Generic placeholder image

Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Review Article

Therapeutic Potential of Superoxide Dismutase Fused with Cell- Penetrating Peptides in Oxidative Stress-Related Diseases

Author(s): Xiao-Lu Wang and Ren-Wang Jiang*

Volume 22, Issue 17, 2022

Published on: 05 April, 2022

Page: [2287 - 2298] Pages: 12

DOI: 10.2174/1389557522666220228150127

Price: $65

Abstract

Superoxide dismutase (SOD) is a well-known cellular antioxidant enzyme. However, exogenous SOD cannot be used to protect tissues from oxidative damage due to the low permeability of the cell membrane. Cell-penetrating peptides (CPPs) are a class of short peptides that can cross the cell membrane. Recombinant fusion protein that fuses SOD protein with CPP (CPP-SOD) can cross various tissues and organs as well as the blood-brain barrier.

CPP-SODs can relieve severe oxidative damage in various tissues caused by radiation, ischemia, inflammation, and chemotherapy by clearing the reactive oxygen species, reducing the expression of inflammatory factors, and inhibiting NF-κB/MAPK signaling pathways. Therefore, the clinical application of CPP-SODs provides new therapeutic strategies for a variety of oxidative stress-related disorders, such as Parkinson’s disease, diabetes, obesity, cardiac fibrosis, and premature aging.

Keywords: Superoxide dismutase, cell-penetrating peptides, permeability, biomembrane, fusion protein, oxidative stress related disorder.

Graphical Abstract

[1]
Rabbani, G.; Ahn, S.N. Structure, enzymatic activities, glycation and therapeutic potential of human serum albumin: A natural cargo. Int. J. Biol. Macromol., 2019, 123, 979-990.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.11.053] [PMID: 30439428]
[2]
Burgoyne, J.R.; Mongue-Din, H.; Eaton, P.; Shah, A.M. Redox signaling in cardiac physiology and pathology. Circ. Res., 2012, 111(8), 1091-1106.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.255216] [PMID: 23023511]
[3]
Lei, Y.; Wang, K.; Deng, L.; Chen, Y.; Nice, E.C.; Huang, C. Redox regulation of inflammation: Old elements, a new story. Med. Res. Rev., 2015, 35(2), 306-340.
[http://dx.doi.org/10.1002/med.21330] [PMID: 25171147]
[4]
Chio, I.I.C.; Tuveson, D.A. ROS in cancer: The burning question. Trends Mol. Med., 2017, 23(5), 411-429.
[http://dx.doi.org/10.1016/j.molmed.2017.03.004] [PMID: 28427863]
[5]
Cross, C.E.; Halliwell, B.; Borish, E.T.; Pryor, W.A.; Ames, B.N.; Saul, R.L.; McCord, J.M.; Harman, D. Oxygen radicals and human disease. Ann. Intern. Med., 1987, 107(4), 526-545.
[http://dx.doi.org/10.7326/0003-4819-107-4-526] [PMID: 3307585]
[6]
Salahuddin, P.; Rabbani, G.; Khan, R.H. The role of advanced glycation end products in various types of neurodegenerative disease: A therapeutic approach. Cell. Mol. Biol. Lett., 2014, 19(3), 407-437.
[http://dx.doi.org/10.2478/s11658-014-0205-5] [PMID: 25141979]
[7]
Liu, Y.Q.; Wang, X.L.; He, D.H.; Cheng, Y.X. Protection against chemotherapy- and radiotherapy-induced side effects: A review based on the mechanisms and therapeutic opportunities of phytochemicals. Phytomedicine, 2021, 80, 153402.
[http://dx.doi.org/10.1016/j.phymed.2020.153402] [PMID: 33203590]
[8]
Liou, G.G.; Hsieh, C.C.; Lee, Y.J.; Li, P.H.; Tsai, M.S.; Li, C.T.; Wang, S.H. N-acetyl cysteine overdose inducing hepatic steatosis and systemic inflammation in both propacetamol-induced hepatotoxic and normal mice. Antioxidants, 2021, 10(3), 442.
[http://dx.doi.org/10.3390/antiox10030442] [PMID: 33809388]
[9]
Kumar, V.; Rahman, S.; Choudhry, H.; Zamzami, M.A.; Sarwar Jamal, M.; Islam, A.; Ahmad, F.; Hassan, M.I. Computing disease-linked SOD1 mutations: Deciphering protein stability and patient-phenotype relations. Sci. Rep., 2017, 7(1), 4678.
[http://dx.doi.org/10.1038/s41598-017-04950-9] [PMID: 28680046]
[10]
Rhee, S.G. Cell signaling. H2O2, a necessary evil for cell signaling. Science, 2006, 312(5782), 1882-1883.
[http://dx.doi.org/10.1126/science.1130481] [PMID: 16809515]
[11]
McCord, J.M.; Fridovich, I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem., 1969, 244(22), 6049-6055.
[http://dx.doi.org/10.1016/S0021-9258(18)63504-5] [PMID: 5389100]
[12]
Fridovich, I. Biological effects of the superoxide radical. Arch. Biochem. Biophys., 1986, 247(1), 1-11.
[http://dx.doi.org/10.1016/0003-9861(86)90526-6] [PMID: 3010872]
[13]
Baig, M.H.; Jan, A.T.; Rabbani, G.; Ahmad, K.; Ashraf, J.M.; Kim, T.; Min, H.S.; Lee, Y.H.; Cho, W.K.; Ma, J.Y.; Lee, E.J.; Choi, I. Methylglyoxal and Advanced Glycation End products: Insight of the regulatory machinery affecting the myogenic program and of its modulation by natural compounds. Sci. Rep., 2017, 7(1), 5916.
[http://dx.doi.org/10.1038/s41598-017-06067-5] [PMID: 28725008]
[14]
Marklund, S.L.; Holme, E.; Hellner, L. Superoxide dismutase in extracellular fluids. Clin. Chim. Acta, 1982, 126(1), 41-51.
