MicroSAGE is highly representative and reproducible but reveals major differences in gene expression among samples obtained from similar tissues

Genome Biology

Volumn 4, Issue 3, 2003, Pages

  Blackshaw, Seth ^a   Kuo, Winston P ^b,c   Park, Peter J ^b   Tsujikawa, Motokazu ^b   Gunnersen, Jenny M ^d   Scott, Hamish S ^d   Boon, Wee Ming ^d   Tan, Seong Seng ^d   Cepko, Constance L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Additional Data File; Adult Retina; Mouse Retina; Outer Nuclear Layer; Retina

Indexed keywords

ADULT; AGED; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MOUSE; RETINA; SERIAL ANALYSIS OF GENE EXPRESSION; AGE; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CELL LINE; CELL STRAIN 3T3; CHEMISTRY; COMPARATIVE STUDY; DNA MICROARRAY; GENE; GENE EXPRESSION PROFILING; GENE LIBRARY; GENETIC VARIABILITY; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR COMPUTER; SEX DIFFERENCE; VALIDATION STUDY;

3T3 CELLS; ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; ANIMALS; CELL LINE; COMPUTERS, MOLECULAR; FEMALE; GENE EXPRESSION PROFILING; GENE LIBRARY; GENES, CDC; HUMANS; MALE; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; RETINA; SEX FACTORS; VARIATION (GENETICS);

EID: 18544392723     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2003-4-3-r17     Document Type: Article

References (57)

1. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW: Serial analysis of gene expression. Science. 1995, 270: 484-487. DOI: 10.1126/science.270.5235.484
2. Velculescu VE, Zhang L, Zhou W, Vogelstein J, Basrai MA, Bassett DE, Hieter P, Vogelstein B, Kinzler KW: Characterization of the yeast transcriptome. Cell. 1997, 88: 243-251. DOI: 10.1016/S0092-8674(00)81845-0
3. Jones SJ, Riddle DL, Pouzyrev AT, Velculescu VE, Hillier L, Eddy SR, Stricklin SL, Baillie DL, Waterston R, Marra MA: Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans. Genome Res. 2001, 11: 1346-1352. 10.1101/gr.184401. DOI: 10.1101/gr.184401
4. Kal AJ, van Zonneveld AJ, Benes V, van den Berg M, Koerkamp MG, Albermann K, Strack N, Ruijter JM, Richter A, Dujon B, et al: Dynamics of gene expression revealed by comparison of serial analysis of gene expression transcript profiles from yeast grown on two different carbon sources. Mol Biol Cell. 1999, 10: 1859-1872. DOI: 10.1091/mbc.10.6.1859
5. Matsumura H, Nirasawa S, Terauchi R: Technical advance: transcript profiling in rice (Oryza sativa L.) seedlings using serial analysis of gene expression (SAGE). Plant J. 1999, 20: 719-726. 10.1046/j.1365-313X.1999.00640.x. DOI: 10.1046/j.1365-313X.1999.00640.x
6. Datson NA, van der Perk-de Jong J, van den Berg MP, de Kloet ER, Vreugdenhil E: MicroSAGE: a modified procedure for serial analysis of gene expression in limited amounts of tissue. Nucleic Acids Res. 1999, 27: 1300-1307. 10.1093/nar/27.5.1300. DOI: 10.1093/nar/27.5.1300
7. Peters DG, Kassam AB, Yonas H, O'Hare EH, Ferrell RE, Brufsky AM: Comprehensive transcript analysis in small quantities of mRNA by SAGE-lite. Nucleic Acids Res. 1999, 27: e39-10.1093/nar/27.24.e39. DOI: 10.1093/nar/27.24.e39
8. Ye SQ, Zhang LQ, Zheng F, Virgil D, Kwiterovich PO: MiniSAGE: gene expression profiling using serial analysis of gene expression from 1 microgram total RNA. Anal Biochem. 2000, 287: 144-152. 10.1006/abio.2000.4846. DOI: 10.1006/abio.2000.4846
9. Virlon B, Cheval L, Buhler JM, Billon E, Doucet A, Elalouf JM: Serial microanalysis of renal transcriptomes. Proc Natl Acad Sci USA. 1999, 96: 15286-15291. 10.1073/pnas.96.26.15286. DOI: 10.1073/pnas.96.26.15286
10. St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, Lal A, Riggins GJ, Lengauer C, Vogelstein B, Kinzler KW: Genes expressed in human tumor endothelium. Science. 2000, 289: 1197-202. 10.1126/science.289.5482.1197. DOI: 10.1126/science.289.5482.1197
11. Croizat B, Berthelot F, Felsani A, Gros F: Complexity of polysomal polyadenylated RNA in mouse whole brain and cortex. FEBS Lett. 1979, 103: 138-143. 10.1016/0014-5793(79)81267-3. DOI: 10.1016/0014-5793(79)81267-3
12. Treisman J, Morabito MA, Barnstable C: Opsin expression in the rat retina is developmentally regulated by transcription activation. Mol Cell Biol. 1988, 8: 1570-1579. DOI: 10.1128/MCB.8.4.1570
13. Blackshaw S, Fraioli RE, Furukawa T, Cepko C: Comprehensive analysis of photoreceptor gene expression and the identification of candidate retina disease genes. Cell. 2001, 107: 579-589. DOI: 10.1016/S0092-8674(01)00574-8
14. Morrow EM, Belliveau MJ, Cepko CL: Two phases of rod photoreceptor differentiation during rat retinal development. J Neurosci. 1998, 18: 3738-3748.
15. Morrow EM, Furukawa T, Cepko CL: Vertebrate photoreceptor cell development and disease. Trends Cell Biol. 1998, 8: 353-358. 10.1016/S0962-8924(98)01341-5. DOI: 10.1016/S0962-8924(98)01341-5
16. Alexiades MR, Cepko CL: Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev Dyn. 1996, 205: 293-307. 10.1002/(SICI)1097-0177(199603)205:3<293::AID-AJA9>3.0.CO;2-D. DOI: 10.1002/(SICI)1097-0177(199603)205:3<293::AID-AJA9>3.0.CO;2-D
17. Young RW: Cell proliferation during postnatal development of the retina in the mouse. Dev Brain Res. 1985, 21: 229-239. 10.1016/0165-3806(85)90211-1. DOI: 10.1016/0165-3806(85)90211-1
18. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, et al: Molecular portraits of human breast tumours. Nature. 2000, 406: 747-752. 10.1038/35021093. DOI: 10.1038/35021093
19. Golub TR, Slonim DK, Tamayo P, Huard C, Gaasenbeek M, Mesirov JP, Coller H, Loh ML, Downing JR, Caligiuri MA, et al: Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999, 286: 531-537. 10.1126/science.286.5439.531. DOI: 10.1126/science.286.5439.531
20. Audic S, Claverie JM: The significance of digital gene expression profiles. Genome Res. 1997, 7: 986-995.
21. Lee ML, Kuo FC, Whitmore GA, Sklar J: Importance of replication in microarray gene expression studies: statistical methods and evidence from repetitive cDNA hybridizations. Proc Natl Acad Sci USA. 2000, 97: 9834-9839. 10.1073/pnas.97.18.9834. DOI: 10.1073/pnas.97.18.9834
22. Yue H, Eastman PS, Wang BB, Minor J, Doctolero MH, Nuttall RL, Stack R, Becker JW, Montgomery JR, Vainer M, Johnston R: An evaluation of the performance of cDNA microarrays for detecting changes in global mRNA expression. Nucleic Acids Res. 2001, 29: e41-10.1093/nar/29.8.e41. DOI: 10.1093/nar/29.8.e41
23. Livesey FJ, Furukawa T, Steffen MA, Church GM, Cepko CL: Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene Crx. Curr Biol. 2000, 10: 301-310. 10.1016/S0960-9822(00)00379-1. DOI: 10.1016/S0960-9822(00)00379-1
24. Margulies EH, Kardia SL, Innis JW: Identification and prevention of a GC content bias in SAGE libraries. Nucleic Acids Res. 2001, 29: e60-10.1093/nar/29.12.e60. DOI: 10.1093/nar/29.12.e60
25. Weindruch R, Kayo T, Lee CK, Prolla TA: Gene expression profiling of aging using DNA microarrays. Mech Ageing Dev. 2002, 123: 177-193. 10.1016/S0047-6374(01)00344-X. DOI: 10.1016/S0047-6374(01)00344-X
26. Haslett JN, Sanoudou D, Kho AT, Bennett RR, Greenberg SA, Kohane IS, Beggs AH, Kunkel LM: Gene expression comparison of biopsies from Duchenne muscular dystrophy (DMD) and normal skeletal muscle. Proc Natl Acad Sci USA. 2002, 99: 15000-15005. 10.1073/pnas.192571199. DOI: 10.1073/pnas.192571199
27. Yoshida S, Yashar BM, Hiriyanna S, Swaroop A: Microarray analysis of gene expression in the aging human retina. Invest Ophthalmol Vis Sci. 2002, 43: 2554-2560.
28. Callow MJ, Dudoit S, Gong EL, Speed TP, Rubin EM: Microarray expression profiling identifies genes with altered expression in HDL-deficient mice. Genome Res. 2000, 10: 2022-2029. 10.1101/gr.10.12.2022. DOI: 10.1101/gr.10.12.2022
29. Zirlinger M, Kreiman G, Anderson DJ: Amygdala-enriched genes identified by microarray technology are restricted to specific amygdaloid subnuclei. Proc Natl Acad Sci USA. 2001, 98: 5270-5275. 10.1073/pnas.091094698. DOI: 10.1073/pnas.091094698
30. Clinton M, Manson J, McBride D, Miele G: Gene expression changes during murine postnatal brain development. Genome Biol. 2000, 1: research0005.1-0005.11. 10.1186/gb-2000-1-3-research0005. DOI: 10.1186/gb-2000-1-3-research0005
31. Chrast R, Scott HS, Papasavvas MP, Rossier C, Antonarakis ES, Barras C, Davisson MT, Schmidt C, Estivill X, Dierssen M, et al: The mouse brain transcriptome by SAGE: differences in gene expression between P30 brains of the partial trisomy 16 mouse model of Down syndrome (Ts65Dn) and normals. Genome Res. 2000, 10: 2006-2021. 10.1101/gr.10.12.2006. DOI: 10.1101/gr.10.12.2006
32. Humpherys D, Eggan K, Akutsu H, Friedman A, Hochedlinger K, Yanagimachi R, Lander ES, Golub TR, Jaenisch R: Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc Natl Acad Sci USA. 2002, 99: 12889-12894. 10.1073/pnas.192433399. DOI: 10.1073/pnas.192433399
33. Tudor M, Akbarian S, Chen RZ, Jaenisch R: Transcriptional profiling of a mouse model for Rett syndrome reveals subtle transcriptional changes in the brain. Proc Natl Acad Sci USA. 2002, 99: 15536-15541. 10.1073/pnas.242566899. DOI: 10.1073/pnas.242566899
34. Alfonso J, Pollevick GD, Castensson A, Jazin E, Frasch AC: Analysis of gene expression in the rat hippocampus reveals high inter-individual variation in mRNA expression levels. J Neurosci Res. 2002, 67: 225-234. 10.1002/jnr.10105. DOI: 10.1002/jnr.10105
35. Pritchard CC, Hsu L, Delrow J, Nelson PS: Project normal: defining normal variance in mouse gene expression. Proc Natl Acad Sci USA. 2001, 98: 13266-13271. 10.1073/pnas.221465998. DOI: 10.1073/pnas.221465998
36. Lee CK, Weindruch R, Prolla TA: Gene-expression profile on the ageing brain in mice. Nat Genet. 2000, 25: 294-297. 10.1038/77046. DOI: 10.1038/77046
37. Lee CK, Klopp RG, Weindruch R, Prolla TA: Gene expression profile of aging and its retardation by caloric restriction. Science. 1999, 285: 1390-1393. 10.1126/science.285.5432.1390. DOI: 10.1126/science.285.5432.1390
38. Sandberg R, Yasuda R, Pankratz DG, Carter TA, Del Rio JA, Wodicka L, Mayford M, Lockhart DJ, Barlow C: Regional and strain-specific gene expression mapping in the adult mouse brain. Proc Natl Acad Sci USA. 2000, 97: 11038-11043. 10.1073/pnas.97.20.11038. DOI: 10.1073/pnas.97.20.11038
39. Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, Schultz PG, Tsien JZ, Hu Y: Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci USA. 2000, 97: 12880-12884. 10.1073/pnas.97.23.12880. DOI: 10.1073/pnas.97.23.12880
40. Yue H, Eastman PS, Wang BB, Minor J, Doctolero MH, Nuttall RL, Stack R, Becker JW, Montgomery JR, Vainer M, Johnston R: An evaluation of the performance of cDNA microarrays for detecting changes in global mRNA expression. Nucleic Acids Res. 2001, 29: e41-10.1093/nar/29.8.e41. DOI: 10.1093/nar/29.8.e41
41. Yuen T, Wurmbach E, Pfeffer RL, Ebersole BJ, Sealfon SC: Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res. 2002, 30: e48-10.1093/nar/30.10.e48. DOI: 10.1093/nar/30.10.e48
42. Kuo WP, Jenssen TK, Butte AJ, Ohno-Machado L, Kohane IS: Analysis of matched mRNA measurements from two different microarray technologies. Bioinformatics. 2002, 18: 405-412. 10.1093/bioinformatics/18.3.405. DOI: 10.1093/bioinformatics/18.3.405
43. Kothapalli R, Yoder SJ, Mane S, Loughran TP: Microarray results: how accurate are they?. BMC Bioinformatics. 2002, 3: 22-10.1186/1471-2105-3-22. DOI: 10.1186/1471-2105-3-22
44. Jeon CJ, Strettoi E, Masland RH: The major cell populations of the mouse retina. J Neurosci. 1998, 18: 8936-8946.
45. Sharon D, Blackshaw S, Cepko CL, Dryja TP: Profile of the genes expressed in the human peripheral retina, macula, and retinal pigment epithelium determined through serial analysis of gene expression (SAGE). Proc Natl Acad Sci USA. 2002, 99: 315-320. 10.1073/pnas.012582799. DOI: 10.1073/pnas.012582799
46. Johnson SA, Morgan DG, Finch CE: Extensive postmortem stability of RNA from rat and human brain. J Neurosci Res. 1986, 16: 267-280. DOI: 10.1002/jnr.490160123
47. Lukiw WJ, Wong L, McLachlan DR: Cytoskeletal messenger RNA stability in human neocortex: studies in normal aging and in Alzheimer's disease. Int J Neurosci. 1990, 55: 81-88. DOI: 10.3109/00207459008985953
48. Marchuk L, Sciore P, Reno C, Frank CB, Hart DA: Postmortem stability of total RNA isolated from rabbit ligament, tendon and cartilage. Biochim Biophys Acta. 1998, 1379: 171-177. 10.1016/S0304-4165(97)00094-9. DOI: 10.1016/S0304-4165(97)00094-9
49. Castensson A, Emilsson L, Preece P, Jazin EE: High-resolution quantification of specific mRNA levels in human brain autopsies and biopsies. Genome Res. 2000, 10: 1219-1229. 10.1101/gr.10.8.1219. DOI: 10.1101/gr.10.8.1219
50. Crabbe JC, Wahlsten D, Dudek BC: Genetics of mouse behavior: interactions with laboratory environment. Science. 1999, 284: 1670-1672. 10.1126/science.284.5420.1670. DOI: 10.1126/science.284.5420.1670
51. Eggan K, Akutsu H, Loring J, Jackson-Grusby L, Klemm M, Rideout WM, Yanagimachi R, Jaenisch R: Hybrid vigor, fetal overgrowth, and viability of mice derived by nuclear cloning and tetraploid embryo complementation. Proc Natl Acad Sci USA. 2001, 98: 6209-6214. 10.1073/pnas.101118898. DOI: 10.1073/pnas.101118898
52. McGue M, Bouchard TJ: Genetic and environmental influences on human behavioral differences. Annu Rev Neurosci. 1998, 21: 1-24. 10.1146/annurev.neuro.21.1.1. DOI: 10.1146/annurev.neuro.21.1.1
53. Cournil A, Kirkwood TB: If you would live long, choose your parents well. Trends Genet. 2001, 17: 233-235. 10.1016/S0168-9525(01)02306-X. DOI: 10.1016/S0168-9525(01)02306-X
54. SAGE: serial analysis of gene expression. [http://www.sagenet.org]
55. Zhang L, Zhou W, Velculescu VE, Kern SE, Hruban RH, Hamilton SR, Vogelstein B, Kinzler KW: Gene expression profiles in normal and cancer cells. Science. 1997, 276: 1268-1272. 10.1126/science.276.5316.1268. DOI: 10.1126/science.276.5316.1268
56. Chen H, Centola M, Altschul SF, Metzger H: Characterization of gene expression in resting and activated mast cells. J Exp Med. 1998, 188: 1657-1668. 10.1084/jem.188.9.1657. DOI: 10.1084/jem.188.9.1657
57. Melbourne brain genome project. [http://www.mbgproject.org/MBGP_Data_files.html]