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Chapter 25 : Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway

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Abstract:

Bacteria use surface molecules to interact with inanimate objects during biofilm development, other bacteria during sociomicrobiological community activities, and host organisms during mutualistic, commensal, and parasitic symbioses. Among the mechanisms for delivering proteins to the surface of Gram-negative bacteria are type V secretion systems (T5SS) ( ). T5SS comprise a passenger domain and an associated β-barrel transporter domain that, once integrated into the outer membrane via the Bam assembly complex, is sufficient for export of the passenger from the periplasm to the cell surface. Based on domain architecture, T5SS are categorized into five classes, with type Vb or two-partner secretion (TPS) pathway systems being distinct because the passenger domain (referred to generically as a TpsA protein) is synthesized independently from the transporter domain (the TpsB protein). This arrangement requires a mechanism for passenger-transporter recognition in the periplasm and may allow reuse of the transporter for export of multiple copies of the same, or closely related, passenger proteins.

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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Figures

Image of Figure 1
Figure 1

Structures of FhaC and the TPS domain of FhaB. Helix 1 (H1; orange) and loop 6 (L6; fuchsia) are located within the pore of the 16-stranded β barrel (blue) of FhaC when the transporter is in the “closed” state. The POTRA domains (POTRA1 and POTRA2; red) remain periplasmic for selective recognition of the FhaB TPS domain. The TPS domain of FhaB adopts a triangular β-helical structure, shown from the side of the helix (left) and top down in a C-terminal to N-terminal direction (right). Termini are indicated by outlined letters.

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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Image of Figure 2
Figure 2

Initial steps in secretion of FhaB. FhaC alternates between a closed state, in which H1 (orange) and L6 (fuchsia) plug the channel, and an open state, in which H1 and L6 localize to the periplasm and the extracellular space, respectively. The POTRA domains of FhaC (red) bind the unfolded FhaB TPS domain (green line), stabilizing FhaC in the open state. The N terminus of FhaB then binds the interior of the FhaC barrel at β-strands B5 to B8 (blue asterisk) and forms into a β-helix as the protein is translocated, preventing backsliding through the channel.

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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Image of Figure 3
Figure 3

Two models for FhaB secretion: distal N-terminus versus hairpin. In the model proposed by Coutte et al. ( ) , the N terminus of FhaB is pushed away from the membrane as more of the polypeptide translocates through FhaC. The protease SphB1 cleaves between the mature C-terminal domain (MCD) and the periplasmic prodomain, causing release of FHA. In the alternative “hairpin” model proposed by Mazar and Cotter ( ) , the N terminus of FhaB remains bound to FhaC during secretion, and the MCD is located at the distal end of the β-helix. A portion of the MCD spans the helix length, as it is tethered to the periplasmic prodomain. The prodomain N terminus (PNT) prevents translocation of the prodomain through FhaC.

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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Image of Figure 4
Figure 4

Model for stepwise processing and release of FhaB. Upon receipt of an unknown maturation signal (yellow bolt), an as-yet-unidentified protease (P3) removes the extreme C terminus (ECT) and exposes a substrate for the protease CtpA. CtpA processively degrades the prodomain through a portion of the PNT, forming FHA′ and shifting the polypeptide to expose the cleavage site of SphB1. FHA is formed from SphB1-dependent cleavage of FHA′, and it is retained at the membrane until the remaining portion of the prodomain exits FhaC (gray barrel).

Citation: Nash Z, Cotter P. 2019. Filamentous Hemagglutinin, a Model for the Two-Partner Secretion Pathway, p 319-328. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0024-2018
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References

/content/book/10.1128/9781683670285.chap25
1. Leo JC,, Grin I,, Linke D . 2012. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Philos Trans R Soc Lond B Biol Sci 367 : 1088 1101.[CrossRef][PubMed]
2. Costa TRD,, Felisberto-Rodrigues C,, Meir A,, Prevost MS,, Redzej A,, Trokter M,, Waksman G . 2015. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13 : 343 359.[CrossRef][PubMed]
3. Fan E,, Chauhan N,, Udatha DBRKG,, Leo JC,, Linke D . 2016. Type V secretion systems in bacteria. Microbiol Spectr 4 : 305 335.
4. Ulrich T,, Rapaport D . 2015. Biogenesis of beta-barrel proteins in evolutionary context. Int J Med Microbiol 305 : 259 264.[CrossRef][PubMed]
5. Gentle I,, Gabriel K,, Beech P,, Waller R,, Lithgow T . 2004. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164 : 19 24.[CrossRef][PubMed]
6. Simmerman RF,, Dave AM,, Bruce BD . 2014. Structure and function of POTRA domains of Omp85/TPS superfamily. Int Rev Cell Mol Biol 308 : 1 34.[CrossRef][PubMed]
7. Clantin B,, Hodak H,, Willery E,, Locht C,, Jacob-Dubuisson F,, Villeret V . 2004. The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc Natl Acad Sci U S A 101 : 6194 6199.[CrossRef][PubMed]
8. Yeo HJ,, Yokoyama T,, Walkiewicz K,, Kim Y,, Grass S,, Geme JW III . 2007. The structure of the Haemophilus influenzae HMW1 pro-piece reveals a structural domain essential for bacterial two-partner secretion. J Biol Chem 282 : 31076 31084.[PubMed]
9. Weaver TM,, Smith JA,, Hocking JM,, Bailey LJ,, Wawrzyn GT,, Howard DR,, Sikkink LA,, Ramirez-Alvarado M,, Thompson JR . 2009. Structural and functional studies of truncated hemolysin A from Proteus mirabilis. J Biol Chem 284 : 22297 22309.[CrossRef][PubMed]
10. Baelen S,, Dewitte F,, Clantin B,, Villeret V . 2013. Structure of the secretion domain of HxuA from Haemophilus influenzae. Acta Crystallogr Sect F Struct Biol Cryst Commun 69 : 1322 1327.[CrossRef][PubMed]
11. Guérin J,, Bigot S,, Schneider R,, Buchanan SK,, Jacob-Dubuisson F . 2017. Two-partner secretion: combining efficiency and simplicity in the secretion of large proteins for bacteria-host and bacteria-bacteria interactions. Front Cell Infect Microbiol 7 : 148.[CrossRef][PubMed]
12. Melvin JA,, Scheller EV,, Miller JF,, Cotter PA . 2014. Bordetella pertussis pathogenesis: current and future challenges. Nat Rev Microbiol 12 : 274 288.[CrossRef][PubMed]
13. Melvin JA,, Scheller EV,, Noël CR,, Cotter PA . 2015. New insight into filamentous hemagglutinin secretion reveals a role for full-length FhaB in Bordetella virulence. mBio 6 : e01189-15.[CrossRef][PubMed]
14. Inatsuka CS,, Julio SM,, Cotter PA . 2005. Bordetella filamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity. Proc Natl Acad Sci U S A 102 : 18578 18583.[CrossRef][PubMed]
15. Alonso S,, Pethe K,, Mielcarek N,, Raze D,, Locht C . 2001. Role of ADP-ribosyltransferase activity of pertussis toxin in toxin-adhesin redundancy with filamentous hemagglutinin during Bordetella pertussis infection. Infect Immun 69 : 6038 6043.[CrossRef][PubMed]
16. Jacob-Dubuisson F,, Buisine C,, Mielcarek N,, Clément E,, Menozzi FD,, Locht C . 1996. Amino-terminal maturation of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 19 : 65 78.[CrossRef][PubMed]
17. Henderson IR,, Navarro-Garcia F,, Nataro JP . 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6 : 370 378.[CrossRef]
18. Desvaux M,, Cooper LM,, Filenko NA,, Scott-Tucker A,, Turner SM,, Cole JA,, Henderson IR . 2006. The unusual extended signal peptide region of the type V secretion system is phylogenetically restricted. FEMS Microbiol Lett 264 : 22 30.[CrossRef][PubMed]
19. Sijbrandi R,, Urbanus ML,, ten Hagen-Jongman CM,, Bernstein HD,, Oudega B,, Otto BR,, Luirink J . 2003. Signal recognition particle (SRP)-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J Biol Chem 278 : 4654 4659.[CrossRef][PubMed]
20. Peterson JH,, Woolhead CA,, Bernstein HD . 2003. Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J Biol Chem 278 : 46155 46162.[CrossRef][PubMed]
21. Desvaux M,, Scott-Tucker A,, Turner SM,, Cooper LM,, Huber D,, Nataro JP,, Henderson IR . 2007. A conserved extended signal peptide region directs posttranslational protein translocation via a novel mechanism. Microbiology 153 : 59 70.[CrossRef][PubMed]
22. Szabady RL,, Peterson JH,, Skillman KM,, Bernstein HD . 2005. An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc Natl Acad Sci U S A 102 : 221 226.[CrossRef][PubMed]
23. Peterson JH,, Szabady RL,, Bernstein HD . 2006. An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J Biol Chem 281 : 9038 9048.[CrossRef][PubMed]
24. Chevalier N,, Moser M,, Koch H-G,, Schimz K-L,, Willery E,, Locht C,, Jacob-Dubuisson F,, Müller M . 2004. Membrane targeting of a bacterial virulence factor harbouring an extended signal peptide. J Mol Microbiol Biotechnol 8 : 7 18.[CrossRef][PubMed]
25. Jacob-Dubuisson F,, Buisine C,, Willery E,, Renauld-Mongénie G,, Locht C . 1997. Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries. J Bacteriol 179 : 775 783.[CrossRef][PubMed]
26. Renauld-Mongénie G,, Cornette J,, Mielcarek N,, Menozzi FD,, Locht C . 1996. Distinct roles of the N-terminal and C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J Bacteriol 178 : 1053 1060.[CrossRef][PubMed]
27. Fan E,, Fiedler S,, Jacob-Dubuisson F,, Müller M . 2012. Two-partner secretion of gram-negative bacteria: a single β-barrel protein enables transport across the outer membrane. J Biol Chem 287 : 2591 2599.[CrossRef][PubMed]
28. Hodak H,, Clantin B,, Willery E,, Villeret V,, Locht C,, Jacob-Dubuisson F . 2006. Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol Microbiol 61 : 368 382.[CrossRef][PubMed]
29. Delattre A-S,, Saint N,, Clantin B,, Willery E,, Lippens G,, Locht C,, Villeret V,, Jacob-Dubuisson F . 2011. Substrate recognition by the POTRA domains of TpsB transporter FhaC. Mol Microbiol 81 : 99 112.[CrossRef][PubMed]
30. Clantin B,, Delattre AS,, Rucktooa P,, Saint N,, Méli AC,, Locht C,, Jacob-Dubuisson F,, Villeret V . 2007. Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317 : 957 961.[CrossRef][PubMed]
31. Baud C,, Guérin J,, Petit E,, Lesne E,, Dupré E,, Locht C,, Jacob-Dubuisson F . 2014. Translocation path of a substrate protein through its Omp85 transporter. Nat Commun 5 : 5271.[CrossRef][PubMed]
32. Aricò B,, Nuti S,, Scarlato V,, Rappuoli R . 1993. Adhesion of Bordetella pertussis to eukaryotic cells requires a time-dependent export and maturation of filamentous hemagglutinin. Proc Natl Acad Sci U S A 90 : 9204 9208.[CrossRef][PubMed]
33. Domenighini M,, Relman D,, Capiau C,, Falkow S,, Prugnola A,, Scarlato V,, Rappuoli R . 1990. Genetic characterization of Bordetella pertussis filamentous haemagglutinin: a protein processed from an unusually large precursor. Mol Microbiol 4 : 787 800.[CrossRef][PubMed]
34. Mazar J,, Cotter PA . 2006. Topology and maturation of filamentous haemagglutinin suggest a new model for two-partner secretion. Mol Microbiol 62 : 641 654.[CrossRef][PubMed]
35. Kajava AV,, Cheng N,, Cleaver R,, Kessel M,, Simon MN,, Willery E,, Jacob-Dubuisson F,, Locht C,, Steven AC . 2001. Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42 : 279 292.[CrossRef][PubMed]
36. Makhov AM,, Hannah JH,, Brennan MJ,, Trus BL,, Kocsis E,, Conway JF,, Wingfield PT,, Simon MN,, Steven AC . 1994. Filamentous hemagglutinin of Bordetella pertussis. A bacterial adhesin formed as a 50-nm monomeric rigid rod based on a 19-residue repeat motif rich in beta strands and turns. J Mol Biol 241 : 110 124.[CrossRef]
37. Kajava AV,, Steven AC . 2006. The turn of the screw: variations of the abundant beta-solenoid motif in passenger domains of type V secretory proteins. J Struct Biol 155 : 306 315.[CrossRef][PubMed]
38. Coutte L,, Antoine R,, Drobecq H,, Locht C,, Jacob-Dubuisson F . 2001. Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J 20 : 5040 5048.[CrossRef][PubMed]
39. Noël CR,, Mazar J,, Melvin JA,, Sexton JA,, Cotter PA . 2012. The prodomain of the Bordetella two-partner secretion pathway protein FhaB remains intracellular yet affects the conformation of the mature C-terminal domain. Mol Microbiol 86 : 988 1006.[CrossRef][PubMed]
40. Fedele G,, Schiavoni I,, Adkins I,, Klimova N,, Sebo P . 2017. Invasion of dendritic cells, macrophages and neutrophils by the Bordetella adenylate cyclase toxin: a subversive move to fool host immunity. Toxins (Basel) 9 : 293.[CrossRef][PubMed]
41. Novak J,, Cerny O,, Osickova A,, Linhartova I,, Masin J,, Bumba L,, Sebo P,, Osicka R . 2017. Structure-function relationships underlying the capacity of Bordetella adenylate cyclase toxin to disarm host phagocytes. Toxins (Basel) 9 : 300.[CrossRef][PubMed]
42. Confer DL,, Eaton JW . 1982. Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science 217 : 948 950.[CrossRef]
43. Kamanova J,, Kofronova O,, Masin J,, Genth H,, Vojtova J,, Linhartova I,, Benada O,, Just I,, Sebo P . 2008. Adenylate cyclase toxin subverts phagocyte function by RhoA inhibition and unproductive ruffling. J Immunol 181 : 5587 5597.[CrossRef][PubMed]
44. Paccani SR,, Dal Molin F,, Benagiano M,, Ladant D,, D’Elios MM,, Montecucco C,, Baldari CT . 2008. Suppression of T-lymphocyte activation and chemotaxis by the adenylate cyclase toxin of Bordetella pertussis. Infect Immun 76 : 2822 2832.[CrossRef][PubMed]
45. Hoffman C,, Eby J,, Gray M,, Heath Damron F,, Melvin J,, Cotter P,, Hewlett E . 2016. Bordetella adenylate cyclase toxin interacts with filamentous haemagglutinin to inhibit biofilm formation in vitro. Mol Microbiol 103 : 214 228.[PubMed]
46. Gray MC,, Donato GM,, Jones FR,, Kim T,, Hewlett EL . 2004. Newly secreted adenylate cyclase toxin is responsible for intoxication of target cells by Bordetella pertussis. Mol Microbiol 53 : 1709 1719.[CrossRef][PubMed]
47. Guermonprez P,, Khelef N,, Blouin E,, Rieu P,, Ricciardi-Castagnoli P,, Guiso N,, Ladant D,, Leclerc C . 2001. The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha(M)beta(2) integrin (CD11b/CD18). J Exp Med 193 : 1035 1044.[CrossRef][PubMed]
48. Van Strijp JA,, Russell DG,, Tuomanen E,, Brown EJ,, Wright SD . 1993. Ligand specificity of purified complement receptor type three (CD11b/CD18, alpha m beta 2, Mac-1). Indirect effects of an Arg-Gly-Asp (RGD) sequence. J Immunol 151 : 3324 3336.[PubMed]
49. Ishibashi Y,, Yoshimura K,, Nishikawa A,, Claus S,, Laudanna C,, Relman DA . 2002. Role of phosphatidylinositol 3-kinase in the binding of Bordetella pertussis to human monocytes. Cell Microbiol 4 : 825 833.[CrossRef][PubMed]
50. Ishibashi Y,, Nishikawa A . 2002. Bordetella pertussis infection of human respiratory epithelial cells up-regulates intercellular adhesion molecule-1 expression: role of filamentous hemagglutinin and pertussis toxin. Microb Pathog 33 : 115 125.[CrossRef][PubMed]
51. Ruhe ZC,, Subramanian P,, Song K,, Nguyen JY,, Stevens TA,, Low DA,, Jensen GJ,, Hayes CS . 2018. Programmed secretion arrest and receptor-triggered toxin export during antibacterial contact-dependent growth inhibition. Cell 175 : 921 933.e14.[CrossRef][PubMed]
52. Coutte L,, Alonso S,, Reveneau N,, Willery E,, Quatannens B,, Locht C,, Jacob-Dubuisson F . 2003. Role of adhesin release for mucosal colonization by a bacterial pathogen. J Exp Med 197 : 735 742.[CrossRef][PubMed]

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