Sensory neurons from Nf1 haploinsufficient mice exhibit increased excitability

Journal of Neurophysiology

Volumn 94, Issue 6, 2005, Pages 3670-3676

  Wang, Yue ^a   Nicol, G D ^a   Clapp, D Wade ^a   Hingtgen, Cynthia M ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATE; NEUROFIBROMIN; RAS GUANOSINE DIPHOSPHATE; RAS GUANOSINE TRIPHOSPHATE; RAS PROTEIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; DEPOLARIZATION; ELECTROPHYSIOLOGY; GENE; GENE MUTATION; GENETIC DISORDER; HETEROZYGOSITY; LATENT PERIOD; MOUSE; NERVE CONDUCTION; NERVE EXCITABILITY; NEUROFIBROMATOSIS; NF1 GENE; NONHUMAN; PAIN; PATCH CLAMP; PRIORITY JOURNAL; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CAPSAICIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; GANGLIA, SPINAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NERVE GROWTH FACTOR; NEUROFIBROMATOSIS 1; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; REACTION TIME;

EID: 28044434605     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00489.2005     Document Type: Article

References (42)

1. Aloe L, Tuveri MA, Carcassi U, and Levi-Montalcini R. Nerve growth factor in the synovial fluid of patients with chronic arthritis. Arthritis Rheum 35: 351-355, 1992a.
2. Aloe L, Tuveri MA, and Levi-Montalcini R. Studies on carrageenan-induced arthritis in adult rats: presence of nerve growth factor and role of sympathetic innervation. Rheumatol Int 12: 213-216, 1992b.
3. Averill S, Delcroix JD, Michael GJ, Tomlinson DR, Fernyhough P, and Priestley JV. Nerve growth factor modulates the activation status and fast axonal transport of ERK 1/2 in adult nociceptive neurones. Mol Cell Neurosci 18: 183-196, 2001.
4. Blochl A, Blumenstein L, and Ahmadian MR. Inactivation and activation of Ras by the neurotrophin receptor p75. Eur J Neurosci 20: 2321-2335, 2004.
5. Bollag G and McCormick F. Differential regulation of rasGAP and neurofibromatosis gene product activities. Nature 351: 576-579, 1991.
6. Bron R, Klesse LJ, Shah K, Parada LF, and Winter J. Activation of Ras is necessary and sufficient for upregulation of vanilloid receptor type 1 in sensory neurons by neurotrophic factors. Mol Cell Neurosci 22: 118-132, 2003.
7. Cichowski K and Jacks T. NF1 tumor suppressor gene function: narrowing the GAP. Cell 104: 593-604, 2001.
8. Corbett KD and Alber T. The many faces of Ras: recognition of small GTP-binding proteins. Trends Biochem Sci 26: 710-716, 2001.
9. Creange A, Zeller J, Rostaing-Rigattieri S, Brugieres P, Degos JD, Revuz J, and Wolkenstein P. Neurological complications of neurofibromatosis type 1 in adulthood. Brain 122: 473-481, 1999.
10. Dobrowsky RT, Werner MH, Castellino AM, Chao MV, and Hannun YA. Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. Science 265: 1596-1599, 1994.
11. Evans AR, Vasko MR, and Nicol GD. The cAMP transduction cascade mediates the PGE2-induced inhibition of potassium currents in rat sensory neurones. J Physiol 516: 163-178, 1999.
12. Fitzgerald EM and Dolphin AC. Regulation of rat neuronal voltage-dependent calcium channels by endogenous p21-ras. Eur J Neurosci 9: 1252-1261, 1997.
13. Ganju P, O'Bryan JP, Der C, Winter J, and James IF. Differential regulation of SHC proteins by nerve growth factor in sensory neurons and PC12 cells. Eur J Neurosci 10: 1995-2008, 1998.
14. Giovannardi S, Forlani G, Balestrini M, Bossi E, Tonini R, Sturani E, Peres A, and Zippel R. Modulation of the inward rectifier potassium channel IRK1 by the Ras signaling pathway. J Biol Chem 277: 12158-12163, 2002.
15. Guha A, Lau N, Huvar I, Gutmann D, Provias J, Pawson T, and Boss G. Ras-GTP levels are elevated in human NF1 peripheral nerve tumors. Oncogene 12: 507-513, 1996.
16. + currents via a Ras- and Raf-1-dependent pathway in cultured oligodendrocytes. J Neurosci 18: 8712-8719, 1998.
17. Holzer P. Capsaicin as a tool for studying sensory neuron functions. Adv Exp Med Biol 298: 3-16, 1991.
18. Huang EJ and Reichardt LF. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642, 2003.
19. Ingram DA, Hiatt K, King AJ, Fisher L, Shivakumar R, Derstine C, Wenning MJ, Diaz B, Travers JB, Hood A, Marshall M, Williams DA, and 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.
20. Jacks T, Shih TS, Schmitt EM, Bronson RT, Bernards A, and Weinberg RA. Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat Genet 7: 353-361, 1994.
21. Ji RR, Samad TA, Jin SX, Schmoll R, and Woolf CJ. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36: 57-68, 2002.
22. Klesse LJ and 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.
23. Lakkis MM and Tennekoon GI. Neurofibromatosis type 1. I. General overview. J Neurosci Res 62: 755-763, 2000.
24. Largaespada DA, Brannan CI, Jenkins NA, and Copeland NG. Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony stimulating factor hypersensitivity and chronic myeloid leukaemia. Nat Genet 12: 137-143, 1996.
25. Lewin GR and Mendell LM. Nerve growth factor and nociception. Trends Neurosci 16: 353-359, 1993.
26. Lewin GR, Ritter AM, and Mendell LM. Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J Neurosci 13: 2136-2148, 1993.
27. Li Y, Bollag G, Clark R, Stevens J, Conroy L, Fults D, Ward K, Friedman E, Samowitz W, and Robertson M. Somatic mutations in the neurofibromatosis 1 gene in human tumors. Cell 69: 275-281, 1992.
28. 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.
29. Martin GA, Viskochil D, Bollag G, McCabe PC, Crosier WJ, Haubruck H, Conroy L, Clark R, O'Connell P, and Cawthon RM. The GAP-related domain of the neurofibromatosis type 1 gene product interacts with ras p21. Cell 63: 843-849, 1990.
30. Riccardi VM and Eichner JE. Neurofibromatosis: Phenotype, Natural History End Pathogenesis. Baltimore, MD: Johns Hopkins University Press, 1992.
31. Rueff A and Mendell LM. Nerve growth factor NT-5 induce increased thermal sensitivity of cutaneous nociceptors in vitro. J Neurophysiol 76: 3593-3596, 1996.
32. Sherman LS, Atit R, Rosenbaum T, Cox AD, and Ratner N. Single cell Ras-GTP analysis reveals altered Ras activity in a subpopulation of neurofibroma Schwann cells but not fibroblasts. J Biol Chem 275: 30740-30745, 2000.
33. Susen K, Heumann R, and Blochl A. Nerve growth factor stimulates MAPK via the low affinity receptor P75(LNTR). FEBS Lett 463: 231-234, 1999.
34. Vogel KS, El-Afandi M, and Parada LF. Neurofibromin negatively regulates neurotrophin signaling through p21ras in embryonic sensory neurons. Mol Cell Neurosci 15: 398-407, 2000.
35. Wallace MR, Marchuk DA, Andersen LB, Letcher R, Odeh HM, Saulino AM, Fountain JW, Brereton A, Nicholson J, and Mitchell AL. Type 1 neurofibromatosis gene: identification of a large transcript disrupted in three NF1 patients. Science 249: 181-186, 1990.
36. Weskamp G and Otten U. An enzyme-linked immunoassay for nerve growth factor (NGF): a tool for studying regulatory mechanisms involved in NGF production in brain and in peripheral tissues. J Neurochem 48: 1779-1786, 1987.
37. Wolkenstein P, Zeller J, Revuz J, Ecosse E, and Leplege A. Quality-of-life impairment in neurofibromatosis type 1: a cross-sectional study of 128 cases. Arch Dermatol 137: 1421-1425, 2001.
38. Woolf CJ, Safieh-Garabedian B, Ma QP, Crilly P, and Winter J. Nerve growth factor contributes to the generation of inflammatory sensory hyper-sensitivity. Neuroscience 62: 327-331, 1994.
39. Zhang YH, Vasko MR, and Nicol GD. Ceramide, a putative second messenger for nerve growth factor, modulates the TTX-resistant Na(+) current and delayed rectifier K(+) current in rat sensory neurons. J Physiol 544: 385-402, 2002.
40. Zhang YY, Vik TA, Ryder JW, Srour EF, Jacks T, Shannon K, and Clapp DW. Nf1 regulates hematopoietic progenitor cell growth and ras signaling in response to multiple cytokines. J Exp Med 187: 1893-1902, 1998.
41. Zhuang ZY, Gerner P, Woolf CJ, and Ji RR. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114: 149-159,2005.
42. Zhuang ZY, Xu H, Clapham DE, and Ji RR. Phosphatidylinositol 3-kinase activites ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPVl sensitization. J Neurosci 24: 8300-8309, 2004.