2-APB prevents atrophic changes and alters cellular signalling during unloading of rat M. Soleus
- 作者: Zaripova K.A.1, Bokov R.O.1, Sharlo K.A.1, Belova S.P.1, Nemirovskaya T.L.1
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隶属关系:
- Institute of Biomedical Problems RAS
- 期: 卷 110, 编号 9 (2024)
- 页面: 1390-1405
- 栏目: EXPERIMENTAL ARTICLES
- URL: https://medjrf.com/0869-8139/article/view/651747
- DOI: https://doi.org/10.31857/S0869813924090084
- EDN: https://elibrary.ru/AJUMSN
- ID: 651747
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详细
IP3 receptors are found in significant quantities in muscle fibers in the sarcoplasmic reticulum, nucleus and mitochondria. We hypothesized that activation of IP3 receptors (IP3Rs) during muscle unloading may induce a weak calcium release signal, both cytosolic and nucleoplasmic, that promotes (possibly with other signaling cascades) the activation of transcription factors, leading to the expression or repression of genes involved in muscle phenotype. This hypothesis was tested by blocking IP3R during unloading of rat muscles by administering 2-APB (2-aminoethoxydiphenyl borate). Wistar rats were administered intraperitoneally at a dose of 10 mg/mg in 5 % DMSO daily. We found that the IP3R state influences the development of atrophic processes in the postural m. soleus during unloading. Administration of the IP3R blocker 2-APB to animals successfully prevented a decrease in m. soleus cross-sectional area (CSA) of both fast and slow muscle fibers. The slowdown in CSA decrease upon administration IP3R inhibitor during 7 days m. soleus unloading is associated with the prevention of a decrease in ribosomal biogenesis and an increase in the expression of autophagy markers ULK-1 and IL-6.
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作者简介
K. Zaripova
Institute of Biomedical Problems RAS
Email: Nemirovskaya@bk.ru
俄罗斯联邦, Moscow
R. Bokov
Institute of Biomedical Problems RAS
Email: Nemirovskaya@bk.ru
俄罗斯联邦, Moscow
K. Sharlo
Institute of Biomedical Problems RAS
Email: Nemirovskaya@bk.ru
俄罗斯联邦, Moscow
S. Belova
Institute of Biomedical Problems RAS
Email: Nemirovskaya@bk.ru
俄罗斯联邦, Moscow
T. Nemirovskaya
Institute of Biomedical Problems RAS
编辑信件的主要联系方式.
Email: Nemirovskaya@bk.ru
俄罗斯联邦, Moscow
参考
- Morey-Holton E, Globus RK, Kaplansky A, Durnova G (2005) The hindlimb unloading rat model: literature overview, technique update and comparison with space flight data. Adv Space Biol Med 10: 7–40. https://doi.org/10.1016/s1569-2574(05)10002-1
- Ingalls CP, Warren GL, Armstrong RB (1999) Intracellular Ca2+ transients in mouse soleus muscle after hindlimb unloading and reloading. J Appl Physiol (1985) 87(1): 386–390. https://doi.org/10.1152/jappl.1999.87.1.386
- Shenkman BS, Nemirovskaya TL (2008) Calcium-dependent signaling mechanisms and soleus fiber remodeling under gravitational unloading. J Muscle Res Cell Motil 29(6–8): 221–230. https://doi.org/10.1007/s10974-008-9164-7
- Yang H, Wang H, Pan F, Guo Y, Cao L, Yan W, Gao Y (2023) New Findings: Hindlimb Unloading Causes Nucleocytoplasmic Ca(2+) Overload and DNA Damage in Skeletal Muscle. Cells 12(7): https://doi.org/10.3390/cells12071077
- Melnikov IY, Tyganov SA, Sharlo KA, Ulanova AD, Vikhlyantsev IM, Mirzoev TM, Shenkman BS (2022) Calpain-dependent degradation of cytoskeletal proteins as a key mechanism for a reduction in intrinsic passive stiffness of unloaded rat postural muscle. Pflugers Arch 474(11): 1171–1183. https://doi.org/10.1007/s00424-022-02740-5
- Mijares A, Allen PD, Lopez JR (2020) Senescence Is Associated With Elevated Intracellular Resting [Ca(2 +)] in Mice Skeletal Muscle Fibers. An in vivo Study. Front Physiol 11: 601189. https://doi.org/10.3389/fphys.2020.601189
- Turner PR, Westwood T, Regen CM, Steinhardt RA (1988) Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335(6192): 735–738. https://doi.org/10.1038/335735a0
