Preview

Siberian journal of oncology

Advanced search

MicroRNA, HPV AND CERVICAL CARCINOGENESIS: MOLECULAR ASPECTS AND PROSPECTS OF CLINICAL APPLICATION

https://doi.org/10.21294/1814-4861-2016-15-4-88-97

Abstract

Cervical cancer is one of the most common cancers of the female reproductive system and a leading cause of mortality in women worldwide. Epidemiologic and experimental data have clearly demonstrated a causal role of Human Papillomavirus in cervical carcinogenesis. Determination of HPV DNA of high carcinogenic risk is relevant screening tool to identify patients with an increased risk of cervical neoplasia. However, the positive predictive value of such an analysis is not high enough. Analysis of additional indicators of infection (viral load, the ratio of episomal and integrated forms of the virus, the duration of its persistence) can be used to improve the diagnostic and prognostic value of HPV testing. In the last decade, studies have shown that HPV induces specific changes in miRNA profile of the infected cell, which reflect the phasing of the disease and may have diagnostic / prognostic value. This review summarizes the current understanding of cellular changes in the profile of microRNAs, caused by infection with HPV, given the known examples of microRNA involvement in cervical carcinogenesis and the perspectives of the possible use of microRNAs as biomarkers in the diagnosis of cervical cancer.

About the Authors

P. A. Arkhangelskaya
N.N. Petrov Institute of Oncology, Saint-Petersburg; North-western State Medical University named after I.I. Mechnikov, Saint-Petersburg
Russian Federation
Arkhangelskaya Polina A., postgraduate, Department of Obstetrics and Gynecology


E. V. Bakhidze
N.N. Petrov Institute of Oncology, Saint-Petersburg; North-western State Medical University named after I.I. Mechnikov, Saint-Petersburg
Russian Federation

Bakhidze Elena V., MD, DSc, Leading Researcher, Department of Gynecologic Oncology, N.N. Petrov Institute of Oncology, SaintPetersburg; Associate Professor of the Department of Obstetrics and Gynecology, North-western State Medical University named after I.I. Mechnikov 

SPIN-code: 5191-8792



I. V. Berlev
N.N. Petrov Institute of Oncology, Saint-Petersburg; North-western State Medical University named after I.I. Mechnikov, Saint-Petersburg
Russian Federation
Berlev Igor V., MD, Professor, Head of Gynecology Department, N.N. Petrov Institute of Oncology, Saint-Petersburg; Head of Department of Obstetrics and Gynecology


R. B. Samsonov
N.N. Petrov Institute of Oncology, Saint-Petersburg; Oncosystem ltd., Saint-Petersburg
Russian Federation

Samsonov Roman B., PhD, Researcher, Endocrinology Laboratory 

 



M. K. Ivanov
Vector-Best closed corporation, Novosibirsk
Russian Federation

Ivanov Mikhail K., PhD, Vector-Best closed corporation, Head of Laboratory of Department of Obstetrics and Gynecology 

SPIN-code: 4416-1250



A. V. Malek
N.N. Petrov Institute of Oncology, Saint-Petersburg; Oncosystem ltd., Saint-Petersburg
Russian Federation
Malek Anastasia V., PhD, Senior Researcher, Endocrine Oncology Laboratory


References

1. World Cancer Report 2014 / Stewart B.W., Wild C.P. France: WHO Press, 2014, 630 p.

2. Malignancies in Russia in 2012 (morbidity and mortality) / A.D. Kaprin, V.V. Starinskiy, G.V. Petrova. Moscow; 2014, 250 p. [in Russian]

3. Merabishvili V.M., Lalianci Je I., Subbotina O.Ju. Cervical cancer: morbidity, mortality (population study). Vopr. onkologii, 2014; 60, (3): 288–297. [in Russian]

4. Chen Z., Schiffman M., Herrero R., Desalle R., Anastos K., Segondy M., Sahasrabuddhe V.V., Gravitt P.E., Hsing A.W., Burk R.D. Evolution and taxonomic classification of human papillomavirus 16 (HPV16)-related variant genomes: HPV31, HPV33, HPV35, HPV52, HPV58 and HPV67. PLoS One. 2011; 6 (5): e20183. doi: 10.1371/journal.pone.0020183.

5. Evstigneeva L.A., Bahidze E.V., Semiglazov V.V. The role of virological factors in the development of cervical cancer in young women. Zhurnal akusherstva i zhenskih boleznej. 2007; 7 (5): 153. [in Russian]

6. Kolomiec L.A., Urazova L.N., Sevast'janova N.V., Churuksaeva O.N. Clinical and morphological aspects of cervical human papillomavirus infection. Vopr. Onkologii. 2002; 48 (1): 43–46. [in Russian]

7. Bosch F.X., Burchell A.N., Schiffman M., Giuliano A.R., de Sanjose S., Bruni L., Tortolero-Luna G., Kjaer S.K., Munoz N. Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine. 2008 Aug 19; 26 Suppl 10: K1-16. doi: 10.1016/j.vaccine.2008.05.064.

8. Kiselev V.I., Kiselev O.I. The aetiological role of human papillomavirus in cervical cancer: genetic and pathogenetic mechanisms. Citokiny i vospalenie. 2003; 2 (4): 31–38. [in Russian]

9. Dillner J., Rebolj M., Birembaut Ph., Petry K.U., Szarewski A., Munk C., de Sanjose S., Naucler P., Lloveras B., Kjaer S., Cuzick J., van Ballegooijen M., Clavel C., Iftner T.; Joint European Cohort Study. Long term predictive values of cytology and human papillomavirus testing in cervical cancer screening: joint European cohort study. BMJ. 2008 Oct 13; 337: a1754. doi: 10.1136/bmj.a1754.

10. Kiseleva V.I., Krikunova L.I., Ljubina L.V. Quantitative load of human papillomavirus type 16 and the prediction of the effectiveness of the treatment of cervical cancer. Radiacija i risk. 2011; 20 (2): 58–63. [in Russian]

11. Komarova E.V., Minkna G.N., Gavrikova M.V., Hramova O.K. HPV – esting and genotyping in the diagnosis of cervical intraepithelial neoplasia. Medicina kriticheskih sostojanij. 2010; 1 (1): 54–61. [in Russian]

12. Marks M., Gravitt P.E., Utaipat U., Gupta S.B., Liaw K., Kim E., Tadesse A., Phongnarisorn C., Wootipoom V., Yuenyao P., Vipupinyo C., Rugpao S., Sriplienchan S., Celentano D.D. Kinetics of DNA load predict HPV 16 viral clearance. J Clin Virol. 2011 May;51(1):44-9. doi: 10.1016/j. jcv.2011.01.011.

13. Kolesnikov N.N., Titov S.E., Veriaskina Iu.A., Karpinskaia E.V., Shevchenko S.P., Akhmerova L.G., Ivanov M.K., Kozlov V.V., Elisaphenko E.A., Guliaeva L.F., Zhimulev I.F. [Microrna, evolution and cancer]. Tsitologiia. 2013; 55 (3): 159–164. [in Russian]

14. Di Leva G., Garofalo M., Croce C.M. MicroRNAs in cancer. Annu Rev Pathol. 2014;9:287-314. doi: 10.1146/annurev-pathol-012513104715.

15. Pedroza-Torres A., Lopez-Urrutia E., Garcia-Castillo V., JacoboHerrera N., Herrera L.A., Peralta-Zaragoza O., Lopez-Camarillo C., De Leon D.C., Fernandez-Retana J., Cerna-Cortes J.F., Perez-Plasencia C. MicroRNAs in cervical cancer: evidences for a miRNA profile deregulated by HPV and its impact on radio-resistance. Molecules. 2014 May 16; 19 (5): 6263–81. doi: 10.3390/molecules19056263.

