Skip to main content

Advertisement

Log in

Rs-10889677 variant in interleukin-23 receptor may contribute to creating an inflammatory milieu more susceptible to bladder tumourigenesis: report and meta-analysis

  • Review
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

Bladder cancer (BLC) is a recurrent high-risk malignancy typified by an inherent localised chronic inflammation. IL-23-receptor (IL-23R), as a positive regulator in the priming of T helper-17 cells, is regarded a principal coordinator of inflammation-propelled neoplasia. In this article, we indented firstly to scrutinise the influence of rs10889677“A/C” SNP located in IL-23R-gene on BLC development and progression among Egyptians. Findings revealed that the rs10889677“C” allele was significantly associated with the increased BLC risk and its higher frequencies were plainly noticeable in high-grade and invasive tumours when applied the dominant/homozygous/allelic genetic models. Under the same genetic models, elevated serum levels of IL-23R protein in BLC patients were pertinently correlated with the rs10889677“A/C” polymorphism. As a corollary, the frequent up-regulation of IL-23R exerts a subsequent activation of the IL-23/17 inflammatory axis. That is experienced as a drastic increase in IL-23 and IL17 levels under the dominant/homozygous/heterozygous/recessive models. Second, study further described how the rs10889677 variant confers its pro-tumoural influences on IL-23R-bearing immune cells, involving tumour-associated macrophages (TAMs), natural killers (NKs) and CD4+ T-helper cells. When the dominant model was adopted, it was observed that patients bearing the rs10889677 “C” allele had lower counts of IL-23R-positive CD56+NKs and CD4+ T-cells, in tandem with higher levels of IL-23R-positive CD14+ TAMs compared with those with rs10889677 “A” allele. To entrench the idea, we did a meta-analysis on BLC patients from three different ethnicities (Asian, Caucasians and African). We observed that rs10889677“SNP” is significantly correlated with increased risk of BLCs in the overall population using over-dominant model. Consequently, authors suggested that the rs10889677 variant could be directly implicated in developing inflammatory environment more prone to generating malignancy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Akbay EA, Koyama S, Liu Y, Dries R, Bufe LE, Silkes M, Alam MM, Magee DM, Jones R, Jinushi M, Kulkarni M, Carretero J, Wang X, Warner-Hatten T, Cavanaugh JD, Osa A, Kumanogoh A, Freeman GJ, Awad MM, Christiani DC, Bueno R, Hammerman PS, Dranoff G, Wong K-K (2017) Interleukin-17A Promotes Lung Tumor Progression through Neutrophil Attraction to Tumor Sites and Mediating Resistance to PD-1 Blockade. J Thorac Oncol 12(8):1268–1279

    Article  PubMed  PubMed Central  Google Scholar 

  • Amirghofran Z, Asiaee E, Kamazani FM (2016) Soluble CD44 and CD44v6 and prognosis in children with B-cell acute lymphoblastic leukemia. Asia Pac J Clin Oncol 12(3):e375–e382

    Article  PubMed  Google Scholar 

  • Antoni S, Ferlay J, Soerjomataram I, Znaor A, Jemal A, Bray F (2017) Bladder Cancer Incidence and Mortality: A Global Overview and Recent Trends. Eur Urol 71(1):96–108

    Article  PubMed  Google Scholar 

  • Antoniades HN, Galanopoulos T, Neville-Golden J, Kiritsy CP, Lynch SE (1991) Injury induces in vivo expression of platelet-derived growth factor (PDGF) and PDGF receptor mRNAs in skin epithelial cells and PDGF mRNA in connective tissue fibroblasts. Proc Natl Acad Sci U S A 88(2):565–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baban CK, Cronin M, O’Hanlon D, O’Sullivan GC, Tangney M (2010) Bacteria as vectors for gene therapy of cancer. Bioeng Bugs 1(6):385–394

