cDNA microarray analysis of bovine embryo gene expression profiles during the pre-implantation period

Reproductive Biology and Endocrinology - Tập 2 - Trang 1-16 - 2004
Koichi Ushizawa1, Chandana B Herath1, Kanako Kaneyama1, Satoshi Shiojima2, Akira Hirasawa2, Toru Takahashi1, Kei Imai1,3, Kazuhiko Ochiai4, Tomoyuki Tokunaga5, Yukio Tsunoda6, Gozoh Tsujimoto2, Kazuyoshi Hashizume1,4
1Reproductive Biology and Technology Laboratory,, Developmental Biology Department, National Institute of Agrobiological Sciences, Tsukuba, Japan
2Department of Genomic Drug Discovery Science, Graduate School of Pharmaceutical Sciences, Kyoto University, Sakyo-ku, Japan
3Department of Technology,, National Livestock Breeding Center, Odakura, Japan
4Department of Veterinary Medicine,, Faculty of Agriculture, Iwate University, Ueda, Japan
5Development and Differentiation Laboratory,, Developmental Biology Department, National Institute of Agrobiological Sciences,, Tsukuba, Japan
6Laboratory of Animal Reproduction,, College of Agriculture, Kinki University, Nakamachi, Japan

Tóm tắt

After fertilization, embryo development involves differentiation, as well as development of the fetal body and extra-embryonic tissues until the moment of implantation. During this period various cellular and molecular changes take place with a genetic origin, e.g. the elongation of embryonic tissues, cell-cell contact between the mother and the embryo and placentation. To identify genetic profiles and search for new candidate molecules involved during this period, embryonic gene expression was analyzed with a custom designed utero-placental complementary DNA (cDNA) microarray. Bovine embryos on days 7, 14 and 21, extra-embryonic membranes on day 28 and fetuses on days 28 were collected to represent early embryo, elongating embryo, pre-implantation embryo, post-implantation extra-embryonic membrane and fetus, respectively. Gene expression at these different time points was analyzed using our cDNA microarray. Two clustering algorithms such as k-means and hierarchical clustering methods identified the expression patterns of differentially expressed genes across pre-implantation period. Novel candidate genes were confirmed by real-time RT-PCR. In total, 1,773 individual genes were analyzed by complete k-means clustering. Comparison of day 7 and day 14 revealed most genes increased during this period, and a small number of genes exhibiting altered expression decreased as gestation progressed. Clustering analysis demonstrated that trophoblast-cell-specific molecules such as placental lactogens (PLs), prolactin-related proteins (PRPs), interferon-tau, and adhesion molecules apparently all play pivotal roles in the preparation needed for implantation, since their expression was remarkably enhanced during the pre-implantation period. The hierarchical clustering analysis and RT-PCR data revealed new functional roles for certain known genes (dickkopf-1, NPM, etc) as well as novel candidate genes (AW464053, AW465434, AW462349, AW485575) related to already established trophoblast-specific genes such as PLs and PRPs. A large number of genes in extra-embryonic membrane increased up to implantation and these profiles provide information fundamental to an understanding of extra-embryonic membrane differentiation and development. Genes in significant expression suggest novel molecules in trophoblast differentiation.

