Spatio-temporal analysis of molecular determinants of neuronal degeneration in the aging mouse cerebellum

Molecular and Cellular Proteomics

Volumn 12, Issue 5, 2013, Pages 1350-1362

  De Graaf, Erik L ^a,b,c   Vermeij, Wilbert P ^c,d   De Waard, Monique C ^c,d   Rijksen, Yvonne ^c,d   Van Der Pluijm, Ingrid ^c,d   Hoogenraad, Casper C ^d   Hoeijmakers, Jan H J ^c,d   Altelaar, A F Maarten ^a,b   Heck, Albert J R ^a,b,c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; MOLECULAR MARKER; STABLE ISOTOPE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOHISTOLOGY; INFLAMMATION; ISOTOPE LABELING; MORPHOLOGY; MOUSE; NERVE CELL; NERVE CELL DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; PURKINJE CELL; SPATIOTEMPORAL ANALYSIS; SYNAPSE;

AGING; ANIMALS; CELL SHAPE; CEREBELLUM; DNA REPAIR; DNA-BINDING PROTEINS; ENDONUCLEASES; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE DEGENERATION; NERVE TISSUE PROTEINS; PROTEOME; PURKINJE CELLS;

EID: 84876589511     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.024950     Document Type: Article

References (34)

1. Hoeijmakers, J. H. (2009) DNA damage, aging, and cancer. N. Engl. J. Med. 361, 1475-1485
2. Wang, J., Clauson, C. L., Robbins, P. D., Niedernhofer, L. J., and Wang, Y. (2012) The oxidative DNA lesions 8,5′-cyclopurines accumulate with aging in a tissue-specific manner. Aging Cell., 11, 714-716
3. Kyng, K. J., and Bohr, V. A. (2005) Gene expression and DNA repair in progeroid syndromes and human aging. Ageing Res. Rev. 4, 579-602 (Pubitemid 43293169)
4. McWhir, J., Selfridge, J., Harrison, D. J., Squires, S., and Melton, D. W. (1993) Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat. Genet. 5, 217-224 (Pubitemid 23330382)
5. Weeda, G., Donker, I., de Wit, J., Morreau, H., Janssens, R., Vissers, C. J., Nigg, A., van Steeg, H., Bootsma, D., and Hoeijmakers, J. H. (1997) Disruption of mouse ERCC1 results in a novel repair syndrome with growth failure, nuclear abnormalities, and senescence. Curr. Biol. 7, 427-439 (Pubitemid 27274796)
6. Niedernhofer, L. J., Garinis, G. A., Raams, A., Lalai, A. S., Robinson, A. R., Appeldoorn, E., Odijk, H., Oostendorp, R., Ahmad, A., van Leeuwen, W., Theil, A. F., Vermeulen, W., van der Horst, G. T., Meinecke, P., Kleijer, W. J., Vijg, J., Jaspers, N. G., and Hoeijmakers, J. H. (2006) A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444, 1038-1043 (Pubitemid 46018517)
7. Lawrence, N. J., Sacco, J. J., Brownstein, D. G., Gillingwater, T. H., and Melton, D. W. (2008) A neurological phenotype in mice with DNA repair gene Ercc1 deficiency. DNA Repair 7, 281-291
8. Végh, M. J., de Waard, M. C., van der Pluijm, I., Ridwan, Y., Sassen, M. J., van Nierop, P., van der Schors, R. C., Li, K. W., Hoeijmakers, J. H., Smit, A. B., and van Kesteren, R. E. (2012) Synaptic proteome changes in a DNA repair-deficient ercc1 mouse model of accelerated aging. J. Proteome Res. 11, 1855-1867
9. Schrimpf, S. P., Meskenaite, V., Brunner, E., Rutishauser, D., Walther, P., Eng, J., Aebersold, R., and Sonderegger, P. (2005) Proteomic analysis of synaptosomes using isotope-coded affinity tags and mass spectrometry. Proteomics 5, 2531-2541 (Pubitemid 40966480)
10. Nielsen, P. A., Olsen, J. V., Podtelejnikov, A. V., Andersen, J. R., Mann, M., and Wisniewski, J. R. (2005) Proteomic mapping of brain plasma membrane proteins. Mol. Cell. Proteomics 4, 402-408 (Pubitemid 40590560)
11. Coughenour, H. D., Spaulding, R. S., and Thompson, C. M. (2004) The synaptic vesicle proteome: a comparative study in membrane protein identification. Proteomics 4, 3141-3155 (Pubitemid 39372396)
12. Cheng, D., Hoogenraad, C. C., Rush, J., Ramm, E., Schlager, M. A., Duong, D. M., Xu, P., Wijayawardana, S. R., Hanfelt, J., Nakagawa, T., Sheng, M., and Peng, J. (2006) Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol. Cell. Proteomics 5, 1158-1170 (Pubitemid 43985938)
13. Barski, J. J., Dethleffsen, K., and Meyer, M. (2000) Cre recombinase expression in cerebellar Purkinje cells. Genesis 28, 93-98
