Unique transcriptomic landscapes identified in idiopathic spontaneous and infection related preterm births compared to normal term births

English version

Autoři: Heather M. Brockway ^aff001; Suhas G. Kallapur ^aff002; Irina A. Buhimschi ^aff003; Catalin S. Buhimschi ^aff003; William E. Ackerman ^aff003; Louis J. Muglia ^aff001; Helen N. Jones ^aff004
Působiště autorů: Center for Preterm Birth, Cincinnati Children’s Hospital Medical Center and Department of Pediatrics University of Cincinnati College of Medicine, Cincinnati, Ohio, United States of America ^aff001; Divisions of Neonatology and Developmental Biology, David Geffen School of Medicine at the University of California, Los Angeles, California, United States of America ^aff002; Department of Obstetrics and Gynecology, The University of Illinois College of Medicine, Chicago, Illinios, United States of America ^aff003; Center for Fetal and Placental Research, Cincinnati Children’s Hospital Medical Center and Department of Surgery University of Cincinnati College of Medicine, Cincinnati, Ohio, United States of America ^aff004
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0225062

Souhrn

Preterm birth (PTB) is leading contributor to infant death in the United States and globally, yet the underlying mechanistic causes are not well understood. Histopathological studies of preterm birth suggest advanced villous maturity may have a role in idiopathic spontaneous preterm birth (isPTB). To better understand pathological and molecular basis of isPTB, we compared placental villous transcriptomes from carefully phenotyped cohorts of PTB due to infection or isPTB between 28–36 weeks gestation and healthy term placentas. Transcriptomic analyses revealed a unique expression signature for isPTB distinct from the age-matched controls that were delivered prematurely due to infection. This signature included the upregulation of three IGF binding proteins (IGFBP1, IGFBP2, and IGFBP6), supporting a role for aberrant IGF signaling in isPTB. However, within the isPTB expression signature, we detected secondary signature of inflammatory markers including TNC, C3, CFH, and C1R, which have been associated with placental maturity. In contrast, the expression signature of the gestational age-matched infected samples included upregulation of proliferative genes along with cell cycling and mitosis pathways. Together, these data suggest an isPTB molecular signature of placental hypermaturity, likely contributing to the premature activation of inflammatory pathways associated with birth and providing a molecular basis for idiopathic spontaneous birth.

Klíčová slova:

Placenta – Gene expression – Birth – Inflammation – Wnt signaling cascade – Transcriptome analysis – RNA sequencing – Preterm birth

Zdroje

1. Dimes M of. 2018 PREMATURE BIRTH REPORT CARD. In: 2018 PREMATURE BIRTH REPORT CARD [Internet]. Available: https://www.marchofdimes.org/mission/prematurity-reportcard-tv.aspx

2. Blencowe H, Cousens S, Chou D, Oestergaard M, Say L, Moller A-B, et al. Born Too Soon: The global epidemiology of 15 million preterm births. Reproductive Health. 2013;10: S2. doi: 10.1186/1742-4755-10-S1-S2 24625129

3. Monangi NK, Brockway HM, House M, Zhang G, Muglia LJ. The genetics of preterm birth: Progress and promise. Seminars in Perinatology. 2015;39: 574–583. doi: 10.1053/j.semperi.2015.09.005 26459968

4. Burton GJ, Fowden AL. The placenta: a multifaceted, transient organ. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2015;370: 20140066. doi: 10.1098/rstb.2014.0066 25602070

5. Maltepe E, Fisher SJ. PLACENTA: The Forgotten Organ. Annual Review of Cell and Developmental Biology. 2014;31: 1–30. doi: 10.1146/annurev-cellbio-100814-125620 26443191

6. Ilekis JV, Tsilou E, Fisher S, Abrahams VM, Soares MJ, Cross JC, et al. Placental origins of adverse pregnancy outcomes: potential molecular targets: an Executive Workshop Summary of the Eunice Kennedy Shriver National Institute of Child Health and Human Development. American Journal of Obstetrics and Gynecology. 2016;215: S1–S46. doi: 10.1016/j.ajog.2016.03.001 26972897

