OpenLB
Open Library of Bioscience
Advanced Search
Science advances
Jul 22, 2022;8 (29): eabn1440.

Measles and Nipah virus assembly: Specific lipid binding drives matrix polymerization.

Michael J Norris, Monica L Husby, William B Kiosses, Jieyun Yin, Roopashi Saxena, Linda J Rennick, Anja Heiner, Stephanie S Harkins, Rudramani Pokhrel, Sharon L Schendel, Kathryn M Hastie, Sara Landeras-Bueno, Zhe Li Salie, Benhur Lee, Prem P Chapagain, Andrea Maisner, W Paul Duprex, Robert V Stahelin, Erica Ollmann Saphire
Author Information
  1. Michael J Norris: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA. ORCID
  2. Monica L Husby: Department of Medicinal Chemistry and Molecular Pharmacology, Purdue Institute of Inflammation, Immunology and Infectious Disease, Purdue University, West Lafayette, IN 47907, USA. ORCID
  3. William B Kiosses: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA. ORCID
  4. Jieyun Yin: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA. ORCID
  5. Roopashi Saxena: Department of Medicinal Chemistry and Molecular Pharmacology, Purdue Institute of Inflammation, Immunology and Infectious Disease, Purdue University, West Lafayette, IN 47907, USA. ORCID
  6. Linda J Rennick: Center for Vaccine Research, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261, USA. ORCID
  7. Anja Heiner: Institute of Virology, Philipps University Marburg, Marburg, Germany.
  8. Stephanie S Harkins: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA. ORCID
  9. Rudramani Pokhrel: Department of Physics, Florida International University, Miami, FL 33199, USA. ORCID
  10. Sharon L Schendel: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA. ORCID
  11. Kathryn M Hastie: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA. ORCID
  12. Sara Landeras-Bueno: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA.
  13. Zhe Li Salie: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA. ORCID
  14. Benhur Lee: Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA. ORCID
  15. Prem P Chapagain: Department of Physics, Florida International University, Miami, FL 33199, USA. ORCID
  16. Andrea Maisner: Institute of Virology, Philipps University Marburg, Marburg, Germany.
  17. W Paul Duprex: Center for Vaccine Research, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261, USA. ORCID
  18. Robert V Stahelin: Department of Medicinal Chemistry and Molecular Pharmacology, Purdue Institute of Inflammation, Immunology and Infectious Disease, Purdue University, West Lafayette, IN 47907, USA. ORCID
  19. Erica Ollmann Saphire: Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, CA 92037, USA. ORCID
PMID: 35857835 DOI: 10.1126/sciadv.abn1440

Abstract

Measles virus, Nipah virus, and multiple other paramyxoviruses cause disease outbreaks in humans and animals worldwide. The paramyxovirus matrix (M) protein mediates virion assembly and budding from host cell membranes. M is thus a key target for antivirals, but few high-resolution structures of paramyxovirus M are available, and we lack the clear understanding of how viral M proteins interact with membrane lipids to mediate viral assembly and egress that is needed to guide antiviral design. Here, we reveal that M proteins associate with phosphatidylserine and phosphatidylinositol 4,5-bisphosphate [PI(4,5)P] at the plasma membrane. Using x-ray crystallography, electron microscopy, and molecular dynamics, we demonstrate that PI(4,5)P binding induces conformational and electrostatic changes in the M protein surface that trigger membrane deformation, matrix layer polymerization, and virion assembly.

References

  1. J Gen Virol. 2019 Dec;100(12):1593-1594 [PMID: 31609197]
  2. J Biol Chem. 2002 Mar 15;277(11):8822-6 [PMID: 11781329]
  3. Biochem Biophys Res Commun. 2007 Apr 20;355(4):1096-101 [PMID: 17336269]
  4. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6232-6 [PMID: 6292897]
  5. PLoS Pathog. 2010 Nov 11;6(11):e1001186 [PMID: 21085610]
  6. Acta Crystallogr D Biol Crystallogr. 2006 Apr;62(Pt 4):439-50 [PMID: 16552146]
  7. Annu Rev Biophys. 2008;37:465-87 [PMID: 18573091]
  8. Annu Rev Cell Dev Biol. 2019 Oct 6;35:111-129 [PMID: 31340125]
  9. Biophys J. 2012 Jun 6;102(11):2517-25 [PMID: 22713567]
  10. Int J Biochem Cell Biol. 2010 Sep;42(9):1416-29 [PMID: 20398786]
  11. Biophys J. 2019 Apr 2;116(7):1239-1247 [PMID: 30902368]
  12. Viruses. 2020 Oct 03;12(10): [PMID: 33022924]
  13. Proc Natl Acad Sci U S A. 1980 Jan;77(1):239-43 [PMID: 6244547]
  14. Trends Cell Biol. 2006 Oct;16(10):538-46 [PMID: 16962778]
  15. J Virol. 2014 Jul;88(13):7602-17 [PMID: 24760890]
  16. PLoS One. 2016 Feb 22;11(2):e0149982 [PMID: 26900944]
  17. Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):13996-4000 [PMID: 22891297]
  18. Proc Natl Acad Sci U S A. 2006 Jul 25;103(30):11364-9 [PMID: 16840558]
  19. FEBS Lett. 2007 May 22;581(11):2089-97 [PMID: 17434167]
  20. J Virol. 2001 May;75(9):4399-401 [PMID: 11287589]
  21. J Gen Virol. 2000 May;81(Pt 5):1305-12 [PMID: 10769073]
  22. J Mol Graph. 1996 Feb;14(1):33-8, 27-8 [PMID: 8744570]
  23. J Virol. 2014 Apr;88(7):3802-14 [PMID: 24429367]
  24. Adv Virus Res. 2017;98:1-55 [PMID: 28433050]
  25. J Pediatric Infect Dis Soc. 2016 Mar;5(1):7-13 [PMID: 26908486]
  26. J Virol. 2013 Mar;87(6):3143-54 [PMID: 23283941]
  27. Nat Methods. 2017 Mar;14(3):290-296 [PMID: 28165473]
  28. Nat Rev Mol Cell Biol. 2008 Feb;9(2):112-24 [PMID: 18216768]
  29. Cell Microbiol. 2019 Mar;21(3):e12996 [PMID: 30585688]
  30. Nucleic Acids Res. 2007 Jul;35(Web Server issue):W522-5 [PMID: 17488841]
  31. Cancer Res. 1994 May 1;54(9):2419-23 [PMID: 8162590]
  32. Biochim Biophys Acta. 2002 Apr 12;1561(2):129-34 [PMID: 11997113]
  33. Nat Struct Mol Biol. 2011 Jul 10;18(8):902-7 [PMID: 21743456]
  34. J Virol. 2015 Sep;89(18):9440-53 [PMID: 26136573]
  35. MMWR Morb Mortal Wkly Rep. 2018 Nov 30;67(47):1323-1329 [PMID: 30496160]
  36. Nat Commun. 2015 Jan 08;6:5974 [PMID: 25569184]
  37. J Virol. 2020 Dec 9;95(1): [PMID: 33028721]
  38. Elife. 2017 Jun 02;6: [PMID: 28574338]
  39. Curr Opin Cell Biol. 2020 Apr;63:57-67 [PMID: 31972475]
  40. J Struct Biol. 2017 Jun;198(3):163-176 [PMID: 28193500]
  41. J Comput Chem. 2005 Dec;26(16):1781-802 [PMID: 16222654]
  42. J Virol. 2016 Jan 20;90(7):3650-60 [PMID: 26792745]
  43. Biophys J. 2017 Nov 7;113(9):2004-2015 [PMID: 29117524]
  44. J Virol. 1999 Nov;73(11):9568-75 [PMID: 10516065]
  45. Viruses. 2014 Aug 07;6(8):3019-54 [PMID: 25105277]
  46. Biotechniques. 2006 Jan;40(1):61-6 [PMID: 16454041]
  47. Nat Methods. 2012 Jun 28;9(7):676-82 [PMID: 22743772]
  48. Science. 2006 Jul 21;313(5785):347-51 [PMID: 16857939]
  49. Biochem J. 1993 Aug 15;294 ( Pt 1):1-14 [PMID: 8363559]
  50. Virology. 2021 Sep;561:17-27 [PMID: 34130198]
  51. J Virol. 2017 May 26;91(12): [PMID: 28356535]
  52. Nature. 2005 Dec 1;438(7068):597-604 [PMID: 16319879]
  53. Protein Sci. 2021 Jan;30(1):70-82 [PMID: 32881101]
  54. Structure. 2014 Jan 7;22(1):136-48 [PMID: 24316400]
  55. J Mol Biol. 2007 Sep 21;372(3):774-97 [PMID: 17681537]
  56. Annu Rev Virol. 2020 Sep 29;7(1):447-473 [PMID: 32991264]
  57. Langmuir. 2011 Jan 4;27(1):304-11 [PMID: 21141948]
  58. PLoS One. 2018 Sep 21;13(9):e0204532 [PMID: 30240452]
  59. J Virol. 2015 Dec 16;90(5):2514-22 [PMID: 26676785]
  60. Curr Biol. 2009 Jan 27;19(2):95-107 [PMID: 19150238]
  61. Nature. 1992 Jan 30;355(6359):472-5 [PMID: 18481394]
  62. Proc Natl Acad Sci U S A. 2013 Jul 2;110(27):11133-8 [PMID: 23776214]
  63. Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501 [PMID: 20383002]
  64. Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41 [PMID: 11517324]
  65. Sci Rep. 2016 Jan 12;6:19125 [PMID: 26753796]
  66. PLoS Pathog. 2011 Jan 27;7(1):e1001263 [PMID: 21304593]
  67. Annu Rev Biophys Biomol Struct. 2005;34:119-51 [PMID: 15869386]
  68. Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4441-6 [PMID: 19251668]
  69. PLoS Pathog. 2019 Apr 29;15(4):e1007733 [PMID: 31034506]
  70. Science. 2008 Jan 11;319(5860):210-3 [PMID: 18187657]
  71. Acta Crystallogr D Biol Crystallogr. 2012 Apr;68(Pt 4):368-80 [PMID: 22505257]
  72. Proc Natl Acad Sci U S A. 2004 Oct 12;101(41):14889-94 [PMID: 15465916]
  73. Nat Commun. 2018 Apr 30;9(1):1736 [PMID: 29712906]
  74. Vet Res. 2017 Oct 26;48(1):68 [PMID: 29073919]
  75. Antimicrob Agents Chemother. 2013 Jul;57(7):3358-68 [PMID: 23650168]
  76. Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21 [PMID: 20124702]
  77. Virus Res. 2002 Feb 26;83(1-2):1-12 [PMID: 11864737]
  78. Biochim Biophys Acta Biomembr. 2017 Oct;1859(10):2012-2020 [PMID: 28711356]
  79. J Virol. 2007 Dec;81(23):12859-71 [PMID: 17898060]
  80. Soft Matter. 2016 Jun 21;12(23):5164-71 [PMID: 27070906]
  81. Virology. 2017 Jan 15;501:127-135 [PMID: 27915128]
  82. J Biol Chem. 2018 Apr 27;293(17):6230-6240 [PMID: 29588369]
  83. Virology. 1988 Sep;166(1):123-32 [PMID: 3413981]
  84. Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):293-302 [PMID: 21460447]
  85. Structure. 2015 May 5;23(5):873-881 [PMID: 25865245]
  86. Viruses. 2018 Aug 20;10(8): [PMID: 30127286]
  87. Phys Chem Chem Phys. 2016 Oct 19;18(41):28409-28417 [PMID: 27757455]
  88. Proc Natl Acad Sci U S A. 2012 Jan 3;109(1):173-8 [PMID: 22184226]
  89. PLoS Pathog. 2015 Mar 17;11(3):e1004739 [PMID: 25782006]
  90. J Gen Virol. 1994 May;75 ( Pt 5):1031-42 [PMID: 8176365]
  91. J Virol. 2004 Sep;78(18):9705-12 [PMID: 15331703]
  92. Mol Cell. 2018 Sep 6;71(5):653-673 [PMID: 30193094]
  93. Methods Mol Biol. 2013;1009:261-71 [PMID: 23681541]
  94. Biophys J. 2001 Jun;80(6):2898-911 [PMID: 11371462]
  95. Elife. 2020 Oct 05;9: [PMID: 33016878]
  96. J Gen Virol. 2014 Mar;95(Pt 3):539-548 [PMID: 24296468]
  97. EMBO J. 1998 Jul 15;17(14):3899-908 [PMID: 9670007]
  98. J Virol. 2018 Jun 13;92(13): [PMID: 29695428]
  99. J Virol. 2017 Jul 27;91(16): [PMID: 28592541]
  100. Lancet Glob Health. 2019 Apr;7(4):e472-e481 [PMID: 30797735]
  101. J Cell Biol. 2007 Nov 19;179(4):627-33 [PMID: 18025300]
  102. Nat Methods. 2017 Jan;14(1):71-73 [PMID: 27819658]
  103. Curr Protoc Bioinformatics. 2006 Oct;Chapter 5:Unit-5.6 [PMID: 18428767]
  104. J Comput Chem. 2014 Oct 15;35(27):1997-2004 [PMID: 25130509]
  105. Proc Soc Exp Biol Med. 1949 May;71(1):50-2 [PMID: 18151474]
  106. J Virol. 2013 Dec;87(24):13343-53 [PMID: 24089563]
  107. Methods Mol Biol. 2006;328:97-112 [PMID: 16785643]
  108. J Virol. 2015 Dec 30;90(6):3074-85 [PMID: 26719280]

Grants

  1. R01 AI123449/NIAID NIH HHS
  2. S10 OD027043/NIH HHS
  3. R01 AI081077/NIAID NIH HHS
  4. P30 GM133894/NIGMS NIH HHS
  5. S10 OD021831/NIH HHS
  6. R01 AI125536/NIAID NIH HHS
Journal Article
Article has an altmetric score of 140

Word Cloud

Created with Highcharts 10.0.0Mvirusmatrixassemblymembrane4MeaslesNipahparamyxovirusproteinvirionviralproteins5bindingpolymerizationmultipleparamyxovirusescausediseaseoutbreakshumansanimalsworldwidemediatesbuddinghostcellmembranesthuskeytargetantiviralshigh-resolutionstructuresavailablelackclearunderstandinginteractlipidsmediateegressneededguideantiviraldesignrevealassociatephosphatidylserinephosphatidylinositol5-bisphosphate[PIP]plasmaUsingx-raycrystallographyelectronmicroscopymoleculardynamicsdemonstratePIPinducesconformationalelectrostaticchangessurfacetriggerdeformationlayerassembly:Specificlipiddrives

Similar Articles

Cited By