A bead-based multiplexed immunoassay to evaluate breast cancer biomarkers for early detection in pre-diagnostic serum

International Journal of Molecular Sciences

Volumn 13, Issue 10, 2012, Pages 13587-13604

  Opstal van Winden, Annemieke W J ^a,b   Rodenburg, Wendy ^c   Pennings, Jeroen L A ^c   van Oostrom, Conny T M ^c   Beijnen, Jos H ^b,d   Peeters, Petra H M ^a,e   van Gils, Carla H ^a   de Vries, Annemieke ^c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Biomarkers; Breast cancer; Detection; Pre diagnostic; Serum

Indexed keywords

ALPHA FETOPROTEIN; BIOLOGICAL MARKER; CA 125 ANTIGEN; CA 15-3 ANTIGEN; CA 19-9 ANTIGEN; CARCINOEMBRYONIC ANTIGEN; HAPTOGLOBIN; LEPTIN; MIGRATION INHIBITION FACTOR; OSTEOPONTIN; PROLACTIN; TUMOR MARKER; FETOPROTEIN; TUMOR ANTIGEN;

ARTICLE; BLOOD SAMPLING; BREAST CANCER; CANCER RISK; CANCER STAGING; CASE CONTROL STUDY; CONTROLLED STUDY; DIAGNOSTIC VALUE; EARLY DIAGNOSIS; FEMALE; HUMAN; IMMUNOASSAY; MAJOR CLINICAL STUDY; PROTEIN BLOOD LEVEL; SENSITIVITY AND SPECIFICITY; AGED; BLOOD; BREAST NEOPLASMS; COHORT ANALYSIS; DEMOGRAPHY; MIDDLE AGED; PATHOLOGY; PRINCIPAL COMPONENT ANALYSIS; PROSPECTIVE STUDY;

AGED; ANTIGENS, NEOPLASM; BREAST NEOPLASMS; CARCINOEMBRYONIC ANTIGEN; CASE-CONTROL STUDIES; COHORT STUDIES; DEMOGRAPHY; FEMALE; FETAL PROTEINS; HAPTOGLOBINS; HUMANS; IMMUNOASSAY; MIDDLE AGED; NEOPLASM STAGING; OSTEOPONTIN; PRINCIPAL COMPONENT ANALYSIS; PROLACTIN; PROSPECTIVE STUDIES; TUMOR MARKERS, BIOLOGICAL;

EID: 84870712444     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms131013587     Document Type: Article

References (73)

1. Boyd, N.F.; Guo, H.; Martin, L.J.; Sun, L.; Stone, J.; Fishell, E.; Jong, R.A.; Hislop, G.; Chiarelli, A.; Minkin, S.; et al. Mammographic density and the risk and detection of breast cancer. N. Engl. J. Med. 2007, 356, 227-236.
2. Ludwig, J.A.; Weinstein, J.N. Biomarkers in cancer staging, prognosis and treatment selection. Nat. Rev. Cancer 2005, 5, 845-856.
3. Kulasingam, V.; Zheng, Y.; Soosaipillai, A.; Leon, A.E.; Gion, M.; Diamandis, E.P. Activated leukocyte cell adhesion molecule: A novel biomarker for breast cancer. Int. J. Cancer 2009, 125, 9-14.
4. Pitteri, S.J.; Amon, L.M.; Busald, B.T.; Zhang, Y.; Johnson, M.M.; Chin, A.; Kennedy, J.; Wong, C.H.; Zhang, Q.; Wang, H.; et al. Detection of elevated plasma levels of epidermal growth factor receptor before breast cancer diagnosis among hormone therapy users. Cancer Res. 2010, 70, 8598-8606.
5. Arslan, N.; Serdar, M.; Deveci, S.; Ozturk, B.; Narin, Y.; Ilgan, S.; Ozturk, E.; Ozguven, M.A. Use of CA15-3, CEA and prolactin for the primary diagnosis of breast cancer and correlation with the prognostic factors at the time of initial diagnosis. Ann. Nucl. Med. 2000, 14, 395-399.
6. Eskelinen, M.; Kataja, V.; Hamalainen, E.; Kosma, V.M.; Penttila, I.; Alhava, E. Serum tumour markers CEA, AFP, CA 15-3, TPS and Neu in diagnosis of breast cancer. Anticancer Res. 1997, 17, 1231-1234.
7. Lumachi, F.; Basso, S.M.; Brandes, A.A.; Pagano, D.; Ermani, M. Relationship between tumor markers CEA and CA 15-3, TNM staging, estrogen receptor rate and MIB-1 index in patients with pT1-2 breast cancer. Anticancer Res. 2004, 24, 3221-3224.
8. Molina, R.; Jo, J.; Filella, X.; Zanon, G.; Pahisa, J.; Munoz, M.; Farrus, B.; Latre, M.L.; Escriche, C.; Estape, J.; et al. c-erbB-2 Oncoprotein, CEA, and CA 15.3 in patients with breast cancer: Prognostic value. Breast Cancer Res. Treat. 1998, 51, 109-119.
9. Robertson, J.F.; Pearson, D.; Price, M.R.; Selby, C.; Pearson, J.; Blamey, R.W.; Howell, A. Prospective assessment of the role of five tumour markers in breast cancer. Cancer Immunol. Immunother. 1991, 33, 403-410.
10. Hwa, H.L.; Kuo, W.H.; Chang, L.Y.; Wang, M.Y.; Tung, T.H.; Chang, K.J.; Hsieh, F.J. Prediction of breast cancer and lymph node metastatic status with tumour markers using logistic regression models. J. Eval. Clin. Pract. 2008, 14, 275-280.
11. Norum, L.F.; Erikstein, B.; Nustad, K. Elevated CA125 in breast cancer-A sign of advanced disease. Tumour Biol. 2001, 22, 223-228.
12. Sturgeon, C.M.; Duffy, M.J.; Stenman, U.H.; Lilja, H.; Brunner, N.; Chan, D.W.; Babaian, R.; Bast, R.C., Jr.; Dowell, B.; Esteva, F.J.; et al. National Academy of Clinical Biochemistry laboratory medicine practice guidelines for use of tumor markers in testicular, prostate, colorectal, breast, and ovarian cancers. Clin. Chem. 2008, 54, e11-e79.
13. Perou, C.M.; Sorlie, T.; Eisen, M.B.; van de Rijn, M.; Jeffrey, S.S.; Rees, C.A.; Pollack, J.R.; Ross, D.T.; Johnsen, H.; Akslen, L.A.; et al. Molecular portraits of human breast tumours. Nature 2000,406, 747-752.
14. Moore, R.G.; McMeekin, D.S.; Brown, A.K.; DiSilvestro, P.; Miller, M.C.; Allard, W.J.; Gajewski, W.; Kurman, R.; Bast, R.C., Jr.; Skates, S.J. A novel multiple marker bioassay utilizing HE4 and CA125 for the prediction of ovarian cancer in patients with a pelvic mass. Gynecol. Oncol. 2009, 112, 40-46.
15. Zhu, C.S.; Pinsky, P.F.; Cramer, D.W.; Ransohoff, D.F.; Hartge, P.; Pfeiffer, R.M.; Urban, N.; Mor, G.; Bast, R.C., Jr.; Moore, L.E.; et al. A framework for evaluating biomarkers for early detection: Validation of biomarker panels for ovarian cancer. Cancer Prev. Res. 2011, 4, 375-383.
16. Das, P.M.; Bast, R.C., Jr. Early detection of ovarian cancer. Biomark. Med. 2008, 2, 291-303.
17. Zhang, Z.; Yu, Y.; Xu, F.; Berchuck, A.; Haaften-Day, C.; Havrilesky, L.J.; de Bruijn, H.W.; van der Zee, A.G.; Woolas, R.P.; Jacobs, I.J.; et al. Combining multiple serum tumor markers improves detection of stage I epithelial ovarian cancer. Gynecol. Oncol. 2007, 107, 526-531.
18. Pepe, M.S.; Etzioni, R.; Feng, Z.; Potter, J.D.; Thompson, M.L.; Thornquist, M.; Winget, M.; Yasui, Y. Phases of biomarker development for early detection of cancer. J. Natl. Cancer. Inst. 2001, 93, 1054-1061.
19. Kim, B.K.; Lee, J.W.; Park, P.J.; Shin, Y.S.; Lee, W.Y.; Lee, K.A.; Ye, S.; Hyun, H.; Kang, K.N.; Yeo, D.; et al. The multiplex bead array approach to identifying serum biomarkers associated with breast cancer. Breast Cancer Res. 2009, 11, R22.
20. Verjans, E.; Noetzel, E.; Bektas, N.; Schutz, A.K.; Lue, H.; Lennartz, B.; Hartmann, A.; Dahl, E.; Bernhagen, J. Dual role of macrophage migration inhibitory factor (MIF) in human breast cancer. BMC Cancer 2009, 9, 230.
21. Xu, X.; Wang, B.; Ye, C.; Yao, C.; Lin, Y.; Huang, X.; Zhang, Y.; Wang, S. Overexpression of macrophage migration inhibitory factor induces angiogenesis in human breast cancer. Cancer Lett. 2008, 261, 147-157.
22. Sarcione, E.J.; Biddle, W. Elevated serum alpha fetoprotein levels in postmenopausal women with primary breast carcinoma. Dis. Markers 1987, 5, 75-79.
23. Park, I.J.; Choi, G.S.; Jun, S.H. Prognostic value of serum tumor antigen CA19-9 after curative resection of colorectal cancer. Anticancer Res. 2009, 29, 4303-4308.
24. Lee, H.; Rhee, H.; Kang, H.J.; Kim, H.S.; Min, B.S.; Kim, N.K.; Kim, H. Macrophage migration inhibitory factor may be used as an early diagnostic marker in colorectal carcinomas. Am. J. Clin. Pathol. 2008, 129, 772-779.
25. Meyer-Siegler, K.L.; Iczkowski, K.A.; Vera, P.L. Further evidence for increased macrophage migration inhibitory factor expression in prostate cancer. BMC Cancer 2005, 5, 73.
26. Xia, H.H.; Yang, Y.; Chu, K.M.; Gu, Q.; Zhang, Y.Y.; He, H.; Wong, W.M.; Leung, S.Y.; Yuen, S.T.; Yuen, M.F.; et al. Serum macrophage migration-inhibitory factor as a diagnostic and prognostic biomarker for gastric cancer. Cancer 2009, 115, 5441-5449.
27. Bando, H.; Matsumoto, G.; Bando, M.; Muta, M.; Ogawa, T.; Funata, N.; Nishihira, J.; Koike, M.; Toi, M. Expression of macrophage migration inhibitory factor in human breast cancer: association with nodal spread. Jpn. J. Cancer Res. 2002, 93, 389-396.
28. Tworoger, S.S.; Eliassen, A.H.; Sluss, P.; Hankinson, S.E. A prospective study of plasma prolactin concentrations and risk of premenopausal and postmenopausal breast cancer. J. Clin. Oncol. 2007, 25, 1482-1488.
29. Wu, M.H.; Chou, Y.C.; Chou, W.Y.; Hsu, G.C.; Chu, C.H.; Yu, C.P.; Yu, J.C.; Sun, C.A. Circulating levels of leptin, adiposity and breast cancer risk. Br. J. Cancer 2009, 100, 578-582.
30. Maccio, A.; Madeddu, C.; Gramignano, G.; Mulas, C.; Floris, C.; Massa, D.; Astara, G.; Chessa, P.; Mantovani, G. Correlation of body mass index and leptin with tumor size and stage of disease in hormone-dependent postmenopausal breast cancer: preliminary results and therapeutic implications. J. Mol. Med. 2010, 88, 677-686.
31. Ozet, A.; Arpaci, F.; Yilmaz, M.I.; Ayta, H.; Ozturk, B.; Komurcu, S.; Yavuz, A.A.; Tezcan, Y.; Acikel, C. Effects of tamoxifen on the serum leptin level in patients with breast cancer. Jpn. J. Clin. Oncol. 2001, 31, 424-427.
32. Tessitore, L.; Vizio, B.; Jenkins, O.; de Stefano, I.; Ritossa, C.; Argiles, J.M.; Benedetto, C.; Mussa, A. Leptin expression in colorectal and breast cancer patients. Int. J. Mol. Med. 2000, 5, 421-426.
33. Wijnhoven, S.W.; Zwart, E.; Speksnijder, E.N.; Beems, R.B.; Olive, K.P.; Tuveson, D.A.; Jonkers, J.; Schaap, M.M.; van den Berg, J.; Jacks, T.; et al. Mice expressing a mammary gland-specific R270H mutation in the p53 tumor suppressor gene mimic human breast cancer development. Cancer Res. 2005, 65, 8166-8173.
34. Krupke, D.M.; Begley, D.A.; Sundberg, J.P.; Bult, C.J.; Eppig, J.T. The mouse tumor biology database. Nat. Rev. Cancer 2008, 8, 459-465.
35. Rodenburg, W.; Pennings, J.L.; van Oostrom, C.T.; Roodbergen, M.; Kuiper, R.V.; Luijten, M.; de Vries, A. Identification of breast cancer biomarkers in transgenic mouse models: A proteomics approach. Proteomics Clin. Appl. 2010, 4, 603-612.
36. Hamrita, B.; Chahed, K.; Trimeche, M.; Guillier, C.L.; Hammann, P.; Chaieb, A.; Korbi, S.; Chouchane, L. Proteomics-based identification of alpha1-antitrypsin and haptoglobin precursors as novel serum markers in infiltrating ductal breast carcinomas. Clin. Chim. Acta 2009, 404, 111-118.
37. Fedarko, N.S.; Jain, A.; Karadag, A.; van Eman, M.R.; Fisher, L.W. Elevated serum bone sialoprotein and osteopontin in colon, breast, prostate, and lung cancer. Clin. Cancer Res. 2001, 7, 4060-4066.
38. Pitteri, S.J.; Faca, V.M.; Kelly-Spratt, K.S.; Kasarda, A.E.; Wang, H.; Zhang, Q.; Newcomb, L.; Krasnoselsky, A.; Paczesny, S.; Choi, G.; et al. Plasma proteome profiling of a mouse model of breast cancer identifies a set of up-regulated proteins in common with human breast cancer cells. J. Proteome Res. 2008, 7, 1481-1489.
39. Whiteaker, J.R.; Lin, C.; Kennedy, J.; Hou, L.; Trute, M.; Sokal, I.; Yan, P.; Schoenherr, R.M.; Zhao, L.; Voytovich, U.J.; et al. A targeted proteomics-based pipeline for verification of biomarkers in plasma. Nat. Biotechnol. 2011, 29, 625-634.
40. Pietrowska, M.; Marczak, L.; Polanska, J.; Behrendt, K.; Nowicka, E.; Walaszczyk, A.; Chmura, A.; Deja, R.; Stobiecki, M.; Polanski, A.; et al. Mass spectrometry-based serum proteome pattern analysis in molecular diagnostics of early stage breast cancer. J. Transl. Med. 2009, 7, 60.
41. Rudland, P.S.; Platt-Higgins, A.; El Tanani, M.; Silva Rudland, S.; Barraclough, R.; Winstanley, J.H.; Howitt, R.; West, C.R. Prognostic significance of the metastasis-associated protein osteopontin in human breast cancer. Cancer Res. 2002, 62, 3417-3427.
42. Tuck, A.B.; O'Malley, F.P.; Singhal, H.; Harris, J.F.; Tonkin, K.S.; Kerkvliet, N.; Saad, Z.; Doig, G.S.; Chambers, A.F. Osteopontin expression in a group of lymph node negative breast cancer patients. Int. J. Cancer 1998, 79, 502-508.
43. Wang, G.; Platt-Higgins, A.; Carroll, J.; Silva Rudland, S.; Winstanley, J.; Barraclough, R.; Rudland, P.S. Induction of metastasis by S100P in a rat mammary model and its association with poor survival of breast cancer patients. Cancer Res. 2006, 66, 1199-1207.
