Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1021-335X Online ISSN: 1791-2431
Journal Cover
August-2017 Volume 38 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
August-2017 Volume 38 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Article

Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro

  • Authors:
    • Julia Eismann
    • Marc Hirschfeld
    • Thalia Erbes
    • Gerta Rücker
    • Markus Jäger
    • Andrea Ritter
    • Daniela Weiss
    • Gerald Gitsch
    • Sebastian Mayer
  • View Affiliations / Copyright

    Affiliations: Department of Obstetrics and Gynecology, Medical Center - University of Freiburg, Freiburg, Germany, Institute for Medical Biometry and Statistics, Medical Center - University of Freiburg, Freiburg, Germany
  • Pages: 993-1004
    |
    Published online on: June 13, 2017
       https://doi.org/10.3892/or.2017.5717
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Due to their post-transcriptional regulatory impact on gene expression, microRNAs (miRNA, miRs) influence decisively cellular processes of differentiation, proliferation and apoptosis. In oncogenic pathways various miRNAs exert either oncogenic or tumor suppressor activities in a stage-specific manner. Dysregulation of miRNA expression pattern has been associated with several human cancers including endometrial cancer (EC). In the present study, expression profile alterations of EC associated secreted miRNAs were determined under the microenvironmental stress situations hypoxia and acidosis occurring in tumor progression and metastasis. The potential influence of hypoxia and acidosis vs. control conditions on the expression levels of 24 EC-relevant miRNA types was quantitatively accessed via real-time PCR in three established EC in vitro models. Expression data were analyzed statistically. In vitro application of hypoxia resulted in downregulation of miR-15a, miR-20a, miR-20b and miR-128-1 in Ishikawa cells (type I EC) and upregulation of miR-21 in EFE-184 cells (type I EC). Acidosis triggered upregulation of tumor promoting miR-125b in AN3-CA cell (type II EC), whereas in Ishikawa cells (type I EC) miRNAs with tumor suppressive function were found altered in divergent directions, both up- (let-7a) and down- (miR-22) regulated. Our current findings emphasize the functional importance of secreted miRNAs in the immediate response of EC cells to exogenic stress situations such as the typical tumor epiphenomena hypoxia and acidosis. Focusing on the specific potential of secreted, thus circulating miRNA molecules, alterations in expression levels not only influence intracellular gene expression and signaling cascades, but also transfer the induction of (tumor)biological cellular changes to adjacent cells.
View Figures

Figure 1

Figure 2

Figure 3

View References

1 

Yanokura M, Banno K, Iida M, Irie H, Umene K, Masuda K, Kobayashi Y, Tominaga E and Aoki D: MicroRNAS in endometrial cancer: Recent advances and potential clinical applications. EXCLI J. 14:190–198. 2015.PubMed/NCBI

2 

Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, et al: MicroRNA signatures in human ovarian cancer. Cancer Res. 67:8699–8707. 2007. View Article : Google Scholar : PubMed/NCBI

3 

Liz J and Esteller M: lncRNAs and microRNAs with a role in cancer development. Biochim Biophys Acta. 1859:169–176. 2016. View Article : Google Scholar : PubMed/NCBI

4 

Lewis BP, Burge CB and Bartel DP: Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 120:15–20. 2005. View Article : Google Scholar : PubMed/NCBI

5 

Sandhu S and Garzon R: Potential applications of microRNAs in cancer diagnosis, prognosis, and treatment. Semin Oncol. 38:781–787. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Thorsen SB, Obad S, Jensen NF, Stenvang J and Kauppinen S: The therapeutic potential of microRNAs in cancer. Cancer J. 18:275–284. 2012. View Article : Google Scholar : PubMed/NCBI

7 

Boren T, Xiong Y, Hakam A, Wenham R, Apte S, Wei Z, Kamath S, Chen DT, Dressman H and Lancaster JM: MicroRNAs and their target messenger RNAs associated with endometrial carcinogenesis. Gynecol Oncol. 110:206–215. 2008. View Article : Google Scholar : PubMed/NCBI

8 

Le XF, Merchant O, Bast RC and Calin GA: The roles of microRNAs in the cancer invasion-metastasis cascade. Cancer Microenviron. 3:137–147. 2010. View Article : Google Scholar : PubMed/NCBI

