Proteomics and Toxicity Analysis of Spinal-Cord Primary Cultures upon Hydrogen Sulfide Treatment
Abstract
:1. Introduction
2. Material and Methods
2.1. Primary Spinal-Cord Culture
2.2. Proteomic Analysis
2.3. Bioinfomatic Analysis
2.4. Protein Ontologies and Network Analysis
2.5. Toxicity Experiments
3. Results
3.1. Proteome Profiling Using Label-Free Proteomics Analysis
3.2. Expression of Inflammation and Oxidative Stress-Related Pathways Is Modified after H2S Treatment
3.3. Hydrogen Sulfide Toxicity Operates through Apoptotic and Necroptotic Pathways
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Davoli, A.; Greco, V.; Spalloni, A.; Guatteo, E.; Neri, C.; Rizzo, G.R.; Cordella, A.; Romigi, A.; Cortese, C.; Bernardini, S.; et al. Evidence of hydrogen sulfide involvement in amyotrophic lateral sclerosis. Ann. Neurol. 2015, 77, 697–709. [Google Scholar] [CrossRef] [PubMed]
- Mustafa, A.K.; Gadalla, M.M.; Snyder, S.H. Signaling by gasotransmitters. Sci. Signal. 2009, 28, re2. [Google Scholar] [CrossRef] [PubMed]
- Szabo, C. Gastransmitters: New frontiers for translational science. Sci. Transl. Med. 2010, 2, 59ps54. [Google Scholar] [CrossRef] [PubMed]
- Paul, B.D.; Snyder, S.H. Gasotransmitter hydrogen sulfide signaling in neuronal health and disease. Biochem. Pharmacol. 2018, 149, 101–109. [Google Scholar] [CrossRef] [PubMed]
- Kimura, H. Signaling molecules: Hydrogen sulfide and polysulfide. Antioxid. Redox Signal. 2015, 22, 362–376. [Google Scholar] [CrossRef] [PubMed]
- Hu, L.F.; Lu, M.; Tiong, C.X.; Dawe, G.S.; Hu, G.; Bian, J.S. Neuroprotective effects of hydrogen sulfide on Parkinson’s disease rat models. Aging Cell 2010, 9, 135–146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cui, W.; Zhang, Y.; Yang, C.; Sun, Y.; Zhang, M.; Wang, S. Hydrogen sulfide prevents Abeta-induced neuronal apoptosis by attenuating mitochondrial translocation of PTEN. Neuroscience 2016, 325, 165–174. [Google Scholar] [CrossRef] [PubMed]
- He, X.L.; Yan, N.; Chen, X.S.; Qi, Y.W.; Yan, Y.; Cai, Z. Hydrogen sulfide down-regulates BACE1 and PS1 via activating PI3K/Akt pathway in the brain of APP/PS1 transgenic mouse. Pharmacol. Rep. 2016, 68, 975–982. [Google Scholar] [CrossRef] [PubMed]
- Christia-Lotter, A.; Bartoli, C.; Piercecchi-Marti, M.D.; Demory, D.; Pelissier-Alicot, A.L.; Sanvoisin, A.; Leonetti, G. Fatal occupational inhalation of hydrogen sulfide. Forensic Sci. Int. 2007, 169, 206–209. [Google Scholar] [CrossRef] [PubMed]
- Maebashi, K.; Iwadate, K.; Sakai, K.; Takatsu, A.; Fukui, K.; Aoyagi, M.; Ochiai, E.; Nagai, T. Toxicological analysis of 17 autopsy cases of hydrogen sulfide poisoning resulting from the inhalation of intentionally generated hydrogen sulfide gas. Forensic Sci. Int. 2011, 207, 91–95. [Google Scholar] [CrossRef] [PubMed]
- Kurokawa, Y.; Sekiguchi, F.; Kubo, S.; Yamasaki, Y.; Matsuda, S.; Okamoto, Y.; Sekimoto, T.; Fukatsu, A.; Nishikawa, H.; Kume, T.; et al. Involvement of ERK in NMDA receptor-independent cortical neurotoxicity of hydrogen sulfide. Biochem. Biophys. Res. Commun. 2011, 414, 727–732. [Google Scholar] [CrossRef] [PubMed]
