The Diverse Structures and Functions of Surfactant Proteins

Trends in Biochemical Sciences

Volumn 41, Issue 7, 2016, Pages 610-620

  Schor, Marieke ^a   Reid, Jack L ^b   MacPhee, Cait E ^a   Stanley Wall, Nicola R ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANT HYDROPHOBIN 1; ABUNDANT HYDROPHOBIN 3; BIOFILM SURFACE LAYER PROTEIN A; CHAPLIN A; CHAPLIN B; CHAPLIN C; CHAPLIN D; CHAPLIN E; CHAPLIN F; CHAPLIN G; CHAPLIN H; HYDROPHOBIN 1; HYDROPHOBIN 2; LATHERIN; PEPTIDES AND PROTEINS; PROTEIN DEWA; PROTEIN EAS; PROTEIN MPG1; PROTEIN NC2; PROTEIN SC3; PROTEIN SC4; RANASPUMIN 1; RANASPUMIN 2; RANASPUMIN 3; RANASPUMIN 4; RANASPUMIN 5; RODLIN PROTEIN A; RODLIN PROTEIN B; SURFACTANT PROTEIN; UNCLASSIFIED DRUG; PROTEIN; SURFACTANT;

AMINO ACID SEQUENCE; CONFORMATIONAL TRANSITION; FILAMENTOUS FUNGUS; FUNGUS HYPHAE; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; SURFACE TENSION;

PROTEIN CONFORMATION; PROTEINS; SURFACE TENSION; SURFACE-ACTIVE AGENTS;

EID: 84969916657     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2016.04.009     Document Type: Review

References (86)

1. 1 Claessen, D., et al. A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev. 17 (2003), 1714–1726.
2. 2 Elliot, M.A., et al. The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev. 17 (2003), 1727–1740.
3. 3 Fleming, R.I., et al. Foam nest components of the tungara frog: a cocktail of proteins conferring physical and biological resilience. Proc. Biol. Sci. 276 (2009), 1787–1795.
4. 4 McDonald, R.E., et al. Latherin: a surfactant protein of horse sweat and saliva. PLoS ONE, 4, 2009, e5726.
5. 5 Wosten, H.A.B., et al. Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. Plant Cell 5 (1993), 1567–1574.
6. 6 Whitsett, J.A., Weaver, T.E., Hydrophobic surfactant proteins in lung function and disease. N. Engl. J. Med. 347 (2002), 2141–2148.
7. 7 Nakano, M.M., et al. Isolation and characterization of sfp: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis. Mol. Gen. Genet. 232 (1992), 313–321.
8. 8 Cooper, A., Kennedy, M.W., Biofoams and natural protein surfactants. Biophys. Chem. 151 (2010), 96–104.
9. 9 Ren, Q., et al. Two forms and two faces, multiple states and multiple uses: properties and applications of the self-assembling fungal hydrophobins. Biopolymers 100 (2013), 601–612.
10. 10 Hakanpaa, J., et al. Atomic resolution structure of the HFBII hydrophobin, a self-assembling amphiphile. J. Biol. Chem. 279 (2004), 534–539.
11. 11 Hakanpaa, J., et al. Two crystal structures of Trichoderma reesei hydrophobin HFBI–the structure of a protein amphiphile with and without detergent interaction. Protein Sci. 15 (2006), 2129–2140.
12. 12 Hissa, D.C., et al. Unique crystal structure of a novel surfactant protein from the foam nest of the frog Leptodactylus vastus. Chembiochem 15 (2014), 393–398.
13. 13 Hobley, L., et al. BslA is a self-assembling bacterial hydrophobin that coats the Bacillus subtilis biofilm. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 13600–13605.
14. 14 Kwan, A.H.Y., et al. Structural basis for rodlet assembly in fungal hydrophobins. Proc. Natl. Acad. Sci. U.S.A. 103 (2006), 3621–3626.
15. 15 Mackenzie, C.D., et al. Ranaspumin-2: structure and function of a surfactant protein from the foam nests of a tropical frog. Biophys. J. 96 (2009), 4984–4992.
16. 16 Ren, Q., et al. Solution structure and interface-driven self-assembly of NC2, a new member of the class II hydrophobin proteins. Proteins 82 (2014), 990–1003.
17. 17 Vance, S.J., et al. The structure of latherin, a surfactant allergen protein from horse sweat and saliva. J. R. Soc. Interface, 10, 2013, 20130453.
18. 18 Morris, V.K., et al. Analysis of the structure and conformational states of DewA gives insight into the assembly of the fungal hydrophobins. J. Mol. Biol. 425 (2013), 244–256.
19. 19 Schuren, F.H., Wessels, J.G., Two genes specifically expressed in fruiting dikaryons of Schizophyllum commune: homologies with a gene not regulated by mating-type genes. Gene 90 (1990), 199–205.
20. 20 Wosten, H.A., et al. How a fungus escapes the water to grow into the air. Curr. Biol. 9 (1999), 85–88.
21. 21 Wosten, H.A., Hydrophobins: multipurpose proteins. Annu. Rev. Microbiol. 55 (2001), 625–646.
22. 22 Bayry, J., et al. Hydrophobins–unique fungal proteins. PLoS Pathog., 8, 2012, e1002700.
23. 23 Aimanianda, V., et al. Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460 (2009), 1117–1121.
24. 24 Paananen, A., et al. Structural hierarchy in molecular films of two class II hydrophobins. Biochemistry 42 (2003), 5253–5258.
25. 25 Torkkeli, M., et al. Aggregation and self-assembly of hydrophobins from Trichoderma reesei: low-resolution structural models. Biophys. J. 83 (2002), 2240–2247.
26. 26 Macindoe, I., et al. Self-assembly of functional, amphipathic amyloid monolayers by the fungal hydrophobin EAS. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), E804–E811.
27. 27 Abeln, S., Frenkel, D., Disordered flanks prevent peptide aggregation. PLoS Comput. Biol., 4, 2008, e1000241.
28. 28 Kisko, K., et al. Self-assembled films of hydrophobin proteins HFBI and HFBII studied in situ at the air/water interface. Langmuir 25 (2009), 1612–1619.
29. 29 Morris, V.K., et al. Recruitment of class I hydrophobins to the air:water interface initiates a multi-step process of functional amyloid formation. J. Biol. Chem. 286 (2011), 15955–15963.
30. 30 Basheva, E.S., et al. Self-assembled bilayers from the protein HFBII hydrophobin: nature of the adhesion energy. Langmuir 27 (2011), 4481–4488.
