Journal of Embryo Transfer (한국수정란이식학회지)

The Korean Society of Embryo Transfer (한국수정란이식학회)
권호 표지

Comparative Analysis of Gene Expression in the Female Reproductive Organs

  • Kim, Min-Goo (Department of Biological Science and Technology, and Institute of Biomaterials, Yonsei University) ;
  • Seo, Hee-Won (Department of Biological Science and Technology, and Institute of Biomaterials, Yonsei University) ;
  • Choi, Yo-Han (Department of Biological Science and Technology, and Institute of Biomaterials, Yonsei University) ;
  • Lee, Chang-Kyu (Department of Agricultural Biotechnology, Animal Biotechnology Major, and Research Institute for Agriculture and Life Sciences, Seoul National University) ;
  • Ka, Hak-Hyun (Department of Biological Science and Technology, and Institute of Biomaterials, Yonsei University)
  • Published : 2009.06.30
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Abstract

To understand molecular and cellular mechanisms of many gene products in the female reproductive organs including the ovary and uterine endometrium as well as during embryo development, researchers have developed and utilized many effective methodologies to analyze gene expression in cells, tissues and animals over the last several decades. For example, blotting techniques have helped to understand molecular functions at DNA, RNA and protein levels, and the reverse transcription-polymerase chain reaction (RT-PCR) method has been widely used in gene expression analysis. However, some conventional methods are not sufficient to understand regulation and function of genes expressed in very complex patterns in many organs. Thus, it is required to adopt more high-throughput and reliable techniques. Here, we describe several techniques used widely recently to analyze gene expression, including annealing control based-PCR, differential display-PCR, expressed sequence tag, suppression subtractive hybridization and microarray techniques. Use of these techniques will help to analyze expression pattern of many genes from small scale to large scale and to compare expression patterns of genes in one sample to another. In this review, we described principles of these methodologies and summarized examples of comparative analysis of gene expression in female reproductive organs with help of those methodologies.

Keywords

References

  1. Adams MD, Kelley JM, Gocayne JD, Dubnick M, Polymeropoulos MH, Xiao H, Merril CR, Wu A, Olde B and Moreno RF, et al. 1991. Complementary DNA sequencing: expressed sequence tags and human genome project. Science 252:1651-1656 https://doi.org/10.1126/science.2047873
  2. Agca C, Ries JE, Kolath SJ, Kim JH, Forrester LJ, Antoniou E, Whitworth KM, Mathialagan N, Springer GK, Prather RS and Lucy MC. 2006. Luteinization of porcine preovulatory follicles leads to systematic changes in follicular gene expression. Reproduction 132:133-145 https://doi.org/10.1530/rep.1.01163
  3. Alwine JC, Kemp DJ and Stark GR. 1977. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc. Natl. Acad. Sci. USA 74:5350-5354 https://doi.org/10.1073/pnas.74.12.5350
  4. Assidi M, Dufort I, Ali A, Hamel M, Algriany O, Dielemann S and Sirard MA. 2008. Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol, Reprod. 79:209-222 https://doi.org/10.1095/biolreprod.108.067686
  5. Berk AJ and Sharp PA. 1977. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell 12:721-732 https://doi.org/10.1016/0092-8674(77)90272-0
  6. Bertioli DJ, Schlichter UH, Adams MJ, Burrows PR, Steinbiss HH and Antoniw JF. 1995. An analysis of differential display shows a strong bias towards high copy number mRNAs. Nucleic Acids Res. 23:4520-4523 https://doi.org/10.1093/nar/23.21.4520
  7. Blomberg LA, Long EL, Sonstegard TS, Van Tassell CP, Dobrinsky JR and Zuelke KA. 2005. Serial analysis of gene expression during elongation of the peri-implantation porcine trophectoderm (conceptus). Physiol. Genomics 20: 188-194 https://doi.org/10.1152/physiolgenomics.00157.2004
  8. Brar AK, Handwerger S, Kessler CA and Aronow BJ. 2001. Gene induction and categorical reprogramming during in vitro human endometrial fibroblast decidualization. Physiol. Genomics 7:135-148 https://doi.org/10.1152/physiolgenomics.00061.2001
  9. Caetano AR, Johnson RK, Ford JJ and Pomp D. 2004. Micro-array profiling for differential gene expression in ovaries and ovarian follicles of pigs selected for increased ovulation rate. Genetics 168:1529-1537 https://doi.org/10.1534/genetics.104.029595
  10. Chang HS, Cheng WT, Wu HK and Choo KB. 2000. Identification of genes expressed in the epithelium of porcine oviduct containing early embryos at various stages of development. Mol. Reprod. Dev. 56:331-335 https://doi.org/10.1002/1098-2795(200007)56:3<331::AID-MRD1>3.0.CO;2-K
  11. Chee M, Yang R, Hubbell E, Berno A, Huang XC, Stern D, Winkler J, Lockhart DJ, Morris MS and Fodor SP. 1996. Accessing genetic information with high-density DNA arrays. Science 274:610-614 https://doi.org/10.1126/science.274.5287.610
  12. Chen Y, Ni H, Ma XH, Hu SJ, Luan LM, Ren G, Zhao YC, Li SJ, Diao HL, Xu X, Zhao ZA and Yang ZM. 2006. Global analysis of differential luminal epithelial gene expression at mouse implantation sites. J. Mol. Endocrinol. 37:147-161 https://doi.org/10.1677/jme.1.02009
  13. Davoli R, Fontanesi L, Zambonelli P, Bigi D, Gellin J, Yerle M, Milc J, Braglia S, Cenci V, Cagnazzo M and Russo V. 2002. Isolation of porcine expressed sequencetags for the construction of a first genomic transcript map of the skeletal muscle in pig. Anim. Genet. 33:3-18 https://doi.org/10.1046/j.1365-2052.2002.00800.x
  14. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED and Siebert PD. 1996. Suppression subtractive hybridization:A method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. USA 93:6025-6030 https://doi.org/10.1073/pnas.93.12.6025
  15. Gielen SC, Santegoets LA, Kuhne LC, Van Ijcken WF, Boers-Sijmons B, Hanifi-Moghaddam P, Helmerhorst TJ, Blok LJ and Burger CW. 2007. Genomic and nongenomic effects of estrogen signaling in human endometrial cells: involvement of the growth factor receptor signaling downstream AKT pathway. Reprod. Sci. 14:646-654 https://doi.org/10.1177/1933719107306872
  16. Gilliland G, Perrin S, Blanchard K and Bunn HF. 1990. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction. Proc. Natl. Acad. Sci. USA 87:2725-2729 https://doi.org/10.1073/pnas.87.7.2725
  17. Gladney CD, Bertani GR, Johnson RK and Pomp D. 2004. Evaluation of geneexpression in pigs selected for enhanced reproduction using differential display PCR and human microarrays: I. Ovarian follicles. J. Anim. Sci. 82:17-31 https://doi.org/10.2527/2004.82117x
  18. Graf D, Fisher AG and Merkenschlager M. 1997. Rational primer design greatly improves differential display-PCR (DDPCR). Nucleic Acids Res. 25:2239-2240 https://doi.org/10.1093/nar/25.11.2239
  19. Green JA, Kim JG, Whitworth KM, Agca C and Prather RS. 2006. The use of microarrays to define functionally-related genes that are differentially expressed in the cycling pig uterus. Soc. Reprod. Fertil. Suppl. 62:163-176
  20. Green ML, Blaeser LL, Simmen FA and Simmen RC. 1996. Molecular cloning of spermidine/spermine N1-acetyltransferase from the periimplantation porcine uterus by messenger ribonucleic acid differential display: temporal and conceptus-modulated gene expression. Endocrinology 137: 5447-5455 https://doi.org/10.1210/en.137.12.5447
  21. Ha Y, Tsukada A, Saito N, Zadworny D and Shimada K. 2008. Identification of differentially expressed genes involved in the regression and development of the chicken Mullerian duct. Int. J. Dev. Biol. 52:1135-1141 https://doi.org/10.1387/ijdb.072441yh
  22. Hara E, Kato T, Nakada S, Sekiya S and Oda K. 1991. Subtractive cDNA cloning using oligo(dT)30-latex and PCR:isolation of cDNA clones specific to undifferentiated human embryonal carcinoma cells. Nucleic Acids Res. 19:7097-7104 https://doi.org/10.1093/nar/19.25.7097
