Alterations in insulin-like growth factor-1 gene and protein expression and type 1 insulin-like growth factor receptors in the brains of ageing rats

Neuroscience

Volumn 88, Issue 1, 1999, Pages 269-279

  Sonntag, W E ^a   Lynch, C D ^a   Bennett, S A ^a   Khan, A S ^a   Thornton, P L ^a   Cooney, P T ^a   Ingram, R L ^a   McShane, T ^a   Brunso Bechtold, J K ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Ageing; Cerebrovasculature; In situ hybridization; Insulin like growth factor 1; Messenger RNA; Type 1 insulin like growth factor receptors

Indexed keywords

SOMATOMEDIN C; SOMATOMEDIN RECEPTOR;

AGING; ANIMAL TISSUE; ARTICLE; BRAIN MATURATION; COGNITIVE DEFECT; GENE EXPRESSION; NERVE CELL DEGENERATION; NERVE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AGING; ANIMALS; ARTERIOLES; BRAIN; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR I; MALE; MICROCIRCULATION; PROTEIN BIOSYNTHESIS; RATS; RATS, INBRED BN; RATS, INBRED F344; RECEPTOR, IGF TYPE 1; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 0032889590     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00192-4     Document Type: Article

References (73)

1. Alavi A., Ferris S., Wolf A., Christman D., Fowler J., MacGregor R., Farkas T., Greenburg J., Dann R., and Reivich M. (1981) Determination of regional cerebral metabolism in dementia using F-18 deoxyglucose and positron emission tomography. In Cerebrovascular Disease 3. International Congress Series 532 (eds Meyer J. S., Lechner H., Reivich M., Ott E., Aranibar, E.), pp. 109-112. Excerpta Medica, Amsterdam.
2. Amano T., Meyer J. S., Okabe T., Shaw T., Mortel K. F. Stable xenon CT cerebral blood flow measurements computed by a single compartment-double integration model in normal ageing and dementia. J. Comput. assist. Tomogr. 6:1982;923-932.
3. Araujo D. M., Lapchak P. A., Collier B., Chabot J. G., Quirion R. Insulin-like growth factor-1 (somatomedin-C) receptors in the rat brain: distribution and interaction with the hippocampal colinergic system. Brain Res. 484:1989;130-138.
4. Beck K. D., Powell-Braxton L., Widner H. R., Walverde J., Hefti F. IGF-1 gene disruption results in reduced brain size, CNS hypomyelinizaton and loss of hippocampal granula and striatal parvalbumin-containing neurons. Neuron. 14:1995;717-730.
5. Bell M. A., Scarrow W. G. Staining for microvascular alkaline phosphatase in thick colloidin sections of nervus tissue: morphometric and pathological applications. Microvasc. Res. 27:1984;189-203.
6. Bennett S. A., Xu X., Lynch C., Sonntag W. E. Insulin-like growth factor-1 (IGF-1) regulates NMDAR1 in the hippocampus of aged animals. Soc. Neurosci. Abstr. 23(1):1997;349.
7. Black J. E., Polinsky M., Greenough W. T. Progressive failure of cerebral angiogenesis supporting neural plasticity in ageing rats. Neurobiol. Aging. 10(4):1989;353-358.
8. Bondy C. A. Transient IGF-1 gene expression during the maturation of functionally related central projection neurons. J. Neurosci. 11(11):1991;3442-3455.
9. Bondy C., Werner H., Roberts C. T. Jr., LeRoith D. Cellular pattern of type-1 insulin-like growth factor receptor gene expression during maturation of the rat brain: comparison with insulin-like growth factors I. Neuroscience. 46(4):1992;909-923.
10. Burton K. A., Kabigting E. B., Clifton D. K., Steiner R. N. Growth hormone receptor messenger ribonucleic acid distribution in the adult male rat brain and its colocalization in hypothalamic somatostatin neurons. Endocrinology. 131:1992;958-963.
11. Cheng B., Mattson M. P. IGF-1 and IGF-II protect cultured hippocampal and septal neurons against calcium-mediated hypoglycemic damage. J. Neurosci. 117(2):1992;114-123.
12. Cohick W. S., Clemmons D. R. The insulin-like growth factors. A. Rev. Physiol. 55:1993;131-153.
13. Cotman C. W., Kahle J. S., Korotzer A. R. (1995) Maintenance and regulation in brain of neurotransmission, trophic factors and immune responses. In Handbook of Physiology: Section 11 Aging (ed. Masoro E. J.), pp. 345-362. Oxford University Press, New York.
14. D'Costa A. P., Xu X., Ingram R. L., Sonntag W. E. Insulin-like growth factor (IGF)-1 stimulation of protein synthesis is attenuated in cortex of ageing rat brains. Neuroscience. 65:1995;805-813.
15. Delafontaine P., Lou H., Alexander R. W. Regulation of insulin-like growth factor I messenger RNA levels in vascular smooth muscle cells. Hypertension. 18:1991;742-747.
16. Delafontaine P. Insulin-like growth factor-1 and its binding proteins in the cardiovascular system. Cardiovasc. Res. 30:1995;825-834.
17. Englemann G. L., Boehm K. D., Haskell J. F., Khairallah P. A., Ilan J. Insulin-like growth factor and cardiomyocyte development: ventricular gene expression and membrane receptor variations I normotensive and hypertensive rats. Molec. cell. Endocr. 63:1989;1-14.
18. Garcia-Sigura L. M., Perez J., Pons S., Rejas M. T., Torres-Aleman I. Localization of insulin-like growth factor (IGF-1)-like immunoreactivity in the developing rat and adult rat brain. Brain Res. 560:1991;167-174.
19. Goldman H., Berman R. F., Gershon S., Murphy S. L., Altman H. J. Correlation of behavioral and cerebrovascular functions in the ageing rat. Neurobiol. Aging. 8:1987;409-416.
20. Han V. K., Lauder J. M., D'Ercole A. J. Rat astroglial somatomedian/insulin-like growth factor binding proteins: characterization and evidence of biological function. J. Neurosci. 8:1988;3135-3143.
21. Hansson H. A., Dahlin L. B., Danielsen N., Fryklund L., Nachemson A. K., Polleryd P., Rozell B., Skottner A., Stemme S., Lundborg G. Evidence indicating trophic importance of IGF-1 in regenerating peripheral nerves. Acta physiol. scand. 126(4):1986;609-614.
22. Hansson H. A., Jennische E., Skottner A. Regenerating endothelial cells express insulin-like growth factor immunoreactivity after arterial injury. Cell Tiss. Res. 250(3):1987;499-505.
23. Hansson H. A., Brandsten C., Lossing C., Petruson K. Transient expression of insulin-like growth factor I immunoreactivity by vascular cells during angiogenesis. Expl molec. Path. 50:1989;125-138.
24. Haug H., Eggers R. Morphometry of the human cortex cerebri and corpus striatum during ageing. Neurobiol. Aging. 12:1991;336-338.
25. Hepler J. E. and Lund P. K. (1990) Molecular biology of the insulin-like growth factors. Relevance to nervous system function. In Molecular Neurobiology (ed. Bazan N.), pp. 93-125. Humana, Totowa, NJ.
26. Hughes C. C., Lantos P. L. A morphometric study of blood vessel, neuron and glial cell distribution in young and old rat brain. J. neurol. Sci. 79:1987;101-110.
27. Hynes M. A., Van Wyk J., Brooks P. J., D'Ercole A. J., Jansen M., Lund P. K. Growth hormone dependence of somatomedin-C/insulin-like growth factor-1 and insulin-like growth factor-II messenger ribonucleic acids. Molec. Endocr. 1(13):1987;233-242.
28. Ingram D. K., Spangler E. L., Iijima S., Ikari H., Kuo H., Greig N. H. Rodent models of memory dysfunction in Alzheimer's disease and normal ageing: moving beyond the colinergic hypothesis. Life Sci. 55(25)(26):1994;2037-2049.
29. Ishii D. N. Relationship of insulin-like growth factor II gene expression in muscle to synaptogenesis. Proc. natn. Acad. Sci. U.S.A. 86:1989;2898-2902.
30. Johansson J. C., Larson G., Andersson M., Elmgren A., Hynsjo L., Lindahl A., Lundbergh P. A., Isaksson O. G., Lindstedt S., Bengtsson B. A. Treatment of growth hormone deficient adults with recombinant human growth hormone increases the concentration of growth hormone in the cerebrospinal fluid and affects neurotransmitters. Neuroendocrinology. 61:1993;57-66.
31. Kanje M., Skottner A., Sjoberg J., Lundborg G. Insulin-like growth factor 1 stimulates regeneration of the rat sciatic nerve. Brain Res. 486:1989;396-398.
32. Kety S. S. Human cerebral blood flow and oxygen consumption as related to ageing. J. Chronic Dis. 8:1956;478-486.
