The Effects of Viral Structural Proteins on Acidic Phospholipids in Host Membranes
Abstract
1. Introduction
2. Classification, Structure, and Cellular Distribution of Phospholipids
3. The Functions and Lateral Distributions of Plasma Membrane Acidic Phospholipids
4. Influenza A Virus (IAV) Assembly and Acidic Phospholipids
4.1. Influenza A Virus Assembly
4.2. The Interplay Between Acidic Phospholipids and Influenza A Virus Structural Proteins
4.2.1. Hemagglutinin (HA) and the Acidic Phospholipids
4.2.2. Matrix Protein-1 (M1) and the Acidic Phospholipids
5. Human Immunodeficiency Virus Type 1 (HIV-1) Assembly and Acidic Phospholipids
5.1. HIV-1 Assembly
5.2. The Interplay Between Cellular Phospholipids and HIV-1 Structural Protein Gag
5.2.1. Gag and PI(4,5)P2
5.2.2. HIV-1 and PS
6. Future Directions
- (1)
- Are viral structural proteins recruited to pre-existing acidic phospholipid-rich areas, or do they cause acidic phospholipids clustering or both?
- (2)
- Do acidic phospholipids play a role in the incorporation of viral transmembrane proteins and the packaging of viral genomes into nascent virus particles?
- (3)
- Do acidic phospholipids regulate the recruitment of host cellular proteins to the assembly sites, and if so, what roles do these host proteins play in the assembly process or virion infectivity?
- (4)
- What is the role, if any, of the incorporated acidic phospholipids for IAV and HIV in viral spread?
- (5)
- How do viral proteins regulate acidic phospholipid distribution locally and globally?
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Welsch, S.; Miller, S.; Romero-Brey, I.; Merz, A.; Bleck, C.K.; Walther, P.; Fuller, S.D.; Antony, C.; Krijnse-Locker, J.; Bartenschlager, R. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 2009, 5, 365–375. [Google Scholar] [CrossRef] [PubMed]
- Mackenzie, J.M.; Jones, M.K.; Young, P.R. Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. Virology 1996, 220, 232–240. [Google Scholar] [CrossRef] [PubMed]
- Barnard, T.R.; Abram, Q.H.; Lin, Q.F.; Wang, A.B.; Sagan, S.M. Molecular Determinants of Flavivirus Virion Assembly. Trends Biochem. Sci. 2021, 46, 378–390. [Google Scholar] [CrossRef]
- Barbosa, N.S.; Mendonca, L.R.; Dias, M.V.S.; Pontelli, M.C.; da Silva, E.Z.M.; Criado, M.F.; da Silva-Januario, M.E.; Schindler, M.; Jamur, M.C.; Oliver, C.; et al. ESCRT machinery components are required for Orthobunyavirus particle production in Golgi compartments. PLoS Pathog. 2018, 14, e1007047. [Google Scholar] [CrossRef] [PubMed]
- Barker, J.; daSilva, L.L.P.; Crump, C.M. Mechanisms of bunyavirus morphogenesis and egress. J. Gen. Virol. 2023, 104, 001845. [Google Scholar] [CrossRef] [PubMed]
- Draganova, E.B.; Valentin, J.; Heldwein, E.E. The Ins and Outs of Herpesviral Capsids: Divergent Structures and Assembly Mechanisms across the Three Subfamilies. Viruses 2021, 13, 1913. [Google Scholar] [CrossRef]
- Selzer, L.; Zlotnick, A. Assembly and Release of Hepatitis B Virus. Cold Spring Harb. Perspect. Med. 2015, 5, a021394. [Google Scholar] [CrossRef]
- Roingeard, P.; Eymieux, S.; Burlaud-Gaillard, J.; Hourioux, C.; Patient, R.; Blanchard, E. The double-membrane vesicle (DMV): A virus-induced organelle dedicated to the replication of SARS-CoV-2 and other positive-sense single-stranded RNA viruses. Cell. Mol. Life Sci. 2022, 79, 425. [Google Scholar] [CrossRef]
- Roberts, S.R.; Compans, R.W.; Wertz, G.W. Respiratory syncytial virus matures at the apical surfaces of polarized epithelial cells. J. Virol. 1995, 69, 2667–2673. [Google Scholar] [CrossRef]
- Cardoso, R.S.; Tavares, L.A.; Jesus, B.L.S.; Criado, M.F.; de Carvalho, A.N.; Souza, J.P.; Bedi, S.; de Souza, M.M.; Silva, M.L.; Lanfredi, G.P.; et al. Host Retromer Protein Sorting Nexin 2 Interacts with Human Respiratory Syncytial Virus Structural Proteins and is Required for Efficient Viral Production. mBio 2020, 11, e01869-20. [Google Scholar] [CrossRef]
- Sugrue, R.J.; Tan, B.H. Defining the Assembleome of the Respiratory Syncytial Virus. In Virus Infected Cells; Subcellular Biochemistry; Springer: Berlin/Heidelberg, Germany, 2023; Volume 106, pp. 227–249. [Google Scholar]
- Rossman, J.S.; Lamb, R.A. Influenza virus assembly and budding. Virology 2011, 411, 229–236. [Google Scholar] [CrossRef] [PubMed]
- Bedi, S.; Noda, T.; Kawaoka, Y.; Ono, A. A Defect in Influenza A Virus Particle Assembly Specific to Primary Human Macrophages. mBio 2018, 9, e01916-18. [Google Scholar] [CrossRef]
- Nayak, D.P.; Balogun, R.A.; Yamada, H.; Zhou, Z.H.; Barman, S. Influenza virus morphogenesis and budding. Virus Res. 2009, 143, 147–161. [Google Scholar] [CrossRef] [PubMed]
- Geisbert, T.W.; Jahrling, P.B. Differentiation of filoviruses by electron microscopy. Virus Res. 1995, 39, 129–150. [Google Scholar] [CrossRef] [PubMed]
- Noda, T.; Ebihara, H.; Muramoto, Y.; Fujii, K.; Takada, A.; Sagara, H.; Kim, J.H.; Kida, H.; Feldmann, H.; Kawaoka, Y. Assembly and budding of Ebolavirus. PLoS Pathog. 2006, 2, e99. [Google Scholar] [CrossRef]
- Dolnik, O.; Becker, S. Assembly and transport of filovirus nucleocapsids. PLoS Pathog. 2022, 18, e1010616. [Google Scholar] [CrossRef]
- Freed, E.O. HIV-1 assembly, release and maturation. Nat. Rev. Microbiol. 2015, 13, 484–496. [Google Scholar] [CrossRef]
- Jouvenet, N.; Neil, S.J.; Bess, C.; Johnson, M.C.; Virgen, C.A.; Simon, S.M.; Bieniasz, P.D. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 2006, 4, e435. [Google Scholar] [CrossRef]
- Finzi, A.; Orthwein, A.; Mercier, J.; Cohen, E.A. Productive human immunodeficiency virus type 1 assembly takes place at the plasma membrane. J. Virol. 2007, 81, 7476–7490. [Google Scholar] [CrossRef]
- Fahy, E.; Subramaniam, S.; Murphy, R.C.; Nishijima, M.; Raetz, C.R.; Shimizu, T.; Spener, F.; van Meer, G.; Wakelam, M.J.; Dennis, E.A. Update of the LIPID MAPS comprehensive classification system for lipids. J. Lipid Res. 2009, 50, S9–S14. [Google Scholar] [CrossRef]
- Harayama, T.; Riezman, H. Understanding the diversity of membrane lipid composition. Nat. Rev. Mol. Cell Biol. 2018, 19, 281–296. [Google Scholar] [CrossRef]
- IUPAC-IUB Commission on Biochemical Nomenclature. Nomenclature of phosphorus-containing compounds of biochemical importance (Recommendations 1976). Proc. Natl. Acad. Sci. USA 1977, 74, 2222–2230. [CrossRef] [PubMed]
- Vance, J.E. Historical perspective: Phosphatidylserine and phosphatidylethanolamine from the 1800s to the present. J. Lipid Res. 2018, 59, 923–944. [Google Scholar] [CrossRef] [PubMed]
- Posor, Y.; Jang, W.; Haucke, V. Phosphoinositides as membrane organizers. Nat. Rev. Mol. Cell Biol. 2022, 23, 797–816. [Google Scholar] [CrossRef] [PubMed]
- Kay, J.G.; Fairn, G.D. Distribution, dynamics and functional roles of phosphatidylserine within the cell. Cell Commun. Signal. 2019, 17, 126. [Google Scholar] [CrossRef]
- van Meer, G.; Voelker, D.R.; Feigenson, G.W. Membrane lipids: Where they are and how they behave. Nat. Rev. Mol. Cell Biol. 2008, 9, 112–124. [Google Scholar] [CrossRef]
- Lolicato, F.; Nickel, W.; Haucke, V.; Ebner, M. Phosphoinositide switches in cell physiology—From molecular mechanisms to disease. J. Biol. Chem. 2024, 300, 105757. [Google Scholar] [CrossRef]