    Article  PubMed  PubMed Central  Google Scholar 

  • Babjuk M, Böhle A, Burger M, Capoun O, Cohen D, Compérat EM, Hernández V, Kaasinen E, Palou J, Rouprêt M, van Rhijn BW, Shariat SF, Soukup V, Sylvester RJ, Zigeuner R (2017) EAU Guidelines on Non-Muscle-invasive Urothelial Carcinoma of the Bladder: Update 2016. Eur Urol 71(3):447–461

    Article  PubMed  Google Scholar 

  • Bagheri MH, Ahlman MA, Lindenberg L, Lin Turkbey B, J, Cahid Civelek A, Malayeri AA, Agarwal PK, Choyke PL, Folio LR, Apolo AB, (2017) Advances in medical imaging for the diagnosis and management of common genitourinary cancers. Urol Oncol 35(7):473–491

    Article  PubMed  PubMed Central  Google Scholar 

  • Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? The Lancet 357(9255):539–545

    Article  CAS  Google Scholar 

  • Ball R (2005) Pathology and genetics of tumours of the urinary system and male genital organs. Histopathology 46(5):586–586

    Article  Google Scholar 

  • Belladonna ML, Renauld J-C, Bianchi R, Vacca C, Fallarino F, Orabona C, Fioretti MC, Grohmann U, Puccetti P (2002) IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J Immunol 168(11):5448–5454

    Article  CAS  PubMed  Google Scholar 

  • Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424

    Article  PubMed  Google Scholar 

  • Cassetta L, Fragkogianni S, Sims AH, Swierczak A, Forrester LM, Zhang H, Soong DYH, Cotechini T, Anur P, Lin EY, Fidanza A, Lopez-Yrigoyen M, Millar MR, Urman A, Ai Z, Spellman PT, Hwang ES, Dixon JM, Wiechmann L, Coussens LM, Smith HO, Pollard JW (2019) Human tumor-associated macrophage and monocyte transcriptional landscapes reveal cancer-specific reprogramming Biomarkers, and Therapeutic Targets. Cancer Cell 35(4):588-602.e10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chamie K, Litwin MS, Bassett JC, Daskivich TJ, Lai J, Hanley JM (2013) Urologic Diseases in America Project. Recurrence of high‐risk bladder cancer: a population‐based analysis. Cancer 119(17):3219-3227

  • Chang AH, Parsonnet J (2010) Role of Bacteria in Oncogenesis. Clin Microbiol Rev 23(4):837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheah MT, Chen JY, Sahoo D, Contreras-Trujillo H, Volkmer AK, Scheeren FA, Volkmer J-P, Weissman IL (2015) CD14-expressing cancer cells establish the inflammatory and proliferative tumor microenvironment in bladder cancer. Proc Natl Acad Sci USA 112(15):4725–4730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Chatterjee N (2007) Exploiting Hardy-Weinberg Equilibrium for Efficient Screening of Single SNP Associations from Case-Control Studies. Hum Hered 63:196–204

    Article  PubMed  Google Scholar 

  • Chen Z, Laurence A, O’Shea JJ (2007) Signal transduction pathways and transcriptional regulation in the control of Th17 differentiation. Semin Immunol 19(6):400–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Wan J, Liu J, Xie W, Diao X, Xu J, Zhu B, Chen Z (2010) Increased IL-17-producing cells correlate with poor survival and lymphangiogenesis in NSCLC patients. Lung Cancer 69(3):348–354

    Article  PubMed  Google Scholar 

  • Chen B, Zeng Z, Xu L, Wu X, Chen M, Hu P, Yu J, Sung JJY, Xue L, Hao Y, Wang Y (2011) IL23R +2199A/C polymorphism is associated with decreased risk of certain subtypes of gastric cancer in Chinese: A case-control study. Cancer Epidemiol 35(2):165–169

    Article  CAS  PubMed  Google Scholar 

  • Chi LJ, Lu HT, Li GL, Wang XM, Su Y, Xu WH, Shen BZ (2010) Involvement of T helper type 17 and regulatory T cell activity in tumour immunology of bladder carcinoma. Clin Exp Immunol 161(3):480–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chien MH, Hsin CH, Shih-Shen Chou L, Chung TT, Lin CH, Weng MS, Chou MY, Chen MK, Yang SF (2012) Interleukin-23 receptor polymorphism as a risk factor for oral cancer susceptibility. Head & Neck 34(4):551–556

