Home LiteratureArticle Details
PMID: 15126686 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Atypical antiinflammatory activation of microglia induced by apoptotic neurons: possible role of phosphatidylserine-phosphatidylserine receptor interaction.

Molecular neurobiology ·Vol. 29 ·No. 2 ·2004-04-00 ·Pages 197-212

De Simone R, Ajmone-Cat MA, Minghetti L

Abstract

In the central nervous system (CNS), apoptosis plays an important role during development and is a primary pathogenic mechanism in several adult neurodegenerative diseases. A main feature of apoptotic cell death is the efficient and fast removal of dying cells by macrophages and nonprofessional phagocytes, without eliciting inflammation in the surrounding tissue. Apoptotic cells undergo several membrane changes, including the externalization of so-called "eat me" signals whose cognate receptors are present on professional phagocytes. Among these signals, the aminophospholipid phosphatidylserine (PS) appears to have a crucial and unique role in preventing the classical pro-inflammatory activation of macrophages, thus ensuring the silent and safe removal of apoptotic cells. Although extensively studied in the peripheral organs, the process of recognition and removal of apoptotic cells in the brain has only recently begun to be unraveled. Here, we summarize the evidence suggesting that upon interaction with PS-expressing apoptotic neurons, microglia may no longer promote the inflammatory cascade, but rather facilitate the elimination of damaged neurons through antiinflammatory and neuroprotective functions. We propose that the anti-inflammatory microglial phenotype induced through the activation of the specific PS receptor (PtdSerR), expressed by resting and activated microglial cells, could be relevant to the final outcome of neurodegenerative diseases, in which apoptosis seems to play a crucial role.

MeSH Terms
Animals Apoptosis/physiology Humans Inflammation/metabolism,pathology,prevention & control Microglia/metabolism Neurons/pathology,physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
De Simone Roberta
Department of Cell Biology and Neurosciences, Istituto Superiore di Sanità, Viale Regina Elena 299, 00161 Italy.
Ajmone-Cat Maria Antonietta
Minghetti Luisa
References (92)
92 references, click to expand
  1. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function.
    J Neurosci. 1996 Apr 15;16(8):2508-21 PMID: 8786427
  2. Microglial-neuronal interactions in synaptic damage and recovery.
    J Neurosci Res. 1999 Oct 1;58(1):191-201 PMID: 10491582
  3. Phagocytic clearance of apoptotic neurons by Microglia/Brain macrophages in vitro: involvement of lectin-, integrin-, and phosphatidylserine-mediated recognition.
    J Neurochem. 2000 Sep;75(3):1060-70 PMID: 10936187
  4. Clearance of apoptotic photoreceptors: elimination of apoptotic debris into the subretinal space and macrophage-mediated phagocytosis via phosphatidylserine receptor and integrin alphavbeta3.
    Am J Pathol. 2003 Jun;162(6):1869-79 PMID: 12759244
  5. The absence of reactive astrocytosis is indicative of a unique inflammatory process in Parkinson's disease.
    Neuroscience. 2000;95(2):425-32 PMID: 10658622
  6. Structural and functional evidence for microglial expression of C1qR(P), the C1q receptor that enhances phagocytosis.
    J Leukoc Biol. 2000 Jan;67(1):109-16 PMID: 10648005
  7. A role for oxidative stress in apoptosis: oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis.
    J Immunol. 2002 Jul 1;169(1):487-99 PMID: 12077280
  8. Phagocytosis and clearance of apoptotic cells is mediated by MER.
    Nature. 2001 May 10;411(6834):207-11 PMID: 11346799
  9. If phosphatidylserine is the death knell, a new phosphatidylserine-specific receptor is the bellringer.
    Cell Death Differ. 2001 Jun;8(6):582-7 PMID: 11536008
  10. Neuronal apoptosis in Creutzfeldt-Jakob disease.
    J Neuropathol Exp Neurol. 1999 Apr;58(4):321-8 PMID: 10218627
  11. Phosphatidylserine-dependent phagocytosis of apoptotic glioma cells by normal human microglia, astrocytes, and glioma cells.
    Neuro Oncol. 2000 Jul;2(3):174-83 PMID: 11302338
  12. Requirement for Rho GTPases and PI 3-kinases during apoptotic cell phagocytosis by macrophages.
    Curr Biol. 2001 Feb 6;11(3):195-9 PMID: 11231156
  13. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes.
    Nature. 1998 Jan 15;391(6664):281-5 PMID: 9440691
  14. Microglial cells protect cerebellar granule neurons from apoptosis: evidence for reciprocal signaling.
    Glia. 2001 Dec;36(3):271-80 PMID: 11746765
  15. CD14-dependent clearance of apoptotic cells: relevance to the immune system.
    Curr Opin Immunol. 2000 Feb;12(1):27-34 PMID: 10679400
  16. Metabolism and functions of phosphatidylserine in mammalian brain.
    Neurochem Res. 2003 Feb;28(2):195-214 PMID: 12608694
  17. Activation of protein kinase C beta II by the stereo-specific phosphatidylserine receptor is required for phagocytosis of apoptotic thymocytes by resident murine tissue macrophages.
    J Biol Chem. 2002 Sep 27;277(39):35906-14 PMID: 12114511
  18. Fibronectin and laminin regulate the in vitro differentiation of microglial cells.
    Neuroscience. 1991;45(3):513-27 PMID: 1663599
  19. Functions of transforming growth factor-beta isoforms in the nervous system. Cues based on localization and experimental in vitro and in vivo evidence.
    Eur J Biochem. 2000 Dec;267(24):6972-5 PMID: 11106405
  20. A blast from the past: clearance of apoptotic cells regulates immune responses.
    Nat Rev Immunol. 2002 Dec;2(12):965-75 PMID: 12461569
  21. Transforming growth factor beta1, the dominant cytokine in murine prion disease: influence on inflammatory cytokine synthesis and alteration of vascular extracellular matrix.
    Neuropathol Appl Neurobiol. 2002 Apr;28(2):107-19 PMID: 11972797
  22. The p38 signal transduction pathway: activation and function.
    Cell Signal. 2000 Jan;12(1):1-13 PMID: 10676842
  23. Phagocytosis of apoptotic inflammatory cells by microglia and its therapeutic implications: termination of CNS autoimmune inflammation and modulation by interferon-beta.
    Glia. 2003 Sep;43(3):231-42 PMID: 12898702
  24. Reciprocal interactions between microglia and neurons: from survival to neuropathology.
    Rev Neurosci. 2002;13(3):221-42 PMID: 12405226
  25. Prostaglandin E(2) induces caspase-dependent apoptosis in rat cortical cells.
    Neurosci Lett. 2002 Jan 11;317(2):61-4 PMID: 11755240
  26. Regulation of prostanoid synthesis in microglial cells and effects of prostaglandin E2 on microglial functions.
    Biochimie. 1998 Nov;80(11):899-904 PMID: 9893949
  27. Physiological actions and clinical applications of transforming growth factor-beta (TGF-beta).
    Growth Factors. 1993;8(1):1-9 PMID: 8448037
  28. beta1 and beta2 integrins activate different signalling pathways in monocytes.
    Biochem J. 2002 Apr 15;363(Pt 2):273-80 PMID: 11931654
  29. Atypical inflammation in the central nervous system in prion disease.
    Curr Opin Neurol. 2002 Jun;15(3):349-54 PMID: 12045736
  30. Cell adhesion to phosphatidylserine mediated by a product of growth arrest-specific gene 6.
    J Biol Chem. 1997 Nov 21;272(47):29411-4 PMID: 9367994
  31. Macrophages and inflammation in the central nervous system.
    Trends Neurosci. 1993 Jul;16(7):268-73 PMID: 7689770
  32. Neuroprotective effects of prostaglandin E2 or cAMP against microglial and neuronal free radical mediated toxicity associated with inflammation.
    J Neurosci Res. 2002 Oct 1;70(1):97-107 PMID: 12237868
  33. Effects of phosphatidylserine on p38 mitogen activated protein kinase, cyclic AMP responding element binding protein and nuclear factor-kappaB activation in resting and activated microglial cells.
    J Neurochem. 2003 Jan;84(2):413-6 PMID: 12559004
  34. Recognition and phagocytosis of apoptotic T cells by resident murine tissue macrophages require multiple signal transduction events.
    J Leukoc Biol. 2002 May;71(5):881-9 PMID: 11994514
  35. Apoptotic cell removal.
    Curr Biol. 2001 Oct 2;11(19):R795-805 PMID: 11591341
  36. Microglial activation varies in different models of Creutzfeldt-Jakob disease.
    J Virol. 1999 Jun;73(6):5089-97 PMID: 10233972
  37. Activators and target genes of Rel/NF-kappaB transcription factors.
    Oncogene. 1999 Nov 22;18(49):6853-66 PMID: 10602461
  38. Apoptotic PC12 cells exposing phosphatidylserine promote the production of anti-inflammatory and neuroprotective molecules by microglial cells.
    J Neuropathol Exp Neurol. 2003 Feb;62(2):208-16 PMID: 12578230
  39. Mechanisms of prostaglandin E2-induced interleukin-6 release in astrocytes: possible involvement of EP4-like receptors, p38 mitogen-activated protein kinase and protein kinase C.
    J Neurochem. 2001 Dec;79(5):950-8 PMID: 11739606
  40. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells.
    J Cell Biol. 2001 Nov 12;155(4):649-59 PMID: 11706053
  41. Externalization of phosphatidylserine may not be an early signal of apoptosis in neuronal cells, but only the phosphatidylserine-displaying apoptotic cells are phagocytosed by microglia.
    J Neurochem. 1998 Nov;71(5):1854-64 PMID: 9798909
  42. Direct temporal analysis of apoptosis induction in living adherent neurons.
    J Histochem Cytochem. 1999 May;47(5):661-72 PMID: 10219058
  43. Increased expression of TGF-beta 1 in brain tissue after ischemic stroke in humans.
    Stroke. 1996 May;27(5):852-7 PMID: 8623105
  44. Expression of phosphatidylserine receptor and down-regulation of pro-inflammatory molecule production by its natural ligand in rat microglial cultures.
    J Neuropathol Exp Neurol. 2002 Mar;61(3):237-44 PMID: 11895038
  45. Cellular signaling roles of TGF beta, TNF alpha and beta APP in brain injury responses and Alzheimer's disease.
    Brain Res Brain Res Rev. 1997 Feb;23(1-2):47-61 PMID: 9063586
  46. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF.
    J Clin Invest. 1998 Feb 15;101(4):890-8 PMID: 9466984
  47. Mannose receptor is present in a functional state in rat microglial cells.
    J Neurosci Res. 1999 Nov 1;58(3):387-95 PMID: 10518112
  48. Recognition and clearance of apoptotic cells: a role for complement and pentraxins.
    Trends Immunol. 2003 Mar;24(3):148-54 PMID: 12615211
  49. Apoptosis and caspases in neurodegenerative diseases.
    N Engl J Med. 2003 Apr 3;348(14):1365-75 PMID: 12672865
  50. 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. 1996 Nov 22;271(47):30022-7 PMID: 8939948
  51. Anti-inflammatory effects of prostaglandin E2 in the central nervous system in response to brain injury and circulating lipopolysaccharide.
    J Neurochem. 2001 Feb;76(3):855-64 PMID: 11158257
  52. 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 U S A. 1995 Feb 28;92(5):1396-400 PMID: 7877989
  53. The contribution of inflammation to acute and chronic neurodegeneration.
    Res Immunol. 1998 Sep-Oct;149(7-8):721-5 PMID: 9851531
  54. Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide.
    Prog Neurobiol. 1998 Jan;54(1):99-125 PMID: 9460796
  55. The function of scavenger receptors expressed by macrophages and their role in the regulation of inflammation.
    Microbes Infect. 2001 Feb;3(2):149-59 PMID: 11251301
  56. A receptor for phosphatidylserine-specific clearance of apoptotic cells.
    Nature. 2000 May 4;405(6782):85-90 PMID: 10811223
  57. Activation of complement in the central nervous system: roles in neurodegeneration and neuroprotection.
    Ann N Y Acad Sci. 2003 May;992:56-71 PMID: 12794047
  58. Microglia as neuroprotective, immunocompetent cells of the CNS.
    Glia. 2002 Nov;40(2):133-9 PMID: 12379901
  59. Microglial interaction with beta-amyloid: implications for the pathogenesis of Alzheimer's disease.
    Microsc Res Tech. 2001 Jul 15;54(2):59-70 PMID: 11455613
  60. Prostaglandin E2 protects cultured cortical neurons against N-methyl-D-aspartate receptor-mediated glutamate cytotoxicity.
    Brain Res. 1994 Nov 14;663(2):237-43 PMID: 7874506
  61. Cell death in health and disease: the biology and regulation of apoptosis.
    Semin Cancer Biol. 1995 Feb;6(1):3-16 PMID: 7548839
  62. Functional characterization of mannose receptor expressed by immunocompetent mouse microglia.
    Glia. 2003 Apr 1;42(1):89-100 PMID: 12594740
  63. Transcriptional regulation by the phosphorylation-dependent factor CREB.
    Nat Rev Mol Cell Biol. 2001 Aug;2(8):599-609 PMID: 11483993
  64. Phagocyte recognition of cells undergoing apoptosis.
    Immunol Today. 1993 Mar;14 (3):131-6 PMID: 8385467
  65. Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve.
    Nature. 1987 Dec 17-23;330(6149):658-9 PMID: 3317065
  66. Alterations in cell surface phosphatidylserine and sugar chains during apoptosis and their time-dependent role in phagocytosis by macrophages.
    Biol Pharm Bull. 2002 Oct;25(10):1277-81 PMID: 12392078
  67. Annexin V binding assay as a tool to measure apoptosis in differentiated neuronal cells.
    J Neurosci Methods. 1998 Dec 31;86(1):63-9 PMID: 9894786
  68. Increased surface phosphatidylserine is an early marker of neuronal apoptosis.
    J Neurosci Res. 1997 Jun 15;48(6):563-70 PMID: 9210526
  69. Nerve growth factor signaling, neuroprotection, and neural repair.
    Annu Rev Neurosci. 2001;24:1217-81 PMID: 11520933
  70. Increased CSF levels of prostaglandin E(2) in variant Creutzfeldt-Jakob disease.
    Neurology. 2002 Jan 8;58(1):127-9 PMID: 11781418
  71. 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. 2000 Nov 6;192(9):1353-64 PMID: 11067883
  72. Increased brain synthesis of prostaglandin E2 and F2-isoprostane in human and experimental transmissible spongiform encephalopathies.
    J Neuropathol Exp Neurol. 2000 Oct;59(10):866-71 PMID: 11079776
  73. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases.
    Science. 1998 Nov 27;282(5394):1717-21 PMID: 9831565
  74. NF-kappa B: a crucial transcription factor for glial and neuronal cell function.
    Trends Neurosci. 1997 Jun;20(6):252-8 PMID: 9185306
  75. Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of transforming growth factor beta, interleukin 4, and prostaglandin E expression in the brain.
    J Exp Med. 1992 Nov 1;176(5):1355-64 PMID: 1383385
  76. Role of p38 and p44/42 mitogen-activated protein kinases in microglia.
    Glia. 2002 Nov;40(2):175-83 PMID: 12379905
  77. A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid.
    J Biol Chem. 2002 Dec 6;277(49):47373-9 PMID: 12239221
  78. Microglia: a sensor for pathological events in the CNS.
    Trends Neurosci. 1996 Aug;19(8):312-8 PMID: 8843599
  79. A novel receptor tyrosine kinase, Mer, inhibits TNF-alpha production and lipopolysaccharide-induced endotoxic shock.
    J Immunol. 1999 Mar 15;162(6):3498-503 PMID: 10092806
  80. Membrane asymmetry and DNA degradation: functionally distinct determinants of neuronal programmed cell death.
    J Neurosci Res. 2000 Feb 15;59(4):568-80 PMID: 10679797
  81. Apoptosis is associated with an inhibition of aminophospholipid translocase (APTL) in CNS-derived HN2-5 and HOG cells and phosphatidylserine is a recognition molecule in microglial uptake of the apoptotic HN2-5 cells.
    Life Sci. 2003 Apr 25;72(23):2617-27 PMID: 12672507
  82. Mannose receptor and its putative ligands in normal murine lymphoid and nonlymphoid organs: In situ expression of mannose receptor by selected macrophages, endothelial cells, perivascular microglia, and mesangial cells, but not dendritic cells.
    J Exp Med. 1999 Jun 21;189(12):1961-72 PMID: 10377192
  83. Apoptosis in the nervous system.
    Nature. 2000 Oct 12;407(6805):802-9 PMID: 11048732
  84. Annexin V labels apoptotic neurons following hypoxia-ischemia.
    Neuroreport. 1997 Dec 22;8(18):3871-5 PMID: 9462458
  85. Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-beta in macrophages that have ingested apoptotic cells.
    J Immunol. 1999 Dec 1;163(11):6164-72 PMID: 10570307
  86. Phosphatidylserine, a death knell.
    Cell Death Differ. 2001 Jun;8(6):551-63 PMID: 11536005
  87. Cyclooxygenase-2 is highly expressed in microglial-like cells in a murine model of prion disease.
    Glia. 2000 Feb 15;29(4):392-6 PMID: 10652449
  88. Appetizing rancidity of apoptotic cells for macrophages: oxidation, externalization, and recognition of phosphatidylserine.
    Am J Physiol Lung Cell Mol Physiol. 2003 Jul;285(1):L1-17 PMID: 12788785
  89. Scavenger receptors in neurobiology and neuropathology: their role on microglia and other cells of the nervous system.
    Glia. 2002 Nov;40(2):195-205 PMID: 12379907
  90. Phagocytic properties of microglia in vitro: implications for a role in multiple sclerosis and EAE.
    Microsc Res Tech. 2001 Jul 15;54(2):81-94 PMID: 11455615
  91. Downregulation of in vitro neurotoxicity of brain macrophages by prostaglandin E2 and a beta-adrenergic agonist.
    Glia. 1994 Aug;11(4):383-6 PMID: 7960041
  92. Detection of NGF-like activity in human brain tissue: increased levels in Alzheimer's disease.
    J Neurosci. 1993 Jun;13(6):2540-50 PMID: 8501520
Article Info
Journal
Molecular neurobiology
Abbr.
Mol Neurobiol
ISSN
0893-7648
Published
2004-04-00
Pages
197-212
Language
English
Region
United States
NLM ID
8900963
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com