Abstract
To understand the cellular origin and mechanism of gene expression in amylase-producing cancers, the phenotyping of amylase isogenes by the polymerase chain reaction and restriction-fragment-length polymorphism using restriction endonucleasesTaqI,DdeI,HinfI, andAfaI were performed for 3 amylase-producing lung adenocarcinomas, 16 lung cancers without hyperamylasemia, other human malignant neoplasms, cultured cell lines, and normal tissues. In addition, amylase mRNA transcripts were semi-quantified by the limited polymerase chain reaction. Amylase mRNA transcripts were detected in all of the tissues examined. TheAMY1 gene (salivary type) was exclusively and highly expressed in the salivary glands and the amylase-producing lung adenocarcinomas. Coexpression of theAMY1 gene andAMY2 gene (pancreatic type) was observed in most of the lung cancers without hyperamylasemia, lung tissue, and cells scraped from the tracheal epithelium, thyroid, and female genital tract (ovary, fallopian tube, and uterus cervix), while minimal levels of mRNA transcripts of theAMY2 gene were detected in other malignant neoplasms, various normal tissues, and the cultured cell lines. All mRNA transcripts identified as being those of theAMY2 gene were further identified as being from theAMY2B gene except for the transcripts from the pancreas, in which theAMY2A gene andAMY2B gene were coexpressed. On the basis of these results, the clinical occurrence of amylase-producing cancer likely relates to the tissues expressing theAMY1 gene, while theAMY2B gene, which evolutionarily is the oldest gene among human amylase isogenes, is constitutively expressed in various tissues.
Key words: Amylase-producing cancer, Lung cancer, Amylase isogenes, Polymerase chain reaction, Restriction-fragment-length polymorphism
Abbreviations
- AMY1
salivary-type amylase gene
- AMY1A, AMY1B, andAMY1C
salivary-type amylase isogenes
- AMY2
pancreatic amylase gene
- AMY2A andAMY2B
pancreatic amylase isogenes
- PCR
polymerase chain reaction
- RT
reverse transcriptase
- RFLP
restriction-fragment-length polymorphism
- LTR
long terminal repeat
References
- Chelly J, Kaplan J-C, Maire P, Gautron S, Kahn A (1988) Transcription of the dystrophin gene in human muscle and non-muscle tissues. Nature 333:858–860 [DOI] [PubMed] [Google Scholar]
- Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299 [DOI] [PubMed] [Google Scholar]
- Clarke PD, Bain BC, Davies A, Levin GE, Lambert HP (1981) Aspiration in seriously ill patients: a study of amylase in bronchial secretions. J Clin Pathol 34:803–805 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corlette MB, Dratch M, Sorger K (1978) Amylase elevation attributable to an ovarian neoplasm. Gastroenterology 74:907–909 [PubMed] [Google Scholar]
- Doi S, Tomita N, Higasiyama M, Yokouchi H, Horii A, Yasuda T, Kobayashi T, Takai S, Ogawa M, Mori T, Matsubara K (1991) Expression of α-amylase isozymes in human thyroid tissues. Cancer Res 51:3544–3549 [PubMed] [Google Scholar]
- Emi M, Horrii A, Tomita N, Nishide T, Ogawa M, Mori T, Matsubara K (1988) Overlapping two genes in human DNA: a salivary amylase gene overlaps with a gamma-actin pseudogene that carries an integrated human endogenous retroviral DNA. Gene 62:229–235 [DOI] [PubMed] [Google Scholar]
