Expression of maternally derived KHDC3, NLRP5, OOEP and TLE6 is associated with oocyte developmental competence in the ovine species

BMC Developmental Biology

Volumn 14, Issue 1, 2014, Pages

  Bebbere, Daniela ^a   Ariu, Federica ^a   Bogliolo, Luisa ^a   Masala, Laura ^a   Murrone, Ombretta ^a   Fattorini, Mauro ^a   Falchi, Laura ^a   Ledda, Sergio ^a  

^a UNIVERSITY OF SASSARI   (Italy)

Author keywords

Oocyte developmental competence; Ovine embryo; Subcortical maternal complex

Indexed keywords

MESSENGER RNA; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; BLASTOCYST; DOMESTIC SHEEP; EMBRYO DEVELOPMENT; FEMALE; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OOCYTE; PREGNANCY;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BLASTOCYST; EMBRYONIC DEVELOPMENT; FEMALE; FERTILITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MOLECULAR SEQUENCE DATA; OOCYTES; ORGAN SPECIFICITY; PREGNANCY; RNA, MESSENGER; RNA-BINDING PROTEINS; SHEEP, DOMESTIC; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84946405192     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/s12861-014-0040-y     Document Type: Article

References (54)

1. Li L, Baibakov B, Dean J: A subcortical maternal complex essential for preimplantation mouse embryogenesis. Dev Cell 2008, 15:416-425.
2. Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E, Bondy CA, Dean J, Nelson LM: Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet 2000, 26:267-268.
3. Tashiro F, Kanai-Azuma M, Miyazaki S, Kato M, Tanaka T, Toyoda S, Yamato E, Kawakami H, Miyazaki T, Miyazaki J: Maternal-effect gene Ces5/Ooep/Moep19/Floped is essential for oocyte cytoplasmic lattice formation and embryonic development at the maternal-zygotic stage transition. Genes Cells 2010, 15:813-828.
4. Zheng P, Dean J: Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis. Proc Natl Acad Sci U S A 2009, 106:7473-7478.
5. Dean J: Oocyte-specific genes regulate follicle formation, fertility and early mouse development. J Reprod Immunol 2002, 53:171-180.
6. Zheng P, Dean J: Oocyte-specific genes affect folliculogenesis, fertilization, and early development. Semin Reprod Med 2007, 25:243-251.
7. Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, Matzuk MM: Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet 2003, 33:187-191.
8. Tong ZB, Nelson LM: A mouse gene encoding an oocyte antigen associated with autoimmune premature ovarian failure. Endocrinology 1999, 140:3720-3726.
9. Gilbert SF: Developmental biology. 6th edition. Sunderland MA: Sinauer Associates; 2000.
10. Evsikov AV, Graber JH, Brockman JM, Hampl A, Holbrook AE, Singh P, Eppig JJ, Solter D, Knowles BB: Cracking the egg: molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo. Genes Dev 2006, 20:2713-2727.
11. Vallee M, Robert C, Methot S, Palin MF, Sirard MA: Cross-species hybridizations on a multi-species cDNA microarray to identify evolutionarily conserved genes expressed in oocytes. BMC Genomics 2006, 7:113.
12. Vallee M, Aiba K, Piao Y, Palin MF, Ko MS, Sirard MA: Comparative analysis of oocyte transcript profiles reveals a high degree of conservation among species. Reproduction 2008, 135:439-448.
13. Telford NA, Watson AJ, Schultz GA: Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 1999, 26:90-100.
14. Bettegowda A, Yao J, Sen A, Li Q, Lee KB, Kobayashi Y, Patel OV, Coussens PM, Ireland JJ, Smith GW: JY-1, an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle. Proc Natl Acad Sci U S A 2007, 104:17602-17607.
15. Hanrahan JP, Gregan SM, Mulsant P, Mullen M, Davis GH, Powell R, Galloway SM: Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol Reprod 2004, 70:900-909.
