Increased expression of neuronal nitric oxide synthase in bladder afferent and spinal neurons following spinal cord injury

Developmental Neuroscience

Volumn 19, Issue 3, 1997, Pages 232-246

  Vizzard, Margaret A ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

Bladder; Dorsal root ganglia; Lateral collateral pathway; Neuronal nitric oxide synthase; Sacral parasympathetic nucleus; Spinal cord transection; Sympathetic autonomic nucleus

Indexed keywords

FLUOROGOLD; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER; CONTROLLED STUDY; ENZYME LOCALIZATION; FEMALE; LUMBAR SPINE; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETROGRADE NERVE FIBER TRANSPORT; SACRUM; SENSORY NERVE CELL; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; SPINAL GANGLION; THORACIC SPINE;

EID: 0030982085     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000111212     Document Type: Article

References (77)

1. Dawson TM. Bredt DS. Fotulii M. Hwang PM. Snyder SH: Nitric oxide synthase and neuronal NADPH-diaphorasc arc identical in brain and peripheral tissues. Proc Natl Acad Sci USA 1991:88:7797-7801.
2. Hope BT. Michael GJ. Knigge KM, Vincent SR: Neuronal NADPH-diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 1991: 88:2811-2814.
3. Anderson CR: NADPH-diaphorasc-positive neurons in the rat spinal cord include a subpopulation of autonomic preganglionic neurons. Ncurosci Lett 1992:139:280-284.
4. Valtschanoff JG. Weinberg RJ. Rustioni A: NADPH-diaphorase in the spinal cord of rats. J Comp Neurol 1992:321:209-222.
5. Saito S. Kidd GJ. Trapp BD. Dawson TM. Bredt DS. Wilson DA. Traystman RJ. Snyder SH. Hanley DF: Rat spinal cord neurons contain nitric oxide synthase. Neuroscience 1994: 59:447-456.
6. Vizzard MA, Erdman SL, de Groat WC: Localization of NADPH-diaphorase in pelvic afferent and efferent pathways of the rat. Neurosci Lett 1993;152:72-76.
7. Vizzard MA. Erdman SL. dc Groat WC: Increased expression of neuronal nitric oxide synthase in visceral neurons after nerve injury. J Neurosci 1995:15:4033-4045.
8. Burnett AL. Lowcnstcin CJ. Bredt DS. Chang TSK. Snyder SH: Nitric oxide: A physiologic mediator of penile erection. Science 1992:257: 401-403.
9. Dail WG. Galloway B. Bordegaray J. Walton G: Functional and histochemical evidence for the involvement of nitric oxide in regulation of penile erectile tissue. Soc Neurosci Abstr 1992: 18:128.
10. Kcast JR: A possible neural source of nitric oxide in the rat penis. Neurosci Lett 1992:143: 69-73.
11. McNeill DL. Traugh NE Jr. Vaidva AM, Hua HT. Papka RE; Origin and distribution of NADPH-diaphorasc-positive neurons and fibers innervating the urinary bladder of the rat. Neurosci Lett 1992:147:33-36.
12. Santer SM. Symons D: Distribution of NADPH-diaphorasc activity in rat paravertebral, prévertébral and pelvic sympathetic ganglia. Cell Tissue Res 1993:271:115-121.
13. Vizzard MA. Erdman SL. dc Groat WC: Localization of NADPH-diaphorase in bladder afferent and postganglionic efferent neurons of the rat. J Auton Nerv Syst 1993;44:85-90.
14. Vizzard MA. Erdman SL. Fôrstermann U, dc Groat WC: Differential distribution of nitric oxide synthase in neural pathways to the urogenital organs (urethra, penis, urinary bladder) of the rat. Brain Res 1994:646:279-291.
15. Vizzard MA. Erdman SL. Roppolo JR. Fôrstermann U, dc Groat WC: Differential localization of neuronal nitric oxide synthase immuno-rcactivity and NADPH-diaphorase activity in the cat spinal cord. Cell Tissue Res 1994:278: 299-309.
16. Vizzard MA. Erdman SL. Erickson VL. Stewart RJ. Roppolo JR. dc Groat WC: Localization of NADPH-diaphorasc in the lumbosacral spinal cord and dorsal root ganglia of the cal. J Comp Neurol 1994:339:62-75.
