A Possible Role of Human Herpes Viruses Belonging to the Subfamily Alphaherpesvirinae in the Development of Some Cancers
Authors:
Mrázová Veronika; Golais František; Daniel. Búda
Authors‘ workplace:
Katedra Mikrobiológie a virológie, PriF UK, Bratislava
Published in:
Klin Onkol 2018; 31(3): 178-183
Category:
Reviews
doi:
https://doi.org/10.14735/amko2018178
Overview
Seroepidemiological studies suggest that human herpes simplex virus type 1 (HSV-1) and 2 (HSV-2) are linked with several types of cancer; however, they do not appear to play a direct role and are considered to be cofactors. The abilities of HSV-1 and -2 to transform cells in vitro can be demonstrated by suppressing their lytic ability via irradiation with a specific dose of ultraviolet light, photoinactivation in the presence of photosensitizers (e. g., neutral red or methylene blue), and culture under specific conditions. Several mechanisms have been proposed to explain the actions of these viruses. According to the hit-and-run mechanism, viral DNA initiates transformation by interacting with cellular DNA and thereby inducing mutations and epigenetic changes, but is not involved in other stages of neoplastic progression. By contrast, according to the hijacking mechanism, viral products in infected cells can activate signaling pathways and thereby cause uncontrolled proliferation. Such products include RR1PK, an oncoprotein that activates the Ras pathway and is encoded by the HSV-2 gene ICP10. Virus-encoded microRNAs may act as cofactors in tumorigenesis of serous ovarian carcinoma and some prostate tumors. Herpes virus-associated growth factors that facilitate or suppress transformation may play important roles in tumor formation. Finally, there is much evidence that HSV-2 increases the risk of cervical cancer after infection of human papilloma viruses.
Key words:
HSV-1 – HSV-2 – cancer – mechanisms of transformation
This work was supported by APVV 0621-12.
The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE recommendation for biomedical papers.
Submitted: 29. 11. 2016
Accepted: 20. 3. 2018
Sources
1. Roizman B, Whitley RJ. An inquiry into the molecular basis of HSV latency and reactivation. Annu Rev Microbiol 2013; 67 (5): 355–374. doi: 10.1146/annurevmicro-092412-155654.
2. Young LS, Murray PG. Epstein-Barr virus and oncogenesis: from latent genes to tumours. Oncogene 2003; 22 (33): 5108–5512. doi: 10.1038/sj.onc.1206556.
3. Maeda E, Akahane M, Kiryu S et al. Spectrum of EpsteinBarr virus-related diseases: a pictorial review. Jpn J Radiol 2009; 27 (1): 4–19. doi: 10.1007/s11604-008-0291-2.
4. Edelman DC. Human herpesvirus 8 – A novel human pathogen. Virol J 2005; 2: 18 doi: 10.1186/1743-422X-2-7-78.
5. Metgud R, Astekar M, Verma M et al. Role of viruses in oral squamous cell carcinoma. Oncol Rev 2012; 6 (2): e21. doi: 10.4081/oncol./2012.e21.
6. Gupta K, Metgud R. Evidence suggesting involvement of viruses in oral squamous cell carcinoma. [online]. Available from: http: //dx.doi.org/10.1155/2013/622496.
7. Aurelian L, Schumann, B, Marcus RL et al. Antibody to HSV-2 induced tumor specific antigens in serums from patients with cervical carcinoma. Science 1973; 181 (4095): 161–164.
8. Nahmias AJ, Naib ZM, Josey WE et al. Prospective studies of the association of genital herpes simplex infection and cervical anaplasia. Cancer Res 1973; 33 (6): 1491–1497.
9. Sabin AB, Tarro G. Herpes simplex and herpes genitalis viruses in etiology of some human cancers. Proc Natl Acad Sci USA 1973; 70 (11): 3225–3229.
10. Aurelian L. Virions and antigens of herpes virus type 2 in cervical carcinoma. Cancer Res. 1973; 33 (6): 1539–1547.
11. Goldberg RJ, Gravell M. A search for herpes simplex virus type 2 markers in cervical carcinoma. Cancer Res 1976; 36 (2): 795–799.
12. Thankamani V, Kumari TV, Vasudevan DM. Detection of herpes simplex virus type 2 antigen (s) in biopsies from carcinoma of uterine cervix. J Exp Pathol 1985; 2 (2): 123–133.
