Progesterone influence on neurite outgrowth involves microglia

Endocrinology

Volumn 150, Issue 1, 2009, Pages 324-332

  Wong, Angela M ^a,c   Rozovsky, Irina ^a   Arimoto, Jason M ^a   Du, Yizhou ^a,d   Wei, Min ^a   Morgan, Todd E ^a   Finch, Caleb E ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b University of California ^*

^c UNIVERSITY OF CALIFORNIA   (United States)

^d GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA [4 (DIMETHYLAMINO)PHENYL] 4',5' DIHYDRO 6BETA METHYLSPIRO[ESTRA 4,9 DIENE 17BETA,2'(3'H) FURAN] 3 ONE; ESTRADIOL; GESTAGEN; MIFEPRISTONE; PROGESTERONE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENTORHINAL CORTEX; ESTRUS CYCLE; HIPPOCAMPUS; MICROGLIA; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; CELL CULTURE TECHNIQUES; ESTRADIOL; ESTROGEN ANTAGONISTS; FEMALE; MICROGLIA; NEURITES; NEURONS; OVARIECTOMY; PROGESTERONE; RATS; SYNAPSES;

EID: 58149460373     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0988     Document Type: Article

References (69)

1. Woolley CS, McEwen BS 1993 Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293-306
2. Choi JM, Romeo RD, Brake WG, Bethea CL, Rosenwaks Z, McEwen BS 2003 Estradiol increases pre- and post-synaptic proteins in the CA1 regions of the hippocampus in female rhesus macaques (Macaca mulatta). Endocrinology 144:4734-4738
3. McEwen BS 2002 Estrogens effects on the brain: multiple sites and molecular mechanisms. J Appl Physiol 91:2785-2801
4. Chen E, Nilsen J, Brinton RD 2006 Dose and temporal pattern of estrogen exposure determines neuroprotective outcome in hippocampal neurons: therapeutic implications. Endocrinology 147:5303-5313
5. Carroll JC, Rosario ER, Chang L, Stanczyk FZ, Oddo S, LaFerla FM, Pike CJ 2007 Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3xTg-AD mice. J Neurosci 27:13357-13365
6. Rosario E, Ramsden M, Pike CJ 2006 Progestins inhibit the neuroprotective effects of estrogen in the rat hippocampus. Brain Res 1099:206-210
7. Nilsen J, Brinton RD 2002 Impact of progestins on estradiol protentiation of the glutamate calcium response. Neuroreport 13:825-830
8. Frye CA, Walf AA 2008 Progesterone enhances performance of aged mice in cortical or hippocampal tasks. Neurosci Lett 437:116-120
9. van Wingen G, van Broekhoven F, Verkes RJ, Petersson KM, Bäckström T, Buitelaar J, Fernández G 2007 How progesterone impairs memory for biologically salient stimuli in healthy young women. J Neurosci 27:11416-11423
10. Freeman EW, Weinstock L, Rickels K, Sondheimer SJ, Coutifaris C 1992 A placebo-controlled study of effects of oral progesterone on performance and mood. Br J Clin Pharmacol 33:293-298
11. Grossman KJ, Goss CW, Stein DG 2004 Effects of progesterone on the inflammatory response to brain injury in the rat. Brain Res 1008:29-39
12. Pettus EH, Wright DW, Stein DG, Hoffman SW 2005 Progesterone treatment inhibits the inflammatory agents that accompany traumatic brain injury. Brain Res 1049:112-119
13. Wright DW, Kellermann AL, Hertzberg VS, Clark PL, Frankel M, Goldstein FC, Salomone JP, Dent LL, Harris OA, Ander DS, Lowery DW, Patel MM, Denson DD, Gordon AB, Wald MM, Gupta S, Hoffman SW, Stein DG 2007 ProTECT: a randomized clinical trial of progesterone for acute traumatic brain injury. Ann Emerg Med 49:391-402
14. Lai AY, Todd KG 2008 Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia 56:259-270
