DOI: 10.1002/path.1711610305. The c‐erbB‐2 proto‐oncogene in human pancreatic cancer

The c‐erbB‐2 proto‐oncogene in human pancreatic cancer

10.1002/path.1711610305

Crossref journal-article

Wiley

The Journal of Pathology (311)

Abstract

AbstractThe c‐erbB‐2 oncogene encodes a 190 kD transmembrane growth factor receptor which is closely related to the EGF receptor and has been found to be amplified and overexpressed in a number of human adenocarcinomas, particularly of the breast. We have analysed, by immunocytochemistry using the 21N antibody, expression of c‐erbB‐2 in a retrospective series of pancreatic adenocarcinoma, chronic pancreatitis, and examples of histologically normal pancreas. In three cases (21 per cent) of chronic pancreatitis, there were focal areas of cytoplasmic immunoreactivity in regenerating epithelium. In 15 cases (17 per cent) of pancreatic adenocarcinoma, cytoplasmic immunoreactivity was seen, while in two cases (2 per cent) strong membrane staining of tumour cells was seen which could be blocked by peptide controls. c‐erbB‐2 immunoreactivity was also demonstrated using a second antibody, 20N, which recognizes another peptide sequence of the c‐erbB‐2 protein. There was no relationship between immunoreactivity and histological subtype or grade, but there was absolute concordance between staining in primary and metastatic deposits. Since the rat homologue (neu) of the c‐erbB‐2 oncogene may be activated by a specific point mutation in its transmembrane region, we have analysed 23 cases from this series for mutations by polymerase chain reaction amplification and sequence‐specific oligonucleotide hybridization. We were unable to identify activity mutations in this series. These data suggest that there is abnormal expression of c‐erbB‐2 oncogene in nearly 20 per cent of cases although mutational activation of this gene is not seen in human pancreatic adenocarcinoma.

Bibliography

Hall, P. A., Hughes, C. M., Staddon, S. L., Richman, P. I., Gullick, W. J., & Lemoine, N. R. (1990). The câerbBâ2 protoâoncogene in human pancreatic cancer. The Journal of Pathology, 161(3), 195â200. Portico.

Authors 6

P. A. Hall (first)
C. M. Hughes (additional)
S. L. Staddon (additional)
P. I. Richman (additional)
W. J. Gullick (additional)
N. R. Lemoine (additional)

