Download PDF
J Neurol Surg A Cent Eur Neurosurg 2023; 84(02): 116-122
DOI: 10.1055/s-0041-1731750
Original Article

Matrix Metalloproteinase-9 is Involved in the Fibrotic Process in Denervated Muscles after Sciatic Nerve Trauma and Recovery

Oleksii Goncharuk
1   Department of Neurosurgery, Bogomolets National Medical University, Kyiv, Ukraine
,
Serhii Savosko 
2   Department of Histology and Embryology, Bogomolets National Medical University, Kyiv, Ukraine
,
Artem Tykhomyrov
3   Department of Neurosurgery, Palladin Institute of Biochemistry of the National Academy of Sciences of Ukraine (NASU), Kyiv, Ukraine
,
Mykhailo Guzyk
3   Department of Neurosurgery, Palladin Institute of Biochemistry of the National Academy of Sciences of Ukraine (NASU), Kyiv, Ukraine
,
Volodymyr Medvediev
1   Department of Neurosurgery, Bogomolets National Medical University, Kyiv, Ukraine
,
Vitaliy Tsymbaliuk
1   Department of Neurosurgery, Bogomolets National Medical University, Kyiv, Ukraine
,
Yuri Chaikovsky
2   Department of Histology and Embryology, Bogomolets National Medical University, Kyiv, Ukraine
› Author Affiliations
› Further Information
Also available at
    Permissions and Reprints

Abstract

Fibrosis of the injured muscles is a problem of recovery from trauma and denervation. The aim of the work was to investigate the interconnection of matrix metalloproteinase-9 (ММР-9) activity in denervated muscles with fibrosis and to estimate its role in nerve restoration by the epineurial suture, fibrin-based glue, and polyethylene glycol hydrogel. The activity of matrix metalloproteinases was estimated by gelatin zymography. Collagen density in muscles was determined histochemically. An increased level of the active MMP-9 is associated with the fibrous changes in the denervated skeletal muscles and after an epineurial suture. The use of fibrin glue and polyethylene glycol hydrogel resulted in a lower level of collagen and ММР-9 activity, which may be a therapeutic target in the treatment of neuromuscular lesions, and has value in fibrosis analysis following microsurgical intervention for peripheral nerve reconstruction.

