Quantitative proteomics-based analyses performed on pre-eclampsia samples in the 2004-2020 period: a systematic review

Rosana Navajas, Fernando Corrales, Alberto Paradela, Rosana Navajas, Fernando Corrales, Alberto Paradela

Abstract

Background: Quantitative proteomics is an invaluable tool in biomedicine for the massive comparative analysis of protein component of complex biological samples. In the last two decades, this technique has been used to describe proteins potentially involved in the pathophysiological mechanisms of preeclampsia as well as to identify protein biomarkers that could be used with diagnostic/prognostic purposes in pre-eclampsia.

Results: We have done a systematic review of all proteomics-based papers describing differentially expressed proteins in this disease. Searching Pubmed with the terms pre-eclampsia and proteomics, restricted to the Title/Abstract and to MeSH fields, and following manual curation of the original list, retrieved 69 original articles corresponding to the 2004-2020 period. We have only considered those results based on quantitative, unbiased proteomics studies conducted in a controlled manner on a cohort of control and pre-eclamptic individuals. The sources of biological material used were serum/plasma (n = 32), placenta (n = 23), urine (n = 9), cerebrospinal fluid (n = 2), amniotic fluid (n = 2) and decidual tissue (n = 1). Overall results were filtered based on two complementary criteria. First, we have only accounted all those proteins described in at least two (urine), three (placenta) and four (serum/plasma) independent studies. Secondly, we considered the consistency of the quantitative data, that is, inter-study agreement in the protein abundance control/pre-eclamptic ratio. The total number of differential proteins in serum/plasma (n = 559), placenta (n = 912), urine (n = 132) and other sources of biological material (n = 26), reached 1631 proteins. Data were highly complementary among studies, resulting from differences on biological sources, sampling strategies, patient stratification, quantitative proteomic analysis methods and statistical data analysis. Therefore, stringent filtering was applied to end up with a cluster of 18, 29 and 16 proteins consistently regulated in pre-eclampsia in placenta, serum/plasma and urine, respectively. The systematic collection, standardization and evaluation of the results, using diverse filtering criteria, provided a panel of 63 proteins whose levels are consistently modified in the context of pre-eclampsia.

Keywords: Biomarkers; Cohort studies; Placenta; Plasma; Pre-eclampsia; Pregnancy; Proteome; Proteomics; Urine.

Conflict of interest statement

The authors declare that they have no competing interests.

References

    1. Sibai B, Dekker G, Kupferminc M, Way AS. Pre-eclampsia. 2005.
    1. Young BC, Levine RJ, Karumanchi SA. Pathogenesis of Preeclampsia. Annu Rev Pathol Mech Dis. 2010;5(1):173–192. doi: 10.1146/annurev-pathol-121808-102149.
    1. Neiger R. Long-term effects of pregnancy complications on maternal health: a review. J Clin Med. 2017;6(8):76. doi: 10.3390/jcm6080076.
    1. Wilson BJ, Watson MS, Prescott GJ, Sunderland S, Campbell DM, Hannaford P, et al. Hypertensive diseases of pregnancy and risk of hypertension and stroke in later life: results from cohort study. Br Med J. 2003;326(7394):845–849. doi: 10.1136/bmj.326.7394.845.
    1. Irgens HU, Reisæter L, Irgens LM, Lie RT. Long term mortality of mothers and fathers after pre-eclampsia: population based cohort study. Br Med J. 2001;323(7323):1213–1216. doi: 10.1136/bmj.323.7323.1213.
    1. Powe CE, Levine RJ, Karumanchi SA. Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation. 2011;123(24):2856–2869. doi: 10.1161/CIRCULATIONAHA.109.853127.
    1. Chau K, Hennessy A, Makris A. Placental growth factor and pre-eclampsia. J Hum Hypertens. 2017;31(12):782–786. doi: 10.1038/jhh.2017.61.
    1. Maynard SE, Min J, Merchan J, Lim K-H, Li J, Mondal S, et al. Excess placental soluble fms-like hypertension , and proteinuria in. J Clin Invest. 2003;111(5):649–58. .
    1. Venkatesha S, Toporsian M, Lam C, Hanai JI, Mammoto T, Kim YM, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med. 2006;12(6):642–649. doi: 10.1038/nm1429.
