Predicting the F(ab)-mediated effect of monoclonal antibodies in vivo by combining cell-level kinetic and pharmacokinetic modelling

Journal of Pharmacokinetics and Pharmacodynamics

Volumn 39, Issue 2, 2012, Pages 125-139

  Krippendorff, Ben Fillippo ^a   Oyarzún, Diego A ^b   Huisinga, Wilhelm ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF POTSDAM   (Germany)

Author keywords

Cell level kinetics; EGFR; Pharmacokinetic models; Therapeutic proteins

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN F(AB')2 FRAGMENT; ZALUTUMUMAB;

ANTIBODY AFFINITY; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CELL LEVEL; COMPARTMENT MODEL; CONCENTRATION RESPONSE; DRUG RECEPTOR BINDING; IN VITRO STUDY; IN VIVO STUDY; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; PREDICTION; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN TARGETING; SYSTEMS BIOLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL LINE, TUMOR; CELL MEMBRANE; FORECASTING; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; MACACA FASCICULARIS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 84861481519     PISSN: 1567567X     EISSN: 15738744     Source Type: Journal    
DOI: 10.1007/s10928-012-9243-7     Document Type: Article

References (61)

1. Meibohm B (2007) The role of pharmacokinetics and pharmacodynamics in the development of biotech drugs. In: Meibohm B (ed) Pharmacokinetics and pharmacodynamics of biotech drugs: principles and case studies in drug development. Wiley-VCH, Weinheim
2. Dirks NL, Nolting A, Kovar A, Meibohm B (2008) Population pharmacokinetics of cetuximab in patients with squamous cell carcinoma of the head and neck. J Clin Pharmacol 48:267-78 (Pubitemid 351257778)
3. Kuester K, Kovar A, Lüpfert C, Brockhaus B, Kloft C (2008) Population pharmacokinetic data analysis of three phase I studies of matuzumab, a humanised anti-EGFR monoclonal antibody in clinical cancer development. Br J Cancer 98:9006
4. Mould DR, Sweeney KRD (2007) The pharmacokinetics and pharmacodynamics of monoclonal antibodies-mechanistic modeling applied to drug development.Curr Opin Drug Discov Devel 10:84-96 (Pubitemid 46438261)
5. Kloft C, Graefe EU, Tanswell P, Scott AM, Hofheinz R, Amelsberg A, Karlsson MO (2004) Population pharmacokinetics of sibrotuzumab, a novel therapeutic monoclonal antibody, in cancer patients. Invest New Drugs 22:3952
6. Lammerts van Bueren JJ, Bleeker WK, Bøgh HO, Houtkamp M, Schuurman J, van de Winkel JGJ, Parren PWHI (2006) Effect of target dynamics on pharmacokinetics of a novel therapeutic antibody against the epidermal growth factor receptor: implications for the mechanisms of action. Cancer Res 66:7630-8 (Pubitemid 44289220)
7. Mager DE, Jusko WJ (2001) General pharmacokinetic model for drugs exhibiting target-mediated drug disposition. J Pharmacokinet Pharmacodyn 28:507-32 (Pubitemid 34289541)
8. Gibiansky L, Gibiansky E, Kakkar T, Ma P (2008) Approximations of the target-mediated drug disposition model and identifiability of model parameters. J Pharmacokinet Pharmacodyn 35: 573-591
9. Gibiansky L, Gibiansky E (2009) Target-mediated drug disposition model: relationships with indirect response models and application to population PK-PD analysis. J Pharmacokinet Pharmacodyn 36:341-351
10. Hood L, Perlmutter RM (2004) The impact of systems approaches on biological problems in drug discovery. Nat Biotechnol 22:1215-7 (Pubitemid 39336768)
11. Kitano H (2007) A robustness-based approach to systems-oriented drug design. Nat Rev Drug Discov 6:202-10
12. Kreeger PK, Lauffenburger DA (2010) Cancer systems biology: a network modeling perspective. Carcinogenesis 31:2-8
13. Chen WW, Schoeberl B, Jasper PJ, Niepel M, Nielsen UB, Lauffenburger DA, Sorger PK (2009) Input-output behavior of ErbB signaling pathways as revealed by a mass action model trained against dynamic data. Mol Syst Biol 5:239
14. Schoeberl B, Pace EA, Fitzgerald JB, Harms BD, Xu L, Nie L, Linggi B, Kalra A, Paragas V, Bukhalid R, Grantcharova V, Kohli N, West KA, Leszczyniecka M, Feldhaus MJ, Kudla AJ, Nielsen UB (2009) Therapeutically targeting ErbB3: a key node in ligand-induced activation of the ErbB receptor-PI3K axis. Sci Signal 2:ra31
15. van der Graaf PH, Benson N (2011) Systems pharmacology: bridging systems biology and pharmacokinetics-pharmacodynamics (PKPD) in drug discovery and development. Pharm res 28:1460-1464
16. Jakobovits A, Amado R, Yang X, Roskos L, Schwab G (2007) From XenoMouse technology to panitumumab, the first fully human antibody product from transgenic mice. Nat Biotechnol 25:1134-1143 (Pubitemid 47542248)
17. Mendelsohn J (2003) Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 21:2787-2799
18. Fujita KA, Toyoshima Y, Uda S, Ozaki YI, Kubota H, Kuroda S (2010) Decoupling of receptor and downstream signals in the Akt pathway by Its low-pass filter characteristics. Sci Signal 3:ra56
19. Shankaran H, Resat H, Wiley HS (2007) Cell surface receptors for signal transduction and ligand transport: a design principles study. PLoS Comput Biol 3:e101
20. Starbuck C, Lauffenburger DA (1992) Mathematical model for the effects of epidermal growth factor receptor trafficking dynamics on fibroblast proliferation responses. Biotechnol Prog 8:132-43
21. Shankaran H, Wiley HS, Resat H (2007) Receptor downregulation and desensitization enhance the information processing ability of signalling receptors. BMC Syst Biol 1:48
22. Hendriks BS, Orr G, Wells A, Wiley HS, LauffenburgerDA(2005) Parsing ERK activation reveals quantitatively equivalent contributions from epidermal growth factor receptor and HER2 in human mammary epithelial cells. J Biol Chem 280:6157-6169 (Pubitemid 40280101)
23. Hendriks BS, Opresko LK, Wiley HS, Lauffenburger DA (2003) Quantitative analysis of HER2-mediated effects on HER2 and epidermal growth factor receptor endocytosis: distribution of homo- and heterodimers depends on relative HER2 levels. J Biol Chem 278:23343-23351 (Pubitemid 36830149)
24. Hendriks BS, Opresko LK, Wiley HS, Lauffenburger DA (2003) Coregulation of epidermal growth factor receptor/human epidermal growth factor receptor 2 (HER2) levels and locations: quantitative analysis of HER2 overexpression effects. Cancer res 63:1130-1137 (Pubitemid 36278448)
25. Bleeker WK, Lammertsvan Bueren JJ, van Ojik HH, Gerritsen AF, Pluyter M, Houtkamp M, Halk E, Goldstein J, Schuurman J, van Dijk MA, van de Winkel JGJ, Parren PWHI (2004) Dual mode of action of a human anti-epidermal growth factor receptor monoclonal antibody for cancer therapy. J Immunol 173:4699-707 (Pubitemid 39280705)
26. Bastholt L, Specht L, Jensen K, Brun E, Loft A, Petersen J, Kastberg H, Eriksen JG (2007) Phase I/II clinical and pharmacokinetic study evaluating a fully human monoclonal antibody against EGFr (HuMax-EGFr) in patients with advanced squamous cell carcinoma of the head and neck. Radiother Oncol 85:24-8 (Pubitemid 47562580)
27. Tang L, Persky A, Hochhaus G, Meibohm B (2004) Pharmacokinetic aspects of biotechnology products. J Pharm Sci 93: 2184-2204 (Pubitemid 39129617)
28. Krippendorff BF, Kuester K, Kloft C, Huisinga W (2009) Nonlinear pharmacokinetics of therapeutic proteins resulting from receptor mediated endocytosis. J Pharmacokinet Pharmacodyn 36:239-60
29. Knauer DJ, Wiley HS, Cunningham DD (1984) Relationship between epidermal growth factor receptor occupancy and mitogenic response. Quantitative analysis using a steady state model system. J Biol Chem 259:5623-31 (Pubitemid 14145024)
30. Brzeziński J, Lewiński A (1998) Increased plasma concentration of epidermal growth factor in female patients with non-toxic nodular goitre. Eur J Endocrinol 138:388-93
31. Masui H, Castro L, Mendelsohn J (1993) Consumption of EGF by A431 cells: evidence for receptor recycling. J Cell Biol 120:85-93 (Pubitemid 23014069)
32. Lin C, Chen W, Kruiger W, Stolarsky L, Weber W, Evans R, Verma I, Gill G, Rosenfeld M (1984) Expression cloning of human EGF receptor complementary DNA: gene amplification and three related messenger RNA products in A431 cells. Sci Agric 224:843-8 (Pubitemid 14102458)
33. Ullrich A, Ullrich A, Coussens L, Coussens L, Hayflick JS, Hayflick JS, Dull TJ, Dull TJ, Gray A, Gray A, Tam AW, Tam AW, Lee J, Lee J, Yarden Y, Yarden Y, Libermann TA, Libermann TA, Schlessinger J, Schlessinger J et al (1984) Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309:418-425 (Pubitemid 14102443)
34. Reddy CC, Wells A, Lauffenburger DA (1994) Proliferative response of fibroblasts expressing internalization-deficient epidermal growth factor (EGF) receptors is altered via differential EGF depletion effect. Biotechnol Prog 10:377-84 (Pubitemid 2129380)
35. Peipp M, Dechant M, Valerius T (2008) Effector mechanisms of therapeutic antibodies against ErbB receptors. Curr Opin Immunol 20:436-43
36. Morell A, Terry W, Waldmann T (1970) Metabolic properties of IgG subclasses in man. J Clin Invest 49:673-680
37. Yang X, Jia X, Corvalan J, Wang P, Davis C (2001) Development of ABX-EGF, a fully human anti-EGF receptor monoclonal antibody, for cancer therapy. Crit Rev Oncol Hematol 38:17-23 (Pubitemid 32194591)
38. Sargent ER, Gomella LG, Belldegrun A, Linehan WM, Kasid A (1989) Epidermal growth factor receptor gene expression in normal human kidney and renal cell carcinoma. J Urol 142: 1364-8 (Pubitemid 19277993)
39. Ogiso Y, Oikawa T, Kondo N, Kuzumaki N, Sugihara T, Ohura T (1988) Expression of proto-oncogenes in normal and tumor tissues of human skin. J Invest Dermatol 90:841-4
40. Sakai K, Mori S, Kawamoto T, Taniguchi S, Kobori O, Morioka Y, Kuroki T, Kano K (1986) Expression of epidermal growth factor receptors on normal human gastric epithelia and gastric carcinomas. J Natl Cancer Inst 77:1047-52 (Pubitemid 17184126)
41. van der Laan BF, Freeman JL, Asa SL (1995) Expression of growth factors and growth factor receptors in normal and tumorous human thyroid tissues. Thyroid 5:67-73
42. Henzen-Logmans SC, van der Burg ME, Foekens JA, Berns PM, Brussée R, Fieret JH, Klijn JG, Chadha S, Rodenburg CJ (1992) Occurrence of epidermal growth factor receptors in benign and malignant ovarian tumors and normal ovarian tissues: an immunohistochemical study. J Cancer Res Clin Oncol 118:303-307
43. Terada T, Ohta T, Nakanuma Y (1994) Expression of transforming growth factor-alpha and its receptor during human liver development and maturation. Virchows Archiv Int J Pathol 424:669-675 (Pubitemid 24245340)
44. Mendelsohn J (2002) Targeting the epidermal growth factor receptor for cancer therapy. J Clin Oncol 20:1S-13S
45. Grandis JR, Melhem MF, Gooding WE, Day R, Holst VA, Wagener MM, Drenning SD, Tweardy DJ (1998) Levels of TGFalpha and EGFR protein in head and neck squamous cell carcinoma and patient survival. J Natl Cancer Inst 90:824-32 (Pubitemid 28280548)
46. Merlino G, Xu Y, Ishii S, Clark A, Semba K, Toyoshima K, Yamamoto T, Pastan I (1984) Amplification and enhanced expression of the epidermal growth factor receptor gene in A431 human carcinoma cells. Science 224:417
47. Rao BM, Lauffenburger DA, Wittrup KD (2005) Integrating celllevel kinetic modeling into the design of engineered protein therapeutics. Nat Biotechnol 23:191-4 (Pubitemid 40255328)
48. Crombet T, Osorio M, Cruz T, Roca C, del Castillo R, Mon R, Iznaga-Escobar N, Figueredo R, Koropatnick J, Renginfo E, Fernández E, Alvárez D, Torres O, Ramos M, Leonard I, Pérez R, Lage A (2004) Use of the humanized anti-epidermal growth factor receptor monoclonal antibody h-R3 in combination with radiotherapy in the treatment of locally advanced head and neck cancer patients. J Clin Oncol 22:1646-54 (Pubitemid 41079803)
49. Carter P (2001) Improving the efficacy of antibody-based cancer therapies. Nat Rev Cancer 1:118-129
50. Messersmith W, Hidalgo M (2007) Panitumumab, a monoclonal anti epidermal growth factor receptor antibody in colorectal cancer: Another one or the one?. Clin Cancer Res 13:4664
51. Talavera A, Friemann R, Gómez-Puerta S, Martinez-Fleites C, Garrido G, Rabasa A, López-Requena A, Pupo A, Johansen RF, Sánchez O, Krengel U, Moreno E (2009) Nimotuzumab, an antitumor antibody that targets the epidermal growth factor receptor, blocks ligand binding while permitting the active receptor conformation. Cancer res 69:5851-5859
52. Lacouture ME (2006) Mechanisms of cutaneous toxicities to EGFR inhibitors. Nat Rev Cancer 6:803-12
53. Peréz-Soler R, Saltz L (2005) Cutaneous adverse effects with HER1/EGFR-targeted agents: is there a silver lining?. J Clin Oncol 23:5235-46 (Pubitemid 46224035)
54. Agoram B (2007) Use of pharmacokinetic/pharmacodynamic modelling for starting dose selection in first-in-human trials of high-risk biologics. Br J Clin Pharmacol 67:53-160
55. Thurber GM, Schmidt MM, Wittrup KD (2008) Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance. Adv Drug Deliv Rev 60:1421-1434
56. Thurber G, Schmidt M, Wittrup KD (2008) Factors determining antibody distribution in tumors. Trends Pharm Sci 29:57-61
57. Urva S, Yang V, Balthasar J (2009) Physiologically based pharmacokinetic model for T84.66: a monoclonal anti-CEA antibody. J Pharm Sci :1-19
58. Davda JP, Jain M, Batra SK, Gwilt PR, Robinson DH (2008) A physiologically based pharmacokinetic (PBPK) model to characterize and predict the disposition of monoclonal antibody CC49 and its single chain Fv constructs. Int Immunopharmacol 8:401-13 (Pubitemid 351221431)
59. Schoeberl B, Eichler-Jonsson C, Gilles ED, Mueller G (2002) Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors. Nat Biotechnol 20:370-5 (Pubitemid 34286330)
60. Borisov N, Aksamitiene E, Kiyatkin A, Legewie S, Berkhout J, Maiwald T, Kaimachnikov NP, Timmer J, Hoek JB, Kholodenko BN (2009) Systems-level interactions between insulin-EGF networks amplify mitogenic signaling. Mol Syst Biol 5:256
61. Kholodenko BN (2006) Cell-signalling dynamics in time and space. Natl Rev Mol Cell Biol 7:165-76