The Maintenance of AMPK Activity Eliminates Abnormally Accelerated Differentiation of Primary Myoblasts Isolated from Atrophied Rat Soleus Muscle

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Аннотация

Mechanical unloading of skeletal muscles leads to the development of atrophic processes and a decrease in the total number of satellite cells (SCs) that are involved in muscle regeneration. In vitro studies revealed an increased differentiation of myoblasts derived from rat soleus muscle after an unloading-induced decrease in AMP-activated protein kinase (AMPK). AMPK is necessary for the activation of SCs and also participates in the regulation of myoblast proliferation and differentiation. It can be assumed that a decrease in the activity of AMPK after mechanical unloading can contribute to the acceleration of myoblast differentiation. The main purpose of this study was to elucidate a possible role of AMPK in the regulation of differentiation of myoblasts isolated from rat soleus muscle after mechanical unloading. To test this hypothesis, a specific AMPK activator, AICAR, was used to prevent a decrease in AMPK activity during differentiation of myoblasts isolated from rat soleus muscle after 7-day unloading. Immunocytochemistry, PCR-RT and Western blotting were used to assess changes during myoblast differentiation. In differentiating myoblasts derived from the unloaded soleus muscle there was a significant decrease in AMPK (Thr172) and ACC (Ser 79) phosphorylation levels, an increase in myotube differentiation index, myoblast fusion factors and the expression of myogenic regulatory factors (MRF). Furthermore, there was a decrease in the expression of slow myosin heavy chains (MyHC) and an increase in the expression of fast MyHC isoforms. AICAR treatment of differentiating myoblasts obtained from the unloaded soleus muscle prevented a decrease in AMPK and ACC phosphorylation, returned the expression levels of MRF and fast isoforms of MyHC to the control levels as well as maintained the expression of slow MyHC. Thus, abnormally accelerated differentiation of myoblasts isolated from atrophied rat soleus muscle can be compensated by maintaining the control levels of AMPK activity using AICAR.

Авторлар туралы

N. Vilchinskaya

Institute of Biomedical Problems of the Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: vilchinskayanatalia@gmail.com
Russia, Moscow

