Prostate cancer-derived holoclones: a novel and effective model for evaluating cancer stemness.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 07 2020
09 07 2020
Historique:
received:
10
02
2020
accepted:
19
06
2020
entrez:
11
7
2020
pubmed:
11
7
2020
medline:
1
1
2021
Statut:
epublish
Résumé
Prostate cancer accounts for approximately 13.5% of all newly diagnosed male cancer cases. Significant clinical burdens remain in terms of ineffective prognostication, with overtreatment of insignificant disease. Additionally, the pathobiology underlying disease heterogeneity remains poorly understood. As the role of cancer stem cells in the perpetuation of aggressive carcinoma is being substantiated by experimental evidence, it is crucially important to understand the molecular mechanisms, which regulate key features of cancer stem cells. We investigated two methods for in vitro cultivation of putative prostate cancer stem cells based on 'high-salt agar' and 'monoclonal cultivation'. Data demonstrated 'monoclonal cultivation' as the superior method. We demonstrated that 'holoclones' expressed canonical stem markers, retained the exclusive ability to generate poorly differentiated tumours in NOD/SCID mice and possessed a unique mRNA-miRNA gene signature. miRNA:Target interactions analysis visualised potentially critical regulatory networks, which are dysregulated in prostate cancer holoclones. The characterisation of this tumorigenic population lays the groundwork for this model to be used in the identification of proteomic or small non-coding RNA therapeutic targets for the eradication of this critical cellular population. This is significant, as it provides a potential route to limit development of aggressive disease and thus improve survival rates.
Identifiants
pubmed: 32647229
doi: 10.1038/s41598-020-68187-9
pii: 10.1038/s41598-020-68187-9
pmc: PMC7347552
doi:
Substances chimiques
Biomarkers, Tumor
0
MicroRNAs
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11329Références
Bray, F. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 68, 394–424. https://doi.org/10.3322/caac.21492 (2018).
doi: 10.3322/caac.21492
Salinas, C. A., Tsodikov, A., Ishak-Howard, M. & Cooney, K. A. Prostate cancer in young men: An important clinical entity. Nat. Rev. Urol. 11, 317–323. https://doi.org/10.1038/nrurol.2014.91 (2014).
doi: 10.1038/nrurol.2014.91
pubmed: 24818853
pmcid: 4191828
Inamura, K. Prostatic cancers: Understanding their molecular pathology and the 2016 WHO classification. Oncotarget 9, 14723–14737. https://doi.org/10.18632/oncotarget.24515 (2018).
doi: 10.18632/oncotarget.24515
pubmed: 29581876
pmcid: 5865702
Gandhi, J. et al. The molecular biology of prostate cancer: Current understanding and clinical implications. Prostate Cancer Prostatic Dis. 21, 22–36. https://doi.org/10.1038/s41391-017-0023-8 (2018).
doi: 10.1038/s41391-017-0023-8
pubmed: 29282359
Hughes, C., Murphy, A., Martin, C., Sheils, O. & O’Leary, J. Molecular pathology of prostate cancer. J. Clin. Pathol. 58, 673–684. https://doi.org/10.1136/jcp.2002.003954 (2005).
doi: 10.1136/jcp.2002.003954
pubmed: 15976331
pmcid: 1770715
Batlle, E. & Clevers, H. Cancer stem cells revisited. Nat. Med. 23, 1124–1134. https://doi.org/10.1038/nm.4409 (2017).
doi: 10.1038/nm.4409
pubmed: 28985214
Maitland, N. J. & Collins, A. T. Cancer stem cells—A therapeutic target?. Curr. Opin. Mol. Ther. 12, 662–673 (2010).
pubmed: 21154158
Packer, J. R. & Maitland, N. J. The molecular and cellular origin of human prostate cancer. Biochim. Biophys. Acta 1238–1260, 2016. https://doi.org/10.1016/j.bbamcr.2016.02.016 (1863).
