Tailoring the biofunctionality of collagen biomaterials via tropoelastin incorporation and EDC-crosslinking
Source abstract
Abstract
Recreating the cell niche of virtually all tissues requires composite materials fabricated from multiple extracellular matrix (ECM) macromolecules. Due to their wide tissue distribution, physical attributes and purity, collagen, and more recently, tropoelastin, represent two appealing ECM components for biomaterials development. Here we blend tropoelastin and collagen, harnessing the cell-modulatory properties of each biomolecule. Tropoelastin was stably co-blended into collagen biomaterials and was retained after EDC-crosslinking. We found that human dermal fibroblasts (HDF), rat glial cells (Rugli) and HT1080 fibrosarcoma cells ligate to tropoelastin via EDTA-sensitive and EDTA-insensitive receptors or do not ligate with tropoelastin, respectively. These differing elastin-binding properties allowed us to probe the cellular response to the tropoelastin-collagen composites assigning specific bioactivity to the collagen and tropoelastin component of the composite material. Tropoelastin addition to collagen increased total Rugli cell adhesion, spreading and proliferation. This persisted with EDC-crosslinking of the tropoelastin-collagen composite. Tropoelastin addition did not affect total HDF and HT1080 cell adhesion; however, it increased the contribution of cation-independent adhesion, without affecting the cell morphology or, for HT1080 cells, proliferation. Instead, EDC-crosslinking dictated the HDF and HT1080 cellular response. These data show that a tropoelastin component dominates the response of cells that possess non-integrin based tropoelastin receptors. EDC modification of the collagen component directs cell function when non-integrin tropoelastin receptors are not crucial for cell activity. Using this approach, we have assigned the biological contribution of each component of tropoelastin-collagen composites, allowing informed biomaterial design for directed cell function via more physiologically relevant mechanisms. STATEMENT OF SIGNIFICANCE: Biomaterials fabricated from multiple extracellular matrix (ECM) macromolecules are required to fully recreate the native tissue niche where each ECM macromolecule engages with a specific repertoire of cell-surface receptors. Here we investigate combining tropoelastin with collagen as they interact with cells via different receptors. We identified specific cell lines, which associate with tropoelastin via distinct classes of cell-surface receptor. These showed that tropoelastin, when combined with collagen, altered the cell behaviour in a receptor-usage dependent manner. Integrin-mediated tropoelastin interactions influenced cell proliferation and non-integrin receptors influenced cell spreading and proliferation. These data shed light on the interplay between biomaterial macromolecular composition, cell surface receptors and cell behaviour, advancing bespoke materials design and providing functionality to specific cell populations.
Source: europepmc · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Collagen: Extraction and Characterization · Connective tissue disorders research · Tribology and Lubrication Engineering
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (49)
Show source-provided references
1. Biomedical applications of collagen10.1016/S0378-5173(01)00691-3 ↗
2. The extracellular matrix at a glance10.1242/jcs.023820 ↗
3. Matricellular proteins: an overview10.1007/s12079-009-0069-z ↗
4. Glycosaminoglycans: key players in cancer cell biology and treatment10.1111/j.1742-4658.2012.08529.x ↗
5. Guide to collagen characterization for biomaterial studies10.1002/jbm.b.31078 ↗
6. Cellular response to collagen-elastin composite materials10.1016/j.actbio.2018.12.033 ↗
7. Vascular wall extracellular matrix proteins and vascular diseases10.1016/j.bbadis.2014.07.008 ↗
8. Collagens at a glance10.1242/jcs.03453 ↗
9. Biochemistry of the elastic fibers in normal connective tissues and its alterations in diseases10.1111/1523-1747.ep12530093 ↗
10. Elastin biology and tissue engineering with adult cells10.1515/bmc-2012-0040 ↗
11. Soluble matrix protein is a potent modulator of mesenchymal stem cell performance10.1073/pnas.1812951116 ↗
12. Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells10.1038/nbt.1687 ↗
13. Elastin binds to a multifunctional 67-kilodalton peripheral membrane protein10.1021/bi00435a014 ↗
