Artículo

Pérez-Pérez, A.; Toro, A.; Vilariño-Garcia, T.; Guadix, P.; Maymó, J.; Dueñas, J.L.; Varone, C.; Sánchez-Margalet, V. "Leptin protects placental cells from apoptosis induced by acidic stress" (2019) Cell and Tissue Research. 375(3):733-742
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Development of the human placenta is critical for a successful pregnancy. The placenta allows the exchange of oxygen and carbon dioxide and is crucial to manage acid-base balance within a narrow pH. It is known that low pH levels are a risk of apoptosis in several tissues. However, there has been little discussion about the effect of acidic stress in the placenta. Leptin is produced by the placenta with a trophic autocrine effect. Previous results of our group have demonstrated that leptin prevents apoptosis of trophoblast cells under different stress conditions such as serum deprivation and hyperthermia. The purpose of the present work is to evaluate acidic stress consequences in trophoblast explant survival and to determine leptin action in these conditions. For this objective, term human trophoblast explants were cultured at physiological pH (pH 7.4) and at acidic pH (pH 6.8) in the presence or absence of leptin. Western blot assays were performed to study the abundance of active caspase-3 and the p89 fragment of PARP-1. Pro-apoptotic and pro-survival members of Bcl-2 family, as Bax, t-Bid, and Bcl-2, were studied. Moreover, p53 pathway was also evaluated including Mdm-2, the main p53 regulator. Active caspase-3 and cleaved PARP-1 abundances were increased at low extracellular pH. Moreover, t-Bid levels were also augmented as well as p53 expression and phosphorylation on S46. Leptin treatment prevents the consequences of acidosis, decreasing p53 expression and increasing Mdm-2 expression. In summary, this work demonstrated for first time that low pH induces apoptosis of human trophoblast explants involving apoptotic intrinsic pathway, and leptin impairs this effect. © 2018, Springer-Verlag GmbH Germany, part of Springer Nature.

Registro:

Documento: Artículo
Título:Leptin protects placental cells from apoptosis induced by acidic stress
Autor:Pérez-Pérez, A.; Toro, A.; Vilariño-Garcia, T.; Guadix, P.; Maymó, J.; Dueñas, J.L.; Varone, C.; Sánchez-Margalet, V.
Filiación:Department of Medical Biochemistry and Molecular Biology and Immunology, School of Medicine, Virgen Macarena University Hospital, University of Seville, Av. Dr. Fedriani 3, Seville, 41071, Spain
Laboratory of Placental Molecular Physiology, Department of Biological Chemistry, School of Sciences, University of Buenos Aires, IQUIBICEN-CONICET, Ciudad Universitaria, Pab. 2, Buenos Aires, Argentina
Department of Obstetrics and gynecology, Virgen Macarena University Hospital, University of Seville, Seville, Spain
Palabras clave:Acidic stress; Apoptosis; Leptin; Placenta
Año:2019
Volumen:375
Número:3
Página de inicio:733
Página de fin:742
DOI: http://dx.doi.org/10.1007/s00441-018-2940-9
Título revista:Cell and Tissue Research
Título revista abreviado:Cell Tissue Res.
