Low molecular weight protamine (LMWP): A nontoxic protamine substitute and an effective cell-penetrating peptide

Journal of Controlled Release

Volumn 193, Issue , 2014, Pages 63-73

  He, Huining ^a,b   Ye, Junxiao ^b   Liu, Ergang ^b   Liang, Qiuling ^a   Liu, Quan ^b   Yang, Victor C ^a,b,c,d  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b TIANJIN UNIVERSITY   (China)

^c UNIVERSITY OF MICHIGAN   (United States)

^d Seoul National University   (South Korea)

Author keywords

Cell penetrating peptide (CPP); Heparin antagonist; Low molecular weight protamine; Protamine; Protein transduction domain (PTD)

Indexed keywords

AMINO ACIDS; BACTERIOPHAGES; CYTOLOGY; GENE TRANSFER; GENES; INSULIN; MAMMALS; MOLECULAR WEIGHT; POLYSACCHARIDES;

CELL-PENETRATING PEPTIDE; HEPARIN ANTAGONIST; LOW MOLECULAR WEIGHT PROTAMINES; PROTAMINE; PROTEIN TRANSDUCTION DOMAINS;

PEPTIDES;

ARGININE; CARBOXYLESTERASE; CELL PENETRATING PEPTIDE; CELL PROTEIN; DRUG CARRIER; GELONIN; HEPARIN; HEPARIN ANTAGONIST; IMMUNOGLOBULIN G ANTIBODY; INSULIN; ISOPHANE INSULIN; LOW MOLECULAR WEIGHT HEPARIN; LOW MOLECULAR WEIGHT PROTAMINE; MAGNETIC NANOPARTICLE; PEPTIDE; POLYCLONAL ANTIBODY; PROTAMINE; PROTEIN ANTIBODY; PROTEIN TRANSDUCTION DOMAIN PEPTIDE; SMALL INTERFERING RNA; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; THERMOLYSIN; THROMBOCYTE FACTOR 4; UNCLASSIFIED DRUG; ANTIBODY; PEPTIDE FRAGMENT;

AFFINITY CHROMATOGRAPHY; ANTICOAGULATION; ANTIGENICITY; ANTINEOPLASTIC ACTIVITY; BLOOD TOXICITY; BRAIN TUMOR; CANCER INHIBITION; CELL ENCAPSULATION; CELLULAR DISTRIBUTION; CLINICAL PRACTICE; COMPLEMENT ACTIVATION; CROSS LINKING; CROSS REACTION; CYTOTOXICITY; DIABETES CONTROL; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG SCREENING; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE; GENE DELIVERY SYSTEM; GENETIC RECOMBINATION; HEMODYNAMICS; IMMUNOGENICITY; INTERNALIZATION; INTESTINE ABSORPTION; LEUKOCYTE COUNT; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; REVIEW; STATIC ELECTRICITY; THROMBOCYTE COUNT; ANIMAL; BLOOD; CHEMISTRY; DRUG EFFECTS; DRUG FORMULATION; IMMUNOLOGY; MOUSE; PROTEIN CONFORMATION;

ANIMALS; ANTIBODIES; CELL-PENETRATING PEPTIDES; CROSS REACTIONS; DRUG COMPOUNDING; HEPARIN ANTAGONISTS; MICE; MOLECULAR WEIGHT; PEPTIDE FRAGMENTS; PROTAMINES; PROTEIN CONFORMATION;

EID: 84908270596     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.05.056     Document Type: Review

References (136)

1. T. Ando, M. Yamsaki, and K. Suzuki Protamine A. Kleinzeller, Molecular Biology, Biochemistry, and Biophysics 1973 Springer-Verlag New York 1 109
2. R. Balhorn The protamine family of sperm nuclear proteins Genome Biol. 8 9 2007 227
3. I.J. Welsby, M.F. Newman, B. Phillips-Bute, R.H. Messier, E.D. Kakkis, and M. Stafford-Smith Hemodynamic changes after protamine administration - association with mortality after coronary artery bypass surgery Anesthesiology 102 2 2005 308 314
4. L.B. Jaques Protamine - antagonist to heparin Can. Med. Assoc. J. 108 10 1973 1291 1297
5. Protamine sulfate American Hospital Formulary Service (AHFS) Drug Information 1989 American Society of Hospital Pharmacists Inc. Bethesda 711 713
6. Insulins American Hospital Formulary Service (AHFS) Drug Information 1989 American Society of Hospital Pharmacists Inc. Bethesda MD 1725 1736
7. M.M. Levinson, and W. Ohm The pathophysiology and treatment of severe protamine reactions in cardiovascular surgery The Heart Surgery Forum 1995
8. R. Porsche, and Z.R. Brenner Allergy to protamine sulfate Heart Lung 28 6 1999 418 428
9. J.M. Weiler, M.A. Gellhaus, J.G. Carter, R.L. Meng, P.M. Benson, R.A. Hottel, K.B. Schillig, A.B. Vegh, and W.R. Clarke A prospective-study of the risk of an immediate adverse reaction to protamine sulfate during cardiopulmonary bypass-surgery J. Allergy Clin. Immunol. 85 4 1990 713 719
10. S. Metz, and J.C. Horrow Protamine and newer heparin antagonists R.K. Stoelting, Pharmacology & Physiology in Anesthetic Practice 1994 1 15
11. M.E. Weiss, and N.F. Adkinson Allergy to protamine Clin. Rev. Allergy Immunol. 9 3-4 1991 339 355
12. J.C. Horrow Protamine allergy J. Cardiothorac. Anesth. 2 1988 225 242
13. B. Lindblad Protamine sulfate: a review of its effects: hypersensitivity and toxicity Eur. J. Vasc. Surg. 3 1989 195 201
14. J.G. Cormack, and J.H. Levy Adverse reactions to protamine Coron. Artery Dis. 4 5 1993 420 425
15. J.A. Carr, and N. Silverman The heparin-protamine interaction - a review J. Cardiovasc. Surg. (Torino) 40 5 1999 659 666
16. G. Blaise Heparin and protamine interaction Can. J. Anaesth. 45 12 1998 1144 1147
17. N.M. Katz, Y.D. Kim, R. Siegelman, S.A. Ved, S.W. Ahmed, and R.B. Wallace Hemodynamics of protamine administration - comparison of right atrial, left atrial, and aortic injections J. Thorac. Cardiovasc. Surg. 94 6 1987 881 886
18. E. Ovrum, H. Lindberg, E.A. Holen, and M. Abdelnoor Hemodynamic-effects of intraaortic versus intravenous protamine administration after cardiopulmonary bypass in man Scand. J. Thorac. Cardiovasc. Surg. 26 2 1992 113 118
19. J.K. Kirklin, D.E. Chenoweth, D.C. Naftel, E.H. Blackstone, J.W. Kirklin, D.D. Bitran, J.G. Curd, J.G. Reves, and P.N. Samuelson Effects of protamine administration after cardiopulmonary bypass on complement, blood-elements, and the hemodynamic state Ann. Thorac. Surg. 41 2 1986 193 199
20. E. Lowenstein, W.E. Johnston, D.G. Lappas, M.N. Dambra, R.C. Schneider, W.M. Daggett, C.W. Akins, and D.M. Philbin Catastrophic pulmonary vasoconstriction associated with protamine reversal of heparin Anesthesiology 59 5 1983 470 473
21. J.O. Justviera, C.R. Fischer, O. Gago, and J.D. Morris Acute reaction to protamine - its importance to surgeons Am. Surg. 50 1 1984 52 60
22. F.E. Ralley The use of nitric oxide for managing catastrophic pulmonary vasoconstriction arising from protamine administration Anesth. Analg. 88 3 1999 505 507
23. M. Hurby, B. Skrovina, and I. Vanek Anaphylactic reaction to protamine in cardiovascular surgery Rozhl. Chir. 74 1995 282 283
24. G.N. Olinger, R.M. Becker, and L.I. Bonchek Noncardiogenic pulmonary-edema and peripheral vascular collapse following cardiopulmonary bypass - rare protamine reaction Ann. Thorac. Surg. 29 1 1980 20 25
25. C.A. Cobb, and D.L. Fung Shock due to protamine hypersensitivity Surg. Neurol. 17 4 1982 245 246
26. M.D. Sharath, W.J. Metzger, H.B. Richerson, R.K. Scupham, R.L. Meng, B.H. Ginsberg, and J.M. Weiler Protamine-induced fatal anaphylaxis - prevalence of antiprotamine immunoglobulin-E antibody J. Thorac. Cardiovasc. Surg. 90 1 1985 86 90
27. P.P. Neidhart, B. Meier, B.S. Polla, J.A. Schifferli, and D.R. Morel Fatal anaphylactoid response to protamine after percutaneous transluminal coronary angioplasty Eur. Heart J. 13 6 1992 856 858
28. C. Kindler, A. Bircher, and P. Stulz Protamine-induced fulminating non-cardiogenic pulmonary edema following cardiopulmonary bypass Eur. J. Cardiothorac. Surg. 10 6 1996 463 466
29. R.B. Hird, T.W. Wakefield, R. Mukherjee, B.U. Jones, F.A. Crawford, P.C. Andrews, J.C. Stanley, and F.G. Spinale Direct effects of protamine sulfate on myocyte contractile processes - cellular and molecular mechanisms Circulation 92 9 1995 433 446
30. T.W. Wakefield, S.K. Wrobleski, B.J. Nichol, A.M. Kadell, and J.C. Stanley Heparin-mediated reductions of the toxic effects of protamine sulfate on rabbit myocardium J. Vasc. Surg. 16 1 1992 47 53
31. W.K. Park, J.J. Pancrazio, and C. Lynch Mechanical and electrophysiological effects of protamine on isolated ventricular myocardium - evidence for calcium overload Cardiovasc. Res. 28 4 1994 505 514
32. J.R. Adkins, and J.D. Hardy Sodium heparin neutralization and anticoagulant effects of protamine sulfate Arch. Surg. 94 2 1967 175 177
33. R.J. Cobelgeard, and H.I. Hassouna Interaction of protamine sulfate with thrombin Am. J. Hematol. 14 3 1983 227 233
34. A.H. Kuitunen, M.T. Salmenpera, J. Heinonen, V.P. Rasi, and G. Myllyla Heparin rebound: a comparative study of protamine chloride and protamine sulfate in patients undergoing coronary artery bypass surgery J. Cardiothorac. Vasc. Anesth. 5 1991 221 226
35. N. Ellison, C.P. Beatty, D.R. Blake, H.A. Wurzel, and H. Macvaugh Heparin rebound - studies in volunteers and patients Transfusion 13 5 1973 364-364
36. R. Kim Anaphylaxis to protamine masquerading as an insulin allergy Del. Med. J. 65 1993 17 23
37. M.E. Bollinger, R.G. Hamilton, and R.A. Wood Protamine allergy as a complication of insulin hypersensitivity: a case report J. Allergy Clin. Immunol. 104 2 1999 462 465
38. C. Blanco, R. Castillo, J. Quiralte, J. Delgado, I. Garcia, P. dePablos, and T. Carrillo Anaphylaxis to subcutaneous neutral protamine Hagedorn insulin with simultaneous sensitization to protamine and insulin Allergy 51 6 1996 421 424
39. Y. Byun, V.K. Singh, and V.C. Yang Low molecular weight protamine: a potential nontoxic heparin antagonist Thromb. Res. 94 1 1999 53 61
40. Y. Byun, L.C. Chang, L.M. Lee, I.S. Han, V.K. Singh, and V.C. Yang Low molecular weight protamine: a potent but nontoxic antagonist to heparin/low molecular weight protamine ASAIO J. 46 4 2000 435 439
41. L.C. Chang, H.F. Lee, Z. Yang, and V.C. Yang Low molecular weight protamine (LMWP) as nontoxic heparin/low molecular weight heparin antidote (I): preparation and characterization AAPS PharmSci. 3 3 2001 E17
42. L.C. Chang, J.F. Liang, H.F. Lee, L.M. Lee, and V.C. Yang Low molecular weight protamine (LMWP) as nontoxic heparin/low molecular weight heparin antidote (II): in vitro evaluation of efficacy and toxicity AAPS PharmSci. 3 3 2001 E18
43. H. He, A.E. David, J. Zhang, Y.S. Park, J. Wang, Y. Huang, J. Wang, and V.C. Yang Low molecular weight protamine/insulin formulation with potential to attenuate protamine-masqueraded insulin allergy Macromol. Res. 19 12 2011 1224 1226
44. Y.J. Park, J.F. Liang, K.S. Ko, S.W. Kim, and V.C. Yang Low molecular weight protamine as an efficient and nontoxic gene carrier: in vitro study J. Gene Med. 5 8 2003 700 711
45. Y.J. Park, L.C. Chang, J.F. Liang, C. Moon, C.P. Chung, and V.C. Yang Nontoxic membrane translocation peptide from protamine, low molecular weight protamine (LMWP), for enhanced intracellular protein delivery: in vitro and in vivo study FASEB J. 19 11 2005 1555 1557
46. J.F. Liang, L. Zhen, L.C. Chang, and V.C. Yang A less toxic heparin antagonist - low molecular weight protamine Biochemistry (Mosc) 68 1 2003 116 120
47. Y.S. Choi, J.Y. Lee, J.S. Suh, Y.M. Kwon, S.J. Lee, J.K. Chung, D.S. Lee, V.C. Yang, C.P. Chung, and Y.J. Park The systemic delivery of siRNAs by a cell penetrating peptide, low molecular weight protamine Biomaterials 31 6 2010 1429 1443
48. Y.S. Park, A.E. David, Y. Huang, J.B. Park, H. He, Y. Byun, and V.C. Yang In vivo delivery of cell-permeable antisense hypoxia-inducible factor 1alpha oligonucleotide to adipose tissue reduces adiposity in obese mice J. Control. Release 161 1 2012 1 9
49. M.C. Shin, J. Zhang, A.E. David, W.E. Trommer, Y.M. Kwon, K.A. Min, J.H. Kim, and V.C. Yang Chemically and biologically synthesized CPP-modified gelonin for enhanced anti-tumor activity J. Control. Release 172 1 2013 169 178
50. H. He, J. Sheng, A.E. David, Y.M. Kwon, J. Zhang, Y. Huang, J. Wang, and V.C. Yang The use of low molecular weight protamine chemical chimera to enhance monomeric insulin intestinal absorption Biomaterials 34 31 2013 7733 7743
51. L.M. Lee, L.C. Chang, S. Wrobleski, T.W. Wakefield, and V.C. Yang Low molecular weight protamine as nontoxic heparin/low molecular weight heparin antidote (III): preliminary in vivo evaluation of efficacy and toxicity using a canine model AAPS PharmSci. 3 3 2001 E19
52. J.C. Horrow Protamine - a review of its toxicity Anesth. Analg. 64 3 1985 348 361
53. J.M. Weiler, P. Freiman, M.D. Sharath, W.J. Metzger, J.M. Smith, H.B. Richerson, Z.K. Ballas, P.C. Halverson, D.J. Shulan, S. Matsuo, and R.L. Wilson Serious adverse reactions to protamine sulfate - are alternatives needed? J. Allergy Clin. Immunol. 75 2 1985 297 303
54. B. Tsui, V.K. Singh, J.F. Liang, and V.C. Yang Reduced cross-reactivity towards anti-protamine antibodies of a low molecular weight protamine analogue Thromb. Res. 101 2001 417 420
55. H.N. Cooper, and Y. Paterson Production of antibodies J.E. Coligan, A.M. Kruisbbeck, D.H. Margulies, Current Protocols in Immunology 1991 Green Publishing Associates & Wiley-Interscience NY.
56. Y. Byun, L.C. Chang, L.M. Lee, I.S. Han, V.K. Singh, and V.C. Yang Low molecular weight protamine: a potent but nontoxic antagonist to heparin/low molecular weight protamine ASAIO J. 6 4 2000 435 439
57. W.H. Howell Heparin, an anticoagulant: preliminary communication Am. J. Physiol. 63 1922 434 435
58. E. Chargaff Studies on the chemistry of blood coagulation. VII. Protamines and blood clotting J. Biol. Chem. 125 1938 671 676
59. V.C. Yang, F.K. Port, J.S. Kim, C.L.C. Teng, G.O. Till, and T.W. Wakefield The use of immobilized protamine in removing heparin and preventing protamine-induced complications during extracorporeal blood-circulation Anesthesiology 75 2 1991 288 297
60. A.D. Frankel, and C.O. Pabo Cellular uptake of the tat protein from human immunodeficiency virus Cell 55 6 1988 1189 1193
61. M. Green, and P.M. Loewenstein Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein Cell 55 6 1988 1179 1188
62. S. Fawell, J. Seery, Y. Daikh, C. Moore, L.L. Chen, B. Pepinsky, and J. Barsoum Tat-mediated delivery of heterologous proteins into cells Proc. Natl. Acad. Sci. 91 2 1994 664 668
63. H. Brooks, B. Lebleu, and E. Vives Tat peptide-mediated cellular delivery: back to basics Adv. Drug Deliv. Rev. 57 4 2005 559 577
64. S. Deshayes, M. Morris, F. Heitz, and G. Divita Delivery of proteins and nucleic acids using a non-covalent peptide-based strategy Adv. Drug Deliv. Rev. 60 4-5 2008 537 547
65. G.P. Dietz, E. Kilic, and M. Bahr Inhibition of neuronal apoptosis in vitro and in vivo using TAT-mediated protein transduction Mol. Cell. Neurosci. 21 1 2002 29 37
66. Y.M. Kwon, Y.T. Li, J.F. Liang, Y.J. Park, L.C. Chang, and V.C. Yang PTD-modified ATTEMPTS system for enhanced asparaginase therapy: a proof-of-concept investigation J. Control. Release 130 3 2008 252 258
67. M. Zhao, and R. Weissleder Intracellular cargo delivery using tat peptide and derivatives Med. Res. Rev. 24 1 2004 1 12
68. E. Vives Present and future of cell-penetrating peptide mediated delivery systems: is the Trojan horse too wild to go only to Troy? J. Control. Release 109 1-3 2005 77 85
69. E. Vives, P. Brodin, and B. Lebleu A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus J. Biol. Chem. 272 25 1997 16010 16017
70. Y. Huang, Y.S. Park, C. Moon, A.E. David, H.S. Chung, and V.C. Yang Synthetic skin-permeable proteins enabling needleless immunization Angew. Chem. Int. Ed. Engl. 49 15 2010 2724 2727
71. H. He, J. Ye, Y. Wang, Q. Liu, H.S. Chung, Y.M. Kwon, M.C. Shin, K. Lee, and V.C. Yang Cell-penetrating peptides meditated encapsulation of protein therapeutics into intact red blood cells and its application J. Control. Release 176C 2014 123 132
72. Y. Huang, Y. Jiang, H. Wang, J. Wang, M.C. Shin, Y. Byun, H. He, Y. Liang, and V.C. Yang Curb challenges of the "Trojan horse" approach: smart strategies in achieving effective yet safe cell-penetrating peptide-based drug delivery Adv. Drug Deliv. Rev. 65 10 2013 1299 1315
73. S.R. Schwarze, A. Ho, A. Vocero-Akbani, and S.F. Dowdy In vivo protein transduction: delivery of a biologically active protein into the mouse Science 285 5433 1999 1569 1572
74. G.P. Dietz, and M. Bahr Peptide-enhanced cellular internalization of proteins in neuroscience Brain Res. Bull. 68 1-2 2005 103 114
75. E.M. Barnett, B. Elangovan, K.E. Bullok, and D. Piwnica-Worms Selective cell uptake of modified Tat peptide-fluorophore conjugates in rat retina in ex vivo and in vivo models Invest. Ophthalmol. Vis. Sci. 47 6 2006 2589 2595
76. N. Kamei, M. Morishita, Y. Eda, N. Ida, R. Nishio, and K. Takayama Usefulness of cell-penetrating peptides to improve intestinal insulin absorption J. Control. Release 132 1 2008 21 25
77. N. Kamei, M. Morishita, and K. Takayama Importance of intermolecular interaction on the improvement of intestinal therapeutic peptide/protein absorption using cell-penetrating peptides J. Control. Release 136 3 2009 179 186
78. L.B. Lopes, C.M. Brophy, E. Furnish, C.R. Flynn, O. Sparks, P. Komalavilas, L. Joshi, A. Panitch, and M.V. Bentley Comparative study of the skin penetration of protein transduction domains and a conjugated peptide Pharm. Res. 22 5 2005 750 757
79. M.C. Shin, J. Zhang, K.A. Min, K. Lee, Y. Byun, A.E. David, H. He, and V.C. Yang Cell-penetrating peptides: achievements and challenges in application for cancer treatment J. Biomed. Mater. Res. A 102 2 2014 575 587
80. F. Wang, Y. Wang, X. Zhang, W. Zhang, S. Guo, and F. Jin Recent progress of cell-penetrating peptides as new carriers for intracellular cargo delivery J. Control. Release 174 2014 126 136
81. F. Heitz, M.C. Morris, and G. Divita Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics Br. J. Pharmacol. 157 2 2009 195 206
82. R. Brasseur, and G. Divita Happy birthday cell penetrating peptides: already 20 years Biochim. Biophys. Acta 1798 12 2010 2177 2181
83. S. Deshayes, M.C. Morris, G. Divita, and F. Heitz Cell-penetrating peptides: tools for intracellular delivery of therapeutics Cell. Mol. Life Sci. 62 16 2005 1839 1849
84. T. Lehto, K. Kurrikoff, and U. Langel Cell-penetrating peptides for the delivery of nucleic acids Expert. Opin. Drug Deliv. 9 7 2012 823 836
85. P. Jarver, K. Langel, S. El-Andaloussi, and U. Langel Applications of cell-penetrating peptides in regulation of gene expression Biochem. Soc. Trans. 35 Pt4 2007 770 774
86. Y.J. Chen, B.R. Liu, Y.H. Dai, C.Y. Lee, M.H. Chan, H.H. Chen, H.J. Chiang, and H.J. Lee A gene delivery system for insect cells mediated by arginine-rich cell-penetrating peptides Gene 493 2 2012 201 210
87. A. Chugh, and F. Eudes Cellular uptake of cell-penetrating peptides pVEC and transportan in plants J. Pept. Sci. 14 4 2008 477 481
88. G.P. Dietz, and M. Bahr Synthesis of cell-penetrating peptides and their application in neurobiology Methods Mol. Biol. 399 2007 181 198
89. S.T. Henriques, J. Costa, and M.A. Castanho Translocation of beta-galactosidase mediated by the cell-penetrating peptide pep-1 into lipid vesicles and human HeLa cells is driven by membrane electrostatic potential Biochemistry 44 30 2005 10189 10198
90. T. Jiang, E.S. Olson, Q.T. Nguyen, M. Roy, P.A. Jennings, and R.Y. Tsien Tumor imaging by means of proteolytic activation of cell-penetrating peptides Proc. Natl. Acad. Sci. 101 51 2004 17867 17872
91. C. Dohmen, and E. Wagner Multifunctional CPP polymer system for tumor-targeted pDNA and siRNA delivery Methods Mol. Biol. 683 2011 453 463
92. K. Splith, and I. Neundorf Antimicrobial peptides with cell-penetrating peptide properties and vice versa Eur. Biophys. J. 40 4 2011 387 397
93. J.W. Hu, B.R. Liu, C.Y. Wu, S.W. Lu, and H.J. Lee Protein transport in human cells mediated by covalently and noncovalently conjugated arginine-rich intracellular delivery peptides Peptides 30 9 2009 1669 1678
94. J.S. Wadia, and S.F. Dowdy Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer Adv. Drug Deliv. Rev. 57 4 2005 579 596
95. S.B. Fonseca, M.P. Pereira, and S.O. Kelley Recent advances in the use of cell-penetrating peptides for medical and biological applications Adv. Drug Deliv. Rev. 61 11 2009 953 964
96. G.P. Dietz, and M. Bahr Delivery of bioactive molecules into the cell: the Trojan horse approach Mol. Cell. Neurosci. 27 2 2004 85 131
97. M. Chang, J.C. Chou, C.P. Chen, B.R. Liu, and H.J. Lee Noncovalent protein transduction in plant cells by macropinocytosis New Phytol. 174 1 2007 46 56
98. Y.W. Hou, M.H. Chan, H.R. Hsu, B.R. Liu, C.P. Chen, H.H. Chen, and H.J. Lee Transdermal delivery of proteins mediated by non-covalently associated arginine-rich intracellular delivery peptides Exp. Dermatol. 16 12 2007 999 1006
99. S. Futaki, T. Suzuki, W. Ohashi, T. Yagami, S. Tanaka, K. Ueda, and Y. Sugiura Arginine-rich peptides - an abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery J. Biol. Chem. 276 8 2001 5836 5840
100. Y. Huang, Y.S. Park, J. Wang, C. Moon, Y.M. Kwon, H.S. Chung, Y.J. Park, and V.C. Yang ATTEMPTS system: a macromolecular prodrug strategy for cancer drug delivery Curr. Pharm. Des. 16 21 2010 2369 2376
101. M.E. Martin, and K.G. Rice Peptide-guided gene delivery AAPS J. 9 1 2007 E18 E29
102. S.R. Schwarze, and S.F. Dowdy In vivo protein transduction: intracellular delivery of biologically active proteins, compounds and DNA Trends Pharmacol. Sci. 21 2 2000 45 48
103. M.A. Zanta, P. Belguise-Valladier, and J.P. Behr Gene delivery: a single nuclear localization signal peptide is sufficient to carry DNA to the cell nucleus Proc. Natl. Acad. Sci. 96 1 1999 91 96
104. T.S. Zatsepin, J.J. Turner, T.S. Oretskaya, and M.J. Gait Conjugates of oligonucleotides and analogues with cell penetrating peptides as gene silencing agents Curr. Pharm. Des. 11 28 2005 3639 3654
105. C. Rudolph, U. Schillinger, A. Ortiz, K. Tabatt, C. Plank, R.H. Muller, and J. Rosenecker Application of novel solid lipid nanoparticle (SLN)-gene vector formulations based on a dimeric HIV-1 TAT-peptide in vitro and in vivo Pharm. Res. 21 9 2004 1662 1669
106. V.P. Torchilin Cell penetrating peptide-modified pharmaceutical nanocarriers for intracellular drug and gene delivery Biopolymers 90 5 2008 604 610
107. V.P. Torchilin Tatp-mediated intracellular delivery of pharmaceutical nanocarriers Biochem. Soc. Trans. 35 Pt4 2007 816 820
108. J.M. de la Fuente, and C.C. Berry Tat peptide as an efficient molecule to translocate gold nanoparticles into the cell nucleus Bioconjug. Chem. 16 5 2005 1176 1180
109. C. Walther, K. Meyer, R. Rennert, and I. Neundorf Quantum dot-carrier peptide conjugates suitable for imaging and delivery applications Bioconjug. Chem. 19 12 2008 2346 2356
110. J. Zhang, M.C. Shin, A.E. David, J. Zhou, K. Lee, H. He, and V.C. Yang Long-circulating heparin-functionalized magnetic nanoparticles for potential application as a protein drug delivery platform Mol. Pharm. 10 10 2013 3892 3902
111. J. Zhou, J. Zhang, A.E. David, and V.C. Yang Magnetic tumor targeting of beta-glucosidase immobilized iron oxide nanoparticles Nanotechnology 24 37 2013 (3751029, 12 pp.)
112. J. Zhang, M.C. Shin, and V.C. Yang Magnetic targeting of novel heparinized iron oxide nanoparticles evaluated in a 9l-glioma mouse model Pharm. Res. 31 3 2013 579 592
113. F. Stirpe, S. Olsnes, and A. Pihl Gelonin, a new inhibitor of protein synthesis, nontoxic to intact cells. Isolation, characterization, and preparation of cytotoxic complexes with concanavalin A J. Biol. Chem. 255 14 1980 6947 6953
114. S.F. Atkinson, T. Bettinger, L.W. Seymour, J.P. Behr, and C.M. Ward Conjugation of folate via gelonin carbohydrate residues retains ribosomal-inactivating properties of the toxin and permits targeting to folate receptor positive cells J. Biol. Chem. 276 30 2001 27930 27935
115. T.Y. Lee, Y.S. Park, G.A. Garcia, R.K. Sunahara, J.H. Woods, and V.C. Yang Cell permeable cocaine esterases constructed by chemical conjugation and genetic recombination Mol. Pharm. 9 5 2012 1361 1373
116. L.M. Matovcik, I.G. Junga, and S.L. Schrier Drug-induced endocytosis of neonatal erythrocytes Blood 65 5 1985 1056 1063
117. C. Lizano, S. Sanz, J. Luque, and M. Pinilla In vitro study of alcohol dehydrogenase and acetaldehyde dehydrogenase encapsulated into human erythrocytes by an electroporation procedure Biochim. Biophys. Acta 1425 2 1998 328 336
118. M. Hamidi, N. Zarei, A. Zarrin, and S. Mohammadi-Samani Preparation and validation of carrier human erythrocytes loaded by bovine serum albumin as a model antigen/protein Drug Deliv. 14 5 2007 295 300
119. G.M. Ihler, R.H. Glew, and F.W. Schnure Enzyme loading of erythrocytes Proc. Natl. Acad. Sci. 70 9 1973 2663 2666
120. S.J. Updike, R.T. Wakamiya, and E.N. Lightfoot Jr. Asparaginase entrapped in red blood cells: action and survival Science 193 4254 1976 681 683
121. M.I. Garin, R.M. Lopez, S. Sanz, M. Pinilla, and J. Luque Erythrocytes as carriers for recombinant human erythropoietin Pharm. Res. 13 6 1996 869 874
122. Y.M. Kwon, H.S. Chung, C. Moon, J. Yockman, Y.J. Park, S.D. Gitlin, A.E. David, and V.C. Yang l-Asparaginase encapsulated intact erythrocytes for treatment of acute lymphoblastic leukemia (ALL) J. Control. Release 139 3 2009 182 189
123. H. He, A. David, B. Chertok, A. Cole, K. Lee, J. Zhang, J. Wang, Y. Huang, and V.C. Yang Magnetic nanoparticles for tumor imaging and therapy: a so-called theranostic system Pharm. Res. 30 10 2013 2445 2458
124. F. Yu, L. Zhang, Y. Huang, K. Sun, A.E. David, and V.C. Yang The magnetophoretic mobility and superparamagnetism of core-shell iron oxide nanoparticles with dual targeting and imaging functionality Biomaterials 31 22 2010 5842 5848
125. E.L. Snyder, and S.F. Dowdy Protein/peptide transduction domains: potential to deliver large DNA molecules into cells Curr. Opin. Mol. Ther. 3 2 2001 147 152
126. M.J. Gait Peptide-mediated cellular delivery of antisense oligonucleotides and their analogues Cell. Mol. Life Sci. 60 5 2003 844 853
127. L.N. Johnson, S.M. Cashman, and R. Kumar-Singh Cell-penetrating peptide for enhanced delivery of nucleic acids and drugs to ocular tissues including retina and cornea Mol. Ther. 16 1 2008 107 114
128. B.R. Meade, and S.F. Dowdy Exogenous siRNA delivery using peptide transduction domains/cell penetrating peptides Adv. Drug Deliv. Rev. 59 2-3 2007 134 140
129. M. Tijsterman, and R.H.A. Plasterk Dicers at RISC: the mechanism of RNAi Cell 117 1 2004 1 3
130. Y.S. Park, Y. Huang, Y.J. Park, A.E. David, L. White, H. He, H.S. Chung, and V.C. Yang Specific down regulation of 3T3-L1 adipocyte differentiation by cell-permeable antisense HIF1alpha-oligonucleotide J. Control. Release 144 1 2012 82 90
131. J.S. Suh, J.Y. Lee, Y.S. Choi, F. Yu, V.C. Yang, S.J. Lee, C.P. Chung, and Y.J. Park Efficient labeling of mesenchymal stem cells using cell permeable magnetic nanoparticles Biochem. Biophys. Res. Commun. 379 3 2009 669 675
132. S.B. McDonald, M. Renna, E.L. Spitznagel, M. Avidan, C.W. Hogue, M.R. Moon, B. Barzilai, R. Saleem, J.M. McDonald, and G.J. Despotis Preoperative use of enoxaparin increases the risk of postoperative bleeding and re-exploration in cardiac surgery patients J. Cardiothorac. Vasc. Anesth. 19 1 2005 4 10
133. N. Do, G. Weindl, L. Grohmann, M. Salwiczek, B. Koksch, H.C. Korting, and M. Schäfer-Korting Cationic membrane-active peptides - anticancer and antifungal activity as well as penetration into human skin Exp. Dermatol. 23 5 2014 326 331
134. J.S. Suh, J.Y. Lee, Y.J. Choi, H.K. You, S.D. Hong, C.P. Chung, and Y.J. Park Intracellular delivery of cell-penetrating peptide-transcriptional factor fusion protein and its role in selective osteogenesis Int. J. Nanomed. 9 2014 1153 1166
135. J.H. Lee, I.H. Bae, J.K. Choi, and J.W. Park Evaluation of a highly skin permeable low-molecular-weight protamine conjugated epidermal growth factor for novel burn wound healing therapy J. Pharm. Sci. 102 11 2013 4109 4120
136. H. Xia, G. Gu, Q. Hu, Z. Liu, M. Jiang, T. Kang, D. Miao, Q. Song, L. Yao, Y. Tu, H. Chen, X. Gao, and J. Chen Activatable cell penetrating peptide-conjugated nanoparticles with enhanced permeability for site-specific targeting delivery of anticancer drug Bioconjug. Chem. 24 3 2013 419 430