Nitrosative Stress in Astronaut Skeletal Muscle in Spaceflight
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Participants
2.2. Muscle Biopsy
2.3. Immunohistochemistry
2.4. Proteomics with Nitro-DIGE
2.4.1. Protein Extraction
2.4.2. Identification of S-Nitrosated Proteins by 2-D CyDye-Maleimide DIGE (Nitro-DIGE)
2.4.3. Image Acquisition
2.4.4. Protein Identification
2.4.5. Immunoblotting
2.4.6. RNA Extraction and qPCR
2.5. Statistics
3. Results
3.1. Quantitative PCR (qPCR) Analyses of NOS1 Transcripts in Astronaut Soleus Muscle Samples
3.2. NOS1 Immunolocalization in Astronaut Soleus Muscle Cryosections
3.3. Nitro-DIGE Analysis of Astronaut Soleus Biosamples
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
ADH5 | alcohol dehydrogenase 5 |
ALDOA | Fructose-bisphosphate aldolase A |
ACO2 | aconitate hydratase proteoforms (a, b or c) |
ARED | advanced resistive exercise device (on ISS) |
BDC | Baseline data collection (on the ground, pre/postflight) |
CA3 | carbonic anhydrase 3 |
CEVIS | cycle ergometer with vibration isolation and stabilization (on ISS) |
CKM | creatine kinase M-type |
CM | countermeasure (physical exercise intervention) |
DLR | Deutsches Zentrum für Luft- und Raumfahrt (German Aerospace Agency) |
EAC | European Astronaut Center (Cologne) |
ESA | European Space Agency |
FDR | False discovery rate (statistics) |
G | gravity vector (1G Earth/µG Space) |
GATD3 | glutamine amidotransferase-like class 1 domain-containing protein 3 |
GOT1 | cytoplasmic aspartate aminotransferase |
GOT2 | mitochondrial aspartate aminotransferase |
GSNOR | S-nitrosoglutathione reductase |
IDH2 | isocitrate dehydrogenase [NADP] |
IPG | immobilized pH gradient |
ISS | International Space Station |
JAXA | Japanese Space Agency |
LDM | long-duration mission (>180 days) |
MDS | Mice drawer system (habitat module on ISS) |
MedOPs | Medical operational team |
MDH1 | cytoplasmic malate dehydrogenase |
MYL3 | myosin light chain 3 |
M.O.M. | mouse-on-mouse (immunocytochemical blocking agent) |
NASA | National Aeronautics and Space Administration |
Nitro-DIGE | S-Nitrosated proteins identified by 2-D CyDye-Maleimide |
NO | nitric oxide |
NOS | NO synthase |
O.D. | optical density |
OGDH | 2-oxoglutarate dehydrogenase complex component E2 |
R+0/1 | return day (landing day on Earth) |
ROS | reactive oxidative species |
RNS | reactive nitrogen species |
RONS | reactive oxidative and nitrosative species |
SDHA | succinate dehydrogenase [ubiquinone] flavoprotein subunit |
SDM | short-duration mission (11 days spaceflight) |
T2 | treadmill on ISS |
TF | serotransferrin |
TNNT1 | slow skeletal muscle troponin T |
TXNRD1 | thioredoxin reductase 1 |
UQCRC1 | cytochrome b-c1 complex subunit 1 |
USOS | United States orbital system |
µG | microgravity |
References
- Juhl, O.J.; Buettmann, E.G.; Friedman, M.A.; DeNapoli, R.C.; Hoppock, G.A.; Donahue, H.J. Update on the effects of microgravity on the musculoskeletal system. NPJ Microgravity 2021, 7, 28. [Google Scholar] [CrossRef] [PubMed]
