Augmented sodium currents contribute to the enhanced excitability of small diameter capsaicin-sensitive sensory neurons isolated from Nf1+/- mice

Journal of Neurophysiology

Volumn 103, Issue 4, 2010, Pages 2085-2094

  Wang, Yue ^a   Duan, J H ^a   Hingtgen, C M ^a,b   Nicol, G D ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; NEUROFIBROMIN; TETRODOTOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; ISOLATION PROCEDURE; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE; NERVE POTENTIAL; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; SENSORY NERVE CELL; SODIUM CURRENT; STEADY STATE;

ACTION POTENTIALS; ANIMALS; CAPSAICIN; DISEASE MODELS, ANIMAL; GUANOSINE TRIPHOSPHATE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; POTASSIUM CHANNELS; PROTO-ONCOGENE PROTEINS P21(RAS); SENSORY RECEPTOR CELLS; SENSORY SYSTEM AGENTS; SODIUM CHANNELS; TETRODOTOXIN;

EID: 77951215603     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01010.2009     Document Type: Article

References (66)

1. Aman TK, Grieco-Calub TM, Chen C, Rusconi R, Slat EA, Isom LL, Raman IM. Regulation of persistent Na current by interactions between beta subunits of voltage-gated Na channels. J Neurosci 29: 2027-2042, 2009.
2. Baker MD, Bostock H. Low-threshold, persistent sodium current in rat large dorsal root ganglion neurons in culture. J Neurophysiol 77: 1503-1513, 1997. (Pubitemid 27137043)
3. 2+ current in the action potentials of nociceptive sensory neurons. J Neurosci 22: 10277-10290, 2002.
4. + current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 23: 10338-10350, 2003.
5. Caffrey JM, Eng DL, Black JA, Waxman SG, Kocsis JD. Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res 592: 283-297, 1992.
6. + channel in vertebrate sensory neurons. Pfluegers 423: 492-496, 1993.
7. + conductance in medium-sized neostriatal neurons: characterization using infrared videomicroscopy and whole cell patch-clamp recordings. J Neurophysiol 74: 1343-1348, 1995.
8. Connor JA, Stevens CF. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol 213: 21-30, 1971.
9. Creange A, Zeller J, Rostaing-Rigattieri S, Brugieres P, Degos JD, Revuz J, Wolkenstein P. Neurological complications of neurofibromatosis type 1 in adulthood. Brain 122: 473-481, 1999. (Pubitemid 29110522)
10. Crill WE. Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58: 349-362, 1996. (Pubitemid 26106725)
11. Cummins TR, Waxman SG. Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury. J Neurosci 17: 3503-3514, 1997.
12. Dasgupta B, Dugan LL, Gutmann DH. The neurofibromatosis 1 gene product neurofibromin regulates pituitary adenylate cyclase-activating polypeptide-mediated signaling in astrocytes. J Neurosci 23: 8949-8954, 2003. (Pubitemid 37210908)
13. Daston MM, Scrable H, Nordlund M, Sturbaum AK, Nissen LM, Ratner N. The protein product of the neurofibromatosis type 1 gene is expressed at highest abundance in neurons, Schwann cells, and oligodendrocytes. Neuron 8: 415-428, 1992.
14. Do MT, Bean BP. Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39: 109-120, 2003.
15. Dugan LL, Kim JS, Zhang Y, Bart RD, Sun Y, Holtzman DM, Gutmann DH. Differential effects of cAMP in neurons and astrocytes. Role of B-raf. J Biol Chem 274: 25842-25848, 1999. (Pubitemid 129530763)
16. Elliott AA, Elliott JR. Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J Physiol 463: 39-56, 1993.
17. 2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase A cascade. J Physiol 495: 429-440, 1996.
18. Evans AR, Vasko MR, Nicol GD. The cAMP transduction cascade mediates the PGE2-induced inhibition of potassium currents in rat sensory neurons. J Physiol 516: 163-178, 1999.
19. Fieber LA. Ionic currents in normal and neurofibromatosis type 1-affected human Schwann cells, induction of tumor cell K current in normal Schwann cells by cyclic AMP. J Neurosci Res 54: 495-506, 1998.
20. Fitzgerald EM, Dolphin AC. Regulation of rat neuronal voltage-dependent calcium channels by endogenous p21-ras. Eur J Neurosci 9: 1252-1261, 1997.
21. French CR, Sah P, Buckett KJ, Gage PW. A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J Gen Physiol 95: 1139-1157, 1990. (Pubitemid 20217307)
22. Friedman JM. Epidemiology of neurofibromatosis type 1. Am J Med Genet 89: 1-6, 1999.
23. Ginty DD, Fanger GR, Wagner JA, Maue RA. The activity of cAMP-dependent protein kinase is required at a posttranslational level for induction of voltage-dependent sodium channels by peptide growth factors in PC12 cells. J Cell Biol 116: 1465-1473, 1992.
24. + current in nociceptors. Proc Natl Acad Sci USA 93: 1108-1112, 1996.
25. Na in rat colonic sensory neurons. J Neurophysiol 88: 1512-1522, 2002.
26. Guha A, Lau N, Huvar I, Gutmann D, Provias J, Pawson T, Boss G. Ras-GTP levels are elevated in human NF1 peripheral nerve tumors. Oncogene 12: 507-513, 1996. (Pubitemid 26059644)
27. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers 391: 85-100, 1981. (Pubitemid 11012976)
28. + current affects resting potential and response to depolarization in simulated spinal sensory neurons. J Neurophysiol 86: 1351-1364, 2001.
29. Higuchi H, Yamashita T, Yoshikawa H, Tohyama M. PKA phosphorylates the p75 receptor and regulates its localization to lipid rafts. EMBO J 22: 1790 - 1800, 2003.
30. Holzer P. Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol Rev 43: 143-201, 1991.
31. Ingram DA, Hiatt K, King AJ, Fisher L, Shivakumar R, Derstine C, Wenning MJ, Diaz B, Travers JB, Hood A, Marshall M, Williams DA, Clapp DW. Hyperactivation of p21(ras) and the hematopoietic-specific Rho GTPase, Rac2, cooperate to alter the proliferation of neurofibromin-deficient mast cells in vivo and in vitro. J Exp Med 194: 57-69, 2001.
32. Jacks T, Shih TS, Schmitt EM, Bronson RT, Bernards A, Weinberg RA. Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat Genet 7: 353-361, 1994.
33. Jeftinija S. Bradykinin excites tetrodotoxin-resistant primary afferent fibers. Brain Res 665: 69-76, 1994.
34. Jin X, Gereau RW 4th. Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J Neurosci 26: 246-255, 2006.
35. Kiernan MC, Baker MD, Bostock H. Characteristics of late Na(+) current in adult rat small sensory neurons. Neuroscience 119: 653-660, 2003.
36. Kim HA, Ratner N, Roberts TM, Stiles CD. Schwann cell proliferative responses to cAMP and Nf1 are mediated by cyclin D1. J Neurosci 21: 1110-1116, 2001.
37. Klesse LJ, Parada LF. p21 ras and phosphatidylinositol-3 kinase are required for survival of wild-type and NF1 mutant sensory neurons. J Neurosci 18: 10420-10428, 1998.
38. 3 responses in PC12 cells. Different pathways. FEBS Lett 324: 147-152, 1993.
39. Lindsay RM. Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J Neurosci 8: 2394-2405, 1988.
40. Neher E. Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol 58: 36-53, 1971.
41. Nicol GD, Vasko MR, Evans AR. Prostaglandins suppress an outward potassium current in embryonic rat sensory neurons. J Neurophysiol 77: 167-176, 1997.
42. North KN, Riccardi V, Samango-Sprouse C, Ferner R, Moore B, Legius E, Ratner N, Denckla MB. Cognitive function and academic performance in neurofibromatosis 1: consensus statement from the NF1 Cognitive Disorders Task Force. Neurology 48: 1121-1127, 1997.
43. 2+ current in newborn rat dorsal root ganglia. Pfluegers 420: 590-594, 1992.
44. Ozonoff S. Cognitive impairment in neurofibromatosis type 1. Am J Med Genet 89: 45-52, 1999.
45. Petruska JC, Napaporn J, Johnson RD, Gu JG, Cooper BY. Subclassified acutely dissociated cells of rat DRG: histochemistry and patterns of capsaicin-, proton-, and ATP-activated currents. J Neurophysiol 84: 2365-2379, 2000.
46. Qu Y, Curtis R, Lawson D, Gilbride K, Ge P, DiStefano PS, Silos-Santiago I, Catterall WA, Scheuer T. Differential modulation of sodium channel gating and persistent sodium currents by the beta1, beta2, and beta3 subunits. Mol Cell Neurosci 18: 570-580, 2001.
47. Roy ML, Narahashi T. Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J Neurosci 12: 2104-2111, 1992.
48. + current heterogeneity in rat nodose neurons and its impact on neuronal discharge. J Neurophysiol 78: 3198-3209, 1997.
49. Sherman LS, Atit R, Rosenbaum T, Cox AD, Ratner N. Single cell Ras-GTP analysis reveals altered Ras activity in a subpopulation of neuro- fibroma Schwann cells but not fibroblasts. J Biol Chem 275: 30740-30745, 2000.
50. Stafstrom CE, Schwindt PC, Crill WE. Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro. Brain Res 236: 221-226, 1982.
51. Stafstrom CE, Schwindt PC, Flatman JA, Crill WE. Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. J Neurophysiol 52: 244-263, 1984.
52. Stessin AM, Zippin JH, Kamenetsky M, Hess KC, Buck J, Levin LR. Soluble adenylyl cyclase mediates nerve growth factor-induced activation of Rap1. J Biol Chem 281: 17253-17258, 2006.
53. Taddese A, Bean BP. Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron 33: 587-600, 2002.
54. + channel expression increases in dorsal root ganglion neurons in the carrageenan inflammatory pain model. Neuroreport 9: 967-972, 1998.
55. Theiss RD, Kuo JJ, Heckman CJ. Persistent inward currents in rat ventral horn neurons. J Physiol 580: 507-522, 2007.
56. Trovo-Marqui AB, Goloni-Bertollo EM, Valerio NI, Pavarino-Bertelli EC, Muniz MP, Teixeira MF, Antonio JR, Tajara EH. High frequencies of plexiform neurofibromas, mental retardation, learning difficulties, and scoliosis in Brazilian patients with neurofibromatosis type 1. Braz J Med Biol Res 38: 1441-1447, 2005.
57. Vogel KS, El-Afandi M, Parada LF. Neurofibromin negatively regulates neurotrophin signaling through p21ras in embryonic sensory neurons. Mol Cell Neurosci 15: 398-407, 2000.
58. Wang Y, Nicol GD, Clapp DW, Hingtgen CM. Sensory neurons from Nf1 haploinsufficient mice exhibit increased excitability. J Neurophysiol 94: 3670-3676, 2005.
59. Waxman SG, Cummins TR, Dib-Hajj S, Fjell J, Black JA. Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain. Muscle Nerve 22: 1177-1187, 1999.
60. Wolkenstein P, Zeller J, Revuz J, Ecosse E, Leplege A. Quality-of-life impairment in neurofibromatosis type 1: a cross-sectional study of 128 cases. Arch Dermatol 137: 1421-1425, 2001.
61. Wu N, Enomoto A, Tanaka S, Hsiao CF, Nykamp DQ, Izhikevich E, Chandler SH. Persistent sodium currents in mesencephalic v neurons participate in burst generation and control of membrane excitability. J Neurophysiol 93: 2710-2722, 2005.
62. + current in Schwann cells: a protein kinase A-mediated mechanism. J Neurosci 22: 9194-9202, 2002.
63. Zhang YH, Fehrenbacher JC, Vasko MR, Nicol GD. Sphingosine-1-phosphate via activation of a G protein-coupled receptor(s) enhances the excitability of rat sensory neurons. J Neurophysiol 96: 1042-1052, 2006a.
64. + current in rat sensory neurons. J Physiol 544: 385-402, 2002.
65. Zhang YH, Vasko MR, Nicol GD. Intracellular sphingosine 1-phosphate mediates the increased excitability produced by nerve growth factor in rat sensory neurons. J Physiol 575: 101-113, 2006b.
66. Zhou Z, Davar G, Strichartz G. Endothelin-1 (ET-1) selectively enhances the activation gating of slowly inactivating tetrodotoxin-resistant sodium currents in rat sensory neurons: a mechanism for the pain-inducing actions of ET-1. J Neurosci 22: 6325-6330, 2002.