Immunohistochemical Expression of WT1 in Nasopharyngeal Carcinoma Among Filipino Patients in a Tertiary Hospital
DOI:
https://doi.org/10.21141/PJP.2019.05Keywords:
nasopharyngeal cancer, Wilms’ tumor, WT1, immunohistochemistry, immunotherapyAbstract
Background. Nasopharyngeal carcinoma (NPC) is endemic in Southeast Asia and the Philippines. Novel treatments are desirable due to the high disease burden and adverse effects of existing modalities. Detection of WT1 expression via immunohistochemistry has been reported in many tumors. Moreover, immunotherapy via WT1 peptide vaccination has shown promising results in a wide range of malignancies. No studies on WT1 expression in NPC have been published in any population.
Objective. Documenting WT1 expression in NPC via immunohistochemistry may provide insight into the possibility of using WT1 vaccination for this disease.
Methodology. This was a retrospective descriptive study. All newly-diagnosed cases of NPC from 2016 to 2017 with samples stored in the Department of Laboratories of the Philippine General Hospital were considered. Cases were included based on specific criteria. The tumor classification of each case was reviewed and WT1 immunohistochemistry staining was performed. Assessment of the strength of WT1 immunostaining was conducted. The results were analyzed using Chi-square test for association with fisher exact correction.
Results. A total of 57 cases were included, all of which were non-keratinizing squamous cell carcinomas (NK-SCCs). Forty-nine were undifferentiated type while eight were differentiated type. The mean age was 48 years. Two thirds were male, one third were female. Seventeen of the 57 cases (29.8%) were positive for WT1 immunostaining, and all were undifferentiated type. The majority (82.32%) of the positive cases showed cytoplasmic expression. There was a significant association between tumor classification and WT1 staining.
Conclusion. Similar to studies conducted in other carcinomas, a considerable subset of NPCs express WT1. This finding opens other avenues for exploration, including the feasibility of WT1 peptide vaccination as a treatment option. Further studies on the associations between WT1 and NPC are recommended.
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References
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7. Gong J, Chehrazi-Raffle A, Reddi S, Salgia R. Development of PD-1 and PD-L1 inhibitors as a form of cancer immunotherapy: a comprehensive review of registration trials and future considerations. J Immunother Cancer. 2018;6(1):8. https://pubmed.ncbi.nlm.nih.gov/29357948. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5778665. https://doi.org/10.1186/s40425-018-0316-z.
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9. Hsu C, Lee SH, Ejadi S, et al. Safety and antitumor activity of pembrolizumab in patients with programmed-death-ligand 1-positive nasopharyngeal carcinoma: results of the KEYNOTE-028 study. J Clin Oncol 2017;35(36):4050-6. https://pubmed.ncbi.nlm.nih.gov/28837405. https://doi.org/10.1200/JCO.2017.73.3675.
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11. Di Stasi A, Jimenez AM, Minagawa K, Al-obaidi M, Rezvani K. Review of the results of WT1 peptide vaccination strategies for myelodysplastic syndromes and acute myeloid leukemia from nine different studies. Front Immunol. 2015;6:36. https://pubmed.ncbi.nlm.nih.gov/25699052. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4316779. https://doi.org/10.3389/fimmu.2015.00036.
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13. Carpentieri DF, Nichols K, Chou PM, Matthews M, Pawel B, Huff D. The expression of WT1 in the differentiation of rhabdomyosarcoma from other pediatric small round blue cell tumors. Mod Pathol. 2002;15(10):1080-6. https://pubmed.ncbi.nlm.nih.gov/12379755. https://doi.org/10.1097/01.MP.0000028646.03760.6B.
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15. Cheever MA, Allison JP, Ferris AS, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res. 2009;15(17):5323-17. https://pubmed.ncbi.nlm.nih.gov/19723653. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5779623. https://doi.org/10.1158/1078-0432.CCR-09-0737.
16. Kumar V, Abbas A, Aster J. Robbins and Cotran pathologic basis of disease, 9th ed. Philadelphia, PA: Elsevier/Saunders, 2015.
17. Call KM, Glaser T, Ito CY, et al Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms’ tumor locus. Cell. 1990;50(3):509-20. https://pubmed.ncbi.nlm.nih.gov/2154335.
