Chronic estrogen deficiency leads to molecular aberrations related to neurodegenerative changes in follitropin receptor knockout female mice

Neuroscience

Volumn 114, Issue 2, 2002, Pages 493-506

  Tam, J ^a   Danilovich, N ^b   Nilsson, K ^a   Sairam, M R ^b   Maysinger, D ^a  

^a MCGILL UNIVERSITY   (Canada)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

Choline acetyltransferase; CNS; Dorsal root ganglia; Estrogen; Follicle stimulating hormone; Mitogen activated protein kinase; Neurofilament

Indexed keywords

CHOLINE ACETYLTRANSFERASE; ESTROGEN; FOLLITROPIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NEUROFILAMENT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TESTOSTERONE;

ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CENTRAL NERVOUS SYSTEM; CHOLINERGIC SYSTEM; CHROMOSOME ABERRATION; CONTROLLED STUDY; CORPUS STRIATUM; ENDOCRINE DISEASE; ENZYME ACTIVITY; ESTRADIOL BLOOD LEVEL; ESTROGEN DEFICIENCY; FEMALE; HIPPOCAMPUS; KNOCKOUT MOUSE; MOUSE; NERVE DEGENERATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM FUNCTION; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SCIATIC NERVE; SENSORY GANGLION; SPINAL GANGLION; TESTOSTERONE BLOOD LEVEL;

ACETYLCHOLINE; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CHOLINE O-ACETYLTRANSFERASE; ENZYME INHIBITORS; ESTROGENS; FEMALE; GANGLIA, SPINAL; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASES; NEURITES; NEURODEGENERATIVE DISEASES; NEUROFILAMENT PROTEINS; PERIPHERAL NERVOUS SYSTEM; RECEPTORS, FSH; TESTOSTERONE; UP-REGULATION;

EID: 0036774154     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00278-6     Document Type: Article

References (97)

