Age-related proteomic changes in the subventricular zone and their association with neural stem/progenitor cell proliferation

Journal of Neuroscience Research

Volumn 90, Issue 6, 2012, Pages 1159-1168

  Mcginn, Melissa J ^a   Colello, Raymond J ^a   Sun, Dong ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Neurogenesis; Proteome; Subventricular zone

Indexed keywords

ALBUMIN; BROXURIDINE; COLLAPSIN RESPONSE MEDIATOR PROTEIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN 4; COLLAPSIN RESPONSE MEDIATOR PROTEIN 5; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE OMEGA; MICROSOMAL PROTEASE ER60; PREPROALBUMIN; PROTEINASE; PROTEOME; UBIQUITIN THIOLESTERASE; UBIQUITIN THIOLESTERASE 1; UNCLASSIFIED DRUG;

AGING; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DISSECTION; MASS SPECTROMETRY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; RAT; SUBVENTRICULAR ZONE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AGING; ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CELL PROLIFERATION; CEREBRAL VENTRICLES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERMEDIATE FILAMENT PROTEINS; MALE; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 84859438357     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23012     Document Type: Article

References (65)

1. Ahlenius H, Visan V, Kokaia M, Lindall O, Kokaia Z. 2009. Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J Neurosci 29: 4408-4419.
2. Alonso G. 2001. Proliferation of progenitor cells in the adult rat brain correlates with the presence of vimentin-expressing astrocytes. Glia 34: 253-266.
3. Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319-335.
4. Babu GJ, Wheeler D, Alzate O, Periasamy M. 2004. Solubilization of membrane proteins for two-dimensional gel electrophoresis: identification of sarcoplasmic reticulum membrane proteins. Anal Biochem 325: 121-125.
5. Bouab M, Paliouras GN, Aumont A, Forest-Berard K, Fernandes KJL. 2011. Aging of the subventricular zone neural stem cell niche: evidence for quiescence-associated changes between early and mid-adulthood. Neuroscience 173: 135-149.
6. Cameron HA, Hazel TG, McKay RD. 1998. Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 36: 287-306.
7. Celli CM, Jaiswal AK. 2003. Role of GRP58 in mitomycin C-induced DNA cross-linking. Cancer Res 63: 6016-6025.
8. Chirumamilla S, Sun D, Bullock MR, Colello RJ. 2002. Traumatic brain injury induced cell proliferation in the adult mammalian central nervous system. J Neurotrauma 19: 693-703.
9. Colello RJ, Fuss B, Fox MA, Alberti J. 2002. A proteomic approach to rapidly elucidate oligodendrocyte-associated proteins expressed in the myelinating rat optic nerve. Electrophoresis 23: 144-151.
10. Della-Maggiore V, Grady CL, McIntosh AR. 2002. Dissecting the effect of aging on the neural substrates of memory: deterioration, preservation or functional reorganization? Rev Neurosci 13: 167-181.
11. Demars M, Hu MS, Gadadhar A, Lazarov O. 2010. Impaired neurogensis is an early event in the etiology of familial Alzheimer's disease in transgenic mice. J Neurosci Res 88: 2103-2117.
12. Doetsch F, Alvarez-Buylla A. 1996. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci U S A 93: 14895-14900.
13. Driscoll I, Sutherland RJ. 2005. The aging hippocampus: navigating between rat and human experiments. Rev Neurosci 16: 87-121.
14. Eiben CF, Anderson TP, Lockman L, Matthews DJ, Dryja R, Martin J, Burrill C, Gottesman N, O'Brian P, Witte L. 1984. Functional outcome of closed head injury in children and young adults. Arch Phys Med Rehabil 65: 168-170.
15. Encinas JM, Michurina TA, Peunova N, Pake JH, Tordo J, Peterson DA, Fishell G, Koulakov A, Enikolopov G. 2011. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8: 566-579.
16. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S. 2004. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24: 8354-8365.
17. Goldfien RD, Seaman WE, Hempel WM, Imboden JB. 1991. Divergent regulation of phospholipase C-alpha and phospholipase C-gamma transcripts during activation of a human T cell line. J Immunol 146: 3703-3708.
18. Gorg A, Weiss W, Dunn MJ. 2004. Current two-dimensional electrophoresis technology for proteomics. Proteomics 4: 3665-3685.
19. Goss JR, Finch CE, Morgan DG. 1991. Age-related changes in glial fibrillary acidic protein mRNA in the mouse brain. Neurobiol Aging 12: 165-170.
20. Hallbergson AF, Gnatenco C, Peterson DA. 2003. Neurogenesis and brain injury: managing a renewable resource for repair. J Clin Invest 112: 1128-1133.
21. Harada T, Harada C, Wang YL, Osaka H, Amanai K, Tanaka K, Takizawa S, Setsuie R, Sakurai M, Sato Y, Noda M, Wada K. 2004. Role of ubiquitin carboxy terminal hydrolase-L1 in neural cell apoptosis induced by ischemic retinal injury in vivo. Am J Pathol 164: 59-64.
22. Hastings NB, Gould E. 1999. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413: 146-154.
23. Hopkins A. 1993. Clinical neurology: a modern approach. New York: Oxford University Press.
24. Hughes EA, Cresswell P. 1998. The thiol oxidoreductase ERp57 is a component of the MHC class I peptide-loading complex. Curr Biol 8: 709-712.
25. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA. 2003. Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2: 175-183.
26. Kempermann G. 2002. Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 22: 635-638.
27. Kim JH, Park KC, Chung SS, Bang O, Chung CH. 2003. Deubiquitinating enzymes as cellular regulators. J Biochem (Tokyo) 134: 9-18.
28. 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.
29. -/- mice. Neurochem Res 29: 2069-2073.
30. Lee CK, Weindruch R, Prolla TA 2000. Gene-expression profile of the ageing brain in mice. Nat Genet 25: 294-297.
31. Lendahl U, Zimmerman LB, McKay RD. 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
32. Lim DA, Alvarez-Buylla A. 1999. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci U S A 96: 7526-7531.
33. Limke TL, Rao MS. 2002. Neural stem cells in aging and disease. J Cell Mol Med 6: 475-496.
34. Liu Y, Lashuel HA, Choi S, Xing X, Case A, Ni J, Yeh LA, Cuny GD, Stein RL, Lansbury PTJr. 2003. Discovery of inhibitors that elucidate the role of UCH-L1 activity in the H1299 lung cancer cell line. Chem Biol 10: 837-846.
35. Lois C, Alvarez-Buylla A. 1993. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A 90: 2074-2077.
36. Lombardino AJ, Li XC, Hertel M, Nottebohm F. 2005. Replaceable neurons and neurodegenerative disease share depressed UCHL1 levels. Proc Natl Acad Sci U S A 102: 8036-8041.
37. Lubec G, Krapfenbauer K, Fountoulakis M. 2003. Proteomics in brain research: potentials and limitations. Prog Neurobiol 69: 193-211.
38. Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC. 2006. The aging neurogenic subventricular zone. Aging Cell 5: 139-152.
39. Madhavan L, Ourednik V, Ourednik J. 2005. Grafted neural stem cells shield the host environment from oxidative stress. Ann N Y Acad Sci 1049: 185-188.
40. 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.
41. Mattson MP, Chan SL, Duan W. 2002. Modification of brain aging and neurodegenerative disorders by genes, diet, and behavior. Physiol Rev 82: 637-672.
42. Miller MW, Nowakowski RS. 1988. Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 457: 44-52.
43. Minturn JE, Fryer HJ, Geschwind DH, Hockfield S. 1995. TOAD-64, a gene expressed early in neuronal differentiation in the rat, is related to unc-33, a C. elegans gene involved in axon outgrowth. J Neurosci 15: 6757-6766.
44. INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443: 448-452.
45. Morrice NA, Powis SJ. 1998. A role for the thiol-dependent reductase ERp57 in the assembly of MHC class I molecules. Curr Biol 8: 713-716.
46. Mortz E, Krogh TN, Vorum H, Gorg A. 2001. Improved silver staining protocols for high sensitivity protein identification using matrix-assisted laser desorption/ionization-time of flight analysis. Proteomics 1: 1359-1363.
47. Nacher J, Rosell DR, McEwen BS. 2000. Widespread expression of rat collapsin response-mediated protein 4 in the telencephalon and other areas of the adult rat central nervous system. J Comp Neurol 424: 628-639.
48. O'Farrell PH. 1975. High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007-2021.
49. Parent JM. 2003. Injury-induced neurogenesis in the adult mammalian brain. Neuroscientist 9: 261-272.
50. Quinn CC, Chen E, Kinjo TG, Kelly G, Bell AW, Elliott RC, McPherson PS, Hockfield S. 2003. TUC-4b, a novel TUC family variant, regulates neurite outgrowth and associates with vesicles in the growth cone. J Neurosci 23: 2815-2823.
51. Rodriguez JJ, Jones VC, Tabuchi M, Allan SM, Knight EM, LaFerla FM, Oddo S, Verkhratsky A. 2008. Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer's disease. PLoS One 3: e2935.
52. Rodriguez JJ, Jones VC, Verkhratsky A. 2009. Impaired cell proliferation in the subventricular zone in an Alzheimer's disease model. Neuroreport 20: 907-912.
53. Seki T. 2002. Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NeuroD in the hippocampus of young adult and aged rodents. J Neurosci Res 70: 327-334.
54. Seki T, Arai Y. 1995. Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6: 2479-2482.
55. Selkoe DJ. 1992. Aging brain, aging mind. Sci Am 267: 134-142.
56. Sun D, McGinn MJ, Zhou Z, Harvey HB, Bullock MR, Colello RJ. 2007. Anatomical integration of newly generated granule neurons following TBI in adult rats and its association to cognitive recovery. Exp Neurol 204: 264-272.
57. Sun D, Bullock MR, McGinn MJ, Zhou Z, Hagood S, Altememi N, Hamm R, Colello RJ. 2009. Basic fibroblast growth factor enhances neurogenesis and improves cognitive recovery in rats following traumatic brain injury. Exp Neurol 216: 56-65.
58. Sun D, Bullock MR, Altememi N, Hagood S, Zhou Z, Rolfe A, McGinn MJ, Hamm R, Colello RJ. 2010. Epidermal growth factor mediated brain repair following traumatic brain injury. J Neurotrauma 27: 923-938.
59. Taylor CM, Pfeiffer SE. 2003. Enhanced resolution of glycosylphosphatidylinositol-anchored and transmembrane proteins from the lipid-rich myelin membrane by two-dimensional gel electrophoresis. Proteomics 3: 1303-1312.
60. Townsend DM, Tew KD. 2003. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 22: 7369-7375.
61. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
62. Veyrac A, Giannetti N, Charrier E, Reymond-Marron I, Aguera M, Rogemond V, Honnorat J, Jourdan F. 2005. Expression of collapsin response mediator proteins 1, 2 and 5 is differentially regulated in newly generated and mature neurons of the adult olfactory system. Eur J Neurosci 21: 2635-2648.
63. Walter J, Keiner S, Witte OW, Redecker C. 2011. Age-related effects on hippocampal precursor cell subpopulations and neurogenesis. Neurobiol Aging 32: 1906-1914.
64. Wilkinson KD. 1997. Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J 11: 1245-256.
65. Wu Y, Zhang AQ, Yew DT. 2005. Age related changes of various markers of astrocytes in senescence-accelerated mice hippocampus. Neurochem Int 46: 565-574.