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01-09-2015 | Clinical

Clinical translation for endometrial cancer stem cells hypothesis

Authors: Maria João Carvalho, Mafalda Laranjo, Ana Margarida Abrantes, Isabel Torgal, Maria Filomena Botelho, Carlos Freire Oliveira

Published in: Cancer and Metastasis Reviews | Issue 3/2015

Abstract

Endometrial cancer is the most frequent gynecological malignancy in developed world. Cancer stem cells (CSC) are recognized as a small proportion of cells among the tumor cell population that are capable of self-renewal, aberrant differentiation, and escape homeostasis. This review aims to systematize the existing evidence of CSC of endometrial cancer and its clinical translation. In endometrial cancer, the cancer stem cell hypothesis has been studied in vitro using the isolation of colony forming units, side population with dye efflux capacity, and tumorospheres. The stem cell markers for endometrial cancer do not have uniform characteristics, albeit CD133 and aldehyde dehydrogenase (ALDH) were being associated with CSC phenotype. The application of endometrial CSC on xenograft models proves the tumorigenic capacity of this small group of cells. The metastatic process has been explained due to epithelial-mesenchymal transition (EMT) in which CSC seems to have a critical role. The chemoresistance is characteristic of CSC that in endometrial cancer has been shown in CSC phenotype and associated with CSC markers. The most ambitious potential for CSC is the development of targeted therapies. Its application on endometrial cancer is still poor, being a future perspective for research.

Colombo, N., Preti, E., Landoni, F., Carinelli, S., Colombo, a, Marini, C., Sessa, C. (2011). Endometrial cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of Oncology/ ESMO, 22 Suppl 6(Supplement 6), vi35–9. doi:10.1093/annonc/mdr374

Burke, W. M., Orr, J., Leitao, M., Salom, E., Gehrig, P., Olawaiye, A. B., & Abu Shahin, F. (2014). Endometrial cancer: a review and current management strategies: part I. Gynecologic Oncology, 134(2), 385–392. doi:10.1016/j.ygyno.2014.05.018.CrossRefPubMed

Fambrini, M., Sorbi, F., Sisti, G., Cioni, R., Turrini, I., Taddei, G., & Guaschino, S. (2014). Endometrial carcinoma in high-risk populations: is it time to consider a screening policy? Cytopathology, 25(2), 71–77. doi:10.1111/cyt.12131.CrossRefPubMed

Weiderpass, E., Antoine, J., Bray, F. I., Oh, J. K., & Arbyn, M. (2014). Trends in corpus uteri cancer mortality in member states of the European Union. European Journal of Cancer, 50(9), 1675–1684. doi:10.1016/j.ejca.2014.02.020.CrossRefPubMed

Murali, R., Soslow, R. A., & Weigelt, B. (2014). Classification of endometrial carcinoma: more than two types. The Lancet Oncology, 15(7), e268–78. doi:10.1016/S1470-2045(13)70591-6.CrossRefPubMed

Pike, M. C., Peters, R. K., Cozen, W., Probst-Hensch, N. M., Wan, P. C., Mack, T. M., & Felix, J. C. (1997). Estrogen-progestin replacement therapy and endometrial cancer. Journal of the National Cancer Institute, 89(15), 1110–1116. doi:10.1093/jnci/89.15.1110.CrossRefPubMed

Soliman, P. T., Wu, D., Tortolero-Luna, G., Schmeler, K. M., Slomovitz, B. M., Bray, M. S., & Lu, K. H. (2006). Association between adiponectin, insulin resistance, and endometrial cancer. Cancer, 106(11), 2376–2381. doi:10.1002/cncr.21866.CrossRefPubMed

Fisher, B., Costantino, J. P., Redmond, C. K., Fisher, E. R., Wickerham, D. L., & Cronin, W. M. (1994). Endometrial cancer in tamoxifen-treated breast cancer patients: findings from the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-14. Journal of the National Cancer Institute, 86(7), 527–537. doi:10.1093/jnci/86.7.527.CrossRefPubMed

Zhou, B., Yang, L., Sun, Q., Cong, R., Gu, H., Tang, N., & Wang, B. (2008). Cigarette smoking and the risk of endometrial cancer: a meta-analysis. The American journal of medicine, 121(6), 501–508.e3. doi:10.1016/j.amjmed.2008.01.044.CrossRefPubMed

10.