ISSN:0302766X
CODEN:CTSRC
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_0302766X_v375_n3_p733_PerezPerez

Referencias:

  • Allanson, E., Waqar, T., White, C., Tunçalp, Ö., Dickinson, J., Umbilical lactate as a measure of acidosis and predictor of neonatal risk: A systematic review (2016) BJOG Int J Obstet Gynaecol, 124 (4), pp. 584-594
  • Aoyama, K., Burns, D.M., Suh, S.W., Garnier, P., Matsumori, Y., Shiina, H., Swanson, R.A., Acidosis causes endoplasmic reticulum stress and caspase-12-mediated astrocyte death (2005) J Cereb Blood Flow Metab, 25 (3), pp. 358-370. , PID: 15689959
  • Apostolova, N., Blas-Garcia, A., Esplugues, J.V., Mitochondria sentencing about cellular life and death: a matter of oxidative stress (2011) Curr Pharm Des, 17 (36), pp. 4047-4060. , PID: 22188454
  • Avagliano, L., Locatelli, A., Danti, L., Felis, S., Mecacci, F., Bulfamante, G.P., Placental histology in clinically unexpected severe fetal acidemia at term (2015) Early Hum Dev, 91 (5), pp. 339-343. , PID: 25875757
  • Barrientos, G., Toro, A., Moschansky, P., Cohen, M., Garcia, M.G., Rose, M., Maskin, B., Varone, C.L., Leptin promotes HLA-G expression on placental trophoblasts via the MEK/Erk and PI3K signaling pathways (2015) Placenta
  • Basanez, G., Soane, L., Hardwick, J.M., A new view of the lethal apoptotic pore (2012) PLoS Biol, 10 (9). , PID: 23049484
  • Bobrow, C.S., Soothill, P.W., Causes and consequences of fetal acidosis (1999) Arch Dis Child Fetal Neonatal Ed, 80 (3), pp. F246-F249. , PID: 10212094
  • Brady, C.A., Attardi, L.D., p53 at a glance (2010) J Cell Sci, 123 (15), pp. 2527-2532. , PID: 20940128
  • Brenner, D., Mak, T.W., Mitochondrial cell death effectors (2009) Curr Opin Cell Biol, 21 (6), pp. 871-877. , PID: 19822411
  • Cartwright, J.E., Keogh, R.J., van Patot, M.C.T., (2007) Hypoxia and placental remodelling. Hypoxia and the Circulation, pp. 113-126. , Springer, Berlin
  • Cartwright, J.E., Fraser, R., Leslie, K., Wallace, A.E., James, J.L., Remodelling at the maternal–fetal interface: relevance to human pregnancy disorders (2010) Reproduction, 140 (6), pp. 803-813. , PID: 20837731
  • Castro-Parodi, M., Szpilbarg, N., Dietrich, V., Sordelli, M., Reca, A., Abán, C., Maskin, B., Damiano, A.E., Oxygen tension modulates AQP9 expression in human placenta (2013) Placenta, 34 (8), pp. 690-698. , PID: 23684380
  • Chaitanya, G.V., Alexander, J.S., Babu, P.P., PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration (2010) Cell Commun Signal, 8 (1), p. 31. , PID: 21176168
  • Cohen, M., Meisser, A., Haenggeli, L., Irminger-Finger, I., Bischof, P., Status of p53 in first-trimester cytotrophoblastic cells (2007) Mol Hum Reprod, 13 (2), pp. 111-116. , PID: 17158854
  • Dai, C., Gu, W., p53 post-translational modification: deregulated in tumorigenesis (2010) Trends Mol Med, 16 (11), pp. 528-536. , PID: 20932800
  • Desoye, G., Hauguel-de Mouzon, S., The human placenta in gestational diabetes mellitus (2007) Diabetes Care, 30, pp. S120-S126. , PID: 17596459
  • Dong, B., Zhou, H., Han, C., Yao, J., Xu, L., Zhang, M., Fu, Y., Xia, Q., Ischemia/reperfusion-induced CHOP expression promotes apoptosis and impairs renal function recovery: the role of acidosis and GPR4 (2014) PLoS One, 9 (10). , PID: 25343248
  • Eischen, C.M., Lozano, G., The Mdm network and its regulation of p53 activities: a rheostat of cancer risk (2014) Hum Mutat, 35 (6), pp. 728-737. , PID: 24488925
  • Elmore, S., Apoptosis: a review of programmed cell death (2007) Toxicol Pathol, 35 (4), pp. 495-516. , PID: 17562483
  • Eskes, R., Desagher, S., Antonsson, B., Martinou, J.-C., Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane (2000) Mol Cell Biol, 20 (3), pp. 929-935. , PID: 10629050
