, AlOthman ZA, Suzuki S (2015) Schiff based ligand containing nano-composite adsorbent for optical copper(II) ions removal from aqueous solutions. Chem Eng J 279:639–647. https://doi.org/10.1016/j.cej.2015.05.049

    Article  CAS  Google Scholar 

  • Azarpazhooh MR et al (2010) Serum high-sensitivity C-reactive protein and heat shock protein 27 antibody titers in patients with stroke and 6-month prognosis. Angiology 61:607–612

    Article  CAS  Google Scholar 

  • Bakthisaran R, Tangirala R, Rao CM (2015) Small heat shock proteins: role in cellular functions and pathology Biochimica et Biophysica Acta (BBA)-Proteins and. Proteomics 1854:291–319

    CAS  Google Scholar 

  • Bashir S, Hussain Q, Shaaban M, Hu H (2018a) Efficiency and surface characterization of different plant derived biochar for cadmium (Cd) mobility, bioaccessibility and bioavailability to Chinese cabbage in highly contaminated soil. Chemosphere 211:632–639

    Article  CAS  Google Scholar 

  • Bashir S et al (2018b) Influence of organic and inorganic passivators on Cd and Pb stabilization and microbial biomass in a contaminated paddy soil. J Soils Sediments 18:2948–2959

    Article  CAS  Google Scholar 

  • Bashir S, Zhu J, Fu Q, Hu H (2018c) Cadmium mobility, uptake and anti-oxidative response of water spinach (Ipomoea aquatic) under rice straw biochar, zeolite and rock phosphate as amendments. Chemosphere 194:579–587

    Article  CAS  Google Scholar 

  • Bashir S et al (2019) Comparative efficiency of wheat straw and sugarcane bagasse biochar reduces the cadmium bioavailability to spinach and enhances the microbial activity in contaminated soil. Int J Phytoremediat 21:1098–1103

    Article  CAS  Google Scholar 

  • Bashir S et al (2020) Role of sepiolite for cadmium (Cd) polluted soil restoration and spinach growth in wastewater irrigated agricultural soil. J Environ Manag 258:110020

    Article  CAS  Google Scholar 

  • Batulan Z, Pulakazhi Venu VK, Li Y, Koumbadinga G, Alvarez-Olmedo DG, Shi C, O’Brien ER (2016) Extracellular release and signaling by heat shock protein 27: role in modifying vascular inflammation. Front Immunol 7:285

    Article  CAS  Google Scholar 

  • Belyaeva EA, Korotkov SM (2003) Mechanism of primary Cd2+-induced rat liver mitochondria dysfunction: discrete modes of Cd2+ action on calcium and thiol-dependent domains. Toxicol Appl Pharmacol 192:56–68

    Article  CAS  Google Scholar 

  • Belyaeva EA, Dymkowska D, Więckowski MR, Wojtczak L (2006) Reactive oxygen species produced by the mitochondrial respiratory chain are involved in Cd2+-induced injury of rat ascites hepatoma AS-30D cells. Biochim Biophys Acta 1757:1568–1574

    Article  CAS  Google Scholar 

  • Belyaeva EA, Sokolova TV, Emelyanova LV, Zakharova IO (2012) Mitochondrial electron transport chain in heavy metal-induced neurotoxicity: effects of cadmium, mercury, and copper. Sci World J 2012. https://doi.org/10.1100/2012/136063

  • Bertin G, Averbeck D (2006) Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88:1549–1559

    Article  CAS  Google Scholar 

  • Björk JK, Sistonen L (2010) Regulation of the members of the mammalian heat shock factor family. FEBS J 277:4126–4139

    Article  CAS  Google Scholar 

  • Bonham RT, Fine MR, Pollock FM, Shelden EA (2003) Hsp27, Hsp70, and metallothionein in MDCK and LLC-PK1 renal epithelial cells: effects of prolonged exposure to cadmium. Toxicol Appl Pharmacol 191:63–73

    Article  CAS  Google Scholar 

  • Boveri M, Pazos P, Gennari A, Casado J, Hartung T, Prieto P (2004) Comparison of the sensitivity of different toxicological endpoints in Caco-2 cells after cadmium chloride treatment. Arch Toxicol 78:201–206

    Article  CAS  Google Scholar 

  • Brat DJ, Bellail AC, Van Meir EG (2005) The role of interleukin-8 and its receptors in gliomagenesis and tumoral angiogenesis. Neuro-oncology 7:122–133

    Article  CAS  Google Scholar 

  • Bridges CC, Zalups RK (2005) Molecular and ionic mimicry and the transport of toxic metals. Toxicol Appl Pharmacol 204:274–308

    Article  CAS  Google Scholar 

  • Brosnan CF, Battistini L, Gao Y-L, Raine CS, Aquino DA (1996) Heat shock proteins and multiple sclerosis: a review. J Neuropathol Exp Neurol 55:389–402

    Article  CAS  Google Scholar 

  • Brzóska MM, Rogalska J, Galazyn-Sidorczuk M, Jurczuk M, Roszczenko A, Tomczyk M (2015) Protective effect of Aronia melanocarpa polyphenols against cadmium-induced disorders in bone metabolism: a study in a rat model of lifetime human exposure to this heavy metal. Chem Biol Interact 229:132–146

    Article  CAS  Google Scholar 

  • Buchko GW, Hess NJ, Kennedy MA (2000) Cadmium mutagenicity and human nucleotide excision repair protein XPA: CD, EXAFS and 1H/15N-NMR spectroscopic studies on the zinc (II)-and cadmium (II)-associated minimal DNA-binding domain (M98–F219). Carcinogenesis 21:1051–1057

    Article  CAS  Google Scholar 

  • Buonanno G, Giovinco G, Morawska L, Stabile L (2015) Lung cancer risk of airborne particles for Italian population. Environ Res 142:443–451

    Article  CAS  Google Scholar 

  • Cai K, Yu Y, Zhang M, Kim K (2019) Concentration, source, and total health risks of cadmium in multiple media in densely populated areas, China. Int J Environ Res Public Health 16:2269

    Article  CAS  Google Scholar 

  • Calderwood SK, Mambula SS, Gray PJ, Theriault JR (2007) Extracellular heat shock proteins in cell signaling. FEBS Lett 581:3689–3694

    Article  CAS  Google Scholar 

  • Cao S et al (2014) Health risks from the exposure of children to As, Se, Pb and other heavy metals near the largest coking plant in China. Sci Total Environ 472:1001–1009

    Article  CAS  Google Scholar 

  • Cartularo L, Laulicht F, Sun H, Kluz T, Freedman JH, Costa M (2015) Gene expression and pathway analysis of human hepatocellular carcinoma cells treated with cadmium. Toxicol Appl Pharmacol 288:399–408

    Article  CAS  Google Scholar 

  • Chand J, Kumar P (2020) Biochemical shift of mustard grown under cadmium contaminated soil. J Pharmacog Phytochem 9:178–183

    CAS  Google Scholar 

  • Chatterjee S, Kundu S, Bhattacharyya A (2008) Mechanism of cadmium induced apoptosis in the immunocyte. Toxicol Lett 177:83–89

    Article  CAS  Google Scholar 

  • Chen X, Zhu Y-H, Cheng X-Y, Zhang Z-W, Xu S-W (2012) The protection of selenium against cadmium-induced cytotoxicity via the heat shock protein pathway in chicken splenic lymphocytes. Molecules 17:14565–14572

    Article  CAS  Google Scholar 

  • Cheng J, Zhang X, Tang Z, Yang Y, Nie Z, Huang Q (2017) Concentrations and human health implications of heavy metals in market foods from a Chinese coal-mining city. Environ Toxicol Pharmacol 50:37–44

    Article  CAS  Google Scholar 

  • Cherif J, Mediouni C, Ammar WB, Jemal F (2011) Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solarium lycopersicum). J Environ Sci 23:837–844

    Article  CAS  Google Scholar 

  • Chikuma T et al (2009) Interleukin-6 induces prostaglandin E 2 synthesis in mouse astrocytes. J Mol Neurosci 39:175–184

