Activating transcription factor 3 induction in sympathetic neurons after axotomy: Response to decreased neurotrophin availability

Neuroscience

Volumn 150, Issue 4, 2007, Pages 887-897

  Hyatt Sachs, H ^a   Schreiber, R C ^a   Shoemaker, S E ^a   Sabe, A ^a   Reed, E ^a   Zigmond, R E ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cell body response; leukemia inhibitory factor; nerve growth factor; nerve injury; sialectomy; superior cervical ganglion

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ANTISERUM; CYTOKINE; LEUKEMIA INHIBITORY FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; OXIDOPAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELL POPULATION; CONTROLLED STUDY; IMMUNOREACTIVITY; MALE; MOTONEURON; MOUSE; NERVE CELL; NERVE FIBER TRANSECTION; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; SALIVARY GLAND; SATELLITE CELL; SCIATIC NERVE; SENSORY NERVE CELL; SIALECTOMY; SUPERIOR CERVICAL GANGLION; SYMPATHETIC GANGLION; SYMPATHETIC NERVE CELL;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; ANTIBODIES; AXOTOMY; GANGLIA, SYMPATHETIC; GENE EXPRESSION REGULATION; LEUKEMIA INHIBITORY FACTOR; MALE; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTOR; NEURONS; OXIDOPAMINE; RATS; RATS, SPRAGUE-DAWLEY; SYMPATHOLYTICS;

EID: 36849094459     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.10.008     Document Type: Article

References (98)

1. Ambron R.T., and Walters E.T. Priming events and retrograde injury signals. A new perspective on the cellular and molecular biology of nerve regeneration. Mol Neurobiol 13 (1996) 61-79
2. Averill S., Michael G.J., Shortland P.J., Leavesley R.C., King V.R., Bradbury E.J., McMahon S.B., and Priestley J.V. 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
3. Bachoo M., Hall A., and Zigmond R.E. Postganglionic axotomy and 6-hydroxydopamine (6-HDA) produce a burst of satellite cell proliferation in adult rat superior cervical ganglion (SCG). Soc Neurosci Abstr 18 (1992) 625
4. Banner L.R., and Patterson P.H. Major changes in the expression of the mRNAs for cholinergic differentiation factor/leukemia inhibitory factor and its receptor after injury to adult peripheral nerves and ganglia. Proc Natl Acad Sci U S A 91 (1994) 7109-7113
5. Belliveau D.J., Krivko I., Kohn J., Lachance C., Pozniak C., Rusakov D., Kaplan D., and Miller F.D. NGF and neurotrophin-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J Cell Biol 136 (1997) 375-388
6. Bjerre B., Bjorklund A., and Edwards D.C. Axonal regeneration of peripheral adrenergic neurons: Effects of antiserum to nerve growth factor in mouse. Cell Tissue Res 148 (1974) 441-476
7. Bjerre B., Wiklund L., and Edwards D.C. A study of the de- and regenerative changes in the sympathetic nervous system of the adult mouse after treatment with the antiserum to nerve growth factor. Brain Res 92 (1975) 257-278
8. Boeshore K.L., Schreiber R.C., Vaccariello S.A., Sachs H.H., Salazar R., Lee J., Ratan R.R., Leahy P., and Zigmond R.E. Novel changes in gene expression following axotomy of a sympathetic ganglion: a microarray analysis. J Neurobiol 59 (2004) 216-235
9. Bowers C.W., and Zigmond R.E. Localization of neurons in the rat superior cervical ganglion that project into different postganglionic trunks. J Comp Neurol 185 (1979) 381-391
10. Brattgard S.O., Edstrom J.E., and Hyden H. The chemical changes in regenerating neurons. J Neurochem 1 (1957) 316-325
11. Bussmann K.A., and Sofroniew M.V. Re-expression of p75NTR by adult motor neurons after axotomy is triggered by retrograde transport of a positive signal from axons regrowing through damaged or denervated peripheral nerve tissue. Neuroscience 91 (1999) 273-281
12. Chen B.P., Wolfgang C.D., and Hai T. Analysis of ATF3, a transcription factor induced by physiological stresses and modulated by gadd153/Chop10. Mol Cell Biol 16 (1996) 1157-1168
13. Cragg B.G. What is the signal for chromatolysis?. Brain Res 23 (1970) 1-21
14. De Felipe C., and Hunt S.P. The differential control of c-jun expression in regenerating sensory neurons and their associated glial cells. J Neurosci 14 (1994) 2911-2923
15. Diamond J., Holmes M., and Coughlin M. Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J Neurosci 12 (1992) 1454-1466
16. Doster S.K., Lozano A.M., Aguayo A.J., and Willard M.B. Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron 6 (1991) 635-647
17. Dussor G.O., Price T.J., and Flores C.M. Activating transcription factor 3 mRNA is upregulated in primary cultures of trigeminal ganglion neurons. Brain Res Mol Brain Res 118 (2003) 156-159
18. Elfvin L.G., Bjorklund H., Dahl D., and Seiger A. Neurofilament-like and glial fibrillary acidic protein-like immunoreactivities in rat and guinea-pig sympathetic ganglia in situ and after perturbation. Cell Tissue Res 250 (1987) 79-86
19. ElShamy W.M., Linnarsson S., Lee K.F., Jaenisch R., and Ernfors P. Prenatal and postnatal requirements of NT-3 for sympathetic neuroblast survival and innervation of specific targets. Development 122 (1996) 491-500
20. Ernfors P., Lee K.F., Kucera J., and Jaenisch R. Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77 (1994) 503-512
21. Escary J.L., Perreau J., Dumenil D., Ezine S., and Brulet P. Leukaemia inhibitory factor is necessary for maintenance of haematopoietic stem cells and thymocyte stimulation. Nature 363 (1993) 361-364
22. Farinas I., Jones K.R., Backus C., Wang X.Y., and Reichardt L.F. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369 (1994) 658-661
23. Fernandes K.J., Fan D.P., Tsui B.J., Cassar S.L., and Tetzlaff W. Influence of the axotomy to cell body distance in rat rubrospinal and spinal motoneurons: differential regulation of GAP-43, tubulins, and neurofilament-M. J Comp Neurol 414 (1999) 495-510
24. Flett D.L., and Bell C. Topography of functional subpopulations of neurons in the superior cervical ganglion of the rat. J Anat 177 (1991) 55-66
25. Francis J.S., Dragunow M., and During M.J. Overexpression of ATF-3 protects rat hippocampal neurons from in vivo injection of kainic acid. Brain Res Mol Brain Res 124 (2004) 199-203
26. Gloster A., and Diamond J. NGF-dependent and NGF-independent recovery of sympathetic function after chemical sympathectomy with 6-hydroxydopamine. J Comp Neurol 359 (1995) 586-594
27. Gold B.G., Austin D.R., and Storm-Dickerson T. Multiple signals underlie the axotomy-induced up-regulation of c-JUN in adult sensory neurons. Neurosci Lett 176 (1994) 123-127
28. Gorin P.D., and Johnson Jr. E.M. Effects of long-term nerve growth factor deprivation on the nervous system of the adult rat: an experimental autoimmune approach. Brain Res 198 1 (1980) 27-42
29. Grafstein B. The nerve cell body response to axotomy. Exp Neurol 48 (1975) 32-51
30. Hai T., and Hartman M.G. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. Gene 273 (2001) 1-11
31. Hai T., Wolfgang C.D., Marsee D.K., Allen A.E., and Sivaprasad U. ATF3 and stress responses. Gene Expr 7 (1999) 321-335
32. Hartman M.G., Lu D., Kim M.L., Kociba G.J., Shukri T., Buteau J., Wang X., Frankel W.L., Guttridge D., Prentki M., Grey S.T., Ron D., and Hai T. Role for activating transcription factor 3 in stress-induced beta-cell apoptosis. Mol Cell Biol 24 (2004) 5721-5732
33. Hendry I.A., Stockel K., Thoenen H., and Iversen L.L. The retrograde axonal transport of nerve growth factor. Brain Res 68 (1974) 103-121
34. Herdegen T., and Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 28 (1998) 370-490
35. Hsu J.C., Laz T., Mohn K.L., and Taub R. Identification of LRF-1, a leucine-zipper protein that is rapidly and highly induced in regenerating liver. Proc Natl Acad Sci U S A 88 (1991) 3511-3515
36. Hunt D., Hossain-Ibrahim K., Mason M.R., Coffin R.S., Lieberman A.R., Winterbottom J., and Anderson P.N. ATF3 upregulation in glia during Wallerian degeneration: differential expression in peripheral nerves and CNS white matter. BMC Neurosci 5 (2004) 9
37. Hyatt-Sachs H., Bachoo M., Schreiber R., Vaccariello S.A., and Zigmond R.E. Chemical sympathectomy and postganglionic nerve transection produce similar increases in galanin and VIP mRNA but differ in their effects on peptide content. J Neurobiol 30 (1996) 543-555
