Profiling the gene signature of endometrial receptivity: Clinical results

Fertility and Sterility

Volumn 99, Issue 4, 2013, Pages 1078-1085

  Garrido Gómez, Tamara ^a   Ruiz Alonso, María ^b   Blesa, David ^a,b   Diaz Gimeno, Patricia ^a,c   Vilella, Felipe ^a   Simón, Carlos ^a,b,d  

^a Biomedical Research Institute Hospital Clinic de Valencia INCLIVA   (Spain)

^b Iviomics SL   (Spain)

^c CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Endometrial Receptivity Array (ERA); Endometrium; infertility; personalized embryo transfer (pET); transcriptomic

Indexed keywords

BIOLOGICAL MARKER; ION CHANNEL;

ADHESION; ALGORITHM; ANGIOGENESIS; APOPTOSIS; BIOINFORMATICS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPUTER; CONFERENCE PAPER; DNA SYNTHESIS; ENDOMETRIUM; ENDOMETRIUM BIOPSY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOMICS; HUMAN; IMPLANTATION; INFERTILITY; INFLAMMATION; MALE INFERTILITY; METABOLISM; MICROARRAY ANALYSIS; MITOSIS INHIBITION; PREDICTION; PRIORITY JOURNAL; TRANSCRIPTOMICS;

BIOLOGICAL MARKERS; EMBRYO TRANSFER; ENDOMETRIUM; FEMALE; FERTILIZATION IN VITRO; HUMANS; INFERTILITY, FEMALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; TRANSCRIPTOME;

EID: 84876405879     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2012.12.005     Document Type: Conference Paper

References (76)