- Cheung, N.S.; Peng, Z.F.; Chen, M.J.; Moore, P.K.; Whiteman, M. Hydrogen sulfide induced neuronal death occurs via glutamate receptor and is associated with calpain activation and lysosomal rupture in mouse primary cortical neurons. Neuropharmacology 2007, 53, 505–514. [Google Scholar] [CrossRef] [PubMed]
- Spalloni, A.; Albo, F.; Ferrari, F.; Mercuri, N.; Bernardi, G.; Zona, C.; Longone, P. Cu/Zn-superoxide dismutase (GLY93→ALA) mutation alters AMPA receptor subunit expression and function and potentiates kainate-mediated toxicity in motor neurons in culture. Neurobiol. Dis. 2004, 2, 340–350. [Google Scholar] [CrossRef] [PubMed]
- Piras, C.; Soggiu, A.; Greco, V.; Martino, P.A.; Del Chierico, F.; Putignani, L.; Urbani, A.; Nally, J.E.; Bonizzi, L.; Roncada, P. Mechanisms of antibiotic resistance to enrofloxacin in uropathogenic Escherichia coli in dog. J. Proteom. 2015, 127, 365–376. [Google Scholar] [CrossRef] [PubMed]
- Piras, C.; Guo, Y.; Soggiu, A.; Chanrot, M.; Greco, V.; Urbani, A.; Charpigny, G.; Bonizzi, L.; Roncada, P.; Humblot, P. Changes in protein expression profiles in bovine endometrial epithelial cells exposed to E. coli LPS challenge. Mol. Biosyst. 2017, 13, 392–405. [Google Scholar] [CrossRef] [PubMed]
- Silva, J.C.; Gorenstein, M.V.; Li, G.Z.; Dissers, J.P.; Geromanos, S.J. Absolute quantification of proteins by LCMSE a virtue of parallel MS acquisition. Mol. Cell. Proteom. 2006, 5, 144–156. [Google Scholar] [CrossRef] [PubMed]
- Vissers, J.P.; Langridge, J.I.; Aerts, J.M. Analysis and quantification of diagnostic serum markers and protein signatures for Gaucher disease. Mol. Cell. Proteom. 2007, 6, 755–766. [Google Scholar] [CrossRef] [PubMed]
- Kimura, Y.; Kimura, H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J. 2004, 18, 1165–1167. [Google Scholar] [CrossRef] [PubMed]
- Nagai, Y.; Tsugane, M.; Oka, J.; Kimura, H. Hydrogen sulfide induces calcium waves in astrocytes. FASEB J. 2004, 18, 557–559. [Google Scholar] [CrossRef] [PubMed]
- Marutani, E.; Yamada, M.; Ida, T.; Tokuda, K.; Ikeda, K.; Kai, S.; Shirozu, K.; Hayashida, K.; Kosugi, S.; Hanaoka, K.; et al. Thiosulfate Mediates Cytoprotective Effects of Hydrogen Sulfide Against Neuronal Ischemia. J. Am. Heart Assoc. 2015, 4. [Google Scholar] [CrossRef]
- Cui, W.; Allen, N.D.; Skynner, M.; Gusterson, B.; Clark, A.J. Inducible ablation of astrocytes shows that these cells are required for neuronal survival in the adult brain. Glia 2001, 34, 272–282. [Google Scholar] [CrossRef] [PubMed]
- Ising, C.; Heneka, M.T. Functional and structural damage of neurons by innate immune mechanisms during neurodegeneration. Cell Death Dis. 2018, 25, 120. [Google Scholar] [CrossRef] [PubMed]
- Nagai, M.; Re, D.B.; Nagata, T.; Chalazonitis, A.; Jessell, T.M.; Wichterle, H.; Przedborski, S. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci. 2007, 10, 615–622. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fayaz, S.M.; Suvanish Kumar, V.S.; Rajanikant, G.K. Necroptosis: Who knew there were so many interesting ways to die? CNS Neurol. Disord. Drug Targets 2014, 13, 42–51. [Google Scholar] [CrossRef] [PubMed]
