Cell-Penetrating Peptides: As a Promising Theranostics Strategy to Circumvent the Blood-Brain Barrier for CNS Diseases

Author(s): Behrang Shiri Varnamkhasti, Samira Jafari, Fereshteh Taghavi, Loghman Alaei, Zhila Izadi, Alireza Lotfabadi, Mojtaba Dehghanian, Mehdi Jaymand, Hossein Derakhshankhah*, Ali Akbar Saboury*

Journal Name: Current Drug Delivery

Volume 17 , Issue 5 , 2020

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Graphical Abstract:


Abstract:

The passage of therapeutic molecules across the Blood-Brain Barrier (BBB) is a profound challenge for the management of the Central Nervous System (CNS)-related diseases. The ineffectual nature of traditional treatments for CNS disorders led to the abundant endeavor of researchers for the design the effective approaches in order to bypass BBB during recent decades. Cell-Penetrating Peptides (CPPs) were found to be one of the promising strategies to manage CNS disorders. CPPs are short peptide sequences with translocation capacity across the biomembrane. With special regard to their two key advantages like superior permeability as well as low cytotoxicity, these peptide sequences represent an appropriate solution to promote therapeutic/theranostic delivery into the CNS. This scenario highlights CPPs with specific emphasis on their applicability as a novel theranostic delivery system into the brain.

Keywords: Cell-penetrating peptide, blood-brain barrier, theranostics, central nervous system, drug delivery, translocation.

[1]
Saunders, N.R.; Habgood, M.D.; Møllgård, K.; Dziegielewska, K.M. The biological significance of brain barrier mechanisms: help or hindrance in drug delivery to the central nervous system? F1000 Res., 2016, 5, 5.
[http://dx.doi.org/10.12688/f1000research.7378.1] [PMID: 26998242]
[2]
Spencer, B.; Trinh, I.; Rockenstein, E.; Mante, M.; Florio, J.; Adame, A.; El-Agnaf, O.M.A.; Kim, C.; Masliah, E.; Rissman, R.A. Systemic peptide mediated delivery of an siRNA targeting α-syn in the CNS ameliorates the neurodegenerative process in a transgenic model of Lewy body disease. Neurobiol. Dis., 2019, 127, 163-177.
[http://dx.doi.org/10.1016/j.nbd.2019.03.001] [PMID: 30849508]
[3]
Kisała, J.; Hęclik, K.I.; Pogocki, K.; Pogocki, D. Essentials and perspectives of computational modelling assistance for CNS-oriented nanoparticle-based drug delivery systems. Curr. Med. Chem., 2018, 25(42), 5894-5913.
[http://dx.doi.org/10.2174/0929867325666180517095742] [PMID: 29768999]
[4]
Keaney, J.; Campbell, M. The dynamic blood-brain barrier. FEBS J., 2015, 282(21), 4067-4079.
[http://dx.doi.org/10.1111/febs.13412] [PMID: 26277326]
[5]
Calias, P.; Pan, J.; Powell, J.; Charnas, L.; McCauley, T.; Wright, T.L.; Pfeifer, R.; Shahrokh, Z. CNS delivery of therapeutic agents., Google Patents WO2011163648A1. 2016.
[6]
Battaglia, L.; Panciani, P.P.; Muntoni, E.; Capucchio, M.T.; Biasibetti, E.; De Bonis, P.; Mioletti, S.; Fontanella, M.; Swaminathan, S. Lipid nanoparticles for intranasal administration: application to nose-to-brain delivery. Expert Opin. Drug Deliv., 2018, 15(4), 369-378.
[http://dx.doi.org/10.1080/17425247.2018.1429401] [PMID: 29338427]
[7]
Park, K. Optimal nanoparticle design for effective transport through the blood-brain barrier. J. Control. Release, 2019, 295, 290.
[http://dx.doi.org/10.1016/j.jconrel.2019.01.024] [PMID: 30704674]
[8]
Gharbavi, M.; Amani, J.; Kheiri-Manjili, H.; Danafar, H.; Sharafi, A. Niosome: a promising nanocarrier for natural drug delivery through blood-brain barrier. Adv. Pharmacol. Sci., 2018, 2018, 6847-6971.