- Lang, T.; Van Loon, J.; Bloomfield, S.; Vico, L.; Chopard, A.; Rittweger, J.; Kyparos, A.; Blottner, D.; Vuori, I.; Gerzer, R.; et al. Towards human exploration of space: The THESEUS review series on muscle and bone research priorities. NPJ Microgravity 2017, 3, 8. [Google Scholar] [CrossRef] [PubMed]
- Bergouignan, A.; Stein, T.P.; Habold, C.; Coxam, V.; O’Gorman, D.; Blanc, S. Towards human exploration of space: The THESEUS review series on nutrition and metabolism research priorities. NPJ Microgravity 2016, 2, 16029. [Google Scholar] [CrossRef] [PubMed]
- Ackermann, M.; van den Bogert, A.J. Predictive simulation of gait at low gravity reveals skipping as the preferred locomotion strategy. J. Biomech. 2012, 45, 1293–1298. [Google Scholar] [CrossRef] [PubMed]
- Antonsen, E.L.; Myers, J.G.; Boley, L.; Arellano, J.; Kerstman, E.; Kadwa, B.; Buckland, D.M.; Van Baalen, M. Estimating medical risk in human spaceflight. NPJ Microgravity 2022, 8, 8. [Google Scholar] [CrossRef] [PubMed]
- Scott, J.P.R.; Weber, T.; Green, D.A. Introduction to the Frontiers Research Topic: Optimization of Exercise Countermeasures for Human Space Flight—Lessons from Terrestrial Physiology and Operational Considerations. Front. Physiol. 2019, 10, 173. [Google Scholar] [CrossRef]
- Indo, H.P.; Majima, H.J.; Terada, M.; Suenaga, S.; Tomita, K.; Yamada, S.; Higashibata, A.; Ishioka, N.; Kanekura, T.; Nonaka, I.; et al. Changes in mitochondrial homeostasis and redox status in astronauts following long stays in space. Sci. Rep. 2016, 6, 39015. [Google Scholar] [CrossRef]
- Powers, S.K.; Goldstein, E.; Schrager, M.; Ji, L.L. Exercise Training and Skeletal Muscle Antioxidant Enzymes: An Update. Antioxidants 2022, 12, 39. [Google Scholar] [CrossRef] [PubMed]
- Yoon, S.; Eom, G.H.; Kang, G. Nitrosative Stress and Human Disease: Therapeutic Potential of Denitrosylation. Int. J. Mol. Sci. 2021, 22, 9794. [Google Scholar] [CrossRef]
- Yfanti, C.; Nielsen, A.R.; Akerstrom, T.; Nielsen, S.; Rose, A.J.; Richter, E.A.; Lykkesfeldt, J.; Fischer, C.P.; Pedersen, B.K. Effect of antioxidant supplementation on insulin sensitivity in response to endurance exercise training. Am. J. Physiol. Endocrinol. Metab. 2011, 300, E761–E770. [Google Scholar] [CrossRef]
- Salanova, M.; Schiffl, G.; Gutsmann, M.; Felsenberg, D.; Furlan, S.; Volpe, P.; Clarke, A.; Blottner, D. Nitrosative stress in human skeletal muscle attenuated by exercise countermeasure after chronic disuse. Redox Biol. 2013, 1, 514–526. [Google Scholar] [CrossRef] [PubMed]
- Arc-Chagnaud, C.; Py, G.; Fovet, T.; Roumanille, R.; Demangel, R.; Pagano, A.F.; Delobel, P.; Blanc, S.; Jasmin, B.J.; Blottner, D.; et al. Evaluation of an Antioxidant and Anti-inflammatory Cocktail Against Human Hypoactivity-Induced Skeletal Muscle Deconditioning. Front. Physiol. 2020, 11, 71. [Google Scholar] [CrossRef] [PubMed]
- Balon, T.W.; Yerneni, K.K. Redox regulation of skeletal muscle glucose transport. Med. Sci. Sports Exerc. 2001, 33, 382–385. [Google Scholar] [CrossRef]
- Nemes, R.; Koltai, E.; Taylor, A.W.; Suzuki, K.; Gyori, F.; Radak, Z. Reactive Oxygen and Nitrogen Species Regulate Key Metabolic, Anabolic, and Catabolic Pathways in Skeletal Muscle. Antioxidants 2018, 7, 85. [Google Scholar] [CrossRef] [PubMed]
- Powers, S.K.; Kavazis, A.N.; McClung, J.M. Oxidative stress and disuse muscle atrophy. J. Appl. Physiol. 2007, 102, 2389–2397. [Google Scholar] [CrossRef] [PubMed]
- Leitner, L.M.; Wilson, R.J.; Yan, Z.; Godecke, A. Reactive Oxygen Species/Nitric Oxide Mediated Inter-Organ Communication in Skeletal Muscle Wasting Diseases. Antioxid. Redox Signal. 2017, 26, 700–717. [Google Scholar] [CrossRef] [PubMed]
- Palomero, J.; Jackson, M.J. Redox regulation in skeletal muscle during contractile activity and aging. J. Anim. Sci. 2010, 88, 1307–1313. [Google Scholar] [CrossRef] [PubMed]
- Bellinger, A.M.; Reiken, S.; Carlson, C.; Mongillo, M.; Liu, X.; Rothman, L.; Matecki, S.; Lacampagne, A.; Marks, A.R. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat. Med. 2009, 15, 325–330. [Google Scholar] [CrossRef] [PubMed]
- Salanova, M.; Schiffl, G.; Rittweger, J.; Felsenberg, D.; Blottner, D. Ryanodine receptor type-1 (RyR1) expression and protein S-nitrosylation pattern in human soleus myofibres following bed rest and exercise countermeasure. Histochem. Cell. Biol. 2008, 130, 105–118. [Google Scholar] [CrossRef] [PubMed]
- Bredt, D.S.; Snyder, S.H. Nitric oxide: A physiologic messenger molecule. Annu. Rev. Biochem. 1994, 63, 175–195. [Google Scholar] [CrossRef]
- Kobzik, L.; Reid, M.B.; Bredt, D.S.; Stamler, J.S. Nitric oxide in skeletal muscle. Nature 1994, 372, 546–548. [Google Scholar] [CrossRef] [PubMed]
- Jones, A.M.; Thompson, C.; Wylie, L.J.; Vanhatalo, A. Dietary Nitrate and Physical Performance. Annu. Rev. Nutr. 2018, 38, 303–328. [Google Scholar] [CrossRef] [PubMed]
- Aguiar, A.F.; Vechetti-Junior, I.J.; Souza, R.W.; Piedade, W.P.; Pacagnelli, F.L.; Leopoldo, A.S.; Casonatto, J.; Dal-Pai-Silva, M. Nitric oxide synthase inhibition impairs muscle regrowth following immobilization. Nitric Oxide 2017, 69, 22–27. [Google Scholar] [CrossRef]
- Christova, T.; Grozdanovic, Z.; Gossrau, R. Nitric oxide synthase (NOS) I during postnatal development in rat and mouse skeletal muscle. Acta Histochem. 1997, 99, 311–324. [Google Scholar] [CrossRef]
- Lee, K.H.; Baek, M.Y.; Moon, K.Y.; Song, W.K.; Chung, C.H.; Ha, D.B.; Kang, M.S. Nitric oxide as a messenger molecule for myoblast fusion. J. Biol. Chem. 1994, 269, 14371–14374. [Google Scholar] [CrossRef]
- Tidball, J.G.; Lavergne, E.; Lau, K.S.; Spencer, M.J.; Stull, J.T.; Wehling, M. Mechanical loading regulates NOS expression and activity in developing and adult skeletal muscle. Am. J. Physiol. 1998, 275, C260–C266. [Google Scholar] [CrossRef]
- Godfrey, E.W.; Schwarte, R.C. The role of nitric oxide signaling in the formation of the neuromuscular junction. J. Neurocytol. 2003, 32, 591–602. [Google Scholar] [CrossRef]
- Kasikcioglu, E.; Dinler, M.; Berker, E. Reduced tolerance of exercise in fibromyalgia may be a consequence of impaired microcirculation initiated by deficient action of nitric oxide. Med. Hypotheses 2006, 66, 950–952. [Google Scholar] [CrossRef]