- Carafoli E, Krebs J (2016) Why Calcium? How Calcium Became the Best Communicator. J Biol Chem 291(40): 20849–20857. https://doi.org/10.1074/jbc.R116.735894
- Chibalin AV, Benziane B, Zakyrjanova GF, Kravtsova VV, Krivoi II (2018) Early endplate remodeling and skeletal muscle signaling events following rat hindlimb suspension. J Cell Physiol 233(10): 6329–6336. https://doi.org/10.1002/jcp.26594
- Georgiev T, Svirin M, Jaimovich E, Fink RH (2015) Localized nuclear and perinuclear Ca(2+) signals in intact mouse skeletal muscle fibers. Front Physiol 6: 263. https://doi.org/10.3389/fphys.2015.00263
- Taylor CW, Tovey SC (2010) IP(3) receptors: toward understanding their activation. Cold Spring Harb Perspect Biol 2(12): a004010. https://doi.org/10.1101/cshperspect.a004010
- Foskett JK, White C, Cheung KH, Mak DO (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87(2): 593–658. https://doi.org/10.1152/physrev.00035.2006
- Berridge MJ (2016) The Inositol Trisphosphate/Calcium Signaling Pathway in Health and Disease. Physiol Rev 96(4): 1261–1296. https://doi.org/10.1152/physrev.00006.2016
- Midrio M, Danieli-Betto D, Megighian A, Betto R (1997) Early effects of denervation on sarcoplasmic reticulum properties of slow-twitch rat muscle fibres. Pflugers Arch 434(4): 398–405. https://doi.org/10.1007/s004240050413
- Sharlo KA, Lvova ID, Tyganov SA, Zaripova KA, Belova SP, Kostrominova TY, Shenkman BS, Nemirovskaya TL (2023) The Effect of SERCA Activation on Functional Characteristics and Signaling of Rat Soleus Muscle upon 7 Days of Unloading. Biomolecules 13(9): https://doi.org/10.3390/biom13091354
- Jaimovich E, Reyes R, Liberona JL, Powell JA (2000) IP(3) receptors, IP(3) transients, and nucleus-associated Ca(2+) signals in cultured skeletal muscle. Am J Physiol Cell Physiol 278(5): C998–C1010. https://doi.org/10.1152/ajpcell.2000.278.5.C998
- Arias-Calderon M, Almarza G, Diaz-Vegas A, Contreras-Ferrat A, Valladares D, Casas M, Toledo H, Jaimovich E, Buvinic S (2016) Characterization of a multiprotein complex involved in excitation-transcription coupling of skeletal muscle. Skelet Muscle 6: 15. https://doi.org/10.1186/s13395-016-0087-5
- Casas M, Altamirano F, Jaimovich E (2012) Measurement of calcium release due to inositol trisphosphate receptors in skeletal muscle. Methods Mol Biol 798: 383–393. https://doi.org/10.1007/978-1-61779-343-1_22
- Cardenas C, Liberona JL, Molgo J, Colasante C, Mignery GA, Jaimovich E (2005) Nuclear inositol 1,4,5-trisphosphate receptors regulate local Ca2+ transients and modulate cAMP response element binding protein phosphorylation. J Cell Sci 118(Pt 14): 3131–3140. https://doi.org/10.1242/jcs.02446
- Araya R, Liberona JL, Cardenas JC, Riveros N, Estrada M, Powell JA, Carrasco MA, Jaimovich E (2003) Dihydropyridine receptors as voltage sensors for a depolarization-evoked, IP3R-mediated, slow calcium signal in skeletal muscle cells. J Gen Physiol 121(1): 3–16. https://doi.org/10.1085/jgp.20028671
- Powell JA, Carrasco MA, Adams DS, Drouet B, Rios J, Muller M, Estrada M, Jaimovich E (2001) IP(3) receptor function and localization in myotubes: an unexplored Ca(2+) signaling pathway in skeletal muscle. J Cell Sci 114(Pt 20): 3673–3683. https://doi.org/10.1242/jcs.114.20.3673
- Altamirano F, Valladares D, Henriquez-Olguin C, Casas M, Lopez JR, Allen PD, Jaimovich E (2013) Nifedipine treatment reduces resting calcium concentration, oxidative and apoptotic gene expression, and improves muscle function in dystrophic mdx mice. PLoS One 8(12): e81222. https://doi.org/10.1371/journal.pone.0081222
- Casas M, Buvinic S, Jaimovich E (2014) ATP signaling in skeletal muscle: from fiber plasticity to regulation of metabolism. Exerc Sport Sci Rev 42(3): 110–116. https://doi.org/10.1249/JES.0000000000000017
