Advertisement

Exploring the Mechanism of Viral Peptide-Induced Membrane Fusion

  • Gourab Prasad Pattnaik
  • Geetanjali Meher
  • Hirak ChakrabortyEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1112)

Abstract

Membrane fusion is essential in several cellular processes in the existence of eukaryotic cells such as cellular trafficking, compartmentalization, intercellular communication, sexual reproduction, cell division, and endo- and exocytosis. Membrane fusion proceeds in model membranes as well as biological membranes through the rearrangement of lipids. The stalk hypothesis provides a picture of the general nature of lipid rearrangement based on mechanical properties and phase behavior of water-lipid mesomorphic systems. In spite of extensive research on exploring the mechanism of membrane fusion, a clear molecular understanding of intermediate and pore formation is lacking. In addition, the mechanism by which proteins and peptides reduce the activation energy for stalk and pore formation is not yet clear though there are several propositions on how they catalyze membrane fusion. In this review, we have discussed about various putative functions of fusion peptides by which they reduce activation barrier and thus promote membrane fusion. A careful analysis of the discussed effects of fusion peptides on membranes might open up new possibilities for better understanding of the membrane fusion mechanism.

Keywords

Membrane fusion Bending energy Void space Membrane curvature Depth-dependent membrane ordering Fusion peptide 

Notes

Acknowledgements

This work was supported by research grants from the University Grants Commission, New Delhi (File No. F.4-5(138-FRP)/2014(BSR)), and Science and Engineering Research Board, Department of Science and Technology (SERB-DST), New Delhi (File No. ECR/2015/000195). H. C. and G. M. thank the University Grants Commission for UGC-Assistant Professor position and UGC-BSR Research Fellowship, respectively. G. P. P. thanks SERB-DST for his project assistantship. We thank the Department of Science and Technology, New Delhi, and UGC for providing instrument facility to the School of Chemistry, Sambalpur University, under the FIST and DRS programs, respectively. We gratefully acknowledge the critical comments and discussions by Dr. S. N. Sahu and the members of Chakraborty group.

