Axotomy induces preprotachykinin gene expression in a subpopulation of dorsal root ganglion neurons
K. Noguchi
Department of Anatomy II, Wakayama Medical College, Wakayama, Japan
Search for more papers by this authorR. Dubner
Neurobiology and Anesthesiology Branch, National Institute of Dental Research, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorM. De Leon
Neurobiology and Anesthesiology Branch, National Institute of Dental Research, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorE. Senba
Department of Anatomy II, Wakayama Medical College, Wakayama, Japan
Search for more papers by this authorCorresponding Author
M. A. Ruda
Neurobiology and Anesthesiology Branch, National Institute of Dental Research, National Institutes of Health, Bethesda, Maryland
National Institutes of Health, Building 49, Room 1A-11, Bethesda, MD 20892Search for more papers by this authorK. Noguchi
Department of Anatomy II, Wakayama Medical College, Wakayama, Japan
Search for more papers by this authorR. Dubner
Neurobiology and Anesthesiology Branch, National Institute of Dental Research, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorM. De Leon
Neurobiology and Anesthesiology Branch, National Institute of Dental Research, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorE. Senba
Department of Anatomy II, Wakayama Medical College, Wakayama, Japan
Search for more papers by this authorCorresponding Author
M. A. Ruda
Neurobiology and Anesthesiology Branch, National Institute of Dental Research, National Institutes of Health, Bethesda, Maryland
National Institutes of Health, Building 49, Room 1A-11, Bethesda, MD 20892Search for more papers by this authorAbstract
The distribution of dorsal root ganglion (DRG) cell sizes that show changes in preprotachykinin (PPT) gene expression and substance P (SP) levels following axotomy was examined using RNA blot analysis, in situ hybridization histochemistry, and immunocytochemistry. PPT mRNA was induced in medium-sized (1,000–2,000 μm2) and large-sized (>2,000 μm2) cells in the DRG after axotomy. There was a 165% increase in the number of labeled cells after sciatic transection and a 260% increase after spinal nerve transection which results in axotomy of all the cells in the ganglion. The further increase after spinal nerve transection suggests that the induction occurred in axotomized neurons. PPT mRNA label was also present in a reduced number of small (<1,000 μm2) cells after axotomy. SP immunoreactivity was also induced in medium-and large-sized cells and reduced in small-sized cells. Our findings suggest that the expression of the PPT gene and SP is differentially regulated in different subpopulations of DRG neurons after axotomy and is consistent with the hypothesis that tachykinins may be important in both sensory transmission and regeneration. © 1994 Wiley-Liss, Inc.
References
- Barbut D, Polak JM, Wall PD, (1984): Substance P in spinal cord dorsal horn decreases following peripheral nerve injury. Brain Res 205: 289–298.
- Brenneman DE, Eiden LE (1986): Vasoactive intestinal peptide and electrical activity influence neuronal survival. Proc Natl Acad Sci USA 83: 1159–1162.
-
Brown AG
(1981):
“ Organization in the Spinal Cord.”
Heidelberg: Springer.
10.1007/978-1-4471-1305-8 Google Scholar
- Cameron AA, Leah JD, Snow PJ (1986): The electrophysiological and morphological characteristics of feline dorsal root ganglion cells. Brain Res 362: 1–6.
- Carter MS, Krause JE (1990): Structure, expression, and some regulatory mechanisms of the rat preprotachykinin gene encoding substance P, neurokinin A, neuropeptide K, and neuropeptide γ. J Neurosci 10: 2203–2214.
- De Leon M, Welcher AA, Suter U, Shooter EM (1991): Identification of transcriptionally regulated genes after sciatic nerve injury. J Neurosci Res 29: 437–448.
- Devor M, Govrin-Lippman R, Frank I, Raber P (1985): Proliferation of primary sensory neurons in adult rat dorsal root ganglion and the kinetics of retrograde cell loss after sciatic nerve section. Somatosensory Res 3: 139–167.
- Dubner R (1991): Neuronal plasticity and pain following peripheral tissue inflammation or nerve injury. In MR Bond, JE Charlton, CJ Woolf (eds): “ Proceedings of the VIth World Congress on Pain.” Amsterdam: Elsevier, p. 263–276.
- Dubner R, Bennett GJ (1983): Spinal and trigeminal mechanisms of nociception. Annu Rev Neurosci 6: 381–418.
- Dubner R, Ruda MA (1992): Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 15: 96–103.
- Harper AA, Lawson SN (1985): Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurons. J Physiol 359: 31–46.
- Henken DB, Battisti WP, Chesselet MF, Murray M, Tessler A (1990): Expression of β-preprotachykinin mRNA and tachykinins in rat dorsal root ganglion cells following peripheral or central axotomy. Neuroscience 39: 733–742.
- Henry JL (1976): Effects of substance P on functionally identified units in cat spinal cord. Brain Res 114: 439–451.
- Heumann R, Korsching S, Bandtlow C, Thoenen H (1987): Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J Cell Biol 104: 1623–1631.
- Himes BT, Tessler A (1989): Death of some dorsal root ganglion neurons and plasticity of others following sciatic nerve section in adult and neonatal rats. Comp Neurol 284: 215–230.
- Hoffman PN (1989): Expression of GAP-43, a rapidly transported growth-associated protein, and class II beta tubulin, a slowly transported cytoskeletal protein, are coordinated in regenerating axons J Neurosci 9: 893–897.
