Molecular responses of human lung epithelial cells to the toxicity of copper oxide nanoparticles inferred from whole genome expression analysis

ACS Nano

Volumn 5, Issue 12, 2011, Pages 9326-9338

  Hanagata, Nobutaka ^a,b   Zhuang, Fei ^a,b   Connolly, Sarah ^a   Li, Jie ^a   Ogawa, Nobuhiro ^a   Xu, Mingsheng ^c  

^a NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

cell cycle arrest; copper oxide nanoparticles; cytotoxicity; DNA microarray; lung epithelial cells

Indexed keywords

A549 CELLS; AURORA KINASE; CELL CYCLE; CELL DIVISIONS; CELL-CYCLE ARREST; COPPER OXIDE NANOPARTICLES; CU IONS; DNA MICROARRAY; DOWN-REGULATION; EXPRESSION ANALYSIS; GROWTH ARREST; HUMAN LUNG; ION CONCENTRATIONS; LUNG EPITHELIAL CELLS; MOLECULAR MECHANISM; MOLECULAR RESPONSE; NUCLEAR RECEPTORS; PROLIFERATING CELL NUCLEAR ANTIGENS; TARGET PROTEINS; UP-REGULATION;

BIOLOGICAL ORGANS; CELL DEATH; CELL PROLIFERATION; COPPER; CYTOTOXICITY; GENES; NANOPARTICLES; TRANSCRIPTION FACTORS;

HEAVY IONS;

COPPER; CUPRIC OXIDE; NANOPARTICLE; PROTEOME;

ARTICLE; CELL LINE; CHROMOSOME MAP; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; LUNG; MATERIALS TESTING; METABOLISM;

CELL LINE; CHROMOSOME MAPPING; COPPER; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; LUNG; MATERIALS TESTING; NANOPARTICLES; PROTEOME;

EID: 84555169247     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn202966t     Document Type: Article

References (58)

