Guidelines for the design, analysis and interpretation of 'omics' data: Focus on human endometrium

Human Reproduction Update

Volumn 20, Issue 1, 2014, Pages 12-28

  Altmäe, Signe ^a,b   Esteban, Francisco J ^c   Stavreus Evers, Anneli ^d   Simón, Carlos ^e   Giudice, Linda ^f   Lessey, Bruce A ^g   Horcajadas, Jose A ^h,i   Macklon, Nick S ^j,k   D'Hooghe, Thomas ^l   Campoy, Cristina ^b   Fauser, Bart C ^k   Salamonsen, Lois A ^m   Salumets, Andres ^a,n  

^a Competence Centre on Reproductive Medicine and Biology ^*  (Estonia)

^b UNIVERSITY OF GRANADA   (Spain)

^c UNIVERSITY OF JAÉN   (Spain)

^d UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^e Instituto Universitario IVI INCLIVA   (Spain)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g GREENVILLE HOSPITAL SYSTEM   (United States)

^h HOSPITAL UNIVERSITARIO MIGUEL SERVET   (Spain)

ⁱ UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^j UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^k UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^l UNIVERSITY OF LEUVEN   (Belgium)

^m HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

ⁿ UNIVERSITY OF TARTU   (Estonia)

more..

Author keywords

Endometrium; Epigenomics; Genomics; Metabolomics; Proteomics

Indexed keywords

BIOLOGICAL MARKER; CHEMOKINE; CYTOKINE; ESTROGEN; HORMONE; LIPOCORTIN 2; LIPOCORTIN 4; MICRORNA; PROGESTERONE; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR COMPONENT 1; PROTEIN; PROTEOME; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; BLOOD SAMPLING; CELL METABOLISM; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; DATA PROCESSING; DNA HYBRIDIZATION; ENDOMETRIAL DISEASE; ENDOMETRIOSIS; ENDOMETRIUM; ENDOMETRIUM BIOPSY; ENDOMETRIUM CANCER; EPIGENETICS; ETHNIC OR RACIAL ASPECTS; FACTUAL DATABASE; FEMALE INFERTILITY; FETUS GROWTH; FETUS MATURITY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE LOCUS; GENETIC ASSOCIATION; GENETIC RISK; GENOMICS; HIGH THROUGHPUT SCREENING; HISTOLOGY; HUMAN; INFORMATION PROCESSING; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MEDICAL LITERATURE; MEDLINE; MENSTRUATION; METABOLOME; METABOLOMICS; MICROARRAY ANALYSIS; NIDATION; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PHYSIOLOGICAL PROCESS; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEOMICS; PROTON NUCLEAR MAGNETIC RESONANCE; QUALITY CONTROL; SALIVA ANALYSIS; SAMPLE SIZE; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL ANALYSIS; SYSTEMATIC REVIEW; SYSTEMS BIOLOGY; TRANSCRIPTOMICS; URINALYSIS; UTERUS FLUID; VALIDATION PROCESS; WESTERN BLOTTING;

ENDOMETRIUM; EPIGENOMICS; GENOMICS; METABOLOMICS; PROTEOMICS;

EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; GENOMICS; GUIDELINES AS TOPIC; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; METABOLOMICS; SYSTEMS BIOLOGY;

EID: 84889672301     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmt048     Document Type: Article

References (196)

