Either nitric oxide or nerve growth factor is required for dorsal root ganglion neurons to survive during embryonic and neonatal development

Developmental Brain Research

Volumn 154, Issue 2, 2005, Pages 153-164

  Thippeswamy, Thimmasettappa ^a   McKay, Jennifer S ^b   Quinn, John ^a   Morris, Richard ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

Author keywords

Apoptosis; Dorsal root ganglia; Nerve growth factor; Neuroprotection; Nitric oxide; Skin

Indexed keywords

NERVE GROWTH FACTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN TYROSINE KINASE A;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SELECTION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; IMMUNOREACTIVITY; MALE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NERVE FIBER; NERVE FIBER TRANSECTION; NEUROPROTECTION; NEWBORN; NONHUMAN; PERINATAL DEVELOPMENT; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SKIN; SPINAL CORD NERVE CELL; SPINAL GANGLION;

EID: 13544250685     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devbrainres.2004.10.011     Document Type: Article

References (73)

1. K.M. Albers, T.N. Perrone, T.P. Goodness, M.E. Jones, M.A. Green, and B.M. Davis Cutaneous over-expression of NT-3 increases sensory and sympathetic neurone number and enhances touch dome and hair follicle innervation J. Cell Biol. 134 1996 487 497
2. O.C. Aszmann, T. Winkler, K. Korak, H. Lassmann, and M. Frey The influence of GDNF on the time course and extent of motoneuron loss in the cervical spinal cord after brachial plexus injury in the neonate Neurol. Res. 26 2004 211 217
3. S. Averill, S.B. McMahon, D.O. Clary, L.F. Reichardt, and J.V. Priestly Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurones Eur. J. Neurosci. 7 1995 1484 1494
4. S. Averill, G.J. Michael, P.J. Shortland, R.C. Leavesley, V.R. King, E.J. Bradbury, S.B. McMahon, and J.V. Priestley NGF and GDNF ameliorate the increase in ATF3 expression, which occurs in dorsal root ganglion cells in response to peripheral nerve injury Eur. J. Neurosci. 19 2004 1437 1445
5. D.L.H. Bennet, G. French, J.V. Priestley, and S.B. McMahon 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 1996 211 220
6. S. Brecht, T. Buschmann, S. Grimm, M. Zimmermann, and T. Herdegen Persisting expression of galanin in axotomized mamillary and septal neurons of adult rats labeled for c-Jun and NADPH-diaphorase Brain Res. Mol. Brain Res. 48 1997 7 16
7. D.S. Bredt, and S.H. Snyder Transient nitric oxide synthase neurones in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium Neuron 13 1994 301 313
8. R.B. Campenot, and B.L. MacInnis Retrograde transport of neurotrophins: fact and function J. Neurobiol. 58 2004 217 229
9. J. Cao, M.M. Semenova, V.T. Solovyan, J. Han, E.T. Coffey, and M.J. Courtney Distinct requirements for p38-alpha and JNK stress-activated protein kinases in different forms of apoptotic neuronal death J. Biol. Chem. 2004 (Jun 10) (electronic publication ahead of print)
10. J.C. Conover, and G.D. Yancopoulos Neurotrophin regulation of the developing nervous system: analyses of knockout mice Rev. Neurosci. 8 1997 13 27
11. C. Crowley, S.D. Spencer, M.C. Nishimura, K.S. Chen, S. Pitts-Meek, M.P. Armanini, L.H. Ling, S.B. McMahon, D.L. Shelton, and H.S. Phillips Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons Cell 76 1994 1001 1011
12. R. Curtis, J.R. Tonra, J.L. Stark, K.M. Adryan, J.S. Park, K.D. Cliffer, R.M. Lindsay, and P.S. DiStefano Neuronal injury increases retrograde axonal transport of the neurotrophins to spinal sensory neurons and motor neurons via multiple receptor mechanisms Mol. Cell. Neurosci. 12 1998 105 118
13. A.M. Davies Intrinsic differences in the growth rate of early nerve fibres related to target distance Nature 337 1989 553 555
14. A.M. Davies Paracrine and autocrine actions of neurotrophic factors Neurochem. Res. 21 1996 749 753
15. A.M. Davies, and A.G.S. Lumsden Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion J. Comp. Neurol. 223 1984 124 137
16. A. Dejam, C.J. Hunter, A.N. Schechter, and M.T. Gladwin Emerging role of nitrite in human biology Blood Cells Mol. Diseases 32 2004 423 429
17. J.D. Delcroix, J. Valletta, C. Wu, C.L. Howe, C.F. Lai, J.D. Cooper, P.V. Belichenko, A. Salehi, and W.C. Mobley Trafficking the NGF signal: implications for normal and degenerating neurons Prog. Brain Res. 146 2004 3 23
18. C. Derek, D.C. Molliver, and D.W. Snider Nerve growth factor receptor TrkAIs down-regulated during postnatal development by a subset of dorsal root ganglion neurons J. Comp. Neurol. 381 1997 428 438
19. P.S. DiStefano, B.S. Friedman, C. Radziejewski, C. Alexander, P. Boland, C.M. Schiek, R.M. Lindsay, and S.J. Wiegard The neurotrophins BDNF, NT-3 and NGF display a distinct pattern of retrograde axonal transport in peripheral and central neurones Neuron 8 1992 983 993
20. U. Ernsberger, and H. Rohrer Neuronal precursor cells in chick DRG: differentiation and survival in vitro Dev. Biol. 126 1988 420 432
21. W. Fayad, P. Czernichow, and R. Scharfmann Implication of nitric oxide in NGF-induced cell differentiation: differences between neuronal and beta cells J. Neuroendocrinol. 9 1997 807 812
22. C.E. Fiallos-Estrada, W. Kummer, B. Mayer, R. Bravo, M. Zimmermann, and T. Herdegen Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and cJun co-expression in dorsal root ganglion neurones following sciatic nerve transaction Neurosci. Lett. 150 1993 169 173
23. M. Fitzgerald A physiological study of the prenatal development of cutaneous sensory inputs to dorsal horn cells in the rat J. Physiol. 432 1991 473 482
24. Y. Gavrieli, Y. Sherman, and S.A. Ben-Sasson Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation J. Cell Biol. 119 1992 493 501
25. S. Harper, and A.M. Davies NGF mRNA expression in developing cutaneous epithelium related to innervation density Development 110 1990 515 519
26. J. Hemish, N. Nakaya, V. Mittal, and G. Enikolopov Nitric oxide activates diverse signaling pathways to regulate gene expression J. Biol. Chem. 278 2003 42321 42329
27. T. Herdegen, P. Skene, and M. Bahr The c-Jun transcription factor-biopotential mediator of neuronal death, survival and regeneration Trends Neurosci. 20 1997 227 231
28. S. Hindley, B.H. Juurlink, J.W. Gysbers, P.J. Middlemiss, M.A. Herman, and M.P. Rathbone Nitric oxide donors enhance neurotrophin-induced neurite outgrowth through a cGMP-dependent mechanism J. Neurosci. Res. 47 1997 427 439
29. T. Hirai, N. Nakamichi, and Y. Yoneda Activator protein-1 complex expressed by magnetism in cultured rat hippocampal neurons Biochem. Biophys. Res. Commun. 292 2002 200 207
30. H. Kashiba, B. Hyon, and E. Senba Glial cell line-derived neurotrophic factor and nerve growth factor receptor mRNAs are expressed in distinct subgroups of dorsal root ganglion neurons and are differentially regulated by peripheral axotomy in the rat Neurosci. Lett. 252 1998 107 110
31. G. Keilhoff, B. Seidel, H. Noack, W. Tischmeyer, D. Stanek, and G. Wolf Patterns of nitric oxide synthase at the messenger RNA and protein levels during early rat brain development Neuroscience 75 1996 1193 2001
32. A.M. Kenney, and J.D. Kocsis Peripheral axotomy induces long-term c-Jun amino-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia in vivo J. Neurosci. 18 1998 1318 1328
33. S. Korsching The neurotrophic factor concept: a re-examination J. Neurosci. 13 1993 2739 2748
34. R.M. Lindsay, S.J. Wiegand, C.A. Altar, and P.S. Di Stefano Neurotrophic factors: from molecule to man Trends Neurosci. 17 1994 182 190
35. Q. Ma, C. Fode, F. Guillemot, and D.J. Anderson Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia Genes Dev. 13 1999 1717 1728
36. C.F. Mang, S. Truempler, D. Erbelding, and H. Kilbinger Modulation by NO of acetylcholine release in the ileum of wild-type and NOS gene knockout mice Am. J. Physiol.: Gasterointest. Liver Physiol. 283 2002 G1132 G1138
37. S.B. McMahon, D.L. Bennett, J.V. Priestley, and D.L. Shelton The biological effects of endogenous nerve growth factor on adult sensory neurones revealed by a trkA-IgG fusion molecule Nat. Med. 1 1995 774 780
38. B. Medelson, K.M. Albers, T.P. Goodness, and B.M. Davis Over-expression of nerve growth factor in epidermis of transgenic mice preserves excess sensory neurones but does not alter the somatotopic organization of cutaneous nerve projections Neurosci. Lett. 211 1996 68 72
39. S.P. Memberg, and A.K. Hall Proliferation, differentiation and survival of rat sensory neuron precursors in vitro require specific factors Mol. Cell. Neurosci. 6 1995 323 335
40. K. Mirnics, and H.R. Koerber Prenatal development of rat primary afferent fibers: I. Peripheral projections J. Comp. Neurol. 355 1995 589 600
41. I. Mizusawa, S. Abe, K. Kanno, A. Yabashi, T. Honda, M. Suto, and K. Hiraiwa Expression of cytokines, neurotrophins, neurotrophin receptors and NOS mRNA in dorsal root ganglion of a rat tourniquet model Leg. Med. 5 2003 S271 S274
42. D.C. Molliver, M. Radeke, S.C. Feinstein, and W.D. Snider Presence or absence of trkA protein distinguishes subsets of small sensory neurones with unique cytochemical characteristics and dorsal horn projections J. Comp. Neurol. 361 1995 404 416
43. I.N. Mungrue, D.S. Bredt, D.J. Stewart, and M. Husain From molecules to mammals: what's NOS got to do with it? Acta Physiol. Scand. 179 2003 123 135
44. B.R. Nelson, K. Claes, V. Todd, M. Chaverra, and F. Lefcort NELL2 promotes motor and sensory neuron differentiation and stimulates mitogenesis in DRG in vivo Dev. Biol. 270 2004 322 335
45. T. Ogura, K. Nakayama, H. Fujisawa, and H. Esumi Neuronal nitric oxide synthase expression in neuronal cell differentiation Neurosci. Lett. 204 1996 89 92
46. H.S. Park, S.H. Huh, M.S. Kim, S.H. Lee, and E.J. Choi Nitric oxide negatively regulates c-Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation Proc. Natl. Acad. Sci. 97 2000 14382 14387
47. T.D. Patel, I. Kramer, J. Kucera, V. Niederkofler, T.M. Jessell, S. Arber, and W.D. Snider Peripheral NT3 signaling is required for ETS protein expression and central patterning of proprioceptive sensory afferents Neuron 38 2003 403 416
48. M. Paveliev, M.S. Airaksinen, and M. Saarma GDNF family ligands activate multiple events during axonal growth in mature sensory neurons Mol. Cell. Neurosci. 25 2004 453 459
49. N. Peunova, and G. Enikolopov Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells Nature 375 1995 68 73
50. E. Pineda-Molina, and S. Lamas Nitric oxide as a regulator of gene expression: studies with the transcription factor proteins cJun and p50 BioFactors 15 2001 113 115
51. L.G. Pinon, L. Minichiello, R. Klein, and A.M. Davies Timing of neuronal death in trkA, trkB and trkC mutant embryos reveals developmental changes in sensory neuron dependence on Trk signalling Development 122 1996 3255 3261
52. G. Raivich, M. Bohatschek, C. Da Costa, O. Iwata, M. Galiano, M. Hristova, A.S. Nateri, M. Makwana, L. Riera-Sans, D.P. Wolfer, H.P. Lipp, A. Aguzzi, E.F. Wagner, and A. Behrens The AP-1 transcription factor c-Jun is required for efficient axonal regeneration Neuron 43 2004 57 67
53. M.L. Reynolds, M. Fitzgerald, and L.I. Benowitz GAP-43 expression in developing cutaneous and muscle nerves in the rat hind limb Neuroscience 41 1991 201 211
54. J.T. Rifkin, V.J. Todd, L.W. Anderson, and F. Lefcort Dynamic expression of neurotrophin receptors during sensory neuron genesis and differentiation Dev. Biol. 227 2000 465 480
55. H.H.H.W. Schmidt, T.D. Warner, M. Nakane, U. Foèrstermann, and F. Murad Regulation and subcellular location of nitrogen oxide synthases in RAW264.7 macrophages Mol. Pharmacol. 41 1992 615 624
56. M.E. Sebert, and E.M. Shooter Expression of mRNA for neurotrophic factors and their receptors in the rat dorsal root ganglion and sciatic nerve following nerve injury J. Neurosci. Res. 36 1993 357 367
57. I. Silos-Santiago, D.C. Molliver, S. Ozaki, R.J. Smeyne, A.M. Fagan, M. Barbacid, and W.D. Snider Non-trkA expressing small DRG neurones are lost in trkA-deficient mice J. Neurosci. 15 1995 5929 5942
58. R.J. Smeyne, R. Klein, A. Schnapp, L.K. Long, S. Bryant, A. Lewin, S.A. Lira, and M. Barbacid Severe sensory neuropathies in mice carrying disrupted trk/NGF receptor gene Nature 368 1994 246 249
59. T. Thippeswamy, and R. Morris Nerve growth factor inhibits the expression of nitric oxide synthase in neurones in dissociated cultures of rat dorsal root ganglia Neurosci. Lett. 230 1997 9 12
60. T. Thippeswamy, and R. Morris Cyclic guanosine 3′, 5′-monophosphate-mediated neuroprotection by nitric oxide in dissociated cultures of rat dorsal root ganglion neurons Brain Res. 774 1997 116 122
61. T. Thippeswamy, R.K. Jain, N. Mumtaz, and R. Morris Inhibition of neuronal nitric oxide synthase results in neurodegenerative changes in the axotomised dorsal root ganglion neurons: evidence for a neuroprotective role of nitric oxide in vivo Neurosci. Res. 40 2001 37 44
62. T. Thippeswamy, J.S. McKay, and R. Morris Bax and caspases are inhibited by endogenous nitric oxide in dorsal root ganglion neurons in vitro Eur. J. Neurosci. 40 2001 1229 1236
63. Thimmasettappa Thippeswamy, J.S. McKay, and J. Quinn NO-cGMP pathway induces nerve growth factor in peripheral glia cells FENS Abstr. 1 2002 AO52.18
64. T. Thippeswamy, J.S. McKay, R. Morris, J. Quinn, L-F. Wong, and D. Murphy Glial-mediated neuroprotection: evidence for the protective role of NO-cGMP pathway in the peripheral nervous system via neuron-glial communication Glia 2004 10.1002/glia.20105
65. G.D. Thomas, P.W. Shaul, I.S. Yuhanna, S.C. Froehner, and M.E. Adams Vasomodulation by skeletal muscle-derived nitric oxide requires alpha-syntrophin-mediated sarcolemmal localization of neuronal nitric oxide synthase Circ. Res. 92 2003 554 560
66. S. Tranguch, and Y. Huet-Hudson Decreased viability of nitric oxide synthase double knockout mice Mol. Reprod. Dev. 65 2003 175 179
67. M.W. Weible, N. Ozsarac, M.L. Grimes, and I.A. Hendry Comparison of nerve terminal events in vivo effecting retrograde transport of vesicles containing neurotrophins or synaptic vesicle components J. Neurosci. Res. 75 2004 771 781
68. R. Weller Nitric oxide: a key mediator in cutaneous physiology Clin. Exp. Dermatol. 28 2003 511 514
69. F.A. White, I. Silos-Saliago, D.C. Molliver, M. Nishimura, H. Phillips, M. Barbacid, and W.D. Snider Synchronous onset of NGF and trkA survival dependence in developing dorsal root ganglia J. Neurosci. 16 1996 4662 4672
70. G. Whiteside, C.A. Doyle, S.P. Hunt, and R. Munglani Differential time course of neuronal and glial apoptosis in neonatal rat dorsal root ganglia after sciatic nerve axotomy Eur. J. Neurosci. 10 1998 3400 3408
71. H. Wu, W.J. Friedman, and C.F. Dreyfus Differential regulation of neurotrophin expression in basal forebrain astrocytes by neuronal signals J. Neurosci. Res. 76 2004 76 85
72. X. Zhang, V. Verge, H.Z. Wiesenfeld, G. Ju, D. Bredt, S.H. Synder, and T. Hokfelt NOS-like immunoreactivity in lumbar DRG and spinal cord of rat and monkey and effect of peripheral axotomy J. Comp. Neurol. 335 1993 563 575
73. X.F. Zhou, Y.S. Deng, E. Chie, Q. Xue, J.H. Zhong, E.M. McLachlan, R.A. Rush, and C.J. Xian Satellite-cell-derived nerve growth factor and neurotrophin-3 are involved in noradrenergic sprouting in the dorsal root ganglia following peripheral nerve injury in the rat Eur. J. Neurosci. 11 1999 1711 1722