1. Xu, M.; Fujita, D.; Kajiwara, S.; Minowa, T.; Li, X.; Takemura, T.; Iwai, H.; Hanagata, N. Contribution of Physicochemical Characteristics of Nano-oxides to Cytotoxicity Biomaterials 2010, 31, 8022-8031
2. Hanagata, N.; Xu, M.; Takemura, T.; Zhuang, F. Cellular Response to ZnO Nanoparticle Toxicity Inferred from Global Gene Expression Profiles Nano Biomed. 2010, 2, 153-169
3. Gabbay, J.; Borkow, G.; Mishal, J.; Magen, E.; Zatcoff, R.; Shemer-Avni, Y. Copper Oxide Impregnated Textiles with Potent Biocidal Activity J. Ind. Textiles 2006, 35, 323-335
4. Chang, H.; Jwo, C. S.; Lo, C. H.; Tsung, T. T.; Kao, M. J.; Lin, H. M. Rheology of CuO Nanoparticle Suspension Prepared by ASNSS Rev. Adv. Mater. Sci. 2005, 10, 128-132 (Pubitemid 41294655)
5. Zhou, K.; Wang, R.; Xu, B.; Li, Y. Synthesis, Characterization and Catalytic Properties of CuO Nanoparticles with Various Shapes Nanotechnology 2006, 17, 3939-3943 (Pubitemid 44424439)
6. Cioffi, N.; Ditaranto, N.; Torsi, L.; Picca, R. A.; Sabbatini, L.; Valentini, A.; Novell, L.; Tantillo, G.; Bleve-Zacheo, T.; Zambonin, P. G. Analytical Characterization of Bioactive Fluoropolymer Ultra-thin Coatings Modified by Copper Nanoparticles Anal. Bioanal. Chem. 2005, 381, 607-616 (Pubitemid 40379331)
7. Xu, L.; Takemura, T.; Xu, M.; Hanagata, N. Toxicity of Silver Nanoparticles As Assessed by Global Gene Expression Analysis Mater. Exp. 2011, 1, 74-79
8. Ahamed, M.; Siddiqui, M. A.; Akhtar, M. J.; Ahmad, I.; Pant, A. B.; Alhadlaq, H. A. Genotoxic Potential of Copper Oxide Nanoparticles in Human Lung Epithelial Cells Biochem. Biophys. Res. Commun. 2010, 396, 578-583
9. Midander, K.; Cronholm, P.; Karlsson, H. L.; Elihn, K.; Moeller, L.; Leygraf, C.; Wallinder, I. O. Surface Characteristics, Copper Release, and Toxicity of Nano- and Micrometer-Sized Copper and Copper(II) Oxide Particles: A Cross-Disciplinary Study Small 2009, 5, 389-399
10. Karlsson, H. L; Cronholm, P; Gustafsson, J; Moeller, L. Copper Oxide Nanoparticles Are Highly Toxic: Comparison between Metal Oxide Nanoparticles and Carbon Nanotubes Chem. Res. Toxicol. 2008, 21, 1726-1732
11. Zhan, Q.; Lord, K. A.; Alamo, I., Jr.; Hollander, M. C.; Carrier, F.; Ron, D.; Kohn, K. W.; Hoffman, B.; Liebermann, D. A.; Fornace, A. J., Jr. The Gadd and MyD Genes Define a Novel Set of Mammalian Genes Encoding Acidic Proteins That Synergistically Suppress Cell Growth Mol. Cell. Biol. 1994, 14, 2361-2371 (Pubitemid 24108218)
12. Fornace, A. J.; Jackman, J.; Hollander, M. C.; Hoffman-Liebermann, B.; Liebermann, D. A. Genotoxic-Stress-Response Genes and Growth Arrest Genes: Gadd, MyD, and Other Genes Induced by Treatments Eliciting Growth Arrest Ann. N.Y. Acad. Sci. 1992, 663, 139-154
13. Papathanasiou, M. A.; Kerr, N. C.; Robbins, J. H.; McBride, O. W.; Alamo, I., Jr.; Barrett, S. F.; Hickson, I. D.; Fornace, A. J., Jr. Mammalian Genes Coordinately Regulated by Growth Arrest Signals and DNA-Damaging Agents Mol. Cell. Biol. 1989, 10, 4196-4203 (Pubitemid 19239587)
