Stem cell and neurogenic gene-expression profiles link prostate basal cells to aggressive prostate cancer

Nature Communications

Volumn 7, Issue , 2016, Pages

  Zhang, Dingxiao ^a   Park, Daechan ^b,e   Zhong, Yi ^a   Lu, Yue ^a   Rycaj, Kiera ^a   Gong, Shuai ^a   Chen, Xin ^a   Liu, Xin ^a   Chao, Hsueh Ping ^a   Whitney, Pamela ^a   Calhoun Davis, Tammy ^a   Takata, Yoko ^a   Shen, Jianjun ^a   Iyer, Vishwanath R ^b   Tang, Dean G ^a,c,d  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

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

^e The University of Texas at Austin   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH1 RECEPTOR; RIBOSOME RNA; STAT3 PROTEIN; TRANSCRIPTOME; BIOLOGICAL MARKER; MYC PROTEIN; MYC PROTEIN, HUMAN;

CANCER; CELLS AND CELL COMPONENTS; DISEASE INCIDENCE; GENE EXPRESSION; PROTEIN;

ADULT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CANCER STEM CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EPITHELIUM BASAL CELL; FETUS; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PROSTATE CANCER; RNA ANALYSIS; SIGNAL TRANSDUCTION; ADENOCARCINOMA; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROSTATE; PROSTATE TUMOR; RIBOSOME; STEM CELL;

ADENOCARCINOMA; BIOMARKERS; CELL LINEAGE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALE; PROSTATE; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; RIBOSOMES; RNA, RIBOSOMAL; STEM CELLS; TRANSCRIPTOME;

EID: 84959432150     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10798     Document Type: Article

References (60)