  23. Hayes BJ, Nilsen K, Berg PR, Grindflek E and Lien S. 2007. SNP detection exploiting multiple sources of redundancy in large EST collections improves validation rates. Bioinformatics 23:1692-1693 https://doi.org/10.1093/bioinformatics/btm154
  24. Hedrick SM, Cohen DI, Nielsen EA and Davis MM. 1984. Isolation of cDNA clones encoding T cell-specific membrane-associated proteins. Nature 308:149-153 https://doi.org/10.1038/308149a0
  25. Heid CA, Stevens J, Livak KJ and Williams PM. 1996. Real time quantitative PCR. Genome. Res. 6:986-994 https://doi.org/10.1101/gr.6.10.986
  26. Holland PM, Abramson RD, Watson R and Gelfand DH. 1991. Detection of specific polymerase chain reaction product by utilizing the 5'----3' exonuclease activity of Thermus aquaticus DNA polymerase. Proc. Natl. Acad. Sci. USA 88:7276-7280 https://doi.org/10.1073/pnas.88.16.7276
  27. Hwang IT, Kim YJ, Kim SH, Kwak CI, Gu YY and Chun JY. 2003. Annealing control primer system for improving specificity of PCR amplification. Biotechniques. 35:1180-1184
  28. Hwang KC, Cui XS, Park SP, Shin MR, Park SY, Kim EY and Kim NH. 2004. Identification of differentially regulated genes in bovine blastocysts using an annealing control primer system. Mol. Reprod. Dev. 69:43-51 https://doi.org/10.1002/mrd.20156
  29. Jones MH, Davey PM, Aplin H and Affara NA. 1995. Expression analysis, genomic structure and mapping to 7q31 of the human sperm adhesion molecule gene SPAM1. Genomics 29:796-800 https://doi.org/10.1006/geno.1995.9931
  30. Ka H, Seo H, Kim M, Choi Y and Lee CK. 2009. Identification of differentially expressed genes in the uterine endometrium on day 12 of the estrous cycle and pregnancy in pigs. Mol. Reprod. Dev. 76:75-84 https://doi.org/10.1002/mrd.20935
  31. Ka H, Seo H, Kim M, Moon S, Kim H and Lee CK. 2008. Gene expression profiling of the uterus with embryos cloned by somatic cell nuclear transfer on day 30 of pregnancy. Anim. Reprod. Sci. 108:79-91 https://doi.org/10.1016/j.anireprosci.2007.07.008
  32. Kao LC, Tulac S, Lobo S, Imani B, Yang JP, Germeyer A, Osteen K, Taylor RN, Lessey BA and Giudice LC. 2002. Global gene profiling in human endometrium during the window of implantation. Endocrinology 143:2119-2138 https://doi.org/10.1210/en.143.6.2119
  33. Kim S, Choi Y, Bazer FW and Spencer TE. 2003. Identification of genes in the ovine endometrium regulated by interferon tau independent of signal transducer and activator of transcription 1. Endocrinology 144:5203-5214 https://doi.org/10.1210/en.2003-0665
  34. Kozian DH and Augustin HG. 1995. Rapid identification of differentially expressed endothelial cell genes by RNA display. Biochem. Biophys. Res. Commun. 209:1068-1075 https://doi.org/10.1006/bbrc.1995.1606
  35. Kulesh DA, Clive DR, Zarlenga DS and Greene JJ. 1987. Identification of interferon-modulated proliferation-related cDNA sequences. Proc. Natl. Acad. Sci. USA 84:8453-8457 https://doi.org/10.1073/pnas.84.23.8453
  36. Kumar S, Li Q, Dua A, Ying YK, Bagchi MK and Bagchi IC. 2001. Messenger ribonucleic acid encoding interferon-inducible guanylate binding protein 1 is induced in human endometrium within the putative window of implantation. J. Clin. Endocrinol. Metab. 86:2420-2427 https://doi.org/10.1210/jc.86.6.2420
  37. Lee SH, Zhao SH, Recknor JC, Nettleton D, Orley S, Kang SK, Lee BC, Hwang WS and Tuggle CK. 2005. Transcriptional profiling using a novel cDNA array identifies differential gene expression during porcine embryo elongation. Mol. Reprod. Dev. 71:129-139 https://doi.org/10.1002/mrd.20291
  38. Liang P and Pardee AB. 1995. Recent advances in differential display. Curr. Opin. Immunol. 7:274-280 https://doi.org/10.1016/0952-7915(95)80015-8
  39. Liang P and Pardee AB. 1992. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967-971 https://doi.org/10.1126/science.1354393
  40. Lievens S, Goormachtig S and Holsters M. 2001. A critical evaluation of differential display as a tool to identify genes involved in legume nodulation: looking back and looking forward. Nucleic Acids Res. 29:3459-3468 https://doi.org/10.1093/nar/29.17.3459
