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Extracellular Matrix Alterations in Human Soleus Muscle under Conditions of Chronic Disorder of Consciousness

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Abstract

Critical illness myopathy (CIM) is a primary myopathy that develops in critically ill patients. Histological features of CIM include a general reduction in muscle fiber cross-sectional area and a predominant loss of the motor protein myosin in the absence of inflammatory infiltrates but with detectable cytokine activation. This study was aimed to examine the state of the soleus muscle extracellular matrix in patients with CIM caused by chronic disorders of consciousness. Incisional needle biopsies of the soleus muscle were taken from 6 patients with a chronic (≥ 2 months) disorder of consciousness, undergoing treatment at the Polenov Neurosurgical Institute (Almazov National Medical Research Center, St. Petersburg), and healthy men (control). Histological staining of soleus muscle sections in patients with CIM revealed a significantly increased collagen area that exceeded control values by 82%. Type I, III and VIa collagen mRNA levels, along with type I and III collagen content, were increased. No changes were found in fibronectin and extracellular tissue growth factor mRNA levels. However, integrin α7 mRNA levels were elevated. Our results indicate significant skeletal muscle fibrosis in CIM, requiring further studies on the signaling pathways that regulate this process.

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REFERENCES

  1. Piradov MA, Suponeva NA, Voznyuk IA, Kondratyev AN, Shchegolev AV, Belkin AA, Zaitsev OS, Pryanikov IV, Petrova MV, Ivanova NE, Gnedovskaya EV, Ryabinkina YuV, Sergeev DV, Iazeva EG, Legostaeva LA, Fufaeva EV, Petrikov SS (2020) Chronic disorders of consciousness: terminology and diagnostic criteria. The results of the first meeting of the Russian Working Group for Chronic Disorders of Consciousness. Annu Clin Exp Neurol 14(1): 5–16.https://doi.org/10.25692/ACEN.2020.1.1

    Article  Google Scholar 

  2. Larsson L, Friedrich O (2016) Critical Illness Myopathy (CIM) and Ventilator-Induced Diaphragm Muscle Dysfunction (VIDD): Acquired Myopathies Affecting Contractile Proteins. Compr Physiol 7(1): 105–112.https://doi.org/10.1002/cphy.c150054

    Article  PubMed  Google Scholar 

  3. Friedrich O, Diermeier S, Larsson L (2018) Weak by the machines: muscle motor protein dysfunction—a side effect of intensive care unit treatment. Acta Physiol (Oxf) 222: 1.https://doi.org/10.1111/apha.12885

  4. Larsson L, Li X, Edstrom L, Eriksson LI, Zackrisson H, Argentini C, Schiaffino S (2000) Acute quadriplegia and loss of muscle myosin in patients treated with nondepolarizing neuromuscular blocking agents and corticosteroids: mechanisms at the cellular and molecular levels. Crit Care Med 28(1): 34–45.https://doi.org/10.1097/00003246-200001000-00006

    Article  CAS  PubMed  Google Scholar 

  5. Derde S, Hermans G, Derese I, Guiza F, Hedstrom Y, Wouters PJ, Bruyninckx F, D’Hoore A, Larsson L, Van den Berghe G, Vanhorebeek I (2012) Muscle atrophy and preferential loss of myosin in prolonged critically ill patients. Crit Care Med 40(1): 79–89.https://doi.org/10.1097/CCM.0b013e31822d7c18

    Article  PubMed  Google Scholar 

  6. Shepherd S, Batra A, Lerner DP (2017) Review of Critical Illness Myopathy and Neuropathy. Neurohospitalist 7(1): 41–48.https://doi.org/10.1177/1941874416663279

    Article  PubMed  Google Scholar 

  7. Kress JP, Hall JB (2014) ICU-acquired weakness and recovery from critical illness. N Engl J Med 370(17): 1626–1635.https://doi.org/10.1056/NEJMra1209390