doi: 10.1016/j.bbamcr.2016.02.016
Dexter, T. M., Allen, T. D. & Lajtha, L. G. Conditions controlling the proliferation of haemopoietic stem cells in vitro. J. Cell Physiol. 91, 335–344. https://doi.org/10.1002/jcp.1040910303 (1977).
doi: 10.1002/jcp.1040910303
pubmed: 301143
Foster, C. S., Dodson, A., Karavana, V., Smith, P. H. & Ke, Y. Prostatic stem cells. J. Pathol. 197, 551–565. https://doi.org/10.1002/path.1194 (2002).
doi: 10.1002/path.1194
pubmed: 12115870
Hall, P. A. & Watt, F. M. Stem cells: The generation and maintenance of cellular diversity. Development 106, 619–633 (1989).
pubmed: 2562658
Barrandon, Y. & Green, H. Three clonal types of keratinocyte with different capacities for multiplication. Proc. Natl. Acad. Sci. USA 84, 2302–2306. https://doi.org/10.1073/pnas.84.8.2302 (1987).
doi: 10.1073/pnas.84.8.2302
pubmed: 2436229
Jordan, C. T., Guzman, M. L. & Noble, M. Cancer stem cells. N. Engl. J. Med. 355, 1253–1261. https://doi.org/10.1056/NEJMra061808 (2006).
doi: 10.1056/NEJMra061808
pubmed: 16990388
Mackenzie, I. C. Retention of stem cell patterns in malignant cell lines. Cell Prolif. 38, 347–355. https://doi.org/10.1111/j.1365-2184.2005.00355.x (2005).
doi: 10.1111/j.1365-2184.2005.00355.x
pubmed: 16300648
pmcid: 6496197
Reya, T., Morrison, S. J., Clarke, M. F. & Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105–111. https://doi.org/10.1038/35102167 (2001).
doi: 10.1038/35102167
pubmed: 11689955
Skvortsov, S., Skvortsova, I. I., Tang, D. G. & Dubrovska, A. Concise review: Prostate cancer stem cells: Current understanding. Stem Cells 36, 1457–1474. https://doi.org/10.1002/stem.2859 (2018).
doi: 10.1002/stem.2859
pubmed: 29845679
Rybak, A. P., Bristow, R. G. & Kapoor, A. Prostate cancer stem cells: Deciphering the origins and pathways involved in prostate tumorigenesis and aggression. Oncotarget 6, 1900–1919. https://doi.org/10.18632/oncotarget.2953 (2015).
doi: 10.18632/oncotarget.2953
pubmed: 25595909
Mei, W. et al. The contributions of prostate cancer stem cells in prostate cancer initiation and metastasis. Cancers (Basel) https://doi.org/10.3390/cancers11040434 (2019).
doi: 10.3390/cancers11040434
Li, J. J. & Shen, M. M. Prostate stem cells and cancer stem cells. Cold Spring Harb. Perspect. Med. https://doi.org/10.1101/cshperspect.a030395 (2019).
doi: 10.1101/cshperspect.a030395
pubmed: 30291148
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 100, 3983–3988. https://doi.org/10.1073/pnas.0530291100 (2003).
doi: 10.1073/pnas.0530291100
pubmed: 12629218
Singh, S. K. et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63, 5821–5828 (2003).
pubmed: 14522905
O’Brien, C. A., Pollett, A., Gallinger, S. & Dick, J. E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445, 106–110. https://doi.org/10.1038/nature05372 (2007).
doi: 10.1038/nature05372
pubmed: 17122772
Li, C., Lee, C. J. & Simeone, D. M. Identification of human pancreatic cancer stem cells. Methods Mol. .Biol 568, 161–173. https://doi.org/10.1007/978-1-59745-280-9_10 (2009).
doi: 10.1007/978-1-59745-280-9_10
pubmed: 19582426
Bertolini, G. et al. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc. Natl. Acad. Sci. USA 106, 16281–16286. https://doi.org/10.1073/pnas.0905653106 (2009).
