OMICS: Current and future perspectives in reproductive medicine and technology

Journal of Human Reproductive Sciences

Volumn 7, Issue 2, 2014, Pages 73-92

  Egea, Rocío Rivera ^a   Puchalt, Nicolás Garrido ^a   Escrivá, Marcos Meseguer ^b   Varghese, Alex C ^c  

^a Andrology Laboratory and Semen Bank   (Spain)

^b Instituto Universitario IVI   (Spain)

^c Dispur College   (India)

Author keywords

Biotechnological technologies; molecular biomarkers; OMICS; reproductive medicine

Indexed keywords

CUMULUS CELL; EMBRYO DEVELOPMENT; ENDOMETRIUM; EPIGENETICS; GENOMICS; GERM CELL; GRANULOSA CELL; HUMAN; INFERTILITY THERAPY; METABOLOMICS; OOCYTE; PLACENTA; PROTEOMICS; REPRODUCTION; REPRODUCTIVE SUCCESS; REVIEW; SPERMATOZOON; TRANSCRIPTOMICS;

EID: 84907006747     PISSN: 09741208     EISSN: 19984766     Source Type: Journal    
DOI: 10.4103/0974-1208.138857     Document Type: Review

References (178)

1. Varghese AC, Goldberg E, Bhattacharyya AK, Agarwal A. Emerging technologies for the molecular study of infertility, and potential clinical applications. Reprod Biomed Online 2007;15:451-6.
2. Garrido N, Remohí J, Martínez-Conejero JA, García-Herrero S, Pellicer A, Meseguer M. Contribution of sperm molecular features to embryo quality and assisted reproduction success. Reprod Biomed Online 2008;17:855-65.
3. Silvestri E, Lombardi A, de Lange P, Glinni D, Senese R, Cioffi F, et al. Studies of complex biological systems with applications to molecular medicine: The need to integrate transcriptomic and proteomic approaches. J Biomed Biotechnol 2011;2011:810242.
4. Waddington CH. The epigenotype. 1942. Int J Epidemiol 2012;41:10-3.
5. Katz-Jaffe MG, Gardner DK. Symposium: Innovative techniques in human embryo viability assessment. Can proteomics help to shape the future of human assisted conception? Reprod Biomed Online 2008;17:497-501.
6. Navarro-Costa P, Nogueira P, Carvalho M, Leal F, Cordeiro I, Calhaz-Jorge C, et al. Incorrect DNA methylation of the DAZL promoter CpG island associates with defective human sperm. Hum Reprod 2010;25:2647-54.
7. Hammoud SS, Nix DA, Hammoud AO, Gibson M, Cairns BR, Carrell DT. Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Hum Reprod 2011;26:2558-69.
8. Boissonnas CC, Abdalaoui HE, Haelewyn V, Fauque P, Dupont JM, Gut I, et al. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Hum Genet 2010;18:73-80.
9. Camprubí C, Pladevall M, Grossmann M, Garrido N, Pons MC, Blanco J. Semen samples showing an increased rate of spermatozoa with imprinting errors have a negligible effect in the outcome of assisted reproduction techniques. Epigenetics 2012;7:1115-24.
10. El Hajj N, Zechner U, Schneider E, Tresch A, Gromoll J, Hahn T, et al. Methylation status of imprinted genes and repetitive elements in sperm DNA from infertile males. Sex Dev 2011;5:60-9.
11. Barbash-Hazan S, Frumkin T, Malcov M, Yaron Y, Cohen T, Azem F, et al. Preimplantation aneuploid embryos undergo self-correction in correlation with their developmental potential. Fertil Steril 2009;92:890-6.
12. Wilton L. Preimplantation genetic diagnosis and chromosome analysis of blastomeres using comparative genomic hybridization. Hum Reprod Update 2005;11:33-41.
13. Voullaire L, Slater H, Williamson R, Wilton L. Chromosome analysis of blastomeres from human embryos by using comparative genomic hybridization. Hum Genet 2000;106:210-7.
14. Schoolcraft WB, Fragouli E, Stevens J, Munne S, Katz-Jaffe MG, Wells D. Clinical application of comprehensive chromosomal screening at the blastocyst stage. Fertil Steril 2010;94:1700-6.
15. Geraedts J, Collins J, Gianaroli L, Goossens V, Handyside A, Harper J, et al. What next for preimplantation genetic screening? A polar body approach! Hum Reprod 2010;25:575-7.
16. Treff NR, Su J, Kasabwala N, Tao X, Miller KA, Scott RT Jr. Robust embryo identification using first polar body single nucleotide polymorphism microarray-based DNA fingerprinting. Fertil Steril 2010;93:2453-5.
17. Treff NR, Su J, Tao X, Levy B, Scott RT Jr. Accurate single cell 24 chromosome aneuploidy screening using whole genome amplification and single nucleotide polymorphism microarrays. Fertil Steril 2010;94:2017-21.
