Skip to main content
  • 397 Accesses

This chapter considers existing knowledge regarding the molecular basis of the mechanisms of bending of cell membranes, and then attempts to relate this knowledge to the possible pathophysiology underlying the neuroacanthocytosis syndromes. Curvature of animal cell membranes can be induced by a series of different mechanisms: by insertion or deletion of phospholipid from inner or outer leaflet; by contraction or expansion of the underlying cytoskeleton; by binding of soluble, typically cytoplasmic, proteins to either the lipid bilayer directly or to adaptor integral proteins; or (theoretically) by change in conformation of integral membrane proteins. Any of these, alone or in combination, could be active in chorea-acanthocytosis/McLeod syndrome. Striking electron micrographs suggest that there is a degree of cytoskeletal disorganisation in both of these conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allan D, Michell RH (1975) Accumulation of 1, 2-diacylglycerol in the plasma membrane may lead to echinocyte transformation of erythrocytes. Nature 258:348–349.

    Article  PubMed  CAS  Google Scholar 

  2. Allan D, Thomas P, Michell RH (1978) Rapid transbilayer diffusion of 1, 2-diacylglycerol and its relevance to control of membrane curvature. Nature 276:289–290.

    Article  PubMed  CAS  Google Scholar 

  3. Allan D, Walkin C (1988) Endovesiculation of human erythrocytes exposed to sphingomyelinase C: a possible explanation for the enzyme-resistant pool of sphingomyelin. Biochim Biophys Acta 938:403–410.

    Article  PubMed  CAS  Google Scholar 

  4. 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 45:5725–5732.

    Article  PubMed  CAS  Google Scholar 

  5. Backman L (1986) Shape control in the human red cell. J Cell Sci 80:281–298.

    PubMed  CAS  Google Scholar 

  6. Behnia R, Munro S (2005) Organelle identity and the signposts for membrane traffic. Nature 438:597–604.

    Article  PubMed  CAS  Google Scholar 

  7. Bhattacharyya AK, Connor WE (1974) Beta-sitosterolemia and xanthomatosis. A newly described lipid storage disease in two sisters. J Clin Invest 53:1033–1043.

    Article  PubMed  CAS  Google Scholar 

  8. Brickner JH, Fuller RS (1997) SOI1 encodes a novel, conserved protein that promotes TGN-endosomal cycling of Kex2p and other membrane proteins by modulating the function of two TGN localization signals. J Cell Biol 139:23–36.

    Article  PubMed  CAS  Google Scholar 

  9. Brooks CC, Scherer PE, Cleveland K, Whittemore JL, Lodish HF, Cheatham B (2000) Pantophysin is a phosphoprotein component of adipocyte transport vesicles and associates with GLUT4-containing vesicles. J Biol Chem 275:2029–2036.

    Article  PubMed  CAS  Google Scholar 

  10. Bruce LJ, Robinson H, Guizouarn H, Harrison P, King M-J, Goede JS, Coles SE, Gore DM, Lutz H, Ficarella R, Layton M, Iolascon A, Ellory JC, Stewart GW (2005) Monovalent cation leaks in human red cells caused by single amino-acid substitutions in the transport domain of the band 3 chloride-bicarbonate exchanger, AE1. Nat Genet 37:1258–1263.

    Article  PubMed  CAS  Google Scholar 

  11. Carella M, Stewart GW, Ajetunmobi JF, Perrotta S, Grootenboer S, Tchernia G, Delaunay J, Totaro A, Zelante L, Gasparini P, Iolascon, A (1998) Genomewide search for dehydrated hereditary stomatocytosis (hereditary xerocytosis): mapping of locus to chromosome 16 (q23-qter). Am J Hum Genet 63:810–816.

    Article  PubMed  CAS  Google Scholar 

  12. Caroni P (2001) Actin cytoskeleton regulation through modulation of PI(4, 5) P(2) rafts. EMBO J 20:4332–4336.

    Article  PubMed  CAS  Google Scholar 

  13. Charest PG, Firtel RA (2007) Big roles for small GTPases in the control of directed cell movement. Biochem J 401:377–390.

    Article  PubMed  CAS  Google Scholar 

  14. Clark MR, Shohet SB, Gottfried EL (1993) Hereditary hemolytic disease with increased red blood cell phosphatidylcholine and dehydration: one, two, or many disorders? Am J Hematol 42:25–30.

    Article  PubMed  CAS  Google Scholar 

  15. Danek A, Rubio JP, Rampoldi L, Ho M, Dobson-Stone C, Tison F, Symmans WA, Oechsner M, Kalckreuth W, Watt JM, Corbett AJ, Hamdalla HH, Marshall AG, Sutton I, Dotti MT, Malandrini A, Walker RH, Daniels G, Monaco AP (2001) McLeod neuroacanthocytosis: genotype and phenotype. Ann Neurol 50:755–764.

    Article  PubMed  CAS  Google Scholar 

  16. Davis J, Bennett V (1985) Human erythrocyte clathrin and clathrin-uncoating protein. J Biol Chem 260:14850–14856.

    PubMed  CAS  Google Scholar 

  17. Dawson JC, Legg JA, Machesky LM (2006) Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol 16:493–498.

    Article  PubMed  CAS  Google Scholar 

  18. Devaux PF, Lopez-Montero I, Bryde S (2006) Proteins involved in lipid translocation in eukaryotic cells. Chem Phys Lipid 141:119–132.

    Article  CAS  Google Scholar 

  19. Downes CP, Michell RH (1982) The control by Ca2+ of the polyphosphoinositide phosphodiesterase and the Ca2+-pump ATPase in human erythrocytes. Biochem J 202:53–58.

    PubMed  CAS  Google Scholar 

  20. Dupree P, Parton RG, Raposo G, Kurzchalia TV, Simons K (1993) Caveolae and sorting in the trans-Golgi network of epithelial cells. EMBO J 12:1597–1605.

    PubMed  CAS  Google Scholar 

  21. Engelman DM (2005) Membranes are more mosaic than fluid. Nature 438:578–580.

    Article  PubMed  CAS  Google Scholar 

  22. Fiedler K, Kobayashi T, Kurzchalia TV, Simons K (1993) Glycosphingolipid-enriched, detergent-insoluble complexes in protein sorting in epithelial cells. Biochemistry 32:6365–6373.

    Article  PubMed  CAS  Google Scholar 

  23. Field CM, Alberts BM (1995) Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol 131:165–178.

    Article  PubMed  CAS  Google Scholar 

  24. Fricke B, Jarvis HG, Reid CD, Aguilar-Martinez P, Robert A, Quittet P, Chetty M, Pizzey A, Cynober T, Lande WF, Mentzer WC, During M, Winter S, Delaunay J, Stewart GW (2004) Four new cases of stomatin-deficient hereditary stomatocytosis syndrome: association of the stomatin-deficient cryohydrocytosis variant with neurological dysfunction. Br J Haematol 125:796–803.

    Article  PubMed  CAS  Google Scholar 

  25. Gallop JL, Jao CC, Kent HM, Butler PJ, Evans PR, Langen R, McMahon HT (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J 25:2898–2910.

    Article  PubMed  CAS  Google Scholar 

  26. Gascard P, Pawelczyk T, Lowenstein JM, Cohen CM (1993) The role of inositol phospholipids in the association of band 4.1 with the human erythrocyte membrane. Eur J Biochem 211:671–681.

    Article  PubMed  CAS  Google Scholar 

  27. Grassme H, Gulbins E, Brenner B, Ferlinz K, Sandhoff K, Harzer K, Lang F, Meyer TF (1997) Acidic sphingomyelinase mediates entry of N. gonorrhoeae into nonphagocytic cells. Cell 91:605–615.

    Article  PubMed  CAS  Google Scholar 

  28. Greco F, Ciana A, Pietra D, Balduini C, Minetti G, Torti M (2006) Rap2, but not Rap1 GTPase is expressed in human red blood cells and is involved in vesiculation. Biochim Biophys Acta 28:28.

    Google Scholar 

  29. Haglund K, Ivankovic-Dikic I, Shimokawa N, Kruh GD, Dikic I (2004) Recruitment of Pyk2 and Cbl to lipid rafts mediates signals important for actin reorganization in growing neuritis. J Cell Sci 117:2557–2568.

    Article  PubMed  CAS  Google Scholar 

  30. Hardie RJ, Pullon HW, Harding AE, Owen JS, Pires M, Daniels GL, Imai Y, Misra VP, King RH, Jacobs JM et al. (1991) Neuroacanthocytosis. A clinical, haematological and pathological study of 19 cases. Brain 114:13–49.

    PubMed  Google Scholar 

  31. Ho M, Chelly J, Carter N, Danek A, Crocker P, Monaco AP (1994) Isolation of the gene for McLeod syndrome that encodes a novel membrane transport protein. Cell 77:869–880.

    Article  PubMed  CAS  Google Scholar 

  32. Holopainen JM, Angelova MI, Kinnunen PK (2000) Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys J 78:830–838.

    Article  PubMed  CAS  Google Scholar 

  33. Jaffe ER, Gottfried EL (1968) Hereditary nonspherocytic hemolytic disease associated with an altered phospholipid composition of the erythrocytes. J Clin Invest 47:1375–1388.

    PubMed  CAS  Google Scholar 

  34. Janmey PA, Kinnunen PK (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16:538–546.

    Article  PubMed  CAS  Google Scholar 

  35. Kalfa TA, Pushkaran S, Mohandas N, Hartwig JH, Fowler VM, Johnson JF, Joiner CH, Williams DA, Zheng Y (2006) Rac GTPases regulate the morphology and deformability of the erythrocyte cytoskeleton. Blood 1:1.

    Google Scholar 

  36. Kwik J, Boyle S, Fooksman D, Margolis L, Sheetz MP, Edidin M (2003) Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4, 5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci U S A 100:13964–13969.

    Article  PubMed  CAS  Google Scholar 

  37. Mangeat P, Roy C, Martin M (1999) ERM protein in cell adhesion and membrane dynamics. Trends Cell Biol 9:187–192.

    Article  PubMed  CAS  Google Scholar 

  38. Maxfield FR, Tabas I (2005) Role of cholesterol and lipid organization in disease. Nature 438:612–621.

    Article  PubMed  CAS  Google Scholar 

  39. McLaughlin S, Wang J, Gambhir A, Murray D (2002) PIP(2) and proteins: interactions, organization, and information flow. Annu Rev Biophys Biomol Struct 31:151–175.

    Article  PubMed  CAS  Google Scholar 

  40. McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodeling. Nature 438:590–596.

    Article  PubMed  CAS  Google Scholar 

  41. McNiven MA (2006) Big gulps: specialized membrane domains for rapid receptor-mediated endocytosis. Trends Cell Biol 16:487–492.

    Article  PubMed  CAS  Google Scholar 

  42. Michell RH, Heath VL, Lemmon MA, Dove SK (2006) Phosphatidylinositol 3, 5-bisphosphate: metabolism and cellular functions. Trends Biochem Sci 31:52–63.

    Article  PubMed  CAS  Google Scholar 

  43. Mohandas N, An X (2006) New insights into function of red cell membrane proteins and their interaction with spectrin-based membrane skeleton. Transfus Clin Biol 13:29–30.

    Article  PubMed  CAS  Google Scholar 

  44. Murphy SC, Samuel BU, Harrison T, Speicher KD, Speicher DW, Reid ME, Prohaska R, Low PS, Tanner MJ, Mohandas N, Haldar K (2004) Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection. Blood 103:1920–1928.

    Article  PubMed  CAS  Google Scholar 

  45. Otto JJ, Kane RE, Bryan J (1979) Formation of filopodia in coelomocytes: localization of fascin, a 58, 000 dalton actin cross-linking protein. Cell 17:285–293.

    Article  PubMed  CAS  Google Scholar 

  46. Pasini EM, Kirkegaard M, Mortensen P, Lutz HU, Thomas AW, Mann M (2006) In-depth analysis of the membrane and cytosolic proteome of red blood cells. Blood 108:791–801.

    Article  PubMed  CAS  Google Scholar 

  47. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–499.

    Article  PubMed  CAS  Google Scholar 

  48. Rampoldi L, Dobson-Stone C, Rubio JP, Danek A, Chalmers RM, Wood NW, Verellen C, Ferrer X, Malandrini A, Fabrizi GM, Brown R, Vance J, Pericak-Vance M, Rudolf G, Carre S, Alonso E, Manfredi M, Nemeth AH, Monaco AP (2001) A conserved sorting-associated protein is mutant in chorea-acanthocytosis. Nat Genet 28:119–120.

    Article  PubMed  CAS  Google Scholar 

  49. Rees D, Iolascon A, Carella M, O’Marcaigh A, Kendra J, Jowitt S, Wales J, Vora A, Nicolaou A, Fisher J, Mann A, Chetty MC, Clayton PT, Gasparini P, Stewart GW (2005) Stomatocytic haemolysis and macrothrombocytopenia (Mediterranean stomatocytosis/macrothrombocytopenia) is the haematological presentation of phytosterolaemia. Br J Haematol 130:297–309.

    Article  PubMed  CAS  Google Scholar 

  50. Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522–529.

    Article  PubMed  CAS  Google Scholar 

  51. Robinson JS, Klionsky DJ, Banta LM, Emr SD (1988) Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol 8:4936–4948.

    PubMed  CAS  Google Scholar 

  52. Rodgers W, Glaser M (1991) Characterization of lipid domains in erythrocyte membranes. Proc Natl Acad Sci U S A 88:1364–1368.

    Article  PubMed  CAS  Google Scholar 

  53. Rodgers W, Glaser M (1993) Distribution of proteins and lipids in the erythrocyte membrane. Biochemistry 32:12592–12598.

    Article  Google Scholar 

  54. Rothberg K, Ying Y, Kolhouse J, Kamen B, Anderson R (1990) The glycosphospholipid linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J Cell Biol 110:637–649.

    Article  PubMed  CAS  Google Scholar 

  55. Rothberg K, Ying Y-S, Kamen B, Anderson R (1990) Cholesterol controls the clustering of the glycolipid-anchored membrane receptor for 5-methyltetrahydrofolate. J Cell Biol 111:2931–2938.

    Article  PubMed  CAS  Google Scholar 

  56. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68:673–682.

    Article  PubMed  CAS  Google Scholar 

  57. Schmid EM, Ford MG, Burtey A, Praefcke GJ, Peak-Chew SY, Mills IG, Benmerah A, McMahon HT (2006) Role of the AP2 beta-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol 4:e262.

    Article  PubMed  CAS  Google Scholar 

  58. Schmid S (1999) Dynamin. In: Kreis T, Vale R (eds) Guidebook to cytoskeletal and motor proteins. Sambrook and Tooze, Oxford, pp 524–527.

    Google Scholar 

  59. Schroeder F, Nemecz G, Wood WG, Joiner C, Morrot G, Ayraut-Jarrier M, Devaux PF (1991) Transmembrane distribution of sterol in the human erythrocyte. Biochim Biophys Acta 1066:183–192.

    Article  PubMed  CAS  Google Scholar 

  60. Seroussi E, Pan HQ, Kedra D, Roe BA, Dumanski JP (1998) Characterization of the human NIPSNAP1 gene from 22q12: a member of a novel gene family. Gene 212:13–20.

    Article  PubMed  CAS  Google Scholar 

  61. Sheetz M, Singer SJ (1974) Biological membranes as bilayer couples: a molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci U S A 71:4457.

    Article  PubMed  CAS  Google Scholar 

  62. Stanfield GM, Horvitz HR (2000) The ced-8 gene controls the timing of programmed cell deaths in C. elegans. Mol Cell 5:423–433.

    Google Scholar 

  63. Steck TL, Ye J, Lange Y (2002) Probing red cell membrane cholesterol movement with cyclodextrin. Biophys J 83:2118–2125.

    Article  PubMed  CAS  Google Scholar 

  64. Svetina S, Zeks B (1983) Bilayer couple hypothesis of red cell shape transformations and osmotic hemolysis. Biomed Biochim Acta 42:S86–S90.

    PubMed  CAS  Google Scholar 

  65. Terada N, Fujii Y, Ueda H, Kato Y, Baba T, Hayashi R, Ohno S (1999) Ultrastructural changes of erythrocyte membrane skeletons in chorea-acanthocytosis and McLeod syndrome revealed by the quick-freezing and deep-etching method. Acta Haematol 101:25–31.

    Article  PubMed  CAS  Google Scholar 

  66. Velayos-Baeza A, Vettori A, Copley RR, Dobson-Stone C, Monaco AP (2004) Analysis of the human VPS13 gene family. Genomics 84:536–549.

    Article  PubMed  CAS  Google Scholar 

  67. Walensky LD, Narla M, Lux SE (2003) Disorders of the red blood cell membrane. In: Handin R, Lux S, Stossel T (eds) Blood: principles and practice of Hematology. Lippincott, Philadelphia, pp 1709–1858.

    Google Scholar 

  68. Weimer RM, Richmond JE (2005) Synaptic vesicle docking: a putative role for the Munc18/Sec1 protein family. Curr Top Dev Biol 65:83–113.

    Article  PubMed  CAS  Google Scholar 

  69. Wong P (2004) A basis of the acanthocytosis in inherited and acquired disorders. Med Hypotheses 62:966–969.

    Article  PubMed  CAS  Google Scholar 

  70. Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7:9–19.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Stewart, G.W., Wilmore, S.M.S., Ohno, S., Terada, N. (2008). Questions of Cell Shape. In: Walker, R.H., Saiki, S., Danek, A. (eds) Neuroacanthocytosis Syndromes II. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-71693-8_9

Download citation

Publish with us

Policies and ethics