Spaceflight increases sarcoplasmic reticulum Ca
Journal
NPJ microgravity
ISSN: 2373-8065
Titre abrégé: NPJ Microgravity
Pays: United States
ID NLM: 101703605
Informations de publication
Date de publication:
19 Jul 2024
19 Jul 2024
Historique:
received:
01
03
2024
accepted:
11
07
2024
medline:
20
7
2024
pubmed:
20
7
2024
entrez:
19
7
2024
Statut:
epublish
Résumé
Spending time in a microgravity environment is known to cause significant skeletal muscle atrophy and weakness via muscle unloading, which can be partly attributed to Ca
Identifiants
pubmed: 39030182
doi: 10.1038/s41526-024-00419-y
pii: 10.1038/s41526-024-00419-y
doi:
Types de publication
Journal Article
Langues
eng
Pagination
78Informations de copyright
© 2024. The Author(s).
Références
Sandona, D. et al. Adaptation of mouse skeletal muscle to long-term microgravity in the MDS mission. PLoS ONE 7, e33232 (2012).
pubmed: 22470446
pmcid: 3314659
doi: 10.1371/journal.pone.0033232
Okada, R. et al. Transcriptome analysis of gravitational effects on mouse skeletal muscles under microgravity and artificial 1 g onboard environment. Sci. Rep. 11, 9168 (2021).
pubmed: 33911096
pmcid: 8080648
doi: 10.1038/s41598-021-88392-4
Widrick, J. J. et al. Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J. Physiol. 516, 915–930 (1999).
pubmed: 10200437
pmcid: 2269300
doi: 10.1111/j.1469-7793.1999.0915u.x
Monti, E. et al. Neuromuscular junction instability and altered intracellular calcium handling as early determinants of force loss during unloading in humans. J. Physiol. 599, 3037–3061 (2021).
pubmed: 33881176
doi: 10.1113/JP281365
Braun, J. L., Geromella, M. S., Hamstra, S. I., Messner, H. N. & Fajardo, V. A. Characterizing SERCA function in murine skeletal muscles after 35–37 days of spaceflight. Int. J. Mol. Sci. https://doi.org/10.3390/ijms222111764 (2021).
Baranowski, R. W. et al. Toward countering muscle and bone loss with spaceflight: GSK3 as a potential target. iScience 26, 107047 (2023).
pubmed: 37360691
pmcid: 10285634
doi: 10.1016/j.isci.2023.107047
Ingalls, C. P., Wenke, J. C. & Armstrong, R. B. Time course changes in [Ca2+]i, force, and protein content in hindlimb-suspended mouse soleus muscles. Aviat. Space Environ. Med. 72, 471–476 (2001).
pubmed: 11346014
Periasamy, M. & Huke, S. SERCA pump level is a critical determinant of Ca(2+)homeostasis and cardiac contractility. J. Mol. Cell. Cardiol. 33, 1053–1063 (2001).
pubmed: 11444913
doi: 10.1006/jmcc.2001.1366
Misquitta, C. M., Mack, D. P. & Grover, A. K. Sarco/endoplasmic reticulum Ca2+ (SERCA)-pumps: link to heart beats and calcium waves. Cell Calcium 25, 277–290 (1999).
pubmed: 10456225
doi: 10.1054/ceca.1999.0032
Eisner, V., Csordás, G. & Hajnóczky, G. Interactions between sarco-endoplasmic reticulum and mitochondria in cardiac and skeletal muscle - pivotal roles in Ca²
pubmed: 23843617
pmcid: 3711195
Qaisar, R. et al. Restoration of SERCA ATPase prevents oxidative stress-related muscle atrophy and weakness. Redox Biol. 20, 68–74 (2019).
pubmed: 30296699
doi: 10.1016/j.redox.2018.09.018
Qaisar, R. et al. Restoration of sarcoplasmic reticulum Ca(2+) ATPase (SERCA) activity prevents age-related muscle atrophy and weakness in mice. Int. J. Mol. Sci. https://doi.org/10.3390/ijms22010037 (2020).
