p75(NTR) immunoreactivity in the rat dentate gyrus is mostly within presynaptic profiles but is also found in some astrocytic and postsynaptic profiles

Journal of Comparative Neurology

Volumn 407, Issue 1, 1999, Pages 77-91

  Dougherty, Karen D ^a   Milner, Teresa A ^b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Electron microscopy; Glia; Granule cells; Neurotrophin receptors; Septohippocampal pathway

Indexed keywords

NEUROTROPHIN RECEPTOR; IMMUNOGLOBULIN G; NERVE GROWTH FACTOR RECEPTOR;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DENTATE GYRUS; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; ANIMAL; CYTOLOGY; DENDRITE; IMMUNOELECTRON MICROSCOPY; METABOLISM; NERVE CELL; NERVE FIBER; SPRAGUE DAWLEY RAT; SYNAPSE; SYNAPTOSOME; ULTRASTRUCTURE;

ANIMALS; ASTROCYTES; AXONS; DENDRITES; DENTATE GYRUS; IMMUNOGLOBULIN G; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, IMMUNOELECTRON; NEURONS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, NERVE GROWTH FACTOR; RECEPTORS, NERVE GROWTH FACTOR; SYNAPSES;

EID: 0033611825     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990428)407:1<77::AID-CNE6>3.0.CO;2-S     Document Type: Article

References (88)

