Materials and surface engineering to control bacterial adhesion and biofilm formation: A review of recent advances

Springer Science and Business Media LLC - Tập 8 - Trang 20-33 - 2014
Huan Gu1, Dacheng Ren1,2
1Department of Biomedical and Chemical Engineering, Syracuse Biomaterials Institute, Syracuse University, Syracuse, USA
2Department of Civil and Environmental Engineering, Department of Biology, Syracuse University, Syracuse, USA

Tóm tắt

Bacterial adhesion to surfaces and subsequent biofilm formation are a leading cause of chronic infections and biofouling. These processes are highly sensitive to environmental factors and present a challenge to research using traditional approaches with uncontrolled surfaces. Recent advances in materials research and surface engineering have brought exciting opportunities to pattern bacterial cell clusters and to obtain synthetic biofilms with well-controlled cell density and morphology of cell clusters. In this article, we will review the recent achievements in this field and comment on the future directions.

Tài liệu tham khảo

Donlan R M. Biofilm formation: A clinically relevant microbiological process. Clinical Infectious Diseases, 2001, 33(8): 1387–1392 Walker J, Surman S, Jass J. Industrial Biofouling: Detection, Prevention and Control. Wiley, 2000: 1–12 Banerjee I, Pangule R C, Kane R S. Antifouling coatings: Recent developments in the des-ign of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Advanced Materials, 2011, 23(6): 690–718 Davey M E, O’Toole G A. Microbial biofilms: From ecology to molecular genetics. Microbiology and Molecular Biology Reviews, 2000, 64(4): 847–867 Donlan R M. Biofilms: Microbial life on surfaces. Emerging Infectious Diseases, 2002, 8(9): 881–890 Dunne W M. Bacterial adhesion: Seen any good biofilms lately? Clinical Microbiology Reviews, 2002, 15(2): 155–166 Stoodley P, Sauer K, Davies D G, Costerton J W. Biofilms as complex differentiated communities. Annual Review of Microbiology, 2002, 56(1): 187–209 Van Houdt R, Michiels C W. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Research in Microbiology, 2005, 156(5–6): 626–633 Bullitt E, Makowski L. Structural polymorphism of bacterial adhesion pili. Nature, 1995, 373(6510): 164–167 Thomas W E, Nilsson L M, Forero M, Sokurenko E V, Vogel V. Shear-dependent “stick-and-roll” adhesion of type 1 fimbriated Escherichia coli. Molecular Microbiology, 2004, 53(5): 1545–1557 Karatan E, Watnick P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiology and Molecular Biology Reviews, 2009, 73(2): 310–347 Palmer J, Flint S, Brooks J. Bacterial cell attachment, the beginning of a biofilm. Journal of Industrial Microbiology & Biotechnology, 2007, 34(9): 577–588 Marshall K C, Stout R, Mitchell R. Mechanisms of the initial events in the absorption of marine bacteria to surfaces. Journal of General Microbiology, 1971, 68(3): 337–348 Das T, Manefield M. Pyocyanin promotes extracellular DNA release in Pseudomonas aeruginosa. PLoS ONE, 2012, 7(10): e46718 Renner L D, Weibel D B. Physicochemical regulation of biofilm formation. MRS bulletin/Materials Research Society, 2011, 36(5): 347–355 Harmsen M, Yang L, Pamp S J, Tolker-Nielsen T. An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunology and Medical Microbiology, 2010, 59(3): 253–268 Jayaraman A, Wood T K. Bacterial quorum sensing: Signals, circuits, and implications for biofilms and disease. Annual Review of Biomedical Engineering, 2008, 10(1): 145–167 Ma L, Conover M, Lu H, Parsek M R, Bayles K, Wozniak D J. Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathogens, 2009, 5(3): e1000354 Ryu J H, Beuchat L R. Biofilm formation by Escherichia coli O157:H7 on stainless steel: Effect of exopolysaccharide and curli production on its resistance to chlorine. Applied and Environmental Microbiology, 2005, 71(1): 247–254 Prigent-Combaret C, Prensier G, Le Thi T T, Vidal O, Lejeune P, Dorel C. Developmental pathway for biofilm formation in curliproducing Escherichia coli strains:Rrole of flagella, curli and colanic acid. Environmental Microbiology, 2000, 2(4): 450–464 Hammer B K, Bassler B L. Quorum sensing controls biofilm formation in Vibrio cholerae. Molecular Microbiology, 2003, 50(1): 101–104 Tischler A D, Camilli A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Molecular Microbiology, 2004, 53(3): 857–869 Berk V, Fong J C N, Dempsey G T, Develioglu O N, Zhuang X, Liphardt J, Yildiz F H, Chu S. Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science, 2012, 337(6091): 236–239 Banin E, Vasil M L, Greenberg E P. Iron and Pseudomonas aeruginosa biofilm formation. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(31): 11076–11081 Barrio A F G, Zuo R, Hashimoto Y, Yang L, Bentley W E, Wood T K. Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). Journal of Bacteriology, 2006, 188(1): 305–316 Wang X, Preston J F, Romeo T. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. Journal of Bacteriology, 2004, 186(9): 2724–2734 Jackson D W, Suzuki K, Oakford L, Simecka J W, Hart M E, Romeo T. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. Journal of Bacteriology, 2002, 184(1): 290–301 Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades J R. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. Journal of Bacteriology, 2001, 183(9): 2888–2896 Pierce C G, Uppuluri P, Lopez-Ribot J L. A method for the formation of Candida biofilms in 96 well microtiter plates and its application to antifungal susceptibility testing. In: Gupta V K, Tuohy M G, Ayyachamy M A, et al., eds. Laboratory Protocols in Fungal Biology. Berlin: Springer, 2013, 217–223 Ghigo J M. Natural conjugative plasmids induce bacterial biofilm development. Nature, 2001, 412(6845): 442–445 Pratt L A, Kolter R. Genetic analysis of Escherichia coli biofilm formation: Roles of flagella, motility, chemotaxis and type I pili. Molecular Microbiology, 1998, 30(2): 285–293 Klausen M, Heydorn A, Ragas P, Lambersten L, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Molecular Microbiology, 2003, 48(6): 1511–1524 Whitchurch C B, Tolker-Nielsen T, Ragas P C, Mattick J S. Extracellular DNA required for bacterial biofilm formation. Science, 2002, 295(5559): 1487 An Y H, Friedman R J. An Y H, Friedman R J. Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. Journal of Biomedical Materials Research, 1998, 43(3): 338–348 MacKintosh E E, Patel J D, Marchant R E, Anderson J M. Effects of biomaterial surface chemistry on the adhesion and biofilm formation of Staphylococcus epidermidis in vitro. Journal of Biomedical Materials Research. Part A, 2006, 78(4): 836–842 Agladze K, Wang X, Romeo T. Spatial periodicity of Escherichia coli K12 biofilm microstructure initiates during a reversible, polar attachment phase of development and requires the polysaccharide adhesin PGA. Journal of Bacteriology, 2005, 187(24): 8237–8246 Wimpenny J, Manz W, Szewzyk U. Heterogeneity in biofilms. FEMS Microbiology Reviews, 2000, 24(5): 661–671 Stewart P S, Franklin M J. Physiological heterogeneity in biofilms. Nature Reviews. Microbiology, 2008, 6(3): 199–210 Weibel D B, Diluzio W R, Whitesides G M. Microfabrication meets microbiology. Nature Reviews. Microbiology, 2007, 5(3): 209–218 O’Toole G A, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Molecular Microbiology, 1998, 30(2): 295–304 Heydorn A, Ersboll B, Kato J, Hentzer M, Parsek M R, Tolker-Nielsen T, Givskov M, Molin S. Statistical analysis of Pseudomonas aeruginosa biofilm development: Impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Applied and Environmental Microbiology, 2002, 68(4): 2008–2017 Reisner A, Haagensen J A, Schembri M A, Zechner E L, Molin S. Development and maturation of Escherichia coli K-12 biofilms. Molecular Microbiology, 2003, 48(4): 933–946 Corona-Izquierdo F P, Membrillo-Hernandez J. A mutation in rpoS enhances biofilm formation in Escherichia coli during exponential phase of growth. FEMS Microbiology Letters, 2002, 211(1): 105–110 Schembri M A, Kjaergaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Molecular Microbiology, 2003, 48(1): 253–267 Ling H, Kang A, Tan M H, Qi X, Chang M W. The absence of the luxS gene increases swimming motility and flagella synthesis in Escherichia coli K12. Biochemical and Biophysical Research Communications, 2010, 401(4): 521–526 Davies D G, Parsek M R, Pearson J P, Iglewski B H, Costerton J W, Greenberg E P. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 1998, 280(5361): 295–298 Baca H K, Ashley C, Carnes E, Lopez D, Flemming J, Dunphy D, Singh S, Chen Z, Liu N, Fan H, Lopez G P, Brozik S M, Werner-Washburne M, Brinker C J. Cell-directed assembly of lipid-silica nanostructures providing extended cell viability. Science, 2006, 313(5785): 337–341 Harper J C, Khirpin C Y, Carnes E C, Ashley C E, Lopez D M, Savage T, Jones H D T, Davis R W, Nunez D E, Brinker L M, Kaehr B, Brozik S M, Brinker C J. Cell-directed integration into three-dimensional lipid-silica nanostructured matrices. ACS Nano, 2010, 4(10): 5539–5550 Lu Y F, Fan H Y, Stump A, Ward T L, Rieker T, Brinker C J. Aerosol-assisted self-assembly of mesostructured spherical nanoparticles. Nature, 1999, 398(6724): 223–226 Carnes E C, Lopez D M, Donegan N P, Cheung A, Gresham H, Timmins G S, Brinker J. Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nature Chemical Biology, 2010, 6(1): 41–45 Wessel A K, Hmelo L, Parsek M R, Whiteley M. Going local: Technologies for exploring bacterial microenvironments. Nature Reviews. Microbiology, 2013, 11(5): 337–348 Falconnet D, Csucs G, Grandin H M, Textor M. Surface engineering approaches to micropattern surfaces for cell-based assays. Biomaterials, 2006, 27(16): 3044–3063 Leong K, Boardman A K, Ma H, Jen A K. Single-cell patterning and adhesion on chemically engineered poly(dimethylsiloxane) surface. Langmuir, 2009, 25(8): 4615–4620 Takeuchi S, DiLuzio W R, Weibel D B, Whitesides G M. Controlling the shape of filamentous cells of Escherichia coli. Nano Letters, 2005, 5(9): 1819–1823 Hochbaum A I, Aizenberg J. Bacteria pattern spontaneously on periodic nanostructure arrays. Nano Letters, 2010, 10(9): 3717–3721 Kim S H, Yamamoto T, Fourmy D, Fujii T. An electroactive microwell array for trapping and lysing single-bacterial cells. Biomicrofluidics, 2011, 5(2): 024114–024117 Rettig J R, Folch A. Large-scale single-cell trapping and imaging using microwell arrays. Analytical Chemistry, 2005, 77(17): 5628–5634 Lovchik R, Von Arx C, Viviani A, Delamarche E. Cellular microarrays for use with capillary-driven microfluidics. Analytical and Bioanalytical Chemistry, 2008, 390(3): 801–808 Di Carlo D, Aghdam N, Lee L P. Single-cell enzyme concentrations, kinetics, and inhibition analysis using high-density hydrodynamic cell isolation arrays. Analytical Chemistry, 2006, 78(14): 4925–4930 Probst C, Grunberger A, Wiechert W, Kohlheyer D. Polydimethylsiloxane (PDMS) sub-micron traps for single-cell analysis of bacteria. Micromachines, 2013, 4(4): 357–369 Balaban N Q, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science, 2004, 305(5690): 1622–1625 Boedicker J Q, Vincent M E, Ismagilov R F. Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angewandte Chemie International Edition, 2009, 48(32): 5908–5911 Churski K, Kaminski T S, Jakiela S, Kamysz W, Baranska-Rybak W, Weibel D B, Garstecki P. Rapid screening of antibiotic toxicity in an automated microdroplet system. Lab on a Chip, 2012, 12(9): 1629–1637 Schmitz C H, Rowat A C, Koster S, Weitz D A. Dropspots: A picoliter array in a microfluidic device. Lab on a Chip, 2009, 9(1): 44–49 Leung K, Zahn H, Leaver T, Konwar K M, Hanson N W, Page A P, Lo C C, Chain P S, Hallam S J, Hansen C L. A programmable droplet-based microfluidic device applied to multiparameter analysis of single microbes and microbial communities. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(20): 7665–7670 Bai Y P, Patil S N, Bowden S D, Poulter S, Pan J, Salmond G P C, Welch M, Huck W T S, Abell C. Intra-species bacterial quorum sensing studied at single cell level in a double droplet trapping system. International Journal of Molecular Sciences, 2013, 14(5): 10570–10581 Kim J H, Lee D Y, Hwang J, Jung H I. Direct pattern formation of bacterial cells using micro-droplets generated by electrohydrodynamic forces. Microfluid Nanofluid, 2009, 7(6): 829–839 Eun Y J, Utada A S, Copeland M F, Takeuchi S, Weibel D B. Encapsulating bacteria in agarose microparticles using microfluidics for high-throughput cell analysis and isolation. ACS Chemical Biology, 2011, 6(3): 260–266 Voskerician G, Shive M S, Shawgo R S, Von Recum H, Anderson J M, Cima M J, Langer R. Biocompatibility and biofouling of MEMS drug delivery devices. Biomaterials, 2003, 24(11): 1959–1967 Song H, Ismagilov R F. Millisecond kinetics on a microfluidic chip using nanoliters of reagents. Journal of the American Chemical Society, 2003, 125(47): 14613–14619 Thorsen T, Roberts R W, Arnold F H, Quake S R. Dynamic pattern formation in a vesicle-generating microfluidic device. Physical Review Letters, 2001, 86(18): 4163–4166 Baret J C, Miler O J, Taly V, Ryckelynck M, El-Harrak A, Frenz L, Rick C, Samuels M L, Hutchison J B, Agresti J J, Link D R, Weitz D A, Griffiths A D. Fluorescence-activated droplet sorting (FADS): Efficient microfluidic cell sorting based on enzymatic activity. Lab on a Chip, 2009, 9(13): 1850–1858 Ahn K, Kerbage C, Hunt T P, Westervelt R M, Link D R, Weitz D A. Dielectrophoretic manipulation of drops for high-speed microfluidic sorting devices. Applied Physics Letters, 2006, 88(2): 024104-1–024104-3 Zeng Y, Novak R, Shuga J, Smith M T, Mathies R A. High-performance single cell genetic analysis using microfluidic emulsion generator arrays. Analytical Chemistry, 2010, 82(8): 3183–3190 Weibel D B, Lee A, Mayer M, Brady S F, Bruzewicz D, Yang J, Diluzio W R, Clardy J, Whitesides G M. Whitesides. Bacterial printing press that regenerates its ink: Contact-printing bacteria using hydrogel stamps. Langmuir, 2005, 21(14): 6436–6442 Yamazoe H, Tanabe T. Cell micropatterning on an albumin-based substrate using an inkjet printing technique. Journal of Biomedical Materials Research. Part A, 2009, 91(4): 1202–1209 Merrin J, Leibler S, Chuang J S. Printing multistrain bacterial patterns with a piezoelectric inkjet printer. PLoS One, 2007, 2(7): e663-1–e663-7 Liberski A R, Delaney J T, Schuber U S. “One cell-one well”: A new approach to inkjet printing single cell microarrays. ACS Combinatorial Science, 2011, 13(2): 190–195 Choi W S, Ha D, Park S, Kim T. Synthetic multicellular cell-to-cell communication in inkjet printed bacterial cell systems. Biomaterials, 2011, 32(10): 2500–2507 Kaehr B, Shear J B. Mask-directed multiphoton lithography. Journal of the American Chemical Society, 2007, 129(7): 1904–1905 Connell J L, Wessel A K, Parsek M R, Ellington A D, Whiteley M, Shear J B. Probing prokaryotic social behaviors with bacterial “lobster traps”. mBio, 2010, 1(4): e00202–00210 Connell J L, Ritschdorff E T, Whiteley M, Shear J B. 3D printing of microscopic bacterial communities. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(46): 18380–18385 Flickinger S T, Copeland M F, Downes E M, Braasch A T, Tuson H H, Eun Y J, Weibel D B. Quorum sensing between Pseudomonas aeruginosa biofilms accelerates cell growth. Journal of the American Chemical Society, 2011, 133(15): 5966–5975 Timp W, Mirsaidov U, Matsudaira P, Timp G. Jamming prokaryotic cell-to-cell communications in a model biofilm. Lab on a Chip, 2009, 9(7): 925–934 Meyer A, Megerle J A, Kuttler C, Muler J, Aguilar C, Eber L, Hense B A, Radler J O. Dynamics of AHL mediated quorum sensing under flow and non-flow conditions. Physical Biology, 2012, 9(2): 026007–026010 Hill R T, Lyon J L, Allen R, Stevenson K J, Shear J B. Microfabrication of three-dimensional bioelectronic architectures. Journal of the American Chemical Society, 2005, 127(30): 10707–10711 Kaehr B, Allen R, Javier D J, Currie J, Shear J B. Guiding neuronal development with in situ microfabrication. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(46): 16104–16108 Kaehr B, Shear J B. Multiphoton fabrication of chemically responsive protein hydrogels for microactuation. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(26): 8850–8854 Mashburn L M, Jett A M, Akins D R, Whiteley M. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. Journal of Bacteriology, 2005, 187(2): 554–566 Dilanji G E, Langebrake J B, Leenheer P D, Hagen S J. Quorum activation at a distance: Spatiotemporal patterns of gene regulation from diffusion of an autoinducer signal. Journal of the American Chemical Society, 2012, 134(12): 5618–5626 Quist A P, Pavlovic E, Oscarsson S. Recent advances in microcontact printing. Analytical and Bioanalytical Chemistry, 2005, 381(3): 591–600 Sgarbi N, Pisignano D, Di Benedetto F, Gigli G, Cingolani R, Rinaldi R. Self-assembled extracellular matrix protein networks by microcontact printing. Biomaterials, 2004, 25(7–8): 1349–1353 Hou S, Burton E A, Simon K A, Blodgett D, Luk Y Y, Ren D C. Inhibition of Escherichia coli biofilm formation by self-assembled monolayers of functional alkanethiols on gold. Applied and Environmental Microbiology, 2007, 73(13): 4300–4307 St John PM, Davis R, Cady N, Czajka J, Batt C A, Craighead H G. Diffraction-based cell detection using a microcontact printed antibody grating. Analytical Chemistry, 1998, 70(6): 1108–1111 Morhard F, Pipper J, Dahint R, Grunze M. Immobilization of antibodies in micropatterns for cell detection by optical diffraction. Sensors and Actuators. B, Chemical, 2000, 70(1–3): 232–242 Howell S W, Inerowicz H D, Regnier F E, Reifenberger R. Pattern protein microarrays for bacterial detection. Langmuir, 2003, 19(2): 436–439 Suh K Y, Khademhosseini A, Yoo P J, Langer R. Patterning and separating infected bacteria using host-parasite and virus-antibody interactions. Biomedical Microdevices, 2004, 6(3): 223–229 Sun K, Xie Y, Ye D, Zhao Y, Cui Y, Long F, Zhang W, Jiang X. Mussel-inspired anchoring for patterning cells using polydopamine. Langmuir, 2012, 28(4): 2131–2136 Love J C, Estroff L A, Kriebel J K, Nuzzo R G, Whitesides G M. Self-assembled monolayers of thiolates on metals as a form of nanotechnology. Chemical Reviews, 2005, 105(4): 1103–1169 Rowan B, Wheeler M A, Crooks R M. Patterning bacteria within hyperbranched polymer film templates. Langmuir, 2002, 18(25): 9914–9917 Rozhok S, Shen C K, Littler P L, Fan Z, Liu C, Mirkin C A, Holz R C. Methods for fabricating microarrays of motile bacteria. Small, 2005, 1(4): 445–451 Hou S, Burton E A, Wu R L, Luk Y Y, Ren D. Prolonged control of patterned biofilm formation by bio-inert surface chemistry. Chemical Communications, 2009, 10: 1207–1209 Gu H, Hou S, Yongyat C, De Tore S, Ren D C. Patterned biofilm formation reveals a mechanism for structural heterogeneity in bacterial biofilms. Langmuir, 2013, 29(35): 11145–11153 Pate K, Wilson M, Parkin I P. Antimicrobial surfaces and their potential in reducing the role of the inanimate environment in the incidence of hospital-acquired infections. Journal of Materials Chemistry, 2009, 19(23): 3819–3831 Bixler G D, Bhushan B. Biofouling: Lessons from nature. Philosophical Transactions A Mathematical Physcial &. Engineering and Science, 2012, 370(1967): 2381–2417 Celia E, Darmanin T, Taffin de Givenchy E, Amigoni S, Guittard F. Recent advances in designing superhydrophobic surfaces. Journal of Colloid and Interface Science, 2013, 402: 1–18 Kamegawa T, Shimizu Y, Yamashita H. Superhydrophobic surfaces with photocatalytic self-cleaning properties by nanocomposite coating of TiO2 and polytetrafluoroethylene. Advanced Materials, 2012, 24(27): 3697–3700 Wu Z P, Xu Q F, Wang J N, Ma J. Preparation of large area double-walled carbon nanotube macro-films with self-cleaning properties. Journal of Materials Science and Technology, 2010, 26(1): 20–26 Shang H M, Wang Y, Limmer S J, Chou T P, Takahashi K, Cao G Z. Optically transparent superhydrophobic silica-based films. Thin Solid Films, 2005, 472(1–2): 37–43 Ling X Y, Phang I Y, Vancso G J, Huskens J, Reinhoudt D N. Stable and transparent superhydrophobic nanoparticle films. Langmuir, 2009, 25(5): 3260–3263 Bravo J, Zhai L, Wu Z, Cohen R E, Rubner M F. Transparent superhydrophobic films based on silica nanoparticles. Langmuir, 2007, 23(13): 7293–7298 Yang J, Zhang Z Z, Men X H, Xu X H. Fabrication of stable, transparent and superhydrophobic nanocomposite films with polystyrene functionalized carbon nanotubes. Applied Surface Science, 2009, 255(22): 9244–9247 Wu D, Ming W, Benthem V R. Width. Superhydrophobic fluorinated polyurethane films. Journal of Adhesion Science and Technology, 2008, 22(15): 1869–1881 Coulson S R, Woodward I, Badyal J P S, Brewer S A, Willis C. Super-repellent composite fluoropolymer surfaces. Journal of Physical Chemistry B, 2000, 104(37): 8836–8840 Barthlott W, Neinhuis C. Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta, 1997, 202(1): 1–8 Ensikat H J, Ditsche-Kuru P, Neinhuis C, Barthlott W. Superhydrophobicity in perfection: The outstanding properties of the lotus leaf. Beilstein Journal of Nanotechnology, 2011, 2: 152–161 Gao L C, McCarthy T J. The “lotus effect” explained: Two reasons why two length scales of topography are important. Langmuir, 2006, 22(7): 2966–2967 Marmur A. The lotus effect: Superhydrophobicity and metastability. Langmuir, 2004, 20(9): 3517–3519 Ganesh V A, Raut H K, Nair A S, Ramakrishna S. A review on self-cleaning coatings. Journal of Materials Chemistry, 2011, 21(41): 16304–16322 Wong T S, Kang S H, Tang S K Y, Smythe E J, Hatton B D, Grinthal A, Aizenberg J. Bioinspired self-repairing slippery surfaces with pressure-stable omniphobicity. Nature, 2011, 477(7365): 443–447 Liu K S, Jiang L. Bio-inspired self-cleaning surfaces. Annual Review of Materials Research, 2012, 42(1): 231–263 Nishimoto S, Bhushan B. Bioinspired self-cleaning surfaces with superhydrophobicity, superoleophobicity, and superhydrophilicity. RSC Advances, 2013, 3(3): 671–690 Kirschner C M, Brennan A B. Bio-inspired antifouling strategies. Annual Review of Materials Research, 2012, 42(1): 211–229 Genzer J, Efimenko K. Recent developments in superhydrophobic surfaces and their relevance to marine fouling: A review. Biofouling, 2006, 22(5): 339–360 Pernites R B, Santos C M, Maldonado M, Ponnapati R R, Rodrigues D F, Advincula R C. Tunable protein and bacterial cell adsorption on colloidally templated superhydrophobic polythiophene films. Chemistry of Materials, 2012, 24(5): 870–880 Moafi H F, Shojaie A F, Zanjanchi M A. Photocatalytic self-cleaning properties of cellulosic fibers modified by nano-sized zinc oxide. Thin Solid Films, 2011, 519(11): 3641–3646 Zhang L, Diller R, Bahnemann D, Vormoor M. Photo-induced hydrophilicity and self-cleaning: Models and reality. Energy & Environmental Science., 2012, 5(6): 7491–7507 Ganesh V A, Nair A S, Raut H K, Walsh T M, Ramakrishna S. Photocatalytic superhydrophilic TiO2 coating on glass by electrospinning. RSC Advances, 2012, 2(5): 2067–2072 Xi B, Verma L K, Li J, Bhatia C S, Danner J, Yang H, Zeng H C. TiO2 thin films prepared via adsorptive self-assembly for self-cleaning applications. ACS Applied Materials & Interfaces, 2012, 4(2): 1093–1102 Afzai S, Daoud W A, Langford S J. Photostable self-cleaning cotton by a copper(II) porphyrin/TiO2 visible-light photocatalytic system. ACS Applied Materials & Interfaces, 2013, 5(11): 4753–4759 Ohko Y, Utsumi Y, Niwa C, Tatsuma T, Kobayakawa K, Satoh Y, Kubota Y, Fujishima A. Self-sterilizing and self-cleaning of silicone catheters coated with TiO2 photocatalyst thin films: A preclinical work. Journal of Biomedical Materials Research, 2001, 58(1): 97–101 Joshi A, Punyani S, Borca-Tascuic T, Kane R S. Nanotube-assisted protein deactivation. Nature Nanotechnology, 2008, 3(1): 41–45 Chung K K, Schumacher J F, Sampson E M, Burne R A, Antonelli P J, Brennan A B. Impact of engineered surface microtopography on biofilm formation of Staphylococcus aureus. Biointerphases, 2007, 2(2): 89–94 Carman M L, Estes T G, Feinberg A W, Schumacher J F, Wilkerson W, Wilson L H, Callow M E, Callow J A, Brennan A B. Engineered antifouling microtopographies — Correlating wettability with cell attachment. Biofouling, 2006, 22(1): 1–11 Schumacher J F, Carman M L, Estes T G, Feinberg A W, Wilson L H, Callow M E, Callow J A, Finlay J A, Brennan A B. Engineered antifouling microtopographies — Effect of feature size, geometry, and roughness on settlement of zoospores of the green alga Ulva. Biofouling, 2007, 23(1): 55–62 He X, Aizenberg M, Kuksenok O, Zarzar L D, Shastri A, Balazs A C, Aizenberg J. Synthetic homeostatic materials with chemomechano-chemical self-regulation. Nature, 2012, 487(7406): 214–218 Stuart M A C, Huck W T S, Genzer J, Muller M, Ober C, Stamm M, Sukhorukov G B, Szleifer I, Tsukruk V V, Urban M, Winnik F, Zauscher S, Luzinov I, Minko S. Emerging applications of stimuli-responsive polymer materials. Nature Materials, 2010, 9(2): 101–113 Lahann J, Mitragotri S, Tran T N, Kaido H, Sundaram J, Choi I S, Hoffer S, Somorjai G A, Langer R. A reversibly switching surfaces. Science, 2003, 299(5605): 371–374 Urban A M, Urban M W. Stimuli-responsive polymeric films and coatings. American Chemical Society, 2005, 912: 1 Ista L K, Mendez S, Lopez G P. Attachment and detachment of bacteria on surfaces with tunable and switchable wettability. Biofouling, 2010, 26(1): 111–118 Ista L K, Perez-Luna V H, Lopez G P. Surface-grafted, environmentally sensitive polymers for biofilm release. Applied and Environmental Microbiology, 1999, 65(4): 1603–1609 Ista L K, Lopez G P. Lower critical solubility temperature materials as biofouling release agents. Journal of Industrial Microbiology & Biotechnology, 1998, 20: 121–125 Ista L K, Mendez S, Perez-Luna V H, Lopez G P. Synthesis of poly (N-isopropylacrylamide) on initiator-modified self-assembled monolayers. Langmuir, 2001, 17(9): 2552–2555