- Valladares D, Utreras-Mendoza Y, Campos C, Morales C, Diaz-Vegas A, Contreras-Ferrat A, Westermeier F, Jaimovich E, Marchi S, Pinton P, Lavandero S (2018) IP(3) receptor blockade restores autophagy and mitochondrial function in skeletal muscle fibers of dystrophic mice. Biochim Biophys Acta Mol Basis Dis 1864(11): 3685–3695. https://doi.org/10.1016/j.bbadis.2018.08.042
- Kravtsova VV, Paramonova II, Vilchinskaya NA, Tishkova MV, Matchkov VV, Shenkman BS, Krivoi II (2021) Chronic Ouabain Prevents Na, K-ATPase Dysfunction and Targets AMPK and IL-6 in Disused Rat Soleus Muscle. Int J Mol Sci 22(8): https://doi.org/10.3390/ijms22083920
- Zaripova KA, Kalashnikova EP, Belova SP, Kostrominova TY, Shenkman BS, Nemirovskaya TL (2021) Role of Pannexin 1 ATP-Permeable Channels in the Regulation of Signaling Pathways during Skeletal Muscle Unloading. Int J Mol Sci 22(19): https://doi.org/10.3390/ijms221910444
- Zaripova KA, Belova SP, Kostrominova TY, Shenkman BS, Nemirovskaya TL (2024) P2Y1 and P2Y2 receptors differ in their role in the regulation of signaling pathways during unloading-induced rat soleus muscle atrophy. Arch Biochem Biophys 751: 109844. https://doi.org/10.1016/j.abb.2023.109844
- Carrasco MA, Riveros N, Rios J, Muller M, Torres F, Pineda J, Lantadilla S, Jaimovich E (2003) Depolarization-induced slow calcium transients activate early genes in skeletal muscle cells. Am J Physiol Cell Physiol 284(6): C1438–С1447. https://doi.org/10.1152/ajpcell.00117.2002
- Kandarian SC, Stevenson EJ (2002) Molecular events in skeletal muscle during disuse atrophy. Exerc Sport Sci Rev 30(3): 111–116. https://doi.org/10.1097/00003677-200207000-00004
- Ye L, Zeng Q, Ling M, Ma R, Chen H, Lin F, Li Z, Pan L (2021) Inhibition of IP3R/Ca2+ Dysregulation Protects Mice From Ventilator-Induced Lung Injury via Endoplasmic Reticulum and Mitochondrial Pathways. Front Immunol 12: 729094. https://doi.org/10.3389/fimmu.2021.729094
- Gambardella J, Morelli MB, Wang X, Castellanos V, Mone P, Santulli G (2021) The discovery and development of IP3 receptor modulators: an update. Expert Opin Drug Discov 16(6): 709–718. https://doi.org/10.1080/17460441.2021.1858792
- Bilmen JG, Wootton LL, Godfrey RE, Smart OS, Michelangeli F (2002) Inhibition of SERCA Ca2+ pumps by 2-aminoethoxydiphenyl borate (2-APB). 2-APB reduces both Ca2+ binding and phosphoryl transfer from ATP, by interfering with the pathway leading to the Ca2+-binding sites. Eur J Biochem 269(15): 3678–3687. https://doi.org/10.1046/j.1432-1033.2002.03060.x
- Kimura S, Inaoka PT, Yamazaki T (2012) Influence of passive stretching on inhibition of disuse atrophy and hemodynamics of rat soleus muscle. J Jpn Phys Ther Assoc 15(1): 9–14. https://doi.org/10.1298/jjpta.Vol15_002
- Baldwin KM, Haddad F (2002) Skeletal muscle plasticity: cellular and molecular responses to altered physical activity paradigms. Am J Phys Med Rehabil 81(11 Suppl): S40–S51. https://doi.org/10.1097/01.PHM.0000029723.36419.0D
- D'Aquila P, Montesanto A, Mandala M, Garasto S, Mari V, Corsonello A, Bellizzi D, Passarino G (2017) Methylation of the ribosomal RNA gene promoter is associated with aging and age-related decline. Aging Cell 16(5): 966–975. https://doi.org/10.1111/acel.12603
- Grummt I, Langst G (2013) Epigenetic control of RNA polymerase I transcription in mammalian cells. Biochim Biophys Acta 1829(3–4): 393–404. https://doi.org/10.1016/j.bbagrm.2012.10.004
- Williams K, Christensen J, Helin K (2011) DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep 13(1): 28–35. https://doi.org/10.1038/embor.2011.233
- Wang Y, Zhang Y (2014) Regulation of TET protein stability by calpains. Cell Rep 6(2): 278–284. https://doi.org/10.1016/j.celrep.2013.12.031
- Bodine SC, Baehr LM (2014) Skeletal muscle atrophy and the E3 ubiquitin ligases MuRF1 and MAFbx/atrogin-1. Am J Physiol Endocrinol Metab 307(6): E469–E484. https://doi.org/10.1152/ajpendo.00204.2014
- Belova SP, Zaripova K, Sharlo K, Kostrominova TY, Shenkman BS, Nemirovskaya TL (2022) Metformin attenuates an increase of calcium-dependent and ubiquitin-proteasome markers in unloaded muscle. J Appl Physiol (1985) https://doi.org/10.1152/japplphysiol.00415.2022