Enns, D. L. & Belcastro, A. N. Early activation and redistribution of calpain activity in skeletal muscle during hindlimb unweighting and reweighting. Can. J. Physiol. Pharm. 84, 601–609 (2006).
doi: 10.1139/y06-013
Hosfield, C. M., Elce, J. S., Davies, P. L. & Jia, Z. Crystal structure of calpain reveals the structural basis for Ca(2+)-dependent protease activity and a novel mode of enzyme activation. EMBO J. 18, 6880–6889 (1999).
pubmed: 10601010
pmcid: 1171751
doi: 10.1093/emboj/18.24.6880
Viner, R. I., Ferrington, D. A., Huhmer, A. F., Bigelow, D. J. & Schoneich, C. Accumulation of nitrotyrosine on the SERCA2a isoform of SR Ca-ATPase of rat skeletal muscle during aging: a peroxynitrite-mediated process? FEBS Lett. 379, 286–290 (1996).
pubmed: 8603707
doi: 10.1016/0014-5793(95)01530-2
Viner, R. I., Ferrington, D. A., Williams, T. D., Bigelow, D. J. & Schöneich, C. Protein modification during biological aging: selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscle. Biochem. J. 340, 657–669 (1999).
pubmed: 10359649
pmcid: 1220296
doi: 10.1042/bj3400657
Viner, R. I., Williams, T. D. & Schöneich, C. Peroxynitrite modification of protein thiols: oxidation, nitrosylation, and S-glutathiolation of functionally important cysteine residue(s) in the sarcoplasmic reticulum Ca-ATPase. Biochemistry 38, 12408–12415 (1999).
pubmed: 10493809
doi: 10.1021/bi9909445
Tupling, A. R. et al. Effects of buthionine sulfoximine treatment on diaphragm contractility and SR Ca2+ pump function in rats. J. Appl. Physiol. 103, 1921–1928 (2007).
pubmed: 17717121
doi: 10.1152/japplphysiol.00529.2007
Braun, J. L., Hamstra, S. I., Messner, H. N. & Fajardo, V. A. SERCA2a tyrosine nitration coincides with impairments in maximal SERCA activity in left ventricles from tafazzin-deficient mice. Physiol. Rep. 7, e14215 (2019).
pubmed: 31444868
pmcid: 6708055
doi: 10.14814/phy2.14215
Braun, J. L. et al. Heterozygous SOD2 deletion selectively impairs SERCA function in the soleus of female mice. Physiol. Rep. 10, e15285 (2022).
pubmed: 35581738
pmcid: 9114654
doi: 10.14814/phy2.15285
Cleverdon, R. E. G. et al. Sarco(endo)plasmic reticulum Ca(2+)-ATPase function is impaired in skeletal and cardiac muscles from young DBA/2J mdx mice. iScience 25, 104972 (2022).
pubmed: 36093052
pmcid: 9459692
doi: 10.1016/j.isci.2022.104972
Qaisar, R. et al. Oxidative stress-induced dysregulation of excitation-contraction coupling contributes to muscle weakness. J. Cachexia Sarcopenia Muscle 9, 1003–1017 (2018).
pubmed: 30073804
pmcid: 6204588
doi: 10.1002/jcsm.12339
Fink, B. D., Bai, F., Yu, L. & Sivitz, W. I. Regulation of ATP production: dependence on calcium concentration and respiratory state. Am. J. Physiol. Cell Physiol. 313, C146–c153 (2017).
pubmed: 28515085
doi: 10.1152/ajpcell.00086.2017
Glancy, B., Willis, W. T., Chess, D. J. & Balaban, R. S. Effect of calcium on the oxidative phosphorylation cascade in skeletal muscle mitochondria. Biochemistry 52, 2793–2809 (2013).
pubmed: 23547908
doi: 10.1021/bi3015983
Kavanagh, N. I., Ainscow, E. K. & Brand, M. D. Calcium regulation of oxidative phosphorylation in rat skeletal muscle mitochondria. Biochim. Biophys. Acta 1457, 57–70 (2000).