1. A. Psyochoyos Uterine receptivity for nidation Ann N Y Acad Sci 476 1986 36 42
2. J. Martín, F. Domínguez, S. Avila, J.L. Castrillo, J. Remohí, and A. Pellicer Human endometrial receptivity: gene regulation J Reprod Immunol 55 2002 131 139
3. C.L. Finn, and L. Martin Control of implantation J Reprod Fertil 39 1974 195 206
4. C.R. Murphy Uterine receptivity and the plasma membrane transformation Cell Res 14 2004 259 267
5. J.C. Martin, M.J. Jasper, D. Valbuena, M. Meseguer, J. Remohí, A. Pellicer, and C. Simón Increased adhesiveness in cultured endometrial-derived cells is related to the absence of moesin expression Biol Reprod 63 2000 1370 1376
6. M. Thie, B. Harrach-Ruprecht, H. Sauer, P. Fuchs, A. Albers, and H.W. Denker Cell adhesion to the apical pole of epithelium: a function of cell polarity Eur J Cell Biol 66 1995 180 191
7. R.W. Noyes, A.T. Hertig, and J. Rock Dating the endometrial biopsy Fertil Steril 1 1950 3 25
8. R.W. Noyes, A.T. Hertig, and J. Rock Dating the endometrial biopsy Am J Obstet Gynecol 122 1975 262 263
9. C. Coutifaris, E.R. Myers, D.S. Guzick, M.P. Diamond, S.A. Carson, and R.S. Legro Histological dating of timed endometrial biopsy tissue is not related to fertility status Fertil Steril 82 2004 1264 1272
10. M.J. Murray, W.R. Meyer, R.J. Zaino, B.A. Lessey, D.B. Novotny, and K. Ireland A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women Fertil Steril 81 2004 1333 1343
11. J. Balasch, J.A. Vanrell, M. Creus, M. Marquez, and J. Gonzalez-Merlo The endometrial biopsy for diagnosis of luteal phase deficiency Fertil Steril 44 1985 699 701
12. J. Balasch, F. Fabregues, M. Creus, and J.A. Vanrell The usefulness of endometrial biopsy for luteal phase evaluation in infertility Hum Reprod 7 1992 973 977
13. R.T. Scott, R.R. Snyder, D.M. Strickland, C.C. Tyburski, J.A. Bagnall, and K.R. Reed The effect of interobserver variation in dating endometrial histology on the diagnosis of luteal phase defects Fertil Steril 50 1988 888 892
14. R.T. Scott, R.R. Snyder, J.W. Bagnall, K.D. Reed, C.F. Adair, and S.D. Hensley Evaluation of the impact of intraobserver variability on endometrial dating and the diagnosis of luteal phase defects Fertil Steril 60 1993 652 657
15. M. Gibson, G.J. Badger, F. Byrn, K.R. Lee, R. Korson, and T.D. Trainer Error in histologic dating of secretory endometrium: variance component analysis Fertil Steril 56 1991 242 247
16. American Society for Reproductive Medicine A Practice Committee report: optimal evaluation of the infertile female 2000 ASRM Birmingham, AL 1-6
17. J.R. Landis, and G.C. Koch The measurement of observer agreement for categorical data Biometrics 33 1977 159 174
18. G. Nikas Cell-surface morphological events relevant to human implantation Hum Reprod 14 1999 37 44
19. B.A. Lessey Assessment of endometrial receptivity Fertil Steril 96 2011 522 529
20. C.E. Quinn, and R.F. Casper Pinopodes: a questionable role in endometrial receptivity Hum Reprod Update 15 2009 229 236
21. B.A. Lessey, L. Damjanovich, C. Coutifaris, A. Castelbaum, S.M. Albelda, and C.A. Buck Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle J Clin Invest 90 1992 188 195
22. M. Meseguer, A. Pellicer, and C. Simon MUC1 and endometrial receptivity Mol Hum Reprod 4 1998 1089 1098
23. S. Kumar, L.J. Zhu, M. Polihronis, S. Cameron, D.T. Baird, and F. Schaltz Progesterone induces calcitonin gene expression in human endometrium within the putative window of implantation J Clin Endocrinol Metab 83 1998 4443 4450
24. C.L. Stewart, P. Kaspar, L.J. Brunet, H. Bhatt, and I. Gadi Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor Nature 359 1992 76 79
25. B.J. Davis, D.E. Lennard, C.A. Lee, H.F. Tiano, S.G. Morham, W.C. Wetsel, and R. Langanbach Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta Endocrinology 140 1999 2685 2695
26. H. Taylor, P. Igarashi, D. Olive, and A. Arici Sex steroids mediate Hoxa11 expression in the human peri-implantation endometrium J Clin Endocrinol Metab 84 1999 1129 1135
27. L. Aghajanova, C. Simon, and J. Horcajadas Are favorite molecules of endometrial receptivity still in favour? Exp Rev Obstet Gynecol 3 2008 487 501
28. M. Schena, D. Shalon, R.W. Davis, and P.O. Brown Quantitative monitoring of gene expression patterns with a complementary DNA microarray Science 270 1995 467 470
29. J.A. Horcajadas, A. Pellicer, and C. Simón Wide genomic analysis of human endometrial receptivity: new times, new opportunities Hum Reprod Update 13 2007 77 86
30. M. Ruiz-Alonso, D. Blesa, and S. Simón The genomics of the human endometrium Biochim Biophys Acta 1822 2012 1931 1942
31. D. Haouzi, K. Mahmoud, M. Fourar, K. Bendhaou, H. Dechaud, and J. De Vos Identification of new biomarkers of human endometrial receptivity in the natural cycle Hum Reprod 24 2009 198 205
