Developmental exposure of fetal ovaries and fetal germ cells to endometriosis in an endometriosis model causes differential gene expression in the preimplantation embryos of the first-generation and second-generation embryos

Fertility and Sterility

Volumn 100, Issue 5, 2013, Pages 1436-1443

  Birt, Julie A ^a,b   Taylor, Kristen H ^a   Davis, J Wade ^a,b   Sharpe Timms, Kathy L ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Apoptosis; embryo; endometriosis; genome analysis; multigenerational

Indexed keywords

APOPTOTIC PEPTIDASE ACTIVATOR FACTOR 1; CARBAMOYL PHOSPHATE SYNTHASE (GLUTAMINE HYDROLYSING); CASPASE 3; DNAJA3 PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NUCLEAR FACTOR KAPPA LIGHT POLYPEPTIDE GENE ENHANCER IN B CELLS INHIBITOR ALPHA; PROTEIN DNAJ; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CYCLE; CONTROLLED STUDY; EMBRYO; ENDOMETRIOSIS; FEMALE; GENE EXPRESSION; GENOME ANALYSIS; GERM CELL; NONHUMAN; OVARY; OXIDATIVE STRESS; PREIMPLANTATION EMBRYO; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; RNA PROCESSING;

APOPTOSIS; EMBRYO; ENDOMETRIOSIS; GENOME ANALYSIS; MULTIGENERATIONAL;

ANIMALS; APOPTOSIS; BLASTOCYST; CELL CYCLE; DISEASE MODELS, ANIMAL; ENDOMETRIOSIS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC PREDISPOSITION TO DISEASE; GERM CELLS; GESTATIONAL AGE; HEREDITY; OVARY; OXIDATIVE STRESS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER;

EID: 84887111816     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2013.07.007     Document Type: Article

References (58)