    1. Wang A, Rana S, Karumanchi SA. Preeclampsia: the role of angiogenic factors in its pathogenesis. Physiology. 2009;24(3):147–158. doi: 10.1152/physiol.00043.2008.
    1. De Vivo A, Baviera G, Giordano D, Todarello G, Corrado F, D’Anna R. Endoglin, PlGF and sFlt-1 as markers for predicting pre-eclampsia. Acta Obstet Gynecol Scand. 2008;87(8):837–842. doi: 10.1080/00016340802253759.
    1. Zeisler H, Llurba E, Chantraine F, Vatish M, Staff AC, Sennström M, et al. Predictive value of the sFlt-1:PlGF ratio in women with suspected preeclampsia. N Engl J Med. 2016;374(1):13–22. doi: 10.1056/NEJMoa1414838.
    1. Agrawal S, Cerdeira AS, Redman C, Vatish M. Meta-analysis and systematic review to assess the role of soluble FMS-like tyrosine kinase-1 and placenta growth factor ratio in prediction of preeclampsia: The SaPPPhirE study. Hypertension. 2018;71(2):306–316. doi: 10.1161/HYPERTENSIONAHA.117.10182.
    1. Kalkunte SS, Neubeck S, Norris WE, Bin CS, Kostadinov S, Hoang DV, et al. Transthyretin is dysregulated in preeclampsia, and its native form prevents the onset of disease in a preclinical mouse model. Am J Pathol. 2013;183(5):1425–1436. doi: 10.1016/j.ajpath.2013.07.022.
    1. Cater JH, Kumita JR, Abdallah RZ, Zhao G, Bernardo-Gancedo A, Henry A, et al. Human pregnancy zone protein stabilizes misfolded proteins including preeclampsia- and Alzheimer’sassociated amyloid beta peptide. Proc Natl Acad Sci USA. 2019;116(13):6101–6110. doi: 10.1073/pnas.1817298116.
    1. Atkinson AJ, Colburn WA, DeGruttola VG, DeMets DL, Downing GJ, Hoth DF, et al. Biomarkers and surrogate endpoints: Preferred definitions and conceptual framework. Clin Pharmacol Ther. 2001;69(3):89–95. doi: 10.1067/mcp.2001.113989.
    1. Benny PA, Alakwaa FM, Schlueter RJ, Lassiter CB, Garmire LX. A review of omics approaches to study preeclampsia. Placenta. 2019;2020(92):17–27.
    1. Horgan RP, Kenny LC. SAC review ‘Omic’ technologies: proteomics and metabolomics Learning objectives: ethical issues. Obstet Gynaecol. 2011;13(3):189–195. doi: 10.1576/toag.13.3.189.27672/full.
    1. Garrido-Gomez T, Dominguez F, Quiñonero A, Diaz-Gimeno P, Kapidzic M, Gormley M, et al. Defective decidualization during and after severe preeclampsia reveals a possible maternal contribution to the etiology. Proc Natl Acad Sci USA. 2017;114(40):E8468–E8477. doi: 10.1073/pnas.1706546114.
    1. Tsang JCH, Vong JSL, Ji L, Poon LCY, Jiang P, Lui KO, et al. Integrative single-cell and cell-free plasma RNA transcriptomics elucidates placental cellular dynamics. Proc Natl Acad Sci USA. 2017;114(37):E7786–E7795. doi: 10.1073/pnas.1710470114.
    1. Austdal M, Brettas Silva G, Bowe S, Vesrheim Thomsen LC, Haugstad L, Bathen TF, et al. Metabolomics identifies placental dysfunction and confirms Flt-1 biomarker specificity. Hypertension. 2019;74(5):1136–1143. doi: 10.1161/HYPERTENSIONAHA.119.13184.
    1. Kelly RS, Croteau-Chonka DC, Dahlin A, Mirzakhani H, Wu AC, Wan ES, et al. Signatures associated with preeclampsia. Metabolomics. 2018;13(1):1–23.
    1. Kazmi N, Sharp GC, Reese SE, Vehmeijer FO, Lahti J, Page CM, et al. Hypertensive disorders of pregnancy and DNA methylation in newborns: findings from the pregnancy and childhood epigenetics consortium. Hypertension. 2019;74(2):375–383. doi: 10.1161/HYPERTENSIONAHA.119.12634.
    1. Bounds KR, Chiasson VL, Pan LJ, Gupta S, Chatterjee P. MicroRNAs: new players in the pathobiology of preeclampsia. Front Cardiovasc Med. 2017.
    1. Nguyen TPH, Patrick CJ, Parry LJ, Familari M. Using proteomics to advance the search for potential biomarkers for preeclampsia: a systematic review and meta-analysis. PLoS ONE. 2019;14(4):1–23.
    1. Nilsson T, Mann M, Aebersold R, Yates JR, Bairoch A, Bergeron JJM. Mass spectrometry in high-throughput proteomics: ready for the big time. Nat Methods. 2010;7(9):681–685. doi: 10.1038/nmeth0910-681.
    1. Görg A, Weiss W, Dunn MJ. Current two-dimensional electrophoresis technology for proteomics. Proteomics. 2004;4(12):3665–3685. doi: 10.1002/pmic.200401031.
    1. Westbrook JA, Noirel J, Brown JE, Wright PC, Evans CA. Quantitation with chemical tagging reagents in biomarker studies. Proteomics Clin Appl. 2015;9(3–4):295–300. doi: 10.1002/prca.201400120.
    1. Doll S, Burlingame AL. Mass spectrometry-based detection and assignment of protein posttranslational modifications. ACS Chem Biol. 2015;10(1):63–71. doi: 10.1021/cb500904b.
    1. Paradela A, Albar JP. Advances in the analysis of protein phosphorylation. J Proteome Res. 2008;7(5):1809. doi: 10.1021/pr7006544.
    1. Cuffe JSM, Holland O, Salomon C, Rice GE, Perkins AV. Review: placental derived biomarkers of pregnancy disorders. Placenta. 2017;54:104–110. doi: 10.1016/j.placenta.2017.01.119.
    1. Goulopoulou S, Davidge ST. Molecular mechanisms of maternal vascular dysfunction in preeclampsia. Trends Mol Med. 2015;21(2):88–97. doi: 10.1016/j.molmed.2014.11.009.
    1. Klein J, Buffin-Meyer B, Mullen W, Carty DM, Delles C, Vlahou A, et al. Clinical proteomics in obstetrics and neonatology. Expert Rev Proteom. 2014;11(1):75–89. doi: 10.1586/14789450.2014.872564.
    1. Mateos J, Carneiro I, Corrales F, Elortza F, Paradela A, del Pino MS, et al. Multicentric study of the effect of pre-analytical variables in the quality of plasma samples stored in biobanks using different complementary proteomic methods. J Proteomics. 2017 doi: 10.1016/j.jprot.2016.09.003.
    1. Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics. 2002;1(11):845–867. doi: 10.1074/mcp.R200007-MCP200.
    1. Staes A, Impens F, Van DP, Ruttens B, Goethals M, Demol H, et al. Selecting protein n-terminal peptides by combined fractional diagonal chromatography. Nat Protoc. 2011;6(8):1130–1141. doi: 10.1038/nprot.2011.355.
    1. Boschetti E, Righetti PG. The ProteoMiner in the proteomic arena: A non-depleting tool for discovering low-abundance species. J Proteomics. 2008;71(3):255–264. doi: 10.1016/j.jprot.2008.05.002.
    1. Gold L, Ayers D, Bertino J, Bock C, Bock A, Brody EN, et al. Aptamer-based multiplexed proteomic technology for biomarker discovery. PLoS ONE. 2010 doi: 10.1038/npre.2010.4538.1.
    1. Kolialexi A, Mavreli D, Tounta G, Mavrou A, Papantoniou N. Urine proteomic studies in preeclampsia. Proteomics Clin Appl. 2015;9(5–6):501–506. doi: 10.1002/prca.201400092.
    1. Ciampa E, Li Y, Dillon S, Lecarpentier E, Sorabella L, Libermann TA, et al. Cerebrospinal fluid protein changes in preeclampsia. Hypertension. 2018;72(1):219–226. doi: 10.1161/HYPERTENSIONAHA.118.11153.
    1. Norwitz ER, Tsen LC, Joong SP, Fitzpatrick PA, Dorfman DM, Saade GR, et al. Discriminatory proteomic biomarker analysis identifies free hemoglobin in the cerebrospinal fluid of women with severe preeclampsia. Am J Obstet Gynecol. 2005;193(3 SUPPL.):957–964. doi: 10.1016/j.ajog.2005.06.055.
    1. Joong SP, Oh KJ, Norwitz ER, Han JS, Choi HJ, Hyo SS, et al. Identification of proteomic biomarkers of preeclampsia in amniotic fluid using SELDI-TOF mass spectrometry. Reprod Sci. 2008;15(5):457–468. doi: 10.1177/1933719108316909.
    1. Vascotto C, Salzano AM, D’Ambrosio C, Fruscalzo A, Marchesoni D, Di Loreto C, et al. Oxidized transthyretin in amniotic fluid as an early marker of preeclampsia. J Proteome Res. 2007;6(1):160–170. doi: 10.1021/pr060315z.
    1. Feng YL, Zhou CJ, Li XM, Liang XQ. Alpha-1-antitrypsin acts as a preeclampsia-related protein: a proteomic study. Gynecol Obstet Invest. 2012;73(3):252–259. doi: 10.1159/000334820.
    1. Phipps EA, Thadhani R, Benzing T, Karumanchi SA. Pre-eclampsia: pathogenesis, novel diagnostics and therapies. Nat Rev Nephrol. 2019;15(5):275–289. doi: 10.1038/s41581-019-0119-6.
    1. Pierik E, Prins JR, van Goor H, Dekker GA, Daha MR, Seelen MAJ, et al. Dysregulation of complement activation and placental dysfunction: a potential target to treat preeclampsia? Front Immunol. 2020;10(January):1–14.
    1. Chiti F, Dobson CM. Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annu Rev Biochem. 2017;86(1):27–68. doi: 10.1146/annurev-biochem-061516-045115.
    1. Kolialexi A, Tsangaris GT, Sifakis S, Gourgiotis D, Katsafadou A, Lykoudi A, et al. Plasma biomarkers for the identification of women at risk for early-onset preeclampsia. Expert Rev Proteom. 2017;14(3):269–276. doi: 10.1080/14789450.2017.1291345.
    1. Smejkal GB. Proteomics sample preparation, preservation, and fractionation. Int J Proteomics. 2012;2012:1–2. doi: 10.1155/2012/701230.
    1. Klont F, Bras L, Wolters JC, Ongay S, Bischoff R, Halmos GB, et al. Assessment of sample preparation bias in mass spectrometry-based proteomics. Anal Chem. 2018;90(8):5405–5413. doi: 10.1021/acs.analchem.8b00600.
    1. Guryča V, Roeder D, Piraino P, Lamerz J, Ducret A, Langen H, et al. Automated sample preparation platform for mass spectrometry-based plasma proteomics and biomarker discovery. Biology (Basel) 2014;3(1):205–219.
    1. Zhang W, Chen X, Yan Z, Chen Y, Cui Y, Chen B, et al. Detergent-insoluble proteome analysis revealed aberrantly aggregated proteins in human preeclampsia placentas. J Proteome Res. 2017;16(12):4468–4480. doi: 10.1021/acs.jproteome.7b00352.
    1. Wang F, Shi Z, Wang P, You W, Liang G. Comparative proteome profile of human placenta from normal and preeclamptic pregnancies. PLoS ONE. 2013;8(10):1–10.
    1. Shin JK, Baek JC, Kang MY, Park JK, Lee SA, Lee JH, et al. Proteomic analysis reveals an elevated expression of heat shock protein 27 in preeclamptic placentas. Gynecol Obstet Invest. 2011;71(3):151–157. doi: 10.1159/000315162.
    1. Gharesi-Fard B, Zolghadri J, Kamali-Sarvestani E. Proteome Differences of Placenta Between Pre-Eclampsia and Normal Pregnancy. Placenta. 2010;31(2):121–125. doi: 10.1016/j.placenta.2009.11.004.
    1. Jin H, Dong MK, Hu R, Chen Y, Yang F, Yao J, et al. Analysis of expression and comparative profile of normal placental tissue proteins and those in preeclampsia patients using proteomic approaches. Anal Chim Acta. 2008;629(1–2):158–164. doi: 10.1016/j.aca.2008.09.015.
    1. Mary S, Kulkarni MJ, Malakar D, Joshi SR, Mehendale SS, Giri AP. Placental proteomics provides insights into pathophysiology of pre-eclampsia and predicts possible markers in plasma. J Proteome Res. 2017;16(2):1050–1060. doi: 10.1021/acs.jproteome.6b00955.
    1. Ma K, Jin H, Hu R, Xiong Y, Zhou S, Ting P, et al. A proteomic analysis of placental trophoblastic cells in preeclampsia-eclampsia. Cell Biochem Biophys. 2014;69(2):247–258. doi: 10.1007/s12013-013-9792-4.
    1. Jin X, Xu Z, Cao J, Shao P, Zhou M, Qin Z, et al. Proteomics analysis of human placenta reveals glutathione metabolism dysfunction as the underlying pathogenesis for preeclampsia. Biochim Biophys Acta Proteins Proteomics. 2017;1865(9):1207–1214. doi: 10.1016/j.bbapap.2017.07.003.
    1. Yang JI, Kong TW, Kim HS, Kim HY. The proteomic analysis of human placenta with pre-eclampsia and normal pregnancy. J Korean Med Sci. 2015;30(6):770–778. doi: 10.3346/jkms.2015.30.6.770.
    1. Xu Z, Jin X, Cai W, Zhou M, Shao P, Yang Z, et al. Proteomics analysis reveals abnormal electron transport and excessive oxidative stress cause mitochondrial dysfunction in placental tissues of early-onset preeclampsia. Proteomics Clin Appl. 2018;12(5):1–11. doi: 10.1002/prca.201700165.
    1. Zhang H, Wang Y, Chen D. Analysis of nitroso-proteomes in normotensive and severe preeclamptic human placentas. Biol Reprod. 2011;84(5):966–975. doi: 10.1095/biolreprod.110.090688.
    1. Baig S, Kothandaraman N, Manikandan J, Rong L, Ee KH, Hill J, et al. Proteomic analysis of human placental syncytiotrophoblast microvesicles in preeclampsia. Clin Proteomics. 2014;11(1):1–8. doi: 10.1186/1559-0275-11-40.
    1. Shi Z, Long W, Zhao C, Guo X, Shen R, Ding H. Comparative proteomics analysis suggests that placental mitochondria are involved in the development of pre-eclampsia. PLoS ONE. 2013;8(5):e64351. doi: 10.1371/journal.pone.0064351.
    1. Sun X, Qu T, He X, Yang X, Guo N, Mao Y, et al. Screening of differentially expressed proteins from syncytiotrophoblast for severe early-onset preeclampsia in women with gestational diabetes mellitus using tandem mass tag quantitative proteomics. BMC Pregnancy Childbirth. 2018;18(1):1–11. doi: 10.1186/s12884-017-1633-9.
    1. Sun LZ, Yang NN, De W, Xiao YS. Proteomic analysis of proteins differentially expressed in preeclamptic trophoblasts. Gynecol Obstet Invest. 2007;64(1):17–23. doi: 10.1159/000098399.
    1. Johnstone ED, Sawicki G, Guilbert L, Winkler-Lowen B, Cadete VJJ, Morrish DW. Differential proteomic analysis of highly purified placental cytotrophoblasts in pre-eclampsia demonstrates a state of increased oxidative stress and reduced cytotrophoblast antioxidant defense. Proteomics. 2011;11(20):4077–4084. doi: 10.1002/pmic.201000505.
    1. Blankley RT, Fisher C, Westwood M, North R, Baker PN, Walker MJ, et al. A label-free selected reaction monitoring workflow identifies a subset of pregnancy specific glycoproteins as potential predictive markers of early-onset pre-eclampsia. Mol Cell Proteomics. 2013;12(11):3148–3159. doi: 10.1074/mcp.M112.026872.
    1. Rasanen J, Girsen A, Lu X, Lapidus JA, Standley M, Reddy A, et al. Comprehensive maternal serum proteomic profiles of preclinical and clinical preeclampsia. J Proteome Res. 2010;9(8):4274–4281. doi: 10.1021/pr100198m.
    1. Tarca AL, Romero R, Benshalom-Tirosh N, Than NG, Gudicha DW, Done B, et al. The prediction of early preeclampsia: results from a longitudinal proteomics study. PLoS ONE. 2019;14:1–34. doi: 10.1371/journal.pone.0217273.
    1. Low HP, Tiwari A, Janjanam J, Qiu L, Chang CI, Strohsnitter WC, et al. Screening preeclamptic cord plasma for proteins associated with decreased breast cancer susceptibility. Genom Proteom Bioinforma. 2013;11(6):335–344. doi: 10.1016/j.gpb.2013.09.009.
    1. Than NG, Romero R, Tarca AL, Kekesi KA, Xu Y, Xu Z, et al. Integrated systems biology approach identifies novel maternal and placental pathways of preeclampsia. Front Immunol. 2018 doi: 10.3389/fimmu.2018.01661.
    1. Hsu TY, Hsieh TT, Yang KD, Tsai CC, Ou CY, Cheng BH, et al. Proteomic profiling reveals α1-antitrypsin, α1-microglobulin, and clusterin as preeclampsia-related serum proteins in pregnant women. Taiwan J Obstet Gynecol. 2015;54(5):499–504. doi: 10.1016/j.tjog.2014.01.007.
    1. Liu C, Zhang N, Yu H, Chen Y, Liang Y, Deng H, et al. Proteomic analysis of human serum for Finding pathogenic factors and potential biomarkers in preeclampsia. Placenta. 2011;32(2):168–174. doi: 10.1016/j.placenta.2010.11.007.
    1. Auer J, Camoin L, Guillonneau F, Rigourd V, Chelbi ST, Leduc M, et al. Serum profile in preeclampsia and intra-uterine growth restriction revealed by iTRAQ technology. J Proteomics. 2010;73(5):1004–1017. doi: 10.1016/j.jprot.2009.12.014.
    1. Kim SM, Cho BK, Kang MJ, Norwitz ER, Lee SM, Lee J, et al. Expression changes of proteins associated with the development of preeclampsia in maternal plasma: a case-control study. Proteomics. 2016;16(10):1581–1589. doi: 10.1002/pmic.201500381.
    1. Blankley RT, Gaskell SJ, Whetton AD, Dive C, Baker PN, Myers JE. A proof-of-principle gel-free proteomics strategy for the identification of predictive biomarkers for the onset of pre-eclampsia. BJOG An Int J Obstet Gynaecol. 2009;116(11):1473–1480. doi: 10.1111/j.1471-0528.2009.02283.x.
    1. Blumenstein M, McMaster MT, Black MA, Wu S, Prakash R, Cooney J, et al. A proteomic approach identifies early pregnancy biomarkers for preeclampsia: Novel linkages between a predisposition to preeclampsia and cardiovascular disease. Proteomics. 2009;9(11):2929–2945. doi: 10.1002/pmic.200800625.
    1. Kolla V, Jenö P, Moes S, Lapaire O, Hoesli I, Hahn S. Quantitative proteomic (iTRAQ) analysis of 1st trimester maternal plasma samples in pregnancies at risk for preeclampsia. J Biomed Biotechnol. 2012 doi: 10.1155/2012/305964.
    1. Ling Y, Su J, Lin J, Wang S. Screening of serum biomarkers of preeclampsia by proteomics combination with bioinformatics. Hypertens Pregnancy. 2019;38(3):184–192. doi: 10.1080/10641955.2019.1640246.
    1. Lu Q, Liu C, Liu Y, Zhang N, Deng H, Zhang Z. Serum markers of pre-eclampsia identified on proteomics. J Obstet Gynaecol Res. 2016;42(9):1111–1118. doi: 10.1111/jog.13037.
    1. Jia R, Li J, Rui C, Ji H, Ding H, Lu Y, et al. Comparative proteomic profile of the human umbilical cord blood exosomes between normal and preeclampsia pregnancies with high-resolution mass spectrometry. Cell Physiol Biochem. 2015;36(6):2299–2306. doi: 10.1159/000430193.
    1. Erez O, Romero R, Maymon E, Chaemsaithong P, Done B, Pacora P, et al. The prediction of late-onset preeclampsia: Results from a longitudinal proteomics study. PLoS ONE. 2017;12(7):1–28. doi: 10.1371/journal.pone.0181468.
    1. Shao X, Wang Y, Liu Y, Guo X, Li D, Huo R, et al. Association of imbalanced sex hormone production with excessive procoagulation factor SerpinF2 in preeclampsia. J Hypertens. 2019;37(1):197–205.
    1. Blumenstein M, McCowan LME, Wu S, Cooper GJS, North RA. Plasma clusterin increased prior to Small for Gestational Age (SGA) associated with preeclampsia and decreased prior to SGA in normotensive pregnancies. Reprod Sci. 2012;19(6):650–657. doi: 10.1177/1933719111430999.
    1. Watanabe H, Hamada H, Yamada N, Sohda S, Yamakawa-Kobayashi K, Yoshikawa H, et al. Proteome analysis reveals elevated serum levels of clusterin in patients with preeclampsia. Proteomics. 2004;4(2):537–543. doi: 10.1002/pmic.200300565.
    1. Myers JE, Tuytten R, Thomas G, Laroy W, Kas K, Vanpoucke G, et al. Integrated proteomics pipeline yields novel biomarkers for predicting preeclampsia. Hypertension. 2013;61(6):1281–1288. doi: 10.1161/HYPERTENSIONAHA.113.01168.
    1. Masoumi Z, Maes GE, Herten K, Cortés-Calabuig Á, Alattar AG, Hanson E, et al. Preeclampsia is associated with sex-specific transcriptional and proteomic changes in fetal erythroid cells. Int J Mol Sci. 2019;20(8):1–20. doi: 10.3390/ijms20082038.
    1. Dai X, Song X, Rui C, Meng L, Xue X, Ding H, et al. Peptidome analysis of human serum from normal and preeclamptic pregnancies. J Cell Biochem. 2017;118(12):4341–4348. doi: 10.1002/jcb.26087.
    1. Wang CC, Yim KW, Poon TCW, Choy KW, Chu CY, Lui WT, et al. Innate immune response by ficolin binding in apoptotic placenta is associated with the clinical syndrome of preeclampsia. Clin Chem. 2007;53(1):42–52. doi: 10.1373/clinchem.2007.074401.
    1. Sergeeva VA, Zakharova NV, Bugrova AE, Starodubtseva NL, Indeykina MI, Kononikhin AS, et al. The high-resolution mass spectrometry study of the protein composition of amyloid-like urine aggregates associated with preeclampsia. Eur J Mass Spectrom. 2020;26(2):158–161. doi: 10.1177/1469066719860076.
    1. Guo HX, Bin ZY, Wu CP, Zhong M, Hu SW. Potential urine biomarkers for gestational hypertension and preeclampsia. Mol Med Rep. 2019;19(4):2463–2470.
    1. Chen G, Zhang Y, Jin X, Zhang L, Zhou Y, Niu J, et al. Urinary proteomics analysis for renal injury in hypertensive disorders of pregnancy with iTRAQ labeling and LC-MS/MS. Proteomics Clin Appl. 2011;5(5–6):300–310. doi: 10.1002/prca.201000100.
    1. Ding W, Qiu B, Cram DS, Chen X, Li S, Zhou X, et al. Isobaric tag for relative and absolute quantitation based quantitative proteomics reveals unique urinary protein profiles in patients with preeclampsia. J Cell Mol Med. 2019;23(8):5822–5826. doi: 10.1111/jcmm.14459.
    1. Starodubtseva N, Nizyaeva N, Baev O, Bugrova A, Gapaeva M, Muminova K, et al. SERPINA1 peptides in urine as a potential marker of preeclampsia severity. Int J Mol Sci. 2020;21(3):1–15. doi: 10.3390/ijms21030914.
    1. Kononikhin AS, Starodubtseva NL, Bugrova AE, Shirokova VA, Chagovets VV, Indeykina MI, et al. An untargeted approach for the analysis of the urine peptidome of women with preeclampsia. J Proteomics. 2016;149:38–43. doi: 10.1016/j.jprot.2016.04.024.
    1. Buhimschi IA, Zhao G, Funai EF, Harris N, Sasson IE, Bernstein IM, et al. Proteomic profiling of urine identifies specific fragments of SERPINA1 and albumin as biomarkers of preeclampsia. Am J Obstet Gynecol. 2008;199(5):551.e1–551.e16. doi: 10.1016/j.ajog.2008.07.006.
    1. Carty DM, Siwy J, Brennand JE, Zürbig P, Mullen W, Franke J, et al. Urinary proteomics for prediction of preeclampsia. Hypertension. 2011;57(3 Part 2):561–569. doi: 10.1161/HYPERTENSIONAHA.110.164285.

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere