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Status of Membrane Asymmetry in Erythrocytes: Role of Spectrin

  • Sauvik Sarkar
  • Dipayan Bose
  • Rajendra P. Giri
  • Mrinmay K. Mukhopadhyay
  • Abhijit ChakrabartiEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1112)

Abstract

Spectrin-based proteinaceous membrane skeletal network has been found to be implicated in membrane disorders like hereditary spherocytosis (HS). HS greatly affects eryptosis via loss of membrane asymmetry which is seen to be the case in haemoglobin disorders like thalassemia and sickle cell disease as well. The biological implications of the status of membrane asymmetry are strongly correlated to spectrin interactions with aminophospholipids, e.g. PE and PS. Fluorescence and X-ray reflectivity (XRR) measurements of spectrin interactions with small unilamellar vesicles (SUVs) and cushioned bilayers of phospholipids, respectively, were studied. Both the XRR and fluorescence measurements led to the characterization of spectrin orientation on the surface of lipid bilayer of phosphatidylcholine (PC) and PC/aminophospholipid mixed membrane systems showing formation of a uniform layer of spectrin on top of the mixed phospholipid bilayer. Fluorescence studies show that spectrin interacts with PC and phosphatidylethanolamine (PE)/phosphatidylserine (PS) membranes with binding dissociation constants (Kd) in the nanomolar range indicating the role of spectrin in the maintenance of the overall membrane asymmetry of erythrocytes.

Keywords

Spectrin Membrane asymmetry Lipid-protein interaction Membrane skeleton 

Abbreviations

DM

Dimyristoyl

HE

Hereditary elliptocytosis

HS

Hereditary spherocytosis

PC

Phosphatidylcholine

PE

Phosphatidylethanolamine

PG

Phosphoglycerate

PI

Phosphatidylinositol

PS

Phosphatidylserine

SUV

Small unilamellar vesicles

References

  1. Alessandrini A, Facci P (2011) Unraveling lipid/protein interaction in model lipid bilayers by atomic force microscopy. J Mol Recognit 24:387–396CrossRefGoogle Scholar
  2. An XL, Takakuwa Y, Manno S, Han BG, Gascard P, Mohandas N (2001) Structural and functional characterization of protein 4.1R-phosphatidylserine interaction: potential role in 4.1R sorting within cells. J Biol Chem 276:35778–35785CrossRefGoogle Scholar
  3. An X, Zhang X, Debnath G, Baines AJ, Mohandas N (2006) Phosphatidylinositol-4,5-biphosphate (PIP2) differentially regulates the interaction of human erythrocyte protein 4.1 (4.1R) with membrane proteins. Biochemistry 45:5725–5732CrossRefGoogle Scholar
  4. Basu A, Chakrabarti A (2015) Defects in erythrocyte membrane skeletal architecture. Adv Exp Med Biol 842:41–59CrossRefGoogle Scholar
  5. Basu JK, Sanyal MK (2002) Ordering and growth of Langmuir–Blodgett films: x-ray scattering studies. Phys Rep 363:1–84CrossRefGoogle Scholar
  6. Basu S, Banerjee D, Chandra S, Chakrabarti A (2010) Eryptosis in hereditary spherocytosis and thalassemia: role of glycoconjugates. Glycoconj J 27:717–722CrossRefGoogle Scholar
  7. Biernatowska A, Podkalicka J, Majkowski M, Hryniewicz-Jankowska A, Augoff K, Kozak K, Korzeniewski J, Sikorski AF (2013) The role of MPP1/p55 and its palmitoylation in resting state raft organization in HEL cells. Biochim Biophys Acta 1833:1876–1884CrossRefGoogle Scholar
  8. Chakrabarti A, Datta P, Bhattacharya D, Basu S, Saha S (2008) Oxidative crosslinking, spectrin and membrane interactions of hemoglobin mixtures in HbEbeta-thalassemia. Hematology 13:361–368CrossRefGoogle Scholar
  9. Datta P, Basu S, Chakravarty SB, Chakravarty A, Banerjee D, Chandra S, Chakrabarti A (2006) Enhanced oxidative cross-linking of hemoglobin E with spectrin and loss of erythrocyte membrane asymmetry in hemoglobin Ebeta-thalassemia. Blood Cells Mol Dis 37:77–81CrossRefGoogle Scholar
  10. DeWolf C, McCauley P, Sikorski AF, Winlove CP, Bailey AI, Kahana E, Pinder JC, Gratzer WB (1997) Interaction of dystrophin fragments with model membranes. Biophys J 72:2599–2604CrossRefGoogle Scholar
  11. Diakowski W, Szopa J, Sikorski AF (2003) Occurrence of lipid receptors inferred from brain and erythrocyte spectrins binding NaOH-extracted and protease-treated neuronal and erythrocyte membranes. Biochim Biophys Acta 1611:115–122CrossRefGoogle Scholar
  12. Edidin M (2006) Switching sides: the actin/membrane lipid connection. Biophys J 91:3963CrossRefGoogle Scholar
  13. El-khouri RJ, Bricarello DA, Watkins EB, Kim CY, Miller CE, Patten TE, Parikh AN, Kuhl TL (2011) pH responsive polymer cushions for probing membrane environment interactions. Nano Lett 11:2169–2172CrossRefGoogle Scholar
  14. Fadeel B, Xue D (2009) The ins and outs of phospholipid asymmetry in the plasma membrane: roles in health and disease. Crit Rev Biochem Mol Biol 44(5):264–277CrossRefGoogle Scholar
  15. Gallagher PG (2005) Red cell membrane disorders. Hematology Am Soc Hematol Educ Program 2005:13–18CrossRefGoogle Scholar
  16. Gauthier E, Guo X, Mohandas N, An X (2011) Phosphorylation-dependent perturbations of the 4.1R-associated multiprotein complex of the erythrocyte membrane. Biochemistry 50:4561–4567CrossRefGoogle Scholar
  17. Gicquaud C (1993) Actin conformation is drastically altered by direct interaction with membrane lipids: a differential scanning calorimetry study. Biochemistry 32:11873–11877CrossRefGoogle Scholar
  18. Gicquaud C, Wong P (1994) Mechanism of interaction between actin and membrane lipids: a pressure-tuning infrared spectroscopy study. Biochem J 303. (Pt 3:769–774CrossRefGoogle Scholar
  19. Giri RP, Chakrabarti A, Mukhopadhyay MK (2017) Cholesterol-induced structural changes in saturated phospholipid model membranes revealed through x-ray scattering technique. J Phys Chem B 121:4081–4090CrossRefGoogle Scholar
  20. Grzybek M, Chorzalska A, Bok E, Hryniewicz-Jankowska A, Czogalla A, Diakowski W, Sikorski AF (2006) Spectrin-phospholipid interactions. Existence of multiple kinds of binding sites? Chem Phys Lipids 141:133–141CrossRefGoogle Scholar
  21. Hyvonen M, Macias MJ, Nilges M, Oschkinat H, Saraste M, Wilmanns M (1995) Structure of the binding site for inositol phosphates in a PH domain. EMBO J 14:4676–4685CrossRefGoogle Scholar
  22. Juliano RL, Kimelberg HK, Papahadjopoulos D (1971) Synergistic effects of a membrane protein (spectrin) and Ca 2+ on the Na + permeability of phospholipid vesicles. Biochim Biophys Acta 241:894–905CrossRefGoogle Scholar
  23. Kennedy SP, Warren SL, Forget BG, Morrow JS (1991) Ankyrin binds to the 15th repetitive unit of erythroid and nonerythroid beta-spectrin. J Cell Biol 115:267–277CrossRefGoogle Scholar
  24. Lach A, Grzybek M, Heger E, Korycka J, Wolny M, Kubiak J, Kolondra A, Boguslawska DM, Augoff K, Majkowski M, Podkalicka J, Kaczor J, Stefanko A, Kuliczkowski K, Sikorski AF (2012) Palmitoylation of MPP1 (membrane-palmitoylated protein 1)/p55 is crucial for lateral membrane organization in erythroid cells. J Biol Chem 287:18974–18984CrossRefGoogle Scholar
  25. Listowski MA, Leluk J, Kraszewski S, Sikorski AF (2015) Cholesterol interaction with the MAGUK protein family member, MPP1, via CRAC and CRAC-like motifs: an in silico docking analysis. PLoS One 10:e0133141CrossRefGoogle Scholar
  26. Liu AP, Fletcher DA (2006) Actin polymerization serves as a membrane domain switch in model lipid bilayers. Biophys J 91:4064–4070CrossRefGoogle Scholar
  27. Machnicka B, Czogalla A, Hryniewicz-Jankowska A, Boguslawska DM, Grochowalska R, Heger E, Sikorski AF (2014) Spectrins: a structural platform for stabilization and activation of membrane channels, receptors and transporters. Biochim Biophys Acta 1838:620–634CrossRefGoogle Scholar
  28. Mitra M, Patra M, Chakrabarti A (2015) Fluorescence study of the effect of cholesterol on spectrin-aminophospholipid interactions. Eur Biophys J 44:635–645CrossRefGoogle Scholar
  29. Mombers C, de Gier J, Demel RA, van Deenen LL (1980) Spectrin-phospholipid interaction. A monolayer study. Biochim Biophys Acta 603:52–62CrossRefGoogle Scholar
  30. Nebl T, Pestonjamasp KN, Leszyk JD, Crowley JL, Oh SW, Luna EJ (2002) Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J Biol Chem 277:43399–43409CrossRefGoogle Scholar
  31. Parratt LG (1954) Surface studies of solids by total reflection of x-rays. Phys Rev 95:359–369CrossRefGoogle Scholar
  32. Podkalicka J, Biernatowska A, Majkowski M, Grzybek M, Sikorski AF (2015) MPP1 as a factor regulating phase separation in Giant plasma membrane-derived vesicles. Biophys J 108:2201–2211CrossRefGoogle Scholar
  33. Ray S, Chakrabarti A (2004) Membrane interaction of erythroid spectrin: surface-density-dependent high-affinity binding to phosphatidylethanolamine. Mol Membr Biol 21:93–100CrossRefGoogle Scholar
  34. Salomao M, Zhang X, Yang Y, Lee S, Hartwig JH, Chasis JA, Mohandas N, An X (2008) Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. Proc Natl Acad Sci USA 105:8026–8031CrossRefGoogle Scholar
  35. Saraste M, Hyvonen M (1995) Pleckstrin homology domains: a fact file. Curr Opin Struct Biol 5:403–408CrossRefGoogle Scholar
  36. Sikorski AF, Hanus-Lorenz B, Jezierski A, Dluzewski AR (2000) Interaction of membrane skeletal proteins with membrane lipid domain. Acta Biochim Pol 47:565–578PubMedGoogle Scholar
  37. Sweet C, Zull JE (1970) Interaction of the erythrocyte--membrane protein, spectrin, with model membrane systems. Biochem Biophys Res Commun 41:135–141CrossRefGoogle Scholar
  38. Takenawa T, Itoh T (2001) Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim Biophys Acta 1533:190–206CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Sauvik Sarkar
    • 1
  • Dipayan Bose
    • 1
  • Rajendra P. Giri
    • 2
  • Mrinmay K. Mukhopadhyay
    • 2
  • Abhijit Chakrabarti
    • 1
    Email author
  1. 1.Crystallography & Molecular Biology DivisionSaha Institute of Nuclear Physics, HBNIKolkataIndia
  2. 2.Surface Physics & Material Science DivisionSaha Institute of Nuclear Physics, HBNIKolkataIndia

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