Skip to main content
SpringerLink
Log in

Clearance of Apoptotic Lymphocytes by Human Kupffer Cells. Phagocytosis of Apoptotic Cells in the Liver: Role of Lectin Receptors and Therapeutic Advantages

  • Chapter
Apoptosis and Its Modulation by Drugs

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 142))

Abstract

This chapter (see also SAVILL and BEBB, , this volume,) deals with the removal of apoptotic cells. The engulfment of cells undergoing apoptosis can be considered a specialized form of phagocytosis, playing a major role in the general tissue homeostasis in physiological and pathological conditions. Phagocytic recognition of apoptotic cells is less well understood than the death program itself, but an increasing number of recent studies are highlighting its importance. A particular aspect of phagocytosis of apoptotic cells will be considered: the Kupffer-cell-mediated removal of apoptotic lymphocytes.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 349.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 449.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 449.99
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

  • Asumendi A, Alvarez A, Martinez I, Smedsrod B, Vidal-Vanaclocha F (1996) Hepatic sinusoidal endothelium heterogeneity with respect to mannose receptor activity is interleukin 1 dependent. Hepatology 23:1521–1529

    Article  PubMed  CAS  Google Scholar 

  • Botto M, Dell’Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, Loos M, Pandolfi PP, Walport MJ (1998) Homozygous Clq deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19:56–59

    Article  PubMed  CAS  Google Scholar 

  • Brunner T, Mogil RJ, LaFace D, Yoo NJ, Mahboubi A, Echeverri F, Martin SJ, Force WR, Lynch DH, Ware CF, Green DR (1995) Cell-autonomous Fas (CD95)/ Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373:441–444

    Article  PubMed  CAS  Google Scholar 

  • Bursch W, Dusterberg B, Schulte-Hermann R (1986) Growth, regression and cell death in rat liver as related to tissue levels of the hepatomitogen cytoproterone acetate. Arch Toxicol 59:221–227

    Article  PubMed  CAS  Google Scholar 

  • Bursch W, Oberhammer F, Schlte-Hermann R (1992) Cell death by apoptosis and its protective role against disease. Trends Pharmacol Sci 13:245–251

    Article  PubMed  CAS  Google Scholar 

  • Burt AD, Le Bail B, Balabaud C, Bioulac-Sage P (1993) Morphological investigation of sinusoidal cells. Semin Liver Dis 13:21–38

    Article  PubMed  CAS  Google Scholar 

  • Carbonari M, Cibati M, Cherchi M, Sbarigia D, Pesce AM, Dell’Anna L, Modica A, Fiorilli M (1994) Detection and characterization of apoptotic peripheral blood lymphocytes in human immunodeficiency virus infection and cancer chemotherapy by a novel flow immunocytometric method. Blood 83:1268–1277

    PubMed  CAS  Google Scholar 

  • Castedo M, Macho A, Zamzami N, Hirsh T, Marchetti P, Uriel J, Kroemer G (1995) Mitochondrial perturbations define lymphocytes undergoing apoptotic depletion in vivo. Eur J Immunol 25:3277–3284

    Article  PubMed  CAS  Google Scholar 

  • Clarke P (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181:195–213

    Article  PubMed  CAS  Google Scholar 

  • Cobb JP, Hotchkiss RS, Karl IE, Buchman TG (1996) Mechanisms of cell injury and death British Journal of Anaesthesia. 77:3–10

    Article  PubMed  CAS  Google Scholar 

  • Columbano A, Ledda-Columbano GM, Coni P, Faa G, Liguori C, Santacruz G, Pani G (1985) Occurrence of cell death (apoptosis) during the involution of liver hyperplasia. Lab Invest 52:670–677

    PubMed  CAS  Google Scholar 

  • Devitt A, Moffatt OD, Raykundalia C, Capra JD, Simmons DL, Gregory CD (1998) Human CD 14 mediates recognition and phagocytosis of apoptotic cells. Nature 392:505–508

    Article  PubMed  CAS  Google Scholar 

  • Dhein J, Walczak H, Baumler C, Debatin KM, Kramer PH (1995) Autocrine T-cell suicide mediated by APO-1/. Nature 373:438–441

    Article  PubMed  CAS  Google Scholar 

  • Dini L, Kolb-Bachofen V (1989) Preclustered receptor arrangement is a prerequisite for galactose-specific clearance of large particulate ligands in rat liver. Exp Cell Res 184:235–240

    Article  PubMed  CAS  Google Scholar 

  • Dini L, Autuori F, Lentini A, Oliverio S, Piacentini M (1992) The clearance of apoptotic cells in the liver is mediated by the asialoglycoprotein receptor. FEBS Lett 296:174–178

    Article  PubMed  CAS  Google Scholar 

  • Dini L, Falasca L, Lentini A, Mattioli P, Piacentini M, Piredda L, Autuori F (1993) Galactose-specific receptor modulation related to the onset of apoptosis in rat liver. Europ J Cell Biol 61:329–337

    PubMed  CAS  Google Scholar 

  • Dini L, Lentini A, Diez Diez G, Rocha M, Falasca L, Serafino L, Vidal-Vanaclocha F (1995) Phagocytosis of apoptotic bodies by liver endothelial cells. J Cell Sci 108:967–973

    PubMed  CAS  Google Scholar 

  • Dini L, Ruzittu M, Falasca L (1996a) Recognition and phagocytosis of apoptotic cells. Scanning microscopy 10:239–252

    PubMed  CAS  Google Scholar 

  • Dini L, Coppola S, Ruzittu M, Ghibelli L (1996b) Multiple pathways for apoptotic nuclear fragmentation. Exp Cell Res 223:340–347

    Article  PubMed  CAS  Google Scholar 

  • Dini L, Carlà EC (1998) Hepatic sinusoidal endothelium heterogeneity with respect to the recognition of apoptotic cells. 240:388–393

    CAS  Google Scholar 

  • Dini L, Ruzittu M, Carlà EC, Falasca L (1998) Relationship between cellular shape and recepto-mediated endocytosis: an ultrastructural and morphometric study in rat Kupffer cells. Liver 18:99–109

    PubMed  CAS  Google Scholar 

  • Dini L, Giudetti AM, Ruzittu M, Gnoni GV, Zara V (1999) Citrate carrier and lipogenic enzyme activities in lead nitrate-induced proliferative and apoptotic phase in rat liver. Biochim Cell Mol Intern 47(4):607–614

    CAS  Google Scholar 

  • Dini L (1999) Endothelial liver cell recognition of apoptotic peripheral blood lymphocytes. Biochemical Society Transactions 26:635–637

    Google Scholar 

  • Durrieu F, Belloc F, Lacoste L, Dumain P, Chabrol J, Dachary-Prigent J, Morjani H, Boisseau MR, Reiffers J, Bernard P, Lacombe F (1998) Caspase activation is an early event in anthracycline-induced apoptosis and allows detection of apoptotic cells before they are ingested by phagocytes. Exp. Cell Res 240:165–175

    Article  PubMed  CAS  Google Scholar 

  • Duvall E, Wyllie AH, Morris RG (1985) Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 56:351–358

    PubMed  CAS  Google Scholar 

  • Ellis RE, Jacobson DM, Horvitz HR (1991a) Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics 129:79–94

    PubMed  CAS  Google Scholar 

  • Ellis RE, Yuan J, Horvitz HR (1991b) Mechanisms and functions of cell death. Annu Rev Cell Biol 7:663–698

    Article  PubMed  CAS  Google Scholar 

  • Emoto K, Toyama-Sorimachi N, Karasuyama H, Inoue K, Umeda M (1997) Exposure of phosphatidylethanolamine on the surface of apoptotic cells. Exp Cell Res 232:430–434

    Article  PubMed  CAS  Google Scholar 

  • Fadok VA, Savill JS, Haslett C, Bratton DL, Doherty DE, Campbell PA, Henson PM (1992a) Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J Immunol 149:4029–4035

    PubMed  CAS  Google Scholar 

  • Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM (1992b) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148:2207–2216

    PubMed  CAS  Google Scholar 

  • Fadok VA, Bratton DL, Frasch SC, Warner ML, Henson PM (1998a) The role of phosphatidylserine in recognition of apoptotic cells by phagocytes. Cell Death Differ 5:551–562

    Article  PubMed  CAS  Google Scholar 

  • Fadok VA, Bratton DL, Konoval A, Freed PW, Westcott JY, Henson PM (1998b) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF, PGE2, and PAF. J Clin Invest 101:890–898

    Article  PubMed  CAS  Google Scholar 

  • Falasca L, Bergamini A, Serafino A, Balabaud C, Dini L (1996) Human Kupffer cell recognition and phagocytosis of apoptotic peripheral blood lymphocytes. Exp Cell Res 224:152–162

    Article  PubMed  CAS  Google Scholar 

  • Flora PK, Gregory CD (1994) Recognition of apoptotic cells by human macrophages: inhibition by a monocyte/macrophage-specific monoclonal antibody. Eur J Immunol 24:2625–2632

    Article  PubMed  CAS  Google Scholar 

  • Friesen C, Herr I, Krammer PH, Debatin KM (1996) Involvement of the CD95 (APO-1/Fas) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nature Med 2:574–577

    Article  PubMed  CAS  Google Scholar 

  • Gerschenson LE, Rotello RJ (1991) Apoptosis and cell proliferation are terms of the growth equation. In: Apoptosis. The molecular basis of cell death. Cold Spring Harbor Laboratory Press, p 175

    Google Scholar 

  • Grasl Kraupp B, Bursch W, Ruttkay Nedecky B, Wagner A, Lauer B, Schulte-Hermann R (1994) Food restiction eliminates preneoplastic cells through apoptosis and antagonizes carcinogenesis in rat liver. Proc Natl Acad Sci USA 91:9995–9999

    Article  PubMed  CAS  Google Scholar 

  • Hall SE, Savill JS, Henson PM, Haslett C (1994) Apoptotic neutrophils are phagocytosed by fibroblasts with participation of the fibroblast vitronectin receptor and involvement of a mannose/fucose-specific lectin. J Immunol 153: 3218–3227

    PubMed  CAS  Google Scholar 

  • Hart SP, Haslett C, Dransfield I (1996) Recognition of apoptotic cells by phagocytes. Experientia 52:950–956

    Article  PubMed  CAS  Google Scholar 

  • Haslett C, Savill JS, Whyte MKB, Stern M, Dransfield I, Meagher LC (1994) Granulocyte apoptosis and the control of inflammation. Phil Trans R Soc London Bbiol Sci 345:327–333

    Article  CAS  Google Scholar 

  • Herrmann M, Voll RE, Zoller OM, Hagenhofer M, Ponner BB, Kalden JR (1998) Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum 41:1241–1250

    Article  PubMed  CAS  Google Scholar 

  • Huang L, Soldevila G, Leeker M, Flavell R, Crispe N (1994) The liver eliminates T cells undergoing antigen-triggered apoptosis in vivo. Immunity 1:741–749

    Article  PubMed  CAS  Google Scholar 

  • Hubbard AL, Wilson G, Ashwell G, Stukenbrok H (1979) An electron microscopic autoradiographic study of the carbohydrate recognition system in rat liver. I distribution of 1251-ligands among the liver cell types. J. Cell Biol 83:47–64

    Article  PubMed  CAS  Google Scholar 

  • Jones EA, Summerfield JA (1982) Kupffer cells In: Arias I, Popper H, Schacter D, Shafritz DA (eds), The liver: biology and pathobiology, Raven Press, New York, p 507

    Google Scholar 

  • Kempka G, Roos P, Kolb-Bachofen V (1990) A membrane-associated form of Creactive protein is the galactose-specific particle receptor on rat Kupffer cells. J Immunol 144:1004–1009

    PubMed  CAS  Google Scholar 

  • Kirn A, Gut JP, Gendrault JL (1982) Interaction of viruses with sinusoidal cells. In: Popper H, Schaffner F (eds) Progress in liver diseases. New York: Grune & Stratton, p377

    Google Scholar 

  • Kolb H, Friedrick E, Suss R (1981) Lectin mediates homing of neuraminidase-treated erythrocytes to the liver as revealed by scintigraphy. Hoppe-Seyler’s Z Physiol Chem 362:1609–1614

    Article  PubMed  CAS  Google Scholar 

  • Kolb-Bachofen V, Schlepper-Schafer J, Vogell W (1982) Electron microscopic observations of the hepatic microscopic evidence for an asailoglycoprotein receptor on Kupffer cells: localization of lectin mediated endocytosis. Cell 29:859–866

    Article  PubMed  CAS  Google Scholar 

  • Kolb-Bachofen V (1992) A review on the biological properties of C-reactive protein. Immunobiol 183:133–145

    Article  Google Scholar 

  • Kornbluthh RS (1994) Significance of T cell apoptosis for macrophages in HIV infection. J Leukoc Biol 56:247–256

    Google Scholar 

  • Kumar S (1995) ICE-like proteases in apoptosis. Trends Biochem Sci 20:198–202

    Article  PubMed  CAS  Google Scholar 

  • Kuypers FA (1998) Phospholipid asymmetry in health and disease Curr Opin Hematol 5:122–131

    Article  PubMed  CAS  Google Scholar 

  • Ledda-Columbano GM, Shinozuka H, Katyal SL, Columbano A (1996) Cell proliferation, cell death and hepatocarcinogenesis. Cell Death Differ 3:17–22

    PubMed  CAS  Google Scholar 

  • Liu QA, Hengartner MO (1998) Candidate adaptor protein CED-6 promotes the engulfment of apoptotic cells in C. elegans. Cell 93:961–972

    Article  CAS  Google Scholar 

  • Luciani MF, Chimini G (1996) The ATP binding cassette transporter ABCD1, is required for the engulfment of corpses generated by apoptotic cell death. EMBO J 15:226–235

    PubMed  CAS  Google Scholar 

  • Martin SJ, Reutelingsperger CPM, McGahon AJ, Rader JA, van Schie RCA, LaFace DM, Green DR (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182:1545–1556

    Article  PubMed  CAS  Google Scholar 

  • Massimi M, Conti Devirgiliis, Kolb-Bachofen V, Dini L (1995) Independent modulation of galactose-specific receptor expression in rat liver cells. Hepatology 22:1819–1828

    PubMed  CAS  Google Scholar 

  • Massimi M, Falasca L, Felici A, Dini L, Conti Devirgiliis L (1996) Expression of the asialoglycoprotein receptor in cultured rat hepatocytes is modulated by cell density. Bioscience Reports 16:477–484

    Article  PubMed  CAS  Google Scholar 

  • McEvoy L, Williamson P, Schlegel RA (1986) Membrane phospholipid asymmetry as a determinant of erytrocyte recognition by macrophages. Proc Natl Acad Sci USA 83:3311–3315

    Article  PubMed  CAS  Google Scholar 

  • McMurchie EJ, Raison JK (1979) Membrane lipid fluidity and its effect on the activation energy of membrane-associated enzymes. Biochim Biophys Acta 554:364–374

    Article  PubMed  CAS  Google Scholar 

  • Meagher LC, Savill JS, Baker A, Fuller R, Haslett C (1992) Phagocytosis of apoptotic neutrophils does not induce macrophage release of thromboxane B2. J Leuk Biol 52:269–273

    CAS  Google Scholar 

  • Morin O, Patry P, and Lafleur L (1984) Heterogeneity of endothelial cells of adult rat liver as resolved by sedimentation velocity and flow cytometry. J Cell Physiol 119:327–334

    Article  PubMed  CAS  Google Scholar 

  • Morris RG, Hargreaves AD, Duvall E, Wyllie AH (1984) Surface changes in thymocytes undergoing apoptosis. Am J Path 115:426–436

    PubMed  CAS  Google Scholar 

  • Nenseter MS, Gudmundsenn O, Roos N, Maelandsmo G, Drevon CA, Berg T (1992) The role of liver endothelial and Kupffer cells in clearing low density lipoprotein from blood in hypercholestrerolemic rabbits. J lipid Res 33:867–877

    PubMed  CAS  Google Scholar 

  • Neaud V, Dubuisson L, Balabaud C, Bioulac-Sage P (1995) Ultrastructure of human Kupffer cells maintained in culture. J Submicrosc Cytol Pathol 27:161–170

    PubMed  CAS  Google Scholar 

  • Nishikawa A, Murata E, Akita M, Kaneko K, Moriya O, Tomita M, Hayashi H (1998) Roles of macrophages in programmed cell death and remodelling of tail and body muscle of Xenopus laevis during metamorphosis. Histochem Cell Biol 109:11–17

    Article  PubMed  CAS  Google Scholar 

  • Ogasawara J, Wtanabe-Fukunaga R, Adachi M, Matsuzawa A, Kasugai T, Kitamura Y, Itoh N, Suda T, Nagata S (1993) Lethal effect of the anti-Fas antibody in mice. Nature 364:806–809

    Article  PubMed  CAS  Google Scholar 

  • Platt N, Pedro da Silva R, Gordon S (1998) Recognizing death: the phagocytosis of apoptotic cells. Trends in Cell Biology 8:365–372

    Article  PubMed  CAS  Google Scholar 

  • Pradhan D, Williamson P, Schlegel RA (1994) Phosphatidylserine vesicles inhibit phagocytosis of erythrocytes with a symmetric transbilayer distribution of phospholipids. Mol Membr Biol 11:181–187

    Article  PubMed  CAS  Google Scholar 

  • Pradhan D, Krahling S, Williamson P, Schlegel RA (1997) Multiple systems for recognition of apoptotic lymphocytes by macrophages. Mol Biol Cell 8:767–778

    PubMed  CAS  Google Scholar 

  • Praaning-van Dalen DP, de Leeuw AM, Brouwer A, Knook DL (1987) Rat liver endothelial cells have a greater capacity than Kupffer cells to endocytose N-acetylglucosamine-and mannose-terminated glycoproteins. Hepatology 7:672–679

    Article  Google Scholar 

  • Ravetch JV (1994) Fc receptors: rubor redux. Cell 78:553–560

    Article  PubMed  CAS  Google Scholar 

  • Ren V, Silverstein RL, Allen J, Savill J (1995) CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J Exp Med 181:1857–1862

    Article  PubMed  CAS  Google Scholar 

  • Ren V, Savill J (1998) Apoptosis: the importance of being eaten. Cell Death Differ 5:563–568

    Article  PubMed  CAS  Google Scholar 

  • Rifai A, Mannik M (1984) Clearance of circulating IgA immune complexes is mediated by a specific receptor on Kupffer cells in mice. J Exp Med 160:125–137

    Article  PubMed  CAS  Google Scholar 

  • Rocha M, Lentini A, Asumendi A, Falasca L, Autuori F, Dini L, Vidal-Vanaclocha F (1993) In situ and in vitro correlation between mannose receptor expression and fenestration pattern in endothelial cells selected from different zones of liver lobule. In Knook D, Wisse E (ed) Cells of the hepatic sinusoid, vol 5. Kupffer Cell Foundation, Leiden, The Netherlands, p 470

    Google Scholar 

  • Roos E, Dingemans KP, Van de Pavert IV, Van den Bergh-Weerman MA (1978) Mammary-carcinoma cells in mouse liver: infiltration of liver tissue and interaction with Kupffer cells. Brit J Cancer 38:88–99

    Article  PubMed  CAS  Google Scholar 

  • Roerdink F, Dijkstra J, Hartman G, et al. (1981) The involvement of parenchymal, Kupffer and endothelial liver cells in the hepatic uptake of intravenously injected liposomes. Effects of lanthanum and gadolinium salts. Biochim Biophys Acta 677:79–89

    Article  PubMed  CAS  Google Scholar 

  • Ruiter DJ, Van der Meulen J, Brouwer A, Hummel MJ, Mauw BJ, Van der Ploeg JC, Wisse E (1981) Uptake by liver cells of endotoxin following its intravenous injection. Lab Invest 45:38–45

    PubMed  CAS  Google Scholar 

  • Savill JS, Henson PM, Haslett C (1989) Phagocytosis of aged human neutrophils by macrophages is mediated by a novel “charge-sensitive” recognition mechanism. J Clin Invest 84:1518–1527

    Article  PubMed  CAS  Google Scholar 

  • Savill J, Dransfield L, Hogg N, Haslett C (1990) Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343:170–173

    Article  PubMed  CAS  Google Scholar 

  • Savill J, Hogg N, Ren Y, Haslett C (1992a) Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest 90:1513–1522

    Article  PubMed  CAS  Google Scholar 

  • Savill J, Smith J, Sarraf C, Ren Y, Abbott F, Ress A (1992b) Glomerular mesangial cells and inflammatory macrophages ingest neutrophilis undergoing apoptosis. Kidney Int 42:924–936

    Article  PubMed  CAS  Google Scholar 

  • Savill J, Fadok V, Henson P, Haslett C (1993) Phagocyte recognition of cells undergoing apoptosis Immunol Today 14:131–136

    Article  PubMed  CAS  Google Scholar 

  • Savill JS (1997) Recognition and phagocytosis of cells undergoing apoptosis. Br Med Bull 53:491–508

    Article  PubMed  CAS  Google Scholar 

  • Savill JS (1998) Phagocytic docking without shocking Nature 392:442–443

    Article  PubMed  CAS  Google Scholar 

  • Schlegel RA, Williamson P (1987) Membrane phospholipid organization as a determinant of blood cell-reticuloendothelial cell interactions. J Cell Physiol 132:381–384

    Article  PubMed  CAS  Google Scholar 

  • Schlegel RA, Callahan M, Krahling S, Pradhan D, Williamson P (1996) Mechanisms for recognition and phagocytosis of apoptotic lymphocytes by macrophages. Adv Exp Med Biol 406:21–28

    PubMed  CAS  Google Scholar 

  • Shiratsuchi A, Osada S, Kanazawa S, Nakanishi Y (1998) Essential role of phosphatidylserine externalization in apoptosing cell phagocytosis by macrophages. Biochem Biophys Res Commun 246:549–555

    Article  PubMed  CAS  Google Scholar 

  • Shiratori Y, Tanaka M, Kawase T, Shiina S, Komatsu Y, Omata M (1993) Quantification of sinusoidal cell function in vivo. Semin LiverDis 13:39–49

    Article  CAS  Google Scholar 

  • Smedsrød B, Pertoft H, Gustafson S, Laurent TC (1990) Scavenger functions of the liver endothelial cell. Biochem J 266:313–327

    PubMed  Google Scholar 

  • Smedsrød B, Deblaser PJ, Braet F, Lovisetti P, Vanderkerken K, Wisse E, Geerts A (1994) Cell biology of liver endothelial and Kupffer cells. Gut 35:1509–1516

    Article  PubMed  Google Scholar 

  • Steer CJ, Clarenburg R (1979) Unique distribution of glycoprotein receptors on parenchymal and sinusoidal cells of rat liver. J Biol Chem 254:4457–4461

    PubMed  CAS  Google Scholar 

  • Steffan AM, Gendrault JL, McCuskey RS, McCuskey PA, Kirn A (1986) Phagocytosis, an unrecognized property of murine endothelial liver cells. Hepatology 6:830–836

    Article  PubMed  CAS  Google Scholar 

  • Stern M, Meagher L, Savill J, Haslett C (1992) Apoptosis in human eosinophils. Programmed cell death in the eosinophil leads to phagocytosis by macrophages and is modulated by IL-5. J Immunol 148:3543–3549

    PubMed  CAS  Google Scholar 

  • Stuart MC, Damoiseaux JG, Frederik PM, Arends JW, Reutelingsperger CP (1998) Surface exposure of phosphatidylserine during apoptosis of rat thymocytes precedes nuclear changes. 76:77–83

    CAS  Google Scholar 

  • Swanson JA, Baer SC (1995) Phagocytosis by zippers and triggers. Trends Cell Biol 5:89–93

    Article  PubMed  CAS  Google Scholar 

  • Tessitore L, Valente G, Bonelli G, Costelli P, Baccino FM (1989) Regulation of cell turnover in the livers of tumor bearing rats: occurrence of apoptosis. Int J Cancer 44:697–700

    Article  PubMed  CAS  Google Scholar 

  • Toth CA, Thomas P (1992) Liver endocytosis and Kupffer cells. Hepatology 16:255–266

    Article  PubMed  CAS  Google Scholar 

  • Van Berkel TJC, De Rijke JB, Kruijt JK (1992) Recognition of modified lipoprotein by various scavenger receptors on Kupffer and endothelial liver cells. In: Windier E, Greten H, eds. Hepatic endocytosis of lipids and proteins. Munchen, FRG: Zuckschwerdt, p 443

    Google Scholar 

  • Vidal-Vanaclocha F, Amezaga C, Asumendi A, Kaplanski G, Dinarello CA (1994) Interleukin-1 receptor blockade reduces the number and size of murine B16 melanome hepatic metastasis. Cancer Res 54:2667–2672

    PubMed  CAS  Google Scholar 

  • Voll RE, Hermann M, Roth EA, Stach C, Kalden JR, Girkontaite I (1997) Immunosuppressive effects of apoptotic cells. Nature 390:350–351

    Article  PubMed  CAS  Google Scholar 

  • Wardle EM (1987) Kupffer cells and their function. Liver 7:63–70

    PubMed  CAS  Google Scholar 

  • Watanabe S (1988) Calmodulin antagonists inhibit the phagocytic activity of cultured Kupffer cells. Lab Invest 59:214–218

    PubMed  CAS  Google Scholar 

  • Watanabe S, Hirose M, Ueno T et al. (1990) Integrity of the cytoskeletal system is important for phagocytosis by Kupffer cells. Liver 10:249–254

    PubMed  CAS  Google Scholar 

  • Wu YC, Horvitz HR (1998) C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK 180. Nature 392:501–504

    Article  PubMed  CAS  Google Scholar 

Download references

Authors
  1. L. Dini
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Pathology Toronto Hospital, General Division, University of Toronto, 200 Elizabeth Street, Toronto, Ontario, Canada, M5G 2C4

    Ross G. Cameron M.D., Ph.D.

  2. Banting Institute Department of Clinical Biochemistry, University of Toronto, Toronto, Ontario, Canada, M5G 2C4

    George Feuer Ph.D., C. Med. Sci.

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Dini, L. (2000). Clearance of Apoptotic Lymphocytes by Human Kupffer Cells. Phagocytosis of Apoptotic Cells in the Liver: Role of Lectin Receptors and Therapeutic Advantages. In: Cameron, R.G., Feuer, G. (eds) Apoptosis and Its Modulation by Drugs. Handbook of Experimental Pharmacology, vol 142. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-57075-9_12

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-57075-9_12

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-63025-5

  • Online ISBN: 978-3-642-57075-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation