Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: Possible implications for sensory sprouting

Journal of Comparative Neurology

Volumn 404, Issue 2, 1999, Pages 143-158

  Tong, Yong Guang ^a   Wang, H Fredrik ^b   Ju, Gong ^a   Grant, Gunnar ^b   Hökfelt, Tomas ^b   Zhang, Xu ^a,b  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

DRG; GM1 monoganglioside; Nerve injury; Pain; Plasticity; Spinal cord

Indexed keywords

CHOLERA TOXIN B SUBUNIT; GANGLIOSIDE GM1; HORSERADISH PEROXIDASE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; HISTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MACACA; MALE; NERVE CELL PLASTICITY; NERVE FIBER TRANSECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; SPINAL CORD; SPINAL GANGLION;

EID: 0033535120     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19990208)404:2<143::aid-cne1>3.0.co;2-%23     Document Type: Article

References (90)

1. Aldskogius H, Wiesenfeld-Hallin Z, Kristenson K. 1988. Selective neuronal destruction by Ricinus communis agglutinin I and its use for the quantitative determination of sciatic nerve dorsal root ganglion cell numbers. Brain Res 461:215-220.
2. Arnér S, Meyerson BA. 1988. Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain 33:11-23.
3. Arnér S, Meyerson BA. 1993. Opioids in neuropathic pain. Pain Digest 3:15-22.
4. Barletta E, Bremer EG, Culp LA. 1991. Neurite outgrowth in dorsal root neuronal hybrid clones modulated by ganglioside GM1 and disintegrins. Exp Cell Res 193:101-111.
5. Bennett DLH, French J, Priestley JV, McMahon SB. 1996. NGF but not NT-3 or BDNF prevents the A fiber sprouting into lamina II of the spinal cord that occurs following axotomy. Mol Cell Neurosci 8:211-220.
6. Besse D, Lombard MC, Perrot S, Besson JM. 1992a. Regulation of opioid binding sites in the superficial dorsal horn of the rat spinal cord following loose ligation of the sciatic nerve: comparison with sciatic nerve section and lumbar dorsal rhizotomy. Neuroscience 50:921-933.
7. Besse D, Weil-Fugazza J, Lombard MC, Butler SH, Besson JM. 1992b. Monoarthritis induces complex changes in μ-, δ-, and κ-opioid binding sites in the superficial dorsal horn of the rat spinal cord. Eur J Pharmacol 223:123-131.
8. Cannella MS, Oderfeld-Nowak B, Gradkowska M, Skup M, Garofalo L, Cuello AC, Ledeen RW. 1990. Derivatives of ganglioside GM1 as neuronotrophic agents: comparison of in vivo and in vitro effects. Brain Res 513:286-294.
9. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364:6-15.
10. Coggeshall RE, Lekan HA, Doubell TP, Allchorne A, Woolf CJ. 1997. Central changes in primary afferent fibers following peripheral nerve lesions. Neuroscience 77:1115-1122.
11. Crain SM, Shen K-F. 1992a. After chronic opioid exposure sensory neurons become supersensitive to the excitatory effects of opioid agonists and antagonists as occurs after acute elevation of GM1 ganglioside. Brain Res 575:13-24.
12. Crain SM, Shen K-F. 1992b. After GM1 ganglioside treatment of sensory neurons naloxone paradoxically prolongs the action potential but still antagonizes opioid inhibition. J Pharmacol Exp Ther 200:182-186.
13. Crain SM, Shen K-F. 1996. Etorphine elicits anomalous excitatory opioid effect on sensory neurons treated with GM1 ganglioside or pertussis toxin in contrast to its potent inhibitory effects on naive or chronic morphine-treated cells. Brain Res 741:275-283.
14. Cuatrecacas P. 1973. Gangliosides and membrane receptors for cholera toxin. Biochemistry 12:3558-3566.
15. Devor M, Govrin-Lippman R, Frank I, Raper P. 1985. Proliferation of primary sensory neurons in adult rat dorsal root ganglion and the kinetics of retrograde cell loss after sciatic nerve section. Somatosens Res 3:139-167.
16. M1 antibodies and B-cholera toxin bind specifically to embryonic chick dorsal root ganglion neurons but do not modulate neurite regeneration. J. Neurochem. 48:1237-1244.
17. 1 does not initiate, but enhances neurite regeneration of nerve growth factor-dependent sensory neurones. J Neurochem 44:1259-1265.
18. Doubell TP, Woolf CJ. 1997. Growth-associated protein 43 immunoreactivity in the superficial dorsal horn of the rat spinal cord is localized in atrophic C-fiber, and not in sprouted A-fiber, central terminals after peripheral nerve injury. J Comp Neurol 386:111-118.
19. Doubell TP, Mannion RJ, Woolf CJ. 1997. Intact sciatic myelinated primary afferent terminals collaterally sprout in the adult rat dorsal horn following section of a neighbouring peripheral nerve. J Comp Neurol 380:95-104.
20. Dray A, Urban L, Dickenson A. 1994. Pharmacology of chronic pain. TIPS 15:190-197.
21. Dumas M, Schwab ME, Thoenen H. 1979. Retrograde axonal transport of specific macromolecules as a tool for characterizing nerve terminal membranes. J Neurobiol 10:179-197.
22. Eriksson NP, Aldskogius H, Grant G, Lindsay RM, Rivero-Melián C. 1997. Effects of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 on the laminar distribution of transganglionically transported choleragenoid in the spinal cord dorsal horn following transection of the sciatic nerve in the adult rat. Neuroscience 78:863-872.
23. Fields HL, Emson PC, Leigh BK, Gilbert RF, Iversen LL. 1980. Multiple opiate receptors on primary afferent fibers. Nature 284:351-353.
24. Florence SL, Garraghty PE, Carlson M, Kaas JH. 1993. Sprouting of peripheral nerve axons in the spinal cord of monkeys. Brain Res 601:343-348.
25. Grant G. 1993. Projection patterns of primary sensory neurons studied by transganglionic methods: somatotopy and target-related organization. Brain Res Bull 30:199-208.
26. Grant G. 1995. Primary afferent projections to the spinal cord. In: Paxinos G, editor. The rat nervous system. New York: Academic Press. p 61-66.
27. Guillery RW, Herrup K. 1997. Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386:2-7.
28. Gundersen HJG, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263.
29. 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. J Comp Neurol 284:215-230.
30. Holmgren J, Lönnroth I, Svennerholm L. 1973. Tissue receptor for cholera exotoxin: postulated structure from studies with GM1 ganglioside and related glycolipids. Infect Immun 8:889-890.
31. Hökfelt T, Zhang X, Wiesenfeld-Hallin Z. 1994. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. TINS 17:22-30.
32. Hökfelt T, Zhang X, Xu Z-Q, Ji R-R, Shi T, Corness J, Kerekes N, Landry M, Holmberg K, Broberger C. 1997. Phenotype regulation in dorsal root ganglion neurons after nerve injury: focus on peptides and their receptors. In: Borsook D, editor. Molecular neurobiology of pain. Seattle: IASP Press. p 115-143.
33. Hsu S-M, Raind L, Fanger H. 1981. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase technique: a comparison between ABC and unlabelled antibody (PAP) procedures. J Histochem Cytochem 29:577-580.
34. 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.
35. Johnson DG, de C Nougueira Araujo GM. 1981. A simple method of reducing the fading of immunofluorescence during microscopy. J Immunol Methods 43:349-350.
36. King CA, van Heyningen WE. 1973. Deactivation of cholera toxin by sialidase-resistant monosialosylganglioside. J Infect Dis 127:639-647.
37. Knyihár-Csillik E, Csillik B. 1981. FRAP: histochemistry of the primary nociceptive neuron. New York: Fischer.
38. Koerber HR, Mirnics K, Brown PB, Mendell LM. 1994. Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 14:3655-3671.
39. Kupers RC, Konings H, Adriensen H, Gybels JM. 1991. Morphine differentially affects the sensory and affective pain ratings in neurogenic and idiopathic forms of pain. Pain 47:5-12.
40. LaMotte CC, Kapadia SE, Shapiro CM. 1991. Central projections of the sciatic, saphenous, median, and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and wheat germ agglutinin-HRP (WGA-HRP). J Comp Neurol 311:546-562.
41. Lekan HA, Carlton SM, Coggeshall RE. 1996. Sprouting of A beta fibers into lamina II of the rat dorsal horn in peripheral neuropathy. Neurosci Lett 208:147-150.
42. Lindh B, Aldskogius H, Hökfelt T. 1989. Simultaneous immunohistochemical demonstration of intra-axonally transported markers and neuropeptides in the peripheral nervous system of the guinea pig. Histochemistry 92:367-376.
43. Lombard MC, Besse D, Chen YL, Besson JM. 1990. Mu-opioid receptors in the superficial spinal dorsal horn in an experimental model of peripheral mononeuropathy in the rat. Eur J Pharmacol 181:2308.
44. Mannion RJ, Doubell TP, Coggeshall RE, Woolf CJ. 1996. Collateral sprouting of uninjured primary afferent A-fibers into the superficial dorsal horn of the adult rat spinal cord after topical capsaicin treatment to the sciatic nerve. J Neurosci 16:5189-5195.
45. Mannion RJ, Boubell TP, Gill H, Woolf CJ. 1998. Deafferentation is insufficient to induce sprouting of A-fibre central terminals in the rat dorsal horn. J Comp Neurol 393:135-144.
46. Maxwell DJ, Réthelyi M. 1987. Ultrastructure and synaptic connections of cutaneous afferent fibres in the spinal cord. TINS 10:117-123.
47. Mesulam M-M, Brushart TM. 1979. Transganglionic and anterograde transport of horseradish peroxidase across dorsal root ganglia: a tetramethylbenzidine method for tracing central sensory connections of muscles and peripheral nerves. J Histochem Cytochem 28:1107-1117.
48. Milani D, Minozzi M-C, Petrelli L, Guidolin D, Skaper SD, Spoerri PE. 1992. Interaction of ganglioside GM1 with the B subunit of cholera toxin modulates intracellular free calcium in sensory neurons. J Neurosci Res 33:466-475.
49. Molander C, Grant G. 1985. Cutaneous projections from the rat hindlimb foot to the substantia gelatinosa of the spinal cord studied by transganglionic transport of WGA-HRP conjugate. J Comp Neurol 237:476-484.
50. Molander C, Wang HF, Rivero-Melián C, Grant G. 1996. Early decline and late restoration of spinal cord binding and transganglionic transport of isolectin B4 from Griffonia simplicifolia I after peripheral nerve transection or crush. Rest Neurol Neurosci 10:123-133.
51. Platt JL, Michael AF. 1983. Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J Histochem Cytochem 31:840-842.
52. Popken GJ, Farel PB. 1997. Sensory neuron number in neonatal and adult rats estimated by means of stereologic and profile-based methods. J Comp Neurol 386:8-15.
53. Réthelyi M. 1977. Preterminal and terminal axon arborization in the substantia gelatinosa of cat's spinal cord. J Comp Neurol 172:511-528.
54. Rivero-Melián C. 1993. The spinal cord projections of dorsal roots and peripheral nerves and their overlap: a neuroanatomical study in the rat. Thesis, Karolinska Institutet, Stockholm, Sweden.
55. Rivero-Melián C, Grant G. 1990a. Distribution of lumbar dorsal root fibers in the lower thoracic and lumbosacral spinal cord of the rat studied with choleragenoid horseradish peroxidase conjugate. J Comp Neurol 299: 470-481.
56. Rivero-Melián C, Grant G. 1990b. Lumbar dorsal root projections to spinocerebellar cell groups in the rat spinal cord: a double labeling study. Exp Brain Res 81:85-94.
57. Rivero-Melián C, Grant G. 1991. Choleragenoid horseradish peroxidase used for studying projections of some hindlimb cutaneous nerves and plantar foot afferents to the dorsal horn and Clarke's column in the rat. Exp Brain Res 84:125-132.
58. Rivero-Melián C, Rosario C, Grant G. 1992. Demonstration of transganglionically transported choleragenoid in rat spinal cord by immunofluorescence cytochemistry. Neurosci Lett 14:114-117.
59. Robertson B, Grant G. 1985. A comparison between wheat germ agglutinin-and choleragenoid-horseradish peroxidase as anterogradely transported markers in central branches of primary sensory neurones in the rat with some observations in the cat. Neuroscience 14:895-905.
60. Saper CB. 1996. Any way you cut it: a new journal policy for the use of unbiased counting methods. J Comp Neurol 364:5.
61. Sbaschnig-Agler M, Ledeen RW, Grafstein B, Alpert RM. 1984. Ganglioside changes in the regenerating goldfish optic system: comparison with glycoproteins and phospholipids. J Neurosci Res 12:221-232.
62. s-linked opioid receptor functions. Brain Res 531:1-7.
63. Shen K-F, Crain SM, Ledeen RW. 1991. Brief treatment of sensory ganglion neurons with GM1 ganglioside enhances the efficacy of opioid excitatory effects on the action potential. Brain Res 559:130-138.
64. Silverman JD, Kruger L. 1988. Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated "nociceptor" thin axons in rat testis and cornea whole-mount preparations. Somatosens Res 5:259-267.
65. Silverman JD, Kruger L. 1990. Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J Neurocytol 19:789-801.
66. Sparrow JR, McGuinness C, Schwartz M, Grafstein B. 1984. Antibodies to gangliosides inhibit goldfish optic nerve regeneration in vivo. J Neurosci Res 12:233-243.
67. Stevens CW, Kajander KC, Bennett GJ, Seybold VS. 1991a. Bilateral and differential changes in spinal mu, delta, and kappa opioid binding in rats with a painful, unilateral neuropathy. Pain 46:315-326.
68. Stevens CW, Lacey CB, Miller KE, Elde RP, Seybold VS. 1991b. Biochemical characterization and regional quantification of μ, δ and κ opioid binding sites in rat spinal cord. Brain Res 550:77-85.
69. Stoeckel K, Schwab M, Thoenen H. 1977. Role of gangliosides in the uptake and retrograde transport of cholera and tetanus toxin as compared to nerve growth factor and wheat germ agglutinin. Brain Res 132:273-285.
70. Streit WJ, Schulte BA, Balentine JD, Spicer SS. 1985. Histochemical localization of galactose-containing glycoconjugates in sensory neurons and their processes in the central and peripheral nervous system of the rat. J Histochem Cytochem 33:1042-1052.
71. Streit WJ, Schulte BA, Balentine JD, Spicer SS. 1986. Evidence for glycoconjugate in nociceptive primary sensory neurons and its origin from the Golgi complex. Brain Res 377:1-17.
72. Tasker RR, Tsuda T, Hawrylyshyn P. 1983. Clinical neurophysiological investigation of deafferentation pain. In: Bonica JJ, Lindblom U, Iggo A, editors. Advances in pain research and therapy. New York: Raven Press. p 713-738.
73. Trojanowski JQ, Gonatas JO, Gonatas NK. 1981. Conjugates of horseradish peroxidase (HRP) conjugates with cholera toxin and wheat germ agglutinin are superior to free HRP as retrogradely transported markers. Brain Res 231:33-50.
74. Trojanowski JQ, Gonatas JO, Gonatas NK. 1982. Horseradish peroxidase (HRP) conjugates of cholera toxin and lectins are more sensitive retrogradely transported markers than free HRP. Brain Res 231:33-50.
75. Verge VMK, Wiesenfeld-Hallin Z, Hökfelt T. 1993. Cholecystokinin in mammalian primary sensory neurons and spinal cord: in situ hybridization studies in rat and monkey. Eur J Neurosci 5:240-250.
76. Wan X-CS, Trojanowksi JQ, Gonatas JO. 1982a. Cholera toxin and wheat germ agglutinin conjugates as neuroanatomical probes: their uptake and clearance, transganglionic and retrograde transport and sensitivity. Brain Res 243:215-224.
77. Wan XST, Trojanowski JQ, Gonatas JO, Liu CN. 1982b. Cytoarchitecture of the extranuclear and commissural dendrites and hypoglossal nucleus neurons as revealed by conjugates of horseradish peroxidase with cholera toxin. Exp Neurol 78:167-175.
78. Wang H, Rivero-Melián C, Robertson B, Grant G. 1994. Transganglionic transport and binding of the isolectin B4 from Griffonia simplicifolia I in rat primary sensory neurons. Neuroscience 62:536-551.
79. Willis WD Jr, Coggeshall RE. 1991. Sensory mechanisms of the spinal cord. New York and London: Plenum Press.
80. Woolf CJ. 1997. Molecular signals responsible for the reorganization of the synaptic circuitry of the dorsal horn after peripheral nerve injury: the mechanisms of tactile allodynia. In: Borsook D, editor. Molecular neurobiology of pain. Seattle: IASP Press. p 171-200.
81. Woolf CJ, Doubell TP. 1994. The pathophysiology of chronic pain: increased sensitivity to low threshold Aβ-fibre inputs. Curr Opion Neurobiol 4:525-534.
82. Woolf CJ, Shortland P, Coggeshall RE. 1992. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355:75-79.
83. Woolf CJ, Shortland P, Reynolds M, Ridings J, Doubell T, Coggeshall RE. 1995. Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J Comp Neurol 360:121-134.
84. Wu G, Lu Z-H, Alfinito P, Ledeen RW. 1997a. Opioid receptor and calcium channel regulation of adenylyl cyclase, modulated by GM1, in NG108-15 cells: competitive interactions. Neurochem Res 22:1281-1289.
85. Wu G, Lu Z-H, Ledeen RW. 1997b. Interaction of the δ-opioid receptor with GM1 ganglioside: conversion from inhibitory to excitatory mode. Mol Brain Res 44:341-346.
86. Ygge J, Grant G. 1983. The organization of the thoracic spinal nerve projection in the rat dorsal horn demonstrated with transganglionic transport of horseradish peroxidase. J Comp Neurol 216:1-9.
87. Zhang X, Dagerlind Å, Elde RP, Castel M-N, Broberger C, Wiesenfeld-Hallin Z, Hökfelt T. 1993a. Marked increase in cholecystokinin B receptor messenger RNA levels in rat dorsal root ganglia after peripheral axotomy. Neuroscience 57:227-233.
88. Zhang X, Ju G, Elde R, Hökfelt T. 1993b. Effect of peripheral nerve cut on neuropeptides in dorsal root ganglia and the spinal cord of monkey with special reference to galanin. J Neurocytol 22:342-381.
89. Zhang X, Bao L, Shi T-J, Ju G, Elde R, Hökfelt T. 1998. Downregulation of μ-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy. Neuroscience 82:223-240.
90. Zigmond RE, Hyatt-Sachs H, Mohney RP, Schreiber RC, Shadiack AM, Sun Y, Vaccariello SA. 1996. Changes in neuropeptide phenotype after axotomy of adult peripheral neurons and the role of leukemia inhibitor factor. Perspect Dev Neurobiol 4:75-90.