Multi-walled carbon nanotubes induce apoptosis via mitochondrial pathway and scavenger receptor

Toxicology in Vitro

Volumn 26, Issue 6, 2012, Pages 799-806

  Wang, Xiang ^a   Guo, Jian ^a,d   Chen, Tian ^a   Nie, Haiyu ^b   Wang, Haifang ^c   Zang, Jiajie ^a   Cui, Xiaoxing ^a   Jia, Guang ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c SHANGHAI UNIVERSITY   (China)

^d CHINA WATERBORNE TRANSPORT RESEARCH INSTITUTE   (China)

Author keywords

Apoptosis; Mitochondria; Multi walled carbon nanotubes (MWCNTs); RAW 264.7 cells; Scavenger receptors

Indexed keywords

CASPASE 9; MULTI WALLED NANOTUBE; SCAVENGER RECEPTOR; TAURINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; MACROPHAGE; MITOCHONDRION; MOUSE; NONHUMAN; PHAGOCYTOSIS;

ANIMALS; APOPTOSIS; CASPASE 9; CELL LINE; CELL SURVIVAL; CYTOCHROMES C; MACROPHAGES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; NANOTUBES, CARBON; PHAGOCYTOSIS; RECEPTORS, SCAVENGER;

MURINAE; MUS;

EID: 84863819640     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2012.05.010     Document Type: Article

References (53)

1. Bottini M., Bruckner S., Nika K., Bottini N., Bellucci S., Magrini A., Bergamaschi A., Mustelin T. Multi-walled carbon nanotubes induce T lymphocyte apoptosis. Toxicol. Lett. 2006, 160:121-126.
2. Brenner C., Marzo I., Kroemer G. A revolution in apoptosis: from a nucleocentric to a mitochondriocentric perspective. Exp. Gerontol. 1998, 33:543-553.
3. Budihardjo I., Oliver H., Lutter M., Luo X., Wang X.D. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 1999, 15:269-290.
4. Canman, C.E., Kastan, M.B.,1996. Signal transduction - three paths to stress relief. Nature 384, 213-214.
5. Casey A., Herzog E., Davoren M., Lyng F.M., Byrne H.J., Chambers G. Spectroscopic analysis confirms the interactions between single walled carbon nanotubes and various dyes commonly used to assess cytotoxicity. Carbon 2007, 45:1425-1432.
6. Cecconi F., Gruss P. Apaf1 in developmental apoptosis and cancer: how many ways to die?. Cell Mol. Life Sci. 2001, 58:1688-1697.
7. Deng X., Jia G., Wang H., Sun H., Wang X., Yang S., Wang T., Liu Y. Translocation and fate of multi-walled carbon nanotubes in vivo. Carbon 2007, 45:1419-1424.
8. Earnshaw W.C., Martins L.M., Kaufmann S.H. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Cell Dev. Biol. 1999, 68:383-424.
9. Elgrabli D., Abella-Gallart S., Robidel F., Rogerieux F., Boczkowski J., Lacroix G. Induction of apoptosis and absence of inflammation in rat lung after intratracheal instillation of multiwalled carbon nanotubes. Toxicology 2008, 253:131-136.
10. Giorgio M.L., Di Bucchianico S., Raqnelli A.M., Aimola P., Santucci S., Poma A. Effect of singe-and multi-walled carbon nanotubes on macrophages: cytotoxicity, genotoxicity and ultrastructural damage. Mutat. Res.-Gen. Toxicol. Environ. 2011, 722:20-31.
11. Hamilton R.F., de Villiers W.J., Holian A. Class A type II scavenger receptor mediates silica-induced apoptosis in Chinese hamster ovary cell line. Toxicol. Appl. Pharm. 2000, 162:100-106.
12. Holian A., Hamilton R.F., Morandi M.T., Brown S.B., Li L. Urban particle-induced apoptosis and phenotype shifts in human alveolar macrophages. Environ. Health Persp. 1998, 106:127-132.
13. Hu X., Cook S., Wang P., Hwang H.M., Liu X., Williams Q.L. In vitro evaluation of cytotoxicity of engineered carbon nanotubes in selected human cell lines. Sci. Total Environ. 2010, 408:1812-1817.
14. Iyer R., Hamilton R.F., Li L., Holian A. Silica-induced apoptosis is mediated via scavenger receptor in human alveolar macrophages. Toxicol. Appl. Pharm. 1996, 141:84-92.
15. Iyer R., Holian A. Involvement of the ICE family of proteases in silica-induced apoptosis in human alveolar macrophages. Am. J. Physiol-Lung C. 1997, 17:760-767.
16. Jia G., Wang F.H., Yan L., Wang X., Pei R.J., Yan T., Zhao Y.L., Guo X.B. Cytotoxicity of carbon nanomaterials: single-wall nanotube, multiwall nanotube, and fullerene. Environ. Sci. Technol. 2005, 39:1378-1383.
17. Kagan V.E., Tyurina Y.Y., Tyurin V.A., Konduru N.V., Potapovich A.I., Osipov A.N., Kisin E.R., Schwegler-Berry D., Mercer R., Castranova V., Shvedova A.A. Direct and indirect effects of single walled carbon nanotubes on RAW264.7 macrophages: role of iron. Toxicol. Lett. 2006, 165:88-100.
18. Kobzik L. Lung macrophages uptake of unopsonized environmental particles: role of scavenger-type receptors. J. Immunol. 1995, 155:367-376.
19. Kodama T., Freeman M., Rohrer L., Zabrecky J., Matsudaira P., Krieger M. Type I macrophage scavenger receptor contains alpha-helical and collagen-like coiled coils. Nature 1990, 343:531-535.
20. Li P., Nijhawan D., Budihardio I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X.D. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91:479-489.
21. Manna S.K., Sarkar S., Barr J., Wise K., Barrera E.V., Jejelowo O., Rice-Ficht A.C., Ramesh G.T. Single-walled carbon nanotube induces oxidative stress and activates nuclear transcription factor-kappa B in human keratinocytes. Nano Lett. 2005, 5:1676-1684.
22. Martinez-Pastor F., Johannisson A., Gil J., Kaabi M., Anel L., Paz P., Rodriguez-Martinez H. Use of chromatin stability assay, mitochondrial stain JC-1, and fluorometric assessment of plasma membrane to evaluate frozen-thawed ram semen. Anim. Reprod. Sci. 2004, 84:121-133.
23. Migliore L., Saracino D., Bonelli A., Colognato R., D'Errico M.R., Magrini A., Bergamaschi A., Bergamaschi E. Carbon nanotubes induce oxidative DNA damage in RAW 264.7 cells. Environ. Mol. Mutagen. 2010, 51:294-303.
24. Monteiro-Riviere N.A., Nemanich R.J., Inman A.O., Wang Y.Y., Riviere J.E. Multi-walled carbon nanotube interactions with human epidermal keratinocytes. Toxicol. Lett. 2005, 155:377-384.
25. Monteiro-Riviere N.A., Inman A.O., Wang Y.Y., Nemanich R.J. Surfactant effects on carbon nanotube interactions with human keratinocytes. Nanomedicine 2005, 1:293-299.
26. Monteiro-Riviere N.A., Inman A.O., Zhang L.W. Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol. Appl. Pharm. 2009, 234:222-235.
27. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
28. Muller J., Huaux F., Moreau N., Misson P., Heilier J.F., Delos M., Arras M., Fonseca A., Nagy J.B., Lison D. Respiratory toxicity of multi-wall carbon nanotubes. Toxicol. Appl. Pharmacol. 2005, 207:221-231.
29. Obot C.J., Morandi M.T., Beebe T.P., Hamilton R.F., Holian A. Surface components of airborne particulate matter induce macrophage apoptosis through scavenger receptors. Toxicol. Appl. Pharm. 2002, 184:98-106.
30. Orrenius S., Nicotera P., Zhivotovsky B. Cell death mechanisms and their implications in toxicology. Toxicol. Sci. 2011, 119:3-19.
31. Palecanda A., Paulauskis J., Al-Mutairi E., Imrich A., Qin G.Z., Sukuki H., Kodama T., Tryggvason K., Koziel H., Kobzik L. Role of the scavenger receptor MARCO in alveolar macrophage binding of unopsonized environmental particles. J. Exp. Med. 1999, 189:1497-1506.
32. Patlolla A., Knighten B., Tchounwou P. Multi-walled carbon nanotubes induce cytotoxicity, genotoxicity and apoptosis in normal human dermal fibroblast cells. Ethnobiol. Dis. 2010, 20:65-72.
33. Pearson A.M. Scavenger receptors in innate immunity. Curr. Opin. Immunol. 1996, 8:20-28.
34. Ravichandran P., Baluchamy S., Sadanandan B., Gopikrishnan R., Biradar S., Ramesh V., Hall J.C., Ramesh G.T. Multiwalled carbon nanotubes activate NF-κB and AP-1 signaling pathways to induce apoptosis in rat lung epithelial cells. Apoptosis 2010, 15:1507-1516.
35. Salvesen G.S., Renatus M. Apoptosome: the seven-spoked death machine. Dev. Cell 2002, 2:256-257.
36. Shen Z.L., Nie H.Y., Wang H.F., Yang B., Zhong L.J., Zou X.J., Liu D., Guo J., Jia G. Two types of MWNTs with differents surface modifications induc differential expression of proteins in RAW 264.7 cells. J. Pek. Univ. (Health Sci.) 2010, 3:345-350.
37. Shvedova A.A., Castranova V., Kisin E.R., Schwegler-Berry D., Murray A.R., Gandelsman V.Z., Maynard A., Baron P. Exposure to carbon nanotube material: Assessment of nanotube cytotoxicity using human keratinocyte cells. J. Toxicol. Environ. Health A 2003, 66:1909-1926.
38. Shvedova A.A., Kisin E.R., Mercer R., Murray A.R., Johnson V.J., Potapovich A.L., Tyurina Y.Y., Gorelik O., Arepalli S., Schwegler-Berry D., Hubbs A.F., Antoini J., Evans D.E., Ku B.K., Ramsey D., Maynard A., Kagan V.E., Castranova V., Baron P. Unusual inflammatory and fibrogenic pulmonary response to single-walled carbon nanotubes in mice. Am. J. Physiol. Lung. Cell. Mol. Physiol. 2005, 289:698-708.
39. Slee E.A., Adrain C., Martin S.J. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J. Bio. Chem. 2001, 276:7320-7326.
40. Sohaebuddin S.K., Thevenot P.T., Baker D., Eaton J.W., Tang L. Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol. 2010, 7:22.
41. Stennicke H.R., Jurgensmeier J.M., Shin H., Deveraux Q., Wolf B.B., Yang X.H., Zhou Q., Ellerby H.M., Ellerby L.M., Bredesen D., Green D.R., Redd J.C., Froelich C.J., Salvesen G.S. Pro-caspase-3 is a major physiologic target of caspase-8. J. Bio. Chem. 1998, 273:27084-27090.
42. Sun Y.P., Fu K., Lin Y., Huang W. Functionalized carbon nanotubes: properties and applications. Acc. Chem. Res. 2002, 35:1096-1104.
43. Tabet L., Bussy C., Amara N., Setyan A., Grodet A., Rossi M.J., Pairon J.C., Boczkowski J., Lanone S. Adverse effects of industival multiwalled carbon nanotubes on human pulmonary cell. J. Toxicol. Environ. Health A 2009, 72:60-73.
44. Tan A.S., Berridge M.V. Superoxide produced by activated neutrophils efficiently reduces the tetrazolium salt, WST-1 to produce a soluble formazan: a simple colorimetric assay for measuring respiratory burst activation and for screening anti-inflammatory agents. J. Immunol. Methods 2000, 238:59-68.
45. Thakur S.A., Hamilton R.F., Holian A. Role of scavenger receptor a family in lung inflammation from exposure to environmental particles. J. Immunotoxicol. 2008, 5:151-157.
46. Van Berkel T.J.C., Van Velzen A., Kruijt J.K., Suzuki H., Kodama T. Uptake and catabolism of modified LDL in scavenger-receptor class A type I/II knock-out mice. Biochem. J. 1998, 331:29-35.
47. Verheij M., Bose R., Lin X.H., Yao B., Jarvis W.D., Grant S., Birrer M.J., Szabo E., Zon L.I., Kyriakis J.M., HaimovitzFriedman A., Fuks Z., Kolesnick R.N. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 1996, 380:75-79.
48. Vermes I., Haanen C., Steffensnakken H., Reutelingsperger C. A novel assay for apoptosis - flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein-labeled annexin-V. J. Immunol. Methods 1995, 184:39-51.
49. Wang X., Jia G., Wang H., Nie H., Yan L., Deng X.Y., Wang S. Diameter effects on cytotoxicity of multi-walled carbon nanotubes. J. Nanosci. Nanotechnol. 2009, 9:3025-3033.
50. Wang X., Zang J.J., Wang H., Nie H., Wang T.C., Deng X.Y., Gu Y.Q., Liu Z.H., Jia G. Pulmonary toxicity in mice exposed to low and medium doses of water-soluble multi-walled carbon nanotubes. J. Nanosci. Nanotechnol. 2010, 10:8516-8526.
51. Xu C., Bailly-Maitre B., Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 2005, 115:2656-2664.
52. Yehia H.N., Draper R.K., Mikoryak C., Walker E.K., Bajaj P., Musselman I.H., Daigrepont M.C., Dieckmann G.R., Pantano P. Single-walled carbon nanotube interactions with Hela cell. J. Nanobiotechnol. 2007, 5:8.
53. Zou H., Henzel W.J., Liu X.S., Lutschg A., Wang X.D. Apaf-1, a human protein homologous to C-elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997, 90:405-413.