TLR9 signaling through NF-κB/RELA and STAT3 promotes tumor-propagating potential of prostate cancer cells

Oncotarget

Volumn 6, Issue 19, 2015, Pages 17302-17313

  Moreira, Dayson ^a   Zhang, Qifang ^a   Hossain, Dewan Md S ^a   Nechaev, Sergey ^a   Li, Haiqing ^a   Kowolik, Claudia M ^a   D'Apuzzo, Massimo ^a   Forman, Stephen ^a   Jones, Jeremy ^a   Pal, Sumanta K ^a   Kortylewski, Marcin ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Prostate cancer; RELA; STAT3; TLR9; Tumor propagating cells

Indexed keywords

COLLAGEN TYPE 1; CPG OLIGODEOXYNUCLEOTIDE; SMALL INTERFERING RNA; STAT3 PROTEIN; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX3.1; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RELA PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN; TLR9 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BMI 1 GENE; CANCER GROWTH; COL1A1 GENE; CONTROLLED STUDY; FEASIBILITY STUDY; GENE; GENE EXPRESSION REGULATION; GENE TARGETING; GENOME ANALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; KLF 4 GENE; LNCAP CELL LINE; MALE; MOUSE; NKX3.1 GENE; NONHUMAN; PROMOTER REGION; PROSTATE CANCER; PROSTATE CANCER CELL LINE; XENOTRANSPLANTATION; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; FLOW CYTOMETRY; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR; REAL TIME POLYMERASE CHAIN REACTION; SCID MOUSE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; NF-KAPPA B; PROSTATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 9; TRANSCRIPTION FACTOR RELA;

EID: 84938254969     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4029     Document Type: Article

References (43)

