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Published in: Virchows Archiv 2/2006

01-08-2006 | Original Article

HPV subtypes in cervical cancer biopsies between 1930and 2004: detection using general primer pair PCR and sequencing

Authors: Bjørn Inge Bertelsen, Kalaiarasy Kugarajh, Robert Skar, Ole Didrik Laerum

Published in: Virchows Archiv | Issue 2/2006

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Abstract

Our objective was to investigate the practicability of sequencing DNA from formalin fixed, paraffin embedded tissue stored for up to 75 years and to study human papillomavirus subtype distribution in cervical neoplasias between 1931 and 2004. Three protocols for DNA retrieval were tested, and magnetic bead DNA extraction proved advantageous, as it gave superior specimen purity and effortless sequencing. Successful sequencing was achieved in more than 70% of the specimens from 1931 to 1960. This technique was utilized in the study of papillomavirus subtypes using general primer pair PCR with sequencing of the products in a series of 97 cases of neoplastic and non-neoplastic cervical specimens from 1931 to 1960 and 73 similar cases from 1992 to 2004. HPV was detected in 61% of neoplastic specimens from 1931 to 1960, and in 89% of those from 1992 to 2004. In specimens from 1931 to 1934, only HPV type 16 was detected, whereas in the specimens from 1940 and up, other HPV subtypes were identified in one-third of the cases. The difference was significant and suggests an increase in papillomavirus subtype heterogeneity in Western Norway during 1930–2000. The results strongly support the feasibility of using DNA from paraffin-embedded specimens for studying cancer etiology and genotypes over extended time periods.
Literature
1.
go back to reference Andersson S, Rylander E, Larsson B, Strand A, Silfversvard C, Wilander E (2001) The role of human papillomavirus in cervical adenocarcinoma carcinogenesis. Eur J Cancer 37:246–250PubMedCrossRef Andersson S, Rylander E, Larsson B, Strand A, Silfversvard C, Wilander E (2001) The role of human papillomavirus in cervical adenocarcinoma carcinogenesis. Eur J Cancer 37:246–250PubMedCrossRef
2.
go back to reference Bertelsen B, Steine S, Sandvei R, Molven A, Laerum O (2006) Molecular analysis of the PI3K-AKT pathway in uterine cervical neoplasia: frequent PIK3CA amplification and AKT phosphorylation. Int J Cancer 118:1877–1883PubMedCrossRef Bertelsen B, Steine S, Sandvei R, Molven A, Laerum O (2006) Molecular analysis of the PI3K-AKT pathway in uterine cervical neoplasia: frequent PIK3CA amplification and AKT phosphorylation. Int J Cancer 118:1877–1883PubMedCrossRef
3.
go back to reference Bjørge T, Thoresen SØ, Skare GB (1993) Incidence, survival and mortality in cervical cancer in Norway, 1956–1990. Eur J Cancer 29A:2291–2297PubMedCrossRef Bjørge T, Thoresen SØ, Skare GB (1993) Incidence, survival and mortality in cervical cancer in Norway, 1956–1990. Eur J Cancer 29A:2291–2297PubMedCrossRef
4.
go back to reference Bosch FX, Lorincz A, Munoz N, Meijer CJ, Shah KV (2002) The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 55:244–265PubMed Bosch FX, Lorincz A, Munoz N, Meijer CJ, Shah KV (2002) The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 55:244–265PubMed
5.
go back to reference Brüstle O, Ohgaki H, Schmitt HP, Walter GF, Ostertag H, Kleihues P (1992) Primitive neuroectodermal tumors after prophylactic central nervous system irradiation in children. Association with an activated K-ras gene. Cancer 69:2385–2392PubMedCrossRef Brüstle O, Ohgaki H, Schmitt HP, Walter GF, Ostertag H, Kleihues P (1992) Primitive neuroectodermal tumors after prophylactic central nervous system irradiation in children. Association with an activated K-ras gene. Cancer 69:2385–2392PubMedCrossRef
6.