  • Eskild, A., Strøm-Roum, E.M., Haavaldsen, C., Does the biological response to fetal hypoxia involve angiogenesis, placental enlargement and preeclampsia? (2016) Paediatr Perinat Epidemiol, 30 (3), pp. 305-309. , PID: 27038011
  • Frühbeck, G., Jebb, S., Prentice, A., Leptin: physiology and pathophysiology (1998) Clin Physiol, 18 (5), pp. 399-419. , PID: 9784936
  • Gottlieb, T.M., Leal, J.F.M., Seger, R., Taya, Y., Oren, M., Cross-talk between Akt, p 53 and Mdm 2: possible implications for the regulation of apoptosis (2002) Oncogene, 21 (8), pp. 1299-1303. , PID: 11850850
  • Grosfeld, A., Turban, S., André, J., Cauzac, M., Challier, J.-C., Hauguel-de Mouzon, S., Guerre-Millo, M., Transcriptional effect of hypoxia on placental leptin (2001) FEBS Lett, 502 (3), pp. 122-126. , PID: 11583112
  • Harmon, A.C., Cornelius, D.C., Amaral, L.M., Faulkner, J.L., Cunningham, M.W., Wallace, K., LaMarca, B., The role of inflammation in the pathology of preeclampsia (2016) Clin Sci, 130 (6), pp. 409-419. , PID: 26846579
  • Heazell, A.E., Sharp, A.N., Baker, P.N., Crocker, I.P., Intra-uterine growth restriction is associated with increased apoptosis and altered expression of proteins in the p53 pathway in villous trophoblast (2011) Apoptosis, 16 (2), pp. 135-144. , PID: 21052841
  • Herrid, M., Palanisamy, S., Ciller, U.A., Fan, R., Moens, P., Smart, N.A., McFarlane, J.R., An updated view of leptin on implantation and pregnancy: a review (2014) Physiol Res, 63, pp. 543-557. , PID: 24908087
  • Houseknecht, K.L., Baile, C.A., Matteri, R.L., Spurlock, M.E., The biology of leptin: a review (1998) J Anim Sci, 76 (5), pp. 1405-1420. , PID: 9621947
  • Huppertz, B., Herrler, A., Regulation of proliferation and apoptosis during development of the preimplantation embryo and the placenta (2005) Birth Defects Res C Embryo Today, 75 (4), pp. 249-261. , PID: 16425254
  • Huppertz, B., Kadyrov, M., Kingdom, J.C., Apoptosis and its role in the trophoblast (2006) Am J Obstet Gynecol, 195 (1), pp. 29-39. , PID: 16579915
  • Inoue, T., Wu, L., Stuart, J., Maki, C.G., Control of p53 nuclear accumulation in stressed cells (2005) FEBS Lett, 579 (22), pp. 4978-4984. , PID: 16115632
  • James, J.L., Stone, P., Chamley, L., The effects of oxygen concentration and gestational age on extravillous trophoblast outgrowth in a human first trimester villous explant model (2006) Hum Reprod, 21 (10), pp. 2699-2705. , PID: 16807282
  • Kaufmann, T., Strasser, A., Jost, P.J., Fas death receptor signalling: roles of Bid and XIAP (2012) Cell Death Differ, 19 (1), pp. 42-50. , PID: 21959933
  • Khacho, M., Tarabay, M., Patten, D., Khacho, P., MacLaurin, J.G., Guadagno, J., Bergeron, R., Park, D.S., Acidosis overrides oxygen deprivation to maintain mitochondrial function and cell survival (2014) Nat Commun, 5, p. ncomms4550
  • Kim, J.Y., Cheng, X., Wölfl, S., Acidic stress induced G1 cell cycle arrest and intrinsic apoptotic pathway in Jurkat T-lymphocytes (2017) Exp Cell Res, 350 (1), pp. 140-146. , PID: 27884681
  • Knöfler, M., Pollheimer, J., Human placental trophoblast invasion and differentiation: a particular focus on Wnt signaling (2013) Front Genet, 4, p. 190. , PID: 24133501
  • Levy, R., Nelson, D.M., To be, or not to be, that is the question. Apoptosis in human trophoblast (2000) Placenta, 21 (1), pp. 1-13. , PID: 10692245
  • Lin, Y.-R., Li, C.-J., Syu, S.-H., Wen, C.-H., Buddhakosai, W., Wu, H.-P., Hsu Chen, C., Chen, W.-L., Early administration of glutamine protects cardiomyocytes from post-cardiac arrest acidosis (2016) Biomed Res Int, 2016, p. 2106342. , PID: 28058255