pubmed: 10692550
doi: 10.1016/S0005-2728(00)00054-2
Pacher, P., Beckman, J. S. & Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87, 315–424 (2007).
pubmed: 17237348
doi: 10.1152/physrev.00029.2006
Miao, L. & St Clair, D. K. Regulation of superoxide dismutase genes: implications in disease. Free Radic. Biol. Med. 47, 344–356 (2009).
pubmed: 19477268
pmcid: 2731574
doi: 10.1016/j.freeradbiomed.2009.05.018
Batinic-Haberle, I., Tovmasyan, A. & Spasojevic, I. An educational overview of the chemistry, biochemistry and therapeutic aspects of Mn porphyrins–from superoxide dismutation to H2O2-driven pathways. Redox Biol. 5, 43–65 (2015).
pubmed: 25827425
pmcid: 4392060
doi: 10.1016/j.redox.2015.01.017
Batinic-Haberle, I. et al. SOD therapeutics: latest insights into their structure-activity relationships and impact on the cellular redox-based signaling pathways. Antioxid. Redox Signal. 20, 2372–2415 (2014).
pubmed: 23875805
pmcid: 4005498
doi: 10.1089/ars.2012.5147
Vujaskovic, Z. et al. A small molecular weight catalytic metalloporphyrin antioxidant with superoxide dismutase (SOD) mimetic properties protects lungs from radiation-induced injury. Free Radic. Biol. Med. 33, 857–863 (2002).
pubmed: 12208373
doi: 10.1016/S0891-5849(02)00980-2
Pearlstein, R. D. et al. Metalloporphyrin antioxidants ameliorate normal tissue radiation damage in rat brain. Int. J. Radiat. Biol. 86, 145–163 (2010).
pubmed: 20148700
doi: 10.3109/09553000903419965
Mao, X. W. et al. Radioprotective effect of a metalloporphyrin compound in rat eye model. Curr. Eye Res. 34, 62–72 (2009).
pubmed: 19172472
doi: 10.1080/02713680802546948
Mao, X. W., Crapo, J. D. & Gridley, D. S. Mitochondrial oxidative stress-induced apoptosis and radioprotection in proton-irradiated rat retina. Radiat. Res. 178, 118–125 (2012).
pubmed: 22780102
doi: 10.1667/RR2821.1
Fajardo, V. A. et al. Dietary docosahexaenoic acid supplementation reduces SERCA Ca2+ transport efficiency in rat skeletal muscle. Chem. Phys. Lipids 187, 56–61 (2015).
pubmed: 25772907
doi: 10.1016/j.chemphyslip.2015.03.001
Bombardier, E., Smith, I. C., Vigna, C., Fajardo, V. A. & Tupling, A. R. Ablation of sarcolipin decreases the energy requirements for Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases in resting skeletal muscle. FEBS Lett. 587, 1687–1692 (2013).
pubmed: 23628781
doi: 10.1016/j.febslet.2013.04.019
Tupling, R., Green, H. & Tupling, S. Partial ischemia reduces the efficiency of sarcoplasmic reticulum Ca2+ transport in rat EDL. Mol. Cell. Biochem. 224, 91–102 (2001).
pubmed: 11693204
doi: 10.1023/A:1011930502758
Yin, H., Xu, L. & Porter, N. A. Free radical lipid peroxidation: mechanisms and analysis. Chem. Rev. 111, 5944–5972 (2011).
pubmed: 21861450
doi: 10.1021/cr200084z
Altaeva, E. G., Ogneva, I. V. & Shenkman, B. Dynamics of calcium ions accumulation and changes of isoforms of sarcoplasmic reticulum Ca-ATPase (SERCA) in soleus muscle fibers of rats and Mongolian gerbils under gravitational unloading of various duration. Cell Tissue Biol. 4, 594–599 (2010).
doi: 10.1134/S1990519X10060118
Tupling, A. R. The sarcoplasmic reticulum in muscle fatigue and disease: role of the Sarco (endo)plasmic reticulum Ca2+-ATPase. Can. J. Appl. Physiol. 29, 308–329 (2004).
pubmed: 15199229
doi: 10.1139/h04-021
Kanazawa, Y., Takahashi, T., Nagano, M., Koinuma, S. & Shigeyoshi, Y. The effects of aging on sarcoplasmic reticulum-related factors in the skeletal muscle of mice. Int. J. Mol. Sci. https://doi.org/10.3390/ijms25042148 (2024).
Fajardo, V. A. et al. Phospholamban overexpression in mice causes a centronuclear myopathy-like phenotype. Dis. Model. Mech. 8, 999–1009 (2015).
pubmed: 26035394
pmcid: 4527296
Braun, J. L. et al. Neuronatin promotes SERCA uncoupling and its expression is altered in skeletal muscles of high-fat diet-fed mice. FEBS Lett. 595, 2756–2767 (2021).
pubmed: 34693525
doi: 10.1002/1873-3468.14213
Stammers, A. N. et al. The regulation of sarco(endo)plasmic reticulum calcium-ATPases (SERCA). Can. J. Physiol. Pharmacol. 93, 843–854 (2015).
pubmed: 25730320
doi: 10.1139/cjpp-2014-0463
Smith, W. S., Broadbridge, R., East, J. M. & Lee, A. G. Sarcolipin uncouples hydrolysis of ATP from accumulation of Ca2+ by the Ca2+-ATPase of skeletal-muscle sarcoplasmic reticulum. Biochem. J. 361, 277–286 (2002).
pubmed: 11772399
pmcid: 1222307
doi: 10.1042/bj3610277
Mao, X., Stanbouly, S., Holley, J., Pecaut, M. & Crapo, J. Evidence of spaceflight-induced adverse effects on photoreceptors and retinal function in the mouse eye. Int. J. Mol. Sci. https://doi.org/10.3390/ijms24087362 (2023).
Mao, X. W. et al. Characterization of mouse ocular response to a 35-day spaceflight mission: evidence of blood-retinal barrier disruption and ocular adaptations. Sci. Rep. 9, 8215 (2019).
pubmed: 31160660
pmcid: 6547757
doi: 10.1038/s41598-019-44696-0
Arutyunyan, R. et al. The contraction of unweighted fast and slow rat muscles in calcium-free solution. Basic Appl. Myol. 5, 169–175 (1995).
Ingalls, C. P., Warren, G. L. & Armstrong, R. B. Intracellular Ca2+ transients in mouse soleus muscle after hindlimb unloading and reloading. J. Appl. Physiol. 87, 386–390 (1999).
pubmed: 10409599
doi: 10.1152/jappl.1999.87.1.386
Nemirovskaya, T. L. & Sharlo, K. A. Roles of ATP and SERCA in the regulation of calcium turnover in unloaded skeletal muscles: current view and future directions. Int. J. Mol. Sci. https://doi.org/10.3390/ijms23136937 (2022).
Shenkman, B. S. How postural muscle senses disuse? Early signs and signals. Int. J. Mol. Sci. https://doi.org/10.3390/ijms21145037 (2020).
Shenkman, B. S. & Nemirovskaya, T. L. Calcium-dependent signaling mechanisms and soleus fiber remodeling under gravitational unloading. J. Muscle Res. Cell Motil. 29, 221–230 (2008).
pubmed: 19130271
doi: 10.1007/s10974-008-9164-7
Yoshioka, T., Shirota, T., Tazoe, T. & Yamashita-Goto, K. Calcium movement of sarcoplasmic reticulum from hindlimb suspended muscle. Acta Astronaut. 38, 209–212 (1996).
pubmed: 11540780
doi: 10.1016/0094-5765(96)00010-0
Kushnir, A. et al. Intracellular calcium leak as a therapeutic target for RYR1-related myopathies. Acta Neuropathol. 139, 1089–1104 (2020).
