New Aspects of Progesterone Interactions with the Actin Cytoskeleton and Neurosteroidogenesis in the Cerebellum and the Neuronal Growth Cone

Journal of Histochemistry and Cytochemistry

Volumn 62, Issue 12, 2014, Pages 835-845

  Wessel, Lisa ^a   Olbrich, Laura ^a   Brand Saberi, Beate ^a   Theiss, Carsten ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

confocal laser scanning microscopy; dorsal root ganglia; life cell imaging; microinjection; PGRMC1; progesterone receptor; purkinje cell

Indexed keywords

PROGESTERONE; PROGESTERONE BINDING PROTEIN; PROGESTERONE BINDING PROTEIN PGRMC1; PROGESTERONE RECEPTOR; UNCLASSIFIED DRUG;

ACTIN FILAMENT; CELL INTERACTION; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CEREBELLUM; DRUG BINDING; GROWTH CONE; HORMONAL REGULATION; HORMONE RECEPTOR INTERACTION; HUMAN; NERVE CELL GROWTH; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NERVOUS TISSUE; NEUROBLAST; NEUROFILAMENT; NEUROPHARMACOLOGY; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PROGESTERONE SYNTHESIS; PURKINJE CELL; REVIEW; SPINAL GANGLION; SPINOGENESIS; STEROID BINDING; ANIMAL; METABOLISM;

ACTIN CYTOSKELETON; ANIMALS; CEREBELLUM; GANGLIA, SPINAL; GROWTH CONES; HUMANS; PROGESTERONE; PURKINJE CELLS; RECEPTORS, PROGESTERONE;

EID: 84912013680     PISSN: 00221554     EISSN: 15515044     Source Type: Journal    
DOI: 10.1369/0022155414550691     Document Type: Review

References (87)