Tài liệu tham khảo

Stanton JA, Macgregor AB, Green DP: Gene expression in the mouse preimplantation embryo. Reproduction. 2003, 125: 457-468. 10.1530/rep.0.1250457. King GJ, Atkinson BA, Robertson HA: Development of the bovine placentome from days 20 to 29 of gestation. J Reprod Fertil. 1980, 59: 95-100. Yamada O, Todoroki J, Kizaki K, Takahashi T, Imai K, Patel OV, Schuler LA, Hashizume K: Expression of prolactin-related protein I at the fetomaternal interface during the implantation period in cows. Reproduction. 2002, 124: 427-437. 10.1530/rep.0.1240427. Wooding FBP: Current topic: The synepitheliochorial placenta of ruminants: Binucleate cell fusions and hormone production. Placenta. 1992, 13: 101-113. Wooding FBP, Flint AP: Placentation. In Marshall's Physiology of Reproduction. Edited by: Lamming GE. 1994, London: Chapman & Hall, 3: 233-460. 4 Tanaka TS, Kunath T, Kimber WL, Jaradat SA, Stagg CA, Usuda M, Yokota T, Niwa H, Rossant J, Ko MSH: Gene expression profiling of embryo-derived stem cells reveals candidate genes associated with pluripotency and lineage specificity. Genome Res. 2002, 12: 1921-1928. 10.1101/gr.670002. Lee J, Inoue K, Ono R, Ogonuki N, Kohda T, Kaneko-Ishino T, Ogura A, Ishino F: Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development. 2002, 129: 1807-1817. 10.1242/dev.00159. Bazer FW, Spencer TE, Ott TL: Interferon tau: a novel pregnancy recognition signal. Am J Reprod Immunol. 1997, 37: 412-420. Flint AP, Guesdon FM, Stewart HJ: Regulation of trophoblast interferon gene expression. Mol Cell Endocrinol. 1994, 100: 93-95. 10.1016/0303-7207(94)90285-2. Whiteside EJ, Kan M, Jackson MM, Thompson JG, McNaughton C, Herington AC, Harvey MB: Urokinase-type plasminogen activator (uPA) and matrix metalloproteinase-9 (MMP-9) expression and activity during early embryo development in the cow. Anat Embryol. 2001, 204: 477-483. 10.1007/s429-001-8004-7. Kizaki K, Nakano H, Nakano H, Takahashi T, Imai K, Hashizume K: Expression of heparanase mRNA in bovine placenta during gestation. Reproduction. 2001, 121: 573-580. 10.1530/rep.0.1210573. Mohan M, Malayer JR, Geisert RD, Morgan GL: Expression patterns of retinoid X receptors, retinaldehyde dehydrogenase, and peroxisome proliferator activated receptor gamma in bovine preattachment embryos. Biol Reprod. 2002, 66: 692-700. Hashizume K, Ishiwata H, Kizaki K, Yamada O, Takahashi T, Imai K, Patel OV, Akagi S, Shimizu M, Takahashi S, Katsuma S, Shiojima S, Hirasawa A, Tsujimoto G, Todoroki J, Izaike Y: Implantation and placental development in somatic cell clone recipient cows. Cloning Stem Cells. 2002, 4: 197-209. 10.1089/15362300260339485. Zhang S, Kubota C, Yang L, Zhang Y, Page R, O'Neill M, Yang X, Tian XC: Genomic Imprinting of H19 in Naturally Reproduced and Cloned Cattle. Biol Reprod. 2004, 71: 1540-1544. 10.1095/biolreprod.104.031807. Ishiwata H, Katsuma S, Kizaki K, Patel OV, Nakano H, Takahashi T, Imai K, Hirasawa A, Shiojima S, Ikawa H, Suzuki Y, Tsujimoto G, Izaike Y, Todoroki J, Hashizume K: Characterization of gene expression profiles in early bovine pregnancy using a custom cDNA microarray. Mol Reprod Dev. 2003, 65: 9-18. 10.1002/mrd.10292. Hartigan JA: Clustering algorithms. 1975, New York: Wiley & Sons Soukas A, Cohen P, Socci ND, Friedman JM: Leptin-specific patterns of gene expression in white adipose tissue. Genes Dev. 2000, 14: 963-980. Eisen MB, Spellman PT, Brown PO, Botstein D: Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA. 1998, 95: 14863-14868. 10.1073/pnas.95.25.14863. Giudice LC, Telles TL, Lobo S, Kao L: The molecular basis for implantation failure in endometriosis: on the road to discovery. Ann NY Acad Sci. 2002, 955: 252-264. Martin J, Dominguez F, Avila S, Castrillo JL, Remohi J, Pellicer A, Simon C: Human endometrial receptivity: gene regulation. J Reprod Immunol. 