Affinity-controlled release of rod-derived cone viability factor enhances cone photoreceptor survival
Source abstract
Abstract
Retinitis pigmentosa (RP) is a group of genetic diseases that results in rod photoreceptor cell degeneration, which subsequently leads to cone photoreceptor cell death, impaired vision and eventual blindness. Rod-derived cone viability factor (RdCVF) is a protein which has two isoforms: a short form (RdCVF) and a long form (RdCVFL) which act on cone photoreceptors in the retina. RdCVFL protects photoreceptors by reducing hyperoxia in the retina; however, sustained delivery of RdCVFL remains challenging. We developed an affinity-controlled release strategy for RdCVFL. An injectable physical blend of hyaluronan and methylcellulose (HAMC) was covalently modified with a peptide binding partner of the Src homology 3 (SH3) domain. This domain was expressed as a fusion protein with RdCVFL, thereby enabling its controlled release from HAMC-binding peptide. Sustained release of RdCVFL was demonstrated for the first time as RdCVFL-SH3 from HAMC-binding peptide for 7 d in vitro. To assess bioactivity, chick retinal dissociates were harvested and treated with the affinity-released recombinant protein from the HAMC-binding peptide vehicle. After 6 d in culture, cone cell viability was greater when cultured with released RdCVFL-SH3 relative to controls. We utilized computational fluid dynamics to model release of RdCVFL-SH3 from our delivery vehicle in the vitreous of the human eye. We demonstrate that our delivery vehicle can prolong the bioavailability of RdCVFL-SH3 in the retina, potentially enhancing its therapeutic effects. Our affinity-based system constitutes a versatile delivery platform for ultimate intraocular injection in the treatment of retinal degenerative diseases. STATEMENT OF SIGNIFICANCE: Retinitis pigmentosa (RP) is the leading cause of inherited blindness in the world. Rod-derived cone viability factor (RdCVF), a novel protein paracrine factor, is effective in preclinical models of RP. To extend its therapeutic effects, we developed an affinity-controlled release strategy for the long form of RdCVF, RdCVFL. We expressed RdCVFL as a fusion protein with an Src homology 3 domain (SH3). We then utilized a hydrogel composed of hyaluronan and methylcellulose (HAMC) and modified it with SH3 binding peptides to investigate its release in vitro. Furthermore, we designed a mathematical model of the human eye to investigate delivery of the protein from the delivery vehicle. This work paves the way for future investigation of controlled release RdCVF.
Source: europepmc · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Retinal Development and Disorders · Photoreceptor and optogenetics research · Connexins and lens biology
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (95)
Show source-provided references
1. Review and update: current treatment trends for patients with retinitis pigmentosa10.1016/j.optm.2008.01.026 ↗
2. Mutations in C2ORF71 cause autosomal-recessive retinitis pigmentosa10.1016/j.ajhg.2010.03.016 ↗
3. Investigating retinitis pigmentosa: a laboratory scientist's perspective10.1016/S1350-9462(96)00032-8 ↗
4. Retinitis pigmentosa10.1016/S0140-6736(06)69740-7 ↗
5. Cone-enriched cultures from the retina of chicken embryos to study rod to cone cellular interactions10.3791/61998 ↗
6. Structure of cone photoreceptors10.1016/j.preteyeres.2009.05.003 ↗
7. Normal retina releases a diffusible factor stimulating cone survival in the retinal degeneration mouse10.1073/pnas.95.14.8357 ↗
8. Identification and characterization of rod-derived cone viability factor10.1038/ng1386 ↗
9. Thioredoxin rod-derived cone viability factor protects against photooxidative retinal damage10.1016/j.freeradbiomed.2015.01.003 ↗
10. Viral-mediated RdCVF and RdCVFL expression protects cone and rod photoreceptors in retinal degeneration10.1172/JCI65654 ↗
11. The thioredoxin encoded by the rod-derived cone viability factor gene protects cone photoreceptors against oxidative stress10.1089/ars.2015.6509 ↗
12. Innate and adaptive immunity of the eye10.1016/S1569-2590(05)10011-1 ↗
13. Delivery strategies for treatment of age-related ocular diseases: from a biological understanding to biomaterial solutions10.1016/j.jconrel.2015.09.065 ↗
14. Ocular drug delivery10.1208/s12248-010-9183-3 ↗
15. Functional cone rescue by RdCVF protein in a dominant model of retinitis pigmentosa10.1038/mt.2009.28 ↗
16. Anti-vascular endothelial growth factor therapy for diabetic macular edema10.1177/2042018813512360 ↗
17. Mini drug pump for ophthalmic use
18. Intravitreal injection of ozurdex® implant in patients with persistent diabetic macular edema, with six-month follow-up10.4137/OED.S38028 ↗
19. Long-term follow-up of patients with retinitis pigmentosa receiving intraocular ciliary neurotrophic factor implants10.1016/j.ajo.2016.07.013 ↗
