Outer Membrane Porins in Gram-Negative Bacteria: History
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Contributor:
Gang Zhou
,
Qian Wang
,
Yingsi Wang
,
Xia Wen
,
Hong Peng
,
Ruqun Peng
,
Qingshan Shi
,
Xiaobao Xie
,
Liangqiu Li

Gram-negative bacteria depend on their cell membranes for survival and environmental adaptation. They contain two membranes, one of which is the outer membrane (OM), which is home to several different outer membrane proteins (Omps). One class of important Omps is porins, which mediate the inflow of nutrients and several antimicrobial drugs. The microorganism’s sensitivity to antibiotics, which are predominantly targeted at internal sites, is greatly influenced by the permeability characteristics of porins.

  • gram-negative bacteria
  • outer membrane proteins
  • permeability properties
  • resistant mechanisms
  • multidrug-resistant bacteria

1. Introduction

The cell membranes of gram-negative bacteria are crucial for their survival and environmental adaptation. Generally, these membranes not only give gram-negative bacteria surface specificity but also operate as a functional and protective barrier for them [1]. Gram-negative bacteria have double membranes that include an outer membrane (OM) made up of outer membrane proteins (Omps) and other components [2][3]. In some circumstances, toxic substances, such as antibiotics, are prevented from transiting through the OM [4][5], creating a considerable obstacle to the eradication of gram-negative infections with traditional or novel antimicrobial agents.
Porins, a subclass of transmembrane pore-forming Omps, create tiny channels in the membrane and allow passive transport of hydrophilic compounds, which helps to modulate cellular permeability and increase antibiotic resistance [5][6][7][8]. In gram-negative bacteria, porins are the most prevalent Omps of the OM, and they can be divided into two groups based on how they function: non-specific porins and specific porins [5][9]. Porins have been studied in a variety of bacteria, including Acinetobacter baumannii [10], Escherichia coli [11][12], Neisseria gonorrhoeae [13][14], and Klebsiella pneumoniae [15][16]. Porins appear to play a role in the envelope integrity of gram-negative bacteria in addition to their role in the passive transport of a range of chemicals. For example, the non-specific porin of outer membrane protein A (OmpA) promotes the passive transport of numerous tiny molecules [17][18]. Additionally, OmpA also has a flexible periplasmic domain that interacts non-covalently with peptidoglycan [19], supporting the integrity of the envelope. Omps are usually encased by an annular shell of asymmetric lipids, which mediates higher-order Omp–lipid–Omp complexes with adjacent Omps, and the basic unit of supramolecular Omp assembly generally extends across the entire cell surface, coupling the OM’s required multifunctionality to its stability and impermeability [20].

2. OmpA

OmpA, a monomeric protein with a β-barrel shape that promotes the diffusion of negatively charged β-lactam antibiotics, has been demonstrated to be involved in drug resistance [10][21][22]. Furthermore, OmpA interacts with the bacterial cell wall to attach the outer membrane, and its C-terminal periplasmic domain non-covalently binds to the peptidoglycan layer via two conservative amino acids in OmpA, aspartate at position 271 and arginine at position 286 [23]. In addition, the periplasmic gap formed by disulfide linkages between OmpA’s β strands 4 and 5 in the N- and C-terminal fragments can increase the protein’s assembly efficiency in E. coli when the cysteine residues are aligned in the completely folded β-barrel [24]. The alleles of ompA were observed to have a considerable effect on cell surface hydrophobicity and charge in E. coli, which are important in stress response [25].
OmpA is a significant non-specific channel that helps various bacteria maintain the integrity of their membranes. In comparison to the wild type (WT) strain, an ompA mutant of A. baumannii showed a 2- to 3-fold reduced permeability to cephalothin/cephaloridine, and the minimal inhibitory concentrations (MICs) of nalidixic acid, chloramphenicol, trimethoprim, aztreonam, imipenem, colistin, and meropenem also decreased in the mutant [26][27][28][29][30]. OmpA’s impact on maintaining membrane integrity helps to explain these results because compromised membrane integrity can increase the intracellular diffusion of antibiotics [26][30]. The primary surface glycoproteins, Pgm6 and Pgm7, in Porphyromonas gingivalis have been demonstrated to cause resistance to the bactericidal activity of human cathelicidin LL-37 and are known as OmpA-like proteins [31]. The ompA mutant of E. coli was more sensitive to a variety of antibiotics, including β-lactams, amphenicols, glycopeptides, and lincosamides, compared to the WT [6]. Furthermore, researchers discovered that Citrobacter werkmanii showed increased 1,2-benzisothiazolin-3-one (BIT) resistance following the inactivation of ompA [32]. By preserving the stability of the outer membrane, OmpA also defends Salmonella Typhimurium from the two β-lactam antibiotics: ceftazidime and meropenem [33].
The flexible C-terminal domain of OmpA interacts non-covalently with peptidoglycan, which is critical for the maintenance of cell wall integrity [19]. OmpA’s C-terminal domains are entirely in charge of how this protein affects antibiotic resistance. The mutant strain of ompA1C, which has the C-terminal domain of OmpA chromosomally deleted, displayed a nearly identical phenotype to the ompA mutant of E. coli in antibiotic sensitivity [6]. The turgor of the bacterial envelope degrades in the absence of peptidoglycan interaction, increasing membrane permeability and antibiotic penetration [6]. In A. baumannii, OmpA typically serves as the main non-specific slow porin, along with β-lactamases and multidrug efflux pumps, such as AdeABC and AdeIJK, to exhibit high levels of intrinsic antibiotic resistance [34]. In addition, OmpA also connects to peptidoglycan (PG) from A. baumannii via its C-terminal region, where Asp271 and Arg286 link to the peptidoglycan’s diaminopimelic acid [35]. This interaction could regulate how bacteria produce outer membrane vesicles (OMVs) and preserve the stability of the membrane [36]. In order to combat antibiotic resistance, OMVs with OmpA in their membrane aggressively drain extracellular drugs [37][38][39].
The expression of OmpA can be regulated by several genes. In Aeromonas veronii, the lower transcription expression of ompA could be caused by the deletion of small protein B (SmpB) and four regions (−46 to −28 bp, −18 to +4 bp, +21 to +31 bp, and +48 to +59 bp) of the OmpA promoter combined by SmpB, which suggests that the SmpB protein was positively responsible for controlling OmpA expression at the stationary stage [40]. In A. baumannii, A1S_0316 displayed a higher affinity for binding to the OmpA promotor region than the global repressor H-NS, and it operates as an anti-repressor on the OmpA promotor region by preventing the binding of the AbH-NS protein [41]. OmpA in Stenotrophomonas maltophilia KJ plays its β-lactam susceptibility response through the sigma (P)-NagA-L1/L2 regulatory circuit, according to transcriptome analysis and real-time quantitative (qRT-PCR) experiments [42]. PG stress, which is generated by the loss of interaction between OmpA and PG layers, triggers the upregulation of RpoP (σP) and the expression of nagA. The increased NagA activity encourages the synthesis of repressor ligands, which are believed to partially displace activator ligands from AmpR and reduce the production of ceftazidime-induced β-lactamases [42]. More recently, it has been found that BlsA, a blue light-sensing protein, can impact the expressional levels of the ompA gene of A. baumannii under light conditions, which affects the efficiency of membrane penetration of lipophilic ethidium bromide (EtBr) and meropenem absorption [43].

3. OmpC

Another porin expressed by gram-negative bacteria is OmpC [44]. OmpC is composed of 16-stranded beta barrels with negatively charged amino acids that contribute to the formation of the porin’s eyelet and promote its size-exclusion and permeability properties [45]. OmpC facilitates both the entry and resistance of antibiotics, such as β-lactams, as well as the movement of hydrophilic substances with a low molecular weight over the outer membrane [44][46]. The mutation of OmpC damages structural integrity and alters OM permeability [7].
OmpC is involved in the transfer of antibiotics [47]. A slight rise in imipenem MIC is connected to the decrease or loss of OmpC in clinical isolates of Enterobacter aerogenes and Enterobacter cloacae [48][49]. The transcription and protein expression of OmpC were decreased in all carbapenem non-susceptible (CP-NS) E. coli isolates, and the carbapenem susceptibility of one isolate was restored by cloning the ompC gene [50]. OmpC mutants have enhanced cefotaxime resistance in clinical isolates of multidrug-resistant E. coli [47]. Meanwhile, the ompC deletion mutant of E. coli was resistant to streptomycin, fusidic acid, and nitrofurantoin; however, it was susceptible to carbapenems, cefepime, carbapenems, fourth-generation cephalosporins, imipenem, vancomycin, and puromycin [6][51][52].
One of the key mechanisms contributing to higher MICs for specific antibiotics was mutations in OmpC. Mutation prediction suggests that the primary contributor to carbapenem resistance is amino acid alterations, such as D192G, in the ompC of carbapenem-resistant E. coli [53]. Additionally, an adjacent region of the OmpC protein in E. coli contained a duplication of eight amino acids [52]. Based on specific R66, L67, Y64, F69, M65, and L67 locations, this duplication might be exploited to create salt bridges with the negatively charged residues lining the other side of the barrel wall and changing the pore’s electrostatic field [52]. Moreover, the following factors can be used to illustrate how the identified insertion affected OmpC function: disruption of tertiary or quaternary structure; preventing phage attachment and sterically restricting the movement of molecules; and disruption of the hydrophobicity and charge of porins by limiting their ability to interact with substances, such as antibiotics, to promote transport [52]. In avian pathogenic E. coli, quantitative real-time reverse transcription PCR (RT-qPCR) research revealed that EnvZ, the histidine kinase (HK) of OmpR/EnvZ, could affect the expression of biofilms and stress response genes, including ompC [54]. Small regulatory RNA (sRNA)-dependent control of gene expression enables cells to quickly and efficiently respond to different growth conditions [55]. Meanwhile, it was discovered that the 109-nucleotide MicC sRNA suppresses OmpC expression in E. coli by directly base-pairing to a 5′ untranslated region of the ompC mRNA, which requires the Hfq RNA chaperone to function [56].

4. OmpF

Another major porin expressed and extensively distributed in gram-negative bacteria OM is OmpF [57]. OmpF folds as a 16-stranded antiparallel β-barrel in tight homotrimers [58]. OmpF constructs its crystal structure with two asymmetric trimers in the tetragonal form [59].
It has been found that OmpF plays a crucial role in the permeation of short antimicrobial peptides (AMPs) by providing access to the lipopolysaccharide (LPS) binding site [60]. The antibiotic resistance of the ompF-deficient mutant indicates that OmpF is commonly the primary pathway by which antibiotics enter the OM [61]. Furthermore, it has been demonstrated that the non-specific porin OmpF of E. coli enables β-lactams (such as zwitterionic, ampicillin, and amoxicillin) and fluoroquinolones (such as enrofloxacin and norfloxacin) to penetrate the OM due to their strong affinity to OmpF [6][45][62][63], which partially depends on a two-step kinetic model. The dipolar molecule first generates an MD-ES0 conformation by aligning to the electric field within the OmpF channel before being reoriented into an MD-ES1 conformation for transport [64]. In addition, the electroosmotic flow rather than the electrophoretic force dominates the dynamics of antibiotic capture and transport of norfloxacin, ciprofloxacin, and enoxacin across a voltage-biased OmpF nanopore [65]. The ompF mutant was found to be resistant to many β-lactam antibiotics (including ampicillin and cefoxitin) in E. aerogenes [66], Pseudomonas aeruginosa [67], E. coli [6][68][69], Serratia marcescens [70], and K. pneumoniae [71]. OmpF also contributes to resisting numerous other different classes of antibiotics in addition to β-lactam antibiotics. In E. coli, the main route for enrofloxacin’s entrance is OmpF [58], and the reduced expression of OmpF led to the spread of quinolone resistance [72]. Studies on E. coli also showed that OmpF expression is activated in response to tetracycline [73][74]. Similarly, S. marcescens lacking OmpF had less antibiotic permeability and much higher nitrofurantoin MIC values [75]. Taken together, the ompF mutant was shown to be resistant to a wide range of antibiotics from various groups, such as β-lactams, tetracyclines, amphenicols, quinolones licosamides, and steroides [6].
Several works have demonstrated that the OmpF expression can be influenced by various systems or genes. The two-component system EnvZ/OmpR controls OmpF expression in response to nalidixic acid resistance [76]. In this system, activation of the response regulator OmpR leads to phosphorylation, and OmpR~P suppresses OmpF expression both at the transcriptional and post-transcriptional stages, the latter through the MicF sRNA [77]. It is known that the micF promoter region is bound by four transcriptional regulators: OmpR, MarA (the key transcriptional regulator encoded by the marRAB operon), SoxS, and Rob, which regulate the activation of micF expression. The micF gene, encoding a non-translated 93 nt antisense RNA, binds its target ompF mRNA and regulates ompF expression by inhibiting its translation and inducing degradation of the message in E. coli [78]. In addition, by binding to a conserved MarA-binding site in the promoter region of ompF, the transcriptional regulator of MarA can directly inhibit the expression of OmpF at the transcriptional level, or indirectly at the post-transcriptional level by activating the previously discussed MicF [79]. UxuR belongs to the GntR family of transcriptional regulators. A reduced amount of outer membrane porin OmpF was observed with the deletion of uxuR in E. coli, which suggests that UxuR regulates OmpF expression with unknown mechanisms [80]. Furthermore, researchers discovered that the OmpF upstream promoter in C. werkmanii and its transcription could be combined with and negatively regulated by the maltose metabolic regulator MalT for the first time, but researchers did not investigate how OmpF mutants might react to various antibiotics [81].

5. OmpW

An eight-stranded β-barrel with a hydrophobic channel is formed by OmpW, a member of the small Omp family [82][83]. OmpW plays a role in the transport of tiny hydrophobic chemicals, which helps to explain why some antimicrobials are less efficient at inhibiting bacterial growth [82].
In E. coli strains resistant to nalidixic acid, OmpW was discovered to be upregulated [76]. However, mass spectrometry and Western blotting results revealed that OmpW was downregulated in kanamycin-resistant E. coli K-12 strains, colistin/carbapenem-resistant A. baumannii mutants, and ceftriaxone-resistant S. typhimurium strains [82][84], and were once more consistent with the fact that porins restrict the entry of β-lactams into cells [85]. According to proteomic research, OmpW in E. coli has been associated with bacterial resistance to drugs such as ampicillin, tetracycline, and ceftriaxone [86]. E. coli also protects itself from enrofloxacin by reducing OmpW expression by restricting the transport and intracellular concentration of this drug [87]. Thereby, it was discovered that under tobramycin stress, the expression of ompW in A. baumannii was markedly downregulated [88]. In A. baumannii isolates, ompW expression increased and decreased in response to ciprofloxacin and imipenem, respectively [89].
The knockout of the ompW gene also demonstrated that OmpW displayed antimicrobial resistance in many bacteria. OmpW appears to be the receptor or a component of the receptor for colicin S4, chlortetracycline, neomycin, and ampicillin, as evidenced by the resistance of E. coli mutants lacking the OmpW to these drugs [90][91][92]. The methyl viologen sensitivity of ΔompW of S. typhimurium is 2.5 times greater than the WT [93]. The loss of OmpW in Actinobacillus pleuropneumoniae affects bacterial susceptibility to penicillin, kanamycin, and polymyxin B [94]. Meanwhile, the ompW of E. coli is also involved in the ethidium multidrug resistance gene E (emrE)-mediated substrate efflux process and is mechanistically connected to EmrE [95].
baeR, a regulator gene of the BaeSR two-component system, was discovered to affect OmpW expression in S. typhimurium [96]. It was discovered that an oxidative stress-related transcriptional SoxS factor negatively regulated OmpW in E. coli [97]. When specific environmental signals are detected by EnvZ, a phosphotransfer from EnvZ’s His243 to OmpR’s Asp55 causes an increase in the cellular level of phosphorylated OmpR (OmpR-P), which implies an active state of EnvZ/OmpR. This state changes the OMP composition and leads to differential expression of ompW and other OMP genes, increasing resistance to β-lactams, while OmpR directly suppresses ompW in Salmonella enteritidis [98].

6. OmpX

OmpX was first described for E. cloacae [99], but its homologs, such as PagC, Lom, Rck, Ail, and y1324, have been found in other gram-negative bacteria, including S. typhimurium [100], E. coli [101], E. aerogenes [102], and Yersinia pestis [103]. An OmpX protein precursor with 172 amino acid residues and a 23 amino acid residue N-terminal signal sequence is encoded by the ompX gene in E. cloacae [99]. According to the X-ray crystallography and NMR structures, OmpX from E. coli forms an eight-stranded antiparallel β-barrel in the DHPC micelles [104]. Recently, it was found that OmpX folding is influenced by both the insert length within a set of equivalent loop insertions and its hydrophobic character [105].
Numerous investigations have revealed that ompX is crucial for regulating how bacterial strains respond to antimicrobials [102][103]. The loss of ompX in a fimbriated strain of E. coli PC31 resulted in antibiotic resistance to numerous antibiotics, which was attributed to increased exopolysaccharide production [75]. The deletion of ompX in E. coli improved resistance to a variety of hydrophobic antibiotics such as amikacin, cephalothin, gentamicin, novobiocin, nalidixic acid, and sulfonamides [75]. Similar to this, researchers also discovered that OmpX in C. werkmanii regulates resistance to drugs, such as tetracycline, ciprofloxacin, chloramphenicol, lincomycin, rifampicin, aminoglycosides (kanamycin and streptomycin), and β-lactams (ampicillin, carbenicillin, ceftazidime, and imipenem) [106]. Meanwhile, the overexpression of OmpX in E. aerogenes results in higher β-lactam resistance, which can be explained by a significant decrease in Omp36 porin [107]. OmpX was found to be 1.7 times more abundant in drug-resistant S. typhimurium isolates than in drug-sensitive isolates [108]. These findings imply that the under or overexpression of ompX affects hydrophobic chemical transport across the membrane but does not impact substrate preference [75]. However, the lack of ompX in E. cloacae had no appreciable effect on porin regulation or susceptibility to β-lactam antibiotics [99].
The ceftriaxone resistance functions of the outer membrane protein STM3031 (Ail/OmpX-like protein) of S. typhimurium are largely achieved via increasing AcrD efflux pump activity [109]. In addition, hydrogen peroxide stress enhanced the expression of ompX mRNA but not OmpX protein in S. typhimurium, showing that ompX is post-transcriptionally regulated in response to hydrogen peroxide [110]. Meanwhile, three sRNAs (MicA, CyaR, and OxyS) were required in an Hfq-dependent manner to stabilize the ompX mRNA [110].

This entry is adapted from the peer-reviewed paper 10.3390/microorganisms11071690

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