Keywords

MMP-9 - muscle atrophy - sciatic nerve - trauma - fibrosis


Publication History

Received: 19 April 2020

Accepted: 29 December 2020

Article published online:
08 September 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Kurzepa J, El-Demerdash FM, Castellazzi M. Matrix metalloproteinases as a pleiotropic biomarker in medicine and biology. Dis Markers 2016; 2016: 9275204
    CrossrefPubMedGoogle Scholar
  • 2 Wang J, Liu Y, Zhang L. et al. Effects of increased matrix metalloproteinase-9 expression on skeletal muscle fibrosis in prolonged alcoholic myopathies of rats. Mol Med Rep 2012; 5 (01) 60-65
    PubMedGoogle Scholar
  • 3 Jones JI, Nguyen TT, Peng Z, Chang M. Targeting MMP-9 in diabetic foot ulcers. Pharmaceuticals (Basel) 2019; 12 (02) 79
    CrossrefPubMedGoogle Scholar
  • 4 Hardy E, Fernandez-Patron C. Destroy to rebuild: the connection between bone tissue remodeling and matrix metalloproteinases. Front Physiol 2020; 11: 47
    CrossrefPubMedGoogle Scholar
  • 5 Li X, Zhao Y, Chen C. et al. Critical role of matrix metalloproteinase 14 in adipose tissue remodeling during obesity. Mol Cell Biol 2020; 40 (08) e00564-e19
    PubMedGoogle Scholar
  • 6 Georgiev GP, Landzhov B, Kotov G, Slavchev SA, Iliev A. Matrix metalloproteinase-2 and -9 expression in the epiligament of the medial collateral and anterior cruciate ligament in human knees: a comparative study. Cureus 2018; 10 (11) e3550
    PubMedGoogle Scholar
  • 7 Chen X, Li Y. Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adhes Migr 2009; 3 (04) 337-341
    CrossrefPubMedGoogle Scholar
  • 8 Gargioli C, Coletta M, De Grandis F, Cannata SM, Cossu G. PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat Med 2008; 14 (09) 973-978
    CrossrefPubMedGoogle Scholar
  • 9 Dahiya S, Bhatnagar S, Hindi SM. et al. Elevated levels of active matrix metalloproteinase-9 cause hypertrophy in skeletal muscle of normal and dystrophin-deficient mdx mice. Hum Mol Genet 2011; 20 (22) 4345-4359
    CrossrefPubMedGoogle Scholar
  • 10 Kamieniak P, Bielewicz J, Kurzepa J, Daniluk B, Kocot J, Trojanowski T. The impact of changes in serum levels of metalloproteinase-2 and metalloproteinase-9 on pain perception in patients with disc herniation before and after surgery. J Pain Res 2019; 12: 1457-1464
    CrossrefPubMedGoogle Scholar
  • 11 Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007; 8 (03) 221-233
    CrossrefPubMedGoogle Scholar
  • 12 Siebert H, Dippel N, Mäder M, Weber F, Brück W. Matrix metalloproteinase expression and inhibition after sciatic nerve axotomy. J Neuropathol Exp Neurol 2001; 60 (01) 85-93
    CrossrefPubMedGoogle Scholar
  • 13 Kim J, Lee J. Matrix metalloproteinase and tissue inhibitor of metalloproteinase responses to muscle damage after eccentric exercise. J Exerc Rehabil 2016; 12 (04) 260-265
    CrossrefPubMedGoogle Scholar
  • 14 Kherif S, Dehaupas M, Lafuma C, Fardeau M, Alameddine HS. Matrix metalloproteinases MMP-2 and MMP-9 in denervated muscle and injured nerve. Neuropathol Appl Neurobiol 1998; 24 (04) 309-319
    CrossrefPubMedGoogle Scholar
  • 15 Cuzner ML, Opdenakker G. Plasminogen activators and matrix metalloproteases, mediators of extracellular proteolysis in inflammatory demyelination of the central nervous system. J Neuroimmunol 1999; 94 (1–2): 1-14
    CrossrefPubMedGoogle Scholar
  • 16 Isaacs J, Klumb I, McDaniel C. Preliminary investigation of a polyethylene glycol hydrogel “nerve glue.”. J Brachial Plex Peripher Nerve Inj 2009; 4 (16) 16
    PubMedGoogle Scholar
  • 17 Amoozgar Z, Rickett T, Park J, Tuchek C, Shi R, Yeo Y. Semi-interpenetrating network of polyethylene glycol and photocrosslinkable chitosan as an in-situ-forming nerve adhesive. Acta Biomater 2012; 8 (05) 1849-1858
    CrossrefPubMedGoogle Scholar
  • 18 Lin KL, Yang DY, Chu IM. et al. DuraSeal as a ligature in the anastomosis of rat sciatic nerve gap injury. J Surg Res 2010; 161 (01) 101-110
    CrossrefPubMedGoogle Scholar
  • 19 Sameem M, Wood TJ, Bain JR. A systematic review on the use of fibrin glue for peripheral nerve repair. Plast Reconstr Surg 2011; 127 (06) 2381-2390
    CrossrefPubMedGoogle Scholar
  • 20 Oliver GW, Stettler-Stevenson WG, Kleiner DE. Zymography, casein zymography, and reverse zymography: activity assays for proteases and their inhibitors. In: Handbook of Proteolytic Enzymes. San Diego, CA: Academic Press; 1999: 61-76
    Google Scholar
  • 21 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193 (01) 265-275
    CrossrefPubMedGoogle Scholar
  • 22 Wegner KA, Keikhosravi A, Eliceiri KW, Vezina CM. Fluorescence of Picrosirius red multiplexed with immunohistochemistry for the quantitative assessment of collagen in tissue sections. J Histochem Cytochem 2017; 65 (08) 479-490
    CrossrefPubMedGoogle Scholar
