Artículo

Abán, C.; Martinez, N.; Carou, C.; Albamonte, I.; Toro, A.; Seyahian, A.; Franchi, A.; Leguizamón, G.; Trigubo, D.; Damiano, A.; Farina, M. "Endocannabinoids participate in placental apoptosis induced by hypoxia inducible factor-1" (2016) Apoptosis. 21(10):1094-1105
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:

During pregnancy, apoptosis is a physiological event critical in the remodeling and aging of the placenta. Increasing evidence has pointed towards the relevance of endocannabinoids (ECs) and hypoxia as modulators of trophoblast cell death. However, the relation between these factors is still unknown. In this report, we evaluated the participation of ECs in placental apoptosis induced by cobalt chloride (CoCl2), a hypoxia mimicking agent that stabilizes the expression of hypoxia inducible factor-1 alpha (HIF-1α). We found that HIF-1α stabilization decreased FAAH mRNA and protein levels, suggesting an increase in ECs tone. Additionally, CoCl2 incubation and Met-AEA treatment reduced cell viability and increased TUNEL-positive staining in syncytiotrophoblast layer. Immunohistochemical analysis demonstrated Bax and Bcl-2 protein expression in the cytoplasm of syncytiotrophoblast. Finally, HIF-1α stabilization produced an increase in Bax/Bcl-2 ratio, activation of caspase 3 and PARP cleavage. All these changes in apoptotic parameters were reversed with AM251, a CB1 antagonist. These results demonstrate that HIF-1α may induce apoptosis in human placenta via intrinsic pathway by a mechanism that involves activation of CB1 receptor suggesting a role of the ECs in this process. © 2016, Springer Science+Business Media New York.

Registro:

Documento: Artículo
Título:Endocannabinoids participate in placental apoptosis induced by hypoxia inducible factor-1
Autor:Abán, C.; Martinez, N.; Carou, C.; Albamonte, I.; Toro, A.; Seyahian, A.; Franchi, A.; Leguizamón, G.; Trigubo, D.; Damiano, A.; Farina, M.
Filiación:Laboratorio de Fisiopatología Placentaria, Centro de Estudios Farmacológicos y Botánicos (CEFYBO, CONICET), Facultad de Medicina, Universidad de Buenos Aires, Paraguay 2155, 16th floor, Buenos Aires, C1121ABG, Argentina
Laboratorio de Biología de la Reproducción, Instituto de Fisiología y Biofísica Bernardo Houssay (IFIBIO) - CONICET- Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina
Cátedra de Histología y Embriología, Facultad de Ciencias Veterinarias, UBA, Buenos Aires, Argentina
Centro de Estudios Biomédicos, Biotecnológicos, Ambientales y Diagnóstico – CEBBAD, Universidad Maimónides, Buenos Aires, Argentina
Departamento de Química Biológica, Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales, Facultad de Ciencias Exactas y Naturales, UBA, Buenos Aires, Argentina
Laboratorio de Fisiopatología de la Preñez y el Parto, (CEFYBO, CONICET), Facultad de Medicina, UBA, Buenos Aires, Argentina
Departamento de Obstetricia y Ginecología, Unidad de Embarazo de Alto Riesgo, Centro de Educación Médica e Investigaciones Clínicas (CEMIC), Buenos Aires, Argentina
