A role for TrkA during maturation of striatal and basal forebrain cholinergic neurons in vivo

Journal of Neuroscience

Volumn 17, Issue 20, 1997, Pages 7644-7654

  Fagan, Anne M ^a   Garber, Melinda ^b   Barbacid, Mariano ^b   Silos Santiago, Inmaculada ^b   Holtzman, David M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

Author keywords

Development; Knockout; Nerve growth factor; Neurotrophin; p75(NTR); TrkA

Indexed keywords

NERVE GROWTH FACTOR; NEUROTROPHIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CHOLINERGIC ACTIVITY; CHOLINERGIC TRANSMISSION; DATA ANALYSIS; HIPPOCAMPUS; MOUSE; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PREDICTION; PRIORITY JOURNAL; QUANTITATIVE DIAGNOSIS;

EID: 0030761205     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-20-07644.1997     Document Type: Article

References (86)

1. Albers KM, Wright DE, Davis BM (1994) Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J Neurosci 14:1422-1432.
2. Alcantara S, Frison J, Del Rio JA, Soriano E, Barbacid M, Silos-Santiago I (1997) TrkB signaling is required for postnatal survival of CNS neurons and protects hippocampal and motor neurons from axotomy-induced death. J Neurosci 17:3623-3633.
3. Alderson RF, Alterman AL, Barde YA, Lindsay RM (1990) Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5:297-306.
4. Anderson KJ, Dam D, Lee S, Cotman CW (1988) Basic fibroblast growth factor prevents death of lesioned cholinergic neurons in vivo. Nature 332:360-361.
5. Barbacid M (1994) The Trk family of neurotrophin receptors. J Neuro-biol 25:1386-1403.
6. Batchelor PE, Armstrong DM, Blaker SM, Gage FH (1989) Nerve-growth factor receptor and choline acetyltransferase colocalization in neurons within the rat forebrain: response to fimbria-fornix transection. J Comp Neurol 284:187-204.
7. Burke MA, Apter JR, Wainer BH, Mufson EJ, Kordower JH (1994a) Age-related vulnerability of developing cholinergic basal forebrain neurons following excitotoxic lesions of the hippocampus. Exp Neurol 128:159-171.
8. Burke MA, Mobley WC, Cho J, Wiegand SJ, Lindsay RM, Mufson EJ, Kordower JH (1994b) Loss of developing cholinergic basal forebrain neurons following excitotoxic lesions of the hippocampus: rescue by neurotrophins. Exp Neurol 130:178-195.
9. NTR decide? Neuron 18:187-190.
10. Cavalieri B (1966) Geometria degli indivisibili. Torino, Italy: Unione Tipografico.
11. Cavicchioli L, Flanigan TP, Vantini G, Fusco M, Polato P, Toffano G, Walsh FS, Leon A (1989) NGF amplifies expression of NGF receptor messenger RNA in forebrain cholinergic neurons of rats. Eur J Neurosci 1:258-262.
12. Chao MV (1992) Neurotrophin receptors: a window into neuronal differentiation. Neuron 9:583-593.
13. Chao MV, Bothwell MA, Ross AH, Koprowski H, Lanahan AA, Buck CR, Sehgal A (1986) Gene transfer and molecular cloning of the human NGF receptor. Science 232:518-521.
14. Clary DO, Reichardt LF (1994) An alternatively spliced form of the nerve growth factor receptor TrkA confers an enhanced response to neurotrophin-3. Proc Natl Acad Sci USA 91:11133-11137.
15. Conover JC, Erickson JT, Katz DM, Bianchi LM, Poueymirou WT, McClain J, Pan L, Helgren M, Ip NY, Boland P, Friedman B, Wiegand S, Vejsada R, Kato AC, DeChiara TM, Yancopoulos GD (1995) Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4. Nature 375:235-238.
16. Cooper JD, Skepper JN, da Penha Berzaghi M, Lindholm D, Sofroniew MV (1996) Delayed death of septal cholinergic neurons after excitotoxic ablation of hippocampal neurons during early postnatal development in the rat. Exp Neurol 139:143-155.
17. Coyle JT, Price DL, DeLong MR (1983) Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219:1184-1190.
18. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts-Meek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD, Phillips HS (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011.
19. Davies AM, Minichiello L, Klein R (1995) Developmental changes in NT3 signaling via TrkA and TrkB in embryonic neurons. EMBO J 14:4482-4489.