18. Yang L, Han Y, Suarez Saiz F, Minden MD. A tumor suppressor and oncogene: the WT1 story. Leukemia. 2007;21(5)868-76. https://pubmed.ncbi.nlm.nih.gov/17361230. https://doi.org/10.1038/sj.leu.2404624.
19. Leader R, Deol-Poonia RK, Sheard J, Triantafyllou A. Immunohistochemical localization of WT1 in epithelial salivary tumors. Pathol Res Pract. 2014;210(11):726-32. https://pubmed.ncbi.nlm.nih.gov/25086675. https://doi.org/0.1016/j.prp.2014.06.029.
20. Al-Adnani M, Williams S, Anderson J, Ashworth M, Malone M, Sebire NJ. Immunohistochemical nuclear positivity for WT1 in childhood acute myeloid leukemia. Fetal Pediatr Pathol. 2007;26(4):193-7. https://pubmed.ncbi.nlm.nih.gov/18075834. https://doi.org/10.1080/15513810701696957.
21. Oji Y, Miyoshi S, Maeda H, et al. Overexpression of the Wilms' tumor gene WT1 in de novo lung cancers. Int J Cancer. 2002;100(3):297-303. https://pubmed.ncbi.nlm.nih.gov/12115544. https://doi.org/10.1002/ijc.10476.
22. Kim A, Park EY, Kim K, et al. Prognostic significance of WT1 expression in soft tissue sarcoma. World J Surg Oncol. 2014;12:214. https://pubmed.ncbi.nlm.nih.gov/25026998. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4114094. https://doi.org/10.1186/1477-7819-12-214.
23. Magro G, Salvatorelli L, Puzzo L, Musumeci G, Bisceglia M, Parenti R. Oncofetal expression of Wilms’ tumor 1 (WT1) protein in human fetal, adult and neoplastic skeletal muscle tissues. Acta Histochem. 2015;117(4-5):492-504. https://pubmed.ncbi.nlm.nih.gov/25800978. https://doi.org/10.1016/j.acthis.2015.02.012.
24. Ueda T, Oji Y, Naka N, et al Overexpression of the Wilms' tumor gene WT1 in human bone and soft-tissue sarcomas. Cancer Sci. 2003;94(3):271-6. https://pubmed.ncbi.nlm.nih.gov/12824921. https://doi.org/10.1111/j.1349-7006.2003.tb01432.x.
25. Oji Y, Suzuki T, Nakano Y, et al. Overexpression of the Wilms' tumor gene WT1 in primary astrocytic tumors. Cancer Sci. 2004;95(10):822-7. https://pubmed.ncbi.nlm.nih.gov/15504250. https://doi.org/10.1111/j.1349-7006.2004.tb02188.x.
26. Niksic M, Slight J, Sanford JR, Caceres JF, Hastie ND. The Wilms’
tumour protein (WT1) shuttles between nucleus and cytoplasm and is present in functional polysomes. Hum Mol Genet. 2004;13(4):463-71. https://pubmed.ncbi.nlm.nih.gov/14681305. https://doi.org/10.1093/hmg/ddh040.
27. Waldstrøm M, Grove A. Immunohistochemical expression of Wilms tumor gene protein in different histologic subtypes of ovarian carcinomas. Arch Pathol Lab Med. 2005;129(1):85-8. https://pubmed.ncbi.nlm.nih.gov/15628914.
28. Foster MR, Johnson JE, Olson SJ, Allred DC. Immunohistochemical analysis of nuclear versus cytoplasmic staining of WT1 in malignant mesotheliomas and primary pulmonary adenocarcinomas. Arch Pathol Lab Med. 2001;125(10)1316-20. https://pubmed.ncbi.nlm.nih.gov/11570906.
29. Ye Y, Raychaudhuri B, Gurney A, Campbell CE, Williams BR. Regulation of WT1 by phosphorylation: inhibition of DNA binding, alteration of transcriptional activity and cellular translocation. EMBO J. 1996;15(20):5606-15. https://pubmed.ncbi.nlm.nih.gov/8896454. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC452305.
