Роль стволовых опухолевых клеток в канцерогенезе рака яичников

Автор: Генинг Снежанна Олеговна, Антонеева Инна Ивановна

Журнал: Ульяновский медико-биологический журнал @medbio-ulsu

Рубрика: Клиническая медицина

Статья в выпуске: 3, 2020 года.

Бесплатный доступ

Рак яичников (РЯ) - агрессивная злокачественная опухоль (ЗО) с рецидивирующим течением и низкой 5-летней выживаемостью пациенток. Большинство случаев диагностируется на распространенных стадиях, а терапевтические опции при РЯ ограничены, поэтому развитие первичной или вторичной резистентности к стандартной химиотерапии часто является фатальным для больной. Гетерогенность ЗО приводит к тому, что в ходе селекции выживают наиболее адаптированные клетки; для дальнейшей экспансии выжившего клона и закрепления устойчивого фенотипа в очаге им необходима высокая туморогенность. Стволовые опухолевые клетки (СОК) сочетают в себе эти характеристики и стоят на вершине иерархической структуры опухоли. Их биологические свойства, такие как способность к самообновлению, мультилинейная дифференцировка, схожи со свойствами нормальных стволовых клеток человека. Пластичность фенотипа и взаимодействие с иными составляющими паренхимы, стромы опухоли, а также внеопухолевыми элементами позволяют СОК противостоять неблагоприятным условиям: воздействию химиопрепаратов, иммунологическому надзору, физическим повреждающим факторам и аноикису в кровеносном и лимфатическом русле, непривычному микроокружению таргетных органов при отдаленном метастазировании. Все больше работ посвящается поиску путей использования СОК как предиктивного и прогностического биомаркера и как мишени для терапии, однако их однозначная идентификация, подсчет и специфическая элиминация представляют сложную проблему. В настоящее время наука находится на этапе накопления данных по этой тематике. В обзоре суммированы современные достижения в понимании биологии СОК и их влияния на клиническое течение РЯ. Поиск литературы осуществлялся по базам данных PubMed, Google Scholar, eLibrary.

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Рак яичников, стволовые опухолевые клетки, химиотерапия, канцерогенез, лекарственная устойчивость

Короткий адрес: https://sciup.org/14117587

IDR: 14117587   |   DOI: 10.34014/2227-1848-2020-3-82-103

Список литературы Роль стволовых опухолевых клеток в канцерогенезе рака яичников

  • Ferlay J., Ervik M., Lam F., Colombet M., Mery L., Pineros M., Znaor A., Soerjomataram I., Bray F. Global Cancer Observatory: Cancer Today. Lyon: International Agency for Research on Cancer; 2018. URL: https://gco.iarc.fr/today, accessed (дата обращения: 20.04.2020)
  • Каприн А.Д., Старинский В.В., Петрова Г.В., ред. Состояние онкологической помощи населению России в 2018 году. Москва: МНИОИ им. П.А. Герцена - филиал ФГБУ "НМИЦ радиологии" Минздрава России; 2019. 236
  • Howlader N., Noone A.M., Krapcho M., Miller D., Brest A., Yu M., Ruhl J., Tatalovich Z., Mariotto A., Lewis D.R., Chen H.S., Feuer E.J., Cronin K.A. (eds.). SEER Cancer Statistics Review, 1975-2017, National Cancer Institute. Bethesda, MD. URL: https://seer.cancer.gov/csr/1975_2017 (дата обращения: 20.04.2020)
  • Ledermann J.A., Raja F.A., Fotopoulou C. Newly diagnosed and relapsed epithelial ovarian carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 2013; 24 (Suppl. 6): 24-32
  • Nowell P.C. The clonal evolution of tumor cell populations. Science. 1976; 194: 23-28
  • Schwarz R.F., Ng C.K., Cooke S.L., Newman S., Temple J., Piskorz A.M., Gale D., Sayal K., Murtaza M., Baldwin P.J., Rosenfeld N., Earl H.M., Sala E., Jimenez-Linan M., Parkinson C.A., Markowetz F., Brenton J.D. Spatial and temporal heterogeneity in high-grade serous ovarian cancer: a phylogenetic analysis. PLoS Med. 2015; 12 (2): e1001789. 10.1371/journal.pmed.1001789. PMID: 25710373. PMCID: PMC4339382
  • DOI: 10.1371/journal.pmed.1001789.PMID
  • Apostoli A.J., Ailles L. Clonal evolution and tumor-initiating cells: New dimensions in cancer patient treatment. Crit. Rev. Clin. Lab. Sci. 2016; 53 (1): 40-51.
  • DOI: 10.3109/10408363.2015.1083944
  • Ge Y., Fuchs E. Stretching the limits: from homeostasis to stem cell plasticity in wound healing and cancer. Nat. Rev. Genet. 2018; 19 (5): 311-325.
  • DOI: 10.1038/nrg.2018.9
  • Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997; 3: 730-737.
  • Hamburger A.W., Salmon S.E. Primary bioassay of human tumor stem cells. Science. 1977; 197: 461-463.
  • Bapat S.A., Mali A.M., Koppikar C.B., Kurrey N.K. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res. 2005; 65 (8): 3025-3029.