[http://dx.doi.org/10.1016/0009-8981(82)90360-6] [PMID: 7172448]
[15]
Zelko, I.N.; Mariani, T.J.; Folz, R.J. Superoxide dismutase multigene family: A comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic. Biol. Med., 2002, 33(3), 337-349.
[http://dx.doi.org/10.1016/S0891-5849(02)00905-X] [PMID: 12126755]
[16]
Pardo, C.A.; Xu, Z.; Borchelt, D.R.; Price, D.L.; Sisodia, S.S.; Cleveland, D.W. Superoxide dismutase is an abundant component in cell bodies, dendrites, and axons of motor neurons and in a subset of other neurons. Proc. Natl. Acad. Sci. USA, 1995, 92(4), 954-958.
[http://dx.doi.org/10.1073/pnas.92.4.954] [PMID: 7862672]
[17]
Collister, J.P.; Bellrichard, M.; Drebes, D.; Nahey, D.; Tian, J.; Zimmerman, M.C. Over-expression of copper/zinc superoxide dismutase in the median preoptic nucleus attenuates chronic angiotensin II-induced hypertension in the rat. Int. J. Mol. Sci., 2014, 15(12), 22203-22213.
[http://dx.doi.org/10.3390/ijms151222203] [PMID: 25474089]
[18]
Jiang, Y.; Brynskikh, A.M. S-Manickam, D.; Kabanov, A.V. SOD1 nanozyme salvages ischemic brain by locally protecting cerebral vasculature. J. Control. Release, 2015, 213, 36-44.
[http://dx.doi.org/10.1016/j.jconrel.2015.06.021] [PMID: 26093094]
[19]
Nizzardo, M.; Simone, C.; Rizzo, F.; Ulzi, G.; Ramirez, A.; Rizzuti, M.; Bordoni, A.; Bucchia, M.; Gatti, S.; Bresolin, N.; Comi, G.P.; Corti, S. Morpholino-mediated SOD1 reduction ameliorates an amyotrophic lateral sclerosis disease phenotype. Sci. Rep., 2016, 6, 21301.
[http://dx.doi.org/10.1038/srep21301] [PMID: 26878886]
[20]
Gopal, T.; Kumar, N.; Perriotte-Olson, C.; Casey, C.A.; Donohue, T.M., Jr; Harris, E.N.; Talmon, G.; Kabanov, A.V.; Saraswathi, V. Nanoformulated SOD1 ameliorates the combined NASH and alcohol-associated liver disease partly via regulating CYP2E1 expression in adipose tissue and liver. Am. J. Physiol. Gastrointest. Liver Physiol., 2020, 318(3), G428-G438.
[http://dx.doi.org/10.1152/ajpgi.00217.2019] [PMID: 31928222]
[21]
Seo, Y.S.; Kim, H.S.; Lee, A.Y.; Chun, J.M.; Kim, S.B.; Moon, B.C.; Kwon, B.I. Codonopsis lanceolata attenuates allergic lung inflammation by inhibiting Th2 cell activation and augmenting mitochondrial ROS dismutase (SOD2) expression. Sci. Rep., 2019, 9(1), 2312.
[http://dx.doi.org/10.1038/s41598-019-38782-6] [PMID: 30783201]
[22]
Luo, T.; Liu, H.; Kim, J.K. Estrogen protects the female heart from ischemia/reperfusion injury through manganese superoxide dismutase phosphorylation by mitochondrial p38β at threonine 79 and Serine 106. PLoS One, 2016, 11(12), e0167761.
[http://dx.doi.org/10.1371/journal.pone.0167761] [PMID: 27930699]
[23]
Yang, C.; Chen, H.X.; Zhou, Y.; Liu, M.X.; Wang, Y.; Wang, J.X.; Ren, S.P.; Han, Y.; Wu, B.Y. Manganese superoxide dismutase gene therapy protects against irradiation- induced intestinal injury. Curr. Gene Ther., 2013, 13(5), 305-314.
[http://dx.doi.org/10.2174/15665232113136660027] [PMID: 24060314]
[24]
Copin, J.C.; Gasche, Y.; Chan, P.H. Overexpression of copper/zinc superoxide dismutase does not prevent neonatal lethality in mutant mice that lack manganese superoxide dismutase. Free Radic. Biol. Med., 2000, 28(10), 1571-1576.
[http://dx.doi.org/10.1016/S0891-5849(00)00280-X] [PMID: 10927183]
[25]
Marklund, S.L. Extracellular superoxide dismutase in human tissues and human cell lines. J. Clin. Invest., 1984, 74(4), 1398-1403.
[http://dx.doi.org/10.1172/JCI111550] [PMID: 6541229]
[26]
Lee, Y.S.; Choi, J.H.; Lee, J.H.; Lee, H.W.; Lee, W.; Kim, W.T.; Kim, T.Y. Extracellular superoxide dismutase ameliorates house dust mite-induced atopic dermatitis-like skin inflammation and inhibits mast cell activation in mice. Exp. Dermatol., 2016, 25(8), 630-635.
[http://dx.doi.org/10.1111/exd.13028] [PMID: 27061078]
[27]
Wei, L.; Zhang, J.; Yang, Z.L.; You, H. Extracellular superoxide dismutase increased the therapeutic potential of human mesenchymal stromal cells in radiation pulmonary fibrosis. Cytotherapy, 2017, 19(5), 586-602.
[http://dx.doi.org/10.1016/j.jcyt.2017.02.359] [PMID: 28314668]
[28]
Kliment, C.R.; Oury, T.D. Extracellular superoxide dismutase protects cardiovascular syndecan-1 from oxidative shedding. Free Radic. Biol. Med., 2011, 50(9), 1075-1080.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.02.014] [PMID: 21334435]
[29]
Zaghloul, N.; Patel, H.; Codipilly, C.; Marambaud, P.; Dewey, S.; Frattini, S.; Huerta, P.T.; Nasim, M.; Miller, E.J.; Ahmed, M. Overexpression of extracellular superoxide dismutase protects against brain injury induced by chronic hypoxia. PLoS One, 2014, 9(9), e108168.
