Macrophage recognition of cells with elevated calcium is mediated by carbohydrate chains of CD43

Cell Structure and Function

Volumn 38, Issue 1, 2013, Pages 43-54

  Miki, Yuichi ^a   Oguri, Emiri ^a   Hirano, Kazuya ^a   Beppu, Masatoshi ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

Author keywords

CD43; Cytoskeleton; Elevated calcium; Macrophage; Nucleolin

Indexed keywords

CALCIMYCIN; CALCIUM; CD43 ANTIBODY; CHEMICAL COMPOUND; LEUKOSIALIN; NUCLEOLIN; NUCLEOLIN ANTIBODY; OLIGOSACCHARIDE; PHOSPHATIDYLSERINE; POLY N ACETYLLACTOSAMINYL; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CALCIUM CELL LEVEL; CARBOHYDRATE ANALYSIS; CELL INTERACTION; CELL SURFACE; CELL VIABILITY; CONTROLLED STUDY; DNA FRAGMENTATION; LEUKEMIA CELL LINE; MACROPHAGE FUNCTION; MOLECULAR RECOGNITION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

ANTIGENS, CD43; APOPTOSIS; CALCIMYCIN; CALCIUM; CARBOHYDRATES; DNA FRAGMENTATION; HEK293 CELLS; HUMANS; IONOMYCIN; JURKAT CELLS; MACROPHAGES; OLIGOSACCHARIDES; PHOSPHOPROTEINS; PROTEIN BINDING; RNA-BINDING PROTEINS;

EID: 84876381797     PISSN: 03867196     EISSN: 13473700     Source Type: Journal    
DOI: 10.1247/csf.12024     Document Type: Article

References (81)

1. Aderem, A. and Underhill, D.M. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol., 17: 593-623.
2. Allan, D. and Michell, R.H. 1975. Accumulation of 1,2-diacylglycerol in the plasma membrane may lead to echinocyte transformation of erythrocytes. Nature, 258: 348-349.
3. Allan, D., Billah, M.M., Finean, J.B., and Michell, R.H. 1976a. Release of diacylglycerol-enriched vesicles from erythrocytes with increased intracellular (Ca2+). Nature, 261: 58-60.
4. Allan, D., Watts, R., and Michell, R.H. 1976b. Production of 1,2-diacylglycerol and phosphatidate in human erythrocytes treated with calcium ions and ionophore A23187. Biochem. J., 156: 225-232.
5. Allan, D. and Michell, R.H. 1978. A calcium-activated polyphosphoinositide phosphodiesterase in the plasma membrane of human and rabbit erythrocytes. Biochim. Biophys. Acta, 508: 277-286.
6. Allan, D. and Thomas, P. 1981. Ca2+-induced biochemical changes in human erythrocytes and their relation to microvesiculation. Biochem. J., 198: 433-440.
7. Alonso-Lebrero, J.L., Serrador, J.M., Dominguez-Jimenez, C., Barreiro, O., Luque, A., Del Pozo, M.A., Snapp, K., Kansas, G., Schwartz-Albiez, R., Furthmayr, H., Lozano, F., and Sanchez-Madrid, F. 2000. Polarization and interaction of adhesion molecules P-selectin glycoprotein ligand 1 and intercellular adhesion molecule 3 with moesin and ezrin in myeloid cells. Blood, 95: 2413-2419.
8. Ando, K., Hagiwara, T., Beppu, M., and Kikugawa, K. 2000. Naturally occurring anti-band 3 antibody binds to apoptotic human T-lymphoid cell line Jurkat through sialylated poly-N-acetyllactosaminyl saccharide chains on the cell surface. Biochem. Biophys. Res. Commun., 275: 412-417.
9. Balasubramanian, K., Mirnikjoo, B., and Schroit, A.J. 2007. Regulated externalization of phosphatidylserine at the cell surface: implications for apoptosis. J. Biol. Chem., 282: 18357-18364.
10. Beppu, M., Ando, K., and Kikugawa, K. 1996a. Poly-N-acetyllactosaminyl saccharide chains of band 3 as determinants for anti-band 3 autoantibody binding to senescent and oxidized erythrocytes. Cell. Mol. Biol. (Noisy-legrand), 42: 1007-1024.
11. Beppu, M., Eda, S., Fujimaki, M., Hishiyama, E., and Kikugawa, K. 1996b. Recognition of poly-N-acetyllactosaminyl saccharide chains on iron-oxidized erythrocytes by human monocytic leukemia cell line THP-1 differentiated into macrophages. Biol. Pharm. Bull., 19: 188-194.
12. Bevers, E.M., Comfurius, P., and Zwaal, R.F. 1983. Changes in membrane phospholipid distribution during platelet activation. Biochim. Biophys. Acta, 736: 57-66.
13. Bose, S., Basu, M., and Banerjee, A.K. 2004. Role of nucleolin in human parainfluenza virus type 3 infection of human lung epithelial cells. J. Virol., 78: 8146-8158.
14. Bourguignon, L.Y. and Pressman, B.C. 1983. Stimulation of lymphocyte receptor capping by the ionophore monensin. J. Membr. Biol., 73: 91-93.
15. Bourguignon, L.Y., Lokeshwar, V.B., Chen, X., and Kerrick, W.G. 1993. Hyaluronic acid-induced lymphocyte signal transduction and HA receptor (GP85/CD44)-cytoskeleton interaction. J. Immunol., 151: 6634-6644.
16. Butikofer, P., Yee, M.C., Schott, M.A., Lubin, B.H., and Kuypers, F.A. 1993. Generation of phosphatidic acid during calcium-loading of human erythrocytes. Evidence for a phosphatidylcholine-hydrolyzing phospholipase D. Eur. J. Biochem., 213: 367-375.
17. De Verdugo, U.R., Selinka, H.C., Huber, M., Kramer, B., Kellermann, J., Hofschneider, P.H., and Kandolf, R. 1995. Characterization of a 100-kilodalton binding protein for the six serotypes of coxsackie B viruses. J. Virol., 69: 6751-6757.
18. Dehghani Zadeh, A., Seveau, S., Halbwachs-Mecarelli, L., and Keller, H.U. 2003. Chemotactically-induced redistribution of CD43 as related to polarity and locomotion of human polymorphonuclear leucocytes. Biol. Cell, 95: 265-273.
19. Dupuis, G., Heroux, J., and Payet, M.D. 1989. Characterization of Ca2+ and K+ currents in the human Jurkat T cell line: effects of phytohaemagglutinin. J. Physiol., 412: 135-154.
20. Eda, S., Beppu, M., Yokoyama, N., and Kikugawa, K. 2001. Novel lectinlike proteins on the surface of human monocytic leukemia cell line THP-1 cells that recognize oxidized cells. Arch. Biochem. Biophys., 385: 186-193.
21. Eda, S., Yamanaka, M., and Beppu, M. 2004 Carbohydrate-mediated phagocytic recognition of early apoptotic cells undergoing transient capping of CD43 glycoprotein. J. Biol. Chem., 279: 5967-5974.
22. Fadok, V.A., Bratton, D.L., and Henson, P.M. 2001. Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences. J. Clin. Invest., 108: 957-962.
23. Feske, S. 2007. Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol., 7: 690-702.
24. Fukuda, M. 1996. Possible roles of tumor-associated carbohydrate antigens. Cancer Res., 56: 2237-2244.
25. Fuller, A.D. and Van Eldik, L.J. 2008. MFG-E8 regulates microglial phagocytosis of apoptotic neurons. J. Neuroimmune Pharmacol., 3: 246-256.
26. Gil-Parrado, S., Fernandez-Montalvan, A., Assfalg-Machleidt, I., Popp, O., Bestvater, F., Holloschi, A., Knoch, T.A., Auerswald, E.A., Welsh, K., Reed, J.C., Fritz, H., Fuentes-Prior, P., Spiess, E., Salvesen, G.S., and Machleidt, W. 2002. Ionomycin-activated calpain triggers apoptosis. A probable role for Bcl-2 family members. J. Biol. Chem., 277: 27217-27226.
27. Ginisty, H., Sicard, H., Roger, B., and Bouvet, P. 1999. Structure and functions of nucleolin. J. Cell Sci., 112 (Pt 6): 761-772.
28. Hajimohammadreza, I., Raser, K.J., Nath, R., Nadimpalli, R., Scott, M., and Wang, K.K. 1997. Neuronal nitric oxide synthase and calmodulin-dependent protein kinase IIalpha undergo neurotoxin-induced proteolysis. J. Neurochem., 69: 1006-1013.
29. Hanayama, R., Tanaka, M., Miwa, K., Shinohara, A., Iwamatsu, A., and Nagata, S. 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature, 417: 182-187.
30. Hanayama, R., Tanaka, M., Miyasaka, K., Aozasa, K., Koike, M., Uchiyama, Y., and Nagata, S. 2004. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science, 304: 1147-1150.
31. Hirano, K., Miki, Y., Hirai, Y., Sato, R., Itoh, T., Hayashi, A., Yamanaka, M., Eda, S., and Beppu, M. 2005. A multifunctional shuttling protein nucleolin is a macrophage receptor for apoptotic cells. J. Biol. Chem., 280: 39284-39293.
32. Hirt, U.A., Gantner, F., and Leist, M. 2000. Phagocytosis of nonapoptotic cells dying by caspase-independent mechanisms. J. Immunol., 164: 6520-6529.
33. Ho, R., Ortiz, D., and Shea, T.B. 2001. Amyloid-beta promotes calcium influx and neurodegeneration via stimulation of L voltage-sensitive calcium channels rather than NMDA channels in cultured neurons. J. Alzheimers Dis., 3: 479-483.
34. Imboden, J.B., Weiss, A., and Stobo, J.D. 1985. The antigen receptor on a human T cell line initiates activation by increasing cytoplasmic free calcium. J. Immunol., 134: 663-665.
35. Jordan, G. 1987. At the heart of the nucleolus. Nature, 329: 489-490.
36. Kim, M.J., Jo, D.G., Hong, G.S., Kim, B.J., Lai, M., Cho, D.H., Kim, K.W., Bandyopadhyay, A., Hong, Y.M., Kim, D.H., Cho, C., Liu, J.O., Snyder, S.H., and Jung, Y.K. 2002. Calpain-dependent cleavage of cain/cabin1 activates calcineurin to mediate calcium-triggered cell death. Proc. Natl. Acad. Sci. USA, 99: 9870-9875.
37. Kondo, T., Takeuchi, K., Doi, Y., Yonemura, S., Nagata, S., and Tsukita, S. 1997. ERM (ezrin/radixin/moesin)-based molecular mechanism of microvillar breakdown at an early stage of apoptosis. J. Cell Biol., 139: 749-758.
38. Lee, K.S., Frank, S., Vanderklish, P., Arai, A., and Lynch, G. 1991. Inhibition of proteolysis protects hippocampal neurons from ischemia. Proc. Natl. Acad. Sci. USA, 88: 7233-7237.
39. Legrand, S.B. 2011. Modern management of malignant hypercalcemia. Am. J. Hosp. Palliat. Care, 28: 515-517.
40. Lew, V.L. and Ferreira, H.G. 1976. Variable Ca sensitivity of a K-selective channel in intact red-cell membranes. Nature, 263: 336-338.
41. Liossis, S. N., Kovacs, B., Dennis, G., Kammer, G.M., and Tsokos, G.C. 1996. B cells from patients with systemic lupus erythematosus display abnormal antigen receptor-mediated early signal transduction events. J. Clin. Invest., 98: 2549-2557.
42. Maderna, P. and Godson, C. 2003. Phagocytosis of apoptotic cells and the resolution of inflammation. Biochim. Biophys. Acta, 1639: 141-151.
43. McConkey, D.J., Hartzell, P., Jondal, M., and Orrenius, S. 1989a. Inhibition of DNA fragmentation in thymocytes and isolated thymocyte nuclei by agents that stimulate protein kinase C. J. Biol. Chem., 264: 13399-13402.
44. McConkey, D.J., Hartzell, P., Nicotera, P., and Orrenius, S. 1989b. Calciumactivated DNA fragmentation kills immature thymocytes. Faseb J., 3: 1843-1849.
45. Miki, Y., Tazawa, T., Hirano, K., Matsushima, H., Kumamoto, S., Hamasaki, N., Yamaguchi, T., and Beppu, M. 2007. Clearance of oxidized erythrocytes by macrophages: involvement of caspases in the generation of clearance signal at band 3 glycoprotein. Biochem. Biophys. Res. Commun., 363: 57-62.
46. Miki, Y., Itoh, T., Hirano, K., Eda, S., Hayashi, A., Yamanaka, M., and Beppu, M. 2009. Clearance of oxidatively damaged cells by macrophages: recognition of glycoprotein clusters by macrophage-surface nucleolin as early apoptotic cells. Biol. Pharm. Bull., 32: 564-572.
47. Minetti, G., Piccinini, G., Balduini, C., Seppi, C., and Brovelli, A. 1996. Tyrosine phosphorylation of band 3 protein in Ca2+/A23187-treated human erythrocytes. Biochem. J., 320 (Pt 2): 445-450.
48. Miyanishi, M., Tada, K., Koike, M., Uchiyama, Y., Kitamura, T., and Nagata, S. 2007. Identification of Tim4 as a phosphatidylserine receptor. Nature, 450: 435-439.
49. Nair, A.M., Michael, B., Datta, A., Fernandez, S., and Lairmore, M.D. 2006. Calcium-dependent enhancement of transcription of p300 by human T-lymphotropic type 1 p12I. Virology, 353: 247-257.
50. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B.A., and Yuan, J. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature, 403: 98-103.
51. Nigg, E.A. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386: 779-787.
52. Nisole, S., Said, E.A., Mische, C., Prevost, M.C., Krust, B., Bouvet, P., Bianco, A., Briand, J.P., and Hovanessian, A.G. 2002. The anti-HIV pentameric pseudopeptide HB-19 binds the C-terminal end of nucleolin and prevents anchorage of virus particles in the plasma membrane of target cells. J. Biol. Chem., 277: 20877-20886.
53. Oertner, T.G. and Matus, A. 2005. Calcium regulation of actin dynamics in dendritic spines. Cell Calcium, 37: 477-482.
54. Ogden, C.A., Decathelineau, A., Hoffmann, P. R., Bratton, D., Ghebrehiwet, B., Fadok, V.A., and Henson, P.M. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med., 194: 781-795.
55. Oguri, E., Miki, Y., Hirano, K., Yamanaka, M., and Beppu, M. 2012. Clearance of CD43-Capped Cells by Macrophages: Capping Alone Leads to Phagocytosis. Biol. Pharm. Bull., 35: 551-558.
56. Oka, K., Sawamura, T., Kikuta, K., Itokawa, S., Kume, N., Kita, T., and Masaki, T. 1998. Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc. Natl. Acad. Sci. USA, 95: 9535-9540.
57. Ossareh, S. 2011. Vascular calcification in chronic kidney disease: mechanisms and clinical implications. Iran. J. Kidney Dis., 5: 285-299.
58. Ostberg, J.R., Barth, R.K., and Frelinger, J.G. 1998. The Roman god Janus: a paradigm for the function of CD43. Immunol. Today, 19: 546-550.
59. Park, S.Y., Jung, M.Y., Kim, H.J., Lee, S.J., Kim, S.Y., Lee, B.H., Kwon, T.H., Park, R.W., and Kim, I.S. 2008. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ., 15: 192-201.
60. Platt, N., Da Silva, R.P., and Gordon, S. 1998. Recognizing death: the phagocytosis of apoptotic cells. Trends Cell Biol., 8: 365-372.
61. Podszywalow-Bartnicka, P., Strzelecka-Kiliszek, A., Bandorowicz-Pikula, J., and Pikula, S. 2007. Calcium and proton-dependent relocation of annexin A6 in Jurkat T cells stimulated for interleukin-2 secretion. Acta Biochim. Pol., 54: 261-271.
62. Ponnappa, B.C., Greenquist, A.C., and Shohet, S.B. 1980. Calciuminduced changes in polyphosphoinositides and phosphatidate in normal erythrocytes, sickle cells and hereditary pyropoikilocytes. Biochim. Biophys. Acta, 598: 494-501.
63. Ren, Y. and Savill, J. 1998. Apoptosis: the importance of being eaten. Cell Death Differ., 5: 563-568.
64. Rigotti, A., Acton, S.L., and Krieger, M. 1995. The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J. Biol. Chem., 270: 16221-16224.
65. Roberts, G.M., Davies, E.V., Pettit, E.J., and Hallett, M.B. 1997. The timing and magnitude of Ca2+ signaling by CD32 depends on its redistribution on the cell surface. Exp. Cell Res., 230: 303-9.
66. Saatman, K.E., Murai, H., Bartus, R.T., Smith, D.H., Hayward, N.J., Perri, B.R., and Mcintosh, T.K. 1996. Calpain inhibitor AK295 attenuates motor and cognitive deficits following experimental brain injury in the rat. Proc. Natl. Acad. Sci. USA, 93: 3428-3433.
67. Said, E.A., Krust, B., Nisole, S., Svab, J., Briand, J.P., and Hovanessian, A.G. 2002. The anti-HIV cytokine midkine binds the cell surfaceexpressed nucleolin as a low affinity receptor. J. Biol. Chem., 277: 37492-37502.
68. Saido, T.C., Sorimachi, H., and Suzuki, K. 1994. Calpain: new perspectives in molecular diversity and physiological-pathological involvement. Faseb J., 8: 814-822.
69. Saito, K., Elce, J.S., Hamos, J.E., and Nixon, R.A. 1993. Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc. Natl. Acad. Sci. USA, 90: 2628-2632.
70. Sambrano, G.R. and Steinberg, D. 1995. Recognition of oxidatively damaged and apoptotic cells by an oxidized low density lipoprotein receptor on mouse peritoneal macrophages: role of membrane phosphatidylserine. Proc. Natl. Acad. Sci. USA, 92: 1396-1400.
71. Sasaki, T. and Hasegawa-Sasaki, H. 1985. Breakdown of phosphatidylinositol 4,5-bisphosphate in a T-cell leukaemia line stimulated by phytohaemagglutinin is not dependent on Ca2+ mobilization. Biochem. J., 227: 971-979.
72. Savill, J., Fadok, V., Henson, P., and Haslett, C. 1993. Phagocyte recognition of cells undergoing apoptosis. Immunol. Today, 14: 131-136.
73. Savill, J. and Fadok, V. 2000. Corpse clearance defines the meaning of cell death. Nature, 407: 784-788.
74. Semenkovich, C.F., Ostlund, R.E., Jr., Olson, M.O., and Yang, J.W. 1990. A protein partially expressed on the surface of HepG2 cells that binds lipoproteins specifically is nucleolin. Biochemistry, 29: 9708-9713.
75. Seveau, S., Lopez, S., Lesavre, P., Guichard, J., Cramer, E.M., and Halbwachs-Mecarelli, L. 1997. Leukosialin (CD43, sialophorin) redistribution in uropods of polarized neutrophils is induced by CD43 cross-linking by antibodies, by colchicine or by chemotactic peptides. J. Cell Sci., 110 (Pt 13): 1465-1475.
76. Seveau, S., Eddy, R.J., Maxfield, F.R., and Pierini, L.M. 2001. Cytoskeleton dependent membrane domain segregation during neutrophil polarization. Mol. Biol. Cell, 12: 3550-3562.
77. Sinclair, J.F. and O'brien, A.D. 2002. Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-gamma of enterohemorrhagic Escherichia coli O157:H7. J. Biol. Chem., 277: 2876-2885.
78. Tsuji, T., Shimohama, S., Kimura, J., and Shimizu, K. 1998. m-Calpain (calcium-activated neutral proteinase) in Alzheimer's disease brains. Neurosci. Lett., 248: 109-112.
79. Verhallen, P.F., Bevers, E.M., Comfurius, P., and Zwaal, R.F. 1987. Correlation between calpain-mediated cytoskeletal degradation and expression of platelet procoagulant activity. A role for the platelet membrane-skeleton in the regulation of membrane lipid asymmetry? Biochim. Biophys. Acta, 903: 206-217.
80. Verhallen, P.F., Bevers, E.M., Comfurius, P., and Zwaal, R.F. 1988. Fluoride-dependent calcium-induced platelet procoagulant activity shows that calpain is involved in increased phospholipid transbilayer movement. Biochim. Biophys. Acta, 942: 150-158.
81. Yamanaka, M., Eda, S., and Beppu, M. 2005. Carbohydrate chains and phosphatidylserine successively work as signals for apoptotic cell removal. Biochem. Biophys. Res. Commun., 328: 273-280.