Endometrial gene expression in early pregnancy: Lessons from human ectopic pregnancy

Reproductive Sciences

Volumn 15, Issue 8, 2008, Pages 797-816

  Savaris, Ricardo F ^a   Hamilton, Amy E ^b   Lessey, Bruce A ^c   Giudice, Linda C ^b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GREENVILLE HOSPITAL SYSTEM   (United States)

Author keywords

Ectopi cpregnancy; Microarray; Transcriptome

Indexed keywords

GLYCAN; GLYCOSPHINGOLIPID; PHOSPHOLIPID;

ADULT; ARTICLE; BLOOD CLOTTING; CLINICAL ARTICLE; CONTROLLED STUDY; ECTOPIC PREGNANCY; ENDOMETRIUM BIOPSY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; LIPID DEGRADATION; LIPOGENESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADULT; ENDOMETRIUM; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; PREGNANCY, ECTOPIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC; YOUNG ADULT;

EID: 54349128441     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719108317585     Document Type: Article

References (67)

1. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Fertil Steril. 1950 ; 1: 3-25.
2. Lessey BA, Damjanovich L., Coutifaris C., Castelbaum A., Albelda SM, Buck CA Integrins adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J Clin Invest. 1992 ; 90: 188-195.
3. Achache H., Revel A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update. 2006 ; 12: 731-746.
4. Giudice LC, Irwin JC Roles of the insulinlike growth factor family in nonpregnant human endometrium and at the decidual:trophoblast interface. Semin Reprod Endocrinol. 1999 ; 17: 13-21.
5. Mooney SB, Giudice LC Fetal Endocrinology. Endotext.com ; 2002.
6. Carson DD, Lagow E., Thathiah A., et al. 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. 2002 ; 8: 871-879.
7. Horcajadas JA, Riesewijk A., Martín J., et al. Global gene expression profiling of human endometrial receptivity. J Reprod Immunol. 2004 ; 63: 41-49.
8. Kao LC, Tulac S., Lobo S., et al. Global gene profiling in human endometrium during the window of implantation. Endocrinology. 2002 ; 143: 2119-2138.
9. Ponnampalam AP, Weston GC, Trajstman AC, Susil B., Rogers PA Molecular classification of human endometrial cycle stages by transcriptional profiling. Mol Hum Reprod. 2004 ; 10: 879-893.
10. Hess AP, Hamilton AE, Talbi S., et al. Decidual stromal cell response to paracrine signals from the trophoblast: amplification of immune and angiogenic modulators. Biol Reprod. 2007 ; 76: 102-117.
11. Popovici RM, Betzler NK, Krause MS, et al. Gene expression profiling of human endometrial-trophoblast interaction in a coculture model. Endocrinology. 2006 ; 147: 5662-5675.
12. Sherwin JR, Sharkey AM, Cameo P., et al. Identification of novel genes regulated by chorionic gonadotropin in baboon endometrium during the window of implantation. Endocrinology. 2007 ; 148: 618-626.
13. Chen HW, Chen JJ, Tzeng CR, et al. Global analysis of differentially expressed genes in early gestational decidua and chorionic villi using a 9600 human cDNA microarray. Mol Hum Reprod. 2002 ; 8: 475-484.
14. Talbi S., Hamilton AE, Vo KC, et al. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology. 2006 ; 147: 1097-1121.
15. Liu P., Hwang JT Quick calculation for sample size while controlling false discovery rate with application to microarray analysis. Bioinformatics. 2007 ; 23: 739-746.
16. Breitling R. Biological microarray interpretation: the rules of engagement. Biochim Biophys Acta. 2006 ; 1759: 319-327.
17. Cui X., Churchill GA Statistical tests for differential expression in cDNA microarray experiments. Genome Biol. 2003 ; 4: 210
18. Viera AJ, Garrett JM Understanding interobserver agreement: the kappa statistic. Fam Med. 2005 ; 37: 360-363.
19. Soriano D., Hugol D., Quang NT, Darai E. Serum concentrations of interleukin-2R (IL-2R), IL-6, IL-8, and tumor necrosis factor alpha in patients with ectopic pregnancy. Fertil Steril. 2003 ; 79: 975-980.
20. Sallam HN, Sallam A., Ezzeldin F., Agamia AF, Abou-Ali A. Reference values for the midluteal plasma progesterone concentration: evidence from human menopausal gonadotropin-stimulated pregnancy cycles. Fertil Steril. 1999 ; 71: 711-714.
