Challenges and New Strategies for Therapeutic Peptide Delivery to the CNS

References

• Lipinski CA . Drug-like properties and the causes of poor solubility and poor permeability. J. Pharmacol. Toxicol. Meth.44 (1), 235–249 (2000).
   PubMed Web of Science ®Google Scholar
• Bidwell GL Raucher D . Therapeutic peptides for cancer therapy. Part I–peptide inhibitors of signal transduction cascades. Exp. Opin. Drug Deliv.6 (10), 1033–1047 (2009).
   PubMed Web of Science ®Google Scholar
• Bidwell GL . Peptides for cancer therapy: a drug-development opportunity and a drug-delivery challenge. Ther. Deliv.3 (5), 609–621 (2012).
   PubMedGoogle Scholar
• Hearst SM Shao Q Lopez M Raucher D Vig PJ . The design and delivery of a PKA inhibitory polypeptide to treat SCA1. J. Neurochem.131 (1), 101–114 (2014).
   PubMed Web of Science ®Google Scholar
• Bicker J Alves G Fortuna A Falcao A . Blood-brain barrier models and their relevance for a successful development of cns drug delivery systems: a review. Eur. J. Pharm. Biopharm.87 (3), 409–432 (2014).
   PubMed Web of Science ®Google Scholar
• Agarwal N Lippmann ES Shusta EV . Identification and expression profiling of blood-brain barrier membrane proteins. J. Neurochem.112 (3), 625–635 (2010).
   PubMed Web of Science ®Google Scholar
• Abraham MH . The factors that influence permeation across the blood-brain barrier. Eur. J. Med. Chem.39 (3), 235–240 (2004).
   PubMed Web of Science ®Google Scholar
• Upadhyay RK . Drug delivery systems, cns protection, and the blood brain barrier. Biomed. Res. Int.2014, 869269 (2014).
   PubMed Web of Science ®Google Scholar
• Salameh TS Banks WA . Delivery of therapeutic peptides and proteins to the cns. Adv. Pharmacol.71, 277–299 (2014).
   PubMedGoogle Scholar
• Bockenhoff A Cramer S Wolte P et al. Comparison of five peptide vectors for improved brain delivery of the lysosomal enzyme arylsulfatase A. J. Neurosci.34 (9), 3122–3129 (2014).
   PubMed Web of Science ®Google Scholar
• Pardridge WM . Drug transport across the blood–brain barrier. J. Cereb. Blood. Flow. Metab.32 (11), 1959–1972 (2012).
   PubMed Web of Science ®Google Scholar
• Boado RJ Lu JZ Hui EK Sumbria RK Pardridge WM . Pharmacokinetics and brain uptake in the rhesus monkey of a fusion protein of arylsulfatase a and a monoclonal antibody against the human insulin receptor. Biotech. Bioeng.110 (5), 1456–1465 (2013).
   PubMed Web of Science ®Google Scholar
• Sumbria RK Boado RJ Pardridge WM . Brain protection from stroke with intravenous tnfalpha decoy receptor-trojan horse fusion protein. J. Cereb. Blood. Flow. Metab.32 (10), 1933–1938 (2012).
   PubMed Web of Science ®Google Scholar
• Ponka P Lok CN . The transferrin receptor: Role in health and disease. Int. J. Biochem. Cell. Biol.31 (10), 1111–1137 (1999).
   PubMed Web of Science ®Google Scholar
• Sumbria RK Zhou QH Hui EK Lu JZ Boado RJ Pardridge WM . Pharmacokinetics and brain uptake of an IgG-TNF decoy receptor fusion protein following intravenous, intraperitoneal, and subcutaneous administration in mice. Mol. Pharm.10 (4), 1425–1431 (2013).
   PubMedGoogle Scholar
• Farrington GK Caram-Salas N Haqqani AS et al. A novel platform for engineering blood–brain barrier-crossing bispecific biologics. FASEB J.28 (11), 4764–4778 (2014).
   PubMed Web of Science ®Google Scholar
• Regina A Demeule M Tripathy S et al. Ang4043, a novel brain-penetrant peptide-mab conjugate, is efficacious against her2-positive intracranial tumors in mice. Mol. Cancer. Ther.14 (1), 129–140 (2015).
   PubMed Web of Science ®Google Scholar
• Georgieva JV Hoekstra D Zuhorn IS . Smuggling drugs into the brain: an overview of ligands targeting transcytosis for drug delivery across the blood–brain barrier. Pharmaceutics6 (4), 557–583 (2014).