- Vaughn, M.W.; Kuo, L.; Liao, J.C. Effective diffusion distance of nitric oxide in the microcirculation. Am. J. Physiol. 1998, 274, H1705–H1714. [Google Scholar] [CrossRef]
- Filippin, L.I.; Cuevas, M.J.; Lima, E.; Marroni, N.P.; Gonzalez-Gallego, J.; Xavier, R.M. The role of nitric oxide during healing of trauma to the skeletal muscle. Inflamm. Res. 2011, 60, 347–356. [Google Scholar] [CrossRef]
- Anderson, J.E. A role for nitric oxide in muscle repair: Nitric oxide-mediated activation of muscle satellite cells. Mol. Biol. Cell. 2000, 11, 1859–1874. [Google Scholar] [CrossRef] [PubMed]
- Buckwalter, J.B.; Curtis, V.C.; Valic, Z.; Ruble, S.B.; Clifford, P.S. Endogenous vascular remodeling in ischemic skeletal muscle: A role for nitric oxide. J. Appl. Physiol. 2003, 94, 935–940. [Google Scholar] [CrossRef]
- Maxwell, A.J.; Schauble, E.; Bernstein, D.; Cooke, J.P. Limb blood flow during exercise is dependent on nitric oxide. Circulation 1998, 98, 369–374. [Google Scholar] [CrossRef]
- Maddali, S.; Rodeo, S.A.; Barnes, R.; Warren, R.F.; Murrell, G.A. Postexercise increase in nitric oxide in football players with muscle cramps. Am. J. Sports Med. 1998, 26, 820–824. [Google Scholar] [CrossRef] [PubMed]
- Swash, M. Nitric oxide and muscle weakness. Neurology 2011, 76, 940–941. [Google Scholar] [CrossRef]
- Sandona, D.; Desaphy, J.F.; Camerino, G.M.; Bianchini, E.; Ciciliot, S.; Danieli-Betto, D.; Dobrowolny, G.; Furlan, S.; Germinario, E.; Goto, K.; et al. Adaptation of mouse skeletal muscle to long-term microgravity in the MDS mission. PLoS ONE 2012, 7, e33232. [Google Scholar] [CrossRef] [PubMed]
- Rudnick, J.; Puttmann, B.; Tesch, P.A.; Alkner, B.; Schoser, B.G.; Salanova, M.; Kirsch, K.; Gunga, H.C.; Schiffl, G.; Luck, G.; et al. Differential expression of nitric oxide synthases (NOS 1-3) in human skeletal muscle following exercise countermeasure during 12 weeks of bed rest. FASEB J. 2004, 18, 1228–1230. [Google Scholar] [CrossRef]
- Blottner, D.; Moriggi, M.; Trautmann, G.; Hastermann, M.; Capitanio, D.; Torretta, E.; Block, K.; Rittweger, J.; Limper, U.; Gelfi, C.; et al. Space Omics and Tissue Response in Astronaut Skeletal Muscle after Short and Long Duration Missions. Int. J. Mol. Sci. 2023, 24, 4095. [Google Scholar] [CrossRef]
- Jaffrey, S.R.; Snyder, S.H. The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE 2001, 86, pl1. [Google Scholar] [CrossRef]
- Montagna, C.; Rizza, S.; Cirotti, C.; Maiani, E.; Muscaritoli, M.; Musaro, A.; Carri, M.T.; Ferraro, E.; Cecconi, F.; Filomeni, G. nNOS/GSNOR interaction contributes to skeletal muscle differentiation and homeostasis. Cell Death Dis. 2019, 10, 354. [Google Scholar] [CrossRef]
- Blottner, D.; Capitanio, D.; Trautmann, G.; Furlan, S.; Gambara, G.; Moriggi, M.; Block, K.; Barbacini, P.; Torretta, E.; Py, G.; et al. Nitrosative Redox Homeostasis and Antioxidant Response Defense in Disused Vastus lateralis Muscle in Long-Term Bedrest (Toulouse Cocktail Study). Antioxidants 2021, 10, 378. [Google Scholar] [CrossRef]
- Goodwin, T.J.; Christofidou-Solomidou, M. Oxidative Stress and Space Biology: An Organ-Based Approach. Int. J. Mol. Sci. 2018, 19, 959. [Google Scholar] [CrossRef]