doi: 10.1073/pnas.0905653106
pubmed: 19805294
Cojoc, M. et al. Aldehyde dehydrogenase is regulated by beta-catenin/TCF and promotes radioresistance in prostate cancer progenitor cells. Cancer Res. 75, 1482–1494. https://doi.org/10.1158/0008-5472.can-14-1924 (2015).
doi: 10.1158/0008-5472.can-14-1924
pubmed: 25670168
Kyriakopoulos, C. E. et al. Chemohormonal therapy in metastatic hormone-sensitive prostate cancer: long-term survival analysis of the randomized phase III E3805 CHAARTED trial. J. Clin. .Oncol 36, 1080–1087. https://doi.org/10.1200/jco.2017.75.3657 (2018).
doi: 10.1200/jco.2017.75.3657
pubmed: 29384722
pmcid: 5891129
Olszewski, W. L., Moscicka, M., Zolich, D. & Machowski, Z. Human keratinocyte stem cells survive for months in sodium chloride and can be successfully transplanted. Transpl. Proc. 37, 525–526. https://doi.org/10.1016/j.transproceed.2004.12.174 (2005).
doi: 10.1016/j.transproceed.2004.12.174
Zhang, K. & Waxman, D. J. PC3 prostate tumor-initiating cells with molecular profile FAM65Bhigh/MFI2low/LEF1low increase tumor angiogenesis. Mol. Cancer 9, 319. https://doi.org/10.1186/1476-4598-9-319 (2010).
doi: 10.1186/1476-4598-9-319
pubmed: 21190562
pmcid: 3024252
Wintzell, M. et al. Repeated cisplatin treatment can lead to a multiresistant tumor cell population with stem cell features and sensitivity to 3-bromopyruvate. Cancer Biol. Ther. 13, 1454–1462. https://doi.org/10.4161/cbt.22007 (2012).
doi: 10.4161/cbt.22007
pubmed: 22954696
pmcid: 3542237
Li, H., Chen, X., Calhoun-Davis, T., Claypool, K. & Tang, D. G. PC3 human prostate carcinoma cell holoclones contain self-renewing tumor-initiating cells. Cancer Res. 68, 1820–1825. https://doi.org/10.1158/0008-5472.can-07-5878 (2008).
doi: 10.1158/0008-5472.can-07-5878
pubmed: 18339862
Locke, M., Heywood, M., Fawell, S. & Mackenzie, I. C. Retention of intrinsic stem cell hierarchies in carcinoma-derived cell lines. Cancer Res. 65, 8944–8950. https://doi.org/10.1158/0008-5472.can-05-0931 (2005).
doi: 10.1158/0008-5472.can-05-0931
pubmed: 16204067
Pfeiffer, M. J. & Schalken, J. A. Stem cell characteristics in prostate cancer cell lines. Eur. Urol. 57, 246–254. https://doi.org/10.1016/j.eururo.2009.01.015 (2010).
doi: 10.1016/j.eururo.2009.01.015
pubmed: 19200636
Patrawala, L. et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25, 1696–1708. https://doi.org/10.1038/sj.onc.1209327 (2006).
doi: 10.1038/sj.onc.1209327
pubmed: 16449977
Tan, L., Sui, X., Deng, H. & Ding, M. Holoclone forming cells from pancreatic cancer cells enrich tumor initiating cells and represent a novel model for study of cancer stem cells. PLoS ONE 6, e23383. https://doi.org/10.1371/journal.pone.0023383 (2011).
doi: 10.1371/journal.pone.0023383
pubmed: 21826251
pmcid: 3149653
Jeter, C. R. et al. Functional evidence that the self-renewal gene NANOG regulates human tumor development. Stem Cells 27, 993–1005. https://doi.org/10.1002/stem.29 (2009).
doi: 10.1002/stem.29
pubmed: 19415763
pmcid: 3327393
Liu, T. J. et al. CD133+ cells with cancer stem cell characteristics associates with vasculogenic mimicry in triple-negative breast cancer. Oncogene 32, 544–553. https://doi.org/10.1038/onc.2012.85 (2013).
doi: 10.1038/onc.2012.85
pubmed: 22469978
Harper, L. J., Piper, K., Common, J., Fortune, F. & Mackenzie, I. C. Stem cell patterns in cell lines derived from head and neck squamous cell carcinoma. J. Oral Pathol. Med. 36, 594–603. https://doi.org/10.1111/j.1600-0714.2007.00617.x (2007).
doi: 10.1111/j.1600-0714.2007.00617.x
pubmed: 17944752
Ferrand, A., Sandrin, M. S., Shulkes, A. & Baldwin, G. S. Expression of gastrin precursors by CD133-positive colorectal cancer cells is crucial for tumour growth. Biochim. Biophys. Acta 1793, 477–488. https://doi.org/10.1016/j.bbamcr.2009.01.004 (2009).
doi: 10.1016/j.bbamcr.2009.01.004
pubmed: 19321126
pmcid: 2692632
Tang, D. G. et al. Prostate cancer stem/progenitor cells: Identification, characterization, and implications. Mol. Carcinog. 46, 1–14. https://doi.org/10.1002/mc.20255 (2007).
doi: 10.1002/mc.20255
pubmed: 16921491
Russell, P. J. et al. Establishing prostate cancer patient derived xenografts: Lessons learned from older studies. Prostate 75, 628–636. https://doi.org/10.1002/pros.22946 (2015).
doi: 10.1002/pros.22946
pubmed: 25560784
pmcid: 4415460
Liu, X. et al. Systematic dissection of phenotypic, functional, and tumorigenic heterogeneity of human prostate cancer cells. Oncotarget 6, 23959–23986. https://doi.org/10.18632/oncotarget.4260 (2015).
doi: 10.18632/oncotarget.4260
pubmed: 26246472
pmcid: 4695164
Rajasekhar, V. K., Studer, L., Gerald, W., Socci, N. D. & Scher, H. I. Tumour-initiating stem-like cells in human prostate cancer exhibit increased NF-kappaB signalling. Nat. Commun. 2, 162. https://doi.org/10.1038/ncomms1159 (2011).
doi: 10.1038/ncomms1159
pubmed: 21245843
pmcid: 3105310
Tokar, E. J., Ancrile, B. B., Cunha, G. R. & Webber, M. M. Stem/progenitor and intermediate cell types and the origin of human prostate cancer. Differentiation 73, 463–473. https://doi.org/10.1111/j.1432-0436.2005.00047.x (2005).
doi: 10.1111/j.1432-0436.2005.00047.x
pubmed: 16351690
Stone, K. R., Mickey, D. D., Wunderli, H., Mickey, G. H. & Paulson, D. F. Isolation of a human prostate carcinoma cell line (DU 145). Int. J. Cancer 21, 274–281. https://doi.org/10.1002/ijc.2910210305 (1978).
doi: 10.1002/ijc.2910210305
pubmed: 631930
Sramkoski, R. M. et al. A new human prostate carcinoma cell line, 22Rv1. Vitro Cell Dev. Biol. Anim. 35, 403–409. https://doi.org/10.1007/s11626-999-0115-4 (1999).
doi: 10.1007/s11626-999-0115-4
Kaighn, M. E., Narayan, K. S., Ohnuki, Y., Lechner, J. F. & Jones, L. W. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest. Urol. 17, 16–23 (1979).
pubmed: 447482
Horoszewicz, J. S. et al. LNCaP model of human prostatic carcinoma. Cancer Res. 43, 1809–1818 (1983).