1. DeSantis CE, Lin CC, Mariotto AB, Siegel RL, Stein KD, Kramer JL, Alteri R, Robbins AS, Jemal A. Cancer treatment and survivorship statistics, 2014. CA: a cancer journal for clinicians. 2014; 64:252-271.
2. De Marzo AM, Platz EA, Sutcliffe S, Xu J, Gronberg H, Drake CG, Nakai Y, Isaacs WB, Nelson WG. Inflammation in prostate carcinogenesis. Nat Rev Cancer. 2007; 7:256-269.
3. Sfanos KS, De Marzo AM. Prostate cancer and inflammation: the evidence. Histopathology. 2012; 60:199-215.
4. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010; 11:373-384.
5. Rayburn ER, Wang W, Zhang Z, Li M, Zhang R, Wang H. Experimental therapy of prostate cancer with an immunomodulatory oligonucleotide: effects on tumor growth, apoptosis, proliferation, and potentiation of chemotherapy. Prostate. 2006; 66:1653-1663.
6. Shatz M, Menendez D, Resnick MA. The human TLR innate immune gene family is differentially influenced by DNA stress and p53 status in cancer cells. Cancer Res. 2012; 72:3948-3957.
7. Ilvesaro JM, Merrell MA, Swain TM, Davidson J, Zayzafoon M, Harris KW, Selander KS. Toll like receptor-9 agonists stimulate prostate cancer invasion in vitro. Prostate. 2007; 67:774-781.
8. Gonzalez-Reyes S, Fernandez JM, Gonzalez LO, Aguirre A, Suarez A, Gonzalez JM, Escaff S, Vizoso FJ. Study of TLR3, TLR4, and TLR9 in prostate carcinomas and their association with biochemical recurrence. Cancer Immunol Immunother. 2011; 60:217-226.
9. Gao C, Kozlowska A, Nechaev S, Li H, Zhang Q, Hossain DM, Kowolik CM, Chu P, Swiderski P, Diamond DJ, Pal SK, Raubitschek A, Kortylewski M. TLR9 Signaling in the Tumor Microenvironment Initiates Cancer Recurrence after Radiotherapy. Cancer Res. 2013; 73:7211-7221.
10. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature. 2010; 464:104-107.
11. Murray PJ, Smale ST. Restraint of inflammatory signaling by interdependent strata of negative regulatory pathways. Nat Immunol. 2012; 13:916-924.
12. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009; 9:798-809.
13. Vicari AP, Chiodoni C, Vaure C, Ait-Yahia S, Dercamp C, Matsos F, Reynard O, Taverne C, Merle P, Colombo MP, O'Garra A, Trinchieri G, Caux C. Reversal of tumor-induced dendritic cell paralysis by CpG immunostimulatory oligonucleotide and anti-interleukin 10 receptor antibody. J Exp Med. 2002; 196:541-549.
14. Kortylewski M, Kujawski M, Herrmann A, Yang C, Wang L, Liu Y, Salcedo R, Yu H. Toll-like receptor 9 activation of signal transducer and activator of transcription 3 constrains its agonist-based immunotherapy. Cancer Res. 2009; 69:2497-2505.
15. Ben-Neriah Y, Karin M. Inflammation meets cancer, with NF-kappaB as the matchmaker. Nat Immunol. 2011; 12:715-723.
16. Lee H, Deng J, Xin H, Liu Y, Pardoll D, Yu H. A Requirement of STAT3 DNA Binding Precludes Th-1 Immunostimulatory Gene Expression by NF-{kappa}B in Tumors. Cancer Res. 2011; 71:3772-3780.
17. Mora LB, Buettner R, Seigne J, Diaz J, Ahmad N, Garcia R, Bowman T, Falcone R, Fairclough R, Cantor A, Muro-Cacho C, Livingston S, Karras J, Pow-Sang J, Jove R. Constitutive activation of Stat3 in human prostate tumors and cell lines: direct inhibition of Stat3 signaling induces apoptosis of prostate cancer cells. Cancer Res. 2002; 62:6659-6666.
18. Zerbini LF, Wang Y, Cho JY, Libermann TA. Constitutive activation of nuclear factor kappaB p50/p65 and Fra-1 and JunD is essential for deregulated interleukin 6 expression in prostate cancer. Cancer Res. 2003; 63:2206-2215.
19. Lou W, Ni Z, Dyer K, Tweardy DJ, Gao AC. Interleukin-6 induces prostate cancer cell growth accompanied by activation of stat3 signaling pathway. Prostate. 2000; 42:239-242.
20. Qin J, Liu X, Laffin B, Chen X, Choy G, Jeter CR, Calhoun-Davis T, Li H, Palapattu GS, Pang S, Lin K, Huang J, Ivanov I, Li W, Suraneni MV, Tang DG. The PSA(-/lo) prostate cancer cell population harbors self-renewing long-term tumor-propagating cells that resist castration. Cell Stem Cell. 2012; 10:556-569.
21. Kreso A, van Galen P, Pedley NM, Lima-Fernandes E, Frelin C, Davis T, Cao L, Baiazitov R, Du W, Sydorenko N, Moon YC, Gibson L, Wang Y, Leung C, Iscove NN, Arrowsmith CH, et al. Self-renewal as a therapeutic target in human colorectal cancer. Nat Med. 2014; 20:29-36.
22. Zhau HE, He H, Wang CY, Zayzafoon M, Morrissey C, Vessella RL, Marshall FF, Chung LW, Wang R. Human prostate cancer harbors the stem cell properties of bone marrow mesenchymal stem cells. Clin Cancer Res. 2011; 17:2159-2169.
23. Lukacs RU, Memarzadeh S, Wu H, Witte ON. Bmi-1 is a crucial regulator of prostate stem cell self-renewal and malignant transformation. Cell stem cell. 2010; 7:682-693.
24. Wang X, Kruithof-de Julio M, Economides KD, Walker D, Yu H, Halili MV, Hu YP, Price SM, Abate-Shen C, Shen MM. A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature. 2009; 461:495-500.
25. Scharer CD, McCabe CD, Ali-Seyed M, Berger MF, Bulyk ML, Moreno CS. Genome-wide promoter analysis of the SOX4 transcriptional network in prostate cancer cells. Cancer Res. 2009; 69:709-717.
26. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature. 2007; 448:318-324.
27. 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; 68:1820-1825.
28. Zhang Q, Hossain DM, Nechaev S, Kozlowska A, Zhang W, Liu Y, Kowolik CM, Swiderski P, Rossi JJ, Forman S, Pal S, Bhatia R, Raubitschek A, Yu H, Kortylewski M. TLR9-mediated siRNA delivery for targeting of normal and malignant human hematopoietic cells in vivo. Blood. 2013; 121:1304-1315.
29. Vaisanen MR, Vaisanen T, Jukkola-Vuorinen A, Vuopala KS, Desmond R, Selander KS, Vaarala MH. Expression of toll-like receptor-9 is increased in poorly differentiated prostate tumors. Prostate. 2010; 70:817-824.
30. Kundu SD, Lee C, Billips BK, Habermacher GM, Zhang Q, Liu V, Wong LY, Klumpp DJ, Thumbikat P. The toll-like receptor pathway: a novel mechanism of infection-induced carcinogenesis of prostate epithelial cells. Prostate. 2008; 68:223-229.
31. Yang T, Rycaj K, Liu ZM, Tang DG. Cancer stem cells: constantly evolving and functionally heterogeneous therapeutic targets. Cancer Res. 2013; 74:2922-2927.
32. Germann M, Wetterwald A, Guzman-Ramirez N, van der Pluijm G, Culig Z, Cecchini MG, Williams ED, Thalmann GN. Stem-like cells with luminal progenitor phenotype survive castration in human prostate cancer. Stem cells (Dayton, Ohio). 2012; 30:1076-1086.
33. Magee JA, Piskounova E, Morrison SJ. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell. 2012; 21:283-296.
34. Oka T, Hikoso S, Yamaguchi O, Taneike M, Takeda T, Tamai T, Oyabu J, Murakawa T, Nakayama H, Nishida K, Akira S, Yamamoto A, Komuro I, Otsu K. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature. 2012; 485:251-255.
35. Jin R, Yi Y, Yull FE, Blackwell TS, Clark PE, Koyama T, Smith JA Jr., Matusik RJ. NF-kappaB gene signature predicts prostate cancer progression. Cancer Res. 2014; 74:2763-2772.
36. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J. 2003; 374:1-20.
37. Drake JM, Graham NA, Lee JK, Stoyanova T, Faltermeier CM, Sud S, Titz B, Huang J, Pienta KJ, Graeber TG, Witte ON. Metastatic castration-resistant prostate cancer reveals intrapatient similarity and interpatient heterogeneity of therapeutic kinase targets. Proc Natl Acad Sci U S A. 2013; 110:E4762-4769.
38. Schroeder A, Herrmann A, Cherryholmes G, Kowolik C, Buettner R, Pal S, Yu H, Muller-Newen G, Jove R. Loss of androgen receptor expression promotes a stem-like cell phenotype in prostate cancer through STAT3 signaling. Cancer Res. 2013; 74:1227-1237.
39. Smith DA, Kiba A, Zong Y, Witte ON. Interleukin-6 and oncostatin-M synergize with the PI3K/AKT pathway to promote aggressive prostate malignancy in mouse and human tissues. Mol Cancer Res. 2013; 11:1159-1165.
40. Bae KM, Su Z, Frye C, McClellan S, Allan RW, Andrejewski JT, Kelley V, Jorgensen M, Steindler DA, Vieweg J, Siemann DW. Expression of pluripotent stem cell reprogramming factors by prostate tumor initiating cells. The Journal of urology. 2010; 183:2045-2053.
41. Chen CL, Tsukamoto H, Liu JC, Kashiwabara C, Feldman D, Sher L, Dooley S, French SW, Mishra L, Petrovic L, Jeong JH, Machida K. Reciprocal regulation by TLR4 and TGF-beta in tumor-initiating stem-like cells. J Clin Invest. 2013; 123:2832-2849.
42. Kortylewski M, Swiderski P, Herrmann A, Wang L, Kowolik C, Kujawski M, Lee H, Scuto A, Liu Y, Yang C, Deng J, Soifer HS, Raubitschek A, Forman S, Rossi JJ, Pardoll DM, et al. In vivo delivery of siRNA to immune cells by conjugation to a TLR9 agonist enhances antitumor immune responses. Nat Biotechnol. 2009; 27:925-932.
43. Rane JK, Pellacani D, Maitland NJ. Advanced prostate cancer-a case for adjuvant differentiation therapy. Nat Rev Urol. 2012; 9:595-602.