Translational physiologically-based pharmacokinetic model for ocular disposition of monoclonal antibodies.

Antibody Eye Human Monkey Ocular Pharmacokinetics Physiologically-Based pharmacokinetic model

Journal

Journal of pharmacokinetics and pharmacodynamics
ISSN: 1573-8744
Titre abrégé: J Pharmacokinet Pharmacodyn
Pays: United States
ID NLM: 101096520

Informations de publication

Date de publication:
09 Aug 2023
Historique:
received: 26 12 2022
accepted: 27 07 2023
medline: 10 8 2023
pubmed: 10 8 2023
entrez: 9 8 2023
Statut: aheadofprint

Résumé

We have previously published a PBPK model comprising the ocular compartment to characterize the disposition of monoclonal antibodies (mAbs) in rabbits. While rabbits are commonly used preclinical species in ocular research, non-human primates (NHPs) have the most phylogenetic resemblance to humans including the presence of macula in the eyes as well as higher sequence homology. However, their use in ocular research is limited due to the strict ethical guidelines. Similarly, in humans the ocular samples cannot be collected except for the tapping of aqueous humor (AH). Therefore, we have translated this rabbit model to monkeys and human species using literature-reported datasets. Parameters describing the tissue volumes, physiological flows, and FcRn-binding were obtained from the literature, or estimated by fitting the model to the data. In the monkey model, the values for the rate of lysosomal degradation for antibodies (K

Identifiants

pubmed: 37558929
doi: 10.1007/s10928-023-09881-9
pii: 10.1007/s10928-023-09881-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIGMS NIH HHS
ID : GM114179
Pays : United States
Organisme : NCI NIH HHS
ID : CA246785
Pays : United States

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Wong WL et al (2014) Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet Glob Health 2(2):e106–e116
pubmed: 25104651 doi: 10.1016/S2214-109X(13)70145-1
Flaxman SR et al (2017) Global causes of blindness and distance vision impairment 1990–2020: a systematic review and meta-analysis. Lancet Glob Health 5(12):e1221–e1234
pubmed: 29032195 doi: 10.1016/S2214-109X(17)30393-5
Mullard A (2021) FDA approves 100th monoclonal antibody product. Nat Rev Drug Discov 20:491–495. https://doi.org/10.1038/d41573-021-00079-7
doi: 10.1038/d41573-021-00079-7 pubmed: 33953368
Kroschinsky F et al (2017) New drugs, new toxicities: severe side effects of modern targeted and immunotherapy of cancer and their management. Critical care (London, England) 21(1):89–89
pubmed: 28407743 doi: 10.1186/s13054-017-1678-1
Perez VL et al (2013) The eye: a window to the soul of the immune system. J Autoimmun 45:7–14
pubmed: 23871641 doi: 10.1016/j.jaut.2013.06.011
Eaton JS et al (2015) Ocular adverse events associated with antibody-drug conjugates in human clinical trials. J Ocul Pharmacol Ther 31(10):589–604
pubmed: 26539624 pmcid: 4677113 doi: 10.1089/jop.2015.0064
Ho WL, Wong H, Yau T (2013) The ophthalmological complications of targeted agents in cancer therapy: what do we need to know as ophthalmologists? Acta Ophthalmol 91(7):604–609
pubmed: 22970709 doi: 10.1111/j.1755-3768.2012.02518.x
Vishnevskia-Dai V et al (2021) Ocular side effects of novel anti-cancer biological therapies. Sci Rep 11(1):787
pubmed: 33436995 pmcid: 7803740 doi: 10.1038/s41598-020-80898-7
Zernii EY et al (2016) Rabbit models of ocular diseases: new relevance for classical approaches. CNS Neurol Disord Drug Targets 15(3):267–291
pubmed: 26553163 doi: 10.2174/1871527315666151110124957
Picaud S et al (2019) The primate model for understanding and restoring vision. Proc Natl Acad Sci 116(52):26280
pubmed: 31871177 pmcid: 6936588 doi: 10.1073/pnas.1902292116
Fernandes A et al (2003) Ocular measurements throughout the adult life span of rhesus monkeys. Invest Ophthalmol Vis Sci 44(6):2373–2380
pubmed: 12766033 doi: 10.1167/iovs.02-0944
Chang B (2013) Mouse models for studies of retinal degeneration and diseases. Methods Mol Biol 935:27–39
pubmed: 23150358 doi: 10.1007/978-1-62703-080-9_2
Hutton-Smith LA et al (2016) A mechanistic model of the intravitreal pharmacokinetics of large molecules and the pharmacodynamic suppression of ocular vascular endothelial growth factor levels by ranibizumab in patients with neovascular age-related macular degeneration. Mol Pharm 13(9):2941–2950
pubmed: 26726925 doi: 10.1021/acs.molpharmaceut.5b00849
Hutton-Smith LA et al (2017) Ocular pharmacokinetics of therapeutic antibodies given by intravitreal injection: estimation of retinal permeabilities using a 3-compartment semi-mechanistic model. Mol Pharm 14(8):2690–2696
pubmed: 28631484 doi: 10.1021/acs.molpharmaceut.7b00164
Park SJ et al (2016) Intraocular pharmacokinetics of intravitreal aflibercept (eylea) in a rabbit model. Invest Ophthalmol Vis Sci 57(6):2612–2617
pubmed: 27258433 doi: 10.1167/iovs.16-19204
Mordenti J et al (1999) Comparisons of the intraocular tissue distribution, pharmacokinetics, and safety of 125I-labeled full-length and Fab antibodies in rhesus monkeys following intravitreal administration. Toxicol Pathol 27(5):536–544
pubmed: 10528633 doi: 10.1177/019262339902700507
Shah DK, Betts AM (2012) Towards a platform PBPK model to characterize the plasma and tissue disposition of monoclonal antibodies in preclinical species and human. J Pharmacokinet Pharmacodyn 39(1):67–86
pubmed: 22143261 doi: 10.1007/s10928-011-9232-2
Bussing D, Dhaval KS (2020) Development of a physiologically-based pharmacokinetic model for ocular disposition of monoclonal antibodies in rabbits. J Pharmacokinet Pharmacodyn 47(6):597–612
pubmed: 32876799 pmcid: 7658046 doi: 10.1007/s10928-020-09713-0
Rohatgi, A., Webplotdigitizer: Version 4.5.
Hinton PR et al (2004) Engineered human IgG antibodies with longer serum half-lives in primates. J Biol Chem 279(8):6213–6216
pubmed: 14699147 doi: 10.1074/jbc.C300470200
