Expression of von Hippel-Lindau Gene Product (pVHL) and S100P in cystic neoplasms of the pancreas - with an implication for their roles in tumorigenesis

Annals of Clinical and Laboratory Science

Volumn 42, Issue 2, 2012, Pages 109-117

  Liu, Haiyan ^a   Shi, Jianhui ^a   Wang, Hanlin L ^b   Zhang, Jun ^c   Brown, Robert E ^d   Wilkerson, Myra ^a   Lin, Fan ^a  

^a GEISINGER MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAYO CLINIC   (United States)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Intraductal papillary mucinous neoplasm; Mucinous cystic neoplasm; S100P; Serous microcystic adenoma; Solid pseudopapillary tumor; Von Hippel Lindau Gene Product (pVHL)

Indexed keywords

PROTEIN S 100; VON HIPPEL LINDAU PROTEIN;

ADENOMA; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DYSPLASIA; GENE EXPRESSION; GENE PRODUCT; HUMAN; IMMUNOHISTOCHEMISTRY; INTRADUCTAL PAPILLARY MUCINOUS TUMOR; MAJOR CLINICAL STUDY; MUCINOUS CYSTIC NEOPLASM; PANCREAS ADENOCARCINOMA; PANCREAS ADENOMA; PANCREAS CANCER; PRIORITY JOURNAL; SEROUS MICROCYSTIC ADENOMA; SOLID PSEUDOPAPILLARY TUMOR;