    Article  CAS  PubMed  Google Scholar 

  8. Ramsay DA, Zochodne DW, Robertson DM, Nag S, Ludwin SK (1993) A syndrome of acute severe muscle necrosis in intensive care unit patients. J Neuropathol Exp Neurol 52(4): 387–398.https://doi.org/10.1097/00005072-199307000-00006

    Article  CAS  PubMed  Google Scholar 

  9. Kalamgi RC, Larsson L (2016) Mechanical Signaling in the Pathophysiology of Critical Illness Myopathy. Front Physiol 7: 23.https://doi.org/10.3389/fphys.2016.00023

    Article  PubMed  PubMed Central  Google Scholar 

  10. Rich MM, Pinter MJ, Kraner SD, Barchi RL (1998) Loss of electrical excitability in an animal model of acute quadriplegic myopathy. Ann Neurol 43(2): 171–179.https://doi.org/10.1002/ana.410430207

    Article  CAS  PubMed  Google Scholar 

  11. Lyu Q, Wen Y, Zhang X, Addinsall AB, Cacciani N, Larsson L (2021) Multi-omics reveals age-related differences in the diaphragm response to mechanical ventilation: a pilot study. Skelet Muscle 11(1): 11.https://doi.org/10.1186/s13395-021-00267-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hermans G, De Jonghe B, Bruyninckx F, Van den Berghe G (2008) Clinical review: Critical illness polyneuropathy and myopathy. Crit Care 12(6): 238.https://doi.org/10.1186/cc7100

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kanova M, Kohout P (2022) Molecular Mechanisms Underlying Intensive Care Unit-Acquired Weakness and Sarcopenia. Int J Mol Sci 23(15): 8396.https://doi.org/10.3390/ijms23158396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Jiroutkova K, Krajcova A, Ziak J, Fric M, Waldauf P, Dzupa V, Gojda J, Nemcova-Furstova V, Kovar J, Elkalaf M, Trnka J, Duska F (2015) Mitochondrial function in skeletal muscle of patients with protracted critical illness and ICU-acquired weakness. Crit Care 19: 448.https://doi.org/10.1186/s13054-015-1160-x

    Article  PubMed  PubMed Central  Google Scholar 

  15. McClave SA, Wischmeyer PE, Miller KR, van Zanten ARH (2019) Mitochondrial Dysfunction in Critical Illness: Implications for Nutritional Therapy. Curr Nutr Rep 8(4): 363–373.https://doi.org/10.1007/s13668-019-00296-y

    Article  PubMed  Google Scholar 

  16. Zink W, Kollmar R, Schwab S (2009) Critical illness polyneuropathy and myopathy in the intensive care unit. Nat Rev Neurol 5(7): 372–379.https://doi.org/10.1038/nrneurol.2009.75

    Article  PubMed  Google Scholar 

  17. Friedrich O, Reid MB, Van den Berghe G, Vanhorebeek I, Hermans G, Rich MM, Larsson L (2015) The Sick and the Weak: Neuropathies/Myopathies in the Critically Ill. Physiol Rev 95(3): 1025–1109.https://doi.org/10.1152/physrev.00028.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Puthucheary ZA, Rawal J, McPhail M, Connolly B, Ratnayake G, Chan P, Hopkinson NS, Phadke R, Dew T, Sidhu PS, Velloso C, Seymour J, Agley CC, Selby A, Limb M, Edwards LM, Smith K, Rowlerson A, Rennie MJ, Moxham J, Harridge SD, Hart N, Montgomery HE (2013) Acute skeletal muscle wasting in critical illness. JAMA 310(15): 1591–1600.https://doi.org/10.1001/jama.2013.278481

    Article  CAS  PubMed  Google Scholar 

  19. Batt J, Herridge MS, Dos Santos CC (2019) From skeletal muscle weakness to functional outcomes following critical illness: a translational biology perspective. Thorax 74(11): 1091–1098.https://doi.org/10.1136/thoraxjnl-2016-208312

    Article  PubMed  Google Scholar 

  20. Ochala J, Gustafson AM, Diez ML, Renaud G, Li M, Aare S, Qaisar R, Banduseela VC, Hedstrom Y, Tang X, Dworkin B, Ford GC, Nair KS, Perera S, Gautel M, Larsson L (2011) Preferential skeletal muscle myosin loss in response to mechanical silencing in a novel rat intensive care unit model: underlying mechanisms. J Physiol 589(Pt 8): 2007–2026.https://doi.org/10.1113/jphysiol.2010.202044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhang W, Liu Y, Zhang H (2021) Extracellular matrix: an important regulator of cell functions and skeletal muscle development. Cell and Biosci 11(1): 65.https://doi.org/10.1186/s13578-021-00579-4

    Article  MathSciNet  CAS  Google Scholar 

  22. Csapo R, Gumpenberger M, Wessner B (2020) Skeletal Muscle Extracellular Matrix—What Do We Know About Its Composition, Regulation, and Physiological Roles? A Narrative Review. Front Physiol 11: 253.https://doi.org/10.3389/fphys.2020.00253

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gillies AR, Lieber RL (2011) Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 44(3): 318–331.https://doi.org/10.1002/mus.22094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Duance VC, Restall DJ, Beard H, Bourne FJ, Bailey AJ (1977) The location of three collagen types in skeletal muscle. FEBS Lett 79(2): 248–252.https://doi.org/10.1016/0014-5793(77)80797-7

    Article  CAS  PubMed  Google Scholar 

  25. Martin GR, Timpl R (1987) Laminin and other basement membrane components. Annu Rev Cell Biol 3: 57–85.https://doi.org/10.1146/annurev.cb.03.110187.000421

    Article  CAS  PubMed  Google Scholar 

  26. Sanes JR (1982) Laminin, fibronectin, and collagen in synaptic and extrasynaptic portions of muscle fiber basement membrane. J Cell Biol 93(2): 442–451.https://doi.org/10.1083/jcb.93.2.442

    Article  CAS  PubMed  Google Scholar 

  27. Kovanen V (2002) Intramuscular extracellular matrix: complex environment of muscle cells. Exerc Sport Sci Rev 30(1): 20–25.https://doi.org/10.1097/00003677-200201000-00005

    Article  PubMed  Google Scholar 

  28. Hurme T, Kalimo H, Sandberg M, Lehto M, Vuorio E (1991) Localization of type I and III collagen and fibronectin production in injured gastrocnemius muscle. Lab Invest 64(1): 76–84.

    CAS  PubMed  Google Scholar 

  29. Segnani C, Ippolito C, Antonioli L, Pellegrini C, Blandizzi C, Dolfi A, Bernardini N (2015) Histochemical Detection of Collagen Fibers by Sirius Red/Fast Green Is More Sensitive than van Gieson or Sirius Red Alone in Normal and Inflamed Rat Colon. PLoS One 10(12): e0144630.https://doi.org/10.1371/journal.pone.0144630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Laurent GJ (1987) Dynamic state of collagen: pathways of collagen degradation in vivo and their possible role in regulation of collagen mass. Am J Physiol 252(1 Pt 1): C1–C9.https://doi.org/10.1152/ajpcell.1987.252.1.C1

    Article  CAS  PubMed  Google Scholar 

  31. Minor RR (1980) Collagen metabolism: a comparison of diseases of collagen and diseases affecting collagen. Am J Pathol 98(1): 225–280.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Karpakka J, Vaananen K, Orava S, Takala TE (1990) The effects of preimmobilization training and immobilization on collagen synthesis in rat skeletal muscle. Int J Sports Med 11(6): 484–488.https://doi.org/10.1055/s-2007-1024842

    Article  CAS  PubMed  Google Scholar 

  33. Karpakka J, Virtanen P, Vaananen K, Orava S, Takala TE (1991) Collagen synthesis in rat skeletal muscle during immobilization and remobilization. J Appl Physiol 70(4): 1775–1780.https://doi.org/10.1152/jappl.1991.70.4.1775

    Article  CAS  PubMed  Google Scholar 

  34. Savolainen J, Vaananen K, Puranen J, Takala TE, Komulainen J, Vihko V (1988) Collagen synthesis and proteolytic activities in rat skeletal muscles: effect of cast-immobilization in the lengthened and shortened positions. Arch Phys Med Rehabil 69(11): 964–969.

