In vitro follicle growth under non-attachment conditions and decreased FSH levels reduces Lhcgr expression in cumulus cells and promotes oocyte developmental competence

Journal of Assisted Reproduction and Genetics

Volumn 29, Issue 2, 2012, Pages 141-152

  Sánchez, Flor ^a   Romero, Sergio ^a   Albuz, Firas K ^a   Smitz, Johan ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

Follicle culture; Follicle stimulating hormone; Gene expression; Luteinizing hormone receptor; Oocyte competence

Indexed keywords

ESTRADIOL; FOLLITROPIN; GROWTH DIFFERENTIATION FACTOR 9; MESSENGER RNA; PROGESTERONE; STEROID;

AMH GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CELL CULTURE; CELL SURVIVAL; CONFORMATION; CONTROLLED STUDY; CUMULUS CELL; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION; HORMONE SYNTHESIS; IN VITRO OOCYTE MATURATION; LHCGR GENE; MATER GENE; MEIOSIS; MOUSE; NMP2 GENE; NON ATTACHMENT CONDITION; NONHUMAN; NUCLEOLUS; NUCLEOTIDE SEQUENCE; OOCYTE; OOCYTE DEVELOPMENT; OVARY FOLLICLE; POLAR BODY; PRIORITY JOURNAL;

ANIMALS; CELL CULTURE TECHNIQUES; CUMULUS CELLS; FEMALE; FERTILIZATION IN VITRO; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, INBRED C57BL; OOCYTES; OVARIAN FOLLICLE; RECEPTORS, LH;

EID: 84857634635     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-011-9690-x     Document Type: Article

References (55)

1. JJ Eppig MJ O'Brien 1996 Development in vitro of mouse oocytes from primordial follicles Biol Reprod 54 197 207 8838017 10.1095/biolreprod54.1.197 1:CAS:528:DyaK2MXhtVSisLjO (Pubitemid 126506815)
2. R Cortvrindt J Smitz AC Van Steirteghem 1996 In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system Hum Reprod 11 2656 2666 9021369 1:STN:280:DyaK2s7ntlClsQ%3D%3D (Pubitemid 27060736)
3. MJ O'Brien JK Pendola JJ Eppig 2003 A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence Biol Reprod 68 1682 1686 12606400 10.1095/biolreprod.102.013029 (Pubitemid 36519772)
4. J Smitz MM Dolmans J Donnez JE Fortune O Hovatta K Jewgenow, et al. 2010 Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation Hum Reprod Update 16 395 414 20124287 10.1093/humupd/dmp056 1:STN:280:DC%2BC3cvhtlymtQ%3D%3D
5. A Trounson C Anderiesz G Jones 2001 Maturation of human oocytes in vitro and their developmental competence Reproduction 121 51 75 11226029 10.1530/rep.0.1210051 1:CAS:528:DC%2BD3MXnslakuw%3D%3D (Pubitemid 32124515)
6. JE Smitz RG Cortvrindt 2002 The earliest stages of folliculogenesis in vitro Reproduction 123 185 202 11866686 10.1530/rep.0.1230185 1:CAS:528:DC%2BD38XhsFChsbo%3D (Pubitemid 34144669)
7. DH Kim DS Ko HC Lee HJ Lee WI Park SS Kim, et al. 2004 Comparison of maturation, fertilization, development, and gene expression of mouse oocytes grown in vitro and in vivo J Assist Reprod Genet 21 233 240 15526980 10.1023/B:JARG.0000042008.83699.cc (Pubitemid 39237798)
8. CMH Combelles RA Fissore DF Albertini C Racowsky 2005 In vitro maturation of human oocytes and cumulus cells using a co-culture three-dimensional collagen gel system Hum Reprod 20 1349 1358 15695316 10.1093/humrep/deh750 1:CAS:528:DC%2BD2MXjsFOmsbk%3D (Pubitemid 40790263)
9. JJ Eppig MJ O'Brien K Wigglesworth A Nicholson W Zhang BA King 2009 Effect of in vitro maturation oocytes on the health of adult offspring Hum Reprod 24 922 928 19151027 10.1093/humrep/den466 1:STN:280: DC%2BD1M3htlyrsw%3D%3D
10. JJ Eppig MJ O'Brien FL Pendola S Watanabe 1998 Factors affecting the developmental competence of mouse oocytes grown in vitro: follicle-stimulating hormone and insulin Biol Reprod 59 1445 1453 9828191 10.1095/biolreprod59.6.1445 1:CAS:528:DyaK1cXnvVOit7s%3D (Pubitemid 28549862)
11. KE Latham FDM Bautista Y Hirao MJ O'Brien JJ Eppig 1999 Comparison of protein synthesis patterns in mouse cumulus cells and mural granulosa cells: effects of follicle-stimulating hormone and insulin on granulosa cell differentiation in vitro Biol Reprod 61 482 492 10411531 10.1095/biolreprod61.2. 482 1:CAS:528:DyaK1MXkslKqt7o%3D (Pubitemid 29344768)
12. JJ Eppig M Hosoe MJ O'Brien FM Pendola A Requena S Watanabe 2000 Conditions that affect acquisition of developmental competence by mouse oocytes in vitro: FSH, insulin, glucose and ascorbic acid Mol Cell Endocrinol 163 109 116 10963882 10.1016/S0303-7207(99)00247-6 1:CAS:528:DC%2BD3cXlvV2ms7o%3D (Pubitemid 30645593)
13. F Sánchez T Adriaenssens S Romero J Smitz 2010 Different follicle-stimulating hormone exposure regimens during antral follicle growth alter gene expression in the cumulus-oocyte complex in mice Biol Reprod 83 514 524 20592308 10.1095/biolreprod.109.083311
14. F Sánchez S Romero J Smitz 2011 Oocyte and cumulus cell transcripts from cultured mouse follicles are induced to deviate from normal in vivo condition by combinations of insulin, follicle-stimulating hormone, and human chorionic gonadotropin Biol Reprod 85 565 574 21565993 10.1095/biolreprod.111.091744
15. PL Nayudu SM Osborn 1992 Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro J Reprod Fertil 95 349 362 1517993 10.1530/jrf.0.0950349 1:CAS:528:DyaK38Xlt1Cqurs%3D
16. LM Mitchell CR Kennedy GM Hartshorne 2002 Effects of varying gonadotropin dose and timing on antrum formation and ovulation efficiency of mouse follicles in vitro Hum Reprod 17 1181 1188 11980736 10.1093/humrep/17.5.1181 1:CAS:528:DC%2BD38Xks1Sqtrg%3D (Pubitemid 34537347)
17. I Adriaens R Cortvrindt J Smitz 2004 Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence Hum Reprod 19 398 408 14747188 10.1093/humrep/deh074 1:CAS:528:DC%2BD2cXos1entQ%3D%3D (Pubitemid 38220014)
18. PL Nayudu A Fehrenbach P Kiesel UA Vitt K Pancharatna S Osborn 2001 Progress toward understanding follicle development in vitro: appearances are not deceiving Arch Med Res 32 587 594 11750734 10.1016/S0188-4409(01)00339-3 1:CAS:528:DC%2BD38XltVentg%3D%3D (Pubitemid 34031751)
19. N Spears NI Boland AA Murray RG Gosden 1994 Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile Hum Reprod 9 527 532 8006146 1:STN:280:DyaK2c3nsVymsQ%3D%3D (Pubitemid 24096411)
20. UM Rose RG Hanssen HJ Kloosterboer 1999 Development and characterization of an in vitro ovulation model using mouse ovarian follicles Biol Reprod 61 503 511 10411533 10.1095/biolreprod61.2.503 1:CAS:528:DyaK1MXkslKqt7g%3D (Pubitemid 29344770)
21. UA Vitt PL Nayudu UM Rose HJ Kloosterboer 2001 Embryonic development after follicle culture is influenced by follicle-stimulating hormone isoelectric point range Biol Reprod 65 1542 1547 11673273 10.1095/biolreprod65.5.1542 1:CAS:528:DC%2BD3MXnvVersLo%3D (Pubitemid 33031514)
22. C Bishonga Y Takahashi S Katagiri M Nagano A Ishikawa 2001 In vitro growth of mouse ovarian preantral follicles and the capacity of their oocytes to develop to the blastocyst stage J Vet Med Sci 63 619 624 11459007 10.1292/jvms.63.619 1:STN:280:DC%2BD38%2Fit1Kgsw%3D%3D (Pubitemid 33641623)
23. SA Pangas H Saudye L Shea T Woodruff 2003 Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes Tissue Eng 9 1013 1021 14633385 10.1089/107632703322495655 1:CAS:528:DC%2BD3sXotlejtLk%3D (Pubitemid 37296832)
24. M Xu E West LD Shea TK Woodruff 2006 Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development Biol Reprod 75 916 923 16957022 10.1095/biolreprod.106.054833 1:CAS:528:DC%2BD28Xht1yjtr7O (Pubitemid 44845598)
25. E West-Farrell M Xu MA Gomberg YH Chow TK Woodruff LD Shea 2009 The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles Biol Reprod 80 432 439 19005169 10.1095/biolreprod.108.071142 1:CAS:528:DC%2BD1MXis1amtL4%3D
26. R Cortvrindt J Smitz 2002 Follicle culture in reproductive toxicology: a tool for in-vitro testing of ovarian function? Hum Reprod Update 8 243 254 12078835 10.1093/humupd/8.3.243 1:STN:280:DC%2BD38zjs1ygsA%3D%3D (Pubitemid 34618943)
27. S Romero F Sánchez T Adriaenssens J Smitz 2011 Mouse cumulus-oocyte complexes from in vitro-cultured preantral follicles suggest an anti-luteinizing role for the EGF cascade in the cumulus cells Biol Reprod 84 1164 1170 21293035 10.1095/biolreprod.110.087551 1:CAS:528:DC%2BC3MXmvFemurs%3D
28. NI Boland PG Humpherson HJ Leese RG Gosden 1993 Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro Biol Reprod 48 798 806 8485244 10.1095/biolreprod48.4.798 1:CAS:528:DyaK3sXks1enuro%3D (Pubitemid 23096949)
29. I Segers T Adriaenssens E Ozturk J Smitz 2010 Acquisition and loss of oocyte meiotic and developmental competence during in vitro antral follicle growth in mouse Fertil Steril 93 2695 2700 20056201 10.1016/j.fertnstert.2009. 11.035
30. S Romero J Smitz 2010 Improvement of in vitro culture of mouse cumulus-oocyte complexes using PDE3-inhibitor followed by meiosis induction with epiregulin Fertil Steril 93 936 944 19022432 10.1016/j.fertnstert.2008.10.016 1:CAS:528:DC%2BC3cXjsFemsrc%3D
31. M Convery JR Brawer 1991 Thecal and interstitial cells in polycystic ovaries (PCO) in the rat Anat Rec 231 324 332 1763814 10.1002/ar.1092310305 1:STN:280:DyaK387gvFaqtA%3D%3D
32. S Lenie J Smitz 2008 Estrogen receptor subtypes localization shifts in cultured mouse ovarian follicles Histochem Cell Biol 129 827 840 18330591 10.1007/s00418-008-0408-9 1:CAS:528:DC%2BD1cXlvFajtL4%3D
33. D Wickramasinghe KM Ebert DF Albertini 1991 Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes Dev Biol 143 162 172 1985016 10.1016/0012-1606(91)90063-9 1:STN:280:DyaK3M%2FosFKntA%3D%3D (Pubitemid 121004214)
34. M Zuccotti A Piccinelli P Giorgi Rossi S Garagna CA Redi 1995 Chromatin organization during mouse oocyte growth Mol Reprod Dev 41 479 485 7576615 10.1002/mrd.1080410410 1:CAS:528:DyaK2MXnt1Wrsbs%3D
35. M Zuccotti P Giorgi Rossi A Martinez S Garagna A Forabosco CA Redi 1998 Meiotic and developmental competence of mouse antral oocytes Biol Reprod 58 700 704 9510956 10.1095/biolreprod58.3.700 1:CAS:528:DyaK1cXhtlagurc%3D (Pubitemid 28117067)
36. C Bouniol-Baly L Hamraoui J Guibert N Beaujean MS Szollosi P Debey 1999 Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes Biol Reprod 60 580 587 10026102 10.1095/biolreprod60.3.580 1:CAS:528:DyaK1MXhsFekt7o%3D (Pubitemid 29102386)
37. R De La Fuente 2006 Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes Dev Biol 296 1 12 10.1016/j.ydbio.2006.04.445 (Pubitemid 44061759)
38. A Fehrenbach N Nüsse PL Nayudu 1998 Patterns of growth, oestradiol and progesterone released by in vitro cultured mouse ovarian follicles indicate consecutive selective events during follicle development J Reprod Fertil 113 287 297 9861169 10.1530/jrf.0.1130287 1:CAS:528:DyaK1cXntFOmsro%3D
39. UA Vitt HJ Kloosterboer UM Rose JW Mulders PS Kiesel S Bete, et al. 1998 Isoforms of human recombinant follicle-stimulating hormone: comparison of effects on murine follicle development in vitro Biol Reprod 59 854 861 9746735 10.1095/biolreprod59.4.854 1:CAS:528:DyaK1cXmsVGrsbo%3D (Pubitemid 28463337)
40. NM Rowghani MK Heise D McKeel EA McGee RR Koepsel AJ Russell 2004 Maintenance of morphology and growth of ovarian follicles in suspension culture Tissue Eng 10 545 552 15165471 10.1089/107632704323061906 (Pubitemid 38580275)
41. PK Kreeger JW Deck TK Woodruff LD Shea 2006 The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels Biomaterials 27 714 723 16076485 10.1016/j.biomaterials.2005.06.016 1:CAS:528:DC%2BD2MXhtFakur3E (Pubitemid 41483822)
42. J Wu PL Nayudu PS Kiesel HW Michelmann 2000 Luteinizing hormone has a stage-limited effect on preantral follicle development in vitro Biol Reprod 63 320 327 10859274 10.1095/biolreprod63.1.320 1:CAS:528:DC%2BD3cXktl2rsbg%3D (Pubitemid 30429417)
43. JE Gomes SC Correia A Gouveia-Oliveira AJ Cidadão CE Plancha 1999 Three-dimensional environments preserve extracellular matrix compartments of ovarian follicles and increase FSH-dependent growth Mol Reprod Dev 54 163 172 10471476 10.1002/(SICI)1098-2795(199910)54:2<163::AID-MRD8>3.0.CO;2-4 1:CAS:528:DyaK1MXmtVSktb0%3D (Pubitemid 29422271)
44. SG Hillier PF Whitelaw CD Smyth 1994 Follicular oestrogen synthesis: the 'two-cell, two-gonadotrophin' model revisited Mol Cell Endocrinol 100 51 54 8056158 10.1016/0303-7207(94)90278-X 1:CAS:528:DyaK2cXktVWisLk%3D (Pubitemid 24109526)
45. MJ Carabatsos J Elvin MM Matzuk DF Albertini 1998 Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice Dev Biol 204 373 384 9882477 10.1006/dbio.1998.9087 1:CAS:528: DyaK1MXmtF2ltA%3D%3D (Pubitemid 29024486)
46. JA Elvin AT Clark P Wang NM Wolfman MM Matzuk 1999 Paracrine actions of growth differentiation factor-9 in the mammalian ovary Mol Endocrinol 13 1035 1048 10379900 10.1210/me.13.6.1035 1:CAS:528:DyaK1MXjs1yns7c%3D (Pubitemid 30645319)
47. UA Vitt M Hayashi C Klein AJW Hsueh 2000 Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles Biol Reprod 62 370 377 10642575 10.1095/biolreprod62.2.370 1:CAS:528:DC%2BD3cXotVOqsA%3D%3D (Pubitemid 30067338)
48. RB Gilchrist LJ Ritter DT Armstrong 2004 Oocyte-somatic cell interactions during follicle development in mammals Anim Reprod Sci 82-83 431 446 15271471 10.1016/j.anireprosci.2004.05.017 (Pubitemid 39027077)
49. ZB Tong L Gold KE Pfeifer H Dorward E Lee CA Bondy, et al. 2000 Mater, a maternal effect gene required for early embryonic development in mice Nature Genet 26 267 740 11062459 10.1038/81547 1:CAS:528:DC%2BD3cXotVWhs7c%3D
50. KH Burns MM Viveiros Y Ren P Wang FJ DeMayo DE Frail, et al. 2003 Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos Science 300 633 636 12714744 10.1126/science.1081813 1:CAS:528:DC%2BD3sXjtVymu7w%3D (Pubitemid 36520586)
51. A Inoue F Aoki 2010 Role of the nucleoplasmin 2 C-terminal domain in the formation of nucleolus-like bodies in mouse oocytes FASEB J 24 485 494 19805576 10.1096/fj.09-143370 1:CAS:528:DC%2BC3cXhs1Ghu70%3D
52. WM Baarends JTJ Uilenbroek P Kramer JW Hoogerbrugge ECM van Leeuwen APN Themmen, et al. 1995 Anti-Müllerian hormone and anti-Müllerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth Endocrinol 136 4951 4962 10.1210/en.136.11.4951 1:CAS:528: DyaK2MXovFOltrs%3D
53. NA Salmon AH Handyside IM Joyce 2004 Oocyte regulation of anti-Müllerian hormone expression in granulosa cells during ovarian follicle development in mice Dev Biol 266 201 208 14729489 10.1016/j.ydbio.2003. 10.009 1:CAS:528:DC%2BD2cXltF2muw%3D%3D (Pubitemid 38083206)
54. FJ Diaz K Wigglesworth JJ Eppig 2007 Oocytes determine cumulus cell lineage in mouse ovarian follicles J Cell Sci 120 1330 1340 17389684 10.1242/jcs.000968 1:CAS:528:DC%2BD2sXlsFSjtLw%3D (Pubitemid 46780026)
55. ML Grøndahl ME Nielsen MB Dal Canto R Fadini IA Rasmussen LG Westergaard, et al. 2011 Anti-Müllerian hormone remains highly expressed in human cumulus cells during the final stages of folliculogenesis Reprod Biomed Online 22 389 398 21353640 10.1016/j.rbmo.2010.12.005