Genome-wide expression profiling and functional characterization of SCA28 lymphoblastoid cell lines reveal impairment in cell growth and activation of apoptotic pathways

BMC Medical Genomics

Volumn 6, Issue 1, 2013, Pages

  Mancini, Cecilia ^a   Roncaglia, Paola ^b,c   Brussino, Alessandro ^a   Stevanin, Giovanni ^d   Lo Buono, Nicola ^a   Krmac, Helena ^c   Maltecca, Francesca ^e   Gazzano, Elena ^a   Bartoletti Stella, Anna ^f   Calvaruso, Maria Antonietta ^f,g   Iommarini, Luisa ^f   Cagnoli, Claudia ^a   Forlani, Sylvie ^d   Le Ber, Isabelle ^d   Durr, Alexandra ^d   Brice, Alexis ^d   Ghigo, Dario ^a   Casari, Giorgio ^e   Porcelli, Anna Maria ^f   Funaro, Ada ^a   Gasparre, Giuseppe ^f   Gustincich, Stefano ^c   Brusco, Alfredo ^a,g   more..

^a UNIVERSITY OF TURIN   (Italy)

^b EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^c SISSA   (Italy)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^e VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^f UNIVERSITY OF BOLOGNA   (Italy)

^g CITTÀ DELLA SALUTE E DELLA SCIENZA HOSPITAL   (Italy)

Author keywords

AFG3L2; Autosomal dominant cerebellar ataxia; Genome wide expression; LCLs; SCA28; Spinocerebellar ataxia

Indexed keywords

DRP1 PROTEIN; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; REACTIVE OXYGEN METABOLITE; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANALYTICAL EQUIPMENT; APOPTOSIS; ARTICLE; CASE REPORT; CELL ACTIVATION; CELL ADHESION; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL FUNCTION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC ASSOCIATION; HOMEOSTASIS; HUMAN; HUMAN CELL; LIPID PEROXIDATION; LYMPHOBLASTOID CELL; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY CHAIN; SCA28 GENE; SPECTROPHOTOMETER; UPREGULATION; VALIDATION STUDY;

APOPTOSIS; ATP-DEPENDENT PROTEASES; CELL LINE, TUMOR; CELL PROLIFERATION; DNA-BINDING PROTEINS; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION PROFILING; GENOME, HUMAN; GTP PHOSPHOHYDROLASES; HUMANS; LIPID PEROXIDATION; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PHENOTYPE; SPINOCEREBELLAR DEGENERATIONS; TRANSCRIPTION FACTORS;

EID: 84879059801     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/1755-8794-6-22     Document Type: Article

References (51)