References

  1. Abrams FS, London E (1993) Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry 32:10826–10831CrossRefGoogle Scholar
  2. Abrams FS, Chattopadhyay A, London E (1992) Determination of the location of fluorescent probes attached to fatty acids using parallax analysis of fluorescence quenching: effect of carboxyl ionization state and environment on depth. Biochemistry 31:5322–5327CrossRefGoogle Scholar
  3. Basanez G, Goni FM, Alonso A (1998) Effect of single chain lipids on phospholipase C-promoted vesicle fusion. A test for the stalk hypothesis of membrane fusion. Biochemistry 37:3901–3908CrossRefGoogle Scholar
  4. Boucrot E, Pick A, Camdere G, Liska N, Evergren E, McMahon HT, Kozlov MM (2012) Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149:124–136CrossRefGoogle Scholar
  5. Campelo F, McMahon HT, Kozlov MM (2008) The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys J 95:2325–2339CrossRefGoogle Scholar
  6. Chakraborty H, Tarafdar PK, Bruno MJ, Sengupta T, Lentz BR (2012) Activation thermodynamics of poly(ethylene glycol)-mediated model membrane fusion support mechanistic models of stalk and pore formation. Biophys J 102:2751–2760CrossRefGoogle Scholar
  7. Chakraborty H, Tarafdar PK, Klapper DG, Lentz BR (2013) Wild-type and mutant hemagglutinin fusion peptides alter bilayer structure as well as kinetics and activation thermodynamics of stalk and pore formation differently: mechanistic implications. Biophys J 105:2495–2506CrossRefGoogle Scholar
  8. Chakraborty H, Sengupta T, Lentz BR (2014) pH alters PEG-mediated fusion of phosphatidylethanolamine-containing vesicles. Biophys J 107:1327–1338CrossRefGoogle Scholar
  9. Chakraborty H, Haldar S, Chong PL, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2015) Depth-dependent organization and dynamics of archaeal and eukaryotic membranes: development of membrane anisotropy gradient with natural evolution. Langmuir 31:11591–11597CrossRefGoogle Scholar
  10. Chakraborty H, Lentz BR, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2017) Depth-dependent membrane ordering by hemagglutinin fusion peptide promotes fusion. J Phys Chem B 121:1640–1648CrossRefGoogle Scholar
  11. Chanturiya A, Leikina E, Zimmerberg J, Chernomordik LV (1999) Short-chain alcohols promote an early stage of membrane hemifusion. Biophys J 77:2035–2045CrossRefGoogle Scholar
  12. Chen Z, Rand RP (1998) Comparative study of the effects of several n-alkanes on phospholipid hexagonal phases. Biophys J 74:944–952CrossRefGoogle Scholar
  13. Chernomordik L (1996) Non-bilayer lipids and biological fusion intermediates. Chem Phys Lipids 81:203–213CrossRefGoogle Scholar
  14. Chernomordik LV, Kozlov MM (2003) Protein-lipid interplay in fusion and fission of biological membranes. Annu Rev Biochem 72:175–207CrossRefGoogle Scholar
  15. Chernomordik LV, Kozlov MM (2005) Membrane hemifusion: crossing a chasm in two leaps. Cell 123:375–382CrossRefGoogle Scholar
  16. Chernomordik LV, Kozlov MM (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15:675–683CrossRefGoogle Scholar
  17. Danieli T, Pelletier SL, Henis YI, White JM (1996) Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J Cell Biol 133:559–569CrossRefGoogle Scholar
  18. Davies SM, Epand RF, Bradshaw JP, Epand RM (1998) Modulation of lipid polymorphism by the feline leukemia virus fusion peptide: implications for the fusion mechanism. Biochemistry 37:5720–5729CrossRefGoogle Scholar
  19. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657CrossRefGoogle Scholar
  20. Dimitrov DS, Golding H, Blumenthal R (1991) Initial stages of HIV-1 envelope glycoprotein-mediated cell fusion monitored by a new assay based on redistribution of fluorescent dyes. AIDS Res Hum Retrovir 7:799–805CrossRefGoogle Scholar
  21. Earp LJ, Delos SE, Park HE, White JM (2005) The many mechanisms of viral membrane fusion proteins. Curr Top Microbiol Immunol 285:25–66PubMedGoogle Scholar
  22. Epand RM (1985) Diacylglycerols, lysolecithin, or hydrocarbons markedly alter the bilayer to hexagonal phase transition temperature of phosphatidylethanolamines. Biochemistry 24:7092–7095CrossRefGoogle Scholar
  23. Epand RM (2003) Fusion peptides and the mechanism of viral fusion. Biochim Biophys Acta 1614:116–121CrossRefGoogle Scholar
  24. Epand RM, Epand RF (1994) Relationship between the infectivity of influenza virus and the ability of its fusion peptide to perturb bilayers. Biochem Biophys Res Commun 202:1420–1425CrossRefGoogle Scholar
  25. Epand RF, Martin I, Ruysschaert JM, Epand RM (1994) Membrane orientation of the SIV fusion peptide determines its effect on bilayer stability and ability to promote membrane fusion. Biochem Biophys Res Commun 205:1938–1943CrossRefGoogle Scholar
  26. Freed EO, Myers DJ, Risser R (1990) Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Proc Natl Acad Sci U S A 87:4650–4654CrossRefGoogle Scholar
  27. Ge M, Freed JH (2009) Fusion peptide from influenza hemagglutinin increases membrane surface order: an electron-spin resonance study. Biophys J 96:4925–4934CrossRefGoogle Scholar
  28. Gething MJ, Doms RW, York D, White J (1986) Studies on the mechanism of membrane fusion: site-specific mutagenesis of the hemagglutinin of influenza virus. J Cell Biol 102:11–23CrossRefGoogle Scholar
  29. Haldar S, Kombrabail M, Krishnamoorthy G, Chattopadhyay A (2012) Depth-dependent heterogeneity in membranes by fluorescence lifetime distribution analysis. J Phys Chem Lett 3:2676–2681CrossRefGoogle Scholar
  30. Haque ME, Koppaka V, Axelsen PH, Lentz BR (2005) Properties and structures of the influenza and HIV fusion peptides on lipid membranes: implications for a role in fusion. Biophys J 89:3183–3194CrossRefGoogle Scholar
  31. Haque ME, Chakraborty H, Koklic T, Komatsu H, Axelsen PH, Lentz BR (2011) Hemagglutinin fusion peptide mutants in model membranes: structural properties, membrane physical properties, and PEG-mediated fusion. Biophys J 101:1095–1104CrossRefGoogle Scholar
  32. Hughson FM (1997) Enveloped viruses: a common mode of membrane fusion? Curr Biol 7:R565–R569CrossRefGoogle Scholar
  33. Jensen D, Schekman R (2011) COPII-mediated vesicle formation at a glance. J Cell Sci 124:1–4CrossRefGoogle Scholar
  34. Kirchhausen T (2000) Three ways to make a vesicle. Nat Rev Mol Cell Biol 1:187–198CrossRefGoogle Scholar
  35. Kozlov MM, Leikin SL, Chernomordik LV, Markin VS, Chizmadzhev YA (1989) Stalk mechanism of vesicle fusion. Intermixing of aqueous contents. Eur Biophys J 17:121–129CrossRefGoogle Scholar
  36. Kozlov MM, Campelo F, Liska N, Chernomordik LV, Marrink SJ, McMahon HT (2014) Mechanisms shaping cell membranes. Curr Opin Cell Biol 29:53–60CrossRefGoogle Scholar
  37. Kucerka N, Liu Y, Chu N, Petrache HI, Tristram-Nagle S, Nagle JF (2005a) Structure of fully hydrated fluid phase DMPC and DLPC lipid bilayers using X-ray scattering from oriented multilamellar arrays and from unilamellar vesicles. Biophys J 88:2626–2637CrossRefGoogle Scholar
  38. Kucerka N, Tristram-Nagle S, Nagle JF (2005b) Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J Membr Biol 208:193–202CrossRefGoogle Scholar
  39. Kucerka N, Tristram-Nagle S, Nagle JF (2006) Closer look at structure of fully hydrated fluid phase DPPC bilayers. Biophys J 90:L83–L85CrossRefGoogle Scholar
  40. Lai AL, Freed JH (2014) HIV gp41 fusion peptide increases membrane ordering in a cholesterol-dependent fashion. Biophys J 106:172–181CrossRefGoogle Scholar
  41. Lai AL, Park H, White JM, Tamm LK (2006) Fusion peptide of influenza hemagglutinin requires a fixed angle boomerang structure for activity. J Biol Chem 281:5760–5770CrossRefGoogle Scholar
  42. Lee J, Lentz BR (1997) Evolution of lipidic structures during model membrane fusion and the relation of this process to cell membrane fusion. Biochemistry 36:6251–6259CrossRefGoogle Scholar
  43. Lee J, Lentz BR (1998) Secretory and viral fusion may share mechanistic events with fusion between curved lipid bilayers. Proc Natl Acad Sci U S A 95:9274–9279CrossRefGoogle Scholar
  44. Leikin S, Kozlov MM, Fuller NL, Rand RP (1996) Measured effects of diacylglycerol on structural and elastic properties of phospholipid membranes. Biophys J 71:2623–2632CrossRefGoogle Scholar
  45. Lentz BR, Malinin V, Haque ME, Evans K (2000) Protein machines and lipid assemblies: current views of cell membrane fusion. Curr Opin Struct Biol 10:607–615CrossRefGoogle Scholar
  46. Li Y, Han X, Lai AL, Bushweller JH, Cafiso DS, Tamm LK (2005) Membrane structures of the hemifusion-inducing fusion peptide mutant G1S and the fusion-blocking mutant G1V of influenza virus hemagglutinin suggest a mechanism for pore opening in membrane fusion. J Virol 79:12065–12076CrossRefGoogle Scholar
  47. Liu Y, Nagle JF (2004) Diffuse scattering provides material parameters and electron density profiles of biomembranes. Phys Rev E Stat Nonlinear Soft Matter Phys 69:040901CrossRefGoogle Scholar
  48. Malinin VS, Lentz BR (2004) Energetics of vesicle fusion intermediates: comparison of calculations with observed effects of osmotic and curvature stresses. Biophys J 86:2951–2964CrossRefGoogle Scholar
  49. Markin VS, Albanesi JP (2002) Membrane fusion: stalk model revisited. Biophys J 82:693–712CrossRefGoogle Scholar
  50. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12:517–533CrossRefGoogle Scholar
  51. McMahon HT, Boucrot E (2015) Membrane curvature at a glance. J Cell Sci 128:1065–1070CrossRefGoogle Scholar
  52. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–499CrossRefGoogle Scholar
  53. Primakoff P, Myles DG (2002) Penetration, adhesion, and fusion in mammalian sperm-egg interaction. Science 296:2183–2185CrossRefGoogle Scholar
  54. Rand RP, Fuller NL, Gruner SM, Parsegian VA (1990) Membrane curvature, lipid segregation, and structural transitions for phospholipids under dual-solvent stress. Biochemistry 29:76–87CrossRefGoogle Scholar
  55. Risselada HJ, Kutzner C, Grubmuller H (2011) Caught in the act: visualization of SNARE-mediated fusion events in molecular detail. Chembiochem 12:1049–1055CrossRefGoogle Scholar
  56. Sengupta T, Chakraborty H, Lentz BR (2014) The transmembrane domain peptide of vesicular stomatitis virus promotes both intermediate and pore formation during PEG-mediated vesicle fusion. Biophys J 107:1318–1326CrossRefGoogle Scholar
  57. Shchelokovskyy P, Tristram-Nagle S, Dimova R (2011) Effect of the HIV-1 fusion peptide on the mechanical properties and leaflet coupling of lipid bilayers. New J Phys 13:25004CrossRefGoogle Scholar
  58. Siegel DP (1999) The modified stalk mechanism of lamellar/inverted phase transitions and its implications for membrane fusion. Biophys J 76:291–313CrossRefGoogle Scholar
  59. Siegel DP, Epand RM (2000) Effect of influenza hemagglutinin fusion peptide on lamellar/inverted phase transitions in dipalmitoleoylphosphatidylethanolamine: implications for membrane fusion mechanisms. Biochim Biophys Acta 1468:87–98CrossRefGoogle Scholar
  60. Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569CrossRefGoogle Scholar
  61. Smrt ST, Draney AW, Lorieau JL (2015) The influenza hemagglutinin fusion domain is an amphipathic helical hairpin that functions by inducing membrane curvature. J Biol Chem 290:228–238CrossRefGoogle Scholar
  62. Sollner T, Rothman JE (1994) Neurotransmission: harnessing fusion machinery at the synapse. Trends Neurosci 17:344–348CrossRefGoogle Scholar
  63. Stein KK, Primakoff P, Myles D (2004) Sperm-egg fusion: events at the plasma membrane. J Cell Sci 117:6269–6274CrossRefGoogle Scholar
  64. Tenchov BG, MacDonald RC, Lentz BR (2013) Fusion peptides promote formation of bilayer cubic phases in lipid dispersions. An x-ray diffraction study. Biophys J 104:1029–1037CrossRefGoogle Scholar
  65. Tristram-Nagle S, Nagle JF (2007) HIV-1 fusion peptide decreases bending energy and promotes curved fusion intermediates. Biophys J 93:2048–2055CrossRefGoogle Scholar
  66. Verkleij AJ, Post JA (2000) Membrane phospholipid asymmetry and signal transduction. J Membr Biol 178:1–10CrossRefGoogle Scholar
  67. Walter A, Yeagle PL, Siegel DP (1994) Diacylglycerol and hexadecane increase divalent cation-induced lipid mixing rates between phosphatidylserine large unilamellar vesicles. Biophys J 66:366–376CrossRefGoogle Scholar
  68. Yang L, Huang HW (2003) A rhombohedral phase of lipid containing a membrane fusion intermediate structure. Biophys J 84:1808–1817CrossRefGoogle Scholar
  69. Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7:9–19CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Gourab Prasad Pattnaik
    • 1
  • Geetanjali Meher
    • 1
  • Hirak Chakraborty
    • 1
    Email author
  1. 1.School of ChemistrySambalpur UniversityBurlaIndia

Personalised recommendations