Distinction of Endocervical and Endometrial Adenocarcinomas: Immunohistochemical p16 Expression Correlated with Human Papillomavirus (HPV) DNA Detection

American Journal of Surgical Pathology

Volumn 28, Issue 2, 2004, Pages 160-167

  Ansari Lari, M Ali ^a   Staebler, Annette ^a,d   Zaino, Richard J ^b   Shah, Keerti V ^c   Ronnett, Brigitte M ^a,e  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

Endocervical adenocarcinoma; Endometrial adenocarcinoma; Human papillomavirus DNA; Immunohistochemistry; In situ hybridization; p16

Indexed keywords

PROTEIN P16; VIRUS DNA;

ADENOCARCINOMA; ARTICLE; BIOPSY; CANCER LOCALIZATION; CLINICAL ARTICLE; CONTROLLED STUDY; CURETTAGE; DISEASE ASSOCIATION; DNA DETERMINATION; ENDOMETRIUM CARCINOMA; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; HYSTERECTOMY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; UTERINE CERVIX CARCINOMA; UTERINE ENDOCERVIX; UTERUS; WART VIRUS;

ADENOCARCINOMA; ADULT; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA, VIRAL; ENDOMETRIAL NEOPLASMS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MIDDLE AGED; PAPILLOMAVIRIDAE; POLYMERASE CHAIN REACTION; UTERINE CERVICAL NEOPLASMS;

EID: 1642494668     PISSN: 01475185     EISSN: None     Source Type: Journal    
DOI: 10.1097/00000478-200402000-00002     Document Type: Article

References (62)

1. Alfsen GC, Thoresen SO, Kristensen GB, et al. Histopathologic subtyping of cervical adenocarcinoma reveals increasing incidence rates of endometrioid tumors in all age groups: a population based study with review of all nonsquamous cervical carcinomas in Norway from 1966 to 1970, 1976 to 1980, and 1986 to 1990. Cancer. 2000;89:1291-1299.
2. Andersson S, Rylander E, Larsson B, et al. The role of human papillomavirus in cervical adenocarcinoma carcinogenesis. Eur J Cancer. 2001;37: 246-250.
3. Cairns P, Polascik TJ, Eby Y, et al. Frequency of homozygous deletion at p16/CDKN2 in primary human tumours. Nat Genet. 1995;11:210-212.
4. Cameron RI, Maxwell P, Jenkins D, et al. Immunohistochemical staining with MIB1, bcl2 and p16 assists in the distinction of cervical glandular intraepithelial neoplasia from tubo-endometrial metaplasia, endometriosis and microglandular hyperplasia. J Urol. 2002;41:313-321.
5. Castrillon DH, Lee KR, Nucci MR. Distinction between endometrial and endocervical adenocarcinoma: an immunohistochemical study. Int J Gynecol Pathol. 2002;21:4-10.
6. Chellappan SP, Hiebert S, Mudryj M, et al. The E2F transcription factor is a cellular target for the RB protein. Cell. 1991;65:1053-1061.
7. Chen PL, Scully P, Shew JY, et al. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell. 1989;58:1193-1198.
8. Chittenden T, Livingston DM, Kaelin WG Jr. The T/E1A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein. Cell. 1991;65:1073-1082.
9. Dabbs DJ, Sturtz K, Zaino RJ. The immunohistochemical discrimination of endometrioid adenocarcinomas. Hum Pathol. 1996;27:172-177.
10. Dallenbach-Hellweg G, Lang-Averous G, Hahn U. The value of immunohistochemistry in the differential diagnosis of endometrial carcinomas. APMIS Suppl. 1991;23:91-99.
11. Duggan MA, McGregor SE, Benoit JL, et al. The human papillomavirus status of invasive cervical adenocarcinoma: a clinicopathological and outcome analysis. Hum Pathol. 1995;26:319-325.
12. Dyson N, Howley PM, Munger K, et al. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science. 1989;243:934-937.
13. Fujita M, Shroyer KR, Markham NE, et al. Association of human papillomavirus with malignant and premalignant lesions of the uterine endometrium. Hum Pathol. 1995;26:650-658.
14. Geradts J, Hruban RH, Schutte M, et al. Immunohistochemical p16INK4a analysis of archival tumors with deletion, hypermethylation, or mutation of the CDKN2/MTS1 gene: a comparison of four commercial antibodies. Appl Immunohistochem Mol Morphol. 2000;8:71-79.
15. Gravitt PE, Peyton CL, Alessi TQ, et al. Improved amplification of genital human papillomaviruses. J Clin Microbiol. 2000;38:357-361.
16. Hatta Y, Hirama T, Takeuchi S, et al. Alterations of the p16 (MTS1) gene in testicular, ovarian, and endometrial malignancies. J Urol. 1995;154: 1954-1957.
17. Hirama T, Miller CW, Wilczynski SP, et al. p16 (CDKN2/cyclin-dependent kinase-4 inhibitor/multiple tumor suppressor-1) gene is not altered in uterine cervical carcinomas or cell lines. Mod Pathol. 1996;9: 26-31.
18. Hording U, Daugaard S, Visfeldt J. Adenocarcinoma of the cervix and adenocarcinoma of the endometrium: distinction with PCR-mediated detection of HPV DNA. APMIS. 1997;105:313-316.
19. Iwasawa A, Nieminen P, Lehtinen M, et al. Human papillomavirus DNA in uterine cervix squamous cell carcinoma and adenocarcinoma detected by polymerase chain reaction. Cancer. 1996;77:2275-2279.
20. Jones MW, Kounelis S, Papadaki H, et al. Well-differentiated villoglandular adenocarcinoma of the uterine cervix: oncogene/tumor suppressor gene alterations and human papillomavirus genotyping. Int J Gynecol Pathol. 2000;19:110-117.
21. Kamb A, Gruis NA, Weaver-Feldhaus J, et al. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 1994;264: 436-440.
22. Keating JT, Cviko A, Riethdorf S, et al. Ki-67, cyclin E, and p16INK4 are complimentary surrogate biomarkers for human papilloma virus-related cervical neoplasia. Am J Surg Pathol. 2001;25:884-891.
23. Khleif SN, DeGregori J, Yee CL, et al. Inhibition of cyclin D-CDK4/CDK6 activity is associated with an E2F-mediated induction of cyclin kinase inhibitor activity. Proc Natl Acad Sci USA. 1996;93:4350-4354.
24. Kim JW, Namkoong SE, Ryu SW, et al. Absence of p15INK4B and p16INK4A gene alterations in primary cervical carcinoma tissues and cell lines with human papillomavirus infection. Gynecol Oncol. 1998;70: 75-79.
25. Klaes R, Friedrich T, Spitkovsky D, et al. Overexpression of p16(INK4A) as a specific marker for dysplastic and neoplastic epithelial cells of the cervix uteri. Int J Cancer. 2001;92:276-284.
26. Koh J, Enders GH, Dynlacht BD, et al. Tumour-derived p16 alleles encoding proteins defective in cell-cycle inhibition. Nature. 1995;375:506-510.
27. Koul A, Willen R, Bendahl PO, et al. Distinct sets of gene alterations in endometrial carcinoma implicate alternate modes of tumorigenesis. Cancer. 2002;94:2369-2379.
28. Lax SF, Pizer ES, Ronnett BM, et al. Clear cell carcinoma of the endometrium is characterized by a distinctive profile of p53, Ki-67, estrogen, and progesterone receptor expression. Hum Pathol. 1998;29:551-558.
29. Lax SF, Pizer ES, Ronnett BM, et al. Comparison of estrogen and progesterone receptor, Ki-67, and p53 immunoreactivity in uterine endometrioid carcinoma and endometrioid carcinoma with squamous, mucinous, secretory, and ciliated cell differentiation. Hum Pathol. 1998;29:924-931.
30. Li Y, Nichols MA, Shay JW, et al. Transcriptional repression of the D-type cyclin-dependent kinase inhibitor p 16 by the retinoblastoma susceptibility gene product pRb. Cancer Res. 1994;54:6078-6082.
