Influence of oxygen tension on dopaminergic differentiation of human fetal stem cells of midbrain and forebrain origin

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Krabbe, Christina ^a   Bak, Sara Thornby ^a   Jensen, Pia ^a   Von Linstow, Christian ^a   Serrano, Alberto Martínez ^b   Hansen, Claus ^c   Meyer, Morten ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; OXYGEN; TYROSINE 3 MONOOXYGENASE; VASCULOTROPIN; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; TUBB3 PROTEIN, HUMAN; TUBULIN; VASCULOTROPIN A;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL DEATH; CELL FATE; CELL LEVEL; CELL PROLIFERATION; CELL STRUCTURE; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; FETAL STEM CELL; FETUS; FOREBRAIN; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MESENCEPHALON; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEWBORN; NONHUMAN; OXYGEN TENSION; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DOPAMINERGIC NEURONS; FETAL STEM CELLS; FETUS; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; KI-67 ANTIGEN; MESENCEPHALON; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; OXYGEN; PROSENCEPHALON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUBULIN; TYROSINE 3-MONOOXYGENASE; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84900445645     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096465     Document Type: Article

References (57)

1. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39: 889-909. (Pubitemid 37130207)
2. Bjorklund A, Dunnett SB, Brundin P, Stoessl AJ, Freed CR, et al. (2003) Neural transplantation for the treatment of Parkinson's disease. Lancet Neurol 2: 437-445. (Pubitemid 36793939)
3. Freed CR, Breeze RE, Rosenberg NL, Schneck SA, Wells TH, et al. (1990) Therapeutic effects of human fetal dopamine cells transplanted in a patient with Parkinson's disease. Prog Brain Res 82: 715-721. (Pubitemid 20299675)
4. Freed CR, Greene PE, Breeze RE, Tsai WY, DuMouchel W, et al. (2001) Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 344: 710-719. (Pubitemid 32204988)
5. Piccini P, Brooks DJ, Bjorklund A, Gunn RN, Grasby PM, et al. (1999) Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nat Neurosci 2: 1137-1140. (Pubitemid 30126374)
6. Lindvall O, Bjorklund A (2004) Cell therapy in Parkinson's disease. NeuroRx 1: 382-393. (Pubitemid 46589366)
7. Sayles M, Jain M, Barker RA (2004) The cellular repair of the brain in Parkinson's disease - past, present and future. Transpl Immunol 12: 321-342. (Pubitemid 38639727)
8. Winkler C, Kirik D, Bjorklund A (2005) Cell transplantation in Parkinson's disease: how can we make it work? Trends Neurosci 28: 86-92. (Pubitemid 40178925)
9. Barker RA, Barrett J, Mason SL, Bjorklund A (2013) Fetal dopaminergic transplantation trials and the future of neural grafting in Parkinson's disease. Lancet Neurol 12: 84-91.
10. Petit GH, Olsson TT, Brundin P (2014) The future of cell therapies and brain repair: Parkinson's disease leads the way. Neuropathol Appl Neurobiol 40: 60-70.
11. Politis M, Lindvall O (2012) Clinical application of stem cell therapy in Parkinson's disease. BMC Med 10: 1.
12. Freeman BA, Crapo JD (1981) Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem 256: 10986-10992. (Pubitemid 12181585)
13. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, et al. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 95: 11715-11720. (Pubitemid 28460480)
14. Erecinska M, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 128: 263-276. (Pubitemid 33051004)
15. Dings J, Meixensberger J, Jager A, Roosen K (1998) Clinical experience with 118 brain tissue oxygen partial pressure catheter probes. Neurosurgery 43: 1082-1095. (Pubitemid 128723302)
16. Csete M (2005) Oxygen in the cultivation of stem cells. Ann N Y Acad Sci 1049: 1-8.
17. Jensen P, Gramsbergen JB, Zimmer J, Widmer HR, Meyer M (2011) Enhanced proliferation and dopaminergic differentiation of ventral mesencephalic precursor cells by synergistic effect of FGF2 and reduced oxygen tension. Exp Cell Res 317: 1649-1662.
18. Krabbe C, Courtois E, Jensen P, Jorgensen JR, Zimmer J, et al. (2009) Enhanced dopaminergic differentiation of human neural stem cells by synergistic effect of Bcl-xL and reduced oxygen tension. J Neurochem 110: 1908-1920.
19. Liu S, Tian Z, Yin F, Zhao Q, Fan M (2009) Generation of dopaminergic neurons from human fetal mesencephalic progenitors after co-culture with striatal-conditioned media and exposure to lowered oxygen. Brain Res Bull 80: 62-68.
20. Stacpoole SR, Bilican B, Webber DJ, Luzhynskaya A, He XL, et al. (2011) Derivation of neural precursor cells from human ES cells at 3% O(2) is efficient, enhances survival and presents no barrier to regional specification and functional differentiation. Cell Death Differ 18: 1016-1023.
21. Storch A, Paul G, Csete M, Boehm BO, Carvey PM, et al. (2001) Long-term proliferation and dopaminergic differentiation of human mesencephalic neural precursor cells. Exp Neurol 170: 317-325. (Pubitemid 32758685)
22. Studer L, Csete M, Lee SH, Kabbani N, Walikonis J, et al. (2000) Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 20: 7377-7383.
23. Santilli G, Lamorte G, Carlessi L, Ferrari D, Rota Nodari L, et al. (2010) Mild hypoxia enhances proliferation and multipotency of human neural stem cells. PLoS One 5: e8575.
24. Stacpoole SR, Bilican B, Webber DJ, Luzhynskaya A, He XL, et al. (2011) Efficient derivation of NPCs, spinal motor neurons and midbrain dopaminergic neurons from hESCs at 3% oxygen. Nat Protoc 6: 1229-1240.
25. Stacpoole SR, Webber DJ, Bilican B, Compston A, Chandran S, et al. (2013) Neural precursor cells cultured at physiologically relevant oxygen tensions have a survival advantage following transplantation. Stem Cells Transl Med 2: 464-472.
26. Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5: 343-354. (Pubitemid 38579472)
27. Semenza GL (1999) Regulation of mammalian O2 homeostasis by hypoxiainducible factor 1. Annu Rev Cell Dev Biol 15: 551-578.
28. Chen ZY, Asavaritikrai P, Prchal JT, Noguchi CT (2007) Endogenous erythropoietin signaling is required for normal neural progenitor cell proliferation. J Biol Chem 282: 25875-25883. (Pubitemid 47372832)
29. Milosevic J, Maisel M, Wegner F, Leuchtenberger J, Wenger RH, et al. (2007) Lack of hypoxia-inducible factor-1 alpha impairs midbrain neural precursor cells involving vascular endothelial growth factor signaling. J Neurosci 27: 412-421. (Pubitemid 46106015)
30. Jin KL, Mao XO, Greenberg DA (2000) Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci U S A 97: 10242-10247.
31. Ganser C, Papazoglou A, Just L, Nikkhah G (2010) Neuroprotective effects of erythropoietin on 6-hydroxydopamine-treated ventral mesencephalic dopaminerich cultures. Exp Cell Res 316: 737-746.
32. Kanaan NM, Collier TJ, Marchionini DM, McGuire SO, Fleming MF, et al. (2006) Exogenous erythropoietin provides neuroprotection of grafted dopamine neurons in a rodent model of Parkinson's disease. Brain Res 1068: 221-229. (Pubitemid 43139281)
33. McLeod M, Hong M, Mukhida K, Sadi D, Ulalia R, et al. (2006) Erythropoietin and GDNF enhance ventral mesencephalic fiber outgrowth and capillary proliferation following neural transplantation in a rodent model of Parkinson's disease. Eur J Neurosci 24: 361-370. (Pubitemid 44100328)
34. Liste I, Garcia-Garcia E, Martinez-Serrano A (2004) The generation of dopaminergic neurons by human neural stem cells is enhanced by Bcl-XL, both in vitro and in vivo. J Neurosci 24: 10786-10795. (Pubitemid 39602390)
35. Villa A, Liste I, Courtois ET, Seiz EG, Ramos M, et al. (2009) Generation and properties of a new human ventral mesencephalic neural stem cell line. Exp Cell Res 315: 1860-1874.
36. Villa A, Navarro-Galve B, Bueno C, Franco S, Blasco MA, et al. (2004) Long-term molecular and cellular stability of human neural stem cell lines. Exp Cell Res 294: 559-570. (Pubitemid 38326752)
37. Villa A, Snyder EY, Vescovi A, Martinez-Serrano A (2000) Establishment and properties of a growth factor-dependent, perpetual neural stem cell line from the human CNS. Exp Neurol 161: 67-84. (Pubitemid 30136530)
38. Liste I, Garcia-Garcia E, Bueno C, Martinez-Serrano A (2007) Bcl-XL modulates the differentiation of immortalized human neural stem cells. Cell Death Differ 14: 1880-1892. (Pubitemid 350011664)
39. Courtois ET, Castillo CG, Seiz EG, Ramos M, Bueno C, et al. (2010) In vitro and in vivo enhanced generation of human A9 dopamine neurons from neural stem cells by Bcl-XL. J Biol Chem 285: 9881-9897.
