Skip to main content
SpringerLink
Log in

Silica dioxide nanoparticles combined with cold exposure induce stronger systemic inflammatory response

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

Abstract

Growing concern has been raised over the potential hazard of nanoparticles (NPs) on human health from ambient particulate air pollution. Silicon dioxide (SiO2) NPs are one of the most widely used nanoparticles in many sectors of industry. Research on NPs has focused mainly on their toxicity in organs. Meanwhile, NPs are present in the air year-round, but are more serious in winter. Thus, the aim of this study was to evaluate the inflammatory response to SiO2 NPs using in vivo test systems. The composition of particulate matter is complicated; however, elemental silicon accounts for a significant proportion. Cold exposure can induce many kinds of systemic reactions. Thus, the second aim of this study was also to evaluate the combined effect of NPs and cold exposure on human health. There is little research on the combined effects of nanoparticles and cold on inflammation. Sprague-Dawley rats were randomly divided into four groups: those exposed to SiO2 NPs by intratracheal instillation, those exposed to at 4 °C 4 h/day for 4 weeks, a combined SiO2 NPs and cold exposure group, and a control group. Inflammatory cell infiltration in the lungs was mainly observed after exposure to SiO2 NPs or cold. Hematoxylin and eosin staining revealed that inflammation of the lungs was more serious in the combined group. In the white adipose tissue and brown adipose tissue of the combined groups, the mRNA expressions of pro-inflammatory cytokines were upregulated. In conclusion, SiO2 NPs combined with cold exposure induced a stronger systemic inflammatory response, accompanied by more serious health hazards.

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

Similar content being viewed by others

References

  • Bachler G, Losert S, Umehara Y, von Goetz N, Rodriguez-Lorenzo L, Petri-Fink A, Rothen-Rutishauser B, Hungerbuehler K (2015) Translocation of gold nanoparticles across the lung epithelial tissue barrier: combining in vitro and in silico methods to substitute in vivo experiments. Part Fibre Toxicol 12

  • Bhaumik G, Srivastava KK, Selvamurthy W, Purkayastha SS (1995) The role of free-radicals in cold injuries. Int J Biometeorol 38:171–175

    Article  CAS  Google Scholar 

  • Bourdon JA, Halappanavar S, Saber AT, Jacobsen NR, Williams A, Wallin H, Vogel U, Yauk CL (2012) Hepatic and pulmonary toxicogenomic profiles in mice intratracheally instilled with carbon black nanoparticles reveal pulmonary inflammation, acute phase response, and alterations in lipid homeostasis. Toxicol Sci 127:474–484

    Article  CAS  Google Scholar 

  • Burch WM (2002) Passage of inhaled particles into the blood circulation in humans. Circulation 106:E141–E141

    Article  Google Scholar 

  • Coccini T, Barni S, Manzo L, Roda E (2013) Apoptosis induction and histological changes in rat kidney following Cd-doped silica nanoparticle exposure: evidence of persisting effects. Toxicol Mech Methods 23:566–575

    Article  CAS  Google Scholar 

  • Coppack SW (2001) Pro-inflammatory cytokines and adipose tissue. Proc Nutr Soc 60:349–356

    Article  CAS  Google Scholar 

  • Crosswhite P, Sun ZJ (2010) Ribonucleic acid interference knockdown of interleukin 6 attenuates cold-induced hypertension. Hypertension 55:1484–U363

    Article  CAS  Google Scholar 

  • Dai L, Zanobetti A, Koutrakis P, Schwartz JD (2014) Associations of fine particulate matter species with mortality in the United States: a multicity time-series analysis. Environ Health Perspect 122:837–842

    Article  CAS  Google Scholar 

  • Diaz MB, Herzig S, Vegiopoulos A (2014) Thermogenic adipocytes: from cells to physiology and medicine. Metab Clin Exp 63:1238–1249

    Article  CAS  Google Scholar 

  • Donaldson K, Tran L, Jimenez LA, Duffin R, Newby DE, Mills N, MacNee W, Stone V (2005) Combustion-derived nanoparticles: a review of their toxicology following inhalation exposure. Particle Fibre Toxicol 2:10–10

    Article  Google Scholar 

  • Dong M, Yang X, Lim S, Cao Z, Honek J, Lu H, Zhang C, Seki T, Hosaka K, Wahlberg E, Yang J, Zhang L, Lanne T, Sun B, Li X, Liu Y, Zhang Y, Cao Y (2013) Cold exposure promotes atherosclerotic plaque growth and instability via UCP1-dependent lipolysis. Cell Metab 18:118–129

    Article  CAS  Google Scholar 

  • Eder K, Baffy N, Falus A, Fulop AK (2009) The major inflammatory mediator interleukin-6 and obesity. Inflamm Res 58:727–736

