Notch1 signaling modulates neuronal progenitor activity in the subventricular zone in response to aging and focal ischemia

Aging Cell

Volumn 12, Issue 6, 2013, Pages 978-987

  Sun, Fen ^a,b   Mao, Xiaoou ^c   Xie, Lin ^c   Ding, Meiping ^a   Shao, Bei ^d   Jin, Kunlin ^b,c  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^c BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^d WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Aged rat brain; Focal cerebral ischemia; Neurogenesis; Notch1 signaling pathway

Indexed keywords

BROXURIDINE; DOUBLECORTIN; JAGGED1; NOTCH1 RECEPTOR;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL PROLIFERATION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; WESTERN BLOTTING;

ANIMALIA; RATTUS;

AGED RAT BRAIN; FOCAL CEREBRAL ISCHEMIA; NEUROGENESIS; NOTCH1 SIGNALING PATHWAY;

AGING; ANIMALS; BEHAVIOR, ANIMAL; BRAIN ISCHEMIA; CALCIUM-BINDING PROTEINS; CELL PROLIFERATION; CEREBRAL INFARCTION; CEREBRAL VENTRICLES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; NEURAL STEM CELLS; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, INBRED F344; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84888134199     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12134     Document Type: Article

References (64)

1. Ables JL, Decarolis NA, Johnson MA, Rivera PD, Gao Z, Cooper DC, Radtke F, Hsieh J, Eisch AJ (2010) Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J. Neurosci. 30, 10484-10492.
2. Ables JL, Breunig JJ, Eisch AJ, Rakic P (2011) Not(ch) just development: Notch signalling in the adult brain. Nat. Rev. Neurosci. 12, 269-283.
3. Adams HP Jr, del Zoppo G, Alberts MJ, Bhatt DL, Brass L, Furlan A, Grubb RL, Higashida RT, Jauch EC, Kidwell C, Lyden PD, Morgenstern LB, Qureshi AI, Rosenwasser RH, Scott PA, Wijdicks EF (2007) Guidelines for the early management of adults with ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council, Clinical Cardiology Council, Cardiovascular Radiology and Intervention Council, and the Atherosclerotic Peripheral Vascular Disease and Quality of Care Outcomes in Research Interdisciplinary Working Groups: the American Academy of Neurology affirms the value of this guideline as an educational tool for neurologists. Stroke 38, 1655-1711.
4. Aguirre A, Rubio ME, Gallo V (2010) Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467, 323-327.
5. Andreu-Agullo C, Morante-Redolat JM, Delgado AC, Farinas I (2009) Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat. Neurosci. 12, 1514-1523.
6. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442, 823-826.
7. Arboleda-Velasquez JF, Zhou Z, Shin HK, Louvi A, Kim HH, Savitz SI, Liao JK, Salomone S, Ayata C, Moskowitz MA, Artavanis-Tsakonas S (2008) Linking Notch signaling to ischemic stroke. Proc. Natl Acad. Sci. USA 105, 4856-4861.
8. Arnold KG (1981) Cerebral blood flow in geriatrics - a review. Age Ageing 10, 5-9.
9. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284, 770-776.
10. Arumugam TV, Chan SL, Jo DG, Yilmaz G, Tang SC, Cheng A, Gleichmann M, Okun E, Dixit VD, Chigurupati S, Mughal MR, Ouyang X, Miele L, Magnus T, Poosala S, Granger DN, Mattson MP (2006) Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke. Nat. Med. 12, 621-623.
11. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963-970.
12. Borlongan CV, Sanberg PR (1995) Elevated body swing test: a new behavioral parameter for rats with 6-hydroxydopamine-induced hemiparkinsonism. J. Neurosci. 15, 5372-5378.
13. Brott T, Bogousslavsky J (2000) Treatment of acute ischemic stroke. N. Engl. J. Med. 343, 710-722.
14. Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat. Neurosci. 2, 894-897.
15. Chojnacki A, Shimazaki T, Gregg C, Weinmaster G, Weiss S (2003) Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J. Neurosci. 23, 1730-1741.
16. Conboy IM, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577.
17. Crews L, Mizuno H, Desplats P, Rockenstein E, Adame A, Patrick C, Winner B, Winkler J, Masliah E (2008) Alpha-synuclein alters Notch-1 expression and neurogenesis in mouse embryonic stem cells and in the hippocampus of transgenic mice. J. Neurosci. 28, 4250-4260.
18. Darsalia V, Heldmann U, Lindvall O, Kokaia Z (2005) Stroke-induced neurogenesis in aged brain. Stroke 36, 1790-1795.
19. De Ryck M, Van Reempts J, Borgers M, Wauquier A, Janssen PA (1989) Photochemical stroke model: flunarizine prevents sensorimotor deficits after neocortical infarcts in rats. Stroke 20, 1383-1390.
20. Ehm O, Goritz C, Covic M, Schaffner I, Schwarz TJ, Karaca E, Kempkes B, Kremmer E, Pfrieger FW, Espinosa L, Bigas A, Giachino C, Taylor V, Frisen J, Lie DC (2010) RBPJkappa-dependent signaling is essential for long-term maintenance of neural stem cells in the adult hippocampus. J. Neurosci. 30, 13794-13807.
21. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317.
22. Gaiano N (2011) Notch in the vertebrate nervous system: an old dog with new tricks. Neuron 69, 840-855.
23. Givogri MI, de Planell M, Galbiati F, Superchi D, Gritti A, Vescovi A, de Vellis J, Bongarzone ER (2006) Notch signaling in astrocytes and neuroblasts of the adult subventricular zone in health and after cortical injury. Dev. Neurosci. 28, 81-91.
24. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, Bondesson M (2005) Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9, 617-628.
25. Irvin DK, Nakano I, Paucar A, Kornblum HI (2004) Patterns of Jagged1, Jagged2, Delta-like 1 and Delta-like 3 expression during late embryonic and postnatal brain development suggest multiple functional roles in progenitors and differentiated cells. J. Neurosci. Res. 75, 330-343.
26. Jin K (2010) Modern biological theories of aging. Aging Dis. 1, 72-74.
27. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (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.
28. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA (2003a) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2, 175-183.
29. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, Greenberg DA (2003b) Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol. Cell. Neurosci. 24, 171-189.
30. Jin K, Minami M, Xie L, Sun Y, Mao XO, Wang Y, Simon RP, Greenberg DA (2004) Ischemia-induced neurogenesis is preserved but reduced in the aged rodent brain. Aging Cell 3, 373-377.
31. Jin K, Sun Y, Xie L, Mao XO, Childs J, Peel A, Logvinova A, Banwait S, Greenberg DA (2005) Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intraventricular, or intravenous transplantation in the rat. Neurobiol. Dis. 18, 366-374.
32. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA (2006) Evidence for stroke-induced neurogenesis in the human brain. PNAS 103, 13198-13202.
33. Jin K, Wang X, Xie L, Mao XO, Greenberg DA (2010) Transgenic ablation of doublecortin-expressing cells suppresses adult neurogenesis and worsens stroke outcome in mice. Proc. Natl Acad. Sci. USA 107, 7993-7998.
34. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, Masel J, Yenari MA, Weissman IL, Uchida N, Palmer T, Steinberg GK (2004) Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. PNAS 101, 11839-11844.
35. Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18, 3206-3212.
36. Kempermann G, Gast D, Gage FH (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol. 52, 135-143.
37. Kondziolka D, Wechsler L, Goldstein S, Meltzer C, Thulborn KR, Gebel J, Jannetta P, DeCesare S, Elder EM, McGrogan M, Reitman MA, Bynum L (2000) Transplantation of cultured human neuronal cells for patients with stroke. Neurology 55, 565-569.
38. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16, 2027-2033.
39. Liu J, Solway K, Messing RO, Sharp FR (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J. Neurosci. 18, 7768-7778.
40. Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC (2006) The aging neurogenic subventricular zone. Aging Cell 5, 139-152.
41. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC (2004) Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J. Neurosci. 24, 1726-1733.
42. McDermott KW, Lantos PL (1991) Distribution and fine structural analysis of undifferentiated cells in the primate subependymal layer. J. Anat. 178, 45-63.
43. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury. Cell 110, 429-441.
44. Nawashiro H, Martin D, Hallenbeck JM (1997) Inhibition of tumor necrosis factor and amelioration of brain infarction in mice. J. Cereb. Blood Flow Metab. 17, 229-232.
45. Ortega F, Costa MR, Simon-Ebert T, Schroeder T, Gotz M, Berninger B (2011) Using an adherent cell culture of the mouse subependymal zone to study the behavior of adult neural stem cells on a single-cell level. Nat. Protoc. 6, 1847-1859.
46. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002) Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52, 802-813.
47. Popa-Wagner A, Badan I, Walker L, Groppa S, Patrana N, Kessler C (2007) Accelerated infarct development, cytogenesis and apoptosis following transient cerebral ischemia in aged rats. Acta Neuropathol. 113, 277-293.
48. Popa-Wagner A, Stocker K, Balseanu AT, Rogalewski A, Diederich K, Minnerup J, Margaritescu C, Schabitz WR (2010) Effects of granulocyte-colony stimulating factor after stroke in aged rats. Stroke 41, 1027-1031.
49. Popa-Wagner A, Buga AM, Kokaia Z (2011) Perturbed cellular response to brain injury during aging. Ageing Res. Rev. 10, 71-79.
50. Ramirez-Lassepas M (1998) Stroke and the aging of the brain and the arteries. Geriatrics 53, S44-S48.
51. Shimizu T, Kagawa T, Inoue T, Nonaka A, Takada S, Aburatani H, Taga T (2008) Stabilized beta-catenin functions through TCF/LEF proteins and the Notch/RBP-Jkappa complex to promote proliferation and suppress differentiation of neural precursor cells. Mol. Cell. Biol. 28, 7427-7441.
52. Stump G, Durrer A, Klein AL, Lutolf S, Suter U, Taylor V (2002) Notch1 and its ligands Delta-like and Jagged are expressed and active in distinct cell populations in the postnatal mouse brain. Mech. Dev. 114, 153-159.
53. Sun F, Xie L, Mao X, Hill J, Greenberg DA, Jin K (2012) Effect of a contralateral lesion on neurological recovery from stroke in rats. Restor. Neurol. Neurosci. 30, 491-495.
54. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR (1990) A semiautomated method for measuring brain infarct volume. J. Cereb. Blood Flow Metab. 10, 290-293.
55. Takizawa T, Ochiai W, Nakashima K, Taga T (2003) Enhanced gene activation by Notch and BMP signaling cross-talk. Nucleic Acids Res. 31, 5723-5731.
56. Tropepe V, Craig CG, Morshead CM, van der Kooy D (1997) Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J. Neurosci. 17, 7850-7859.
57. Wang L, Chopp M, Zhang RL, Zhang L, Letourneau Y, Feng YF, Jiang A, Morris DC, Zhang ZG (2009a) The Notch pathway mediates expansion of a progenitor pool and neuronal differentiation in adult neural progenitor cells after stroke. Neuroscience 158, 1356-1363.
58. Wang X, Mao X, Xie L, Greenberg DA, Jin K (2009b) Involvement of Notch1 signaling in neurogenesis in the subventricular zone of normal and ischemic rat brain in vivo. J. Cereb. Blood Flow Metab. 29, 1644-1654.
59. Won SJ, Xie L, Kim SH, Tang H, Wang Y, Mao X, Banwait S, Jin K (2006) Influence of age on the response to fibroblast growth factor-2 treatment in a rat model of stroke. Brain Res. 1123, 237-244.
60. Yagita Y, Kitagawa K, Ohtsuki T, Takasawa K, Miyata T, Okano H, Hori M, Matsumoto M (2001) Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 32, 1890-1896.
61. Yamashita T, Ninomiya M, Hernandez Acosta P, Garcia-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, Araki N, Abe K, Okano H, Sawamoto K (2006) Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J. Neurosci. 26, 6627-6636.
62. Yang Q, Yan W, Li X, Hou L, Dong H, Wang Q, Wang S, Zhang X, Xiong L (2012) Activation of canonical notch signaling pathway is involved in the ischemic tolerance induced by sevoflurane preconditioning in mice. Anesthesiology 117, 996-1005.
63. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc. Natl Acad. Sci. USA 98, 5874-5879.
64. Zhao Y, Chen X, Ma L, Zuo Z, Zhu Z, Zhu X, Wang Q, He E, Xiong L, Pei J, Xu L, Hou L, Chen S (2012) Electroacupuncture pretreatment induces tolerance against focal cerebral ischemia through activation of canonical Notch pathway. BMC Neurosci. 13, 111.