17. Aimi Y. Fujimura M, Vincent SR, Kimura I: Localization of NADPH-diaphorase containing neurons in sensory ganglia of the rat. J Comp Neurol 1991:306:382-392.
18. Vizzard MA. Erdman SL. dc Groat WC: The effect of rhizotomy on NADPH-diaphorase staining in the lumbar spinal cord of the rat. Brain Res 1993:607:349-353.
19. Nadelhaft I. Booth AM: The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: A horseradish peroxidase study. J Comp Neurol 1984:226:238-245.
20. Steers WD. Ciantbolti J. Etzel B. Erdman S, de Groat WC: Alterations in afferent pathways from the urinary bladder of the rat in response to partial urethral obstruction. J Comp Neurol 1991;310:1-10.
21. Kawatani M. Lowe I. Nadelhaft I. Morgan C. de Groat WC: Vasoactive intestinal polypeptide in visceral afferent pathways to the sacral cord of the cat. Neurosci Lett 1983:42:311-316.
22. Kawatani M, Erdman SL. dc Groat WC: Vasoactive intestinal polypeptide and substance P in primary afferent pathways to the sacral spinal cord of the cat. J Comp Neurol 1985:241: 327-347.
23. Honda CN, Rcthelyi M, Pctrusz P: Preferential immunohistochemical localization of vasoactive intestinal polypeptide in the sacral spinal cord of the cat: Light and electron microscopic observations. J Ncurosci 1983:3:2183-2196.
24. Basbaum AI. Glazer EJ: Immunoreactivc vasoactive intestinal polypeptide is concentrated in the sacral spinal cord: A possible marker for pelvic visceral afferent fibers. Somatoscns Res 1983:1:69-82.
25. Ruda MA. Besse D. lnagaki S. DeLeon M. Ren K: Nitric oxide expression and regulation in the dorsal root ganglion and spinal cord; in Chiuch CC. Gilbert DL. Colton CA (eds): The Neurobiology of NO and OH. New York. New York Academy of Sciences. 1994, pp 181-200.
26. Verge VMK. Zhang X. Xu X-J. Wicscnfcld-Hallin Z, Hôkfelt T: Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: In situ hybridization and functional studies. Proc Natl Acad Sci USA 1992:89:11617-11621.
27. Zhang X. Verge V. Wicscnfeld-Hallin Z. Ju G. Bredt D. Snyder SH. Hokfell T: Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J Comp Neurol 1993;335:563-575.
28. Vizzard MA, Erdman SL. dc Groat WC: Increased expression of neuronal nitric oxide synthase in dorsal root ganglion neurons after systemic capsaicin administration. Neuroscience 1995:67:1-5.
29. Vizzard MA. Erdman SL. dc Groat WC: Increased expression of neuronal nitric oxide synthase in bladder afferent pathways following chronic bladder irritation. J Comp Neurol 1996:370:191-202.
30. Gonzalez MF. Sharp FR. Sagar SM: Axotomy increases NADPH-diaphorase staining in rat vagal motor neurons. Brain Res Bull 1987,18: 417-427.
31. Wu W. Liuzzi FJ. Sehinco FP. Deplo AS. Li Y. Mong JA. Dawson TM. Snyder SH: Neuronal nitric oxide synthase is induced in spinal neurons by traumatic injury. Neuroscience 1994: 61:719-726.
32. Cord JP. Iskandar E. Enquist LW: Inducible expression of nitric oxide synthase in virally infected neurons. Soc Ncurosci Abstr 1995:21: 775.
33. Sharma HS, Westman J. Olsson Y. Aim P: Involvement of nitric oxide in acute spinal cord injury: An immunocylochcmical study using light and electron microscopy in the rat. Neurosci Res 1996;24:373-384.
34. Guizar-Sagagun G. Garcia-Lopez P. Espitia AL. Mendez S. Castaneda-Hemandez G. Ma-drazo I, Franco-Bourlan RE: Histochemical evidence of the increased expression of nicotinamide adenine dinucleotide phosphate-dependent diaphorasc in neurons of the myenteric plexus after acute spinal cord injury in adult rats. Neurosci Lett 1996:206:185-188.
35. de Groat WC. Booth AM. Yoshimura N: Neurophysiology of micturition and its modification in animal models of human disease: in Maggi CA (ed): The Autonomic Nervous System. Nervous Control of the Urogenital System. London. Harwood Academic Publishers. 1993. vol 3. pp 227-290.
36. de Groat WC. Kruse MN: Central processing and morphological plasticity in lumbosacral afferent pathways from the lower urinary tract: in Mayer EA. Raybould HE (eds): Basic and Clinical Aspects of Chronic Abdominal Pain. Pain Research and Clinical Management. Amsterdam. Elsevier Science Publishers. 1993. vol 9. pp 219-235.
37. Kuru M: Nervous control of micturition. Physiol Rev 1965:45:425-494.
38. Torrens M. Morrison JFB: The Physiology of the Lower Urinary Tract. Berlin. Springer. 1987.
39. Kruse MN, de Groat WC: Micturition reflexes in decerebrate and spinalized neonatal rats. Am J Physiol 1990;25S:R1508-R1511.
40. Kruse MN. dc Groat WC: Changes in lower urinary tract function follow ing spinal cord injury. J Restor Neurol Neurosci 1993:5:79-80.
41. Kruse MN, de Groat WC: Consequences of spinal cord injury during the neonatal period on micturition reflexes in the rat. Exp Neurol 1994;125:87-92.
42. Kruse MN. Belton AL, de Groat WC: Changes in bladder and external urethral sphincter function following spinal cord injury in the rat. Am J Physiol 1993;264:RI 157-RI163.
43. Levine LA. Richie JP: Urological complications of cyclophosphamide. J Urol 1989:141: 1063-1069.
44. Pétrone RL, Agha AH, Roy JB. Hurst RE: Uro-dynamic findings in patients with interstitial cystitis. J Urol 1995:153:290A.
45. Kruse MN. Bray LA. dc Groat WC: Influence of spinal cord injury on the morphology of bladder afferent and efferent neurons. J Auton Nerv Syst 1995:54:215-224.
46. Donovan MK, Wintemilz SR, Wyss JM: An analysis of the sensory innervation of the urinary system of the rat. Brain Res Bull 1983; 11: 321-324.
47. Keast JR. de Groat WC: Segmental distribution and peptide content of primary allèrent neurons innervating the urogenital organs and colon of male rats. J Comp Neurol 1992:319: 615-623.
48. Su HC. Polak JM. Mulderry PK, Ghatei MA, Gibson SJ. Terenghi G, Morrison JFB, Ballesta J. Bloom SR: Calcitonin gene-related peptide immunoreactivity in afferent neurons supplying the urinary tract: Combined retrograde tracing and immunohistochemistry. Neuroscience 1986; 18:727-747.
49. de Groat WC, Kawalani M, Hisamitsu T, Booth AM. Roppolo JR. Thor K, Tuttle P. Nagel J: Neural control of micturition: The role of neuropeptides. J Auton Nerv Syst 1986; (suppl):369-387.
50. de Groat WC. Ryall RW: Reflexes to sacral parasympathetic neurones concerned with micturition in the cat. J Physiol (Lond) 1969; 200:87-108.
51. de Groat WC: Nervous control of the urinary bladder of the cat. Brain Res 1975:87:201-211.
52. McGuire EJ. Brady S: Detrusor-sphincter dys-synergia. J Urol 1979:121:774-777.
53. Morrison JFB: Reflex control of the lower urinary tract; in Torrens M. Morrison JFB (cds): The Physiology of the Lower Urinary Tract. New York. Springer. 1987.
54. Wyndaclc JJ: Urethral sphincter dyssynergia in spinal cord injury patients. Paraplegia 1987;25: 10-15.
55. Yoshimura N, de Groat WC: Plasticity of sodium and potassium channels in rat bladder afferent neurons following spinal cord injury or partial urethral obstruction. Soc Ncurosci Abstr 1993:19:1762.
56. Yoshimura N, de Groat WC: Changes in elec-trophysiological and pharmacological properties of rat bladder afferent neurons following spinal cord injury. J Urol 1993;149:340A.
57. de Groat WC, Kawatani M, Hisamitsu T, Cheng C-L, Ma C-P, Thor K, Steers W, Roppolo JR: Mechanisms underlying the recovery of urinary bladder function following spinal cord injury. J Auton Nerv Syst 1990;30:571-578.
58. Fall M, Lindstrom S. Mazieres L: A bladder-to-bladder cooling reflex in the cat. J Physiol 1990:427:281-300.
59. de Groat WC, Nadelhaft I, Milne RJ. Booth AM, Morgan C. Thor K: Organization of the sacral parasympathetic reflex pathways to the urinary bladder and large intestine. J Auton Nerv Syst 1981:3:135-160.
60. Mallory B, Steers WD, de Groat WC: Electro-physiological study of micturition reflexes in rats. Am J Physiol 1989;257:R410-R421.
61. Maggi CA: The dual function of capsaicin-sensitive sensory' nerves in the bladder and urethra; in Maggi CA (ed): The Autonomic Nervous System. Nervous Control of the Urogenital System. London, Harwood Academic Publishers, 1992, vol 2.
62. Maggi CA, Meli A: The role of neuropeptides in the regulation of the micturition reflex. J Auton Pharmacol 1986;6:133-162.
63. Steers WD. Kolbeck S, Creedon D. Tuttle JB: Nerve growth factor in urinary bladder of the adult rat regulates neuronal form and function. J Clin Invest 1991;88:1709-1715.
64. Steers WD, de Groat WC: Effect of bladder outlet obstruction on micturition reflex pathways in the rat. J Urol 1988:140:864-871.
65. Vizzard MA, Erickson VL, Card JP, Roppolo JR, de Groat WC: Transncuronal labeling of neurons in the adult rat brainstem and spinal cord after injection of pseudorabics virus into the urethra. J Comp Neurol 1995:355:629-640.
66. Bscheidl C, Hanesch U, Heppelmann B: NADPH-diaphorase reactivity in articular af-ferents of a normal and inflamed knee joint in thecal. Brain Res 1994;668:266-270.
67. Yu W-H A: Nitric oxide synthase in motor neurons after axotomy. J Histochem Cytochem 1994;42:451-457.
68. de Groat WC, Yoshimura N, Roppolo JR, Erd-man SL, Erickson VL, Yu YB, Card JP, Vizzard MA: Identification of bladder preganglionic and intemeurons in the L6-S1 spinal cord of the adult rat using pseudorabies and fluorogold dye tracing techniques. Soc Neuro-sci Abstr 1994;20:114.
69. Birder LA, Roppolo JR, de Groat WC: C-fos as a marker for subsets of visceral second-order neurons in the rat lumbosacral spinal cord. Soc Neurosci Abstr 1990; 16:703.
70. McNeill D, Papka RE, Hamilton MO, O’Don-oghue DL, Mayer B: Relationship of nitric oxide synthase to L6/S1 spinal neurons that project to the pontine micturition center in the rat. Soc Neurosci Abstr 1993; 19:509.
71. Bakhit C, Armanini M, Wong WLT, Bcnnet GL, Wrathall JR: Increase in nerve growth factor-like immunoreactivity and decrease in choline acetyltransferase following contusive spinal cord injury'. Brain Res 1991;554:264-271.
72. Roisen F, Lu CL, Johnson JR. Linden RD, Niznik G, Ray L, Shields CB, Wang L-J. Yorke G, Zhang YP: Spinal injury alters circulating neurotrophic activity. Soc Neurosci Abstr 1992; 18:1295.
73. Vantini G, Skaper SD: Neurotrophic factors: From physiology to pharmacology. Pharmacol Res 1992;26:1-15.
74. Oppenheim RW, Prevette D, Qin-Wei Y, Collins R, MacDonald J: Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 1991:251:1616-1618.
75. Unsicker K, Reichert-Prcibsch H, Wewetzer K: Stimulation of neuron survival by basic FGF and CNTF is a direct effect and not mediated by non-neuronal cells: Evidence from single cell cultures. Dev Brain Res 1992;65:285-288.
76. Kakizaki H, de Groat WC: Role of nitric oxide in the facilitation of the micturition reflex by bladder irritation. J Urol 1996;155:355-360.
77. Rice ASC: Topical spinal administration of a nitric oxide synthase inhibitor prevents the hyper-reflexia associated with a rat model of persistent visceral pain. Neurosci Lett 1995; 187:111-114