- Nicolson, G.L. The Fluid-Mosaic Model of Membrane Structure: Still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochim. Biophys. Acta 2014, 1838, 1451–1466. [Google Scholar] [CrossRef]
- Sakuragi, T.; Nagata, S. Regulation of phospholipid distribution in the lipid bilayer by flippases and scramblases. Nat. Rev. Mol. Cell Biol. 2023, 24, 576–596. [Google Scholar] [CrossRef]
- Kervin, T.A.; Overduin, M. Membranes are functionalized by a proteolipid code. BMC Biol. 2024, 22, 46. [Google Scholar] [CrossRef]
- Thakur, R.; Naik, A.; Panda, A.; Raghu, P. Regulation of Membrane Turnover by Phosphatidic Acid: Cellular Functions and Disease Implications. Front. Cell Dev. Biol. 2019, 7, 83. [Google Scholar] [CrossRef] [PubMed]
- McLaughlin, S.; Murray, D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 2005, 438, 605–611. [Google Scholar] [CrossRef] [PubMed]
- Shin, J.J.H.; Loewen, C.J.R. Putting the pH into phosphatidic acid signaling. BMC Biol. 2011, 9, 85. [Google Scholar] [CrossRef] [PubMed]
- Hirama, T.; Lu, S.M.; Kay, J.G.; Maekawa, M.; Kozlov, M.M.; Grinstein, S.; Fairn, G.D. Membrane curvature induced by proximity of anionic phospholipids can initiate endocytosis. Nat. Commun. 2017, 8, 1393. [Google Scholar] [CrossRef]
- Bills, B.L.; Knowles, M.K. Phosphatidic Acid Accumulates at Areas of Curvature in Tubulated Lipid Bilayers and Liposomes. Biomolecules 2022, 12, 1707. [Google Scholar] [CrossRef]
- Gericke, A. Is Calcium Fine-Tuning Phosphoinositide-Mediated Signaling Events Through Clustering? Biophys. J. 2018, 114, 2483–2484. [Google Scholar] [CrossRef]
- Schink, K.O.; Tan, K.W.; Stenmark, H. Phosphoinositides in Control of Membrane Dynamics. Annu. Rev. Cell Dev. Biol. 2016, 32, 143–171. [Google Scholar] [CrossRef]
- Beziau, A.; Brand, D.; Piver, E. The Role of Phosphatidylinositol Phosphate Kinases during Viral Infection. Viruses 2020, 12, 1124. [Google Scholar] [CrossRef]
- Adu-Gyamfi, E.; Johnson, K.A.; Fraser, M.E.; Scott, J.L.; Soni, S.P.; Jones, K.R.; Digman, M.A.; Gratton, E.; Tessier, C.R.; Stahelin, R.V. Host Cell Plasma Membrane Phosphatidylserine Regulates the Assembly and Budding of Ebola Virus. J. Virol. 2015, 89, 9440–9453. [Google Scholar] [CrossRef]
- Gc, J.B.; Gerstman, B.S.; Stahelin, R.V.; Chapagain, P.P. The Ebola virus protein VP40 hexamer enhances the clustering of PI(4,5)P(2) lipids in the plasma membrane. Phys. Chem. Chem. Phys. 2016, 18, 28409–28417. [Google Scholar] [CrossRef]
- Johnson, K.A.; Taghon, G.J.; Scott, J.L.; Stahelin, R.V. The Ebola Virus matrix protein, VP40, requires phosphatidylinositol 4,5-bisphosphate (PI(4,5)P2) for extensive oligomerization at the plasma membrane and viral egress. Sci. Rep. 2016, 6, 19125. [Google Scholar] [CrossRef] [PubMed]
- Acciani, M.D.; Lay Mendoza, M.F.; Havranek, K.E.; Duncan, A.M.; Iyer, H.; Linn, O.L.; Brindley, M.A. Ebola Virus Requires Phosphatidylserine Scrambling Activity for Efficient Budding and Optimal Infectivity. J. Virol. 2021, 95, e0116521. [Google Scholar] [CrossRef] [PubMed]
- Cioffi, M.D.; Husby, M.L.; Gerstman, B.S.; Stahelin, R.V.; Chapagain, P.P. Role of phosphatidic acid lipids on plasma membrane association of the Ebola virus matrix protein VP40. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2024, 1869, 159464. [Google Scholar] [CrossRef] [PubMed]
- Johnson, K.A.; Budicini, M.R.; Bhattarai, N.; Sharma, T.; Urata, S.; Gerstman, B.S.; Chapagain, P.P.; Li, S.; Stahelin, R.V. PI(4,5)P(2) binding sites in the Ebola virus matrix protein VP40 modulate assembly and budding. J. Lipid Res. 2024, 65, 100512. [Google Scholar] [CrossRef] [PubMed]
- Norris, M.J.; Husby, M.L.; Kiosses, W.B.; Yin, J.; Saxena, R.; Rennick, L.J.; Heiner, A.; Harkins, S.S.; Pokhrel, R.; Schendel, S.L.; et al. Measles and Nipah virus assembly: Specific lipid binding drives matrix polymerization. Sci. Adv. 2022, 8, eabn1440. [Google Scholar] [CrossRef]
- Eisenberg, S.; Haimov, E.; Walpole, G.F.W.; Plumb, J.; Kozlov, M.M.; Grinstein, S. Mapping the electrostatic profiles of cellular membranes. Mol. Biol. Cell 2021, 32, 301–310. [Google Scholar] [CrossRef]
- Yeung, T.; Gilbert, G.E.; Shi, J.; Silvius, J.; Kapus, A.; Grinstein, S. Membrane phosphatidylserine regulates surface charge and protein localization. Science 2008, 319, 210–213. [Google Scholar] [CrossRef]
- McLaughlin, S. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 1989, 18, 113–136. [Google Scholar] [CrossRef]
- Raghupathy, R.; Anilkumar, A.A.; Polley, A.; Singh, P.P.; Yadav, M.; Johnson, C.; Suryawanshi, S.; Saikam, V.; Sawant, S.D.; Panda, A.; et al. Transbilayer lipid interactions mediate nanoclustering of lipid-anchored proteins. Cell 2015, 161, 581–594. [Google Scholar] [CrossRef]
- Leventis, P.A.; Grinstein, S. The distribution and function of phosphatidylserine in cellular membranes. Annu. Rev. Biophys. 2010, 39, 407–427. [Google Scholar] [CrossRef]
- Varga, K.; Jiang, Z.J.; Gong, L.W. Phosphatidylserine is critical for vesicle fission during clathrin-mediated endocytosis. J. Neurochem. 2020, 152, 48–60. [Google Scholar] [CrossRef] [PubMed]
- Hallett, M.B. Localisation of Intracellular Signals and Responses during Phagocytosis. Int. J. Mol. Sci. 2023, 24, 2825. [Google Scholar] [CrossRef]
- Bohdanowicz, M.; Grinstein, S. Role of phospholipids in endocytosis, phagocytosis, and macropinocytosis. Physiol. Rev. 2013, 93, 69–106. [Google Scholar] [CrossRef]
- Uchida, Y.; Hasegawa, J.; Chinnapen, D.; Inoue, T.; Okazaki, S.; Kato, R.; Wakatsuki, S.; Misaki, R.; Koike, M.; Uchiyama, Y.; et al. Intracellular phosphatidylserine is essential for retrograde membrane traffic through endosomes. Proc. Natl. Acad. Sci. USA 2011, 108, 15846–15851. [Google Scholar] [CrossRef]
- Fairn, G.D.; Hermansson, M.; Somerharju, P.; Grinstein, S. Phosphatidylserine is polarized and required for proper Cdc42 localization and for development of cell polarity. Nat. Cell Biol. 2011, 13, 1424–1430. [Google Scholar] [CrossRef]
- Ammar, M.R.; Kassas, N.; Chasserot-Golaz, S.; Bader, M.F.; Vitale, N. Lipids in Regulated Exocytosis: What are They Doing? Front. Endocrinol. 2013, 4, 125. [Google Scholar] [CrossRef]
- McLaughlin, S.; Wang, J.; Gambhir, A.; Murray, D. PIP(2) and proteins: Interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct. 2002, 31, 151–175. [Google Scholar] [CrossRef]
- Katan, M.; Cockcroft, S. Phosphatidylinositol(4,5)bisphosphate: Diverse functions at the plasma membrane. Essays Biochem. 2020, 64, 513–531. [Google Scholar]
- Jost, M.; Simpson, F.; Kavran, J.M.; Lemmon, M.A.; Schmid, S.L. Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr. Biol. 1998, 8, 1399–1402. [Google Scholar] [CrossRef]
- Crul, T.; Maleth, J. Endoplasmic Reticulum-Plasma Membrane Contact Sites as an Organizing Principle for Compartmentalized Calcium and cAMP Signaling. Int. J. Mol. Sci. 2021, 22, 4703. [Google Scholar] [CrossRef]
- Lahiri, S.; Toulmay, A.; Prinz, W.A. Membrane contact sites, gateways for lipid homeostasis. Curr. Opin. Cell Biol. 2015, 33, 82–87. [Google Scholar] [CrossRef] [PubMed]
- Thallmair, V.; Schultz, L.; Evers, S.; Jolie, T.; Goecke, C.; Leitner, M.G.; Thallmair, S.; Oliver, D. Localization of the tubby domain, a PI(4,5)P2 biosensor, to E-Syt3-rich endoplasmic reticulum-plasma membrane junctions. J. Cell Sci. 2023, 136, jcs260848. [Google Scholar] [CrossRef] [PubMed]
