Memory acquisition and retrieval impact different epigenetic processes that regulate gene expression

BMC Genomics

Volumn 16, Issue 5, 2015, Pages

  Peixoto, Lucia L ^a   Wimmer, Mathieu E ^a   Poplawski, Shane G ^a   Tudor, Jennifer C ^a   Kenworthy, Charles A ^a,b   Liu, Shichong ^a   Mizuno, Keiko ^c   Garcia, Benjamin A ^a   Zhang, Nancy R ^d   Giese, K Peter ^c   Abel, Ted ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Gene expression; Histone variants; Learning and memory; MicroRNAs; Normalization of unwanted variance

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II GAMMA; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; HISTONE; MICRORNA; RBFOX1 PROTEIN, MOUSE; RNA BINDING PROTEIN; RNA SPLICING FACTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CIRCADIAN RHYTHM; CONTROLLED STUDY; EPIGENETICS; FEAR CONDITIONING TEST; GENE; GENE EXPRESSION REGULATION; GENOME; HIPPOCAMPUS; IN VIVO STUDY; LONG TERM MEMORY; MALE; MEMORY DISORDER; MICRORNA 219 GENE; MOUSE; NONHUMAN; PROTEOMICS; QUANTITATIVE ANALYSIS; RBFOX1 GENE; TRANSCRIPTION TERMINATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CONDITIONING; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; SHORT TERM MEMORY;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CONDITIONING (PSYCHOLOGY); EPIGENESIS, GENETIC; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HISTONES; MALE; MEMORY, LONG-TERM; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; MICRORNAS; RNA SPLICING FACTORS; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84969264863     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-16-S5-S5     Document Type: Article

References (88)

1. Scherer A: Batch effects and noise in microarray experiments: sources and solutions. 2009, John Wiley & Sons
2. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003, 4: 249-264. 10.1093/biostatistics/4.2.249.
3. Agranoff BW, Davis RE, Casola L, Lim R: Actinomycin D blocks formation of memory of shock-avoidance in goldfish. Science. 1967, 158: 1600-1601. 10.1126/science.158.3808.1600.
4. Flood JF, Rosenzweig MR, Bennett EL, Orme AE: The influence of duration of protein synthesis inhibition on memory. Physiology & behavior. 1973, 10: 555-562. 10.1016/0031-9384(73)90221-7.
5. Zovkic IB, Guzman-Karlsson MC, Sweatt JD: Epigenetic regulation of memory formation and maintenance. Learn Mem. 2013, 20: 61-74. 10.1101/lm.026575.112.
6. Peixoto L, Abel T: The role of histone acetylation in memory formation and cognitive impairments. Neuropsychopharmacology. 2013, 38: 62-76. 10.1038/npp.2012.86.
7. Nelson ED, Monteggia LM: Epigenetics in the mature mammalian brain: effects on behavior and synaptic transmission. Neurobiol Learn Mem. 2011, 96: 53-60. 10.1016/j.nlm.2011.02.015.
8. Alberini CM: Transcription factors in long-term memory and synaptic plasticity. Physiol Rev. 2009, 89: 121-145. 10.1152/physrev.00017.2008.
9. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER: Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem. 1998, 5: 365-374.
10. Igaz LM, Vianna MR, Medina JH, Izquierdo I: Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning. J Neurosci. 2002, 22: 6781-6789.
11. Bekinschtein P, Katche C, Slipczuk L, Gonzalez C, Dorman G, Cammarota M, Izquierdo I, Medina JH: Persistence of Long-Term Memory Storage: New Insights into its Molecular Signatures in the Hippocampus and Related Structures. Neurotox Res.
12. Vianna MR, Igaz LM, Coitinho AS, Medina JH, Izquierdo I: Memory extinction requires gene expression in rat hippocampus. Neurobiol Learn Mem. 2003, 79: 199-203. 10.1016/S1074-7427(03)00003-0.
13. Power AE, Berlau DJ, McGaugh JL, Steward O: Anisomycin infused into the hippocampus fails to block "reconsolidation" but impairs extinction: the role of re-exposure duration. Learn Mem. 2006, 13: 27-34. 10.1101/lm.91206.
14. Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, Frankland PW, Kida S: Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci. 2009, 29: 402-413. 10.1523/JNEUROSCI.4639-08.2009.
15. Motanis H, Maroun M: Differential involvement of protein synthesis and actin rearrangement in the reacquisition of contextual fear conditioning. Hippocampus. 2012, 22: 494-500. 10.1002/hipo.20915.
16. Hermey G, Mahlke C, Gutzmann JJ, Schreiber J, Bluthgen N, Kuhl D: Genome-wide profiling of the activity-dependent hippocampal transcriptome. PLoS One. 2013, 8: e76903-10.1371/journal.pone.0076903.
17. Keeley MB, Wood MA, Isiegas C, Stein J, Hellman K, Hannenhalli S, Abel T: Differential transcriptional response to nonassociative and associative components of classical fear conditioning in the amygdala and hippocampus. Learning & memory. 2006, 13: 135-142. 10.1101/lm.86906.
18. Levenson JM, Choi S, Lee SY, Cao YA, Ahn HJ, Worley KC, Pizzi M, Liou HC, Sweatt JD: A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2004, 24: 3933-3943. 10.1523/JNEUROSCI.5646-03.2004.
19. Barnes P, Kirtley A, Thomas KL: Quantitatively and qualitatively different cellular processes are engaged in CA1 during the consolidation and reconsolidation of contextual fear memory. Hippocampus. 2012, 22: 149-171. 10.1002/hipo.20879.
20. Griggs EM, Young EJ, Rumbaugh G, Miller CA: MicroRNA-182 regulates amygdala-dependent memory formation. J Neurosci. 2013, 33: 1734-1740. 10.1523/JNEUROSCI.2873-12.2013.
21. Ahn HJ, Hernandez CM, Levenson JM, Lubin FD, Liou HC, Sweatt JD: c-Rel, an NF-kappaB family transcription factor, is required for hippocampal long-term synaptic plasticity and memory formation. Learn Mem. 2008, 15: 539-549. 10.1101/lm.866408.
22. Leach PT, Poplawski SG, Kenney JW, Hoffman B, Liebermann DA, Abel T, Gould TJ: Gadd45b knockout mice exhibit selective deficits in hippocampus-dependent long-term memory. Learn Mem. 2012, 19: 319-324. 10.1101/lm.024984.111.
23. Abdi H, Williams LJ: Principal component analysis. Wiley Interdisciplinary Reviews: Computational Statistics. 2010, 2: 433-459. 10.1002/wics.101.
24. Devan BD, Goad EH, Petri HL, Antoniadis EA, Hong NS, Ko CH, Leblanc L, Lebovic SS, Lo Q, Ralph MR, McDonald RJ: Circadian phase-shifted rats show normal acquisition but impaired long-term retention of place information in the water task. Neurobiology of learning and memory. 2001, 75: 51-62. 10.1006/nlme.1999.3957.
25. Tapp WN, Holloway FA: Phase shifting circadian rhythms produces retrograde amnesia. Science. 1981, 211: 1056-1058. 10.1126/science.7193351.
26. Stephan FK, Kovacevic NS: Multiple retention deficit in passive avoidance in rats is eliminated by suprachiasmatic lesions. Behavioral biology. 1978, 22: 456-462. 10.1016/S0091-6773(78)92565-8.
27. Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, Baggs JE, Panda S, Hogenesch JB: Harmonics of circadian gene transcription in mammals. PLoS genetics. 2009, 5: e1000442-10.1371/journal.pgen.1000442.
28. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, et al: A gene atlas of the mouse and human protein-encoding transcriptomes. Proceedings of the National Academy of Sciences of the United States of America. 2004, 101: 6062-6067. 10.1073/pnas.0400782101.
29. Steward O, Wallace CS, Lyford GL, Worley PF: Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron. 1998, 21: 741-751. 10.1016/S0896-6273(00)80591-7.
30. Zheng F, Zhou X, Moon C, Wang H: Regulation of brain-derived neurotrophic factor expression in neurons. International journal of physiology, pathophysiology and pharmacology. 2012, 4: 188-200.
31. Oike Y, Hata A, Mamiya T, Kaname T, Noda Y, Suzuki M, Yasue H, Nabeshima T, Araki K, Yamamura K: Truncated CBP protein leads to classical Rubinstein-Taybi syndrome phenotypes in mice: implications for a dominant-negative mechanism. Human molecular genetics. 1999, 8: 387-396. 10.1093/hmg/8.3.387.
32. Wood MA, Kaplan MP, Park A, Blanchard EJ, Oliveira AM, Lombardi TL, Abel T: Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learning & memory. 2005, 12: 111-119. 10.1101/lm.86605.
33. Alarcon JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, Barco A: Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron. 2004, 42: 947-959. 10.1016/j.neuron.2004.05.021.
34. Korzus E, Rosenfeld MG, Mayford M: CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron. 2004, 42: 961-972. 10.1016/j.neuron.2004.06.002.
35. Bourtchouladze R, Lidge R, Catapano R, Stanley J, Gossweiler S, Romashko D, Scott R, Tully T: A mouse model of Rubinstein-Taybi syndrome: defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proceedings of the National Academy of Sciences of the United States of America. 2003, 100: 10518-10522. 10.1073/pnas.1834280100.
36. Oliveira AM, Estevez MA, Hawk JD, Grimes S, Brindle PK, Abel T: Subregion-specific p300 conditional knock-out mice exhibit long-term memory impairments. Learning & memory. 2011, 18: 161-169. 10.1101/lm.1939811.
37. Oliveira AM, Wood MA, McDonough CB, Abel T: Transgenic mice expressing an inhibitory truncated form of p300 exhibit long-term memory deficits. Learning & memory. 2007, 14: 564-572. 10.1101/lm.656907.
38. Efron B: Large-scale simultaneous hypothesis testing: The choice of a null hypothesis. Journal of the American Statistical Association. 2004, 99: 96-104. 10.1198/016214504000000089.
39. Benjamini Y, Hochberg Y: Controlling the False Discovery Rate - a Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B-Methodological. 1995, 57: 289-300.
40. Farioli-Vecchioli S, Saraulli D, Costanzi M, Leonardi L, Cina I, Micheli L, Nutini M, Longone P, Oh SP, Cestari V, Tirone F: Impaired terminal differentiation of hippocampal granule neurons and defective contextual memory in PC3/Tis21 knockout mice. PLoS One. 2009, 4: e8339-10.1371/journal.pone.0008339.
41. Li H, Radford JC, Ragusa MJ, Shea KL, McKercher SR, Zaremba JD, Soussou W, Nie Z, Kang YJ, Nakanishi N, et al: Transcription factor MEF2C influences neural stem/progenitor cell differentiation and maturation in vivo. Proc Natl Acad Sci USA. 2008, 105: 9397-9402. 10.1073/pnas.0802876105.
42. Cole CJ, Mercaldo V, Restivo L, Yiu AP, Sekeres MJ, Han JH, Vetere G, Pekar T, Ross PJ, Neve RL, et al: MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nat Neurosci. 2012, 15: 1255-1264. 10.1038/nn.3189.
43. Berdeaux R, Goebel N, Banaszynski L, Takemori H, Wandless T, Shelton GD, Montminy M: SIK1 is a class II HDAC kinase that promotes survival of skeletal myocytes. Nat Med. 2007, 13: 597-603. 10.1038/nm1573.
44. Finsterwald C, Carrard A, Martin JL: Role of salt-inducible kinase 1 in the activation of MEF2-dependent transcription by BDNF. PLoS One. 2013, 8: e54545-10.1371/journal.pone.0054545.
45. Li S, Zhang C, Takemori H, Zhou Y, Xiong ZQ: TORC1 regulates activity-dependent CREB-target gene transcription and dendritic growth of developing cortical neurons. J Neurosci. 2009, 29: 2334-2343. 10.1523/JNEUROSCI.2296-08.2009.
46. Katoh Y, Takemori H, Lin XZ, Tamura M, Muraoka M, Satoh T, Tsuchiya Y, Min L, Doi J, Miyauchi A, et al: Silencing the constitutive active transcription factor CREB by the LKB1-SIK signaling cascade. FEBS J. 2006, 273: 2730-2748. 10.1111/j.1742-4658.2006.05291.x.
47. Jilg A, Lesny S, Peruzki N, Schwegler H, Selbach O, Dehghani F, Stehle JH: Temporal dynamics of mouse hippocampal clock gene expression support memory processing. Hippocampus. 2010, 20: 377-388.
48. Cheval H, Chagneau C, Levasseur G, Veyrac A, Faucon-Biguet N, Laroche S, Davis S: Distinctive features of Egr transcription factor regulation and DNA binding activity in CA1 of the hippocampus in synaptic plasticity and consolidation and reconsolidation of fear memory. Hippocampus. 2012, 22: 631-642. 10.1002/hipo.20926.
49. Lubin FD, Roth TL, Sweatt JD: Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci. 2008, 28: 10576-10586. 10.1523/JNEUROSCI.1786-08.2008.
50. Sakamoto K, Karelina K, Obrietan K: CREB: a multifaceted regulator of neuronal plasticity and protection. Journal of neurochemistry. 2011, 116: 1-9. 10.1111/j.1471-4159.2010.07080.x.
51. Oikawa K, Odero GL, Platt E, Neuendorff M, Hatherell A, Bernstein MJ, Albensi BC: NF-kappaB p50 subunit knockout impairs late LTP and alters long term memory in the mouse hippocampus. BMC neuroscience. 2012, 13: 45-10.1186/1471-2202-13-45.
52. Chen P, Zhao J, Li G: Histone variants in development and diseases. J Genet Genomics. 2013, 40: 355-365. 10.1016/j.jgg.2013.05.001.
53. Pina B, Suau P: Changes in histones H2A and H3 variant composition in differentiating and mature rat brain cortical neurons. Dev Biol. 1987, 123: 51-58. 10.1016/0012-1606(87)90426-X.
54. Santoro SW, Dulac C: The activity-dependent histone variant H2BE modulates the life span of olfactory neurons. Elife. 2012, 1: e00070-
55. Fogel BL, Wexler E, Wahnich A, Friedrich T, Vijayendran C, Gao F, Parikshak N, Konopka G, Geschwind DH: RBFOX1 regulates both splicing and transcriptional networks in human neuronal development. Hum Mol Genet. 2012, 21: 4171-4186. 10.1093/hmg/dds240.
56. Gehman LT, Stoilov P, Maguire J, Damianov A, Lin CH, Shiue L, Ares M, Mody I, Black DL: The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat Genet. 2011, 43: 706-711. 10.1038/ng.841.
57. Mikhail FM, Lose EJ, Robin NH, Descartes MD, Rutledge KD, Rutledge SL, Korf BR, Carroll AJ: Clinically relevant single gene or intragenic deletions encompassing critical neurodevelopmental genes in patients with developmental delay, mental retardation, and/or autism spectrum disorders. Am J Med Genet A. 2011, 2386-2396. 155A
58. Antunes-Martins A, Mizuno K, Irvine EE, Lepicard EM, Giese KP: Sex-dependent up-regulation of two splicing factors, Psf and Srp20, during hippocampal memory formation. Learn Mem. 2007, 14: 693-702. 10.1101/lm.640307.
59. Wibrand K, Panja D, Tiron A, Ofte ML, Skaftnesmo KO, Lee CS, Pena JT, Tuschl T, Bramham CR: Differential regulation of mature and precursor microRNA expression by NMDA and metabotropic glutamate receptor activation during LTP in the adult dentate gyrus in vivo. Eur J Neurosci. 2010, 31: 636-645. 10.1111/j.1460-9568.2010.07112.x.
60. Tognini P, Pizzorusso T: MicroRNA212/132 family: molecular transducer of neuronal function and plasticity. Int J Biochem Cell Biol. 2012, 44: 6-10. 10.1016/j.biocel.2011.10.015.
61. Kocerha J, Faghihi MA, Lopez-Toledano MA, Huang J, Ramsey AJ, Caron MG, Sales N, Willoughby D, Elmen J, Hansen HF, et al: MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction. Proc Natl Acad Sci USA. 2009, 106: 3507-3512. 10.1073/pnas.0805854106.
62. Tsien JZ, Huerta PT, Tonegawa S: The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell. 1996, 87: 1327-1338. 10.1016/S0092-8674(00)81827-9.
63. Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S: NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci. 2004, 5: 361-372. 10.1038/nrn1385.
64. Han Z, He H, Zhang F, Huang Z, Liu Z, Jiang H, Wu Q: Spatiotemporal expression pattern of Mirg, an imprinted non-coding gene, during mouse embryogenesis. J Mol Histol. 2012, 43: 1-8. 10.1007/s10735-011-9367-x.
65. Wheeler G, Ntounia-Fousara S, Granda B, Rathjen T, Dalmay T: Identification of new central nervous system specific mouse microRNAs. FEBS Lett. 2006, 580: 2195-2200. 10.1016/j.febslet.2006.03.019.
66. Hansen KF, Karelina K, Sakamoto K, Wayman GA, Impey S, Obrietan K: miRNA-132: a dynamic regulator of cognitive capacity. Brain Struct Funct. 2013, 218: 817-831. 10.1007/s00429-012-0431-4.
67. Hansen KF, Sakamoto K, Wayman GA, Impey S, Obrietan K: Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS One. 2010, 5: e15497-10.1371/journal.pone.0015497.
68. Chen L, Zhang J, Feng Y, Li R, Sun X, Du W, Piao X, Wang H, Yang D, Sun Y, et al: MiR-410 regulates MET to influence the proliferation and invasion of glioma. Int J Biochem Cell Biol. 2012, 44: 1711-1717. 10.1016/j.biocel.2012.06.027.
69. Campbell DB, D'Oronzio R, Garbett K, Ebert PJ, Mirnics K, Levitt P, Persico AM: Disruption of cerebral cortex MET signaling in autism spectrum disorder. Ann Neurol. 2007, 62: 243-250. 10.1002/ana.21180.
70. Rogelj B, Hartmann CE, Yeo CH, Hunt SP, Giese KP: Contextual fear conditioning regulates the expression of brain-specific small nucleolar RNAs in hippocampus. Eur J Neurosci. 2003, 18: 3089-3096. 10.1111/j.1460-9568.2003.03026.x.
71. Da Silva WC, Cardoso G, Bonini JS, Benetti F, Izquierdo I: Memory reconsolidation and its maintenance depend on L-voltage-dependent calcium channels and CaMKII functions regulating protein turnover in the hippocampus. Proc Natl Acad Sci USA. 2013, 110: 6566-6570. 10.1073/pnas.1302356110.
72. Fiorenza NG, Rosa J, Izquierdo I, Myskiw JC: Modulation of the extinction of two different fear-motivated tasks in three distinct brain areas. Behav Brain Res. 2012, 232: 210-216. 10.1016/j.bbr.2012.04.015.
73. Myers KM, Carlezon WA, Davis M: Glutamate receptors in extinction and extinction-based therapies for psychiatric illness. Neuropsychopharmacology. 2011, 36: 274-293. 10.1038/npp.2010.88.
74. Sanhueza M, Lisman J: The CaMKII/NMDAR complex as a molecular memory. Molecular Brain. 2013, 6: 10-10.1186/1756-6606-6-10.
75. Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S: Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci. 2004, 24: 4787-4795. 10.1523/JNEUROSCI.5491-03.2004.
76. von Hertzen LS, Giese KP: Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci. 2005, 25: 1935-1942. 10.1523/JNEUROSCI.4707-04.2005.
77. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al: Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004, 5: R80-10.1186/gb-2004-5-10-r80.
78. Gasch AP, Eisen MB: Exploring the conditional coregulation of yeast gene expression through fuzzy k-means clustering. Genome Biology. 2002, 3: RESEARCH0059-
79. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA: DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 2003, 4: P3-10.1186/gb-2003-4-5-p3.
80. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, Jensen LJ: STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Research. 2013, 41: D808-815. 10.1093/nar/gks1094.
81. Hartigan JA, Wong MA: Algorithm AS 136: A K-Means Clustering Algorithm. Journal of the Royal Statistical Society Series C (Applied Statistics). 1979, 28: 100-108.
82. Plazas-Mayorca MD, Zee BM, Young NL, Fingerman IM, LeRoy G, Briggs SD, Garcia BA: One-pot shotgun quantitative mass spectrometry characterization of histones. J Proteome Res. 2009, 8: 5367-5374. 10.1021/pr900777e.
83. Fischer S, Brunk BP, Chen F, Gao X, Harb OS, Iodice JB, Shanmugam D, Roos DS, Stoeckert CJ: Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Curr Protoc Bioinformatics. 2011, Chapter 6 (Unit 6 12): 11-19.
84. Taly JF, Magis C, Bussotti G, Chang JM, Di Tommaso P, Erb I, Espinosa-Carrasco J, Kemena C, Notredame C: Using the T-Coffee package to build multiple sequence alignments of protein, RNA, DNA sequences and 3D structures. Nat Protoc. 2011, 6: 1669-1682. 10.1038/nprot.2011.393.
85. Criscuolo A: morePhyML: improving the phylogenetic tree space exploration with PhyML 3. Mol Phylogenet Evol. 2011, 61: 944-948. 10.1016/j.ympev.2011.08.029.
86. Letunic I, Bork P: Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 2011, 39: W475-478. 10.1093/nar/gkr201.
87. Jiao XL, Sherman BT, Huang DW, Stephens R, Baseler MW, Lane HC, Lempicki RA: DAVID-WS: a stateful web service to facilitate gene/protein list analysis. Bioinformatics. 2012, 28: 1805-1806. 10.1093/bioinformatics/bts251.
88. Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C: T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 2011, 39: W13-17. 10.1093/nar/gkr245.