Departamento de Ciencias Biológicas, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Apoptosis; Endocannabinoids; Hipoxia inducible factor 1; Placenta; cannabinoid 1 receptor; caspase 3; chorionic gonadotropin beta subunit; endocannabinoid; fatty acid amidase; hypoxia inducible factor 1; lactate dehydrogenase; messenger RNA; nicotinamide adenine dinucleotide adenosine diphosphate ribosyltransferase; protein Bax; protein bcl 2; BCL2 protein, human; CASP3 protein, human; caspase 3; cobalt; cobalt chloride; endocannabinoid; hypoxia inducible factor 1alpha; protein bcl 2; apoptosis; Article; cell viability; controlled study; enzyme activation; female; hormone synthesis; human; human tissue; hypoxia; immunoreactivity; intracellular signaling; placenta; placenta tissue; priority journal; protein cleavage; protein expression; protein induction; protein localization; protein stability; syncytiotrophoblast; upregulation; cell hypoxia; cell survival; cytology; drug effects; genetics; metabolism; placenta; pregnancy; signal transduction; Apoptosis; Caspase 3; Cell Hypoxia; Cell Survival; Cobalt; Endocannabinoids; Female; Humans; Hypoxia-Inducible Factor 1, alpha Subunit; Placenta; Pregnancy; Proto-Oncogene Proteins c-bcl-2; Signal Transduction
Año:2016
Volumen:21
Número:10
Página de inicio:1094
Página de fin:1105
DOI: http://dx.doi.org/10.1007/s10495-016-1274-x
Título revista:Apoptosis
Título revista abreviado:Apoptosis
ISSN:13608185
CODEN:APOPF
CAS:caspase 3, 169592-56-7; fatty acid amidase, 153301-19-0; lactate dehydrogenase, 9001-60-9; nicotinamide adenine dinucleotide adenosine diphosphate ribosyltransferase, 58319-92-9; protein bcl 2, 219306-68-0; cobalt, 7440-48-4; cobalt chloride, 1332-82-7, 7646-79-9; BCL2 protein, human; CASP3 protein, human; Caspase 3; Cobalt; cobaltous chloride; Endocannabinoids; Hypoxia-Inducible Factor 1, alpha Subunit; Proto-Oncogene Proteins c-bcl-2
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_13608185_v21_n10_p1094_Aban

Referencias:

  • Habayeb, O.M., Taylor, A.H., Evans, M.D., Cooke, M.S., Taylor, D.J., Bell, S.C., Konje, J.C., Plasma levels of the endocannabinoid anandamide in women–a potential role in pregnancy maintenance and labor? (2004) J Clin Endocrinol Metab, 89 (11), pp. 5482-5487. , COI: 1:CAS:528:DC%2BD2cXhtVSisb3I, PID: 15531501
  • Di Marzo, V., Fontana, A., Cadas, H., Schinelli, S., Cimino, G., Schwartz, J.C., Piomelli, D., Formation and inactivation of endogenous cannabinoid anandamide in central neurons (1994) Nature, 372 (6507), pp. 686-691. , PID: 7990962
  • Cravatt, B.F., Lichtman, A.H., The enzymatic inactivation of the fatty acid amide class of signaling lipids (2002) Chem Phys Lipids, 121 (1-2), pp. 135-148. , COI: 1:CAS:528:DC%2BD38Xpslans7o%3D, PID: 12505696
  • Park, B., Gibbons, H.M., Mitchell, M.D., Glass, M., Identification of the CB1 cannabinoid receptor and fatty acid amide hydrolase (FAAH) in the human placenta (2003) Placenta, 24 (10), pp. 990-995. , COI: 1:CAS:528:DC%2BD3sXot1GrtL0%3D, PID: 14580383
  • Marczylo, T.H., Lam, P.M., Amoako, A.A., Konje, J.C., Anandamide levels in human female reproductive tissues: solid-phase extraction and measurement by ultraperformance liquid chromatography tandem mass spectrometry (2010) Anal Biochem, 400 (2), pp. 155-162. , COI: 1:CAS:528:DC%2BC3cXjs1Oht7s%3D, PID: 20026294
  • Aban, C., Leguizamon, G.F., Cella, M., Damiano, A., Franchi, A.M., Farina, M.G., Differential expression of endocannabinoid system in normal and preeclamptic placentas: effects on nitric oxide synthesis (2013) Placenta, 34 (1), pp. 67-74. , COI: 1:CAS:528:DC%2BC3sXhs1emsro%3D, PID: 23122699