  41. Livak KJ and Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods. 25:402-408 https://doi.org/10.1006/meth.2001.1262
  42. Lobo SC, Huang ST, Germeyer A, Dosiou C, Vo KC, Tulac S, Nayak NR and Giudice LC. 2004. The immune environment in human endometrium during the window of implantation. Am. J. Reprod. Immunol. 52:244-251 https://doi.org/10.1111/j.1600-0897.2004.00217.x
  43. Ma XH, Hu SJ, Ni H, Zhao YC, Tian Z, Liu JL, Ren G, Liang XH, Yu H, Wan P and Yang ZM. 2006. Serial analysis of gene expression in mouse uterus at the implantation site. J. Biol, Chem. 281:9351-9360 https://doi.org/10.1074/jbc.M511512200
  44. Mahadeva H, Starkey MP, Sheikh FN, Mundy CR and Samani NJ. 1998. A simple and efficient method for the isolation of differentially expressed genes. J. Mol. Biol. 284:1391-1398 https://doi.org/10.1006/jmbi.1998.2292
  45. Maniatis T, Efstratiadis A, Sim GK and Kafatos F. 1978. Amplification and characterization of eukaryotic structural genes. Natl. Cancer. Inst. Monogr. 48:9-10
  46. Mihm M, Baker PJ, Ireland JL, Smith GW, Coussens PM, Evans AC and Ireland JJ. 2006. Molecular evidence that growth of dominant follicles involves a reduction in follicle-stimulating hormone dependence and an increase in luteinizing hormone dependence in cattle. BioI. Reprod. 74:1051-1059 https://doi.org/10.1095/biolreprod.105.045799
  47. Misirlioglu M, Page GP, Sagirkaya H, Kaya A, Parrish JJ, First NL and Memili E. 2006. Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proc. Natl. Acad. Sci. USA 103:18905-18910 https://doi.org/10.1073/pnas.0608247103
  48. Mitko K, Ulbrich SE, Wenigerkind H, Sinowatz F, Blum H, Wolf E and Bauersachs S. 2008. Dynamic changes in messenger RNA profiles of bovine endometrium during the oestrous cycle. Reproduction 135:225-240 https://doi.org/10.1530/REP-07-0415
  49. Nie GY, Li Y, Wang J, Minoura H, Findlay JK and Salamonsen LA. 2000. Complex regulation of calcium-binding protein D9k (calbindin-D(9k)) in the mouse uterus during early pregnancy and at the site of embryo implantation. BioI. Reprod. 62:27-36 https://doi.org/10.1095/biolreprod62.1.27
  50. Nobis W, Ren X, Suchyta SP, Suchyta TR, Zanella AJ and Coussens PM. 2003. Development of a porcine brain cDNA library, EST database and microarray resource. Physiol. Genomics. 16:153-159 https://doi.org/10.1152/physiolgenomics.00099.2003
  51. O'Brien JE, Peterson TJ, Tong MH, Lee EJ, Pfaff LE, Hewitt SC, Korach KS, Weiss J and Jameson JL. 2006. Estrogen-induced proliferation of uterine epithelial cells is independent of estrogen receptor alpha binding to classical estrogen response elements. J. BioI. Chem. 281:26683-26692 https://doi.org/10.1074/jbc.M601522200
  52. Okada H, Nakajima T, Yoshimura T, Yasuda K and Kanzaki H. 2003. Microarray analysis of genes controlled by progesterone in human endometrial stromal cells in vitro. Gynecol. Endocrinol. 17:271-280 https://doi.org/10.1080/713603290
  53. Popovici RM, Kao LC and Giudice LC. 2000. Discovery of new inducible genes in in vitro decidualized human endometrial stromal cells using microarray technology. Endocrinology 141:3510-3513 https://doi.org/10.1210/en.141.9.3510
  54. Punyadeera C, Dassen H, Klomp J, Dunselman G, Kamps R, Dijcks F, Ederveen A, de Goeij A and Groothuis P. 2005. Oestrogen-modulated gene expression in the human endometrium. Cell Mol. Life Sci. 62:239-250 https://doi.org/10.1007/s00018-004-4435-y
  55. Ross JW, Ashworth MD, Hurst AG, Malayer JR and Geisert RD. 2003. Analysis and characterization of differential gene expression during rapid trophoblastic elongation in the pig using suppression subtractive hybridization. Reprod. BioI. Endocrinol. 1:23 https://doi.org/10.1186/1477-7827-1-23
  56. Rossi M, Sharkey AM, Vigano P, Fiore G, Furlong R, Florio P, Ambrosini G, Smith SK and Petraglia F. 2005. Identification of genes regulated by interleukin-l beta in human endometrial stromal cells. Reproduction 130:721-729 https://doi.org/10.1530/rep.1.00688