40. Gramsbergen JB, Sandberg M, Moller Dall A, Kornblit B, Zimmer J (2002) Glutathione depletion in nigrostriatal slice cultures: GABA loss, dopamine resistance and protection by the tetrahydrobiopterin precursor sepiapterin. Brain Res 935: 47-58. (Pubitemid 34327844)
41. Jorgensen JR, Juliusson B, Henriksen KF, Hansen C, Knudsen S, et al. (2006) Identification of novel genes regulated in the developing human ventral mesencephalon. Exp Neurol 198: 427-437.
42. Larsen TR, Soderling AS, Caidahl K, Roepstorff P, Gramsbergen JB (2008) Nitration of soluble proteins in organotypic culture models of Parkinson's disease. Neurochem Int 52: 487-494.
43. Meyer M, Johansen J, Gramsbergen JB, Johansen TE, Zimmer J (2000) Improved survival of embryonic porcine dopaminergic neurons in coculture with a conditionally immortalized GDNF-producing hippocampal cell line. Exp Neurol 164: 82-93. (Pubitemid 30490725)
44. Meyer M, Matarredona ER, Seiler RW, Zimmer J, Widmer HR (2001) Additive effect of glial cell line-derived neurotrophic factor and neurotrophin-4/5 on rat fetal nigral explant cultures. Neuroscience 108: 273-284. (Pubitemid 33152968)
45. Campbell K, Gotz M (2002) Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci 25: 235-238. (Pubitemid 34327796)
46. Shibata T, Yamada K, Watanabe M, Ikenaka K, Wada K, et al. (1997) Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J Neurosci 17: 9212-9219. (Pubitemid 27498449)
47. Seiz EG, Ramos-Gomez M, Courtois ET, Tonnesen J, Kokaia M, et al. (2012) Human midbrain precursors activate the expected developmental genetic program and differentiate long-term to functional A9 dopamine neurons in vitro. Enhancement by Bcl-X(L). Exp Cell Res 318: 2446-2459.
48. Milosevic J, Schwarz SC, Krohn K, Poppe M, Storch A, et al. (2005) Low atmospheric oxygen avoids maturation, senescence and cell death of murine mesencephalic neural precursors. J Neurochem 92: 718-729. (Pubitemid 40229543)
49. Pistollato F, Chen HL, Schwartz PH, Basso G, Panchision DM (2007) Oxygen tension controls the expansion of human CNS precursors and the generation of astrocytes and oligodendrocytes. Mol Cell Neurosci 35: 424-435. (Pubitemid 46992832)
50. Andersen RK, Johansen M, Blaabjerg M, Zimmer J, Meyer M (2007) Neural tissue-spheres: a microexplant culture method for propagation of precursor cells from the rat forebrain subventricular zone. J Neurosci Methods 165: 55-63. (Pubitemid 47077500)
51. Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7: 150-161.
52. Shiman R, Akino M, Kaufman S (1971) Solubilization and partial purification of tyrosine hydroxylase from bovine adrenal medulla. J Biol Chem 246: 1330-1340.
53. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, et al. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275. (Pubitemid 29246458)
54. Ohh M, Park CW, Ivan M, Hoffman MA, Kim TY, et al. (2000) Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat Cell Biol 2: 423-427.
55. Chandel NS, Budinger GR (2007) The cellular basis for diverse responses to oxygen. Free Radic Biol Med 42: 165-174. (Pubitemid 44970533)
56. Budinger GR, Tso M, McClintock DS, Dean DA, Sznajder JI, et al. (2002) Hyperoxia-induced apoptosis does not require mitochondrial reactive oxygen species and is regulated by Bcl-2 proteins. J Biol Chem 277: 15654-15660. (Pubitemid 34967837)
57. Nishino H, Hida H, Takei N, Kumazaki M, Nakajima K, et al. (2000) Mesencephalic neural stem (progenitor) cells develop to dopaminergic neurons more strongly in dopamine-depleted striatum than in intact striatum. Exp Neurol 164: 209-214. (Pubitemid 30490738)