[http://dx.doi.org/10.1371/journal.pone.0108168] [PMID: 25268361]
[30]
Raucher, D.; Ryu, J.S. Cell-penetrating peptides: Strategies for anticancer treatment. Trends Mol. Med., 2015, 21(9), 560-570.
[http://dx.doi.org/10.1016/j.molmed.2015.06.005] [PMID: 26186888]
[31]
Park, L.; Min, D.; Kim, H.; Park, J.; Choi, S.; Park, Y. The combination of metallothionein and superoxide dismutase protects pancreatic β cells from oxidative damage. Diabetes Metab. Rev., 2011, 27(8), 802-808.
[http://dx.doi.org/10.1002/dmrr.1254] [PMID: 22069263]
[32]
Choi, H.S.; An, J.J.; Kim, S.Y.; Lee, S.H.; Kim, D.W.; Yoo, K.Y.; Won, M.H.; Kang, T.C.; Kwon, H.J.; Kang, J.H.; Cho, S.W.; Kwon, O.S.; Park, J.; Eum, W.S.; Choi, S.Y. PEP-1-SOD fusion protein efficiently protects against paraquat-induced dopaminergic neuron damage in a Parkinson disease mouse model. Free Radic. Biol. Med., 2006, 41(7), 1058-1068.
[http://dx.doi.org/10.1016/j.freeradbiomed.2006.06.006] [PMID: 16962931]
[33]
Ye, N.; Liu, S.; Lin, Y.; Rao, P. Protective effects of intraperitoneal injection of TAT-SOD against focal cerebral ischemia/reperfusion injury in rats. Life Sci., 2011, 89(23-24), 868-874.
[http://dx.doi.org/10.1016/j.lfs.2011.09.015] [PMID: 21983418]
[34]
Zhang, Y.E.; Fu, S.Z.; Li, X.Q.; Chen, P.; Wang, J.L.; Che, J.; Tang, J.M.; Chen, S.Y.; Wang, J.N. PEP-1-SOD1 protects brain from ischemic insult following asphyxial cardiac arrest in rats. Resuscitation, 2011, 82(8), 1081-1086.
[http://dx.doi.org/10.1016/j.resuscitation.2011.01.034] [PMID: 21531066]
[35]
Martorana, F.; Brambilla, L.; Valori, C.F.; Bergamaschi, C.; Roncoroni, C.; Aronica, E.; Volterra, A.; Bezzi, P.; Rossi, D. The BH4 domain of Bcl-X(L) rescues astrocyte degeneration in amyotrophic lateral sclerosis by modulating intracellular calcium signals. Hum. Mol. Genet., 2012, 21(4), 826-840.
[http://dx.doi.org/10.1093/hmg/ddr513] [PMID: 22072391]
[36]
Sclip, A.; Tozzi, A.; Abaza, A.; Cardinetti, D.; Colombo, I.; Calabresi, P.; Salmona, M.; Welker, E.; Borsello, T. c-Jun N-terminal kinase has a key role in Alzheimer disease synaptic dysfunctionin vivo. Cell Death Dis., 2014, 5, e1019.
[http://dx.doi.org/10.1038/cddis.2013.559] [PMID: 24457963]
[37]
Zhang, Y.E.; Wang, J.N.; Tang, J.M.; Guo, L.Y.; Yang, J.Y.; Huang, Y.Z.; Tan, Y.; Fu, S.Z.; Kong, X.; Zheng, F. In vivo protein transduction: Delivery of PEP-1-SOD1 fusion protein into myocardium efficiently protects against ischemic insult. Mol. Cells, 2009, 27(2), 159-166.
[http://dx.doi.org/10.1007/s10059-009-0020-4] [PMID: 19277497]
[38]
Huang, G.Q.; Wang, J.N.; Tang, J.M.; Zhang, L.; Zheng, F.; Yang, J.Y.; Guo, L.Y.; Kong, X.; Huang, Y.Z.; Liu, Y.; Chen, S.Y. The combined transduction of copper, zinc-superoxide dismutase and catalase mediated by cell-penetrating peptide, PEP-1, to protect myocardium from ischemia-reperfusion injury. J. Transl. Med., 2011, 9, 73.
[http://dx.doi.org/10.1186/1479-5876-9-73] [PMID: 21600015]
[39]
Crombez, L.; Morris, M.C.; Dufort, S.; Aldrian-Herrada, G.; Nguyen, Q.; Mc Master, G.; Coll, J.L.; Heitz, F.; Divita, G. Targeting cyclin B1 through peptide-based delivery of siRNA prevents tumour growth. Nucleic Acids Res., 2009, 37(14), 4559-4569.
[http://dx.doi.org/10.1093/nar/gkp451] [PMID: 19483097]
[40]
Abes, R.; Arzumanov, A.A.; Moulton, H.M.; Abes, S.; Ivanova, G.D.; Iversen, P.L.; Gait, M.J.; Lebleu, B. Cell-penetrating-peptide-based delivery of oligonucleotides: An overview. Biochem. Soc. Trans., 2007, 35(Pt 4), 775-779.
[http://dx.doi.org/10.1042/BST0350775] [PMID: 17635146]
[41]
Touchard, E.; Omri, S.; Naud, M.C.; Berdugo, M.; Deloche, C.; Abadie, C.; Jonet, L.; Jeanny, J.C.; Crisanti, P.; de Kozak, Y.; Combette, J.M.; Behar-Cohen, F. A peptide inhibitor of c-Jun N-terminal kinase for the treatment of endotoxin-induced uveitis. Invest. Ophthalmol. Vis. Sci., 2010, 51(9), 4683-4693.
