17β-estradiol promotes extracellular vesicle release and selective miRNA loading in ERα-positive breast cancer-Reference-Cited by-同舟云学术

17β-estradiol promotes extracellular vesicle release and selective miRNA loading in ERα-positive breast cancer

Published:2023-05-30 Issue:23 Volume:120 Page:
ISSN:0027-8424
Container-title:Proceedings of the National Academy of Sciences
language:en
Short-container-title:Proc. Natl. Acad. Sci. U.S.A.

Author:

Drula Rares¹²^ORCID,Pardini Barbara³⁴^ORCID,Fu Xiao⁵⁶,De los Santos Mireia Cruz⁵⁷^ORCID,Jurj Ancuta¹²^ORCID,Pang Lan¹^ORCID,El-Daly Sherien M.⁵⁸^ORCID,Fabris Linda¹^ORCID,Knutsen Erik⁵⁹¹⁰^ORCID,Dragomir Mihnea P.⁵¹¹¹²¹³^ORCID,Bayraktar Recep¹^ORCID,Li Yongfeng⁵¹⁴,Chen Meng¹^ORCID,Del Vecchio Filippo¹⁵^ORCID,Berland Léa⁵¹⁶,Dae Jessica⁵¹⁷^ORCID,Fan Daniel¹¹⁷,Shimizu Masayoshi¹,Tran Anh M.⁵¹⁸^ORCID,Barzi Mercedes¹⁹,Pioppini Carlotta⁵²⁰^ORCID,Gutierrez Angelica M.²¹^ORCID,Ivan Cristina⁵²²,Meas Salyna²³^ORCID,Hall Carolyn S.²³^ORCID,Alahari Suresh K.²⁴^ORCID,Berindan-Neagoe Ioana²^ORCID,Fabbri Muller¹⁵²⁵^ORCID,Lucci Anthony²³^ORCID,Arun Banu²¹,Anfossi Simone¹^ORCID,Calin George A.¹²²^ORCID

Affiliation:

1. Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030

2. The Research Center for Functional Genomics, Biomedicine and Translational Medicine, Iuliu Hatieganu University of Medicine and Pharmacy, 400337 Cluj Napoca, Romania

3. Italian Institute for Genomic Medicine, c/o FPO-IRCCS Candiolo, 10060 Candiolo, Italy

4. Candiolo Cancer Institute, FPO-IRCCS, 10060 Candiolo, Italy

5. Department of Experimental Therapeutics, The University of Texas MD Anderson Cancer Center, Houston, TX 77030

6. Department of Medical Oncology, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, 710061 Shaanxi, China

7. Department of Oncology-Pathology, Karolinska Institutet, Karolinska University Hospital, 17164 Solna, Sweden

8. Medical Biochemistry Department, Medical Research and Clinical Studies Institute, National Research Centre, Cairo 12622, Egypt

9. Department of Medical Biology, Faculty of Health Sciences, UiT, The Artic University of Norway, N-9037 Tromso, Norway

10. Centre for Clinical Research and Education, University Hospital of North Norway, N-9037 Tromso, Norway

11. Institute of Pathology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, 10178 Berlin, Germany

12. German Cancer Research Center (DKFZ), Partner Site Berlin, and German Cancer Consortium (DKTK), 69120 Heidelberg, Germany

13. Berlin Institute of Health, 10178 Berlin, Germany

14. Department of Breast Surgery, Zhejiang Cancer Hospital, Hangzhou, 310022 Zhejiang, P.R. China

15. University of Hawaii Cancer Center, Cancer Biology Program, Honolulu, HI 96813

16. Department of Research Imaging, Dana Farber Cancer Institute, Boston, MA 02215

17. College of Natural Sciences, The University of Texas at Austin, Austin, TX 78712

18. Department of Chemistry, Mount Holyoke College, South Hadley, MA 01075

19. Department of Pediatrics, Duke University, Durham, NC 27708

20. Department of Nephrology and Medical Intensive Care, Charité—Universitätsmedizin Berlin, 10117 Berlin, Germany

21. Department of Breast Medical Oncology, Division of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX 77030

22. Center for RNA Interference and Non-Coding RNAs, The University of Texas MD Anderson Cancer Center, Houston, TX 77030

23. Breast Surgical Oncology, Division of Cancer Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX 77030

24. Department of Biochemistry and Molecular Biology, Stanley S Scott Cancer Center, Louisiana State University School of Medicine, New Orleans, LA 70112

25. Center for Cancer and Immunology Research, Children’s National Hospital, Washington DC 20010

Abstract

The causes and consequences of abnormal biogenesis of extracellular vesicles (EVs) are not yet well understood in malignancies, including in breast cancers (BCs). Given the hormonal signaling dependence of estrogen receptor–positive (ER+) BC, we hypothesized that 17β-estradiol (estrogen) might influence EV production and microRNA (miRNA) loading. We report that physiological doses of 17β-estradiol promote EV secretion specifically from ER+ BC cells via inhibition of miR-149-5p, hindering its regulatory activity on SP1, a transcription factor that regulates the EV biogenesis factor nSMase2. Additionally, miR-149-5p downregulation promotes hnRNPA1 expression, responsible for the loading of let-7’s miRNAs into EVs. In multiple patient cohorts, we observed increased levels of let-7a-5p and let-7d-5p in EVs derived from the blood of premenopausal ER+ BC patients, and elevated EV levels in patients with high BMI, both conditions associated with higher levels of 17β-estradiol. In brief, we identified a unique estrogen-driven mechanism by which ER+ BC cells eliminate tumor suppressor miRNAs in EVs, with effects on modulating tumor-associated macrophages in the microenvironment.

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

Link

https://pnas.org/doi/pdf/10.1073/pnas.2122053120

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