    Article  Google Scholar 

  • Chu H, Wang M, Zhang Z (2013) Bladder cancer epidemiology and genetic susceptibility. J Biomed Res 27(3):170–178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crew J, Brien TO, Bradburn M, Fuggle S, Bicknell R, Cranston D, Harris AL (1998) Vascular Endothelial Growth Factor is a Predictor of Relapse and Stage Progression in Superficial Bladder Cancer

  • Cochran WG (1954) Some methods for strengthening the common χ 2 tests. Biometrics 10(4):417–451

    Article  Google Scholar 

  • Compérat EM, Burger M, Gontero P, Mostafid AH, Palou J, Rouprêt M, van Rhijn BW, Shariat SF, Sylvester RJ, Zigeuner R (2019) Grading of urothelial carcinoma and the new “World Health Organisation classification of Tumours of the urinary system and male genital organs 2016.” Eur Urol Focus 5(3):457–466

    Article  PubMed  Google Scholar 

  • DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188

    Article  CAS  PubMed  Google Scholar 

  • Duerr RH, Taylor KD, Brant SR, Rioux JD, Silverberg MS, Daly MJ, Steinhart AH, Abraham C, Regueiro M, Griffiths A, Dassopoulos T, Bitton A, Yang H, Targan S, Datta LW, Kistner EO, Schumm LP, Lee AT, Gregersen PK, Barmada MM, Rotter JI, Nicolae DL, Cho JH (2006) A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314(5804):1461–1463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Gedamy M, El-khayat Z, Abol-Enein H, El-said A, El-Nahrery E (2021) Rs-1884444 G/T variant in IL-23 receptor is likely to modify risk of bladder urothelial carcinoma by regulating IL-23/IL-17 inflammatory pathway. Cytokine 138:155355

    Article  CAS  PubMed  Google Scholar 

  • El-Hakim A, Weiss GH, Lee BR, Smith AD (2004) Correlation of ureteroscopic appearance with histologic grade of upper tract transitional cell carcinoma. Urology 63(4):647–650

    Article  PubMed  Google Scholar 

  • Fahmy O, Khairul-Asri MG, Schubert T, Renninger M, Kübler H, Stenzl A, Gakis G (2018) Urethral recurrence after radical cystectomy for urothelial carcinoma: A systematic review and meta-analysis. Urol Oncol 36(2):54–59

    Article  PubMed  Google Scholar 

  • Gakis G (2014) The Role of Inflammation in Bladder Cancer. Adv Exp Med Biol 816:183–196

    Article  CAS  PubMed  Google Scholar 

  • Glen P, Prashar A, Hawary A (2016) Sterile pyuria: a practical management guide. Br J Gen Pract 66(644):e225–e227

    Article  PubMed  PubMed Central  Google Scholar 

  • Grohmann U, Bianchi R, Belladonna ML, Vacca C, Silla S, Ayroldi E, Fioretti MC, Puccetti P (1999) IL-12 acts selectively on CD8α− dendritic cells to enhance presentation of a tumor peptide in vivo. J Immunol 163(6):3100–3105

    Article  CAS  PubMed  Google Scholar 

  • Hanada T, Nakagawa M, Emoto A, Nomura T, Nasu N, Nomura Y (2000) Prognostic value of tumor-associated macrophage count in human bladder cancer. Int J Urol 7(7):263–269

    Article  CAS  PubMed  Google Scholar 

  • He D, Li H, Yusuf N, Elmets CA, Li J, Mountz JD, Xu H (2010) IL-17 Promotes Tumor Development through the Induction of Tumor Promoting Microenvironments at Tumor Sites and Myeloid-Derived Suppressor Cells. J Immunol 184(5):2281–2288

    Article  CAS  PubMed  Google Scholar 

  • Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560

    Article  PubMed  PubMed Central  Google Scholar 

  • Horimoto Y, Polanska UM, Takahashi Y, Orimo A (2012) Emerging roles of the tumor-associated stroma in promoting tumor metastasis. Cell Adh Migr 6(3):193–202

    Article  PubMed  PubMed Central  Google Scholar 

  • Hughes R, Qian B-Z, Rowan C, Muthana M, Keklikoglou I, Olson OC, Tazzyman S, Danson S, Addison C, Clemons M (2015) Perivascular M2 macrophages stimulate tumor relapse after chemotherapy. Can Res 75(17):3479–3491

    Article  CAS  Google Scholar 

  • Ibrahim AS, Khaled HM, Mikhail NN, Baraka H, Kamel H (2014) Cancer incidence in Egypt: results of the national population-based cancer registry program. J Cancer Epidemiol

  • Iida T, Iwahashi M, Katsuda M, Ishida K, Nakamori M, Nakamura M, Naka T, Ojima T, Ueda K, Hayata K (2011) Tumor-infiltrating CD4+ Th17 cells produce IL-17 in tumor microenvironment and promote tumor progression in human gastric cancer. Oncol Rep 25(5):1271–1277

    CAS  PubMed  Google Scholar 

  • Imtiaz F, Shafique K, Mirza SS, Ayoob Z, Vart P, Rao S (2012) Neutrophil lymphocyte ratio as a measure of systemic inflammation in prevalent chronic diseases in Asian population. Int Arch Med 5(1):2–2

    Article  PubMed  PubMed Central  Google Scholar 

  • Iwakura Y, Ishigame H (2006) The IL-23/IL-17 axis in inflammation. J Clin Investig 116(5):1218–1222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JK, Moon KC, Jeong CW, Kwak C, Kim HH, Ku JH (2017) Papillary Urothelial Neoplasm of Low Malignant Potential (PUNLMP) After Initial TUR-BT: Comparative Analyses with Noninvasive Low-Grade Papillary Urothelial Carcinoma (LGPUC). J Cancer 8(15):2885–2891

    Article  PubMed  PubMed Central  Google Scholar 

  • Konjević GM, Vuletić AM, Martinović KMM, Larsen AK, Jurišić VB (2019) The role of cytokines in the regulation of NK cells in the tumor environment. Cytokine 117:30–40

    Article  PubMed  CAS  Google Scholar 

  • Koutros S, Lynch CF, Ma X, Lee WJ, Hoppin JA, Christensen CH, Alavanja MC (2009) Heterocyclic aromatic amine pesticide use and human cancer risk: results from the US Agricultural Health Study. Int J Cancer 124(5):1206–1212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krajewski W, Karabon L, Partyka A, Tomkiewicz A, Poletajew S, Tukiendorf A, Kołodziej A, Zdrojowy R (2020) Polymorphisms of genes encoding cytokines predict the risk of high-grade bladder cancer and outcomes of BCG immunotherapy. Cent Eur J Immunol 45(1):37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krochmal M, van Kessel KEM, Zwarthoff EC, Belczacka I, Pejchinovski M, Vlahou A, Mischak H, Frantzi M (2019) Urinary peptide panel for prognostic assessment of bladder cancer relapse. Sci Rep 9(1):7635–7635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kryczek I, Wei S, Zou L, Altuwaijri S, Szeliga W, Kolls WJ, Chang A, Zou W (2007) Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J Immunol (Baltimore, Md. : 1950) 178(11):6730–6733

  • Landskron G, De la Fuente M, Thuwajit P, Thuwajit C, Hermoso MA (2014) Chronic inflammation and cytokines in the tumor microenvironment. J Immunol Res 2014:149185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Langowski JL, Zhang X, Wu L, Mattson JD, Chen T, Smith K, Basham B, McClanahan T, Kastelein RA, Oft M (2006) IL-23 promotes tumour incidence and growth. Nature 442:461

    Article  CAS  PubMed  Google Scholar 

  • Li FF, Zhu XD, Yan P, Jin MH, Yue H, Zhang Q, Fu J, Liu SL (2016) Characterization of variations in IL23A and IL23R genes: possible roles in multiple sclerosis and other neuroinflammatory demyelinating diseases. Aging (Albany NY) 8(11):2734–2744

