Minimal fertility defects in mice deficient in oocyte-expressed Smad4

Biology of Reproduction

Volumn 86, Issue 1, 2012, Pages

  Li, Xiaohui ^a   Tripurani, Swamy K ^a   James, Rebecca ^a   Pangas, Stephanie A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Activin; Egg; Follicular development; Infertility; Oocyte development; Ovary; Reproduction; Smad; Transgenic knockout model

Indexed keywords

CRE RECOMBINASE; GROWTH DIFFERENTIATION FACTOR 9; SMAD4 PROTEIN; CELL SURFACE RECEPTOR; EGG PROTEIN; GDF9 PROTEIN, MOUSE; MEMBRANE PROTEIN; SMAD4 PROTEIN, MOUSE; ZONA PELLUCIDA GLYCOPROTEINS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FEMALE INFERTILITY; GENE DELETION; HISTOLOGY; IMMUNOFLUORESCENCE; LITTER SIZE; MOUSE; NONHUMAN; OOCYTE; OVARY FOLLICLE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SUPEROVULATION; ZONA PELLUCIDA; ANIMAL; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; GRANULOSA CELL; METABOLISM; MOUSE MUTANT; OVARY; OVULATION; PHYSIOLOGY;

MUS;

ANIMALS; EGG PROTEINS; FEMALE; FERTILITY; GENE EXPRESSION REGULATION; GRANULOSA CELLS; GROWTH DIFFERENTIATION FACTOR 9; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; OOCYTES; OVARY; OVULATION; PROMOTER REGIONS, GENETIC; RECEPTORS, CELL SURFACE; SMAD4 PROTEIN;

EID: 84856820947     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.094375     Document Type: Article

References (46)

