Factors regulating placental angio/vasculogenesis in complications of pregnancy and childbirth

1. Selvam S., Kumar T., Fruttiger M. Retinal vasculature development in health and disease. Prog. Retin. Eye Res. 2018; 63: 1-19. https://dx.doi.org/10.1016/j.preteyeres.2017.11.001.
2. Cheng R., Ma J.X. Angiogenesis in diabetes and obesity. Rev. Endocr. Metab. Disord. 2015; 16(1): 67-75. https://dx.doi.org/10.1007/s11154-015-9310-7.
3. Umapathy A., Chamley L.W., James J.L. Reconciling the distinct roles of angiogenic/anti-angiogenic factors in the placenta and maternal circulation of normal and pathological pregnancies. Angiogenesis. 2020; 23(2): 105-17. https://dx.doi.org/10.1007/s10456-019-09694-w.
4. Pereira R.D., De Long N.E., Wang RC., Yazdi F.T., Holloway A.C., Raha S. Angiogenesis in the placenta: the role of reactive oxygen species signaling. Biomed. Res. Int. 2015; 2015: 814543. https://dx.doi.org/10.1155/2015/814543.
5. Alfaidy N., Hoffmann P., Boufettal H., Samouh N., Aboussaouira T., Benharouga M. et al. The multiple roles of EG-VEGF/PROK1 in normal and pathological placental angiogenesis. Biomed. Res. Int. 2014; 2014: 451906.https://dx.doi.org/10.1155/2014/451906.
6. Chappell L.C., Duckworth S., Seed P.T., Griffin M., Myers J., Mackillop L. et al. Diagnostic accuracy of placental growth factor in women with suspected preeclampsia: a prospective multicenter study. Circulation. 2013; 128(19): 2121-31. https://dx.doi.org/10.1161/circulationaha.113.003215.
7. Benton S.J., McCowan L.M., Heazell A.E., Grynspan D., Hutcheon J.A., Senger C. et al. Placental growth factor as a marker of fetal growth restriction caused by placental dysfunction. Placenta. 2016; 42: 1-8. https://dx.doi.org/10.1016/j.placenta.2016.03.010.
8. Цибизова В.И., Первунина Т.М., Артеменко В.А., Бицадзе В.О., Гоциридзе К.Э., Аверкин И.И., Блинов Д.В., Новикова Н.Ю. Ключевая функция плаценты в формировании врожденного порока сердца плода. Акушерство, гинекология и репродукция. 2022; 16(1): 66-72. [Tsibizova V.I., Pervunina T.M., Artemenko V.A., Bitsadze V.O., Gotsiridze K.E.,Averkin I.I., Blinov D.V., Novikova N.Yu. Placenta crucially affects formation of fetal congenital heart disease. Obstetrics, Gynecology and Reproduction. 2022; 16(1): 66-72. (in Russian)]. https://dx.doi.org/10.17749/2313-7347/ob.gyn.rep.2022.262.
9. Laakkonen J.P., Lähteenvuo J., Jauhiainen S., Heikura T., Ylä-Herttuala S.Beyond endothelial. cells: vascular endothelial growth factors in heart, vascular anomalies and placenta. Vascul. Pharmacol. 2019; 112: 91-101.https://dx.doi.org/10.1016/j. vph.2018.10.005.
10. Llurba E., Sanchez O., Ferrer Q., Nicolaides K.H., Ruíz A., Domínguez C. et al. Maternal and foetal angiogenic imbalance in congenital heart defects. Eur. Heart J. 2014; 35(11): 701-7. https://dx.doi.org/10.1093/eurheartj/eht389.
11. Brodwall K., Leirgul E., Greve G., Vollset S.E., Holmstrøm H., Tell G.S.,Øyen N. Possible common aetiology behind maternal preeclampsia and congenital heart defects in the child: a cardiovascular diseases in Norway project study. Paediatr. Perinat. Epidemiol. 2016; 30(1): 76-85.https://dx.doi.org/10.1111/ppe.12252.
12. Melincovici C.S., Boşca A.B., Şuşman S., Mărginean M., Mihu C., Istrate M. et al. Vascular endothelial growth factor (VEGF) - key factor in normal and pathological angiogenesis. Rom. J. Morphol. Embryol. 2018; 59(2): 455-67.
13. Miron L., Gafton B., Marinca M. Angiogeneza tumorală – implicaţii în terapia cancerelor. Jurnalul de Chirurgie, Iaşi. 2010; 6(2): 104-10.
14. Arcondéguy T., Lacazette E., Millevoi S., Prats H., Touriol C. VEGF-A mRNA processing, stability and translation: a paradigm for intricate regulation of gene expression at the posttranscriptional level. Nucleic Acids Res. 2013; 41(17): 7997-8010. https://dx.doi.org/10.1093/nar/gkt539.
15. Iyer S., Acharya K.R. Tying the knot: the cystine signature and mo-lecular-recognition processes of the vascular endothelial growth factor family of angiogenic cytokines. FEBS J. 2011; 278(22): 4304-22.https://dx.doi.org/10.1111/j.1742-4658.2011.08350.x.
16. Duffy A.M., Bouchier-Hayes D.J., Harmey J.H. Vascular endothelial growth factor (VEGF) and its role in non-endothelial cells: autocrine signalling by VEGF. In: Madame Curie Bioscience Database (formerly, Eurekah Bioscience Database). Angiogenesis. Landes Bioscience, Austin (TX), USA, 2000-2013. Available at: https://www.ncbi.nlm.nih.gov/books/NBK6482/
17. Koch S., Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harb. Perspect. Med. 2012; 2(7): a006502.https://dx.doi.org/10.1101/cshperspect.a006502.
18. Борзилова Ю.А., Болдырева Л.А., Шлык И.В. Васкулоэндотелиальные факторы роста (VEGF): роль и место в патологических процессах. Вестник офтальмологии. 2016; 132(4): 98-103. [Borzilova Yu.A., Boldyreva L.A., Shlyk I.V. Vascular endothelial growth factors (VEGF): role in pathological processes. Bulletin of Oftalmology. 2016; 132(4): 98-103. (in Russian)].https://dx.doi.org/10.17116/oftalma2016132498-103.
19. Klettner A., Westhues D., Lassen J., Bartsch S., Roider J. Regulation of constitutive vascular endothelial growth factor secretion in retinal pigment epithelium/choroid organ cultures: p38, nuclear factor κB, and the vascular endothelial growth factor receptor-2/phosphatidylinositol 3 kinase pathway. Mol. Vis. 2013; 19: 281-91.
20. Wang J.J., Zhu M., Le Y.Z. Functions of Müller cell-derived vascular endothelial growth factor in diabetic retinopathy. World J. Diabetes. 2015; 6(5): 726-33. https://dx.doi.org/10.4239/wjd.v6.i5.726.
21. Maloney J.P., Gao L. Proinflammatory cytokines increase vascular endothelial growth factor expression in alveolar epithelial cells. Mediators Inflamm. 2015; 2015: 387842. https://dx.doi.org/10.1155/2015/387842.
22. Zhang F., Tang Z., Hou X., Lennartsson J., Li Y., Koch A.W. et al. VEGF-B is dispensable for blood vessel growth but critical for their survival, and VEGF-B targeting inhibits pathological angiogenesis. Proc. Natl. Acad. Sci. USA. 2009; 106(15): 6152-7. https://dx.doi.org/110.1073/pnas.0813061106.
23. Tammela T., Zarkada G., Nurmi H., Jakobsson L., Heinolainen K., Tvorogov D. et al. VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing notch signalling. Nat. Cell Biol. 2011; 13(10): 1202-13.https://dx.doi.org/10.1038/ncb2331.
24. Shibuya M. Vascular endothelial growth factor (VEGF) and its receptor (VEGFR) signaling in angiogenesis: a crucial target for anti- and pro-angiogenic therapies genes. Genes Cancer. 2011; 2(12): 1097-105.https://dx.doi.org/10.1177/1947601911423031.