   PubMedGoogle Scholar
• Boado RJ Hui EK Lu JZ Pardridge WM . IgG-enzyme fusion protein: pharmacokinetics and anti-drug antibody response in rhesus monkeys. Bioconj. Chem.24 (1), 97–104 (2013).
   PubMed Web of Science ®Google Scholar
• Cornford EM Hyman S . Localization of brain endothelial luminal and abluminal transporters with immunogold electron microscopy. NeuroRx2 (1), 27–43 (2005).
   PubMedGoogle Scholar
• Pinzon-Daza ML Salaroglio IC Kopecka J et al. The cross-talk between canonical and non-canonical Wnt-dependent pathways regulates p-glycoprotein expression in human blood-brain barrier cells. J. Cereb. Blood Flow Metab.34 (8), 1258–1269 (2014).
   PubMed Web of Science ®Google Scholar
• Liu JS Wang JH Zhou J et al. Enhanced brain delivery of lamotrigine with pluronic((r)) p123-based nanocarrier. Int. J. Nanomed.9, 3923–3935 (2014).
   PubMed Web of Science ®Google Scholar
• Beccaria K Canney M Goldwirt L et al. Opening of the blood-brain barrier with an unfocused ultrasound device in rabbits. J. Neurosurg.119 (4), 887–898 (2013).
   PubMed Web of Science ®Google Scholar
• Chen H Chen CC Acosta C Wu SY Sun T Konofagou EE . A new brain drug delivery strategy: focused ultrasound-enhanced intranasal drug delivery. PLoS ONE9 (10), e108880 (2014).
   PubMed Web of Science ®Google Scholar
• Fasano A Fiorentini C Donelli G et al. Zonula occludens toxin modulates tight junctions through protein kinase c-dependent actin reorganization, in vitro. J. Clin. Invest.96 (2), 710–720 (1995).
   PubMed Web of Science ®Google Scholar
• Lu R Wang W Uzzau S Vigorito R Zielke HR Fasano A . Affinity purification and partial characterization of the zonulin/zonula occludens toxin (Zot) receptor from human brain. J. Neurochem.74 (1), 320–326 (2000).
   PubMed Web of Science ®Google Scholar
• Menon D Karyekar CS Fasano A Lu R Eddington ND . Enhancement of brain distribution of anticancer agents using deltag, the 12 kDa active fragment of Zot. Int. J. Pharm.306 (1–2), 122–131 (2005).
   PubMedGoogle Scholar
• Kim DG Bynoe MS . A2a adenosine receptor regulates the human blood–brain barrier permeability. Mol. Neurobiol. (2014) ( Epub ahead of print).
   Web of Science ®Google Scholar
• Sarkar G Curran GL Sarkaria JN Lowe VJ Jenkins RB . Peptide carrier-mediated non-covalent delivery of unmodified cisplatin, methotrexate and other agents via intravenous route to the brain. PLoS ONE9 (5), e97655 (2014).
   PubMed Web of Science ®Google Scholar
• Foley CP Rubin DG Santillan A et al. Intra-arterial delivery of aav vectors to the mouse brain after mannitol mediated blood brain barrier disruption. J. Control. Release196, 71–78 (2014).
   PubMed Web of Science ®Google Scholar
• Okuma Y Wang F Toyoshima A et al. Mannitol enhances therapeutic effects of intra-arterial transplantation of mesenchymal stem cells into the brain after traumatic brain injury. Neurosci. Lett.554, 156–161 (2013).
   PubMed Web of Science ®Google Scholar
• Joshi S Ergin A Wang M et al. Inconsistent blood brain barrier disruption by intraarterial mannitol in rabbits: Implications for chemotherapy. J. Neurooncol.104 (1), 11–19 (2011).
   PubMed Web of Science ®Google Scholar
• Kozler P Riljak V Jandova K Pokorny J . CT imaging and spontaneous behavior analysis after osmotic blood–brain barrier opening in wistar rat. Physiol. Res.63 (Suppl. 4), S529–S534 (2014).
   PubMedGoogle Scholar
• Hall WA Doolittle ND Daman M et al. Osmotic blood–brain barrier disruption chemotherapy for diffuse pontine gliomas. J. Neurooncol.77 (3), 279–284 (2006).
   PubMed Web of Science ®Google Scholar
• Mitragotri S . Devices for overcoming biological barriers: The use of physical forces to disrupt the barriers. Adv. Drug Deliv. Rev.65 (1), 100–103 (2013).
