Microglia-derived TNFα induces apoptosis in neural precursor cells via transcriptional activation of the Bcl-2 family member Puma

Cell Death and Disease

Volumn 4, Issue 3, 2013, Pages

  Guadagno, J ^a,b   Xu, X ^a   Karajgikar, M ^a   Brown, A ^a   Cregan, S P ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Apoptosis; Microglia; Neural precursor cells; Neuroinflammation

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; PROTEIN BAX; PUMA PROTEIN; TUMOR NECROSIS FACTOR ALPHA; 3-(4-METHYLPHENYLSULFONYL)-2-PROPENENITRILE; APOPTOSIS REGULATORY PROTEIN; BAX PROTEIN, MOUSE; NITRILE; PUMA PROTEIN, MOUSE; SULFONE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL STIMULATION; CONTROLLED STUDY; CULTURE MEDIUM; FEMALE; INTRACELLULAR SIGNALING; MICROGLIA; MITOCHONDRION; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; DRUG EFFECT; GENETICS; INFLAMMATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD INJURY; TRANSPLANTATION;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CULTURE MEDIA, CONDITIONED; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; MICE, KNOCKOUT; MICROGLIA; MITOCHONDRIA; NEURAL STEM CELLS; NF-KAPPA B; NITRILES; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD INJURIES; SULFONES; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEINS;

EID: 84875874620     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.59     Document Type: Article

References (56)

1. Taupin P, Gage FH. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 2002; 69: 745-749.
2. Whitney NP, Eidem TM, Peng H, Huang Y, Zheng JC. Inflammation mediates varying effects in neurogenesis: Relevance to the pathogenesis of brain injury and neurodegenerative disorders. J Neurochem 2009; 108: 1343-1359.
3. Ekdahl CT, Mohapel P, Weber E, Bahr B, Blomgren K, Lindvall O. Caspase-mediated death of newly formed neurons in the adult rat dentate gyrus following status epilepticus. Eur J Neurosci 2002; 16: 1463-1471.
4. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002; 8: 963-970.
5. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010; 6: 193-201.
6. Ekdahl CT, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: The dual role of microglia. Neuroscience 2009; 158: 1021-1029.
7. Tambuyzer BR, Ponsaerts P, Nouwen EJ. Microglia: Gatekeepers of central nervous system immunology. J Leukoc Biol 2009; 85: 352-370.
8. Aarum J, Sandberg K, Haeberlein SL, Persson MA. Migration and differentiation of neural precursor cells can be directed by microglia. Proc Natl Acad Sci USA 2003; 100: 15983-15988.
9. Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM, Marshall GP et al. Microglia instruct subventricular zone neurogenesis. Glia 2006; 54: 815-825.
10. Cacci E, jmone-Cat MA, Anelli T, Biagioni S, Minghetti L. In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia 2008; 56: 412-425.
11. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 2003; 100: 13632-13637.
12. Hoehn BD, Palmer TD, Steinberg GK. Neurogenesis in rats after focal cerebral ischemia is enhanced by indomethacin. Stroke 2005; 36: 2718-2724.
13. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003; 302: 1760-1765.
14. Cabal-Hierro L, Lazo PS. Signal transduction by tumor necrosis factor receptors. Cell Signal 2012; 24: 1297-1305.
15. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003; 114: 181-190.
16. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005; 1: 112-119.
17. Vandenabeele P, Galluzzi L, Vanden BT, Kroemer G. Molecular mechanisms of necroptosis: An ordered cellular explosion. Nat Rev Mol Cell Biol 2010; 11: 700-714.
18. Youle RJ, Strasser A. The BCL-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.
19. Zou H, Li Y, Liu X, Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 1999; 274: 11549-11556.
20. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ et al. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-730.
21. Cheng EH, Wei MC, Weiler S, Flavell RA, Mak TW, Lindsten T et al. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell 2001; 8: 705-711.
22. Puthalakath H, Strasser A. Keeping killers on a tight leash: Transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ 2002; 9: 505-512.
23. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998; 94: 491-501.
24. Han J, Flemington C, Houghton AB, Gu Z, Zambetti GP, Lutz RJ et al. Expression of bbc3, a pro-apoptotic BH3-only gene, is regulated by diverse cell death and survival signals. Proc Natl Acad Sci USA 2001; 98: 11318-11323.
25. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001; 7: 683-694.
26. Hayden MS, Ghosh S. NF-kappaB, the first quarter-century: Remarkable progress and outstanding questions. Genes Dev 2012; 26: 203-234.
27. Dutta J, Fan Y, Gupta N, Fan G, Gelinas C. Current insights into the regulation of programmed cell death by NF-kappaB. Oncogene 2006; 25: 6800-6816.
28. Perkins ND, Gilmore TD. Good cop, bad cop: The different faces of NF-kappaB. Cell Death Differ 2006; 13: 759-772.
29. Walker WS, Gatewood J, Olivas E, Askew D, Havenith CE. Mouse microglial cell lines differing in constitutive and interferon-gamma-inducible antigen-presenting activities for naive and memory CD4? and CD8? T cells. J Neuroimmunol 1995; 63: 163-174.
30. Ben-Hur T, Ben-Menachem O, Furer V, Einstein O, Mizrachi-Kol R, Grigoriadis N. Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol Cell Neurosci 2003; 24: 623-631.
31. Cacci E, Claasen JH, Kokaia Z. Microglia-derived tumor necrosis factor-alpha exaggerates death of newborn hippocampal progenitor cells in vitro. J Neurosci Res 2005; 80: 789-797.
32. Liu YP, Lin HI, Tzeng SF. Tumor necrosis factor-alpha and interleukin-18 modulate neuronal cell fate in embryonic neural progenitor culture. Brain Res 2005; 1054: 152-158.
33. Wong G, Goldshmit Y, Turnley AM. Interferon-gamma but not TNF alpha promotes neuronal differentiation and neurite outgrowth of murine adult neural stem cells. Exp Neurol 2004; 187: 171-177.
34. van Raam BJ, Salvesen GS. Proliferative versus apoptotic functions of caspase-8 Hetero or homo: The caspase-8 dimer controls cell fate. Biochim Biophys Acta 2012; 1824: 113-122.
35. Gross A, Yin XM, Wang K, Wei MC, Jockel J, Milliman C et al. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 1999; 274: 1156-1163.
36. Karin M. How NF-kappaB is activated: The role of the IkappaB kinase (IKK) complex. Oncogene 1999; 18: 6867-6874.
37. Conti A, Cardali S, Genovese T, Di PR, La RG. Role of inflammation in the secondary injury following experimental spinal cord trauma. J Neurosurg Sci 2003; 47: 89-94.
38. Genovese T, Mazzon E, Crisafulli C, Di PR, Muia C, Esposito E et al. TNF-alpha blockage in a mouse model of SCI: Evidence for improved outcome. Shock 2008; 29: 32-41.
39. Pineau I, Lacroix S. Proinflammatory cytokine synthesis in the injured mouse spinal cord: Multiphasic expression pattern and identification of the cell types involved. J Comp Neurol 2007; 500: 267-285.
40. Lee SI, Kim BG, Hwang DH, Kim HM, Kim SU. Overexpression of Bcl-XL in human neural stem cells promotes graft survival and functional recovery following transplantation in spinal cord injury. J Neurosci Res 2009; 87: 3186-3197.
41. Oh JS, Kim KN, An SS, Pennant WA, Kim HJ, Gwak SJ et al. Cotransplantation of mouse neural stem cells (mNSCs) with adipose tissue-derived mesenchymal stem cells improves mNSC survival in a rat spinal cord injury model. Cell Transplant 2011; 20: 837-849.
42. Liu Z, Fan Y, Won SJ, Neumann M, Hu D, Zhou L et al. Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 2007; 38: 146-152.
43. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S et al. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 2006; 31: 149-160.
44. Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S, Kokaia Z et al. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 2006; 26: 9703-9712.
45. Iosif RE, Ahlenius H, Ekdahl CT, Darsalia V, Thored P, Jovinge S et al. Suppression of stroke-induced progenitor proliferation in adult subventricular zone by tumor necrosis factor receptor 1. J Cereb Blood Flow Metab 2008; 28: 1574-1587.
46. Gurzov EN, Germano CM, Cunha DA, Ortis F, Vanderwinden JM, Marchetti P et al. p53 upregulated modulator of apoptosis (PUMA) activation contributes to pancreatic beta-cell apoptosis induced by proinflammatory cytokines and endoplasmic reticulum stress. J Biol Chem 2010; 285: 19910-19920.
47. Omori K, Mitsuhashi M, Ishiyama K, Nair I, Rawson J, Todorov I et al. mRNA of the proapoptotic gene BBC3 serves as a molecular marker for TNF-alpha-induced islet damage in humans. Diabetologia 2011; 54: 2056-2066.
48. Wang P, QiuW, Dudgeon C, Liu H, Huang C, ZambettiGP et al. PUMA is directly activated by NFkappaB and contributes to TNF-alpha-induced apoptosis. Cell Death Differ 2009; 16: 1192-1202.
49. Fujioka S, Schmidt C, Sclabas GM, Li Z, Pelicano H, Peng B et al. Stabilization of p53 is a novel mechanism for proapoptotic function of NF-kappaB. J Biol Chem 2004; 279: 27549-27559.
50. Ryan KM, Ernst MK, Rice NR, Vousden KH. Role of NF-kappaB in p53-mediated programmed cell death. Nature 2000; 404: 892-897.
51. Cregan SP, Maclaurin JG, Craig CG, Robertson GS, Nicholson DW, Park DS et al. Baxdependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons. J Neurosci 1999; 19: 7860-7869.
52. Villunger A, Michalak EM, Coultas L, Mullauer F, Bock G, Ausserlechner MJ et al. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003; 302: 1036-1038.
53. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der KD. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 1999; 208: 166-188.
54. Steckley D, Karajgikar M, Dale LB, Fuerth B, Swan P, Drummond-Main C et al. Puma is a dominant regulator of oxidative stress induced Bax activation and neuronal apoptosis. J Neurosci 2007; 27: 12989-12999.
55. Cregan SP, Fortin A, Maclaurin JG, Callaghan SM, Cecconi F, Yu SW et al. Apoptosisinducing factor is involved in the regulation of caspase-independent neuronal cell death. J Cell Biol 2002; 158: 507-517.
56. Xu X, Geremia N, Bao F, Pniak A, Rossoni M, Brown A. Schwann cell coculture improves the therapeutic effect of bone marrow stromal cells on recovery in spinal cord-injured mice. Cell Transplant 2011; 20: 1065-1086.