  • Magarinos, M.P., Sanchez-Margalet, V., Kotler, M., Calvo, J.C., Varone, C.L., Leptin promotes cell proliferation and survival of trophoblastic cells (2007) Biol Reprod, 76 (2), pp. 203-210. , PID: 17021346
  • Masuzaki, H., Ogawa, Y., Sagawa, N., Hosoda, K., Matsumoto, T., Mise, H., Nishimura, H., Nakao, K., Nonadipose tissue production of leptin: leptin as a novel placenta-derived hormone in humans (1997) Nat Med, 3 (9), pp. 1029-1033. , PID: 9288733
  • Meek, D.W., Anderson, C.W., Posttranslational modification of p53: cooperative integrators of function (2009) Cold Spring Harb Perspect Biol, 1 (6), p. a000950. , PID: 20457558
  • Meißner, U., Spranger, R., Lehner, M., Allabauer, I., Rascher, W., Dötsch, J., Hypoxia-induced leptin production in human trophoblasts does not protect from apoptosis (2005) Eur J Endocrinol, 153 (3), pp. 455-461. , PID: 16131609
  • Mise, H., Sagawa, N., Matsumoto, T., Yura, S., Nanno, H., Itoh, H., Mori, T., Ogawa, Y., Augmented placental production of leptin in preeclampsia: possible involvement of placental hypoxia 1 (1998) J Clin Endocrinol Metab, 83 (9), pp. 3225-3229. , PID: 9745432
  • Omo-Aghoja, L., Maternal and fetal acid-base chemistry: a major determinant of perinatal outcome (2014) Ann Med \\Health Sci Res, 4 (1), pp. 8-17. , PID: 24669324
  • Ortner, C.M., Combrinck, B., Allie, S., Story, D., Landau, R., Cain, K., Dyer, R., Strong ion and weak acid analysis in severe preeclampsia: potential clinical significance (2015) Br J Anaesth, 115 (2), pp. 275-284. , PID: 26170350
  • Perez-Perez, A., Maymo, J., Duenas, J.L., Goberna, R., Calvo, J.C., Varone, C., Sanchez-Margalet, V., Leptin prevents apoptosis of trophoblastic cells by activation of MAPK pathway (2008) Arch Biochem Biophys, 477 (2), pp. 390-395. , PID: 18619412
  • Perez-Perez, A., Maymo, J., Gambino, Y., Duenas, J.L., Goberna, R., Varone, C., Sanchez-Margalet, V., Leptin stimulates protein synthesis-activating translation machinery in human trophoblastic cells (2009) Biol Reprod, 81 (5), pp. 826-832. , PID: 19553602
  • Perez-Perez, A., Gambino, Y., Maymo, J., Goberna, R., Fabiani, F., Varone, C., Sanchez-Margalet, V., MAPK and PI3K activities are required for leptin stimulation of protein synthesis in human trophoblastic cells (2010) Biochem Biophys Res Commun, 396 (4), pp. 956-960. , PID: 20465992
  • Perez-Perez, A., Sanchez-Jimenez, F., Maymo, J., Duenas, J.L., Varone, C., Sanchez-Margalet, V., Role of leptin in female reproduction (2015) Clin Chem Lab Med, 53 (1), pp. 15-28. , PID: 25014521
  • Pérez-Pérez, A., Toro, A.R., Vilarino-Garcia, T., Guadix, P., Maymó, J.L., Dueñas, J.L., Varone, C.L., Sánchez-Margalet, V., Leptin reduces apoptosis triggered by high temperature in human placental villous explants: the role of the p53 pathway (2016) Placenta, 42, pp. 106-113. , PID: 27238720
  • Pérez-Pérez, A., Vilariño-García, T., Fernández-Riejos, P., Martín-González, J., Segura-Egea, J.J., Sánchez-Margalet, V., Role of leptin as a link between metabolism and the immune system (2017) Cytokine Growth Factor Rev, 35, pp. 71-84. , PID: 28285098
  • Pérez-Pérez, A., Toro, A., Vilariño-García, T., Maymó, J., Guadix, P., Dueñas, J.L., Fernández-Sánchez, M., Sánchez-Margalet, V., Leptin action in normal and pathological pregnancies (2017) J Cell Mol Med, 22 (2), pp. 716-727
  • Pringle, K., Kind, K., Sferruzzi-Perri, A., Thompson, J., Roberts, C., Beyond oxygen: Complex regulation and activity of hypoxia inducible factors in pregnancy (2009) Hum Reprod Update, p. dmp046
  • Rehman, K., Akash, M.S.H., Alina, Z., Leptin: a new therapeutic target for treatment of diabetes mellitus (2018) J Cell Biochem, 119 (7), pp. 5016-5027. , PID: 29236298
  • Rodesch, F., Simon, P., Donner, C., Jauniaux, E., Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy (1992) Obstet Gynecol, 80 (2), pp. 283-285. , PID: 1635745
