Phagocytosis in the developing CNS: More than clearing the corpses

Current Opinion in Neurobiology

Volumn 15, Issue 1, 2005, Pages 101-107

  Mallat, Michel ^a   Marín Teva, José Luis ^b   Chéret, Cyril ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS; CELL DEATH; CENTRAL NERVOUS SYSTEM; DROSOPHILA; ECTODERM; GLIA CELL; MACROPHAGE; MICROGLIA; NEMATODE; NERVE CELL; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW;

EID: 13844275290     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2005.01.006     Document Type: Review

References (59)

1. J.F. Kerr, A.H. Wyllie, and A.R. Currie Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br J Cancer 26 1972 239 257
2. A.H. Wyllie, J.F. Kerr, and A.R. Currie Cell death: the significance of apoptosis Int Rev Cytol 68 1980 251 306
3. D.B. Kantor, and A.L. Kolodkin Curbing the excesses of youth: molecular insights into axonal pruning Neuron 38 2003 849 852
4. G.M. Innocenti, S. Clarke, and H. Koppel Transitory macrophages in the white matter of the developing visual cortex. II. Development and relations with axonal pathways Brain Res 313 1983 55 66
5. M.A. Cuadros, and J. Navascués The origin and differentiation of microglial cells during development Prog Neurobiol 56 1998 173 189
6. C. Kaur, A.J. Hao, C.H. Wu, and E.A. Ling Origin of microglia Microsc Res Tech 54 2001 2 9
7. J.L. Marín-Teva, M.A. Cuadros, R. Calvente, A. Almendros, and J. Navascués Naturally occurring cell death and migration of microglial precursors in the quail retina during normal development J Comp Neurol 412 1999 255 275
8. T.M. O'Connor, and C.R. Wyttenbach Cell death in the embryonic chick spinal cord J Cell Biol 60 1974 448 459
9. R. Parnaik, M.C. Raff, and J. Scholes Differences between the clearance of apoptotic cells by professional and non-professional phagocytes Curr Biol 10 2000 857 860
10. P. Berbel, and G.M. Innocenti The development of the corpus callosum in cats: a light- and electron-microscopic study J Comp Neurol 276 1988 132 156
11. J. Savill, I. Dransfield, C. Gregory, and C. Haslett A blast from the past: clearance of apoptotic cells regulates immune responses Nat Rev Immunol 2 2002 965 975
12. P.W. Reddien, and H.R. Horvitz The engulfment process of programmed cell death in Caenorhabditis elegans Annu Rev Cell Dev Biol 20 2004 193 221
13. P.W. Reddien, S. Cameron, and H.R. Horvitz Phagocytosis promotes programmed cell death in C. elegans Nature 412 2001 198 202
14. D.J. Hoeppner, M.O. Hengartner, and R. Schnabel Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans Nature 412 2001 202 206
15. D.W. Nicholson Caspase structure, proteolytic substrates, and function during apoptotic cell death Cell Death Differ 6 1999 1028 1042
16. K. Kuida, T.S. Zheng, S. Na, C. Kuan, D. Yang, H. Karasuyama, P. Rakic, and R.A. Flavell Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice Nature 384 1996 368 372
17. Q.L. Deveraux, R. Takahashi, G.S. Salvesen, and J.C. Reed X-linked IAP is a direct inhibitor of cell-death proteases Nature 388 1997 300 304
18. K.J. Harvey, D. Lukovic, and D.S. Ucker Caspase-dependent Cdk activity is a requisite effector of apoptotic death events J Cell Biol 148 2000 59 72
19. M. Jäättelä, D. Wissing, K. Kokholm, T. Kallunki, and M. Egeblad Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases EMBO J 17 1998 6124 6134
20. S.C. Wright, U. Schellenberger, H. Wang, D.H. Kinder, J.W. Talhouk, and J.W. Larrick Activation of CPP32-like proteases is not sufficient to trigger apoptosis: inhibition of apoptosis by agents that suppress activation of AP24, but not CPP32-like activity J Exp Med 186 1997 1107 1117
21. C. Miossec, V. Dutilleul, F. Fassy, and A. Diu-Hercend Evidence for CPP32 activation in the absence of apoptosis during T lymphocyte stimulation J Biol Chem 272 1997 13459 13462
22. T.Q. Nhan, W.C. Liles, A. Chait, J.T. Fallon, and S.M. Schwartz The p17 cleaved form of caspase-3 is present within viable macrophages in vitro and in atherosclerotic plaque Arterioscler Thromb Vasc Biol 23 2003 1276 1282
23. J.L. Marín-Teva, I. Dusart, C. Colin, A. Gervais, N. van Rooijen, and M. Mallat Microglia promote the death of developing Purkinje cells Neuron 41 2004 535 547 This study provided the first demonstration that microglial cells promote the developmental cell death of neurons engaged in synaptogenesis. The authors describe a method for investigating the function of microglia through selective targeting of these cells with liposomes, and discuss the role of microglia in relation to extracellular signals regulating neuron survival.
24. L.A. Allen Mechanisms of pathogenesis: evasion of killing by polymorphonuclear leukocytes Microbes Infect 5 2003 1329 1335
25. K. Lauber, E. Bohn, S.M. Krober, Y.J. Xiao, S.G. Blumenthal, R.K. Lindemann, P. Marini, C. Wiedig, A. Zobywalski, and S. Baksh Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal Cell 113 2003 717 730 This study provides a molecular mechanism supporting the widely held hypothesis that apoptotic cells attract mononuclear phagocytes. The chemotactic role of LPC released in the supernatants of cultured apoptotic cells is shown in an in vitro transwell assay measuring migration of monocytic cell lines or human primary macrophages. The authors have also performed a detailed analysis of how caspase-3 might specifically activate iPLA2, the enzyme that produces LPC in apoptotic cells. They discuss several open issues such as the possible existence of cofactors required for LPC chemotactic activity and the types of receptor targeted by LPC on mononuclear cells.
26. C. Grimsley, and K.S. Ravichandran Cues for apoptotic cell engulfment: eat-me, don't eat-me and come-get-me signals Trends Cell Biol 13 2003 648 656
27. K. Lauber, S.G. Blumenthal, M. Waibel, and S. Wesselborg Clearance of apoptotic cells: getting rid of the corpses Mol Cell 14 2004 277 287
28. V.A. Fadok, D.R. Voelker, P.A. Campbell, J.J. Cohen, D.L. Bratton, and P.M. Henson Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages J Immunol 148 1992 2207 2216
29. N.A. Maianski, F.P.J. Mul, J.D. van Buul, D. Roos, and T.W. Kuijpers Granulocyte colony-stimulating factor inhibits the mitochondria-dependent activation of caspase-3 in neutrophils Blood 99 2002 672 679
30. S. Arur, E.U. Uche, K. Rezaul, M. Fong, V. Scranton, A.E. Cowan, W. Mohler, and D.K. Han Annexin I is an endogeneous ligand that mediates apoptotic cell engulfment Dev Cell 4 2003 587 598
31. K. Maiese, and A.M. Vincent Membrane asymmetry and DNA degradation: functionally distinct determinants of neuronal programmed cell death J Neurosci Res 59 2000 568 580
32. V.A. Fadok, D.L. Bratton, D.M. Rose, A. Pearson, R.A. Ezekewitz, and P.M. Henson A receptor for phosphatidylserine-specific clearance of apoptotic cells Nature 405 2000 85 90
33. R. De Simone, M.A. Ajmone-Cat, A. Nicolini, and L. Minghetti Expression of phophatidylserine receptor and downregulation of proinflammatory molecule production by its natural ligand in rat microglial cultures J Neuropathol Exp Neurol 61 2002 237 244
34. A. Witting, P. Muller, A. Herrmann, H. Kettenmann, and C. Nolte Phagocytic clearance of apoptotic neurons by microglia/brain macrophages in vitro: involvement of lectin-, integrin-, and phosphatidylserine-mediated recognition J Neurochem 75 2000 1060 1070
35. M.O. Li, M.R. Sarkisian, W.Z. Mehal, P. Rakic, and R.A. Flavell Phosphatidylserine receptor is required for clearance of apoptotic cells Science 302 2003 1560 1563 The study provides evidence for a physiological role of the PSR receptor in cell corpse elimination by focusing on alterations in the development of lung, brain and retina in PSR-deficient embryos.
36. Y. Kunisaki, S. Masuko, M. Noda, A. Inayoshi, T. Sanui, M. Harada, T. Sasazuki, and Y. Fukui Defective fetal liver erythropoiesis and T lymphopoiesis in mice lacking the phosphatidylserine receptor Blood 103 2004 3362 3364
37. P. Cui, B. Qin, N. Liu, G. Pan, and D. Pei Nuclear localization of the phosphatidylserine receptor protein via multiple nuclear localization signals Exp Cell Res 293 2004 154 163
38. J.M. Frade, and Y.A. Barde Microglia-derived nerve growth factor causes cell death in the developing retina Neuron 20 1998 35 41
39. F. Sedel, C. Bechade, S. Vyas, and A. Triller Macrophage-derived tumor necrosis factor alpha, an early developmental signal for motoneuron death J Neurosci 24 2004 2236 2246
40. R.A. Lang, and J.M. Bishop Macrophages are required for cell death and tissue remodeling in the developing mouse eye Cell 74 1993 453 462
41. G. Diez-Roux, and R.A. Lang Macrophages induce apoptosis in normal cells in vivo Development 124 1997 3633 3638
42. R. Lang, M. Lustig, F. Francois, M. Sellinger, and H. Plesken Apoptosis during macrophage-dependent ocular tissue remodelling Development 120 1994 3395 3403
43. M.J. Sonnenfeld, and J.R. Jacobs Macrophages and glia participate in the removal of apoptotic neurons from the Drosophila embryonic nervous system J Comp Neurol 359 1995 644 652
44. R. Cantera, and G.M. Technau Glial cells phagocytose neuronal debris during the metamorphosis of the central nervous system in Drosophila melanogaster Dev Genes Evol 206 1996 277 280
45. U. Tepass, L.I. Fessler, A. Aziz, and V. Hartenstein Embryonic origin of hemocytes and their relationship to cell death in Drosophila Development 120 1994 1829 1837
46. M.J. Sonnenfeld, and J.R. Jacobs Apoptosis of the midline glia during Drosophila embryogenesis: a correlation with axon contact Development 121 1995 569 578
47. J.M. Abrams, K. White, L.I. Fessler, and H. Steller Programmed cell death during Drosophila embryogenesis Development 117 1993 29 43
48. H.C. Sears, C.J. Kennedy, and P.A. Garrity Macrophage-mediated corpse engulfment is required for normal Drosophila CNS morphogenesis Development 130 2003 3557 3565 To demonstrate that phagocytes are needed for normal CNS development, hemocyte and macrophage generation, migration and function were inhibited by several genetic approaches, including hemocyte targeting with dominant negative pvr and use of mutant serpent, which encodes a GATA-family transcription factor required for hemocyte development. Inhibition of phagocytosis by loss of Croquemort function was obtained using RNAi. Hypotheses about how inhibition of cell corpse phagocytosis by macrophages might alter CNS morphogenesis are discussed.
49. K. Brückner, L. Kockel, P. Duchek, C.M. Luque, P. Rorth, and N. Perrimon The PDGF/VEGF receptor controls blood cell survival in Drosophila Dev Cell 7 2004 73 84
50. N.C. Franc, P. Heitzler, R.A. Ezekowitz, and K. White Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila Science 284 1999 1991 1994
51. J. Mergliano, and J.S. Minden Caspase-independent cell engulfment mirrors cell death pattern in Drosophila embryos Development 130 2003 5779 5789 Engulfment of selected cells labeled by photoactivated marker green fluorescent protein genes was detected in living embryos by use of a substrate incorporated in all embryonic cells and converted to a fluorescent product in phagosomes. The technique was applied to mutants deficient in genes that induce cell death or that express the pan-caspase inhibitor p35, and provides compelling evidence for caspase-independent cell engulfment.
52. R.J. Watts, E.D. Hoopfer, and L. Luo Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system Neuron 38 2003 871 885
53. R.J. Watts, O. Schuldiner, J. Perrino, C. Larsen, and L. Luo Glia engulf degenerating axons during developmental axon pruning Curr Biol 14 2004 678 684 This study used the clonal technique known as mosaic analysis with a repressible cell marker to selectively label Drosophila gamma neurons, and showed at the ultrastructural level that degenerating axons are engulfed by glial cell processes. Consistent with an instructive role for glia in axon degeneration, the study also showed that gamma axons are surrounded by these glial cells before axon fragmentation and persist when axon pruning is blocked by targeted interference with the ubiquitin-proteasome system in gamma neurons.
54. •], this study demonstrated the role of engulfing glia in the triggering of axon fragmentation and provided evidence for neuron-to-glia signaling by using dominant negative constructs that interfere with dynamin function in glial cells or inhibit ecdysone receptors in gamma neurons.
55. T. Lee, S. Marticke, C. Sung, S. Robinow, and L. Luo Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila Neuron 28 2000 807 818
56. M.R. Freeman, J. Delrow, J. Kim, E. Johnson, and C.Q. Doe Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function Neuron 38 2003 567 580
57. A.M. Davies Regulation of neuronal survival and death by extracellular signals during development Embo J 22 2003 2537 2545
58. J. Böse, A.D. Gruber, L. Helming, S. Schiebe, I. Wegener, M. Hafner, M. Beales, F. Köntgen, and A. Lengeling The phosphatidylserine receptor has essential functions during embryogenesis but not in apoptotic cell removal J Biol 3 2004 15.1 15.18
59. J.R. Hong, G.H. Lin, C.J. Lin, W.P. Wang, C.C. Lee, T.L. Lin, and J.L. Wu Phophatidylserine receptor is required for the engulfment of dead apoptotic cells and for normal embryonic development in zebrafish Development 131 2004 5417 5427