Molecular evidence of human papillomaviruses in the retinoblastoma tumor

Abstract

Retinoblastoma tumor (RB) is one of the most prevalent ocular cancers among children. RB may be caused by inherited mutations in RB1 gene as well as some environmental risk factors. Human papillomaviruses (HPV) are suspected as a risk factor of RB due to their pRb inactivating protein. This study evaluated the molecular prevalence of HPV among the RB tumor specimens in Iran. The RB tumor samples were tested for detection of HPV-L1 gene using a nested-PCR approach, and then followed by sequencing and phylogenetic analysis to reveal HPV types. Overall, there were 61 RB tumor samples; 54/61 (88.5%) had unilateral and 7/61 (11.5%) bilateral RB; 55/61 cases (90.2%) had sporadic non-familial RB tumor. HPV-DNA was detected in 6/61 (9.8%) of patients’ tumors; the HPV positive RB cases all had unilateral and unfamiliar sporadic RB tumor. HPV type 16 was the most prevalent type identified across the RB tumor samples (3/61, 4.9%). The rate of detected HPV among the RB specimens seems to be considerable. Further investigations are required to elucidate the exact association between HPV and progression to RB.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. 1.

    Anand B, Ramesh C, Appaji L, Kumari BSA, Shenoy AM, Nanjundappa, et al. Prevalence of high-risk human papillomavirus genotypes in retinoblastoma. Br J Ophthalmol. 2011;95(7):1014–8.

    PubMed  Google Scholar 

  2. 2.

    Antoneli CBG, Ribeiro KB, Sredni ST, Arias VEA, Andreoli MA, de Camargo B, et al. Low prevalence of HPV in Brazilian children with retinoblastoma. J Med Virol. 2011;83(1):115–8.

    PubMed  Google Scholar 

  3. 3.

    Bhuvaneswari A, Pallavi VR, Jayshree RS, Kumar RV. Maternal transmission of human papillomavirus in retinoblastoma: a possible route of transfer. Indian J Med Paediatr Oncol. 2012;33(4):210–5.

    PubMed  PubMed Central  Google Scholar 

  4. 4.

    Bunin GR, Meadows AT, Emanuel BS, Buckley JD, Woods WG, Hammond GD. Pre-and postconception factors associated with sporadic heritable and nonheritable retinoblastoma. Cancer Res. 1989;49(20):5730–5.

    CAS  PubMed  Google Scholar 

  5. 5.

    Chandana V, Gaguturu RB. Prevalence and determinants of high risk human papilloma virus in Hyderabad, India. Int J Reprod Contracept Obstet Gynecol. 2018;7(3):1012–8.

    Google Scholar 

  6. 6.

    Chauhan S, Sen S, Singh N, Sharma A, Chawla B, Kashyap S. Human papillomavirus detection strategies in retinoblastoma. Pathol Oncol Res. 2019;26:1–4.

    Google Scholar 

  7. 7.

    Chintagumpala M, Chevez-Barrios P, Paysse EA, Plon SE, Hurwitz R. Retinoblastoma: review of current management. Oncologist. 2007;12(10):1237–46.

    PubMed  Google Scholar 

  8. 8.

    de Martel C, Plummer M, Vignat J, Franceschi S. Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int J Cancer. 2017;141(4):664–70.

    PubMed  PubMed Central  Google Scholar 

  9. 9.

    de Paula Silva N, de Souza Reis R, Cunha RG, Oliveira JF, de Oliveira Santos M, Pombo-de-Oliveira MS, de Camargo B. Maternal and birth characteristics and childhood embryonal solid tumors: a population-based report from Brazil. PLoS ONE. 2016;11(10):e0164398.

    Google Scholar 

  10. 10.

    De Villiers E-M, Fauquet C, Broker TR, Bernard H-U, zur Hausen H. Classification of papillomaviruses. Virology. 2004;324(1):17–27.

    PubMed  Google Scholar 

  11. 11.

    Di Girolamo N. Association of human papilloma virus with pterygia and ocular-surface squamous neoplasia. Eye. 2011;26:202.

    PubMed  PubMed Central  Google Scholar 

  12. 12.

    Füle T, Máthé M, Suba Z, Csapó Z, Szarvas T, Tátrai P, et al. The presence of human papillomavirus 16 in neural structures and vascular endothelial cells. Virology. 2006;348(2):289–96.

    PubMed  Google Scholar 

  13. 13.

    Füle T, Máthé M, Suba Z, Csapó Z, Szarvas T, Tátrai P, Paku S, Kovalszky I. The presence of human papillomavirus 16 in neural structures and vascular endothelial cells. Virology. 2006;348(2):289–96.

    PubMed  Google Scholar 

  14. 14.

    Gillison ML, Chen R, Goshu E, Rushlow D, Chen N, Banister C, et al. Human retinoblastoma is not caused by known pRb-inactivating human DNA tumor viruses. Int J Cancer. 2007;120(7):1482–90.