    Article  CAS  Google Scholar 

  • Choi YK, Jo PG, Choi CY (2008) Cadmium affects the expression of heat shock protein 90 and metallothionein mRNA in the Pacific oyster, Crassostrea gigas. Comparat Biochem Physiol C Toxicol Pharmacol 147:286–292

    Article  CAS  Google Scholar 

  • Choong G, Liu Y, Templeton DM (2014) Interplay of calcium and cadmium in mediating cadmium toxicity. Chem Biol Interact 211:54–65

    Article  CAS  Google Scholar 

  • Chouchene L et al (2016) Inhibitory effect of cadmium on estrogen signaling in zebrafish brain and protection by zinc. J Appl Toxicol 36:863–871

    Article  CAS  Google Scholar 

  • Clarke JP, Mearow KM (2013) Cell stress promotes the association of phosphorylated HspB1 with F-actin. PLoS One 8(7):e68978. https://doi.org/10.1371/journal.pone.0068978

  • Cormet-Boyaka E et al (2012) An NF-κB–independent and Erk1/2-dependent mechanism controls CXCL8/IL-8 responses of airway epithelial cells to cadmium. Toxicol Sci 125:418–429

    Article  CAS  Google Scholar 

  • Costa LG (2008) Toxic effects of pesticides. In: Casarett and Doull’s toxicology: the basic science of poisons, vol 8, pp 883–930

    Google Scholar 

  • Council NR (1997) Toxicity and related data on selected cadmium compounds. In: Toxicologic assessment of the army’s zinc cadmium sulfide dispersion tests. National Academies Press (US)

  • Croute F, Beau B, Murat J-C, Vincent C, Komatsu H, Obata F, Soleilhavoup J-P (2005) Expression of stress-related genes in a cadmium-resistant A549 human cell line. J Toxic Environ Health A 68:703–718

    Article  CAS  Google Scholar 

  • Cwiklinska H, Mycko MP, Szymanska B, Matysiak M, Selmaj KW (2010) Aberrant stress-induced Hsp70 expression in immune cells in multiple sclerosis. J Neurosci Res 88:3102–3110

    Article  CAS  Google Scholar 

  • Dai X, Nie G, Cao H, Xing C, Hu G, Zhang C (2019) In vivo assessment of molybdenum and cadmium co-induced the mRNA levels of heat shock proteins, inflammatory cytokines and apoptosis in shaoxing duck (Anas platyrhyncha) testicles. Poult Sci 98:5424–5431

    Article  CAS  Google Scholar 

  • Dakeshita S et al (2009) Gene expression signatures in peripheral blood cells from Japanese women exposed to environmental cadmium. Toxicology 257:25–32

    Article  CAS  Google Scholar 

  • Darwish WS, Chen Z, Li Y, Wu Y, Chiba H, Hui S-P (2020) Identification of cadmium-produced lipid hydroperoxides, transcriptomic changes in antioxidant enzymes, xenobiotic transporters, and pro-inflammatory markers in human breast cancer cells (MCF7) and protection with fat-soluble vitamins. Environ Sci Pollut Res 27:1978–1990

    Article  CAS  Google Scholar 

  • Dilworth C, Hamilton G, George E, Timbrell J (2000) The use of liver spheroids as an in vitro model for studying induction of the stress response as a marker of chemical toxicity. Toxicol in Vitro 14:169–176

    Article  CAS  Google Scholar 

  • Dobrikova AG et al (2021) Cadmium toxicity in Salvia sclarea L.: an integrative response of element uptake, oxidative stress markers, leaf structure and photosynthesis. Ecotoxicol Environ Saf 209:111851

    Article  CAS  Google Scholar 

  • Ecobichon D, Klaassen C (2001) Casarett and Doull’s Toxicology: the basic science of poisons. In: Toxic effects of pesticides. McGraw-Hill, New York, pp 769–774

    Google Scholar 

  • Eduviges Z-CY et al (2020) Impact of cadmium toxicity on cartilage loss in a 3D in vitro model. Environ Toxicol Pharmacol 74:103307

    Article  CAS  Google Scholar 

  • Egger AE et al (2019) Chemical imaging and assessment of cadmium distribution in the human body. Metallomics 11:2010–2019. https://doi.org/10.1039/C9MT00178F

    Article  CAS  Google Scholar 

  • El-Tarras AE-S, Attia HF, Soliman MM, El Awady MA, Amin AA (2016) Neuroprotective effect of grape seed extract against cadmium toxicity in male albino rats. Int J Immunopathol Pharmacol 29:398–407

    Article  Google Scholar 

  • Engström KS et al (2010) Chronic exposure to cadmium and arsenic strongly influences concentrations of 8-oxo-7, 8-dihydro-2′-deoxyguanosine in urine. Free Radic Biol Med 48:1211–1217

    Article  CAS  Google Scholar 

  • Fahad S et al (2015) Effects of tire rubber ash and zinc sulfate on crop productivity and cadmium accumulation in five rice cultivars under field conditions. Environ Sci Pollut Res 22:12424–12434

    Article  CAS  Google Scholar 

  • Faisal AAH, Al-Wakel SFA, Assi HA, Naji LA, Naushad M (2020) Waterworks sludge-filter sand permeable reactive barrier for removal of toxic lead ions from contaminated groundwater. J Water Process Eng 33:101112. https://doi.org/10.1016/j.jwpe.2019.101112

    Article  Google Scholar 

  • Ferat-Osorio E et al (2014) Heat shock protein 70 down-regulates the production of toll-like receptor-induced pro-inflammatory cytokines by a heat shock factor-1/constitutive heat shock element-binding factor-dependent mechanism. J Inflamm 11:19

    Article  CAS  Google Scholar 

  • Filipič M (2012) Mechanisms of cadmium induced genomic instability. Mutat Res 733:69–77

    Article  CAS  Google Scholar 

  • Flanagan PR, McLellan JS, Haist J, Cherian MG, Chamberlain MJ, Valberg LS (1978) Increased dietary cadmium absorption in mice and human subjects with iron deficiency. Gastroenterology 74:841–846

    Article  CAS  Google Scholar 

  • Flora S, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy Indian. J Med Res 128:501

    CAS  Google Scholar 

  • Forcella M et al (2020) Neuronal specific and non-specific responses to cadmium possibly involved in neurodegeneration: a toxicogenomics study in a human neuronal cell model. NeuroToxicology 76:162–173

    Article  CAS  Google Scholar 

  • Forti E, Bulgheroni A, Cetin Y, Hartung T, Jennings P, Pfaller W, Prieto P (2010) Characterisation of cadmium chloride induced molecular and functional alterations in airway epithelial cells. Cell Physiol Biochem 25:159–168

    Article  CAS  Google Scholar 

  • Freitas M, Fernandes E (2011) Zinc, cadmium and nickel increase the activation of NF-κB and the release of cytokines from THP-1 monocytic cells. Metallomics 3:1238–1243

    Article  CAS  Google Scholar 

  • Fu Z, Xi S (2020) The effects of heavy metals on human metabolism. Toxicol Mech Methods 30:167–176

    Article  CAS  Google Scholar 

  • Garg N, Bhandari P (2014) Cadmium toxicity in crop plants and its alleviation by arbuscular mycorrhizal (AM) fungi: an overview. Plant Biosyst 148:609–621

    Article  Google Scholar 

  • Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity Plant. Cell Environ 29:1956–1969

    Article  CAS  Google Scholar 

  • Gehrmann M et al (2014) Hsp70-a biomarker for tumor detection and monitoring of outcome of radiation therapy in patients with squamous cell carcinoma of the head and neck. Radiat Oncol 9:131

    Article  Google Scholar 

  • Ghayour-Mobarhan M et al (2008) Antibody titres to heat shock protein 27 are elevated in patients with acute coronary syndrome. Int J Exp Pathol 89:209–215

    Article  CAS  Google Scholar 

  • Ghayour-Mobarhan M, Saber H, Ferns GA (2012) The potential role of heat shock protein 27 in cardiovascular disease. Clin Chim Acta 413:15–24