16. Au Yeung C.L., Tsang T.Y., Yau P.L., Kwok T.T. Human papillomavirus type 16 E6 induces cervical cancer cell migration through the p53/ microRNA-23b/urokinase-type plasminogen activator pathway. Oncogene. 2011 May 26; 30 (21): 2401–10. doi: 10.1038/onc.2010.613.

17. Greco D., Kivi N., Qian K., Leivonen S.K., Auvinen P., Auvinen E. Human papillomavirus 16 E5 modulates the expression of host microRNAs. PLoS One. 2011; 6 (7): e21646. doi: 10.1371/journal.pone.0021646.

18. Bernard X., Robinson P., Nomine Y., Masson M., Charbonnier S., Ramirez-Ramos J.R., Deryckere F., Trave G., Orfanoudakis G. Proteasomal degradation of p53 by human papillomavirus E6 oncoprotein relies on the structural integrity of p53 core domain. PLoS One. 2011; 6 (10): e25981. doi: 10.1371/journal.pone.0025981.

19. Nomine Y., Masson M., Charbonnier S., Zanier K., Ristriani T., Deryckere F., Sibler A. P., Desplancq D., Atkinson R. A., Weiss E., Orfanoudakis G., Kieffer B., Trave G. Structural and functional analysis of E6 oncoprotein: insights in the molecular pathways of human papillomavirusmediated pathogenesis. Mol Cell. 2006 Mar 3; 21 (5): 665–78.

20. Wang X., Wang H.K., McCoy J.P., Banerjee N.S., Rader J.S., Broker T.R., Meyers C., Chow L.T., Zheng Z.M. Oncogenic HPV infection interrupts the expression of tumor-suppressive miR-34a through viral oncoprotein E6. RNA. 2009 Apr; 15 (4): 637–47. doi: 10.1261/rna.1442309.

21. Turner M.A., Palefsky J.M. Urokinase plasminogen activator expression by primary and HPV 16-transformed keratinocytes. Clin Exp Metastasis. 1995 Jul; 13 (4): 260–8.

22. Martinez I., Gardiner A.S., Board K.F., Monzon F.A., Edwards R.P., Khan S.A. Human papillomavirus type 16 reduces the expression of microRNA-218 in cervical carcinoma cells. Oncogene. 2008 Apr 17; 27 (18): 2575–82.

23. Myklebust M.P., Bruland O., Fluge O., Skarstein A., Balteskard L., Dahl O. MicroRNA-15b is induced with E2F-controlled genes in HPVrelated cancer. Br J Cancer. 2011 Nov 22; 105 (11): 1719–25. doi: 10.1038/ bjc.2011.457.

24. Yamamoto N., Kinoshita T., Nohata N., Itesako T., Yoshino H., Enokida H., Nakagawa M., Shozu M., Seki N. Tumor suppressive microRNA-218 inhibits cancer cell migration and invasion by targeting focal adhesion pathways in cervical squamous cell carcinoma. Int J Oncol. 2013 May; 42 (5): 1523–32. doi: 10.3892/ijo.2013.1851.

25. Banno K., Iida M., Yanokura M., Kisu I., Iwata T., Tominaga E., Tanaka K., Aoki D. MicroRNA in cervical cancer: OncomiRs and tumor suppressor miRs in diagnosis and treatment. ScientificWorldJournal. 2014 Jan 2; 2014: 178075. doi: 10.1155/2014/178075.

26. Gocze K., Gombos K., Kovacs K., Juhasz K., Gocze P., Kiss I. MicroRNA expressions in HPV-induced cervical dysplasia and cancer. Anticancer Res. 2015 Jan; 35 (1): 523–30.

27. Kogo R., How C., Chaudary N., Bruce J., Shi W., Hill R.P., Zahedi P., Yip K.W., Liu F.F. The microRNA-218~Survivin axis regulates migration, invasion, and lymph node metastasis in cervical cancer. Oncotarget. 2015 Jan 20; 6 (2): 1090–100.

