The Tardigrade Damage Suppressor Protein Modulates Transcription Factor and DNA Repair Genes in Human Cells Treated with Hydroxyl Radicals and UV-C
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Cell Transfection
2.2. Evaluation of Dsup Transcript Presence by Endpoint and Real-Time Reverse Transcriptase-PCR
2.3. Cell Viability
2.4. Cyclobutane Pyrimidine Dimers (CPDs) Evaluation
2.5. Transcription Factor Evaluation
2.6. Gene Expression Analysis
2.7. Statistical Analysis
3. Results
3.1. Cell Survival under Stress Conditions
3.2. Transcription Factor Activation in Response to Stress Condition
3.3. Gene Expression in Response to Stress Conditions
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Hashimoto, T.; Horikawa, D.D.; Saito, Y.; Kuwahara, H.; Kozuka-Hata, H.; Shin-I, T.; Minakuchi, Y.; Ohishi, K.; Motoyama, A.; Aizu, T.; et al. Extremotolerant Tardigrade Genome and Improved Radiotolerance of Human Cultured Cells by Tardigrade-Unique Protein. Nat. Commun. 2016, 7, 12808. [Google Scholar] [CrossRef] [PubMed]
- Guidetti, R.; Rizzo, A.M.; Altiero, T.; Rebecchi, L. What Can We Learn from the Toughest Animals of the Earth? Water Bears (Tardigrades) as Multicellular Model Organisms in Order to Perform Scientific Preparations for Lunar Exploration. Planet. Space Sci. 2012, 74, 97–102. [Google Scholar] [CrossRef]
- Hengherr, S.; Worland, M.R.; Reuner, A.; Brümmer, F.; Schill, R.O. High-Temperature Tolerance in Anhydrobiotic Tardigrades Is Limited by Glass Transition. Physiol. Biochem. Zool. 2009, 82, 749–755. [Google Scholar] [CrossRef]
- Horikawa, D.D.; Kunieda, T.; Abe, W.; Watanabe, M.; Nakahara, Y.; Yukuhiro, F.; Sakashita, T.; Hamada, N.; Wada, S.; Funayama, T.; et al. Establishment of a Rearing System of the Extremotolerant Tardigrade Ramazzottius Varieornatus: A New Model Animal for Astrobiology. Astrobiology 2008, 8, 549–556. [Google Scholar] [CrossRef] [PubMed]
- Ono, F.; Saigusa, M.; Uozumi, T.; Matsushima, Y.; Ikeda, H.; Saini, N.L.; Yamashita, M. Effect of High Hydrostatic Pressure on to Life of the Tiny Animal Tardigrade. J. Phys. Chem. Solids 2008, 69, 2297–2300. [Google Scholar] [CrossRef]
- Ingemar Jönsson, K.; Harms-Ringdahl, M.; Torudd, J. Radiation Tolerance in the Eutardigrade Richtersius Coronifer. Int. J. Radiat. Biol. 2005, 81, 649–656. [Google Scholar] [CrossRef]
- Jönsson, K.I.; Rabbow, E.; Schill, R.O.; Harms-Ringdahl, M.; Rettberg, P. Tardigrades Survive Exposure to Space in Low Earth Orbit. Curr. Biol. 2008, 18, R729–R731. [Google Scholar] [CrossRef] [Green Version]
- Chavez, C.; Cruz-Becerra, G.; Fei, J.; Kassavetis, G.A.; Kadonaga, J.T. The Tardigrade Damage Suppressor Protein Binds to Nucleosomes and Protects DNA from Hydroxyl Radicals. eLife 2019, 8, e47682. [Google Scholar] [CrossRef]
- Dunker, A.; Lawson, J.D.; Brown, C.J.; Williams, R.M.; Romero, P.; Oh, J.S.; Oldfield, C.J.; Campen, A.M.; Ratliff, C.M.; Hipps, K.W.; et al. Intrinsically disordered protein. J. Mol. Graph. Model. 2001, 19, 26–59. [Google Scholar] [CrossRef] [Green Version]
- Kirke, J.; Jin, X.-L.; Zhang, X.-H. Expression of a Tardigrade Dsup Gene Enhances Genome Protection in Plants. Mol. Biotechnol. 2020, 62, 563–571. [Google Scholar] [CrossRef]