18. Treff NR, Northrop LE, Kasabwala K, Su J, Levy B, Scott RT Jr. Single nucleotide polymorphism microarray-based concurrent screening of 24-chromosome aneuploidy and unbalanced translocations in preimplantation human embryos. Fertil Steril 2011;95:1606-121.
19. García-Herrero S, Meseguer M, Martínez-Conejero JA, Remohí J, Pellicer A, Garrido N. The transcriptome of spermatozoa used in homologous intrauterine insemination varies considerably between samples that achieve pregnancy and those that do not. Fertil Steril 2010;94:1360-73.
20. García-Herrero S, Garrido N, Martínez-Conejero JA, Remohí J, Pellicer A, Meseguer M. Ontological evaluation of transcriptional differences between sperm of infertile males and fertile donors using microarray analysis. J Assist Reprod Genet 2010;27:111-20.
21. García-Herrero S, Garrido N, Martínez-Conejero JA, Remohí J, Pellicer A, Meseguer M. Differential transcriptomic profile in spermatozoa achieving pregnancy or not via ICSI. Reprod Biomed Online 2011;22:25-36.
22. Garcia-Herrero S, Garrido N, Martinez-Conejero JA, Remohi J, Pellicer A, Meseguer M. Profound transcriptomic differences found between sperm samples from sperm donors vs. patients undergoing (Artificial Reproductive Techniques) tends to disappear after swim-up sperm preparation technique. Int J Fertil Steril 2010;4:114-21.
23. Bonache S, Mata A, Ramos MD, Bassas L, Larriba S. Sperm gene expression profile is related to pregnancy rate after insemination and is predictive of low fecundity in normozoospermic men. Hum Reprod 2012;27:1556-67.
24. Ouandaogo ZG, Frydman N, Hesters L, Assou S, Haouzi D, Dechaud H, et al. Differences in transcriptomic profiles of human cumulus cells isolated from oocytes at GV, MI and MII stages after in vivo and in vitro oocyte maturation. Hum Reprod 2012;27:2438-47.
25. Fragouli E, Wells D. Transcriptomic analysis of follicular cells provides information on the chromosomal status and competence of unfertilized oocytes. Expert Rev Mol Diagn 2012;12:1-4.
26. Assou S, Boumela I, Haouzi D, Monzo C, Dechaud H, Kadoch IJ, et al. Transcriptome analysis during human trophectoderm specification suggests new roles of metabolic and epigenetic genes. PLoS One 2012;7:e39306.
27. Fox MS, Ares VX, Turek PJ, Haqq C, Reijo Pera RA. Feasibility of global gene expression analysis in testicular biopsies from infertile men. Mol Reprod Dev 2003;66:403-21.
28. Oliva R, de Mateo S, Estanyol JM. Sperm cell proteomics. Proteomics 2009;9:1004-17.
29. Rolland AD, Lavigne R, Dauly C, Calvel P, Kervarrec C, Freour T, et al. Identification of genital tract markers in the human seminal plasma using an integrative genomics approach. Hum Reprod 2013;28:199-209.
30. de Mateo S, Martínez-Heredia J, Estanyol JM, Domínguez-Fandos D, Vidal-Taboada JM, Ballescà JL, et al. Marked correlations in protein expression identified by proteomic analysis of human spermatozoa. Proteomics 2007;7:4264-77.
31. Pixton KL, Deeks ED, Flesch FM, Moseley FL, Björndahl L, Ashton PR, et al. Sperm proteome mapping of a patient who experienced failed fertilization at IVF reveals altered expression of at least 20 proteins compared with fertile donors: Case report. Hum Reprod 2004;19:1438-47.
32. du Plessis SS, Kashou AH, Benjamin DJ, Yadav SP, Agarwal A. Proteomics: A subcellular look at spermatozoa. Reprod Biol Endocrinol 2011;9:36.
33. Li J, Tan Z, Li M, Xia T, Liu P, Yu W. Proteomic analysis of endometrium in fertile women during the prereceptive and receptive phases after luteinizing hormone surge. Fertil Steril 2011;95:1161-3.
34. Cortezzi SS, Garcia JS, Ferreira CR, Braga DP, Figueira RC, Iaconelli A Jr, et al. Secretome of the preimplantation human embryo by bottom-up label-free proteomics. Anal Bioanal Chem 2011;401:1331-9.
35. Twigt J, Steegers-Theunissen RP, Bezstarosti K, Demmers JA. Proteomic analysis of the microenvironment of developing oocytes. Proteomics 2012;12:1463-71.
36. Zhang P, Ni X, Guo Y, Guo X, Wang Y, Zhou Z, et al. Proteomic-based identification of maternal proteins in mature mouse oocytes. BMC Genomics 2009;10:348.
37. Garrido-Gomez T, Dominguez F, Lopez JA, Camafeita E, Quiñonero A, Martinez-Conejero JA, et al. Modeling human endometrial decidualization from the interaction between proteome and secretome. J Clin Endocrinol Metab 2011;96:706-16.
