9
Views
5
CrossRef citations to date
0
Altmetric
Reviews

Endometriosis and infertility: biomarkers affecting implantation rate

, &
Pages 467-473 | Published online: 10 Jan 2014

References

  • Bulun SE. Endometriosis. N. Engl. J. Med. 360(3), 268–279 (2009).
  • Kennedy S, Bergqvist A, Chapron C et al. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum. Reprod. 20(10), 2698–2704 (2005).
  • Giudice LC, Kao LC. Endometriosis. Lancet 364(9447), 1789–1799 (2004).
  • Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosis-associated infertility. Fertil. Steril. 90(2), 247–257 (2008).
  • Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil. Steril. 77(6), 1148–1155 (2002).
  • Carvalho L, Podgaec S, Bellodi-Privato M, Falcone T, Abrao MS. Role of eutopic endometrium in pelvic endometriosis. J. Minim. Invasive Gynecol. 18(4), 419–427 (2011).
  • Brosens I, Brosens JJ, Benagiano G. The eutopic endometrium in endometriosis: are the changes of clinical significance? Reprod. Biomed. Online 24(5), 496–502 (2012).
  • Strowitzki T, Germeyer A, Popovici R, von Wolff M. The human endometrium as a fertility-determining factor. Hum. Reprod. Update 12(5), 617–630 (2006).
  • Navot D, Bergh P. Preparation of the human endometrium for implantation. Ann. N. Y. Acad. Sci. 622, 212–219 (1991).
  • Stoikos CJ, Salamonsen LA, Hannan NJ, O'Connor AE, Rombauts L, Dimitriadis E. Activin A regulates trophoblast cell adhesive properties: implications for implantation failure in women with endometriosis-associated infertility. Hum. Reprod. 25(7), 1767–1774 (2010).
  • van Mourik MS, Macklon NS, Heijnen CJ. Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment. J. Leukoc. Biol. 85(1), 4–19 (2009).
  • Xiao Y, Sun X, Yang X et al. Leukemia inhibitory factor is dysregulated in the endometrium and uterine flushing fluid of patients with adenomyosis during implantation window. Fertil. Steril. 94(1), 85–89 (2010).
  • Dimitriadis E, Stoikos C, Stafford-Bell M et al. Interleukin-11, IL-11 receptoralpha and leukemia inhibitory factor are dysregulated in endometrium of infertile women with endometriosis during the implantation window. J Reprod. Immunol. 69(1), 53–64 (2006).
  • Schofield G, Kimber SJ. Leukocyte subpopulations in the uteri of leukemia inhibitory factor knockout mice during early pregnancy. Biol. Reprod. 72(4), 872–878 (2005).
  • Kralickova M, Sima R, Vanecek T et al. Leukemia inhibitory factor gene mutations in the population of infertile women are not restricted to nulligravid patients. Eur. J. Obstet. Gynecol. Reprod. Biol. 127(2), 231–235 (2006).
  • Cork BA, Tuckerman EM, Li TC, Laird SM. Expression of interleukin (IL)-11 receptor by the human endometrium in vivo and effects of IL-11, IL-6 and LIF on the production of MMP and cytokines by human endometrial cells in vitro. Mol. Hum. Reprod. 8(9), 841–848 (2002).
  • Robb L, Li R, Hartley L, Nandurkar HH, Koentgen F, Begley CG. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat. Med. 4(3), 303–308 (1998).
  • Fowler DJ, Nicolaides KH, Miell JP. Insulin-like growth factor binding protein-1 (IGFBP-1): a multifunctional role in the human female reproductive tract. Hum. Reprod. Update 6(5), 495–504 (2000).
  • Giudice LC. Multifaceted roles for IGFBP-1 in human endometrium during implantation and pregnancy. Ann. N. Y. Acad. Sci. 828, 146–156 (1997).
  • Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil. Steril. 85(3), 564–572 (2006).
  • Yin X, Pavone ME, Lu Z, Wei J, Kim JJ. Increased activation of the PI3K/AKT pathway compromises decidualization of stromal cells from endometriosis. J. Clin. Endocrinol. Metab. 97(1), E35–E43 (2012).
  • Wei Q, St Clair JB, Fu T, Stratton P, Nieman LK. Reduced expression of biomarkers associated with the implantation window in women with endometriosis. Fertil. Steril. 91(5), 1686–1691 (2009).
  • Brown SE, Mandelin E, Oehninger S, Toner JP, Seppala M, Jones HW Jr. Endometrial glycodelin-A expression in the luteal phase of stimulated ovarian cycles. Fertil. Steril. 74(1), 130–133 (2000).
  • Vigne JL, Hornung D, Mueller MD, Taylor RN. Purification and characterization of an immunomodulatory endometrial protein, glycodelin. J. Biol. Chem. 276(20), 17101–17105 (2001).
  • Johnson GA, Burghardt RC, Bazer FW, Spencer TE. Osteopontin: roles in implantation and placentation. Biol. Reprod. 69(5), 1458–1471 (2003).
