The effect of hypoxia on human trophoblast in culture: Morphology, glucose transport and metabolism
Open accessAbstract
The response to hypoxia of trophoblast isolated from term placenta and maintained in culture was studied. Trophoblast exposed to normoxic (PO2 120-130 mmHg) or hypoxic (PO2 12-14 mmHg) conditions were examined by electron microscopy. After 48 h, the cytoplasm of the hypoxic cells was more electron-dense with increased numbers of mitochondria, lysosomes and vacuoles. Compared to normoxic cells, the surface microvilli of the hypoxic cells were sparse, short and unevenly distributed. [3H]thymidine incorporation by both hypoxic and normoxic trophoblast fell rapidly and equivalently after 2 days in culture. The percentage of cells with the proliferation-associated nuclear antigen, Ki 67, also decreased, but remained higher in hypoxic cells suggesting that hypoxia retarded completion of the cell cycle (normoxia, 10.80 +/- 2.51 s.e.; hypoxia, 19.87 +/- 2.73, P < 0.01). Glucose consumption was elevated in hypoxia (3.73 +/- 1.07 s.e. mumol/10(6) cells/24 h) as compared to normoxia (1.46 +/- 0.83, P = 0.01). Although lactate production was consistently higher in hypoxia, the difference was not statistically significant (hypoxia 5.38 +/- 1.54 mumol/10(6) cells/24 h versus normoxia, 1.52 +/- 0.29, P = 0.07). After 48 h, uptake of [3H]2-deoxglucose ([3H]2DG) by hypoxic cells was reduced to 12 per cent +/- 4.3 s.e. of that in normoxic cells; return to normoxia resulted in recovery within 10 min. Lineweaver-Burk plots of [3H]2DG uptake indicated high affinity (KM 2.2 +/- 0.4 x 10(-4) M) and low affinity transporters (KM 4.5 +/- 1.6 x 10(-3) M). Northern blot analysis identified mRNA for GLUT1 and GLUT3. In hypoxia, steady-state GLUT1 and GLUT3 mRNA were approximately three- and 10-fold higher than in normoxia respectively. Inhibitors of oxidative metabolism of glucose increased the uptake of [3H]2DG within 2 h, whereas hypoxia reduced uptake. Hence, trophoblast in culture survives in extreme hypoxia, but manifests striking changes in morphology and in glucose metabolism and transport. Completion of cell cycle appears to be retarded.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the human placenta in vitro, acute hypoxia leads to upregulated expression of GLUT1 and GLUT3.
“In the human placenta in vitro, acute hypoxia leads to upregulated expression of the GLUT1 and GLUT3 (178, 249).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [178]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease
Chirgwin, J. M., Przybyla, A., MacDonald, R. J., & Rutter, W. J. (1979) · Biochemistry · doi:10.1021/bi00591a005 · Cited by 21,725 · see citing works
Gerdes, J., Lemke, H., Baisch, H., Wacker, H. H., Schwab, U., & Stein, H. (1984) · The Journal of Immunology · doi:10.4049/jimmunol.133.4.1710 · Cited by 4,173 · see citing works
Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1.