16. Moore RK, Erickson GF, Shimasaki S: Are BMP-15 and GDF-9 primary determinants of ovulation quota in mammals? Trends Endocrinol Metab 2004, 15:356-361.
17. Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, Beattie AE, Davis GH, Ritvos O: Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 2000, 25:279-283.
18. Galloway SM, Gregan SM, Wilson T, McNatty KP, Juengel JL, Ritvos O, Davis GH: Bmp15 mutations and ovarian function. Mol Cell Endocrinol 2002, 191:15-18.
19. Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, Celeste AJ, Matzuk MM: Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 2001, 15:854-866.
20. Dade S, Callebaut I, Mermillod P, Monget P: Identification of a new expanding family of genes characterized by atypical LRR domains: localization of a cluster preferentially expressed in oocyte. FEBS Lett 2003, 555:533-538.
21. Dade S, Callebaut I, Paillisson A, Bontoux M, Dalbies-Tran R, Monget P: In silico identification and structural features of six new genes similar to MATER specifically expressed in the oocyte. Biochem Biophys Res Commun 2004, 324:547-553.
22. Paillisson A, Dade S, Callebaut I, Bontoux M, Dalbies-Tran R, Vaiman D, Monget P: Identification, characterization and metagenome analysis of oocyte-specific genes organized in clusters in the mouse genome. BMC Genomics 2005, 6:76.
23. Swanson WJ, Vacquier VD: The rapid evolution of reproductive proteins. Nat Rev Genet 2002, 3:137-144.
24. Bebbere D, Bogliolo L, Ariu F, Fois S, Leoni GG, Tore S, Succu S, Berlinguer F, Naitana S, Ledda S: Expression pattern of zygote arrest 1(ZAR1), maternal antigen that embryo requires (MATER), growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) genes in ovine oocytes and in vitro-produced preimplantation embryos. Reprod Fertil Dev 2008, 20:908-915.
25. Pisani LF, Ramelli P, Lazzari B, Braglia S, Ceciliani F, Mariani P: Characterization of maternal antigen that embryos require (MATER/NLRP5) gene and protein in pig somatic tissues and germ cells. J Reprod Dev 2010, 56:41-48.
26. Zhang P, Dixon M, Zucchelli M, Hambiliki F, Levkov L, Hovatta O, Kere J: Expression analysis of the NLRP gene family suggests a role in human preimplantation development. PLoS One 2008, 3:e2755.
27. Pierre A, Gautier M, Callebaut I, Bontoux M, Jeanpierre E, Pontarotti P, Monget P: Atypical structure and phylogenomic evolution of the new eutherian oocyte- and embryo-expressed KHDC1/DPPA5/ECAT1/OOEP gene family. Genomics 2007, 90:583-594.
28. Tervit HR, Whittingham DG, Rowson LE: Successful culture in vitro of sheep and cattle ova. J Reprod Fertil 1972, 30:493-497.
29. Walker SK, Hill JL, Kleemann DO, Nancarrow CD: Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations. Biol Reprod 1996, 55:703-708.
30. Bogliolo L, Ariu F, Leoni G, Uccheddu S, Bebbere D: High hydrostatic pressure treatment improves the quality of in vitro-produced ovine blastocysts. Reprod Fertil Dev 2011, 23:809-817.
31. Evsikov AV, Marín De Evsikova C: Gene expression during the oocyte-toembryo transition in mammals. Mol Reprod Dev 2009, 76:805-818.
32. Su YQ, Sugiura K, Woo Y, Wigglesworth K, Kamdar S, Affourtit J, Eppig JJ: Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev Biol 2007, 302:104-117.
33. Ohsugi M, Zheng P, Baibakov B, Li L, Dean J: Maternally derived FILIA-MATER complex localizes asymmetrically in cleavage-stage mouse embryos. Development 2008, 135:259-269.
34. Armstrong DT, Holm P, Irvine B, Petersen BA, Stubbings RB, McLean D, Stevens G, Seamark RF: Pregnancies and live birth from in vitro fertilization of calf oocytes collected by laparoscopic follicular aspiration. Theriogenology 1992, 38:667-678.
