Pancreatic intraepithelial neoplasia and pancreatic tumorigenesis: Of mice and men

Archives of Pathology and Laboratory Medicine

Volumn 133, Issue 3, 2009, Pages 375-381

  Ottenhof, Niki A ^a   Milne, Anya N A ^a   Morsink, Folkert H M ^a   Drillenburg, Paul ^b   Ten Kate, Fiebo J W ^a   Maitra, Anirban ^c   Offerhaus, G Johan ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ONZE LIEVE VROUWE GASTHUIS   (Netherlands)

^c DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER INVASION; CANCER MODEL; CANCER SURVIVAL; CARCINOGENESIS; EARLY DIAGNOSIS; GENE MUTATION; HUMAN; NONHUMAN; ONCOGENE; PANCREAS CANCER; PANCREATIC INTRAEPITHELIAL NEOPLASIA; PROGNOSIS; REVIEW; SURVIVAL RATE; SURVIVAL TIME; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE;

ADENOCARCINOMA; ANIMALS; CARCINOMA IN SITU; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; MICE; MICE, TRANSGENIC; PANCREATIC NEOPLASMS; PROGNOSIS;

EID: 62249126245     PISSN: 00039985     EISSN: 15432165     Source Type: Journal    
DOI: None     Document Type: Review

