Increased Expression of the Bacterial Glycolipid MPIase is Required for Efficient Protein Translocation Across Membranes in Cold Conditions

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2019 Apr 3

PMID 30936205

Citations 6

Authors

Katsuhiro Sawasato

Sonomi Suzuki

Ken-Ichi Nishiyama

Affiliations

Soon will be listed here.

Abstract

Protein integration into and translocation across biological membranes are vital events for organismal survival and are fundamentally conserved among many organisms. Membrane protein integrase (MPIase) is a glycolipid that drives membrane protein integration into the cytoplasmic membrane in MPIase also stimulates protein translocation across the membrane, but how its expression is regulated is incompletely understood. In this study, we found that the expression level of MPIase significantly increases in the cold (<25 °C), whereas that of the SecYEG translocon does not. Using previously created gene-knockout strains, we also found that either the or gene, both encoding rate-limiting enzymes for MPIase biosynthesis, is responsible for the increase in the MPIase expression. Furthermore, using pulse-chase experiments and protein integration assays, we demonstrated that the increase in MPIase levels is important for efficient protein translocation, but not for protein integration. We conclude that MPIase expression is required to stimulate protein translocation in cold conditions and is controlled by and gene expression.

Citing Articles

Key contributions of a glycolipid to membrane protein integration.

Shimamoto K, Fujikawa K, Osawa T, Mori S, Nomura K, Nishiyama K Proc Jpn Acad Ser B Phys Biol Sci. 2024; 100(7):387-413.

PMID: 39085064 PMC: 11413397. DOI: 10.2183/pjab.100.026.

Structures, functions, and syntheses of glycero-glycophospholipids.

Osawa T, Fujikawa K, Shimamoto K Front Chem. 2024; 12:1353688.

PMID: 38389730 PMC: 10881803. DOI: 10.3389/fchem.2024.1353688.

CdsA, a CDP-diacylglycerol synthase involved in phospholipid and glycolipid MPIase biosynthesis, possesses multiple initiation codons.

Hikage R, Sekiya Y, Sawasato K, Nishiyama K Genes Cells. 2024; 29(4):347-355.

PMID: 38351722 PMC: 11448367. DOI: 10.1111/gtc.13104.

The Role of the Universally Conserved ATPase YchF/Ola1 in Translation Regulation during Cellular Stress.

Landwehr V, Milanov M, Hong J, Koch H Microorganisms. 2022; 10(1).

PMID: 35056463 PMC: 8779481. DOI: 10.3390/microorganisms10010014.

The bacterial protein YidC accelerates MPIase-dependent integration of membrane proteins.

Sasaki M, Nishikawa H, Suzuki S, Moser M, Huber M, Sawasato K J Biol Chem. 2019; 294(49):18898-18908.

PMID: 31662434 PMC: 6901323. DOI: 10.1074/jbc.RA119.011248.

References

Nishiyama K, Mizushima S, Tokuda H . The carboxyl-terminal region of SecE interacts with SecY and is functional in the reconstitution of protein translocation activity in Escherichia coli. J Biol Chem. 1992; 267(10):7170-6. View

Tani K, Tokuda H, Mizushima S . Translocation of ProOmpA possessing an intramolecular disulfide bridge into membrane vesicles of Escherichia coli. Effect of membrane energization. J Biol Chem. 1990; 265(28):17341-7. View

Sugai R, Takemae K, Tokuda H, Nishiyama K . Topology inversion of SecG is essential for cytosolic SecA-dependent stimulation of protein translocation. J Biol Chem. 2007; 282(40):29540-8. DOI: 10.1074/jbc.M704716200. View

Wickner W, Driessen A, Hartl F . The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu Rev Biochem. 1991; 60:101-24. DOI: 10.1146/annurev.bi.60.070191.000533. View

Nishiyama K, Suzuki T, Tokuda H . Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell. 1996; 85(1):71-81. DOI: 10.1016/s0092-8674(00)81083-1. View

Marr A, Ingraham J . EFFECT OF TEMPERATURE ON THE COMPOSITION OF FATTY ACIDS IN ESCHERICHIA COLI. J Bacteriol. 1962; 84(6):1260-7. PMC: 278056. DOI: 10.1128/jb.84.6.1260-1267.1962. View

du Plessis D, Nouwen N, Driessen A . The Sec translocase. Biochim Biophys Acta. 2010; 1808(3):851-65. DOI: 10.1016/j.bbamem.2010.08.016. View

Sawasato K, Sato R, Nishikawa H, Iimura N, Kamemoto Y, Fujikawa K . CdsA is involved in biosynthesis of glycolipid MPIase essential for membrane protein integration in vivo. Sci Rep. 2019; 9(1):1372. PMC: 6362211. DOI: 10.1038/s41598-018-37809-8. View

Nishiyama K, Hanada M, Tokuda H . Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature. EMBO J. 1994; 13(14):3272-7. PMC: 395223. DOI: 10.1002/j.1460-2075.1994.tb06628.x. View

10.

Nishiyama K, Shimamoto K . Glycolipozyme membrane protein integrase (MPIase): recent data. Biomol Concepts. 2014; 5(5):429-38. DOI: 10.1515/bmc-2014-0030. View

11.

Kaufmann A, Manting E, Veenendaal A, Driessen A, van der Does C . Cysteine-directed cross-linking demonstrates that helix 3 of SecE is close to helix 2 of SecY and helix 3 of a neighboring SecE. Biochemistry. 1999; 38(28):9115-25. DOI: 10.1021/bi990539d. View

12.

Murakami A, Nakatogawa H, Ito K . Translation arrest of SecM is essential for the basal and regulated expression of SecA. Proc Natl Acad Sci U S A. 2004; 101(33):12330-5. PMC: 514405. DOI: 10.1073/pnas.0404907101. View

13.

Tamura Y, Harada Y, Nishikawa S, Yamano K, Kamiya M, Shiota T . Tam41 is a CDP-diacylglycerol synthase required for cardiolipin biosynthesis in mitochondria. Cell Metab. 2013; 17(5):709-18. PMC: 3654088. DOI: 10.1016/j.cmet.2013.03.018. View

14.

Samuelson J, Chen M, Jiang F, Moller I, Wiedmann M, Kuhn A . YidC mediates membrane protein insertion in bacteria. Nature. 2000; 406(6796):637-41. DOI: 10.1038/35020586. View

15.

Breyton C, Haase W, Rapoport T, Kuhlbrandt W, Collinson I . Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature. 2002; 418(6898):662-5. DOI: 10.1038/nature00827. View

16.

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

17.

Kiefer D, Kuhn A . YidC-mediated membrane insertion. FEMS Microbiol Lett. 2018; 365(12). DOI: 10.1093/femsle/fny106. View

18.

Shimizu H, Nishiyama K, Tokuda H . Expression of gpsA encoding biosynthetic sn-glycerol 3-phosphate dehydrogenase suppresses both the LB- phenotype of a secB null mutant and the cold-sensitive phenotype of a secG null mutant. Mol Microbiol. 1998; 26(5):1013-21. DOI: 10.1046/j.1365-2958.1997.6392003.x. View

19.

Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M . Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006; 2:2006.0008. PMC: 1681482. DOI: 10.1038/msb4100050. View

20.

Sato R, Sawasato K, Nishiyama K . YnbB is a CdsA paralogue dedicated to biosynthesis of glycolipid MPIase involved in membrane protein integration. Biochem Biophys Res Commun. 2019; 510(4):636-642. DOI: 10.1016/j.bbrc.2019.01.145. View