[http://dx.doi.org/10.1155/2018/6847971] [PMID: 30651728]
[9]
Zou, L.L.; Ma, J.L.; Wang, T.; Yang, T-B.; Liu, C-B. Cell-penetrating Peptide-mediated therapeutic molecule delivery into the central nervous system. Curr. Neuropharmacol., 2013, 11(2), 197-208.
[http://dx.doi.org/10.2174/1570159X11311020006] [PMID: 23997754]
[10]
Kanazawa, T.; Akiyama, F.; Kakizaki, S.; Takashima, Y.; Seta, Y. Delivery of siRNA to the brain using a combination of nose-to-brain delivery and cell-penetrating peptide-modified nano-micelles. Biomaterials, 2013, 34(36), 9220-9226.
[http://dx.doi.org/10.1016/j.biomaterials.2013.08.036] [PMID: 23992922]
[11]
Bera, S.; Bhunia, A. Cell-penetrating peptides as theranostics against impaired blood-brain barrier permeability: implications for pathogenesis and therapeutic treatment of neurodegenerative disease. Blood-Brain Barrier; Springer, 2019, pp. 115-136.
[12]
Persidsky, Y.; Ramirez, S.H.; Haorah, J.; Kanmogne, G.D. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J. Neuroimmune Pharmacol., 2006, 1(3), 223-236.
[http://dx.doi.org/10.1007/s11481-006-9025-3] [PMID: 18040800]
[13]
Dong, X. Current strategies for brain drug delivery. Theranostics, 2018, 8(6), 1481-1493.
[http://dx.doi.org/10.7150/thno.21254] [PMID: 29556336]
[14]
Xia, H.; Gao, X.; Gu, G.; Liu, Z.; Zeng, N.; Hu, Q.; Song, Q.; Yao, L.; Pang, Z.; Jiang, X.; Chen, J.; Chen, H. Low molecular weight protamine-functionalized nanoparticles for drug delivery to the brain after intranasal administration. Biomaterials, 2011, 32(36), 9888-9898.
[http://dx.doi.org/10.1016/j.biomaterials.2011.09.004] [PMID: 21937105]
[15]
Halle, B.; Mongelard, K.; Poulsen, F.R. Convection-enhanced drug delivery for glioblastoma: a systematic review focused on methodological differences in the use of the convection-enhanced delivery method. Asian J. Neurosurg., 2019, 14(1), 5-14.
[http://dx.doi.org/10.4103/ajns.AJNS_302_17] [PMID: 30937002]
[16]
Stine, C.A.; Munson, J.M. Convection enhanced delivery: connection to and impact of interstitial fluid flow. Front. Oncol., 2019, 9, 966.
[http://dx.doi.org/10.3389/fonc.2019.00966] [PMID: 31632905]
[17]
Bankiewicz, K.S.; Eberling, J.L.; Kohutnicka, M.; Jagust, W.; Pivirotto, P.; Bringas, J.; Cunningham, J.; Budinger, T.F.; Harvey-White, J. Convection-enhanced delivery of AAV vector in parkinsonian monkeys; in vivo detection of gene expression and restoration of dopaminergic function using pro-drug approach. Exp. Neurol., 2000, 164(1), 2-14.
[http://dx.doi.org/10.1006/exnr.2000.7408] [PMID: 10877910]
[18]
Lai, C-H.; Kuo, K-H.; Leo, J.M. Critical role of actin in modulating BBB permeability. Brain Res. Brain Res. Rev., 2005, 50(1), 7-13.
[http://dx.doi.org/10.1016/j.brainresrev.2005.03.007] [PMID: 16291072]
[19]
Aryal, M.; Arvanitis, C.D.; Alexander, P.M.; McDannold, N. Ultrasound-mediated blood-brain barrier disruption for targeted drug delivery in the central nervous system. Adv. Drug Deliv. Rev., 2014, 72, 94-109.
[http://dx.doi.org/10.1016/j.addr.2014.01.008] [PMID: 24462453]
[20]
Choi, M.; Ku, T.; Chong, K.; Yoon, J.; Choi, C. Minimally invasive molecular delivery into the brain using optical modulation of vascular permeability. Proc. Natl. Acad. Sci. USA, 2011, 108(22), 9256-9261.