28. Campos-Viguri G.E., Jimenez-Wences H., Peralta-Zaragoza O., Torres-Altamirano G., Soto-Flores D.G., Hernandez-Sotelo D., AlarconRomero Ldel C., Jimenez-Lopez M.A., Illades-Aguiar B., Fernandez-Tilapa G. miR-23b as a potential tumor suppressor and its regulation by DNA methylation in cervical cancer. Infect Agent Cancer. 2015 Nov 30; 10: 42. doi: 10.1186/s13027-015-0037-6.

29. Honegger A., Schilling D., Bastian S., Sponagel J., Kuryshev V., Sultmann H., Scheffner M., Hoppe-Seyler K., Hoppe-Seyler F. Dependence of intracellular and exosomal microRNAs on viral E6/E7 oncogene expression in HPV-positive tumor cells. PLoS Pathog. 2015 Mar 11; 11 (3): e1004712. doi: 10.1371/journal.ppat.1004712.

30. Zheng Z.M., Wang X. Regulation of cellular miRNA expression by human papillomaviruses. Biochim Biophys Acta. 2011 Nov-Dec; 1809 (11–12): 668–77. doi: 10.1016/j.bbagrm.2011.05.005.

31. Ben W., Yang Y., Yuan J., Sun J., Huang M., Zhang D., Zheng J. Human papillomavirus 16 E6 modulates the expression of host microRNAs in cervical cancer. Taiwan J Obstet Gynecol. 2015 Aug; 54 (4): 364–70. doi: 10.1016/j.tjog.2014.06.007.

32. Wang X., Wang H.K., Li Y., Hafner M., Banerjee N.S., Tang S., Briskin D., Meyers C., Chow L.T., Xie X., Tuschl T., Zheng Z.M. microRNAs are biomarkers of oncogenic human papillomavirus infections. Proc Natl Acad Sci USA. 2014 Mar 18; 111 (11): 4262–7. doi: 10.1073/pnas.1401430111.

33. Wang L., Yu J., Xu J., Zheng C., Li X., Du J. The analysis of microRNA-34 family expression in human cancer studies comparing cancer tissues with corresponding pericarcinous tissues. Curr Pharm Des. 2014; 20 (11): 1639–46.

34. Yuan F., Sun R., Chen P., Liang Y., Ni S., Quan Y., Huang J., Zhang L., Gao L. Combined analysis of pri-miR-34b/c rs4938723 and TP53 Arg72Pro with cervical cancer risk. Tumour Biol. 2016 May; 37 (5): 6267–73. doi: 10.1007/s13277-015-4467-y.

35. Chen Y., Ma C., Zhang W., Chen Z., Ma L. Down regulation of miR-143 is related with tumor size, lymph node metastasis and HPV16 infection in cervical squamous cancer. Diagn Pathol. 2014 Apr 28; 9: 88. doi: 10.1186/1746-1596-9-88.

36. Liu L., Wang Y.L., Wang J.F. [Differential expression of miR-21, miR-126, miR-143, miR-373 in normal cervical tissue, cervical cancer tissue and Hela cell]. Sichuan Da Xue Xue Bao Yi Xue Ban. 2012 Jul; 43 (4): 536–9.

37. Yuan W., Xiaoyun H., Haifeng Q., Jing L., Weixu H., Ruofan D., Jinjin Y., Zongji S. MicroRNA-218 enhances the radiosensitivity of human cervical cancer via promoting radiation induced apoptosis. Int J Med Sci. 2014 May 6; 11 (7): 691–6. doi: 10.7150/ijms.8880.

38. Zhu Y.K., Cheng N., Hu Y., Cen Y.Z. The role of microRNAs in the pathogenesis of cervical cancer and its relationship to HPV. Sheng Li Ke Xue Jin Zhan. 2012 Aug; 43 (4): 251–6.

39. Botezatu A., Goia-Rusanu C.D., Iancu I.V., Huica I., Plesa A., Socolov D., Ungureanu C., Anton G. Quantitative analysis of the relationship between microRNA124a, -34b and -203 gene methylation and cervical oncogenesis. Mol Med Rep. 2011 Jan-Feb; 4 (1): 121–8. doi: 10.3892/mmr.2010.394.