    Article  CAS  Google Scholar 

  • Ghonim A, Abdeen A, El-Shawarby R, Abdel-Aleem N, El-Shewy E, Abdo M, Abdelhiee E (2017) Protective effect of cinnamon against cadmium-induced hepatorenal oxidative damage in rats. Int J Pharmacol Toxicol 5:17–22

    Article  Google Scholar 

  • Ghosh D, Saha R, Ghosh A, Nandi R, Saha B (2015) A review on toxic cadmium biosorption from contaminated wastewater. Desalin Water Treat 53:413–420

    Article  CAS  Google Scholar 

  • Gobbo J, Gaucher-Di-Stasio C, Weidmann S, Guzzo J, Garrido C (2011) Quantification of HSP27 and HSP70 molecular chaperone activities. In: Molecular Chaperones. Springer, pp 137–143

  • Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. J Occupat Med Toxicol 1:1–6

    Google Scholar 

  • Guo K, Ge J, Zhang C, Lv M-W, Zhang Q, Talukder M, Li J-L (2020) Cadmium induced cardiac inflammation in chicken (Gallus gallus) via modulating cytochrome P450 systems and Nrf2 mediated antioxidant defense. Chemosphere 249:125858

    Article  CAS  Google Scholar 

  • Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377–384

    Article  CAS  Google Scholar 

  • Han SG, 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 Toxic Environ Health A 70:852–860

    Article  CAS  Google Scholar 

  • Hassan MJ, Shao G, Zhang G (2005) Influence of cadmium toxicity on growth and antioxidant enzyme activity in rice cultivars with different grain cadmium accumulation. J Plant Nutr 28:1259–1270

    Article  CAS  Google Scholar 

  • Hassan MJ, Zhang G, Zhu Z (2008) Influence of cadmium toxicity on plant growth and nitrogen uptake in rice as affected by nitrogen form. J Plant Nutr 31:251–262

    Article  CAS  Google Scholar 

  • Hawkes SJ (1997) What is a “heavy metal”? J Chem Educ 74:1374

    Article  CAS  Google Scholar 

  • Hawse JR, Cumming JR, Oppermann B, Sheets NL, Reddy VN, Kantorow M (2003) Activation of metallothioneins and α-crystallin/sHSPs in human lens epithelial cells by specific metals and the metal content of aging clear human lenses. Invest Ophthalmol Vis Sci 44:672–679

    Article  Google Scholar 

  • Heidari-Bakavoli AR et al (2012) Changes in plasma level of heat shock protein 27 after acute coronary syndrome. Angiology 63:12–16

    Article  CAS  Google Scholar 

  • Hekmatimoghaddam S, Zare-Khormizi MR, Pourrajab F (2017) Underlying mechanisms and chemical/biochemical therapeutic approaches to ameliorate protein misfolding neurodegenerative diseases. Biofactors 43:737–759

    Article  CAS  Google Scholar 

  • Henderson B, Pockley AG (2012) Cellular trafficking of cell stress proteins in health and disease vol 6. Springer Science & Business Media

  • Hendriks G, Derr RS, Misovic B, Morolli B, Calleja FM, Vrieling H (2016) The extended ToxTracker assay discriminates between induction of DNA damage, oxidative stress, and protein misfolding. Toxicol Sci 150:190–203

    Article  CAS  Google Scholar 

  • Hirano S et al (2005) p38 MAPK/HSP25 signaling mediates cadmium-induced contraction of mesangial cells and renal glomeruli. Am J Physiol Renal Physiol 288:F1133–F1143

    Article  CAS  Google Scholar 

  • Hiranuma K et al (1993) Induction of mitochondrial chaperonin, hsp60, by cadmium in human hepatoma cells. Biochem Biophys Res Commun 194:531–536

    Article  CAS  Google Scholar 

  • Hofmann U, Michaelis S, Winckler T, Wegener J, Feller K-H (2013) A whole-cell biosensor as in vitro alternative to skin irritation tests. Biosens Bioelectron 39:156–162

    Article  CAS  Google Scholar 

  • Hofmann U, Priem M, Bartzsch C, Winckler T, Feller K-H (2014) A sensitive sensor cell line for the detection of oxidative stress responses in cultured human keratinocytes. Sensors 14:11293–11307

    Article  CAS  Google Scholar 

  • Horiguchi H, Mukaida N, Okamoto S-I, Teranishi H, Kasuya M, Matsushima K (1993) Cadmium induces interleukin-8 production in human peripheral blood mononuclear cells with the concomitant generation of superoxide radicals. Lymphokine Cytokine Res 12:421–428

    CAS  Google Scholar 

  • Howarth AJ, Liu Y, Li P, Li Z, Wang TC, Hupp JT, Farha OK (2016) Chemical, thermal and mechanical stabilities of metal–organic frameworks. Nat Rev Mater 1:15018

    Article  CAS  Google Scholar 

  • Ikediobi CO, Badisa VL, Ayuk-Takem LT, Latinwo LM, 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  Google Scholar 

  • Ikwegbue PC, Masamba P, Oyinloye BE, Kappo AP (2018) Roles of heat shock proteins in apoptosis, oxidative stress, human inflammatory diseases, and cancer. Pharmaceuticals 11:2

    Article  CAS  Google Scholar 

  • Im JY, Paik SG, Han PL (2006) Cadmium-induced astroglial death proceeds via glutathione depletion. J Neurosci Res 83:301–308

    Article  CAS  Google Scholar 

  • Imran M et al (2020) Molybdenum supply alleviates the cadmium toxicity in fragrant rice by modulating oxidative stress and antioxidant gene expression. Biomolecules 10:1582

    Article  CAS  Google Scholar 

  • Jackson AP, Alloway BJ (2017) The transfer of cadmium from agricultural soils to the human food chain. In: Biogeochemistry of trace metals. CRC Press, pp 121–170

  • Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520

    Article  CAS  Google Scholar 

  • James KA, Meliker JR (2013) Environmental cadmium exposure and osteoporosis: a review. Int J Public Health 58:737–745

    Article  Google Scholar 

  • Jan AT, Azam M, Siddiqui K, Ali A, Choi I, Haq QM (2015) Heavy metals and human health: mechanistic insight into toxicity and counter defense system of antioxidants. Int J Mol Sci 16:29592–29630

    Article  CAS  Google Scholar 

  • Janus P et al (2011) NF-κB signaling pathway is inhibited by heat shock independently of active transcription factor HSF1 and increased levels of inducible heat shock proteins. Genes Cells 16:1168–1175

    Article  CAS  Google Scholar 

  • Jee H (2016) Size dependent classification of heat shock proteins: a mini-review. J Exerc Rehabilit 12:255

    Article  Google Scholar 

  • Jibril SA, Hassan SA, Ishak CF, Megat Wahab PE (2017) Cadmium toxicity affects phytochemicals and nutrient elements composition of lettuce (Lactuca sativa L.). Adv Agric

  • Jin L, Ni J, Tao Y, Weng X, Zhu Y, Yan J, Hu B (2019) N-acetylcysteine attenuates PM2. 5-induced apoptosis by ROS-mediated Nrf2 pathway in human embryonic stem cells. Sci Total Environ 666:713–720

    Article  CAS  Google Scholar 

  • Johri N, Jacquillet G, Unwin R (2010) Biometals: an international journal on the role of metal ions in biology, biochemistry, and medicine. Biometals 23:783–792

    Article  CAS  Google Scholar 

  • Kamal S, Prasad R, Varma A (2010) Soil microbial diversity in relation to heavy metals. In: Soil heavy metals. Springer, pp 31–63

  • Karri V, Schuhmacher M, Kumar V (2016) Heavy metals (Pb, Cd, As and MeHg) as risk factors for cognitive dysfunction: a general review of metal mixture mechanism in brain. Environ Toxicol Pharmacol 48:203–213

    Article  CAS  Google Scholar 

  • Kaur M, Kumar A, Mehra R, Kaur I (2020) Quantitative assessment of exposure of heavy metals in groundwater and soil on human health in Reasi district, Jammu and Kashmir. Environ Geochem Health 42:77–94

    Article  CAS  Google Scholar 

  • Kesarwani P, Murali AK, Al-Khami AA, Mehrotra S (2013) Redox regulation of T-cell function: from molecular mechanisms to significance in human health and disease. Antioxid Redox Signal 18:1497–1534