  • DOI: 10.1158/0008-5472.CAN-04-3931
  • Szotek P.P., Pieretti-Vanmarcke R., Masiakos P.T., Dinulescu D.M., Connolly D., Foster R., Dombkowski D., Preffer F., Maclaughlin D.T., Donahoe P.K. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc. Natl. Acad. Sci USA. 2006; 103 (30): 11154-11159. 10.1073/pnas.0603672103. PMID: 16849428. PMCID: PMC1544057.
  • DOI: 10.1073/pnas.0603672103.PMID
  • Zhang S., Balch C., Chan M.W., Lai H.C., Matei D., Schilder J.M., Yan P.S., Huang T.H., Nephew K.P. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 2008; 68 (11): 4311-4320. 10.1158/0008-5472.CAN-08-0364. PMID: 18519691. PMCID: PMC2553722.
  • DOI: 10.1158/0008-5472.CAN-08-0364.PMID
  • Alvero A.B., Chen R., Fu H.H., Montagna M., Schwartz P.E., Rutherford T., Silasi D.A., Steffensen K.D., Waldstrom M., Visintin I., Mor G. Molecular phenotyping of human ovarian cancer stem cells unravels the mechanisms for repair and chemoresistance. Cell Cycle. 2009; 8 (1): 158-166. 10.4161/cc.8.1.7533. PMID: 19158483. PMCID: PMC3041590.
  • DOI: 10.4161/cc.8.1.7533.PMID
  • Flesken-Nikitin A., Hwang C.I., Cheng C. Y., Michurina T.V., Enikolopov G., Nikitin A. Y. Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche. Nature. 2013; 495 (7440): 241-245.
  • DOI: 10.1038/nature11979
  • Krivtsov A.V., Twomey D., Feng Z., Stubbs M.C., Wang Y., Faber J., Levine J.E., Wang J., Hahn W.C., Gilliland D.G., Golub T.R., Armstrong S.A. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 2006; 442: 818-822.
  • DOI: 10.1038/nature04980
  • Niederhuber J.E., Armitage J.O., Kastan M.B., Doroshow J.H., Tepper J.E. (eds). Abeloff's Clinical Oncology. 6th Edition. Elsevier; 2020. 2072.
  • DOI: 10.1016/C2015-0-05400-4
  • Janiszewska M. The microcosmos of intratumor heterogeneity: the space-time of cancer evolution. Oncogene. 2020; 39: 2031-2039.
  • DOI: 10.1038/s41388-019-1127-5
  • Lu X., Kang Y. Cell fusion hypothesis of the cancer stem cell. Adv. Exp. Med. Biol. 2011; 714: 129-140.
  • DOI: 10.1007/978-94-007-0782-5_6
  • Ischenko I., Zhi J., Moll U.M., Nemajerova A., Petrenko O. Direct reprogramming by oncogenic Ras and Myc. Proc. Natl. Acad. Sci USA. 2013; 110 (10): 3937-3942.
  • DOI: 10.1073/pnas.1219592110
  • Nguyen V.H.L., Hough R., Bernaudo S., Peng C. Wnt/ß-catenin signalling in ovarian cancer: Insights into its hyperactivation and function in tumorigenesis. J. Ovarian Res. 2019; 12 (1): 122. 10.1186/s13048-019-0596-z. PMID: 31829231. PMCID: PMC6905042.
  • DOI: 10.1186/s13048-019-0596-z.PMID
  • Nagendra P.B., Goad J., Nielsen S., Rassam L., Lombard J.M., Nahar P., Tanwar P.S. Ovarian hormones through Wnt signalling regulate the growth of human and mouse ovarian cancer initiating lesions. Oncotarget. 2016; 7 (40): 64836-64853. 10.18632/Oncotarget.11711. PMID: 27588493. PMCID: PMC5323120.
  • DOI: 10.18632/oncotarget.11711.PMID
  • Kotrbová A., Ovesná P., Gybel' T., Radaszkiewicz T., Bednaříková M., Hausnerová J., Jandáková E., Minář L., Crha I., Weinberger V., Záveský L., Bryja V., Pospíchalová V. WNT signaling inducing activity in ascites predicts poor outcome in ovarian cancer. Theranostics. 2020; 10 (2): 537-552. 10.7150/thno.37423. PMID: 31903136. PMCID: PMC6929979.
  • DOI: 10.7150/thno.37423.PMID
  • Nagaraj A.B., Joseph P., Kovalenko O., Singh S., Armstrong A., Redline R., Resnick K., Zanotti K., Waggoner S., DiFeo A. Critical role of Wnt/ß-catenin signaling in driving epithelial ovarian cancer platinum resistance. Oncotarget. 2015; 6 (27): 23720-23734. 10.18632/Oncotarget.4690. PMID: 26125441. PMCID: PMC4695147.
  • DOI: 10.18632/oncotarget.4690.PMID
  • Bar J., Grelewski P., Deszcz I., Noga L., Hirnle L., Lis-Nawara A. Association between p53 protein phosphorylated at serine 20 expression and ovarian carcinoma stem cells phenotype: correlation with clinico-pathological parameters of ovarian cancer. Neoplasma. 2019; 2019: 181012N764.
  • Deng J., Bai X., Feng X., Ni J., Beretov J., Graham P., Li Y. Inhibition of PI3K/Akt/mTOR signaling pathway alleviates ovarian cancer chemoresistance through reversing epithelial-mesenchymal transition and decreasing cancer stem cell marker expression. BMC Cancer. 2019; 19 (1): 618.