    CAS  PubMed  Google Scholar 

  15. 15.

    Hausen H. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst. 2000;92(9):690–8.

    PubMed  Google Scholar 

  16. 16.

    Heck JE, Omidakhsh N, Azary S, Ritz B, von Ehrenstein OS, Bunin GR, Ganguly A. A case–control study of sporadic retinoblastoma in relation to maternal health conditions and reproductive factors: a report from the Children’s Oncology group. BMC Cancer. 2015;15(1):735.

    PubMed  PubMed Central  Google Scholar 

  17. 17.

    Javanmard D, Namaei MH, Haghighi F, Ziaee M, Behravan M, Mirzaei J, et al. The frequency and typing of human Papilloma virus among women with normal and abnormal cytology in Southern Khorasan, Eastern Iran. Jundishapur J Microbiol. 2017;10(4):e43213.

    Google Scholar 

  18. 18.

    Javanmard D, Behravan M, Ghannadkafi M, Salehabadi A, Ziaee M, Namaei MH. Detection of Chlamydia trachomatis in pap smear samples from South Khorasan Province of Iran. Int J Fertil Steril. 2018;12(1):31.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Karbalaie Niya MH, Keyvani H, Safarnezhad Tameshkel F, Salehi-Vaziri M, Teaghinezhad-S S, Bokharaei Salim F, et al. Human papillomavirus type 16 integration analysis by real-time PCR assay in associated cancers. Transl Oncol. 2018;11(3):593–8.

    PubMed  PubMed Central  Google Scholar 

  20. 20.

    Khorasanizadeh F, Hassanloo J, Khaksar N, Mohammad Taheri S, Marzaban M, H Rashidi B, et al. Epidemiology of cervical cancer and human papilloma virus infection among Iranian women—analyses of national data and systematic review of the literature. Gynecol Oncol. 2013;128(2):277–81.

    PubMed  Google Scholar 

  21. 21.

    Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 70 for bigger datasets. Mol Biol Evol. 2016;33(7):1870–4.

    CAS  Google Scholar 

  22. 22.

    Mammas IN, Sourvinos G, Spandidos DA. The ‘Trojan horse’oncogenic strategy of HPVs in childhood. Future Virol. 2013;8(8):801–8.

    CAS  Google Scholar 

  23. 23.

    Mohan A, Venkatesan N, Kandalam M, Pasricha G, Acharya P, Khetan V, et al. Detection of human papillomavirus DNA in retinoblastoma samples: a preliminary study. J Pediatr Hematol Oncol. 2009;31(1):8–13.

    CAS  PubMed  Google Scholar 

  24. 24.

    Montoya-Fuentes H, de la Paz Ramirez-Munoz M, Villar-Calvo V, Suarez-Rincon AE, Ornelas-Aguirre JM, Vazquez-Camacho G, et al. Identification of DNA sequences and viral proteins of 6 human papillomavirus types in retinoblastoma tissue. Anticancer Res. 2003;23(3c):2853–62.

    CAS  PubMed  Google Scholar 

  25. 25.

    Naru J, Aggarwal R, Singh U, Kakkar N, Bansal D. HPV-16 detected in one-fourth eyes with retinoblastoma: a prospective case-control study from North India. J Pediatr Hematol Oncol. 2016;38(5):367–71.

    PubMed  Google Scholar 

  26. 26.

    Naseripour M, Nazari H, Bakhtiari P, Modarres-zadeh M, Vosough P, Ausari M. Retinoblastoma in Iran: outcomes in terms of patients’ survival and globe survival. Br J Ophthalmol. 2009;93(1):28–32.

    CAS  PubMed  Google Scholar 

  27. 27.

    Nevins JR. The Rb/E2F pathway and cancer. Hum Mol Genet. 2001;10(7):699–703.

    CAS  PubMed  Google Scholar 

  28. 28.

    Niya MHK, Tameshkel FS, Panahi M, Salim FB, Monavari SHR, Keyvani H. Human papillomavirus investigation in head and neck squamous cell carcinoma: initial report from the low risk HPV types associations. Asian Pac J Cancer Prev. 2017;18(9):2573.

    PubMed Central  Google Scholar 

  29. 29.

    Nobre RJ, de Almeida LP, Martins TC. Complete genotyping of mucosal human papillomavirus using a restriction fragment length polymorphism analysis and an original typing algorithm. J Clin Virol. 2008;42(1):13–21.

    CAS  PubMed  Google Scholar 

  30. 30.

    Orjuela M, Castaneda VP, Ridaura C, Lecona E, Leal C, Abramson DH, et al. Presence of human papilloma virus in tumor tissue from children with retinoblastoma: an alternative mechanism for tumor development. Clin Cancer Res. 2000;6(10):4010–6.

    CAS  PubMed  Google Scholar 

  31. 31.

