Whole-exome sequencing of endometriosis identifies frequent alterations in genes involved in cell adhesion and chromatin-remodeling complexes

Human Molecular Genetics

Volumn 23, Issue 22, 2014, Pages 6008-6021

  Li, Xiaolei ^a   Zhang, Yan ^a   Zhao, Luyang ^a   Wang, Lingxiong ^a   Wu, Zhiqiang ^a   Mei, Qian ^a   Nie, Jing ^a   Li, Xiang ^a   Li, Yali ^a   Fu, Xiaobing ^a   Wang, Xiaoning ^a   Meng, Yuanguang ^a   Han, Weidong ^a  

^a CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; CHROMATIN;

ARTICLE; BLOOD SAMPLING; CELL ADHESION; CELL JUNCTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; ENDOMETRIUM CELL; EXOME; FEMALE; GENE FREQUENCY; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC RISK; GENETIC VARIABILITY; HUMAN; LASER CAPTURE MICRODISSECTION; MENSTRUATION; MUTATION RATE; PATHOGENESIS; PELVIS; PERITONEUM; PREDICTIVE VALUE; SOMATIC MUTATION; UTERINE TUBE; ADULT; CASE CONTROL STUDY; CHROMATIN; DNA SEQUENCE; GENETIC ASSOCIATION; GENETICS; METABOLISM; MUTATION; PATHOPHYSIOLOGY;

ADULT; CASE-CONTROL STUDIES; CELL ADHESION; CHROMATIN; ENDOMETRIOSIS; EXOME; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MUTATION; SEQUENCE ANALYSIS, DNA;

EID: 84911385472     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu330     Document Type: Article

References (72)

