Aging-and injury-related differential apoptotic response in the dentate gyrus of the hippocampus in rats following brain trauma

Frontiers in Aging Neuroscience

Volumn 5, Issue DEC, 2013, Pages

  Sun, Dong ^a   McGinn, Melissa ^a   Hankins, Jeanette E ^a   Mays, Katherine M ^a   Rolfe, Andrew ^a   Colello, Raymond J ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Aging; Apoptosis; Dentate gyrus; Neurogenesis; Proteomics; Traumatic brain injury

Indexed keywords

HEAT SHOCK PROTEIN 27; HIPPOCALCIN; NUCLEAR PROTEIN; PROTEOME;

AGED; AGING; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; COMPARATIVE STUDY; CONTROLLED STUDY; DENTATE GYRUS; GEL ELECTROPHORESIS; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LIMIT OF QUANTITATION; MALE; MASS SPECTROMETRY; MICROGLIA; NICK END LABELING; NONHUMAN; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; RAT; STRATUM RADIATUM; TISSUE PREPARATION; TRAUMATIC BRAIN INJURY;

EID: 84895804116     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2013.00095     Document Type: Article

References (59)

1. Bruey, J. M., Paul, C., Fromentin, A., Hilpert, S., Arrigo, A. P., Solary, E., et al. (2000). Differential regulation of Hsp27 oligomerization in tumor cells grown in vitro and in vivo. Oncogene 19, 4855-4863. doi: 10.1038/sj.onc.1203850.
2. Charette, S. J., and Landry, J. (2000). The interaction of HSP27 with Daxx identifies a potential regulatory role of HSP27 in Fas-induced apoptosis. Ann. N. Y. Acad. Sci. 926, 126-131. doi: 10.1111/j.1749-6632.2000.tb05606.x.
3. Chirumamilla, S., Sun, D., Bullock, M. R., and Colello, R. J. (2002). Traumatic brain injury induced cell proliferation in the adult mammalian central nervous system. J. Neurotrauma 19, 693-703. doi: 10.1089/08977150260139084.
4. Clark, R. S. B., Chen, J., Watkins, S. C., Kochanek, P. M., Chen, M., Stetler, R. A., et al. (1997). Apoptosis-supressor gene bcl-2 expression after traumatic brain injury in rats. J. Neurosci. 17, 9172-9182.
5. Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D. Jr., Fragniere, A., Tyers, P., et al. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210-213. doi: 10.1126/science.1173215.
6. Colello, R. J., Fuss, B., Fox, M. A., and Alberti, J. (2002). A proteomic approach to rapidly elucidate oligodendrocyte-associated proteins expressed in the myelinating rat optic nerve. Electrophoresis 23, 144-151. doi: 10.1002/1522-2683(200201)23:1<144::AID-ELPS144>3.0.CO;2-P.
7. Conti, A. C., Raghupathi, R., Trojanowski, J. Q., and McIntosh, T. K. (1998). Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J. Neurosci. 18, 5663-5672.
8. Dayer, A. G., Ford, A. A., Cleaver, K. M., Yassaee, M., and Cameron, H. A. (2003). Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol. 460, 563-572. doi: 10.1002/cne.10675.
9. Deng, W., Saxe, M. D., Gallina, I. S., and Gage, F. H. (2009). Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J. Neurosci. 29, 13532-13542. doi: 10.1523/JNEUROSCI.3362-09.2009.
10. Dickstein, D. L., Kabaso, D., Rocher, A. B., Luebke, J. I., Wearne, S. L., and Hof, P. R. (2007). Changes in the structural complexity of the aged brain. Aging Cell 6, 275-284. doi: 10.1111/j.1474-9726.2007.00289.x.
11. Fineman, I., Hovda, D. A., Smith, A., Yoshino, A., and Becker, D. P. (1993). Concussive brain injury is associated with a prolonged accumulation of calcium: a 45Ca autoradiographic study. Brain Res. 624, 94-102. doi: 10.1016/0006-8993(93)90064-T.
12. Fox, G. B., Fan, L., Levasseur, R. A., and Faden, A. I. (1998). Sustained sensory/motor and cognitive deficits with neuronal apoptosis following controlled cortical impact brain injury in the mouse. J. Neurotrauma 15, 599-614. doi: 10.1089/neu.1998.15.599.
13. Frank, M. G., Barrientos, R. M., Biedenkapp, J. C., Rudy, J. W., Watkins, L. R., and Maier, S. F. (2006). mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol. Aging 27, 717-722. doi: 10.1016/j.neurobiolaging.2005.03.013.
14. Furuta, Y., Kobayashi, M., Masaki, T., and Takamatsu, K. (1999). Age-related changes in expressionof hippocalcin and NVP2 in rat brain. Neurochem. Res. 24, 651-658. doi: 10.1023/A:1021000425070.
15. Gao, X., Deng-Bryant, Y., Cho, W., Carrico, K. M., and Chen, J. (2008). Selective death of newborn neurons in hippocampual dentate gyrus following moderate experimental traumatic brain injury. J. Neurosci. Res. 86, 2258-2270. doi: 10.1002/jnr.21677.
16. Guay, J., Lambert, H., Gingras-breton, G., Lavoie, J. N., Huot, J., and Landry, J. (1997). Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J. Cell Sci. 110, 357-368.
17. Habrukowich, C., Han, D. K., Le, A., Rezaul, K., Pan, W., Ghosh, M., et al. (2010). Sphingosine interaction with acidic leucine-rich nuclear phosphoprotein-32A (ANP32A) regulates PP2A activity and cyclooxygenase (COX)-2 expression in human endothelial cells. J. Bio. Chem. 285, 26825-26831. doi: 10.1074/jbc. M110.147058.
18. Havasi, A., Li, Z., Wang, Z., Martin, J. L., Botla, V., Ruchalski, K., et al. (2008). Hsp27 inhibits Bax activation and apoptosis via a phosphatidylinositol 3-kinase-dependent mechanism. J. Biol. Chem. 283, 12305-12313. doi: 10.1074/jbc. M801291200.
19. Heine, V. M., Maslam, S., Joels, M., and Lucassen, P. J. (2004). Prominant decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitaty-adrenal axis activation. Neurobiol. Aging 25, 361-375. doi: 10.1016/S0197-4580(03)00090-3.
20. Horwitz, J. (1992). Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. U.S.A. 89, 10449-10453. doi: 10.1073/pnas.89.21.10449.
21. Kim, W. R., Park, O. H., Choi, S. Y., Park, S. K., Lee, K. J., Rhyu, I. J., et al. (2009). The mainteneance of specific aspects of neuronal function and behavior is dependent on programmed cell death of adult-generated neurons in the dentate gyrus. Eur. J. Neurosci. 29, 1408-1421. doi: 10.1111/j.1460-9568.2009.06693.x.
22. Kobayashi, M., Masaki, T., Hori, K., Masuo, Y., Miyamoto, M., Tsubokawa, H., et al. (2005). Hippocalcin-deficient mice display a defect in cAMP response element-binding protein activation associated with impaired spatial and associative memory. Neuroscience 133, 471-484. doi: 10.1016/j.neuroscience.2005.02.034.
23. Kobe, B., and Deisenhofer, J. (1994). The leucine-rich repeat: a versatile binding motif. Trends Biochem. Sci. 19, 415-421. doi: 10.1016/0968-0004(94)90090-6.
24. Korkohonene, L., Hansson, I., Kukkonen, J. P., Brannvall, K., Kobayashi, M., Takamatsu, K., et al. (2005). Hippocalcin protects against caspase-12-induced and age-dependent neuronal degeneration. Mol. Cell. Neurosci. 28, 85-95. doi: 10.1016/j.mcn.2004.08.015.
25. Kuhn, H. G., Biebl, M., Wilhelm, D., Li, M., Friedlander, R. M., and Winkler, J. (2005). Increased generation of granule cells in adult Bcl-2-overexpressing mice: a role for cell death during continued hippocampal neurogenesis. Eur. J. Neurosci. 22, 1907-1915. doi: 10.1111/j.1460-9568.2005.04377.x.
26. Kular, R. K., Cvetanovic, M., Sifed, S., Kini, A. R., and Opal, P. (2009). Neuronal differentiation is regulated by leucine-rich acidic nuclear protein (LANP), a member of the inhibitor of histone acetyltransferase complex. J. Bio. Chem. 284, 7783-7792. doi: 10.1074/jbc. M806150200.
27. Landry, J., Chretien, P., Lambert, H., Hickey, E., and Weber, L. A. (1989). Heat shock resistance conferred by expression of the human hsp27 gene in rodent cells. J. Cell Biol. 109, 7-15. doi: 10.1083/jcb.109.1.7.
28. Mattson, M. P., and Magnus, T. (2006). Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 7, 278-294. doi: 10.1038/nrn1886.
29. Masuo, Y., Ogura, A., Kobayashi, M., Masaki, T., Furuta, Y., Ono, T., et al. (2007). Hippocalcin protects hippocampal neurons against excitotoxin damage by enhancing calcium extrusion. Neursci. 145, 495-504. doi: 10.1016/j.neuroscience.2006.12.011.
30. Matsuoka, K., Taoka, M., Satozawa, N., Nakayama, H., Ichimura, T., Takahashi, N., et al. (1994). A nuclear factor containing the leucine-rich repeats expressed in murine cerebellar neurons. Proc. Natl. Acad. Sci. U.S.A. 91, 9670-9674. doi: 10.1073/pnas.91.21.9670.
31. Mehlen, P., Briolay, J., Smith, L., Diaz-Latoud, C., Fabre, N., Pauli, D., et al. (1993). Analysis of resistance to heat and hydrogen peroxide stresses in COS cells transiently expressing wild type or deletion mutants of the Drosophilia 27-kDa heat shock protein. Eur. J. Biochem. 215, 277-284. doi: 10.1111/j.1432-1033.1993.tb18032.x.
32. Mehlen, P., Kretz-Remy, C., Preville, X., and Arrigo, A. P. (1996). Human hsp27, Drosphilia hsp27 and human (B-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNF(-induced cell death. EMBO J. 15, 2695-2706.
33. Mehlen, P., Preville, X., Chareyron, P., Briolay, J., Kelemenz, R., and Arrigo, A. P. (1995). Constituitive expression of human hsp27, Drosophilia hsp27, or human αB-crystallin confers resistance to TNF-and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J. Immunol. 215, 363-374.
34. Mercer, E. A., Korhonen, L., Skoglosa, Y., Olsson, P. A., Kukkonen, J. P., and Lindholm, D. (2000). NAIP interacts with hippocalcin and protects neurons against calcium-induced cell death through caspase-3-dependent and-independent pathways. EMBO J. 19, 3597-3607. doi: 10.1093/emboj/19.14.3597.
35. Newcomb, J. K., Zhao, X., Pike, B. R., and Hayes, R. L. (1999). Temporal profiles of apoptotic-like changes in neurons and astrocytes following controlled cortical impact injury in the rat. Exp. Neurol. 158, 76-88. doi: 10.1006/exnr.1999.7071.
36. O'Farrell, P. H. (1975). High resolution two-dimentional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
37. Olariu, A., Cleaver, K. M., and Cameron, H. A. (2007). Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J. Comp. Neurol. 501, 659-667. doi: 10.1002/cne.21268.
38. Palmer, C. L., Lim, W., Hastie, P. G. R., Toward, M., Korolchuk, V. I., Burbidge, S. A., et al. (2005). Happocalcin functions as a calcium sensor in hippocampal LTD. Neuron 47, 487-494. doi: 10.1016/j.neuron.2005.06.014.
39. Pan, W., da Graca, L. S., Shao, Y., Yin, Q., Wu, H., and Jiang, X. (2009). PHAPI/pp32 suppresses tumorigenesis by stimulating apoptosis. J. Biol. Chem. 284, 6946-6954. doi: 10.1074/jbc. M805801200.
40. Pavlopoulos, E., Jones, S., Kosmidis, S., Close, M., Kim, C., Kovalerchik, O., et al. (2013). Molecular mechanism for age-related memory loss: the histone-binding protein RbAp48. Sci. Transl. Med. 5, 200ra115. doi:10.1056/NEJMicm.
41. Paxinos, G., and Watson, C. (1986). The Rrat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, Inc.
42. Raghupathi, R. (2004). Cell death mechanisms following traumatic brain injury. Brain Pathol. 14, 215-222. doi: 10.1111/j.1750-3639.2004.tb00056.x.
43. Ramirez-Amaya, V., Marrone, D. F., Gage, F. H., Worley, P. F., and Barnes, C. A. (2006). Integration of new neurons into functional neural networks. J. Neurosci. 26, 12237-12241. doi: 10.1523/JNEUROSCI.2195-06.2006.
44. Rao, M. S., Hattiangady, B., and Shetty, A. K. (2006). The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5, 545-558. doi: 10.1111/j.1474-9726.2006.00243.x.
45. Sandhir, R., Onyszchuk, G., and Berman, N. E. (2008). Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury. Exp. Neurol. 213, 372-380. doi: 10.1016/j.expneurol.2008.06.013.
46. Shao, C., Roberts, K. N., Markesbery, W. R., Scheff, S. W., Lovell, M. A. (2006). Oxidative stress in head trauma in aging. Free Radic. Biol. Med. 41, 77-85. doi: 10.1016/j.freeradbiomed.2006.03.007.
47. Shapira, Y., Yadid, G., Cotev, S., and Shohami, E. (1989). Accumulation of calcium in the brain following head trauma. Neurol. Res. 11, 169-172.
48. Sierra, A., Encinas, J. M., Deudero, J. J., Chancey, J. H., Nikolopov, G., and Overstreet-Wadiche, L. S. (2010). Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7, 483-495. doi: 10.1016/j.stem.2010.08.014.
49. Small, S. A., Schobel, S. S., Buxton, R. B., Witter, M. P., and Barnes, C. A. (2011). A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 12, 585-601. doi: 10.1038/nrn3085.
50. Sun, D., Colello, R. J., Daugherty, W. P., Kwon, T. H., McGinn, M. J., Harvey, H. B., et al. (2005). Cell proliferation and neuronal differentiation in the dentate gyrus in juvenile and adult rats following traumatic brain injury. J. Neurotrauma 22, 95-105. doi: 10.1089/neu.2005.22.95.
51. Sun, D., McGinn, M. J., Zhou, Z., Harvey, H. B., Bullock, M. R., and Colello, R. J. (2007). Anatomical integration of newly generated dentate granule neurons following traumatic brain injury in adult rats and its association to cognitive recovery. Exp. Neurol. 204, 264-272. doi: 10.1016/j.expneurol.2006.11.005.
52. Sun, W., Winseck, A., Vinstant, S., Park, O. H., Kim, H., and Oppenheim, R. W. (2004). Programmed cell death of adult-generated hippocampal neurons is mediated by the proapoptotic gene Bax. J. Neurosci. 24, 11205-11213. doi: 10.1523/JNEUROSCI.1436-04.2004.
53. Timaru-Kast, R., Luh, C., Gotthardt, P., Huang, C., Schafer, M. K., Engelhard, K., et al. (2012). Influence of age on brain edema formation, secondary brain damage and inflammatory response after brain trauma in mice. PLoS ONE 7:e43829. doi: 10.1371/journal.pone.0043829.
54. van Pragg, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., and Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034. doi: 10.1038/4151030a.
55. Vidyasagar, A., Wilson, N. A., and Djamali, A. (2012). Theat shock protein 27 (Hsp27); biomarker of disease and therapeutic target. Fibrogenesis Tissue Repair 5, 1-7.
56. Wagstaff, M. J. D., Collaco-Moraes, Y., Smith, J., de Belleroche, J. S., Coffin, R. S., and Latchman, D. S. (1999). Protection of neuronal cells from apoptosis by Hsp27 delivered with a herpes simplex virus-based vector. J. Biol. Chem. 274, 5061-5069. doi: 10.1074/jbc.274.8.5061.
57. Walter, J., Keiner, S., Witte, O. W., and Redecker, C. (2011). Age-related effects on hippocmapal precursor cell subpopulations and neurogenesis. Neurobiol. Aging 32, 1904-1914. doi: 10.1016/j.neurobiolaging.2009.11.011.
58. Williams, S., Raghupathi, R., Mackinnon, M. A., McIntosh, T. K., Saatman, K. E., and Graham, D. I. (2001). In situ DNA fragmentation occurs in white matter up to 12 months after head injury in man. Acta Neuropathol. 102, 581-590. doi:10.1007/s004010100410.
59. Zipfel, G. J., Babcock, D. J., Lee, J. M., and Choi, D. W. (2000). Neuronal apoptosis after CNS injury: the role of glutamate and calcium. J. Neurotrauma 17, 857-869. doi: 10.1089/neu.2000.17.857.