2002, 55: 131-139. 10.1016/S0165-0378(01)00140-1. Chen HW, Chen JJ, Tzeng CR, Li HN, Chang SJ, Cheng YF, Chang CW, Wang RS, Yang PC, Lee YT: Global analysis of differentially expressed genes in early gestational decidua and chorionic villi using a 9600 human cDNA microarray. Mol Hum Reprod. 2002, 8: 475-484. 10.1093/molehr/8.5.475. Aronow BJ, Richardson BD, Handwerger S: Microarray analysis of trophoblast differentiation: gene expression reprogramming in key gene function categories. Physiol Genomics. 2001, 6: 105-116. Reese J, Das SK, Paria BC, Lim H, Song H, Matsumoto H, Knudtson KL, DuBois RN, Dey SK: Global gene expression analysis to identify molecular markers of uterine receptivity and embryo implantation. J Biol Chem. 2001, 276: 44137-44145. 10.1074/jbc.M107563200. Tanaka TS, Jaradat SA, Lim MK, Kargul GJ, Wang X, Grahovac MJ, Pantano S, Sano Y, Piao Y, Nagaraja R, Doi H, Wood WH, Becker KG, Ko MSH: Genome-wide expression profiling of mid-gestation placenta and embryo using a 15,000 mouse developmental cDNA microarray. Proc Natl Acad Sci USA. 2000, 97: 9127-9132. 10.1073/pnas.97.16.9127. Salamonsen LA: Role of proteases in implantation. Rev Reprod. 1999, 4: 11-22. 10.1530/ror.0.0040011. Kizaki K, Yamada O, Nakano H, Takahashi T, Yamauchi N, Imai K, Hashizume K: Cloning and localization of heparanase in bovine placenta. Placenta. 2003, 24: 424-430. 10.1053/plac.2002.0909. Luo H, Kimura K, Aoki M, Hirako M: Vascular endothelial growth factor (VEGF) promotes the early development of bovine embryo in the presence of cumulus cells. J Vet Med Sci. 2002, 64: 967-971. 10.1292/jvms.64.967. Huppertz B, Kertschanska S, Demir AY, Frank HG, Kaufmann P: Immunohistochemistry of matrix metalloproteinases (MMP), their substrates, and their inhibitors (TIMP) during trophoblast invasion in the human placenta. Cell Tissue Res. 1998, 291: 133-148. 10.1007/s004410050987. Krussel JS, Bielfeld P, Polan ML, Simon C: Regulation of embryonic implantation. Eur J Obstet Gynecol Reprod Biol. 2003, 110 (Suppl 1): S2-9. 10.1016/S0301-2115(03)00167-2. Yang YH, Dudoit S, Callow MJ, Speed TP: Statistical method for identifying differentially expressed genes in replicated cDNA microarray experiment. Statistica Sinica. 2002, 12: 111-139. Herath CB, Shiojima S, Ishiwata H, Katsuma S, Kadowaki T, Ushizawa K, Imai K, Takahashi T, Hirasawa A, Tsujimoto G, Hashizume K: Pregnancy-associated changes in genome-wide gene expression profiles in the liver of cow throughout pregnancy. Biochem Biophys Res Commun. 2004, 313: 666-680. 10.1016/j.bbrc.2003.11.151. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J: TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003, 34: 374-378. Patel OV, Yamada O, Kizaki K, Takahashi T, Imai K, Hashizume K: Quantitative analysis throughout pregnancy of placentomal and interplacentomal expression of pregnancy-associated glycoproteins-1 and -9 in the cow. Mol Reprod Dev. 2004, 67: 257-263. 10.1002/mrd.20017. Zhao H, Hastie T, Whitfield ML, Brresen-Dale A-L, Jeffrey SS: Optimization and evaluation of T7 based RNA linear amplification protocols for cDNA microarray analysis. BMC genomics. 2002, 3: 31-45. 10.1186/1471-2164-3-31. Puskas LG, Zvara A, Hackler L, Van Hummelen P: RNA amplification results in reproducible microarray data with slight ratio bias. Biotechniques. 2002, 32: 1330-1334. Cross JC, Werb Z, Fisher SJ: Implantation and the placenta: key pieces of the development puzzle. Science. 1994, 266: 1508-1518. 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. 10.1016/S0093-691X(99)00162-4. Schultz RM, Davis W, Stein P, Svoboda P: Reprogramming of gene expression during preimplantation development. J Exp Zool. 1999, 285: 276-282. 10.1002/(SICI)1097-010X(19991015)285:3<276::AID-JEZ11>3.0.CO;2-K. Lonergan P, Rizos D, Gutierrez-Adan A, Moreira PM, Pintado B, de la Fuente J, Boland MP: Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol Reprod. 2003, 69: 1424-1431. 10.1095/biolreprod.103.018168. Vigneault C, McGraw S, Massicotte L, Sirard MA: Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition. Biol Reprod. 2004, 70: 1701-1709. 10.1095/biolreprod.103.022970. King GJ, Atkinson BA, Robertson HA: Development of the intercaruncular areas during early gestation and establishment of the bovine placenta. J Reprod Fertil. 1981, 61: 469-474. Grealy M, Diskin MG, Sreenan JM: Protein content of cattle oocytes and embryos from the two-cell to the elongated blastocyst stage at day 16. J Reprod Fertil. 1996, 107: 229-233. Farin CE, Imakawa K, Hansen TR, McDonnell JJ, Murphy CN, Farin PW, Roberts RM: Expression of trophoblastic interferon genes in sheep and cattle. Biol Reprod. 1990, 43: 210-218. Anthony RV, Liang R, Kayl EP, Pratt SL: The growth hormone/prolactin gene family in ruminant placentae. J Reprod Fertil Suppl. 1995, 49: 83-95. Kessler MA, Duello TM, Schuler LA: Expression of prolactin-related hormones in the early bovine conceptus, and potential for paracrine effect on the endometrium. Endocrinology. 1991, 129: 1885-1895. Green JA, Xie S, Quan X, Bao B, Gan X, Mathialagan N, Beckers JF, Roberts RM: Pregnancy-associated bovine and ovine glycoproteins exhibit spatially and temporally distinct expression patterns during pregnancy. Biol Reprod. 2000, 62: 1624-1631. Pushpakumara PG, Robinson RS, Demmers KJ, Mann GE, Sinclair KD, Webb R, Wathes DC: Expression of the insulin-like growth factor (IGF) system in the bovine oviduct at oestrus and during early pregnancy. Reproduction. 2002, 123: 859-868. 10.1530/rep.0.1230859. Block J, Drost M, Monson RL, Rutledge JJ, Rivera RM, Paula-Lopes FF, Ocon OM, Krininger CE, Liu J, Hansen PJ: Use of insulin-like growth factor-I during embryo culture and treatment of recipients with gonadotropin-releasing hormone to increase pregnancy rates following the transfer of in vitro-produced embryos to heat-stressed, lactating cows. J Anim Sci. 2003, 81: 1590-1602. Lescure A, Gautheret D, Carbon P, Krol A: Novel selenoproteins identified in silico and in vivo by using a conserved RNA structural motif. J Biol Chem. 1999, 274: 38147-38154. 10.1074/jbc.274.53.38147. Niemann H, Wrenzycki C: Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology. 2000, 53: 21-34. 10.1016/S0093-691X(99)00237-X. Putney DJ, Malayer JR, Gross TS, Thatcher WW, Hansen PJ, Drost M: Heat stress-induced alterations in the synthesis and secretion of proteins and prostaglandins by cultured bovine conceptuses and uterine endometrium. Biol Reprod. 1988, 39: 717-728. Voss AK, Thomas T, Gruss P: Mice lacking HSP90beta fail to develop a placental labyrinth. Development. 2000, 127: 1-11. Imakawa K, Anthony RV, Kazemi M, Marotti KR, Polites HG, Roberts RM: Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm. Nature. 1987, 330: 377-379. 10.1038/330377a0. Thatcher WW, Binelli M, Burke J, Staples CR, Ambrose JD, Coelho S: Antiluteolytic signals between the conceptus and endometrium. Theriogenology. 1997, 47: 131-140. 10.1016/S0093-691X(96)00347-0. Ealy AD, Larson SF, Liu L, Alexenko AP, Winkelman GL, Kubisch HM, Bixby JA, Roberts RM: Polymorphic forms of expressed bovine interferon-tau genes: relative transcript abundance during early placental development, promoter sequences of genes and biological activity of protein products. Endocrinology. 