1. Stern, R.C., Dash, R., Bentley, R.C., Snyder, M.J., Haney, A.F. and Robboy, S.J. (2001) Malignancy in endometriosis: frequency and comparison of ovarian and extraovarian types. Int. J. Gynecol. Pathol., 20, 133-139.
2. Bulun, S.E. (2009) Endometriosis. N. Engl. J. Med., 360, 268-279.
3. Giudice, L.C. and Kao, L.C. (2004) Endometriosis. Lancet, 364, 1789-1799.
4. Anonymous. (1985) Revised American Fertility Society classification of endometriosis: 1985. Fertil. Steril., 43, 351-352.
5. Bischoff, F. and Simpson, J.L. (2004) Genetic basis of endometriosis. Ann. N. Y. Acad. Sci., 1034, 284-299.
6. Zondervan, K.T., Cardon, L.R. and Kennedy, S.H. (2001) The genetic basis of endometriosis. Curr. Opin. Obstet. Gynecol., 13, 309-314.
7. Stefansson, H., Geirsson, R.T., Steinthorsdottir, V., Jonsson, H., Manolescu, A., Kong, A., Ingadottir, G., Gulcher, J. and Stefansson, K. (2002) Genetic factors contribute to the risk of developing endometriosis. Hum. Reprod., 17, 555-559.
8. Nyholt, D.R., Low, S.K., Anderson, C.A., Painter, J.N., Uno, S., Morris, A.P.,MacGregor, S., Gordon, S.D., Henders, A.K., Martin, N.G. et al. (2012) Genome-wide association meta-analysis identifies new endometriosis risk loci. Nat. Genet., 44, 1355-1359.
9. Painter, J.N., Anderson, C.A., Nyholt, D.R., Macgregor, S., Lin, J., Lee, S.H., Lambert, A., Zhao, Z.Z., Roseman, F., Guo, Q. et al. (2011) Genome-wide association study identifies a locus at 7p15.2 associated with endometriosis. Nat. Genet., 43, 51-54.
10. Painter, J.N., Nyholt, D.R., Morris, A., Zhao, Z.Z., Henders, A.K., Lambert, A., Wallace, L., Martin, N.G., Kennedy, S.H., Treloar, S.A. et al. (2011) High-density fine-mapping of a chromosome 10q26 linkage peak suggests association between endometriosis and variants close to CYP2C19. Fertil. Steril., 95, 2236-2240.
11. Treloar, S.A., Wicks, J., Nyholt, D.R., Montgomery, G.W., Bahlo, M., Smith, V., Dawson, G., Mackay, I.J., Weeks, D.E., Bennett, S.T. et al. (2005) Genomewide linkage study in 1,176 affected sister pair families identifies a significant susceptibility locus for endometriosis on chromosome 10q26. Am. J. Hum. Genet., 77, 365-376.
12. Uno, S., Zembutsu, H., Hirasawa, A., Takahashi, A., Kubo, M., Akahane, T., Aoki, D., Kamatani, N., Hirata, K. andNakamura, Y. (2010)Agenome-wide association study identifies genetic variants in the CDKN2BAS locus associated with endometriosis in Japanese. Nat. Genet., 42, 707-710.
13. Greenman, C., Stephens, P., Smith, R., Dalgliesh, G.L., Hunter, C., Bignell, G., Davies, H., Teague, J., Butler, A., Stevens, C. et al. (2007) Patterns of somatic mutation in human cancer genomes. Nature, 446, 153-158.
14. Zang, Z.J., Cutcutache, I., Poon, S.L., Zhang, S.L., McPherson, J.R., Tao, J., Rajasegaran, V., Heng, H.L., Deng, N., Gan, A. et al. (2012) Exome sequencing of gastric adenocarcinoma identifies recurrent somatic mutations in cell adhesion and chromatin remodeling genes. Nat. Genet., 44, 570-574.
15. Cancer Genome Atlas, N. (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature, 487, 330-337.
16. Cancer Genome Atlas Research Network, Kandoth, C., Schultz, N., Cherniack, A.D., Akbani, R., Liu, Y., Shen, H., Robertson, A.G., Pashtan, I., Shen, R. et al. (2013) Integrated genomic characterization of endometrial carcinoma. Nature, 497, 67-73.
17. Sato, Y., Yoshizato, T., Shiraishi, Y., Maekawa, S., Okuno, Y., Kamura, T., Shimamura, T., Sato-Otsubo, A., Nagae, G., Suzuki, H. et al. (2013) Integrated molecular analysis of clear-cell renal cell carcinoma. Nat. Genet., 45, 860-867.
