DOI QR코드

DOI QR Code

Quantitative Analysis of Nucleic Acids - the Last Few Years of Progress

  • Ding, Chunming (Bioinformatics Program and Center for Advanced Biotechnology, Boston University) ;
  • Cantor, Charles R. (Bioinformatics Program and Center for Advanced Biotechnology, Boston University)
  • 발행 : 2004.01.31

초록

DNA and RNA quantifications are widely used in biological and biomedical research. In the last ten years, many technologies have been developed to enable automated and high-throughput analyses. In this review, we first give a brief overview of how DNA and RNA quantifications are carried out. Then, five technologies (microarrays, SAGE, differential display, real time PCR and real competitive PCR) are introduced, with an emphasis on how these technologies can be applied and what their limitations are. The technologies are also evaluated in terms of a few key aspects of nucleic acids quantification such as accuracy, sensitivity, specificity, cost and throughput.

키워드

참고문헌

  1. Albertson, D. G. (2003) Profiling breast cancer by array CGH. Breast Cancer Res. Treat. 78, 289-298. https://doi.org/10.1023/A:1023025506386
  2. Alizadeh, A. A., Eisen, M. B., Davis, R. E., Ma, C., Lossos, I. S., Rosenwald, A., Boldrick, J. C., Sabet, H., Tran, T., Yu, X., et al. (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403, 503-511. https://doi.org/10.1038/35000501
  3. Alwine, J. C., Kemp, D. J. and Stark, G. R. (1977) Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc. Natl. Acad. Sci. USA 74, 5350-5354. https://doi.org/10.1073/pnas.74.12.5350
  4. Arbeitman, M. N., Furlong, E. E., Imam, F., Johnson, E., Null, B. H., Baker, B. S., Krasnow, M. A., Scott, M. P., Davis, R. W. and White, K. P. (2002) Gene expression during the life cycle of Drosophila melanogaster. Science 297, 2270-2275. https://doi.org/10.1126/science.1072152
  5. Becker-Andre, M. and Hahlbrock, K. (1989) Absolute mRNA quantification using the polymerase chain reaction (PCR). A novel approach by a PCR aided transcript titration assay (PATTY). Nucleic Acids Res. 17, 9437-9446. https://doi.org/10.1093/nar/17.22.9437
  6. Cheadle, C., Vawter, M. P., Freed, W. J. and Becker, K. G. (2003) Analysis of microarray data using z score transformation. J. Mol. Diagn. 5, 73-81. https://doi.org/10.1016/S1525-1578(10)60455-2
  7. Chen, J., Sun, M., Lee, S., Zhou, G., Rowley, J. D. and Wang, S. M. (2002) Identifying novel transcripts and novel genes in the human genome by using novel SAGE tags. Proc. Natl. Acad. Sci. USA 99, 12257-12262. https://doi.org/10.1073/pnas.192436499
  8. Chen, J. J., Lee, S., Zhou, G., Rowley, J. D. and Wang, S. M. (2003) Generation of longer cDNA fragments from SAGE tags for gene identification. Methods Mol. Biol. 221, 207-222.