pubmed: 32236737
pmcid: 7788518
doi: 10.1007/s00401-020-02150-w
Lotteau, S. et al. A mechanism for statin-induced susceptibility to myopathy. JACC Basic Transl. Sci. 4, 509–523 (2019).
pubmed: 31468006
pmcid: 6712048
doi: 10.1016/j.jacbts.2019.03.012
Kushnir, A. et al. Ryanodine receptor calcium leak in circulating B-lymphocytes as a biomarker in heart failure. Circulation 138, 1144–1154 (2018).
pubmed: 29593014
pmcid: 6162180
doi: 10.1161/CIRCULATIONAHA.117.032703
Robin, G., Berthier, C. & Allard, B. Sarcoplasmic reticulum Ca2+ permeation explored from the lumen side in mdx muscle fibers under voltage control. J. Gen. Physiol. 139, 209–218 (2012).
pubmed: 22371362
pmcid: 3289961
doi: 10.1085/jgp.201110738
Mukhina, A. M., Altaeva, E. G., Nemirovskaya, T. L. & Shenkman, B. S. The role of L-type calcium channels in the accumulation of Ca2+ in soleus muscle fibers in the rat and changes in the ratio of myosin and serca isoforms in conditions of gravitational unloading. Neurosci. Behav. Physiol. 38, 181–188 (2008).
pubmed: 18197386
doi: 10.1007/s11055-008-0027-x
Froud, R. J., Earl, C. R., East, J. M. & Lee, A. G. Effects of lipid fatty acyl chain structure on the activity of the (Ca2+ + Mg2+)-ATPase. Biochim. Biophys. Acta 860, 354–360 (1986).
pubmed: 2943317
doi: 10.1016/0005-2736(86)90532-8
Cornea, R. L. & Thomas, D. D. Effects of membrane thickness on the molecular dynamics and enzymatic activity of reconstituted Ca-ATPase. Biochemistry 33, 2912–2920 (1994).
pubmed: 8130205
doi: 10.1021/bi00176a022
Van der Paal, J., Neyts, E. C., Verlackt, C. C. W. & Bogaerts, A. Effect of lipid peroxidation on membrane permeability of cancer and normal cells subjected to oxidative stress. Chem. Sci. 7, 489–498 (2016).
pubmed: 28791102
doi: 10.1039/C5SC02311D
Hirata, Y. et al. Lipid peroxidation increases membrane tension, Piezo1 gating, and cation permeability to execute ferroptosis. Curr. Biol. 33, 1282–1294.e1285 (2023).
pubmed: 36898371
doi: 10.1016/j.cub.2023.02.060
Wong-Ekkabut, J. et al. Effect of lipid peroxidation on the properties of lipid bilayers: a molecular dynamics study. Biophys. J. 93, 4225–4236 (2007).
pubmed: 17766354
pmcid: 2098729
doi: 10.1529/biophysj.107.112565
Kravtsova, V. V. et al. Isoform-specific Na,K-ATPase alterations precede disuse-induced atrophy of rat soleus muscle. Biomed. Res. Int. 2015, 720172 (2015).
pubmed: 25654120
pmcid: 4309216
doi: 10.1155/2015/720172
Kravtsova, V. V. et al. Chronic ouabain prevents Na,K-ATPase dysfunction and targets AMPK and IL-6 in disused rat soleus muscle. Int. J. Mol. Sci. https://doi.org/10.3390/ijms22083920 (2021).
Avila-Medina, J. et al. In Calcium Signaling (ed. Islam, M. S.) 489–504 (Springer Int. Publishing, 2020).