- Berrios, D.C.; Galazka, J.; Grigorev, K.; Gebre, S.; Costes, S.V. NASA GeneLab: Interfaces for the exploration of space omics data. Nucleic Acids Res. 2021, 49, D1515–D1522. [Google Scholar] [CrossRef]
- Cope, H.; Willis, C.R.G.; MacKay, M.J.; Rutter, L.A.; Toh, L.S.; Williams, P.M.; Herranz, R.; Borg, J.; Bezdan, D.; Giacomello, S.; et al. Routine omics collection is a golden opportunity for European human research in space and analog environments. Patterns 2022, 3, 100550. [Google Scholar] [CrossRef] [PubMed]
- Rutter, L.; Barker, R.; Bezdan, D.; Cope, H.; Costes, S.V.; Degoricija, L.; Fisch, K.M.; Gabitto, M.I.; Gebre, S.; Giacomello, S.; et al. A New Era for Space Life Science: International Standards for Space Omics Processing. Patterns 2020, 1, 100148. [Google Scholar] [CrossRef]
- Schmidt, M.A.; Goodwin, T.J. Personalized medicine in human space flight: Using Omics based analyses to develop individualized countermeasures that enhance astronaut safety and performance. Metabolomics 2013, 9, 1134–1156. [Google Scholar] [CrossRef]
- Afshinnekoo, E.; Scott, R.T.; MacKay, M.J.; Pariset, E.; Cekanaviciute, E.; Barker, R.; Gilroy, S.; Hassane, D.; Smith, S.M.; Zwart, S.R.; et al. Fundamental Biological Features of Spaceflight: Advancing the Field to Enable Deep-Space Exploration. Cell 2020, 183, 1162–1184. [Google Scholar] [CrossRef]
- Schmidt, M.A.; Meydan, C.; Schmidt, C.M.; Afshinnekoo, E.; Mason, C.E. The NASA Twins Study: The Effect of One Year in Space on Long-Chain Fatty Acid Desaturases and Elongases. Lifestyle Genom. 2020, 13, 107–121. [Google Scholar] [CrossRef]
- Lechado, I.T.A.; Vitadello, M.; Traini, L.; Namuduri, A.V.; Gastaldello, S.; Gorza, L. Sarcolemmal loss of active nNOS (Nos1) is an oxidative stress-dependent, early event driving disuse atrophy. J. Pathol. 2018, 246, 433–446. [Google Scholar] [CrossRef]
- Balke, J.E.; Zhang, L.; Percival, J.M. Neuronal nitric oxide synthase (nNOS) splice variant function: Insights into nitric oxide signaling from skeletal muscle. Nitric Oxide 2019, 82, 35–47. [Google Scholar] [CrossRef]
- Loehr, J.A.; Guilliams, M.E.; Petersen, N.; Hirsch, N.; Kawashima, S.; Ohshima, H. Physical Training for Long-Duration Spaceflight. Aerosp. Med. Hum. Perform. 2015, 86, A14–A23. [Google Scholar] [CrossRef]
- Petersen, N.; Jaekel, P.; Rosenberger, A.; Weber, T.; Scott, J.; Castrucci, F.; Lambrecht, G.; Ploutz-Snyder, L.; Damann, V.; Kozlovskaya, I.; et al. Exercise in space: The European Space Agency approach to in-flight exercise countermeasures for long-duration missions on ISS. Extrem Physiol. Med. 2016, 5, 9. [Google Scholar] [CrossRef]
- Li, J.; Cao, F.; Yin, H.L.; Huang, Z.J.; Lin, Z.T.; Mao, N.; Sun, B.; Wang, G. Ferroptosis: Past, present and future. Cell Death Dis. 2020, 11, 88. [Google Scholar] [CrossRef]
- Khiati, S.; Bonneau, D.; Lenaers, G. Are Your Mitochondria Ready for a Space Odyssey? Trends Endocrinol. Metab. 2021, 32, 193–195. [Google Scholar] [CrossRef]
