Gene expression patterns in human placenta
Open accessAbstract
The placenta is the principal metabolic, respiratory, excretory, and endocrine organ for the first 9 months of fetal life. Its role in fetal and maternal physiology is remarkably diverse. Because of the central role that the placenta has in fetal and maternal physiology and development, the possibility that variation in placental gene expression patterns might be linked to important abnormalities in maternal or fetal health, or even variations in later life, warrants investigation. As an initial step, we used DNA microarrays to analyze gene expression patterns in 72 samples of amnion, chorion, umbilical cord, and sections of villus parenchyma from 19 human placentas from successful full-term pregnancies. The umbilical cord, chorion, amnion, and villus parenchyma samples were readily distinguished by differences in their global gene-expression patterns, many of which seemed to be related to physiology and histology. Differentially expressed genes have roles that include placental trophoblast secretion, signal transduction, metabolism, immune regulation, cell adhesion, and structure. We found interindividual differences in expression patterns in villus parenchyma and systematic differences between the maternal, fetal, and intermediate layers. A group of genes that was expressed in both the maternal and fetal villus parenchyma sections of placenta included genes that may be associated with preeclampsia. We identified sets of genes whose expression in placenta was significantly correlated with the sex of the fetus. This study provides a rich and diverse picture of the molecular variation in the placenta from healthy pregnancies.
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Placentas associated with female fetuses tend to have higher expression of genes involved in immune regulation, endocrine functions, and placental growth, while those from males have more inflammatory profiles.
“Placentas associated with female fetuses tend to have higher expression of genes involved in immune regulation, endocrine functions and placental growth (71, 512), whilst those from males have more inflammatory profiles (136).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [512]
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Cites
Molecular portraits of human breast tumours
Perou, C., Sørlie, T., Eisen, M., van de Rijn, M., Jeffrey, S., Rees, C. A., Pollack, J., Ross, D., Johnsen, H., Akslen, L., et al. (2000) · Nature · doi:10.1038/35021093 · Cited by 16,551 · see citing works
Self-citationCluster analysis and display of genome-wide expression patterns
Eisen, M. B., Spellman, P. T., Brown, P. O., & Botstein, D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.14863 · Cited by 16,077 · see citing works
Self-citationNishimura, R., Osako, T., Nishiyama, Y., Tashima, R., Nakano, M., Fujisue, M., Toyozumi, Y., & Arima, N. (2013) · Oncology · doi:10.1159/000353099 · Cited by 13,239 · see citing works
In silico prediction of protein-protein interactions in human macrophages
Souiai, O., Guerfali, F. Z., Miled, S. B., Brun, C., & Benkahla, A. (2014) · BMC Research Notes · doi:10.1186/1756-0500-7-157 · Cited by 10,785 · see citing works
Significance analysis of microarrays applied to the ionizing radiation response
Tusher, V. G., Tibshirani, R., & Chu, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091062498 · Cited by 10,568 · see citing works
Ki67 expression in breast cancer
Elkablawy, M. A., Albasri, A. M., Mohammed, R. A., Hussainy, A. S., Nouh, M. M., & Alhujaily, A. S. (2016) · Saudi Medical Journal · doi:10.15537/smj.2016.2.12285 · Cited by 4,382 · see citing works
Maynard, S. E., Min, J.-Y., Merchan, J., Lim, K.-H., Li, J., Mondal, S., Libermann, T. A., Morgan, J. P., Sellke, F. W., Stillman, I. E., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17189 · Cited by 4,101 · see citing works
Fetal nutrition and cardiovascular disease in adult life
Barker, D. J. P., Godfrey, K. M., Gluckman, P. D., Harding, J. E., Owens, J. A., & Robinson, J. S. (1993) · The Lancet · doi:10.1016/0140-6736(93)91224-a · Cited by 2,753 · see citing works
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,123 · see citing works
Living with the Past: Evolution, Development, and Patterns of Disease
