Plasmid delivery to muscle: Recent advances in polymer delivery systems

Advanced Drug Delivery Reviews

Volumn 30, Issue 1-3, 1998, Pages 151-172

  Mumper, Russell J ^a   Rolland, Alain P ^a  

^a GeneMedicine Inc   (United States)

Author keywords

Amphiphilic; Complexation; DNA; Gene delivery; Hydrogen bonding; Muscle; Plasmid; Polyvinyl alcohol; Polyvinyl pyrrolidone

Indexed keywords

CELLS; COMPLEXATION; DNA; GENES; HORMONES; HYDROGEN BONDS; MEDICAL PROBLEMS; MUSCLE; ORGANIC POLYMERS; PHARMACOKINETICS; PHYSIOLOGY; POLYVINYL ALCOHOLS;

BIOAVAILABILITY; HUMAN GROWTH HORMONE; PLASMID; POLYVINYL PYRROLIDONE;

DRUG THERAPY;

BETA GALACTOSIDASE; BUPIVACAINE; HUMAN GROWTH HORMONE; MACROGOL; NUCLEIC ACID; PLASMID DNA; POLYMER; POLYVINYL ALCOHOL; POLYVINYL DERIVATIVE; POVIDONE; SOMATOMEDIN C; SUCROSE; TOXIN; VACCINE;

CLINICAL TRIAL; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG STRUCTURE; DRUG UPTAKE; GENE DOSAGE; GENE EXPRESSION; GENE TARGETING; HUMAN; IMMUNOHISTOCHEMISTRY; INJECTION; INTRAMUSCULAR DRUG ADMINISTRATION; MUSCLE FUNCTION; MUSCLE REGENERATION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; SKELETAL MUSCLE; STRUCTURE ACTIVITY RELATION; SUSTAINED RELEASE PREPARATION;

EID: 0032473414     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-409X(97)00113-0     Document Type: Review

References (108)