18. Ojesina, A.I., Lichtenstein, L., Freeman, S.S., Pedamallu, C.S., Imaz-Rosshandler, I., Pugh, T.J., Cherniack, A.D., Ambrogio, L., Cibulskis, K., Bertelsen, B. et al. (2014) Landscape of genomic alterations in cervical carcinomas. Nature, 506, 371-375.
19. Jones, S., Zhang, X., Parsons, D.W., Lin, J.C., Leary, R.J., Angenendt, P., Mankoo, P., Carter, H., Kamiyama, H., Jimeno, A. et al. (2008) Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science, 321, 1801-1806.
20. Pleasance, E.D., Cheetham, R.K., Stephens, P.J., McBride, D.J., Humphray, S.J., Greenman, C.D., Varela, I., Lin, M.L., Ordonez, G.R., Bignell, G.R. et al. (2010)Acomprehensive catalogue of somatic mutations from a human cancer genome. Nature, 463, 191-196.
21. Walter, M.J., Shen, D., Ding, L., Shao, J., Koboldt, D.C., Chen, K., Larson, D.E., McLellan, M.D., Dooling, D., Abbott, R. et al. (2012) Clonal architecture of secondary acute myeloid leukemia. N. Engl. J. Med., 366, 1090-1098.
22. Welch, J.S., Ley, T.J., Link, D.C., Miller, C.A., Larson, D.E., Koboldt, D.C., Wartman, L.D., Lamprecht, T.L., Liu, F., Xia, J. et al. (2012) The origin and evolution of mutations in acute myeloid leukemia. Cell, 150, 264-278.
23. Sjoblom, T., Jones, S., Wood, L.D., Parsons, D.W., Lin, J., Barber, T.D., Mandelker, D., Leary, R.J., Ptak, J., Silliman, N. et al. (2006) The consensus coding sequences of human breast and colorectal cancers. Science, 314, 268-274.
24. Cancer Genome Atlas Research, N. (2011) Integrated genomic analyses of ovarian carcinoma. Nature, 474, 609-615.
25. Berger, M.F., Lawrence, M.S., Demichelis, F., Drier, Y., Cibulskis, K., Sivachenko, A.Y., Sboner, A., Esgueva, R., Pflueger, D., Sougnez, C. et al. (2011) The genomic complexity of primary human prostate cancer. Nature, 470, 214-220.
26. Chapman, M.A., Lawrence, M.S., Keats, J.J., Cibulskis, K., Sougnez, C., Schinzel, A.C., Harview, C.L., Brunet, J.P., Ahmann, G.J., Adli, M. et al. (2011) Initialgenomesequencing and analysis of multiplemyeloma.Nature, 471, 467-472.
27. Cancer Genome Atlas Research, N. (2012) Comprehensive genomic characterization of squamous cell lung cancers. Nature, 489, 519-525.
28. Locci, R., Nisolle, M., Angioni, S., Foidart, J.M. and Munaut, C. (2013) Expression of the gamma 2 chain of laminin-332 in eutopic and ectopic endometrium of patients with endometriosis. Reprod. Biol. Endocrinol., 11, 94.
29. Sundqvist, J., Andersson, K.L., Scarselli, G., Gemzell-Danielsson, K. and Lalitkumar, P.G. (2012) Expression of adhesion, attachment and invasion markers in eutopic and ectopic endometrium: a link to the aetiology of endometriosis. Hum. Reprod., 27, 2737-2746.
30. Ng, P.C. and Henikoff, S. (2003) SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res., 31, 3812-3814.
31. Adzhubei, I.A., Schmidt, S., Peshkin, L., Ramensky, V.E., Gerasimova, A., Bork, P., Kondrashov, A.S. and Sunyaev, S.R. (2010) A method and server for predicting damaging missense mutations. Nat. Methods, 7, 248-249.
32. Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W.H., Pages, F., Trajanoski, Z. and Galon, J. (2009) ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics, 25, 1091-1093.
33. Bindea, G., Galon, J. and Mlecnik, B. (2013) CluePedia Cytoscape plugin: pathway insights using integrated experimental and in silico data. Bioinformatics, 29, 661-663.
34. Vercellini, P., Vigano, P., Somigliana, E. and Fedele, L. (2013) Endometriosis: pathogenesis and treatment. Nat. Rev. Endocrinol., 10, 261-275.
35. Delbandi, A.A., Mahmoudi, M., Shervin, A., Akbari, E., Jeddi-Tehrani, M., Sankian, M., Kazemnejad, S. and Zarnani, A.H. (2013) Eutopic and ectopic stromal cells from patients with endometriosis exhibit differential invasive, adhesive, and proliferative behavior. Fertil. Steril., 100, 761-769.