1. Ahima RS,Garcia MM,Harlan RE.Intracellular localization of corticosteroid receptors in brain: potential interactions with signal transduction pathways.Proc Soc Exp Biol Med. 1992;201:244-253
2. Argiro V,Bunge MB,Johnson MI.Correlation between growth form and movement and their dependence on neuronal age.J Neurosci. 1984;4:3051-3062
3. Baulieu EE,Robel P.Neurosteroids: a new brain function?.The Journal of Steroid Biochemistry and Molecular Biology. 1990;37:395-403
4. Behl C,Trapp T,Skutella T,Holsboer F.Protection against oxidative stress-induced neuronal cell death–a novel role for RU486.Eur J Neurosci. 1997;9:912-920
5. Bentley D,Toroian-Raymond A.Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment.Nature. 1986;323:712-715
6. Bertagna X,Bertagna C,Luton JP,Husson JM,Girard F.The new steroid analog RU 486 inhibits glucocorticoid action in man.J Clin Endocrinol Metab. 1984;59:25-28
7. Bramham CR,Wells DG.Dendritic mRNA: transport, translation and function.Nat Rev Neurosci. 2007;8:776-789
8. Brinton RD,Thompson RF,Foy MR,Baudry M,Wang J,Finch CE,Morgan TE,Pike CJ,Mack WJ,Stanczyk FZ,Nilsen J.Progesterone receptors: form and function in brain.Front Neuroendocrinol. 2008;29:313-339
9. Cadepond F,Ulmann A,Baulieu EE.RU486 (mifepristone): mechanisms of action and clinical uses.Annu Rev Med. 1997;48:129-156
10. Chan JR,Rodriguez-Waitkus PM,Ng BK,Liang P,Glaser M.Progesterone synthesized by Schwann cells during myelin formation regulates neuronal gene expression.Mol Biol Cell. 2000;11:2283-2295
11. Chien CB,Rosenthal DE,Harris WA,Holt CE.Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain.Neuron. 1993;11:237-251
12. Compagnone NA,Bulfone A,Rubenstein JL,Mellon SH.Steroidogenic enzyme P450c17 is expressed in the embryonic central nervous system.Endocrinology. 1995;136:5212-5223
13. Coronel MF,Labombarda F,Roig P,Villar MJ,De Nicola AF,González SL.Progesterone prevents nerve injury- induced allodynia and spinal NMDA receptor upregulation in rats.Pain Med. 2011;12:1249-1261
14. Craven RJ,Mallory JC,Hand RA.Regulation of iron homeostasis mediated by the heme-binding protein Dap1 (damage resistance protein 1) via the P450 protein erg11/Cyp51.J Biol Chem. 2007;282:36543-36551
15. Dableh LJ,Henry JL.Progesterone prevents development of neuropathic pain in a rat model: Timing and duration of treatment are critical.J Pain Res. 2011;4:91-101
16. DeMarzo AM,Beck CA,Onate SA,Edwards DP.Dimerization of mammalian progesterone receptors occurs in the absence of DNA and is related to the release of the 90-kDa heat shock protein.Proc Natl Acad Sci U S A. 1991;88:72-76
17. Dent EW,Kalil K.Axon branching requires interactions between dynamic microtubules and actin filaments.J Neurosci. 2001;21:9757-9769
18. Dent EW,Gertler FB.Cytoskeletal dynamics and transport in growth cone motility and axon guidance.Neuron. 2003;40:209-227
19. Dent EW,Gupton SL,Gertler FB.The growth cone cytoskeleton in axon outgrowth and guidance.Cold Spring Harb Perspect Biol. 2011;3:a001800
20. Deutsch ER,Espinoza TR,Atif F,Woodall E,Kaylor J,Wright DW.Progesterone’s role in neuroprotection, a review of the evidence.Brain Res. 2013;1530:82-105
21. Dickson BJ.Molecular mechanisms of axon guidance.Science. 2002;298:1959-1964
22. Djebaili M,Hoffman SW,Stein DG.Allopregnanolone and progesterone decrease cell death and cognitive deficits after a contusion of the rat pre-frontal cortex.Neuroscience. 2004;123:349-359
23. Djebaili M,Guo Q,Pettus EH,Hoffman SW,Stein DG.The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury in rats.J Neurotrauma. 2005;22:106-118
24. Do Rego JL,Seong JY,Burel D,Leprince J,Luu-The V,Tsutsui K,Tonon MC,Pelletier G,Vaudry H.Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides.Front Neuroendocrinol. 2009;30:259-301
25. Edwards DP,DeMarzo AM,Onate SA,Beck CA,Estes PA,Nordeen SK.Mechanisms controlling steroid receptor binding to specific DNA sequences.Steroids. 1991;56:271-278
