Nicotinamide rescues human embryonic stem cell-derived neuroectoderm from parthanatic cell death

Stem Cells

Volumn 27, Issue 8, 2009, Pages 1772-1781

  Cimadamore, Flavio ^a   Curchoe, Carol Lynn ^a   Alderson, Nazilla ^a   Scott, Fiona ^a   Salvesen, Guy ^a   Terskikh, Alexey V ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Human embryonic stem cells; Human neural progenitors; Nicotinamide; Parthanatos; Poly(ADP ribose) polymerase 1

Indexed keywords

ANTIOXIDANT; APOPTOSIS INDUCING FACTOR; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRION; NERVE DEGENERATION; NEUROECTODERM; NEUROEPITHELIUM; PARTHANATOS; PROTEIN TRANSPORT;

ANIMALS; APOPTOSIS INDUCING FACTOR; CELL CULTURE TECHNIQUES; CELL DEATH; CELL GROWTH PROCESSES; CELLS, CULTURED; EMBRYONIC STEM CELLS; ENZYME ACTIVATION; HUMANS; MICE; MITOCHONDRIA; NEURAL PLATE; NEURONS; NIACINAMIDE; OXIDATIVE STRESS; POLY(ADP-RIBOSE) POLYMERASES; RNA, SMALL INTERFERING;

EID: 69249097078     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.107     Document Type: Article

References (43)

1. Flax JD, Aurora S, Yang C et al. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat Biotechnol 1998;16:1033-1039.
2. Lindvall O, Kokaia Z, Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Med 2004;10(suppl):S42-S50.
3. Tamaki S, Eckert K, He D et al. Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. J Neurosci Res 2002;69:976-986.
4. Zeng X, Rao MS. Human embryonic stem cells: long term stability, absence of senescence and a potential cell source for neural replacement. Neuroscience 2007;145:1348-1358.
5. Muñoz-Sanjuán I, Brivanlou AH. Neural induction, the default model and embryonic stem cells. Nat Rev Neurosci 2002;3:271-280.
6. Tropepe V, Hitoshi S, Sirard C et al. Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 2001;30:65-78.
7. Smukler SR, Runciman SB, Xu S et al. Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J Cell Biol 2006;172:79-90.
8. Pankratz MT, Li XJ, Lavaute TM et al. Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 2007;25:1511-1520.
9. Bajpai R, Coppola G, Kaul M et al. Molecular stages of rapid and uniform neuralization of human embryonic stem cells. Cell Death Differ 2009;16:807-815.
10. Masson M, Niedergang C, Schreiber V et al. XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 1998;18:3563-3571.
11. Samper E, Goytisolo FA, Menissier-de Murcia J et al. Normal telomere length and chromosomal end capping in poly(ADP-ribose) polymerase-deficient mice and primary cells despite increased chromosomal instability. J Cell Biol 2001;154:49-60.
12. D'Amours D, Desnoyers S, D'Silva I et al. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 1999;342(pt 2):249-268.
13. de Murcia G, Schreiber V, Molinete M et al. Structure and function of poly(ADP-ribose) polymerase. Mol Cell Biochem 1994;138:15-24.
14. Yu SW, Andrabi SA, Wang H et al. Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 2006;103:18314-18319.
15. Yu SW, Wang H, Poitras MF et al. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002;297:259-263.
16. Wang H, Yu SW, Koh DW et al. Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J Neurosci 2004;24:10963-10973.
17. 3) improves neurological outcome and reduces infarct volume after transient focal cerebral ischemia in Wistar rats. Stroke 2000;31:1679-1685.
18. Yang J, Klaidman LK, Chang ML et al. Nicotinamide therapy protects against both necrosis and apoptosis in a stroke model. Pharmacol Biochem Behav 2002;73:901-910.
19. Xu C, Inokuma MS, Denham J et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001;19:971-974.
20. Elkabetz Y, Panagiotakos G, Al Shamy G et al. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 2008;22:152-165.
21. Bieberich E, MacKinnon S, Silva J et al. Regulation of cell death in mitotic neural progenitor cells by asymmetric distribution of prostate apoptosis response 4 (PAR-4) and simultaneous elevation of endogenous ceramide. J Cell Biol 2003;162:469-479.
22. Nat R, Nilbratt M, Narkilahti S et al. Neurogenic neuroepithelial and radial glial cells generated from six human embryonic stem cell lines in serum-free suspension and adherent cultures. Glia 2007;55:385-399.
23. Eliasson MJ, Sampei K, Mandir AS et al. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med 1997;3:1089-1095.
24. Mandir AS, Poitras MF, Berliner AR et al. NMDA but not non-NMDA excitotoxicity is mediated by poly(ADP-ribose) polymerase. J Neurosci 2000;20:8005-8011.
25. 2 cytotoxicity by inhibiting poly(ADP-ribose) polymerase. Biochem Biophys Res Commun 2000;278:590-598.
26. Shieh WM, Ame JC, Wilson MV et al. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J Biol Chem 1998;273:30069-30072.
27. Andrabi SA, Kim NS, Yu SW et al. Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci USA 2006;103:18308-18313.
28. Carpenter MK, Cui X, Hu ZY et al. In vitro expansion of a multipotent population of human neural progenitor cells. Exp Neurol 1999;158:265-278.
29. Vescovi AL, Reynolds BA, Fraser DD et al. bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 1993;11:951-966.
30. + depletion and mitochondrial permeability transition. J Biol Chem 2004;279:18895-18902.
31. + homeostasis in man. Cell Mol Life Sci 2004;61:19-34.
32. Benjamin RC, Gill DM. ADP-ribosylation in mammalian cell ghosts. Dependence of poly(ADP-ribose) synthesis on strand breakage in DNA J Biol Chem 1980;255:10493-10501.
33. Gradwohl G, Menissier de Murcia JM, Molinete M et al. The second zinc-finger domain of poly(ADP-ribose) polymerase determines specificity for single-stranded breaks in DNA. Proc Natl Acad Sci USA 1990;87:2990-2994.
34. Erecińska M, Silver IA. Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 2001;128:263-276.
35. Daugas E, Susin SA, Zamzami N et al. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J 2000;14:729-739.
36. 2+-independent mechanism. J Bioenerg Biomembr 2004;36:165-170.
37. Prozorovski T, Schulze-Topphoff U, Glumm R et al. Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol 2008;10:385-394.
38. Chen HL, Pistollato F, Hoeppner DJ et al. Oxygen tension regulates survival and fate of mouse central nervous system precursors at multiple levels. Stem Cells 2007;25:2291-2301.
39. Studer L, Csete M, Lee SH et al. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 2000;20:7377-7383.
40. Kuan CY, Roth KA, Flavell RA et al. Mechanisms of programmed cell death in the developing brain. Trends Neurosci 2000;23:291-297.
41. Mutch L, Alberman E, Hagberg B et al. Cerebral palsy epidemiology: where are we now and where are we going? Dev Med Child Neurol 1992;34:547-551.
42. Aycicek A, Iscan A. Oxidative and antioxidative capacity in children with cerebral palsy. Brain Res Bull 2006;69:666-668.
43. Haynes RL, Folkerth RD, Keefe RJ et al. Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 2003;62:441-450.