Biomarker method validation in anticancer drug development

British Journal of Pharmacology

Volumn 153, Issue 4, 2008, Pages 646-656

  Cummings, J ^a   Ward, T H ^a   Greystoke, A ^a   Ranson, M ^b   Dive, C ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b CHRISTIE HOSPITAL   (United Kingdom)

Author keywords

Anticancer drugs; Biomarker; Clinical trials; M30 and M65 ELISAs; Mass spectrometry; Method validation

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CYTOKERATIN 18; CYTOKERATIN 19; CYTOKERATIN 8; PROSTATE SPECIFIC ANTIGEN; TUMOR MARKER;

CANCER DIAGNOSIS; CANCER RESEARCH; CELL DEATH; DIAGNOSTIC ACCURACY; ENZYME LINKED IMMUNOSORBENT ASSAY; GOOD CLINICAL PRACTICE; GOOD LABORATORY PRACTICE; MASS SPECTROMETRY; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN PHOSPHORYLATION; QUALITY CONTROL; REVIEW; VALIDATION STUDY;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOMARKERS, PHARMACOLOGICAL; CELL DEATH; CLINICAL TRIALS AS TOPIC; DRUG EVALUATION, PRECLINICAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GUIDELINE ADHERENCE; GUIDELINES AS TOPIC; HUMANS; KERATIN-18; LABORATORIES; MASS SPECTROMETRY; PROTEINS; QUALITY CONTROL; REPRODUCIBILITY OF RESULTS; TERMINOLOGY AS TOPIC;

EID: 39449114054     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0707441     Document Type: Review

References (103)

1. Aebersold R, Goodlett DR (2001). Mass spectrometry in proteomics. Chem Rev 101: 269-295.
2. Baggerly KA, Morris JS, Coombes KR (2004). Reproducibility of SELDI-TOF protein patterns in serum: comparing datasets from different experiments. Bioinformatics 20: 777-785.
3. Baggerly KA, Morris JS, Edmonson SR, Coombes KR (2005). Signal in noise: evaluating reported reproducibility of serum proteomic tests for ovarian cancer. J Natl Cancer Inst 97: 307-309.
4. Bansal S, DeStefano A (2007). Key elements of bioanalytical method validation for small molecules. AAPS J 9: E109-E114.
5. Bantel H, Lugering A, Heidemann J, Volkmann X, Poremba C, Strassburg CP et al. (2004). Detection of apoptotic caspase activation in sera from patients with chronic HCV infection is associated with fibrotic liver injury. Hepatology 40: 1078-1087.
6. Barak V, Goike H, Panaretakis KW, Einarsson R (2004). Clinical utility of cytokeratins as tumor markers. Clin Biochem 37: 529-540.
7. Barker PE (2003). Cancer biomarker validation: standards and process: roles for the National Institute of Standards and Technology (NIST). Ann NY Acad Sci 983: 142-150.
8. Barnidge DR, Goodmanson MK, Klee GG, Muddiman DC (2004). Absolute quantification of the model biomarker prostate-specific antigen in serum by LC-MS/MS using protein cleavage and isotope dilution mass spectrometry. J Proteome Res 3: 644-652.
9. Basil CF, Zhao Y, Zavaglia K, Jin P, Panelli MC, Voiculescu S et al. (2006). Common cancer biomarkers. Cancer Res 66: 2953-2961.
10. Baskin-Bey ES, Washburn K, Feng S, Oltersdorf T, Shapiro D, Huyghe M et al. (2007). Clinical trial of the pan-caspase inhibitor, IDN-6556, in human liver preservation injury. Am J Transplant 7: 218-225.
11. Bast Jr RC, Lilja H, Urban N, Rimm DL, Fritsche H, Gray J et al. (2005). Translational crossroads for biomarkers. Clin Cancer Res 11: 6103-6108.
12. Biven K, Erdal H, Hagg M, Ueno T, Zhou R, Lynch M et al. (2003). A novel assay for discovery and characterization of pro-apoptotic drugs and for monitoring apoptosis in patient sera. Apoptosis 8: 263-268.
13. Bottari P, Aebersold R, Turecek F, Gelb MH (2004). Design and synthesis of visible isotope-coded affinity tags for the absolute quantification of specific proteins in complex mixtures. Bioconjug Chem 15: 380-388.
14. Bronstrup M (2004). Absolute quantification strategies in proteomics based on mass spectrometry. Expert Rev Proteomics 1: 503-512.
15. Carr NJ (2000). M30 expression demonstrates apoptotic cells, correlates with in situ end-labeling, and is associated with Ki-67 expression in large intestinal neoplasms. Arch Pathol Lab Med 124: 1768-1772.
16. Collins I, Workman P (2006). New approaches to molecular cancer therapeutics. Nat Chem Biol 2: 689-700.
17. Cummings J, Ranson M, Butt F, Moore D, Dive C (2007). Qualification of M30 and M65 ELISAs as surrogate biomarkers of cell death: long term antigen stability in cancer patient plasma. Cancer Chemother Pharmacol Online first.
18. Cummings J, Ranson M, Lacasse E, Ganganagari JR, St-Jean M, Jayson G et al. (2006). Method validation and preliminary qualification of pharmacodynamic biomarkers employed to evaluate the clinical efficacy of an antisense compound (AEG35156) targeted to the X-linked inhibitor of apoptosis protein XIAP. Br J Cancer 95: 42-48.
19. Cummings J, Ward TH, Lacasse E, Lefebvre C, St-Jean M, Durkin J et al. (2005). Validation of pharmacodynamic assays to evaluate the clinical efficacy of an antisense compound (AEG 35156) targeted to the X-linked inhibitor of apoptosis protein XIAP. Br J Cancer 92: 532-538.
20. Demiray M, Ulukaya EE, Arslan M, Gokgoz S, Saraydaroglu O, Ercan I et al. (2006). Response to neoadjuvant chemotherapy in breast cancer could be predictable by measuring a novel serum apoptosis product, caspase-cleaved cytokeratin 18: a prospective pilot study. Cancer Invest 24: 669-676.
21. DeSilva B, Smith W, Weiner R, Kelley M, Smolec J, Lee B et al. (2003). Recommendations for the bioanalytical method validation of ligand-binding assays to support pharmacokinetic assessments of macromolecules. Pharm Res 20: 1885-1900.
22. Ditzel HJ, Strik MC, Larsen MK, Willis AC, Waseem A, Kejling K et al. (2002). Cancer-associated cleavage of cytokeratin 8/18 heterotypic complexes exposes a neoepitope in human adenocarcinomas. J Biol Chem 277: 21712-21722.
23. Duan WR, Garner DS, Williams SD, Funckes-Shippy CL, Spath IS, Blomme EA (2003). Comparison of immunohistochemistry for activated caspase-3 and cleaved cytokeratin 18 with the TUNEL method for quantification of apoptosis in histological sections of PC-3 subcutaneous xenografts. J Pathol 199: 221-228.
24. Einarsson R, Barak V (1997). TPS: a cytokeratin serum tumour marker for effective therapy control of cancer patient with focus on breast cancer. J Clin Ligand Assay 22: 348-351.
25. Engwegen JY, Gast MC, Schellens JH, Beijnen JH (2006). Clinical proteomics: searching for better tumour markers with SELDI-TOF mass spectrometry. Trends Pharmacol Sci 27: 251-259.
26. FDA (1997). Code of Federal Regulation Title 21, Part 11. Electronic Records, Electronic Signatures.
27. FDA (2001a). Guidance for Industry: Bioanalytical Method Validation.
28. FDA (2001b). Code of Federal Regulation Title 42, Vol 3. Clinical Laboratory Improvement Amendment.
29. Fenselau C (2007). A review of quantitiative methods for proteomic studies. J Chromatogr B Analyt Technol Biomed Life Sci 855: 14-20.
30. Findlay JW, Smith WC, Lee JW, Nordblom GD, Das I, DeSilva BS et al. (2000). Validation of immunoassays for bioanalysis: a pharmaceutical industry perspective. J Pharm Biomed Anal 21: 1249-1273.
31. Fontaine N, Rosengren B (2001). Directive 2001/20/EC of the European Parliament and of the Council: on the approximation of the laws, regulations and administrative provisions of the Member States relating to the implementation of good clinical practice in the conduct of clinical trials on medicinal products for human use. OJEC L121: 34-44.
32. Fuchs E, Weber K (1994). Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem 63: 345-382.
33. Gerber SA, Rush J, Stemman O, Kirschner MW, Gygi SP (2003). Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc Natl Acad Sci USA 100: 6940-6945.
34. Goodsaid F, Frueh F (2007). Biomarker qualification pilot process at the US Food and Drug Administration. AAPS J 9: E105-E108.
35. Gu S, Pan S, Bradbury EM, Chen X (2002). Use of deuterium-labeled lysine for efficient protein identification and peptide de novo sequencing. Anal Chem 74: 5774-5785.
36. Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999). Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17: 994-999.
37. HMSO (2004). UK Statutory Instrument 2004 No. 1031. The Medicines for Human Use (Clinical Trials) Regulations 2004.
38. HMSO (2006). UK Statutory Instrument 2006 No. 1928. The Medicines for Human Use (Clinical Trials) Amendment Regulations 2006.
39. James CA, Hill HM (2007). Procedural elements involved in maintaining bioanalytical data integrity for good laboratory practices and regulated clinical studies. AAPS J 9: E123-E127.
40. Johann Jr DJ, McGuigan MD, Patel AR, Tomov S, Ross S, Conrads TP et al. (2004). Clinical proteomics and biomarker discovery. Ann NY Acad Sci 1022: 295-305.
41. Jones CD, Yeung C, Zehnder JL (2003). Comprehensive validation of a real-time quantitative bcr-abl assay for clinical laboratory use. Am J Clin Pathol 120: 42-48.
42. Kadyrov M, Kaufmann P, Huppertz B (2001). Expression of a cytokeratin 18 neo-epitope is a specific marker for trophoblast apoptosis in human placenta. Placenta 22: 44-48.
43. Kelloff GJ, Bast Jr RC, Coffey DS, D'Amico AV, Kerbel RS, Park JW et al. (2004). Biomarkers, surrogate end points, and the acceleration of drug development for cancer prevention and treatment: an update prologue. Clin Cancer Res 10: 3881-3884.
44. Kelloff GJ, Sigman CC (2005). New science-based endpoints to accelerate oncology drug development. Eur J Cancer 41: 491-501.
45. Kirkpatrick DS, Gerber SA, Gygi SP (2005). The absolute quantification strategy: a general procedure for the quantification of proteins and post-translational modifications. Methods 35: 265-273.
46. Korfmacher WA (2005). Principles and applications of LC-MS in new drug discovery. Drug Discov Today 10: 1357-1367.
47. Kramer G, Erdal H, Mertens HJ, Nap M, Mauermann J, Steiner G et al. (2004). Differentiation between cell death modes using measurements of different soluble forms of extracellular cytokeratin 18. Cancer Res 64: 1751-1756.
48. Kramer G, Schwarz S, Hagg M, Havelka AM, Linder S (2006). Docetaxel induces apoptosis in hormone refractory prostate carcinomas during multiple treatment cycles. Br J Cancer 94: 1592-1598.
49. Kronenberger B, Wagner M, Herrmann E, Mihm U, Piiper A, Sarrazin C et al. (2005). Apoptotic cytokeratin 18 neoepitopes in serum of patients with chronic hepatitis C. J Viral Hepat 12: 307-314.
50. Ku NO, Liao J, Omary MB (1997). Apoptosis generates stable fragments of human type I keratins. J Biol Chem 272: 33197-33203.
51. Kummar S, Gutierrez M, Doroshow JH, Murgo AJ (2006). Drug development in oncology: classical cytotoxics and molecularly targeted agents. Br J Clin Pharmacol 62: 15-26.
52. Lee JW, Devanarayan V, Barrett YC, Weiner R, Allinson J, Fountain S et al. (2006). Fit-for-purpose method development and validation for successful biomarker measurement. Pharm Res 23: 312-328.
53. Lee JW, Figeys D, Vasilescu J (2007). Biomarker assay translation from discovery to clinical studies in cancer drug development: quantification of emerging protein biomarkers. Adv Cancer Res 96: 269-298.
54. Lee JW, Weiner RS, Sailstad JM, Bowsher RR, Knuth DW, O'Brien PJ et al. (2005). Method validation and measurement of biomarkers in nonclinical and clinical samples in drug development: a conference report. Pharm Res 22: 499-511.
55. Leers MP, Bjorklund V, Bjorklund B, Jornvall H, Nap M (2002). An immunohistochemical study of the clearance of apoptotic cellular fragments. Cell Mol Life Sci 59: 1358-1365.
56. Leers MP, Kolgen W, Bjorklund V, Bergman T, Tribbick G, Persson B et al. (1999). Immunocytochemical detection and mapping of a cytokeratin 18 neo-epitope exposed during early apoptosis. J Pathol 187: 567-572.
57. Lesko LJ, Atkinson Jr AJ (2001). Use of biomarkers and surrogate endpoints in drug development and regulatory decision making: criteria, validation, strategies. Annu Rev Pharmacol Toxicol 41: 347-366.
58. Lin S, Shaler TA, Becker CH (2006). Quantification of intermediate-abundance proteins in serum by multiple reaction monitoring mass spectrometry in a single-quadrupole ion trap. Anal Chem 78: 5762-5767.
59. Linder S, Havelka AM, Ueno T, Shoshan MC (2004). Determining tumor apoptosis and necrosis in patient serum using cytokeratin 18 as a biomarker. Cancer Lett 214: 1-9.
60. Liu MY, Xydakis AM, Hoogeveen RC, Jones PH, Smith EO, Nelson KW et al. (2005). Multiplexed analysis of biomarkers related to obesity and the metabolic syndrome in human plasma, using the Luminex-100 system. Clin Chem 51: 1102-1109.
61. Ludwig JA, Weinstein JN (2005). Biomarkers in cancer staging, prognosis and treatment selection. Nat Rev Cancer 5: 845-856.
62. Maruvada P, Srivastava S (2006). Joint National Cancer Institute-Food and Drug Administration workshop on research strategies, study designs, and statistical approaches to biomarker validation for cancer diagnosis and detection. Cancer Epidemiol Biomarkers Prev 15: 1078-1082.
63. Miller KJ, Bowsher RR, Celniker A, Gibbons J, Gupta S, Lee JW et al. (2001). Workshop on bioanalytical methods validation for macromolecules: summary report. Pharm Res 18: 1373-1383.
64. NIH (2001). Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 69: 89-95.
65. Nowatzke W, Wood E (2007). Best practices during bioanalytical method validation for the characterisation of assay reagents and the evaluation of analyte stability in assay standards, quality controls and study samples. AAPS J 9: E117-E122.
66. Olofsson MH, Ueno T, Pan Y, Xu R, Cai F, van der Kuip H et al. (2007). Cytokeratin-18 is a useful serum biomarker for early determination of response of breast carcinomas to chemotherapy. Clin Cancer Res 13: 3198-3206.
67. Pepe MS, Etzioni R, Feng Z, Potter JD, Thompson ML, Thornquist M et al. (2001). Phases of biomarker development for early detection of cancer. J Natl Cancer Inst 93: 1054-1061.
68. Peters FT, Drummer OH, Musshoff F (2007). Validation of new methods. Forensic Sci Int 165: 216-224.
69. Petricoin EF, Ardekani AM, Hitt BA, Levine PJ, Fusaro VA, Steinberg SM et al. (2002). Use of proteomic patterns in serum to identify ovarian cancer. Lancet 359: 572-577.
70. Poon TC (2007). Opportunities and limitations of SELDI-TOF-MS in biomedical research: practical advices. Expert Rev Proteomics 4: 51-65.
71. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S et al. (2004). Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3: 1154-1169.
72. Roth GA, Krenn C, Brunner M, Moser B, Ploder M, Spittler A et al. (2004). Elevated serum levels of epithelial cell apoptosis-specific cytokeratin 18 neoepitope M30 in critically ill patients. Shock 22: 218-220.
73. Rupa JD, de Bruine AP, Gerbers AJ, Leers MP, Nap M, Kessels AG et al. (2003). Simultaneous detection of apoptosis and proliferation in colorectal carcinoma by multiparameter flow cytometry allows separation of high and low-turnover tumors with distinct clinical outcome. Cancer 97: 2404-2411.
74. Sarker D, Workman P (2007). Pharmacodynamic biomarkers for molecular cancer therapeutics. Adv Cancer Res 96: 213-268.
75. Scholler N, Crawford M, Sato A, Drescher CW, O'Briant KC, Kiviat N et al. (2006). Bead-based ELISA for validation of ovarian cancer early detection markers. Clin Cancer Res 12: 2117-2124.
76. Schutte B, Henfling M, Kolgen W, Bouman M, Meex S, Leers MP et al. (2004). Keratin 8/18 breakdown and reorganization during apoptosis. Exp Cell Res 297: 11-26.
77. Seligson DB (2005). The tissue micro-array as a translational research tool for biomarker profiling and validation. Biomarkers 10 (Suppl 1): S77-S82.
78. Shah VP (2007). The history of bioanalytical method validation and regulation: evolution of a guidance document on bioanalytical methods validation. AAPS J 9: E43-E47.
79. Shah VP, Midha KK, Dighe S, McGilveray IJ, Skelly JP, Yacobi A et al. (1991). Analytical methods validation: bioavailability, bioequivalence and pharmacokinetic studies. Conference report. Eur J Drug Metab Pharmacokinet 16: 249-255.
80. Shah VP, Midha KK, Findlay JW, Hill HM, Hulse JD, McGilveray IJ et al. (2000). Bioanalytical method validation - a revisit with a decade of progress. Pharm Res 17: 1551-1557.
81. Simpkins F, Czechowicz JA, Liotta L, Kohn EC (2005). SELDI-TOF mass spectrometry for cancer biomarker discovery and serum proteomic diagnostics. Pharmacogenomics 6: 647-653.
82. Smith WC, Sittampalam GS (1998). Conceptual and statistical issues in the validation of analytic dilution assays for pharmaceutical applications. J Biopharm Stat 8: 509-532.
83. Smolec J, DeSilva B, Smith W, Weiner R, Kelly M, Lee B et al. (2005). Bioanalytical method validation for macromolecules in support of pharmacokinetic studies. Pharm Res 22: 1425-1431.
84. Stemmann O, Zou H, Gerber SA, Gygi SP, Kirschner MW (2001). Dual inhibition of sister chromatid separation at metaphase. Cell 107: 715-726.
85. Stiles T (2004). Good Clinical Laboratory Practice Accreditation Scheme.
86. Stiles T, Grant V, Mawbery N (2003). Good Clinical Laboratory Practice (GCLP): BARQA.
87. Strnad P, Windoffer R, Leube RE (2002). Induction of rapid and reversible cytokeratin filament network remodeling by inhibition of tyrosine phosphatases. J Cell Sci 115: 4133-4148.
88. Sundstrom BE, Stigbrand TI (1994). Cytokeratins and tissue polypeptide antigen. Int J Biol Markers 9: 102-108.
89. Ueno T, Toi M, Biven K, Bando H, Ogawa T, Linder S (2003). Measurement of an apoptotic product in the sera of breast cancer patients. Eur J Cancer 39: 769-774.
90. Ulukaya E, Yilmaztepe A, Akgoz S, Linder S, Karadag M (2007). The levels of caspase-cleaved cytokeratin 18 are elevated in serum from patients with lung cancer and helpful to predict the survival. Lung Cancer 40: 651-655.
91. Unwin RD, Evans CA, Whetton AD (2006). Relative quantification in proteomics: new approaches for biochemistry. Trends Biochem Sci 31: 473-484.
92. Unwin RD, Pierce A, Watson RB, Sternberg DW, Whetton AD (2005). Quantitative proteomic analysis using isobaric protein tags enables rapid comparison of changes in transcript and protein levels in transformed cells. Mol Cell Proteomics 4: 924-935.
93. van der Merwe DE, Oikonomopoulou K, Marshall J, Diamandis EP (2007). Mass spectrometry: uncovering the cancer proteome for diagnostics. Adv Cancer Res 96: 23-50.
94. Verma M, Srivastava S (2003). New cancer biomarkers deriving from NCI early detection research. Recent Results Cancer Res 163: 72-84; discussion 264-266.
95. Wagner JA (2002). Overview of biomarkers and surrogate endpoints in drug development. Dis Markers 18: 41-46.
96. Wagner JA, Williams SA, Webster CJ (2007). Biomarkers and surrogate end points for fit-for-purpose development and regulatory evaluation of new drugs. Clin Pharmacol Ther 81: 104-107.
97. Weber K, Osborn M, Moll R, Wiklund B, Luning B (1984). Tissue polypeptide antigen (TPA) is related to the non-epidermal keratins 8, 18 and 19 typical of simple and non-squamous epithelia: re-evaluation of a human tumor marker. EMBO J 3: 2707-2714.
98. Westgard JO, Barry PL, Hunt MR, Groth T (1981). A multi-rule Shewhart chart for quality control in clinical chemistry. Clin Chem 27: 493-501.
99. Workman P (2006). Using biomarkers in drug development. Clin Adv Hematol Oncol 4: 736-739.
100. Yagmur E, Trautwein C, Leers MP, Gressner AM, Tacke F (2007). Elevated apoptosis-associated cytokeratin 18 fragments (CK18Asp386) in serum of patients with chronic liver diseases indicate hepatic and biliary inflammation. Clin Biochem.
101. Yamada S, Wirtz D, Coulombe PA (2002). Pairwise assembly determines the intrinsic potential for self organization and mechanical properties of keratin filament. Mol Biol Cell 13: 382-391.
102. Yao X, Afonso C, Fenselau C (2003). Dissection of proteolytic 18O labeling: endoprotease-catalyzed 16O-to-18O exchange of truncated peptide substrates. J Proteome Res 2: 147-152.
103. Zhang X, Wei D, Yap Y, Li L, Guo S, Chen F (2007). Mass spectrometry-based 'omics' technologies in cancer diagnostics. Mass Spectrom Rev 26: 403-431.