593
Views
2
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Graphene Oxide Decreases Pro-Inflammatory Proteins Production in Skeletal Muscle Cells Exposed to SARS-CoV-2 Spike Protein

, , , ORCID Icon, ORCID Icon, ORCID Icon, , , ORCID Icon & show all
Pages 1-18 | Received 29 Sep 2022, Accepted 21 Dec 2022, Published online: 19 Jan 2023

References

  • Gonzalez A, Orozco-Aguilar J, Achiardi O, Simon F, Cabello-Verrugio C. SARS-CoV-2/renin-angiotensin system: deciphering the clues for a couple with potentially harmful effects on skeletal muscle. Int J Mol Sci. 2020;21(21):7904. doi:10.3390/ijms21217904
  • Rabbani G, Ahn SN. Review: roles of human serum albumin in prediction, diagnoses and treatment of COVID-19. Int J Biol Macromol. 2021;193(Pt A):948–955. doi:10.1016/j.ijbiomac.2021.10.095
  • Pum A, Ennemoser M, Adage T, Kungl AJ. Cytokines and chemokines in SARS-CoV-2 infections-therapeutic strategies targeting cytokine storm. Biomolecules. 2021;11(1):91. doi:10.3390/biom11010091
  • Yang L, Xie X, Tu Z, Fu J, Xu D, Zhou Y. The signal pathways and treatment of cytokine storm in COVID-19. Signal Transduct Target Ther. 2021;6(1):255. doi:10.1038/s41392-021-00679-0
  • Chen Y, Wang J, Liu C, et al. IP-10 and MCP-1 as biomarkers associated with disease severity of COVID-19. Mol Med. 2020;26(1):97. doi:10.1186/s10020-020-00230-x
  • Long B, Carius BM, Chavez S, et al. Clinical update on COVID-19 for the emergency clinician: presentation and evaluation. Am J Emerg Med. 2022;54:46–57.
  • Meacci E, Pierucci F, Garcia-Gil M. Skeletal muscle and COVID-19: the potential involvement of bioactive sphingolipids. Biomedicines. 2022;10(5):117.
  • Disser NP, De Micheli AJ, Schonk MM, et al. Musculoskeletal consequences of COVID-19. J Bone Joint Surg Am. 2020;102(14):1197–1204.
  • Suh J, Amato AA. Neuromuscular complications of coronavirus disease-19. Curr Opin Neurol. 2021;34(5):669–674.
  • Hikmet F, Méar L, Edvinsson Å, Micke P, Uhlén M, Lindskog C. The protein expression profile of ACE2 in human tissues. Mol Syst Biol. 2020;16(7):e9610. doi:10.15252/msb.20209610
  • Riquelme C, Acuña MJ, Torrejón J, et al. ACE2 is augmented in dystrophic skeletal muscle and plays a role in decreasing associated fibrosis. PLoS One. 2014;9(4):e93449. doi:10.1371/journal.pone.0093449
  • Perez-Valera M, Martinez-Canton M, Gallego-Selles A, et al. Angiotensin-converting enzyme 2 (SARS-CoV-2 receptor) expression in human skeletal muscle. Scand J Med Sci Sports. 2021;31(12):2249–2258. doi:10.1111/sms.14061
  • Yamamoto K, Takeshita H, Rakugi H. ACE2, angiotensin 1-7 and skeletal muscle: review in the era of COVID-19. Clin Sci. 2020;134(22):3047–3062. doi:10.1042/CS20200486
  • Alsaad KO, Hajeer AH, Al Balwi M, et al. Histopathology of Middle East respiratory syndrome coronovirus (MERS-CoV) infection - clinicopathological and ultrastructural study. Histopathology. 2018;72(3):516–524. doi:10.1111/his.13379
  • Gallagher D, Visser M, De Meersman RE, et al. Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol. 1997;83(1):229–239. doi:10.1152/jappl.1997.83.1.229
  • Frontera WR, Ochala J. Skeletal muscle: a brief review of structure and function. Calcif Tissue Int. 2015;96(3):183–195. doi:10.1007/s00223-014-9915-y
  • Paliwal VK, Garg RK, Gupta A, Tejan N. Neuromuscular presentations in patients with COVID-19. Neurol Sci. 2020;41(11):3039–3056. doi:10.1007/s10072-020-04708-8
  • Schniepp HC, Li JL, McAllister MJ, et al. Functionalized single graphene sheets derived from splitting graphite oxide. J Phys Chem B. 2006;110(17):8535–8539. doi:10.1021/jp060936f
  • Maiolo D, Del Pino P, Metrangolo P, Parak WJ, Baldelli Bombelli F. Nanomedicine delivery: does protein Corona route to the target or off road? Nanomedicine. 2015;10(21):3231–3247. doi:10.2217/nnm.15.163
  • Kurantowicz N, Sawosz E, Halik G, et al. Toxicity studies of six types of carbon nanoparticles in a chicken-embryo model. Int J Nanomedicine. 2017;12:2887–2898. doi:10.2147/IJN.S131960
  • Hu W, Peng C, Lv M, et al. Protein Corona-mediated mitigation of cytotoxicity of graphene oxide. ACS Nano. 2011;5(5):3693–3700. doi:10.1021/nn200021j
  • Bałaban J, Wierzbicki M, Zielińska M, et al. Effects of graphene oxide nanofilm and chicken embryo muscle extract on muscle progenitor cell differentiation and contraction. Molecules. 2020;25(8). doi:10.3390/molecules25081991
  • Bałaban J, Zielińska M, Wierzbicki M, et al. Effect of muscle extract and graphene oxide on muscle structure of chicken embryos. Animals. 2021;11(12):1–18. doi:10.3390/ani11123467
  • Kurantowicz N, Strojny B, Sawosz E, et al. Biodistribution of a high dose of diamond, graphite, and graphene oxide nanoparticles after multiple intraperitoneal injections in rats. Nanoscale Res Lett. 2015;10(1):398. doi:10.1186/s11671-015-1107-9
  • Strojny B, Kurantowicz N, Sawosz E, et al. Long term influence of carbon nanoparticles on health and liver status in rats. PLoS One. 2015;10(12):1–19. doi:10.1371/journal.pone.0144821
  • Zielińska-Górska M, Sawosz E, Sosnowska M, et al. Molecular biocompatibility of a silver nanoparticle complex with graphene oxide to human skin in a 3D epidermis in vitro model. Pharm. 2022;14(7):116.
  • Jaworski S, Strojny-Cieślak B, Wierzbicki M, et al. Comparison of the toxicity of pristine graphene and graphene oxide, using four biological models. Mater. 2021;14(15):4250. doi:10.3390/ma14154250
  • Tan GW, Kondo T, Imamura K, et al. Simple derivation of skeletal muscle from human pluripotent stem cells using temperature-sensitive Sendai virus vector. J Cell Mol Med. 2021;25(20):9586–9596. doi:10.1111/jcmm.16899
  • Motta-Santos D, Dos Santos RAS, Oliveira M, et al. Effects of ACE2 deficiency on physical performance and physiological adaptations of cardiac and skeletal muscle to exercise. Hypertens Res. 2016;39(7):506–512. doi:10.1038/hr.2016.28
  • He Q, Sudibya HG, Yin Z, et al. Centimeter-long and large-scale micropatterns of reduced graphene oxide films: fabrication and sensing applications. ACS Nano. 2010;4:3201. doi:10.1021/nn100780v
  • Ferrandi PJ, Alway SE, Mohamed JS. The interaction between SARS-CoV-2 and ACE2 may have consequences for skeletal muscle viral susceptibility and myopathies. J Appl Physiol. 2020;129(4):864–867. doi:10.1152/japplphysiol.00321.2020
  • Ali AM, Kunugi H. Skeletal muscle damage in COVID-19: a call for action. Medicina. 2021;57(4):372. doi:10.3390/medicina57040372
  • Piotrowicz K, Gąsowski J, Michel JP, Veronese N. Post-COVID-19 acute sarcopenia: physiopathology and management. Aging Clin Exp Res. 2021;33(10):2887–2898. doi:10.1007/s40520-021-01942-8
  • Ramani SL, Samet J, Franz CK, et al. Musculoskeletal involvement of COVID-19: review of imaging. Skeletal Radiol. 2021;50(9):1763–1773. doi:10.1007/s00256-021-03734-7
  • Caress JB, Castoro RJ, Simmons Z, et al. COVID-19-associated Guillain-Barré syndrome: the early pandemic experience. Muscle Nerve. 2020;62(4):485–491. doi:10.1002/mus.27024
  • Rabbani G, Ahn SN, Kwon H, Ahmad K, Choi I. Penta-peptide ATN-161 based neutralization mechanism of SARS-CoV-2 spike protein. Biochem Biophys Reports. 2021;28:101170. doi:10.1016/j.bbrep.2021.101170
  • Angeli F, Reboldi G, Trapasso M, Zappa M, Spanevello A, Verdecchia P. COVID-19, vaccines and deficiency of ACE(2) and other angiotensinases. Closing the loop on the “Spike effect”. Eur J Intern Med. 2022;103:23–28. doi:10.1016/j.ejim.2022.06.015
  • Seixas ML, Mitre LP, Shams S, et al. Unraveling muscle impairment associated with COVID-19 and the role of 3D culture in its investigation. Front Nutr. 2022;9:825629. doi:10.3389/fnut.2022.825629
  • Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. doi:10.1016/S0140-6736(20)30183-5
  • Bickel M. The role of interleukin-8 in inflammation and mechanisms of regulation. J Periodontol. 1993;64(5 Suppl):456–460.
