Biomimetic Bioactive Biomaterials: The Next ... - ACS Publications

---

Editorial pubs.acs.org/journal/abseba

Biomimetic Bioactive Biomaterials: The Next Generation of Implantable Devices

I

addition to its optimal biophysical features, have controlled and localized delivery capacity of various cargos (e.g., cells,40−42 bioactive molecules43−46) to stimulate and promote functional regeneration. Over the years, numerous natural or synthetic in origin nano- to microscale scaffolds have been assessed as delivery vehicles in multiple clinical indications. Data to-date clearly illustrate that the scaffold enhances the cargo’s localization and activity at the site of injury,47,48 reducing that way the need for multiple operations, avoiding toxicity issues associated with the nontargeted systemic delivery, and offering more effective therapies. This special issue discusses natural and synthetic biomimetic, bioinspired, and bioactive biomaterials over different length scales and their capacity to modulate cellular functions and/or to deliver in localized and sustained fashion various therapeutics.49−74 It is evidenced that significant strides have been achieved. We anticipate that in the years to come, these elegant technologies will reach clinical translation and commercialization.

njuries and degenerative conditions continuously increase and financially stress the already stretched healthcare systems worldwide. Given that advances in medicine have prolonged life expectancy, it is becoming imperative to develop functional therapies that would repair and regenerate damaged organs and tissues. Tissue grafts, in the form of autografts,1,2 allografts,3,4 and xenografts,5,6 constitute the first line of defense and are often characterized as the “gold standard” in clinical practice. However, limitations associated with scarce availability, insufficient remodelling, substandard stability, poor biological response, and adverse immune reactions have questioned their clinical suitability7,8 and gave rise to the field of biomaterials. The first generation of biomaterials-based therapies imitated the gross composition and mechanical properties of the tissue to be replaced. However, it soon became apparent that this approach does not recapitulate the complexity of the native tissue microenvironment. The new frontier in biomaterials design is based on the principle of biomimicry.9 We are aspiring to engineer biomimetic,10−12 bioinspired,13−15 and bioactive16−18 biomaterials that would imitate the intricate extracellular matrix (ECM) composition and architecture and provide the necessary bioactive cues/instructive signals that would offer control over cellular functions in vitro and positively interact with the host and actively contribute to the process of tissue regeneration in vivo. Advancements in engineering, chemistry, biology, and medicine have been catalytic toward this goal.19 Architectural (e.g., topography) and mechanical (e.g., elasticity) features of the ECM regulate cellular migration, functionality and lineage commitment and directional neotissue formation. Thus, recapitulation of the native tissue biophysical properties is fundamental for functional repair and regeneration. Nano- and micro- fabrication technologies, such as additive manufacturing, electro-spinning and imprinting lithography, have been used extensively due to their high biomimicry, reproducibility and versatility.20−26 These sophisticated biomaterials’ fabrication technologies have enabled the development of tissue culture substrates that control cellular functions in vitro27−30 and can be used as high-throughput screening platforms to study the interplay between surface topography and cell behavior in vitro.31 They have also facilitated the development of microfluidic devices32−34 and in vitro models35,36 to study physiological and pathophysiological processes, with higher level of accuracy/biomimicry than traditional two-dimensional culture systems. They have also allowed the engineering of implantable devices that closely imitate architectural features of native ECM supramolecular assemblies down to the nanometer level and have been shown to promote functional repair and regeneration in a plethora of preclinical models.37−39 Tissue regeneration is a complex and well-orchestrated spatiotemporal process of a diverse range of biochemical and biological signals. It is therefore important that the scaffold, in © 2017 American Chemical Society

Dimitrios Tsiapalis†

National University of Ireland Galway

Andrea De Pieri†

National University of Ireland Galway and Proxy Biomedical Ltd.

Manus Biggs, Guest Editor National University of Ireland Galway

Abhay Pandit, Guest Editor National University of Ireland Galway

Dimitrios I. Zeugolis, Guest Editor

■

National University of Ireland Galway

AUTHOR INFORMATION

Notes

Views expressed in this editorial are those of the authors and not necessarily the views of the ACS. † D.T. and A.D.P. share first authorship.

■

REFERENCES

(1) Busin, M.; Breda, C.; Bertolin, M.; Bovone, C.; Ponzin, D.; Ferrari, S.; Barbaro, V.; Elbadawy, H. M. Corneal epithelial stem cells repopulate the donor area within 1 year from limbus removal for limbal autograft. Ophthalmology 2016, 123 (12), 2481−2488. (2) Slone, H. S.; Romine, S. E.; Premkumar, A.; Xerogeanes, J. W. Quadriceps tendon autograft for anterior cruciate ligament reconstruction: A comprehensive review of current literature and systematic review of clinical results. Arthroscopy: the journal of arthroscopic & related surgery: official publication of the Arthroscopy Association of North

Special Issue: Biomimetic Bioactive Biomaterials: The Next Generation of Implantable Devices Received: June 12, 2017 Published: July 10, 2017 1172

DOI: 10.1021/acsbiomaterials.7b00372 ACS Biomater. Sci. Eng. 2017, 3, 1172−1174

ACS Biomaterials Science & Engineering

Editorial

America and the International Arthroscopy Association 2015, 31 (3), 541−54. (3) Rinkinen, J.; Selley, R.; Agarwal, S.; Loder, S.; Levi, B. Skin allograft and vascularized composite allograft: Potential for long-term efficacy in the context of lymphatic modulation. Journal of burn care & research: official publication of the American Burn Association 2014, 35 (5), 355−61. (4) Palmer, J. E.; Russell, J. P.; Grieshober, J.; Iacangelo, A.; Ellison, B. A.; Lease, T. D.; Kim, H.; Henn, R. F., 3rd; Hsieh, A. H. A biomechanical comparison of allograft tendons for ligament reconstruction. American journal of sports medicine 2017, 45 (3), 701−707. (5) Shibuya, N.; Jupiter, D. C. Bone graft substitute: Allograft and xenograft. Clinics in podiatric medicine and surgery 2015, 32 (1), 21−34. (6) Seyler, T. M.; Bracey, D. N.; Plate, J. F.; Lively, M. O.; Mannava, S.; Smith, T. L.; Saul, J. M.; Poehling, G. G.; Van Dyke, M. E.; Whitlock, P. W. The development of a xenograft-derived scaffold for tendon and ligament reconstruction using a decellularization and oxidation protocol. Arthroscopy: the journal of arthroscopic & related surgery: official publication of the Arthroscopy Association of North America and the International Arthroscopy Association 2017, 33 (2), 374−386. (7) Janssen, R. P.; van der Wijk, J.; Fiedler, A.; Schmidt, T.; Sala, H. A.; Scheffler, S. U. Remodelling of human hamstring autografts after anterior cruciate ligament reconstruction. Knee surgery, sports traumatology, arthroscopy: official journal of the ESSKA 2011, 19 (8), 1299−306. (8) Bolton, E. M.; Bradley, J. A. Avoiding immunological rejection in regenerative medicine. Regener. Med. 2015, 10 (3), 287−304. (9) Pellowe, A.; Gonzalez, A. Extracellular matrix biomimicry for the creation of investigational and therapeutic devices. Wiley Interdiscip Rev. Nanomed Nanobiotechnol 2016, 8 (1), 5−22. (10) Ma, P. X. Biomimetic materials for tissue engineering. Adv. Drug Delivery Rev. 2008, 60 (2), 184−198. (11) Lee, N.; Robinson, J.; Lu, H. Biomimetic strategies for engineering composite tissues. Curr. Opin. Biotechnol. 2016, 40, 64−74. (12) Diesendruck, C.; Sottos, N.; Moore, J.; White, S. Biomimetic self-healing. Angew. Chem., Int. Ed. 2015, 54 (36), 10428−10447. (13) Fisher, O.; Khademhosseini, A.; Langer, R.; Peppas, N. Bioinspired materials for controlling stem cell fate. Acc. Chem. Res. 2010, 43 (3), 419−428. (14) Zhao, Y.; Sakai, F.; Su, L.; Liu, Y.; Wei, K.; Chen, G.; Jiang, M. Progressive macromolecular self-assembly: From biomimetic chemistry to bio-inspired materials. Adv. Mater. 2013, 25 (37), 5215−5256. (15) Zan, G.; Wu, Q. Biomimetic and bioinspired synthesis of nanomaterials/nanostructures. Adv. Mater. 2016, 28 (11), 2099−2147. (16) Davis, H.; Leach, J. Designing bioactive delivery systems for tissue regeneration. Ann. Biomed. Eng. 2011, 39 (1), 1−13. (17) Gabriel, D.; Dvir, T.; Kohane, D. Delivering bioactive molecules as instructive cues to engineered tissues. Expert Opin. Drug Delivery 2012, 9 (4), 473−492. (18) DeForest, C.; Anseth, K. Advances in bioactive hydrogels to probe and direct cell fate. Annu. Rev. Chem. Biomol. Eng. 2012, 3, 421− 444. (19) Zeugolis, D.; Pandit, A. Regenerative medicine in the 21st century: Advances in engineering, chemistry, biology and medicine revolutionize healthcare. Adv. Healthcare Mater. 2015, 4 (16), 2324− 2325. (20) Ryan, C. N.; Fuller, K. P.; Larranaga, A.; Biggs, M.; Bayon, Y.; Sarasua, J. R.; Pandit, A.; Zeugolis, D. I. An academic, clinical and industrial update on electrospun, additive manufactured and imprinted medical devices. Expert Rev. Med. Devices 2015, 12 (5), 601−12. (21) Abbah, S. A.; Delgado, L. M.; Azeem, A.; Fuller, K.; Shologu, N.; Keeney, M.; Biggs, M. J.; Pandit, A.; Zeugolis, D. I. Harnessing hierarchical nano- and micro-fabrication technologies for musculoskeletal tissue engineering. Adv. Healthcare Mater. 2015, 4 (16), 2488−99. (22) Biggs, M.; Pandit, A.; Zeugolis, D. 2D imprinted substrates and 3D electrospun scaffolds revolutionize biomedicine. Nanomedicine (London, U. K.) 2016, 11 (9), 989−992.

(23) Dvir, T.; Timko, B. P.; Kohane, D. S.; Langer, R. Nanotechnological strategies for engineering complex tissues. Nat. Nanotechnol. 2011, 6 (1), 13−22. (24) Leijten, J.; Rouwkema, J.; Zhang, Y. S.; Nasajpour, A.; Dokmeci, M. R.; Khademhosseini, A. Advancing tissue engineering: A tale of nano-, micro-, and macroscale integration. Small 2016, 12 (16), 2130− 45. (25) Fuller, K.; Pandit, A.; Zeugolis, D. The multifaceted potential of electro-spinning in regenerative medicine. Pharm. Nanotechnol. 2014, 2 (1), 23−34. (26) Mota, C.; Puppi, D.; Chiellini, F.; Chiellini, E. Additive manufacturing techniques for the production of tissue engineering constructs. J. Tissue Eng. Regener. Med. 2015, 9 (3), 174−190. (27) Azeem, A.; English, A.; Kumar, P.; Satyam, A.; Biggs, M.; Jones, E.; Tripathi, B.; Basu, N.; Henkel, J.; Vaquette, C.; Rooney, N.; Riley, G.; O’Riordan, A.; Cross, G.; Ivanovski, S.; Hutmacher, D.; Pandit, A.; Zeugolis, D. The influence of anisotropic nano- to micro-topography on in vitro and in vivo osteogenesis. Nanomedicine (London, U. K.) 2015, 10 (5), 693−711. (28) English, A.; Azeem, A.; Spanoudes, K.; Jones, E.; Tripathi, B.; Basu, N.; McNamara, K.; Tofail, S.; Rooney, N.; Riley, G.; O’Riordan, A.; Cross, G.; Hutmacher, D.; Biggs, M.; Pandit, A.; Zeugolis, D. Substrate topography: A valuable in vitro tool, but a clinical red herring for in vivo tenogenesis. Acta Biomater. 2015, 27, 3−12. (29) Abagnale, G.; Steger, M.; Nguyen, V.; Hersch, N.; Sechi, A.; Joussen, S.; Denecke, B.; Merkel, R.; Hoffmann, B.; Dreser, A.; Schnakenberg, U.; Gillner, A.; Wagner, W. Surface topography enhances differentiation of mesenchymal stem cells towards osteogenic and adipogenic lineages. Biomaterials 2015, 61, 316−326. (30) Hyysalo, A.; Ristola, M.; Joki, T.; Honkanen, M.; Vippola, M.; Narkilahti, S. Aligned poly(ε-caprolactone) nanofibers guide the orientation and migration of human pluripotent stem cell-derived neurons, astrocytes, and oligodendrocyte precursor cells in vitro. Macromol. Biosci. 2017, 1600517. (31) Unadkat, H.; Hulsman, M.; Cornelissen, K.; Papenburg, B.; Truckenmüller, R.; Carpenter, A.; Wessling, M.; Post, G.; Uetz, M.; Reinders, M.; Stamatialis, D.; van Blitterswijk, C.; de Boer, J. An algorithm-based topographical biomaterials library to instruct cell fate. Proc. Natl. Acad. Sci. U. S. A. 2011, 108 (40), 16565−16570. (32) Bhatia, S. N.; Ingber, D. E. Microfluidic organs-on-chips. Nat. Biotechnol. 2014, 32 (8), 760−72. (33) Kobel, S.; Lutolf, M. P. Biomaterials meet microfluidics: Building the next generation of artificial niches. Curr. Opin. Biotechnol. 2011, 22 (5), 690−7. (34) Sackmann, E. K.; Fulton, A. L.; Beebe, D. J. The present and future role of microfluidics in biomedical research. Nature 2014, 507 (7491), 181−9. (35) Shologu, N.; Szegezdi, E.; Lowery, A.; Kerin, M.; Pandit, A.; Zeugolis, D. Recreating complex pathophysiologies in vitro with extracellular matrix surrogates for anticancer therapeutics screening. Drug Discovery Today 2016, 21 (9), 1521−1531. (36) Janani, G.; Pillai, M.; Selvakumar, R.; Bhattacharyya, A.; Sabarinath, C. An in vitro 3D model using collagen coated gelatin nanofibers for studying breast cancer metastasis. Biofabrication 2017, 9 (1), 015016. (37) Ingavle, G.; Leach, J. Advancements in electrospinning of polymeric nanofibrous scaffolds for tissue engineering. Tissue Eng., Part B 2014, 20 (4), 277−293. (38) Muerza-Cascante, M.; Haylock, D.; Hutmacher, D.; Dalton, P. Melt electrospinning and its technologization in tissue engineering. Tissue Eng., Part B 2015, 21 (2), 187−202. (39) Giannitelli, S.; Mozetic, P.; Trombetta, M.; Rainer, A. Combined additive manufacturing approaches in tissue engineering. Acta Biomater. 2015, 24, 1−11. (40) Schulze, M.; Tobiasch, E. Artificial scaffolds and mesenchymal stem cells for hard tissues. Adv. Biochem. Eng./Biotechnol. 2011, 126, 153−94. (41) Wan, A.; Ying, J. Nanomaterials for in situ cell delivery and tissue regeneration. Adv. Drug Delivery Rev. 2010, 62 (7−8), 731−740. 1173

DOI: 10.1021/acsbiomaterials.7b00372 ACS Biomater. Sci. Eng. 2017, 3, 1172−1174

ACS Biomaterials Science & Engineering

Editorial

(42) Abbah, S.; Spanoudes, K.; O’Brien, T.; Pandit, A.; Zeugolis, D. Assessment of stem cell carriers for tendon tissue engineering in preclinical models. Stem Cell Res. Ther. 2014, 5 (2), 38. (43) Park, K. Controlled drug delivery systems: Past forward and future back. J. Controlled Release 2014, 190, 3−8. (44) Vo, T. N.; Kasper, F. K.; Mikos, A. G. Strategies for controlled delivery of growth factors and cells for bone regeneration. Adv. Drug Delivery Rev. 2012, 64 (12), 1292−309. (45) Spiller, K. L.; Nassiri, S.; Witherel, C. E.; Anfang, R. R.; Ng, J.; Nakazawa, K. R.; Yu, T.; Vunjak-Novakovic, G. Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds. Biomaterials 2015, 37, 194−207. (46) Raisin, S.; Belamie, E.; Morille, M. Non-viral gene activated matrices for mesenchymal stem cells based tissue engineering of bone and cartilage. Biomaterials 2016, 104, 223−37. (47) Hakimi, O.; Murphy, R.; Stachewicz, U.; Hislop, S.; Carr, A. An electrospun polydioxanone patch for the localisation of biological therapies during tendon repair. Eur. Cell Mater. 2012, 24, 344−357. (48) Gao, W.; Zhang, Y.; Zhang, Q.; Zhang, L. Nanoparticlehydrogel: A hybrid biomaterial system for localized drug delivery. Ann. Biomed. Eng. 2016, 44 (6), 2049−2061. (49) Bracaglia, L. G.; Messina, M.; Vantucci, C.; Baker, H. B.; Pandit, A.; Fisher, J. P., Controlled delivery of tissue inductive factors in a cardiovascular hybrid biomaterial scaffold. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00460. (50) Babo, P. S.; Pires, R. L.; Santos, L.; Franco, A.; Rodrigues, F.; Leonor, I.; Reis, R. L.; Gomes, M. E., Platelet lysate-loaded photocrosslinkable hyaluronic acid hydrogels for periodontal endogenous regenerative technology. ACS Biomater. Sci. Eng. 2017, 10.1021/ acsbiomaterials.6b00508. (51) Breen, B. A.; Kraskiewicz, H.; Ronan, R.; Kshiragar, A.; Patar, A.; Sargeant, T.; Pandit, A.; McMahon, S. S., Therapeutic effect of neurotrophin-3 treatment in an injectable collagen scaffold following rat spinal cord hemisection injury. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00167. (52) Kotla, N. G.; Chandrasekar, B.; Rooney, P.; Sivaraman, G.; Larrañaga, A.; Krishna, K. V.; Pandit, A.; Rochev, Y., Biomimetic Llpidbased nanosystems for enhanced dermal delivery of drugs and bioactive agents. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00681. (53) O’Leary, C.; O’Brien, F. J.; Cryan, S.-A., Retinoic acid-loaded collagen-hyaluronate scaffolds: A bioactive material for respiratory tissue regeneration. ACS Biomater. Sci. Eng. 2017, 10.1021/ acsbiomaterials.6b00561. (54) Järvinen, T. A. H.; Rashid, J.; Valmari, T.; May, U.; Ahsan, F., Systemically administered, target-specific therapeutic recombinant proteins and nanoparticles for regenerative medicine. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00746. (55) Tsekoura, E. K.; K.C., R. B.; Uludag, H., Biomaterials to facilitate delivery of RNA agents in bone regeneration and repair. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00387. (56) Liu, S.; Gao, Y.; A, S.; Zhou, D.; Greiser, U.; Guo, T.; Guo, R.; Wang, W., Biodegradable highly branched poly(β-amino esters) for targeted cancer cell gene transfection. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00503. (57) Berndt, M.; Li, Y.; Seyedhassantehrani, N.; Yao, L., Fabrication and characterization of microspheres encapsulating astrocytes for neural regeneration. ACS Biomater. Sci. Eng. 2017, 10.1021/ acsbiomaterials.6b00229. (58) Shao, W.; He, J.; Wang, Q.; Cui, S.; Ding, B., Biomineralized poly(l-lactic-co-glycolic acid)/graphene oxide/tussah silk fibroin nanofiber scaffolds with multiple orthogonal layers enhance osteoblastic differentiation of mesenchymal stem cells. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00533. (59) Azeem, A.; Marani, L.; Fuller, K.; Spanoudes, K.; Pandit, A.; Zeugolis, D. I., Influence of nonsulfated polysaccharides on the properties of electrospun poly(lactic-co-glycolic acid) fibers. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00206.

(60) Picca, R. A.; Paladini, F.; Sportelli, M. C.; Pollini, M.; Giannossa, L. C.; Di Franco, C.; Panico, A.; Mangone, A.; Valentini, A.; Cioffi, N., Combined approach for the development of efficient and safe nanoantimicrobials: The case of nanosilver-modified polyurethane foams. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00597. (61) Zhou, J.; Li, B.; Zhao, L.; Zhang, L.; Han, Y., F-doped micropore/nanorod hierarchically patterned coatings for improving antibacterial and osteogenic activities of bone implants in bacteriainfected cases. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00710. (62) Watson, E.; Tatara, A. M.; Kontoyiannis, D. P.; Mikos, A. G., Inherently antimicrobial biodegradable polymers in tissue engineering. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00501. (63) Chrobak, M. O.; Hansen, K. J.; Gershlak, J. R.; Vratsanos, M.; Kanellias, M.; Gaudette, G. R.; Pins, G. D., Design of a fibrin microthread-based composite layer for use in a cardiac patch. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00547. (64) Costa-Almeida, R.; Gasperini, L.; Borges, J.; Babo, P. S.; Rodrigues, M. T.; Mano, J. F.; Reis, R. L.; Gomes, M. E., Microengineered multicomponent hydrogel fibers: Combining polyelectrolyte complexation and microfluidics. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00331. (65) Ratheesh, G.; Venugopal, J. R.; Chinappan, A.; Ezhilarasu, H.; Sadiq, A.; Ramakrishna, S., 3D fabrication of polymeric scaffolds for regenerative therapy. ACS Biomater. Sci. Eng. 2017, 10.1021/ acsbiomaterials.6b00370. (66) Civantos, A.; Martínez-Campos, E.; Ramos, V.; Elvira, C.; Gallardo, A.; Abarrategi, A., Titanium coatings and surface modifications: Toward clinically useful bioactive implants. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00604. (67) Dikina, A. D.; Almeida, H. V.; Cao, M.; Kelly, D. J.; Alsberg, E., Scaffolds derived from ECM produced by chondrogenically induced human MSC condensates support human MSC chondrogenesis. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00654. (68) Papadimitriou, L.; Kaliva, M.; Vamvakaki, M.; Chatzinikolaidou, M., Immunomodulatory potential of chitosan-graft-poly(ε-caprolactone) copolymers toward the polarization of bone-marrow-derived macrophages. ACS Biomater. Sci. Eng. 2017,10.1021/acsbiomaterials.6b00440. (69) Deidda, G.; Jonnalagadda, S. V. R.; Spies, J. W.; Ranella, A.; Mossou, E.; Forsyth, V. T.; Mitchell, E. P.; Bowler, M. W.; Tamamis, P.; Mitraki, A., Self-assembled amyloid peptides with Arg-Gly-Asp (RGD) motifs as scaffolds for tissue engineering. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00570. (70) Thorat, N. D.; Bohara, R. A.; Noor, M. R.; Dhamecha, D.; Soulimane, T.; Tofail, S. A. M., Effective cancer theranostics with polymer encapsulated superparamagnetic nanoparticles: Combined effects of magnetic hyperthermia and controlled drug release. ACS Biomater. Sci. Eng. 2017,10.1021/acsbiomaterials.6b00420. (71) Uzunalli, G.; Mammadov, R.; Yesildal, F.; Alhan, D.; Ozturk, S.; Ozgurtas, T.; Guler, M. O.; Tekinay, A. B., Angiogenic heparinmimetic peptide nanofiber gel improves regenerative healing of acute wounds. ACS Biomater. Sci. Eng. 2017, 10.1021/acsbiomaterials.6b00165. (72) Lackington, W. A.; Ryan, A. J.; O’Brien, F. J., Advances in nerve guidance conduit-based therapeutics for peripheral nerve repair. ACS Biomater. Sci. Eng. 2017,10.1021/acsbiomaterials.6b00500. (73) Nakamura, N.; Kimura, T.; Kishida, A., Overview of the development, applications, and future perspectives of decellularized tissues and organs. ACS Biomater. Sci. Eng. 2017, 10.1021/ acsbiomaterials.6b00506. (74) Thomas, R. C.; Vu, P.; Modi, S. P.; Chung, P. E.; Landis, R. C.; Khaing, Z. Z.; Hardy, J. G.; Schmidt, C. E., Sacrificial crystal templated hyaluronic acid hydrogels as biomimetic 3D tissue scaffolds for nerve tissue regeneration. ACS Biomater. Sci. Eng. 2017, 10.1021/ acsbiomaterials.7b00002.

1174

DOI: 10.1021/acsbiomaterials.7b00372 ACS Biomater. Sci. Eng. 2017, 3, 1172−1174