- Figueiredo-Freitas, C.; Dulce, R.A.; Foster, M.W.; Liang, J.; Yamashita, A.M.; Lima-Rosa, F.L.; Thompson, J.W.; Moseley, M.A.; Hare, J.M.; Nogueira, L.; et al. S-Nitrosylation of Sarcomeric Proteins Depresses Myofilament Ca2+ Sensitivity in Intact Cardiomyocytes. Antioxid. Redox Signal. 2015, 23, 1017–1034. [Google Scholar] [CrossRef]
- Horenberg, A.L.; Houghton, A.M.; Pandey, S.; Seshadri, V.; Guilford, W.H. S-nitrosylation of cytoskeletal proteins. Cytoskeleton 2019, 76, 243–253. [Google Scholar] [CrossRef]
- Dowling, P.; Gargan, S.; Swandulla, D.; Ohlendieck, K. Fiber-Type Shifting in Sarcopenia of Old Age: Proteomic Profiling of the Contractile Apparatus of Skeletal Muscles. Int. J. Mol. Sci. 2023, 24, 2415. [Google Scholar] [CrossRef]
- Widrick, J.J.; Knuth, S.T.; Norenberg, K.M.; Romatowski, J.G.; Bain, J.L.; Riley, D.A.; Karhanek, M.; Trappe, S.W.; Trappe, T.A.; Costill, D.L.; et al. Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J. Physiol. 1999, 516 (Pt 3), 915–930. [Google Scholar] [CrossRef]
- O’Connell, K.; Gannon, J.; Doran, P.; Ohlendieck, K. Proteomic profiling reveals a severely perturbed protein expression pattern in aged skeletal muscle. Int. J. Mol. Med. 2007, 20, 145–153. [Google Scholar] [CrossRef]
- Jiang, L.; Wang, M.; Lin, S.; Jian, R.; Li, X.; Chan, J.; Dong, G.; Fang, H.; Robinson, A.E.; Consortium, G.T.; et al. A Quantitative Proteome Map of the Human Body. Cell 2020, 183, 269–283.e19. [Google Scholar] [CrossRef]
- Dowling, P.; Gargan, S.; Zweyer, M.; Sabir, H.; Swandulla, D.; Ohlendieck, K. Proteomic profiling of carbonic anhydrase CA3 in skeletal muscle. Expert Rev. Proteom. 2021, 18, 1073–1086. [Google Scholar] [CrossRef]
- Staunton, L.; Zweyer, M.; Swandulla, D.; Ohlendieck, K. Mass spectrometry-based proteomic analysis of middle-aged vs. aged vastus lateralis reveals increased levels of carbonic anhydrase isoform 3 in senescent human skeletal muscle. Int. J. Mol. Med. 2012, 30, 723–733. [Google Scholar] [CrossRef]
- Montagna, C.; Di Giacomo, G.; Rizza, S.; Cardaci, S.; Ferraro, E.; Grumati, P.; De Zio, D.; Maiani, E.; Muscoli, C.; Lauro, F.; et al. S-nitrosoglutathione reductase deficiency-induced S-nitrosylation results in neuromuscular dysfunction. Antioxid. Redox Signal. 2014, 21, 570–587. [Google Scholar] [CrossRef]
- Cebula, M.; Schmidt, E.E.; Arner, E.S. TrxR1 as a potent regulator of the Nrf2-Keap1 response system. Antioxid. Redox Signal. 2015, 23, 823–853. [Google Scholar] [CrossRef]
- Maejima, Y.; Kuroda, J.; Matsushima, S.; Ago, T.; Sadoshima, J. Regulation of myocardial growth and death by NADPH oxidase. J. Mol. Cell. Cardiol. 2011, 50, 408–416. [Google Scholar] [CrossRef]
- Sakellariou, G.K.; Vasilaki, A.; Palomero, J.; Kayani, A.; Zibrik, L.; McArdle, A.; Jackson, M.J. Studies of mitochondrial and nonmitochondrial sources implicate nicotinamide adenine dinucleotide phosphate oxidase(s) in the increased skeletal muscle superoxide generation that occurs during contractile activity. Antioxid. Redox Signal. 2013, 18, 603–621. [Google Scholar] [CrossRef]
- Powers, S.K.; Wiggs, M.P.; Duarte, J.A.; Zergeroglu, A.M.; Demirel, H.A. Mitochondrial signaling contributes to disuse muscle atrophy. Am. J. Physiol. Endocrinol. Metab. 2012, 303, E31–E39. [Google Scholar] [CrossRef]
- Boardman, N.T.; Trani, G.; Scalabrin, M.; Romanello, V.; Wust, R.C.I. Intracellular to Interorgan Mitochondrial Communication in Striated Muscle in Health and Disease. Endocr. Rev. 2023, 44, 668–692. [Google Scholar] [CrossRef]
- Da Silveira, W.A.; Fazelinia, H.; Rosenthal, S.B.; Laiakis, E.C.; Kim, M.S.; Meydan, C.; Kidane, Y.; Rathi, K.S.; Smith, S.M.; Stear, B.; et al. Comprehensive Multi-omics Analysis Reveals Mitochondrial Stress as a Central Biological Hub for Spaceflight Impact. Cell 2020, 183, 1185–1201.e20. [Google Scholar] [CrossRef]
- Larsen, F.J.; Schiffer, T.A.; Ortenblad, N.; Zinner, C.; Morales-Alamo, D.; Willis, S.J.; Calbet, J.A.; Holmberg, H.C.; Boushel, R. High-intensity sprint training inhibits mitochondrial respiration through aconitase inactivation. FASEB J. 2016, 30, 417–427. [Google Scholar] [CrossRef]
- Lushchak, O.V.; Piroddi, M.; Galli, F.; Lushchak, V.I. Aconitase post-translational modification as a key in linkage between Krebs cycle, iron homeostasis, redox signaling, and metabolism of reactive oxygen species. Redox Rep. 2014, 19, 8–15. [Google Scholar] [CrossRef]
- Andersson, U.; Leighton, B.; Young, M.E.; Blomstrand, E.; Newsholme, E.A. Inactivation of aconitase and oxoglutarate dehydrogenase in skeletal muscle in vitro by superoxide anions and/or nitric oxide. Biochem. Biophys. Res. Commun. 1998, 249, 512–516. [Google Scholar] [CrossRef]
- Smith, A.J.; Advani, J.; Brock, D.C.; Nellissery, J.; Gumerson, J.; Dong, L.; Aravind, L.; Kennedy, B.; Swaroop, A. GATD3A, a mitochondrial deglycase with evolutionary origins from gammaproteobacteria, restricts the formation of advanced glycation end products. BMC Biol. 2022, 20, 68. [Google Scholar] [CrossRef]
- Blottner, D.; Hastermann, M.; Weber, R.; Lenz, R.; Gambara, G.; Limper, U.; Rittweger, J.; Bosutti, A.; Degens, H.; Salanova, M. Reactive Jumps Preserve Skeletal Muscle Structure, Phenotype, and Myofiber Oxidative Capacity in Bed Rest. Front. Physiol. 2019, 10, 1527. [Google Scholar] [CrossRef]
- Irimia, J.M.; Guerrero, M.; Rodriguez-Miguelez, P.; Cadefau, J.A.; Tesch, P.A.; Cusso, R.; Fernandez-Gonzalo, R. Metabolic adaptations in skeletal muscle after 84 days of bed rest with and without concurrent flywheel resistance exercise. J. Appl. Physiol. (1985) 2017, 122, 96–103. [Google Scholar] [CrossRef]
- Edgerton, V.R.; Zhou, M.Y.; Ohira, Y.; Klitgaard, H.; Jiang, B.; Bell, G.; Harris, B.; Saltin, B.; Gollnick, P.D.; Roy, R.R.; et al. Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J. Appl. Physiol. 1995, 78, 1733–1739. [Google Scholar] [CrossRef]
- Jackson, M.J.; Pollock, N.; Staunton, C.; Jones, S.; McArdle, A. Redox Control of Signalling Responses to Contractile Activity and Ageing in Skeletal Muscle. Cells 2022, 11, 1698. [Google Scholar] [CrossRef]
- Powers, S.K.; Deminice, R.; Ozdemir, M.; Yoshihara, T.; Bomkamp, M.P.; Hyatt, H. Exercise-induced oxidative stress: Friend or foe? J. Sport Health Sci. 2020, 9, 415–425. [Google Scholar] [CrossRef]
