Ligation of complement receptor 1 increases erythrocyte membrane deformability

Blood

Volumn 116, Issue 26, 2010, Pages 6063-6071

  Glodek, Aleksandra M ^a   Mirchev, Rossen ^a   Golan, David E ^a,b   Khoory, Joseph A ^c   Burns, Jennie M ^d   Shevkoplyas, Sergey S ^d   Nicholson Weller, Anne ^a   Ghiran, Ionita C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c Worcester Polytechnic Institute   (United States)

^d Tulane University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; COMPLEMENT COMPONENT C3B RECEPTOR; SPECTRIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ERYTHROCYTE MEMBRANE; ERYTHROCYTE SHAPE; HUMAN; HUMAN CELL; OPSONIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT;

EID: 78650649899     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-04-273904     Document Type: Article

References (54)

1. Nelson RAJ. The immune adherence phenomenon: an immunologically specfic reaction between microorganisms and erythrocytes leading to enhanced phagocytosis. Science. 1953;118(3077):733-737.
2. Fearon DT. Identification of the membrane glyco-protein that is the C3b receptor of the human erythrocyte, polymorphonuclear leukocyte, B lymphocyte and monocyte. J Exp Med. 1980;152(1):20-30.
3. Ng YC, Schifferli JA, Walport MJ. Immune complexes and erythrocyte CR1 (complement receptor type 1): effect of CR1 numbers on binding and release reactions. Clin Exp Immunol. 1988;71(3):481-485.
4. Hess C, Schifferli JA. Immune adherence revisited: novel players in an old game. News Physiol Sci. 2003;18:104-108.
5. Nelson RAJ. The immune-adherence phenomenon. A hypothetical role of erythrocytes in defense against bacteria and viruses. Proc Royal Soc Med. 1956;49:55-58.
6. Pilsczek FH, Nicholson-Weller A, Ghiran I. Phagocytosis of Salmonella montevideo by human neutrophils: immune adherence increases phagocytosis, whereas the bacterial surface determines the route of intracellular processing. J Infect Dis. 2005;192(2):200-209.
7. Ghiran I, Glodek AM, Weaver G, Klickstein LB, Nicholson-Weller A. Ligation of erythrocyte CR1 induces its clustering in complex with scaffolding protein FAP-1. Blood. 2008;112(8):3465-3473.
8. Brown FL. Regulation of protein mobility via thermal membrane undulations. Biophys J. 2003;84(2 Pt 1):842-853.
9. Manno S, Takakuwa Y, Nagao K, Mohandas N. Modulation of erythrocyte membrane mechanical function by beta-spectrin phosphorylation and dephosphorylation. J Biol Chem. 1995;270(10):5659-5665.
10. Matsuoka Y, Hughes CA, Bennett V. Adducin regulation. Definition of the calmodulin-binding domain and sites of phosphorylation by protein kinases A and C. J Biol Chem. 1996;271(41):25157-25166.
11. Manno S, Takakuwa Y, Mohandas N. Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J Biol Chem. 2005;280(9):7581-7587.
12. Changelian PS, Jack RM, Collins LA, Fearon DT. PMA induces the ligand-independent internalization of CR1 on human neutrophils. J Immunol. 1985;134(3):1851-1858.
13. Chen CH, Ghiran I, Beurskens FJ, et al. Antibody CR1-2B11 recognizes a non-polymorphic epitope of human CR1 (CD35). Clin Exp Immunol. 2007;148(3):546-554.
14. Gee KR, Brown KA, Chen WN, Bishop-Stewart J, Gray D, Johnson I. Chemical and physiological characterization of fluo-4 Ca (2+)-indicator dyes. Cell Calcium. 2000;27(2):97-106.
15. Hochmuth RM, Worthy PR, Evans EA. Red cell ex-tensional recovery and the determination of membrane viscosity. Biophys J. 1979;26(1):101-114.
16. Shevkoplyas SS, YoshidaT, Gifford SC, Bitensky MW. Direct measurement of the impact of impaired erythrocyte deformability on microvascular network perfusion in a microfluidic device. Lab Chip. 2006;6(7):914-920.
17. Wilson JG, Murphy EE, Wong WW, Klickstein LB, Weis JH, Fearon DT. Identification of a restriction fragment length polymorphism by a CR1 cDNA that correlates with the number of CR1 on erythrocytes. J Exp Med. 1986;164(1):50-59.
18. Larsen FL, Katz S, Roufogalis BD, Brooks DE. Physiological shear stresses enhance the Ca2 + permeability of human erythrocytes. Nature. 1981;294(5842):667-668.
19. Brain MC, Pihl C, Robertson L, Brown CB. Evidence for a mechanosensitive calcium influx into red cells. Blood Cells Mol Dis. 2004;32(3):349-352.
20. Suchyna TM, Johnson JH, Hamer K, et al. Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J Gen Physiol. 2000;115(5):583-598.
21. Riccio A, Medhurst AD, Mattei C, et al. mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res Mol Brain Res. 2002;109(1-2): 95-104.
22. Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP. TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol. 2005;7(2):179-185.
23. Clapham DE, Julius D, Montell C, Schultz G. International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol Rev. 2005;57(4):427-450.
24. Kwan HY, Shen B, Ma X, et al. TRPC1 associates with BK (Ca) channel to form a signal complex in vascular smooth muscle cells. Circ Res. 2009;104(5):670-678.
25. Young B. Wheater's Functional Histology: A Text and Colour Atlas (5th ed.) Edinburgh: Churchill Livingstone/Elsevier; 2006.
26. Karnchanaphanurach P, Mirchev R, Ghiran I, et al. C3b deposition on human erythrocytes induces the formation of a membrane skeleton-linked protein complex. J Clin Invest. 2009;119(4):788-801.
27. Mirchev R, Golan DE. Single-particle tracking and laser optical tweezers studies of the dynamics of individual protein molecules in membranes of intact human and mouse red cells. Blood Cells Mol Dis. 2001;27(1):143-147.
28. Bambardekar K, Dharmadhikari AK, Dharmadhikari JA, Mathur D, Sharma S. Measuring erythrocyte deformability with fluorescence, fluid forces, and optical trapping. J Biomed Opt. 2008;13(6):064021.
29. Brandao MM, Fontes A, Barjas-Castro ML, et al. Optical tweezers for measuring red blood cell elasticity: application to the study of drug response in sickle cell disease. Eur J Haematol. 2003;70(4):207-211.
30. Shevkoplyas SS, Gifford SC, Yoshida T, Bitensky MW. Prototype of an in vitro model of the micro-circulation. Microvasc Res. 2003;65(2):132-136.
31. Henon S, Lenormand G, Richert A, Gallet F. A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys J. 1999;76(2):1145-1151.
32. Li J, Dao M, Lim CT, Suresh S. Spectrin-level modeling of the cytoskeleton and optical tweezers stretching of the erythrocyte. Biophys J. 2005;88(5):3707-3719.
33. Gardos G. The function of calcium in the potassium permeability of human erythrocytes. Bio-chim Biophys Acta. 1958;30(3):653-654.
34. Mohandas N, Gallagher PG. Red cell membrane: past, present, and future. Blood. 2008;112(10):3939-3948.
35. Schifferli JA, Ng YC, Estreicher J, Walport MJ. The clearance of tetanus toxoid-anti-tetanus tox-oid immune complexes from the circulation of humans. Complement-and erythrocyte complement receptor 1-dependent mechanisms. J Immunol. 1988;140(3):899-904.
36. Halma C, Daha MR, Camps JA, Evers-Schouten JH, Pauwels EK, Van E. Deficiency of complement component C3 is associated with accelerated removal of soluble 123I-labelled aggregates of IgG from the circulation. Clin Exp Immunol. 1992;90(3):394-400.
37. de Oliveira S, Silva-Herdade AS, Saldanha C. Modulation of erythrocyte deformability by PKC activity. Clin Hemorheol Microcirc. 2008;39(1-4): 363-373.
38. Wei T, Tao M. Human erythrocyte casein kinase II: characterization and phosphorylation of membrane cytoskeletal proteins. Arch Biochem Bio-phys. 1993;307(1):206-216.
39. Rena G, Bain J, Elliott M, Cohen P. D4476, a cell-permeant inhibitor of CK1, suppresses the site-specific phosphorylation and nuclear exclusion of FOXO1a. EMBO Rep. 2004;5(1):60-65.
40. Hora R, Bridges DJ, Craig A, Sharma A. Erythro-cytic casein kinase II regulates cytoadherence of Plasmodium falciparum-infected red blood cells. J Biol Chem. 2009;284(10):6260-6269.
41. Changelian PS, Fearon DT. Tissue-specific phos-phorylation of complement receptors CR1 and CR2. J Exp Med. 1986;163(1):101-115.
42. Vaya A, Lopez JM, Contreras MT, et al. Erythro-cyte deformability in survivors of acute myocar-dial infarction measured by two different methodologies. Clin Hemorheol Microcirc. 2002;27(1):17-25.
43. Koksal C, Ercan M, Bozkurt AK. Hemorrheologi-cal variables in critical limb ischemia. Int Angiol. 2002;21(4):355-359.
44. Kalfa TA, Pushkaran S, Mohandas N, et al. Rac GTPases regulate the morphology and deform-ability of the erythrocyte cytoskeleton. Blood. 2006;108(12):3637-3645.
45. Chasis JA, Mohandas N, Shohet SB. Erythrocyte membrane rigidity induced by glycophorin A-li-gand interaction. Evidence for a ligand-induced association between glycophorin A and skeletal proteins. J Clin Invest 1985;75(6):1919-1926.
46. Johnson RM. Membrane stress increases cation permeability in red cells. BiophysJ. 1994;67(5):1876-1881.
47. Parker CJ, Soldato CM, Rosse WF. Abnormality of glycophorin-α on paroxysmal nocturnal hemoglobinuria erythrocytes. J Clin Invest 1984;73(4):1130-1143.
48. Markiewski MM, DeAngelis RA, Lambris JD. Complexity of complement activation in sepsis. J Cell Mol Med. 2008;12(6 A): 2245-2254.
49. Ohi H, Tamano M, Okada N. Low CR1 (C3b receptor) level on erythrocytes is associated with poor prognosis in hemodialysis patients. Nephron Clin Pract 2008;108(1): c23-c27.
50. An X, Debnath G, Guo X, et al. Identification and functional characterization of protein 4.1R and actin-binding sites in erythrocyte beta spectrin: regulation of the interactions by phosphatidylino-sitol-4, 5-bisphosphate. Biochemistry. 2005;44(31):10681-10688.
51. An X, Guo X, Sum H, Morrow J, Gratzer W, Mohandas N. Phosphatidylserine binding sites in erythroid spectrin: location and implications for membrane stability. Biochemistry. 2004;43(2):310-315.
52. Bain J, Plater L, Elliott M, et al. The selectivity of protein kinase inhibitors: a further update. Bio-chem J. 2007;408(3):297-315.
53. Gross SD, Anderson RA. Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. Cell Signal. 1998;10(10):699-711.
54. Usui H, Imazu M, Maeta K, Tsukamoto H, Azuma K, Takeda M. Three distinct forms of type 2A protein phosphatase in human erythrocyte cytosol. J Biol Chem. 1988;263(8):3752-3761.