References 41 Referenced 127

10.1016/0092-8674(88)90571-5
10.1093/nar/16.16.7773
10.1002/ijc.2910430614
10.1111/j.1349-7006.1989.tb01687.x
{'key': 'e_1_2_1_6_2', 'first-page': '1137', 'article-title': 'Direct sequencing analyses of exon 1 of the c‐K‐ras gene shows a low frequency of mutations in human pancreatic‐adenocarcinoma', 'volume': '4', 'author': 'Gonzales‐Cadavid NF', 'year': '1989', 'journal-title': 'Oncogene'} / Oncogene / Direct sequencing analyses of exon 1 of the c‐K‐ras gene shows a low frequency of mutations in human pancreatic‐adenocarcinoma by Gonzales‐Cadavid NF (1989)
{'key': 'e_1_2_1_7_2', 'first-page': '3713', 'article-title': 'Oncogenes, anti‐oncogenes and the molecular basis of multistep carcinogenesis', 'volume': '49', 'author': 'Weinberg RA', 'year': '1989', 'journal-title': 'Cancer Res'} / Cancer Res / Oncogenes, anti‐oncogenes and the molecular basis of multistep carcinogenesis by Weinberg RA (1989)
10.1038/304596a0
10.1038/312513a0
10.1002/ijc.2910400221
10.1016/S0140-6736(86)91782-4
{'key': 'e_1_2_1_12_2', 'first-page': '38', 'volume-title': 'The Molecular Basis of Cancer', 'author': 'Gullick WJ', 'year': '1989'} / The Molecular Basis of Cancer by Gullick WJ (1989)
10.1126/science.3798106
10.1016/S0140-6736(87)92736-X
10.1007/BF02899192
10.1038/bjc.1988.238
10.1016/0092-8674(86)90779-8
10.1128/MCB.8.9.3969
10.1038/339587a0
10.1038/339230a0
10.1128/MCB.8.12.5570
{'key': 'e_1_2_1_22_2', 'first-page': '79', 'volume-title': 'Pancreatic Pathology', 'author': 'Kloppel G.', 'year': '1984'} / Pancreatic Pathology by Kloppel G. (1984)
10.1002/path.1711590204
{'key': 'e_1_2_1_24_2', 'first-page': '237', 'article-title': 'Absence of activating transmembrane mutations the c‐erbB‐2 proto‐oncogene in human breast cancer', 'volume': '5', 'author': 'Lemoine NR', 'year': '1990', 'journal-title': 'Oncogene'} / Oncogene / Absence of activating transmembrane mutations the c‐erbB‐2 proto‐oncogene in human breast cancer by Lemoine NR (1990)
{'key': 'e_1_2_1_25_2', 'first-page': '159', 'article-title': 'High frequency of ras oncogene activation in all stages of human tumorigenesis', 'volume': '4', 'author': 'Lemoine NR', 'year': '1989', 'journal-title': 'Oncogene'} / Oncogene / High frequency of ras oncogene activation in all stages of human tumorigenesis by Lemoine NR (1989)
10.1073/pnas.85.5.1629
10.1089/dna.1.1988.7.515
{'key': 'e_1_2_1_28_2', 'first-page': '336a', 'article-title': 'The pattern of c‐erbB‐2 oncoprotein expression in normal adult tissues', 'volume': '158', 'author': 'Colling PN', 'year': '1989', 'journal-title': 'J Pathol'} / J Pathol / The pattern of c‐erbB‐2 oncoprotein expression in normal adult tissues by Colling PN (1989)
10.1007/BF02899192
10.1083/jcb.102.2.500
{'key': 'e_1_2_1_31_2', 'first-page': '209', 'article-title': 'Visualisation of epidermal growth factor receptor in cryo‐sections of cultured A431 cells by immunogold labelling', 'volume': '36', 'author': 'Boonstra J', 'year': '1985', 'journal-title': 'Eur J Cell Biol'} / Eur J Cell Biol / Visualisation of epidermal growth factor receptor in cryo‐sections of cultured A431 cells by immunogold labelling by Boonstra J (1985)
10.1038/bjc.1989.221
{'key': 'e_1_2_1_33_2', 'first-page': '148', 'article-title': 'The neu(c‐erbB‐2) oncogene', 'volume': '16', 'author': 'Maguire HC', 'year': '1989', 'journal-title': 'Semin Oncol'} / Semin Oncol / The neu(c‐erbB‐2) oncogene by Maguire HC (1989)
{'key': 'e_1_2_1_34_2', 'first-page': '81', 'article-title': 'Expression pattern of the neu (NGL) gene‐encoded growth factor receptor protein (p185neu) in normal and transformed epithelial tissues of the digestive tract', 'volume': '4', 'author': 'Cohen JA', 'year': '1989', 'journal-title': 'Oncogene'} / Oncogene / Expression pattern of the neu (NGL) gene‐encoded growth factor receptor protein (p185neu) in normal and transformed epithelial tissues of the digestive tract by Cohen JA (1989)
{'key': 'e_1_2_1_35_2', 'first-page': '283', 'article-title': 'Genetic alterations of the c‐erbB‐2 oncogene occur frequently in tubular adenocarcinoma of the stomach and are often accompanied by amplification of the v‐erbA homologue', 'volume': '2', 'author': 'Yokota J', 'year': '1988', 'journal-title': 'Oncogene'} / Oncogene / Genetic alterations of the c‐erbB‐2 oncogene occur frequently in tubular adenocarcinoma of the stomach and are often accompanied by amplification of the v‐erbA homologue by Yokota J (1988)
{'key': 'e_1_2_1_36_2', 'first-page': '371', 'article-title': 'Studies of the HER/neu proto‐oncogene in human breast cancer', 'volume': '7', 'author': 'Slamon DJ', 'year': '1989', 'journal-title': 'Cancer Cells'} / Cancer Cells / Studies of the HER/neu proto‐oncogene in human breast cancer by Slamon DJ (1989)
{'key': 'e_1_2_1_37_2', 'volume-title': 'Molecular Biology of Cancer Genes', 'author': 'Lemoine NR'} / Molecular Biology of Cancer Genes by Lemoine NR
10.1002/j.1460-2075.1988.tb02906.x
10.1073/pnas.85.15.5389
10.1016/0092-8674(89)90843-X
{'key': 'e_1_2_1_41_2', 'first-page': '623', 'article-title': 'Immunocytochemical detection of epidermal growth factor receptors (EGFR) and transferrin receptor (TR) on normal, inflamed and neo‐plastic pancreatic tissue', 'volume': '4', 'author': 'Kloppel G', 'year': '1989', 'journal-title': 'Pancreas'} / Pancreas / Immunocytochemical detection of epidermal growth factor receptors (EGFR) and transferrin receptor (TR) on normal, inflamed and neo‐plastic pancreatic tissue by Kloppel G (1989)
{'key': 'e_1_2_1_42_2', 'first-page': '649', 'article-title': 'Immunohistochemical study on epidermal growth factor and its receptor in human pancreatic carcinoma', 'volume': '4', 'author': 'Yamanaka Y', 'year': '1989', 'journal-title': 'Pancreas'} / Pancreas / Immunohistochemical study on epidermal growth factor and its receptor in human pancreatic carcinoma by Yamanaka Y (1989)

Dates

Type	When
Created	20 years, 2 months ago (June 22, 2005, 10:03 a.m.)
Deposited	1 year, 10 months ago (Oct. 22, 2023, 2:48 p.m.)
Indexed	1 month ago (July 23, 2025, 9 a.m.)
Issued	35 years, 1 month ago (July 1, 1990)
Published	35 years, 1 month ago (July 1, 1990)
Published Online	20 years, 2 months ago (June 16, 2005)
Published Print	35 years, 1 month ago (July 1, 1990)

Funders 0

None

BibTeX

@article{Hall_1990, title={The c‐erbB‐2 proto‐oncogene in human pancreatic cancer}, volume={161}, ISSN={1096-9896}, url={http://dx.doi.org/10.1002/path.1711610305}, DOI={10.1002/path.1711610305}, number={3}, journal={The Journal of Pathology}, publisher={Wiley}, author={Hall, P. A. and Hughes, C. M. and Staddon, S. L. and Richman, P. I. and Gullick, W. J. and Lemoine, N. R.}, year={1990}, month=jul, pages={195–200} }

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