Cell Penetrating Peptide: Sequence-Based Computational Prediction for Intercellular Delivery of Arginine Deiminase

Author(s): Mahboubeh Zarei, Mohammad Reza Rahbar, Manica Negahdaripour, Mohammad Hossein Morowvat, Navid Nezafat*, Younes Ghasemi*.

Journal Name: Current Proteomics

Volume 17 , Issue 2 , 2020

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Graphical Abstract:


Abstract:

Background: Cell-Penetrating Peptides (CPPs), a family of short peptides, are broadly used as the carrier in the delivery of drugs and different therapeutic agents. Thanks to the existence of valuable databases, computational screening of the experimentally validated CPPs can help the researchers to select more effective CPPs for the intercellular delivery of therapeutic proteins. Arginine deiminase of Mycoplasma hominis, an arginine-degrading enzyme, is currently in the clinical trial for treating several arginine auxotrophic cancers. However, some tumor cells have developed resistance to ADI treatment. The ADI resistance arises from the over-expression of argininosuccinate synthetase 1 enzyme, which is involved in arginine synthesis. Intracellular delivery of ADI into tumor cells is suggested as an efficient approach to overcome the aforesaid drawback.

Objective: In this study, in-silico tools were used for evaluating the experimentally validated CPPs to select the best CPP candidates for the intracellular delivery of ADI.

Results: In this regard, 150 CPPs of protein cargo available at CPPsite were retrieved and evaluated by the CellPPD server. The best CPP candidates for the intracellular delivery of ADI were selected based on stability and antigenicity of the ADI-CPP fusion form. The conjugated forms of ADI with each of the three CPPs including EGFP-hcT (9-32), EGFP-ppTG20, and F(SG)4TP10 were stable and nonantigenic; thus, these sequences were introduced as the best CPP candidates for the intracellular delivery of ADI. In addition, the proposed CPPs had appropriate positive charge and lengths for an efficient cellular uptake.

Conclusion: These three introduced CPPs not only are appropriate for the intracellular delivery of ADI, but also can overcome the limitation of its therapeutic application, including short half-life and antigenicity.

Keywords: Cell penetrating peptide, intracellular delivery, arginine deiminase, therapeutic protein, bioinformatics, in silico.

[1]
Dinca, A.; Chien, W.M.; Chin, M.T. Intracellular delivery of proteins with cell-penetrating peptides for therapeutic uses in human disease. Int. J. Mol. Sci., 2016, 17(2), 263.
[http://dx.doi.org/10.3390/ijms17020263] [PMID: 26907261]
[2]
Kristensen, M.; Birch, D.; Mørck Nielsen, H. Applications and challenges for use of cell-penetrating peptides as delivery vectors for peptide and protein cargos. Int. J. Mol. Sci., 2016, 17(2), 185.
[http://dx.doi.org/10.3390/ijms17020185] [PMID: 26840305]
[3]
Guidotti, G.; Brambilla, L.; Rossi, D. Cell-penetrating peptides: From basic research to clinics. Trends Pharmacol. Sci., 2017, 38(4), 406-424.
[http://dx.doi.org/10.1016/j.tips.2017.01.003] [PMID: 28209404]
[4]
Derakhshankhah, H.; Jafari, S. Cell penetrating peptides: A concise review with emphasis on biomedical applications. Biomed. Pharmacother., 2018, 108, 1090-1096.
[http://dx.doi.org/10.1016/j.biopha.2018.09.097] [PMID: 30372809]
[5]
Borrelli, A.; Tornesello, A.L.; Tornesello, M.L.; Buonaguro, F.M. Cell penetrating peptides as molecular carriers for anti-cancer agents. Molecules, 2018, 23(2), 295.
[http://dx.doi.org/10.3390/molecules23020295] [PMID: 29385037]
[6]
Klimpel, A.; Lützenburg, T.; Neundorf, I. Recent advances of anti-cancer therapies including the use of cell-penetrating peptides. Curr. Opin. Pharmacol., 2019, 47, 8-13.