7. Khong YT, Mooney EE, Ariel I, Balmus NC, Boyd TK, Brundler M-A, et al. Sampling and Definitions of Placental Lesions: Amsterdam Placental Workshop Group Consensus Statement. Archives of Pathology & Laboratory Medicine. 2016;140: 698–713. doi: 10.5858/arpa.2015-0225-CC 27223167

8. Morgan TK. Role of the Placenta in Preterm Birth: A Review. American Journal of Perinatology. 2016;33: 258–266. doi: 10.1055/s-0035-1570379 26731184

9. Morgan TK, Tolosa JE, Mele L, Wapner RJ, Spong CY, Sorokin Y, et al. Placental villous hypermaturation is associated with idiopathic preterm birth. The Journal of Maternal-Fetal & Neonatal Medicine. 2012;26: 647–653. doi: 10.3109/14767058.2012.746297 23130816

10. Nijman TA, van Vliet EO, Benders MJ, Mol BW, Franx A, Nikkels PG, et al. Placental histology in spontaneous and indicated preterm birth: A case control study. Placenta. 2016;48: 56–62. doi: 10.1016/j.placenta.2016.10.006 27871473

11. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308

12. Forbes K, Westwood M. Maternal growth factor regulation of human placental development and fetal growth. Journal of Endocrinology. 2010;207: 1–16. doi: 10.1677/JOE-10-0174 20817666

13. Forbes BE, McCarthy P, Norton RS. Insulin-Like Growth Factor Binding Proteins: A Structural Perspective. Frontiers in Endocrinology. 2012;3: 38. doi: 10.3389/fendo.2012.00038 22654863

14. Bach L. 40 YEARS OF IGF1: IGF-binding proteins. Journal of Molecular Endocrinology. 2018;61: T11–T28. doi: 10.1530/JME-17-0254 29255001

15. Díaz P, Powell TL, Jansson T. The Role of Placental Nutrient Sensing in Maternal-Fetal Resource Allocation. Biology of Reproduction. 2014;91. doi: 10.1095/biolreprod.114.121798 25122064

16. Jansson N, Rosario FJ, Gaccioli F, Lager S, Jones HN, Roos S, et al. Activation of placental mTOR signaling and amino acid transporters in obese women giving birth to large babies. The Journal of clinical endocrinology and metabolism. 2012;98: 105–13. doi: 10.1210/jc.2012-2667 23150676

17. Chua C, Liu Y, Granberg K, Hu L, Haapasalo H, Annala M, et al. IGFBP2 potentiates nuclear EGFR–STAT3 signaling. Oncogene. 2016;35: 738. doi: 10.1038/onc.2015.131 25893308

18. Iosef C, Vilk G, Gkourasas T, Lee K-J, Chen B, Fu P, et al. Insulin-like growth factor binding protein-6 (IGFBP-6) interacts with DNA-end binding protein Ku80 to regulate cell fate. Cellular Signalling. 2010;22: 1033–1043. doi: 10.1016/j.cellsig.2010.02.006 20188166

19. Ma B, Hottiger MO. Crosstalk between Wnt/β-Catenin and NF-κB Signaling Pathway during Inflammation. Frontiers in Immunology. 2016;7: 378. doi: 10.3389/fimmu.2016.00378 27713747

20. Yu LJ, Wang B, Parobchak N, Roche N, Rosen T. STAT3 cooperates with the non-canonical NF-κB signaling to regulate pro-labor genes in the human placenta. Placenta. 2015;36: 581–586. doi: 10.1016/j.placenta.2015.02.013 25771405

21. Muller C, Paupert J, Monferran S, Cycle SB. The double life of the Ku protein: facing the DNA breaks and the extracellular environment. 2005; doi: 10.4161/cc.4.3.1565 15738653

22. Zhang J, Rane G, Dai X, Shanmugam MK, Arfuso F, Samy R, et al. Ageing and the telomere connection: An intimate relationship with inflammation. Ageing Research Reviews. 2016;25: 55–69. doi: 10.1016/j.arr.2015.11.006 26616852

23. Allsopp R, Shimoda J, Easa D, Ward K. Long Telomeres in the Mature Human Placenta. Placenta. 2007;28: 324–327. doi: 10.1016/j.placenta.2006.04.003 16806460

24. Phillippe M. Cell-Free Fetal DNA, Telomeres, and the Spontaneous Onset of Parturition. Reproductive Sciences. 2015;22: 1186–1201. doi: 10.1177/1933719115592714 26134037

25. Midwood KS, Chiquet M, Tucker RP, Orend G. Tenascin-C at a glance. J Cell Sci. 2016;129: 4321–4327. doi: 10.1242/jcs.190546 27875272

26. Derzsy Z, Prohászka Z, Rigó J, Füst G, Molvarec A. Activation of the complement system in normal pregnancy and preeclampsia. Molecular Immunology. 2010;47: 1500–1506. doi: 10.1016/j.molimm.2010.01.021 20181396

27. Rathore S, Gupta A, Batra H, Res RR. Comparative study of trace elements and serum ceruloplasmin level in normal and pre-eclamptic pregnancies with their cord blood. 2011;

28. Skarżyńska E, Zborowska H, Jakimiuk AJ, Karlińska M, Lisowska-Myjak B. Variations in serum concentrations of C-reactive protein, ceruloplasmin, lactoferrin and myeloperoxidase and their interactions during normal human pregnancy and postpartum period. Journal of Trace Elements in Medicine and Biology. 2018;46: 83–87. doi: 10.1016/j.jtemb.2017.11.015 29413114

29. Pei Y, Zhang Y, Lei Y, Wu D, Ma T, Oncotarget LX. Hypermethylation of the CHRDL1 promoter induces proliferation and metastasis by activating Akt and Erk in gastric cancer. 2017;

30. Li Y, Parast MM. BMP4 regulation of human trophoblast development. International Journal of Developmental Biology. 2014;58: 239–246. doi: 10.1387/ijdb.130341mp 25023690

31. Girardi G, Bulla R, Salmon JE, Tedesco F. The complement system in the pathophysiology of pregnancy. Molecular Immunology. 2006;43: 68–77. doi: 10.1016/j.molimm.2005.06.017 16023727

32. Lynch AM, Gibbs RS, Murphy JR, Giclas PC, Salmon JE, Holers MV. Early Elevations of the Complement Activation Fragment C3a and Adverse Pregnancy Outcomes. Obstetrics & Gynecology. 2011;117: 75–83. doi: 10.1097/AOG.0b013e3181fc3afa 21173647

33. Sonderegger S, Pollheimer J, Knöfler M. Wnt Signalling in Implantation, Decidualisation and Placental Differentiation–Review. Placenta. 2010;31: 839–847. doi: 10.1016/j.placenta.2010.07.011 20716463

34. Niida A, Hiroko T, Kasai M, Furukawa Y, Nakamura Y, Suzuki Y, et al. DKK1, a negative regulator of Wnt signaling, is a target of the β-catenin/TCF pathway. Oncogene. 2004;23: 1207892. doi: 10.1038/sj.onc.1207892 15378020

35. Ackerman WE, Buhimschi IA, Eidem HR, Rinker DC, Rokas A, Rood K, et al. Comprehensive RNA profiling of villous trophoblast and decidua basalis in pregnancies complicated by preterm birth following intra-amniotic infection. Placenta. 2016;44: 23–33. doi: 10.1016/j.placenta.2016.05.010 27452435

36. Stampone E, Caldarelli I, Zullo A, Bencivenga D, Mancini F, Ragione F, et al. Genetic and Epigenetic Control of CDKN1C Expression: Importance in Cell Commitment and Differentiation, Tissue Homeostasis and Human Diseases. International Journal of Molecular Sciences. 2018;19: 1055. doi: 10.3390/ijms19041055 29614816

37. Fowden AL, Coan PM, Angiolini E, Burton GJ, Constancia M. Imprinted genes and the epigenetic regulation of placental phenotype. Progress in Biophysics and Molecular Biology. 2011;106: 281–288. doi: 10.1016/j.pbiomolbio.2010.11.005 21108957

38. Frank D, Fortino W, Clark L, Musalo R, Wang W, Saxena A, et al. Placental overgrowth in mice lacking the imprinted gene Ipl. Proceedings of the National Academy of Sciences. 2002;99: 7490–7495. doi: 10.1073/pnas.122039999 12032310

39. Rachmilewitz J, Goshen R, Ariel I, Schneider T, de Groot N, Hochberg A. Parental imprinting of the human H19 gene. FEBS Letters. 1992;309: 25–28. doi: 10.1016/0014-5793(92)80731-u 1380925

40. Hart SN, Therneau TM, Zhang Y, Poland GA, Kocher J-PP. Calculating sample size estimates for RNA sequencing data. Journal of computational biology: a journal of computational molecular cell biology. 2013;20: 970–8. doi: 10.1089/cmb.2012.0283 23961961

41. Gardosi J, Francis A, Turner S, Williams M. Customized growth charts: rationale, validation and clinical benefits. American Journal of Obstetrics and Gynecology. 2018;218: S609–S618. doi: 10.1016/j.ajog.2017.12.011 29422203

42. Committee Opinion No. 700 Summary. Obstetrics & Gynecology. 2017;129: 967–968. doi: 10.1097/AOG.0000000000002042 28426616

43. Buhimschi IA, Zhao G, Rosenberg VA, Abdel-Razeq S, Thung S, Buhimschi CS. Multidimensional Proteomics Analysis of Amniotic Fluid to Provide Insight into the Mechanisms of Idiopathic Preterm Birth. PLoS ONE. 2008;3: e2049. doi: 10.1371/journal.pone.0002049 18431506

44. AOG. Practice Bulletin No. 130: Prediction and Prevention of Preterm Birth. Obstetric Anesthesia Digest. 2013;33: 193. doi: 10.1097/01.aoa.0000436305.40425.86

45. Boekel J, Chilton JM, Cooke IR, Horvatovich PL, Jagtap PD, Käll L, et al. Multi-omic data analysis using Galaxy. Nature Biotechnology. 2015;33: 137–139. doi: 10.1038/nbt.3134 25658277

46. Adrews S. FASTQC, a quality control tool for highthroughput sequence data [Internet]. 2010. Available: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

47. Kruger F. TrimGalore! A tool to automate quality and adapter trimming for highthroughput sequencing [Internet]. 2012. Available: http://www.bioinformatics.babraham.ac.uk/projects/trim_galore/

48. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature Methods. 2012;9: 357. doi: 10.1038/nmeth.1923 22388286

49. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30: 923–930. doi: 10.1093/bioinformatics/btt656 24227677

50. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology. 2010;11: R25. doi: 10.1186/gb-2010-11-3-r25 20196867

51. Jones HN, Olbrych SK, Smith KL, Cnota JF, Habli M, Ramos-Gonzales O, et al. Hypoplastic left heart syndrome is associated with structural and vascular placental abnormalities and leptin dysregulation. Placenta. 2015;36: 1078–1086. doi: 10.1016/j.placenta.2015.08.003 26278057

52. Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D, et al. PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements. Nucleic Acids Research. 2017;45: D183–D189. doi: 10.1093/nar/gkw1138 27899595

Unique transcriptomic landscapes identified in idiopathic spontaneous and infection related preterm births compared to normal term births

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz