Elevated expression of the colony-stimulating factor 1 (CSF1) induces prostatic intraepithelial neoplasia dependent of epithelial-Gp130.
Journal
Oncogene
ISSN: 1476-5594
Titre abrégé: Oncogene
Pays: England
ID NLM: 8711562
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
03
09
2021
accepted:
22
12
2021
revised:
06
12
2021
pubmed:
10
1
2022
medline:
11
3
2022
entrez:
9
1
2022
Statut:
ppublish
Résumé
Macrophages are increased in human benign prostatic hyperplasia and prostate cancer. We generate a Pb-Csf1 mouse model with prostate-specific overexpression of macrophage colony-stimulating factor (M-Csf/Csf1). Csf1 overexpression promotes immune cell infiltration into the prostate, modulates the macrophage polarity in a lobe-specific manner, and induces senescence and low-grade prostatic intraepithelial neoplasia (PIN). The Pb-Csf1 prostate luminal cells exhibit increased stem cell features and undergo an epithelial-to-mesenchymal transition. Human prostate cancer patients with high CSF-1 expression display similar transcriptional alterations with the Pb-Csf1 model. P53 knockout alleviates senescence but fails to progress PIN lesions. Ablating epithelial Gp130 but not Il1r1 substantially blocks PIN lesion formation. The androgen receptor (AR) is downregulated in Pb-Csf1 mice. ChIP-Seq analysis reveals altered AR binding in 2482 genes although there is no significant widespread change in global AR transcriptional activity. Collectively, our study demonstrates that increased macrophage infiltration causes PIN formation but fails to transform prostate cells.
Identifiants
pubmed: 34999736
doi: 10.1038/s41388-021-02169-7
pii: 10.1038/s41388-021-02169-7
pmc: PMC8882147
mid: NIHMS1766779
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1309-1323Subventions
Organisme : Wellcome Trust
ID : 107436
Pays : United Kingdom
Organisme : NIDDK NIH HHS
ID : R01 DK107436
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA190378
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK092202
Pays : United States
Organisme : NCI NIH HHS
ID : R21 CA196570
Pays : United States
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
De Marzo AM, Platz EA, Sutcliffe S, Xu J, Gronberg H, Drake CG, et al. Inflammation in prostate carcinogenesis. Nat Rev Cancer. 2007;7:256–69.
pubmed: 17384581
pmcid: 3552388
doi: 10.1038/nrc2090
Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454:436–44.
pubmed: 18650914
doi: 10.1038/nature07205
Kazma R, Mefford JA, Cheng I, Plummer SJ, Levin AM, Rybicki BA, et al. Association of the innate immunity and inflammation pathway with advanced prostate cancer risk. PLoS One. 2012;7:e51680.
pubmed: 23272139
pmcid: 3522730
doi: 10.1371/journal.pone.0051680
Platz EA, Kulac I, Barber JR, Drake CG, Joshu CE, Nelson WG, et al. A prospective study of chronic inflammation in benign prostate tissue and risk of prostate cancer: linked PCPT and SELECT cohorts. Cancer Epidemiol, Biomark Prev: a Publ Am Assoc Cancer Res, cosponsored Am Soc Preventive Oncol. 2017;26:1549–57.
doi: 10.1158/1055-9965.EPI-17-0503
Gurel B, Lucia MS, Thompson IM Jr., Goodman PJ, Tangen CM, Kristal AR, et al. Chronic inflammation in benign prostate tissue is associated with high-grade prostate cancer in the placebo arm of the prostate cancer prevention trial. Cancer Epidemiol, Biomark Prev: a Publ Am Assoc Cancer Res, cosponsored Am Soc Preventive Oncol. 2014;23:847–56.
doi: 10.1158/1055-9965.EPI-13-1126
Dennis LK, Lynch CF, Torner JC. Epidemiologic association between prostatitis and prostate cancer. Urology. 2002;60:78–83.
pubmed: 12100928
doi: 10.1016/S0090-4295(02)01637-0
De Marzo AM, Marchi VL, Epstein JI, Nelson WG. Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol. 1999;155:1985–92.
pubmed: 10595928
pmcid: 1866955
doi: 10.1016/S0002-9440(10)65517-4
Endo Y, Marusawa H, Kinoshita K, Morisawa T, Sakurai T, Okazaki IM, et al. Expression of activation-induced cytidine deaminase in human hepatocytes via NF-kappaB signaling. Oncogene. 2007;26:5587–95.
pubmed: 17404578
doi: 10.1038/sj.onc.1210344
Hmadcha A, Bedoya FJ, Sobrino F, Pintado E. Methylation-dependent gene silencing induced by interleukin 1beta via nitric oxide production. J Exp Med. 1999;190:1595–604.
pubmed: 10587350
pmcid: 2195731
doi: 10.1084/jem.190.11.1595
Debelec-Butuner B, Alapinar C, Varisli L, Erbaykent-Tepedelen B, Hamid SM, Gonen-Korkmaz C, et al. Inflammation-mediated abrogation of androgen signaling: an in vitro model of prostate cell inflammation. Mol carcinogenesis. 2014;53:85–97.
doi: 10.1002/mc.21948
Zhu P, Baek SH, Bourk EM, Ohgi KA, Garcia-Bassets I, Sanjo H. et al. Macrophage/cancer cell interactions mediate hormone resistance by a nuclear receptor derepression pathway. Cell . 2006;124:615–29.
pubmed: 16469706
doi: 10.1016/j.cell.2005.12.032
Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140:883–99.
pubmed: 20303878
pmcid: 2866629
doi: 10.1016/j.cell.2010.01.025
Kwon OJ, Zhang B, Zhang L, Xin L. High fat diet promotes prostatic basal-to-luminal differentiation and accelerates initiation of prostate epithelial hyperplasia originated from basal cells. Stem cell Res. 2016;16:682–91.
pubmed: 27107344
doi: 10.1016/j.scr.2016.04.009
Kwon OJ, Zhang L, Ittmann MM, Xin L. Prostatic inflammation enhances basal-to-luminal differentiation and accelerates initiation of prostate cancer with a basal cell origin. Proc Natl Acad Sci USA. 2014;111:E592–600.
pubmed: 24367088
doi: 10.1073/pnas.1318157111
Jin RJ, Lho Y, Connelly L, Wang Y, Yu X, Saint Jean L, et al. The nuclear factor-kappaB pathway controls the progression of prostate cancer to androgen-independent growth. Cancer Res. 2008;68:6762–9.
pubmed: 18701501
pmcid: 2840631
doi: 10.1158/0008-5472.CAN-08-0107
Luo JL, Tan W, Ricono JM, Korchynskyi O, Zhang M, Gonias SL, et al. Nuclear cytokine-activated IKKalpha controls prostate cancer metastasis by repressing Maspin. Nature. 2007;446:690–4.
pubmed: 17377533
doi: 10.1038/nature05656
Birbach A, Eisenbarth D, Kozakowski N, Ladenhauf E, Schmidt-Supprian M, Schmid JA. Persistent inflammation leads to proliferative neoplasia and loss of smooth muscle cells in a prostate tumor model. Neoplasia. 2011;13:692–703.
pubmed: 21847361
pmcid: 3156660
doi: 10.1593/neo.11524
Elkahwaji JE, Zhong W, Hopkins WJ, Bushman W. Chronic bacterial infection and inflammation incite reactive hyperplasia in a mouse model of chronic prostatitis. Prostate. 2007;67:14–21.
pubmed: 17075821
doi: 10.1002/pros.20445
Fong L, Ruegg CL, Brockstedt D, Engleman EG, Laus R. Induction of tissue-specific autoimmune prostatitis with prostatic acid phosphatase immunization: implications for immunotherapy of prostate cancer. J Immunol. 1997;159:3113–7.
pubmed: 9317107
Haverkamp JM, Charbonneau B, Crist SA, Meyerholz DK, Cohen MB, Snyder PW, et al. An inducible model of abacterial prostatitis induces antigen specific inflammatory and proliferative changes in the murine prostate. Prostate. 2011;71:1139–50.