[http://dx.doi.org/10.1167/iovs.09-4733] [PMID: 20393119]
[42]
Beydoun, T.; Deloche, C.; Perino, J.; Kirwan, B.A.; Combette, J.M.; Behar-Cohen, F. Subconjunctival injection of XG-102, a JNK inhibitor peptide, in patients with intraocular inflammation: A safety and tolerability study. J. Ocul. Pharmacol. Ther., 2015, 31(2), 93-99.
[http://dx.doi.org/10.1089/jop.2013.0247] [PMID: 25347151]
[43]
Edeas, M.A.; Emerit, I.; Khalfoun, Y.; Lazizi, Y.; Cernjavski, L.; Levy, A.; Lindenbaum, A. Clastogenic factors in plasma of HIV-1 infected patients activate HIV-1 replication in vitro: Inhibition by superoxide dismutase. Free Radic. Biol. Med., 1997, 23(4), 571-578.
[http://dx.doi.org/10.1016/S0891-5849(97)00002-6] [PMID: 9215803]
[44]
Bechara, C.; Sagan, S. Cell-penetrating peptides: 20 years later, where do we stand? FEBS Lett., 2013, 587(12), 1693-1702.
[http://dx.doi.org/10.1016/j.febslet.2013.04.031] [PMID: 23669356]
[45]
Frankel, A.D.; Pabo, C.O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell, 1988, 55(6), 1189-1193.
[http://dx.doi.org/10.1016/0092-8674(88)90263-2] [PMID: 2849510]
[46]
Green, M.; Loewenstein, P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell, 1988, 55(6), 1179-1188.
[http://dx.doi.org/10.1016/0092-8674(88)90262-0] [PMID: 2849509]
[47]
Vivès, E.; Brodin, P.; Lebleu, B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem., 1997, 272(25), 16010-16017.
[http://dx.doi.org/10.1074/jbc.272.25.16010] [PMID: 9188504]
[48]
Park, J.; Ryu, J.; Kim, K.A.; Lee, H.J.; Bahn, J.H.; Han, K.; Choi, E.Y.; Lee, K.S.; Kwon, H.Y.; Choi, S.Y. Mutational analysis of a human immunodeficiency virus type 1 Tat protein transduction domain which is required for delivery of an exogenous protein into mammalian cells. J. Gen. Virol., 2002, 83(Pt 5), 1173-1181.
[http://dx.doi.org/10.1099/0022-1317-83-5-1173] [PMID: 11961273]
[49]
Pan, J.; Su, Y.; Hou, X.; He, H.; Liu, S.; Wu, J.; Rao, P. Protective effect of recombinant protein SOD-TAT on radiation-induced lung injury in mice. Life Sci., 2012, 91(3-4), 89-93.
[http://dx.doi.org/10.1016/j.lfs.2012.06.003] [PMID: 22727792]
[50]
Gu, Q.; Feng, T.; Cao, H.; Tang, Y.; Ge, X.; Luo, J.; Xue, J.; Wu, J.; Yang, H.; Zhang, S.; Cao, J. HIV-TAT mediated protein transduction of Cu/Zn-superoxide dismutase-1 (SOD1) protects skin cells from ionizing radiation. Radiat. Oncol., 2013, 8, 253.
[http://dx.doi.org/10.1186/1748-717X-8-253] [PMID: 24175971]
[51]
Pan, J.; He, H.; Su, Y.; Zheng, G.; Wu, J.; Liu, S.; Rao, P. In vivo radioprotective activity of cell-permeable bifunctional antioxidant enzyme GST-TAT-SOD against whole-body ionizing irradiation in mice. Oxid. Med. Cell. Longev., 2017, 2017, 2689051.
[http://dx.doi.org/10.1155/2017/2689051] [PMID: 28804533]
[52]
Chen, X.; Liu, S.; Rao, P.; Bradshaw, J.; Weller, R. Topical application of superoxide dismutase mediated by HIV-TAT peptide attenuates UVB-induced damages in human skin. Eur. J. Pharm. Biopharm., 2016, 107, 286-294.
[http://dx.doi.org/10.1016/j.ejpb.2016.07.023] [PMID: 27460952]
[53]
Pan, J.; He, H.; Su, Y.; Zheng, G.; Wu, J.; Liu, S.; Rao, P. GST-TAT-SOD: Cell permeable bifunctional antioxidant enzyme-a potential selective radioprotector. Oxid. Med. Cell. Longev., 2016, 2016, 5935080.
[http://dx.doi.org/10.1155/2016/5935080] [PMID: 27313832]
[54]
Guo, J.K.; Xu, M.M.; Zheng, M.F.; Liu, S.T.; Zhou, J.W.; Ke, L.J.; Chen, T.B.; Rao, P.F. Topical application of TAT-superoxide dismutase in acupoints LI 20 on allergic rhinitis; Evid-Based Compl Alt, 2016.
[http://dx.doi.org/10.1155/2016/3830273]
[55]
Kim, H.A.; Kim, D.W.; Park, J.; Choi, S.Y. Transduction of Cu, Zn-superoxide dismutase mediated by an HIV-1 Tat protein basic domain into human chondrocytes. Arthritis Res. Ther., 2006, 8(4), R96.
[http://dx.doi.org/10.1186/ar1972] [PMID: 16792821]
[56]
Chang, S.N.; Khan, I.; Dey, D.K.; Cho, K.H.; Hwang, B.S.; Bae, K.B.; Kang, S.C.; Park, J.G. Decursinol angelate ameliorates 12-O-tetradecanoyl phorbol-13-acetate (TPA) -induced NF-κB activation on mice ears by inhibiting exaggerated inflammatory cell infiltration, oxidative stress and pro-inflammatory cytokine production. Food Chem. Toxicol., 2019, 132, 110699.
[http://dx.doi.org/10.1016/j.fct.2019.110699] [PMID: 31351099]
[57]
Khan, A.Q.; Khan, R.; Qamar, W.; Lateef, A.; Rehman, M.U.; Tahir, M.; Ali, F.; Hamiza, O.O.; Hasan, S.K.; Sultana, S. Geraniol attenuates 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced oxidative stress and inflammation in mouse skin: Possible role of p38 MAP Kinase and NF-κB. Exp. Mol. Pathol., 2013, 94(3), 419-429.