    Palazzi MA, Yunes JA, Cardinalli IA, Stangenhaus GP, Brandalise SR, Ferreira SA, et al. Detection of oncogenic human papillomavirus in sporadic retinoblastoma. Acta Ophthalmol Scand. 2003;81(4):396–8.

    CAS  PubMed  Google Scholar 

  32. 32.

    Pizzol D, Putoto G, Chhaganlal KD. Human papillomavirus (HPV) infection: a Mozambique overview. Virusdisease. 2016;27(2):116–22.

    PubMed  PubMed Central  Google Scholar 

  33. 33.

    Ryoo N-K, Kim J-E, Choung H-K, Kim N, Lee M-J, Khwarg S-I. Human papilloma virus in retinoblastoma tissues from Korean patients. Korean J Ophthalmol. 2013;27(5):368–71.

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Sagi M, Frenkel A, Eilat A, Weinberg N, Frenkel S, Peer J, et al. Genetic screening in patients with Retinoblastoma in Israel. Fam Cancer. 2015;14(3):471–80.

    CAS  PubMed  Google Scholar 

  35. 35.

    Sahu S, Banavali S, Pai S, Nair C, Kurkure P, Motwani S, et al. Retinoblastoma: problems and perspectives from India. Pediatr Hematol Oncol. 1998;15(6):501–8.

    CAS  PubMed  Google Scholar 

  36. 36.

    Saktanasate J, Saksiriwutto P, Uiprasertkul M, Horthongkham N, Trinavarat A, Atchaneeyasakul L. Human papillomavirus DNA in paraffin-embedded retinoblastoma. J Med Assoc Thai. 2018;101:229–31.

    Google Scholar 

  37. 37.

    Salehi-Vaziri M, Sadeghi F, Bokharaei-Salim F, Younesi S, Alinaghi S, Monavari SH, et al. The prevalence and genotype distribution of human papillomavirus in the genital tract of males in Iran. Jundishapur J Microbiol. 2015;8(12):e21912.

    PubMed  PubMed Central  Google Scholar 

  38. 38.

    Salehi-Vaziri M, Sadeghi F, Alamsi-Hashiani A, Haeri H, Monavari SH, Keyvani H. Merkel cell polyomavirus and human papillomavirus infections in cervical disease in Iranian women. Adv Virol. 2015;160(5):1181–7.

    CAS  Google Scholar 

  39. 39.

    Salehi-Vaziri M, Sadeghi F, Hashemi FS, Haeri H, Bokharaei-Salim F, Monavari SH, et al. Distribution of human papillomavirus genotypes in Iranian women according to the severity of the cervical lesion. Iran Red Crescent Med J. 2016;18(4):e24458.

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Schmitz M, Driesch C, Jansen L, Runnebaum IB, Dürst M. Non-random integration of the HPV genome in cervical cancer. PLoS ONE. 2012;7(6):e39632.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Shetty OA, Naresh KN, Banavali SD, Shet T, Joshi R, Qureshi S, et al. Evidence for the presence of high risk human papillomavirus in retinoblastoma tissue from nonfamilial retinoblastoma in developing countries. Pediatr Blood Cancer. 2012;58(2):185–90.

    PubMed  Google Scholar 

  42. 42.

    Skoczyński M, Goździcka-Józefiak A, Kwaśniewska A. Risk factors of the vertical transmission of human papilloma virus in newborns from singleton pregnancy—preliminary report. J Matern Fetal Neonatal Med. 2014;27(3):239–42.

    PubMed  Google Scholar 

  43. 43.

    Walter SD, Harbour JW. Molecular biology of retinoblastoma. In: Francis J, Abramson D (editors) Recent advances in retinoblastoma treatment. Essentials in Ophthalmology. Cham: Springer; 2015. pp. 1–13.

    Google Scholar 

  44. 44.

    Yahyapour Y, Shamsi-Shahrabadi M, Mahmoudi M, Motevallian A, Siadati S, Shefaii S, et al. High-risk and low-risk human papillomavirus in esophageal squamous cell carcinoma at Mazandaran, Northern Iran. Pathol Oncol Res. 2013;19(3):385–91.

    CAS  PubMed  Google Scholar 

  45. 45.

    Yun J, Li Y, Xu C-T, Pan B-R. Epidemiology and Rb1 gene of retinoblastoma. Int J Ophthalmol. 2011;4(1):103.

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Maryam Esghaei.

Ethics declarations

Conflict of interest

All the authors have stated to have no conflict of interest to declare.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 45 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Javanmard, D., Moein, M., Esghaei, M. et al. Molecular evidence of human papillomaviruses in the retinoblastoma tumor. VirusDis. 30, 360–366 (2019). https://doi.org/10.1007/s13337-019-00540-7

Download citation

Keywords

  • Retinoblastoma tumor
  • RB
  • Human papillomavirus
  • HPV
  • Iran