9 

Ratner ES, Tuck D, Richter C, Nallur S, Patel RM, Schultz V, Hui P, Schwartz PE, Rutherford TJ and Weidhaas JB: MicroRNA signatures differentiate uterine cancer tumor subtypes. Gynecol Oncol. 118:251–257. 2010. View Article : Google Scholar : PubMed/NCBI

10 

Kosaka N, Iguchi H and Ochiya T: Circulating microRNA in body fluid: A new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 101:2087–2092. 2010. View Article : Google Scholar : PubMed/NCBI

11 

Huang YK and Yu JC: Circulating microRNAs and long non-coding RNAs in gastric cancer diagnosis: An update and review. World J Gastroenterol. 21:9863–9886. 2015. View Article : Google Scholar : PubMed/NCBI

12 

Kosaka N and Ochiya T: Unraveling the mystery of cancer by secretory microRNA: Horizontal microRNA transfer between living cells. Front Genet. 2:972012. View Article : Google Scholar : PubMed/NCBI

13 

Turchinovich A, Weiz L, Langheinz A and Burwinkel B: Characterization of extracellular circulating microRNA. Nucleic Acids Res. 39:7223–7233. 2011. View Article : Google Scholar : PubMed/NCBI

14 

Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, et al: Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA. 108:5003–5008. 2011. View Article : Google Scholar : PubMed/NCBI

15 

Wang K, Zhang S, Weber J, Baxter D and Galas DJ: Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 38:7248–7259. 2010. View Article : Google Scholar : PubMed/NCBI

16 

Zhang J, Li S, Li L, Li M, Guo C, Yao J and Mi S: Exosome and exosomal microRNA: Trafficking, sorting, and function. Genomics Proteomics Bioinformatics. 13:17–24. 2015. View Article : Google Scholar : PubMed/NCBI

17 

Siegel RL, Miller KD and Jemal A: Cancer statistics, 2016. CA Cancer J Clin. 66:7–30. 2016. View Article : Google Scholar : PubMed/NCBI

18 

Sorosky JI: Endometrial cancer. Obstet Gynecol. 120:383–397. 2012. View Article : Google Scholar : PubMed/NCBI

19 

Hecht JL and Mutter GL: Molecular and pathologic aspects of endometrial carcinogenesis. J Clin Oncol. 24:4783–4791. 2006. View Article : Google Scholar : PubMed/NCBI

20 

Murali R, Soslow RA and Weigelt B: Classification of endometrial carcinoma: More than two types. Lancet Oncol. 15:e268–e278. 2014. View Article : Google Scholar : PubMed/NCBI

21 

Sianou A, Galyfos G, Moragianni D, Andromidas P, Kaparos G, Baka S and Kouskouni E: The role of microRNAs in the pathogenesis of endometrial cancer: A systematic review. Arch Gynecol Obstet. 292:271–282. 2015. View Article : Google Scholar : PubMed/NCBI

22 

Chung TK, Lau TS, Cheung TH, Yim SF, Lo KW, Siu NS, Chan LK, Yu MY, Kwong J, Doran G, et al: Dysregulation of microRNA-204 mediates migration and invasion of endometrial cancer by regulating FOXC1. Int J Cancer. 130:1036–1045. 2012. View Article : Google Scholar : PubMed/NCBI

23 

Devor EJ, Hovey AM, Goodheart MJ, Ramachandran S and Leslie KK: microRNA expression profiling of endometrial endometrioid adenocarcinomas and serous adenocarcinomas reveals profiles containing shared, unique and differentiating groups of microRNAs. Oncol Rep. 26:995–1002. 2011.PubMed/NCBI

24 

Kontomanolis EN and Koukourakis MI: MicroRNA: The Potential Regulator of Endometrial Carcinogenesis. MicroRNA. 4:18–25. 2015. View Article : Google Scholar : PubMed/NCBI

25 

Myatt SS and Lam EW: The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer. 7:847–859. 2007. View Article : Google Scholar : PubMed/NCBI

26 

Myatt SS, Wang J, Monteiro LJ, Christian M, Ho KK, Fusi L, Dina RE, Brosens JJ, Ghaem-Maghami S and Lam EW: Definition of microRNAs that repress expression of the tumor suppressor gene FOXO1 in endometrial cancer. Cancer Res. 70:367–377. 2010. View Article : Google Scholar : PubMed/NCBI