    Article  CAS  Google Scholar 

  • Kim D, Somji S, Garrett SH, Sens MA, Shukla D, Sens DA (2001) Expression of hsp 27, hsp 60, hsc 70, and hsp 70 by immortalized human proximal tubule cells (HK-2) following exposure to heat shock, sodium arsenite, or cadmium chloride. J Toxicol Environ Health A 63:475–493

    Article  CAS  Google Scholar 

  • Kim J-S, Kim H, Yim B, Rhee J-S, Won E-J, Lee Y-M (2018) Identification and molecular characterization of two Cu/Zn-SODs and Mn-SOD in the marine ciliate Euplotes crassus: modulation of enzyme activity and transcripts in response to copper and cadmium. Aquat Toxicol 199:296–304

    Article  CAS  Google Scholar 

  • Klaassen CD, Liu J (1997) Role of metallothionein in cadmium-induced hepatotoxicity and nephrotoxicity. Drug Metab Rev 29:79–102

    Article  CAS  Google Scholar 

  • Klaassen CD, Liu J, Diwan BA (2009) Metallothionein protection of cadmium toxicity. Toxicol Appl Pharmacol 238:215–220

    Article  CAS  Google Scholar 

  • Kostenko S, Moens U (2009) Heat shock protein 27 phosphorylation: kinases, phosphatases, functions and pathology. Cell Mol Life Sci 66:3289–3307

    Article  CAS  Google Scholar 

  • Kurochkin IO, Etzkorn M, Buchwalter D, Leamy L, Sokolova IM (2011) Top-down control analysis of the cadmium effects on molluscan mitochondria and the mechanisms of cadmium-induced mitochondrial dysfunction. Am J Phys Regul Integr Comp Phys 300:R21–R31

    CAS  Google Scholar 

  • Kwakowsky A, Milne MR, Waldvogel HJ, Faull RL (2016) Effect of estradiol on neurotrophin receptors in basal forebrain cholinergic neurons: relevance for Alzheimer’s disease. Int J Mol Sci 17:2122

    Article  CAS  Google Scholar 

  • Lagaudrière-Gesbert C, Newmyer SL, Gregers TF, Bakke O, Ploegh HL (2002) Uncoating ATPase Hsc70 is recruited by invariant chain and controls the size of endocytic compartments. Proc Natl Acad Sci 99:1515–1520

    Article  CAS  Google Scholar 

  • Lämmer F, Delbridge C, Würstle S, Neff F, Meyer B, Schlegel J, Kessel KA, Schmid TE, Schilling D, Combs SE (2019) Cytosolic Hsp70 as a biomarker to predict clinical outcome in patients with glioblastoma. PLoS One 14(8):e0221502. https://doi.org/10.1371/journal.pone.0221502

  • Lanocha N, Kalisinska E, Kosik-Bogacka DI, Budis H, Sokolowski S, Bohatyrewicz A (2012) Concentrations of trace elements in bones of the hip joint from patients after hip replacement surgery. J Trace Elem Med Biol 26:20–25

    Article  CAS  Google Scholar 

  • Leal RB, Posser T, Rigon AP, Oliveira CS, Gonçalves CA, Gelain DP, Dunkley PR (2007) Cadmium stimulates MAPKs and Hsp27 phosphorylation in bovine adrenal chromaffin cells. Toxicology 234:34–43

    Article  CAS  Google Scholar 

  • Lechner P, Buck D, Sick L, Hemmer B, Multhoff G (2018) Serum heat shock protein 70 levels as a biomarker for inflammatory processes in multiple sclerosis Multiple Sclerosis. J Exp Translat Clin 4:2055217318767192

    Google Scholar 

  • Lee J-S et al (2005) Heat shock protein 27 interacts with vimentin and prevents insolubilization of vimentin subunits induced by cadmium. Exp Mol Med 37:427–435

    Article  CAS  Google Scholar 

  • Lee HJ, Lee JH, Lee SM, Kim NH, Moon YG, Tak TK, Hyun M, Heo JD (2020) Cadmium induces cytotoxicity in normal mouse renal MM55. K cells. Int J Environ Health Res:1–10. https://doi.org/10.1080/09603123.2020.1739236

  • Lemaire J et al (2020) Cadmium-induced renal cell toxicity is associated with MicroRNA deregulation. Int J Toxicol 39:103–114

    Article  CAS  Google Scholar 

  • León-Vaz A, Romero LC, Gotor C, León R, Vigara J (2021) Effect of cadmium in the microalga Chlorella sorokiniana: a proteomic study. Ecotoxicol Environ Saf 207:111301

    Article  CAS  Google Scholar 

  • Li Z, Menoret A, Srivastava P (2002) Roles of heat-shock proteins in antigen presentation and cross-presentation. Curr Opin Immunol 14:45–51

    Article  CAS  Google Scholar 

  • Li L, Zhang X-j, Jiang S-r, Ding Z-n, Ding G-x, Huang J, Cheng Y-l (2007) Heat shock protein 27 regulates oxidative stress-induced apoptosis in cardiomyocytes: mechanisms via reactive oxygen species generation and Akt activation. Chin Med J 120:2271–2277

    Article  Google Scholar 

  • Li H, Liu Y, Gu Z, Li L, Liu Y, Wang L, Su L (2018) p38 MAPK-MK2 pathway regulates the heat-stress-induced accumulation of reactive oxygen species that mediates apoptotic cell death in glial cells. Oncol Lett 15:775–782

    Google Scholar 

  • Lian S et al (2015) Cadmium induces matrix metalloproteinase-9 expression via ROS-dependent EGFR, NF-кB, and AP-1 pathways in human endothelial cells. Toxicology 338:104–116

    Article  CAS  Google Scholar 

  • Liaudet L, Rosenblatt-Velin N (2013) Role of innate immunity in cardiac inflammation after myocardial infarction. Front Biosci (Schol Ed) 5:86–104

    Article  Google Scholar 

  • Lichtenfels M, da Silva DA, dos Santos PF, Blank M, de Farias CB, Roesler R, Schwartsmann G (2017) The anticancer estrogen receptor antagonist tamoxifen impairs consolidation of inhibitory avoidance memory through estrogen receptor alpha. J Neural Transm 124:1331–1339

    Article  CAS  Google Scholar 

  • Lin Y-F, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206

    Article  CAS  Google Scholar 

  • Liu X, Kumar A (2015) Differential signaling mechanism for HIV-1 Nef-mediated production of IL-6 and IL-8 in human astrocytes. Sci Rep 5:9867

    Article  Google Scholar 

  • Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238:209–214

    Article  CAS  Google Scholar 

  • Liu L, Yang B, Cheng Y, Lin H (2015) Ameliorative effects of selenium on cadmium-induced oxidative stress and endoplasmic reticulum stress in the chicken kidney. Biol Trace Elem Res 167:308–319

    Article  CAS  Google Scholar 

  • Luo Y et al (2019) Senkyunolide H protects against MPP+-induced apoptosis via the ROS-mediated mitogen-activated protein kinase pathway in PC12 cells. Environ Toxicol Pharmacol 65:73–81

    Article  CAS  Google Scholar 

  • Ma J, Zhao S, Gao G, Chang H, Ma P, Jin B (2015) Probucol protects against asymmetric dimethylarginine-induced apoptosis in the cultured human brain microvascular endothelial cells. J Mol Neurosci 57:546–553

    Article  CAS  Google Scholar 

  • Maiti P, Manna J, Veleri S, Frautschy S (2014) Molecular chaperone dysfunction in neurodegenerative diseases and effects of curcumin. Biomed Res Int. https://doi.org/10.1155/2014/495091

  • Manikandan R, Chitrapriya N, Jang YJ, Viswanathamurthi P (2013) Evaluation of DNA-binding, radical scavenging and cytotoxic activity of five coordinated Cd (ii) complexes containing 2-acetylpyridine-N 4-substituted thiosemicarbazone. RSC Adv 3:11647–11657

    Article  CAS  Google Scholar 

  • Martins VV, Zanetti MOB, Pitondo-Silva A, Stehling EG (2014) Aquatic environments polluted with antibiotics and heavy metals: a human health hazard. Environ Sci Pollut Res 21:5873–5878

    Article  CAS  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684. https://doi.org/10.1007/s00018-004-4464-6

    Article  CAS  Google Scholar 

  • McLellan J, Flanagan P, Chamberlain M, Valberg L (1978) Measurement of dietary cadmium absorption in humans. J Toxicol Environ Health 4:131–138

    Article  CAS  Google Scholar 

  • McNeill RV, Mason AS, Hodson ME, Catto JW, Southgate J (2019) Specificity of the Metallothionein-1 Response by Cadmium-Exposed Normal Human Urothelial Cells. Int J Mol Sci 20:1344

    Article  CAS  Google Scholar 

  • Melcher A, Todryk S, Hardwick N, Ford M, Jacobson M, Vile RG (1998) Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nat Med 4:581–587

    Article  CAS  Google Scholar 

  • Mladenović J, Ognjanović B, Đorđević N, Matić M, Knežević V, Štajn A, Saičić Z (2014) Protective effects of oestradiol against cadmium-induced changes in blood parameters and oxidative damage in rats. Arch Ind Hyg Toxicol 65:37–46

    Google Scholar 

  • Mlejnek P, Dolezel P, Maier V, Kikalova K, Skoupa N (2019) N-acetylcysteine dual and antagonistic effect on cadmium cytotoxicity in human leukemia cells. Environ Toxicol Pharmacol 71:103213

    Article  CAS  Google Scholar 

  • Monteiro C, Ferreira de Oliveira JMP, Pinho F, Bastos V, Oliveira H, Peixoto F, Santos C (2018) Biochemical and transcriptional analyses of cadmium-induced mitochondrial dysfunction and oxidative stress in human osteoblasts. J Toxic Environ Health A 81:705–717

    Article  CAS  Google Scholar 

  • Moon S, Lee C, Nam M (2019) Cytoprotective effects of taxifolin against cadmium-induced apoptosis in human keratinocytes. Hum Exp Toxicol 38:992–1003

    Article  CAS  Google Scholar 

  • Mosser DD, Caron AW, Bourget L, Meriin AB, Sherman MY, Morimoto RI, Massie B (2000) The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol 20:7146–7159

    Article  CAS  Google Scholar 

  • Mouro VGS et al (2020) Cadmium-induced testicular toxicity in mice: subacute and subchronic route-dependent effects. Biol Trace Elem Res 193:466–482

    Article  CAS  Google Scholar 

  • Moyano P et al (2018) Cadmium alters heat shock protein pathways in SN56 cholinergic neurons, leading to Aβ and phosphorylated Tau protein generation and cell death. Food Chem Toxicol 121:297–308

    Article  CAS  Google Scholar 

  • Mycko MP, Cwiklinska H, Walczak A, Libert C, Raine CS, Selmaj KW (2008) A heat shock protein gene (Hsp70. 1) is critically involved in the generation of the immune response to myelin antigen. Eur J Immunol 38:1999–2013

    Article  CAS  Google Scholar 

  • Nahomi RB, Palmer A, Green KM, Fort PE, Nagaraj RH (2014) Pro-inflammatory cytokines downregulate Hsp27 and cause apoptosis of human retinal capillary endothelial cells. Biochim Biophys Acta 1842:164–174. https://doi.org/10.1016/j.bbadis.2013.11.011

    Article  CAS  Google Scholar 

  • Naushad M, Alothman ZA (2015) Separation of toxic Pb2+ metal from aqueous solution using strongly acidic cation-exchange resin: analytical applications for the removal of metal ions from pharmaceutical formulation. Desalin Water Treat 53:2158–2166. https://doi.org/10.1080/19443994.2013.862744

    Article  CAS  Google Scholar 

  • Naushad M, Al-Othman ZA, Islam M (2013) Adsorption of cadmium ion using a new composite cation-exchanger polyaniline Sn(IV) silicate: kinetics, thermodynamic and isotherm studies. Int J Environ Sci Technol 10:567–578. https://doi.org/10.1007/s13762-013-0189-0

    Article  CAS  Google Scholar 

  • Naushad M, Alothman ZA, Awual MR, Alam MM, Eldesoky GE (2015) Adsorption kinetics, isotherms, and thermodynamic studies for the adsorption of Pb 2+ and Hg 2+ metal ions from aqueous medium using Ti(IV) iodovanadate cation exchanger. Ionics 21:2237–2245. https://doi.org/10.1007/s11581-015-1401-7

    Article  CAS  Google Scholar 

  • Nemmiche S (2017) Oxidative signaling response to cadmium exposure. Toxicol Sci 156:4–10

    CAS  Google Scholar 

  • Neumann D, Lichtenberger O, Günther D, Tschiersch K, Nover L (1994) Heat-shock proteins induce heavy-metal tolerance in higher plants. Planta 194:360–367. https://doi.org/10.1007/BF00197536

    Article  CAS  Google Scholar 

  • Nilash MM, Hashemzadeh A, Fakhari AR, Amini MM (2019) Novel Schiff base-functionalized metal–organic framework nanoparticles for dispersive solid phase extraction of copper ions from vegetable and water samples. Anal Methods 11:2683–2691

    Article  Google Scholar 

  • Njie-Mbye YF, Chitnis MK, Opere CA, Ohia SE (2013) Lipid peroxidation: pathophysiological and pharmacological implications in the eye. Front Physiol 4:366

    Article  Google Scholar 

  • Nookala AR, Kumar A (2014) Molecular mechanisms involved in HIV-1 Tat-mediated induction of IL-6 and IL-8 in astrocytes. J Neuroinflammation 11:214

    Article  CAS  Google Scholar 

  • Nordberg GF et al (2018) Risk assessment of effects of cadmium on human health (IUPAC Technical Report). Pure Appl Chem 90:755–808

    Article  CAS  Google Scholar 

  • O’Reilly S (2015) Pound the alarm: danger signals in rheumatic diseases. Clin Sci 128:297–305

    Article  CAS  Google Scholar 

  • Ohtsuka K, Hata M (2000a) Mammalian HSP40/DNAJ homologs: cloning of novel cDNAs and a proposal for their classification and nomenclature. Cell Stress Chaperones 5:98–112

    Article  CAS  Google Scholar 

  • Ohtsuka K, Hata M (2000b) Molecular chaperone function of mammalian Hsp70 and Hsp40-a review. Int J Hyperth 16:231–245

    Article  CAS  Google Scholar 

  • Oka Y, Akagi Y, Kinugasa T, Ishibashi N, Iwakuma N, Shiratsuchi I, Shirouzu K (2013) Heat-shock pre-treatment reduces liver injury and aids liver recovery after partial hepatectomy in mice. Anticancer Res 33:2887–2894

    CAS  Google Scholar 

  • Oldani M et al (2020) Cadmium elicits alterations in mitochondrial morphology and functionality in C3H10T1/2Cl8 mouse embryonic fibroblasts. Biochim Biophys Acta Gen Subj 1864:129568

    Article  CAS  Google Scholar 

  • Organization WH (2019) Preventing disease through healthy environments: exposure to cadmium: a major public health concern. World Health Organization

  • Pan J, Plant JA, Voulvoulis N, Oates CJ, Ihlenfeld C (2010) Cadmium levels in Europe: implications for human health. Environ Geochem Health 32:1–12

    Article  CAS  Google Scholar 

  • Panjwani N, Akbari O, Garcia S, Brazil M, Stockinger B (1999) The HSC73 molecular chaperone: involvement in MHC class II antigen presentation. J Immunol 163:1936–1942

    Article  CAS  Google Scholar 

  • Parcellier A et al (2003) HSP27 is a ubiquitin-binding protein involved in I-κBα proteasomal degradation. Mol Cell Biol 23:5790–5802

    Article  CAS  Google Scholar 

  • Patra RC, Rautray AK, Swarup D (2011) Oxidative stress in lead and cadmium toxicity and its amelioration. Vet Med Int. https://doi.org/10.4061/2011/457327

