Studies of the dynamics of nuclear clustering in human syncytiotrophoblast

Reproduction

Volumn 151, Issue 6, 2016, Pages 657-671

  Calvert, S J ^a,b   Longtine, M S ^c   Cotter, S ^a   Jones, C J P ^a,b   Sibley, C P ^a,b   Aplin, J D ^a,b   Nelson, D M ^c   Heazell, A E P ^a,b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b ST MARY S HOSPITAL   (United Kingdom)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHORIONIC GONADOTROPIN; CYTOKERATIN 7; INTERMEDIATE FILAMENT PROTEIN; OXYGEN;

ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL MEMBRANE; CELL MOTION; CELL NUCLEUS; CHORION VILLUS; COMPUTER MODEL; CONDITIONED MEDIUM; CONTROLLED STUDY; CYTOSKELETON; CYTOTROPHOBLAST; EMBRYO; EXPLANT; FEMALE; GONADOTROPIN RELEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; OXYGEN CONCENTRATION; OXYGENATION; PLACENTA; PREGNANCY DISORDER; PRIORITY JOURNAL; SYNCYTIAL NUCLEAR AGGREGATE; SYNCYTIOTROPHOBLAST; TROPHOBLAST; FLUORESCENT ANTIBODY TECHNIQUE; PREGNANCY; TIME LAPSE IMAGING; ULTRASTRUCTURE;

CELL MEMBRANE; CELL NUCLEUS; CYTOSKELETON; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; PLACENTA; PREGNANCY; TIME-LAPSE IMAGING; TROPHOBLASTS;

EID: 84973293281     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-15-0544     Document Type: Article

References (69)