- Roy, S. Impact of UV Radiation on Genome Stability and Human Health. Adv. Exp. Med. Biol. 2017, 996, 207–219. [Google Scholar] [CrossRef]
- Berens, P.J.T.; Molinier, J. Formation and Recognition of UV-Induced DNA Damage within Genome Complexity. Int. J. Mol. Sci. 2020, 21, 6689. [Google Scholar] [CrossRef]
- Clancy, S. DNA Damage & Repair: Mechanisms for Maintaining DNA Integrity. Nat. Educ. 2008, 1, 103. [Google Scholar]
- Doksani, Y.; Bermejo, R.; Fiorani, S.; Haber, J.E.; Foiani, M. Replicon Dynamics, Dormant Origin Firing, and Terminal Fork Integrity after Double-Strand Break Formation. Cell 2009, 137, 247–258. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jazayeri, A.; Falck, J.; Lukas, C.; Bartek, J.; Smith, G.C.M.; Lukas, J.; Jackson, S.P. ATM- and Cell Cycle-Dependent Regulation of ATR in Response to DNA Double-Strand Breaks. Nat. Cell Biol. 2006, 8, 37–45. [Google Scholar] [CrossRef] [PubMed]
- Wagh, V.; Joshi, P.; Jariyal, H.; Chauhan, N. ATM and ATR Checkpoint Kinase Pathways: A Concise Review. Adv. Hum. Biol. 2020, 10, 51. [Google Scholar] [CrossRef]
- Roy, R.; Chun, J.; Powell, S.N. BRCA1 and BRCA2: Different Roles in a Common Pathway of Genome Protection. Nat. Rev. Cancer 2012, 12, 68–78. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nandi, A.; Yan, L.-J.; Jana, C.K.; Das, N. Role of Catalase in Oxidative Stress- and Age-Associated Degenerative Diseases. Oxidative Med. Cell. Longev. 2019, 2019, 9613090. [Google Scholar] [CrossRef] [Green Version]
- Fukai, T.; Ushio-Fukai, M. Superoxide Dismutases: Role in Redox Signaling, Vascular Function, and Diseases. Antioxid. Redox Signal. 2011, 15, 1583–1606. [Google Scholar] [CrossRef] [Green Version]
- Lynch, K.; Pergolizzi, R.G. In Vitro Method to quantify UV mediated DNA damage. J. Young Investig. 2010, 20, 2–9. [Google Scholar]
- Xiang, J.; Wan, C.; Guo, R.; Guo, D. Is Hydrogen Peroxide a Suitable Apoptosis Inducer for All Cell Types? Biomed. Res. Int. 2016, 2016, 7343965. [Google Scholar] [CrossRef] [Green Version]
- Li, X.; Zhan, J.; Hou, Y.; Hou, Y.; Chen, S.; Luo, D.; Luan, J.; Wang, L.; Lin, D. Coenzyme Q10 Regulation of Apoptosis and Oxidative Stress in H2O2 Induced BMSC Death by Modulating the Nrf-2/NQO-1 Signaling Pathway and Its Application in a Model of Spinal Cord Injury. Oxid Med. Cell Longev. 2019, 2019, 6493081. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Redza-Dutordoir, M.; Averill-Bates, D.A. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim. Biophys. Acta 2016, 1863, 2977–2992. [Google Scholar] [CrossRef] [PubMed]
- Marinho, H.S.; Real, C.; Cyrne, L.; Soares, H.; Antunes, F. Hydrogen Peroxide Sensing, Signaling and Regulation of Transcription Factors. Redox Biol. 2014, 2, 535–562. [Google Scholar] [CrossRef] [Green Version]
- Pregi, N.; Belluscio, L.M.; Berardino, B.G.; Castillo, D.S.; Cánepa, E.T. Oxidative Stress-Induced CREB Upregulation Promotes DNA Damage Repair Prior to Neuronal Cell Death Protection. Mol. Cell Biochem. 2017, 425, 9–24. [Google Scholar] [CrossRef]
- Shi, Y.; Venkataraman, S.L.; Dodson, G.E.; Mabb, A.M.; LeBlanc, S.; Tibbetts, R.S. Direct Regulation of CREB Transcriptional Activity by ATM in Response to Genotoxic Stress. Proc. Natl. Acad. Sci. USA 2004, 101, 5898–5903. [Google Scholar] [CrossRef] [Green Version]
- Rajabi, H.N.; Baluchamy, S.; Kolli, S.; Nag, A.; Srinivas, R.; Raychaudhuri, P.; Thimmapaya, B. Effects of Depletion of CREB-Binding Protein on c-Myc Regulation and Cell Cycle G1-S Transition. J. Biol. Chem. 2005, 280, 361–374. [Google Scholar] [CrossRef] [Green Version]
- Benassi, B.; Fanciulli, M.; Fiorentino, F.; Porrello, A.; Chiorino, G.; Loda, M.; Zupi, G.; Biroccio, A. C-Myc Phosphorylation Is Required for Cellular Response to Oxidative Stress. Mol. Cell 2006, 21, 509–519. [Google Scholar] [CrossRef]
- Ray Chaudhuri, A.; Nussenzweig, A. The Multifaceted Roles of PARP1 in DNA Repair and Chromatin Remodelling. Nat. Rev. Mol. Cell Biol. 2017, 18, 610–621. [Google Scholar] [CrossRef] [PubMed]
- Ali, A.A.E.; Timinszky, G.; Arribas-Bosacoma, R.; Kozlowski, M.; Hassa, P.O.; Hassler, M.; Ladurner, A.G.; Pearl, L.H.; Oliver, A.W. The Zinc-Finger Domains of PARP1 Cooperate to Recognize DNA Strand Breaks. Nat. Struct. Mol. Biol. 2012, 19, 685–692. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, M.; Yu, X. Function of BRCA1 in the DNA Damage Response Is Mediated by ADP-Ribosylation. Cancer Cell 2013, 23, 693–704. [Google Scholar] [CrossRef] [Green Version]
- Indran, I.R.; Hande, M.P.; Pervaiz, S. HTERT Overexpression Alleviates Intracellular ROS Production, Improves Mitochondrial Function, and Inhibits ROS-Mediated Apoptosis in Cancer Cells. Cancer Res. 2011, 71, 266–276. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiong, J.; Fan, S.; Meng, Q.; Schramm, L.; Wang, C.; Bouzahza, B.; Zhou, J.; Zafonte, B.; Goldberg, I.D.; Haddad, B.R.; et al. BRCA1 Inhibition of Telomerase Activity in Cultured Cells. Mol. Cell. Biol. 2003, 23, 8668–8690. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dell’Orco, M.; Milani, P.; Arrigoni, L.; Pansarasa, O.; Sardone, V.; Maffioli, E.; Polveraccio, F.; Bordoni, M.; Diamanti, L.; Ceroni, M.; et al. Hydrogen Peroxide-Mediated Induction of SOD1 Gene Transcription Is Independent from Nrf2 in a Cellular Model of Neurodegeneration. Biochim. Biophys. Acta (BBA)—Gene Regul. Mech. 2016, 1859, 315–323. [Google Scholar] [CrossRef] [PubMed]
- Eleutherio, E.C.A.; Silva Magalhães, R.S.; de Araújo Brasil, A.; Monteiro Neto, J.R.; de Holanda Paranhos, L. SOD1, More than Just an Antioxidant. Arch. Biochem. Biophys. 2021, 697, 108701. [Google Scholar] [CrossRef] [PubMed]
- Glorieux, C.; Calderon, P.B. Catalase, a Remarkable Enzyme: Targeting the Oldest Antioxidant Enzyme to Find a New Cancer Treatment Approach. Biol. Chem. 2017, 398, 1095–1108. [Google Scholar] [CrossRef] [Green Version]
- Marais, T.L.D.; Kluz, T.; Xu, D.; Zhang, X.; Gesumaria, L.; Matsui, M.S.; Costa, M.; Sun, H. Transcription Factors and Stress Response Gene Alterations in Human Keratinocytes Following Solar Simulated Ultra Violet Radiation. Sci. Rep. 2017, 7, 13622. [Google Scholar] [CrossRef]
- Ismail, A.; Yusuf, N. Type I Interferons: Key Players in Normal Skin and Select Cutaneous Malignancies. Dermatol. Res. Pract. 2014, 2014, 847545. [Google Scholar] [CrossRef]