40. Seifoleslami M., Khameneie M.K., Mashayekhi F., Sedaghati F., Ziari K., Mansouri K., Safari A. Identification of microRNAs (miR-203/ miR-7) as potential markers for the early detection of lymph node metastases in patients with cervical cancer. Tumour Biol. 2015 Oct 22.

41. Zhu X., Er K., Mao C., Yan Q., Xu H., Zhang Y., Zhu J., Cui F., Zhao W., Shi H. miR-203 suppresses tumor growth and angiogenesis by targeting VEGFA in cervical cancer. Cell Physiol Biochem. 2013; 32 (1): 64–73. doi: 10.1159/000350125.

42. Lee J.W., Choi C.H., Choi J.J., Park Y.A., Kim S.J., Hwang S.Y., Kim W.Y., Kim T.J., Lee J.H., Kim B.G., Bae D.S. Altered MicroRNA expression in cervical carcinomas. Clin Cancer Res. 2008 May 1; 14 (9): 2535–42. doi: 10.1158/1078-0432.CCR-07-1231.

43. You W., Wang Y., Zheng J. Plasma miR-127 and miR-218 Might Serve as Potential Biomarkers for Cervical Cancer. Reprod Sci. 2015 Aug; 22 (8): 1037–41. doi: 10.1177/1933719115570902.

44. Tian Q., Li Y., Wang F., Li Y., Xu J., Shen Y., Ye F., Wang X., Cheng X., Chen Y., Wan X., Lu W., Xie X. MicroRNA detection in cervical exfoliated cells as a triage for human papillomavirus-positive women. J Natl Cancer Inst. 2014 Sep 4; 106 (9). pii: dju241. doi: 10.1093/jnci/dju241.

45. Han Y., Xu G.X., Lu H., Yu D.H., Ren Y., Wang L., Huang X.H., Hou W.J., Wei Z.H., Chen Y.P., Cao Y.G., Zhang R. Dysregulation of miRNA-21 and their potential as biomarkers for the diagnosis of cervical cancer. Int J Clin Exp Pathol. 2015 Jun 1; 8 (6): 7131–9.

46. Shishodia G., Shukla S., Srivastava Y., Masaldan S., Mehta S., Bhambhani S., Sharma S., Mehrotra R., Das B.C., Bharti A.C. Alterations in microRNAs miR-21 and let-7a correlate with aberrant STAT3 signaling and downstream effects during cervical carcinogenesis. Mol Cancer. 2015 Jun 9; 14: 116. doi: 10.1186/s12943-015-0385-2.

47. Leonard S.M., Wei W., Collins S.I., Pereira M., Diyaf A., ConstandinouWilliams C., Young L.S., Roberts S., Woodman C.B. Oncogenic human papillomavirus imposes an instructive pattern of DNA methylation changes which parallel the natural history of cervical HPV infection in young women. Carcinogenesis. 2012 Jul; 33 (7): 1286–93. doi: 10.1093/ carcin/bgs157.

48. Burgers W.A., Blanchon L., Pradhan S., de Launoit Y., Kouzarides T., Fuks F. Viral oncoproteins target the DNA methyltransferases. Oncogene. 2007 Mar 8; 26 (11): 1650–5.

49. Jimenez-Wences H., Peralta-Zaragoza O., Fernandez-Tilapa G. Human papilloma virus, DNA methylation and microRNA expression in cervical cancer (Review). Oncol Rep. 2014 Jun; 31 (6): 2467–76. doi: 10.3892/or.2014.3142.

50. Wilting S.M., van Boerdonk R.A., Henken F.E., Meijer C.J., Diosdado B., Meijer G.A., le Sage C., Agami R., Snijders P.J., Steenbergen R.D. Methylation-mediated silencing and tumour suppressive function of hsa-miR-124 in cervical cancer. Mol Cancer. 2010 Jun 26; 9: 167. doi: 10.1186/1476-4598-9-167.

51. Wang J.T., Ding L., Jiang S.W., Hao J., Zhao W.M., Zhou Q., Yang Z.K., Zhang L. Folate deficiency and aberrant expression of DNA methyltransferase 1 were associated with cervical cancerization. Curr Pharm Des. 2014; 20 (11): 1639–46.

52. Hu Z., Zhu D., Wang W., Li W., Jia W., Zeng X., Ding W., Yu L., Wang X., Wang L., Shen H., Zhang C., Liu H., Liu X., Zhao Y., Fang X., Li S., Chen W., Tang T., Fu A., Wang Z., Chen G., Gao Q., Li S., Xi L., Wang C., Liao S., Ma X., Wu P., Li K., Wang S., Zhou J., Wang J., Xu X., Wang H., Ma D. Genome-wide profiling of HPV integration in cervical cancer identifies clustered genomic hot spots and a potential microhomologymediated integration mechanism. Nat Genet. 2015 Feb;47 (2): 158–63. doi: 10.1038/ng.3178.

53. Calin G.A., Sevignani C., Dumitru C.D., Hyslop T., Noch E., Yendamuri S., Shimizu M., Rattan S., Bullrich F., Negrini M., Croce C.M. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA. 2004 Mar 2; 101 (9): 2999–3004.

54. Wentzensen N., Vinokurova S., von Knebel Doeberitz M. Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Res. 2004 Jun 1; 64 (11): 3878–84.

55. Zubillaga-Guerrero M.I., Alarcon-Romero Ldel C., Illades-Aguiar B., Flores-Alfaro E., Bermudez-Morales V.H., Deas J., Peralta-Zaragoza O. MicroRNA miR-16-1 regulates CCNE1 (cyclin E1) gene expression in human cervical cancer cells. Int J Clin Exp Med. 2015 Sep 15; 8 (9): 15999–6006.

56. Gunasekharan V., Laimins L.A. Human papillomaviruses modulate microRNA 145 expression to directly control genome amplification. J Virol. 2013 May; 87 (10): 6037–43. doi: 10.1128/JVI.00153-13.

57. Tian Q., Li Y., Wang F., Li Y., Xu J., Shen Y., Ye F., Wang X., Cheng X., Chen Y., Wan X., Lu W., Xie X. MicroRNA detection in cervical exfoliated cells as a triage for human papillomavirus-positive women. J Natl Cancer Inst. 2014 Sep 4; 106 (9). pii: dju241. doi: 10.1093/jnci/dju241.

58. Ribeiro J., Marinho-Dias J., Monteiro P., Loureiro J., Baldaque I., Medeiros R., Sousa H. miR-34a and miR-125b Expression in HPV Infection and Cervical Cancer Development Biomed Res Int. 2015; 2015: 304584. doi: 10.1155/2015/304584.

59. He Y., Lin J., Ding Y., Liu G., Luo Y., Huang M., Xu C., Kim T.K., Etheridge A., Lin M., Kong D., Wang K. A systematic study on dysregulated microRNAs in cervical cancer development. Int J Cancer. 2016 Mar 15; 138 (6): 1312–27. doi: 10.1002/ijc.29618.

60. Mo W., Tong C., Zhang Y., Lu H. microRNAs’ differential regulations mediate the progress of Human Papillomavirus (HPV)-induced Cervical Intraepithelial Neoplasia (CIN). BMC Syst Biol. 2015 Feb 7; 9: 4. doi: 10.1186/s12918-015-0145-3.


Review

For citations:


Arkhangelskaya P.A., Bakhidze E.V., Berlev I.V., Samsonov R.B., Ivanov M.K., Malek A.V. MicroRNA, HPV AND CERVICAL CARCINOGENESIS: MOLECULAR ASPECTS AND PROSPECTS OF CLINICAL APPLICATION. Siberian journal of oncology. 2016;15(4):88-97. (In Russ.) https://doi.org/10.21294/1814-4861-2016-15-4-88-97

Views: 1114


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1814-4861 (Print)
ISSN 2312-3168 (Online)