14. Zhang, W.; Bae, I.; Krishnaraju, K.; Azam, N.; Fan, W.; Smith, K.; Hoffman, B.; Liebermann, D. A. CR6: A Third Member in the MyD118 & Gadd 45 Gene Family Which Functions in Negative Growth Control Oncogene 1999, 18, 4899-4907 (Pubitemid 29425296)
15. Beadling, C.; Johnson, K. W.; Smith, K. A. Isolation of Interleukin 2-Induced Immediate-Early Genes Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 2719-2723 (Pubitemid 23113488)
16. Liebermann, D. A.; Hoffman, B. MyD Genes in Negative Growth Control Oncogene Rev. 1998, 17, 3319-3330
17. Vairapandi, M.; Balliet, A. G.; Hoffman, B.; Liebermann, D. A. GADD45b and GADD45g Are cdc2/cyclinB1 Kinase Inhibitors with a Role in S and G2/M Cell Cycle Checkpoints Induced by Genotoxic Stress J. Cell Physiol. 2002, 192, 327-338 (Pubitemid 34827609)
18. Wang, X. W.; Zhan, Q.; Coursen, J. D.; Khan, M. A.; Kontny, H. U.; Yu, L.; Hollander, M. C.; OConnor, P. M.; Fornace, A. J., Jr.; Harris, C. C. GADD45 Induction of a G2/M Cell Cycle Checkpoint Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 3706-3711 (Pubitemid 29168974)
19. Jin, S.; Antinore, M. J.; Lung, F. D.; Dong, X.; Zhao, H.; Fan, F.; Colchagie, A. B.; Blanck, P. The GADD45 Inhibition of Cdc2 Kinase Correlates with GADD45-Mediated Growth Suppression J. Biol. Chem. 2000, 275, 16602-16608 (Pubitemid 30398886)
20. Vairapandi, M.; Balliet, A. G.; Hoffman, B.; Liebermann, D. A. The Differentiation Primary Response Gene MyD118, Related to GADD45, Encodes for a Nuclear Protein Which Interacts with PCNA and p21WAF1/CIP1 Oncogene 1996, 12, 2579-2594 (Pubitemid 26237787)
21. Smith, M. L.; Chen, I. T.; Zhan, Q.; Bae, I.; Chen, C. Y.; Gilmer, T. M.; Kastan, M. B.; OConnor, P. M.; Fornace, A. J., Jr. Protein Interaction of the p53-Regulated Protein Gadd45 with Proliferating Cell Nuclear Antigen Science 1994, 266, 1376-1380
22. Smith, M. L.; Ford, J. M.; Hollander, M. C.; Bortnick, R. A.; Amundson, S. A.; Seo, Y. R.; Deng, C.-X.; Hanawalt, P. C.; Fornace, A. J., Jr. p53-Mediated DNA Repair Responses to UV Radiation: Studies of Mouse Cells Lacking p53, p21, and/or Gadd45 Genes Mol. Cell. Biol. 2000, 20, 3705-3714 (Pubitemid 30243916)
23. Smith, M. L.; Kontny, H. U.; Zhan, Q.; Sreenath, A.; OConnor, P. M.; Fornace, A. J., Jr. Antisense GADD45 Expression Results in Decreased DNA Repair and Sensitizes Cells to U.V.-Irradiation or Cisplatin Oncogene 1996, 13, 2255-2263 (Pubitemid 26411576)
24. Gupta, M.; Gupta, S. K.; Balliet, A. G.; Hollander, M. C.; Albert, J.; Fornace, A. J., Jr.; Hoffman, B.; Liebermann, D. A. Hematopoietic Cells from Gadd45a and Gadd45b Deficient Mice Are Sensitized to Genotoxic-Stress Induced Apoptosis Oncogene 2005, 24, 7170-7179 (Pubitemid 41679279)
25. Gupta, M.; Gupta, S. K.; Hoffman, B.; Liebermann, D. A. Gadd45a gadd45b Protect Hematopoietic Cells from UV Induced Apoptosis via Distinct Signaling Pathways Including p38 Activation and JNK Inhibition J. Biol. Chem. 2006, 281, 17552-17558 (Pubitemid 44035554)
26. De Smaele, E.; Zazzeroni, F.; Papa, S.; Nguyen, D. U.; Jin, R.; Jones, J.; Cong, R.; Franzoso, G. Induction of Gadd45β by NF-κB Downregulates Pro-apoptotic JNK Signalling Nature 2001, 414, 308-313 (Pubitemid 33097807)