21. Critchley HO, Jones RL, Lea RG, et al. Role of inflammatory mediators in human endometrium during progesterone withdrawal and early pregnancy. J Clin Endocrinol Metab. 1999 ; 84: 240-248.
22. Tierney EP, Tulac S., Huang ST, Giudice LC Activation of the protein kinase A pathway in human endometrial stromal cells reveals sequential categorical gene regulation. Physiol Genomics. 2003 ; 16: 47-66.
23. Burney RO, Talbi S., Hamilton AE, et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007 ; 148: 3814-3826.
24. Tabibzadeh S., Kong QF, Babaknia A., May LT Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window. Hum Reprod. 1995 ; 10: 2793-2799.
25. Otani T., Minami S., Kokawa K., Shikone T., Yamoto M., Nakano R. Immunohistochemical localization of activin A in human endometrial tissues during the menstrual cycle and in early pregnancy. Obstet Gynecol. 1998 ; 91 (5 Pt 1). 685-692.
26. Jones RL, Salamonsen LA, Zhao YC, Ethier JF, Drummond AE, Findlay JK Expression of activin receptors, follistatin and betaglycan by human endometrial stromal cells; consistent with a role for activins during decidualization. Mol Hum Reprod. 2002 ; 8: 363-374.
27. Grinius L., Kessler C., Schroeder J., Handwerger S. Forkhead transcription factor FOXO1A is critical for induction of human decidualization. J Endocrinol. 2006 ; 189: 179-187.
28. Labied S., Kajihara T., Madureira PA, et al. Progestins regulate the expression and activity of the forkhead transcription factor FOXO1 in differentiating human endometrium. Mol Endocrinol. 2006 ; 20: 35-44.
29. Sasaki A., Shinkawa O., Yoshinaga K. Placental corticotropinreleasing hormone may be a stimulator of maternal pituitary adrenocorticotropic hormone secretion in humans. J Clin Invest. 1989 ; 84: 1997-2001.
30. Rogatsky I., Wang JC, Derynck MK, et al. Target-specific utilization of transcriptional regulatory surfaces by the glucocorticoid receptor. Proc Natl Acad Sci U S A. 2003 ; 100: 13845-13850.
31. Tulac S., Nayak NR, Kao LC, et al. Identification, characterization, and regulation of the canonical Wnt signaling pathway in human endometrium. J Clin Endocrinol Metab. 2003 ; 88: 3860-3866.
32. Xu C., Mao D., Holers VM, Palanca B., Cheng AM, Molina H. A critical role for murine complement regulator crry in fetomaternal tolerance. Science. 2000 ; 287: 498-501.
33. Young SL, Lessey BA, Fritz MA, et al. In vivo and in vitro evidence suggest that HB-EGF regulates endometrial expression of human decay-accelerating factor. J Clin Endocrinol Metab. 2002 ; 87: 1368-1375.
34. Low JM, Moore TL A role for the complement system in rheumatoid arthritis. Curr Pharm Des. 2005 ; 11: 655-670.
35. Markiewski MM, Lambris JD The role of complement in inflammatory diseases from behind the scenes into the spotlight. Am J Pathol. 2007 ; 171: 715-727.
36. Borregaard N., Theilgaard-Mönch K., Cowland JB, Ståhle M., Sørensen OE Neutrophils and keratinocytes in innate immunity-cooperative actions to provide antimicrobial defense at the right time and place. J Leukoc Biol. 2005 ; 77: 439-443.
37. Bratt T. Lipocalins and cancer. Biochim Biophys Acta. 2000 ; 1482: 318-326.
38. Sørensen OE, Cowland JB, Theilgaard-Mönch K., Liu L., Ganz T., Borregaard N. Wound healing and expression of antimicrobial peptides/polypeptides in human keratinocytes, a consequence of common growth factors. J Immunol. 2003 ; 170: 5583-5589.
39. Seth P., Porter D., Lahti-Domenici J., Geng Y., Richardson A., Polyak K. Cellular and molecular targets of estrogen in normal human breast tissue. Cancer Res. 2002 ; 62: 4540-4544.
40. Yao MW, Lim H., Schust DJ, et al. Gene expression profiling reveals progesterone-mediated cell cycle and immunoregulatory roles of Hoxa-10 in the preimplantation uterus. Mol Endocrinol. 2003 ; 17: 610-627.
41. Ziegler S., Röhrs S., Tickenbrock L., et al. Lipocalin 24p3 is regulated by the Wnt pathway independent of regulation by iron. Cancer Genet Cytogenet. 2007 ; 174: 16-23.
42. Berger T., Togawa A., Duncan GS, et al. Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc Natl Acad Sci U S A. 2006 ; 103: 1834-1839.