44. Bramwell, V.H.; Doig, G.S.; Tuck, A.B.; Wilson, S.M.; Tonkin, K.S.; Tomiak, A.; Perera, F.; Vandenberg, T.A.; Chambers, A.F. Serial plasma osteopontin levels have prognostic value in metastatic breast cancer. Clin. Cancer Res. 2006, 12, 3337-3343.
45. Singhal, H.; Bautista, D.S.; Tonkin, K.S.; O'Malley, F.P.; Tuck, A.B.; Chambers, A.F.; Harris, J.F. Elevated plasma osteopontin in metastatic breast cancer associated with increased tumor burden and decreased survival. Clin. Cancer Res. 1997, 3, 605-611.
46. Schwenk, J.M.; Gry, M.; Rimini, R.; Uhlen, M.; Nilsson, P. Antibody suspension bead arrays within serum proteomics. J. Proteome Res. 2008, 7, 3168-3179.
47. Schwenk, J.M.; Igel, U.; Kato, B.S.; Nicholson, G.; Karpe, F.; Uhlen, M.; Nilsson, P. Comparative protein profiling of serum and plasma using an antibody suspension bead array approach. Proteomics 2010, 10, 532-540.
48. Boker, L.K.; van Noord, P.A.; van der Schouw, Y.T.; Koot, N.V.; Bueno de Mesquita, H.B.; Riboli, E.; Grobbee, D.E.; Peeters, P.H. Prospect-EPIC Utrecht: Study design and characteristics of the cohort population. European Prospective Investigation into Cancer and Nutrition. Eur. J. Epidemiol. 2001, 17, 1047-1053.
49. Garofalo, C.; Surmacz, E. Leptin and cancer. J. Cell. Physiol. 2006, 207, 12-22.
50. Pepe, M.S.; Feng, Z.; Janes, H.; Bossuyt, P.M.; Potter, J.D. Pivotal evaluation of the accuracy of a biomarker used for classification or prediction: standards for study design. J. Natl. Cancer. Inst. 2008, 100, 1432-1438.
51. Jacobs, I.; Menon, U. The sine qua non of discovering novel biomarkers for early detection of ovarian cancer: Carefully selected preclinical samples. Cancer Prev. Res. 2011, 4, 299-302.
52. Opstal-van Winden, A.W.; Krop, E.J.; Karedal, M.H.; Gast, M.C.; Lindh, C.H.; Jeppsson, M.C.; Jonsson, B.A.; Grobbee, D.E.; Peeters, P.H.; Beijnen, J.H.; et al. Searching for early breast cancer biomarkers by serum protein profiling of pre-diagnostic serum; a nested case-control study. BMC Cancer 2011, 11, 381.
53. Conrads, T.P.; Fusaro, V.A.; Ross, S.; Johann, D.; Rajapakse, V.; Hitt, B.A.; Steinberg, S.M.; Kohn, E.C.; Fishman, D.A.; Whitely, G.; et al. High-resolution serum proteomic features for ovarian cancer detection. Endocr. Relat. Cancer 2004, 11, 163-178.
54. Ransohoff, D.F. Bias as a threat to the validity of cancer molecular-marker research. Nat. Rev. Cancer 2005, 5, 142-149.
55. Banks, R.E.; Stanley, A.J.; Cairns, D.A.; Barrett, J.H.; Clarke, P.; Thompson, D.; Selby, P.J. Influences of blood sample processing on low-molecular-weight proteome identified by surface-enhanced laser desorption/ionization mass spectrometry. Clin. Chem. 2005, 51, 1637-1649.
56. Engwegen, J.Y.; Alberts, M.; Knol, J.C.; Jimenez, C.R.; Depla, A.C.; Tuynman, H.; Snel, P.; Smits, M.E.; Cats, A.; Schellens, J.H.; et al. Influence of variations in sample handling on SELDI-TOF MS serum protein profiles for colorectal cancer. Proteomics Clin. Appl. 2008, 2, 936-945.
57. Hsieh, S.Y.; Chen, R.K.; Pan, Y.H.; Lee, H.L. Systematical evaluation of the effects of sample collection procedures on low-molecular-weight serum/plasma proteome profiling. Proteomics 2006, 6, 3189-3198.
58. Timms, J.F.; Arslan-Low, E.; Gentry-Maharaj, A.; Luo, Z.; T'Jampens, D.; Podust, V.N.; Ford, J.; Fung, E.T.; Gammerman, A.; Jacobs, I.; et al. Preanalytic influence of sample handling on SELDI-TOF serum protein profiles. Clin. Chem. 2007, 53, 645-656.
59. West-Nielsen, M.; Hogdall, E.V.; Marchiori, E.; Hogdall, C.K.; Schou, C.; Heegaard, N.H. Sample handling for mass spectrometric proteomic investigations of human sera. Anal. Chem. 2005, 77, 5114-5123.
60. Karsan, A.; Eigl, B.J.; Flibotte, S.; Gelmon, K.; Switzer, P.; Hassell, P.; Harrison, D.; Law, J.; Hayes, M.; Stillwell, M.; et al. Analytical and preanalytical biases in serum proteomic pattern analysis for breast cancer diagnosis. Clin. Chem. 2005, 51, 1525-1528.
61. Villanueva, J.; Philip, J.; Chaparro, C.A.; Li, Y.; Toledo-Crow, R.; DeNoyer, L.; Fleisher, M.; Robbins, R.J.; Tempst, P. Correcting common errors in identifying cancer-specific serum peptide signatures. J. Proteome Res. 2005, 4, 1060-1072.
62. Skates, S.J.; Menon, U.; MacDonald, N.; Rosenthal, A.N.; Oram, D.H.; Knapp, R.C.; Jacobs, I.J. Calculation of the risk of ovarian cancer from serial CA-125 values for preclinical detection in postmenopausal women. J. Clin. Oncol. 2003, 21, 206s-210s.
63. Pols, M.A.; Peeters, P.H.; Ocke, M.C.; Slimani, N.; Bueno-de-Mesquita, H.B.; Collette, H.J. Estimation of reproducibility and relative validity of the questions included in the EPIC Physical Activity Questionnaire. Int. J. Epidemiol. 1997, 26, S181-S189.
64. Troyanskaya, O.; Cantor, M.; Sherlock, G.; Brown, P.; Hastie, T.; Tibshirani, R.; Botstein, D.; Altman, R.B. Missing value estimation methods for DNA microarrays. Bioinformatics 2001, 17, 520-525.
65. The R Project for Statistical Computing. Available online: http://www.R-project.org (accessed on 26 October 2009).
66. Jackson, J.E. A User's Guide to Principal Components; Wiley: New York, NY, USA, 2003.
67. Ringner, M. What is principal component analysis? Nat. Biotechnol. 2008, 26, 303-304.
68. Breiman, L. Random Forests. Mach. Learn. 2001, 45, 5-32.
69. Liaw, A.; Wiener, M. Classification and Regression by Random Forests. R. News 2002, 2, 18-22.
70. Barrett, J.H.; Cairns, D.A. Application of the random forest classification method to peaks detected from mass spectrometric proteomic profiles of cancer patients and controls. Stat. Appl. Genet. Mol. Biol. 2008, 7, Article4.
71. Diaz-Uriarte, R.; Alvarez de Andrés, S. Gene selection and classification of microarray data using random forest. BMC Bioinf. 2006, 7, 3.
72. Lunetta, K.L.; Hayward, L.B.; Segal, J.; Van, E.P. Screening large-scale association study data: exploiting interactions using random forests. BMC Genet. 2004, 5, 32.
73. Carlsson, A.; Wingren, C.; Ingvarsson, J.; Ellmark, P.; Baldertorp, B.; Ferno, M.; Olsson, H.; Borrebaeck, C.A. Serum proteome profiling of metastatic breast cancer using recombinant antibody microarrays. Eur. J. Cancer 2008, 44, 472-480.