1.
2.
3.
4.
5.
6.
7.
8.
9.
Strisovsky K. 2016. Why cells need Intramembrane proteases - a
mechanistic perspective. FEBS J 283:1837–1845. https://doi.org/10.1111/
febs.13638
Kühnle N, Dederer V, Lemberg MK. 2019. Intramembrane proteolysis at a
glance: from signalling to protein degradation. J Cell Sci 132:jcs217745.
https://doi.org/10.1242/jcs.217745
Kroos L, Akiyama Y. 2013. Biochemical and structural insights into
intramembrane metalloprotease mechanisms. Biochim Biophys Acta
1828:2873–2885. https://doi.org/10.1016/j.bbamem.2013.03.032
Weihofen A, Martoglio B. 2003. Intramembrane-cleaving proteases:
Controlled liberation of proteins and bioactive peptides. Trends Cell Biol
13:71–78. https://doi.org/10.1016/s0962-8924(02)00041-7
Sun L, Li X, Shi Y. 2016. Structural biology of intramembrane proteases:
mechanistic insights from rhomboid and S2P to γ-Secretase. Curr Opin
Struct Biol 37:97–107. https://doi.org/10.1016/j.sbi.2015.12.008
Schneider JS, Glickman MS. 2013. Function of Site-2 proteases in
bacteria and bacterial pathogens. Biochim Biophys Acta 1828:2808–
2814. https://doi.org/10.1016/j.bbamem.2013.04.019
Chen G, Zhang X. 2010. New insights into S2P signaling cascades:
regulation, variation, and conservation. Protein Sci 19:2015–2030. https:/
/doi.org/10.1002/pro.496
Kanehara K, Akiyama Y, Ito K. 2001. Characterization of the yaeL gene
product and its S2P-protease motifs in Escherichia coli. Gene 281:71–79.
https://doi.org/10.1016/s0378-1119(01)00823-x
Kanehara K, Ito K, Akiyama Y. 2002. YaeL (EcfE) activates the σE pathway
of stress response through a site-2 cleavage of anti-σE, RseA. Genes Dev
16:2147–2155. https://doi.org/10.1101/gad.1002302
July/August Volume 14
Issue 4
10.
11.
12.
13.
14.
15.
16.
17.
Alba BM, Leeds JA, Onufryk C, Lu CZ, Gross CA. 2002. DegS and YaeL
participate sequentially in the cleavage of RseA to activate the σEdependent extracytoplasmic stress response. Genes Dev 16:2156–2168.
https://doi.org/10.1101/gad.1008902
Ades SE. 2008. Regulation by destruction: design of the σE envelope
stress response. Curr Opin Microbiol 11:535–540. https://doi.org/10.
1016/j.mib.2008.10.004
Yokoyama T, Niinae T, Tsumagari K, Imami K, Ishihama Y, Hizukuri Y,
Akiyama Y. 2021. The Escherichia coli S2P intramembrane protease RseP
regulates ferric citrate uptake by cleaving the sigma factor regulator
FecR. J Biol Chem 296:100673. https://doi.org/10.1016/j.jbc.2021.100673
Saito A, Hizukuri Y, Matsuo E, Chiba S, Mori H, Nishimura O, Ito K,
Akiyama Y. 2011. Post-liberation cleavage of signal peptides is catalyzed
by the Site-2 protease (S2P) in bacteria. Proc Natl Acad Sci U S A
108:13740–13745. https://doi.org/10.1073/pnas.1108376108
Hizukuri Y, Oda T, Tabata S, Tamura-Kawakami K, Oi R, Sato M, Takagi J,
Akiyama Y, Nogi T. 2014. A structure-based model of substrate
discrimination by a noncanonical PDZ tandem in the intramembranecleaving protease RseP. Structure 22:326–336. https://doi.org/10.1016/j.
str.2013.12.003
Hizukuri Y, Akiyama Y. 2012. PDZ domains of RseP are not essential for
sequential cleavage of RseA or stress-induced σE activation in vivo. Mol
Microbiol 86:1232–1245. https://doi.org/10.1111/mmi.12053
Kanehara K, Ito K, Akiyama Y. 2003. YaeL proteolysis of RseA is controlled
by the PDZ domain of YaeL and a Gln-rich region of RseA. EMBO J
22:6389–6398. https://doi.org/10.1093/emboj/cdg602
Imaizumi Y, Takanuki K, Miyake T, Takemoto M, Hirata K, Hirose M, Oi R,
Kobayashi T, Miyoshi K, Aruga R, Yokoyama T, Katagiri S, Matsuura H,
10.1128/mbio.01086-23 19
Downloaded from https://journals.asm.org/journal/mbio on 04 February 2024 by 2001:2f8:181:8184::fa.
