Protein transduction domain of translationally controlled tumor protein: characterization and application in drug delivery

References

• Amzallag N, Passer BJ, Allanic D, et al. (2004). TSAP6 facilitates the secretion of translationally controlled tumor protein/histamine-releasing factor via a nonclassical pathway. J Biol Chem 279:46104–12. https://doi.org/10.1074/jbc.M404850200
   PubMed Web of Science ®Google Scholar
• An X, Martinez-Paniagua M, Rezvan A, et al. (2021). Single-dose intranasal vaccination elicits systemic and mucosal immunity against SARS-CoV-2. iScience 24:103037. https://doi.org/10.1016/j.isci.2021.103037
   PubMed Web of Science ®Google Scholar
• Asoh S, Ohta S. (2008). PTD-mediated delivery of anti-cell death proteins/peptides and therapeutic enzymes. Adv Drug Deliv Rev 60:499–516. https://doi.org/10.1016/j.addr.2007.09.011
   PubMed Web of Science ®Google Scholar
• Bae H, Lee K. (2013). On employing a translationally controlled tumor protein-derived protein transduction domain analog for transmucosal delivery of drugs. J Control Release 170:358–64. https://doi.org/10.1016/j.jconrel.2013.06.010
   PubMed Web of Science ®Google Scholar
• Bae H-D, Kim M, Lee J, Lee K. (2018a). Modified translationally controlled tumor protein-derived protein transduction domain enhances nasal delivery of exendin-4 as shown with insulin. Drug Deliv 25:1579–84. https://doi.org/10.1080/10717544.2018.1491653
   PubMed Web of Science ®Google Scholar
• Bae H-D, Lee J, Jin X-H, Lee K. (2016). Potential of translationally controlled tumor protein-derived protein transduction domains as antigen carriers for nasal vaccine delivery. Mol Pharm 13:3196–205. https://doi.org/10.1021/acs.molpharmaceut.6b00408
   PubMed Web of Science ®Google Scholar
• Bae H-D, Lee J, Jun K-Y, et al. (2018b). Modification of translationally controlled tumor protein-derived protein transduction domain for improved intranasal delivery of insulin. Drug Deliv 25:1025–32. https://doi.org/10.1080/10717544.2018.1464081
   PubMed Web of Science ®Google Scholar
• Bienert S, Waterhouse A, de Beer TAP, et al. (2017). The SWISS-MODEL repository-new features and functionality. Nucleic Acids Res 45:D313–D319. https://doi.org/10.1093/nar/gkw1132
   PubMed Web of Science ®Google Scholar
• Bommer U-A, Kawakami T. (2021). Role of TCTP in cell biological and disease processes. Cells 10:2290. https://doi.org/10.3390/cells10092290
   PubMed Web of Science ®Google Scholar
• Bommer U-A, Thiele B-J. (2004). The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol 36:379–85. https://doi.org/10.1016/s1357-2725(03)00213-9
   PubMed Web of Science ®Google Scholar
• Chauhan A, Tikoo A, Kapur AK, Singh M. (2007). The taming of the cell penetrating domain of the HIV Tat: myths and realities. J Control Release 117:148–62. https://doi.org/10.1016/j.jconrel.2006.10.031
   PubMed Web of Science ®Google Scholar
• Chiu Y-L, Ali A, Chu C-Y, et al. (2004). Visualizing a correlation between siRNA localization, cellular uptake, and RNAi in living cells. Chem Biol 11:1165–75. https://doi.org/10.1016/j.chembiol.2004.06.006
   PubMed Web of Science ®Google Scholar
• Choi J-M, Ahn M-H, Chae W-J, et al. (2006). Intranasal delivery of the cytoplasmic domain of CTLA-4 using a novel protein transduction domain prevents allergic inflammation. Nat Med 12:574–9. https://doi.org/10.1038/nm1385
   PubMed Web of Science ®Google Scholar
• Conner SD, Schmid SL. (2003). Regulated portals of entry into the cell. Nature 422:37–44. https://doi.org/10.1038/nature01451
   PubMed Web of Science ®Google Scholar
• Coyle JT, Puttfarcken P. (1993). Oxidative stress, glutamate, and neurodegenerative disorders. Science 262:689–95. https://doi.org/10.1126/science.7901908
   PubMed Web of Science ®Google Scholar
• Davis SS, Illum L. (2003). Absorption enhancers for nasal drug delivery. Clin Pharmacokinet 42:1107–28. https://doi.org/10.2165/00003088-200342130-00003[PMC][14531723]
   PubMed Web of Science ®Google Scholar
• Derossi D, Joliot AH, Chassaing G, Prochiantz A. (1994). The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 269:10444–50.
   PubMed Web of Science ®Google Scholar
• Dom G, Shaw-Jackson C, Matis C, et al. (2003). Cellular uptake of Antennapedia Penetratin peptides is a two-step process in which phase transfer precedes a tryptophan-dependent translocation. Nucleic Acids Res 31:556–61. https://doi.org/10.1093/nar/gkg160
   PubMed Web of Science ®Google Scholar
• Drin G, Déméné H, Temsamani J, Brasseur R. (2001). Translocation of the pAntp peptide and its amphipathic analogue AP-2AL. Biochemistry 40:1824–34. https://doi.org/10.1021/bi002019k
   PubMed Web of Science ®Google Scholar
• Duchardt F, Fotin-Mleczek M, Schwarz H, et al. (2007). A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8:848–66. https://doi.org/10.1111/j.1600-0854.2007.00572.x
   PubMed Web of Science ®Google Scholar
• Duchardt F, Ruttekolk IR, Verdurmen WPR, et al. (2009). A cell-penetrating peptide derived from human lactoferrin with conformation-dependent uptake efficiency. J Biol Chem 284:36099–108. https://doi.org/10.1074/jbc.M109.036426
   PubMed Web of Science ®Google Scholar
• Ellerby HM, Arap W, Ellerby LM, et al. (1999). Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med 5:1032–8. https://doi.org/10.1038/12469
   PubMed Web of Science ®Google Scholar
• Fawell S, Seery J, Daikh Y, et al. (1994). Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci U S A 91:664–8. https://doi.org/10.1073/pnas.91.2.664
   PubMed Web of Science ®Google Scholar
• Feng Y, Liu D, Yao H, Wang J. (2007). Solution structure and mapping of a very weak calcium-binding site of human translationally controlled tumor protein by NMR. Arch Biochem Biophys 467:48–57. https://doi.org/10.1016/j.abb.2007.08.021
   PubMed Web of Science ®Google Scholar
• Ferrari A, Pellegrini V, Arcangeli C, et al. (2003). Caveolae-mediated internalization of extracellular HIV-1 tat fusion proteins visualized in real time. Mol Ther J Am Soc Gene Ther 8:284–94. https://doi.org/10.1016/s1525-0016(03)00122-9
   PubMed Web of Science ®Google Scholar
• Fittipaldi A, Ferrari A, Zoppé M, et al. (2003). Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J Biol Chem 278:34141–9. https://doi.org/10.1074/jbc.M303045200
   PubMed Web of Science ®Google Scholar
• Foillard S, Jin Z, Garanger E, et al. (2008). Synthesis and biological characterisation of targeted pro-apoptotic peptide. Chembiochem 9:2326–32. https://doi.org/10.1002/cbic.200800327
   PubMed Web of Science ®Google Scholar
• Frankel AD, Pabo CO. (1988). Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55:1189–93. https://doi.org/10.1016/0092-8674(88)90263-2
   PubMed Web of Science ®Google Scholar
• Futaki S, Suzuki T, Ohashi W, et al. (2001). Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J Biol Chem 276:5836–40. https://doi.org/10.1074/jbc.M007540200
   PubMed Web of Science ®Google Scholar
• Gessner I, Neundorf I. (2020). Nanoparticles modified with cell-penetrating peptides: conjugation mechanisms, physicochemical properties, and application in cancer diagnosis and therapy. IJMS 21:2536. https://doi.org/10.3390/ijms21072536
   Google Scholar
• Goun EA, Pillow TH, Jones LR, et al. (2006). Molecular transporters: synthesis of oligoguanidinium transporters and their application to drug delivery and real-time imaging. Chembiochem 7:1497–515. https://doi.org/10.1002/cbic.200600171
   PubMed Web of Science ®Google Scholar
• Green M, Loewenstein PM. (1988). Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 55:1179–88. https://doi.org/10.1016/0092-8674(88)90262-0
   PubMed Web of Science ®Google Scholar
• Gros E, Deshayes S, Morris MC, et al. (2006). A non-covalent peptide-based strategy for protein and peptide nucleic acid transduction. Biochim Biophys Acta 1758:384–93. https://doi.org/10.1016/j.bbamem.2006.02.006
   PubMed Web of Science ®Google Scholar
• Gross B, Gaestel M, Böhm H, Bielka H. (1989). cDNA sequence coding for a translationally controlled human tumor protein. Nucleic Acids Res 17:8367. https://doi.org/10.1093/nar/17.20.8367
   PubMed Web of Science ®Google Scholar
• Gupta SK, Bhandari B, Shrestha A, et al. (2012). Mammalian zona pellucida glycoproteins: structure and function during fertilization. Cell Tissue Res 349:665–78. https://doi.org/10.1007/s00441-011-1319-y
   PubMed Web of Science ®Google Scholar
• Jeon H-J, Bai G-Y, Park Y, et al. (2019). Prevention of quality decline and delivery of siRNA using exogenous TCTP translocation across the zona pellucida in mouse oocytes. Sci Rep 9:18845. https://doi.org/10.1038/s41598-019-55449-4
   PubMed Web of Science ®Google Scholar
• Jeon H-J, Cui X-S, Guo J, et al. (2017). TCTP regulates spindle assembly during postovulatory aging and prevents deterioration in mouse oocyte quality. Biochim Biophys Acta Mol Cell Res 1864:1328–34. https://doi.org/10.1016/j.bbamcr.2017.05.002
   PubMed Web of Science ®Google Scholar
• Joliot A, Pernelle C, Deagostini-Bazin H, Prochiantz A. (1991). Antennapedia homeobox peptide regulates neural morphogenesis. Proc Natl Acad Sci U S A 88:1864–8. https://doi.org/10.1073/pnas.88.5.1864
   PubMed Web of Science ®Google Scholar
• Joliot A, Prochiantz A. (2004). Transduction peptides: from technology to physiology. Nat Cell Biol 6:189–96. https://doi.org/10.1038/ncb0304-189
   PubMed Web of Science ®Google Scholar
• Khafagy E-S, Morishita M, Isowa K, et al. (2009). Effect of cell-penetrating peptides on the nasal absorption of insulin. J Control Release 133:103–8. https://doi.org/10.1016/j.jconrel.2008.09.076
   PubMed Web of Science ®Google Scholar
• Khafagy E-S, Morishita M, Takayama K. (2010). The role of intermolecular interactions with penetratin and its analogue on the enhancement of absorption of nasal therapeutic peptides. Int J Pharm 388:209–12. https://doi.org/10.1016/j.ijpharm.2009.12.060
   PubMed Web of Science ®Google Scholar
• Kim DI, Song M-K, Lee K. (2019). Comparison of asthma phenotypes in OVA-induced mice challenged via inhaled and intranasal routes. BMC Pulm Med 19:241. https://doi.org/10.1186/s12890-019-1001-9
   PubMed Web of Science ®Google Scholar
• Kim HY, Kim S, Pyun HJ, et al. (2015). Cellular uptake mechanism of TCTP-PTD in human lung carcinoma cells. Mol Pharm 12:194–203. https://doi.org/10.1021/mp500547f
   PubMedGoogle Scholar
• Kim HY, Kim S, Youn H, et al. (2011a). The cell penetrating ability of the proapoptotic peptide, KLAKLAKKLAKLAK fused to the N-terminal protein transduction domain of translationally controlled tumor protein, MIIYRDLISH. Biomaterials 32:5262–8. https://doi.org/10.1016/j.biomaterials.2011.03.074
   PubMed Web of Science ®Google Scholar
• Kim M, Kim M, Kim HY, et al. (2011b). A protein transduction domain located at the NH2-terminus of human translationally controlled tumor protein for delivery of active molecules to cells. Biomaterials 32:222–30. https://doi.org/10.1016/j.biomaterials.2010.08.077
   PubMed Web of Science ®Google Scholar
• Kim M, Maeng J, Jung J, et al. (2011c). Design and evaluation of variants of the protein transduction domain originated from translationally controlled tumor protein. Eur J Pharm Sci 43:25–31. https://doi.org/10.1016/j.ejps.2011.03.007
   PubMed Web of Science ®Google Scholar
• Kim M, Maeng J, Lee K. (2013). Dimerization of TCTP and its clinical implications for allergy. Biochimie 95:659–66. https://doi.org/10.1016/j.biochi.2012.10.007
   PubMed Web of Science ®Google Scholar
• Kim M, Min HJ, Won HY, et al. (2009). Dimerization of translationally controlled tumor protein is essential for its cytokine-like activity. PloS One 4:e6464. https://doi.org/10.1371/journal.pone.0006464
   PubMed Web of Science ®Google Scholar
• Kristensen M, de Groot AM, Berthelsen J, et al. (2015). Conjugation of cell-penetrating peptides to parathyroid hormone affects its structure, potency, and transepithelial permeation. Bioconjug Chem 26:477–88. https://doi.org/10.1021/bc5005763
   PubMed Web of Science ®Google Scholar
• Kwon M-K, Nam J-O, Park R-W, et al. (2008). Antitumor effect of a transducible fusogenic peptide releasing multiple proapoptotic peptides by caspase-3. Mol Cancer Ther 7:1514–22. https://doi.org/10.1158/1535-7163.MCT-07-2009
   PubMed Web of Science ®Google Scholar
• Law B, Quinti L, Choi Y, et al. (2006). A mitochondrial targeted fusion peptide exhibits remarkable cytotoxicity. Mol Cancer Ther 5:1944–9. https://doi.org/10.1158/1535-7163.MCT-05-0509
   PubMed Web of Science ®Google Scholar
• Lee J, Kim S, Shin DH, et al. (2011). Neuroprotective effect of Cu,Zn-superoxide dismutase fused to a TCTP-derived protein transduction domain. Eur J Pharmacol 666:87–92. https://doi.org/10.1016/j.ejphar.2011.05.040
   PubMed Web of Science ®Google Scholar
• Levine S, Klaiber-Franco R, Paradiso PR. (1987). Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J Gen Virol 68: 2521–4. https://doi.org/10.1099/0022-1317-68-9-2521
   PubMed Web of Science ®Google Scholar
• Li S, Ge F. (2017). Current understanding of the TCTP Interactome. Results Probl Cell Differ 64:127–36. https://doi.org/10.1007/978-3-319-67591-6_5[PMC][29149405]
   PubMedGoogle Scholar
• Liang JF, Yang VC. (2005). Insulin-cell penetrating peptide hybrids with improved intestinal absorption efficiency. Biochem Biophys Res Commun 335:734–8. https://doi.org/10.1016/j.bbrc.2005.07.142
   PubMed Web of Science ®Google Scholar
• Lim S, Kim W, Kim Y, Choi J-M. (2012). Identification of a novel cell-penetrating peptide from human phosphatidate phosphatase LPIN3. Mol Cells 34:577–82. https://doi.org/10.1007/s10059-012-0284-y
   PubMed Web of Science ®Google Scholar
• Lönn P, Dowdy SF. (2015). Cationic PTD/CPP-mediated macromolecular delivery: charging into the cell. Expert Opin Drug Deliv 12:1627–36. https://doi.org/10.1517/17425247.2015.1046431
   PubMed Web of Science ®Google Scholar
• MacDonald SM, Rafnar T, Langdon J, Lichtenstein LM. (1995). Molecular identification of an IgE-dependent histamine-releasing factor. Science 269:688–90. https://doi.org/10.1126/science.7542803
   PubMed Web of Science ®Google Scholar
• Maeng J, Kim HY, Shin DH, Lee K. (2013). Transduction of translationally controlled tumor protein employing TCTP-derived protein transduction domain. Anal Biochem 435:47–53. https://doi.org/10.1016/j.ab.2012.11.029
   PubMed Web of Science ®Google Scholar
• McCarthy S, Somayajulu M, Sikorska M, et al. (2004). Paraquat induces oxidative stress and neuronal cell death; neuroprotection by water-soluble Coenzyme Q10. Toxicol Appl Pharmacol 201:21–31. https://doi.org/10.1016/j.taap.2004.04.019
   PubMed Web of Science ®Google Scholar
• McLellan JS, Ray WC, Peeples ME. (2013). Structure and function of respiratory syncytial virus surface glycoproteins. Curr Top Microbiol Immunol 372:83–104. https://doi.org/10.1007/978-3-642-38919-1_4[PMC][24362685]
   PubMed Web of Science ®Google Scholar
• Mondola P, Damiano S, Sasso A, Santillo M. (2016). The Cu, Zn superoxide dismutase: not only a dismutase enzyme. Front Physiol 7:594. https://doi.org/10.3389/fphys.2016.00594
   Google Scholar
• Morishita M, Kamei N, Ehara J, et al. (2007). A novel approach using functional peptides for efficient intestinal absorption of insulin. J Control Release 118:177–84. https://doi.org/10.1016/j.jconrel.2006.12.022
   PubMed Web of Science ®Google Scholar
• Muto K, Kamei N, Yoshida M, et al. (2016). Cell-penetrating peptide penetratin as a potential tool for developing effective nasal vaccination systems. J Pharm Sci 105:2014–7. https://doi.org/10.1016/j.xphs.2016.03.026
   PubMed Web of Science ®Google Scholar
• Park J, Ryu J, Kim K-A, et al. (2002). 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 83:1173–81. https://doi.org/10.1099/0022-1317-83-5-1173
   PubMed Web of Science ®Google Scholar
• Patel LN, Zaro JL, Shen W-C. (2007). Cell penetrating peptides: intracellular pathways and pharmaceutical perspectives. Pharm Res 24:1977–92. https://doi.org/10.1007/s11095-007-9303-7
   PubMed Web of Science ®Google Scholar
• Prochiantz A. (2000). Messenger proteins: homeoproteins, TAT and others. Curr Opin Cell Biol 12:400–6. https://doi.org/10.1016/s0955-0674(00)00108-3
   PubMed Web of Science ®Google Scholar
• Prochiantz A, Joliot A. (2003). Can transcription factors function as cell-cell signalling molecules? Nat Rev Mol Cell Biol 4:814–9. https://doi.org/10.1038/nrm1227
   PubMed Web of Science ®Google Scholar
• Richard JP, Melikov K, Brooks H, et al. (2005). Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J Biol Chem 280:15300–6. https://doi.org/10.1074/jbc.M401604200
   PubMed Web of Science ®Google Scholar
• Rothbard JB, Jessop TC, Lewis RS, et al. (2004). Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells. J Am Chem Soc 126:9506–7. https://doi.org/10.1021/ja0482536
   PubMed Web of Science ®Google Scholar
• Ruseska I, Zimmer A. (2020). Internalization mechanisms of cell-penetrating peptides. Beilstein J Nanotechnol 11:101–23. https://doi.org/10.3762/bjnano.11.10
   PubMed Web of Science ®Google Scholar
• Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF. (1999). In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285:1569–72. https://doi.org/10.1126/science.285.5433.1569
   PubMed Web of Science ®Google Scholar
• Skotland T, Iversen TG, Torgersen ML, Sandvig K. (2015). Cell-penetrating peptides: possibilities and challenges for drug delivery in vitro and in vivo. Molecules 20:13313–23. https://doi.org/10.3390/molecules200713313
   PubMed Web of Science ®Google Scholar
• Song Y, Wang Y, Thakur R, et al. (2004). Mucosal drug delivery: membranes, methodologies, and applications. Crit Rev Ther Drug Carrier Syst 21:195–256. https://doi.org/10.1615/critrevtherdrugcarriersyst.v21.i3.20
   PubMedGoogle Scholar
• Swanson JA. (2008). Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 9:639–49. https://doi.org/10.1038/nrm2447
   PubMed Web of Science ®Google Scholar
• van den Berg A, Dowdy SF. (2011). Protein transduction domain delivery of therapeutic macromolecules. Curr Opin Biotechnol 22:888–93. https://doi.org/10.1016/j.copbio.2011.03.008
   PubMed Web of Science ®Google Scholar
• Vargason AM, Anselmo AC, Mitragotri S. (2021). The evolution of commercial drug delivery technologies. Nat Biomed Eng 5:951–67. https://doi.org/10.1038/s41551-021-00698-w
   PubMed Web of Science ®Google Scholar
• Vivès E, Brodin P, Lebleu B. (1997). A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 272:16010–7. https://doi.org/10.1074/jbc.272.25.16010
   PubMed Web of Science ®Google Scholar
• Wadia JS, Stan RV, Dowdy SF. (2004). Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 10:310–5. https://doi.org/10.1038/nm996
   PubMed Web of Science ®Google Scholar
• Wassarman PM. (2008). Zona pellucida glycoproteins. J Biol Chem 283:24285–9. https://doi.org/10.1074/jbc.R800027200
   PubMed Web of Science ®Google Scholar
• Wender PA, Mitchell DJ, Pattabiraman K, et al. (2000). The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters. Proc Natl Acad Sci U S A 97:13003–8. https://doi.org/10.1073/pnas.97.24.13003
   PubMed Web of Science ®Google Scholar
• Yap MKK, Misuan N. (2019). Exendin-4 from Heloderma suspectum venom: from discovery to its latest application as type II diabetes combatant. Basic Clin Pharmacol Toxicol 124:513–27. https://doi.org/10.1111/bcpt.13169
   PubMed Web of Science ®Google Scholar
• Yin Y, Li B, Zhou L, et al. (2020). Protein transduction domain-mediated influenza NP subunit vaccine generates a potent immune response and protection against influenza virus in mice. Emerg Microbes Infect 9:1933–42. https://doi.org/10.1080/22221751.2020.1812436
   PubMed Web of Science ®Google Scholar
• Yu J-R, Kim S, Lee J-B, Chang J. (2008). Single intranasal immunization with recombinant adenovirus-based vaccine induces protective immunity against respiratory syncytial virus infection. J Virol 82:2350–7. https://doi.org/10.1128/JVI.02372-07
   PubMed Web of Science ®Google Scholar
• Yusuf H, Kett V. (2017). Current prospects and future challenges for nasal vaccine delivery. Hum Vaccin Immunother 13:34–45. https://doi.org/10.1080/21645515.2016.1239668
   PubMed Web of Science ®Google Scholar
• Zhang X, Zhang X, Wang F. (2012). Intracellular transduction and potential of Tat PTD and its analogs: from basic drug delivery mechanism to application. Expert Opin Drug Deliv 9:457–72. https://doi.org/10.1517/17425247.2012.663351
   PubMed Web of Science ®Google Scholar
• Ziegler A. (2008). Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans. Adv Drug Deliv Rev 60:580–97. https://doi.org/10.1016/j.addr.2007.10.005
   PubMed Web of Science ®Google Scholar