1. Liu, X. et al. Systematic dissection of phenotypic, functional, and tumorigenic heterogeneity of human prostate cancer cells. Oncotarget 6, 23959-23986 (2015).
2. Qin, J. et al. The PSA(-/lo) prostate cancer cell population harbors selfrenewing long-term tumor-propagating cells that resist castration. Cell Stem Cell 10, 556-569 (2012).
3. Shen, M. M. & Abate-Shen, C. Molecular genetics of prostate cancer: new prospects for old challenges. Genes Dev. 24, 1967-2000 (2010).
4. Pignon, J. C. et al. p63-expressing cells are the stem cells of developing prostate, bladder, and colorectal epithelia. Proc. Natl Acad. Sci. USA 110, 8105-8110 (2013).
5. Burger, P. E. et al. Sca-1 expression identifies stem cells in the proximal region of prostatic ducts with high capacity to reconstitute prostatic tissue. Proc. Natl Acad. Sci. USA 102, 7180-7185 (2005).
6. Goldstein, A. S., Huang, J., Guo, C., Garraway, I. P. & Witte, O. N. Identification of a cell of origin for human prostate cancer. Science 329, 568-571 (2010).
7. Lawson, D. A., Xin, L., Lukacs, R. U., Cheng, D. & Witte, O. N. Isolation and functional characterization of murine prostate stem cells. Proc. Natl Acad. Sci. USA 104, 181-186 (2007).
8. Leong, K. G., Wang, B. E., Johnson, L. & Gao, W. Q. Generation of a prostate from a single adult stem cell. Nature 456, 804-808 (2008).
9. Choi, N., Zhang, B., Zhang, L., Ittmann, M. & Xin, L. Adult murine prostate basal and luminal cells are self-sustained lineages that can both serve as targets for prostate cancer initiation. Cancer Cell 21, 253-265 (2012).
10. Ousset, M. et al. Multipotent and unipotent progenitors contribute to prostate postnatal development. Nat. Cell Biol. 14, 1131-1138 (2012).
11. Wang, J. et al. Symmetrical and asymmetrical division analysis provides evidence for a hierarchy of prostate epithelial cell lineages. Nat. Commun. 5, 4758 (2014).
12. Collins, A. T., Habib, F. K., Maitland, N. J. & Neal, D. E. Identification and isolation of human prostate epithelial stem cells based on alpha(2)beta(1)-integrin expression. J. Cell Sci. 114, 3865-3872 (2001).
13. Wang, Z. A., Toivanen, R., Bergren, S. K., Chambon, P. & Shen, M. M. Luminal cells are favored as the cell of origin for prostate cancer. Cell Rep. 8, 1339-1346 (2014).
14. Baca, S. C. et al. Punctuated evolution of prostate cancer genomes. Cell 153, 666-677 (2013).
15. Grasso, C. S. et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 487, 239-243 (2012).
16. Asangani, I. A. et al. Therapeutic targeting of BET bromodomain proteins in castration-resistant prostate cancer. Nature 510, 278-282 (2014).
17. Ngan, S. et al. Microarray coupled to quantitative RT-PCR analysis of androgen-regulated genes in human LNCaP prostate cancer cells. Oncogene 28, 2051-2063 (2009).
18. Wang, Y. et al. Comparative RNA-seq analysis reveals potential mechanisms mediating the conversion to androgen independence in an LNCaP progression cell model. Cancer Lett. 342, 130-138 (2014).
19. Karthaus, W. R. et al. Identification of multipotent luminal progenitor cells in human prostate organoid cultures. Cell 159, 163-175 (2014).
20. Wang, Z. A. et al. Lineage analysis of basal epithelial cells reveals their unexpected plasticity and supports a cell-of-origin model for prostate cancer heterogeneity. Nat. Cell Biol. 15, 274-283 (2013).
21. Valdez, J. M. et al. Notch and TGFb form a reciprocal positive regulatory loop that suppresses murine prostate basal stem/progenitor cell activity. Cell Stem Cell 11, 676-688 (2012).
22. Bendall, S. C. et al. IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 448, 1015-1021 (2007).
23. Azare, J. et al. Constitutively activated Stat3 induces tumorigenesis and enhances cell motility of prostate epithelial cells through integrin beta 6. Mol. Cell Biol. 27, 4444-4453 (2007).
24. Schroeder, A. et al. Loss of androgen receptor expression promotes a stem-like cell phenotype in prostate cancer through STAT3 signaling. Cancer Res. 74, 1227-1237 (2014).
25. Efroni, S. et al. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2, 437-447 (2008).
26. van Riggelen, J., Yetil, A. & Felsher, D. W. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat. Rev. Cancer 10, 301-309 (2010).
27. Hayashi, Y. et al. Downregulation of rRNA transcription triggers cell differentiation. PLoS ONE 9, e98586 (2014).
28. Watanabe-Susaki, K. et al. Biosynthesis of ribosomal RNA in nucleoli regulates pluripotency and differentiation ability of pluripotent stem cells. Stem Cells 32, 3099-3111 (2014).
29. Zhang, Q., Shalaby, N. A. & Buszczak, M. Changes in rRNA transcription influence proliferation and cell fate within a stem cell lineage. Science 343, 298-301 (2014).
30. Drygin, D. et al. Targeting RNA polymerase I with an oral small molecule CX-5461 inhibits ribosomal RNA synthesis and solid tumor growth. Cancer Res. 71, 1418-1430 (2011).
31. Delmore, J. E. et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 146, 904-917 (2011).
32. Neman, J. et al. Human breast cancer metastases to the brain display GABAergic properties in the neural niche. Proc. Natl Acad. Sci. USA 111, 984-989 (2014).
33. Ring, K. L. et al. Direct reprogramming of mouse and human fibroblasts into multipotent neural stem cells with a single factor. Cell Stem Cell 11, 100-109 (2012).
34. Yu, K. R. et al. Rapid and efficient direct conversion of human adult somatic cells into neural stem cells by HMGA2/let-7b. Cell Rep. 10, 441-452 (2015).
35. Li, W. et al. Rapid induction and long-term self-renewal of primitive neural precursors from human embryonic stem cells by small molecule inhibitors. Proc. Natl Acad. Sci. USA 108, 8299-8304 (2011).
36. Magnon, C. et al. Autonomic nerve development contributes to prostate cancer progression. Science 341, 1236361 (2013).
37. Nishino, J., Kim, I., Chada, K. & Morrison, S. J. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf expression. Cell 135, 227-239 (2008).
38. Andreeva, A. V. & Kutuzov, M. A. Cadherin 13 in cancer. Genes Chromosomes Cancer 49, 775-790 (2010).
39. Liu, A. Y., Roudier, M. P. & True, L. D. Heterogeneity in primary and metastatic prostate cancer as defined by cell surface CD profile. Am. J. Pathol. 165, 1543-1556 (2004).
40. Forster, N. et al. Basal cell signaling by p63 controls luminal progenitor function and lactation via NRG1. Dev. Cell 28, 147-160 (2014).
41. Beltran, H. et al. Aggressive variants of castration-resistant prostate cancer. Clin. Cancer Res. 20, 2846-2850 (2014).
42. Beltran, H. et al. Molecular characterization of neuroendocrine prostate cancer and identification of new drug targets. Cancer Discov. 1, 487-495 (2011).
43. Tzelepi, V. et al. Modeling a lethal prostate cancer variant with small-cell carcinoma features. Clin. Cancer Res. 18, 666-677 (2012).
44. Irshad, S. et al. A molecular signature predictive of indolent prostate cancer. Sci. Transl. Med. 5, 202ra122 (2013).
45. Rajan, P. et al. Next-generation sequencing of advanced prostate cancer treated with androgen-deprivation therapy. Eur. Urol. 66, 32-39 (2014).
46. Stoyanova, T. et al. Prostate cancer originating in basal cells progresses to adenocarcinoma propagated by luminal-like cells. Proc. Natl Acad. Sci. USA 110, 20111-20116 (2013).
47. Bywater, M. J. et al. Inhibition of RNA polymerase I as a therapeutic strategy to promote cancer-specific activation of p53. Cancer Cell 22, 51-65 (2012).
48. Smith, B. A. et al. A basal stem cell signature identifies aggressive prostate cancer phenotypes. Proc. Natl Acad. Sci. USA 112, E6544-E6552 (2015).
49. Goldstein, A. S. et al. Purification and direct transformation of epithelial progenitor cells from primary human prostate. Nat. Protoc. 6, 656-667 (2011).
50. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
51. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
52. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
53. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
54. Huang, da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
55. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).
56. Tibshirani, R., Hastie, T., Narasimhan, B. & Chu, G. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc. Natl Acad. Sci. USA 99, 6567-6572 (2002).
57. Ince, T. A. et al. Transformation of different human breast epithelial cell types leads to distinct tumor phenotypes. Cancer Cell 12, 160-170 (2007).
58. Bhatia, B. et al. Critical and distinct roles of p16 and telomerase in regulating the proliferative life span of normal human prostate epithelial progenitor cells. J. Biol. Chem. 283, 27957-27972 (2008).
59. Zhang, D., Jiang, P., Xu, Q. & Zhang, X. Arginine and glutamate-rich 1 (ARGLU1) interacts with mediator subunit 1 (MED1) and is required for estrogen receptor-mediated gene transcription and breast cancer cell growth. J. Biol. Chem. 286, 17746-17754 (2011).
60. Xin, L., Lukacs, R. U., Lawson, D. A., Cheng, D. &Witte, O. N. Self-renewal and multilineage differentiation in vitro from murine prostate stem cells. Stem Cells 25, 2760-2769 (2007).