1. Wolff J.A., Malone R.W., Williams P., Chong W., Acsadi G., Jani A. Direct gene transfer into mouse muscle in vivo. Science. 247:1990;1465-1468.
2. Hagstrom J.E., Rybakova I.N., Staeva T., Wolff J.A., Ervasti J.M. Non-nuclear DNA binding proteins in striated muscle. Biochem. Mol. Med. 58:1996;113-121.
3. Wolff J.A., Ludtke J.J., Acsadi G., Williams P., Jani A. Long-term persistence of plasmid DNA and foreign gene expression in mouse muscle. Hum. Mol. Genet. 1:1992;363-369.
4. P.L. Felgner, J.A. Wolff, G.H. Rhodes, R.W. Malone, D.A. Carson, Delivery of exogenous DNA sequences in a mammal. Patent Number 05580859. December 3, 1996.
5. Acsadi G., Dickson G., Love D.R., Jani A., Walsh F.S., Wolff J.A. Human dystrophin expression in mdx mice after intramuscular injection of DNA constructs. Nature. 352:1991;815-818.
6. Karpati G., Acsadi G. The potential for gene therapy in Duchenne Muscular Dystrophy and other genetic muscle diseases. Muscle Nerve. 16:1993;1141-1153.
7. Miller J.B., Boyce F.M. Gene therapy by and for muscle cells. Trends Genet. 11:1995;163-165.
8. M.E. Coleman, D. Criswell, F.W. Booth, H.A. Alila, Non-viral IGF-I gene therapy reduces atrophy and loss of muscle strength in tibialis anterior muscles of hindlimb suspended mice, 1997, unpublished.
9. H. Alila, M. Coleman, M. French, H. Nitta, Q. Liu, J. Wang, J. Nordstrom, A. Rolland, Expression of biologically active human insulin-like growth factor-I following intramuscular injection of a formulated DNA plasmid in rats, 1997, Submitted to Hum. Gene Ther.
10. E. Rabinovsky, M. Kataash, H. Nitta, H. Alila, Q. Liu, T. Meyer, R. Schwartz, M. Coleman, Non-viral gene therapy enhances recovery following sciatic nerve crush, 1997, submitted to Nature Med.
11. K. Anwer, M. Shi, M.F. French, S.R. Muller, W. Chen, Q. Liu, B.L. Thompson, J. Wang, R.J. Mumper, A.P. Rolland, H. Alila, Systemic effect of human growth hormone after intramuscular injection of a single dose of a muscle-specific gene medicine, 1997, submitted to Nature Med.
12. Kuwahara-Rundell A.Y., Margalith M., Rhodes G., Yankauckas M., Dwarki V.J. Expression of dog Factor-IX protein after intramuscular DNA injections in mice. J. Cell. Biochem. Suppl. 18A:1994;233.
13. Miller G., Steinbrecher R.A., Murdock P., Pasi K.J., Tuddenham E.G.D., Lee C.A., Goldspink G. Expression of Factor-VII in vitro and in vivo following direct gene transfer into muscle: a model for hemophilia. Gene Ther. 1 Suppl. 2:1994;S16.
14. S.K. Tripathy, E.C. Svensson, H.B. Black, E. Goldwasser, et al., Long-term expression of erythropoietin in the systemic circulation of mice after intramuscular injection of a plasmid DNA vector. Proc. Natl. Acad. Sci. U.S.A. 93, 10876-10880.
15. Dahler A., Wade R.P., Muscat G.E.O., Waters M.J. Expression vectors encoding human growth hormone (hGH) controlled by human muscle-specific promoters: prospects for regulated production of hGH delivered by myoblast transfer or intravenous injection. Gene. 145:1994;305-310.
16. Levy M.Y., Barron L.G., Meyer K.B., Szoka F.C. Characterization of plasmid DNA transfer into mouse skeletal muscle: evaluation of uptake mechanism, expression and secretion of gene products into blood. Gene Ther. 3:1996;201-211.
17. Raz E., Watanabe A., Baird S.M.et al. Systemic immunological effects of cytokine genes injected into skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 90:1993;4523-4527.
18. Fazio V.M., Fazio S., Rinaldi M., Catani M.V., Zotti S., Ciafre S.A. Accumulation of human apolipoprotein-E in rat plasma after in vivo intramuscular injection of naked DNA. Biochem. Biophys. Res. Commun. 200:1994;298-305.
19. Ma J., Yang Z., Chao J., Chao L. Intramuscular delivery of rat kallikrein-binding protein gene reverses hypotension in transgenic mice expressing human tissue kallikrein. J. Biol. Chem. 270:1995;451-455.
20. Xiong W., Chao J., Chao L. Muscle delivery of human kallikrein gene reduces blood pressure in hypertensive rats. Hypertension. 25:1995;715-719.
21. Manickan E., Rouse R.J., Yu Z., Wire W.S., Rouse B.T. Genetic immunization against herpes simplex virus. Protection is mediated by CD4+ T lymphocytes. J. Immunol. 155:1995;259-265.
22. Ghiasi H., Cai S., Slanina S., Nesburn A.B., Wechsler S.L. Vaccination of mice with herpes simplex virus type 1 glycoprotein D DNA produces low levels of protection against lethal HSV-1 challenge. Antiviral Res. 28:1995;147-157.
23. McClements W.L., Armstrong M.E., Keys R.D., Liu M.A. Immunization with DNA vaccines encoding glycoprotein D or glycoprotein B, alone or in combination, induces protective immunity in animal models of herpes simplex virus-2 disease. Proc. Natl. Acad. Sci. U.S.A. 93:1996;11414-11420.
24. Kriesel J.D., Spruance S.L., Daynes R.A., Araneo B.A. Nucleic acid vaccine encoding gD2 protects mice from herpes simplex virus type 2 disease. J. Infect. Dis. 173:1996;536-541.
25. Davis H.L., McCluskie M.J., Gerin J.L., Purcell R.H. DNA vaccine for hepatitis B: evidence for immunogenicity in chimpanzees and comparison with other vaccines. Proc. Natl. Acad. Sci. U.S.A. 93:1996;7213-7218.
26. Davis H.L., Michel M.L., Whalen R.G. DNA-based immunization for hepatitis B induces continuous secretion of antigen and high levels of circulating antibody. Hum. Mol. Genet. 2:1993;1847-1851.
27. Davis H.L., Michel M.L., Mancini M., Schleef M., Whalen R.G. Direct gene transfer in skeletal muscle: plasmid DNA-based immunization against the hepatitis B virus surface antigen. Vaccine. 12:1994;1503-1509.
28. Donnelly J.J., Friedman A., Martinez D., Montgomery D.L.et al. Preclinical efficacy of a prototype DNA vaccine: enhanced protection against antigenic drift in influenza virus. Nat. Med. 1:1995;521-522.
29. J.B. Ulmer, J.J. Donnelly, S.E. Parker, G.H. Rhodes, P.L. Felgner, et al., Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259 (1993) 1745-1749.
30. Ulmer J.B., Deck R.R., DeWitt C.M., Friedman A., Donnelly J.J., Liu M.A. Protective immunity by intramuscular injection of low doses of influenza DNA vaccines. Vaccine. 12:1994;1541-1544.
31. Lowrie D.B., Tascon R.E., Colston M.J., Silva C.L. Towards a DNA vaccine against tuberculosis. Vaccine. 12:1994;1537-1540.
32. Tascon R.E., Colston M.J., Ragno S., Stavropoulos E., Gregory D., Lowrie D.B. Vaccination against tuberculosis by DNA injection. Nat. Med. 2:1996;888-892.
33. Shiver J.W., Perry H.C., Davies M.E., Freed D.C., Liu M.A. Cytotoxic T lymphocyte and helper T cell responses following HIV polynucleotide vaccination. Ann. N.Y. Acad. Sci. 772:1995;198-208.
34. Coney L., Wang B., Ugen K.E., Boyer J.et al. Facilitated DNA inoculation induces anti-HIV-1 immunity in vivo. Vaccine. 12:1994;1545-1550.
35. Wang B., Ugen K.E., Srikantan V., Agadjanyan M.G.et al. Gene inoculation generates immune responses against human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U.S.A. 90:1993;4156-4160.
36. Russell S.J., Winter G., Stevenson F.K., Hamblin T.J., Hawkins R.E. Plasmid vaccination to elicit anti-idiotypic immune responses against surface immunoglobulin-positive B-cell malignancies. Br. J. Haematol. Suppl. 1. 86:1994;74.
37. Hoffman S.L., Doolan D.L., Sedegah M., Gramzinski R.et al. Nucleic acid malaria vaccines. Current status and potential. Ann. N.Y. Acad. Sci. 772:1995;88-94.
38. Sedegah M., Hedstrom R., Hobart P., Hoffman S.L. Protection against malaria by immunization with circumsporozoite protein plasmid DNA. Proc. Natl. Acad. Sci. U.S.A. 91:1994;9866-9870.
39. Major M.E., Vitvitski L., Mink M.A., Schleef M.et al. DNA-based immunization with chimeric vectors for the induction of immune responses against the hepatitis C virus nucleocapsid. J. Virol. 69:1995;5798-5805.
40. Lagging L.M., Meyer K., Hoft D., Houghton M., Belshe R.B., Ray R. Immune response to plasmid DNA encoding the hepatitis C virus core protein. J. Virol. 69:1995;5859-5863.
41. Phillpotts R.J., Venugopal K., Brooks T. Immunization with DNA polynucleotides protects mice against lethal challenge with St. Louis encephalitis virus. Arch. Virol. 141:1996;743-749.
42. Pande H., Campo K., Tanamachi B., Forman S.J., Zaia J.A. Direct DNA immunization of mice with plasmid DNA encoding the tegument protein pp65(ppUL83) of human cytomegalovirus induces high levels of circulating antibody to the encoded protein. Scand. J. Infect. Dis. Suppl. 99:1995;117-120.
43. Lopez-Macias C., Lopez-Hernandez M.A., Gonzalez C.R., Isibasi A., Ortiz-Navarrete V. Induction of antibodies against Salmonella typhi OmpC porin by naked DNA immunization. Ann. N.Y. Acad. Sci. 772:1995;285-288.
44. Lai W.C., Bennet M., Johnston S.A., Barry M.A., Pakes S.P. Protection against Mycoplasma pulmonis infection by genetic vaccination. DNA Cell Biol. 14:1995;643-651.
45. Xiang Z.Q., Spitalnik S.L., Cheng J., Erikson J., Wojczyk B., Ertl H.C. Immune response to nucleic acid vaccines to rabies virus. Virology. 209:1995;569-579.
46. Mumper R.J., Duguid J.G., Anwer K., Barron M.K., Nitta H., Rolland A.P. Polyvinyl derivatives for controlled gene delivery to muscle. Pharm. Res. 13:1996;701-709.
47. R.J. Mumper, J. Wang, H. Nitta, K. Anwer, F. Tagliaferri, A.P. Rolland, Protective interactive non-condensing (PINC) polymers for enhanced plasmid distribution and expression in rat skeletal muscle, 1997, submitted to Gene Ther.
48. A.C. Guyton, Contraction of skeletal muscle, in: Textbook of Medical Physiology, W.B. Saunders, Philadelphia, 1976, pp. 130-147.
49. L. Stryer, Muscle contraction and cell motility, in: Biochemistry, W.H. Freeman, San Francisco, 1975, pp. 826-840.
50. D.R. Wilkie, Contractile and motile systems, in: A.L. Lehninger (Ed.), Biochemistry: The Molecular Basis of Cell Structure and Function, Worth Publishers, New York, 1970, pp. 583-604.
51. L.C. Junqueira, J. Carneiro, Muscle tissue, in: Basic Histology, 3rd edition, Lange Medical Publications, Los Altos, CA, 1980, p. 218.
52. R.J. Schwartz, F.J. DeMayo, B.W. O'Malley, Myogenic vector systems, United States Patent Number 5,298,422, March 29, 1994.
53. Seiler-Tuyns A., Eldridge J.D., Paterson B.M. Expression and regulation of chicken actin genes introduced into mouse myogenic and nonmyogenic cells. Proc. Natl. Acad. Sci. U.S.A. 81:1984;2980-2984.
54. MacLellan W.R., Lee T.C., Schwartz R.J., Schneider M.D. Transforming growth factor-β response elements of the skeletal α-actin gene. J. Biol. Chem. 269:1994;16754-16760.
55. Gunning P., Ponte P., Blau H., Kedes L. α-Skeletal and α-cardiac actin genes are coexpressed in adult human skeletal muscle and heart. Mol. Cell. Biol. 3:1983;1985-1995.
56. Muscat G.E., Kedes L. Multiple 5′ flanking regions of the human α-skeletal actin gene synergistically modulate muscle-specific expression. Mol. Cell. Biol. 7:1987;4089-4099.
57. Toyofuku T., Hoffman J.R., Zak R., Carlson B.M. Expression of α-cardiac and α-skeletal actin mRNAs in relation to innervation in regenerating and non-regenerating rat skeletal muscles. Dev. Dyn. 193:1992;332-339.
58. Cribbs L.L., Shimizu N., Yockey C.E., Levin L.E.et al. Muscle-specific regulation of a transfected rabbit myosin heavy chain β gene promoter. J. Biol. Chem. 264:1989;10672-10678.
59. Daubas P., Klarsfeld A., Garner L., Pinset C., Cox R., Buckingham M. Functional activity of the two promoters of the myosin alkali light chain gene in primary muscle cell cultures: comparison with other muscle gene promoters and other culture systems. Nucleic Acids Res. 16:1988;1251-1271.
60. Takeda S., North D.L., Lakich M.M., Russell S.D., Whalen R.G. A possible regulatory role for conserved promoter motifs in an adult-specific muscle myosin gene from mouse. J. Biol. Chem. 267:1992;16957-16967.
61. Steinbrecher R.A., Lewis E., Lee C.A., Goldspink G. Characterization of new promoter elements from myosin heavy chain gene isoforms. Muscle specific regulatory elements combined to a strong expression cassette for direct gene injection into muscle. J. Cell. Biochem. Suppl. 21A:1995;384.
62. Jaynes J.B., Chamberlain J.S., Buskin J.N., Johnson J.E., Hauschka S.D. Transcriptional regulation of the muscle creatine kinase gene and regulated expression in transfected mouse myoblasts. Mol. Cell. Biol. 6:1986;2855-2864.
63. Manthorpe M., Cornefert-Jensen F., Hartikka J.et al. Gene therapy by intramuscular injection of plasmid DNA: studies on firefly luciferase gene expression in mice. Hum. Gene Ther. 4:1993;419-431.
64. Parmacek M.S., Resai Bengur A., Vora A.J., Leiden J.M. The structure and regulation of expression of the murine fast skeletal troponin C gene. J. Biol. Chem. 165:1990;15970-15976.
65. Davis H.L., Whalen R.G., Demeneix B.A. Direct gene transfer into skeletal muscle in vivo: factors affecting efficiency of transfer and stability of expression. Hum. Gene Ther. 4:1993;151-159.
66. Wolff J.A., Williams P., Acsadi G., Jiao S., Jani A., Chong W. Conditions affecting direct gene transfer into rodent muscle in vivo. Biotechniques. 11:1991;474-485.
67. Wolff J.A., Dowty M.E., Jiao S., Repetto G.et al. Expression of naked plasmids by cultured mytotubes and entry of plasmids into T tubules and caveolae of mammalian skeletal muscle. J. Cell Sci. 103:1992;1249-1259.
68. Jiao S., Williams P., Berg R.K.et al. Direct gene transfer into nonhuman primate myofibers in vivo. Hum. Gene Ther. 3:1992;21-33.
69. Vitadello M., Schiaffino M.V., Picard A., Scarpa M., Schiaffino S. Gene transfer in regenerating muscle. Hum. Gene Ther. 5:1994;11-18.
70. Danko I., Fritz J.D., Jiao S., Hogan K., Latendresse J.S., Wolff J.A. Pharmacological enhancement of in vivo foreign gene expression in muscle. Gene Ther. 1:1994;114-121.
71. Davis H.L., Demeneix B.A., Quantin B., Coulombe J., Whalen R.G. Plasmid DNA is superior to viral vectors for direct gene transfer into adult mouse skeletal muscle. Hum. Gene Ther. 4:1993;733-740.
72. Wells D.J. Improved gene transfer by direct plasmid injection associated with regeneration in mouse skeletal muscle. FEBS. Lett. 332:1993;179-182.
73. M.E. Dowty, J.A. Wolff, Possible mechanisms of DNA uptake in skeletal muscle, in: J.A. Wolff (Ed.), Gene Therapeutics: Methods and Applications of Direct Gene Transfer, Birkhauser, Boston, 1994, pp. 82-98.
74. Wells D.J., Goldspink G. Age and sex influence expression of plasmid DNA directly injected into mouse skeletal muscle. FEBS. Lett. 306:1992;203-205.
75. Winegar R.A., Monforte J.A., Suing K.D., O'Loughlin K.G., Rudd C.J., Macgregor J.T. Determination of tissue distribution of an intramuscular plasmid vaccine using PCR and in situ DNA hybridization. Hum. Gene Ther. 7:1996;2185-2194.
76. Dowty M.E., Williams P., Zhang G., Hagstrom J.E., Wolff J.A. Plasmid DNA entry into postmitotic nuclei of primary rat myotubes. Proc. Natl. Acad. Sci. U.S.A. 92:1995;4572-4576.
77. Anderson R.G.W., Kamen B.A., Rothberg K.G., Lacey S.W. Potocytosis: sequestration and transport of small molecules by caveolae. Science. 255:1992;410-411.
78. Benoit P.W., Belt W.D. Destruction and regeneration of skeletal muscle after treatment with a local anaesthetic, bupivacaine (marcaine). J. Anat. 107:1970;547-556.
79. Hall-Craggs E.C.B. Early ultrastructural changes in skeletal muscle exposed to the local anaesthetic bupivacaine (marcaine). Br. J. Exp. Pathol. 61:1980;139-149.
80. Akiyama C., Kobayashi S., Nonaka I. Comparison of behavior in muscle fiber regeneration after bupivacaine hydrochloride- and acid anhydride-induced myonecrosis. Acta Neuropathol. 83:1992;584-589.
81. Carlson B.M., Shepard B., Komorowski T.E. A histological study of local anesthetic-induced muscle degeneration and regeneration in the monkey. J. Orthop. Res. 8:1990;485-494.
82. Grounds M.D. Towards understanding skeletal muscle regeneration. Pathol. Res. Pract. 187:1991;1-22.
83. Carlson B.M. Regeneration of entire skeletal muscle. Feder. Proc. 45:1988;1456-1460.
84. Ontell M. Morphological aspects of muscle fiber regeneration. Feder. Proc. 45:1985;1461-1465.
85. Engel A.G., Biesecker G. Complement activation in muscle fiber necrosis: demonstration of the membrane attack complex of complement in necrotic fibers. Ann. Neurol. 12:1982;289-296.
86. B. Synderman, B.C. Lane, Inflammation and chemotaxis, in: L.J. De Groot (Ed.), Endocrinology, 2nd edition, Part XII, 1989, pp. 2466-2479.
87. Naffakh N., Pinset C., Montarras D.et al. Long-term secretion of therapeutic proteins from genetically modified skeletal muscles. Hum. Gen. Ther. 7:1996;11-21.
88. M.A. Liu, M.R. Hilleman, R. Kurth (Eds.), DNA Vaccines: A new era in vaccinology, Ann. NY. Acad. Sci. New York, 1995, Vol. 772.
89. Kumar V., Sercarz E. Genetic vaccination: the advantages of going naked. Nat. Med. 2:1996;857-859.
90. Ulmer J.B., Sadoff J.C., Liu M.A. DNA vaccines. Curr. Opin. Immunol. 8:1996;531-536.
91. Donnelly J.J., Ulmer J.B., Liu M.A. Immunization with DNA. J. Immunol. Methods. 176:1994;145-152.
92. J.B. Ulmer, R.R. Deck, C.M. DeWitt, J.J. Donnelly, M.A. Liu, Antigen presentation by non-muscle cells for MHC class 1-restricted cytotoxic T lymphocytes following viral protein expression by muscle cells, 1996, Immunology, in press.
93. Corr M., Lee D.J., Carson D.A., Tighe H. Gene vaccination with naked plasmid DNA: mechanism of CTL priming. J. Exp. Med. 184:1996;1555-1560.
94. Doe B., Selby M., Barnett S., Baenziger J., Walker C.M. Induction of cytotoxic T lymphocytes by intramuscular immunization with plasmid DNA is facilitated by bone marrow-derived cells. Proc. Natl. Acad. Sci. U.S.A. 93:1996;8578-8583.
95. March K.L., Madison J.E., Trapnell B.C. Pharmacokinetics of adenoviral vector-mediated gene delivery to vascular smooth muscle cells: modulation by poloxamer 407 and implications for cardiovascular gene therapy. Hum. Gene Ther. 6:1995;41-53.
96. E. Mathiowitz, Y.S. Jong, K. Boekelheide, Polymeric gene delivery systems, WO 95/24929, September 21, 1995.
97. V. Buhler, Kollidon: Polyvinylpyrrolidone for the pharmaceutical industry, BASF Aktiengescellschaft Feinchemie, Ludwigshafen, 1993, pp 39-42.
98. Galaev Y., Garg N., Mattiasson B. Interaction of cibacron blue with polymers: implications for polymer-shielded dye-affinity chromatography of phosphofructokinase from baker's yeast. J. Chromatogr. A. 684:1994;45-54.
99. Tarantino R.et al. N-Methyl-2-pyrrolidone as a cosolvent: relationship of cosolvent effect with solute polarity and the presence of proton-donating groups on model drug compounds. J. Pharm. Sci. 83:1994;1213-1216.
100. Zia H., Ma J.K., O'Donnell J.P., Luzzi L.A. Cosolvency of dimethyl isosorbide for steroid solubility. Pharm. Res. 8:1991;502-504.
101. Kabanov A.V., Kabanov V.A. DNA complexes with polycations for the delivery of genetic material into cells. Bioconj. Chem. 6:1995;7-20.
102. Kabanov A.V., Astafyeva I.V., Chikindas M.L., Rosenblat G.F.et al. DNA interpolyelectrolyte complexes as a tool for efficient cell transformation. Biopolymers. 31:1991;1437-1443.
103. Yaroslavov A.A., Sukhishvili S.A., Obolsky O.L., Yaroslavova E.G., Kabanov A.V., Kabanov V.A. DNA affinity to biological membranes is enhanced due to complexation with hydrophobized polycation. FEBS Lett. 384:1996;177-180.
104. Ishii D.N., Recio-Pinto E., Spinelli W., Mill J.F., Sonnenfeld K.H. Neurite formation modulated by nerve growth factor, insulin, and tumor promoter receptors. Int. J. Neurosci. 26:1985;109-127.
105. Neff N.T., Prevette D., Houenou L.J., Lewis M.E.et al. Insulin-like growth factors: putative muscle-derived trophic agents that promote motoneuron survival. J. Neurobiol. 24:1993;1578-1588.
106. Sjoberg J., Kanje M. Insulin-like growth factor (IGF-1) as a stimulator of regeneration in the freeze-injured rat sciatic nerve. Brain Res. 485:1989;102-108.
107. Caroni P., Grandes P. Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J. Cell Biol. 110:1990;1307-1317.
108. Haida N., Fowler W.M., Abresch R.T.et al. Effect of hind-limb suspension on young and adult skeletal muscle. Exp. Neurol. 103:1989;68-76.