Mitochondrial Impairment Induced by Sub-Chronic Exposure to Multi-Walled Carbon Nanotubes
Abstract
:1. Introduction
2. Materials and Methods
2.1. Pristine and Functionalized MWCNTs
2.2. Cell Cultures and Exposure Conditions
2.3. Evaluation of Mitochondrial and Cellular Enzymatic Activity and Cytochrome c Release
2.4. Assessment of mPTP Opening
2.5. Fluorimetric Analysis for the Assessment of Mitochondrial Transmembrane Potential and ROS Production
2.6. Apoptosis Detection
2.7. Cell Proliferation Index
2.8. Statistical Analyses
3. Results
3.1. MWCNT Effects in Lung Epithelial Cells
3.2. Mitochondrial Impairment and MWCNT-Induced Apoptosis
3.3. Cellular Enzymatic Activity and ROS Production in Exposed Cells
3.4. Proliferation Index
4. Discussion
Author Contributions
Funding
Conflicts of Interest
References
- Mercer, R.R.; Hubbs, A.F.; Scabilloni, J.F.; Wang, L.; Battelli, L.A.; Schwegler-Berry, D.; Castranova, V.; Porter, D.W. Distribution and persistence of pleural penetrations by multi-walled carbon nanotubes. Part. Fibre Toxicol. 2010, 4, 7–28. [Google Scholar]
- Helland, A.; Wick, P.; Koehler, A.; Schmid, K.; Som, C. Reviewing the environmental and human health knowledge base of carbon nanotubes. Environ. Health Perspect. 2007, 115, 1125–1131. [Google Scholar] [CrossRef] [PubMed]
- Kayat, J.; Gajbhiye, V.; Tekade, R.K.; Jain, N.K. Pulmonary toxicity of carbon nanotubes: A systematic report. Nanomedicine 2011, 7, 40–49. [Google Scholar] [CrossRef] [PubMed]
- Sobhani, Z.; Behnam, M.A.; Emami, F.; Dehghanian, A.; Jamhiri, I. Photothermal therapy of melanoma tumor using multiwalled carbon nanotubes. Int. J. Nanomed. 2017, 12, 4509–4517. [Google Scholar] [CrossRef] [PubMed]
- Cha, C.; Shin, S.R.; Annabi, N.; Dokmeci, M.R.; Khademhosseini, A. Carbon-based nanomaterials: Multifunctional materials for biomedical engineering. ACS Nano 2013, 7, 2891–2897. [Google Scholar] [CrossRef] [PubMed]
- Shvedova, A.A.; Pietroiusti, A.; Fadeel, B.; Kagan, V.E. Mechanisms of carbon nanotube—Induced toxicity: Focus on oxidative stress. Toxicol. Appl. Pharmacol. 2012, 261, 121–133. [Google Scholar] [CrossRef] [PubMed]
- Nagai, H.; Okazaki, Y.; Chew, S.H.; Misawa, N.; Yamashita, Y.; Akatsuka, S.; Ishihara, T.; Yamashita, K.; Yoshikawa, Y.; Yasui, H.; et al. Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. Proc. Natl. Acad. Sci. USA 2011, 108, E1330–E1388. [Google Scholar] [CrossRef] [PubMed]
- Tabet, L.; Bussy, C.; Setyan, A.; Simon-Deckers, A.; Rossi, M.J.; Boczkowski, J.; Lanone, S. Coating carbon nanotubes with a polystyrene-based polymer protects against pulmonary toxicity. Part. Fibre Toxicol. 2011, 8, 3. [Google Scholar] [CrossRef] [Green Version]
- Schrurs, F.; Lison, D. Focusing the research efforts. Nat. Nano 2012, 7, 546–548. [Google Scholar] [CrossRef] [PubMed]
- Kumarathasan, P.; Breznan, D.; Das, D.; Salam, M.A.; Siddiqui, Y.; MacKinnon-Roy, C.; Guan, J.; De Silva, N.; Simard, B.; Vincent, R. Cytotoxicity of carbon nanotube variants: A comparative in vitro exposure study with A549 epithelial and J774 macrophage cells. Nanotoxicology 2015, 2, 148–161. [Google Scholar] [CrossRef] [PubMed]
- Bussy, C.; Paineau, E.; Cambedouzou, J.; Brun, N.; Mory, C.; Fayard, B.; Salomé, M.; Pinault, M.; Huard, M.; Belade, E.; et al. Intracellular fate of carbon nanotubes inside murine macrophages: pH-dependent detachment of iron catalyst nanoparticles. Part. Fibre Toxicol. 2013, 10, 24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Visalli, G.; Facciolà, A.; Iannazzo, D.; Piperno, A.; Pistone, A.; Di Pietro, A. The role of the iron catalyst in the toxicity of multi-walled carbon nanotubes (MWCNTs). J. Trace Elem. Med. Biol. 2017, 43, 153–160. [Google Scholar] [CrossRef] [PubMed]