1. Matzuk MM, Burns K, Viveiros MM, Eppig J. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 2002; 296:2178-2180.
2. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001; 122:829-838.
3. Kidder GM, Vanderhyden BC. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can J Physiol Pharmacol 2010; 88:399-413.
4. Joyce IM, Pendola FL, Wigglesworth K, Eppig JJ. Oocyte regulation of kit ligand expression in mouse ovarian follicles. Dev Biol 1999; 214:342-353.
5. Thomas FH, Vanderhyden BC. Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reprod Biol Endocrinol 2006; 4:19.
6. Pangas S, Matzuk MM. The TGF-B family in the reproductive tract. In: Derynck R, Miyazono K (eds.), The TGF-beta family. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2008:861-888.
7. Myers M, Pangas SA. Regulatory roles of transforming growth factor beta family members in folliculogenesis. Wiley Interdiscip Rev Syst Biol Med 2010; 2:117-125.
8. Richards JS, Pangas SA. The ovary: basic biology and clinical implications. J Clin Invest 2010; 120:963-972.
9. Findlay JK, Drummond AE, Dyson ML, Baillie AJ, Robertson DM, Ethier JF. Recruitment and development of the follicle: the roles of the transforming growth factor-beta superfamily. Mol Cell Endocrinol 2002; 191:35-43.
10. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996; 383:531-535.
11. Myers M, Middlebrook BS, Matzuk MM, Pangas SA. Loss of inhibin alpha uncouples oocyte-granulosa cell dynamics and disrupts postnatal folliculogenesis. Dev Biol 2009; 334:458-467.
12. Carabatsos MJ, Elvin JA, Matzuk MM, Albertini DF. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev Biol 1998; 204:373-384.
13. Arnold SJ, Maretto S, Islam A, Bikoff EK, Robertson EJ. Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo. Dev Biol 2006; 296:104-118.
14. Chu GC, Dunn NR, Anderson DC, Oxburgh L, Robertson EJ. Differential requirements for Smad4 in TGFbeta-dependent patterning of the early mouse embryo. Development 2004; 131:3501-3512.
15. Tremblay KD, Dunn NR, Robertson EJ. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 2001; 128:3609-3621.
16. Tremblay KD, Hoodless PA, Bikoff EK, Robertson EJ. Formation of the definitive endoderm in mouse is a Smad2-dependent process. Development 2000; 127:3079-3090.
17. Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 1999; 126:1631-1642.
18. Huang Z, Wang D, Ihida-Stansbury K, Jones PL, Martin JF. Defective pulmonary vascular remodeling in Smad8 mutant mice. Hum Mol Genet 2009; 18:2791-2801.
19. Zhu Y, Richardson JA, Parada LF, Graff JM. Smad3 mutant mice develop metastatic colorectal cancer. Cell 1998; 94:703-714.
20. Li Q, Pangas SA, Jorgez CJ, Graff JM, Weinstein M, Matzuk MM. Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo. Mol Cell Biol 2008; 28:7001-7011.
21. Pangas SA, Li X, Robertson EJ, Matzuk MM. Premature luteinization and cumulus cell defects in ovarian-specific Smad4 knockout mice. Mol Endocrinol 2006; 20:1406-1422.
22. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin JF, Jamin SP, Behringer RR, Robertson EJ, Matzuk MM. Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol 2008; 28:248-257.
23. Sidis Y, Fujiwara T, Leykin L, Isaacson K, Toth T, Schneyer A. Characterization of inhibin/activin subunit, activin receptor, and follistatin messenger ribonucleic acid in human and mouse oocytes: evidence for activin's paracrine signaling from granulosa cells to oocytes. Biol Reprod 1998; 59:807-812.
24. Cameron V, Nishimura E, Mathews L, Lewis K, Sawchenko P, Vale W. Hybridization histochemical localization of activin receptor subtypes in rat brain, pituitary, ovary, and testis. Endocrinology 1994; 134:799-808.
25. Di Simone N, Crowley WF Jr, Wang QF, Sluss PM, Schneyer AL. Characterization of inhibin/activin subunit, follistatin, and activin type II receptors in human ovarian cancer cell lines: a potential role in autocrine growth regulation. Endocrinology 1996; 137:486-494.
26. Alak BM, Coskun S, Friedman CI, Kennard EA, Kim MH, Seifer DB. Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Fertil Steril 1998; 70:1126-1130.
27. Alak BM, Smith GD, Woodruff TK, Stouffer RL, Wolf DP. Enhancement of primate oocyte maturation and fertilization in vitro by inhibin A and activin A. Fertil Steril 1996; 66:646-653.
28. Pangas SA, Rademaker AW, Fishman DA, Woodruff TK. Localization of the activin signal transduction components in normal human ovarian follicles: implications for autocrine and paracrine signaling in the ovary. J Clin Endocrinol Metab 2002; 87:2644-2657.
29. Erickson GF, Shimasaki S. The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod Biol Endocrinol 2003; 1:9-28.
30. Feary ES, Juengel JL, Smith P, French MC, O'Connell AR, Lawrence SB, Galloway SM, Davis GH, McNatty KP. Patterns of expression of messenger RNAs encoding GDF9, BMP15, TGFBR1, BMPR1B, and BMPR2 during follicular development and characterization of ovarian follicular populations in ewes carrying the Woodlands FecX2W mutation. Biol Reprod 2007; 77:990-998.
31. Wilson T, Wu XY, Juengel JL, Ross IK, Lumsden JM, Lord EA, Dodds KG, Walling GA, McEwan JC, O'Connell AR, McNatty KP, Montgomery GW. Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol Reprod 2001; 64:1225-1235.
32. Abir R, Ben-Haroush A, Melamed N, Felz C, Krissi H, Fisch B. Expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB, and II in human ovaries from fetuses and adults. Fertil Steril 2008; 89:1430-1440.
33. Ingman WV, Robker RL, Woittiez K, Robertson SA. Null mutation in transforming growth factor beta1 disrupts ovarian function and causes oocyte incompetence and early embryo arrest. Endocrinology 2006; 147:835-845.
34. de Vries WN, Binns LT, Fancher KS, Dean J, Moore R, Kemler R, Knowles BB. Expression of Cre recombinase in mouse oocytes: a means to study maternal effect genes. Genesis 2000; 26:110-112.
35. Lan ZJ, Xu X, Cooney AJ. Differential oocyte-specific expression of Cre recombinase activity in GDF-9-iCre, Zp3cre, and Msx2Cre transgenic mice. Biol Reprod 2004; 71:1469-1474.
36. Lan ZJ, Gu P, Xu X, Jackson KJ, DeMayo FJ, O'Malley BW, Cooney AJ. GCNF-dependent repression of BMP-15 and GDF-9 mediates gamete regulation of female fertility. EMBO J 2003; 22:4070-4081.
37. Tripurani SK, Lee KB, Wang L, Wee G, Smith GW, Lee YS, Latham KE, Yao J. A novel functional role for the oocyte-specific transcription factor newborn ovary homeobox (NOBOX) during early embryonic development in cattle. Endocrinology 2011; 152:1013-1023.
38. Su YQ, Wu X, O'Brien MJ, Pendola FL, Denegre JN, Matzuk MM, Eppig JJ. Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol 2004; 276:64-73.
39. Pangas SA, Jorgez CJ, Tran M, Agno J, Li X, Brown CW, Kumar TR, Matzuk MM. Intraovarian activins are required for female fertility. Mol Endocrinol 2007; 21:2458-2471.
40. Yan C, Wang P, DeMayo J, DeMayo F, Elvin J, Carino C, Prasad S, Skinner S, Dunbar B, Dube J, Celeste A, Matzuk M. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 2001; 15:854-866.
41. Tian X, Halfhill AN, Diaz FJ. Localization of phosphorylated SMAD proteins in granulosa cells, oocytes and oviduct of female mice. Gene Expr Patterns 2010; 10:105-112.
42. Gueripel X, Benahmed M, Gougeon A. Sequential gonadotropin treatment of immature mice leads to amplification of transforming growth factor beta action, via upregulation of receptor-type 1, Smad 2 and 4, and downregulation of Smad 6. Biol Reprod 2004; 70:640-648.
43. Biggers JD, McLaren A, Michie D. Variance control in the animal house. Nature 1958; 182:77-80.
44. Sun QY, Liu K, Kikuchi K. Oocyte-specific knockout: a novel in vivo approach for studying gene functions during folliculogenesis, oocyte maturation, fertilization, and embryogenesis. Biol Reprod 2008; 79:1014-1020.
45. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T, Peng SL, Lan ZJ, Cooney AJ, et al. Oocytespecific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008; 319:611-613.
46. Jagarlamudi K, Liu L, Adhikari D, Reddy P, Idahl A, Ottander U, Lundin E, Liu K. Oocyte-specific deletion of Pten in mice reveals a stage-specific function of PTEN/PI3K signaling in oocytes in controlling follicular activation. PLoS One 2009; 4:e6186.