26. Fu XD,Simoncini T.Non-genomic sex steroid actions in the vascular system.Semin Reprod Med. 2007;25:178-186
27. Furukawa A,Miyatake A,Ohnishi T,Ichikawa Y.Steroidogenic acute regulatory protein (StAR) transcripts constitutively expressed in the adult rat central nervous system: colocalization of StAR, cytochrome P-450SCC (CYP XIA1), and 3beta-hydroxysteroid dehydrogenase in the rat brain.Journal of Neurochemistry. 1998;71:2231-2238
28. Gaillard RC,Riondel A,Muller AF,Herrmann W,Baulieu EE.RU 486: a steroid with antiglucocorticosteroid activity that only disinhibits the human pituitary-adrenal system at a specific time of day.Proc Natl Acad Sci U S A. 1984;81:3879-3882
29. Garay L,Deniselle MC,Lima A,Roig P,De Nicola AF.Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis.J Steroid Biochem Mol Biol. 2007;107:228-237
30. Garay L,Gonzalez Deniselle MC,Gierman L,Meyer M,Lima A,Roig P,De Nicaola AF.Steroid protection in the experimental autoimmune encephalomyelitis model of multiple sclerosis.Neuroimmunomodulation. 2008;15:76-83
31. Garay L,Deniselle MC,Meyer M,Costa JJ,Lima A,Roig P,De Nicola AF.Protective effects of progesterone administration on axonal pathology in mice with experimental autoimmune encephalomyelitis.Brain Res. 2009;1283:177-185
32. Ghoumari AM,Dusart I,El-Etr M,Tronche F,Sotelo C,Schumacher M,Baulieu EE.Mifepristone (RU486) protects Purkinje cells from cell death in organotypic slice cultures of postnatal rat and mouse cerebellum.Proc Natl Acad Sci U S A. 2003;100:7953-7958
33. Ghoumari AM,Piochon C,Tomkiewicz C,Eychenne B,Levenes C,Dusart I,Schumacher M,Baulieu EE.Neuroprotective effect of mifepristone involves neuron depolarization.FASEB J. 2006;20:1377-1386
34. Giatti S,Caruso D,Boraso M,Abbiati F,Ballarini E,Calabrese D,Pesaresi M,Rigolio R,Santos-Galindo M,Viviani B,Cavaletti G,Garcia-Segura LM,Melcangi RC.Neuroprotective effects of progesterone in chronic experimental autoimmune encephalomyelitis.J Neuroendocrinol. 2012;24:851-861
35. Giretti MS,Simoncini T.Rapid regulatory actions of sex steroids on cell movement through the actin cytoskeleton.Steroids. 2008;73:895-900
36. Goldberg DJ,Burmeister DW.Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy.J Cell Biol. 1986;103:1921-1931
37. Gu W,Pan F,Zhang H,Bassell GJ,Singer RH.A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons.J Cell Biol. 2002;156:41-51
38. Guennoun R,Schumacher M,Robert F,Delespierre B,Gouézou M,Eychenne B,Akwa Y,Robel P,Baulieu EE.Neurosteroids: expression of functional 3beta-hydroxysteroid dehydrogenase by rat sensory neurons and Schwann cells.Eur J Neurosci. 1997;9:2236-2247
39. Guennoun R,Meffre D,Labombarda F,Gonzalez SL,Deniselle MC,Stein DG,De Nicola AF,Schumacher M.The membraneassociated progesterone binding protein 25-Dx: expression, cellular localization and up-regulation after brain and spinal cord injuries.Brain Res Rev. 2008;57:493-505
40. Hughes AL,Powell DW,Bard M,Eckstein J,Barbuch R,Link AJ,Espenshade PJ.Dap1/PGRMC1 binds and regulates cytochrome P450 enzymes.Cell Metabolism. 2007;5:143-149
41. Ishrat T,Sayeed I,Atif F,Stein DG.Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats.BrainRes. 2009;1257:94-101
42. Katzenellenbogen BS,Katzenellenbogen JA.Biomedicine. Defining the “S” in SERMs.Science. 2002;295:2380-2381
43. Koenig HL,Schumacher M,Ferzaz B,Thi AN,Ressouches A,Guennoun R,Jung-Testas I,Robel P,Akwa Y,Baulieu EE.Progesterone synthesis and myelin formation by Schwann cells.Science. 1995;268:1500-1503
44. Krebs CJ,Jarvis ED,Chan J,Lydon JP,Ogawa S,Pfaff DW.A membrane-associated progesterone-binding protein, 25-Dx, is regulated by progesterone in brain regions involved in female reproductive behaviors.Proc Natl Acad Sci U S A. 2000;97:12816-12821