1. C. Allaire Endometriosis and infertility: a review J Reprod Med 51 2006 164 168
2. H. Stefansson, R.T. Geirsson, V. Steinthorsdottir, H. Jonsson, A. Manolescu, A. Kong, G. Ingadottir, J. Gulcher, and K. Stefansson Genetic factors contribute to the risk of developing endometriosis Hum Reprod 17 2002 555 559
3. K.A. Hansen, and K.M. Eyster Clin Obstet Gynecol 53 2010 403 412
4. J.L. Simpson, F.Z. Bischoff, A. Kamat, J.E. Buster, and S.A. Carson Genetics of endometriosis Obstet Gynecol Clin North Am 30 2003 21 40 vii
5. H.M. Albertsen, R. Chettier, P. Farrington, and K. Ward Genome-wide association study link novel Loci to endometriosis PLoS One 8 2013 e58257
6. W. Di, and S.W. Guo The search for genetic variants predisposing women to endometriosis Curr Opin Obstet Gynecol 19 2007 395 401
7. N. Garrido, J. Navarro, J. Garcia-Velasco, J. Remoh, A. Pellice, and C. Simon The endometrium versus embryonic quality in endometriosis-related infertility Hum Reprod Update 8 2002 95 103
8. I. Matalliotakis, H. Cakmak, Y. Fragouli, A. Goumenou, N. Mahutte, and A. Arici Epidemiological characteristics in women with and without endometriosis in the Yale series Arch Gynecol Obstet 277 2008 389 393
9. J.A. Stilley, J.A. Birt, and K.L. Sharpe-Timms Cellular and molecular basis for endometriosis-associated infertility Cell Tissue Res 349 2012 849 862
10. C.L. Brizek, S. Schlaff, V.A. Pellegrini, J.B. Frank, and K.C. Worrilow Increased incidence of aberrant morphological phenotypes in human embryogenesis - an association with endometriosis J Assist Reprod Genet 12 1995 106 112
11. A. Pellicer, N. Oliveira, A. Ruiz, J. Remohi, and C. Simon Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction Hum Reprod 10 Suppl 2 1995 91 97
12. T. Tanbo, A. Omland, P.O. Dale, and T. Abyholm In vitro fertilization/embryo transfer in unexplained infertility and minimal peritoneal endometriosis Acta Obstet Gynecol Scand 74 1995 539 543
13. E.H. Yanushpolsky, C.L. Best, K.V. Jackson, R.N. Clarke, R.L. Barbieri, and M.D. Hornstein Effects of endometriomas on oocyte quality, embryo quality, and pregnancy rates in in vitro fertilization cycles: a prospective, case-controlled study J Assist Reprod Genet 15 1998 193 197
14. D.J. Cahill, and M.G. Hull Pituitary-ovarian dysfunction and endometriosis Hum Reprod Update 6 2000 56 66
15. K. Barnhart, R. Dunsmoor-Su, and C. Coutifaris Effect of endometriosis on in vitro fertilization Fertil Steril 77 2002 1148 1155
16. M. Groll Endometriosis and spontaneous abortion Fertil Steril 41 1984 933 935
17. D.A. Metzger, D.L. Olive, G.F. Stohs, and R.R. Franklin Association of endometriosis and spontaneous abortion: effect of control group selection Fertil Steril 45 1986 18 22
18. P. Tummers, P. De Sutter, and M. Dhont Risk of spontaneous abortion in singleton and twin pregnancies after IVF/ICSI Hum Reprod 18 2003 1720 1723
19. C. Tomassetti, C. Meuleman, A. Pexsters, A. Mihalyi, C. Kyama, P. Simsa, and T.M. D'Hooghe Endometriosis, recurrent miscarriage and implantation failure: is there an immunological link? Reprod Biomed Online 13 2006 58 64
20. B.G. Patel, and B.A. Lessey Clinical assessment and management of the endometrium in recurrent early pregnancy loss Semin Reprod Med 29 2011 491 506
21. S. Geber, T. Paraschos, G. Atkinson, R. Margara, and R.M. Winston Results of IVF in patients with endometriosis: the severity of the disease does not affect outcome, or the incidence of miscarriage Hum Reprod 10 1995 1507 1511
22. L. Sung, T. Mukherjee, T. Takeshige, M. Bustillo, and A.B. Copperman Endometriosis is not detrimental to embryo implantation in oocyte recipients J Assist Reprod Genet 14 1997 152 156
23. MG Hull, J.A. Williams, B. Ray, E.A. McLaughlin, V.A. Akande, and W.C. Ford The contribution of subtle oocyte or sperm dysfunction affecting fertilization in endometriosis-associated or unexplained infertility: a controlled comparison with tubal infertility and use of donor spermatozoa Hum Reprod 13 1998 1825 1830
24. D.E. Pittaway, C. Vernon, and J.A. Fayez Spontaneous abortions in women with endometriosis Fertil Steril 50 1988 711 715
25. R. Matorras, F. Rodriguez, G. Gutierrez de Teran, J.I. Pijoan, O. Ramon, and F.J. Rodriguez-Escudero Endometriosis and spontaneous abortion rate: a cohort study in infertile women Eur J Obstet Gynecol Reprod Biol 77 1998 101 105
26. M.W. Vernon, and E.A. Wilson Studies on the surgical induction of endometriosis in the rat Fertil Steril 44 1985 684 694
27. J.A. Stilley, R. Woods-Marshall, M. Sutovsky, P. Sutovsky, and K.L. Sharpe-Timms Reduced fecundity in female rats with surgically induced endometriosis and in their daughters: a potential role for tissue inhibitors of metalloproteinase 1 Biol Reprod 80 2009 649 656
28. J.A. Stilley, J.A. Birt, S.C. Nagel, M. Sutovsky, P. Sutovsky, and K.L. Sharpe-Timms Neutralizing TIMP1 restores fecundity in a rat model of endometriosis and treating control rats with TIMP1 causes anomalies in ovarian function and embryo development Biol Reprod 83 2010 185 194
29. National Research Council Guide for the care and use of laboratory animals 1996 National Academy Press Washington, DC