- Parys JB, Decuypere JP, Bultynck G (2012) Role of the inositol 1,4,5-trisphosphate receptor/Ca2+-release channel in autophagy. Cell Commun Signal 10(1): 17. https://doi.org/10.1186/1478-811X-10-17
- Criollo A, Vicencio JM, Tasdemir E, Maiuri MC, Lavandero S, Kroemer G (2007) The inositol trisphosphate receptor in the control of autophagy. Autophagy 3(4): 350–353. https://doi.org/10.4161/auto.4077
- Yakabe M, Ogawa S, Ota H, Iijima K, Eto M, Ouchi Y, Akishita M (2018) Inhibition of interleukin-6 decreases atrogene expression and ameliorates tail suspension-induced skeletal muscle atrophy. PLoS One 13(1): e0191318. https://doi.org/10.1371/journal.pone.0191318
- Вильчинская НА, Парамонова ИИ, Немировская ТЛ, Ломоносова ЮН, Шенкман БС (ред) (2020) Экспрессия интерлейкина-6 в камбаловидной мышце крысы в условиях функциональной разгрузки. Динамика процесса и роль кальциевых каналов L-типа. Авиакосм экол мед 54(3): 70–78. [Vil'chinskaya NA, Paramonova II, Nemirovskaya TL, Lomonosova YN, Shenkman BS (2020) Expression of interleukin-6 in the rat soleus muscle under conditions of functional unloading. Dynamics of the process and the role of L-type calcium channels. Aviakosm ekol med 54(3): 70–78. (In Russ)]. https://doi.org/10.21687/0233-528X-2020-54-3-70-78
- Hodge DR, Cho E, Copeland TD, Guszczynski T, Yang E, Seth AK, Farrar WL (2007) IL-6 enhances the nuclear translocation of DNA cytosine-5-methyltransferase 1 (DNMT1) via phosphorylation of the nuclear localization sequence by the AKT kinase. Cancer Genomics Proteomics 4(6): 387–398. https://doi.org/
- Rose AJ, Kiens B, Richter EA (2006) Ca2+-calmodulin-dependent protein kinase expression and signalling in skeletal muscle during exercise. J Physiol 574(Pt 3): 889–903. https://doi.org/10.1113/jphysiol.2006.111757
- Rostas JAP, Skelding KA (2023) Calcium/Calmodulin-Stimulated Protein Kinase II (CaMKII): Different Functional Outcomes from Activation, Depending on the Cellular Microenvironment. Cells 12(3): https://doi.org/10.3390/cells12030401
- Sun H, Sun J, Li M, Qian L, Zhang L, Huang Z, Shen Y, Law BY, Liu L, Gu X (2021) Transcriptome Analysis of Immune Receptor Activation and Energy Metabolism Reduction as the Underlying Mechanisms in Interleukin-6-Induced Skeletal Muscle Atrophy. Front Immunol 12: 730070. https://doi.org/10.3389/fimmu.2021.730070
- Witczak CA, Sharoff CG, Goodyear LJ (2008) AMP-activated protein kinase in skeletal muscle: from structure and localization to its role as a master regulator of cellular metabolism. Cell Mol Life Sci 65(23): 3737–3755. https://doi.org/10.1007/s00018-008-8244-6
- Raney MA, Turcotte LP (2008) Evidence for the involvement of CaMKII and AMPK in Ca2+-dependent signaling pathways regulating FA uptake and oxidation in contracting rodent muscle. J Appl Physiol (1985) 104(5): 1366–1373. https://doi.org/10.1152/japplphysiol.01282.2007
- Liang Q, Zhang Y, Zeng M, Guan L, Xiao Y, Xiao F (2018) The role of IP3R-SOCCs in Cr(vi)-induced cytosolic Ca(2+) overload and apoptosis in L-02 hepatocytes. Toxicol Res (Camb) 7(3): 521–528. https://doi.org/10.1039/c8tx00029h
- Hohendanner F, Maxwell JT, Blatter LA (2015) Cytosolic and nuclear calcium signaling in atrial myocytes: IP3-mediated calcium release and the role of mitochondria. Channels (Austin) 9(3): 129–138. https://doi.org/10.1080/19336950.2015.1040966
- Gomes DA, Leite MF, Bennett AM, Nathanson MH (2006) Calcium signaling in the nucleus. Can J Physiol Pharmacol 84(3–4): 325–332. https://doi.org/10.1139/y05-117
- Park S, Scheffler TL, Gerrard DE (2011) Chronic high cytosolic calcium decreases AICAR-induced AMPK activity via calcium/calmodulin activated protein kinase II signaling cascade. Cell Calcium 50(1): 73–83. https://doi.org/10.1016/j.ceca.2011.05.009
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