25. Lecarpentier É., Vieillefosse S., Haddad B., Fournier T., Leguy M.C., Guibourdenche J., Tsatsaris V. Placental growth factor (PlGF) and sFlt-1 during pregnancy: physiology, assay and interest in preeclampsia. Ann. Biol. Clin. (Paris). 2016; 74(3): 259-67. https://dx.doi.org/10.1684/abc.2016.1158.
26. Binder N.K., Evans J., Salamonsen L.A., Gardner D.K., Kaitu’u-Lino T.J., Hannan N.J. Placental growth factor is secreted by the human endometrium and has potential important functions during embryo development and implantation. PLoS One. 2016; 11(10): e0163096. https://dx.doi.org/10.1371/journal.pone.0163096.
27. Albonici L., Benvenuto M., Focaccetti C., Cifaldi L., Miele M.T., Limana F. et al. PlGF immunological impact during pregnancy. Int. J. Mol. Sci. 2020; 21(22): 8714. https://dx.doi.org/10.3390/ijms21228714.
28. Griffith O.W., Chavan A.R., Protopapas S., Maziarz J., Romero R.,Wagner G.P. Embryo implantation evolved from an ancestral inflammatory attachment reaction. Proc. Natl. Acad. Sci. USA. 2017; 114: E6566-575.https://dx.doi.org/10.1073/pnas.1701129114.
29. Simons M., Gordon E., Claesson-Welsh L. Mechanisms and regulation of endothelial VEGF receptor signalling. Nat. Rev. Mol. Cell Biol. 2016; 17(10): 611-25. https://dx.doi.org/10.1038/nrm.2016.87.
30. Tudisco L., Orlandi A., Tarallo V., De Falco S. Hypoxia activates placental growth factor expression in lymphatic endothelial cells. Oncotarget. 2017; 8(20):32873-83. https://dx.doi.org/10.18632/oncotarget.15861.
31. Roy S., Bag A.K., Singh R.K., Talmadge J.E., Batra S.K., Datta K. Multifaceted role of neuropilins in the immune system: potential targets for immunotherapy. Front. Immunol. 2017; 8: 1228. https://dx.doi.org/10.3389/fimmu.2017.01228.
32. Holme A.M., Roland M.C., Henriksen T., Michelsen T.M. In vivo uteroplacental release of placental growth factor and soluble Fms-like tyrosine kinase-1 in normal and preeclamptic pregnancies. Am. J. Obstet. Gynecol. 2016;215(6): 782e1-e9. https://dx.doi.org/10.1016/j.ajog.2016.07.056.
33. Chau K., Hennessy A., Makris A. Placental growth factor and pre-eclampsia. J. Hum. Hypertens. 2017; 31(12): 782-6. https://dx.doi.org/10.1038/jhh.2017.61.
34. Ratsep M.T., Carmeliet P., Adams M.A., Croy B.A. Impact of placental growth factor deficiency on early mouse implant site angiogenesis. Placenta. 2014; 35(9): 772-5. https://dx.doi.org/10.1016/j.placenta.2014.07.006.
35. Yonekura Collier A.R., Zsengeller Z., Pernicone E., Salahuddin S., Khankin E.V., Karumanchi S.A. Placental sFLT1 is associated with complement activation and syncytiotrophoblast damage in preeclampsia. Hypertens. Pregnancy. 2019; 38(3): 193-9. https://ddx.oi.org/10.1080/10641955.2019.1640725.
36. Niu G., Chen X. Vascular endothelial growth factor as an anti-angiogenic target for cancer therapy. Curr. Drug Targets. 2010; 11(8): 1000-17.https://dx.doi.org/10.2174/138945010791591395.
37. Jung J.J., Tiwari A., Inamdar S.M., Thomas C.P., Goel A., Choudhury A. Secretion of soluble vascular endothelial growth factor receptor 1 (sVEGFR1/sFlt1) requires Arf1, Arf6, and Rab11 GTPases. PLoS One. 2012; 7(9): e44572. https://dx.doi.org/10.1371/journal.pone.0044572.
38. Verlohren S., Herraiz I., Lapaire O., Schlembach D., Zeisler H., Calda P. et al. Newgestational phase-specific cutoff values for the use of the soluble fms-like tyrosine kinase-1/placental growth factor ratio as a diagnostic test for preeclampsia. Hypertension. 2014; 63(2): 346-52. https://dx.doi.org/10.1161/hypertensionaha.113.01787.
39. Бурлев В.А. Инверсия ангиогенеза у беременных. Проблемы репродукции. 2013; (3): 58-66. [Burlev V.A. Angiogenesis inversion in pregnancy. Russian Journal of Human Reproduction. 2013; (3): 58-66. (in Rus-sian)].
40. Thomas-Schoemann A., Blanchet B., Boudou-Rouquette P., Gol-mard J.L., Noé G., Chenevier-Gobeaux C. et al. Soluble VEGFR-1: a new biomarker of sorafenib-related hypertension (i.e., sorafenib-related is the compound adjective?). J. Clin. Pharmacol. 2015; 55(4): 478-9. https://dx.doi.org/10.1002/jcph.429.
41. Фомина М.П., Дивакова Т.С., Ржеусская Л.Д. Эндотелиальная дисфункция и баланс ангиогенных факторов у беременных с плацентарными нарушениями. Медицинские новости. 2014; 3: 63-7. [Famina M.P., Divakova T.S., Rzheusskaya L.D. Endothelial dysfunction and balance of angiogenic factors in pregnant women with placental abnormalities. Medical News. 2014; (3): 63-7. (in Russian)].
42. Sovio U., Gaccioli F., Cook E., Charnock-Jones D.S., Smith G.C.S. Slowing of fetal growth and elevated maternal serum sFLT1:PlGF are associated with early term spontaneous labor. Am. J. Obstet. Gynecol. 2021; 225(5): 520.e1-10. https://dx.doi.org/10.1016/j.ajog.2021.04.232.
43. Dunn L., Flatley C., Kumar S. Changes in maternal placental growth factor levels during term labour. Placenta. 2018; 61: 11-6. https://dx.doi.org/10.1016/j.placenta.2017.11.003.
44. Poon L.C.Y., Akolekar R., Lachmann R., Beta J., Nicolaides K.H. Hypertensive disorders in pregnancy: screening by biophysical and biochemical markers at 11-13 weeks. Ultrasound Obstet. Gynecol. 2010; 35(6): 662-70.https://dx.doi.org/10.1002/uog.7628.
45. Приходько Н.Г. Роль факторов роста в инвазии трофобласта и их ассоциация с патологическим течением беременности. Бюллетень физиологии и патологии дыхания. 2019; 74: 111-8. [Prikhodko N.G. The role of growth factors in trophoblast invasion and their association witn the pathological course of pregnancy. Bulletin of Physiology and Pathology of Respiration. 2019; (74): 111-8. (in Russian)]. https://dx.doi.org/10.36604/1998-5029-2019-74-111-118.
46. Зиганшина М.М., Кречетова Л.В., Ванько Л.В., Ходжаева З.С., Мусиенко Е.В., Сухих Г.Т. Про- и антиангиогенные факторы в патогенезе ранних потерь беременности. Часть 1. Особенности содержания про- и антиангиогенных сывороточных факторов в ранние сроки беременности. Акушерство и гинекология. 2012; 3: 14-9. [Ziganshina M.M., Krechetova L.V., Vanko L.V., Khodzhayeva Z.S., Musiyenko E.V.,Sukhikh G.T. Pro- and antiangiogenic factors in the pathogenesis of early pregnancy losses. Part 1. The specific features of pro- and antiangiogenic serum factors in early pregnancy. Obstetrics and Gynecology. 2012; (3); 14-9.(in Russian)].
47. Курцер М.А., Сичинава Л.Г., Алажажи А.О., Нормантович Т.О., Николаева Е.В. Прогностическая значимость соотношения ангиоген-ных факторов sFlt-1/PlGF в качестве маркера преэклампсии у беременных двойней. Вопросы гинекологии, акушерства и перинатологии. 2022; 21(2): 5-12. [Kurtser M.A., Sichinava L.G., Alazhazhi A.O., Normantovich T.O., Ni-kolaeva E.V. Prognostic value of angiogenic factors (sFlt-1/PlGF ratio) as a marker for pre-eclampsia in twin pregnancy. Gynecology, Obstetrics and Peri-natology. 2022; 21(2): 5-12. (in Russian)]. https://dx.doi.org/10.20953/1726-1678-2022-2-5-12.
48. Boeldt D.S., Bird I.M. Vascular adaptation in pregnancy and endothelial dysfunction in preeclampsia. J. Endocrinol. 2017; 232(1): R27-44.https://dx.doi.org/10.1530/joe-16-0340.
49. Opichka M.A., Rappelt M.W., Gutterman D.D., Grobe J.L., McIn-tosh J.J. Vascular dysfunction in preeclampsia. Cells. 2021; 10: 3055.https://dx.doi.org/10.3390/ cells10113055.
50. Nirupama R., Divyashree S., Janhavi P., Muthukumar S.P., Ravindra P.V. Preeclampsia: pathophysiology and management. J. Gynecol. Obstet. Hum. Reprod. 2021; 50(2): 101975. https://dx.doi.org/10.1016/j.jogoh.2020.101975.
51. Bligh L.N., Greer R.M., Kumar S. The relationship between maternal placental growth factor levels and intrapartum fetal compromise. Placenta. 2016; 48: 63-7. https://dx.doi.org/10.1016/j.placenta.2016.10.007.
52. Dunn L., Kumar S. Changes in intrapartum maternal placental growth factor levels in pregnancies complicated by fetal compromise at term. Placenta. 2018; 74: 9-13. https://dx.doi.org/10.1016/j.placenta.2018.12.010.
53. Bligh L.N., Alsolai A.A., Greer R.M., Kumar S. Prelabor screening for intrapartum fetal compromise in low-risk pregnancies at term: cerebroplacental ratio and placental growth factor. Ultrasound Obstet. Gynecol. 2018; 52(6): 750-6. https://dx,doi.org/10.1002/uog.18981.
54. Bowe S., Mitlid-Mork B., Georgieva A., Gran J.M., Redman C.W.G., Staff A.C., Sugulle M. The association between placenta-associated circulating biomarkers and composite adverse delivery outcome of a likely placental cause in healthy post-date pregnancies. Acta Obstet. Gynecol. Scand. 2021; 100(10): 1893-901. https://dx.doi.org/10.1111/aogs.14223.
55. Zych B., Górka A., Myszka A., Błoniarz D., Siekierzyn ́ska A., Błaz W. Status of oxidative stress during low-risk labour: preliminary data. Int. J. Environ. Res. Public Health. 2023; 20(1): 157. https://dx.doi.org/10.3390/ijerph20010157.
56. Díaz-Castro J., Florido J., Kajarabille N., Prados S., de Paco C., Ocon O.,Pulido-Moran M., Ochoa J.J. A new approach to oxidative stress and inflammatory signaling during labour in healthy mothers and neonates. Oxid. Med. Cell. Longev. 2015; 2015: 178536. https://dx.doi.org/10.1155/2015/178536.
57. Dunn L., Flatley C., Kumar S. Changes in maternal placental growth factor levels during term labour. Placenta. 2018; 61: 11-6. https://dx.doi.org/10.1016/j.placenta.2017.11.003.
58. Tanaka H., Tanaka K., Takakura S., Enomoto N., Maki S., Ikeda T. Placental growth factor level is correlated with intrapartum fetal heart rate findings BMC Pregnancy Childbirth. 2022; 22(1): 215. https://dx.doi.org/10.1186/s12884-022-04562-w.
59. Mizuuchi M., Cindrova-Davies T., Olovsson M., Charnock-Jones D.S., Burton G.J., Yung H.W. Placental endoplasmic reticulum stress negatively regulates transcription of placental growth factor via ATF4 andATF6b: implications for the pathophysiology of human pregnancy complications, J. Pathol. 2016; 238(4): 550e-61. https://dx.doi.org/10.1002/path.4678.
60. Низяева Н.В., Приходько А.М., Евграфова А.В., Тысячный О.В., Баев О.Р.Клинико-морфологические особенности плаценты при острой внутри­утробной гипоксии плода в родах. Акушерство и гинекология. 2019; 12: 96-104. [Nizyaeva N.V., Prikhodko A.M., Evgrafova A.V., Tysyachnyi O.V., Baev O.R. Clinical and morphological features of the placenta in acute intrauterine hypoxia during childbirth. Obstetrics and Gynecology. 2019; (12): 96-104. (in Russian)]. https://dx.doi.org/10.18565/aig.2019.12.96-104.
61. Nucci M., Poon L.C., Demirdjian G., Darbouret B., Nicolaides K.H. Maternal serum placental growth factor (PlGF) isoforms 1 and 2 at 11-13 weeks'gestation in normal and pathological pregnancies. Fetal Diagn. Ther. 2014; 36(2): 106-16. https://dx.doi.org/10.1159/000357842.
62. Bdolah Y., Elchalal U., Natanson-Yaron S., Yechiam H., Bdolah-Abram T., Greenfield C. et al. Relationship between nulliparity and preeclampsia may be explained by altered circulating soluble fms-like tyrosine kinase 1. Hypertens. Pregnancy. 2014; 33(2): 250-9. https://dx.doi.org/10.3109/10641955.2013.858745.
63. Goldman-Wohl D., Gamliel M., Mandelboim O., Yagel S. Learning from experience: cellular and molecular bases for improved outcome in subsequent pregnancies. Am. J. Obstet. Gynecol. 2019; 221(3): 183-93.https://dx.doi.org/10.1016/j.ajog.2019.02.037.
64. Litwin S., Cortina M.E., Barrientos G.L., Prados M.B., Roux M.E., Miranda S.E. Multiparity increases trophoblast invasion and vascular endothelial growth factor expression at the maternal-fetal interface in mice. J. Reprod. Immunol. 2010; 85(2): 161-7. https://dx.doi.org/10.1016/j.jri.2010.03.004.
65. Triunfo S., Parra-Saavedra M., Rodriguez-Sureda V., Crovetto F., Dominguez C.,Gratac E., Figueras F. Angiogenic factors and doppler evaluation in normally growing fetuses at routine third-trimester scan: prediction of subsequent low birth weight. Fetal Diagn. Ther. 2016; 40(1): 13-20.https://dx.doi.org/10.1159/000440650.
66. Shah D.A., Khalil R.A. Bioactive factors in uteroplacental and systemic circulation link placental ischemia to generalized vascular dysfunction in hypertensive pregnancy and preeclampsia. Biochem. Pharmacol. 2015; 95(4): 211-26. https://dx.doi.org/10.1016/j.bcp.2015.04.012.
67. Rasmussen L.G., Lykke J.A., Staff A.C. Angiogenic biomarkers in pregnancy: defining maternal and fetal health, Acta Obstet. Gynecol. Scand. 2015; 94(8): 820-32. https://dx.doi.org/10.1111/aogs.12629.
68. Баев О.Р., Приходько А.М., Зиганшина М.М., Евграфова А.В., Хомякова Е.В. Антенатальные и интранатальные факторы риска, ассоциированные с гипоксией плода в родах. Акушерство и гинекология. 2022; 8: 47-53. [Baev O.R., Prikhodko A.M., Ziganshina M.M., Evgrafova A.V., Khomyakova E.V. Antenatal and intrapartum risk factors associated with fetal hypoxia in labor. Obstetrics and Gynecology. 2022; (8): 47-53. (in Russian)]. https://dx.doi.org/10.18565/aig.2022.8.47-53.

Received 13.06.2023

Accepted 28.06.2023