Placental proteome in late‑onset of fetal growth restriction
- Authors:
- Tomasz Gęca
- Aleksandra Stupak
- Robert Nawrot
- Anna Goździcka‑Józefiak
- Anna Kwaśniewska
- Wojciech Kwaśniewski
-
Affiliations: Department of Obstetrics and Pathology of Pregnancy, Medical University of Lublin, 20‑081 Lublin, Poland, Department of Molecular Virology, Institute of Experimental Biology, Adam Mickiewicz University in Poznań, 61‑614 Poznan, Poland, Department of Gynecologic Oncology and Gynecology, Medical University of Lublin, 20‑081 Lublin, Poland - Published online on: October 14, 2022 https://doi.org/10.3892/mmr.2022.12872
- Article Number: 356
-
Copyright: © Gęca et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
|
Zhang S, Lin H, Kong S, Wang S, Wang H, Wang H and Armant DR: Physiological and molecular determinants of embryo implantation. Mol Aspects Med. 34:939–980. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Zhan X, Long Y and Lu M: Exploration of variations in proteome and metabolome for predictive diagnostics and personalized treatment algorithms: Innovative approach and examples for potential clinical application. J Proteomics. 188:30–40. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Handelman SK, Romero R, Tarca AL, Pacora P, Ingram B, Maymon E, Chaiworapongsa T, Hassan SS and Erez O: The plasma metabolome of women in early pregnancy differs from that of non-pregnant women. PLoS One. 14:e02246822019. View Article : Google Scholar : PubMed/NCBI | |
|
Lain KY and Catalano PM: Metabolic changes in pregnancy. Clin Obstet Gynecol. 50:938–948. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Zeng Z, Liu F and Li S: Metabolic adaptations in pregnancy: A review. Ann Nutr Metab. 70:59–65. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Herrera E and Desoye G: Maternal and fetal lipid metabolism under normal and gestational diabetic conditions. Horm Mol Biol Clin Investig. 26:109–127. 2016.PubMed/NCBI | |
|
McLachlan KA, O'Neal D, Jenkins A and Alford FP: Do adiponectin, TNFα, leptin and CRP relate to insulin resistance in pregnancy? Studies in women with and without gestational diabetes, during and after pregnancy. Diabet Metab Res Rev. 22:131–138. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Catalano PM, Roman-Drago NM, Amini SB and Sims EAH: Longitudinal changes in body composition and energy balance in lean women with normal and abnormal glucose tolerance during pregnancy. Am J Obstetr Gynecol. 179:156. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Jauniaux E, Hempstock J, Teng C, Battaglia FC and Burton GJ: Polyol concentrations in the fluid compartments of the human concentrations in the fluid compartments of the human conceptus during the first trimester of pregnancy: Maintenance of redox potential in a low oxygen environment. J Clin Endocrinol Metab. 90:1171–1175. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Murgia F, Iuculano A, Peddes C, Santoru ML, Tronci L, Deiana M, Atzori L and Monni G: Metabolic fingerprinting of chorionic villous samples in normal pregnancy and chromosomal disorders. Prenat Diagn. 39:848–858. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Jauniaux E, Cindrova-Davies T, Johns J, Dunster C, Hempstock J, Kelly FJ and Burton GJ: Distribution and transfer pathways of antioxidant molecules inside the first trimester human gestational sac. J Clin Endocrinol Metab. 89:1452–1458. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Burton GJ, Watson AL, Hempstock J, Skepper JN and Jauniaux E: Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J Clin Endocrinol Metab. 87:2954–2959. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN and Burton GJ: Onset of maternal arterial blood flow and placental oxidative stress: A possible factor in human early pregnancy failure. Am J Pathol. 157:2111–2122. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Burton GJ and Jauniaux E: Placental oxidative stress: From miscarriage to preeclampsia. Reprod Sci. 11:342–352. 2004. | |
|
King VJ, Bennet L, Stone PR, Clark A, Gunn AJ and Dhillon SK: Fetal growth restriction and stillbirth: Biomarkers for identifying at risk fetuses. Front Physiol. 13:9597502022. View Article : Google Scholar : PubMed/NCBI | |