Timmermans, A., Opmeer, B. C., Khan, K. S., Bachmann, L. M., Epstein, E., Clark, T. J., & Mol, B. W. J. (2010). Endometrial thickness measurement for detecting endometrial cancer in women with postmenopausal bleeding: a systematic review and meta-analysis. Obstetrics and Gynecology, 116(1), 160–167. doi:10.1097/AOG.0b013e3181e3e7e8.CrossRefPubMed

11.

Bokhman, J. V. (1983). Two pathogenetic types of endometrial carcinoma. Gynecologic Oncology, 15(1), 10–17.CrossRefPubMed

12.

Chiang, S., & Soslow, R. A. (2014). Updates in diagnostic immunohistochemistry in endometrial carcinoma. Seminars in Diagnostic Pathology, 31(3), 205–215. doi:10.1053/j.semdp.2014.03.002.CrossRefPubMed

13.

Simpkins, S. B., Peiffer-Schneider, S., Mutch, D. G., Gersell, D., & Goodfellow, P. J. (1998). PTEN mutations in endometrial cancers with 10q LOH: additional evidence for the involvement of multiple tumor suppressors. Gynecologic Oncology, 71(3), 391–395. doi:10.1006/gyno.1998.5208.CrossRefPubMed

14.

Darvishian, F., Hummer, A. J., Thaler, H. T., Bhargava, R., Linkov, I., Asher, M., & Soslow, R. A. (2004). Serous endometrial cancers that mimic endometrioid adenocarcinomas: a clinicopathologic and immunohistochemical study of a group of problematic cases. The American Journal of Surgical Pathology, 28(12), 1568–1578.CrossRefPubMed

15.

Llauradó, M., Ruiz, A., Majem, B., Ertekin, T., Colás, E., Pedrola, N., & Reventós, J. (2012). Molecular bases of endometrial cancer: new roles for new actors in the diagnosis and the therapy of the disease. Molecular and Cellular Endocrinology, 358(2), 244–255. doi:10.1016/j.mce.2011.10.003.CrossRefPubMed

16.

Zannoni, G. F., Vellone, V. G., Arena, V., Prisco, M. G., Scambia, G., Carbone, A., & Gallo, D. (2010). Does high-grade endometrioid carcinoma (grade 3 FIGO) belong to type I or type II endometrial cancer? A clinical-pathological and immunohistochemical study. Virchows Archiv, 457(1), 27–34. doi:10.1007/s00428-010-0939-z.CrossRefPubMed

17.

Yamamoto, S., Tsuda, H., Aida, S., Shimazaki, H., Tamai, S., & Matsubara, O. (2007). Immunohistochemical detection of hepatocyte nuclear factor 1beta in ovarian and endometrial clear-cell adenocarcinomas and nonneoplastic endometrium. Human Pathology, 38(7), 1074–1080. doi:10.1016/j.humpath.2006.12.018.CrossRefPubMed

18.

Moreno-Bueno, G., Hardisson, D., Sarrió, D., Sánchez, C., Cassia, R., Prat, J., & Palacios, J. (2003). Abnormalities of E- and P-cadherin and catenin (beta-, gamma-catenin, and p120ctn) expression in endometrial cancer and endometrial atypical hyperplasia. The Journal of Pathology, 199(4), 471–478. doi:10.1002/path.1310.CrossRefPubMed

19.

Schlosshauer, P. W., Ellenson, L. H., & Soslow, R. A. (2002). Beta-catenin and E-cadherin expression patterns in high-grade endometrial carcinoma are associated with histological subtype. Modern Pathology, 15(10), 1032–1037. doi:10.1097/01.MP.0000028573.34289.04.CrossRefPubMed

20.