pubmed: 6831420
Pulukuri, S. M. et al. RNA interference-directed knockdown of urokinase plasminogen activator and urokinase plasminogen activator receptor inhibits prostate cancer cell invasion, survival, and tumorigenicity in vivo. J. Biol. Chem. 280, 36529–36540. https://doi.org/10.1074/jbc.M503111200 (2005).
doi: 10.1074/jbc.M503111200
pubmed: 16127174
Gallagher, M. F. et al. Enhanced regulation of cell cycle and suppression of osteoblast differentiation molecular signatures by prostate cancer stem-like holoclones. J. Clin. Pathol. 68, 692–702. https://doi.org/10.1136/jclinpath-2015-203001 (2015).
doi: 10.1136/jclinpath-2015-203001
pubmed: 26038242
Lynam-Lennon, N. et al. MicroRNA-17 is downregulated in esophageal adenocarcinoma cancer stem-like cells and promotes a radioresistant phenotype. Oncotarget 8, 11400–11413. https://doi.org/10.18632/oncotarget.13940 (2017).
doi: 10.18632/oncotarget.13940
pubmed: 28002789
Patrawala, L., Calhoun-Davis, T., Schneider-Broussard, R. & Tang, D. G. Hierarchical organization of prostate cancer cells in xenograft tumors: the CD44+alpha2beta1+ cell population is enriched in tumor-initiating cells. Cancer Res. 67, 6796–6805. https://doi.org/10.1158/0008-5472.can-07-0490 (2007).
doi: 10.1158/0008-5472.can-07-0490
pubmed: 17638891
Matsuda, S. et al. Cancer stem cells maintain a hierarchy of differentiation by creating their niche. Int. J. Cancer 135, 27–36. https://doi.org/10.1002/ijc.28648 (2014).
doi: 10.1002/ijc.28648
pubmed: 24323788
Wei, C., Guomin, W., Yujun, L. & Ruizhe, Q. Cancer stem-like cells in human prostate carcinoma cells DU145: The seeds of the cell line?. Cancer Biol. Ther. 6, 763–768. https://doi.org/10.4161/cbt.6.5.3996 (2007).
doi: 10.4161/cbt.6.5.3996
pubmed: 17592251
Rochat, A., Kobayashi, K. & Barrandon, Y. Location of stem cells of human hair follicles by clonal analysis. Cell 76, 1063–1073 (1994).
doi: 10.1016/0092-8674(94)90383-2
Pellegrini, G. et al. Location and clonal analysis of stem cells and their differentiated progeny in the human ocular surface. J. Cell Biol. 145, 769–782. https://doi.org/10.1083/jcb.145.4.769 (1999).
doi: 10.1083/jcb.145.4.769
pubmed: 10330405
pmcid: 2133195
Papini, S. et al. Isolation and clonal analysis of human epidermal keratinocyte stem cells in long-term culture. Stem Cells 21, 481–494. https://doi.org/10.1634/stemcells.21-4-481 (2003).
doi: 10.1634/stemcells.21-4-481
pubmed: 12832701
Zhou, Z. H. et al. A novel approach to the identification and enrichment of cancer stem cells from a cultured human glioma cell line. Cancer Lett. 281, 92–99. https://doi.org/10.1016/j.canlet.2009.02.033 (2009).
doi: 10.1016/j.canlet.2009.02.033
pubmed: 19324493
Collins, A. T., Berry, P. A., Hyde, C., Stower, M. J. & Maitland, N. J. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 65, 10946–10951. https://doi.org/10.1158/0008-5472.can-05-2018 (2005).
doi: 10.1158/0008-5472.can-05-2018
pubmed: 16322242
Beaver, C. M., Ahmed, A. & Masters, J. R. Clonogenicity: holoclones and meroclones contain stem cells. PLoS ONE 9, e89834. https://doi.org/10.1371/journal.pone.0089834 (2014).
doi: 10.1371/journal.pone.0089834
pubmed: 24587067
pmcid: 3935944
Moltzahn, F. & Thalmann, G. N. Cancer stem cells in prostate cancer. Transl. Androl. Urol. 2, 242–253. https://doi.org/10.3978/j.issn.2223-4683.2013.09.06 (2013).