  • DOI: 10.1186/s12885-019-5824-9
  • Motohara T., Masuko S., Ishimoto T., Yae T., Onishi N., Muraguchi T., Hirao A., Matsuzaki Y., Tashi-ro H., Katabuchi H., Saya H., Nagano O. Transient depletion of p53 followed by transduction of c-Myc and K-Ras converts ovarian stem-like cells into tumor-initiating cells. Carcinogenesis. 2011; 32 (11): 1597-1606. 10.1093/carcin/bgr183. PMID: 21828057.
  • DOI: 10.1093/carcin/bgr183.PMID
  • Wang D., Xiang T., Zhao Z., Lin K., Yin P., Jiang L., Liang Z., Zhu B. Autocrine interleukin-23 promotes self-renewal of CD133+ ovarian cancer stem-like cells. Oncotarget. 2016; 7 (46): 76006-76020. 10.18632/Oncotarget. 12579. PMID: 27738346. PMCID: PMC5342794.
  • DOI: 10.18632/oncotarget.12579.PMID
  • Thankamony A.P., Saxena K., Murali R., Jolly M.K., Nair R. Cancer Stem Cell Plasticity - A Deadly Deal. Front Mol Biosci. 2020; 7: 79. 10.3389/fmolb.2020.00079. PMID: 32426371. PMCID: PMC7203492.
  • DOI: 10.3389/fmolb.2020.00079.PMID
  • Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003; 100 (7): 3983-3988.
  • Yang L., Shi P., Zhao G., Xu J., Peng W., Zhang J., Zhang G., Wang X., Dong Z., Chen F., Cui H. Targeting cancer stem cell pathways for cancer therapy. Signal Transduct. Target Ther. 2020; 5: 8.
  • DOI: 10.1038/s41392-020-0110-5
  • Ferrandina G., Bonanno G., Pierelli L., Perillo A., Procoli A., Mariotti A., Corallo M., Martinelli E., Rutella S., Paglia A., Zannoni G., Mancuso S., Scambia G. Expression of CD133-1 and CD133-2 in ovarian cancer. Int. J. Gynecol. Cancer. 2008; 18 (3): 506-514. 10.1111/j.1525-1438.2007.01056.x. PMID: 17868344.
  • DOI: 10.1111/j.1525-1438.2007.01056.x.PMID
  • Zhang J., Guo X., Chang D.Y., Rosen D.G., Mercado-Uribe I., Liu J. CD133 expression associated with poor prognosis in ovarian cancer. Mod. Pathol. 2012; 25 (3): 456-464.
  • DOI: 10.1038/mod-pathol.2011.170
  • Bourguignon L.Y., Peyrollier K., Xia W., Gilad E. Hyaluronan-CD44 interaction activates stem cell marker Nanog, Stat-3-mediated MDR1 gene expression, and ankyrin-regulated multidrug efflux in breast and ovarian tumor cells. J. Biol. Chem. 2008; 283: 17635-17651.
  • Zhu Y., Zhang H., Zhang G., Shi Y., Huang J. Co-expression of CD44/MyD88 is a poor prognostic factor in advanced epithelial ovarian cancer. Ann. Transl. Med. 2019; 7 (5): 91. 10.21037/atm.2019.01.28. PMID: 31019941. PMCID: PMC6462660.
  • DOI: 10.21037/atm.2019.01.28.PMID
  • Chau W.K., Ip C.K., Mak A.S., Lai H.C., Wong A.S. c-Kit mediates chemoresistance and tumor-initiating capacity of ovarian cancer cells through activation of Wnt/beta-catenin-ATP-binding cassette G2 signaling. Oncogene. 2013; 32: 2767-2781.
  • DOI: 10.1038/onc.2012.290
  • Yang B., Yan X., Liu L., Jiang C., Hou S. Overexpression of the cancer stem cell marker CD117 predicts poor prognosis in epithelial ovarian cancer patients: evidence from meta-analysis. Onco Targets Ther. 2017; 10: 2951-2961. 10.2147/OTT.S136549. PMID: 28652777. PMCID: PMC5476715.
  • DOI: 10.2147/OTT.S136549.PMID
  • Gao M.Q., Choi Y.P., Kang S., Youn J.H., Cho N.H. CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene. 2010; 29 (18): 2672-2680. 10.1038/onc.2010.35. PMID: 20190812.
  • DOI: 10.1038/onc.2010.35.PMID
  • Burgos-Ojeda D., Wu R., McLean K., Chen Y.C., Talpaz M., Yoon E., Cho K.R., Buckanovich R.J. CD24+ Ovarian Cancer Cells Are Enriched for Cancer-Initiating Cells and Dependent on JAK2 Signaling for Growth and Metastasis. Mol. Cancer. Ther. 2015; 14 (7): 1717-1727. 10.1158/1535-7163.MCT-14-0607. PMID: 25969154. PMCID: PMC4496272.
  • DOI: 10.1158/1535-7163.MCT-14-0607.PMID
  • Meng E., Long B., Sullivan P., McClellan S., Finan M.A., Reed E., Shevde L., Rocconi R.P. CD44+/CD24-ovarian cancer cells demonstrate cancer stem cell properties and correlate to survival. Clin. Exp. Metastasis. 2012; 29 (8): 939-948. 10.1007/s10585-012-9482-4. PMID: 22610780.
  • DOI: 10.1007/s10585-012-9482-4.PMID
  • Rebollido-Rios R., Venton G., Sanchez-Redondo S., Iglesias I., Felip C., Fournet G., Gonzalez E., Romero Fernandez W., Borroto Escuela D. O., Di Stefano B., Penarroche-Diaz R., Martin G., Ceylan I., Costello R., Perez-Alea M. Dual disruption of aldehyde dehydrogenases 1 and 3 promotes functional changes in the glutathione redox system and enhances chemosensitivity in nonsmall cell lung cancer. Oncogene. 2020; 39 (13): 2756-2771. 10.1038/s41388-020-1184-9. PMID: 32015486. PMCID: PMC7098886.
  • DOI: 10.1038/s41388-020-1184-9.PMID
  • Kuroda T., Hirohashi Y., Torigoe T., Yasuda K., Takahashi A., Asanuma H., Morita R., Mariya T., Asano T., Mizuuchi M., Saito T., Sato N. ALDH1-high ovarian cancer stem-like cells can be isolated from serous and clear cell adenocarcinoma cells, and ALDH1 high expression is associated with poor prognosis. PLoS One. 2013; 8 (6): e65158. 10.1371/journal.pone.0065158. PMID: 23762304. PMCID: PMC3675199.
  • DOI: 10.1371/journal.pone.0065158.PMID
  • Ruscito I., Darb-Esfahani S., Kulbe H., Bellati F., Zizzari I.G., Rahimi Koshkaki H., Napoletano C., Caserta D., Rughetti A., Kessler M., Sehouli J., Nuti M., Braicu E.I. The prognostic impact of cancer stemlike cell biomarker aldehyde dehydrogenase-1 (ALDH1) in ovarian cancer: A meta-analysis. Gynecol. Oncol. 2018; 150 (1): 151-157. 10.1016/j.ygyno.2018.05.006. PMID: 29753392.
  • DOI: 10.1016/j.ygyno.2018.05.006.PMID
  • Lupia M., Angiolini F., Bertalot G., Freddi S., Sachsenmeier K.F., Chisci E., Kutryb-Zajac B., Confalonieri S., Smolenski R.T., Giovannoni R., Colombo N., Bianchi F., Cavallaro U. CD73 Regulates Sternness and Epithelial-Mesenchymal Transition in Ovarian Cancer-Initiating Cells. Stem. Cell Reports. 2018; 10 (4): 1412-1425. 10.1016/j.stemcr.2018.02.009. PMID: 29551673. PMCID: PMC5998305.
  • DOI: 10.1016/j.stemcr.2018.02.009.PMID
  • Li H., Lv M., Qiao B., Li X. Blockade pf CD73/adenosine axis improves the therapeutic efficacy of docetaxel in epithelial ovarian cancer. Arch. Gynecol. Obstet. 2019; 299 (6): 1737-1746. 10.1007/s00404-019-05139-3. PMID: 30941556.
  • DOI: 10.1007/s00404-019-05139-3.PMID
  • Connor E.V., Saygin C., Braley C., Wiechert A.C., Karunanithi S., Crean-Tate K., Abdul-Karim F.W., Michener C.M., Rose P.G., Lathia J.D., Reizes O. Thy-1 predicts poor prognosis and is associated with self-renewal in ovarian cancer. J. Ovarian Res. 2019; 12 (1): 112. 10.1186/s13048-019-0590-5. PMID: 31735168. PMCID: PMC6858973.
  • DOI: 10.1186/s13048-019-0590-5.PMID
  • Winterhoff B.J., Maile M., Mitra A.K., Sebe A., Bazzaro M., Geller M.A., Abrahante J.E., Klein M., Hellweg R., Mullany S.A., Beckman K., Daniel J., Starr T.K. Single cell sequencing reveals heterogeneity within ovarian cancer epithelium and cancer associated stromal cells. Gynecol. Oncol. 2017; 144 (3): 598-606. 10.1016/j.ygyno.2017.01.015. PMID: 28111004. PMCID: PMC5316302.
  • DOI: 10.1016/j.ygyno.2017.01.015.PMID
  • Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.J., Wicha M.S. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes. Dev. 2003; 17 (10): 1253-1270.
  • DOI: 10.1101/gad.1061803
  • Golebiewska A., Brons N.H.C., Bjerkvig R., Niclou S.P. Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem. Cell. 2011; 8 (2): 136-147.
  • DOI: 10.1016/j.stem.2011.01.007
  • Kretzschmar K., Watt F.M. Lineage Tracing. Cell. 2012; 148 (1-2): 33-45.
  • DOI: 10.1016/j.cell.2012.01.002
  • Pastrana E., Silva-Vargas V., Doetsch F. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem. Cell. 2011; 8 (5): 486-498.
  • DOI: 10.1016/j.stem.2011.04.007
  • Stewart J.M., Shaw P.A., Gedye C., Bernardini M.Q., Neel B.G., Ailles L.E. Phenotypic heterogeneity and instability of human ovarian tumor-initiating cells. Proc. Natl. Acad. Sci USA. 2011; 108 (16): 6468-6473.
  • DOI: 10.1073/pnas.1005529108
  • Кайгородова Е.В., Федулова Н.В., Очиров М.О., Дьяков Д.А., Молчанов С.В., Часовских Н.Ю. Различные популяции опухолевых клеток в асцитической жидкости больных раком яичников. Бюллетень сибирской медицины. 2020; 19 (1): 50-58.