Edwards, J. N. et al. Upregulation of store-operated Ca2+ entry in dystrophic mdx mouse muscle. Am. J. Physiol. Cell Physiol. 299, C42–C50 (2010).
pubmed: 20427714
doi: 10.1152/ajpcell.00524.2009
Vandebrouck, C., Martin, D., Colson-Van Schoor, M., Debaix, H. & Gailly, P. Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J. Cell Biol. 158, 1089–1096 (2002).
pubmed: 12235126
pmcid: 2173225
doi: 10.1083/jcb.200203091
Lacruz, R. S. & Feske, S. Diseases caused by mutations in ORAI1 and STIM1. Ann. N. Y. Acad. Sci. 1356, 45–79 (2015).
pubmed: 26469693
pmcid: 4692058
doi: 10.1111/nyas.12938
Indo, H. P. et al. Changes in mitochondrial homeostasis and redox status in astronauts following long stays in space. Sci. Rep. 6, 39015 (2016).
pubmed: 27982062
pmcid: 5159838
doi: 10.1038/srep39015
Gehrig, S. M. et al. Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature 484, 394–398 (2012).
pubmed: 22495301
doi: 10.1038/nature10980
da Silveira, W. A. et al. Comprehensive multi-omics analysis reveals mitochondrial stress as a central biological hub for spaceflight impact. Cell 183, 1185–1201. e1120 (2020).
pubmed: 33242417
pmcid: 7870178
doi: 10.1016/j.cell.2020.11.002
Garrett-Bakelman, F. E. et al. The NASA Twins Study: a multidimensional analysis of a year-long human spaceflight. Science https://doi.org/10.1126/science.aau8650 (2019).
Mao, X. W. et al. Role of NADPH oxidase as a mediator of oxidative damage in low-dose irradiated and hindlimb-unloaded mice. Radiat. Res. 188, 392–399 (2017).
pubmed: 28763287
doi: 10.1667/RR14754.1
Kumar, A., Tahimic, C. G., Almeida, E. A. & Globus, R. K. Spaceflight modulates the expression of key oxidative stress and cell cycle related genes in heart. Int. J. Mol. Sci. 22, 9088 (2021).
pubmed: 34445793
pmcid: 8396460
doi: 10.3390/ijms22169088
Andersson, D. C. et al. Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab. 14, 196–207 (2011).
pubmed: 21803290
pmcid: 3690519
doi: 10.1016/j.cmet.2011.05.014
Agrawal, A. et al. Redox modification of ryanodine receptor contributes to impaired Ca(2+) homeostasis and exacerbates muscle atrophy under high altitude. Free Radic. Biol. Med. 160, 643–656 (2020).
pubmed: 32916280
doi: 10.1016/j.freeradbiomed.2020.09.001
Bellinger, A. M. et al. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat. Med. 15, 325–330 (2009).
pubmed: 19198614
pmcid: 2910579
doi: 10.1038/nm.1916
Sharlo, K. A. et al. The effect of SERCA activation on functional characteristics and signaling of rat soleus muscle upon 7 days of unloading. Biomolecules https://doi.org/10.3390/biom13091354 (2023).
Chambers, P. J., Juracic, E. S., Fajardo, V. A. & Tupling, A. R. Role of SERCA and sarcolipin in adaptive muscle remodeling. Am. J. Physiol. Cell Physiol. 322, C382–c394 (2022).
pubmed: 35044855
doi: 10.1152/ajpcell.00198.2021
Choi, S. Y. et al. Validation of a new rodent experimental system to investigate consequences of long duration space habitation. Sci. Rep. 10, 2336 (2020).
pubmed: 32047211
pmcid: 7012842
doi: 10.1038/s41598-020-58898-4
Sun, G. S. et al. Evaluation of the nutrient-upgraded rodent food bar for rodent spaceflight experiments. Nutrition 26, 1163–1169 (2010).
pubmed: 20116210
doi: 10.1016/j.nut.2009.09.018
Overbey, E. G. et al. Spaceflight influences gene expression, photoreceptor integrity, and oxidative stress-related damage in the murine retina. Sci. Rep. 9, 13304 (2019).
pubmed: 31527661
pmcid: 6746706
doi: 10.1038/s41598-019-49453-x
Kremsky, I. et al. Spaceflight-induced gene expression profiles in the mouse brain are attenuated by treatment with the antioxidant BuOE. Int. J. Mol. Sci. https://doi.org/10.3390/ijms241713569 (2023).