The role of the Hoxa10/HOXA10 gene in the etiology of endometriosis and its related infertility: A review

Journal of Assisted Reproduction and Genetics

Volumn 27, Issue 12, 2010, Pages 701-710

  Zanatta, Alysson ^a,b   Rocha, André M ^a   Carvalho, Filomena M ^b   Pereira, Ricardo M A ^a   Taylor, Hugh S ^c   Motta, Eduardo L A ^a,d   Baracat, Edmund C ^b   Serafini, Paulo C ^a,b  

^a Huntington Medicina Reprodutiva   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Endometriosis; Etiology; Homeobox genes; Hoxa10; Infertility; Surgery

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; HOX PROTEIN; MESSENGER RNA; PROGESTERONE; TRANSCRIPTION FACTOR HOXA10; TRANSCRIPTION FACTOR HOXA9;

ARTICLE; DISEASE ASSOCIATION; DROSOPHILA; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; ENDOMETRIOSIS; ENDOMETRIUM CELL; FEMALE GENITAL SYSTEM; GENE EXPRESSION; GENE MUTATION; HUMAN; INFERTILITY; MUELLERIAN DUCT; MYOMETRIUM; NIDATION; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; UTERINE CERVIX; UTERUS; VAGINA ADENOSIS;

ADULT; EMBRYO IMPLANTATION; ENDOMETRIOSIS; ENDOMETRIUM; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; HUMANS; INFERTILITY, FEMALE; PREGNANCY; PROGESTERONE; TRANSCRIPTION FACTORS;

EID: 78651283949     PISSN: 10580468     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10815-010-9471-y     Document Type: Article

References (68)