  • 23 Kumar A, Bhatnagar S, Kumar A. Matrix metalloproteinase inhibitor batimastat alleviates pathology and improves skeletal muscle function in dystrophin-deficient mdx mice. Am J Pathol 2010; 177 (01) 248-260
    CrossrefPubMedGoogle Scholar
  • 24 Zuo J, Hernandez YJ, Muir D. Chondroitin sulfate proteoglycan with neurite-inhibiting activity is up-regulated following peripheral nerve injury. J Neurobiol 1998; a 34 (01) 41-54
    CrossrefPubMedGoogle Scholar
  • 25 Wang W, Pan H, Murray K, Jefferson BS, Li Y. Matrix metalloproteinase-1 promotes muscle cell migration and differentiation. Am J Pathol 2009; 174 (02) 541-549
    CrossrefPubMedGoogle Scholar
  • 26 Tatsumi R. Mechano-biology of skeletal muscle hypertrophy and regeneration: possible mechanism of stretch-induced activation of resident myogenic stem cells. Anim Sci J 2010; 81 (01) 11-20
    CrossrefPubMedGoogle Scholar
  • 27 Mu X, Urso ML, Murray K, Fu F, Li Y. Relaxin regulates MMP expression and promotes satellite cell mobilization during muscle healing in both young and aged mice. Am J Pathol 2010; 177 (05) 2399-2410
    CrossrefPubMedGoogle Scholar
  • 28 Zimowska M, Olszynski KH, Swierczynska M, Streminska W, Ciemerych MA. Decrease of MMP-9 activity improves soleus muscle regeneration. Tissue Eng Part A 2012; 18 (11-12): 1183-1192
    CrossrefPubMedGoogle Scholar
  • 29 Hindi SM, Shin J, Ogura Y, Li H, Kumar A. Matrix metalloproteinase-9 inhibition improves proliferation and engraftment of myogenic cells in dystrophic muscle of mdx mice. PLoS One 2013; 8 (08) e72121
    CrossrefPubMedGoogle Scholar
  • 30 Obradović H, Krstić J, Kukolj T. et al. Doxycycline inhibits IL-17-stimulated MMP-9 expression by downregulating ERK1/2 activation: implications in myogenic differentiation. Mediators Inflamm 2016; 2016: 2939658
    CrossrefPubMedGoogle Scholar
  • 31 Krekoski CA, Neubauer D, Graham JB, Muir D. Metalloproteinase-dependent predegeneration in vitro enhances axonal regeneration within acellular peripheral nerve grafts. J Neurosci 2002; 22 (23) 10408-10415
    CrossrefPubMedGoogle Scholar
  • 32 Alameddine HS, Morgan JE. Matrix metalloproteinases and tissue inhibitor of metalloproteinases in inflammation and fibrosis of skeletal muscles. J Neuromuscul Dis 2016; 3 (04) 455-473
    CrossrefPubMedGoogle Scholar
  • 33 La Fleur M, Underwood JL, Rappolee DA, Werb Z. Basement membrane and repair of injury to peripheral nerve: defining a potential role for macrophages, matrix metalloproteinases, and tissue inhibitor of metalloproteinases-1. J Exp Med 1996; 184 (06) 2311-2326
    CrossrefPubMedGoogle Scholar
  • 34 Liu X, Lee D, Natsuhara K, Manzano G, Kim HT. Role of MMP-2 in Denervation-Induced Skeletal Muscle Atrophy. Poster No. 1490 presented at the 55th Annual Meeting of the Orthopaedic Research Society, Las Vegas, Nevada, February 22–25, 2009
    PubMedGoogle Scholar
  • 35 Kim Y, Remacle AG, Chernov AV. et al. The MMP-9/TIMP-1 axis controls the status of differentiation and function of myelin-forming Schwann cells in nerve regeneration. PLoS One 2012; 7 (03) e33664
    CrossrefPubMedGoogle Scholar
  • 36 Yamada M, Sankoda Y, Tatsumi R. et al. Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner. Int J Biochem Cell Biol 2008; 40 (10) 2183-2191
    CrossrefPubMedGoogle Scholar
  • 37 Mierzejewski B, Archacka K, Grabowska I, Florkowska A, Ciemerych MA, Brzoska E. Human and mouse skeletal muscle stem and progenitor cells in health and disease. Semin Cell Dev Biol 2020; 104: 93-104
    CrossrefPubMedGoogle Scholar
  • 38 Remacle AG, Hullugundi SK, Dolkas J. et al. Acute- and late-phase matrix metalloproteinase (MMP)-9 activity is comparable in female and male rats after peripheral nerve injury. J Neuroinflammation 2018; 15 (01) 89
    CrossrefPubMedGoogle Scholar
  • 39 Souza MV, Leite RD, Souza Lino AD. et al. Resistance training improves body composition and increases matrix metalloproteinase 2 activity in biceps and gastrocnemius muscles of diet-induced obese rats. Clinics (São Paulo) 2014; 69 (04) 265-270
    CrossrefPubMedGoogle Scholar
  • 40 Zhang H, Chang M, Hansen CN, Basso DM, Noble-Haeusslein LJ. Role of matrix metalloproteinases and therapeutic benefits of their inhibition in spinal cord injury. Neurotherapeutics 2011; 8 (02) 206-220
    CrossrefPubMedGoogle Scholar
  • 41 de Sousa Neto IV, Durigan JLQ, Guzzoni V. et al. Effects of resistance training on matrix metalloproteinase activity in skeletal muscles and blood circulation during aging. Front Physiol 2018; 9: 190
    CrossrefPubMedGoogle Scholar
  • 42 Kragstrup TW, Kjaer M, Mackey AL. Structural, biochemical, cellular, and functional changes in skeletal muscle extracellular matrix with aging. Scand J Med Sci Sports 2011; 21 (06) 749-757
    CrossrefPubMedGoogle Scholar
  • 43 Zotz TG, Capriglione LG, Zotz R. et al. Acute effects of stretching exercise on the soleus muscle of female aged rats. Acta Histochem 2016; 118 (01) 1-9
    CrossrefPubMedGoogle Scholar