2001, 142: 2906-2915. 10.1210/en.142.7.2906. Roberts RM, Ezashi T, Rosenfeld CS, Ealy AD, Kubisch HM: Evolution of the interferon-tau genes and their promoters, and maternal-trophoblast interactions in control of their expression. Reprod Suppl. 2003, 61: 239-251. Li Q, Zhang M, Kumar S, Zhu LJ, Chen D, Bagchi MK, Bagchi IC: Identification and implantation stage-specific expression of an interferon-alpha-regulated gene in human and rat endometrium. Endocrinology. 2001, 142: 2390-2400. 10.1210/en.142.6.2390. Roberts RM, Imakawa K, Niwano Y, Kazemi M, Malathy PV, Hansen TR, Glass AA, Kronenberg LH: Interferon production by the preimplantation sheep embryo. J Interferon Res. 1989, 9: 175-187. Zuckermann FA, Head JR: Expression of MHC antigens on murine trophoblast and their modulation by interferon. J Immunol. 1986, 137: 846-853. Bowen JA, Bazer FW, Burghardt RC: Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vitro. Biol Reprod. 1997, 56: 409-415. Xiang W, MacLaren LA: Expression of fertilin and CD9 in bovine trophoblast and endometrium during implantation. Biol Reprod. 2002, 66: 1790-1796. Kliem A, Tetens F, Klonisch T, Grealy M, Fischer B: Epidermal growth factor receptor and ligands in elongating bovine blastocysts. Mol Reprod Dev. 1998, 51: 402-412. Matsumoto H, Daikoku T, Wang H, Sato E, Dey SK: Differential expression of ezrin/radixin/moesin (ERM) and ERM-associated adhesion molecules in the blastocyst and uterus suggests their functions during implantation. Biol Reprod. 2004, 70: 729-736. 10.1095/biolreprod.103.022764. Nakano H, Takahashi T, Imai K, Hashizume K: Expression of placental lactogen and cytokeratin in bovine placental binucleate cells in culture. Cell Tissue Res. 2001, 303: 263-270. 10.1007/s004410000316. Glinka A, Wu W, Delius H, Monaghan AP, Blumenstock C, Niehrs C: Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature. 1998, 391: 357-62. 10.1038/34848. Benz J, Hofmann A: Annexins: from structure to function. Biol Chem. 1997, 378: 177-183. Teahan CG, Totty NF, Segal AW: Isolation and characterization of grancalcin, a novel 28 kDa EF-hand calcium-binding protein from human neutrophils. Biochem J. 1992, 286 (Pt 2): 549-554. Mullins RD, Pollard TD: Structure and function of the Arp2/3 complex. Curr Opin Struct Biol. 1999, 9: 244-249. 10.1016/S0959-440X(99)80034-7. Won KA, Schumacher RJ, Farr GW, Horwich AL, Reed SI: Maturation of human cyclin E requires the function of eukaryotic chaperonin CCT. Mol Cell Biol. 1998, 18: 7584-7589. Chan PK, Chan FY, Morris SW, Xie Z: Isolation and characterization of the human nucleophosmin/B23 (NPM) gene: identification of the YY1 binding site at the 5' enhancer region. Nucleic Acids Res. 1997, 25: 1225-1232. 10.1093/nar/25.6.1225. Zani VJ, Asou N, Jadayel D, Heward JM, Shipley J, Nacheva E, Takasuki K, Catovsky D, Dyer MJ: Molecular cloning of complex chromosomal translocation t(8;14;12)(q24.1;q32.3;q24.1) in a Burkitt lymphoma cell line defines a new gene (BCL7A) with homology to caldesmon. Blood. 1996, 87: 3124-3134. Kurella M, Hsiao L-L, Yoshida T, Randall JD, Chow G, Sarang SS, Jensen R, Gullans SR: DNA microarray analysis of complex biological Processes. J Am Soc Nephrol. 2001, 12: 1072-1078. Smith TPL, Grosse WM, Freking BA, Roberts AJ, Stone RT, Casas E, Wray JE, White J, Cho J, Fahrenkrug SC, Bennett GL, Heaton MP, Laegreid WW, Rohrer GA, Chitko-McKown CG, Pertea G, Holt I, Karamycheva S, Liang F, Quackenbush J, Keele JW: Sequence evaluation of four pooled-tissue normalized bovine cDNA libraries and construction of a gene index for cattle. Genome Res. 2001, 11: 626-630. 10.1101/gr.170101.