doi: 10.3978/j.issn.2223-4683.2013.09.06
pubmed: 26816738
pmcid: 4708185
Hess, D. A. et al. Functional characterization of highly purified human hematopoietic repopulating cells isolated according to aldehyde dehydrogenase activity. Blood 104, 1648–1655. https://doi.org/10.1182/blood-2004-02-0448 (2004).
doi: 10.1182/blood-2004-02-0448
pubmed: 15178579
Ginestier, C. et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1, 555–567. https://doi.org/10.1016/j.stem.2007.08.014 (2007).
doi: 10.1016/j.stem.2007.08.014
pubmed: 18371393
pmcid: 2423808
Corti, S. et al. Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. Stem Cells 24, 975–985. https://doi.org/10.1634/stemcells.2005-0217 (2006).
doi: 10.1634/stemcells.2005-0217
pubmed: 16293577
Doherty, R. E., Haywood-Small, S. L., Sisley, K. & Cross, N. A. Aldehyde dehydrogenase activity selects for the holoclone phenotype in prostate cancer cells. Biochem. Biophys. Res. Commun. 414, 801–807. https://doi.org/10.1016/j.bbrc.2011.10.010 (2011).
doi: 10.1016/j.bbrc.2011.10.010
pubmed: 22005464
Bissell, M. J. & Labarge, M. A. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment?. Cancer Cell 7, 17–23. https://doi.org/10.1016/j.ccr.2004.12.013 (2005).
doi: 10.1016/j.ccr.2004.12.013
pubmed: 15652746
pmcid: 2933216
Zhou, Y. et al. Isolation and identification of cancer stem cells from PC3 human prostate carcinoma cell line. Int. J. Clin. Exp. Pathol. 10, 8377–8382 (2017).
pubmed: 31966689
pmcid: 6965485
Liu, C. et al. MicroRNA-141 suppresses prostate cancer stem cells and metastasis by targeting a cohort of pro-metastasis genes. Nat. Commun. 8, 14270. https://doi.org/10.1038/ncomms14270 (2017).
doi: 10.1038/ncomms14270
pubmed: 28112170
pmcid: 5264244
Hsieh, I. S. et al. MicroRNA-320 suppresses the stem cell-like characteristics of prostate cancer cells by downregulating the Wnt/beta-catenin signaling pathway. Carcinogenesis 34, 530–538. https://doi.org/10.1093/carcin/bgs371 (2013).
doi: 10.1093/carcin/bgs371
pubmed: 23188675
Jin, M. et al. miRNA-128 suppresses prostate cancer by inhibiting BMI-1 to inhibit tumor-initiating cells. Cancer Res. 74, 4183–4195. https://doi.org/10.1158/0008-5472.can-14-0404 (2014).
doi: 10.1158/0008-5472.can-14-0404
pubmed: 24903149
pmcid: 4174451
Huang, S. et al. miR-143 and miR-145 inhibit stem cell characteristics of PC-3 prostate cancer cells. Oncol. Rep. 28, 1831–1837. https://doi.org/10.3892/or.2012.2015 (2012).
doi: 10.3892/or.2012.2015
pubmed: 22948942
Sadeghi, M. et al. MicroRNA and transcription factor gene regulatory network analysis reveals key regulatory elements associated with prostate cancer progression. PLoS ONE 11, e0168760. https://doi.org/10.1371/journal.pone.0168760 (2016).
doi: 10.1371/journal.pone.0168760
pubmed: 28005952
pmcid: 5179129
Tao, Z. Q. et al. Role of microRNA in prostate cancer stem/progenitor cells regulation. Eur. Rev. Med. Pharmacol. Sci. 20, 3040–3044 (2016).
