The role of lipid rafts in the immune system and SARS-CoV-2 cell invasion
https://doi.org/10.36604/1998-5029-2023-89-146-158
Abstract
Introduction. Glycosphingolipids are compounds composed of hydrophilic sugar structures and hydrophobic ceramides. These molecules form lipid rafts or microdomains in the cell membrane together with cholesterol, sphingomyelin, glycosylphosphatidylinositol and molecules, which determines their properties.
Aim. To systematize data on the structure of lipid rafts, their involvement in the functioning of immunocompetent cells and the development of the immune response, and the mechanisms of SARS-CoV-2 viral invasion.
Materials and methods. From these positions, literary sources for 1981-2023 are analyzed. Literature search was carried out in information systems: PubMed and Google Scholar.
Results. There are separate works that reflect the role of lipid rafts as mediators of signal transduction in the development of innate and adaptive immune responses. Other studies describe their importance in pathogen-host interaction and avoidance of immune control. Recently, studies have appeared on the effect of lipid microdomains of the cell membrane on viral invasion, including that caused by SARS-CoV-2.
Conclusion. This review makes a significant contribution to understanding the role of lipid rafts in the functioning of the immune system and viral invasion, which determines the prospects for further research and the possibility of their use as therapeutic targets in the development of immunomodulatory drugs.
About the Authors
E. M. UstinovRussian Federation
Egor M. Ustinov, Research Laboratory Assistant, Laboratory of Mechanisms of Etiopathogenesis and Recovery Processes of the Respiratory System at Non-Specific Lung Diseases
22 Kalinina Str., Blagoveshchensk, 675000
I. A. Andrievskaya
Russian Federation
Irina A. Andrievskaya, PhD, DSc (Biol.), Professor of RAS, Head of Laboratory of Mechanisms of Etiopathogenesis and Recovery Processes of the Respiratory System at Non-Specific Lung Diseases
22 Kalinina Str., Blagoveshchensk, 675000
K. S. Lyazgiyan
Russian Federation
Karen S. Lyazgiyan, PhD student, Laboratory of Mechanisms of Etiopathogenesis and Recovery Processes of the Respiratory System at Non-Specific Lung Diseases
22 Kalinina Str., Blagoveshchensk, 675000
References
1. Hakomori S. Glycosphingolipids in cellular interaction, differentiation, and oncogenesis. Annu. Rev. Biochem. 1981; 50(1):733–764. https://doi.org/10.1146/annurev.bi.50.070181.003505
2. Kusumi A., Fujiwara T.K., Tsunoyama T.A., Kasai R.S., Liu A., Hirosawa K.M., Kinoshita M., Matsumori N., Komura N., Ando H., Suzuki K.G. Defining raft domains in the plasma membrane. Traffic 2019; 21(1):106–137. https://doi.org/10.1111/tra.12718
3. Murate M., Abe M., Kasahara K., Iwabuchi K., Umeda M., Kobayashi T. Transbilayer lipid distribution in Nano Scale. J. Cell. Sci. 2015; 128(8):1627−1638. https://doi.org/10.1242/jcs.163105
4. Iwabuchi K., Nakayama H., Oizumi A., Suga Y., Ogawa H., Takamori K. Role of ceramide from glycosphingolipids and its metabolites in immunological and inflammatory responses in humans. Mediators Inflamm. 2015; 2015:120748. https://doi.org/10.1155/2015/120748
5. Schengrund C-L. “Multivalent” Saccharides: Development of new approaches for inhibiting the effects of glycosphingolipid-binding pathogens. Biochem. Pharmacol. 2003; 65(5):699–707. https://doi.org/10.1016/s0006-2952(02)01553-8
6. Yates A., Rampersaud A. Sphingolipids as receptor modulators: An overview. Ann. N.Y. Acad. Sci. 1998; 845(1):57– 71. https://doi.org/10.1111/j.1749-6632.1998.tb09662.x
