Abstract
The placenta is the most variable organ, in terms of structure, among the species. Besides it, all placental types have the same function: production of viable offspring, independent of pregnancy length, litter number, or invasion level. The angiogenesis is a central mechanism for placental functionality, due to proper maternal-fetal communication and exchanges. Much is known about the vasculature structure, but little is known about vasculature development and cellular interactions. Pericytes are perivascular cells that were described to control vasculature stability and permeability. Nowadays there are several new functions discovered, such as lymphocyte modulation and activation, macrophage-like phagocytic properties, tissue regenerative and repair processes, and also the ability to modulate stem cells, majorly the hematopoietic. In parallel, placental tissues are known to be a particularly immune microenvironment and a rich stem cell niche. The pericyte function plethora could be similar in the placental microenvironment and could have a central role in placental development and homeostasis.
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References
(1955) The normal anatomy of the uterine artery. Acta Radiol. 43:21–36. doi: 10.3109/00016925509170755, http://dx.doi.org/10.3109/00016925509170755
Abrahamsohn PA, Zorn TMT (1993) Implantation and decidualization in rodents. J Exp Zool 266:603–628. https://doi.org/10.1002/jez.1402660610
Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC (2002) Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 250:358–373
Al Ahmad A, Taboada CB, Gassmann M, Ogunshola OO (2011) Astrocytes and Pericytes differentially modulate blood—brain barrier characteristics during development and hypoxic insult. J Cereb Blood Flow Metab 31:693–705. https://doi.org/10.1038/jcbfm.2010.148
Aluvihare VR, Kallikourdis M, Betz AG (2004) Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5:266–271. https://doi.org/10.1038/ni1037
Antoniadou E, David AL (2016) Placental stem cells. Best Pract Res Clin Obstet Gynaecol 31:13–29. https://doi.org/10.1016/J.BPOBGYN.2015.08.014
Arck PC, Hecher K (2013) Fetomaternal immune cross-talk and its consequences for maternal and offspring’s health. Nat Med 19:548–556. https://doi.org/10.1038/nm.3160
Armulik A, Genové G, Mäe M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C (2010) Pericytes regulate the blood–brain barrier. Nature 468:557–561. https://doi.org/10.1038/nature09522
Armulik A, Genové G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21:193–215. https://doi.org/10.1016/j.devcel.2011.07.001
Aronoff DM, Correa H, Rogers LM, Arav-Boger R, Alcendor DJ (2017) Placental pericytes and cytomegalovirus infectivity: implications for HCMV placental pathology and congenital disease. Am J Reprod Immunol 78. https://doi.org/10.1111/aji.12728
Arts NF (1961) Investigations on the vascular system of the placenta. I. General introduction and the fetal vascular system. Am J Obstet Gynecol 82:147–158
Balabanov R, Washington R, Wagnerova J, Dore-Duffy P (1996) CNS microvascular pericytes express macrophage-like function, cell surface integrin alpha M, and macrophage marker ED-2. Microvasc Res 52:127–142. https://doi.org/10.1006/mvre.1996.0049
Balabanov R, Beaumont T, Dore-Duffy P (1999) Role of central nervous system microvascular pericytes in activation of antigen-primed splenic T-lymphocytes. J Neurosci Res 55:578–587. https://doi.org/10.1002/(SICI)1097-4547(19990301)55:5<578::AID-JNR5>3.0.CO;2-E
Bandeira DS, Casamitjana J, Crisan M (2017) Pharmacology & Therapeutics Pericytes , integral components of adult hematopoietic stem cell niches. Pharmacol Ther 171:104–113. https://doi.org/10.1016/j.pharmthera.2016.11.006
Barreto RSN, Bressan FF, Oliveira LJ, Pereira FTV, Perecin F, Ambrósio CE, Meirelles FV, Miglino MA (2011) Gene expression in placentation of farm animals: an overview of gene function during development. Theriogenology 76:589–597. https://doi.org/10.1016/j.theriogenology.2011.03.001
Baur R (1977) Morphometry of the placental exchange area. Adv Anat Embryol Cell Biol 53:3–65
Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, Zlokovic BV (2010) Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68:409–427. https://doi.org/10.1016/j.neuron.2010.09.043
Bergers G, Song S (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro-Oncology 7:452–464. https://doi.org/10.1215/S1152851705000232
Bjarnegard M (2004) Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131:1847–1857. https://doi.org/10.1242/dev.01080