35. Armstrong DT, Kotaras PJ, Earl CR: Advances in production of embryos in vitro from juvenile and prepubertal oocytes from the calf and lamb. Reprod Fertil Dev 1997, 9:333-339.
36. Ledda S, Bogliolo L, Leoni G, Naitana S: Production and lambing rate of blastocysts derived from in vitro matured oocytes after gonadotrophin treatment of prepubertal ewes. J Anim Sci 1999, 77:2234-2239.
37. Eppig JJ: Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod Fertil Dev 1996, 8:485-489.
38. Leoni GG, Bebbere D, Succu S, Berlinguer F, Mossa F, Galioto M, Bogliolo L, Ledda S, Naitana S: Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol Reprod Dev 2007, 74:249-257.
39. Walser CB, Lipshitz HD: Transcript clearance during the maternal-tozygotic transition. Curr Opin Genet Dev 2011, 21:431-443.
40. Magen A, Ast G: The importance of being divisible by three in alternative splicing. Nucleic Acids Res 2005, 33:5574-5582.
41. Maquat LE: Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 2004, 5:89-99.
42. Lewis BP, Green RE, Brenner SE: Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci U S A 2003, 100:189-192.
43. Lareau LF, Green RE, Bhatnagar RS, Brenner SE: The evolving roles of alternative splicing. Curr Opin Struct Biol 2004, 14:273-282.
44. Hillman RT, Green RE, Brenner SE: An unappreciated role for RNA surveillance. Genome Biol 2004, 5:R8.
45. Wang J, Xu M, Zhu K, Li L, Liu X: The N-terminus of FILIA forms an atypical KH domain with a unique extension involved in interaction with RNA. PLoS One 2012, 7:e30209.
46. Van Den Veyver IB, Al-Hussaini TK: Biparental hydatidiform moles: a maternal effect mutation affecting imprinting in the offspring. Hum Reprod Update 2006, 12:233-242.
47. Parry DA, Logan CV, Hayward BE, Shires M, Landolsi H, Diggle C, Carr I, Rittore C, Touitou I, Philibert L, Fisher RA, Fallahian M, Huntriss JD, Picton HM, Malik S, Taylor GR, Johnson CA, Bonthron DT, Sheridan EG: Mutations causing familial biparental hydatidiform mole implicate C6orf221 as a possible regulator of genomic imprinting in the human oocyte. Am J Hum Genet 2011, 89:451-458.
48. Fallahian M, Sebire NJ, Savage PM, Seckl MJ, Fisher RA: Mutations in NLRP7 and KHDC3L confer a complete hydatidiform mole phenotype on digynic triploid conceptions. Hum Mutat 2013, 34:301-308.
49. Reddy R, Akoury E, Phuong Nguyen NM, Abdul-Rahman OA, Dery C, Gupta N, Daley WP, Ao A, Landolsi H, Ann Fisher R, Touitou I, Slim R: Report of four new patients with protein-truncating mutations in C6orf221/KHDC3L and colocalization with NLRP7. Eur J Hum Genet 2013, 21:957-964.
50. Andreasen L, Bolund L, Niemann I, Hansen ES, Sunde L: Mosaic moles and non-familial biparental moles are not caused by mutations in NLRP7, NLRP2 or C6orf221. Mol Hum Reprod 2012, 18:593-598.
51. Manokhina I, Hanna CW, Stephenson MD, McFadden DE, Robinson WP: Maternal NLRP7 and C6orf221 variants are not a common risk factor for androgenetic moles, triploidy and recurrent miscarriage. Mol Hum Reprod 2013, 19:539-544.
52. Pennetier S, Uzbekova S, Perreau C, Papillier P, Mermillod P, Dalbiès-Tran R: Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes, and preimplantation embryos. Biol Reprod 2004, 71:1359-1366.
53. Leader B, Lim H, Carabatsos MJ, Harrington A, Ecsedy J, Pellman D, Maas R, Leder P: Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 2002, 4:921-928.
54. Leader B, Leder P: Formin-2, a novel formin homology protein of the cappuccino subfamily, is highly expressed in the developing and adult central nervous system. Mech Dev 2000, 93:221-231.