journal article·2018-03Open access

Short peptide analogs as alternatives to collagen in pro-regenerative corneal implants

Jaganmohan R. Jangamreddy, Michel K.C. Haagdorens, M. Mirazul Islam, Philip Lewis, Ayan Samanta, Per Fagerholm, Aneta Liszka, Monika K. Ljunggren, Oleksiy Buznyk, Emilio I. Alarcon, Nadia Zakaria, Keith M. Meek, May Griffith

Acta Biomaterialia· Volume 69

Abstract

Short collagen-like peptides (CLPs) are being proposed as alternatives to full-length collagen for use in tissue engineering, on their own as soft hydrogels, or conjugated to synthetic polymer for mechanical strength. However, despite intended clinical use, little is known about their safety and efficacy, mechanism of action or degree of similarity to the full-length counterparts they mimic. Here, we show the functional equivalence of a CLP conjugated to polyethylene glycol (CLP-PEG) to full-length recombinant human collagen in vitro and in promoting stable regeneration of corneal tissue and nerves in a pre-clinical mini-pig model. We also show that these peptide analogs exerted their pro-regeneration effects through stimulating extracellular vesicle production by host cells. Our results support future use of CLP-PEG implants for corneal regeneration, suggesting the feasibility of these or similar peptide analogs in clinical application in the eye and other tissues. STATEMENT OF SIGNIFICANCE: Although biomaterials comprising full-length recombinant human collagen and extracted animal collagen have been evaluated and used clinically, these macromolecules provide only a limited number of functional groups amenable to chemical modification or crosslinking and are demanding to process. Synthetic, customizable analogs that are functionally equivalent, and can be readily scaled-up are therefore very desirable for pre-clinical to clinical translation. Here, we demonstrate, using cornea regeneration as our test bed, that collagen-like-peptides conjugated to multifunctional polyethylene glycol (CLP-PEG) when grafted into mini-pigs as corneal implants were functionally equivalent to recombinant human collagen-based implants that were successfully tested in patients. We also show for the first time that these materials affected regeneration through stimulation of extracellular vesicle production by endogenous host cells that have migrated into the CLP-PEG scaffolds.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Corneal Surgery and Treatments · Collagen: Extraction and Characterization · Ocular Surface and Contact Lens

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (40)

Show source-provided references
1. ECM and ECM-like materials – Biomaterials for applications in regenerative medicine and cancer therapy10.1016/j.addr.2015.11.019 ↗
2. The powerful functions of peptide-based bioactive matrices for regenerative medicine10.1007/s10439-014-1166-6 ↗
3. Self-assembling peptide-based nanostructures for regenerative medicine10.1002/9783527628155.nanotech062 ↗
4. Self-assembled collagen-like-peptide implants as alternatives to human donor corneal transplantation10.1039/C6RA08895C ↗
5. Global survey of corneal transplantation and eye banking10.1001/jamaophthalmol.2015.4776 ↗
6. Anti-inflammatory and protective effects of 2-methacryloyloxyethyl phosphorylcholine polymer on oral epithelial cells10.1002/jbm.a.35201 ↗
7. A biosynthetic alternative to human donor tissue for inducing corneal regeneration: 24-month follow-up of a phase 1 clinical study10.1126/scitranslmed.3001022 ↗
8. Stable corneal regeneration four years after implantation of a cell-free recombinant human collagen scaffold10.1016/j.biomaterials.2013.11.079 ↗
9. Bioengineered corneas grafted as alternatives to human donor corneas in three high-risk patients10.1111/cts.12293 ↗
10. Reactions to a bovine collagen implant. Clinical and immunologic study in 705 patients10.1016/S0190-9622(89)70330-3 ↗
11. Collagen: animal sources and biomedical application10.7324/JAPS.2015.50322 ↗
12. Safety and efficacy of composite collagen-silver nanoparticle hydrogels as tissue engineering scaffolds10.1039/C5NR03826J ↗
13. A stromal cell-derived factor-1 releasing matrix enhances the progenitor cell response and blood vessel growth in ischaemic skeletal muscle10.22203/eCM.v022a09 ↗
14. Tissue-engineered injectable collagen-based matrices for improved cell delivery and vascularization of ischemic tissue using CD133+ progenitors expanded from the peripheral blood
15. Functional fabrication of recombinant human collagen-phosphorylcholine hydrogels for regenerative medicine applications10.1016/j.actbio.2014.10.035 ↗
16. Tissue-engineered recombinant human collagen-based corneal substitutes for implantation: performance of type I versus type III collagen10.1167/iovs.07-1348 ↗
17. Infrared spectroscopy of collagen and collagen-like polypeptides10.1002/bip.1975.360140505 ↗
18. Assessing the cytotoxic and mutagenic effects of secondary metabolites produced by several fungal biological control agents with the Ames assay and the VITOTOX((R)) test10.1016/j.mrgentox.2011.01.004 ↗
19. An SV40-immortalized human corneal epithelial cell line and its characterization
20. A quantitative rabbit model of vaccinia keratitis10.1167/iovs.09-5106 ↗
21. Light transmission in the human cornea as a function of position across the ocular surface: theoretical and experimental aspects10.1529/biophysj.108.132316 ↗
22. Refractive index of the human corneal epithelium and stroma10.3928/1081-597X-19950301-09 ↗
23. A comparison of biomechanical properties between human and porcine cornea10.1016/S0021-9290(00)00219-0 ↗
24. FTIR studies of collagen model peptides: complementary experimental and simulation approaches to conformation and unfolding10.1021/ja071154i ↗
25. Evaluation of cytotoxicity and genotoxicity of some Philippine medicinal plants10.4103/0973-1296.80683 ↗
26. Distribution of types I, II, III, IV and V collagen in normal and keratoconus corneas10.1159/000265406 ↗
27. Type V collagen and Bowman's membrane. Quantitation of mRNA in corneal epithelium and stroma10.1016/S0021-9258(17)31483-7 ↗
28. Exosomes: composition, biogenesis and function10.1038/nri855 ↗
29. Multi-hierarchical self-assembly of a collagen mimetic peptide from triple helix to nanofibre and hydrogel10.1038/nchem.1123 ↗
30. Rapid characterization of peptide secondary structure by FT-IR spectroscopy
31. In-vitro degradation test for screening of biomaterials
32. Bandyopadhyay · 2013
33. Biosynthetic corneal implants for replacement of pathologic corneal tissue: performance in a controlled rabbit alkali burn model10.1167/iovs.10-5224 ↗
34. Advances in the design and higher-order assembly of collagen mimetic peptides for regenerative medicine10.1016/j.copbio.2016.10.013 ↗
35. Role of epithelial hyperplasia in regression following photorefractive keratectomy10.1136/bjo.80.6.545 ↗
36. Factors affecting epithelial hyperplasia after photorefractive keratectomy10.1016/S0886-3350(97)80078-8 ↗
37. Effect of surgical technique on corneal implant performance10.1167/tvst.3.2.6 ↗
38. Secretion of collagen by corneal epithelium. I. morphology of the collagenous products produced by isolated epithelia grown on frozen-killed lens10.1083/jcb.57.1.190 ↗
39. Secretion of collagen types I and II by epithelial and endothelial cells in the developing chick cornea demonstrated by in situ hybridization and immunohistochemistry10.1242/dev.103.1.27 ↗
40. Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction10.1161/CIRCRESAHA.117.305990 ↗