Insulin-like growth factor (IGF) gene expression is reduced in neural tissues and liver from rats with non-insulin-dependent diabetes mellitus, and IGF treatment ameliorates diabetic neuropathy

Journal of Pharmacology and Experimental Therapeutics

Volumn 283, Issue 1, 1997, Pages 366-374

  Zhuang, Hui Xin ^a   Wuarin, Laura ^a   Fei, Zhi Jian ^a   Ishii, Douglas N ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NEUROTROPHIC FACTOR; RECOMBINANT SOMATOMEDIN B; SOMATOMEDIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; COMPLICATION; CONTROLLED STUDY; DIABETIC NEUROPATHY; DRUG THERAPY; GENE EXPRESSION; HYPERALGESIA; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; LIVER; MALE; NERVE REGENERATION; NERVOUS TISSUE; NEUROLOGIC DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SPINAL CORD; SUBCUTANEOUS DRUG ADMINISTRATION;

ANIMALS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC NEUROPATHIES; GENE EXPRESSION REGULATION; HYPERGLYCEMIA; INSULIN-LIKE GROWTH FACTOR II; LIVER; MALE; NERVOUS SYSTEM; OBESITY; RATS; RATS, SPRAGUE-DAWLEY; RATS, ZUCKER; RNA, MESSENGER; SOMATOMEDINS;

EID: 0030803172     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (83)

1. ARAKI, Y., NOMURA, M., TANAKA, H., YAMAMOTO, H., YAMAMOTO, T., TSUKAGUCHI, I. AND NAKAMURA, H.: MRI of the brain in diabetes mellitus. Neuroradiology 36: 101-103, 1994.
2. ARCHER, A. G., WATKINS, P. J., THOMAS, P. K., SHARMA, A. K. AND PAYAN, J.: The natural history of acute painful neuropathy in diabetes mellitus. J. Neurol. Neurosurg. Psychiatry 46: 491-499, 1983.
3. BAXTER, R. C., BROWN, A. S. AND TURTLE, J. R.: Decrease in serum receptor-reactive somatomedin in diabetes. Horm. Metab. Res. 11: 216-220, 1979.
4. BODKIN, N. L., SPORTSMAN, R., DIMARCHI, R. D. AND HANSEN, B. C.: Insulin-like growth factor-I in non-insulin-dependent diabetic monkeys: Basal plasma concentrations and metabolic effects of exogenously administered biosynthetic hormone. Metabolism 40: 1131-1137, 1991.
5. BONI-SCHNETZLER, M., BINZ, K., MARY, J. L., SCHMID, C., SCHWANDER, J. AND FROESCH, E. R.: Regulation of hepatic expression of IGF-I and fetal IGF binding protein mRNA in streptozotocin diabetes. FEBS Lett. 251: 253-256, 1989.
6. BORNFELDT, K. E., ARNQVIST, H. J., ENBERG, B., MATHEWS, L. S. AND NORSTEDT, G.: Regulation of insulin-like growth factor-I and growth hormone receptor gene expression by diabetes and nutritional state in rat tissues. J. Endocrinol. 122: 651-656, 1989.
7. BROWN, A. L., GRAHAM, D. E., NISSLEY, S. P., HILL, D. J., STRAIN, A. J. AND RECHLER, M. M.: Developmental regulation of insulin-like growth factor II mRNA in different rat tissues. J. Biol. Chem. 261: 13144-13150, 1986.
8. CARLSSON-SKWIRUT, C., LAKE, M., HARTMANIS, M., HALL, K. AND SARA, V. R.: A comparison of the biological activity of the recombinant intact and truncated insulin-like growth factor I. Biochim. Biophys. Acta 1011: 192-197, 1989.
9. CARONI, P. AND GRANDES, P.: Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J. Cell Biol. 110: 1307-1317, 1990.
10. CHOMCZYNSKI, P. AND SACCHI, N.: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159, 1987.
11. CORNBLATH, D. R., DELLON, A. L. AND MACKINNON, S. E.: Spontaneous diabetes mellitus in a rhesus monkey: Neurophysiological studies. Muscle Nerve 12: 233-235, 1989.
12. COURTEIX, C., ESCHALIER, A. AND LAVARENNE, J.: Streptozocin-induced diabetic rats: Behavioural evidence for a model of chronic pain. Pain 53: 81-88, 1993.
13. DECHIARA, T. M., ROBERTSON, E. J. AND EFSTRATIADIS, A.: Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64: 849-859, 1991.
14. DYCK, P. J., THOMAS, P. K., ASBURY, A. K., WINEGRAD, A. I. AND PORTE, D., JR.: Diabetic Neuropathy, W. B. Saunders, Philadelphia, 1987.
15. EKSTROM, P. A. R. AND TOMLINSON, D. R.: Impaired nerve regeneration in streptozotocin-diabetic rats: Effects of treatment with an aldose reductase inhibitor. J. Neurol. Sci. 93: 231-237, 1989.
16. FAGIN, J. A., ROBERTS, C. T., JR., LEROITH, D. AND BROWN, A. T.: Coordinate decrease of tissue insulin-like growth factor I post-transcriptional alternative mRNA transcripts in diabetes mellitus. Diabetes 38: 428-434, 1989.
17. GLAZNER, G. W. AND ISHII, D. N.: Insulin-like growth factor gene expression in rat muscle during reinnervation. Muscle Nerve 18: 1433-1442, 1995.
18. GLAZNER, G. W., LUPIEN, S., MILLER, J. A. AND ISHII, D. N.: Insulin-like growth factor-II increases the rate of sciatic nerve regeneration in rats. Neuroscience 54: 791-797, 1993.
19. GLAZNER, G. W., MORRISON, A. E. AND ISHII, D. N.: Elevated insulin-like growth factor (IGF) gene expression in sciatic nerves during IGF-supported nerve regeneration. Mol. Brain Res. 25: 265-272, 1994.
20. GREENE, D. A.: Glycemic control. In Diabetic Neuropathy, ed. by P. J. Dyck, P. K. Thomas, A. K. Asbury, A. I. Winegrad and D. Porte, Jr., pp. 177-187, W. B. Saunders, Philadelphia, 1987.
21. HALL, K. AND SARA, V. R.: Somatomedin levels in childhood, adolescence and adult life. Clin. Endocrinol. Metab. 13: 91-112, 1984.
22. HARLEY, C. B.: Hybridization of oligo(dT) to RNA on nitrocellulose. Gene Anal. Tech. 4: 17-22, 1987.
23. HARRISON, H. E. AND ROBINSON, T. E.: Impaired growth hormone secretion in streptozotocin diabetic rats. Horm. Metab. Res. 12: 556-557, 1980.
24. HU, J.-F., VU, T. H. AND HOFFMAN, A. R.: Different biallelic activation of three insulin-like growth factor II promoters in the mouse central nervous system. Mol. Endocrinol. 9: 628-636, 1995.
25. HYNES, M. A., BROOKS, P. J., VAN WYK, J. J. AND LUND, P. K.: Insulin-like growth factor II messenger ribonucleic acids are synthesized in the choroid plexus of the rat brain. Mol. Endocrinol. 2: 47-54, 1988.
26. HYNES, M. A., VAN WYK, J. J., BROOKS, P. J., D'ERCOLE, A. J., JANSEN, M. AND LUND, P. K.: Growth hormone dependence of somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II messenger ribonucleic acids. Mol. Endocrinol. 1: 233-242, 1987.
27. ICHIMIYA, Y., EMSON, P. C., NORTHROP, A. J. AND GILMOUR, R. S.: Insulin-like growth factor II in the rat choroid plexus. Mol. Brain Res. 4: 167-170, 1988.
28. ISHII, D. N.: Neurobiology of insulin and insulin-like growth factors. In Neurotrophic Factors, ed. by S. E. Loughlin and J. H. Fallon, pp. 415-442, Academic Press, New York, 1993.
29. ISHII, D. N.: Implication of insulin-like growth factors in the pathogenesis of diabetic neuropathy. Brain Res. Rev. 20: 47-67, 1995.
30. ISHII, D. N., GUERTIN, D. M. AND WHALEN, L. R.: Reduced insulin-like growth factor I mRNA content in liver, adrenal glands and spinal cord of diabetic rats. Diabetologia 37: 1073-1081, 1994.
31. ISHII, D. N. AND LUPIEN, S. B.: Insulin-like growth factors protect against diabetic neuropathy: effects on sensory nerve regeneration in rats. J. Neurosci. Res. 40: 138-144, 1995.
32. JACOBS, J. M.: Penetration of systemically injected horseradish peroxidase into ganglia and nerves of the autonomic nervous system. J. Neurocytol. 6: 607-612, 1977.
33. JACOBS, J. M., MACFABLANE, R. M. AND CAVANAGH, J. B.: Vascular leakage in the dorsal root ganglia of the rat studied with horseradish peroxidase. J. Neurol. Sci. 29: 95-107, 1976.
34. JAKOBSEN, J., SIDENIUS, P., GUNDERSEN, H. J. G. AND OSTERBY, R.: Quantitative changes of cerebral neocortical structure in insulin-treated long-term streptozotocin-diabetic rats. Diabetes 36: 597-606, 1987.
35. KAFATOS, F., JONES, C. W. AND EFSTRATIADIS, A.: Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res. 7: 1541-1553, 1979.
36. LEHRACH, H., DIAMOND, D., WOZNEY, J. M. AND BOEDTKER, H.: Ribonucleic acid molecular weight determination by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry 16: 4743-4751, 1977.
37. LOGAN, A., GONZALEZ, A.-M., HILL, D. J., BERRY, M., GREGSON, N. A. AND BAIRD, A.: Coordinated pattern of expression and localization of insulin-like growth factor-II (IGF-II) and IGF-binding protein-2 in the adult rat brain. Endocrinology 135: 2255-2264, 1994.
38. LONGO, F. M., POWELL, H. C., LEBEAU, J., GERRERO, M. R., HECKMAN, H. AND MYERS, R. R.: Delayed nerve regeneration in streptozotocin diabetic rats. Muscle Nerve 9: 385-393, 1986.
39. LUSTMAN, P. J., GRIFFITH, L. S. AND CLOUSE, R. E.: Depression in adults with diabetes. Results of 5-yr follow-up study. Diabetes Care 11: 605-612, 1988.
40. MATHEWS, L. S., HAMMER, R. E., BEHRINGER, R. R., D'ERCOLE, A. J., BELL, G. I., BRINSTER, R. L. AND PALMITER, R. D.: Growth enhancement of transgenic mice expressing human insulin-like growth factor I. Endocrinology 123: 2827-2833, 1988.
41. MIGDALIS, I. N., KALOGEROPOULOU, K., KALALANTZIS, L., NOUNOPOULOS, C., BOULOUKOS, A. AND SAMARTZIS, M.: Insulin-like growth factor-I and IGF-I receptors in diabetic patients with neuropathy. Diabetic Med. 12: 823-827, 1995.
42. MILL, J. F., CHAO, M. V. AND ISHII, D. N.: Insulin, insulin-like growth factor II, and nerve growth factor effects on tubulin mRNA levels and neurite formation. Proc. Natl. Acad. Sci. USA 82: 7126-7130, 1985.
43. MIZOBUCHI, M. AND FROHMAN, L. A.: A rapid and simple method for labeling short DNA fragments using Taq polymerase. Biotechniques 12: 350-354, 1992.
44. NEAR, S. L., WHALEN, L. R., MILLER, J. A. AND ISHII, D. N.: Insulin-like growth factor-II stimulates motor nerve regeneration. Proc. Natl. Acad. Sci. USA 89: 11716-11720, 1992.
45. PERLMUTER, L. C., HAKAMI, M. K., HODGSON-HARRINGTON, C., GINSBERG, J., KATZ, J., SINGER, D. E. AND NATHAN, D. M.: Decreased cognitive function in aging non-insulin-dependent diabetic patients. Am. J. Med. 77: 1043-1048, 1984.
46. PETERSON, R. G., SHAW, W. N., NEEL, M.-A., LITTLE, L. A. AND EICHBERG, J.: Zucker diabetic fatty rat as a model for non-insulin-dependent diabetes mellitus. ILAR News 32: 16-19, 1990.
47. PHILLIPS, L. S. AND YOUNG, H. S.: Nutrition and somatomedin. II. Serum somatomedin activity and cartilage growth activity in streptozotocin-diabetic rats. Diabetes 25: 516-527, 1976.
48. POPKIN, M. K., CALLIES, A. L., LENTZ, R. D., COLON, E. A. AND SUTHERLAND, D. E.: Prevalence of major depression, simple phobia, and other psychiatric disorders in patients with long-standing type-I diabetes mellitus. Arch. Gen. Psychiatry 45: 64-68, 1988.
49. PU, S.-F., ZHUANG, H.-X. AND ISHII, D. N.: Differential spatio-temporal expression of the insulin-like growth factor genes in regenerating sciatic nerve. Mol. Brain Res. 34: 18-28, 1995.
50. PU, S.-F., ZHUANG, H.-X., MARSH, D. J. AND ISHII, D. N.: Insulin-like growth factor is required for spinal motoneuron survival following sciatic nerve axotomy. Soc. Neurosci. Abstr. 21: 1789, 1995.
51. PUISSANT. C. AND HOUDEBINE, L.-M.: An improvement of the single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Biotechniques 8: 148-149, 1990.
52. RECIO-PINTO, E. AND ISHII, D. N.: Insulin and related growth factors: Effects on the nervous system and mechanism for neurite growth and regeneration. Neurochem. Int. 12: 397-414, 1988a.
53. RECIO-PINTO, E. AND ISHII, D. N.: Insulin and insulinlike growth factor receptors regulating neurite formation in cultured human neuroblastoma cells. J. Neurosci. Res. 19: 312-320, 1988b.
54. RESKE-NIELSEN, E., LUNDBAEK, K. AND RAFAELSEN, O. U.: Pathological changes in the central and peripheral nervous systems of young long-term diabetics. I. Diabetic encephalopathy. Diabetologia 1: 233-241, 1965.
55. ROTWEIN, P., BURGESS, S. K., MILBRANDT, J. D. AND KRAUSE, J. E.: Differential expression of insulin-like growth factor genes in rat central nervous system. Proc. Natl. Acad. Sci. USA 85: 265-269, 1988.
56. RUNNEBAUM, I. B., SYKA, P. AND SUKUMAR, S.: Vector PCR. Biotechniques 11: 446-452, 1991.
57. RYAN, C. M.: Neurobehavioral complications of type I diabetes. Diabetes Care 11: 86-93, 1988.
58. SAID, G., SLAMA, G. AND SELVA, J.: Progressive centripetal degeneration of axons in small fibre diabetic polyneuropathy: A clinical and pathological study. Brain 106: 791-807, 1983.
59. SAIKI, R. K., SCHARF, S., FALOONA, F., MULLIS, K. B., HORN, G. T., ERLICH, H. A. AND ARNHEIM, N.: Enzymatic amplification of β-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230: 1350-1354, 1985.
60. SAMBROOK, J., FRITSCH, E. F. AND MANIATIS, T.: Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1989.
61. SCHEIWILLER, E., GULER, H.-P., MERRYWEATHER, J., SCANDELLA, C., MAERKI, W., ZAPF, J. AND FROESCH, E. R.: Growth restoration of insulin-deficient diabetic rats by recombinant human insulin-like growth factor I. Nature (Lond.) 323: 169-171, 1986.
62. SCHWANDER, J. C., HAURI, C., ZAPF, J. AND FROESCH, E. R.: Synthesis and secretion of insulin-like growth factor and its binding protein by the perfused rat liver: Dependence on growth hormone status. Endocrinology 113: 297-305, 1983.
63. SCOTT, C. D., MARTIN, J. L. AND BAXTER, R. C.: Production of insulin-like growth factor I and its binding protein by adult rat hepatocytes in primary culture. Endocrinology 116: 1094-1101, 1985.
64. SHIMATSU, A. AND ROTWEIN, P.: Mosaic evolution of the insulin-like growth factors: organization, sequence, and expression of the rat insulin-like growth factor I gene. J. Biol. Chem. 262: 7894-7900, 1987.
65. SIMA, A. A. F., NATHANIEL, V., BRIL, V., MCEWEN, T. A. J. AND GREENE, D. A.: Histopathological heterogeneity of neuropathy in insulin-dependent and non-insulin dependent diabetes, and demonstration of axo-glial dysjunction in human diabetic neuropathy. J. Clin. Invest. 81: 349-364, 1988.
66. SLAGER, U. T. AND WEBB, A. T.: Pathologic findings in the spinal cord. Arch Pathol. 96: 388-394, 1973.
67. SOARES, M. B., ISHII, D. N. AND EFSTRATIADIS, A.: Developmental and tissue-specific expression of a family of transcripts related to rat insulin-like growth factor II mRNA. Nucleic Acids Res. 13: 1119-1134, 1985.