- Hökfelt T, Kellerth JO, Nilsson G, Pernow B (1975): Substance P: Localization in the central nervous system and in some primary sensory neurons. Science 190: 889–890.
- Hökfelt T, Wiesenfeld-Hallin Z, Villar M, Melander T (1987): Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci Lett 83: 217–220.
- Jessell T, Tsunoo A, Kanazawa I, Otsuka M (1979): Substance P: Depletion in the dorsal horn of the rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain Res 168: 247–259.
- Kageyama R, Sasai Y, Nakanishi S (1991): Molecular characterization of transcription factors that bind to the cAMP responsive region of the substance P precursor gene. J Biol Chem 266: 15525–15531.
- Krause JE, Chirgwin JM, Carter MS, Xu ZS, Hershey AD (1987): Three rat preprotachykinin mRNAs encode the neuropeptides substance P and neurokinin A. Proc Natl Acad Sci USA 84: 881–885.
- Lembeck F (1953): Zur Frage der zentralen Übertragung afferenter Impulse. III. Mitteilung. Das Vorkommen und die Bedeutung der Substanz P in den dorsalen Wurzeln des Rückenmarks. Naunyn-Schmiedebergs Arch Pharmakol 219: 197–213.
- Light AR, Perl ER (1979): Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186: 133–150.
- Lindsay RM, Harmar AJ (1989): Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature 337: 362–364.
- Magistretti PJ, Morrison JH, Shoemaker WJ, Sapin V, Bloom FE (1981): Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: A possible regulatory mechanism for the local control of energy metabolism. Proc Natl Acad Sci USA 78: 6535–6539.
- McCullock J, Kelly PAT (1983): A functional role for vasoactive intestinal polypeptide in anterior cingulate gyrus. Nature 304: 438–440.
- McGregor GP, Gibson SJ, Sabate IM, Blank MA, Christofides ND, Wall PD, Polak JM, Bloom SR (1984): Effect of peripheral nerve section and nerve crush on spinal cord neuropeptides in the rat: Increased VIP and PHI in the dorsal horn. Neuroscience 13: 207–216.
- Narumi S, Maki Y (1978): Stimulatory effects of substance P on neurite extension and cyclic AMP levels in cultured neuroblastoma cells. J Neurochem 30: 1321–1326.
- Nawa H, Patterson PH (1990): Separation and partial characterization of neuropeptide-inducing factors in heart cell conditioned medium. Neuron 4: 269–277.
- Nielsch U, Keen P (1989): Reciprocal regulation of tachykinin-and vasoactive intestinal peptide-gene expression in rat sensory neurones following cut and crush injury. Brain Res 481: 25–30.
- Noguchi K, Ruda MA (1992): Gene regulation in an ascending nociceptive pathway: Inflammation-induced increase in preprotachykinin mRNA in rat lamina I spinal projection neurons. J Neurosci 12: 2563–2572.
- Noguchi K, Senba E, Morita Y, Sato M, Tohyama M (1989): Prepro-VIP and preprotachykin mRNAs in the rat dorsal root ganglion cells following peripheral axotomy. Mol Brain Res 6: 327–330.
- Noguchi K, Senba E, Morita Y, Sato M, Tohyama M (1990): α-CGRP and β-CGRP mRNAs are differentially regulated in the rat spinal cord and dorsal root ganglion. Mol Brain Res 7: 299–304.
- Noguchi K, De Leon M, Nahin RL, Senba E, Ruda MA (1993): Quantification of axotomy-induced alteration of neuropeptide mRNAs in dorsal root ganglion neurons with a special reference to neuropeptide Y mRNA and the effects of neonatal capsacin treatment. J Neurosci Res 35: 54–66.
- Pernow B (1953): Studies on substance P. Purification, occurrence and biological actions. Acta Physiol Scand 29 (Suppl 105): 1–90.
- Shehab SAS, Atkinson ME (1984): Sciatic nerve section has variable effects on primary afferent neuropeptides. J Anat 139: 725.
- Shehab SAS, Atkinson ME (1986): Vasoactive intestinal polypeptide increases in areas of the dorsal horn of the spinal cord from which other neuropeptides are depleted following peripheral axotomy. Exp Brain Res 62: 422–430.
- Tetzlaff W, Zwiers H, Lederis K, Cassar L, Bisby MA (1989): Axonal transport and localization of B-50/GAP-43-like immunoreactivity in regenerating sciatic and facial nerves of the rat. J Neurosci 9: 1303–1313.
- Villar MJ, Cortés R, Theodorsson E, Wiesenfeld-Hallin Z, Schalling M, Fahrenkrug J, Emson PC, Hökfelt T, (1989): Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33: 587–604.
- Wakisaka S, Kajander KC, Bennett GJ (1991): Increased neuropeptide (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci Lett 124: 200–203.
- Wong J, Oblinger MM (1991): NGF rescues substance P expression but not neurofilament or tubulin gene expression in axotomized sensory neurons. J Neurosci 11: 543–552.
- Woolf CJ, Shortland P, Coggeshall RE (1992): Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355: 75–77.
- Xu X-J, Wiesenfeld-Hallin Z, Villar MJ, Fahrenkrug J, Hökfelt T, (1990): On the role of galanin, substance P and other neuropeptides in primary sensory neurons of the rat: Studies on spinal reflex excitability and peripheral axotomy. Eur J Neurosci 2: 733–743.
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