- Re, D.B.; Le Verche, V.; Yu, C.; Amoroso, M.W.; Politi, K.A.; Phani, S.; Ikiz, B.; Hoffmann, L.; Koolen, M.; Nagata, T.; et al. Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron 2014, 81, 1001–1008. [Google Scholar] [CrossRef] [PubMed]
- Ito, Y.; Ofengeim, D.; Najafov, A.; Das, S.; Saberi, S.; Li, Y.; Hitomi, J.; Zhu, H.; Chen, H.; Mayo, L.; et al. RIPK1 mediates axonal degeneration by promoting inflammation and necroptosis in ALS. Science 2016, 353, 603–608. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, F.; Sun, X.; Beech, W.; Teter, B.; Wu, S.; Sigel, J.; Vinters, H.V.; Frautschy, S.A.; Cole, G.M. Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and plaque-associated neurons and microglia in Alzheimer’s diseases. Am. J. Pathol. 1998, 152, 379–389. [Google Scholar] [PubMed]
- Suurmeijer, A.J.; van der Wijk, J.; van Veldhuisen, D.; Yang, F.; Cole, G.M. Fractin immunostaining for the detection of apoptotic cells and apoptotic bodies in Formalin-fixed and paraffin-embedded tissues. Lab. Investig. 1999, 79, 619–620. [Google Scholar] [PubMed]
- Li, P.; Nijhawan, D.; Budihardjo, I.; Srinivasula, S.M.; Ahmad, M.; Alnemri, E.S.; Wang, X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91, 479–489. [Google Scholar] [CrossRef]
- Zou, H.; Henzel, W.J.; Liu, X.; Lutschg, A.; Wang, X. 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. [Google Scholar] [CrossRef]
- Jurgensmeier, J.M.; Xie, Z.; Deveraux, Q.; Ellerby, L.; Bredesen, D.; Reed, J.C. Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. USA 1998, 95, 4997–5002. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lovell, J.F.; Billen, L.P.; Bindner, S.; Shamas-Din, A.; Fradin, C.; Leber, B.; Andrews, D.W. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 2008, 135, 1074–1084. [Google Scholar] [CrossRef] [PubMed]
- Shore, G.C.; Nguyen, M. Bcl-2 proteins and apoptosis: Choose your partner. Cell 2008, 35, 1004–1006. [Google Scholar] [CrossRef] [PubMed]
- Lakhani, S.A.; Masud, A.; Kuida, K.; Porter, G.A., Jr.; Booth, C.J.; Mehal, W.Z.; Inayat, I.; Flavell, R.A. Caspases 3 and 7: Key mediators of mitochondrial events of apoptosis. Science 2006, 311, 847–851. [Google Scholar] [CrossRef] [PubMed]
- Galluzzi, L.; Kepp, O.; Chan, F.K.; Kroemer, G. Necroptosis: Mechanisms and Relevance to Disease. Annu. Rev. Pathol. 2017, 12, 103–130. [Google Scholar] [CrossRef] [PubMed]
- Irrinki, K.M.; Mallilankaraman, K.; Thapa, R.J.; Chandramoorthy, H.C.; Smith, F.J.; Jog, N.R.; Gandhirajan, R.K.; Kelsen, S.G.; Houser, S.R.; May, M.J.; et al. Requirement of FADD, NEMO, and BAX/BAK for aberrant mitochondrial function in tumor necrosis factor alpha-induced necrosis. Mol. Cell. Biol. 2011, 18, 3745–3758. [Google Scholar] [CrossRef] [PubMed]
- Karch, J.; Kanisicak, O.; Brody, M.J.; Sargent, M.A.; Michael, D.M.; Molkentin, J.D. Necroptosis Interfaces with MOMP and the MPTP in Mediating Cell Death. PLoS ONE 2015, 10, e0130520. [Google Scholar] [CrossRef] [PubMed]