ADENOMA; CALCIUM-BINDING PROTEINS; CARCINOMA, PAPILLARY; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASM PROTEINS; NEOPLASMS, CYSTIC, MUCINOUS, AND SEROUS; PANCREATIC NEOPLASMS; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84864130232     PISSN: 00917370     EISSN: 15508080     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Becker T, Gerke V, Kube E, Weber K. S100P, a novel Ca (2+)-binding protein from human placenta. cDNA cloning, recombinant protein expression and Ca2+ binding properties. Eur J Biochem 1992;207:541-547.
2. Dowen SE, Crnogorac-Jurcevic T, Gangeswaran R, Hansen M, Eloranta JJ, Bhakta V, Brentnall TA, Lüttges J, Klöppel G, Lemoine NR. Expression of S100P and its novel binding partner S100PBPR in early pancreatic cancer. Am J Pathol 2005;166:81-92.
3. Lin F, Shi J, Liu H, Hull ME, Dupree W, Prichard JW, Brown RE, Zhang J, Wang HL, Schuerch C. Diagnostic utility of S100P and von Hippel-Lindau gene product (pVHL) in pancreatic adenocarcinoma-with implication of their roles in early tumorigenesis. Am J Surg Pathol 2008;32:78-91.
4. Ohuchida K, Mizumoto K, Egami T, Yamaguchi H, Fujii K, Konomi H, Nagai E, Yamaguchi K, Tsuneyoshi M, Tanaka M. S100P is an early developmental marker of pancreatic carcinogenesis. Clin Cancer Res 2006;12:5411-5416.
5. Dorion P, Shi J, Zhang K, Schuerch C, Lin F. Utility of S100P in differentiating adenocarcinoma of the lung from papillary carcinoma and follicular carcinoma of the thyroid. Mod Pathol 2008;21:340A, #1551.
6. Higgins JP, Kaygusuz G, Wang L, Montgomery K, Mason V, Zhu SX, Marinelli RJ, Presti JC Jr, van de Rijn M, Brooks JD. Placental S100 (S100P) and GATA3: markers for transitional epithelium and urothelial carcinoma discovered by complementary DNA microarray. Am J Surg Pathol 2007;31:673-680.
7. Sato N, Maitra A, Fukushima N, van Heek NT, Matsubayashi H, Iacobuzio-Donahue CA, Rosty C, Goggins M. Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Cancer Res 2003;63:4158-4166.
8. Arumugam T, Simeone DM, Van Golen K, Logsdon CD. S100P promotes pancreatic cancer growth, survival and invasion. Clin Cancer Res 2005;11:5356-5364.
9. Lonser RR, Glenn GM, Walther M, Chew EY, Libutti SK, Linehan WM, Oldfield EH. von Hippel-Lindau disease. Lancet 2003;361:2059-2067.
10. Seizinger BR, Smith DI, Filling-Katz MR, Neumann H, Green JS, Choyke PL, Anderson KM, Freiman RN, Klauck SM, Whaley J, Decker H-JH, Hsia YE, Scherer G, Drabkin HA, Aronin N, Schinzel A, Martuza RL, Gusella JF, Haines JL. Genetic flanking markers refine diagnostic criteria and provide insights into the genetics of Von Hippel Lindau disease. Proc Natl Acad Sci U S A 1991;88:2864-2868.
11. Kaelin WG Jr. Molecular basis of the VHL hereditary cancer syndrome. Nat Rev Cancer 2002;2:673-682.
12. Lin F, Shi J, Liu H, Zhang J, Zhang PL, Wang HL, Yang XJ, Schuerch C. Immunohistochemical detection of the von Hippel-Lindau gene product (pVHL) in human tissues and tumors: a useful marker for metastatic renal cell carcinoma and clear cell carcinoma of the ovary and uterus. Am J Clin Pathol 2008;12:592-605.
13. Hruban RH, Pitman MB, Klimstra DS. Atlas of Tumor Pathology: Tumors of the Pancreas, Series 4, Armed Forces Institute of Pathology, Washington DC, 2007; pp 51-110.
14. Solcia E, Capella C, Kloppel G. Atlas of Tumor Pathology: Tumors of the Pancreas, Series 3, Armed Forces Institute of Pathology, Washington, DC, 1997; pp 41-63.
15. DiGiuseppe JA, Hruban RH, Goodman SN, Polak M, van den Berg FM, Allison DC, Cameron JL, Offerhaus GJ. Overexpression of p53 protein in adenocarcinoma of the pancreas. Am J Clin Pathol 1994;101:684-688.
16. Lüttges J, Galehdari H, Bröcker V, Schwarte-Waldhoff I, Henne-Bruns D, Klöppel G, Schmiegel W, Hahn SA. Allelic loss is often the first hit in the biallelic inactivation of the p53 and DPC4 genes during pancreatic carcinogenesis. Am J Pathol 2001;158:1677-1683.
17. Satoh K, Shimosegawa T, Moriizumi S, Koizumi M, Toyota T. K-ras mutation and p53 protein accumulation in intraductal mucin-hypersecreting neoplasms of the pancreas. Pancreas 1996;12:362-368.
18. Wada K. p16 and p53 gene alterations and accumulations in the malignant evolution of intraductal papillary-mucinous tumors of the pancreas. J Hepatobiliary Pancreat Surg 2002;9:76-85.
19. Hoshi T, Imai M, Ogawa K. Frequent K-ras mutations and absence of p53 mutations in mucin-producing tumors of the pancreas. J Surg Oncol 1994;55:84-91.
20. House MG, Guo M, Iacobuzio-Donahue C, Herman JG. Molecular progression of promoter methylation in intraductal papillary mucinous neoplasms (IPMN) of the pancreas. Carcinogenesis 2003;24(2):193-198.
21. Satoh K, Sawai T, Shimosegawa T, Koizumi M, Yamazaki T, Mochizuki F, Toyota T. The point mutation of c-Ki-ras at codon 12 in carcinoma of the pancreatic head region and in intraductal mucin-hypersecreting neoplasm of the pancreas. Int J Pancreatol 1993;14:135-143.
22. Sessa F, Solcia E, Capella C, Bonato M, Scarpa A, Zamboni G, Pellegata NS, Ranzani GN, Rickaert F, Klöppel G. 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;425:357-367.
23. Yamaguchi K, Chijiiwa K, Noshiro H, Torata N, Kinoshita M, Tanaka M. Ki-ras codon 12 point mutation and p53 mutation in pancreatic diseases. Hepatogastroenterology 1999;46:2575-2581.
24. Yoshizawa K, Nagai H, Sakurai S, Hironaka M, Morinaga S, Saitoh K, Fukayama M. Clonality and K-ras mutation analyses of epithelia in intraductal papillary mucinous tumor and mucinous cystic tumor of the pancreas. Virchows Arch 2002;441:437-443.
25. Z'graggen K, Rivera JA, Compton CC, Pins M, Werner J, Fernández-del Castillo C, Rattner DW, Lewandrowski KB, Rustgi AK, Warshaw AL. Prevalence of activating K-ras mutations in the evolutionary stages of neoplasia in intraductal papillary mucinous tumors of the pancreas. Ann Surg 1997;226:491-498; discussion 498-500.
26. Biankin AV, Biankin SA, Kench JG, Morey AL, Lee CS, Head DR, Eckstein RP, Hugh TB, Henshall SM, Sutherland RL. Aberrant p16(INK4A) and DPC4/Smad4 expression in intraductal papillary mucinous tumours of the pancreas is associated with invasive ductal adenocarcinoma. Gut 2002;50:861-868.
27. Wilentz RE, Geradts J, Maynard R, Offerhaus GJ, Kang M, Goggins M, Yeo CJ, Kern SE, Hruban RH. Inactivation of the p16 (INK4A) tumor-suppressor gene in pancreatic duct lesions: loss of intranuclear expression. Cancer Res 1998;58:4740-4744.
28. Sasaki S, Yamamoto H, Kaneto H, Ozeki I, Adachi Y, Takagi H, Matsumoto T, Itoh H, Nagakawa T, Miyakawa H, Muraoka S, Fujinaga A, Suga T, Satoh M, Itoh F, Endo T, Imai K. Differential roles of alterations of p53, p16, and SMAD4 expression in the progression of intraductal papillary-mucinous tumors of the pancreas. Oncol Rep 2003;10:21-25.
29. Iacobuzio-Donahue CA, Klimstra DS, Adsay NV, Wilentz RE, Argani P, Sohn TA, Yeo CJ, Cameron JL, Kern SE, Hruban RH. Dpc-4 protein is expressed in virtually all human intraductal papillary mucinous neoplasms of the pancreas: comparison with conventional ductal adenocarcinomas. Am J Pathol 2000;157:755-761.
30. Nakata B, Yashiro M, Nishioka N, Aya M, Yamada S, Takenaka C, Ohira M, Ishikawa T, Nishino H, Wakasa K, Seki S, Hirakawa K. Very low incidence of microsatellite instability in intraductal papillary-mucinous neoplasm of the pancreas. Int J Cancer 2002;102:655-659.
31. Fukushima N, Sato N, Sahin F, Su GH, Hruban RH, Goggins M. Aberrant methylation of suppressor of cytokine signalling-1 (SOCS-1) gene in pancreatic ductal neoplasms. Br J Cancer 2003;89:338-343.
32. Kashima K, Ohike N, Mukai S, Sato M, Takahashi M, Morohoshi T. Expression of the tumor suppressor gene maspin and its significance in intraductal papillary mucinous neoplasms of the pancreas. Hepatobiliary Pancreat Dis Int 2008;7:86-90.
33. Sato N, Fukushima N, Matsubayashi H, Goggins M. Identification of maspin and S100P as novel hypomethylation targets in pancreatic cancer using global gene expression profiling. Oncogene 2004;23:1531-1538.
34. Gold DV, Karanjawala Z, Modrak DE, Goldenberg DM, Hruban RH. PAM4-reactive MUC1 is a biomarker for early pancreatic adenocarcinoma. Clin Cancer Res 2007;13:7380-7387.
35. Kim SG, Wu TT, Lee JH, Yun YK, Issa JP, Hamilton SR, Rashid A. Comparison of epigenetic and genetic alterations in mucinous cystic neoplasm and serous microcystic adenoma of pancreas. Mod Pathol 2003;16:1086-1094.
36. Fukushima N, Sato N, Prasad N, Leach SD, Hruban RH, Goggins M. Characterization of gene expression in mucinous cystic neoplasms of the pancreas using oligonucleotide microarrays. Oncogene 2004;23:9042-9051.
37. Bartsch D, Bastian D, Barth P, Schudy A, Nies C, Kisker O, Wagner HJ, Rothmund M. K-ras oncogene mutations indicate malignancy in cystic tumors of the pancreas. Ann Surg 1998;228:79-86.
38. Fléjou JF, Boulange B, Bernades P, Belghiti J, Hénin D. p53 protein expression and DNA ploidy in cystic tumors of the pancreas. Pancreas 1996;13:247-252.
39. Cheng TY, Su CH, Shyr YM, Liu WY. Management of pancreatic lesions in von Hippel-Lindau disease. World J Surg 1997;21:307-312.
40. Mohr VH, Vortmeyer AO, Zhuang Z, Libutti SK, Walther MM, Choyke PL, Zbar B, Linehan WM, Lubensky IA. Histopathology and molecular genetics of multiple cysts and microcystic (serous) adenomas of the pancreas in von Hippel-Lindau patients. Am J Pathol 2000;157:1615-1621.
41. Vortmeyer AO, Lubensky IA, Fogt F, Linehan WM, Khettry U, Zhuang Z. Allelic deletion and mutation of the von Hippel-Lindau (VHL) tumor suppressor gene in pancreatic microcystic adenomas. Am J Pathol 1997;151:951-956.
42. Abraham SC, Klimstra DS, Wilentz RE, Yeo CJ, Conlon K, Brennan M, Cameron JL, Wu TT, Hruban RH. Solidpseudopapillary tumors of the pancreas are genetically distinct from pancreatic ductal adenocarcinomas and almost always harbor beta-catenin mutations. Am J Pathol 2002;160:1361-1369.
43. Kim MJ, Jang SJ, Yu E. Loss of E-cadherin and cytoplasmicnuclear expression of beta-catenin are the most useful immunoprofiles in the diagnosis of solid-pseudopapillary neoplasm of the pancreas. Hum Pathol 2008;39:251-258
44. Peruzzi B, Athauda G, Bottaro DP. The von Hippel-Lindau tumor suppressor gene product represses oncogenic betacatenin signaling in renal carcinoma cells. Proc Natl Acad Sci U S A 2006;103:14531-14536.
45. Schmidt-Ott KM, Masckauchan TN, Chen X, Hirsh BJ, Sarkar A, Yang J, Paragas N, Wallace VA, Dufort D, Pavlidis P, Jagla B, Kitajewski J, Barasch J. Beta-catenin/TCF/Lef controls a differentiation-associated transcriptional program in renal epithelial progenitors. Development 2007;134:3177-3190.