  9. Cheung, V. G., Morley, M., Aguilar, F., Massimi, A., Kucherlapati, R. and Childs, G. (1999) Making and reading microarrays. Nat. Genet. 21, 15-19. https://doi.org/10.1038/4439
  10. Cho, R. J., Campbell, M. J., Winzeler, E. A., Steinmetz, L., Conway, A., Wodicka, L., Wolfsberg, T. G., Gabrielian, A. E., Landsman, D., Lockhart, D. J. and Davis, R. W. (1998) A genome-wide transcriptional analysis of the mitotic cell cycle. Mol. Cell. 2, 65-73. https://doi.org/10.1016/S1097-2765(00)80114-8
  11. Cui, X. and Churchill, G. A. (2003) Statistical tests for differential expression in cDNA microarray experiments. Genome Biol. 4, 210. https://doi.org/10.1186/gb-2003-4-4-210
  12. Ding, C. and Cantor, C. R. (2003a) Direct molecular haplotyping of long-range genomic DNA with M1-PCR. Proc. Natl. Acad. Sci. USA 100, 7449-7453. https://doi.org/10.1073/pnas.1232475100
  13. Ding, C. and Cantor, C. R. (2003b) A high-throughput gene expression analysis technique using competitive PCR and matrix-assisted laser desorption ionization time-of-flight MS. Proc. Natl. Acad. Sci. USA 100, 3059-3064. https://doi.org/10.1073/pnas.0630494100
  14. Emmert-Buck, M. R., Bonner, R. F., Smith, P. D., Chuaqui, R. F., Zhuang, Z., Goldstein, S. R., Weiss, R. A. and Liotta, L. A. (1996) Laser capture microdissection. Science 274, 998-1001. https://doi.org/10.1126/science.274.5289.998
  15. Fambrough, D., McClure, K., Kazlauskas, A. and Lander, E. S. (1999) Diverse signaling pathways activated by growth factor receptors induce broadly overlapping, rather than independent, sets of genes. Cell 97, 727-741. https://doi.org/10.1016/S0092-8674(00)80785-0
  16. Fink, L., Seeger, W., Ermert, L., Hanze, J., Stahl, U., Grimminger, F., Kummer, W. and Bohle, R. M. (1998) Real-time quantitative RT-PCR after laser-assisted cell picking. Nat. Med. 4, 1329-1333. https://doi.org/10.1038/3327
  17. Gibson, U. E., Heid, C. A. and Williams, P. M. (1996) A novel method for real time quantitative RT-PCR. Genome Res. 6, 995-1001. https://doi.org/10.1101/gr.6.10.995
  18. Ginzinger, D. G., Godfrey, T. E., Nigro, J., Moore, D. H. 2nd., Suzuki, S., Pallavicini, M. G., Gray, J. W. and Jensen, R. H. (2000) Measurement of DNA copy number at microsatellite loci using quantitative PCR analysis. Cancer Res. 60, 5405-5409.
  19. Goidin, D., Mamessier, A., Staquet, M. J., Schmitt, D. and Berthier-Vergnes, O. (2001) Ribosomal 18S RNA prevails over glyceraldehyde-3-phosphate dehydrogenase and beta-actin genes as internal standard for quantitative comparison of mRNA levels in invasive and noninvasive human melanoma cell subpopulations. Anal. Biochem. 295, 17-21. https://doi.org/10.1006/abio.2001.5171
  20. Golub, T. R., Slonim, D. K., Tamayo, P., Huard, C., Gaasenbeek, M., Mesirov, J. P., Coller, H., Loh, M. L., Downing, J. R., Caligiuri, M. A., Blloomfield, C. D. and Lander, E. S. (1999) Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286, 531-537. https://doi.org/10.1126/science.286.5439.531
  21. Harkin, D. P., Bean, J. M., Miklos, D., Song, Y. H., Truong, V. B., Englert, C., Christians, F. C., Ellisen, L. W., Maheswaran, S., Oliner, J. D. and Haber, D. A. (1999) Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1. Cell 97, 575-586. https://doi.org/10.1016/S0092-8674(00)80769-2
  22. Hayward-Lester, A., Oefner P. J. and Doris P. A. (1996) Rapid quantification of gene expression by competitive RT-PCR and ion- pair reversed-phase HPLC. Biotechniques 20, 250-257.
  23. Herzenberg, L. A., Parks, D., Sahaf, B., Perez, O., Roederer, M. and Herzenberg, L. A. (2002) The history and future of the fluorescence activated cell sorter and flow cytometry: a view from Stanford. Clin. Chem. 48, 1819-1827.
  24. Hyduke, D. R., Rohlin, L., Kao, K. C. and Liao, J. C. (2003) A software package for cDNA microarray data normalization and assessing confidence intervals. Omics 7, 227-234. https://doi.org/10.1089/153623103322452369
  25. Irie, T., Oshida, T., Hasegawa, H., Matsuoka, Y., Li, T., Oya, Y., Tanaka, T., Tsujimoto, G. and Kambara, H. (2000) Automated DNA fragment collection by capillary array gel electrophoresis in search of differentially expressed genes. Electrophoresis 21, 367-374. https://doi.org/10.1002/(SICI)1522-2683(20000101)21:2<367::AID-ELPS367>3.0.CO;2-1
  26. Ito, T., Kito, K., Adati, N., Mitsui, Y., Hagiwara, H. and Sakaki, Y. (1994) Fluorescent differential display: arbitrarily primed RT-PCR fingerprinting on an automated DNA sequencer. FEBS Lett 351, 231-236. https://doi.org/10.1016/0014-5793(94)00867-1
  27. Ivanova, A. V. and Ivanov, S. V. (2002) Differential display analysis of gene expression in yeast. Cell. Mol. Life Sci. 59, 1241-1245. https://doi.org/10.1007/s00018-002-8502-y
  28. Kashiwagi, H. and Uchida, K. (2000) Genome-wide profiling of gene amplification and deletion in cancer. Hum. Cell 13, 135-141.
  29. Knight, J. (2001a) Geneticists' work in disarray as DNA-chip producer pulls the plug. Nature 414, 135-136.
  30. Knight, J. (2001b) When the chips are down. Nature 410, 860-861. https://doi.org/10.1038/35073680
  31. Kooperberg, C., Sipione, S., LeBlanc, M., Strand, A. D., Cattaneo, E. and Olson, J. M. (2002) Evaluating test statistics to select interesting genes in microarray experiments. Hum. Mol. Genet. 11, 2223-2232. https://doi.org/10.1093/hmg/11.19.2223
  32. Kruglyak, L. (1999) Prospects for whole-genome linkage disequilibrium mapping of common disease genes. Nat. Genet. 22, 139-144. https://doi.org/10.1038/9642
  33. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921.
  34. Lee, M. L. and Whitmore, G. A. (2002) Power and sample size for DNA microarray studies. Stat. Med. 21, 3543-3570.
  35. Lee, S. B., Huang, K., Palmer, R., Truong, V. B., Herzlinger, D., Kolquist, K. A., Wong, J., Paulding, C., Yoon, S. K., Gerald, W., Oliner, J. D. and Haber, D. A. (1999) The Wilms tumor suppressor WT1 encodes a transcriptional activator of amphiregulin. Cell 98, 663-673. https://doi.org/10.1016/S0092-8674(00)80053-7
  36. Leung, Y. F. and Cavalieri, D. (2003) Fundamentals of cDNA microarray data analysis. Trends Genet. 19, 649-659. https://doi.org/10.1016/j.tig.2003.09.015
  37. Liang, P. (2002) A decade of differential display. Biotechniques 33, 338-44, 346.
  38. Liang, P. and Pardee, A. B. (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257, 967-971. https://doi.org/10.1126/science.1354393
  39. Liang, P. and Pardee, A. B. (1997) Differential display methods and protocols. Humana Press, Totowa, NJ, USA.
  40. Liao, V. H. and Freedman, J. H. (2002) Differential display analysis of gene expression in invertebrates. Cell. Mol. Life Sci. 59, 1256-1263. https://doi.org/10.1007/s00018-002-8504-9
  41. Lockhart, D. J., Dong, H., Byrne, M. C., Follettie, M. T., Gallo, M. V., Chee, M. S., Mittmann, M., Wang, C., Kobayashi, M., Horton, H. and Brown, E. L. (1996) Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat. Biotechnol. 14, 1675-1680. https://doi.org/10.1038/nbt1296-1675
  42. Lockhart, D. J. and Winzeler, E. A. (2000) Genomics, gene expression and DNA arrays. Nature 405, 827-836. https://doi.org/10.1038/35015701
  43. Man, M. Z., Wang, X. and Wang, Y. (2000) POWER_SAGE: comparing statistical tests for SAGE experiments. Bioinformatics 16, 953-959. https://doi.org/10.1093/bioinformatics/16.11.953
  44. Margulies, E. H. and Innis, J. W. (2000) eSAGE: managing and analysing data generated with serial analysis of gene expression (SAGE). Bioinformatics 16, 650-651. https://doi.org/10.1093/bioinformatics/16.7.650
  45. Mikulowska-Mennis, A., Taylor, T. B., Vishnu, P., Michie, S. A., Raja, R., Horner, N. and Kunitake, S. T. (2002) High-quality RNA from cells isolated by laser capture microdissection. Biotechniques 33, 176-179.