32. L. Aghajanova, A.E. Hamilton, and L.C. Giudice Uterine receptivity to human embryonic implantation: histology, biomarkers, and transcriptomics Semin Cell Dev Biol 19 2008 204 211
33. A. Tapia, C. Vilos, J.C. Marín, H.B. Croxatto, and L. Devoto Bioinformatic detection of E47, E2F1 and SREBP1 transcription factors as potential regulators of genes associated to acquisition of endometrial receptivity Reprod Biol Endocrinol 27 2011 9 14
34. J.A. Horcajadas, A. Riesewijk, J. Martín, A. Cervero, S. Mosselman, and A. Pellicer Global gene expression profiling of human endometrial receptivity J Reprod Immunol 63 2004 41 49
35. A.P. Ponnampalam, G.C. Weston, A.C. Trajstman, B. Susil, and P.A. Rogers Molecular classification of human endometrial cycle stages by transcriptional profiling Mol Hum Reprod 10 2004 879 893
36. L.C. Kao, S. Tulac, S. Lobo, B. Imani, J.P. Yang, and A. Germeyer Global gene profiling in human endometrium during the window of implantation Endocrinology 143 2002 2119 2138
37. D.D. Carson, E. Lagow, A. Thathiah, R. Al-Shami, M.C. Farach-Carson, and M. Vernon Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening Mol Hum Reprod 8 2002 871 879
38. J.M. Borthwick, D.S. Charnock-Jones, B.D. Tom, M.L. Hull, R. Teirney, and S.C. Phillips Determination of the transcript profile of human endometrium Mol Hum Reprod 9 2003 19 33
39. A. Riesewijk, J. Martin, R. van Os, J.A. Horcajadas, J. Polman, and A. Pellicer Gene expression profiling of human endometrial receptivity on days LH+2 versus LH+7 by microarray technology Mol Hum Reprod 9 2003 253 264
40. C. Punyadeera, H. Dassen, J. Klomp, G. Dunselman, R. Kamps, and F. Dijcks Oestrogen-modulated gene expression in the human endometrium Cell Mol Life Sci 62 2005 239 250
41. A. Revel, H. Achache, J. Stevens, Y. Smith, and R. Reich MicroRNAs are associated with human embryo implantation defects Hum Reprod 26 2011 2830 2840
42. I. Vaerenbergh, R. McIntire, L. Van Lommel, P. Devroey, L. Giudice, and C. Bourgain Gene expression during successful implantation in a natural cycle Fertil Steril 93 2010 15 18
43. A. Yanaihara, Y. Otsuka, S. Iwasaki, T. Aida, T. Tachikawa, and T. Irie Differences in gene expression in the proliferative human endometrium Fertil Steril 83 2005 1206 1215
44. S. Mirkin, M. Arslan, D. Churikov, A. Corica, J.I. Diaz, and S. Williams In search of candidate genes critically expressed in the human endometrium during the window of implantation Hum Reprod 20 2005 2104 2117
45. S. Talbi, A.E. Hamilton, K.C. Vo, S. Tulac, M.T. Overgaard, and C. Dosiou Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women Endocrinology 147 2006 1097 1121
46. H.O. Critchley, K.A. Robertson, T. Forster, T.A. Henderson, A.R. Williams, and P. Ghazal Gene expression profiling of mid to late secretory phase endometrial biopsies from women with menstrual complaint Am J Obstet Gynecol 195 2006 1 16
47. S. Kuokkanen, B. Chen, L. Ojalvo, L. Benard, N. Santoro, and J.W. Pollard Genomic profiling of microRNAs and messenger RNAs reveals hormonal regulation in microRNA expression in human endometrium Biol Reprod 82 2010 791 801
48. L.H. Tseng, I. Chen, M.Y. Chen, H. Yan, C.N. Wang, and C.L. Lee Genome-based expression profiling as a single standardized microarray platform for the diagnosis of endometrial disorder: an array of 126-gene model Fertil Steril 94 2010 114 119
49. P. Diaz-Gimeno, J.A. Horcajadas, J.A. Martinez-Conejero, F.J. Esteban, P. Alama, and A. Pellicer A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature Fertil Steril 95 2011 50 60
50. S. Altmae, J.A. Martinez-Conejero, A. Salumets, C. Simon, J.A. Horcajadas, and A. Stavreus-Evers Endometrial gene expression analysis at the time of embryo implantation in women with unexplained infertility Mol Hum Reprod 16 2010 178 187
51. M. Koler, H. Achache, A. Tsafrir, Y. Smith, A. Revel, and R. Reich Disrupted gene pattern in patients with repeated in vitro fertilization (IVF) failure Hum Reprod 24 2009 2541 2548
52. S. Matsuzaki DNA microarray analysis in endometriosis for development of more effective targeted therapies Front Biosci 3 2011 1139 1153
53. J.K. Habermann, N.K. Bundgen, T. Gemoll, S. Hautaniemi, C. Lundgren, and D. Wangsa Genomic instability influences the transcriptome and proteome in endometrial cancer subtypes Mol Cancer 10 2011 132
54. J.A. Horcajadas, P. Minguez, J. Dopazo, F.J. Esteban, F. Dominguez, and L.C. Giudice Controlled ovarian stimulation induces a functional genomics delay of the endometrium with potential clinical implications J Clin Endocrinol Metab 93 2008 4500 4510
55. S. Mirkin, G. Nikas, J.G. Hsiu, J. Diaz, and S. Oehninger Gene expression profiles and structural/functional features of the peri-implantation endometrium in natural and gonadotropin-stimulated cycles J Clin Endocrinol Metab 89 2004 5742 5752
56. C. Simon, J. Oberye, J. Bellver, C. Vidal, E. Bosch, and J.A. Horcajadas Similar endometrial development in oocyte donors treated with either high- or standard-dose GnRH antagonist compared to treatment with a GnRH agonist or in natural cycles Hum Reprod 20 2005 3318 3327
57. J.A. Horcajadas, A. Riesewijk, J. Polman, R. van Os, A. Pellicer, and S. Mosselman Effect of controlled ovarian hyperstimulation in IVF on endometrial gene expression profiles Mol Hum Reprod 11 2005 195 205
58. Y. Liu, K.F. Lee, E.H. Ng, W.S. Yeung, and P.C. Ho Gene expression profiling of human peri-implantation endometria between natural and stimulated cycles Fertil Steril 90 2008 2152 2164
59. N.S. Macklon, M.H. van der Gaast, A. Hamilton, B.C. Fauser, and L.C. Giudice The impact of ovarian stimulation with recombinant FSH in combination with GnRH antagonist on the endometrial transcriptome in the window of implantation Reprod Sci 15 2008 357 365
60. D. Haouzi, S. Assou, K. Mahmoud, S. Tondeur, T. Reme, and B. Hedon Gene expression profile of human endometrial receptivity: comparison between natural and stimulated cycles for the same patients Hum Reprod 24 2009 1436 1445
61. D. Haouzi, S. Assou, C. Dechanet, T. Anahory, H. Dechaud, and J. De Vos Controlled ovarian hyperstimulation for in vitro fertilization alters endometrial receptivity in humans: protocol effects Biol Reprod 82 2010 679 686
62. C. Blockeel, I. Van Vaerenbergh, H.M. Fatemi, L. Van Lommel, P. Devroey, and C. Bourgain Gene expression profile in the endometrium on the day of oocyte retrieval after ovarian stimulation with low-dose hCG in the follicular phase Mol Hum Reprod 1 2011 33 41
63. E. Labarta, J.A. Martínez-Conejero, P. Alamá, J.A. Horcajadas, A. Pellicer, and C. Simón Endometrial receptivity is affected in women with high circulating progesterone levels at the end of the follicular phase: a functional genomics analysis Hum Reprod 26 2011 1813 1825
64. I. Van Vaerenbergh, H.M. Fatemi, C. Blockeel, L. Van Lommel, P. In't Veld, and F. Schuit Progesterone rise on HCG day in GnRH antagonist/rFSH stimulated cycles affects endometrial gene expression Reprod Biomed Online 22 2011 263 271
65. G.E. Evans, J.A. Martínez-Conejero, G.T. Phillipson, C. Simón, L.A. McNoe, and P.H. Sykes Gene and protein expression signature of endometrial glandular and stromal compartments during the window of implantation Fertil Steril 97 2012 1365 1373
66. R.G. Petracco, A. Kong, O. Grechukhina, G. Krikun, and H.S. Taylor Global gene expression profiling of proliferative phase endometrium reveals distinct functional subdivisions Reprod Sci 10 2012 1138 1145
67. F. Domínguez, A. Avila, A. Cervero, J. Martin, A. Pellicer, and J.L. Castrillo A combined approach for gene discovery identifies insulin-like growth factor-binding protein-related protein 1 as a new gene implicated in human endometrial receptivity J Clin Endocrinol Metab 88 2003 1849 1857
68. J.A. Horcajadas, A.M. Sharkey, R.D. Catalano, J.R. Sherwin, F. Domínguez, and L.A. Burgos Effect of an intrauterine device on the gene expression profile of the endometrium J Clin Endocrinol Metab 91 2006 3199 3207
69. Fundacion IVI. Endometrial database. Available at: http://www. endometrialdatabase.com. Last accessed January 2, 2013.
70. T.R. Golub, D.K. Slonim, P. Tamayo, C. Huard, M. Gaasenbeek, and J.P. Mesirov Molecular classification of cancer: class discovery and class prediction by gene expression monitoring Science 286 1999 531 537
71. G. Bloom, I.V. Yang, D. Boulware, K.Y. Kwong, D. Coppola, and S. Eschrich Multiplatform, multi-site, microarray-based human tumor classification Am J Pathol 164 2004 9 16
72. S. Eschrich, I. Yang, G. Bloom, K.Y. Kwong, D. Boulware, and A. Cantor Molecular staging for survival prediction of colorectal cancer patients J Clin Oncol 23 2005 3526 3535
73. J. Quackenbush Microarray analysis and tumor classification N Engl J Med 354 2006 2463 2472
74. T.S. Furey, N. Cristianini, N. Duffy, D.W. Bednarski, M. Schummer, and D. Haussler Support vector machine classification and validation of cancer tissue samples using microarray expression data Bioinformatics 16 2000 906 914
75. P. Díaz-Gimeno, M. Ruiz-Alonso, D. Blesa, N. Bosch, J.A. Martínez-Conejero, and P. Alamá The accuracy and reproducibility of the endometrial receptivity array is superior to histology as a diagnostic method for endometrial receptivity Fertil Steril 99 2013 508 517
76. Simon C. The endometrial receptivity array (ERA) as diagnosis and personalized embryo transfer (pET) as treatment for patients with repeated implantation failure (RIF). Available at: http://clinicaltrials.gov/ct2/show/ NCT01668693. Last accessed February 26, 2013.