Semenza, G., Roth, P. H., Fang, H. M., & Wang, G. L. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)31580-6 · Cited by 1,892 · see citing works
Kliman, H. J., Nestler, J. E., SERMASI, E., Sanger, J. M., & Strauss, J. F. (1986) · Endocrinology · doi:10.1210/endo-118-4-1567 · Cited by 1,572 · see citing works
Mammalian Facilitative Glucose Transporter Family: Structure and Molecular Regulation
Pessin, J. E., & Bell, G. I. (1992) · Annual Review of Physiology · doi:10.1146/annurev.ph.54.030192.004403 · Cited by 422 · see citing works
Key, G., Becker, M., Baron, B., Duchrow, M., Schlüter, C., Flad, H. D., & Gerdes, J. (1993) · PubMed · Cited by 376 · see citing works
Jansson, T., Wennergren, M., & Illsley, N. P. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.77.6.8263141 · Cited by 320 · see citing works
An ultrastructural and ultrahistochemical study of the human placenta in maternal pre-eclampsia
Jones, C., & Fox, H. (1980) · Placenta · doi:10.1016/s0143-4004(80)80016-6 · Cited by 237 · see citing works
Burant, C., & Bell, G. I. (1992) · Biochemistry · doi:10.1021/bi00157a032 · Cited by 199 · see citing works
Hypoxia induces glucose transporter expression in endothelial cells
Loike, J. D., Cao, L., Brett, J., Ogawa, S., Silverstein, S. C., & Stern, D. (1992) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1992.263.2.c326 · Cited by 179 · see citing works
Tissue distribution of the human GLUT3 glucose transporter
Haber, R. S., Weinstein, S. P., O'Boyle, E., & Morgello, S. (1993) · Endocrinology · doi:10.1210/endo.132.6.8504756 · Cited by 165 · see citing works
Effects of Hypoxia-Ischemia on GLUT1 and GLUT3 Glucose Transporters in Immature Rat Brain
Vannucci, S. J., Seaman, L. B., & Vannucci, R. C. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199601000-00009 · Cited by 155 · see citing works
THE METABOLISM OF HUMAN PLACENTA IN VITRO
Villee, C. A. (1953) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)77237-8 · Cited by 155 · see citing works
Transfer of Amino Acids across the In Vitro Perfused Human Placenta
Schneider, H., Kh, M., & Dancis, J. (1979) · Pediatric Research · doi:10.1203/00006450-197904000-00005 · Cited by 96 · see citing works
Self-citationLittle missed markers and Ki-67.
Schwarting, R. (1993) · PubMed · Cited by 83 · see citing works
Shetty, M., Loeb, J., & Ismail‐Beigi, F. (1992) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1992.262.2.c527 · Cited by 78 · see citing works
Self-citationEndothelial cell hypoxia associated proteins are cell and stress specific
Graven, K. K., Zimmerman, L. H., Dickson, E. W., Weinhouse, G. L., & Farber, H. W. (1993) · Journal of Cellular Physiology · doi:10.1002/jcp.1041570314 · Cited by 71 · see citing works
MacLennan, A. H., Sharp, F., & Shaw‐Dunn, J. (1972) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1972.tb15763.x · Cited by 70 · see citing works
MacLennan, A. H., Sharp, F., & Shaw‐Dunn, J. (1972) · PubMed · Cited by 67 · see citing works
The effect of hypoxia on term trophoblast: Hormone synthesis and release
Esterman, A. L., Finlay, T. H., & Dancis, J. (1996) · Placenta · doi:10.1016/s0143-4004(96)90041-7 · Cited by 61 · see citing works
Self-citationCOMPARISON OF PLACENTAS FROM TWO SOCIOECONOMIC GROUPS. I. MORPHOMETRY
Laga, E. M., Driscoll, S. G., & Munro, H. N. (1972) · PEDIATRICS · doi:10.1542/peds.50.1.24 · Cited by 58 · see citing works
In vitro perfusion of human placenta
Challier, J.-C., Schneider, H., & Dancis, J. (1976) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(76)90287-8 · Cited by 57 · see citing works
Self-citationPlacenta as a Model and a Source
(1989) · Springer eBooks · doi:10.1007/978-1-4613-0823-2 · Cited by 49 · see citing works
Illsley, N. P., Aarnoudse, J. G., Penfold, P., Bardsley, S. E., Coade, S. B., Stacey, T. E., & Hytten, F. E. (1984) · Placenta · doi:10.1016/s0143-4004(84)80031-4 · Cited by 46 · see citing works
Induction of GLUT1 mRNA in response to inhibition of oxidative phosphorylation
Shetty, M., Ismail-Beigi, N., Loeb, J. N., & Ismail‐Beigi, F. (1993) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1993.265.5.c1224 · Cited by 43 · see citing works
Self-citationPlacental oxygen consumption in vitro
Friedman, E. A., & Sachtleben, M. R. (1960) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(60)90511-1 · Cited by 26 · see citing works
Fetal and maternal placental circulations
Ramsey, E. M., Martin, C. B., & Donner, M. W. (1967) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(67)90164-0 · Cited by 23 · see citing works
Placental neurohormones: secretion and physiological implications
Petraglia, F. (1991) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(91)90115-9 · Cited by 23 · see citing works
An image analysis workstation for the pathology laboratory.
Erler, B. S., Chein, K., & Marchevsky, A. M. (1993) · PubMed · Cited by 23 · see citing works
STUDIES OF THE OXYGEN CONSUMPTION OF FRESH PLACENTAL TISSUE FROM NORMAL AND ABNORMAL PREGNANCIES
Mackay, R. (1958) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1958.tb08874.x · Cited by 21 · see citing works
Schneider, H., Malek, A., Duft, R., & Bersinger, N. A. (1989) · Springer eBooks · doi:10.1007/978-1-4613-0823-2_4 · Cited by 15 · see citing works
Intervillous blood oxygen studies.
Wf, H., HUNTER, C. A., & Cp, H. (1961) · PubMed · Cited by 12 · see citing works
The Effect of Zidovudine and 2′3'‐Dideoxyinosine on Human Trophoblast in Culture
Esterman, A. L., Rosenberg, C. R., Brown, T., & Dancis, J. (1995) · Pharmacology & Toxicology · doi:10.1111/j.1600-0773.1995.tb00110.x · Cited by 4 · see citing works
Self-citation
Flagged first, then by citations
1 of the 34 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
The facilitative glucose transporter GLUT3: 20 years of distinction
Simpson, I. A., Dwyer, D., Malide, D., Moley, K. H., Travis, A., & Vannucci, S. J. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90388.2008 · Cited by 473 · see citing works
CURRENT TOPIC: Glucose Transporters in the Human Placenta
Illsley, N. P. (2000) · Placenta · doi:10.1053/plac.1999.0448 · Cited by 334 · see citing works
Preeclampsia is associated with reduced serum levels of placenta growth factor
Torry, D. S., Wang, H., Wang, T., Caudle, M. R., & Torry, R. J. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70021-3 · Cited by 286 · see citing works
Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy
Pringle, K. G., Kind, K. L., Sferruzzi-Perri, A. N., Thompson, J. G., & Roberts, C. T. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmp046 · Cited by 259 · see citing works
Placental Glucose Transfer and Fetal Growth
Baumann, M. U., Deborde, S., & Illsley, N. P. (2002) · Endocrine · doi:10.1385/endo:19:1:13 · Cited by 256 · see citing works
Placental Phenotypes of Intrauterine Growth
Sibley, C. P., Turner, M. A., Cetin, I., Ayuk, P. T.-Y., Boyd, C. A. R., D'Souza, S. W., Glazier, J. D., Greenwood, S. L., Jansson, T., & Powell, T. L. (2005) · Pediatric Research · doi:10.1203/01.pdr.0000181381.82856.23 · Cited by 250 · see citing works
Hayashi, M., Sakata, M., Takeda, T., Yamamoto, T., Okamoto, Y., Sawada, K., Kimura, A., Minekawa, R., Tahara, M., Tasaka, K., et al. (2004) · Journal of Endocrinology · doi:10.1677/joe.1.05599 · Cited by 234 · see citing works
Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia
Tidwell, S., Ho, H., Chiu, W.-H., Torry, R. J., & Torry, D. S. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.113129 · Cited by 231 · see citing works
Regulation of Placental Nutrient Transport – A Review
Jones, H. N., Powell, T. L., & Jansson, T. (2007) · Placenta · doi:10.1016/j.placenta.2007.05.002 · Cited by 226 · see citing works
Rosario, F. J., Kanai, Y., Powell, T. L., & Jansson, T. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.238014 · Cited by 185 · see citing works
Anatomy and Genesis of the Placenta
Burton, G. J., Kaufmann, P., & Huppertz, B. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50010-5 · Cited by 146 · see citing works
Colson, A., Sonveaux, P., Debiève, F., & Sferruzzi-Perri, A. N. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa053 · Cited by 145 · see citing works