[http://dx.doi.org/10.1016/j.yexmp.2013.01.006] [PMID: 23399806]
[58]
Song, H.Y.; Lee, J.A.; Ju, S.M.; Yoo, K.Y.; Won, M.H.; Kwon, H.J.; Eum, W.S.; Jang, S.H.; Choi, S.Y.; Park, J. Topical transduction of superoxide dismutase mediated by HIV-1 Tat protein transduction domain ameliorates 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced inflammation in mice. Biochem. Pharmacol., 2008, 75(6), 1348-1357.
[http://dx.doi.org/10.1016/j.bcp.2007.11.015] [PMID: 18164693]
[59]
Lee, J.A.; Song, H.Y.; Ju, S.M.; Lee, S.J.; Kwon, H.J.; Eum, W.S.; Jang, S.H.; Choi, S.Y.; Park, J.S. Differential regulation of inducible nitric oxide synthase and cyclooxygenase-2 expression by superoxide dismutase in lipopolysaccharide stimulated RAW 264.7 cells. Exp. Mol. Med., 2009, 41(9), 629-637.
[http://dx.doi.org/10.3858/emm.2009.41.9.069] [PMID: 19478557]
[60]
Liu, T.P.; Chen, Y.P.; Chou, C.M.; Chiu, T.T.; Chen, C.T. Therapeutic evaluation of HIV transduction basic domain-conjugated superoxide dismutase solution on suppressive effects of the formation of peroxynitrite and expression of COX-2 in murine skin. J. Biomed. Sci., 2016, 23, 11.
[http://dx.doi.org/10.1186/s12929-016-0226-7] [PMID: 26786970]
[61]
Park, S.H.; Shin, M.J.; Kim, D.W.; Park, J.; Choi, S.Y.; Kang, Y.H. Blockade of monocyte-endothelial trafficking by transduced Tat-superoxide dismutase protein. Int. J. Mol. Med., 2016, 37(2), 387-397.
[http://dx.doi.org/10.3892/ijmm.2015.2444] [PMID: 26707483]
[62]
Song, H.Y.; Ju, S.M.; Goh, A.R.; Kwon, D.J.; Choi, S.Y.; Park, J. Suppression of TNF-alpha-induced MMP-9 expression by a cell-permeable superoxide dismutase in keratinocytes. BMB Rep., 2011, 44(7), 462-467.
[http://dx.doi.org/10.5483/BMBRep.2011.44.7.462] [PMID: 21777517]
[63]
Guo, J.; Chen, Y.; Yuan, B.; Liu, S.; Rao, P. Effects of intracellular superoxide removal at acupoints with TAT-SOD on obesity. Free Radic. Biol. Med., 2011, 51(12), 2185-2189.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.09.036] [PMID: 22019441]
[64]
Eum, W.S.; Choung, I.S.; Li, M.Z.; Kang, J.H.; Kim, D.W.; Park, J.; Kwon, H.Y.; Choi, S.Y. HIV-1 Tat-mediated protein transduction of Cu,Zn-superoxide dismutase into pancreatic beta cells in vitro andin vivo. Free Radic. Biol. Med., 2004, 37(3), 339-349.
[http://dx.doi.org/10.1016/j.freeradbiomed.2004.04.036] [PMID: 15223067]
[65]
Min, D.; Kim, H.; Park, L.; Kim, T.H.; Hwang, S.; Kim, M.J.; Jang, S.; Park, Y. Amelioration of diabetic neuropathy by TAT-mediated enhanced delivery of metallothionein and SOD. Endocrinology, 2012, 153(1), 81-91.
[http://dx.doi.org/10.1210/en.2011-1639] [PMID: 22128026]
[66]
Lee, J.A.; Song, H.Y.; Ju, S.M.; Lee, S.J.; Seo, W.Y.; Sin, D.H.; Goh, A.R.; Choi, S.Y.; Park, J. Suppression of inducible nitric oxide synthase and cyclooxygenase-2 by cell-permeable superoxide dismutase in lipopolysaccharide-stimulated BV-2 microglial cells. Mol. Cells, 2010, 29(3), 245-250.
[http://dx.doi.org/10.1007/s10059-010-0031-1] [PMID: 20108167]
[67]
Pan, J.; Li, L.; Liang, L.; He, H.; Su, Y.; Wang, X.; Liu, S. Cytoprotective effects of cell-permeable bifunctional antioxidant enzyme, GST-TAT-SOD, against cisplatin-induced cell damage. Oxid. Med. Cell. Longev., 2017, 2017, 9530791.
[http://dx.doi.org/10.1155/2017/9530791] [PMID: 29333214]
[68]
Yao, W.; Zhao, H.; Shi, R.; Li, X.; Li, Y.; Ke, C.; Liu, J. Recombinant protein transduction domain-Cu/Zn superoxide dismutase alleviates bone cancer pain via peroxiredoxin 4 modulation and antioxidation. Biochem. Biophys. Res. Commun., 2017, 486(4), 1143-1148.
[http://dx.doi.org/10.1016/j.bbrc.2017.04.017] [PMID: 28391978]
[69]
Guo, H.; Zhang, N.; Liu, D.; Wang, P.; Ma, X. Inhibitory effect on the proliferation of human heptoma induced by cell-permeable manganese superoxide dismutase. Biomed. Pharmacother., 2016, 83, 1379-1386.
[http://dx.doi.org/10.1016/j.biopha.2016.08.054] [PMID: 27583978]
[70]
Morris, M.C.; Depollier, J.; Mery, J.; Heitz, F.; Divita, G. A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat. Biotechnol., 2001, 19(12), 1173-1176.
[http://dx.doi.org/10.1038/nbt1201-1173] [PMID: 11731788]
[71]
Choi, S.H.; Kim, D.W.; Kim, S.Y.; An, J.J.; Lee, S.H.; Choi, H.S.; Sohn, E.J.; Hwang, S.I.; Won, M.H.; Kang, T.C.; Kwon, H.J.; Kang, J.H.; Cho, S.W.; Park, J.; Eum, W.S.; Choi, S.Y. Transduced human copper chaperone for Cu,Zn-SOD (PEP-1-CCS) protects against neuronal cell death. Mol. Cells, 2005, 20(3), 401-408.
[PMID: 16404156]
[72]
Hwang, I.K.; Eum, W.S.; Yoo, K.Y.; Cho, J.H.; Kim, D.W.; Choi, S.H.; Kang, T.C.; Kwon, O.S.; Kang, J.H.; Choi, S.Y.; Won, M.H. Copper chaperone for Cu,Zn-SOD supplement potentiates the Cu,Zn-SOD function of neuroprotective effects against ischemic neuronal damage in the gerbil hippocampus. Free Radic. Biol. Med., 2005, 39(3), 392-402.
[http://dx.doi.org/10.1016/j.freeradbiomed.2005.03.027] [PMID: 15993338]
[73]
Yoo, D.Y.; Shin, B.N.; Kim, I.H.; Kim, W.; Kim, D.W.; Yoo, K.Y.; Choi, J.H.; Lee, C.H.; Yoon, Y.S.; Choi, S.Y.; Won, M.H.; Hwang, I.K. Effects of Cu,Zn-superoxide dismutase on cell proliferation and neuroblast differentiation in the mouse dentate gyrus. Neurochem. Res., 2012, 37(2), 261-267.
[http://dx.doi.org/10.1007/s11064-011-0605-0] [PMID: 21927927]
[74]
Eum, W.S.; Kim, D.W.; Hwang, I.K.; Yoo, K.Y.; Kang, T.C.; Jang, S.H.; Choi, H.S.; Choi, S.H.; Kim, Y.H.; Kim, S.Y.; Kwon, H.Y.; Kang, J.H.; Kwon, O.S.; Cho, S.W.; Lee, K.S.; Park, J.; Won, M.H.; Choi, S.Y. In vivo protein transduction: Biologically active intact pep-1-superoxide dismutase fusion protein efficiently protects against ischemic insult. Free Radic. Biol. Med., 2004, 37(10), 1656-1669.
[http://dx.doi.org/10.1016/j.freeradbiomed.2004.07.028] [PMID: 15477017]
[75]
Cho, J.H.; Hwang, I.K.; Yoo, K.Y.; Kim, S.Y.; Kim, D.W.; Kwon, Y.G.; Choi, S.Y.; Won, M.H. Effective delivery of Pep-1-cargo protein into ischemic neurons and long-term neuroprotection of Pep-1-SOD1 against ischemic injury in the gerbil hippocampus. Neurochem. Int., 2008, 52(4-5), 659-668.
[http://dx.doi.org/10.1016/j.neuint.2007.08.013] [PMID: 17919780]
[76]
Tanaka, Y.; Marumo, T.; Omura, T.; Yoshida, S. Early increases in serum S100B are associated with cerebral hemorrhage in a rat model of focal cerebral ischemia. Brain Res., 2008, 1227, 248-254.
[http://dx.doi.org/10.1016/j.brainres.2008.06.076] [PMID: 18621038]
[77]
Rundgren, M.; Karlsson, T.; Nielsen, N.; Cronberg, T.; Johnsson, P.; Friberg, H. Neuron specific enolase and S-100B as predictors of outcome after cardiac arrest and induced hypothermia. Resuscitation, 2009, 80(7), 784-789.
[http://dx.doi.org/10.1016/j.resuscitation.2009.03.025] [PMID: 19467754]
[78]
Cunningham, R.T.; Young, I.S.; Winder, J.; O’Kane, M.J.; McKinstry, S.; Johnston, C.F.; Dolan, O.M.; Hawkins, S.A.; Buchanan, K.D. Serum neurone specific enolase (NSE) levels as an indicator of neuronal damage in patients with cerebral infarction. Eur. J. Clin. Invest., 1991, 21(5), 497-500.
[http://dx.doi.org/10.1111/j.1365-2362.1991.tb01401.x] [PMID: 1752289]
[79]
Tatarkova, Z.; Kovalska, M.; Sivonova, M.K.; Racay, P.; Lehotsky, J.; Kaplan, P. Tyrosine nitration of mitochondrial proteins during myocardial ischemia and reperfusion. J. Physiol. Biochem., 2019, 75(2), 217-227.
[http://dx.doi.org/10.1007/s13105-019-00683-7] [PMID: 31115776]
[80]
Goswami, D.G.; Kant, R.; Ammar, D.A.; Agarwal, C.; Gomez, J.; Agarwal, R.; Saba, L.M.; Fritz, K.S.; Tewari-Singh, N. Toxic consequences and oxidative protein carbonylation from chloropicrin exposure in human corneal epithelial cells. Toxicol. Lett., 2020, 322, 1-11.
[http://dx.doi.org/10.1016/j.toxlet.2019.12.023] [PMID: 31884112]
[81]
Yune, T.Y.; Lee, J.Y.; Jiang, M.H.; Kim, D.W.; Choi, S.Y.; Oh, T.H. Systemic administration of PEP-1-SOD1 fusion protein improves functional recovery by inhibition of neuronal cell death after spinal cord injury. Free Radic. Biol. Med., 2008, 45(8), 1190-1200.
[http://dx.doi.org/10.1016/j.freeradbiomed.2008.07.016] [PMID: 18722523]
[82]
Kim, W.; Kim, D.W.; Yoo, D.Y.; Chung, J.Y.; Hwang, I.K.; Won, M.H.; Choi, S.Y.; Jeon, S.W.; Jeong, J.H.; Hwang, H.S.; Moon, S.M. Neuroprotective effects of PEP-1-Cu,Zn-SOD against ischemic neuronal damage in the rabbit spinal cord. Neurochem. Res., 2012, 37(2), 307-313.
