Transcriptional response to cardiac injury in the zebrafish: Systematic identification of genes with highly concordant activity across in vivo models

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Rodius, Sophie ^a   Nazarov, Petr V ^a   Nepomuceno Chamorro, Isabel A ^b   Jeanty, Céline ^a   González Rosa, Juan M ^c   Ibberson, Mark ^d   da Costa, Ricardo M B ^e   Xenarios, Ioannis ^d,e,f   Mercader, Nadia ^g   Azuaje, Francisco ^a  

^a LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^b UNIVERSITY OF SEVILLE   (Spain)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

^f UNIVERSITY OF GENEVA   (Switzerland)

^g CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

Heart regeneration; Myocardial infarction; Transcriptional association networks; Transcriptional responses; Ventricular amputation; Ventricular cryoinjury; Zebrafish

Indexed keywords

COLLAGENASE 3; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 4; UBIQUITIN; UBIQUITIN SPECIFIC PEPTIDASE 2; UNCLASSIFIED DRUG; CYTOCHROME P450; PROTEIN P53; PROTEINASE; TRANSCRIPTOME; ZEBRAFISH PROTEIN;

ACTA1 GENE; ARTICLE; CA2 GENE; CELL DIFFERENTIATION; CELL FATE; COLD INJURY; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; HEART INJURY; IN VIVO STUDY; MAPK4 GENE; MICROARRAY ANALYSIS; MMP13A GENE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN FUNCTION; PTGIS GENE; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION; RNA EXTRACTION; SGCE GENE; SIGNAL TRANSDUCTION; TISSUE REGENERATION; TISSUE REPAIR; TRANSCRIPTION INITIATION; USP2A GENE; ZEBRA FISH; ANIMAL; BIOLOGY; DISEASE MODEL; DNA MICROARRAY; GENETICS; HEART; HEART MUSCLE; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REGENERATION; TIME;

DANIO RERIO;

ANIMALS; COMPUTATIONAL BIOLOGY; CYTOCHROME P-450 ENZYME SYSTEM; DISEASE MODELS, ANIMAL; ENDOPEPTIDASES; HEART; HEART INJURIES; MYOCARDIUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REGENERATION; TIME FACTORS; TRANSCRIPTOME; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84910074878     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-852     Document Type: Article

References (77)

1. Bakkers J. Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res 2011, 91(2):279-288. 10.1093/cvr/cvr098, 3125074, 21602174.
2. Gemberling M, Bailey TJ, Hyde DR, Poss KD. The zebrafish as a model for complex tissue regeneration. Trends Genet 2013, 29(11):611-620. 10.1016/j.tig.2013.07.003, 23927865.
3. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, Evans T, Macrae CA, Stainier DY, Poss KD. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 2010, 464(7288):601-605. 10.1038/nature08804, 3040215, 20336144.
4. Jopling C, Sleep E, Raya M, Marti M, Raya A, Izpisua Belmonte JC. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464(7288):606-609. 10.1038/nature08899, 2846535, 20336145.
5. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, et al. Heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation 2014, 129(3):e28-e292. 10.1161/01.cir.0000441139.02102.80, 24352519.
6. Laflamme MA, Murry CE. Heart regeneration. Nature 2011, 473(7347):326-335. 10.1038/nature10147, 4091722, 21593865.
7. Rosenzweig A. Medicine. Cardiac regeneration. Science 2012, 338(6114):1549-1550. 10.1126/science.1228951, 23258880.
8. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assuncao JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013, 496(7446):498-503. 10.1038/nature12111, 3703927, 23594743.
9. Lawson ND, Wolfe SA. Forward and reverse genetic approaches for the analysis of vertebrate development in the zebrafish. Dev Cell 2011, 21(1):48-64. 10.1016/j.devcel.2011.06.007, 21763608.
10. Skromne I, Prince VE. Current perspectives in zebrafish reverse genetics: moving forward. Dev Dyn 2008, 237(4):861-882. 10.1002/dvdy.21484, 18330930.
11. Chen JN, Haffter P, Odenthal J, Vogelsang E, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Nusslein-Volhard C. Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development 1996, 123:293-302.
12. Stainier DY, Fouquet B, Chen JN, Warren KS, Weinstein BM, Meiler SE, Mohideen MA, Neuhauss SC, Solnica-Krezel L, Schier AF, Zwartkruis F, Stemple DL, Malicki J, Driever W, Fishman MC. Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development 1996, 123:285-292.
13. Huang CJ, Jou TS, Ho YL, Lee WH, Jeng YT, Hsieh FJ, Tsai HJ. Conditional expression of a myocardium-specific transgene in zebrafish transgenic lines. Dev Dyn 2005, 233(4):1294-1303. 10.1002/dvdy.20485, 15977161.
14. Davison JM, Akitake CM, Goll MG, Rhee JM, Gosse N, Baier H, Halpern ME, Leach SD, Parsons MJ. Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Dev Biol 2007, 304(2):811-824. 10.1016/j.ydbio.2007.01.033, 3470427, 17335798.
15. Knopf F, Schnabel K, Haase C, Pfeifer K, Anastassiadis K, Weidinger G. Dually inducible TetON systems for tissue-specific conditional gene expression in zebrafish. Proc Natl Acad Sci U S A 2010, 107(46):19933-19938. 10.1073/pnas.1007799107, 2993373, 21041642.
16. Vogel B, Meder B, Just S, Laufer C, Berger I, Weber S, Katus HA, Rottbauer W. In-vivo characterization of human dilated cardiomyopathy genes in zebrafish. Biochem Biophys Res Commun 2009, 390(3):516-522. 10.1016/j.bbrc.2009.09.129, 19800866.
17. Pelster B, Burggren WW. Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (Danio rerio). Circ Res 1996, 79(2):358-362. 10.1161/01.RES.79.2.358, 8756015.
18. Zon LI, Peterson RT. In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 2005, 4(1):35-44. 10.1038/nrd1606, 15688071.
19. Kikuchi K, Poss KD. Cardiac regenerative capacity and mechanisms. Annu Rev Cell Dev Biol 2012, 28:719-741. 10.1146/annurev-cellbio-101011-155739, 3586268, 23057748.
20. Lien CL, Harrison MR, Tuan TL, Starnes VA. Heart repair and regeneration: recent insights from zebrafish studies. Wound Repair Regen 2012, 20(5):638-646. 10.1111/j.1524-475X.2012.00814.x, 3445789, 22818295.
21. Poss KD, Wilson LG, Keating MT. Heart regeneration in zebrafish. Science 2002, 298(5601):2188-2190. 10.1126/science.1077857, 12481136.
22. van den Bos EJ, Mees BM, de Waard MC, de Crom R, Duncker DJ. A novel model of cryoinjury-induced myocardial infarction in the mouse: a comparison with coronary artery ligation. Am J Physiol Heart Circ Physiol 2005, 289(3):H1291-H1300. 10.1152/ajpheart.00111.2005, 15863462.
23. Gonzalez-Rosa JM, Martin V, Peralta M, Torres M, Mercader N. Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 2011, 138(9):1663-1674. 10.1242/dev.060897, 21429987.
24. Gonzalez-Rosa JM, Mercader N. Cryoinjury as a myocardial infarction model for the study of cardiac regeneration in the zebrafish. Nat Protoc 2012, 7(4):782-788. 10.1038/nprot.2012.025, 22461067.
25. Schnabel K, Wu CC, Kurth T, Weidinger G. Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PLoS One 2011, 6(4):e18503. 10.1371/journal.pone.0018503, 3075262, 21533269.
26. Chablais F, Veit J, Rainer G, Jazwinska A. The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Dev Biol 2011, 11:21. 10.1186/1471-213X-11-21, 3078894, 21473762.
27. Chablais F, Jazwinska A. Induction of myocardial infarction in adult zebrafish using cryoinjury. J Vis Exp 2012, (62):3666. doi:10.3791/3666.
28. Wang J, Panakova D, Kikuchi K, Holdway JE, Gemberling M, Burris JS, Singh SP, Dickson AL, Lin YF, Sabeh MK, Werdich AA, Yelon D, Macrae CA, Poss KD. The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 2011, 138(16):3421-3430. 10.1242/dev.068601, 3143562, 21752928.
29. Sleep E, Boue S, Jopling C, Raya M, Raya A, Izpisua Belmonte JC. Transcriptomics approach to investigate zebrafish heart regeneration. J Cardiovasc Med (Hagerstown) 2010, 11(5):369-380. 10.2459/JCM.0b013e3283375900, 20179605.
30. Fang Y, Gupta V, Karra R, Holdway JE, Kikuchi K, Poss KD. Translational profiling of cardiomyocytes identifies an early Jak1/Stat3 injury response required for zebrafish heart regeneration. Proc Natl Acad Sci U S A 2013, 110(33):13416-13421. 10.1073/pnas.1309810110, 3746860, 23901114.
31. Lien CL, Schebesta M, Makino S, Weber GJ, Keating MT. Gene expression analysis of zebrafish heart regeneration. PLoS Biol 2006, 4(8):e260. 10.1371/journal.pbio.0040260, 1523227, 16869712.
32. Kikuchi K, Holdway JE, Major RJ, Blum N, Dahn RD, Begemann G, Poss KD. Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev Cell 2011, 20(3):397-404. 10.1016/j.devcel.2011.01.010, 3071981, 21397850.
33. Kim J, Wu Q, Zhang Y, Wiens KM, Huang Y, Rubin N, Shimada H, Handin RI, Chao MY, Tuan TL, Starnes VA, Lien CL. PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc Natl Acad Sci U S A 2010, 107(40):17206-17210. 10.1073/pnas.0915016107, 2951463, 20858732.
34. Choi WY, Gemberling M, Wang J, Holdway JE, Shen MC, Karlstrom RO, Poss KD. In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development 2013, 140(3):660-666. 10.1242/dev.088526, 3561784, 23293297.
35. Chablais F, Jazwinska A. The regenerative capacity of the zebrafish heart is dependent on TGFbeta signaling. Development 2012, 139(11):1921-1930. 10.1242/dev.078543, 22513374.
36. Zhao L, Borikova AL, Ben-Yair R, Guner-Ataman B, MacRae CA, Lee RT, Burns CG, Burns CE. Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc Natl Acad Sci U S A 2014, 111(4):1403-1408. 10.1073/pnas.1311705111, 3910613, 24474765.
37. Nepusz T, Yu H, Paccanaro A. Detecting overlapping protein complexes in protein-protein interaction networks. Nat Methods 2012, 9(5):471-472. 10.1038/nmeth.1938, 3543700, 22426491.
38. Nepomuceno-Chamorro IA, Aguilar-Ruiz JS, Riquelme JC. Inferring gene regression networks with model trees. BMC Bioinformatics 2010, 11:517. 10.1186/1471-2105-11-517, 2978221, 20950452.
39. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008, 9:559. 10.1186/1471-2105-9-559, 2631488, 19114008.
40. Kizil C, Otto GW, Geisler R, Nusslein-Volhard C, Antos CL. Simple controls cell proliferation and gene transcription during zebrafish caudal fin regeneration. Dev Biol 2009, 325(2):329-340. 10.1016/j.ydbio.2008.09.032, 19014929.
41. Conway SJ, Molkentin JD. Periostin as a heterofunctional regulator of cardiac development and disease. Curr Genomics 2008, 9(8):548-555. 10.2174/138920208786847917, 2694556, 19516962.
42. Snider P, Standley KN, Wang J, Azhar M, Doetschman T, Conway SJ. Origin of cardiac fibroblasts and the role of periostin. Circ Res 2009, 105(10):934-947. 10.1161/CIRCRESAHA.109.201400, 2786053, 19893021.
43. Oka T, Xu J, Kaiser RA, Melendez J, Hambleton M, Sargent MA, Lorts A, Brunskill EW, Dorn GW, Conway SJ, Aronow BJ, Robbins J, Molkentin JD. Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res 2007, 101(3):313-321. 10.1161/CIRCRESAHA.107.149047, 2680305, 17569887.
44. Shimazaki M, Nakamura K, Kii I, Kashima T, Amizuka N, Li M, Saito M, Fukuda K, Nishiyama T, Kitajima S, Saga Y, Fukayama M, Sata M, Kudo A. Periostin is essential for cardiac healing after acute myocardial infarction. J Exp Med 2008, 205(2):295-303. 10.1084/jem.20071297, 2271007, 18208976.
45. Kuhn B, del Monte F, Hajjar RJ, Chang YS, Lebeche D, Arab S, Keating MT. Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair. Nat Med 2007, 13(8):962-969. 10.1038/nm1619, 17632525.
46. Gonzalez-Rosa JM, Peralta M, Mercader N. Pan-epicardial lineage tracing reveals that epicardium derived cells give rise to myofibroblasts and perivascular cells during zebrafish heart regeneration. Dev Biol 2012, 370(2):173-186. 10.1016/j.ydbio.2012.07.007, 22877945.
47. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J 1995, 9(9):726-735.
48. Stevenson LF, Sparks A, Allende-Vega N, Xirodimas DP, Lane DP, Saville MK. The deubiquitinating enzyme USP2a regulates the p53 pathway by targeting Mdm2. EMBO J 2007, 26(4):976-986. 10.1038/sj.emboj.7601567, 1852834, 17290220.
49. Wong AK, Park CY, Greene CS, Bongo LA, Guan Y, Troyanskaya OG. IMP: a multi-species functional genomics portal for integration, visualization and prediction of protein functions and networks. Nucleic Acids Res 2012, 40(Web Server issue):W484-W490. 3394282, 22684505.
50. Van Vliet P, Wu SM, Zaffran S, Puceat M. Early cardiac development: a view from stem cells to embryos. Cardiovasc Res 2012, 96(3):352-362. 10.1093/cvr/cvs270, 3500045, 22893679.
51. Takeuchi JK, Bruneau BG. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009, 459(7247):708-711. 10.1038/nature08039, 2728356, 19396158.
52. Alsan BH, Schultheiss TM. Regulation of avian cardiogenesis by Fgf8 signaling. Development 2002, 129(8):1935-1943.
53. Holtzinger A, Rosenfeld GE, Evans T. Gata4 directs development of cardiac-inducing endoderm from ES cells. Dev Biol 2010, 337(1):63-73. 10.1016/j.ydbio.2009.10.003, 2799892, 19850025.
54. Rouleau M, Medawar A, Hamon L, Shivtiel S, Wolchinsky Z, Zhou H, De Rosa L, Candi E, de la Forest DS, Mikkola ML, van Bokhoven H, Missero C, Melino G, Puceat M, Aberdam D. TAp63 is important for cardiac differentiation of embryonic stem cells and heart development. Stem Cells 2011, 29(11):1672-1683. 10.1002/stem.723, 21898690.
55. Frangogiannis NG. Matricellular proteins in cardiac adaptation and disease. Physiol Rev 2012, 92(2):635-688. 10.1152/physrev.00008.2011, 22535894.
56. Lu B, Yu H, Zwartbol M, Ruifrok WP, van Gilst WH, de Boer RA, Sillje HH. Identification of hypertrophy- and heart failure-associated genes by combining in vitro and in vivo models. Physiol Genomics 2012, 44(8):443-454. 10.1152/physiolgenomics.00148.2011, 22353257.
57. Kyritsis N, Kizil C, Zocher S, Kroehne V, Kaslin J, Freudenreich D, Iltzsche A, Brand M. Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 2012, 338(6112):1353-1356. 10.1126/science.1228773, 23138980.
58. Hsueh YC, Wu JM, Yu CK, Wu KK, Hsieh PC. Prostaglandin E(2) promotes post-infarction cardiomyocyte replenishment by endogenous stem cells. EMBO Mol Med 2014, 6(4):496-503. 3992076, 24448489.
59. Alvarez BV, Quon AL, Mullen J, Casey JR. Quantification of carbonic anhydrase gene expression in ventricle of hypertrophic and failing human heart. BMC Cardiovasc Disord 2013, 13:2. 10.1186/1471-2261-13-2, 3570296, 23297731.
60. Nowak KJ, Wattanasirichaigoon D, Goebel HH, Wilce M, Pelin K, Donner K, Jacob RL, Hubner C, Oexle K, Anderson JR, Verity CM, North KN, Iannaccone ST, Muller CR, Nurnberg P, Muntoni F, Sewry C, Hughes I, Sutphen R, Lacson AG, Swoboda KJ, Vigneron J, Wallgren-Pettersson C, Beggs AH, Laing NG. Mutations in the skeletal muscle alpha-actin gene in patients with actin myopathy and nemaline myopathy. Nat Genet 1999, 23(2):208-212. 10.1038/13837, 10508519.
61. Feng JJ, Marston S. Genotype-phenotype correlations in ACTA1 mutations that cause congenital myopathies. Neuromuscul Disord 2009, 19(1):6-16. 10.1016/j.nmd.2008.09.005, 18976909.
62. D'Amico A, Graziano C, Pacileo G, Petrini S, Nowak KJ, Boldrini R, Jacques A, Feng JJ, Porfirio B, Sewry CA, Santorelli FM, Limongelli G, Bertini E, Laing N, Marston SB. Fatal hypertrophic cardiomyopathy and nemaline myopathy associated with ACTA1 K336E mutation. Neuromuscul Disord 2006, 16(9-10):548-552.
63. Kim SY, Park YE, Kim HS, Lee CH, Yang DH, Kim DS. Nemaline myopathy and non-fatal hypertrophic cardiomyopathy caused by a novel ACTA1 E239K mutation. J Neurol Sci 2011, 307(1-2):171-173.
64. Gatayama R, Ueno K, Nakamura H, Yanagi S, Ueda H, Yamagishi H, Yasui S. Nemaline myopathy with dilated cardiomyopathy in childhood. Pediatrics 2013, 131(6):e1986-e1990. 10.1542/peds.2012-1139, 23650303.
65. Lim DS, Roberts R, Marian AJ. Expression profiling of cardiac genes in human hypertrophic cardiomyopathy: insight into the pathogenesis of phenotypes. J Am Coll Cardiol 2001, 38(4):1175-1180. 10.1016/S0735-1097(01)01509-1, 2776821, 11583900.
66. Lancioni A, Rotundo IL, Kobayashi YM, D'Orsi L, Aurino S, Nigro G, Piluso G, Acampora D, Cacciottolo M, Campbell KP, Nigro V. Combined deficiency of alpha and epsilon sarcoglycan disrupts the cardiac dystrophin complex. Hum Mol Genet 2011, 20(23):4644-4654. 10.1093/hmg/ddr398, 3209833, 21890494.
67. Priolo C, Tang D, Brahamandan M, Benassi B, Sicinska E, Ogino S, Farsetti A, Porrello A, Finn S, Zimmermann J, Febbo P, Loda M. The isopeptidase USP2a protects human prostate cancer from apoptosis. Cancer Res 2006, 66(17):8625-8632. 10.1158/0008-5472.CAN-06-1374, 16951176.
68. Liu Z, Zanata SM, Kim J, Peterson MA, Di Vizio D, Chirieac LR, Pyne S, Agostini M, Freeman MR, Loda M. The ubiquitin-specific protease USP2a prevents endocytosis-mediated EGFR degradation. Oncogene 2013, 32(13):1660-1669. 10.1038/onc.2012.188, 3866888, 22710717.
69. Yun MH, Gates PB, Brockes JP. Regulation of p53 is critical for vertebrate limb regeneration. Proc Natl Acad Sci U S A 2013, 110(43):17392-17397. 10.1073/pnas.1310519110, 3808590, 24101460.
70. Lepilina A, Coon AN, Kikuchi K, Holdway JE, Roberts RW, Burns CG, Poss KD. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 2006, 127(3):607-619. 10.1016/j.cell.2006.08.052, 17081981.
71. BLAST: Basic Local Alignment Search Tool 2012, Available from: http://www.ncbi.nlm.nih.gov/BLAST/Blast.cgi.
72. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009, 55(4):611-622. 10.1373/clinchem.2008.112797, 19246619.
73. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article 3.
74. Nazarov PV, Reinsbach SE, Muller A, Nicot N, Philippidou D, Vallar L, Kreis S. Interplay of microRNAs, transcription factors and target genes: linking dynamic expression changes to function. Nucleic Acids Res 2013, 41(5):2817-2831. 10.1093/nar/gks1471, 3597666, 23335783.
75. Gillespie CS, Lei G, Boys RJ, Greenall A, Wilkinson DJ. Analysing time course microarray data using Bioconductor: a case study using yeast2 Affymetrix arrays. BMC Res Notes 2010, 3:81. 10.1186/1756-0500-3-81, 2880961, 20302631.
76. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13(11):2498-2504. 10.1101/gr.1239303, 403769, 14597658.
77. Malerba D, Esposito F, Ceci M, Appice A. Top-down induction of model trees with regression and splitting nodes. IEEE Trans Pattern Anal Mach Intell 2004, 26(5):612-625. 10.1109/TPAMI.2004.1273937, 15460282.