1. Adachi S, Tajima A, Quan J, Haino K, Yoshihara K, Masuzaki H, Katabuchi H, Ikuma K, Suginami H, Nishida N et al. Meta-analysis of genome-wide association scans for genetic susceptibility to endometriosis in Japanese population. J Hum Genet 2010; 55:816-821.
2. Adriaens ME, Jaillard M, Eijssen LM, MayerCD, EveloCT.An evaluation of two-channel ChIP-on-chip and DNA methylation microarray normalization strategies. BMC Genomics 2012;13:42.
3. Aebersold R, Burlingame AL, Bradshaw RA. Western Blots vs. SRM Assays: Time to turn the tables? Mol Cell Proteomics 2013.
4. Aghajanova L, Hamilton AE, Giudice LC. Uterine receptivity to human embryonic implantation: histology, biomarkers, and transcriptomics. Semin Cell Dev Biol 2008a;19:204-211.
5. Aghajanova L, Simón C, Horcajadas JA. Are favorite molecules of endometrial receptivity still in favor? Expert Rev Obstet Gynecol 2008b;3:487-501.
6. Allen J, Davey HM, Broadhurst D, Heald JK, Rowland JJ, Oliver SG, Kell DB. High-throughput classification of yeast mutants for functional genomics using metabolic footprinting. Nat Biotechnol 2003;21:692-696.
7. Altmäe S, Martinez-Conejero JA, Salumets A, Simon C, Horcajadas JA, Stavreus-Evers A. Endometrial gene expression analysis at the time of embryo implantation in women with unexplained infertility. Mol Hum Reprod 2010; 16:178-187.
8. Altmäe S, Salumets A.Anovel genomic diagnostic tool for sperm quality? Reprod Biomed Online 2011.
9. Altmäe S, Hovatta O, Stavreus-Evers A, Salumets A. Genetic predictors of controlled ovarian hyperstimulation: where do we stand today? Hum Reprod Update 2011; 17:813-828.
10. Altmäe S, Reimand J, Hovatta O, Zhang P, Kere J, Laisk T, Saare M, Peters M, Vilo J, Stavreus-Evers A et al. Research resource: interactome of human embryo implantation: identification of gene expression pathways, regulation, and integrated regulatory networks. Mol Endocrinol 2012;26:203-217.
11. Altmäe S, Martinez-Conejero JA, Esteban FJ, Ruiz-Alonso M, Stavreus-Evers A, Horcajadas JA, Salumets A. MicroRNAs miR-30b, miR-30d, and miR-494 Regulate Human Endometrial Receptivity. Reproduct Sci 2013;20:308-317.
12. Aranibar N, Ott KH, Roongta V, Mueller L. Metabolomic analysis using optimizedNMR and statistical methods. Anal Biochem 2006;355:62-70.
13. Assou S, Haouzi D, De Vos J, Hamamah S. Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Mol Hum Reproduct 2010;16:531-538.
14. Baker M. Gene data to hit milestone. Nature 2012;487:282-283.
15. Barash A, Dekel N, Fieldust S, Segal I, Schechtman E, Granot I. Local injury to the endometrium doubles the incidence of successful pregnancies in patients undergoing in vitro fertilization. Fertil Steril 2003;79:1317-1322.
16. Becnel LB, McKenna NJ. Minireview: progress and challenges in proteomics data management, sharing, and integration. Mol Endocrinol 2012;26:1660-1674.
17. Beisvag V, Kauffmann A, Malone J, Foy C, Salit M, Schimmel H, Bongcam-Rudloff E, Landegren U, Parkinson H, Huber W et al. Contributions of the EMERALD project to assessing and improving microarray data quality. Biotechniques 2011; 50:27-31.
18. Bellver J, Mundi M, Esteban FJ, Mosquera S, Horcajadas JA. '-OMICs' technology and human reproduction: reproductomics. Expert Rev Obstet Gynecol 2012; 7:493-506.
19. Berlanga O, Bradshaw HB, Vilella-Mitjana F, Garrido-Gomez T, Simon C. How endometrial secretomics can help in predicting implantation. Placenta 2011; 32(Suppl. 3):S271-275.
20. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006;125:1111-1124.
21. Boomsma CM, Kavelaars A, Eijkemans MJ, Amarouchi K, Teklenburg G, Gutknecht D, Fauser BJ, Heijnen CJ, Macklon NS. Cytokine profiling in endometrial secretions: a non-invasive window on endometrial receptivity. Reprod Biomed Online 2009a; 18:85-94.
22. Boomsma CM, Kavelaars A, Eijkemans MJ, Lentjes EG, Fauser BC, Heijnen CJ, Macklon NS. Endometrial secretion analysis identifies a cytokine profile predictive of pregnancy in IVF. Hum Reprod 2009b;24:1427-1435.
23. Borghese B, Barbaux S, Mondon F, Santulli P, Pierre G, Vinci G, Chapron C, Vaiman D. Research resource: genome-wide profiling of methylated promoters in endometriosis reveals a subtelomeric location of hypermethylation. Mol Endocrinol 2010;24:1872-1885.
24. Botros L, Sakkas D, Seli E. Metabolomics and its application for non-invasive embryo assessment in IVF. Mol Hum Reprod 2008;14:679-690.
25. Brady PD, Vermeesch JR. Genomic microarrays: a technology overview. Prenat Diagn 2012;32:336-343.
26. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC et al. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 2001; 29:365-371.
27. Brinsden PR, Alam V, de Moustier B, Engrand P. Recombinant human leukemia inhibitory factor does not improve implantation and pregnancy outcomes after assisted reproductive techniques in women with recurrent unexplained implantation failure. Fertil Steril 2009;91:1445-1447.
28. Bryc K, Auton A, Nelson MR, Oksenberg JR, Hauser SL, Williams S, Froment A, Bodo JM, Wambebe C, Tishkoff SA et al. Genome-wide patterns of population structure and admixture in West Africans and African Americans. Proc Natl Acad SciUSA 2010;107:786-791.