31. Lu X, Shiozawa T, Nakayama K, et al. Abnormal expression of sex steroid receptors and cell cycle-related molecules in adenocarcinoma in situ of the uterine cervix [in process citation]. Int J Gynecol Pathol. 1999;18: 109-114.
32. Matsushime H, Ewen ME, Strom DK, et al. Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D type G1 cyclins. Cell. 1992;71:323-334.
33. McCluggage WG, Sumathi VP, McBride HA, et al. A panel of immunohistochemical stains, including carcinoembryonic antigen, vimentin, and estrogen receptor, aids the distinction between primary endometrial and endocervical adenocarcinomas. Int J Gynecol Pathol. 2002;21:11-15.
34. Merlo A, Herman JG, Mao L, et al. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat Med. 1995;1:686-692.
35. Milde-Langosch K, Bamberger AM, Goemann C, et al. Expression of cell-cycle regulatory proteins in endometrial carcinomas: correlations with hormone receptor status and clinicopathologic parameters. J Cancer Res Clin Oncol. 2001;127:537-544.
36. Milde-Langosch K, Bamberger AM, Rieck G, et al. Overexpression of the p16 cell cycle inhibitor in breast cancer is associated with a more malignant phenotype. Breast Cancer Res Treat. 2001;67:61-70.
37. Milde-Langosch K, Riethdorf L, Bamberger AM, et al. p16/MTS1 and pRB expression in endometrial carcinomas. Virchows Arch. 1999;434: 23-28.
38. Milde-Langosch K, Riethdorf S, Kraus-Poppinghaus A, et al. Expression of cyclin-dependent kinase inhibitors p16MTS1, p21WAF1, and p27KIP1 in HPV-positive and HPV-negative cervical adenocarcinomas. Virchows Arch. 2001;439:55-61.
39. Murphy N, Ring M, Killalea AG, et al. p16INK4A as a marker for cervical dyskaryosis: CIN and cGIN in cervical biopsies and ThinPrep smears. J Clin Pathol. 2003;56:56-63.
40. Nakao Y, Yang X, Yokoyama M, et al. Induction of p16 during immortalization by HPV 16 and 18 and not during malignant transformation. Br J Cancer. 1997;75:1410-1416.
41. Nakashima R, Fujita M, Enomoto T, et al. Alteration of p16 and p15 genes in human uterine tumours. Br J Cancer. 1999;80:458-467.
42. Negri G, Egarter-Vigl E, Kasal A, et al. p16INK4a is a useful marker for the diagnosis of adenocarcinoma of the cervix uteri and its precursors: an immunohistochemical study with immunocytochemical correlations. Am J Surg Pathol. 2003;27:187-193.
43. Nobori T, Miura K, Wu DJ, et al. Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature. 1994;368:753-756.
44. O'Leary JJ, Landers RJ, Crowley M, et al. Human papillomavirus and mixed epithelial tumors of the endometrium. Hum Pathol. 1998;29:383-389.
45. Peiffer SL, Bartsch D, Whelan AJ, et al. Low frequency of CDKN2 mutation in endometrial carcinomas. Mol Carcinog. 1995;13:210-212.
46. Pirog EC, Kleter B, Olgac S, et al. Prevalence of human papillomavirus DNA in different histological subtypes of cervical adenocarcinoma. Am J Pathol. 2000;157:1055-1062.
47. Riethdorf L, Riethdorf S, Lee KR, et al. Human papillomaviruses, expression of p16, and early endocervical glandular neoplasia. Hum Pathol. 2002;33:899-904.
48. Riethdorf S, Riethdorf L, Milde-Langosch K, et al. Differences in HPV 16- and HPV 18 E6/E7 oncogene expression between in situ and invasive adenocarcinomas of the cervix uteri. Virchows Arch. 2000;437:491-500.
49. Salvesen HB, Das S, Akslen LA. Loss of nuclear p16 protein expression is not associated with promoter methylation but defines a subgroup of aggressive endometrial carcinomas with poor prognosis. Clin Cancer Res. 2000;6:153-159.
50. Sano T, Masuda N, Oyama T, et al. Overexpression of p16 and p 14ARF is associated with human papillomavirus infection in cervical squamous cell carcinoma and dysplasia. Pathol Int. 2002;52:375-383.
51. Sano T, Oyama T, Kashiwabara K, et al. Expression status of p16 protein is associated with human papillomavirus oncogenic potential in cervical and genital lesions. Am J Pathol. 1998;153:1741-1748.
52. Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature. 1993;366: 704-707.
53. Shiozawa T, Nikaido T, Shimizu M, et al. Immunohistochemical analysis of the expression of cdk4 and p16INK4 in human endometrioid-type endometrial carcinoma. Cancer. 1997;80:2250-2256.
54. Staebler A, Sherman ME, Zaino RJ, et al. Hormone receptor immunohistochemistry and human papillomavirus in situ hybridization are useful for distinguishing endocervical and endometrial adenocarcinomas. Am J Surg Pathol. 2002;26:998-1006.
55. Tenti P, Romagnoli S, Silini E, et al. Human papillomavirus types 16 and 18 infection in infiltrating adenocarcinoma of the cervix: PCR analysis of 138 cases and correlation with histologic type and grade. Am J Clin Pathol. 1996;106:52-56.
56. Tsuda H, Yamamoto K, Inoue T, et al. The role of p16-cyclin d/CDK-pRb pathway in the tumorigenesis of endometrioid-type endometrial carcinoma. Br J Cancer. 2000;82:675-682.
57. Weintraub SJ, Prater CA, Dean DC. Retinoblastoma protein switches the E2F site from positive to negative element. Nature. 1992;358:259-261.
58. Wong YF, Chung TK, Cheung TH, et al. p16INK4 and p15INK4B alterations in primary gynecologic malignancy. Gynecol Oncol. 1997;65:319-324.
59. Wong YF, Chung TK, Cheung TH, et al. Methylation of p16INK4A in primary gynecologic malignancy. Cancer Lett. 1999;136:231-235.
60. Yamazawa K, Matsui H, Seki K, et al. Human papillomavirus-positive well-differentiated villoglandular adenocarcinoma of the uterine cervix: a case report and review of the literature. Gynecol Oncol. 2000;77:473-477.
61. Zaino RJ. Glandular lesions of the uterine cervix. Mod Pathol. 2000;13: 261-274.
62. Zaino RJ. The fruits of our labors: distinguishing endometrial from endocervical adenocarcinoma. Int J Gynecol Pathol. 2002;21:1-3.