Single-cell transcriptomics of the human placenta: Inferring the cell communication network of the maternal-fetal interface

Genome Research

Volumn 27, Issue 3, 2017, Pages 349-361

  Pavličev, Mihaela ^a,b   Wagner, Günter P ^c,d,e   Chavan, Arun Rajendra ^c   Owens, Kathryn ^a   Maziarz, Jamie ^c   Dunn Fletcher, Caitlin ^b   Kallapur, Suhas G ^a,b   Muglia, Louis ^a,b   Jones, Helen ^a,b  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c YALE UNIVERSITY   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM12 PROTEIN; ALPHA5 INTEGRIN; AROMATASE; CD146 ANTIGEN; CD163 ANTIGEN; CD19 ANTIGEN; CD209 ANTIGEN; CSH2 PROTEIN; CSHL1 PROTEIN; G PROTEIN COUPLED RECEPTOR; GCM1 PROTEIN; GH2 PROTEIN; GLYCOPROTEIN; GROWTH FACTOR; GROWTH HORMONE; HLA DPA1 ANTIGEN; HLA DQB1 ANTIGEN; HLA DR ANTIGEN; HLA DRB1 ANTIGEN; HLA G ANTIGEN; HPGD PROTEIN; KRT7 PROTEIN; KRT8 PROTEIN; LIGAND; PROSTAGLANDIN; PROTEIN; RIBOSOME PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; UVOMORULIN; VASCULOTROPIN RECEPTOR 1;

ARTICLE; CELL COMMUNICATION; CELL CULTURE; CELL DIFFERENTIATION; CELL INTERACTION; CLINICAL ASSESSMENT; DECIDUA; DECIDUALIZATION; ENDOMETRIUM CELL; FEMALE; FETUS CELL; FETUS DEVELOPMENT; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; MOTHER FETUS RELATIONSHIP; PLACENTA; PREGNANCY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE CELL TRANSCRIPTOMICS; STROMA CELL; SYNCYTIOTROPHOBLAST; TRANSCRIPTOMICS; TROPHOBLAST; UPREGULATION; UTERUS; CELL LINE; CYTOLOGY; FETOMATERNAL TRANSFUSION; GENETICS; METABOLISM; SINGLE CELL ANALYSIS;

CELL COMMUNICATION; CELL LINE; CELLS, CULTURED; DECIDUA; FEMALE; HUMANS; MATERNAL-FETAL EXCHANGE; PREGNANCY; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS; TRANSCRIPTOME; UP-REGULATION;

EID: 85016478151     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.207597.116     Document Type: Article

References (60)

1. Bernard C. 1856. Introduction l'étude de la médecine expérimentale. J.B. Baillière, Paris.
2. Bernard C, Greene HC, Henderson LJ. 1927. An introduction to the study of experimental medicine. Macmillan, New York.
3. Biadasiewicz K, Fock V, Dekan S, Proestling K, Velicky P, Haider S, Knofler M, Frohlich C, Pollheimer J. 2014. Extravillous trophoblast-associated ADAM12 exerts pro-invasive properties, including induction of integrin 1-mediated cellular spreading. Biol Reprod 90: 101.
4. Bischof P, Meisser A, Campana A. 2000. Paracrine and autocrine regulators of trophoblast invasion-a review. Placenta 21: S55-S60.
5. Borbely AU, Sandri S, Fernandes IR, Prado KM, Cardoso EC, Correa-Silva S, Albuquerque R, Knofler M, Beltrao-Braga P, Campa A, et al. 2014. The term basal plate of the human placenta as a source of functional extravillous trophoblast cells. Reprod Biol Endocrinol 12: 7.
6. Bradford W, Buckholz A, Morton J, Price C, Jones AM, Urano D. 2013. Eukaryotic G protein signaling evolved to require G protein-coupled receptors for activation. Sci Signal 6: ra37.
7. Brar AK, Handwerger S, Kessler CA, Aronow BJ. 2001. Gene induction and categorical reprogramming during in vitro human endometrial fibroblast decidualization. Physiol Genomics 7: 135-148.
8. Brunskill EW, Park JS, Chung E, Chen F, Magella B, Potter SS. 2014. Single cell dissection of early kidney development: multilineage priming. Development 141: 3093-3101.
9. Buettner F, Natarajan KN, Casale FP, Proserpio V, Scialdone A, Theis FJ, Teichmann SA, Marioni JC, Stegle O. 2015. Computational analysis of cell-to-cell heterogeneity in single-cell RNA-sequencing data reveals hidden subpopulations of cells. Nat Biotechnol 33: 155-160.
10. Butts CL, Candando KM, Warfel J, Belyavskaya E,D'Agnillo F, Sternberg EM. 2010. Progesterone regulation of uterine dendritic cell function in rodents is dependent on the stage of estrous cycle. Mucosal Immunol 3: 496-505.
11. Calabria AR, Shusta EV. 2008. A genomic comparison of in vivo and in vitro brain microvascular endothelial cells. J Cereb Blood Flow Metab 28: 135-148.
12. Crosetto N, Bienko M, van Oudenaarden A. 2015. Spatially resolved transcriptomics and beyond. Nat Rev Genet 16: 57-66.
13. de Mendoza A, Sebé-Pedrós A, Ruiz-Trillo I. 2014. The evolution of the GPCR signaling system in eukaryotes: modularity, conservation, and the transition to metazoan multicellularity. Genome Biol Evol 6: 606-619.
14. D'Souza AW, Wagner GP. 2014. Malignant cancer and invasive placentation: a case for positive pleiotropy between endometrial and malignancy phenotypes. Evol Med Public Health 2014: 136-145.
15. Emig D, Salomonis N, Baumbach J, Lengauer T, Conklin BR, Albrecht M. 2010. AltAnalyze and DomainGraph: analyzing and visualizing exon expression data. Nucleic Acids Res 38: W755-W762.
16. Erlebacher A. 2013. Immunology of the maternal-fetal interface. Annu Rev Immunol 31: 387-411.
17. Fock V, Mairhofer M, Otti GR, Hiden U, Spittler A, Zeisler H, Fiala C, Knofler M, Pollheimer J. 2013. Macrophage-derived IL-33 is a critical factor for placental growth. J Immunol 191: 3734-3743.
18. Gellersen B, Brosens JJ. 2014. Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr Rev 35: 851-905.
19. Godbole G, Suman P, Gupta SK, Modi D. 2011. Decidualized endometrial stromal cell derived factors promote trophoblast invasion. Fertil Steril 95: 1278-1283.
20. Gu Z, Gu L, Eils R, Schlesner M, Brors B. 2014. circlize implements and enhances circular visualization in R. Bioinformatics 30: 2811-2812.
21. Handwerger S, AronowB. 2003. Dynamic changes in gene expression during human trophoblast differentiation. Recent Prog Horm Res 58: 263-281.
22. Hannon T, Innes BA, Lash GE, Bulmer JN, Robson SC. 2012. Effects of local decidua on trophoblast invasion and spiral artery remodeling in focal placenta creta-an immunohistochemical study. Placenta 33: 998-1004.
23. Hou X, Tan Y, Li M, Dey SK, Das SK. 2004. Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol 18: 3035-3049.
24. Hughes GC, Thomas S, Li C, Kaja MK, Clark EA. 2008. Cutting edge: Progesterone regulates IFN-a production by plasmacytoid dendritic cells. J Immunol 180: 2029-2033.
25. Ivanova E, Kyurkchiev D, Altankova I, Dimitrov J, Binakova E, Kyurkchiev S. 2005. CD83+ monocyte-derived dendritic cells are present in human decidua and progesterone induces their differentiation in vitro. Am J Reprod Immunol 53: 199-205.
26. Ji L, Brkic J, Liu M, Fu G, Peng C, Wang YL. 2013. Placental trophoblast cell differentiation: physiological regulation and pathological relevance to preeclampsia. Mol Aspects Med 34: 981-1023.
27. Jouve N, Despoix N, Espeli M, Gauthier L, Cypowyj S, Fallague K, Schiff C, Dignat-George F, Vely F, Leroyer AS. 2013. The involvement of CD146 and its novel ligand Galectin-1 in apoptotic regulation of endothelial cells. J Biol Chem 288: 2571-2579.
28. Kammerer U, Schoppet M, McLellan AD, Kapp M, Huppertz HI, Kampgen E, Dietl J. 2000. Human decidua contains potent immunostimulatory CD83+ dendritic cells. Am J Pathol 157: 159-169.
29. Kammerer U, Kruse A, Barrientos G, Arck PC, Blois SM. 2008. Role of dendritic cells in the regulation of maternal immune responses to the fetus during mammalian gestation. Immunol Invest 37: 499-533.
30. Karalis K, Goodwin G, Majzoub JA. 1996. Cortisol blockade of progesterone: a possible molecular mechanisminvolved in the initiation of human labor. Nat Med 2: 556-560.
31. Kaspi E, Guillet B, Piercecchi-Marti MD, Alfaidy N, Bretelle F, Bertaud-Foucault A, Stalin J, Rambeloson L, Lacroix O, Blot-Chabaud M, et al. 2013. Identification of soluble CD146 as a regulator of trophoblast migration: potential role in placental vascular development. Angiogenesis 16: 329-342.
32. Klein D, Demory A, Peyre F, Kroll J, Augustin HG, HelfrichW, Kzhyshkowska J, Schledzewski K, Arnold B, Goerdt S. 2008. Wnt2 acts as a cell type-specific, autocrine growth factor in rat hepatic sinusoidal endothelial cells cross-stimulating the VEGF pathway. Hepatology 47: 1018-1031.
33. Knofler M. 2010. Critical growth factors and signalling pathways controlling human trophoblast invasion. Int J Dev Biol 54: 269-280.
34. Knofler M, Pollheimer J. 2012. IFPA Award in Placentology lecture: molecular regulation of human trophoblast invasion. Placenta 33: S55-S62.
35. Knofler M, Pollheimer J. 2013. Human placental trophoblast invasion and differentiation: a particular focus on Wnt signaling. Front Genet 4: 190.
36. Kotas ME, Medzhitov R. 2015. Homeostasis, inflammation, and disease susceptibility. Cell 160: 816-827.
37. Lei K, Chen L, Georgiou EX, Sooranna SR, Khanjani S, Brosens JJ, Bennett PR, Johnson MR. 2012. Progesterone acts via the nuclear glucocorticoid receptor to suppress IL-1-induced COX-2 expression in human term myometrial cells. PLoS One 7: e50167.
38. Lewis MP, Morlese JF, Sullivan MH, Elder MG. 1993. Evidence for decidua-trophoblast interactions in early human pregnancy. Hum Reprod 8: 965-968.
39. LoVerso PR, Wachter CM, Cui F. 2015. Cross-species transcriptomic comparison of in vitro and in vivo mammalian neural cells. Bioinform Biol Insights 9: 153-164.
40. Lyons JP, Mueller UW, Ji H, Everett C, Fang X, Hsieh JC, Barth AM, McCrea PD. 2004. Wnt-4 activates the canonical catenin-mediated Wnt pathway and binds Frizzled-6 CRD: functional implications of Wnt/catenin activity in kidney epithelial cells. Exp Cell Res 298: 369-387.
41. Maltepe E, Fisher SJ. 2015. Placenta: the forgotten organ. Annu Rev Cell Dev Biol 31: 523-552.
42. Menkhorst EM, Lane N, Winship AL, Li P, Yap J, Meehan K, Rainczuk A, Stephens A, Dimitriadis E. 2012. Decidual-secreted factors alter invasive trophoblast membrane and secreted proteins implying a role for decidual cell regulation of placentation. PLoS One 7: e31418.
43. Mess A. 2014. Placental evolution within the supraordinal clades of eutheria with the perspective of alternative animal models for human placentation. Adv Biol 2014: 1-21.
44. Olsson A, Venkatasubramanian M, Chaudhri VK, Aronow BJ, Salomonis N, Singh H, Grimes HL. 2016. Single-cell analysis of mixed-lineage states leading to a binary cell fate choice. Nature 537: 698-702.
45. Roberts A, Pachter L. 2013. Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods 10: 71-73.
46. Samson WK, Zhang JV, Avsian-Kretchmer O, Cui K, Yosten GL, Klein C, Lyu RM, Wang YX, Chen XQ, Yang J, et al. 2008. Neuronostatin encoded by the somatostatin gene regulates neuronal, cardiovascular, and metabolic functions. J Biol Chem 283: 31949-31959.
47. Semrau S, van Oudenaarden A. 2015. Studying lineage decision-making in vitro: emerging concepts and novel tools. Annu Rev Cell Dev Biol 31: 317-345.
48. Stegle O, Teichmann SA, Marioni JC. 2015. Computational and analytical challenges in single-cell transcriptomics. Nat Rev Genet 16: 133-145.
49. Tagliani E, Erlebacher A. 2011. Dendritic cell function at the maternal-fetal interface. Expert Rev Clin Immunol 7: 593-602.
50. Talayev VY, Matveichev AV, Lomunova MA, Talayeva MV, Tsaturov ME, Zaichenko IY, Babaykina ON. 2010. The effect of human placenta cytotrophoblast cells on the maturation and T cell stimulating ability of dendritic cells in vitro. Clin Exp Immunol 162: 91-99.
51. Telugu BP, Adachi K, Schlitt JM, Ezashi T, Schust DJ, Roberts RM, Schulz LC. 2013. Comparison of extravillous trophoblast cells derived from human embryonic stem cells and from first trimester human placentas. Placenta 34: 536-543.
52. TrojaW, Kil K,KlankeC,JonesHN.2014.Interactionbetweenhumanplacental microvascular endothelial cells and a model of human trophoblasts: effects on growth cycle and angiogenic profile. Physiol Rep 2: e00244.
53. Wagner GP, Kin K, Lynch VJ. 2012. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci 131: 281-285.
54. Wagner GP, Kin K, Muglia L, Pavlicev M. 2014. Evolution of mammalian pregnancy and the origin of the decidual stromal cell. Int J Dev Biol 58: 117-126.
55. Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R. 2006. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc Natl Acad Sci 103: 3203-3208.
56. Ye Z, Zhang C, Tu T, Sun M, Liu D, Lu D, Feng J, Yang D, Liu F, Yan X. 2013. Wnt5a uses CD146 as a receptor to regulate cell motility and convergent extension. Nat Commun 4: 2803.
57. Yosten GL, Redlinger LJ, Samson WK. 2012. Evidence for an interaction of neuronostatin with the orphan G protein-coupled receptor, GPR107. Am J Physiol Regul Integr Comp Physiol 303: R941-R949.
58. Yosten GL, Elrick MM, Salvatori A, Stein LM, Kolar GR, Ren J, Corbett JA, Samson WK. 2015. Understanding peptide biology: the discovery and characterization of the novel hormone, neuronostatin. Peptides 72: 192-195.
59. Zhou Y, Fisher SJ, Janatpour M, Genbacev O, Dejana E, Wheelock M, Damsky CH. 1997. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest 99: 2139-2151.
60. Zhu XM, Han T, Sargent IL, Wang YL, Yao YQ. 2009. Conditioned medium from human decidual stromal cells has a concentration-dependent effect on trophoblast cell invasion. Placenta 30: 74-78.