    Article  Google Scholar 

  • Lihong W, Wei L, Wei J, Jing L, Yongdong J, Bo L, Da P (2012) A miRNA Binding Site SingleNucleotide Polymorphism in the 3-UTR Region of the IL23R Gene Is Associated with Breast Cancer. PLoS One 7(12)

  • Lin C, Lin W, Yeh S, Li L, Chang C (2015) Infiltrating neutrophils increase bladder cancer cell invasion via modulation of androgen receptor (AR)/MMP13 signals. Oncotarget 6(40):43081–43089

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu XH, Dai ZM, Kang HF, Lin S, Ma XB, Wang M, Liu K, Dai C, Wang XJ, Dai ZJ (2015) Association of IL-23R Polymorphisms (rs6682925, rs10889677, rs1884444) With Cancer Risk: A PRISMA-Compliant Meta-Analysis. Medicine 94(52):e2361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Wang L, Wang T, Wang J (2018) Expression of IL-23R and IL-17 and the pathology and prognosis of urinary bladder carcinoma. Oncology letters 16(4):4325–4330

    PubMed  PubMed Central  Google Scholar 

  • Mantel N, Haenszel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22(4):719–748

    CAS  PubMed  Google Scholar 

  • Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454:436

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Lostao L, Anel A, Pardo J (2015) How do cytotoxic lymphocytes kill cancer cells? Clin Cancer Res 21(22):5047–5056

    Article  PubMed  CAS  Google Scholar 

  • Martin-Orozco AL, Dong C (2009) The IL-17/IL-23 axis of inflammation in cancer: Friend or foe?

  • Michaud DS (2007) Chronic inflammation and bladder cancer. Urol Oncol 25(3):260–268

    Article  CAS  PubMed  Google Scholar 

  • Miyashita M, Sasano H, Tamaki K, Hirakawa H, Takahashi Y, Nakagawa S, Watanabe G, Tada H, Suzuki A, Ohuchi N, Ishida T (2015) Prognostic significance of tumor-infiltrating CD8+ and FOXP3+ lymphocytes in residual tumors and alterations in these parameters after neoadjuvant chemotherapy in triple-negative breast cancer: a retrospective multicenter study. Breast Cancer Res : BCR 17(1):124

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Moch H, Cubilla AL, Humphrey PA, Reuter VE, Ulbright TM (2016) The 2016 WHO classification of tumours of the urinary system and male genital organs—part A: renal, penile, and testicular tumours. Eur Urol 70(1):93–105

    Article  PubMed  Google Scholar 

  • Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Sys Rev 4(1):1

    Article  Google Scholar 

  • Mosallaei M, Simonian M, Esmaeilzadeh E, Bagheri H, Miraghajani M, Salehi AR, Mehrzad V, Salehi R (2019) Single nucleotide polymorphism rs10889677 in miRNAs Let-7e and Let-7f binding site of IL23R gene is a strong colorectal cancer determinant: Report and meta-analysis. Cancer Genet 239:46–53

    Article  PubMed  Google Scholar 

  • Moschen AR, Tilg H, Raine T (2019) IL-12, IL-23 and IL-17 in IBD: immunobiology and therapeutic targeting. Nat Rev Gastroenterol Hepatol 16(3):185–196

    Article  CAS  PubMed  Google Scholar 

  • Mostafa MH, Sheweita SA, O’Connor PJ (1999) Relationship between schistosomiasis and bladder cancer. Clin Microbiol Rev 12(1):97–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moudi B, Heidari Z, Mahmoudzadeh-Sagheb H, Hashemi M (2016) Gene polymorphisms of macrophage migration inhibitory factor affect susceptibility to chronic hepatitis B virus infection in an Iranian cohort. MIM Microbiol and Immunol 60(6):390–396

    Article  CAS  Google Scholar 

  • Moussa M, & Abou Chakra M (2018) Urothelial carcinoma arising from a bladder diverticulum containing multiple stones: a case report. Urology Case Reports 20(80)

  • Murugaiyan G, Saha B (2009) Protumor vs Antitumor Functions of IL-17. J Immunol 183(7):4169

    Article  CAS  PubMed  Google Scholar 

  • Nakae S, Saijo S, Horai R, Sudo K, Mori S, Iwakura Y (2003) IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci USA 100(10):5986–5990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakae S, Iwakura Y, Suto H, Galli SJ (2007) Phenotypic differences between Th1 and Th17 cells and negative regulation of Th1 cell differentiation by IL-17. J Leukoc Biol 81(5):1258–1268

    Article  CAS  PubMed  Google Scholar 

  • Nemati K, Golmoghaddam H, Hosseini SV, Ghaderi A, Doroudchi M (2015) Interleukin-17FT7488 allele is associated with a decreased risk of colorectal cancer and tumor progression. Gene 561(1):88–94

    Article  CAS  PubMed  Google Scholar 

  • Nesi G, Nobili S, Cai T, Caini S, Santi R (2015) Chronic inflammation in urothelial bladder cancer. Virchows Arch 467(6):623–633

    Article  CAS  PubMed  Google Scholar 

  • Ni B, Chen S, Xie H, Ma H, Miao X (2014) Functional Polymorphisms in Interleukin-23 Receptor and Susceptibility to Esophageal Squamous Cell Carcinoma in Chinese Population. PLoS One 9(2):e89111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Numasaki M, Fukushi J-I, Ono M, Narula SK, Zavodny PJ, Kudo T, Robbins PD, Tahara H, Lotze MT (2003) Interleukin-17 promotes angiogenesis and tumor growth. Blood 101(7):2620–2627

    Article  CAS  PubMed  Google Scholar 

  • O’Connor W, Kamanaka M, Booth C, Town T, Nakae S, Iwakura Y, Kolls J, Flavell R (2009) A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol 10:603–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omrane I, Baroudi O, Bougatef K, Mezlini A, Abidi A, Medimegh I, Stambouli N, Ayari H, Kourda N, Uhrhammer N, Bignon YJ, Benammar Elgaaied A, Marrakchi R (2014) Significant association between IL23R and IL17F polymorphisms and clinical features of colorectal cancer. IMLET Immunol Letters 158(1–2):89–194

    Google Scholar 

  • Parham C, Chirica M, Timans J, Vaisberg E, Travis M, Cheung J, Pflanz S, Zhang R, Singh KP, Vega F, To W, Wagner J, O’Farrell AM, cClanahan TM, Zurawski S, Hannum C, Gorman D, Rennick DM, Kastelein, de Waal RA, Malefyt R, Moore KW, (2002) A Receptor for the Heterodimeric Cytokine IL-23 Is Composed of IL-12Rβ1 and a Novel Cytokine Receptor Subunit, IL-23R. J Immunol 168(11):5699–5708

    Article  CAS  PubMed  Google Scholar 

  • Paunescu V, Bojin FM, Tatu CA, Gavriliuc OI, Rosca A, Gruia AT, Tanasie G, Bunu C, Crisnic D, Gherghiceanu M, Tatu FR, Tatu CS, Vermesan S (2011) Tumour-associated fibroblasts and mesenchymal stem cells: more similarities than differences. J Cell Mol Med 15(3):635–646

    Article  CAS  PubMed  Google Scholar 

  • Prasad SM, Decastro GJ, Steinberg GD (2011) Medscape, Urothelial carcinoma of the bladder: definition, treatment and future efforts. Nature Rev Urol 8(11):631–642

    Article  CAS  Google Scholar 

  • Qin B, Ma N, Tang Q, Wei T, Yang M, Fu H, Hu Z, Liang Y, Yang Z, Zhong R (2016) Neutrophil to lymphocyte ratio (NLR) and platelet to lymphocyte ratio (PLR) were useful markers in assessment of inflammatory response and disease activity in SLE patients. Mod Rheumatol 26(3):372–376

    Article  PubMed  Google Scholar 

  • Richards KA, Ham S, Cohn JA, Steinberg GD (2016) Urinary tract infection-like symptom is associated with worse bladder cancer outcomes in the Medicare population: Implications for sex disparities. Int J Urol 23(1):42–47

    Article  PubMed  Google Scholar 

  • Saito K, Kihara K (2013) Role of C-reactive protein in urological cancers: A useful biomarker for predicting outcomes. Int J Urol 20(2):161–171

    Article  CAS  PubMed  Google Scholar 

  • Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M (1995) Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25), Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155(3):1151–1164

    Article  CAS  PubMed  Google Scholar 

  • Seitz M, Zaak D, Knüchel-Clarke R, Stief C (2005) Urinary bladder tumours. The new 2004 WHO classification. Der Urologe. Ausg. A. 44(9):1073–86

  • Sheweita SA, Alsamghan AS (2020) Molecular Mechanisms Contributing Bacterial Infections to the Incidence of Various Types of Cancer. Mediators Inflamm 2020:4070419

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sonawane MD, Nimse SB (2017) C-Reactive protein: a major inflammatory biomarker. Anal Methods 9(23):3400–3413

    Article  CAS  Google Scholar 

  • Sterne JA, Gavaghan D, Egger M (2000) Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J Clin Epidemiol 53(11):1119–1129

    Article  CAS  PubMed  Google Scholar 

  • Stone L (2015) Bladder cancer: Urinary tract infection increases risk. Nat Rev Urol 12(1):4–4

    Article  PubMed  Google Scholar 

  • Sui X, Lei L, Chen L, Xie T, Li X (2017) Inflammatory microenvironment in the initiation and progression of bladder cancer. Oncotarget 8(54):93279

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun L, He C, Nair L, Yeung J, Egwuagu CE (2015) Interleukin 12 (IL-12) family cytokines: Role in immune pathogenesis and treatment of CNS autoimmune disease. Cytokine 75(2):249–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sylvester R (2011) Bacillus Calmette-Guérin treatment of non-muscle invasive bladder cancer. Inte J Urol :J Japanese Urol Assoc 18:113–120

    Article  CAS  Google Scholar 

  • Takahashi H, Numasaki M, Lotze MT, Sasaki H (2005) Interleukin-17 enhances bFGF-HGF-and VEGF-induced growth of vascular endothelial cells. Immunol Letters 98(2):189–193

    Article  CAS  Google Scholar 

  • Tang T, Xue H, Cui S, Gong Z, Fei Z, Cheng S, Gui C (2014) Association of interleukin-23 receptor gene polymorphisms with risk of bladder cancer in Chinese. Familial Cancer Dordrecht 13(4):619–623

    Article  CAS  Google Scholar 

  • Teng MWL, Andrews DM, McLaughlin N, von Scheidt B, Ngiow SF, Möller A, Hill GR, Iwakura Y, Oft M, Smyth MJ (2010a) IL-23 suppresses innate immune response independently of IL-17A during carcinogenesis and metastasis. Proc Natl Acad Sci U S A 107(18):8328–8333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson DB, Siref LE, Feloney MP, Hauke RJ, Agrawal DK (2015) Immunological basis in the pathogenesis and treatment of bladder cancer. Expert Rev Clin Immunol 11(2):265–279

    Article  CAS  PubMed  Google Scholar 

  • Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B (2006) TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24(2):179–189

    Article  CAS  PubMed  Google Scholar 

  • Vermeulen SH, Hanum N, Grotenhuis AJ, Castano-Vinyals G, van der Heijden AG, Aben KK, Mysorekar IU, Kiemeney LA (2015) Recurrent urinary tract infection and risk of bladder cancer in the Nijmegen bladder cancer study. Br J Cancer 112(3):594–600

    Article  CAS  PubMed  Google Scholar 

  • Vignali DA, Kuchroo VK (2012) IL-12 family cytokines: immunological playmakers. Nat Immunol 13(8):722–728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volpe E, Servant N, Zollinger R, Bogiatzi S, Hupé P, Barillot E, Soumelis V (2008) A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nat Immunol 9(6):650

  • Wang W, Fan Y, Xiong G, Wu J (2012) Nitrate in drinking water and bladder cancer: A meta-analysis. Journal of Huazhong University of Science and Technology [Medical Sciences] 32(6):912–918

    Article  CAS  Google Scholar 

  • Wang L, Liu W, Jiang W, Lin J, Jiang Y, Li B, Pang D (2012) A miRNA binding site single-nucleotide polymorphism in the 3′-UTR region of the IL23R gene is associated with breast cancer. PLoS One 7(12):e49823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams CB, Yeh ES, Soloff AC (2016) Tumor-associated macrophages: unwitting accomplices in breast cancer malignancy. Npj Breast Cancer 2:15025

    Article  PubMed  PubMed Central  Google Scholar 

  • Wong MCS, Fung FDH, Leung C, Cheung WWL, Goggins WB, Ng CF (2018) The global epidemiology of bladder cancer: a joinpoint regression analysis of its incidence and mortality trends and projection. Sci Rep 8(1):1129

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu X, Yang C, Chen J, Liu J, Shi Y, Yu P (2018) Interleukin-23 promotes the migration and invasion of gastric cancer cells by inducing epithelial-to-mesenchymal transition via the STAT3 pathway. Biochem Biophys Res Commun 499(2):273–278

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Kang H, Fung A, Zhao H, Wang T, Ma D (2014) The role of interleukin 17 in tumour proliferation, angiogenesis, and metastasis. Mediators Inflamm 2014:623759–623759

    Article  PubMed  PubMed Central  Google Scholar 

  • Zahorec R (2001) Ratio of neutrophil to lymphocyte counts-rapid and simple parameter of systemic inflammation and stress in critically ill. Bratisl Lek Listy 102(1):5–14

    CAS  PubMed  Google Scholar 

  • Zhang Z, Zhou B, Zhang J, Chen Y, Lai T, Yan L, Liang A, Li Y, Wang Y, Chen Y, Zhang L, Xi M-R (2010) Association of interleukin-23 receptor gene polymorphisms with risk of ovarian cancer. CGC Cancer Genet Cytogenet 196(2):146–152

    Article  CAS  Google Scholar 

  • Zheng J, Jiang L, Zhang L, Yang L, Deng J, You Y, Li N, Wu H, Li W, Lu J, Zhou Y (2012) Functional genetic variations in the IL-23 receptor gene are associated with risk of breast, lung and nasopharyngeal cancer in Chinese populations. Carcinogenesis 33(12):2409–2416

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Ruan Y, Yu H, Chen Y, Yao Y, Ma Y, Gao Y (2013) Functional IL-23R rs10889677 genetic polymorphism and risk of multiple solid tumors: a meta-analysis. PLoS One 8(11):e80627

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu Z, Shen Z, Xu C (2012) Inflammatory pathways as promising targets to increase chemotherapy response in bladder cancer. Mediators Inflamm 2012:528690–528690

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zwiers A, Kraal L, van de Pouw Kraan TC, Wurdinger T, Bouma G, Kraal G (2012) Cutting edge: a variant of the IL-23R gene associated with inflammatory bowel disease induces loss of microRNA regulation and enhanced protein production. J Immunol 188(4):1573–1577

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors also would like to sincerely thank Dr. Rami Elshazli (Horus University, Egypt) and Prof. Ahmad settin (Mansoura University, Egypt) for their sincere recommendations and helpful comments regarding the statistical analyses. In addition, the authors expressed their appreciation to the colleagues of the Departments of Pathology and Urology, Urology and Nephrology Center, University of Mansoura, Egypt, for their cooperation in picking the right UBC cases under research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammed El-Gedamy.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El-Gedamy, M., El-khayat, Z., Abol-Enein, H. et al. Rs-10889677 variant in interleukin-23 receptor may contribute to creating an inflammatory milieu more susceptible to bladder tumourigenesis: report and meta-analysis. Immunogenetics 73, 207–226 (2021). https://doi.org/10.1007/s00251-021-01205-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-021-01205-w

Keywords

Navigation