30. Oji Y, Yamamoto H, Nomura M, et al. Overexpression of the Wilms’ tumor gene WT1 in colorectal adenocarcinoma. Cancer Sci. 2003;94(8):712-7. https://pubmed.ncbi.nlm.nih.gov/12901797. https://doi.org/10.1111/j.1349-7006.2003.tb01507.x.
31. Mikami T, Hada T, Chosa N, Ishisaki A, Mizuki H, Takeda Y. Expression of Wilms’ tumor 1 (WT1) in oral squamous cell carcinoma. J Oral Pathol Med. 2013;42(2):133-9. https://pubmed.ncbi.nlm.nih.gov/22672247. https://doi.org/10.1111/j.1600-0714.2012.01182.x.
32. Li X, Ottosson S, Wang S, et al. Wilms’ tumor gene 1 regulates p63 and promotes cell proliferation in squamous cell carcinoma of the head and neck. BMC Cancer. 2015;15:342. https://pubmed.ncbi.nlm.nih.gov/25929687. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4421988. https://doi.org/10.1186/s12885-015-1356-0.
33. Lee A, Lydiatt W, Colevas A, et al. Nasopharynx. In: Amin MB, et al. (eds). AJCC cancer staging manual. 8th ed., 2017.
34. Oji Y, Inohara H, Nakazawa M. Overexpression of the Wilms' tumor gene WT1 in head and neck squamous cell carcinoma. Cancer Sci. 2003;94(6):523-9. https://pubmed.ncbi.nlm.nih.gov/12824878. https://doi.org/10.1111/j.1349-7006.2003.tb01477.x.
35. Fattahi S, Rahmani SZ, Vosoughhosseini S, Rahmani SP. Configuring the expression of Wilms’ tumor 1 in oral squamous cell carcinoma and its relationship with clinicopathologic features. J Dent App. 2016;3(4):349-52.
36. Ohno S, Okuyama R, Aruga A, Sugiyama H, Yamamoto M. Phase I trial of Wilms’ tumor 1 (WT1) peptide vaccine with GM-CSF or CpG in patients with solid malignancy. Anticancer Res. 2012;32(6):2263-9. https://pubmed.ncbi.nlm.nih.gov/22641661.
37. Oka Y, Tsuboi A, Nakata J, et al. Wilms' tumor gene 1 (WT1) peptide vaccine therapy for hematological malignancies: from CTL epitope identification to recent progress in clinical studies including a cure-oriented strategy. Oncol Res Treat. 2017; 40(11):682-90. https://pubmed.ncbi.nlm.nih.gov/29041012. https://doi.org/10.1159/000481353.
38. Nishida S, Ishikawa T, Egawa S, et al. Combination gemcitabine and WT1 peptide vaccination improves progression-free survival in advanced pancreatic ductal adenocarcinoma: a phase II randomized study. Cancer Immunol Res. 2018;6(3):320-21. https://pubmed.ncbi.nlm.nih.gov/29358173. https://doi.org/10.1158/2326-6066.CIR-17-0386.
39. Qi XW, Zhang F, Wu H, et al. Wilms’ tumor 1 (WT1) expression and prognosis in solid cancer patients: a systematic review and meta-analysis. Sci Rep. 2015;5:8924. https://pubmed.ncbi.nlm.nih.gov/25748047. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4352850. https://doi.org/10.1038/srep08924.
40. Hu C, Wei W, Chen X, et al. A global view of the oncogenic landscape in nasopharyngeal carcinoma: an integrated analysis at the genetic and expression levels. PLoS ONE. 2012;7(7):e41055. https://pubmed.ncbi.nlm.nih.gov/22815911. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3398876. https://doi.org/10.1371/journal.pone.0041055.
2. El-Naggar AK, Chan JKC, Grandis JR, Takata T, Slootweg PJ, eds. World Health Organization classification of head and neck tumours, 4th ed, Vol. 9. Lyon: International Agency for Research on Cancer (IARC), 2017.
3. Goldblum J, Lamps L, McKenney J, Myers J. In: Rosai and Ackermann’s surgical pathology, 11th ed. USA: Mosby, Elsevier Inc., 2018.
