Screening of Self-Assembling of Collagen IV Fragments into Stable Structures Potentially Useful in Regenerative Medicine

The aim of the research was to check whether it is possible to use fragments of type IV collagen to obtain, as a result of self-assembling, stable spatial structures that could be used to prepare new materials useful in regenerative medicine. Collagen IV fragments were obtained by using DMT/NMM/TosO− as a coupling reagent. The ability to self-organize and form stable spatial structures was tested by the CD method and microscopic techniques. Biological studies covered: resazurin assay (cytotoxicity assessment) on BJ, BJ-5TA and C2C12 cell lines; an alkaline version of the comet assay (genotoxicity), Biolegend Legendplex human inflammation panel 1 assay (SC cell lines, assessment of the inflammation activity) and MTT test to determine the cytotoxicity of the porous materials based on collagen IV fragments. It was found that out of the pool of 37 fragments (peptides 1–33 and 2.1–2.4) reconstructing the outer sphere of collagen IV, nine fragments (peptides: 2, 4, 5, 6, 14, 15, 25, 26 and 30), as a result of self-assembling, form structures mimicking the structure of the triple helix of native collagens. The stability of spatial structures formed as a result of self-organization at temperatures of 4 °C, 20 °C, and 40 °C was found. The application of the MST method allowed us to determine the Kd of binding of selected fragments of collagen IV to ITGα1β1. The stability of the spatial structures of selected peptides made it possible to obtain porous materials based on their equimolar mixture. The formation of the porous materials was found for cross-linked structures and the material stabilized only by weak interactions. All tested peptides are non-cytotoxic against all tested cell lines. Selected peptides also showed no genotoxicity and no induction of immune system responses. Research on the use of porous materials based on fragments of type IV collagen, able to form stable spatial structures as scaffolds useful in regenerative medicine, will be continued.

[1]  V. Uversky,et al.  The signal peptide of the amyloid precursor protein forms amyloid-like aggregates and enhances Aβ42 aggregation , 2021, Cell Reports Physical Science.

[2]  I. Majsterek,et al.  Physico-Chemical Properties and Biocompatibility of Thermosensitive Chitosan Lactate and Chitosan Chloride Hydrogels Developed for Tissue Engineering Application , 2021, Journal of functional biomaterials.

[3]  J. Diehl,et al.  The Potential Role of Small-Molecule PERK Inhibitor LDN-0060609 in Primary Open-Angle Glaucoma Treatment , 2021, International journal of molecular sciences.

[4]  M. Matsusaki,et al.  Bioprinted Vascularized Mature Adipose Tissue with Collagen Microfibers for Soft Tissue Regeneration , 2021, Cyborg and bionic systems.

[5]  C. Goergen,et al.  Regenerative tissue filler for breast conserving surgery and other soft tissue restoration and reconstruction needs , 2021, Scientific Reports.

[6]  Yujia Xu,et al.  Collagen Mimetic Peptides , 2021, Bioengineering.

[7]  Prahasanti Chiquita,et al.  Collagen from marine source for regenerative therapy: A literature review , 2020 .

[8]  Andrew J. Robinson,et al.  Review of Integrin‐Targeting Biomaterials in Tissue Engineering , 2020, Advanced healthcare materials.

[9]  Mariusz Dudek,et al.  Conjugates of Chitosan and Calcium Alginate with Oligoproline and Oligohydroxyproline Derivatives for Potential Use in Regenerative Medicine , 2020, Materials.

[10]  S. MacNeil,et al.  Bioengineered airway epithelial grafts with mucociliary function based on collagen IV- and laminin-containing extracellular matrix scaffolds , 2020, European Respiratory Journal.

[11]  K. Klimek,et al.  Proteins and Peptides as Important Modifiers of the Polymer Scaffolds for Tissue Engineering Applications—A Review , 2020, Polymers.

[12]  Julien Nicolas,et al.  3D Extracellular matrix mimics: fundamental concepts and role of materials chemistry to influence the stem cell fate. , 2020, Biomacromolecules.

[13]  Lele Tang,et al.  Novel Modification of Collagen: Realizing Desired Water Solubility and Thermostability in a Conflict-Free Way , 2020, ACS omega.

[14]  H. Sunami,et al.  Advances in regenerative therapy: A review of the literature and future directions , 2020, Regenerative therapy.

[15]  K. Majchrzycka,et al.  Multifunctional Polymer Composites Produced by Melt-Blown Technique to Use in Filtering Respiratory Protective Devices , 2020, Materials.

[16]  Xinpeng Xu,et al.  Elastic Anisotropy Governs the Range of Cell-Induced Displacements. , 2020, Biophysical journal.

[17]  Marcin Kolasa,et al.  Conjugates of Copper Alginate with Arginine-Glycine-Aspartic Acid (RGD) for Potential Use in Regenerative Medicine , 2020, Materials.

[18]  J. Hubbell,et al.  Targeting inflammatory sites through collagen affinity enhances the therapeutic efficacy of anti-inflammatory antibodies , 2019, Science Advances.

[19]  D. Zeugolis,et al.  Hydrolyzed Collagen—Sources and Applications , 2019, Molecules.

[20]  M. Bachmann,et al.  Cell Adhesion by Integrins. , 2019, Physiological reviews.

[21]  Robert P. Jenkins,et al.  Extracellular matrix anisotropy is determined by TFAP2C-dependent regulation of cell collisions , 2019, Nature Materials.

[22]  S. Van Vlierberghe,et al.  Collagen-Based Tissue Engineering Strategies for Vascular Medicine , 2019, Front. Bioeng. Biotechnol..

[23]  J. Cornish,et al.  The Role of In Vitro Immune Response Assessment for Biomaterials , 2019, Journal of functional biomaterials.

[24]  L. Katwa,et al.  What is the role of peptide fragments of collagen I and IV in health and disease? , 2019, Life sciences.

[25]  I. Gonçalves,et al.  Activation of immune responses against the basement membrane component collagen type IV does not affect the development of atherosclerosis in ApoE-deficient mice , 2019, Scientific Reports.

[26]  Anthony Atala,et al.  Skin tissue regeneration for burn injury , 2019, Stem Cell Research & Therapy.

[27]  P. Campochiaro,et al.  A collagen IV-derived peptide disrupts α5β1 integrin and potentiates Ang2/Tie2 signaling. , 2019, JCI insight.

[28]  T. Rabelink,et al.  Concise Review: The Endothelial Cell Extracellular Matrix Regulates Tissue Homeostasis and Repair , 2018, Stem cells translational medicine.

[29]  F. Fahimipour,et al.  Dual Porosity Protein-based Scaffolds with Enhanced Cell Infiltration and Proliferation , 2018, Scientific Reports.

[30]  Z. Shao,et al.  Shape-memory collagen scaffold for enhanced cartilage regeneration: native collagen versus denatured collagen. , 2018, Osteoarthritis and cartilage.

[31]  Lai‐Chang Zhang,et al.  Early plastic deformation behaviour and energy absorption in porous β-type biomedical titanium produced by selective laser melting , 2018, Scripta Materialia.

[32]  D. Laight,et al.  Effects of collagen-derived bioactive peptides and natural antioxidant compounds on proliferation and matrix protein synthesis by cultured normal human dermal fibroblasts , 2018, Scientific Reports.

[33]  K. Marra,et al.  Current Therapeutic Strategies for Adipose Tissue Defects/Repair Using Engineered Biomaterials and Biomolecule Formulations , 2018, Front. Pharmacol..

[34]  L. Rasmussen,et al.  A role for collagen type IV in cardiovascular disease? , 2018, American journal of physiology. Heart and circulatory physiology.

[35]  K. Jansen,et al.  Mechanotransduction at the cell-matrix interface. , 2017, Seminars in cell & developmental biology.

[36]  S. Gangloff,et al.  Collagen-Based Medical Device as a Stem Cell Carrier for Regenerative Medicine , 2017, International journal of molecular sciences.

[37]  D. Zeugolis,et al.  In Vitro Enzymatic Degradation of Tissue Grafts and Collagen Biomaterials by Matrix Metalloproteinases: Improving the Collagenase Assay. , 2017, ACS biomaterials science & engineering.

[38]  C. Kubiak,et al.  Effects of electron transfer on the stability of hydrogen bonds† †Electronic supplementary information (ESI) available. See DOI: 10.1039/c7sc03361c Click here for additional data file. , 2017, Chemical science.

