Tumour-Associated Autoantibodies as Diagnostic Biomarkers for Breast Cancer: A Systematic Review and Meta-Analysis

Scandinavian Journal of Immunology

Volumn 83, Issue 6, 2016, Pages 393-408

  Xia, J ^a   Shi, J ^a   Wang, P ^a   Song, C ^a   Wang, K ^a   Zhang, J ^a   Ye, H ^a  

^a ZHENGZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CANCER ANTIBODY; CYCLIN B1 AUTOANTIBODY; HER2 AUTOANTIBODY; MUCIN 1 AUTOANTIBODY; NUCLEIC ACID; P53 AUTOANTIBODY; TUMOR ASSOCIATED AUTOANTIBODY; TUMOR MARKER; UNCLASSIFIED DRUG;

BREAST CANCER; CANCER DIAGNOSIS; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; MAMMOGRAPHY; MEDLINE; META ANALYSIS; NOMOGRAM; NORMAL VALUE; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN MICROARRAY; REVIEW; SENSITIVITY AND SPECIFICITY; SYSTEMATIC REVIEW; WEB OF SCIENCE;

EID: 84990208613     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/sji.12430     Document Type: Review

References (110)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87–108.
2. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015;65:5–29.
3. Lacombe J, Mangé A, Solassol J. Use of autoantibodies to detect the onset of breast cancer. J Immunol Res 2014;2014:1–8.
4. Lacombe J, Mange A, Jarlier M et al. Identification and validation of new autoantibodies for the diagnosis of DCIS and node negative early-stage breast cancers. Int J Cancer 2013;132:1105–13.
5. Anon. Cancer screening with digital mammography for women at average risk for breast cancer, magnetic resonance imaging (MRI) for women at high risk: an evidence-based analysis. Ont Health Technol Assess Ser 2010;10:1–55.
6. Fernandez-Madrid F, Maroun MC. Autoantibodies in breast cancer. Adv Clin Chem 2014;64:221–40.
7. Anderson KS, LaBaer J. The sentinel within: exploiting the immune system for cancer biomarkers. J Proteome Res 2005;4:1123–33.
8. Desmetz C, Mange A, Maudelonde T, Solassol J. Autoantibody signatures: progress and perspectives for early cancer detection. J Cell Mol Med 2011;15:2013–24.
9. Tan HT, Low J, Lim SG, Chung MC. Serum autoantibodies as biomarkers for early cancer detection. FEBS J 2009;276:6880–904.
10. Burford B, Gentry-Maharaj A, Graham R et al. Autoantibodies to MUC1 glycopeptides cannot be used as a screening assay for early detection of breast, ovarian, lung or pancreatic cancer. Br J Cancer 2013;108:2045–55.
11. Lu H, Ladd J, Feng Z et al. Evaluation of known oncoantibodies, HER2, p53, and cyclin B1, in prediagnostic breast cancer sera. Cancer Prev Res 2012;5:1036–43.
12. Hermsen BB, Verheijen RH, Menko FH et al. Humoral immune responses to MUC1 in women with a BRCA1 or BRCA2 mutation. Eur J Cancer 2007;43:1556–63.
13. Sangrajrang S, Arpornwirat W, Cheirsilpa A et al. Serum p53 antibodies in correlation to other biological parameters of breast cancer. Cancer Detect Prev 2003;27:182–6.
14. Croce MV, Isla-Larrain MT, Demichelis SO, Gori JR, Price MR, Segal-Eiras A. Tissue and serum MUC1 mucin detection in breast cancer patients. Breast Cancer Res Treat 2003;81:195–207.
15. Sorokine I, Ben-Mahrez K, Bracone A et al. Presence of circulating anti-c-myb oncogene product antibodies in human sera. Int J Cancer 1991;47:665–9.
16. Newman RA, Klein PJ, Uhlenbruck G, Citoler P, Karduck D. The presence and significance of the Thomsen-Friedenreich antigen in breast cancer. I. Serological studies. J Cancer Res Clin Oncol 1979;93:181–8.
17. Zhang T, Zhong W. Meta-DiSc software in meta-analysis of diagnostic test. J Evid Based Med 2008;8:97–100, +8.
18. Hayden SR, Brown MD. Likelihood ratio: a powerful tool for incorporating the results of a diagnostic test into clinical decisionmaking. Ann Emerg Med 1999;33:575–80.
19. Deeks JJ, Macaskill P, Irwig L. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol 2005;58:882–93.
20. Roscilli G, Cappelletti M, De Vitis C et al. Circulating MMP11 and specific antibody immune response in breast and prostate cancer patients. J Transl Med 2014;12:54.
21. Liu X, Chai Y, Li J et al. Autoantibody response to a novel tumor-associated antigen p90/CIP2A in breast cancer immunodiagnosis. Tumour Biol 2014;35:2661–7.
22. Liu T, Song YN, Shi QY, Liu Y, Bai XN, Pang D. Study of circulating antibodies against CD25 and FOXP3 in breast cancer. Tumour Biol 2014;35:3779–83.
23. Evans RL, Pottala JV, Egland KA. Classifying patients for breast cancer by detection of autoantibodies against a panel of conformation-carrying antigens. Cancer Prev Res 2014;7:545–55.
24. Ye H, Sun C, Ren P et al. Mini-array of multiple tumor-associated antigens (TAAs) in the immunodiagnosis of breast cancer. Oncol Lett 2013;5:663–8.
25. Yang Z, Chevolot Y, Gehin T et al. Improvement of protein immobilization for the elaboration of tumor-associated antigen microarrays: application to the sensitive and specific detection of tumor markers from breast cancer sera. Biosens Bioelectron 2013;40:385–92.
26. Olsen DA, Jakobsen EH, Brandslund I. Quantification of EGFR autoantibodies in the amplification phenomenon of HER2 in breast cancer. Clin Chem Lab Med 2013;51:2325–9.
27. Heo CK, Hwang HM, Ruem A et al. Identification of a mimotope for circulating anti-cytokeratin 8/18 antibody and its usage for the diagnosis of breast cancer. Int J Oncol 2013;42:65–74.
28. Dong X, Yang M, Sun H et al. Combined measurement of CA 15-3 with novel autoantibodies improves diagnostic accuracy for breast cancer. Onco Targets Ther 2013;6:273–9.
29. Sun Y, Zhang R, Wang M, Zhang Y, Qi J, Li J. SOX2 autoantibodies as noninvasive serum biomarker for breast carcinoma. Cancer Epidemiol Biomark Prev 2012;21:2043–7.
30. Lopez-Arias E, Aguilar-Lemarroy A, Felipe Jave-Suarez L et al. Alpha 1-antitrypsin: a novel tumor-associated antigen identified in patients with early-stage breast cancer. Electrophoresis 2012;33:2130–7.
31. Eric-Nikolic A, Milovanovic Z, Sanchez D et al. Overexpression of calreticulin in malignant and benign breast tumors: relationship with humoral immunity. Oncology 2012;82:48–55.
32. Chen X, Dong K, Long M et al. Serum anti-AEG-1 auto-antibody is a potential novel biomarker for malignant tumors. Oncol Lett 2012;4:319–23.
33. Mojtahedi Z, Safaei A, Yousefi Z, Ghaderi A. Immunoproteomics of HER2-positive and HER2-negative breast cancer patients with positive lymph nodes. OMICS 2011;15:409–18.
34. Marzocchella L, Sini V, Buonomo O et al. Spontaneous immunogenicity of ribosomal P0 protein in patients with benign and malignant breast lesions and delay of mammary tumor growth in P0-vaccinated mice. Cancer Sci 2011;102:509–15.
35. Lauterlein JJ, Petersen ER, Olsen DA, Ostergaard B, Brandslund I. Quantification of HER2 autoantibodies in the amplification phenomenon of HER2 in breast cancer. Clin Chem Lab Med 2011;49:877–83.
