Muscle-targeted hydrodynamic gene introduction of insulin-like growth factor-1 using polyplex nanomicelle to treat peripheral nerve injury

Journal of Controlled Release

Volumn 183, Issue 1, 2014, Pages 27-34

  Nagata, Kazuya ^a   Itaka, Keiji ^a   Baba, Miyuki ^a   Uchida, Satoshi ^a   Ishii, Takehiko ^b   Kataoka, Kazunori ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Gene delivery; Hydrodynamic injection; Insulin like growth factor 1 (IGF 1); Muscle atrophy; Peripheral nerve injury; Polyplex nanomicelle

Indexed keywords

BIOCOMPATIBILITY; BIOMOLECULES; DNA; GENE TRANSFER; GENES; HYDRODYNAMICS; INSULIN; MAMMALS; PATHOLOGY; RECOVERY;

GENE DELIVERY; HYDRODYNAMIC INJECTION; INSULIN-LIKE GROWTH FACTOR-1; MUSCLE ATROPHY; NANOMICELLE; PERIPHERAL NERVES;

MUSCLE;

MYOD PROTEIN; MYOGENIN; PLASMID DNA; SOMATOMEDIN C; BIOMATERIAL; DNA; DRUG CARRIER; INSULIN-LIKE GROWTH FACTOR-1, MOUSE; MICELLE; MYOGENIC FACTOR; NANOMATERIAL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOCOMPATIBILITY; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; HISTOLOGY; HYDRODYNAMICS BASED TRANSFECTION; MALE; MICELLE; MOTOR PERFORMANCE; MOUSE; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE HYPERTROPHY; MUSCLE MASS; NERVE REGENERATION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PARALYSIS; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; QUADRICEPS FEMORIS MUSCLE; SCIATIC NERVE INJURY; SKELETAL MUSCLE; TRICEPS SURAE MUSCLE; UPREGULATION; WALKING; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; GENE EXPRESSION; GENE TRANSFER; GENETICS; HYDRODYNAMICS; INNERVATION; INTRAMUSCULAR DRUG ADMINISTRATION; METABOLISM; MOTOR ACTIVITY; MUSCULAR ATROPHY; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PERIPHERAL NERVE INJURIES; PHYSIOLOGY; PLASMID; SCIATIC NERVE;

ANIMALS; BIOCOMPATIBLE MATERIALS; DNA; DRUG CARRIERS; FEMALE; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; HYDRODYNAMICS; INJECTIONS, INTRAMUSCULAR; INSULIN-LIKE GROWTH FACTOR I; MICE, INBRED BALB C; MICELLES; MOTOR ACTIVITY; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOGENIC REGULATORY FACTORS; NANOSTRUCTURES; ORGAN SIZE; PERIPHERAL NERVE INJURIES; PLASMIDS; SCIATIC NERVE;

EID: 84898075717     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.03.021     Document Type: Article

References (42)