Lin YS et al (1999) Preclinical pharmacokinetics, interspecies scaling, and tissue distribution of a humanized monoclonal antibody against vascular endothelial growth factor. J Pharmacol Exp Ther 288(1):371–378
pubmed: 9862791
Miyake T et al (2010) Pharmacokinetics of bevacizumab and its effect on vascular endothelial growth factor after intravitreal injection of bevacizumab in macaque eyes. Invest Ophthalmol Vis Sci 51(3):1606–1608
pubmed: 19875666 doi: 10.1167/iovs.09-4140
Yu DA et al (2018) Preclinical pharmacokinetics of a recombinant humanized rabbit anti-VEGF monoclonal antibody in rabbits and monkeys. Toxicol Lett 292:73–77
pubmed: 29709424 doi: 10.1016/j.toxlet.2018.04.031
Curtin F et al (2016) Serum pharmacokinetics and cerebrospinal fluid concentration analysis of the new IgG4 monoclonal antibody GNbAC1 to treat multiple sclerosis: a phase 1 study. MAbs 8(5):854–860
pubmed: 27030142 pmcid: 4968100 doi: 10.1080/19420862.2016.1168956
Weisman MH et al (2003) Efficacy, pharmacokinetic, and safety assessment of adalimumab, a fully human anti-tumor necrosis factor-alpha monoclonal antibody, in adults with rheumatoid arthritis receiving concomitant methotrexate: a pilot study. Clin Ther 25(6):1700–1721
pubmed: 12860493 doi: 10.1016/S0149-2918(03)80164-9
Markus R et al (2017) A phase I, randomized, single-dose study evaluating the pharmacokinetic equivalence of biosimilar ABP 215 and bevacizumab in healthy adult men. Cancer Chemother Pharmacol 80(4):755–763
pubmed: 28864922 pmcid: 5696486 doi: 10.1007/s00280-017-3416-4
Knight B et al (2016) A phase I pharmacokinetics study comparing PF-06439535 (a potential biosimilar) with bevacizumab in healthy male volunteers. Cancer Chemother Pharmacol 77(4):839–846
pubmed: 26984210 pmcid: 4819942 doi: 10.1007/s00280-016-3001-2
Avery RL et al (2017) Systemic pharmacokinetics and pharmacodynamics of intravitreal aflibercept, bevacizumab and ranibizumab. Retina 37(10):1847–1858
pubmed: 28106709 pmcid: 5642319 doi: 10.1097/IAE.0000000000001493
Krohne TU et al (2008) Intraocular pharmacokinetics of bevacizumab after a single intravitreal injection in humans. Am J Ophthalmol 146(4):508–512
pubmed: 18635152 doi: 10.1016/j.ajo.2008.05.036
Meyer CH, Krohne TU, Holz FG (2011) Intraocular pharmacokinetics after a single intravitreal injection of 1.5 mg versus 3.0 mg of bevacizumab in humans. Retina 31(9):1877–1884
pubmed: 21738089 doi: 10.1097/IAE.0b013e318217373c
Zhu Q et al (2008) Vitreous levels of bevacizumab and vascular endothelial growth factor-A in patients with choroidal neovascularization. Ophthalmology 115(10):1750–1755
pubmed: 18708261 doi: 10.1016/j.ophtha.2008.04.023
D’Argenio DZ, Schumitzky A, Wang X (2009) ADAPT 5 User’s guide: pharmacokinetic/pharmacodynamic systems analysis software. Biomedical Simulations Resource, Los Angeles
Smith DW, Lee CJ, Gardiner BS (2020) No flow through the vitreous humor: How strong is the evidence? Prog Retin Eye Res 78:100845
doi: 10.1016/j.preteyeres.2020.100845
Chang HY et al (2019) A translational platform PBPK model for antibody disposition in the brain. J Pharmacokinet Pharmacodyn 46(4):319–338
pubmed: 31115858 pmcid: 8409011 doi: 10.1007/s10928-019-09641-8
Missel PJ (2012) Simulating intravitreal injections in anatomically accurate models for rabbit, monkey, and human eyes. Pharm Res 29(12):3251–3272
pubmed: 22752935 pmcid: 3497967 doi: 10.1007/s11095-012-0721-9
Short BG (2008) Safety evaluation of ocular drug delivery formulations: techniques and practical considerations. Toxicol Pathol 36(1):49–62
pubmed: 18337221 doi: 10.1177/0192623307310955
Vézina M (2013) Comparative ocular anatomy in commonly used laboratory animals. In: Weir AB, Collins M (eds) Assessing ocular toxicology in laboratory animals. Humana Press, Totowa, NJ, pp 1–21
Rowe-Rendleman CL et al (2014) Drug and gene delivery to the back of the eye: from bench to bedside. Invest Ophthalmol Vis Sci 55(4):2714–2730
pubmed: 24777644 pmcid: 4004426 doi: 10.1167/iovs.13-13707
Cauvin AJ, Peters C, Brennan F (2015) Advantages and limitations of commonly used nonhuman primate species in research and development of biopharmaceuticals. The nonhuman primate in nonclinical drug development and safety assessment. Elsevier, Amsterdam, pp 379–395
doi: 10.1016/B978-0-12-417144-2.00019-6
Augusteyn RC (2010) On the growth and internal structure of the human lens. Exp Eye Res 90(6):643–654
pubmed: 20171212 pmcid: 2871961 doi: 10.1016/j.exer.2010.01.013
Maurice DM, Mishima S (1984) Ocular Pharmacokinetics. In: Sears ML (ed) Pharmacology of the eye. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 19–116
doi: 10.1007/978-3-642-69222-2_2
Lee CJ et al (2006) Determination of human lens capsule permeability and its feasibility as a replacement for Bruch’s membrane. Biomaterials 27(8):1670–1678
pubmed: 16199085 doi: 10.1016/j.biomaterials.2005.09.008
Kastner C et al (2013) Permeability of the anterior lens capsule for large molecules and small drugs. Curr Eye Res 38(10):1057–1063
pubmed: 23885713 doi: 10.3109/02713683.2013.803288
Langner S et al (2010) 7.1.T MRI to assess the anterior segment of the eye. Invest Ophthalmol Vis Sci 51(12):6575–6581
pubmed: 20688731 doi: 10.1167/iovs.09-4865
Pitkänen L et al (2004) Neural retina limits the nonviral gene transfer to retinal pigment epithelium in an in vitro bovine eye model. AAPS J 6(3):e25–e25
pubmed: 15760110 doi: 10.1208/aapsj060325
Ramsay E et al (2019) Role of retinal pigment epithelium permeability in drug transfer between posterior eye segment and systemic blood circulation. Eur J Pharm Biopharm 143:18–23
pubmed: 31419586 doi: 10.1016/j.ejpb.2019.08.008
Ahmed I et al (1989) The kinetics of timolol in the rabbit lens: implications for ocular drug delivery. Pharm Res 6(9):772–778
pubmed: 2813274 doi: 10.1023/A:1015923514012
Himmelstein KJ, Guvenir I, Patton TF (1978) Preliminary pharmacokinetic model of pilocarpine uptake and distribution in the eye. J Pharm Sci 67(5):603–606
pubmed: 641790 doi: 10.1002/jps.2600670507
Merdy M et al (2019) Application of mechanistic ocular absorption modeling and simulation to understand the impact of formulation properties on ophthalmic bioavailability in rabbits: a case study using dexamethasone suspension. AAPS J. https://doi.org/10.1208/s12248-019-0334-x
doi: 10.1208/s12248-019-0334-x pubmed: 31111305
Le Merdy M et al (2020) Ocular physiologically based pharmacokinetic modeling for ointment formulations. Pharm Res 37(12):245
pubmed: 33215336 pmcid: 7677276 doi: 10.1007/s11095-020-02965-y
Lamminsalo M et al (2018) Extended pharmacokinetic model of the rabbit eye for intravitreal and intracameral injections of macromolecules: quantitative analysis of anterior and posterior elimination pathways. Pharm Res 35(8):153
pubmed: 29855726 doi: 10.1007/s11095-018-2435-0
Alm A, Bill A (1973) Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp Eye Res 15(1):15–29
pubmed: 4630581 doi: 10.1016/0014-4835(73)90185-1
Choi K et al (2016) Reference values of hematology, biochemistry, and blood type in cynomolgus monkeys from cambodia origin. Lab Anim Res 32:46
pubmed: 27051442 pmcid: 4816996 doi: 10.5625/lar.2016.32.1.46
Gabelt BT et al (2003) Aqueous humor dynamics and trabecular meshwork and anterior ciliary muscle morphologic changes with age in rhesus monkeys. Invest Ophthalmol Vis Sci 44(5):2118–2125
pubmed: 12714651 doi: 10.1167/iovs.02-0569
Cantrill HL, Pederson JE (1984) Experimental retinal detachment. VI. The permeability of the blood-retinal barrier. Arch Ophthalmol 102(5):747–751
pubmed: 6721768 doi: 10.1001/archopht.1984.01040030595029
Greenbaum S et al (1985) The optically determined corneal and anterior chamber volumes of the cynomolgus monkey. Curr Eye Res 4(3):187–190
pubmed: 4017622 doi: 10.3109/02713688509000849
Prausnitz MR, Noonan JS (1998) Permeability of cornea, sclera, and conjunctiva: a literature analysis for drug delivery to the eye. J Pharm Sci 87(12):1479–1488
pubmed: 10189253 doi: 10.1021/js9802594
Struble C, Howard S, Relph J (2014) Comparison of ocular tissue weights (volumes) and tissue collection techniques in commonly used preclinical animal species. Acta Ophthalmol. https://doi.org/10.1111/j.1755-3768.2014.S005.x
doi: 10.1111/j.1755-3768.2014.S005.x
Sun M et al (2018) Study of retina and choroid biological parameters of rhesus monkeys eyes on scleral collagen cross-linking by riboflavin and ultraviolet A. PLoS ONE 13(2):e0192718–e0192718
pubmed: 29420622 pmcid: 5805357 doi: 10.1371/journal.pone.0192718
Wang Q et al (2016) Vascular density in retina and choriocapillaris as measured by optical coherence tomography angiography. Am J Ophthalmol 168:95–109
pubmed: 27183862 doi: 10.1016/j.ajo.2016.05.005
Ames A, Nesbett FB (1966) Intracellular and extracellular compartments of mammalian central nervous tissue. J Physiol 184(1):215–238
pubmed: 5921539 pmcid: 1357556 doi: 10.1113/jphysiol.1966.sp007912
Wang JC et al (2017) Diabetic choroidopathy: choroidal vascular density and volume in diabetic retinopathy with swept-source optical coherence tomography. Am J Ophthalmol 184:75–83
pubmed: 28988899 doi: 10.1016/j.ajo.2017.09.030
Sonoda S et al (2015) Luminal and stromal areas of choroid determined by binarization method of optical coherence tomographic images. Am J Ophthalmol 159(6):1123-1131.e1
pubmed: 25790737 doi: 10.1016/j.ajo.2015.03.005
Williamson TH, Harris A (1994) Ocular blood flow measurement. Br J Ophthalmol 78(12):939–945
pubmed: 7819179 pmcid: 504997 doi: 10.1136/bjo.78.12.939
Cirillo M et al (1992) Hematocrit, blood pressure, and hypertension. The Gubbio population study. Hypertension 20(3):319–326
pubmed: 1516951 doi: 10.1161/01.HYP.20.3.319
Geyer O et al (2003) Gender and age effects on pulsatile ocular blood flow. Ophthalmic Res 35(5):247–250
pubmed: 12920336 doi: 10.1159/000072144
Wang Y et al (2009) Measurement of total blood flow in the normal human retina using Doppler Fourier-domain optical coherence tomography. Br J Ophthalmol 93(5):634–637
pubmed: 19168468 doi: 10.1136/bjo.2008.150276
Kupfer C, Ross K (1971) Studies of aqueous humor dynamics in man. I. Measurements in young normal subjects. Invest Ophthalmol 10(7):518–522
pubmed: 5091190
Toris CB et al (1999) Aqueous humor dynamics in the aging human eye. Am J Ophthalmol 127(4):407–412
pubmed: 10218693 doi: 10.1016/S0002-9394(98)00436-X
Brubaker RF (1991) Flow of aqueous humor in humans [The Friedenwald Lecture]. Invest Ophthalmol Vis Sci 32(13):3145–3166
pubmed: 1748546
Kwok LS (1984) Calculation and application of the anterior surface area of a model human cornea. J Theor Biol 108(2):295–313
pubmed: 6748693 doi: 10.1016/S0022-5193(84)80072-7
Nagra M et al (2017) Determination of retinal surface area. J Anat 231(3):319–324
pubmed: 28620965 pmcid: 5554828 doi: 10.1111/joa.12641
Wu CD et al (1970) Determination of the wet and dry weight of iris, ciliary body and choroid in man and in different animal species. Ophthalmic Res 1(2):124–128
doi: 10.1159/000264414
Entezari M et al (2018) Choroidal thickness in healthy subjects. J Ophthalmic Vis Res 13(1):39–43
pubmed: 29403588 pmcid: 5782455 doi: 10.4103/jovr.jovr_148_16
Arshinoff SA, Modabber M (2016) Dose and administration of intracameral moxifloxacin for prophylaxis of postoperative endophthalmitis. J Cataract Refract Surg 42(12):1730–1741
pubmed: 28007104 doi: 10.1016/j.jcrs.2016.10.017
Silva AF, Alves MA, Oliveira MSN (2017) Rheological behaviour of vitreous humour. Rheol Acta 56(4):377–386
doi: 10.1007/s00397-017-0997-0
Snydacker D (1956) The relation of the volume of the crystalline lens to the depth of the anterior chamber. Trans Am Ophthalmol Soc 54:675–708
pubmed: 13433793 pmcid: 1312653
El-Malah MA, Abo-Hussein N (2014) Comparative measurement of central corneal thickness using Pentacam, ocular response analyzer, and ultrasound pachymetry devices for normal, glaucomatous, and keratoconic eyes. J Egypt Ophthalmol Soc 107(1):16–19
doi: 10.4103/2090-0686.134936
Feke GT et al (1989) Blood flow in the normal human retina. Invest Ophthalmol Vis Sci 30(1):58–65
pubmed: 2643588

Auteurs

Sanika Naware (S)

Department of Pharmaceutical Sciences, School of Pharmacy and Pharmaceutical Sciences, The State University of New York, University at Buffalo 455 Kapoor Hall, Buffalo, NY, 14214-8033, USA.

David Bussing (D)

Department of Pharmaceutical Sciences, School of Pharmacy and Pharmaceutical Sciences, The State University of New York, University at Buffalo 455 Kapoor Hall, Buffalo, NY, 14214-8033, USA.

Dhaval K Shah (DK)

Department of Pharmaceutical Sciences, School of Pharmacy and Pharmaceutical Sciences, The State University of New York, University at Buffalo 455 Kapoor Hall, Buffalo, NY, 14214-8033, USA. dshah4@buffalo.edu.

Classifications MeSH