36. Hamrita B, Ben Nasr H, Hammann P et al. An elongation factor-like protein (EF-Tu) elicits a humoral response in infiltrating ductal breast carcinomas: an immunoproteomics investigation. Clin Biochem 2011;44:1097–104.
37. Blixt O, Bueti D, Burford B et al. Autoantibodies to aberrantly glycosylated MUC1 in early stage breast cancer are associated with a better prognosis. Breast Cancer Res 2011;13:R25.
38. Anderson KS, Sibani S, Wallstrom G et al. Protein microarray signature of autoantibody biomarkers for the early detection of breast cancer. J Proteome Res 2011;10:85–96.
39. Andersen RS, Sorensen RB, Ritter C et al. Identification of a cyclin B1-derived CTL epitope eliciting spontaneous responses in both cancer patients and healthy donors. Cancer Immunol Immunother 2011;60:227–34.
40. Wu M, Mao C, Chen Q, Cu X-W, Zhang W-S. Serum p53 protein and anti-p53 antibodies are associated with increased cancer risk: a case-control study of 569 patients and 879 healthy controls. Mol Biol Rep 2010;37:339–43.
41. Wandall HH, Blixt O, Tarp MA et al. Cancer biomarkers defined by autoantibody signatures to aberrant O-glycopeptide epitopes. Cancer Res 2010;70:1306–13.
42. Tang Y, Wang L, Zhang P et al. Detection of circulating anti-mucin 1 (MUC1) antibodies in breast tumor patients by indirect enzyme-linked immunosorbent assay using a recombinant MUC1 protein containing six tandem repeats and expressed in Escherichia coli. Clin Vaccine Immunol 2010;17:1903–8.
43. Shih NY, Lai HL, Chang GC et al. Anti-alpha-enolase autoantibodies are down-regulated in advanced cancer patients. Jpn J Clin Oncol 2010;40:663–9.
44. Kulic A, Sirotkovic-Skerlev M, Jelisavac-Cosic S, Herceg D, Kovac Z, Vrbanec D. Anti-p53 antibodies in serum: relationship to tumor biology and prognosis of breast cancer patients. Med Oncol 2010;27:887–93.
45. Yi JK, Chang JW, Han W et al. Autoantibody to tumor antigen, alpha 2-HS glycoprotein: a novel biomarker of breast cancer screening and diagnosis. Cancer Epidemiol Biomark Prev 2009;18:1357–64.
46. Tamesa MS, Kuramitsu Y, Fujimoto M et al. Detection of autoantibodies against cyclophilin A and triosephosphate isomerase in sera from breast cancer patients by proteomic analysis. Electrophoresis 2009;30:2168–81.
47. Souza AP, Albuquerque C, Torronteguy C et al. HspBP1 levels are elevated in breast tumor tissue and inversely related to tumor aggressiveness. Cell Stress Chaperones 2009;14:301–10.
48. Desmetz C, Bascoul-Mollevi C, Rochaix P et al. Identification of a new panel of serum autoantibodies associated with the presence of in situ carcinoma of the breast in younger women. Clin Cancer Res 2009;15:4733–41.
49. Zhong L, Ge K, Zu JC et al. Autoantibodies as potential biomarkers for breast cancer. Breast Cancer Res 2008;10:R40.
50. Wang CC, Huang YL, Ren CT et al. Glycan microarray of Globo H and related structures for quantitative analysis of breast cancer. Proc Natl Acad Sci USA 2008;105:11661–6.
51. Hamrita B, Chahed K, Kabbage M et al. Identification of tumor antigens that elicit a humoral immune response in breast cancer patients' sera by serological proteome analysis (SERPA). Clin Chim Acta 2008;393:95–102.
52. Desmetz C, Bibeau F, Boissiere F et al. Proteomics-based identification of HSP60 as a tumor-associated antigen in early stage breast cancer and ductal carcinoma in situ. J Proteome Res 2008;7:3830–7.
53. Anderson KS, Ramachandran N, Wong J et al. Application of protein microarrays for multiplexed detection of antibodies to tumor antigens in breast cancer. J Proteome Res 2008;7:1490–9.
54. Salama O, Herrmann S, Tziknovsky A et al. Chemiluminescent optical fiber immunosensor for detection of autoantibodies to ovarian and breast cancer-associated antigens. Biosens Bioelectron 2007;22:1508–16.
55. Chapman C, Murray A, Chakrabarti J et al. Autoantibodies in breast cancer: their use as an aid to early diagnosis. Ann Oncol 2007;18:868–73.
56. Pavoni E, Pucci A, Vaccaro P et al. A study of the humoral immune response of breast cancer patients to a panel of human tumor antigens identified by phage display. Cancer Detect Prev 2006;30:248–56.
57. Muller M, Meyer M, Schilling T et al. Testing for anti-p53 antibodies increases the diagnostic sensitivity of conventional tumor markers. Int J Oncol 2006;29:973–80.
58. Monstad SE, Storstein A, Dorum A et al. Yo antibodies in ovarian and breast cancer patients detected by a sensitive immunoprecipitation technique. Clin Exp Immunol 2006;144:53–8.
59. Mischo A, Kubuschok B, Ertan K et al. Prospective study on the expression of cancer testis genes and antibody responses in 100 consecutive patients with primary breast cancer. Int J Cancer 2006;118:696–703.
60. Looi K, Megliorino R, Shi FD, Peng XX, Chen Y, Zhang JY. Humoral immune response to p16, a cyclin-dependent kinase inhibitor in human malignancies. Oncol Rep 2006;16:1105–10.
61. Balogh GA, Mailo DA, Corte MM et al. Mutant p53 protein in serum could be used as a molecular marker in human breast cancer. Int J Oncol 2006;28:995–1002.
62. Bachelot T, Ratel D, Menetrier-Caux C, Wion D, Blay JY, Berger F. Autoantibodies to endostatin in patients with breast cancer: correlation to endostatin levels and clinical outcome. Br J Cancer 2006;94:1066–70.
63. Yagihashi A, Ohmura T, Asanuma K et al. Detection of autoantibodies to survivin and livin in sera from patients with breast cancer. Clin Chim Acta 2005;362:125–30.
64. Suzuki H, Graziano DF, McKolanis J, Finn OJ. T cell-dependent antibody responses against aberrantly expressed cyclin B1 protein in patients with cancer and premalignant disease. Clin Cancer Res 2005;11:1521–6.
65. Gao RJ, Bao HZ, Yang Q, Cong Q, Song JN, Wang L. The presence of serum anti-p53 antibodies from patients with invasive ductal carcinoma of breast: correlation to other clinical and biological parameters. Breast Cancer Res Treat 2005;93:111–5.
66. Atalay C, Atalay G, Yilmaz KB, Altinok M. The role of anti-CENP-B and anti-SS-B antibodies in breast cancer. Neoplasma 2005;52:32–5.
67. Fernandez-Madrid F, Tang N, Alansari H et al. Autoantibodies to annexin XI-A and other autoantigens in the diagnosis of breast cancer. Cancer Res 2004;64:5089–96.
68. Di Modugno F, Bronzi G, Scanlan MJ et al. Human Mena protein, a serex-defined antigen overexpressed in breast cancer eliciting both humoral and CD8+ T-cell immune response. Int J Cancer 2004;109:909–18.
69. Zhang JY, Casiano CA, Peng XX, Koziol JA, Chan EKL, Tan EM. Enhancement of antibody detection in cancer using panel of recombinant tumor-associated antigens. Cancer Epidemiol Biomark Prev 2003;12:136–43.
70. Shimada H, Ochiai T, Nomura F. Titration of serum p53 antibodies in 1085 patients with various types of malignant tumors – a multiinstitutional analysis by the Japan p53 Antibody Research Group. Cancer 2003;97:682–9.
71. Carter D, Dillon DC, Reynolds LD et al. Serum antibodies to lipophilin B detected in late stage breast cancer patients. Clin Cancer Res 2003;9:749–54.
72. Tomkiel JE, Alansari H, Tang N et al. Autoimmunity to the M(r) 32,000 subunit of replication protein A in breast cancer. Clin Cancer Res 2002;8:752–8.
73. Portefaix JM, Fanutti C, Granier C et al. Detection of anti-p53 antibodies by ELISA using p53 synthetic or phage-displayed peptides. J Immunol Methods 2002;259:65–75.
74. Tominaga O, Unsal K, Zalcman G, Soussi T. Detection of p73 antibodies in patients with various types of cancer: immunological characterization. Br J Cancer 2001;84:57–63.
75. Le Naour F, Misek DE, Krause MC et al. Proteomics-based identification of RS/DJ-1 as a novel circulating tumor antigen in breast cancer. Clin Cancer Res 2001;7:3328–35.
76. Hansen MH, Ostenstad B, Sioud M. Antigen-specific IgG antibodies in stage IV long-time survival breast cancer patients. Mol Med 2001;7:230–9.
77. von Mensdorff-Pouilly S, Verstraeten AA, Kenemans P et al. Survival in early breast cancer patients is favorably influenced by a natural humoral immune response to polymorphic epithelial mucin. J Clin Oncol 2000;18:574–83.
78. Haidopoulos D, Konstadoulakis MM, Antonakis PT et al. Circulating anti-CEA antibodies in the sera of patients with breast cancer. Eur J Surg Oncol 2000;26:742–6.
79. Pasquinelli R, Barba P, Capasso I et al. Circulating antibodies against the breast tumor marker GCDFP-15/gp17 in mammary carcinoma patients and in patients carrying benign breast conditions. Int J Cancer 1999;84:568–72.
80. Lenner P, Wiklund F, Emdin SO et al. Serum antibodies against p53 in relation to cancer risk and prognosis in breast cancer: a population-based epidemiological study. Br J Cancer 1999;79:927–32.
81. Stockert E, Jager E, Chen YT et al. A survey of the humoral immune response of cancer patients to a panel of human tumor antigens. J Exp Med 1998;187:1349–54.
82. Smyth PP, Shering SG, Kilbane MT et al. Serum thyroid peroxidase autoantibodies, thyroid volume, and outcome in breast carcinoma. J Clin Endocrinol Metab 1998;83:2711–6.
83. Jasinska J, Wiltschke C, Brodowicz T, Zielinski CC, Hoffmann-Sommergruber K, Zeillinger R. Anti-HER-2/neu antibodies detected in sera of patients with breast cancer, but also in healthy females. Eur J Cancer 1998;34:2135.
84. Frenkel K, Karkoszka J, Glassman T et al. Serum autoantibodies recognizing 5-hydroxymethyl-2′-deoxyuridine, an oxidized DNA base, as biomarkers of cancer risk in women. Cancer Epidemiol Biomark Prev 1998;7:49–57.
85. Fanelli MA, Cuello Carrion FD, Dekker J, Schoemaker J, Ciocca DR. Serological detection of heat shock protein hsp27 in normal and breast cancer patients. Cancer Epidemiol Biomark Prev 1998;7:791–5.
86. Coomber DW, Hawkins NJ, Dalley D, Ward RL. The significance of anti-sialyl-Tn antibodies in patients with colorectal and breast cancer. Neoplasma 1998;45:12–6.
87. Coomber D, Hawkins NJ, Clark M, Meagher A, Ward RL. Characterisation and clinicopathological correlates of serum anti-p53 antibodies in breast and colon cancer. J Cancer Res Clin Oncol 1996;122:757–62.
88. Mudenda B, Green JA, Green B et al. The relationship between serum p53 autoantibodies and characteristics of human breast cancer. Br J Cancer 1994;69:1115–9.
89. Green JA, Mudenda B, Jenkins J et al. Serum p53 auto-antibodies: incidence in familial breast cancer. Eur J Cancer 1994;30A:580–4.
90. Angelopoulou K, Diamandis EP, Sutherland DJ, Kellen JA, Bunting PS. Prevalence of serum antibodies against the p53 tumor suppressor gene protein in various cancers. Int J Cancer 1994;58:480–7.
91. Crawford LV, Pim DC, Bulbrook RD. Detection of antibodies against the cellular protein p53 in sera from patients with breast cancer. Int J Cancer 1982;30:403–8.
92. Zuo X, Chen L, Liu L et al. Identification of a panel of complex autoantigens (LGALS3, PHB2, MUC1, and GK2) in combination with CA15-3 for the diagnosis of early-stage breast cancer. Tumour Biol 2015; doi: 10.1007/s13277-015-3932-y
93. Wang J, Figueroa JD, Wallstrom G et al. Plasma autoantibodies associated with basal-like breast cancers. Cancer Epidemiol Biomark Prev 2015;24:1332–40.
94. Liu W, Li Y, Wang B, Dai L, Qian W, Zhang JY. Autoimmune response to IGF2 mRNA-binding protein 2 (IMP2/p62) in breast cancer. Scand J Immunol 2015;81:502–7.
95. Liu W, De La Torre IG, Gutierrez-Rivera MC et al. Detection of autoantibodies to multiple tumor-associated antigens (TAAs) in the immunodiagnosis of breast cancer. Tumour Biol 2015;36:1307–12.
96. Huang Y, Zhang C, Chen C et al. Investigation of circulating antibodies to ANXA1 in breast cancer. Tumour Biol 2015;36:1233–6.
97. Fernandez-Grijalva AL, Aguilar-Lemarroy A, Jave-Suarez LF et al. Alpha 2HS-glycoprotein, a tumor-associated antigen (TAA) detected in Mexican patients with early-stage breast cancer. J Proteomics 2015;112:301–12.
98. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–60.
99. Baldwin RW. Immunity to transplanted tumour: the effect of tumour extracts on the growth of homologous tumours in rats. Br J Cancer 1955;9:646–51.
100. John B, Graham RMG. Antibodies elicited by cancer in patients. Cancer 1955;8:409–16.
101. Tan EM, Zhang J. Autoantibodies to tumor-associated antigens: reporters from the immune system. Immunol Rev 2008;222:328–40.
102. Fernandez Madrid F. Autoantibodies in breast cancer sera: candidate biomarkers and reporters of tumorigenesis. Cancer Lett 2005;230:187–98.
103. Zaenker P, Ziman MR. Serologic autoantibodies as diagnostic cancer biomarkers–a review. Cancer Epidemiol Biomark Prev 2013;22:2161–81.
104. Mischo A, Wadle A, Watzig K et al. Recombinant antigen expression on yeast surface (RAYS) for the detection of serological immune responses in cancer patients. Cancer Immun 2003;3:5.
105. Schmetzer O, Moldenhauer G, Riesenberg R, Pires JR, Schlag P, Pezzutto A. Quality of recombinant protein determines the amount of autoreactivity detected against the tumor-associated epithelial cell adhesion molecule antigen: low frequency of antibodies against the natural protein. J Immunol 2005;174:942–52.
106. Ziegler A, Konig IR, Schulz-Knappe P. Challenges in planning and conducting diagnostic studies with molecular biomarkers. Dtsch Med Wochenschr 2013;138:e2–24.
107. Werner S, Chen H, Tao S, Brenner H. Systematic review: serum autoantibodies in the early detection of gastric cancer. Int J Cancer 2015;136:2243–52.
108. Swets JA. Measuring the accuracy of diagnostic systems. Science 1988;240:1285–93.
109. Kenneth F, Schulz DAG. The LANCET Handbook of Essential Concepts in Clinical Research. Beijing: People's Medical Publishing Housing, 2006:223 ISBN: 978-7-117-12873-5.
110. Fagan TJ. Letter: Nomogram for Bayes theorem. N Engl J Med 1975;293:257.