38. Iversen L.L., Stockel K., and Thoenen H. Autoradiographic studies of the retrograde axonal transport of nerve growth factor in mouse sympathetic neurones. Brain Res 88 (1975) 37-43
39. Jonsson G., and Sachs C. Effects of 6-hydroxydopamine on the uptake and storage of noradrenaline in sympathetic adrenergic neurons. Eur J Pharmacol 9 (1970) 141-155
40. Kenney A.M., and Kocsis J.D. Temporal variability of jun family transcription factor levels in peripherally or centrally transected adult rat dorsal root ganglia. Brain Res Mol Brain Res 52 (1997) 53-61
41. Klimaschewski L., Tran T.D., Nobiling R., and Heym C. Plasticity of postganglionic sympathetic neurons in the rat superior cervical ganglion after axotomy. Microsc Res Tech 29 (1994) 120-130
42. Koistinaho J., Pelto-Huikko M., Sagar S.M., Dagerlind A., Roivainen R., and Hokfelt T. Injury-induced long-term expression of immediate early genes in the rat superior cervical ganglion. Neuroreport 4 (1993) 37-40
43. Korsching S., and Thoenen H. Treatment with 6-hydroxydopamine and colchicine decreases nerve growth factor levels in sympathetic ganglia and increases them in the corresponding target tissues. J Neurosci 5 (1985) 1058-1061
44. Korsching S., and Thoenen H. Developmental changes of nerve growth factor levels in sympathetic ganglia and their target organs. Dev Biol 126 (1988) 40-46
45. Kuruvilla R., Zweifel L.S., Glebova N.O., Lonze B.E., Valdez G., Ye H., and Ginty D.D. A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 118 (2004) 243-255
46. Lahtivirta S., Koistinaho J., and Hervonen A. A subpopulation of large neurons of the sympathetic superior cervical ganglion innervates the NGF-rich submandibular salivary gland in young adult and aged mice. J Auton Nerv Syst 50 (1995) 283-289
47. Levi-Montalcini R., and Angeletti P.U. Nerve growth factor. Physiol Rev 48 (1968) 534-569
48. Lieberman A.R. The axon reaction: A review of the principal features of perikaryal responses to axon injury. In: Pfeiffer C.C., and Smythies J.R. (Eds). International review of neurobiology Vol. 14 (1971), Academic Press, London 49-129
49. Lieberman A.R. Some factors affecting retrograde neuronal responses to axonal lesion. In: Bellies R., and Gray E.G. (Eds). Essays on the nervous system (1974), Cleared Press, Oxford 71-105
50. Lindwall C., and Kanje M. The Janus role of c-Jun: cell death versus survival and regeneration of neonatal sympathetic and sensory neurons. Exp Neurol 196 (2005) 184-194
51. Malmfors T., and Sachs C. Degeneration of adrenergic nerves produced by 6-hydroxydopamine. Eur J Pharmacol 3 (1968) 89-92
52. Mason M.R., Lieberman A.R., and Anderson P.N. Corticospinal neurons up-regulate a range of growth-associated genes following intracortical, but not spinal, axotomy. Eur J Neurosci 18 (2003) 789-802
53. Mathew T.C., and Miller F.D. Induction of Tα1-α-tubulin mRNA during neuronal regeneration is a function of the amount of axon lost. Dev Biol 158 (1993) 467-474
54. Mayumi-Matsuda K., Kojima S., Nakayama T., Suzuki H., and Sakata T. Scanning gene expression during neuronal cell death evoked by nerve growth factor depletion. Biochim Biophys Acta 1489 (1999) 293-302
55. Mearow K.M., and Kril Y. Anti-NGF treatment blocks the upregulation of NGF receptor mRNA expression associated with collateral sprouting of rat dorsal root ganglion neurons. Neurosci Lett 184 (1995) 55-58
56. Miller F.D., Speelman A., Mathew T.C., Fabian J., Chang E., Pozniak C., and Toma J.G. Nerve growth factor derived from terminals selectively increases the ratio of p75 to trkA NGF receptors on mature sympathetic neurons. Dev Biol 161 (1994) 206-217
57. Mizusawa I., Abe S., Kanno K., Yabashi A., Honda T., Suto M., and Hiraiwa K. Expression of cytokines, neurotrophins, neurotrophin receptors and NOS mRNA in dorsal root ganglion of a rat tourniquet model. Leg Med (Tokyo) 5 Suppl 1 (2003) S271-S274
58. Moix L.J., Greeson D.M., Armstrong D.M., and Wiley R.G. Separate signals mediate hypoglossal motor neuron response to axonal injury. Brain Res 564 (1991) 176-180
59. Nagata Y., Andy M., Takahama K., Iwata M., Hori S., and Kato K. Retrograde transport of endogenous nerve growth factor in superior cervical ganglion of adult rats. J Neurochem 49 (1987) 296-302
60. Nakagomi S., Suzuki Y., Namikawa K., Kiryu-Seo S., and Kiyama H. Expression of the activating transcription factor 3 prevents c-Jun N-terminal kinase-induced neuronal death by promoting heat shock protein 27 expression and Akt activation. J Neurosci 23 (2003) 5187-5196
61. Nja A., and Purves D. The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea-pig. J Physiol 277 (1978) 55-75
62. Obata K., Yamanaka H., Fukuoka T., Yi D., Tokunaga A., Hashimoto N., Yoshikawa H., and Noguchi K. Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats. Pain 101 (2003) 65-77
63. Otten U., Goedert M., Schwab M., and Thibault J. Immunization of adult rats against 2.5 S NGF: effects on the peripheral sympathetic nervous system. Brain Res 176 (1979) 79-90
64. Palmatier M.A., Hartman B.K., and Johnson Jr. E.M. Demonstration of retrogradely transported endogenous nerve growth factor in axons of sympathetic neurons. J Neurosci 4 (1984) 751-756
65. Paravicini U., Stoeckel K., and Thoenen H. Biological importance of retrograde axonal transport of nerve growth factor in adrenergic neurons. Brain Res 84 (1975) 279-291
66. Pearson A.G., Gray C.W., Pearson J.F., Greenwood J.M., During M.J., and Dragunow M. ATF3 enhances c-Jun-mediated neurite sprouting. Brain Res Mol Brain Res 120 (2003) 38-45
67. Rao M.S., Sun Y., Escary J.L., Perreau J., Tresser S., Patterson P.H., Zigmond R.E., Brulet P., and Landis S.C. Leukemia inhibitory factor mediates an injury response but not a target-directed developmental transmitter switch in sympathetic neurons. Neuron 11 (1993) 1175-1185
68. Ruit K.G., Osborne P.A., Schmidt R.E., Johnson Jr. E.M., and Snider W.D. Nerve growth factor regulates sympathetic ganglion cell morphology and survival in the adult mouse. J Neurosci 10 (1990) 2412-2419
69. Schreiber R.C., Shadiack A.M., Bennett T.A., Sedwick C.E., and Zigmond R.E. Changes in the macrophage population of the rat superior cervical ganglion after postganglionic nerve injury. J Neurobiol 27 (1995) 141-153
70. Schreiber R.C., Vaccariello S.A., Boeshore K., Shadiack A.M., and Zigmond R.E. A comparison of the changes in the non-neuronal cell populations of the superior cervical ganglia following decentralization and axotomy. J Neurobiol 53 (2002) 68-79
71. Seijffers R., Allchorne A.J., and Woolf C.J. The transcription factor ATF-3 promotes neurite outgrowth. Mol Cell Neurosci 32 (2006) 143-154
72. Shadiack A.M., Vaccariello S.A., Sun Y., and Zigmond R.E. Nerve growth factor inhibits sympathetic neurons' response to an injury cytokine. Proc Natl Acad Sci U S A 95 (1998) 7727-7730
73. Shadiack A., Sun Y., and Zigmond R. Nerve growth factor antiserum induces axotomy-like changes in neuropeptide expression in intact sympathetic and sensory neurons. J Neurosci 21 (2001) 363-371
74. Sheng M., and Greenberg M.E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4 (1990) 477-485
75. Shoemaker S.E., Sachs H.H., Vaccariello S.A., and Zigmond R.E. Reduction in nerve growth factor availability leads to a conditioning lesion-like effect in sympathetic neurons. J Neurobiol 66 (2006) 1322-1337
76. Sun Y., Rao M.S., Zigmond R.E., and Landis S.C. Regulation of vasoactive intestinal peptide expression in sympathetic neurons in culture and after axotomy: The role of cholinergic differentiation factor/leukemia inhibitory factor. J Neurobiol 25 (1994) 415-430
77. Sun Y., and Zigmond R.E. Involvement of leukemia inhibitory factor in the increases in galanin and vasoactive intestinal peptide mRNA and the decreases in neuropeptide Y and tyrosine hydroxylase mRNA in sympathetic neurons after axotomy. J Neurochem 67 (1996) 1751-1760
78. Takahashi N., Kikuchi S., Dai Y., Kobayashi K., Fukuoka T., and Noguchi K. Expression of auxiliary beta subunits of sodium channels in primary afferent neurons and the effect of nerve injury. Neuroscience 121 (2003) 441-450
79. Takeda M., Kato H., Takamiya A., Yoshida A., and Kiyama H. Injury-specific expression of activating transcription factor-3 in retinal ganglion cells and its colocalized expression with phosphorylated c-Jun. Invest Ophthalmol Vis Sci 41 (2000) 2412-2421
80. Tetzlaff W., Alexander S.W., Miller F.D., and Bisby M.A. Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43. J Neurosci 11 (1991) 2528-2544
81. Theriault E., Tetzlaff W., and Tator C.H. Elevated gene expression in the red nucleus after spinal cord compression injury. Neuroreport 3 (1992) 559-562
82. Tranzer J.P., and Thoenen H. An electron microscopic study of selective, acute degeneration of sympathetic nerve terminals after administration of 6-hydroxydopamine. Experientia 24 (1968) 155-156
83. Tranzer J.P., and Richards J.G. Fine structural aspects of the effect of 6-hydroxydopamine on peripheral adrenergic neurons. In: Malmfors T., and Thoenen H. (Eds). 6-Hydroxydopamine and catecholamine neurons (1971), North Holland Bulb, Amsterdam 15-31
84. Tranzer J.P., Thoenen H., Snipes R.L., and Richards J.G. Recent developments on the ultrastructural aspect of adrenergic nerve endings in various experimental conditions. Prog Brain Res 31 (1969) 33-46
85. Tsujino H., Kondo E., Fukuoka T., Dai Y., Tokunaga A., Miki K., Yonenobu K., Ochi T., and Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: A novel neuronal marker of nerve injury. Mol Cell Neurosci 15 (2000) 170-182
86. Tsuzuki K., Kondo E., Fukuoka T., Yi D., Tsujino H., Sakagami M., and Noguchi K. Differential regulation of P2X(3) mRNA expression by peripheral nerve injury in intact and injured neurons in the rat sensory ganglia. Pain 91 (2001) 351-360
87. Vaidyanathan U., Hyat-Sachs H., and Zigmond R.E. Increases in the glial fibrillary acidic protein (GFAP)-like immunoreactivity (IR) in the rat superior cervical ganglion (SCG) after decentralization, axotomy and explantation. Soc Neurosci Abstr 18 (1992) 624
88. Van der Zee C.E., Rashid K., Le K., Moore K.A., Stanisz J., Diamond J., Racine R.J., and Fahnestock M. Intraventricular administration of antibodies to nerve growth factor retards kindling and blocks mossy fiber sprouting in adult rats. J Neurosci 15 (1995) 5316-5323
89. Voyvodic J.T. Peripheral target regulation of dendritic geometry in the rat superior cervical ganglion. J Neurosci 9 (1989) 1997-2010
90. Wang R., Guo W., Ossipov M.H., Vanderah T.W., Porreca F., and Lai J. Glial cell line-derived neurotrophic factor normalizes neurochemical changes in injured dorsal root ganglion neurons and prevents the expression of experimental neuropathic pain. Neuroscience 121 (2003) 815-824
91. Watson W.E. Cellular responses to axotomy and to related procedures. Br Med Bull 30 (1974) 112-115
92. Wong J., and Oblinger M.M. NGF rescues substance P expression but not neurofilament or tubulin gene expression in axotomized sensory neurons. J Neurosci 11 (1991) 543-552
93. Zhou X.F., and Rush R. Sympathetic neurons in neonatal rats require endogenous neurotrophin-3 for survival. J Neurosci 15 (1995) 6521-6530
94. Zhou X.F., and Rush R.A. Endogenous nerve growth factor is required for regulation of the low affinity neurotrophin receptor (p75) in sympathetic but not sensory ganglia. J Comp Neurol 372 (1996) 37-48
95. Zhou X.F., Settler C., and Rush R.A. An improved procedure for the immunohistochemical localization of nerve growth factor-like immunoreactivity. J Neurosci Methods 54 (1994) 95-102
96. Zhou X.F., Chie E.T., Deng Y.S., and Rush R.A. Rat mature sympathetic neurones derive neurotrophin 3 from peripheral effector tissues. Eur J Neurosci 9 (1997) 2753-2764
97. Zhou Y., Deneris E., and Zigmond R.E. Differential regulation of levels of nicotinic receptor subunit transcripts in adult sympathetic neurons after axotomy. J Neurobiol 34 (1998) 164-178
98. Zigmond R.E., and Vaccariello S.A. Activating transcription factor 3 immunoreactivity identifies small populations of axotomized neurons in rat cervical sympathetic ganglia after transection of the preganglionic cervical sympathetic trunk. Brain Res 1159 (2007) 119-123