13. Aurelian L, Standberg JD, Melendez LV et al. Herpes virus type 2 isolated from cervical tumor cells grown in tissue culture. Science 1971; 174 (4010): 704–707.
14. Li S, Wen X. Seropositivity to herpes simplex virus type 2, but not to type 1 is associated with cervical cancer: NHANES (1999–2014). BMC Cancer 2017; 17 (1): 726. doi: 10.1186s12885-017-3734-2.
15. Koanga MML, Ngono NA, Ngawa G et al. Association of cervical inflammation and cervical abnormalities in women infected with herpes simplex virus 2 (HSV2). Int J Trop Public Health 2014; 4 (1): 10–14.
16. Tomkins A, White C, Higgins SP. Primary herpes simplex virus infection mimicking cervical cancer. BMJ Case Reports 2015; 2015. pii: bcr2015210194. doi: 10.1136/bcr-2015-210194.
17. Vonka V, Kanka J, Hirsch I et al. Prospective study on the relationship betwen cervical neoplasia and herpes simplex type 2 virus. II. Herpes simplex type 2 antibody presence in sera taken at enrollment. Int J Cancer 1984; 33 (1): 61–66.
18. Lehtinen M, Koskela P, Jellum E et al. Herpes simplex virus and risk of cervical cancer: A longitudinal, nested case-control study in the nordic countries. Am J Epidemiol 2002; 156 (8): 687–692.
19. Bosch FX, Lorincz A, Munoz N et al. The casual relation between human papillomavirus and cervical cancer. J Clin Pathol 2002; 55 (4): 244–265.
20. Burd EM Human papillomavirus and cervical cancerr. Clin Microbiol Rev 2003; 16 (1): 1–17.
21. Váňová B, Golais F. Onkogénny potenciál papilómavírusov. Klin Onkol 2013; 26 (6): 399–403.
22. Smith JS, Herrero R, Bosetti C et al. Herpes simplex virus-2 as a human papillomavirus cofactor in the etiology of invasive cervical cancer. J Natl Cancer Inst 2002; 94 (21): 1604–1613.
23. Szostek S, Zawilinska B, Kopec J et al. Herpesviruses as possible cofactors in HPV-16 related oncogenesis. Acta Biochim Pol 2009; 56 (2): 337–342.
24. Zhao Y, Cao X, Zheng Y et al. Relationship betwen cervical disease and infection with human papillomavirus types 16 and 18, and herpes simplex virus 1 and 2. J Med Virol 2012; 84 (12): 1920–1927. doi: 10.1002/jmv.23353.
25. Weismanová E, Weismann P. HPV a krčok maternice: Genetická podstata malígnej transformácie bunky. Onkológia; 2008; 3 (6): 389–392.
26. Ortoski RA, Kell CS. Anal cancer and screening guidelines for human papillomavirus in men. J Am Osteopath Ass 2011; 111 (3 suppl 2): S35–S43.
27. Raju K. Virus and cervical cancer: Role and implication: A review. Biomed Res Ther 2015; 2 (3): 220–230. doi: 10.7603/s40730-015-0007-z.
28. Parker TM, Smith EM, Ritchie JM et al. Head and neck cancer associated with herpes simplex virus 1 and 2 and other risk factors. Oral Oncol 2006; 42 (3): 288–296. doi: 10.1016/j.oraloncology.2005.08.003.
29. Shillitoe EJ, Silverman S. Oral cancer and herpes simplex virus – a review. Oral Surg Oral Med Oral Pathol 1979; 48 (3): 216–224.
30. Vijayakumar T, Kumari TV, Vasudevan DM et al. Demonstration of HSV-1 antigen in patients with orea cancer by immunofluorescence and immunoperoxidase techniques. J Exp Pathol 1987; 3 (1): 75–86.
31. Steele C, Shillitoe EJ. Viruses and oral cancer. Crit Rev Oral Biol Med 1991; 2 (2): 153–175.
32. Star JR, Daling JR, Fitzgibbons ED et al. Serologic evidence of herpes simplex virus 1 infection and oropharyngeal cancer risk. Cancer Res 2001; 61 (23): 8459–8464.
33. Jain M. Assesment of correlation of herpes simplex virus-1 with oral cancer and precancer – A comparative study. J Clin Diagn Res 2016; 10 (8): 14–17. doi: 10.7860/JCDR/2016/18593.8229.
