Serum antibodies to the HPV16 proteome as biomarkers for head and neck cancer

British Journal of Cancer

Volumn 104, Issue 12, 2011, Pages 1896-1905

  Anderson, K S ^a   Wong, J ^a   D'Souza, G ^b   Riemer, A B ^a   Lorch, J ^a   Haddad, R ^a   Pai, S I ^c   Longtine, J ^d   McClean, M ^e   Labaer, J ^f   Kelsey, K T ^g   Posner, M ^h  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c DEPARTMENT OF PATHOLOGY   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e BOSTON UNIVERSITY SCHOOL OF PUBLIC HEALTH   (United States)

^f ARIZONA STATE UNIVERSITY   (United States)

^g BROWN UNIVERSITY   (United States)

^h MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

autoantibodies; biomarker; head and neck cancer; HPV; Luminex

Indexed keywords

AUTOANTIBODY; BIOLOGICAL MARKER; GLYCOPROTEIN E1; GLYCOPROTEIN E2; PROTEIN E4; PROTEIN E6; PROTEIN E7; PROTEOME; UNCLASSIFIED DRUG; VIRUS ANTIBODY;

ADULT; AGED; ANTIBODY BLOOD LEVEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FLUORESCENCE; HEAD AND NECK CANCER; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; MAJOR CLINICAL STUDY; MALE; NONHUMAN; OROPHARYNX CANCER; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; VIRUS CAPSID;

AGED; AGED, 80 AND OVER; ANTIBODIES, VIRAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMANS; MALE; MIDDLE AGED; ONCOGENE PROTEINS, VIRAL; OROPHARYNGEAL NEOPLASMS; PAPILLOMAVIRUS E7 PROTEINS; PROTEOME; REPRESSOR PROTEINS; TUMOR MARKERS, BIOLOGICAL;

EID: 79958087380     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2011.171     Document Type: Article

References (57)