20. Nanoparticles in porous microparticles prepared by supercritical infusion and pressure quench technology for sustained delivery of bevacizumab10.1021/mp400487f ↗
21. Suprachoroidal drug delivery to the back of the eye using hollow microneedles10.1007/s11095-010-0271-y ↗
22. Subconjunctival nano- and microparticles sustain retinal delivery of budesonide, a corticosteroid capable of inhibiting VEGF expression10.1167/iovs.02-0791 ↗
23. Drug delivery methods for posterior segment disease10.1097/ICU.0b013e3281108000 ↗
24. Tunable growth factor delivery from injectable hydrogels for tissue engineering10.1021/ja210638x ↗
25. Designer protein delivery: from natural to engineered affinity-controlled release systems10.1126/science.aac4750 ↗
26. Fast-gelling injectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord10.1016/j.biomaterials.2005.11.015 ↗
27. Intrathecal delivery of a polymeric nanocomposite hydrogel after spinal cord injury10.1016/j.biomaterials.2010.07.004 ↗
28. Hydrogel-mediated co-transplantation of retinal pigmented epithelium and photoreceptors restores vision in an animal model of advanced retinal degeneration10.1016/j.biomaterials.2020.120233 ↗
29. A hydrogel-based stem cell delivery system to treat retinal degenerative diseases10.1016/j.biomaterials.2009.12.004 ↗
30. A hyaluronan-based injectable hydrogel improves the survival and integration of stem cell progeny following transplantation10.1016/j.stemcr.2015.04.008 ↗
31. The pros and cons of vertebrate animal models for functional and therapeutic research on inherited retinal dystrophies10.1016/j.preteyeres.2015.04.004 ↗
32. Photoreceptor organisation and phenotypic characterization in retinas of two diurnal rodent species: potential use as experimental animal models for human vision research10.1016/j.visres.2007.08.011 ↗
33. Specific binding of peanut lectin to a class of retinal photoreceptor cells. A species comparison
34. Circadian regulation of cGMP-gated cationic channels of chick retinal cones: Erk MAP Kinase and Ca2+/calmodulin-dependent protein kinase II10.1016/S0896-6273(01)00195-7 ↗
35. In vitro and computational modelling of drug delivery across the outer blood–retinal barrier10.1098/rsfs.2019.0132 ↗
36. Intravitreal vancomycin: retinal toxicity, clearance, and interaction with gentamicin10.1001/archopht.1987.01060060117045 ↗
37. Computational fluid dynamics with imaging of cleared tissue and of in vivo perfusion predicts drug uptake and treatment responses in tumours10.1038/s41551-018-0306-y ↗
38. Prediction of ocular drug distribution from systemic blood circulation10.1021/acs.molpharmaceut.5b00729 ↗
39. Mathematical model accurately predicts protein release from an affinity-based delivery system10.1016/j.jconrel.2014.10.032 ↗
40. Affinity-based release of chondroitinase ABC from a modified methylcellulose hydrogel10.1016/j.jconrel.2013.06.029 ↗
41. Hydrogel for simultaneous tunable growth factor delivery and enhanced viability of encapsulated cells in vitro10.1021/acs.biomac.5b01366 ↗
42. Rod-derived cone viability factor promotes cone survival by stimulating aerobic glycolysis10.1016/j.cell.2015.03.023 ↗
43. Change in human lens dimensions, lens refractive index distribution and ciliary body ring diameter with accommodation10.1364/BOE.9.001272 ↗
44. Variations in eyeball diameters of the healthy adults10.1155/2014/503645 ↗
45. Retinal thickness measured by spectral domain optical coherence tomography in eyes without retinal abnormalities: the beaver dam eye study10.1016/j.ajo.2014.11.025 ↗
46. Computer modeling of drug delivery to the posterior eye: effect of active transport and loss to choroidal blood flow10.1007/s11095-008-9691-3 ↗
47. Computational modeling of drug delivery to the posterior eye10.1016/j.ces.2014.01.005 ↗
48. Diurnal variation of episcleral venous pressure in healthy patients: a pilot study10.1097/00061198-200102000-00005 ↗
49. Computer simulation of convective and diffusive transport of controlled-release drugs in the vitreous humor10.1023/A:1022207026982 ↗
50. Modeling the effects of disease, drug properties, and material on drug transport from intraocular lenses10.1167/tvst.11.5.14 ↗
51. Common errors in mass spectrometry-based analysis of post-translational modifications10.1002/pmic.201500355 ↗
52. Large-scale analysis of post-translational modifications in E. coli under glucose-limiting conditions10.1186/s12864-017-3676-8 ↗
53. An equation to estimate the difference between theoretically predicted and SDS PAGE-displayed molecular weights for an acidic peptide10.1038/srep13370 ↗
54. Controlled release strategy designed for intravitreal protein delivery to the retina10.1016/j.jconrel.2018.11.012 ↗
55. T m -Values and unfolded fraction can predict aggregation rates for granulocyte colony stimulating factor variant formulations but not under predominantly native conditions10.1021/acs.molpharmaceut.7b00876 ↗
56. Mechanisms of solute release from porous hydrophilic polymers10.1016/0378-5173(83)90064-9 ↗