34. Osman AH, Enan KA, Mohamed EA. Molecular detection of herpes simplex virus (1,2) in oral squamous cell carcinoma at Khartom. Clin Med J 2017; 3 (2): 10–14.
35. Lowenthal BM, Lin GY. Herpes simplex virus positive, human papillomavirus negative laryngeal squamous cell carcinoma presenting in an immunocompetent male with dysphonia. Hum Pathol 2017; 10: 50–51. doi: 10.1016/j.ehpc.2017.06.001.
36. Devillers-Mendoza DD, Chang JV. Cytopathologic herpes simplex virus features in laryngeal squamous cell carcinoma. Philipp J Otolaryngol Head Nech Surg 2016; 31 (1): 61–64.
37. Turunen A, Hukkanen V, Kulmala J et al. HSV-1 infection modulates the radioresponse of a HPV16 positive head and neck cancer cell line. Anticancer Res 2016; 36 (2): 565–574.
38. Jensen K, Patel A, Hoperia V et al. Human herpes simplex viruses in benign and malignant thyroid tumours. J Pathol 2010; 221 (2): 193–200. doi: 10.1002/path.2701.
39. Stamatiou DP, Derdas SP, Zoras OL et al. Herpes and polyoma family viruses in thyroid cancer. Oncol Lett 2016; 11 (3): 1635–1644. doi: 10.3892/ol.2016.4144.
40. Kofman A, Marcinkiewicz L, Dupart E et al. The roles of viruses in brain tumorinitiation and oncomodulation. J Neurooncol 2011; 105 (3): 451–466. doi: 10.1007/s11060-011-0658-6.
41. Thomas F, Elguero E, Brodeur J et al. Herpes simplex virus type 2 and cancer: A medical geography approach. Int Genet Evol 2011; 11 (6): 1239–1242. doi: 10.1016/j.meegid.2011.04.009.
42. Ypiranga S, de Moraes AM. Prevalence of human herpes virus type 1 in epithelial skin cancer. An Bras Dermatol 2009; 84 (2): 137–142.
43. Modrow S, Falke D, Truyen U (eds). Molekulare Virologie. 3. vydání. Heidelberg: Spektrum Akademischer Verlag 2010: 45–52.
44. Freshney RI. Culture of animal cells: A manual basic technique and specialized applications. 6th edition. Hoboken, New Jersey: John Wiley & Sons 2011: 279–297.
45. Duff R, Rapp F. Properties of hamster embryo fibroblasts transformed in vitro after exposure to ultraviolet-irradiated herpes simplex virus type 2. J Virol 1971; 8 (4): 469–477.
46. Rapp F, Duff R. Transformation of hamster embryo fibroblasts by herpes simplex viruses type 1 and 2. Cancer Res 1973; 33 (6): 1527–1534.
47. Boyd AL, Orme TW. Transformation of mouse cells after infection with ultraviolet irradioation-inactivated herpes simplex virus type 2. Int J Cancer 1975; 16 (4): 526–538.
48. Rapp F, Reed C. Experimental evidence for the oncogenic potential of herpes simplex vius. Cancer Res 1976; 36 (2): 800–806.
49. Simas JP, Efstathiou S. Murine gammaherpesvirus 68: a model for the study of gammaherpesvirus pathogenesis. Trends Microbiol 1998; 6 (7): 276–282.
50. Mistríková, FJ, Rašlová H, Mrmusová M et al. A murine gammaherpesvirus. Acta virol 2000; 44 (3): 211–226.
51. Nash AA, Dutia BM, Stewart JP et al. Natural history of murine gammaherpesvirus infection. Phil Trans R Soc Lond B Biol Sci 2001; 356 (1408): 569–579. doi: 10.1098/rstb.2000.0779.
52. Mrázová V. Betáková T, Kudelová M et al. Murine gammaherpesvirus (MHV-68) transforms cultured cells in vitro. Intervirology 2015; 58 (2): 69–72. doi: 10.1159/000370 071.
53. Li JL, Jerkofsky MA, Rapp F. Demonstration of oncogenic potential of mammalian cells by DNA-containing viruses following photodynamic inactivation. Int J Cancer 1975; 15 (2): 190–202.