T. Mirzoev

Institute of Biomedical Problems of the Russian Academy of Sciences

Email: vilchinskayanatalia@gmail.com
Russia, Moscow

B. Shenkman

Institute of Biomedical Problems of the Russian Academy of Sciences

Email: vilchinskayanatalia@gmail.com
Russia, Moscow

Әдебиет тізімі

  1. Oganov VS, Skuratova SA, Murashko LM, Guba F, Takach O (1988) Effect of short-term space flights on physiological properties and composition of myofibrillar proteins of the skeletal muscles of rats. Kosm Biol Aviakosm Med 22 (4): 50–54.
  2. Shenkman BS (2016) From Slow to Fast: Hypogravity-Induced Remodeling of Muscle Fiber Myosin Phenotype. Acta Naturae 8 4(31): 47–59.https://doi.org/10.32607/20758251-2016-8-4-47-59
  3. Ohira Y, Yoshinaga T, Nomura T, Kawano F, Ishihara A, Nonaka I, Roy RR, Edgerton VR (2002) Gravitational unloading effects on muscle fiber size, phenotype and myonuclear number. Adv Space Res 30(4): 777–781. https://doi.org/10.1016/s0273-1177(02)00395-2
  4. Thomason DB, Biggs RB, Booth FW (1989) Protein metabolism and beta-myosin heavy-chain mRNA in unweighted soleus muscle. Am J Physiol 257(Pt 2): R300–R305. https://doi.org/10.1152/ajpregu.1989.257.2.R300
  5. Yin H, Price F, Rudnicki MA (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93(1): 23–67. https://doi.org/10.1152/physrev.00043.2011
  6. Dumont NA, Bentzinger CF, Sincennes MC, Rudnicki MA (2015) Satellite Cells and Skeletal Muscle Regeneration. Compr Physiol 5(3): 1027–1059. https://doi.org/10.1002/cphy.c140068
  7. Wang YX, Dumont NA, Rudnicki MA (2014) Muscle stem cells at a glance. J Cell Sci 127(Pt 21): 4543–4548. https://doi.org/10.1242/jcs.151209
  8. Wagers AJ, Conboy IM (2005) Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 122(5): 659–667. https://doi.org/10.1016/j.cell.2005.08.021
  9. Shenkman BS, Turtikova OV, Nemirovskaya TL, Grigoriev AI (2010) Skeletal muscle activity and the fate of myonuclei. Acta Naturae 2(2): 59–66.
  10. Nakanishi R, Hirayama Y, Tanaka M, Maeshige N, Kondo H, Ishihara A, Roy RR, Fujino H (2016) Nucleoprotein supplementation enhances the recovery of rat soleus mass with reloading after hindlimb unloading-induced atrophy via myonuclei accretion and increased protein synthesis. Nutr Res 36(12): 1335–1344. https://doi.org/10.1016/j.nutres.2016.10.007
  11. Mitchell PO, Pavlath GK (2004) Skeletal muscle atrophy leads to loss and dysfunction of muscle precursor cells. Am J Physiol Cell Physiol 287(6): C1753–C1762. https://doi.org/10.1152/ajpcell.00292.2004
  12. Matsuba Y, Goto K, Morioka S, Naito T, Akema T, Hashimoto N, Sugiura T, Ohira Y, Beppu M, Yoshioka T (2009) Gravitational unloading inhibits the regenerative potential of atrophied soleus muscle in mice. Acta Physiol (Oxf) 196(3): 329–339. https://doi.org/10.1111/j.1748-1716.2008.01943.x
  13. Ferreira R, Neuparth MJ, Ascensao A, Magalhaes J, Vitorino R, Duarte JA, Amado F (2006) Skeletal muscle atrophy increases cell proliferation in mice gastrocnemius during the first week of hindlimb suspension. Eur J Appl Physiol 97(3): 340–346. https://doi.org/10.1007/s00421-006-0197-6
  14. Guitart M, Lloreta J, Manas-Garcia L, Barreiro E (2018) Muscle regeneration potential and satellite cell activation profile during recovery following hindlimb immobilization in mice. J Cell Physiol 233(5): 4360–4372. https://doi.org/10.1002/jcp.26282
  15. Mirzoev T, Tyganov S, Vilchinskaya N, Lomonosova Y, Shenkman B (2016) Key Markers of mTORC1-Dependent and mTORC1-Independent Signaling Pathways Regulating Protein Synthesis in Rat Soleus Muscle During Early Stages of Hindlimb Unloading. Cell Physiol Biochem 39(3): 1011–1020. https://doi.org/10.1159/000447808
  16. Hardie DG (2005) New roles for the LKB1–>AMPK pathway. Curr Opin Cell Biol 17 (2): 167–173. https://doi.org/10.1016/j.ceb.2005.01.006
  17. Mounier R, Lantier L, Leclerc J, Sotiropoulos A, Pende M, Daegelen D, Sakamoto K, Foretz M, Viollet B (2009) Important role for AMPKalpha1 in limiting skeletal muscle cell hypertrophy. FASEB J 23(7): 2264–2273. https://doi.org/10.1096/fj.08-119057