  57. Spencer TE, Stagg AG, Joyce MM, Jenster G, Wood CG, Bazer FW, Wiley AA and Bartol FF. 1999. Discovery and characterization of endometrial epithelial messenger ribonucleic acids using the ovine uterine gland knockout model. Endocrinology 140:4070-4080 https://doi.org/10.1210/en.140.9.4070
  58. Stein J and Liang P. 2002. Differential display technology: A general guide. Cell Mol. Life Sci. 59:1235-1240 https://doi.org/10.1007/s00018-002-8501-z
  59. Stollberg J, Urschitz J, Urban Z and Boyd CD. 2000. A quantitative evaluation of SAGE. Genome Res. 10:1241-1248 https://doi.org/10.1101/gr.10.8.1241
  60. Tierney EP, Tulac S, Huang ST and Giudice LC. 2003. Activation of the protein kinase A pathway in human endometrial stromal cells reveals sequential categorical gene regulation. Physiol. Genomics. 16:47-66 https://doi.org/10.1152/physiolgenomics.00066.2003
  61. Tuggle CK, Green JA, Fitzsimmons C, Woods R, Prather RS, Malchenko S, Soares BM, Kucaba T, Crouch K, Smith C, Tack D, Robinson N, O'Leary B, Scheetz T, Casavant T, Pomp D, Edeal BJ, Zhang Y, Rothschild MF, Garwood K and Beavis W. 2003. EST-based gene discovery in pig: virtual expression patterns and comparative mapping to human. Mamm. Genome. 14:565-579 https://doi.org/10.1007/s00335-002-2263-7
  62. Tuggle CK, Wang Y and Couture O. 2007. Advances in swine transcriptomics. Int. J. BioI. Sci. 3:132-152
  63. Vallee M, Beaudry D, Roberge C, Matte JJ, Blouin R and Palin MF. 2003. Isolation of differentially expressed genes in conceptuses and endometrial tissue of sows in early gestation. BioI. Reprod. 69:1697-1706 https://doi.org/10.1095/biolreprod.103.019307
  64. Vallee M, Robert C, Methot S, Palin MF and Sirard MA. 2006. Cross-species hybridizations on a multi-species cDNA microarray to identify evolutionarily conserved genes expressed in oocytes. BMC. Genomics. 7:113 https://doi.org/10.1186/1471-2164-7-113
  65. elculescu VE, Zhang L, Vogelstein B and Kinzler KW. 1995. Serial analysis of gene expression. Science 270:484-487 https://doi.org/10.1126/science.270.5235.484
  66. Wesolowski SR, Raney NE and Ernst CW. 2004. Developmental changes in the fetal pig transcriptome. Physiol. Genomics 16:268-274 https://doi.org/10.1152/physiolgenomics.00167.2003
  67. Whitworth K, Springer GK, Forrester LJ, Spollen WG, Ries J, Lamberson WR, Bivens N, Murphy CN, Mathialagan N, Green JA and Prather RS. 2004. Developmental expression of 2489 gene clusters during pig embryogenesis: an expressed sequence tag project. BioI. Reprod. 71:1230-1243 https://doi.org/10.1095/biolreprod.104.030239
  68. Whitworth KM, Agca C, Kim JG, Patel RV, Springer GK, Bivens NJ, Forrester LJ, Mathialagan N, Green JA and Prather RS. 2005. Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos. BioI. Reprod. 72:1437-1451 https://doi.org/10.1095/biolreprod.104.037952
  69. Winer J, Jung CK, Shackel I and Williams PM. 1999. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal. Biochem. 270:41-49 https://doi.org/10.1006/abio.1999.4085
  70. Wu WX, Zhang Q, Ma XH, Unno Nand Nathanielsz PW. 1999. Suppression subtractive hybridization identified a marked increase in thrombospondin-1 associated with parturition in pregnant sheep myometrium. Endocrinology 140:2364-2371 https://doi.org/10.1210/en.140.5.2364
  71. Yao J, Coussens PM, Saama P, Suchyta S and Ernst CW. 2002. Generation of expressed sequence tags from a normalized porcine skeletal muscle eDNA library. Anim. Biotechnol. 13:211-222 https://doi.org/10.1081/ABIO-120016190
  72. Zielak AE, Canty MJ, Forde N, Coussens PM, Smith GW, Lonergan P, Ireland JJ and Evans AC. 2008. Differential expression of genes for transcription factors in theca and granulosa cells following selection of a dominant follicle in cattle. Mol. Reprod. Dev. 75:904-914 https://doi.org/10.1002/mrd.20819
  73. Zielak AE, Forde N, Park SD, Doohan F, Coussens PM, Smith GW, Ireland JJ, Lonergan P and Evans AC. 2007. Identification of novel genes associated with dominant follicle development in cattle. Reprod. Fertil. Dev. 19:967-975 https://doi.org/10.1071/RD07102