Hopanoids as functional analogues of cholesterol in bacterial membranes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 38, 2015, Pages 11971-11976

  Sáenz, James P ^a   Grosser, Daniel ^a   Bradley, Alexander S ^b   Lagny, Thibaut J ^a   Lavrynenko, Oksana ^a   Broda, Martyna ^a,c   Simons, Kai ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF WROC AW   (Poland)

Author keywords

Hopanoids; Membrane order; Methylobacterium; Multidrug efflux; Outer membrane

Indexed keywords

CHOLESTEROL; GLYCOLIPID; HOPANOID; SPHINGOLIPID; DIPLOPTEROL; LIPID; LIPID A; PHOSPHOLIPID; TRITERPENE;

BACTERIAL OUTER MEMBRANE; BILAYER MEMBRANE; CONFERENCE PAPER; LIPOGENESIS; METHYLOBACTERIUM EXTORQUENS; METHYLOBACTERIUM ORGANOPHILUM; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; CELL MEMBRANE; CHEMISTRY; ENERGY METABOLISM; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CELL MEMBRANE; CHOLESTEROL; ENERGY METABOLISM; LIPID A; LIPIDS; METHYLOBACTERIUM EXTORQUENS; PHOSPHOLIPIDS; TRITERPENES;

EID: 84942908911     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1515607112     Document Type: Article

References (69)

1. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: Where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112-124.
2. Kaiser H-J, et al. (2011) Molecular convergence of bacterial and eukaryotic surface order. J Biol Chem 286(47):40631-40637.
3. Ohtomo Y, Kakegawa T, Ishida A, Nagase T, Rosing MT (2014) Evidence for biogenic graphite in early Archaean Isua metasedimentary rocks. Nat Geosci 7(1):25-28.
4. Brocks JJ, Logan GA, Buick R, Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285(5430):1033-1036.
5. Ourisson G, Albrecht P (1992) Hopanoids. 1. Geohopanoids: The most abundant natural products on earth? Acc Chem Res 25(9):398-402.
6. Briggs DEG, Summons RE (2014) Ancient biomolecules: Their origins, fossilization, and role in revealing the history of life. BioEssays 36(5):482-490.
7. Kannenberg EL, Poralla K (1999) Hopanoid biosynthesis and function in bacteria. Naturwissenschaften 86(4):168-176.
8. Ourisson G, Rohmer M, Poralla K (1987) Prokaryotic hopanoids and other polyterpenoid sterol surrogates. Annu Rev Microbiol 41(1):301-333.
9. Wendt KU, Poralla K, Schulz GE (1997) Structure and function of a squalene cyclase. Science 277(5333):1811-1815.
10. Frickey T, Kannenberg E (2009) Phylogenetic analysis of the triterpene cyclase protein family in prokaryotes and eukaryotes suggests bidirectional lateral gene transfer. Environ Microbiol 11(5):1224-1241.
11. Mouritsen OG, Zuckermann MJ (2004) What's so special about cholesterol? Lipids 39(11):1101-1113.
12. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327(5961):46-50.
13. Kannenberg E, Blume A, McElhaney RN, Poralla K (1983) Monolayer and calorimetric studies of phosphatidylcholines containing branched-chain fatty-acids and of their interactions with cholesterol and with a bacterial hopanoid in model membranes. Biochim Biophys Acta 733(1):111-116.
14. Poralla K, Kannenberg E, Blume A (1980) A glycolipid containing hopane isolated from the acidophilic, thermophilic Bacillus acidocaldarius, has a cholesterol-like function in membranes. FEBS Lett 113(1):107-110.
15. Sáenz JP, Sezgin E, Schwille P, Simons K (2012) Functional convergence of hopanoids and sterols in membrane ordering. Proc Natl Acad Sci USA 109(35):14236-14240.
16. Wu C-H, Bialecka-Fornal M, Newman DK (2015) Methylation at the C-2 position of hopanoids increases rigidity in native bacterial membranes. eLife, 10.7554/eLife.05663.
17. Poger D, Mark AE (2013) The relative effect of sterols and hopanoids on lipid bilayers: When comparable is not identical. J Phys Chem B 117(50):16129-16140.
18. Rohmer M, Bouvier-Nave P, Ourisson G (1984) Distribution of hopanoid triterpenes in prokaryotes. J Gen Microbiol 130:1137-1150.
19. Pearson A, Flood Page SR, Jorgenson TL, Fischer WW, Higgins MB (2007) Novel hopanoid cyclases from the environment. Environ Microbiol 9(9):2175-2188.
20. Welander PV, et al. (2009) Hopanoids play a role in membrane integrity and pH homeostasis in Rhodopseudomonas palustris TIE-1. J Bacteriol 191(19):6145-6156.
21. Kulkarni G, Wu C-H, Newman DK (2013) The general stress response factor EcfG regulates expression of the C-2 hopanoid methylase HpnP in Rhodopseudomonas palustris TIE-1. J Bacteriol 195(11):2490-2498.
22. Malott RJ, Steen-Kinnaird BR, Lee TD, Speert DP (2012) Identification of hopanoid biosynthesis genes involved in polymyxin resistance in Burkholderia multivorans. Antimicrob Agents Chemother 56(1):464-471.
23. Malott RJ, et al. (2014) Fosmidomycin decreases membrane hopanoids and potentiates the effects of colistin on Burkholderia multivorans clinical isolates. Antimicrob Agents Chemother 58(9):5211-5219.
24. Schmerk CL, Bernards MA, Valvano MA (2011) Hopanoid production is required for low-pH tolerance, antimicrobial resistance, and motility in Burkholderia cenocepacia. J Bacteriol 193(23):6712-6723.
25. López D, Kolter R (2010) Functional microdomains in bacterial membranes. Genes Dev 24(17):1893-1902.
26. Lorenzen W, Ring MW, Schwär G, Bode HB (2009) Isoprenoids are essential for fruiting body formation in Myxococcus xanthus. J Bacteriol 191(18):5849-5853.
27. Bradley A, Pearson A, Sáenz J, Marx C (2010) Adenosylhopane: The first intermediate in hopanoid side chain biosynthesis. Org Geochem 41(10):1075-1081.
28. Renoux JM, Rohmer M (1985) Prokaryotic triterpenoids. New bacteriohopanetetrol cyclitol ethers from the methylotrophic bacterium Methylobacterium-organophilum. Eur J Biochem 151(2):405-410.
29. Hancock IC, Williams KM (1986) The outer membrane of Methylobacterium organophilum. Microbiology 132(3):599-610.
30. Parasassi T, De Stasio G, d'Ubaldo A, Gratton E (1990) Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys J 57(6):1179-1186.
31. Sezgin E, Sadowski T, Simons K (2014) Measuring lipid packing of model and cellular membranes with environment sensitive probes. Langmuir 30(27):8160-8166.
32. Olsen I, Jantzen E (2001) Sphingolipids in bacteria and fungi. Anaerobe 7(2):103-112.
33. Nikaido H, Vaara M (1985) Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49(1):1-32.
34. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67(4):593-656.
35. Coskun Ü, Grzybek M, Drechsel D, Simons K (2011) Regulation of human EGF receptor by lipids. Proc Natl Acad Sci USA 108(22):9044-9048.
36. Welander PV, et al. (2012) Identification and characterization of Rhodopseudomonas palustris TIE-1 hopanoid biosynthesis mutants. Geobiology 10(2):163-177.
37. Nikaido H (1996) Multidrug efflux pumps of gram-negative bacteria. J Bacteriol 178(20):5853-5859.
38. Loh B, Grant C, Hancock RE (1984) Use of the fluorescent probe 1-N-phenylnaphthylamine to study the interactions of aminoglycoside antibiotics with the outer membrane of Pseudomonas aeruginosa. Antimicrob Agents Chemother 26(4):546-551.
39. van den Berg van Saparoea HB, Lubelski J, vanMerkerk R, Mazurkiewicz PS, Driessen A J M (2005) Proton motive force-dependent Hoechst 33342 transport by the ABC transporter LmrA of Lactococcus lactis. Biochemistry 44(51):16931-16938.
40. Shapiro AB, Ling V (1995) Reconstitution of drug transport by purified P-glycoprotein. J Biol Chem 270(27):16167-16175.
41. Shapiro AB, Corder AB, Ling V (1997) P-glycoprotein-mediated Hoechst 33342 transport out of the lipid bilayer. Eur J Biochem 250(1):115-121.
42. Kim M, et al. (2002) The multidrug resistance transporter ABCG2(breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietic stem cells. Clin Cancer Res 8(1):22-28.
43. Doughty DM, et al. (2011) The RND-family transporter, HpnN, is required for hopanoid localization to the outer membrane of Rhodopseudomonas palustris TIE-1. Proc Natl Acad Sci USA 108(45):E1045-E1051.
44. Doughty DM, Hunter RC, Summons RE, Newman DK (2009) 2-Methylhopanoids are maximally produced in akinetes of Nostoc punctiforme: Geobiological implications. Geobiology 7(5):524-532.
45. Simonin P, Jürgens UJ, Rohmer M (1996) Bacterial triterpenoids of the hopane series from the prochlorophyte Prochlorothrix hollandica and their intracellular localization. Eur J Biochem 241(3):865-871.
46. Jahnke LL, Stan-Lotter H, Kato K, Hochstein LI (1992) Presence of methyl sterol and bacteriohopanepolyol in an outer-membrane preparation from Methylococcus capsulatus (Bath). J Gen Microbiol 138(8):1759-1766.
47. Silipo A, et al. (2014) Covalently linked hopanoid-lipid A improves outer-membrane resistance of a Bradyrhizobium symbiont of legumes. Nat Commun 5:5106.
48. Komaniecka I, et al. (2014) Occurrence of an unusual hopanoid-containing lipid A among lipopolysaccharides from Bradyrhizobium species. J Biol Chem 289(51):35644-35655.
49. Rexroth S, et al. (2011) The plasma membrane of the cyanobacterium Gloeobacter violaceus contains segregated bioenergetic domains. Plant Cell 23(6):2379-2390.
50. Berry AM, et al. (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 90(13):6091-6094.
51. LaRocca TJ, et al. (2013) Proving lipid rafts exist: membrane domains in the prokaryote Borrelia burgdorferi have the same properties as eukaryotic lipid rafts. PLoS Pathog 9(5):e1003353.
52. Zgurskaya HI, Krishnamoorthy G, Ntreh A, Lu S (2011) Mechanism and Function of the Outer Membrane Channel TolC in Multidrug Resistance and Physiology of Enterobacteria. Front Microbiol 2:189.
53. Oswald C, Pos KM (2011) Drug resistance: A periplasmic ménage à trois. Chem Biol 18(4):405-407.
54. Koronakis V, Eswaran J, Hughes C (2004) Structure and function of TolC: The bacterial exit duct for proteins and drugs. Annu Rev Biochem 73:467-489.
55. Du D, et al. (2014) Structure of the AcrAB-TolC multidrug efflux pump. Nature 509(7501):512-515.
56. Lingwood D, et al. (2011) Cholesterol modulates glycolipid conformation and receptor activity. Nat Chem Biol 7(5):260-262.
57. Bramkamp M, Lopez D (2015) Exploring the existence of lipid rafts in bacteria. Microbiol Mol Biol Rev 79(1):81-100.
58. Strahl H, Bürmann F, Hamoen LW (2014) The actin homologue MreB organizes the bacterial cell membrane. Nat Commun 5:3442.
59. Lee MC, Chou HH, Marx CJ (2009) Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Evolution 63(11):2816-2830.
60. Marx CJ (2008) Development of a broad-host-range sacB-based vector for unmarked allelic exchange. BMC Res Notes 1(1):1.
61. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911-917.
62. Christian AE, Haynes MP, Phillips MC, Rothblat GH (1997) Use of cyclodextrins for manipulating cellular cholesterol content. J Lipid Res 38(11):2264-2272.
63. Grzybek M, Kubiak J, Łach A, Przybyło M, Sikorski AF (2009) A raft-associated species of phosphatidylethanolamine interacts with cholesterol comparably to sphingomyelin. A Langmuir-Blodgett monolayer study. PLoS One 4(3):e5053.
64. Karkhanis YD, Zeltner JY, Jackson JJ, Carlo DJ (1978) A new and improved microassay to determine 2-keto-3-deoxyoctonate in lipopolysaccharide of Gram-negative bacteria. Anal Biochem 85(2):595-601.
65. Schindelin J, et al. (2012) Fiji: An open-source platform for biological-image analysis. Nat Methods 9(7):676-682.
66. Ejsing CS, et al. (2009) Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc Natl Acad Sci USA 106(7):2136-2141.
67. Herzog R, et al. (2012) LipidXplorer: A software for consensual cross-platform lipidomics. PLoS One 7(1):e29851.
68. Gibson DG (2011) Enzymatic assembly of overlapping DNA fragments. Methods in Enzymology 498:349-361.
69. Delaney NF, et al. (2013) Development of an optimized medium, strain and highthroughput culturing methods for Methylobacterium extorquens. PLoS One 8(4):e62957.