[http://dx.doi.org/10.1016/j.coph.2019.01.003] [PMID: 30771730]
[7]
Jauset, T.; Beaulieu, M.E. Bioactive cell penetrating peptides and proteins in cancer: A bright future ahead. Curr. Opin. Pharmacol., 2019, 47, 133-140.
[http://dx.doi.org/10.1016/j.coph.2019.03.014] [PMID: 31048179]
[8]
Habault, J.; Poyet, J.L. Recent advances in cell penetrating peptide-based anticancer therapies. Molecules, 2019, 24(5)E927
[http://dx.doi.org/10.3390/molecules24050927] [PMID: 30866424]
[9]
Milletti, F. Cell-penetrating peptides: Classes, origin, and current landscape. Drug Discov. Today, 2012, 17(15-16), 850-860.
[http://dx.doi.org/10.1016/j.drudis.2012.03.002] [PMID: 22465171]
[10]
Lindgren, M.; Langel, U. Classes and prediction of cell-penetrating peptides. Methods Mol. Biol., 2011, 683, 3-19.
[http://dx.doi.org/10.1007/978-1-60761-919-2_1] [PMID: 21053118]
[11]
Fischer, R.; Fotin-Mleczek, M.; Hufnagel, H.; Brock, R. Break on through to the other side-biophysics and cell biology shed light on cell-penetrating peptides. ChemBioChem, 2005, 6(12), 2126-2142.
[http://dx.doi.org/10.1002/cbic.200500044] [PMID: 16254940]
[12]
Verdurmen, W.P.; Bovee-Geurts, P.H.; Wadhwani, P.; Ulrich, A.S.; Hällbrink, M.; van Kuppevelt, T.H.; Brock, R. Preferential uptake of L- versus D-amino acid cell-penetrating peptides in a cell type-dependent manner. Chem. Biol., 2011, 18(8), 1000-1010.
[http://dx.doi.org/10.1016/j.chembiol.2011.06.006] [PMID: 21867915]
[13]
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]
[14]
Copolovici, D.M.; Langel, K.; Eriste, E.; Langel, Ü. Cell-penetrating peptides: design, synthesis, and applications. ACS Nano, 2014, 8(3), 1972-1994.
[http://dx.doi.org/10.1021/nn4057269] [PMID: 24559246]
[15]
Böhmová, E.; Machová, D.; Pechar, M.; Pola, R.; Venclíková, K.; Janoušková, O.; Etrych, T. Cell-penetrating peptides: a useful tool for the delivery of various cargoes into cells. Physiol. Res., 2018, 67(Suppl. 2), S267-S279.
[PMID: 30379549]
[16]
McClorey, G.; Banerjee, S. Cell-penetrating peptides to enhance delivery of oligonucleotide-based therapeutics. Biomedicines, 2018, 6(2), 51.
[http://dx.doi.org/10.3390/biomedicines6020051] [PMID: 29734750]
[17]
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]
[18]
Silva, S.; Almeida, A.J.; Vale, N. Combination of cell-penetrating peptides with nanoparticles for therapeutic application: A review. Biomolecules, 2019, 9(1), 22.
[http://dx.doi.org/10.3390/biom9010022] [PMID: 30634689]
[19]
Smith, D.W.; Ganaway, R.L.; Fahrney, D.E. Arginine deiminase from mycoplasma arthritidis. Structure-activity relationships among substrates and competitive inhibitors. J. Biol. Chem., 1978, 253(17), 6016-6020.
[PMID: 681336]
[20]
Ni, Y.; Schwaneberg, U.; Sun, Z-H. Arginine deiminase, a potential anti-tumor drug. Cancer Lett., 2008, 261(1), 1-11.