1. Alonso A, Köhler C. 1984. A study of the reciprocal connections between the septum and the entorhinal area using anterograde and retrograde axonal transport methods in the rat brain. J Comp Neurol 225:327-343.
2. Amaral DG, Kurz J. 1985. An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J Comp Neurol 240:37-59.
3. Appel SH. 1981. A unifying hypothesis for the cause of amyotrophic lateral sclerosis, Parkinsonism, and Alzheimer's disease. Ann Neurol 10:499-505.
4. Barde YA, Edgar D, Thoenen H. 1982. Purification of a new neurotrophic factor from mammalian brain. EMBO J 1:549-553.
5. NTR reduces NGF binding to trkA on PC12 cells. Neuron 13:203-215.
6. Barrett GL, Georgiou A. 1996. The low-affinity nerve growth factor receptor p75 mediates death of PC12 cells after nerve growth factor withdrawal. J Neurosci Res 45:117-128.
7. Bernard P, Martinez HJ, Dreyfus CF, Black IB. 1988. Localization of high-affinity and low-affinity nerve growth factor receptors in cultured rat basal forebrain. Neuroscience 26:121-129.
8. Canossa M, Twiss JL, Verity AN, Shooter EM. 1997. p75 NGFR and trkA receptors collaborate to rapidly activate a p75 NGFR-associated protein kinase. EMBO J 15:3369-3376.
9. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV. 1996. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383:716-719.
10. Chan J, Aoki C, Pickel VM. 1990. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J Neurosci Methods 33: 113-127.
11. Chandler CE, Parsons LM, Hosang H, Shooter EM. 1984. A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells. J Biol Chem 259:6882-6889.
12. Clarke DJ. 1985. Cholinergic innervation of the rat dentate gyrus: an immunocytochemical and electron microscopical study. Brain Res 360: 349-354.
13. Cordon-Cardo C, Tapley P, Jing S, Nanduri V, O'Rourke E, Lamballe F, Kovary K, Klein R, Jones KR, Reichardt LF, Barbacid, M. 1991. The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell 66:173-183.
14. Dawbarn D, Allen SJ, Semenenko FM. 1988. Coexistence of choline acetyl-transferase and nerve growth factor receptors in the rat basal forebrain. Neurosci Lett 94:138-144.
15. Dobrowsky RT, Jenkins GM, Hannum YA. 1995. Neurotrophins induce sphingomyelin hydroysis-modulation by co-expression of p75(ntr) with trk receptors. J Biol Chem 270:135-145.
16. Ehlers MD, Kaplan DR, Price DL, Koliatsos VE. 1995. NGF-stimulated retrograde transport of trkA in the mammalian nervous system. J Cell Biol 130:149-156.
17. Ernfors P, Wetmore C, Olson L, Persson H. 1990. Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5:511-526.
18. Ferrari G, Fabris M, Fiori MG, Gabellini N, Volonte C. 1992. Gangliosides prevent the inhibition by K-252a of NGF responses in PC12 cells. Dev Brain Res 65:35-42.
19. Fischer W, Wictorin K, Bjorklund A, Williams LR, Varon S, Gage FH. 1987. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329:65-68.
20. Frade JM, Rodriguez-Tebar A, Barde YA. 1996. Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 383:166-168.
21. Frotscher M, Leranth C. 1985. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopy study. J Comp Neurol 239:237-246.
22. Gage FH, Armstrong DM, Williams LR, Varon S. 1988. Morphological response of axotomized septal neurons to nerve growth factor. J Comp Nourol 269:147-155.
23. NGFr and up-regulation by nerve growth factor. J Comp Neurol 341:324-339.
24. Gilad GM, Gilad VH. 1995. Chemotaxis and accumulation of nerve growth factor by microglia and macrophages. J Neurosci Res 41:594-602.
25. Goldschmidt RB, Steward O. 1980. Preferential neurotoxicity of colchicine for granule cells of the dentate gyrus of the adult rat. Proc Natl Acad Sci USA 77:3047-3051.
26. Grimes ML, Zhou J, Beattie EC, Yuen EC, Hall D, Valletta JS, Topp KS, LaVail JH, Bunnett NW, Mobley WC. 1996. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J Neurosci 16:7950-7964.
27. Grove J, Gomez J, Kentroti S, Vernadakis A. 1998. Plasticity of astrocytes derived from aged mouse cerebral hemispheres: changes with cell passage and immortalization. Brain Res 39:211-217.
28. Hallbook F, Ibanez CF, Persson H. 1991. Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6:845-858.
29. Hefti F, Werner WJ. 1986. Nerve growth factor and Alzheimer's disease. Ann Neurol 20:275-281.
30. Hefti F, Hartikka J, Salvatierra A, Weiner W, Mash D. 1986. Localization of nerve growth factor receptors in cholinergic neurons of the human basal forebrain. Neurosci Lett 69:37-41.
31. Hefti F, Hartikka J, Knusel B. 1989. Function of neurotrophic factors in the adult and aging brain and their possible use in the treatment of neurodegenerative diseases. Neurobiol Aging 10:515-533.