|
Nardozza LM, Caetano AC, Zamarian AC, Mazzola JB, Silva CP, Marçal VM, Lobo TF, Peixoto AB and Araujo Júnior E: Fetal growth restriction: Current knowledge. Arch Gynecol Obstet. 295:1061–1077. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Visentin S, Grumolato F, Nardelli GB, Di Camillo B, Grisan E and Cosmi E: Early origins of adult disease: Low birth weight and vascular remodeling. Atherosclerosis. 237:391–399. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Yzydorczyk C, Armengaud JB, Peyter AC, Chehade H, Cachat F, Juvet C, Siddeek B, Simoncini S, Sabatier F, Dignat-George F, et al: Endothelial dysfunction in individuals born after fetal growth restriction: Cardiovascular and renal consequences and preventive approaches. J Dev Orig Health Dis. 8:448–464. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Kalanithi LE, Illuzzi JL, Nossov VB, Frisbaek Y, Abdel-Razeq S, Copel JA and Norwitz ER: Intrauterine growth restriction and placental location. J Ultrasound Med. 26:1481–1489. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Unterscheider J, Daly S, Geary MP, Kennelly MM, McAuliffe FM, O'Donoghue K, Hunter A, Morrison JJ, Burke G, Dicker P, et al: Optimizing the definition of intrauterine growth restriction: The multicenter prospective PORTO Study. Am J Obstet Gynecol. 208:290.e1–e6. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Gordijn SJ, Beune IM, Thilaganathan B, Papageorghiou A, Baschat AA, Baker PN, Silver RM, Wynia K and Ganzevoort W: Consensus definition of fetal growth restriction: A Delphi procedure. Ultrasound Obstet Gynecol. 48:333–339. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Baschat AA: Late onset FGR is generally linked with milder placental insufficiency than early-onset FGR, but the risk of stillbirth is high due to wors fetal hemodynamic adaptation. Planning management and delivery of the growth-restricted fetus. Best Pract Res Clin Obstet Gynaecol. 49:53–65. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zeitlin J, Ancel PY, Saurel-Cubizolles MJ and Papiernik E: The relationship between intrauterine growth restriction and preterm delivery: An empirical approach using data from a European case-control study. BJOG. 107:750–758. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Parker SE and Werler MM: Epidemiology of ischemic placental disease: A focus on preterm gestations. Semin Perinatol. 38:133–138. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Figueras F and Gratacós E: Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther. 36:86–98. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Monteith C, Flood K, Pinnamaneni R, Levine TA, Alderdice FA, Unterscheider J, McAuliffe FM, Dicker P, Tully EC, Malone FD and Foran A: An abnormal cerebroplacental ratio (CPR) is predictive of early childhood delayed neurodevelopment in the setting of fetal growth restriction. Am J Obstet Gynecol. 221:273.e1–273.e9. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Khalil A, Morales-Roselló J, Townsend R, Morlando M, Papageorghiou A, Bhide A and Thilaganathan B: Value of third-trimester cerebroplacental ratio and uterine artery Doppler indices as predictors of stillbirth and perinatal loss. Ultrasound Obstet Gynecol. 47:74–80. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Mecacci F, Avagliano L, Lisi S, Clemenza S, Serena C, Vannuccini S, Rambaldi MP, Simeone S, Ottanelli S and Petragli F: Fetal growth restriction: Does an integrated maternal hemodynamic-placental model fit better? Rep Sci. 28:2422–2435. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Leite DFB, Morillon AC, Melo Júnior EF, Souza RT, McCarthy FP, Khashan A, Baker P, Kenny LC and Cecatti JG: Examining the predictive accuracy of metabolomics for small-for-gestational-age babies: A systematic review. BMJ Open. 9:e0312382019. View Article : Google Scholar : PubMed/NCBI | |
|
Law KP, Han TL, Tong C and Baker PN: Mass spectrometry-based proteomics for pre-eclampsia and preterm birth. Int J Mol Sci. 16:10952–10985. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Nguyen TPH, Patrick CJ, Parry LJ and Familari M: Using proteomics to advance the search for potential biomarkers for preeclampsia: A systematic review and meta-analysis. PLoS One. 14:e02146712019. View Article : Google Scholar : PubMed/NCBI | |