  • Phuagkhaopong S, Ospondpant D, Kasemsuk T, Sibmooh N, Soodvilai S, Power C, Vivithanaporn P (2017) Cadmium-induced IL-6 and IL-8 expression and release from astrocytes are mediated by MAPK and NF-κB pathways. Neurotoxicology 60:82–91

    Article  CAS  Google Scholar 

  • Piscopo M, Notariale R, Troisi J (2017) hsp70 as new cadmium bioaccumulation marker to prevent the risks of mussels consumption in human nutrition Madridge. J Clin Res 1:39–45

    Google Scholar 

  • Pockley AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362:469–476

    Article  CAS  Google Scholar 

  • Pockley AG, Muthana M, Calderwood SK (2008) The dual immunoregulatory roles of stress proteins. Trends Biochem Sci 33:71–79

    Article  CAS  Google Scholar 

  • Polykretis P, Cencetti F, Donati C, Luchinat E, Banci L (2019) Cadmium effects on superoxide dismutase 1 in human cells revealed by NMR. Redox Biol 21:101102

    Article  CAS  Google Scholar 

  • Prince WS, Kumar PS, Doberschutz KD, Subburam V (2002) Cadmium toxicity in mulberry plants with special reference to the nutritional quality of leaves. J Plant Nutr 25(4). https://doi.org/10.1081/PLN-120002952

  • Prozialeck WC, Edwards JR (2010) Early biomarkers of cadmium exposure and nephrotoxicity. Biometals 23:793–809

    Article  CAS  Google Scholar 

  • Prozialeck WC, Edwards JR, Lamar PC, Liu J, Vaidya VS, Bonventre JV (2009a) Expression of kidney injury molecule-1 (Kim-1) in relation to necrosis and apoptosis during the early stages of Cd-induced proximal tubule injury. Toxicol Appl Pharmacol 238:306–314

    Article  CAS  Google Scholar 

  • Prozialeck WC, Edwards JR, Vaidya VS, Bonventre JV (2009b) Preclinical evaluation of novel urinary biomarkers of cadmium nephrotoxicity. Toxicol Appl Pharmacol 238:301–305

    Article  CAS  Google Scholar 

  • Rahnama M, Johnson R, Voisey C, Simpson W, Fleetwood D (2018) The global regulatory protein VelA Is required for symbiosis between the endophytic fungus Epichloë festucae and Lolium perenne. Mol Plant-Microbe Interact 31:591–604

    Article  CAS  Google Scholar 

  • Rahnama M, Maclean P, Fleetwood D, Johnson R (2019) The LaeA orthologue in Epichloë festucae is required for symbiotic interaction with Lolium perenne. Fungal Genet Biol 129:74–85

    Article  CAS  Google Scholar 

  • Rajendran P, Rengarajan T, Nishigaki Y, Palaniswami R, Nishigaki I (2016) In vitro studies on mangiferin protection against cadmium-induced human renal endothelial damage and cell death via the MAP kinase and NF-κ B pathways. J Recept Signal Transduc 36:57–66

    Article  CAS  Google Scholar 

  • Rani A, Kumar A, Lal A, Pant M (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 24:378–399

    Article  CAS  Google Scholar 

  • Razzuoli E et al (2018) Impact of cadmium exposure on swine enterocytes. Toxicol Lett 287:92–99

    Article  CAS  Google Scholar 

  • Relja B, Mörs K, Marzi I (2018) Danger signals in trauma. Eur J Trauma Emerg Surg 44:301–316

    Article  Google Scholar 

  • Rennolds J, Malireddy S, Hassan F, Tridandapani S, Parinandi N, Boyaka PN, Cormet-Boyaka E (2012) Curcumin regulates airway epithelial cell cytokine responses to the pollutant cadmium. Biochem Biophys Res Commun 417:256–261

    Article  CAS  Google Scholar 

  • Rérole A-L, Jego G, Garrido C (2011) Hsp70: anti-apoptotic and tumorigenic protein. In: Molecular Chaperones. Springer, pp 205–230

  • Rezazadeh-Reyhani Z, Razi M, Malekinejad H, Sadrkhanlou R (2015) Cytotoxic effect of nanosilver particles on testicular tissue: evidence for biochemical stress and Hsp70-2 protein expression. Environ Toxicol Pharmacol 40:626–638

    Article  CAS  Google Scholar 

  • Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18:571–573

    Article  CAS  Google Scholar 

  • Roberts TL (2014) Cadmium and phosphorous fertilizers: the issues and the science. Procedia Eng 83:52–59

    Article  CAS  Google Scholar 

  • Roels HA, Hoet P, Lison D (1999) Usefulness of biomarkers of exposure to inorganic mercury, lead, or cadmium in controlling occupational and environmental risks of nephrotoxicity. Ren Fail 21:251–262

    Article  CAS  Google Scholar 

  • Rudd C, Herschman H (1979) Metallothionein in a human cell line: the response of HeLa cells to cadmium and zinc. Toxicol Appl Pharmacol 47:273–278

    Article  CAS  Google Scholar 

  • Sahebkar A et al (2011) A cross-sectional study of the association between heat shock protein 27 antibody titers, pro-oxidant–antioxidant balance and metabolic syndrome in patients with angiographically-defined coronary artery disease. Clin Biochem 44:1390–1395

    Article  CAS  Google Scholar 

  • Saini S, Dhania G (2020) Cadmium as an environmental pollutant: ecotoxicological effects, health hazards, and bioremediation approaches for its detoxification from contaminated sites. In: Bioremediation of Industrial Waste for Environmental Safety. Springer, pp 357–387

  • Sandalio L, Dalurzo H, Gomez M, Romero-Puertas M, Del Rio L (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    Article  CAS  Google Scholar 

  • Sandbichler AM, Höckner M (2016) Cadmium protection strategies—a hidden trade-off? Int J Mol Sci 17:139

    Article  CAS  Google Scholar 

  • Santagata S (2002) Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evol Dev 4:28–42

    Article  Google Scholar 

  • Saroj V, Nakade U, Sharma A, Yadav R, Hajare S, Garg S (2017) Functional involvement of L-type calcium channels and cyclic nucleotide-dependent pathways in cadmium-induced myometrial relaxation in rats. Hum Exp Toxicol 36:276–286

    Article  CAS  Google Scholar 

  • Satarug S, Nishijo M, Ujjin P, Vanavanitkun Y, Moore MR (2005) Cadmium-induced nephropathy in the development of high blood pressure. Toxicol Lett 157:57–68

    Article  CAS  Google Scholar 

  • Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265:12111–12114

    Article  CAS  Google Scholar 

  • Selim ME, El Hamidi AR, Aleisa NA, Daghestani MH (2012) The protection role of heat shock protein 70 (HSP-70) in the testes of cadmium-exposed rats. Bioinformation 8:58

    Article  Google Scholar 

  • Şenol N, Nazıroğlu M (2014) Melatonin reduces traumatic brain injury-induced oxidative stress in the cerebral cortex and blood of rats. Neural Regen Res 9:1112

    Article  CAS  Google Scholar 

  • Shaikh Z, Smith L (1984) Biological indicators of cadmium exposure and toxicity. Experientia 40:36–43

    Article  CAS  Google Scholar 

  • Shamelashvili K, Ostrovska S, Shatorna V (2020) The toxic effect of cadmium on a living organism and its detoxification by zinc ions. Modern Sci Moderni Veda 3:150–157

  • Sharma G, Naushad M (2020) Adsorptive removal of noxious cadmium ions from aqueous medium using activated carbon/zirconium oxide composite: Isotherm and kinetic modelling. J Mol Liq 310:113025. https://doi.org/10.1016/j.molliq.2020.113025

    Article  CAS  Google Scholar 

  • Shashidharamurthy R, Koteiche HA, Dong J, Mchaourab HS (2005) Mechanism of chaperone function in small heat shock proteins dissociation of the hsp27 oligomer is required for recognition and binding of destabilized t4 lysozyme. J Biol Chem 280:5281–5289

    Article  CAS  Google Scholar 

  • Shimada H, Funakoshi T, Waalkes MP (2000) Acute, nontoxic cadmium exposure inhibits pancreatic protease activities in the mouse. Toxicol Sci 53:474–480

    Article  CAS  Google Scholar 

  • Shin KD et al (2005) Blocking tumor cell migration and invasion with biphenyl isoxazole derivative KRIBB3, a synthetic molecule that inhibits Hsp27 phosphorylation. J Biol Chem 280:41439–41448

    Article  CAS  Google Scholar 

  • Shinkai Y, Masuda A, Akiyama M, Xian M, Kumagai Y (2017) Cadmium-mediated activation of the HSP90/HSF1 pathway regulated by reactive persulfides/polysulfides. Toxicol Sci 156:412–421

    CAS  Google Scholar 

  • Shirkhanloo H, Ghazaghi M, Mousavi HZ (2016) Cadmium determination in human biological samples based on trioctylmethyl ammonium thiosalicylate as a task-specific ionic liquid by dispersive liquid–liquid microextraction method. J Mol Liq 218:478–483

    Article  CAS  Google Scholar 

  • Sigel A, Sigel H, Sigel RK (2013) Cadmium: from toxicity to essentiality vol 11. Springer

  • Simeonov LI, Kochubovski MV, Simeonova BG (2010) Environmental heavy metal pollution and effects on child mental development: risk assessment and prevention strategies. Springer

  • Singh VP (2005) Metal toxicity and tolerance in plants and animals. Sarup & sons

  • Singh S, Eapen S, D’souza S (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233–246

    Article  CAS  Google Scholar 

  • Singh R, Gautam N, Mishra A, Gupta R (2011) Heavy metals and living systems: an overview. Indian J Pharm 43:246

    Article  CAS  Google Scholar 

  • Skipper A, Sims JN, Yedjou CG, Tchounwou PB (2016) Cadmium chloride induces DNA damage and apoptosis of human liver carcinoma cells via oxidative stress. Int J Environ Res Public Health 13:88

    Article  CAS  Google Scholar 

  • Somji S, Sens MA, Garrett SH, Gurel V, Todd JH, Sens DA (2002) Expression of hsp 90 in the human kidney and in proximal tubule cells exposed to heat, sodium arsenite and cadmium chloride. Toxicol Lett 133:241–254

    Article  CAS  Google Scholar 

  • Souza V, del Carmen EM, Gómez-Quiroz L, Bucio L, Hernández E, Cossio EC, Gutiérrez-Ruiz MC (2004) Acute cadmium exposure enhances AP-1 DNA binding and induces cytokines expression and heat shock protein 70 in HepG2 cells. Toxicology 197:213–228

    Article  CAS  Google Scholar 

  • Spooren A, Kolmus K, Laureys G, Clinckers R, De Keyser J, Haegeman G, Gerlo S (2011) Interleukin-6, a mental cytokine. Brain Res Rev 67:157–183

    Article  CAS  Google Scholar 

  • Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2:185–194

    Article  CAS  Google Scholar 

  • Srivastava S, Pant A, Trivedi S, Pandey R (2016) Curcumin and β-caryophellene attenuate cadmium quantum dots induced oxidative stress and lethality in Caenorhabditis elegans model system. Environ Toxicol Pharmacol 42:55–62

    Article  CAS  Google Scholar 

  • Stohs SJ, Bagchi D, Hassoun E, Bagchi M (2001) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 20:2. https://doi.org/10.1615/JEnvironPatholToxicolOncol.v20.i2.10

  • Suwazono Y et al (2009) Biological half-life of cadmium in the urine of inhabitants after cessation of cadmium exposure. Biomarkers 14:77–81

    Article  CAS  Google Scholar 

  • Tamás MJ, Sharma SK, Ibstedt S, Jacobson T, Christen P (2014) Heavy metals and metalloids as a cause for protein misfolding and aggregation. Biomolecules 4:252–267

    Article  CAS  Google Scholar 

  • Tang L, Su J, Liang P (2017) Modeling cadmium-induced endothelial toxicity using human pluripotent stem cell-derived endothelial cells. Sci Rep 7:1–12

    Article  CAS  Google Scholar 

  • Taylor AR, Robinson MB, Gifondorwa DJ, Tytell M, Milligan CE (2007) Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases. Dev Neurobiol 67:1815–1829

    Article  CAS  Google Scholar 

  • Tian X, Zhao L, Song X, Yan Y, Liu N, Li T, Yan B, Liu B (2016) HSP27 inhibits homocysteine-induced endothelial apoptosis by modulation of ROS production and mitochondrial caspase-dependent apoptotic pathway. Biomed Res Int 2016. https://doi.org/10.1155/2016/4847874

  • Tobian AA, Canaday DH, Harding CV (2004) Bacterial heat shock proteins enhance class II MHC antigen processing and presentation of chaperoned peptides to CD4+ T cells. J Immunol 173:5130–5137

    Article  CAS  Google Scholar 

  • Tsai M-F et al (2006) A new tumor suppressor DnaJ-like heat shock protein, HLJ1, and survival of patients with non–small-cell lung carcinoma. J Natl Cancer Inst 98:825–838

    Article  CAS  Google Scholar 

  • Tsan M-F, Gao B (2004) Cytokine function of heat shock proteins. Am J Phys Cell Phys 286:C739–C744

    CAS  Google Scholar 

  • Tucker PG (2011) Cadmium toxicity: What is the biological fate of cadmium in the body. Agency for Toxic Substances and Disease Registry (ATSDR): Case Studies in Environmental Medicine:10-44

  • Urani C, Melchioretto P, Fabbri M, Bowe G, Maserati E, Gribaldo L (2014) Cadmium impairs p53 activity in HepG2 cells. International Scholarly Research Notices 2014. https://doi.org/10.1155/2014/976428

  • Valbonesi P, Ricci L, Franzellitti S, Biondi C, Fabbri E (2008) Effects of cadmium on MAPK signalling pathways and HSP70 expression in a human trophoblast cell line. Placenta 29:725–733. https://doi.org/10.1016/j.placenta.2008.05.004

    Article  CAS  Google Scholar 

  • Valko M, Rhodes C, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1–40

    Article  CAS  Google Scholar 

  • Vesey DA (2010) Transport pathways for cadmium in the intestine and kidney proximal tubule: Focus on the interaction with essential metals. Toxicol Lett 198:13–19. https://doi.org/10.1016/j.toxlet.2010.05.004

    Article  CAS  Google Scholar 

  • Viberg H, Fredriksson A, Eriksson P (2003) Neonatal exposure to polybrominated diphenyl ether (PBDE 153) disrupts spontaneous behaviour, impairs learning and memory, and decreases hippocampal cholinergic receptors in adult mice. Toxicol Appl Pharmacol 192:95–106

    Article  CAS  Google Scholar 

  • Vidyasagar A, Wilson NA, Djamali A (2012) Heat shock protein 27 (HSP27): biomarker of disease and therapeutic target. Fibrogenesis Tissue Repair 5:7

    Article  CAS  Google Scholar 

  • Vilaboa NE, Calle C, Perez C, de Blas E, Garcia-Bermejo L, Aller P (1995) cAMP increasing agents prevent the stimulation of heat-shock protein 70 (HSP70) gene expression by cadmium chloride in human myeloid cell lines. J Cell Sci 108:2877–2883

    Article  CAS  Google Scholar 

  • Vivithanaporn P, Maingat F, Lin L-T, Na H, Richardson CD, Agrawal B, Cohen EA, Jhamandas JH, Power C (2010) Hepatitis C virus core protein induces neuroimmune activation and potentiates Human Immunodeficiency Virus-1 neurotoxicity. PLoS One 5(9):e12856. https://doi.org/10.1371/journal.pone.0012856

  • Waalkes MP (2000) Cadmium carcinogenesis in review. J Inorg Biochem 79:241–244

    Article  CAS  Google Scholar 

  • Waheed R et al (2020) Thermal stress accelerates mercury chloride toxicity in Oreochromis niloticus via up-regulation of mercury bioaccumulation and HSP70 mRNA expression. Sci Total Environ 718:137326

    Article  CAS  Google Scholar 

  • Wallin RP, Lundqvist A, Moré SH, von Bonin A, Kiessling R, Ljunggren H-G (2002) Heat-shock proteins as activators of the innate immune system. Trends Immunol 23:130–135