    CAS  PubMed  Google Scholar 

  35. Haus JM, Carrithers JA, Carroll CC, Tesch PA, Trappe TA (2007) Contractile and connective tissue protein content of human skeletal muscle: effects of 35 and 90 days of simulated microgravity and exercise countermeasures. Am J Physiol Regul Integr Comp Physiol 293(4): R1722–R1727.https://doi.org/10.1152/ajpregu.00292.2007

    Article  CAS  PubMed  Google Scholar 

  36. Huang Y, Fan Y, Salanova M, Yang X, Sun L, Blottner D (2018) Effects of Plantar Vibration on Bone and Deep Fascia in a Rat Hindlimb Unloading Model of Disuse. Front Physiol 9: 616.https://doi.org/10.3389/fphys.2018.00616

    Article  PubMed  PubMed Central  Google Scholar 

  37. Tyganov SA, Belova SP, Turtikova OV, Vikhlyantsev IM, Nemirovskaya TL, Shenkman BS (2023) Changes in the Mechanical Properties of Fast and Slow Skeletal Muscle after 7 and 21 Days of Restricted Activity in Rats. Int J Mol Sci 24(4): 4141.https://doi.org/10.3390/ijms24044141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tyganov SA, Mochalova EP, Melnikov IY, Vikhlyantsev IM, Ulanova AD, Sharlo KA, Mirzoev TM, Shenkman BS (2021) NOS-dependent effects of plantar mechanical stimulation on mechanical characteristics and cytoskeletal proteins in rat soleus muscle during hindlimb suspension. FASEB J 35(10): e21905.https://doi.org/10.1096/fj.202100783R

    Article  CAS  PubMed  Google Scholar 

  39. Schoenrock B, Zander V, Dern S, Limper U, Mulder E, Veraksits A, Viir R, Kramer A, Stokes MJ, Salanova M, Peipsi A, Blottner D (2018) Bed Rest, Exercise Countermeasure and Reconditioning Effects on the Human Resting Muscle Tone System. Front Physiol 9: 810.https://doi.org/10.3389/fphys.2018.00810

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lemoine JK, Haus JM, Trappe SW, Trappe TA (2009) Muscle proteins during 60-day bedrest in women: impact of exercise or nutrition. Muscle Nerve 39(4): 463–471.https://doi.org/10.1002/mus.21189

    Article  CAS  PubMed  Google Scholar 

  41. Grzelkowska-Kowalczyk K (2016) The Importance of Extracellular Matrix in Skeletal Muscle Development and Function. In: Composition and Function of the Extracellular Matrix in the Human Body. IntechOpen.https://doi.org/10.5772/62230

  42. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Hirose T, Nakazato K, Song H, Ishii N (2008) TGF-beta1 and TNF-alpha are involved in the transcription of type I collagen alpha2 gene in soleus muscle atrophied by mechanical unloading. J Appl Physiol 104(1): 170–177.https://doi.org/10.1152/japplphysiol.00463.2006

    Article  CAS  PubMed  Google Scholar 

  44. Guilhot C, Fovet T, Delobel P, Dargegen M, Jasmin BJ, Brioche T, Chopard A, Py G (2022) Severe Muscle Deconditioning Triggers Early Extracellular Matrix Remodeling and Resident Stem Cell Differentiation into Adipocytes in Healthy Men. Int J Mol Sci 23(10): 5489.https://doi.org/10.3390/ijms23105489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ramazani Y, Knops N, Elmonem MA, Nguyen TQ, Arcolino FO, van den Heuvel L, Levtchenko E, Kuypers D, Goldschmeding R (2018) Connective tissue growth factor (CTGF) from basics to clinics. Matrix Biol 68: 44–66.https://doi.org/10.1016/j.matbio.2018.03.007

