Immunohistochemical, histochemical and radioassay analysis of nitric oxide synthase immunoreactivity in the lumbar and sacral dorsal root ganglia of the dog

Cellular and Molecular Neurobiology

Volumn 26, Issue 1, 2006, Pages 17-44

  Lukáčová, Nadežda ^a   Kolesár, Dalibor ^a   Maršala, Martin ^b   Maršala, Jozef ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Densitometry; Neuromodulator; Nitric oxide activity; Nitric oxide expression; Primary sensory neurons

Indexed keywords

NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL SIZE; CONTROLLED STUDY; DENSITOMETRY; DOG; FEMALE; FEMORAL NERVE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; RADIOASSAY; SCIATIC NERVE; SPINAL GANGLION;

ANIMALS; DOGS; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; LUMBAR VERTEBRAE; NADPH DEHYDROGENASE; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; RADIOLIGAND ASSAY; SACRUM;

CANIS FAMILIARIS;

EID: 33745595631     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-006-8843-4     Document Type: Article

References (76)

1. Aimi, Y., Fujimura, M., Vincent, S. R., and Kimura, H. (1991). Localization of NADPH diaphorase-containing neurons in sensory ganglia in the rat. J. Comp. Neurol. 306:382-392.
2. Aoki, M., and Mori, S. (1978). Changes in monosynaptic EPSPs of quadriceps motoneurons in monkeys with the spinal cord chronically hemisected at the thoracic level. In Ito, M., Tsukahara, N., Kubota, K., and Yagi, K. (eds.), Integrative Control Functions of the Brain, Vol. 1, Elsevier, Amsterdam, pp. 170-171.
3. Ashby, P., Stalberg, E., Winkler, T., and Hunter, J. P. (1987). Further observations on the depression of group Ia facilitation of motoneurons by vibration in man. Exp. Brain Res. 69:1-6.
4. Basbaum, A. I., and Glazer, E. J. (1983). Immunoreactive vasoactive intestinal polypeptide is concentrated in the sacral spinal cord: A possible marker for pelvic visceral afferent fibers. Somatosens. Res. 1:69-82.
5. Berardelli, A., Sabra, A. F., Hallett, M., Berenberg, W., and Simon, S. R. (1983). Stretch reflexes of triceps surae in patients with upper motor neuron syndromes. J. Neurol. Neurosurg. Psychiatry 46:54-60.
6. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
7. Bredt, D. S., Glatt, C. E., Hwang, P. M., Fotuhi, M., Dawson, T. M., and Snyder, S. H. (1991). Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7:615-624.
8. Bredt, D. S., Hwang, P. M., and Snyder, S. H. (1990). Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768-770.
9. Cameron, A. A., Leah, J. D., and Snow, P. J. (1986). The electrophysiological and morphological characteristics of feline dorsal root ganglion cells. Brain Res. 362:1-6.
10. Cameron, A. A., Leah, J. D., and Snow, P. J. (1988). The coexistence of neuropeptides in feline sensory neurons. Neuroscience 27:969-979.
11. Dalsgaard, C., Ygge, J., Vincent, S., Ohrling, M., Dockray, G., and Elde, R. (1984). Peripheral projections and neuropeptide coexistence in a subpopulation of fluoride-resistant acid phosphatase reactive spinal primary sensory neurons. Neurosci. Lett. 51:139-144.
12. DeGroat, W. C. (1987). Neuropeptides in pelvic afferent pathways. Experientia 43:801-813.
13. Dun, N. J., Dun, S. L., Wu, S. Y., Försterman, U., Schmidt, H. H. H. M., and Tseng, L. F. (1993). Nitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrel monkey spinal cord. Neuroscience 54:845-857.
14. Egberongbe, Y. I., Gentleman, S. M., Falkai, P., Bogerts, B., Polak, J. M., and Roberts, G. W. (1994). The distribution of nitric oxide synthase immunoreactivity in the human brain. Neuroscience 59:561-578.
15. Fournier, E., Meunier, S., Pierrot-Deseilligny, E., and Shindo, M. (1986). Evidence for interneuronally mediated Ia excitatory effects to human quadriceps motoneurones. J. Physiol. 377:143-169.
16. Franco-Cereceda, A., Henke, H., Lundberg, J. M., Petermann, J. B., Hökfelt, T., and Fischer, J. A. (1987). Calcitonin gene related-peptide (CGRP) in capsaicin-sensitive substance P-immunoreactive sensory neurons in animals and man: Distribution and release by capsaicin. Peptides 8:399-410.