References (80)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin. 2006;56:106-130.
2. American Cancer Society. Cancer Facts & Figures 2007. Atlanta, GA: American Cancer Society; 2007:1-52.
3. Sohn TA, Yeo CJ, Cameron JL, et al. Resected adenocarcinoma of the pancreas-616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg. 2000;4:567-579.
4. Winter JM, Cameron JL, Campbell KA, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: a single-institution experience. J Gastrointest Surg. 2006;10:1199-1210.
5. Li D, Xie K, Wolff R, Abbruzzese JL. Fancreatic cancer. Lancet. 2004;363:1049-1057.
6. Hruban RH, Adsay NV, Albores-Saavedra J, et al. Fancreatic intraepithelial neoplasia: a new nomenclature and classification system for pancreatic duct lesions. Am J Surg Pathol. 2001;25:579-586.
7. Hruban RH, Takaori K, Klimstra DS, et al. An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillarymucinous neoplasms. Am J Surg Pathol. 2004;28:977-987.
8. Maitra A, Adsay NV, Argani F, et al. Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray. Mod Pathol. 2003;16:902-912.
9. Leach SD. Mouse models of pancreatic cancer: the fur is finally flying! Cancer Cell. 2004;5:7-11.
10. Hruban RH, Klimstra DS, Pitman MB. Tumors of the Pancreas. Washington, DC: Armed Forces Institute of Pathology; 2007. Atlas of Tumor Pathology; 4th series, fascicle 6.
11. Cubilla AL, Fitzgerald PJ. Morphological lesions associated with human primary invasive nonendocrine pancreas cancer. Cancer Res. 1976;36:2690-2698.
12. Andea A, Sarkar F, Adsay VN. Clinicopathological correlates of pancreatic intraepithelial neoplasia: a comparative analysis of 82 cases with and 152 cases without pancreatic ductal adenocarcinoma. Mod Pathol. 2003;16:996-1006.
13. 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;22:163-169.
14. Kornmann M, Ishiwata T, Itakura J, Tangvoranuntakul P, Beger HG, Korc M. Increased cyclin D1 in human pancreatic cancer is associated with decreased postoperative survival. Oncology. 1998;55:363-369.
15. van Rees BP, Ristimaki A. Cyclooxygenase-2 in carcinogenesis of the gastrointestinal tract. Scand J Gastroenterol. 2001;36:897-903.
16. Maitra A, Ashfaq R, Gunn CR, et al. Cyclooxygenase 2 expression in pancreatic adenocarcinoma and pancreatic intraepithelial neoplasia: an immunohis-tochemical analysis with automated cellular imaging. Am J Clin Pathol. 2002;118:194-201.
17. Keller JJ, Giardiello FM. Chemoprevention strategies using NSAIDs and COX-2 inhibitors. Cancer Biol Ther. 2003;2:140S-149S.
18. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell.1996;87:159-170.
19. Hruban RH, Goggins M, Parsons J, Kern SE. Progression model for pancreatic cancer. Clin Cancer Res. 2000;6:2969-2972.
20. Hruban RH, van Mansfeld AD, Offerhaus GJ, et al. K-ras oncogene activation in adenocarcinoma of the human pancreas: a study of 82 carcinomas using a combination of mutant-enriched polymerase chain reaction analysis and allelespecific oligonucleotide hybridization. Am J Pathol. 1 993;143:545-554.
21. Sturm PD, Hruban RH, Ramsoekh TB, et al. The potential diagnostic use of K-ras codon 12 and p53 alterations in brush cytology from the pancreatic head region. J Pathol. 1998;186:247-253.
22. Tascilar M, Caspers E, Sturm PD, Goggins M, Hruban RH, Offerhaus GJ. Role of tumor markers and mutations in cells and pancreatic juice in the diagnosis of pancreatic cancer. Ann Oncol. 1999;10(suppl 4):107-110.
23. Hingorani SR, Tuveson DA. Ras redux: rethinking how and where Ras acts. Curr Opin Genet Dev. 2003;13:6-13.
24. Löhr M, Klöppel G, Maisonneuve P, Lowenfels AB, Lüttges J. Frequency of K-ras mutations in pancreatic intraductal neoplasias associated with pancreatic ductal adenocarcinoma and chronic pancreatitis: a meta-analysis. Neoplasia. 2005;7:17-23.
25. Lüttges 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;88:2495-2504.
26. Hingorani SR, Petricoin EF, Maitra A, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. CancerCell.2003;4:437-450.
27. WooPark S, Davison JM, Rhee J, Hruban RH, Maitra A, Leach SD. Oncogenic KRAS induces progenitor cell expansion and malignant transformation in zebrafish exocrine pancreas. Gastroenterology. 2008;134:2080-2090.
28. van Es JM, Polak MM, van den Berg FM, et al. Molecular markers for diagnostic cytology of neoplasms in the head region of the pancreas: mutation of K-ras and overexpression of the p53 protein product. J Clin Pathol. 1995;48:218-222.
29. Sturm PD, Rauws EA, Hruban RH, et al. Clinical value of K-ras codon 12 analysis and endobiliary brush cytology for the diagnosis of malignant extrahepatic bile duct stenosis. Clin Cancer Res. 1999;5:629-635.
30. van Heek NT, Rauws EA, Caspers E, Drillenburg P, Gouma DJ, Offerhaus GJ. Long-term follow-up of patients with a clinically benign extrahepatic biliary stenosis and K-ras mutation in endobiliary brush cytology. Gastrointest Endosc. 2002;55:883-888.
31. Brentnall TA, Bronner MP, Byrd DR, Haggitt RC, Kimmey MB. Early diagnosis and treatment of pancreatic dysplasia in patients with a family history of pancreatic cancer. Ann Intern Med. 1999;131:247-255.
32. Karp JE, Lancet JE. Development of farnesyltransferase inhibitors for clinical cancer therapy: focus on hematologic malignancies. CancerInvest. 2007;25:484-494.
33. Caldas C, Hahn SA, da Costa LT, et al. Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nat Genet. 1994;8:27-32.
34. Schutte M, Hruban RH, Geradts J, et al. Abrogation of the Rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Cancer Res.1997;57:3126-3130.
35. Sherr CJ. Cell cycle control and cancer. Harvey Lect. 2000-2001;96:73-92.
36. Sellers WR, Rodgers JW, Kaelin WG Jr. A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc Natl Acad Sci USA. 1995;92:11544-11548.
37. Wilentz RE, Geradts J, Maynard R, et al. Inactivation of the p16 (INK4A) tumor-suppressor gene in pancreatic duct lesions: loss of intranuclear expression. Cancer Res. 1998;58:4740-4744.
38. de Vos tot Nederveen Cappel WH, Offerhaus GJ, van Puijenbroek M, et al. Pancreatic carcinoma in carriers of a specific 19 base pair deletion of CDKN2A/p16 (p16-leiden). Clin Cancer Res. 2003;9:3598-3605.
39. Koorstra JB, Hustinx SR, Offerhaus GJ, MaitraA. Pancreatic carcinogenesis. Pancreatology. 2008;8:110-125.
40. Hustinx SR, Leoni LM, Yeo CJ, et al. Concordant loss of MTAP and p16/CDKN2A expression in pancreatic intraepithelial neoplasia: evidence of homozygous deletion in a noninvasive precursor lesion. Mod Pathol. 2005;18:959-963.
41. Kern SE, Kinzler KW, Bruskin A, et al. Identification of p53 as a sequence-specific DNA-binding protein. Science. 1991;252:1708-1711.
42. Kern SE. p53: tumor suppression through control of the cell cycle. Gastroenterology. 1994;106:1708-1711.
43. Redston MS, Caldas C, Seymour AB, et al. p53 mutations in pancreatic carcinoma and evidence of common involvement of homocopolymer tracts in DNA microdeletions. Cancer Res. 1994;54:3025-3033.
44. Baas IO, Mulder JW, Offerhaus GJ, Vogelstein B, Hamilton SR. An evaluation of six antibodies for immunohistochemistry of mutant p53 gene product in archival colorectal neoplasms. J Pathol. 1994;172:5-12.
45. Tascilar M, Sturm PD, Caspers E, et al. Diagnostic p53 immunostaining of endobiliary brush cytology: preoperative cytology compared with the surgical specimen. Cancer. 1999;87:306-311.
46. Schutte M, Hruban RH, Hedrick L, et al. DPC4 gene in various tumor types. Cancer Res. 1996;56:2527-2530.
47. Hahn SA, Schutte M, Hoque AT, et al. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science. 1996;271:350-353.
48. Wilentz RE, Su GH, Dai JL, et al. Immunohistochemical labeling for dpc4 mirrors genetic status in pancreatic adenocarcinomas: a new marker of DPC4 inactivation. Am J Pathol. 2000;156:37-43.
49. Wilentz RE, Iacobuzio-Donahue CA, Argani P, et al. Loss of expression of Dpc4 in pancreatic intraepithelial neoplasia: evidence that DPC4 inactivation occurs late in neoplastic progression. Cancer Res. 2000;60:2002-2006.
50. Blobe GC, Schiemann WP, Lodish HF. Role of transforming growth factor beta in human disease. N Engl J Med. 2000;342:1350-1358.
51. van der Heijden MS, Yeo CJ, Hruban RH, Kern SE. Fanconi anemia gene mutations in young-onset pancreatic cancer. Cancer Res. 2003;63:2585-2588.
52. van der Heijden MS, Brody JR, Gallmeier E, et al. Functional defects in the Fanconi anemia pathway in pancreatic cancer cells. Am J Pathol. 2004;165:651-657.
53. van der Heijden MS, Brody JR, Dezentje DA, et al. In vivo therapeutic responses contingent on Fanconi anemia/BRCA2 status of the tumor. Clin Cancer Res. 2005;11:7508-7515.
54. Goggins M, Schutte M, Lu J, et al. Germline BRCA2 gene mutations in patients with apparently sporadic pancreatic carcinomas. Cancer Res. 1996;56:5360-5364.
55. Hahn SA, Greenhalf B, Ellis I, et al. BRCA2 germline mutations in familial pancreatic carcinoma. J Natl Cancer Inst. 2003;95:214-221.
56. Goggins M, Hruban RH, Kern SE. BRCA2 is inactivated late in the development of pancreatic intraepithelial neoplasia: evidence and implications. Am J Pathol. 2000;156:1767-1771.
57. Goggins M, Offerhaus GJ, Hilgers W, et al. Pancreatic adenocarcinomas with DNA replication errors (RER+) are associated with wild-type K-ras and characteristic histopathology: poor differentiation, a syncytial growth pattern, and pushing borders suggest RER+. Am J Pathol. 1998;152:1 501-1507.
58. Wilentz RE, Goggins M, Redston M, et al. Genetic, immunohistochemical, and clinical features of medullary carcinoma of the pancreas: a newly described and characterized entity. Am J Pathol. 2000;156:1641-1651.
59. van Heek NT, Meeker AK, Kern SE, et al. Telomere shortening is nearly universal in pancreatic intraepithelial neoplasia. Am J Pathol. 2002;161:1541-1547.
60. Maitra A, Kern SE, Hruban RH. Molecular pathogenesis of pancreatic cancer. Best Pract Res Clin Gastroenterol. 2006;20:211-226.
61. Kim SK, MacDonald RJ. Signaling and transcriptional control ofpancreatic organogenesis. Curr Opin Genet Dev. 2002;12:540-547.
62. Hebrok M, Kim SK, Melton DA. Notochord repression of endodermal Sonic hedgehog permits pancreas development. Genes Dev. 1998;12:1705-1713.
63. Hebrok M, Kim SK, St Jacques B, McMahon AP, Melton DA. Regulation of pancreas development by hedgehog signaling. Development.2000;127:4905- 4913.
64. Offield MF, Jetton TL, Labosky PA, et al. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development. 1996;122:983-995.
65. Li H, Arber S, Jessell TM, Edlund H. Selective agenesis of the dorsal pancreas in mice lacking homeobox gene Hlxb9. Nat Genet. 1999;23:67-70.
66. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet. 2002;32:128-134.
67. Schwitzgebel VM. Programming of the pancreas. Mol Cell Endocrinol. 2001;185:99-108.
68. Apelqvist A, Li H, Sommer L, et al. Notch signalling controls pancreatic cell differentiation. Nature. 1999;400:877-881.
69. Esni F, Ghosh B, Biankin AV, et al. Notch inhibits Ptf1 function and acinar cell differentiation in developing mouse and zebrafish pancreas. Development. 2004;131:4213-4224.
70. Miyamoto Y, Maitra A, Ghosh B, et al. Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell. 2003;3:565-576.
71. Berman DM, Karhadkar SS, Maitra A, et al. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature.2003;425:846-851.
72. van den Brink GR, Offerhaus GJ. The morphogenetic code and colon cancer development. Cancer Cell. 2007;11:109-117.
73. Hruban RH, Adsay NV, Albores-Saavedra J, et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations. Cancer Res. 2006;66:95-106.
74. Aguirre AJ, Bardeesy N, Sinha M, et al. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev. 2003;17:3112-3126.
75. Hingorani SR, Wang L, Multani AS, et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell. 2005;7:469-483.
76. Guerra C, Schuhmacher AJ, Cañamero M, et al. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell. 2007;11:291-302.
77. Murtaugh LC, Leach SD. A case of mistaken identity?: nonductal origins of pancreatic "ductal" cancers. Cancer Cell. 2007;11:211-213.
78. Boerma D, Straatsburg IH, Offerhaus GJ, Gouma DJ, van Gulik TM. Experimental model of obstructive, chronic pancreatitis in pigs. Dig Surg. 2003;20:520-526.
79. Brune K, Abe T, Canto M, et al. Multifocal neoplastic precursor lesions associated with lobular atrophy of the pancreas in patients having a strong family history of pancreatic cancer. Am J Surg Pathol. 2006;30:1067-1076.
80. Shi C, Hong SM, Lim P, et al. KRAS2 gene mutations in human pancreatic acinar-ductal metaplastic lesions are limited to those associated with pancreatic intraepithelial neoplasia. Mol Cancer Res. 2009. In press.