[http://dx.doi.org/10.1073/pnas.1018790108] [PMID: 21576460]
[21]
Yuan, H.; Wilson, C.M.; Xia, J.; Doyle, S.L.; Li, S.; Fales, A.M.; Liu, Y.; Ozaki, E.; Mulfaul, K.; Hanna, G.; Palmer, G.M.; Wang, L.V.; Grant, G.A.; Vo-Dinh, T. Plasmonics-enhanced and optically modulated delivery of gold nanostars into brain tumor. Nanoscale, 2014, 6(8), 4078-4082.
[http://dx.doi.org/10.1039/C3NR06770J] [PMID: 24619405]
[22]
Oller-Salvia, B.; Sánchez-Navarro, M.; Giralt, E.; Teixidó, M. Blood-brain barrier shuttle peptides: an emerging paradigm for brain delivery. Chem. Soc. Rev., 2016, 45(17), 4690-4707.
[http://dx.doi.org/10.1039/C6CS00076B] [PMID: 27188322]
[23]
Pavan, B.; Dalpiaz, A.; Ciliberti, N.; Biondi, C.; Manfredini, S.; Vertuani, S. Progress in drug delivery to the central nervous system by the prodrug approach. Molecules, 2008, 13(5), 1035-1065.
[http://dx.doi.org/10.3390/molecules13051035] [PMID: 18560328]
[24]
Kumar, H.; Mishra, G.; Sharma, A.K.; Gothwal, A.; Kesharwani, P.; Gupta, U. Intranasal drug delivery: a non-invasive approach for the better delivery of neurotherapeutics. Pharm. Nanotechnol., 2017, 5(3), 203-214.
[PMID: 28521670]
[25]
Quintana, D.S.; Steen, N.E.; Andreassen, O.A. The promise of intranasal esketamine as a novel and effective antidepressant. JAMA Psychiatry, 2018, 75(2), 123-124.
[http://dx.doi.org/10.1001/jamapsychiatry.2017.3738] [PMID: 29282452]
[26]
Barone, E.; Tramutola, A.; Triani, F.; Calcagnini, S.; Di Domenico, F.; Ripoli, C.; Gaetani, S.; Grassi, C.; Butterfield, D.A.; Cassano, T.; Perluigi, M. Biliverdin reductase-A mediates the beneficial effects of intranasal insulin in Alzheimer disease. Mol. Neurobiol., 2019, 56(4), 2922-2943.
[http://dx.doi.org/10.1007/s12035-018-1231-5] [PMID: 30073505]
[27]
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]
[28]
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]
[29]
Regberg, J.; Srimanee, A.; Langel, U. Applications of cell-penetrating peptides for tumor targeting and future cancer therapies. Pharmaceuticals (Basel), 2012, 5(9), 991-1007.
[http://dx.doi.org/10.3390/ph5090991] [PMID: 24280701]
[30]
Madani, F.; Lindberg, S.; Langel, U.; Futaki, S.; Gräslund, A. Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys., 2011, 2011, 414729
[http://dx.doi.org/10.1155/2011/414729] [PMID: 21687343]
[31]
(a) Conner, S.D.; Schmid, S.L. Regulated portals of entry into the cell. Nature, 2003, 422(6927), 37-44.
[http://dx.doi.org/10.1038/nature01451] [PMID: 12621426]
(b) Rizzuti, M.; Nizzardo, M.; Zanetta, C.; Ramirez, A.; Corti, S. Therapeutic applications of the cell-penetrating HIV-1 Tat peptide. Drug Discov. Today, 2015, 20(1), 76-85.
[http://dx.doi.org/10.1016/j.drudis.2014.09.017] [PMID: 25277319]
[32]
Yan, L.; Wang, H.; Jiang, Y.; Liu, J.; Wang, Z.; Yang, Y.; Huang, S.; Huang, Y. Cell-penetrating peptide-modified PLGA nanoparticles for enhanced nose-to-brain macromolecular delivery. Macromol. Res., 2013, 21(4), 435-441.
[http://dx.doi.org/10.1007/s13233-013-1029-2]
[33]
Chaudhary, S.; Smith, C.A.; Del Pino, P.; de la Fuente, J.M.; Mullin, M.; Hursthouse, A.; Stirling, D.; Berry, C.C. Elucidating the function of penetratin and a static magnetic field in cellular uptake of magnetic nanoparticles. Pharmaceuticals (Basel), 2013, 6(2), 204-222.