1. Alessi D.R., Cuenda A., Cohen P., Dudley D.T., Saltiel A.R. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270:1995;27489-27494.
2. Athlan E.S., Sacher M.G., Mushynski W.E. Associations between intermediate filament proteins expressed in cultured dorsal root ganglion neurons. J. Neurosci. Res. 47:1997;300-310.
3. Azcoitia I., Sierra A., Veiga S., Honda S., Harada N., Garcia-Segura L.M. Brain aromatase is neuroprotective. J. Neurobiol. 47:2001;318-329.
4. Beaulieu J.M., Jacomy H., Julien J.P. Formation of intermediate filament protein aggregates with disparate effects in two transgenic mouse models lacking the neurofilament light subunit. J. Neurosci. 20:2000;5321-5328.
5. Beaulieu J.M., Robertson J., Julien J.P. Interactions between peripherin and neurofilaments in cultured cells: disruption of peripherin assembly by the NF-M and NF-H subunits. Biochem. Cell Biol. 77:1999;41-45.
6. Benten W.P., Stephan C., Lieberherr M., Wunderlich F. Estradiol signaling via sequestrable surface receptors. Endocrinology. 142:2001;1669-1677.
7. Beyer C. Estrogen and the developing mammalian brain. Anat. Embryol. (Berl.). 199:1999;379-390.
8. Bi R., Foy M.R., Vouimba R.M., Thompson R.F., Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc. Natl. Acad. Sci. USA. 98:2001;13391-13395.
9. Bilsland J., Rigby M., Young L., Harper S. A rapid method for semi-quantitative analysis of neurite outgrowth from chick DRG explants using image analysis. J. Neurosci. Methods. 92:1999;75-85.
10. Blurton-Jones M.M., Roberts J.A., Tuszynski M.H. Estrogen receptor immunoreactivity in the adult primate brain: neuronal distribution and association with p75, trkA, and choline acetyltransferase. J. Comp. Neurol. 405:1999;529-542.
11. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
12. Choudhary S., Joshi K., Gill K.D. Possible role of enhanced microtubule phosphorylation in dichlorous induced delayed neurotoxicity in rat. Brain Res. 897:2001;60-70.
13. Cowley S.M., Parker M.G. A comparison of transcriptional activation by ER alpha and ER beta. J. Steroid Biochem. Mol. Biol. 69:1999;165-175.
14. Creedon D.J., Johnson E.M., Lawrence J.C. Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J. Biol. Chem. 271:1996;20713-20718.
15. Cuello, A.C., Carson, S., 1983. Microdissection of fresh rat brain tissue slices. In: Cuello, A.C. (Ed.), Brain Microdissection Techniques. Wiley, New York, pp. 37-125.
16. Danilovich N., Babu P.S., Xing W., Gerdes M., Krishnamurthy H., Sairam M.R. Estrogen deficiency, obesity, and skeletal abnormalities in follicle-stimulating hormone receptor knockout (FORKO) female mice. Endocrinology. 141:2000;4295-4308.
17. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell. 103:2000;239-252.
18. del Alonso C.A., Zaidi T., Novak M., Barra H.S., Grundke-Iqbal I., Iqbal K. Interaction of tau isoforms with Alzheimer's disease abnormally hyperphosphorylated tau and in vitro phosphorylation into the disease-like protein. J. Biol. Chem. 276:2001;37967-37973.
19. Diaz H., Lorenzo A., Carrer H.F., Caceres A. Time lapse study of neurite growth in hypothalamic dissociated neurons in culture: sex differences and estrogen effects. J. Neurosci. Res. 33:1992;266-281.
20. Dierich A., Sairam M.R., Monaco L., Fimia G.M., Gansmuller A., LeMeur M., Sassone-Corsi P. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl. Acad. Sci. USA. 95:1998;13612-13617.
21. Dina O.A., Aley K.O., Isenberg W., Messing R.O., Levine J.D. Sex hormones regulate the contribution of PKCepsilon and PKA signalling in inflammatory pain in the rat. Eur. J. Neurosci. 13:2001;2227-2233.
22. Dluzen D.E., McDermott J.L., Liu B. Estrogen as a neuroprotectant against MPTP-induced neurotoxicity in C57/B1 mice. Neurotoxicol. Teratol. 18:1996;603-606.
23. Dubal D.B., Wise P.M. Neuroprotective effects of estradiol in middle-aged female rats. Endocrinology. 142:2001;43-48.
24. Eilers A., Whitfield J., Shah B., Spadoni C., Desmond H., Ham J. Direct inhibition of c-Jun N-terminal kinase in sympathetic neurones prevents c-jun promoter activation and NGF withdrawal-induced death. J. Neurochem. 76:2001;1439-1454.
25. Fernyhough P., Gallagher A., Averill S.A., Priestley J.V., Hounsom L., Patel J., Tomlinson D.R. Aberrant neurofilament phosphorylation in sensory neurons of rats with diabetic neuropathy. Diabetes. 48:1999;881-889.
