open access

Vol 57, No 2 (2019)
REVIEW
Published online: 2019-05-16
Submitted: 2019-02-08
Accepted: 2019-04-17
Get Citation

MPP1-based mechanism of resting state raft organization in the plasma membrane. Is it a general or specialized mechanism in erythroid cells?

Magdalena Trybus, Lukasz Niemiec, Agnieszka Biernatowska, Anita Hryniewicz-Jankowska, Aleksander F. Sikorski
DOI: 10.5603/FHC.a2019.0007
·
Pubmed: 31099889
·
Folia Histochem Cytobiol 2019;57(2):43-55.

open access

Vol 57, No 2 (2019)
REVIEW
Published online: 2019-05-16
Submitted: 2019-02-08
Accepted: 2019-04-17

Abstract

Biological membranes are organized in various microdomains, one of the best known being called membrane rafts. The major function of these is thought to organize signaling partners into functional complexes. An important protein found in membrane raft microdomains of erythroid and other blood cells is MPP1 (membrane palmitoylated protein 1)/p55. MPP1 (p55) belongs to the MAGUK (membrane-associated guanylate kinase homolog) family and it is a major target of palmitoylation in the red blood cells (RBCs) membrane. The well-known function of this protein is to participate in formation of the junctional complex of the erythrocyte mem­brane skeleton. However, its function as a “raft organizer” is not well understood. In this review we focus on recent reports concerning MPP1 participation in membrane rafts organization in erythroid cells, including its role in signal transduction. Currently it is not known whether MPP1 could have a similar role in cell types other than erythroid lineage. We present also preliminary data regarding the expression level of MPP1 gene in several non-erythroid cell lines.

Abstract

Biological membranes are organized in various microdomains, one of the best known being called membrane rafts. The major function of these is thought to organize signaling partners into functional complexes. An important protein found in membrane raft microdomains of erythroid and other blood cells is MPP1 (membrane palmitoylated protein 1)/p55. MPP1 (p55) belongs to the MAGUK (membrane-associated guanylate kinase homolog) family and it is a major target of palmitoylation in the red blood cells (RBCs) membrane. The well-known function of this protein is to participate in formation of the junctional complex of the erythrocyte mem­brane skeleton. However, its function as a “raft organizer” is not well understood. In this review we focus on recent reports concerning MPP1 participation in membrane rafts organization in erythroid cells, including its role in signal transduction. Currently it is not known whether MPP1 could have a similar role in cell types other than erythroid lineage. We present also preliminary data regarding the expression level of MPP1 gene in several non-erythroid cell lines.

Get Citation

Keywords

membrane palmitoylated protein 1 (MPP1); resting state rafts; lateral membrane organization; raft-associated proteins

About this article
Title

MPP1-based mechanism of resting state raft organization in the plasma membrane. Is it a general or specialized mechanism in erythroid cells?

Journal

Folia Histochemica et Cytobiologica

Issue

Vol 57, No 2 (2019)

Pages

43-55

Published online

2019-05-16

DOI

10.5603/FHC.a2019.0007

Pubmed

31099889

Bibliographic record

Folia Histochem Cytobiol 2019;57(2):43-55.

Keywords

membrane palmitoylated protein 1 (MPP1)
resting state rafts
lateral membrane organization
raft-associated proteins

Authors

Magdalena Trybus
Lukasz Niemiec
Agnieszka Biernatowska
Anita Hryniewicz-Jankowska
Aleksander F. Sikorski

References (91)
  1. Machnicka B, Czogalla A, Hryniewicz-Jankowska A, et al. Spectrins: a structural platform for stabilization and activation of membrane channels, receptors and transporters. Biochim Biophys Acta. 2014; 1838(2): 620–634.
  2. Machnicka B, Grochowalska R, Bogusławska DM, et al. Spectrin-based skeleton as an actor in cell signaling. Cell Mol Life Sci. 2012; 69(2): 191–201.
  3. Lux SE. Anatomy of the red cell membrane skeleton: unanswered questions. Blood. 2016; 127(2): 187-199. .
  4. Sikorski AF, Podkalicka J, Jones W, et al. Membrane rafts in the erythrocyte membrane: a novel role of MPP1p55. Adv Exp Med Biol. 2015; 842: 61–78.
  5. Koshino I, Takakuwa Y. Disruption of lipid rafts by lidocaine inhibits erythrocyte invasion by Plasmodium falciparum. Exp Parasitol. 2009; 123(4): 381–383.
  6. Kamata K, Manno S, Ozaki M, et al. Functional evidence for presence of lipid rafts in erythrocyte membranes: Gsalpha in rafts is essential for signal transduction. Am J Hematol. 2008; 83(5): 371–375.
  7. Hashimoto M, Hossain S, Katakura M, et al. The binding of Aβ1-42 to lipid rafts of RBC is enhanced by dietary docosahexaenoic acid in rats: Implicates to Alzheimer's disease. Biochim Biophys Acta. 2015; 1848(6): 1402–1409.
  8. Leonard C, Conrard L, Guthmann M, et al. Contribution of plasma membrane lipid domains to red blood cell (re) shaping. Sci Rep. 2017; 7(1): 4264.
  9. Simons K, Ikonen E. Functional rafts in cell membranes. Nature. 1997; 387(6633): 569–572.
  10. Raghunathan K, Kenworthy AK. Dynamic pattern generation in cell membranes: Current insights into membrane organization. Biochim Biophys Acta Biomembr. 2018; 1860(10): 2018–2031.
  11. Bieberich E. Sphingolipids and lipid rafts: Novel concepts and methods of analysis. Chem Phys Lipids. 2018; 216: 114–131.
  12. Kinoshita M, Suzuki KGN, Murata M, et al. Evidence of lipid rafts based on the partition and dynamic behavior of sphingomyelins. Chem Phys Lipids. 2018; 215: 84–95.
  13. Rawat SS, Zimmerman C, Johnson BT, et al. Restricted lateral mobility of plasma membrane CD4 impairs HIV-1 envelope glycoprotein mediated fusion. Mol Membr Biol. 2008; 25(1): 83–94.
  14. Pucadyil TJ, Chattopadhyay A. Effect of cholesterol on lateral diffusion of fluorescent lipid probes in native hippocampal membranes. Chem Phys Lipids. 2006; 143(1-2): 11–21.
  15. Simons K, Vaz WLC. Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct. 2004; 33: 269–295.
  16. Lingwood D, Simons K. Detergent resistance as a tool in membrane research. Nat Protoc. 2007; 2(9): 2159–2165.
  17. Lichtenberg D, Goñi FM, Heerklotz H. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem Sci. 2005; 30(8): 430–436.
  18. Pike LJ, Han X, Gross RW. Epidermal Growth Factor Receptors Are Localized to Lipid Rafts. J Biol Chem 2005;280(29): 26796-26804 . .
  19. Grzybek M, Kubiak J, Łach A, et al. A raft-associated species of phosphatidylethanolamine interacts with cholesterol comparably to sphingomyelin. A Langmuir-Blodgett monolayer study. PLoS One. 2009; 4(3): e5053.
  20. Brown DA, London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem. 2000; 275(23): 17221–17224.
  21. Browman DT, Hoegg MB, Robbins SM. The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol. 2007; 17(8): 394–402.
  22. Wang TY, Leventis R, Silvius JR. Fluorescence-based evaluation of the partitioning of lipids and lipidated peptides into liquid-ordered lipid microdomains: a model for molecular partitioning into. Biophys J. 2000; 79(2): 919–933.
  23. Fantini J, Barrantes FJ. How cholesterol interacts with membrane proteins: an exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains. Front Physiol. 2013; 4: 31.
  24. Mahfoud R, Garmy N, Maresca M, et al. Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins. J Biol Chem. 2002; 277(13): 11292–11296.
  25. Boggon TJ, Eck MJ. Structure and regulation of Src family kinases. Oncogene. 2004; 23(48): 7918–7927.
  26. Pike L. Lipid rafts. Journal of Lipid Research. 2003; 44(4): 655–667.
  27. Aydar E, Palmer CP, Djamgoz MBA. Sigma receptors and cancer: possible involvement of ion channels. Cancer Res. 2004; 64(15): 5029–5035.
  28. Hryniewicz-Jankowska A, Augoff K, Biernatowska A, et al. Membrane rafts as a novel target in cancer therapy. Biochim Biophys Acta. 2014; 1845(2): 155–165.
  29. Staubach S, Hanisch FG. Lipid rafts: signaling and sorting platforms of cells and their roles in cancer. Expert Rev Proteomics. 2011; 8(2): 263–277.
  30. Field KA, Holowka D, Baird B. Fc epsilon RI-mediated recruitment of p53/56lyn to detergent-resistant membrane domains accompanies cellular signaling. Proc Natl Acad Sci U S A. 1995; 92(20): 9201–9205.
  31. Varshney P, Yadav V, Saini N. Lipid rafts in immune signalling: current progress and future perspective. Immunology. 2016; 149(1): 13–24.
  32. Dick RA, Goh SL, Feigenson GW, et al. HIV-1 Gag protein can sense the cholesterol and acyl chain environment in model membranes. Proc Natl Acad Sci U S A. 2012; 109(46): 18761–18766.
  33. Chinnapen DJF, Chinnapen H, Saslowsky D, et al. Rafting with cholera toxin: endocytosis and trafficking from plasma membrane to ER. FEMS Microbiol Lett. 2007; 266(2): 129–137.
  34. Sandvig K, Bergan J, Kavaliauskiene S, et al. Lipid requirements for entry of protein toxins into cells. Prog Lipid Res. 2014; 54: 1–13.
  35. Raghunathan K, Foegeding NJ, Campbell AM, et al. Determinants of Raft Partitioning of the Helicobacter pylori Pore-Forming Toxin VacA. Infect Immun. 2018; 86(5).
  36. Morey P, Pfannkuch L, Pang E, et al. Helicobacter pylori Depletes Cholesterol in Gastric Glands to Prevent Interferon Gamma Signaling and Escape the Inflammatory Response. Gastroenterology. 2018; 154(5): 1391–1404.e9.
  37. Rios FJO, Ferracini M, Pecenin M, et al. Uptake of oxLDL and IL-10 production by macrophages requires PAFR and CD36 recruitment into the same lipid rafts. PLoS One. 2013; 8(10): e76893.
  38. Rios FJ, Koga MM, Pecenin M, et al. Oxidized LDL induces alternative macrophage phenotype through activation of CD36 and PAFR. Mediators Inflamm. 2013; 2013: 198193.
  39. Kaul S, Xu H, Zabalawi M, et al. Lipid-Free Apolipoprotein A-I Reduces Progression of Atherosclerosis by Mobilizing Microdomain Cholesterol and Attenuating the Number of CD131 Expressing Cells: Monitoring Cholesterol Homeostasis Using the Cellular Ester to Total Cholesterol Ratio. J Am Heart Assoc. 2016; 5(11).
  40. Huang SS, Liu IH, Chen CL, et al. 7-Dehydrocholesterol (7-DHC), But Not Cholesterol, Causes Suppression of Canonical TGF-β Signaling and Is Likely Involved in the Development of Atherosclerotic Cardiovascular Disease (ASCVD). J Cell Biochem. 2017; 118(6): 1387–1400.
  41. Hancock JF. Lipid rafts: contentious only from simplistic standpoints. Nat Rev Mol Cell Biol. 2006; 7(6): 456–462.
  42. Simons K, Gerl MJ. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol. 2010; 11(10): 688–699.
  43. Pike LJ. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J Lipid Res. 2006; 47(7): 1597–1598.
  44. Sezgin E, Levental I, Mayor S, et al. The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat Rev Mol Cell Biol. 2017; 18(6): 361–374.
  45. Sevcsik E, Schütz GJ. With or without rafts? Alternative views on cell membranes. Bioessays. 2016; 38(2): 129–139.
  46. Ramstedt B, Slotte JP. Interaction of cholesterol with sphingomyelins and acyl-chain-matched phosphatidylcholines: a comparative study of the effect of the chain length. Biophys J. 1999; 76(2): 908–915.
  47. Lozano MM, Hovis JS, Moss FR, et al. Dynamic Reorganization and Correlation among Lipid Raft Components. J Am Chem Soc. 2016; 138(31): 9996–10001.
  48. Schwarzer R, Levental I, Gramatica A, et al. The cholesterol-binding motif of the HIV-1 glycoprotein gp41 regulates lateral sorting and oligomerization. Cell Microbiol. 2014; 16(10): 1565–1581.
  49. Tulodziecka K, Diaz-Rohrer BB, Farley MM, et al. Remodeling of the postsynaptic plasma membrane during neural development. Mol Biol Cell. 2016; 27(22): 3480–3489.
  50. Contreras FX, Ernst AM, Haberkant P, et al. Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature. 2012; 481(7382): 525–529.
  51. Dalton G, An SW, Al-Juboori SI, et al. Soluble klotho binds monosialoganglioside to regulate membrane microdomains and growth factor signaling. Proc Natl Acad Sci U S A. 2017; 114(4): 752–757.
  52. Pitre A, Ge Y, Lin W, et al. An unexpected protein interaction promotes drug resistance in leukemia. Nat Commun. 2017; 8(1): 1547.
  53. Killian JA, von Heijne G. How proteins adapt to a membrane-water interface. Trends Biochem Sci. 2000; 25(9): 429–434.
  54. Köster DV, Mayor S. Cortical actin and the plasma membrane: inextricably intertwined. Curr Opin Cell Biol. 2016; 38: 81–89.
  55. Marguet D, Lenne PF, Rigneault H, et al. Dynamics in the plasma membrane: how to combine fluidity and order. EMBO J. 2006; 25(15): 3446–3457.
  56. Honigmann A, Sadeghi S, Keller J, et al. A lipid bound actin meshwork organizes liquid phase separation in model membranes. Elife. 2014; 3: e01671.
  57. Ehrig J, Petrov EP, Schwille P. Near-critical fluctuations and cytoskeleton-assisted phase separation lead to subdiffusion in cell membranes. Biophys J. 2011; 100(1): 80–89.
  58. Levental I, Grzybek M, Simons K. Raft domains of variable properties and compositions in plasma membrane vesicles. Proc Natl Acad Sci U S A. 2011; 108(28): 11411–11416.
  59. Baumgart T, Hammond AT, Sengupta P, et al. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc Natl Acad Sci U S A. 2007; 104(9): 3165–3170.
  60. Sezgin E, Kaiser HJ, Baumgart T, et al. Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat Protoc. 2012; 7(6): 1042–1051.
  61. Biernatowska A, Podkalicka J, Majkowski M, et al. The role of MPP1/p55 and its palmitoylation in resting state raft organization in HEL cells. Biochim Biophys Acta. 2013; 1833(8): 1876–1884.
  62. Dimitratos SD, Woods DF, Stathakis DG, et al. Signaling pathways are focused at specialized regions of the plasma membrane by scaffolding proteins of the MAGUK family. Bioessays. 1999; 21(11): 912–921, doi: 10.1002/(SICI)1521-1878(199911)21:11<912::AID-BIES3>3.0.CO;2-Z.
  63. Anderson JM. Cell signalling: MAGUK magic. Curr Biol. 1996; 6(4): 382–384.
  64. Ruff P, Speicher DW, Husain-Chishti A. Molecular identification of a major palmitoylated erythrocyte membrane protein containing the src homology 3 motif. Proc Natl Acad Sci U S A. 1991; 88(15): 6595–6599.
  65. Seo PS, Quinn BJ, Khan AA, et al. Identification of erythrocyte p55/MPP1 as a binding partner of NF2 tumor suppressor protein/Merlin. Exp Biol Med (Maywood). 2009; 234(3): 255–262.
  66. Marfatia SM, Morais-Cabral JH, Kim AC, et al. The PDZ domain of human erythrocyte p55 mediates its binding to the cytoplasmic carboxyl terminus of glycophorin C. Analysis of the binding interface by in vitro mutagenesis. J Biol Chem. 1997; 272(39): 24191–24197.
  67. Hemming NJ, Anstee DJ, Staricoff MA, et al. Identification of the membrane attachment sites for protein 4.1 in the human erythrocyte. J Biol Chem. 1995; 270(10): 5360–5366.
  68. Podkalicka J, Biernatowska A, Majkowski M, et al. MPP1 as a Factor Regulating Phase Separation in Giant Plasma Membrane-Derived Vesicles. Biophys J. 2015; 108(9): 2201–2211.
  69. Levental I, Lingwood D, Grzybek M, et al. Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Natl Acad Sci U S A. 2010; 107(51): 22050–22054.
  70. Podkalicka J, Biernatowska A, Olszewska P, et al. The microdomain-organizing protein MPP1 is required for insulin-stimulated activation of H-Ras. Oncotarget. 2018; 9(26): 18410–18421.
  71. Chishti AH. Function of p55 and its nonerythroid homologues. Curr Opin Hematol. 1998; 5(2): 116–121.
  72. Marfatia SM, Lue RA, Branton D, et al. In vitro binding studies suggest a membrane-associated complex between erythroid p55, protein 4.1, and glycophorin C. J Biol Chem. 1994; 269(12): 8631–8634.
  73. Diakowski W, Grzybek M, Sikorski AF. Protein 4.1, a component of the erythrocyte membrane skeleton and its related homologue proteins forming the protein 4.1/FERM superfamily. Folia Histochem Cytobiol. 2006; 44(4): 231–248.
  74. Ward RE, Schweizer L, Lamb RS, et al. The protein 4.1, ezrin, radixin, moesin (FERM) domain of Drosophila Coracle, a cytoplasmic component of the septate junction, provides functions essential for embryonic development and imaginal cell proliferation. Genetics. 2001; 159(1): 219–228.
  75. Biernatowska A, Augoff K, Podkalicka J, et al. MPP1 directly interacts with flotillins in erythrocyte membrane - Possible mechanism of raft domain formation. Biochim Biophys Acta Biomembr. 2017; 1859(11): 2203–2212.
  76. Lang DM, Lommel S, Jung M, et al. Identification of reggie-1 and reggie-2 as plasmamembrane-associated proteins which cocluster with activated GPI-anchored cell adhesion molecules in non-caveolar micropatches in neurons. J Neurobiol. 1998; 37(4): 502–523.
  77. Neumann-Giesen C, Fernow I, Amaddii M, et al. Role of EGF-induced tyrosine phosphorylation of reggie-1/flotillin-2 in cell spreading and signaling to the actin cytoskeleton. J Cell Sci. 2007; 120(Pt 3): 395–406.
  78. Amaddii M, Meister M, Banning A, et al. Flotillin-1/reggie-2 protein plays dual role in activation of receptor-tyrosine kinase/mitogen-activated protein kinase signaling. J Biol Chem. 2012; 287(10): 7265–7278.
  79. Ludwig A, Otto GP, Riento K, et al. Flotillin microdomains interact with the cortical cytoskeleton to control uropod formation and neutrophil recruitment. J Cell Biol. 2010; 191(4): 771–781.
  80. Nakamura H, Sudo T, Tsuiki H, et al. Identification of a novel human homolog of the Drosophila dlg, P-dlg, specifically expressed in the gland tissues and interacting with p55. FEBS Lett. 1998; 433(1-2): 63–67.
  81. Mburu P, Kikkawa Y, Townsend S, et al. Whirlin complexes with p55 at the stereocilia tip during hair cell development. Proc Natl Acad Sci U S A. 2006; 103(29): 10973–10978.
  82. Quinn BJ, Welch EJ, Kim AC, et al. Erythrocyte scaffolding protein p55/MPP1 functions as an essential regulator of neutrophil polarity. Proc Natl Acad Sci U S A. 2009; 106(47): 19842–19847.
  83. Evans DG. Neurofibromatosis type 2 (NF2): a clinical and molecular review. Orphanet J Rare Dis. 2009; 4: 16.
  84. Listowski MA, Leluk J, Kraszewski S, et al. Cholesterol Interaction with the MAGUK Protein Family Member, MPP1, via CRAC and CRAC-Like Motifs: An In Silico Docking Analysis. PLoS One. 2015; 10(7): e0133141.
  85. Elderdfi M, Zegarlińska J, Jones W, et al. MPP1 interacts with DOPC/SM/Cholesterol in an artificial membrane system using Langmuir-Blodgett monolayer. Gen Physiol Biophys. 2017; 36(4): 443–454.
  86. Elderdfi M, Sikorski AF. Interaction of membrane palmitoylated protein-1 with model lipid membranes. Gen Physiol Biophys. 2018; 37(6): 603–617.
  87. Sharma P, Varma R, Sarasij RC, et al. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell. 2004; 116(4): 577–589.
  88. Mayor S, Rao M. Rafts: scale-dependent, active lipid organization at the cell surface. Traffic. 2004; 5(4): 231–240.
  89. Fujita M, Kinoshita T. Structural remodeling of GPI anchors during biosynthesis and after attachment to proteins. FEBS Lett. 2010; 584(9): 1670–1677.
  90. Eggeling C, Ringemann C, Medda R, et al. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature. 2009; 457(7233): 1159–1162.
  91. Navarro-Lérida I, Sánchez-Perales S, Calvo M, et al. A palmitoylation switch mechanism regulates Rac1 function and membrane organization. EMBO J. 2012; 31(3): 534–551.

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

By "Via Medica sp. z o.o." sp.k., ul. Świętokrzyska 73, 80–180 Gdańsk

tel.:+48 58 320 94 94, faks:+48 58 320 94 60, e-mail:  viamedica@viamedica.pl