Bouchard BA, Shatos MA, Tracy PB (1997) Human brain pericytes differentially regulate expression of procoagulant enzyme complexes comprising the extrinsic pathway of blood coagulation. Arterioscler Thromb Vasc Biol 17:1–9
Burton GJ, Charnock-Jones DS, Jauniaux E (2009) Regulation of vascular growth and function in the human placenta. Reproduction 138:895–902. https://doi.org/10.1530/REP-09-0092
Carter AM, Mess A (2007) Evolution of the placenta in eutherian mammals. Placenta 28:259–262. https://doi.org/10.1016/j.placenta.2006.04.010
Castejón OJ (2011) Ultrastructural pathology of cortical capillary pericytes in human traumatic brain oedema. Folia Neuropathol 49:162–173
Caumartin J, Favier B, Daouya M, Guillard C, Moreau P, Carosella ED, LeMaoult J (2007) Trogocytosis-based generation of suppressive NK cells. EMBO J 26:1423–1433. https://doi.org/10.1038/sj.emboj.7601570
Cecati M, Giannubilo SR, Emanuelli M, Tranquilli AL, Saccucci F (2011) HLA-G and pregnancy adverse outcomes. Med Hypotheses 76:782–784. https://doi.org/10.1016/j.mehy.2011.02.017
Challier JC, Kacemi A, Galtier M, Boucher M, Tangapregassom MJ, Vervelle C, Bintein T, Espié MJ, Olive G (1997) Phenotype of cultured fetal perivascular cells from human placenta studied by scanning electron microscopy. Anat Embryol (Berl) 195:79–86. https://doi.org/10.1007/s004290050027
Challier JC, Galtier M, Kacemi A, Guillaumin D (1999) Pericytes of term human foeto-placental microvessels: ultrastructure and visualization. Cell Mol Biol (Noisy-le-Grand) 45:89–100
Chen S, Lechleider RJ (2004) Transforming growth factor—induced differentiation of smooth muscle from a neural crest stem cell line. Circ Res 94:1195–1202. https://doi.org/10.1161/01.RES.0000126897.41658.81
Chen C-W, Okada M, Proto JD, Gao X, Sekiya N, Beckman SA, Corselli M, Crisan M, Saparov A, Tobita K, Péault B, Huard J (2013) Human pericytes for ischemic heart repair. Stem Cells 31:305–316. https://doi.org/10.1002/stem.1285
Chen WCW, Baily JE, Corselli M, Díaz ME, Sun B, Xiang G, Gray GA, Huard J, Péault B (2015) Human myocardial pericytes: multipotent mesodermal precursors exhibiting cardiac specificity. Stem Cells 33:557–573. https://doi.org/10.1002/stem.1868
Corselli M, Chin CJ, Parekh C, Sahaghian A, Wang W, Ge S, Evseenko D, Wang X, Montelatici E, Lazzari L, Crooks GM, Péault B (2013) Perivascular support of human hematopoietic stem/progenitor cells. Blood 121:2891–2901. https://doi.org/10.1182/blood-2012-08-451864
Crisan M, Yap S, Casteilla L, Chen C, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng P, Traas J, Schugar R, Deasy BM, Badylak S, Lazzari L, Huard J, Pe B (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313. https://doi.org/10.1016/j.stem.2008.07.003
Croy BA, Yamada AT, DeMayo FJ, Adamson SL (2015) The guide to investigation of mouse pregnancy. Elsevier, San Diego, CA
Cuevas P, Gutierrez-Diaz JA, Reimers D, Dujovny M, Diaz FG, Ausman JI (1984) Pericyte endothelial gap junctions in human cerebral capillaries. Anat Embryol (Berl) 170:155–159
Daneman R, Zhou L, Kebede AA, Barres BA (2010) Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468:562–566. https://doi.org/10.1038/nature09513
Dantzer V (2002) Endometrium of epitheliochorial and endotheliochorial placentae. In: Glasser SR, Aplin JD, Giudice LC, Tabibzadeh S (eds) The endometrium. Taylor & Francis, New York, pp 352–368
Dellavalle A, Maroli G, Covarello D, Azzoni E, Innocenzi A, Perani L, Antonini S, Sambasivan R, Brunelli S, Tajbakhsh S, Cossu G (2011) Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2:499. https://doi.org/10.1038/ncomms1508
Demir R, Kaufmann P, Castelluce M, Erbeng T, Kotowsk A (1989) Fetal vasculogenesis and angiogenesis in human placental villi. Cells Tissues Organs 136:190–203. https://doi.org/10.1159/000146886
Deveci E, Soker S, Turgut A, Aktas A, Ayaz E, Sak S, Seker U (2013) The immunohistochemical and ultrastructural evaluation of pericytes in human full term placentas of gestasyonal diabetes mellitus. Acta Medica Mediterr 29:697–700
Ding R, Darland DC, Parmacek MS, D’amore PA (2004) Endothelial–mesenchymal interactions in vitro reveal molecular mechanisms of smooth muscle/Pericyte differentiation. Stem Cells Dev 13:509–520. https://doi.org/10.1089/scd.2004.13.509
Ding L, Saunders TL, Enikolopov G, Morrison SJ (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481:457–462. https://doi.org/10.1038/nature10783
Djurisic S, Teiblum S, Tolstrup CK, Christiansen OB, Hviid TVF (2014) Allelic imbalance modulates surface expression of the tolerance-inducing HLA-G molecule on primary trophoblast cells. Mol Hum Reprod 21:281–295. https://doi.org/10.1093/molehr/gau108
Domev H, Milkov I, Itskovitz-Eldor J, Dar A (2014) Immunoevasive Pericytes from human pluripotent stem cells preferentially modulate induction of allogeneic regulatory T cells. Stem Cells Transl Med 3:1169–1181. https://doi.org/10.5966/sctm.2014-0097
Dubova EA, Buranova FB, Fyodorova TA, Shchyogolev AI, Sukhikh GT (2013) Morphological characteristics of the terminal villi in placental failure. Bull Exp Biol Med 155:507–511
Duffield JS, Lupher M, Thannickal VJ, Wynn TA (2013) Host responses in tissue repair and fibrosis. Annu Rev Pathol 8:241–276. https://doi.org/10.1146/annurev-pathol-020712-163930
Dulauroy S, Di Carlo SE, Langa F, Eberl G, Peduto L (2012) Lineage tracing and genetic ablation of ADAM12+ perivascular cells identify a major source of profibrotic cells during acute tissue injury. Nat Med 18:1262–1270. https://doi.org/10.1038/nm.2848
Dzierzak E, Robin C (2010) Placenta as a source of hematopoietic stem cells. Trends Mol Med 16:361–367. https://doi.org/10.1016/j.molmed.2010.05.005
Enders AC, Blankenship TN, Lantz KC, Enders SS (1998) Morphological variation in the interhemal areas of chorioallantoic placentae: a review. Placenta 19:1–19. https://doi.org/10.1016/S0143-4004(98)80030-1
Enge M, Bjarnegård M, Gerhardt H, Gustafsson E, Kalén M, Asker N, Hammes H-P, Shani M, Fässler R, Betsholtz C (2002) Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21:4307–4316
Fabry Z, Fitzsimmons KM, Herlein JA, Moninger TO, Dobbs MB, Hart MN (1993) Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. J Neuroimmunol 47:23–34
Farrington-Rock C, Crofts NJ, Doherty MJ, Ashton BA, Griffin-Jones C, Canfield AE (2004) Chondrogenic and adipogenic potential of microvascular pericytes. Circulation 110:2226–2232. https://doi.org/10.1161/01.CIR.0000144457.55518.E5
Favaron PO, Miglino MA (2017) Fetal membranes-derived stem cells microenvironment. Adv Exp Med Biol 1041:235–244
Feng J, Mantesso A, De Bari C, Nishiyama A, Sharpe PT (2011) Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci U S A 108:6503–6508. https://doi.org/10.1073/pnas.1015449108
Firth JA, Leach L (1996) Not trophoblast alone: a review of the contribution of the fetal microvasculature to transplacental exchange. Placenta 17:89–96. https://www.ncbi.nlm.nih.gov/pubmed/8730878
Fisher M (2009) Pericyte Signaling in the neurovascular unit. Stroke 40:S13–S15. https://doi.org/10.1161/STROKEAHA.108.533117
Furuya M, Ishida J, Inaba S, Kasuya Y, Kimura S, Nemori R, Fukamizu A (2008) Impaired placental neovascularization in mice with pregnancy-associated hypertension. Lab Investig 88:416–429. https://doi.org/10.1038/labinvest.2008.7
Gekas C, Rhodes KE, Vanhandel B, Chhabra A, Ueno M, Mikkola HKA (2010) Hematopoietic stem cell development in the placenta. Int J Dev Biol 54:1089–1098. https://doi.org/10.1387/ijdb.103070cg
Golub R, Cumano A (2013) Embryonic hematopoiesis. Blood Cells Mol Dis 51:226–231. https://doi.org/10.1016/j.bcmd.2013.08.004
Guerin LR, Prins JR, Robertson SA (2009) Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment? Hum Reprod Update 15:517–535. https://doi.org/10.1093/humupd/dmp004
Hasan M, Glees P (1990) The fine structure of human cerebral perivascular pericytes and juxtavascular phagocytes: their possible role in hydrocephalic edema resolution. J Hirnforsch 31:237–249
He N, van Iperen L, de Jong D, Szuhai K, Helmerhorst FM, van der Westerlaken LAJ, Chuva de Sousa Lopes SM (2017) Human extravillous trophoblasts penetrate decidual veins and lymphatics before remodeling spiral arteries during early pregnancy. PLoS One 12:e0169849. https://doi.org/10.1371/journal.pone.0169849
Heinrich D, Aoki A, Metz J (1988) Fetal capillary organization in different types of placenta. Trophobl Res 3:149–162. https://doi.org/10.1007/978-1-4615-8109-3_11
Helige C, Ahammer H, Hammer A, Huppertz B, Frank H-G, Dohr G (2008) Trophoblastic invasion in vitro and in vivo: similarities and differences. Hum Reprod 23:2282–2291. https://doi.org/10.1093/humrep/den198
Hellerbrand C (2013) Hepatic stellate cells—the pericytes in the liver. Pflügers Arch Eur J Physiol 465:775–778. https://doi.org/10.1007/s00424-012-1209-5
Hellström M, Gerhardt H, Kalén M, Li X, Eriksson U, Wolburg H, Betsholtz C (2001) Lack of Pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153:543–553
Herrmann M, Bara JJ, Sprecher CM, Menzel U, Jalowiec JM, Osinga R, Scherberich A, Alini M, Verrier S (2016) Pericyte plasticity—comparative investigation of the angiogenic and multilineage potential of pericytes from different human tissues. Eur Cells Mater 31:236–249. https://doi.org/10.22203/eCM.v031a16
Holmgren L, Glaser A, Pfeifer-Ohlsson S, Ohlsson R (1991) Angiogenesis during human extraembryonic development involves the spatiotemporal control of PDGF ligand and receptor gene expression. Development 113:749–754