45. Labombarda F,Gonzalez SL,Deniselle MC,Vinson GP,Schumacher M,De Nicola AF,Guennoun R.Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-Dx expression in the rat spinal cord.J Neurochem. 2003;87:902-913
46. Lafont F,Rouget M,Rousselet A,Valenza C,Prochiantz A.Specific responses of axons and dendrites to cytoskeleton perturbations: an in vitro study.J Cell Sci. 1993;104 (Pt 2): 433-443
47. Lawson A,Ahima RS,Krozowski Z,Harlan RE.Postnatal development of corticosteroid receptor immunoreactivity in the rat cerebellum and brain stem.Neuroendocrinology. 1992;55:695-707
48. Leonhardt SA,Boonyaratanakornkit V,Edwards DP.Progesterone receptor transcription and non-transcription signaling mechanisms.Steroids. 2003;68:761-770
49. Liu Z,Auboeuf D,Wong J,Chen JD,Tsai SY,Tsai MJ,O’Malley BW.Coactivator/corepressor ratios modulate PR-mediated transcription by the selective receptor modulator RU486.Proc Natl Acad Sci U S A. 2002;99:7940-7944
50. Lowery LA,Van Vactor D.The trip of the tip: understanding the growth cone machinery.Nat Rev Mol Cell Biol. 2009;10:332-343
51. Marín O,Valiente M,Ge X,Tsai LH.Guiding neuronal cell migrations.Cold Spring Harb Perspect Biol. 2010;2:a001834
52. Marsh L,Letourneau PC.Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B.J Cell Biol. 1984;99:2041-2047
53. McCullers DL,Sullivan PG,Scheff SW,Herman JP.Mifepristone protects CA1 hippocampal neurons following traumatic brain injury in rat.Neuroscience. 2002;109:219-230
54. Mellon SH,Deschepper CF.Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain.Brain Research. 1993;629:283-292
55. Meyer ME,Pornon A,Ji J,Bocquel MT,Chambon P,Gronemeyer H.Agoinstic and antagonistic activities of RU486 on the function of the human progesterone receptor.EMBO J. 1990;9:3923-3932
56. Min L,Takemori H,Nonaka Y,Katoh Y,Doi J,Horike N,Osamu H,Raza FS,Vinson GP,Okamoto M.Characterization of the adrenal-specific antigen IZA (inner zone antigen) and its role in the steroidogenesis.Mol Cell Endocrinol. 2004;215:143-148
57. Okabe S,Hirokawa N.Actin dynamics in growth cones.J Neurosci. 1991;11:1918-1929
58. Olbrich L,Wessel L,Balakrishnan-Renuka A,Böing M,Brand-Saberi B,Theiss C.Rapid impact of progesterone on the neuronal growth cone.Endocrinology. 2013;154:3784-3795
59. O’Malley BW,Shermant MR,Toft DO.Progesterone “Receptors” in the Cytoplasm and Nucleus of Chick Oviduct Target Tissue.Proc Natl Acad Sci U S A. 1970;67:501-508
60. Rakotomamonjy J,Levenes C,Baulieu EE,Schumacher M,Ghoumari AM.Novel protective effect of mifepristone on detrimental GABAA receptor activity to immature Purkinje neurons.FASEB J. 2011;25:3999-4010
61. Rohe HJ,Ahmed IS,Twist KE,Craven RJ.PGRMC1 (progesterone receptor membrane component 1): a targetable protein with multiple functions in steroid signaling, P450 activation and drug binding.Pharmacol Ther. 2009;121:14-19
62. Roof RL,Hoffman SW,Stein DG.Progesterone protects against lipid peroxidation following traumatic brain injury in rats.Molecular and Chemical Neuropathology. 1997;31:1-11
63. Sakamoto H,Ukena K,Tsutsui K.Effects of progesterone synthesized de novo in the developing Purkinje cell on its dendritic growth and synaptogenesis.Journal of Neuroscience. 2001;21:6221-6232
64. Sakamoto H,Ukena K,Tsutsui K.Dendritic spine formation in response to progesterone synthesized de novo in the developing Purkinje cell in rats.Neuroscience Letters. 2002;322:111-115
65. Sakamoto H,Shikimi H,Ukena K,Tsutsui K.Neonatal expression of progesterone receptor isoforms in the cerebellar Purkinje cell in rats.Neuroscience Letters. 2003;343:163-166
66. Sakamoto H,Ukena K,Takemori H,Okamoto M,Kawata M,Tsutsui K.Expression and localization of 25-Dx, a membrane-associated putative progesterone-binding protein in the developing Purkinje cell.Neuroscience. 2004;126:325-334
