Skip to main content
SpringerLink
Log in

Molecules Involved in Recognition and Clearance of Apoptotic/Necrotic Cells and Cell Debris

  • Chapter
Phagocytosis of Dying Cells: From Molecular Mechanisms to Human Diseases

Abstract

Disposal of apoptotic or necrotic cells or cell remnants is of paramount importance for the survival of multicellular organisms. Plasma membrane rupture of accumulating dying cells would lead to a deluge of cellular components into the extracellular spaces and could lead to impairment of tissue organisation, occlusion of vessels and the induction of inflammatory and autoimmune reactions. Therefore, efficient mechanisms exist, that secure safe disposal of dying cells and their contents. Neighbouring cells and professional phagocytes like macrophages and immature dendritic cells are the main effector cells of these processes. The mechanism of engulfment of dying cells and the signalling pathways leading to phagocytosis are described. In addition, extracellular mechanisms seem to exist that are activated for the disposal of necrotic cells and their remnants.

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 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

  • Agah A, Kyriakides TR, Lawler J et al (2002) The lack of thrombospondin-1 (TSP1) dictates the course of wound healing in double-TSP1/TSP2-null mice. Am J Pathol 161(3):831–839

    PubMed  CAS  Google Scholar 

  • Akakura S, Singh S, Spataro M et al (2004) The opsonin MFG-E8 is a ligand for the alphavbeta5 integrin and triggers DOCK180-dependent Rac1 activation for the phagocytosis of apoptotic cells. Exp Cell Res 292(2):403–416

    Article  PubMed  CAS  Google Scholar 

  • Akpovi CD, Yoon SR, Vitale ML et al (2006) The predominance of one of the SR-BI isoforms is associated with increased esterified cholesterol levels not apoptosis in mink testis. J Lipid Res 47(10):2233–2247

    Article  PubMed  CAS  Google Scholar 

  • Albert ML, Kim JI, Birge RB (2000) alphavbeta5 integrin recruits the CrkII-Dock180-rac1 complex for phagocytosis of apoptotic cells. Nat Cell Biol 2(12):899–905

    Article  PubMed  CAS  Google Scholar 

  • Albert ML, Pearce SF, Francisco LM et al (1998a) Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med 188(7):1359–1368

    Article  CAS  Google Scholar 

  • Albert ML, Sauter B, Bhardwaj N (1998b) Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392(6671):86–89

    Article  CAS  Google Scholar 

  • Anderson HA, Maylock CA, Williams JA et al (2003) Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat Immunol 4(1):87–91

    Article  PubMed  CAS  Google Scholar 

  • Arur S, Uche UE, Rezaul K et al (2003) Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev Cell 4(4):587–598

    Article  PubMed  CAS  Google Scholar 

  • Asch AS, Barnwell J, Silverstein RL et al (1987) Isolation of the thrombospondin membrane receptor. J Clin Invest 79(4):1054–1061

    Article  PubMed  CAS  Google Scholar 

  • Atsumi G, Murakami M, Kojima K et al (2000) Distinct roles of two intracellular phospholipase A2s in fatty acid release in the cell death pathway. Proteolytic fragment of type IVA cytosolic phospholipase A2alpha inhibits stimulus-induced arachidonate release, whereas that of type VI Ca2+-independent phospholipase A2 augments spontaneous fatty acid release. J Biol Chem 275(24):18248–18258

    Article  PubMed  CAS  Google Scholar 

  • Atsumi G, Murakami M, Tajima M et al (1997) The perturbed membrane of cells undergoing apoptosis is susceptible to type II secretory phospholipase A2 to liberate arachidonic acid. Biochim Biophys Acta 1349(1):43–54

    PubMed  CAS  Google Scholar 

  • Balasubramanian K, Chandra J, Schroit AJ (1997) Immune clearance of phosphatidylserineexpressing cells by phagocytes. The role of beta2-glycoprotein I in macrophage recognition. J Biol Chem 272(49):31113–31117

    Article  PubMed  CAS  Google Scholar 

  • Balasubramanian K, Maiti SN, Schroit AJ (2005) Recruitment of beta-2-glycoprotein 1 to cell surfaces in extrinsic and intrinsic apoptosis. Apoptosis 10(2):439–446

    Article  PubMed  CAS  Google Scholar 

  • Balasubramanian K, Schroit AJ (1998) Characterization of phosphatidylserine-dependent beta2-glycoprotein I macrophage interactions. Implications for apoptotic cell clearance by phagocytes. J Biol Chem 273(44):29272–29277

    Article  PubMed  CAS  Google Scholar 

  • Barker RN, Erwig LP, Hill KS et al (2002) Antigen presentation by macrophages is enhanced by the uptake of necrotic, but not apoptotic, cells. Clin Exp Immunol 127(2):220–225

    Article  PubMed  CAS  Google Scholar 

  • Baron WF, Pan CQ, Spencer SA et al (1998) Cloning and characterization of an actin-resistant DNase I-like endonuclease secreted by macrophages. Gene 215(2):291–301

    Article  PubMed  CAS  Google Scholar 

  • Bennett RM, Gabor GT, Merritt MM (1985) DNA binding to human leukocytes. Evidence for a receptor-mediated association, internalization, and degradation of DNA. J Clin Invest 76(6):2182–2190

    Article  PubMed  CAS  Google Scholar 

  • Bevers EM, Comfurius P, Dekkers DW et al (1999) Lipid translocation across the plasma membrane of mammalian cells. Biochim Biophys Acta 1439(3):317–330

    PubMed  CAS  Google Scholar 

  • Bickerstaff MC, Botto M, Hutchinson WL et al (1999) Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat Med 5(6):694–697

    Article  PubMed  CAS  Google Scholar 

  • Bijl M, Horst G, Bijzet J et al (2003) Serum amyloid P component binds to late apoptotic cells and mediates their uptake by monocyte-derived macrophages. Arthritis Rheum 48(1):248–254

    Article  PubMed  CAS  Google Scholar 

  • Bilyy R, Stoika R (2007) Search for novel cell surface markers of apoptotic cells. Autoimmunity 40(4):249–253

    Article  PubMed  CAS  Google Scholar 

  • Boes M, Schmidt T, Linkemann K et al (2000) Accelerated development of IgG autoantibodies and autoimmune disease in the absence of secreted IgM. Proc Natl Acad Sci U S A 97(3):1184–1189

    Article  PubMed  CAS  Google Scholar 

  • Borisenko GG, Iverson SL, Ahlberg S et al (2004) Milk fat globule epidermal growth factor 8 (MFG-E8) binds to oxidized phosphatidylserine: implications for macrophage clearance of apoptotic cells. Cell Death Differ 11(8):943–945

    Article  PubMed  CAS  Google Scholar 

  • Borth W (1992) Alpha 2-macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J 6(15):3345–3353

    PubMed  CAS  Google Scholar 

  • Bose J, Gruber AD, Helming L et al (2004) The phosphatidylserine receptor has essential functions during embryogenesis but not in apoptotic cell removal. J Biol 3(4):15

    Article  PubMed  Google Scholar 

  • Bottcher A, Gaipl US, Furnrohr BG et al (2006) Involvement of phosphatidylserine, alphavbeta3, CD14, CD36, and complement C1q in the phagocytosis of primary necrotic lymphocytes by macrophages. Arthritis Rheum 54(3):927–938

    Article  PubMed  CAS  Google Scholar 

  • Botto M, Dell’Agnola C, Bygrave AE et al (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19(1):56–59

    Article  PubMed  CAS  Google Scholar 

  • Brouckaert G, Kalai M, Krysko DV et al (2004) Phagocytosis of necrotic cells by macrophages is phosphatidylserine dependent and does not induce inflammatory cytokine production. Mol Biol Cell 15(3):1089–1100

    Article  PubMed  CAS  Google Scholar 

  • Brown S, Heinisch I, Ross E et al (2002) Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature 418(6894):200–203

    Article  PubMed  CAS  Google Scholar 

  • Callahan MK, Williamson P, Schlegel RA (2000) Surface expression of phosphatidylserine on macrophages is required for phagocytosis of apoptotic thymocytes. Cell Death Differ 7(7):645–653

    Article  PubMed  CAS  Google Scholar 

  • Campisi J, Leem TH, Fleshner M (2003) Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress Chaperones 8(3):272–286

    Article  PubMed  CAS  Google Scholar 

  • Casciola-Rosen L, Rosen A, Petri M et al (1996) Surface blebs on apoptotic cells are sites of enhanced procoagulant activity: implications for coagulation events and antigenic spread in systemic lupus erythematosus. Proc Natl Acad Sci U S A 93(4):1624–1629

    Article  PubMed  CAS  Google Scholar 

  • Casciola-Rosen LA, Anhalt G, Rosen A (1994) Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med 179(4):1317–1330

    Article  PubMed  CAS  Google Scholar 

  • Choi JJ, Reich CF, 3rd, Pisetsky DS (2005) The role of macrophages in the in vitro generation of extracellular DNA from apoptotic and necrotic cells. Immunology 115(1):55–62

    Article  PubMed  CAS  Google Scholar 

  • Chung S, Gumienny TL, Hengartner MO et al (2000) A common set of engulfment genes mediates removal of both apoptotic and necrotic cell corpses in C. elegans. Nat Cell Biol 2(12):931–937

    Article  PubMed  CAS  Google Scholar 

  • Clayton AR, Prue RL, Harper L et al (2003) Dendritic cell uptake of human apoptotic and necrotic neutrophils inhibits CD40, CD80, and CD86 expression and reduces allogeneic T cell responses: relevance to systemic vasculitis. Arthritis Rheum 48(8):2362–2374

    Article  PubMed  CAS  Google Scholar 

  • Cocco RE, Ucker DS (2001) Distinct modes of macrophage recognition for apoptotic and necrotic cells are not specified exclusively by phosphatidylserine exposure. Mol Biol Cell 12(4):919–930

    PubMed  CAS  Google Scholar 

  • Cohen PL, Caricchio R, Abraham V et al (2002) Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med 196(1):135–140

    Article  PubMed  CAS  Google Scholar 

  • Cvetanovic M, Ucker DS (2004) Innate immune discrimination of apoptotic cells: repression of proinflammatory macrophage transcription is coupled directly to specific recognition. J Immunol 172(2):880–889

    PubMed  CAS  Google Scholar 

  • D’Cruz PM, Yasumura D, Weir J et al (2000) Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet 9(4):645–651

    Article  PubMed  CAS  Google Scholar 

  • deCathelineau AM, Henson PM (2003) The final step in programmed cell death: phagocytes carry apoptotic cells to the grave. Essays Biochem 39:105–117

    PubMed  CAS  Google Scholar 

  • Devitt A, Parker KG, Ogden CA et al (2004) Persistence of apoptotic cells without autoimmune disease or inflammation in CD14-/- mice. J Cell Biol 167(6):1161–1170

    Article  PubMed  CAS  Google Scholar 

  • Duncan JL, LaVail MM, Yasumura D et al (2003) An RCS-like retinal dystrophy phenotype in mer knockout mice. Invest Ophthalmol Vis Sci 44(2):826–838

    Article  PubMed  Google Scholar 

  • Duvall E, Wyllie AH, Morris RG (1985) Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 56(2):351–358

    PubMed  CAS  Google Scholar 

  • Eggleton P, Tenner AJ, Reid KB (2000) C1q receptors. Clin Exp Immunol 120(3):406–412

    Article  PubMed  CAS  Google Scholar 

  • Ehrenstein MR, Cook HT, Neuberger MS (2000) Deficiency in serum immunoglobulin (Ig)M predisposes to development of IgG autoantibodies. J Exp Med 191(7):1253–1258

    Article  PubMed  CAS  Google Scholar 

  • Eliceiri BP, Puente XS, Hood JD et al (2002) Src-mediated coupling of focal adhesion kinase to integrin alpha(v)beta5 in vascular endothelial growth factor signalling. J Cell Biol 157(1):149–160

    Article  PubMed  CAS  Google Scholar 

  • Enari M, Sakahira H, Yokoyama H et al (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391(6662):43–50

    Article  PubMed  CAS  Google Scholar 

  • Erwig LP, Henson PM (2008) Clearance of apoptotic cells by phagocytes. Cell Death Differ 15(2):243–250

    Article  PubMed  CAS  Google Scholar 

  • Eum HA, Cha YN, Lee SM (2007) Necrosis and apoptosis: sequence of liver damage following reperfusion after 60 min ischemia in rats. Biochem Biophys Res Commun 358(2):500–505

    Article  PubMed  CAS  Google Scholar 

  • Fadeel B (2004) Plasma membrane alterations during apoptosis: role in corpse clearance. Antioxid Redox Signal 6(2):269–275

    Article  PubMed  CAS  Google Scholar 

  • Fadok VA, Bratton DL, Guthrie L et al (2001) Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J Immunol 166(11):6847–6854

    PubMed  CAS  Google Scholar 

  • Fadok VA, Bratton DL, Rose DM et al (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405(6782):85–90

    Article  PubMed  CAS  Google Scholar 

  • Fadok VA, Voelker DR, Campbell PA et al (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148(7):2207–2216

    PubMed  CAS  Google Scholar 

  • Familian A, Zwart B, Huisman HG et al (2001) Chromatin-independent binding of serum amyloid P component to apoptotic cells. J Immunol 167(2):647–654

    PubMed  CAS  Google Scholar 

  • Fan X, Krahling S, Smith D et al (2004) Macrophage surface expression of annexins I and II in the phagocytosis of apoptotic lymphocytes. Mol Biol Cell 15(6):2863–2872

    Article  PubMed  CAS  Google Scholar 

  • Feng W, Yasumura D, Matthes MT et al (2002) Mertk triggers uptake of photoreceptor outer segments during phagocytosis by cultured retinal pigment epithelial cells. J Biol Chem 277(19):17016–17022

    Article  PubMed  CAS  Google Scholar 

  • Festjens N, Vanden Berghe T, Vandenabeele P (2006) Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757(9–10):1371–1387

    PubMed  CAS  Google Scholar 

  • Fiers W, Beyaert R, Declercq W et al (1999) More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene 18(54):7719–1730

    Article  PubMed  CAS  Google Scholar 

  • Fink SL, Cookson BT (2005) Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73(4):1907–1916

    Article  PubMed  CAS  Google Scholar 

  • Finnemann SC (2003) Focal adhesion kinase signalling promotes phagocytosis of integrin-bound photoreceptors. EMBO J 22(16):4143–4154

    Article  PubMed  CAS  Google Scholar 

  • Finnemann SC, Bonilha VL, Marmorstein A D et al (1997) Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalization. Proc Natl Acad Sci U S A 94(24):12932–12937

    Article  PubMed  CAS  Google Scholar 

  • Finnemann SC, Rodriguez-Boulan E (1999) Macrophage and retinal pigment epithelium phagocytosis: apoptotic cells and photoreceptors compete for alphavbeta3 and alphavbeta5 integrins, and protein kinase C regulates alphavbeta5 binding and cytoskeletal linkage. J Exp Med 190(6):861–874

    Article  PubMed  CAS  Google Scholar 

  • Flierman R, Daha MR (2007) The clearance of apoptotic cells by complement. Immunobiology 212(4–5):363–370

    Article  PubMed  CAS  Google Scholar 

  • Gaipl US, Beyer TD, Heyder P et al (2004) Cooperation between C1q and DNase I in the clearance of necrotic cell-derived chromatin. Arthritis Rheum 50(2):640–649

    Article  PubMed  CAS  Google Scholar 

  • Gaipl US, Kuenkele S, Voll RE et al (2001) Complement binding is an early feature of necrotic and a rather late event during apoptotic cell death. Cell Death Differ 8(4):327–334

    Article  PubMed  CAS  Google Scholar 

  • Gaipl US, Munoz LE, Rodel F et al (2007) Modulation of the immune system by dying cells and the phosphatidylserine-ligand annexin A5. Autoimmunity 40(4):254–259

    Article  PubMed  CAS  Google Scholar 

  • Gardai SJ, Bratton DL, Ogden CA et al (2006) Recognition ligands on apoptotic cells: a perspective. J Leukocyte Biol 79(5):896–903

    Article  PubMed  CAS  Google Scholar 

  • Gardai SJ, McPhillips KA, Frasch SC et al (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123(2):321–334

    Article  PubMed  CAS  Google Scholar 

  • Gershov D, Kim S, Brot N et al (2000) C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J Exp Med 192(9):1353–1364

    Article  PubMed  CAS  Google Scholar 

  • Godson C, Mitchell S, Harvey K et al (2000) Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol 164(4):1663–1667

    PubMed  CAS  Google Scholar 

  • Golstein P, Kroemer G (2007) Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32(1):37–43

    Article  PubMed  CAS  Google Scholar 

  • Gorgani NN, Smith BA, Kono DH et al (2002) Histidine-rich glycoprotein binds to DNA and Fc gamma RI and potentiates the ingestion of apoptotic cells by macrophages. J Immunol 169(9):4745–4751

    PubMed  Google Scholar 

  • Greenberg ME, Sun M, Zhang R et al (2006) Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J Exp Med 203(12):2613–2625

    Article  PubMed  CAS  Google Scholar 

  • Gujral JS, Farhood A, Jaeschke H (2003) Oncotic necrosis and caspase-dependent apoptosis during galactosamine-induced liver injury in rats. Toxicol Appl Pharmacol 190(1):37–46

    Article  PubMed  CAS  Google Scholar 

  • Gujral JS, Knight TR, Farhood A et al (2002) Mode of cell death after acetaminophen overdose in mice: apoptosis or oncotic necrosis? Toxicol Sci 67(2):322–328

    Article  PubMed  CAS  Google Scholar 

  • Hack CE, Wolbink GJ, Schalkwijk C et al (1997) A role for secretory phospholipase A2 and Creactive protein in the removal of injured cells. Immunol Today 18(3):111–115

    Article  PubMed  CAS  Google Scholar 

  • Hafizi S, Dahlback B (2006) Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J 273(23):5231–5244

    Article  PubMed  CAS  Google Scholar 

  • Hall MO, Obin MS, Heeb MJ et al (2005) Both protein S and Gas6 stimulate outer segment phagocytosis by cultured rat retinal pigment epithelial cells. Exp Eye Res 81(5):581–591

    Article  PubMed  CAS  Google Scholar 

  • Hall MO, Prieto AL, Obin MS et al (2001) Outer segment phagocytosis by cultured retinal pigment epithelial cells requires Gas6. Exp Eye Res 73(4):509–520

    Article  PubMed  CAS  Google Scholar 

  • Hamon Y, Broccardo C, Chambenoit O et al (2000) ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol 2(7):399–406

    Article  PubMed  CAS  Google Scholar 

  • Hanayama R, Nagata S (2005) Impaired involution of mammary glands in the absence of milk fat globule EGF factor 8. Proc Natl Acad Sci USA 102(46):16886–16891

    Article  PubMed  CAS  Google Scholar 

  • Hanayama R, Tanaka M, Miwa K et al (2002) Identification of a factor that links apoptotic cells to phagocytes. Nature 417(6885):182–187

    Article  PubMed  CAS  Google Scholar 

  • Hanayama R, Tanaka M, Miyasaka K et al (2004) Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304(5674):1147–1150

    Article  PubMed  CAS  Google Scholar 

  • Hart SP, Alexander KM, MacCall SM et al (2005) C-reactive protein does not opsonize early apoptotic human neutrophils, but binds only membrane-permeable late apoptotic cells and has no effect on their phagocytosis by macrophages. J Inflamm (Lond) 2:5.

    Article  CAS  Google Scholar 

  • Hicks PS, Saunero-Nava L, Du Clos TW et al (1992) Serum amyloid P component binds to histones and activates the classical complement pathway. J Immunol 149(11):3689–3694

    PubMed  CAS  Google Scholar 

  • Higami Y, Tsuchiya T, To K et al (2004) Expression of DNase gamma during Fas-independent apoptotic DNA fragmentation in rodent hepatocytes. Cell Tissue Res 316(3):403–407

    Article  PubMed  CAS  Google Scholar 

  • Hirt UA, Leist M (2003) Rapid, noninflammatory and PS-dependent phagocytic clearance of necrotic cells. Cell Death Differ 10(10):1156–1164

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann PR, deCathelineau AM, Ogden CA et al (2001) Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol 155(4):649–659

    Article  PubMed  CAS  Google Scholar 

  • Hughes J, Liu Y, Van Damme J et al (1997) Human glomerular mesangial cell phagocytosis of apoptotic neutrophils: mediation by a novel CD36-independent vitronectin receptor/thrombospondin recognition mechanism that is uncoupled from chemokine secretion. J Immunol 158(9):4389–4397

    PubMed  CAS  Google Scholar 

  • Ip WK, Lau YL (2004) Distinct maturation of, but not migration between, human monocytederived dendritic cells upon ingestion of apoptotic cells of early or late phases. J Immunol 173(1):189–196

    PubMed  CAS  Google Scholar 

  • Jacob M, Mannherz HG, Napirei M (2007) Chromatin breakdown by deoxyribonuclease1 promotes acetaminophen-induced liver necrosis: an ultrastructural and histochemical study on male CD-1 mice. Histochem Cell Biol 128(1):19–33

    Article  PubMed  CAS  Google Scholar 

  • Jaeschke H, Lemasters JJ (2003) Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 125(4):1246–1257

    Article  PubMed  CAS  Google Scholar 

  • Jehle AW, Gardai SJ, Li S et al (2006) ATP-binding cassette transporter A7 enhances phagocytosis of apoptotic cells and associated ERK signalling in macrophages. J Cell Biol 174(4):547–556

    Article  PubMed  CAS  Google Scholar 

  • Jensen ML, Honore C, Hummelshoj T et al (2007) Ficolin-2 recognizes DNA and participates in the clearance of dying host cells. Mol Immunol 44(5):856–865

    Article  PubMed  CAS  Google Scholar 

  • Jiang H, Cooper B, Robey FA et al (1992) DNA binds and activates complement via residues 14-26 of the human C1q A chain. J Biol Chem 267(35):25597–25601

    PubMed  CAS  Google Scholar 

  • Jones AL, Hulett MD, Parish CR (2005a) Histidine-rich glycoprotein: A novel adaptor protein in plasma that modulates the immune, vascular and coagulation systems. Immunol Cell Biol 83(2):106–118

    Article  CAS  Google Scholar 

  • Jones AL, Poon IK, Hulett MD et al (2005b) Histidine-rich glycoprotein specifically binds to necrotic cells via its amino-terminal domain and facilitates necrotic cell phagocytosis. J Biol Chem 280(42):35733–35741

    Article  CAS  Google Scholar 

  • Kacani L, Wurm M, Schwentner I et al (2005) Maturation of dendritic cells in the presence of living, apoptotic and necrotic tumour cells derived from squamous cell carcinoma of head and neck. Oral Oncol 41(1):17–24

    Article  PubMed  Google Scholar 

  • Kagan VE, Borisenko GG, Serinkan BF et al (2003) Appetizing rancidity of apoptotic cells for macrophages: oxidation, externalization, and recognition of phosphatidylserine. Am J Physiol Lung Cell Mol Physiol 285(1):L1–17

    PubMed  CAS  Google Scholar 

  • Kaplan MH, Volanakis JE (1974) Interaction of C-reactive protein complexes with the complement system. I. Consumption of human complement associated with the reaction of C-reactive protein with pneumococcal C-polysaccharide and with the choline phosphatides, lecithin and sphingomyelin. J Immunol 112(6):2135–2147

    PubMed  CAS  Google Scholar 

  • Kawane K, Fukuyama H, Kondoh G et al (2001) Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver. Science 292(5521):1546–1549

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki Y, Nakagawa A, Nagaosa K et al (2002) Phosphatidylserine binding of class B scavenger receptor type I, a phagocytosis receptor of testicular sertoli cells. J Biol Chem 277(30):27559–27566

    Article  PubMed  CAS  Google Scholar 

  • Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257

    PubMed  CAS  Google Scholar 

  • Khandelwal S, van Rooijen N, Saxena RK (2007) Reduced expression of CD47 during murine red blood cell (RBC) senescence and its role in RBC clearance from the circulation. Transfusion 47(9):1725–1732

    Article  PubMed  Google Scholar 

  • Kim SJ, Gershov D, Ma X et al (2002) I-PLA(2) activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J Exp Med 196(5):655–665

    Article  PubMed  CAS  Google Scholar 

  • Kinchen JM, Cabello J, Klingele D et al (2005) Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans. Nature 434(7029):93–99

    Article  PubMed  CAS  Google Scholar 

  • Korb LC, Ahearn JM (1997) C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J Immunol 158(10):4525–4528

    PubMed  CAS  Google Scholar 

  • Korkmaz B, Moreau T, Gauthier F (2008) Neutrophil elastase, proteinase 3 and cathepsin G: Physicochemical properties, activity and physiopathological functions. Biochimie 90(2):227–242

    Article  PubMed  CAS  Google Scholar 

  • Krieser RJ, MacLea KS, Longnecker DS et al (2002) Deoxyribonuclease IIalpha is required during the phagocytic phase of apoptosis and its loss causes perinatal lethality. Cell Death Differ 9(9):956–962

    Article  PubMed  CAS  Google Scholar 

  • Krysko DV, Brouckaert G, Kalai M et al (2003) Mechanisms of internalization of apoptotic and necrotic L929 cells by a macrophage cell line studied by electron microscopy. J Morphol 258(3):336–345

    Article  PubMed  Google Scholar 

  • Krysko DV, D’Herde K, Vandenabeele P (2006a) Clearance of apoptotic and necrotic cells and its immunological consequences. Apoptosis 11(10):1709–1726

    Article  Google Scholar 

  • Krysko DV, Denecker G, Festjens N et al (2006b) Macrophages use different internalization mechanisms to clear apoptotic and necrotic cells. Cell Death Differ 13(12):2011–2022

    Article  CAS  Google Scholar 

  • Krysko O, De Ridder L, Cornelissen M (2004) Phosphatidylserine exposure during early primary necrosis (oncosis) in JB6 cells as evidenced by immunogold labeling technique. Apoptosis 9(4):495–500

    Article  PubMed  CAS  Google Scholar 

  • Kuraya M, Ming Z, Liu X et al (2005) Specific binding of L-ficolin and H-ficolin to apoptotic cells leads to complement activation. Immunobiology 209(9):689–697

    Article  PubMed  CAS  Google Scholar 

  • Lauber K, Blumenthal SG, Waibel M et al (2004) Clearance of apoptotic cells: getting rid of the corpses. Mol Cell 14(3):277–287

    Article  PubMed  CAS  Google Scholar 

  • Lauber K, Bohn E, Krober SM et al (2003) Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113(6):717–730

    Article  PubMed  CAS  Google Scholar 

  • Law RH, Zhang Q, McGowan S et al (2006) An overview of the serpin superfamily. Genome Biol 7(5):216

    Article  PubMed  CAS  Google Scholar 

  • Lecoeur H, Prevost MC, Gougeon ML (2001) Oncosis is associated with exposure of phosphatidylserine residues on the outside layer of the plasma membrane: a reconsideration of the specificity of the annexin V/propidium iodide assay. Cytometry 44(1):65–72

    Article  PubMed  CAS  Google Scholar 

  • Lee KD, Pitas RE, Papahadjopoulos D (1992) Evidence that the scavenger receptor is not involved in the uptake of negatively charged liposomes by cells. Biochim Biophys Acta 1111(1):1–6

    Article  PubMed  CAS  Google Scholar 

  • Leverrier Y, Lorenzi R, Blundell MP et al (2001) Cutting edge: the Wiskott-Aldrich syndrome protein is required for efficient phagocytosis of apoptotic cells. J Immunol 166(8):4831–4834

    PubMed  CAS  Google Scholar 

  • Leverrier Y, Ridley AJ (2001) Requirement for Rho GTPases and PI 3-kinases during apoptotic cell phagocytosis by macrophages. Curr Biol 11(3):195–199

    Article  PubMed  CAS  Google Scholar 

  • Li LY, Luo X, Wang X (2001) Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412(6842):95–99

    Article  PubMed  CAS  Google Scholar 

  • Linder E, Helin H, Chang CM et al (1983) Complement-mediated binding of monocytes to intermediate filaments in vitro. Am J Pathol 112(3):267–277

    PubMed  CAS  Google Scholar 

  • Liu X, Li P, Widlak P et al (1998) The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc Natl Acad Sci U S A 95(15):8461–8466

    Article  PubMed  CAS  Google Scholar 

  • Luciani MF, Chimini G (1996) The ATP binding cassette transporter ABC1, is required for the engulfment of corpses generated by apoptotic cell death. EMBO J 15(2):226–235

    PubMed  CAS  Google Scholar 

  • Ma K, Simantov R, Zhang JC et al (2000) High affinity binding of beta 2-glycoprotein I to human endothelial cells is mediated by annexin II. J Biol Chem 275(20):15541–15548

    Article  PubMed  CAS  Google Scholar 

  • Maiuri MC, Zalckvar E, Kimchi A et al (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8(9):741–752

    Article  PubMed  CAS  Google Scholar 

  • Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146(1):3–15

    PubMed  CAS  Google Scholar 

  • Malhotra R, Thiel S, Reid KB et al (1990) Human leukocyte C1q receptor binds other soluble proteins with collagen domains. J Exp Med 172(3):955–959

    Article  PubMed  CAS  Google Scholar 

  • Mandal D, Mazumder A, Das P et al (2005) Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J Biol Chem 280(47):39460–39467

    Article  PubMed  CAS  Google Scholar 

  • Mannherz HG, Mach M, Malicka-Blaszkiewicz M et al (2007) Lamellipodial and amoeboid cell locomotion: The role of actin-cycling and bleb formation. Biophysical Reviews and Letters 2(1):5–22

    Article  CAS  Google Scholar 

  • Martin SJ, Reutelingsperger CP, McGahon AJ et al (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(5):1545–1556

    Article  PubMed  CAS  Google Scholar 

  • Mevorach D, Mascarenhas JO, Gershov D et al (1998) Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med 188(12):2313–2320

    Article  PubMed  CAS  Google Scholar 

  • Mitchell S, Thomas G, Harvey K et al (2002) Lipoxins, aspirin-triggered epi-lipoxins, lipoxin stable analogues, and the resolution of inflammation: stimulation of macrophage phagocytosis of apoptotic neutrophils in vivo. J Am Soc Nephrol 13(10):2497–2507

    Article  PubMed  CAS  Google Scholar 

  • Miyanishi M, Tada K, Koike M et al (2007) Identification of Tim4 as a phosphatidylserine receptor. Nature 450(7168):435–439

    Article  PubMed  CAS  Google Scholar 

  • Moffatt OD, Devitt A, Bell ED et al (1999) Macrophage recognition of ICAM-3 on apoptotic leukocytes. J Immunol 162(11):6800–6810

    PubMed  CAS  Google Scholar 

  • Mold C, Baca R, Du Clos TW (2002) Serum amyloid P component and C-reactive protein opsonize apoptotic cells for phagocytosis through Fcgamma receptors. J Autoimmun 19(3):147–154

    Article  PubMed  Google Scholar 

  • Moore KJ, Freeman MW (2006) Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler Thromb Vasc Biol 26(8):1702–1711

    Article  PubMed  CAS  Google Scholar 

  • Murphy JE, Tedbury PR, Homer-Vanniasinkam S et al (2005) Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis 182(1):1–15

    Article  PubMed  CAS  Google Scholar 

  • Nagata K, Ohashi K, Nakano T et al (1996) Identification of the product of growth arrest-specific gene 6 as a common ligand for Axl, Sky, and Mer receptor tyrosine kinases. J Biol Chem 271(47):30022–30027

    Article  PubMed  CAS  Google Scholar 

  • Nakano T, Ishimoto Y, Kishino J et al (1997) Cell adhesion to phosphatidylserine mediated by a product of growth arrest-specific gene 6. J Biol Chem 272(47):29411–29414

    Article  PubMed  CAS  Google Scholar 

  • Nandrot EF, Anand M, Almeida D et al (2007) Essential role for MFG-E8 as ligand for alphavbeta5 integrin in diurnal retinal phagocytosis. Proc Natl Acad Sci U S A 104(29):12005–12010

    Article  PubMed  CAS  Google Scholar 

  • Nandrot EF, Kim Y, Brodie SE et al (2004) Loss of synchronized retinal phagocytosis and agerelated blindness in mice lacking alphavbeta5 integrin. J Exp Med 200(12):1539–1545

    Article  PubMed  CAS  Google Scholar 

  • Napirei M, Basnakian AG, Apostolov EO et al (2006a) Deoxyribonuclease 1 aggravates acetaminophen-induced liver necrosis in male CD-1 mice. Hepatology 43(2):297–305

    Article  CAS  Google Scholar 

  • Napirei M, Gultekin A, Kloeckl T et al (2006b) Systemic lupus-erythematosus: Deoxyribonuclease 1 in necrotic chromatin disposal. Int J Biochem Cell Biol 38(3):297–306

    Article  CAS  Google Scholar 

  • Napirei M, Karsunky H, Zevnik B et al (2000) Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat Genet 25(2):177–181

    Article  PubMed  CAS  Google Scholar 

  • Napirei M, Wulf S, Eulitz D et al (2005) Comparative characterization of rat deoxyribonuclease 1 (Dnase1) and murine deoxyribonuclease 1-like 3 (Dnase113). Biochem J 389(Pt 2):355–364

    PubMed  CAS  Google Scholar 

  • Napirei M, Wulf S, Mannherz HG (2004) Chromatin breakdown during necrosis by serum Dnase1 and the plasminogen system. Arthritis Rheum 50(6):1873–1883

    Article  PubMed  CAS  Google Scholar 

  • Nauta AJ, Raaschou-Jensen N, Roos A et al (2003) Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur J Immunol 33(10):2853–2863

    Article  PubMed  CAS  Google Scholar 

  • Nimpf J, Bevers EM, Bomans P et al (1986) Prothrombinase activity of human platelets is inhibited by beta 2-glycoprotein-I. Biochim Biophys Acta 884(1):142–149

    PubMed  CAS  Google Scholar 

  • Ogden CA, deCathelineau A, Hoffmann PR et al (2001) C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 194(6):781–795

    Article  PubMed  CAS  Google Scholar 

  • Oka K, Sawamura T, Kikuta K et al (1998) Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc Natl Acad Sci U S A 95(16):9535–9540

    Article  PubMed  CAS  Google Scholar 

  • Oldenborg PA, Zheleznyak A, Fang YF et al (2000) Role of CD47 as a marker of self on red blood cells. Science 288(5473):2051–2054

    Article  PubMed  CAS  Google Scholar 

  • Palaniyar N, Nadesalingam J, Clark H et al (2004) Nucleic acid is a novel ligand for innate, immune pattern recognition collectins surfactant proteins A and D and mannose-binding lectin. J Biol Chem 279(31):32728–32736

    Article  PubMed  CAS  Google Scholar 

  • Patel VA, Longacre A, Hsiao K et al (2006) Apoptotic cells, at all stages of the death process, trigger characteristic signalling events that are divergent from and dominant over those triggered by necrotic cells: Implications for the delayed clearance model of autoimmunity. J Biol Chem 281(8):4663–4670

    Article  PubMed  CAS  Google Scholar 

  • Peng Y, Kowalewski R, Kim S et al (2005) The role of IgM antibodies in the recognition and clearance of apoptotic cells. Mol Immunol 42(7):781–787

    Article  PubMed  CAS  Google Scholar 

  • Pepys MB, Booth SE, Tennent GA et al (1994) Binding of pentraxins to different nuclear structures: C-reactive protein binds to small nuclear ribonucleoprotein particles, serum amyloid P component binds to chromatin and nucleoli. Clin Exp Immunol 97(1):152–157

    Article  PubMed  CAS  Google Scholar 

  • Pepys MB, Butler PJ (1987) Serum amyloid P component is the major calcium-dependent specific DNA binding protein of the serum. Biochem Biophys Res Commun 148(1):308–313

    Article  PubMed  CAS  Google Scholar 

  • Pisetsky DS, Fairhurst AM (2007) The origin of extracellular DNA during the clearance of dead and dying cells. Autoimmunity 40(4):281–284

    Article  PubMed  CAS  Google Scholar 

  • Platt N, Suzuki H, Kodama T et al (2000) Apoptotic thymocyte clearance in scavenger receptor class A-deficient mice is apparently normal. J Immunol 164(9):4861–4867

    PubMed  CAS  Google Scholar 

  • Podor TJ, Joshua P, Butcher M et al (1992) Accumulation of type 1 plasminogen activator inhibitor and vitronectin at sites of cellular necrosis and inflammation. Ann N Y Acad Sci 667:173–177

    Article  PubMed  CAS  Google Scholar 

  • Proskuryakov SY, Gabai VL, Konoplyannikov AG et al (2005) Immunology of apoptosis and necrosis. Biochemistry (Mosc) 70(12):1310–1320

    Article  CAS  Google Scholar 

  • Pugin J, Heumann ID, Tomasz A et al (1994) CD14 is a pattern recognition receptor. Immunity 1(6):509–516

    Article  PubMed  CAS  Google Scholar 

  • Quartier P, Potter PK, Ehrenstein MR et al (2005) Predominant role of IgM-dependent activation of the classical pathway in the clearance of dying cells by murine bone marrow-derived macrophages in vitro. Eur J Immunol 35(1):252–260

    Article  PubMed  CAS  Google Scholar 

  • Raucci A, Palumbo R, Bianchi ME (2007) HMGB1: a signal of necrosis. Autoimmunity 40(4):285–289

    Article  PubMed  CAS  Google Scholar 

  • Rauch F, Prud’homme J, Arabian A et al (2000) Heart, brain, and body wall defects in mice lacking calreticulin. Exp Cell Res 256(1):105–111

    Article  PubMed  CAS  Google Scholar 

  • Reddy SM, Hsiao KH, Abernethy VE et al (2002) Phagocytosis of apoptotic cells by macrophages induces novel signalling events leading to cytokine-independent survival and inhibition of proliferation: activation of Akt and inhibition of extracellular signal-regulated kinases 1 and 2. J Immunol 169(2):702–713

    PubMed  CAS  Google Scholar 

  • Ren Y, Silverstein RL, Allen J et al (1995) CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J Exp Med 181(5):1857–1862

    Article  PubMed  CAS  Google Scholar 

  • Reutelingsperger CP, van Heerde WL (1997) Annexin V, the regulator of phosphatidylserine-catalyzed inflammation and coagulation during apoptosis. Cell Mol Life Sci 53(6):527–532

    Article  PubMed  CAS  Google Scholar 

  • Rigotti A, Acton SL, Krieger M (1995) The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J Biol Chem 270(27):16221–16224

    Article  PubMed  CAS  Google Scholar 

  • Robey FA, Jones KD, Tanaka T et al (1984) Binding of C-reactive protein to chromatin and nucleosome core particles. A possible physiological role of C-reactive protein. J Biol Chem 259(11):7311–7316

    PubMed  CAS  Google Scholar 

  • Rovere-Querini P, Capobianco A, Scaffidi P et al (2004) HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 5(8):825–830

    Article  PubMed  CAS  Google Scholar 

  • Rovere P, Peri G, Fazzini F et al (2000) The long pentraxin PTX3 binds to apoptotic cells and regulates their clearance by antigen-presenting dendritic cells. Blood 96(13):4300–4306

    PubMed  CAS  Google Scholar 

  • Russell L, Waring P, Beaver JP (1998) Increased cell surface exposure of fucose residues is a late event in apoptosis. Biochem Biophys Res Commun 250(2):449–453

    Article  PubMed  CAS  Google Scholar 

  • Ryeom SW, Sparrow JR, Silverstein RL (1996) CD36 participates in the phagocytosis of rod outer segments by retinal pigment epithelium. J Cell Sci 109 (Pt 2):387–395./bib>

    PubMed  CAS  Google Scholar 

  • Sauter B, Albert ML, Francisco L et al (2000) Consequences of cell death: exposure to necrotic tumour cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med 191(3):423–434

    Article  PubMed  CAS  Google Scholar 

  • Savill J, Hogg N, Ren Y et al (1992) Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest 90(4):1513–1522

    Article  PubMed  CAS  Google Scholar 

  • Scannell M, Flanagan MB, deStefani A et al (2007) Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J Immunol 178(7):4595–4605

    PubMed  CAS  Google Scholar 

  • Schagat TL, Wofford JA, Wright JR (2001) Surfactant protein A enhances alveolar macrophage phagocytosis of apoptotic neutrophils. J Immunol 166(4):2727–2733

    PubMed  CAS  Google Scholar 

  • Schroit AJ, Madsen JW, Tanaka Y (1985) In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J Biol Chem 260(8):5131–5138

    PubMed  CAS  Google Scholar 

  • Scott RS, McMahon EJ, Pop SM et al (2001) Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411(6834):207–211

    Article  PubMed  CAS  Google Scholar 

  • Shi Y, Evans JE, Rock KL (2003) Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425(6957):516–521

    Article  PubMed  CAS  Google Scholar 

  • Shiokawa D, Ohyama H, Yamada T et al (1994) Identification of an endonuclease responsible for apoptosis in rat thymocytes. Eur J Biochem 226(1):23–30

    Article  PubMed  CAS  Google Scholar 

  • Shiratsuchi A, Kawasaki Y, Ikemoto M et al (1999) Role of class B scavenger receptor type I in phagocytosis of apoptotic rat spermatogenic cells by Sertoli cells. J Biol Chem 274(9):5901–5908

    Article  PubMed  CAS  Google Scholar 

  • Smith AJ, Schlichtenbrede FC, Tschernutter M et al (2003) AAV-Mediated gene transfer slows photoreceptor loss in the RCS rat model of retinitis pigmentosa. Mol Ther 8(2):188–195

    Article  PubMed  CAS  Google Scholar 

  • Stein MP, Mold C, Du Clos TW (2000) C-reactive protein binding to murine leukocytes requires Fc gamma receptors. J Immunol 164(3):1514–1520

    PubMed  CAS  Google Scholar 

  • Stern M, Savill J, Haslett C (1996) Human monocyte-derived macrophage phagocytosis of senescent eosinophils undergoing apoptosis. Mediation by alpha v beta 3/CD36/thrombospondin recognition mechanism and lack of phlogistic response. Am J Pathol 149(3):911–921

    PubMed  CAS  Google Scholar 

  • Stitt TN, Conn G, Gore M et al (1995) The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell 80(4):661–670

    Article  PubMed  CAS  Google Scholar 

  • Stuart LM, Takahashi K, Shi L et al (2005) Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J Immunol 174(6):3220–3226

    PubMed  CAS  Google Scholar 

  • Tada K, Tanaka M, Hanayama R et al (2003) Tethering of apoptotic cells to phagocytes through binding of CD47 to Src homology 2 domain-bearing protein tyrosine phosphatase substrate-1. J Immunol 171(11):5718–5726

    PubMed  CAS  Google Scholar 

  • Takizawa F, Tsuji S, Nagasawa S (1996) Enhancement of macrophage phagocytosis upon iC3b deposition on apoptotic cells. FEBS Lett 397(2–3):269–272

    Article  PubMed  CAS  Google Scholar 

  • Terpstra V, Kondratenko N, Steinberg D (1997) Macrophages lacking scavenger receptor A show a decrease in binding and uptake of acetylated low-density lipoprotein and of apoptotic thymocytes, but not of oxidatively damaged red blood cells. Proc Natl Acad Sci U S A 94(15):8127–8131

    Article  PubMed  CAS  Google Scholar 

  • Theiss C, Mazur A, Meller K et al (2007) Changes in gap junction organization and decreased coupling during induced apoptosis in lens epithelial and NIH-3T3 cells. Exp Cell Res 313(1):38–52

    Article  PubMed  CAS  Google Scholar 

  • Van Cruchten S, Van Den Broeck W (2002) Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat Histol Embryol 31(4):214–223

    Article  PubMed  Google Scholar 

  • van Rossum AP, Fazzini F, Limburg PC et al (2004) The prototypic tissue pentraxin PTX3, in contrast to the short pentraxin serum amyloid P, inhibits phagocytosis of late apoptotic neutrophils by macrophages. Arthritis Rheum 50(8):2667–2674

    Article  PubMed  CAS  Google Scholar 

  • Vandivier RW, Fadok VA, Hoffmann PR et al (2002a) Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J Clin Invest 109(5):661–670

    CAS  Google Scholar 

  • Vandivier RW, Ogden CA, Fadok VA et al (2002b) Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J Immunol 169(7):3978–3986

    CAS  Google Scholar 

  • Verbovetski I, Bychkov H, Trahtemberg U et al (2002) Opsonization of apoptotic cells by autologous iC3b facilitates clearance by immature dendritic cells, down-regulates DR and CD86, and up-regulates CC chemokine receptor 7. J Exp Med 196(12):1553–1561

    Article  PubMed  CAS  Google Scholar 

  • Volanakis JE, Wirtz KW (1979) Interaction of C-reactive protein with artificial phosphatidylcholine bilayers. Nature 281(5727):155–157

    Article  PubMed  CAS  Google Scholar 

  • Wang WZ, Fang XH, Stephenson LL et al (2007) Ischemia/reperfusion-induced necrosis and apoptosis in the cells isolated from rat skeletal muscle. J Orthop Res

    Google Scholar 

  • Wolf A, Schmitz C Bottger A (2007) Changing story of the receptor for phosphatidylserinedependent clearance of apoptotic cells. EMBO Rep 8(5):465–469

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Singh S, Georgescu MM et al (2005) A role for Mer tyrosine kinase in alphavbeta5 integrinmediated phagocytosis of apoptotic cells. J Cell Sci 118(Pt 3):539–553

    Article  PubMed  CAS  Google Scholar 

  • Wu YC, Horvitz HR (1998) The C. elegans cell corpse engulfment gene ced-7 encodes a protein similar to ABC transporters. Cell 93(6):951–960

    Article  PubMed  CAS  Google Scholar 

  • Yoshida H, Kawane K, Koike M et al (2005) Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 437(7059):754–758

    Article  PubMed  CAS  Google Scholar 

  • Zakeri Z, Bursch W, Tenniswood M et al (1995) Cell death: programmed, apoptosis, necrosis, or other? Cell Death Differ 2(2):87–96

    PubMed  CAS  Google Scholar 

  • Zhou Z, Hartwieg E, Horvitz HR (2001) CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104(1):43–56

    Article  PubMed  CAS  Google Scholar 

  • Zwart B, Ciurana C, Rensink I et al (2004) Complement activation by apoptotic cells occurs predominantly via IgM and is limited to late apoptotic (secondary necrotic) cells. Autoimmunity 37(2):95–102

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Embryology, Ruhr-University Bochum, Universitätsstraße 150, 44801, Bochum, Germany

    Markus Napirei (Medical Faculty) & Hans Georg Mannherz (Medical Faculty)

Authors
  1. Markus Napirei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hans Georg Mannherz
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. VIB Department for Molecular Biomedical Research, VIB and Ghent University, Technologiepark 927, 9052, Ghent, Belgium

    Dmitri V. Krysko M.D., Ph.D.  & Peter Vandenabeele Ph.D.  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Napirei, M., Mannherz, H.G. (2009). Molecules Involved in Recognition and Clearance of Apoptotic/Necrotic Cells and Cell Debris. In: Krysko, D.V., Vandenabeele, P. (eds) Phagocytosis of Dying Cells: From Molecular Mechanisms to Human Diseases. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-9293-0_4

Download citation

Publish with us

Policies and ethics

Search

Navigation