30. J.A. Stilley, and K.L. Sharpe-Timms TIMP1 contributes to ovarian anomalies in both an MMP-dependent and -independent manner in a rat model Biol Reprod 86 2012 47
31. K.L. Sharpe, and M.W. Vernon Polypeptides synthesized and released by rat ectopic uterine implants differ from those of the uterus in culture Biol Reprod 48 1993 1334 1340
32. K.L. Sharpe, M.C. Bertero, and M.W. Vernon Rapid regression of endometriosis by a new gonadotropin-releasing hormone antagonist in rats with surgically induced disease Prog Clin Biol Res 323 1990 449 458
33. K.L. Sharpe, M.C. Bertero, and M.W. Vernon Spontaneous and steroid-induced recurrence of endometriosis following suppression by a gonadotropin releasing hormone antagonist in the rat Amer J Obstet Gynecol 164 1991 187 194
34. Y. Agca, and J.K. Critser Assisted reproductive technologies and genetic modifications in rats M.A. Suckow, S.H. Weisbroth, C.L. Franklin, The laboratory rat 2nd ed. 2006 Elsevier Amsterdam 165 168
35. N.A. Telford, A.J. Watson, and G.A. Schultz Transition from maternal to embryonic control in early mammalian development: a comparison of several species Mol Reprod Dev 26 1990 90 100
36. W. Reik, W. Dean, and J. Walter Epigenetic reprogramming in mammalian development Science 293 2001 1089 1093
37. K.E. Pelch, A.L. Schroder, P.A. Kimball, K.L. Sharpe-Timms, J.W. Davis, and S.C. Nagel Aberrant gene expression profile in a mouse model of endometriosis mirrors that observed in women Fertil Steril 93 2010 1615 1627
38. Y. Benjamini, D. Drai, G. Elmer, N. Kafkafi, and I. Golani Controlling the false discovery rate in behavior genetics research Behav Brain Res 125 2001 279 284
39. D.W. Huang, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources Nature Protoc 4 2009 44 57
40. D.W. Huang, B.T. Sherman, and R.A. Lempicki Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res 37 2009 1 13
41. G. Mansour, R.K. Sharma, A. Agarwal, and T. Falcone Endometriosis-induced alterations in mouse metaphase II oocyte microtubules and chromosomal alignment: a possible cause of infertility Fertil Steril 94 2010 1894 1899
42. M.G. Melka, F. Rings, M. Hölker, E. Tholen, V. Havlicek, U. Besenfelder, K. Schellander, and D. Tesfaye Expression of apoptosis regulatory genes and incidence of apoptosis in different morphological quality groups of in vitro-produced bovine pre-implantation embryos Reprod Domest Anim 45 2010 915 921
43. A. Philchenkov Caspases: potential targets for regulating cell death J Cell Mol Med 8 2004 432 444
44. Y.A. Lazebnik, S.H. Kaufmann, S. Desnoyers, G.G. Poirier, and W.C. Earnshaw Cleavage of oly(ADP-ribose) polymerase by a proteinase with properties like ICE Nature 371 1994 346 347
45. D.W. Koh, T.M. Dawson, and V.L. Dawson Mediation of cell death by poly(ADP-ribose) polymerase-1 Pharmacol Res 52 2005 5 14
46. R. Krishnakumar, and W.L. Kraus The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets Mol Cell 39 2010 8 24
47. J. Zhang, V.L. Dawson, T.M. Dawson, and S.H. Snyder Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity Science 263 1994 687 689
48. M. Huang, P. Kozlowski, M. Collins, Y. Wang, T.A. Haystead, and L.M. Graves Caspase-dependent cleavage of carbamoyl phosphate synthetase II during apoptosis Mol Pharmacol 61 2002 569 577
49. Y. Shi Mechanisms of caspase activation and inhibition during apoptosis Mol Cell 9 2002 459 470
50. M. Martinez-Velazquez, J. Melendez-Zajgla, and V. Maldonado Apoptosis induced by cAMP requires Smac/DIABLO transcriptional upregulation Cell Signal 19 2007 1212 1220
51. P. Justo, A. Sanz, C. Lorz, D. Gómez-Garre, S. Mezzano, J. Egido, and A. Ortiz Expression of Smac/Diablo in tubular epithelial cells and during acute renal failure Kidney Int Suppl 86 2003 S52 S56
52. P. Vercellini, F. De Benedetti, E. Rossi, A. Colombo, L. Trespidi, and P.G. Crosignani Tumor necrosis factor in plasma and peritoneal fluid of women with and without endometriosis Gynecol Obstet Invest 36 1993 39 41
53. A.N. Elwi, B. Lee, H.C. Meijndert, J.E. Braun, and S.W. Kim Mitochondrial chaperone DnaJA3 induces Drp1-dependent mitochondrial fragmentation Int J Biochem Cell Biol v44 2012 1366 1376
54. H.W. Chen, H.T. Kuo, S.J. Wang, T.S. Lu, and R.C. Yang In vivo heat shock protein assembles with septic liver NF-κB/I-κB complex regulating NF-κB activity Shock 24 2005 232 238
55. Y. Wu, A. Starzinski-Powitz, and S.W. Guo Constitutive and tumor necrosis factor-alpha-stimulated activation of nuclear factor-kappaB in immortalized endometriotic cells and their suppression by trichostatin A Gynecol Obstet Invest 70 2010 23 33
56. A. Agoulea, G. Mastorakos, I. Lambrinoudaki, G. Christodoulakos, and G. Creatsas The role of oxidative-stress in the endometriosis related infertility Gynecol Endocrinol 25 2009 75 81
57. J.M. Zeller, I. Henig, E. Radwanska, and W.P. Dmowski Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis Am J Reprod Immunol Microbiol 13 1987 78 82
58. A.A. Murphy, W. Palinski, S. Rakin, A.J. Morales, and S. Parthasarathy Evidence for oxidatively modified lipid-portein complexes in endomerium and endometriosis Fertil Steril 69 1998 1092 1094