17. Garry, M. G., Miller, K. E., and Seybold, V. S. (1989). Lumbar dorsal root ganglia of the cat: A quantitative study of peptide immunoreactivity and cell size. J. Comp. Neurol. 284:36-47.
18. Gerebtzoff, M. A., and Maeda, T. (1968). Caractères et localisation histochimique d́un isoenzyme fluororésistant de la phosphatase acide dans la moelle épinière du rat. C. R. Soc. Biol. (Paris) 162:2032-2035.
19. Gibbins, I. L., Furness, J. B., and Costa, M. (1987). Pathway-specific patterns of the co-existence of substance P, calcitonin gene-related peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig. Cell Tissue Res. 248:417-437.
20. Gibbins, I. L., Furness, J. B., Costa, M., MacIntyre, I., Hillyard, C. J., and Girgis, S. (1985). Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci. Lett. 57:125-130.
21. Gibson, S. J., Polak, J. M., Bloom, S. R., Sabate, I. M., Mulderry, P. M., Ghatei, M. A., McGregor, G. P., Morrison, J. F., Kelly, J. S., and Evans, R. M. (1984). Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J. Neurosci. 4:3101-3111.
22. González-Hernández, T. and Rustioni, A. (1999a). Expresion of three forms of nitric oxide synthase in peripheral nerve regeneration. J. Neurosci. Res. 55:198-207.
23. González-Hernández, T., and Rustioni, A. (1999b). Nitric oxide synthase and growth-associated protein are coexpressed in primary sensory neurons after peripheral injury. J. Comp. Neurol. 404:64-74.
24. Halčák, L., Pecháňová, O., Žigová, Z., Klemová, L., Novacký, M., and Bernátová, I. (2000). Inhibition of NO syntase activity in nervous tissue leads to decreased motor activity in the rat. Physiol. Res. 49:143-149.
25. Harper, A. A., and Lawson, S. N. (1982). Physiology and morphology in rat and mouse primary afferent neurons. J. Physiol. (Lond.) 327:22P-23P.
26. Herbison, G. J., Isaac, Z., Cohen, M. E., and Ditunno, J. F., Jr. (1996). Strength post-spinal cord injury: Myometer vs manual muscle test. Spinal Cord 34:543-548.
27. Hökfelt, T., Kellerth, J. O., Nilssen, G. and Pernow, B. (1975). Substance P: Localisation in the central nervous system and in some primary sensory neurons. Science 19:889-890.
28. Hökfelt, T., Wiesenfeld-Hallin, Z., Villar, M., and Melander, T. (1987). Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci. Lett. 83:217-220.
29. Ju, G., Melander, T., Ceccatelli, S., Hökfelt, T., and Frey, P. (1987). Immunohistochemical evidence for a spinothalamic pathway co-containing cholecystokinin and galanin-like immunoreactivities in the rat. Neuroscience 20:439-456.
30. Kai-Kai, M. A., Anderton, B. H., and Keen, P. (1986). A quantitative analysis of the interrelationships between subpopulations of rat sensory neurons containing arginine vasopressin or oxytocin and those containing substance P, fluoride-resistant acid phosphatase or neurofilament protein. Neuroscience 18:475-486.
31. Kawatani, M., Lowe, I. P., Nadelhaft, I., Morgan, C., and DeGroat, W. C. (1983). Vasoactive intestinal polypeptide in visceral afferent pathways to the sacral spinal cord of the cat. Neurosci. Lett. 42:311-316.
32. Keilhoff, G., Fansa, H., and Wolf, G. (2002). Neuronal nitric oxide synthase is the dominant nitric oxide supplier for the survival of dorsal root ganglia after peripheral nerve axotomy. J. Chem. Neuroanat. 24:181-187.
33. Knyihár, E. (1971). Fluoride resistant acid phosphatase system of nociceptive dorsal root afferents. Experientia 27:1205-1207.
34. Lawson, S. N. (1979). The postnatal development of large light and small dark neurons in mouse dorsal root ganglia: A statistical analysis of cell numbers and size. J. Neurocytol. 8:275-294.
35. Lawson, S. N., and Harper, A. A. (1983). Correlations between electrophysiology and cell type in rat dorsal root ganglion neurons. In Davey, D. F. (ed.), Proc. Int. Union. Physiol. Sci. 15:188-200.
36. Lazorthes, Y., Sol, J.-C., Sallerin, B., and Verdié, J.-C. (2002). The surgical management of spasticity. Eur. J. Neurol. 9:35-41.
37. Leah, J. D., Cameron, A. A., Kelly, W. L., and Snow, P. J. (1985). Coexistence of peptide immunoreactivity in sensory neurons of the cat. Neuroscience 16:683-690.
38. Lee, Y., Takami, K., Kawai, Y., Girgis, S., Hillyard, C. J., MacIntyre, I., Emson, P. C., and Tohyama, M. (1985). Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistance with substance P. Neuroscience 15:1227-1237.
39. Lee, K. H., Chung, K., Chung, J. M., and Coggeshall, R. E. (1986). Correlation of cell body size, axon size, and signal conduction velocity for individually labelled dorsal root ganglia cells in the cat. J. Comp. Neurol. 243:335-346.
40. Lloyd, D. P. C. (1943). Neuron patterns controlling transmission of ipsilateral hindlimb reflexes in cat. J. Neurophysiol. 6:293-326.
41. Lukáčová, N., Čížková, D., Maršala, M., Jalč, P., and Maršala, J. (1999). Segmental and laminar distributions of nicotinamide adenine dinucleotide phosphate-diaphorase-expressing and neuronal nitric oxide synthase- immunoreactive neurons versus radioassay detection of catalytic nitric oxide synthase activity in the rabbit spinal cord. Neuroscience 94:229-237.
42. Lundberg, J., Franco-Cereceda, H. X., Hökfelt, T., and Fischer, J. A. (1985). Co-existence of substance P and calcitonin gene-related peptide-like immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin. Eur. J. Pharmacol. 108:315-319.
43. Manjarrez, E., Rocha, T., Rojas-Piloni, G., Mendez, I., Velez, D., and Flores, A. (2001). NO donor SIN-1 potentiates monosynaptic reflexes in the cat spinal cord. Neuroreport 12:2667-2671.
44. Maršala, J., Kluchová, D., and Maršala, M. (1997). Spinal cord gray matter layers rich in NADPH diaphorase-positive neurons are refractory to ischemia-reperfusion-induced injury: A histochemical and silver impregnation study in rabbit. Exp. Neurol. 145:165-179.
45. Maršala, J., Maršala, M., Vanický, I., and Taira, Y. (1999). Localization of NADPHd-exhibiting neurons in the spinal cord of the rabbit. J. Comp. Neurol. 406:263-284.
46. Maršala, J., Vanický, I., Maršala, M., Jalč, P., Orendáčová, J., and Taira, Y. (1998). Reduced nicotinamide adenine dinucleotide phosphate diaphorase in the spinal cord of dogs. Neuroscience 85:847-862.
47. Matthews, P. B. C. (1972). Where does Sherrington's "muscular sense" originate? Muscles, joints, corollary discharge. Annu. Rev. Neurosci. 5:189-218.
48. Mizukawa, K., McGreer, P. L., Vincent, S. R., and McGeer, R. (1989). Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system. J. Comp. Neurol. 279:281-311.
49. Molander, C., Ygge, J., and Dalsgaard, C. J. (1987). Substance P-, somatostatin- and calcitonin gene-related peptide-like immunoreactivity and fluoride resistant acid phosphatase-activity in relation to retrogradely labeled cutaneous, muscular and visceral primary sensory neurons in the rat. Neurosci. Lett. 74:37-42.
50. Nagy, J. I., and Hunt, S. P. (1982). Fluoride-resistant acid phosphatase-containing neurons in dorsal root ganglia are separate from those containing substance P or somatostatin. Neuroscience 7:89-97.
51. Park, J. H., Straub, V. A., and O'Shea, M. (1998). Anterograde signaling by nitric oxide: Characterization and in vitro reconstitution of an identified nitrergic synapse. J. Neurosci. 18:5463-5476.
52. Philippides, A., Husbands, P., and O'Shea, M. (2000). Four-dimensional neuronal signaling by nitric oxide: A computational analysis. J. Neurosci. 20:1199-1207.
53. Pierrot-Deseilligny, E., Morin, C., Bergego, C., and Tankov, N. (1981). Pattern of group I fibre projections from ankle flexor and extensor muscles in man. Exp. Brain Res. 42:337-350.
54. Price, J. (1985). An immunohistochemical and quantitative examination of dorsal root ganglion neuronal subpopulations. J. Neurosci. 5:2051-2059.
55. Rambourg, A., Clermont, Y., and Beaudet, A. (1983). Ultrastructural features of six types of neurons in rat dorsal root ganglia. J. Neurocytol. 12:47-66.
56. Saito, S., Kidd, G. J., Trapp, B. D., Dawson, T. M., Bredt, D. S., Wilson, D. A., Traystman, R. J., Snyder, S. H., and Hanley, D. F. (1994). Rat spinal cord neurons contain nitric oxide synthase. Neuroscience 59:447-456.
57. Shepherd, G. M. (1988). Neurobiology. Oxford University Press, Oxford.
58. Scherer-Singler, U., Vincent, S. R., Kimura, H., and McGeer, E. G. (1983). Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Methods 9:229-234.
59. Skofitsch, G., and Jacobowitz, D. M. (1985). Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat. Peptides 6:747-754.
60. Sommer, E. W., Kazimierczak, J., and Droz, B. (1985). Neuronal subpopulations in the dorsal root ganglion of the mouse as characterized by combination of ultrastructural and cytochemical features. Brain Res. 346:310-326.
61. Stone, J. R., and Marletta, M. A. (1996). Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide. Biochemistry 35:1093-1099.
62. Strosznajder, J., and Chalimoniuk, M. (1996). Biphasic enhancement of nitric oxide synthase activity and cGMP level following brain ischemia in gerbils. Acta Neurobiol. Exp. 56:71-81.
63. Tasci, N., Ankarali, S., and Demir, S. (2003). Further evidence for enhancing effects of NO on monosynaptic and polysynaptic spinal reflexes in cats. Brain Res. 980:109-116.
64. Terenghi, G., Riveros-Moreno, V., Hudson, L. D., Ibrahim, N. B., and Polak, J. M. (1993). Immunohistochemistry of nitric oxide synthase demonstrates immunoreactive neurons in spinal cord and dorsal root ganglia of man and rat. J. Neurol. Sci. 118:34-37.
65. Tsai, S., Tew, J., McLean, J., and Shipley, M. (1988). Cerebral arterial innervation by nerve fibers containing calcitonin gene-related peptide (CGRP): I. Distribution and origin of CGRP perivascular innervation in the rat. J. Comp. Neurol. 271:435-444.
66. Tuchscherer, M. M., and Seybold, V. S. (1985). Immunohistochemical studies of substance P, cholecystokinin-octapeptide and somatostatin in dorsal root ganglia of the rat. Neuroscience 14:593-605.
67. Tuchscherer, M. M., and Seybold, V. S. (1989). A quantitative study of the coexistence of peptides in varicosities within the superficial laminae of the dorsal horn of the rat spinal cord. J. Neurosci. 9:195-205.
68. Valtschanoff, J. G., Weinberg, R. J., and Rustioni, A. (1992). NADPH diaphorase in the spinal cord of rats. J. Comp. Neurol. 321:209-222.
69. Vanderhorst, V. G., and Holstege, G. (1997). Organization of lumbosacral motoneuronal cell groups innervating hindlimb, pelvic floor, and axial muscles in the cat. J. Comp. Neurol. 382:46-76.
70. Vizzard, M. A., Erdman, S. L., Ericson, V. L., Stewart, R. J., Roppolo, R. J., and de Groat, W. C. (1994). Localization of NADPH diaphorase in the lumbosacral spinal cord and dorsal root ganglia of the cat. J. Comp. Neurol. 339:62-75.
71. Wetts, R., and Vaughn, J. E. (1994). Choline acetyltransferase and NADPH diaphorase are co-expressed in rat spinal cord neurons. Neuroscience 63:1117-1124.
72. Wiesenfeld-Hallin, Z., Hökfelt, T., Lundberg, J. M., Forssmann, W. G., Reinecke, M., Tschopp, F. A., and Fischer, J. A. (1984). Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat. Neurosci. Lett. 52:199-204.
73. Willis, W. D., and Coggeshall, R. E. (1991). Sensory Mechanisms of the Spinal Cord. Plenum Press, New York.
74. Wood, J., and Garthwaite, J. (1994). Models of the diffusional spread of nitric oxide: Implications for neuralnitric oxide signalling and its pharmacological properties. Neuropharmacology 33:1235-1244.
75. Yoshida, S., and Matsuda, Y. (1979). Studies on sensory neurons of the mouse with intracellular recording and horseradish peroxidase injection techniques. J. Neurophysiol. 42:1134-1146.
76. Yoshida, S., Matsuda, Y., and Semejima, A. (1978). Tetrodotoxin-resistant sodium and calcium components of action potentials in dorsal root ganglion cells of the adult mouse. J. Neurophysiol. 41:1096-1106.