Cheung, L. W. T., Hennessy, B. T., Li, J., Yu, S., Myers, A. P., Djordjevic, B., & Mills, G. B. (2011). High frequency of PIK3R1 and PIK3R2 mutations in endometrial cancer elucidates a novel mechanism for regulation of PTEN protein stability. Cancer Discovery, 1(2), 170–185. doi:10.1158/2159-8290.CD-11-0039.PubMedCentralCrossRefPubMed

21.

McConechy, M. K., Ding, J., Cheang, M. C. U., Wiegand, K. C., Senz, J., Tone, A. A., & Huntsman, D. G. (2012). Use of mutation profiles to refine the classification of endometrial carcinomas. Journal of Pathology. doi:10.1002/path.4056.PubMedCentralPubMed

22.

Tashiro, H., Isacson, C., Levine, R., Kurman, R. J., Cho, K. R., & Hedrick, L. (1997). p53 gene mutations are common in uterine serous carcinoma and occur early in their pathogenesis. The American Journal of Pathology, 150(1), 177–185.PubMedCentralPubMed

23.

Jia, L., Liu, Y., Yi, X., Miron, A., Crum, C. P., Kong, B., & Zheng, W. (2008). Endometrial glandular dysplasia with frequent p53 gene mutation: a genetic evidence supporting its precancer nature for endometrial serous carcinoma. Clinical Cancer Research, 14(8), 2263–2269. doi:10.1158/1078-0432.CCR-07-4837.CrossRefPubMed

24.

Network, C. G. A. R., Institute, G. sequencing centres: B., Getz, G., Gabriel, S. B., Cibulskis, K., Lander, E., … Committee, W. (2013). Integrated genomic characterization of endometrial carcinoma. Nature, 497(7447), 67–73. doi:10.1038/nature12113

25.

Gargett, C. E., & Masuda, H. (2010). Adult stem cells in the endometrium. Molecular Human Reproduction, 16(11), 818–834. doi:10.1093/molehr/gaq061.CrossRefPubMed

26.

Gargett, C. E., Chan, R. W. S., & Schwab, K. E. (2008). Hormone and growth factor signaling in endometrial renewal: role of stem/progenitor cells. Molecular and Cellular Endocrinology, 288(1-2), 22–29. doi:10.1016/j.mce.2008.02.026.CrossRefPubMed

27.

Salamonsen, L. A. (2003). Tissue injury and repair in the female human reproductive tract. Reproduction, 125(3), 301–311. doi:10.1530/rep.0.1250301.CrossRefPubMed

28.

Giudice, L. C. (2003). Elucidating endometrial function in the post-genomic era. Human Reproduction Update, 9(3), 223–235. doi:10.1093/humupd/dmg019.CrossRefPubMed

29.

Chan, R. W. S., Schwab, K. E., & Gargett, C. E. (2004). Clonogenicity of human endometrial epithelial and stromal cells. Biology of Reproduction, 70(6), 1738–1750. doi:10.1095/biolreprod.103.024109.CrossRefPubMed

30.

Kato, K., Yoshimoto, M., Kato, K., Adachi, S., Yamayoshi, A., Arima, T., & Wake, N. (2007). Characterization of side-population cells in human normal endometrium. Human Reproduction, 22(5), 1214–1223. doi:10.1093/humrep/del514.CrossRefPubMed

31.

Chan, R. W. S., & Gargett, C. E. (2006). Identification of label-retaining cells in mouse endometrium. Stem cells, 24(6), 1529–1538. doi:10.1634/stemcells.2005-0411.CrossRefPubMed

32.

Cervelló, I., Martínez-Conejero, J. A., Horcajadas, J. A., Pellicer, A., & Simón, C. (2007). Identification, characterization and co-localization of label-retaining cell population in mouse endometrium with typical undifferentiated markers. Human Reproduction (Oxford, England), 22(1), 45–51. doi:10.1093/humrep/del332.CrossRef

33.