1. P Vercellini E Somigliana P Vigano A Abbiati G Barbara L Fedele 2009 Chronic pelvic pain in women: etiology, pathogenesis and diagnostic approach Gynecol Endocrinol 25 149 158 10.1080/09513590802549858 19347704
2. B Eskenazi ML Warner 1997 Epidemiology of endometriosis Obstet Gynecol Clin North Am 24 235 258 1:STN:280:DyaK2szgs1Cltg%3D%3D 10.1016/S0889-8545(05) 70302-8 9163765 (Pubitemid 27225159)
3. JA Sampson 1927 Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity Am J Obstet Gynecol 14 422 469
4. SE Bulun 2009 Endometriosis N Engl J Med 360 268 279 1:CAS:528: DC%2BD1MXnsFGhtA%3D%3D 10.1056/NEJMra0804690 19144942
5. PG Signorile F Baldi R Bussani M D'Armiento FM De A Baldi 2009 Ectopic endometrium in human foetuses is a common event and sustains the theory of mullerianosis in the pathogenesis of endometriosis, a disease that predisposes to cancer J Exp Clin Cancer Res 28 49 10.1186/1756-9966-28-49 19358700
6. C Chapron A Fauconnier M Vieira H Barakat B Dousset V Pansini, et al. 2003 Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification Hum Reprod 18 157 161 10.1093/humrep/deg009 12525459 (Pubitemid 36138869)
7. J Halme MG Hammond JF Hulka SG Raj LM Talbert 1984 Retrograde menstruation in healthy women and in patients with endometriosis Obstet Gynecol 64 151 154 1:STN:280:DyaL2c3ks1GrtA%3D%3D 6234483
8. DB Redwine 2003 'Invisible' microscopic endometriosis: a review Gynecol Obstet Invest 55 63 67 10.1159/000070176 12771451 (Pubitemid 36667673)
9. DB Redwine 2002 Was Sampson wrong? Fertil Steril 78 686 693 10.1016/S0015-0282(02)03329-0 12372441
10. TS Cullen 1914 Adenomyoma of the rectovaginal septum JAMA 62 835 839
11. Redwine DB. Mulleriosis. The single best fit model of the origin of endometriosis. Reprod Med. 1988;33:11:915-20.
12. H Browne H Taylor 2006 HOXA10 expression in ectopic endometrial tissue Fertil Steril 85 1386 1390 1:CAS:528:DC%2BD28XlsVelsb0%3D 10.1016/j.fertnstert. 2005.10.072 16647375
13. W McGinnis R Krumlauf 1992 Homeobox genes and axial patterning Cell 68 283 302 1:CAS:528:DyaK38XhtVShs7o%3D 10.1016/0092-8674(92)90471-N 1346368
14. HS Taylor GB Vanden Heuvel P Igarashi 1997 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 1338 1345 1:CAS:528:DyaK2sXnvVWns7w%3D 10.1095/biolreprod57.6.1338 9408238
15. HS Taylor A Arici D Olive P Igarashi 1998 HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium J Clin Invest 101 1379 1384 1:CAS:528:DyaK1cXitleksLw%3D 9525980
16. C Simon A Gutierrez A Vidal MJ de los Santos JJ Tarin J Remohi, et al. 1994 Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation Hum Reprod 9 725 729 1:STN:280:DyaK2czitFGnsw%3D%3D 8046030
17. A Arici E Oral O Bukulmez A Duleba DL Olive EE Jones 1996 The effect of endometriosis on implantation: results from the Yale University in vitro fertilization and embryo transfer program Fertil Steril 65 603 607 1:STN:280:DyaK28zntVequw%3D%3D 8774295
18. MG Hull JA Williams B Ray EA McLaughlin VA Akande WC Ford 1998 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 1825 1830 1:STN:280:DyaK1cvhtFWnuw%3D%3D 10.1093/humrep/13.7.1825 9740433
19. HS Taylor C Bagot A Kardana D Olive A Arici 1999 HOX gene expression is altered in the endometrium of women with endometriosis Hum Reprod 14 1328 1331 1:STN:280:DyaK1M3mt1Ogsg%3D%3D 10.1093/humrep/14.5.1328 10325287 (Pubitemid 29224916)
20. EB Lewis 1978 A gene complex controlling segmentation in Drosophila Nature 276 565 570 1:STN:280:DyaE1M%2FntlWgsQ%3D%3D 10.1038/276565a0 103000
21. R Krumlauf 1994 Hox genes in vertebrate development Cell 78 191 201 1:CAS:528:DyaK2cXlsFeqsb0%3D 10.1016/0092-8674(94)90290-9 7913880 (Pubitemid 24241088)