27 

Hiroki E, Suzuki F, Akahira J, Nagase S, Ito K, Sugawara J, Miki Y, Suzuki T, Sasano H and Yaegashi N: MicroRNA-34b functions as a potential tumor suppressor in endometrial serous adenocarcinoma. Int J Cancer. 131:E395–E404. 2012. View Article : Google Scholar : PubMed/NCBI

28 

Park YA, Lee JW, Choi JJ, Jeon HK, Cho Y, Choi C, Kim TJ, Lee NW, Kim BG and Bae DS: The interactions between MicroRNA-200c and BRD7 in endometrial carcinoma. Gynecol Oncol. 124:125–133. 2012. View Article : Google Scholar : PubMed/NCBI

29 

Snowdon J, Zhang X, Childs T, Tron VA and Feilotter H: The microRNA-200 family is upregulated in endometrial carcinoma. PLoS One. 6:e228282011. View Article : Google Scholar : PubMed/NCBI

30 

Torres A, Torres K, Paszkowski T, Radej S, Staśkiewicz GJ, Ceccaroni M, Pesci A and Maciejewski R: Highly increased maspin expression corresponds with up-regulation of miR-21 in endometrial cancer: a preliminary report. Int J Gynecol Cancer. 21:8–14. 2011. View Article : Google Scholar : PubMed/NCBI

31 

Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, et al: Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 18:997–1006. 2008. View Article : Google Scholar : PubMed/NCBI

32 

Jia W, Wu Y, Zhang Q, Gao G, Zhang C and Xiang Y: Identification of four serum microRNAs from a genome-wide serum microRNA expression profile as potential non-invasive biomarkers for endometrioid endometrial cancer. Oncol Lett. 6:261–267. 2013.PubMed/NCBI

33 

Blick C, Ramachandran A, McCormick R, Wigfield S, Cranston D, Catto J and Harris AL: Identification of a hypoxia-regulated miRNA signature in bladder cancer and a role for miR-145 in hypoxia-dependent apoptosis. Br J Cancer. 113:634–644. 2015. View Article : Google Scholar : PubMed/NCBI

34 

Jung KO, Youn H, Lee CH, Kang KW and Chung JK: Visualization of exosome-mediated miR-210 transfer from hypoxic tumor cells. Oncotarget. 8:9899–9910. 2017.PubMed/NCBI

35 

Dai L, Lou W, Zhu J, Zhou X and Di W: MiR-199a inhibits the angiogenic potential of endometrial stromal cells under hypoxia by targeting HIF-1α/VEGF pathway. Int J Clin Exp Pathol. 8:4735–4744. 2015.PubMed/NCBI

36 

Lin SC, Wang CC, Wu MH, Yang SH, Li YH and Tsai SJ: Hypoxia-induced microRNA-20a expression increases ERK phosphorylation and angiogenic gene expression in endometriotic stromal cells. J Clin Endocrinol Metab. 97:E1515–E1523. 2012. View Article : Google Scholar : PubMed/NCBI

37 

Xu TX, Zhao SZ, Dong M and Yu XR: Hypoxia responsive miR-210 promotes cell survival and autophagy of endometriotic cells in hypoxia. Eur Rev Med Pharmacol Sci. 20:399–406. 2016.PubMed/NCBI

38 

Harris AL: Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer. 2:38–47. 2002. View Article : Google Scholar : PubMed/NCBI

39 

Umezu T, Tadokoro H, Azuma K, Yoshizawa S, Ohyashiki K and Ohyashiki JH: Exosomal miR-135b shed from hypoxic multiple myeloma cells enhances angiogenesis by targeting factor-inhibiting HIF-1. Blood. 124:3748–3757. 2014. View Article : Google Scholar : PubMed/NCBI

40 

Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, et al: A microRNA signature of hypoxia. Mol Cell Biol. 27:1859–1867. 2007. View Article : Google Scholar : PubMed/NCBI

41 

Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, Ji Y, Zhao C, Wang J, Yang BB, et al: MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One. 1:e1162006. View Article : Google Scholar : PubMed/NCBI