Holmgren L, Claesson-welsh L, Heldin C-H, Ohlsson R (1992) The expression of PDGF α- and β-receptors in subpopulations of PDGF-producing cells implicates autocrine stimulatory loops in the control of proliferation in Cytotrophoblasts that have invaded the maternal endometrium. Growth Factors 6:219–231. https://doi.org/10.3109/08977199209026929
Hurtado-Alvarado G, Cabañas-Morales AM, Gómez-Gónzalez B (2014) Pericytes: brain-immune interface modulators. Front Integr Neurosci 7:80. https://doi.org/10.3389/fnint.2013.00080
James AW, Zara JN, Zhang X, Askarinam A, Goyal R, Chiang M, Yuan W, Chang L, Corselli M, Shen J, Pang S, Stoker D, Wu B, Ting K, Péault B, Soo C (2012) Perivascular stem cells: a prospectively purified mesenchymal stem cell population for bone tissue engineering. Stem Cells Transl Med 1:510–519. https://doi.org/10.5966/sctm.2012-0002
Jeynes B (1985) Reactions of granular pericytes in a rabbit cerebrovascular ischemia model. Stroke 16:121–125
Jiang F, Zhao H, Wang L, Guo X, Wang X, Yin G, Hu Y, Li Y, Yao Y (2015) Role of HLA-G1 in trophoblast cell proliferation, adhesion and invasion. Biochem Biophys Res Commun 458:154–160. https://doi.org/10.1016/j.bbrc.2015.01.085
Jones CJP, Desoye G (2011) A new possible function for placental pericytes. Cells Tissues Organs 194:76–84. https://doi.org/10.1159/000322394
Kamouchi M, Ago T, Kitazono T (2011) Brain Pericytes: emerging concepts and functional roles in brain homeostasis. Cell Mol Neurobiol 31(2):175–193. https://doi.org/10.1007/s10571-010-9605-x
Katare R, Riu F, Mitchell K, Gubernator M, Campagnolo P, Cui Y, Fortunato O, Avolio E, Cesselli D, Beltrami AP, Angelini G, Emanueli C, Madeddu P (2011) Transplantation of human pericyte progenitor cells improves the repair of infarcted heart through activation of an angiogenic program involving micro-RNA-132. Circ Res 109:894–906. https://doi.org/10.1161/CIRCRESAHA.111.251546
Kaufmann P, Luckhardt M, Leiser R (1988) Three-dimensional representation of the Fetal vessel system in the human placenta. Trophobl Res 3:113–137. https://doi.org/10.1007/978-1-4615-8109-3_9
Kaufmann P, Mayhew TM, Charnock-Jones DS (2004) Aspects of human Fetoplacental Vasculogenesis and angiogenesis. II. Changes during Normal pregnancy. Placenta 25:114–126. https://doi.org/10.1016/j.placenta.2003.10.009
Khodadi E, Shahrabi S, Shahjahani M, Azandeh S, Saki N (2016) Role of stem cell factor in the placental niche. Cell Tissue Res 366:523–531. https://doi.org/10.1007/s00441-016-2429-3
Kim JA, Tran ND, Li Z, Yang F, Zhou W, Fisher MJ (2006) Brain endothelial Hemostasis regulation by Pericytes. J Cereb Blood Flow Metab 26:209–217. https://doi.org/10.1038/sj.jcbfm.9600181
Kim KR, Sung CO, Kwon TJ, Lee JB, Robboy SJ (2015) Defective pericyte recruitment of villous stromal vessels as the possible etiologic cause of hydropic change in complete hydatidiform mole. PLoS One 10:1–13. https://doi.org/10.1371/journal.pone.0122266
Knox K, Baker JC (2008) Genomic evolution of the placenta using co-option and duplication and divergence. Genome Res 18:695–705. https://doi.org/10.1101/gr.071407.107
Krautler NJ, Kana V, Kranich J, Tian Y, Perera D, Lemm D, Schwarz P, Armulik A, Browning JL, Tallquist M, Buch T, Oliveira-Martins JB, Zhu C, Hermann M, Wagner U, Brink R, Heikenwalder M, Aguzzi A (2012) Follicular dendritic cells emerge from ubiquitous perivascular precursors. Cell 150:194–206. https://doi.org/10.1016/j.cell.2012.05.032
Krueger M, Bechmann I (2010) CNS pericytes: concepts, misconceptions, and a way out. Glia 58:1–10. https://doi.org/10.1002/glia.20898
Kučera T, Vyletěl I, Moravcová M, Krejčí V, Žižka Z, Jirkovská M (2010) Pericyte coverage of fetoplacental vessels in pregnancies complicated by type 1 diabetes mellitus. Placenta 31:1120–1122. https://doi.org/10.1016/j.placenta.2010.09.014
Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D, Mizoguchi T, Wei Q, Lucas D, Ito K, Mar JC, Bergman A, Frenette PS (2013) Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502:637–643. https://doi.org/10.1038/nature12612
Lachenmayer L (1971a) Adrenergic innervation of the umbilical vessels. Light- and fluorescence microscopic studies. Z Zellforsch Mikrosk Anat 120:120–136
Lachenmayer L (1971b) Adrenergic innervation of the umbilical vessels. Zeitschrift für Zellforsch und Mikroskopische Anat 120:120–136. https://doi.org/10.1007/BF00331246
Lash GE, Otun HA, Innes BA, Percival K, Searle RF, Robson SC, Bulmer JN (2010) Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age. Hum Reprod 25:1137–1145. https://doi.org/10.1093/humrep/deq050
Lee LK, Ueno M, Van Handel B, Mikkola HK (2010) Placenta as a newly identified source of hematopoietic stem cells. Curr Opin Hematol 17:313–318. https://doi.org/10.1097/MOH.0b013e328339f295
Leiser R, Kaufmann P (1994) Placental structure: in a comparative aspect. Exp Clin Endocrinol 102:122–134
Leiser R, Kohler T (1983) The blood vessels of the cat girdle placenta. Observations on corrosion casts, scanning electron microscopical and histological studies—I. Maternal vasculature. Anat Embryol (Berl) 167:85–93. https://doi.org/10.1007/BF00304602
Leiser R, Kohler T (1984) The blood vessels of the cat girdle placenta. Observations on corrosion casts, scanning electron microscopical and histological studies—II. Fetal vasculature. Anat Embryol (Berl) 170:209–216. https://doi.org/10.1007/BF00319006
Leiser R, Krebs C, Ebert B, Dantzer V (1997a) Placental vascular corrosion cast studies: a comparison between ruminants and humans. Microsc Res Tech 38:76–87. https://doi.org/10.1002/(SICI)1097-0029(19970701/15)38:1/2<76::AID-JEMT9>3.0.CO;2-S
Leiser R, Krebs C, Klisch K, Ebert B, Dantzer V, Schuler G, Hoffmann B (1997b) Fetal villosity and microvasculature of the bovine placentome in the second half of gestation. J Anat 191:517–527. https://doi.org/10.1017/S0021878297002690
Leiser R, Pfarrer C, Abd-Elnaeim M, Dantzer V (1998) Feto-maternal anchorage in epitheliochorial and endotheliochorial placental types studied by histology and microvascular corrosion casts. Placenta 19:21–39. https://doi.org/10.1016/S0143-4004(98)80031-3
Leno-Durán E, Hatta K, Bianco J, Yamada ÁT, Ruiz-Ruiz C, Olivares EG, Croy BA (2010) Fetal-placental hypoxia does not result from failure of spiral arterial modification in mice. Placenta 31:731–737. https://doi.org/10.1016/j.placenta.2010.06.002
Leonard S, Murrant C, Tayade C, Vandenheuvel M, Watering R, Croy B (2006) Mechanisms regulating immune cell contributions to spiral artery modification—facts and hypotheses—a review. Placenta 27:40–46. https://doi.org/10.1016/j.placenta.2005.11.007
Levéen P, Pekny M, Gebre-Medhin S, Swolin B, Larsson E, Betsholtz C (1994) Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 8:1875–1887
Li C, Houser BL, Nicotra ML, Strominger JL (2009) HLA-G homodimer-induced cytokine secretion through HLA-G receptors on human decidual macrophages and natural killer cells. Proc Natl Acad Sci U S A 106:5767–5772. https://doi.org/10.1073/pnas.0901173106
Lindahl P, Johansson BR, Levéen P, Betsholtz C (1997) Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277:242–245
Lobo SE, Leonel LCPC, Miranda CMFC, Coelho TM, Ferreira GAS, Mess A, Abrão MS, Miglino MA (2016) The placenta as an organ and a source of stem cells and extracellular matrix: a review. Cells Tissues Organs 201:239–252. https://doi.org/10.1159/000443636
Looman C, Sun T, Yu Y, Zieba A, Ahgren A, Feinstein R, Forsberg H, Hellberg C, Heldin CH, Zhang XQ, Forsberg-Nilsson K, Khoo N, Fundele R, Heuchel R (2007) An activating mutation in the PDGF receptor-beta causes abnormal morphology in the mouse placenta. Int J Dev Biol 51:361–370. https://doi.org/10.1387/ijdb.072301cl
Macara L, Kingdom JC, Kaufmann P, Kohnen G, Hair J, More IA, Lyall F, Greer IA (1996) Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms. Placenta 17:37–48
Maier CL, Pober JS (2011) Human placental pericytes poorly stimulate and actively regulate allogeneic CD4 T cell responses. Arterioscler Thromb Vasc Biol 31:183–189. https://doi.org/10.1161/ATVBAHA.110.217117
Maier CL, Shepherd BR, Yi T, Pober JS (2010) Explant outgrowth, propagation and characterization of human pericytes. Microcirculation 17:367–380. https://doi.org/10.1111/j.1549-8719.2010.00038.x
Méndez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, MacArthur BD, Lira SA, Scadden DT, Ma’ayan A, Enikolopov GN, Frenette PS (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466:829–834. https://doi.org/10.1038/nature09262
Mess A, Carter AM (2007) Evolution of the placenta during the early radiation of placental mammals. Comp Biochem Physiol A Mol Integr Physiol 148(4):769–779
Mezrich JD, Fechner JH, Zhang X, Johnson BP, Burlingham WJ, Bradfield CA (2010) An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J Immunol 185:3190–3198. https://doi.org/10.4049/jimmunol.0903670
Moffett A, Loke C (2006) Immunology of placentation in eutherian mammals. Nat Rev Immunol 6:584–594. https://doi.org/10.1038/nri1897
Mónica Brauer M, Smith PG (2015) Estrogen and female reproductive tract innervation: cellular and molecular mechanisms of autonomic neuroplasticity. Auton Neurosci 187:1–17
Moreau JLM, Artap ST, Shi H, Chapman G, Leone G, Sparrow DB, Dunwoodie SL (2014) Cited2 is required in trophoblasts for correct placental capillary patterning. Dev Biol 392:62–79. https://doi.org/10.1016/j.ydbio.2014.04.023
Moser G, Weiss G, Sundl M, Gauster M, Siwetz M, Lang-Olip I, Huppertz B (2017) Extravillous trophoblasts invade more than uterine arteries: evidence for the invasion of uterine veins. Histochem Cell Biol 147:353–366. https://doi.org/10.1007/s00418-016-1509-5
Mossman HW (1987) Vertebrate fetal membranes. Rutgers University Press, New Brunswisk
Muñoz-Fernández R, de la Mata C, Prados A, Perea A, Ruiz-Magaña MJ, Llorca T, Fernández-Rubio P, Blanco O, Abadía-Molina AC, Olivares EG (2018) Human predecidual stromal cells have distinctive characteristics of pericytes: cell contractility, chemotactic activity, and expression of pericyte markers and angiogenic factors. Placenta 61:39–47. https://doi.org/10.1016/j.placenta.2017.11.010
Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409:614–618. https://doi.org/10.1038/35054550
Murrant CL (2014) Intravital imaging of Vasoactivity in the uterine arterial vasculature tree during pregnancy. In: Croy BA, Yamada A, DeMayo F, Lee Adamson S (eds) The guide to investigation of mouse pregnancy. Elseiver, San Diego, CA
Myatt L (1992) Control of vascular resistance in the human placenta. Placenta 13:329–341. https://doi.org/10.1016/0143-4004(92)90057-Z
Nadeau V, Charron J (2014) Essential role of the ERK/MAPK pathway in blood-placental barrier formation. Development 141:2825–2837. https://doi.org/10.1242/dev.107409
Nakagawa S, Deli MA, Nakao S, Honda M, Hayashi K, Nakaoke R, Kataoka Y, Niwa M (2007) Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell Mol Neurobiol 27:687–694. https://doi.org/10.1007/s10571-007-9195-4
Nakamura K, Kamouchi M, Kitazono T, Kuroda J, Matsuo R, Hagiwara N, Ishikawa E, Ooboshi H, Ibayashi S, Iida M (2008) Role of NHE1 in calcium signaling and cell proliferation in human CNS pericytes. AJP Hear Circ Physiol 294:H1700–H1707. https://doi.org/10.1152/ajpheart.01203.2007
Nees S, Weiss DR, Juchem G (2013) Focus on cardiac pericytes. Pflügers Arch - Eur J Physiol 465:779–787. https://doi.org/10.1007/s00424-013-1240-1
Nikolov SD, Schiebler TH (1973) Über das fetale Gefäßsystem der reifen menschlichen Placenta. Zeitschrift für Zellforsch und Mikroskopische Anat 139:333–350. https://doi.org/10.1007/BF00306590
Nomura M, Yamagishi SI, Harada SI, Hayashi Y, Yamashima T, Yamashita J, Yamamoto H (1995) Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J Biol Chem 270:28316–28324. https://doi.org/10.1074/jbc.270.47.28316
Ogino S, Redline RW (2000) Villous capillary lesions of the placenta: distinctions between chorangioma, chorangiomatosis, and chorangiosis. Hum Pathol 31:945–954. https://doi.org/10.1053/hupa.2000.9036
Ohlsson R, Falck P, Hellstrom M, Lindahl P, Bostrom H, Franklin G, Ährlund-Richter L, Pollard J, Soriano P, Betsholtz C (1999) PDGFB regulates the development of the labyrinthine layer of the mouse fetal placenta. Dev Biol 212:124–136. https://doi.org/10.1006/dbio.1999.9306
Oliveira MS, Barreto-Filho JB (2015) Placental-derived stem cells: culture, differentiation and challenges. World J Stem Cells 7:769–775. https://doi.org/10.4252/wjsc.v7.i4.769
Ottersbach K, Dzierzak E (2010) The placenta as a haematopoietic organ. Int J Dev Biol 54:1099–1106. https://doi.org/10.1387/ijdb.093057ko
Pallone TL, Silldorff EP (2001) Pericyte regulation of renal medullary blood flow. Exp Nephrol 9:165–170. doi: 52608
Pallone TL, Silldorff EP, Turner MR (1998) Intrarenal blood flow: microvascular anatomy and the regulation of medullary perfusion. Clin Exp Pharmacol Physiol 25:383–392
Pallone TL, Zhang Z, Rhinehart K (2003) Physiology of the renal medullary microcirculation. Am J Physiol Ren Physiol 284:F253–F266. https://doi.org/10.1152/ajprenal.00304.2002
Pan S-Y, Chang Y-T, Lin S-L (2014) Microvascular pericytes in healthy and diseased kidneys. Int J Nephrol Renovasc Dis 7:39–48. https://doi.org/10.2147/IJNRD.S37892
Pereira FTV, Oliveira LJ, Barreto RSN, Mess A, Perecin F, Bressan FF, Mesquita LG, Miglino MA, Pimentel JR, Neto PF, Meirelles FV (2013) Fetal-maternal interactions in the Synepitheliochorial placenta using the eGFP cloned cattle model. PLoS One 8:e64399. https://doi.org/10.1371/journal.pone.0064399
Persson E, Rodriguez-Martinez H (1997) Immunocytochemical localization of growth factors and intermediate filaments during the establishment of the porcine placenta. Microsc Res Tech 38:165–175. https://doi.org/10.1002/(SICI)1097-0029(19970701/15)38:1/2<165::AID-JEMT17>3.0.CO;2-N
Pfister F, Przybyt E, Harmsen MC, Hammes H-P (2013) Pericytes in the eye. Pflügers Arch Eur J Physiol 465:789–796. https://doi.org/10.1007/s00424-013-1272-6
Prazeres PHDM, Sena IFG, IDT B, de Azevedo PO, Andreotti JP, de Paiva AE, de Almeida VM, de Paula Guerra DA, Pinheiro Dos Santos GS, Mintz A, Delbono O, Birbrair A (2017) Pericytes are heterogeneous in their origin within the same tissue. Dev Biol 427:6–11. https://doi.org/10.1016/j.ydbio.2017.05.001
Ramsey EM, Martin CB, Donner MW (1967) Fetal and maternal placental circulations. Simultaneous visualization in monkeys by radiography. Am J Obstet Gynecol 98:419–423
Resta L, Capobianco C, Marzullo A, Piscitelli D, Sanguedolce F, Schena FP, Gesualdo L (2006) Confocal laser scanning microscope study of terminal villi vessels in Normal term and pre-eclamptic placentas. Placenta 27:735–739. https://doi.org/10.1016/j.placenta.2005.07.006
Rhodin J (1968) Ultrastructure of mammalian venous capillaries, venules, and small collecting veins. J Ultrastruct Res 25:452–500. https://doi.org/10.1016/S0022-5320(68)80098-X
Rizzo R, Lo Monte G, Bortolotti D, Graziano A, Gentili V, Di Luca D, Marci R (2015) Impact of soluble HLA-G levels and endometrial NK cells in uterine flushing samples from primary and secondary unexplained infertile women. Int J Mol Sci 16:5510–5516. https://doi.org/10.3390/ijms16035510
Robin C, Bollerot K, Mendes S, Haak E, Crisan M, Cerisoli F, Lauw I, Kaimakis P, Jorna R, Vermeulen M, Kayser M, van der Linden R, Imanirad P, Verstegen M, Nawaz-Yousaf H, Papazian N, Steegers E, Cupedo T, Dzierzak E (2009) Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Cell Stem Cell 5(4):385–395. https://doi.org/10.1016/j.stem.2009.08.020
Rodriguez-Martinez H, Persson E, Hurst M, Stanchev P (1992) Immunohistochemical localization of platelet-derived growth factor receptors in the porcine uterus during the oestrous cycle and pregnancy. J Vet Med Ser A 39:1–10. https://doi.org/10.1111/j.1439-0442.1992.tb00151.x
Rouget C-MB (1873) Mémoire sur le développement, la structure et les proprietés physiologiques des capillaires sanguins et lymphatiques. Arch Psys 5:603–610
Rucker HK, Wynder HJ, Thomas WE (2000) Cellular mechanisms of CNS pericytes. Brain Res Bull 51:363–369
Sato K, Yamashita N, Baba M, Matsuyama T (2003) Modified myeloid dendritic cells act as regulatory dendritic cells to induce anergic and regulatory T cells. Blood 101:3581–3589. https://doi.org/10.1182/blood-2002-09-2712
Shimizu F, Sano Y, Maeda T, Abe M, Nakayama H, Takahashi R, Ueda M, Ohtsuki S, Terasaki T, Obinata M, Kanda T (2008) Peripheral nerve pericytes originating from the blood-nerve barrier expresses tight junctional molecules and transporters as barrier-forming cells. J Cell Physiol 217:367–380. https://doi.org/10.1002/jcp.21508
Sims DE (2000) Diversity within Pericytes. Clin Exp Pharmacol Physiol 27:842–846. https://doi.org/10.1046/j.1440-1681.2000.03343.x
Soriano P (1994) Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev 8:1888–1896
Stark K, Eckart A, Haidari S, Tirniceriu A, Lorenz M, Von Brühl ML, Gärtner F, Khandoga AG, Legate KR, Pless R, Hepper I, Lauber K, Walzog B, Massberg S (2013) Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and “instruct” them with pattern-recognition and motility programs. Nat Immunol 14(1):41–51. https://doi.org/10.1038/ni.2477
Talwadekar MD, Kale VP, Limaye LS (2015) Placenta-derived mesenchymal stem cells possess better immunoregulatory properties compared to their cord-derived counterparts–a paired sample study. Sci Rep 5:15784. https://doi.org/10.1038/srep15784
Thanabalasundaram G, Schneidewind J, Pieper C, Galla H-J (2011) The impact of pericytes on the blood-brain barrier integrity depends critically on the pericyte differentiation stage. Int J Biochem Cell Biol 43(9):1284–1293. https://doi.org/10.1016/j.biocel.2011.05.002
Thomas WE (1999) Brain macrophages: on the role of pericytes and perivascular cells. Brain Res Brain Res Rev 31:42–57
Thornburg KL, Bagby SP, Giraud GD (2006) Maternal adaptation to pregnancy. In: Neill JD (ed) Knobil and Neill’s physiology of reproduction. Elseiver, Amsterdam
Tilburgs T, Crespo ÂC, van der Zwan A, Rybalov B, Raj T, Stranger B, Gardner L, Moffett A, Strominger JL (2015) Human HLA-G+ extravillous trophoblasts: immune-activating cells that interact with decidual leukocytes. Proc Natl Acad Sci 112:7219–7224. https://doi.org/10.1073/pnas.1507977112
Tu Z, Li Y, Smith DS, Sheibani N, Huang S, Kern T, Lin F (2011) Retinal pericytes inhibit activated T cell proliferation. Invest Ophthalmol Vis Sci 52:9005–9010. https://doi.org/10.1167/iovs.11-8008
Ueno H, Weissman IL (2010) The origin and fate of yolk sac hematopoiesis: application of chimera analyses to developmental studies. Int J Dev Biol 54:1019–1031. https://doi.org/10.1387/ijdb.093039hu
van der Heijden GW, Dieker JW, Derijck AAHA, Muller S, Berden JHM, Braat DDM, van der Vlag J, de Boer P (2005) Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev 122:1008–1022. https://doi.org/10.1016/j.mod.2005.04.009
Verbeek MM, Westphal JR, Ruiter DJ, de Waal RM (1995) T lymphocyte adhesion to human brain pericytes is mediated via very late antigen-4/vascular cell adhesion molecule-1 interactions. J Immunol 154:5876–5884
Vogel P (2005) The current molecular phylogeny of eutherian mammals challenges previous interpretations of placental evolution. Placenta 26:591–596. https://doi.org/10.1016/j.placenta.2004.11.005
Wehrenberg WB, Chaichareon DP, Dierschke DJ, Rankin JH, Ginther OJ (1977) Vascular dynamics of the reproductive tract in the female rhesus monkey: relative contributions of ovarian and uterine arteries. Biol Reprod 17:148–153
Wooding FBP, Burton GJ (2008a) Comparative placentation: structures, functions and evolution. Springer, New York
Wooding P, Burton GJ (2008b) Haemochorial placentation: mouse, rabbit, man, apes, monkeys. In: Comparative placentation. Springer, Berlin, pp 185–230
Wooding FBP, Flint APF (1994) Placentation. In: Lamming GE (ed) Marshall’s physiology of reproduction, 4th edn. Springer-Science, London, pp 233–429
Wynn RM (1974) Ultrastructural development of the human decidua. Am J Obstet Gynecol 118(5):652–670. https://doi.org/10.1016/S0002-9378(16)33740-1
Yamada AT, Bianco JR, Lippe EMO, Degaki KY, Dalmorin AF, Edwards AK, Lima PDA, Paffaro VA (2014) Unique features of endometrial dynamics during pregnancy. In: Anne Croy B, Yamada A, DeMayo F, Lee Adamson S (eds) The guide to investigation of mouse pregnancy. Elseiver, San Diego, CA
Yamagishi S, Kawakamia T, Fujimoria H, Yonekura H, Tanaka N, Yamamoto Y, Urayama H, Watanabe Y, Yamamoto H (1999a) Insulin stimulates the growth and tube formation of human microvascular endothelial cells through autocrine vascular endothelial growth factor. Microvasc Res 57:329–339
Yamagishi S, Yonekura H, Yamamoto Y, Fujimori H, Sakurai S, Tanaka N, Yamamoto H (1999b) Vascular endothelial growth factor acts as a pericyte mitogen under hypoxic conditions. Lab Investig 79(4):501–509
Yonekura H, Sakurai S, Liu X, Migita H, Wang H, Yamagishi S, Nomura M, Abedin MJ, Unoki H, Yamamoto Y, Yamamoto H (1999) Placenta growth factor and vascular endothelial growth factor B and C expression in microvascular endothelial cells and Pericytes. J Biol Chem 274:35172–35178
Zebardast N, Lickorish D, Davies JE (2010) Human umbilical cord perivascular cells (HUCPVC): a mesenchymal cell source for dermal wound healing. Organogenesis 6:197–203. https://doi.org/10.4161/org.6.4.12393
Zhang EG, Burton GJ, Smith SK, Charnock-Jones DS (2002) Placental vessel adaptation during gestation and to high altitude: changes in diameter and perivascular cell coverage. Placenta 23(10):751–762. https://doi.org/10.1016/S0143-4004(02)90856-8
Zhao H, Feng J, Seidel K, Shi S, Klein O, Sharpe P, Chai Y (2014) Secretion of shh by a neurovascular bundle niche supports mesenchymal stem cell homeostasis in the adult mouse incisor. Cell Stem Cell 14:160–173. https://doi.org/10.1016/j.stem.2013.12.013
Zhu Y, Yang Y, Zhang Y, Hao G, Liu T, Wang L, Yang T, Wang Q, Zhang G, Wei J, Li Y (2014) Placental mesenchymal stem cells of fetal and maternal origins demonstrate different therapeutic potentials. Stem Cell Res Ther 5:48. https://doi.org/10.1186/scrt436
Zygmunt M, Herr F, Münstedt K, Lang U, Liang OD (2003) Angiogenesis and vasculogenesis in pregnancy. Eur J Obstet Gynecol Reprod Biol 110(Suppl 1):S10–S18
Acknowledgments
Alexander Birbrair is supported by a grant from Instituto Serrapilheira/Serra-1708-15285, a grant from Pró-reitoria de Pesquisa/Universidade Federal de Minas Gerais (PRPq/UFMG) (Edital 05/2016), a grant from the National Institute of Science and Technology in Theranostics and Nanobiotechnology (CNPq/CAPES/FAPEMIG, Process No. 465669/2014-0), a grant from FAPEMIG [Rede Mineira de Engenharia de Tecidos e Terapia Celular (REMETTEC, RED-00570-16)], and a grant from FAPEMIG [Rede De Pesquisa Em Doenças Infecciosas Humanas E Animais Do Estado De Minas Gerais (RED-00313-16)].
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Barreto, R.S.N., Romagnolli, P., Cereta, A.D., Coimbra-Campos, L.M.C., Birbrair, A., Miglino, M.A. (2019). Pericytes in the Placenta: Role in Placental Development and Homeostasis. In: Birbrair, A. (eds) Pericyte Biology in Different Organs. Advances in Experimental Medicine and Biology, vol 1122. Springer, Cham. https://doi.org/10.1007/978-3-030-11093-2_8
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