Hypoglycemia and the Origin of Hypoxia-Induced Reduction in Human Fetal Growth
Zamudio, S., Torricos, T., Fik, E., Oyala, M., Echalar, L., Pullockaran, J., Tutino, E., Martin, B., Belliappa, S., Balanza, E., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008551 · Cited by 141 · see citing works
Defect of Villous Cytotrophoblast Differentiation into Syncytiotrophoblast in Down’s Syndrome1
Frendo, J., Vidaud, M., Guibourdenche, J., Luton, D., MULLER, F. M., Bellet, D. H., Giovagrandi, Y., Couturier‐Tarrade, A., Porquet, D., Blot, P., et al. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.10.6915 · Cited by 138 · see citing works
Human placental glucose transport in fetoplacental growth and metabolism
Illsley, N. P., & Baumann, M. U. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.12.010 · Cited by 138 · see citing works
Nelson, D. M., Johnson, R. D., Smith, S. D., Anteby, E. Y., & Sadovsky, Y. (1999) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(99)70661-7 · Cited by 131 · see citing works
Baumann, M. U., Zamudio, S., & Illsley, N. P. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00075.2007 · Cited by 123 · see citing works
Effects of chronic hypoxia in vivo on the expression of human placental glucose transporters
Zamudio, S., Baumann, M. U., & Illsley, N. P. (2006) · Placenta · doi:10.1016/j.placenta.2004.12.010 · Cited by 114 · see citing works
Invasion of cytotrophoblastic JEG-3 cells is stimulated by hCG in vitro
Zygmunt, M., Hahn, D., Münstedt, K., Bischof, P., & Lang, U. E. (1998) · Placenta · doi:10.1016/s0143-4004(98)90019-4 · Cited by 111 · see citing works
Rendić, S., & Guengerich, F. P. (2010) · Current Drug Metabolism · doi:10.2174/138920010791110917 · Cited by 109 · see citing works
Glucose transporter 3 (GLUT3) protein expression in human placenta across gestation
Brown, K., Heller, D. S., Zamudio, S., & Illsley, N. P. (2011) · Placenta · doi:10.1016/j.placenta.2011.09.014 · Cited by 108 · see citing works
Illsley, N. P., Caniggia, I., & Zamudio, S. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082798ni · Cited by 107 · see citing works
Defect of Villous Cytotrophoblast Differentiation into Syncytiotrophoblast in Down's Syndrome
Frendo, J. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.10.3700 · Cited by 104 · see citing works
Bukovský, A., Caudle, M. R., Cekanova, M., Fernando, R. I., Wimalasena, J., Foster, J. S., Henley, D. C., & Elder, R. F. (2003) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-1-36 · Cited by 98 · see citing works
Enhanced placental GLUT1 and GLUT3 expression in dexamethasone-induced fetal growth retardation
LANGDOWN, M. L., & Sugden, M. C. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00629-3 · Cited by 92 · see citing works
Janzen, C., Lei, M. Y. Y., Cho, J., Sullivan, P., Shin, B., & Devaskar, S. U. (2013) · Placenta · doi:10.1016/j.placenta.2013.08.010 · Cited by 91 · see citing works
Frendo, J., Thérond, P., Bird, T. H., Massin, N., MULLER, F. M., Guibourdenche, J., Luton, D., Vidaud, M., Anderson, W. B., & Evain‐Brion, D. (2001) · Endocrinology · doi:10.1210/endo.142.8.8329 · Cited by 90 · see citing works
Decreased Maternal Serum Placenta Growth Factor in Early Second Trimester and Preeclampsia
