Skip to main content
SpringerLink
Log in

Surface-dependent cytotoxicity on bacteria as a model for environmental stress of halloysite nanotubes

  • Brief Communication
  • Published:
Journal of Nanoparticle Research Aims and scope Submit manuscript

Abstract

This study examined the cytotoxicity of halloysite nanotubes (HNTs) by investigating physiological responses of Escherichia coli, from cell growth to protein expression. Surfaces of HNTs were modified by amine functionalization (NH2-HNTs) or bovine serum albumin (BSA) coating and their cytotoxicity levels were compared with that of non-modified HNTs (Bare-HNTs). Bare- and NH2-HNTs exhibited accelerated cell death rates at ≥0.5 mg/ml of HNTs. It was also found that concentration as low as 0.01 mg/ml of HNTs exerted significant toxic effects on the bacterial cells. Cellular viability, metabolic activity, and DNA replication all decreased with increasing concentrations of Bare- and NH2-HNTs. In contrast, 0.01 mg/ml of BSA-coated HNTs (BSA-HNTs) coated showed no evidence of cytotoxicity. Even at concentrations ≤0.1 mg/ml, the cytocompatibility of BSA-HNTs was significantly better than those of Bare- and NH2-HNTs, which was confirmed by the observation of (i) the same or similar levels of cell proliferation and cell viability to the control, and (ii) higher levels of metabolic activity and plasmid DNA replication than those of Bare- and NH2-HNTs. In addition, higher ranaspumin-2 protein yield was observed from bacterial culture supplemented with BSA-HNTs (100, 83, and 80 % of yield at 0.01, 0.05, and 0.1 mg/ml, respectively, relative to the control). This work showed that the increase of bacterial cytotoxicity of HNTs correlated well with elevating HNT concentration and that surface modification of HNTs with amine functional group and BSA coating was an effective strategy to reduce cytotoxicity up to 0.1 mg/ml of HNTs.

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

References

  • An H, Jin B (2012) Prospects of nanoparticle-DNA binding and its implications in medical biotechnology. Biotechnol Adv 30(6):1721–1732

    Article  CAS  Google Scholar 

  • Arshady R (1990) Albumin microspheres and microcapsules: methodology of manufacturing techniques. J Controlled Release 14(2):111–131

    Article  CAS  Google Scholar 

  • Barrientos-Ramírez S, Oca-Ramírez G, Ramos-Fernández E, Sepúlveda-Escribano A, Pastor-Blas M, González-Montiel A (2011) Surface modification of natural halloysite clay nanotubes with aminosilanes. Application as catalyst supports in the atom transfer radical polymerization of methyl methacrylate. Appl Catal A 406(1):22–33

    Google Scholar 

  • Bates TF, Hildebrand FA, Swineford A (1950) Morphology and structure of endellite and halloysite. Am Mineral 35(7–8):463–484

    CAS  Google Scholar 

  • Belkin S, Smulski DR, Vollmer AC, Van Dyk TK, LaRossa RA (1996) Oxidative stress detection with Escherichia coli harboring a katG’: lux fusion. Appl Environ Microbiol 62(7):2252–2256

    CAS  Google Scholar 

  • Choi HJ, Ebersbacher CF, Myung NV, Montemagno CD (2012) Synthesis of nanoparticles with frog foam nest proteins. J Nanopart Res 14(9):1–13

    Article  Google Scholar 

  • Deen I, Pang X, Zhitomirsky I (2012) Electrophoretic deposition of composite chitosan-halloysite nanotube-hydroxyapatite films. Colloids Surf A 410(20):38–44

    Article  CAS  Google Scholar 

  • Du M, Guo B, Liu M, Jia D (2006) Preparation and characterization of polypropylene grafted halloysite and their compatibility effect to polypropylene/halloysite composite. Polym J 38(11):1198–1204

    Article  CAS  Google Scholar 

  • Du ML, Guo BC, Jia DM (2010) Newly emerging applications of halloysite nanotubes: a review. Polym Int 59(5):574–582

    CAS  Google Scholar 

  • Duan JM, Liu RC, Chen T, Zhang B, Liu JD (2012) Halloysite nanotube-Fe3O4 composite for removal of methyl violet from aqueous solutions. Desalination 293:46–52

    Article  CAS  Google Scholar 

  • Fubini B, Hubbard A (2003) Reactive oxygen species (ROS) and reactive nitrogen species (RNS) generation by silica in inflammation and fibrosis. Free Radic Biol Med 34(12):1507–1516

    Article  CAS  Google Scholar 

  • Guo B, Zou Q, Lei Y, Jia D (2009) Structure and performance of polyamide 6/halloysite nanotubes nanocomposites. Polym J 41(10):835–842