54. Kucera LS, Gusdon JP, Edwards I et al. Oncogenic transformation of rat embryo fibroblasts with photoinactivated herpes simplex virus: rapid in vitro cloning of transformed cells. J Gen Virol 1977; 35 (3): 473–485. doi: 10.1099/0022-1317-35-3-473.
55. Yen GSL, Simon EH. Photosensitization of herpes simplex virus type 1 with neutral red. J Gen Virol 1978; 41 (2): 273–281.
56. Takahashi M, Yamanishi K. Transformation of hamster embryo and human embryo cells by temperature sensitive mutants of herpes simplex virus type 2. Virology 1974; 61 (1): 306–311.
57. Darai G, Braun R, Flügel RM et al. Malignant transformation of rat embryo fibroblasts by herpes simplex virus types 1 and 2 at suboptimal temperature. Nature 1997; 265 (5596): 744–746.
58. Wentz WB, Reagan JV, Heggle AD et al. Induction of uterine cancer with inactivated herpes simplex virus types 1 and 2. Cancer 1981; 48 (8): 1787–1790.
59. Anthony DD, Wentz WB, Reagan JW et al. Induction of cervical neoplasia in the mouse by herpes simplex virus type 2 DNA. Proc Natl Acad Sci USA 1989; 86 (12): 4520–4524.
60. Skinner GR. Transformation of primary hamster fibroblasts by type 2 herpes simplex virus: evidence for a „hit and run“ mechanism. Br J Exp Path 1976; 57 (4): 361–376.
61. Galloway DA, McDoughall JK. The onbcogenic potential of herpes simplex viruses: evidence for a „hit-and-run“ mechanism. Nature 1983; 302 (5903): 21–24.
62. McDoughall JK. „Hit and run“ transformation leading to carcinogenesis. Dev Biol (Basel) 2001; 106: 77–82.
63. Stevenson PG, May JS, Connor V et al. Vaccination against a „hit and run“ viral cancer. J Gen Virol 2010; 91 (9): 2176–2185. doi: 10.1099/vir.0.023507-0.
64. Galloway DA, Copple CD, McDoughall JK. Analysis of viral DNA sequences in hamster cells transformed by herpes simplex virus type 2. Proc Natl Acad Sci USA 1980; 77 (2): 880–884.
65. Reyes GR, LaFemina R, Hayward SD et al. Morphological transformation by DNA fragment of human herpesviruses: Evidence for two distinct transforming regions in herpes simplex viruses types 1 and 2 and lack of correlation with biochemical transformation of the thymidine kinase gene. Cold Spring HarbSymp Quant Biol 1980; 44 (1): 629–641.
66. Galloway DA, Nelson JA, McDoughall JK. Small fragments of herpesvirus DNA with transforming activity contain insertion sequence-like structures. Proc Natl Acad Sci USA 1984; 81 (15): 4736–4740.
67. Hayashi Y, Iwasaka T, Smith CC et al. Multistep transformation by defined fragments of herpes simplex virus type 2 DNA: oncogenic region and its gene products. Proc Natl Acad Sci USA 1985; 82 (24): 8493–8497.
68. Cameron IR, Park M, Dutia BM et al. Herpes simplex virus sequences involved in the intiation of oncogenic morphological transformation of rat cells are not required for maintenance of the transformed state. J Gen Virol 1985; 66 (3): 517–527. doi: 10.1099/0022-1317-66-3-517.
69. Bauer G, Kahl S, Sawhney IS et al. Transformation of rodent fibroblasts by herpes simplex virus: Presence of morphological transforming region 1 (MTR1) is not required for the maintenance of the transformed state. Int J Cancer 1992; 51 (5): 754–760.
70. Niller HH, Wolf H, Minarovits J. Viral hit and run-oncogenesis: Genetic and epigenetic scenarios. Cancer Lett 2011; 305 (2): 200–217. doi: 10.1016/j.canlet.2010.08.007.
71. Filippakis H, Spandidos DA, Sourvinos G. Herpesviruses: Hijacking the Ras signaling pathway. Biochim Biophys Acta 2010; 1803 (7): 777–785. doi: 10.1016/j.bbamcr.2010.03.007.
72. Spandidodos DA, Sourvinos G, Tsatsanis C et al. Normal ras genes: their onco-suppressor and pro-apoptotic functions (review). Int J Oncol 2002; 21 (2): 237–241.
73. Smith CC, Kulka M, Wymer JP et al. Expression of the large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) is required for virus growth and neoplastic transformation. J Gen Virol 1992; 73 (6): 1417–1428. doi: 10.1099/0022-1317-73-6-1417
74. Smith CC, Aurelian L. The large subunit of herpes simplex virus type 2 ribonucleotide reductase (ICP10) is associated with the virion tegument and has PK activity. Virology 1997; 234 (2): 235–242.
75. Aurelian L. Herpes simplex virus type 2: unique biological properties include neoplastic potential mediated by the PK domain of the large subunit of ribonucleotide reductase. Front Biosci 1998; 3: 237–249.
76. Perkins D, Pereira EF, Aurelian L. The herpes simplex virus type 2 R1 protein kinase (ICP10PK) functions as a dominant regulator of apoptosis in hippocampal neurons involving activation of the ERK survival pathway and upregulation of the antiapoptic protein Bag-1. J Virol 2003; 77 (2): 1292–1305.
77. Smith CC. The herpes simplex virus type 2 protein ICP10PK: a master of versatility. Front Biosci 2005; 10: 2820–2831.
78. Aurelian L, Kessler II, Rosenhein NB et al. Viruses and gynecologic cancers: herpesvirus protein (ICP10/AG-4). a cervical tummor antigen that fulfills the criteria for a marker of cancerogenity. Cancer 1981; 48 (Suppl 2): 455–471.
79. Aurelian L, Smith CC, Klacsman KT et al. Expression and cellularcompartmentalizatio of a herpes simplex type 2 protein (ICP10) in productively infected and cervical tumor cells. Cancer Invest 1983; 1 (4): 301–313.
80. Iwasaka T, Smith C, Aurelian L et al. The cervical tumor-associated antigen (ICP10/AG4) is encoded by the transforming region of the genome of herpes simplex virus type 2. Jpn J Canc Res 1985; 76 (10): 946–958.
81. Smith CC, Yu YX, Kulka M et al. A novel human gene similar to the protein kinase (PK) coding domain of the large subunit of herpes simplex virus type 2 ribonucleitide reductase (ICP10) codes for a serine-threonine PK and is expressed in melanoma cells. J Biol Chem 2000; 275 (33): 25690–25699. doi: 10.1074/jbc.M002140 200.
82. Sze P, Herman RC. The herpes simplex virus type 1 ICP6 gene is regulated by a „leaky“ early promoter. Virus Res 1992; 26 (2): 141–152.
83. Matis J, Kúdelová M. Early shutoff of host protein synthesis in cells infected with herpes simplex viruses. Acta virol 2001; 45 (5–6): 269–277.
84. LaThangue NB, Latchman DS. A cellular protein related to heat-shock protein 90 accumulated during virus infection and is everexpressed in transformed cells. Exp Cell Res 1988; 178 (1): 169–179.
85. Mackowiak PA, Goggans ML, Raese J et al. Heat-shock protein induction by herpes simplex virus type 1 in MD canine kidney cells. J Therm Biol 1992; 17 (3): 169–174. doi: 10.1016/0306-4565 (92) 90029-F.
86. Galvan V, Roizman B. Herpes simplex virus 1 induces and blocks apoptosis at multiple steps during infection and protects cells from exogenous inducers in a cell-type-dependent manner. Proc Natl Acad Sci USA 1998; 95 (7): 3931–3936.
87. Nguyen ML, Blaho AJ. Apoptosis during herpes simplex virus infection. Adv Virus Res 2007; 69: 67–97. doi: 10.1016/S0065-3527 (06) 69002-7.
88. Nunes-Alves C. Viral pathogenesis: HSV avoids the RIPper. Nature Rev Microbiol 2015; 13 (4): 185–189. doi: 10.1038/nrmicro3453.
89. Pfeffer S, Voinnet O. Viruses, microRNAs and cancer. Oncogene 2006; 25 (46): 6211–6219. doi: 10.1038/sj.onc.1209915.
90. Friedman JM, Jones PA. MicroRNAs: critical mediators of differentiation, development and disease. Swiss Med Wkly 2009; 139 (33–34): 466–472. doi: smw-12794.
91. Zhuo Y, Gao G, Shi JA et al. MiRNAs, biogenesis, origin and evolution, functions on virus-host interaction. Cell Physiol Biochem 2013; 32 (3): 499–510. doi: 10.1159/000354455.
92. Grundhoff A, Sullivan CS. Virus-encoded microRNAs. Virology 2011; 411 (2): 325–343. doi: 10.1016/j.virol.2011.01.002.
93. Boss IW, Plaisance KB, Renner R. Role of virus-encoded microRNAs in herpesvirus biology. Trends of Microbiol 2009; 17 (12): 544–553. doi: 10.1016/j.tim.2009.09.002.
94. Sun L, Li Q. The microRNAs of Herpes simplex virus (HSV). Virol Sin 2012; 27 (6): 332–337.
95. Umbach JL, Kramer MF, Jurak I et al. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 2008; 454 (7205): 780–783. doi: 10.1038/nature07103.
96. Grey F. Role of microRNAs in herpesvirus latency and persistence. J Gen Virol 2015; 96 (4): 739–751. doi: 10.1099/vir.0.070862-0.
97. Feldman ER, Tibbetts SA. Emerging roles of herpesvirus microRNAs during in vivo infection and pathogenesis. Curr Pathobiol Rep 2015; 3 (3): 209–217. doi: 10.1007/s40139-015-0085-z.
98. Pandya D, Mariani M, McHugh M et al. Herpes simplex virus microRNA expression and significance in serous ovarian cancer. PLoS One 2014; 9 (12): e114750. doi: 10.1371/journal.pone.0114750.
99. Yun SJ, Jeong P, Kang HW et al. Urinary microRNAs of prostate cancer: virus-encoded hsv1-miR-H18 and hsv2-miR-H9-5p could be valuable diagnostic markers. Int Neurourol J 2015; 19 (2): 74–84. doi: 10.5213/inj.2015.19.2.74.
100. Yun SJ, Jeong P, Kang HW et al. Increased expression of herpes-virus-encoded hsv1-miR-H18 and hsv2-miR-H9-5p in cancer-containing prostate tissue compared to that in benign prostate hyperplasia tissue. Int Neurol J 2016; 20 (2): 122–130. doi: 10.5213/inj.1632552. 276.
101. Wang X, Lin S, Zhou Z et al. A herpes simplex virus type 2-encoded microRNA promotes cell metastasis by targeting supressor of cytokine signaling 2 in lung cancer. Tumour Biol 2017; 39 (5): 1010428317701633. doi: 10.1177/1010428317701633.
102. Golais F, Sabó A, Bačíková D. Transforming activity of crude extract of pseudorabies virus-transformed cells. Acta virol 1988; 32 (1): 83–85.
103. Golais F, Csabayová M, Leško J et al. Herpes simplex virus type 2 and pseudorabies virus associated growth factors and their role in the latency invitro. Acta virol 1992; 36 (6): 505–515.
104. Golais F, Košťál M, Csabayová M et al. The glycoprotein B gene and its syn3 locus of herpes simplex virus type 1 are involved in the synthesis of virus-associated growth factor (HSGF-1). Acta virol 1992; 36 (6): 516–523.
105. Konvalina I, Gašperík J, Golais F. A novel class of growth factors related to herpesviruses. Acta vet 2002; 71 (1): 29–36.
106. Šupolíková M, Vojs Staňová A, Kudelová M et al. Cells transformed by murine herpresvirus 68 (MHV-68) release compound with transforming and transformed phenotype repressing activity resembling growth factors. Acta virol 2015; 59 (4): 418–422.
107. Haverkos H, Rohrer M, Pickworth W. The cause of invasive cervical cancer could be multifactorial. Biomed Pharmacother 2000; 54 (1): 54–59.
108. Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 2010; 10 (8): 550–560. doi: 10.1038/nrc2886.
109. Burd EM. Human papillomavirus and cervical cancer. Clin Microbiol Rev 2003; 16 (1): 1–17.
Labels
Paediatric clinical oncology Surgery Clinical oncologyArticle was published in
Clinical Oncology
2018 Issue 3
Most read in this issue
- Potential of the Flavonoid Quercetin to Prevent and Treat Cancer – Current Status of Research
- Histopathology of Neuroendocrine Neoplasms of the Gastrointestinal System
- Resection of Abdominal, Pelvic and Retroperitoneal Tumors
- A Possible Role of Human Herpes Viruses Belonging to the Subfamily Alphaherpesvirinae in the Development of Some Cancers