Integrated proteome and acetylome analyses unveil protein features of gestational diabetes mellitus and preeclampsia.
gestational diabetes
lysine acetylation
mellitus
oxidative stress
preeclampsia
proteomics
Journal
Proteomics
ISSN: 1615-9861
Titre abrégé: Proteomics
Pays: Germany
ID NLM: 101092707
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
17
08
2022
received:
27
03
2022
accepted:
25
08
2022
pubmed:
14
9
2022
medline:
25
11
2022
entrez:
13
9
2022
Statut:
ppublish
Résumé
Gestational diabetes mellitus (GDM) and preeclampsia (PE) are associated with maternal and infant health. Although the pathogenesis of PE and GDM remains controversial, oxidative stress is involved in the underlying pathology of GDM and PE. Protein lysine acetylation (Kac) plays an important regulatory role in biological processes. There is little data regarding the association of the maternal acetylome with GDM and PE. This study aimed to assess the potential value of the proteome and acetylome for GDM and PE. In our study, we included placental tissues from healthy individuals (n = 6), GDM patients (n = 6), and PE patients (n = 6) to perform 4D-label free quantification proteomics analysis and PRM analysis. We identified 22 significantly regulated proteins and 192 significantly regulated acetylated proteins between the GDM and PE groups. Furthermore, 192 significantly regulated acetylated proteins were mainly enriched in endoplasmic reticulum stress (ERS) and ferroptosis pathways. Seventeen acetylated sites in these two pathways were verified by PRM analysis. Our comprehensive analysis revealed key features of GDM/PE-significantly regulated acetylated proteins in the placentas from GDM and PE. The results of signaling pathway analysis focused on ERS and ferroptosis. These findings may help explore the underlying pathology, new biomarkers, and therapeutic targets of GDM and PE.
Identifiants
pubmed: 36097143
doi: 10.1002/pmic.202200124
doi:
Substances chimiques
Proteome
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2200124Informations de copyright
© 2022 Wiley-VCH GmbH.
Références
Yu, Y., Soohoo, M., Sørensen, H. T., Li, J., & Arah, O. A. (2022). Gestational diabetes mellitus and the risks of overall and type-specific cardiovascular diseases: A Population- and Sibling-Matched cohort study. Diabetes Care., 45(1), 151-159. https://doi.org/10.2337/dc21-1018
Mcintyre, H. D., Catalano, P., Zhang, C., Desoye, G., Mathiesen, E. R., & Damm, P. (2019). Gestational diabetes mellitus. Nat. Rev. Dis. Primers, 5(1), 47. https://doi.org/10.1038/s41572-019-0098-8
Schneider, S., Bock, C., Wetzel, M., Maul, H., & Loerbroks, A. (2012). The prevalence of gestational diabetes in advanced economies. J. Perinat. Med., 40(5), 511-520. https://doi.org/10.1515/jpm-2012-0015
Schneider, S., Freerksen, N., Röhrig, S., Hoeft, B., & Maul, H. (2012). Gestational diabetes and preeclampsia - Similar risk factor profiles? Early Hum. Dev., 88(3), 179-184. doi: https://doi.org/10.1016/j.earlhumdev.2011.08.004
Weissgerber, T. L., & Mudd, L. M. (2015). Preeclampsia and diabetes. Curr. Diab. Rep., 15(3), 9. https://doi.org/10.1007/s11892-015-0579-4
Say, L., Chou, D., Gemmill, A., Tunçalp, Ö., Moller, A. B., Daniels, J., Gülmezoglu, A. M., Temmerman, M., & Alkema, L. (2014). Global causes of maternal death: A WHO systematic analysis. Lancet Global Health, 2(6), e323-e333. https://doi.org/10.1016/s2214-109x(14)70227-x
Ananth, C. V., Keyes, K. M., & Wapner, R. J. (2013). Pre-eclampsia rates in the united states, 1980-2010: Age-period-cohort analysis. BMJ, 347, f6564. https://doi.org/10.1136/bmj.f6564
Koprinarova, M., Schnekenburger, M., & Diederich, M. (2016). Role of histone acetylation in cell cycle regulation. Curr. Top. Med. Chem., 16(7), 732-744. https://doi.org/10.2174/1568026615666150825140822
Li, P., Ge, J., & Li, H. (2020). Lysine acetyltransferases and lysine deacetylases as targets for cardiovascular disease. Nat. Rev. Cardiol., 17(2), 96-115. https://doi.org/10.1038/s41569-019-0235-9
Wang, M., & Lin, H. (2021). Understanding the function of mammalian sirtuins and protein lysine acylation. Annu. Rev. Biochem., 90, 245-285. https://doi.org/10.1146/annurev-biochem-082520-125411
Zhang, B., Kim, M. Y., Elliot, G., Zhou, Y., Zhao, G., Li, D., Lowdon, R. F., Gormley, M., Kapidzic, M., Robinson, J. F., Mcmaster, M. T., Hong, C., Mazor, T., Hamilton, E., Sears, R. L., Pehrsson, E. C., Marra, M. A., Jones, S. J. M., Bilenky, M., … & Fisher, S. J. (2021). Human placental cytotrophoblast epigenome dynamics over gestation and alterations in placental disease. Dev. Cell, 56(9), 1238-1252.e5. https://doi.org/10.1016/j.devcel.2021.04.001
Zhao, Y., Jia, X., Yang, X., Bai, X., Lu, Y., Zhu, L., Cheng, W., Shu, M., Zhu, Y., Du, X., Wang, L., Shu, Y., Song, Y., & Jin, S. (2022). Deacetylation of caveolin-1 by sirt6 induces autophagy and retards high glucose-stimulated LDL transcytosis and atherosclerosis formation. Metabolism, 131, 155162. https://doi.org/10.1016/j.metabol.2022.155162
Shangguan, Y., Wang, Y., Shi, W., Guo, R., Zeng, Z., Hu, W., Cai, W., Yan, Q., Xu, Y., Tang, D., & Dai, Y. (2021). Systematic proteomics analysis of lysine acetylation reveals critical features of placental proteins in pregnant women with preeclampsia. J. Cell. Mol. Med., 25(22), 10614-10626. https://doi.org/10.1111/jcmm.16997
Kamrani, A., Alipourfard, I., Ahmadi-Khiavi, H., Yousefi, M., Rostamzadeh, D., Izadi, M., & Ahmadi, M. (2019). The role of epigenetic changes in preeclampsia. Biofactors, 45(5), 712-724. https://doi.org/10.1002/biof.1542
Zhu, H., & Wang, C. (2021). HDAC2-mediated proliferation of trophoblast cells requires the miR-183/FOXA1/IL-8 signaling pathway. J. Cell. Physiol., 236(4), 2544-2558. https://doi.org/10.1002/jcp.30026
Liu, Y., Fan, X., Wang, R., Lu, X., Dang, Y.-L., Wang, H., Lin, H.-Y., Zhu, C., Ge, H., Cross, J. C., & Wang, H. (2018). Single-cell RNA-seq reveals the diversity of trophoblast subtypes and patterns of differentiation in the human placenta. Cell Res., 28(8), 819-832. https://doi.org/10.1038/s41422-018-0066-y
Joo, E. H., Kim, Y. R., Kim, N., Jung, J. E., Han, S. H, & Cho, H. Y. (2021). Effect of endogenic and exogenic oxidative stress triggers on adverse pregnancy outcomes: Preeclampsia, fetal growth restriction, gestational diabetes mellitus and preterm birth. Int. J. Mol. Sci., 22(18), 10122. https://doi.org/10.3390/ijms221810122
ACOG Practice Bulletin No, 202. (2019). Gestational hypertension and preeclampsia. Obstet. Gynecol., 133(1), 1. https://doi.org/10.1097/aog.0000000000003018
American Diabetes Association. (2020). 14. Management of diabetes in pregnancy: Standards of medical care in diabetes-2020. Diabetes Care., 43(Suppl 1), S183-S192. https://doi.org/10.2337/dc20-S014
Wu, T., Hu, E., Xu, S., Chen, M., Guo, P., Dai, Z., Feng, T., Zhou, L., Tang, W., Zhan, L., Fu, X., Liu, S., Bo, X., & Yu, G. (2021). clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. Innovation (N Y), 2(3), 100141. https://doi.org/10.1016/j.xinn.2021.100141
Mavreli, D., Evangelinakis, N., Papantoniou, N., & Kolialexi, A. (2020). Quantitative comparative proteomics reveals candidate biomarkers for the early prediction of gestational diabetes mellitus: A preliminary study. In Vivo, 34(2), 517-525. doi: 10.21873/invivo.11803
Youssef, L., Miranda, J., Blasco, M., Paules, C., Crovetto, F., Palomo, M., Torramade-Moix, S., García-Calderó, H., Tura-Ceide, O., Dantas, A. P., Hernandez-Gea, V., Herrero, P., Canela, N., Campistol, J. M., Garcia-Pagan, J. C., Diaz-Ricart, M., Gratacos, E., & Crispi, F. (2021). Complement and coagulation cascades activation is the main pathophysiological pathway in early-onset severe preeclampsia revealed by maternal proteomics. Sci. Rep., 11(1), 3048. https://doi.org/10.1038/s41598-021-82733-z
Lai, M., Liu, Y., Ronnett, G. V., Wu, A., Cox, B. J., Dai, F. F., Röst, H. L., Gunderson, E. P., & Wheeler, M. B. (2020). Amino acid and lipid metabolism in post-gestational diabetes and progression to type 2 diabetes: A metabolic profiling study. PLoS Med., 17(5), e1003112. https://doi.org/10.1371/journal.pmed.1003112
Alur, V., Raju, V., Vastrad, B., Tengli, A., Vastrad, C., & Kotturshetti, S. (2021). Integrated bioinformatics analysis reveals novel key biomarkers and potential candidate small molecule drugs in gestational diabetes mellitus. Biosci. Rep., 41(5), BSR20210617. https://doi.org/10.1042/bsr20210617
Jung, Y. W., Shim, J. I., Shim, S. H., Shin, Y.-J., Shim, S. H., Chang, S. W., & Cha, D. H. (2019). Global gene expression analysis of cell-free RNA in amniotic fluid from women destined to develop preeclampsia. Medicine (Baltimore)., 98(3), e13971. https://doi.org/10.1097/md.0000000000013971
Løset, M., Mundal, S. B., Johnson, M. P., Fenstad, M. H., Freed, K. A., Lian, I. A., Eide, I. P., Bjørge, L., Blangero, J., Moses, E. K., & Austgulen, R. (2011). A transcriptional profile of the decidua in preeclampsia. Am. J. Obstet. Gynecol., 204(1), 84.e1-84.e27. https://doi.org/10.1016/j.ajog.2010.08.043
Xu, Z., Wu, C., Liu, Y., Wang, N., Gao, S., Qiu, S., Wang, Z., Ding, J., Zhang, L., Wang, H., Wu, W., Wan, B., Yu, J., Fang, J., Yang, P., & Shao, Q. (2020). Identifying key genes and drug screening for preeclampsia based on gene expression profiles. Oncol. Lett., 20(2), 1585-1596. https://doi.org/10.3892/ol.2020.11721
Lorenzon-Ojea, A. R., Yung, H. W., Burton, G. J., & Bevilacqua, E. (2020). The potential contribution of stromal cell-derived factor 2 (SDF2) in endoplasmic reticulum stress response in severe preeclampsia and labor-onset. Biochimica et Biophysica Acta - Molecular Basis of Disease, 1866(2), 165386. https://doi.org/10.1016/j.bbadis.2019.01.012
Walter, P., & Ron, D. (2011). The unfolded protein response: From stress pathway to homeostatic regulation. Science, 334(6059), 1081-1086. https://doi.org/10.1126/science.1209038
Bastida-Ruiz, D., Aguilar, E., Ditisheim, A. S., Yart, L., & Cohen, M. (2017). Endoplasmic reticulum stress responses in placentation - A true balancing act. Placenta, 57, 163-169. doi: https://doi.org/10.1016/j.placenta.2017.07.004
Cheng, S. B., Nakashima, A., Huber, W. J., Davis, S., Banerjee, S., Huang, Z., Saito, S., Sadovsky, Y., & Sharma, S. (2019). Pyroptosis is a critical inflammatory pathway in the placenta from early onset preeclampsia and in human trophoblasts exposed to hypoxia and endoplasmic reticulum stressors. Cell Death. Dis., 10(12), 927. https://doi.org/10.1038/s41419-019-2162-4
Yung, H. W., Alnaes-Katjavivi, P., Jones, C. J. P., El-Bacha, T., Golic, M., Staff, A.-C., & Burton, G. J. (2016). Placental endoplasmic reticulum stress in gestational diabetes: The potential for therapeutic intervention with chemical chaperones and antioxidants. Diabetologia, 59(10), 2240-2250. https://doi.org/10.1007/s00125-016-4040-2
Matsumura, Y., Sakai, J., & Skach, W. R. (2013). Endoplasmic reticulum protein quality control is determined by cooperative interactions between Hsp/c70 protein and the CHIP E3 ligase. J. Biol. Chem., 288(43), 31069-31079. https://doi.org/10.1074/jbc.M113.479345
Torres-Salazar, Q., Martínez-López, Y., Reyes-Romero, M., Pérez-Morales, R., Sifuentes-Álvarez, A., & Salvador-Moysén, J. (2020). Differential methylation in promoter regions of the genes NR3C1 and HSP90AA1, involved in the regulation, and bioavailability of cortisol in leukocytes of women with preeclampsia. Front Med (Lausanne), 7, 206. https://doi.org/10.3389/fmed.2020.00206
Mahmood, F., Xu, R., Awan, M. U. N., Song, Y., Han, Q., Xia, X., & Zhang, J. (2021). PDIA3: Structure, functions and its potential role in viral infections. Biomed. Pharmacother., 143, 112110. https://doi.org/10.1016/j.biopha.2021.112110
Mo, H. Q., Tian, F. J., Ma, X. L., Zhang, Y. C., Zhang, C. X., Zeng, W. H., Zhang, Y., & Lin, Y. (2020). PDIA3 regulates trophoblast apoptosis and proliferation in preeclampsia via the MDM2/p53 pathway. Reproduction, 160(2), 293-305. https://doi.org/10.1530/rep-20-0156
Fekete, A., Vér, A., Bögi, K., Treszl, A., & Rigó, J. Jr. (2006). Is preeclampsia associated with higher frequency of HSP70 gene polymorphisms? Eur. J. Obstet. Gynecol. Reprod. Biol., 126(2), 197-200. https://doi.org/10.1016/j.ejogrb.2005.08.021
Eddy, A. C., Chapman, H., & George, E. M. (2019). Acute hypoxia and chronic ischemia induce differential total changes in placental epigenetic modifications. Reproductive Science, 26(6), 766-773. https://doi.org/10.1177/1933719118799193
Xie, Y., Hou, W., Song, X., Yu, Y., Huang, J., Sun, X., Kang, R., & Tang, D. (2016). Ferroptosis: Process and function. Cell Death Differ., 23(3), 369-379. https://doi.org/10.1038/cdd.2015.158
Lee, Y. S., Lee, D. H., Choudry, H. A., Bartlett, D. L., & Lee, Y. J. (2018). Ferroptosis-Induced endoplasmic reticulum stress: Cross-talk between ferroptosis and apoptosis. Mol. Cancer Res., 16(7), 1073-1076. https://doi.org/10.1158/1541-7786.Mcr-18-0055
Zhang, H., He, Y., Wang, J. X., Chen, M. H., Xu, J. J., Jiang, M. H., Zhang, Z., Zhang, L., Zhou, L., Lei, Y., Zhang, Y., & Huang, C. (2019). Redox signaling and unfolded protein response coordinate cell fate decisions under ER stress. Redox. Biol., 25, 101047. https://doi.org/10.1016/j.redox.2018.11.005
Galaris, D., Barbouti, A., & Pantopoulos, K. (2019). Iron homeostasis and oxidative stress: An intimate relationship. Biochimica et Biophysica Acta - Molecular Cell Research, 1866(12), 118535. https://doi.org/10.1016/j.bbamcr.2019.118535
Zhang, H., He, Y., Wang, J. X., Chen, M. H., Xu, J. J., Jiang, M. H., Feng, Y.-L., & Gu, Y.-F. (2020). miR-30-5p-mediated ferroptosis of trophoblasts is implicated in the pathogenesis of preeclampsia. Redox. Biol., 29, 101402. https://doi.org/10.1016/j.redox.2019.101402
Yang, N., Wang, Q., Ding, B., Gong, Y., Wu, Y., Sun, J., Wang, X., Liu, L., Zhang, F., Du, D., & Li, X. (2022). Expression profiles and functions of ferroptosis-related genes in the placental tissue samples of early- and late-onset preeclampsia patients. BMC Pregnancy Childbirth, 22(1), 87. https://doi.org/10.1186/s12884-022-04423-6
Han, D., Jiang, L., Gu, X., Huang, S., Pang, J., Wu, Y., Yin, J., & Wang, J. (2020). SIRT3 deficiency is resistant to autophagy-dependent ferroptosis by inhibiting the AMPK/mTOR pathway and promoting GPX4 levels. J. Cell. Physiol., 235(11), 8839-8851. https://doi.org/10.1002/jcp.29727
Yang, Y., Luo, M., Zhang, K., Zhang, J., Gao, T., Connell, D. O., Yao, F., Mu, C., Cai, B., Shang, Y., & Chen, W. (2020). Nedd4 ubiquitylates VDAC2/3 to suppress erastin-induced ferroptosis in melanoma. Nat. Commun., 11(1), 433. https://doi.org/10.1038/s41467-020-14324-x
Chen, Y., Liu, Y., Lan, T., Qin, W., Zhu, Y., Qin, K., Gao, J., Wang, H., Hou, X., Chen, N., Friedmann Angeli, J. P., Conrad, M., & Wang, C. (2018). Quantitative profiling of protein carbonylations in ferroptosis by an aniline-derived probe. J. Am. Chem. Soc., 140(13), 4712-4720. https://doi.org/10.1021/jacs.8b01462
Chen, H., Li, J., Cai, S., Tang, S., Zeng, S., Chu, C., Hocher, C. -. F., Rösing, B., Krämer, B. K., Hu, L., Lin, G., Gong, F., & Hocher, B. (2022). Blastocyst transfer: A risk factor for gestational diabetes mellitus in women undergoing in vitro fertilization. J. Clin. Endocrinol. Metab., 107(1), e143-e152. https://doi.org/10.1210/clinem/dgab594