4. Kong L, Lu JJ, Guo X, Wu Y, Zhang Y. The risk of second primary tumors in patients with nasopharyngeal carcinoma after definitive radiotherapy. Cancer. 2006;107(6):1287-93. https://pubmed.ncbi.nlm.nih.gov/16909425. https://doi.org/10.1002/cncr.22119.
5. Oka Y, Sugiyama H. WT1 peptide vaccine, one of the most promising cancer vaccines: its present status and the future prospects. Immunotherapy. 2010;2(5):591-4. https://pubmed.ncbi.nlm.nih.gov/20874639. https://doi.org/10.2217/imt.10.58.
6. Oiseth SJ, Aziz MS. Cancer immunotherapy: a brief review of the history, possibilities, and challenges ahead. J Cancer Metastasis Treat. 2017;3:250-61. https://doi.org/10.20517/2394-4722.2017.41.
7. Gong J, Chehrazi-Raffle A, Reddi S, Salgia R. Development of PD-1 and PD-L1 inhibitors as a form of cancer immunotherapy: a comprehensive review of registration trials and future considerations. J Immunother Cancer. 2018;6(1):8. https://pubmed.ncbi.nlm.nih.gov/29357948. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5778665. https://doi.org/10.1186/s40425-018-0316-z.
8. Jain A, Chia WK, Toh HC. Immunotherapy for nasopharyngeal cancer – a review. Chin Clin Oncol. 2016;5(2):22. https://pubmed.ncbi.nlm.nih.gov/27121882. https://doi.org/10.21037/cco.2016.03.08.
9. Hsu C, Lee SH, Ejadi S, et al. Safety and antitumor activity of pembrolizumab in patients with programmed-death-ligand 1-positive nasopharyngeal carcinoma: results of the KEYNOTE-028 study. J Clin Oncol 2017;35(36):4050-6. https://pubmed.ncbi.nlm.nih.gov/28837405. https://doi.org/10.1200/JCO.2017.73.3675.
10. Oka Y, Tsuboi A, Taguchi T, et al Induction of WT1 (Wilms' tumor gene)-specific cytotoxic T lymphocytes by WT1 peptide vaccine and the resultant cancer regression. Proc Natl Acad Sci USA. 2004;101(38):13885-90. https://pubmed.ncbi.nlm.nih.gov/15365188. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC518848. https://doi.org/10.1073/pnas.0405884101.
11. Di Stasi A, Jimenez AM, Minagawa K, Al-obaidi M, Rezvani K. Review of the results of WT1 peptide vaccination strategies for myelodysplastic syndromes and acute myeloid leukemia from nine different studies. Front Immunol. 2015;6:36. https://pubmed.ncbi.nlm.nih.gov/25699052. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4316779. https://doi.org/10.3389/fimmu.2015.00036.
12. Oka Y, Tsuboi A, Kawakami M, et al. Development of WT1 peptide cancer vaccine against hematopoietic malignancies and solid cancers. Curr Med Chem. 2006;13(20):2345-52. https://pubmed.ncbi.nlm.nih.gov/16918359.
13. Carpentieri DF, Nichols K, Chou PM, Matthews M, Pawel B, Huff D. The expression of WT1 in the differentiation of rhabdomyosarcoma from other pediatric small round blue cell tumors. Mod Pathol. 2002;15(10):1080-6. https://pubmed.ncbi.nlm.nih.gov/12379755. https://doi.org/10.1097/01.MP.0000028646.03760.6B.
14. Nakatsuka S, Oji Y, Horiuchi T, et al Immunohistochemical detection of WT1 protein in a variety of cancer cells. Mod Pathol. 2006;19(6)804-14. https://pubmed.ncbi.nlm.nih.gov/16547468. https://doi.org/10.1038/modpathol.3800588.
15. Cheever MA, Allison JP, Ferris AS, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res. 2009;15(17):5323-17. https://pubmed.ncbi.nlm.nih.gov/19723653. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5779623. https://doi.org/10.1158/1078-0432.CCR-09-0737.
16. Kumar V, Abbas A, Aster J. Robbins and Cotran pathologic basis of disease, 9th ed. Philadelphia, PA: Elsevier/Saunders, 2015.
17. Call KM, Glaser T, Ito CY, et al Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms’ tumor locus. Cell. 1990;50(3):509-20. https://pubmed.ncbi.nlm.nih.gov/2154335.
18. Yang L, Han Y, Suarez Saiz F, Minden MD. A tumor suppressor and oncogene: the WT1 story. Leukemia. 2007;21(5)868-76. https://pubmed.ncbi.nlm.nih.gov/17361230. https://doi.org/10.1038/sj.leu.2404624.
19. Leader R, Deol-Poonia RK, Sheard J, Triantafyllou A. Immunohistochemical localization of WT1 in epithelial salivary tumors. Pathol Res Pract. 2014;210(11):726-32. https://pubmed.ncbi.nlm.nih.gov/25086675. https://doi.org/0.1016/j.prp.2014.06.029.
20. Al-Adnani M, Williams S, Anderson J, Ashworth M, Malone M, Sebire NJ. Immunohistochemical nuclear positivity for WT1 in childhood acute myeloid leukemia. Fetal Pediatr Pathol. 2007;26(4):193-7. https://pubmed.ncbi.nlm.nih.gov/18075834. https://doi.org/10.1080/15513810701696957.
21. Oji Y, Miyoshi S, Maeda H, et al. Overexpression of the Wilms' tumor gene WT1 in de novo lung cancers. Int J Cancer. 2002;100(3):297-303. https://pubmed.ncbi.nlm.nih.gov/12115544. https://doi.org/10.1002/ijc.10476.
22. Kim A, Park EY, Kim K, et al. Prognostic significance of WT1 expression in soft tissue sarcoma. World J Surg Oncol. 2014;12:214. https://pubmed.ncbi.nlm.nih.gov/25026998. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4114094. https://doi.org/10.1186/1477-7819-12-214.
23. Magro G, Salvatorelli L, Puzzo L, Musumeci G, Bisceglia M, Parenti R. Oncofetal expression of Wilms’ tumor 1 (WT1) protein in human fetal, adult and neoplastic skeletal muscle tissues. Acta Histochem. 2015;117(4-5):492-504. https://pubmed.ncbi.nlm.nih.gov/25800978. https://doi.org/10.1016/j.acthis.2015.02.012.
24. Ueda T, Oji Y, Naka N, et al Overexpression of the Wilms' tumor gene WT1 in human bone and soft-tissue sarcomas. Cancer Sci. 2003;94(3):271-6. https://pubmed.ncbi.nlm.nih.gov/12824921. https://doi.org/10.1111/j.1349-7006.2003.tb01432.x.
25. Oji Y, Suzuki T, Nakano Y, et al. Overexpression of the Wilms' tumor gene WT1 in primary astrocytic tumors. Cancer Sci. 2004;95(10):822-7. https://pubmed.ncbi.nlm.nih.gov/15504250. https://doi.org/10.1111/j.1349-7006.2004.tb02188.x.
26. Niksic M, Slight J, Sanford JR, Caceres JF, Hastie ND. The Wilms’
tumour protein (WT1) shuttles between nucleus and cytoplasm and is present in functional polysomes. Hum Mol Genet. 2004;13(4):463-71. https://pubmed.ncbi.nlm.nih.gov/14681305. https://doi.org/10.1093/hmg/ddh040.
27. Waldstrøm M, Grove A. Immunohistochemical expression of Wilms tumor gene protein in different histologic subtypes of ovarian carcinomas. Arch Pathol Lab Med. 2005;129(1):85-8. https://pubmed.ncbi.nlm.nih.gov/15628914.
28. Foster MR, Johnson JE, Olson SJ, Allred DC. Immunohistochemical analysis of nuclear versus cytoplasmic staining of WT1 in malignant mesotheliomas and primary pulmonary adenocarcinomas. Arch Pathol Lab Med. 2001;125(10)1316-20. https://pubmed.ncbi.nlm.nih.gov/11570906.
29. Ye Y, Raychaudhuri B, Gurney A, Campbell CE, Williams BR. Regulation of WT1 by phosphorylation: inhibition of DNA binding, alteration of transcriptional activity and cellular translocation. EMBO J. 1996;15(20):5606-15. https://pubmed.ncbi.nlm.nih.gov/8896454. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC452305.
30. Oji Y, Yamamoto H, Nomura M, et al. Overexpression of the Wilms’ tumor gene WT1 in colorectal adenocarcinoma. Cancer Sci. 2003;94(8):712-7. https://pubmed.ncbi.nlm.nih.gov/12901797. https://doi.org/10.1111/j.1349-7006.2003.tb01507.x.
31. Mikami T, Hada T, Chosa N, Ishisaki A, Mizuki H, Takeda Y. Expression of Wilms’ tumor 1 (WT1) in oral squamous cell carcinoma. J Oral Pathol Med. 2013;42(2):133-9. https://pubmed.ncbi.nlm.nih.gov/22672247. https://doi.org/10.1111/j.1600-0714.2012.01182.x.
32. Li X, Ottosson S, Wang S, et al. Wilms’ tumor gene 1 regulates p63 and promotes cell proliferation in squamous cell carcinoma of the head and neck. BMC Cancer. 2015;15:342. https://pubmed.ncbi.nlm.nih.gov/25929687. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4421988. https://doi.org/10.1186/s12885-015-1356-0.
33. Lee A, Lydiatt W, Colevas A, et al. Nasopharynx. In: Amin MB, et al. (eds). AJCC cancer staging manual. 8th ed., 2017.
34. Oji Y, Inohara H, Nakazawa M. Overexpression of the Wilms' tumor gene WT1 in head and neck squamous cell carcinoma. Cancer Sci. 2003;94(6):523-9. https://pubmed.ncbi.nlm.nih.gov/12824878. https://doi.org/10.1111/j.1349-7006.2003.tb01477.x.
35. Fattahi S, Rahmani SZ, Vosoughhosseini S, Rahmani SP. Configuring the expression of Wilms’ tumor 1 in oral squamous cell carcinoma and its relationship with clinicopathologic features. J Dent App. 2016;3(4):349-52.
36. Ohno S, Okuyama R, Aruga A, Sugiyama H, Yamamoto M. Phase I trial of Wilms’ tumor 1 (WT1) peptide vaccine with GM-CSF or CpG in patients with solid malignancy. Anticancer Res. 2012;32(6):2263-9. https://pubmed.ncbi.nlm.nih.gov/22641661.
37. Oka Y, Tsuboi A, Nakata J, et al. Wilms' tumor gene 1 (WT1) peptide vaccine therapy for hematological malignancies: from CTL epitope identification to recent progress in clinical studies including a cure-oriented strategy. Oncol Res Treat. 2017; 40(11):682-90. https://pubmed.ncbi.nlm.nih.gov/29041012. https://doi.org/10.1159/000481353.
38. Nishida S, Ishikawa T, Egawa S, et al. Combination gemcitabine and WT1 peptide vaccination improves progression-free survival in advanced pancreatic ductal adenocarcinoma: a phase II randomized study. Cancer Immunol Res. 2018;6(3):320-21. https://pubmed.ncbi.nlm.nih.gov/29358173. https://doi.org/10.1158/2326-6066.CIR-17-0386.
39. Qi XW, Zhang F, Wu H, et al. Wilms’ tumor 1 (WT1) expression and prognosis in solid cancer patients: a systematic review and meta-analysis. Sci Rep. 2015;5:8924. https://pubmed.ncbi.nlm.nih.gov/25748047. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4352850. https://doi.org/10.1038/srep08924.
40. Hu C, Wei W, Chen X, et al. A global view of the oncogenic landscape in nasopharyngeal carcinoma: an integrated analysis at the genetic and expression levels. PLoS ONE. 2012;7(7):e41055. https://pubmed.ncbi.nlm.nih.gov/22815911. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3398876. https://doi.org/10.1371/journal.pone.0041055.
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05/22/2019
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Manasan, C. V., Atun, J. M., & Carnate Jr., J. (2019). Immunohistochemical Expression of WT1 in Nasopharyngeal Carcinoma Among Filipino Patients in a Tertiary Hospital. PJP, 4(1), 25–33. https://doi.org/10.21141/PJP.2019.05
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