38. Thacker S, Yadav SP, Sharma RK, Kashou A, Willard B, Zhang D, et al. Evaluation of sperm proteins in infertile men: A proteomic approach. Fertil Steril 2011;95:2745-8.
39. Brosens JJ, Hodgetts A, Feroze-Zaidi F, Sherwin JR, Fusi L, Salker MS, et al. Proteomic analysis of endometrium from fertile and infertile patients suggests a role for apolipoprotein A-I in embryo implantation failure and endometriosis. Mol Hum Reprod 2010;16:273-85.
40. Brison DR, Houghton FD, Falconer D, Roberts SA, Hawkhead J, Humpherson PG, et al. Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod 2004;19:2319-24.
41. Scott R, Seli E, Miller K, Sakkas D, Scott K, Burns DH. Noninvasive metabolomic profiling of human embryo culture media using Raman spectroscopy predicts embryonic reproductive potential: A prospective blinded pilot study. Fertil Steril 2008;90:77-83.
42. Nagy ZP, Sakkas D, Behr B. Symposium: Innovative techniques in human embryo viability assessment. Non-invasive assessment of embryo viability by metabolomic profiling of culture media ('metabolomics'). Reprod Biomed Online 2008;17:502-7.
43. Seli E, Botros L, Sakkas D, Burns DH. Noninvasive metabolomic profiling of embryo culture media using proton nuclear magnetic resonance correlates with reproductive potential of embryos in women undergoing in vitro fertilization. Fertil Steril 2008;90:2183-9.
44. Díaz-Gimeno P, Horcajadas JA, Martínez-Conejero JA, Esteban FJ, Alamá P, Pellicer A, et al. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril 2011;95:50-60, 60.e1-15.
45. Jarkovska K, Kupcova Skalnikova H, Halada P, Hrabakova R, Moos J, Rezabek K, et al. Development of ovarian hyperstimulation syndrome: Interrogation of key proteins and biological processes in human follicular fluid of women undergoing in vitro fertilization. Mol Hum Reprod 2011;17:679-92.
46. Estes SJ, Ye B, Qiu W, Cramer D, Hornstein MD, Missmer SA. A proteomic analysis of IVF follicular fluid in women
47. Singh K, Jaiswal D. Human male infertility: A complex multifactorial phenotype. Reprod Sci 2011;18:418-25.
48. Zama AM, Uzumcu M. Epigenetic effects of endocrine-disrupting chemicals on female reproduction: An ovarian perspective. Front Neuroendocrinol 2010;31:420-39.
49. Iliadou AN, Janson PC, Cnattingius S. Epigenetics and assisted reproductive technology. J Intern Med 2011;270:414-20.
50. van Montfoort AP, Hanssen LL, de Sutter P, Viville S, Geraedts JP, de Boer P. Assisted reproduction treatment and epigenetic inheritance. Hum Reprod Update 2012;18:171-97.
51. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007;447:407-12.
52. Odom LN, Segars J. Imprinting disorders and assisted reproductive technology. Curr Opin Endocrinol Diabetes Obes 2010;17:517-22.
53. Stouder C, Paoloni-Giacobino A. Specific transgenerational imprinting effects of the endocrine disruptor methoxychlor on male gametes. Reproduction 2011;141:207-16.
54. Suter MA, Aagaard K. What changes in DNA methylation take place in individuals exposed to maternal smoking in utero? Epigenomics 2012;4:115-8.
55. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 2007;22:26-35.
56. Geuns E, De Temmerman N, Hilven P, Van Steirteghem A, Liebaers I, De Rycke M. Methylation analysis of the intergenic differentially methylated region of DLK1-GTL2 in human. Eur J Hum Genet 2007;15:352-61.
57. Godmann M, Lambrot R, Kimmins S. The dynamic epigenetic program in male germ cells: Its role in spermatogenesis, testis cancer, and its response to the environment. Microsc Res Tech 2009;72:603-19.
58. Roeleveld N, Bretveld R. The impact of pesticides on male fertility. Curr Opin Obstet Gynecol 2008;20:229-33.
59. Vigodner M, Shrivastava V, Gutstein LE, Schneider J, Nieves E, Goldstein M, et al. Localization and identification of sumoylated proteins in human sperm: Excessive sumoylation is a marker of defective spermatozoa. Hum Reprod 2013;28:210-23.
60. Lefièvre L, Chen Y, Conner SJ, Scott JL, Publicover SJ, Ford WC, et al. Human spermatozoa contain multiple targets for protein S-nitrosylation: An alternative mechanism of the modulation of sperm function by nitric oxide? Proteomics 2007;7:3066-84.
61. Sutovsky P, Terada Y, Schatten G. Ubiquitin-based sperm assay for the diagnosis of male factor infertility. Hum Reprod 2001;16:250-8.
62. Fulka H, Mrazek M, Tepla O, Fulka J Jr. DNA methylation pattern in human zygotes and developing embryos. Reproduction 2004;128:703-8.
63. Santos F, Hyslop L, Stojkovic P, Leary C, Murdoch A, Reik W, et al. Evaluation of epigenetic marks in human embryos derived from IVF and ICSI. Hum Reprod 2010;25:2387-95.
64. Small KS, Hedman AK, Grundberg E, Nica AC, Thorleifsson G, Kong A, et al. Identification of an imprinted master trans regulator at the KLF14 locus related to multiple metabolic phenotypes. Nat Genet 2011;43:561-4.
65. Banno K, Kisu I, Yanokura M, Masuda K, Ueki A, Kobayashi Y, et al. Epigenetics and genetics in endometrial cancer: New carcinogenic mechanisms and relationship with clinical practice. Epigenomics 2012;4:147-62.
66. Munné S, Alikani M, Tomkin G, Grifo J, Cohen J. Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities. Fertil Steril 1995;64:382-91.
67. Dailey T, Dale B, Cohen J, Munné S. Association between nondisjunction and maternal age in meiosis-II human oocytes. Am J Hum Genet 1996;59:176-84.
68. Munné S, Chen S, Colls P, Garrisi J, Zheng X, Cekleniak N, et al. Maternal age, morphology, development and chromosome abnormalities in over 6000 cleavage-stage embryos. Reprod Biomed Online 2007;14:628-34.
69. Thornhill AR, de Die-Smulders CE, Geraedts JP, Harper JC, Harton GL, Lavery SA, et al. ESHRE PGD Consortium 'Best practice guidelines for clinical preimplantation genetic diagnosis (PGD) and preimplantation genetic screening (PGS)'. Hum Reprod 2005;20:35-48.
70. Practice Committee of Society for Assisted Reproductive Technology, Practice Committee of American Society for Reproductive Medicine. Preimplantation genetic testing: A Practice Committee opinion. Fertil Steril 2008;90:S136-43.
71. Harper J, Coonen E, De Rycke M, Fiorentino F, Geraedts J, Goossens V, et al. What next for preimplantation genetic screening (PGS)? A position statement from the ESHRE PGD Consortium Steering Committee. Hum Reprod 2010;25:821-3.
72. Sher G, Keskintepe L, Keskintepe M, Maassarani G, Tortoriello D, Brody S. Genetic analysis of human embryos by metaphase comparative genomic hybridization (mCGH) improves efficiency of IVF by increasing embryo implantation rate and reducing multiple pregnancies and spontaneous miscarriages. Fertil Steril 2009;92:1886-94.
73. van Echten-Arends J, Mastenbroek S, Sikkema-Raddatz B, Korevaar JC, Heineman MJ, van der Veen F, et al. Chromosomal mosaicism in human preimplantation embryos: A systematic review. Hum Reprod Update 2011;17:620-7.
74. Bielanska M, Tan SL, Ao A. Chromosomal mosaicism throughout human preimplantation development in vitro: Incidence, type, and relevance to embryo outcome. Hum Reprod 2002;17:413-9.
75. Dupont C, Segars J, De Cherney A, Bavister BD, Armant DR, Brenner CA. Incidence of chromosomal mosaicism in morphologically normal nonhuman primate preimplantation embryos. Fertil Steril 2010;93:2545-50.
76. Geraedts J, Montag M, Magli MC, Repping S, Handyside A, Staessen C, et al. Polar body array CGH for prediction of the status of the corresponding oocyte. Part I: Clinical results. Hum Reprod 2011;26:3173-80.
77. Magli MC, Montag M, Köster M, Muzi L, Geraedts J, Collins J, et al. Polar body array CGH for prediction of the status of the corresponding oocyte. Part II: Technical aspects. Hum Reprod 2011;26:3181-5.
78. Wells D, Delhanty JD. Comprehensive chromosomal analysis of human preimplantation embryos using whole genome amplification and single cell comparative genomic hybridization. Mol Hum Reprod 2000;6:1055-62.
79. Dean FB, Hosono S, Fang L, Wu X, Faruqi AF, Bray-Ward P, et al. Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci U S A 2002;99:5261-6.
80. Fiorentino F, Spizzichino L, Bono S, Biricik A, Kokkali G, Rienzi L, et al. PGD for reciprocal and Robertsonian translocations using array comparative genomic hybridization. Hum Reprod 2011;26:1925-35.
81. Brezina PR, Benner A, Rechitsky S, Kuliev A, Pomerantseva E, Pauling D, et al. Single-gene testing combined with single nucleotide polymorphism microarray preimplantation genetic diagnosis for aneuploidy: A novel approach in optimizing pregnancy outcome. Fertil Steril 2011;95:1786.e5-8.
82. Konstantinidis M. A novel tool for the assessment of IVF embryos. Hum Reprod (Oxford, England) 2011;26 Suppl 1:I24-6.
