Differential gene expression between skin and cervix induced by the E7 oncoprotein in a transgenic mouse model

Virology

Volumn 433, Issue 2, 2012, Pages 337-345

  Ibarra Sierra, E ^a   Diaz Chavez J ^b   Cortes Malagon E M ^c   Uribe Figueroa, L ^d   Hidalgo Miranda, A ^d   Lambert, P F ^e   Gariglio, P ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS   (Mexico)

^c HOSPITAL JUÁREZ DE MÉXICO   (Mexico)

^d INSTITUTO NACIONAL DE MEDICINA GENÓMICA   (Mexico)

^e UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Cervical cancer; HPV16; K14E7; Microarrays; Transgenic mice

Indexed keywords

ESTRADIOL; PROTEIN E7;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL METABOLISM; CELL TRANSPORT; CONTROLLED STUDY; DMBT1 GENE; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GLI1 GENE; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNE RESPONSE; INFLAMMATION; MICROARRAY ANALYSIS; MMP12 GENE; MMP14 GENE; MMP19 GENE; MMP2 GENE; MMP27 GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PENETRANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN; SKIN TUMOR; TRANSGENIC MOUSE; UTERINE CERVIX; UTERINE CERVIX TUMOR;

ANIMALS; BASE SEQUENCE; CERVIX UTERI; DISEASE MODELS, ANIMAL; FEMALE; GENES, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, VIRAL; SKIN; TRANSCRIPTOME; UTERINE CERVICAL NEOPLASMS;

MUS; MUS MUSCULUS;

EID: 84867218834     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.08.024     Document Type: Article

References (63)

1. Antinore M.J., Birrer M.J., Patel D., Nader L., McCance D.J. The human papillomavirus type 16 E7 gene product interacts with and transactivates the AP1 family of transcription factors. EMBO J. 1996, 15(8):1950-1960.
2. Arbeit J.M., Munger K., Howley P.M., Hanahan D. Progressive squamous epithelial neoplasia in K14-human papillomavirus type 16 transgenic mice. J. Virol. 1994, 68(7):4358.
3. Bae D., Cho S., Kim Y., Whang J., Song S., Park C., Kim D., Lee J. Aberrant expression of cyclin D1 is associated with poor prognosis in early stage cervical cancer of the uterus. Gynecol. Oncol. 2001, 81(3):341-347.
4. Bergers G., Brekken R., McMahon G., Vu T., Itoh T., Tamaki K., Tanzawa K., Thorpe P., Itohara S., Werb Z. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2000, 2(10):737-744.
5. Bonilla-Delgado J., Bulut G., Liu X., Cortes-Malagon E.M., Schlegel R., Flores-Maldonado C., Contreras R.G., Chung S.H., Lambert P.F., Uren A., Gariglio P. The E6 oncoprotein from HPV16 enhances the canonical Wnt/beta-catenin pathway in skin epidermis in vivo. Mol. Cancer Res. 2012, 10:250-258.
6. Brake T., Connor J.P., Petereit D.G., Lambert P.F. Comparative analysis of cervical cancer in women and in a human papillomavirus-transgenic mouse model: identification of minichromosome maintenance protein 7 as an informative biomarker for human cervical cancer. Cancer Res. 2003, 63(23):8173-8180.
7. Brake T., Lambert P.F. Estrogen contributes to the onset, persistence, and malignant progression of cervical cancer in a human papillomavirus-transgenic mouse model. Proc. Nat. Acad. Sci. U.S.A. 2005, 102(7):2490-2495.
8. Ciró M., Prosperini E., Quarto M., Grazini U., Walfridsson J., McBlane F., Nucifero P., Pacchiana G., Capra M., Christensen J. ATAD2 is a novel cofactor for MYC, overexpressed and amplified in aggressive tumors. Cancer Res. 2009, 69(21):8491.
9. Daud I., Scott M., Ma Y., Shiboski S., Farhat S., Moscicki A. Association between toll-like receptor expression and human papillomavirus type 16 persistence. Int. J. Cancer 2010.
10. Diaz-Chavez J., Hernandez-Pando R., Lambert P., Gariglio P. Down-regulation of transforming growth factor-type II receptor (TGF-RII) protein and mRNA expression in cervical cancer. Mol. Cancer 2008, 7:3.
11. Du J., Guan M., Fan J., Jiang H. Loss of DMBT1 Expression in human prostate cancer and its correlation with clinical progressive features. Urology 2011.
12. Ghittoni R., Accardi R., Hasan U., Gheit T., Sylla B., Tommasino M. The biological properties of E6 and E7 oncoproteins from human papillomaviruses. Virus Genes 2010, 40(1):1-13.
13. Hartshorn K., White M., Mogues T., Ligtenberg T., Crouch E., Holmskov U. Lung and salivary scavenger receptor glycoprotein-340 contribute to the host defense against influenza A viruses. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2003, 285(5):1066.
14. Helmke B., Renner M., Poustka A., Schirmacher P., Mollenhauer J., Kern M. DMBT1 expression distinguishes anorectal from cutaneous melanoma. Histopathology 2009, 54(2):233-240.
15. Herber R., Liem A., Pitot H., Lambert P. Squamous epithelial hyperplasia and carcinoma in mice transgenic for the human papillomavirus type 16 E7 oncogene. J. Virol. 1996, 70(3):1873.
16. Herber R., Liem A., Pitot H., Lambert P.F. Squamous epithelial hyperplasia and carcinoma in mice transgenic for the human papillomavirus type 16 E7 oncogene. J. Virol. 1996, 70(3):1873-1881.
17. Hwang S.G., Lee D., Kim J., Seo T., Choe J. Human papillomavirus type 16 E7 binds to E2F1 and activates E2F1-driven transcription in a retinoblastoma protein-independent manner. J. Biol. Chem. 2002, 277(4):2923-2930.
18. Ishimi Y., Okayasu I., Kato C., Kwon H., Kimura H., Yamada K., Song S. Enhanced expression of Mcm proteins in cancer cells derived from uterine cervix. Eur. J. Biochem. 2003, 270(6):1089-1101.
19. Jung T., Baek W., Suh S., Jang B., Song D., Bae J., Kwon K., Cha S., Bae I. Down-regulation of peroxisome proliferator-activated receptor gamma in human cervical carcinoma. Gynecol. Oncol. 2005, 97(2):365-373.
20. Kerkelä E., Ala-aho R., Jeskanen L., Rechardt O., Grenman R., Shapiro S., Kähäri V., Saarialho-Kere U. Expression of human macrophage metalloelastase (MMP-12) by tumor cells in skin cancer. J. Invest. Dermatol. 2000, 114(6):1113-1119.
21. Kerkelä E., Ala aho R., Klemi P., Grénman S., Shapiro S., Kähäri V., Saarialho Kere U. Metalloelastase (MMP 12) expression by tumour cells in squamous cell carcinoma of the vulva correlates with invasiveness, while that by macrophages predicts better outcome. J. Pathol. 2002, 198(2):258-269.
22. Kitawaki J., Koshiba H., Ishihara H., Kusuki I., Tsukamoto K., Honjo H. Progesterone induction of 17beta-hydroxysteroid dehydrogenase type 2 during the secretory phase occurs in the endometrium of estrogen-dependent benign diseases but not in normal endometrium. J. Clin. Endocrinol. Metab. 2000, 85(9):3292-3296.
23. Kolligs F., Bommer G., Göke B. Wnt/beta-catenin/tcf signaling: a critical pathway in gastrointestinal tumorigenesis. Digestion 2000, 66(3):131-144.
24. Lambert P., Brake T. Models for human cervical cancer. Drug Discovery Today: Dis. Models 2005, 2(1):15-20.
25. Larue L., Delmas V. The WNT/Beta-catenin pathway in melanoma. Front. Biosci. 2006, 11:733-742.
26. Lehrke M., Lazar M.A. The many faces of PPARgamma. Cell 2005, 123(6):993-999.
27. Long L., Geng G., Li Q. Effect of Gleditsia sinensis stings on growth inhibition and expression of PCNA and p53 in mice bearing uterine cervical carcinoma (U14). Zhongguo Zhong yao za zhi=Zhongguo zhongyao zazhi=China journal of Chinese materia medica 2006, 31(2):150.
28. Lucero O., Dawson D., Moon R., Chien A. A re-evaluation of the "oncogenic" nature of Wnt/-catenin signaling in melanoma and other cancers. Curr. Oncol. Rep. 2010, 1-5.
29. Maldonado E., Cabrejos M.E., Banks L., Allende J.E. Human papillomavirus-16 E7 protein inhibits the DNA interaction of the TATA binding transcription factor. J. Cell. Biochem. 2002, 85(4):663-669.
30. Mansur C., Androphy E. Cellular transformation by papillomavirus oncoproteins. BBA, CR. Rev. Cancer 1993, 1155(3):323-345.
31. Martinez I., Wang J., Hobson K.F., Ferris R.L., Khan S.A. Identification of differentially expressed genes in HPV-positive and HPV-negative oropharyngeal squamous cell carcinomas. Eur. J. Cancer 2007, 43(2):415-432.
32. McLaughlin-Drubin M., Münger K. The human papillomavirus E7 oncoprotein. Virology 2009, 384(2):335-344.
33. McLaughlin-Drubin M.E., Crum C.P., Munger K. Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc. Nat. Acad. Sci. U.S.A. 2011, 108(5):2130-2135.
34. McLaughlin-Drubin M.E., Munger K. The human papillomavirus E7 oncoprotein. Virology 2009, 384(2):335-344.
35. Mendoza-Villanueva D., Diaz-Chavez J., Uribe-Figueroa L., Rangel-Escareao C., Hidalgo-Miranda A., March-Mifsut S., Jimenez-Sanchez G., Lambert P., Gariglio P. Gene expression profile of cervical and skin tissues from human papillomavirus type 16 E6 transgenic mice. BMC Cancer 2008, 8:347.
36. Mollenhauer J., Helmke B., Muller H., Kollender G., Lyer S., Diedrichs L., Holmskov U., Ligtenberg T., Herbertz S., Krebs I., Wiemann S., Madsen J., Bikker F., Schmitt L., Otto H.F., Poustka A. Sequential changes of the DMBT1 expression and location in normal lung tissue and lung carcinomas. Genes Chromosomes Cancer 2002, 35(2):164-169.
37. Mollenhauer J., Wiemann S., Scheurlen W., Korn B., Hayashi Y., Wilgenbus K., von Deimling A., Poustka A. DMBT1, a new member of the SRCR superfamily, on chromosome 10q25. 3-26.1 is deleted in malignant brain tumours. Nat. Genet. 1997, 17(1):32-39.
38. Munger K., Basile J.R., Duensing S., Eichten A., Gonzalez S.L., Grace M., Zacny V.L. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 2001, 20(54):7888-7898.
39. Munoz N., Bosch F.X., de Sanjose S., Herrero R., Castellsague X., Shah K.V., Snijders P.J., Meijer C.J. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. 2003, 348(6):518-527.
40. Murphy N., Ring M., Heffron C., King B., Killalea A., Hughes C., Martin C., McGuinness E., Sheils O., O'Leary J. p16INK4A, CDC6, and MCM5: predictive biomarkers in cervical preinvasive neoplasia and cervical cancer. J. Clin. Pathol. 2005, 58(5):525.
41. Pyeon D., Newton M.A., Lambert P.F., den Boon J.A., Sengupta S., Marsit C.J., Woodworth C.D., Connor J.P., Haugen T.H., Smith E.M., Kelsey K.T., Turek L.P., Ahlquist P. Fundamental differences in cell cycle deregulation in human papillomavirus-positive and human papillomavirus-negative head/neck and cervical cancers. Cancer Res. 2007, 67(10):4605-4619.
42. Radisky E., Radisky D. Matrix metalloproteinase-induced epithelial-mesenchymal transition in breast cancer. J. Mammary Gland Biol. Neoplasia 2010, 15(2):201-212.
43. Rampias T., Boutati E., Pectasides E., Sasaki C., Kountourakis P., Weinberger P., Psyrri A. Activation of Wnt signaling pathway by human papillomavirus E6 and E7 oncogenes in HPV16-positive oropharyngeal squamous carcinoma cells. Mol. Cancer Res. 2010, 8(3):433.
44. Riley R., Duensing S., Brake T., Münger K., Lambert P., Arbeit J. Dissection of human papillomavirus E6 and E7 function in transgenic mouse models of cervical carcinogenesis. Cancer Res. 2003, 63(16):4862.
45. Rosen E.D., Spiegelman B.M. PPARgamma: a nuclear regulator of metabolism, differentiation, and cell growth. J. Biol. Chem. 2001, 276(41):37731-37734.
46. Rosenstiel P., Sina C., End C., Renner M., Lyer S., Till A., Hellmig S., Nikolaus S., Folsch U., Helmke B. Regulation of DMBT1 via NOD2 and TLR4 in intestinal epithelial cells modulates bacterial recognition and invasion. J. Immunol. 2007, 178(12):8203.
47. Shai A., Brake T., Somoza C., Lambert P. The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res. 2007, 67(4):1626.
48. Shin M.K., Balsitis S., Brake T., Lambert P.F. Human papillomavirus E7 oncoprotein overrides the tumor suppressor activity of p21Cip1 in cervical carcinogenesis. Cancer Res. 2009, 69(14):5656-5663.
49. Song S., Pitot H., Lambert P. The human papillomavirus type 16 E6 gene alone is sufficient to induce carcinomas in transgenic animals. J Virol. 1999, 73(7):5887.
50. Stanley M. Immune responses to human papillomavirus. Vaccine 2006, 24:S16-S22.
51. Stelzer M.K., Pitot H.C., Liem A., Schweizer J., Mahoney C., Lambert P.F. A mouse model for human anal cancer. Cancer Prev. Res. (Phila) 2010, 3(12):1534-1541.
52. Strati K., Pitot H.C., Lambert P.F. Identification of biomarkers that distinguish human papillomavirus (HPV)-positive versus HPV-negative head and neck cancers in a mouse model. Proc. Nat. Acad. Sci. U.S.A. 2006, 103(38):14152-14157.
53. Tachibana K., Gonzalez M., Coleman N. Cell cycle dependent regulation of DNA replication and its relevance to cancer pathology. J. Pathol. 2005, 205(2):123-129.
54. Takito J., Al-Awqati Q. Conversion of ES cells to columnar epithelia by hensin and to squamous epithelia by laminin. J. Cell Biol. 2004, 166(7):1093.
55. Tan Y.F., Li F.X., Piao Y.S., Sun X.Y., Wang Y.L. Global gene profiling analysis of mouse uterus during the oestrous cycle. Reproduction 2003, 126(2):171-182.
56. Thomas M.K., Pitot H.C., Liem A., Lambert P.F. Dominant role of HPV16 E7 in anal carcinogenesis. Virology 2011, 421(2):114-118.
57. Van Trappen P., Ryan A., Carroll M., Lecoeur C., Goff L., Gyselman V., Young B., Lowe D., Pepper M., Shepherd J. A model for co-expression pattern analysis of genes implicated in angiogenesis and tumour cell invasion in cervical cancer. Br. J. Cancer 2002, 87(5):537-544.
58. Vazquez-Ortiz G., Pina-Sanchez P., Vazquez K., Duenas A., Taja L., Mendoza P., Garcia J., Salcedo M. Overexpression of cathepsin F, matrix metalloproteinases 11 and 12 in cervical cancer. BMC Cancer 2005, 5(1):68.
59. Yalcin A. Quantification of thioredoxin mRNA expression in the rat hippocampus by real-time PCR following oxidative stress. Acta Biochim. Pol. 2004, 51(4):1059-1065.
60. Yu L., Wang L., Li M., Zhong J., Wang Z., Chen S. Expression of toll-like receptor 4 is down-regulated during progression of cervical neoplasia. Cancer Immunol. Immunother. 2010, 59(7):1021-1028.
61. Zerfass K., Schulze A., Spitkovsky D., Friedman V., Henglein B., Jansen-Durr P. Sequential activation of cyclin E and cyclin A gene expression by human papillomavirus type 16 E7 through sequences necessary for transformation. J. Virol. 1995, 69(10):6389.
62. zur Hausen H. Papillomavirus infections-a major cause of human cancers. Biochim. Biophys. Acta 1996, 1288(2):F55-F78.
63. zur Hausen H. Papillomaviruses in the causation of human cancers-a brief historical account. Virology 2009, 384(2):260-265.