    Article  CAS  Google Scholar 

  • Wang R, Kovalchin JT, Muhlenkamp P, Chandawarkar RY (2006) Exogenous heat shock protein 70 binds macrophage lipid raft microdomain and stimulates phagocytosis, processing, and MHC-II presentation of antigens. Blood 107:1636–1642

    Article  CAS  Google Scholar 

  • Wang X, Chen M, Zhou J, Zhang X (2014) HSP27, 70 and 90, anti-apoptotic proteins, in clinical cancer therapy. Int J Oncol 45:18–30

    Article  CAS  Google Scholar 

  • Wang F et al (2015) Heat shock protein-70 neutralizes apoptosis inducing factor in Bcr/Abl expressing cells. Cell Signal 27:1949–1955

    Article  CAS  Google Scholar 

  • Wierzbicka M et al (2007) Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma 231:99–111

    Article  CAS  Google Scholar 

  • Wirth D, Christians E, Li X, Benjamin IJ, 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

    Article  CAS  Google Scholar 

  • Wissing S, Kayser O, Müller R (2004) Solid lipid nanoparticles for parenteral drug delivery. Adv Drug Deliv Rev 56:1257–1272

    Article  CAS  Google Scholar 

  • Wu W, Welsh MJ (1996a) Expression of the 25-kDa heat-shock protein (HSP27) correlates withresistance to the toxicity of cadmium chloride, mercuric chloride, cis-platinum (II)-diammine dichloride, or sodium arsenite in mouse embryonic stem cells transfected with sense or antisense HSP27 cDNA. Toxicol Appl Pharmacol 141:330–339

    Article  CAS  Google Scholar 

  • Wu W, Welsh MJ (1996b) Expression of the 25-kDa heat-shock protein (HSP27) correlates withresistance to the toxicity of cadmium chloride, mercuric chloride, cis-platinum(II)-diammine dichloride, or sodium arsenite in mouse embryonic stem cells transfected with sense or antisense HSP27 cDNA. Toxicol Appl Pharmacol 141:330–339. https://doi.org/10.1016/S0041-008X(96)80039-1

    Article  CAS  Google Scholar 

  • Wu J, Liu T, Rios Z, Mei Q, Lin X, Cao S (2017) Heat shock proteins and cancer. Trends Pharmacol Sci 38:226–256

    Article  CAS  Google Scholar 

  • Xia B, Cao H, Luo J, Liu P, Guo X, Hu G, Zhang C (2015) The co-induced effects of molybdenum and cadmium on antioxidants and heat shock proteins in duck kidneys. Biol Trace Elem Res 168:261–268

    Article  CAS  Google Scholar 

  • Xiao J, H-m C, Yang F, Peng X, Cui Y (2011) Effect of dietary high molybdenum on the cell cycle and apoptosis of kidney in broilers. Biol Trace Elem Res 142:523–531

    Article  CAS  Google Scholar 

  • Xu Y-M, Zhou Y, Chen D-J, Huang D-Y, Chiu J-F, Lau AT (2013) Proteomic analysis of cadmium exposure in cultured lung epithelial cells: evidence for oxidative stress-induced cytotoxicity. Toxicol Res 2:280–287

    Article  CAS  Google Scholar 

  • Yazdi MET et al (2018) Phyto-synthesis of silver nanoparticles using aerial extract of Salvia leriifolia Benth and evaluation of their antibacterial and photo-catalytic properties. Res Chem Intermed 45(3):1105–1116. https://doi.org/10.1007/s11164-018-3666-8

  • Yin B et al (2018) Vitamin C and sodium bicarbonate enhance the antioxidant ability of H9C2 cells and induce HSPs to relieve heat stress. Cell Stress Chaperones 23:735–748

    Article  CAS  Google Scholar 

  • Yourtchi MS, Bayat HR (2013) Effect of cadmium toxicity on growth, cadmium accumulation and macronutrient content of durum wheat (Dena CV.). Int J Agric Crop Sci (IJACS) 6:1099–1103

    CAS  Google Scholar 

  • Yuan Y et al (2016) Cadmium activates reactive oxygen species-dependent AKT/mTOR and mitochondrial apoptotic pathways in neuronal cells. Biomed Environ Sci 29:117–126

    CAS  Google Scholar 

  • Zaza S, de Balogh K, Palmery M, Pastorelli AA, Stacchini P (2015) Human exposure in Italy to lead, cadmium and mercury through fish and seafood product consumption from Eastern Central Atlantic Fishing Area. J Food Compos Anal 40:148–153

    Article  CAS  Google Scholar 

  • Zeng X, Xu X, Boezen HM, Huo X (2016) Children with health impairments by heavy metals in an e-waste recycling area. Chemosphere 148:408–415

    Article  CAS  Google Scholar 

  • Zhang Q et al (2016) Cadmium-induced immune abnormality is a key pathogenic event in human and rat models of preeclampsia. Environ Pollut 218:770–782

    Article  CAS  Google Scholar 

  • Zhang J, Zheng S, Wang S, Liu Q, Xu S (2020) Cadmium-induced oxidative stress promotes apoptosis and necrosis through the regulation of the miR-216a-PI3K/AKT axis in common carp lymphocytes and antagonized by selenium. Chemosphere 258:127341

    Article  CAS  Google Scholar 

  • Zhao Q et al (2014) Potential health risks of heavy metals in cultivated topsoil and grain, including correlations with human primary liver, lung and gastric cancer, in Anhui province, Eastern China. Sci Total Environ 470:340–347

    Article  CAS  Google Scholar 

  • Zheng S, Wang Q, Yuan Y, Sun W (2020) Human health risk assessment of heavy metals in soil and food crops in the Pearl River Delta urban agglomeration of China. Food Chem 316:126213

    Article  CAS  Google Scholar 

  • Zhou Z, Wang C, Liu H, Huang Q, Wang M, Lei Y (2013) Cadmium induced cell apoptosis, DNA damage, decreased DNA repair capacity, and genomic instability during malignant transformation of human bronchial epithelial cells. Int J Med Sci 10:1485

    Article  CAS  Google Scholar 

  • Zhou X, Hao W, Shi H, Hou Y, Xu Q (2015) Calcium homeostasis disruption-a bridge connecting cadmium-induced apoptosis, autophagy and tumorigenesis. Oncol Res Treatment 38:311–315

    Article  CAS  Google Scholar 

  • Ziętara N et al (2009) Absence of IFN-β impairs antigen presentation capacity of splenic dendritic cells via down-regulation of heat shock protein 70. J Immunol 183:1099–1109

    Article  CAS  Google Scholar 

  • Zolkiewski M, Zhang T, Nagy M (2012) Aggregate reactivation mediated by the Hsp100 chaperones. Arch Biochem Biophys 520:1–6

    Article  CAS  Google Scholar 

  • Zou H et al (2020) Cadmium-induced cytotoxicity in mouse liver cells is associated with the disruption of autophagic flux via inhibiting the fusion of autophagosomes and lysosomes. Toxicol Lett 321:32–43

    Article  CAS  Google Scholar 

Download references

Funding

The authors appreciatively acknowledge the support and assistance provided by Mashhad University of Medical Sciences.

Author information

Authors and Affiliations

Authors

Contributions

ME.TY and MS.A conceived of the presented idea, data extraction, and analysis. F.N. and F.F. draw the shapes and developed the contents. ME.TY, M.R., and SH.M authors contributed to the final version of the manuscript. SH.M. supervised the project. All authors discussed the results and contributed to the final manuscript.

Corresponding author

Correspondence to Seyed Hadi Mousavi.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

The corresponding author has the consent of all coauthors.

Consent for publication

The corresponding author has the consent to publish.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

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

Taghavizadeh Yazdi, M.E., Amiri, M.S., Nourbakhsh, F. et al. Bio-indicators in cadmium toxicity: Role of HSP27 and HSP70. Environ Sci Pollut Res 28, 26359–26379 (2021). https://doi.org/10.1007/s11356-021-13687-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-13687-y

Keywords

Navigation