Wilms' tumor gene 1 immunotherapy in pelvic gynecological malignancies

Expert Review of Clinical Immunology

Volumn 10, Issue 6, 2014, Pages 705-711

  Coosemans, A ^a   Vergote, I ^a,b   Van Gool, S W ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

DC; dendritic cell; immunotherapy; ovarian cancer; uterine cancer; Wilms' tumor gene 1; WT1

Indexed keywords

CYCLINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; MESSENGER RNA; PROTEIN P53; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; WART VIRUS VACCINE; WT1 PROTEIN; WT1 PROTEIN, HUMAN;

ACTIVE IMMUNIZATION; ARTICLE; CANCER GROWTH; CANCER IMMUNOTHERAPY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DNA IMMUNIZATION; ENDOMETRIUM CANCER; GYNECOLOGIC CANCER; IMMUNOGENICITY; KIDNEY CANCER; NATURAL KILLER CELL; OVARY CANCER; PELVIS CANCER; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SEX CORD TUMOR; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; UTERUS CANCER; UTERUS SARCOMA; FEMALE; GENITAL NEOPLASMS, FEMALE; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; PATHOLOGY; PELVIC NEOPLASMS;

ANTIGENS, NEOPLASM; FEMALE; GENITAL NEOPLASMS, FEMALE; HUMANS; IMMUNOTHERAPY; PELVIC NEOPLASMS; WT1 PROTEINS;

EID: 84901007308     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2014.910119     Document Type: Article

References (85)

1. Arora V, Quinn MA. Endometrial cancer. Best Pract Res Clin Obstet Gynaecol 2012;26:311-24
2. Amant F, Coosemans A, Debiec-Rychter M, et al. Clinical management of uterine sarcomas. Lancet Oncol 2009;10:1188-98
3. Vergote I, Amant F, Kristensen G, et al. Primary surgery or neoadjuvant chemotherapy followed by interval debulking surgery in advanced ovarian cancer. Eur J Cancer 2011;47:S88-92
4. Peiretti M, Zapardiel I, Zanagnolo V, et al. Managment of recurrent cervical cancer: a review of the literature. Surg Oncol 2012;21:e59-66
5. Kahn JA. HPV vaccination for the prevention of cervical intraepithelial neoplasia. N Eng J Med 2009;361:271-8
6. Hohenstein P, Hastie ND. The many facets of the Wilms' tumor gene WT1. Hum Mol Genet 2006;15:R196-201
7. Ye Y, Raychaudhuri B, Gurney A, et al. Regulation of WT1 by phosphorylation: inhibition of DNA binding, alteration of transcriptional activity and cellular translocation. EMBO J 1996;15:5606-15
8. Morrison AA, Viney RL, Ladomery MR The post-transcriptional roles of WT1, a multifunctional zinc-finger protein. Biochim Biophys Acta 2008;1785:55-62
9. Yang L, Han Y, Suarez-Saiz F, et al. A tumor suppressor and oncogene: the WT1 story. Leukemia 2007;21:868-76
10. Niksic M, Slight J, Sanford JR, et al. The Wilms' tumor protein (WT1) shuttles between nucleus and cytoplasm and is present in functional polysomes. Hum Mol Genet 2004;13:463-71
11. 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;15:5323-37
12. Coosemans A, Moerman P, Verbist L, et al. Wilms' tumor gene 1 (WT1) in endometrial carcinoma. Gynecol Oncol 2008;111:502-8
13. Nofech-Mozes S, Resty G, Ismiil N, et al. Immunohistochemical characterization of endocervical papillary serous carcinoma. Int J Gynecol Cancer 2006;16:286-92
14. Carlson JW, Nucci MR, Brodsky J, et al. Biomarker-assisted diagnosis of ovarian, cervical and pulmonary small cell carcinomas: the role of TTF-1, WT1 and HPV analysis. Histopathology 2007;51: 305-12
15. Dohi S, Ohno S, Ohno Y, et al. Correlation between WT1 expression and cell proliferation in endometrial cancer. Anticancer Res 2009;29:4887-91
16. Coosemans A, Van Calster B, Verbist G, et al. WT1 is a prognostic marker in high grade uterine sarcoma. Int J Gynecol Cancer 2011;21:302-8
17. Barbolina MV, Adley BP, Shea LD, Stack MS. Wilms tumor gene protein 1 is associated with ovarian cancer metastasis and modulates cell invasion. Cancer 2008;112:1632-41
18. Sagarra RA, Andrade LA, Martinez EZ, et al. P53 and Bcl-2 as prognostic predictors in epithelial ovarian cancer. Int J Gynecol Cancer 2002;12:720-7
19. Maheswaran S, Park S, Bernard A, et al. Physical and functional interaction between WT1 and p53 proteins. Proc Natl Acad Sci USA 1993;90:5100-4
20. Vermeij R, de Bock GH, Leffers N, et al. Tumor-infiltrating cytotoxic T lymphocytes as independent prognostic factor in epithelial ovarian cancer with Wilms tumor protein 1 overexpression. J Immunother 2011;34:516-23
21. Zhao C, Vinh TN, McManus K, et al. Identification of the most sensitive and robust immunohistochemical markers in different categories of ovarian sex cord-stromal tumors. Am J Surg Pathol 2009;33:354-66
22. Van Driessche A, Berneman Z, Van Tendeloo V. Active specific immunotherapy targeting the Wilms' tumor protein 1 (WT1) for patients with hematological malignancies and solid tumors: lessons from early clinical trials. Oncologist 2012;17:250-9
23. Coosemans A, Wolfl M, Berneman ZN, et al. Immunological response after therapeutic vaccination with WT1 mRNA-loaded dendritic cells in end-stage endometrial carcinoma. Anticancer Res 2010;30:3709-14
24. Coosemans A, Vanderstraeten A, Tuyaerts S, et al. Immunological response after WT1 mRNA-loaded dendritic cell immunotherapy in ovarian carcinoma and carcinosarcoma. Anticancer Res 33:3855-9
25. Coosemans A, Vanderstraeten A, Tuyaerts S, et al. Wilms' tumor gene 1 (WT1)-loaded dendritic cell immunotherapy in patients with uterine tumors: a phase I/II clinical trial. Anticancer Res 2013;33:5495-500
26. Ohno S, Kyo S, Moyojo S, et al. Wilms tumor 1 (WT1) peptide immunotherapy for gynecological malignancy. Anticancer Res 2009;29:4779-84
27. Dohi S, Ohno S, Ohno Y, et al. WT1 peptide vaccine stabilized intractable ovarian cancer patient for one year: a case report. Anticancer Res 2011;31:2441-5
28. Miyatake T, Ueda Y, Morimoto A, et al. WT1 peptide immunotherapy for gynecological malignancies resistant to conventional therapies: a phase II trial. J Cancer Res Clin Oncol 2013;139:457-63
29. Gilboa E. DC-based cancer vaccines. J Clin Invest 2007;117:1195-203
30. Michiels A, Tuyaerts S, Bonehill A, et al. Electroporation of immature and mature dendritic cells: implications for dendritic cell-based vaccines. Gene Ther 2005; 12:772-82
31. Rezvani K, Young ASM, Mielke S, et al. Repeated PR1 and WT1 peptide vaccination in Montanide adjuvant fails to induce sustained high-avidity, epitope-specific CD8+ T cells in myeloid malignancies. Haematologica 2011;96: 432-40
32. Uttenthal B, Martinez-Davila I, Ivey A, et al. Wilms' Tumour 1 (WT1) peptide vaccination in patients with acute myeloid leukaemia induces short-lived WT1-specificimmune responses. Br J Haematol 2014;164:366-75
33. Busse A, Letsch A, Scheibenbogen C, et al. Mutation or loss of Wilms' tumor gene 1 (WT1) are not major reasons for immune escape in patients with AML receiving WT1 peptide vaccination. J Transl Med 2010;8:5
34. Bonini C, Lee SP, Riddell SR, et al. Targeting antigen in mature dendritic cells for simultaneous stimulation of mRNA electroporation for the purpose of therapeutic vaccination in melanoma patients. Clin Cancer Res 2009;15:3366-75
35. Obermajer N, Muthuswamy R, Odunsi K, et al. PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Res 2011;71: 7463-70
36. Gallois A, Bhardwaj N. Dendritic cell-targeted approaches to modulate immune dysfunction in the tumor microenvironment. Front Immunol 2013;4:436
37. Ardon H, Van Gool SW, Verschuere T, et al. Integration of autologous dendritic cell-based immunotherapy in the standard of care treatment for patients with newlydiagnosed glioblastoma: results of the HGG-2006 phase I/II trial. Cancer Immunol Immunother 2012;61:2033-44
38. Chiang CL, Kandalaft LE, Tanyi J, et al. A dendritic cell vaccine pulsed with autologous hypochlorous acid-oxidized ovarian cancer lysate primes effective broad antitumor immunity: from bench to bedside. Clin Cancer Res 2013;19:4801-15
39. Schilling B, Harasymczuk M, Schuler P, et al. IRX-2, a novel immunotherapeutic, enhances functions of human dendritic cells. PLoS One 2013;8:e47234
40. Van Lint S, Goyvaerts C, Maenhout S, et al. Preclinical evaluation of TriMix and antigen mRNA-based antitumor therapy. Cancer Res 2012;72:1661-71
41. Anguille S, Smits EL, Cools N, et al. Short-term cultured, interleukin-15 differentiated dendritic cells have potent immunostimulatory properties. J Transl Med 2009;7:109
42. Harfuddin Z, Kwajah S, ChingNyiSim A, et al. CD137L-stimulated dendritic cells are more potent than conventional dendritic cells at eliciting cytotoxic T-cell responses. Oncoimmunology 2013;2:e26859
43. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret ally: immunostimulation by anticancer drugs. Nat Rev Drug Discov 2012;11:215-33
44. Duraiswamy J, Freeman GJ, Coukos G. Therapeutic PD-1 pathway blockade augments with other modalities of immunotherapy to prevent immune decline in ovarian cancer. Cancer Res 2013;73: 3591-603
45. Gutkin DW, Shurin MR. Clinical evaluation of systemic and local immune responses in cancer: time for integration. Cancer Immunol Immunother 2014;63: 45-57
46. Pectasides D, Pectasides E, Kassanos D. Germ cell tumor of the ovary. Cancer Treat Rev 2008;34:427-41
47. Goldstein NS, Uzieblo A. WT1 immunoreactivity in uterine papillary serous carcinomas is different from ovarian serous carcinomas. Am J Clin Pathol 2002;117:541-5
48. Zhang Q, Wright T, Alexis D, Mansukhani M. Differential expression of WT1 in uterine serous and endometrioid carcinoma. Mod Pathol 2003;16:A988
49. Hashi A, Yuminamochi T, Murata S, et al. Wilms tumor gene immunoreactivity in primary serous carcinomas of the fallopian tube, ovary, endometrium, and peritoneum. Int J Gynecol Pathol 2003;22:374-7
50. Shevchuk MM, Lallas TA, DaSilva M. Endometrial carcinoma: do oncogene studies separate types I and II. Mod Pathol 2003; 16:A216.
51. Kiyokawa T, Kanetsuna Y, Harada T, et al. WT-1 expression in ovarian epithelial tumors and endometrial serous carcinoma. Mod Pathol 2003;16:A837
52. Dupont J, Wang X, Marshall DS, et al. Wilms Tumor Gene (WT1) and p53 expression in endometrial carcinomas: a study of 130 cases using a tissue microarray. Gynecol Oncol 2004;94:449-55
53. Acs G, Pasha T, Zhang PJ. WT1 is differentially expressed in serous, endometrioid, clear cell, and mucinous carcinomas of the peritoneum, fallopian tube, ovary, and endometrium. Int J Gynecol Pathol 2004;23:110-18
54. Egan JA, Ionescu MC, Eapen E, et al. Differential expression of WT1 and p53 in serous and endometrioid carcinomas of the endometrium. Int J Gynecol Pathol 2004;23:119-22
55. Al Hussaini M, Stockman A, Foster H, McCluggage WG. WT-1 assists in distinguishing ovarian from uterine serous carcinoma and in distinguishing between serous and endometrioid ovarian carcinoma. Histopathology 2004;44:109-15
56. Euscher ED, Malpica A, Deavers MT, Silva EG. Differential expression of WT-1 in serous carcinomas in the peritoneum with or without associated serous carcinoma in endometrial polyps. Am J Surg Pathol 2005;29:1074-8
57. Chitale DA, Jungbluth AA, Marshall DS, et al. Expression of cancer-testis antigens in endometrial carcinomas using a tissue microarray. Mod Pathol 2005;18:119-26
58. Nakatsuka S, Oji Y, Horiuchi T, et al. Immunohistochemical detection of WT1 protein in a variety of cancer cells. Mod Pathol 2006;19:804-14