- Bellinger, A.M.; Reiken, S.; Dura, M.; Murphy, P.W.; Deng, S.X.; Landry, D.W.; Nieman, D.; Lehnart, S.E.; Samaru, M.; LaCampagne, A.; et al. Remodeling of ryanodine receptor complex causes “leaky” channels: A molecular mechanism for decreased exercise capacity. Proc. Natl. Acad. Sci. USA 2008, 105, 2198–2202. [Google Scholar] [CrossRef]
- Suhr, F.; Gehlert, S.; Grau, M.; Bloch, W. Skeletal muscle function during exercise-fine-tuning of diverse subsystems by nitric oxide. Int. J. Mol. Sci. 2013, 14, 7109–7139. [Google Scholar] [CrossRef]
- Hord, N.G.; Tang, Y.; Bryan, N.S. Food sources of nitrates and nitrites: The physiologic context for potential health benefits. Am. J. Clin. Nutr. 2009, 90, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Butler, A.R.; Feelisch, M. Therapeutic uses of inorganic nitrite and nitrate: From the past to the future. Circulation 2008, 117, 2151–2159. [Google Scholar] [CrossRef] [PubMed]
- Stein, T.P. Space flight and oxidative stress. Nutrition 2002, 18, 867–871. [Google Scholar] [CrossRef] [PubMed]
- Barbacini, P.; Blottner, D.; Capitanio, D.; Trautmann, G.; Block, K.; Torretta, E.; Moriggi, M.; Salanova, M.; Gelfi, C. Effects of Omega-3 and Antioxidant Cocktail Supplement on Prolonged Bed Rest: Results from Serum Proteome and Sphingolipids Analysis. Cells 2022, 11, 2120. [Google Scholar] [CrossRef] [PubMed]
- Gomez, X.; Sanon, S.; Zambrano, K.; Asquel, S.; Bassantes, M.; Morales, J.E.; Otanez, G.; Pomaquero, C.; Villarroel, S.; Zurita, A.; et al. Key points for the development of antioxidant cocktails to prevent cellular stress and damage caused by reactive oxygen species (ROS) during manned space missions. NPJ Microgravity 2021, 7, 35. [Google Scholar] [CrossRef] [PubMed]
- Hackney, K.J.; Scott, J.M.; Hanson, A.M.; English, K.L.; Downs, M.E.; Ploutz-Snyder, L.L. The Astronaut-Athlete: Optimizing Human Performance in Space. J. Strength Cond. Res. 2015, 29, 3531–3545. [Google Scholar] [CrossRef]
- Petersen, N.; Lambrecht, G.; Scott, J.; Hirsch, N.; Stokes, M.; Mester, J. Postflight reconditioning for European Astronauts—A case report of recovery after six months in space. Musculoskelet Sci. Pract. 2017, 27 (Suppl. 1), S23–S31. [Google Scholar] [CrossRef]
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Blottner, D.; Moriggi, M.; Trautmann, G.; Furlan, S.; Block, K.; Gutsmann, M.; Torretta, E.; Barbacini, P.; Capitanio, D.; Rittweger, J.; et al. Nitrosative Stress in Astronaut Skeletal Muscle in Spaceflight. Antioxidants 2024, 13, 432. https://doi.org/10.3390/antiox13040432
Blottner D, Moriggi M, Trautmann G, Furlan S, Block K, Gutsmann M, Torretta E, Barbacini P, Capitanio D, Rittweger J, et al. Nitrosative Stress in Astronaut Skeletal Muscle in Spaceflight. Antioxidants. 2024; 13(4):432. https://doi.org/10.3390/antiox13040432
Chicago/Turabian StyleBlottner, Dieter, Manuela Moriggi, Gabor Trautmann, Sandra Furlan, Katharina Block, Martina Gutsmann, Enrica Torretta, Pietro Barbacini, Daniele Capitanio, Joern Rittweger, and et al. 2024. "Nitrosative Stress in Astronaut Skeletal Muscle in Spaceflight" Antioxidants 13, no. 4: 432. https://doi.org/10.3390/antiox13040432