Transcriptome landscape of the human placenta

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Kim, Jinsil ^a   Zhao, Keyan ^a   Jiang, Peng ^a   Lu, Zhi xiang ^a   Wang, Jinkai ^a   Murray, Jeffrey C ^a,b   Xing, Yi ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c IA United States   (United States)

Author keywords

Alternative splicing; Amnion; Chorion; Decidua; Functional interaction network; Novel transcriptional active region; Placenta; Rna seq; Transcriptome

Indexed keywords

TRANSCRIPTOME; ESRP1 PROTEIN, HUMAN; RNA BINDING PROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; EPITHELIAL SPECIFIC SPLICING FACTOR 1 GENE; EXON SKIPPING; FEMALE; GENE; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN TISSUE; INFANT; MALE; PATHOGENESIS; PLACENTA DEVELOPMENT; PLACENTA FUNCTION; PREGNANCY DISORDER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TISSUE DISTRIBUTION; TRANSCRIPTOMICS; AMNION; ANTIBODY SPECIFICITY; CHORION; DECIDUA; EXON; GENETICS; METABOLISM; PLACENTA; PREGNANCY; PREGNANCY COMPLICATION; RNA SPLICING;

AMNION; CHORION; DECIDUA; EXONS; FEMALE; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; ORGAN SPECIFICITY; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; RNA SPLICING; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, RNA;

EID: 84862830326     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-115     Document Type: Article

References (82)

1. Kay HH, Nelson DM, Wang Y. The placenta: from development to disease. 2011, Chichester, West Sussex: Wiley-Blackwell.
2. Roberts DJ, Post MD. The placenta in pre-eclampsia and intrauterine growth restriction. J Clin Pathol 2008, 61(12):1254-1260. 10.1136/jcp.2008.055236, 18641412.
3. Faye-Petersen OM. The placenta in preterm birth. Journal of Clinical Pathology 2008, 61(12):1261-1275. 10.1136/jcp.2008.055244, 19074631.
4. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet 2008, 371(9606):75-84. 10.1016/S0140-6736(08)60074-4, 18177778.
5. Martin JA, Hamilton BE, Ventura SJ, Osterman MJ, Kirmeyer S, Mathews TJ, Wilson E. Births: final data for 2009. Natl Vital Stat Rep 2011, 60(1):1-104.
6. Mikheev AM, Nabekura T, Kaddoumi A, Bammler TK, Govindarajan R, Hebert MF, Unadkat JD. Profiling gene expression in human placentae of different gestational ages: an OPRU Network and UW SCOR Study. Reprod Sci 2008, 15(9):866-877. 10.1177/1933719108322425, 2702165, 19050320.
7. Haddad R, Tromp G, Kuivaniemi H, Chaiworapongsa T, Kim YM, Mazor M, Romero R. Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. American journal of obstetrics and gynecology 2006, 195(2):394-405. 10.1016/j.ajog.2005.08.057, 1800883, 16890549.
8. Sitras V, Paulssen RH, Gronaas H, Vartun A, Acharya G. Gene expression profile in labouring and non-labouring human placenta near term. Molecular Human Reproduction 2008, 14(1):61-65. 10.1093/molehr/gam083, 18048457.
9. Sitras V, Paulssen RH, Gronaas H, Leirvik J, Hanssen TA, Vartun A, Acharya G. Differential Placental Gene Expression in Severe Preeclampsia. Placenta 2009, 30(5):424-433. 10.1016/j.placenta.2009.01.012, 19249095.
10. Sood R, Zehnder JL, Druzin ML, Brown PO. Gene expression patterns in human placenta. Proc Natl Acad Sci USA 2006, 103(14):5478-5483. 10.1073/pnas.0508035103, 1414632, 16567644.
11. Knox K, Baker JC. Genomic evolution of the placenta using co-option and duplication and divergence. Genome Res 2008, 18(5):695-705. 10.1101/gr.071407.107, 2336813, 18340042.
12. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 2008, 40(12):1413-1415. 10.1038/ng.259, 18978789.
13. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456(7221):470-476. 10.1038/nature07509, 2593745, 18978772.
14. Chen M, Manley JL. Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nature Reviews Molecular Cell Biology 2009, 10(11):741. 2958924, 19773805.
15. Wang GS, Cooper TA. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet 2007, 8(10):749-761. 10.1038/nrg2164, 17726481.
16. Caceres JF, Kornblihtt AR. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet 2002, 18(4):186-193. 10.1016/S0168-9525(01)02626-9, 11932019.
17. Soleymanlou N, Wu Y, Wang JX, Todros T, Ietta F, Jurisicova A, Post M, Caniggia I. A novel Mtd splice isoform is responsible for trophoblast cell death in pre-eclampsia. Cell Death Differ 2005, 12(5):441-452. 10.1038/sj.cdd.4401593, 15775999.
18. Sela S, Itin A, Natanson-Yaron S, Greenfield C, Goldman-Wohl D, Yagel S, Keshet E. A novel human-specific soluble vascular endothelial growth factor receptor 1: cell-type-specific splicing and implications to vascular endothelial growth factor homeostasis and preeclampsia. Circ Res 2008, 102(12):1566-1574. 10.1161/CIRCRESAHA.108.171504, 18515749.
19. Heydarian M, McCaffrey T, Florea L, Yang Z, Ross MM, Zhou W, Maynard SE. Novel splice variants of sFlt1 are upregulated in preeclampsia. Placenta 2009, 30(3):250-255. 10.1016/j.placenta.2008.12.010, 19147226.
20. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009, 10(1):57-63. 10.1038/nrg2484, 2949280, 19015660.
21. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 2010, 28(5):511-515. 10.1038/nbt.1621, 3146043, 20436464.
22. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5(7):621-628. 10.1038/nmeth.1226, 18516045.
23. 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. Proc Natl Acad Sci USA 2004, 101(16):6062-6067. 10.1073/pnas.0400782101, 395923, 15075390.
24. Blake JA, Bult CJ, Kadin JA, Richardson JE, Eppig JT. The Mouse Genome Database (MGD): premier model organism resource for mammalian genomics and genetics. Nucleic Acids Res 2011, (39 Database):D842-848.
25. The Mouse Genome Informatics database. , http://www.informatics.jax.org/
26. Dolan SM, Hollegaard MV, Merialdi M, Betran AP, Allen T, Abelow C, Nace J, Lin BK, Khoury MJ, Ioannidis JP, et al. Synopsis of preterm birth genetic association studies: the preterm birth genetics knowledge base (PTBGene). Public Health Genomics 2010, 13(7-8):514-523. 10.1159/000294202, 20484876.
27. The Preterm Birth Genetics Knowledge Base. , http://bioinformatics.aecom.yu.edu/ptbgene/index.html
28. 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(5):P3. 10.1186/gb-2003-4-5-p3, 12734009.
29. The Database for Annotation, Visualization and Integrated Discovery. , http://david.abcc.ncifcrf.gov/
30. Benirschke K. Pathology of the human placenta 2012, New York: Springer.
31. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A. PANTHER: a library of protein families and subfamilies indexed by function. Genome Research 2003, 13(9):2129-2141. 10.1101/gr.772403, 403709, 12952881.
32. Thomas PD, Kejariwal A, Guo N, Mi H, Campbell MJ, Muruganujan A, Lazareva-Ulitsky B. Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools. Nucleic Acids Research 2006, (34 Web Server):W645-650.
33. Lash GE, Warren AY, Underwood S, Baker PN. Vascular endothelial growth factor is a chemoattractant for trophoblast cells. Placenta 2003, 24(5):549-556. 10.1053/plac.2002.0923, 12744932.
34. Baker PN, Krasnow J, Roberts JM, Yeo KT. Elevated serum levels of vascular endothelial growth factor in patients with preeclampsia. Obstet Gynecol 1995, 86(5):815-821. 10.1016/0029-7844(95)00259-T, 7566855.
35. Akercan F, Cirpan T, Terek MC, Ozcakir HT, Giray G, Sagol S, Karadadas N. The immunohistochemical evaluation of VEGF in placenta biopsies of pregnancies complicated by preeclampsia. Arch Gynecol Obstet 2008, 277(2):109-114. 10.1007/s00404-007-0430-5, 17710429.
36. Cirpan T, Akercan F, Terek MC, Kazandi M, Ozcakir HT, Giray G, Sagol S. Evaluation of VEGF in placental bed biopsies from preeclamptic women by immunohistochemistry. Clin Exp Obstet Gynecol 2007, 34(4):228-231.
37. Farina A, Sekizawa A, De Sanctis P, Purwosunu Y, Okai T, Cha DH, Kang JH, Vicenzi C, Tempesta A, Wibowo N, et al. Gene expression in chorionic villous samples at 11 weeks' gestation from women destined to develop preeclampsia. Prenat Diagn 2008, 28(10):956-961. 10.1002/pd.2109, 18792924.
38. Farina A, Zucchini C, Sekizawa A, Purwosunu Y, de Sanctis P, Santarsiero G, Rizzo N, Morano D, Okai T. Performance of messenger RNAs circulating in maternal blood in the prediction of preeclampsia at 10-14 weeks. American journal of obstetrics and gynecology 2010, 203(6):575. e571-577.
39. Semczuk-Sikora A, Krzyzanowski A, Kwiatek M, Semczuk M. [Maternal serum concentration of placental growth factor (PIGF) and endothelial growth factor (VEGF) in pregnancies complicated by preeclampsia]. Ginekol Pol 2007, 78(11):873-876.
40. Sandman CA, Glynn L, Schetter CD, Wadhwa P, Garite T, Chicz-DeMet A, Hobel C. Elevated maternal cortisol early in pregnancy predicts third trimester levels of placental corticotropin releasing hormone (CRH): priming the placental clock. Peptides 2006, 27(6):1457-1463. 10.1016/j.peptides.2005.10.002, 16309788.
41. Vitoratos N, Papadias K, Makrakis E, Christodoulakos G, Panoulis K, Creatsas G. Association between serum tumor necrosis factor-alpha and corticotrophin-releasing hormone levels in women with preterm labor. J Obstet Gynaecol Res 2006, 32(5):497-501. 10.1111/j.1447-0756.2006.00441.x, 16984517.
42. Grosso AR, Gomes AQ, Barbosa-Morais NL, Caldeira S, Thorne NP, Grech G, von Lindern M, Carmo-Fonseca M. Tissue-specific splicing factor gene expression signatures. Nucleic Acids Res 2008, 36(15):4823-4832. 10.1093/nar/gkn463, 2528195, 18653532.
43. Yeo GW, Coufal NG, Liang TY, Peng GE, Fu X-D, Gage FH. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol 2009, 16(2):130. 10.1038/nsmb.1545, 2735254, 19136955.
44. Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol Cell 2009, 33(5):591-601. 10.1016/j.molcel.2009.01.025, 2702247, 19285943.
45. de la Grange P, Gratadou L, Delord M, Dutertre M, Auboeuf D. Splicing factor and exon profiling across human tissues. Nucleic Acids Res 2010, 38(9):2825-2838. 10.1093/nar/gkq008, 2875023, 20110256.
46. Warzecha CC, Jiang P, Amirikian K, Dittmar KA, Lu H, Shen S, Guo W, Xing Y, Carstens RP. An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition. EMBO J 2010, 29(19):3286-3300. 10.1038/emboj.2010.195, 2957203, 20711167.
47. Bland CS, Wang ET, Vu A, David MP, Castle JC, Johnson JM, Burge CB, Cooper TA. Global regulation of alternative splicing during myogenic differentiation. Nucleic Acids Res 2010, 38(21):7651-7664. 10.1093/nar/gkq614, 2995044, 20634200.
48. Shen S, Won Park J, Huang J, Dittmar KA, Lu ZX, Zhou Q, Carstens RP, Xing Y. MATS: a Bayesian framework for flexible detection of differential alternative splicing from RNA-Seq data. Nucleic Acids Res 2012, doi:10.1093/nar/gkr1291.
49. Tamura RN, Cooper HM, Collo G, Quaranta V. Cell type-specific integrin variants with alternative alpha chain cytoplasmic domains. Proc Natl Acad Sci USA 1991, 88(22):10183-10187. 10.1073/pnas.88.22.10183, 52892, 1946438.
50. Lee EC, Lotz MM, Steele GD, Mercurio AM. The integrin alpha 6 beta 4 is a laminin receptor. J Cell Biol 1992, 117(3):671-678. 10.1083/jcb.117.3.671, 2289449, 1533398.
51. Heinemann T, Bulwin GC, Randall J, Schnieders B, Sandhoff K, Volk HD, Milford E, Gullans SR, Utku N. Genomic organization of the gene coding for TIRC7, a novel membrane protein essential for T cell activation. Genomics 1999, 57(3):398-406. 10.1006/geno.1999.5751, 10329006.
52. Smirnova AS, Morgun A, Shulzhenko N, Silva ID, Gerbase-DeLima M. Identification of new alternative splice events in the TCIRG1 gene in different human tissues. Biochem Biophys Res Commun 2005, 330(3):943-949. 10.1016/j.bbrc.2005.03.065, 15809087.
53. Hu Y, Leo C, Yu S, Huang BC, Wang H, Shen M, Luo Y, Daniel-Issakani S, Payan DG, Xu X. Identification and functional characterization of a novel human misshapen/Nck interacting kinase-related kinase, hMINK beta. The Journal of biological chemistry 2004, 279(52):54387-54397. 10.1074/jbc.M404497200, 15469942.
54. Wu G, Feng X, Stein L. A human functional protein interaction network and its application to cancer data analysis. Genome Biology 2010, 11(5):R53-R53. 10.1186/gb-2010-11-5-r53, 2898064, 20482850.
55. Girvan M, Newman ME. Community structure in social and biological networks. Proc Natl Acad Sci USA 2002, 99(12):7821-7826. 10.1073/pnas.122653799, 122977, 12060727.
56. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010, 28(5):503-510. 10.1038/nbt.1633, 2868100, 20436462.
57. Salomonis N, Nelson B, Vranizan K, Pico AR, Hanspers K, Kuchinsky A, Ta L, Mercola M, Conklin BR. Alternative splicing in the differentiation of human embryonic stem cells into cardiac precursors. PLoS Comput Biol 2009, 5(11):e1000553. 10.1371/journal.pcbi.1000553, 2764345, 19893621.
58. Yeo GW, Xu X, Liang TY, Muotri AR, Carson CT, Coufal NG, Gage FH. Alternative splicing events identified in human embryonic stem cells and neural progenitors. PLoS Comput Biol 2007, 3(10):1951-1967. 2041973, 17967047.
59. Delorme MA, Burrows RF, Ofosu FA, Andrew M. Thrombin regulation in mother and fetus during pregnancy. Semin Thromb Hemost 1992, 18(1):81-90. 10.1055/s-2007-1002413, 1574718.
60. Jabbour HN, Critchley HO. Potential roles of decidual prolactin in early pregnancy. Reproduction 2001, 121(2):197-205. 10.1530/rep.0.1210197, 11226044.
61. Randhawa RS. The insulin-like growth factor system and fetal growth restrictionn. Pediatr Endocrinol Rev 2008, 6(2):235-240.
62. Coan PM, Fowden AL, Constancia M, Ferguson-Smith AC, Burton GJ, Sibley CP. Disproportional effects of Igf2 knockout on placental morphology and diffusional exchange characteristics in the mouse. J Physiol 2008, 586(Pt 20):5023-5032. 2614051, 18755750.
63. Prager S, Wollmann HA, Mergenthaler S, Mavany M, Eggermann K, Ranke MB, Eggermann T. Characterization of genomic variants in CSH1 and GH2, two candidate genes for Silver-Russell syndrome in 17q24-q25. Genet Test 2003, 7(3):259-263. 10.1089/109065703322537304, 14642004.
64. Rull K, Laan M. Expression of beta-subunit of HCG genes during normal and failed pregnancy. Hum Reprod 2005, 20(12):3360-3368. 10.1093/humrep/dei261, 1403819, 16123088.
65. Henderson DJ, Bennett PR, Moore GE. Expression of human chorionic gonadotrophin alpha and beta subunits is depressed in trophoblast from pregnancies with early embryonic failure. Hum Reprod 1992, 7(10):1474-1478.
66. Hunt JS, Langat DK, McIntire RH, Morales PJ. The role of HLA-G in human pregnancy. Reprod Biol Endocrinol 2006, (4 Suppl 1):S10.
67. Hunt JS, Petroff MG, McIntire RH, Ober C. HLA-G and immune tolerance in pregnancy. FASEB J 2005, 19(7):681-693. 10.1096/fj.04-2078rev, 15857883.
68. Izumi-Yoneda N, Toda A, Okabe M, Koike C, Takashima S, Yoshida T, Konishi I, Saito S, Nikaido T. Alpha 1 antitrypsin activity is decreased in human amnion in premature rupture of the fetal membranes. Mol Hum Reprod 2009, 15(1):49-57. 10.1093/molehr/gan071, 19073710.
69. Niknejad H, Peirovi H, Jorjani M, Ahmadiani A, Ghanavi J, Seifalian AM. Properties of the amniotic membrane for potential use in tissue engineering. Eur Cell Mater 2008, 15:88-99.
70. Burrows TD, King A, Loke YW. Trophoblast migration during human placental implantation. Hum Reprod Update 1996, 2(4):307-321. 10.1093/humupd/2.4.307, 9080228.
71. Massague J. How cells read TGF-beta signals. Nat Rev Mol Cell Biol 2000, 1(3):169-178.
72. Fryer BH, Simon MC. Hypoxia, HIF and the placenta. Cell Cycle 2006, 5(5):495-498. 10.4161/cc.5.5.2497, 16552177.
73. Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 2004, 131(7):1619-1628. 10.1242/dev.01037, 14998921.
74. Harkness ML, Harkness RD. The growth of collagen in the foetus, placenta and foetal membranes of the rat. J Physiol 1955, 128(2):225-234. 1365853, 14392603.
75. Shen S, Lin L, Cai JJ, Jiang P, Kenkel EJ, Stroik MR, Sato S, Davidson BL, Xing Y. Widespread establishment and regulatory impact of Alu exons in human genes. Proc Natl Acad Sci USA 2011, 108(7):2837-2842. 10.1073/pnas.1012834108, 3041063, 21282640.
76. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
77. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
78. Lu ZX, Jiang P, Cai JJ, Xing Y. Context-dependent robustness to 5' splice site polymorphisms in human populations. Hum Mol Genet 2011, 20(6):1084-1096. 10.1093/hmg/ddq553, 3043661, 21224255.
79. Schuelke M. An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 2000, 18(2):233-234. 10.1038/72708, 10657137.
80. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262, 11846609.
81. Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2010, 27(3):431-432. 3031041, 21149340.
82. Yoon J, Blumer A, Lee K. An algorithm for modularity analysis of directed and weighted biological networks based on edge-betweenness centrality. Bioinformatics 2006, 22(24):3106-3108. 10.1093/bioinformatics/btl533, 17060356.