42 

Gatenby RA, Gawlinski ET, Gmitro AF, Kaylor B and Gillies RJ: Acid-mediated tumor invasion: A multidisciplinary study. Cancer Res. 66:5216–5223. 2006. View Article : Google Scholar : PubMed/NCBI

43 

Chiche J, Brahimi-Horn MC and Pouysségur J: Tumour hypoxia induces a metabolic shift causing acidosis: A common feature in cancer. J Cell Mol Med. 14:771–794. 2010. View Article : Google Scholar : PubMed/NCBI

44 

Lardner A: The effects of extracellular pH on immune function. J Leukoc Biol. 69:522–530. 2001.PubMed/NCBI

45 

Bristow RG and Hill RP: Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer. 8:180–192. 2008. View Article : Google Scholar : PubMed/NCBI

46 

Aqeilan RI, Calin GA and Croce CM: miR-15a and miR-16-1 in cancer: Discovery, function and future perspectives. Cell Death Differ. 17:215–220. 2010. View Article : Google Scholar : PubMed/NCBI

47 

Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L, D'Urso L, Pagliuca A, Biffoni M, Labbaye C, et al: The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med. 14:1271–1277. 2008. View Article : Google Scholar : PubMed/NCBI

48 

Castilla MA, Moreno-Bueno G, Romero-Pérez L, Van De Vijver K, Biscuola M, López-García MÁ, Prat J, Matías-Guiu X, Cano A, Oliva E, et al: Micro-RNA signature of the epithelial-mesenchymal transition in endometrial carcinosarcoma. J Pathol. 223:72–80. 2011. View Article : Google Scholar : PubMed/NCBI

49 

Chen J, Zhang K, Xu Y, Gao Y, Li C, Wang R and Chen L: The role of microRNA-26a in human cancer progression and clinical application. Tumour Biol. 37:7095–7108. 2016. View Article : Google Scholar : PubMed/NCBI

50 

Dai Y, Xia W, Song T, Su X, Li J, Li S, Chen Y, Wang W, Ding H, Liu X, et al: MicroRNA-200b is overexpressed in endometrial adenocarcinomas and enhances MMP2 activity by downregulating TIMP2 in human endometrial cancer cell line HEC-1A cells. Nucleic Acid Ther. 23:29–34. 2013. View Article : Google Scholar : PubMed/NCBI

51 

Doebele C, Bonauer A, Fischer A, Scholz A, Reiss Y, Urbich C, Hofmann WK, Zeiher AM and Dimmeler S: Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells. Blood. 115:4944–4950. 2010. View Article : Google Scholar : PubMed/NCBI

52 

Fuziwara CS and Kimura ET: Insights into regulation of the miR-17-92 cluster of miRNAs in cancer. Front Med (Lausanne). 2:642015.PubMed/NCBI

53 

Jiang F, Liu T, He Y, Yan Q, Chen X, Wang H and Wan X: MiR-125b promotes proliferation and migration of type II endometrial carcinoma cells through targeting TP53INP1 tumor suppressor in vitro and in vivo. BMC Cancer. 11:4252011. View Article : Google Scholar : PubMed/NCBI

54 

Kim J, Siverly AN, Chen D, Wang M, Yuan Y, Wang Y, Lee H, Zhang J, Muller WJ, Liang H, et al: Ablation of miR-10b suppresses oncogene-induced mammary tumorigenesis and metastasis and reactivates tumor-suppressive pathways. Cancer Res. 76:6424–6435. 2016. View Article : Google Scholar : PubMed/NCBI

55 

Kolenda T, Przybyła W, Teresiak A, Mackiewicz A and Lamperska KM: The mystery of let-7d - a small RNA with great power. Contemp Oncol (Pozn). 18:293–301. 2014.PubMed/NCBI

56 

Li BL, Lu W, Lu C, Qu JJ, Yang TT, Yan Q and Wan XP: CpG island hypermethylation-associated silencing of microRNAs promotes human endometrial cancer. Cancer Cell Int. 13:442013. View Article : Google Scholar : PubMed/NCBI

57 

Li S, Hu R, Wang C, Guo F, Li X and Wang S: miR-22 inhibits proliferation and invasion in estrogen receptor α-positive endometrial endometrioid carcinomas cells. Mol Med Rep. 9:2393–2399. 2014.PubMed/NCBI

58 

Liu P, Qi M, Ma C, Lao G and Liu Y and Liu Y and Liu Y: Let7a inhibits the growth of endometrial carcinoma cells by targeting Aurora-B. FEBS Lett. 587:2523–2529. 2013. View Article : Google Scholar : PubMed/NCBI

59 

Lu J, Zhang X, Zhang R and Ge Q: MicroRNA heterogeneity in endometrial cancer cell lines revealed by deep sequencing. Oncol Lett. 10:3457–3465. 2015.PubMed/NCBI

60 

Mozos A, Catasús L, D'Angelo E, Serrano E, Espinosa I, Ferrer I, Pons C and Prat J: The FOXO1-miR27 tandem regulates myometrial invasion in endometrioid endometrial adenocarcinoma. Hum Pathol. 45:942–951. 2014. View Article : Google Scholar : PubMed/NCBI

61 

Park SL, Cho TM, Won SY, Song JH, Noh DH, Kim WJ and Moon SK: MicroRNA-20b inhibits the proliferation, migration and invasion of bladder cancer EJ cells via the targeting of cell cycle regulation and Sp-1-mediated MMP-2 expression. Oncol Rep. 34:1605–1612. 2015.PubMed/NCBI

62 

Park SY, Lee JH, Ha M, Nam JW and Kim VN: miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol. 16:23–29. 2009. View Article : Google Scholar : PubMed/NCBI

63 

Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S and Rainaldi G: MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 108:3068–3071. 2006. View Article : Google Scholar : PubMed/NCBI

64 

Qin X, Yan L, Zhao X, Li C and Fu Y: microRNA-21 overexpression contributes to cell proliferation by targeting PTEN in endometrioid endometrial cancer. Oncol Lett. 4:1290–1296. 2012.PubMed/NCBI

65 

Ramón LA, Braza-Boïls A, Gilabert J, Chirivella M, España F, Estellés A and Gilabert-Estellés J: microRNAs related to angiogenesis are dysregulated in endometrioid endometrial cancer. Hum Reprod. 27:3036–3045. 2012. View Article : Google Scholar : PubMed/NCBI

66 

Romero-Pérez L, Castilla MA, López-García MA, Díaz-Martín J, Biscuola M, Ramiro-Fuentes S, Oliva E, Matias-Guiu X, Prat J, Cano A, et al: Molecular events in endometrial carcinosarcomas and the role of high mobility group AT-hook 2 in endometrial carcinogenesis. Hum Pathol. 44:244–254. 2013. View Article : Google Scholar : PubMed/NCBI

67 

Shan ZN, Tian R, Zhang M, Gui ZH, Wu J, Ding M, Zhou XF and He J: miR128-1 inhibits the growth of glioblastoma multiforme and glioma stem-like cells via targeting BMI1 and E2F3. Oncotarget. 7:78813–78826. 2016.PubMed/NCBI

68 

Shang C, Lu YM and Meng LR: MicroRNA-125b down-regulation mediates endometrial cancer invasion by targeting ERBB2. Med Sci Monit. 18:BR149–BR155. 2012. View Article : Google Scholar : PubMed/NCBI

69 

Torres A, Kozak J, Korolczuk A, Wdowiak P, Domańska-Glonek E, Maciejewski R and Torres K: In vitro and in vivo activity of miR-92a-Locked Nucleic Acid (LNA)-inhibitor against endometrial cancer. BMC Cancer. 16:8222016. View Article : Google Scholar : PubMed/NCBI

70 

Tsukamoto O, Miura K, Mishima H, Abe S, Kaneuchi M, Higashijima A, Miura S, Kinoshita A, Yoshiura K and Masuzaki H: Identification of endometrioid endometrial carcinoma-associated microRNAs in tissue and plasma. Gynecol Oncol. 132:715–721. 2014. View Article : Google Scholar : PubMed/NCBI

71 

Wang J, Li Y, Ding M, Zhang H, Xu X and Tang J: Molecular mechanisms and clinical applications of miR-22 in regulating malignant progression in human cancer (Review). Int J Oncol. 50:345–355. 2017.(Review). PubMed/NCBI

72 

Yang N, Kaur S, Volinia S, Greshock J, Lassus H, Hasegawa K, Liang S, Leminen A, Deng S, Smith L, et al: MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res. 68:10307–10314. 2008. View Article : Google Scholar : PubMed/NCBI

73 

Zhang R, He Y, Zhang X, Xing B, Sheng Y, Lu H and Wei Z: Estrogen receptor-regulated microRNAs contribute to the BCL2/BAX imbalance in endometrial adenocarcinoma and precancerous lesions. Cancer Lett. 314:155–165. 2012. View Article : Google Scholar : PubMed/NCBI

74 

Zhao C, Wang G, Zhu Y, Li X, Yan F, Zhang C, Huang X and Zhang Y: Aberrant regulation of miR-15b in human malignant tumors and its effects on the hallmarks of cancer. Tumour Biol. 37:177–183. 2016. View Article : Google Scholar : PubMed/NCBI

75 

Zhao H, Xu Z, Qin H, Gao Z and Gao L: miR-30b regulates migration and invasion of human colorectal cancer via SIX1. Biochem J. 460:117–125. 2014. View Article : Google Scholar : PubMed/NCBI

76 

Nishida M: The Ishikawa cells from birth to the present. Hum Cell. 15:104–117. 2002. View Article : Google Scholar : PubMed/NCBI

77 

Pfaffl MW, Tichopad A, Prgomet C and Neuvians TP: Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett. 26:509–515. 2004. View Article : Google Scholar : PubMed/NCBI

78 

Chou CH, Chang NW, Shrestha S, Hsu SD, Lin YL, Lee WH, Yang CD, Hong HC, Wei TY, Tu SJ, et al: miRTarBase 2016: Updates to the experimentally validated miRNA-target interactions database. Nucleic Acids Res. 44:D239–D247. 2016. View Article : Google Scholar : PubMed/NCBI

79 

Fang JS, Gillies RD and Gatenby RA: Adaptation to hypoxia and acidosis in carcinogenesis and tumor progression. Semin Cancer Biol. 18:330–337. 2008. View Article : Google Scholar : PubMed/NCBI

80 

Gatenby RA and Gillies RJ: Why do cancers have high aerobic glycolysis? Nat Rev Cancer. 4:891–899. 2004. View Article : Google Scholar : PubMed/NCBI

81 

Gatenby RA, Smallbone K, Maini PK, Rose F, Averill J, Nagle RB, Worrall L and Gillies RJ: Cellular adaptations to hypoxia and acidosis during somatic evolution of breast cancer. Br J Cancer. 97:646–653. 2007. View Article : Google Scholar : PubMed/NCBI

82 

Sameni M, Mullins S, Moin K, Sloane B and Osuala K: Importance of the tumor microenvironment. Breast Cancer Metastasis and Drug Resistance: Progress and Prospects. Ahmad A: New York: Springer; pp. 178–179. 2013

83 

Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, et al: Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet. 38:1060–1065. 2006. View Article : Google Scholar : PubMed/NCBI

84 

Suárez Y, Fernández-Hernando C, Yu J, Gerber SA, Harrison KD, Pober JS, Iruela-Arispe ML, Merkenschlager M and Sessa WC: Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci USA. 105:14082–14087. 2008. View Article : Google Scholar : PubMed/NCBI

85 

Lei Z, Li B, Yang Z, Fang H, Zhang GM, Feng ZH and Huang B: Regulation of HIF-1alpha and VEGF by miR-20b tunes tumor cells to adapt to the alteration of oxygen concentration. PLoS One. 4:e76292009. View Article : Google Scholar : PubMed/NCBI

86 

Danza K, Silvestris N, Simone G, Signorile M, Saragoni L, Brunetti O, Monti M, Mazzotta A, De Summa S, Mangia A, et al: Role of miR-27a, miR-181a and miR-20b in gastric cancer hypoxia-induced chemoresistance. Cancer Biol Ther. 17:400–406. 2016. View Article : Google Scholar : PubMed/NCBI

87 

Chen PH, Cheng CH, Shih CM, Ho KH, Lin CW, Lee CC, Liu AJ, Chang CK and Chen KC: The inhibition of microRNA-128 on IGF-1-activating mTOR signaling involves in Temozolomide-induced glioma cell apoptotic death. PLoS One. 11:e01670962016. View Article : Google Scholar : PubMed/NCBI

88 

Stefani G and Slack FJ: Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol. 9:219–230. 2008. View Article : Google Scholar : PubMed/NCBI

89 

Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, Harano T, Yatabe Y, Nagino M, Nimura Y, et al: Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 64:3753–3756. 2004. View Article : Google Scholar : PubMed/NCBI

90 

Tsuji T, Umekita Y, Ohi Y, Kamio M, Douchi T and Yoshida H: Maspin expression is up-regulated during the progression of endometrioid endometrial carcinoma. Histopathology. 51:871–874. 2007. View Article : Google Scholar : PubMed/NCBI

91 

Mirra P, Raciti GA, Nigro C, Fiory F, D'Esposito V, Formisano P, Beguinot F and Miele C: Circulating miRNAs as intercellular messengers, potential biomarkers and therapeutic targets for Type 2 diabetes. Epigenomics. 7:653–667. 2015. View Article : Google Scholar : PubMed/NCBI

92 

Turchinovich A, Samatov TR, Tonevitsky AG and Burwinkel B: Circulating miRNAs: Cell-cell communication function? Front Genet. 4:1192013. View Article : Google Scholar : PubMed/NCBI

93 

Gambari R, Brognara E, Spandidos DA and Fabbri E: Targeting oncomiRNAs and mimicking tumor suppressor miRNAs: Νew trends in the development of miRNA therapeutic strategies in oncology (Review). Int J Oncol. 49:5–32. 2016.PubMed/NCBI

94 

Bai JX, Yan B, Zhao ZN, Xiao X, Qin WW, Zhang R, Jia LT, Meng YL, Jin BQ, Fan DM, et al: Tamoxifen represses miR-200 microRNAs and promotes epithelial-to-mesenchymal transition by up-regulating c-Myc in endometrial carcinoma cell lines. Endocrinology. 154:635–645. 2013. View Article : Google Scholar : PubMed/NCBI

95 

Shen Y, Lu L, Xu J, Meng W, Qing Y, Liu Y, Zhang B and Hu H: Bortezomib induces apoptosis of endometrial cancer cells through microRNA-17-5p by targeting p21. Cell Biol Int. 37:1114–1121. 2013. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Eismann J, Hirschfeld M, Erbes T, Rücker G, Jäger M, Ritter A, Weiss D, Gitsch G and Mayer S: Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro. Oncol Rep 38: 993-1004, 2017.
APA
Eismann, J., Hirschfeld, M., Erbes, T., Rücker, G., Jäger, M., Ritter, A. ... Mayer, S. (2017). Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro. Oncology Reports, 38, 993-1004. https://doi.org/10.3892/or.2017.5717
MLA
Eismann, J., Hirschfeld, M., Erbes, T., Rücker, G., Jäger, M., Ritter, A., Weiss, D., Gitsch, G., Mayer, S."Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro". Oncology Reports 38.2 (2017): 993-1004.
Chicago
Eismann, J., Hirschfeld, M., Erbes, T., Rücker, G., Jäger, M., Ritter, A., Weiss, D., Gitsch, G., Mayer, S."Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro". Oncology Reports 38, no. 2 (2017): 993-1004. https://doi.org/10.3892/or.2017.5717
Copy and paste a formatted citation
x
Spandidos Publications style
Eismann J, Hirschfeld M, Erbes T, Rücker G, Jäger M, Ritter A, Weiss D, Gitsch G and Mayer S: Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro. Oncol Rep 38: 993-1004, 2017.
APA
Eismann, J., Hirschfeld, M., Erbes, T., Rücker, G., Jäger, M., Ritter, A. ... Mayer, S. (2017). Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro. Oncology Reports, 38, 993-1004. https://doi.org/10.3892/or.2017.5717
MLA
Eismann, J., Hirschfeld, M., Erbes, T., Rücker, G., Jäger, M., Ritter, A., Weiss, D., Gitsch, G., Mayer, S."Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro". Oncology Reports 38.2 (2017): 993-1004.
Chicago
Eismann, J., Hirschfeld, M., Erbes, T., Rücker, G., Jäger, M., Ritter, A., Weiss, D., Gitsch, G., Mayer, S."Hypoxia- and acidosis-driven aberrations of secreted microRNAs in endometrial cancer in vitro". Oncology Reports 38, no. 2 (2017): 993-1004. https://doi.org/10.3892/or.2017.5717
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team