59. Coosemans A, AminiNik S, Caluwaerts S, et al. Upregulation of WT1 in uterine sarcomas. Eur J Cancer 2007;43:1630-7
60. Nofech-Mozes S, Khalifa MA, Ismiil N, et al. Immunophenotyping of serous carcinoma of the female genital tract. Mod Pathol 2008;21:1147-55
61. Hirschowitz L, Ganesan R, McCluggage WG. WT1, p53 and hormone receptor expression in uterine serous carcinoma. Histopathology 2009;55:478-82
62. Franko A, Magliocco AM, Duan Q, Duggan MA. WT1 immunoprofiling and comparison of malignant Mullerian mixed tumors of the female genital tract. Int J Gynecol Pathol 2010;29:452-8
63. Agoff SN, Grieco VS, Garcia R, Grown AM. Immunohistochemical distinction of endometrial stromal sarcoma and cellular leiomyoma. Appl Immunohistochem Mol Morphol 2001;9: 164-9
64. Sumathi VP, Al Hussaini M, Connolly LE, et al. Endometrial stromal neoplasms are immunoreactive with WT-1 antibody. Int J Gynecol Pathol 2004;23:241-7
65. Bing Z, Pasha TL, Acs G, Zhang PJ. Cytoplasmic overexpression of WT-1 in gastrointestinal stromal tumor and other soft tissue tumors. Appl Immunohistochem Mol Morphol 2008;16:316-21
66. Carvalho JC, Thomas DG, Lucas DR. Cluster analysis of immunohistochemical markers in leiomyosarcoma delineates specific anatomic and gender subgroups. Cancer 2009;115:4186-95
67. Goldstein NS, Bassi D, Uzieblo A. WT1 is an integral component of an antibody panel to distinguish pancreaticobiliary and some ovarian epithelial neoplasms. Am J Clin Pathol 2001;116:246-52
68. Logani S, Oliva E, Amin MB, et al. Immunoprofile of ovarian tumors with putative transitional cell (urothelial) differentiation using novel urothelial markers: histogenetic and diagnostic implications. Am J Surg Pathol 2003;27: 1434-41
69. Hwang H, Quenneville L, Yaziji H, Gown AM. Wilms tumor gene product: sensitive and contextually specific marker of serous carcinomas of ovarian surface epithelial origin. Appl Immunohistochem Mol Morphol 2004;12:122-6
70. Ramalingam P, Malpica A, Silva EG, et al. The use of cytokeratin 7 and EMA in differentiating ovarian yolk sac tumors from endometrioid and clear cell carcinomas. Am J Surg Pathol 2004;28:1499-505
71. O'Neill CJ, Deavers MT, Malpica A, et al. An immunohistochemical comparison between low-grade and high-grade ovarian serous carcinomas: significantly higher expression of p53, MIB1, BCL2, Her-2/neu, and C-KIT in high-grade neoplasms. Am J Surg Pathol 2005;29:1034-41
72. Waldstrom M, Grove A. Immunohistochemical expression of wilms tumor gene protein in different histologic subtypes of ovarian carcinomas. Arch Pathol Lab Med 2005;129:85-8
73. Cathro HP, Stoler MH. The utility of calretinin, inhibin, and WT1 immunohistochemical staining in the differential diagnosis of ovarian tumors. Hum Pathol 2005;36:195-201
74. Hylander B, Repasky E, Shrikant P. Expression of Wilms tumor gene (WT1) in epithelial ovarian cancer. Gynecol Oncol 2006;101:12-17
75. Netinatsunthorn W, Hanprasertpong J, Dechsukhum C, et al. WT1 gene expression as a prognostic marker in advanced serous epithelial ovarian carcinoma: an immunohistochemical study. BMC Cancer 2006;6:90
76. Yamamoto S, Tsuda H, Kita T, et al. Clinicopathological significance of WT1 expression in ovarian cancer: a possible accelerator of tumor progression in serous adenocarcinoma. Virchows Arch 2007;451:27-35
77. Hogdall EV, Christensen L, Kjaer SK, et al. Expression level of Wilms tumor (WT1) protein has limited prognostic value in epithelial ovarian cancer: from the Danish "MALOVA" ovarian cancer study. Gynecol Oncol 2007;106:318-24
78. Zhao C, Bratthauer GL, Barner R, Vang R. Diagnostic utility of WT1 immunostaining in ovarian sertoli cell tumor. Am J Surg Pathol 2007;31:1378-86
79. Stewart CJ, Brennan BA, Chan T, Netreba J. WT1 expression in endometrioid ovarian carcinoma with and without associated endometriosis. Pathology 2008;40:592-9
80. Köbel M, Kalloger SE, Carrick J, et al. A limited panel of immunomarkers can reliably distinguish between clear cell and high-grade serous carcinoma of the ovary. Am J Surg Pathol 2009;33:14-21
81. Madore J, Ren F, Filali-Mouhim A, et al. Characterization of the molecular differences between ovarian endometrioid carcinoma and ovarian serous carcinoma. J Pathol 2010;220:392-400
82. Tabrizi AD, Kalloger SE, Köbel M, et al. Primary ovarian mucinous carcinoma of intestinal type: significance of pattern of invasion and immunohistochemical expression profile in a series of 31 cases. Int J Gynecol Pathol 2010;29:99-107
83. Kalloger SE, Köbel M, Leung S, et al. Calculator for ovarian carcinoma subtype prediction. Mod Pathol 2011;24:512-21
84. Liliac L, Carcangiu ML, Canevari S, et al. The value of PAX8 and WT1 molecules in ovarian cancer diagnosis. Rom J Morphol Embryol 2013;54:17-27
85. Deavers MT, Malpica A, Liu J, et al. Ovarian sex cord-stromal tumors: an immunohistochemical study including a comparison of calretinin and inhibin. Mod Pathol 2003;16:584-90