[http://dx.doi.org/10.3390/ph6020204] [PMID: 24275948]
[34]
(a) Heitz, F.; Morris, M.C.; Divita, G. Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics. Br. J. Pharmacol., 2009, 157(2), 195-206.
[http://dx.doi.org/10.1111/j.1476-5381.2009.00057.x] [PMID: 19309362]
(b) 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]
[35]
Mendes, M.; Sousa, J.J.; Pais, A.; Vitorino, C. Targeted theranostic nanoparticles for brain tumor treatment. Pharmaceutics, 2018, 10(4), 181.
[http://dx.doi.org/10.3390/pharmaceutics10040181] [PMID: 30304861]
[36]
Prieto, C.; Linares, I. Nanoparticles and nanothermia for malignant brain tumors, a suggestion of treatment for further investigations. Rep. Pract. Oncol. Radiother., 2018, 23(5), 474-480.
[http://dx.doi.org/10.1016/j.rpor.2018.08.001] [PMID: 30263017]
[37]
Zhu, Y.; Jiang, Y.; Meng, F.; Deng, C.; Cheng, R.; Zhang, J.; Feijen, J.; Zhong, Z. Highly efficacious and specific anti-glioma chemotherapy by tandem nanomicelles co-functionalized with brain tumor-targeting and cell-penetrating peptides. J. Control. Release, 2018, 278, 1-8.
[http://dx.doi.org/10.1016/j.jconrel.2018.03.025] [PMID: 29596873]
[38]
Joshi, S.; Cooke, J.R.N.; Ellis, J.A.; Emala, C.W.; Bruce, J.N. Targeting brain tumors by intra-arterial delivery of cell-penetrating peptides: a novel approach for primary and metastatic brain malignancy. J. Neurooncol., 2017, 135(3), 497-506.
[http://dx.doi.org/10.1007/s11060-017-2615-5] [PMID: 28875440]
[39]
Ge, J.; Zhang, Q.; Zeng, J.; Gu, Z.; Gao, M. Radiolabeling nanomaterials for multimodality imaging: New insights into nuclear medicine and cancer diagnosis. Biomaterials, 2020, 228, 119553
[http://dx.doi.org/10.1016/j.biomaterials.2019.119553] [PMID: 31689672]
[40]
Salvanou, E.A.; Bouziotis, P.; Tsoukalas, C. Radiolabeled nano-particles in nuclear oncology. Adv. Nano Res., 2018, 1(1), 38-55.
[http://dx.doi.org/10.21467/anr.1.1.38-55]
[41]
Wang, L.; Filer, J.E.; Lorenz, M.M.; Henry, C.S.; Dandy, D.S.; Geiss, B.J. An ultra-sensitive capacitive microwire sensor for pathogen specific serum antibody responses. Biosens. Bioelectron., 2019, 131, 46-52.
[http://dx.doi.org/10.1016/j.bios.2019.01.040] [PMID: 30822687]
[42]
Graham, W.V.; Bonito-Oliva, A.; Agostinelli, R.; Karim, R.; Deguzman, J.; Kelleher, K.; Petro, M.; Lindstrom, A-K.; Graff, C.; Wood, K.M. Discovery of conformation-sensitive anti-amyloid protofibril monoclonal antibodies using an engineered chaperone-like amy-loid binding protein. bioRxiv, 2019, 55, 8809.
[43]
Yang, S.; Li, L.; Yin, S.; Shang, Y.; Khan, M.U.Z.; He, X.; Yuan, L.; Gao, X.; Liu, X.; Cai, J. Single-domain antibodies as promising experimental tools in imaging and isolation of porcine epidemic diarrhea virus. Appl. Microbiol. Biotechnol., 2018, 102(20), 8931-8942.
[http://dx.doi.org/10.1007/s00253-018-9324-7] [PMID: 30143837]
[44]
Chen, S.; Cui, J.; Jiang, T.; Olson, E.S.; Cai, Q-Y.; Yang, M.; Wu, W.; Guthrie, J.M.; Robertson, J.D.; Lipton, S.A.; Ma, L.; Tsien, R.Y.; Gu, Z. Gelatinase activity imaged by activatable cell-penetrating peptides in cell-based and in vivo models of stroke. J. Cereb. Blood Flow Metab., 2017, 37(1), 188-200.
[http://dx.doi.org/10.1177/0271678X15621573] [PMID: 26681768]
[45]
(a) 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]
(b) Green, M.; Loewenstein, P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat transactivator protein. Cell, 1988, 55(6), 1179-1188.
[http://dx.doi.org/10.1016/0092-8674(88)90262-0] [PMID: 2849509]
[46]
Rothbard, J.B.; Garlington, S.; Lin, Q.; Kirschberg, T.; Kreider, E.; McGrane, P.L.; Wender, P.A.; Khavari, P.A. Conjugation of arginine oligomers to cyclosporin A facilitates topical delivery and inhibition of inflammation. Nat. Med., 2000, 6(11), 1253-1257.
[http://dx.doi.org/10.1038/81359] [PMID: 11062537]
[47]
Lebleu, B.; Moulton, H.M.; Abes, R.; Ivanova, G.D.; Abes, S.; Stein, D.A.; Iversen, P.L.; Arzumanov, A.A.; Gait, M.J. Cell penetrating peptide conjugates of steric block oligonucleotides. Adv. Drug Deliv. Rev., 2008, 60(4-5), 517-529.
[http://dx.doi.org/10.1016/j.addr.2007.09.002] [PMID: 18037527]
[48]
Moulton, H.M.; Moulton, J.D. Antisense morpholino oligomers and their peptide conjugates; Therapeut. Oligonucleot, 2008, pp. 43-79.
[http://dx.doi.org/10.1039/9781847558275-00043]
[49]
Meyer-Losic, F.; Nicolazzi, C.; Quinonero, J.; Ribes, F.; Michel, M.; Dubois, V.; de Coupade, C.; Boukaissi, M.; Chéné, A-S.; Tranchant, I.; Arranz, V.; Zoubaa, I.; Fruchart, J.S.; Ravel, D.; Kearsey, J. DTS-108, a novel peptidic prodrug of SN38: in vivo efficacy and toxicokinetic studies. Clin. Cancer Res., 2008, 14(7), 2145-2153.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-4580] [PMID: 18381956]
[50]
(a) Zahid, M.; Robbins, P.D. Cell-type specific penetrating peptides: therapeutic promises and challenges. Molecules, 2015, 20(7), 13055-13070.
[http://dx.doi.org/10.3390/molecules200713055] [PMID: 26205050]
(b) Orange, J.S.; May, M.J. Cell penetrating peptide inhibitors of nuclear factor-kappa B. Cell. Mol. Life Sci., 2008, 65(22), 3564-3591.
[http://dx.doi.org/10.1007/s00018-008-8222-z] [PMID: 18668204]
[51]
Löfgren, K.; Wahlström, A.; Lundberg, P.; Langel, U.; Gräslund, A.; Bedecs, K. Antiprion properties of prion protein-derived cell-penetrating peptides. FASEB J., 2008, 22(7), 2177-2184.
[http://dx.doi.org/10.1096/fj.07-099549] [PMID: 18296502]
[52]
Ezzat, K.; Andaloussi, S.E.; Zaghloul, E.M.; Lehto, T.; Lindberg, S.; Moreno, P.M.; Viola, J.R.; Magdy, T.; Abdo, R.; Guterstam, P.; Sillard, R.; Hammond, S.M.; Wood, M.J.; Arzumanov, A.A.; Gait, M.J.; Smith, C.I.; Hällbrink, M.; Langel, Ü. PepFect 14, a novel cell penetrating peptide for oligonucleotide delivery in solution and as solid formulation. Nucleic Acids Res., 2011, 39(12), 5284-5298.
[http://dx.doi.org/10.1093/nar/gkr072] [PMID: 21345932]
[53]
(a) Zhao, F.; Zhao, Y.; Liu, Y.; Chang, X.; Chen, C.; Zhao, Y. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small, 2011, 7(10), 1322-1337.
(b) Hällbrink, M.; Kilk, K.; Elmquist, A.; Lundberg, P.; Lind-gren, M.; Jiang, Y.; Pooga, M.; Soomets, U.; Langel, Ü. Prediction of cell-penetrating peptides. Int. J. Pept. Res. Ther., 2005, 11(4), 249-259.
[http://dx.doi.org/10.1007/s10989-005-9393-1]
[54]
Fonseca, S.B.; Pereira, M.P.; Kelley, S.O. Recent advances in the use of cell-penetrating peptides for medical and biological applications. Adv. Drug Deliv. Rev., 2009, 61(11), 953-964.
[http://dx.doi.org/10.1016/j.addr.2009.06.001] [PMID: 19538995]
[55]
(a) Herce, H.D.; Garcia, A.E. Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes. Proc. Natl. Acad. Sci. USA, 2007, 104(52), 20805-20810.
[http://dx.doi.org/10.1073/pnas.0706574105] [PMID: 18093956]
(b) Herce, H.D.; Garcia, A.E.; Litt, J.; Kane, R.S.; Martin, P.; Enrique, N.; Rebolledo, A.; Milesi, V. Arginine-rich peptides destabilize the plasma membrane, consistent with a pore formation translocation mechanism of cell-penetrating peptides. Biophys. J., 2009, 97(7), 1917-1925.
[http://dx.doi.org/10.1016/j.bpj.2009.05.066] [PMID: 19804722]
[56]
Herce, H.D.; Garcia, A.E.; Cardoso, M.C. Fundamental molecular mechanism for the cellular uptake of guanidinium-rich molecules. J. Am. Chem. Soc., 2014, 136(50), 17459-17467.
[http://dx.doi.org/10.1021/ja507790z] [PMID: 25405895]
[57]
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]
[58]
Richard, J.P.; Melikov, K.; Vives, E.; Ramos, C.; Verbeure, B.; Gait, M.J.; Chernomordik, L.V.; Lebleu, B. Cell penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem., 2003, 278(1), 585-590.
[http://dx.doi.org/10.1074/jbc.M209548200] [PMID: 12411431]
[59]
Futaki, S.; Nakase, I.; Tadokoro, A.; Takeuchi, T.; Jones, A.T. Arginine-rich peptides and their internalization mechanisms. Biochem. Soc. Trans., 2007, 35(Pt 4), 784-787.
[60]
El-Andaloussi, S.; Järver, P.; Johansson, H.J.; Langel, U. Cargo-dependent cytotoxicity and delivery efficacy of cell-penetrating peptides: a comparative study. Biochem. J., 2007, 407(2), 285-292.
[http://dx.doi.org/10.1042/BJ20070507] [PMID: 17627607]
[61]
Alves, I.D.; Goasdoué, N.; Correia, I.; Aubry, S.; Galanth, C.; Sagan, S.; Lavielle, S.; Chassaing, G. Membrane interaction and perturbation mechanisms induced by two cationic cell penetrating peptides with distinct charge distribution. Biochim. Biophys. Acta, 2008, 1780(7-8), 948-959.
[http://dx.doi.org/10.1016/j.bbagen.2008.04.004] [PMID: 18498774]
[62]
Mäler, L. Solution NMR studies of cell-penetrating peptides in model membrane systems. Adv. Drug Deliv. Rev., 2013, 65(8), 1002-1011.
[http://dx.doi.org/10.1016/j.addr.2012.10.011] [PMID: 23137785]
[63]
Prochiantz, A. Homeoprotein intercellular transfer, the hidden face of cell-penetrating peptides. Cell-Penetrating Peptides; Springer, 2011, pp. 249-257.
[64]
(a) Pouny, Y.; Rapaport, D.; Mor, A.; Nicolas, P.; Shai, Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry, 1992, 31(49), 12416-12423.
[http://dx.doi.org/10.1021/bi00164a017] [PMID: 1463728]
(b) Thennarasu, S.; Tan, A.; Penumatchu, R.; Shelburne, C.E.; Heyl, D.L.; Ramamoorthy, A. Antimicrobial and membrane disrupting activities of a peptide derived from the human cathelicidin antimicrobial peptide LL37. Biophys. J., 2010, 98(2), 248-257.
[http://dx.doi.org/10.1016/j.bpj.2009.09.060] [PMID: 20338846]
[65]
(a) Mor, A.; Nguyen, V.H.; Delfour, A.; Migliore-Samour, D.; Nicolas, P. Isolation, amino acid sequence, and synthesis of dermaseptin, a novel antimicrobial peptide of amphibian skin. Biochemistry, 1991, 30(36), 8824-8830.