14. Doig, J., Anderson, C., Lawrence, N. J., Selfridge, J., Brownstein, D. G., and Melton, D. W. (2006) Mice with skin-specific DNA repair gene (Ercc1) inactivation are hypersensitive to ultraviolet irradiation-induced skin cancer and show more rapid actinic progression. Oncogene 25, 6229-6238 (Pubitemid 44564740)
15. Boersema, P. J., Raijmakers, R., Lemeer, S., Mohammed, S., and Heck, A. J. (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat. Protoc. 4, 484-494
16. Gauci, S., Helbig, A. O., Slijper, M., Krijgsveld, J., Heck, A. J., and Mohammed, S. (2009) Lys-N and trypsin cover complementary parts of the phosphoproteome in a refined SCX-based approach. Anal. Chem. 81, 4493-4501
17. Roxas, B. A., and Li, Q. (2008) Significance analysis of microarray for relative quantitation of LC/MS data in proteomics. BMC Bioinformatics 9, 187
18. Dahlhaus, M., Li, K. W., van der Schors, R. C., Saiepour, M. H., van Nierop, P., Heimel, J. A., Hermans, J. M., Loos, M., Smit, A. B., and Levelt, C. N. (2011) The synaptic proteome during development and plasticity of the mouse visual cortex. Mol. Cell. Proteomics 10, M110 005413
19. Munoz, J., Low, T. Y., Kok, Y. J., Chin, A., Frese, C. K., Ding, V., Choo, A., and Heck, A. J. (2011) The quantitative proteomes of human-induced pluripotent stem cells and embryonic stem cells. Mol. Syst. Biol. 7, 550
20. Tusher, V. G., Tibshirani, R., and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 98, 5116-5121 (Pubitemid 32397092)
21. Jaarsma, D., Haasdijk, E. D., Grashorn, J. A., Hawkins, R., van Duijn, W., Verspaget, H. W., London, J., and Holstege, J. C. (2000) Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol. Dis. 7, 623-643 (Pubitemid 32044287)
22. Nadler, J. V., and Evenson, D. A. (1983) Use of excitatory amino acids to make axon-sparing lesions of hypothalamus. Methods Enzymol. 103, 393-400
23. de Waard, M. C., van der Pluijm, I., Zuiderveen Borgesius, N., Comley, L. H., Haasdijk, E. D., Rijksen, Y., Ridwan, Y., Zondag, G., Hoeijmakers, J. H., Elgersma, Y., Gillingwater, T. H., and Jaarsma, D. (2010) Age-related motor neuron degeneration in DNA repair-deficient Ercc1 mice. Acta Neuropathol. 120, 461-475
24. Walther, D. M., and Mann, M. (2011) Accurate quantification of more than 4000 mouse tissue proteins reveals minimal proteome changes during aging. Mol. Cell. Proteomics 10, M110 004523
25. Borgesius, N. Z., de Waard, M. C., van der Pluijm, I., Omrani, A., Zondag, G. C., van der Horst, G. T., Melton, D. W., Hoeijmakers, J. H., Jaarsma, D., and Elgersma, Y. (2011) Accelerated age-related cognitive decline and neurodegeneration, caused by deficient DNA repair. J. Neurosci. 31, 12543-12553
26. Lu, T., Pan, Y., Kao, S. Y., Li, C., Kohane, I., Chan, J., and Yankner, B. A. (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429, 883-891 (Pubitemid 38843301)
27. Penkowa, M., Carrasco, J., Giralt, M., Moos, T., and Hidalgo, J. (1999) CNS wound healing is severely depressed in metallothionein I- and II-deficient mice. J. Neurosci. 19, 2535-2545 (Pubitemid 29162402)
28. Gilman, C. P., and Mattson, M. P. (2002) Do apoptotic mechanisms regulate synaptic plasticity and growth-cone motility? Neuromolecular Med. 2, 197-214 (Pubitemid 37012504)
29. Jacobs, B., Driscoll, L., and Schall, M. (1997) Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J. Comp. Neurol. 386, 661-680 (Pubitemid 27415497)
30. Esiri, M. M. (2007) Ageing and the brain. J. Pathol. 211, 181-187
31. Garinis, G. A., van der Horst, G. T., Vijg, J., and Hoeijmakers, J. H. (2008) DNA damage and ageing: new-age ideas for an age-old problem. Nat. Cell Biol. 10, 1241-1247
32. Deupree, D. L., Bradley, J., and Turner, D. A. (1993) Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol. Aging 14, 249-258 (Pubitemid 23161546)
33. Nicholson, D. A., Yoshida, R., Berry, R. W., Gallagher, M., and Geinisman, Y. (2004) Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J. Neurosci. 24, 7648-7653 (Pubitemid 39186819)
34. Geinisman, Y., deToledo-Morrell, L., Morrell, F., Persina, I. S., and Rossi, M. (1992) Age-related loss of axospinous synapses formed by two afferent systems in the rat dentate gyrus as revealed by the unbiased stereological dissector technique. Hippocampus 2, 437-444