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Combination of Cell-Penetrating Peptides with Nanoparticles for Therapeutic Application: a Review

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Combination of Cell-Penetrating Peptides with Nanoparticles for Therapeutic Application: a Review biomolecules Review Combination of Cell-Penetrating Peptides with Nanoparticles for Therapeutic Application: A Review Sara Silva 1,2,* , António J. Almeida 2 and Nuno Vale 1,3,4,5 1 Laboratory of Pharmacology, Department of Drug Sciences, Faculty of Pharmacy, University of Porto, Rua de Jorge Viterbo Ferreira 228, 4050-313 Porto, Portugal; [email protected] 2 Research Institute for Medicines (iMed.ULisboa), Faculty of Pharmacy, Universidade de Lisboa, 1964-003 Lisbon, Portugal; [email protected] 3 Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), Rua Júlio Amaral de Carvalho, 45, 4200-135 Porto, Portugal 4 Instituto de Investigação e Inovação em Saúde (i3S), University of Porto, Rua Alfredo Allen, 208, 4200-135 Porto, Portugal 5 Department of Molecular Pathology and Immunology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua de Jorge Viterbo Ferreira 228, 4050-313 Porto, Portugal * Correspondence: [email protected]; Tel.: +351-220-428-500 Received: 17 December 2018; Accepted: 3 January 2019; Published: 10 January 2019 Abstract: Cell-penetrating peptides (CPPs), also known as protein translocation domains, membrane translocating sequences or Trojan peptides, are small molecules of 6 to 30 amino acid residues capable of penetrating biological barriers and cellular membranes. Furthermore, CPP have become an alternative strategy to overcome some of the current drug limitations and combat resistant strains since CPPs are capable of delivering different therapeutic molecules against a wide range of diseases. In this review, we address the recent conjugation of CPPs with nanoparticles, which constitutes a new class of delivery vectors with high pharmaceutical potential in a variety of diseases. Keywords: cell-penetrating peptides; membrane translocation; delivery systems; therapeutic molecule; nanoparticles 1. Cell-Penetrating Peptides The limited ability of current drugs to achieve penetration of the interior of the cell has contributed to their lack of biological action, decreased therapeutic efficacy and enhanced toxicity. These limitations have potentiated the development of alternative strategies, routes, vectors of delivery and administration methods. Over the last years, different cellular translocation techniques have been developed including physical methods—electroporation and microinjection; chemical methods—calcium phosphate; and viral vectors. However, these methods have been considered highly toxic to cells, thus, decreasing the cellular viability and potentiating viral recombination in the case of viral vectors [1]. Ongoing research has discovered some protein transduction domains of peptides that are capable of translocating cell membrane efficiently without compromising their integrity [2]. These are cell-penetrating peptides (CPPs), normally with a maximum length of 30 amino acid residues, and are characterized by a high content of basic amino acid residues, resulting in an overall positive net charge. CPPs are advantageous over other translocation methods because they possess high cellular permeability rates, ability to translocate into a wide spectrum of cell types, large cargo capacity and low cell toxicity associated with no immunological response [3]. The first CPP, discovered in 1988, by Frankel et al. was HIV-Tat protein responsible for virus replication and considered a powerful transactivation factor of viral and cellular gene expression [4]. HIV-Tat of 86 amino acid residues act as a viral growth factor and is taken up by the cells [4]. Some Biomolecules 2019, 9, 22; doi:10.3390/biom9010022 www.mdpi.com/journal/biomolecules Biomolecules 2019, 9, 22 2 of 24 years later, Vives et al. recognized the domain responsible for the rapid penetration of this peptide through plasma membrane—the truncated version of the HIV-Tat basic domain (48–57) [5]. In addition, Drosophila antennapedia homeobox sequence (pAntp) was reported as capable of entering nerve cells and accumulating in the nucleus [6]. In 1994, Derossi et al. identified Penetratin, a 16-mer peptide derived from the C-terminal region of the third helix of the homeodomain of Antennapedia and capable of penetrating cells [7,8]. The discovery of these two peptides with penetrating activities prompted more studies and the discovery of new CPPs. Over the next years, more CPPs were added to the listCPPs and nowadays a database has beenStructure/Sequence built that permits one to browse existing CPPsRef. based on chemicalCPPs modifications, category, cargoStructure/Sequence or peptide length [9] (Table1). In this reviewRef. we will address CPPs mechanisms of penetration and the recent papers on the conjugation of CPPs with CPPs Structure/Sequence Ref. complex structures such as nanoparticles (NPs) [10–12], micelles [13] or liposomes [14], which results TAT [4] in enhancedCPPs stability, bioavailability and efficiencyStructure/Sequence of CPPs. Ref. TAT [4] CPPs Structure/Sequence Ref. Table 1. Molecular structure of some cell-penetratingGRKKRRQRRRP peptides (CPPs) referred to in the present review. TAT [4] CPPs Structure/SequenceGRKKRRQRRRP Ref. CPPs Structure/Sequence Ref. TAT [4] GRKKRRQRRRP TAT [4] GRKKRRQRRRP R8 [15] TATTAT [4][4 ] GRKKRRQRRRP R8 [15] GRKKRRQRRRPGRKKRRQRRRPRRRRRRRR R8 [15] RRRRRRRR R8 [15] RRRRRRRR R8R8 [15][15 ] RRRRRRRR TGN [16] R8 [15] RRRRRRRRRRRRRRRR TGN TGNYKALHPHNG [16] RRRRRRRR TGN TGNYKALHPHNG [16] TGN [16] TGN TGNYKALHPHNG [16] DerivedTGN [16] TGNYKALHPHNGTGNYKALHPHNG [17] Ku‐70 DerivedTGN [16] TGNYKALHPHNGVPMLK [17] Ku‐70 DerivedDerived TGNYKALHPHNGVPMLK [17][17 ] Ku-70Ku‐70 Derived VPMLKVPMLK [17] Ku‐70 Derived VPMLK [17] Ku‐70 DerivedRW(n) [18] VPMLK [17] Ku‐70 RW(n)RW(n) [18][18 ] VPMLK RW( n) RW(n) [18] RW(RW( n)) RW(n) [18] RW(n) RW(n)CPP [18] CPP (RRRR (RRRR RW(n) RRGGRRW(n)CPP [19][18][19 ] RRRG)RRGGR (RRRR RW(n) RRRG)CPP [19] RRGGR RRRRRRGGRRRRGRRRRRRGGRRRRG (RRRR RW(n) RRRG)CPP [19] RRGGR RRRRRRGGRRRRG (RRRRSVS‐1 [20] RRRG)CPP [19] RRGGR RRRRRRGGRRRRG (RRRRSVS‐1 [20] RRRG)CPP [19] RRGGR RRRRRRGGRRRRG (RRRRSVS‐1 [20] RRRG) [19] RRGGR RRRRRRGGRRRRG SVS‐1 [20] RRRG) RRRRRRGGRRRRG SVS‐1 1 [20] SVS‐1 1 [20] 1 1 1 1 Biomolecules 2019, 9, 22 3 of 24 Table 1. Cont. CPPs Structure/Sequence Ref. KVKVKVKVDPPTKVKVKVK‐NH2 KVKVKVKVDPPTKVKVKVK‐NH2 Biomolecules 2019, 9, 22 KVKVKVKVDPPTKVKVKVK‐NH2 3 of 24 SVS-1 [20] KVKVKVKVDPPTKVKVKVK‐NH2 L‐CPP [21] KVKVKVKVDPPTKVKVKVK‐NH2 L‐CPP [21] KVKVKVKVDPPTKVKVKVKKVKVKVKVDPPTKVKVKVK-NH2LAGRRRRRRRRRK ‐NH2 L‐CPPSVS -1 [20][21] LAGRRRRRRRRRK L‐CPP [21] LAGRRRRRRRRRK L-CPPL‐CPP [21][21 ] KVKVKVKVDPPTKVKVKVKLAGRRRRRRRRRK -NH2 RLW HN NH2 HN NH2 HN NH2 HN NH2 HN NH2 [22] L‐CPP NH NH NH NH NH [21] O O LAGRRRRRRRRRKLAGRRRRRRRRRKO O O O O H H H H H H H N N N N N N N RLW H N N N N N N OH [22] H H H H H H O RLWMRWYSPRTRAYGO O O O O L-CPP LAGRRRRRRRRRK [21] RLW NH NH NH NH [22] NH2 RLWMRWYSPRTRAYGHN NH2 HN NH2 HN NH2 HN NH2 RLWRLW LAGRRRRRRRRRK [22][22 ] RLWMRWYSPRTRAYG RLW [22] K16Apo RLWMRWYSPRTRAYGRLWMRWYSPRTRAYG [23] RLWERLW [22][22] K16Apo RLWMRWYSPRTRAYG [23] E KKKKKKKKKKKKKKKKLRVRLASHLRKLRKRLLRDARLWMRWYSPRTRAYG K16Apo RLWMRWYSPRTRAYGHN NH2 HN NH2 NH2 K16ApoE NH NH [23][23 ] O E KKKKKKKKKKKKKKKKLRVRLASHLRKLRKRLLRDAOH H O O O O O O O O O O OH O N H H H H H H H H H H K16Apo H N N N N N N N N N N N N N N N N N N N N OH K16Apo H H H H H H H H H H [23] O O O O O O O O O O E KKKKKKKKKKKKKKKKLRVRLASHLRKLRKRLLRDAKKKKKKKKKKKKKKKKLRVRLASHLRKLRKRLLRDANH [23] K16ApoE NH NH N NH NH NH NH 2 2 16 HN NH HN NH HN NH HN NH [23] 2 2 2 2 AngiopE KKKKKKKKKKKKKKKKLRVRLASHLRKLRKRLLRDA K16Apo KKKKKKKKKKKKKKKKLRVRLASHLRKLRKRLLRDA [24] ep‐2 [23] AngiopE KKKKKKKKKKKKKKKKLRVRLASHLRKLRKRLLRDA Angiopep-2 [24][24 ] epAngiop‐2 TFFYGGSRGKRNNFKTEEY Angiop KKKKKKKKKKKKKKKKLRVRLASHLRKLRKRLLRDA [24] ep-2 [24] ep‐2 TFFYGGSRGKRNNFKTEEYTFFYGGSRGKRNNFKTEEY Angiop [24] ep‐2 TFFYGGSRGKRNNFKTEEYTFFYGGSRGKRNNFKTEEY Angiop [24] ep‐2 TFFYGGSRGKRNNFKTEEY ACPPAngiopACPP [12][12 ] ACPP [12][24] ep‐2 TFFYGGSRGKRNNFKTEEY ACPP [12] EEEEEEEEPLGLAGRRRRRRRRNEEEEEEEEPLGLAGRRRRRRRRN EEEEEEEEPLGLAGRRRRRRRRNTFFYGGSRGKRNNFKTEEY ACPP [12] EEEEEEEEPLGLAGRRRRRRRRN ACPP [12] EEEEEEEEPLGLAGRRRRRRRRN KAFAKKAFAK [25] [25] KAFAKACPP KAFAKLAARLYRKALARQLGVAA [12][25] EEEEEEEEPLGLAGRRRRRRRRN KAFAKACPP KAFAKLAARLYRKALARQLGVAAKAFAKLAARLYRKALARQLGVAA [25][12] EEEEEEEEPLGLAGRRRRRRRRN KAFAKhCT ( 9– [25] hCT (9– EEEEEEEEPLGLAGRRRRRRRRN2 [26] hCT (9–32)32) [26][26 ] KAFAK32) [25] LGTYTQDFNKFHTFPQTAIGVGAP2 LGTYTQDFNKFHTFPQTAIGVGAP KAFAK LGTYTQDFNKFHTFPQTAIGVGAP [25] 2 KAFAK [25] VP22 2 [27] 2 VP22 DAATATRGRSAASRPTQRPRAPARSASRPRRPVE2 [27] DAATATRGRSAASRPTQRPRAPARSASRPRRPVE 3 KAFAKLAARLYRKALARQLGVAA Biomolecules 2019, 9, 22 4 of 24 hCT (9– [26] 32) LGTYTQDFNKFHTFPQTAIGVGAPTable 1. Cont. CPPs Structure/Sequence Ref. VP22VP22 [27][27 ] DAATATRGRSAASRPTQRPRAPARSASRPRRPVEDAATATRGRSAASRPTQRPRAPARSASRPRRPVE 1.1. Mechanism of Penetration The exact mechanism of CPPs cell penetration still remains unknown [28]. Over the years, some discrepancies between studies have generated controversial data. A variety of features and conditions are crucial to the efficiency of cellular translocation and mode of penetration, and influence the different outcomes observed, such as cargo, cell type, incubation time, sample handling (washing, fixation, delays), fluorophore, CPPs concentration, cell density, stage of cell cycle, read out (uptake distribution), etc. [29–31]. One of the first problems reported was the over-quantification of peptide uptake, and respective localization in the interior of the cell. The experimental fixation
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