Regulation of the phosphoinositide-3 kinase and mitogen-activated protein kinase signaling pathways by progesterone and its reduced metabolites in the rat brain

Journal of Neuroscience Research

Volumn 87, Issue 2, 2009, Pages 470-481

  Guerra Araiza, Christian ^a   Amorim, Miguel A R ^b   Pinto Almazán, Rodolfo ^a   González Arenas, Aliesha ^c   Campos, Maria G ^a   Garcia Segura, Luis M ^b  

^a HOSPITAL DE ESPECIALIDADES   (Mexico)

^b INSTITUTO CAJAL   (Spain)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Akt; Dihydroprogesterone; Extracellular signal regulated kinase; Tetrahydroprogesterone

Indexed keywords

20ALPHA DIHYDROPROGESTERONE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE; PROTEIN KINASE B; PROTEIN P110; PROTEIN P85; TETRAHYDROPROGESTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; HIPPOCAMPUS; HORMONE ACTION; HYPOTHALAMUS; METABOLITE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; METABOLISM; PHYSIOLOGY; WISTAR RAT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BLOTTING, WESTERN; BRAIN; FEMALE; MITOGEN-ACTIVATED PROTEIN KINASES; OVARIECTOMY; PROGESTERONE; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION;

EID: 62849085196     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21848     Document Type: Article

References (97)

1. Alonso G, Phan V, Guillemain I, Saunier M, Legrand A, Anoal M, Maurice T. 2000. Immunocytochemical localization of the sigma(1) receptor in the adult rat central nervous system. Neuroscience 97:155-170.
2. Arimura N, Kaibuchi K. 2005. Key regulators in neuronal polarity. Neuron 48:881-884.
3. Avila J, Lucas JJ, Perez M, Hernandez F. 2004. Role of tau protein in both physiological and pathological conditions. Physiol Rev 84:361-384.
4. Bagowski CP, Myers JW, Ferrell JE. 2001. The classical progesterone receptor associates with p42 MAPK and is involved in phosphatidylinositol 3-kinase signaling in Xenopus oocytes. J Biol Chem. 276:37708-37714.
5. Barbaccia ML, Serra M, Purdy RH, Biggio G. 2001. Stress and neuroactive steroids. Int Rev Neurobiol 46:243-272.
6. Baulieu E, Schumacher M. 2000. Progesterone as a neuroactive neurosteroid, with special reference to the effect of progesterone on myelination. Steroids 65:605-612.
7. A receptor. Nat Rev Neurosci 6:565-575.
8. Belelli D, Herd MB, Mitchell EA, Peden DR, Vardy AW, Gentet L, Lambert JJ. 2006. Neuroactive steroids and inhibitory neurotransmission: mechanisms of action and physiological relevance. Neuroscience 138:821-829.
9. Beyer C. 2007. Neuroendocrine regulation of estrous behavior in the rabbit: similarities and differences with the rat. Horm Behav 52:2-11.
10. Birzniece V, Backstrom T, Johansson IM, Lindblad C, Lundgren P, Lofgren M, Olsson T, Ragagnin G, Taube M, Turkmen S, Wahlstrom G, Wang MD, Wihlback AC, Zhu D. 2006. Neuroactive steroid effects on cognitive functions with a focus on the serotonin and GABA systems. Brain Res Brain Res Rev 51:212-239.
11. Boonyaratanakornkit V, Bi Y, Rudd M, Edwards DP. 2008. The role and mechanism of progesterone receptor activation of extra-nuclear signaling pathways in regulating gene transcription and cell cycle progression. Steroids (in press).
12. 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.
13. Cardona-Gómez GP, Chowen JA, Garcia-Segura LM. 2000. Estradiol and progesterone regulate the expression of insulin-like growth factor-I receptor and insulin-like growth factor binding protein-2 in the hypothalamus of adult female rats. J Neurobiol 43:269-281.
14. Ciriza I, Azcoitia I, Garcia-Segura LM. 2004. Reduced progesterone metabolites protect rat hippocampal neurones from kainic acid excito-toxicity in vivo. J Neuroendocrinol 16:58-63.
15. Ciriza I, Carrero P, Frye CA, Garcia-Segura LM. 2006. Reduced metabolites mediate neuroprotective effects of progesterone in the adult rat hippocampus. The synthetic progestin medroxyprogesterone acetate (Provera) is not neuroprotective. J Neurobiol 66:916-928.
16. Curtis J, Finkbeiner S. 1999. Sending signals from the synapse to the nucleus: possible roles for CaMK, Ras/ERK, and SAPK pathways in the regulation of synaptic plasticity and neuronal growth. J Neurosci Res 58: 88-95.
17. De Nicola AF, Gonzalez SL, Labombarda F, Deniselle MC, Garay L, Guennoun R, Schumacher M. 2006. Progesterone treatment of spinal cord injury: effects on receptors, neurotrophins, and myelination. J Mol Neurosci 28:3-15.
18. Djebaili M, Hoffman SW, Stein DG. 2004. Allopregnanolone and progesterone decrease cell death and cognitive deficits after a contusion of the rat pre-frontal cortex. Neuroscience 123:349-359.
19. Djebaili M, Guo Q, Pettus EH, Hoffman SW, Stein DG. 2005. The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury in rats. J Neurotrauma 22:106-118.
20. Drew PD, Chavis JA. 2000. Female sex steroids: effects upon microglial cell activation. J Neuroimmunol 111:77-85.
21. Dueñas M, Luquín S, Chowen JA, Torres-Alemán I, Naftolin F, Garcia-Segura LM. 1994. Gonadal hormone regulation of insulin-like growth factor-I-like immunoreactivity in hypothalamic astroglia of developing and adult rats. Neuroendocrinology 59:528-538.
22. El-Bakri NK, Islam A, Suliman I, Lindgren U, Winblad B, Adem A. 2004. Ovariectomy and gonadal hormone treatment: effects on insulin-like growth factor-1 receptors in the rat brain. Growth Horm IGF Res 14:388-393.
23. Engel SR, Grant KA. 2001. Neurosteroids and behavior. Int Rev Neurobiol 46:321-348.
24. Etgen AM. 2003. Ovarian steroid and growth factor regulation of female reproductive function involves modification of hypothalamic alpha 1-adrenoceptor signaling. Ann NY Acad Sci 1007:153-161.
25. Etgen AM, Acosta-Martinez M. 2003. Participation of growth factor signal transduction pathways in estradiol facilitation of female reproductive behavior. Endocrinology 144:3828-3835.
26. Etgen AM, Garcia-Segura LM. 2008. Estrogen regulation of neurotransmitter and growth factor signaling in the brain. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior,2nd ed. San Diego: Elsevier Science (in press).
27. Etgen AM, Gonzalez-Flores O, Todd BJ. 2006. The role of insulin-like growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors. Front Neuroendocrinol 27:363-375.
28. A receptor plasticity during long-term exposure to and withdrawal from progesterone. Brain Res Brain Res Rev 37:81-90.
29. Frank C, Sagratella S. 2000. Neuroprotective effects of allopregnenolone on hippocampal irreversible neurotoxicity in vitro. Prog Neuropsychopharmacol Biol Psychiatry 24:1117-1126.
30. Frye CA. 1995. The neurosteroid 3 alpha, 5 apha-THP has antiseizure and possible neuroprotective effects in an animal model of epilepsy. Brain Res 696:113-120.
31. Frye CA. 2007. Progestins influence motivation, reward, conditioning, stress, and/or response to drugs of abuse. Pharmacol Biochem Behav 86:209-219.
32. Frye CA, Scalise TJ. 2000. Anti-seizure effects of progesterone and 3alpha, 5alpha-THP in kainic acid and perforant pathway models of epilepsy. Psychoneuroendocrinology 25:407-420.
33. Fukunaga K, Miyamoto E. 1998. Role of MAP kinase in neurons. Mol Neurobiol 16:79-95.
34. Galea LA, Spritzer MD, Barker JM, Pawluski JL. 2006. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 16:225-232.
35. Ganter S, Northoff H, Mannel D, Gebicke-Harter PJ. 1992. Growth control of cultured microglia. J Neurosci Res 33:218-230.
36. Garcia-Estrada J, Del Rio JA, Luquin S, Soriano E, Garcia-Segura LM. 1993. Gonadal hormones down-regulate reactive gliosis and astrocyte proliferation after a penetrating brain injury. Brain Res 628:271-278.
37. Garcia-Segura LM, Melcangi RC. 2006. Steroids and glial cell function. Glia 54:485-498.
38. Garcia-Segura LM, Chowen JA, Parducz A, Naftolin F. 1994. Gonadal hormones as promoters of structural synaptic plasticity: cellular mechanisms. Prog Neurobiol 44:279-307.
39. Ghoumari AM, Baulieu EE, Schumacher M. 2005. Progesterone increases oligodendroglial cell proliferation in rat cerebellar slice cultures. Neuroscience 135:47-58.
40. Giovannim MG. 2006. The role of the extracellular signal-regulated kinase pathway in memory encoding. Rev Neurosci 17:619-634.
41. Gonzalez SL, Labombarda F, Gonzalez Deniselle MC, Guennoun R, Schumacher M, De Nicola AP. 2004. Progesterone up-regulates neuronal brain-derived neurotrophic factor expression in the injured spinal cord. Neuroscience 125:605-614.
42. Gonzalez SL, Labombarda F, Deniselle MC, Mougel A, Guennoun R, Schumacher M, De Nicola AF. 2005. Progesterone neuroprotection in spinal cord trauma involves up-regulation of brain-derived neurotrophic factor in motoneurons. J Steroid Biochem Mol Biol 94:143-149.
43. Gonzalez Deniselle MC, Garay L, Gonzalez SL, Saravia F, Labombarda F, Guennoun R, Schumacher M, De Nicola AF. 2007. Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating Wobbler motoneurons. Exp Neurol 203:406-414.
44. Grewal SS, York RD, Stork PJ. 1999. Extracellular-signal-regulated kinase signalling in neurons. Curr Opin Neurobiol 9:544-553.
45. Guennoun R, Meffre D, Labombarda F, Gonzalez SL, Deniselle MC, Stein DG, De Nicola AF, Schumacher M. 2008. The membrane-associated progesterone-binding protein 25-Dx: expression, cellular localization and up-regulation after brain and spinal cord injuries. Brain Res Brain Res Rev 57:493-505.
46. Guerra-Araiza C, Villamar-Cruz O, González-Arenas A, Chavira R, Camacho-Arroyo I. 2003. Changes in progesterone receptor isoforms content in the rat brain during the oestrous cycle and after oestradiol and progesterone treatments. J Neuroendocrinol 15:984-990.
47. Guerra-Araiza C, Amorim MA, Camacho-Arroyo I, Garcia-Segura LM. 2007. Effects of progesterone and its reduced metabolites, dihydroprogesterone and tetrahydroprogesterone, on the expression and phosphorylation of glycogen synthase kinase-3 and the microtubule-associated protein tau in the rat derebellum. Dev Neurobiol 67:510-520.
48. Hanna R, Pang Y, Thomas P, Zhu Y. 2006. Cell-surface expression, progestin binding, and rapid nongenomic signaling of zebrafish membrane progestin receptors alpha and beta in transfected cells. J Endocrinol 190:247-260.
49. He J, Hoffman SW, Stein DG. 2004. Allopregnanolone, a progesterone metabolite, enhances behavioral recovery and decreases neuronal loss after traumatic brain injury. Restor Neurol Neurosci 2:19-31.
50. A receptor subunits in the adult C57 mouse as assessed with in situ hybridization. Neuroscience 150:370-385.
51. Jung-Testas I, Schumacher M, Robel P, Baulieu EE. 1994. Actions of steroid hormones- and growth factors on glial cells of the central and peripheral nervous system. J Steroid Biochem Mol Biol 48:145-154.
52. Kaur P, Jodhka PK, Underwood WA, Bowles CA, de Fiebre NC, de Fiebre CM, Singh M. 2007. Progesterone increases brain-derived neuroptrophic factor expression and protects against glutamate toxicity in a mitogen-activated protein kinase- and phosphoinositide-3 kinase-dependent manner in cerebral cortical explants. J Neurosci Res 85:2441-2449.
53. Krebs CJ, Jarvis ED, Chan J, Lydon JP, Ogawa S, Pfaff DW. 2000. A membrane-associated progesterone-binding protein, 25-Dx, is regulated by progesterone in brain regions involved in female reproductive behaviors. Proc Natl Acad Sci USA 97:12816-12821.
54. A receptors. Prog Neurobiol 71:67-80.
55. Lindwall G, Cole RD. 1984. Phosphorylation affects the ability of tau protein to promote microtubule assembly. J Biol Chem 259:5301-5301.
56. Majewska MD. 1992. Neurosteroids: endogenous bimodal modulators of the GABAA receptor. Mechanism of action and physiological significance. Prog Neurobiol 38:379-395.
57. Mannella P, Brinton RD. 2006. Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: a unified mechanism of estrogen action. J Neurosci 26:9439-9447.
58. Marin R, Guerra B, Alonso R, Ramírez CM, Díaz M. 2005. Estrogen activates classical and alternative mechanisms to orchestrate neuroprotection. Curr Neurovasc Res 2:287-301.
59. 1) receptor: pharmacological evidences and therapeutic opportunities. Jpn J Pharmacol 81:125-155.
60. Meffre D, Delespierre B, Gouezou M, Leclerc P, Vinson GP, Schumacher M, Stein DG, Guennoun R. 2005. The membrane-associated progesterone-binding protein 25-Dx is expressed in brain regions involved in water homeostasis and is up-regulated after traumatic brain injury. J Neurochem 93:1314-1326.
61. Melcangi RC, Magnaghi V, Martini L. 1999. Steroid metabolism and effects in central and peripheral glial cells. J Neurobiol 40:471-493.
62. Melcangi RC, Garcia-Segura LM, Mensah-Nyagan AG. 2008. Neuroactive steroids: state of the art and new perspectives. Cell Mol Life Sci 65:777-797.
63. Micevych P, Sinchak K. 2008. Synthesis and function of hypothalamic neuroprogesterone in reproduction. Endocrinology 149:2739-2742.
64. Nilsen J, Brinton RD. 2003. Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling. Proc Natl Acad Sci USA 100:10506-10511.
65. Patte-Mensah C, Kibaly C, Mensah-Nyagan AG. 2005. Substance P inhibits progesterone conversion to neuroactive metabolites in spinal sensory circuit: a potential component of nociception. Proc Natl Acad Sci USA 102:9044-9049.
66. Perez J, Luquin S, Naftolin F, Garcia-Segura LM. 1993. The role of estradiol and progesterone in phased synaptic remodelling of the rat arcuate nucleus. Brain Res 608:38-44.
67. Pfaff DW. 1989. Features of a hormone-driven defined neural circuit for a mammalian behavior. Principles illustrated, neuroendocrine syllogisms, and multiplicative steroid effects. Ann N Y Acad Sci 563:131-147.
68. A receptors. Neuron 4:759-765.
69. Rhodes ME, Frye CA. 2004. Progestins in the hippocampus of female rats have antiseizure effects in a pentylenetetrazole seizure model. Epilepsia 45:1531-1538.
70. Rhodes ME, McCormick CM, Frye CA. 2004. 3Alpha,5alpha-THP mediates progestins' effects to protect against adrenalectomy-induced cell death in the dentate gyrus of female and male rats. Pharmacol-Biochem Behav 78:505-512.
71. Ronnekleiv OK, Kelly MJ. 2005. Diversity of ovarian steroid signaling in the hypothalamus. Front Neuroendocrinol 26:65-84.
72. Rupprecht R. 2003. Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psyphoneuroendocrinology 28: 139-168.
73. Rupprecht R, Reul JM, Trapp T, Van SB, Wetzel C, Damm K, Zieglgansberger W, Holsboer F. 1993. Progesterone receptor-mediated effects of neuroactive steroids. Neuron 11:523-530.
74. Sakamoto H, Ukena K, Tsutsui K. 2001. Effects of progesterone synthesized de novo in the developing Purkinje cell on its dendritic growth and synaptogenesis. J Neurosci 21:6221-6232.
75. Sakamoto H, Ukena K, Tsutsui K. 2002. Dendritic spine formation in response to progesterone synthesized de novo in the developing Purkinje cell in rats. Neurosci Lett 322:111-115.
76. Sakamoto H, Ukena K, Takemori H, Okamoto M, Kawata M, Tsutsui K. 2004. Expression and localization of 25-Dx, a membrane-associated putative progesterone-binding protein, in the developing Purkinje cell. Neuroscience 126:325-334.
77. Schumacher M, Guennoun R, Robert F, Carelli C, Gago N, Ghoumari A, Gonzalez Deniselle MC, Gonzalez SL, Ibanez C, Labombarda F, Coirini H, Baulieu EE, De Nicola AF. 2004. Local synthesis and dual actions progesterone in the nervous system: neuroprotection and myelination. Growth Horm IGF Res 14(Suppl A):Sl8-S33.
78. Selye H. 1941. Anesthetics of steroid hormones. Proc Soc Exp Biol Med 46:116-121.
79. Singh M. 2001. Ovarian hormones elicit phosphorylation of Akt and extracellular-signal regulated kinase in explants of the cerebral cortex. Endocrine 14:407-415.
80. Skeberdis VA, Lan J, Zheng X, Zukin RS, Bennett MV. 2001. Insulin promotes rapid delivery of N-methyl-D-aspartate receptors to the cell surface by exocytosis. Proc Natl Acad Sci USA 98:3561-3566.
81. A receptor subtype. Brain Res Bull 23:317-322.
82. Smith SS. 1991. Progesterone administration attenuates excitatory amino acid responses of cerebellar Purkinje cells. Neuroscience 42:309-320.
83. Smith SS, Waterhouse BD, Woodward DJ. 1987a, Sex steroid effects on extrahypothalamic CNS. II. Progesterone, alone and in combination with estrogen, modulates cerebellar responses to amino acid neurotransmitters. Brain Res 422:52-62.
84. Smith SS, Waterhouse BD, Woodward DJ. 1987b. Locally applied progesterone metabolites alter neuronal responsiveness in the cerebellum. Brain Res Bull 18:739-747.
85. Smith SS, Waterhouse BD, Chapin JK, Woodward DJ. 1987c. Progesterone alters GABA and glutamate responsiveness: a possible mechanism for its anxiolytic action. Brain Res 406:353-359.
86. Stein DG. 2005. The case for progesterone. Ann NY Acad Sci 1052: 152-169.
87. Sweatt JD. 2001. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10.
88. Swiatek-De Lange M, Stampfl A, Hauck SM, Zaschka H, Gloeckner CJ, Deeg CA, Ueffing M. 2007. Membrane-initiated effects of progesterone on calcium dependent signaling and activation of VEGF gene expression in retinal glial cells. Glia 55:1061-1073.
89. Thomas P. 2008. Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Front Neuroendocrinol 29:292-312.
90. Tsutsui K, Sakamoto H, Shikimi H, Ukena K. 2004. Organizing actions of neurosteroids in the Purkinje neuron. Neurosci Res 49:273-279.
91. Vallee M, Mayo W, Le Moal M. 2001. Role of pregnenolone, dehydroepiandrosterone and their sulfate esters on learning and memory in cognitive aging. Brain Res Brain Res Rev 37:301-312.
92. van der Heide LP, Ramakers GM, Smidt MP. 2006. Insulin signaling in the central nervous system: learning to survive. Prog Neurobiol 79: 205-221.
93. A receptors. Neuropharmacology 52:146-155.
94. 18F]FPS. Synapse 61:540-546.
95. 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.
96. Zhao H, Sapolsky RM, Steinberg GK. 2006. Phosphoinositide-3-kinase/akt survival signal pathways are implicated in neuronal survival after stroke. Mol Neurobiol 34:249-270.
97. Zhu Y, Rice CD, Pang Y, Pace M, Thomas P. 2003. Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc Natl Acad Sci USA 100:2231-2236.