The dichotomy in the preinvasive neoplasia to invasive carcinoma sequence in the pancreas: Differential expression of MUC1 and MUC2 supports the existence of two separate pathways of carcinogenesis

Modern Pathology

Volumn 15, Issue 10, 2002, Pages 1087-1095

  Adsay, N Volkan ^a   Merati, Kambiz ^a   Andea, Aleodor ^a   Sarkar, Fazlul ^a   Hruban, Ralph H ^b   Wilentz, Robb E ^b   Goggins, Micheal ^b   Iocobuzio Donahue, Christine ^b   Longnecker, Daniel S ^c   Klimstra, David S ^d  

^a WAYNE STATE UNIVERSITY   (United States)

^b JOHNS HOPKINS HOSPITAL   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Carcinogenesis; Carcinoma; Dysplasia; Immunohistochemistry; Intraductal; Intraepithelial; MUC1; MUC2; Mucin; Neoplasm; Pancreas

Indexed keywords

GLYCOPROTEIN; MUCIN 1; MUCIN 2; TUMOR MARKER;

ARTICLE; CANCER GROWTH; CANCER SURVIVAL; CARCINOGENESIS; COLLOID CARCINOMA; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INVASIVE CARCINOMA; MALIGNANT TRANSFORMATION; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PANCREAS CARCINOMA; PANCREAS TUMOR; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CA-15-3 ANTIGEN; CARCINOMA IN SITU; CARCINOMA, PANCREATIC DUCTAL; HUMANS; IMMUNOENZYME TECHNIQUES; MUCINS; PANCREATIC NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 18644383374     PISSN: 08933952     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.MP.0000028647.98725.8B     Document Type: Article

References (67)