[http://dx.doi.org/10.1007/s11064-011-0613-0] [PMID: 21964799]
[83]
Yoo, D.Y.; Kim, D.W.; Chung, J.Y.; Jung, H.Y.; Kim, J.W.; Yoon, Y.S.; Hwang, I.K.; Choi, J.H.; Choi, G.M.; Choi, S.Y.; Moon, S.M. Cu, Zn-Superoxide dismutase increases the therapeutic potential of adipose-derived mesenchymal stem cells by maintaining antioxidant enzyme levels. Neurochem. Res., 2016, 41(12), 3300-3307.
[http://dx.doi.org/10.1007/s11064-016-2062-2] [PMID: 27743287]
[84]
Song, H.Y.; Ju, S.M.; Lee, J.A.; Kwon, H.J.; Eum, W.S.; Jang, S.H.; Choi, S.Y.; Park, J. Suppression of HIV-1 Tat-induced monocyte adhesiveness by a cell-permeable superoxide dismutase in astrocytes. Exp. Mol. Med., 2007, 39(6), 778-786.
[http://dx.doi.org/10.1038/emm.2007.84] [PMID: 18160848]
[85]
Liu, J.; Hou, J.; Xia, Z.Y.; Zeng, W.; Wang, X.; Li, R.; Ke, C.; Xu, J.; Lei, S.; Xia, Z. Recombinant PTD-Cu/Zn SOD attenuates hypoxia-reoxygenation injury in cardiomyocytes. Free Radic. Res., 2013, 47(5), 386-393.
[http://dx.doi.org/10.3109/10715762.2013.780286] [PMID: 23445361]
[86]
Ke, Z.; Gao, A.; Xu, P.; Wang, J.; Ji, L.; Yang, J. Preconditioning with PEP-1-SOD1 fusion protein attenuates ischemia/reperfusion-induced ventricular arrhythmia in isolated rat hearts. Exp. Ther. Med., 2015, 10(1), 352-356.
[http://dx.doi.org/10.3892/etm.2015.2440] [PMID: 26170961]
[87]
Tan, L.G.; Xiao, J.H.; Yu, D.L.; Zhang, L.; Zheng, F.; Guo, L.Y.; Yang, J.Y.; Tang, J.M.; Chen, S.Y.; Wang, J.N. PEP-1-SOD1 fusion proteins block cardiac myofibroblast activation and angiotensin II-induced collagen production; Bmc Cardiovasc Disor, 2015, p. 15.
[88]
Choi, J.H.; Kim, D.W.; Yoo, D.Y.; Jeong, H.J.; Kim, W.; Jung, H.Y.; Nam, S.M.; Kim, J.H.; Yoon, Y.S.; Choi, S.Y.; Hwang, I.K. Repeated administration of PEP-1-Cu,Zn-superoxide dismutase and PEP-1-peroxiredoxin-2 to senescent mice induced by D-galactose improves the hippocampal functions. Neurochem. Res., 2013, 38(10), 2046-2055.
[http://dx.doi.org/10.1007/s11064-013-1112-2] [PMID: 23892988]
[89]
Choi, Y.J.; Lee, J.Y.; Chung, C.P.; Park, Y.J. Cell-penetrating superoxide dismutase attenuates oxidative stress-induced senescence by regulating the p53-p21(Cip1) pathway and restores osteoblastic differentiation in human dental pulp stem cells. Int. J. Nanomedicine, 2012, 7, 5091-5106.
[PMID: 23049256]
[90]
Kim, M.; Maeng, J.; Jung, J.; Kim, H.Y.; Kim, H.J.; Kwon, Y.; Lee, K. Design and evaluation of variants of the protein transduction domain originated from translationally controlled tumor protein. Eur. J. Pharm. Sci., 2011, 43(1-2), 25-31.
[http://dx.doi.org/10.1016/j.ejps.2011.03.007] [PMID: 21440624]
[91]
Lee, J.; Kim, S.; Shin, D.H.; Kim, H.J.; Lee, K. Neuroprotective effect of Cu,Zn-superoxide dismutase fused to a TCTP-derived protein transduction domain. Eur. J. Pharmacol., 2011, 666(1-3), 87-92.
[http://dx.doi.org/10.1016/j.ejphar.2011.05.040] [PMID: 21651901]
[92]
Wender, P.A.; Mitchell, D.J.; Pattabiraman, K.; Pelkey, E.T.; Steinman, L.; Rothbard, J.B. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: Peptoid molecular transporters. Proc. Natl. Acad. Sci. USA, 2000, 97(24), 13003-13008.
[http://dx.doi.org/10.1073/pnas.97.24.13003] [PMID: 11087855]
[93]
Tünnemann, G.; Ter-Avetisyan, G.; Martin, R.M.; Stöckl, M.; Herrmann, A.; Cardoso, M.C. Live-cell analysis of cell penetration ability and toxicity of oligo-arginines. J. Pept. Sci., 2008, 14(4), 469-476.
[http://dx.doi.org/10.1002/psc.968] [PMID: 18069724]
[94]
Park, J.; Ryu, J.; Jin, L.H.; Bahn, J.H.; Kim, J.A.; Yoon, C.S.; Kim, D.W.; Han, K.H.; Eum, W.S.; Kwon, H.Y.; Kang, T.C.; Won, M.H.; Kang, J.H.; Cho, S.W.; Choi, S.Y. 9-polylysine protein transduction domain: Enhanced penetration efficiency of superoxide dismutase into mammalian cells and skin. Mol. Cells, 2002, 13(2), 202-208.
[PMID: 12018841]
[95]
Zhang, Z.; Huang, L.; Wu, Q.; Yang, E.; Zhang, G.; Sun, H.; Wang, F. A recombinant trans-membrane protein hMnSOD-R9 inhibits the proliferation of cervical cancer cells in vitro. Mol. Cell. Biochem., 2014, 385(1-2), 79-86.
[http://dx.doi.org/10.1007/s11010-013-1816-2] [PMID: 24078003]
[96]
Eiamphungporn, W.; Yainoy, S.; Prachayasittikul, V. Angiopep-2-Mediated delivery of human manganese superoxide dismutase in brain endothelial cells and its protective effect against oxidative stress. Int. J. Pept. Res. Ther., 2015, 21(1), 63-71.
[http://dx.doi.org/10.1007/s10989-014-9433-9]
[97]
Wang, X.L.; Wang, L.; Lin, F.L.; Li, S.S.; Lin, T.X.; Jiang, R.W. Protective Effect of Penetratin Analogue-Tagged SOD1 on cisplatin-induced nephrotoxicity through inhibiting oxidative stress and JNK/p38 MAPK signaling pathway. Oxid. Med. Cell. Longev., 2021, 2021, 5526053.
[http://dx.doi.org/10.1155/2021/5526053] [PMID: 34471466]
[98]
Carillon, J.; Rouanet, J.M.; Cristol, J.P.; Brion, R. Superoxide dismutase administration, a potential therapy against oxidative stress related diseases: Several routes of supplementation and proposal of an original mechanism of action. Pharm. Res., 2013, 30(11), 2718-2728.
[http://dx.doi.org/10.1007/s11095-013-1113-5] [PMID: 23793992]
[99]
Palm, C.; Jayamanne, M.; Kjellander, M.; Hällbrink, M. Peptide degradation is a critical determinant for cell-penetrating peptide uptake. Biochim. Biophys. Acta, 2007, 1768(7), 1769-1776.
[http://dx.doi.org/10.1016/j.bbamem.2007.03.029] [PMID: 17499577]
[100]
Järver, P.; Mäger, I.; Langel, Ü. In vivo biodistribution and efficacy of peptide mediated delivery. Trends Pharmacol. Sci., 2010, 31(11), 528-535.
[http://dx.doi.org/10.1016/j.tips.2010.07.006] [PMID: 20828841]
[101]
Luangwattananun, P.; Eiamphungporn, W.; Songtawee, N.; Bülow, L.; Isarankura Na Ayudhya, C.; Prachayasittikul, V.; Yainoy, S. Improving enzymatic activities and thermostability of a tri-functional enzyme with SOD, catalase and cell-permeable activities. J. Biotechnol., 2017, 247, 50-59.
[http://dx.doi.org/10.1016/j.jbiotec.2017.03.001] [PMID: 28274879]
[102]
Liu, J.; Wei, B.; Che, C.; Gong, Z.; Jiang, Y.; Si, M.; Zhang, J.; Yang, G. Enhanced stability of manganese superoxide dismutase by amino acid replacement designed via molecular dynamics simulation. Int. J. Biol. Macromol., 2019, 128, 297-303.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.01.126] [PMID: 30685308]
[103]
Yan, X.X.; Li, H.L.; Zhang, Y.T.; Wu, S.Y.; Lu, H.L.; Yu, X.L.; Meng, F.G.; Sun, J.H.; Gong, L.K. A new recombinant MS-superoxide dismutase alleviates 5-fluorouracil-induced intestinal mucositis in mice. Acta Pharmacol. Sin., 2020, 41(3), 348-357.
[http://dx.doi.org/10.1038/s41401-019-0295-8] [PMID: 31506573]
[104]
Mathieu, E.; Bernard, A.S.; Ching, H.Y.V.; Somogyi, A.; Medjoubi, K.; Fores, J.R.; Bertrand, H.C.; Vincent, A.; Trépout, S.; Guerquin-Kern, J.L.; Scheitler, A.; Ivanović-Burmazović, I.; Seksik, P.; Delsuc, N.; Policar, C. Anti-inflammatory activity of superoxide dismutase mimics functionalized with cell-penetrating peptides. Dalton Trans., 2020, 49(7), 2323-2330.
[http://dx.doi.org/10.1039/C9DT04619D] [PMID: 32022053]
[105]
Nishikawa, M.; Nagatomi, H.; Nishijima, M.; Ohira, G.; Chang, B.J.; Sato, E.; Inoue, M. Targeting superoxide dismutase to renal proximal tubule cells inhibits nephrotoxicity of cisplatin and increases the survival of cancer-bearing mice. Cancer Lett., 2001, 171(2), 133-138.
[http://dx.doi.org/10.1016/S0304-3835(01)00591-2] [PMID: 11520596]
[106]
Shuvaev, V.V.; Kiseleva, R.Y.; Arguiri, E.; Villa, C.H.; Muro, S.; Christofidou-Solomidou, M.; Stan, R.V.; Muzykantov, V.R. Targeting superoxide dismutase to endothelial caveolae profoundly alleviates inflammation caused by endotoxin. J. Control. Release, 2018, 272, 1-8.
[http://dx.doi.org/10.1016/j.jconrel.2017.12.025] [PMID: 29292038]
[107]
Saar, K.; Lindgren, M.; Hansen, M.; Eiríksdóttir, E.; Jiang, Y.; Rosenthal-Aizman, K.; Sassian, M.; Langel, U. Cell-penetrating peptides: A comparative membrane toxicity study. Anal. Biochem., 2005, 345(1), 55-65.
[http://dx.doi.org/10.1016/j.ab.2005.07.033] [PMID: 16137634]
[108]
Tréhin, R.; Merkle, H.P. Chances and pitfalls of cell penetrating peptides for cellular drug delivery. Eur. J. Pharm. Biopharm., 2004, 58(2), 209-223.
[http://dx.doi.org/10.1016/j.ejpb.2004.02.018] [PMID: 15296950]
[109]
Amantana, A.; Moulton, H.M.; Cate, M.L.; Reddy, M.T.; Whitehead, T.; Hassinger, J.N.; Youngblood, D.S.; Iversen, P.L. Pharmacokinetics, biodistribution, stability and toxicity of a cell-penetrating peptide-morpholino oligomer conjugate. Bioconjug. Chem., 2007, 18(4), 1325-1331.
[http://dx.doi.org/10.1021/bc070060v] [PMID: 17583927]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy