Angiogenesis in Schistosoma haematobium-associated urinary bladder cancer
Anderson Dematei
Ciências Químicas e das Biomoléculas, Escola Superior de Saúde, Instituto Politécnico do Porto, Porto, Portugal
Search for more papers by this authorRúben Fernandes
Ciências Químicas e das Biomoléculas, Escola Superior de Saúde, Instituto Politécnico do Porto, Porto, Portugal
I3S, Instituto de Investigação e Inovação da Universidade do Porto, Porto, Portugal
Search for more papers by this authorRaquel Soares
I3S, Instituto de Investigação e Inovação da Universidade do Porto, Porto, Portugal
Departamento de Biomedicina, Unidade de Bioquímica, Faculdade de Medicina, Universidade do Porto, Porto, Portugal
Search for more papers by this authorHelena Alves
Department of Health Promotion and Chronic Diseases, INSA – National Institute of Health Dr. Ricardo Jorge, Porto, Portugal
Fundação Professor Ernesto Morais, Porto, Portugal
Search for more papers by this authorJoachim Richter
Institute of Tropical Medicine and International Health, Charité – Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorCorresponding Author
Monica C. Botelho
I3S, Instituto de Investigação e Inovação da Universidade do Porto, Porto, Portugal
Department of Health Promotion and Chronic Diseases, INSA – National Institute of Health Dr. Ricardo Jorge, Porto, Portugal
Mónica C. Botelho, Department of Health Promotion and Chronic Diseases, INSA – National Institute of Health Dr. Ricardo Jorge, Rua Alexandre Herculano 321, Porto 4000-055, Portugal. e-mails: [email protected]; [email protected]Search for more papers by this authorAnderson Dematei
Ciências Químicas e das Biomoléculas, Escola Superior de Saúde, Instituto Politécnico do Porto, Porto, Portugal
Search for more papers by this authorRúben Fernandes
Ciências Químicas e das Biomoléculas, Escola Superior de Saúde, Instituto Politécnico do Porto, Porto, Portugal
I3S, Instituto de Investigação e Inovação da Universidade do Porto, Porto, Portugal
Search for more papers by this authorRaquel Soares
I3S, Instituto de Investigação e Inovação da Universidade do Porto, Porto, Portugal
Departamento de Biomedicina, Unidade de Bioquímica, Faculdade de Medicina, Universidade do Porto, Porto, Portugal
Search for more papers by this authorHelena Alves
Department of Health Promotion and Chronic Diseases, INSA – National Institute of Health Dr. Ricardo Jorge, Porto, Portugal
Fundação Professor Ernesto Morais, Porto, Portugal
Search for more papers by this authorJoachim Richter
Institute of Tropical Medicine and International Health, Charité – Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorCorresponding Author
Monica C. Botelho
I3S, Instituto de Investigação e Inovação da Universidade do Porto, Porto, Portugal
Department of Health Promotion and Chronic Diseases, INSA – National Institute of Health Dr. Ricardo Jorge, Porto, Portugal
Mónica C. Botelho, Department of Health Promotion and Chronic Diseases, INSA – National Institute of Health Dr. Ricardo Jorge, Rua Alexandre Herculano 321, Porto 4000-055, Portugal. e-mails: [email protected]; [email protected]Search for more papers by this authorAbstract
Schistosoma haematobium, a parasitic flatworm that infects more than 100 million people, mostly in the developing world, is the causative agent of urogenital schistosomiasis, and is associated with a high incidence of squamous cell carcinoma (SCC) of the bladder. During infection, eggs are deposited in the bladder causing an intense inflammatory reaction. Angiogenesis is defined as the formation of new blood vessels from preexisting ones and is recognized as a key event in cell proliferation and carcinogenesis and spread of malignant lesions. A growing amount of evidence points to angiogenesis playing a key role in schistosomiasis-associated bladder cancer. Thus, identifying biomarkers of this process plays an important role in the study of cancer. Here, we review recent findings on the role of angiogenesis in bladder cancer and the growth factors that induce and assist in their development, particularly SCC of the bladder associated to urogenital schistosomiasis.
References
- 1Mott KE. Contrasts in the control of schistosomiasis. Mem Inst Oswaldo Cruz 1989; 84: 3–19.
- 2 World Health Organization. Weekly epidemiological record, 90th year, 2015; 90, 25–32. http://www.who.int/wer
- 3 WHO. Schistosomiasis: Progress Report 2001–2011, Strategic Plan 2012–2020. Geneva: World Health Organization, 2013.
- 4Botelho MC, Alves H, Richter J. Halting Schistosoma haematobium -associated bladder cancer. Ira J Can Prev (in press).
- 5Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis and estimates of people at risk. Lancet Infect Dis 2006; 6: 411–425.
- 6Holtfreter MC, Moné H, Müller-Stöver I, Mouahid G, Richter J. Schistosoma haematobium infections acquired in Corsica, France, August 2013. Euro Surveill 2014; 19: pii 20821.
10.2807/1560-7917.ES2014.19.22.20821 Google Scholar
- 7Botelho MC, Vale N, Gouveia MJ, Rinaldi G, Santos J, Santos LL, et al. Tumour-like phenotypes in urothelial cells after exposure to antigens from eggs of Schistosoma haematobium: an oestrogen-DNA adducts mediated pathway? Int J Parasitol 2013; 43: 17–26.
- 8van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, Habbema JD, et al. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 2003; 86: 125–39.
- 9Hotez PJ, Fenwick A, Kjetland EF. Africa's 32 cents solution for HIV/AIDS. PLoS Negl Trop Dis 2009; 3: e430.
- 10King CH. Parasites and poverty: the case of schistosomiasis. Acta Trop 2010; 113: 95–104.
- 11Hodder SL, Mahmoud AA, Sorenson K, Weinert DM, Stein RL, Ouma JH, et al. Predisposition to urinary tract epithelial metaplasia in Schistosoma haematobium infection. Am J Trop Med Hyg 2000; 63: 133–8
- 12Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 2006; 118: 3030–44
- 13Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El GhissassiF, et al. A review of human carcinogens – Part B: biological agents. Lancet Oncol 2009; 10: 321–2.
- 14 IARC, Biological agents. Volume 100 B. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum 2012; 100(Pt B): 1–441.
- 15Mostafa MH, Sheweita SA, O'Connor PJ. Relationship between schistosomiasis and bladder cancer. Clin Microbiol Rev 1999; 12: 97–111.
- 16Zhong X, Isharwal S, Naples JM, Shiff C, Veltri RW, Shao C, et al. Hypermethylation of genes detected in urine from Ghanaian adults with bladder pathology associated with Schistosoma haematobium infection. PLoS One 2013; 8: e59089.
- 17Shiff C, Veltri R, Naples J, Quartey J, Otchere J, Anyan W, et al. Ultrasound verification of bladder damage is associated with known biomarkers of bladder cancer in adults chronically infected with Schistosoma haematobium in Ghana. Trans R Soc Trop Med Hyg 2006; 100: 847–54.
- 18Rambau PF, Chalya PL, Jackson K. Schistosomiasis and urinary bladder cancer in North Western Tanzania: a retrospective review of 185 patients. Infect Agent Cancer 2013; 8: 19.
- 19Honeycutt J, Hammam O, Fu CL, Hsieh MH. Controversies and challenges in research on urogenital s Controversies and challenges in research on urogenital schistosomiasis-associated bladder cancer. Trends Parasitol 2014; 30: 324–32.
- 20Botelho MC, Oliveira PA, Lopes C, Correia da Costa JM, Machado JC. Urothelial dysplasia and inflammation induced by Schistosoma haematobium total antigen instillation in mice normal urothelium. Urol Oncol 2011; 29: 809–14.
- 21Botelho MC, Alves H, Barros A, Rinaldi G, Brindley PJ, Sousa M. The role of estrogens and estrogen receptor signaling pathways in cancer and infertility: the case of schistosomes. Trends Parasitol 2015; 31: 246–50.
- 22Botelho MC, Alves H, Richter J. Estrogen metabolites for the diagnosis of schistosomiasis associated urinary bladder cancer. SM Trop Med J 2016; 1: 1004
- 23Botelho MC, Alves H, Richter J. Estrogen catechols detection as biomarkers in schistosomiasis induced cancer and infertility. Lett Drug Des Discov 2017; 14: 135–8
- 24Botelho MC, Teixeira JP, Oliveira PA. Carcinogenesis, In: P Wexler, editor. Encyclopedia of Toxicology ( 3rd edn). Oxford: Academic Press, 2014: 713–29.
10.1016/B978-0-12-386454-3.00371-7 Google Scholar
- 25Van de Vijver KK, Colpaert CG, Jacobs W, Kuypers K, Hokke CH, Deelder AM, et al. The host's genetic background determines the extent of angiogenesis induced by schistosome egg antigens. Acta Trop 2006; 99: 243–51.
- 26Miyata Y, Kanda S, Ohba K, Nomata K, Hayashida Y, Eguchi J, et al. Lymphangiogenesis and angiogenesis in bladder cancer: prognostic implications and regulation by vascular endothelial growth factors-A, -C, and -D. Clin Cancer Res 2006; 12: 800–6.
- 27Eissa S, Swellam M, Labib RA, El-Zayat T, El Ahmady O. A panel of angiogenic factors for early bladder cancer detection: enzyme immunoassay and Western blot. J Urol 2009; 181: 1353–60.
- 28Wartiovaara U, Salven P, Mikkola H, Lassila R, Kaukonen J, Joukov V, et al. Peripheral blood platelets express VEGF-C and VEGF which are released during platelet activation. Thromb Haemost 1998; 80: 171–5.
- 29Hashimoto I, Kodama J, Seki N, Hongo A, Yoshinouchi M, Okuda H, et al. Vascular endothelial growth factor-C expression and its relationship to pelvic lymph node status in invasive cervical cancer. Br J Cancer 2001; 85: 93–7.
- 30Hirai M, Nakagawara A, Oosaki T, Hayashi Y, Hirono M, Yoshihara T. Expression of vascular endothelial growth factors (VEGF-A/VEGF-1 and VEGF-C/VEGF-2) in postmenopausal uterine endometrial carcinoma. Gynecol Oncol 2001; 80: 181–8.
- 31Nishida N, Yano H, Komai K, Nishida T, Kamura T, Kojiro M. Vascular endothelial growth factor C and vascular endothelial growth factor receptor 2 are related closely to the prognosis of patients with ovarian carcinoma. Cancer 2004; 101: 1364–74.
- 32Amioka T, Kitadai Y, Tanaka S, Haruma K, Yoshihara M, Yasui W, et al. Vascular endothelial growth factor-C expression predicts lymph node metastasis of human gastric carcinomas invading the submucosa. Eur J Cancer 2002; 38: 1413–9.
- 33Furudoi A, Tanaka S, Haruma K, Kitadai Y, Yoshihara M, Chayama K, et al. Clinical significance of vascular endothelial growth factor C expression and angiogenesis at the deepest invasive site of advanced colorectal carcinoma. Oncology 2002; 62: 157–66.
- 34Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P, et al. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 2001; 7: 192–8.
- 35Kajita T, Ohta Y, Kimura K, Tamura M, Tanaka Y, Tsunezuka Y, et al. The expression of vascular endothelial growth factor C and its receptors in non-small cell lung cancer. Br J Cancer 2001; 85: 255–60.
- 36O-charoenrat P, Rhys-Evans P, Eccles SA. Expression of vascular endothelial growth factor family members in head and neck squamous cell carcinoma correlates with lymph node metastasis. Cancer 2001; 92: 556–68.
10.1002/1097-0142(20010801)92:3<556::AID-CNCR1355>3.0.CO;2-Q CAS PubMed Web of Science® Google Scholar
- 37Jussila L, Valtola R, Partanen TA, Salven P, Heikkilä P, Matikainen MT, et al. Lymphatic endothelium and Kaposi's sarcoma spindle cells detected by antibodies against the vascular endothelial growth factor receptor-3. Cancer Res 1998; 58: 1599–604.
- 38Ohta Y, Shridhar V, Bright RK, Kalemkerian GP, Du W, Carbone M, et al. VEGF and VEGF type C play an important role in angiogenesis and lymphangiogenesis in human malignant mesothelioma tumours. Br J Cancer 1999; 81: 54–61.
- 39Stacker SA, Achen MG, Jussila L, Baldwin ME, Alitalo K. Lymphangiogenesis and cancer metastasis. Nat Rev Cancer 2002; 2: 573–83.
- 40Elsobky E, El-Baz M, Gomha M, Abol-Enein H, Shaaban AA. Prognostic value of angiogenesis in schistosoma-associated squamous cell carcinoma of the urinary bladder. Urology 2002; 60: 69–73.
- 41Christiansen A, Detmar M. Lymphangiogenesis and cancer. Genes Cancer 2011; 2: 1146–58.
- 42Matsuo T, Miyata Y, Mitsunari K, Yasuda T, Ohba K, Sakai H. Pathological significance and prognostic implications of heme oxygenase 1 expression in non-muscle-invasive bladder cancer: correlation with cell proliferation, angiogenesis, lymphangiogenesis and expression of VEGFs and COX-2. Oncol Lett 2017; 13: 275–80.
- 43Khadim MT, Ahmed SA, Khan FA, Ikram A, Shaikh SY. Evaluation of vascular endothelial growth factors A, C and D as indicators of lymphangiogenesis and angiogenesis in invasive and non-invasive urothelial carcinoma bladder. J Pak Med Assoc 2015; 65: 851–6.
- 44Fernández MI, Bolenz C, Trojan L, Steidler A, Weiss C, Alken P, et al. Prognostic implications of lymphangiogenesis in muscle-invasive transitional cell carcinoma of the bladder. Eur Urol 2008; 53: 571–8.
- 45Weinkopff T, Konradt C, Christian DA, Discher DE, Hunter CA, Scott P. Leishmania major infection-induced VEGF-A/VEGFR-2 signaling promotes lymphangiogenesis that controls disease. J Immunol 2016; 197: 1823–31.
- 46Chakraborty S, Gurusamy M, Zawieja DC, Muthuchamy M. Lymphatic filariasis: perspectives on lymphatic remodeling and contractile dysfunction in filarial disease pathogenesis. Microcirculation 2013; 20: 349–64.
- 47Andrade ZA, Santana TS. Angiogenesis and schistosomiasis. Mem Inst Oswaldo Cruz 2010; 105: 4.
- 48Botelho MC, Alves H, Richter J. Wound healing and cancer progression in Opisthorchis viverrini associated cholangiocarcinoma. Parasitol Res 2016; 115: 2913–4.
- 49Kanse SM, Liang O, Schubert U, Haas H, Preissner KT, Doenhoff MJ, et al. Characterisation and partial purification of Schistosoma mansoni egg-derived pro-angiogenic factor. Mol Biochem Parasitol 2005; 144: 76–85.
- 50Loeffler DA, Lundy SK, Singh KP, Gerard HC, Hudson AP, Boros DL. Soluble egg antigens from Schistosoma mansoni induce angiogenesis-related processes by up-regulating vascular endothelial growth factor in human endothelial cells. J Infect Dis 2002; 185: 1650–6.
- 51Tawfeek GM, Alafifi AM, Azmy MF. Immunological indicators of morbidity in human schistosomiasis mansoni: role of vascular endothelial growth factor and anti-soluble egg antigen IgG4 in disease progression. J Egypt Soc Parasitol 2003; 33: 597–614.
- 52Shariati F, Pérez-Arellano JL, Carranza C, López-Abán J, Vicente B, Arefi M, et al. Evaluation of the role of angiogenic factors in the pathogenesis of schistosomiasis. Exp Parasitol 2011; 128: 44–9.
- 53Machicado C, Marcos LA. Carcinogenesis associated with parasites other than Schistosoma, Opisthorchis and Clonorchis: a systematic review. Int J Cancer 2016; 138: 2915–21.
- 54Dickinson AJ, Fox SB, Persad RA, Hollyer J, Sibley GN, Harris AL. Quantification of angiogenesis as an independent predictor of prognosis in invasive bladder carcinomas. Br J Urol 1994; 74: 762–6.
- 55El Sobky E, Gomha M, El-Baz M, Abol-Enein H, Shaaban AA. Prognostic significance of tumour angiogenesis in schistosoma-associated adenocarcinoma of the urinary bladder. BJU Int 2002; 89: 126–32.
- 56Croquet V, Moal F, Veal N, Wang J, Oberti F, Roux J, et al. Hemodynamic and antifibrotic effects of losartan in rats with liver fibrosis and/or portal hypertension. J Hepatol 2002; 37: 773–80.