22. M Akam 1989 Hox and HOM: homologous gene clusters in insects and vertebrates Cell 57 347 349 1:CAS:528:DyaL1MXktVWlsrY%3D 10.1016/0092-8674(89) 90909-4 2566382 (Pubitemid 19126268)
23. M Mlodzik A Fjose WJ Gehring 1988 Molecular structure and spatial expression of a homeobox gene from the labial region of the Antennapedia-complex EMBO J 7 2569 2578 1:CAS:528:DyaL1MXhtV2hsbk%3D 2461299
24. RA Conlon J Rossant 1992 Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo Development 116 357 368 1:CAS:528:DyaK3sXpvVOltg%3D%3D 1363087
25. L Ma GV Benson H Lim SK Dey RL Maas 1998 Abdominal B (AbdB) Hoxa genes: regulation in adult uterus by estrogen and progesterone and repression in mullerian duct by the synthetic estrogen diethylstilbestrol (DES) Dev Biol 197 141 154 1:CAS:528:DyaK1cXjslCksLo%3D 10.1006/dbio.1998.8907 9630742 (Pubitemid 28265448)
26. W McGinnis MS Levine E Hafen A Kuroiwa WJ Gehring 1984 A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes Nature 308 428 433 1:CAS:528:DyaL2cXhs12gsb4%3D 10.1038/308428a0 6323992
27. GV Benson H Lim BC Paria I Satokata SK Dey RL Maas 1996 Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression Development 122 2687 2696 1:CAS:528:DyaK28XlvFCktro%3D 8787743
28. D Cermik M Karaca HS Taylor 2001 HOXA10 expression is repressed by progesterone in the myometrium: differential tissue-specific regulation of HOX gene expression in the reproductive tract J Clin Endocrinol Metab 86 3387 3392 1:CAS:528:DC%2BD3MXlt1Gjurk%3D 10.1210/jc.86.7.3387 11443215 (Pubitemid 32673512)
29. SC Hewitt JC Harrell KS Korach 2005 Lessons in estrogen biology from knockout and transgenic animals Annu Rev Physiol 67 285 308 1:CAS:528: DC%2BD2MXjsFeksr4%3D 10.1146/annurev.physiol.67.040403.115914 15709960 (Pubitemid 40404493)
30. M Magnusson AC Brun N Miyake J Larsson M Ehinger JM Bjornsson, et al. 2007 HOXA10 is a critical regulator for hematopoietic stem cells and erythroid/megakaryocyte development Blood 109 3687 3696 1:CAS:528: DC%2BD2sXkvFCit74%3D 10.1182/blood-2006-10-054676 17234739 (Pubitemid 46641717)
31. Q Wei JB St Clair T Fu P Stratton LK Nieman 2009 Reduced expression of biomarkers associated with the implantation window in women with endometriosis Fertil Steril 91 1686 1691 10.1016/j.fertnstert.2008.02.121 18672236
32. GS Daftary HS Taylor 2006 Endocrine regulation of HOX genes Endocr Rev 27 331 355 1:CAS:528:DC%2BD28Xms1ylsbo%3D 10.1210/er.2005-0018 16632680 (Pubitemid 43848302)
33. JJ Kim HS Taylor Z Lu O Ladhani JM Hastings KS Jackson, et al. 2007 Altered expression of HOXA10 in endometriosis: potential role in decidualization Mol Hum Reprod 13 323 332 1:CAS:528:DC%2BD2sXotVOitLo%3D 10.1093/molehr/gam005 17350963 (Pubitemid 47061643)
34. Z Lu J Hardt JJ Kim 2008 Global analysis of genes regulated by HOXA10 in decidualization reveals a role in cell proliferation Mol Hum Reprod 14 357 366 1:CAS:528:DC%2BD1cXns1Sitb8%3D 10.1093/molehr/gan023 18456676 (Pubitemid 351865909)
35. K Horie K Takakura K Imai S Liao T Mori 1992 Immunohistochemical localization of androgen receptor in the human endometrium, decidua, placenta and pathological conditions of the endometrium Hum Reprod 7 1461 1466 1:STN:280:DyaK3s7nvFGnsA%3D%3D 1291578
36. D Cermik B Selam HS Taylor 2003 Regulation of HOXA-10 expression by testosterone in vitro and in the endometrium of patients with polycystic ovary syndrome J Clin Endocrinol Metab 88 238 243 1:CAS:528:DC%2BD3sXkvVequg%3D%3D 10.1210/jc.2002-021072 12519859 (Pubitemid 36115172)
37. H Du GS Daftary SI Lalwani HS Taylor 2005 Direct regulation of HOXA10 by 1, 25-(OH)2D3 in human myelomonocytic cells and human endometrial stromal cells Mol Endocrinol 19 2222 2233 1:CAS:528:DC%2BD2MXpvFOjs7c%3D 10.1210/me.2004-0336 15905361 (Pubitemid 41252818)