- Cockcroft, S.; Raghu, P. Phospholipid transport protein function at organelle contact sites. Curr. Opin. Cell Biol. 2018, 53, 52–60. [Google Scholar] [CrossRef]
- Seki, K.; Sheu, F.S.; Huang, K.P. Binding of myristoylated alanine-rich protein kinase C substrate to phosphoinositides attenuates the phosphorylation by protein kinase C. Arch. Biochem. Biophys. 1996, 326, 193–201. [Google Scholar] [CrossRef]
- Denisov, G.; Wanaski, S.; Luan, P.; Glaser, M.; McLaughlin, S. Binding of basic peptides to membranes produces lateral domains enriched in the acidic lipids phosphatidylserine and phosphatidylinositol 4,5-bisphosphate: An electrostatic model and experimental results. Biophys. J. 1998, 74 Pt 1, 731–744. [Google Scholar] [CrossRef]
- Laux, T.; Fukami, K.; Thelen, M.; Golub, T.; Frey, D.; Caroni, P. GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J. Cell Biol. 2000, 149, 1455–1472. [Google Scholar] [CrossRef]
- Rauch, M.E.; Ferguson, C.G.; Prestwich, G.D.; Cafiso, D.S. Myristoylated alanine-rich C kinase substrate (MARCKS) sequesters spin-labeled phosphatidylinositol 4,5-bisphosphate in lipid bilayers. J. Biol. Chem. 2002, 277, 14068–14076. [Google Scholar] [CrossRef]
- Pemberton, J.G.; Balla, T. Polyphosphoinositide-Binding Domains: Insights from Peripheral Membrane and Lipid-Transfer Proteins. Adv. Exp. Med. Biol. 2019, 1111, 77–137. [Google Scholar]
- Wills, R.C.; Hammond, G.R.V. PI(4,5)P2: Signaling the plasma membrane. Biochem. J. 2022, 479, 2311–2325. [Google Scholar] [CrossRef]
- Harlan, J.E.; Hajduk, P.J.; Yoon, H.S.; Fesik, S.W. Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 1994, 371, 168–170. [Google Scholar] [CrossRef]
- Lomasney, J.W.; Cheng, H.F.; Wang, L.P.; Kuan, Y.; Liu, S.; Fesik, S.W.; King, K. Phosphatidylinositol 4,5-bisphosphate binding to the pleckstrin homology domain of phospholipase C-delta1 enhances enzyme activity. J. Biol. Chem. 1996, 271, 25316–25326. [Google Scholar] [CrossRef] [PubMed]
- Lemmon, M.A. Pleckstrin homology (PH) domains and phosphoinositides. Biochem. Soc. Symp. 2007, 74, 81–93. [Google Scholar] [CrossRef] [PubMed]
- Powis, G.; Meuillet, E.J.; Indarte, M.; Booher, G.; Kirkpatrick, L. Pleckstrin Homology [PH] domain, structure, mechanism, and contribution to human disease. Biomed. Pharmacother. 2023, 165, 115024. [Google Scholar] [CrossRef] [PubMed]
- Singh, N.; Reyes-Ordonez, A.; Compagnone, M.A.; Moreno, J.F.; Leslie, B.J.; Ha, T.; Chen, J. Redefining the specificity of phosphoinositide-binding by human PH domain-containing proteins. Nat. Commun. 2021, 12, 4339. [Google Scholar] [CrossRef]
- Mattila, P.K.; Pykalainen, A.; Saarikangas, J.; Paavilainen, V.O.; Vihinen, H.; Jokitalo, E.; Lappalainen, P. Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J. Cell Biol. 2007, 176, 953–964. [Google Scholar] [CrossRef]
- Ahmed, S.; Bu, W.; Lee, R.T.; Maurer-Stroh, S.; Goh, W.I. F-BAR domain proteins: Families and function. Commun. Integr. Biol. 2010, 3, 116–121. [Google Scholar] [CrossRef]
- Itoh, T.; Koshiba, S.; Kigawa, T.; Kikuchi, A.; Yokoyama, S.; Takenawa, T. Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 2001, 291, 1047–1051. [Google Scholar] [CrossRef]
- Ford, M.G.; Pearse, B.M.; Higgins, M.K.; Vallis, Y.; Owen, D.J.; Gibson, A.; Hopkins, C.R.; Evans, P.R.; McMahon, H.T. Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 2001, 291, 1051–1055. [Google Scholar] [CrossRef]
- Roux, A.; Koster, G.; Lenz, M.; Sorre, B.; Manneville, J.B.; Nassoy, P.; Bassereau, P. Membrane curvature controls dynamin polymerization. Proc. Natl. Acad. Sci. USA 2010, 107, 4141–4146. [Google Scholar] [CrossRef]
- Kadlecova, Z.; Spielman, S.J.; Loerke, D.; Mohanakrishnan, A.; Reed, D.K.; Schmid, S.L. Regulation of clathrin-mediated endocytosis by hierarchical allosteric activation of AP2. J. Cell Biol. 2017, 216, 167–179. [Google Scholar] [CrossRef]
- Krauss, M.; Kukhtina, V.; Pechstein, A.; Haucke, V. Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4,5)-bisphosphate synthesis by AP-2mu-cargo complexes. Proc. Natl. Acad. Sci. USA 2006, 103, 11934–11939. [Google Scholar] [CrossRef] [PubMed]
- Mu, L.; Tu, Z.; Miao, L.; Ruan, H.; Kang, N.; Hei, Y.; Chen, J.; Wei, W.; Gong, F.; Wang, B.; et al. A phosphatidylinositol 4,5-bisphosphate redistribution-based sensing mechanism initiates a phagocytosis programing. Nat. Commun. 2018, 9, 4259. [Google Scholar] [CrossRef] [PubMed]
- Flannagan, R.S.; Jaumouille, V.; Grinstein, S. The cell biology of phagocytosis. Annu. Rev. Pathol. 2012, 7, 61–98. [Google Scholar] [CrossRef] [PubMed]
- Golebiewska, U.; Kay, J.G.; Masters, T.; Grinstein, S.; Im, W.; Pastor, R.W.; Scarlata, S.; McLaughlin, S. Evidence for a fence that impedes the diffusion of phosphatidylinositol 4,5-bisphosphate out of the forming phagosomes of macrophages. Mol. Biol. Cell 2011, 22, 3498–3507. [Google Scholar] [CrossRef]
- Swanson, J.A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 2008, 9, 639–649. [Google Scholar] [CrossRef]
- Yang, X.; Tu, W.; Gao, X.; Zhang, Q.; Guan, J.; Zhang, J. Functional regulation of syntaxin-1: An underlying mechanism mediating exocytosis in neuroendocrine cells. Front. Endocrinol. 2023, 14, 1096365. [Google Scholar] [CrossRef]
- Liang, T.; Xie, L.; Chao, C.; Kang, Y.; Lin, X.; Qin, T.; Xie, H.; Feng, Z.P.; Gaisano, H.Y. Phosphatidylinositol 4,5-biphosphate (PI(4,5)P2) modulates interaction of syntaxin-1A with sulfonylurea receptor 1 to regulate pancreatic beta-cell ATP-sensitive potassium channels. J. Biol. Chem. 2014, 289, 6028–6040. [Google Scholar] [CrossRef]
- Lam, A.D.; Tryoen-Toth, P.; Tsai, B.; Vitale, N.; Stuenkel, E.L. SNARE-catalyzed fusion events are regulated by Syntaxin1A-lipid interactions. Mol. Biol. Cell 2008, 19, 485–497. [Google Scholar] [CrossRef]
- Honigmann, A.; van den Bogaart, G.; Iraheta, E.; Risselada, H.J.; Milovanovic, D.; Mueller, V.; Mullar, S.; Diederichsen, U.; Fasshauer, D.; Grubmuller, H.; et al. Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nat. Struct. Mol. Biol. 2013, 20, 679–686. [Google Scholar] [CrossRef]
- van den Bogaart, G.; Meyenberg, K.; Risselada, H.J.; Amin, H.; Willig, K.I.; Hubrich, B.E.; Dier, M.; Hell, S.W.; Grubmuller, H.; Diederichsen, U.; et al. Membrane protein sequestering by ionic protein-lipid interactions. Nature 2011, 479, 552–555. [Google Scholar] [CrossRef]
- Hammond, G.R. Does PtdIns(4,5)P2 concentrate so it can multi-task? Biochem. Soc. Trans. 2016, 44, 228–233. [Google Scholar] [CrossRef] [PubMed]
- Han, K.; Kim, S.H.; Venable, R.M.; Pastor, R.W. Design principles of PI(4,5)P(2) clustering under protein-free conditions: Specific cation effects and calcium-potassium synergy. Proc. Natl. Acad. Sci. USA 2022, 119, e2202647119. [Google Scholar] [CrossRef] [PubMed]
- Golebiewska, U.; Nyako, M.; Woturski, W.; Zaitseva, I.; McLaughlin, S. Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol. Biol. Cell 2008, 19, 1663–1669. [Google Scholar] [CrossRef]
- Gambhir, A.; Hangyas-Mihalyne, G.; Zaitseva, I.; Cafiso, D.S.; Wang, J.; Murray, D.; Pentyala, S.N.; Smith, S.O.; McLaughlin, S. Electrostatic sequestration of PI(4,5)P2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys. J. 2004, 86, 2188–2207. [Google Scholar] [CrossRef] [PubMed]
- Koldso, H.; Shorthouse, D.; Helie, J.; Sansom, M.S. Lipid clustering correlates with membrane curvature as revealed by molecular simulations of complex lipid bilayers. PLoS Comput. Biol. 2014, 10, e1003911. [Google Scholar] [CrossRef]
- Dou, D.; Revol, R.; Ostbye, H.; Wang, H.; Daniels, R. Influenza A Virus Cell Entry, Replication, Virion Assembly and Movement. Front. Immunol. 2018, 9, 1581. [Google Scholar] [CrossRef]
- Carter, T.; Iqbal, M. The Influenza A Virus Replication Cycle: A Comprehensive Review. Viruses 2024, 16, 316. [Google Scholar] [CrossRef]
- Wu, N.C.; Wilson, I.A. Influenza Hemagglutinin Structures and Antibody Recognition. Cold Spring Harb. Perspect. Med. 2020, 10, a038778. [Google Scholar] [CrossRef]
- Chlanda, P.; Mekhedov, E.; Waters, H.; Sodt, A.; Schwartz, C.; Nair, V.; Blank, P.S.; Zimmerberg, J. Palmitoylation Contributes to Membrane Curvature in Influenza A Virus Assembly and Hemagglutinin-Mediated Membrane Fusion. J. Virol. 2017, 91, e00947-17. [Google Scholar] [CrossRef]
- McAuley, J.L.; Gilbertson, B.P.; Trifkovic, S.; Brown, L.E.; McKimm-Breschkin, J.L. Influenza Virus Neuraminidase Structure and Functions. Front. Microbiol. 2019, 10, 39. [Google Scholar] [CrossRef]
- Martin, K.; Helenius, A. Nuclear transport of influenza virus ribonucleoproteins: The viral matrix protein (M1) promotes export and inhibits import. Cell 1991, 67, 117–130. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Gu, M.; Zheng, Q.; Gao, R.; Liu, X. Packaging signal of influenza A virus. Virol. J. 2021, 18, 36. [Google Scholar] [CrossRef] [PubMed]
- Petrich, A.; Dunsing, V.; Bobone, S.; Chiantia, S. Influenza A M2 recruits M1 to the plasma membrane: A fluorescence fluctuation microscopy study. Biophys. J. 2021, 120, 5478–5490. [Google Scholar] [CrossRef] [PubMed]
- Rossman, J.S.; Jing, X.; Leser, G.P.; Lamb, R.A. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 2010, 142, 902–913. [Google Scholar] [CrossRef]
- Tam, V.C.; Quehenberger, O.; Oshansky, C.M.; Suen, R.; Armando, A.M.; Treuting, P.M.; Thomas, P.G.; Dennis, E.A.; Aderem, A. Lipidomic profiling of influenza infection identifies mediators that induce and resolve inflammation. Cell 2013, 154, 213–227. [Google Scholar] [CrossRef]
- Lin, S.; Liu, N.; Yang, Z.; Song, W.; Wang, P.; Chen, H.; Lucio, M.; Schmitt-Kopplin, P.; Chen, G.; Cai, Z. GC/MS-based metabolomics reveals fatty acid biosynthesis and cholesterol metabolism in cell lines infected with influenza A virus. Talanta 2010, 83, 262–268. [Google Scholar] [CrossRef]
- Ivanova, P.T.; Myers, D.S.; Milne, S.B.; McClaren, J.L.; Thomas, P.G.; Brown, H.A. Lipid composition of viral envelope of three strains of influenza virus—Not all viruses are created equal. ACS Infect. Dis. 2015, 1, 399–452. [Google Scholar] [CrossRef]
- Tanner, L.B.; Chng, C.; Guan, X.L.; Lei, Z.; Rozen, S.G.; Wenk, M.R. Lipidomics identifies a requirement for peroxisomal function during influenza virus replication. J. Lipid Res. 2014, 55, 1357–1365. [Google Scholar] [CrossRef]
- Tisoncik-Go, J.; Gasper, D.J.; Kyle, J.E.; Eisfeld, A.J.; Selinger, C.; Hatta, M.; Morrison, J.; Korth, M.J.; Zink, E.M.; Kim, Y.M.; et al. Integrated Omics Analysis of Pathogenic Host Responses during Pandemic H1N1 Influenza Virus Infection: The Crucial Role of Lipid Metabolism. Cell Host Microbe 2016, 19, 254–266. [Google Scholar] [CrossRef]
- Woods, P.S.; Doolittle, L.M.; Rosas, L.E.; Joseph, L.M.; Calomeni, E.P.; Davis, I.C. Lethal H1N1 influenza A virus infection alters the murine alveolar type II cell surfactant lipidome. Am. J. Physiol. Lung Cell. Mol. Physiol. 2016, 311, L1160–L1169. [Google Scholar] [CrossRef]
- Schmitt, A.P.; Lamb, R.A. Influenza virus assembly and budding at the viral budozone. Adv. Virus Res. 2005, 64, 383–416. [Google Scholar] [PubMed]
- Leser, G.P.; Lamb, R.A. Lateral Organization of Influenza Virus Proteins in the Budozone Region of the Plasma Membrane. J. Virol. 2017, 91, e02104-16. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.J.; Chen, C.Y.; Yang, J.H.; Chiu, Y.F. Modulating cholesterol-rich lipid rafts to disrupt influenza A virus infection. Front. Immunol. 2022, 13, 982264. [Google Scholar] [CrossRef] [PubMed]
- Veit, M.; Engel, S.; Thaa, B.; Scolari, S.; Herrmann, A. Lipid domain association of influenza virus proteins detected by dynamic fluorescence microscopy techniques. Cell. Microbiol. 2013, 15, 179–189. [Google Scholar] [CrossRef]
- Ono, A.; Freed, E.O. Role of lipid rafts in virus replication. Adv. Virus Res. 2005, 64, 311–358. [Google Scholar]
- Zhang, J.; Pekosz, A.; Lamb, R.A. Influenza virus assembly and lipid raft microdomains: A role for the cytoplasmic tails of the spike glycoproteins. J. Virol. 2000, 74, 4634–4644. [Google Scholar] [CrossRef]
- Skibbens, J.E.; Roth, M.G.; Matlin, K.S. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts. J. Cell Biol. 1989, 108, 821–832. [Google Scholar] [CrossRef]
- Barman, S.; Nayak, D.P. Analysis of the transmembrane domain of influenza virus neuraminidase, a type II transmembrane glycoprotein, for apical sorting and raft association. J. Virol. 2000, 74, 6538–6545. [Google Scholar] [CrossRef]
- Kundu, A.; Avalos, R.T.; Sanderson, C.M.; Nayak, D.P. Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells. J. Virol. 1996, 70, 6508–6515. [Google Scholar] [CrossRef]
- Ali, A.; Avalos, R.T.; Ponimaskin, E.; Nayak, D.P. Influenza virus assembly: Effect of influenza virus glycoproteins on the membrane association of M1 protein. J. Virol. 2000, 74, 8709–8719. [Google Scholar] [CrossRef]
- Schroeder, C. Cholesterol-binding viral proteins in virus entry and morphogenesis. In Cholesterol Binding and Cholesterol Transport Proteins; Subcellular Biochemistry; Springer: Berlin/Heidelberg, Germany, 2010; Volume 51, pp. 77–108. [Google Scholar]
- Leser, G.P.; Lamb, R.A. Influenza virus assembly and budding in raft-derived microdomains: A quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology 2005, 342, 215–227. [Google Scholar] [CrossRef] [PubMed]
- Petrich, A.; Chiantia, S. Influenza A Virus Infection Alters Lipid Packing and Surface Electrostatic Potential of the Host Plasma Membrane. Viruses 2023, 15, 1830. [Google Scholar] [CrossRef] [PubMed]
- Scheiffele, P.; Rietveld, A.; Wilk, T.; Simons, K. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 1999, 274, 2038–2044. [Google Scholar] [CrossRef]
- Veit, M.; Thaa, B. Association of influenza virus proteins with membrane rafts. Adv. Virol. 2011, 2011, 370606. [Google Scholar] [CrossRef] [PubMed]
- Gerl, M.J.; Sampaio, J.L.; Urban, S.; Kalvodova, L.; Verbavatz, J.M.; Binnington, B.; Lindemann, D.; Lingwood, C.A.; Shevchenko, A.; Schroeder, C.; et al. Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J. Cell Biol. 2012, 196, 213–221. [Google Scholar] [CrossRef]
- Raut, P.; Weller, S.R.; Obeng, B.; Soos, B.L.; West, B.E.; Potts, C.M.; Sangroula, S.; Kinney, M.S.; Burnell, J.E.; King, B.L.; et al. Cetylpyridinium chloride (CPC) reduces zebrafish mortality from influenza infection: Super-resolution microscopy reveals CPC interference with multiple protein interactions with phosphatidylinositol 4,5-bisphosphate in immune function. Toxicol. Appl. Pharmacol. 2022, 440, 115913. [Google Scholar] [CrossRef]
- Hess, S.T.; Gould, T.J.; Gudheti, M.V.; Maas, S.A.; Mills, K.D.; Zimmerberg, J. Dynamic clustered distribution of hemagglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proc. Natl. Acad. Sci. USA 2007, 104, 17370–17375. [Google Scholar] [CrossRef]
- Hess, S.T.; Kumar, M.; Verma, A.; Farrington, J.; Kenworthy, A.; Zimmerberg, J. Quantitative electron microscopy and fluorescence spectroscopy of the membrane distribution of influenza hemagglutinin. J. Cell Biol. 2005, 169, 965–976. [Google Scholar] [CrossRef]
- Scolari, S.; Engel, S.; Krebs, N.; Plazzo, A.P.; De Almeida, R.F.; Prieto, M.; Veit, M.; Herrmann, A. Lateral distribution of the transmembrane domain of influenza virus hemagglutinin revealed by time-resolved fluorescence imaging. J. Biol. Chem. 2009, 284, 15708–15716. [Google Scholar] [CrossRef]
- Wilson, R.L.; Frisz, J.F.; Klitzing, H.A.; Zimmerberg, J.; Weber, P.K.; Kraft, M.L. Hemagglutinin clusters in the plasma membrane are not enriched with cholesterol and sphingolipids. Biophys. J. 2015, 108, 1652–1659. [Google Scholar] [CrossRef]
- Chlanda, P.; Zimmerberg, J. Protein-lipid interactions critical to replication of the influenza A virus. FEBS Lett. 2016, 590, 1940–1954. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Casey, L.; Pike, L.J. Compartmentalization of phosphatidylinositol 4,5-bisphosphate in low-density membrane domains in the absence of caveolin. Biochem. Biophys. Res. Commun. 1998, 245, 684–690. [Google Scholar] [CrossRef] [PubMed]
- Hope, H.R.; Pike, L.J. Phosphoinositides and phosphoinositide-utilizing enzymes in detergent-insoluble lipid domains. Mol. Biol. Cell 1996, 7, 843–851. [Google Scholar] [CrossRef] [PubMed]
- Pike, L.J. Lipid rafts: Bringing order to chaos. J. Lipid Res. 2003, 44, 655–667. [Google Scholar] [CrossRef]
- Raut, P.; Obeng, B.; Waters, H.; Zimmerberg, J.; Gosse, J.A.; Hess, S.T. Phosphatidylinositol 4,5-Bisphosphate Mediates the Co-Distribution of Influenza A Hemagglutinin and Matrix Protein M1 at the Plasma Membrane. Viruses 2022, 14, 2509. [Google Scholar] [CrossRef]
- Curthoys, N.M.; Mlodzianoski, M.J.; Parent, M.; Butler, M.B.; Raut, P.; Wallace, J.; Lilieholm, J.; Mehmood, K.; Maginnis, M.S.; Waters, H.; et al. Influenza Hemagglutinin Modulates Phosphatidylinositol 4,5-Bisphosphate Membrane Clustering. Biophys. J. 2019, 116, 893–909. [Google Scholar] [CrossRef]
- Tatulian, S.A.; Tamm, L.K. Secondary structure, orientation, oligomerization, and lipid interactions of the transmembrane domain of influenza hemagglutinin. Biochemistry 2000, 39, 496–507. [Google Scholar] [CrossRef]
- Mineev, K.S.; Lyukmanova, E.N.; Krabben, L.; Serebryakova, M.V.; Shulepko, M.A.; Arseniev, A.S.; Kordyukova, L.V.; Veit, M. Structural investigation of influenza virus hemagglutinin membrane-anchoring peptide. Protein Eng. Des. Sel. 2013, 26, 547–552. [Google Scholar] [CrossRef]
- Ngo, V.N.; Winski, D.P.; Aho, B.; Kamath, P.L.; King, B.L.; Waters, H.; Zimmerberg, J.; Sodt, A.; Hess, S.T. Conserved sequence features in intracellular domains of viral spike proteins. Virology 2024, 599, 110198. [Google Scholar] [CrossRef]
- Gudheti, M.V.; Curthoys, N.M.; Gould, T.J.; Kim, D.; Gunewardene, M.S.; Gabor, K.A.; Gosse, J.A.; Kim, C.H.; Zimmerberg, J.; Hess, S.T. Actin mediates the nanoscale membrane organization of the clustered membrane protein influenza hemagglutinin. Biophys. J. 2013, 104, 2182–2192. [Google Scholar] [CrossRef]
- Zhang, J.; Lamb, R.A. Characterization of the membrane association of the influenza virus matrix protein in living cells. Virology 1996, 225, 255–266. [Google Scholar] [CrossRef] [PubMed]
- Peukes, J.; Xiong, X.; Erlendsson, S.; Qu, K.; Wan, W.; Calder, L.J.; Schraidt, O.; Kummer, S.; Freund, S.M.V.; Krausslich, H.G.; et al. The native structure of the assembled matrix protein 1 of influenza A virus. Nature 2020, 587, 495–498. [Google Scholar] [CrossRef] [PubMed]
- Hofer, C.T.; Di Lella, S.; Dahmani, I.; Jungnick, N.; Bordag, N.; Bobone, S.; Huang, Q.; Keller, S.; Herrmann, A.; Chiantia, S. Structural determinants of the interaction between influenza A virus matrix protein M1 and lipid membranes. Biochim. Biophys. Acta Biomembr. 2019, 1861, 1123–1134. [Google Scholar] [CrossRef] [PubMed]
- Kerviel, A.; Dash, S.; Moncorge, O.; Panthu, B.; Prchal, J.; Decimo, D.; Ohlmann, T.; Lina, B.; Favard, C.; Decroly, E.; et al. Involvement of an Arginine Triplet in M1 Matrix Protein Interaction with Membranes and in M1 Recruitment into Virus-Like Particles of the Influenza A(H1N1)pdm09 Virus. PLoS ONE 2016, 11, e0165421. [Google Scholar] [CrossRef]
- Ruigrok, R.W.; Barge, A.; Durrer, P.; Brunner, J.; Ma, K.; Whittaker, G.R. Membrane interaction of influenza virus M1 protein. Virology 2000, 267, 289–298. [Google Scholar] [CrossRef]
- Baudin, F.; Petit, I.; Weissenhorn, W.; Ruigrok, R.W. In vitro dissection of the membrane and RNP binding activities of influenza virus M1 protein. Virology 2001, 281, 102–108. [Google Scholar] [CrossRef]
- Das, S.C.; Watanabe, S.; Hatta, M.; Noda, T.; Neumann, G.; Ozawa, M.; Kawaoka, Y. The highly conserved arginine residues at positions 76 through 78 of influenza A virus matrix protein M1 play an important role in viral replication by affecting the intracellular localization of M1. J. Virol. 2012, 86, 1522–1530. [Google Scholar] [CrossRef]
- Thaa, B.; Herrmann, A.; Veit, M. The polybasic region is not essential for membrane binding of the matrix protein M1 of influenza virus. Virology 2009, 383, 150–155. [Google Scholar] [CrossRef]
- Dahmani, I.; Ludwig, K.; Chiantia, S. Influenza A matrix protein M1 induces lipid membrane deformation via protein multimerization. Biosci. Rep. 2019, 39, BSR20191024. [Google Scholar] [CrossRef]
- Shtykova, E.V.; Dadinova, L.A.; Fedorova, N.V.; Golanikov, A.E.; Bogacheva, E.N.; Ksenofontov, A.L.; Baratova, L.A.; Shilova, L.A.; Tashkin, V.Y.; Galimzyanov, T.R.; et al. Influenza virus Matrix Protein M1 preserves its conformation with pH, changing multimerization state at the priming stage due to electrostatics. Sci. Rep. 2017, 7, 16793. [Google Scholar] [CrossRef]
- Hilsch, M.; Goldenbogen, B.; Sieben, C.; Hofer, C.T.; Rabe, J.P.; Klipp, E.; Herrmann, A.; Chiantia, S. Influenza A matrix protein M1 multimerizes upon binding to lipid membranes. Biophys. J. 2014, 107, 912–923. [Google Scholar] [CrossRef] [PubMed]
- Kordyukova, L.V.; Konarev, P.V.; Fedorova, N.V.; Shtykova, E.V.; Ksenofontov, A.L.; Loshkarev, N.A.; Dadinova, L.A.; Timofeeva, T.A.; Abramchuk, S.S.; Moiseenko, A.V.; et al. The Cytoplasmic Tail of Influenza A Virus Hemagglutinin and Membrane Lipid Composition Change the Mode of M1 Protein Association with the Lipid Bilayer. Membranes 2021, 11, 772. [Google Scholar] [CrossRef] [PubMed]
- Bobone, S.; Hilsch, M.; Storm, J.; Dunsing, V.; Herrmann, A.; Chiantia, S. Phosphatidylserine Lateral Organization Influences the Interaction of Influenza Virus Matrix Protein 1 with Lipid Membranes. J. Virol. 2017, 91, e00267-17. [Google Scholar] [CrossRef] [PubMed]
- Loshkareva, A.S.; Popova, M.M.; Shilova, L.A.; Fedorova, N.V.; Timofeeva, T.A.; Galimzyanov, T.R.; Kuzmin, P.I.; Knyazev, D.G.; Batishchev, O.V. Influenza A Virus M1 Protein Non-Specifically Deforms Charged Lipid Membranes and Specifically Interacts with the Raft Boundary. Membranes 2023, 13, 76. [Google Scholar] [CrossRef]
- Sha, B.; Luo, M. Structure of a bifunctional membrane-RNA binding protein, influenza virus matrix protein M1. Nat. Struct. Biol. 1997, 4, 239–244. [Google Scholar] [CrossRef]
- Kakisaka, M.; Yamada, K.; Yamaji-Hasegawa, A.; Kobayashi, T.; Aida, Y. Intrinsically disordered region of influenza A NP regulates viral genome packaging via interactions with viral RNA and host PI(4,5)P2. Virology 2016, 496, 116–126. [Google Scholar] [CrossRef]
- Gottlinger, H.G.; Sodroski, J.G.; Haseltine, W.A. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 1989, 86, 5781–5785. [Google Scholar] [CrossRef]
- Bryant, M.; Ratner, L. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc. Natl. Acad. Sci. USA 1990, 87, 523–527. [Google Scholar] [CrossRef]
- Zhou, W.; Parent, L.J.; Wills, J.W.; Resh, M.D. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J. Virol. 1994, 68, 2556–2569. [Google Scholar] [CrossRef]
- Yuan, X.; Yu, X.; Lee, T.H.; Essex, M. Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor. J. Virol. 1993, 67, 6387–6394. [Google Scholar] [CrossRef]
- Hermida-Matsumoto, L.; Resh, M.D. Human immunodeficiency virus type 1 protease triggers a myristoyl switch that modulates membrane binding of Pr55(gag) and p17MA. J. Virol. 1999, 73, 1902–1908. [Google Scholar] [CrossRef] [PubMed]
- Paillart, J.C.; Gottlinger, H.G. Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of gag membrane targeting. J. Virol. 1999, 73, 2604–2612. [Google Scholar] [CrossRef] [PubMed]
- Saad, J.S.; Loeliger, E.; Luncsford, P.; Liriano, M.; Tai, J.; Kim, A.; Miller, J.; Joshi, A.; Freed, E.O.; Summers, M.F. Point mutations in the HIV-1 matrix protein turn off the myristyl switch. J. Mol. Biol. 2007, 366, 574–585. [Google Scholar] [CrossRef] [PubMed]
- Spearman, P.; Horton, R.; Ratner, L.; Kuli-Zade, I. Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism. J. Virol. 1997, 71, 6582–6592. [Google Scholar] [CrossRef] [PubMed]
- Ono, A.; Freed, E.O. Binding of human immunodeficiency virus type 1 Gag to membrane: Role of the matrix amino terminus. J. Virol. 1999, 73, 4136–4144. [Google Scholar] [CrossRef]
- Tang, C.; Loeliger, E.; Luncsford, P.; Kinde, I.; Beckett, D.; Summers, M.F. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc. Natl. Acad. Sci. USA 2004, 101, 517–522. [Google Scholar] [CrossRef]
- Freed, E.O.; Orenstein, J.M.; Buckler-White, A.J.; Martin, M.A. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J. Virol. 1994, 68, 5311–5320. [Google Scholar] [CrossRef]
- Ono, A.; Orenstein, J.M.; Freed, E.O. Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly. J. Virol. 2000, 74, 2855–2866. [Google Scholar] [CrossRef]
- Kleinpeter, A.B.; Freed, E.O. HIV-1 Maturation: Lessons Learned from Inhibitors. Viruses 2020, 12, 940. [Google Scholar] [CrossRef]
- Thornhill, D.; Murakami, T.; Ono, A. Rendezvous at Plasma Membrane: Cellular Lipids and tRNA Set up Sites of HIV-1 Particle Assembly and Incorporation of Host Transmembrane Proteins. Viruses 2020, 12, 842. [Google Scholar] [CrossRef]
- Ono, A.; Ablan, S.D.; Lockett, S.J.; Nagashima, K.; Freed, E.O. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc. Natl. Acad. Sci. USA 2004, 101, 14889–14894. [Google Scholar] [CrossRef] [PubMed]
- Chan, R.; Uchil, P.D.; Jin, J.; Shui, G.; Ott, D.E.; Mothes, W.; Wenk, M.R. Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J. Virol. 2008, 82, 11228–11238. [Google Scholar] [CrossRef] [PubMed]
- Monde, K.; Chukkapalli, V.; Ono, A. Assembly and replication of HIV-1 in T cells with low levels of phosphatidylinositol-(4,5)-bisphosphate. J. Virol. 2011, 85, 3584–3595. [Google Scholar] [CrossRef]
- Chan, J.; Dick, R.A.; Vogt, V.M. Rous sarcoma virus gag has no specific requirement for phosphatidylinositol-(4,5)-bisphosphate for plasma membrane association in vivo or for liposome interaction in vitro. J. Virol. 2011, 85, 10851–10860. [Google Scholar] [CrossRef]
- Mucksch, F.; Laketa, V.; Muller, B.; Schultz, C.; Krausslich, H.G. Synchronized HIV assembly by tunable PIP(2) changes reveals PIP(2) requirement for stable Gag anchoring. eLife 2017, 6, e25287. [Google Scholar] [CrossRef]
- Chukkapalli, V.; Hogue, I.B.; Boyko, V.; Hu, W.S.; Ono, A. Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphosphate is essential for efficient gag membrane binding. J. Virol. 2008, 82, 2405–2417. [Google Scholar] [CrossRef]
- Gerber, P.P.; Cabrini, M.; Jancic, C.; Paoletti, L.; Banchio, C.; von Bilderling, C.; Sigaut, L.; Pietrasanta, L.I.; Duette, G.; Freed, E.O.; et al. Rab27a controls HIV-1 assembly by regulating plasma membrane levels of phosphatidylinositol 4,5-bisphosphate. J. Cell Biol. 2015, 209, 435–452. [Google Scholar] [CrossRef]
- Gonzales, B.; de Rocquigny, H.; Beziau, A.; Durand, S.; Burlaud-Gaillard, J.; Lefebvre, A.; Krull, S.; Emond, P.; Brand, D.; Piver, E. Type I Phosphatidylinositol-4-Phosphate 5-Kinases alpha and gamma Play a Key Role in Targeting HIV-1 Pr55(Gag) to the Plasma Membrane. J. Virol. 2020, 94, e00189-20. [Google Scholar] [CrossRef]
- Thornhill, D.; Olety, B.; Ono, A. Relationships between MA-RNA Binding in Cells and Suppression of HIV-1 Gag Mislocalization to Intracellular Membranes. J. Virol. 2019, 93, e00756-19. [Google Scholar] [CrossRef]
- Chukkapalli, V.; Oh, S.J.; Ono, A. Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain. Proc. Natl. Acad. Sci. USA 2010, 107, 1600–1605. [Google Scholar] [CrossRef]
- Mercredi, P.Y.; Bucca, N.; Loeliger, B.; Gaines, C.R.; Mehta, M.; Bhargava, P.; Tedbury, P.R.; Charlier, L.; Floquet, N.; Muriaux, D.; et al. Structural and Molecular Determinants of Membrane Binding by the HIV-1 Matrix Protein. J. Mol. Biol. 2016, 428, 1637–1655. [Google Scholar] [CrossRef] [PubMed]
- Murphy, R.E.; Samal, A.B.; Vlach, J.; Mas, V.; Prevelige, P.E.; Saad, J.S. Structural and biophysical characterizations of HIV-1 matrix trimer binding to lipid nanodiscs shed light on virus assembly. J. Biol. Chem. 2019, 294, 18600–18612. [Google Scholar] [CrossRef] [PubMed]
- Junkova, P.; Pleskot, R.; Prchal, J.; Sys, J.; Ruml, T. Differences and commonalities in plasma membrane recruitment of the two morphogenetically distinct retroviruses HIV-1 and MMTV. J. Biol. Chem. 2020, 295, 8819–8833. [Google Scholar] [CrossRef]
- Barros, M.; Heinrich, F.; Datta, S.A.K.; Rein, A.; Karageorgos, I.; Nanda, H.; Lösche, M. Membrane Binding of HIV-1 Matrix Protein: Dependence on Bilayer Composition and Protein Lipidation. J. Virol. 2016, 90, 4544–4555. [Google Scholar] [CrossRef]
- Keller, H.; Krausslich, H.G.; Schwille, P. Multimerizable HIV Gag derivative binds to the liquid-disordered phase in model membranes. Cell. Microbiol. 2013, 15, 237–247. [Google Scholar] [CrossRef]
- Tran, R.J.; Lalonde, M.S.; Sly, K.L.; Conboy, J.C. Mechanistic Investigation of HIV-1 Gag Association with Lipid Membranes. J. Phys. Chem. B 2019, 123, 4673–4687. [Google Scholar] [CrossRef]
- Carlson, L.A.; Hurley, J.H. In vitro reconstitution of the ordered assembly of the endosomal sorting complex required for transport at membrane-bound HIV-1 Gag clusters. Proc. Natl. Acad. Sci. USA 2012, 109, 16928–16933. [Google Scholar] [CrossRef]
- Saad, J.S.; Miller, J.; Tai, J.; Kim, A.; Ghanam, R.H.; Summers, M.F. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl. Acad. Sci. USA 2006, 103, 11364–11369. [Google Scholar] [CrossRef]
- Qu, K.; Ke, Z.; Zila, V.; Anders-Osswein, M.; Glass, B.; Mucksch, F.; Muller, R.; Schultz, C.; Muller, B.; Krausslich, H.G.; et al. Maturation of the matrix and viral membrane of HIV-1. Science 2021, 373, 700–704. [Google Scholar] [CrossRef]
- Olety, B.; Veatch, S.L.; Ono, A. Phosphatidylinositol-(4,5)-Bisphosphate Acyl Chains Differentiate Membrane Binding of HIV-1 Gag from That of the Phospholipase Cdelta1 Pleckstrin Homology Domain. J. Virol. 2015, 89, 7861–7873. [Google Scholar] [CrossRef]
- Lochrie, M.A.; Waugh, S.; Pratt, D.G., Jr.; Clever, J.; Parslow, T.G.; Polisky, B. In vitro selection of RNAs that bind to the human immunodeficiency virus type-1 gag polyprotein. Nucleic Acids Res. 1997, 25, 2902–2910. [Google Scholar] [CrossRef] [PubMed]
- Purohit, P.; Dupont, S.; Stevenson, M.; Green, M.R. Sequence-specific interaction between HIV-1 matrix protein and viral genomic RNA revealed by in vitro genetic selection. RNA 2001, 7, 576–584. [Google Scholar] [CrossRef]
- Cimarelli, A.; Luban, J. Translation elongation factor 1-alpha interacts specifically with the human immunodeficiency virus type 1 Gag polyprotein. J. Virol. 1999, 73, 5388–5401. [Google Scholar] [CrossRef]
- Ramalingam, D.; Duclair, S.; Datta, S.A.; Ellington, A.; Rein, A.; Prasad, V.R. RNA aptamers directed to human immunodeficiency virus type 1 Gag polyprotein bind to the matrix and nucleocapsid domains and inhibit virus production. J. Virol. 2011, 85, 305–314. [Google Scholar] [CrossRef]
- Jones, C.P.; Datta, S.A.; Rein, A.; Rouzina, I.; Musier-Forsyth, K. Matrix domain modulates HIV-1 Gag’s nucleic acid chaperone activity via inositol phosphate binding. J. Virol. 2011, 85, 1594–1603. [Google Scholar] [CrossRef]
- Hearps, A.C.; Wagstaff, K.M.; Piller, S.C.; Jans, D.A. The N-terminal basic domain of the HIV-1 matrix protein does not contain a conventional nuclear localization sequence but is required for DNA binding and protein self-association. Biochemistry 2008, 47, 2199–2210. [Google Scholar] [CrossRef]
- Alfadhli, A.; Still, A.; Barklis, E. Analysis of human immunodeficiency virus type 1 matrix binding to membranes and nucleic acids. J. Virol. 2009, 83, 12196–12203. [Google Scholar] [CrossRef]
- Socas, L.B.P.; Ambroggio, E.E. HIV-1 Gag specificity for PIP(2) is regulated by macromolecular electric properties of both protein and membrane local environments. Biochim. Biophys. Acta Biomembr. 2023, 1865, 184157. [Google Scholar] [CrossRef]
- Sumner, C.; Kotani, O.; Liu, S.; Musier-Forsyth, K.; Sato, H.; Ono, A. Molecular Determinants in tRNA D-arm Required for Inhibition of HIV-1 Gag Membrane Binding. J. Mol. Biol. 2022, 434, 167390. [Google Scholar] [CrossRef]
- Todd, G.C.; Duchon, A.; Inlora, J.; Olson, E.D.; Musier-Forsyth, K.; Ono, A. Inhibition of HIV-1 Gag-membrane interactions by specific RNAs. RNA 2017, 23, 395–405. [Google Scholar] [CrossRef]
- Inlora, J.; Collins, D.R.; Trubin, M.E.; Chung, J.Y.; Ono, A. Membrane binding and subcellular localization of retroviral Gag proteins are differentially regulated by MA interactions with phosphatidylinositol-(4,5)-bisphosphate and RNA. mBio 2014, 5, e02202. [Google Scholar] [CrossRef]
- Chukkapalli, V.; Inlora, J.; Todd, G.C.; Ono, A. Evidence in support of RNA-mediated inhibition of phosphatidylserine-dependent HIV-1 Gag membrane binding in cells. J. Virol. 2013, 87, 7155–7159. [Google Scholar] [CrossRef] [PubMed]
- Kutluay, S.B.; Zang, T.; Blanco-Melo, D.; Powell, C.; Jannain, D.; Errando, M.; Bieniasz, P.D. Global changes in the RNA binding specificity of HIV-1 gag regulate virion genesis. Cell 2014, 159, 1096–1109. [Google Scholar] [CrossRef] [PubMed]
- Inlora, J.; Chukkapalli, V.; Derse, D.; Ono, A. Gag localization and virus-like particle release mediated by the matrix domain of human T-lymphotropic virus type 1 Gag are less dependent on phosphatidylinositol-(4,5)-bisphosphate than those mediated by the matrix domain of HIV-1 Gag. J. Virol. 2011, 85, 3802–3810. [Google Scholar] [CrossRef]
- Dick, R.A.; Kamynina, E.; Vogt, V.M. Effect of multimerization on membrane association of Rous sarcoma virus and HIV-1 matrix domain proteins. J. Virol. 2013, 87, 13598–13608. [Google Scholar] [CrossRef] [PubMed]
- Alfadhli, A.; McNett, H.; Tsagli, S.; Bachinger, H.P.; Peyton, D.H.; Barklis, E. HIV-1 matrix protein binding to RNA. J. Mol. Biol. 2011, 410, 653–666. [Google Scholar] [CrossRef]
- Gaines, C.R.; Tkacik, E.; Rivera-Oven, A.; Somani, P.; Achimovich, A.; Alabi, T.; Zhu, A.; Getachew, N.; Yang, A.L.; McDonough, M.; et al. HIV-1 Matrix Protein Interactions with tRNA: Implications for Membrane Targeting. J. Mol. Biol. 2018, 430, 2113–2127. [Google Scholar] [CrossRef]
- Bou-Nader, C.; Muecksch, F.; Brown, J.B.; Gordon, J.M.; York, A.; Peng, C.; Ghirlando, R.; Summers, M.F.; Bieniasz, P.D.; Zhang, J. HIV-1 matrix-tRNA complex structure reveals basis for host control of Gag localization. Cell Host Microbe 2021, 29, 1421–1436.e7. [Google Scholar] [CrossRef]
- Charlier, L.; Louet, M.; Chaloin, L.; Fuchs, P.; Martinez, J.; Muriaux, D.; Favard, C.; Floquet, N. Coarse-grained simulations of the HIV-1 matrix protein anchoring: Revisiting its assembly on membrane domains. Biophys. J. 2014, 106, 577–585. [Google Scholar] [CrossRef]
- Banerjee, P.; Qu, K.; Briggs, J.A.G.; Voth, G.A. Molecular dynamics simulations of HIV-1 matrix-membrane interactions at different stages of viral maturation. Biophys. J. 2024, 123, 389–406. [Google Scholar] [CrossRef]
- Favard, C.; Chojnacki, J.; Merida, P.; Yandrapalli, N.; Mak, J.; Eggeling, C.; Muriaux, D. HIV-1 Gag specifically restricts PI(4,5)P2 and cholesterol mobility in living cells creating a nanodomain platform for virus assembly. Sci. Adv. 2019, 5, eaaw8651. [Google Scholar] [CrossRef] [PubMed]
- Mucksch, F.; Citir, M.; Luchtenborg, C.; Glass, B.; Traynor-Kaplan, A.; Schultz, C.; Brugger, B.; Krausslich, H.G. Quantification of phosphoinositides reveals strong enrichment of PIP(2) in HIV-1 compared to producer cell membranes. Sci. Rep. 2019, 9, 17661. [Google Scholar] [CrossRef] [PubMed]
- Wen, Y.; Feigenson, G.W.; Vogt, V.M.; Dick, R.A. Mechanisms of PI(4,5)P2 Enrichment in HIV-1 Viral Membranes. J. Mol. Biol. 2020, 432, 5343–5364. [Google Scholar] [CrossRef]
- Yandrapalli, N.; Lubart, Q.; Tanwar, H.S.; Picart, C.; Mak, J.; Muriaux, D.; Favard, C. Self assembly of HIV-1 Gag protein on lipid membranes generates PI(4,5)P(2)/Cholesterol nanoclusters. Sci. Rep. 2016, 6, 39332. [Google Scholar] [CrossRef]
- Grover, J.R.; Veatch, S.L.; Ono, A. Basic motifs target PSGL-1, CD43, and CD44 to plasma membrane sites where HIV-1 assembles. J. Virol. 2015, 89, 454–467. [Google Scholar] [CrossRef]
- Murakami, T.; Carmona, N.; Ono, A. Virion-incorporated PSGL-1 and CD43 inhibit both cell-free infection and transinfection of HIV-1 by preventing virus-cell binding. Proc. Natl. Acad. Sci. USA 2020, 117, 8055–8063. [Google Scholar] [CrossRef]
- Murakami, T.; Kim, J.; Li, Y.; Green, G.E.; Shikanov, A.; Ono, A. Secondary lymphoid organ fibroblastic reticular cells mediate trans-infection of HIV-1 via CD44-hyaluronan interactions. Nat. Commun. 2018, 9, 2436. [Google Scholar] [CrossRef]
- Murakami, T.; Ono, A. Roles of Virion-Incorporated CD162 (PSGL-1), CD43, and CD44 in HIV-1 Infection of T Cells. Viruses 2021, 13, 1935. [Google Scholar] [CrossRef]
- Fu, Y.; He, S.; Waheed, A.A.; Dabbagh, D.; Zhou, Z.; Trinite, B.; Wang, Z.; Yu, J.; Wang, D.; Li, F.; et al. PSGL-1 restricts HIV-1 infectivity by blocking virus particle attachment to target cells. Proc. Natl. Acad. Sci. USA 2020, 117, 9537–9545. [Google Scholar] [CrossRef]
- Liu, Y.; Song, Y.; Zhang, S.; Diao, M.; Huang, S.; Li, S.; Tan, X. PSGL-1 inhibits HIV-1 infection by restricting actin dynamics and sequestering HIV envelope proteins. Cell Discov. 2020, 6, 53. [Google Scholar] [CrossRef]
- Liu, Y.; Fu, Y.; Wang, Q.; Li, M.; Zhou, Z.; Dabbagh, D.; Fu, C.; Zhang, H.; Li, S.; Zhang, T.; et al. Proteomic profiling of HIV-1 infection of human CD4(+) T cells identifies PSGL-1 as an HIV restriction factor. Nat. Microbiol. 2019, 4, 813–825. [Google Scholar] [CrossRef]
- Cardoso, R.d.S.; Murakami, T.; Jacobovitz, B.; Veatch, S.L.; Ono, A. PI(4,5)P2 promotes the incorporation of CD43, PSGL-1 and CD44 into nascent HIV-1 particles. bioRxiv 2024. [CrossRef]
- Dalton, A.K.; Ako-Adjei, D.; Murray, P.S.; Murray, D.; Vogt, V.M. Electrostatic interactions drive membrane association of the human immunodeficiency virus type 1 Gag MA domain. J. Virol. 2007, 81, 6434–6445. [Google Scholar] [CrossRef]
- Vlach, J.; Saad, J.S. Trio engagement via plasma membrane phospholipids and the myristoyl moiety governs HIV-1 matrix binding to bilayers. Proc. Natl. Acad. Sci. USA 2013, 110, 3525–3530. [Google Scholar] [CrossRef]
- Monje-Galvan, V.; Voth, G.A. Binding mechanism of the matrix domain of HIV-1 gag on lipid membranes. eLife 2020, 9, e58621. [Google Scholar] [CrossRef]
- Sumner, C.; Ono, A. The “basics” of HIV-1 assembly. PLoS Pathog. 2024, 20, e1011937. [Google Scholar] [CrossRef]
- Chua, B.A.; Ngo, J.A.; Situ, K.; Morizono, K. Roles of phosphatidylserine exposed on the viral envelope and cell membrane in HIV-1 replication. Cell Commun. Signal. 2019, 17, 132. [Google Scholar] [CrossRef]
- Moller-Tank, S.; Maury, W. Phosphatidylserine receptors: Enhancers of enveloped virus entry and infection. Virology 2014, 468–470, 565–580. [Google Scholar] [CrossRef]
- Callahan, M.K.; Popernack, P.M.; Tsutsui, S.; Truong, L.; Schlegel, R.A.; Henderson, A.J. Phosphatidylserine on HIV envelope is a cofactor for infection of monocytic cells. J. Immunol. 2003, 170, 4840–4845. [Google Scholar] [CrossRef]
- Fadok, V.A.; Voelker, D.R.; Campbell, P.A.; Cohen, J.J.; Bratton, D.L.; Henson, P.M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 1992, 148, 2207–2216. [Google Scholar] [CrossRef]
- Segawa, K.; Nagata, S. An Apoptotic ‘Eat Me’ Signal: Phosphatidylserine Exposure. Trends Cell Biol. 2015, 25, 639–650. [Google Scholar] [CrossRef]
- Mercer, J.; Helenius, A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008, 320, 531–535. [Google Scholar] [CrossRef]
- Mercer, J.; Knebel, S.; Schmidt, F.I.; Crouse, J.; Burkard, C.; Helenius, A. Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry. Proc. Natl. Acad. Sci. USA 2010, 107, 9346–9351. [Google Scholar] [CrossRef]
- Li, M.; Ablan, S.D.; Miao, C.; Zheng, Y.M.; Fuller, M.S.; Rennert, P.D.; Maury, W.; Johnson, M.C.; Freed, E.O.; Liu, S.L. TIM-family proteins inhibit HIV-1 release. Proc. Natl. Acad. Sci. USA 2014, 111, E3699–E3707. [Google Scholar] [CrossRef]
- Rosa, A.; Chande, A.; Ziglio, S.; De Sanctis, V.; Bertorelli, R.; Goh, S.L.; McCauley, S.M.; Nowosielska, A.; Antonarakis, S.E.; Luban, J.; et al. HIV-1 Nef promotes infection by excluding SERINC5 from virion incorporation. Nature 2015, 526, 212–217. [Google Scholar] [CrossRef]
- Usami, Y.; Wu, Y.; Gottlinger, H.G. SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef. Nature 2015, 526, 218–223. [Google Scholar] [CrossRef]
- Sid Ahmed, S.; Bajak, K.; Fackler, O.T. Beyond Impairment of Virion Infectivity: New Activities of the Anti-HIV Host Cell Factor SERINC5. Viruses 2024, 16, 284. [Google Scholar] [CrossRef]
- Leonhardt, S.A.; Purdy, M.D.; Grover, J.R.; Yang, Z.; Poulos, S.; McIntire, W.E.; Tatham, E.A.; Erramilli, S.K.; Nosol, K.; Lai, K.K.; et al. Antiviral HIV-1 SERINC restriction factors disrupt virus membrane asymmetry. Nat. Commun. 2023, 14, 4368. [Google Scholar] [CrossRef]
- Raghunath, G.; Abbott, E.H.; Marin, M.; Wu, H.; Reyes Ballista, J.M.; Brindley, M.A.; Melikyan, G.B. Disruption of Transmembrane Phosphatidylserine Asymmetry by HIV-1 Incorporated SERINC5 Is Not Responsible for Virus Restriction. Biomolecules 2024, 14, 570. [Google Scholar] [CrossRef]
- Harrison, M.S.; Sakaguchi, T.; Schmitt, A.P. Paramyxovirus assembly and budding: Building particles that transmit infections. Int. J. Biochem. Cell Biol. 2010, 42, 1416–1429. [Google Scholar] [CrossRef]
- Swain, J.; Bierre, M.; Veyrie, L.; Richard, C.A.; Eleouet, J.F.; Muriaux, D.; Bajorek, M. Selective targeting and clustering of phosphatidylserine lipids by RSV M protein is critical for virus particle production. J. Biol. Chem. 2023, 299, 105323. [Google Scholar] [CrossRef]
- Wang, J.; Gambhir, A.; Hangyas-Mihalyne, G.; Murray, D.; Golebiewska, U.; McLaughlin, S. Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions. J. Biol. Chem. 2002, 277, 34401–34412. [Google Scholar] [CrossRef]
- Murphy, R.E.; Samal, A.B.; Vlach, J.; Saad, J.S. Solution Structure and Membrane Interaction of the Cytoplasmic Tail of HIV-1 gp41 Protein. Structure 2017, 25, 1708–1718.e05. [Google Scholar] [CrossRef]
- Harris, A.; Cardone, G.; Winkler, D.C.; Heymann, J.B.; Brecher, M.; White, J.M.; Steven, A.C. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl. Acad. Sci. USA 2006, 103, 19123–19127. [Google Scholar] [CrossRef]
- Calder, L.J.; Wasilewski, S.; Berriman, J.A.; Rosenthal, P.B. Structural organization of a filamentous influenza A virus. Proc. Natl. Acad. Sci. USA 2010, 107, 10685–10690. [Google Scholar] [CrossRef]
- Inamdar, K.; Tsai, F.C.; Dibsy, R.; de Poret, A.; Manzi, J.; Merida, P.; Muller, R.; Lappalainen, P.; Roingeard, P.; Mak, J.; et al. Full assembly of HIV-1 particles requires assistance of the membrane curvature factor IRSp53. eLife 2021, 10, e67321. [Google Scholar]
- Kumakura, M.; Kawaguchi, A.; Nagata, K. Actin-myosin network is required for proper assembly of influenza virus particles. Virology 2015, 476, 141–150. [Google Scholar] [CrossRef]
- Bedi, S.; Ono, A. Friend or Foe: The Role of the Cytoskeleton in Influenza A Virus Assembly. Viruses 2019, 11, 46. [Google Scholar] [CrossRef]
- Morizono, K.; Chen, I.S. Role of phosphatidylserine receptors in enveloped virus infection. J. Virol. 2014, 88, 4275–4290. [Google Scholar]
- Amara, A.; Mercer, J. Viral apoptotic mimicry. Nat. Rev. Microbiol. 2015, 13, 461–469. [Google Scholar]
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de Souza Cardoso, R.; Ono, A. The Effects of Viral Structural Proteins on Acidic Phospholipids in Host Membranes. Viruses 2024, 16, 1714. https://doi.org/10.3390/v16111714
de Souza Cardoso R, Ono A. The Effects of Viral Structural Proteins on Acidic Phospholipids in Host Membranes. Viruses. 2024; 16(11):1714. https://doi.org/10.3390/v16111714
Chicago/Turabian Stylede Souza Cardoso, Ricardo, and Akira Ono. 2024. "The Effects of Viral Structural Proteins on Acidic Phospholipids in Host Membranes" Viruses 16, no. 11: 1714. https://doi.org/10.3390/v16111714
APA Stylede Souza Cardoso, R., & Ono, A. (2024). The Effects of Viral Structural Proteins on Acidic Phospholipids in Host Membranes. Viruses, 16(11), 1714. https://doi.org/10.3390/v16111714