20. Davis BM, Albers KM, Seroogy KM, Katz DM (1994) Overexpression of nerve growth factor in transgenic mice induces novel sympathetic projections to primary sensory neurons. J Comp Neurol 349:464-474.
21. Edwards RH, Rutter WJ, Hanahan D (1989) Directed expression of NGF to pancreatic B cells in transgenic mice leads to selective hyper-innervation of the islets. Cell 58:161-170.
22. Ernfors P, Lee KF, Jaenisch R (1994) Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368:147-150.
23. Fagan AM, Zhang H, Landis S, Smeync RJ, Silos-Santiago I, Barbacid M (1996) TrkA, but not TrkC, receptors are essential for survival of sympathetic neurons in vivo. J Neurosci 16:6208-6218.
24. Fagan AM, Suhr ST, Lucidi-Phillipi CA, Peterson DA, Holtzman DH, Gage FH (1997) Endogenous FGF-2 is important for cholinergic sprouting in the denervated hippocampus. J Neurosci 17:2499-2511.
25. Farinas I, Jones KR, Backus C, Wang X, Reichardt LF (1994) Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369:658-661.
26. Friedman WJ, Ibanez CF, Hallbook F, Persson H, Cain LD, Dreyfus CF, Black IB (1993) Differential actions of neurotrophins in the locus cocruleus and basal forebrain. Exp Neurol 119:72-78.
27. Gage FH, Tuszynski MH, Chen KS, Fagan AM, Higgins GA (1991) Nerve growth factor function in the central nervous system. In: Current topics in microbiology and immunology: neuronal growth factors (Bothwell M, ed), pp 71-93. Berlin: Springer.
28. Gallyas F, Wolff JR, Bottcher H, Zaborszky L (1980) A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system. Stain Technol 55:299-306.
29. Gnahn H, Hefti F, Heumann R, Schwab ME, Thoenen H (1983) NGF-mediated increase of cholinc acetyltransferase (ChAT) in the neonatal rat forebrain: evidence for a physiological role of NGF in the brain. Dev Brain Res 9:42-52.
30. Gundersen HJG (1986) Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson, J Microsc 143:3-45.
31. Hagg T, Vahlsing HL, Manthorpe M, Varon S (1990) Nerve growth factor infusion into the denervated adult rat hippocampal formation promotes its cholinergic reinnervation. J Neurosci 10:3087-3092.
32. Hagg T, Quon D, Higaki J, Varon S (1992) Ciliary neurotrophic factor prevents neuronal degeneration and promotes low affinity NGF receptor expression in the adult rat CNS. Neuron 8:145-158.
33. Hefti F, Hartikka J, Salvatierra A, Weiner WJ, Mash DC (1986) Localization of nerve growth factor receptors in cholinergic neurons of the human basal forebrain. Neurosci Lett 69:37-41.
34. Higgins GA, Koh S, Chen KS, Gage FH (1989) NGF induction of NGF receptor gene expression and cholinergic neuronal hypertrophy within the basal forebrain of the adult rat. Neuron 3:247-256.
35. Holtzman DM, Lowenstein DH (1995) Selective inhibition of axon out-growth by antibodies to NGF in a model of temporal lobe epilepsy. J Neurosci 15:7062-7070.
36. Holtzman DM, Li Y, Parada LF, Kinsman S, Chen CK, Valletta JS, Zhou J, Long J, Mobley WC (1992) pl40 mRNA marks NGF-responsive forebrain neurons: evidence that trk gene expression is induced by NGF. Neuron 9:465-478.
37. Holtzman DM, Kilbridge J, Bredt DS, Black SM, Li Y, Clary DO, Reichardt LF, Mobley WC (1994) NOS induction by NGF in basal forebrain cholinergic neurons: evidence for regulation of brain NOS by a neurotrophin. Neurobiol Dis 1:51-60.
38. Holtzman DM, Kilbridge J, Li Y, Cunningham ET, Lenn NJ, Clary DO, Reichardt LF, Mobley WC (1995) TrkA expression in the CNS: evidence for the existence of several novel NGF-responsive CNS neurons. J Neurosci 15:1567-1576.
39. Holtzman DM, Santucci D, Kilbridge J, Chua-Couzens J, Fontana DJ, Daniels SE, Johnson RM, Chen KS, Sun Y, Carlson E, Alleva E, Epstein CJ, Mobley WC (1996) Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc Natl Acad Sci USA 93:13333-13338.
40. Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD (1993) Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10:137-149.
41. Johnson EM, Gorin PG (1980) Dorsal root ganglion neurons are destroyed by exposure in utero to maternal antibody to nerve growth factor. Science 210:916-918.
42. Jones KR, Farinas I, Backus C, Reichardt LF (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-999.
43. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF (1991) The trk proto-oncogene product: a signal-transducing receptor for nerve growth factor. Science 252:554-558.
44. Klein R, Nanduri V, Jing SA, Lamballe F, Tapley P, Bryant S, Cordon-Cardo C, Jones KR, Reichardt LF, Barbacid M (1991) The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66:395-403.
45. Klein R, Smeyne RJ, Wurst W, Long LK, Auerback BA, Joyner AL, Barbacid M (1993) Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesion and neonatal death. Cell 75:113-122.
46. Klein R, Silos-Santiago I, Smeyne RJ, Lira SA, Brambilla R, Bryant S, Zhang L, Snider WD, Barbacid M (1994) Disruption of the neurotrophin-3 receptor gene trkC eliminates la muscle afferents and results in abnormal movements. Nature 368:249-251.
47. Knusel B, Winslow JW, Rosenthal A, Burton LE, Seid DP, Nikolies K, Hefti F (1991) Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin 3. Proc Natl Acad Sci USA 88:961-965.
48. Koliatsos VE, Price DL, Gouras GK, Cayouette MH, Burton LE, Winslow JW (1994) Highly selective effects of nerve growth factor, brain derived neurotrophic factor, and neurotrophin-3 on intact and injured basal forebrain magnocellular neurons. J Comp Neurol 343:247-262.
49. Lamballe F. Klein R. Barbacid M (1991) TrkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3, Cell 66:967-979.
50. Large TH, Bodary SC, Clegg DO, Weskamp G, Otten U, Reichardt LF (1986) Nerve growth factor gene expression in the developing rat brain. Science 234:352-355.
51. Lauterborn JC, Bizon JL, Tran TM, Gall CM (1995) NGF mRNA is expressed by GABAergic but not cholinergic neurons in rat basal forebrain. J Comp Neurol 360:454-462.
52. Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237:1154-1161.
53. Li Y, Holtzman DM, Kromer LF, Kaplan DR, Chua-Couzens J, Clary DO, Knusel B, Mobley WC (1995) Regulation of trkA and ChAT expression in developing rat basal forebrain: evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J Neurosci 15:2888-2905.
54. Liu X, Ernfors P, Wu H, Jaenisch R (1995) Sensory but not motor neuron deficits in mice lacking NT4 and BDNF, Nature 375:238-241.
55. Longo FM, Holtzman DM, Grimes ML, Mobley WC (1992) Nerve growth factor: actions in the peripheral and central nervous systems. In: Neurotrophic factors (Fallon J, Loughlin S, eds), pp 209-256. New York: Academic.
56. Lu B, Buck CR, Dreyfus CF, Black IB (1989) Expression of NGF and NGF receptor mRNAs in the developing brain: evidence for local delivery and action of NGF. Exp Neurol 104:191-199.
57. Martinez HJ, Dreyfus CF, Jonakait GM, Black IB (1985) Nerve growth factor promotes cholinergic development in brain striatal cultures. Proc Nail Acad Sci USA 82:7777-7781.
58. Meakin SO, Shooter EM (1991) Tyrosine kinase activity coupled to the high-affinity nerve growth factor-receptor complex. Proc Natl Acad Sci USA 88:5862-5866.
59. Milner TA, Loy R, Amaral DG (1983) An anatomical study of the development of the septohippocampal projection in the rat. Dev Brain Res 8:343-371.
60. Minichiello L, Klein R (1996) TrkB and TrkC neurotrophin receptors cooperate in promoting survival of hippocampal and cerebellar granule neurons. Genes Dev 10:2849-2858.
61. Mobley WC, Rutkowski JL, Tennekoon SJ, Buchanan K, Johnston MV (1985) Choline acetyltransferase in striatum of neonatal rats increased by nerve growth factor. Science 229:284-287.
62. Mobley WC, Rutkowski JL, Tennekoon GI, Gemski J, Buchanan K, Johnston MV (1986) Nerve growth factor increases choline acetyl-transferase activity in developing basal forebrain neurons. Mol Brain Res 387:53-62.
63. Mobley WC, Woo JE, Edwards RH, Riopelle RJ, Longo FM, Weskamp G, Otten U, Valletta JS, Johnston MV (1989) Developmental regulation of nerve growth factor and its receptor in the rat caudate-putamun. Neuron 3:655-664.