- Kolosnjaj-Tabi, J.; Hartman, K.B.; Boudjemaa, S.; Ananta, J.S.; Morgant, G.; Szwarc, H.; Wilson, L.J.; Moussa, F. In vivo behavior of large doses of ultrashort and full-length single-walled carbon nanotubes after oral and intraperitoneal administration to Swiss mice. ACS Nano 2010, 4, 1481–1492. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Wang, B.; Meng, X.; Sun, G.; Gao, C. Influences of acid-treated multiwalled carbon nanotubes on fibroblasts: Proliferation, adhesion, migration, and wound healing. Ann. Biomed. Eng. 2011, 39, 414–426. [Google Scholar] [CrossRef] [PubMed]
- Donaldson, K.; Murphy, F.; Schinwald, A.; Duffin, R.; Poland, C.A. Identifying the pulmonary hazard of high aspect ratio nanoparticles to enable their safety-by-design. Nanomedicine 2012, 6, 143–156. [Google Scholar] [CrossRef] [PubMed]
- Fubini, B.; Fenoglio, I.; Tomatis, M.; Turci, F. Effect of chemical composition and state of the surface on the toxic response to high aspect ratio nanomaterials. Nanomedicine 2011, 6, 899–920. [Google Scholar] [CrossRef] [PubMed]
- Møller, P.; Christophersen, D.V.; Jensen, D.M.; Kermanizadeh, A.; Roursgaard, M.; Jacobsen, N.R.; Hemmingsen, J.G.; Danielsen, P.H.; Cao, Y.; Jantzen, K.; et al. Role of oxidative stress in carbon nanotube-generated health effects. Arch. Toxicol. 2014, 88, 1939–1964. [Google Scholar] [CrossRef] [PubMed]
- Visalli, G.; Bertuccio, M.P.; Iannazzo, D.; Piperno, A.; Pistone, A.; Di Pietro, A. Toxicological assessment of multi-walled carbon nanotubes on A549 human lung epithelial cells. Toxicol. In Vitro 2015, 29, 352–362. [Google Scholar] [CrossRef] [PubMed]
- Visalli, G.; Currò, M.; Iannazzo, D.; Pistone, A.; Pruiti Ciarello, M.; Acri, G.; Testagrossa, B.; Bertuccio, M.P.; Squeri, R.; Di Pietro, A. In vitro assessment of neurotoxicity and neuroinflammation of homemade MWCNTs. Environ. Toxicol. Pharmacol. 2017, 56, 121–128. [Google Scholar] [CrossRef] [PubMed]
- Velali, E.; Papachristou, E.; Pantazaki, A.; Choli-Papadopoulou, T.; Planou, S.; Kouras, A.; Manoli, E.; Besis, A.; Voutsa, D.; Samara, C. Redox activity and in vitro bioactivity of the water-soluble fraction of urban particulate matter in relation to particle size and chemical composition. Environ. Pollut. 2016, 208, 774–786. [Google Scholar] [CrossRef] [PubMed]
- Zhou, W.; Tian, D.; He, J.; Zhang, L.; Tang, X.; Zhang, L.; Wang, Y.; Li, L.; Zhao, J.; Yuan, X.; et al. Exposure scenario: Another important factor determining the toxic effects of PM2.5 and possible mechanisms involved. Environ. Pollut. 2017, 226, 412–425. [Google Scholar] [CrossRef] [PubMed]
- Huang, S.X.; Partridge, M.A.; Ghandhi, S.A.; Davidson, M.M.; Amundson, S.A.; Hei, T.K. Mitochondria-derived reactive intermediate species mediate asbestos-induced genotoxicity and oxidative stress-responsive signaling pathways. Environ. Health Perspect. 2012, 120, 840–847. [Google Scholar] [CrossRef] [PubMed]
- Di Pietro, A.; Visalli, G.; Baluce, B.; Micale, R.T.; La Maestra, S.; Spataro, P.; De Flora, S. Multigenerational mitochondrial alterations in pneumocytes exposed to oil fly ash metals. Int. J. Hyg. Environ. Health 2011, 214, 138–144. [Google Scholar] [CrossRef] [PubMed]
- Visalli, G.; Baluce, B.; Bertuccio, M.P.; Picerno, I.; Di Pietro, A. Mitochondrial-mediated apoptosis pathway in alveolar epithelial cells exposed to the metals in combustion-generated particulate matter. J. Toxicol. Environ. Health A 2015, 78, 697–709. [Google Scholar] [CrossRef] [PubMed]
- Visalli, G.; Bertuccio, M.P.; Picerno, I.; Spataro, P.; Di Pietro, A. Mitochondrial dysfunction by pro-oxidant vanadium: Ex vivo assessment of individual susceptibility. Environ. Toxicol. Pharmacol. 2015, 39, 93–101. [Google Scholar] [CrossRef] [PubMed]
- Green, D.R.; Llambi, F. Cell Death Signaling. Cold Spring Harb. Perspect. Biol. 2015, 7, a006080. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trifunovic, A.; Larsson, N.G. Mitochondrial dysfunction as a cause of ageing. J. Intern. Med. 2008, 263, 167–178. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cheng, W.W.; Lin, Z.Q.; Wei, B.F.; Zeng, Q.; Han, B.; Wei, C.X.; Fan, X.J.; Hu, C.L.; Liu, L.H.; Huang, J.H.; et al. Single-walled carbon nanotube induction of rat aortic endothelial cell apoptosis: Reactive oxygen species are involved in the mitochondrial pathway. Int. J. Biochem. Cell Biol. 2011, 43, 564–572. [Google Scholar] [CrossRef] [PubMed]
- Liu, Z.; Dong, X.; Song, L.; Zhang, H.; Liu, L.; Zhu, D.; Song, C.; Leng, X. Carboxylation of multiwalled carbon nanotube enhanced its biocompatibility with L02 cells through decreased activation of mitochondrial apoptotic pathway. J. Biomed. Mater. Res. A 2014, 102, 665–673. [Google Scholar] [CrossRef] [PubMed]
- Paradies, G.; Paradies, V.; De Benedictis, V.; Ruggiero, F.M.; Petrosillo, G. Functional role of cardiolipin in mitochondrial bioenergetics. Biochim. Biophys. Acta 2014, 1837, 408–417. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, J.; Huang, K.; O’Neill, K.L.; Pang, X.; Luo, X. Bax/Bak activation in the absence of Bid, Bim, Puma, and p53. Cell Death Dis. 2016, 7, e2266. [Google Scholar] [CrossRef] [PubMed]
- Pena-Blanco, A.; Garcia-Saez, A.J. Bax, Bak and beyond—Mitochondrial performance in apoptosis. FEBS J. 2017, 285, 416–431. [Google Scholar] [CrossRef] [PubMed]
- Monian, P.; Jiang, X. Clearing the final hurdles to mitochondrial apoptosis: Regulation post cytochrome C release. Exp. Oncol. 2012, 34, 185–191. [Google Scholar] [PubMed]
- Pistone, A.; Ferlazzo, A.; Lanza, M.; Milone, C.; Iannazzo, D.; Piperno, A.; Piperopoulos, E.; Galvagno, S. Morphological modification of MWCNT functionalized with HNO3/H2SO4 mixtures. J Nanosci. Nanotechnol. 2012, 12, 5054–5060. [Google Scholar] [CrossRef] [PubMed]
- Iannazzo, D.; Piperno, A.; Ferlazzo, A.; Pistone, A.; Milone, C.; Lanza, M.; Cimino, F.; Speciale, A.; Trombetta, D.; Saija, A.; et al. Functionalization of multi-walled carbon nanotubes with coumarin derivatives and their biological evaluation. Org. Biomol. Chem. 2012, 10, 1025–1031. [Google Scholar] [CrossRef] [PubMed]
- Petronilli, V.; Miotto, G.; Canton, M.; Brini, M.; Colonna, R.; Bernardi, P.; Di Lisa, F. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 1999, 76, 725–734. [Google Scholar] [CrossRef]
- Mu, Q.; Broughton, D.L.; Yan, B. Endosomal leakage and nuclear translocation of multiwalled carbon nanotubes: Developing a model for cell uptake. Nano Lett. 2009, 12, 4370–4375. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.T.; Rubio, N.; Kafa, H.; Venturelli, E.; Fabbro, C.; Ménard-Moyon, C.; Da Ros, T.; Sosabowski, J.K.; Lawson, A.D.; Robinson, M.K.; et al. Kinetics of functionalised carbon nanotube distribution in mouse brain after systemic injection: Spatial to ultra-structural analyses. J. Control. Release 2016, 224, 22–32. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trovato, M.C.; Andronico, D.; Sciacchitano, S.; Ruggeri, R.M.; Picerno, I.; Di Pietro, A.; Visalli, G. Nanostructures: Between natural environment and medical practice. Rev. Environ. Health 2018, 33, 259–307. [Google Scholar] [CrossRef] [PubMed]
- Facciolà, A.; Visalli, G.; La Maestra, S.; Ceccarelli, M.; D’Aleo, F.; Nunnari, G.; Pellicanò, G.F.; Di Pietro, A. Carbon nanotubes and central nervous system: Environmental risks, toxicological aspects and future perspectives. Environ. Toxicol. Pharmacol. 2019, 65, 23–30. [Google Scholar] [CrossRef]
- Bonora, M.; Morganti, C.; Morciano, G.; Giorgi, C.; Wieckowski, M.R.; Pinton, P. Comprehensive analysis of mitochondrial permeability transition pore activity in living cells using fluorescence-imaging-based techniques. Nat. Protoc. 2016, 11, 1067–1080. [Google Scholar] [CrossRef] [PubMed]
- Estaquier, J.; Vallette, F.; Vayssiere, J.L.; Mignotte, B. The mitochondrial pathways of apoptosis. Adv. Exp. Med. Biol. 2012, 942, 157–183. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.T.; Wu, S.B.; Wei, Y.H. Metabolic reprogramming of human cells in response to oxidative stress: Implications in the pathophysiology and therapy of mitochondrial diseases. Curr. Pharm. Des. 2014, 20, 5510–5526. [Google Scholar] [CrossRef] [PubMed]
- De Marchi, E.; Bonora, M.; Giorgi, C.; Pinton, P. The mitochondrial permeability transition pore is a dispensable element for mitochondrial calcium efflux. Cell Calcium 2014, 56, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Milane, L.; Trivedi, M.; Singh, A.; Talekar, M.; Amiji, M. Mitochondrial biology, targets, and drug delivery. J. Control. Release 2015, 207, 40–58. [Google Scholar] [CrossRef] [PubMed]
- Braymer, J.J.; Lill, R. Iron-sulfur cluster biogenesis and trafficking in mitochondria. J. Biol. Chem. 2017, 292, 12754–12763. [Google Scholar] [CrossRef] [PubMed]
- Lopez-Fabuel, I.; Le Douce, J.; Logan, A.; James, A.M.; Bonvento, G.; Murphy, M.P.; Almeida, A.; Bolanos, J.P. Complex I assembly into supercomplexes determines differential mitochondrial ROS production in neurons and astrocytes. Proc. Natl. Acad. Sci. USA 2016, 113, 13063–13068. [Google Scholar] [CrossRef] [PubMed]
- Nelson, G.; Wordsworth, J.; Wang, C.; Jurk, D.; Lawless, C.; Martin-Ruiz, C.; von Zglinicki, T.A. senescent cell bystander effect: Senescence-induced senescence. Aging Cell 2012, 11, 345–349. [Google Scholar] [CrossRef] [PubMed]
- Groebe, K.; Krause, F.; Kunstmann, B.; Unterluggauer, H.; Reifschneider, N.H.; Scheckhuber, C.Q.; Sastri, C.; Stegmann, W.; Wozny, W.; Schwall, G.P.; et al. Differential proteomic profiling of mitochondria from Podospora anserina, rat and human reveals distinct patterns of age-related oxidative changes. Exp. Gerontol. 2007, 42, 887–898. [Google Scholar] [CrossRef] [PubMed]
- Bause, A.S.; Haigis, M.C. SIRT3 regulation of mitochondrial oxidative stress. Exp. Gerontol. 2013, 48, 634–639. [Google Scholar] [CrossRef] [PubMed]
- Szklarczyk, R.; Nooteboom, M.; Osiewacz, H.D. Control of mitochondrial integrity in ageing and disease. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369, 201304439. [Google Scholar] [CrossRef] [PubMed]
- Lopez-Otin, C.; Blasco, M.A.; Partridge, L.; Serrano, M.; Kroemer, G. The hallmarks of aging. Cell 2013, 153, 1194–1217. [Google Scholar] [CrossRef] [PubMed]
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Visalli, G.; Facciolà, A.; Currò, M.; Laganà, P.; La Fauci, V.; Iannazzo, D.; Pistone, A.; Di Pietro, A. Mitochondrial Impairment Induced by Sub-Chronic Exposure to Multi-Walled Carbon Nanotubes. Int. J. Environ. Res. Public Health 2019, 16, 792. https://doi.org/10.3390/ijerph16050792
Visalli G, Facciolà A, Currò M, Laganà P, La Fauci V, Iannazzo D, Pistone A, Di Pietro A. Mitochondrial Impairment Induced by Sub-Chronic Exposure to Multi-Walled Carbon Nanotubes. International Journal of Environmental Research and Public Health. 2019; 16(5):792. https://doi.org/10.3390/ijerph16050792
Chicago/Turabian StyleVisalli, Giuseppa, Alessio Facciolà, Monica Currò, Pasqualina Laganà, Vincenza La Fauci, Daniela Iannazzo, Alessandro Pistone, and Angela Di Pietro. 2019. "Mitochondrial Impairment Induced by Sub-Chronic Exposure to Multi-Walled Carbon Nanotubes" International Journal of Environmental Research and Public Health 16, no. 5: 792. https://doi.org/10.3390/ijerph16050792