  • Lessey BA. Implantation defects in infertile women with endometriosis. Ann. N. Y. Acad. Sci. 955, 265–280; discussion 293–265, 396–406 (2002).
  • Cho S, Ahn YS, Choi YS et al. Endometrial osteopontin mRNA expression and plasma osteopontin levels are increased in patients with endometriosis. Am. J. Reprod. Immunol. 61(4), 286–893 (2009).
  • Casals G, Ordi J, Creus M et al. Expression pattern of osteopontin and alphavbeta3 integrin during the implantation window in infertile patients with early stages of endometriosis. Hum. Reprod. 27(3), 805–813 (2012).
  • Genbacev OD, Prakobphol A, Foulk RA et al. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science 299(5605), 405–408 (2003).
  • Minas V, Loutradis D, Makrigiannakis A. Factors controlling blastocyst implantation. Reprod. Biomed. Online, 10(2), 205–216 (2005).
  • Wang B, Sheng JZ, He RH, Qian YL, Jin F, Huang HF. High expression of L-selectin ligand in secretory endometrium is associated with better endometrial receptivity and facilitates embryo implantation in human being. Am. J. Reprod. Immunol. 60(2), 127–134 (2008).
  • Foulk RA, Zdravkovic T, Genbacev O, Prakobphol A. Expression of L-selectin ligand MECA-79 as a predictive marker of human uterine receptivity. J. Assist. Reprod. Genet. 24(7), 316–321 (2007).
  • Lai TH, Shih Ie M, Vlahos N, Ho CL, Wallach E, Zhao Y. Differential expression of L-selectin ligand in the endometrium during the menstrual cycle. Fertil. Steril. 83 (Suppl. 1), 1297–1302 (2005).
  • Margarit L, Gonzalez D, Lewis PD et al. L-selectin ligands in human endometrium: comparison of fertile and infertile subjects. Hum. Reprod. 24(11), 2767–2777 (2009).
  • Lessey BA, Castelbaum AJ, Sawin SW et al. Aberrant integrin expression in the endometrium of women with endometriosis. J. Clin. Endocrinol. Metab. 79(2), 643–649 (1994).
  • Lessey BA. The use of integrins for the assessment of uterine receptivity. Fertil. Steril. 61(5), 812–814 (1994).
  • Lessey BA, Castelbaum AJ, Buck CA, Lei Y, Yowell CW, Sun J. Further characterization of endometrial integrins during the menstrual cycle and in pregnancy. Fertil. Steril. 62(3), 497–506 (1994).
  • Lessey BA, Young SL. Integrins and other cell adhesion molecules in endometrium and endometriosis. Semin. Reprod. Endocrinol. 15(3), 291–299 (1997).
  • Cakmak H, Taylor HS. Implantation failure: molecular mechanisms and clinical treatment. Hum. Reprod. Update 17(2), 242–253 (2011).
  • Paria BC, Zhao X, Das SK, Dey SK, Yoshinaga K. Zonula occludens-1 and E-cadherin are coordinately expressed in the mouse uterus with the initiation of implantation and decidualization. Dev. Biol. 208(2), 488–501 (1999).
  • Matsuzaki S, Darcha C, Maleysson E, Canis M, Mage G. Impaired down-regulation of E-cadherin and beta-catenin protein expression in endometrial epithelial cells in the mid-secretory endometrium of infertile patients with endometriosis. J. Clin. Endocrinol. Metab. 95(7), 3437–3445 (2010).
  • Margarit L, Taylor A, Roberts MH et al. MUC1 as a discriminator between endometrium from fertile and infertile patients with PCOS and endometriosis. J. Clin. Endocrinol. Metab. 95(12), 5320–5329 (2010).
  • Ye X, Chun J. Lysophosphatidic acid (LPA) signaling in vertebrate reproduction. Trends Endocrinol. Metab. 21(1), 17–24 (2010).
  • Ye X, Hama K, Contos JJ et al. LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature 435(7038), 104–108 (2005).
  • Shah BH, Catt KJ. Roles of LPA3 and COX-2 in implantation. Trends Endocrinol. Metab. 16(9), 397–399 (2005).
  • Aghajanova L, Velarde MC, Giudice LC. Altered gene expression profiling in endometrium: evidence for progesterone resistance. Semin. Reprod. Med. 28(1), 51–58 (2010).
  • Giudice LC, Telles TL, Lobo S, Kao L. The molecular basis for implantation failure in endometriosis: on the road to discovery. Ann. N. Y. Acad. Sci. 955, 252–264; discussion 293–255, 396–406 (2002).
  • Wu Y, Strawn E, Basir Z, Halverson G, Guo SW. Promoter hypermethylation of progesterone receptor isoform B (PR-B) in endometriosis. Epigenetics 1(2), 106–111 (2006).
  • Tranguch S, Wang H, Daikoku T, Xie H, Smith DF, Dey SK. FKBP52 deficiency-conferred uterine progesterone resistance is genetic background and pregnancy stage specific. J. Clin. Invest. 117(7), 1824–1834 (2007).
  • Aghajanova L, Velarde MC, Giudice LC. The progesterone receptor coactivator Hic-5 is involved in the pathophysiology of endometriosis. Endocrinology 150(8), 3863–3870 (2009).
  • McGinnis W, Krumlauf R. Homeobox genes and axial patterning. Cell 68(2), 283–302 (1992).
  • Zanatta A, Rocha AM, Carvalho FM et al. The role of the Hoxa10/HOXA10 gene in the etiology of endometriosis and its related infertility: a review. J. Assist. Reprod. Genet. 27(12), 701–710 (2010).
  • Taylor HS, Arici A, Olive D, Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J. Clin. Invest. 101(7), 1379–1384 (1998).
  • Cakmak H, Taylor HS. Molecular mechanisms of treatment resistance in endometriosis: the role of progesterone-hox gene interactions. Semin. Reprod. Med. 28(1), 69–74 (2010).
  • Daftary GS, Taylor HS. Endocrine regulation of HOX genes. Endocr. Rev. 27(4), 331–355 (2006).
  • Kim JJ, Taylor HS, Lu Z et al. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol. Hum. Reprod. 13(5), 323–332 (2007).
  • Wu Y, Halverson G, Basir Z, Strawn E, Yan P, Guo SW. Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am. J. Obstet. Gynecol. 193(2), 371–380 (2005).
  • Yang H, Zhou Y, Edelshain B, Schatz F, Lockwood CJ, Taylor HS. FKBP4 is regulated by HOXA10 during decidualization and in endometriosis. Reproduction 143(4), 531–538 (2012).
  • Troy PJ, Daftary GS, Bagot CN, Taylor HS. Transcriptional repression of peri-implantation EMX2 expression in mammalian reproduction by HOXA10. Mol. Cell Biol. 23(1), 1–13 (2003).
  • Daftary GS, Taylor HS. EMX2 gene expression in the female reproductive tract and aberrant expression in the endometrium of patients with endometriosis. J. Clin. Endocrinol. Metab. 89(5), 2390–2396 (2004).
  • Taylor HS, Vanden Heuvel GB, Igarashi P. A conserved Hox axis in the mouse and human female reproductive system: late establishment and persistent adult expression of the Hoxa cluster genes. Biol. Reprod. 57(6), 1338–1345 (1997).
  • Taylor HS, Fei X. Emx2 regulates mammalian reproduction by altering endometrial cell proliferation. Mol. Endocrinol. 19(11), 2839–2846 (2005).
  • Lessey BA. Assessment of endometrial receptivity. Fertil. Steril. 96(3), 522–529 (2011).
  • Halme J. Role of peritoneal inflammation in endometriosis-associated infertility. Ann. N. Y. Acad. Sci. 622, 266–274 (1991).
  • Agarwal A, Gupta S, Sekhon L, Shah R. Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid. Redox. Signal 10(8), 1375–1403 (2008).
  • Halis G, Arici A. Endometriosis and inflammation in infertility. Ann. N. Y. Acad. Sci. 1034, 300–315 (2004).
  • Illera MJ, Juan L, Stewart CL, Cullinan E, Ruman J, Lessey BA. Effect of peritoneal fluid from women with endometriosis on implantation in the mouse model. Fertil. Steril. 74(1), 41–48 (2000).
  • Steinleitner A, Lambert H, Kazensky C, Danks P. Peritoneal fluid from endometriosis patients affects reproductive outcome in an in vivo model. Fertil. Steril. 53(5), 926–929 (1990).
  • Osborn BH, Haney AF, Misukonis MA, Weinberg JB. Inducible nitric oxide synthase expression by peritoneal macrophages in endometriosis-associated infertility. Fertil. Steril. 77(1), 46–51 (2002).
  • Gnainsky Y, Granot I, Aldo PB et al. Local injury of the endometrium induces an inflammatory response that promotes successful implantation. Fertil. Steril. 94(6), 2030–2036 (2010).
  • Zhou L, Li R, Wang R, Huang HX, Zhong K. Local injury to the endometrium in controlled ovarian hyperstimulation cycles improves implantation rates. Fertil. Steril. 89(5), 1166–1176 (2008).
  • Huang SY, Wang CJ, Soong YK et al. Site-specific endometrial injury improves implantation and pregnancy in patients with repeated implantation failures. Reprod. Biol. Endocrinol. 9, 140 (2011).
  • Li R, Hao G. Local injury to the endometrium: its effect on implantation. Curr. Opin. Obstet. Gynecol. 21(3), 236–239 (2009).
  • Miller PB, Parnell BA, Bushnell G et al. Endometrial receptivity defects during IVF cycles with and without letrozole. Hum. Reprod. 27(3), 881–888 (2012).
  • Revel A, Helman A, Koler M et al. Heparanase improves mouse embryo implantation. Fertil. Steril. 83(3), 580–586 (2005).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.