  46. Mir, K. U. (2000) The hypothesis is there is no hypothesis. The Microarray Meeting, Scottsdale, Arizona, USA, 22-25 September 1999. Trends Genet. 16. 63-64. https://doi.org/10.1016/S0168-9525(99)01947-2
  47. Morrison, T. B, Weis, J. J. and Wittwer, C. T. (1998) Quantification of low-copy transcripts by continuous SYBR Green I monitoring during amplification. Biotechniques 24, 954-8, 960, 962.
  48. Nigro, J. M., Takahashi, M. A., Ginzinger, D. G., Law, M., Passe, S., Jenkins, R. B. and Aldape, K. (2001) Detection of 1p and 19q loss in oligodendroglioma by quantitative microsatellite analysis, a real-time quantitative polymerase chain reaction assay. Am. J. Pathol. 158, 1253-1262. https://doi.org/10.1016/S0002-9440(10)64076-X
  49. Nyberg-Hoffman, C., Shabram, P., Li, W., Giroux, D. and Aguilar-Cordova, E. (1997) Sensitivity and reproducibility in adenoviral infectious titer determination. Nat. Med. 3, 808-811. https://doi.org/10.1038/nm0797-808
  50. Palmer, S., Wiegand, A. P., Maldarelli, F., Bazmi, H., Mican, J. M., Polis, M., Dewar, R. L., Planta, A., Liu, S., Metcalf, J. A., Mellors, J. W. and Coffin, J. M. (2003) New real-time reverse transcriptase-initiated PCR assay with single-copy sensitivity for human immunodeficiency virus type 1 RNA in plasma. J. Clin. Microbiol. 41, 4531-4536. https://doi.org/10.1128/JCM.41.10.4531-4536.2003
  51. Sachidanandam, R., Weissman, D., Schmidt, S. C., Kakol, J. M., Stein, L. D., Marth, G., Sherry, S., Mullikin, J. C., Mortimore, B. J., Willey, D. L., et al. (2001) A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature 409, 928-933. https://doi.org/10.1038/35057149
  52. Schena, M., Shalon, D., Davis, R. W. and Brown, P. O. (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467-470. https://doi.org/10.1126/science.270.5235.467
  53. Simon, H. G. (2002) Messenger RNA differential display strategies in birds and amphibians. Cell. Mol. Life Sci. 59, 1264-1273. https://doi.org/10.1007/s00018-002-8505-8
  54. Singhal, S., Kyvernitis, C. G., Johnson, S. W., Kaiser, L. R., Liebman, M. N. and Albelda, S. M. (2003) Microarray data simulator for improved selection of differentially expressed genes. Cancer Biol. Ther. 2, 383-391. https://doi.org/10.4161/cbt.2.4.431
  55. Solanas, M., Moral, R. and Escrich, E. (2001). Unsuitability of using ribosomal RNA as loading control for Northern blot analyses related to the imbalance between messenger and ribosomal RNA content in rat mammary tumors. Anal. Biochem. 288, 99-102. https://doi.org/10.1006/abio.2000.4889
  56. Southern, E. M. (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98, 503-517. https://doi.org/10.1016/S0022-2836(75)80083-0
  57. Stein, S. and Liang, P. (2002) Differential display analysis of gene expression in mammals: a p53 story. Cell. Mol. Life Sci. 59, 1274-1279. https://doi.org/10.1007/s00018-002-8506-7
  58. Tyagi, S. and Kramer, F. R. (1996) Molecular beacons: probes that fluoresce upon hybridization. Nat. Biotechnol. 14, 303-308. https://doi.org/10.1038/nbt0396-303
  59. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034.
  60. Velculescu, V. E., Zhang, L., Vogelstein, B. and Kinzler, K. W. (1995) Serial analysis of gene expression. Science 270, 484-487. https://doi.org/10.1126/science.270.5235.484
  61. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A., et al. (2001) The sequence of the human genome. Science 291, 1304-1351. https://doi.org/10.1126/science.1058040
  62. Wells, D. and Levy, B. (2003) Cytogenetics in reproductive medicine: the contribution of comparative genomic hybridization (CGH). Bioessays 25, 289-300. https://doi.org/10.1002/bies.10232
  63. Wodicka, L., Dong, H., Mittmann, M., Ho, M. H. and Lockhart, D. J. (1997) Genome-wide expression monitoring in Saccharomyces cerevisiae. Nat. Biotechnol. 15, 1359-1367. https://doi.org/10.1038/nbt1297-1359
  64. Wooster, R. (2000) Cancer classification with DNA microarrays is less more? Trends Genet. 16, 327-329. https://doi.org/10.1016/S0168-9525(00)02064-3
  65. Yamazaki, M. and Saito, K. (2002) Differential display analysis of gene expression in plants. Cell. Mol. Life Sci. 59, 1246-1255. https://doi.org/10.1007/s00018-002-8503-x
  66. Yan, H., Dobbie, Z., Gruber, S. B., Markowitz, S., Romans, K., Giardiello, F. M., Kinzler, K. W. and Vogelstein, B. (2002) Small changes in expression affect predisposition to tumorigenesis. Nat. Genet. 30, 25-26. https://doi.org/10.1038/ng799

피인용 문헌

  1. Laser-assisted microdissection for real-time PCR sample preparation vol.27, pp.2-3, 2006, https://doi.org/10.1016/j.mam.2005.12.006
  2. Microbead device for isolating biotinylated oligonucleotides for use in mass spectrometric analysis vol.384, pp.1, 2009, https://doi.org/10.1016/j.ab.2008.09.005
  3. Mechanistic data and cancer risk assessment: The need for quantitative molecular endpoints vol.45, pp.2-3, 2005, https://doi.org/10.1002/em.20093
  4. Quantitative evaluation of oligonucleotide surface concentrations using polymerization-based amplification vol.392, pp.1-2, 2008, https://doi.org/10.1007/s00216-008-2259-6
  5. Quantitative multi-gene transcriptional profiling using real-time PCR with a master template vol.79, pp.1, 2005, https://doi.org/10.1016/j.yexmp.2005.03.004
  6. Identification and validation of reference genes for gene expression studies in water buffalo vol.4, pp.06, 2010, https://doi.org/10.1017/S1751731110000042
  7. Head and neck squamous cell carcinoma transcriptome analysis by comprehensive validated differential display vol.25, pp.12, 2006, https://doi.org/10.1038/sj.onc.1209203
  8. Determination of Trace Deoxyribonucleic Acid by Using Fluorescein Isothiocyanate-Phenosafranine as a Double-Luminescent Phosphorescence Probe vol.21, pp.1, 2011, https://doi.org/10.1007/s10895-010-0705-2
  9. The ongoing evolution of qPCR vol.50, pp.4, 2010, https://doi.org/10.1016/j.ymeth.2010.02.005
  10. Analysis of gene expression as a new tool in ecotoxicology and environmental monitoring vol.26, pp.11, 2007, https://doi.org/10.1016/j.trac.2007.09.009
  11. Development and evaluation of real competitive PCR for high-throughput quantitative applications vol.339, pp.2, 2005, https://doi.org/10.1016/j.ab.2005.01.040
  12. Microarray analysis of the astrocyte transcriptome in the aging brain: relationship to Alzheimer's pathology and APOE genotype vol.32, pp.10, 2011, https://doi.org/10.1016/j.neurobiolaging.2011.04.013
  13. A simulation approach to assess the minimal number of real-time PCR replicates for GM quantification vol.227, pp.6, 2008, https://doi.org/10.1007/s00217-008-0899-6
  14. Involvement of the ubiquitin pathway in decreasing Ku70 levels in response to drug-induced apoptosis vol.312, pp.4, 2006, https://doi.org/10.1016/j.yexcr.2005.11.016
  15. Naked Eye DNA detection: Synthesis, characterization and DNA binding studies of a novel azo-guanidine vol.105, 2013, https://doi.org/10.1016/j.saa.2012.12.020
  16. Quantitative real-time RT-PCR data analysis: current concepts and the novel “gene expression’s C T difference” formula vol.84, pp.11, 2006, https://doi.org/10.1007/s00109-006-0097-6
  17. Retrieval Efficiency of DNA-Based Databases of Digital Signals vol.8, pp.3, 2009, https://doi.org/10.1109/TNB.2009.2026371
  18. Development of salt-tolerance interface for an high performance liquid chromatography/inductively coupled plasma mass spectrometry system and its application to accurate quantification of DNA samples vol.713, 2012, https://doi.org/10.1016/j.aca.2011.11.039
  19. Global Expression Profiling in Epileptogenesis: Does It Add to the Confusion? vol.20, pp.1, 2010, https://doi.org/10.1111/j.1750-3639.2008.00254.x
  20. Competitive PCR for precise nucleic acid quantification vol.2, pp.9, 2007, https://doi.org/10.1038/nprot.2007.299
  21. Isolation of male germ-line stem cells; influence of GDNF vol.279, pp.1, 2005, https://doi.org/10.1016/j.ydbio.2004.12.006
  22. Present and future of rapid and/or high-throughput methods for nucleic acid testing vol.363, pp.1-2, 2006, https://doi.org/10.1016/j.cccn.2005.07.009
  23. Ultrasensitive Determination of Absolute mRNA Amounts at Attomole Levels of Nearly Identical Plant Genes with High-Throughput Mass Spectrometry (MassARRAY) vol.48, pp.9, 2007, https://doi.org/10.1093/pcp/pcm103
  24. Comparison and evaluation of RNA quantification methods using viral, prokaryotic, and eukaryotic RNA over a 104 concentration range vol.387, pp.1, 2009, https://doi.org/10.1016/j.ab.2009.01.003
  25. Assessment of arbuscular mycorrhizal fungi on the phytoremediation potential of Ipomoea aquatica on cadmium uptake vol.2, pp.3, 2012, https://doi.org/10.1007/s13205-012-0046-8
  26. Estimation of microbial cover distributions at Mammoth Hot Springs using a multiple clone library resampling method vol.8, pp.7, 2006, https://doi.org/10.1111/j.1462-2920.2006.01003.x
  27. Feeding genetically modified maize (MON810) to dairy cows: comparison of gene expression pattern of markers for apoptosis, inflammation and cell cycle vol.7, pp.3, 2012, https://doi.org/10.1007/s00003-012-0778-8
  28. Calibration-curve-free quantitative PCR: A quantitative method for specific nucleic acid sequences without using calibration curves vol.369, pp.1, 2007, https://doi.org/10.1016/j.ab.2007.06.047
  29. Adaptive response in embryogenesis: VI. Comparative microarray analysis of gene expressions in mouse fetuses vol.85, pp.1, 2009, https://doi.org/10.1080/09553000802635039
  30. Biotechnological utilization of plant genetic resources for the production of phytopharmaceuticals vol.3, pp.02, 2005, https://doi.org/10.1079/PGR200564
  31. Selection of endogenous reference genes for gene expression analysis in Leishmania major developmental stages vol.101, pp.2, 2007, https://doi.org/10.1007/s00436-007-0491-1
  32. Prostate-specific antigen mRNA and protein levels in laser microdissected cells of human prostate measured by real-time reverse transcriptase–quantitative polymerase chain reaction and immuno–quantitative polymerase chain reaction vol.39, pp.10, 2008, https://doi.org/10.1016/j.humpath.2008.02.012
  33. Prolactin gene expression in primary central nervous system tumors vol.12, pp.1, 2013, https://doi.org/10.1186/1477-5751-12-4
  34. Evaluation of telomere length in human cardiac tissues using cardiac quantitative FISH vol.12, pp.9, 2017, https://doi.org/10.1038/nprot.2017.082
  35. Telomere Length vol.63, pp.4, 2014, https://doi.org/10.1097/NNR.0000000000000037
  36. Combined analysis of transcriptome and proteome data as a tool for the identification of candidate biomarkers in renal cell carcinoma vol.9, pp.6, 2009, https://doi.org/10.1002/pmic.200700288
  37. Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia vol.13, pp.2, 2008, https://doi.org/10.1038/sj.mp.4002011
  38. Photoperiodic mediation of differential gene expression in Scytosiphon lomentaria (Phaeophyceae) vol.60, pp.2, 2012, https://doi.org/10.1111/j.1440-1835.2012.00642.x
  39. Hepatic vasculitis presenting with multiple sterile liver abscesses in a patient with systemic lupus erythematosus vol.10, pp.1, 2007, https://doi.org/10.1111/j.1479-8077.2007.00259.x
  40. From differential gene expression to differential gene function and back vol.1, pp.2, 2004, https://doi.org/10.1016/j.ddtec.2004.09.005
  41. Identification of pathogenesis-related ESTs in the crucifer downy mildew oomycete Hyaloperonospora parasitica by high-throughput differential display analysis of distinct phenotypic interactions with Brassica oleracea vol.66, pp.3, 2006, https://doi.org/10.1016/j.mimet.2006.01.015
  42. Molecular predictors of response and outcome in ovarian cancer vol.60, pp.1, 2006, https://doi.org/10.1016/j.critrevonc.2006.03.003
  43. Quantitative DNA perturbations of p53 in endometriosis: analysis of American and Icelandic cases vol.84, pp.5, 2005, https://doi.org/10.1016/j.fertnstert.2005.05.031
  44. Development of a Taqman RT-PCR assay for the detection and quantification of negatively stranded RNA of human enteroviruses: Evidence for false-priming and improvement by tagged RT-PCR vol.153, pp.2, 2008, https://doi.org/10.1016/j.jviromet.2008.07.010
  45. Minimizing18O/16O back-exchange in the relative quantification of ribonucleic acids vol.44, pp.8, 2009, https://doi.org/10.1002/jms.1596
  46. ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development vol.39, pp.5, 2004, https://doi.org/10.1111/j.1365-313X.2004.02178.x
  47. Locked nucleic acids for optimizing displacement probes for quantitative real-time PCR vol.348, pp.2, 2006, https://doi.org/10.1016/j.ab.2005.10.037
  48. Gene expression analysis of wild Leishmania major isolates: identification of genes preferentially expressed in amastigotes vol.100, pp.2, 2007, https://doi.org/10.1007/s00436-006-0277-x
  49. Aerosolization of mycobacteria and legionellae during dental treatment: low exposure despite dental unit contamination vol.9, pp.11, 2007, https://doi.org/10.1111/j.1462-2920.2007.01395.x
  50. Isolation by size of epithelial tumor cells in peripheral blood of patients with breast cancer: correlation with real-time reverse transcriptase–polymerase chain reaction results and feasibility of molecular analysis by laser microdissection vol.37, pp.6, 2006, https://doi.org/10.1016/j.humpath.2006.01.026
  51. Relevant Spatial Scales of Chemical Variation in Aplysina aerophoba vol.9, pp.12, 2011, https://doi.org/10.3390/md9122499
  52. Bench-to-bedside review: Future novel diagnostics for sepsis - a systems biology approach vol.17, pp.5, 2013, https://doi.org/10.1186/cc12693
  53. Monitoring Differentiation of Human Embryonic Stem Cells Using Real-Time PCR vol.23, pp.10, 2005, https://doi.org/10.1634/stemcells.2005-0093
  54. Reference genes for quantitative analysis on Clonorchis sinensis gene expression by real-time PCR vol.104, pp.2, 2009, https://doi.org/10.1007/s00436-008-1195-x
  55. NMDA receptor subunit expression in GABAergic interneurons in the prefrontal cortex: Application of laser microdissection technique vol.176, pp.2, 2009, https://doi.org/10.1016/j.jneumeth.2008.09.013
  56. Epigenetic-based treatments emphasize the biologic differences of core-binding factor acute myeloid leukemias vol.32, pp.6, 2008, https://doi.org/10.1016/j.leukres.2007.11.038
  57. Bone marrow aspirate and biopsy: a pathologist's perspective. II. interpretation of the bone marrow aspirate and biopsy vol.23, pp.5, 2009, https://doi.org/10.1002/jcla.20305
  58. An efficient and economic enhancer mix for PCR vol.347, pp.3, 2006, https://doi.org/10.1016/j.bbrc.2006.06.151
  59. Selection of reference genes for qPCR in hairy root cultures of peanut vol.4, pp.1, 2011, https://doi.org/10.1186/1756-0500-4-392
  60. A single nucleotide polymorphism based approach for the identification and characterization of gene expression modulation using MassARRAY vol.573, pp.1-2, 2005, https://doi.org/10.1016/j.mrfmmm.2005.01.007
  61. DNA quantification approach by GE-ICP-SFMS and complementary total phosphorus determination by ICP-SFMS vol.21, pp.11, 2006, https://doi.org/10.1039/B607340A
  62. Pacific harbor seals (Phoca vitulina) and salmon: genetics presents hard numbers for elucidating predator-prey dynamics vol.147, pp.6, 2005, https://doi.org/10.1007/s00227-005-0047-9