67. Sakamoto H,Ukena K,Kawata M,Tsutsui K.Expression, localization and possible actions of 25-Dx, a membraneassociated putative progesterone-binding protein, in the developing Purkinje cell of the cerebellum: a new insight into the biosynthesis, metabolism and multiple actions of progesterone as a neurosteroid.Cerebellum. 2008;7:18-25
68. Sayeed I,Wali B,Stein DG.Progesterone inhibits ischemic brain injury in a rat model of permanent middle cerebral artery occlusion.Restor Neurol Neurosci. 2007;25:151-159
69. Schaefer AW,Kabir N,Forscher P.Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones.J Cell Biol. 2002;158:139-152
70. Schaeffer V,Meyer L,Patte-Mensah C,Mensah-Nyagan AG.Progress in dorsal root ganglion neurosteroidogenic activity: basic evidence and pathophysiological correlation.Prog Neurobiol. 2010;92:33-41
71. Selmin O,Lucier GW,Clark GC,Tritscher AM,Vanden Heuvel JP,Gastel JA,Walker NJ,Sutter TR,Bell DA.Isolation and characterization of a novel gene induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in rat liver.Carcinogenesis. 1996;17:2609-2615
72. Simoncini T,Genazzani AR.Non-genomic actions of sex steroid hormones.Eur J Endocrinol. 2003;148:281-292
73. Smith DF,Toft DO.Steroid receptors and their associated proteins.Mol Endocrinol. 1993;7:4-11
74. Tsai MJ,O’Malley BW.Molecular mechanism of action of steroid/thyroid receptor superfamily members.Annu Rev Biochem. 1994;63:451-486
75. Tsutsui K,Ukena K,Usui M,Sakamoto H,Takase M.Novel brain function: biosynthesis and actions of neurosteroids in neurons.Neuroscience Research. 2000;36:261-273
76. Ukena K,Usui M,Kohchi C,Tsutsui K.Cytochrome P450 side-chain cleavage enzyme in the cerebellar Purkinje neuron and its neonatal change in rats.Endocrinology. 1998;139:137-147
77. Ukena K,Kohchi C,Tsutsui K.Expression and activity of 3beta hydroxysteroid dehydrogenase/delta5-delta4-isomerase in the rat Purkinje neuron during neonatal life.Endocrinology. 1999;140:805-813
78. Wang J,Jiang C,Liu C,Li X,Chen N,Hao Y.Neuroprotective effects of progesterone following stroke in aged rats.Behav Brain Res. 2010;209:119-122
79. Waters EM,Torres-Reveron A,McEwen BS,Milner TA.Ultrastructural localization of extranuclear progestin receptors in the rat hippocampal formation.J Comp Neurol. 2008;511:34-46
80. Wessel L,Balakrishnan-Renuka A,Henkel C,Meyer HE,Meller K,Brand-Saberi B,Theiss C.Long-term incubation with mifepristone (MLTI) increases the spine density in developing Purkinje cells: new insights into progesterone receptor mechanisms.Cell Mol Life Sci. 2014;71:1723-1740
81. 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.ProTECT: a randomized clinical trial of progesterone for acute traumatic brain injury.Annals of Emergency. 2007;49:391-402
82. Xiao G,Wei J,Yan W,Wang W,Lu Z.Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: a randomized controlled trial.Critical Care. 2008;12:R61
83. Xu J,Zeng C,Chu W,Pan F,Rothfuss JM,Zhang F,Tu Z,Zhou D,Zeng D,Vangveravong S,Johnston F,Spitzer D,Chang KC,Hotchkiss RS,Hawkins WG,Wheeler KT,Mach RH.Identification of the PGRMC1 protein complex as the putative sigma-2 receptor binding site.Nature Comm. 2011;2:380
84. Yates MA,Li Y,Chlebeck P,Proctor T,Vandenbark AA,Offner H.Progesterone treatment reduces disease severity and increases IL-10 in experimental autoimmune encephalomyelitis.J Neuroimmunol. 2010;220:136-139
85. Yu HJ,Fei J,Chen XS,Cai QY,Liu HL,Liu GD,Yao ZX.Progesterone attenuates neurological behavioral deficits of experimental autoimmune encephalomyelitis through remyelination with nucleus-sublocalized Olig1 protein.Neurosci Lett. 2010;476:42-45
86. Yu WH.Survival of motoneurons following axotomyis enhanced by lactation or by progesterone treatment.Brain Res. 1989;491:379-382
87. Zhao L,Morgan TE,Mao Z,Lin S,Cadenas E,Finch CE,Pike CJ,Mack WJ,Brinton RD.Continuous versus cyclic progesterone exposure differentially regulates hippocampal gene expression and functional profiles.PLoS One. 2012;7:e31267