  • Heazell, A.E., Crocker, I.P., Live and let die—regulation of villous trophoblast apoptosis in normal and abnormal pregnancies (2008) Placenta, 29 (9), pp. 772-783. , COI: 1:CAS:528:DC%2BD1cXhtVOhsrvL, PID: 18706691
  • Smith, S.C., Baker, P.N., Symonds, E.M., Increased placental apoptosis in intrauterine growth restriction (1997) Am J Obstet Gynecol, 177 (6), pp. 1395-1401. , COI: 1:STN:280:DyaK1c%2FosVemtQ%3D%3D, PID: 9423741
  • Leung, D.N., Smith, S.C., To, K.F., Sahota, D.S., Baker, P.N., Increased placental apoptosis in pregnancies complicated by preeclampsia (2001) Am J Obstet Gynecol, 184 (6), pp. 1249-1250. , COI: 1:STN:280:DC%2BD3Mzls1SltA%3D%3D, PID: 11349196
  • Harris, A.L., Hypoxia–a key regulatory factor in tumour growth (2002) Nat Rev Cancer, 2 (1), pp. 38-47. , COI: 1:CAS:528:DC%2BD38XhvF2jtL4%3D, PID: 11902584
  • Pringle, K.G., Kind, K.L., Sferruzzi-Perri, A.N., Thompson, J.G., Roberts, C.T., Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy (2010) Hum Reprod Update, 16 (4), pp. 415-431. , COI: 1:CAS:528:DC%2BC3cXntVGhsbY%3D, PID: 19926662
  • Déry, M.A., Michaud, M.D., Richard, D.E., Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators (2005) Int J Biochem Cell Biol, 37 (3), pp. 535-540. , PID: 15618010
  • Rajakumar, A., Conrad, K.P., Expression, ontogeny, and regulation of hypoxia inducible transcription factors in the human placenta (2000) Biol Reprod, 63 (2), pp. 559-569. , COI: 1:CAS:528:DC%2BD3cXltl2gtbc%3D, PID: 10906065
  • Rajakumar, A., Michael, H.M., Daftary, A., Jeyabalan, A., Gilmour, A., Conrad, K.P., Proteasomal activity in placentas from women with preeclampsia and intrauterine growth restriction: implications for expression of HIF-alpha proteins (2008) Placenta, 29 (3), pp. 290-299. , COI: 1:CAS:528:DC%2BD1cXjtlKjsr0%3D, PID: 18222538
  • Costa, M.A., The endocannabinoid system: a novel player in human placentation (2016) Reprod Toxicol, 61, pp. 58-67. , COI: 1:CAS:528:DC%2BC28XktFKgt78%3D, PID: 26965993
  • Castro-Parodi, M., Szpilbarg, N., Dietrich, V., Sordelli, M., Reca, A., Aban, C., Maskin, B., Damiano, A.E., Oxygen tension modulates AQP9 expression in human placenta (2013) Placenta, 34 (8), pp. 690-698. , COI: 1:CAS:528:DC%2BC3sXnvVOgtLg%3D, PID: 23684380
  • Miller, R.K., Genbacev, O., Turner, M.A., Aplin, J.D., Caniggia, I., Huppertz, B., Human placental explants in culture: approaches and assessments (2005) Placenta, 26 (6), pp. 439-448. , COI: 1:CAS:528:DC%2BD2MXltFeitbk%3D, PID: 15950058
  • Lee, J.H., Choi, S.H., Baek, M.W., Kim, M.H., Kim, H.J., Kim, S.H., Oh, S.J., Jung, J.Y., CoCl2 induces apoptosis through the mitochondria- and death receptor-mediated pathway in the mouse embryonic stem cells (2013) Mol Cell Biochem, 379 (1-2), pp. 133-140. , COI: 1:CAS:528:DC%2BC3sXlsFCis78%3D, PID: 23568501
  • Maccarrone, M., Bisogno, T., Valensise, H., Lazzarin, N., Fezza, F., Manna, C., Di Marzo, V., Finazzi-Agro, A., Low fatty acid amide hydrolase and high anandamide levels are associated with failure to achieve an ongoing pregnancy after IVF and embryo transfer (2002) Mol Hum Reprod, 8 (2), pp. 188-195. , COI: 1:CAS:528:DC%2BD38XitFOgsrY%3D, PID: 11818522
  • Chamley, L.W., Bhalla, A., Stone, P.R., Liddell, H., O’Carroll, S., Kearn, C., Glass, M., Nuclear localization of the endocannabinoid metabolizing enzyme fatty acid amide hydrolase (FAAH) in invasive trophoblasts and an association with recurrent miscarriage (2008) Placenta, 29 (11), pp. 970-975. , COI: 1:CAS:528:DC%2BD1cXht12ltL%2FF, PID: 18805581
  • Habayeb, O.M., Taylor, A.H., Finney, M., Evans, M.D., Konje, J.C., Plasma anandamide concentration and pregnancy outcome in women with threatened miscarriage (2008) JAMA, 299 (10), pp. 1135-1136. , COI: 1:CAS:528:DC%2BD1cXjt1aqtbY%3D, PID: 18334688
  • Endsley, M.P., Thill, R., Choudhry, I., Williams, C.L., Kajdacsy-Balla, A., Campbell, W.B., Nithipatikom, K., Expression and function of fatty acid amide hydrolase in prostate cancer (2008) Int J Cancer, 123 (6), pp. 1318-1326. , COI: 1:CAS:528:DC%2BD1cXhtVCltLzI, PID: 18566995
  • Cippitelli, A., Cannella, N., Braconi, S., Duranti, A., Tontini, A., Bilbao, A., Defonseca, F.R., Ciccocioppo, R., Increase of brain endocannabinoid anandamide levels by FAAH inhibition and alcohol abuse behaviours in the rat (2008) Psychopharmacology, 198 (4), pp. 449-460. , COI: 1:CAS:528:DC%2BD1cXmsVegurs%3D, PID: 18446329
  • Jian, H., Liu, B., Zhang, J., Hypoxia and hypoxia-inducible factor 1 repress SEMA4B expression to promote non-small cell lung cancer invasion (2014) Tumour Biol, 35 (5), pp. 4949-4955. , COI: 1:CAS:528:DC%2BC2cXntlOku70%3D, PID: 24474252
  • Zheng, J., Sun, X., Wang, W., Lu, S., Hypoxia-inducible factor-1alpha modulates the down-regulation of the homeodomain protein CDX2 in colorectal cancer (2010) Oncol Rep, 24 (1), pp. 97-104. , COI: 1:CAS:528:DC%2BC3cXpt1ahtL0%3D, PID: 20514449
  • Costa, M.A., Fonseca, B.M., Keating, E., Teixeira, N.A., Correia-da-Silva, G., Transient receptor potential vanilloid 1 is expressed in human cytotrophoblasts: induction of cell apoptosis and impairment of syncytialization (2014) Int J Biochem Cell Biol, 57, pp. 177-185. , COI: 1:CAS:528:DC%2BC2cXhvVSms7vJ, PID: 25450464
  • Costa, M.A., Fonseca, B.M., Teixeira, N.A., Correia-da-Silva, G., The endocannabinoid anandamide induces apoptosis in cytotrophoblast cells: involvement of both mitochondrial and death receptor pathways (2015) Placenta, 36 (1), pp. 69-76. , COI: 1:CAS:528:DC%2BC2cXhvVOktrfL, PID: 25465706
  • Roh, C.R., Lee, J.W., Kang, B.H., Yang, S.H., Kim, B.G., Bae, D.S., Kim, J.H., Lee, J.H., Differential expressions of Fas and Fas ligand in human placenta (2002) J Korean Med Sci, 17 (2), pp. 213-216. , COI: 1:CAS:528:DC%2BD38XjvFGls7o%3D, PID: 11961305
  • Pongcharoen, S., Searle, R.F., Bulmer, J.N., Placental Fas and Fas ligand expression in normal early, term and molar pregnancy (2004) Placenta, 25 (4), pp. 321-330. , COI: 1:CAS:528:DC%2BD2cXitFKmtb0%3D, PID: 15028424
  • Ishihara, N., Matsuo, H., Murakoshi, H., Laoag-Fernandez, J.B., Samoto, T., Maruo, T., Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation (2002) Am J Obstet Gynecol, 186 (1), pp. 158-166. , PID: 11810103
  • De Falco, M., Penta, R., Laforgia, V., Cobellis, L., De Luca, A., Apoptosis and human placenta: expression of proteins belonging to different apoptotic pathways during pregnancy (2005) J Exp Clin Cancer Res, 24 (1), pp. 25-33. , PID: 15943028
  • Ratts, V.S., Tao, X.J., Webster, C.B., Swanson, P.E., Smith, S.D., Brownbill, P., Krajewski, S., Nelson, D.M., Expression of BCL-2, BAX and BAK in the trophoblast layer of the term human placenta: a unique model of apoptosis within a syncytium (2000) Placenta, 21 (4), pp. 361-366. , COI: 1:CAS:528:DC%2BD3cXksFSiu7k%3D, PID: 10833371
  • Huppertz, B., Frank, H.G., Kingdom, J.C., Reister, F., Kaufmann, P., Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta (1998) Histochem Cell Biol, 110 (5), pp. 495-508. , COI: 1:CAS:528:DyaK1cXmtlektLs%3D, PID: 9826129
  • Abumaree, M.H., Stone, P.R., Chamley, L.W., Changes in the expression of apoptosis-related proteins in the life cycle of human villous trophoblast (2012) Reprod Sci, 19 (6), pp. 597-606. , COI: 1:CAS:528:DC%2BC2cXovFygt7k%3D, PID: 22138542
  • Huppertz, B., Kingdom, J., Caniggia, I., Desoye, G., Black, S., Korr, H., Kaufmann, P., Hypoxia favours necrotic versus apoptotic shedding of placental syncytiotrophoblast into the maternal circulation (2003) Placenta, 24 (2-3), pp. 181-190. , COI: 1:STN:280:DC%2BD3s%2Fls1Oksw%3D%3D, PID: 12566245
  • Tomiyama, K., Funada, M., Cytotoxicity of synthetic cannabinoids on primary neuronal cells of the forebrain: the involvement of cannabinoid CB1 receptors and apoptotic cell death (2014) Toxicol Appl Pharmacol, 274 (1), pp. 17-23. , COI: 1:CAS:528:DC%2BC3sXhvFOksL3N, PID: 24211273
  • Fonseca, B.M., Correia-da-Silva, G., Teixeira, N.A., Anandamide-induced cell death: dual effects in primary rat decidual cell cultures (2009) Placenta, 30 (8), pp. 686-692. , COI: 1:CAS:528:DC%2BD1MXptVSitL4%3D, PID: 19560819
  • 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
  • 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. , COI: 1:CAS:528:DC%2BC3cXhtFKjtL3P, PID: 20367628
  • Caniggia, I., Winter, J.L., Adriana and Luisa Castellucci Award lecture 2001 Hypoxia inducible factor-1: oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies–a review (2002) Placenta, 23, pp. S47-S57. , PID: 11978059

Citas:

---------- APA ----------
Abán, C., Martinez, N., Carou, C., Albamonte, I., Toro, A., Seyahian, A., Franchi, A.,..., Farina, M. (2016) . Endocannabinoids participate in placental apoptosis induced by hypoxia inducible factor-1. Apoptosis, 21(10), 1094-1105.
http://dx.doi.org/10.1007/s10495-016-1274-x
---------- CHICAGO ----------
Abán, C., Martinez, N., Carou, C., Albamonte, I., Toro, A., Seyahian, A., et al. "Endocannabinoids participate in placental apoptosis induced by hypoxia inducible factor-1" . Apoptosis 21, no. 10 (2016) : 1094-1105.
http://dx.doi.org/10.1007/s10495-016-1274-x
---------- MLA ----------
Abán, C., Martinez, N., Carou, C., Albamonte, I., Toro, A., Seyahian, A., et al. "Endocannabinoids participate in placental apoptosis induced by hypoxia inducible factor-1" . Apoptosis, vol. 21, no. 10, 2016, pp. 1094-1105.
http://dx.doi.org/10.1007/s10495-016-1274-x
---------- VANCOUVER ----------
Abán, C., Martinez, N., Carou, C., Albamonte, I., Toro, A., Seyahian, A., et al. Endocannabinoids participate in placental apoptosis induced by hypoxia inducible factor-1. Apoptosis. 2016;21(10):1094-1105.
http://dx.doi.org/10.1007/s10495-016-1274-x