Breast-cancer anti-estrogen resistance 4 (BCAR4) encodes a novel maternal-effect protein in bovine and is expressed in the oocyte of humans and other non-rodent mammals

Human Reproduction

Volumn 28, Issue 2, 2013, Pages 430-441

  Angulo, L ^a,b,c,d,e   Perreau, C ^a,b,c,d   Lakhdari, N ^a,b,c,d   Uzbekov, R ^c   Papillier, P ^a,b,c,d   Freret, S ^a,b,c,d   Cadoret, V ^a,b,c,d,f   Guyader Joly, C ^e   Royere, D ^a,b,c,d,f   Ponsart, C ^e   Uzbekova, S ^a,b,c,d   Dalbies Tran, R ^a,b,c,d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d IFCE   (France)

^e Union Nationale des Coopératives d'Elevage et d'Insémination Animale   (France)

^f UNIVERSITY HOSPITAL OF TOURS   (France)

Author keywords

animal model; embryo development; gene expression; oocyte quality

Indexed keywords

BREAST CANCER ANTIESTROGEN RESISTANCE 4 PROTEIN; MEMBRANE PROTEIN; PHOSPHOPROTEIN; RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; COW; ELECTRON MICROSCOPY; EMBRYO DEVELOPMENT; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN VIVO STUDY; NONHUMAN; OOCYTE; OVARIECTOMY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 84872525272     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/des412     Document Type: Article

References (58)

