Immunocytochemical localization of neurokinin B in the rat spinal dorsal horn and its association with substance P and GABA: An electron microscopic study

Journal of Comparative Neurology

Volumn 420, Issue 3, 2000, Pages 349-362

  McLeod, Amber L ^a   Krause, James E ^b   Ribeiro Da Silva, Alfredo ^a  

^a MCGILL UNIVERSITY   (Canada)

^b NEUROGEN CORPORATION   (United States)

Author keywords

Nociception; Spinal cord; Tachykinin; Ultrastructure

Indexed keywords

4 AMINOBUTYRIC ACID; NEUROKININ B; SUBSTANCE P; TACHYKININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CROSS LINKING; DENDRITIC CELL; ELECTRON MICROSCOPY; GABAERGIC TRANSMISSION; IMMUNOCYTOCHEMISTRY; LAMINA PROPRIA; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; RAT; SPINAL CORD DORSAL HORN;

ANIMALS; AXONS; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; NEUROKININ B; NOCICEPTORS; PAIN; POSTERIOR HORN CELLS; RATS; RATS, WISTAR; SUBSTANCE P;

EID: 0034621646     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000508)420:3<349::AID-CNE6>3.0.CO;2-K     Document Type: Article

References (58)

1. Adams JC. 1981. Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775.
2. Bean AJ, Zhang X, Hökfelt T. 1994. Peptide secretion: what do we know. FASEB J 8:630-638.
3. Bonner IT, Affolter HU, Young AC, Young WS III. 1987. A cDNA encoding the precursor of the rat neuropeptide, neurokinin Brain Res Mol Brain Res 2:243-249.
4. Chan-Palay V, Palay SL. 1977. Ultrastructural identification of substance P cells and their processes in rat sensory ganglia and their terminals in the spinal cord by immunocytochemistry. Proc Natl Acad Sci USA 74:4050-4054.
5. Coimbra A, Ribeiro-da-Silva A, Pignatelli D. 1984. Effects of dorsal rhizotomy on the several types of primary afferent terminals in laminae I-III of the rat spinal cord. An electron microscope study. Anat Embryol (Berl) 170:279-287.
6. Couture R, Boucher S, Picard P, Regoli D. 1993. Receptor characterization of the spinal action of neurokinins on nociception: a three receptor hypothesis. Regul Pept 46:426-429.
7. Cruz F, Lima D, Coimbra A. 1987. Several morphological types of terminal arborizations of primary afferents in laminae I-II of the rat spinal cord, as shown after HRP labeling and Golgi impregnation. J Comp Neurol 261:221-236.
8. Cuello AC, Kanazawa I. 1978. The distribution of substance P immunoreactive fibers in the rat central nervous system. J Comp Neurol 178: 129-156.
9. Cuello AC, Jessell TM, Kanazawa I, Iversen LL. 1977. Substance P: localization in synaptic vesicles in rat central nervous system. J Neurochem 29:747-751.
10. Cuello AC, Galfre G, Milstein C. 1979. Detection of substance P in the central nervous system by a monoclonal antibody. Proc Natl Acad Sci USA 76:3532-3536.
11. Dalsgaard CJ, Haegerstrand A, Theodorsson-Norheim E, Brodin E, Hökfelt T. 1985. Neurokinin A-like immunoreactivity in rat primary sensory neurons; coexistence with substance P. Histochemistry 83:37-39.
12. De Biasi S, Rustioni A. 1988. Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord. Proc Natl Acad Sci USA 85:7820-7824.
13. Ding YQ, Shigemoto R, Takada M, Ohishi H, Nakanishi S, Mizuno N. 1996. Localization of the neuromedin K receptor (NK3) in the central nervous system of the rat. J Comp Neurol 364:290-310.
14. Duncan D, Morales R. 1978. Relative numbers of several types of synaptic connections in the substantia gelatinosa of the cat spinal cord. J Comp Neurol 182:601-610.
15. Gray EG. 1969. Electron microscopy of excitatory and inhibitory synapses: a brief review. Prog Brain Res 31:141-155.
16. Gundersen V, Chaudhry FA, Bjaalie JG, Fonnum F, Ottersen OP, Storm-Mathisen J. 1998. Synaptic vesicular localization and exocytosis of L-aspartate in excitatory nerve terminals: a quantitative immunogold analysis in rat hippocampus. J Neurosci 18:6059-6070.
17. 3 receptor antagonist, SR 142801, studied in isolated neonatal rat spinal cord. Neuropeptides 32:537-542.
18. Heike CJ, Krause JE, Mantyh PW, Couture R, Bannon MJ. 1990. Diversity of mammalian tachykinin peptidergic neurons: multiple peptides, receptors, and regulatory mechanisms. FASEB J 4:1606-1615.
19. 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.
20. Kenigsberg RL, Semenenko FM, Cuello AC. 1990. Development of a bispecific monoclonal antibody for simultaneous detection of rabbit IgG and horseradish peroxidase: use as a general reagent in immunocytochemistry and enzyme-linked immunosorbent assay. J Histochem Cytochem 38:191-198.
21. Kosaka T, Nagatsu I, Wu J-Y, Hama K. 1986. Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18:975-990.
22. Kotani H, Hoshimaru M, Nawa H, Nakanishi S. 1986. Structure and gene organization of bovine neuromedin K precursor. Proc Natl Acad Sci USA 83:7074-7078.
23. 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.
24. Laing I, Todd AJ, Heizmann CW, Schmidt HHHW. 1994. Subpopulations of GABAergic neurons in laminae I-III of rat spinal dorsal horn defined by coexistence with classical transmitters, peptides, nitric oxide synthase or parvalbumin. Neuroscience 61:123-132.
25. Laneuville O, Dorais J, Couture R. 1988. Characterization of the effects produced by neurokinins and three agonists selective for neurokinin receptor subtypes in a spinal nociceptive reflex of the rat. Life Sci 42:1295-1305.
26. 3 receptors mediate thermal but not mechanical hyperalgesia via nitric oxide. Pain 80:309-317.
27. 3 receptors facilitate the nociceptive flexor reflex via a pathway involving nitric oxide. Pain 80:301-308.
28. Lucas LR, Hurley DL, Krause JE, Harlan RE. 1992. Localization of the tachykinin neurokinin B precursor peptide in rat brain by immunocytochemistry and in situ hybridization. Neuroscience 51:317-345.
29. Marksteiner J, Sperk G, Krause JE. 1992a. Distribution of neurons expressing neurokinin B in the rat brain: immunohistochemistry and in situ hybridization. J Comp Neurol 317:341-356.
30. Marksteiner J, Saria A, Krause JE. 1992b. Comparative distribution of neurokinin B-, substance P- and enkephalin-like immunoreactivities and neurokinin B messenger RNA in the basal forebrain of the rat: evidence for neurochemical compartmentation. Neuroscience 51:107-120.
31. Maxwell DJ, Christie WM, Short AD, Storm-Mathisen J, Ottersen OP. 1990. Central boutons of glomeruli in the spinal cord of the cat are enriched with L-glutamate-like immunoreactivity. Neuroscience 36: 83-104.
32. McCarson KE, Krause JE. 1994. NK-1 and NK-3 type tachykinin receptor mRNA expression in the rat spinal cord dorsal horn is increased during adjuvant or formalin-induced nociception. J Neurosci 14:712-720.
33. McCarson KE, Krause JE. 1995. The formalin-induced expression of tachykinin peptide and neurokinin receptor messenger rnas in rat sensory ganglia and spinal cord is modulated by opiate preadministration. Neuroscience 64:729-739.
34. McLeod AL, Krause JE, Cuello AC, Ribeiro-da-Silva A. 1998. Preferential synaptic relationships between substance P-immunoreactive boutons and neurokinin 1 receptor sites in the rat spinal cord. Proc Natl Acad Sci USA 95:15,775-15,780.
35. Meller ST, Gebhart GF. 1993. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52:127-136.
36. Merighi A, Polak JM, Fumagalli G, Theodosis DT. 1989. Ultrastructural localization of neuropeptides and GABA in rat dorsal horn: a comparison of different Immunogold labeling techniques. J Histochem Cytochem 37:529-540.
