The distribution of insertionally polymorphic endogenous retroviruses in breast cancer patients and cancer-free controls

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Wildschutte, Julia H ^a,c   Ram, Daniel ^a   Subramanian, Ravi ^a   Stevens, Victoria L ^b   Coffin, John M ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b AMERICAN CANCER SOCIETY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Betaretroviridae; Breast cancer; Endogenous retrovirus; HERV K; JSRV; MMTV; Provirus

Indexed keywords

GENOMIC DNA;

ADULT; AGED; ARTICLE; BREAST CANCER; CASE CONTROL STUDY; COMPUTER MODEL; CONTROLLED STUDY; DNA SCREENING; ENDOGENOUS RETROVIRUS; FEMALE; GENE AMPLIFICATION; GENE LOCUS; GENE SEQUENCE; GENOME; HUMAN; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RESTRICTION MAPPING; BREAST TUMOR; GENETICS; ISOLATION AND PURIFICATION; LONG TERMINAL REPEAT; PROVIRUS; VIROLOGY;

JAAGSIEKTE SHEEP RETROVIRUS; MOUSE MAMMARY TUMOR VIRUS;

BREAST NEOPLASMS; CASE-CONTROL STUDIES; ENDOGENOUS RETROVIRUSES; FEMALE; HUMANS; PROVIRUSES; TERMINAL REPEAT SEQUENCES;

EID: 84908270121     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0062-3     Document Type: Article

References (60)

1. Howlader M, Noone AM, Krapcho M, Garsell J, Miler D, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatlovich Z, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA. SEER Cancer Statistics Review (CSR) 1975-2011 2014, National Cancer Institute, Bethesda, MD.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013, 63:11-30. 23335087.
3. CHEK2*1100delC and susceptibility to breast cancer: a collaborative analysis involving 10,860 breast cancer cases and 9,065 controls from 10 studies. Am J Hum Genet 2004, 74:1175-1182.
4. Easton DF, Pooley KA, Dunning AM, Pharoah PD, Thompson D, Ballinger DG, Struewing JP, Morrison J, Field H, Luben R, Wareham N, Ahmed S, Healey CS, Bowman R, Meyer KB, Haiman CA, Kolonel LK, Henderson BE, Le Marchand L, Brennan P, Sangrajrang S, Gaborieau V, Odefrey F, Shen CY, Wu PE, Wang HC, Eccles D, Evans DG, Peto J, Fletcher O, et al. Genome-wide association study identifies novel breast cancer susceptibility loci. Nature 2007, 447:1087-1093. 17529967.
5. Renwick A, Thompson D, Seal S, Kelly P, Chagtai T, Ahmed M, North B, Jayatilake H, Barfoot R, Spanova K, McGuffog L, Evans DG, Eccles D, Easton DF, Stratton MR, Rahman N. ATM mutations that cause ataxia-telangiectasia are breast cancer susceptibility alleles. Nat Genet 2006, 38:873-875. 16832357.
6. Wooster R, Weber BL. Breast and ovarian cancer. N Engl J Med 2003, 348:2339-2347. 12788999.
7. Meijers-Heijboer H, van den Ouweland A, Klijn J, Wasielewski M, de Snoo A, Oldenburg R, Hollestelle A, Houben M, Crepin E, van Veghel-Plandsoen M, Elstrodt F, van Duijn C, Bartels C, Meijers C, Schutte M, McGuffog L, Thompson D, Easton D, Sodha N, Seal S, Barfoot R, Mangion J, Chang-Claude J, Eccles D, Eeles R, Evans DG, Houlston R, Murday V, Narod S, Peretz T, et al. Low-penetrance susceptibility to breast cancer due to CHEK2(*)1100delC in noncarriers of BRCA1 or BRCA2 mutations. Nat Genet 2002, 31:55-59. 11967536.
8. Rahman N, Seal S, Thompson D, Kelly P, Renwick A, Elliott A, Reid S, Spanova K, Barfoot R, Chagtai T, Jayatilake H, McGuffog L, Hanks S, Evans DG, Eccles D, Easton DF, Stratton MR. PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene. Nat Genet 2007, 39:165-167. 17200668.
9. Seal S, Thompson D, Renwick A, Elliott A, Kelly P, Barfoot R, Chagtai T, Jayatilake H, Ahmed M, Spanova K, North B, McGuffog L, Evans DG, Eccles D, Easton DF, Stratton MR, Rahman N. Truncating mutations in the Fanconi anemia J gene BRIP1 are low-penetrance breast cancer susceptibility alleles. Nat Genet 2006, 38:1239-1241. 17033622.
10. Ripperger T, Gadzicki D, Meindl A, Schlegelberger B. Breast cancer susceptibility: current knowledge and implications for genetic counselling. Eur J Hum Genet 2009, 17:722-731. 19092773.
11. A physical map of the human genome. Nature 2001, 409:934-941.
12. Boeke JD, Stoye JP. Retrotransposons, endogenous retroviruses, and the evolution of retroelements. Retroviruses 1997, 343-435. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, Hughes S, Varmus H.
13. Jern P, Coffin JM. Effects of retroviruses on host genome function. Annu Rev Genet 2008, 42:709-732. 18694346.
14. Stoye J, Frankel W, Coffin J. DNA hybridization in dried gels with fragmented probes:an improvement over blotting techniques. Technique 1991, 3:123-128.
15. Barbulescu M, Turner G, Seaman MI, Deinard AS, Kidd KK, Lenz J. Many human endogenous retrovirus K (HERV-K) proviruses are unique to humans. Curr Biol 1999, 9:861-868. 10469592.
16. Belshaw R, Dawson AL, Woolven-Allen J, Redding J, Burt A, Tristem M. Genomewide screening reveals high levels of insertional polymorphism in the human endogenous retrovirus family HERV-K(HML2): implications for present-day activity. J Virol 2005, 79:12507-12514. 16160178.
17. Hughes JF, Coffin JM. Human endogenous retrovirus K solo-LTR formation and insertional polymorphisms: implications for human and viral evolution. Proc Natl Acad Sci U S A 2004, 101:1668-1672. 14757818.
18. Medstrand P, Mager DL. Human-specific integrations of the HERV-K endogenous retrovirus family. J Virol 1998, 72:9782-9787. 9811713.
19. Subramanian RP, Wildschutte JH, Russo C, Coffin JM. Identification, characterization, and comparative genomic distribution of the HERV-K (HML-2) group of human endogenous retroviruses. Retrovirology 2011, 8:90. 22067224.
20. Turner G, Barbulescu M, Su M, Jensen-Seaman MI, Kidd KK, Lenz J. Insertional polymorphisms of full-length endogenous retroviruses in humans. Curr Biol 2001, 11:1531-1535. 11591322.
21. Belshaw R, Pereira V, Katzourakis A, Talbot G, Paces J, Burt A, Tristem M. Long-term reinfection of the human genome by endogenous retroviruses. Proc Natl Acad Sci U S A 2004, 101:4894-4899. 15044706.
22. Beimforde N, Hanke K, Ammar I, Kurth R, Bannert N. Molecular cloning and functional characterization of the human endogenous retrovirus K113. Virology 2008, 371:216-225. 18076964.
23. Boller K, Schonfeld K, Lischer S, Fischer N, Hoffmann A, Kurth R, Tonjes RR. Human endogenous retrovirus HERV-K113 is capable of producing intact viral particles. J Gen Virol 2008, 89:567-572. 18198388.
24. Flockerzi A, Ruggieri A, Frank O, Sauter M, Maldener E, Kopper B, Wullich B, Seifarth W, Muller-Lantzsch N, Leib-Mosch C, Meese E, Mayer J. Expression patterns of transcribed human endogenous retrovirus HERV-K(HML-2) loci in human tissues and the need for a HERV Transcriptome Project. BMC Genomics 2008, 9:354. 18664271.
25. Seifarth W, Frank O, Zeilfelder U, Spiess B, Greenwood AD, Hehlmann R, Leib-Mosch C. Comprehensive analysis of human endogenous retrovirus transcriptional activity in human tissues with a retrovirus-specific microarray. J Virol 2005, 79:341-352. 15596828.
26. Costas J. Evolutionary dynamics of the human endogenous retrovirus family HERV-K inferred from full-length proviral genomes. J Mol Evol 2001, 53:237-243. 11523010.
27. Reus K, Mayer J, Sauter M, Scherer D, Muller-Lantzsch N, Meese E. Genomic organization of the human endogenous retrovirus HERV-K(HML-2.HOM) (ERVK6) on chromosome 7. Genomics 2001, 72:314-320. 11401447.
28. Dewannieux M, Harper F, Richaud A, Letzelter C, Ribet D, Pierron G, Heidmann T. Identification of an infectious progenitor for the multiple-copy HERV-K human endogenous retroelements. Genome Res 2006, 16:1548-1556. 17077319.
29. Lee YN, Bieniasz PD. Reconstitution of an infectious human endogenous retrovirus. PLoS Pathog 2007, 3:e10. 17257061.
30. Wang-Johanning F, Liu J, Rycaj K, Huang M, Tsai K, Rosen DG, Chen DT, Lu DW, Barnhart KF, Johanning GL. Expression of multiple human endogenous retrovirus surface envelope proteins in ovarian cancer. Int J Cancer 2007, 120:81-90. 17013901.
31. Boller K, Konig H, Sauter M, Mueller-Lantzsch N, Lower R, Lower J, Kurth R. Evidence that HERV-K is the endogenous retrovirus sequence that codes for the human teratocarcinoma-derived retrovirus HTDV. Virology 1993, 196:349-353. 8356806.
32. Herbst H, Sauter M, Kuhler-Obbarius C, Loning T, Mueller-Lantzsch N. Human endogenous retrovirus (HERV)-K transcripts in germ cell and trophoblastic tumours. APMIS 1998, 106:216-220. 9524581.
33. Lower R, Lower J, Frank H, Harzmann R, Kurth R. Human teratocarcinomas cultured in vitro produce unique retrovirus-like viruses. J Gen Virol 1984, 65(Pt 5):887-898. 6202829.
34. Ruprecht K, Ferreira H, Flockerzi A, Wahl S, Sauter M, Mayer J, Mueller-Lantzsch N. Human endogenous retrovirus family HERV-K(HML-2) RNA transcripts are selectively packaged into retroviral particles produced by the human germ cell tumor line Tera-1 and originate mainly from a provirus on chromosome 22q11.21. J Virol 2008, 82:10008-10016. 18684837.
35. Buscher K, Hahn S, Hofmann M, Trefzer U, Ozel M, Sterry W, Lower J, Lower R, Kurth R, Denner J. Expression of the human endogenous retrovirus-K transmembrane envelope, Rec and Np9 proteins in melanomas and melanoma cell lines. Melanoma Res 2006, 16:223-234. 16718269.
36. Buscher K, Trefzer U, Hofmann M, Sterry W, Kurth R, Denner J. Expression of human endogenous retrovirus K in melanomas and melanoma cell lines. Cancer Res 2005, 65:4172-4180. 15899808.
37. Hahn S, Ugurel S, Hanschmann KM, Strobel H, Tondera C, Schadendorf D, Lower J, Lower R. Serological response to human endogenous retrovirus K in melanoma patients correlates with survival probability. AIDS Res Hum Retroviruses 2008, 24:717-723. 18462078.
38. Mangeney M, Pothlichet J, Renard M, Ducos B, Heidmann T. Endogenous retrovirus expression is required for murine melanoma tumor growth in vivo. Cancer Res 2005, 65:2588-2591. 15805254.
39. Muster T, Waltenberger A, Grassauer A, Hirschl S, Caucig P, Romirer I, Fodinger D, Seppele H, Schanab O, Magin-Lachmann C, Lower R, Jansen B, Pehamberger H, Wolff K. An endogenous retrovirus derived from human melanoma cells. Cancer Res 2003, 63:8735-8741. 14695188.
40. Singh S, Kaye S, Francis N, Peston D, Gore M, McClure M, Bunker C. Human endogenous retrovirus K (HERV-K) rec mRNA is expressed in primary melanoma but not in benign naevi or normal skin. Pigment Cell Melanoma Res 2013, 26:426-428. 23311654.
41. Contreras-Galindo R, Kaplan MH, Leissner P, Verjat T, Ferlenghi I, Bagnoli F, Giusti F, Dosik MH, Hayes DF, Gitlin SD, Markovitz DM. Human endogenous retrovirus K (HML-2) elements in the plasma of people with lymphoma and breast cancer. J Virol 2008, 82:9329-9336. 18632860.
42. Iwabuchi H, Kakihara T, Kobayashi T, Imai C, Tanaka A, Uchiyama M, Fukuda T. A gene homologous to human endogenous retrovirus overexpressed in childhood acute lymphoblastic leukemia. Leuk Lymphoma 2004, 45:2303-2306. 15512821.
43. Armbruester V, Sauter M, Krautkraemer E, Meese E, Kleiman A, Best B, Roemer K, Mueller-Lantzsch N. A novel gene from the human endogenous retrovirus K expressed in transformed cells. Clin Cancer Res 2002, 8:1800-1807. 12060620.
44. Frank O, Verbeke C, Schwarz N, Mayer J, Fabarius A, Hehlmann R, Leib-Mosch C, Seifarth W. Variable transcriptional activity of endogenous retroviruses in human breast cancer. J Virol 2008, 82:1808-1818. 18077721.
45. Ono M, Kawakami M, Ushikubo H. Stimulation of expression of the human endogenous retrovirus genome by female steroid hormones in human breast cancer cell line T47D. J Virol 1987, 61:2059-2062. 2883329.
46. Wang-Johanning F, Frost AR, Jian B, Epp L, Lu DW, Johanning GL. Quantitation of HERV-K env gene expression and splicing in human breast cancer. Oncogene 2003, 22:1528-1535. 12629516.
47. Wang-Johanning F, Frost AR, Johanning GL, Khazaeli MB, LoBuglio AF, Shaw DR, Strong TV. Expression of human endogenous retrovirus k envelope transcripts in human breast cancer. Clin Cancer Res 2001, 7:1553-1560. 11410490.
48. Willer A, Saussele S, Gimbel W, Seifarth W, Kister P, Leib-Mosch C, Hehlmann R. Two groups of endogenous MMTV related retroviral env transcripts expressed in human tissues. Virus Genes 1997, 15:123-133. 9421877.
49. Faff O, Murray AB, Schmidt J, Leib-Mosch C, Erfle V, Hehlmann R. Retrovirus-like particles from the human T47D cell line are related to mouse mammary tumour virus and are of human endogenous origin. J Gen Virol 1992, 73(Pt 5):1087-1097. 1375276.
50. Seifarth W, Baust C, Murr A, Skladny H, Krieg-Schneider F, Blusch J, Werner T, Hehlmann R, Leib-Mosch C. Proviral structure, chromosomal location, and expression of HERV-K-T47D, a novel human endogenous retrovirus derived from T47D particles. J Virol 1998, 72:8384-8391. 9733890.
51. Seifarth W, Skladny H, Krieg-Schneider F, Reichert A, Hehlmann R, Leib-Mosch C. Retrovirus-like particles released from the human breast cancer cell line T47-D display type B- and C-related endogenous retroviral sequences. J Virol 1995, 69:6408-6416. 7545247.
52. Hook LM, Agafonova Y, Ross SR, Turner SJ, Golovkina TV. Genetics of mouse mammary tumor virus-induced mammary tumors: linkage of tumor induction to the gag gene. J Virol 2000, 74:8876-8883. 10982330.
53. Salmons B, Gunzburg WH. Current perspectives in the biology of mouse mammary tumour virus. Virus Res 1987, 8:81-102. 2823501.
54. Burmeister T, Ebert AD, Pritze W, Loddenkemper C, Schwartz S, Thiel E. Insertional polymorphisms of endogenous HERV-K113 and HERV-K115 retroviruses in breast cancer patients and age-matched controls. AIDS Res Hum Retroviruses 2004, 20:1223-1229. 15588344.
55. Krzysztalowska-Wawrzyniak M, Ostanek M, Clark J, Binczak-Kuleta A, Ostanek L, Kaczmarczyk M, Loniewska B, Wyrwicz LS, Brzosko M, Ciechanowicz A. The distribution of human endogenous retrovirus K-113 in health and autoimmune diseases in Poland. Rheumatology (Oxford) 2010, 7:13-21.
56. Moyes DL, Goris A, Ban M, Compston A, Griffiths DJ, Sawcer S, Venables PJ. HERV-K113 is not associated with multiple sclerosis in a large family-based study. AIDS Res Hum Retroviruses 2008, 24:363-365. 18327982.
57. Moyes DL, Martin A, Sawcer S, Temperton N, Worthington J, Griffiths DJ, Venables PJ. The distribution of the endogenous retroviruses HERV-K113 and HERV-K115 in health and disease. Genomics 2005, 86:337-341. 16024218.
58. Frankel WN, Stoye JP, Taylor BA, Coffin JM. A linkage map of endogenous murine leukemia proviruses. Genetics 1990, 124:221-236. 2155154.
59. Calle EE, Rodriguez C, Jacobs EJ, Almon ML, Chao A, McCullough ML, Feigelson HS, Thun MJ. The American Cancer Society Cancer Prevention Study II Nutrition Cohort: rationale, study design, and baseline characteristics. Cancer 2002, 94:500-511. 11900235.
60. Otowa T, Tochigi M, Rogers M, Umekage T, Kato N, Sasaki T. Insertional polymorphism of endogenous retrovirus HERV-K115 in schizophrenia. Neurosci Lett 2006, 408:226-229. 17000049.