29. Burney RO. The genetics and biochemistry of endometriosis. Curr Opin Obstet Gynecol 2013;25:280-286.
30. Burney RO, Talbi S, Hamilton AE, Vo KC, Nyegaard M, Nezhat CR, Lessey BA, Giudice LC. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 2007;148:3814-3826.
31. Burney RO, Hamilton AE, Aghajanova L, Vo KC, Nezhat CN, Lessey BA, Giudice LC. MicroRNA expression profiling of eutopic secretory endometrium in women with versus without endometriosis. Mol Hum Reprod 2009;15:625-631.
32. Burnum KE, Tranguch S, Mi D, Daikoku T, Dey SK, Caprioli RM. Imaging mass spectrometry reveals unique protein profiles during embryo implantation. Endocrinology 2008;149:3274-3278.
33. Cairns DA, Perkins DN, Stanley AJ, Thompson D, Barrett JH, Selby PJ, Banks RE. Integrated multi-level quality control for proteomic profiling studies using mass spectrometry. BMC Bioinformatics 2008;9:519.
34. Callinan PA, Feinberg AP. The emerging science of epigenomics. Hum Mol Genet 2006; 15:R95-101.
35. Cappadona S, Baker PR, Cutillas PR, Heck AJ, van Breukelen B. Current challenges in software solutions for mass spectrometry-based quantitative proteomics. Amino Acids 2012;43:1087-1108.
36. Carthew RW, Sontheimer EJ. Origins and Mechanisms of miRNAs and siRNAs. Cell 2009;136:642-655.
37. Casado-Vela J, Rodriguez-Suarez E, Iloro I, Ametzazurra A, Alkorta N, Garcia-Velasco JA, Matorras R, Prieto B, Gonzalez S, Nagore D et al. Comprehensive proteomic analysis of human endometrial fluid aspirate. J Proteome Res 2009;8:4622-4632.
38. Cheong Y, Boomsma C, Heijnen C, Macklon N. Uterine secretomics: a window on the maternal-embryo interface. Fertil Steril 2013;99:1093-1099.
39. Chervitz SA, Deutsch EW, Field D, Parkinson H, Quackenbush J, Rocca-Serra P, Sansone SA, Stoeckert CJ Jr., Taylor CF, Taylor R et al. Data standards for Omics data: the basis of data sharing and reuse. Methods Mol Biol 2011;719:31-69.
40. Clark IM, Swingler TE, Young DA. Acetylation in the regulation of metalloproteinase and tissue inhibitor of metalloproteinases gene expression. Front Biosci 2007; 12:528-535.
41. Cordero F, Botta M, Calogero RA. Microarray data analysis and mining approaches. Brief Funct Genomic Proteomic 2007;6:265-281.
42. Coutifaris C, Myers ER, Guzick DS, Diamond MP, Carson SA, Legro RS, McGovern PG, Schlaff WD, Carr BR, Steinkampf MP et al. Histological dating of timed endometrial biopsy tissue is not related to fertility status. Fertil Steril 2004;82:1264-1272.
43. Cox J, Mann M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu Rev Biochem 2011;80:273-299.
44. Creighton CJ, Benham AL, Zhu H, Khan MF, Reid JG, Nagaraja AK, Fountain MD, Dziadek O, Han D, Ma L et al. Discovery of novel microRNAs in female reproductive tract using next generation sequencing. PLoS ONE 2010;5:e9637.
45. Csordas A, Ovelleiro D,Wang R, Foster JM, Rios D, Vizcaino JA, Hermjakob H. PRIDE: quality control in a proteomics data repository. Database (Oxford) 2012; 2012:bas004.
46. Day FR, Loos RJ. Developments in obesity genetics in the era of genome-wide association studies. J Nutrigenet Nutrigenomics 2011;4:222-238.
47. Deatherage DE, Potter D, Yan PS, Huang TH, Lin S. Methylation analysis by microarray. Methods Mol Biol 2009;556:117-139.
48. Diaz-Gimeno P, Horcajadas JA, Martinez-Conejero JA, Esteban FJ, Alama P, Pellicer A, Simon C. Agenomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril 2011;95:50-60, 60 e51-15.
49. Diaz-Gimeno P, Ruiz-Alonso M, Blesa D, Bosch N, Martinez-Conejero JA, Alama P, Garrido N, Pellicer A, Simon C. The accuracy and reproducibility of the endometrial receptivity array is superior to histology as a diagnostic method for endometrial receptivity. Fertil Steril 2013;99:508-517.
50. Doll A, Abal M, Rigau M, Monge M, Gonzalez M, Demajo S, Colas E, Llaurado M, Alazzouzi H, Planaguma J et al. Novel molecular profiles of endometrial cancer-new light through old windows. J Steroid Biochem Mol Biol 2008; 108:221-229.
51. Dominguez F, Garrido-Gomez T, Lopez JA, Camafeita E, Quinonero A, Pellicer A, Simon C. Proteomic analysis of the human receptive versus non-receptive endometrium using differential in-gel electrophoresis and MALDI-MS unveils stathmin 1 and annexin A2 as differentially regulated. Hum Reprod 2009; 24:2607-2617.
52. Durinck S. Pre-processing of microarray data and analysis of differential expression. Methods Mol Biol 2008;452:89-110.
53. Edgell TA, Rombauts LJF, Salamonsen LA. Assessing receptivity in the endometrium: the need for a rapid, non-invasive test. Reprod Biomed Online 2013; in press. Editorial Method of the Year 2012. Nat Methods 2013;10:1.
54. Estella C, Herrer I, Moreno-Moya JM, Quinonero A, Martinez S, Pellicer A, Simon C. miRNA signature and Dicer requirement during human endometrial stromal decidualization in vitro. PLoS ONE 2012;7:e41080.
55. Evans GE, Martinez-Conejero JA, Phillipson GT, Simon C, McNoe LA, Sykes PH, Horcajadas JA, Lam EY, Print CG, Sin IL et al. Gene and protein expression signature of endometrial glandular and stromal compartments during the window of implantation. Fertil Steril 2012a;97:1365-1373 e1361-1362.
56. Evans GE, Phillipson GT, Sin IL, Frampton CM, Kirker JA, Bigby SM, Evans JJ. Gene expression confirms a potentially receptive endometrium identified by histology in fertile women. Hum Reprod 2012b;27:2747-2755.
57. Fassbender A, Simsa P, Kyama CM,Waelkens E, Mihalyi A, Meuleman C, Gevaert O, Van de Plas R, de Moor B, D'Hooghe TM. TRIzol treatment of secretory phase endometrium allows combined proteomic and mRNA microarray analysis of the same sample in women with and without endometriosis. Reprod Biol Endocrinol 2010;8:123.
58. Fassbender A, Verbeeck N, Bornigen D, Kyama CM, Bokor A, Vodolazkaia A, Peeraer K, Tomassetti C, Meuleman C, Gevaert O et al. Combined mRNA microarray and proteomic analysis of eutopic endometrium of women with and without endometriosis. Hum Reprod 2012a;27:2020-2029.
59. Fassbender A,Waelkens E, Verbeeck N, Kyama CM, Bokor A, Vodolazkaia A, Van de Plas R, Meuleman C, Peeraer K, TomassettiCet al. Proteomics analysis of plasma for early diagnosis of endometriosis. Obstet Gynecol 2012b;119:276-285.
60. Fassbender A, Vodolazkaia A, Saunders P, Lebovic D, Waelkens E, De Moor B, D'Hooghe T. Biomarkers of endometriosis. Fertil Steril 2013;99:1135-1145.
61. Garrido-Gomez T, Dominguez F, Simon C. Proteomics of embryonic implantation. Handb Exp Pharmacol 2010;67-78.
62. Garrido-GomezT, Ruiz-Alonso M, Blesa D, Diaz-Gimeno P, Vilella F, Simon C. Profiling the gene signature of endometrial receptivity: clinical results. Fertil Steril 2013; 99:1078-1085.
63. Gilabert-Estelles J, Braza-Boils A, Ramon LA, Zorio E, Medina P, Espana F, Estelles A. Role of microRNAs in gynecological pathology. Curr Med Chem 2012; 19:2406-2413.
64. Giudice LC. Potential biochemical markers of uterine receptivity. Hum Reprod 1999; 14(Suppl. 2):3-16.
65. Giudice LC. Application of functional genomics to primate endometrium: insights into biological processes. Reprod Biol Endocrinol 2006;4(Suppl. 1):S4.
66. Giudice LC, Talbi S, Hamilton AE, Lessey BA. Transcriptomics. In: The Endometrium. London: Informa, 2008.
67. Gracie S, Pennell C, Ekman-Ordeberg G, Lye S, McManaman J, Williams S, Palmer L, Kelley M, Menon R, Gravett M. An integrated systems biology approach to the study of preterm birth using '-omic' technology - a guideline for research. BMC Pregnancy Childbirth 2011;11:71.
68. Gunaratne PH, Creighton CJ, Watson M, Tennakoon JB. Large-scale integration of MicroRNA and gene expression data for identification of enriched microRNA-mRNA associations in biological systems. Methods Mol Biol 2010; 667:297-315.
69. Guo SW. The association of endometriosis risk and genetic polymorphisms involving dioxin detoxification enzymes: a systematic review. Eur J Obstet Gynecol Reprod Biol 2006;124:134-143.
70. Guo SW. The endometrial epigenome and its response to steroid hormones. Mol Cell Endocrinol 2012;358:185-196.
71. Guo SW, Wu Y, Strawn E, Basir Z, Wang Y, Halverson G, Montgomery K, Kajdacsy-Balla A. Genomic alterations in the endometrium may be a proximate cause for endometriosis. Eur J Obstet Gynecol Reprod Biol 2004;116:89-99.
72. Ha TY. MicroRNAs in human diseases: from lung, liver and kidney diseases to infectious disease, sickle cell disease and endometrium disease. Immune Netw 2011; 11:309-323.
73. Hannan NJ, Stoikos CJ, Stephens AN, Salamonsen LA. Depletion of high-abundance serum proteins from human uterine lavages enhances detection of lower-abundance proteins. J Proteome Res 2009;8:1099-1103.
74. Hannan NJ, Stephens AN, Rainczuk A, Hincks C, Rombauts LJ, Salamonsen LA. 2D-DiGE analysis of the human endometrial secretome reveals differences between receptive and nonreceptive states in fertile and infertile women. J Proteome Res 2010;9:6256-6264.
75. Hannan NJ, Evans J, Salamonsen LA. Alternate roles for immune regulators: establishing endometrial receptivity for implantation. Expert Rev Clin Immunol 2011a;7:789-802.
76. Hannan NJ, Paiva P, Meehan KL, Rombauts LJ, Gardner DK, Salamonsen LA. Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology 2011b;152:4948-4956.
77. Hannan NJ, Nie G, Rainzcuk A, Rombauts LJ, Salamonsen LA. Uterine lavage or aspirate: which view of the intrauterine environment? Reprod Sci 2012; 19:1125-1132.
78. Hansen KA, Eyster KM. Genetics and genomics of endometriosis. Clin Obstet Gynecol 2010;53:403-412.
79. Haouzi D, Mahmoud K, Fourar M, Bendhaou K, Dechaud H, De Vos J, Reme T, Dewailly D, Hamamah S. Identification of new biomarkers of human endometrial receptivity in the natural cycle. Hum Reprod 2009;24:198-205.
80. Haouzi D, Dechaud H, Assou S,DeVos J,HamamahS. Insights into human endometrial receptivity from transcriptomic and proteomic data. Reprod Biomed Online 2012; 24:23-34.
81. Harper MJ. The implantation window. Baillieres Clin Obstet Gynaecol 1992;6:351-371.
82. Hawkins SM, Creighton CJ, Han DY, Zariff A, Anderson ML, Gunaratne PH, Matzuk MM. Functional microRNA involved in endometriosis. Mol Endocrinol 2011;25:821-832.
83. Horcajadas JA, Riesewijk A, Dominguez F, Cervero A, Pellicer A, Simon C. Determinants of endometrial receptivity. Ann N Y Acad Sci 2004;1034:166-175.
84. Horcajadas JA, Pellicer A, Simon C. Wide genomic analysis of human endometrial receptivity: new times, new opportunities. Hum Reprod Update 2007;13:77-86.
