Increased NGF proforms in aged sympathetic neurons and their targets

Neurobiology of Aging

Volumn 28, Issue 1, 2007, Pages 122-134

  Bierl, Michael A ^a   Isaacson, Lori G ^a  

^a MIAMI UNIVERSITY   (United States)

Author keywords

Extracerebral blood vessels; Heart; Iris; Nerve growth factor; Neurotrophin 3; Pineal gland; Proneurotrophin; proNT 3; RT PCR; Superior cervical ganglion; Western blot analysis

Indexed keywords

MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN 3;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGING; CONTROLLED STUDY; FEMALE; IRIS; NEUROCHEMISTRY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; RAT; REGULATORY MECHANISM; SUPERIOR CERVICAL GANGLION; SYMPATHETIC INNERVATION; SYMPATHETIC NERVE;

AGING; ANIMALS; CELLS, CULTURED; DRUG DELIVERY SYSTEMS; FEMALE; NERVE GROWTH FACTOR; NEURONS; NEUROTROPHIN 3; PROTEIN ISOFORMS; RATS; RATS, INBRED F344; SYMPATHETIC NERVOUS SYSTEM; TISSUE DISTRIBUTION; TRANS-ACTIVATION (GENETICS); UP-REGULATION;

EID: 33751208303     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2005.11.008     Document Type: Article

References (96)

1. Andrews T.J., Thrasivoulou C., Nesbit W., and Cowen T. Target-specific differences in the dendritic morphology and neuropeptide content of neurons in the rat SCG during development and aging. J Comp Neurol 368 1 (1996) 33-44
2. Beattie M.S., Harrington A.W., Lee R., Kim J.Y., Boyce S.L., Longo F.M., et al. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36 (2002) 375-386
3. Bellinger D.L., Ackerman K.D., Felten S.Y., and Felten D.L. A longitudinal study of age-related loss of noradrenergic nerves and lymphoid cells in the rat spleen. Exp Neurol 116 3 (1992) 295-311
4. Benedetti M., Levi A., and Chao M.V. Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. PNAS 90 (1993) 7859-7863
5. Berger E.A., and Shooter E.M. Evidence for pro-β-nerve growth factor, a biosynthetic precursor to β-nerve growth factor. PNAS 74 9 (1977) 3647-3651
6. Bergman E., Fundin B.T., and Ulfhake B. Effects of aging and axotomy on the expression of neurotrophin receptors in primary sensory neurons. J Comp Neurol 410 (1999) 368-386
7. Biedenbach M.A., Kalu D.N., and Herbert D.C. Effects of aging and food restriction on the trigeminal ganglion-a morphometric study. Mech Aging Dev 65 2/3 (1992) 111-125
8. Bierl MA, Isaacson LG. Altered proneurotrophin expression in aged sympathetic ganglia and target tissues, Program No. 727.13. 2004 Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, DC, 2004 [Online].
9. Bierl M.A., Jones E.E., Crutcher K.A., and Isaacson L.G. 'Mature' nerve growth factor is a minor species in most peripheral tissues. Neurosci Lett 380 (2005) 133-137
10. Bjorling D.E., Beckman M., Clayton M.K., and Wang Z.-Y. Modulation of nerve growth factor in peripheral organs by estrogen and progesterone. Neuroscience 110 1 (2002) 155-167
11. Bronfman F.C., and Fainzilber M. Multi-tasking by the p75 neurotrophin receptor: sortilin things out?. EMBO Reports 5 9 (2004) 867-871
12. Bruzzone P., Cavallotti C., Mancone M., and Tranquilli Leali F.M. Age-related changes in catecholaminergic nerve fibers of rat heart and coronary vessels. Gerontology 49 (2003) 80-85
13. Butowt R., and von Bartheld C.S. Sorting of internalized neurotrophins into an endocytic transcytosis pathway via the Golgi system: ultrastructural analysis in retinal ganglion cells. J Neurosci 21 22 (2001) 8915-8930
14. Chakrabarti S., Sima A.A.F., Lee J., Brachet P., and Dicou E. Nerve growth factor (NGF), proNGF and NGF receptor-like immunoreactivity in BB rat retina. Brain Res 523 (1990) 11-15
15. Chao M.V., and Bothwell M. Neurotrophins: to cleave or not to cleave. Neuron 33 1 (2002) 9-12
16. Chen Y., Dicou E., and Djakiew D. Characterization of nerve growth factor precursor protein expression in rat round spermatids and the trophic effects of nerve growth factor in maintenance of Sertoli cell viability. Mol Cell Endocrinol 127 (1997) 129-136
17. Cowen T., and Gavazzi I. Plasticity in adult and ageing sympathetic neurons. Prog Neurobiol 54 (1998) 249-288
18. Cowen T., Gavazzi I., Weingartner J., and Crutcher K.A. Levels of NGF protein do not correlate with changes in innervation of the rat iris in old age. Neuroreport 7 13 (1996) 2216-2220
19. Cowen T., Woodhoo A., Sullivan C.D., Jolly R., Crutcher K.A., Wyatt S., et al. Reduced age-related plasticity of neurotrophin receptor expression in selected sympathetic neurons of the rat. Aging Cell 2 1 (2003) 59-69
20. Crowley C., Spencer S.D., Nishimura M.C., Chen K.S., Pitts-Meek S., Armanini M.P., et al. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76 6 (1994) 101-111
21. Darling T.L.J., Petrides P.E., Beguin P., Frey P., Shooter E.M., Selby M., et al. The biosynthesis and processing of proteins in the mouse 7S nerve growth factor complex. Cold Spring Harb Sym 48 Pt 1 (1993) 427-434
22. Davis B.M., Wang H.S., Albers K.M., Carlson S.L., Goodness T.P., and McKinnon D. Effects of NGF overexpression on anatomical and physiological properties of sympathetic postganglionic neurons. Brain Res 724 (1996) 47-54
23. DeCouto S.A., Jones E.E., Kudwa A.E., Shoemaker S.E., Shafer A.J., Brieschke M.A., et al. The effects of deafferentation and exogenous NGF on neurotrophins and neurotrophin receptor mRNA expression in the adult superior cervical ganglion. Mol Brain Res 119 (2003) 73-82
24. Delsite R., and Djakiew D. Characterization of nerve growth factor precursor protein expression by human prostate stromal cells: a role in selective neurotrophin stimulation of prostate epithelial cell growth. Prostate 41 (1999) 39-48
25. Deshmukh M., and Johnson Jr. E.M. Programmed cell death in neurons: focus on the pathway of nerve growth factor deprivation-induced death of sympathetic neurons. Mol Pharmacol 51 6 (1997) 897-906
26. Dickason A.K., and Isaacson L.G. Plasticity of aged perivascular axons following exogenous NGF: analysis of catecholamines. Neurobiol Aging 23 (2002) 125-134
27. Dicou E. Nerve growth factor precursors in the rat thyroid and hippocampus. Mol Brain Res 14 (1992) 136-138
28. Dicou E., Lee J., and Brachet P. Synthesis of nerve growth factor mRNA and precursor protein in the thyroid and parathyroid glands of the rat. PNAS 83 (1986) 7084-7088
29. Ebendal T., Olson L., and Seiger A. The level of nerve growth factor (NGF) as a function of innervation. A correlation radio immunoassay and bioassay study of the rat iris. Exp Cell Res 148 2 (1983) 311-317
30. Edwards R.H., Selby M.J., Garcia P.D., and Rutter W.J. Processing of the native nerve growth factor precursor to form biologically active nerve growth factor. J Biol Chem 263 14 (1988) 6810-6815
31. Edwards R.H., Selby M.J., Mobley W.C., Weinrich S.L., Hruby D.E., and Rutter W.J. Processing and secretion of nerve growth factor: expression in mammalian cells with a vaccinia virus vector. Mol Cell Biol 8 6 (1988) 2456-2464
32. Edwards R.H., Selby M.J., and Rutter W.J. Differential RNA splicing predicts two distinct nerve growth factor precursors. Nature 319 27 (1986) 784-787
33. Egger B, Reinshagen M, Geerling I, Huff K, Vijaya SR, Lakshmanan J, Identification of nerve growth factor prohormone isoforms in gastric juice of rats. Gastroenterology 1998; 114(4):A877, G3597, Part 2 Suppl S.
34. Fahnestock M., Michalski B., Xu B., and Coughlin M.D. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol Cell Neurosci 18 (2001) 210-220
35. Fahnestock M., Yu G., Michalski B., Mathew S., Colquhoun A., Ross G.M., et al. The nerve growth factor precursor proNGF exhibits neurotrophic activity but is less active than mature nerve growth factor. J Neurochem 89 (2004) 581-592
36. Farhadi H.F., Mowla S.J., Petrecca K., Morris S.J., Seidah N.G., and Murphy R.A. Neurotrophin-3 sorts to the constitutive secretory pathway of hippocampal neurons and is diverted to the regulated secretory pathway by coexpression with brain-derived neurotrophic factor. J Neurosci 20 11 (2000) 4059-4068
37. Farhadi H., Pareek S., Day R., Dong W., Chrétien M., Bergeron J.J.M., et al. Prohormone convertases in mouse submandibular gland: Co-localization of furin and nerve growth factor. J Histochem Cytochem 45 6 (1997) 795-804
38. 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 6482 (1994) 658-661
39. Francis N., Farinas I., Brennan C., Rivas-Plata K., Backus C., Reichardt L., et al. NT-3, like NGF, is required for survival of sympathetic neurons, but not their precursors. Dev Biol 210 (1999) 411-427
40. Fundin B.T., Bergman E., and Ulfhake B. Alterations in mystacial pad innervation in the aged rat. Exp Brain Res 117 (1997) 324-340
41. Gatzinsky K.P., Haugland R.P., Thrasivoulou C., Orike N., Budi-Santoso A.W., and Cowen T. p75 and TrkA receptors are both required for uptake of NGF in adult sympathetic neurons: use of a novel fluorescent NGF conjugate. Brain Res 920 (2001) 226-238
42. Gatzinsky K.P., Thrasivoulou C., Campioni-Noack M., Underwood C., and Cowen T. The role of NGF uptake in selective vulnerablility to cell death in ageing sympathetic neurons. Eur J Neurosci (2004) 2848-2856
43. Gavazzi I., Canavan R.E.M., and Cowen T. Influence of age and anti-nerve growth factor treatment on the sympathetic and sensory innervation of the rat iris. Neuroscience 73 4 (1996) 1069-1079
44. Gavazzi I., Railton K.L., Ong E., and Cowen T. Responsiveness of sympathetic and sensory iridial nerves to NGF treatment in young and aged rats. Neurobiol Aging 22 (2001) 287-297
45. Greene L.A. Quantitative in vitro studies on the nerve growth factor (NGF) requirement of neurons. Dev Biol 58 1 (1977) 96-105
46. Greene L.A., Seeley P.J., Rukenstein A., DiPiazza M., and Howard A. Rapid activation of tyrosine hydroxylase in response to nerve growth factor. J Neurochem (1984) 1728-1734
47. Harrington A.W., Leiner B., Blechschmitt C., Arevalo J.C., Lee R., Mörl K., et al. Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. PNAS 101 16 (2004) 6226-6230
48. Hasan W., Pedchenko T., Krizsan-Agbas D., Baum L., and Smith P.G. Sympathetic neurons synthesize and secrete pro-nerve growth factor protein. J Neurobiol 57 (2003) 38-53
49. Huff K., Reinshagen M., Geerling I., and Soinila S. Localization of neurotrophin-3 prohormone isoforms in developing and adult rat hippocampus and cerebellum. Ann Neurol 42 3 (1997) 1
50. Isaacson LG, Maynard LM, Jones EE. Aged sympathetic neurons show increased NT3 protein expression. Soc Neurosci Abs Viewer 2003;No 302.8.
51. Kaye D., and Esler M. Sympathetic neuronal regulation of the heart in aging and heart failure. Cardiovascular Res 38 (2005) 145-152
52. Kendall S., Yeo M., Henttu P., and Tomlinson D.R. Alternative splicing of the neurotrophin-3 gene gives rise to different transcripts in a number of human and rat tissues. J Neurochem 75 (2000) 41-47
53. Kuchel G.A. Alterations in target innervation and collateral sprouting in the aging sympathetic nervous system. Exp Neurol 124 (1993) 381-386
54. Kuchel G.A., Crutcher K.A., Naheed U., Thrasivoulou C., and Cowen T. NGF expression in the aged rat pineal gland does not correlate with loss of sympathetic axonal branches and varicosities. Neurobiol Aging 20 (1999) 685-693
55. Kuchel G.A., Rowe W., Meaney M.J., and Richard C. Neurotrophin receptor and tyrosine hydroxylase gene expression in aged sympathetic neurons. Neurobiol Aging 18 1 (1997) 67-79
56. Kudwa A.E., Shoemaker S.E., Crutcher K.A., and Isaacson L.G. Evidence for reduced accumulation of exogenous neurotrophin by aged sympathetic neurons. Brain Res 948 (2002) 24-32
57. 4. Nature 227 (1970) 680-685
58. Lakshmanan J., Beattie G.M., Hayek A., Burns C., and Fisher D.A. Biological actions of 53 kDa nerve growth factor as studied by a blot and culture technique. Neurosci Lett 99 (1989) 263-267
59. Lee R., Kermani P., Teng K.K., and Hempstead B.L. Regulation of cell survival by secreted proneurotrophins. Science 294 (2001) 1945-1948
60. Leingartner A., and Lindholm D. Two promoters direct transcription of the mouse NT-3 gene. Eur J Neurosci 6 7 (1994) 1149-1159
61. Levi-Montalcini R. The nerve growth factor 35 years later. Science 237 4819 (1987) 1154-1162
62. Levi-Montalcini R., and Booker B. Destruction of sympathetic ganglia in mammals by an antiserum to a nerve-growth protein. PNAS 46 3 (1960) 384-391
63. Levi-Montalcini R., and Booker B. Excessive growth of sympathetic ganglia evoked by a protein isolated from mouse salivary glands. PNAS 46 3 (1960) 373-384
64. Lobos E., Gebhardt C., Kluge A., and Spanel-Borowski K. Expression of nerve growth factor (NGF) isoforms in the rat uterus during pregnancy: accumulation of precursor proNGF. Endocrinology 146 4 (2005) 1922-1929
65. Loudes C., Petit F., Kordon C., and Faivre-Bauman A. Distinct populations of hypothalamic dopaminergic neurons exhibit differential responses to brain-derived neurotrophic factor (BDNF) and neurotrophin-3 (NT3). Eur J Neurosci 11 (1999) 617-624
66. Lu B. Pro-region of neurotrophins: role in synaptic modulation. Neuron 39 (2003) 735-738
67. MacGrogen D., Després G., Romand R., and Dicou E. Expression of the β-nerve growth factor gene in male sex organs of the mouse, rat, and guinea pig. J Neurosci Res 28 (1991) 567-573
68. Madden K.S., Rajan S., Bellinger D.L., Felten S.Y., and Felten D.L. Age-associated alterations in sympathetic neural interactions with the immune system. Develop Comp Immunol 21 6 (1997) 479-486
69. Martin D.P., Schmidt R.E., DiStefano P.S., Lowry O.H., Carter J.G., and Johnson Jr. E.M. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol 106 3 (1988) 829-844
70. Michalski B., and Fahnestock M. Pro-brain-derived neurotrophic factor is decreased in parietal cortex in Alzheimer's disease. Mol Brain Res 111 (2003) 148-154
71. Mitsiadis T.A., Couble P., Dicou E., Rudkin B.B., and Magloire H. Patterns of nerve growth factor (NGF), proNGF, and p75 NGF receptor expression in the rat incisor: comparison with expression in the molar. Differentiation 54 (1993) 161-175
72. Mobley W.C., Schenker A., and Shooter E.M. Characterization and isolation of proteolytically modified nerve growth factor. Biochemistry 25 25 (1976) 5543-5552
73. Murphy R.A., Singer R.H., Saide J.D., Pantazis N.J., Blanchard M.H., Byron K.S., et al. Synthesis and secretion of a high molecular weight form of nerve growth factor by skeletal muscle cells in culture. PNAS 74 10 (1977) 4496-4500
74. Nykjaer A., Lee R., Teng K.K., Jansen P., Madsen P., Nielsen M.S., et al. Sortilin is essential for proNGF-induced neuronal death. Nature 427 6977 (2004) 843-848
75. Pedraza C.E., Podlesniy P., Vidal N., Arévalo J.C., Lee R., Hempstead B., et al. ProNGF isolated from the human brain affected by Alzheimer's disease induces neuronal apoptosis mediated by p75NTR. Am J Path 166 2 (2005) 533-543
76. Peng S., Wuu J., Mufson E.J., and Fahnestock M. Increased proNGF levels in subjects with mild cognitive impairment and mild Alzheimer's disease. J Neuropath Exp Neurol 63 6 (2004) 641-649
77. Reinshagen M., Geerling I., Eysselein V.E., Adler G., Huff K.R., Morre G.P., et al. Commercial recombinant human β-nerve growth factor and adult rat dorsal root ganglia contain an identical molecular species of nerve growth factor prohormone. J Neurochem 74 (2000) 2127-2133
78. Reinshagen M, Geerling I, Huff KR. Localization of NT-3 prohormone in adult rat dorsal root ganglion (DRG), superior cervical ganglion (SCG), and hippocampus. Soc Neurosci Abs Viewer 2002;No. 732.3.
79. Reinshagen M., Geerling I., Lakshmana J., Rohm H., Lutz M.P., Soinila S., et al. Commercial mouse and human nerve growth factors contain nerve growth factor prohormone isoforms. J Neurosci Meth 76 (1997) 75-81
80. Reuss S. Trigeminal innervation of the mammalian pineal gland. Micro Res Tech 46 (1999) 305-309
81. 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 7 (1990) 2412-2419
82. Rush R.A., Chie E., Liu D., Tafreshi A., Zettler C., and Zhou X.F. Neurotrophic factors are required by mature sympathetic neurons for survival, transmission and connectivity. Clin Exp Pharmacol P 24 8 (1997) 549-555
83. Saboori A.M., and Young M. Nerve growth factor: biosynthetic products of the mouse salivary glands. Characterization of stable high molecular weight and 32,000-dalton nerve growth factors. Biochemistry 25 19 (1986) 5565-5571
84. Seidah N.G., Benjannet S., Pareek S., Chrétien M., and Murphy R.A. Cellular processing of the neurotrophin precursors of NT3 and BDNF by the mammalian proprotein convertases. FEBS Lett 379 (1996) 247-250
85. Seidah N.G., Benjannet S., Pareek S., Savaria D., Hamelin J., Goulet B., et al. Cellular processing of the nerve growth factor precursor by the mammalian pro-protein convertases. Biochem J 314 (1996) 951-960
86. Sekimoto M., Fukamachi K., Nemoto F., Miyata S., Degawa M., Senba E., et al. Novel alternative splicing in the 5′ exon of the neurotrophin-3 gene. Mol Neurosci 9 (1998) 3675-3679
87. Shoemaker S.E., and Isaacson L.G. Nerve growth factor mediates the formation of sensory pericellular baskets in the rat trigeminal ganglion. Neurosci Lett 331 (2002) 183-187
88. Soinila J., Salo A., Uusitalo H., Yanaihara N., and Happola O. CGRP-immunoreactive sensory nerve fibers in the submandibular gland of the rat. Histochemistry 91 6 (1989) 455-460
89. Suenga M., Ohmae H., Tsuji S., Takashi I., and Nishimura O. Renaturation of recombinant human neurotrophin-3 from inclusion bodies using an aggregation suppressor. Biotechnol Appl Biochem 28 (1998) 119-124
90. Tafreshi A.P., Zhou X.-F., and Rush R.A. Endogenous nerve growth factor and neurotrophin-3 act simultaneously to ensure the survival of postnatal sympathetic neurons in vivo. Neuroscience 83 2 (1998) 373-380
91. Thrasivoulou C., and Cowen T. Regulation of rat sympathetic nerve density by target tissues and NGF in maturity and old age. Eur J Neurosci 7 3 (1995) 381-387
92. Westergaard U.B., Kirkegaard K., Sørensen E.S., Jacobsen C., Nielsen M.S., Petersen C.M., et al. SorCS3 does not require propeptide cleavage to bind nerve growth factor. FEBS Lett 579 (2005) 1172-1176
93. Wu Y.-H., and Swaab D.F. The human pineal gland and melatonin in aging and Alzheimer's disease. J Pineal Res 38 (2005) 145-152
94. Yardley G., Relf B., Lakshmanan J., Reinshage M., and Moore G.P.M. Expression of nerve growth factor mRNA and its translation products in the anagen hair follicle. Exp Dermatol 9 (2000) 283-289
95. Yiangou Y., Facer P., Sinicropi D.V., Boucher T.J., Bennett D.L.H., McMahon S.B., et al. Molecular forms of NGF in human and rat neuropathic tissues: decreased NGF precursor-like immunoreactivity in human diabetic skin. J Peri Nerv Syst 7 (2002) 190-197
96. Zhou X.F., and Rush R.A. Sympathetic neurons in neonatal rats require endogenous neurotrophin-3 for survival. J Neurosci 15 10 (1995) 6521-6530