64. Olton D, Markowska A, Voytoko ML, Givens B, Gormon L, Wenk G (1991) Basal forebrain cholinergic system: a functional analysis. Adv Exp Med Biol 295:353-372.
65. Otto D, Frotscher M, Unsicker K (1989) Basic fibroblast growth factor and nerve growth factor administered in gelfoam rescue medial septal neurons after fimbria fornix transection. J Neurosci Res 22:83-91.
66. NGFR involved in developmental neural cell death? Dev Neurosci 16:207-211.
67. Rabizadeh S. Oh J, Zhong L, Yang J, Bitler CM, Butcher LL, Bredesen DE (1993) Induction of apoptosis by the low-affinity NGF receptor. Science 261:345-358.
68. Radeke MJ, Misko TP, Hsu C, Herzenberg LA, Shooter EM (1987) Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 325:593-597.
69. Richardson RT, DeLong MR (1988) A reappraisal of the functions of the nucleus basalis of Meynert. Trends Neurosci 11:264-267.
70. Rodriguez-Tebar A, Dechant G, Barde YA (1990) Binding of brain-derived neurotropic factor to the nerve growth factor receptor. Neuron 4:487-492.
71. Rodriguez-Tebar A, Dechant G, Gotz R, Barde YA (1992) Binding of neurotrophin-3 to its neuronal receptors and interactions with nerve growth factor and brain-derived neurotrophic factor. EMBO J 11:917-922.
72. Saffran BN, Woo JE, Mobley WC, Crutcher KA (1989) Intraventricular NGF infusion in the mature rat brain enhances sympathetic innervation of cerebrovascular targets but fails to elicit sympathetic ingrowth. Brain Res 492:245-254.
73. Schwarz M, Ikonomidou C, Klockgether T, Turski L, Ellenbroek B, Sontag KH (1986) The role of striatal cholinergic mechanisms for the development of limb rigidity: an electromyographic study in rats. Brain Res 373:378-381.
74. Silos-Santiago I, Molliver DC, Ozaki S, Smeyne RJ, Fagan AM, Barbacid M, Snider WD (1995) Non-TrkA-expressing small DRG neurons are lost in trkA deficient mice. J Neurosci 15:5929-5942.
75. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M (1994) Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368:246-249.
76. Snider WD (1994) Functions of the neurotrophins during development: what the knockouts are teaching us. Cell 77:627-638.
77. Sobreviela T, Clary DO, Reichardt LF, Brandabur MM, Kordower JH, Mufson EJ (1994) TrkA-immunoreactive profiles in the central nervous system: colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. J Comp Neurol 350:587-611.
78. Soppet D, Escandon E, Maragos J, Middlemas DS, Reid SW, Blair J, Burton LE, Stanton BR, Kaplan DR, Hunter T, Nikolics K, Parada LF (1991) The neurotrophic factors brain-derived neurotrophic factors and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65:895-903.
79. Squinto SP, Stitt TN, Aldrich TH, Davis S, Bianco SM, Radziejewski C, Glass DJ, Masiakowski P, Furth ME, Valenzuela DM, Distefano PS, Yancopoulos GD (1991) trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65:885-893.
80. Steininger TL, Wainer BH, Klein R, Barbacid M, Palfrey HC (1993) High-affinity nerve growth factor receptor (Trk) immunoreactivity is localized in cholinergic neurons of the basal forebrain and striatum in the adult rat brain. Brain Res 612:330-335.
81. Thoenen H (1991) The changing scene of neurotrophic factors. Trends Neurosci 14:165-170.
82. NGFR-deficient mice. Science 274:1729-1732.
83. Vantini G, Schavo N, DiMartino A, Polato P, Triban C, Callegaro L, Toffano G, Leon A (1989) Evidence for a physiological role for nerve growth factor in the central nervous system of neonatal rats. Neuron 3:267-273.
84. Weskamp G, Reichardt LF (1991) Evidence that biological activity of NGF is mediated through a novel subclass of high-affinity receptors. Neuron 6:649-663.
85. West MJ (1993) New stereological methods for counting neurons. Neurobiol Aging 14:275-285.
86. Whittemore SR, Ebendal T, Larkfors L, Olson L, Seiger A, Stromberg I, Persson H (1986) Developmental and regional expression of beta-nerve growth factor messenger RNA and protein in the rat central nervous system. Proc Natl Acad Sci USA 83:817-821.