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1.B.6 The OmpA-OmpF Porin (OOP) Family

The large OOP family includes the functionally well characterized OmpA porin of E. coli as well as the OmpF (OprF) porin of Pseudomonas aeruginosa (Baldermann et al., 1998). Both proteins contain an N-terminal 8 β-strand transmembrane domain and a cell surface C-terminal peptidoglycan-interaction domain (Grizot and Buchanan, 2004). Only this latter domain exhibits extensive sequence similarity with E. coli OmpA and M. tuberculosis OmpATb. OmpATb has been reported to be a low activity channel that is essential for adaptation of M. tuberculosis to low pH and survival in mouse macrophage, but channel activity has been questioned (Niederweis, 2003).OmpA proteins and their many homologues probably all form structures consisting of eight transmembrane, all next neighbor, antiparallel, amphipathic β-strands. They form small β-barrels with short turns at the periplasmic barrel ends, and long flexible loops at the external ends. A 1.65 Å resolution monomeric structure is available for the E. coli OmpA porin (Pautsch and Schulz, 2000). A tetrameric quarternary structure has been proposed in which the subunits of the tetramer dissociate relatively readily. However, monomeric structures are proposed for other members of this family (Gribun et al., 2004).

The OmpA family consists of heat-modifiable, surface-exposed, porin proteins that are in high-copy number in the outer membranes of many Gram-negative bacteria. OmpA proteins generally have  an N-terminal, eight-stranded, anti-parallel β barrel embedded in the outer membrane while the C-terminal domain is globular and located in the periplasmic space. Escherichia coli OmpA is the best characterized of the proteins, but homologues from pathogenic bacteria include Pseudomonas aeruginosa OprF, Haemophilus influenzae P5, Klebsiella pneumoniae OmpA, and Chlamydia trachomatis major outer membrane protein (MOMP). OmpA from the veterinary pathogens Mannheimia haemolytica, Haemophilus parasuis, Leptospira interrogans, and Pasteurella multocida have been studied to a lesser extent (Confer and Ayalew 2013). Among many of the pathogenic bacteria, OmpA proteins have important pathogenic roles including bacterial adhesion, invasion, or intracellular survival as well as evasion of host defenses or stimulators of pro-inflammatory cytokine production. These pathogenic roles are most commonly associated with central nervous system, respiratory and urogenital diseases. Additionally, OmpA family proteins can serve as targets of the immune system with immunogenicity related to surface-exposed loops of the molecule. In several cases, OmpA proteins are under evaluation as potential vaccine candidates (Confer and Ayalew 2013).

The P. aeruginosa OmpF (1.B.6.1.2) exists in two conformations: a minority single domain conformer and a majority two domain conformer (Sugawara et al., 2006). Only the former inserts into liposomes to give high conductance channel activity (Nestorovich et al., 2006). The active conformation is present only for short times (Nestorovich et al., 2006) accounting for low permeability reported previously.

The OOP family proteins may exhibit structural similarity with well-characterized virulence proteins such as the neisserial opacity (Opa) adhesins, the Salmonella Rck complement resistance protein, the Salmonella PagC intramacrophage survival protein, and the Yersinia Ail attachment/invasion protein (Baldermann et al., 1998). However, sequence similarity with these proteins is insufficient to establish homology. These protein β-barrels resemble those of the lipocalin family although the members of these two protein families serve entirely different functions and show no observable sequence similarity. OmpA of E. coli is required for bacterial conjugation and for maintenance of outer membrane stability.

Members of the Ail/Lom family of outer membrane proteins, which are homologous to OmpA of E. coli (1.B.6.1.2), provide protection from complement-dependent killing for a number of pathogenic bacteria. The Y. pestis KIM genome encodes four Ail/Lom family proteins. The Ail (Attachment inversion locus; 182aas) protein is essential for Y. pestis to resist complement-mediated killing. High-level expression of the three other Y. pestis Ail/Lom family proteins (the y1682, y2034, and y2446 proteins) provided no protection against complement-mediated bacterial killing (Bartra et al., 2008).

Intragenic duplication of the 8-stranded OmpX β-barrel produces a functional pore (Omp2X) the size of the OmpC porin (1.B.1.1.3) channel, a natural 16 stranded β-barrel (Arnold et al. 2007).  This provides a potential mechanism for generating larger porins of 16 TMSs from smaller porins of 8 TMSs.

 

This family belongs to the: Porin Superfamily I.

References associated with 1.B.6 family:

Arnold, T., M. Poynor, S. Nussberger, A.N. Lupas, and D. Linke. (2007). Gene duplication of the eight-stranded β-barrel OmpX produces a functional pore: a scenario for the evolution of transmembrane β-barrels. J. Mol. Biol. 366: 1174-1184. 17217961
Arora, A., D. Rinehart, G. Szabo, and L.K. Tamm. (2000). Refolded outer membrane protein A of Escherichia coli forms ion channels with two conductance states in planar lipid bilayers. J. Biol. Chem. 275: 1594-1600. 10636850
Baldermann, C., A. Lupas, J. Lubieniecki, and H. Engelhardt. (1998). The regulated outer membrane protein Omp21 from Comamonas acidovorans is identified as a member of a new family of eight-stranded β-sheet proteins by its sequence and properties. J. Bacteriol. 180: 3741-3749. 9683466
Bartra, S.S., K.L. Styer, D.M. O'Bryant, M.L. Nilles, B.J. Hinnebusch, A. Aballay, and G.V. Plano. (2008). Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer membrane protein. Infect. Immun. 76: 612-622. 18025094
Brinkman, F.S., M. Bains, and R.E.W. Hancock. (2000). The amino terminus of Pseudomonas aeruginosa outer membrane protein OprF forms channels in lipid bilayer membranes: correlation with a three-dimensional model. J. Bacteriol. 182: 5251-5255. 10960112
Chevalier, G., H. Duclohier, D. Thomas, E. Shechter, and H. Wróblewski. (1993). Purification and characterization of protein H, the major porin of Pasteurella multocida. J. Bacteriol. 175: 266-276. 7677992
Confer, A.W. and S. Ayalew. (2013). The OmpA family of proteins: roles in bacterial pathogenesis and immunity. Vet Microbiol 163: 207-222. 22986056
Dupont, M., E. Dé, R. Chollet, J. Chevalier, and J.M. Pagès. (2004). Enterobacter aerogenes OmpX, a cation-selective channel mar- and osmo-regulated. FEBS Lett. 569: 27-30. 15225603
Gribun, A., D.J. Katcoff, G. Hershkovits, I. Pechatnikov, and Y. Nitzan. (2004). Cloning and characterization of the gene encoding for OMP-PD porin: the major Photobacterium damsela outer membrane protein. Curr. Microbiol. 48: 167-174. 15057460
Gribun, A., Y. Nitzan, I. Pechatnikov, G. Hershkovits, and D.J. Katcoff. (2003). Molecular and structural characterization of the HMP-AB gene encoding a pore-forming protein from a clinical isolate of Actinetobacter baumannii. Curr. Microbiol. 47: 434-443. 14669924
Grizot, S. and S.K. Buchanan. (2004). Structure of the OmpA-like domain of RmpM from Neisseria meningitidis. Mol. Microbiol. 51: 1027-1037. 14763978
Hancock, R.E.W. and F.S.L. Brinkman. (2002). Function of Pseudomonas porins in uptake and efflux. Annu. Rev. Microbiol. 56: 17-38. 12142471
Hou, V.C., G.R. Moe, Z. Raad, T. Wuorimaa, and D.M. Granoff. (2003). Conformational epitopes recognized by protective anti-neisserial surface protein A antibodies. Infect. Immun. 71: 6844-6849. 14638771
Iida, A., Y. Ohnishi, and S. Horinouchi. (2008). An OmpA family protein, a target of the GinI/GinR quorum-sensing system in Gluconacetobacter intermedius, controls acetic acid fermentation. J. Bacteriol. 190: 5009-5019. 18487322
Jeanteur, D., J.H. Lakey, and F. Pattus. (1991). The bacterial porin superfamily: sequence alignment and structure prediction. Mol. Microbiol. 5: 2153-2164. 1662760
Jeanteur, D., J.H. Lakey, and F. Pattus. (1994). The porin superfamily: diversity and common features. In: Bacterial Cell Wall (Ghuysen, J.M. and R. Hakenbeck,eds.). Elsevier, Amsterdam, pp. 363-380.
Kleinschmidt, J.H. and L.K. Tamm. (1996). Folding intermediates of a β-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism. Biochemistry 35: 12993-13000. 8855933
Mahalakshmi R. and Marassi FM. (2008). Orientation of the Escherichia coli outer membrane protein OmpX in phospholipid bilayer membranes determined by solid-State NMR. Biochemistry. 47(25):6531-8. 18512961
Mahalakshmi, R., C.M. Franzin, J. Choi, and F.M. Marassi. (2007). NMR structural studies of the bacterial outer membrane protein OmpX in oriented lipid bilayer membranes. Biochim. Biophys. Acta. 1768: 3216-3224. 17916325
Marassi, F.M. (2011). Mycobacterium tuberculosis Rv0899 defines a family of membrane proteins widespread in nitrogen-fixing bacteria. Proteins 79: 2946-2955. 21905117
Molle, V., N. Saint, S. Campagna, L. Kremer, E. Lea, P. Draper, and G. Molle. (2006). pH-dependent pore-forming activity of OmpATb from Mycobacterium tuberculosis and characterization of the channel by peptidic dissection. Mol. Microbiol. 61: 826-837. 16803587
Nestorovich, E.M., E. Sugawara, H. Nikaido, and S.M. Bezrukov. (2006). Pseudomonas aeruginosa porin OprF: properties of the channel. J. Biol. Chem. 281: 16230-16237. 16617058
Niederweis, M. (2003). Mycobacterial porins – new channel proteins in unique outer membranes. Mol. Microbiol. 49: 1167-1177. 12940978
Nikaido, H. (1992). Porins and specific channels of bacterial outer membranes. Mol. Microbiol. 6: 435-442. 1373213
Pautsch, A. and G.E. Schulz. (2000). High-resolution structure of the OmpA membrane domain. J. Mol. Biol. 298: 273-282. 10764596
Renault, M., O. Saurel, P. Demange, V. Reat, and A. Milon. (2010). Solution-state NMR spectroscopy of membrane proteins in detergent micelles: structure of the Klebsiella pneumoniae outer membrane protein A, KpOmpA. Methods Mol Biol 654: 321-339. 20665274
Saint, N., C. El Hamel, E. Dé, and G. Molle. (2000). Ion channel formation by N-terminal domain: a common feature of OprFs of Pseudomonas and OmpA of Escherichia coli. FEMS Microbiol. Lett. 190: 261-265. 11034289
Schulz, G.E. (1996). Porins: general to specific, native to engineered passive pores. Curr. Opin. Struc. Biol. 6: 485-490. 8794162
Senaratne, R.H., J. Mobasheri, K.G. Papavinasasundaram, P. Jenner, E.D.A. Lea, and P. Draper. (1998). Expression of a gene for a porin-like protein of the OmpA family from Mycobacterium tuberculosis H37Rv. J. Bacteriol. 180: 3541-3547. 9657995
Song, H., J. Huff, K. Janik, K. Walter, C. Keller, S. Ehlers, S.H. Bossmann, and M. Niederweis. (2011). Expression of the ompATb operon accelerates ammonia secretion and adaptation of Mycobacterium tuberculosis to acidic environments. Mol. Microbiol. 80: 900-918. 21410778
Sugawara, E. and H. Nikaido. (1992). Pore-forming activity of OmpA protein of Escherichia coli. J. Biol. Chem. 267: 2507-2511. 1370823
Sugawara, E. and H. Nikaido. (1994). OmpA protein of Escherichia coli outer membrane occurs in open and closed channel forms. J. Biol. Chem. 269: 17981-17987. 7517935
Sugawara, E., E.M. Nestorovich, S.M. Bezrukov, and H. Nikaido. (2006). Pseudomonas aeruginosa porin OprF exists in two different conformations. J. Biol. Chem. 281: 16220-16229. 16595653
Sugawara, E., K. Nagano, and H. Nikaido. (2010). Factors affecting the folding of Pseudomonas aeruginosa OprF porin into the one-domain open conformer. MBio 1:. 20978537
Sugawara, E., M. Steiert, S. Rouhani, and H. Nikaido. (1996). Secondary structure of the outer membrane proteins OmpA of Escherichia coli and OprF of Pseudomonas aeruginosa. J. Bacteriol. 178: 6067-6069. 8830709
Teriete, P., Y. Yao, A. Kolodzik, J. Yu, H. Song, M. Niederweis, and F.M. Marassi. (2010). Mycobacterium tuberculosis Rv0899 Adopts a Mixed alpha/β-Structure and Does Not Form a Transmembrane β-Barrel. Biochemistry 49: 2768-2777. 20199110
Veyron-Churlet, R., B. Brust, L. Kremer, and A.B. Blanc-Potard. (2011). Expression of OmpATb is dependent on small membrane proteins in Mycobacterium bovis BCG. Tuberculosis (Edinb) 91: 544-548. 21802366
White, P.A., S.P. Nair, M.J. Kim, M. Wilson, and B. Henderson. (1998). Molecular characterization of an outer membrane protein of Actinobacillus actinomycetemcomitans belonging to the OmpA family. Infect. Immun. 66: 369-372. 9423883