1. V.T. Ribeiro-Resende, A. Carrier-Ruiz, R.L. RM, R.A. Reis, and R. Mendez-Otero Bone marrow-derived fibroblast growth factor-2 induces glial cell proliferation in the regenerating peripheral nervous system Mol. Neurodegener. 7 2012 34
2. S. Barati, P.R. Hurtado, S.H. Zhang, R. Tinsley, I.A. Ferguson, and R.A. Rush GDNF gene delivery via the p75(NTR) receptor rescues injured motor neurons Exp. Neurol. 202 2006 179 188 (Pubitemid 44344257)
3. F.C. Cheng, M.H. Tai, M.L. Sheu, C.J. Chen, D.Y. Yang, H.L. Su, S.P. Ho, S.Z. Lai, and H.C. Pan Enhancement of regeneration with glia cell line-derived neurotrophic factor-transduced human amniotic fluid mesenchymal stem cells after sciatic nerve crush injury J. Neurosurg. 112 2010 868 879
4. V.J. Tom, H.R. Sandrow-Feinberg, K. Miller, C. Domitrovich, J. Bouyer, V. Zhukareva, M.C. Klaw, M.A. Lemay, and J.D. Houle Exogenous BDNF enhances the integration of chronically injured axons that regenerate through a peripheral nerve grafted into a chondroitinase-treated spinal cord injury site Exp. Neurol. 239C 2012 91 100
5. A. Brockington, C. Lewis, S. Wharton, and P.J. Shaw Vascular endothelial growth factor and the nervous system Neuropathol. Appl. Neurobiol. 30 2004 427 446 (Pubitemid 39423031)
6. F.R. Pereira Lopes, B.C. Lisboa, F. Frattini, F.M. Almeida, M.A. Tomaz, P.K. Matsumoto, F. Langone, S. Lora, P.A. Melo, R. Borojevic, S.W. Han, and A.M. Martinez Enhancement of sciatic nerve regeneration after vascular endothelial growth factor (VEGF) gene therapy Neuropathol. Appl. Neurobiol. 37 2011 600 612
7. J.R. Florini, D.Z. Ewton, and S.A. Coolican Growth hormone and the insulin-like growth factor system in myogenesis Endocr. Rev. 17 1996 481 517 (Pubitemid 26346639)
8. A. Musaro, K. McCullagh, A. Paul, L. Houghton, G. Dobrowolny, M. Molinaro, E.R. Barton, H.L. Sweeney, and N. Rosenthal Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle Nat. Genet. 27 2001 195 200 (Pubitemid 32157448)
9. E.D. Rabinovsky, E. Gelir, S. Gelir, H. Lui, M. Kattash, F.J. DeMayo, S.M. Shenaq, and R.J. Schwartz Targeted expression of IGF-1 transgene to skeletal muscle accelerates muscle and motor neuron regeneration FASEB J. 17 2003 53 55
10. T. Shavlakadze, J.D. White, M. Davies, J.F. Hoh, and M.D. Grounds Insulin-like growth factor I slows the rate of denervation induced skeletal muscle atrophy Neuromuscul. Disord. 15 2005 139 146 (Pubitemid 40202740)
11. G.R. Adams, and S.A. McCue Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats J. Appl. Physiol. 84 1998 1716 1722 (Pubitemid 28225913)
12. C. Kasemkijwattana, J. Menetrey, P. Bosch, G. Somogyi, M.S. Moreland, F.H. Fu, B. Buranapanitkit, S.S. Watkins, and J. Huard Use of growth factors to improve muscle healing after strain injury Clin. Orthop. Relat. Res. 2000 272 285 (Pubitemid 30059163)
13. A.M. Payne, Z. Zheng, M.L. Messi, C.E. Milligan, E. Gonzalez, and O. Delbono Motor neurone targeting of IGF-1 prevents specific force decline in ageing mouse muscle J. Physiol. 570 2006 283 294
14. J.D. Schertzer, and G.S. Lynch Comparative evaluation of IGF-I gene transfer and IGF-I protein administration for enhancing skeletal muscle regeneration after injury Gene Ther. 13 2006 1657 1664 (Pubitemid 44774210)
15. E.R. Barton-Davis, D.I. Shoturma, A. Musaro, N. Rosenthal, and H.L. Sweeney Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function Proc. Natl. Acad. Sci. U. S. A. 95 1998 15603 15607 (Pubitemid 29018746)
16. T. Takahashi, K. Ishida, K. Itoh, Y. Konishi, K.I. Yagyu, A. Tominaga, J.I. Miyazaki, and H. Yamamoto IGF-I gene transfer by electroporation promotes regeneration in a muscle injury model Gene Ther. 10 2003 612 620 (Pubitemid 36553606)
17. M.B. Alzghoul, D. Gerrard, B.A. Watkins, and K. Hannon Ectopic expression of IGF-I and Shh by skeletal muscle inhibits disuse-mediated skeletal muscle atrophy and bone osteopenia in vivo FASEB J. 18 2004 221 223
18. S. Lee, E.R. Barton, H.L. Sweeney, and R.P. Farrar Viral expression of insulin-like growth factor-I enhances muscle hypertrophy in resistance-trained rats J. Appl. Physiol. 96 2004 1097 1104 (Pubitemid 38248688)
19. J.E. Stevens-Lapsley, F. Ye, M. Liu, S.E. Borst, C. Conover, K.E. Yarasheski, G.A. Walter, H.L. Sweeney, and K. Vandenborne Impact of viral-mediated IGF-I gene transfer on skeletal muscle following cast immobilization Am. J. Physiol. Endocrinol. Metab. 299 2010 E730 E740
20. F. Liu, Y. Song, and D. Liu Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA Gene Ther. 6 1999 1258 1266 (Pubitemid 29359019)
21. J.E. Hagstrom, J. Hegge, G. Zhang, M. Noble, V. Budker, D.L. Lewis, H. Herweijer, and J.A. Wolff A facile nonviral method for delivering genes and siRNAs to skeletal muscle of mammalian limbs Mol. Ther. 10 2004 386 398 (Pubitemid 39117883)
22. K. Itaka, K. Osada, K. Morii, P. Kim, S.H. Yun, and K. Kataoka Polyplex nanomicelle promotes hydrodynamic gene introduction to skeletal muscle J. Control. Release 143 2010 112 119
23. K. Itaka, and K. Kataoka Progress and prospects of polyplex nanomicelles for plasmid DNA delivery Curr. Gene Ther. 11 2011 457 465
24. K. Itaka, and K. Kataoka Recent development of nonviral gene delivery systems with virus-like structures and mechanisms Eur. J. Pharm. Biopharm. 71 2009 475 483
25. N. Kanayama, S. Fukushima, N. Nishiyama, K. Itaka, W.D. Jang, K. Miyata, Y. Yamasaki, U.I. Chung, and K. Kataoka A PEG-based biocompatible block catiomer with high buffering capacity for the construction of polyplex micelles showing efficient gene transfer toward primary cells ChemMedChem 1 2006 439 444
26. K. Itaka, T. Ishii, Y. Hasegawa, and K. Kataoka Biodegradable polyamino acid-based polycations as safe and effective gene carrier minimizing cumulative toxicity Biomaterials 31 2010 3707 3714
27. K. Itaka, S. Ohba, K. Miyata, H. Kawaguchi, K. Nakamura, T. Takato, U.I. Chung, and K. Kataoka Bone regeneration by regulated in vivo gene transfer using biocompatible polyplex nanomicelles Mol. Ther. 15 2007 1655 1662 (Pubitemid 47289009)
28. M. Harada-Shiba, I. Takamisawa, K. Miyata, T. Ishii, N. Nishiyama, K. Itaka, K. Kangawa, F. Yoshihara, Y. Asada, K. Hatakeyama, N. Nagaya, and K. Kataoka Intratracheal gene transfer of adrenomedullin using polyplex nanomicelles attenuates monocrotaline-induced pulmonary hypertension in rats Mol. Ther. 17 2009 1180 1186
29. S. Uchida, K. Itaka, Q. Chen, K. Osada, K. Miyata, T. Ishii, M. Harada-Shiba, and K. Kataoka Combination of chondroitin sulfate and polyplex micelles from poly(ethylene glycol)-poly{N′-[N-(2-aminoethyl)-2- aminoethyl]aspartamide} block copolymer for prolonged in vivo gene transfection with reduced toxicity J. Control. Release 155 2011 296 302
30. J.R. Bain, S.E. Mackinnon, and D.A. Hunter Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat Plast. Reconstr. Surg. 83 1989 129 138
31. T. Kawamoto, and M. Shimizu A method for preparing 2- to 50-micron-thick fresh-frozen sections of large samples and undecalcified hard tissues Histochem. Cell Biol. 113 2000 331 339 (Pubitemid 30341300)
32. T. Kawamoto Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants Arch. Histol. Cytol. 66 2003 123 143 (Pubitemid 36834422)
33. M.M. Inserra, D.A. Bloch, and D.J. Terris Functional indices for sciatic, peroneal, and posterior tibial nerve lesions in the mouse Microsurgery 18 1998 119 124 (Pubitemid 28294803)
34. T. Murakami, M. Arai, Y. Sunada, and A. Nakamura VEGF 164 gene transfer by electroporation improves diabetic sensory neuropathy in mice J. Gene Med. 8 2006 773 781
35. M. Nakamura-Craig, and R.L. Follenfant Effect of lamotrigine in the acute and chronic hyperalgesia induced by PGE2 and in the chronic hyperalgesia in rats with streptozotocin-induced diabetes Pain 63 1995 33 37
36. Y. Choi, Y.W. Yoon, H.S. Na, S.H. Kim, and J.M. Chung Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain Pain 59 1994 369 376
37. P. Muangman, L.A. Muffley, J.P. Anthony, M.L. Spenny, R.A. Underwood, J.E. Olerud, and N.S. Gibran Nerve growth factor accelerates wound healing in diabetic mice Wound Repair Regen. 12 2004 44 52 (Pubitemid 38249135)
38. J.M. Kennedy, and D.W. Zochodne Impaired peripheral nerve regeneration in diabetes mellitus J. Peripher. Nerv. Syst. 10 2005 144 157 (Pubitemid 40984889)
39. K.A. Sullivan, B. Kim, and E.L. Feldman Insulin-like growth factors in the peripheral nervous system Endocrinology 149 2008 5963 5971
40. Q. Chu, R. Moreland, N.S. Yew, J. Foley, R. Ziegler, and R.K. Scheule Systemic insulin-like growth factor-1 reverses hypoalgesia and improves mobility in a mouse model of diabetic peripheral neuropathy Mol. Ther. 16 2008 1400 1408
41. M. Miura, M. Sasaki, K. Mizukoshi, M. Shibasaki, Y. Izumi, G. Shimosato, and F. Amaya Peripheral sensitization caused by insulin-like growth factor 1 contributes to pain hypersensitivity after tissue injury Pain 152 2011 888 895
42. T.B. Seo, M.J. Oh, B.G. You, K.B. Kwon, I.A. Chang, J.H. Yoon, C.Y. Lee, and U. Namgung ERK1/2-mediated Schwann cell proliferation in the regenerating sciatic nerve by treadmill training J. Neurotrauma 26 2009 1733 1744