Streptozotocin-induced diabetes is associated with altered expression of peptide-encoding mRNAs in rat sensory neurons

Peptides

Volumn 17, Issue 6, 1996, Pages 1017-1022

  Rittenhouse, Peter A ^a   Marchand, James E ^b   Chen, Juan ^a   Kream, Richard M ^b   Leeman, Susan E ^a  

^a BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CGRP; dorsal root ganglion; in situ hybridization; neuropeptide Y; somatostatin; substance P

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; MESSENGER RNA; NEUROPEPTIDE Y; SOMATOSTATIN; STREPTOZOCIN; SUBSTANCE P; TACHYKININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; GENE EXPRESSION; IN SITU HYBRIDIZATION; MALE; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; RAT; SENSORY NERVE;

ANIMALIA;

EID: 0029855222     PISSN: 01969781     EISSN: None     Source Type: Journal    
DOI: 10.1016/0196-9781(96)00129-5     Document Type: Article

References (42)

1. 1. Boehmer, C. G.; Norman, J.; Catton, M.; Fine, L. G.; Mantyh, P. W. High levels of mRNA coding for substance P, somatostatin and α-tubulin are expressed by rat and rabbit dorsal root ganglia neurons. Peptides 10:1179-1194; 1989.
2. 2. Brain, S. D.; Williams, T. J.; Tippins, J. R.; Morris, H. R.; MacIntyre, I. Calcitonin gene-related peptide is a potent vasodilator. Nature 313:54-56; 1985.
3. 3. Brain, S. D.; Williams, T. J. Inflammatory oedema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability. Br. J. Pharmacol. 86:855-860; 1985.
4. 4. Brewster, W. J.; Diemel, L. T.; Leach, R. M.; Tomlinson, D. R. Reduced sciatic nerve substance P and calcitonin gene-related peptide in rats with short-term diabetes or central hypoxaemia co-exist with normal messenger RNA levels in the lumbar dorsal root ganglia. Neuroscience 58:323-330; 1994.
5. 1 receptor antagonist, relieves chronic hyperalgesia in diabetic rats. Eur. J. Pharmacol. 241:267-270; 1993.
6. 6. Courteix, C.; Eschalier, A.; Lavarenne, J. Streptoicocin-induced diabetic rats: Behavioural evidence for a model of chronic pain. Pain 53:81-88; 1993.
7. 7. Cuello, A. C. Peptides as neuromodulators in primary sensory neurons. Neuropharmacology 26:971-979; 1987.
8. 8. Diemel, L. T.; Brewster, W. J.; Fernyhough, P.; Tomlinson, D. R. Expression of neuropeptides in experimental diabetes; effects of treatment with nerve growth factor or brain-derived neurotrophic factor. Mol. Brain Res. 21:171-175; 1994.
9. 9. Fernyhough, P.; Diemel, L. T.; Brewster, W. J.; Tomlinson, D. R. Deficits in sciatic nerve neuropeptide content coincide with a reduction in target tissue nerve growth factor messenger RNA in streptozotocin-diabetic rats: Effects of insulin treatment. Neuroscience 62:337-344; 1994.
10. 10. Ferrari, P.; Weidmann P. Editorial review: Insulin, insulin sensitivity and hypertension. J. Hypertens. 8:491-500; 1990.
11. 11. Henderson, G. S.; Conary, J. T.; Davidson, J. M.; Stewart, S. J.; House, F. S.; McCurley, T. L. A reliable method for northern blot analysis using synthetic oligonucleotide probes. Biotechniques 10:190-197; 1991.
12. 12. Holzer, P. Local effector functions of capsaicin-sensitive sensory nerve endings: Involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24:739-768; 1988.
13. 13. Hylden, J. L. K.; Wilcox, G. L. Intrathecal substance P elicits a caudally directed biting and scratching behavior in mice. Brain Res. 217:212-215; 1981.
14. 14. Jonassen, J. A.; Mullikin-Kilpatrick, D.; McAdam, A.; Leeman, S. E. Thyroid hormone status regulates preprotachykinin-A gene expression in male rat anterior pituitary. Endocrinology 121:1555-1561; 1987.
15. 15. Ju, G.; Hökfelt, T.; Brodin, E.; Fahrenkrug, J.; Fischer, J. A.; Frey, P.; Elde, R. P.; Brown, J. C. Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res. 247:417-431; 1987.
16. 16. Kamei, J.; Hitosuge, H.; Kasuya, Y. Nociceptive responses to intrathecally administered substance P and somatostatin in diabetic mice. Life Sci. 52:31-36; 1992.
17. 17. Karakida, T.; Sakai, M.; Ito, S.; Yamada, Y.; Homma, S. Changes of substance P and somatostatin contents in the gastrointestinal tract of streptozotocin diabetic rats. Neurosci. Lett. 129:173-176; 1991.
18. 18. Kashiba, H.; Noguchi, K.; Ueda, Y.; Senba E. Neuropeptide Y and galanin are coexpressed in rat large type A sensory neurons after peripheral transection. Peptides 15:411-416; 1994.
19. 19. Lawson, S. N. Morphological and biochemical cell types of sensory neurons. In: Scott, S. A., Ed. Sensory neurons: Diversity, development, and plasticity. New York: Oxford University Press; 1992:27-59.
20. 20. Liuzzi, F. J.; Suwamwalaikorn, S.; Le Beau, J. M.; Mamplata, N.; Vinik A. I. Effects of diabetes on substance P gene expression in rat lumbar dorsal root ganglia during sciatic nerve regeneration. Soc. Neurosci. Abstr. 19:339.4; 1993.
21. 21. Marchand, J. E.; Zaccheo, T. S.; Connelly, C. S.; Kream, R. M. Selective in situ hybridization histochemical analyses of alternatively spliced mRNAs encoding β- and τ-preprotachykinins in rat central nervous system. Mol. Brain Res. 17:83-94; 1993.
22. 22. Marchand, J. E.; Wurm, W. H.; Kato, T.; Kream, R. M. Altered tachykinin expression by dorsal root ganglion neurons in a rat model of neuropathic pain. Pain 58:219-231; 1994.
23. 23. Max, M. B.; Lynch, S. A.; Muir, J.; Shoaf, S. E.; Smoller, B.; Dubner, R. Effects of desipramine, amitriptyline, and fluoxetine on pain in diabetic neuropathy. N. Engl. J. Med. 326:1250-1256; 1992.
24. 24. Meller, S. T.; Bebhart, G. F.; Maves, T. J. Neonatal capsaicin treatment prevents the development of the thermal hyperalgesia produced in a model of neuropathic pain in the rat. Pain 51:317-321; 1992.
25. 25. Nahin, R. L.; Ren, K.; De León, M.; Ruda, M. Primary sensory neurons exhibit altered gene expression in a rat model of neuropathic pain. Pain 58:95-198; 1994.
26. 26. Noguchi, K.; Senba, E.; Morita, Y.; Sato, M.; Tohyama, M. Prepro-VIP and preprotachykinin mRNAs in the rat dorsal root ganglion cells following peripheral axotomy. Mol. Brain Res. 6:327-330; 1989.
27. 27. Nothias, F.; Tessler, A.; Murray, M. Restoration of substance P and calcitonin gene-related peptide in dorsal root ganglia and dorsal horn after neonatal sciatic nerve lesion. J. Comp. Neurol. 334:370-384; 1993.
28. 28. Ohkubo, T.; Shibata, M.; Takahashi, H.; Inoki, R. Roles of substance P and somatostatin on transmission of nociceptive information induced by formalin in spinal cord. J. Pharmacol. Exp. Ther. 252:1261-1268; 1990.
29. 29. Otsuka, M.; Yoshioka, K. Neurotransmitter functions of mammalian tachykinins. Physiol. Rev. 73:229-308; 1993.
30. 30. Perl, E. R. Function of dorsal root ganglion neurons: an overview. In: Scott, S. A., Ed. Sensory neurons: Diversity, development, and plasticity. New York: Oxford University Press; 1992;3-23.
31. 31. Schmidt, R. E.; Dorsey, D. A.; Roth, K. A. Immunohistochemical characterization of NPY and substance P containing nerve terminals in aged and diabetic human sympathetic ganglia. Brain Res. 583:320-326; 1992.
32. 32. Seybold, V. S.; Hylden, J. L. K.; Wilcox, G. L. Intrathecal substance P and somatostatin in rats: behaviors indicative of sensation. Peptides 3:49-54; 1982.
33. 33. Sipols, A. J.; Baskin, D. G.; Schwartz, M. W. Effect of intracere-broventricular insulin infusion on diabetic hyperphagia and hypothalmic neuropeptide gene expression. Diabetes 44:147-151; 1994.
34. 34. Smith, G. D.; Seckl, J. R.; Harmar, A. J. Distribution of neuropeptides in dorsal root ganglia of the rat; substance P, somatostatin and calcitonin gene-related peptide. Neurosci. Lett. 153:5-8; 1993.
35. 35. Tomlinson, K. C.; Gardiner, S. M.; Hebden, R. A.; Bennet, T. Functional consequences of streptozotocin-induced diabetes mellitus, with particular reference to the cardiovascular system. Pharmacol. Rev. 44:103-150; 1992.
36. 36. Too, H. P.; Maggio, J. E. Radioimmunoassay of tachykinins. In: Conn, P. M., Ed. Methods in neurosciences, vol. 6. New York: Academic Press; 1991;232-247.
37. 37. Tracey, D. J.; Romm, M. A.; Yao, N. N. L. Peripheral hyperalgesia in experimental neuropathy: Exacerbation by neuropeptide Y. Brain Res. 669:245-254; 1995.
38. 38. Tuchscherer, M. M.; Seybold, V. S. Immunohistochemical studies of substance P, cholecystokinin-octapeptide and somatostatin in dorsal root ganglia of the rat. Neuroscience 14:593-605; 1985.
39. 39. Wahlestedt, C.; Reis, D. J. Neuropeptide Y-related peptides and their receptors - are the receptors potential therapeutic drug targets? Annu. Rev. Pharmacol. Toxicol. 32:309-352; 1993.
40. 40. Wakisaka, S.; Kajander, K. C.; Bennet, G. J. Increased neuropeptide Y (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci. Lett. 124:200-203; 1991.
41. 41. White, J. D.; Olchovsky, D.; Kershaw, M.; Berelowitz, M. Increased hypothalamic content of preproneuropeptide-Y messenger ribonucleic acid in streptozotocin-diabetic rats. Endocrinology 126:765-772; 1990.
42. 42. Zaccheo, T. S.; Gonsalves, R. A.; Kream, R. M. Detection and estimation of mRNA levels using a nonlinear model in neurons labeled by in situ hybridization histochemistry. Neuroimage 1:151-161; 1993.