Proteins are a class of biomaterials having a vast array of functions, including the catalysis of metabolic reactions, DNA replication, stimuli response and transportation of molecules. Recent progress in laser-based fabrication technologies has enabled the formation of three-dimensional (3D) proteinaceous micro- and nano-structures by femtosecond laser cross-linking, which has expanded the possible applications of proteins. This article reviews the current knowledge and recent advancements in the femtosecond laser cross-linking of proteins. An overview of previous studies related to fabrication using a variety of proteins and detailed discussions of the associated mechanisms are provided. In addition, advances and applications utilizing specific protein functions are introduced. This review thus provides a valuable summary of the 3D micro- and nano-fabrication of proteins for biological and medical applications.
[Opto-Electron Adv, 2018, 1(4)] Fabrication of three-dimensional proteinaceous micro- and nano-structures by femtosecond laser cross-linking
First published at:Mar 01, 2019
1. Maskarinec S A, Tirrell D A. Protein engineering approaches to biomaterials design. Curr Opin Biotechnol 16, 422–426 (2005).
2. Latour Jr R A. Biomaterials: protein–surface interactions. In Bowlin G L, Wnek G. Encyclopedia of Biomaterials and Bio-medical Engineering 270 (Marcel Dekker, 2013).
3. Ruel-Gariépy E, Leroux J C. In situ-forming hydrogels—review of temperature-sensitive systems. Eur J Pharm Biopharm 58, 409–426 (2004).
4. Teixeira L S M, Feijen J, van Blitterswijk C A, Dijkstra P J, Karperien M. Enzyme-catalyzed crosslinkable hydrogels: emerging strategies for tissue engineering. Biomaterials 33, 1281–1290 (2012).
5. Shen W, Lammertink R G H, Sakata J K, Kornfield J A, Tirrell D A. Assembly of an artificial protein hydrogel through leucine zipper aggregation and disulfide bond formation. Macromolecules 38, 3909–3916 (2005).
6. Williams R J, Hall T E, Glattauer V, White J, Pasic P J et al. The in vivo performance of an enzyme-assisted self-assembled peptide/protein hydrogel. Biomaterials 32, 5304–5310 (2011).
7. Zubtsov D A, Ivanov S M, Rubina A Y, Dementieva E I, Chechetkin V R et al. Effect of mixing on reaction–diffusion kinetics for protein hydrogel-based microchips. J Biotechnol 122, 16–27 (2006).
8. Wu J H, Li P F, Dong C L, Jiang H T, Xue B et al. Rationally designed synthetic protein hydrogels with predictable mechanical properties. Nat Commun 9, 620 (2018).
9. Elzoghby A O, Samy W M, Elgindy N A. Protein-based nanocarriers as promising drug and gene delivery systems. J Control Release 161, 38–49 (2012).
10. Kou S Z, Yang Z G, Sun F. Protein hydrogel microbeads for selective uranium mining from seawater. ACS Appl Mater In-terfaces 9, 2035–2039 (2017).
11. Onoe H, Okitsu T, Itou A, Kato-Negishi M, Gojo R et al. Me-tre-long cell-laden microfibres exhibit tissue morphologies and functions. Nat Mater 12, 584–590 (2013).
12. Hsiao A Y, Okitsu T, Onoe H, Kiyosawa M, Teramae H et al. Smooth muscle-like tissue constructs with circumferentially oriented cells formed by the cell fiber technology. PLoS One 10, e0119010 (2015).
13. Kato-Negishi M, Onoe H, Ito A, Takeuchi S. Rod-shaped neural units for aligned 3D neural network connection. Adv Healthc Mater 6, 1700143 (2017).
14. Bahukudumbi P, Carson K H, Rice-Ficht A C, Andrews M J. On the diameter and size distributions of bovine serum albumin (BSA)-based microspheres. J Microencapsul 21, 787–803 (2004).
15. Suslick K S, Grinstaff M W, Kolbeck K J, Wong M. Characterization of sonochemically prepared proteinaceous microspheres. Ultrason Sonochem 1, S65-S68 (1994).
16. Silva R, Ferreira H, Vasconcelos A, Gomes A C, Cavaco-Paulo A. Sonochemical proteinaceous microspheres for wound healing. In Zahavy E, Ordentlich A, Yitzhaki S, Shafferman A. Nano-Biotechnology for Biomedical and Diagnostic Research 733 (Springer, 2012).
17. Forsberg F, Goldberg B B, Liu J B, Merton D A, Rawool N M. On the feasibility of real-time, in vivo harmonic imaging with proteinaceous microspheres. Ultrasound 15, 853–860 (1996).
18. Boland T, Xu T, Damon B, Cui X F. Application of inkjet printing to tissue engineering. Biotechnol J 1, 910–917 (2006).
19. Roth E A, Xu T, Das M, Gregory C, Hickman J J et al. Inkjet printing for high-throughput cell patterning. Biomaterials 25, 3707–3715 (2004).
20. Geckil H, Xu F, Zhang X H, Moon S J, Utkan D. Engineering hydrogels as extracellular matrix mimics. Nanomedicine 5, 469–484 (2010).
21. Kang H W, Lee S J, Ko I K, Kengla C, Yoo J J et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol 34, 312–319 (2016).
22. Delaporte P, Alloncle A P. Laser-induced forward transfer: a high resolution additive manufacturing technology. Opt Laser Technol 78, 33–41 (2016).
23. Zergioti I, Karaiskou A, Papazoglou D G, Fotakis C, Kapsetaki M et al. Femtosecond laser microprinting of biomaterials. Appl Phys Lett 86, 163902 (2005).
24. Hopp B, Smausz T, Kresz N, Barna N, Bor Z et al. Survival and proliferative ability of various living cell types after la-ser-induced forward transfer. Tissue Eng 11, 1817–1823 (2005).
25. Kattamis N T, Purnick P E, Weiss R, Arnold C B. Thick film laser induced forward transfer for deposition of thermally and mechanically sensitive materials. Appl Phys Lett 91, 171120 (2007).
26. Spikes J D, Shen H R, Kopečková P, Kopeček J. Photodynamic crosslinking of proteins. III. Kinetics of the FMN-and rose Bengal-sensitized photooxidation and intermolecular crosslinking of model tyrosine-containing N-(2-hydroxypropyl) methacrylamide copolymers. Photochem Photobiol 70, 130–137 (1999).
27. Moss T, Dimitrov S I, Houde D. UV-laser crosslinking of pro-teins to DNA. Methods 11, 225–234 (1997).
28. Gebicki S, Gebicki J M. Crosslinking of DNA and proteins induced by protein hydroperoxides. Biochem J 338, 629–636 (1999).
29. Sugioka K, Cheng Y. Ultrafast lasers—reliable tools for ad-vanced materials processing. Light Sci Appl 3, e149 (2014).
30. Sugioka K, Cheng Y. Femtosecond laser three-dimensional micro- and nanofabrication. Appl Phys Rev 1, 041303 (2014).
31. Fischer J, Wegener M. Three-dimensional optical laser lithography beyond the diffraction limit. Laser Photon Rev 7, 22–44 (2013).
32. Pitts J D, Campagnola P J, Epling G A, Goodman S L. Submicron multiphoton free-form fabrication of proteins and polymers: studies of reaction efficiencies and applications in sustained release. Macromolecules 33, 1514–1523 (2000).
33. Serien D, Takeuchi S. Fabrication of submicron proteinaceous structures by direct laser writing. Appl Phys Lett 107, 013702 (2015).
34. Spivey E C, Ritschdorff E T, Connell J L, McLennon C A, Schmidt C E et al. Multiphoton lithography of unconstrained three-dimensional protein microstructures. Adv Func Mater 23, 333–339 (2013).
35. Lin C L, Pan M J, Chen H W, Lin C K, Lin C F et al. Laser cross-linking protein captures for living cells on a biochip. Proc SPIE 9310, 93100D (2015).
36. Iosin M, Scheul T, Nizak C, Stephan O, Astilean S et al. Laser microstructuration of three-dimensional enzyme reactors in microfluidic channels. Microfluid Nanofluid 10, 685–690 (2011).
37. Serien D, Kawano H, Miyawaki A, Midorikawa K, Sugioka K. Femtosecond laser direct write integration of multi-protein patterns and 3D microstructures into 3D glass microfluidic devices. Appl Sci 8, 147 (2018).
38. Basu S, Campagnola P J. Enzymatic activity of alkaline phosphatase inside protein and polymer structures fabricated via multiphoton excitation. Biomacromolecules 5, 572–579 (2004).
39. Kaehr B, Shear J B. Multiphoton fabrication of chemically responsive protein hydrogels for microactuation. Proc Natl Acad Sci USA 105, 8850–8854 (2008).
40. Lee M R, Phang I Y, Cui Y, Lee Y H, Ling X Y. Shape-shifting 3D protein microstructures with programmable directionality via quantitative nanoscale stiffness modulation. Small 11, 740–748 (2015).
41. Sun Y L, Dong W F, Niu L G, Jiang T, Liu D X et al. Pro-tein-based soft micro-optics fabricated by femtosecond laser direct writing. Light Sci Appl 3, e129 (2014).
42. Sun S M, Sun Y L, Zheng B Y, Wang P, Hou Z S et al. Pro-tein-based Y-junction optical micro-splitters with environ-ment-stimulus-actuated adjustments. Sens Actuators B Chem 232, 571–576 (2016).
43. Serien D, Takeuchi S. Multi-Component microscaffold with 3D spatially defined proteinaceous environment. ACS Biomater Sci Eng 3, 487–494 (2017).
44. Engelhardt S, Hoch E, Borchers K, Meyer W, Krüger H et al. Fabrication of 2D protein microstructures and 3D poly-mer–protein hybrid microstructures by two-photon polymerization. Biofabrication 3, 025003 (2011).
45. Khripin C Y, Brinker C J, Kaehr B. Mechanically tunable multiphoton fabricated protein hydrogels investigated using atomic force microscopy. Soft Matter 6, 2842–2848 (2010).
46. Hill R T, Lyon J L, Allen R, Stevenson K J, Shear J B. Microfabrication of three-dimensional bioelectronic architec-tures. J Am Chem Soc 127, 10707–10711 (2005).
47. Connell J L, Ritschdorff E T, Shear J B. Three-dimensional printing of photoresponsive biomaterials for control of bacterial microenvironments. Anal Chem 88, 12264–12271 (2016).
48. Turunen S, Käpylä E, Terzaki K, Viitanen J, Fotakis C et al. Pico- and femtosecond laser-induced crosslinking of protein microstructures: evaluation of processability and bioactivity. Biofabrication 3, 045002 (2011).
49. Kaehr B, Ertas N, Nielson R, Allen R, Hill R T et al. Direct-write fabrication of functional protein matrixes using a low-cost Q-switched laser. Anal Chem 78, 3198–3202 (2006).
50. Iosin M, Stephan O, Astilean S, Duperray A, Baldeck P. Microstructuration of protein matrices by laser-induced photochemistry. J Optoelectron Adv M 9, 716–720 (2007).
51. Basu S, Wolgemuth C W, Campagnola P J. Measurement of normal and anomalous diffusion of dyes within protein struc-tures fabricated via multiphoton excited cross-linking. Biomacromolecules 5, 2347–2357 (2004).
52. Basu S, Cunningham L P, Pins G D, Bush K A, Taboada R et al. Multiphoton excited fabrication of collagen matrixes cross-linked by a modified benzophenone dimer: bioactivity and enzymatic degradation. Biomacromolecules 6, 1465–1474 (2005).
53. Sun Y L, Hou Z S, Sun S M, Zheng B Y, Ku J F et al. Pro-tein-based three-dimensional whispering-gallery-mode mi-cro-lasers with stimulus-responsiveness. Sci Rep 5, 12852 (2015).
54. Lawson J L, Jenness N, Wilson S, Clark R L. Method of creating microscale prototypes using SLM based holographic lithography. Proc SPIE 8612, 86120L (2013).
55. Sun Y L, Dong W F, Yang R Z, Meng X, Zhang L et al. Dynamically tunable protein microlenses. Angew Chem Int Ed 51, 1558–1562 (2012).
56. Kaehr B, Allen R, Javier D J, Currie J, Shear J B. Guiding neuronal development with in situ microfabrication. Proc Natl Acad Sci USA 101, 16104–16108 (2004).
57. Harper J C, Brozik S M, Brinker C J, Kaehr B. Biocompatible microfabrication of 3D isolation chambers for targeted con-finement of individual cells and their progeny. Anal Chem 84, 8985–8989 (2012).
58. Nielson R, Kaehr B, Shear J B. Microreplication and design of biological architectures using dynamic-mask multiphoton lithography. Small 5, 120–125 (2009).
59. Da Sie Y, Li Y C, Chang N S, Campagnola P J, Chen S J. Fabrication of three-dimensional multi-protein microstructures for cell migration and adhesion enhancement. Biomed Opt Express 6, 480–490 (2015).
60. Ritschdorff E T, Nielson R, Shear J B. Multi-focal multiphoton lithography. Lab Chip 12, 867–871 (2012).
61. Allen R, Nielson R, Wise D D, Shear J B. Catalytic three-dimensional protein architectures. Anal Chem 77, 5089–5095 (2005).
62. Lay C L, Lee M R, Lee H K, Phang I Y, Ling X Y. Transformative two-dimensional array configurations by geometrical shape-shifting protein microstructures. ACS Nano 9, 9708–9717 (2015).
63. Lay C L, Lee Y H, Lee M R, Phang I Y, Ling X Y. Formulating an ideal protein photoresist for fabricating dynamic microstructures with high aspect ratios and uniform responsiveness. ACS Appli Mater Interfaces 8, 8145–8153 (2016).
64. Hernandez D S, Ritschdorff E T, Seidlits S K, Schmidt C E, Shear J B. Functionalizing micro-3D-printed protein hydrogels for cell adhesion and patterning. J Mater Chem B 4, 1818–1826 (2016).
65. Jenness N J, Hill R T, Hucknall A, Chilkoti A, Clark R L. A versatile diffractive maskless lithography for single-shot and serial microfabrication. Opt Express 18, 11754–11762 (2010).
66. Serien D, Takeuchi S. Two-Photon direct laser writing for proteinaceous microstructures with additional sensitizer. J Laser Micro/Nanoeng 12, 80–85 (2017).
67. Bell A, Kofron M, Nistor V. Multiphoton crosslinking for bio-compatible 3D printing of type I collagen. Biofabrication 7, 035007 (2015).
68. Lyon J L, Hill R T, Shear J B, Stevenson K J. Direct electro-chemical and spectroscopic assessment of heme integrity in multiphoton photo-cross-linked cytochrome c structures. Anal Chem 79, 2303–2311 (2007).
69. Basu S, Campagnola P J. Properties of crosslinked protein matrices for tissue engineering applications synthesized by multiphoton excitation. J Biomed Mater Res A 71A, 359–368 (2004).
70. Sun Y L, Li Q, Sun S M, Huang J C, Zheng B Y et al. Aqueous multiphoton lithography with multifunctional silk-centred bio-resists. Nat Commun 6, 8612 (2015).
71. Vagenende V, Yap M G S, Trout B L. Mechanisms of protein stabilization and prevention of protein aggregation by glycerol. Biochemistry 48, 11084–11096 (2009).
72. Hand D B. The refractivity of protein solutions. J Biol Chem 108, 703–707 (1935).
73. Burley S K, Berman H M, Christie C, Duarte J M, Feng Z et al. RCSB Protein Data Bank: Sustaining a living digital data resource that enables breakthroughs in scientific research and biomedical education. Protein Sci 27, 316-330 (2018).
74. Livingstone C D, Barton G J. Protein sequence alignments: a strategy for the hierarchical analysis of residue conservation. Bioinformatics 9, 745–756 (1993).
75. Eitner K, Koch U, Gawęda T, Marciniak J. Statistical distribution of amino acid sequences: a proof of Darwinian evolution. Bioinformatics 26, 2933–2935 (2010).
76. Peters T. Serum albumin. Adv Clin Chem 13, 37–111 (1970).
77. Yu T, Ober C K, Kuebler S M, Zhou W, Marder S R et al. Chemically amplified positive resists for two-photon three-dimensional microfabrication. Adv Mater 15, 517–521 (2003).
78. Coenjarts C A, Ober C K. Two-photon three-dimensional microfabrication of poly(dimethylsiloxane) elastomers. Chem Mater 16, 5556–5558 (2004).
79. Oster G. Dye-sensitized photopolymerization. Nature 173, 300–301 (1954).
80. Dubbelman T M A R, De Goeij A F P M, Van Steveninck J. Protoporphyrin-induced photodynamic effects on transport processes across the membrane of human erythrocytes. Biochim Biophys Acta Biomembr 595, 133–139 (1980).
81. Shen H R, Spikes J D, Kopečková P, Kopeček J. Photodynamic crosslinking of proteins II. Photocrosslinking of a model protein-ribonuclease A. J Photochem Photobiol B 35, 213–219 (1996).
82. Requejo R, Hurd T R, Costa N J, Murphy M P. Cysteine residues exposed on protein surfaces are the dominant intramitochondrial thiol and may protect against oxidative damage. FEBS J 277, 1465–1480 (2010).
83. Sackmann E K, Fulton A L, Beebe D J. The present and future role of microfluidics in biomedical research. Nature 507, 181–189 (2014).
84. Huh D, Torisawa Y S, Hamilton G A, Kim H J, Ingber D E. Microengineered physiological biomimicry: organs-on-Chips. Lab Chip 12, 2156–2164 (2012).
85. Fan X D, White I M. Optofluidic microsystems for chemical and biological analysis. Nat Photonics 5, 591–597 (2011).
86. Wu D, Wu S Z, Xu J, Niu L G, Midorikawa K et al. Hybrid femtosecond laser microfabrication to achieve true 3D glass/polymer composite biochips with multiscale features and high performance: the concept of ship-in-a-bottle biochip. Laser Photon Rev 8, 458–467 (2014).
RIKEN SPDR program,The Amada Foundation Research Grant (Jyuten-Kenkyu-Kaihatsu-Josei A)
Get Citation: Serien D, Sugioka K. Fabrication of three-dimensional proteinaceous micro- and nano-structures by femtosecond laser cross-linking[J]. Opto-Electronic Advances, 2018, 1(4): 180008.
Previous: [Opto-Electron Adv, 2018, 1(4)] Scanning cathodoluminescence microscopy: applications in semiconductor and metallic nanostructures
Optics & Laser Technology, 2019
Pure proteinaceous high-aspect-ratio microstructures made by femtosecond laser multiphoton cross-linking
Microfluidics, BioMEMS, and Medical, 2019
Applied Physics Reviews, 2019
Laser-induced Microplasma as Effective Tool for Phase Elements Fabrication on Amorphous and Crystalline Materials
JLMN-Journal of Laser Micro/Nanoengineering, 2018