[http://dx.doi.org/10.1021/bi00100a014] [PMID: 1909573]
(b) Marcos, J.F.; Gandía, M. Antimicrobial peptides: to membranes and beyond. Expert Opin. Drug Discov., 2009, 4(6), 659-671.
[http://dx.doi.org/10.1517/17460440902992888] [PMID: 23489158]
[66]
Shai, Y. Mode of action of membrane active antimicrobial peptides. Biopolymers, 2002, 66(4), 236-248.
[http://dx.doi.org/10.1002/bip.10260] [PMID: 12491537]
[67]
Cardoso, A.M.; Trabulo, S.; Cardoso, A.L.; Lorents, A.; Morais, C.M.; Gomes, P.; Nunes, C.; Lúcio, M.; Reis, S.; Padari, K.; Pooga, M.; Pedroso de Lima, M.C.; Jurado, A.S. S4(13)-PV cell-penetrating peptide induces physical and morphological changes in membrane-mimetic lipid systems and cell membranes: implications for cell internalization. Biochim. Biophys. Acta, 2012, 1818(3), 877-888.
[http://dx.doi.org/10.1016/j.bbamem.2011.12.022] [PMID: 22230348]
[68]
Kalafatovic, D.; Giralt, E. Cell-penetrating peptides: design strategies beyond primary structure and amphipathicity. Molecules, 2017, 22(11), 1929.
[http://dx.doi.org/10.3390/molecules22111929] [PMID: 29117144]
[69]
Zhang, T-T.; Li, W.; Meng, G.; Wang, P.; Liao, W. Strategies for transporting nanoparticles across the blood-brain barrier. Biomater. Sci., 2016, 4(2), 219-229.
[http://dx.doi.org/10.1039/C5BM00383K] [PMID: 26646694]
[70]
Derossi, D.; Joliot, A.H.; Chassaing, G.; Prochiantz, A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem., 1994, 269(14), 10444-10450.
[PMID: 8144628]
[71]
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]
[72]
Elmquist, A.; Lindgren, M.; Bartfai, T.; Langel U, VE-cadherin derived cell-penetrating peptide, pVEC, with carrier functions. Exp. Cell Res., 2001, 269(2), 237-244.
[http://dx.doi.org/10.1006/excr.2001.5316] [PMID: 11570816]
[73]
Pooga, M.; Hällbrink, M.; Zorko, M.; Langel, U. Cell penetration by transportan. FASEB J., 1998, 12(1), 67-77.
[http://dx.doi.org/10.1096/fsb2fasebj.12.1.67] [PMID: 9438412]
[74]
Morris, M.C.; Vidal, P.; Chaloin, L.; Heitz, F.; Divita, G. A new peptide vector for efficient delivery of oligonucleotides into mammalian cells. Nucleic Acids Res., 1997, 25(14), 2730-2736.
[http://dx.doi.org/10.1093/nar/25.14.2730] [PMID: 9207018]
[75]
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]
[76]
Oehlke, J.; Scheller, A.; Wiesner, B.; Krause, E.; Beyermann, M.; Klauschenz, E.; Melzig, M.; Bienert, M. Cellular uptake of an α-helical amphipathic model peptide with the potential to deliver polar compounds into the cell interior non-endocytically. Biochim. Biophys. Acta, 1998, 1414(1-2), 127-139.
[http://dx.doi.org/10.1016/S0005-2736(98)00161-8] [PMID: 9804921]
[77]
Delaroche, D.; Aussedat, B.; Aubry, S.; Chassaing, G.; Burlina, F.; Clodic, G.; Bolbach, G.; Lavielle, S.; Sagan, S. Tracking a new cell penetrating (W/R) nonapeptide, through an enzyme-stable mass spectrometry reporter tag. Anal. Chem., 2007, 79(5), 1932-1938.
[http://dx.doi.org/10.1021/ac061108l] [PMID: 17260976]


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VOLUME: 17
ISSUE: 5
Year: 2020
Published on: 31 July, 2020
Page: [375 - 386]
Pages: 12
DOI: 10.2174/1567201817666200415111755
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