go back to reference Busby-Earle RMC, Steel CM, Williams ARW, Cohen B, Bird CC (1994) p53 mutations in cervical carcinogenesis—low frequency and lack of correlation with human papillomavirus status. Br J Cancer 69:732–737PubMed Busby-Earle RMC, Steel CM, Williams ARW, Cohen B, Bird CC (1994) p53 mutations in cervical carcinogenesis—low frequency and lack of correlation with human papillomavirus status. Br J Cancer 69:732–737PubMed
7.
go back to reference Baak JP, Kruse AJ, Garland SM, Skaland I, Janssen EA, Tabrizi S, Fagerheim S, Robboy S, Nilsen ST (2005) Combined p53 and retinoblastoma protein detection identifies persistent and regressive cervical high-grade squamous intraepithelial lesions. Am J Surg Pathol 29:1062–1066PubMed Baak JP, Kruse AJ, Garland SM, Skaland I, Janssen EA, Tabrizi S, Fagerheim S, Robboy S, Nilsen ST (2005) Combined p53 and retinoblastoma protein detection identifies persistent and regressive cervical high-grade squamous intraepithelial lesions. Am J Surg Pathol 29:1062–1066PubMed
8.
go back to reference Collins JE, Jenkins D, McCance DJ (1988) Detection of human papillomavirus DNA sequences by in situ DNA-DNA hybridisation in cervical intraepithelial neoplasia and invasive carcinoma: a retrospective study. J Clin Pathol 41:289–295PubMedCrossRef Collins JE, Jenkins D, McCance DJ (1988) Detection of human papillomavirus DNA sequences by in situ DNA-DNA hybridisation in cervical intraepithelial neoplasia and invasive carcinoma: a retrospective study. J Clin Pathol 41:289–295PubMedCrossRef
9.
go back to reference de Roda Husman A-M, Walboomers JMM, van den Brule AJC, Meijer CJLM, Snijders PJF (1995) The use of general primers GP5 and GP6 elongated at their 3′ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol 76:1057–1062PubMedCrossRef de Roda Husman A-M, Walboomers JMM, van den Brule AJC, Meijer CJLM, Snijders PJF (1995) The use of general primers GP5 and GP6 elongated at their 3′ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol 76:1057–1062PubMedCrossRef
10.
go back to reference Dubeau L, Chandler LA, Gralow JR, Nichols PW, Jones PA (1986) Southern blot analysis of DNA extracted from formalin-fixed pathology specimens. Cancer Res 46:2964–2969PubMed Dubeau L, Chandler LA, Gralow JR, Nichols PW, Jones PA (1986) Southern blot analysis of DNA extracted from formalin-fixed pathology specimens. Cancer Res 46:2964–2969PubMed
11.
go back to reference Goelz SE, Hamilton SR, Vogelstein B (1985) Purification of DNA from formaldehyde fixed and paraffin embedded human tissue. Biochem Biophys Res Commun 130:118–126PubMedCrossRef Goelz SE, Hamilton SR, Vogelstein B (1985) Purification of DNA from formaldehyde fixed and paraffin embedded human tissue. Biochem Biophys Res Commun 130:118–126PubMedCrossRef
12.
go back to reference Greer CE, Wheeler CM, Manos MM (1994) Sample preparation and PCR amplification from paraffin-embedded tissues. PCR Methods Appl 3:S113–S122PubMed Greer CE, Wheeler CM, Manos MM (1994) Sample preparation and PCR amplification from paraffin-embedded tissues. PCR Methods Appl 3:S113–S122PubMed
13.
go back to reference Hummel S (2003) Ancient DNA typing. Methods, strategies and applications, 1st edn. Springer, Berlin Heidelberg New York Hummel S (2003) Ancient DNA typing. Methods, strategies and applications, 1st edn. Springer, Berlin Heidelberg New York
14.
go back to reference Ibrahim SO, Vasstrand EN, Johannessen AC, Idris AM, Magnusson B, Nilsen R, Lillehaug JR (1999) Mutations of the p53 gene in oral squamous-cell carcinomas from Sudanese dippers of nitrosamine-rich toombak and non-snuff-dippers from the Sudan and Scandinavia. Int J Cancer 81:527–534PubMedCrossRef Ibrahim SO, Vasstrand EN, Johannessen AC, Idris AM, Magnusson B, Nilsen R, Lillehaug JR (1999) Mutations of the p53 gene in oral squamous-cell carcinomas from Sudanese dippers of nitrosamine-rich toombak and non-snuff-dippers from the Sudan and Scandinavia. Int J Cancer 81:527–534PubMedCrossRef
15.