32. Heumann R, Schwab ME, Merkl R, Thoenen H. 1984. Nerve growth factor-mediated induction of choline acetyltransferase in PC12 cells: evaluation of the site of action of nerve growth factor and the involvement of lysosomal degradation products of nerve growth factor. J Neurosci 4:3039-3050.
33. Hsu SM, Raine L, Danger H. 1981. The use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (peroxidase) procedures. J Histochem Cytochem 29:577-590.
34. Jing S, Tapley P, Barbacid M. 1992. Nerve growth factor mediates signal transduction through trk homodimer receptors. Neuron 9:1067-1079.
35. Johnson EM, Taniuchi M, Clark HB, Springer JE, Koh S, Tayrien MW, Loy R. 1987. Demonstration of the retrograde transport of nerve growth factor receptor in the peripheral and central nervous system. J Neurosci 7:923-929.
36. Junier MP, Suzuki F, Onteniente B, Peschanski M. 1994. Target-deprived CNS neurons express the NGF gene while reactive glia around their axonal terminals contain low and high affinity NGF receptors. Brain Res Mol Brain Res 24:247-260.
37. Kawaja MD, Gage FH. 1991. Nerve growth factor receptor immunoreactivity in the rat septohippocampal pathway: a light and electron microscopy investigation. J Comp Neurol 307:517-529.
38. Kerwin JM, Morris CM, Oakley A, Perry RH, Perry EK. 1991. Distribution of nerve growth factor receptor immunoreactivity in the human hippocampus. Neurosci Lett 121:178-182.
39. Kerwin JM, Morris CM, Perry RH, Perry EK. 1992. Hippocampal nerve growth factor receptor immunoreactivity in patients with Alzheimer's disease and Parkinson's disease. Neurosci Lett 143:101-104.
40. Knipper M, Leung LS, Zhao D, Rylett RJ. 1994. Short-term modulation of glutamatergic synapses in adult rat hippocampus by NGF. NeuroReport 5:2433-2436.
41. Knusel B, Hefti F. 1992. K-252 compounds: modulators of neurotrophin signal transduction. J Neurochem 59:1987-1996.
42. Kornfeld S, Mellman I. 1989. The biogenesis of lysosomes. Annu Rev Cell Biol 5:483-525.
43. Kromer LF. 1987. Nerve growth treatment after brain injury prevents neuronal death. Science 225:214-216.
44. Kuffler SW. 1967. Neuroglial cells: physiological properties and a potassium-mediated effect of neuronal activity on the glia membrane potential. Proc R Soc Lond 168:1-21.
45. Kumar S, Pena LA, de Villis J. 1993. CNS glial cells express neurotrophin receptors whose levels are regulated by NGF. Brain Res Mol Brain Res 17:163-168.
46. Lamballe F, Klein R, Barbacid M. 1991. trkC, a new member of the family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66:967-979.
47. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsaki G. 1994. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033-1047.
48. Levi-Montalcini R, Hamburger V. 1951. Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J Exp Zool 116:321-361.
49. Levine ES, Dreyfus CF, Black IB, Plummer MR. 1995. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc Natl Acad Sci USA 92:8074-8077.
50. Levine ES, Dreyfus CF, Black IB, Plummer MR. 1996. Selective role for trkB neurotrophin receptors in rapid modulation of hippocampal synaptic transmission. Mol Brain Res 38:300-303.
51. Lewis PR, Shute CCD. 1967. The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system and the subfornical organ and supraoptic crest. Brain 90:521-540.
52. 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.
53. Loy R, Clagett-Dame M, DiStefano PS. 1990. Localization of NGF receptors in normal and Alzheimer's basal forebrain with monoclonal antibodies against the truncated form of the receptor. J Neurosci Res 27:651-664.
54. Maisonpierre PC, Belluscio L, Squinto SP, Ip NY, Furth ME, Lindsay RM, Yancopoulos GD. 1990. Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247:1446-1451.
55. Mandel RJ, Gage FH, Thal LJ. 1989. Spatial learning in rats: correlation with cortical choline acetyltransferase and improvement with NGF following NBM damage. Exp Neurol 104:208-217.
56. Martinez-Murillo R, Fernandez T, Alguacil MM, Aguado F, Achaval M, Bovolenta P, Rodrigo J, Nieto-Sampedro M. 1991. Subcellular localization of nerve growth factor receptors in identified cells of the rat nucleus basalis magnocellularis: an immunocytochemical study. Neuroscience 42:463-472.
57. 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.
58. Milner TA, Wiley RG, Kurucz OS, Prince SR, Pierce JP. 1997. Selective changes in hippocampal neuropeptide Y neurons following removal of the cholinergic septal inputs. J Comp Neurol 386:46-59.
59. 2A-adrenergic receptors are located predominantly presynaptically but are also found postsynaptically and in selective astrocytes. J Comp Neurol 395:310-327.
60. Mufson EJ, Conner JM, Varon S, Kordower JH. 1994. Nerve growth factor-like immunoreactive profiles in the primate basal forebrain and hippocampal formation. J Comp Neurol 341:507-519.
61. Mufson EJ, Conner JM, Kordower JH. 1995. Nerve growth factor in Alzheimer's disease: defective retrograde transport to nucleus basalis. NeuroReport 6:1063-1066.
62. Parada LF, Tsoulfas P, Tessarollo L, Blair J, Reid SW, Soppet D. 1992. The Trk family of tyrosine kinases: receptors for NGF-related neurotrophins. Cold Spring Harbor Symp Quant Biol 57:43-51.
63. Peters, A., Palay SL, Webster HD. 1991. The Fine Structure of the Nervous System, 3rd ed. New York: Oxford University Press.
64. Pioro EP, Cuello AC. 1990. Distribution of NGF receptor-like immunoreactivity in the adult rat CNS: effect of colchicine and correlation with the cholinergic system. I. Forebrain. Neuroscience 34:57-87.
65. Pioro EP, Ribeiro-da-Silva A, Cuello AC. 1990. Immunoelectron microscopic evidence of nerve growth factor receptor metabolism and internalization in rat nucleus basalis neurons. Brain Res 527:109-115.
66. 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 261:345-348.
67. Rudge JS, Alderson RF, Pasnikowski E, McClain J, Ip NY, Landsay RM. 1992. Expression of ciliary neurotrophic factor and neurotrophins -nerve growth factor, brain-derived nerve growth factor, and neurotrophin-3 in cultured rat hippocampal astrocytes. Eur J Neurosci 4:459-471.
68. Rudge JS, Pasnikowski E, Holst P, Lindsay RM. 1995. Changes in neurotrophic factor expression and receptor activation following exposure of hippocampal neuron/astrocyte cocultures to kainic acid. J Neurosci 15:6856-6867.
69. Saporito MS, Carswell S. 1995. High levels of synthesis and local effects of nerve growth factor in the septal region of the adult rat brain. J Neurosci 15:2280-2286.
70. Seiler M, Schwab ME. 1984. Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Res 300:33-39.
71. 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.
72. 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.
73. Springer JE. 1988. Nerve growth factor receptors in the central nervous system. Exp Neurol 102:354-365.
74. Springer JE, Robbins E, Meyer S, Baldino F, Lewis ME. 1990. Localization of nerve growth factor receptor mRNA in the rat basal forebrain with in situ hybridization histochemistry. Cell Mol Neurobiol 10:33-39.
75. Squinto SP, Stitt TN, Aldrich TH, Davis S, Bianco SM, Radziejewski C, Glass DJ, Masiakowski P, Furth ME, Valenzuela DM, Di Stefano PS, Yancopoulor, GD. 1991. TrkB encodes a functional receptor for brain-derived neurotrophin factor and neurotrophin-3 but not nerve growth factor. Cell 65:885-893.
76. Steckler T, Keith AB, Wiley RG, Sahgal A. 1995. Cholinergic lesions by 192-IgG saporin and short term memory: role of the septohippocampal projection. Neuroscience 66:101-114.
77. Torres EM, Perry TA, Blokland A, Wilkinson LS, Wiley RG, Lappi DA, Dunnett SB. 1994. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the nasal forebrain cholinergic system. Neuroscience 63:95-122.
78. Venkatesan C, Song XZ, Go CG, Kurose H, Aoki C. 1996. Cellular and subcellular distribution of alpha2-adrenergic receptors in the visual cortex of neonatal and adult rats. J Comp Neurol 365:79-95.
79. Veznedaroglu E, Milner TA. 1992. Elimination of artifactual labeling of hippocampal mossy fibers seen following pre-embedding immunogold-silver technique by pretreatment with zinc chelator. Microsc Res Tech 23:100-101.
80. Walsh TJ, Herzog CD, Gandhi C, Stackman RW, Wiley RG. 1996. Injection of IgG 192-saporin into medial septum produces cholinergic hypofunction and dose-dependent working memory deficits. Brain Res 726: 69-79.
81. Whitehouse PJ, Price DL, Clark AW, Coyle JT, DeLong MR. 1981. Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann Neurol 10:122-126.
82. Wiley RG, Oeltmann TN, Lappi DA. 1991. Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res 562:149-153.
83. Winn SR, Hammang JP, Emerich DF, Lee A, Palmiter RD, Baetge EE. 1994. Polymer-encapsulated cells genetically modified to secrete human nerve growth factor promote the survival of axotomized septal cholinergic neurons. Proc Natl Acad Sci USA 91:2324-2328.
84. Woolf NJ, Gould E, Butcher LL. 1989. Nerve growth factor receptor is associated with cholinergic neurons of the basal forebrain but not the pontomesenscephalon. Neuroscience 30:143-152.
85. NTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. J Neurosci 17:7594-7605.
86. Yokoyama M, Black IB, Dreyfus CF. 1993. NGF increases brain astrocyte number in culture. Exp Neurol 124:377-380.
87. Yoon SO, Casaccia-Bonnefil P, Carter B, Chao MV. 1998. Competitive signaling between trkA and p75 nerve growth factor receptors determines cell survival. J Neurosci 18:3273-3281.
88. Zhou J, Valletta JS, Grimes ML, Mobley WC. 1995. Multiple levels for regulation of trkA in PC12 cells by nerve growth factor. J Neurochem 65:1146-1156.