85. Horgan RP, Clancy OH, Myers JE, Baker PN. An overview of proteomic and metabolomic technologies and their application to pregnancy research. BJOG 2009;116:173-181.
86. Huang J, Qi R, Quackenbush J, Dauway E, Lazaridis E, Yeatman T. Effects of ischemia on gene expression. J Surg Res 2001;99:222-227.
87. Ikeda Y, Oda K, Nakagawa S, Murayama-Hosokawa S, Yamamoto S, Ishikawa S, Wang L, Takazawa Y, Maeda D, Wada-Hiraike O et al. Genome-wide single nucleotide polymorphism arrays as a diagnostic tool in patients with synchronous endometrial and ovarian cancer. Int J Gynecol Cancer 2012;22:725-731.
88. Illig T, Gieger C, Zhai G, Romisch-Margl W, Wang-Sattler R, Prehn C, Altmaier E, Kastenmuller G, Kato BS, Mewes HW et al. A genome-wide perspective of genetic variation in human metabolism. Nat Genet 2010;42:137-141.
89. Ioannidis JP, Allison DB, Ball CA, Coulibaly I, Cui X, Culhane AC, Falchi M, Furlanello C, Game L, Jurman G et al. Repeatability of published microarray gene expression analyses. Nat Genet 2009;41:149-155.
90. IzawaM, Taniguchi F, Terakawa N, Harada T. Epigenetic aberration of gene expression in endometriosis. Front Biosci (Elite Ed) 2013;E5:900-910.
91. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, Osteen K, Lessey BA, Giudice LC. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003;144:2870-2881.
92. Kinsinger CR, Apffel J, Baker M, Bian X, Borchers CH, Bradshaw R, Brusniak MY, Chan DW, Deutsch EW, Domon B et al. Recommendations for mass spectrometry data quality metrics for open access data (corollary to the Amsterdam Principles). J Proteome Res 2012;11:1412-1419.
93. Koks S, Velthut A, Sarapik A, Altmae S, Reinmaa E, Schalkwyk LC, Fernandes C, LadHV, Soomets U, Jaakma U et al. The differential transcriptome and ontology profiles of floating and cumulus granulosa cells in stimulated human antral follicles. Mol Hum Reprod 2010;16:229-240.
94. Koot YE, Teklenburg G, Salker MS, Brosens JJ, Macklon NS. Molecular aspects of implantation failure. Biochim Biophys Acta 2012;1822:1943-1950.
95. Koulman A, Lane GA, Harrison SJ, Volmer DA. From differentiating metabolites to biomarkers. Anal Bioanal Chem 2009;394:663-670.
96. Kumar C, Mann M. Bioinformatics analysis of mass spectrometry-based proteomics data sets. FEBS Lett 2009;583:1703-1712.
97. Kuokkanen S, Chen B, Ojalvo L, Benard L, Santoro N, Pollard JW. Genomic profiling of microRNAs and messenger RNAs reveals hormonal regulation in microRNA expression in human endometrium. Biol Reprod 2010;82:791-801.
98. Lagarde M, Geloen A, Record M, Vance D, Spener F. Lipidomics is emerging. Biochim Biophys Acta 2003;1634:61.
99. Lessey BA. The role of the endometrium during embryo implantation. Hum Reprod 2000;15(Suppl. 6):39-50.
100. Lessey BA. Fine tuning of endometrial function by estrogen and progesterone through microRNAs. Biol Reprod 2010;82:653-655.
101. Lessey BA. Assessment of endometrial receptivity. Fertil Steril 2011;96:522-529.
102. Li R, Qiao J,Wang L, Li L, Zhen X, Liu P, Zheng X. MicroRNA array and microarray evaluation of endometrial receptivity in patients with high serum progesterone levels on the day of hCG administration. Reprod Biol Endocrinol 2011;9:29.
103. Licht P, Russu V, Lehmeyer S, Wildt L. Molecular aspects of direct LH/hCG effects on human endometrium - lessons from intrauterine microdialysis in the human female in vivo. Reprod Biol 2001;1:10-19.
104. Longuespee R, Gagnon H, Boyon C, Strupat K, Dauly C, Kerdraon O, Ighodaro A, Desmons A, Dupuis J, Wisztorski M et al. Proteomic analyses of serous and endometrioid epithelial ovarian cancers - cases studies - molecular insights of a possible histological etiology of serous ovarian cancer. Proteomics Clin Appl 2013; 7:337-354.
105. Loven J, Orlando DA, Sigova AA, Lin CY, Rahl PB, Burge CB, Levens DL, Lee TI, Young RA. Revisiting global gene expression analysis. Cell 2012;151:476-482.
106. Malone JH, Oliver B. Microarrays, deep sequencing and the true measure of the transcriptome. BMC Biol 2011;9:34.
107. Mannello F, Ligi D, Magnani M. Deciphering the single-cell omic: innovative application for translational medicine. Expert Rev Proteomics 2012;9:635-648.
108. Marabita F, Almgren M, Lindholm M, Ruhrmann S, Fagerstrom-Billai F, Jagodic M, Sundberg CJ, Ekstrom TJ, Teschendorff AE, Tegner J et al. An evaluation of analysis pipelines for DNA methylation profiling using the Illumina HumanMethylation450 BeadChip platform. Epigenetics 2013;8:333-346.
109. Martinez-Conejero JA, Simon C, Pellicer A, Horcajadas JA. Is ovarian stimulation detrimental to the endometrium? Reprod Biomed Online 2007;15:45-50.
110. Matsuzaki S. DNA microarray analysis in endometriosis for development of more effective targeted therapies. Front Biosci (Elite Ed) 2011;3:1139-1153.
111. Matthiesen R, Azevedo L, Amorim A, Carvalho AS. Discussion on common data analysis strategies used in MS-based proteomics. Proteomics 2011;11: 604-619.
112. May KE, Villar J, Kirtley S, Kennedy SH, Becker CM. Endometrial alterations in endometriosis: a systematic review of putative biomarkers. Hum Reprod Update 2011;17:637-653.