83. rd. Molecular abnormalities in oocytes from women with polycystic ovary syndrome revealed by microarray analysis. J Clin Endocrinol Metab 2007;92:705-13.
84. Biase FH, Everts RE, Oliveira R, Santos-Biase WK, Fonseca Merighe GK, Smith LC, et al. Messenger RNAs in metaphase II oocytes correlate with successful embryo development to the blastocyst stage. Zygote 2012;10:1-11.
85. Zhang X, Jafari N, Barnes RB, Confino E, Milad M, Kazer RR. Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil Steril 2005;83 Suppl 1:1169-79.
86. Inan MS, Al-Hassan S, Ozand P, Coskun S. Transcriptional profiling of granulosa cells from a patient with recurrent empty follicle syndrome. Reprod Biomed Online 2006;13:481-91.
87. Gasca S, Pellestor F, Assou S, Loup V, Anahory T, Dechaud H, et al. Identifying new human oocyte marker genes: A microarray approach. Reprod Biomed Online 2007;14:175-83.
88. McKenzie LJ, Pangas SA, Carson SA, Kovanci E, Cisneros P, Buster JE, et al. Human cumulus granulosa cell gene expression: A predictor of fertilization and embryo selection in women undergoing IVF. Hum Reprod 2004;19:2869-74.
89. Assidi M, Dufort I, Ali A, Hamel M, Algriany O, Dielemann S, et al. 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 2008;79:209-22.
90. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, et al. The human cumulus - Oocyte complex gene-expression profile. Hum Reprod 2006;21:1705-19.
91. Zheng P, Patel B, McMenamin M, Moran E, Paprocki AM, Kihara M, et al. Effects of follicle size and oocyte maturation conditions on maternal messenger RNA regulation and gene expression in rhesus monkey oocytes and embryos. Biol Reprod 2005;72:890-7.
92. Zheng P, Vassena R, Latham KE. Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signaling genes in rhesus monkey oocytes and preimplantation embryos. Mol Hum Reprod 2007;13:361-71.
93. Assou S, Haouzi D, De Vos J, Hamamah S. Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Mol Hum Reprod 2010;16:531-8.
94. Ouandaogo ZG, Haouzi D, Assou S, Dechaud H, Kadoch IJ, De Vos J, et al. Human cumulus cells molecular signature in relation to oocyte nuclear maturity stage. PLoS One 2011;6:e27179.
95. Kõks S, Velthut A, Sarapik A, Altmäe S, Reinmaa E, Schalkwyk LC, et al. The differential transcriptome and ontology profiles of floating and cumulus granulosa cells in stimulated human antral follicles. Mol Hum Reprod 2010;16:229-40.
96. Bettegowda A, Patel OV, Lee KB, Park KE, Salem M, Yao J, et al. Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: Functional and diagnostic implications. Biol Reprod 2008;79:301-9.
97. Assou S, Haouzi D, Mahmoud K, Aouacheria A, Guillemin Y, Pantesco V, et al. A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: A proof of concept study. Mol Hum Reprod 2008;14:711-9.
98. Gebhardt KM, Feil DK, Dunning KR, Lane M, Russell DL. Human cumulus cell gene expression as a biomarker of pregnancy outcome after single embryo transfer. Fertil Steril 2011;96:47-522.
99. Hamel M, Dufort I, Robert C, Gravel C, Leveille MC, Leader A, et al. Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod 2008;23:1118-27.
100. Huang Z, Wells D. The human oocyte and cumulus cells relationship: New insights from the cumulus cell transcriptome. Mol Hum Reprod 2010;16:715-25.
101. Fragouli E, Huang Z, Bianchi V. Follicle-specific predisposition to aneuploidy as revealed by transcriptomic analysis of cumulus cells. Hum Reprod 2011;26 Suppl 1:87.
102. Maman E, Yung Y, Kedem A, Yerushalmi GM, Konopnicki S, Cohen B, et al. High expression of luteinizing hormone receptors messenger RNA by human cumulus granulosa cells is in correlation with decreased fertilization. Fertil Steril 2012;97:592-8.
103. Li C, Zhou X. Gene transcripts in spermatozoa: Markers of male infertility. Clin Chim Acta 2012;413:1035-8.
104. Hamatani T. Human spermatozoal RNAs. Fertil Steril 2012;97:275-81.
105. Wang X, Zhao H, Andersson R. Proteomics and leukocytes: An approach to understanding potential molecular mechanisms of inflammatory responses. J Proteome Res 2004;3:921-9.
106. He Z, Chan WY, Dym M. Microarray technology offers a novel tool for the diagnosis and identification of therapeutic targets for male infertility. Reproduction 2006;132:11-9.
107. Boerke A, Dieleman SJ, Gadella BM. A possible role for sperm RNA in early embryo development. Theriogenology 2007;68 Suppl 1:S147-55.
108. Dadoune JP. Spermatozoal RNAs: What about their functions? Microsc Res Tech 2009;72:536-51.
109. Martins RP, Krawetz SA. RNA in human sperm. Asian J Androl 2005;7:115-20.
110. Miller D, Ostermeier GC. Towards a better understanding of RNA carriage by ejaculate spermatozoa. Hum Reprod Update 2006;12:757-67.
111. Guyonnet B, Dacheux F, Dacheux JL, Gatti JL. The epididymal transcriptome and proteome provide some insights into new epididymal regulations. J Androl 2011;32:651-64.
112. Hamatani T, Daikoku T, Wang H, Matsumoto H, Carter MG, Ko MS, et al. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc Natl Acad Sci U S A 2004;101:10326-31.
113. Wang H, Ding T, Brown N, Yamamoto Y, Prince LS, Reese J, et al. Zonula occludens-1 (ZO-1) is involved in morula to blastocyst transformation in the mouse. Dev Biol 2008;318:112-25.
114. Cui XS, Li XY, Shen XH, Bae YJ, Kang JJ, Kim NH. Transcription profile in mouse four-cell, morula, and blastocyst: Genes implicated in compaction and blastocoel formation. Mol Reprod Dev 2007;74:133-43.
115. de A Camargo LS, Powell AM, do Vale Filho VR, Wall RJ. Comparison of gene expression in individual preimplantation bovine embryos produced by in vitro fertilisation or somatic cell nuclear transfer. Reprod Fertil Dev 2005;17:487-96.
116. Wrenzycki C, Herrmann D, Lucas-Hahn A, Korsawe K, Lemme E, Niemann H. Messenger RNA expression patterns in bovine embryos derived from in vitro procedures and their implications for development. Reprod Fertil Dev 2005;17:23-35.
117. Smith SL, Everts RE, Tian XC, Du F, Sung LY, Rodriguez-Zas SL, et al. Global gene expression profiles reveal significant nuclear reprogramming by the blastocyst stage after cloning. Proc Natl Acad Sci U S A 2005;102:17582-7.
118. Jones GM, Cram DS, Song B, Kokkali G, Pantos K, Trounson AO. Novel strategy with potential to identify developmentally competent IVF blastocysts. Hum Reprod 2008;23:1748-59.
119. El-Sayed A, Hoelker M, Rings F, Salilew D, Jennen D, Tholen E, et al. Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiol Genomics 2006;28:84-96.
120. Salilew-Wondim D, Schellander K, Hoelker M, Tesfaye D. Oviductal, endometrial and embryonic gene expression patterns as molecular clues for pregnancy establishment. Anim Reprod Sci 2012;134:9-18.
121. Ruiz-Alonso M, Blesa D, Simón C. The genomics of the human endometrium. Biochim Biophys Acta 2012;1822:1931-42.
122. Díaz-Gimeno P, Ruiz-Alonso M, Blesa D, Bosch N, Martínez-Conejero JA, Alamá P, et al. The accuracy and reproducibility of the endometrial receptivity array is superior to histology as a diagnostic method for endometrial receptivity. Fertil Steril 2013;99:508-17.
123. Haouzi D, Dechaud H, Assou S, Monzo C, de Vos J, Hamamah S. Transcriptome analysis reveals dialogues between human trophectoderm and endometrial cells during the implantation period. Hum Reprod 2011;26:1440-9.
124. Murray MJ, Meyer WR, Zaino RJ, Lessey BA, Novotny DB, Ireland K, et al. A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women. Fertil Steril 2004;81:1333-43.
125. Talbi S, Hamilton AE, Vo KC, Tulac S, Overgaard MT, Dosiou C, et al. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 2006;147:1097-121.
126. Verrills NM. Clinical proteomics: Present and future prospects. Clin Biochem Rev 2006;27:99-116.
127. Seli E, Robert C, Sirard MA. OMICS in assisted reproduction: Possibilities and pitfalls. Mol Hum Reprod 2010;16:513-30.
128. 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.
129. Meng Y, Liu XH, Ma X, Shen Y, Fan L, Leng J, et al. The protein profile of mouse mature cumulus-oocyte complex. Biochim Biophys Acta 2007;1774:1477-90.
130. Ma M, Guo X, Wang F, Zhao C, Liu Z, Shi Z, et al. Protein expression profile of the mouse metaphase-II oocyte. J Proteome Res 2008;7:4821-30.
131. Pfeiffer MJ, Siatkowski M, Paudel Y, Balbach ST, Baeumer N, Crosetto N, et al. Proteomic analysis of mouse oocytes reveals 28 candidate factors of the "reprogrammome". J Proteome Res 2011;10:2140-53.
132. Royère D, Feuerstein P, Cadoret V, Puard V, Uzbekova S, Dalbies-Tran R, et al. Non invasive assessment of embryo quality: Proteomics, metabolomics and oocyte-cumulus dialogue. Gynecol Obstet Fertil 2009;37:917-20.
133. McReynolds S, Dzieciatkowska M, McCallie BR, Mitchell SD, Stevens J, Hansen K, et al. Impact of maternal aging on the molecular signature of human cumulus cells. Fertil Steril 2012;98:1574-805.
134. Kushnir MM, Naessén T, Wanggren K, Rockwood AL, Crockett DK, Bergquist J. Protein and steroid profiles in follicular fluid after ovarian hyperstimulation as potential biomarkers of IVF outcome. J Proteome Res 2012;11:5090-100.
135. Dai G, Lu G. Different protein expression patterns associated with polycystic ovary syndrome in human follicular fluid during controlled ovarian hyperstimulation. Reprod Fertil Dev 2012;24:893-904.
136. Martínez-Heredia J, de Mateo S, Vidal-Taboada JM, Ballescà JL, Oliva R. Identification of proteomic differences in asthenozoospermic sperm samples. Hum Reprod 2008;23:783-91.
137. Botta T, Blescia S, Martinez-Heredia J, Lafuente R, Brassesco M, Ballesca JL, et al. Identification of proteomic differences in oligozoospermic sperm samples. Rev Int Androl 2009;7:14-9.
138. Zylbersztejn DS, Andreoni C, Del Giudice PT, Spaine DM, Borsari L, Souza GH, et al. Proteomic analysis of seminal plasma in adolescents with and without varicocele. Fertil Steril 2013;99:92-8.
139. Fu-Jun L, Xiao-Fang S. Comparative analysis of human reproductive proteomes identifies candidate proteins of sperm maturation. Mol Biol Rep 2012;39:10257-63.
140. Katz-Jaffe MG, Gardner DK, Schoolcraft WB. Proteomic analysis of individual human embryos to identify novel biomarkers of development and viability. Fertil Steril 2006;85:101-7.
141. Katz-Jaffe MG, Linck DW, Schoolcraft WB, Gardner DK. A proteomic analysis of mammalian preimplantation embryonic development. Reproduction 2005;130:899-905.
142. Katz-Jaffe MG, Gardner DK. Embryology in the era of proteomics. Theriogenology 2007;68 Suppl 1:S125-30.
143. Katz-Jaffe MG, McReynolds S, Gardner DK, Schoolcraft WB. The role of proteomics in defining the human embryonic secretome. Mol Hum Reprod 2009;15:271-7.
144. Domínguez F, Gadea B, Esteban FJ, Horcajadas JA, Pellicer A, Simón C. Comparative protein-profile analysis of implanted versus non-implanted human blastocysts. Hum Reprod 2008;23:1993-2000.
145. O'Neill C. The role of paf in embryo physiology. Hum Reprod Update 2005;11:215-28.
146. Cervero A, Horcajadas JA, Domínguez F, Pellicer A, Simón C. Leptin system in embryo development and implantation: A protein in search of a function. Reprod Biomed Online 2005;10:217-23.
147. Balakier H, Xiao R, Zhao J, Zaver S, Dziak E, Szczepanska K, et al. Expression of survivin in human oocytes and preimplantation embryos. Fertil Steril 2013;99:518-25.
148. Warner CM, Lampton PW, Newmark JA, Cohen J. Symposium: Innovative techniques in human embryo viability assessment. Soluble human leukocyte antigen-G and pregnancy success. Reprod Biomed Online 2008;17:470-85.
149. Yao YQ, Barlow DH, Sargent IL. Differential expression of alternatively spliced transcripts of HLA-G in human preimplantation embryos and inner cell masses. J Immunol 2005;175:8379-85.
150. Vercammen MJ, Verloes A, Van de Velde H, Haentjens P. Accuracy of soluble human leukocyte antigen-G for predicting pregnancy among women undergoing infertility treatment: Meta-analysis. Hum Reprod Update 2008;14:209-18.
151. Dominguez F, Gadea B, Mercader A, Esteban FJ, Pellicer A, Simón C. Embryologic outcome and secretome profile of implanted blastocysts obtained after coculture in human endometrial epithelial cells versus the sequential system. Fertil Steril 2010;93:774-7821.
152. Scott RT Jr, Treff NR. Assessing the reproductive competence of individual embryos: A proposal for the validation of new "-omics" technologies. Fertil Steril 2010;94:791-4.
153. Domínguez F, Garrido-Gomez T, López JA, Camafeita E, Quiñonero A, Pellicer A, et al. 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;24:2607-17.
154. Rai P, Kota V, Sundaram CS, Deendayal M, Shivaji S. Proteome of human endometrium: Identification of differentially expressed proteins in proliferative and secretory phase endometrium. Proteomics Clin Appl 2010;4:48-59.
155. Fowler PA, Tattum J, Bhattacharya S, Klonisch T, Hombach-Klonisch S, Gazvani R, et al. An investigation of the effects of endometriosis on the proteome of human eutopic endometrium: A heterogeneous tissue with a complex disease. Proteomics 2007;7:130-42.
156. Habermann JK, Bündgen NK, Gemoll T, Hautaniemi S, Lundgren C, Wangsa D, et al. Genomic instability influences the transcriptome and proteome in endometrial cancer subtypes. Mol Cancer 2011;10:132.
157. Salamonsen LA, Edgell T, Rombauts LJ, Stephens AN, Robertson DM, Rainczuk A, et al. Proteomics of the human endometrium and uterine fluid: A pathway to biomarker discovery. Fertil Steril 2013;99:1086-92.
158. Brison DR, Hollywood K, Arnesen R, Goodacre R. Predicting human embryo viability: The road to non-invasive analysis of the secretome using metabolic footprinting. Reprod Biomed Online 2007;15:296-302.
159. Singh R, Sinclair KD. Metabolomics: Approaches to assessing oocyte and embryo quality. Theriogenology 2007;68 Suppl 1:S56-62.
160. Deepinder F, Chowdary HT, Agarwal A. Role of metabolomic analysis of biomarkers in the management of male infertility. Expert Rev Mol Diagn 2007;7:351-8.
161. Gupta A, Mahdi AA, Ahmad MK, Shukla KK, Jaiswer SP, Shankhwar SN. 1H NMR spectroscopic studies on human seminal plasma: A probative discriminant function analysis classification model. J Pharm Biomed Anal 2011;54:106-13.
162. Seli E, Sakkas D, Scott R, Kwok SC, Rosendahl SM, Burns DH. Noninvasive metabolomic profiling of embryo culture media using Raman and near-infrared spectroscopy correlates with reproductive potential of embryos in women undergoing in vitro fertilization. Fertil Steril 2007;88:1350-7.
163. Vergouw CG, Botros LL, Roos P, Lens JW, Schats R, Hompes PG, et al. Metabolomic profiling by near-infrared spectroscopy as a tool to assess embryo viability: A novel, non-invasive method for embryo selection. Hum Reprod 2008;23:1499-504.
164. Reese J, Zhao X, Ma WG, Brown N, Maziasz TJ, Dey SK. Comparative analysis of pharmacologic and/or genetic disruption of cyclooxygenase-1 and cyclooxygenase-2 function in female reproduction in mice. Endocrinology 2001;142:3198-206.
165. Wang H, Dey SK. Lipid signaling in embryo implantation. Prostaglandins Other Lipid Mediat 2005;77:84-102.
166. Achache H, Tsafrir A, Prus D, Reich R, Revel A. Defective endometrial prostaglandin synthesis identified in patients with repeated implantation failure undergoing in vitro fertilization. Fertil Steril 2010;94:1271-8.
167. Downie J, Poyser NL, Wunderlich M. Levels of prostaglandins in human endometrium during the normal menstrual cycle. J Physiol 1974;236:465-72.
168. Aghajanova L. Leukemia inhibitory factor and human embryo implantation. Ann N Y Acad Sci 2004;1034:176-83.
169. Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P. Follicular fluid content and oocyte quality: From single biochemical markers to metabolomics. Reprod Biol Endocrinol 2009;7:40.
170. Thomas N, Goodacre R, Timmins EM, Gaudoin M, Fleming R. Fourier transform infrared spectroscopy of follicular fluids from large and small antral follicles. Hum Reprod 2000;15:1667-71.
171. Wallace M, Cottell E, Gibney MJ, McAuliffe FM, Wingfield M, Brennan L. An investigation into the relationship between the metabolic profile of follicular fluid, oocyte developmental potential, and implantation outcome. Fertil Steril 2012;97:1078-841.
172. Piñero-Sagredo E, Nunes S, de Los Santos MJ, Celda B, Esteve V. NMR metabolic profile of human follicular fluid. NMR Biomed 2010;23:485-95.
173. Pacella L, Zander-Fox DL, Armstrong DT, Lane M. Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment. Fertil Steril 2012;98:986-41.
174. Valckx SD, De Pauw I, De Neubourg D, Inion I, Berth M, Fransen E, et al. BMI-related metabolic composition of the follicular fluid of women undergoing assisted reproductive treatment and the consequences for oocyte and embryo quality. Hum Reprod 2012;27:3531-9.
175. Nagy ZP, Jones-Colon S, Roos P, Botros L, Greco E, Dasig J, et al. Metabolomic assessment of oocyte viability. Reprod Biomed Online 2009;18:219-25.
176. Lane M, Gardner DK. Selection of viable mouse blastocysts prior to transfer using a metabolic criterion. Hum Reprod 1996;11:1975-8.
177. Sturmey RG, Brison DR, Leese HJ. Symposium: Innovative techniques in human embryo viability assessment. Assessing embryo viability by measurement of amino acid turnover. Reprod Biomed Online 2008;17:486-96.
178. Haggarty P, Wood M, Ferguson E, Hoad G, Srikantharajah A, Milne E, et al. Fatty acid metabolism in human preimplantation embryos. Hum Reprod 2006;21:766-73.