27. Amanullah, A.; Azam, N.; Balliet, A.; Hollander, C.; Hoffman, B.; Fornace, A.; Liebermann, D. Cell Signalling: Cell Survival and a Gadd45-Factor Deficiency Nature 2003, 424, 741-742 (Pubitemid 37021694)
28. Takekawa, M.; Saito, H. A Family of Stress-Inducible GADD45-like Proteins Mediate Activation of the Stress-Responsive MTK1/MEKK4/MAPKKK Cell 1998, 95, 521-530 (Pubitemid 28533308)
29. Selvakumaran, M.; Lin, H. K.; Miyashita, T.; Wang, H. G.; Krajewski, S.; Reed, J. C.; Hoffman, B.; Liebermann, D. Immediate Early Up-Regulation of Bax Expression by p53 But Not TGF beta 1: A Paradigm for Distinct Apoptotic Pathways Oncogene 1994, 9, 1791-1798 (Pubitemid 24163410)
30. Selvakumaran, M.; Lin, H. K.; Tjin Tham Sjin, R.; Reed, J.; Liebermann, D.; Hoffman, B. The Novel Primary Response Gene MyD118 and the Proto-Oncogenes Myb, Myc and Bcl-2 Modulate Transforming Growth Factor b1-Induced Apoptosis of Myeloid Leukemia Cells Mol. Cell. Biol. 1994, 14, 2352-2360 (Pubitemid 24108217)
31. Zhang, W.; Hoffman, B.; Liebermann, D. A. Ectopic Expression of MyD118/Gadd45/CR6 (Gadd45beta/alpha/gamma) Sensitizes Neoplastic Cells to Genotoxic Stress-Induced Apoptosis Int. J. Oncol. 2001, 18, 749-757
32. Yoo, J.; Ghiassi, M.; Jirmanova, L.; Balliet, A. G.; Hoffman, B.; Fornace, A. J., Jr.; Liebermann, D. A.; Bottinger, E. P.; Roberts, A. B. TGF-beta-Induced Apoptosis Is Mediated by Smad-Dependent Expression of GADD45B through p38 Activation J. Biol. Chem. 2003, 278, 43001-43007 (Pubitemid 37345913)
33. Vairapandi, M.; Azam, N.; Balliet, A. G.; Hoffmann, D. A. Characterization of MyD118, Gadd45, and PCNA Impedes MyD/Gadd45 Mediated Negative Growth Control J. Biol. Chem. 2000, 275, 16810-16819
34. Azam, N.; Vairapandi, M.; Zhang, W.; Hoffman, B.; Liebermann, D. A. Interaction of CR6 (GADD45 gamma) with Proliferating Cell Nuclear Antigen Impedes Negative Growth Control J. Biol. Chem. 2001, 276, 2766-2774
35. Harkin, D. P.; Bean, J. M.; Miklos, D.; Song, Y. H.; Truong, V. B.; Englert, C.; Christians, F. C. Induction of GADD45 and JNK/SAPK-Dependent Apoptosis Following Inducible Expression of BRCA1 Cell 1999, 97, 575-586 (Pubitemid 29256961)
36. Kojima, S.; Mayumi-Matsuda, K.; Suzuki, H.; Sakata, T. Molecular Cloning of Rat GADD45gamma, Gene Induction and Its Role during Neuronal Cell Death FEBS Lett. 1999, 446, 313-317 (Pubitemid 29132750)
37. Hildesheim, J.; Bulavin, D. V.; Anver, M. R.; Alvord, W. G.; Hollander, M. C.; Vardanian, L.; Fornace, A. J., Jr. Gadd45a Protects Against UV Irradiation-Induced Skin Tumors, and Promotes Apoptosis and Stress Signaling via MAPK and p53 Cancer Res. 2002, 62, 7305-7315 (Pubitemid 36025254)
38. CDKN1A Does Not Interfere with Loading of PCNA at DNA Replication Sites, but Inhibits Subsequent Binding of DNA Polymerase δ at the G1/S Phase Transition Cell Cycle 2003, 2, 596-603
39. OConnor, P. M. Mammalian G1 and G2 Phase Checkpoints Cancer Surv. 1997, 29, 151-182
40. Elledge, S. J. Cell Cycle Checkpoints: Preventing an Identity Crisis Science 1996, 274, 1664-1672 (Pubitemid 26414889)
41. Kufer, T. A.; Sillje, H. H. W.; Koerner, R.; Gruss, O.; Meraldi, P.; Nigg, E. Human TPX2 Is Required for Targeting Aurora-A Kinase to the Spindle J. Cell Biol. 2002, 158, 617-623 (Pubitemid 34920101)
42. Lu, B.; Yu, H.; Chow, C.; Li, B.; Zheng, W.; Davis, R. J.; Flavell, R. A. GADD45gamma Mediates the Activation of the p38 and JNK MAP Kinase Pathways and Cytokine Production in Effector TH1 Cells Immunity 2001, 14, 583-590 (Pubitemid 32520869)
43. Yang, J.; Zhu, H.; Murphy, T. L.; Ouyang, W.; Murphy, K. M. IL-18-Stimulated GADD45 beta Required in Cytokine-Induced, but Not TCR-Induced, IFN-gamma Production Nat. Immunol. 2001, 2, 157-164 (Pubitemid 33707936)
44. Angel, P.; Karin, M. The Role of Jun, Fos and the AP-1 Complex in Cell-Proliferation and Transformation Biochim. Biophys. Acta 1991, 1072, 129-157 (Pubitemid 121007534)
45. Karin, M.; Liu, Z.-G.; Zandi, E. AP-1 Function and Regulation Curr. Opin. Cell Biol. 1997, 9, 240-246 (Pubitemid 27135992)
46. Shaulian, E.; Karin, M. AP-1 in Cell Proliferation and Survival Oncogene 2001, 20, 2390-2400 (Pubitemid 32531297)
47. Shaulian, E.; Karin, M. AP-1 As a Regulator of Cell Life and Death Nat. Cell Biol. 2002, 4, E131-E136
48. Li, Q. X.; Ke, N.; Sundaram, R.; Wong-Staal, F. NR4A1, 2, 3 - An Orphan Nuclear Hormone Receptor Family Involved in Cell Apoptosis and Carcinogenesis Histol. Histopathol. 2006, 21, 533-540
49. Moll, U. M.; Marchenko, N.; Zhang, X.-K. p53 and Nur77/TR3-Transcription Factors That Directly Target Mitochondria for Cell Death Induction Oncogene 2006, 25, 4725-4743 (Pubitemid 44187622)
50. Giono, L. E.; Manfreid, J. J. The p53 Tumor Suppressor Participates in Multiple Cell Cycle Checkpoints J. Cell. Physiol. 2006, 209, 13-20 (Pubitemid 44318664)
51. Kastan, M. B.; Zhan, Q.; El-Deiry, W. S.; Carrier, F.; Jacks, T.; Walsh, W. V.; Plunkett, B. S.; Vogelstein, B.; Fornace, A. J., Jr. A Mammalian Cell Cycle Checkpoint Pathway Utilizing p53 and GADD45 is Defective in Ataxia-Telangiectasia Cell 1992, 71, 587-597
52. Guillouf, C.; Grana, X.; Selvakumaran, M.; Hoffman, B.; Giordano, A.; Liebermann, D. A. Dissection of the Genetic Programs of p53-Mediated G1 Growth Arrest and Apoptosis: Blocking p53-Induced Apoptosis Unmasks G1 Arrest Blood 1995, 85, 2691-269
53. Vogelstein, B.; Lane, D.; Levine, A. J. Surfing the p53 Network Nature 2000, 408, 307-310
54. Vousden, K. H. p53: Death Star Cell 2000, 103, 691-694
55. Andrews, G. K. Regulation of Metallothionein Gene Expression by Oxidative Stress and Metal Ions Biochem. Pharmacol. 2000, 59, 95-104
56. Huang, Y.-C. T.; Li, Z.; Carter, J. D.; Soukup, J. M.; Schwartz, D. A.; Yang, I. V. Fine Ambient Particles Induce Oxidative Stress and Metal Binding Genes in Human Alveolar Macrophages Am. J. Respir. Cell Mol. Biol. 2009, 41, 544-552
57. Min, K.-S.; Morishita, F.; Tetsuchikawahara, N.; Onosaka, S. Induction of Hepatic and Renal Metallothionein Synthesis by Ferric Nitrilotriacetate in Mice: The Role of MT as an Antioxidant Toxicol. Appl. Pharmacol. 2005, 204, 9-17 (Pubitemid 40387563)
58. Kumari, M. V. R.; Hiramatsu, M.; Ebadi, M. Free Radical Scavenging Actions of Metallothionein Isoforms I and II Free Radical Res. 1998, 29, 93-101 (Pubitemid 28451388)