36. Dalgliesh, G.L., Furge, K., Greenman, C., Chen, L., Bignell, G., Butler, A., Davies, H., Edkins, S., Hardy, C., Latimer, C. et al. (2010) Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature, 463, 360-363.
37. Fujimoto, A., Totoki, Y., Abe, T., Boroevich, K.A., Hosoda, F., Nguyen, H.H., Aoki, M., Hosono, N., Kubo, M., Miya, F. et al. (2012) Whole-genome sequencing of liver cancers identifies etiological influences on mutation patterns and recurrent mutations in chromatin regulators. Nat. Genet., 44, 760-764.
38. Gui, Y., Guo, G., Huang, Y., Hu, X., Tang, A., Gao, S., Wu, R., Chen, C., Li, X., Zhou, L. et al. (2011) Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat. Genet., 43, 875-878.
39. Jones, S., Wang, T.L., Shih Ie, M., Mao, T.L., Nakayama, K., Roden, R., Glas, R., Slamon, D., Diaz, L.A. Jr., Vogelstein, B. et al. (2010) Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science, 330, 228-231.
40. Le Gallo, M., O'Hara, A.J., Rudd, M.L., Urick, M.E., Hansen, N.F., O'Neil, N.J., Price, J.C., Zhang, S., England, B.M., Godwin, A.K. et al. (2012) Exomesequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes. Nat. Genet., 44, 1310-1315.
41. Church, D.N., Briggs, S.E., Palles, C., Domingo, E., Kearsey, S.J., Grimes, J.M., Gorman, M., Martin, L., Howarth, K.M., Hodgson, S.V. et al. (2013) DNA polymerase epsilon and delta exonuclease domain mutations in endometrial cancer. Hum. Mol. Genet., 22, 2820-2828.
42. Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
43. Huang da, W., Sherman, B.T., Tan, Q., Kir, J., Liu, D., Bryant, D., Guo, Y., Stephens, R., Baseler, M.W., Lane, H.C. et al. (2007) DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res., 35, W169-W175.
44. Giudice, L.C. (2010) Clinical practice. Endometriosis. N. Engl. J. Med., 362, 2389-2398.
45. Dinulescu, D.M., Ince, T.A., Quade, B.J., Shafer, S.A., Crowley, D. and Jacks, T. (2005) Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat. Med., 11, 63-70.
46. Wiegand, K.C., Shah, S.P., Al-Agha, O.M., Zhao, Y., Tse, K., Zeng, T., Senz, J., McConechy, M.K., Anglesio, M.S., Kalloger, S.E. et al. (2010) ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med., 363, 1532-1543.
47. Murphy, A.A. (2002) Clinical aspects of endometriosis. Ann. N. Y. Acad. Sci., 955, 1-10.
48. Bonner, R.F., Emmert-Buck, M., Cole, K., Pohida, T., Chuaqui, R., Goldstein, S. and Liotta, L.A. (1997) Laser capture microdissection: molecular analysis of tissue. Science, 278, 1481, 1483.
49. Wu, Y., Basir, Z., Kajdacsy-Balla, A., Strawn, E., Macias, V., Montgomery, K. and Guo, S.W. (2003) Resolution of clonal origins for endometriotic lesions using laser capture microdissection and thehumanandrogen receptor (HUMARA) assay. Fertil. Steril., 79(Suppl. 1), 710-717.
50. Saare, M., Soritsa, D., Vaidla, K., Palta, P., Remm, M., Laan, M., Karro, H., Soritsa, A., Salumets, A., D'Hooghe, T. et al. (2012) No evidence of somatic DNA copy number alterations in eutopic and ectopic endometrial tissue in endometriosis. Hum. Reprod., 27, 1857-1864.
51. Cooke, P.S., Buchanan, D.L., Young, P., Setiawan, T., Brody, J., Korach, K.S., Taylor, J., Lubahn, D.B. and Cunha, G.R. (1997) Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc. Natl. Acad. Sci. U. S. A., 94, 6535-6540.
52. Sampson, J.A. (1927) Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am. J. Obstet. Gynecol., 14, 422-469.
53. Kyama, C.M., Overbergh, L., Mihalyi, A., Meuleman, C., Mwenda, J.M., Mathieu, C. and D'Hooghe, T.M. (2008) Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis. Fertil. Steril., 89, 301-310.