  18. Villanueva-Paz M, Cotan D, Garrido-Maraver J, Oropesa-Avila M, de la Mata M, Delgado-Pavon A, de Lavera I, Alcocer-Gomez E, Alvarez-Cordoba M, Sanchez-Alcazar JA (2016) AMPK Regulation of Cell Growth, Apoptosis, Autophagy, and Bioenergetics. Exp Suppl 107: 45–71. https://doi.org/10.1007/978-3-319-43589-3_3
  19. Thomson DM (2018) The Role of AMPK in the Regulation of Skeletal Muscle Size, Hypertrophy, and Regeneration. Int J Mol Sci 19(10): 3125. https://doi.org/10.3390/ijms19103125
  20. Fu X, Zhu MJ, Dodson MV, Du M (2015) AMP-activated protein kinase stimulates Warburg-like glycolysis and activation of satellite cells during muscle regeneration. J Biol Chem 290 (44): 26445–26456. https://doi.org/10.1074/jbc.M115.665232
  21. Fu X, Zhao JX, Zhu MJ, Foretz M, Viollet B, Dodson MV, Du M (2013) AMP-activated protein kinase alpha1 but not alpha2 catalytic subunit potentiates myogenin expression and myogenesis. Mol Cell Biol 33 (22): 4517–4525. https://doi.org/10.1128/MCB.01078-13
  22. Fu X, Zhu M, Zhang S, Foretz M, Viollet B, Du M (2016) Obesity Impairs Skeletal Muscle Regeneration Through Inhibition of AMPK. Diabetes 65 (1): 188–200. https://doi.org/10.2337/db15-0647
  23. Steinberg GR, Michell BJ, van Denderen BJ, Watt MJ, Carey AL, Fam BC, Andrikopoulos S, Proietto J, Gorgun CZ, Carling D, Hotamisligil GS, Febbraio MA, Kay TW, Kemp BE (2006) Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab 4(6): 465–474. https://doi.org/10.1016/j.cmet.2006.11.005
  24. Williamson DL, Butler DC, Alway SE (2009) AMPK inhibits myoblast differentiation through a PGC-1alpha-dependent mechanism. Am J Physiol Endocrinol Metab 297 (2): E304–E314. https://doi.org/10.1152/ajpendo.91007.2008
  25. Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, Sauve AA, Sartorelli V (2008) Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14(5): 661–673. https://doi.org/10.1016/j.devcel.2008.02.004
  26. Komarova MY, Rozhkov SV, Ivanova OA, Turtikova OV, Mirzoev TM, Dmitrieva RI, Shenkman BS, Vilchinskaya NA (2022) Cultured Myoblasts Derived from Rat Soleus Muscle Show Altered Regulation of Proliferation and Myogenesis during the Course of Mechanical Unloading. Int J Mol Sci 23(16): 9150. https://doi.org/10.3390/ijms23169150
  27. Vilchinskaya NA, Rozhkov SV, Komarova MY, Dmitrieva RI, Shenkman BS (2022) Effect of simulated gravitational unloading on m. Soleus satellite cells. Aviakosm Ekol Med (Russia) 56(1): 20–29. https://doi.org/10.21687/0233-528X-2022-56-2-20-29
  28. Novikov VE, Ilyin EA (1981) Age-related reactions of rat bones to their unloading. Avia Space Environ Med 52(9): 551–553.
  29. Morey-Holton ER, Globus RK (2002) Hindlimb unloading rodent model: technical aspects. J Appl Physiol (1985) 92(4): 1367–1377. https://doi.org/10.1152/japplphysiol.00969.2001
  30. Theret M, Gsaier L, Schaffer B, Juban G, Ben Larbi S, Weiss-Gayet M, Bultot L, Collodet C, Foretz M, Desplanches D, Sanz P, Zang Z, Yang L, Vial G, Viollet B, Sakamoto K, Brunet A, Chazaud B, Mounier R (2017) AMPKalpha1-LDH pathway regulates muscle stem cell self-renewal by controlling metabolic homeostasis. EMBO J 36(13): 1946–1962. https://doi.org/10.15252/embj.201695273
  31. Fu X, Zhao JX, Liang J, Zhu MJ, Foretz M, Viollet B, Du M (2013) AMP-activated protein kinase mediates myogenin expression and myogenesis via histone deacetylase 5. Am J Physiol Cell Physiol 305 (8): C887–C895. https://doi.org/10.1152/ajpcell.00124.2013
  32. Vilchinskaya NA, Mochalova EP, Nemirovskaya TL, Mirzoev TM, Turtikova OV, Shenkman BS (2017) Rapid decline in MyHC I(beta) mRNA expression in rat soleus during hindlimb unloading is associated with AMPK dephosphorylation. J Physiol 595 (23): 7123–7134. https://doi.org/10.1113/JP275184
  33. Belova SP, Vilchinskaya NA, Mochalova EP, Mirzoev TM, Nemirovskaya TL, Shenkman BS (2019) Elevated p70S6K phosphorylation in rat soleus muscle during the early stage of unloading: Causes and consequences. Arch Biochem Biophys 674: 108105. https://doi.org/10.1016/j.abb.2019.108105