pubmed: 21656824
pmcid: 3136647
doi: 10.1002/pros.21327
Khalili M, Mutton LN, Gurel B, Hicks JL, De Marzo AM, Bieberich CJ. Loss of Nkx3.1 expression in bacterial prostatitis: a potential link between inflammation and neoplasia. Am J Pathol. 2010;176:2259–68.
pubmed: 20363913
pmcid: 2861091
doi: 10.2353/ajpath.2010.080747
Barron DA, Strand DW, Ressler SJ, Dang TD, Hayward SW, Yang F, et al. TGF-beta1 induces an age-dependent inflammation of nerve ganglia and fibroplasia in the prostate gland stroma of a novel transgenic mouse. PLoS One. 2010;5:e13751.
pubmed: 21060787
pmcid: 2966419
doi: 10.1371/journal.pone.0013751
Liu G, Zhang J, Frey L, Gang X, Wu K, Liu Q, et al. Prostate-specific IL-6 transgene autonomously induce prostate neoplasm through amplifying inflammation in the prostate and peri-prostatic adipose tissue. J Hematol Oncol. 2017;10:14.
pubmed: 28077171
pmcid: 5225646
doi: 10.1186/s13045-016-0386-7
Wang X, Lin WJ, Izumi K, Jiang Q, Lai KP, Xu D, et al. Increased infiltrated macrophages in benign prostatic hyperplasia (BPH): role of stromal androgen receptor in macrophage-induced prostate stromal cell proliferation. J Biol Chem. 2012;287:18376–85.
pubmed: 22474290
pmcid: 3365773
doi: 10.1074/jbc.M112.355164
Lissbrant IF, Stattin P, Wikstrom P, Damber JE, Egevad L, Bergh A. Tumor associated macrophages in human prostate cancer: relation to clinicopathological variables and survival. Int J Oncol. 2000;17:445–51.
pubmed: 10938382
Zhang B, Kwon OJ, Henry G, Malewska A, Wei X, Zhang L, et al. Non-cell-autonomous regulation of prostate epithelial homeostasis by androgen receptor. Mol cell. 2016;63:976–89.
pubmed: 27594448
pmcid: 5026614
doi: 10.1016/j.molcel.2016.07.025
Stanley ER, Chitu V. CSF-1 receptor signaling in myeloid cells. Cold Spring Harbor perspectives in biology. 2014;6:1–21.
doi: 10.1101/cshperspect.a021857
Kirma N, Luthra R, Jones J, Liu YG, Nair HB, Mandava U, et al. Overexpression of the colony-stimulating factor (CSF-1) and/or its receptor c-fms in mammary glands of transgenic mice results in hyperplasia and tumor formation. Cancer Res. 2004;64:4162–70.
pubmed: 15205327
doi: 10.1158/0008-5472.CAN-03-2971
Malinen M, Niskanen EA, Kaikkonen MU, Palvimo JJ. Crosstalk between androgen and pro-inflammatory signaling remodels androgen receptor and NF-kappaB cistrome to reprogram the prostate cancer cell transcriptome. Nucleic acids Res. 2017;45:619–30.
pubmed: 27672034
doi: 10.1093/nar/gkw855
Park JH, Walls JE, Galvez JJ, Kim M, Abate-Shen C, Shen MM, et al. Prostatic intraepithelial neoplasia in genetically engineered mice. Am J Pathol. 2002;161:727–35.
pubmed: 12163397
pmcid: 1850748
doi: 10.1016/S0002-9440(10)64228-9
The Cancer Genome Atlas Research Network. The molecular taxonomy of primary prostate cancer. Cell. 2015;163:1011–25.
Simons BW, Durham NM, Bruno TC, Grosso JF, Schaeffer AJ, Ross AE, et al. A human prostatic bacterial isolate alters the prostatic microenvironment and accelerates prostate cancer progression. J Pathol. 2015;235:478–89.
pubmed: 25348195
pmcid: 4352321
doi: 10.1002/path.4472
Shinohara DB, Vaghasia AM, Yu SH, Mak TN, Bruggemann H, Nelson WG, et al. A mouse model of chronic prostatic inflammation using a human prostate cancer-derived isolate of Propionibacterium acnes. Prostate. 2013;73:1007–15.
pubmed: 23389852
pmcid: 3991131
doi: 10.1002/pros.22648
Vignozzi L, Cellai I, Santi R, Lombardelli L, Morelli A, Comeglio P, et al. Antiinflammatory effect of androgen receptor activation in human benign prostatic hyperplasia cells. J Endocrinol. 2012;214:31–43.
pubmed: 22562653
doi: 10.1530/JOE-12-0142
Cioni B, Zaalberg A, van Beijnum JR, Melis MHM, van Burgsteden J, Muraro MJ, et al. Androgen receptor signalling in macrophages promotes TREM-1-mediated prostate cancer cell line migration and invasion. Nat Commun. 2020;11:4498.
pubmed: 32908142
pmcid: 7481219
doi: 10.1038/s41467-020-18313-y
Ormandy CJ, Clarke CL, Kelly PA, Sutherland RL. Androgen regulation of prolactin-receptor gene expression in MCF-7 and MDA-MB-453 human breast cancer cells. Int J cancer J Int du cancer. 1992;50:777–82.
doi: 10.1002/ijc.2910500519
Graham TR, Yacoub R, Taliaferro-Smith L, Osunkoya AO, Odero-Marah VA, Liu T, et al. Reciprocal regulation of ZEB1 and AR in triple negative breast cancer cells. Breast cancer Res Treat. 2010;123:139–47.
pubmed: 19921427
doi: 10.1007/s10549-009-0623-7
Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell. 2009;15:103–13.
pubmed: 19185845
pmcid: 2667107
doi: 10.1016/j.ccr.2009.01.001
Bollrath J, Phesse TJ, von Burstin VA, Putoczki T, Bennecke M, Bateman T, et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell. 2009;15:91–102.
pubmed: 19185844
doi: 10.1016/j.ccr.2009.01.002
Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science. 2007;317:121–4.
pubmed: 17615358
doi: 10.1126/science.1140485
Chan KS, Sano S, Kiguchi K, Anders J, Komazawa N, Takeda J, et al. Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis. J Clin Investig. 2004;114:720–8.
pubmed: 15343391
pmcid: 514583
doi: 10.1172/JCI200421032
Strobel O, Dor Y, Alsina J, Stirman A, Lauwers G, Trainor A, et al. In vivo lineage tracing defines the role of acinar-to-ductal transdifferentiation in inflammatory ductal metaplasia. Gastroenterology. 2007;133:1999–2009.
pubmed: 18054571
doi: 10.1053/j.gastro.2007.09.009
Husaini Y, Qiu MR, Lockwood GP, Luo XW, Shang P, Kuffner T, et al. Macrophage inhibitory cytokine-1 (MIC-1/GDF15) slows cancer development but increases metastases in TRAMP prostate cancer prone mice. PLoS One. 2012;7:e43833. Epub 2012/09/07
pubmed: 22952779
pmcid: 3428289
doi: 10.1371/journal.pone.0043833
Spranger S, Bao R, Gajewski TF. Melanoma-intrinsic beta-catenin signalling prevents anti-tumour immunity. Nature. 2015;523:231–5.
pubmed: 25970248
doi: 10.1038/nature14404
Kortlever RM, Sodir NM, Wilson CH, Burkhart DL, Pellegrinet L, Brown Swigart L, et al. Myc Cooperates with Ras by Programming Inflammation and Immune Suppression. Cell. 2017;171:1301–15.
pubmed: 29195074
pmcid: 5720393
doi: 10.1016/j.cell.2017.11.013
Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med. 2001;193:727–40.
pubmed: 11257139
pmcid: 2193412
doi: 10.1084/jem.193.6.727
Ide H, Seligson DB, Memarzadeh S, Xin L, Horvath S, Dubey P, et al. Expression of colony-stimulating factor 1 receptor during prostate development and prostate cancer progression. Proc Natl Acad Sci USA. 2002;99:14404–9.
pubmed: 12381783
pmcid: 137896
doi: 10.1073/pnas.222537099
Kumar V, Donthireddy L, Marvel D, Condamine T, Wang F, Lavilla-Alonso S, et al. Cancer-associated fibroblasts neutralize the anti-tumor effect of CSF1 receptor blockade by inducing PMN-MDSC infiltration of tumors. Cancer Cell. 2017;32:654–68.
pubmed: 29136508
pmcid: 5827952
doi: 10.1016/j.ccell.2017.10.005
Vignozzi L, Morelli A, Sarchielli E, Comeglio P, Filippi S, Cellai I, et al. Testosterone protects from metabolic syndrome-associated prostate inflammation: an experimental study in rabbit. J Endocrinol. 2012;212:71–84.
pubmed: 22010203
doi: 10.1530/JOE-11-0289
Maggio M, Basaria S, Ceda GP, Ble A, Ling SM, Bandinelli S, et al. The relationship between testosterone and molecular markers of inflammation in older men. J endocrinological Investig. 2005;28:116–9.
Maggio M, Blackford A, Taub D, Carducci M, Ble A, Metter EJ, et al. Circulating inflammatory cytokine expression in men with prostate cancer undergoing androgen deprivation therapy. J Androl. 2006;27:725–8.
pubmed: 16775253
doi: 10.2164/jandrol.106.000141
Sorrentino C, Musiani P, Pompa P, Cipollone G, Di Carlo E. Androgen deprivation boosts prostatic infiltration of cytotoxic and regulatory T lymphocytes and has no effect on disease-free survival in prostate cancer patients. Clin Cancer Res. 2011;17:1571–81.
pubmed: 21159885
doi: 10.1158/1078-0432.CCR-10-2804
Traish A, Bolanos J, Nair S, Saad F, Morgentaler A. Do androgens modulate the pathophysiological pathways of inflammation? appraising the contemporary evidence. J Clin Med. 2018;7:549.
Becerra-Diaz M, Strickland AB, Keselman A, Heller NM. Androgen and androgen receptor as enhancers of M2 macrophage polarization in allergic lung inflammation. J Immunol. 2018;201:2923–33.
pubmed: 30305328
doi: 10.4049/jimmunol.1800352
Chen T, Wang LH, Farrar WL. Interleukin 6 activates androgen receptor-mediated gene expression through a signal transducer and activator of transcription 3-dependent pathway in LNCaP prostate cancer cells. Cancer Res. 2000;60:2132–5.
pubmed: 10786674
Zhang L, Altuwaijri S, Deng F, Chen L, Lal P, Bhanot UK, et al. NF-kappaB regulates androgen receptor expression and prostate cancer growth. Am J Pathol. 2009;175:489–99.
pubmed: 19628766
pmcid: 2716950
doi: 10.2353/ajpath.2009.080727
Wang Z, Hu L, Salari K, Bechis SK, Ge R, Wu S, et al. Androgenic to oestrogenic switch in the human adult prostate gland is regulated by epigenetic silencing of steroid 5alpha-reductase 2. J Pathol. 2017;243:457–67.
pubmed: 28940538
pmcid: 6212292
doi: 10.1002/path.4985
Leach DA, Panagopoulos V, Nash C, Bevan C, Thomson AA, Selth LA, et al. Cell-lineage specificity and role of AP-1 in the prostate fibroblast androgen receptor cistrome. Mol Cell Endocrinol. 2017;439:261–72.
pubmed: 27634452
doi: 10.1016/j.mce.2016.09.010
Valdez JM, Zhang L, Su Q, Dakhova O, Zhang Y, Shahi P, et al. Notch and TGFbeta form a reciprocal positive regulatory loop that suppresses murine prostate basal stem/progenitor cell activity. cell stem cell. 2012;11:676–88.
pubmed: 23122291
pmcid: 3490134
doi: 10.1016/j.stem.2012.07.003
Hewitt SC, Li L, Grimm SA, Chen Y, Liu L, Li Y, et al. Research resource: whole-genome estrogen receptor alpha binding in mouse uterine tissue revealed by ChIP-seq. Mol Endocrinol. 2012;26:887–98.
pubmed: 22446102
pmcid: 3355558
doi: 10.1210/me.2011-1311