1. Autosomal dominant cerebellar ataxias: polyglutamine expansions and beyond. Durr A, Lancet Neurol 2010 9 9 885 894 10.1016/S1474-4422(10)70183-6 20723845
2. SCA28, a novel form of autosomal dominant cerebellar ataxia on chromosome 18p11.22-q11.2. Cagnoli C, Mariotti C, Taroni F, Seri M, Brussino A, Michielotto C, Grisoli M, Di Bella D, Migone N, Gellera C, et al. Brain 2006 129 Pt 1 235 242 16251216 (Pubitemid 43063774)
3. Mutations in the mitochondrial protease gene AFG3L2 cause dominant hereditary ataxia SCA28. Di Bella D, Lazzaro F, Brusco A, Plumari M, Battaglia G, Pastore A, Finardi A, Cagnoli C, Tempia F, Frontali M, et al. Nat Genet 2010 42 4 313 321 10.1038/ng.544 20208537
4. Missense mutations in the AFG3L2 proteolytic domain account for approximately 1.5% of European autosomal dominant cerebellar ataxias. Cagnoli C, Stevanin G, Brussino A, Barberis M, Mancini C, Margolis RL, Holmes SE, Nobili M, Forlani S, Padovan S, et al. Hum Mutat 2010 31 10 1117 1124 10.1002/humu.21342 20725928
5. Early onset and slow progression of SCA28, a rare dominant ataxia in a large four-generation family with a novel AFG3L2 mutation. Edener U, Wollner J, Hehr U, Kohl Z, Schilling S, Kreuz F, Bauer P, Bernard V, Gillessen-Kaesbach G, Zuhlke C, Eur J Hum Genet 2010 18 8 965 968 10.1038/ejhg.2010.40 20354562
6. Identification and characterization of AFG3L2, a novel paraplegin-related gene. Banfi S, Bassi MT, Andolfi G, Marchitiello A, Zanotta S, Ballabio A, Casari G, Franco B, Genomics 1999 59 1 51 58 10.1006/geno.1999.5818 10395799 (Pubitemid 29339872)
7. Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Leonhard K, Stiegler A, Neupert W, Langer T, Nature 1999 398 6725 348 351 10.1038/18704 10192337 (Pubitemid 29161691)
8. The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Arlt H, Tauer R, Feldmann H, Neupert W, Langer T, Cell 1996 85 6 875 885 10.1016/S0092-8674(00)81271-4 8681382 (Pubitemid 26192138)
9. Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Leonhard K, Guiard B, Pellecchia G, Tzagoloff A, Neupert W, Langer T, Mol Cell 2000 5 4 629 638 10.1016/S1097-2765(00)80242-7 10882099
10. The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria. Nolden M, Ehses S, Koppen M, Bernacchia A, Rugarli EI, Langer T, Cell 2005 123 2 277 289 10.1016/j.cell.2005.08.003 16239145 (Pubitemid 41457217)
11. Autocatalytic processing of m-AAA protease subunits in mitochondria. Koppen M, Bonn F, Ehses S, Langer T, Mol Biol Cell 2009 20 19 4216 4224 10.1091/mbc.E09-03-0218 19656850
12. Mitochondrial AAA proteases-Towards a molecular understanding of membrane-bound proteolytic machines. Gerdes F, Tatsuta T, Langer T, Biochim Biophys Acta 2011 1823 1 49 55 22001671
13. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Casari G, De Fusco M, Ciarmatori S, Zeviani M, Mora M, Fernandez P, De Michele G, Filla A, Cocozza S, Marconi R, et al. Cell 1998 93 6 973 983 10.1016/S0092-8674(00)81203-9 9635427 (Pubitemid 28280791)
14. Whole-exome sequencing identifies homozygous AFG3L2 mutations in a spastic ataxia-neuropathy syndrome linked to mitochondrial m-AAA proteases. Pierson TM, Adams D, Bonn F, Martinelli P, Cherukuri PF, Teer JK, Hansen NF, Cruz P, Blakesley RW, Mullikin For The Nisc Comparative Sequencing Program JC, et al. PLoS Genet 2011 7 10 1002325 10.1371/journal.pgen.1002325 22022284
15. Spastic paraplegia gene 7 in patients with spasticity and/or optic neuropathy. Klebe S, Depienne C, Gerber S, Challe G, Anheim M, Charles P, Fedirko E, Lejeune E, Cottineau J, Brusco A, et al. Brain 2012 135 Pt 10 2980 2993 23065789
16. The mitochondrial protease AFG3L2 is essential for axonal development. Maltecca F, Aghaie A, Schroeder DG, Cassina L, Taylor BA, Phillips SJ, Malaguti M, Previtali S, Guenet JL, Quattrini A, et al. J Neurosci 2008 28 11 2827 2836 10.1523/JNEUROSCI.4677-07.2008 18337413 (Pubitemid 351398887)
17. Haploinsufficiency of AFG3L2, the gene responsible for spinocerebellar ataxia type 28, causes mitochondria-mediated Purkinje cell dark degeneration. Maltecca F, Magnoni R, Cerri F, Cox GA, Quattrini A, Casari G, J Neurosci 2009 29 29 9244 9254 10.1523/JNEUROSCI.1532-09.2009 19625515
18. Bioconductor http://www.bioconductor.org
19. MultiExperiment Viewer http://www.tm4.org/mev/
20. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. Breitling R, Armengaud P, Amtmann A, Herzyk P, FEBS Lett 2004 573 1-3 83 92 15327980 (Pubitemid 39141040)
21. Significance analysis of microarrays applied to the ionizing radiation response. Tusher VG, Tibshirani R, Chu G, Proc Natl Acad Sci USA 2001 98 9 5116 5121 10.1073/pnas.091062498 11309499 (Pubitemid 32397092)
22. Gene ontology: tool for the unification of biology, The Gene Ontology Consortium. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Nat Genet 2000 25 1 25 29 10.1038/75556 10802651 (Pubitemid 30257031)
23. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. da Huang W, Sherman BT, Lempicki RA, Nat Protoc 2009 4 1 44 57 19131956
24. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. da Huang W, Sherman BT, Lempicki RA, Nucleic Acids Res 2009 37 1 1 13 10.1093/nar/gkn923 19033363
25. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA, Genome Biol 2003 4 5 3 10.1186/gb-2003-4-5-p3 12734009
26. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Livak KJ, Schmittgen TD, Methods 2001 25 4 402 408 10.1006/meth.2001.1262 11846609 (Pubitemid 34164012)
27. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Mosmann T, J Immunol Methods 1983 65 1-2 55 63 6606682 (Pubitemid 14203433)
28. Overview of flow cytometry and fluorescent probes for flow cytometry. Cunningham RE, Methods Mol Biol 2010 588 319 326 10.1007/978-1-59745-324-0-31 20012842
29. A novel assay for apoptosis, Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C, J Immunol Methods 1995 184 1 39 51 10.1016/0022-1759(95)00072-I 7622868
30. Expression and purification of recombinant annexin V for the detection of membrane alterations on apoptotic cells. Brumatti G, Sheridan C, Martin SJ, Methods 2008 44 3 235 240 10.1016/j.ymeth.2007.11.010 18314054 (Pubitemid 351296441)
31. Use of fibroblast and lymphoblast cultures for detection of respiratory chain defects. Robinson BH, Methods Enzymol 1996 264 454 464 8965718
32. Luminometric assays of ATP, phosphocreatine, and creatine for estimation of free ADP and free AMP. Ronner P, Friel E, Czerniawski K, Frankle S, Anal Biochem 1999 275 2 208 216 10.1006/abio.1999.4317 10552906
33. Caspase-independent death of Leber's hereditary optic neuropathy cybrids is driven by energetic failure and mediated by AIF and Endonuclease G. Zanna C, Ghelli A, Porcelli AM, Martinuzzi A, Carelli V, Rugolo M, Apoptosis 2005 10 5 997 1007 10.1007/s10495-005-0742-5 16151635 (Pubitemid 41285578)
34. Mineral fiber-induced malondialdehyde formation and effects of oxidant scavengers in phagocytic cells. Yano E, Int Arch Occup Environ Health 1988 61 1-2 19 23 2848774 (Pubitemid 19001463)
35. Revisiting the issue of mitochondrial DNA content in optic mitochondriopathies. Iommarini L, Maresca A, Caporali L, Valentino ML, Liguori R, Giordano C, Carelli V, Neurology 2012 79 14 1517 1519 10.1212/WNL. 0b013e31826d5f72 22993283
36. Detection and characterization of mitochondrial DNA rearrangements in Pearson and Kearns-Sayre syndromes by long PCR. Kleinle S, Wiesmann U, Superti-Furga A, Krahenbuhl S, Boltshauser E, Reichen J, Liechti-Gallati S, Hum Genet 1997 100 5-6 643 650 9341886 (Pubitemid 28072370)
37. Mouse brain expression patterns of Spg7, Afg3l1, and Afg3l2 transcripts, encoding for the mitochondrial m-AAA protease. Sacco T, Boda E, Hoxha E, Pizzo R, Cagnoli C, Brusco A, Tempia F, BMC Neurosci 2010 11 55 10.1186/1471-2202-11- 55 20426821
38. National Center for Biotechnology Information http://www.ncbi.nlm.nih.gov
39. Allelic variation in human gene expression. Yan H, Yuan W, Velculescu VE, Vogelstein B, Kinzler KW, Science 2002 297 5584 1143 10.1126/science.1072545 12183620 (Pubitemid 36193340)
40. Natural variation in human gene expression assessed in lymphoblastoid cells. Cheung VG, Conlin LK, Weber TM, Arcaro M, Jen KY, Morley M, Spielman RS, Nat Genet 2003 33 3 422 425 10.1038/ng1094 12567189 (Pubitemid 36278862)
41. Gene expression profiling in human neurodegenerative disease. Cooper-Knock J, Kirby J, Ferraiuolo L, Heath PR, Rattray M, Shaw PJ, Nat Rev Neurol 2012 8 9 518 530 10.1038/nrneurol.2012.156 22890216
42. Cell division in the CNS: protective response or lethal event in post-mitotic neurons? Yang Y, Herrup K, Biochim Biophys Acta 2007 1772 4 457 466 10.1016/j.bbadis.2006.10.002 17158035 (Pubitemid 46420409)
43. Cell cycle dependent morphology changes and associated mitochondrial DNA redistribution in mitochondria of human cell lines. Margineantu DH, Gregory Cox W, Sundell L, Sherwood SW, Beechem JM, Capaldi RA, Mitochondrion 2002 1 5 425 435 10.1016/S1567-7249(02)00006-5 16120295 (Pubitemid 34461241)
44. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. Parone PA, Da Cruz S, Tondera D, Mattenberger Y, James DI, Maechler P, Barja F, Martinou JC, PLoS One 2008 3 9 3257 10.1371/journal.pone.0003257 18806874
45. Identification of a novel putative non-selenocysteine containing phospholipid hydroperoxide glutathione peroxidase (NPGPx) essential for alleviating oxidative stress generated from polyunsaturated fatty acids in breast cancer cells. Utomo A, Jiang X, Furuta S, Yun J, Levin DS, Wang YC, Desai KV, Green JE, Chen PL, Lee WH, J Biol Chem 2004 279 42 43522 43529 10.1074/jbc.M407141200 15294905 (Pubitemid 39390652)
46. Pituitary adenylate cyclase-activating polypeptide protects astroglial cells against oxidative stress-induced apoptosis. Masmoudi-Kouki O, Douiri S, Hamdi Y, Kaddour H, Bahdoudi S, Vaudry D, Basille M, Leprince J, Fournier A, Vaudry H, et al. J Neurochem 2011 117 3 403 411 10.1111/j.1471-4159.2011.07185.x 21244427
47. FOXO3a regulates reactive oxygen metabolism by inhibiting mitochondrial gene expression. Ferber EC, Peck B, Delpuech O, Bell GP, East P, Schulze A, Cell Death Differ 2012 19 6 968 979 10.1038/cdd.2011.179 22139133
48. Evidence for mitochondrial DNA damage by lipid peroxidation. Hruszkewycz AM, Biochem Biophys Res Commun 1988 153 1 191 197 10.1016/S0006-291X(88)81207-5 2837198
49. Lipid peroxidation triggers neurodegeneration: A redox proteomics view into the Alzheimer disease brain. Sultana R, Perluigi M, Allan Butterfield D, Free Radic Biol Med 2012 S0891-5849 12 01161-01166
50. Mitochondrial transcription factor A (TFAM): roles in maintenance of mtDNA and cellular functions. Kang D, Kim SH, Hamasaki N, Mitochondrion 2007 7 1-2 39 44 17280879 (Pubitemid 46351974)
51. TFAM-dependent and independent dynamics of mtDNA levels in C2C12 myoblasts caused by redox stress. Noack H, Bednarek T, Heidler J, Ladig R, Holtz J, Szibor M, Biochim Biophys Acta 2006 1760 2 141 150 10.1016/j.bbagen.2005.12. 007 16439064 (Pubitemid 43320501)