Skip to main content
Springer Nature Link
Log in

Thulium Ion Promotes Apoptosis of Primary Mouse Bone Marrow Stromal Cells

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Bone is one of the main target organs for the lanthanides (Ln). Biodistribution studies of Tm-based compounds in vivo showed that bone had significant uptake. But the effect of Tm3+ on primary mouse bone marrow stromal cells (BMSCs) has not been reported. So we investigated the effect and underlying mechanisms of Tm3+ on BMSCs. Cell viability, cell apoptosis, reactive oxygen species (ROS) level, lactate dehydrogenase (LDH) activity and mitochondrial membrane potential (MMP) were studied. The results indicated that Tm3+ increased the viability of BMSCs at concentrations of 1 × 10−7, 1 × 10−6, 1 × 10−5, and 1 × 10−4 mol/L in a dose-dependent manner, turned to decrease the viability of BMSCs at the highest concentration of 1 × 10−3 mol/L for 24, 48, and 72 h. Tm3+ at 1 × 10−3 mol/L promoted apoptosis of BMSCs, increased the ROS and LDH levels, and decreased MMP in BMSCs. Taken together, we demonstrated that Tm3+ at 1 × 10−3 mol/L might induce cellular apoptosis through mitochondrial pathway. These results may be helpful for more rational application of Tm-based compounds in the future.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Abbreviations

BMSCs:

Bone marrow stromal cells

CEST:

Chemical exchange-dependent saturation transfer

DAPI:

4′,6-Diamidino-2-phenylindole

DCFH-DA:

2′,7′-Dichlorofluorescein diacetate

DMEM:

Dulbecco’s modified Eagle’s medium

DMSO:

Dimethyl sulfoxide

DOTA:

1,4,7,10-Tetraazacyclododecane-1,4,7,10-tetraacetate

DOTMA:

1,4,7,10-Tetraazacyclododecane-1,4,7,10-tetramethyl-1,4,7,10-tetraacetate

DOTP:

1,4,7,10-Tetraazacyclododecane-N,N′,N″,N′″-tetra (methylenephosphonate)

EDTMP:

Ethylene diamine tetramethylene phosphonate

FITC:

Fluorescein isothiocyanate

FTIR:

Fourier transform infrared spectrometer

KM:

Kunming

LDH:

Lactate dehydrogenase

Ln:

Lanthanides

MMP:

Mitochondrial membrane potential

MR:

Magnetic resonance

MRI:

Magnetic resonance imaging

MTT:

3-[4,5-Dimetylthiazole-2-yl]-2,5-diphenyl tetrazolium bromide

NBS:

Neonatal bovine serum

OD:

Optical density

PBS:

Phosphate buffered saline

PI:

Propidium iodide

Rh123:

Rhodamine 123

ROS:

Reactive oxygen species

SD:

Standard deviation

SPF:

Specific pathogen free

sub-G1:

Subdiploid DNA contents

References

  1. Li LL, Zhang RB, Yin LL et al (2012) Biomimetic surface engineering of lanthanide-doped upconversion nanoparticles as versatile bioprobes. Angew Chem 124:6225–6229

    Article  Google Scholar 

  2. Diamente PR, Raudsepp M, Veggel FCJM (2007) Dispersible Tm3+-doped nanoparticles that exhibit strong 1.47 μm photoluminescence. Adv Funct Mater 17:363–368

    Article  CAS  Google Scholar 

  3. Liu JN, Bu WB, Zhang SJ et al (2012) Controlled synthesis of uniform and monodisperse upconversion core/mesoporous silica shell nanocomposites for bimodal imaging. Chem Eur J 18:2335–2341

    Article  PubMed  CAS  Google Scholar 

  4. Yi GS, Chow GM (2006) Synthesis of hexagonal-phase NaYF4:Yb, Er and NaYF4:Yb, Tm nanocrystals with efficient up-conversion fluorescence. Adv Funct Mater 16:2324–2329

    Article  CAS  Google Scholar 

  5. Burdinski D, Lub J, Pikkemaat JA et al (2008) The thulium complex of 1,4,7,10-tetrakis{[N-(1H-imidazol-2-yl)carbamoyl]methyl}-1,4,7,10-tetraazacyclododecane (dotami) as a paraCEST contrast agent contrast agent. Chem Biodivers 5:1505–1512

    Article  PubMed  CAS  Google Scholar 

  6. Colet JM, Makos JD, Malloy CR et al (1998) Determination of the intracellular sodium concentration in perfused mouse liver by 31P and 23Na magnetic resonance spectroscopy. Magn Reson Med 39:155–159

    Article  PubMed  CAS  Google Scholar 

  7. Das T, Chakraborty S, Sarma HD et al (2009) 170Tm-EDTMP: a potential cost-effective alternative to 89SrCl2 for bone pain palliation. Nucl Med Biol 36:561–568

    Article  PubMed  CAS  Google Scholar 

  8. Hirano S, Suzuki KT (1996) Exposure, metabolism, and toxicity of rare earths and related compounds. Environ Health Perspect 104:85–95

    PubMed  CAS  Google Scholar 

  9. Shirvani-Arani S, Bahrami-Samani A, Jalilian AR et al (2012) Development of 170Tm-DOTA-cetuximab for radioimmunotherapy. J Labelled Comp Radiopharm 55:103–107

    Article  CAS  Google Scholar 

  10. Zhang J, Liu CL, Li YP et al (2010) Effect of cerium ion on the proliferation, differentiation and mineralization function of primary mouse osteoblasts in vitro. J Rare Earths 28:138–142

    Article  CAS  Google Scholar 

  11. Yi CQ, Liu DD, Fong CC et al (2010) Gold nanoparticles promote osteogenic differentiation of mesenchymal stem cells through p38 MAPK pathway. ACS Nano 4:6439–6448

    Article  PubMed  CAS  Google Scholar 

  12. Liu DD, Yi CQ, Zhang DW et al (2010) Inhibition of proliferation and differentiation of mesenchymal stem cells by carboxylated carbon nanotubes. ACS Nano 4:2185–2195

    Article  PubMed  CAS  Google Scholar 

  13. Ferlini C, Cesare S, Rainaldi G et al (1996) Flow cytometric ananlysis of the early phases of apoptosis by cellular and nuclear techniques. Cytometry 24:106–115

    Article  PubMed  CAS  Google Scholar 

  14. Chen Z, Chen H, Meng H et al (2008) Bio-distribution and metabolic paths of silica coated CdSeS quantum dots. Toxicol Appl Pharmacol 230:364–371

    Article  PubMed  CAS  Google Scholar 

  15. Zhao WH, Gou BD, Zhang TL et al (2012) Lanthanum chloride bidirectionally influences calcification in bovine vascular smooth muscle cells. J Cell Biochem 113:1776–1786

    PubMed  CAS  Google Scholar 

  16. Ye YY, Liu JW, Xu JH et al (2010) Nano-SiO2 induces apoptosis via activation of p53 and Bax mediated by oxidative stress in human hepatic cell line. Toxicol in Vitro 24:751–758

    Article  PubMed  CAS  Google Scholar 

  17. Heo HJ, Lee CY (2005) Strawberry and its anthocyanins reduce oxidative stress-induced apoptosis in PC12 cells. J Agric Food Chem 53:1984–1989

    Article  PubMed  CAS  Google Scholar 

  18. Tanimoto Y, Shibata Y, Kataoka Y et al (2008) Osteoblast-like cell proliferation on tape-cast and sintered tricalcium phosphate sheets. Acta Biomater 4:397–402

    Article  PubMed  CAS  Google Scholar 

  19. Ehrlich H, Hanke T, Simon P et al (2010) Carboxymethylation of the fibrillar collagen with respect to formation of hydroxyapatite. J Biomed Mater Res B Appl Biomater 92:542–551

    PubMed  Google Scholar 

  20. Frescaline G, Bouderlique T, Huynh MB et al (2012) Glycosaminoglycans mimetics potentiate the clonogenicity, proliferation, migration and differentiation properties of rat mesenchymal stem cells. Stem Cell Res 8:180–192

    Article  PubMed  CAS  Google Scholar 

  21. Lee CF, Liu CY, Chen SM et al (2005) Attenuation of UV-induced apoptosis by coenzyme Q10 in human cells harboring large-scale deletion of mitochondrial DNA. Ann N Y Acad Sci 1042:429–438

    Article  PubMed  CAS  Google Scholar 

  22. Dumont A, Hehner SP, Hofmann TG et al (1999) Hydrogen peroxide-induced apoptosis is CD95-independent, requires the release of mitochondria-derived reactive oxygen species and the activation of NF-kB. Oncogene 18:747–757

    Article  PubMed  CAS  Google Scholar 

  23. Karlsson HL, Gustafsson J, Cronholm P et al (2009) Size-dependent toxicity of metal oxide particles—a comparison between nano- and micrometer size. Toxicol Lett 188:112–118

    Article  PubMed  CAS  Google Scholar 

  24. Li JX, Liu JC, Wang K et al (2010) Gadolinium-containing bioparticles as an active entity to promote cell cycle progression in mouse embryo fibroblast NIH3T3 cells. J Biol Inorg Chem 15:547–557

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by Chinese Natural Science Foundation project (no. 21271059), Research Fund for the Doctoral Program of Higher Education of China (no. 20111301110004) and the Natural Science Foundation of Hainan Province, China (no. 213017).

Author information

Authors and Affiliations

  1. College of Chemistry & Environmental Science, Chemical Biology Key Laboratory of Hebei Province, Hebei University, Baoding, People’s Republic of China

    Chunyan Dai, Gong Chen, Yaqiong Dong, Jianlei Duan, Shuxiang Wang & Jinchao Zhang

  2. Key Laboratory of Medicinal Chemistry and Molecular Diagnosis of Ministry of Education, Hebei University, Baoding, 071002, China

    Shuxiang Wang & Jinchao Zhang

  3. Key Laboratory of Tropical Medicinal Plant Chemistry of Ministry of Education, College of Chemistry & Chemical Engineering, Hainan Normal University, Haikou, China

    Chunyan Dai

Authors
  1. Chunyan Dai
    View author publications

    Search author on:PubMed Google Scholar

  2. Gong Chen
    View author publications

    Search author on:PubMed Google Scholar

  3. Yaqiong Dong
    View author publications

    Search author on:PubMed Google Scholar

  4. Jianlei Duan
    View author publications

    Search author on:PubMed Google Scholar

  5. Shuxiang Wang
    View author publications

    Search author on:PubMed Google Scholar

  6. Jinchao Zhang
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Jinchao Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dai, C., Chen, G., Dong, Y. et al. Thulium Ion Promotes Apoptosis of Primary Mouse Bone Marrow Stromal Cells. Biol Trace Elem Res 156, 188–195 (2013). https://doi.org/10.1007/s12011-013-9825-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-013-9825-2

Keyword