57. A simple equation for description of solute release I. Fickian and non-fickian release from non-swellable devices in the form of slabs, spheres, cylinders or discs10.1016/0168-3659(87)90034-4 ↗
58. Reengineering biocatalysts: computational redesign of chondroitinase ABC improves efficacy and stability10.1126/sciadv.abc6378 ↗
59. Heparin microparticle effects on presentation and bioactivity of bone morphogenetic protein-210.1016/j.biomaterials.2014.05.011 ↗
60. Hydrolysis and sulfation pattern effects on release of bioactive bone morphogenetic protein-2 from heparin-based microparticles10.1039/C5TB00933B ↗
61. The effect of sulfation of alginate hydrogels on the specific binding and controlled release of heparin-binding proteins10.1016/j.biomaterials.2008.04.025 ↗
62. Gabapentin attenuates oxidative stress and apoptosis in the diabetic rat retina10.1007/s12640-019-00018-w ↗
63. Is there excess oxidative stress and damage in eyes of patients with retinitis pigmentosa?10.1089/ars.2015.6327 ↗
64. Neurodegenerative influence of oxidative stress in the retina of a murine model of diabetes10.1007/s00125-009-1655-6 ↗
65. Intraretinal oxygen distribution in rats as a function of systemic blood pressure10.1152/ajpheart.1994.267.6.H2498 ↗
66. Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease10.1016/S1350-9462(00)00027-6 ↗
67. Trophic factor expression, retinal oxygen status, and photoreceptor function in the P23H Rat10.1167/iovs.03-0845 ↗
68. The Thioredoxin-like protein rod-derived cone viability factor (RdCVFL) interacts with TAU and inhibits its phosphorylation in the retina*10.1074/mcp.M800406-MCP200 ↗
69. Redox control of resistance to cis-diamminedichloroplatinum (II) (CDDP): protective effect of human thioredoxin against CDDP-induced cytotoxicity10.1172/JCI118668 ↗
70. Adult T cell leukemia-derived factor/human thioredoxin protects endothelial F-2 cell injury caused by activated neutrophils or hydrogen peroxide10.1016/0165-2478(94)90038-8 ↗
71. Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene10.1006/dbio.1996.0208 ↗
72. Gene therapy for neurological disorders: progress and prospects10.1038/nrd.2018.110 ↗
73. Antigen-selective modulation of AAV immunogenicity with tolerogenic rapamycin nanoparticles enables successful vector re-administration10.1038/s41467-018-06621-3 ↗
74. AAV immunogenicity: a matter of sensitivity10.1016/j.ymthe.2018.09.001 ↗
75. Short-lived recombinant adeno-associated virus transgene expression in dystrophic muscle is associated with oxidative damage to transgene mRNA10.1038/mtm.2015.10 ↗
76. Affinity selection of FGF2-binding heparan sulfates for ex vivo expansion of human mesenchymal stem cells10.1002/jcp.25454 ↗
77. Characterization, stability, and in vivo efficacy studies of recombinant human CNTF and its permeation into the neural retina in ex vivo organotypic retinal explant culture models10.3390/pharmaceutics12070611 ↗
78. Increasing the homogeneity, stability and activity of human serum albumin and interferon-α2b fusion protein by linker engineering10.1016/j.pep.2008.04.013 ↗
79. Recombinant granulocyte colony-stimulating factor-transferrin fusion protein as an oral myelopoietic agent10.1073/pnas.0500062102 ↗
80. Plasticity and differentiation of embryonic retinal cells after terminal mitosis10.1126/science.2911751 ↗
81. Differentiation of retinal precursor cells born in vitro10.1016/0012-1606(92)90109-T ↗
82. Subsets of retinal progenitors display temporally regulated and distinct biases in the fates of their progeny10.1242/dev.124.6.1119 ↗
83. CRB2 in immature photoreceptors determines the superior-inferior symmetry of the developing retina to maintain retinal structure and function10.1093/hmg/ddy194 ↗
84. Analysis of retinal cell development in chick embryo by immunohistochemistry and in ovo electroporation techniques10.1186/1471-213X-10-8 ↗
85. Development of the pattern of photoreceptors in the chick retina10.1523/JNEUROSCI.16-04-01430.1996 ↗
86. Bone morphogenetic protein 7 increases chick photoreceptor outer segment initiation10.1167/iovs.06-0079 ↗
87. Insulin and fibroblast growth factor 2 activate a neurogenic program in müller glia of the chicken retina10.1523/JNEUROSCI.22-21-09387.2002 ↗
88. Is monthly retreatment with intravitreal bevacizumab (Avastin®) necessary in neovascular age-related macular degeneration?10.2147/OPTH.S8598 ↗
89. Biocompatible reverse thermal gel sustains the release of intravitreal bevacizumab in vivo10.1167/iovs.13-13120 ↗
90. Injectable chemically crosslinked hydrogel for the controlled release of bevacizumab in vitreous: A 6-month in vivo study10.1167/tvst.4.2.5 ↗
91. Highlights of prescribing information
92. Finite element modeling of drug distribution in the vitreous humor of the rabbit eye10.1007/BF02648045 ↗
93. Intravitreal injection technique
94. The short-needle intravitreal injection technique
95. Ranibizumab for neovascular age-related macular degeneration10.1056/NEJMoa054481 ↗