Su, Y. N., Lee, C., Cheng, W., Shau, W. Y., Chow, S. N., & Hsieh, F. J. (2001) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(01)01341-2 · Cited by 89 · see citing works
Fitzpatrick, T. E., & Graham, C. H. (1998) · Experimental Cell Research · doi:10.1006/excr.1998.4240 · Cited by 88 · see citing works
Gaccioli, F., Aye, I. L. M. H., Roos, S., Lager, S., Ramirez, V. I., Kanai, Y., Powell, T. L., & Jansson, T. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0054-8 · Cited by 85 · see citing works
Oxygenation of the placental–fetal unit in humans
Schneider, H. (2011) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2011.05.009 · Cited by 84 · see citing works
Hypoxia inhibits adipocyte differentiation in a HDAC-independent manner
Kim, K. H., Song, M. J., Chung, J., Park, H., & Kim, J. B. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.06.023 · Cited by 83 · see citing works
Transcriptional effect of hypoxia on placental leptin
Grosfeld, A., Turban, S., André, J., Caüzac, M., Challier, J.-C., Mouzon, S. H., & Guerre-Millo, M. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02673-4 · Cited by 83 · see citing works
Hu, R. H., Jin, H., Zhou, S., Yang, P., & Li, X. (2006) · Placenta · doi:10.1016/j.placenta.2006.07.005 · Cited by 73 · see citing works
Ong, C. Y. T., Liao, A. W., Cacho, A. M., Spencer, K., & Nicolaides, K. H. (2001) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(01)01528-9 · Cited by 71 · see citing works
Glycaemic regulation of glucose transporter expression and activity in the human placenta
Illsley, N. P., Sellers, M. C., & Wright, R. L. (1998) · Placenta · doi:10.1016/s0143-4004(98)91045-1 · Cited by 67 · see citing works
Sferruzzi-Perri, A. N., Owens, J. A., Standen, P., Taylor, R. L., Heinemann, G. K., Robinson, J. S., & Roberts, C. T. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00320.2006 · Cited by 65 · see citing works
Sferruzzi-Perri, A. N., Owens, J. A., Standen, P., Taylor, R. L., Robinson, J. S., & Roberts, C. T. (2007) · Endocrinology · doi:10.1210/en.2007-0411 · Cited by 62 · see citing works
Winterhager, E., & Gellhaus, A. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00951 · Cited by 59 · see citing works
Placenta Growth Factor: Potential Role in Pregnancy
Torry, D. S., Ahn, H., Barnes, E. L., & Torry, R. J. (1999) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1999.tb00078.x · Cited by 59 · see citing works
From maternal glucose to fetal glycogen: expression of key regulators in the human placenta
Hahn, D. (2001) · Molecular Human Reproduction · doi:10.1093/molehr/7.12.1173 · Cited by 59 · see citing works
Lange, K. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2002.282.1.c1 · Cited by 59 · see citing works
Christensen, D. R., Calder, P. C., & Houghton, F. D. (2015) · Scientific Reports · doi:10.1038/srep17500 · Cited by 58 · see citing works
Bowen, R. S., Zhang, Y., Gu, Y., Lewis, D. F., & Wang, Y. (2004) · Placenta · doi:10.1016/j.placenta.2004.07.007 · Cited by 52 · see citing works
Analysis of expression and posttranslational modification of proteins during hypoxia
Kumar, G. K., & Klein, J. B. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00818.2003 · Cited by 50 · see citing works
Trophoblast biology, responses to hypoxia and placental dysfunction in preeclampsia
Rampersad, R. M. (2006) · Frontiers in bioscience · doi:10.2741/2246 · Cited by 47 · see citing works