54. Quenby, S., Anim-Somuah, M., Kalumbi, C., Farquharson, R. and Aplin, J.D. (2007) Different types of recurrent miscarriage are associated with varying patterns of adhesion molecule expression in endometrium. Reprod. Biomed. Online, 14, 224-234.
55. Singh, H. and Aplin, J.D. (2009) Adhesion molecules in endometrial epithelium: tissue integrity and embryo implantation. J. Anat., 215, 3-13.
56. Witz, C.A., Monotoya-Rodriguez, I.A. and Schenken, R.S. (1999) Whole explants of peritoneum and endometrium: a novel model of the early endometriosis lesion. Fertil. Steril., 71, 56-60.
57. Witz, C.A., Takahashi, A., Montoya-Rodriguez, I.A., Cho, S. and Schenken, R.S. (2000) Expression of the alpha2beta1 and alpha3beta1 integrins at the surface of mesothelial cells: a potential attachment site of endometrial cells. Fertil. Steril., 74, 579-584.
58. Dmowski, W.P., Ding, J., Shen, J., Rana, N., Fernandez, B.B. and Braun, D.P. (2001) Apoptosis in endometrial glandular and stromal cells in women with and without endometriosis. Hum. Reprod., 16, 1802-1808.
59. Li, M.Q., Li, H.P., Meng, Y.H., Wang, X.Q., Zhu, X.Y., Mei, J. and Li, D.J. (2012) Chemokine CCL2 enhances survival and invasiveness of endometrial stromal cells in an autocrine manner by activating Akt and MAPK/Erk1/2 signal pathway. Fertil. Steril., 97, 919-929.
60. Aghajanova, L., Tatsumi, K., Horcajadas, J.A., Zamah, A.M., Esteban, F.J., Herndon, C.N., Conti, M. and Giudice, L.C. (2011) Unique transcriptome, pathways, and networks in the human endometrial fibroblast response to progesterone in endometriosis. Biol. Reprod., 84, 801-815.
61. Wu, Y., Kajdacsy-Balla, A., Strawn, E., Basir, Z., Halverson, G., Jailwala, P., Wang, Y., Wang, X., Ghosh, S. and Guo, S.W. (2006) Transcriptional characterizations of differences between eutopic and ectopic endometrium. Endocrinology, 147, 232-246.
62. Sanchez, A.M., Vigano, P., Quattrone, F., Pagliardini, L., Papaleo, E., Candiani, M. and Panina-Bordignon, P. (2014) The WNT/beta-catenin signaling pathway and expression of survival promoting genes in luteinized granulosa cells: endometriosis as a paradigm for a dysregulated apoptosis pathway. Fertil. Steril., doi: 10.1016/j.fertnstert.2014.02.040.
63. Cantley, L.C. (2002) The phosphoinositide 3-kinase pathway. Science, 296, 1655-1657.
64. Chang, L. and Karin, M. (2001) Mammalian MAP kinase signalling cascades. Nature, 410, 37-40.
65. Reya, T. and Clevers, H. (2005) WNT signalling in stem cells and cancer. Nature, 434, 843-850.
66. Maruyama, T. and Yoshimura, Y. (2012) Stem cell theory for the pathogenesis of endometriosis. Front. Biosci., 4, 2854-2863.
67. Forte, A., Cipollaro, M. and Galderisi, U. (2014) Genetic, epigenetic and stem cell alterations in endometriosis: new insights and potential therapeutic perspectives. Clin. Sci., 126, 123-138.
68. Forte, A., Schettino, M.T., Finicelli, M., Cipollaro, M., Colacurci, N., Cobellis, L. and Galderisi, U. (2009) Expression pattern of stemness-related genes in human endometrial and endometriotic tissues. Mol. Med., 15, 392-401.
69. Kitano, H. (2003) Cancer robustness: tumour tactics. Nature, 426, 125.
70. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
71. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M. et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res., 20, 1297-1303.
72. Koboldt, D.C., Zhang, Q., Larson, D.E., Shen, D., McLellan, M.D., Lin, L., Miller, C.A., Mardis, E.R., Ding, L. and Wilson, R.K. (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome res., 22, 568-576.