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Prostate cancer

CXCR4 and CXCR7 signaling promotes tumor progression and obesity-associated epithelial-mesenchymal transition in prostate cancer cells

  • Bhurosy T, Jeewon R. Overweight and obesity epidemic in developing countries: a problem with diet, physical activity, or socioeconomic status? Scientific World Journal. 2014;2014:964236.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fryar CD, Carroll MD, Ogden CL. Prevalence of overweight, obesity, and severe obesity among adults aged 20 and over: United States, 1960–1962 through 2015–2016. NCHS Health E-Stats. 2018.

  • Hales CM, Carroll MD, Fryar CD, Ogden CL. Prevalence of obesity among adults and youth: United States, 2015–2016. NCHS Data Brief. 2017;1–8.

  • Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 2003;348:1625–38.

    PubMed 

    Google Scholar
     

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7–30.

    PubMed 

    Google Scholar
     

  • Wright ME, Chang SC, Schatzkin A, Albanes D, Kipnis V, Mouw T, et al. Prospective study of adiposity and weight change in relation to prostate cancer incidence and mortality. Cancer 2007;109:675–84.

    PubMed 

    Google Scholar
     

  • Gong Z, Agalliu I, Lin DW, Stanford JL, Kristal AR. Obesity is associated with increased risks of prostate cancer metastasis and death after initial cancer diagnosis in middle-aged men. Cancer 2007;109:1192–202.

    PubMed 

    Google Scholar
     

  • Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, et al. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 1998;279:563–6.

    CAS 
    PubMed 

    Google Scholar
     

  • Saglam K, Aydur E, Yilmaz M, Goktas S. Leptin influences cellular differentiation and progression in prostate cancer. J Urol. 2003;169:1308–11.

    CAS 
    PubMed 

    Google Scholar
     

  • Silva KR, Cortes I, Liechocki S, Carneiro JR, Souza AA, Borojevic R, et al. Characterization of stromal vascular fraction and adipose stem cells from subcutaneous, preperitoneal and visceral morbidly obese human adipose tissue depots. PLoS ONE. 2017;12:e0174115.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Laurent V, Guerard A, Mazerolles C, Le Gonidec S, Toulet A, Nieto L, et al. Periprostatic adipocytes act as a driving force for prostate cancer progression in obesity. Nat Commun. 2016;7:10230.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kolonin MG, DiGiovanni J. The role of adipose stroma in prostate cancer aggressiveness. Transl Androl Urol. 2019;8:S348–S350.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Su F, Ahn S, Saha A, DiGiovanni J, Kolonin MG. Adipose stromal cell targeting suppresses prostate cancer epithelial-mesenchymal transition and chemoresistance. Oncogene 2019;38:1979–88.

    CAS 
    PubMed 

    Google Scholar
     

  • Daquinag AC, Zhang Y, Amaya-Manzanares F, Simmons PJ, Kolonin MG. An isoform of decorin is a resistin receptor on the surface of adipose progenitor cells. Cell Stem Cell. 2011;9:74–86.

    CAS 
    PubMed 

    Google Scholar
     

  • Daquinag AC, Tseng C, Salameh A, Zhang Y, Amaya-Manzanares F, Dadbin A, et al. Depletion of white adipocyte progenitors induces beige adipocyte differentiation and suppresses obesity development. Cell Death Differ. 2015;22:351–63.

    CAS 
    PubMed 

    Google Scholar
     

  • Zhang Y, Daquinag A, Traktuev DO, Amaya-Manzanares F, Simmons PJ, March KL, et al. White adipose tissue cells are recruited by experimental tumors and promote cancer progression in mouse models. Cancer Res. 2009;69:5259–66.

    CAS 
    PubMed 

    Google Scholar
     

  • Blando J, Moore T, Hursting S, Jiang G, Saha A, Beltran L, et al. Dietary energy balance modulates prostate cancer progression in Hi-Myc mice. Cancer Prev Res. 2011;4:2002–14.

    CAS 

    Google Scholar
     

  • Saha A, Ahn S, Blando J, Su F, Kolonin MG, DiGiovanni J. Proinflammatory CXCL12-CXCR4/CXCR7 signaling axis drives Myc-induced prostate cancer in obese mice. Cancer Res. 2017;77:5158–68.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shi Y, Riese DJ 2nd, Shen J. The role of the CXCL12/CXCR4/CXCR7 chemokine axis in cancer. Front Pharmacol. 2020;11:574667.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Luker KE, Luker GD. Functions of CXCL12 and CXCR4 in breast cancer. Cancer Lett. 2006;238:30–41.