pubmed: 27460733
Rane, J. K. et al. MicroRNA expression profile of primary prostate cancer stem cells as a source of biomarkers and therapeutic targets. Eur. Urol. 67, 7–10. https://doi.org/10.1016/j.eururo.2014.09.005 (2015).
doi: 10.1016/j.eururo.2014.09.005
pubmed: 25234358
Wang, D., Lu, G., Shao, Y. & Xu, D. MiR-182 promotes prostate cancer progression through activating Wnt/beta-catenin signal pathway. Biomed. Pharmacother. 99, 334–339. https://doi.org/10.1016/j.biopha.2018.01.082 (2018).
doi: 10.1016/j.biopha.2018.01.082
pubmed: 29353209
Baumann, B. et al. Association of high miR-182 levels with low-risk prostate cancer. Am. J. Pathol. 189, 911–923. https://doi.org/10.1016/j.ajpath.2018.12.014 (2019).
doi: 10.1016/j.ajpath.2018.12.014
pubmed: 30703341
pmcid: 6446228
Guan, H. et al. MicroRNA-744 promotes prostate cancer progression through aberrantly activating Wnt/beta-catenin signaling. Oncotarget 8, 14693–14707. https://doi.org/10.18632/oncotarget.14711 (2017).
doi: 10.18632/oncotarget.14711
pubmed: 28107193
pmcid: 5362436
Zhang, M., Li, H., Zhang, Y. & Li, H. Oncogenic miR-744 promotes prostate cancer growth through direct targeting of LKB1. Oncol. Lett. 17, 2257–2265. https://doi.org/10.3892/ol.2018.9822 (2019).
doi: 10.3892/ol.2018.9822
pubmed: 30675291
Vlachos, I. S. et al. DIANA-miRPath v3.0: Deciphering microRNA function with experimental support. Nucleic Acids Res. 43, W460–W466. https://doi.org/10.1093/nar/gkv403 (2015).
doi: 10.1093/nar/gkv403
pubmed: 25977294
pmcid: 4489228
Liu, C. et al. Distinct microRNA expression profiles in prostate cancer stem/progenitor cells and tumor-suppressive functions of let-7. Cancer Res. 72, 3393–3404. https://doi.org/10.1158/0008-5472.can-11-3864 (2012).
doi: 10.1158/0008-5472.can-11-3864
pubmed: 22719071
Duan, F. et al. Area under the curve as a tool to measure kinetics of tumor growth in experimental animals. J. Immunol. Methods 382, 224–228. https://doi.org/10.1016/j.jim.2012.06.005 (2012).
doi: 10.1016/j.jim.2012.06.005
pubmed: 22698786
Joshi, N. A. & Fass, J. N. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33) [Software]. Available at https://github.com/najoshi/sickle (2011).
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12. https://doi.org/10.14806/ej.17.1.200 (2011).
doi: 10.14806/ej.17.1.200
Chen, C., Khaleel, S. S., Huang, H. & Wu, C. H. Software for pre-processing Illumina next-generation sequencing short read sequences. Source Code Biol. Med. 9, 8. https://doi.org/10.1186/1751-0473-9-8 (2014).
doi: 10.1186/1751-0473-9-8
pubmed: 24955109
pmcid: 4064128
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25. https://doi.org/10.1186/gb-2009-10-3-r25 (2009).
doi: 10.1186/gb-2009-10-3-r25
pubmed: 19261174
pmcid: 2690996
Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105–1111. https://doi.org/10.1093/bioinformatics/btp120 (2009).
doi: 10.1093/bioinformatics/btp120
pubmed: 19289445
pmcid: 2672628
Anders, S., Pyl, P. T. & Huber, W. HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169. https://doi.org/10.1093/bioinformatics/btu638 (2015).
doi: 10.1093/bioinformatics/btu638
pubmed: 25260700
pmcid: 25260700
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140. https://doi.org/10.1093/bioinformatics/btp616 (2010).
doi: 10.1093/bioinformatics/btp616
pubmed: 19910308
pmcid: 19910308