68. SOARES, M. B., TURKEN, A., ISHII, D. N., MILLS, L., EPISKOPOU, V., COTTER, S., ZEITLIN, S. AND EFSTRATIADIS, A.: Rat insulin-like growth factor II gene: A single gene with two promoters expressing a multitranscript family. J. Mol. Biol. 192: 737-752, 1986.
69. SOININEN, H., PURANEN, M., HELKALA, E.-L., LAAKSON, M. AND RIEKKINEN, P.: Diabetes mellitus and brain atrophy: A computerized tomography study in an elderly population. Neurobiol. Aging 13: 717-721, 1992.
70. STROWIG, S. AND RASKIN, P.: Glycemic control and diabetic complications. Diabetes Care 15: 1126-1140, 1992.
71. STYLIANOPOULOU, F., HERBERT, J., SOARES, M. B. AND EFSTRATIAIDS, A.: Expression of the insulin-like growth factor II gene in the choroid plexus and the leptomeninges of the adult rat central nervous system. Proc. Natl. Acad. Sci. USA 85: 141-145, 1988.
72. SUSSENBACH, J. S., STEENBERGH, P. H., JANSEN, E., MEINSMA, D., DIJK, M. A., HOLTHUIZEN, P., DEMOOR, C. H., JANSEN, M. AND VAN DEN BRANDE, J. L.: Structure and post-translational regulation of expression of the human IGF-I and -II genes. In Modern Concepts of Insulin-Like Growth Factors, ed. by E. M. Spencer, pp. 639-654, Elsevier, New York, 1991.
73. TAN, K. AND BAXTER, R. C.: Serum insulin-like growth factor I levels in adult diabetic patients: the effect of age. J. Clin. Endocrinol. Metab. 63: 651-655, 1986.
74. THOMAS, P. K. AND TOMLINSON, D. R.: Diabetic and hypoglycemic neuropathy. In Peripheral Neuropathy, ed. by P. J. Dyck, P. K. Thomas, J. W. Griffin, P. A. Low and J. F. Poduslo, pp. 1219-1250, W. B. Saunders, Philadelphia, 1993.
75. THOMAS, P. S.: Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. USA 77: 5201-5205, 1980.
76. VINIK, A. I., HOLLAND, M. T., LEBEAU, J. M., LIUZZI, F. J., STANSBERRY, K. B. AND COLEN, L. B.: Diabetic neuropathies. Diabetes Care 15: 1926-1975, 1992.
77. WANG, C., LI, Y., WIBLE, B., ANGELIDES, K. J. AND ISHII, D. N.: Effects of insulin and insulin-like growth factors on neurofilament mRNA and tubulin mRNA content in human neuroblastoma SH-Y5Y cells. Mol. Brain Res. 13: 289-300, 1992.
78. WOLTMAN, H. W. AND WILDER, R. M.: Diabetes mellitus: Pathologic changes in spinal cord and peripheral nerves. Arch. Intern. Med. 44: 576-603, 1929.
79. WUARIN, L., GUERTIN, D. M. AND ISHII, D. N.: Reduction in insulin-like growth factor (IGF) gene expression in nerves precedes the onset of diabetic neuropathy. Exp. Neurol. 130: 106-114, 1994.
80. WUARIN, L., NAMDEV, J., BURNS, J. G., FEI, Z. AND ISHII, D. N.: Brain insulin-like growth factor-II mRNA content is reduced in insulin-dependent and non-insulin-dependent diabetes mellitus. J. Neurochem. 67: 1-10, 1996.
81. WUARIN-BIERMAN, L., ZAHND, G. R., KAUFMANN, F., BURCKLEN, L. AND ADLER, J.: Hyperalgesia in spontaneous and experimental models of diabetic neuropathy. Diabetologia 30: 653-658, 1987.
82. YAGIHASHI, S.: Pathology and pathogenetic mechanisms of diabetic neuropathy. Diabetes Metab. Rev. 11: 193-226, 1995.
83. ZHUANG, H.-X., SNYDER, C. K., PU, S.-F. AND ISHII, D. N.: Insulin-like growth factors reverse or arrest diabetic neuropathy: Effects on hyperalgesia and impaired nerve regeneration in rats. Exp. Neurol. 140: 198-205, 1996.