Supplemental Material
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
Iwasaki K, Kato T, Kaneko MK, Kato Y, Tajiri M, Akashi S, Nureki O, Hizukuri
Y, Akiyama Y, Nogi T. 2022. Mechanistic insights into intramembrane
proteolysis by E. coli Site-2 protease Homolog RseP. Sci Adv 8:eabp9011.
https://doi.org/10.1126/sciadv.abp9011
Miyake T, Hizukuri Y, Akiyama Y. 2020. Involvement of a membranebound amphiphilic helix in substrate discrimination and binding by an
Escherichia coli S2P peptidase RseP. Front Microbiol 11:607381. https://
doi.org/10.3389/fmicb.2020.607381
Akiyama K, Hizukuri Y, Akiyama Y. 2017. Involvement of a conserved GFG
motif region in substrate binding by RseP, an Escherichia coli S2P
protease. Mol Microbiol 104:737–751. https://doi.org/10.1111/mmi.
13659
Akiyama K, Mizuno S, Hizukuri Y, Mori H, Nogi T, Akiyama Y. 2015. Roles
of the membrane-reentrant β-hairpin-like loop of RseP protease in
selective substrate cleavage. eLife 4:e08928. https://doi.org/10.7554/
eLife.08928
Weidenbach K, Gutt M, Cassidy L, Chibani C, Schmitz RA. 2022. Small
proteins in archaea, a mainly unexplored world. J Bacteriol
204:e0031321. https://doi.org/10.1128/JB.00313-21
Sberro H, Fremin BJ, Zlitni S, Edfors F, Greenfield N, Snyder MP,
Pavlopoulos GA, Kyrpides NC, Bhatt AS. 2019. Large-scale analyses of
human microbiomes reveal thousands of small, novel genes. Cell
178:1245–1259. https://doi.org/10.1016/j.cell.2019.07.016
Yadavalli SS, Yuan J. 2022. Bacterial small membrane proteins: The Swiss
Army knife of regulators at the lipid bilayer. J Bacteriol 204:e0034421.
https://doi.org/10.1128/JB.00344-21
Hemm MR, Weaver J, Storz G. 2020. Escherichia coli small Proteome.
EcoSal Plus 9:1128/ecosalplus.ESP-0031–2019. https://doi.org/10.1128/
ecosalplus.esp-0031-2019
Ito K, Akiyama Y. 2005. Cellular functions, mechanism of action, and
regulation of FtsH protease. Annu Rev Microbiol 59:211–231. https://doi.
org/10.1146/annurev.micro.59.030804.121316
Akiyama Y. 2009. Quality control of cytoplasmic membrane proteins in
Escherichia coli. J Biochem 146:449–454. https://doi.org/10.1093/jb/
mvp071
Pedersen K, Gerdes K. 1999. Multiple hok genes on the chromosome of
Escherichia coli. Mol Microbiol 32:1090–1102. https://doi.org/10.1046/j.
1365-2958.1999.01431.x
Wilmaerts D, Bayoumi M, Dewachter L, Knapen W, Mika JT, Hofkens J,
Dedecker P, Maglia G, Verstraeten N, Michiels J. 2018. The persistenceinducing toxin HokB forms dynamic pores that cause ATP leakage. mBio
9:e00744-18. https://doi.org/10.1128/mBio.00744-18
Wilmaerts D, Dewachter L, De Loose PJ, Bollen C, Verstraeten N, Michiels
J. 2019. HokB monomerization and membrane repolarization control
persister awakening. Mol Cell 75:1031–1042. https://doi.org/10.1016/j.
molcel.2019.06.015
Verstraeten N, Knapen WJ, Kint CI, Liebens V, Van den Bergh B,
Dewachter L, Michiels JE, Fu Q, David CC, Fierro AC, Marchal K, Beirlant J,
Versées W, Hofkens J, Jansen M, Fauvart M, Michiels J. 2015. Obg and
membrane depolarization are part of a microbial bet-hedging strategy
that leads to antibiotic tolerance. Mol Cell 59:9–21. https://doi.org/10.
1016/j.molcel.2015.05.011
Dewachter L, Fauvart M, Michiels J. 2019. Bacterial heterogeneity and
antibiotic survival: Understanding and combatting persistence and
heteroresistance. Mol Cell 76:255–267. https://doi.org/10.1016/j.molcel.
2019.09.028
Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting
transmembrane protein topology with a hidden markov model:
application to complete genomes. J Mol Biol 305:567–580. https://doi.
org/10.1006/jmbi.2000.4315
Tsirigos KD, Peters C, Shu N, Käll L, Elofsson A. 2015. The TOPCONS web
server for consensus prediction of membrane protein topology and
signal peptides. Nucleic Acids Res 43:W401–7. https://doi.org/10.1093/
nar/gkv485
Fontaine F, Fuchs RT, Storz G. 2011. Membrane localization of small
proteins in Escherichia coli. J Biol Chem 286:32464–32474. https://doi.
org/10.1074/jbc.M111.245696
Akiyama Y, Kanehara K, Ito K. 2004. RseP (YaeL), an Escherichia coli RIP
protease, cleaves transmembrane sequences. EMBO J 23:4434–4442.
https://doi.org/10.1038/sj.emboj.7600449
July/August Volume 14
Issue 4
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
Flynn JM, Levchenko I, Sauer RT, Baker TA. 2004. Modulating substrate
choice: The SspB adaptor delivers a regulator of the extracytoplasmicstress response to the AAA+ protease ClpXP for degradation. Genes Dev
18:2292–2301. https://doi.org/10.1101/gad.1240104
Chaba R, Grigorova IL, Flynn JM, Baker TA, Gross CA. 2007. Design
principles of the proteolytic cascade governing the σE-mediated
envelope stress response in Escherichia coli: keys to graded, buffered,
and rapid signal transduction. Genes Dev 21:124–136. https://doi.org/
10.1101/gad.1496707
Shimizu Y, Kanamori T, Ueda T. 2005. Protein synthesis by pure
translation systems. Methods 36:299–304. https://doi.org/10.1016/j.
ymeth.2005.04.006
Shimizu Y, Inoue A, Tomari Y, Suzuki T, Yokogawa T, Nishikawa K, Ueda T.
2001. Cell-free translation reconstituted with purified components. Nat
Biotechnol 19:751–755. https://doi.org/10.1038/90802
Fujii Y, Kaneko M, Neyazaki M, Nogi T, Kato Y, Takagi J. 2014. PA tag: A
versatile protein tagging system using a super high affinity antibody
against a dodecapeptide derived from human podoplanin. Protein Expr
Purif 95:240–247. https://doi.org/10.1016/j.pep.2014.01.009
Harms A, Brodersen DE, Mitarai N, Gerdes K. 2018. Toxins, targets, and
triggers: an overview of toxin-antitoxin biology. Mol Cell 70:768–784.
https://doi.org/10.1016/j.molcel.2018.01.003
Gerdes K, Rasmussen PB, Molin S. 1986. Unique type of plasmid
maintenance function: postsegregational killing of plasmid-free cells.
Proc Natl Acad Sci U S A 83:3116–3120. https://doi.org/10.1073/pnas.83.
10.3116
Ogura T, Hiraga S. 1983. Mini-F plasmid genes that couple host cell
division to plasmid proliferation. Proc Natl Acad Sci U S A 80:4784–4788.
https://doi.org/10.1073/pnas.80.15.4784
Loh SM, Cram DS, Skurray RA. 1988. Nucleotide sequence and
transcriptional analysis of a third function (Flm) involved in F-plasmid
maintenance.
Gene
66:259–268.
https://doi.org/10.1016/03781119(88)90362-9
Safarian S, Hahn A, Mills DJ, Radloff M, Eisinger ML, Nikolaev A, MeierCredo J, Melin F, Miyoshi H, Gennis RB, Sakamoto J, Langer JD, Hellwig P,
Kühlbrandt W, Michel H. 2019. Active site rearrangement and structural
divergence in prokaryotic respiratory oxidases. Science 366:100–104.
https://doi.org/10.1126/science.aay0967
Fisher RA, Gollan B, Helaine S. 2017. Persistent bacterial infections and
persister cells. Nat Rev Microbiol 15:453–464. https://doi.org/10.1038/
nrmicro.2017.42
Karimova G, Davi M, Ladant D. 2012. The β-lactam resistance protein Blr,
a small membrane polypeptide, is a component of the Escherichia coli
cell division machinery. J Bacteriol 194:5576–5588. https://doi.org/10.
1128/JB.00774-12
Lippa AM, Goulian M. 2009. Feedback inhibition in the PhoQ/PhoP
signaling system by a membrane peptide. PLoS Genet 5:e1000788.
https://doi.org/10.1371/journal.pgen.1000788
Bomjan R, Zhang M, Zhou D, DiRita VJ. 2019. YshB promotes intracellular
replication and is required for Salmonella virulence . J Bacteriol
201:e00314–19. https://doi.org/10.1128/JB.00314-19
Ellermeier CD, Losick R. 2006. Evidence for a novel protease governing
regulated intramembrane proteolysis and resistance to antimicrobial
peptides in Bacillus subtilis. Genes Dev 20:1911–1922. https://doi.org/10.
1101/gad.1440606
Hastie JL, Williams KB, Ellermeier CD. 2013. The activity of σv, an
extracytoplasmic function σ factor of Bacillus subtilis, is controlled by
regulated proteolysis of the anti-σ factor RsiV. J Bacteriol 195:3135–3144.
https://doi.org/10.1128/JB.00292-13
Bramkamp M, Weston L, Daniel RA, Errington J. 2006. Regulated
intramembrane proteolysis of FtsL protein and the control of cell
division in Bacillus subtilis. Mol Microbiol 62:580–591. https://doi.org/10.
1111/j.1365-2958.2006.05402.x
Matson JS, DiRita VJ. 2005. Degradation of the membrane-localized
virulence activator TcpP by the YaeL protease in Vibrio cholerae. Proc Natl
Acad Sci U S A 102:16403–16408. https://doi.org/10.1073/pnas.
0505818102
Almagro-Moreno S, Kim TK, Skorupski K, Taylor RK, Casadesús J. 2015.
Proteolysis of virulence regulator ToxR is associated with entry of Vibrio
cholerae into a dormant state. PLoS Genet 11:e1005145. https://doi.org/
10.1371/journal.pgen.1005145
10.1128/mbio.01086-23 20
Downloaded from https://journals.asm.org/journal/mbio on 04 February 2024 by 2001:2f8:181:8184::fa.
mBio
Research Article
55.
56.
mBio
Sklar JG, Makinoshima H, Schneider JS, Glickman MS. 2010. M.
tuberculosis intramembrane protease Rip1 controls transcription
through three anti-sigma factor substrates. Mol Microbiol 77:605–617.
https://doi.org/10.1111/j.1365-2958.2010.07232.x
Mukherjee P, Sureka K, Datta P, Hossain T, Barik S, Das KP, Kundu M, Basu
J. 2009. Novel role of Wag31 in protection of mycobacteria under
oxidative stress. Mol Microbiol 73:103–119. https://doi.org/10.1111/j.
1365-2958.2009.06750.x
July/August Volume 14
Issue 4
57.
58.
Schneider JS, Sklar JG, Glickman MS. 2014. The Rip1 protease of
Mycobacterium tuberculosis controls the SigD regulon. J Bacteriol
196:2638–2645. https://doi.org/10.1128/JB.01537-14
Beverin S, Sheppard DE, Park SS. 1971. D-Fucose as a gratuitous inducer
of the L-arabinose operon in strains of Escherichia coli B-r mutant in gene
araC. J Bacteriol 107:79–86. https://doi.org/10.1128/jb.107.1.79-86.1971
10.1128/mbio.01086-23 21
Downloaded from https://journals.asm.org/journal/mbio on 04 February 2024 by 2001:2f8:181:8184::fa.
Research Article
...