    CAS 
    PubMed 

    Google Scholar
     

  • Phillips RJ, Burdick MD, Lutz M, Belperio JA, Keane MP, Strieter RM. The stromal derived factor-1/CXCL12-CXC chemokine receptor 4 biological axis in non-small cell lung cancer metastases. Am J Respir Crit Care Med. 2003;167:1676–86.

    PubMed 

    Google Scholar
     

  • Singh S, Singh UP, Grizzle WE, Lillard JW Jr. CXCL12-CXCR4 interactions modulate prostate cancer cell migration, metalloproteinase expression and invasion. Lab Investig. 2004;84:1666–76.

    CAS 
    PubMed 

    Google Scholar
     

  • Yasumoto K, Koizumi K, Kawashima A, Saitoh Y, Arita Y, Shinohara K, et al. Role of the CXCL12/CXCR4 axis in peritoneal carcinomatosis of gastric cancer. Cancer Res. 2006;66:2181–7.

    CAS 
    PubMed 

    Google Scholar
     

  • Kim D, Kim J, Yoon JH, Ghim J, Yea K, Song P, et al. CXCL12 secreted from adipose tissue recruits macrophages and induces insulin resistance in mice. Diabetologia 2014;57:1456–65.

    CAS 
    PubMed 

    Google Scholar
     

  • Shirozu M, Nakano T, Inazawa J, Tashiro K, Tada H, Shinohara T, et al. Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene. Genomics 1995;28:495–500.

    CAS 
    PubMed 

    Google Scholar
     

  • Su F, Daquinag AC, Ahn S, Saha A, Dai Y, Zhao Z, et al. Progression of prostate carcinoma is promoted by adipose stromal cell-secreted CXCL12 signaling in prostate epithelium. NPJ Precis Oncol. 2021;5:26.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao H, Guo L, Zhao H, Zhao J, Weng H, Zhao B. CXCR4 over-expression and survival in cancer: a system review and meta-analysis. Oncotarget 2015;6:5022–40.

    PubMed 

    Google Scholar
     

  • Darash-Yahana M, Pikarsky E, Abramovitch R, Zeira E, Pal B, Karplus R, et al. Role of high expression levels of CXCR4 in tumor growth, vascularization, and metastasis. FASEB J. 2004;18:1240–2.

    CAS 
    PubMed 

    Google Scholar
     

  • Cui K, Zhao W, Wang C, Wang A, Zhang B, Zhou W, et al. The CXCR4-CXCL12 pathway facilitates the progression of pancreatic cancer via induction of angiogenesis and lymphangiogenesis. J Surg Res. 2011;171:143–50.

    CAS 
    PubMed 

    Google Scholar
     

  • Teicher BA, Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res. 2010;16:2927–31.

    CAS 
    PubMed 

    Google Scholar
     

  • Scala S. Molecular pathways: targeting the CXCR4-CXCL12 axis–untapped potential in the tumor microenvironment. Clin Cancer Res. 2015;21:4278–85.

    CAS 
    PubMed 

    Google Scholar
     

  • Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med. 1996;184:1101–9.

    CAS 
    PubMed 

    Google Scholar
     

  • Sun X, Cheng G, Hao M, Zheng J, Zhou X, Zhang J, et al. CXCL12/CXCR4/CXCR7 chemokine axis and cancer progression. Cancer Metastasis Rev. 2010;29:709–22.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hernandez L, Magalhaes MA, Coniglio SJ, Condeelis JS, Segall JE. Opposing roles of CXCR4 and CXCR7 in breast cancer metastasis. Breast Cancer Res. 2011;13:R128.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Saha A, Blando J, Fernandez I, Kiguchi K, DiGiovanni J. Linneg Sca-1high CD49fhigh prostate cancer cells derived from the Hi-Myc mouse model are tumor-initiating cells with basal-epithelial characteristics and differentiation potential in vitro and in vivo. Oncotarget 2016;7:25194–207.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dubrovska A, Elliott J, Salamone RJ, Telegeev GD, Stakhovsky AE, Schepotin IB, et al. CXCR4 expression in prostate cancer progenitor cells. PLoS ONE. 2012;7:e31226.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Trautmann F, Cojoc M, Kurth I, Melin N, Bouchez LC, Dubrovska A, et al. CXCR4 as biomarker for radioresistant cancer stem cells. Int J Radiat Biol. 2014;90:687–99.

    CAS 
    PubMed 

    Google Scholar
     

  • Miki J, Furusato B, Li H, Gu Y, Takahashi H, Egawa S, et al. Identification of putative stem cell markers, CD133 and CXCR4, in hTERT-immortalized primary nonmalignant and malignant tumor-derived human prostate epithelial cell lines and in prostate cancer specimens. Cancer Res. 2007;67:3153–61.

    CAS 
    PubMed 

    Google Scholar
     

  • Ellerby HM, Arap W, Ellerby LM, Kain R, Andrusiak R, Rio GD, et al. Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med. 1999;5:1032–8.

    CAS 
    PubMed 

    Google Scholar
     

  • Zabel BA, Wang Y, Lewen S, Berahovich RD, Penfold ME, Zhang P, et al. Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol. 2009;183:3204–11.

    CAS 
    PubMed 

    Google Scholar
     

  • Singh AK, Arya RK, Trivedi AK, Sanyal S, Baral R, Dormond O, et al. Chemokine receptor trio: CXCR3, CXCR4 and CXCR7 crosstalk via CXCL11 and CXCL12. Cytokine Growth Factor Rev. 2013;24:41–49.

    CAS 
    PubMed 

    Google Scholar
     

  • Dickerman BA, Torfadottir JE, Valdimarsdottir UA, Giovannucci E, Wilson KM, Aspelund T, et al. Body fat distribution on computed tomography imaging and prostate cancer risk and mortality in the AGES-Reykjavik study. Cancer 2019;125:2877–85.

    PubMed 

    Google Scholar
     

  • Sun K, Kusminski CM, Scherer PE. Adipose tissue remodeling and obesity. J Clin Investig. 2011;121:2094–101.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Himbert C, Delphan M, Scherer D, Bowers LW, Hursting S, Ulrich CM. Signals from the adipose microenvironment and the obesity-cancer link-a systematic review. Cancer Prev Res. 2017;10:494–506.

    CAS 

    Google Scholar
     

  • Bellows CF, Zhang Y, Chen J, Frazier ML, Kolonin MG. Circulation of progenitor cells in obese and lean colorectal cancer patients. Cancer Epidemiol Biomark Prev. 2011;20:2461–8.

    CAS 

    Google Scholar
     

  • Su F, Wang X, Pearson T, Lee J, Krishnamurthy S, Ueno NT, et al. Ablation of stromal cells with a targeted proapoptotic peptide suppresses cancer chemotherapy resistance and metastasis. Mol Ther Oncolytics. 2020;18:579–86.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lengyel E, Makowski L, DiGiovanni J, Kolonin MG. Cancer as a matter of fat: the crosstalk between adipose tissue and tumors. Trends Cancer. 2018;4:374–84.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yang J, Tang H, Huang J, An H. Upregulation of CXCR7 is associated with poor prognosis of prostate cancer. Med Sci Monit. 2018;24:5185–91.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang J, Shiozawa Y, Wang J, Wang Y, Jung Y, Pienta KJ, et al. The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem. 2008;283:4283–94.

    CAS 
    PubMed 

    Google Scholar
     

  • Mochizuki H, Matsubara A, Teishima J, Mutaguchi K, Yasumoto H, Dahiya R, et al. Interaction of ligand-receptor system between stromal-cell-derived factor-1 and CXC chemokine receptor 4 in human prostate cancer: a possible predictor of metastasis. Biochem Biophys Res Commun. 2004;320:656–63.

    CAS 
    PubMed 

    Google Scholar
     

  • De Clercq E. Mozobil(R) (Plerixafor, AMD3100), 10 years after its approval by the US Food and Drug Administration. Antivir Chem Chemother. 2019;27:2040206619829382.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lawrence M, Daujat S, Schneider R. Lateral thinking: how histone modifications regulate gene expression. Trends Genet. 2016;32:42–56.

    CAS 
    PubMed 

    Google Scholar
     

  • Stillman B. Histone modifications: insights into their influence on gene expression. Cell 2018;175:6–9.

    CAS 
    PubMed 

    Google Scholar
     

  • Couture JF, Collazo E, Ortiz-Tello PA, Brunzelle JS, Trievel RC. Specificity and mechanism of JMJD2A, a trimethyllysine-specific histone demethylase. Nat Struct Mol Biol. 2007;14:689–95.

    CAS 
    PubMed 

    Google Scholar
     

  • Kim TD, Jin F, Shin S, Oh S, Lightfoot SA, Grande JP, et al. Histone demethylase JMJD2A drives prostate tumorigenesis through transcription factor ETV1. J Clin Investig. 2016;126:706–20.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Song ZY, Wang F, Cui SX, Gao ZH, Qu XJ. CXCR7/CXCR4 heterodimer-induced histone demethylation: a new mechanism of colorectal tumorigenesis. Oncogene 2019;38:1560–75.

    CAS 
    PubMed 

    Google Scholar
     

  • Wang F, Li Y, Shan F, Zhang Q, Wang L, Sheng B, et al. Upregulation of JMJD2A promotes migration and invasion in bladder cancer through regulation of SLUG. Oncol Rep. 2019;42:1431–40.

    CAS 
    PubMed 

    Google Scholar
     

  • Li M, Cheng J, Ma Y, Guo H, Shu H, Huang H, et al. The histone demethylase JMJD2A promotes glioma cell growth via targeting Akt-mTOR signaling. Cancer Cell Int. 2020;20:101.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li Y, Wang Y, Xie Z, Hu H. JMJD2A facilitates growth and inhibits apoptosis of cervical cancer cells by downregulating tumor suppressor miR4915p. Mol Med Rep. 2019;19:2489–96.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yang N, Chen T, Wang L, Liu R, Niu Y, Sun L, et al. CXCR4 mediates matrix stiffness-induced downregulation of UBTD1 driving hepatocellular carcinoma progression via YAP signaling pathway. Theranostics 2020;10:5790–801.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang X, Cao Y, Zhang S, Chen Z, Fan L, Shen X, et al. Stem cell autocrine CXCL12/CXCR4 stimulates invasion and metastasis of esophageal cancer. Oncotarget 2017;8:36149–60.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tian Y, Song Y, Bai W, Ma X, Ren Z. CXCR4 knockdown inhibits the growth and invasion of nasopharyngeal cancer stem cells. Oncol Lett. 2017;13:2253–9.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ablett MP, O’Brien CS, Sims AH, Farnie G, Clarke RB. A differential role for CXCR4 in the regulation of normal versus malignant breast stem cell activity. Oncotarget 2014;5:599–612.

    PubMed 

    Google Scholar
     

  • Balic A, Sorensen MD, Trabulo SM, Sainz B Jr., Cioffi M, Vieira CR, et al. Chloroquine targets pancreatic cancer stem cells via inhibition of CXCR4 and hedgehog signaling. Mol Cancer Ther. 2014;13:1758–71.

    CAS 
    PubMed 

    Google Scholar
     

  • Mimeault M, Batra SK. Frequent gene products and molecular pathways altered in prostate cancer- and metastasis-initiating cells and their progenies and novel promising multitargeted therapies. Mol Med. 2011;17:949–64.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Moore T, Beltran L, Carbajal S, Strom S, Traag J, Hursting SD, et al. Dietary energy balance modulates signaling through the Akt/mammalian target of rapamycin pathways in multiple epithelial tissues. Cancer Prev Res. 2008;1:65–76.

    CAS 

    Google Scholar
     

  • Nunez NP, Perkins SN, Smith NC, Berrigan D, Berendes DM, Varticovski L, et al. Obesity accelerates mouse mammary tumor growth in the absence of ovarian hormones. Nutr Cancer. 2008;60:534–41.

    CAS 
    PubMed 

    Google Scholar
     

  • Nunez NP, Carpenter CL, Perkins SN, Berrigan D, Jaque SV, Ingles SA, et al. Extreme obesity reduces bone mineral density: complementary evidence from mice and women. Obesity 2007;15:1980–7.

    CAS 
    PubMed 

    Google Scholar
     

  • Daquinag AC, Dadbin A, Snyder B, Wang X, Sahin AA, Ueno NT, et al. Non-glycanated decorin is a drug target on human adipose stromal cells. Mol Ther Oncolytics. 2017;6:1–9.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, et al. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Res. 2004;64:2270–305.

    CAS 
    PubMed 

    Google Scholar
     

  • Zhao W, Sachsenmeier K, Zhang L, Sult E, Hollingsworth RE, Yang H. A new bliss independence model to analyze drug combination data. J Biomol Screen. 2014;19:817–21.

    PubMed 

    Google Scholar
     

  • Kshattry S, Saha A, Gries P, Tiziani S, Stone E, Georgiou G, et al. Enzyme-mediated depletion of l-cyst(e)ine synergizes with thioredoxin reductase inhibition for suppression of pancreatic tumor growth. NPJ Precis Oncol. 2019;3:16.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Saha A, Blando J, Tremmel L, DiGiovanni J. Effect of metformin, rapamycin and their combination on growth and progression of prostate tumors in HiMyc mice. Cancer Prev Res. 2015;8:597–606.

    CAS 

    Google Scholar