1. Evans DB, Abruzzese JL, Rich TA. Cancer of the pancreas. In: Devita VT, Hellman S, Rosenberg SA, editors. Cancer: principles and practice of oncology. 5th ed. Philadelphia: Lippincott-Raven; 1997. p. 1144-234.
2. Solcia E, Capella C, Klöppel G. Tumors of the pancreas. Armed Forces Institute of Pathology atlas of tumor pathology. Vol. 20. Washington, D.C.: American Registry of Pathology; 1997. p. 53-64.
3. Klöppel G, Solcia E, Longnecker DS, Capella C, Sobin LH. World Health Organization international histologic classification of tumors. Vol. 2. Histologic typing of tumors of the exocrine pancreas. Geneva, Switzerland: Springer; 1996.
4. Sommers SC, Murphy SA, Warren S. Pancreatic duct hyperplasia and cancer. Gastroenterology 1954;27:629-40.
5. Klöppel G, Bommer G, Ruckert K, Seifert G. Intraductal proliferation in the pancreas and its relationship to human and experimental carcinogenesis. Virchows Arch 1980;387:221-33.
6. Brat DJ, Lillemoe KD, Yeo CJ, Warfield PB, Hruban RH. Progression of pancreatic intraductal neoplasias to infiltrating adenocarcinoma of the pancreas. Am J Surg Pathol 1998; 22:163-9.
7. Furukawa T, Chiba R, Kobari M, Matsuno S, Nagura H, Takahashi T. Varying grades of epithelial atypia in the pancreatic ducts of humans. Classification based on morphometry and multivariate analysis and correlated with positive reactions of carcinoembryonic antigen. Arch Pathol Lab Med 1994;118:227-34.
8. Hruban RH, Wilentz RE, Kern SE. Genetic progression in the pancreatic ducts. Am J Pathol 2000;156:1821-5.
9. Longnecker DS. The quest for preneoplastic lesions in the pancreas. Arch Pathol Lab Med 1994;118:226.
10. Luttges J, Diederichs A, Menke MA, Vogel I, Kremer B, Klöppel G. Ductal lesions in patients with chronic pancreatitis show K-ras mutations in a frequency similar to that in the normal pancreas and lack nuclear immunoreactivity for p53. Cancer 2000;88:2495-504.
11. Klimstra DS, Longnecker DS. K-ras mutations in pancreatic ductal proliferative lesions [letter; comment]. Am J Pathol 1994;145:1547-50.
12. Kozuka S, Sassa R, Taki T, Masamoto K, Nagasawa S, Saga S, et al. Relation of pancreatic duct hyperplasia to carcinoma. Cancer 1979;43:1418-28.
13. Hruban RH, Adsay NV, Albores-Saavedra J, Compton C, Garrett ES, Goodman SN, et al. Pancreatic intraepithelial neoplasia: a new nomenclature and classification system for pancreatic duct lesions. Am J Surg Pathol 2001;25:579-86.
14. Payan MJ, Xerri L, Moncada K, Bastid C, Agostini S, Sastre B, et al. Villous adenoma of the main pancreatic duct: a potentially malignant tumor? Am J Gastroenterol 1990;85:459-63.
15. Rogers PN, Seywright MM, Murray WR. Diffuse villous adenoma of the pancreatic duct. Pancreas 1987;2:727-30.
16. Morohoshi T, Kanda M, Asanuma K, Klöppel G. Intraductal papillary neoplasms of the pancreas. A clinicopathologic study of six patients. Cancer 1989;64:1329-35.
17. Kojima Y, Akiyama T, Saito H, Kosaka T, Kita I, Takashima S, et al. Multifocal intraductal papillary adenocarcinoma of the pancreas: report of a case. Surg Today 1993;23:471-5.
18. Yamada M, Kozuka S. Yamao K, Nakazawa S, Naitoh Y, Tsukamoto Y. Mucin-producing tumor of the pancreas. Cancer 1991;68:159-68.
19. Shimizu M, Manabe T. Mucin-producing pancreatic tumors: historical review of its nosological concept. Zentralbl Pathol 1994;140:211-23.
20. Itai Y, Ohhashi K, Nagai H, Murakami Y, Kokubo T. Makita K, et al. "Ductectatic" mucinous cystadenoma and cystadeno-carcinoma of the pancreas. Radiology 1986;161:697-700.
21. Yanagisawa A, Ohashi K, Hori M, Takagi K, Kitagawa T, Sugano H, et al. Ductectatic-type mucinous cystadenoma and cystadenocarcinoma of the human pancreas: a novel clinicopathological entity. Jpn J Cancer Res 1993;84:474-9.
22. Agostini S, Choux R, Payan MJ, Sastre B, Sahel J, Clement JP. Mucinous pancreatic duct ectasia in the body of the pancreas. Radiology 1989;170:815-6.
23. Adsay NV, Longnecker DS, Klimstra DS. Pancreatic tumors with cystic dilatation of the ducts: intraductal papillary mucinous neoplasm and intraductal oncocytic papillary neoplasms. Semin Diagn Pathol 2000;17:16-31.
24. Adsay NV, Klimstra DS, Compton CC. Cystic lesions of the pancreas. Semin Diagn Pathol 2000;17:1-6.