    Article  CAS  PubMed  Google Scholar 

  46. Leask A, Parapuram SK, Shi-Wen X, Abraham DJ (2009) Connective tissue growth factor (CTGF, CCN2) gene regulation: a potent clinical bio-marker of fibroproliferative disease? J Cell Commun Signal 3(2): 89–94.https://doi.org/10.1007/s12079-009-0037-7

    Article  PubMed  PubMed Central  Google Scholar 

  47. Rebolledo DL, Lipson KE, Brandan E (2021) Driving fibrosis in neuromuscular diseases: Role and regulation of Connective tissue growth factor (CCN2/CTGF). Matrix Biol Plus 6: 11: 100059.https://doi.org/10.1016/j.mbplus.2021.100059

    Article  CAS  Google Scholar 

  48. Henderson CA, Gomez CG, Novak SM, Mi-Mi L, Gregorio CC (2017) Overview of the Muscle Cytoskeleton. Compr Physiol 7(3): 891–944.https://doi.org/10.1002/cphy.c160033

    Article  PubMed  PubMed Central  Google Scholar 

  49. Sun M, Opavsky MA, Stewart DJ, Rabinovitch M, Dawood F, Wen WH, Liu PP (2003) Temporal response and localization of integrins beta1 and beta3 in the heart after myocardial infarction: regulation by cytokines. Circulation 107(7): 1046–1052.https://doi.org/10.1161/01.cir.0000051363.86009.3c

    Article  CAS  PubMed  Google Scholar 

  50. Docheva D, Popov C, Alberton P, Aszodi A (2014) Integrin signaling in skeletal development and function. Birth Defects Res C Embryo Today 102(1): 13–36.https://doi.org/10.1002/bdrc.21059

    Article  CAS  PubMed  Google Scholar 

  51. Zhang H, Liu Y, Li C, Zhang W (2022) ITGbeta6 Facilitates Skeletal Muscle Development by Maintaining the Properties and Cytoskeleton Stability of Satellite Cells. Life (Basel) 12(7): 926.https://doi.org/10.3390/life12070926

  52. McClure MJ, Ramey AN, Rashid M, Boyan BD, Schwartz Z (2019) Integrin-alpha7 signaling regulates connexin 43, M-cadherin, and myoblast fusion. Am J Physiol Cell Physiol 316(6): C876–C887.https://doi.org/10.1152/ajpcell.00282.2018

    Article  CAS  PubMed  Google Scholar 

  53. Bayer ML, Svensson RB, Schjerling P, Williams AS, Wasserman DH, Kjaer M (2020) Influence of the integrin alpha-1 subunit and its relationship with high-fat diet upon extracellular matrix synthesis in skeletal muscle and tendon. Cell and Tissue Res 381(1): 177–187.https://doi.org/10.1007/s00441-020-03184-y

    Article  CAS  Google Scholar 

  54. Savolainen J, Myllyla V, Myllyla R, Vihko V, Vaananen K, Takala TE (1988) Effects of denervation and immobilization on collagen synthesis in rat skeletal muscle and tendon. Am J Physiol 254(6 Pt 2): R897–R902.https://doi.org/10.1152/ajpregu.1988.254.6.R897

    Article  CAS  PubMed  Google Scholar 

  55. Edom-Vovard F, Schuler B, Bonnin MA, Teillet MA, Duprez D (2002) Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Dev Biol 247(2): 351–366.https://doi.org/10.1006/dbio.2002.0707

    Article  CAS  PubMed  Google Scholar 

  56. Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84(2): 649–698.https://doi.org/10.1152/physrev.00031.2003

    Article  CAS  PubMed  Google Scholar 

  57. Tyganov SA, Zaripova KA, Turtikova OV, Skiteva EN, Belova SP, Zabrodskaya YM, Kondratiev SA, Kondratieva EA, Kondratiev AN, Shenkman BS (2023) Desmin degradation in the skeletal muscle of patients with chronic critical illness. J Evol Biochem Physiol 59(6): 2381–2389.

    Article  CAS  Google Scholar 

  58. Kragstrup TW, Kjaer M, Mackey AL (2011) Structural, biochemical, cellular, and functional changes in skeletal muscle extracellular matrix with aging. Scand J Med Sci in Sports 21(6): 749–757.https://doi.org/10.1111/j.1600-0838.2011.01377.x

    Article  CAS  Google Scholar 

  59. Csapo R, Malis V, Sinha U, Du J, Sinha S (2014) Age-associated differences in triceps surae muscle composition and strength—an MRI-based cross-sectional comparison of contractile, adipose and connective tissue. BMC Musculoskelet Disord 15: 209.https://doi.org/10.1186/1471-2474-15-209

    Article  PubMed  PubMed Central  Google Scholar 

  60. Haus JM, Carrithers JA, Trappe SW, Trappe TA (2007) Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J Appl Physiol 103(6): 2068–2076.https://doi.org/10.1152/japplphysiol.00670.2007

    Article  CAS  PubMed  Google Scholar 

  61. Gumpenberger M, Wessner B, Graf A, Narici MV, Fink C, Braun S, Hoser C, Blazevich AJ, Csapo R (2020) Remodeling the Skeletal Muscle Extracellular Matrix in Older Age-Effects of Acute Exercise Stimuli on Gene Expression. Int J Mol Sci 21(19): 7089.https://doi.org/10.3390/ijms21197089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wood LK, Kayupov E, Gumucio JP, Mendias CL, Claflin DR, Brooks SV (2014) Intrinsic stiffness of extracellular matrix increases with age in skeletal muscles of mice. J Appl Physiol 117(4): 363–369.https://doi.org/10.1152/japplphysiol.00256.2014

    Article  PubMed  PubMed Central  Google Scholar 

  63. Silver FH, DeVore D, Siperko LM (2003) Invited Review: Role of mechanophysiology in aging of ECM: effects of changes in mechanochemical transduction. J Appl Physiol 95(5): 2134–2141.https://doi.org/10.1152/japplphysiol.00429.2003

    Article  PubMed  Google Scholar 

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ACKNOWLEDGMENTS

The authors are deeply grateful to E.M. Lednev and T.F. Vepkhvadze for conducting needle biopsy, as well as K.K. Kukanov and N.E. Voinov for biopsy sampling.

Funding

This work was supported by the Russian Science Foundation (project No. 22-25-00615). No other grants were obtained to carry out or supervise this particular research.

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Contributions

Conceptualization and experimental design (B.S.Sh., A.N.K., Yu.M.Z., S.A.K.), muscle biopsy (S.A.K., E.N.S.), data collection (S.A.T., E.N.S., K.A.Z., O.N.T.), data processing (S.A.T., K.A.Z., O.N.T.), writing and editing the manuscript (S.A.T., B.S.Sh., E.A.K., S.A.K., Yu.M.Z.).

Corresponding author

Correspondence to S. A. Tyganov.

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ETHICS APPROVAL

All studies were conducted in accordance with the principles of biomedical ethics set forth in the 1964 Declaration of Helsinki and its subsequent amendments. They were also approved by the local Ethics Committee of the Almazov National Medical Research Center, Minutes No. 1411-20 of November 16, 2020. Muscle biopsy sampling was performed for diagnostic purposes with the written consent of the patients’ legal representatives.

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The authors declare that they have no conflict of interest.

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Translated by A. Polyanovsky

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Zaripova, K.A., Tyganov, S.A., Turtikova, O.V. et al. Extracellular Matrix Alterations in Human Soleus Muscle under Conditions of Chronic Disorder of Consciousness. J Evol Biochem Phys 60, 432–442 (2024). https://doi.org/10.1134/S0022093024010332

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