Götte, M., Wolf, M., Staebler, A., Buchweitz, O., Kelsch, R., Schüring, A. N., & Kiesel, L. (2008). Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. The Journal of Pathology, 215(3), 317–329. doi:10.1002/path.2364.CrossRefPubMed

34.

Visvader, J. E., & Lindeman, G. J. (2008). Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nature Reviews Cancer, 8(10), 755–768. doi:10.1038/nrc2499.CrossRefPubMed

35.

Allegra, A., Alonci, A., Penna, G., Innao, V., Gerace, D., Rotondo, F., & Musolino, C. (2014). The cancer stem cell hypothesis: a guide to potential molecular targets. Cancer Investigation, 32(9), 470–495. doi:10.3109/07357907.2014.958231.CrossRefPubMed

36.

Rosen, J. M., & Jordan, C. T. (2009). The increasing complexity of the cancer stem cell paradigm. Science, 324(5935), 1670–1673.PubMedCentralCrossRefPubMed

37.

Hubbard, S. A., & Gargett, C. E. (2010). A cancer stem cell origin for human endometrial carcinoma? Reproduction, 140(1), 23–32. doi:10.1530/REP-09-0411.CrossRefPubMed

38.

Tang, D. G. (2012). Understanding cancer stem cell heterogeneity and plasticity. Cell Research, 22(3), 457–472. doi:10.1038/cr.2012.13.PubMedCentralCrossRefPubMed

39.

Skidan, I., & Steiniger, S. (2014). Review article in vivo models for cancer stem cells research: a clinical guide. Jornal of Physiology and Pharmacology, 65(2), 157–169.

40.

Charafe-Jauffret, E., Ginestier, C., & Birnbaum, D. (2009). Breast cancer stem cells: tools and models to rely on. BMC Cancer, 9, 202. doi:10.1186/1471-2407-9-202.PubMedCentralCrossRefPubMed

41.

Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J., & Clarke, M. F. (2003). Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 3983–3988. doi:10.1073/pnas.0530291100.PubMedCentralCrossRefPubMed

42.

Morel, A. P., Lièvre, M., Thomas, C., Hinkal, G., Ansieau, S., & Puisieux, A. (2008). Generation of breast cancer stem cells through epithelial-mesenchymal transition. PloS One, 3(8), e2888. doi:10.1371/journal.pone.0002888.PubMedCentralCrossRefPubMed

43.

Onder, T. T., Gupta, P. B., Mani, S. A., Yang, J., Lander, E. S., & Weinberg, R. A. (2008). Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Research, 68(10), 3645–3654. doi:10.1158/0008-5472.CAN-07-2938.CrossRefPubMed

44.

Eramo, A., Lotti, F., Sette, G., Pilozzi, E., Biffoni, M., Di Virgilio, A., & De Maria, R. (2008). Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death and Differentiation, 15, 504–514. doi:10.1038/sj.cdd.4402283.CrossRefPubMed

45.

Zhang, W. C., Ng, S. C., Yang, H., Rai, A., Umashankar, S., Ma, S., & Lim, B. (2012). Glycine decarboxylase activity drives non-small cell lung cancer tumor-initiating cells and tumorigenesis. Cell, 148(1-2), 259–272. doi:10.1016/j.cell.2011.11.050.CrossRefPubMed

46.

Yamashita, T., Ji, J., Budhu, A., Forgues, M., Yang, W., Wang, Y., Wang, X. W. (2010). NIH Public Access, 136(3), 1012–1024. doi:10.1053/j.gastro.2008.12.004.EpCAM-positive.

47.

López, J., Valdez-Morales, F. J., Benítez-Bribiesca, L., Cerbón, M., & Carrancá, A. G. (2013). Normal and cancer stem cells of the human female reproductive system. Reproductive Biology and Endocrinology : RB&E, 11(Table 2), 53. 10.1186/1477-7827-11-53

48.

Silva, I. A., Bai, S., McLean, K., Yang, K., Griffith, K., Thomas, D., & Buckanovich, R. J. (2011). Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Research, 71(11), 3991–4001. doi:10.1158/0008-5472.CAN-10-3175.PubMedCentralCrossRefPubMed

49.