37. Munekata E. 1991. Neurokinin A and B. Comp Biochem Physiol [C] 98C: 171-179.
38. Murray M, Goldberger ME. 1986. Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral lumbosacral dorsal rhizotomy in adult cats. J Neurosci 6:3205-3217.
39. Nakanishi S. 1987. Substance P precursor & kininogen: their structures, gene organization and regulation. Physiol Rev 67:1117-1142.
40. Nawa H, Hirose T, Takashima H, Inayama S, Nakanishi S. 1983. Nucleotide sequences of cloned cDNAs for two types of bovine brain, substance P precursor. Nature 306:32-36.
41. Ogawa T, Kanazawa I, Kimura S. 1985. Regional distribution of substance P, neurokinin α and neurokinin β in rat spinal cord, nerve roots and dorsal root ganglia, and the effects of dorsal root section or spinal transection. Brain Res 359:152-157.
42. Priestley JV, Somogyi P, Cuello AC. 1982. Immunocytochemical localization of substance P in the spinal trigeminal nucleus of the rat: a light and electron microscopic study. J Comp Neurol 211:31-49.
43. Ribeiro-da-Silva A. 1995. Substantia gelatinosa of spinal cord. In: Paxinos G, editor. The rat nervous system. Sydney: Academic Press, p 47-59.
44. Ribeiro-da-Silva A, Coimbra A. 1982. Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord. J Comp Neurol 209:176-186.
45. Ribeiro-da-Silva A, Castro-Lopes JM, Coimbra A. 1986. Distribution of glomeruli with fluoride-resistant acid phosphatase (FRAP)-containing terminals in the substantia gelatinosa of the rat. Brain Res 377:323-329.
46. Ribeiro-da-Silva A, Tagari P, Cuello AC. 1989. Morphological characterization of substance P-like immunoreactive glomeruli in the superficial dorsal horn of the rat spinal cord and trigeminal subnucleus caudalis: a quantitative study. J Comp Neurol 281:497-415.
47. Ribeiro-da-Silva A, Priestley JV, Cuello AC. 1993. Pre-embedding ultra-structural immunocytochemistry. In: Cuello AC, editor. Immunohistochemistry II. Chichester: John Wiley & Sons, p 181-227.
48. Schmid G, Carità F, Bonanno G, Raiteri M. 1998. NK-3 receptors mediate enhancement of substance P release from capsaicin-sensitive spinal cord afferent terminals. Br J Pharmacol 125:621-626.
49. 3 receptor-immunoreactivity to subpopulations of neurons in rat spinal cord. J Comp Neurol 381:439-448.
50. Snider WD, McMahon SB. 1998. Tackling pain at the source: new ideas about nociceptors. Neuron 20:629-632.
51. Somogyi P, Halasy K, Somogyi J, Storm-Mathisen J, Ottersen OP. 1986. Quantification of Immuno-gold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience 19:1045-1050.
52. Suresh MR, Cuello AC, Milstein C. 1986. Advantages of bispecific hybridomas in one-step immunocytochemistry and immunoassays. Proc Natl Acad Sci USA 83:7989-7993.
53. Too HP, Maggio JE. 1991. Immunocytochemical localization of neuromedin K (neurokinin B) in rat spinal ganglia and cord. Peptides 12:431-443.
54. Uchizono K. 1965. Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature 207:642-643.
55. Valtschanoff JG, Phend KD, Bernards PS, Weinberg RJ, Rustioni A. 1994. Amino acid immunocytochemistry of primary afferent terminals in the rat dorsal horn. J Comp Neurol 346:237-252.
56. Warden MK, Young WS. 1988. Distribution of cells containing mRNAs encoding substance P and neurokinin B in the rat central nervous system. J Comp Neurol 272:90-113.
57. Willis WD, Westlund KN, Carlton SM. 1995. Pain. In: Paxinos G, editor. The rat nervous system. Sydney: Academic Press, p 725-750.
58. Zhuo H, Heike CJ. 1993. Neurokinin B peptide-2 neurons project from the hypothalamus to the thoracolumbar spinal cord of the rat. Neuroscience 52:1019-1028.