    Article  CAS  Google Scholar 

  • Gupta PK, Hung C, Perrier D (1986) Albumin microspheres. I: release characteristics of adriamycin. Int J Pharm 33(1):137–146

    Article  CAS  Google Scholar 

  • Jacobsen NR, Pojana G, White P, Møller P, Cohn CA, Smith Korsholm K, Vogel U, Marcomini A, Loft S, Wallin H (2008) Genotoxicity, cytotoxicity, and reactive oxygen species induced by single-walled carbon nanotubes and C60 fullerenes in the FE1-Muta™ mouse lung epithelial cells. Environ Mol Mutagen 49(6):476–487

    Article  CAS  Google Scholar 

  • Jinhua W, Xiang Z, Bing Z, Yafei Z, Rui Z, Jindun L, Rongfeng C (2010) Rapid adsorption of Cr(VI) on modified halloysite nanotubes. Desalination 259(1):22–28

    Article  Google Scholar 

  • Joussein E, Petit S, Churchman J, Theng B, Righi D, Delvaux B (2005) Halloysite clay minerals: a review. Clay Miner 40(4):383–426

    Article  CAS  Google Scholar 

  • Kang S, Pinault M, Pfefferle LD, Elimelech M (2007) Single-walled carbon nanotubes exhibit strong antimicrobial activity. Langmuir 23(17):8670–8673

    Article  CAS  Google Scholar 

  • Kang S, Herzberg M, Rodrigues DF, Elimelech M (2008) Antibacterial effects of carbon nanotubes: size does matter. Langmuir 24(13):6409–6413

    Article  CAS  Google Scholar 

  • Kiani G, Dostali M, Rostami A, Khataee AR (2011) Adsorption studies on the removal of malachite green from aqueous solutions onto halloysite nanotubes. Appl Clay Sci 54(1):34–39

    CAS  Google Scholar 

  • Kim CK, Chung MH, Oh YK, Lah WL (1993) Hydrophilic albumin microspheres as cytarabine carriers. Arch Pharm Res 16(2):123–128

    Article  CAS  Google Scholar 

  • Krug HF, Wick P (2011) Nanotoxicology: an interdisciplinary challenge. Angew Chem Int Ed 50(6):1260–1278

    Article  CAS  Google Scholar 

  • Levis S, Deasy P (2003) Use of coated microtubular halloysite for the sustained release of diltiazem hydrochloride and propranolol hydrochloride. Int J Pharm 253(1):145–157

    Article  CAS  Google Scholar 

  • Li Y, Sun L, Jin M, Du Z, Liu X, Guo C, Huang P, Sun Z (2011) Size-dependent cytotoxicity of amorphous silica nanoparticles in human hepatoma HepG2 cells. Toxicol In Vitro 25(7):1343–1352

    Article  CAS  Google Scholar 

  • Liu H, Wang C, Zou S, Wei Z, Tong Z (2012a) Facile fabrication of polystyrene/halloysite nanotube microspheres with core–shell structure via pickering suspension polymerization. Polym Bull 69:765–777

    Google Scholar 

  • Liu L, Wan YZ, Xie YD, Zhai R, Zhang B, Liu JD (2012b) The removal of dye from aqueous solution using alginate-halloysite nanotube beads. Chem Eng J 187:210–216

    Article  CAS  Google Scholar 

  • Liu RC, Fu KM, Zhang B, Mei DD, Zhang HQ, Liu JD (2012c) Removal of methyl orange by modified halloysite nanotubes. J Dispers Sci Technol 33(5):711–718

    Article  CAS  Google Scholar 

  • Lordan S, Kennedy JE, Higginbotham CL (2011) Cytotoxic effects induced by unmodified and organically modified nanoclays in the human hepatic HepG2 cell line. J Appl Toxicol 31(1):27–35

    Article  CAS  Google Scholar 

  • Luo P, Zhao Y, Zhang B, Liu J, Yang Y (2010) Study on the adsorption of neutral red from aqueous solution onto halloysite nanotubes. Water Res 44(5):1489–1497

    Article  CAS  Google Scholar 

  • Lvov YM, Shchukin DG, Mohwald H, Price RR (2008) Halloysite clay nanotubes for controlled release of protective agents. ACS Nano 2(5):814–820

    Article  CAS  Google Scholar 

  • Marney D, Russell L, Wu D, Nguyen T, Cramm D, Rigopoulos N, Wright N, Greaves M (2008) The suitability of halloysite nanotubes as a fire retardant for nylon 6. Polym Degrad Stab 93(10):1971–1978

    Article  CAS  Google Scholar 

  • McClellan SJ, Franses EI (2005) Adsorption of bovine serum albumin at solid/aqueous interfaces. Colloids Surf A 260(1–3):265–275

    Article  CAS  Google Scholar 

  • Nan A, Bai X, Son SJ, Lee SB, Ghandehari H (2008) Cellular uptake and cytotoxicity of silica nanotubes. Nano Lett 8(8):2150–2154

    Article  CAS  Google Scholar 

  • Pan J, Yao H, Xu L, Ou H, Huo P, Li XX, Yan Y (2011) Selective recognition of 2,4,6-trichlorophenol by molecularly imprinted polymers based on magnetic halloysite nanotubes composites. J Phys Chem C 115(13):5440–5449

    Article  CAS  Google Scholar 

  • Park MV, Neigh AM, Vermeulen JP, de la Fonteyne LJ, Verharen HW, Briede JJ, van Loveren H, de Jong WH (2011) The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. Biomaterials 32(36):9810–9817

    Article  CAS  Google Scholar 

  • Parks GA (1965) The isoelectric points of solid oxides, solid hydroxides, and aqueous hydroxo complex systems. Chem Rev 65(2):177–198

    Article  CAS  Google Scholar 

  • Qi R, Guo R, Shen M, Cao X, Zhang L, Xu J, Yu J, Shi X (2010) Electrospun poly (lactic-co-glycolic acid)/halloysite nanotube composite nanofibers for drug encapsulation and sustained release. J Mater Chem 20(47):10622–10629

    Article  CAS  Google Scholar 

  • Rooj S, Das A, Thakur V, Mahaling R, Bhowmick AK, Heinrich G (2010) Preparation and properties of natural nanocomposites based on natural rubber and naturally occurring halloysite nanotubes. Mater Des 31(4):2151–2156

    Article  CAS  Google Scholar 

  • Shchukin DG, Möhwald H (2007) Surface-engineered nanocontainers for entrapment of corrosion inhibitors. Adv Funct Mater 17(9):1451–1458

    Article  CAS  Google Scholar 

  • Shi YF, Tian Z, Zhang Y, Shen HB, Jia NQ (2011) Functionalized halloysite nanotube-based carrier for intracellular delivery of antisense oligonucleotides. Nanoscale Res Lett 6(1):608

    Article  Google Scholar 

  • Singh B (1996) Why does halloysite roll? A new model. Clays Clay Miner 44(2):191–196

    Article  CAS  Google Scholar 

  • Tierrablanca E, Romero-García J, Roman P, Cruz-Silva R (2010) Biomimetic polymerization of aniline using hematin supported on halloysite nanotubes. Appl Catal A 381(1):267–273

    CAS  Google Scholar 

  • Vergaro V, Abdullayev E, Lvov YM, Zeitoun A, Cingolani R, Rinaldi R, Leporatti S (2010) Cytocompatibility and uptake of halloysite clay nanotubes. Biomacromolecules 11(3):820–826

    Article  CAS  Google Scholar 

  • Vergaro V, Lvov YM, Leporatti S (2012) Halloysite clay nanotubes for resveratrol delivery to cancer cells. Macromol Biosci 12(9):1265–1271

    Article  CAS  Google Scholar 

  • Wei W, Abdullayev E, Hollister A, Mills D, Lvov YM (2012) Clay nanotube/poly (methyl methacrylate) bone cement composites with sustained antibiotic release. Macromol Mater 297(7):645–653

    Article  CAS  Google Scholar 

  • Xie Y, Qian D, Wu D, Ma X (2011) Magnetic halloysite nanotubes/iron oxide composites for the adsorption of dyes. Chem Eng J 168(2):959–963

    Article  CAS  Google Scholar 

  • Ye Y, Chen H, Wu J, Ye L (2007) High impact strength epoxy nanocomposites with natural nanotubes. Polymer 48(21):6426–6433

    Article  CAS  Google Scholar 

  • Zhao M, Liu P (2008) Adsorption behavior of methylene blue on halloysite nanotubes. Microporous Mesoporous Mater 112(1):419–424

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Charles Ebersbacher for helpful discussions.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. National Institute for Nanotechnology, Nanotechnology Accelerator and Department of Chemical and Materials Engineering, University of Alberta, Edmonton, AB, T6G 2M9, Canada

    Hyo-Jick Choi & Carlo D. Montemagno

  2. School of Energy, Environmental, Biological and Medical Engineering, University of Cincinnati, Cincinnati, OH, 45221, USA

    Theodore J. Stazak Jr.

Authors
  1. Hyo-Jick Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Theodore J. Stazak Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carlo D. Montemagno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hyo-Jick Choi or Carlo D. Montemagno.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Choi, HJ., Stazak, T.J. & Montemagno, C.D. Surface-dependent cytotoxicity on bacteria as a model for environmental stress of halloysite nanotubes. J Nanopart Res 15, 2008 (2013). https://doi.org/10.1007/s11051-013-2008-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11051-013-2008-4

Keywords

Search

Navigation