- Rohde, K.; Kleinesudeik, L.; Roesler, S.; Löwe, O.; Heidler, J.; Schröder, K.; Wittig, I.; Dröse, S.; Fulda, S.A. Bak-dependent mitochondrial amplification step contributes to Smac mimetic/glucocorticoid-induced necroptosis. Cell Death Differ. 2017, 24, 83–97. [Google Scholar] [CrossRef] [PubMed]
- Tait, S.W.; Oberst, A.; Quarato, G.; Milasta, S.; Haller, M.; Wang, R.; Karvela, M.; Ichim, G.; Yatim, N.; Albert, M.L.; et al. Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep. 2013, 5, 878–885. [Google Scholar] [CrossRef] [PubMed]
- Linkermann, A.; Bräsen, J.H.; Darding, M.; Jin, M.K.; Sanz, A.B.; Heller, J.O.; De Zen, F.; Weinlich, R.; Ortiz, A.; Walczak, H.; et al. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc. Natl. Acad. Sci. USA 2013, 110, 12024–12029. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johnson, J.A.; Johnson, D.A.; Kraft, A.D.; Calkins, M.J.; Jakel, R.J.; Vargas, M.R.; Chen, P.C. The Nrf2-ARE pathway: An indicator and modulator of oxidative stress in neurodegeneration. Ann. N. Y. Acad. Sci. 2008, 1147, 61–69. [Google Scholar] [CrossRef] [PubMed]
- Shih, A.Y.; Imbeault, S.; Barakauskas, V.; Erb, H.; Jiang, L.; Li, P.; Murphy, T.H. Induction of the Nrf2-driven antioxidant response confers neuroprotection during mitochondrial stress in vivo. J. Biol. Chem. 2005, 280, 22925–22936. [Google Scholar] [CrossRef] [PubMed]
- Hybertson, B.M.; Gao, B.; Bose, S.K.; McCord, J.M. Oxidative stress in health and disease: The therapeutic potential of Nrf2 activation. Mol. Asp. Med. 2011, 32, 234–246. [Google Scholar] [CrossRef] [PubMed]
- Calkins, M.J.; Jakel, R.J.; Johnson, D.A.; Chan, K.; Kan, Y.W.; Johnson, J.A. Protection from mitochondrial complex II inhibition in vitro and in vivo by Nrf2-mediated transcription. Proc. Natl. Acad. Sci. USA 2005, 102, 244–249. [Google Scholar] [CrossRef] [PubMed]
- Innamorato, N.G.; Jazwa, A.; Rojo, A.I.; García, C.; Fernández-Ruiz, J.; Grochot-Przeczek, A.; Stachurska, A.; Jozkowicz, A.; Dulak, J.; Cuadrado, A. Different susceptibility to the Parkinson’s toxin MPTP in mice lacking the redox master regulator Nrf2 or its target gene heme oxygenase-1. PLoS ONE 2010, 5, e11838. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vargas, M.R.; Johnson, D.A.; Sirkis, D.W.; Messing, A.; Johnson, J.A. Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J. Neurosci. 2008, 28, 13574–13581. [Google Scholar] [CrossRef] [PubMed]
- Vargas, M.R.; Burton, N.C.; Kutzke, J.; Gan, L.; Johnson, D.A.; Schäfer, M.; Werner, S.; Johnson, J.A. Absence of Nrf2 or its selective overexpression in neurons and muscle does not affect survival in ALS-linked mutant hSOD1 mouse models. PLoS ONE 2013, 8, e56625. [Google Scholar] [CrossRef]
- Shaw, P.J.; Ince, P.G.; Falkous, G.; Mantle, D. Oxidative damage to protein in sporadic motor neuron disease spinal cord. Ann. Neurol. 1995, 38, 691–695. [Google Scholar] [CrossRef] [PubMed]
- Smith, R.G.; Henry, Y.K.; Mattson, M.P.; Appel, S.H. Presence of 4-hydroxynonenal in cerebrospinal fluid of patients with sporadic amyotrophic lateral sclerosis. Ann. Neurol. 1998, 44, 696–699. [Google Scholar] [CrossRef] [PubMed]
- Shibata, N.; Nagai, R.; Miyata, S.; Jono, T.; Horiuchi, S.; Hirano, A.; Kato, S.; Sasaki, S.; Asayama, K.; Kobayashi, M. Nonoxidative protein glycation is implicated in familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Acta Neuropathol. 2000, 100, 275–284. [Google Scholar] [CrossRef] [PubMed]
- Shibata, N.; Nagai, R.; Uchida, K.; Horiuchi, S.; Yamada, S.; Hirano, A.; Kawaguchi, M.; Yamamoto, T.; Sasaki, S.; Kobayashi, M. Morphological evidence for lipid peroxidation and protein glycoxidation in spinal cords from sporadic amyotrophic lateral sclerosis patients. Brain Res. 2001, 917, 97–104. [Google Scholar] [CrossRef]
- Kraft, A.D.; Resch, J.M.; Johnson, D.A.; Johnson, J.A. Activation of the Nrf2-ARE pathway in muscle and spinal cord during ALS-like pathology in mice expressing mutant SOD1. Exp. Neurol. 2007, 207, 107–117. [Google Scholar] [CrossRef] [PubMed]
- Perkins, A.; Nelson, K.J.; Parsonage, D.; Poole, L.B.; Karplus, P.A. Peroxiredoxins: Guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem. Sci. 2015, 40, 435–445. [Google Scholar] [CrossRef] [PubMed]
- Knoops, B.; Argyropoulou, V.; Becker, S.; Ferté, L.; Kuznetsova, O. Multiple Roles of Peroxiredoxins in Inflammation. Mol. Cells 2016, 39, 60–64. [Google Scholar] [PubMed] [Green Version]
- Kato, M.; Kato, S.; Abe, Y.; Nishino, T.; Ohama, E.; Aoki, M.; Itoyama, Y. Histological recovery of the hepatocytes is based on the redox system upregulation in the animal models of mutant superoxide dismutase (SOD)1-linked amyotrophic lateral sclerosis. Histol. Histopathol. 2006, 21, 729–742. [Google Scholar] [PubMed]
- Wenger, R.H. Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J. 2002, 16, 1151–1162. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.L.; Jiang, B.H.; Rue, E.A.; Semenza, G.L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA 1995, 92, 5510–5514. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Sun, M.; Wang, L.; Jiao, B. HIFs, angiogenesis, and cancer. J. Cell. Biochem. 2013, 114, 967–974. [Google Scholar] [CrossRef] [PubMed]
- Semenza, G.L. Hypoxia pathway linked to kidney failure. Nat. Med. 2006, 12, 996–997. [Google Scholar] [CrossRef] [PubMed]
- Spagnuolo, R.D.; Recalcati, S.; Tacchini, L.; Cairo, G. Role of hypoxia-inducible factors in the dexrazoxane-mediated protection of cardiomyocytes from doxorubicin-induced toxicity. Br. J. Pharmacol. 2011, 163, 299–312. [Google Scholar] [CrossRef] [PubMed]
- Yee Koh, M.; Spivak-Kroizman, T.R.; Powis, G. HIF-1 regulation: Not so easy come, easy go. Trends Biochem. Sci. 2008, 33, 526–534. [Google Scholar] [CrossRef] [PubMed]
- Cuevasanta, E.; Möller, M.N.; Alvarez, B. Biological chemistry of hydrogen sulfide and persulfides. Arch. Biochem. Biophys. 2017, 617, 9–25. [Google Scholar] [CrossRef] [PubMed]
- Wu, B.; Teng, H.; Zhang, L.; Li, H.; Li, J.; Wang, L.; Li, H. Interaction of Hydrogen Sulfide with Oxygen Sensing under Hypoxia. Oxid. Med. Cell. Longev. 2015, 2015, 758678. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Pan, L.; Zhuo, Y.; Gong, Q.; Rose, P.; Zhu, Y. Hypoxia-inducible factor-1α is involved in the pro-angiogenic effect of hydrogen sulfide under hypoxic stress. Biol. Pharm. Bull. 2010, 33, 1550–1554. [Google Scholar] [CrossRef] [PubMed]