Gluckman, P. D., & Hanson, M. A. (2004) · Science · doi:10.1126/science.1095292 · Cited by 1,921 · see citing works
Large-scale analysis of the human and mouse transcriptomes
Su, A. I., Cooke, M. P., Ching, K. A., Hakak, Y., Walker, J. R., Wiltshire, T., Orth, A. P., Vega, R. G., Sapinoso, L. M., Moqrich, A., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012025199 · Cited by 1,466 · see citing works
Differential Roles of Hypoxia-Inducible Factor 1α (HIF-1α) and HIF-2α in Hypoxic Gene Regulation
Hu, C.-J., Wang, L.-Y., Chodosh, L. A., Keith, B., & Simon, M. C. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.24.9361-9374.2003 · Cited by 1,386 · see citing works
Individuality and variation in gene expression patterns in human blood
Whitney, A. R., Diehn, M., Popper, S. J., Alizadeh, A. A., Boldrick, J. C., Relman, D. A., & Brown, P. O. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.252784499 · Cited by 775 · see citing works
Self-citationNatural variation in human gene expression assessed in lymphoblastoid cells
Cheung, V. G., Conlin, L. K., Weber, T. M., Arcaro, M., Jen, K., Morley, M. P., & Spielman, R. S. (2003) · Nature Genetics · doi:10.1038/ng1094 · Cited by 550 · see citing works
A Critical Role for Murine Complement Regulator Crry in Fetomaternal Tolerance
Xu, C., Mao, D., Holers, V. M., Palanca, B. J. A., Cheng, A. M., & Molina, H. D. (2000) · Science · doi:10.1126/science.287.5452.498 · Cited by 523 · see citing works
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes
Reik, W., Constância, M., Fowden, A. L., Anderson, N. F., Dean, W., Ferguson‐Smith, A. C., Tycko, B., & Sibley, C. P. (2003) · The Journal of Physiology · doi:10.1111/j.1469-7793.2003.00035.x · Cited by 409 · see citing works
Tanaka, T. S., Jaradat, S. A., Lim, M. K., Kargul, G. J., Wang, X., Grahovac, M. J., Pantano, S., Sano, Y., Piao, Y., Nagaraja, R., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.16.9127 · Cited by 407 · see citing works
Pathology of the Human Placenta
Benirschke, K., & Kaufmann, P. (2000) · Springer eBooks · doi:10.1007/978-1-4757-4199-5 · Cited by 400 · see citing works
Molecular Evidence of Placental Hypoxia in Preeclampsia
Soleymanlou, N., Jurišica, I., Nevo, O., Ietta, F., Zhang, X., Zamudio, S., Post, M., & Caniggia, I. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0078 · Cited by 394 · see citing works
Sex hormones as immunomodulators in health and disease
Verthelyi, D. I. (2001) · International Immunopharmacology · doi:10.1016/s1567-5769(01)00044-3 · Cited by 380 · see citing works
Clayton, A., Harris, C. L., Court, J., Mason, M. D., & Morgan, B. P. (2003) · European Journal of Immunology · doi:10.1002/immu.200310028 · Cited by 347 · see citing works
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes
Reik, W., Constância, M., Fowden, A. L., et al. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.033274 · Cited by 315 · see citing works
How to make a placenta: Mechanisms of trophoblast cell differentiation in mice – A Review
Cross, J. C. (2005) · Placenta · doi:10.1016/j.placenta.2005.01.015 · Cited by 255 · see citing works
Excessive placental secretion of neurokinin B during the third trimester causes pre-eclampsia
Page, N., Woods, R. J., Gardiner, S. M., Lomthaisong, K., Gladwell, R. T., Butlin, D., Manyonda, I., & Lowry, P. J. (2000) · Nature · doi:10.1038/35015579 · Cited by 250 · see citing works
A DNA microarray survey of gene expression in normal human tissues
Shyamsundar, R., Kim, Y. H., Higgins, J., Montgomery, K. D., Jorden, M. A., Sethuraman, A., van de Rijn, M., Botstein, D., Brown, P. O., & Pollack, J. R. (2005) · Genome biology · doi:10.1186/gb-2005-6-3-r22 · Cited by 226 · see citing works
Self-citationThe genetics of variation in gene expression
Cheung, V. G., & Spielman, R. S. (2002) · Nature Genetics · doi:10.1038/ng1036 · Cited by 220 · see citing works
The complement system in the pathophysiology of pregnancy
Girardi, G., Bulla, R., Salmon, J. E., & Tedesco, F. (2005) · Molecular Immunology · doi:10.1016/j.molimm.2005.06.017 · Cited by 184 · see citing works
Holmes, C. H., Simpson, K. L., Okada, H., et al. (1992) · European Journal of Immunology · doi:10.1002/eji.1830220635 · Cited by 158 · see citing works
MUC1/episialin: a critical barrier in the female reproductive tract
DeSouza, M. M., Surveyor, G. A., Price, R. E., et al. (2000) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(99)00046-7 · Cited by 153 · see citing works
The electrophysiology of feeding circuits
Jobst, E. E., Enriori, P. J., & Cowley, M. A. (2004) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2004.10.007 · Cited by 139 · see citing works
MUC1 and MUC2 in pancreatic neoplasia: Figure 1
Levi, E., Klimstra, D. S., Adsay, V. N., Andea, A. A., & Baştürk, O. (2004) · Journal of Clinical Pathology · doi:10.1136/jcp.2003.013292 · Cited by 127 · see citing works
Allele-specific gene expression differences in humans
Buckland, P. R. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh227 · Cited by 124 · see citing works
Male gender predisposes to prolongation of pregnancy
Divon, M. Y., Ferber, A., Nisell, H., & Westgren, M. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.126645 · Cited by 121 · see citing works
Roh, C., Budhraja, V., Kim, H.-S., Nelson, D. M., & Sadovsky, Y. (2004) · Placenta · doi:10.1016/j.placenta.2004.06.013 · Cited by 113 · see citing works
An extracellular activator of the Drosophila JAK/STAT pathway is a sex-determination signal element
Sefton, L., Timmer, J. R., Zhang, Y., Béranger, F., & Cline, T. W. (2000) · Nature · doi:10.1038/35016119 · Cited by 78 · see citing works
Local production and action of follistatin in human placenta
Petraglia, F., Gallinelli, A., Grande, A., Florio, P., Ferrari, S., Genazzani, A. R., LING, N. C., & DePaolo, L. V. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.78.1.8288705 · Cited by 75 · see citing works
Expression and localization of aquaporin 1 and 3 in human fetal membranes
Mann, S. E., Ricke, E. A., Yang, B. A., et al. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.127168 · Cited by 72 · see citing works
Sun, I. Y., Overgaard, M. T., Oxvig, C., et al. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020561 · Cited by 66 · see citing works
Incidence of Microbial Infection After Amniotic Membrane Transplantation
Marangon, F. B., Alfonso, E. C., Miller, D., et al. (2004) · Cornea · doi:10.1097/00003226-200404000-00008 · Cited by 54 · see citing works
Pulmonary Vascular Responses to Chronic Hypoxia Mediated by Hypoxia-inducible Factor 1
Semenza, G. L. (2005) · Proceedings of the American Thoracic Society · doi:10.1513/pats.200404-029ms · Cited by 47 · see citing works
Immunology of reproduction: Protecting the placenta
Morgan, B. P., & Holmes, C. H. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00476-0 · Cited by 43 · see citing works
The Neonatal Implications of a High Placental Ratio in Small-for-Gestational Age Infants
Lao, T. T. H., & Wong, W.-M. (1999) · Placenta · doi:10.1053/plac.1999.0432 · Cited by 34 · see citing works
Human placenta and fetal membranes express follistatin-related gene mRNA and protein
Ciarmela, P., Florio, P., Toti, P., et al. (2003) · Journal of Endocrinological Investigation · doi:10.1007/bf03347022 · Cited by 31 · see citing works
Tannetta, D., Muttukrishna, S., Groome, N. P., et al. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021924 · Cited by 27 · see citing works
Profile of neurokinin B concentrations in maternal and cord blood in normal pregnancy
Sakamoto, R., Osada, H., Iitsuka, Y., et al. (2003) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2003.01758.x · Cited by 27 · see citing works
Comings, D. E., Wu, S., González, N., et al. (2001) · Molecular Genetics and Metabolism · doi:10.1006/mgme.2001.3208 · Cited by 24 · see citing works
Hochachka's “Hypoxia Defense Strategies” and the development of the pathway for oxygen
Land, S. C. (2004) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpc.2004.02.016 · Cited by 18 · see citing works
Early postnatal skin colour changes in term newborns with subclinical histological chorioamnionitis
Felice, C. D., Vacca, P., Vecchio, A. D., Criscuolo, M., Lozupone, A., & Latini, G. (2004) · European Journal of Pediatrics · doi:10.1007/s00431-004-1488-8 · Cited by 10 · see citing works
Felice, C. D., Latini, G., Ginanneschi, C., et al. (2004) · European Journal of Pediatrics · doi:10.1007/s00431-004-1552-4 · Cited by 6 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [35]Sakamoto, R., Osada, H., Iitsuka, Y., Masuda, K., Kaku, K., Seki, K. & Sekiya, S. (2003) Clin . Endocrinol . (Oxford) 58, 597-600.
- [44]Cotran, R. S., Kumar, V. & Collins, T. (1999) Robbins Pathological Basis of Disease (Saunders, Philadelphia).
Cited by
Sorted by citations
The Placenta Harbors a Unique Microbiome
Aagaard, K., Ma, J., Antony, K. M., Ganu, R., Petrosino, J., & Versalovic, J. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008599 · Cited by 2,494 · see citing works
Review: Sex and the human placenta: Mediating differential strategies of fetal growth and survival
Clifton, V. L. (2010) · Placenta · doi:10.1016/j.placenta.2009.11.010 · Cited by 868 · see citing works
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
Gabory, A., Roseboom, T. J., Moore, T., Moore, L. G., & Junien, C. (2013) · Biology of Sex Differences · doi:10.1186/2042-6410-4-5 · Cited by 344 · see citing works
Bronson, S. L., & Bale, T. L. (2014) · Endocrinology · doi:10.1210/en.2014-1040 · Cited by 299 · see citing works
Mao, J., Zhang, X., Sieli, P. T., Falduto, M. T., Torres, K. E., & Rosenfeld, C. S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000440107 · Cited by 261 · see citing works
Tarrade, A., Panchenko, P., Junien, C., & Gabory, A. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110320 · Cited by 251 · see citing works
The omniscient placenta: Metabolic and epigenetic regulation of fetal programming
Nugent, B. M., & Bale, T. L. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.09.001 · Cited by 222 · see citing works
King, S., Dancause, K., Turcotte‐Tremblay, A., Veru, F., & Laplante, D. P. (2012) · Birth Defects Research Part C: Embryo Today: Reviews · doi:10.1002/bdrc.21026 · Cited by 232 · see citing works
Gallou-Kabani, C., Gabory, A., Tost, J., Karimi, M., Mayeur, S., Lesage, J., Boudadi, E., Gross, M.-S., Taurelle, J., Vigé, A., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014398 · Cited by 229 · see citing works
Gur, T. L., Shay, L., Palkar, A. V., Fisher, S., Varaljay, V. A., Dowd, S., & Bailey, M. T. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.12.021 · Cited by 213 · see citing works
Gabory, A., Ferry, L., Fajardy, I., Jouneau, L., Gothié, J.-D., Vigé, A., Fleur, C., Mayeur, S., Gallou-Kabani, C., Gross, M.-S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047986 · Cited by 204 · see citing works
Buckberry, S., Bianco-Miotto, T., Bent, S. J., Dekker, G. A., & Roberts, C. T. (2014) · Molecular Human Reproduction · doi:10.1093/molehr/gau035 · Cited by 186 · see citing works
Impaired mitochondrial function in human placenta with increased maternal adiposity
Mele, J., Muralimanoharan, S., Maloyan, A., & Myatt, L. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00025.2014 · Cited by 163 · see citing works
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Bruce-Keller, A. J., Fernandez-Kim, S.-O., Townsend, R. L., Kruger, C., Carmouche, R., Newman, S., Salbaum, J. M., & Berthoud, H.-R. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175577 · Cited by 76 · see citing works
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- Authors
- Sood, R., Zehnder, J. L., Druzin, M. L., & Brown, P. O.
- Affiliations
- Stanford University (US)
- Pathology, and
- Stanford Medicine (US)
- Departments of *Biochemistry,
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2006-04-04
- Volume
- 103
- Issue
- 14
- Pages
- 5478-5483
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1414632
- OpenAlex
- W2032337062
- Cited by
- 454
- References
- 49
- Citations by year
- 2026: 13 · 2025: 16 · 2024: 24 · 2023: 35 · 2022: 27 · 2021: 25 · 2020: 34 · 2019: 23 · 2018: 20 · 2017: 34 · 2016: 28 · 2015: 24 · 2014: 22 · 2013: 16 · 2012: 29
- FWCI
- 16.98
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- placenta, gene expression patterns, amniotic membrane, chorion, umbilical cord, interindividual variability, preeclampsia, fetal sex, placental trophoblast, placental immunity, placental metabolism
- MeSH terms
- Female, Humans, Male, Placenta, Gene Expression, Oligonucleotide Array Sequence Analysis
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