Functionalization of in vivo tissue-engineered living biotubes enhance patency and endothelization without the requirement of systemic anticoagulant administration

Niklason, 2020, Bioengineered human blood vessels, Science, 370, 10.1126/science.aaw8682 Fayon, 2021, Cellularized small-caliber tissue-engineered vascular grafts: looking for the ultimate gold standard, Npj Regenerative Medicine, 6, 1, 10.1038/s41536-021-00155-x Gupta, 2021, Tissue-engineered vascular grafts: emerging trends and technologies, Adv. Funct. Mater., 31, 10.1002/adfm.202100027 Dimitrievska, 2020, Glycocalyx-like hydrogel coatings for small diameter vascular grafts, Adv. Funct. Mater., 30, 10.1002/adfm.201908963 Gorbet, 2019, The blood compatibility challenge. Part 3: material associated activation of blood cascades and cells, Acta Biomater., 94, 25, 10.1016/j.actbio.2019.06.020 Radke, 2018, Tissue engineering at the blood-contacting surface: a review of challenges and strategies in vascular graft development, Adv. Healthc. Mater., 7, 10.1002/adhm.201701461 Solo, 2019, Antithrombotic treatment after coronary artery bypass graft surgery: systematic review and network meta-analysis, Br. Med. J., 367 Sostres, 2019, Risk of rebleeding, vascular events and death after gastrointestinal bleeding in anticoagulant and/or antiplatelet users, Aliment, Pharmacol. Ther., 50, 919 Peng, 2020, Multi-functional zwitterionic coating for silicone-based biomedical devices, Chem. Eng. J., 398, 10.1016/j.cej.2020.125663 Zhang, 2019, Zwitterionic oolymer-grafted polylactic acid vascular patches based on a decellularized scaffold for tissue engineering, ACS Biomater. Sci. Eng., 5, 4366, 10.1021/acsbiomaterials.9b00684 Ji, 2013, Dual functionalization of poly(epsilon-caprolactone) film surface through supramolecular assembly with the aim of promoting in situ endothelial progenitor cell attachment on vascular grafts, Biomacromolecules, 14, 4099, 10.1021/bm401239a Zhang, 2002, Biocompatibility evaluation of ePTFE membrane modified with PEG in atmospheric pressure glow discharge, J. Biomed. Mater. Res., 60, 502, 10.1002/jbm.1294 Khalifehzadeh, 2018, Surface fluorination of polylactide as a path to improve platelet associated hemocompatibility, Acta Biomater., 78, 23, 10.1016/j.actbio.2018.07.042 Paven, 2013, Super liquid-repellent gas membranes for carbon dioxide capture and heart-lung machines, Nat. Commun., 4, 2512, 10.1038/ncomms3512 Jaffer, 2015, Medical device-induced thrombosis: what causes it and how can we prevent it?, J. Thromb. Haemostasis, 13, S72, 10.1111/jth.12961 Irvine, 2012, Anti-platelet and tissue engineering approaches to biomaterial blood compatibilization: how well have these been translated into the clinic?, Drug Deliv. Transl. Res., 2, 384, 10.1007/s13346-012-0077-z Wang, 2021, A multi-in-one strategy with glucose-triggered long-term antithrombogenicity and sequentially enhanced endothelialization for biological valve leaflets, Biomaterials, 275, 10.1016/j.biomaterials.2021.120981 Yang, 2020, Endothelium-mimicking multifunctional coating modified cardiovascular stents via a stepwise metal-catechol-(amine) surface engineering strategy, Research, 2020 Heath, 2017, Promoting endothelialization of polymeric cardiovascular biomaterials, Macromol. Chem. Phys., 218, 10.1002/macp.201600574 Deng, 2017, Heparin/DNA aptamer co-assembled multifunctional catecholamine coating for EPC capture and improved hemocompatibility of vascular devices, Mat Sci Eng C-Mater., 79, 305, 10.1016/j.msec.2017.05.057 Duan, 2019, Co-immobilization of CD133 antibodies, vascular endothelial growth factors, and REDV peptide promotes capture, proliferation, and differentiation of endothelial progenitor cells, Acta Biomater., 96, 137, 10.1016/j.actbio.2019.07.004 Kou, 2020, Endothelial progenitor cells as the target for cardiovascular disease prediction, personalized prevention, and treatments: progressing beyond the state-of-the-art, EPMA J., 11, 629, 10.1007/s13167-020-00223-0 Collier, 2011, Evolving the use of peptides as components of biomaterials, Biomaterials, 32, 4198, 10.1016/j.biomaterials.2011.02.030 Wei, 2015, Colorimetric assay for protein detection based on "nano-pumpkin" induced aggregation of peptide-decorated gold nanoparticles, Biosens. Bioelectron., 71, 348, 10.1016/j.bios.2015.04.072 Yang, 2020, Bioclickable and mussel adhesive peptide mimics for engineering vascular stent surfaces, Proc. Natl. Acad. Sci. USA, 117, 16127, 10.1073/pnas.2003732117 Chen, 2015, Construction of a multifunctional coating consisting of phospholipids and endothelial progenitor cell-specific peptides on titanium substrates, Appl. Surf. Sci., 347, 169, 10.1016/j.apsusc.2015.02.032 Chen, 2016, Multifunctional coating based on EPC-specific peptide and phospholipid polymers for potential applications in cardiovascular implants fate, J. Mater. Chem.B, 4, 7870, 10.1039/C6TB01811D Chen, 2016, Immobilization of serum albumin and peptide aptamer for EPC on polydopamine coated titanium surface for enhanced in-situ self-endothelialization, Mat Sci Eng C-Mater., 60, 219, 10.1016/j.msec.2015.11.044 Li, 2013, Functionalization of the surface of electrospun poly(epsilon-caprolactone) mats using zwitterionic poly(carboxybetaine methacrylate) and cell-specific peptide for endothelial progenitor cells capture, Mat Sci Eng C-Mater., 33, 1646, 10.1016/j.msec.2012.12.074 Munisso, 2017, Novel peptides for small-caliber graft functionalization selected by a phage display of endothelial-positive/platelet-negative combined selection, J. Mater. Chem. B, 5, 9354, 10.1039/C7TB02652H Fang, 2016, Orthogonally functionalizable polyurethane with subsequent modification with heparin and endothelium-inducing peptide aiming for vascular reconstruction, ACS Appl. Mater., 8, 14442, 10.1021/acsami.6b04289 Veleva, 2008, Selective endothelial cell attachment to peptide-modified terpolymers, Biomaterials, 29, 3656, 10.1016/j.biomaterials.2008.05.022 Pang, 2015, In situ endothelialization: bioengineering considerations to translation, Small, 11, 6248, 10.1002/smll.201402579 Ren, 2015, Surface modification and endothelialization of biomaterials as potential scaffolds for vascular tissue engineering applications, Chem. Soc. Rev., 44, 5680, 10.1039/C4CS00483C Li, 2013, Functionalization of the surface of electrospun poly(epsilon-caprolactone) mats using zwitterionic poly(carboxybetaine methacrylate) and cell-specific peptide for endothelial progenitor cells capture, Mat Sci Eng C-Mater., 33, 1646, 10.1016/j.msec.2012.12.074 Avci-Adali, 2013, In vivo tissue engineering: mimicry of homing factors for self-endothelialization of blood-contacting materials, Pathobiology, 80, 176, 10.1159/000347222 Badv, 2020, Single and multi-functional coating strategies for enhancing the biocompatibility and tissue integration of blood-contacting medical implants, Biomaterials, 258, 10.1016/j.biomaterials.2020.120291 Navarro, 2021, Biomimetic tubular scaffold with heparin conjugation for rapid degradation in in situ regeneration of a small diameter neoartery, Biomaterials, 274, 10.1016/j.biomaterials.2021.120874 Dimitrievska, 2015, Click-coated, heparinized, decellularized vascular grafts, Acta Biomater., 13, 177, 10.1016/j.actbio.2014.11.015 Lee, 2011, Direct thrombin inhibitors, Br. J. Clin. Pharmacol., 72, 581, 10.1111/j.1365-2125.2011.03916.x Pacelli, 2016, Tailoring biomaterial surface properties to modulate host-implant interactions: implication in cardiovascular and bone therapy, J. Mater. Chem. B, 4, 1586, 10.1039/C5TB01686J Eitzman, 1994, Heparin neutralization by platelet-rich thrombi. Role of platelet factor 4, Circulation, 89, 1523, 10.1161/01.CIR.89.4.1523 Van Delden, 1996, The effect of protein adsorption on the anticoagulant activity of surface immobilized heparin, J. Biomater. Sci. Polym. Ed., 7, 727, 10.1163/156856296X00499 Ashcraft, 2021, Combination strategies for antithrombotic biomaterials: an emerging trend towards hemocompatibility, Biomater. Sci., 9, 2413, 10.1039/D0BM02154G Larsen, 2021, Thrombin: a pivotal player in hemostasis and beyond, Semin, Thromb. Hemost, 47, 759, 10.1055/s-0041-1727116 Lee, 2006, Bivalirudin in acute coronary syndrome's and percutaneous coronary intervention, Rev. Cardiovasc. Med., 7, S27 Ramana, 2008, Percutaneous coronary intervention in patients with acute coronary syndrome: focus on bivalirudin, Vasc, Healthc. Risk Manag., 4, 493 Moen, 2005, Bivalirudin - a review of its use in patients undergoing percutaneous coronary intervention, Drugs, 65, 1869, 10.2165/00003495-200565130-00010 Yamanami, 2010, Development of a completely autologous valved conduit with the sinus of Valsalva using in-body tissue architecture technology: a pilot study in pulmonary valve replacement in a beagle model, Circulation, 122, S100 Geelhoed, 2017, Utilizing the foreign body response to grow tissue engineered blood vessels in vivo, J. Cardiovasc. Transl. Res., 10, 167, 10.1007/s12265-017-9731-7 Zhi, 2022, Mechanically reinforced biotubes for arterial replacement and arteriovenous grafting inspired by architectural engineering, Sci. Adv., 8, 10.1126/sciadv.abl3888 Rothuizen, 2016, Development and evaluation of in vivo tissue engineered blood vessels in a porcine model, Biomaterials, 75, 82, 10.1016/j.biomaterials.2015.10.023 Teramura, 2010, Cell surface modification with polymers for biomedical studies, Soft Matter, 6, 1081, 10.1039/b913621e Yan, 2020, Targeted repair of vascular injury by adipose-derived stem cells modified with P-selectin binding peptide, Adv. Sci., 7, 10.1002/advs.201903516 Geelhoed, 2017, Utilizing the foreign body response to grow tissue engineered blood vessels in vivo, J. Cardiovasc. Transl., 10, 167, 10.1007/s12265-017-9731-7 Nakayama, 2018, Development of long in vivo tissue-engineered "Biotube" vascular grafts, Biomaterials, 185, 232, 10.1016/j.biomaterials.2018.09.032 Elson, 2015, Non-destructive monitoring of viability in an ex vivo organ culture model of osteochondral tissue, Eur. Cell. Mater., 29, 356, 10.22203/eCM.v029a27 Park, 2018, Engineering the surface of therapeutic "living" cells, Chem. Rev., 118, 1664, 10.1021/acs.chemrev.7b00157 De Koker, 2007, Vivo cellular uptake, degradation, and biocompatibility of polyelectrolyte microcapsules, Adv. Funct. Mater., 17, 3754, 10.1002/adfm.200700416 Zhang, 2021, Recent progress and perspectives on cell surface modification, Chem. Asian J., 16, 3250, 10.1002/asia.202100852 Cheng, 2012, Stem cell membrane engineering for cell rolling using peptide conjugation and tuning of cell-selectin interaction kinetics, Biomaterials, 33, 5004, 10.1016/j.biomaterials.2012.03.065 Manrique-Moreno, 2010, Effects of the nonsteroidal anti-inflammatory drug naproxen on human erythrocytes and on cell membrane molecular models, Biophys. Chem., 147, 53, 10.1016/j.bpc.2009.12.010 Tatsumi, 2012, The non-invasive cell surface modification of hepatocytes with PEG-lipid derivatives, Biomaterials, 33, 821, 10.1016/j.biomaterials.2011.10.016 Edelman, 1993, Flow velocity quantification in human coronary arteries with fast, breath-hold MR angiography, JMRI, 3, 699, 10.1002/jmri.1880030503 Teramura, 2011, Improvement of graft survival by surface modification with poly(ethylene glycol)-lipid and urokinase in intraportal islet transplantation, Transplantation, 91, 271, 10.1097/TP.0b013e3182034fa4 Miura, 2006, Encapsulation of islets with ultra-thin polyion complex membrane through poly(ethylene glycol)-phospholipids anchored to cell membrane, Biomaterials, 27, 5828, 10.1016/j.biomaterials.2006.07.039 Leslie, 2014, A bioinspired omniphobic surface coating on medical devices prevents thrombosis and biofouling, Nat. Biotechnol., 32, 1134, 10.1038/nbt.3020 Lugovskoy, 2011, Calix 4 arene methylenebisphosphonic acids as inhibitors of fibrin polymerization, FEBS J., 278, 1244, 10.1111/j.1742-4658.2011.08045.x Miyachi, 2018, Bone marrow-derived mononuclear cell seeded bioresorbable vascular graft improves acute graft patency by inhibiting thrombus formation via platelet adhesion, Int. J. Cardiol., 266, 61, 10.1016/j.ijcard.2018.01.059 Yang, 2012, Direct thrombin inhibitor-bivalirudin functionalized plasma polymerized allylamine coating for improved biocompatibility of vascular devices, Biomaterials, 33, 7959, 10.1016/j.biomaterials.2012.07.050 Jordan, 2007, Novel thromboresistant materials, J. Vasc. Surg., 45, 104A, 10.1016/j.jvs.2007.02.048 Campbell, 2008, Cellular procoagulant activity dictates clot structure and stability as a function of distance from the cell surface, Arterioscler. Thromb. Vasc. Biol., 28, 2247, 10.1161/ATVBAHA.108.176008 Campbell, 2009, Contributions of extravascular and intravascular cells to fibrin network formation, structure, and stability, Blood, 114, 4886, 10.1182/blood-2009-06-228940 Kattula, 2017, Fibrinogen and fibrin in hemostasis and thrombosis, Arterioscler. Thromb. Vasc. Biol., 37, E13, 10.1161/ATVBAHA.117.308564 Gao, 2020, Metal-catechol-(amine) networks for surface synergistic catalytic modification: therapeutic gas generation and biomolecule grafting, Biomaterials, 248, 10.1016/j.biomaterials.2020.119981 Yang, 2012, Mussel-inspired coating of polydopamine directs endothelial and smooth muscle cell fate for re-endothelialization of vascular devices, Adv. Healthc. Mater., 1, 548, 10.1002/adhm.201200073 Ma, 2020, Multifunctional 3D micro-nanostructures fabricated through temporally shaped femtosecond laser processing for preventing thrombosis and bacterial infection, ACS Appl. Mater. Interfaces, 12, 17155, 10.1021/acsami.9b20766 Kimmelstiel, 2011, Bivalirudin is a dual inhibitor of thrombin and collagen-dependent platelet activation in patients undergoing percutaneous coronary intervention, Circ. Cardiovasc. Interv., 4, 171, 10.1161/CIRCINTERVENTIONS.110.959098 Qiu, 2021, Phenolic-amine chemistry mediated synergistic modification with polyphenols and thrombin inhibitor for combating the thrombosis and inflammation of cardiovascular stents, Biomaterials, 269, 10.1016/j.biomaterials.2020.120626 Yang, 2018, Polydopamine modified TiO2 nanotube arrays for long-term controlled elution of bivalirudin and improved hemocompatibility, ACS Appl. Mater. Interfaces, 10, 7649, 10.1021/acsami.7b06108 Dahan, 2017, Dynamic autologous reendothelialization of small-caliber arterial extracellular matrix: a preclinical large animal study, Tissue Eng., 23, 69, 10.1089/ten.tea.2016.0126 Ren, 2014, Complementary density gradient of poly(hydroxyethyl methacrylate) and YIGSR selectively guides migration of endotheliocytes, Biomacromolecules, 15, 2256, 10.1021/bm500385n Yu, 2016, Preparation of an Arg-Glu-Asp-Val peptide density gradient on hyaluronic acid-coated poly(epsilon-caprolactone) film and its influence on the selective adhesion and directional migration of endothelial cells, ACS Appl. Mater. Interfaces, 8, 29280, 10.1021/acsami.6b09375 Seeto, 2013, Peptide-grafted poly(ethylene glycol) hydrogels support dynamic adhesion of endothelial progenitor cells, Acta Biomater., 9, 8279, 10.1016/j.actbio.2013.05.023 Hao, 2017, Discovery and characterization of a potent and specific peptide ligand targeting endothelial progenitor cells and endothelial cells for tissue regeneration, ACS Chem. Biol., 12, 1075, 10.1021/acschembio.7b00118 Shitole, 2019, Clopidogrel eluting electrospun polyurethane/polyethylene glycol thromboresistant, hemocompatible nanofibrous scaffolds, J. Biomater. Appl., 33, 1327, 10.1177/0885328219832984 Kuang, 2019, Electrospun bilayer composite vascular graft with an inner layer modified by polyethylene glycol and haparin to regenerate the blood vessel, J. Biomed. Nanotechnol., 15, 77, 10.1166/jbn.2019.2666 Choi, 2016, Enhanced patency and endothelialization of small-caliber vascular grafts fabricated by coimmobilization of heparin and cell-adhesive peptides, ACS Appl. Mater. Interfaces, 8, 4336, 10.1021/acsami.5b12052 Sakiyama-Elbert, 2000, Development of fibrin derivatives for controlled release of heparin-binding growth factors, J. Contr. Release, 65, 389, 10.1016/S0168-3659(99)00221-7 Walker, 2019, Generating surface-anchored zwitterionic networks and studying their resistance to bovine serum albumin adsorption, ACS Appl. Polym. Mater., 1, 3323, 10.1021/acsapm.9b00772 Xu, 2021, Zwitterionic PMCP-functionalized titanium surface resists protein adsorption, promotes cell adhesion, and enhances osteogenic activity, Colloids Surf. B Biointerfaces, 206, 10.1016/j.colsurfb.2021.111928 Boswell, 2012, Platelet-rich plasma: a milieu of bioactive factors, Arthroscopy, 28, 429, 10.1016/j.arthro.2011.10.018 Burnouf, 2013, Blood-derived biomaterials and platelet growth factors in regenerative medicine, Blood Rev., 27, 77, 10.1016/j.blre.2013.02.001 Wei, 2013, Surface engineering of cardiovascular stent with endothelial cell selectivity for in vivo re-endothelialisation, Biomaterials, 34, 2588, 10.1016/j.biomaterials.2012.12.036 Deng, 2016, Fabrication of endothelial progenitor cell capture surface via DNA aptamer modifying dopamine/polyethyleneimine copolymer film, Appl. Surf. Sci., 386, 138, 10.1016/j.apsusc.2016.06.015 Qiu, 2019, Biomimetic engineering endothelium-like coating on cardiovascular stent through heparin and nitric oxide-generating compound synergistic modification strategy, Biomaterials, 207, 10, 10.1016/j.biomaterials.2019.03.033 Melchiorri, 2015, Contrasting biofunctionalization strategies for the enhanced endothelialization of biodegradable vascular grafts, Biomacromolecules, 16, 437, 10.1021/bm501853s Wang, 2017, Functional modification of electrospun poly(epsilon-caprolactone) vascular grafts with the fusion protein VEGF-HGFI enhanced vascular regeneration, ACS Appl. Mater. Interfaces, 9, 11415, 10.1021/acsami.6b16713 Hao, 2020, Rapid endothelialization of small diameter vascular grafts by a bioactive integrin-binding ligand specifically targeting endothelial progenitor cells and endothelial cells, Acta Biomater., 108, 178, 10.1016/j.actbio.2020.03.005 Sanchez, 2018, Endothelialization mechanisms in vascular grafts, J. Tissue Eng. Regen. Med., 12, 2164, 10.1002/term.2747 He, 2005, Paracrine mitogenic effect of human endothelial progenitor cells: role of interleukin-8, Am. J. Physiol. Heart Circ. Physiol., 289, H968, 10.1152/ajpheart.01166.2004 Burger, 2015, Human endothelial colony-forming cells protect against acute kidney injury : role of exosomes, Am. J. Pathol., 185, 2309, 10.1016/j.ajpath.2015.04.010 Valgimigli, 2017, ESC focused update on dual antiplatelet therapy in coronary artery disease developed in collaboration with EACTS, Eur. Heart J., 39, 213, 10.1093/eurheartj/ehx419 Thames, 2017, The effects of clopidogrel and omeprazole on platelet function in normal dogs, J. Vet. Pharmacol. Therapeut., 40, 130, 10.1111/jvp.12340 McLewee, 2018, Effects of aspirin dose escalation on platelet function and urinary thromboxane and prostacyclin levels in normal dogs, J. Vet. Pharmacol. Therapeut., 41, 60, 10.1111/jvp.12432 Haines, 2016, Vitro and in vivo assessment of platelet function in healthy dogs during administration of a low-dose aspirin regimen, Am. J. Vet. Res., 77, 174, 10.2460/ajvr.77.2.174 Sugiura, 2018, Tissue-engineered vascular grafts in children with congenital heart disease: intermediate term follow-up, Semin. Thorac. Cardiovasc. Surg., 30, 175, 10.1053/j.semtcvs.2018.02.002 Blois, 2010, Effects of aspirin, carprofen, deracoxib, and meloxicam on platelet function and systemic prostaglandin concentrations in healthy dogs, Am. J. Vet. Res., 71, 349, 10.2460/ajvr.71.3.349 Sharma, 2019, Upgrading prevascularization in tissue engineering: a review of strategies for promoting highly organized microvascular network formation, Acta Biomater., 95, 112, 10.1016/j.actbio.2019.03.016 Kargozar, 2018, Bioactive Glasses: sprouting angiogenesis in tissue engineering, Trends Biotechnol., 36, 430, 10.1016/j.tibtech.2017.12.003 Shang, 2019, Supramolecular nanofibers with superior bioactivity to insulin-like growth factor-I, Nano Lett., 19, 1560, 10.1021/acs.nanolett.8b04406 Headen, 2018, Local immunomodulation with Fas ligand-engineered biomaterials achieves allogeneic islet graft acceptance, Nat. Mater., 17, 732, 10.1038/s41563-018-0099-0