Platelets in fetal growth restriction: role of reactive oxygen species, oxygen metabolism, and aggregation.
Abstract
Fetal growth restriction (FGR) is mainly caused by failure of the uteroplacental unit. The
exact pathogenesis remains unclear. The cause is thought to be related to abnormal platelet activation,
which may result in microthrombus formation in the small vessels of the placenta. Reactive oxygen
species (ROS) may initiate the pathological process of platelet activation. This study aimed to evaluate
selected platelet parameters in pregnancy complicated by FGR and relate them to the severity of
hemodynamic abnormalities. A total of 135 women (pregnant with FGR, with an uncomplicated
pregnancy, and non-pregnant) were enrolled to study different platelet parameters: count (PLT), mean
volume (MPV), ROS levels, intracellular oxygen level, oxygen consumption, and aggregation indices.
No abnormalities in PLT and MPV were found in the FGR group, although it revealed increased ROS
levels in platelets, lower platelet oxygen consumption, and intraplatelet deprivation. Aggregation
parameters were similar as in uncomplicated pregnancy. No significant relationships were observed
between hemodynamic abnormalities and the studied parameters. Platelets in pregnancies compli-
cated by FGR may reveal an impaired oxidative metabolism, which may, in turn, lead to oxidative
stress and, consequently, to an impaired platelet function. This study adds to the understanding of
the role of platelets in the etiology of FGR.
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Cells
no. 11,
pages 1 - 13,
ISSN: 2073-4409 - Publication year:
- 2022
- DOI:
- Digital Object Identifier (open in new tab) 10.3390/cells11040724
- Bibliography: test
-
- Gagnon, R. Placental Insufficiency and Its Consequences. Eur. J. Obstet. Gynecol. Reprod. Biol. 2003, 11 (Suppl. S1), 99-107. [CrossRef] open in new tab
- Figueras, F.; Gratacós, E. Update on the Diagnosis and Classification of Fetal Growth Restriction and Proposal of a Stage-Based Management Protocol. Fetal Diagn. Ther. 2014, 36, 86-98. [CrossRef] [PubMed] open in new tab
- American College of Obstetricians and Gynecologists' Committee on Practice Bulletins-Obstetrics and the Society forMaternal- FetalMedicin. ACOG Practice Bulletin No. 204: Fetal Growth Restriction. Obstet. Gynecol. 2019, 133, e97-e109. [CrossRef] [PubMed] open in new tab
- Salafia, C.M.; Minior, V.K.; Pezzullo, J.C.; Popek, E.J.; Rosenkrantz, T.S.; Vintzileos, A.M. Intrauterine Growth Restriction in Infants of Less than Thirty-Two Weeks' Gestation: Associated Placental Pathologic Features. Am. J. Obstet. Gynecol. 1995, 173, 1049-1057. [CrossRef] open in new tab
- Doppler Studies in Fetal Hypoxemic Hypoxia. Available online: https://sonoworld.com/client/fetus/html/doppler/capitulos- html/chapter_04.htm (accessed on 4 February 2022). open in new tab
- Brosens, I.; Dixon, H.G.; Robertson, W.B. Fetal Growth Retardation and the Arteries of the Placental Bed. Br. J. Obstet. Gynaecol. 1977, 84, 656-663. [CrossRef] open in new tab
- Khong, T.; Wolf, F.D.; Robertson, W.B.; Brosens, I. Inadequate Maternal Vascular Response to Placentation in Pregnancies Complicated by Pre-Eclampsia and by Small-for-Gestational Age Infants. Br. J. Obstet. Gynaecol. 1986, 93, 1049-1059. [CrossRef] open in new tab
- Giles, W.B.; Trudinger, B.J.; Baird, P.J. Fetal Umbilical Artery Flow Velocity Waveforms and Placental Resistance: Pathological Correlation. Br. J. Obstet. Gynaecol. 1985, 92, 31-38. [CrossRef] open in new tab
- Sheppard, B.L.; Bonnar, J. An Ultrastructural Study of Utero-Placental Spiral Arteries in Hypertensive and Normotensive Pregnancy and Fetal Growth Retardation. Br. J. Obstet. Gynaecol. 1981, 88, 695-705. [CrossRef] open in new tab
- Norris, L.A.; Sheppard, B.L.; Burke, G.; Bonnar, J. Platelet Activation in Normotensive and Hypertensive Pregnancies Complicated by Intrauterine Growth Retardation. Br. J. Obstet. Gynaecol. 1994, 101, 209-214. [CrossRef] open in new tab
- Burton, G.J.; Jauniaux, E. Pathophysiology of Placental-Derived Fetal Growth Restriction. Am. J. Obstet. Gynecol. 2018, 218, S745-S761. [CrossRef] open in new tab
- Ellison, P.T.; Jasienska, G. Constraint, Pathology, and Adaptation: How Can We Tell Them Apart? Am. J. Hum. Biol. 2007, 19, 622-630. [CrossRef] open in new tab
- Gardosi, J.; Madurasinghe, V.; Williams, M.; Malik, A.; Francis, A. Maternal and Fetal Risk Factors for Stillbirth: Population Based Study. BMJ 2013, 346, f108. [CrossRef] open in new tab
- Klinger, M.H.F.; Jelkmann, W. Role of Blood Platelets in Infection and Inflammation. J. Interferon Cytokine Res. 2002, 22, 913-922. [CrossRef] open in new tab
- Sugimura, M.; Kobayashi, T.; Shu, F.; Kanayama, N.; Terao, T. Annexin V Inhibits Phosphatidylserine-Induced Intrauterine Growth Restriction in Mice. Placenta 1999, 20, 555-560. [CrossRef] open in new tab
- Gordijn, S.J.; Beune, I.M.; Thilaganathan, B.; Papageorghiou, A.; Baschat, A.A.; Baker, P.N.; Silver, R.M.; Wynia, K.; Ganzevoort, W. Consensus Definition of Fetal Growth Restriction: A Delphi Procedure. Ultrasound Obstet. Gynecol. 2016, 48, 333-339. [CrossRef] open in new tab
- Lewandowska, M.; Sajdak, S.; Więckowska, B.; Manevska, N.; Lubiński, J. The Influence of Maternal BMI on Adverse Pregnancy Outcomes in Older Women. Nutrients 2020, 12, 2838. [CrossRef] open in new tab
- Komosa, A.; Rzymski, P.; Perek, B.; Ropacka-Lesiak, M.; Lesiak, M.; Siller-Matula, J.M.; Poniedziałek, B. Platelets Redox Balance Assessment: Current Evidence and Methodological Considerations. Vasc. Pharmacol. 2017, 93-95, 6-13. [CrossRef] open in new tab
- Gomes, A.; Fernandes, E.; Lima, J.L.F.C. Fluorescence Probes Used for Detection of Reactive Oxygen Species. J. Biochem. Biophys. Methods 2005, 65, 45-80. [CrossRef] open in new tab
- Dikalov, S.I.; Harrison, D.G. Methods for Detection of Mitochondrial and Cellular Reactive Oxygen Species. Antioxid. Redox Signal. 2014, 20, 372-382. [CrossRef] open in new tab
- Poniedziałek, B.; Nowaczyk, J.; Ropacka-Lesiak, M.; Niedzielski, P.; Komosa, A.; Pańczak, K.; Rzymski, P. The Altered Platelet Mineral Ratios in Pregnancy Complicated with Intrauterine Growth Restriction. Reprod. Toxicol. 2018, 76, 46-52. [CrossRef] open in new tab
- Barker, D.J.; Osmond, C.; Law, C.M. The Intrauterine and Early Postnatal Origins of Cardiovascular Disease and Chronic Bronchitis. J. Epidemiol. Community Health 1989, 43, 237-240. [CrossRef] open in new tab
- de Jong, M.; Cranendonk, A.; van Weissenbruch, M.M. Components of the Metabolic Syndrome in Early Childhood in Very-Low- Birth-Weight Infants and Term Small and Appropriate for Gestational Age Infants. Pediatr. Res. 2015, 78, 457-461. [CrossRef] open in new tab
- Kesavan, K.; Devaskar, S.U. Intrauterine Growth Restriction: Postnatal Monitoring and Outcomes. Pediatr. Clin. N. Am. 2019, 66, 403-423. [CrossRef] open in new tab
- Schoots, M.H.; Gordijn, S.J.; Scherjon, S.A.; van Goor, H.; Hillebrands, J.-L. Oxidative Stress in Placental Pathology. Placenta 2018, 69, 153-161. [CrossRef] open in new tab
- Burton, G.J.; Jauniaux, E. Oxidative Stress. Best Pract. Res. Clin. Obstet. Gynaecol. 2011, 25, 287-299. [CrossRef] open in new tab
- Theilen, L.H.; Campbell, H.D.; Mumford, S.L.; Purdue-Smithe, A.C.; Sjaarda, L.A.; Perkins, N.J.; Radoc, J.G.; Silver, R.M.; Schisterman, E.F. Platelet Activation and Placenta-Mediated Adverse Pregnancy Outcomes: An Ancillary Study to the Effects of Aspirin in Gestation and Reproduction Trial. Am. J. Obstet. Gynecol. 2020, 223, 741.e1-741.e12. [CrossRef] open in new tab
- Krötz, F.; Sohn, H.-Y.; Pohl, U. Reactive Oxygen Species: Players in the Platelet Game. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 1988-1996. [CrossRef] open in new tab
- Wachowicz, B.; Olas, B.; Zbikowska, H.M.; Buczyński, A. Generation of Reactive Oxygen Species in Blood Platelets. Platelets 2002, 13, 175-182. [CrossRef] open in new tab
- Pratico, D.; Iuliano, L.; Pulcinelli, F.M.; Bonavita, M.S.; Gazzaniga, P.P.; Violi, F. Hydrogen Peroxide Triggers Activation of Human Platelets Selectively Exposed to Nonaggregating Concentrations of Arachidonic Acid and Collagen. J. Lab. Clin. Med. 1992, 119, 364-370.
- Irani, K.; Pham, Y.; Coleman, L.D.; Roos, C.; Cooke, G.E.; Miodovnik, A.; Karim, N.; Wilhide, C.C.; Bray, P.F.; Goldschmidt- Clermont, P.J. Priming of Platelet AlphaIIbbeta3 by Oxidants Is Associated with Tyrosine Phosphorylation of Beta3. Arterioscler. Thromb. Vasc. Biol. 1998, 18, 1698-1706. [CrossRef] open in new tab
- Leo, R.; Praticò, D.; Iuliano, L.; Pulcinelli, F.M.; Ghiselli, A.; Pignatelli, P.; Colavita, A.R.; FitzGerald, G.A.; Violi, F. Platelet Activation by Superoxide Anion and Hydroxyl Radicals Intrinsically Generated by Platelets That Had Undergone Anoxia and Then Reoxygenated. Circulation 1997, 95, 885-891. [CrossRef] [PubMed] open in new tab
- Yamagishi, S.I.; Edelstein, D.; Du, X.L.; Brownlee, M. Hyperglycemia Potentiates Collagen-Induced Platelet Activation through Mitochondrial Superoxide Overproduction. Diabetes 2001, 50, 1491-1494. [CrossRef] [PubMed] open in new tab
- Krötz, F.; Sohn, H.Y.; Gloe, T.; Zahler, S.; Riexinger, T.; Schiele, T.M.; Becker, B.F.; Theisen, K.; Klauss, V.; Pohl, U. NAD(P)H Oxidase-Dependent Platelet Superoxide Anion Release Increases Platelet Recruitment. Blood 2002, 100, 917-924. [CrossRef] [PubMed] open in new tab
- Clutton, P.; Miermont, A.; Freedman, J.E. Regulation of Endogenous Reactive Oxygen Species in Platelets Can Reverse Aggrega- tion. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 187-192. [CrossRef] open in new tab
- Oparka, M.; Walczak, J.; Malinska, D.; van Oppen, L.M.P.E.; Szczepanowska, J.; Koopman, W.J.H.; Wieckowski, M.R. Quantifying ROS Levels Using CM-H2DCFDA and HyPer. Methods 2016, 109, 3-11. [CrossRef] open in new tab
- Ravera, S.; Panfoli, I. Platelet Aerobic Metabolism: New Perspectives. J. Unexplor. Med. Data 2019, 2019, 7. [CrossRef] open in new tab
- Perry, C.G.R.; Kane, D.A.; Lanza, I.R.; Neufer, P.D. Methods for Assessing Mitochondrial Function in Diabetes. Diabetes 2013, 62, 1041-1053. [CrossRef] open in new tab
- Dmitriev, R.I.; Zhdanov, A.V.; Jasionek, G.; Papkovsky, D.B. Assessment of Cellular Oxygen Gradients with a Panel of Phospho- rescent Oxygen-Sensitive Probes. Anal. Chem. 2012, 84, 2930-2938. [CrossRef] open in new tab
- Somkhit, J.; Loyant, R.; Brenet, A.; Hassan-Abdi, R.; Yanicostas, C.; Porceddu, M.; Borgne-Sanchez, A.; Soussi-Yanicostas, N. A Fast, Simple, and Affordable Technique to Measure Oxygen Consumption in Living Zebrafish Embryos. Zebrafish 2020, 17, 268-270. [CrossRef] open in new tab
- Hynes, J.; Marroquin, L.D.; Ogurtsov, V.I.; Christiansen, K.N.; Stevens, G.J.; Papkovsky, D.B.; Will, Y. Investigation of Drug- Induced Mitochondrial Toxicity Using Fluorescence-Based Oxygen-Sensitive Probes. Toxicol. Sci. 2006, 92, 186-200. [CrossRef] open in new tab
- Will, Y.; Hynes, J.; Ogurtsov, V.I.; Papkovsky, D.B. Analysis of Mitochondrial Function Using Phosphorescent Oxygen-Sensitive Probes. Nat. Protoc. 2006, 1, 2563-2572. [CrossRef] open in new tab
- Kondrashina, A.V.; Ogurtsov, V.I.; Papkovsky, D.B. Comparison of the Three Optical Platforms for Measurement of Cellular Respiration. Anal. Biochem. 2015, 468, 1-3. [CrossRef] open in new tab
- Fercher, A.; Borisov, S.M.; Zhdanov, A.V.; Klimant, I.; Papkovsky, D.B. Intracellular O 2 Sensing Probe Based on Cell-Penetrating Phosphorescent Nanoparticles. ACS Nano 2011, 5, 5499-5508. [CrossRef] open in new tab
- Fercher, A.; O'Riordan, T.C.; Zhdanov, A.V.; Dmitriev, R.I.; Papkovsky, D.B. Imaging of Cellular Oxygen and Analysis of Metabolic Responses of Mammalian Cells. Methods Mol. Biol. 2010, 591, 257-273. [CrossRef] open in new tab
- Rumsey, W.L.; Vanderkooi, J.M.; Wilson, D.F. Imaging of Phosphorescence: A Novel Method for Measuring Oxygen Distribution in Perfused Tissue. Science 1988, 241, 1649-1651. [CrossRef] open in new tab
- O'Riordan, T.C.; Fitzgerald, K.; Ponomarev, G.V.; Mackrill, J.; Hynes, J.; Taylor, C.; Papkovsky, D.B. Sensing Intracellular Oxygen Using Near-Infrared Phosphorescent Probes and Live-Cell Fluorescence Imaging. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292, R1613-R1620. [CrossRef] open in new tab
- Melchinger, H.; Jain, K.; Tyagi, T.; Hwa, J. Role of Platelet Mitochondria: Life in a Nucleus-Free Zone. Front. Cardiovasc. Med. 2019, 6, 153. [CrossRef] open in new tab
- Valera, M.-C.; Parant, O.; Vayssiere, C.; Arnal, J.-F.; Payrastre, B. Physiologic and Pathologic Changes of Platelets in Pregnancy. Platelets 2010, 21, 587-595. [CrossRef] open in new tab
- Kanat-Pektas, M.; Yesildager, U.; Tuncer, N.; Arioz, D.T.; Nadirgil-Koken, G.; Yilmazer, M. Could Mean Platelet Volume in Late First Trimester of Pregnancy Predict Intrauterine Growth Restriction and Pre-Eclampsia? J. Obstet. Gynaecol. Res. 2014, 40, 1840-1845. [CrossRef] open in new tab
- Manten, G.T.R.; Sikkema, M.J.; Voorbij, H.A.M.; Visser, G.H.A.; Bruinse, H.W.; Franx, A. Risk Factors for Cardiovascular Disease in Women with a History of Pregnancy Complicated by Preeclampsia or Intrauterine Growth Restriction. Hypertens. Pregnancy 2007, 26, 39-50. [CrossRef] open in new tab
- Bujold, E.; Roberge, S.; Lacasse, Y.; Bureau, M.; Audibert, F.; Marcoux, S.; Forest, J.-C.; Giguère, Y. Prevention of Preeclampsia and Intrauterine Growth Restriction with Aspirin Started in Early Pregnancy: A Meta-Analysis. Obstet. Gynecol. 2010, 116, 402-414. [CrossRef] open in new tab
- Blomqvist, L.R.F.; Strandell, A.M.; Baghaei, F.; Hellgren, M.S.E. Platelet Aggregation in Healthy Women during Normal Pregnancy-A Longitudinal Study. Platelets 2019, 30, 438-444. [CrossRef] open in new tab
- Can, M.M.; Kaymaz, C.; Can, E.; Tanboga, I.H.; Api, O.; Kars, B.; Ceren Tokgoz, H.; Turkyilmaz, E.; Akgun, T.; Sonmez, K.; et al. Whole Blood Platelet Aggregation Failed to Detect Differences between Preeclampsia and Normal Pregnancy. Platelets 2010, 21, 496-497. [CrossRef] open in new tab
- Navaratnam, K.; Alfirevic, A.; Jorgensen, A.; Alfirevic, Z. Aspirin Non-Responsiveness in Pregnant Women at High-Risk of Pre-Eclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 2018, 221, 144-150. [CrossRef] open in new tab
- Norris, L.A.; Gleeson, N.; Sheppard, B.L.; Bonnar, J. Whole Blood Platelet Aggregation in Moderate and Severe Pre-Eclampsia. BJOG Int. J. Obstet. Gynaecol. 1993, 100, 684-688. [CrossRef] [PubMed] open in new tab
- Lam, F.W.; Vijayan, K.V.; Rumbaut, R.E. Platelets and Their Interactions with Other Immune Cells. Compr. Physiol. 2015, 5, 1265-1280. [CrossRef] open in new tab
- Tsoupras, A.; Zabetakis, I.; Lordan, R. Platelet Aggregometry Assay for Evaluating the Effects of Platelet Agonists and Antiplatelet Compounds on Platelet Function in Vitro. MethodsX 2019, 6, 63-70. [CrossRef] open in new tab
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