Visualization and Quantitative Assessment of the Brain Distribution of Insulin through Nose-to-Brain Delivery Based on the Cell-Penetrating Peptide Noncovalent Strategy

Molecular Pharmaceutics

Volumn 13, Issue 3, 2016, Pages 1004-1011

  Kamei, Noriyasu ^a   Shingaki, Tomotaka ^b   Kanayama, Yousuke ^b   Tanaka, Misa ^a   Zochi, Riyo ^b   Hasegawa, Koki ^c,d   Watanabe, Yasuyoshi ^b   Takeda Morishita, Mariko ^a  

^a KOBE GAKUIN UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

^d KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

biopharmaceuticals; brain delivery; cell penetrating peptides; insulin; intranasal administration

Indexed keywords

COPPER 64; DEXTRO PENETRATIN; LEVO PENETRATIN; N HYDROXYSUCCINIMIDE; PENETRATIN; RECOMBINANT HUMAN INSULIN; UNCLASSIFIED DRUG; 1-(1,3-CARBOXYPROPYL)-4,7-CARBOXYMETHYL-1,4,7-TRIAZACYCLONONANE; ACETIC ACID DERIVATIVE; ANTIDIABETIC AGENT; COPPER; INSULIN; SINGLE HETEROCYCLIC RINGS;

ANIMAL EXPERIMENT; ARTICLE; AUTORADIOGRAPHY; BRAIN CORTEX; BRAIN STEM; CEREBELLUM; CEREBROSPINAL FLUID; CONTROLLED STUDY; DRUG ABSORPTION; DRUG ACCUMULATION; DRUG BRAIN LEVEL; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG TRANSPORT; ENZYME LINKED IMMUNOSORBENT ASSAY; GAMMA COUNTER; HYPOTHALAMUS; IN VIVO STUDY; ISOTOPE LABELING; MALE; NONHUMAN; NOSE CAVITY; OLFACTORY BULB; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RADIOACTIVITY; RAT; ANIMAL; BRAIN; CHEMISTRY; INTESTINE ABSORPTION; INTRANASAL DRUG ADMINISTRATION; METABOLISM; NOSE; SPRAGUE DAWLEY RAT; TISSUE DISTRIBUTION;

ACETATES; ADMINISTRATION, INTRANASAL; ANIMALS; AUTORADIOGRAPHY; BRAIN; COPPER RADIOISOTOPES; DRUG DELIVERY SYSTEMS; HETEROCYCLIC COMPOUNDS, 1-RING; HYPOGLYCEMIC AGENTS; INSULIN; INTESTINAL ABSORPTION; MALE; NOSE; RATS; RATS, SPRAGUE-DAWLEY; TISSUE DISTRIBUTION;

EID: 84960146154     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/acs.molpharmaceut.5b00854     Document Type: Article

References (33)