   PubMed Web of Science ®Google Scholar
• Chen H Konofagou EE . The size of blood–brain barrier opening induced by focused ultrasound is dictated by the acoustic pressure. J. Cereb. Blood Flow Metab.34 (7), 1197–1204 (2014).
   PubMed Web of Science ®Google Scholar
• Sato S Yoshida K Kawauchi S et al. Highly site-selective transvascular drug delivery by the use of nanosecond pulsed laser-induced photomechanical waves. J. Control. Release192, 228–235 (2014).
   PubMed Web of Science ®Google Scholar
• Hearst SM Walker LR Shao Q Lopez M Raucher D Vig PJ . The design and delivery of a thermally responsive peptide to inhibit s100b-mediated neurodegeneration. Neuroscience197, 369–380 (2011).
   PubMed Web of Science ®Google Scholar
• Liu W Dreher MR Chow DC Zalutsky MR Chilkoti A . Tracking the in vivo fate of recombinant polypeptides by isotopic labeling. J. Control. Release114 (2), 184–192 (2006).
   PubMed Web of Science ®Google Scholar
• Bidwell GL, 3rd Whittom AA Thomas E Lyons D Hebert MD Raucher D . A thermally targeted peptide inhibitor of symmetrical dimethylation inhibits cancer-cell proliferation. Peptides31 (5), 834–841 (2010).
   PubMed Web of Science ®Google Scholar
• Shamji MF Whitlatch L Friedman AH Richardson WJ Chilkoti A Setton LA . An injectable and in situ-gelling biopolymer for sustained drug release following perineural administration. Spine (Phila Pa 1976)33 (7), 748–754 (2008).
   PubMed Web of Science ®Google Scholar
• Bidwell GL, 3rd Perkins E Hughes J Khan M James JR Raucher D . Thermally targeted delivery of a c-myc inhibitory polypeptide inhibits tumor progression and extends survival in a rat glioma model. PLoS ONE8 (1), e55104 (2013).
   PubMed Web of Science ®Google Scholar
• Urry DW Parker TM Reid MC Gowda DC . Biocompatibility of the bioelastic materials, poly(gvgvp) and its γ-irradiation cross-linked matrix: summary of generic biological test results. Journal of Bioactive and Compatible Polymers6 (3), 263–282 (1991).
   Web of Science ®Google Scholar
• Toba M Alzoubi A O'Neill K et al. A novel vascular homing peptide strategy to selectively enhance pulmonary drug efficacy in pulmonary arterial hypertension. Am. J. Pathol.184 (2), 369–375 (2014).
   PubMed Web of Science ®Google Scholar
• Metildi CA Felsen CN Savariar EN et al. Ratiometric activatable cell-penetrating peptides label pancreatic cancer, enabling fluorescence-guided surgery, which reduces metastases and recurrence in orthotopic mouse models. Ann. Surg. Oncol.22 (6), 2082–2087 (2014).
   PubMed Web of Science ®Google Scholar
• Ouahab A Cheraga N Onoja V Shen Y Tu J . Novel ph-sensitive charge-reversal cell penetrating peptide conjugated peg-pla micelles for docetaxel delivery: In vitro study. Int. J. Pharm.466 (1–2), 233–245 (2014).
   PubMedGoogle Scholar
• Heffernan C Sumer H Guillemin GJ Manuelpillai U Verma PJ . Design and screening of a glial cell-specific, cell penetrating peptide for therapeutic applications in multiple sclerosis. PLoS ONE7 (9), e45501 (2012).
   PubMed Web of Science ®Google Scholar
• Schwarze SR Ho A Vocero-Akbani A Dowdy SF . In vivo protein transduction: delivery of a biologically active protein into the mouse. Science285 (5433), 1569–1572 (1999).
   PubMed Web of Science ®Google Scholar
• Davoli E Sclip A Cecchi M et al. Determination of tissue levels of a neuroprotectant drug: the cell permeable jnk inhibitor peptide. J. Pharm. Tox. Meth.70 (1), 55–61 (2014).
   PubMed Web of Science ®Google Scholar
• Rousselle C Clair P Temsamani J Scherrmann JM . Improved brain delivery of benzylpenicillin with a peptide-vector-mediated strategy. J. Drug Targ.10 (4), 309–315 (2002).
   PubMed Web of Science ®Google Scholar
• Liu H Zhang W Ma L et al. The improved blood–brain barrier permeability of endomorphin-1 using the cell-penetrating peptide synb3 with three different linkages. Int. J. Pharm.476 (1–2), 1–8 (2014).
   PubMedGoogle Scholar
• Meloni BP Craig AJ Milech N Hopkins RM Watt PM Knuckey NW . The neuroprotective efficacy of cell-penetrating peptides tat, penetratin, arg-9, and pep-1 in glutamic acid, kainic acid, and in vitro ischemia injury models using primary cortical neuronal cultures. Cell. Mol. Neurobiol.34 (2), 173–181 (2014).
   PubMed Web of Science ®Google Scholar
• Wolf Y Pritz S Abes S Bienert M Lebleu B Oehlke J . Structural requirements for cellular uptake and antisense activity of peptide nucleic acids conjugated with various peptides. Biochemistry45 (50), 14944–14954 (2006).
   PubMed Web of Science ®Google Scholar
• Pardridge WM . The blood–brain barrier: Bottleneck in brain drug development. NeuroRx2 (1), 3–14 (2005).
   PubMedGoogle Scholar
• Kuo YC Lee CL . Methylmethacrylate-sulfopropylmethacrylate nanoparticles with surface rmp-7 for targeting delivery of antiretroviral drugs across the blood–brain barrier. Coll. Surf. B. Biointer.90, 75–82 (2012).
   PubMed Web of Science ®Google Scholar
• Cho K Wang X Nie S Chen ZG Shin DM . Therapeutic nanoparticles for drug delivery in cancer. Clin. Cancer. Res.14 (5), 1310–1316 (2008).
   PubMed Web of Science ®Google Scholar
• Lajunen T Viitala L Kontturi LS et al. Light induced cytosolic drug delivery from liposomes with gold nanoparticles. J. Control. Release203C, 85–98 (2015).
   Google Scholar
• Knudsen KB Northeved H Ek PK et al. Differential toxicological response to positively and negatively charged nanoparticles in the rat brain. Nanotox.8 (7), 764–774 (2014).
   PubMed Web of Science ®Google Scholar
• Au C Mutkus L Dobson A Riffle J Lalli J Aschner M . Effects of nanoparticles on the adhesion and cell viability on astrocytes. Biol. Trace Elem. Res.120 (1–3), 248–256 (2007).
   PubMed Web of Science ®Google Scholar
• Kim JS Yoon TJ Yu KN et al. Toxicity and tissue distribution of magnetic nanoparticles in mice. Toxicol. Sci.89 (1), 338–347 (2006).
   PubMed Web of Science ®Google Scholar
• Mclennan DN Porter CJ Charman SA . Subcutaneous drug delivery and the role of the lymphatics. Drug Discov. Today Technol.2 (1), 89–96 (2005).
   PubMedGoogle Scholar
• Dhuria SV Hanson LR Frey WH 2nd . Intranasal delivery to the central nervous system: Mechanisms and experimental considerations. J. Pharm. Sci.99 (4), 1654–1673 (2010).
   PubMed Web of Science ®Google Scholar
• Falcone JA Salameh TS Yi X et al. Intranasal administration as a route for drug delivery to the brain: Evidence for a unique pathway for albumin. J. Pharmacol. Exp. Ther.351 (1), 54–60 (2014).
   PubMed Web of Science ®Google Scholar
• Danielyan L Schafer R Von Ameln-Mayerhofer A et al. Therapeutic efficacy of intranasally delivered mesenchymal stem cells in a rat model of parkinson disease. Rejuv. Res.14 (1), 3–16 (2011).
   PubMed Web of Science ®Google Scholar
• 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. Biomaterials34 (36), 9220–9226 (2013).
   PubMed Web of Science ®Google Scholar
• Walker LR Ryu JS Perkins E Mcnally LR Raucher D . Fusion of cell-penetrating peptides to thermally responsive biopolymer improves tumor accumulation of p21 peptide in a mouse model of pancreatic cancer. Drug Des. Devel. Ther.8, 1649–1658 (2014).
   PubMed Web of Science ®Google Scholar
• Sun Z Worden M Wroczynskyj Y et al. Magnetic field enhanced convective diffusion of iron oxide nanoparticles in an osmotically disrupted cell culture model of the blood–brain barrier. Int. J. Nanomed.9, 3013–3026 (2014).
   PubMed Web of Science ®Google Scholar
• Li J Zhang C Fan L et al. Brain delivery of nap with peg-plga nanoparticles modified with phage display peptides. Pharm. Res.30 (7), 1813–1823 (2013).
   PubMed Web of Science ®Google Scholar