Gene bionetworks that regulate ovarian primordial follicle assembly

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Nilsson, Eric ^a   Zhang, Bin ^b   Skinner, Michael K ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Assembly; Female fertility; Genomics; Ovarian development; Ovary; PCO; POI; Primordial follicle; System biology; Transcriptome

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GROWTH HORMONE; HORMONE; MITOGEN ACTIVATED PROTEIN KINASE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DISEASE ASSOCIATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; HORMONAL THERAPY; HORMONE RESPONSE; NEWBORN; NONHUMAN; OOCYTE; OVARY DISEASE; OVARY FOLLICLE ASSEMBLY; OVARY FUNCTION; PROTEIN TARGETING; RAT; SYSTEMS BIOLOGY; TISSUE CULTURE;

ANIMALS; FEMALE; GENE REGULATORY NETWORKS; HORMONES; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; OVARIAN DISEASES; OVARIAN FOLLICLE; RATS; RATS, SPRAGUE-DAWLEY; SYSTEMS BIOLOGY; TRANSCRIPTOME;

RATTUS;

EID: 84880334158     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-496     Document Type: Article

References (55)

1. Nilsson EE, Schindler R, Savenkova MI, Skinner MK. Inhibitory actions of Anti-Mullerian Hormone (AMH) on ovarian primordial follicle assembly. PLoS One 2011, 6(5):e20087. 10.1371/journal.pone.0020087, 3103528, 21637711.
2. Hirshfield AN. Development of follicles in the mammalian ovary. Int Rev Cytol 1991, 124:43-101.
3. Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update 2005, 11(5):461-471. 10.1093/humupd/dmi020, 16006439.
4. Rajah R, Glaser EM, Hirshfield AN. The changing architecture of the neonatal rat ovary during histogenesis. Dev Dyn 1992, 194(3):177-192. 10.1002/aja.1001940303, 1467554.
5. Sarraj MA, Drummond AE. Mammalian foetal ovarian development: consequences for health and disease. Reproduction 2012, 143(2):151-163. 10.1530/REP-11-0247, 22106406.
6. Pepling ME. Follicular assembly: mechanisms of action. Reproduction 2012, 143(2):139-149. 10.1530/REP-11-0299, 22065859.
7. Richards JS, Pangas SA. The ovary: basic biology and clinical implications. J Clin Invest 2010, 120(4):963-972. 10.1172/JCI41350, 2846061, 20364094.
8. Pepling ME, Spradling AC. Female mouse germ cells form synchronously dividing cysts. Development 1998, 125(17):3323-3328.
9. Gondos B. Germ cell degeneration and intercellular bridges in the human fetal ovary. Z Zellforsch Mikrosk Anat 1973, 138(1):23-30. 10.1007/BF00307075, 4697124.
10. Byskov AG. Differentiation of mammalian embryonic gonad. Physiol Rev 1986, 66(1):71-117.
11. Borum K. Oogenesis in the mouse. A study of the meiotic prophase. Exp Cell Res 1961, 24:495-507. 10.1016/0014-4827(61)90449-9, 13871511.
12. McGee EA, Hsu SY, Kaipia A, Hsueh AJ. Cell death and survival during ovarian follicle development. Mol Cell Endocrinol 1998, 140(1-2):15-18.
13. Pepling ME, Sundman EA, Patterson NL, Gephardt GW, Medico L, Wilson KI. Differences in oocyte development and estradiol sensitivity among mouse strains. Reproduction 2010, 139(2):349-357. 10.1530/REP-09-0392, 19846484.
14. De Vos M, Devroey P, Fauser BC. Primary ovarian insufficiency. Lancet 2010, 376(9744):911-921. 10.1016/S0140-6736(10)60355-8, 20708256.
15. Maclaran K, Panay N. Premature ovarian failure. J Fam Plann Reprod Health Care 2011, 37(1):35-42. 10.1136/jfprhc.2010.0015, 21367702.
16. Schindler R, Nilsson E, Skinner MK. Induction of ovarian primordial follicle assembly by connective tissue growth factor CTGF. PLoS One 2010, 5(9):e12979. 10.1371/journal.pone.0012979, 2945314, 20886044.
17. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 2007, 148(8):3580-3590. 10.1210/en.2007-0088, 17446182.
18. Yang MY, Fortune JE. The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biol Reprod 2008, 78(6):1153-1161. 10.1095/biolreprod.107.066688, 18305225.
19. Wang C, Roy SK. Development of primordial follicles in the hamster: role of estradiol-17beta. Endocrinology 2007, 148(4):1707-1716.