Islam, F., Qiao, B., Smith, R. A., Gopalan, V., & Lam, A. K. Y. (2015). Cancer stem cell: Fundamental experimental pathological concepts and updates. Experimental and Molecular Pathology. doi:10.1016/j.yexmp.2015.02.002.PubMed

50.

Gorai, I., Yanagibashi, T., Taki, A., Udagawa, K., Miyagi, E., Nakazawa, T., & Minaguchi, H. (1997). Uterine carcinosarcoma is derived from a single stem cell: an in vitro study. International Journal of Cancer, 72(December 1996), 821–827. doi:10.1002/(SICI)1097-0215(19970904)72:5<821::AID-IJC19>3.0.CO;2-B.CrossRef

51.

Hubbard, S. A., Friel, A. M., Kumar, B., Zhang, L., Rueda, B. R., & Gargett, C. E. (2009). Evidence for cancer stem cells in human endometrial carcinoma. Cancer Research, 69(21), 8241–8248. doi:10.1158/0008-5472.CAN-08-4808.CrossRefPubMed

52.

Friel, A. M., Sergent, P. A., Patnaude, C., Szotek, P. P., Oliva, E., Scadden, D. T., & Rueda, B. R. (2008). Functional analyses of the cancer stem cell-like properties of human endometrial tumor initiating cells. Cell Cycle, 7(2), 242–249. doi:10.4161/cc.7.2.5207.CrossRefPubMed

53.

Kato, K., Takao, T., Kuboyama, A., Tanaka, Y., Ohgami, T., Yamaguchi, S., & Wake, N. (2010). Endometrial cancer side-population cells show prominent migration and have a potential to differentiate into the mesenchymal cell lineage. The American Journal of Pathology, 176(1), 381–392. doi:10.2353/ajpath.2010.090056.PubMedCentralCrossRefPubMed

54.

Tomiyasu, S., Miyamoto, T., Mori, M., Yaguchi, T., Yakushiji, H., Ohno, S., & Ohno, E. (2014). Isolation of side population cells from endometrial cancer cells using a violet laser diode. Human Cell, 27, 36–42. doi:10.1007/s13577-013-0079-2.CrossRefPubMed

55.

Götte, M., Greve, B., Kelsch, R., Müller-Uthoff, H., Weiss, K., Kharabi Masouleh, B., & Buchweitz, O. (2011). The adult stem cell marker Musashi-1 modulates endometrial carcinoma cell cycle progression and apoptosis via Notch-1 and p21WAF1/CIP1. International Journal of Cancer, 129(8), 2042–2049. doi:10.1002/ijc.25856.CrossRef

56.

Zhou, X., Zhou, Y.-P., Huang, G.-R., Gong, B.-L., Yang, B., Zhang, D.-X., & Xu, S.-R. (2011). Expression of the stem cell marker, Nanog, in human endometrial adenocarcinoma. International Journal of Gynecological Pathology, 30(3), 262–270. doi:10.1097/PGP.0b013e3182055a1f.PubMedCentralCrossRefPubMed

57.

Park, I.-H., Zhao, R., West, J. A., Yabuuchi, A., Huo, H., Ince, T. A., & Daley, G. Q. (2008). Reprogramming of human somatic cells to pluripotency with defined factors. Nature, 451, 141–146. doi:10.1038/nature06534.CrossRefPubMed

58.

Wu, Y., Liu, S., Xin, H., Jiang, J., Younglai, E., Sun, S., & Wang, H. (2011). Up-regulation of microRNA-145 promotes differentiation by repressing OCT4 in human endometrial adenocarcinoma cells. Cancer, 117(17), 3989–3998. doi:10.1002/cncr.25944.CrossRefPubMed

59.

Honig, A., Weidler, C., Häusler, S., Krockenberger, M., Buchholz, S., Köster, F., & Engel, J. B. (2010). Overexpression of polycomb protein BMI-1 in human specimens of breast, ovarian, endometrial and cervical cancer. Anticancer Research, 30(5), 1559–1564.PubMed

60.

Dong, P., Kaneuchi, M., Watari, H., Hamada, J., Sudo, S., Ju, J., & Sakuragi, N. (2011). MicroRNA-194 inhibits epithelial to mesenchymal transition of endometrial cancer cells by targeting oncogene BMI-1. Molecular Cancer, 10, 99. doi:10.1186/1476-4598-10-99.PubMedCentralCrossRefPubMed

61.

Yang, M.-H., Hsu, D. S.-S., Wang, H.-W., Wang, H.-J., Lan, H.-Y., Yang, W.-H., & Wu, K.-J. (2010). Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nature Cell Biology, 12(10), 982–992. doi:10.1038/ncb2099.CrossRefPubMed

62.

Chang, S.-J., Wang, T.-Y., Tsai, C.-Y., Hu, T.-F., Chang, M. D.-T., & Wang, H.-W. (2009). Increased epithelial stem cell traits in advanced endometrial endometrioid carcinoma. BMC Genomics, 10, 613. doi:10.1186/1471-2164-10-613.PubMedCentralCrossRefPubMed

63.

Mirantes, C., Espinosa, I., Ferrer, I., Dolcet, X., Prat, J., & Matias-Guiu, X. (2013). Epithelial-to-mesenchymal transition and stem cells in endometrial cancer. Human Pathology, 44(10), 1973–1981. doi:10.1016/j.humpath.2013.04.009.CrossRefPubMed

64.

Cervelló, I., Mirantes, C., Santamaria, X., Dolcet, X., Matias-Guiu, X., & Simón, C. (2011). Stem cells in human endometrium and endometrial carcinoma. International Journal of Gynecological Pathology, 30(4), 317–327. doi:10.1097/PGP.0b013e3182102754.CrossRefPubMed

65.

Dong, P., Kaneuchi, M., Konno, Y., Watari, H., Sudo, S., & Sakuragi, N. (2013). Emerging therapeutic biomarkers in endometrial cancer. BioMed Research International. doi:10.1155/2013/130362.

66.

Kusunoki, S., Kato, K., Tabu, K., Inagaki, T., Okabe, H., Kaneda, H., & Takeda, S. (2013). The inhibitory effect of salinomycin on the proliferation, migration and invasion of human endometrial cancer stem-like cells. Gynecologic Oncology, 129, 598–605. doi:10.1016/j.ygyno.2013.03.005.CrossRefPubMed

67.

Yusuf, N., Inagaki, T., Kusunoki, S., Okabe, H., Yamada, I., Matsumoto, A., & Kato, K. (2014). SPARC was overexpressed in human endometrial cancer stem-like cells and promoted migration activity. Gynecologic Oncology, 134, 356–363. doi:10.1016/j.ygyno.2014.04.009.CrossRefPubMed

68.

Kim, J. Y., Tavaré, S., & Shibata, D. (2005). Counting human somatic cell replications: methylation mirrors endometrial stem cell divisions. Proceedings of the National Academy of Sciences of the United States of America, 102(49), 17739–17744. doi:10.1073/pnas.0503976102.PubMedCentralCrossRefPubMed

69.

Friel, A. M., Zhang, L., Curley, M. D., Therrien, V. A., Sergent, P. A., Belden, S. E., & Rueda, B. R. (2010). Epigenetic regulation of CD133 and tumorigenicity of CD133 positive and negative endometrial cancer cells. Reproductive Biology and Endocrinology, 8(1), 147. doi:10.1186/1477-7827-8-147.PubMedCentralCrossRefPubMed

70.

Dong, P., Konno, Y., Watari, H., Hosaka, M., Noguchi, M., & Sakuragi, N. (2014). The impact of microRNA-mediated PI3K/AKT signaling on epithelial-mesenchymal transition and cancer stemness in endometrial cancer. Journal of Translational Medicine, 12(1), 231. doi:10.1186/s12967-014-0231-0.PubMedCentralCrossRefPubMed

71.