31. 31 Lienemann, M., et al. Charge-based engineering of hydrophobin HFBI: effect on interfacial assembly and interactions. Biomacromolecules 16 (2015), 1283–1292.
32. 32 Magarkar, A., et al. Hydrophobin film structure for HFBI and HFBII and mechanism for accelerated film formation. PLoS Comput. Biol., 10, 2014, e1003745.
33. 33 Cheung, D.L., Molecular simulation of hydrophobin adsorption at an oil–water interface. Langmuir 28 (2012), 8730–8736.
34. 34 Claessen, D., et al. The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol. Microbiol. 53 (2004), 433–443.
35. 35 Claessen, D., et al. Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic surface. Mol. Microbiol. 44 (2002), 1483–1492.
36. 36 Kodani, S., et al. The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc. Natl. Acad. Sci. U.S.A. 101 (2004), 11448–11453.
37. 37 Tillotson, R.D., et al. A surface active protein involved in aerial hyphae formation in the filamentous fungus Schizophillum commune restores the capacity of a bald mutant of the filamentous bacterium Streptomyces coelicolor to erect aerial structures. Mol. Microbiol. 30 (1998), 595–602.
38. 38 Willey, J., et al. Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor. Cell 65 (1991), 641–650.
39. 39 Di Berardo, C., et al. Function and redundancy of the chaplin cell surface proteins in aerial hypha formation, rodlet assembly, and viability in Streptomyces coelicolor. J. Bacteriol. 190 (2008), 5879–5889.
40. 40 de Jong, W., et al. SapB and the rodlins are required for development of Streptomyces coelicolor in high osmolarity media. FEMS Microbiol. Lett. 329 (2012), 154–159.
41. 41 Sawyer, E.B., et al. The assembly of individual chaplin peptides from Streptomyces coelicolor into functional amyloid fibrils. PLoS ONE, 6, 2011, e18839.
42. 42 Ekkers, D.M., et al. Surface modification using interfacial assembly of the Streptomyces chaplin proteins. Appl. Microbiol. Biotechnol. 98 (2014), 4491–4501.
43. 43 Kobayashi, K., Iwano, M., BslA (YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol. Microbiol. 85 (2012), 51–66.
44. 44 Morikawa, M., Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. J. Biosci. Bioeng. 101 (2006), 1–8.
45. 45 Bais, H.P., et al. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134 (2004), 307–319.
46. 46 Hobley, L., et al. Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiol. Rev. 39 (2015), 649–669.
47. 47 Ostrowski, A., et al. YuaB functions synergistically with the exopolysaccharide and TasA amyloid fibers to allow biofilm formation by Bacillus subtilis. J. Bacteriol. 193 (2011), 4821–4831.
48. 48 Bromley, K.M., et al. Interfacial self-assembly of a bacterial hydrophobin. Proc. Natl Acad. Sci. U.S.A. 112 (2015), 5419–5424.
49. 49 Brandani, G.B., et al. The bacterial hydrophobin BslA is a switchable ellipsoidal Janus nanocolloid. Langmuir 31 (2015), 11558–11563.
50. 50 Wang, Z.G., et al. A narrow amide I vibrational band observed by sum frequency generation spectroscopy reveals highly ordered structures of a biofilm protein at the air/water interface. Chem. Commun. (Camb.) 52 (2016), 2956–2959.
51. 51 Cooper, A., et al. Adsorption of frog foam nest proteins at the air–water interface. Biophys. J. 88 (2005), 2114–2125.
52. 52 Pugh, R.J., Foaming, foam films, antifoaming and defoaming. Adv. Colloid Interface Sci. 64 (1996), 67–142.
53. 53 Hissa, D.C., et al. Novel surfactant proteins are involved in the structure and stability of foam nests from the frog Leptodactylus vastus. J. Exp. Biol. 211 (2008), 2707–2711.
54. 54 Morris, R.J., et al. The conformation of interfacially adsorbed ranaspumin-2 is an arrested state on the unfolding pathway. arXiv, 2016 Published online February 12, 2016 arXiv:1602.04099.
55. 55 Beeley, J.G., et al. Isolation and characterization of latherin, a surface-active protein from horse sweat. Biochem. J. 235 (1986), 645–650.
56. 56 Bingle, C.D., Craven, C.J., PLUNC: a novel family of candidate host defence proteins expressed in the upper airways and nasopharynx. Hum. Mol. Genet. 11 (2002), 937–943.
57. 57 Gakhar, L., et al. PLUNC is a novel airway surfactant protein with anti-biofilm activity. PLoS ONE, 5, 2010, e9098.
58. 58 Wosten, H.A., Scholtmeijer, K., Applications of hydrophobins: current state and perspectives. Appl. Microbiol. Biotechnol. 99 (2015), 1587–1597.
59. 59 Boeuf, S., et al. Engineering hydrophobin DewA to generate surfaces that enhance adhesion of human but not bacterial cells. Acta Biomater. 8 (2012), 1037–1047.
60. 60 Li, X.X., et al. Patterning of neural stem cells on poly(lactic-co-glycolic acid) film modified by hydrophobin. Colloids Surf. B Biointerfaces 74 (2009), 370–374.
61. 61 Valo, H.K., et al. Multifunctional hydrophobin: toward functional coatings for drug nanoparticles. ACS Nano 4 (2010), 1750–1758.
62. 62 Wang, X.S., et al. Noncovalently functionalized multi-wall carbon nanotubes in aqueous solution using the hydrophobin HFBI and their electroanalytical application. Biosens. Bioelectron. 26 (2010), 1104–1108.
63. 63 Yang, W.R., et al. Surface functionalization of carbon nanomaterials by self-assembling hydrophobin proteins. Biopolymers 99 (2013), 84–94.
64. 64 Haas Jimoh Akanbi, M., et al. Use of hydrophobins in formulation of water insoluble drugs for oral administration. Colloids Surf. B Biointerfaces 75 (2010), 526–531.
65. 65 Dickinson, E., Colloids in food: ingredients, structure, and stability. Annu. Rev. Food. Sci. Technol. 6 (2015), 211–233.
66. 66 Green, A.J., et al. Formation and stability of food foams and aerated emulsions: hydrophobins as novel functional ingredients. Curr. Opin. Colloid Interface Sci. 18 (2013), 292–301.
67. 67 Stanley-Wall, N.R., MacPhee, C.E., Connecting the dots between bacterial biofilms and ice cream. Phys. Biol., 12, 2015, 063001.
68. 68 Frey, S.L., et al. A non-foaming proteosurfactant engineered from ranaspumin-2. Colloids Surf. B Biointerfaces 133 (2015), 239–245.
69. 69 Capstick, D.S., et al. SapB and the chaplins: connections between morphogenetic proteins in Streptomyces coelicolor. Mol. Microbiol. 64 (2007), 602–613.
70. 70 DeGroot, P.W.J., et al. The Agaricus bisporus hypA gene encodes a hydrophobin and specifically accumulates in peel tissue of mushroom caps during fruit body development. J. Mol. Biol. 257 (1996), 1008–1018.
71. 71 Lugones, L.G., et al. An abundant hydrophobin (ABH1) forms hydrophobic rodlet layers in Agaricus bisporus fruiting bodies. Microbiology 142 (1996), 1321–1329.
72. 72 Lugones, L.G., et al. Hydrophobins line air channels in fruiting bodies of Schizophyllum commune and Agaricus bisporus. Mycol. Res. 103 (1999), 635–640.
73. 73 Lugones, L.G., et al. A hydrophobin (ABH3) specifically secreted by vegetatively growing hyphae of Agaricus bisporus (common white button mushroom). Microbiology 144 (1998), 2345–2353.
74. 74 Zhang, S.Z., et al. Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana. Mol. Microbiol. 80 (2011), 811–826.
75. 75 van Wetter, M.A., et al. SC3 and SC4 hydrophobins have distinct roles in formation of aerial structures in dikaryons of Schizophyllum commune. Mol. Microbiol. 36 (2000), 201–210.
76. 76 Wosten, H.A.B., et al. Interfacial self-assembly of a hydrophobin into an amphipathic protein membrane mediates fungal attachment to hydrophobic surfaces. EMBO J. 13 (1994), 5848–5854.
77. 77 Bruns, S., et al. Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog., 6, 2010, e1000873.
78. 78 Paris, S., et al. Conidial hydrophobins of Aspergillus fumigatus. Appl. Environ. Microbiol. 69 (2003), 1581–1588.
79. 79 Stringer, M.A., et al. Rodletless, a new Aspergillus developmental mutant induced by directed gene inactivation. Genes Dev. 5 (1991), 1161–1171.
80. 80 Mackay, J.P., et al. The hydrophobin EAS is largely unstructured in solution and functions by forming amyloid-like structures. Structure 9 (2001), 83–91.
81. 81 Talbot, N.J., et al. Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5 (1993), 1575–1590.
82. 82 Talbot, N.J., et al. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8 (1996), 985–999.
83. 83 Askolin, S., et al. The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diverse functions in fungal development. FEMS Microbiol. Lett. 253 (2005), 281–288.
84. 84 Cox, A.R., et al. Surface properties of class II hydrophobins from Trichoderma reesei and influence on bubble stability. Langmuir 23 (2007), 7995–8002.
85. 85 Bailey, M.J., et al. Process technological effects of deletion and amplification of hydrophobins I and II in transformants of Trichoderma reesei. Appl. Microbiol. Biotechnol. 58 (2002), 721–727.
86. 86 Humphrey, W., et al. VMD: visual molecular dynamics. J. Mol. Graph. 14 (1996), 33–38.