113. Meehan KL, Rainczuk A, Salamonsen LA, Stephens AN. Proteomics and the search for biomarkers of female reproductive diseases. Reproduction 2010;140:505-519.
114. Micke P, Ohshima M, Tahmasebpoor S, Ren ZP, Ostman A, Ponten F, Botling J. Biobanking of fresh frozen tissue: RNA is stable in nonfixed surgical specimens. Lab Invest 2006;86:202-211.
115. Mirkin S, Arslan M, Churikov D, Corica A, Diaz JI, Williams S, Bocca S, Oehninger S. In search of candidate genes critically expressed in the human endometrium during the window of implantation. Hum Reprod 2005;20:2104-2117.
116. Mocellin S,Rossi CR. Principles of gene microarray data analysis. Adv ExpMed Biol 2007; 593:19-30.
117. Munro SK, Farquhar CM, Mitchell MD, Ponnampalam AP. Epigenetic regulation of endometrium during the menstrual cycle. Mol Hum Reprod 2010;16:297-310.
118. Murray MJ, Meyer WR, Zaino RJ, Lessey BA, Novotny DB, Ireland K, Zeng D, Fritz MA. A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women. Fertil Steril 2004;81:1333-1343.
119. Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, Salamonsen LA. Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS ONE 2013; 8:e58502.
120. Nicholson JK, Lindon JC. Systems biology: Metabonomics. Nature 2008; 455:1054-1056.
121. Nielsen J, Oliver S. The next wave in metabolome analysis. Trends Biotechnol 2005; 23:544-546.
122. Ning K, Fermin D, Nesvizhskii AI. Comparative analysis of different label-free mass spectrometry based protein abundance estimates and their correlation with RNA-Seq gene expression data. J Proteome Res 2012;11:2261-2271.
123. NoyesRW, Hertig AT, Rock J. Dating the endometrial biopsy. Fertil Steril 1950;1:3-25.
124. NoyesRW, HertigAT, Rock J. Dating the endometrial biopsy.AmJ Obstet Gynecol 1975; 122:262-263.
125. Nyholt DR, Low SK, Anderson CA, Painter JN, Uno S, Morris AP, MacGregor S, Gordon SD, Henders AK, Martin NG et al. Genome-wide association meta-analysis identifies new endometriosis risk loci. Nat Genet 2012; 44:1355-1359.
126. Painter JN, Anderson CA,Nyholt DR, Macgregor S, Lin J, Lee SH, Lambert A, Zhao ZZ, Roseman F, GuoQet al. Genome-wide association study identifies a locus at 7p15.2 associated with endometriosis. Nat Genet 2011;43:51-54.
127. Paiva P, Hannan NJ, Hincks C, Meehan KL, Pruysers E, Dimitriadis E, Salamonsen LA. Human chorionic gonadotrophin regulates FGF2 and other cytokines produced by human endometrial epithelial cells, providing a mechanism for enhancing endometrial receptivity. Hum Reprod 2011;26:1153-1162.
128. Pinto D, Darvishi K, Shi X, Rajan D, Rigler D, Fitzgerald T, Lionel AC, Thiruvahindrapuram B, Macdonald JR, Mills R et al. Comprehensive assessment of array-based platforms and calling algorithms for detection of copy number variants. Nature Biotechnol 2011;29:512-520.
129. Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: approaches and considerations. Nat Rev Genet 2012;13:358-369.
130. Rahmioglu N, Missmer SA, Montgomery GW, Zondervan KT. Insights into Assessing the Genetics of Endometriosis. Curr Obstet Gynecol Rep 2012;1:124-137.
131. Rahnama F, Thompson B, Steiner M, Shafiei F, Lobie PE, Mitchell MD. Epigenetic regulation of E-cadherin controls endometrial receptivity. Endocrinology 2009; 150:1466-1472.
132. Ramon LA, Braza-Boils A, Gilabert J, Chirivella M, Espana F, Estelles A, Gilabert-Estelles J. microRNAs related to angiogenesis are dysregulated in endometrioid endometrial cancer. Hum Reprod 2012;27:3036-3045.
133. Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, Fiegler H, Shapero MH, Carson AR, ChenWet al. Global variation in copy number in the human genome. Nature 2006;444:444-454.
134. Revel A, Achache H, Stevens J, SmithY, Reich R. MicroRNAs are associated with human embryo implantation defects. Hum Reprod 2011;26:2830-2840.
135. Robert C. Microarray analysis of gene expression during early development: a cautionary overview. Reproduction 2010;140:787-801.
136. Rubio C, Rodrigo L, Mercader A, Mateu E, Buendia P, Pehlivan T, Viloria T, De los Santos MJ, Simon C, Remohi J et al. Impact of chromosomal abnormalities on preimplantation embryo development. Prenat Diagn 2007;27:748-756.
137. Ruiz-Alonso M, Blesa D, Simon C. The genomics of the human endometrium. Biochim Biophys Acta 2012;1822:1931-1942.
138. Ruiz-Alonso M, Blesa D, Diaz-Gimeno P, Vilella F, Pellicer A, Simon C. The endometrial receptivity array as diagnosis and personalized embryo transfer as treatment for patients with receptive implantation failure. Fertil Steril 2013;100:818-824.
139. Saare M, Soritsa D, Vaidla K, Palta P, Remm M, Laan M, Karro H, Soritsa A, Salumets A, D'Hooghe T et al. No evidence of somatic DNA copy number alterations in eutopic and ectopic endometrial tissue in endometriosis. Hum Reprod 2012;27:1857-1864.
140. Salamonsen LA, Nie G, Hannan NJ, Dimitriadis E. Society for Reproductive Biology Founders' Lecture 2009. Preparing fertile soil: the importance of endometrial receptivity. Reprod Fertil Dev 2009;21:923-934.
141. Salamonsen LA, Edgell T, Rombauts LJ, Stephens AN, Robertson DM, Rainczuk A, Nie G, Hannan NJ. Proteomics of the human endometrium and uterine fluid: a pathway to biomarker discovery. Fertil Steril 2013;99:1086-1092.
142. Sarkar D, Parkin R, Wyman S, Bendoraite A, Sather C, Delrow J, Godwin AK, Drescher C, Huber W, Gentleman R et al. Quality assessment and data analysis for microRNA expression arrays. Nucleic Acids Res 2009;37:e17.
143. Savaris RF, Giudice LC. Genomics analysis: endometrium. Methods Mol Biol 2009; 590:91-113.
144. Schwamborn K, Krieg RC, Uhlig S, Ikenberg H, Wellmann A. MALDI imaging as a specific diagnostic tool for routine cervical cytology specimens. Int J Mol Med 2011;27:417-421.
145. Scotchie JG, Fritz MA, Mocanu M, Lessey BA, Young SL. Proteomic analysis of the luteal endometrial secretome. Reprod Sci 2009;16:883-893.
146. Seli E, Robert C, Sirard MA. OMICS in assisted reproduction: possibilities and pitfalls. Mol Hum Reprod 2010;16:513-530.
147. Sha AG, Liu JL, Jiang XM, Ren JZ, Ma CH, Lei W, Su RW, Yang ZM. Genome-wide identification of micro-ribonucleic acids associated with human endometrial receptivity in natural and stimulated cycles by deep sequencing. Fertil Steril 2011; 96:150-155 e155.
148. Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, Halliday N, Khan Y, Warley A, McCann FE, Hider RC et al. Identification of an intestinal heme transporter. Cell 2005;122:789-801.
149. Sheldon E, Vo KC, McIntire RA, Aghajanova L, Zelenko Z, Irwin JC, Giudice LC. Biobanking human endometrial tissue and blood specimens: standard operating procedure and importance to reproductive biology research and diagnostic development. Fertil Steril 2011;95:2120-2122, 2122, e2121-2112.
150. Sherwin R, Catalano R, Sharkey A. Large-scale gene expression studies of the endometrium: what have we learnt? Reproduction 2006;132:1-10.
151. Slattery M, Ankisetty S, Corrales J, Marsh-Hunkin KE, Gochfeld DJ, Willett KL, Rimoldi JM. Marine proteomics: a critical assessment of an emerging technology. J Nat Prod 2012;75:1833-1877.
152. Spitzer TL, Rojas A, Zelenko Z, Aghajanova L, Erikson DW, Barragan F, Meyer M, Tamaresis JS, Hamilton AE, Irwin JC et al. Perivascular human endometrial mesenchymal stem cells express pathways relevant to self-renewal, lineage specification, and functional phenotype. Biol Reprod 2012;86:58.
153. Spruessel A, Steimann G, Jung M, Lee SA, Carr T, Fentz AK, Spangenberg J, Zornig C, Juhl HH, David KA. Tissue ischemia time affects gene and protein expression patterns within minutes following surgical tumor excision. Biotechniques 2004; 36:1030-1037.
154. Stephens AN, Hannan NJ, Rainczuk A, Meehan KL, Chen J, Nicholls PK, Rombauts LJ, Stanton PG, Robertson DM, Salamonsen LA. Post-translational modifications and protein-specific isoforms in endometriosis revealed by 2D DIGE. J Proteome Res 2010;9:2438-2449.
155. Suarez E, Burguete A, McLachlan GJ. Microarray data analysis for differential expression: a tutorial. P R Health Sci J 2009;28:89-104.
156. Sundaresh S, Doolan DL, Hirst S, Mu Y, Unal B, Davies DH, Felgner PL, Baldi P. Identification of humoral immune responses in protein microarrays using DNA microarray data analysis techniques. Bioinformatics 2006;22:1760-1766.
157. Sundqvist J, Xu H, Vodolazkaia A, Fassbender A, Kyama C, Bokor A, Gemzell-Danielsson K, D'Hooghe TM, Falconer H. Replication of endometriosis-associated single-nucleotide polymorphisms from genome-wide association studies in a Caucasian population. Hum Reprod 2013;28:835-839.
158. Talbi S, Hamilton AE,VoKC, Tulac S, OvergaardMT, Dosiou C, Le Shay N, NezhatCN, Kempson R, Lessey BA et al. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 2006;147:1097-1121.
159. Tapia A, Vilos C, Marin JC, Croxatto HB, Devoto L. Bioinformatic detection of E47, E2F1 and SREBP1 transcription factors as potential regulators of genes associated to acquisition of endometrial receptivity. Reprod Biol Endocrinol 2011;9:14.
160. TaylorCF,FieldD,SansoneSA,Aerts J,ApweilerR,AshburnerM,BallCA,BinzPA,BogueM, Booth T et al. Promoting coherent minimum reporting guidelines for biological and biomedical investigations: the MIBBI project. Nat Biotechnol 2008;26:889-896.
161. Teklenburg G, Macklon NS. Review: in vitro models for the study of early human embryo-endometrium interactions. Reprod Sci 2009;16:811-818.
162. Teklenburg G, Salker M, Molokhia M, Lavery S, Trew G, Aojanepong T, Mardon HJ, Lokugamage AU, Rai R, Landles C et al. Natural selection of human embryos: decidualizing endometrial stromal cells serve as sensors of embryo quality upon implantation. PLoS ONE 2010;5:e10258.
163. Torres A, Torres K, Pesci A, Ceccaroni M, Paszkowski T, Cassandrini P, Zamboni G, Maciejewski R. Diagnostic and prognostic significance of miRNA signatures in tissues and plasma of endometrioid endometrial carcinoma patients. Int J Cancer 2013;132:1633-1645.
164. Toth B, WurfelW, Germeyer A, Hirv K, Makrigiannakis A, Strowitzki T. Disorders of implantation-are there diagnostic and therapeutic options?. J Reprod Immunol 2011; 90:117-123.
165. Treff NR. Genome-wide analysis of human preimplantation aneuploidy. Semin Reprod Med 2012;30:283-288.
166. Uchida H, Maruyama T, Nagashima T, Asada H, Yoshimura Y. Histone deacetylase inhibitors induce differentiation of human endometrial adenocarcinoma cells through up-regulation of glycodelin. Endocrinology 2005;146:5365-5373.