  • Schanton, M., Maymó, J.L., Pérez-Pérez, A., Sanchez-Margalet, V., Varone, C., Involvement of leptin in the molecular physiology of the placenta (2017) Reproduction, 155 (1), pp. RR1-R12
  • Sharma, V., Kaur, R., Bhatnagar, A., Kaur, J., Low-pH-induced apoptosis: role of endoplasmic reticulum stress-induced calcium permeability and mitochondria-dependent signaling (2015) Cell Stress Chaperones, 20 (3), pp. 431-440. , PID: 25823563
  • Sharp, A.N., Heazell, A.E., Crocker, I.P., Mor, G., Placental apoptosis in health and disease (2010) Am J Reprod Immunol, 64 (3), pp. 159-169. , PID: 20367628
  • Sinha, K., Das, J., Pal, P.B., Sil, P.C., Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis (2013) Arch Toxicol, 87 (7), pp. 1157-1180. , PID: 23543009
  • Sohr, S., Engeland, K., The tumor suppressor p53 induces expression of the pregnancy-supporting human chorionic gonadotropin (hCG) CGB7 gene (2011) Cell Cycle, 10 (21), pp. 3758-3767. , PID: 22032922
  • Toro, A.R., Maymó, J.L., Ibarbalz, F.M., Pérez, A.P., Maskin, B., Faletti, A.G., Margalet, V.S., Varone, C.L., Leptin is an anti-apoptotic effector in placental cells involving p53 downregulation (2014) PLoS One, 9 (6). , PID: 24922063
  • Toro, A.R., Pérez-Pérez, A., Gutiérrez, I.C., Sánchez-Margalet, V., Varone, C.L., Mechanisms involved in p53 downregulation by leptin in trophoblastic cells (2015) Placenta, 36 (11), pp. 1266-1275. , PID: 26386653
  • Tzschoppe, A., Struwe, E., Rascher, W., Dörr, H.G., Schild, R.L., Goecke, T.W., Beckmann, M.W., Dötsch, J., Intrauterine growth restriction (IUGR) is associated with increased leptin synthesis and binding capability in neonates (2011) Clin Endocrinol, 74 (4), pp. 459-466
  • Vaupel, P., Kallinowski, F., Okunieff, P., Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review (1989) Cancer Res, 49 (23), pp. 6449-6465. , PID: 2684393
  • Wulff, C., Weigand, M., Kreienberg, R., Fraser, H.M., Angiogenesis during primate placentation in health and disease (2003) Reproduction, 126 (5), pp. 569-577. , PID: 14611629
  • Yang, J.M., Wang, K.G., Relationship between acute fetal distress and maternal-placental-fetal circulations in severe preeclampsia (1995) Acta Obstet Gynecol Scand, 74 (6), pp. 419-424. , PID: 7604683
  • Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., Friedman, J.M., Positional cloning of the mouse obese gene and its human homologue (1994) Nature, 372 (6505), pp. 425-432. , PID: 7984236

Citas:

---------- APA ----------
Pérez-Pérez, A., Toro, A., Vilariño-Garcia, T., Guadix, P., Maymó, J., Dueñas, J.L., Varone, C.,..., Sánchez-Margalet, V. (2019) . Leptin protects placental cells from apoptosis induced by acidic stress. Cell and Tissue Research, 375(3), 733-742.
http://dx.doi.org/10.1007/s00441-018-2940-9
---------- CHICAGO ----------
Pérez-Pérez, A., Toro, A., Vilariño-Garcia, T., Guadix, P., Maymó, J., Dueñas, J.L., et al. "Leptin protects placental cells from apoptosis induced by acidic stress" . Cell and Tissue Research 375, no. 3 (2019) : 733-742.
http://dx.doi.org/10.1007/s00441-018-2940-9
---------- MLA ----------
Pérez-Pérez, A., Toro, A., Vilariño-Garcia, T., Guadix, P., Maymó, J., Dueñas, J.L., et al. "Leptin protects placental cells from apoptosis induced by acidic stress" . Cell and Tissue Research, vol. 375, no. 3, 2019, pp. 733-742.
http://dx.doi.org/10.1007/s00441-018-2940-9
---------- VANCOUVER ----------
Pérez-Pérez, A., Toro, A., Vilariño-Garcia, T., Guadix, P., Maymó, J., Dueñas, J.L., et al. Leptin protects placental cells from apoptosis induced by acidic stress. Cell Tissue Res. 2019;375(3):733-742.
http://dx.doi.org/10.1007/s00441-018-2940-9