go back to reference Isola J, DeVries S, Chu L, Ghazvini S, Waldman F (1994) Analysis of changes in DNA sequence copy number by comparative genomic hybridization in archival paraffin-embedded tumor samples. Am J Pathol 145:1301–1308PubMed Isola J, DeVries S, Chu L, Ghazvini S, Waldman F (1994) Analysis of changes in DNA sequence copy number by comparative genomic hybridization in archival paraffin-embedded tumor samples. Am J Pathol 145:1301–1308PubMed
16.
go back to reference Iwamoto KS, Mizuno T, Ito T, Akiyama M, Takeichi N, Mabuchi K, Seyama T (1996) Feasibility of using decades-old archival tissues in molecular oncology/epidemiology. Am J Pathol 149:399–406PubMed Iwamoto KS, Mizuno T, Ito T, Akiyama M, Takeichi N, Mabuchi K, Seyama T (1996) Feasibility of using decades-old archival tissues in molecular oncology/epidemiology. Am J Pathol 149:399–406PubMed
17.
go back to reference Karlsen F, Kalantari M, Chitemerere M, Johansson B, Hagmar B (1994) Modifications of human and viral deoxyribonucleic acid by formaldehyde fixation. Lab Invest 71:604–611PubMed Karlsen F, Kalantari M, Chitemerere M, Johansson B, Hagmar B (1994) Modifications of human and viral deoxyribonucleic acid by formaldehyde fixation. Lab Invest 71:604–611PubMed
18.
go back to reference Kraus I, Molden T, Erno LE, Skomedal H, Karlsen F, Hagmar B (2004) Human papillomavirus oncogenic expression in the dysplastic portio; an investigation of biopsies from 190 cervical cones. Br J Cancer 90:1407–1413PubMedCrossRef Kraus I, Molden T, Erno LE, Skomedal H, Karlsen F, Hagmar B (2004) Human papillomavirus oncogenic expression in the dysplastic portio; an investigation of biopsies from 190 cervical cones. Br J Cancer 90:1407–1413PubMedCrossRef
19.
go back to reference Kösel S, Graeber MB (1994) Use of neuropathological tissue for molecular genetic studies: parameters affecting DNA extraction and polymerase chain reaction. Acta Neuropathol (Berl) 88:19–25CrossRef Kösel S, Graeber MB (1994) Use of neuropathological tissue for molecular genetic studies: parameters affecting DNA extraction and polymerase chain reaction. Acta Neuropathol (Berl) 88:19–25CrossRef
20.
go back to reference Lehmann U, Kreipe H (2001) Real-time PCR analysis of DNA and RNA extracted from formalin-fixed and paraffin-embedded biopsies. Methods 25:409–418PubMedCrossRef Lehmann U, Kreipe H (2001) Real-time PCR analysis of DNA and RNA extracted from formalin-fixed and paraffin-embedded biopsies. Methods 25:409–418PubMedCrossRef
21.
go back to reference Lewis F, Maughan NJ, Smith V, Hillan K, Quirke P (2001) Unlocking the archive-gene expression in paraffin-embedded tissue. J Pathol 195:66–71PubMedCrossRef Lewis F, Maughan NJ, Smith V, Hillan K, Quirke P (2001) Unlocking the archive-gene expression in paraffin-embedded tissue. J Pathol 195:66–71PubMedCrossRef
22.
go back to reference Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348:518–527PubMedCrossRef Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348:518–527PubMedCrossRef
23.
go back to reference Munoz N, Bosch FX, Castellsague X, Diaz M, de Sanjose S, Hammouda D, Shah KV, Meijer CJ (2004) Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int J Cancer 111:278–285PubMedCrossRef Munoz N, Bosch FX, Castellsague X, Diaz M, de Sanjose S, Hammouda D, Shah KV, Meijer CJ (2004) Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int J Cancer 111:278–285PubMedCrossRef
24.
go back to reference Rekand T, Male R, Myking AO, Nygaard SJ, Aarli JA, Haarr L, Langeland N (2003) Detection of viral sequences in archival spinal cords from fatal cases of poliomyelitis in 1951–1952. J Virol Methods 114:91–96PubMedCrossRef Rekand T, Male R, Myking AO, Nygaard SJ, Aarli JA, Haarr L, Langeland N (2003) Detection of viral sequences in archival spinal cords from fatal cases of poliomyelitis in 1951–1952. J Virol Methods 114:91–96PubMedCrossRef
25.
go back to reference Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, New York Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, New York
26.
go back to reference Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129–1136PubMedCrossRef Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129–1136PubMedCrossRef
27.
go back to reference Shibata D, Martin W, Arnheim N (1988) Analysis of DNA sequences in forty-year-old paraffin-embedded thin-tissue sections: A bridge between molecular biology and classical histology. Cancer Res 48:4564–4566PubMed Shibata D, Martin W, Arnheim N (1988) Analysis of DNA sequences in forty-year-old paraffin-embedded thin-tissue sections: A bridge between molecular biology and classical histology. Cancer Res 48:4564–4566PubMed
28.
go back to reference Spandidos DA, Dokianakis DN, Kallergi G, Aggelakis E (2000) Molecular basis of gynecological cancer. Ann N Y Acad Sci 900:56–64PubMedCrossRef Spandidos DA, Dokianakis DN, Kallergi G, Aggelakis E (2000) Molecular basis of gynecological cancer. Ann N Y Acad Sci 900:56–64PubMedCrossRef
29.
go back to reference Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG (2005) Characterization of the 1918 influenza virus polymerase genes. Nature 437:889–893PubMedCrossRef Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG (2005) Characterization of the 1918 influenza virus polymerase genes. Nature 437:889–893PubMedCrossRef
30.
go back to reference Thompson CH, Rose BR, Cossart YE (1992) Detection of HPV DNA in archival specimens of cervical cancer using in situ hybridisation and the polymerase chain reaction. J Med Virol 36:54–59PubMedCrossRef Thompson CH, Rose BR, Cossart YE (1992) Detection of HPV DNA in archival specimens of cervical cancer using in situ hybridisation and the polymerase chain reaction. J Med Virol 36:54–59PubMedCrossRef
31.
go back to reference Tumpey TM, Basler CF, Aguilar PV, Zeng H, Solorzano A, Swayne DE, Cox NJ, Katz JM, Taubenberger JK, Palese P, Garcia-Sastre A (2005) Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77–80PubMedCrossRef Tumpey TM, Basler CF, Aguilar PV, Zeng H, Solorzano A, Swayne DE, Cox NJ, Katz JM, Taubenberger JK, Palese P, Garcia-Sastre A (2005) Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77–80PubMedCrossRef
32.
go back to reference WHO (1995) Human papillomaviruses, 1st edn. World Health Organization, Lyon WHO (1995) Human papillomaviruses, 1st edn. World Health Organization, Lyon
33.
go back to reference WHO (1997) The world health report 1997: conquering suffering, enriching humanity. World Health Organization, Geneva WHO (1997) The world health report 1997: conquering suffering, enriching humanity. World Health Organization, Geneva
34.
go back to reference Zariwala M, Schmid S, Pfaltz M, Ohgaki H, Kleihues P, Schafer R (1994) p53 gene mutations in oropharyngeal carcinomas: a comparison of solitary and multiple primary tumours and lymph-node metastases. Int J Cancer 56:807–811PubMedCrossRef Zariwala M, Schmid S, Pfaltz M, Ohgaki H, Kleihues P, Schafer R (1994) p53 gene mutations in oropharyngeal carcinomas: a comparison of solitary and multiple primary tumours and lymph-node metastases. Int J Cancer 56:807–811PubMedCrossRef
35.
go back to reference Zsikla V, Baumann M, Cathomas G (2004) Effect of buffered formalin on amplification of DNA from paraffin wax embedded small biopsies using real-time PCR. J Clin Pathol 57:654–656PubMedCrossRef Zsikla V, Baumann M, Cathomas G (2004) Effect of buffered formalin on amplification of DNA from paraffin wax embedded small biopsies using real-time PCR. J Clin Pathol 57:654–656PubMedCrossRef
Metadata
Title
HPV subtypes in cervical cancer biopsies between 1930and 2004: detection using general primer pair PCR and sequencing
Authors
Bjørn Inge Bertelsen
Kalaiarasy Kugarajh
Robert Skar
Ole Didrik Laerum
Publication date
01-08-2006
Publisher
Springer-Verlag
Published in
Virchows Archiv / Issue 2/2006
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-006-0232-3

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