15. Shie FS, Woltjer RL 2007 Manipulation of microglial activation as a therapeutic strategy in Alzheimer's disease. Curr Med Chem 14:2865-2871
16. Geddes JW, Monaghan DT, Cotman CW, Lott IT, Kim RC, Chui HC 1985 Plasticity of hippocampal circuitry in Alzheimer's disease. Science 23:1179-1181
17. Morse JK, DeKosky ST, Scheff SW 1992 Neurotrophic effects of steroids on lesion-induced growth in the hippocampus. II. Hormone replacement. Exp Neurol 118:47-52
18. Stone DJ, Song Y, Anderson CP, Krohn KK, Finch CE, Rozovsky I 1998 Bidirectional transcription regulation of glial fibrillary acidic protein by estradiol in vivo and in vitro. Endocrinology 139:3202-3209
19. Kadish I, van Groen T 2002 Low levels of estrogen significantly diminish axonal sprouting after entorhinal cortex lesions in the mouse. J Neurosci 22: 4095-4102
20. Stroub TR, DeToledo-Morrell L, Stebbins GT, Leurgans S, Bennett DA, Shah RC 2006 Hippocampal disconnection contributes to memory dysfunction in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci USA 103:10041-10045
21. Ramirez JJ, McQuilkin M, Carrigan T, MacDonald K, Kelley MS 1996 Progressive entorhinal cortex lesions accelerate hippocampal sprouting and spare spatial memory in rats. Proc Natl Acad Sci USA 93:15512-15517
22. Ramirez JJ, Bulsara K, Moore SC, Ruch K, Abrams W 1999 Progressive unilateral damage of the entorhinal cortex enhances synaptic efficacy of the crossed entorhinal afferent to dentate granule cells. J Neurosci 19:RC42
23. Teter B, Harris-White ME, Frautschy SA, Cole GM 1999 Role of apolipoprotein E and estrogen in mossy fiber sprouting in hippocampal slice cultures. Neurosci 91:1009-1016
24. Quadros PS, Pfau JL, Wagner CK 2007 Distribution of progesterone receptor immunoreactivity in the fetal and neonatal rat forebrain. J Comp Neurol 504:42-56
25. Holmes W, Young JZ 1942 Nerve regeneration after immediate and delayed suture. J Anat 77:63-96
26. Rozovsky I, Finch CE, Morgan TE 1998 Age-related activation of microglia and astrocytes: in vitro studies show persistent phenotypes of aging, increased proliferation, and resistance to down-regulation. Neurobiol Aging 19:97-103
27. McCarthy KD, deVellis J 1980 Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902
28. Rozovsky I, Wei M, Stone DJ, Zanjani H, Anderson CP, Morgan TE, Finch CE 2002 Estradiol (E2) enhances neurite outgrowth by repressing glial fibrillary acidic protein expression and reorganizing laminin. Endocrinology 143:636-646
29. Cotman CW, Nieto-Sampedro M 1984 Cell biology of synaptic plasticity. Science 225:1287-1294
30. Stone DJ, Rozovsky I, Morgan TE, Anderson CP, Lopez LM, Schick J, Finch CE 2000 Effects of age on gene expression during estrogen-induced synaptic sprouting in the female rat. Exp Neurol 165:46-57
31. McEwen BS, Woolley CS 1994 Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Exp Gerontol 29:431-436
32. McMillian MK, Thai Hong JS, O'Callahan JP, Pennypacker KR 1994 Brain injury in a dish: a model for reactive gliosis. Trends Neurosci 17:138-142
33. Lefrancois T, Fages C, Peschanski M, Tardy M 1997 Neuritic outgrowth associated with astroglial phenotypic changes induced by antisense glial fibrillary acidic protein (GFAP) mRNA in injured neuron-astrocyte cocultures. J Neurosci 17:4121-4128
34. Stone DJ, Rozovsky I, Morgan TE, Anderson CP, Hajian H, Finch CE 1997 Astrocytes and microglia respond to estrogen with increased apoE mRNA in vivo and in vitro. Exp Neurol 143:313-318