38. K Shukunami W Tsunezawa F Kotsuji 2000 Unicornuate uterus with a noncommunicating cavitary, laterally dislocated rudimentary horn presenting with adenomyosis, associated with ipsilateral renal agenesis Arch Gynecol Obstet 264 88 89 1:STN:280:DC%2BD3cvpvF2msA%3D%3D 10.1007/s004049900045 11045330
39. MD Keltz L Peck S Liu AH Kim A Arici DL Olive 1995 Large bowel-to-pelvic sidewall adhesions associated with chronic pelvic pain J Am Assoc Gynecol Laparosc 3 55 59 1:STN:280:DyaK2s3jvVCisA%3D%3D 10.1016/S1074-3804(05)80137-9 9050617
40. RM Pereira CD Preti FJ Paula V Maia-Filho ELA Motta P Serafini 2005 Microscopic proven endometriosis in pericolic adhesions showing peritoneal typical and atypical lesions Fertil Steril 84 S244 S244 10.1016/j.fertnstert. 2005.07.503
41. KT Mai HM Yazdi DG Perkins W Parks 1997 Pathogenetic role of the stromal cells in endometriosis and adenomyosis Histopathology 30 430 442 1:STN:280:DyaK2szisFeisw%3D%3D 10.1046/j.1365-2559.1997.4910725.x 9181364
42. S Landi M Ceccaroni A Perutelli C Allodi F Barbieri A Fiaccavento, et al. 2006 Laparoscopic nerve-sparing complete excision of deep endometriosis: is it feasible? Hum Reprod 21 774 781 1:STN:280:DC%2BD287ksVWgsg%3D%3D 10.1093/humrep/dei324 16449312 (Pubitemid 43372987)
43. F Parazzini V Mais S Cipriani 2006 Adhesions and pain in women with first diagnosis of endometriosis: results from a cross-sectional study J Minim Invasive Gynecol 13 49 54 10.1016/j.jmig.2005.10.002 16431323 (Pubitemid 43129733)
44. C Chapron N Chopin B Borghese H Foulot B Dousset MC Vacher-Lavenu, et al. 2006 Deeply infiltrating endometriosis: pathogenetic implications of the anatomical distribution Hum Reprod 21 1839 1845 10.1093/humrep/del079 16543256 (Pubitemid 44028259)
45. K Nakayama H Masuzawa SF Li F Yoshikawa T Toki T Nikaido, et al. 1994 Immunohistochemical analysis of the peritoneum adjacent to endometriotic lesions using antibodies for Ber-EP4 antigen, estrogen receptors, and progesterone receptors: implication of peritoneal metaplasia in the pathogenesis of endometriosis Int J Gynecol Pathol 13 348 358 1:STN:280:DyaK2M7htlKhsw%3D%3D 10.1097/00004347-199410000-00009 7814197
46. S Matsuzaki M Canis C Darcha JL Pouly G Mage 2009 HOXA-10 expression in the mid-secretory endometrium of infertile patients with either endometriosis, uterine fibromas or unexplained infertility Hum Reprod 24 3180 3187 1:CAS:528:DC%2BD1MXhsVKls7rM 10.1093/humrep/dep306 19736237
47. A Zanatta P Serarini AM Rocha FM Carvalho EC Baracat HS Taylor 2009 HOXA10 is expressed in the endometrial stroma and in the muscle of rectosigmoid endometriosis Fertil Steril 92 S12 S12 10.1016/j.fertnstert.2009.07.1679
48. BA Lessey AJ Castelbaum SW Sawin CA Buck R Schinnar W Bilker, et al. 1994 Aberrant integrin expression in the endometrium of women with endometriosis J Clin Endocrinol Metab 79 643 649 1:STN:280:DyaK2czitFCqtg%3D%3D 10.1210/jc.79.2.643 7519194 (Pubitemid 24256567)
49. K Barnhart R Dunsmoor-Su C Coutifaris 2002 Effect of endometriosis on in vitro fertilization Fertil Steril 77 1148 1155 10.1016/S0015-0282(02)03112-6 12057720 (Pubitemid 34626321)
50. LC Kao A Germeyer S Tulac S Lobo JP Yang RN Taylor, et al. 2003 Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility Endocrinology 144 2870 2881 1:CAS:528:DC%2BD3sXkvF2ksbk%3D 10.1210/en.2003-0043 12810542 (Pubitemid 36819889)
51. WP Hu SK Tay Y Zhao 2006 Endometriosis-specific genes identified by real-time reverse transcription-polymerase chain reaction expression profiling of endometriosis versus autologous uterine endometrium J Clin Endocrinol Metab 91 228 238 1:CAS:528:DC%2BD28Xms1amsQ%3D%3D 10.1210/jc.2004-1594 16249290 (Pubitemid 43069143)
52. KM Eyster O Klinkova V Kennedy KA Hansen 2007 Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium Fertil Steril 88 1505 1533 1:CAS:528:DC%2BD1cXhsVygtrw%3D 10.1016/j.fertnstert.2007.01.056 17462640 (Pubitemid 350216849)
53. I Satokata G Benson R Maas 1995 Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice Nature 374 460 463 1:CAS:528:DyaK2MXkslSlsbs%3D 10.1038/374460a0 7700356
54. RL Gendron H Paradis HM Hsieh-Li DW Lee SS Potter E Markoff 1997 Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice Biol Reprod 56 1097 1105 1:CAS:528: DyaK2sXisl2ls7w%3D 10.1095/biolreprod56.5.1097 9160706
55. CN Bagot PJ Troy HS Taylor 2000 Alteration of maternal Hoxa10 expression by in vivo gene transfection affects implantation Gene Ther 7 1378 1384 1:CAS:528:DC%2BD3cXlvFajs7o%3D 10.1038/sj.gt.3301245 10981664
56. PJ Troy GS Daftary CN Bagot HS Taylor 2003 Transcriptional repression of peri-implantation EMX2 expression in mammalian reproduction by HOXA10 Mol Cell Biol 23 1 13 1:CAS:528:DC%2BD3sXhtVOmtQ%3D%3D 10.1128/MCB.23.1.1-13.2003 12482956 (Pubitemid 36008496)
57. N Miyamoto M Yoshida S Kuratani I Matsuo S Aizawa 1997 Defects of urogenital development in mice lacking Emx2 Development 124 1653 1664 1:CAS:528:DyaK2sXjs1Kntrc%3D 9165114
58. GS Daftary HS Taylor 2004 EMX2 gene expression in the female reproductive tract and aberrant expression in the endometrium of patients with endometriosis J Clin Endocrinol Metab 89 2390 2396 1:CAS:528:DC%2BD2cXjvFyrur4%3D 10.1210/jc.2003-031389 15126568 (Pubitemid 38619880)
59. HS Taylor X Fei 2005 Emx2 regulates mammalian reproduction by altering endometrial cell proliferation Mol Endocrinol 19 2839 2846 1:CAS:528: DC%2BD2MXhtFyjsrfF 10.1210/me.2005-0130 15994197 (Pubitemid 41577253)
60. HS Taylor P Igarashi DL Olive A Arici 1999 Sex steroids mediate HOXA11 expression in the human peri-implantation endometrium J Clin Endocrinol Metab 84 1129 1135 1:CAS:528:DyaK1MXhvFens7Y%3D 10.1210/jc.84.3.1129 10084606
61. Y Wu G Halverson Z Basir E Strawn P Yan SW Guo 2005 Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis Am J Obstet Gynecol 193 371 380 1:CAS:528: DC%2BD2MXns1Wms7w%3D 10.1016/j.ajog.2005.01.034 16098858 (Pubitemid 41159530)
62. B Lee H Du HS Taylor 2009 Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium Biol Reprod 80 79 85 10.1095/biolreprod.108.070391 18799756
63. GR Attia K Zeitoun D Edwards A Johns BR Carr SE Bulun 2000 Progesterone receptor isoform A but not B is expressed in endometriosis J Clin Endocrinol Metab 85 2897 2902 1:CAS:528:DC%2BD3cXnslahsbw%3D 10.1210/jc.85.8.2897 10946900 (Pubitemid 32269170)
64. PH Bianchi RM Pereira A Zanatta JR Alegretti EL Motta PC Serafini 2009 Extensive excision of deep infiltrative endometriosis before in vitro fertilization significantly improves pregnancy rates J Minim Invasive Gynecol 16 174 180 10.1016/j.jmig.2008.12.009 19249705
65. JL Sarno F Schatz CJ Lockwood ST Huang HS Taylor 2006 Thrombin and interleukin-1beta regulate HOXA10 expression in human term decidual cells: implications for preterm labor J Clin Endocrinol Metab 91 2366 2372 1:CAS:528:DC%2BD28XlvVCgt70%3D 10.1210/jc.2005-1807 16551735 (Pubitemid 43855029)
66. SM Salih HS Taylor 2004 HOXA10 gene expression in human fallopian tube and ectopic pregnancy Am J Obstet Gynecol 190 1404 1406 1:CAS:528: DC%2BD2cXkt1Wqtrg%3D 10.1016/j.ajog.2004.01.066 15167850 (Pubitemid 38692229)
67. GS Daftary HS Taylor 2002 Hydrosalpinx fluid diminishes endometrial cell HOXA10 expression Fertil Steril 78 577 580 10.1016/S0015-0282(02)03306-X 12215336
68. GS Daftary U Kayisli E Seli O Bukulmez A Arici HS Taylor 2007 Salpingectomy increases peri-implantation endometrial HOXA10 expression in women with hydrosalpinx Fertil Steril 87 367 372 1:CAS:528:DC%2BD2sXivF2ltbY%3D 10.1016/j.fertnstert.2006.06.041 17173899 (Pubitemid 46176925)