167. UchidaH, Maruyama T,Ohta K,OnoM,Arase T, KagamiM,OdaH,KajitaniT,AsadaH, YoshimuraY.Histonedeacetylase inhibitor-inducedglycodelin enhances theinitial step of implantation. Hum Reprod 2007;22:2615-2622.
168. Ulbrich SE, Groebner AE, Bauersachs S. Transcriptional profiling to address molecular determinants of endometrial receptivity - lessons from studies in livestock species. Methods 2013;59:108-115.
169. Uno S, Zembutsu H, Hirasawa A, Takahashi A, Kubo M, Akahane T, Aoki D, Kamatani N, Hirata K, Nakamura Y. A genome-wide association study identifies genetic variants in the CDKN2BAS locus associated with endometriosis in Japanese. Nat Genet 2010;42:707-710.
170. Upadhyay RD, Balasinor NH, Kumar AV, Sachdeva G, Parte P, Dumasia K. Proteomics in reproductive biology: beacon for unraveling the molecular complexities. Biochim Biophys Acta 2013;1834:8-15.
171. Vanneste E, Bittman L, Van der Aa N, Voet T, Vermeesch JR. Newarray approaches to explore single cells genomes. Front Genet 2012;3:44.
172. Veiga-Castelli LC, Silva JC, Meola J, Ferriani RA, Yoshimoto M, Santos SA, Squire JA, Martelli L. Genomic alterations detected by comparative genomic hybridization in ovarian endometriomas. Braz J Med Biol Res 2010;43:799-805.
173. Venter JC, Adams MD, MyersEW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA et al. The sequence of the human genome. Science 2001; 291:1304-1351.
174. Vigano P, Somigliana E, Panina P, Rabellotti E, Vercellini P, Candiani M. Principles of phenomics in endometriosis. Hum Reprod Update 2012;18:248-259.
175. Vilella F, Ramirez LB, Simon C. Lipidomics as an emerging tool to predict endometrial receptivity. Fertil Steril 2013.
176. Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 2013;41:D1063-D1069.
177. Vouk K, Hevir N, Ribic-Pucelj M, Haarpaintner G, Scherb H, Osredkar J, Moller G, Prehn C, Rizner TL, Adamski J. Discovery of phosphatidylcholines and sphingomyelins as biomarkers for ovarian endometriosis. Hum Reprod 2012; 27:2955-2965.
178. Weeraratna AT, Taub DD. Microarray data analysis: an overview of design, methodology, and analysis. Methods Mol Biol 2007;377:1-16.
179. Weichenhan D, Plass C. The evolving epigenome. Human Mol Genet 2013; in press.
180. Weimar CH, Kavelaars A, Brosens JJ, Gellersen B, de Vreeden-Elbertse JM, Heijnen CJ, Macklon NS. Endometrial stromal cells of women with recurrent miscarriage fail to discriminate between high- and low-quality human embryos. PLoS ONE 2012; 7:e41424.
181. Weinstein JN. Searching for pharmacogenomic markers: the synergy between omic and hypothesis-driven research. Dis Markers 2001;17:77-88.
182. Wells D, Levy B. Cytogenetics in reproductive medicine: the contribution of comparative genomic hybridization (CGH). BioEssays 2003;25:289-300.
183. Werner T. Next generation sequencing allows deeper analysis and understanding of genomes and transcriptomes including aspects to fertility. Reprod Fertil Dev 2011; 23:75-80.
184. WestonAD,Hood L. Systems biology, proteomics, and the future of health care: toward predictive, preventative, and personalized medicine. J Proteome Res 2004;3:179-196.
185. White CA, Salamonsen LA. A guide to issues in microarray analysis: application to endometrial biology. Reproduction 2005;130:1-13.
186. Wilcox AJ, Baird DD,Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med 1999;340:1796-1799.
187. Wishart DS. Computational approaches to metabolomics. Methods Mol Biol 2010; 593:283-313.
188. Wu Y, Strawn E, Basir Z, Wang Y, Halverson G, Jailwala P, Guo SW. Genomic alterations in ectopic and eutopic endometria of women with endometriosis. Gynecol Obstet Invest 2006;62:148-159.
189. WuJM,Ward RM, Allen-Brady KL, Edwards TL, Norton PA, Hartmann KE, Hauser ER, Edwards DR. Phenotyping clinical disorders: lessons learned from pelvic organ prolapse. Am J Obstet Gynecol 2013;208:360-365.
190. Yamada N, Nishida Y, Tsutsumida H, Hamada T, Goto M, Higashi M, Nomoto M, Yonezawa S. MUC1 expression is regulated by DNA methylation and histone H3 lysine 9 modification in cancer cells. Cancer Res 2008;68:2708-2716.
191. Yanaihara A, Otsuka Y, Iwasaki S, Aida T, Tachikawa T, Irie T, Okai T. Differences in gene expression in the proliferative human endometrium. Fertil Steril 2005; 83(Suppl. 1):1206-1215.
192. Yang H, Zhou B, Prinz M, Siegel D. Proteomic analysis of menstrual blood. Mol Cell Proteomics 2012;11:1024-1035.
193. Yin JQ, Zhao RC, Morris KV. Profiling microRNA expression with microarrays. Trends Biotechnol 2008;26:70-76.
194. Zelenko Z, Aghajanova L, Irwin JC, Giudice LC. Nuclear receptor, coregulator signaling, and chromatin remodeling pathways suggest involvement of the epigenome in the steroid hormone response of endometrium and abnormalities in endometriosis. Reprod Sci 2012;19:152-162.
195. ZhangY, Szustakowski J, Schinke M. Bioinformatics analysis of microarray data. Methods Mol Biol 2009;573:259-284.
196. Zhang D, Sun C, Ma C, Dai H, ZhangW. Data mining of spatial-temporal expression of genes in the human endometrium during the window of implantation. Reprod Sci 2012;19:1085-1098.