35. Rang SW, Shin YJ, Shim YJ, Jeong SY, Park IS, Min BH 2005 Clusterin interacts with SCLIP (SCG10-like protein) and promotes neurite outgrowth of PC12 cells. Exp Cell Res 309:305-315
36. Schmechel DE, Brighman MW, Marangos PJ 1980 Neurons switch from nonneuronal enolase to neuron-specific enolase during differentiation. Brain Res 190:195-214
37. Sarnat HB, Nochlin D, Born DE 1998 Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev 20:88-94
38. Unal-Cevik I, Kilinc M, Gursoy-Ozdemir Y, Gurer G, Dalkara T 2004 Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res 1015:169-174
39. Collombet JM, Masqueliez C, Four E, Burckhart MF, Bernabe D, Baubichon D, Lallement G 2006 Early reduction of NeuN antigenicity induced by soman poisoning in mice can be used to predict delayed neuronal degeneration in the hippocampus. Neurosci Lett 398:337-342
40. Hailer NP, Bechmann I, Heizmann S, Nitsch R 1997 Adhesion molecule expression on phagocytic microglial cells following anterograde degeneration of perforant path axons. Hippocampus 7:341-349
41. Hailer NP, Grampp A, Nitsch R 1999 Proliferation of microglia and astrocytes in the dentate gyrus following entorhinal cortex lesion: a quantitative bromodeoxyuridine-labelling study. Eur J Neurosci 11:3359-3364
42. Dietrich A, Fulop ZL, Chambers MD, Darrell RS, Stein DG 2000 The effect of Ginkgo biloba extract (EGb 761) on gliotic reactions in the hippocampal formation after unilateral entorhinal cortex lesions. Restorative Neurol Neurosci 16:87-96
43. Gall C, Rose G, Lynch G 1979 Proliferative and migratory activity of glial cells in the partially deafferented hippocampus. J Comp Neurol 183:539-549
44. Singh M, Sumien N, Kyser C, Simpkins JW 2008 Estrogens and P4 as neuroprotectants: what animal models teach us. Front Biosci 13:1083-1089
45. Chien HF, Yeh KY, Jiang-Shieh YF, Wei IH, Chang CY, Chang ML, Wu CH 2005 Signal transduction pathways of nitric oxide release in primary microglial culture challenged with gram-positive bacterial constituent, lipoteichoic acid. Neurosci 133:423-436
46. Xie Z, Wei M, Morgan TE, Fabrizio P, Han D, Finch CE, Longo YD 2002 Peroxynitrite mediates neurotoxicity of amyloid β-peptidel-42-and lipopolysaccharide-activated microglia. J Neurosci 22:3384-3492
47. Kloosterboer HJ, Deckers GH, Schoonen WG 1994 Pharmacology of two new very selective antiprogestagens: Org 31710 and Org 31806. Hum Reprod 9(Suppl 1):47-52
48. Sanchez-Criado JE, Tebar M, Bellido C, De Jong FH 2000 Comparison of the effects of antiprogestins RU38486, ZK98299 and ORG31710 on periovulatory hypophysial, ovarian and adrenal hormone secretion in the rat. J Endocrinol Invest 23:151-157
49. Thomas CP, Liu KZ, Vats HS 2006 Medroxyprogesterone acetate binds the glucocorticoid receptor to stimulate α-ENaC and sgk1 expression in renal collecting duct epithelia. Am J Physiol Renal Physiol 290:F306-F312
50. Hodgen GD, van Uem JF, Chillik CF, Danforth DR, Wolf JP, Neulen J, Williams RF, Chwalisz K 1994 Non-competitive anti-oestrogenic activity of progesterone antagonists in primate models. Hum Reprod 9(Suppl 1):77-81
51. McDonnell DP, Goldman ME 1994 RU486 exerts antiestrogenic activities through a novel progesterone receptor A form-mediated mechanism. J Biol Chem 269:11945-11949
52. Drojdahl N, Fenger C, Nielsen HH, Owens T, Finsen B 2004 Dynamics of oligodendrocyte responses to anterograde axonal (Wallerian) and terminal degeneration in normal and TNF-transgenic mice. J Neurosci Res 75:203-217