  • DOI: 10.20538/1682-0363-2020-1-50-58
  • Roy L., Bobbs A., Sattler R., Kurkewich J.L., Dausinas P.B., Nallathamby P., Cowden Dahl K.D. CD133 Promotes Adhesion to the Ovarian Cancer Metastatic Niche. Cancer Growth Metastasis. 2018; 11. 10.1177/1179064418767882. PMID: 29662326. PMCID: PMC5894897.
  • DOI: 10.1177/1179064418767882.PMID
  • Nakamura K., Sawada K., Kinose Y., Yoshimura A., Toda A., Nakatsuka E., Hashimoto K., Mabuchi S., Morishige K.I., Kurachi H., Lengyel E., Kimura T. Exosomes Promote Ovarian Cancer Cell Invasion through Transfer of CD44 to Peritoneal Mesothelial Cells. Mol. Cancer Res. 2017; 15 (1): 78-92. 10.1158/1541-7786.MCR-16-0191. PMID: 27758876.
  • DOI: 10.1158/1541-7786.MCR-16-0191.PMID
  • Nieman K.M., Kenny H.A., Penicka C.V., Ladanyi A., Buell-Gutbrod R., Zillhardt M.R., Romero I.L., Carey M.S., Mills G.B., Hotamisligil G.S., Yamada S.D., Peter M.E., Gwin K., Lengyel E. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat. Med. 2011; 17 (11): 1498-1503. 10.1038/nm.2492. PMID: 22037646. PMCID: PMC4157349.
  • DOI: 10.1038/nm.2492.PMID
  • Worzfeld T., Pogge von Strandmann E., Huber M., Adhikary T., Wagner U., Reinartz S., Müller R. The Unique Molecular and Cellular Microenvironment of Ovarian Cancer. Front. Oncol. 2017; 7: 24. 10.3389/fonc.2017.00024. PMID: 28275576. PMCID: PMC5319992.
  • DOI: 10.3389/fonc.2017.00024.PMID
  • Long H., Xie R., Xiang T., Zhao Z., Lin S., Liang Z., Chen Z., Zhu B. Autocrine CCL5 signaling promotes invasion and migration of CD133+ ovarian cancer stem-like cells via NF-KB-mediated MMP-9 upregulation. Stem. Cells. 2012; 30 (10): 2309-2319. 10.1002/stem.1194. PMID: 22887854.
  • DOI: 10.1002/stem.1194.PMID
  • Chen J., Wang J., Chen D., Yang J., Yang C., Zhang Y., Zhang H., Dou J. Evaluation of characteristics of CD44+CD117+ ovarian cancer stem cells in three dimensional basement membrane extract scaffold versus two dimensional monocultures. BMC Cell Biol. 2013; 14: 7. 10.1186/1471-2121-14-7. PMID: 23368632. PMCID: PMC3565868.
  • DOI: 10.1186/1471-2121-14-7.PMID
  • Yin M., Li X., Tan S., Zhou H.J., Ji W., Bellone S., Xu X., Zhang H., Santin A.D., Lou G., Min W. Tumor-associated macrophages drive spheroid formation during early transcoelomic metastasis of ovarian cancer. J. Clin. Invest. 2016; 126 (11): 4157-4173. 10.1172/JCI87252. PMID: 27721235. PMCID: PMC5096908.
  • DOI: 10.1172/JCI87252.PMID
  • Raghavan S., Mehta P., Xie Y., Lei Y.L., Mehta G. Ovarian cancer stem cells and macrophages reciprocally interact through the WNT pathway to promote pro-tumoral and malignant phenotypes in 3D engineered microenvironments. J. Immunother. Cancer. 2019; 7 (1): 190. 10.1186/s40425-019-0666-1. PMID: 31324218. PMCID: PMC6642605.
  • DOI: 10.1186/s40425-019-0666-1.PMID
  • Luo L., Zeng J., Liang B., Zhao Z., Sun L., Cao D., Yang J., Shen K. Ovarian cancer cells with the CD117 phenotype are highly tumorigenic and are related to chemotherapy outcome. Exp. Mol. Pathol. 2011; 91 (2): 596-602. 10.1016/j.yexmp.2011.06.005. PMID: 21787767.
  • DOI: 10.1016/j.yexmp.2011.06.005.PMID
  • Alvero A.B., Fu H.H., Holmberg J., Visintin I., Mor L., Marquina C.C., Oidtman J., Silasi D.A., Mor G. Stem-like ovarian cancer cells can serve as tumor vascular progenitors. Stem Cells. 2009; 27 (10): 24052413. 10.1002/stem.191. PMID: 19658191. PMCID: PMC2783765.
  • DOI: 10.1002/stem.191.PMID
  • Krishnapriya S., Sidhanth C., Manasa P., Sneha S., Bindhya S., Nagare R.P., Ramachandran B., Vishwanathan P., Murhekar K., Shirley S., Ganesan T.S. Cancer stem cells contribute to angiogenesis and lymphangiogenesis in serous adenocarcinoma of the ovary. angiogenesis. 2019; 22 (3): 441-455. 10.1007/s10456-019-09669-x. PMID: 31161471.
  • DOI: 10.1007/s10456-019-09669-x.PMID
  • Vera N., Acuna-Gallardo S., Grünenwald F., Caceres-Verschae A., Realini O., Acuna R., Lladser A., Illanes S.E., Varas-Godoy M. Small Extracellular Vesicles Released from Ovarian Cancer Spheroids in Response to Cisplatin Promote the Pro-Tumorigenic Activity of Mesenchymal Stem Cells. Int. J. Mol. Sci. 2019; 20 (20): 4972. 10.3390/ijms20204972. PMID: 31600881. PMCID: PMC6834150.
  • DOI: 10.3390/ijms20204972.PMID
  • Wang Y., Zong X., Mitra S., Mitra A.K., Matei D., Nephew K.P. IL-6 mediates platinum-induced enrichment of ovarian cancer stem cells. JCI Insight. 2018; 3 (23): e122360. 10.1172/jci.insight.122360. PMID: 30518684. PMCID: PMC6328027.
  • DOI: 10.1172/jci.insight.122360.PMID
  • Abubaker K., Luwor R.B., Zhu H., McNally O., Quinn M.A., Burns C.J., Thompson E. W., Findlay J.K., Ahmed N. Inhibition of the JAK2/STAT3 pathway in ovarian cancer results in the loss of cancer stem cell-like characteristics and a reduced tumor burden. BMC Cancer. 2014; 14: 317. 10.1186/14712407-14-317. PMID: 24886434. PMCID: PMC4025194.
  • DOI: 10.1186/14712407-14-317.PMID
  • Latifi A., Abubaker K., Castrechini N., Ward A.C., Liongue C., Dobill F., Kumar J., Thompson E. W., Quinn M.A., Findlay J.K., Ahmed N. Cisplatin treatment of primary and metastatic epithelial ovarian carcinomas generates residual cells with mesenchymal stem cell-like profile. J. Cell Biochem. 2011; 112 (10): 2850-2864. 10.1002/jcb.23199. PMID: 21618587.
  • DOI: 10.1002/jcb.23199.PMID
  • Steg A.D., Bevis K.S., Katre A.A., Ziebarth A., Dobbin Z.C., Alvarez R.D., Zhang K., Conner M., Landen C.N. Stem cell pathways contribute to clinical chemoresistance in ovarian cancer. Clin. Cancer Res. 2012; 18 (3): 869-881.
  • DOI: 10.1158/1078-0432.CCR-11-2188
  • Crea F., Nur Saidy N.R., Collins C.C., Wang Y. The epigenetic/noncoding origin of tumor dormancy. Trends Mol. Med. 2015; 21 (4): 206-211.
  • DOI: 10.1016/j.molmed.2015.02.005
  • Ravindran Menon D., Hammerlindl H., Torrano J., Schaider H., Fujita M. Epigenetics and metabolism at the crossroads of stress-induced plasticity, sternness and therapeutic resistance in cancer. Theranostics. 2020; 10 (14): 6261-6277. 10.7150/thno.42523. PMID: 32483452. PMCID: PMC7255038.
  • DOI: 10.7150/thno.42523.PMID
  • De Angelis M.L., Francescangeli F., La Torre F., Zeuner A. Stem Cell Plasticity and Dormancy in the Development of Cancer Therapy Resistance. Front. Oncol. 2019; 9: 626.
  • DOI: 10.3389/fonc.2019.00626
  • Milanovic M., Fan D.N.Y., Belenki D., Däbritz J.H.M., Zhao Z., Yu Y., Dörr J.R., Dimitrova L., Lenze D., Monteiro Barbosa I.A., Mendoza-Parra M.A., Kanashova T., Metzner M., Pardon K., Reimann M., Trumpp A., Dörken B., Zuber J., Gronemeyer H., Hummel M., Dittmar G., Lee S., Schmitt C.A. Senescence-associated reprogramming promotes cancer sternness. Nature. 2018; 553 (7686): 96-100.
  • DOI: 10.1038/nature25167
  • Sotgia F., Fiorillo M., Lisanti M.P. Hallmarks of the cancer cell of origin: Comparisons with "energetic" cancer stem cells (e-CSCs). Aging (Albany NY). 2019; 11 (3): 1065-1068.
  • DOI: 10.18632/aging.101822
  • Pagotto A., Pilotto G., Mazzoldi E.L., Nicoletto M.O., Frezzini S., Pastd A., Amadori A. Autophagy inhibition reduces chemoresistance and tumorigenic potential of human ovarian cancer stem cells. Cell Death Dis. 2017; 8 (7): e2943.
  • DOI: 10.1038/cddis.2017.327
  • Sharif T., Martell E., Dai C., Kennedy B.E., Murphy P., Clements D.R., Kim Y., Lee P.W., Gujar S.A. Autophagic homeostasis is required for the pluripotency of cancer stem cells. Autophagy. 2017; 13 (2): 264-284. 10.1080/15548627.2016.1260808. PMID: 27929731. PMCID: PMC5324853.
  • DOI: 10.1080/15548627.2016.1260808.PMID
  • Gammon L., Biddle A., Heywood H.K., Johannessen A.C., Mackenzie I.C. Sub-sets of cancer stem cells differ intrinsically in their patterns of oxygen metabolism. PLoS One. 2013; 8 (4): e62493. 10.1371/journal.pone.0062493. PMID: 23638097. PMCID: PMC3640080.
  • DOI: 10.1371/journal.pone.0062493.PMID
  • Chang C.W., Chen Y.S., Chou S.H., Han C.L., Chen Y.J., Yang C.C., Huang C.Y., Lo J.F. Distinct subpopulations of head and neck cancer cells with different levels of intracellular reactive oxygen species exhibit diverse sternness, proliferation, and chemosensitivity. Cancer Res. 2014; 74 (21): 6291-305.
  • DOI: 10.1158/0008-5472.CAN-14-0626
  • Dar S., Chhina J., Mert I., Chitale D., Buekers T., Kaur H., Giri S., Munkarah A., Rattan R. Bioenergetic Adaptations in Chemoresistant Ovarian Cancer Cells. Sci. Rep. 2017; 7 (1): 8760. 10.1038/s41598- 017-09206-0. PMID: 28821788. PMCID: PMC5562731.
  • DOI: 10.1038/s41598-017-09206-0.PMID
  • El Hout M., Cosialls E., Mehrpour M., Hamai A. Crosstalk between autophagy and metabolic regulation of cancer stem cells. Mol. Cancer. 2020; 19 (1): 27.
  • DOI: 10.1186/s12943-019-1126-8
  • Huang C., Sheng S., Li R., Sun X., Liu J., Huang G. Lactate promotes resistance to glucose starvation via upregulation of Bcl-2 mediated by mTOR activation. Oncol. Rep. 2015; 33 (2): 875-884.
  • DOI: 10.3892/or.2014.3655
  • Sato M., Kawana K., Adachi K., Fujimoto A., Yoshida M., Nakamura H., Nishida H., Inoue T., Taguchi A., Ogishima J., Eguchi S., Yamashita A., Tomio K., Komatsu A., Wada-Hiraike O., Oda K., Nagamatsu T., Osuga Y., Fujii T. Detachment from the primary site and suspension in ascites as the initial step in metabolic reprogramming and metastasis to the omentum in ovarian cancer. Oncol. Lett. 2018; 15 (1): 1357-1361. 10.3892/ol.2017.7388. PMID: 29399186. PMCID: PMC5772787.
  • DOI: 10.3892/ol.2017.7388.PMID
  • Li J., Condello S., Thomes-Pepin J., Ma X., Xia Y., Hurley T.D., Matei D., Cheng J.X. Lipid Desaturation Is a Metabolic Marker and Therapeutic Target of Ovarian Cancer Stem Cells. Cell Stem. Cell. 2017;(3): 303-314. 10.1016/j.stem.2016.11.004. PMID: 28041894. PMCID: PMC5337165.
  • DOI: 10.1016/j.stem.2016.11.004.PMID
  • Singh S., Brocker C., Koppaka V., Chen Y., Jackson B.C., Matsumoto A., Thompson D.C., Vasiliou V. Aldehyde dehydrogenases in cellular responses to oxidative/electrophilic stress. Free Radic. Biol. Med. 2013; 56: 89-101. 10.1016/j.freeradbiomed.2012.11.010. PMID: 23195683. PMCID: PMC3631350.
  • DOI: 10.1016/j.freeradbiomed.2012.11.010.PMID
  • Hu L., McArthur C., Jaffe R.B. Ovarian cancer stem-like side-population cells are tumourigenic and chemoresistant. Br. J. Cancer. 2010; 102 (8): 1276-1283.
  • DOI: 10.1038/sj.bjc.6605626
  • Chau W.K., Ip C.K., Mak A.S., Lai H.C., Wong A.S. c-Kit mediates chemoresistance and tumor-initiating capacity of ovarian cancer cells through activation of Wnt/ß-catenin-ATP-binding cassette G2 signaling. Oncogene. 2013; 32 (22): 2767-2781. 10.1038/onc.2012.290. PMID: 22797058.
  • DOI: 10.1038/onc.2012.290.PMID
  • Begicevic R.R., Falasca M. ABC Transporters in Cancer Stem Cells: Beyond Chemoresistance. Int. J. Mol. Sci. 2017; 18 (11): 2362.
  • DOI: 10.3390/ijms18112362
  • Zhang M., Behbod F., Atkinson R.L., Landis M.D., Kittrell.F, Edwards D., Medina D., Tsimelzon A., Hilsenbeck S., Green J.E., Michalowska A.M., Rosen J.M. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res. 2008; 68 (12): 4674-4682.
  • DOI: 10.1158/0008-5472.CAN-07-6353
  • Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006; 444 (7120): 756-760.
  • DOI: 10.1038/nature05236
  • Srivastava A.K., Han C., Zhao R., Cui T., Dai Y., Mao C., Zhao W., Zhang X., Yu J., Wang Q.E. Enhanced expression of DNA polymerase eta contributes to cisplatin resistance of ovarian cancer stem cells. Proc. Natl. Acad. Sci. USA. 2015; 112 (14): 4411-4416. 10.1073/pnas.1421365112. PMID: 25831546. PMCID: PMC4394248.
  • DOI: 10.1073/pnas.1421365112.PMID
  • Maccalli C., Rasul K.I., Elawad M., Ferrone S. The role of cancer stem cells in the modulation of anti-tumor immune responses. Semin Cancer Biol. 2018; 53: 189-200.
  • DOI: 10.1016/j.semcancer.2018.09.006
  • You Y., Li Y., Li M., Lei M., Wu M., Qu Y., Yuan Y., Chen T., Jiang H. Ovarian cancer stem cells promote tumour immune privilege and invasion via CCL5 and regulatory T cells. Clin. Exp. Immunol. 2018; 191 (1): 60-73. 10.1111/cei.13044. PMID: 28868628. PMCID: PMC5721255.
  • DOI: 10.1111/cei.13044.PMID
  • Lee H., Kim J.W., Kim D.K., Choi D.K., Lee S., Yu J.H., Kwon O.B., Lee J., Lee D.S., Kim J.H., Min S.H. Calcium Channels as Novel Therapeutic Targets for Ovarian Cancer Stem Cells. Int. J. Mol Sci. 2020;(7).
  • DOI: 10.3390/ijms21072327
  • Martinez-Serrano M.J., Caballero-Banos M., Vilella R., Vidal L., Pahisa J., Martmez-Roman S. Is sphere assay useful for the identification of cancer initiating cells of the ovary? Int. J. Gynecol. Cancer. 2015; 25 (1): 12-17.
  • DOI: 10.1097/IGC.0000000000000320
  • Zeng J., Ruan J., Luo L., Shi J., Cui Q., Yang J., Shen K. Molecular portraits of heterogeneity related to cancer stem cells in human ovarian cancer. Int. J. Gynecol. Cancer. 2014; 24 (1): 29-35. 10.1097/IGC.0000000000000024. PMID: 24300467.
  • DOI: 10.1097/IGC.0000000000000024.PMID
  • Kenda Suster N., Frkovic Grazio S., Virant-Klun I., Verdenik I., Smrkolj S. Cancer Stem Cell-Related Marker NANOG Expression in Ovarian Serous Tumors: A Clinicopathological Study of 159 Cases. Int. J. Gynecol. Cancer. 2017; 27 (9): 2006-2013. 10.1097/IGC.0000000000001105. PMID: 28906309.
  • DOI: 10.1097/IGC.0000000000001105.PMID
  • Chen W., Dong J., Haiech J., Kilhoffer M.C., Zeniou M. Cancer Stem Cell Quiescence and Plasticity as Major Challenges in Cancer Therapy. Stem. Cells Int. 2016; 2016: 1740936.
  • DOI: 10.1155/2016/1740936
  • Ong M.S., Cai W., Yuan Y., Leong H.C., Tan T.Z., Mohammad A., You M.L., Arfuso F., Goh B.C., Warrier S., Sethi G., Tolwinski N.S., Lobie P.E., Yap C.T., Hooi S.C., Huang R.Y., Kumar A.P. 'Lnc'-ing Wnt in female reproductive cancers: therapeutic potential of long non-coding RNAs in Wnt signalling. Br. J. Pharmacol. 2017; 174 (24): 4684-4700. 10.1111/bph. 13958. PMID: 28736855. PMCID: PMC5727316.
  • DOI: 10.1111/bph.13958.PMID
  • Strauss R., Li Z.Y., Liu Y., Beyer I., Persson J., Sova P., Möller T., Pesonen S., Hemminki A., Hamerlik P., Drescher C., Urban N., Bartek J., Lieber A. Analysis of epithelial and mesenchymal markers in ovarian cancer reveals phenotypic heterogeneity and plasticity. PLoS One. 2011; 6 (1): e16186.
  • DOI: 10.1371/journal.pone.0016186
  • Shiwarski D.J., Shao C., Bill A., Kim J., Xiao D., Bertrand C.A., Seethala R.S., Sano D., Myers J.N., Ha P., Grandis J., Gaither L.A., Puthenveedu M.A., Duvvuri U. To "grow" or "go": TMEM16A expression as a switch between tumor growth and metastasis in SCCHN. Clin. Cancer Res. 2014; 20 (17): 4673-4688. 10.1158/1078-0432.CCR-14-0363. PMID: 24919570. PMCID: PMC4160843.
  • DOI: 10.1158/1078-0432.CCR-14-0363.PMID
  • Parte S.C., Batra S.K., Kakar S.S. Characterization of stem cell and cancer stem cell populations in ovary and ovarian tumors. J. Ovarian Res. 2018; 11 (1): 69.
  • DOI: 10.1186/s13048-018-0439-3
  • Jolly M.K., Boareto M., Huang B., Jia D., Lu M., Ben-Jacob E., Onuchic J.N., Levine H. Implications of the Hybrid Epithelial/Mesenchymal Phenotype in Metastasis. Front. Oncol. 2015; 5: 155. 10.3389/fonc.2015.00155. PMID: 26258068. PMCID: PMC4507461.
  • DOI: 10.3389/fonc.2015.00155.PMID
  • Vessoni A.T., Filippi-Chiela E.C., Lenz G., Batista L.F.Z. Tumor propagating cells: drivers of tumor plasticity, heterogeneity, and recurrence. Oncogene. 2020; 39: 2055-2068.
  • DOI: 10.1038/s41388-019-1128-4
  • Kleinmanns K., Fosse V., Davidson B., de Jalon E.G., Tenstad O., Bj0rge L., McCormack E. CD24-targeted intraoperative fluorescence image-guided surgery leads to improved cytoreduction of ovarian cancer in a preclinical orthotopic surgical model. EBioMedicine. 2020; 56: 102783. 10.1016/j.ebiom.2020.102783. PMID: 32454402. PMCID: PMC7248677.
  • DOI: 10.1016/j.ebiom.2020.102783.PMID
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