  • De Rossi M, Bernasconi P, Baggi F, de Waal Malefyt R, Mantegazza R. Cytokines and chemokines are both expressed by human myoblasts: possible relevance for the immune pathogenesis of muscle inflammation. Int Immunol. 2000;12(9):1329–1335. doi:10.1093/intimm/12.9.1329
  • Akerstrom T, Steensberg A, Keller P, Keller C, Penkowa M, Pedersen BK. Exercise induces interleukin-8 expression in human skeletal muscle. J Physiol. 2005;563(2):507–516. doi:10.1113/jphysiol.2004.077610
  • Heidemann J, Ogawa H, Dwinell MB, et al. Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2. J Biol Chem. 2003;278(10):8508–8515. doi:10.1074/jbc.M208231200
  • Addison CL, Daniel TO, Burdick MD, et al. The CXC chemokine receptor 2, CXCR2, is the putative receptor for ELR + CXC chemokine-induced angiogenic activity. J Immunol. 2000;165(9):5269–5277. doi:10.4049/jimmunol.165.9.5269
  • van der Meer IM, de Maat MPM, Bots ML, et al. Inflammatory mediators and cell adhesion molecules as indicators of severity of atherosclerosis: the Rotterdam study. Arterioscler Thromb Vasc Biol. 2002;22(5):838–842. doi:10.1161/01.ATV.0000016249.96529.B8
  • Xiang S, Dong N, Liu J, et al. Inhibitory effects of suppressor of cytokine signaling 3 on inflammatory cytokine expression and migration and proliferation of IL-6/IFN-γ-induced vascular smooth muscle cells. J Huazhong Univ Sci Technol. 2013;33(5):615–622. doi:10.1007/s11596-013-1168-x
  • Li YS, Shyy YJ, Wright JG, Valente AJ, Cornhill JF, Kolattukudy PE. The expression of monocyte chemotactic protein (MCP-1) in human vascular endothelium in vitro and in vivo. Mol Cell Biochem. 1993;126(1):61–68. doi:10.1007/BF01772208
  • Tang N, Li D, Wang X, Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost. 2020;18(4):844–847. doi:10.1111/jth.14768
  • Perico L, Benigni A, Casiraghi F, Ng LFP, Renia L, Remuzzi G. Immunity, endothelial injury and complement-induced coagulopathy in COVID-19. Nat Rev Nephrol. 2021;17(1):46–64. doi:10.1038/s41581-020-00357-4
  • Evers-van Gogh IJA, Oteng AB, Alex S, et al. Muscle-specific inflammation induced by MCP-1 overexpression does not affect whole-body insulin sensitivity in mice. Diabetologia. 2016;59(3):624–633. doi:10.1007/s00125-015-3822-2
  • Smith-Norowitz TA, Loeffler J, Norowitz YM, Kohlhoff S. Intracellular adhesion molecule-1 (ICAM-1) levels in convalescent COVID-19 serum: a case report. Ann Clin Lab Sci. 2021;51(5):730–734.
  • Liu H, Tan J, Liu J, Feng H, Pan D. Altered mast cell activity in response to rhinovirus infection provides novel insight into asthma. J Asthma. 2020;57(5):459–467.
  • Dearth CL, Goh Q, Marino JS, et al. Skeletal muscle cells express ICAM-1 after muscle overload and ICAM-1 contributes to the ensuing hypertrophic response. PLoS One. 2013;8(3):e58486. doi:10.1371/journal.pone.0058486
  • Della Gatta PA, Garnham AP, Peake JM, Cameron-Smith D. Effect of exercise training on skeletal muscle cytokine expression in the elderly. Brain Behav Immun. 2014;39:80–86.
  • Palazzetti S, Richard MJ, Favier A, Margaritis I. Overloaded training increases exercise-induced oxidative stress and damage. Can J Appl Physiol. 2003;28(4):588–604.
  • Ebihara T, Matsumoto H, Matsubara T, et al. Resistin associated with cytokines and endothelial cell adhesion molecules is related to worse outcome in COVID-19. Front Immunol. 2022;13:830061.
  • Ren J, Braileanu G, Gorgojo P, et al. On the biocompatibility of graphene oxide towards vascular smooth muscle cells. Nanotechnology. 2020;32(5):55101.
  • Cicuéndez M, Casarrubios L, Barroca N, et al. Benefits in the macrophage response due to graphene oxide reduction by thermal treatment. Int J Mol Sci. 2021;22:13.
  • Wen KP, Chen YC, Chuang CH, Chang HY, Lee CY, Tai NH. Accumulation and toxicity of intravenously-injected functionalized graphene oxide in mice. J Appl Toxicol. 2015;35(10):1211–1218.
  • Takahashi Y, Hayakawa A, Sano R, et al. Histone deacetylase inhibitors suppress ACE2 and ABO simultaneously, suggesting a preventive potential against COVID-19. Sci Rep. 2021;11(1):3379.
  • Shi TT, Yang FY, Liu C, et al. Angiotensin-converting enzyme 2 regulates mitochondrial function in pancreatic β-cells. Biochem Biophys Res Commun. 2018;495(1):860–866.
  • Graham KA, Kulawiec M, Owens KM, et al. NADPH oxidase 4 is an oncoprotein localized to mitochondria. Cancer Biol Ther. 2010;10(3):223–231.
  • Mitsopoulos P, Lapohos O, Weraarpachai W, Antonicka H, Chang YH, Madrenas J. Stomatin-like protein 2 deficiency results in impaired mitochondrial translation. PLoS One. 2017;12:e0179967.
  • Kitada M, Xu J, Ogura Y, Monno I, Koya D. Manganese superoxide dismutase dysfunction and the pathogenesis of kidney disease. Front Physiol. 2020;11:755.
  • Warner BB, Stuart L, Gebb S, Wispé JR. Redox regulation of manganese superoxide dismutase. Am J Physiol. 1996;271(1 Pt 1):L150–8.
  • Kim SH, Lee JY, Kim J. Characterization of a wide range base-damage-endonuclease activity of mammalian rpS3. Biochem Biophys Res Commun. 2005;328(4):962–967.
  • Kim KH, Rodriguez AM, Carrico PM, Melendez JA. Potential mechanisms for the inhibition of tumor cell growth by manganese superoxide dismutase. Antioxid Redox Signal. 2001;3(3):361–373.
  • Fokunang C. Overview of non-steroidal anti-inflammatory drugs (nsaids) in resource limited countries. MOJ Toxicol. 2018;4(1):5–13.
  • Weinheimer EM, Jemiolo B, Carroll CC, et al. Resistance exercise and cyclooxygenase (COX) expression in human skeletal muscle: implications for COX-inhibiting drugs and protein synthesis. Am J Physiol Regul Integr Comp Physiol. 2007;292(6):R2241–8.
  • Williams CS, Mann M, DuBois RN. The role of cyclooxygenases in inflammation, cancer, and development. Oncogene. 1999;18(55):7908–7916.
  • Gupta RA, Tejada LV, Tong BJ, et al. Cyclooxygenase-1 is overexpressed and promotes angiogenic growth factor production in ovarian cancer. Cancer Res. 2003;63(5):906–911.
  • Attiq A, Yao LJ, Afzal S, Khan MA. The triumvirate of NF-κB, inflammation and cytokine storm in COVID-19. Int Immunopharmacol. 2021;101(Pt B):108255.
  • Huang Y, Qiao F, Abagyan R, Hazard S, Tomlinson S. Defining the CD59-C9 binding interaction. J Biol Chem. 2006;281(37):27398–27404.
  • Chidlow JHJ, Sessa WC. Caveolae, caveolins, and cavins: complex control of cellular signalling and inflammation. Cardiovasc Res. 2010;86(2):219–225.
  • Ciuba K, Hawkes W, Tojkander S, et al. Calponin-3 is critical for coordinated contractility of actin stress fibers. Sci Rep. 2018;8(1):17670.
  • Monroy JA, Powers KL, Gilmore LA, Uyeno TA, Lindstedt SL, Nishikawa KC. What is the role of titin in active muscle? Exerc Sport Sci Rev. 2012;40(2):73–78.
  • Duan G, Kang S, Tian X, et al. Protein Corona mitigates the cytotoxicity of graphene oxide by reducing its physical interaction with cell membrane. Nanoscale. 2015;7(37):15214–15224.
  • Chung C, Kim YK, Shin D, Ryoo SR, Hong BH, Min DH. Biomedical applications of graphene and graphene oxide. Acc Chem Res. 2013;46(10):2211–2224.
  • Wang M, Gustafsson OJR, Siddiqui G, et al. Human plasma proteome association and cytotoxicity of nano-graphene oxide grafted with stealth polyethylene glycol and poly(2-ethyl-2-oxazoline). Nanoscale. 2018;10(23):10863–10875.
  • Hajipour MJ, Raheb J, Akhavan O, et al. Personalized disease-specific protein Corona influences the therapeutic impact of graphene oxide. Nanoscale. 2015;7(19):8978–8994.
  • Di Santo R, Digiacomo L, Quagliarini E, et al. Personalized graphene oxide-protein corona in the human plasma of pancreatic cancer patients. Front Bioeng Biotechnol. 2020;8:491.