53. Schumacher M, Guennoun R, Ghoumari A, Massaad C, Robert F, El-Etr M, Akwa Y, Rajkowski K, Baulieu EE 2007 Novel perspectives for progesterone in hormone replacement therapy, with special reference to the nervous system. Endocr Rev 28:387-439
54. Garcia-Ovejero D, Azcoitia I, Doncarlos LL, Melcangi RC, Garcia-Segura LM 2005 Glia cross-talk in the neuroprotective mechanisms of sex steroid hormones. Brain Res Brain Res Rev 48:273-286
55. Magnaghi V, Veiga S, Ballabio M, Gonzalez LC, Garcia-Segura LM, Melcangi RC 2006 Sex-dimorphic effects of progesterone and its reduced metabolites on gene expression of myelin proteins by rat Schwann cells. J Peripher Nerv Syst 11:111-118
56. Sierra A, Gottfried-Blackmore A, Milner TA, McEwen BS, Bulloch K 2008 Steroid hormone receptor expression and function in microglia. Glia 56: 659-674
57. Brinton RD, Thompson RF, Foy MR, Baudry M, Wang J, Finch CE, Morgan TE, Pike CJ, Mack WJ, Stanczyk FZ, Nilsen J 2008 Progesterone receptors: form and function in brain. Front Neuroendocrinol 29:313-339
58. Griffin R, Nally R, Nolan Y, McCartney Y, Linden J, Lynch MA 2006 The age-related attenuation in long-term potentiation is associated with microglial activation. J Neurochem 99:1263-1272
59. Eyupoglu IY, Bechmann I, Nitsch R 2003 Modification of microglia function protects from lesion-induced neuronal alterations and promotes sprouting in the hippocampus. FASEB J 17:1110-1111
60. Sherwin BB, Henry JF 2008 Brain aging modulates the neuroprotective effects of estrogen on selective aspects of cognition in women: a critical review. Front Neuroendocrinol 29:88-113
61. Rozovsky I, Wei M, Morgan TE, Finch CE 2005 Reversible age impairments in neurite outgrowth by manipulations of astrocytic GFAP. Neurobiol Aging 26:705-715
62. Johnson AB, Sohrabji F 2005 Estrogen's effects on central and circulating immune cells vary with reproductive age. Neurobiol Aging 26:1365-1374
63. Espeland MA, Rapp SR, Shumaker SA, Brunner R, Manson JE, Sheerwin BB, Hsia J, Margolis KL, Hogan PE, Wallace R, Dailey M, Freeman R, Hays J 2004 Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291:2959-2968
64. Rapp SR, Espeland MA, Shumaker SA, Henderson VW, Brunner RL, Manson JE, Gass ML, Stefanick ML, LD, Hays J, Johnson KC, Coker LH, Dailey M, Bowen D 2003 Effect of estrogen plus progestin on global cognitive function in postmenopausal women: The Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289:2663-2672
65. Shumaker SA, Legault C, Rapp SR, Thal L, Wallace RB, Ockene JK, Hendrix SL, Jones 3rd BN, Assaf AR, Jackson RD, Kotchen JM, Wassertheil-Smoller S, Wactawski-Wende J; WHIMS Investigators 2003 Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289:2651-2662
66. Shumaker SA, Legault C, Kuller L, Rapp SR, Thal L, Lane DS, Fillit H, Stefanick ML, Hendrix SL, Lewis CE, Masaki K, Coker LH 2004 Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291:2947-2958
67. Resnick SM, Maki PM, Rapp SR, Espeland MA, Brunner R, Coker LH, Granek IA, Hogan P, Ockene JK, Shumaker SA; Women's Health Initiative Study of Cognitive Aging Investigators 2006 Effects of combination estrogen plus progestin hormone treatment on cognition and affect. J Clin Endocrinol Metab 91:1802-1810
68. Henderson VW, Sherwin BB 2007 Surgical versus natural menopause: cognitive issues. Menopause 14:572-579
69. Grossman KJ, Goss CW, Stein DG 2004 Effects of progesterone on the inflammatory response to brain injury in the rat. Brain Res 1008:29-39