- Erba HP, Gunning P, Kedes L (1986) Nucleotide sequence of the human γ cytoskeletal actin mRNA: anomalous evolution of vertebrate nonmuscle actin genes. Nucleic Acids Res 14:5275–5294 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Erba HP, Eddy R, Shows T, Kedes L, Gunning P (1988) Structure, chromosome location, and expression of the human γ-actin gene: differential evolution, location, and expression of the cytoskeletal β- and γ-actin genes. Mol Cell Biol 8:1775–1789 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green CL (1957) Identification of alpha-amylase as a secretion of the human fallopian tube and “tubelike” epithelium of Müllerian and mesonephric duct origin. Am J Obstet Gynecol 73:402–408 [DOI] [PubMed] [Google Scholar]
- Groot PC, Bleeker MJ, Pronk JC, Arwert F, Mager WH, Planta RJ, Eriksson AW, Frants RR (1989a) The human α-amylase multigene family consists of haplotypes with variable numbers of genes. Genomics 5:29–42 [DOI] [PubMed] [Google Scholar]
- Groot PC, Mager WH, Frants RR, Meisler MH, Samuelson LC (1989b) The human amylase-encoding genesamy2 andamy3 are identical toAMY2A andAMY2B. Gene 85:567–568 [DOI] [PubMed] [Google Scholar]
- Gumucio DL, Wiebauer K, Caldwell RM, Samuelson LC, Meisler MH (1988) Concerted evolution of human amylase genes. Mol Cell Biol 8:1197–1205 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hata H, Matsuzaki H, Tanaka K, Nomura H, Kagimoto T, Takeya M, Yamane N, Takatsuki K (1988) Ectopic production of salivary-type amylase by a IgA-γ-type multiple myeloma. Cancer 62:1511–1515 [DOI] [PubMed] [Google Scholar]
- Hata H, Matsuzaki H, Sanada I, Takatsuki K (1990) Genetic analysis of amylase0producing cell lines: ectopic activation of the amylase gene by translocation. Jpn J Clin Oncol 20:246–251 [PubMed] [Google Scholar]
- Hayakawa T, Kameya A, Mizuno R, Noda A, Kondo T, Hirabayashi N (1984) Hyperamylasemia with papillary serous cystadenocarcinoma of the ovary. Cancer 54:1662–1665 [DOI] [PubMed] [Google Scholar]
- Hayashi Y, Fukayama M, Koike M, Nakayama T (1986) Amylase in human lungs and the female genital tract. Histochemical and immuno-histochemical localization. Histochemistry 85:491–496 [DOI] [PubMed] [Google Scholar]
- Hodes ME, Sisk CJ, Karn RC, Ehrlich CE, Lehrner LM, Roth LM, Morley DJ, Merritt AD (1985) An amylase-producing serous cystadeno-carcinoma of the ovary. Oncology 42:242–247 [DOI] [PubMed] [Google Scholar]
- Horii A, Emi M, Tomita N, Nishide T, Ogawa M, Mori T, Matsubara K (1987) Primary structure of human pancreatic α-amylase gene: its comparison with human salivary α-amylase gene. Gene 60:57–64 [DOI] [PubMed] [Google Scholar]
- Katayama S, Ikeuchi M, Kanazawa Y, Akanuma Y, Kosaka K, Takeuchi T, Nakayama T (1981) Amlyase-producing lung cancer: case report and review of the literature. Cancer 48:2499–2502 [DOI] [PubMed] [Google Scholar]
- Maeda M, Otsuki M, Yuu H, Saeki S, Yamasaki T, Baba S (1982) Salivary-type hyperamylasemia in primary lung cancer: observation of a possible precursor of the salivary-type isoamylase. Eur J Cancer Clin Oncol 18:123–128 [DOI] [PubMed] [Google Scholar]
- Matsuzaki H, Hata H, Takatsuki K (1988) Establishment and characterization of an amylase-producing human myeloma cell line. Blood 72:978–982 [PubMed] [Google Scholar]
- Mocharla H, Mocharla R, Hodes ME (1990) Coupled reverse transcription-polymerase chain reaction (RT-PCR) as a sensitive and rapid method for isozyme genotyping. Gene 93:271–275 [DOI] [PubMed] [Google Scholar]
- Nakamura Y, Ogawa M, Nishide T, Emi M, Kosaki G, Himeno S, Matsubara K (1984) Sequences of cDNAs for human salivary and pancreatic α-amylases. Gene 28:263–270 [DOI] [PubMed] [Google Scholar]
- Nishide T, Nakamura Y, Emi M, Yamamoto T, Ogawa M, Mori T, Matsubara K (1986a) Primary structure of human salivary α-amylase gene. Gene 41:299–304 [DOI] [PubMed] [Google Scholar]
- Nishide T, Emi M, Nakamura Y, Matsubara K (1986b) Corrected sequences of cDNAs for human salivary and pancreatic α-amylases. Gene 50:371–372 [DOI] [PubMed] [Google Scholar]
- Ohtsuki T, Yawata Y, Wada H, Sugihara T, Mori M, Namba M (1989) Two human myeloma cell lines, amylase-producing KMS-12-PE and amylase-non-producing KMS-12-BM, were established from a patient, having the same chromosome marker, t(11; 14)(q13;q32). Br J Haematol 73:199–204 [DOI] [PubMed] [Google Scholar]
- Omichi K, Hase S (1992) Detection of human urinary α-amylase encoded by theAMY2B gene using fluorogenic substrate, FG5P. J Biochem (Tokyo) 112:303–305 [DOI] [PubMed] [Google Scholar]
- Otsuki M, Yuu H, Maeda M, Saeki S, Yamasaki T, Baba S (1977) Amylase in the lung. Cancer 39:1656–1663 [DOI] [PubMed] [Google Scholar]
- Robles F, López de la Osa E, Lerner U, Johannisson E, Brenner P, Hagenfeldt K, Diczfalusy E (1972) α-Amylase, glycogen synthetase and phosphorylase in the human endometrium: influence of the cycle and of the Cu−T device. Contraception 6:373–384 [DOI] [PubMed] [Google Scholar]
- Samuelson LC, Wiebauer K, Gumucio DL, Meisler MH (1988) Expression of the human amylase genes: recent origin of a salivary amylase promoter from an actin pseudogene. Nucleic Acids Res 16:8261–8276 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Samuelson LC, Wiebauer K, Snow CM, Meisler MH (1990) Retroviral and pseudogene insertion sites reveal the lineage of human salivary and pancreatic amylase genes from a single gene during primate evolution. Mol Cell Biol 10:2513–2520 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skude G, Mårdh PA, Weström L (1976) Amylases of the genital tract. I. Isoamylases of genital tract tissue homogenates and peritoneal fluid. Am J Obstet Gynecol 126:652–656 [DOI] [PubMed] [Google Scholar]
- Ting C-N, Rosenberg MP, Snow CM, Samuelson LC, Meisler MH (1992) Endogenous retroviral sequences are required for tissue-specific expression of a human saliry amylase gene. Genes Dev 6:1457–1465 [DOI] [PubMed] [Google Scholar]
- Tomita N, Matsuura N, Horii A, Emi M, Nishide T, Ogawa M, Mori T, Doi O, Matsubara K (1988) Expression of α-amylase in human lung cancers. Cancer Res 48:3292–3296 [PubMed] [Google Scholar]
- Tomita N, Horii A, Doi S, Yokouchi H, Shiosaki K, Higashiyama M, Matsuura N, Ogawa M, Mori T, Matsubara K (1989) A novel type of human α-amylase produced in lung carcinoid tumor. Gene 76:11–18 [DOI] [PubMed] [Google Scholar]
- Weiss MJ, Edmondson HA, Wertman M (1951) Elevated serum amylase associated with bronchogenic carcinoma. Am J Clin Pathol 21:1057–1061 [DOI] [PubMed] [Google Scholar]
- Yokouchi H, Horii A, Emi M, Tomita N, Doi S, Ogawa M, Mori T, Matsubara K (1990) Cloning and characterization of a third type of human α-amylase gene,AMY2B. Gene 90:281–286 [DOI] [PubMed] [Google Scholar]
- Zabel BU, Naylor SL, Sakaguchi AY, Bell GI, Shows TB (1983) High-resolution chromosomal localization of human genes for amylase, proopiomelanocortin, somatostatin, and a DNA fragment (D3S1) by in situ hybridization. Proc Natl Acad Sci USA 80:6932–6936 [DOI] [PMC free article] [PubMed] [Google Scholar]
