Advertisement

Molecular evidence of human papillomaviruses in the retinoblastoma tumor

  • Davod Javanmard
  • Masood Moein
  • Maryam EsghaeiEmail author
  • Masood Naseripour
  • Seyed Hamidreza Monavari
  • Farah Bokharaei‐Salim
  • Alireza Sadeghipour
Original Article

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.

Keywords

Retinoblastoma tumor RB Human papillomavirus HPV Iran 

Notes

Compliance with ethical standards

Conflict of interest

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

Supplementary material

13337_2019_540_MOESM1_ESM.doc (46 kb)
Supplementary material 1 (DOC 45 kb)

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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
  11. 11.
    Di Girolamo N. Association of human papilloma virus with pterygia and ocular-surface squamous neoplasia. Eye. 2011;26:202.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.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.CrossRefGoogle 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.CrossRefGoogle Scholar
  27. 27.
    Nevins JR. The Rb/E2F pathway and cancer. Hum Mol Genet. 2001;10(7):699–703.CrossRefGoogle 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.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.CrossRefGoogle 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.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.CrossRefGoogle Scholar
  32. 32.
    Pizzol D, Putoto G, Chhaganlal KD. Human papillomavirus (HPV) infection: a Mozambique overview. Virusdisease. 2016;27(2):116–22.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.Google Scholar

Copyright information

© Indian Virological Society 2019

Authors and Affiliations

  • Davod Javanmard
    • 1
  • Masood Moein
    • 1
  • Maryam Esghaei
    • 1
    Email author
  • Masood Naseripour
    • 2
  • Seyed Hamidreza Monavari
    • 1
  • Farah Bokharaei‐Salim
    • 1
    • 3
  • Alireza Sadeghipour
    • 4
  1. 1.Department of VirologyIran University of Medical SciencesTehranIran
  2. 2.Eye Research Center, Rassoul Akram HospitalIran University of Medical SciencesTehranIran
  3. 3.HIV Laboratory of National Center, Deputy of HealthIran University of Medical SciencesTehranIran
  4. 4.Department of Pathology, Rassoul Akram HospitalIran University of Medical SciencesTehranIran

Personalised recommendations