Nishiguchi, A., Gilmore, C. E., Sood, A., Matsusaki, M., Collett, G. P., Tannetta, D., Sargent, I. L., McGarvey, J., Halemani, N. D., Hanley, J. G., et al. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.08.025 · Cited by 45 · see citing works
Silencing of GLUT ‐1 inhibits sensitization of oral cancer cells to cisplatin during hypoxia
Shimanishi, M., Ogi, K., Sogabe, Y., Kaneko, T., Dehari, H., Miyazaki, A., & Hiratsuka, H. (2012) · Journal of Oral Pathology and Medicine · doi:10.1111/jop.12028 · Cited by 44 · see citing works
McClements, L., Richards, C., Patel, N., Chen, H., Sesperez, K., Bubb, K. J., Karlstaedt, A., & Aksentijević, D. (2022) · Scientific Reports · doi:10.1038/s41598-022-05120-2 · Cited by 42 · see citing works
Role of Placental Glucose Transporters in Determining Fetal Growth
Joshi, N. P., Mane, A. R., Sahay, A. S., Sundrani, D. P., Joshi, S., & Yajnik, C. S. (2021) · Reproductive Sciences · doi:10.1007/s43032-021-00699-9 · Cited by 38 · see citing works
Impact of Trisomy 21 on Human Trophoblast Behaviour and Hormonal Function
Pidoux, G., Guibourdenche, J., Frendo, J., Gerbaud, P., Conti, M., Luton, D., MULLER, F. M., & Evain‐Brion, D. (2004) · Placenta · doi:10.1016/j.placenta.2004.01.007 · Cited by 38 · see citing works
Insulin and carbohydrate metabolism
Beardsall, K., Diderholm, B., & Dunger, D. B. (2008) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2007.10.001 · Cited by 35 · see citing works
Zhang, Y., Zhao, W., Jiang, Y., Zhang, R., Wang, J., Li, C., Zhao, H., Gao, L., Cui, Y., Zhou, Z., et al. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.110.090589 · Cited by 35 · see citing works
Hypoxia-induced leptin production in human trophoblasts does not protect from apoptosis
Meißner, U., Spranger, R., Lehner, M., Allabauer, I., Rascher, W., & Dötsch, J. (2005) · European Journal of Endocrinology · doi:10.1530/eje.1.01979 · Cited by 30 · see citing works
Effects of low oxygen levels on the expression and function of transporter OCTN2 in BeWo cells
Rytting, E., & Audus, K. L. (2007) · Journal of Pharmacy and Pharmacology · doi:10.1211/jpp.59.8.0006 · Cited by 30 · see citing works
Frendo, J., Thérond, P., Guibourdenche, J., Bidart, J., Vidaud, M., & Evain‐Brion, D. (2000) · Placenta · doi:10.1053/plac.2000.0575 · Cited by 29 · see citing works
Hypoxia Stimulates ecNOS mRNA Expression by Differentiated Human Trophoblasts
Seligman, S. P., NISHIWAKI, T., KADNER, S. S., Dancis, J., & Finlay, T. H. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48538.x · Cited by 25 · see citing works
Self-citationPlacenta and Placental Transport Function
Sadovsky, Y., & Jansson, T. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00039-9 · Cited by 24 · see citing works
Cell Commitment by Asymmetric Division and Immune System Involvement
Bukovský, A. (2007) · Progress in molecular and subcellular biology · doi:10.1007/978-3-540-69161-7_8 · Cited by 23 · see citing works
Thromboxane A2 Limits Differentiation and Enhances Apoptosis of Cultured Human Trophoblasts
Yusuf, K., Smith, S. D., Levy, R., Schaiff, W. T., Wyatt, S. M., Sadovsky, Y., & Nelson, D. M. (2001) · Pediatric Research · doi:10.1203/00006450-200108000-00007 · Cited by 23 · see citing works
Can Oxygen Tension Contribute to an Abnormal Placental Cytokine Milieu?
Peltier, M. R., Gurzenda, E. M., Murthy, A., Chawala, K., Lerner, V., Kharode, I., Arita, Y., Rhodes, A. J., Maari, N., Moawad, A., et al. (2011) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2011.00998.x · Cited by 22 · see citing works
Hypoxia Inhibits Activin A Production by Term Villous Trophoblast In Vitro
Blumenstein, M., Mitchell, M. D., Groome, N. P., & Keelan, J. A. (2002) · Placenta · doi:10.1016/s0143-4004(02)90868-4 · Cited by 22 · see citing works
Di, L., Deng, N., Wang, S., Huang, J., & Fan, C. (2019) · Placenta · doi:10.1016/j.placenta.2019.10.009 · Cited by 20 · see citing works
Kiss, H., Schneeberger, C., Tschugguel, W., Lass, H., Huber, J., Husslein, P. W., & Knöfler, M. (1998) · Placenta · doi:10.1016/s0143-4004(98)90021-2 · Cited by 19 · see citing works
Blumenstein, M., Keelan, J. A., & Mitchell, M. D. (2001) · Placenta · doi:10.1053/plac.2001.0689 · Cited by 18 · see citing works
Basak, S., Vilasagaram, S., Naidu, K., & Duttaroy, A. K. (2018) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-018-3396-7 · Cited by 15 · see citing works
Thamotharan, S., Raychaudhuri, N., Tomi, M., Shin, B., & Devaskar, S. U. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00513.2012 · Cited by 14 · see citing works
Zhao, F., Lei, F., Zhang, S., Yan, X., Wang, W., & Zheng, Y. (2017) · Nitric Oxide · doi:10.1016/j.niox.2017.07.003 · Cited by 14 · see citing works
Ferré-Dolcet, L., Yeste, M., Vendrell-Flotats, M., Rigau, T., Rodríguez-Gil, J. E., & del Alamo, M. M. R. (2018) · Theriogenology · doi:10.1016/j.theriogenology.2018.08.002 · Cited by 14 · see citing works
Viability of primary term cytotrophoblast cell culture in normoxia and hypoxia
Depoix, C. L., Barret, L. A., Hubinont, C., & Debiève, F. (2012) · Molecular Human Reproduction · doi:10.1093/molehr/gas042 · Cited by 13 · see citing works
Pak, B. J., Park, H., Chang, E. R., Pang, S. C.-N., & Graham, C. H. (1998) · Placenta · doi:10.1016/s0143-4004(98)91041-4 · Cited by 13 · see citing works
Placental angiogenesis and angiogenesis related risk factors in severe pre-eclampsia
Järvenpää, J. (2008) · Cited by 13 · see citing works
Regulation of glucose uptake in differentiated cells
Lange, K. (2001) · Frontiers in bioscience · doi:10.2741/a632 · Cited by 10 · see citing works
Placental Transport in Early Pregnancy—A Workshop Report
Glazier, J. D., & Jansson, T. (2004) · Placenta · doi:10.1016/j.placenta.2004.01.022 · Cited by 9 · see citing works
Yokoi, R., Hayashi, M., Tamura, T., Kobayashi, K., Kuroda, J., Kusama, H., KAGAMI, H., & Ono, T. (2008) · The Journal of Toxicological Sciences · doi:10.2131/jts.33.585 · Cited by 9 · see citing works
Chang, Y., Chang, S., Chao, A., Sieber, M. A., Tsai, C.-L., & Cheng, P. (2022) · Genes · doi:10.3390/genes13050752 · Cited by 8 · see citing works
Korneyeva, K., Rodriguez, R. R., & Ralchenko, S. (2016) · The Ukrainian Biochemical Journal · doi:10.15407/ubj88.01.088 · Cited by 8 · see citing works
Abou-Elghait, A. T., Abdelaziz, H., & Mahmoud, F. (2012) · The Egyptian Journal of Histology · doi:10.1097/01.ehx.0000414585.81633.b3 · Cited by 7 · see citing works
Алексеевна, Д. Е., Ka, P., Kulikova, G. V., Shchegolev, A. I., & Sukhikh, G. T. (2013) · Health · doi:10.4236/health.2013.57a4014 · Cited by 7 · see citing works
Huang, C., Li, H., Powell, J. S., Ouyang, Y., Wendell, S. G., Suresh, S., Hsia, K. J., Sadovsky, Y., & Quinn, D. (2022) · Placenta · doi:10.1016/j.placenta.2022.02.019 · Cited by 6 · see citing works
Down syndrome screening: imagining the screening test of the future
Koster, M., Heetkamp, K. M., Pennings, J. L. A., de Vries, A., Visser, G. H. A., & Schielen, P. C. J. I. (2010) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.10.32 · Cited by 6 · see citing works
Effect of reduced inspired oxygen on fetal growth and maternal glucose metabolism in rat pregnancy
Saker, F., Voora, D., Mahajan, S. D., Kılıç, İ., Ismail-Beigi, F., & Kalhan, S. C. (1999) · Metabolism · doi:10.1016/s0026-0495(99)90173-7 · Cited by 4 · see citing works
Self-citationAspects of fetoplacental nutrition in intrauterine growth restriction and macrosomia
Regnault, T. R. H., Limesand, S. W., & Hay, W. W. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511544712.004 · Cited by 4 · see citing works
Cord Compression May Rapidly Influence the Expression of Placental Angiogenic Genes in Pre-Eclampsia
Järvenpää, J., Vuoristo, J. T., Ukkola, O. H., Hirvikoski, P. P., Savolainen, E., Raudaskoski, T., & Ryynänen, M. (2008) · Placenta · doi:10.1016/j.placenta.2008.02.010 · Cited by 2 · see citing works
Knöfler, M., Stenzel, M., Mösl, B., Strohmer, H., & Husslein, P. W. (1998) · Placenta · doi:10.1016/s0143-4004(98)80056-8 · Cited by 2 · see citing works
Strukturelle und funktionelle Veränderungen in der Plazenta bei Diabetes in der Schwangerschaft
Schneider, H., & Desoyé, G. (1998) · Der Gynäkologe · doi:10.1007/pl00003109 · Cited by 2 · see citing works
Glucose and Amino Acid and Their Roles in Placentation
Duttaroy, A. K., & Basak, S. (2016) · Springer eBooks · doi:10.1007/978-3-319-38804-5_3 · Cited by 1 · see citing works
Fetal Growth and Its Restriction
Longo, L. D. (2018) · Springer eBooks · doi:10.1007/978-1-4939-7483-2_12 · Cited by 1 · see citing works
Redman, C. W. G., SARGENT, I. L., & Linton, E. A. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511545207.015
Moffett, A., Loke, C., & McLaren, A. L. D. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511545207.013
Yavuz, A., Dolanbay, M., Akgün, H., Ozgun, G. Y., Çağlı, F., & Özgün, M. T. (2022) · Journal of Surgery and Medicine · doi:10.28982/josam.7347
Toledano, J. M., Puche-Juárez, M., Badillo, M. P. C., Díaz‐Castro, J., Sánchez‐Romero, J., Ocaña-Peinado, F. M., Matallana, C. D. P., Martín‐Álvarez, E., Moreno‐Fernández, J., & Ochoa, J. J. (2026) · Life Sciences · doi:10.1016/j.lfs.2026.124338
Sabri, A. (2013) · The Sydney eScholarship Repository (The University of Sydney)
- Authors
- Esterman, A., Greco, M. A., Mitani, Y., Finlay, T. H., Ismail-Beigi, F., & Dancis, J.
- Affiliations
- NYU Langone Health (US)
- Case Western Reserve University (US)
- Corresponding author
- Dancis, J.
- ORCID
- Esterman, A.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 1997-03
- Volume
- 18
- Issue
- 2-3
- Pages
- 129-136
- ISSN
- 0143-4004 (ISSN-L)
- OpenAlex
- W2114524395
- Cited by
- 95
- References
- 34
- Citations by year
- 2026: 1 · 2022: 4 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 5 · 2017: 2 · 2016: 3 · 2015: 2 · 2014: 1 · 2013: 5 · 2012: 4
- FWCI
- 7.23
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Placenta (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01dk045945-07)
- U.S. Public Health Service (A1-32298)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-45945)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Keywords
- hypoxia, trophoblast, glucose transport, GLUT1, GLUT3, glucose metabolism, cell cycle, Ki-67, lactic acid production, mitochondrial proliferation, cell morphology, oxygen partial pressure, cell proliferation, gene expression regulation, hypoxia adaptation, apoptosis, necrosis
- MeSH terms
- Biological Transport, Cell Division, Cells, Cultured, Glucose, Humans, Microscopy, Electron, Trophoblasts, Blotting, Northern, Cell Hypoxia
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
