Hypoxia and neural stem cells: From invertebrates to brain cancer stem cells

International Journal of Developmental Biology

Volumn 55, Issue 6, 2011, Pages 569-581

  Mannello, Ferdinando ^a   Medda, Virginia ^a   Tonti, Gaetana A ^a,b  

^a UNIVERSITY OF URBINO   (Italy)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

Central nervous system; Development; Differentiation; Hypoxia; Neural stem cell

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OXYGEN;

ADAPTIVE BEHAVIOR; BRAIN DEVELOPMENT; BRAIN TUMOR; CANCER STEM CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; CELL HYPOXIA; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; HUMAN; INVERTEBRATE; MOLECULAR MECHANICS; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; VERTEBRATE;

ANIMALS; BRAIN NEOPLASMS; CELL HYPOXIA; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; MICE; NEOPLASTIC STEM CELLS; NEURAL STEM CELLS; NEUROGENESIS; NF-KAPPA B; OXYGEN;

INVERTEBRATA; VERTEBRATA;

EID: 80052729096     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.103186fm     Document Type: Review

References (48)

1. ACKER, T. and ACKER, H. (2004) Cellular oxygen sensing need in CNS function: physiological and pathological implications. J. Exp. Biol. 207: 3171-3188.
2. Brahimi-Horn M.C., Pouyssegur J. (2009) H IF at a glance. J. Cell Science 122: 1055-1057.
3. BRANICKY, R.S. and SCHAFER, W.R. (2008) Oxygen homeostasis: how the worm adapts to variable oxygen levels. Curr. Biol. 18: R559-560.
4. BRAY, S.J. (2006) Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7: 678-689.
5. BGRGERS, H.F., SCHELSHORN, D.W., WAGNER, W., KUSCHINSKY, W. and MAURER, M.H. (2008) Acute anoxia stimulates proliferation in adult neural stem cells from the rat brain. Exp. Brain. Res. 188: 33-43.
6. CACCI, E., VILLA, A., PARMAR M, CAVALLARO, M., MANDAHL, N., LINDVALL, O., Martinez-Serrano A., Kokaia Z. (2007) Generation of human cortical neurons from a new immortal fetal neural stem cell line. Exp. Cell Res. 313:588-601.
7. CHANG, A.J. and BARGMANN, C.I. (2008) Hypoxia and the HIF-1 transcriptional pathway reorganize a neuronal circuit for oxygen-dependent behavior in Caenor-habditis elegans. Proc. Natl. Acad. Sci. USA 105: 7321-7326.
8. CHEN, H.L., PISTOLLATO, F, HOEPPNER, D.J., Nl, H.T., MCKAY, R.D.G. and PANCHISION, D.M. (2007) Oxygen tension regulates serviva and fate of mouse central nervous system precursors at multiple levels. Stem Cells 25: 2291-2301.
9. CLARKE, L. and VAN DER KOOY, D. (2009) Low oxygen enhances primitive and definitive neural stem cell colony formation by inhibiting distinct cell death pathways. Stem Cells 27: 1879-1886.
10. CUMMINS, E.P, BERRA, E., COMERFORD, K. M., GINOUVES, A., FITZGERALD, K. T, SEEBALLUCK, F, GODSON, C, NIELSEN, J. E., MOYNAGH, P., POUYSSEGUR, J. and TAYLOR, C. T. (2006) Prolyl hidroxylase-1 negatively regulates IkB kinase-9, giving insight into hypoxia-induded NFkB activity. Proc. Natl. Acad. Sci. USA 103: 18154-18159.
11. FELLING, R.J., SNYDER, M.J., ROMANKO, M.J., ROTHSTEIN, R.P., ZIEGLER, A.N., YANG, Z., GIVOGRI, M.I., BONGARZONE, E.R., LEVISON, S.W. (2006) Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J. Neurosci. 26: 4359-4369.
12. GALLI, R., GRITTI, A., BONFANTI, L. and VESCOVI, A.L. (2003) Neural stem cells: an overview. Circ. Res. 92: 598-608.
13. GUSTAFSSON, M.V, ZHENG, X., PEREIRS, T, GRADIN K., JIN, S., LUNDKVIST, J., RUAS, J.L., POELLINGER, L., LENDAHL, U., BONDENSSON, M. (2005) Hypoxia requires notch signalling to maintain the undifferentiated cell state. Dev. Cell. 9: 617-628.
14. HEDDLESTON, J.M, LI, Z., LATHIA, J.D., HJELMELAND, A.B. and RICH, J.N. (2010) Hypoxia inducible factors in cancer stem cells. Br. J. Cancer] 02:789-795.