- Aragane, Y.; Kulms, D.; Luger, T.A.; Schwarz, T. Down-Regulation of Interferon -Activated STAT1 by UV Light. Proc. Natl. Acad. Sci. USA 1997, 94, 11490–11495. [Google Scholar] [CrossRef] [Green Version]
- Shaulian, E.; Schreiber, M.; Piu, F.; Beeche, M.; Wagner, E.F.; Karin, M. The Mammalian UV Response: C-Jun Induction Is Required for Exit from P53-Imposed Growth Arrest. Cell 2000, 103, 897–907. [Google Scholar] [CrossRef] [Green Version]
- Herold, S.; Wanzel, M.; Beuger, V.; Frohme, C.; Beul, D.; Hillukkala, T.; Syvaoja, J.; Saluz, H.-P.; Haenel, F.; Eilers, M. Negative Regulation of the Mammalian UV Response by Myc through Association with Miz-1. Mol. Cell 2002, 10, 509–521. [Google Scholar] [CrossRef]
- Pathania, S.; Nguyen, J.; Hill, S.J.; Scully, R.; Adelmant, G.O.; Marto, J.A.; Feunteun, J.; Livingston, D.M. BRCA1 Is Required for Postreplication Repair after UV-Induced DNA Damage. Mol. Cell 2011, 44, 235–251. [Google Scholar] [CrossRef] [Green Version]
- Pavey, S.; Pinder, A.; Fernando, W.; D’Arcy, N.; Matigian, N.; Skalamera, D.; Lê Cao, K.; Loo-Oey, D.; Hill, M.M.; Stark, M.; et al. Multiple Interaction Nodes Define the Postreplication Repair Response to UV-induced DNA Damage That Is Defective in Melanomas and Correlated with UV Signature Mutation Load. Mol. Oncol. 2020, 14, 22–41. [Google Scholar] [CrossRef] [PubMed]
- Lefkofsky, H.B.; Veloso, A.; Ljungman, M. Transcriptional and Post-Transcriptional Regulation of Nucleotide Excision Repair Genes in Human Cells. Mutat. Res. Fundam. Mol. Mech. Mutagen. 2015, 776, 9–15. [Google Scholar] [CrossRef] [Green Version]
- Ohashi, E.; Takeishi, Y.; Ueda, S.; Tsurimoto, T. Interaction between Rad9–Hus1–Rad1 and TopBP1 Activates ATR–ATRIP and Promotes TopBP1 Recruitment to Sites of UV-Damage. DNA Repair 2014, 21, 1–11. [Google Scholar] [CrossRef]
- Stepanenko, A.A.; Heng, H.H. Transient and stable vector transfection: Pitfalls, off-target effects, artifacts. Mutat. Res. Rev. Mutat. Res. 2017, 773, 91–103. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 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 (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ricci, C.; Riolo, G.; Marzocchi, C.; Brunetti, J.; Pini, A.; Cantara, S. The Tardigrade Damage Suppressor Protein Modulates Transcription Factor and DNA Repair Genes in Human Cells Treated with Hydroxyl Radicals and UV-C. Biology 2021, 10, 970. https://doi.org/10.3390/biology10100970
Ricci C, Riolo G, Marzocchi C, Brunetti J, Pini A, Cantara S. The Tardigrade Damage Suppressor Protein Modulates Transcription Factor and DNA Repair Genes in Human Cells Treated with Hydroxyl Radicals and UV-C. Biology. 2021; 10(10):970. https://doi.org/10.3390/biology10100970
Chicago/Turabian StyleRicci, Claudia, Giulia Riolo, Carlotta Marzocchi, Jlenia Brunetti, Alessandro Pini, and Silvia Cantara. 2021. "The Tardigrade Damage Suppressor Protein Modulates Transcription Factor and DNA Repair Genes in Human Cells Treated with Hydroxyl Radicals and UV-C" Biology 10, no. 10: 970. https://doi.org/10.3390/biology10100970