Activated microglia cause reversible apoptosis of pheochromocytoma cells, inducing their cell death by phagocytosis

Journal of Cell Science

Volumn 129, Issue 1, 2016, Pages 65-79

  Hornik, Tamara C ^a   Vilalta, Anna ^a   Brown, Guy C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cancer; Caspase; Inflammation; Neuroinflammation; Phagocytosis; Phosphatidylserine

Indexed keywords

CASPASE; LACTADHERIN; NITRIC OXIDE; PHOSPHATIDYLSERINE; PURINERGIC P2Y6 RECEPTOR; VITRONECTIN RECEPTOR; LIPOPOLYSACCHARIDE; MEMBRANE ANTIGEN; MFGE8 PROTEIN, RAT; MILK PROTEIN; PURINERGIC P2 RECEPTOR; TUMOR NECROSIS FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL LOSS; COCULTURE; CONTROLLED STUDY; ENZYME ACTIVATION; MICROGLIA; MOUSE; NERVE CELL CULTURE; NONHUMAN; PC12 CELL LINE; PHAGOCYTOSIS; PHAGOPTOSIS; PRIORITY JOURNAL; RAT; ADRENAL TUMOR; ANIMAL; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; METABOLISM; PATHOLOGY; PHEOCHROMOCYTOMA;

ADRENAL GLAND NEOPLASMS; ANIMALS; ANTIGENS, SURFACE; APOPTOSIS; CASPASES; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; ENZYME ACTIVATION; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; MILK PROTEINS; MODELS, BIOLOGICAL; NITRIC OXIDE; PC12 CELLS; PHAGOCYTOSIS; PHEOCHROMOCYTOMA; PHOSPHATIDYLSERINES; RATS; RECEPTORS, PURINERGIC P2; RECEPTORS, VITRONECTIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84958962949     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.174631     Document Type: Article

References (59)

1. Akiyama, H., Kawamata, T., Dedhar, S. and McGeer, P. L. (1991). Immunohistochemical localization of vitronectin, its receptor and beta-3 integrin in Alzheimer brain tissue. J. Neuroimmunol. 32, 19-28.
2. Bal-Price, A. and Brown, G. C. (2000). Nitric-oxide-induced necrosis and apoptosis in PC12 cells mediated by mitochondria. J. Neurochem. 75, 1455-1464.
3. Bal-Price, A. and Brown, G. C. (2001). Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J. Neurosci. 21, 6480-6491.
4. Barcia, C., Ros, C. M., Annese, V., Carrillo-de Sauvage, M. A., Ros-Bernal, F., Gómez, A., Yuste, J. E., Campuzano, C. M., de Pablos, V., Fernandez-Villalba, E. et al. (2012). ROCK/Cdc42-mediated microglial motility and gliapse formation lead to phagocytosis of degenerating dopaminergic neurons in vivo. Sci. Rep. 2, 809.
5. Bevers, E. M. and Williamson, P. L. (2010). Phospholipid scramblase: an update. FEBS Lett. 584, 2724-2730.
6. Blasi, E., Barluzzi, R., Bocchini, V., Mazzolla, R. and Bistoni, F. (1990). Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J. Neuroimmunol. 27, 229-237.
7. Bocchini, V., Mazzolla, R., Barluzzi, R., Blasi, E., Sick, P. and Kettenmann, H. (1992). An immortalized cell line expresses properties of activated microglial cells. J. Neurosci. Res. 31, 616-621.
8. Brown, G. and Neher, J. (2010). Inflammatory neurodegeneration and mechanisms of microglial killing of neurons. Mol. Neurobiol. 41, 242-247.
9. Brown, G. C. and Neher, J. J. (2012). Eaten alive! Cell death by primary phagocytosis: 'phagoptosis'. Trends Biochem. Sci. 37, 325-332.
10. Brown, G. C. and Neher, J. J. (2014). Microglial phagocytosis of live neurons. Nat. Rev. Neurosci. 15, 209-216.
11. Chao, M. P., Jaiswal, S., Weissman-Tsukamoto, R., Alizadeh, A. A., Gentles, A. J., Volkmer, J., Weiskopf, K., Willingham, S. B., Raveh, T., Park, C. Y. et al. (2010). Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci. Transl. Med. 2, 63ra94.
12. Chao, M. P., Weissman, I. L. and Majeti, R. (2012). The CD47-SIRPalpha pathway in cancer immune evasion and potential therapeutic implications. Curr. Opin. Immunol. 24, 225-232.
13. Choi, Y. H. and Park, H. Y. (2012). Anti-inflammatory effects of spermidine in lipopolysaccharide-stimulated BV2 microglial cells. J. Biomed. Sci. 19, 31.
14. Chong, Z. Z., Kang, J. -Q. and Maiese, K. (2004). Essential cellular regulatory elements of oxidative stress in early and late phases of apoptosis in the central nervous system. Antioxid. Redox Signal. 6, 277-287.
15. Cunningham, C. L., Martinez-Cerdeno, V. and Noctor, S. C. (2013). Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33, 4216-4233.
16. D'Amelio, M., Sheng, M. and Cecconi, F. (2012). Caspase-3 in the central nervous system: beyond apoptosis. Trends Neurosci. 35, 700-709.
17. Edris, B., Weiskopf, K., Volkmer, A. K., Volkmer, J. -P., Willingham, S. B., Contreras-Trujillo, H., Liu, J., Majeti, R., West, R. B., Fletcher, J. A. et al. (2012). Antibody therapy targeting the CD47 protein is effective in a model of aggressive metastatic leiomyosarcoma. Proc. Natl. Acad. Sci. USA 109, 6656-6661.
18. Elliott, J. A. and Winn, W. C. Jr. (1986). Treatment of alveolar macrophages with cytochalasin D inhibits uptake and subsequent growth of Legionella pneumophila. Infect. Immun. 51, 31-36.
19. Emmrich, J. V., Hornik, T. C., Neher, J. J. and Brown, G. C. (2013). Rotenone induces neuronal death by microglial phagocytosis of neurons. FEBS J. 280, 5030-5038.
20. Feelisch, M. (1998). The use of nitric oxide donors in pharmacological studies. Naunyn Schmiedebergs Arch. Pharmacol. 358, 113-122.
21. Fricker, M., Neher, J. J., Zhao, J. -W., Théry, C., Tolkovsky, A. M. and Brown, G. C. (2012a). MFG-E8 mediates primary phagocytosis of viable neurons during neuroinflammation. J. Neurosci. 32, 2657-2666.
22. Fricker, M., Oliva-Martín, M. J. and Brown, G. C. (2012b). Primary phagocytosis of viable neurons by microglia activated with LPS or Aβ is dependent on calreticulin/LRP phagocytic signalling. J. Neuroinflammation 9, 196.
23. Fuller, A. D. and Van Eldik, L. J. (2008). MFG-E8 regulates microglial phagocytosis of apoptotic neurons. J. Neuroimmune Pharmacol. 3, 246-256.
24. Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S. et al. (2012). Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 19, 107-120.
25. Goto, H., Kojima, Y., Matsuda, K., Kariya, R., Taura, M., Kuwahara, K., Nagai, H., Katano, H. and Okada, S. (2014). Efficacy of anti-CD47 antibody-mediated phagocytosis with macrophages against primary effusion lymphoma. Eur. J. Cancer 50, 1836-1846.
26. Greene, L. (1978). Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium. J. Cell Biol. 78, 747-755.
27. Greene, L. A. and Tischler, A. S. (1976). Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 73, 2424-2428.
28. Gül, N., Babes, L., Siegmund, K., Korthouwer, R., Bögels, M., Braster, R., Vidarsson, G., ten Hagen, T. L. M., Kubes, P. and van Egmond, M. (2014). Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J. Clin. Invest. 124, 812-823.
29. Hammill, A., Uhr, J. and Scheuermann, R. (1999). Annexin V staining due to loss of membrane asymmetry can be reversible and precede commitment to apoptotic death. Exp. Cell Res. 251, 16-21.
30. Haubner, R., Gratias, R., Diefenbach, B., Goodman, S. L., Jonczyk, A. and Kessler, H. (1996). Structural and functional aspects of RGD-containing cyclic pentapeptides as highly potent and selective integrin α V β 3 antagonists. J. Am. Chem. Soc. 118, 7461-7472.
31. Hedgecock, E. M., Sulston, J. E. and Thomson, J. N. (1983). Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. Science 220, 1277-1279.
32. Hoeppner, D. J., Hengartner, M. O. and Schnabel, R. (2001). Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature 412, 202-206.
33. Hornik, T. C., Neniskyte, U. and Brown, G. C. (2014). Inflammation induces multinucleation of Microglia via PKC inhibition of cytokinesis, generating highly phagocytic multinucleated giant cells. J. Neurochem. 128, 650-661.
34. Kerr, J. F. R., Wyllie, A. H. and Currie, A. R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
35. Koizumi, S., Shigemoto-Mogami, Y., Nasu-Tada, K., Shinozaki, Y., Ohsawa, K., Tsuda, M., Joshi, B. V., Jacobson, K. A., Kohsaka, S. and Inoue, K. (2007). UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446, 1091-1095.
36. Kopatz, J., Beutner, C., Welle, K., Bodea, L. G., Reinhardt, J., Claude, J., Linnartz-Gerlach, B. and Neumann, H. (2013). Siglec-h on activated microglia for recognition and engulfment of glioma cells. Glia 61, 1122-1133.
37. Kumar, A., Chen, S. H., Kadiiska, M. B., Hong, J. -S., Zielonka, J., Kalyanaraman, B. and Mason, R. P. (2014). Inducible nitric oxide synthase is key to peroxynitrite-mediated, LPS-induced protein radical formation in murine microglial BV2 cells. Free Radic. Biol. Med. 73, 51-59.
38. Liu, G., Fiala, M., Mizwicki, M. T., Sayre, J., Magpantay, L., Siani, A., Mahanian, M., Chattopadhyay, M., La Cava, A. and Wiedau-Pazos, M. (2012). Neuronal phagocytosis by inflammatory macrophages in ALS spinal cord: inhibition of inflammation by resolvin D1. Am. J. Neurodegener. Dis. 1, 60-74.
39. Mackenzie, A. B., Young, M. T., Adinolfi, E. and Surprenant, A. (2005). Pseudoapoptosis induced by brief activation of ATP-gated P2X7 receptors. J. Biol. Chem. 280, 33968-33976.
40. Mamedova, L. K., Joshi, B. V., Gao, Z. -G., von Kügelgen, I. and Jacobson, K. A. (2004). Diisothiocyanate derivatives as potent, insurmountable antagonists of P2Y6 nucleotide receptors. Biochem. Pharmacol. 67, 1763-1770.
41. McArthur, S., Cristante, E., Paterno, M., Christian, H., Roncaroli, F., Gillies, G. E. and Solito, E. (2010). Annexin A1: a central player in the anti-inflammatory and neuroprotective role of microglia. J. Immunol. 185, 6317-6328.
42. Neher, J. J., Neniskyte, U., Zhao, J. -W., Bal-Price, A., Tolkovsky, A. M. and Brown, G. C. (2011). Inhibition of microglial phagocytosis is sufficient to prevent inflammatory neuronal death. J. Immunol. 186, 4973-4983.
43. Neher, J. J., Neniskyte, U. and Brown, G. C. (2012). Primary phagocytosis of neurons by inflamed microglia: potential roles in neurodegeneration. Front. Pharmacol. 3, 27.
44. Neher, J. J., Emmrich, J. V., Fricker, M., Mander, P. K., Théry, C. and Brown, G. C. (2013). Phagocytosis executes delayed neuronal death after focal brain ischemia. Proc. Natl. Acad. Sci. USA 110, E4098-E4107.
45. Neher, J. J., Neniskyte, U., Hornik, T. and Brown, G. C. (2014). Inhibition of UDP/P2Y6 purinergic signaling prevents phagocytosis of viable neurons by activated microglia in vitro and in vivo. Glia 62, 1463-1475.
46. Neniskyte, U. and Brown, G. C. (2013). Lactadherin/MFG-E8 is essential for microglia-mediated neuronal loss and phagoptosis induced by amyloid β. J. Neurochem. 126, 312-317.
47. Neniskyte, U., Neher, J. J. and Brown, G. C. (2011). Neuronal death induced by nanomolar amyloid β is mediated by primary phagocytosis of neurons by microglia. J. Biol. Chem. 286, 39904-39913.
48. Neukomm, L. J., Frei, A. P., Cabello, J., Kinchen, J. M., Zaidel-Bar, R., Ma, Z., Haney, L. B., Hardin, J., Ravichandran, K. S., Moreno, S. et al. (2011). Loss of the RhoGAP SRGP-1 promotes the clearance of dead and injured cells in Caenorhabditis elegans. Nat. Cell Biol. 13, 79-86.
49. Peterson, P. K., Verhoef, J. and Quie, P. G. (1977). Influence of temperature on opsonization and phagocytosis of staphylococci. Infect. Immun. 15, 175-179.
50. Reddien, P. W., Cameron, S. and Horvitz, H. R. (2001). Phagocytosis promotes programmed cell death in C. elegans. Nature 412, 198-202.
51. Stowell, S., Karmakar, S., Arthur, C. M., Ju, T., Rodrigues, L. C., Riul, T. B., Dias-Baruffi, M., Miner, J., McEver, R. P. and Cummings, R. D. (2009). Galectin-1 induces reversible phosphatidylserine exposure at the plasma membrane. Mol. Biol. Cell 20, 1408-1418.
52. Suzuki, J., Umeda, M., Sims, P. J. and Nagata, S. (2010). Calcium-dependent phospholipid scrambling by TMEM16F. Nature 468, 834-838.
53. Tang, H. L., Yuen, K. L., Tang, H. M. and Fung, M. C. (2009). Reversibility of apoptosis in cancer cells. Br. J. Cancer 100, 118-122.
54. Tang, H. L., Tang, H. M., Mak, K. H., Hu, S., Wang, S. S., Wong, K. M., Wong, C. S. T., Wu, H. Y., Law, H. T., Liu, K. et al. (2012). Cell survival, DNA damage, and oncogenic transformation after a transient and reversible apoptotic response. Mol. Biol. Cell 23, 2240-2252.
55. van Genderen, H. O., Kenis, H., Hofstra, L., Narula, J. and Reutelingsperger, C. P. M. (2008). Extracellular annexin A5: functions of phosphatidylserine-binding and two-dimensional crystallization. Biochim. Biophys. Acta 1783, 953-963.
56. Wen, J., Ribeiro, R. and Zhang, Y. (2011). Specific PKC isoforms regulate LPS-stimulated iNOS induction in murine microglial cells. J. Neuroinflammation 8, 38.
57. Willingham, S. B., Volkmer, J. -P., Gentles, A. J., Sahoo, D., Dalerba, P., Mitra, S. S., Wang, J., Contreras-Trujillo, H., Martin, R., Cohen, J. D. et al. (2012). The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc. Natl. Acad. Sci. USA 109, 6662-6667.
58. Ye, J., Liu, Z., Wei, J., Lu, L., Huang, Y., Luo, L. and Xie, H. (2013). Protective effect of SIRT1 on toxicity of microglial-derived factors induced by LPS to PC12 cells via the p53-caspase-3-dependent apoptotic pathway. Neurosci. Lett. 553, 72-77.
59. Zwaal, R. F. A., Comfurius, P. and Bevers, E. M. (2005). Surface exposure of phosphatidylserine in pathological cells. Cell. Mol. Life Sci. 62, 971-988.