Cell cycle regulation by carboxylated multiwalled carbon nanotubes through p53-independent induction of p21 under the control of the BMP signaling pathway

Chemical Research in Toxicology

Volumn 25, Issue 6, 2012, Pages 1212-1221

  Zhang, Yi ^a,b   Yan, Bing ^a,b  

^a SHANDONG UNIVERSITY   (China)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CARBOXYLATED MULTIWALLED CCRBON NANOTUBE; CYCLIN D; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; INHIBITOR OF DIFFERENTIATION PROTEIN; MULTI WALLED NANOTUBE; PROTEIN P21; PROTEIN P53; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE REGULATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CARBOXYLIC ACIDS; CELL CYCLE; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; HEK293 CELLS; HUMANS; MICE; MODELS, BIOLOGICAL; NANOTUBES, CARBON; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84862535131     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300059m     Document Type: Article

References (57)

1. Centi, G. and Perathoner, S. (2011) Carbon nanotubes for sustainable energy applications ChemSusChem 4, 913-925
2. Yu, C., Choi, K., Yin, L., and Grunlan, J. C. (2011) Light-weight flexible carbon nanotube based organic composites with large thermoelectric power factors ACS Nano 5, 7885-7892
3. Karn, B., Kuiken, T., and Otto, M. (2009) Nanotechnology and in situ remediation: a review of the benefits and potential risks Environ. Health Perspect. 117, 1813-1831
4. Sanbonmatsu, K. Y. and Tung, C. S. (2007) High performance computing in biology: Multimillion atom simulations of nanoscale systems J. Struct. Biol. 157, 470-480
5. Woodrow Wilson International Center for Scholars, Pew Charitable Trusts. The Project on Emerging Nanotechnologies. http://www.nanotechproject.org/ inventories/consumer/
6. Zhang, Y., Bai, Y., and Yan, B. (2010) Functionalized carbon nanotubes for potential medicinal applications Drug Discovery Today 15, 428-435
7. Liu, Z., Sun, X., Nakayama-Ratchford, N., and Dai, H. (2007) Supramolecular chemistry on water-soluble carbon nanotubes for drug loading and delivery ACS Nano 1, 50-56
8. Liu, Z., Tabakman, S., Welsher, K., and Dai, H. (2009) Carbon nanotubes in biology and medicine: in vitro and in vivo detection, imaging and drug delivery Nano Res. 2, 85-120
9. De La Zerda, A., Zavaleta, C., Keren, S., Vaithilingam, S., Bodapati, S., and Liu, Z. 2008, Carbon nanotubes as photoacoustic molecular imaging agents in living mice Nat. Nanotechnol. 3, 557-562
10. Kostarelos, K., Bianco, A., and Prato, M. (2009) Promises, facts and challenges for carbon nanotubes in imaging and therapeutics Nat. Nanotechnol. 4, 627-633
11. Harrison, B. S. and Atala, A. (2007) Carbon nanotube applications for tissue engineering Biomaterials 28, 344-353 (Pubitemid 44537381)
12. Donaldson, K., Murphy, F., Duffin, R., and Poland, C. (2010) Asbestos, carbon nanotubes and the pleural mesothelium: a review of the hypothesis regarding the role of long fibre retention in the parietal pleura, inflammation and mesothelioma Part. Fibre Toxicol. 7, 5
13. Nel, A., Xia, T., Mädler, L., and Li, N. (2006) Toxic potential of materials at the nanolevel Science 311, 622-627 (Pubitemid 43191298)
14. Hartwell, L. and Weinert, T. (1989) Checkpoints: controls that ensure the order of cell cycle events Science 246, 629-634 (Pubitemid 19283354)
15. Pietenpol, J. A. and Stewart, Z. A. (2002) Cell cycle checkpoint signaling: Cell cycle arrest versus apoptosis Toxicology 181-182, 475-481 (Pubitemid 36015741)
16. Offer, H., Erez, N., Zurer, I., Tang, X., Milyavsky, M., and Goldfinger, N. 2002, The onset of p53-dependent DNA repair or apoptosis is determined by the level of accumulated damaged DNA Carcinogenesis 23, 1025-1032 (Pubitemid 34752959)
17. Sriram, V. and Patterson, C. (2001) Cell cycle in vasculoproliferative diseases: potential interventions and routes of delivery Circulation 103, 2414-2419 (Pubitemid 32448809)
18. Yang, G., Chang, B., Yang, F., Guo, X., Cai, K. Q., and Xiao, X. 2010, Aurora kinase A promotes ovarian tumorigenesis through dysregulation of the cell cycle and suppression of BRCA2 Clin. Cancer Res. 16, 3171-3181
19. Sargent, L. M., Shvedova, A. A., Hubbs, A. F., Salisbury, J. L., Benkovic, S. A., and Kashon, M. L. 2009, Induction of aneuploidy by single-walled carbon nanotubes Environ. Mol. Mutagen. 50, 708-717
20. Wang, L., Luanpitpong, S., Castranova, V., Tse, W., Lu, Y., and Pongrakhananon, V. 2011, Carbon nanotubes induce malignant transformation and tumorigenesis of human lung epithelial cells Nano Lett. 11, 2796-2803
21. Kayes, O. J., Loddo, M., Patel, N., Patel, P., Minhas, S., and Ambler, G. 2009, DNA replication licensing factors and aneuploidy are linked to tumor cell cycle state and clinical outcome in penile carcinoma Clin. Cancer Res. 15, 7335-7344
22. Mukherjee, S., Manna, S., Pal, D., Mukherjee, P., and Panda, C. K. (2010) Sequential loss of cell cycle checkpoint control contributes to malignant transformation of murine embryonic fibroblasts induced by 20-methylcholanthrene J. Cell. Physiol. 224, 49-58
23. Cui, D., Tian, F., Ozkan, C. S., Wang, M., and Gao, H. (2005) Effect of single wall carbon nanotubes on human HEK293 cells Toxicol. Lett. 155, 73-85 (Pubitemid 39600739)
24. Nam, C. W., Kang, S., Kang, Y., and Kwak, M. K. (2011) Cell growth inhibition and apoptosis by SDS-solubilized single-walled carbon nanotubes in normal rat kidney epithelial cells Arch. Pharmacol. Res. 34, 661-669
25. Ding, L., Stilwell, J., Zhang, T., Elboudwarej, O., Jiang, H., and Selegue, J. P. 2005, Molecular characterization of the cytotoxic mechanism of multiwall carbon nanotubes and nano-onions on human skin fibroblast Nano Lett. 5, 2448-2464 (Pubitemid 43090840)
26. Zhou, H., Mu, Q., Gao, N., Liu, A., Xing, Y., and Gao, S. 2008, A nano-combinatorial library strategy for the discovery of nanotubes with reduced protein-binding, cytotoxicity, and immune response Nano Lett. 8, 859-865
27. Thompson, J., Zamboni, W. C., Cheshire, P. J., Lutz, L., Luo, X., and Li, Y. 1997, Efficacy of systemic administration of irinotecan against neuroblastoma xenografts Clin. Cancer. Res. 3, 423-431 (Pubitemid 27158067)
28. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., and Brown, J. P. 1998, Requirement for p53 and p21 to sustain G2 arrest after DNA damage Science 282, 1497-1501 (Pubitemid 28538613)
29. Maclean, K. H., Dorsey, F. C., Cleveland, J. L., and Kastan, M. B. (2008) Targeting lysosomal degradation induces p53-dependent cell death and prevents cancer in mouse models of lymphomagenesis J. Clin. Invest. 118, 79-88
30. Bai, Y., Zhang, Y., Zhang, J., Mu, Q., Zhang, W., and Butch, E. R. 2010, Repeated administrations of carbon nanotubes in male mice cause reversible testis damage without affecting fertility Nat. Nanotechnol. 5, 683-689
31. Gao, N., Zhang, Q., Mu, Q., Bai, Y., Li, L., and Zhou, H. 2011, Steering carbon nanotubes to scavenger receptor recognition by nanotube surface chemistry modification partially alleviates NF?B activation and reduces its immunotoxicity ACS Nano 5, 4581-4591
32. Kagan, V. E., Tyurina, Y. Y., Tyurin, V. A., Konduru, N. V., Potapovich, A. I., and Osipov, A. N. 2006, Direct and indirect effects of single walled carbon nanotubes on RAW 264.7 macrophages: Role of iron Toxicol. Lett. 165, 88-100 (Pubitemid 43867182)
33. Pumera, M. and Miyahara, Y. (2009) What amount of metallic impurities in carbon nanotubes is small enough not to dominate their redox properties? Nanoscale 1, 260-265
34. Cellot, G., Toma, F. M., Kasap Varley, Z., Laishram, J., Villari, A., and Quintana, M. 2011, Carbon nanotube scaffolds tune synaptic strength in cultured neural circuits: novel frontiers in nanomaterial-tissue interactions J. Neurosci. 31, 12945-12953
35. Veetil, J. V. and Ye, K. (2009) Tailored carbon nanotubes for tissue engineering applications Biotechnol. Prog. 25, 709-721
36. Humphrey, T. and Brooks, G. (2005) Cell Cycle Control-Mechanisms and Protocols, Vol. 296, Humana Press, New York.
37. Sherr, C. J. and McCormick, F. (2002) The RB and p53 pathways in cancer Cancer cell 2, 103-112 (Pubitemid 41039110)
38. Watanabe, G., Pena, P., Shambaugh, G. E., Haines, G. K., and Pestell, R. G. (1998) Regulation of cyclin dependent kinase inhibitor proteins during neonatal cerebella development Brain Res. Dev. Brain Res. 15, 77-87 (Pubitemid 28332821)
39. Pei, X. H. and Xiong, Y. (2005) Biochemical and cellular mechanisms of mammalian CDK inhibitors: a few unresolved issues Oncogene 24, 2787-2795 (Pubitemid 40638090)
40. Modestou, M., Puig-Antich, V., Korgaonkar, C., Eapen, A., and Quelle, D. E. (2001) The alternative reading frame tumor suppressor inhibits growth through p21-dependent and p21-independent pathways Cancer Res. 61, 3145-3150 (Pubitemid 32691967)
41. Wade Harper, J., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases Cell 75, 805-816 (Pubitemid 23346377)
42. Caussinus, E., Kanca, O., and Affolter, M. (2012) Fluorescent fusion protein knockout mediated by anti-GFP nanobody Nat. Struct. Mol. Biol. 19, 117-121
43. Ezhevsky, S. A., Hikaru Nagahara, H, Vocero-Akbani, A. M., Gius, D. R., Wei, M. C., and Dowdy, S. F. (1997) Hypo-phosphorylation of the retinoblastoma protein (pRb) by cyclin D:Cdk4/6 complexes results in active pRb Proc. Natl. Acad. Sci. U.S.A. 94, 10699-10704 (Pubitemid 27430797)
44. Sherr, C. J. and Roberts, J. M. (1995) Inhibitors of mammalian G1 cyclin-dependent kinases Genes. Dev. 9, 1149-1163
45. Li, C., Tzeng, S., Cheng, Y., and Kang, J. (2005) Chloramphenicol-induced mitochondrial stress increases p21 expression and prevents cell apoptosis through a p21-dependent pathway J. Biol. Chem. 282, 26193-26199 (Pubitemid 41022215)
46. Lynch, I. and Dawson, K. A. (2008) Protein-nanoparticle interactions Nano Today 3, 40-47 (Pubitemid 351298587)
47. Pellegata, N. S., Antoniono, R. J., Redpath, J. L., and Stanbridge, E. J. (1996) DNA damage and p53-mediated cell cycle arrest: A reevaluation Proc. Natl. Acad. Sci. U.S.A. 93, 15209-15214 (Pubitemid 27009578)
48. Attardi, L. D., de Vries, A., and Jacks, T. (2004) Activation of the p53-dependent G1 checkpoint response in mouse embryo fibroblasts depends on the specific DNA damage inducer Oncogene 23, 973-980 (Pubitemid 38250943)
49. Jia, G., Wang, H., Yan, L., Wang, X., Pei, R., and Yan, T. 2005, Cytotoxicity of carbon nanomaterials:single-wall nanotube, multi-wall nanotube, and fullerene Environ. Sci. Technol. 39, 1378-1383 (Pubitemid 40333400)
50. Fiorito, S., Serafino, A., Andreola, F., and Bernier, P. (2006) Effects of fullerenes and single-wall carbon nanotubes on murine and human macrophages Carbon 44, 1100-1105 (Pubitemid 43202167)
51. GhibellI, L., De Nicola, M., Somma, G., Cerella, C., DAlessio, M., and Romeo, E. 2005, Lack of direct cytotoxic effect of intracellular nanotubes G. Ital. Med. Lavoro Ergon. 27, 383-384 (Pubitemid 41416205)
52. Macleod, K. F., Sherry, N., Hannon, G., Beach, D., Tokino, T., and Kinzler, K. 1995, p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage Genes. Dev. 9, 935-944
53. Mu, Q., Du, G., Chen, T., Zhang, B., and Yan, B. (2009) Suppression of human bone morphogenetic protein signaling by carboxylated single-walled carbon nanotubes ACS Nano 3, 1139-1144
54. Martinez, V. G., Hernandez-Lopez, C., Valencia, J., Hidalgo, L., Entrena, A., and Zapata, A. G. 2011, The canonical BMP signaling pathway is involved in human monocyte-derived dendritic cell maturation Immunol. Cell Biol. 89, 610-618
55. Pagliuca, A., Gallo, P., De Luca, P., and Lania, L. (2000) Class A helix-loop-helix proteins are positive regulators of several cyclin-dependent kinase inhibitors promoter activity and negatively affect cell growth Cancer Res. 60, 1376-1382 (Pubitemid 30152010)
56. Miyazono, K. and Miyazawa, K. (2002) Id: A target of BMP signaling Sci. STKE 2002, pe40
57. Liu, Y., Encinas, M., Comella, J. X., Aldea, M., and Gallego, C. (2004) Basic helix-loop-helix proteins bind to TrkB and p21Cip1 promoters linking differentiation and cell cycle arrest in neuroblastoma cells Mol. Cell. Biol. 24, 2662-2672 (Pubitemid 38381259)