1. Chen, Y.; Liu, L. Modern methods for delivery of drugs across the blood-brain barrier Adv. Drug Delivery Rev. 2012, 64 (7) 640-65 10.1016/j.addr.2011.11.010
2. Pardridge, W. M. Re-engineering biopharmaceuticals for delivery to brain with molecular Trojan horses Bioconjugate Chem. 2008, 19 (7) 1327-1338 10.1021/bc800148t
3. Herve, F.; Ghinea, N.; Scherrmann, J. M. CNS delivery via adsorptive transcytosis AAPS J. 2008, 10 (3) 455-72 10.1208/s12248-008-9055-2
4. Lochhead, J. J.; Thorne, R. G. Intranasal delivery of biologics to the central nervous system Adv. Drug Delivery Rev. 2012, 64 (7) 614-28 10.1016/j.addr.2011.11.002
5. Dhuria, S. V.; Hanson, L. R.; Frey, W. H., 2nd. Intranasal delivery to the central nervous system: mechanisms and experimental considerations J. Pharm. Sci. 2010, 99 (4) 1654-73 10.1002/jps.21924
6. Thorne, R. G.; Emory, C. R.; Ala, T. A.; Frey, W. H., 2nd. Quantitative analysis of the olfactory pathway for drug delivery to the brain Brain Res. 1995, 692 (1-2) 278-82 10.1016/0006-8993(95)00637-6
7. Thorne, R. G.; Pronk, G. J.; Padmanabhan, V.; Frey, W. H., 2nd. Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration Neuroscience 2004, 127 (2) 481-96 10.1016/j.neuroscience.2004.05.029
8. Thorne, R. G.; Hanson, L. R.; Ross, T. M.; Tung, D.; Frey, W. H., 2nd. Delivery of interferon-beta to the monkey nervous system following intranasal administration Neuroscience 2008, 152 (3) 785-97 10.1016/j.neuroscience.2008.01.013
9. Banks, W. A.; During, M. J.; Niehoff, M. L. Brain uptake of the glucagon-like peptide-1 antagonist exendin(9-39) after intranasal administration J. Pharmacol. Exp. Ther. 2004, 309 (2) 469-75 10.1124/jpet.103.063222
10. Nonaka, N.; Farr, S. A.; Kageyama, H.; Shioda, S.; Banks, W. A. Delivery of galanin-like peptide to the brain: targeting with intranasal delivery and cyclodextrins J. Pharmacol. Exp. Ther. 2008, 325 (2) 513-9 10.1124/jpet.107.132381
11. Renner, D. B.; Svitak, A. L.; Gallus, N. J.; Ericson, M. E.; Frey, W. H., 2nd; Hanson, L. R. Intranasal delivery of insulin via the olfactory nerve pathway J. Pharm. Pharmacol. 2012, 64 (12) 1709-14 10.1111/j.2042-7158.2012.01555.x
12. Fliedner, S.; Schulz, C.; Lehnert, H. Brain uptake of intranasally applied radioiodinated leptin in Wistar rats Endocrinology 2006, 147 (5) 2088-94 10.1210/en.2005-1016
13. Dufes, C.; Olivier, J.-C.; Gaillard, F.; Gaillard, A.; Couet, W.; Muller, J.-M. Brain delivery of vasoactive intestinal peptide (VIP) following nasal administration to rats Int. J. Pharm. 2003, 255 (1-2) 87-97 10.1016/S0378-5173(03)00039-5
14. Kamei, N.; Takeda-Morishita, M. Brain delivery of insulin boosted by intranasal coadministration with cell-penetrating peptides J. Controlled Release 2015, 197, 105-10 10.1016/j.jconrel.2014.11.004
15. Lee, S.; Kim, K.; Kumar, T. S.; Lee, J.; Kim, S. K.; Lee, D. Y.; Lee, Y. K.; Byun, Y. Synthesis and biological properties of insulin-deoxycholic acid chemical conjugates Bioconjugate Chem. 2005, 16 (3) 615-20 10.1021/bc049871e
16. Obata, A.; Kasamatsu, S.; McCarthy, D. W.; Welch, M. J.; Saji, H.; Yonekura, Y.; Fujibayashi, Y. Production of therapeutic quantities of (64)Cu using a 12 MeV cyclotron Nucl. Med. Biol. 2003, 30 (5) 535-9 10.1016/S0969-8051(03)00024-6
17. McCarthy, D. W.; Shefer, R. E.; Klinkowstein, R. E.; Bass, L. A.; Margeneau, W. H.; Cutler, C. S.; Anderson, C. J.; Welch, M. J. Efficient production of high specific activity 64Cu using a biomedical cyclotron Nucl. Med. Biol. 1997, 24 (1) 35-43 10.1016/S0969-8051(96)00157-6
18. Hirai, S.; Yashiki, T.; Matsuzawa, T.; Mima, H. Absorption of drugs from the nasal mucosa of rat Int. J. Pharm. 1981, 7 (4) 317-325 10.1016/0378-5173(81)90058-2
19. Khafagy; el, S.; Morishita, M.; Isowa, K.; Imai, J.; Takayama, K. Effect of cell-penetrating peptides on the nasal absorption of insulin J. Controlled Release 2009, 133 (2) 103-8 10.1016/j.jconrel.2008.09.076
20. Khafagy; el, S.; Kamei, N.; Nielsen, E. J.; Nishio, R.; Takeda-Morishita, M. One-month subchronic toxicity study of cell-penetrating peptides for insulin nasal delivery in rats Eur. J. Pharm. Biopharm. 2013, 85 (3) 736-43 10.1016/j.ejpb.2013.09.014
21. Schioth, H. B.; Craft, S.; Brooks, S. J.; Frey, W. H., 2nd; Benedict, C. Brain insulin signaling and Alzheimer's disease: current evidence and future directions Mol. Neurobiol. 2012, 46 (1) 4-10 10.1007/s12035-011-8229-6
22. Aoki, Y.; Yahata, N.; Watanabe, T.; Takano, Y.; Kawakubo, Y.; Kuwabara, H.; Iwashiro, N.; Natsubori, T.; Inoue, H.; Suga, M.; Takao, H.; Sasaki, H.; Gonoi, W.; Kunimatsu, A.; Kasai, K.; Yamasue, H. Oxytocin improves behavioural and neural deficits in inferring others' social emotions in autism Brain 2014, 137 (11) 3073-86 10.1093/brain/awu231
23. Schulz, C.; Paulus, K.; Lehnert, H. Central nervous and metabolic effects of intranasally applied leptin Endocrinology 2004, 145 (6) 2696-701 10.1210/en.2003-1431
24. Shingaki, T.; Inoue, D.; Furubayashi, T.; Sakane, T.; Katsumi, H.; Yamamoto, A.; Yamashita, S. Transnasal Delivery of Methotrexate to Brain Tumors in Rats: A New Strategy for Brain Tumor Chemotherapy Mol. Pharmaceutics 2010, 7, 1561-1568 10.1021/mp900275s
25. 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 Delivery Rev. 2009, 61 (11) 953-64 10.1016/j.addr.2009.06.001
26. Heitz, F.; Catherine, M.; Divita, G. Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics Br. J. Pharmacol. 2009, 157, 195-206 10.1111/j.1476-5381.2009.00057.x
27. Foerg, C.; Merkle, H. P. On the biomedical promise of cell penetrating peptides: limits versus prospects J. Pharm. Sci. 2008, 97 (1) 144-62 10.1002/jps.21117
28. Brock, R. The uptake of arginine-rich cell-penetrating peptides: putting the puzzle together Bioconjugate Chem. 2014, 25 (5) 863-8 10.1021/bc500017t
29. El-Sayed, A.; Futaki, S.; Harashima, H. Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment AAPS J. 2009, 11 (1) 13-22 10.1208/s12248-008-9071-2
30. Said Hassane, F.; Saleh, A. F.; Abes, R.; Gait, M. J.; Lebleu, B. Cell penetrating peptides: overview and applications to the delivery of oligonucleotides Cell. Mol. Life Sci. 2010, 67 (5) 715-26 10.1007/s00018-009-0186-0
31. Kamei, N.; Morishita, M.; Takayama, K. Importance of intermolecular interaction on the improvement of intestinal therapeutic peptide/protein absorption using cell-penetrating peptides J. Controlled Release 2009, 136 (3) 179-86 10.1016/j.jconrel.2009.02.015
32. Khafagy, E.-S.; Morishita, M.; Takayama, K. The role of intermolecular interactions with penetratin and its analogue on the enhancement of absorption of nasal therapeutic peptides Int. J. Pharm. 2010, 388 (1-2) 209-12 10.1016/j.ijpharm.2009.12.060
33. Kamei, N.; Onuki, Y.; Takayama, K.; Takeda-Morishita, M. Mechanistic study of the uptake/permeation of cell-penetrating peptides across a caco-2 monolayer and their stimulatory effect on epithelial insulin transport J. Pharm. Sci. 2013, 102 (11) 3998-4008 10.1002/jps.23708