26. Ferreira A., Caceres A. Estrogen-enhanced neurite growth: evidence for a selective induction of Tau and stable microtubules. J. Neurosci. 11:1991;392-400.
27. Fonnum F. A rapid radiochemical method for the determination of choline acetyltransferase. J. Neurochem. 24:1975;407-409.
28. Fukunaga K., Miyamoto E. Role of MAP kinase in neurons. Mol. Neurobiol. 16:1998;79-95.
29. Garcia-Segura L.M., Azcoitia I., DonCarlos L.L. Neuroprotection by estradiol. Prog. Neurobiol. 63:2001;29-60.
30. Garcia M.L., Cleveland D.W. Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell. Biol. 13:2001;41-48.
31. Giasson B.I., Mushynski W.E. Aberrant stress-induced phosphorylation of perikaryal neurofilaments. J. Biol. Chem. 271:1996;30404-30409.
32. Giasson B.I., Mushynski W.E. Study of proline-directed protein kinases involved in phosphorylation of the heavy neurofilament subunit. J. Neurosci. 17:1997;9466-9472.
33. Gibbs R.B. Estrogen and nerve growth factor-related systems in brain. Effects on basal forebrain cholinergic neurons and implications for learning and memory processes and aging. Ann. N.Y. Acad. Sci. 743:1994;165-196.
34. Gibbs R.B. Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function. Exp. Neurol. 151:1998;289-302.
35. Gibbs R.B., Wu D., Hersh L.B., Pfaff D.W. Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp. Neurol. 129:1994;70-80.
36. 3H]dopa in various regions of the brain. J. Neurochem. 13:1966;655-669.
37. Gotow T., Tanaka J. Phosphorylation of neurofilament H subunit as related to arrangement of neurofilaments. J. Neurosci. Res. 37:1994;691-713.
38. Grant P., Sharma P., Pant H.C. Cyclin-dependent protein kinase 5 (Cdk5) and the regulation of neurofilament metabolism. Eur. J. Biochem. 268:2001;1534-1546.
39. Hall J.M., Couse J.F., Korach K.S. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276:2001;36869-36872.
40. Hansen T.O., Rehfeld J.F., Nielsen F.C. Cyclic AMP-induced neuronal differentiation via activation of p38 mitogen-activated protein kinase. J. Neurochem. 75:2000;1870-1877.
41. Hashimoto R., Nakamura Y., Komai S., Kashiwagi Y., Matsumoto N., Shiosaka S., Takeda M. Phosphorylation of neurofilament-L during LTD. NeuroReport. 11:2000;2739-2742.
42. Henderson V.W. The epidemiology of estrogen replacement therapy and Alzheimer's disease. Neurology. 48:1997;S27-S35.
43. Hensley K., Floyd R.A., Zheng N.Y., Nael R., Robinson K.A., Nguyen X., Pye Q.N., Stewart C.A., Geddes J., Markesbery W.R., Patel E., Johnson G.V., Bing G. p38 kinase is activated in the Alzheimer's disease brain. J. Neurochem. 72:1999;2053-2058.
44. Hoffman P.N., Cleveland D.W., Griffin J.W., Landes P.W., Cowan N.J., Price D.L. Neurofilament gene expression: a major determinant of axonal caliber. Proc. Natl. Acad. Sci. USA. 84:1987;3472-3476.
45. Kaufman H., Vadasz C., Lajtha A. Effects of estradiol and dexamethasone on choline acetyltransferase activity in various rat brain regions. Brain Res. 453:1988;389-392.
46. Kelly M.J., Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 12:2001;152-156.
47. Lanlua P., Decorti F., Gangula P.R., Chung K., Taglialatela G., Yallampalli C. Female steroid hormones modulate receptors for nerve growth factor in rat dorsal root ganglia. Biol. Reprod. 64:2001;331-338.
48. Levkovitz Y., O'Donovan K.J., Baraban J.M. Blockade of NGF-induced neurite outgrowth by a dominant-negative inhibitor of the egr family of transcription regulatory factors. J. Neurosci. 21:2001;45-52.
49. Li B.S., Veeranna Gu J., Grant P., Pant H.C. Activation of mitogen-activated protein kinases (Erk1 and Erk2) cascade results in phosphorylation of NF-M tail domains in transfected NIH 3T3 cells. Eur. J. Biochem. 262:1999;211-217.
50. Li R. Culture methods for selective growth of normal rat and human Schwann cells. Methods Cell Biol. 57:1998;167-186.
51. Mahalik T.J., Carrier A., Owens G.P., Clayton G. The expression of GAP43 mRNA during the late embryonic and early postnatal development of the CNS of the rat: an in situ hybridization study. Brain Res. Dev. Brain Res. 67:1992;75-83.
52. Manolagas S.C. Cellular and molecular mechanisms of osteoporosis. Aging (Milan). 10:1998;182-190.
53. Marszalek J.R., Williamson T.L., Lee M.K., Xu Z., Hoffman P.N., Becher M.W., Crawford T.O., Cleveland D.W. Neurofilament subunit NF-H modulates axonal diameter by selectively slowing neurofilament transport. J. Cell Biol. 135:1996;711-724.
54. Masaki R., Saito T., Yamada K., Ohtani-Kaneko R. Accumulation of phosphorylated neurofilaments and increase in apoptosis-specific protein and phosphorylated c-Jun induced by proteasome inhibitors. J. Neurosci. Res. 62:2000;75-83.
55. Matthews K.A., Meilahn E., Kuller L.H., Kelsey S.F., Caggiula A.W., Wing R.R. Menopause and risk factors for coronary heart disease. N. Engl. J. Med. 321:1989;641-646.
56. McMillan P.J., Singer C.A., Dorsa D.M. The effects of ovariectomy and estrogen replacement on trkA and choline acetyltransferase mRNA expression in the basal forebrain of the adult female Sprague-Dawley rat. J. Neurosci. 16:1996;1860-1865.
57. Migheli A., Piva R., Atzori C., Troost D., Schiffer D. c-Jun, JNK/SAPK kinases and transcription factor NF-kappa B are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 56:1997;1314-1322.
58. Miranda R.C., Sohrabji F., Toran-Allerand C.D. Neuronal colocalization of mRNAs for neurotrophins and their receptors in the developing central nervous system suggests a potential for autocrine interactions. Proc. Natl. Acad. Sci. USA. 90:1993;6439-6443.
59. Monks D.A., Getsios S., MacCalman C.D., Watson N.V. N-cadherin is regulated by gonadal steroids in the adult hippocampus. Proc. Natl. Acad. Sci. USA. 98:2001;1312-1316.
60. Monteiro M.J., Hoffman P.N., Gearhart J.D., Cleveland D.W. Expression of NF-L in both neuronal and nonneuronal cells of transgenic mice: increased neurofilament density in axons without affecting caliber. J. Cell Biol. 111:1990;1543-1557.
61. Moosmann B., Behl C. The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties. Proc. Natl. Acad. Sci. USA. 96:1999;8867-8872.
62. Mufson E.J., Cai W.J., Jaffar S., Chen E., Stebbins G., Sendera T., Kordower J.H. Estrogen receptor immunoreactivity within subregions of the rat forebrain: neuronal distribution and association with perikarya containing choline acetyltransferase. Brain Res. 849:1999;253-274.
63. Nakamura Y., Hashimoto R., Kashiwagi Y., Aimoto S., Fukusho E., Matsumoto N., Kudo T., Takeda M. Major phosphorylation site (Ser55) of neurofilament L by cyclic AMP-dependent protein kinase in rat primary neuronal culture. J. Neurochem. 74:2000;949-959.
64. Nakamura Y., Hashimoto R., Kashiwagi Y., Wada Y., Sakoda S., Miyamae Y., Kudo T., Takeda M. Casein kinase II is responsible for phosphorylation of NF-L at Ser-473. FEBS Lett. 455:1999;83-86.
65. Namgung U., Xia Z. Arsenite-induced apoptosis in cortical neurons is mediated by c-Jun N-terminal protein kinase 3 and p38 mitogen-activated protein kinase. J. Neurosci. 20:2000;6442-6451.
66. Oda Y. Choline acetyltransferase: the structure, distribution and pathologic changes in the central nervous system. Pathol. Int. 49:1999;921-937.
67. Papasozomenos S.C. The heat shock-induced hyperphosphorylation of tau is estrogen-independent and prevented by androgens: implications for Alzheimer disease. Proc. Natl. Acad. Sci. USA. 94:1997;6612-6617.
68. Patrone C., Andersson S., Korhonen L., Lindholm D. Estrogen receptor-dependent regulation of sensory neuron survival in developing dorsal root ganglion. Proc. Natl. Acad. Sci. USA. 96:1999;10905-10910.
69. Pearson G., Robinson F., Beers G.T., Xu B.E., Karandikar M., Berman K., Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22:2001;153-183.
70. Pelligrino D.A., Ye S., Tan F., Santizo R.A., Feinstein D.L., Wang Q. Nitric-oxide-dependent pial arteriolar dilation in the female rat: effects of chronic estrogen depletion and repletion. Biochem. Biophys. Res. Commun. 269:2000;165-171.
71. Perron J.C., Bixby J.L. Distinct neurite outgrowth signaling pathways converge on ERK activation. Mol. Cell. Neurosci. 13:1999;362-378.
72. Purves T., Middlemas A., Agthong S., Jude E.B., Boulton A.J., Fernyhough P., Tomlinson D.R. A role for mitogen-activated protein kinases in the etiology of diabetic neuropathy. FASEB J. 15:2001;2508-2514.
73. Salh B.S., Martens J., Hundal R.S., Yoganathan N., Charest D., Mui A., Gomez-Munoz A. PD98059 attenuates hydrogen peroxide-induced cell death through inhibition of Jun N-terminal kinase in HT29 cells. Mol. Cell Biol. Res. Commun. 4:2000;158-165.
74. Sihag R.K., Jaffe H., Nixon R.A., Rong X. Serine-23 is a major protein kinase A phosphorylation site on the amino-terminal head domain of the middle molecular mass subunit of neurofilament proteins. J. Neurochem. 72:1999;491-499.
75. Simpkins J.W., Rajakumar G., Zhang Y.Q., Simpkins C.E., Greenwald D., Yu C.J., Bodor N., Day A.L. Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J. Neurosurg. 87:1997;724-730.
76. Simpson E.R., Davis S.R. Minireview: aromatase and the regulation of estrogen biosynthesis-some new perspectives. Endocrinology. 142:2001;4589-4594.
77. Singh M. Ovarian hormones elicit phosphorylation of Akt and extracellular-signal regulated kinase in explants of the cerebral cortex. Endocrine. 14:2001;407-415.
78. Singh M., Setalo G. Jr., Guan X., Frail D.E., Toran-Allerand C.D. Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-alpha knock-out mice. J. Neurosci. 20:2000;1694-1700.
79. Sjogreen B., Wiklund P., Ekstrom P.A. Mitogen activated protein kinase inhibition by PD98059 blocks nerve growth factor stimulated axonal outgrowth from adult mouse dorsal root ganglia in vitro. Neuroscience. 100:2000;407-416.
80. Sohrabji F., Miranda R.C., Toran-Allerand C.D. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J. Neurosci. 14:1994;459-471.
81. Tanzer L., Jones K.J. Gonadal steroid regulation of hamster facial nerve regeneration: effects of dihydrotestosterone and estradiol. Exp. Neurol. 146:1997;258-264.
82. Toran-Allerand C.D. Mechanisms of estrogen action during neural development: mediation by interactions with the neurotrophins and their receptors? J. Steroid Biochem. Mol. Biol. 56:1996;169-178.
83. Toran-Allerand C.D., Singh M., Setalo G. Jr. Novel mechanisms of estrogen action in the brain: new players in an old story. Front. Neuroendocrinol. 20:1999;97-121.
84. Van der Zee C.E., Nielander H.B., Vos J.P., Lopes S., Verhaagen J., Oestreicher A.B., Schrama L.H., Schotman P., Gispen W.H. Expression of growth-associated protein B-50 (GAP43) in dorsal root ganglia and sciatic nerve during regenerative sprouting. J. Neurosci. 9:1989;3505-3512.
85. Vaucher E., Pierret P., Julien J., Kuchel G.A. Ovariectomy up-regulates neuronal neurofilament light chain mRNA expression with regional and temporal specificity. Neuroscience. 103:2001;629-637.
86. Veeranna Amin N.D., Ahn N.G., Jaffe H., Winters C.A., Grant P., Pant H.C. Mitogen-activated protein kinases (Erk1, 2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J. Neurosci. 18:1998;4008-4021.
87. Vegeto E., Bonincontro C., Pollio G., Sala A., Viappiani S., Nardi F., Brusadelli A., Viviani B., Ciana P., Maggi A. Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. J. Neurosci. 21:2001;1809-1818.
88. Wang L., Andersson S., Warner M., Gustafsson J.A. Morphological abnormalities in the brains of estrogen receptor beta knockout mice. Proc. Natl. Acad. Sci. USA. 98:2001;2792-2796.
89. Watters J.J., Campbell J.S., Cunningham M.J., Krebs E.G., Dorsa D.M. Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription. Endocrinology. 138:1997;4030-4033.
90. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Bottner M. Minireview: neuroprotective effects of estrogen-new insights into mechanisms of action. Endocrinology. 142:2001;969-973.
91. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Liu Y. Estrogens: trophic and protective factors in the adult brain. Front. Neuroendocrinol. 22:2001;33-66.
92. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 270:1995;1326-1331.
93. Xu Z., Marszalek J.R., Lee M.K., Wong P.C., Folmer J., Crawford T.O., Hsieh S.T., Griffin J.W., Cleveland D.W. Subunit composition of neurofilaments specifies axonal diameter. J. Cell. Biol. 133:1996;1061-1069.
94. Yabe J.T., Chylinski T., Wang F.S., Pimenta A., Kattar S.D., Linsley M.D., Chan W.K., Shea T.B. Neurofilaments consist of distinct populations that can be distinguished by C-terminal phosphorylation, bundling, and axonal transport rate in growing axonal neurites. J. Neurosci. 21:2001;2195-2205.
95. Yang D.D., Kuan C.Y., Whitmarsh A.J., Rincon M., Zheng T.S., Davis R.J., Rakic P., Flavell R.A. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature. 389:1997;865-870.
96. Zhang Y., Moheban D.B., Conway B.R., Bhattacharyya A., Segal R.A. Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation. J. Neurosci. 20:2000;5671-5678.
97. Zhou Y., Watters J.J., Dorsa D.M. Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain. Endocrinology. 137:1996;2163-2166.