Two-photon polymerization of hydrogels - versatile solutions to fabricate well-defined 3D structures

Hydrogels are cross-linked water-containing polymer networks that are formed by physical, ionic or covalent interactions. In recent years, they have attracted significant attention because of their unique physical properties, which make them promising materials for numerous applications in food and cosmetic processing, as well as in drug delivery and tissue engineering. Hydrogels are highly water-swellable materials, which can considerably increase in volume without losing cohesion, are biocompatible and possess excellent tissue-like physical properties, which can mimic in vivo conditions. When combined with highly precise manufacturing technologies, such as two-photon polymerization (2PP), well-defined three-dimensional structures can be obtained. These structures can become scaffolds for selective cell-entrapping, cell/drug delivery, sensing and prosthetic implants in regenerative medicine. 2PP has been distinguished from other rapid prototyping methods because it is a non-invasive and efficient approach for hydrogel cross-linking. This review discusses the 2PP-based fabrication of 3D hydrogel structures and their potential applications in biotechnology. A brief overview regarding the 2PP methodology and hydrogel properties relevant to biomedical applications is given together with a review of the most important recent achievements in the field.

[1]  U. Kandalam,et al.  Swelling, strength, and biocompatibility of acrylate-based superporous hydrogel hybrids , 2014 .

[2]  Wei He,et al.  A novel thermo-sensitive hydrogel based on thiolated chitosan/hydroxyapatite/beta-glycerophosphate. , 2014, Carbohydrate polymers.

[3]  T. Kasuga,et al.  Effective encapsulation of laccase in an aluminium silicate nanotube hydrogel , 2014 .

[4]  P. Campagnola,et al.  Freeform multiphoton excited microfabrication for biological applications using a rapid prototyping CAD-based approach. , 2006, Optics express.

[5]  R. Anderson,et al.  The optics of human skin. , 1981, The Journal of investigative dermatology.

[6]  J. Hubbell,et al.  Prevention of Postoperative Adhesions in the Rat by In Situ Photopolymerization of Bioresorbable Hydrogel Barriers , 1994, Obstetrics and gynecology.

[7]  Kytai Truong Nguyen,et al.  Photopolymerizable hydrogels for tissue engineering applications. , 2002, Biomaterials.

[8]  Jason B. Shear,et al.  Multiphoton Lithography of Unconstrained Three‐Dimensional Protein Microstructures , 2013 .

[9]  C. Bowman,et al.  Photopolymerization : fundamentals and applications , 1997 .

[10]  Wouter Olthuis,et al.  Hydrogel-based devices for biomedical applications , 2010 .

[11]  D. Stone,et al.  Stromal Melting Associated With a Cosmetic Contact Lens Over a Boston Keratoprosthesis: Treatment With a Conjunctival Flap , 2013, Eye & contact lens.

[12]  Boris N. Chichkov,et al.  Two Photon Polymerization of Polymer–Ceramic Hybrid Materials for Transdermal Drug Delivery , 2007 .

[13]  Jennifer L. West,et al.  Three-dimensional photolithographic patterning of multiple bioactive ligands in poly(ethylene glycol) hydrogels , 2010 .

[14]  Seth R. Marder,et al.  Photoresponsive Hydrogel Microstructure Fabricated by Two‐Photon Initiated Polymerization , 2002 .

[15]  C. Gonçalves,et al.  Self-Assembled Hydrogel Nanoparticles for Drug Delivery Applications , 2010, Materials.

[16]  Hyoungshin Park,et al.  Application of a dense gas technique for sterilizing soft biomaterials , 2011, Biotechnology and bioengineering.

[17]  Jason B Shear,et al.  Mask-directed multiphoton lithography. , 2007, Journal of the American Chemical Society.

[18]  F. J. Duarte,et al.  Coherence and Ultrashort Pulse Laser Emission , 2010 .

[19]  J. Plumb,et al.  A cisplatin slow-release hydrogel drug delivery system based on a formulation of the macrocycle cucurbit[7]uril, gelatin and polyvinyl alcohol. , 2014, Journal of inorganic biochemistry.

[20]  Aleksandr Ovsianikov,et al.  Photo-sensitive hydrogels for three-dimensional laser microfabrication in the presence of whole organisms , 2012, Journal of biomedical optics.

[21]  J. A. Hubbell,et al.  A new photopolymerizable blood vessel glue that seals human vessel anastomoses without augmenting thrombogenicity. , 1995, Plastic and reconstructive surgery.

[22]  Jiyuan Yang,et al.  Smart self-assembled hybrid hydrogel biomaterials. , 2012, Angewandte Chemie.

[23]  M. Kellomäki,et al.  Investigation of the optimal processing parameters for picosecond laser-induced microfabrication of a polymer–ceramic hybrid material , 2011 .

[24]  Aleksandr Ovsianikov,et al.  Laser photofabrication of cell-containing hydrogel constructs. , 2014, Langmuir : the ACS journal of surfaces and colloids.

[25]  R. Kopelman,et al.  Hydrogel Nanoparticles with Thermally Controlled Drug Release , 2014, ACS macro letters.

[26]  Jennifer L. West,et al.  Three‐Dimensional Biochemical and Biomechanical Patterning of Hydrogels for Guiding Cell Behavior , 2006 .

[27]  A. Ovsianikov,et al.  Three-Dimensional Microfabrication of Protein Hydrogels via Two-Photon-Excited Thiol-Vinyl Ester Photopolymerization , 2013 .

[28]  I. Kiviranta,et al.  Preparation and characterization of collagen/PLA, chitosan/PLA, and collagen/chitosan/PLA hybrid scaffolds for cartilage tissue engineering , 2014, Journal of Materials Science: Materials in Medicine.

[29]  Risto Penttinen,et al.  Extracellular Matrix Molecules: Potential Targets in Pharmacotherapy , 2009, Pharmacological Reviews.

[30]  Ajazuddin,et al.  Alginate based hydrogel as a potential biopolymeric carrier for drug delivery and cell delivery systems: present status and applications. , 2012, Current drug delivery.

[31]  K. Matyjaszewski,et al.  The development of microgels/nanogels for drug delivery applications , 2008 .

[32]  S. Goodman,et al.  3-Dimensional Submicron Polymerization of Acrylamide by Multiphoton Excitation of Xanthene Dyes , 2000 .

[33]  J. Hubbell,et al.  Efficacy of a resorbable hydrogel barrier, oxidized regenerated cellulose, and hyaluronic acid in the prevention of ovarian adhesions in a rabbit model. , 1994, Fertility and sterility.

[34]  D. Correa,et al.  Two-Photon Polymerization Fabrication of Doped Microstructures , 2012 .

[35]  T. O’Halloran,et al.  Emission ratiometric imaging of intracellular zinc: design of a benzoxazole fluorescent sensor and its application in two-photon microscopy. , 2004, Journal of the American Chemical Society.

[36]  Sabrina Schlie-Wolter,et al.  Hyaluronic acid based materials for scaffolding via two-photon polymerization. , 2014, Biomacromolecules.

[37]  T. Anirudhan,et al.  Novel pH switchable gelatin based hydrogel for the controlled delivery of the anti cancer drug 5-fluorouracil , 2014 .

[38]  J L West,et al.  Smooth muscle cell growth in photopolymerized hydrogels with cell adhesive and proteolytically degradable domains: synthetic ECM analogs for tissue engineering. , 2001, Biomaterials.

[39]  Cheng-Lun Tsai,et al.  Near-infrared Absorption Property of Biological Soft Tissue Constituents , 2001 .

[40]  Jason A Burdick,et al.  Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid. , 2011, Biomaterials.

[41]  L. Schaefer,et al.  Proteoglycans: from structural compounds to signaling molecules , 2009, Cell and Tissue Research.

[42]  K. Dušek,et al.  Transition in swollen polymer networks induced by intramolecular condensation , 1968 .

[43]  Alexander Kros,et al.  Photoresponsive hydrogels for biomedical applications. , 2011, Advanced drug delivery reviews.

[44]  Anthony Atala,et al.  Methods Of Tissue Engineering , 2006 .

[45]  Aleksandr Ovsianikov,et al.  Multiphoton microscopy of transdermal quantum dot delivery using two photon polymerization-fabricated polymer microneedles. , 2011, Faraday discussions.

[46]  P. Campagnola,et al.  Properties of crosslinked protein matrices for tissue engineering applications synthesized by multiphoton excitation. , 2004, Journal of biomedical materials research. Part A.

[47]  O. Soppera,et al.  Photopolymerization and photostructuring of molecularly imprinted polymers for sensor applications , 2012, 2012 IEEE Sensors.

[48]  Jenna A. Bilbrey,et al.  Advances in smart materials: Stimuli‐responsive hydrogel thin films , 2013 .

[49]  Paul J. Campagnola,et al.  Submicron Multiphoton Free-Form Fabrication of Proteins and Polymers: Studies of Reaction Efficiencies and Applications in Sustained Release , 2000 .

[50]  Fuyao Liu,et al.  Fabricating three-dimensional carbohydrate hydrogel microarray for lectin-mediated bacterium capturing. , 2014, Biosensors & bioelectronics.

[51]  B. Chichkov,et al.  Two photon induced polymerization of organic-inorganic hybrid biomaterials for microstructured medical devices. , 2006, Acta biomaterialia.

[52]  Qingquan Liu,et al.  Fabrication and Physical Properties of Gelatin/Sodium Alginate/Hyaluronic Acid Composite Wound Dressing Hydrogel , 2014 .

[53]  G. Pins,et al.  Multiphoton excited fabrication of collagen matrixes cross-linked by a modified benzophenone dimer: bioactivity and enzymatic degradation. , 2005, Biomacromolecules.

[54]  A. P. Serro,et al.  Comparison of two hydrogel formulations for drug release in ophthalmic lenses. , 2014, Journal of biomedical materials research. Part B, Applied biomaterials.

[55]  D. Mooney,et al.  Hydrogels for tissue engineering: scaffold design variables and applications. , 2003, Biomaterials.

[56]  Jenni E. Koskela,et al.  Two‐photon microfabrication of poly(ethylene glycol) diacrylate and a novel biodegradable photopolymer—comparison of processability for biomedical applications , 2012 .

[57]  J.-Y. Lin,et al.  Fabricating high-aspect-ratio sub-diffraction-limit structures on silicon with two-photon photopolymerization and reactive ion etching , 2004 .

[58]  A. Kasko,et al.  Two-photon lithography in the future of cell-based therapeutics and regenerative medicine: a review of techniques for hydrogel patterning and controlled release. , 2010, Future medicinal chemistry.

[59]  Taketoshi Fujimoto,et al.  Infrared studies of stereoregular polymerization of methyl methacrylate and methacrylonitrile by organometallic compounds , 1968 .

[60]  Guangming Chen,et al.  Novel Nanocomposite Hydrogels Consisting of Layered Double Hydroxide with Ultrahigh Tensibility and Hierarchical Porous Structure at Low Inorganic Content , 2014, Advanced materials.

[61]  Dogu Baran Aydogan,et al.  Direct laser writing of synthetic poly(amino acid) hydrogels and poly(ethylene glycol) diacrylates by two-photon polymerization. , 2014, Materials science & engineering. C, Materials for biological applications.

[62]  P Lenz,et al.  In vivo EXCITATION OF PHOTOSENSITIZERS BY INFRARED LIGHT , 1995, Photochemistry and photobiology.

[63]  Olivier De Wever,et al.  Stromal myofibroblasts are drivers of invasive cancer growth , 2008, International journal of cancer.

[64]  Niklas Pucher,et al.  A Straightforward Synthesis and Structure−Activity Relationship of Highly Efficient Initiators for Two-Photon Polymerization , 2013 .

[65]  Kristi S. Anseth,et al.  Photodegradable Hydrogels for Dynamic Tuning of Physical and Chemical Properties , 2009, Science.

[66]  R. Burghardt,et al.  Promoter methylation is associated with the age-dependent loss of N-cadherin in the rat kidney. , 2008, American journal of physiology. Renal physiology.

[67]  Justine J. Roberts,et al.  Comparison of photopolymerizable thiol-ene PEG and acrylate-based PEG hydrogels for cartilage development. , 2013, Biomaterials.

[68]  George Filippidis,et al.  Two-photon polymerization of an Eosin Y-sensitized acrylate composite , 2006 .

[69]  Jun Wang,et al.  New Photoactivators for Multiphoton Excited Three-dimensional Submicron Cross-linking of Proteins: Bovine Serum Albumin and Type 1 Collagen¶,† , 2002, Photochemistry and photobiology.

[70]  In Vivo Writing using Two-Photon-Polymerization , 2010 .

[71]  Aleksandr Ovsianikov,et al.  Laser Fabrication of 3D Gelatin Scaffolds for the Generation of Bioartificial Tissues , 2011, Materials.

[72]  Jason A. Burdick,et al.  Patterning hydrogels in three dimensions towards controlling cellular interactions , 2011 .

[73]  J. Zach Hilt,et al.  Hydrogel nanocomposites: a review of applications as remote controlled biomaterials , 2010 .

[74]  B. Tighe A Decade of Silicone Hydrogel Development: Surface Properties, Mechanical Properties, and Ocular Compatibility , 2013, Eye & contact lens.

[75]  Aleksandr Ovsianikov,et al.  Two‐photon polymerization technique for microfabrication of CAD‐designed 3D scaffolds from commercially available photosensitive materials , 2007, Journal of tissue engineering and regenerative medicine.

[76]  K Sternberg,et al.  Three-dimensional laser micro- and nano-structuring of acrylated poly(ethylene glycol) materials and evaluation of their cytoxicity for tissue engineering applications. , 2011, Acta biomaterialia.

[77]  Dongan Wang,et al.  Bioresponsive hydrogel scaffolding systems for 3D constructions in tissue engineering and regenerative medicine. , 2013, Nanomedicine.

[78]  Jinqing Wang,et al.  A Novel Wound Dressing Based on Ag/Graphene Polymer Hydrogel: Effectively Kill Bacteria and Accelerate Wound Healing , 2014 .

[79]  Peter Dubruel,et al.  A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. , 2012, Biomaterials.

[80]  R. Landers,et al.  Rapid prototyping of scaffolds derived from thermoreversible hydrogels and tailored for applications in tissue engineering. , 2002, Biomaterials.

[81]  Tatiana Segura,et al.  Design of cell-matrix interactions in hyaluronic acid hydrogel scaffolds. , 2014, Acta biomaterialia.

[82]  B N Chichkov,et al.  Femtosecond laser-induced two-photon polymerization of inorganic-organic hybrid materials for applications in photonics. , 2003, Optics letters.

[83]  S. Tretiak,et al.  Enhanced Two‐Photon Absorption of Organic Chromophores: Theoretical and Experimental Assessments , 2008 .

[84]  M. Alini,et al.  Degradation of synthetic polymeric scaffolds for bone and cartilage tissue repairs , 2009 .

[85]  O. Wichterle,et al.  Hydrophilic Gels for Biological Use , 1960, Nature.

[86]  C. Fotakis,et al.  Pico- and femtosecond laser-induced crosslinking of protein microstructures: evaluation of processability and bioactivity , 2011, Biofabrication.

[87]  Aleksandr Ovsianikov,et al.  Initiation efficiency and cytotoxicity of novel water-soluble two-photon photoinitiators for direct 3D microfabrication of hydrogels , 2013 .

[88]  Jeffrey A. Hubbell,et al.  Polymeric biomaterials with degradation sites for proteases involved in cell migration , 1999 .

[89]  Ali Khademhosseini,et al.  Microengineered hydrogels for tissue engineering. , 2007, Biomaterials.

[90]  Toru Takehisa,et al.  Nanocomposite Hydrogels: A Unique Organic–Inorganic Network Structure with Extraordinary Mechanical, Optical, and Swelling/De‐swelling Properties , 2002 .

[91]  Yuxia Zhao,et al.  Water-soluble benzylidene cyclopentanone dye for two-photon photopolymerization , 2009 .

[92]  L. Koch,et al.  Laser printing of cells into 3D scaffolds , 2010, Biofabrication.

[93]  W. Webb,et al.  Two-Photon Fluorescence Excitation Cross Sections of Biomolecular Probes from 690 to 960 nm. , 1998, Applied optics.

[94]  Bahaa E. A. Saleh,et al.  Acrylic-based resin with favorable properties for three-dimensional two-photon polymerization , 2004 .

[95]  Aleksandr Ovsianikov,et al.  Laser fabrication of three-dimensional CAD scaffolds from photosensitive gelatin for applications in tissue engineering. , 2011, Biomacromolecules.

[96]  Anil Kumar Bajpai,et al.  Responsive polymers in controlled drug delivery , 2008 .

[97]  Aleksandr Ovsianikov,et al.  Hydrogels for Two‐Photon Polymerization: A Toolbox for Mimicking the Extracellular Matrix , 2013 .

[98]  R. Marchant,et al.  Design properties of hydrogel tissue-engineering scaffolds , 2011, Expert review of medical devices.

[99]  Jennifer L. West,et al.  Three-dimensional micropatterning of bioactive hydrogels via two-photon laser scanning photolithography for guided 3D cell migration. , 2008, Biomaterials.

[100]  Jindřich Kopeček,et al.  The photoelastic behaviour of dry and swollen networks of poly (N,N-diethylacrylamide) and of its copolymer with N-tert.butylacrylamide , 1981 .

[101]  Maria Goeppert-Mayer Über Elementarakte mit zwei Quantensprüngen , 1931 .

[102]  Kristi S. Anseth,et al.  Cytocompatible Click-based Hydrogels with Dynamically-Tunable Properties Through Orthogonal Photoconjugation and Photocleavage Reactions , 2011, Nature chemistry.

[103]  Jean-Pierre Fouassier,et al.  Photoinitiation, photopolymerization, and photocuring , 1995 .

[104]  Toyoichi Tanaka Collapse of Gels and the Critical Endpoint , 1978 .

[105]  Jason B Shear,et al.  Guiding neuronal development with in situ microfabrication. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[106]  M. Shoichet,et al.  Tunable Growth Factor Delivery from Injectable Hydrogels for Tissue Engineering , 2011, Journal of the American Chemical Society.

[107]  Jason B Shear,et al.  Multiphoton fabrication of chemically responsive protein hydrogels for microactuation , 2008, Proceedings of the National Academy of Sciences.

[108]  Loon-Seng Tan,et al.  Direct three-dimensional microfabrication of hydrogels via two-photon lithography in aqueous solution. , 2009, Chemistry of materials : a publication of the American Chemical Society.

[109]  J. Kopeček Hydrogel biomaterials: a smart future? , 2007, Biomaterials.