Increased chromosome instability dramatically disrupts neural genome integrity and mediates cerebellar degeneration in the ataxia-telangiectasia brain

Human Molecular Genetics

Volumn 18, Issue 14, 2009, Pages 2656-2669

  Iourov, Ivan Y ^a,b   Vorsanova, Svetlana G ^a,b   Liehr, Thomas ^c   Kolotii, Alexei D ^b   Yurov, Yuri B ^a,b  

^a MENTAL HEALTH RESEARCH CENTER   (Russian Federation)

^b PIROGOV RUSSIAN NATIONAL RESEARCH MEDICAL UNIVERSITY   (Russian Federation)

^c Institute of Human Genetics and Anthropology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR FOXG1B; NEURO ONCOLOGICAL VENTRAL ANTIGEN 1; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ANEUPLOIDY; ARTICLE; ATAXIA TELANGIECTASIA; BRAIN; CEREBELLUM; CEREBELLUM DEGENERATION; CHILD; CHROMOSOMAL INSTABILITY; CHROMOSOME 14; CHROMOSOME 14Q; CHROMOSOME 7; CHROMOSOME BREAKAGE; CHROMOSOME MAP; CHROMOSOME MARKER; CHROMOSOME REARRANGEMENT; CLINICAL ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; GENE LOCUS; GENOMIC INSTABILITY; HUMAN; HUMAN TISSUE; MALE; NEOPLASM; NERVE CELL; PRIORITY JOURNAL; PROMOTER REGION; SCHOOL CHILD; X CHROMOSOME;

ADULT; ANEUPLOIDY; ATAXIA TELANGIECTASIA; CASE-CONTROL STUDIES; CEREBELLUM; CHROMOSOMAL INSTABILITY; CHROMOSOME BREAKAGE; CHROMOSOMES, HUMAN, PAIR 14; FEMALE; GENOMIC INSTABILITY; HUMANS; MALE; NEURONS; YOUNG ADULT;

ATAXIA TELANGIECTASIA;

EID: 67649859655     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp207     Document Type: Article

References (50)

1. Gatti, R.A. (1998) Ataxia-telangiectasia. McGraw-Hill, New York, NY.
2. McKinnon, P.J. (2004) ATM and ataxia telangiectasia. EMBO Rep., 5, 772-776.
3. Kulkarni, A. and Wilson, D.M. III (2008) The involvement of DNA-damage and -repair defects in neurological dysfunction. Am. J. Hum. Genet. 82, 539-566.
4. Jones, J.M. and Gellert, M. (2004) The timing of transposon: V(D)J recombination and the immune system. Immunol. Rev., 200, 233-248.
5. Kojis, T.L., Schreck, R.R., Gatti, R.A. and Sparkes, R.S. (1989) Tissue specificity of chromosome rearrangements in ataxia-telangiectasia. Hum. Genet., 83, 347-352.
6. Gao, Y., Sun, Y., Frank, K.M., Dikkes, P., Fujiwara, Y., Bronson, R.T., Malynn, B.A., Bryans, M., Zhu, C., Chaudhuri, J. et al. (1998) A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell, 95, 891-902.
7. Wu, Q. and Maniatis, T. (1999) A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell, 97, 779-790.
8. Silva, E., Tiong, S., Pedersen, M., Homola, E., Royou, A., Fasulo, B., Siriaco, G. and Campbell, S. (2004) ATM is required for telomere maintenance and chromosome stability during Drosophila development. Curr. Biol., 14, 1341-1347.
9. Allen, D.M., Praag van, H., Ray, J., Weaver, Z., Winrow, C.J., Carter, T.A., Braquet, R., Harrington, E., Ried, T., Brown, K.D. et al. (2001) Ataxia telangiectasia mutated is essential during adult neurogenesis. Genes Dev., 15, 554-566.
10. McConnell, M.J., Kaushal, D., Yang, A.H., Kingsbury, M.A., Rehen, S.K., Treuner, K., Helton, R., Annas, E.G., Chun, J. and Barlow, C. (2004) Failed clearance of aneuploidy embryonic neural progenitor cells leads to excess aneuploidy in the Atm-deficient but not the Trp53-deficient adult cerebral cortex. J. Neurosci., 24, 8090-8096.
11. Frappart, P.O. and McKinnon, P.J. (2006) Ataxia-telangiectasia and related diseases. Neuromol Med., 8, 495-511.
12. Iourov, Y., Vorsanova, S.G., Liehr, T. and Yurov, Y.B. (2009) Aneuploidy in the normal, Alzheimer's disease and ataxia-telangiectasia brain: differential expression and pathological meaning. Neurobiol. Dis., 34, 212-220.
13. Iourov, I.Y., Liehr, T., Vorsanova, S.G., Kolotii, A.D. and Yurov, Y.B. (2006) Visualization of interphase chromosomes of the human brain by multicolour banding (MCB). Chromosome Res., 14, 223-229.
14. Iourov, I.Y., Liehr, T., Vorsanova, S.G. and Yurov, Y.B. (2007) Interphase chromosome-specific multicolor banding (ICS-MCB): A new tool for analysis of interphase chromosomes in their integrity. Biomol. Eng., 24, 415-417.
15. Katyal, S. and McKinnon, P.J. (2008) DNA strand breaks, neurodegeneration and aging in the brain. Mech. Ageing Dev., 129, 483-491.
16. Iourov, I.Y., Vorsanova, S.G. and Yurov, Y.B. (2007) Ataxia telangiectasia paradox can be explained by chromosome instability at the subtissue level. Med. Hypotheses, 68, 716.
17. Herzog, K.H., Chong, M.J., Kapsetaki, M., Morgan, J.I. and McKinnon, P.J. (1998) Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science, 280, 1089-1091.
18. Rehen, S.K., McConnel, M.J., Kaushal, D., Kingsbury, M.A., Yang, A.H. and Chun, J. (2001) Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proc. Natl. Acad. Sci. USA, 98, 13361-13366.
19. Yurov, Y.B., Iourov, I.Y., Vorsanova, S.G., Liehr, T., Kolotii, A.D., Kutsev, S.I., Pellestor, F., Beresheva, A.K., Demidova, I.A., Kravets, V.S. et al. (2007) Aneuploidy and confined chromosomal mosaicism in the developing human brain. PloS ONE, 2, e558.
20. Orii, K.E., Lee, Y., Kondo, N. and McKinnon, P.J. (2006) Selective utilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development. Proc. Natl. Acad. Sci. USA, 103, 10017-10022.
21. Ariani, F., Hayek, G., Rondinella, D., Artuso, R., Mencarelli, A., Spanhol-Rosseto, A., Pollazzon, M., Buoni, S., Spiga, O., Ricciardi, S. et al. (2008) FOXG1 is responsible for the congenital variant of Rett syndrome. Am. J. Hum. Genet., 83, 89-93.
22. Papa, F.T., Mencarelli, M.A., Caselli, R., Katzaki, E., Sampieri, K., Meloni, I., Ariani, F., Longo, I., Maggio, A., Balestri, P. et al. (2008) A 3 Mb deletion in 14q12 causes severe mental retardation, mild facial dysmorphisms and Rett-like features. Am. J. Med. Genet., 146A, 1994-1998.
23. Shoichet, S.A., Kunde, S.A., Viertel, P., Schell-Apacik, C., von Voss, H., Tommerup, N., Ropers, H.H. and Kalscheuer, V.M. (2005) Haploinsufficiency of novel FOXG1B variants in a patient with severe mental retardation, brain malformations and microcephaly. Hum. Genet. 117, 536-544.
24. Buckanovich, R.J., Posner, J.B. and Darnell, R.B. (1993) Nova, the paraneoplastic Ri antigen, is homologous to an RNA-binding protein and is specifically expressed in the developing motor system. Neuron, 11, 657-672.
25. Jelen, N., Ule, J., Zivin, M. and Darnell, R.B. (2007) Evolution of Nova-dependent splicing regulation in the brain. PLoS Genet., 3 e173.
26. Licatalosi, D.D. and Darnell, R.B. (2006) Splicing regulation in neurologic disease. Neuron, 52, 93-101.
27. Pagani, F., Buratti, E., Stuani, C., Bendix, R., Dörk, T. and Baralle, F.E. (2002) A new type of mutation causes a splicing defect in ATM. Nat. Genet., 30, 426-429.
28. Vanasse, G.J., Concannon, P. and Willerford, D.M. (1999) Regulated genomic instability and neoplasia in the lymphoid lineage. Blood, 94, 3997-4010.
29. Curtis, M.A., Penney, E.B., Pearson, A.G., van Roon-Mom, W.M.C., Buttenworth, N.J., Dragunow, M., Connor, B. and Faull, R.L. (2003) Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc. Natl. Acad. Sci. USA, 100, 9023-9027.
30. Jin, K., Peel, A.L., Mao, X.O., Xie, L., Cottrell, B., Henshall, D.C. and Greenberg, D.A. (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. USA, 101, 343-347.
31. Ponti, G., Peretto, P. and Bonfanti, L. (2008) Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. Plos ONE, 3, e2366.
32. Muotri, A.R. and Gage, F.H. (2006) Generation of neuronal variability and complexity. Nature, 441, 903-910.
33. Mezey, E., Chandross, K.J., Harta, G., Maki, R.A. and McKercher, S.R. (2000) Turning blood into brain: Cells bearing neuronal antigens generated in vivo from bone marrow. Science, 290, 1779-1782.
34. Mezey, E., Key, S., Vogelsang, G., Szalayova, I., Lange, D.G. and Crain, B. (2003) Transplanted bone marrow generates new neurons in human brains. Proc. Natl. Acad. Sci. USA, 100, 1364-1369.
35. Weimann, J.M., Charlton, C.A., Brazelton, T.R., Hackman, R.C. and Blau, H.M. (2003) Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brain. Proc. Natl. Acad. Sci. USA, 100 2088-2093.
36. Iourov, I.Y., Vorsanova, S.G. and Yurov, Y.B. (2006) Chromosomal variations in mammalian neuronal cells: Known facts and attractive hypotheses. Int. Rev. Cytol., 249, 143-191.
37. Iourov, I., Vorsanova, S.G. and Yurov, Y.B. (2006) Intercellular genomic (chromosomal) variations resulting in somatic mosaicism: Mechanisms and consequences. Curr. Genomics, 7, 435-446.
38. Kingsbury, M.A., Yung, Y.C., Peterson, S.E., Westra, J.W. and Chun, J. (2006) Aneuploidy in the normal and diseased brain. Cell. Mol. Life. Sci., 63, 2626-2641.
39. Yurov, Y.B., Vorsanova, S.G., Iourov, I.Y., Demidova, I.A., Beresheva, A.K., Kravetz, V.S., Monakhov, V.V., Kolotii, A.D., Voinova-Ulas, V.Y. and Gorbachevskaya, N.L. (2007) Unexplained autism is frequently associated with low-level mosaic aneuploidy. J. Med. Genet., 44 521-535.
40. Yurov, Y.B., Iourov, I.Y., Vorsanova, S.G., Demidova, I.A., Kravetz, V.S., Beresheva, A.K., Kolotii, A.D., Monakchov, V.V., Uranova, N.A., Vostrikov, V.M. et al. (2008) The schizophrenia brain exhibits low-level aneuploidy involving chromosome 1. Schizophr. Res., 98, 137-147.
41. Iourov, I.Y., Vorsanova, S.G. and Yurov, Y.B. (2008) Molecular cytogenetics and cytogenomics of brain diseases. Curr. Genomics, 9, 452-465.
42. Iourov, I.Y., Vorsanova, S.G., Pellestor, F. and Yurov, Y.B. (2006) Brain tissue preparation for chromosomal PRINS labeling. Methods Mol. Biol., 334, 123-132.
43. Yurov, Y.B., Vosrtikov, V.M., Vorsanova, S.G., Monakhov, V.V. and Iourov, I.Y. (2001) Multicolor fluorescent in situ hybridization on post mortem brain in schizophrenia as an approach for identification of low-level chromosomal aneuploidy in neuropsychiatric diseases. Brain Dev., 23, S186-S190.
44. Yurov, Y.B., Iourov, I.Y., Monackhov, V.V., Soloviev, I.V., Vostrikov, V.M. and Vorsanova, S.G. (2005) The variation of aneuploidy frequency in the developing and adult human brain revealed by an interphase FISH study. J. Histochem. Cytochem., 53, 385-390.
45. Soloviev, I.V., Yurov, Y.B., Vorsanova, S.G., Fayet, F., Roizes, G. and Malet, P. (1995) Prenatal diagnosis of trisomy 21 using interphase fluorescence in situ hybridization of post-replicated cells with site-specific cosmid and cosmid contig probes. Prenat. Diagn., 15, 237-248.
46. Yurov, Y.B., Soloviev, I.V., Vorsanova, S.G., Marcais, B., Roizes, G. and Lewis, R. (1996) High resolution fluorescence in situ hybridization using cyanine and fluorescein dyes: Ultra-rapid chromosome detection by directly fluorescently labeled alphoid DNA probes. Hum. Genet., 97, 390-398.
47. Vorsanova, S.G., Kolotii, A.D., Iourov, I.Y., Monakhov, V.V., Kirillova, E.A., Soloviev, I.V. and Yurov, Y.B. (2005) Evidence for high frequency of chromosomal mosaicism in spontaneous abortions revealed by interphase FISH analysis. J. Histochem. Cytochem., 53, 375-380.
48. Liehr, T., Heller, A., Starke, H., Rubtsov, N., Trifonov, V., Mrasek, K., Weise, A., Kuechler, A. and Claussen, U. (2002) Microdissection based high resolution multicolor banding for all 24 human chromosomes. Int. J. Mol. Med., 9, 335-339.
49. Lemke, J., Claussen, J., Michel, S., Chudoba, I., Mühlig, P., Westermann, M., Sperling, K., Rubtsov, N., Grummt, U.W., Ullmann, P. et al. (2002) The DNA-based structure of human chromosome 5 in interphase. Am. J. Hum. Genet., 71, 1051-1059.
50. Iourov, I.Y., Soloviev, I.V., Vorsanova, S.G., Monakhov, V.V. and Yurov, Y.B. (2005) An approach for quantitative assessment of fluorescence in situ hybridization (FISH) signals for applied human molecular cytogenetics. J. Histochem. Cytochem., 53, 401-408.