The detection of microRNA associated with alzheimer's disease in biological fluids using next-generation sequencing technologies

Frontiers in Genetics

Volumn 4, Issue AUG, 2013, Pages

  Cheng, Lesley ^a,b   Quek, Camelia Y J ^a,b   Sun, Xin ^a,b   Bellingham, Shayne A ^a,b   Hill, Andrew F ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Alzheimer's disease; Biological fluids; Deep sequencing; Exosomes; MicroRNA

Indexed keywords

EID: 84883492783     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00150     Document Type: Article

References (135)

1. Ahmadian, A., Ehn, M., and Hober, S. (2006). Pyrosequencing: history, biochemistry and future. Clin. Chim. Acta 363, 83-94. doi: 10.1016/j.cccn.2005.04.038
2. Alexandrov, P. N., Dua, P., Hill, J. M., Bhattacharjee, S., Zhao, Y., and Lukiw, W. J. (2012). microRNA (miRNA) speciation in Alzheimer's disease (AD) cerebrospinal fluid (CSF) and extracellular fluid (ECF). Int. J. Biochem. Mol. Biol. 3, 365-373.
3. Alvarez, M. L., Khosroheidari, M., Kanchi Ravi, R., and Distefano, J. K. (2012). Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers. Kidney Int. 82, 1024-1032. doi: 10.1038/ki.2012.256
4. Arroyo, J. D., Chevillet, J. R., Kroh, E. M., Ruf, I. K., Pritchard, C. C., Gibson, D. F., et al. (2011). Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. U.S.A. 108, 5003-5008. doi: 10.1073/pnas.1019055108
5. Babak, T., Zhang, W., Morris, Q., Blencowe, B. J., and Hughes, T. R. (2004). Probing microRNAs with microarrays: tissue specificity and functional inference. RNA 10, 1813-1819. doi: 10.1261/rna.7119904
6. Balakathiresan, N., Bhomia, M., Chandran, R., Chavko, M., McCarron, R. M., and Maheshwari, R. K. (2012). MicroRNA let-7i is a promising serum biomarker for blast-induced traumatic brain injury. J. Neurotrauma 29, 1379-1387. doi: 10.1089/neu.2011.2146
7. Baraniskin, A., Deckert, M., Schulte-Altedorneburg, G., Schlegel, U., and Schroers, R. (2012a). Current strategies in the diagnosis of diffuse large B-cell lymphoma of the central nervous system. Br. J. Haematol. 156, 421-432.
8. Baraniskin, A., Kuhnhenn, J., Schlegel, U., Chan, A., Deckert, M., Gold, R., et al. (2011). Identification of microRNAs in the cerebrospinal fluid as marker for primary diffuse large B-cell lymphoma of the central nervous system. Blood 117, 3140-3146. doi: 10.1182/blood-2010-09-308684
9. Baraniskin, A., Kuhnhenn, J., Schlegel, U., Maghnouj, A., Zollner, H., Schmiegel, W., et al. (2012b). Identification of microRNAs in the cerebrospinal fluid as biomarker for the diagnosis of glioma. Neuro Oncol. 14, 29-33.
10. Barzon, L., Lavezzo, E., Militello, V., Toppo, S., and Palu, G. (2011). Applications of next-generation sequencing technologies to diagnostic virology. Int. J. Mol. Sci. 12, 7861-7884. doi: 10.3390/ijms12117861
11. Begley, D. J., and Brightman, M. W. (2003). Structural and functional aspects of the blood-brain barrier. Prog. Drug Res. 61, 39-78.
12. Bellingham, S. A., Coleman, B. M., and Hill, A. F. (2012a). Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res. 40, 10937-10949.
13. Bellingham, S. A., Guo, B. B., Coleman, B. M., and Hill, A. F. (2012b). Exosomes: vehicles for the transfer of toxic proteins associated with neurodegenerative diseases?. Front. Physiol. 3:124. doi: 10.3389/fphys.2012.00124
14. Bentley, D. R., Balasubramanian, S., Swerdlow, H. P., Smith, G. P., Milton, J., Brown, C. G., et al. (2008). Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456, 53-59. doi: 10.1038/nature07517
15. Berzin, T. M., Zipser, B. D., Rafii, M. S., Kuo-Leblanc, V., Yancopoulos, G. D., Glass, D. J., et al. (2000). Agrin and microvascular damage in Alzheimer's disease. Neurobiol. Aging 21, 349-355. doi: 10.1016/S0197-4580(00)00121-4
16. Blennow, K., Wallin, A., Fredman, P., Karlsson, I., Gottfries, C. G., and Svennerholm, L. (1990). Blood-brain barrier disturbance in patients with Alzheimer's disease is related to vascular factors. Acta Neurol. Scand. 81, 323-326. doi: 10.1111/j.1600-0404.1990.tb01563.x
17. Brase, J. C., Wuttig, D., Kuner, R., and Sultmann, H. (2010). Serum microRNAs as non-invasive biomarkers for cancer. Mol. Cancer 9, 306.
18. Bryant, R. J., Pawlowski, T., Catto, J. W., Marsden, G., Vessella, R. L., Rhees, B., et al. (2012). Changes in circulating microRNA levels associated with prostate cancer. Br. J. Cancer 106, 768-774. doi: 10.1038/bjc.2011.595
19. Caltagarone, J., Jing, Z., and Bowser, R. (2007). Focal adhesions regulate A?? signaling and cell death in Alzheimer's disease. Biochim. Biophys. Acta Mol. Basis Dis. 1772, 438-445. doi: 10.1016/j.bbadis.2006.11.007
20. Chapman, P. F., White, G. L., Jones, M. W., Cooper-Blacketer, D., Marshall, V. J., Irizarry, M., et al. (1999). Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci. 2, 271-276. doi: 10.1038/6374
21. Chen, X., Ba, Y., Ma, L., Cai, X., Yin, Y., Wang, K., et al. (2008). Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 18, 997-1006. doi: 10.1038/cr.2008.282
22. Chen, Y. R., Zheng, Y., Liu, B., Zhong, S. L., Giovannoni, J., and Fei, Z. J. (2012). A cost-effective method for Illumina small RNA-Seq library preparation using T4 RNA ligase 1 adenylated adapters. Plant Methods 8, 41-45. doi: 10.1186/1746-4811-8-41
23. Church, G. M. (2006). Genomes for all. Sci. Am. 294, 46-54. doi: 10.1038/scientificamerican0106-46
24. Cogswell, J. P., Ward, J., Taylor, I. A., Waters, M., Shi, Y., Cannon, B., et al. (2008). Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers Dis. 14, 27-41.
25. Cole, S. L., and Vassar, R. (2008). The role of amyloid precursor protein processing by BACE1, the beta-secretase, in Alzheimer disease pathophysiology. J. Biol. Chem. 283, 29621-29625. doi: 10.1074/jbc.R800015200
26. Cortez, M. A., Bueso-Ramos, C., Ferdin, J., Lopez-Berestein, G., Sood, A. K., and Calin, G. A. (2011). MicroRNAs in body fluids-the mix of hormones and biomarkers. Nat. Rev. Clin. Oncol. 8, 467-477. doi: 10.1038/nrclinonc.2011.76
27. Debey-Pascher, S., Chen, J., Voss, T., and Staratschek-Jox, A. (2012). Blood-based miRNA preparation for noninvasive biomarker development. Methods Mol. Biol. 822, 307-338. doi: 10.1007/978-1-61779-427-8_22
28. Defrancesco, L., and Subbaraman, N. (2011). Sequencing firms eye pathology labs as next big market opportunity. Nat. Biotechnol. 29, 379-380. doi: 10.1038/nbt0511-379
29. Edbauer, D., Neilson, J. R., Foster, K. A., Wang, C. F., Seeburg, D. P., Batterton, M. N., et al. (2010). Regulation of synaptic structure and function by FMRPassociated microRNAs miR-125b and miR-132. Neuron 65, 373-384. doi: 10.1016/j.neuron.2010.01.005
30. Etheridge, A., Lee, I., Hood, L., Galas, D., and Wang, K. (2011). Extracellular microRNA: a new source of biomarkers. Mutat. Res. 717, 85-90. doi: 10.1016/j.mrfmmm.2011.03.004
31. Eyre, D. W., Golubchik, T., Gordon, N. C., Bowden, R., Piazza, P., Batty, E. M., et al. (2012). A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2:e001124. doi: 10.1136/bmjopen-2012-001124
32. Fang, M., Wang, J., Zhang, X., Geng, Y., Hu, Z., Rudd, J. A., et al. (2012). The miR-124 regulates the expression of BACE1/beta-secretase correlated with cell death in Alzheimer's disease. Toxicol. Lett. 209, 94-105. doi: 10.1016/j.toxlet.2011.11.032
33. Fehniger, T. A., Wylie, T., Germino, E., Leong, J. W., Magrini, V. J., Koul, S., et al. (2010). Next-generation sequencing identifies the natural killer cell microRNA transcriptome. Genome Res. 20, 1590-1604. doi: 10.1101/gr.107995.110
34. Fuller, C. W., Middendorf, L. R., Benner, S. A., Church, G. M., Harris, T., Huang, X. H., et al. (2009). The challenges of sequencing by synthesis. Nat. Biotechnol. 27, 1013-1023. doi: 10.1038/nbt.1585
35. Gallego, J., Gordon, M., Claycomb, K., Bhatt, M., Lencz, T., and Malhotra, A. (2012). In vivo microRNA detection and quantitation in cerebrospinal fluid. J. Mol. Neurosci. 47, 243-248. doi: 10.1007/s12031-012-9731-7
36. Gao, J., Wang, W. Y., Mao, Y. W., Graff, J., Guan, J. S., Pan, L., et al. (2010). A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466, 1105-1109. doi: 10.1038/nature09271
37. Geekiyanage, H., and Chan, C. (2011). MicroRNA-137/181c regulates serine palmitoyltransferase and in turn amyloid beta, novel targets in sporadic Alzheimer's disease. J. Neurosci. 31, 14820-14830. doi: 10.1523/JNEUROSCI.3883-11.2011
38. Geekiyanage, H., Jicha, G. A., Nelson, P. T., and Chan, C. (2012). Blood serum miRNA: non-invasive biomarkers for Alzheimer's disease. Exp. Neurol. 235, 491-496. doi: 10.1016/j.expneurol.2011.11.026
39. Gilad, S., Meiri, E., Yogev, Y., Benjamin, S., Lebanony, D., Yerushalmi, N., et al. (2008). Serum microRNAs are promising novel biomarkers. PLoS ONE 3:e3148. doi: 10.1371/journal.pone.0003148
40. Haghikia, A., Hellwig, K., Baraniskin, A., Holzmann, A., Decard, B. F., Thum, T., et al. (2012). Regulated microRNAs in the CSF of patients with multiple sclerosis: a case-control study. Neurology 79, 2166-2170. doi: 10.1212/WNL.0b013e3182759621
41. Hall, N. (2007). Advanced sequencing technologies and their wider impact in microbiology. J. Exp. Biol. 210, 1518-1525. doi: 10.1242/jeb.001370
42. Hansson, O., Zetterberg, H., Vanmechelen, E., Vanderstichele, H., Andreasson, U., Londos, E., et al. (2010). Evaluation of plasma Abeta(40) and Abeta(42) as predictors of conversion to Alzheimer's disease in patients with mild cognitive impairment. Neurobiol. Aging 31, 357-367. doi: 10.1016/j.neurobiolaging.2008.03.027
43. Haqqani, A. S., Delaney, C. E., Tremblay, T. L., Sodja, C., Sandhu, J. K., and Stanimirovic, D. B. (2013). Method for isolation and molecular characterization of extracellular microvesicles released from brain endothelial cells. Fluids Barriers CNS 10:4. doi: 10.1186/2045-8118-10-4
44. Hardy, J., and Allsop, D. (1991). Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 12, 383-388. doi: 10.1016/0165-6147(91)90609-V
45. Harismendy, O., Ng, P. C., Strausberg, R. L., Wang, X. Y., Stockwell, T. B., Beeson, K. Y., et al. (2009). Evaluation of next generation sequencing platforms for population targeted sequencing studies. Genome Biol. 10:R32. doi: 10.1186/gb-2009-10-3-r32
46. He, L., and Hannon, G. J. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5, 522-531. doi: 10.1038/nrg1379
47. Hebert, S. S., Horre, K., Nicolai, L., Bergmans, B., Papadopoulou, A. S., Delacourte, A., et al. (2009). MicroRNA regulation of Alzheimer's Amyloid precursor protein expression. Neurobiol. Dis. 33, 422-428. doi: 10.1016/j.nbd.2008.11.009
48. Hebert, S. S., Horre, K., Nicolai, L., Papadopoulou, A. S., Mandemakers, W., Silahtaroglu, A. N., et al. (2008). Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc. Natl. Acad. Sci. U.S.A. 105, 6415-6420. doi: 10.1073/pnas.0710263105
49. Hebert, S. S., Sergeant, N., and Buee, L. (2012). MicroRNAs and the Regulation of Tau Metabolism. Int. J. Alzheimers Dis. 2012:406561. doi: 10.1155/2012/406561
50. Horner, D. S., Pavesi, G., Castrignano, T., De Meo, P. D., Liuni, S., Sammeth, M., et al. (2010). Bioinformatics approaches for genomics and post genomics applications of next-generation sequencing. Brief. Bioinform. 11, 181-197. doi: 10.1093/bib/bbp046
51. Huang, T., Liu, Y., Huang, M., Zhao, X., and Cheng, L. (2010). Wnt1-cre-mediated conditional loss of Dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in mice. J. Mol. Cell Biol. 2, 152-163. doi: 10.1093/jmcb/mjq008
52. Hunter, M. P., Ismail, N., Zhang, X., Aguda, B. D., Lee, E. J., Yu, L., et al. (2008). Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 3:e3694. doi: 10.1371/journal.pone.0003694
53. Hutchison, C. A. (2007). DNA sequencing: bench to bedside and beyond. Nucleic Acids Res. 35, 6227-6237. doi: 10.1093/nar/gkm688
54. Jin, P., Wang, E., Ren, J., Childs, R., Shin, J. W., Khuu, H., et al. (2008). Differentiation of two types of mobilized peripheral blood stem cells by microRNA and cDNA expression analysis. J. Transl. Med. 6:39. doi: 10.1186/1479-5876-6-39
55. Jones, C. I., Zabolotskaya, M. V., King, A. J., Stewart, H. J., Horne, G. A., Chevassut, T. J., et al. (2012). Identification of circulating microRNAs as diagnostic biomarkers for use in multiple myeloma. Br. J. Cancer 107, 1987-1996. doi: 10.1038/bjc.2012.525
56. Kawase-Koga, Y., Otaegi, G., and Sun, T. (2009). Different timings of Dicer deletion affect neurogenesis and gliogenesis in the developing mouse central nervous system. Dev. Dyn. 238, 2800-2812. doi: 10.1002/dvdy.22109
57. Kodama, Y., Shumway, M., and Leinonen, R. (2012). The sequence read archive: explosive growth of sequencing data. Nucleic Acids Res. 40, D54-D56. doi: 10.1093/nar/gkr854
58. Kole, A. J., Swahari, V., Hammond, S. M., and Deshmukh, M. (2011). miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. Genes Dev. 25, 125-130. doi: 10.1101/gad.1975411
59. Koss, L. G., and Sherman, A. B. (1984). Image analysis of cells in the sediment of voided urine. Monogr. Clin. Cytol. 9, 148-162.
60. Kozomara, A., and Griffiths-Jones, S. (2011). miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, D152-D157. doi: 10.1093/nar/gkq1027
61. Krol, J., Loedige, I., and Filipowicz, W. (2010). The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597-610. doi: 10.1038/nrg2843
62. Kumar, V. S., and Webster, M. (2011). The personal genome machine-DNA decoding with semiconductors. Clin. Chem. 57, 1786-1788. doi: 10.1373/clinchem.2011.175893
63. Lee, L. W., Zhang, S., Etheridge, A., Ma, L., Martin, D., Galas, D., et al. (2010). Complexity of the microRNA repertoire revealed by next-generation sequencing. RNA 16, 2170-2180. doi: 10.1261/rna.2225110
64. Lehmann, S., Krüger, C., Park, B., Derkow, K., Rosenberger, K., Baumgart, J., et al. (2012). An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat. Neurosci. 15, 827-835. doi: 10.1038/nn.3113
65. Loman, N. J., Constantinidou, C., Chan, J. Z. M., Halachev, M., Sergeant, M., Penn, C. W., et al. (2012a). High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nat. Rev. Microbiol. 10, 599-606.
66. Loman, N. J., Misra, R. V., Dallman, T. J., Constantinidou, C., Gharbia, S. E., Wain, J., et al. (2012b). Performance comparison of benchtop high-throughput sequencing platforms. Nat. Biotechnol. 30, 434-439.
67. Lukiw, W. J., Alexandrov, P. N., Zhao, Y., Hill, J. M., and Bhattacharjee, S. (2012). Spreading of Alzheimer's disease inflammatory signaling through soluble micro- RNA. Neuroreport 23, 621-626. doi: 10.1097/WNR.0b013e32835542b0
68. Lukiw, W. J., and Pogue, A. I. (2007). Induction of specific micro RNA (miRNA) species by ROS-generating metal sulfates in primary human brain cells. J. Inorg. Biochem. 101, 1265-1269. doi: 10.1016/j.jinorgbio.2007.06.004
69. Maes, O. C., Chertkow, H. M., Wang, E., and Schipper, H. M. (2009). MicroRNA: implications for Alzheimer disease and other human CNS disorders. Curr. Genomics 10, 154-168. doi: 10.2174/138920209788185252
70. Makeyev, E. V., Zhang, J., Carrasco, M. A., and Maniatis, T. (2007). The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 27, 435-448. doi: 10.1016/j.molcel.2007.07.015
71. Mamanova, L., Coffey, A. J., Scott, C. E., Kozarewa, I., Turner, E. H., Kumar, A., et al. (2010). Target-enrichment strategies for next-generation sequencing. Nat. Methods 7, 111-118. doi: 10.1038/nmeth.1419
72. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., et al. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380.
73. Meldrum, C., Doyle, M. A., and Tothill, R. W. (2011). Next-generation sequencing for cancer diagnostics: a practical perspective. Clin. Biochem. Rev. 32, 177.
74. Melkonyan, H. S., Feaver, W. J., Meyer, E., Scheinker, V., Shekhtman, E. M., Xin, Z., et al. (2008). Transrenal nucleic acids: from proof of principle to clinical tests. Ann. N.Y. Acad. Sci. 1137, 73-81. doi: 10.1196/annals.1448.015
75. Mitchell, P. S., Parkin, R. K., Kroh, E. M., Fritz, B. R., Wyman, S. K., Pogosova-Agadjanyan, E. L., et al. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. U.S.A. 105, 10513-10518.
76. Morozova, O., and Marra, M. A. (2008). Applications of next-generation sequencing technologies in functional genomics. Genomics 92, 255-264. doi: 10.1016/j.ygeno.2008.07.001
77. Natrajan, R., and Reis, J. S. (2011). Next-generation sequencing applied to molecular diagnostics. Expert Rev. Mol. Diagn. 11, 425-444. doi: 10.1586/erm.11.18
78. Nix, D. A., Di Sera, T. L., Dalley, B. K., Milash, B. A., Cundick, R. M., Quinn, K. S., et al. (2010). Next generation tools for genomic data generation, distribution, and visualization. BMC Bioinformatics 11:455. doi: 10.1186/1471-2105-11-455
79. Ogawa, Y., Taketomi, Y., Murakami, M., Tsujimoto, M., and Yanoshita, R. (2013). Small RNA transcriptomes of two types of exosomes in human whole saliva determined by next generation sequencing. Biol. Pharm. Bull. 36, 66-75. doi: 10.1248/bpb.b12-00607
80. Ozsolak, F., and Milos, P. M. (2010). RNA sequencing: advances, challenges and opportunities. Nat. Rev. Genet. 12, 87-98. doi: 10.1038/nrg2934
81. Pacifici, M., Delbue, S., Ferrante, P., Jeansonne, D., Kadri, F., Nelson, S., et al. (2013). Cerebrospinal fluid miRNA profile in HIV-encephalitis. J. Cell. Physiol. 228, 1070-1075. doi: 10.1002/jcp.24254
82. Pandey, V., Nutter, R. C., and Prediger, E. (Applied). "2008 Biosystems SOLiD™ System: ligation-based sequencing," in Next Generation Genome Sequencing, ed M. Janitz (Weinheim: Wiley-VCH), 29-42.
83. Pareek, C. S., Smoczynski, R., and Tretyn, A. (2011). Sequencing technologies and genome sequencing. J. Appl. Genet. 52, 413-435. doi: 10.1007/s13353-011-0057-x
84. Patel, R. S., Jakymiw, A., Yao, B., Pauley, B. A., Carcamo, W. C., Katz, J., et al. (2011). High resolution of microRNA signatures in human whole saliva. Arch. Oral Biol. 56, 1506-1513. doi: 10.1016/j.archoralbio.2011.05.015
85. Patz, S., Trattnig, C., Grunbacher, G., Ebner, B., Gully, C., Novak, A., et al. (2013). More than cell dust: microparticles isolated from cerebrospinal fluid of brain injured patients are messengers carrying mRNAs, miRNAs and proteins. J. Neurotrauma 30, 1232-1242. doi: 10.1089/neu.2012.2596
86. Prvulovic, D., and Hampel, H. (2011). Amyloid beta (Abeta) and phospho-tau (p-tau) as diagnostic biomarkers in Alzheimer's disease. Clin. Chem. Lab. Med. 49, 367 -374. doi: 10.1515/cclm.2011.087
87. Qi, J., Wang, J., Katayama, H., Sen, S., and Liu, S. M. (2012). Circulating microRNAs (cmiRNAs) as novel potential biomarkers for hepatocellular carcinoma. Neoplasma 30, 434-439.
88. Quail, M. A., Smith, M., Coupland, P., Otto, T. D., Harris, S. R., Connor, T. R., et al. (2012). A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 13:341. doi: 10.1186/1471-2164-13-341
89. Radford, A. D., Chapman, D., Dixon, L., Chantrey, J., Darby, A. C., and Hall, N. (2012). Application of next-generation sequencing technologies in virology. J. Gen. Virol. 93, 1853-1868. doi: 10.1099/vir.0.043182-0
90. Richter, B. G., and Sexton, D. P. (2009). Managing and analyzing next-generation sequence data. PLoS Comput. Biol. 5:e1000369. doi: 10.1371/journal.pcbi.1000369
91. Rizzo, J. M., and Buck, M. J. (2012). Key principles and clinical applications of "Next-Generation" DNA sequencing. Cancer Prev. Res. 5, 887-900. doi: 10.1158/1940-6207.CAPR-11-0432
92. Rosenmann, H. (2012). CSF biomarkers for amyloid and tau pathology in Alzheimer's disease. J. Mol. Neurosci. 47, 1-14. doi: 10.1007/s12031-011-9665-5
93. Roth, K. (2001). Caspases, apoptosis, and Alzheimer disease: causation, correlation, and confusion. J. Neuropathol. Exp. Neurol. 60, 829-838.
94. Rothberg, J. M., Hinz, W., Rearick, T. M., Schultz, J., Mileski, W., Davey, M., et al. (2011). An integrated semiconductor device enabling non-optical genome sequencing. Nature 475, 348-352. doi: 10.1038/nature10242
95. Rothberg, J. M., and Leamon, J. H. (2008). The development and impact of 454 sequencing. Nat. Biotechnol. 26, 1117-1124. doi: 10.1038/nbt1485
96. Russo, F., Di Bella, S., Nigita, G., Macca, V., Laganà, A., Giugno, R., et al. (2012). miRandola: extracellular circulating microRNAs database. PLoS ONE 7:e47786. doi: 10.1371/journal.pone.0047786
97. Saunders, L. R., Sharma, A. D., Tawney, J., Nakagawa, M., Okita, K., Yamanaka, S., et al. (2010). miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adult mouse tissues. Aging (Albany NY) 2, 415-431.
98. Schaefer, A., O'Carroll, D., Tan, C. L., Hillman, D., Sugimori, M., Llinas, R., et al. (2007). Cerebellar neurodegeneration in the absence of microRNAs. J. Exp. Med. 204, 1553-1558. doi: 10.1084/jem.20070823
99. Schipper, H., Maes, O., Chertkow, H., and Wang, E. (2007). MicroRNA expression in Alzheimer blood mononuclear cells. Gene Regul. Syst. Biol. 1, 263-274.
100. Scholz, M. B., Lo, C. C., and Chain, P. S. G. (2011). Next generation sequencing and bioinformatic bottlenecks: the current state of metagenomic data analysis. Curr. Opin. Biotechnol. 23, 9-15. doi: 10.1016/j.copbio.2011.11.013
101. Schonrock, N., Humphreys, D. T., Preiss, T., and Gotz, J. (2012). Target gene repression mediated by miRNAs miR-181c and miR-9 both of which are downregulated by amyloid-beta. J. Mol. Neurosci. 46, 324-335. doi: 10.1007/s12031-011-9587-2
102. Schonrock, N., Ke, Y. D., Humphreys, D., Staufenbiel, M., Ittner, L. M., Preiss, T., et al. (2010). Neuronal microRNA deregulation in response to Alzheimer's disease amyloid-beta. PLoS ONE 5:e11070. doi: 10.1371/journal.pone.0011070
103. Schwartz, S., Oren, R., and Ast, G. (2011). Detection and removal of biases in the analysis of next-generation sequencing reads. PLoS ONE 6:e16685. doi: 10.1371/journal.pone.0016685
104. Sempere, L. F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., and Ambros, V. (2004). Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5:R13. doi: 10.1186/gb-2004-5-3-r13
105. Sheinerman, K. S., Tsivinsky, V. G., Crawford, F., Mullan, M. J., Abdullah, L., and Umansky, S. R. (2012). Plasma microRNA biomarkers for detection of mild cognitive impairment. Aging (Albany NY) 4, 590-605.
106. Shendure, J., and Ji, H. L. (2008). Next-generation DNA sequencing. Nat. Biotechnol. 26, 1135-1145. doi: 10.1038/nbt1486
107. Shendure, J., Mitra, R. D., Varma, C., and Church, G. M. (2004). Advanced sequencing technologies: methods and goals. Nat. Rev. Genet. 5, 335-344. doi: 10.1038/nrg1325
108. Shibata, M., Nakao, H., Kiyonari, H., Abe, T., and Aizawa, S. (2011). MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J. Neurosci. 31, 3407-3422. doi: 10.1523/JNEUROSCI.5085-10.2011
109. Skog, J., Wurdinger, T., Van Rijn, S., Meijer, D. H., Gainche, L., Sena-Esteves, M., et al. (2008). Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470-1476. doi: 10.1038/ncb1800
110. Smirnova, L., Grafe, A., Seiler, A., Schumacher, S., Nitsch, R., and Wulczyn, F. G. (2005). Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci. 21, 1469-1477. doi: 10.1111/j.1460-9568.2005.03978.x
111. Szulwach, K. E., Li, X., Smrt, R. D., Li, Y., Luo, Y., Lin, L., et al. (2010). Cross talk between microRNA and epigenetic regulation in adult neurogenesis. J. Cell Biol. 189, 127-141. doi: 10.1083/jcb.200908151
112. Tan, S. L., Ohtsuka, T., Gonzalez, A., and Kageyama, R. (2012). MicroRNA9 regulates neural stem cell differentiation by controlling Hes1 expression dynamics in the developing brain. Genes Cells 17, 952-961. doi: 10.1111/gtc.12009
113. Tanzi, R. E., Moir, R. D., and Wagner, S. L. (2004). Clearance of Alzheimer's Abeta peptide: the many roads to perdition. Neuron 43, 605-608.
114. Taylor, D. D., and Gercel-Taylor, C. (2008). MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110, 13- 21. doi: 10.1016/j.ygyno.2008.04.033
115. Teer, J. K., Bonnycastle, L. L., Chines, P. S., Hansen, N. F., Aoyama, N., Swift, A. J., et al. (2010). Systematic comparison of three genomic enrichment methods for massively parallel DNA sequencing. Genome Res. 20, 1420-1431. doi: 10.1101/gr.106716.110
116. Teplyuk, N. M., Mollenhauer, B., Gabriely, G., Giese, A., Kim, E., Smolsky, M., et al. (2012). MicroRNAs in cerebrospinal fluid identify glioblastoma and metastatic brain cancers and reflect disease activity. Neuro Oncol. 14, 689-700. doi: 10.1093/neuonc/nos074
117. Tsujiura, M., Ichikawa, D., Komatsu, S., Shiozaki, A., Takeshita, H., Kosuga, T., et al. (2010). Circulating microRNAs in plasma of patients with gastric cancers. Br. J. Cancer 102, 1174-1179. doi: 10.1038/sj.bjc.6605608
118. Tucker, T., Marra, M., and Friedman, J. M. (2009). Massively parallel sequencing: the next big thing in genetic medicine. Am. J. Hum. Genet. 85, 142-154. doi: 10.1016/j.ajhg.2009.06.022
119. Turchinovich, A., Weiz, L., Langheinz, A., and Burwinkel, B. (2011). Characterization of extracellular circulating microRNA. Nucleic Acids Res. 39, 7223-7233. doi: 10.1093/nar/gkr254
120. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J., and Lotvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659. doi: 10.1038/ncb1596
121. Vickers, K. C., and Remaley, A. T. (2012). Lipid-based carriers of microRNAs and intercellular communication. Curr. Opin. Lipidol. 23, 91-97. doi: 10.1097/MOL.0b013e328350a425
122. Villemagne, V. L., Burnham, S., Bourgeat, P., Brown, B., Ellis, K. A., Salvado, O., et al. (2013). Amyloid ?? deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study. Lancet Neurol. 12, 357-367. doi: 10.1016/S1474-4422(13)70044-9
123. Vogel, U., Szczepanowski, R., Claus, H., Jünemann, S., Prior, K., and Harmsen, D. (2012). Ion torrent personal genome machine sequencing for genomic typing of Neisseria meningitidis for rapid determination of multiple layers of typing information. J. Clin. Microbiol. 50, 1889-1894. doi: 10.1128/JCM.00038-12
124. Wall, P. K., Leebens-Mack, J., Chanderbali, A. S., Barakat, A., Wolcott, E., Liang, H., et al. (2009). Comparison of next generation sequencing technologies for transcriptome characterization. BMC Genomics 10:347. doi: 10.1186/1471-2164-10-347
125. Walsh, D. M., and Selkoe, D. J. (2004). Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44, 181-193. doi: 10.1016/j.neuron.2004.09.010
126. Wang, G., Chan, E. S., Kwan, B. C., Li, P. K., Yip, S. K., Szeto, C. C., et al. (2012a). Expression of microRNAs in the urine of patients with bladder cancer. Clin. Genitourin. Cancer 10, 106-113.
127. Wang, G., Kwan, B. C., Lai, F. M., Chow, K. M., Li, P. K., and Szeto, C. C. (2012b). Urinary miR-21, miR-29, and miR-93: novel biomarkers of fibrosis. Am. J. Nephrol. 36, 412-418.
128. Wang, G., Kwan, B. C. H., Lai, F. M. M., Chow, K. M., Li, P. K. T., and Szeto, C. C. (2012c). Urinary miR-21, miR-29, and miR-93: novel biomarkers of fibrosis. Am. J. Nephrol. 36, 412-418.
129. Wang, G., Kwan, B. C., Lai, F. M., Chow, K. M., Kam-Tao Li, P., and Szeto, C. C. (2010). Expression of microRNAs in the urinary sediment of patients with IgA nephropathy. Dis. Markers 28, 79-86. doi: 10.1155/2010/396328
130. Watt, A. D., Perez, K. A., Faux, N. G., Pike, K. E., Rowe, C. C., Bourgeat, P., et al. (2011). Increasing the predictive accuracy of amyloid-beta blood-borne biomarkers in Alzheimer's disease. J. Alzheimers Dis. 24, 47-59.
131. Weber, J. A., Baxter, D. H., Zhang, S., Huang, D. Y., Huang, K. H., Lee, M. J., et al. (2010). The microRNA spectrum in 12 body fluids. Clin. Chem. 56, 1733-1741. doi: 10.1373/clinchem.2010.147405
132. Wilson, D. J. (2012). Insights from Genomics into Bacterial Pathogen Populations. PLoS Pathog. 8:e1002874. doi: 10.1371/journal.ppat.1002874
133. Xu, S., Yu, B., Chertkow, H., Wang, E., and Schipper, H. (2007). Transcriptional profiling of Alzheimer blood mononuclear cells by microarray. Neurobiol. Aging 28, 1795-1809.
134. Zhang, J., Chiodini, R., Badr, A., and Zhang, G. F. (2011). The impact of next-generation sequencing on genomics. J. Genet. Genomics 38, 95-109. doi: 10.1016/j.jgg.2011.02.003
135. Zipser, B. D., Johanson, C. E., Gonzalez, L., Berzin, T. M., Tavares, R., Hulette, C. M., et al. (2007). Microvascular injury and blood-brain barrier leakage in Alzheimer's disease. Neurobiol. Aging 28, 977-986. doi: 10.1016/j.neurobiolaging.2006.05.016