7. Kabayama K., Sato T., Saito K., Loberto N., Prinetti A., Sonnino S., Kinjo M., Igarashi Y., Inokuchi J. Dissociation of the insulin receptor and caveolin-1 complex by ganglioside GM3 in the state of insulin resistance. Proc. Nat. Acad. Sci. USA. 2007; 104(34):13678–13683. https://doi.org/10.1073/pnas.0703650104
8. Prasanna X., Jafurulla M.D., Sengupta D., Chattopadhyay A. The ganglioside GM1 interacts with the serotonin 1A receptor via the sphingolipid binding domain. Biochim. Biophys. Acta 2016; 1858(11):2818–2826. https://doi.org/10.1016/j.bbamem.2016.08.009
9. Kumar A., Suryadevara N., Hill T.M., Bezbradica J.S., Van Kaer L., Joyce S. Natural killer T cells: An Ecological Evolutionary Developmental Biology Perspective. Front. Immunol. 2017; 8:1858. https://doi.org/10.3389/fimmu.2017.01858
10. Blander J.M., Medzhitov R. Regulation of phagosome maturation by signals from toll-like receptors. Science 2004; 304(5673):1014–1018. https://doi.org/10.1126/science.1096158
11. Duan Z., He Y., Wang J., Chen X., Chen Q., Li M. Candida auris induces phagocytosis, reactive oxygen species production and inflammation through TLR2, TLR4 and dectin-1 dependent signaling in macrophages. Research Square 2023; preprint (version 1). https://doi.org/10.21203/rs.3.rs-2765520/v1
12. Houde M., Gottschalk M., Gagnon F., Van Calsteren M-R., Segura M. Streptococcus suis capsular polysaccharide inhibits phagocytosis through destabilization of lipid microdomains and prevents lactosylceramide-dependent recognition. Infect. Immun. 2012; 80(2):506–517. https://doi.org/10.1128/IAI.05734-11
13. Nakayama H., Kurihara H., Morita Y.S., Kinoshita T., Mauri L., Prinetti A., Sonnino S., Yokoyama N., Ogawa H., Takamori K., Iwabuchi K. Lipoarabinomannan binding to lactosylceramide in lipid rafts is essential for the phagocytosis of Mycobacteria by human neutrophils. Sci. Signal. 2016; 9(449):ra101. https://doi.org/10.1126/scisignal.aaf1585
14. Hakomori S. Structure, organization, and function of glycosphingolipids in membrane. Curr. Opin. Hematol. 2003; 10(1):16–24. https://doi.org/10.1097/00062752-200301000-00004
15. Álvarez R., López D.J., Casas J., Lladó V., Higuera M., Nagy T., Barceló M., Busquets X., Escribá P.V. G protein– membrane interactions I: Gαi1 myristoyl and palmitoyl modifications in protein–lipid interactions and its implications in membrane microdomain localization. Biochim. Biophys. Acta 2015; 1851(11):1511–1520. https://doi.org/10.1016/j.bbalip.2015.08.001
16. Chiricozzi E., Ciampa M.G., Brasile G., Compostella F., Prinetti A., Nakayama H., Ekyalongo R.C., Iwabuchi K., Sonnino S., Mauri L. Direct interaction, instrumental for signaling processes, between LacCer and Lyn in the lipid rafts of neutrophil-like cells. J. Lipid Res. 2015; 56(1):129–141. https://doi.org/10.1194/jlr.M055319
17. Arnaout M. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 1990; 75(5):1037– 1050. PMID: 1968349.
18. Piccardoni P., Manarini S., Federico L., Bagoly Z., Pecce R., Martelli N., Piccoli A., Totani L., Cerletti C and Evangelista V. SRC-dependent outside-in signalling is a key step in the process of autoregulation of beta2 integrins in polymorphonuclear cells. Biochem. J. 2004; 380(Pt1):57–65. https://doi.org/10.1042/BJ20040151
19. Vetvicka V., Thornton B.P., Ross G.D. Soluble beta-glucan polysaccharide binding to the lectin site of neutrophil or natural killer cell complement receptor type 3 (CD11B/CD18) generates a primed state of the receptor capable of mediating cytotoxicity of IC3B-opsonized target cells. J. Clin. Invest. 1996; 98(1):50–61. https://doi.org/10.1172/JCI118777
20. Kulkarni R., Wiemer E.A., Chang W. Role of lipid rafts in pathogen-host interaction − A Mini Review. Front. Immunol. 2022; 12:815020. https://doi.org/10.3389/fimmu.2021.815020
21. Kotzé L.A., Young C., Leukes V.N., John V., Fang Z., Walzl G., Lutz M.B., du Plessis N. Mycobacterium tuberculosis and myeloid-derived suppressor cells: Insights into caveolin rich lipid rafts. EBioMedicine 2020; 53:102670. https://doi.org/10.1016/j.ebiom.2020.102670
22. Iwabuchi K., Nakayama H., Hanafusa K. Lactosylceramide-enriched microdomains mediate human neutrophil immunological functions via carbohydrate-carbohydrate interaction. Glycoconj. J. 2022; 39(2):239–46. https://doi.org/10.1007/s10719-022-10060-0
23. Hanafusa K., Hotta T., Iwabuchi K. Glycolipids: Linchpins in the organization and function of membrane microdomains. Front. Cell Dev. Biol. 2020; 8:589799. https://doi.org/10.3389/fcell.2020.589799
24. Thomas S., Preda-Pais A., Casares S., Brumeanu T. Analysis of lipid rafts in T cells. Mol. Immunol. 2004; 41(4):399–409. https://doi.org/10.1016/j.molimm.2004.03.022
25. Hosokawa H., Rothenberg E.V. Cytokines, transcription factors, and the initiation of T-cell development. Cold Spring Harb. Perspect. Biol. 2018; 10(5):a028621. https://doi.org/10.1101/cshperspect.a028621
26. Yamasaki S., Saito T. Molecular basis for pre-tcr-mediated autonomous signaling. Trends Immunol. 2007; 28(1):39– 43. https://doi.org/10.1016/j.it.2006.11.006
27. Saint-Ruf C., Panigada M., Azogui O., Debey P., von Boehmer H., Grassi F. Different initiation of pre-TCR and γδTCR signalling. Nature 2000; 406(6795):524–527. https://doi.org/10.1038/35020093
28. Ferrera D., Panigada M., Porcellini S., Grassi F. Recombinase-deficient T cell development by selective accumulation of CD3 into lipid rafts. Eur. J. Immunol. 2008; 38(4):1148–1156. https://doi.org/10.1002/eji.200737917
29. Fu G., Yu M., Chen Y., Zheng Y., Zhu W., Newman D.K., Wang D., Wen R. Phospholipase Cγ1 is required for preTCR signal transduction and pre-T cell development. Eur. J. Immunol. 2018; 47(1):74–83. https://doi.org/10.1002/eji.201646522
30. Bovolenta E.R., García-Cuesta E.M., Horndler L., Ponomarenko J., Schamel W.W., Mellado M., Castro M., Abia D., van Santen H.M. A set point in the selection of the αβtcr T cell repertoire imposed by pre-TCR signaling strength. Proc. Natl Acad. Sci. USA. 2022; 119(22):e2201907119. https://doi.org/10.1073/pnas.2201907119
31. Popovic Z.V., Rabionet M., Jennemann R., Krunic D., Sandhoff R., Gröne H-J., Porubsky S. Glucosylceramide synthase is involved in development of invariant natural killer T cells. Front. Immunol. 2017; 8:848. https://doi.org/10.3389/fimmu.2017.00848
32. Petrov A.M., Zefirov A.L. [Cholesterol and lipid rafts in the biological membranes. Role in the release, reception and ion channel functions]. Uspekhi Fiziologicheskikh Nauk 2013; 44(1):17−38 (in Russian).
33. Inokuchi J., Nagafuku M., Ohno I., Suzuki A. Distinct selectivity of gangliosides required for CD4+ T and CD8+ T cell activation. Biochim. Biophys. Acta 2015; 1851(1):98–106. https://doi.org/10.1016/j.bbalip.2014.07.013
34. Imanishi T., Saito T. T cell co-stimulation and functional modulation by innate signals. Trends Immunol. 2020; 41(3):200–212. https://doi.org/10.1016/j.it.2020.01.003
35. Chapoval A.I., Chapoval S.P., Shcherbakova N.S., Shcherbakov D.N. Immune checkpoints of the B7 family. Part 2. representatives of the B7 family B7-H3, B7-H4, B7-H5, B7-H6, B7-H7, and ILDR2 and their receptors. Russ. J. Bioorg. Chem. 2019; 45(5):321–334. https://doi.org/10.1134/S1068162019050091
36. Kläsener K., Maity P.C., Hobeika E., Yang J., Reth M. B cell activation involves nanoscale receptor reorganizations and inside-out signaling by Syk. eLife 2014; 3:e02069. https://doi.org/10.7554/eLife.02069
37. Minguet S., Kläsener K., Schaffer A-M., Fiala GJ., Osteso-Ibánez T., Raute K., Navarro-Lérida I., Hartl F.A., Seidl M., Reth M., Del Pozo MA. Caveolin-1-dependent nanoscale organization of the BCR regulates B cell tolerance. Nat. Immunol. 2018; 18(10):1150–1159. https://doi.org/10.1038/ni.3813
38. Palacios-Rápalo S.N., De Jesús-González L.A., Cordero-Rivera C.D., Farfan-Morales C.N., Osuna-Ramos JF., Martínez-Mier G., Quistián-Galván J., Muñoz-Pérez A., Bernal-Dolores V., del Ángel R.M., Reyes-Ruiz J.M. Cholesterol-rich lipid rafts as platforms for SARS-COV-2 entry. Front. Immunol. 2021; 12:796855. https://doi.org/10.3389/fimmu.2021.796855
39. Llorente García I., Marsh M. A biophysical perspective on receptor-mediated virus entry with a focus on HIV. Biochim. Biophys. Acta Biomembr. 2020; 1862(6):183158. https:// doi.org/10.1016/j.bbamem.2019.183158
40. Wang Y., Grunewald M., Perlman S. Coronaviruses: An updated overview of their replication and pathogenesis. Methods Mol. Biol. 2020; 2203:1–29. https://doi.org/10.1007/978-1-0716-0900-2_1
41. Sviridov D., Miller Y.I., Ballout R.A., Remaley A.T., Bukrinsky M. Targeting lipid rafts ‒ a potential therapy for COVID-19. Front. Immunol. 2020; 11:574508. https://doi.org/10.3389/fimmu.2020.574508
42. Hoffmann M., Kleine-Weber H., Schroeder S., Krüger N., Herrler T., Erichsen S., Schiergens T.S., Herrler G., Wu N-H., Nitsche A., Müller M.A., Drosten C., Pöhlmann S. SARS-COV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 2020; 181(2):271‒280. https://doi.org/10.1016/j.cell.2020.02.052
43. Ballout R.A., Sviridov D., Bukrinsky M.I., Remaley A.T. The lysosome: A potential juncture between SARS‐CoV‐2 infectivity and niemann‐pick disease type C, with therapeutic implications. FASEB J. 2020; 34(6):7253–7264. https://doi.org/10.1096/fj.202000654R
44. Owczarek K., Szczepanski A., Milewska A., Baster Z., Rajfur Z., Sarna M., Pyrc K. Early events during human coronavirus OC43 entry to the cell. Sci. Rep. 2018; 8:7124. https://doi.org/10.1038/s41598-018-25640-0
45. Ewers H., Helenius A. Lipid-mediated endocytosis. Cold Spring Harb. Perspect. Biol. 2011; 3(8):a004721. https://doi.org/10.1101/cshperspect.a004721
46. Guo H., Huang M., Yuan Q., Wei Y., Gao Y., Mao L., Gu L., Tan Y.W., Zhong Y., Liu D., Sun S. The important role of lipid raft-mediated attachment in the infection of cultured cells by coronavirus infectious bronchitis virus Beaudette strain. PLoS One 2017; 12(1):e0170123. https://doi.org/10.1371/journal.pone.0170123
47. Faisal H.M.N., Katti K.S., Katti D.R. Binding of SARS-COV-2 (COVID-19) and SARS-COV to human ACE2: Identifying binding sites and consequences on ACE2 stiffness. Chem. Phys. 2021; 551:111353. https://doi.org/10.1016/j.chemphys.2021.111353
48. Lu Y., Liu D.X., Tam J.P. Lipid rafts are involved in SARS-COV entry into Vero E6 cells. Biochem Biophys. Res. Commun. 2008; 369(2):344–349. https://doi.org/10.1016/j.bbrc.2008.02.023
49. Chaudhary N., Gomez G.A., Howes M.T., Lo H.P., McMahon K-A., Rae J.A., Schieber N.L., Hill M.M., Gaus K., Yap A.S., Parton R.G. Endocytic crosstalk: Cavins, caveolins, and caveolae regulate clathrin-independent endocytosis. PLoS Biol. 2014; 12(4):e1001832. https://doi.org/10.1371/journal.pbio.1001832
50. Jolly C., Sattentau Q.J. Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity. J. Virol. 2005; 79(18):12088–12094. https://doi.org/10.1128/JVI.79.18.12088-12094.2005
51. Wang H., Yang P., Liu K., Guo F., Zhang Y., Zhang G., Jiang C. SARS coronavirus entry into host cells through a novel clathrin- and caveolae-independent endocytic pathway. Cell Res. 2008; 18(2):290–301. https://doi.org/10.1038/cr.2008.15
Review
For citations:
Ustinov E.M., Andrievskaya I.A., Lyazgiyan K.S. The role of lipid rafts in the immune system and SARS-CoV-2 cell invasion. Bulletin Physiology and Pathology of Respiration. 2023;(89):146-158. (In Russ.) https://doi.org/10.36604/1998-5029-2023-89-146-158