Surface-Exposed Lipoproteins: An Emerging Secretion Phenomenon in Gram-Negative Bacteria

Trends in Microbiology

Volumn 24, Issue 3, 2016, Pages 198-208

  Wilson, Marlena M ^a   Bernstein, Harris D ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Gram negative bacteria; Lipoproteins; Outer membrane; Protein secretion; Protein translocation

Indexed keywords

BACTERIAL PROTEIN; FATTY ACID DERIVATIVE; LIPOPROTEIN; MEMBRANE PROTEIN; PROTEIN DERIVATIVE; OUTER MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; CELL MEMBRANE; CELL SURFACE; GRAM NEGATIVE BACTERIUM; HUMAN; HYDROPHILICITY; INNER MEMBRANE; LIPOPROTEIN SECRETION; MEMBRANE BINDING; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; GRAM-NEGATIVE BACTERIA; LIPOPROTEINS; PROTEIN TRANSPORT;

EID: 84958769895     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2015.11.006     Document Type: Review

References (86)

1. Hayashi S., Wu H.C. Lipoproteins in bacteria. J. Bioenerg. Biomembr. 1990, 22:451-471.
2. LoVullo E.D., et al. Revisiting the Gram-negative lipoprotein paradigm. J. Bacteriol. 2015, 197:1705-1715.
3. Babu M.M., et al. A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J. Bacteriol. 2006, 188:2761-2773.
4. Braun V. Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim. Biophys. Acta 1975, 415:335-377.
5. Ichihara S., et al. Characterization of new membrane lipoproteins and their precursors of Escherichia coli. J. Biol. Chem. 1981, 256:3125-3129.
6. Okuda S., Tokuda H. Lipoprotein sorting in bacteria. Annu. Rev. Microbiol. 2011, 65:239-259.
7. Narita S., Tokuda H. Amino acids at positions 3 and 4 determine the membrane specificity of Pseudomonas aeruginosa lipoproteins. J. Biol. Chem. 2007, 282:13372-13378.
8. Masuda K., et al. Elucidation of the function of lipoprotein-sorting signals that determine membrane localization. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:7390-7395.
9. Manning P.A., et al. Outer membrane of Escherichia coli: properties of the F sex factor traT protein which is involved in surface exclusion. J. Bacteriol. 1980, 142:285-294.
10. Perumal N.B., Minkley E.G. The product of the F sex factor traT surface exclusion gene is a lipoprotein. J. Biol. Chem. 1984, 259:5357-5360.
11. Chamberlain N.R., et al. Major integral membrane protein immunogens of Treponema pallidum are proteolipids. Infect. Immun. 1989, 57:2872-2877.
12. Brandt M.E., et al. Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins. Infect. Immun. 1990, 58:983-991.
13. Suzuki T., et al. Identification and characterization of a chromosomal virulence gene, vacJ, required for intercellular spreading of Shigella flexneri. Mol. Microbiol. 1994, 11:31-41.
14. Pugsley A.P., et al. Extracellular pullulanase of Klebsiella pneumoniae is a lipoprotein. J. Bacteriol. 1986, 166:1083-1088.
15. Bunikis J., Barbour A.G. Access of antibody or trypsin to an integral outer membrane protein (P66) of Borrelia burgdorferi is hindered by Osp lipoproteins. Infect. Immun. 1999, 67:2874-2883.
16. Zückert W.R., et al. Cross-species surface display of functional spirochetal lipoproteins by recombinant Borrelia burgdorferi. Infect. Immun. 2004, 72:1463-1469.
17. El-Hage N., et al. Surface exposure and protease insensitivity of Borrelia burgdorferi Erp (OspEF-related) lipoproteins. Microbiology 2001, 147:821-830.
18. Zhang L., et al. Molecular interactions that enable movement of the Lyme disease agent from the tick gut into the hemolymph. PLoS Pathog. 2011, 7:e1002079.
19. Kumar M., et al. Borrelia burgdorferi BBA52 is a potential target for transmission blocking Lyme disease vaccine. Vaccine 2011, 29:9012-9019.
20. Zhi H., et al. The BBA33 lipoprotein binds collagen and impacts Borrelia burgdorferi pathogenesis. Mol. Microbiol. 2015, 96:68-83.
21. Zückert W.R. Secretion of bacterial lipoproteins: through the cytoplasmic membrane, the periplasm and beyond. Biochim. Biophys. Acta 2014, 1843:1509-1516.
22. Pizza M., et al. Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 2000, 287:1816-1820.
23. Masignani V., et al. Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J. Exp. Med. 2003, 197:789-799.
24. van Ulsen P., et al. A neisserial autotransporter NalP modulating the processing of other autotransporters. Mol. Microbiol. 2003, 50:1017-1030.
25. Fletcher L.D., et al. Vaccine potential of the Neisseria meningitidis 2086 lipoprotein. Infect. Immun. 2004, 72:2088-2100.
26. Leuzzi R., et al. Ng-MIP, a surface-exposed lipoprotein of Neisseria gonorrhoeae, has a peptidyl-prolyl cis/trans isomerase (PPIase) activity and is involved in persistence in macrophages. Mol. Microbiol. 2005, 58:669-681.
