TGF-beta signalling in the adult neurogenic niche promotes stem cell quiescence as well as generation of new neurons

Journal of Cellular and Molecular Medicine

Volumn 18, Issue 7, 2014, Pages 1444-1459

  Kandasamy, Mahesh ^a,f   Lehner, Bernadette ^b   Kraus, Sabrina ^c   Sander, Paul Ramm ^b,c   Marschallinger, Julia ^a   Rivera, Francisco J ^a   Trümbach, Dietrich ^d   Ueberham, Uwe ^e   Reitsamer, Herbert A ^a   Strauss, Olaf ^c   Bogdahn, Ulrich ^b   Couillard Despres, Sebastien ^a   Aigner, Ludwig ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^c UNIVERSITY OF REGENSBURG   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF LEIPZIG   (Germany)

^f NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

Author keywords

Cell cycle; Differentiation; Doublecortin; Smad2; Stem cells; TGF 1

Indexed keywords

BIOLOGICAL MARKER; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; CELL AGING; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DNA MICROARRAY; ELECTROPHYSIOLOGY; FEMALE; FISCHER 344 RAT; GENE EXPRESSION PROFILING; GENETICS; HIPPOCAMPUS; HUMAN; METABOLISM; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; STEM CELL NICHE; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BIOMARKERS; BLOTTING, WESTERN; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; ELECTROPHYSIOLOGY; FEMALE; GENE EXPRESSION PROFILING; HIPPOCAMPUS; HUMANS; MICE; MICE, TRANSGENIC; NEUROGENESIS; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, INBRED F344; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELL NICHE; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84901991741     PISSN: 15821838     EISSN: 15824934     Source Type: Journal    
DOI: 10.1111/jcmm.12298     Document Type: Article

References (43)

1. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci. 2005; 28: 223-50.
2. Gage FH. Mammalian neural stem cells. Science. 2000; 287: 1433-8.
3. Nguyen L, Besson A, Roberts JM, et al. Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle. 2006; 5: 2314-8.
4. Goto T, Mitsuhashi T, Takahashi T. Altered patterns of neuron production in the p27 knockout mouse. Dev Neurosci. 2004; 26: 208-17.
5. Kippin TE, Martens DJ, van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 2005; 19: 756-67.
6. Ruzankina Y, Pinzon-Guzman C, Asare A, et al. Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell. 2007; 1: 113-26.
7. Aigner L, Bogdahn U. TGF-beta in neural stem cells and in tumors of the central nervous system. Cell Tissue Res. 2008; 331: 225-41.
8. Wachs FP, Winner B, Couillard-Despres S, et al. Transforming growth factor-beta1 is a negative modulator of adult neurogenesis. J Neuropathol Exp Neurol. 2006; 65: 358-70.
9. Buckwalter MS, Yamane M, Coleman BS, et al. Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol. 2006; 169: 154-64.
10. Kandasamy M, Couillard-Despres S, Raber KA, et al. Stem cell quiescence in the hippocampal neurogenic niche is associated with elevated transforming growth factor-beta signaling in an animal model of Huntington disease. J Neuropathol Exp Neurol. 2010; 69: 717-28.
11. Kohl Z, Kandasamy M, Winner B, et al. Physical activity fails to rescue hippocampal neurogenesis deficits in the R6/2 mouse model of Huntington's disease. Brain Res. 2007; 1155: 24-33.
12. Pineda JR, Daynac M, Chicheportiche A, et al. Vascular-derived TGF-beta increases in the stem cell niche and perturbs neurogenesis during aging and following irradiation in the adult mouse brain. EMBO Mol Med. 2013; 5: 548-62.
13. Mathieu P, Piantanida AP, Pitossi F. Chronic expression of transforming growth factor-beta enhances adult neurogenesis. NeuroImmunoModulation. 2010; 17: 200-1.
14. Ma M, Ma Y, Yi X, et al. Intranasal delivery of transforming growth factor-beta1 in mice after stroke reduces infarct volume and increases neurogenesis in the subventricular zone. BMC Neurosci. 2008; 9: 117.
15. Dhandapani KM, Brann DW. Transforming growth factor-beta: a neuroprotective factor in cerebral ischemia. Cell Biochem Biophys. 2003; 39: 13-22.
16. Zhu Y, Ahlemeyer B, Bauerbach E, et al. TGF-beta1 inhibits caspase-3 activation and neuronal apoptosis in rat hippocampal cultures. Neurochem Int. 2001; 38: 227-35.
17. Wyss-Coray T. Tgf-Beta pathway as a potential target in neurodegeneration and Alzheimer's. Curr Alzheimer Res. 2006; 3: 191-5.
18. Ueberham U, Ueberham E, Bruckner MK, et al. Inducible neuronal expression of transgenic TGF-beta1 in vivo: dissection of short-term and long-term effects. Eur J Neurosci. 2005; 22: 50-64.
19. Prehn JH, Backhauss C, Krieglstein J. Transforming growth factor-beta 1 prevents glutamate neurotoxicity in rat neocortical cultures and protects mouse neocortex from ischemic injury in vivo. J Cereb Blood Flow Metab. 1993; 13: 521-5.
20. Henrich-Noack P, Prehn JH, Krieglstein J. TGF-beta 1 protects hippocampal neurons against degeneration caused by transient global ischemia. Dose-response relationship and potential neuroprotective mechanisms. Stroke. 1996; 27: 1609-14; discussion 15.
21. Caraci F, Battaglia G, Bruno V, et al. TGF-beta1 pathway as a new target for neuroprotection in Alzheimer's disease. CNS Neurosci Ther. 2009; 17: 237-49.
22. Wachs FP, Couillard-Despres S, Engelhardt M, et al. High efficacy of clonal growth and expansion of adult neural stem cells. Lab Invest. 2003; 83: 949-62.
23. Aigner L, Arber S, Kapfhammer JP, et al. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell. 1995; 83: 269-78.
24. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002; 30: 207-10.
25. Ramm P, Couillard-Despres S, Plotz S, et al. A nuclear magnetic resonance biomarker for neural progenitor cells: is it all neurogenesis? Stem Cells. 2009; 27: 420-3.
26. Massague J. How cells read TGF-beta signals. Nat Rev Mol Cell Biol. 2000; 1: 169-78.
27. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, et al. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol. 2003; 467: 1-10.
28. Hocevar BA, Smine A, Xu XX, et al. The adaptor molecule Disabled-2 links the transforming growth factor beta receptors to the Smad pathway. EMBO J. 2001; 20: 2789-801.
29. Zwaagstra JC, Kassam Z, O'Connor-Mccourt MD. Down-regulation of transforming growth factor-beta receptors: cooperativity between the types I, II, and III receptors and modulation at the cell surface. Exp Cell Res. 1999; 252: 352-62.
30. Imayoshi I, Sakamoto M, Yamaguchi M, et al. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci. 2010; 30: 3489-98.
31. Lin AH, Luo J, Mondshein LH, et al. Global analysis of Smad2/3-dependent TGF-beta signaling in living mice reveals prominent tissue-specific responses to injury. J Immunol. 2005; 175: 547-54.
32. Luo J, Daniels SB, Lennington JB, et al. The aging neurogenic subventricular zone. Aging Cell. 2006; 5: 139-52.
33. Luo J, Wyss-Coray T. Bioluminescence analysis of Smad-dependent TGF-beta signaling in live mice. Methods Mol Biol. 2009; 574: 193-202.
34. Doyle E, Regan CM, Shiotani T. Nefiracetam (DM-9384) preserves hippocampal neural cell adhesion molecule-mediated memory consolidation processes during scopolamine disruption of passive avoidance training in the rat. J Neurochem. 1993; 61: 266-72.
35. Vincze C, Pal G, Wappler EA, et al. Distribution of mRNAs encoding transforming growth factors-beta1, -2, and -3 in the intact rat brain and after experimentally induced focal ischemia. J Comp Neurol. 2010; 518: 3752-70.
36. Brionne TC, Tesseur I, Masliah E, et al. Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron. 2003; 40: 1133-45.
37. Tesseur I, Zou K, Esposito L, et al. Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer's pathology. J Clin Invest. 2006; 116: 3060-9.
38. Wang L, Nomura M, Goto Y, et al. Smad2 protein disruption in the central nervous system leads to aberrant cerebellar development and early postnatal ataxia in mice. J Biol Chem. 2011; 286: 18766-74.
39. Wyss-Coray T, Masliah E, Mallory M, et al. Amyloidogenic role of cytokine TGF-beta1 in transgenic mice and in Alzheimer's disease. Nature. 1997; 389: 603-6.
40. Wyss-Coray T, Lin C, Sanan DA, et al. Chronic overproduction of transforming growth factor-beta1 by astrocytes promotes Alzheimer's disease-like microvascular degeneration in transgenic mice. Am J Pathol. 2000; 156: 139-50.
41. Abdipranoto-Cowley A, Park JS, Croucher D, et al. Activin A is essential for neurogenesis following neurodegeneration. Stem Cells. 2009; 27: 1330-46.
42. Kandasamy M, Reilmann R, Winkler J, et al. Transforming growth factor-beta signaling in the neural stem cell niche: a therapeutic target for Huntington's disease. Neurol Res Int. 2011; 2011: 124256.
43. Kraus S, Lehner B, Reichhart N, et al. Transforming growth factor-beta1 primes proliferating adult neural progenitor cells to electrophysiological functionality. Glia. 2013; 61: 1767-83.