1. 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 USA 2007;104: 17602-17607.
2. Braude P, Bolton V, Moore S. Human gene expression first occurs between the four-and eight-cell stages of preimplantation development. Nature 1988;332: 459-461.
3. Brinsko SP, Ball BA, Ignotz GG, Thomas PG, Currie WB, Ellington JE. Initiation of transcription and nucleologenesis in equine embryos. Mol Reprod Dev 1995;42: 298-302.
4. Brown N, Deb K, Paria BC, Das SK, Reese J. Embryo-uterine interactions via the neuregulin family of growth factors during implantation in the mouse. Biol Reprod 2004;71: 2003-2011.
5. Brunet-Simon A, Henrion G, Renard JP, Duranthon V. Onset of zygotic transcription and maternal transcript legacy in the rabbit embryo. Mol Reprod Dev 2001;58: 127-136.
6. Burns KH, Viveiros MM, Ren Y, Wang P, DeMayo FJ, Frail DE, Eppig JJ, Matzuk MM. Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 2003;300: 633-636.
7. Bysted BV, Dieleman SJ, Hyttel P, Greve T. Embryonic developmental stages in relation to the LH peak in dogs. J Reprod Fertil Suppl 2001; 57: 181-186.
8. Camous S, Kopecny V, Flechon JE. Autoradiographic detection of the earliest stage of [3H]-uridine incorporation into the cow embryo. Biol Cell 1986;58: 195-200.
9. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000;17: 540-552.
10. Davidson G. The cell cycle and Wnt. Cell Cycle 2010;9: 1667-1668.
11. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008; 36: W465-W469.
12. De Vries WN, Evsikov AV, Haac BE, Fancher KS, Holbrook AE, Kemler R, Solter D, Knowles BB. Maternal beta-catenin and E-cadherin in mouse development. Development 2004;131: 4435-4445.
13. Donnay I, Faerge I, Grondahl C, Verhaeghe B, Sayoud H, Ponderato N, Galli C, Lazzari G. Effect of prematuration, meiosis activating sterol and enriched maturation medium on the nuclear maturation and competence to development of calf oocytes. Theriogenology 2004; 62: 1093-1107.
14. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32: 1792-1797.
15. Godinho MF, Sieuwerts AM, Look MP, Meijer D, Foekens JA, Dorssers LC, van Agthoven T. Relevance of BCAR4 in tamoxifen resistance and tumour aggressiveness of human breast cancer. Br J Cancer 2010;103: 1284-1291.
16. Godinho M, Meijer D, Setyono-Han B, Dorssers LC, van Agthoven T. Characterization of BCAR4, a novel oncogene causing endocrine resistance in human breast cancer cells. J Cell Physiol 2011; 226: 1741-1749.
17. Gustofson RL, Tong Z, Larsen FW, Nelson LM. Women who meet the clinical characteristics of a maternal effect gene defect have a higher incidence of unexplained infertility. Fertil Steril 2005;4: S140-S141.
18. Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 2004;6: 117-131.
19. Holm P, Booth PJ, Schmidt MH, Greve T, Callesen H. High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 1999;52: 683-700.
20. Jiang GJ, Wang K, Miao DQ, Guo L, Hou Y, Schatten H, Sun QY. Protein profile changes during porcine oocyte aging and effects of caffeine on protein expression patterns. PLoS One 2011;6: e28996.
21. Kall L, Krogh A, Sonnhammer EL. Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucleic Acids Res 2007;35: W429-W432.
22. Kocabas AM, Crosby J, Ross PJ, Otu HH, Beyhan Z, Can H, Tam WL, Rosa GJ, Halgren RG, Lim B et al. The transcriptome of human oocytes. Proc Natl Acad Sci USA 2006;103: 14027-14032.
23. Krisher RL. Utility of animal models for human embryo culture development: domestic species. Methods Mol Biol 2012;912: 27-37.
24. Krupinski P, Chickarmane V, Peterson C. Simulating the mammalian blastocyst-molecular and mechanical interactions pattern the embryo. PLoS Comput Biol 2011;7: e1001128.
25. la Cour T, Kiemer L, Molgaard A, Gupta R, Skriver K, Brunak S. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel 2004;17: 527-536.
26. 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.
27. Letunic I, Doerks T, Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 2012;40: D302-D305.
28. Li L, Zheng P, Dean J. Maternal control of early mouse development. Development 2010;137: 859-870.
29. Lingenfelter BM, Tripurani SK, Tejomurtula J, Smith GW, Yao J. Molecular cloning and expression of bovine nucleoplasmin 2 (NPM2): a maternal effect gene regulated by miR-181a. Reprod Biol Endocrinol 2011;9: 40.
30. Matzuk MM, Lamb DJ. Genetic dissection of mammalian fertility pathways. Nat Cell Biol 2002;4(Suppl): s41-s49.
31. Meijer D, van Agthoven T, Bosma PT, Nooter K, Dorssers LC. Functional screen for genes responsible for tamoxifen resistance in human breast cancer cells. Mol Cancer Res 2006;4: 379-386.
32. Menezo YJ, Herubel F. Mouse and bovine models for human IVF. Reprod Biomed Online 2002;4: 170-175.
33. Minami N, Aizawa A, Ihara R, Miyamoto M, Ohashi A, Imai H. Oogenesin is a novel mouse protein expressed in oocytes and early cleavage-stage embryos. Biol Reprod 2003;69: 1736-1742.
34. Murai S, Stein P, Buffone MG, Yamashita S, Schultz RM. Recruitment of Orc6l, a dormant maternal mRNA in mouse oocytes, is essential for DNA replication in 1-cell embryos. Dev Biol 2010;341: 205-212.
35. Nganvongpanit K, Muller H, Rings F, Gilles M, Jennen D, Holker M, Tholen E, Schellander K, Tesfaye D. Targeted suppression of E-cadherin gene expression in bovine preimplantation embryo by RNA interference technology using double-stranded RNA. Mol Reprod Dev 2006;73: 153-163.
36. Ohsugi M, Hwang SY, Butz S, Knowles BB, Solter D, Kemler R. Expression and cell membrane localization of catenins during mouse preimplantation development. Dev Dyn 1996;206: 391-402.
37. Paronetto MP, Bianchi E, Geremia R, Sette C. Dynamic expression of the RNA-binding protein Sam68 during mouse pre-implantation development. Gene Expr Patterns 2008;8: 311-322.
38. Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, Zahn D, Colledge WH, Carlton MB, Nakano T, Surani MA. Stella is a maternal effect gene required for normal early development in mice. Curr Biol 2003;13: 2110-2117.
39. Pennetier S, Uzbekova S, Guyader-Joly C, Humblot P, Mermillod P, Dalbies-Tran R. Genes preferentially expressed in bovine oocytes revealed by subtractive and suppressive hybridization. Biol Reprod 2005;73: 713-720.
40. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011;8: 785-786.
41. Potireddy S, Vassena R, Patel BG, Latham KE. Analysis of polysomal mRNA populations of mouse oocytes and zygotes: dynamic changes in maternal mRNA utilization and function. Dev Biol 2006;298: 155-166.
42. Ryley DA, Wu HH, Leader B, Zimon A, Reindollar RH, Gray MR. Characterization and mutation analysis of the human formin-2 (FMN2) gene inwomenwith unexplained infertility. Fertil Steril 2005;83: 1363-1371.
43. Sheth B, Nowak RL, Anderson R, Kwong WY, Papenbrock T, Fleming TP. Tight junction protein ZO-2 expression and relative function of ZO-1 and ZO-2 during mouse blastocyst formation. Exp Cell Res 2008; 314: 3356-3368.
44. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 2004;101: 6062-6067.
45. 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.
46. Telford NA, Watson AJ, Schultz GA. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 1990;26: 90-100.
47. Thelie A, Papillier P, Pennetier S, Perreau C, Traverso JM, Uzbekova S, Mermillod P, Joly C, Humblot P, Dalbies-Tran R. Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev Biol 2007;7: 125.
48. 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 2000a;26: 267-268.
49. Tong ZB, Nelson LM, Dean J. Mater encodes a maternal protein in mice with a leucine-rich repeat domain homologous to porcine ribonuclease inhibitor. Mamm Genome 2000b;11: 281-287.
50. van Agthoven T, Godinho MF, Wulfkuhle JD, Petricoin EF III, Dorssers LC. Protein pathway activation mapping reveals molecular networks associated with antiestrogen resistance in breast cancer cell lines. Int J Cancer 2012;131: 1998-2007.
51. Vestweber D, Gossler A, Boller K, Kemler R. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev Biol 1987;124: 451-456.
52. Vigneron C, Nuttinck F, Perreau C, Reinaud P, Charpigny G, Mermillod P. Effect of roscovitine, a cdk1 inhibitor, and of the presence of oocyte on bovine cumulus cell expansion and cyclooxygenase-2 expression. Mol Reprod Dev 2003;65: 114-121.
53. Wang H, Zhao JX, Hu N, Ren J, Du M, Zhu MJ. Side-stream smoking reduces intestinal inflammation and increases expression of tight junction proteins. World J Gastroenterol 2011;18: 2180-2187.
54. 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.
55. Yoshida Y, Miyamura M, Hamano S, Yoshida M. Expression of growth factor ligand and their receptor mRNAs in bovine ova during in vitro maturation and after fertilization in vitro. J Vet Med Sci 1998; 60: 549-554.
56. Zeng F, Baldwin DA, Schultz RM. Transcript profiling during preimplantation mouse development. Dev Biol 2004;272: 483-496.
57. Zernicka-Goetz M. Activation of embryonic genes during preimplantation rat development. Mol Reprod Dev 1994;38: 30-35.
58. Zheng LP, Huang J, Zhang DL, Xu LQ, Li F, Wu L, Liu ZY, Zheng YH. c-erbB2 and c-myb induce mouse oocyte maturation involving activation of maturation promoting factor. DNA Cell Biol 2012; 31: 164-170.