43. Huang HL, Chu ST, Chen YH Ovarian steroids regulate 24p3 expression in mouse uterus during the natural estrous cycle and the preimplantation period. J Endocrinol. 1999 ; 162: 11-19.
44. King A., Burrows T., Verma S., Hiby S., Loke YW Human uterine lymphocytes. Hum Reprod Update. 1998 ; 4: 480-485.
45. Huddleston H., Schust DJ Immune interactions at the maternal-fetal interface: a focus on antigen presentation. Am J Reprod Immunol. 2004 ; 51: 283-289.
46. Lee N., Llano M., Carretero M., et al. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci U S A. 1998 ; 95: 5199-5204.
47. Le BP, Tabiasco J. Killers become builders during pregnancy. Nat Med. 2006 ; 12: 991-992.
48. Kobayashi Y. The role of chemokines in neutrophil biology. Front Biosci. 2008 ; 13: 2400-2407.
49. Foell D., Wittkowski H., Vogl T., Roth J. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol. 2007 ; 81: 28-37.
50. Dong JC, Dong H., Campana A., Bischof P. Matrix metalloproteinases and their specific tissue inhibitors in menstruation. Reproduction. 2002 ; 123: 621-631.
51. Zhai Y., Wu R., Schwartz DR, et al. Role of beta-catenin/ T-cell factor-regulated genes in ovarian endometrioid adenocarcinomas. Am J Pathol. 2002 ; 160: 1229-1238.
52. Raouf A., Li V., Kola I., Watson DK, Seth A. The Ets1 proto-oncogene is upregulated by retinoic acid: characterization of a functional retinoic acid response element in the Ets1 promoter. Oncogene. 2000 ; 19: 1969-1974.
53. Takeshita S., Kikuno R., Tezuka K., Amann E. Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J. 1993 ; 294 (Pt 1). 271-278.
54. Gillan L., Matei D., Fishman DA, Gerbin CS, Karlan BY, Chang DD Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res. 2002 ; 62: 5358-5364.
55. Horiuchi K., Amizuka N., Takeshita S., et al. Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res. 1999 ; 14: 1239-1249.
56. Sasaki H., Lo KM, Chen LB, et al. Expression of periostin, homologous with an insect cell adhesion molecule, as a prognostic marker in non-small cell lung cancers. Jpn J Cancer Res. 2001 ; 92: 869-873.
57. Litvin J., Chen X., Keleman S., Zhu S., Autieri M. Expression and function of periostin-like factor in vascular smooth muscle cells. Am J Physiol Cell Physiol. 2007 ; 292: C1672 - C1680.
58. Grigoriadis A., Mackay A., Reis-Filho JS, et al. Establishment of the epithelial-specific transcriptome of normal and malignant human breast cells based on MPSS and array expression data. Breast Cancer Res. 2006 ; 8: R56
59. Kudo Y., Siriwardena BS, Hatano H., Ogawa I., Takata T. Periostin: novel diagnostic and therapeutic target for cancer. Histol Histopathol. 2007 ; 22: 1167-1174.
60. Oka T., Xu J., Kaiser RA, et al. Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res. 2007 ; 101: 313-321.
61. Yoshiba N., Yoshiba K., Hosoya A., et al. Association of TIMP-2 with extracellular matrix exposed to mechanical stress and its co-distribution with periostin during mouse mandible development. Cell Tissue Res. 2007 ; 330: 133: 145.
62. Floridon C., Nielsen O., Hølund B., et al. Does plasminogen activator inhibitor-1 (PAI-1) control trophoblast invasion? A study of fetal and maternal tissue in intrauterine, tubal and molar pregnancies. Placenta. 2000 ; 21: 754-762.
63. Lockwood CJ, Krikun G., Papp C., et al. The role of progestationally regulated stromal cell tissue factor and type-1 plasminogen activator inhibitor (PAI-1) in endometrial hemostasis and menstruation. Ann N Y Acad Sci. 1994 ; 734: 57-79.
64. Dossenbach-Glaninger A., van Trotsenburg M., Dossenbach M., et al. Plasminogen activator inhibitor 1 4G/5G polymorphism and coagulation factor XIII Val34Leu polymorphism: impaired fibrinolysis and early pregnancy loss. Clin Chem. 2003 ; 49: 1081-1086.
65. Smith SK Regulation of angiogenesis in the endometrium. Trends Endocrinol Metab. 2001 ; 12: 147-151.
66. Strieter RM, Kunkel SL, Elner VM, et al. Interleukin-8. A corneal factor that induces neovascularization. Am J Pathol. 1992 ; 141: 1279-1284.
67. Iozzo RV The family of the small leucine-rich proteoglycans: key regulators of matrix assembly and cellular growth. Crit Rev Biochem Mol Biol. 1997 ; 32: 141-174.