Decreased skin sensory innervation in transgenic mice overexpressing insulin-like growth factor-II

Neuroscience

Volumn 79, Issue 3, 1997, Pages 789-797

  Reynolds, M L ^a   Ward, A ^b   Graham, C F ^b   Coggeshall, R ^c   Fitzgerald, M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Cutaneous nerve; Dorsal root ganglia; Nerve growth factor; Neurotrophin; Sensory neuron; Skin innervation

Indexed keywords

NERVE GROWTH FACTOR; NEUROTROPHIN; SOMATOMEDIN B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SKIN NERVE; SPINAL GANGLION; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR II; MICE; MICE, TRANSGENIC; NEURONS, AFFERENT; SKIN;

EID: 0030765436     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00043-2     Document Type: Article

References (57)

1. Albers K. M., Wright D. E., Davis B. M. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 14:1994;1422-1432.
2. Barde Y.-A. Trophic factors and neuronal survival. Neuron. 2:1989;1525-1534.
3. Bondy C. A., Werner H., Roberts C. T. Jr., LeRoith D. Cellular pattern of insulin-lke growth factor-I (IGF-I) and type I IGF receptor gene expression in early organogenesis: comparison with IGFII gene expression. Molec. Endocr. 4:1990;1386-1398.
4. 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.
5. Coggeshall R. E., Pover C. M., Fitzgerald M. Dorsal root ganglion cell death and surviving cell numbers in relation to the development of sensory innervation in the rat hindlimb. Devl Brain Res. 82:1994;193-212.
6. Coggeshall R. E. A consideration of neural counting methods. Trends Neurosci. 15:1992;9-13.
7. Crowley C., Spencer S. D., Nishimura M. C., Chen K. S., Pitts M. S., Armanini M. P., Ling L. H., McMahon S. B., Shelton D. L., Levinson A. D., Phillips H. S. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell. 76:1994;1001-1011.
8. Da Costa T. H. M., Williamson D. H., Ward A., Bates P., Fisher R., Richardson L., Hill D. J., Robinson I. C. A. F., Graham C. F. High plasma insulin-like growth factor-II and low lipid content in transgenic mice: measurements of lipid metabolism. J. Endocr. 143:1994;433-439.
9. Daughaday W. H., Rotwein P. Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, scrum and tissue concentrations. Endocrine Rev. 10:1989;68-91.
10. Davies A. M. (1992) Cell death and the trophic requirements of developing sensory neurons. In Sensory Neurons (ed Scott S.A.), pp. 194-214, Oxford University Press, New York.
11. Davies A. M. The neurotrophic hypothesis: where does it stand? Phil. Trans. R. Soc. 351:1996;389-394.
12. Davies A. M., Bandtlow C., Heumann R., Korsching S., Rohrer H., Thoenen H. Timing and site of nerve growth factor synthesis in the developing skin in relation to innervation and expression of the receptor. Nature. 326:1987;353-358.
13. D'Ercole A. J., Dai Z., Xing Y., Boney C., Wilkie M. B., Lauder J. M., Han V. K., Clemmons D. R. Brain growth retardation due to the expression of human insulin like growth factor binding protein-1 in transgenic mice: an in vivo model for the analysis of IGF function in the brain. Devl. Brain Res. 82:1994;213-222.
14. Detwiler S. R. On the hyperplasia of nerve centers resulting from excessive peripheral loading. Proc. natn. Acad. Sci. U.S.A. 6:1920;96-101.
15. Diamond J., Gloster A., Kitchener P. (1992) Regulation of the sensory innervation of skin: trophic control of collateral sprouting. In Sensory Neurons (ed. Scott S.A.), pp. 309-322. Oxford University Press, New York.
16. Elkabes S., Dreyfus C. F., Schaar D. G., Black I. B. Embryonic sensory development: local expression of neurotrophin-3 and target expression of nerve growth factor. J. comp. Neurol. 341:1994;204-213.
17. Ernfors P., Persson H. Developmentally regulated expression of HDNF/NT-3 mRNA in rat spinal cord motoneurons and expression of BDNF mRNA in embryonic dorsal root ganglion. Eur. J. Neurosci. 3:1991;953-961.
18. Eustache I., Seyfritz N., Gueritaud J. P. Effects of insulin-like growth factors on organotypic cocultures of embryonic rat brainstem slices and skeletal muscle fibres. Devl Brain Res. 81:1994;284-292.
19. Fitzgerald M. J. T. Perinatal changes in the epidermal innervation in the rat and mouse. J. comp. Neurol. 126:1966;37-42.
20. Gaese F., Kolbeck R., Barde Y.-A. Sensory ganglia require neurotrophin-3 early in development. Development. 120:1994;1613-1619.
21. Gavrilovic J., Brennan A., Mirsky R., Jessen K. R. Fibroblast growth factors and insulin growth factors combine to promote survival of rat Schwann cell precursors without induction of DNA synthesis. Eur. J. Neurosci. 7:1995;77-85.
22. Glazner G. W., Lupien S., Miller J. A., Ishii D. N. Insulin-like growth factor-II increases the rate of sciatic nerve regeneration in rats. Neuroscience. 54:1983;791-797.
23. Hamburger V. The effects of wing bud extirpation on the development of the central nervous system in chick embryos. J. exp. Zool. 68:1934;449-494.
24. Hamburger V. Motor and sensory hyperplasia following limb bud transplantations in chick embryos. Physiol. Zool. 12:1939;268-284.
25. Hamburger V., Yip J. W. Reduction of experimentally induced neuronal death in spinal ganglia of the chick embryo by nerve growth factor. J. Neurosci. 4:1984;767-774.
26. Harper S., Davies A. M. NGFmRNA expression in developing cutaneous epithelium related to innervation density. Development. 110:1990;515-519.
27. Jessen K. R., Brennan A., Morgan L., Mirsky R., Kent A., Hashimoto Y., Gavrilovic J. The Schwann cell precursor and its fate: a study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron. 12:1994;509-527.
28. Ishii D. N. Effect of tumor promoters on the response of cultured embryonic chick ganglia to nerve growth factor. Cancer Res. 38:1978;3886-3893.
29. Ishii D. N. (1993) Neurobiology of insulin and insulin-like growth factors. In Neurotrophic Factors (eds Loughlin S.E. and Fallon J.H.), pp. 415-442. Academic Press, San Diego.
30. Ishii D. N. Implication of insulin-like growth factors in the pathogenesis of diabetic neuropathy. Brain Res. Rev. 20:1995;47-67.
31. Ishii D. N., Lupien S. B. Insulin-like growth factors protect against diabetic neuropathy: effects on sensory nerve regeneration in rats. J. Neurosci. Res. 40:1995;138-144.
32. Kinnman E., Aldskogius H. Collateral sprouting of sensory axons in the glabrous skin of the hindpaw after chronic sciatic nerve lesion in adult and neonatal rats: a morphological study. Brain Res. 377:1986;73-82.
33. Konishi Y., Takahashi K., Chui D. H., Rosenfeld R. G., Himeno M., Tabira T. Insulin-like growth factor II promotes in vitro cholinergic development of mouse septal neurons: comparison with the effects of insulin-like growth factor I. Brain Res. 649:1994;53-61.
34. LeRoith D., Lowe W. L. Jr., Shemer J. Development of brain insulin receptors. Int. J. Biochem. 20:1988;225-230.
35. LeRoith D., Werner H., Faria T. N., Kato H., Adamo M., Roberts C. T. Jr. Insulin-like growth factor receptors. Implications for nervous system function. Ann. N. Y. Acad. Sci. 692:1993;22-32.
36. Maisonpierre P., Belluscio L., Squinto S., Ip N. Y., Furth M. E., Lindsay R. M., Yancopoulos G. D. NT-3, BDNF and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron. 5:1990;501-509.
37. Ocrant I., Fay C. T., Parmalee J. T. Characterization of insulin-like growth factor binding proteins produced in the rat central nervous system. Endocrinology. 127:1990;1260-1267.
38. Okamoto T., Katada T., Murayama Y., Ui M., Ogata E., Nishimoto I. A simple structure encodes G protein activating function of the IGFII/mannose-6-phosphate receptor. Cell. 62:1990;709-717.
39. Prestige M. C. The control of cell number in the lumbar spinal ganglia during the development of Xenopus laevis tadpoles. J. Embryol. exp. Morph. 17:1967;453-471.
40. Recio-Pinto E., Ishii D. N. Effects of insulin, insulin growth factor II and nerve growth factor on neurite formation and survival in cultured human neuroblastoma cells. Brain Res. 302:1984;323-334.
41. Recio-Pinto E., Rechler M. M., Ishii D. N. Effects of insulin, insulin-like growth factor H and nerve growth factor on neurite formation and survival in cultured sympathetic and sensory neurons. J. Neurosci. 6:1986;1211-1219.
42. Reynolds M. L., Fitzgerald M., Benowitz L. I. GAP-43 expression in developing cutaneous and muscle nerves in the rat hindlimb. Neuroscience. 41:1991;201-211.
43. Rottwein P., Burgess S. K., Milbrandt J. D., Krause J. E. Differential expression of insulin-like growth factor genes in rat central nervous system. Proc. natn. Acad. Sci. U.S.A. 85:1988;265-269.
44. Ruit K. G., Elliott J. L., Osborne P. A., Yan Q., Snider W. D. Selective dependence of mammalian dorsal root ganglion neurons on nerve growth factor during embryonic development. Neuron. 8:1992;573-587.
45. Schechterson L. C., Bothwell M. Novel roles for neurotrophins are suggested by BDNF and NT3 mRNA expression in developing neurons. Neuron. 9:1992;449-463.
46. Scott S. A. The development of the segmental pattern of skin sensory innervation in embryonic chick hindlimb. J. Physiol. 330:1982;203-220.
47. Shorey M. L. The effect of the destruction of peripheral areas on the differentiation of the neuroblasts. J. exp. Zool. 7:1909;25-63.
48. Sklar M. M., Kiess C. L., Thomas C. L., Nissley S. P. Developmental expression of the tissue insulin like growth factor H/mannose 6-phosphate in the rat. Measurement by quantitative immunoblotting. J. biol. Chem. 264:1989;16733-16740.
49. Smeyne R. J., Klein R., Scnapp A., Long L. K., Bryant S., Lewin A., Lira S. A., Barbacid M. Severe sensory and sympathetic neuropathies in mice carrying a disrupted TRK/NGF receptor gene. Nature. 368:1994;246-249.
50. Snider V. Y. D., Silos-Santiago I. Dorsal root ganglion cells require functional neurotrophin receptors for survival during development. Phil. Trans. R. Soc. 351:1996;395-403.
51. Valentino K. L., Ocrant I., Rosenfeld R. G. Developmental expression of insulin-like growth factor-II receptor immunoreactivity in the rat central nervous system. Endocrinology. 126:1990;914-920.
52. Voyvodic J. T. Peripheral target regulation of dendritic geometry in the rat superior cervical ganglion. J. Neurosci. 9:1987;1997-2010.
53. Ward A., Bates P., Fisher R., Richardson L., Graham C. Disproportionate growth in mice with Igf2 transgenes. Proc. natn. Acad. Sci. U.S.A. 91:1994;10365-10369.
54. Weskamp G., Otten U. An enzyme-linked immunoassay for nerve growth factor (NGF): a tool for studying regulatory mechanisms involved in NGF production in brain and in peripheral tissues. J. Neurochem. 48:1987;1779-1786.
55. White F. A., Silos-Santiago I., Molliver D. C., Harding J. C., Saxena M. T., Barbacid M., Snider W. D. Lumbar DRGs of trkA(-/-) mice exhibit massive apoptosis prior to innervation of distal hindlimb targets. Soc. Neurosci. Abstr. 21:1995;1539.
56. Wolf E., Kramer R., Blum W. F., Foll J., Brem G. Consequences of postnatally elevated insulin-like growth factor-II in transgenic mice: endocrine changes and effects on body and organ growth. Endocrinology. 135:1994;1877-1886.
57. Zackenfels K., Oppenheim R. W., Rohrer H. Evidence for an important role of IGF-I and IGF-II for the early development of chick sympathetic neurons. Neuron. 14:1995;731-741.