  34. 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
  35. Hilder TL, Baer LA, Fuller PM, Fuller CA, Grindeland RE, Wade CE, Graves LM (2005) Insulin-independent pathways mediating glucose uptake in hindlimb-suspended skeletal muscle. J Appl Physiol (1985) 99(6): 2181–2188. https://doi.org/10.1152/japplphysiol.00743.2005
  36. Inoki K, Zhu T, Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115(5): 577–590. https://doi.org/10.1016/s0092-8674(03)00929-2
  37. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30(2): 214–226. https://doi.org/10.1016/j.molcel.2008.03.003
  38. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS (2002) AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 277(27): 23977–23980. https://doi.org/10.1074/jbc.C200171200
  39. Williamson DL, Bolster DR, Kimball SR, Jefferson LS (2006) Time course changes in signaling pathways and protein synthesis in C2C12 myotubes following AMPK activation by AICAR. Am J Physiol Endocrinol Metab 291(1): E80–E89. https://doi.org/10.1152/ajpendo.00566.2005
  40. Nakashima K, Ishida A (2022) AMP-activated Protein Kinase Activation Suppresses Protein Synthesis and mTORC1 Signaling in Chick Myotube Cultures. J Poult Sci 59 (1): 81–85. https://doi.org/10.2141/jpsa.0210021
  41. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, Nir T, Dor Y, Zisman P, Meyuhas O (2005) Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 19(18): 2199–2211. https://doi.org/10.1101/gad.351605
  42. Cuenda A, Cohen P (1999) Stress-activated protein kinase-2/p38 and a rapamycin-sensitive pathway are required for C2C12 myogenesis. J Biol Chem 274(7): 4341–4346. https://doi.org/10.1074/jbc.274.7.4341
  43. Pollard HJ, Willett M, Morley SJ (2014) mTOR kinase-dependent, but raptor-independent regulation of downstream signaling is important for cell cycle exit and myogenic differentiation. Cell Cycle 13(16): 2517–2525. https://doi.org/10.4161/15384101.2014.941747
  44. Rion N, Castets P, Lin S, Enderle L, Reinhard JR, Eickhorst C, Ruegg MA (2019) mTOR controls embryonic and adult myogenesis via mTORC1. Development 146(7): 172460. https://doi.org/10.1242/dev.172460
  45. Zhang P, Liang X, Shan T, Jiang Q, Deng C, Zheng R, Kuang S (2015) mTOR is necessary for proper satellite cell activity and skeletal muscle regeneration. Biochem Biophys Res Commun 463(1-2): 102–108. https://doi.org/10.1016/j.bbrc.2015.05.032
  46. Wheeler MT, Snyder EC, Patterson MN, Swoap SJ (1999) An E-box within the MHC IIB gene is bound by MyoD and is required for gene expression in fast muscle. Am J Physiol 276(5): C1069–C1078. https://doi.org/10.1152/ajpcell.1999.276.5.C1069
  47. Hughes SM, Koishi K, Rudnicki M, Maggs AM (1997) MyoD protein is differentially accumulated in fast and slow skeletal muscle fibres and required for normal fibre type balance in rodents. Mech Dev 61(1-2): 151–163. https://doi.org/10.1016/s0925-4773(96)00631-4
  48. Seward DJ, Haney JC, Rudnicki MA, Swoap SJ (2001) bHLH transcription factor MyoD affects myosin heavy chain expression pattern in a muscle-specific fashion. Am J Physiol Cell Physiol 280(2): C408–C413. https://doi.org/10.1152/ajpcell.2001.280.2.C408
  49. Ekmark M, Rana ZA, Stewart G, Hardie DG, Gundersen K (2007) De-phosphorylation of MyoD is linking nerve-evoked activity to fast myosin heavy chain expression in rodent adult skeletal muscle. J Physiol 584 (Pt 2): 637–650. https://doi.org/10.1113/jphysiol.2007.141457
  50. Paramonova II, Vilchinskaya NA, Shenkman BS (2021) HDAC4 Is Indispensable for Reduced Slow Myosin Expression at the Early Stage of Hindlimb Unloading in Rat Soleus Muscle. Pharmaceuticals (Basel) 14(11): 1167. https://doi.org/10.3390/ph14111167
  51. Mita Y, Zhu H, Furuichi Y, Hamaguchi H, Manabe Y, Fujii NL (2022) R-spondin3 is a myokine that differentiates myoblasts to type I fibres. Sci Rep 12(1): 13020. https://doi.org/10.1038/s41598-022-16640-2

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