- Kai, S.; Tanaka, T.; Daijo, H.; Harada, H.; Kishimoto, S.; Suzuki, K.; Takabuchi, S.; Takenaga, K.; Fukuda, K.; Hirota, K. Hydrogen sulfide inhibits hypoxia- but not anoxia-induced hypoxia-inducible factor 1 activation in a von hippel-lindau- and mitochondria-dependent manner. Antioxid. Redox Signal. 2012, 16, 203–216. [Google Scholar] [CrossRef] [PubMed]
Canonical Pathway | p-Value |
PI3K/AKT Signaling | 1.54 × 10−12 |
Cell Cycle: G2/M DNA Damage Checkpoint Regulation | 3.60 ×10−11 |
Nrf-2-mediated Oxidative Stress Response | 4.30 × 10−11 |
Top Tox Lists | p-Value |
Nrf-2-mediated Oxidative Stress Response | 4.98 × 10−14 |
Oxidative Stress | 4.63 × 10−11 |
Hypoxia-Inducible Factor Signaling | 3.60 × 10−3 |
Top Diseases and Biofunctions | p-Value |
Free-Radical Scavenging | 2.89 × 10−4–2.50 × 10−8 |
Small-Molecule Biochemistry | 3.21 × 10−4–2.50 × 10−8 |
Cell Death and Survival | 7.12 ×10−4–3.22 × 10−8 |
Accession 1 | Description 2 | Score PLGS 3 | Highly Expressed 4 | NT:NaHS Ratio 5 | NT:NaHS Log(e) Ratio 6 | NT:NaHS Log(e) Std Dev 7 |
---|---|---|---|---|---|---|
Q9CQV8 | 14-3-3 protein beta/alpha | 2336.96 | 1.33 | 0.29 | 0.11 | |
P62259 | 14-3-3 protein epsilon | 992.11 | 1.03 | 0.03 | 0.19 | |
P61982 | 14-3-3 protein gamma | 832.06 | 1.43 | 0.36 | 0.12 | |
O70456 | 14-3-3 protein sigma | 684.53 | 1.03 | 0.03 | 0.24 | |
P68254 | 14-3-3 protein theta | 895.91 | 1.24 | 0.22 | 0.11 | |
P20029 | 78 kDa glucose-regulated protein | 635.95 | 1.12 | 0.11 | 0.09 | |
P60710 | Actin, cytoplasmic 1 | 339.07 | 0.94 | −0.06 | 0.02 | |
P07901 | Heat-shock protein HSP 90-alpha | 833.68 | 1.25 | 0.23 | 0.1 | |
P11499 | Heat-shock protein HSP 90-beta | 1344.62 | 1.15 | 0.14 | 0.07 | |
P35700 | Peroxiredoxin-1 | 3181.26 | NaHS | |||
Q61171 | Peroxiredoxin-2 | 898.73 | 0.9 | −0.1 | 0.08 | |
O08709 | Peroxiredoxin-6 | 566.13 | NaHS | 0.09 | ||
P08228 | Superoxide dismutase [Cu-Zn] | 572.41 | 0.9 | −0.06 | 0.03 | |
O54790 | Transcription factor MafG 1 | 363.28 | NaHS | |||
P20152 | Vimentin | 23,689.85 | 0.77 | −0.26 | 0.04 |
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Greco, V.; Spalloni, A.; Corasolla Carregari, V.; Pieroni, L.; Persichilli, S.; Mercuri, N.B.; Urbani, A.; Longone, P. Proteomics and Toxicity Analysis of Spinal-Cord Primary Cultures upon Hydrogen Sulfide Treatment. Antioxidants 2018, 7, 87. https://doi.org/10.3390/antiox7070087
Greco V, Spalloni A, Corasolla Carregari V, Pieroni L, Persichilli S, Mercuri NB, Urbani A, Longone P. Proteomics and Toxicity Analysis of Spinal-Cord Primary Cultures upon Hydrogen Sulfide Treatment. Antioxidants. 2018; 7(7):87. https://doi.org/10.3390/antiox7070087
Chicago/Turabian StyleGreco, Viviana, Alida Spalloni, Victor Corasolla Carregari, Luisa Pieroni, Silvia Persichilli, Nicola B. Mercuri, Andrea Urbani, and Patrizia Longone. 2018. "Proteomics and Toxicity Analysis of Spinal-Cord Primary Cultures upon Hydrogen Sulfide Treatment" Antioxidants 7, no. 7: 87. https://doi.org/10.3390/antiox7070087