Mitochondrial Oxidative Phosphorylation Transcriptome Alterations in Human Amyotrophic Lateral Sclerosis Spinal Cord and Blood

NeuroMolecular Medicine

Volumn 16, Issue 4, 2014, Pages 714-726

  Ladd, Amy C ^a   Keeney, Paula M ^a   Govind, Maria M ^a   Bennett, James P ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

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

Author keywords

ALS; Mitochondria; Oxidative phosphorylation; Peripheral blood; Quantitative PCR; Spinal cord

Indexed keywords

MESSENGER RNA; MITOCHONDRIAL DNA; TRANSCRIPTION FACTOR; TRANSCRIPTOME; ZALCITABINE;

AGED; AMYOTROPHIC LATERAL SCLEROSIS; BIOSYNTHESIS; DRUG EFFECTS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; MIDDLE AGED; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL GENE; MITOCHONDRION; MONONUCLEAR CELL; NEURAL STEM CELL; OXIDATIVE PHOSPHORYLATION; PHYSIOLOGY; SPINAL CORD;

AGED; AMYOTROPHIC LATERAL SCLEROSIS; DNA, MITOCHONDRIAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, MITOCHONDRIAL; HUMANS; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; MITOCHONDRIA; MITOCHONDRIAL TURNOVER; NEURAL STEM CELLS; OXIDATIVE PHOSPHORYLATION; RNA, MESSENGER; SPINAL CORD; TRANSCRIPTION FACTORS; TRANSCRIPTOME; ZALCITABINE;

EID: 84928101986     PISSN: 15351084     EISSN: 15591174     Source Type: Journal    
DOI: 10.1007/s12017-014-8321-y     Document Type: Article

References (46)

1. Bernardini, C., Censi, F., Lattanzi, W., Barba, M., Calcagnini, G., Giuliani, A., et al. (2013). Mitochondrial network genes in the skeletal muscle of amyotrophic lateral sclerosis patients. PLoS ONE,8(2), e57739. doi:10.1371/journal.pone.0057739.
2. Bindoff, L. A., Birch-Machin, M. A., Cartlidge, N. E., Parker, W. D., Jr, & Turnbull, D. M. (1991). Respiratory chain abnormalities in skeletal muscle from patients with Parkinson’s disease. Journal of the Neurological Sciences,104(2), 203–208.
3. Boillee, S., Vande Velde, C., & Cleveland, D. W. (2006). ALS: A disease of motor neurons and their nonneuronal neighbors. Neuron,52(1), 39–59. doi:10.1016/j.neuron.2006.09.018.
4. Brockington, A., Ning, K., Heath, P. R., Wood, E., Kirby, J., Fusi, N., et al. (2013). Unravelling the enigma of selective vulnerability in neurodegeneration: Motor neurons resistant to degeneration in ALS show distinct gene expression characteristics and decreased susceptibility to excitotoxicity. Acta Neuropathologica,125(1), 95–109. doi:10.1007/s00401-012-1058-5.
5. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., et al. (2009). The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry,55(4), 611–622. doi:10.1373/clinchem.2008.112797.
6. Cassina, P., Cassina, A., Pehar, M., Castellanos, R., Gandelman, M., de Leon, A., et al. (2008). Mitochondrial dysfunction in SOD1G93A-bearing astrocytes promotes motor neuron degeneration: Prevention by mitochondrial-targeted antioxidants. Journal of Neuroscience,28(16), 4115–4122. doi:10.1523/JNEUROSCI.5308-07.2008.
7. Chandrasekaran, K., Giordano, T., Brady, D. R., Stoll, J., Martin, L. J., & Rapoport, S. I. (1994). Impairment in mitochondrial cytochrome oxidase gene expression in Alzheimer disease. Brain Research. Molecular Brain Research,24(1–4), 336–340.
8. Chen, C. H., & Cheng, Y. C. (1989). Delayed cytotoxicity and selective loss of mitochondrial DNA in cells treated with the anti-human immunodeficiency virus compound 2′,3′-dideoxycytidine. Journal of Biological Chemistry,264(20), 11934–11937.
9. Clement-Ziza, M., Gentien, D., Lyonnet, S., Thiery, J. P., Besmond, C., & Decraene, C. (2009). Evaluation of methods for amplification of picogram amounts of total RNA for whole genome expression profiling. BMC Genomics,10, 246. doi:10.1186/1471-2164-10-246.
10. Cozzolino, M., & Carri, M. T. (2012). Mitochondrial dysfunction in ALS. Progress in Neurobiology,97(2), 54–66. doi:10.1016/j.pneurobio.2011.06.003.
11. Dangond, F., Hwang, D., Camelo, S., Pasinelli, P., Frosch, M. P., Stephanopoulos, G., et al. (2004). Molecular signature of late-stage human ALS revealed by expression profiling of postmortem spinal cord gray matter. Physiological Genomics,16(2), 229–239. doi:10.1152/physiolgenomics.00087.2001.
12. DeJesus-Hernandez, M., Mackenzie, I. R., Boeve, B. F., Boxer, A. L., Baker, M., Rutherford, N. J., et al. (2011). Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron,72(2), 245–256. doi:10.1016/j.neuron.2011.09.011.
13. Denisov, V., Strong, W., Walder, M., Gingrich, J., & Wintz, H. (2008). In I. Bio-Rad Laboratories (Ed.), Development and validation of RQI: An RNA quality indicator for the experionTM automated electrophoresis system (Vol. Bulletin 5761 Rev B). BioRad. http://www.gene-quantification.com/Bio-Rad-bulletin-5761.pdf.
14. Dupuis, L., Pradat, P. F., Ludolph, A. C., & Loeffler, J. P. (2011). Energy metabolism in amyotrophic lateral sclerosis. Lancet Neurology,10(1), 75–82. doi:10.1016/S1474-4422(10)70224-6.
15. Fujita, K., Yamauchi, M., Shibayama, K., Ando, M., Honda, M., & Nagata, Y. (1996). Decreased cytochrome c oxidase activity but unchanged superoxide dismutase and glutathione peroxidase activities in the spinal cords of patients with amyotrophic lateral sclerosis. Journal of Neuroscience Research,45(3), 276–281. doi:10.1002/(SICI)1097-4547(19960801)45:3<276:AID-JNR9>3.0.CO;2-A.
16. Hall, E. D., Oostveen, J. A., & Gurney, M. E. (1998). Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia,23(3), 249–256.
17. Heath, P. R., Kirby, J., & Shaw, P. J. (2013). Investigating cell death mechanisms in amyotrophic lateral sclerosis using transcriptomics. Frontiers in Cellular Neuroscience,7, 259. doi:10.3389/fncel.2013.00259.
18. Hedlund, E., Karlsson, M., Osborn, T., Ludwig, W., & Isacson, O. (2010). Global gene expression profiling of somatic motor neuron populations with different vulnerability identify molecules and pathways of degeneration and protection. Brain,133(Pt 8), 2313–2330. doi:10.1093/brain/awq167.
19. Henriques, A., & Gonzalez De Aguilar, J. L. (2011). Can transcriptomics cut the gordian knot of amyotrophic lateral sclerosis? Current Genomics,12(7), 506–515. doi:10.2174/138920211797904043.
20. Jiang, Y. M., Yamamoto, M., Kobayashi, Y., Yoshihara, T., Liang, Y., Terao, S., et al. (2005). Gene expression profile of spinal motor neurons in sporadic amyotrophic lateral sclerosis. Annals of Neurology,57(2), 236–251. doi:10.1002/ana.20379.
21. Keeney, P. M., & Bennett, J. P., Jr. (2010). ALS spinal neurons show varied and reduced mtDNA gene copy numbers and increased mtDNA gene deletions. Molecular Neurodegenerative,5, 21. doi:10.1186/1750-1326-5-21.
22. Kish, S. J., Bergeron, C., Rajput, A., Dozic, S., Mastrogiacomo, F., Chang, L. J., et al. (1992). Brain cytochrome oxidase in Alzheimer’s disease. Journal of Neurochemistry,59(2), 776–779.
23. Kwiatkowski, T. J., Jr, Bosco, D. A., Leclerc, A. L., Tamrazian, E., Vanderburg, C. R., Russ, C., et al. (2009). Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science,323(5918), 1205–1208. doi:10.1126/science.1166066.
24. Malaspina, A., & de Belleroche, J. (2004). Spinal cord molecular profiling provides a better understanding of amyotrophic lateral sclerosis pathogenesis. Brain Research. Brain Research Reviews,45(3), 213–229. doi:10.1016/j.brainresrev.2004.04.002.
25. Malaspina, A., Kaushik, N., & de Belleroche, J. (2001). Differential expression of 14 genes in amyotrophic lateral sclerosis spinal cord detected using gridded cDNA arrays. Journal of Neurochemistry,77(1), 132–145.
26. Mytilineou, C., Werner, P., Molinari, S., Di Rocco, A., Cohen, G., & Yahr, M. D. (1994). Impaired oxidative decarboxylation of pyruvate in fibroblasts from patients with Parkinson’s disease. Journal of Neural Transmission. Parkinson’s Disease and Dementia Section,8(3), 223–228.
27. Parker, W. D., Jr, Boyson, S. J., & Parks, J. K. (1989). Abnormalities of the electron transport chain in idiopathic Parkinson’s disease. Annals of Neurology,26(6), 719–723. doi:10.1002/ana.410260606.
28. Penna, I., Vella, S., Gigoni, A., Russo, C., Cancedda, R., & Pagano, A. (2011). Selection of candidate housekeeping genes for normalization in human postmortem brain samples. International Journal of Molecular Sciences,12(9), 5461–5470. doi:10.3390/ijms12095461.
29. Philips, T., Bento-Abreu, A., Nonneman, A., Haeck, W., Staats, K., Geelen, V., et al. (2013). Oligodendrocyte dysfunction in the pathogenesis of amyotrophic lateral sclerosis. Brain,136(Pt 2), 471–482. doi:10.1093/brain/aws339.
30. Rabin, S. J., Kim, J. M., Baughn, M., Libby, R. T., Kim, Y. J., Fan, Y., et al. (2010). Sporadic ALS has compartment-specific aberrant exon splicing and altered cell-matrix adhesion biology. Human Molecular Genetics,19(2), 313–328. doi:10.1093/hmg/ddp498.
31. Reddy, P. H., & Reddy, T. P. (2011). Mitochondria as a therapeutic target for aging and neurodegenerative diseases. Current Alzheimer Research,8(4), 393–409.
32. Renton, A. E., Majounie, E., Waite, A., Simon-Sanchez, J., Rollinson, S., Gibbs, J. R., et al. (2011). A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron,72(2), 257–268. doi:10.1016/j.neuron.2011.09.010.
33. Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., et al. (1993). Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature,362(6415), 59–62. doi:10.1038/362059a0.
34. Saris, C. G., Horvath, S., van Vught, P. W., van Es, M. A., Blauw, H. M., Fuller, T. F., et al. (2009). Weighted gene co-expression network analysis of the peripheral blood from Amyotrophic Lateral Sclerosis patients. BMC Genomics,10, 405. doi:10.1186/1471-2164-10-405.
35. Scarpulla, R. C. (2012). Nucleus-encoded regulators of mitochondrial function: Integration of respiratory chain expression, nutrient sensing and metabolic stress. Biochimica et Biophysica Acta,1819(9–10), 1088–1097. doi:10.1016/j.bbagrm.2011.10.011.
36. Scarpulla, R. C., Vega, R. B., & Kelly, D. P. (2012). Transcriptional integration of mitochondrial biogenesis. Trends in Endocrinology and Metabolism,23(9), 459–466. doi:10.1016/j.tem.2012.06.006.
37. Schapira, A. H., Cooper, J. M., Dexter, D., Jenner, P., Clark, J. B., & Marsden, C. D. (1989). Mitochondrial complex I deficiency in Parkinson’s disease. Lancet,1(8649), 1269.
38. Shaw, P. J., & Eggett, C. J. (2000). Molecular factors underlying selective vulnerability of motor neurons to neurodegeneration in amyotrophic lateral sclerosis. Journal of Neurology,247(Suppl 1), I17–I27.
39. Sreedharan, J., Blair, I. P., Tripathi, V. B., Hu, X., Vance, C., Rogelj, B., et al. (2008). TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science,319(5870), 1668–1672. doi:10.1126/science.1154584.
40. Swerdlow, R. H., Parks, J. K., Cassarino, D. S., Trimmer, P. A., Miller, S. W., Maguire, D. J., et al. (1998). Mitochondria in sporadic amyotrophic lateral sclerosis. Experimental Neurology,153(1), 135–142. doi:10.1006/exnr.1998.6866.
41. Thomas, R. R., Keeney, P. M., & Bennett, J. P. (2012). Impaired complex-I mitochondrial biogenesis in Parkinson disease frontal cortex. Journal of Parkinson’s Disease,2(1), 67–76. doi:10.3233/JPD-2012-11074.
42. Vermeulen, J., Derveaux, S., Lefever, S., De Smet, E., De Preter, K., Yigit, N., et al. (2009). RNA pre-amplification enables large-scale RT-qPCR gene-expression studies on limiting sample amounts. BMC Research Notes,2, 235. doi:10.1186/1756-0500-2-235.
43. Wallace, D. C. (1999). Mitochondrial diseases in man and mouse. Science,283(5407), 1482–1488.
44. Wang, X. S., Simmons, Z., Liu, W., Boyer, P. J., & Connor, J. R. (2006). Differential expression of genes in amyotrophic lateral sclerosis revealed by profiling the post mortem cortex. Amyotrophic Lateral Sclerosis,7(4), 201–210. doi:10.1080/17482960600947689.
45. Young-Collier, K. J., McArdle, M., & Bennett, J. P. (2012). The dying of the light: Mitochondrial failure in Alzheimer’s disease. Journal of Alzheimer’s Disease,28(4), 771–781. doi:10.3233/JAD-2011-111487.
46. Zhang, R., Hadlock, K. G., Do, H., Yu, S., Honrada, R., Champion, S., et al. (2011). Gene expression profiling in peripheral blood mononuclear cells from patients with sporadic amyotrophic lateral sclerosis (sALS). Journal of Neuroimmunology,230(1–2), 114–123. doi:10.1016/j.jneuroim.2010.08.012.