Zhou, X., Gao, Q., Wang, J., Zhang, X., Liu, K., & Duan, Z. (2014). Linc-RNA-RoR acts as a “sponge” against mediation of the differentiation of endometrial cancer stem cells by microRNA-145. Gynecologic Oncology, 133(2), 333–339. doi:10.1016/j.ygyno.2014.02.033.CrossRefPubMed

72.

Gao, Y., Liu, T., & Huang, Y. (2015). MicroRNA-134 suppresses endometrial cancer stem cells by targeting POGLUT1 and Notch pathway proteins. FEBS Letters, 589(2), 207–214. doi:10.1016/j.febslet.2014.12.002.CrossRefPubMed

73.

Konno, Y., Dong, P., Xiong, Y., Suzuki, F., & Lu, J. (2014). MicroRNA-101 targets EZH2, MCL-1 and FOS to suppress proliferation, invasion and stem cell-like phenotype of aggressive endometrial cancer cells. Oncotarget, 5(15), 6049–6062.PubMedCentralCrossRefPubMed

74.

Li, a, Jiao, Y., Yong, K. J., Wang, F., Gao, C., Yan, B., Chai, L. (2013). SALL4 is a new target in endometrial cancer. Oncogene, (November 2013), 1–10. doi:10.1038/onc.2013.529.

75.

Ginestier, C., Hur, M. H., Charafe-Jauffret, E., Monville, F., Dutcher, J., Brown, M., & Dontu, G. (2007). ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell, 1(5), 555–567. doi:10.1016/j.stem.2007.08.014.PubMedCentralCrossRefPubMed

76.

Rahadiani, N., Ikeda, J., Mamat, S., Matsuzaki, S., Ueda, Y., Umehara, R., & Morii, E. (2011). Expression of aldehyde dehydrogenase 1 (ALDH1) in endometrioid adenocarcinoma and its clinical implications. Cancer Science, 102(4), 903–908. doi:10.1111/j.1349-7006.2011.01864.x.CrossRefPubMed

77.

Mamat, S., Ikeda, J.-I., Tian, T., Wang, Y., Luo, W., Aozasa, K., & Morii, E. (2011). Transcriptional regulation of aldehyde dehydrogenase 1A1 gene by alternative spliced forms of nuclear factor Y in tumorigenic population of endometrial adenocarcinoma. Genes & Cancer, 2(10), 979–984. doi:10.1177/1947601911436009.CrossRef

78.

Mizrak, D., Brittan, M., & Alison, M. R. (2008). CD133: molecule of the moment. The Journal of Pathology, 214, 3–9. doi:10.1002/path.2283.CrossRefPubMed

79.

Rutella, S., Bonanno, G., Procoli, A., Mariotti, A., Corallo, M., Prisco, M. G., & Ferrandina, G. (2009). Cells with characteristics of cancer stem/progenitor cells express the CD133 antigen in human endometrial tumors. Clinical Cancer Research, 15(13), 4299–4311. doi:10.1158/1078-0432.CCR-08-1883.CrossRefPubMed

80.

Nakamura, M., Kyo, S., Zhang, B., Zhang, X., Mizumoto, Y., Takakura, M., & Inoue, M. (2010). Prognostic impact of CD133 expression as a tumor-initiating cell marker in endometrial cancer. Human Pathology, 41(11), 1516–1529. doi:10.1016/j.humpath.2010.05.006.CrossRefPubMed

81.

Burke, W. M., Orr, J., Leitao, M., Salom, E., Gehrig, P., Olawaiye, A. B., & Shahin, F. A. (2014). Endometrial cancer: a review and current management strategies: part II. Gynecologic Oncology, 134(2), 393–402. doi:10.1016/j.ygyno.2014.06.003.CrossRefPubMed

82.

Vasiliou, V., Vasiliou, K., & Nebert, D. W. (2009). Human ATP-binding cassette (ABC) transporter family. Human Genomics, 3, 281–290. doi:10.1186/1479-7364-3-3-281.PubMedCentralCrossRefPubMed

83.

Cojoc, M., Mäbert, K., Muders, M. H., & Dubrovska, A. (2014). A role for cancer stem cells in therapy resistance: cellular and molecular mechanisms. Seminars in Cancer Biology. doi:10.1016/j.semcancer.2014.06.004.PubMed

84.

Singh, S., Brocker, C., Koppaka, V., Chen, Y., Jackson, B. C., Matsumoto, A., & Vasiliou, V. (2013). Aldehyde dehydrogenases in cellular responses to oxidative/electrophilic stress. Free Radical Biology & Medicine, 56(303), 89–101. doi:10.1016/j.freeradbiomed.2012.11.010.CrossRef

85.

Hirschmann-Jax, C., Foster, A. E., Wulf, G. G., Nuchtern, J. G., Jax, T. W., Gobel, U., & Brenner, M. K. (2004). A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proceedings of the National Academy of Sciences of the United States of America, 101(39), 14228–14233. doi:10.1073/pnas.0400067101.PubMedCentralCrossRefPubMed

86.

Dean, M., Fojo, T., & Bates, S. (2005). Tumour stem cells and drug resistance. Nature Reviews Cancer, 5(April), 275–284. doi:10.1038/nrc1590.CrossRefPubMed

87.

Chen, L., Chang, W.-C., Hung, Y.-C., Chang, Y.-Y., Bao, B.-Y., Huang, H.-C., & Ma, W.-L. (2013). Androgen receptor increases CD133 expression and progenitor-like population that associate with cisplatin resistance in endometrial cancer cell line. Reproductive Sciences (Thousand Oaks, Calif.), 21(3), 386–394. doi:10.1177/1933719113497281.CrossRef

88.

Li, S., & Li, Q. (2014). Cancer stem cells and tumor metastasis (Review). International Journal of Oncology, 44(6), 1806–12. doi:10.3892/ijo.2014.2362.PubMedCentralPubMed

89.

Folkins, C., Shaked, Y., Man, S., Tang, T., Lee, C. R., Zhu, Z., & Kerbel, R. S. (2009). Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1. Cancer Research, 69(18), 7243–7251. doi:10.1158/0008-5472.CAN-09-0167.PubMedCentralCrossRefPubMed

90.

Liao, W. W. W., Ye, Y. Y., Deng, Y. Y., Bian, X. X., & Ding, Y. Y. (2014). Metastatic cancer stem cells : from the concept to therapeutics. Americam Journal of Stem Cells, 3(2), 46–62.

91.

Alonso-alconada, L., Muinelo-Romay, L., Madissoo, K., Diaz-lopez, A., Krakstad, C., Trovik, J., Romano, A. (2014). Molecular profiling of circulating tumor cells links plasticity to the metastatic process in endometrial cancer, 1–10.

92.

Dedes, K. J., Wetterskog, D., Ashworth, A., Kaye, S. B., & Reis-Filho, J. S. (2011). Emerging therapeutic targets in endometrial cancer. Nature reviewsClinical Oncology, 8(5), 261–271. doi:10.1038/nrclinonc.2010.216.CrossRef

93.

Kato, K., Kuhara, A., Yoneda, T., Inoue, T., Takao, T., Ohgami, T., & Wake, N. (2011). Sodium butyrate inhibits the self-renewal capacity of endometrial tumor side-population cells by inducing a DNA damage response. Molecular Cancer Therapeutics, 10(August), 1430–1439. doi:10.1158/1535-7163.MCT-10-1062.CrossRefPubMed

94.

Vanneman, M., & Dranoff, G. (2012). Combining immunotherapy and targeted therapies in cancer treatment. Nature Reviews Cancer. doi:10.1038/nrc3237.PubMedCentralPubMed

Title: Clinical translation for endometrial cancer stem cells hypothesis
Authors: Maria João Carvalho
Mafalda Laranjo
Ana Margarida Abrantes
Isabel Torgal
Maria Filomena Botelho
Carlos Freire Oliveira
Publication date: 01-09-2015
Publisher: Springer US
Published in: Cancer and Metastasis Reviews / Issue 3/2015
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI: https://doi.org/10.1007/s10555-015-9574-0

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