HOX Genes and Endometriosis

Endometriosis: Science and Practice

Volumn , Issue , 2012, Pages 184-189

  Kulp, Jennifer L ^a   Cakmak, Hakan ^a   Taylor, Hugh S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endometriosis; Endometrium; Epigenetics; Fertility; Homeobox; HOX; HOXA10; HOXA11; Methylation; Transcription

Indexed keywords

EID: 84886974236     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781444398519.ch18     Document Type: Chapter

References (62)

1. Gehring WJ, Hiromi Y. Homeotic genes and the homeobox. Annu Rev Genet. 1986; 20:147-173.
2. Apiou F, Flagiello D, Cillo C et al. Fine mapping of human HOX gene clusters. Cytogenet Cell Genet 1996; 73:114-115.
3. Scott MP. Vertebrate homeobox gene nomenclature. Cell 1992; 71: 551-553.
4. Dekker EE, Kitson RP. 2-Keto-4-hydroxyglutarate aldolase: purification and characterization of the homogeneous enzyme from bovine kidney. J Biol Chem 1992; 267:10507-10514.
5. 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 1997; 57:1338-1345.
6. Daftary GS, Taylor HS. Endocrine regulation of HOX genes. Endocr Rev 2006; 27:331-355.
7. Balling R, Mutter G, Gruss P et al. Craniofacial abnormalities induced by ectopic expression of the homeobox gene Hox-1.1 in transgenic mice. Cell 1989; 58:337-347.
8. Hunt P, Gulisano M, Cook M et al. A distinct Hox code for the branchial region of the vertebrate head. Nature 1991; 353:861-864.
9. Block K, Kardana A, Igarashi P et al. In utero diethylstilbestrol (DES) exposure alters Hox gene expression in the developing mullerian system. Faseb J 2000; 14:1101-1108.
10. Benson GV, Lim H, Paria BC et al. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 1996; 122:2687-2696.
11. Taylor HS, Arici A, Olive D et al. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest 1998; 101:1379-1384.
12. Taylor HS, Igarashi P, Olive DL et al. Sex steroids mediate HOXA11 expression in the human peri-implantation endometrium. J Clin Endocrinol Metab 1999; 84:1129-1135.
13. Gendron RL, Paradis H, Hsieh-Li HM et al. Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biol Reprod 1997; 56:1097-1105.
14. Ma L, Benson GV, Lim H et al. 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 1998; 197:141-154.
15. Akbas GE, Song J, Taylor HS. A HOXA10 estrogen response element (ERE) is differentially regulated by 17 beta-estradiol and diethylstilbestrol (DES). J Mol Biol 2004; 340:1013-1023.
16. Martin R, Taylor MB, Krikun G et al. Differential cell-specific modulation of HOXA10 by estrogen and specificity protein 1 response elements. J Clin Endocrinol Metab 2007; 92:1920-1926.
17. 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.
18. Qian K, Chen H, Wei Y et al. Differentiation of endometrial stromal cells in vitro: down-regulation of suppression of the cell cycle inhibitor p57 by HOXA10? Mol Hum Reprod 2005; 11:245-251.
19. Hsieh-Li HM, Witte DP, Weinstein M et al. Hoxa 11 structure, extensive antisense transcription, and function in male and female fertility. Development 1995; 121:1373-1385.
20. Satokata I, Benson G, Maas R. Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice. Nature 1995; 374:460-463.
21. Bagot CN, Troy PJ, Taylor HS. Alteration of maternal Hoxa10 expression by in vivo gene transfection affects implantation. Gene Ther 2000; 7:1378-1384.
22. Nikas G, Drakakis P, Loutradis D et al. Uterine pinopodes as markers of the 'nidation window' in cycling women receiving exogenous oestradiol and progesterone. Hum Reprod 1995; 10: 1208-1213.
23. Singh MM, Chauhan SC, Trivedi RN et al. Correlation of pinopod development on uterine luminal epithelial surface with hormonal events and endometrial sensitivity in rat. Eur J Endocrinol 1996; 135:107-117.
24. Bagot CN, Kliman HJ, Taylor HS. Maternal Hoxa10 is required for pinopod formation in the development of mouse uterine receptivity to embryo implantation. Dev Dyn 2001; 222:538-544.
25. Lessey BA, Damjanovich L, Coutifaris C et al. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J Clin Invest 1992; 90:188-195.
26. Sueoka K, Shiokawa S, Miyazaki T et al. Integrins and reproductive physiology: expression and modulation in fertilization, embryogenesis, and implantation. Fertil Steril 1997; 67:799-811.
27. Daftary GS, Troy PJ, Bagot CN et al. Direct regulation of beta3-integrin subunit gene expression by HOXA10 in endometrial cells. Mol Endocrinol 2002; 16:571-579.
28. Hustin J, Philippe E, Teisner B et al. Immunohistochemical localization of two endometrial proteins in the early days of human pregnancy. Placenta 1994; 15:701-708.
29. Irwin JC, Suen LF, Faessen GH et al. Insulin-like growth factor (IGF)-II inhibition of endometrial stromal cell tissue inhibitor of metalloproteinase-3 and IGF-binding protein-1 suggests paracrine interactions at the decidua:trophoblast interface during human implantation. J Clin Endocrinol Metab 2001; 86:2060-2064.
30. Foucher I, Volovitch M, Frain M et al. Hoxa5 overexpression correlates with IGFBP1 upregulation and postnatal dwarfism: evidence for an interaction between Hoxa5 and Forkhead box transcription factors. Development 2002; 129:4065-4074.
31. Kim JJ, Jaffe RC, Fazleabas AT. Insulin-like growth factor binding protein-1 expression in baboon endometrial stromal cells: regulation by filamentous actin and requirement for de novo protein synthesis. Endocrinology 1999; 140:997-1004.
32. Kim JJ, Taylor HS, Lu Z et al. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol Hum Reprod 2007; 13:323-332.
33. Taylor HS, Bagot C, Kardana A et al. HOX gene expression is altered in the endometrium of women with endometriosis. Hum Reprod 1999; 14:1328-1331.
34. Houston DE. Evidence for the risk of pelvic endometriosis by age, race and socioeconomic status. Epidemiol Rev 1984; 6:167-191.
35. Strathy JH, Molgaard CA, Coulam CB et al. Endometriosis and infertility: a laparoscopic study of endometriosis among fertile and infertile women. Fertil Steril 1982; 38:667-672.
36. Simon C, Gutierrez A, Vidal A et al. Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod 1994; 9:725-729.
37. Tummon IS, Maclin VM, Radwanska E et al. Occult ovulatory dysfunction in women with minimal endometriosis or unexplained infertility. Fertil Steril 1988; 50:716-720.
38. Ulukus M, Cakmak H, Arici A. The role of endometrium in endometriosis. J Soc Gynecol Invest 2006; 13:467-476.
39. Lee B, Du H, Taylor HS. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod 2009; 80:79-85.
40. Fazleabas AT, Brudney A, Chai D et al. Steroid receptor and aromatase expression in baboon endometriotic lesions. Fertil Steril 2003; 80(Suppl 2):820-827.
41. 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.
42. Kamat AA, Younes PS, Sayeeduddin M et al. Protein expression profiling of endometriosis: validation of 2-mm tissue microarrays. Fertil Steril 2004; 82:1681-1683.
43. Kao LC, Germeyer A, Tulac S et al. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003; 144:2870-2881.
44. Klemmt PA, Carver JG, Kennedy SH et al. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril 2006; 85:564-572.
45. Lessey BA, Castelbaum AJ, Sawin SW et al. Aberrant integrin expression in the endometrium of women with endometriosis. J Clin Endocrinol Metab 1994; 79:643-649.
46. Vitiello D, Kodaman PH, Taylor HS. HOX genes in implantation. Semin Reprod Med 2007; 25:431-436.
47. Troy PJ, Daftary GS, Bagot CN et al. Transcriptional repression of peri-implantation EMX2 expression in mammalian reproduction by HOXA10. Mol Cell Biol 2003; 23:1-13.
48. 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 2004; 89:2390-2396.
49. Taylor HS, Fei X. Emx2 regulates mammalian reproduction by altering endometrial cell proliferation. Mol Endocrinol 2005; 19:2839-2846.
50. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293:1089-1093.
51. Robertson KD. DNA methylation and human disease. Nat Rev Genet 2005; 6:597-610.
52. Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril 2002; 77:1148-1155.
53. Wu Y, Halverson G, Basir Z et al. Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am J Obstet Gynecol 2005; 193:371-380.
54. Wu Y, Strawn E, Basir Z et al. Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis. Fertil Steril 2007; 87:24-32.
55. Sutton CJ, Ewen SP, Whitelaw N et al. Prospective, randomized, double- blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis. Fertil Steril 1994; 62:696-700.
56. Sutton CJ, Pooley AS, Ewen SP et al. Follow-up report on a randomized controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal to moderate endometriosis. Fertil Steril 1997; 68:1070-1074.
57. Marcoux S, Maheux R, Berube S. Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian Collaborative Group on Endometriosis. N Engl J Med 1997; 337:217-222.
58. Chan RW, Gargett CE. Identification of label-retaining cells in mouse endometrium. Stem Cells 2006; 24:1529-1538.
59. Chan RW, Schwab KE, Gargett CE. Clonogenicity of human endometrial epithelial and stromal cells. Biol Reprod 2004; 70:1738-1750.
60. Dimitrov R, Timeva T, Kyurkchiev D et al. Characterization of clonogenic stromal cells isolated from human endometrium. Reproduction 2008; 135:551-558.
61. Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA 2004; 292:81-85.
62. Du H, Taylor HS. Contribution of bone marrow-derived stem cells to endometrium and endometriosis. Stem Cells 2007; 25:2082-2086.