Proteome profiling of human placenta reveals developmental stage-dependent alterations in protein signature
Tóm tắt
Placenta is a complex organ that plays a significant role in the maintenance of pregnancy health. It is a dynamic organ that undergoes dramatic changes in growth and development at different stages of gestation. In the first-trimester, the conceptus develops in a low oxygen environment that favors organogenesis in the embryo and cell proliferation and angiogenesis in the placenta; later in pregnancy, higher oxygen concentration is required to support the rapid growth of the fetus. This oxygen transition, which appears unique to the human placenta, must be finely tuned through successive rounds of protein signature alterations. This study compares placental proteome in normal first-trimester (FT) and term human placentas (TP). Normal human first-trimester and term placental samples were collected and differentially expressed proteins were identified using two-dimensional liquid chromatography-tandem mass spectrometry. Despite the overall similarities, 120 proteins were differently expressed in first and term placentas. Out of these, 72 were up-regulated and 48 were down-regulated in the first when compared with the full term placentas. Twenty out of 120 differently expressed proteins were sequenced, among them seven showed increased (GRP78, PDIA3, ENOA, ECH1, PRDX4, ERP29, ECHM), eleven decreased (TRFE, ALBU, K2C1, ACTG, CSH2, PRDX2, FABP5, HBG1, FABP4, K2C8, K1C9) expression in first-trimester compared to the full-term placentas and two proteins exclusively expressed in first-trimester placentas (MESD, MYDGF). According to Reactome and PANTHER softwares, these proteins were mostly involved in response to chemical stimulus and stress, regulation of biological quality, programmed cell death, hemostatic and catabolic processes, protein folding, cellular oxidant detoxification, coagulation and retina homeostasis. Elucidation of alteration in protein signature during placental development would provide researchers with a better understanding of the critical biological processes of placentogenesis and delineate proteins involved in regulation of placental function during development.
Tài liệu tham khảo
Dizon-Townson DS, Lu J, Morgan TK, Ward KJ. Genetic expression by fetal chorionic villi during the first trimester of human gestation. Am J Obstet Gynecol. 2000;183(3):706–11.
Morrish DW, Dakour J, Li H. Functional regulation of human trophoblast differentiation. J Reprod Immunol. 1998;39(1–2):179–95.
Sitras V, Fenton C, Paulssen R, Vårtun Å, Acharya G. Differences in gene expression between first and third trimester human placenta: a microarray study. PloS ONE. 2012;7(3):e33294.
Mikheev AM, Nabekura T, Kaddoumi A, Bammler TK, Govindarajan R, Hebert MF, et al. Profiling gene expression in human placentae of different gestational ages: an OPRU Network and UW SCOR Study. Reprod Sci. 2008;15(9):866–77.
Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, et al. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Investig. 2004;114(6):744–54.
Burton GJ. Oxygen, the Janus gas; its effects on human placental development and function. J Anat. 2009;215(1):27–35.
Maltepe E, Fisher SJ. Placenta: the forgotten organ. Annu Rev Cell Dev Biol. 2015;31:523–52.
Wakeland AK, Soncin F, Moretto-Zita M, Chang C-W, Horii M, Pizzo D, et al. Hypoxia directs human extravillous trophoblast differentiation in a hypoxia-inducible factor–dependent manner. Am J Pathol. 2017;187(4):767–80.
Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30(4):393–402.
Carmeliet P, Dor Y, Herbert J-M, Fukumura D, Brusselmans K, Dewerchin M, et al. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature. 1998;394(6692):485–90.
Robinson J, Ackerman W IV, Kniss D, Takizawa T, Vandre D. Proteomics of the human placenta: promises and realities. Placenta. 2008;29(2):135–43.
Mine K, Katayama A, Matsumura T, Nishino T, Kuwabara Y, Ishikawa G, et al. Proteome analysis of human placentae: pre-eclampsia versus normal pregnancy. Placenta. 2007;28(7):676–87.
Mushahary D, Gautam P, Sundaram CS, Sirdeshmukh R. Expanded protein expression profile of human placenta using two-dimensional gel electrophoresis. Placenta. 2013;34(2):193–6.
Robinson JM, Ackerman WE, Kniss DA, Takizawa T, Vandre DD. Proteomics of the human placenta: promises and realities. Placenta. 2008;29(2):135–43.
Assi E, D’Addio F, Mando C, Maestroni A, Loretelli C, Ben Nasr M, et al. Placental proteome abnormalities in women with gestational diabetes and large-for-gestational-age newborns. BMJ Open Diabetes Res Care. 2020;8(2):e001586.
Szklanna PB, Wynne K, Nolan M, Egan K, Áinle FN, Maguire PB. Comparative proteomic analysis of trophoblast cell models reveals their differential phenotypes, potential uses, and limitations. Proteomics. 2017;17(10):1700037.
Ner-Kluza J, Wawrzykowski J, Franczyk M, Siberring J, Kankofer M. Identification of protein patterns in bovine placenta at early-mid pregnancy - Pilot studies. Rapid Commun Mass Spectrom. 2019;33(12):1084–90.
Kankofer M, Wawrzykowski J, Hoedemaker M. Profile of bovine proteins in retained and normally expelled placenta in dairy cows. Reprod Domest Anim. 2014;49(2):270–4.
Abdulghani M, Song G, Kaur H, Walley JW, Tuteja G. Comparative analysis of the transcriptome and proteome during mouse placental development. J Proteome Res. 2019;18(5):2088–99.
Vandré DD, Ackerman WE IV, Tewari A, Kniss DA, Robinson JM. A placental sub-proteome: the apical plasma membrane of the syncytiotrophoblast. Placenta. 2012;33(3):207–13.
Fisher JJ, McKeating DR, Cuffe JS, Bianco-Miotto T, Holland OJ, Perkins AV. Proteomic analysis of placental mitochondria following trophoblast differentiation. Front Physiol. 2019;10:1536.
Tong M, Kleffmann T, Pradhan S, Johansson CL, DeSousa J, Stone PR, et al. Proteomic characterization of macro-, micro-and nano-extracellular vesicles derived from the same first trimester placenta: relevance for feto-maternal communication. Hum Reprod. 2016;31(4):687–99.
Heywood WE, Preece R-L, Pryce J, Hallqvist J, Clayton R, Virasami A, et al. Proteomic profiling reveals sub proteomes of the human placenta. Placenta. 2017;59:69–72.
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):770–8.
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):40.
Huuskonen P, Amezaga MR, Bellingham M, Jones LH, Storvik M, Häkkinen M, et al. The human placental proteome is affected by maternal smoking. Reprod Toxicol. 2016;63:22–31.
Gharesi-Fard B, Zolghadri J, Kamali-Sarvestani E. Proteome differences of placenta between pre-eclampsia and normal pregnancy. Placenta. 2010;31(2):121–5.
Gharesi-Fard B, Zolghadri J, Kamali-Sarvestani E. Alteration in the expression of proteins in unexplained recurrent pregnancy loss compared with in the normal placenta. J Reprod Dev. 2014;60(4):261–7.
Miao Z, Chen M, Wu H, Ding H, Shi Z. Comparative proteomic profile of the human placenta in normal and fetal growth restriction subjects. Cell Physiol Biochem. 2014;34(5):1701–10.
Chen CP, Chen YH, Chern SR, Chang SJ, Tsai TL, Li SH, et al. Placenta proteome analysis from Down syndrome pregnancies for biomarker discovery. Mol Biosyst. 2012;8(9):2360–72.
Gharesi-Fard B, Zolghadri J, Kamali-Sarvestani E. Proteome differences in the first- and third-trimester human placentas. Reprod Sci. 2015;22(4):462–8.
Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc. 2006;1(6):2856–60.
Fazel R, Guan Y, Vaziri B, Krisp C, Heikaus L, Saadati A, et al. Structural and in vitro functional comparability analysis of AltebrelTM, a proposed etanercept biosimilar: focus on primary sequence and glycosylation. Pharmaceuticals. 2019;12(1):14.
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):e78025.
Woods L, Perez-Garcia V, Hemberger M. Regulation of placental development and its impact on fetal growth-new insights from mouse models. Front Endocrinol. 2018;9:570.
Lash GE, Postovit L-M, Matthews NE, Chung EY, Canning MT, Pross H, et al. Oxygen as a regulator of cellular phenotypes in pregnancy and cancer. Can J Physiol Pharmacol. 2002;80(2):103–9.
Turco MY, Moffett A. Development of the human placenta. Development. 2019;146(22):dev163428.
Bortnov V, Tonelli M, Lee W, Lin Z, Annis DS, Demerdash ON, et al. Solution structure of human myeloid-derived growth factor suggests a conserved function in the endoplasmic reticulum. Nat Commun. 2019;10(1):1–14.
Qin K, Ma S, Li H, Wu M, Sun Y, Fu M, et al. GRP78 impairs production of lipopolysaccharide-induced cytokines by interaction with CD14. Front Immunol. 2017;8:579.
Jiang Q, Liu G, Chen J, Yao K, Yin Y. Crosstalk between nuclear glucose-regulated protein 78 and tumor protein 53 contributes to the lipopolysaccharide aggravated apoptosis of endoplasmic reticulum stress-responsive porcine intestinal epithelial cells. Cell Physiol Biochem. 2018;48(6):2441–55.
Fradet S, Pierredon S, Ribaux P, Epiney M, Shin Ya K, Irion O, et al. Involvement of membrane GRP78 in trophoblastic cell fusion. PLoS ONE. 2012;7(8):e40596.
Gharesi-Fard B, Jafarzadeh L, Ghaderi-shabankareh F, Zolghadri J, Kamali-Sarvestani E. Presence of autoantibody against two placental proteins, peroxiredoxin 3 and peroxiredoxin 4, in sera of recurrent pregnancy loss patients. Am J Reprod Immunol. 2013;69(3):248–55.
Stresing V, Baltziskueta E, Rubio N, Blanco J, Arriba MC, Valls J, et al. Peroxiredoxin 2 specifically regulates the oxidative and metabolic stress response of human metastatic breast cancer cells in lungs. Oncogene. 2013;32(6):724–35.
Knoops B, Argyropoulou V, Becker S, Ferté L, Kuznetsova O. Multiple roles of peroxiredoxins in inflammation. Mol Cells. 2016;39(1):60.
Schulte J. Peroxiredoxin 4: a multifunctional biomarker worthy of further exploration. BMC Med. 2011;9:137.
Wu F, Tian F, Zeng W, Liu X, Fan J, Lin Y, et al. Role of peroxiredoxin2 downregulation in recurrent miscarriage through regulation of trophoblast proliferation and apoptosis. Cell Death Dis. 2017;8(6):e2908.
Donangelo C, Bezerra F. In: Caballero, B, Finglas, P, Toldrá, F(Eds). Pregnancy: metabolic adaptations and nutritional requirements. The Encyclopedia of Food and Health. 2016; 1st Edition; Academic Press; Oxford; 4:484-90. 10.1016/B978-0-12-384947-2.00565-1.
Zeng Z, Liu F, Li S. Metabolic adaptations in pregnancy: a review. Ann Nutr Metab. 2017;70(1):59–65.
Makkar A, Mishima T, Chang G, Scifres C, Sadovsky Y. Fatty acid binding protein-4 is expressed in the mouse placental labyrinth, yet is dispensable for placental triglyceride accumulation and fetal growth. Placenta. 2014;35(10):802–7.
Duttaroy AK, Basak S. Maternal dietary fatty acids and their roles in human placental development. Prostagland Leukotrienes Essent Fatty Acids. 2020;55:102080.
Scifres CM, Catov JM, Simhan H. Maternal serum fatty acid binding protein 4 (FABP4) and the development of preeclampsia. J Clin Endocrinol Metab. 2012;97(3):E349–56.
Yu S, Levi L, Casadesus G, Kunos G, Noy N. Fatty acid-binding protein 5 (FABP5) regulates cognitive function both by decreasing anandamide levels and by activating the nuclear receptor peroxisome proliferator-activated receptor beta/delta (PPARbeta/delta) in the brain. J Biol Chem. 2014;289(18):12748–58.
Kizilgul M. The possible role of human placental lactogen in worse outcomes of differentiated thyroid cancer in pregnancy. HYPOTHESIS. 2015;1:4.
Lighthouse JK, Zhang L, Hsieh JC, Rosenquist T, Holdener BC. MESD is essential for apical localization of megalin/LRP2 in the visceral endoderm. Dev Dyn. 2011;240(3):577–88.
Corazzari M, Gagliardi M, Fimia GM, Piacentini M. Endoplasmic reticulum stress, unfolded protein response, and cancer cell fate. Front Oncol. 2017;7:78.
Shnyder SD, Hubbard MJ. ERp29 is a ubiquitous resident of the endoplasmic reticulum with a distinct role in secretory protein production. J Histochem Cytochem. 2002;50(4):557–66.
Zou S, Dong R, Zou P, Meng X, Zhang T, Luo L, et al. ERp29 affects the migratory and invasive ability of human extravillous trophoblast HTR-8/SVneo cells via modulating the epithelial-mesenchymal transition. J Biochem Mol Toxicol. 2020;34(4):e22454.
Wang Y, GrangerIn DN, Granger JP (EDS).Vascular biology of the placenta. Colloquium Series on Integrated Systems Physiology: From Molecule to Function. Morgan & Claypool Life Sciences; Louisiana State University. 2010;2(1):1-98. 10.4199/C00016ED1V01Y201008/SP009
Kralova A, Svetlikova M, Madar J, Ulcova-Gallova Z, Bukovsky A, Peknicova J. Differential transferrin expression in placentae from normal and abnormal pregnancies: a pilot study. Reprod Biol Endocrinol. 2008;6(1):27.
Chasteen ND. Human serotransferrin: structure and function. Coord Chem Rev. 1977;22(1–2):1–36.
Sun L, Lu T, Tian K, Zhou D, Yuan J, Wang X, et al. Alpha-enolase promotes gastric cancer cell proliferation and metastasis via regulating AKT signaling pathway. Eur J Pharmacol. 2019;845:8–15.
Plow EF, Das R. Enolase-1 as a plasminogen receptor. Blood, The Journal of the American Society of Hematology. 2009 May 28;113(22):5371-2.