Continuous versus cyclic progesterone exposure differentially regulates hippocampal gene expression and functional profiles

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Zhao, Liqin ^a   Morgan, Todd E ^a   Mao, Zisu ^a   Lin, Sharon ^a   Cadenas, Enrique ^a   Finch, Caleb E ^a   Pike, Christian J ^a   Mack, Wendy J ^b   Brinton, Roberta D ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; PROGESTERONE; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR MEMBRANE COMPONENT 1; UNCLASSIFIED DRUG; AMYLOID PROTEIN; ESTROGEN; F(6) ATPASE; LIVER X RECEPTOR; ORPHAN NUCLEAR RECEPTOR; PEROXIREDOXIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATP SYNTHASE ALPHA SUBUNIT GENE; BETA SECRETASE 1 GENE; CONTROLLED STUDY; DOSAGE SCHEDULE COMPARISON; FEMALE; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIGH THROUGHPUT SEQUENCING; HIPPOCAMPUS; INSULIN LIKE GROWTH FACTOR 1 GENE; LIVER X RECEPTOR ALPHA SUBTYPE GENE; LONG TERM EXPOSURE; NONHUMAN; PEROXIREDOXIN 5 GENE; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RAT; ANIMAL; BIOLOGY; COUPLING FACTOR; HOMEOSTASIS; METABOLISM; METHODOLOGY; MITOCHONDRION; OVARIECTOMY; OXIDATION REDUCTION REACTION;

RATTUS;

AMYLOIDOGENIC PROTEINS; ANIMALS; COMPUTATIONAL BIOLOGY; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HOMEOSTASIS; INSULIN-LIKE GROWTH FACTOR I; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; ORPHAN NUCLEAR RECEPTORS; OVARIECTOMY; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION COUPLING FACTORS; PEROXIREDOXINS; PROGESTERONE; RATS; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE;

EID: 84863258361     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031267     Document Type: Article

References (58)

1. Brinton RD, Nilsen J, (2003) Effects of estrogen plus progestin on risk of dementia. JAMA 290: 1706.
2. Nilsen J, Brinton RD, (2003) Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling. Proc Natl Acad Sci U S A 100: 10506-10511.
3. Brinton RD, Thompson RF, Foy MR, Baudry M, Wang J, et al. (2008) Progesterone receptors: form and function in brain. Front Neuroendocrinol 29: 313-339.
4. Rapp SR, Espeland MA, Shumaker SA, Henderson VW, Brunner RL, et al. (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.
5. Shumaker SA, Legault C, Rapp SR, Thal L, Wallace RB, et al. (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.
6. Espeland MA, Rapp SR, Shumaker SA, Brunner R, Manson JE, et al. (2004) Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291: 2959-2968.
7. Shumaker SA, Legault C, Kuller LH, Rapp SR, Thal L, et al. (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.
8. Irwin RW, Yao J, Ahmed SS, Hamilton RT, Cadenas E, et al. (2011) Medroxyprogesterone acetate antagonizes estrogen up-regulation of brain mitochondrial function. Endocrinology 152: 556-567.
9. Yao J, Chen S, Cadenas E, Brinton RD, (2011) Estrogen protection against mitochondrial toxin-induced cell death in hippocampal neurons: antagonism by progesterone. Brain research 1379: 2-10.
10. Irwin RW, Yao J, Hamilton RT, Cadenas E, Brinton RD, et al. (2008) Progesterone and estrogen regulate oxidative metabolism in brain mitochondria. Endocrinology 149: 3167-3175.
11. Carroll JC, Rosario ER, Chang L, Stanczyk FZ, Oddo S, et al. (2007) Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3xTg-AD mice. J Neurosci 27: 13357-13365.
12. Carroll JC, Rosario ER, Villamagna A, Pike CJ, (2010) Continuous and cyclic progesterone differentially interact with estradiol in the regulation of Alzheimer-like pathology in female 3xTransgenic-Alzheimer's disease mice. Endocrinology 151: 2713-2722.
13. Kohama SG, Anderson CP, Finch CE, (1989) Progesterone implants extend the capacity for 4-day estrous cycles in aging C57BL/6J mice and protect against acyclicity induced by estradiol. Biology of reproduction 41: 233-244.
14. Rowe WB, Blalock EM, Chen KC, Kadish I, Wang D, et al. (2007) Hippocampal expression analyses reveal selective association of immediate-early, neuroenergetic, and myelinogenic pathways with cognitive impairment in aged rats. The Journal of neuroscience: the official journal of the Society for Neuroscience 27: 3098-3110.
15. Kadish I, Thibault O, Blalock EM, Chen KC, Gant JC, et al. (2009) Hippocampal and cognitive aging across the lifespan: a bioenergetic shift precedes and increased cholesterol trafficking parallels memory impairment. The Journal of neuroscience: the official journal of the Society for Neuroscience 29: 1805-1816.
16. Yao J, Irwin RW, Zhao L, Nilsen J, Hamilton RT, et al. (2009) Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proceedings of the National Academy of Sciences of the United States of America 106: 14670-14675.
17. Miller JA, Oldham MC, Geschwind DH, (2008) A systems level analysis of transcriptional changes in Alzheimer's disease and normal aging. The Journal of neuroscience: the official journal of the Society for Neuroscience 28: 1410-1420.
18. Abrahams JP, Leslie AG, Lutter R, Walker JE, (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370: 621-628.
19. Boyer PD, (1997) The ATP synthase-a splendid molecular machine. Annual review of biochemistry 66: 717-749.
20. Das AM, (2003) Regulation of the mitochondrial ATP-synthase in health and disease. Molecular genetics and metabolism 79: 71-82.
21. Reed T, Perluigi M, Sultana R, Pierce WM, Klein JB, et al. (2008) Redox proteomic identification of 4-hydroxy-2-nonenal-modified brain proteins in amnestic mild cognitive impairment: insight into the role of lipid peroxidation in the progression and pathogenesis of Alzheimer's disease. Neurobiology of disease 30: 107-120.
22. Schmidt C, Lepsverdize E, Chi SL, Das AM, Pizzo SV, et al. (2008) Amyloid precursor protein and amyloid beta-peptide bind to ATP synthase and regulate its activity at the surface of neural cells. Molecular psychiatry 13: 953-969.
23. Terni B, Boada J, Portero-Otin M, Pamplona R, Ferrer I, (2010) Mitochondrial ATP-synthase in the entorhinal cortex is a target of oxidative stress at stages I/II of Alzheimer's disease pathology. Brain pathology 20: 222-233.
24. Rhee SG, Kang SW, Chang TS, Jeong W, Kim K, (2001) Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52: 35-41.
25. Wood ZA, Schroder E, Robin Harris J, Poole LB, (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28: 32-40.
26. Patenaude A, Murthy MR, Mirault ME, (2005) Emerging roles of thioredoxin cycle enzymes in the central nervous system. Cell Mol Life Sci 62: 1063-1080.
27. Cox AG, Winterbourn CC, Hampton MB, (2010) Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. The Biochemical journal 425: 313-325.
28. Declercq JP, Evrard C, Clippe A, Stricht DV, Bernard A, et al. (2001) Crystal structure of human peroxiredoxin 5, a novel type of mammalian peroxiredoxin at 1.5 A resolution. J Mol Biol 311: 751-759.
29. Smeets A, Marchand C, Linard D, Knoops B, Declercq JP, (2008) The crystal structures of oxidized forms of human peroxiredoxin 5 with an intramolecular disulfide bond confirm the proposed enzymatic mechanism for atypical 2-Cys peroxiredoxins. Arch Biochem Biophys 477: 98-104.
30. Yao J, Hamilton RT, Cadenas E, Brinton RD, (2010) Decline in mitochondrial bioenergetics and shift to ketogenic profile in brain during reproductive senescence. Biochimica et biophysica acta 1800: 1121-1126.
31. Blalock EM, Grondin R, Chen KC, Thibault O, Thibault V, et al. (2010) Aging-related gene expression in hippocampus proper compared with dentate gyrus is selectively associated with metabolic syndrome variables in rhesus monkeys. The Journal of neuroscience: the official journal of the Society for Neuroscience 30: 6058-6071.
32. McRory JE, Sherwood NM, (1997) Ancient divergence of insulin and insulin-like growth factor. DNA and cell biology 16: 939-949.
33. Torres-Aleman I, (2010) Toward a comprehensive neurobiology of IGF-I. Developmental neurobiology 70: 384-396.
34. Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I, (2002) Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nature medicine 8: 1390-1397.
35. Sharma S, Prasanthi RPJ, Schommer E, Feist G, Ghribi O, (2008) Hypercholesterolemia-induced Abeta accumulation in rabbit brain is associated with alteration in IGF-1 signaling. Neurobiology of disease 32: 426-432.
36. Zhao WQ, Lacor PN, Chen H, Lambert MP, Quon MJ, et al. (2009) Insulin receptor dysfunction impairs cellular clearance of neurotoxic oligomeric a{beta}. The Journal of biological chemistry 284: 18742-18753.
37. Garcia-Segura LM, Sanz A, Mendez P, (2006) Cross-talk between IGF-I and estradiol in the brain: focus on neuroprotection. Neuroendocrinology 84: 275-279.
38. Garcia-Segura LM, Arevalo MA, Azcoitia I, (2010) Interactions of estradiol and insulin-like growth factor-I signalling in the nervous system: new advances. Progress in brain research 181: 251-272.
39. Chesik D, De Keyser J, (2010) Progesterone and dexamethasone differentially regulate the IGF-system in glial cells. Neuroscience letters 468: 178-182.
40. Zhao C, Dahlman-Wright K, (2010) Liver X receptor in cholesterol metabolism. The Journal of endocrinology 204: 233-240.
41. Vaya J, Schipper HM, (2007) Oxysterols, cholesterol homeostasis, and Alzheimer disease. Journal of neurochemistry 102: 1727-1737.
42. Cole SL, Vassar R, (2008) The role of amyloid precursor protein processing by BACE1, the beta-secretase, in Alzheimer disease pathophysiology. The Journal of biological chemistry 283: 29621-29625.
43. Hampel H, Shen Y, (2009) Beta-site amyloid precursor protein cleaving enzyme 1 (BACE1) as a biological candidate marker of Alzheimer's disease. Scandinavian journal of clinical and laboratory investigation 69: 8-12.
44. Guennoun R, Gasc JM, (1990) Estrogen-independent and estrogen-induced progesterone receptors, and their regulation by progestins in the hypothalamus and pituitary of the chick embryo: an immunohistochemical study. Brain research Developmental brain research 55: 151-159.
45. Intlekofer KA, Petersen SL, (2011) 17beta-estradiol and progesterone regulate multiple progestin signaling molecules in the anteroventral periventricular nucleus, ventromedial nucleus and sexually dimorphic nucleus of the preoptic area in female rats. Neuroscience 176: 86-92.
46. Guerra-Araiza C, Villamar-Cruz O, Gonzalez-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. Journal of neuroendocrinology 15: 984-990.
47. Szabo M, Kilen SM, Nho SJ, Schwartz NB, (2000) Progesterone receptor A and B messenger ribonucleic acid levels in the anterior pituitary of rats are regulated by estrogen. Biology of reproduction 62: 95-102.
48. Bali N, Arimoto J, Iwata N, Lin S, Zhao L, et al. (2011) Differential responses of progesterone receptor membrane component-1 (Pgrmc1) and the classical progesterone receptor (Pgr) to 17b-estradiol and progesterone in hippocampal subregions that support synaptic remodeling and neurogenesis. Endocrinology In Press.
49. Quadros PS, Wagner CK, (2008) Regulation of progesterone receptor expression by estradiol is dependent on age, sex and region in the rat brain. Endocrinology 149: 3054-3061.
50. Marriott LK, McGann-Gramling KR, Hauss-Wegrzyniak B, Sheldahl LC, Shapiro RA, et al. (2007) Estrogen replacement regimen and brain infusion of lipopolysaccharide differentially alter steroid receptor expression in the uterus and hypothalamus. Endocrine 32: 317-328.
51. Rohe HJ, Ahmed IS, Twist KE, Craven RJ, (2009) PGRMC1 (progesterone receptor membrane component 1): a targetable protein with multiple functions in steroid signaling, P450 activation and drug binding. Pharmacology & therapeutics 121: 14-19.
52. Viero C, Mechaly I, Aptel H, Puech S, Valmier J, et al. (2006) Rapid inhibition of Ca2+ influx by neurosteroids in murine embryonic sensory neurones. Cell calcium 40: 383-391.
53. Peluso JJ, Romak J, Liu X, (2008) Progesterone receptor membrane component-1 (PGRMC1) is the mediator of progesterone's antiapoptotic action in spontaneously immortalized granulosa cells as revealed by PGRMC1 small interfering ribonucleic acid treatment and functional analysis of PGRMC1 mutations. Endocrinology 149: 534-543.
54. Sakamoto H, Ukena K, Takemori H, Okamoto M, Kawata M, et al. (2004) Expression and localization of 25-Dx, a membrane-associated putative progesterone-binding protein, in the developing Purkinje cell. Neuroscience 126: 325-334.
55. Liu L, Wang J, Zhao L, Nilsen J, McClure K, et al. (2009) Progesterone increases rat neural progenitor cell cycle gene expression and proliferation via extracellularly regulated kinase and progesterone receptor membrane components 1 and 2. Endocrinology 150: 3186-3196.
56. Goulter AB, Harmer DW, Clark KL, (2006) Evaluation of low density array technology for quantitative parallel measurement of multiple genes in human tissue. BMC Genomics 7: 34.
57. Denisov V, Strong W, Walder M, Gringrich J, Wintz H, (2008) Development and validation of RQI: an RNA Quality Indicator for the Experion Automated Electrophoresis System. Bio-Rad Electrophoresis Tech Note 5761.
58. Livak KJ, Schmittgen TD, (2008) Analyzing real-time PCR data using the comparative Ct method. Nature Protocols 3: 1101-1108.