    Article  CAS  Google Scholar 

  • Enerback S (2010) Human brown adipose tissue. Cell Metab 11:248–252

    Article  Google Scholar 

  • Esposito K, Pontillo A, Giugliano F, Giugliano G, Marfella R, Nicoletti G, Giugliano D (2003) Association of low interleukin-10 levels with the metabolic syndrome in obese women. J Clin Endocrinol Metab 88:1055–1058

    Article  CAS  Google Scholar 

  • Fabian E, Landsiedel R, Ma-Hock L, Wiench K, Wohlleben W, van Ravenzwaay B (2008) Tissue distribution and toxicity of intravenously administered titanium dioxide nanoparticles in rats. Arch Toxicol 82:151–157

    Article  CAS  Google Scholar 

  • Fruijtier-Poelloth C (2012) The toxicological mode of action and the safety of synthetic amorphous silica—a nanostructured material. Toxicology 294:61–79

    Article  CAS  Google Scholar 

  • Gurevitch D, Shuster-Meiseles T, Nov O, Zick Y, Rudich A, Rudich Y (2012) TiO2 nanoparticles induce insulin resistance in liver-derived cells both directly and via macrophage activation. Nanotoxicology 6:804–812

    Article  CAS  Google Scholar 

  • Hardardottir I, Gruenfeld C, Feingold KR (1994) Effects of endotoxin and cytokines on lipid metabolism. Curr Opin Lipidol 5:207–215

    Article  CAS  Google Scholar 

  • Harju T, Makinen T, Nayha S, Laatikainen T, Jousilahti P, Hassi J (2010) Cold-related respiratory symptoms in the general population. Clin Respir J 4:176–185

    Article  Google Scholar 

  • Hubbs AF, Mercer RR, Benkovic SA, Harkema J, Sriram K, Schwegler-Berry D, Goravanahally MP, Nurkiewicz TR, Castranova V, Sargent LM (2011) Nanotoxicology—a pathologist’s perspective. Toxicol Pathol 39:301–324

    Article  CAS  Google Scholar 

  • Husain M, Saber AT, Guo C, Jacobsen NR, Jensen KA, Yauk CL, Williams A, Vogel U, Wallin H, Halappanavar S (2013) Pulmonary instillation of low doses of titanium dioxide nanoparticles in mice leads to particle retention and gene expression changes in the absence of inflammation. Toxicol Appl Pharmacol 269:250–262

    Article  CAS  Google Scholar 

  • Husain M, Wu D, Saber AT, Decan N, Jacobsen NR, Williams A, Yauk CL, Wallin H, Vogel U, Halappanavar S (2015) Intratracheally instilled titanium dioxide nanoparticles translocate to heart and liver and activate complement cascade in the heart of C57BL/6 mice. Nanotoxicology 9:1013–1022

    Article  Google Scholar 

  • Jackson P, Halappanavar S, Hougaard KS, Williams A, Madsen AM, Lamson JS, Andersen O, Yauk C, Wallin H, Vogel U (2013) Maternal inhalation of surface-coated nanosized titanium dioxide (UV-Titan) in C57BL/6 mice: effects in prenatally exposed offspring on hepatic DNA damage and gene expression. Nanotoxicology 7:85–96

    Article  CAS  Google Scholar 

  • Jasnic N, Djordjevic J, Djurasevic S, Lakic I, Vujovic P, Spasojevic N, Cvijic G (2012) Specific regulation of ACTH secretion under the influence of low and high ambient temperature—the role of catecholamines and vasopressin. J Therm Biol 37:469–474

    Article  CAS  Google Scholar 

  • Kang GS, Gillespie PA, Gunnison A, Moreira AL, Tchou-Wong KM, Chen LC (2011) Long-term inhalation exposure to nickel nanoparticles exacerbated atherosclerosis in a susceptible mouse model. Environ Health Perspect 119:176–181

    CAS  Google Scholar 

  • Kreyling WG, Semmler M, Moller W (2004) Dosimetry and toxicology of ultrafine particles. J Aerosol Med Depos Clearance Eff Lung 17:140–152

    Article  CAS  Google Scholar 

  • Li M, Li Q, Yang G, Kolosov VP, Perelman JM, Zhou XD (2011) Cold temperature induces mucin hypersecretion from normal human bronchial epithelial cells in vitro through a transient receptor potential melastatin 8 (TRPM8)-mediated mechanism. J Allergy Clin Immunol 128:626–U293

    Article  CAS  Google Scholar 

  • Li JQ, Li L, Chen HQ, Chang Q, Liu XD, Wu Y, Wei CX, Li R, Kwan JKC, Yeung KL, Xi ZG, Lu ZS, Yang X (2014) Application of vitamin E to antagonize SWCNTs-induced exacerbation of allergic asthma. Sci Report:4

  • Lin Y, Li X, Zhang L, Zhang Y, Zhu H, Zhang Y, Xi Z, Yang D (2016) Inhaled SiO2 nanoparticles blunt cold-exposure-induced WAT-browning and metabolism activation in white and brown adipose tissue. Toxicol Res 5:1106–1114

    Article  CAS  Google Scholar 

  • Lu SL, Feng M, Yao ZK, Jing A, Yufang Z, Wu MH, Sheng GY, Fu JM, Yonemochi S, Zhang JP, Wang QY, Donaldson K (2011) Physicochemical characterization and cytotoxicity of ambient coarse, fine, and ultrafine particulate matters in Shanghai atmosphere. Atmos Environ 45:736–744

    Article  CAS  Google Scholar 

  • Malfatti MA, Palko HA, Kuhn EA, Turteltaub KW (2012) Determining the pharmacokinetics and long-term biodistribution of SiO2 nanoparticles in vivo using accelerator mass spectrometry. Nano Lett 12:5532–5538

    Article  CAS  Google Scholar 

  • Mila-Kierzenkowska C, Jurecka A, Wozniak A, Szpinda M, Augustynska B, Wozniak B (2013) The effect of submaximal exercise preceded by single whole-body cryotherapy on the markers of oxidative stress and inflammation in blood of volleyball players. Oxidative Med Cell Longev:10

  • Mineo PM, Cassell EA, Roberts ME, Schaeffer PJ (2012) Chronic cold acclimation increases thermogenic capacity, non-shivering thermogenesis and muscle citrate synthase activity in both wild-type and brown adipose tissue deficient mice. Comp Biochem Physiol-Mol Integr Physiol 161:395–400

    Article  CAS  Google Scholar 

  • Nedergaard J, Cannon B (2010) The changed metabolic world with human brown adipose tissue: therapeutic visions. Cell Metab 11:268–272

    Article  CAS  Google Scholar 

  • Oberdorster G, Sharp Z, Atudorei V, Elder A, Gelein R, Lunts A, Kreyling W, Cox C (2002) Extrapulmonary translocation of ultrafine carbon particles following whole-body inhalation exposure of rats. J Toxicol Environ Health-Part A 65:1531–1543

    Article  CAS  Google Scholar 

  • Oberdorster G, Oberdorster E, Oberdorster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839

    Article  CAS  Google Scholar 

  • Pucci Molineris M, Di Venanzio G, Mamprin ME, Mediavilla MG (2013) Evaluation of the protection exerted by Pisum sativum ferredoxin-NADP(H) reductase against injury induced by hypothermia on Cos-7 cells. Cryobiology 67:76–83

    Article  CAS  Google Scholar 

  • Shim KH, Hulme J, Maeng EH, Kim M-K, An SSA (2014) Analysis of SiO2 nanoparticles binding proteins in rat blood and brain homogenate. Int J Nanomedicine 9:207–215

    Article  Google Scholar 

  • Silva LFO, da Boit KM (2011) Nanominerals and nanoparticles in feed coal and bottom ash: implications for human health effects. Environ Monit Assess 174:187–197

    Article  CAS  Google Scholar 

  • Simeonova PP, Erdely A (2009) Engineered nanoparticle respiratory exposure and potential risks for cardiovascular toxicity: predictive tests and biomarkers. Inhal Toxicol 21(Suppl 1):68–73

    Article  CAS  Google Scholar 

  • Song P, Ding Y, Wen D (2013) A reactive molecular dynamic simulation of oxidation of a silicon nanocluster. J Nanopart Res 15

  • Wen D (2010) Nanofuel as a potential secondary energy carrier. Energy Environ Sci 3:591–600

    Article  CAS  Google Scholar 

  • Xia X-R, Monteiro-Riviere NA, Riviere JE (2010) An index for characterization of nanomaterials in biological systems. Nat Nanotechnol 5:671–675

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the grants from Tianjin Institute of Health and Environmental Medicine, 300050, China and National Natural Science Foundation of China (No. 81372948).

Author information

Authors and Affiliations

  1. Tianjin Institute of Health and Environmental Medicine, No.1 DaLi Road, Tianjin, 300050, China

    Yongqiang Zhang, Yangsheng Lin, Xi Li, Li Zhang, Huili Zhu, Zhuge Xi & Danfeng Yang

  2. Tianjin No. 254 Hospital, Tianjin, 300142, China

    Wei Pan

Authors
  1. Yongqiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yangsheng Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Li Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wei Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Huili Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhuge Xi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Danfeng Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhuge Xi or Danfeng Yang.

Ethics declarations

All experiments involving the care and use of animals were performed in accordance with the guidelines and regulations concerning the ethics of science research of the Institute of Health and Environmental Medicine and were approved by the Ethics Review Board of the Institute of Health and Environmental Medicine.

Competing interests

The authors declare that they have no competing interests.

Additional information

Responsible editor: Philippe Garrigues

Yongqiang Zhang, Yangsheng Lin, Zhuge Xi and Danfeng Yang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Lin, Y., Li, X. et al. Silica dioxide nanoparticles combined with cold exposure induce stronger systemic inflammatory response. Environ Sci Pollut Res 24, 291–298 (2017). https://doi.org/10.1007/s11356-016-7649-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7649-2

Keywords

Search

Navigation