Defining a population of stem-like human prostate cancer cells that can generate and propagate castration-resistant prostate cancer

Clinical Cancer Research

Volumn 22, Issue 17, 2016, Pages 4505-4516

  Chen, Xin ^a,b,c   Li, Qiuhui ^a,c   Liu, Xin ^a   Liu, Can ^a   Liu, Ruifang ^a,c   Rycaj, Kiera ^a,c   Zhang, Dingxiao ^a,c   Liu, Bigang ^a   Jeter, Collene ^a   Calhoun Davis, Tammy ^a   Lin, Kevin ^a   Lu, Yue ^a   Chao, Hsueh Ping ^a   Shen, Jianjun ^a   Tang, Dean G ^a,c,d,e  

^a UNIVERSITY OF TEXAS   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d First Affiliated Hospital of Fourth Military Medical University   (China)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HERMES ANTIGEN; MICRORNA; MIR 499 5P; UNCLASSIFIED DRUG; ANDROGEN; SOX9 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX9; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CASTRATION RESISTANT PROSTATE CANCER; CELL ACTIVITY; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR PROMOTION; TUMOR XENOGRAFT; ANIMAL; CASTRATION; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETICS; IMMUNOPHENOTYPING; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHENOTYPE; TUMOR CELL CULTURE; TUMOR CELL LINE; XENOGRAFT;

ANDROGENS; ANIMALS; BIOMARKERS, TUMOR; CASTRATION; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; HETEROGRAFTS; HUMANS; IMMUNOPHENOTYPING; MALE; MICE; MICE, KNOCKOUT; MICRORNAS; NEOPLASTIC STEM CELLS; PHENOTYPE; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; SOX9 TRANSCRIPTION FACTOR; TUMOR CELLS, CULTURED;

EID: 84988662413     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-2956     Document Type: Article

References (44)

1. Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell 2014;14:275-91.
2. Tang DG. Understanding cancer stem cell heterogeneity and plasticity. Cell Res 2012;22:457-72.
3. Korkaya H, Wicha MS. Breast cancer stem cells: we've got them surrounded. Clin Cancer Res 2013;19:511-3.
4. Chen X, Rycaj K, Liu X, Tang DG. New insights into prostate cancer stem cells. Cell Cycle 2013;12:579-86.
5. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005; 65:10946-51.
6. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 2006;25:1696-708.
7. Patrawala L, Calhoun T, Schneider-Broussard R, Tang DG. Hierarchical organization of prostate cancer cells in xenograft tumors: the CD44+ α2β1+ cell population is enriched in tumor-initiating cells. Cancer Res 2007;67: 6796-805.
8. Li H, Chen X, Calhoun-Davis T, Claypool K, Tang DG. PC3 human prostate carcinoma cell holoclones contain self-renewing tumor-initiating cells. Cancer Res 2008;68:1820-5.
9. Dubrovska A, Kim S, Salamone RJ, Walker JR, Maira SM, Garcia-Echeverria C, et al. The role of PTEN/AKT/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc Natl Acad Sci U S A 2009;106:268-73.
10. Li T, Su Y, Mei Y, Leng Q, Leng B, Liu Z, et al. ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients' outcome. Lab Invest 2010;90:234-44.
11. Van den Hoogen C, van der Horst G, Cheung H, Buijs JT, Lippitt JM, Guzman-Ramirez N, et al. High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res 2010;70:5163-73.
12. Rajasekhar VK, Studer L, Gerald W, Socci ND, Scher HI. Tumor-initiating stem-like cells in human prostate cancer exhibit increased NF-κB signalling. Nat Commun 2011;2:162.
13. Domingo-Domenech J, Vidal SJ, Rodriguez-Bravo V, Castillo-Martin M, Quinn SA, Rodriguez-Barrueco R, et al. Suppression of acquired docetaxel resistance in prostate cancer through depletion of notch- and hedgehogdependent tumor-initiating cells. Cancer Cell 2012;22:373-88.
14. Germann M, Wetterwald A, Guzman-Ramirez N, van der Pluijm G, Culig Z, Cecchini MG, et al. Stem-like cells with luminal progenitor phenotype survive castration in human prostate cancer. Stem Cells 2012;30:1076-86.
15. Mulholland DJ, Kobayashi N, Ruscetti M, Zhi A, Tran LM, Huang J, et al. Pten loss and RAS/MAPK activation cooperate to promote EMT and metastasis initiated from prostate stem/progenitor cells. Cancer Res 2012; 72:1878-89.
16. Qin J, Liu X, Laffin B, Chen X, Choy G, Jeter CR, et al. The PSA-/lo prostate cancer cell population harbors self-renewing long-term tumor-propagating cells that resist castration. Cell Stem Cell 2012;10:556-69.
17. Yoshioka T, Otero J, Chen Y, Kim YM, Koutcher JA, Satagopan J, et al. b4 Integrin signaling induces expansion of prostate tumor progenitors. J Clin Invest 2013;123:682-99.
18. Li X, Liu Y, Chen W, Fang Y, Xu H, Zhu HH, et al. TOP2Ahigh is the phenotype of recurrence and metastasis whereas TOP2Aneg cells represent cancer stem cells in prostate cancer. Oncotarget 2014;5:9498-513.
19. Liu X, Chen X, Rycaj K, Chao HP, Deng Q, Jeter C, et al. Systematic dissection of phenotypic, functional, and tumorigenic heterogeneity of human prostate cancer cells. Oncotarget 2015;6:23959-86.
20. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015;65:5-29.
21. Kwon OJ, Xin L. Prostate epithelial stem and progenitor cells. Am J Clin Exp Urol 2014;2:209-18.
22. Goldstein AS, Huang J, Guo C, Garraway IP, Witte ON. Identification of a cell of origin for human prostate cancer. Science 2010;329:568-71.
23. Jiao J, Hindoyan A, Wang S, Tran LM, Goldstein AS, Lawson D, et al. Identification of CD166 as a surface marker for enriching prostate stem/ progenitor and cancer initiating cells. PLoS One 2012;7:e42564.
24. Tanaka H, Kono E, Tran CP, Miyazaki H, Yamashiro J, Shimomura T, et al. Monoclonal antibody targeting of N-Cadherin inhibits prostate cancer growth, metastasis and castration resistance. Nat Med 2010;16:1414-20.
25. Chen X, Liu B, Li Q, Honorio S, Liu X, Liu C, et al. Dissociated primary human prostate cancer cells coinjected with the immortalized Hs5 bone marrow stromal cells generate undifferentiated tumors in NOD/SCID-g mice. PLoS One 2013;8:e56903.
26. Chen CD, Welsbie DS, Tran C, Baek SH, Chen R, Vessella R, et al. Molecular determinants of resistance to androgen therapy. Nat Med 2004;10:33-9.
27. Cojoc M, Peitzsch C, Kurth I, Trautmann F, Kunz-Schughart LA, Telegeev GD, et al. Aldehyde dehydrogenase is regulated by b-catenin/TCF and promotes radioresistance in prostate cancer progenitor cells. Cancer Res 2015;75:1482-94.
28. Le Magnen C, Bubendorf L, Rentsch CA, Mengus C, Gsponer J, Zellweger T, et al. Characterization and clinical relevance of ALDHbright populations in prostate cancer. Clin Cancer Res 2013;19:5361-71.
29. Rycaj K, Tang DG. Cell-of-origin of cancer versus cancer stem cells: Assays and interpretations. Cancer Res 2015;75:4003-11.
30. Goldstein AS, Drake JM, Burnes DL, Finley DS, Zhang H, Reiter RE, et al. Purification and direct transformation of epithelial progenitor cells from primary human prostate. Nat Protoc 2011;6:656-67.
31. Karthaus WR, Iaquinta PJ, Drost J, Gracanin A, van Boxtel R, Wongvipat J, et al. Identification of multipotent luminal progenitor cells in human prostate organoid cultures. Cell 2014;159:163-75.
32. Gu Z, Rubin MA, Yang Y, Deprimo SE, Zhao H, Horvath S, et al. Reg IV: a promising marker of hormone refractory metastatic prostate cancer. Clin Cancer Res 2005;11:2237-43.
33. Wang Q, Li W, Zhang Y, Yuan X, Xu K, Yu J, et al. Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 2009;138:245-56.
34. Cai C, Wang H, He HH, Chen S, He L, Ma F, et al. ERG induces androgen receptor-mediated regulation of SOX9 in prostate cancer. J Clin Invest 2013;123:1109-22.
35. Xie Y, Lu W, Liu S, Yang Q, Carver BS, Li E, et al. Crosstalk between nuclear MET and SOX9/b-catenin correlates with castration-resistant prostate cancer. Mol Endocrinol 2014;28:1629-39.
36. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 2011;17:211-5.
37. Liu C, Tang DG. MicroRNA regulation of cancer stem cells. Cancer Res 2011;71:5950-4.
38. Jin M, Zhang T, Liu C, Badeaux MA, Liu B, Liu R, et al. miRNA-128 suppresses prostate cancer by inhibiting BMI-1 to inhibit tumor-initiating cells. Cancer Res 2014;74:4183-95.
39. Liu X, Zhang Z, Sun L, Chai N, Tang S, Jin J, et al. MiroRNA-499-5P promotes cellular invasion and tumor metastasis in colorectal cancer by targeting FOXO4 and PDCD4. Carcinogenesis 2011;32: 1798-805.
40. Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer 2013;13:714-26.
41. Wilson PM, Danenberg PV, Johnston PG, Lenz HJ, Ladner RD. Standing the test of time: targeting thymidylate biosynthesis in cancer therapy. Nat Rev Clin Oncol 2014;11:282-98.
42. Nelson WG, Yegnasubramanian S. Resistance emerges to second-generation antiandrogens in prostate cancer. Cancer Discov 2013;3:971-4.
43. Isaacs JT, Coffey DS. Adaptation versus selection as the mechanism responsible for the relapse of prostatic cancer to androgen ablation therapy as studied in the Dunning R-3327-H adenocarcinoma. Cancer Res 1981;41:5070-5.
44. Craft N, Chhor C, Tran C, Belldegrun A, DeKernion J, Witte ON, et al. Evidence for clonal outgrowth of androgen-independent prostate cancer cells from androgen-dependent tumors through a two-step process. Cancer Res 1999;59:5030-6.