25. Thompson LDR, Becker RC, Pryzgodski RM, Adair CF, Heffess C. Mucinous cystic neoplasm (mucinous cystadenocarcinoma of low malignant potential) of the pancreas: a clinicopathologic study of 130 cases. Am J Surg Pathol 1999;23: 1-16.
26. Wilentz RE, Albores-Saavedra J, Hruban RH. Mucinous cystic neoplasms of the pancreas. Semin Diagn Pathol 2000;17: 31-43.
27. Zamboni G, Scarpa A, Bogina G, Iacono C, Bassi C, Talamini G, et al. Mucinous cystic tumors of the pancreas: clinicopathological features, prognosis, and relationship to other mucinous cystic tumors. Am J Surg Pathol 1999;23:410-22.
28. Klöppel G. Clinicopathologic view of intraductal papillarymucinous tumor of the pancreas. Hepatogastroenterology 1998;45:1981-5.
29. Azar C, Van de Stadt J, Rickaert F, Deviere M, Baize M, Klöppel G, et al. Intraductal papillary mucinous tumours of the pancreas. Clinical and therapeutic issues in 32 patients. Gut 1996;39:457-64.
30. Cellier C, Cuillerier E, Palazzo L, Rickaert F, Flejou JF, Napoleon B, et al. Intraductal papillary and mucinous tumors of the pancreas: accuracy of preoperative computed tomography, endoscopic retrograde pancreatography and endoscopic ultrasonography, and long-term outcome in a large surgical series. Gastrointest Endosc 1998;47:42-9.
31. Fukishima N, Mukai K, Kanai Y, Hasabe T, Shimada K, Ozaki H, et al. Intraductal papillary tumors and mucinous cystic tumors of the pancreas: clinicopathologic study of 38 cases. Hum Pathol 1997;28:1010-7.
32. Nagai E, Ueki T, Chijiiwa K, Tanaka M, Tsuneyoshi M. Intraductal papillary mucinous neoplasms of the pancreas associated with so-called "mucinous ductal ectasia." Histochemical and immunohistochemical analysis of 29 cases. Am J Surg Pathol 1995;19:576-89.
33. Sessa F, Solcia E, Capella C, Bonato M, Scarpa A, Zamboni G, et al. Intraductal papillary-mucinous tumours represent a distinct group of pancreatic neoplasms: an investigation of tumour cell differentiation and K-ras, p53 and c-erbB-2 abnormalities in 26 patients. Virchows Arch 1994;425:357-67.
34. Loftus EV Jr, Olivares-Pakzad BA, Batts, KP, Adkins MC, Stephens DH, Sarr MG, et al. Intraductal papillary-mucinous tumors of the pancreas: clinicopathologic features, outcome, and nomenclature. Members of the Pancreas Clinic, and Pancreatic Surgeons of Mayo Clinic. Gastroenterology 1996; 110:1909-18.
35. Adsay V, Conlon K, Brennan MF, Klimstra DS. Intraductal papillary mucinous neoplasms: a clinicopathologic study of in-situ and invasive carcinomas associated with 28 cases. Cancer 2002;94:62-77.
36. Yamao K, Ohashi K, Nakamura T, Suzuki T, Shimizu Y, Nakamura Y, et al. The prognosis of intraductal papillary mucinous tumors of the pancreas. Hepatogastroenterology 2000;47:1129-34.
37. Cuillerier E, Cellier C, Palazzo L, Deviere J, Wind P, Rickaert F, et al. Outcome after surgical resection of intraductal papillary and mucinous tumors of the pancreas. Am J Gastroenterol 2000;95:441-5.
38. Adsay NV, Pierson C, Sarkar F, Abrams J, Weaver D, Conlon KC, et al. Colloid (mucinous noncystic) carcinoma of the pancreas. Am J Surg Pathol 2001;25:26-42.
39. Siedel G, Iacobuzio-Donahue C, Sohn TA, Adsay NV, Yeo CJ, Lillemoe K, et al. Almost all infiltrating colloid carcinomas of the pancreas and periampullary region arise from in-situ papillary neoplasms: a study of 33 cases. Am J Surg Pathol 2002;26:56-63.
40. Luttges J, Brocker V, Kremer B, Klöppel G. Immunohistochemical mucin expression and DPC4 status in intraductal papillary mucinous tumors (IPMTs) of the pancreas [abstract]. Pancreas 2000;21:459.
41. Yonezawa S, Taira M, Osako M, Kubo M, Tanaka S, Sakoda K, et al. MUC-1 mucin expression in invasive areas of intraductal papillary mucinous tumors of the pancreas [letterl. Pathol Int 1998;48:319-22.
42. Yonezawa S, Horinouchi M, Osako M, Kubo M, Takao S, Arimura Y, et al. Gene expression of gastric type mucin (MUC5AC) in pancreatic tumors; its relationship with the biological behavior of the tumor. Pathol Int 1999;49:45-54.
43. Yonezawa S, Sato E. Expression of mucin antigens in human cancers and its relationship with malignancy potential. Pathol Int 1997;47:813-30.
44. Yonezawa S, Sueyoshi K, Nomoto M, Kitamura H, Nagata K, Arimura Y, et al. MUC2 gene expression is found in noninvasive tumors but not in invasive tumors of the pancreas and liver: its close relationship with prognosis of the patients. Hum Pathol 1997;28:344-52.
45. Osako M, Yonezawa S, Siddiki B, Huang J, Ho JJ, Kim YS, et al. Immunohistochemical study of mucin carbohydrates and core proteins in human pancreatic tumors. Cancer 1993; 71:2191-9.
46. Yonezawa S, Byrd JC, Dahiya R, Ho JJ, Gum JR, Griffiths B, et al. Differential mucin gene expression in human pancreatic and colon cancer cells. Biochem J 1991;276:599-605.
47. Yuan M. Histological localization of mucin core polypeptide MUC-2 in application to the differential diagnosis of adenocarcinoma. Chung Hua Ping Li Hsueh Tsa Chih 1992;21:139-41.
48. Hollingsworth MA, Strawhecker JM, Caffrey TC, Mack DR. Expression of MUC1, MUC2, MUC3 and MUC4 mucin mRNAs in human pancreatic and intestinal tumor cell lines. Int J Cancer 1994;57:198-203.
49. Balague C, Gambus G, Carrato C, Porchet N, Aubert JP, Kim YS, et al. Altered expression of MUC2, MUC4, and MUC5 mucin genes in pancreas tissues and cancer cell lines. Gastroenterology 1994;106:1054-61.
50. Luttges J, Zamboni G, Longnecker D, Klöppel G. The immunohistochemical mucin expression pattern distinguishes different types of intraductal papillary mucinous neoplasms of the pancreas and determines their relationship to mucinous noncystic carcinoma and ductal adenocarcinoma. Am J Surg Pathol 2001;25:942-8.
51. Merati K, Klimstra DS, Abrams J, Hruban RH, Iacobuzio-Donahue CD, Sarkar F, et al. Intraductal papillary mucinous neoplasms (IPMNs) of the pancreas exhibit three morphologically and immunophenotypically distinct epithelium [abstract]. Mod Pathol 2001;14:200A.
52. Andea A, Munn T, Sarkar F, Cheng JD, Adsay NV. A comparative analysis of pancreatic intraepithelial neoplasia (PanIN) in malignant and benign pancreata [abstract]. Mod Pathol 2002;15:282A.
53. Brockie E, Anand A, Albores-Saavedra J. Progression of atypical ductal hyperplasia/carcinoma in situ of the pancreas to invasive adenocarcinoma. Ann Diagn Pathol 1998;2:286-92.
54. Volkholz H, Stolte M, Becker V. Epithelial dysplasias in chronic pancreatitis. Virchows Archiv A Pathol Anat Histol 1982;396:331-49.
55. Grignon D. Neoplasms of the urinary bladder. In: Bostwick D, Eble J, editors. Urologic surgical pathology. St. Louis, MO: Mosby; 1996. p. 225-30.
56. Fujii H, Inagaki M, Kasai S, Miyokawa N, Tokusashi Y, Gabrielson E, et al. Genetic progression and heterogeneity in intraductal papillary-mucinous neoplasms of the pancreas. Am J Pathol 1997;151:1447-54.
57. Gloor E, Hurlimann J. Cervical intraepithelial glandular neoplasia (adenocarcinoma in situ and glandular dysplasia). A correlative study of 23 cases with histologic grading, histochemical analysis of mucins, and immunohistochemical determination of the affinity for four lectins. Cancer 1986;58: 1272-80.
58. Griffioen G, Bosman FT, Verspaget HW, de Bruin PA, Biemond I, Lamers CB. Mucin profiles and potential for malignancy of human colorectal adenomatous polyps. Cancer 1989;63:1587-91.
59. Agawa S, Jass JR. Sialic acid histochemistry and the adenoma-carcinoma sequence in colorectum. J Clin Pathol 1990;43:527-32.
60. Peuchmaur M, Potet F, Goldfain D. Mucin histochemistry of the columnar epithelium of the oesophagus (Barrett's oesophagus): a prospective biopsy study. J Clin Pathol 1984;37: 607-10.
61. Lapertosa G, Baracchini P, Fulcheri E. Mucin histochemical analysis in the interpretation of Barrett's esophagus. Results of a multicenter study. The Operative Group for the Study of Esophageal Precancer. Am J Clin Pathol 1992;98:61-6.
62. Yamao K, Nakazawa S, Fujimoto M, Tsuda H, Matsumoto K, Iwase T. A mucous histochemical and immunohistochemical study of precancerous and neoplastic lesions in the human pancreas. Int J Pancreatol 1993;14:37-44.
63. Xerri L, Payan MJ, Choux R, Gros N, Figarella-Branger D, Sarles H. Predominance of sialomucin secretion in malignant and premalignant pancreatic lesions. Hum Pathol 1990; 21:927-31.
64. Kimura W, Nagai H, Kuroda A, Muto T, Esaki Y. Analysis of small cystic lesions of the pancreas. Int J Pancreatol 1995; 18:197-206.
65. Ende VV, Riniker P. Gelatinous carcinoma of the appendix. Schweiz Med Wochenschr 1969;99:716-8.
66. Jacobson J, Ying L, Hoda S. Pure mammary mucinous carcinoma: an invasive or a non-invasive neoplasm [abstract]? Mod Pathol 1998;11:11A.
67. Rosai J. Ackerman's surgical pathology. Vol 2. St. Louis: Mosby, 1996. p. 1607-9.