|
Dahabiyeh LA: The discovery of protein biomarkers in pre-eclampsia: The promising role of mass spectrometry. Biomarkers. 23:609–621. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Paules C, Youssef L, Miranda J, Crovetto F, Estanyol JM, Fernandez G, Crispi F and Gratacós E: Maternal proteomic profiling reveals alterations in lipid metabolism in late-onset fetal growth restriction. Sci Rep. 10:210332020. View Article : Google Scholar : PubMed/NCBI | |
|
Conrad MS, Gardner ML, Miguel C, Freitas MA, Rood KM and Ma'ayeh M: Proteomic analysis of the umbilical cord in fetal growth restriction and preeclampsia. PLoS One. 17:e02620412022. View Article : Google Scholar : PubMed/NCBI | |
|
Hadlock FP, Harrist RB, Sharman RS, Deter RL and Park SK: Estimation of fetal weight with the use of head, body and femur measurements-a prospective study. Am J Obstet Gynecol. 151:333–337. 1985. View Article : Google Scholar : PubMed/NCBI | |
|
Ebbing C, Rasmussen S and Kiserud T: Middle cerebral artery blood flow velocities and pulsatility index and the cerebroplacental pulsatility ratio: Longitudinal reference ranges and terms for serial measurements. Ultrasound Obstet Gynecol. 30:287–296. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Jugović D, Tumbri J, Medić M, Jukić MK, Kurjak A, Arbeille P and Salihagić-Kadić A: New Doppler index for prediction of perinatal brain damage in growth-restricted and hypoxic fetuses. Ultrasound Obstet Gynecol. 30:303–311. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680–685. 1970. View Article : Google Scholar : PubMed/NCBI | |
|
Neuhoff V, Arold N, Taube D and Ehrhardt W: Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with a clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R250. Electrophoresis. 9:255–262. 1988. View Article : Google Scholar : PubMed/NCBI | |
|
Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J and Mann M: Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics. 4:1265–1272. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Bahado-Singh RO, Turkoglu O, Yilmaz A, Kumar P, Zeb A, Konda S, Sherman E, Kirma J, Allos M, Odibo A, et al: Metabolomic identification of placental alterations in fetal growth restriction. J Mater Fetal Neonatal Med. 35:447–456. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Youssef L, Simões RV, Miranda J, García-Martín ML, Paules C, Crovetto F, Amigó N, Cañellas N, Gratacos E and Crispi F: Paired maternal and fetal metabolomics reveal a differential fingerprint in preeclampsia versus fetal growth restriction. Sci Rep. 11:144222021. View Article : Google Scholar : PubMed/NCBI | |
|
Heazell AE, Brown M, Dunn WB, Worton SA, Crocker IP, Baker PN and Kell DB: Analysis of the metabolic footprint and tissue metabolome of placental villous explants cultured at different oxygen tensions reveals novel redox biomarkers. Placenta. 29:691–698. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Arimura Y, Ikura M, Fujita R, Noda M, Kobayashi W, Horikoshi N, Sun J, Shi L and Kusakabe M: Cancer-associated mutations of histones H2B, H3.1 and H2A.Z.1 affect the structure and stability of the nucleosome. Nucleic Acids Res. 46:10007–10018. 2018.PubMed/NCBI | |
|
Patel D, McAllister SL and Teckman JH: Alpha-1 antitrypsin deficiency liver disease. Transl Gastroenterol Hepatol. 6:232021. View Article : Google Scholar : PubMed/NCBI | |
|
Xi Y, Rong Y and Wang Y: Roles of Annexin A protein family in autophagy regulation and therapy. Biomed Pharmacother. 130:1105912020. View Article : Google Scholar : PubMed/NCBI | |
|
D'Acquisto F, Perretti M and Flower RJ: Annexin-A1: A pivotal regulator of the innate and adaptive immune systems. J Pharmacol. 155:152–169. 2008. | |
|
Peng W, Liu Y, Qi H and Li Q: Alpha-actinin-4 is essential for maintaining normal trophoblast proliferation and differentiation during early pregnancy. Rep Biol Endoc. 19:482021. View Article : Google Scholar | |
|
Mangaraj M, Nanda R and Panda S: Apolipoprotein A-I: A molecule of diverse function. Indian J Clin Biochem. 31:253–259. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Pennington KL, Chan TY, Torres MP and Andersen IJ: The dynamic and stress-adaptive signaling hub of 14-3-3: Emerging mechanisms of regulation and context-dependent protein-protein interactions. Oncogene. 37:5587–5604. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Wierenga RK, Kapetaniou EG and Venkatesan R: Triosephosphate isomerase: A highly evolved biocatalyst. Cell Mol Life Sci. 67:3961–3982. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Fu W, Wang W, Hao J, Zhu X and Sun M: Purification and characterization of catalase from marine bacterium Acinetobacter sp. YS0810. Biomed Res Int. 2014:4096262014. View Article : Google Scholar : PubMed/NCBI | |
|
Poillerat V, Gentinetta T, Leon J, Wassmer A, Edler M, Torset C, Luo D, Tuffin G and Roumenina LT: Hemopexin as an inhibitor of hemolysis-induced complement activation. Front Immunol. 11:16842020. View Article : Google Scholar : PubMed/NCBI | |
|
Varricchio L, Falchi M, Dall'Ora M, De Benediyyis C, Ruggeri A, Uversky VN and Migliaccio AR: Calreticulin: Challenges posed by the intrinsically disordered nature of calreticulin to the study of its function. Front Cell Dev Biol. 6:962017. View Article : Google Scholar : PubMed/NCBI | |
|
Khan HA and Mutus B: Protein disulfide isomerase a multifunctional protein with multiple physiological roles. Front Chem. 2:702014.PubMed/NCBI | |
|
Karvar S, Ansa-Addo SA, Suda J, Singh S, Zhu L, Li Z and Dony DC: Moesin, an Ezrin/Radixin/Moesin family member, regulates hepatic fibrosis. Hepatology. 72:1073–1084. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Sizemore ST, Zhang M, Cho JH, Sizemore GM, Hurwitz B, Kaur B, Lehman NL, Ostrowski MC, Robe PA, Miao W, et al: Pyruvate kinase M2 regulates homologous recombinationmediated DNA double-strand break repair. Cell Res. 28:1090–1102. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Wilkinson HC and Dalby PA: The Two-species model of transketolase explains donor substrate-binding, inhibition and heat-activation. Sci Rep. 10:41482020. View Article : Google Scholar : PubMed/NCBI | |
|
Bernard JY, Tint MT, Aris IM, Chenc LW, Quaha PL, Tand KH, Yeo GS, Fortier MV, Yap F, Shek L, et al: Maternal plasma phosphatidylcholine polyunsaturated fatty acids during pregnancy and offspring growth and adiposity. Prostaglandins Leukot Essent Fatty Acids. 121:21–29. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Visentin S, Crotti S, Donazzolo E, D'Aronco S, Nitti D, Cosmi E and Agostini M: Medium chain fatty acids in intrauterine growth restricted and small for gestational age pregnancies. Metabolomics. 13:542017. View Article : Google Scholar | |
|
Clinton CM, Bain JR, Muehlbauer MJ, Li YY, Li L, O'Neal SK and Ferguson KK: Non-targeted urinary metabolomics in pregnancy and associations with fetal growth restriction. Sci Rep. 10:53072020. View Article : Google Scholar : PubMed/NCBI | |
|
Dessì A, Atzori L, Noto A, Visser GH, Gazzolo D, Zanardo V, Barberini L, Puddu M, Ottonello G, Atzei A, et al: Metabolomics in newborns with intrauterine growth retardation (IUGR): Urine reveals markers of metabolic syndrome. J Mater Fetal Neonat Med. 24 (Suppl 2):S35–S39. 2011. View Article : Google Scholar | |
|
Raff H, Bruder ED, Jankowski BM and Goodfriend TL: Neonatal hypoxic hyperlipidemia in the rat: Effects on aldosterone and corticosterone synthesis in vitro. Am J Physiol Regul Integr Comp Physiol. 278:R663–R668. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Jiang F, Zhang Y and Dusting GJ: NADPH oxidase-mediated redox signaling: Roles in cellular stress response, stress tolerance and tissue repair. Pharmacol Rev. 63:218–242. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Sena LA and Chandel NS: Physiological roles of mitochondrial reactive oxygen species. Mol Cell. 48:158–167. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Schieber M and Chandel NS: ROS function in redox signaling and oxidative stress. Curr Biol. 24:R453–R462. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Gretes MC, Poole LB and Karplus PA: Peroxiredoxins in parasites. Antioxid Redox Signal. 17:608–633. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Sun HN, Kim SU, Huang SM, Kim JM, Park YH, Kim SH, Yang HY, Chung KJ, Lee TH, Choi HS, et al: Microglial peroxiredoxin V acts as an inducible anti-inflammatory antioxidant through cooperation with redox signaling cascades. J Neurochem. 114:39–50. 2010.PubMed/NCBI | |
|
Diet A, Abbas K, Bouton C, Guillon B, Tomasello F, Fourquet S, Toledano MB and Drapier JC: Regulation of peroxiredoxins by nitric oxide in immunostimulated macrophages. J Biol Chem. 282:36199–36205. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Vinchi F, Costa da Silva M, Ingoglia G, Petrillo S, Brinkman N, Zuercher A, Cerwenka A, Tolosano E and Muckenthaler MU: Hemopexin therapy reverts heme-induced pro-inflammatory phenotypic switching of macrophages in a mouse model of sickle cell disease. Blood. 127:473–486. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Li R, Saleem S, Zhen G, Cao W, Zhuang H, Lee J, Smith A, Altruda F, Tolosano E and Doré S: Heme-hemopexin complex attenuates neuronal cell death and stroke damage. J Cereb Blood Flow Metab. 29:953–964. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Yang Y, Dong B, Lu J, Wang G and Yu Y: Hemopexin reduces blood-brain barrier injury and protects synaptic plasticity in cerebral ischemic rats by promoting EPCs through the HO-1 pathway. Brain Res. 1699:177–185. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Belkacemi L, Bédard I, Simoneau L and Lafond J: Calcium channels, transporters and exchangers in placenta: A review. Cell Calcium. 37:1–8. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Michalak M, Groenendyk J, Szabo E, Gold LI and Opas M: Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J. 417:651–666. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Yamamoto M, Ikezaki M, Toujima S, Iwahashi N, Mizoguchi M, Nanjo S, Minami S, Ihara Y and Ino K: Calreticulin is involved in invasion of human extravillous trophoblasts through functional regulation of integrin beta1. Endocrinology. 158:3874–3889. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Iwahashi N, Ikezaki M, Matsuzaki I, Yamamoto M, Toujima S, Murata SI, Ihara Y and Ino K: Calreticulin regulates syncytialization through control of the synthesis and transportation of E-cadherin in BeWo cells. Endocrinology. 160:359–374. 2019.PubMed/NCBI | |
|
Gold LI, Eggleton P, Sweetwyne MT, Van Duyn LB, Greives MR, Naylor SM and Murphy-Ullrich JE: Calreticulin: Non-endoplasmic reticulum functions in physiology and disease. FASEB J. 24:665–683. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Shi Z, Hou W, Hua X, Zhang X, Liu X and Wang X and Wang X: Overexpression of calreticulin in pre-eclamptic placentas: Effect on apoptosis, cell invasion and severity of pre-eclampsia. Cell Biochem Biophys. 63:183–189. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Gu VY, Wong MH, Stevenson JL, Crawford KE, Brennecke SP and Gude NM: Calreticulin in human pregnancy and pre-eclampsia. Mol Hum Reprod. 14:309–315. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Iwahashi N, Ikezaki M, Nishitsuji K, Yamamoto M, Matsuzaki I, Kato N, Takaoka N, Taniguchi M, Murata SI, Ino K and Ihara Y: Extracellularly released calreticulin induced by endoplasmic reticulum stress impairs syncytialization of cytotrophoblast model BeWo cells. Cells. 10:13052021. View Article : Google Scholar : PubMed/NCBI | |
|
Mo HQ, Tian FJ, Ma XL, Zhang YC, Zhang CX, Zeng WH, Zhang Y and Lin Y: PDIA3 regulates trophoblast apoptosis and proliferation in preeclampsia via the MDM2/p53 pathway. Reproduction. 160:293–305. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Foote M and Zhou Y: 14-3-3 proteins in neurological disorders. Int J Biochem Mol Biol. 3:152–164. 2012.PubMed/NCBI | |
|
Muslin AJ and Xing H: 14-3-3 proteins: Regulation of subcellular localization by molecular interference. Cell Signal. 12:703–709. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Mackintosh C: Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J. 381:329–342. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Kaplan A, Morquette B, Kroner A, Leong SY, Madwar C, Sanz R, Benerjee SL, Antel J, Bisson N, David S and Fournier AE: Small-molecule stabilization of 14-3-3 Protein-protein interactions stimulates axon regeneration. Neuron. 93:1082–1093.e5. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Kwon OK, Lee W, Kim SJ, Lee YM, Lee JY, Kim JY, Bae JS and Lee S: In-depth proteomics approach of secretome to identify novel biomarker for sepsis in LPS-stimulated endothelial cells. Electrophoresis. 36:2851–2858. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Lee W, Kwon OK, Han MS, Lee YM, Kim SW, Kim KM, Lee T, Lee S and Bae JS: Role of moesin in HMGB1-stimulated severe inflammatory responses. Thromb Haemost. 114:350–363. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Y, Wang J, Zhang L, Zhu J, Zeng Y and Huang JA: Moesin is a novel biomarker of endothelial injury in sepsis. J Immunol Res. 2021:66956792021. View Article : Google Scholar : PubMed/NCBI | |
|
Satooka H, Matsui M, Ichioka S, Nakamura Y and Hirata T: The ERM protein moesin regulates natural killer cell homeostasis in vivo. Cell Immunol. 371:1044562022. View Article : Google Scholar : PubMed/NCBI | |
|
Hasan D, Gamen E, Tarboush NA, Ismail Y, Pak O and Azab B: PKM2 and HIF1α regulation in prostate cancer cell lines. PLoS One. 13:e02037452018. View Article : Google Scholar : PubMed/NCBI | |
|
Li Z, Yang P and Li Z: The multifaceted regulation and functions of PKM2 in tumor progression. Biochim Biophys Acta Rev Cancer. 1846:285–296. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Li L, Zhang Y, Qiao J, Yang JJ and Liu ZR: Pyruvate kinase M2 in blood circulation facilitates tumor growth by promoting angiogenesis. J Biol Chem. 289:25812–25821. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Xu Q, Liu LZ, Yin Y, He J, Li Q, Qian X, You Y, Lu Z, Peiper SC, Shu Y and Jiang BH: Regulatory circuit of PKM2/NFκB/miR-148a/152-modulated tumor angiogenesis and cancer progression. Oncogene. 34:5482–5493. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Azoitei N, Becher A, Steinestel K, Rouhi A, Diepold K, Genze F, Simmet T and Seufferlein T: PKM2 promotes tumor angiogenesis by regulating HIF-1α through NF-κB activation. Mol Cancer. 15:32016. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Y, Zhang T, Zeng S, Xu R, Jin K, Coorey NJ, Wang Y, Wang K, Lee SR, Yam M, et al: Transketolase in human Müller cells is critical to resist light stress through the pentose phosphate and NRF2 pathways. Redox Biol. 54:1023792022. View Article : Google Scholar : PubMed/NCBI | |
|
Jiang P, Du W and Yang X: A critical role of glucose-6-phosphate dehydrogenase in TAp73-mediated cell proliferation. Cell Cycle. 12:3720–3726. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Krockenberger M, Engel JB, Schmidt M, Kohrenhagen N, Häusler SF, Dombrowski Y, Kapp M, Dietl J and Honig A: Expression of transketolase-like 1 protein (TKTL1) in human endometrial cancer. Anticancer Res. 30:1653–1659. 2010.PubMed/NCBI | |
|
Staiger WI, Coy JF, Grobholz R, Hofheinz RD, Lukan N, Post S, Schwarzbach MH and Willeke F: Expression of the mutated transketolase TKTL1, a molecular marker in gastric cancer. Oncol Rep. 16:657–661. 2006.PubMed/NCBI | |
|
Hertl M and Cosimi AB: Liver transplantation for malignancy. Oncologist. 10:269–281. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Sun J, Hoshino H, Takaku K, Nakajima O, Muto A, Suzuki H, Tashiro S, Takahashi S, Shibahara S, Alam J, et al: Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J. 21:5216–5224. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Mitsuishi Y, Taguchi K, Kawatani Y, Shibata T, Nukiwa T, Aburatani H, Yamamoto M and Motohashi H: Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell. 22:66–79. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Sjoblom B, Salmazo A and Djinovic-Carugo K: Alpha-actinin structure and regulation. Cell Mol Life Sci. 65:2688–2701. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Mills M, Yang N, Weinberger R, Vander Woude DL, Beggs AH, Easteal S and North K: Differential expression of the actin-binding proteins, alpha-actinin-2 and −3, in different species: Implications for the evolution of functional redundancy. Hum Mol Genet. 10:1335–1346. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Hamill KJ, Hopkinson SB, Skalli O and Jones JC: Actinin-4 in keratinocytes regulates motility via an effect on lamellipodia stability and matrix adhesions. FASEB J. 27:546–556. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Bridger PS, Haupt S, Leiser R, Johnson GA, Burghardt RC, Tinneberg HR and Pfarrer C: Integrin activation in bovine placentomes and in caruncular epithelial cells isolated from pregnant cows. Biol Reprod. 79:274–282. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang YY, Tabataba H, Liu XY, Wang JY, Yan XG, Farrelly M, Jiang CC, Guo ST, Liu T, Kao HY, et al: ACTN4 regulates the stability of RIPK1 in melanoma. Oncogene. 37:4033–4045. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Pollheimer J, Vondra S, Baltayeva J, Beristain AG and Knöfler M: Regulation of placental extravillous trophoblasts by the maternal uterine environment. Front Immunol. 9:25972018. View Article : Google Scholar : PubMed/NCBI | |
|
Kennedy DJ, Fan Y, Wu Y, Pepoy M, Hazen SL and Tang WH: Plasma ceruloplasmin, a regulator of nitric oxide activity and incident cardiovascular risk in patients with CKD. Clin J Am Soc Nephrol. 9:462–467. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Göçmen AY, Sahin E, Semiz E and Gümuşlü S: Is elevated serum ceruloplasmin level associated with increased risk of coronary artery disease? Can J Cardiol. 24:209–212. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Ziakas A, Gavrilidis S, Souliou E, Giannoglou G, Stiliadis I, Karvounis H, Efthimiadis G, Mochlas S, Vayona MA, Hatzitolios A, et al: Ceruloplasmin is a better predictor of the long-term prognosis compared with fibrinogen, CRP, and IL-6 in patients with severe unstable angina. Angiology. 60:50–59. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Hammadah M, Fan Y, Wu Y, Hazen SL and Tang WH: Prognostic value of elevated serum ceruloplasmin levels in patients with heart failure. J Card Fail. 20:946–952. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Guller S, Buhimschi CS, Ma YY, Huang ST, Yang L, Kuczynski E, Zambrano E, Lockwood CJ and Buhimschi IA: Placental expression of ceruloplasmin in pregnancies complicated by severe preeclampsia. Lab Invest. 88:1057–1067. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Bellos I, Papantoniou N and Pergialiotis V: Serum ceruloplasmin levels in preeclampsia: A meta-analysis. J Matern Fetal Neonatal Med. 31:2342–2348. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Surekha MV, Sujatha T, Gadhiraju S, Kumar PU, Kotturu SK, Sharada K and Bhaskar V: Impact of maternal iron deficiency anaemia on the expression of the newly discovered multi-copper ferroxidase, Zyklopen, in term placentas. J Obstet Gynaecol. 42:74–82. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Ozgu-Erdinc AS, Cavkaytar S, Aktulay A, Buyukkagnici U, Erkaya S and Danisman N: Mid-trimester maternal serum and amniotic fluid biomarkers for the prediction of preterm delivery and intrauterine growth retardation. J Obstet Gynaecol Res. 40:1540–1546. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Pogorelova TN, Linde VA, Gunko VO and Selyutina SN: The imbalance of metal-containing proteins and free metal ions in the amniotic fluid during fetal growth. Biomed Khim. 62:69–72. 2016.(In Russian). View Article : Google Scholar : PubMed/NCBI | |
|
Ayala R, Shu T and Tsai LH: Trekking across the brain: The journey of neuronal migration. Cell. 128:29–43. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Tischfield MA and Engle EC: Distinct alpha- and beta-tubulin isotypes are required for the positioning, differentiation and survival of neurons: New support for the ‘multi-tubulin’ hypothesis. Biosci Rep. 30:319–330. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Bahi-Buisson N, Poirier K, Fourniol F, Saillour Y, Valence S, Lebrun N, Hully M, Bianco CF, Boddaert N, Elie C, et al: The wide spectrum of tubulinopathies: What are the key features for the diagnosis? Brain. 137:1676–1700. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Hebebrand M, Hüffmeier U, Trollmann R, Hehr U, Uebe S, Ekici AB, Kraus C, Krumbiegel M, Reis A, Thiel CT and Popp B: The mutational and phenotypic spectrum of TUBA1A-associated tubulinopathy. Orphanet J Rare Dis. 14:382019. View Article : Google Scholar : PubMed/NCBI | |
|
Romaniello R, Zucca C, Arrigoni F, Bonanni P, Panzeri E, Bassi MT and Borgatti R: Epilepsy in tubulinopathy: Personal series and literature review. Cells. 8:6692019. View Article : Google Scholar : PubMed/NCBI | |
|
Wang X, Zhang J, Zhou L, Xu B, Ren X, He K, Nie L, Li X, Liu J, Yang X and Yuan J: Long-term iron exposure causes widespread molecular alterations associated with memory impairment in mice. Food Chem Toxicol. 130:242–252. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Monceau V, Belikova Y, Kratassiouk G, Charue D, Camors E, Communal C, Trouvé P, Russo-Marie F and Charlemagne D: Externalization of endogenous annexin A5 participates in apoptosis of rat cardiomyocytes. Cardiovass Res. 64:496–506. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Li A, Su X, Tian Y, Song G, Zan L and Wang H: Effect of actin alpha cardiac Muscle 1 on the proliferation and differentiation of bovine myoblasts and preadipocytes. Animals (Basel). 11:34682021. View Article : Google Scholar : PubMed/NCBI | |
|
Yuan SM and Wu N: Aortic α-smooth muscle actin expressions in aortic disorders and coronary artery disease: An immunohistochemical study. Anatol J Cardiol. 19:11–16. 2018.PubMed/NCBI | |
|
Jonckheere A, Smeitink JM and Rodenburg RJT: Mitochondrial ATP synthase: Architecture, function and pathology. J Inherit Metab Dis. 35:211–225. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Männik J, Vaas P, Rull K, Teesalu P and Laan M: Differential placental expression profile of human Growth Hormone/Chorionic Somatomammotropin genes in pregnancies with pre-eclampsia and gestational diabetes mellitus. Mol Cell Endocrinol. 355:180–187. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Bays JL and DeMali KA: Vinculin in cell-cell and cell-matrix adhesions. Cell Mol Life Sci. 74:2999–3009. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Patino MG, Neiders MS, Mirdza E, Sebastiano A, Noble B and Cohen RE: Collagen: An overview. Implant Dent. 11:280–285. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Sudo H, Tsuji AB, Sugyo A, Abe M, Hino O and Saga T: AHNAK is highly expressed and plays a key role in cell migration and invasion in mesothelioma. Inter J Oncol. 20:530–538. 2013. | |
|
Sun H, Zhao A, Li M, Dong H, Sun Y, Zhang X, Zhu Q, Bukhari AA, Cao CH, Su D, et al: Interaction of calcium binding protein S100A16 with myosin-9 promotes cytoskeleton reorganization in renal tubulointerstitial fibrosis. Cell Death Dis. 11:1462020. View Article : Google Scholar : PubMed/NCBI | |
|
Su W, Mruk DD and Cheng CY: Filamin A: A regulator of blood-testis barrier assembly during post-natal development. Spermatogenesis. 2:73–78. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Burrudge K: Talin: A protein designed for mechanotransduction. Emerg Top Life Sci. 2:673–675. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Duan T, Fan K, Chen S, Yao O, Zeng R, Hong Z, Peng L, Shao Y and Yao B: Role of peroxiredoxin 2 in H2O2 induced oxidative stress of primary Leydig cells. Molec Med Rep. 13:4807–4813. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Stockley RA: The multiple facets of alpha-1-antitrypsin. Ann Transl Med. 3:1302015.PubMed/NCBI | |
|
Feng D, Notbohm J, Benjamin A, He S, Wang M, Ang LH, Bantawa M, Bouzid M, Del Gado E, Krishnan R and Pollak MR: Disease-causing mutation in α-actinin-4 promotes podocyte detachment through maladaptation to periodic stretch. Proc Natl Acad Sci USA. 115:1517–1522. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zanardi A, Conti MA, Cremones P, D'Adamo E, Gilberti P, Apostoli C, Cannistraci A, Piperno S, David S and Alessio M: Ceruloplasmin replacement therapy ameliorates neurological symptoms in a preclinical model of aceruloplasminemia. EMBO Mol Med. 10:91–106. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Lehmann SG, Bourgoin-Voillard S, Seve M and Rachidi W: Tubulin beta-3 chain as a new candidate protein biomarker of human skin aging: A preliminary study. Oxid Med Cell Longev. 2017:51403602017. View Article : Google Scholar : PubMed/NCBI |