27. Arenas J., et al. Locus NMB0035 codes for a 47-kDa surface-accessible conserved antigen in Neisseria. Int. Microbiol. 2006, 9:273-280.
28. Pettersson A., et al. Vaccine potential of the Neisseria meningitidis lactoferrin-binding proteins LbpA and LbpB. Vaccine 2006, 24:3545-3557.
29. DeRocco A.J., Cornelissen C.N. Identification of transferrin-binding domains in TbpB expressed by Neisseria gonorrhoeae. Infect. Immun. 2007, 75:3220-3232.
30. Hsu C.A., et al. Immunoproteomic identification of the hypothetical protein NMB1468 as a novel lipoprotein ubiquitous in Neisseria meningitidis with vaccine potential. Proteomics 2008, 8:2115-2125.
31. Sardiñas G., et al. Assessment of vaccine potential of the Neisseria-specific protein NMB0938. Vaccine 2009, 27:6910-6917.
32. Madico G., et al. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J. Immunol. 2006, 177:501-510.
33. Serruto D., et al. Neisseria meningitidis GNA2132, a heparin-binding protein that induces protective immunity in humans. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3770-3775.
34. Serruto D., et al. The new multicomponent vaccine against meningococcal serogroup B, 4CMenB: immunological, functional and structural characterization of the antigens. Vaccine 2012, 30(Suppl. 2):B87-B97.
35. Anderson J.E., et al. Gonococcal transferrin-binding protein 2 facilitates but is not essential for transferrin utilization. J. Bacteriol. 1994, 176:3162-3170.
36. Pettersson A., et al. Molecular characterization of LbpB, the second lactoferrin-binding protein of Neisseria meningitidis. Mol. Microbiol. 1998, 27:599-610.
37. Roussel-Jazédé V., et al. Lipidation of the autotransporter NalP of Neisseria meningitidis is required for its function in the release of cell-surface-exposed proteins. Microbiology 2013, 159:286-295.
38. Braun V., Rehn K. Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. Eur. J. Biochem. 1969, 10:426-438.
39. Braun V., Bosch V. Sequence of the murein-lipoprotein and the attachment site of the lipid. Eur. J. Biochem. 1972, 28:51-69.
40. Braun V., Wolff H. The murein-lipoprotein linkage in the cell wall of Escherichia coli. Eur. J. Biochem. 1970, 14:387-391.
41. Braun V., Sieglin U. The covalent murein-lipoprotein structure of the Escherichia coli cell wall. The attachment site of the lipoprotein on the murein. Eur. J. Biochem. 1970, 13:336-346.
42. Cowles C.E., et al. The free and bound forms of Lpp occupy distinct subcellular locations in Escherichia coli. Mol. Microbiol. 2011, 79:1168-1181.
43. Michel L.V., et al. Dual orientation of the outer membrane lipoprotein Pal in Escherichia coli. Microbiology 2015, 161:1251-1259.
44. Murphy T.F., et al. Identification of a 16,600-dalton outer membrane protein on nontypeable Haemophilus influenzae as a target for human serum bactericidal antibody. J. Clin. Invest. 1986, 78:1020-1027.
45. Konovalova A., et al. Transmembrane domain of surface-exposed outer membrane lipoprotein RcsF is threaded through the lumen of β-barrel proteins. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:E4350-E4358.
46. Cho S.H., et al. Detecting envelope stress by monitoring β-barrel assembly. Cell 2014, 159:1652-1664.
47. Webb C.T., et al. Dynamic association of BAM complex modules includes surface exposure of the lipoprotein BamC. J. Mol. Biol. 2012, 422:545-555.
48. Dong C., et al. Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 2006, 444:226-229.
49. Goyal P., et al. Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG. Nature 2014, 516:250-253.
50. Shipman J.A., et al. Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J. Bacteriol. 2000, 182:5365-5372.
51. Phansopa C., et al. Structural and functional characterization of NanU, a novel high-affinity sialic acid-inducible binding protein of oral and gut-dwelling Bacteroidetes species. Biochem. J. 2014, 458:499-511.
52. Larsbrink J., et al. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 2014, 506:498-502.
53. Sijbrandi R., et al. Pbp, a cell-surface exposed plasminogen binding protein of Bacteroides fragilis. Microbes Infect. 2008, 10:514-521.
54. Weinacht K.G., et al. Tyrosine site-specific recombinases mediate DNA inversions affecting the expression of outer surface proteins of Bacteroides fragilis. Mol. Microbiol. 2004, 53:1319-1330.
55. Fletcher C.M., et al. A general O-glycosylation system important to the physiology of a major human intestinal symbiont. Cell 2009, 137:321-331.
56. Galvão B.P., et al. Identification of a collagen type I adhesin of Bacteroides fragilis. PLoS ONE 2014, 9:e91141.
57. Wilson M.M., et al. Analysis of the outer membrane proteome and secretome of Bacteroides fragilis reveals a multiplicity of secretion mechanisms. PLoS ONE 2015, 10:e0117732.
58. Manfredi P., et al. The genome and surface proteome of Capnocytophaga canimorsus reveal a key role of glycan foraging systems in host glycoproteins deglycosylation. Mol. Microbiol. 2011, 81:1050-1060.
59. Noinaj N., et al. Structural basis for iron piracy by pathogenic Neisseria. Nature 2012, 483:53-58.
60. d'Enfert C., et al. Cloning and expression in Escherichia coli of the Klebsiella pneumoniae genes for production, surface localization and secretion of the lipoprotein pullulanase. EMBO J. 1987, 6:3531-3538.
61. Odenbreit S., et al. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 1999, 31:1537-1548.
62. Coutte L., et al. Surface anchoring of bacterial subtilisin important for maturation function. Mol. Microbiol. 2003, 49:529-539.
63. Ashgar S.S., et al. CapA, an autotransporter protein of Campylobacter jejuni, mediates association with human epithelial cells and colonization of the chicken gut. J. Bacteriol. 2007, 189:1856-1865.
64. Ieva R., Bernstein H.D. Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19120-19125.
65. Junker M., et al. Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol. Microbiol. 2009, 71:1323-1332.
66. Dunstan R.A., et al. Assembly of the secretion pores GspD, Wza and CsgG into bacterial outer membranes does not require the Omp85 proteins BamA or TamA. Mol. Microbiol. 2015, 97:616-629.
67. Chen S., Zückert W.R. Probing the Borrelia burgdorferi surface lipoprotein secretion pathway using a conditionally folding protein domain. J. Bacteriol. 2011, 193:6724-6732.
68. Schulze R.J., et al. Translocation of Borrelia burgdorferi surface lipoprotein OspA through the outer membrane requires an unfolded conformation and can initiate at the C-terminus. Mol. Microbiol. 2010, 76:1266-1278.
69. Kumru O.S., et al. Surface localization determinants of Borrelia OspC/Vsp family lipoproteins. J. Bacteriol. 2011, 193:2814-2825.
70. Schulze R.J., Zückert W.R. Borrelia burgdorferi lipoproteins are secreted to the outer surface by default. Mol. Microbiol. 2006, 59:1473-1484.
71. Lenhart T.R., Akins D.R. Borrelia burgdorferi locus BB0795 encodes a BamA orthologue required for growth and efficient localization of outer membrane proteins. Mol. Microbiol. 2010, 75:692-709.
72. Yamanaka H., et al. MacAB is involved in the secretion of Escherichia coli heat-stable enterotoxin II. J. Bacteriol. 2008, 190:7693-7698.
73. Francetić O., Pugsley A.P. Towards the identification of type II secretion signals in a nonacylated variant of pullulanase from Klebsiella oxytoca. J. Bacteriol. 2005, 187:7045-7055.
74. Ostberg K.L., et al. Conserved regions of gonococcal TbpB are critical for surface exposure and transferrin iron utilization. Infect. Immun. 2013, 81:3442-3450.
75. Poquet I., et al. Stable periplasmic secretion intermediate in the general secretory pathway of Escherichia coli. EMBO J. 1993, 12:271-278.
76. d'Enfert C., et al. Export and secretion of the lipoprotein pullulanase by Klebsiella pneumoniae. Mol. Microbiol. 1987, 1:107-116.
77. Keenan J., et al. Immune response to an 18-kilodalton outer membrane antigen identifies lipoprotein 20 as a Helicobacter pylori vaccine candidate. Infect. Immun. 2000, 68:3337-3343.
78. Dashper S.G., et al. Characterization of a novel outer membrane hemin-binding protein of Porphyromonas gingivalis. J. Bacteriol. 2000, 182:6456-6462.
79. Coutte L., et al. Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J. 2001, 20:5040-5048.
80. Jin S., et al. JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol. Microbiol. 2001, 39:1225-1236.
81. Arambula D., et al. Surface display of a massively variable lipoprotein by a Legionella diversity-generating retroelement. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:8212-8217.
82. Pride A.C., et al. The outer surface lipoprotein VolA mediates utilization of exogenous lipids by Vibrio cholerae. MBio 2013, 4. e00305-13.
83. Michel L.V., et al. Dual orientation of the outer membrane lipoprotein P6 of nontypeable Haemophilus influenzae. J. Bacteriol. 2013, 195:3252-3259.
84. Fleury C., et al. Identification of a Haemophilus influenzae factor H-Binding lipoprotein involved in serum resistance. J. Immunol. 2014, 192:5913-5923.
85. Qin A., et al. FipB, an essential virulence factor of Francisella tularensis subsp. tularensis, has dual roles in disulfide bond formation. J. Bacteriol. 2014, 196:3571-3581.
86. Wang W., et al. Identification of an outer membrane lipoprotein involved in nasopharyngeal colonization by Moraxella catarrhalis in an animal model. Infect. Immun. 2014, 82:2287-2299.