14. Val-Gly-Val-Ala-Pro-Gly, a repeating peptide in elastin, is chemotactic for fibroblasts and monocytes10.1083/jcb.99.3.870 ↗
15. Tropoelastin interacts with cell-surface glycosaminoglycans via its COOH-terminal domain10.1074/jbc.M507309200 ↗
16. A novel cell adhesion region in tropoelastin mediates attachment to integrin αVβ510.1074/jbc.M113.518381 ↗
17. A cell adhesive peptide from tropoelastin promotes sequential cell attachment and spreading via distinct receptors10.1111/febs.14114 ↗
18. Cell adhesion to tropoelastin is mediated via the C-terminal GRKRK motif and integrin αvβ310.1074/jbc.M109.017525 ↗
19. Domains 12 to 16 of tropoelastin promote cell attachment and spreading through interactions with glycosaminoglycan and integrins alphaV and alpha5beta110.1111/febs.15702 ↗
20. Integrin ligands at a glance10.1242/jcs.03098 ↗
21. Integrin recognition motifs in the human collagens10.1007/978-94-017-9153-3_9 ↗
22. Elastin-based materials10.1039/b919452p ↗
23. Modification and functional inactivation of the tropoelastin carboxy-terminal domain in cross-linked elastin10.1016/j.matbio.2008.06.001 ↗
24. Biocompatibility and remodeling potential of pure arterial elastin and collagen scaffolds10.1016/j.biomaterials.2005.06.013 ↗
25. Tailoring the porosity and pore size of electrospun synthetic human elastin scaffolds for dermal tissue engineering10.1016/j.biomaterials.2011.05.065 ↗
26. Insoluble elastin reduces collagen scaffold stiffness, improves viscoelastic properties, and induces a contractile phenotype in smooth muscle cells10.1016/j.biomaterials.2015.09.003 ↗
27. Surface characterization of collagen/elastin based biomaterials for tissue regeneration10.1016/j.apsusc.2009.05.127 ↗
28. The interplay between physical and chemical properties of protein films affects their bioactivity10.1002/jbm.a.34187 ↗
29. Investigating the morphological, mechanical and degradation properties of scaffolds comprising collagen, gelatin and elastin for use in soft tissue engineering10.1016/j.jmbbm.2012.02.028 ↗
30. Preparation and evaluation of molecularly-defined collagen-elastin-glycosaminoglycan scaffolds for tissue engineering10.1016/S0142-9612(03)00273-4 ↗
31. Tissue response of defined collagen-elastin scaffolds in young and adult rats with special attention to calcification10.1016/j.biomaterials.2004.02.011 ↗
32. From nano to micro: topographical scale and its impact on cell adhesion, morphology and contact guidance10.1088/0953-8984/28/18/183001 ↗
33. Elastin as a nonthrombogenic biomaterial10.1089/ten.teb.2010.0432 ↗
34. Processing of collagen based biomaterials and the resulting materials properties10.1186/s12938-019-0647-0 ↗
35. Current methods of collagen cross-linking: review10.1016/j.ijbiomac.2020.06.075 ↗
36. Control of crosslinking for tailoring collagen-based scaffolds stability and mechanics10.1016/j.actbio.2015.07.034 ↗
37. Cross-linking of dermal sheep collagen using a water-soluble carbodiimide10.1016/0142-9612(96)81413-X ↗
38. Farndale · Biochem. Soc. Trans. · 2008 · 36 · 24110.1042/BST0360241 ↗
39. Fundamental insight into the effect of carbodiimide crosslinking on cellular recognition of collagen-based scaffolds10.1016/j.actbio.2016.11.059 ↗
40. Shape of tropoelastin, the highly extensible protein that controls human tissue elasticity10.1073/pnas.1014280108 ↗
41. In situ polymerization of tropoelastin in the absence of chemical cross-linking10.1016/j.biomaterials.2008.10.018 ↗
42. Integrin αvβ3 binds a unique non-RGD site near the C-terminus of human tropoelastin10.1016/j.biochi.2004.03.002 ↗
43. Tropoelastin massively associates during coacervation to form quantized protein spheres10.1021/bi0610092 ↗
44. Role of Liquid–Liquid Phase Separation in Assembly of Elastin and Other Extracellular Matrix Proteins10.1016/j.jmb.2018.06.010 ↗
45. Impact of elastin incorporation into electrochemically aligned collagen fibers on mechanical properties and smooth muscle cell phenotype10.1088/1748-6041/11/2/025008 ↗
46. Self-assembly of collagen bundles and enhanced piezoelectricity induced by chemical crosslinking10.1039/C9NR04750F ↗
47. Directed cell attachment by tropoelastin on masked plasma immersion ion implantation treated PTFE10.1016/j.biomaterials.2011.05.060 ↗
48. Signaling pathways transduced through the elastin receptor facilitate proliferation of arterial smooth muscle cells10.1074/jbc.M205630200 ↗
49. Structural basis of collagen recognition by integrin α2β110.1016/S0092-8674(00)80622-4 ↗