20. Zachos NC, Billiar RB, Albrecht ED, Pepe GJ. Developmental regulation of baboon fetal ovarian maturation by estrogen. Biol Reprod 2002, 67(4):1148-1156. 10.1095/biolreprod67.4.1148, 12297530.
21. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW, Kipp JL, Shea LD, Mayo KE, Woodruff TK. Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool. Dev Biol 2006, 298(1):132-148. 10.1016/j.ydbio.2006.06.025, 16930587.
22. Nilsson EE, Skinner MK. Progesterone regulation of primordial follicle assembly in bovine fetal ovaries. Mol Cell Endocrinol 2009, 313(1-2):9-16. 2757495, 19747959.
23. Nilsson EE, Stanfield J, Skinner MK. Interactions between progesterone and tumor necrosis factor-alpha in the regulation of primordial follicle assembly. Reproduction 2006, 132(6):877-886. 10.1530/REP-06-0045, 17127748.
24. Marcinkiewicz JL, Balchak SK, Morrison LJ. The involvement of tumor necrosis factor-alpha (TNF) as an intraovarian regulator of oocyte apoptosis in the neonatal rat. Front Biosci 2002, 7:d1997-d2005. 10.2741/marcin, 12161343.
25. Morrison LJ, Marcinkiewicz JL. Tumor necrosis factor alpha enhances oocyte/follicle apoptosis in the neonatal rat ovary. Biol Reprod 2002, 66(2):450-457. 10.1095/biolreprod66.2.450, 11804962.
26. Trombly DJ, Woodruff TK, Mayo KE. Suppression of Notch signaling in the neonatal mouse ovary decreases primordial follicle formation. Endocrinology 2009, 150(2):1014-1024. 2646529, 18818300.
27. Spears N, Molinek MD, Robinson LL, Fulton N, Cameron H, Shimoda K, Telfer EE, Anderson RA, Price DJ. The role of neurotrophin receptors in female germ-cell survival in mouse and human. Development 2003, 130(22):5481-5491. 10.1242/dev.00707, 14507777.
28. Kerr B, Garcia-Rudaz C, Dorfman M, Paredes A, Ojeda SR. NTRK1 and NTRK2 receptors facilitate follicle assembly and early follicular development in the mouse ovary. Reproduction 2009, 138(1):131-140. 10.1530/REP-08-0474, 3150184, 19357131.
29. Wang J, Roy SK. Growth differentiation factor-9 and stem cell factor promote primordial follicle formation in the hamster: modulation by follicle-stimulating hormone. Biol Reprod 2004, 70(3):577-585.
30. Kezele PR, Ague JM, Nilsson E, Skinner MK. Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol Reprod 2005, 72(1):241-255. 10.1095/biolreprod.104.032060, 15371273.
31. Nilsson EE, Savenkova MI, Schindler R, Zhang B, Schadt EE, Skinner MK. Gene bionetwork analysis of ovarian primordial follicle development. PLoS One 2010, 5(7):e11637. 10.1371/journal.pone.0011637, 2905436, 20661288.
32. Zhang B, Horvath S. A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 2005, 4:17.
33. Lum PY, Chen Y, Zhu J, Lamb J, Melmed S, Wang S, Drake TA, Lusis AJ, Schadt EE. Elucidating the murine brain transcriptional network in a segregating mouse population to identify core functional modules for obesity and diabetes. J Neurochem 2006, 97(Suppl 1):50-62.
34. Millstein J, Winrow CJ, Kasarskis A, Owens JR, Zhou L, Summa KC, Fitzpatrick K, Zhang B, Vitaterna MH, Schadt EE, et al. Identification of causal genes, networks, and transcriptional regulators of REM sleep and wake. Sleep 2011, 34(11):1469-1477. 3198032, 22043117.
35. Wang IM, Zhang B, Yang X, Zhu J, Stepaniants S, Zhang C, Meng Q, Peters M, He Y, Ni C, et al. Systems analysis of eleven rodent disease models reveals an inflammatome signature and key drivers. Mol Syst Biol 2012, 8:594. 3421440, 22806142.
36. Schadt EE, Lamb J, Yang X, Zhu J, Edwards S, Guhathakurta D, Sieberts SK, Monks S, Reitman M, Zhang C, et al. An integrative genomics approach to infer causal associations between gene expression and disease. Nat Genet 2005, 37(7):710-717. 10.1038/ng1589, 2841396, 15965475.
37. Ravasz E, Somera AL, Mongru DA, Oltvai ZN, Barabasi AL. Hierarchical organization of modularity in metabolic networks. Science 2002, 297(5586):1551-1555. 10.1126/science.1073374, 12202830.
38. Arkell RS, Dickinson RJ, Squires M, Hayat S, Keyse SM, Cook SJ. DUSP6/MKP-3 inactivates ERK1/2 but fails to bind and inactivate ERK5. Cell Signal 2008, 20(5):836-843. 10.1016/j.cellsig.2007.12.014, 18280112.
39. Molina G, Vogt A, Bakan A, Dai W, de Queiroz Oliveira P, Znosko W, Smithgall TE, Bahar I, Lazo JS, Day BW, et al. Zebrafish chemical screening reveals an inhibitor of Dusp6 that expands cardiac cell lineages. Nat Chem Biol 2009, 5(9):680-687. 10.1038/nchembio.190, 2771339, 19578332.
40. Li G, Yu M, Lee WW, Tsang M, Krishnan E, Weyand CM, Goronzy JJ. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat Med 2012, 18(10):1518-1524. 10.1038/nm.2963, 3466346, 23023500.
41. Nilsson E, Rogers N, Skinner MK. Actions of anti-Mullerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 2007, 134(2):209-221. 10.1530/REP-07-0119, 17660231.
42. MacFarlane LA, Murphy PR. Regulation of FGF-2 by an endogenous antisense RNA: effects on cell adhesion and cell-cycle progression. Mol Carcinog 2010, 49(12):1031-1044. 10.1002/mc.20686, 20945415.
43. Yang D, Li Y, Xiao H, Liu Q, Zhang M, Zhu J, Ma W, Yao C, Wang J, Wang D, et al. Gaining confidence in biological interpretation of the microarray data: the functional consistence of the significant GO categories. Bioinformatics 2008, 24(2):265-271. 10.1093/bioinformatics/btm558, 18006543.
44. Zhu J, Wiener MC, Zhang C, Fridman A, Minch E, Lum PY, Sachs JR, Schadt EE. Increasing the power to detect causal associations by combining genotypic and expression data in segregating populations. PLoS Comput Biol 2007, 3(4):e69. 10.1371/journal.pcbi.0030069, 1851982, 17432931.
45. Gargalovic PS, Imura M, Zhang B, Gharavi NM, Clark MJ, Pagnon J, Yang WP, He A, Truong A, Patel S, et al. Identification of inflammatory gene modules based on variations of human endothelial cell responses to oxidized lipids. Proc Natl Acad Sci U S A 2006, 103(34):12741-12746. 10.1073/pnas.0605457103, 1568918, 16912112.
46. Horvath S, Zhang B, Carlson M, Lu KV, Zhu S, Felciano RM, Laurance MF, Zhao W, Qi S, Chen Z, et al. Analysis of oncogenic signaling networks in glioblastoma identifies ASPM as a molecular target. Proc Natl Acad Sci U S A 2006, 103(46):17402-17407. 10.1073/pnas.0608396103, 1635024, 17090670.
47. Holt JE, Jackson A, Roman SD, Aitken RJ, Koopman P, McLaughlin EA. CXCR4/SDF1 interaction inhibits the primordial to primary follicle transition in the neonatal mouse ovary. Dev Biol 2006, 293(2):449-460. 10.1016/j.ydbio.2006.02.012, 16545793.
48. Slot KA, Kastelijn J, Bachelot A, Kelly PA, Binart N, Teerds KJ. Reduced recruitment and survival of primordial and growing follicles in GH receptor-deficient mice. Reproduction 2006, 131(3):525-532. 10.1530/rep.1.00946, 16514195.
49. Dunaif A. Polycystic ovary syndrome in 2011: Genes, aging and sleep apnea in polycystic ovary syndrome. Nat Rev Endocrinol 2012, 8(2):72-74.
50. Dole G, Nilsson EE, Skinner MK. Glial-derived neurotrophic factor promotes ovarian primordial follicle development and cell-cell interactions during folliculogenesis. Reproduction 2008, 135(5):671-682. 10.1530/REP-07-0405, 18304989.
51. Oktay K, Schenken RS, Nelson JF. Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biol Reprod 1995, 53(2):295-301. 10.1095/biolreprod53.2.295, 7492681.
52. Parrott JA, Skinner MK. Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 1999, 140(9):4262-4271. 10.1210/en.140.9.4262, 10465300.
53. Skinner MK, Manikkam M, Haque MM, Zhang B, Savenkova M. Epigenetic Transgenerational Inheritance of Somatic Transcriptomes and Epigenetic Control Regions. Genome Biol 2012, 13(10):R91. 10.1186/gb-2012-13-10-r91, 3491419, 23034163.
54. Langfelder P, Horvath S. Eigengene networks for studying the relationships between co-expression modules. BMC Syst Biol 2007, 1:54. 10.1186/1752-0509-1-54, 2267703, 18031580.
55. Draghici S, Khatri P, Tarca AL, Amin K, Done A, Voichita C, Georgescu C, Romero R. A systems biology approach for pathway level analysis. Genome Res 2007, 17(10):1537-1545. 10.1101/gr.6202607, 1987343, 17785539.