33. Landfield P. W., Baskin R. K., Pitler T. A. Brain ageing correlates: retardation by hormonal-pharmacological treatments. Science. 214:1981;581-584.
34. Lee W. H., Michels K. M., Bondy C. A. Localization of insulin-like growth factor binding protein-2 messenger RNA during postnatal brain development: correlation with insulin-like growth factors I and II. Neuroscience. 53(1):1993;251-265.
35. Lefevre M., Rucker R. B. Aorta elastin turnover in normal and hypercholesterolemic Japanese quail. Biochim. biophys. Acta. 630:1980;519-529.
36. Lenoir D., Honnegar P. Insulin-like growth factor 1 (IGF-1) stimulates DNA synthesis in fetal rat brain cell cultures. Brain Res. 283:1983;205-213.
37. Lopez-Fernandez J., Sanchez-Franco F., Velasco B., Tolon R. M., Pazos F., Cacicedo L. Growth hormone induces somatostatin and insulin-like growth factor 1 gene expression in the cerebral hemispheres of ageing rats. Endocrinology. 137(10):1996;4384-4391.
38. Lowe W. L. Jr., Lasky S. R., LeRoith D., Roberts C. T. Jr. Distribution and regulation of rat insulin-like growth factor I messenger ribonucleic acids encoding alternative carboxyterminal E-peptides: evidence for differential processing and regulation in liver. Molec. Endocr. 2(6):1988;528-535.
39. Lucidi-Phillipi C. A., Gage F. H. The neurotrophic hypothesis and the cholinergic basal forebrain projection. Prog. Brain Res. 98:1993;241-249.
40. Lund P. K., Moat-Staats B. M., Hynes M. A., Simmons J. G., Jansen M., D'Ercole A. J., Van Wyk J. J. Somatomedin-C/insulin-like growth factor-1 and insulin-like growth factor II mRNAs in rat fetal and adult tissues. J. biol. Chem. 261:1986;14539-14544.
41. Malamed E., Levy S., Bentin S., Cooper G., Rinot Y. Reduction in regional cerebral blood flow during normal ageing in man. Stroke. 11:1980;31-35.
42. Mathews L. S., Enberg B., Norstedt G. Regulation of rat growth hormone receptor gene expression. J. biol. Chem. 264:1989;9905-9910.
43. McMorris F. A., Smith T. M., DeSalvo S., Furlanetto R. W. Insulin-like growth factor 1/somatomedin-C: a potent inducer of oligodendrocyte development. Proc. natn. Acad. Sci. U.S.A. 83:1986;822-826.
44. McMorris F. A., Dubois-Dalcq M. Insulin-like growth factor 1 promotes cell proliferation and oligodendroglial commitment in rat glial progenitor cells developing in vitro. J. Neurosci. Res. 21:1988;199-209.
45. Mooney M., Sonntag W. E., Barra M., Xu X., Bennett S., Ingram R., Poe B., Markowska A. L. Insulin-like growth factor-1 (IGF-1) increases working memory in aged animals. Soc. Neurosci. Abstr. 22(2):1996;1237.
46. Morgan D. and May P. C. (1990) Age related changes in synaptic neurochemistry, In Handbook of the Biology of Ageing (eds Schneider E. L. and Rowe J. W.), 3rd edn, pp. 219-234. Academic, London.
47. Nachemson A. K., Lundborg G., Hansson H. A. Insulin-like growth factor 1 promotes nerve regeneration: an experimental study on rat sciatic nerve. Growth Factors. 3(4):1990;309-314.
48. Niblock M. M., Lynch C. D., Cooney P. T., McShane T., Brunso-Bechtold J. K., Sonntag W. E. Neuronal IGF-1 mRNA expression during development and ageing in Fischer 344XBrown-Norway rats. Soc. Neurosci. Abstr. 22(2):1996;1236.
49. Nilsson L., Sara V. R., Nordberg A. Insulin-like growth factor 1 stimulates the release of acetylcholine from rat cortical slices. Neurosci. Lett. 88:1988;221-226.
50. Paxinos G. and Watson C. (1982) The Rat Brain in Stereotaxic Coordinates. Academic, New York.
51. Pepeu G., Casamenti F., Pepeu I. M., Scali C. The brain cholinergic system in ageing mammals. J. Reprod. Fertil. 46(Supp.):1993;155-162.
52. Recio-Pinto E., Lang F. F., Ishii D. N. Insulin and insulin-like growth factor II permit nerve growth factor binding and the neurite formation response in cultured human neuroblastoma cells. Proc. natn. Acad. Sci. U.S.A. 81:1984;2563-2566.
53. Recio-Pinto E., Rechler M. M., Ishii D. N. Effects of insulin, insulin-like growth factor II and nerve growth factor on neurite formation and survival in cultured sympathetic and sensory neurons. J. Neurosci. 6:1986;1211-1219.
54. Recio-Pinto E., Ishii D. N. Effects of insulin, insulin-like growth factor-II and nerve growth factor on neurite outgrowth in cultured human neuroblastoma cells. Brain Res. 302:1990;323-334.
55. Reinhardt R. R., Bondy C. Insulin-like growth factors cross the blood-brain barrier. Endocrinology. 135:1995;1753-1761.
56. Roth G. S., Joseph J. A., Mason R. P. Membrane alterations as causes of impaired signal tranduction in Alzheimer's disease and ageing. Trends Neurosci. 18(11):1995;483-483.
57. Rymaszewski Z., Cohen R. M., Chomczynski P. Human growth hormone stimulates proliferation of human retinal microvascular endothelial cells in vitro. Proc. natn. Acad. Sci. U.S.A. 88:1991;617-621.
58. Saneto R. P., Low K. G., Melner M. H., de Villis J. Insulin/insulin-like growth factor 1 and other epigenetic modulators of myelin basic protein expression in isolated oligodendrocyte progenitor cells. J. Neurosci. Res. 21:1988;210-219.
59. Shaw T. G., Mortel K. F., Meyer J. S., Rogers R. L., Hardenberg J., Cutaia M. M. Cerebral blood flow changes in benign ageing and cerebrovascular disease. Neurology. 34:1984;855-862.
60. Shermer J., Raizada M. K., Masters B. A., Ota A., LeRoith D. Insulin-like growth factor I receptor in neural and glial cells. Characterization and biological effects in primary culture. J. biol. Chem. 262:1987;7693-7697.
61. Shinar Y., McMorris F. A. Developing oligodendroglia express mRNA for insulin-like growth factor-1, a regulator of oligodendrocyte development. J. neurol. Res. 42(4):1995;516-527.
62. Simard M., Manthos H., Giaid A., Lebefvre Y., Goodyer C. G. Ontogeny of growth hormone receptors in human tissues: an immunohistochemical study. J. clin. Endocr. Metab. 81(8):1996;3097-3102.
63. Sonntag W. E., Steger R. W., Forman L. J., Meites J. Decreased pulsatile release of growth hormone in old male rats. Endocrinology. 107:1980;1875-1879.
64. Sonntag W. E., Boyd R. L. Chronic ethanol feeding inhibits plasma levels of insulin-like growth factor-1. Life Sci. 43:1988;1325-1330.
65. Sonntag W. E., Lynch C. D., Cooney P. T., Hutchins P. M. Decreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor-1. Endocrinology. 138(8):1997;3515-3520.
66. Swaab D. F. Brain ageing and Alzheimer's disease, "Wear and Tear" versus "Use it or Lose It" Neurobiol. Aging. 12:1991;317-324.
67. Terry R. D. Some biological aspects of the aging brain. Mechs Aging Dev. 14:1980;191-201.
68. Torran-Allerand C. D., Ellis L., Pfenninger K. H. Estrogen and insulin synergism in neurite growth enhancement in vitro: mediation of steroid effects by interactions with growth factor 1. Devl Brain Res. 41:1988;87-100.
69. Torres-Alleman I., Naftolin F., Robbins R. J. Growth promoting effects of IGF-1 on fetal hypothalamic cell lines under serum-free culture conditions. Int. J. dev. Neurosci. 7:1989;195-202.
70. Van der Pal R., Koper J. W., van Golde L. M., Lopes-Cadozo M. Effects of insulin and insulin-like growth factor (IGF-1) on oligodendrocyte-enriched glial cultures. J. Neurosci. Res. 19:1989;483-490.
71. Werther G. A., Abate M., Hogg A., Chessman H., Oldfield B., Hards D., Hudson P., Power B., Freed K., Herington A. C. Localization of insulin-like growth factor 1 mRNA in rat brain by in situ hybridization - relationship to IGF-1 receptors. Molec. Endocr. 4:1990;773-778.
72. Yamaguchi F., Itano T., Mizobuchi M., Miyamoto O., Janjua N. A., Matsui H., Tokuda M., Ohmoto T., Hosokawa K., Hatase O. Insulin-like growth factor 1 (IGF-1) distribution in the tissue and extracellular compartment in different regions of the brain. Brain Res. 533:1990;344-347.
73. Xu X., Sonntag W. E. Growth hormone and ageing: regulation, signal transduction and replacement therapy. Trends Endocr. Metab. 7:1996;145-150.