1. Agoston ES, Robinson SJ, Mehra KK, Birch C, Semmel D, Mirkovic J, Haddad RI, Posner MR, Kindelberger D, Krane JF, Brodsky J, Crum CP (2010) Polymerase chain reaction detection of HPV in squamous carcinoma of the oropharynx. Am J Clin Pathol 134: 36-41
2. Agrawal Y, Koch WM, Xiao W, Westra WH, Trivett AL, Symer DE, Gillison ML (2008) Oral human papillomavirus infection before and after treatment for human papillomavirus 16-positive and human papilloma-virus 16-negative head and neck squamous cell carcinoma. Clin Cancer Res 14: 7143-7150
3. Anderson KS, LaBaer J (2005) The sentinel within: exploiting the immune system for cancer biomarkers. J Proteome Res 4: 1123-1133 (Pubitemid 41208670)
4. Anderson KS, Ramachandran N, Wong J, Raphael JV, Hainsworth E, Demirkan G, Cramer D, Aronzon D, Hodi FS, Harris L, Logvinenko T, LaBaer J (2008) Application of protein microarrays for multiplexed detection of antibodies to tumor antigens in breast cancer. J Proteome Res 7: 1490-1499
5. Andl T, Kahn T, Pfuhl A, Nicola T, Erber R, Conradt C, Klein W, Helbig M, Dietz A, Weidauer H, Bosch FX (1998) Etiological involvement of oncogenic human papillomavirus in tonsillar squamous cell carcinomas lacking retinoblastoma cell cycle control. Cancer Res 58: 5-13 (Pubitemid 28027707)
6. Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tan PF, Westra WH, Chung CH, Jordan RC, Lu C, Kim H, Axelrod R, Silverman CC, Redmond KP, Gillison ML (2010) Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 363: 24-35
7. Chung CH, Gillison ML (2009) Human papillomavirus in head and neck cancer: its role in pathogenesis and clinical implications. Clin Cancer Res 15: 6758-6762
8. D'Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, Westra WH, Gillison ML (2007) Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 356: 1944-1956 (Pubitemid 46740304)
9. Di Bonito P, Grasso F, Mochi S, Accardi L, Dona MG, Branca M, Costa S, Mariani L, Agarossi A, Ciotti M, Syrjanen K, Giorgi C (2006) Serum antibody response to Human papillomavirus (HPV) infections detected by a novel ELISA technique based on denatured recombinant HPV16 L1, L2, E4, E6 and E7 proteins. Infect Agent Cancer 1: 6
10. Dias D, Van Doren J, Schlottmann S, Kelly S, Puchalski D, Ruiz W, Boerckel P, Kessler J, Antonello JM, Green T, Brown M, Smith J, Chirmule N, Barr E, Jansen KU, Esser MT (2005) Optimization and validation of a multiplexed luminex assay to quantify antibodies to neutralizing epitopes on human papillomaviruses 6, 11, 16, and 18. Clin Diagn Lab Immunol 12: 959-969
11. Dillner J, Lenner P, Lehtinen M, Eklund C, Heino P, Wiklund F, Hallmans G, Stendahl U (1994) A population-based seroepidemiological study of cervical cancer. Cancer Res 54: 134-141 (Pubitemid 24042100)
12. Dillner J, Wiklund F, Lenner P, Eklund C, Frederiksson-Shanazarian V, Schiller JT, Hibma M, Hallmans G, Stendahl U (1995) Antibodies against linear and conformational epitopes of human papillomavirus type 16 that independently associate with incident cervical cancer. Int J Cancer 60: 377-382
13. Dunne EF, Unger ER, Sternberg M, McQuillan G, Swan DC, Patel SS, Markowitz LE (2007) Prevalence of HPV infection among females in the United States. JAMA 297: 813-819 (Pubitemid 46333946)
14. Faust H, Knekt P, Forslund O, Dillner J (2010) Validation of multiplexed human papillomavirus serology using pseudovirions bound to heparin coated beads. J Gen Virol 91: 1840-1848
15. Ferguson M, Wilkinson DE, Zhou T (2009) WHO meeting on the standardization of HPV assays and the role of the WHO HPV Laboratory Network in supporting vaccine introduction held on 24-25 January 2008, Geneva, Switzerland. Vaccine 27: 337-347
16. Frazer IH (2009) Interaction of human papillomaviruses with the host immune system: a well evolved relationship. Virology 384: 410-414
17. Furniss CS, McClean MD, Smith JF, Bryan J, Nelson HH, Peters ES, Posner MR, Clark JR, Eisen EA, Kelsey KT (2007) Human papillomavirus 16 and head and neck squamous cell carcinoma. Int J Cancer 120: 2386-2392 (Pubitemid 46642125)
18. Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, Zahurak ML, Daniel RW, Viglione M, Symer DE, Shah KV, Sidransky D (2000) Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 92: 709-720 (Pubitemid 30365531)
19. Herrero R, Castellsague X, Pawlita M, Lissowska J, Kee F, Balaram P, Rajkumar T, Sridhar H, Rose B, Pintos J, Fernandez L, Idris A, Sanchez MJ, Nieto A, Talamini R, Tavani A, Bosch FX, Reidel U, Snijders PJ, Meijer CJ, Viscidi R, Munoz N, Franceschi S (2003) Human papilloma-virus and oral cancer: the International Agency for Research on Cancer multicenter study. J Natl Cancer Inst 95: 1772-1783 (Pubitemid 38008900)
20. Kirnbauer R, Hubbert NL, Wheeler CM, Becker TM, Lowy DR, Schiller JT (1994) A virus-like particle enzyme-linked immunosorbent assay detects serum antibodies in a majority of women infected with human papillomavirus type 16. J Natl Cancer Inst 86: 494-499 (Pubitemid 24111004)
21. Kreimer AR, Clifford GM, Snijders PJ, Castellsague X, Meijer CJ, Pawlita M, Viscidi R, Herrero R, Franceschi S (2005) HPV16 semiquantitative viral load and serologic biomarkers in oral and oropharyngeal squamous cell carcinomas. Int J Cancer 115: 329-332 (Pubitemid 40586745)
22. Lehtinen M, Pawlita M, Zumbach K, Lie K, Hakama M, Jellum E, Koskela P, Luostarinen T, Paavonen J, Pukkala E, Sigstad E, Thoresen S, Dillner J (2003) Evaluation of antibody response to human papillomavirus early proteins in women in whom cervical cancer developed 1 to 20 years later. Am J Obstet Gynecol 188: 49-55 (Pubitemid 36135597)
23. Loning T, Ikenberg H, Becker J, Gissmann L, Hoepfer I, zur Hausen H (1985) Analysis of oral papillomas, leukoplakias, and invasive carcinomas for human papillomavirus type related DNA. J Invest Dermatol 84: 417-420 (Pubitemid 15056667)
24. Luevano M, Bernard HU, Barrera-Saldana HA, Trevino V, Garcia-Carranca A, Villa LL, Monk BJ, Tan X, Davies DH, Felgner PL, Kalantari M (2010) High-throughput profiling of the humoral immune responses against thirteen human papillomavirus types by proteome microarrays. Virology 405: 31-40
25. Markowitz LE, Sternberg M, Dunne EF, McQuillan G, Unger ER (2009) Seroprevalence of human papillomavirus types 6, 11, 16, and 18 in the United States: National Health and Nutrition Examination Survey 2003-2004. J Infect Dis 200: 1059-1067
26. Marur S, D'Souza G, Westra WH, Forastiere AA (2010) HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol 11: 781-789
27. Mork J, Lie AK, Glattre E, Hallmans G, Jellum E, Koskela P, Moller B, Pukkala E, Schiller JT, Youngman L, Lehtinen M, Dillner J (2001) Human papillomavirus infection as a risk factor for squamous-cell carcinoma of the head and neck. N Engl J Med 344: 1125-1131 (Pubitemid 32285233)
28. Opalka D, Lachman CE, MacMullen SA, Jansen KU, Smith JF, Chirmule N, Esser MT (2003) Simultaneous quantitation of antibodies to neutralizing epitopes on virus-like particles for human papillomavirus types 6, 11, 16, and 18 by a multiplexed luminex assay. Clin Diagn Lab Immunol 10: 108-115 (Pubitemid 36133838)
29. Posner MR, Lorch JH, Goloubeva O, Tan M, Schumaker LM, Sarlis NJ, Haddad RI, Cullen KJ (2011) Survival and human papillomavirus in oropharynx cancer in TAX 324: a subset analysis from an international phase III trial. Ann Oncol 22: 1071-1077
30. Rajeevan MS, Swan DC, Nisenbaum R, Lee DR, Vernon SD, Ruffin MT, Horowitz IR, Flowers LC, Kmak D, Tadros T, Birdsong G, Husain M, Srivastava S, Unger ER (2005) Epidemiologic and viral factors associated with cervical neoplasia in HPV-16-positive women. Int J Cancer 115: 114-120 (Pubitemid 40559675)
31. Ralston Howe E, Li Z, McGlennen RC, Hellerstedt WL, Downs Jr LS (2009) Type-specific prevalence and persistence of human papillomavirus in women in the United States who are referred for typing as a component of cervical cancer screening. Am J Obstet Gynecol 200: 245. e1-7
32. Ramachandran N, Anderson KS, Raphael JV, Hainsworth E, Sibani S, Montor W, Pacek M, Wong J, Eljanne M, Sanda MG, Hu Y, Logvinenko T, Labaer J (2008a) Tracking humoral responses using self assembling protein microarrays. Proteomics Clin Appl 2: 1518-1527
33. Ramachandran N, Hainsworth E, Bhullar B, Eisenstein S, Rosen B, Lau AY, Walter JC, LaBaer J (2004) Self-assembling protein microarrays. Science 305: 86-90 (Pubitemid 38869377)
34. Ramachandran N, Raphael JV, Hainsworth E, Demirkan G, Fuentes MG, Rolfs A, Hu Y, LaBaer J (2008b) Next-generation high-density self-assembling functional protein arrays. Nat Methods 5: 535-538 (Pubitemid 351761761)
35. Ravaggi A, Romani C, Pasinetti B, Tassi RA, Bignotti E, Bandiera E, Odicino FE, Ragnoli M, Donzelli C, Falchetti M, Calza S, Santin AD, Pecorelli S (2006) Correlation between serological immune response analyzed by a new ELISA for HPV-16/18 E7 oncoprotein and clinical characteristics of cervical cancer patients. Arch Virol 151: 1899-1916 (Pubitemid 44440492)
36. Reuschenbach M, Waterboer T, Wallin KL, Einenkel J, Dillner J, Hamsikova E, Eschenbach D, Zimmer H, Heilig B, Kopitz J, Pawlita M, Doeberitz MK, Wentzensen N (2008) Characterization of humoral immune responses against p16, p53, HPV16 E6 and HPV16 E7 in patients with HPV-associated cancers. Int J Cancer 123: 2626-2631
37. Ringstrom E, Peters E, Hasegawa M, Posner M, Liu M, Kelsey KT (2002) Human papillomavirus type 16 and squamous cell carcinoma of the head and neck. Clin Cancer Res 8: 3187-3192 (Pubitemid 35155029)
38. Rosales R, Lopez-Contreras M, Cortes RR (2001) Antibodies against human papillomavirus (HPV) type 16 and 18 E2, E6 and E7 proteins in sera: correlation with presence of papillomavirus DNA. J Med Virol 65: 736-744 (Pubitemid 33135103)
39. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378 (Pubitemid 36184095)
40. Schwartz SM, Daling JR, Doody DR, Wipf GC, Carter JJ, Madeleine MM, Mao EJ, Fitzgibbons ED, Huang S, Beckmann AM, McDougall JK, Galloway DA (1998) Oral cancer risk in relation to sexual history and evidence of human papillomavirus infection. J Natl Cancer Inst 90: 1626-1636 (Pubitemid 28523437)
41. Schwartz SR, Yueh B, McDougall JK, Daling JR, Schwartz SM (2001) Human papillomavirus infection and survival in oral squamous cell cancer: a population-based study. Otolaryngol Head Neck Surg 125: 1-9 (Pubitemid 33661083)
42. Smith EM, Pawlita M, Rubenstein LM, Haugen TH, Hamsikova E, Turek LP (2010) Risk factors and survival by HPV-16 E6 and E7 antibody status in human papillomavirus positive head and neck cancer. Int J Cancer 127: 111-117
43. Smith EM, Ritchie JM, Pawlita M, Rubenstein LM, Haugen TH, Turek LP, Hamsikova E (2007a) Human papillomavirus seropositivity and risks of head and neck cancer. Int J Cancer 120: 825-832 (Pubitemid 46175403)
44. Smith EM, Rubenstein LM, Ritchie JM, Lee JH, Haugen TH, Hamsikova E, Turek LP (2008a) Does pretreatment seropositivity to human papillo-mavirus have prognostic significance for head and neck cancers? Cancer Epidemiol Biomarkers Prev 17: 2087-2096
45. Smith EM, Summersgill KF, Allen J, Hoffman HT, McCulloch T, Turek LP, Haugen TH (2000) Human papillomavirus and risk of laryngeal cancer. Ann Otol Rhinol Laryngol 109: 1069-1076
46. Smith EM, Swarnavel S, Ritchie JM, Wang D, Haugen TH, Turek LP (2007b) Prevalence of human papillomavirus in the oral cavity/oropharynx in a large population of children and adolescents. Pediatr Infect Dis J 26: 836-840 (Pubitemid 47329857)
47. Smith EM, Wang D, Rubenstein LM, Morris WA, Turek LP, Haugen TH (2008b) Association between p53 and human papillomavirus in head and neck cancer survival. Cancer Epidemiol Biomarkers Prev 17: 421-427 (Pubitemid 351272796)
48. Smith JF, Kowalski R, Esser MT, Brown MJ, Bryan JT (2008c) Evolution of type-specific immunoassays to evaluate the functional immune response to Gardasil: a vaccine for human papillomavirus types 16, 18, 6 and 11. Hum Vaccin 4: 134-142 (Pubitemid 351881182)
49. Summersgill KF, Smith EM, Levy BT, Allen JM, Haugen TH, Turek LP (2001) Human papillomavirus in the oral cavities of children and adolescents. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 91: 62-69 (Pubitemid 33601612)
50. van Houten VM, Snijders PJ, van den Brekel MW, Kummer JA, Meijer CJ, van Leeuwen B, Denkers F, Smeele LE, Snow GB, Brakenhoff RH (2001) Biological evidence that human papillomaviruses are etiologically involved in a subgroup of head and neck squamous cell carcinomas. Int J Cancer 93: 232-235 (Pubitemid 32574279)
51. Vonka V, Sobotkova E, Hamsikova E, Smahel M, Zak R, Kitasato H, Sainerova H (1998) Induction of anti-tumour immunity by suicide-gene-modified HPV-16-transformed hamster cells. Int J Cancer 77: 470-475 (Pubitemid 28299887)
52. Wang SS, Schiffman M, Herrero R, Carreon J, Hildesheim A, Rodriguez AC, Bratti MC, Sherman ME, Morales J, Guillen D, Alfaro M, Clayman B, Burk RD, Viscidi RP (2004) Determinants of human papillomavirus 16 serological conversion and persistence in a population-based cohort of 10 000 women in Costa Rica. Br J Cancer 91: 1269-1274 (Pubitemid 39424786)
53. Waterboer T, Sehr P, Michael KM, Franceschi S, Nieland JD, Joos TO, Templin MF, Pawlita M (2005) Multiplex human papillomavirus serology based on in situ-purified glutathione s-transferase fusion proteins. Clin Chem 51: 1845-1853 (Pubitemid 41368175)
54. Wilczynski SP, Lin BT, Xie Y, Paz IB (1998) Detection of human papillomavirus DNA and oncoprotein overexpression are associated with distinct morphological patterns of tonsillar squamous cell carcinoma. Am J Pathol 152: 145-156 (Pubitemid 28028055)
55. Wilson VG, West M, Woytek K, Rangasamy D (2002) Papillomavirus E1 proteins: form, function, and features. Virus Genes 24: 275-290 (Pubitemid 34615304)
56. Wong J, Sibani S, Lokko NN, LaBaer J, Anderson KS (2009) Rapid detection of antibodies in sera using multiplexed self-assembling bead arrays. J Immunol Methods 350: 171-182
57. Zumbach K, Hoffmann M, Kahn T, Bosch F, Gottschlich S, Gorogh T, Rudert H, Pawlita M (2000) Antibodies against oncoproteins E6 and E7 of human papillomavirus types 16 and 18 in patients with head-and-neck squamous-cell carcinoma. Int J Cancer 85: 815-818 (Pubitemid 30131472)