15. HORIE, N., SO, K., MORIYA, T, KITAGAWA, N., TSUTSUMI, K., NAGATA, I. and SHINOHARA, K. (2008) Effects of oxygen concentration on the proliferation and differentiation of mouse neural stem cells in vitro. Cell Mol. Neurobiol28:833-845.
16. JIN, K., MAO, X.O., SUN, Y, XIE, L., GREENBERG, D. A. (2002a) Stem cell factor stimulates neurogenesis in vitro and in vivo. J. Clin. Invest. 110: 311-319.
17. JIN, K., MAO, X.O., SUN, Y, XIE, L, NISHI, E., KLAGSBRUN, M. and GREENBERG, D.A. (2002b) Heparin-binding epidermal growth-factor like growth factor: Hypoxia-inducible expression in vitro and stimulation of neurogenesis in vitro and in vivo. J. Neurosci. 22: 5365-5373.
18. JIN, K., MINAMI, M. and LAN, J.Q. (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. USA 98: 4710-4715.
19. JÖGI, A., Vallo-Christersson J., Holmquist L, Axelson H., Borg A., Pahlma, S. (2004) Human neuroblastoma cells to hypoxia: induction of genes associated with growth, survival, and aggressive behavior. Exp. Cell Res. 295: 469-487.
20. KEWLEY, R.J., WHITELAW, M.L. and Chapman-Smith, A. (2004) The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. Int. J. Biochem. & Cell. Biol. 36: 189-204.
21. KIM, T.S., MISUMI, S., JUNG, C.G., MASUDA, T, ISOBE, Y, FURUYAMA, E, Nis-Hino, H. and HIDA, H. (2008) Increase in dopaminergic neurons from mouse embryonic stem cell-derived neural progenitor/stem cells is mediated by hypoxia inducible factor-1α. J. Neurosci. Res. 86: 2353-2362.
22. KOONG, A.C., CHEN, K.Y and GIACCIA, A.J. (1994) Hypoxia causes the activation of nuclear factor kappa through the phosphorylation of IKBa on tyrosine residues. Cancer Res 54:1425-30.
23. KRABBE, C, COURTOIS, E., JENSEN, P., JORGENSES, J.R., ZIMMER, J., Martinez-Serrano, A. and MEYER, M. (2009) Enhanced dopaminergic differentiation of human neural stem cells by synergistic effect of Bcl-x, and reduced oxygen tension. J. Neurochem. 110: 1908-1920.
24. LIU Y.V., SEMENZA, G. L. (2007) RACK1 vs. HSP90: competition for HIF-1 alpha degradation vs. stabilization. Cell Cycle. 6: 656-659.
25. MANNELLO F and TONTI GA. (2007) Concise review: no breakthroughs for human mesenchymal and embryonic stem cell culture: conditioned medium, feeder layer, or feeder-free; medium with fetal calf serum, human serum, or enriched plasma; serum-free, serum replacement nonconditioned medium, or ad hoc formula? All that glitters is not gold! Stem Cells 25: 1603-1609.
26. MAZUMDAR, J., DONDETI, V. and SIMON, M.C. (2009) Hypoxia-inducible factors in stem cells and cancer. J. Cell Mol. Med. 13: 4319-4328.
27. MILISEVIC, J., ADLER, I., MANAEKO, A., SCHWARZ, S.C., WALKINSHAW, S.C. AREND.M., FILIPPIN, L.A., STORCH, A., and SCHWARZ, J. (2009) Non-hypoxic stabilization of hypoxia-inducible factor alpha (HIF-alpha): relevance in neural progenitor/stem cells. Neurotox. Res. 15: 367-380.
28. MILOSEVIC, J., MAIS EL, M., WEGNER, E, LEUCHTENBERG, J., WEGNER, R.H., GERLACH, M., STORCH, A. and SCHWARZ, J. (2007) Lack of hypoxia-inducible factor-1 α impairs midbrain neural precursor cell involving vascular endothelial growth factor signalling. J. Neurosci. 27: 412-421.
29. PANCHISION, D.M. (2009) The role of oxygen in regulating neural stem cells in development and disease. J. Cell. Physiol. 220: 562-568.
30. PIERFELICE, T.J., SCHRECK, K.C., EBERHART, C.G. and GAIANO, N. (2008) Notch, neural stem cells, and brain tumors. Cold Spring Harb. Symp. Quant. Biol. 73: 367-375.
31. PISTOLLATO, F, CHEN, H.L., SCHWARTZ, PH., BASSO, G. and PANCHISION, D.M. (2007) Oxygen tension controls the expansion of human CNS precursors and the generation of astrocytes and oligodendrocytes. Mol. Cell. Neurosci. 35:424-435.
32. Rodriguez-Jimenez, F.J., Moreno-Manzano V, Lucas-Doming Uez R., Sanchez-Puelles, J.M. (2008) Hypoxia causes downregulation of mismatch repair system and genomic instability in stem cells. Stem Cells 26: 2052-2062.
33. SCHOFIELD C.J., RATCLIFFE P.J. (2004) Oxygen sensing by H IF hydroxylases. Nat. Rev. Mol. Cell. Biol. 5: 343-354.
34. SHINGO, T, SOROKAN, T, SHIMAZAKI, T. and WEISS, S. (2001) Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J. Neurosci. 21: 9733-9743.
35. Silverman-Gavrila, L.B., LU, T.Z., PRASHAD, R.C., NEJATBAKHSH, N., CHARLTON, M. P., FENG Z. P. (2009) Neural phosphoproteomics of a chronic hypoxia model-Lymnaea stagnalis. Neurosci. 161: 621-634.
36. SKULSKII, I.A., PIVOVAROVA, N.B., GAPON, S.A. and KOROTKOV, S.M. (1991) The effect of anoxia and energy metabolism inhibitors on potassium and sodium homeostasis in the neurons of the gastropod mollusk.Ne/rofiz/o/og//a23:313-321.
37. STUDER, L., CSETE, M., LEE, S.H., KABBANI, N., WALIKONIS, J., WOLD, B. and MCKAY, R. (2000) Enhanced prolifetaion, survival, and dopaminergic differentiation of CNS precursor in lowered oxygen. J. Neurosci. 20: 7377-7383.
38. SUNG, S.M., JUNG, D.S., KWON, C.H., PARK, J.Y, KANG, S.K., KIM YK. (2007) Hypoxia/reoxygenation stimulates proliferation through PKC-dependent activation of ERK and Akt in mouse neural progenitor cells. Neurochem. Res. 32: 1932-1939.
39. THEUS, M.H., WEI, L., CUI, L., FRANCIS, K., HU, X., KEOGH, C. and YU, S.P. (2008) In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Exp. Neurobiol. 210: 656-670.
40. TONTI GA and MANNELLO F. (2008) From bone marrow to therapeutic applications: different behaviour and genetic/epigenetic stability during mesenchymal stem cell expansion in autologous and foetal bovine sera? Int. J. Dev Biol. 52:1023-1032.
41. TONTI GA, MANNELLO F CACCI E and BIAGIONI S. (2009) Neural stem cells at the cross road: MMPs may tell the way. Int. J. Dev. Biol. 53: 1-17
42. XIONG, L., ZHAO, T, HUANG, X., LIU, Z.H., ZHAO, H., LI M.M., WU, L.Y, SHU, H.B., ZHU, L.L. and FAN, M. (2009) Heat shock protein 90 is involved in regulation ot hypoxia-driven proliferation of embryonic neural stem/progenitor cells. Cell Stress and Chaperones 14: 183-192.
43. XU, Q., WANG, S., JIANG, X., ZHAO Y, GAO M., ZHANG Y, WANG X., TANO K., KANEHARA M., ZHANG W., ISHIDA T. (2007) Hypoxia-induced astrocytes promote the migration of neural progenitor cells via vascular endothelial factor, stem cellfactor, stromal-derived factor-1 aand monocyte chemoattractantprotein-1 upregulation in vitro. Clin. Exp. Pharmacol. Physiol. 34: 624-631.
44. ZHANG, C.P, ZHU, L.L., ZHAO, T, ZHAO, H., HUANG, X., MA, X., WANG, H. and FAN, M. (2006) Characterization of neural stem cells expanded in lowered oxygen andthe potential role of hypoxia-induciblefactor-1 alpha. Neurosignals 15:259-265.
45. ZHANG, X.R, ZHENG, G. and LOU, L. (2008) Notch activation promotes cell prolife-ration and the formation of neural stem cell-like colonies in human glioma cells. Mol. Cell. Biochem. 307: 101-108.
46. ZHAO, D., NAJBAUER, J., GARCIA, E., METZ, M.Z., GUTOVA, M., GLACKIN, C.A., KIM, S.U. and ABOODY, K.S. (2008) Neural stem cell tropism to glioma: critical role of tumor hypoxia. Mol. Cancer Res. 6: 1819-1829.
47. ZHOU, L. and MILLER, C.A. (2006) Mitogen-activated protein kinase signalling, oxygen sensors and hypoxic induction of neurogenesis. Neurodegener. Dis. 3: 50-55.
48. ZHOU, J., SCHMID, T, FRANK, R. and BRUNE, B. (2004) PI3K/Akt is required for heat shock proteins to protect HIF-1 alpha from pVHL-independent degradation. J. Biol. Chem. 279: 13506-13513.