[http://dx.doi.org/10.1016/j.canlet.2007.11.038] [PMID: 18179862]
[21]
Zarei, M.; Rahbar, M.R.; Morowvat, M.H.; Nezafat, N.; Negahdaripour, M.; Berenjian, A.; Ghasemi, Y. Arginine deiminase: Current understanding and applications. Recent Pat. Biotechnol., 2019, 13(2), 124-136.
[http://dx.doi.org/10.2174/1872208313666181220121400] [PMID: 30569861]
[22]
Qiu, F.; Huang, J.; Sui, M. Targeting arginine metabolism pathway to treat arginine-dependent cancers. Cancer Lett., 2015, 364(1), 1-7.
[http://dx.doi.org/10.1016/j.canlet.2015.04.020] [PMID: 25917076]
[23]
Riess, C.; Shokraie, F.; Classen, C.F.; Kreikemeyer, B.; Fiedler, T.; Junghanss, C.; Maletzki, C. Arginine-depleting enzymes - an increasingly recognized treatment strategy for therapy-refractory malignancies. Cell. Physiol. Biochem., 2018, 51(2), 854-870.
[http://dx.doi.org/10.1159/000495382] [PMID: 30466103]
[24]
Pokrovsky, V.S.; Chepikova, O.E.; Davydov, D.Z.; Zamyatnin, A.A., Jr; Lukashev, A.N.; Lukasheva, E.V. Amino acid degrading enzymes and their application in cancer therapy. Curr. Med. Chem., 2019, 26(3), 446-464.
[http://dx.doi.org/10.2174/0929867324666171006132729] [PMID: 28990519]
[25]
Kremer, J.C.; Van Tine, B.A. Therapeutic arginine starvation in ASS1-deficient cancers inhibits the Warburg effect. Mol. Cell. Oncol., 2017, 4(3)e1295131
[http://dx.doi.org/10.1080/23723556.2017.1295131] [PMID: 28616574]
[26]
Abou-Alfa, G.K.; Qin, S.; Ryoo, B.Y.; Lu, S.N.; Yen, C.J.; Feng, Y.H.; Lim, H.Y.; Izzo, F.; Colombo, M.; Sarker, D.; Bolondi, L.; Vaccaro, G.; Harris, W.P.; Chen, Z.; Hubner, R.A.; Meyer, T.; Sun, W.; Harding, J.J.; Hollywood, E.M.; Ma, J.; Wan, P.J.; Ly, M.; Bomalaski, J.; Johnston, A.; Lin, C.C.; Chao, Y.; Chen, L.T. Phase III randomized study of second line ADI-PEG 20 plus best supportive care versus placebo plus best supportive care in patients with advanced hepatocellular carcinoma. Ann. Oncol., 2018, 29(6), 1402-1408.
[http://dx.doi.org/10.1093/annonc/mdy101] [PMID: 29659672]
[27]
Shen, L.J.; Shen, W.C. Drug evaluation: ADI-PEG-20--a PEGylated arginine deiminase for arginine-auxotrophic cancers. Curr. Opin. Mol. Ther., 2006, 8(3), 240-248.
[PMID: 16774044]
[28]
Miraki-Moud, F.; Ghazaly, E.; Ariza-McNaughton, L.; Hodby, K.A.; Clear, A.; Anjos-Afonso, F.; Liapis, K.; Grantham, M.; Sohrabi, F.; Cavenagh, J.; Bomalaski, J.S.; Gribben, J.G.; Szlosarek, P.W.; Bonnet, D.; Taussig, D.C. Arginine deprivation using pegylated arginine deiminase has activity against primary acute myeloid leukemia cells in vivo. Blood, 2015, 125(26), 4060-4068.
[http://dx.doi.org/10.1182/blood-2014-10-608133] [PMID: 25896651]
[29]
Ott, P.A.; Carvajal, R.D.; Pandit-Taskar, N.; Jungbluth, A.A.; Hoffman, E.W.; Wu, B.W.; Bomalaski, J.S.; Venhaus, R.; Pan, L.; Old, L.J.; Pavlick, A.C.; Wolchok, J.D. Phase I/II study of pegylated arginine deiminase (ADI-PEG 20) in patients with advanced melanoma. Invest. New Drugs, 2013, 31(2), 425-434.
[http://dx.doi.org/10.1007/s10637-012-9862-2] [PMID: 22864522]
[30]
Synakiewicz, A.; Stachowicz-Stencel, T.; Adamkiewicz-Drozynska, E. The role of arginine and the modified arginine deiminase enzyme ADI-PEG 20 in cancer therapy with special emphasis on Phase I/II clinical trials. Expert Opin. Investig. Drugs, 2014, 23(11), 1517-1529.
[http://dx.doi.org/10.1517/13543784.2014.934808] [PMID: 24965808]
[31]
Szlosarek, P.W.; Steele, J.P.; Nolan, L.; Gilligan, D.; Taylor, P.; Spicer, J.; Lind, M.; Mitra, S.; Shamash, J.; Phillips, M.M.; Luong, P.; Payne, S.; Hillman, P.; Ellis, S.; Szyszko, T.; Dancey, G.; Butcher, L.; Beck, S.; Avril, N.E.; Thomson, J.; Johnston, A.; Tomsa, M.; Lawrence, C.; Schmid, P.; Crook, T.; Wu, B.W.; Bomalaski, J.S.; Lemoine, N.; Sheaff, M.T.; Rudd, R.M.; Fennell, D.; Hackshaw, A. Arginine deprivation with pegylated arginine deiminase in patients with argininosuccinate synthetase 1-deficient malignant pleural mesothelioma: A randomized clinical trial. JAMA Oncol., 2017, 3(1), 58-66.
[http://dx.doi.org/10.1001/jamaoncol.2016.3049] [PMID: 27584578]
[32]
Long, Y.; Tsai, W.B.; Wangpaichitr, M.; Tsukamoto, T.; Savaraj, N.; Feun, L.G.; Kuo, M.T. Arginine deiminase resistance in melanoma cells is associated with metabolic reprogramming, glucose dependence, and glutamine addiction. Mol. Cancer Ther., 2013, 12(11), 2581-2590.
[http://dx.doi.org/10.1158/1535-7163.MCT-13-0302] [PMID: 23979920]
[33]
Alexandrou, C.; Al-Aqbi, S.S.; Higgins, J.A.; Boyle, W.; Karmokar, A.; Andreadi, C.; Luo, J.L.; Moore, D.A.; Viskaduraki, M.; Blades, M.; Murray, G.I.; Howells, L.M.; Thomas, A.; Brown, K.; Cheng, P.N.; Rufini, A. Sensitivity of colorectal cancer to arginine deprivation therapy is shaped by differential expression of urea cycle enzymes. Sci. Rep., 2018, 8(1), 12096.
[http://dx.doi.org/10.1038/s41598-018-30591-7] [PMID: 30108309]
[34]
Shen, L.J.; Lin, W.C.; Beloussow, K.; Shen, W.C. Resistance to the anti-proliferative activity of recombinant arginine deiminase in cell culture correlates with the endogenous enzyme, argininosuccinate synthetase. Cancer Lett., 2003, 191(2), 165-170.
[http://dx.doi.org/10.1016/S030-43835(02)00693-6] [PMID: 12618329]
[35]
Chang, K-Y.; Chiang, N-J.; Yen, C-J.; Wu, S-Y.; Chen, S-H.; Johnston, A.; Bomalaski, J.S.; Wu, B-W.; Chen, L-T. A phase Ib study of ADI-PEG 20 plus pembrolizumab in advanced solid cancers. Am. Soc. Clin. Oncol. J., 2018, 36(15), 2556.
[http://dx.doi.org/10.1200/JCO.2018.36.15_suppl.2556]
[36]
Lowery, M.A.; Yu, K.H.; Kelsen, D.P.; Harding, J.J.; Bomalaski, J.S.; Glassman, D.C.; Covington, C.M.; Brenner, R.; Hollywood, E.; Barba, A.; Johnston, A.; Liu, K.C.; Feng, X.; Capanu, M.; Abou-Alfa, G.K.; O’Reilly, E.M. A phase 1/1B trial of ADI-PEG 20 plus nab-paclitaxel and gemcitabine in patients with advanced pancreatic adenocarcinoma. Cancer, 2017, 123(23), 4556-4565.
[http://dx.doi.org/10.1002/cncr.30897] [PMID: 28832976]
[37]
Tomlinson, B.K.; Thomson, J.A.; Bomalaski, J.S.; Diaz, M.; Akande, T.; Mahaffey, N.; Li, T.; Dutia, M.P.; Kelly, K.; Gong, I.Y.; Semrad, T.; Gandara, D.R.; Pan, C.X.; Lara, P.N., Jr; Phase, I. Phase I trial of arginine deprivation therapy with ADI-PEG 20 plus docetaxel in patients with advanced malignant solid tumors. Clin. Cancer Res., 2015, 21(11), 2480-2486.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-2610] [PMID: 25739672]
[38]
Beddowes, E.; Spicer, J.; Chan, P.Y.; Khadeir, R.; Corbacho, J.G.; Repana, D.; Steele, J.P.; Schmid, P.; Szyszko, T.; Cook, G.; Diaz, M.; Feng, X.; Johnston, A.; Thomson, J.; Sheaff, M.; Wu, B.W.; Bomalaski, J.; Pacey, S.; Szlosarek, P.W. Phase 1 dose-escalation study of pegylated arginine deiminase, cisplatin, and pemetrexed in patients with argininosuccinate synthetase 1-deficient thoracic cancers. J. Clin. Oncol., 2017, 35(16), 1778-1785.
[http://dx.doi.org/10.1200/JCO.2016.71.3230] [PMID: 28388291]
[39]
Prudner, B.C.; Rathore, R.; Robinson, A.M.; Godec, A.J.; Chang, S.F.; Hawkins, W.G.; Hirbe, A.C.; Van Tine, B.A. Arginine starvation and docetaxel induce c-Myc-driven hENT1 surface expression to overcome gemcitabine resistance in ASS1-negative tumors. Clin. Cancer Res., 2019, 25(16), 5122-5134.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-0206] [PMID: 31113844]
[40]
McAlpine, J.A.; Lu, H-T.; Wu, K.C.; Knowles, S.K.; Thomson, J.A. Down-regulation of argininosuccinate synthetase is associated with cisplatin resistance in hepatocellular carcinoma cell lines: Implications for PEGylated arginine deiminase combination therapy. BMC Cancer, 2014, 14(1), 621.
[http://dx.doi.org/10.1186/1471-2407-14-621] [PMID: 25164070]
[41]
Thongkum, A.; Wu, C.; Li, Y.Y.; Wangpaichitr, M.; Navasumrit, P.; Parnlob, V.; Sricharunrat, T.; Bhudhisawasdi, V.; Ruchirawat, M.; Savaraj, N. The combination of arginine deprivation and 5-fluorouracil improves therapeutic efficacy in argininosuccinate synthetase negative hepatocellular carcinoma. Int. J. Mol. Sci., 2017, 18(6)E1175
[http://dx.doi.org/10.3390/ijms18061175] [PMID: 28587170]
[42]
Wu, F.L.; Yeh, T.H.; Chen, Y.L.; Chiu, Y.C.; Cheng, J.C.; Wei, M.F.; Shen, L.J. Intracellular delivery of recombinant Arginine Deiminase (rADI) by heparin-binding hemagglutinin adhesion peptide restores sensitivity in rADI-resistant cancer cells. Mol. Pharm., 2014, 11(8), 2777-2786.
[http://dx.doi.org/10.1021/mp5001372] [PMID: 24950134]
[43]
Yeh, T.H.; Chen, Y.R.; Chen, S.Y.; Shen, W.C.; Ann, D.K.; Zaro, J.L.; Shen, L.J. Selective intracellular delivery of recombinant Arginine Deiminase (ADI) using pH-sensitive cell penetrating peptides to overcome ADI resistance in hypoxic breast cancer cells. Mol. Pharm., 2016, 13(1), 262-271.
[http://dx.doi.org/10.1021/acs.molpharmaceut.5b00706] [PMID: 26642391]
[44]
Manica, N.; Navid, N.; Nasim, H.; Seyyed Soheil, R.; Mohammad Hossein, M.; Younes, G. In silico study of different signal peptides for secretory production of interleukin-11 in Escherichia coli. Curr. Proteomics, 2017, 14(2), 112-121.
[http://dx.doi.org/10.2174/1570164614666170106110848]
[45]
Chou, K-C. Modeling the tertiary structure of human cathepsin-E. Biochem. Biophys. Res. Commun., 2005, 331(1), 56-60.
[http://dx.doi.org/10.1016/j.bbrc.2005.03.123] [PMID: 15845357]
[46]
Chou, K.C. Insights from modeling three-dimensional structures of the human potassium and sodium channels. J. Proteome Res., 2004, 3(4), 856-861.
[http://dx.doi.org/10.1021/pr049931q] [PMID: 15359741]
[47]
Chou, K.C. Insights from modeling the tertiary structure of human BACE2. J. Proteome Res., 2004, 3(5), 1069-1072.
[http://dx.doi.org/10.1021/pr049905s] [PMID: 15473697]
[48]
Zarei, M.; Nezafat, N.; Morowvat, M.H.; Dehshahri, A.; Ghoshoon, M.B.; Berenjian, A.; Ghasemi, Y. Medium optimization for recombinant soluble arginine deiminase expression in Escherichia coli using response surface methodology. Curr. Pharm. Biotechnol., 2017, 18(11), 935-941.
[http://dx.doi.org/10.2174/1389201019666180115144752] [PMID: 29336257]
[49]
Takaku, H.; Matsumoto, M.; Misawa, S.; Miyazaki, K. Anti-tumor activity of arginine deiminase from mycoplasma argini and its growth-inhibitory mechanism. Jpn. J. Cancer Res., 1995, 86(9), 840-846.
[http://dx.doi.org/10.1111/j.1349-7006.1995.tb03094.x] [PMID: 7591961]
[50]
Zarei, M.; Nezafat, N.; Rahbar, M.R.; Negahdaripour, M.; Sabetian, S.; Morowvat, M.H.; Ghasemi, Y. Decreasing the immunogenicity of arginine deiminase enzyme via structure-based computational analysis. J. Biomol. Struct. Dyn., 2019, 37(2), 523-536.
[http://dx.doi.org/10.1080/07391102.2018.1431151] [PMID: 29363409]
[51]
Agrawal, P.; Bhalla, S.; Usmani, S.S.; Singh, S.; Chaudhary, K.; Raghava, G.P.; Gautam, A. CPPsite 2.0: a repository of experimentally validated cell-penetrating peptides. Nucleic Acids Res., 2016, 44(D1), D1098-D1103.
[http://dx.doi.org/10.1093/nar/gkv1266] [PMID: 26586798]
[52]
Consortium, U. UniProt: the universal protein knowledgebase. Nucleic Acids Res., 2017, 45(D1), D158-D169.
[http://dx.doi.org/10.1093/nar/gkw1099] [PMID: 27899622]
[53]
Gautam, A.; Chaudhary, K.; Kumar, R.; Sharma, A.; Kapoor, P.; Tyagi, A.; Raghava, G.P. In silico approaches for designing highly effective cell penetrating peptides. J. Transl. Med., 2013, 11(1), 74.
[http://dx.doi.org/10.1186/1479-5876-11-74] [PMID: 23517638]
[54]
Walker, J.M. The proteomics protocols handbook; Springer, Humana Press, 2005, pp. 1-998.
[http://dx.doi.org/10.1385/1592598900]
[55]
Gasteiger, E.; Hoogland, C.; Gattiker, A.; Wilkins, M.R.; Appel, R.D.; Bairoch, A. Protein identification and analysis tools on the ExPASy server. The proteomics protocols handbook; Humana Press, 2005, pp. 571-607.
[http://dx.doi.org/10.1385/1-59259-890-0:571]
[56]
Doytchinova, I.A.; Flower, D.R. VaxiJen: a server for prediction of protective antigens, tumour antigens and subunit vaccines. BMC Bioinformatics, 2007, 8(1), 4.
[http://dx.doi.org/10.1186/1471-2105-8-4] [PMID: 17207271]
[57]
Kolaskar, A.S.; Tongaonkar, P.C. A semi-empirical method for prediction of antigenic determinants on protein antigens. FEBS Lett., 1990, 276(1-2), 172-174.
[http://dx.doi.org/10.1016/0014-5793(90)80535-Q] [PMID: 1702393]
[58]
Ko, J.; Park, H.; Heo, L.; Seok, C. Galaxy WEB server for protein structure prediction and refinement. Nucleic Acids Res.,, 2012, 40(Web Server issue), W294-7.
[http://dx.doi.org/10.1093/nar/gks493] [PMID: 22649060]
[59]
Chen, V.B.; Arendall, W.B., III; Headd, J.J.; Keedy, D.A.; Immormino, R.M.; Kapral, G.J.; Murray, L.W.; Richardson, J.S.; Richardson, D.C. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr., 2010, 66(Pt 1), 12-21.
[http://dx.doi.org/10.1107/S0907444909042073] [PMID: 20057044]
[60]
Harasawa, R.; Koshimizu, K.; Kitagawa, M.; Asada, K.; Kato, I. Nucleotide sequence of the arginine deiminase gene of Mycoplasma hominis. Microbiol. Immunol., 1992, 36(6), 661-665.
[http://dx.doi.org/10.1111/j.1348-0421.1992.tb02068.x] [PMID: 1522817]
[61]
Bailey, T.L.; Boden, M.; Buske, F.A.; Frith, M.; Grant, C.E.; Clementi, L.; Ren, J.; Li, W.W.; Noble, W.S. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res.,, 2009, 37(Web Server issue), W202-208.
[http://dx.doi.org/10.1093/nar/gkp335]
[62]
Rashid, M.; Saha, S.; Raghava, G.P. Support vector machine-based method for predicting subcellular localization of mycobacterial proteins using evolutionary information and motifs. BMC Bioinformatics, 2007, 8, 337.
[http://dx.doi.org/10.1186/1471-2105-8-337] [PMID: 17854501]
[63]
Ma, J.; Xu, J.; Guan, L.; Hu, T.; Liu, Q.; Xiao, J.; Zhang, Y. Cell-penetrating peptides mediated protein cross-membrane delivery and its use in bacterial vector vaccine. Fish Shellfish Immunol., 2014, 39(1), 8-16.
[http://dx.doi.org/10.1016/j.fsi.2014.04.003] [PMID: 24746937]
[64]
Sayers, E.J.; Cleal, K.; Eissa, N.G.; Watson, P.; Jones, A.T. Distal phenylalanine modification for enhancing cellular delivery of fluorophores, proteins and quantum dots by cell penetrating peptides. J. Control. Release, 2014, 195, 55-62.
[http://dx.doi.org/10.1016/j.jconrel.2014.07.055] [PMID: 25108152]
[65]
Vasconcelos, L.; Madani, F.; Arukuusk, P.; Pärnaste, L.; Gräslund, A.; Langel, U. Effects of cargo molecules on membrane perturbation caused by transportan10 based cell-penetrating peptides. Biochim. Biophys. Acta, 2014, 1838(12), 3118-3129.
[http://dx.doi.org/10.1016/j.bbamem.2014.08.011] [PMID: 25135660]
[66]
Trabulo, S.; Cardoso, A.L.; Mano, M.; De Lima, M.C.P. Cell-penetrating peptides-mechanisms of cellular uptake and generation of delivery systems. Pharmaceuticals (Basel), 2010, 3(4), 961-993.
[http://dx.doi.org/10.3390/ph3040961] [PMID: 27713284]
[67]
Guterstam, P.; Madani, F.; Hirose, H.; Takeuchi, T.; Futaki, S.; El Andaloussi, S.; Gräslund, A.; Langel, U. Elucidating cell-penetrating peptide mechanisms of action for membrane interaction, cellular uptake, and translocation utilizing the hydrophobic counter-anion pyrenebutyrate. Biochim. Biophys. Acta, 2009, 1788(12), 2509-2517.
[http://dx.doi.org/10.1016/j.bbamem.2009.09.014] [PMID: 19796627]
[68]
Ichimizu, S.; Watanabe, H.; Maeda, H.; Hamasaki, K.; Ikegami, K.; Chuang, V.T.G.; Kinoshita, R.; Nishida, K.; Shimizu, T.; Ishima, Y.; Ishida, T.; Seki, T.; Katsuki, H.; Futaki, S.; Otagiri, M.; Maruyama, T. Cell-penetrating mechanism of intracellular targeting albumin: contribution of macropinocytosis induction and endosomal escape. J. Control. Release, 2019, 304, 156-163.
[http://dx.doi.org/10.1016/j.jconrel.2019.05.015] [PMID: 31082432]
[69]
Zorko, M.; Langel, U. Cell-penetrating peptides: Mechanism and kinetics of cargo delivery. Adv. Drug Deliv. Rev., 2005, 57(4), 529-545.
[http://dx.doi.org/10.1016/j.addr.2004.10.010] [PMID: 15722162]
[70]
Gestin, M.; Dowaidar, M.; Langel, Ü. Uptake mechanism of cell-penetrating peptides. Adv. Exp. Med. Biol., 2017, 1030, 255-264.
[http://dx.doi.org/10.1007/978-3-319-66095-0_11] [PMID: 29081057]
[71]
Brasseur, R.; Divita, G. Happy birthday cell penetrating peptides: Already 20 years. Biochim. Biophys. Acta, 2010, 1798(12), 2177-2181.
[http://dx.doi.org/10.1016/j.bbamem.2010.09.001] [PMID: 20826125]
[72]
Hansen, M.; Kilk, K.; Langel, U. Predicting cell-penetrating peptides. Adv. Drug Deliv. Rev., 2008, 60(4-5), 572-579.
[http://dx.doi.org/10.1016/j.addr.2007.09.003] [PMID: 18045726]
[73]
Stalmans, S.; Wynendaele, E.; Bracke, N.; Gevaert, B.; D’Hondt, M.; Peremans, K.; Burvenich, C.; De Spiegeleer, B. Chemical-functional diversity in cell-penetrating peptides. PLoS One, 2013, 8(8)e71752
[http://dx.doi.org/10.1371/journal.pone.0071752] [PMID: 23951237]
[74]
Ramaker, K.; Henkel, M.; Krause, T.; Röckendorf, N.; Frey, A. Cell penetrating peptides: A comparative transport analysis for 474 sequence motifs. Drug Deliv., 2018, 25(1), 928-937.
[http://dx.doi.org/10.1080/10717544.2018.1458921] [PMID: 29656676]


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VOLUME: 17
ISSUE: 2
Year: 2020
Page: [117 - 131]
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DOI: 10.2174/1570164616666190701120351
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