1. Al-Allaf L, Jarjees M & Al-Nuaimy W 2008 Histological changes of human placenta in prolonged pregnancy. JBMS Journal of the Bahrain Medical Society 20 60-67.
2. Aplin JD 2010 Developmental cell biology of human villous trophoblast: current research problems. International Journal of Developmental Biology 54 323-329. (doi:10.1387/ijdb.082759ja)
3. Arnholdt H, Meisel F, Fandrey K & Löhrs U 1991 Proliferation of villous trophoblast of the human placenta in normal and abnormal pregnancies. Virchows Archiv B: Cell Pathology Including Molecular Pathology 60 365-372. (doi:10.1007/BF02899568)
4. Askelund K & Chamley L 2011 Trophoblast deportation part I: review of the evidence demonstrating trophoblast shedding and deportation during human pregnancy. Placenta 32 716-723. (doi:10.1016/j.placenta.2011.07.081)
5. Audette MC, Greenwood SL, Sibley CP, Jones CJP, Challis JRG, Matthews SG & Jones RL 2010 Dexamethasone stimulates placental system A transport and trophoblast differentiation in term villous explants. Placenta 31 97-105. (doi:10.1016/j.placenta.2009.11.016)
6. Beham A, Denk H & Desoye G 1988 The distribution of intermediate filament proteins, actin and desmoplakins in human placental tissue as revealed by polyclonal and monoclonal antibodies. Placenta 9 479-492. (doi:10.1016/0143-4004(88)90020-3)
7. Bianchi DW 2004 Circulating fetal DNA: its origin and diagnostic potential - a review. Placenta 25 (Supplement A) S93-S101. (doi:10.1016/j.placenta.2004.01.005)
8. Boyd JD & Hamilton WJ 1967 Development and structure of the human placenta from the end of the 3rd month of gestation. Journal of Obstetrics and Gynaecology of the British Commonwealth 74 161-226. (doi:10.1111/bjo.1967.74.issue-2)
9. Boyd JD & Hamilton WJ 1970 The human placenta. Cambridge, UK: Heffer.
10. Bradbury FM & Ockleford CD 1990 A confocal and conventional epifluorescence microscope study of the intermediate filaments in chorionic villi. Journal of Anatomy 169 173-187.
11. Burton GJ & Jones CJP 2009 Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta. Taiwanese Journal of Obstetrics and Gynecology 48 28-37. (doi:10.1016/S1028-4559(09)60032-2)
12. Calvert SJ, Jones CJP, Sibley CP, Aplin JD & Heazell AEP 2013 Analysis of syncytial nuclear aggregates in preeclampsia shows increased sectioning artefacts and decreased inter-villous bridges compared to healthy placentas. Placenta 34 1251-1254. (doi:10.1016/j.placenta.2013.10.001)
13. Cantle SJ, Kaufmann P, Luckhardt M & Schweikhart G 1987 Interpretation of syncytial sprouts and bridges in the human placenta. Placenta 8 221-234. (doi:10.1016/0143-4004(87)90046-4)
14. Carvalho L, Stuhmer J, Bois JS, Kalaidzidis Y, Lecaudey V & Heisenberg CP 2009 Control of convergent yolk syncytial layer nuclear movement in zebrafish. Development 136 1305-1315. (doi:10.1242/dev.026922)
15. Chaddha V, Viero S, Huppertz B & Kingdom J 2004 Developmental biology of the placenta and the origins of placental insufficiency. Seminars in Fetal and Neonatal Medicine 9 357-369. (doi:10.1016/j.siny.2004.03.006)
16. Chamley LW, Holland OJ, Chen Q, Viall CA, Stone PR & Abumaree M 2014 Review: where is the maternofetal interface? Placenta 35 S74-S80. (doi:10.1016/j.placenta.2013.10.014)
17. Chen B, Nelson DM & Sadovsky Y 2006 N-myc down-regulated gene 1 modulates the response of term human trophoblasts to hypoxic injury. Journal of Biological Chemistry 281 2764-2772. (doi:10.1074/jbc.M507330200)
18. Chen B, Longtine MS & Nelson DM 2013 Pericellular oxygen concentration of cultured primary human trophoblasts. Placenta 34 106-109. (doi:10.1016/j.placenta.2012.11.011)
19. Coleman SJ, Gerza L, Jones CJP, Sibley CP, Aplin JD & Heazell AEP 2013 Syncytial nuclear aggregates in normal placenta show increased nuclear condensation, but apoptosis and cytoskeletal redistribution are uncommon. Placenta 34 449-455. (doi:10.1016/j.placenta.2013.02.007)
20. Corrêa RRM, Gilio DB, Cavellani CL, Paschoini MC, Oliveira FA, Peres LC, Reis MA, Teixeira VPA & Castro ECC 2008 Placental morphometrical and histopathology changes in the different clinical presentations of hypertensive syndromes in pregnancy. Archives of Gynecology and Obstetrics 277 201-206. (doi:10.1007/s00404-007-0452-z)
21. Crocker IP, Tansinda DM & Baker PN 2004 Altered cell kinetics in cultured placental villous explants in pregnancies complicated by pre-eclampsia and intrauterine growth restriction. Journal of Pathology 204 1118. (doi:10.1002/(ISSN)1096-9896)
22. Douglas GC & King BF 1993 Colchicine inhibits human trophoblast differentiation in vitro. Placenta 14 187-201. (doi:10.1016/S0143-4004(05)80260-7)
23. Fogarty NME, Ferguson-Smith AC & Burton GJ 2013 Syncytial knots (Tenney-Parker changes in the human placenta: evidence of loss of transcriptional activity and oxidative damage. American Journal of Pathology 183 144-152. (doi:10.1016/j.ajpath.2013.03.016)
24. Frendo JL, Cronier L, Bertin G, Guibourdenche J, Vidaud M, Evain-Brion D & Malassine A 2003 Involvement of connexin 43 in human trophoblast cell fusion and differentiation. Journal of Cell Science 116 3413-3421. (doi:10.1242/jcs.00648)
25. Friederich E, Kreis TE & Louvard D 1993 Villin-induced growth of microvilli is reversibly inhibited by cytochalasin D. Journal of Cell Science 105 765-775.
26. Frock RL, Kudlow BA, Evans AM, Jameson SA, Hauschka SD & Kennedy BK 2006 Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes & Development 20 486-500. (doi:10.1101/gad.1364906)
27. Garcia-Lloret MI, Yui J, Winkler-Lowen B & Guilbert LJ 1996 Epidermal growth factor inhibits cytokine-induced apoptosis of primary human trophoblasts. Journal of Cellular Physiology 167 324-332. (doi:10.1002/(ISSN)1097-4652)
28. Germain SJ, Sacks GP, Soorana SR, Sargent IL & Redman CW 2007 Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. Journal of Immunology 178 5949-5956. (doi:10.4049/jimmunol.178.9.5949)
29. Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CWG, Sargent IL & von Dadelszen P 2006 Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta 27 5661. (doi:10.1016/j.placenta.2004.11.007)
30. Hahn S, Huppertz B & Holzgreve W 2005 Fetal cells and cell free fetal nucleic acids in maternal blood: new tools to study abnormal placentation? Placenta 26 515-526. (doi:10.1016/j.placenta.2004.10.017)
31. Heazell A, Harris L, Forbes K & Crocker I 2006 Placental cell turnover in health and disease. Reviews in Gynaecological and Perinatal Practice 6 8086. (doi:10.1016/j.rigapp.2005.12.003)
32. Heazell AEP, Moll SJ, Jones CJP, Baker PN & Crocker IP 2007 Formation of syncytial knots is increased by hyperoxia, hypoxia and reactive oxygen species. Placenta 28 S33-S40. (doi:10.1016/j.placenta.2006.10.007)
33. Heazell AEP, Buttle HR, Baker PN & Crocker IP 2008a Altered expression of regulators of caspase activity within trophoblast of normal pregnancies and pregnancies complicated by preeclampsia. Reproductive Sciences 15 1034-1043. (doi:10.1177/1933719108322438)
34. Heazell AEP, Lacey HA, Jones CJP, Huppertz B, Baker PN & Crocker IP 2008b Effects of oxygen on cell turnover and expression of regulators of apoptosis in human placental trophoblast. Placenta 29 175-186. (doi:10.1016/j.placenta.2007.11.002)
35. Humphrey RG, Sonnenberg-Hirche C, Smith SD, Hu C, Barton A, Sadovsky Y & Nelson DM 2008 Epidermal growth factor abrogates hypoxia-induced apoptosis in cultured human trophoblasts through phosphorylation of BAD Serine 112. Endocrinology 149 2131-2137. (doi:10.1210/en.2007-1253)
36. Huppertz B, Kaufmann P & Kingdom J 2002 Trophoblast turnover in health and disease. Fetal and Maternal Medicine Review 13 103-118. (doi:10.1017/S0965539502000220)
37. Huppertz B, Kingdom J, Caniggia I, Desoye G, Black S, Korr H & Kaufmann P 2003 Hypoxia favours necrotic versus apoptotic shedding of placental syncytiotrophoblast into the maternal circulation. Placenta 24 181-190. (doi:10.1053/plac.2002.0903)
38. Huppertz B, Kadyrov M & Kingdom JCP 2006 Apoptosis and its role in the trophoblast. American Journal of Obstetrics and Gynecology 195 2939. (doi:10.1016/j.ajog.2005.07.039)
39. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN & Burton GJ 2000 Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. American Journal of Pathology 157 2111-2122. (doi:10.1016/S0002-9440(10)64849-3)
40. Johnstone ED, Sibley C P, Lowen B & Guilbert LJ 2005 Epidermal growth factor stimulation of trophoblast differentiation requires MAPK11/14 (p38 MAP kinase) activation. Biology of Reproduction 73 1282-1288. (doi:10.1095/biolreprod.105.044206)
41. Jones CJP & Fox H 1977 Syncytial knots and intervillous bridges in the human placenta: an ultrastructural study. Journal of Anatomy 124 275-286.
42. Jones CJP & Fox H 1978 Ultrastructure of the placenta in prolonged pregnancy. Journal of Pathology 126 173-179. (doi:10.1002/path.1711260306)
43. Jones CJP, Mosley SM, Jeffrey IJM & Stoddart RW 1987 Elimination of the non-specific binding of avidin to tissue sections. Histochemical Journal 19 264-268. (doi:10.1007/BF01675685)
44. Kim DI, Birendra KC & Roux KJ 2015 Making the LINC: SUN and KASH protein interactions. Biological Chemistry 396 295-310. (doi:10.1515/hsz-2014-0267)
45. Kliman HJ, Nestler JE, Sermasi E, Sanger JM & Strauss JF 1986 Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 118 1567-1582. (doi:10.1210/endo-118-4-1567)
46. Longtine M, Chen B, Odibo A, Zhong Y & Nelson D 2012a Caspase-mediated apoptosis of trophoblasts in term human placental villi is restricted to cytotrophoblasts and absent from the multinucleated syncytiotrophoblast. Reproduction 143 107-121. (doi:10.1530/REP-11-0340)
47. Longtine MS, Barton A, Chen B & Nelson DM 2012b Live-cell imaging shows apoptosis initiates locally and propagates as a wave throughout syncytiotrophoblasts in primary cultures of human placental villous trophoblasts. Placenta 33 971-976. (doi:10.1016/j.placenta.2012.09.013)
48. Malone CJ, Fixsen WD, Horvitz HR & Han M 1999 UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development 126 3171-3181.
49. Mayhew TM 2014 Turnover of human villous trophoblast in normal pregnancy: what do we know and what do we need to know? Placenta 35 229-240. (doi:10.1016/j.placenta.2014.01.011)
50. Mayhew TM, Leach L, McGee R, Ismail WW, Myklebust R & Lammiman MJ 1999 Proliferation, differentiation and apoptosis in villous trophoblast at 13-41 weeks of gestation (including observations on annulate lamellae and nuclear pore complexes). Placenta 20 407-422. (doi:10.1053/plac.1999.0399)
51. McKinnon T, Chakraborty C, Gleeson LM, Chidiac P & Lala PK 2001 Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G Protein(s) and phosphorylation of MAPK. Journal of Clinical Endocrinology & Metabolism 86 3665-3674. (doi:10.1210/jcem.86.8.7711)
52. 2 consumption in monolayer cell cultures. Respiration Physiology 100 101-106. (doi:10.1016/0034-5687(94)00125-J)
53. Moll SJ, Jones CJP, Crocker IP, Baker PN & Heazell AEP 2007 Epidermal growth factor rescues trophoblast apoptosis induced by reactive oxygen species. Apoptosis 12 1611-1622. (doi:10.1007/s10495-007-0092-6)
54. Morrish DW, Bhardwaj D, Dabbagh LK, Marusyk H & Siy O 1987 Epidermal growth factor induces differentiation and secretion of human chorionic gonadotropin and placental lactogen in normal human placenta. Journal of Clinical Endocrinology & Metabolism 65 1282-1290. (doi:10.1210/jcem-65-6-1282)
55. Morrish DW, Dakour J, Li H, Xiao J, Miller R, Sherburne R, Berdan RC & Guilbert LJ 1997 In vitro cultured human term cytotrophoblast: a model for normal primary epithelial cells demonstrating a spontaneous differentiation programme that requires EGF for extensive development of syncytium. Placenta 18 577-585. (doi:10.1016/0143-4004(77)90013-3)
56. Pettersen EO, Larsen LH, Ramsing NB & Ebbensen P 2005 Pericellular oxygen depletion during ordinary tissue culturing, measured with oxygen microsensors. Cell Proliferation 38 257-267. (doi:10.1111/cpr.2005.38.issue-4)
57. Pringle KG, Kind KL, Sferruzzi-Perri AN, Thompson JG & Roberts CT 2010 Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy. Human Reproduction Update 16 415-431. (doi:10.1093/humupd/dmp046)
58. Rhee S, Jiang H, Ho C-H & Grinnell F 2007 Microtubule function in fibroblast spreading is modulated according to the tension state of cell-matrix interactions. PNAS 104 5425-5430. (doi:10.1073/pnas.0608030104)
59. Richard J, Leikina E & Chernomordik L 2009 Cytoskeleton reorganization in infuenza hemagglutinin-initiated syncytium formation. Biochimica et Biophysica Acta (BBA) - Biomembranes 1788 450-457. (doi:10.1016/j. bbamem.2008.09.014)
60. Rote NS, Wei B-R, Xu C, Luo L 2010 Caspase 8 and human villous cytotrophoblast differentiation. Placenta 31 8996. (doi:10.1016/j.placenta.2009.12.014)
61. Schneider CA, Rasband WS & Eliceiri KW 2012 NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9 671-675. (doi:10.1038/nmeth.2089)
62. Siman CM, Sibley CP, Jones CJP, Turner MA & Greenwood SL 2001 The functional regeneration of syncytiotrophoblast in cultured explants of term placenta. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 280 R1116-R1122.
63. Starr DA 2007 Communication between the cytoskeleton and the nuclear envelope to position the nucleus. Molecular Biosystems 3 583-589. (doi:10.1039/b703878j)
64. Sullivan M, Galea P & Latif S 2006 What is the appropriate oxygen tension for in vitro culture? Molecular Human Reproduction 12 653. (doi:10.1093/molehr/gal081)
65. Tarjan R 1972 Depth-first search and linear graph algorithms. SIAM Journal on Computing 1 146-160. (doi:10.1137/0201010)
66. Tenney B & Parker F 1940 The placenta in toxemia of pregnancy. American Journal of Obstetrics and Gynecology 39 1000-1005.
67. Tuuli MG, Longtine MS & Nelson DM 2011 Review: oxygen and trophoblast biology - a source of controversy. Placenta 32 S109-S118. (doi:10.1016/j.placenta.2010.12.013)
68. Uhlenbeck GE & Ornstein LS 1930 On the theory of the Brownian motion. Physical Review 36 823-841. (doi:10.1103/PhysRev.36.823)
69. Zieve GW, Turnbull D, Mullins JM & McIntosh JR 1980 Production of large numbers of mitotic mammalian cells by use of the reversible microtubule inhibitor Nocodazole. Experimental Cell Research 126 397-405. (doi:10.1016/0014-4827(80)90279-7)