[39]  K. Mak,et al.  Basement Membrane Type IV Collagen and Laminin: An Overview of Their Biology and Value as Fibrosis Biomarkers of Liver Disease , 2017, Anatomical record.

[40]  A. Rokas,et al.  Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues , 2017, eLife.

[41]  M. Kjaer,et al.  Connective tissue regeneration in skeletal muscle after eccentric contraction-induced injury. , 2017, Journal of applied physiology.

[42]  B. Hudson,et al.  Lysyl Oxidase-like-2 Cross-links Collagen IV of Glomerular Basement Membrane* , 2016, The Journal of Biological Chemistry.

[43]  R. Cameron,et al.  Collagen: a network for regenerative medicine , 2016, Journal of materials chemistry. B.

[44]  A. Sutter,et al.  Genotoxicity assessment of peptide/protein-related biotherapeutics: points to consider before testing. , 2016, Mutagenesis.

[45]  M. Stoddart,et al.  A surprisingly poor correlation between in vitro and in vivo testing of biomaterials for bone regeneration: results of a multicentre analysis. , 2016, European cells & materials.

[46]  Matthew A. Cooper,et al.  Contribution of Amphipathicity and Hydrophobicity to the Antimicrobial Activity and Cytotoxicity of β-Hairpin Peptides , 2016, ACS infectious diseases.

[47]  R. Cameron,et al.  Parameterizing the Transport Pathways for Cell Invasion in Complex Scaffold Architectures , 2016, Tissue engineering. Part C, Methods.

[48]  Yonggang Lv,et al.  Application of Collagen Scaffold in Tissue Engineering: Recent Advances and New Perspectives , 2016, Polymers.

[49]  Íñigo Valiente-Alandí,et al.  Extracellular matrix-mediated cellular communication in the heart. , 2016, Journal of molecular and cellular cardiology.

[50]  R. Cameron,et al.  Tailoring chitosan/collagen scaffolds for tissue engineering: Effect of composition and different crosslinking agents on scaffold properties. , 2015, Carbohydrate polymers.

[51]  Frank Wien,et al.  Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy , 2015, Proceedings of the National Academy of Sciences.

[52]  Kayoko Kawakami,et al.  Inhibitory effect of collagen-derived tripeptides on dipeptidylpeptidase-IV activity , 2014, Journal of enzyme inhibition and medicinal chemistry.

[53]  M. Ndagijimana,et al.  Low molecular weight bioactive peptides derived from the enzymatic hydrolysis of collagen after isoelectric solubilization/precipitation process of turkey by-products. , 2014, Poultry science.

[54]  Yoshihiko Hayashi,et al.  Potency of Fish Collagen as a Scaffold for Regenerative Medicine , 2014, BioMed research international.

[55]  C. Pace,et al.  Contribution of hydrogen bonds to protein stability , 2014, Protein science : a publication of the Protein Society.

[56]  D. Braun,et al.  Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions. , 2013, Methods.

[57]  Joseph A Loo,et al.  Investigation of stable and transient protein–protein interactions: Past, present, and future , 2013, Proteomics.

[58]  Miroslav Požek,et al.  Role of microscopic phase separation in gelation of aqueous gelatin solutions. , 2012, Soft matter.

[59]  R. Pöllänen,et al.  Basement membrane collagen type IV expression by human mesenchymal stem cells during adipogenic differentiation , 2012, Journal of cellular and molecular medicine.

[60]  M. S. Howard,et al.  Collagen IV in Normal Skin and in Pathological Processes , 2012, North American journal of medical sciences.

[61]  A. Popel,et al.  Development of a biomimetic peptide derived from collagen IV with anti-angiogenic activity in breast cancer , 2011, Cancer biology & therapy.

[62]  M. Karsdal,et al.  Assessment of proteolytic degradation of the basement membrane: a fragment of type IV collagen as a biochemical marker for liver fibrosis , 2011, Fibrogenesis & tissue repair.

[63]  J. Turnbull,et al.  Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. , 2011, The Journal of endocrinology.

[64]  P. Yurchenco.  Basement membranes: cell scaffoldings and signaling platforms. , 2011, Cold Spring Harbor perspectives in biology.

[65]  James M. Anderson,et al.  Biocompatibility of implants: lymphocyte/macrophage interactions , 2011, Seminars in Immunopathology.

[66]  Xuejun Xu,et al.  An Engineered α1 Integrin-binding Collagenous Sequence , 2010, The Journal of Biological Chemistry.

[67]  R. Cameron,et al.  Binding and release characteristics of insulin-like growth factor-1 from a collagen-glycosaminoglycan scaffold. , 2010, Tissue engineering. Part C, Methods.

[68]  G. Lajoie,et al.  Matrigel: A complex protein mixture required for optimal growth of cell culture , 2010, Proteomics.

[69]  N. Miosge,et al.  Basement membrane components are key players in specialized extracellular matrices , 2010, Cellular and Molecular Life Sciences.

[70]  Janice M Reichert,et al.  Current trends in the clinical development of peptide therapeutics. , 2009, IDrugs : the investigational drugs journal.

[71]  Fanling Meng,et al.  A single-point mutation converts the highly amyloidogenic human islet amyloid polypeptide into a potent fibrillization inhibitor. , 2007, Journal of the American Chemical Society.

[72]  Herbert Edelsbrunner,et al.  Protein-protein interfaces: properties, preferences, and projections. , 2007, Journal of proteome research.

[73]  H. Kleinman,et al.  Matrigel: basement membrane matrix with biological activity. , 2005, Seminars in cancer biology.

[74]  K. Pietrucha.  Changes in denaturation and rheological properties of collagen-hyaluronic acid scaffolds as a result of temperature dependencies. , 2005, International journal of biological macromolecules.

[75]  U. Schlötzer-Schrehardt,et al.  Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development , 2004, Development.

[76]  T. Aigner,et al.  Collagens--structure, function, and biosynthesis. , 2003, Advanced drug delivery reviews.

[77]  R. Kalluri.  Basement membranes: structure, assembly and role in tumour angiogenesis , 2003, Nature reviews. Cancer.

[78]  I. Selak,et al.  Type IV collagen immunoreactivity of basement membrane in inflammatory-regenerative and dysplastic lesions of the flat colonic mucosa. , 2003, Bosnian journal of basic medical sciences.

[79]  B. Olsen,et al.  The role of collagen-derived proteolytic fragments in angiogenesis. , 2001, Matrix biology : journal of the International Society for Matrix Biology.

[80]  D. Eisenberg,et al.  A census of protein repeats. , 1999, Journal of molecular biology.

[81]  A Oosterhof,et al.  Preparation and characterization of porous crosslinked collagenous matrices containing bioavailable chondroitin sulphate. , 1999, Biomaterials.

[82]  K. Chou,et al.  A Model for Structure-Dependent Binding of Congo Red to Alzheimer β-Amyloid Fibrils , 1998, Neurobiology of Aging.

[83]  H. Kawasaki,et al.  Comparison of serum 7S fragment of type IV collagen and serum central triple-helix of type IV collagen for assessment of liver fibrosis in patients with chronic viral liver disease. , 1996, Journal of hepatology.

[84]  J. Pettegrew,et al.  Quantitative evaluation of congo red binding to amyloid-like proteins with a beta-pleated sheet conformation. , 1989, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[85]  J. Bella,et al.  Fibrillar Collagens. , 2017, Sub-cellular biochemistry.

[86]  B. Kolesińska,et al.  The Effect of Counterion and Tertiary Amine on the Efficiency of N‐Triazinylammonium Sulfonates in Solution and Solid‐Phase Peptide Synthesis , 2015 .

[87]  S. Ricard-Blum.  The collagen family. , 2011, Cold Spring Harbor perspectives in biology.

[88]  D. Birk,et al.  Collagens, Suprastructures, and Collagen Fibril Assembly , 2011 .

[89]  Jürgen Engel,et al.  An Overview of Extracellular Matrix Structure and Function , 2011 .

[90]  M. Khrestchatisky,et al.  Synthetic therapeutic peptides: science and market. , 2010, Drug discovery today.

[91]  N. Greenfield.  Using circular dichroism spectra to estimate protein secondary structure , 2007, Nature Protocols.

[92]  Peter Lloyd Jones,et al.  The Extracellular Matrix in Development , 2022 .