Genipa americana (Rubiaceae) fruit extract affects mitogen-activated protein kinase cell pathways in human trophoblast-derived bewo cells: Implications for placental development

Journal of Medicinal Food

Volumn 14, Issue 5, 2011, Pages 483-494

  Da Conceição, Aline Oliveira ^a   Rossi, Maria Helena ^b   De Oliveira, Fernando Faustino ^c   Takser, Larissa ^d   Lafond, Julie ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^b INSTITUTO BIOLÓGICO   (Brazil)

^c DEPARTAMENTO DE CIÊNCIAS BIOLÓGICAS   (Brazil)

^d UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

choriocharcinoma; ERK1 2; forskolin; p38; placenta; syncytiotrophoblast

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CHORIONIC GONADOTROPIN; CYCLIC AMP; DIMETHYL SULFOXIDE; FORSKOLIN; GENIPA AMERICANA EXTRACT; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; PLANT EXTRACT; UNCLASSIFIED DRUG;

ARTICLE; BEWO CELL; CANCER CELL CULTURE; CELL DIFFERENTIATION; CELL FUSION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFECT; DRUG ISOLATION; DRUG MECHANISM; FRUIT; GENIPA AMERICANA; HUMAN; HUMAN CELL; PHYTOCHEMISTRY; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUALITATIVE ANALYSIS; RUBIACEAE; SIGNAL TRANSDUCTION; TROPHOBLAST;

ADENOSINE MONOPHOSPHATE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CHORIONIC GONADOTROPIN; DIMETHYL SULFOXIDE; DRUG EVALUATION; FEMALE; FLAVONOIDS; FLUORESCENT ANTIBODY TECHNIQUE; FRUIT; HUMANS; IMIDAZOLES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PLACENTATION; PLANT EXTRACTS; PREGNANCY; PYRIDINES; RUBIACEAE; SIGNAL TRANSDUCTION; TROPHOBLASTS;

BOVINAE; GENIPA AMERICANA; RUBIACEAE;

EID: 79956158588     PISSN: 1096620X     EISSN: 15577600     Source Type: Journal    
DOI: 10.1089/jmf.2009.0279     Document Type: Article

References (65)

1. Keeler C: Genipa americana in native tropical medicina. Dermatol Trop Ecol Geog 1964:104-107.
2. Lorenzi H, Matos FJA (eds): Plantas Medicinais No Brasil: Nativas e Exóticas. São Paulo, Brazil, Instituto Plantarum, 2002, p. 512.
3. da Rocha Silva AJ, Andraded LHC: Cultural significance of plants in communities located in the coastal forest zone of the state of Pernambuco, Brazil. Human Ecol 2006;34:447-465.
4. Mors WB, Rizzini CT, Pereira NA: Medicinal Plants of Brazil. Algonac, Michigan, Reference Publications, 2000.
5. Moreira RCT, Costa LCB, Costa RCS, Rocha EA: Abordagem etnobotânica acerca do uso de plantas medicinais na Vila Cachoeira, Ilhéus, Bahia, Brasil. Acta Farm Bonaerense 2002;21:1-7.
6. Robineau L (ed): Hacia Una Pharmacopea Caribeña. Santo Domingo, TRAMIL 7 endacaribe UAG & Universidade de Antioquia Santo Domingo, 1995, p. 696.
7. Saintonge J, Rosso P: Placental blood flow and transfer of nutrient analogues during normal gestation in the guinea pig. Placenta 1983;4:31-39. (Pubitemid 13109023)
8. Audus KL, Soares MJ, Hunt JS: Characteristics of the fetal/ maternal interface with potential usefulness in the development of future immunological and pharmacological strategies. J Pharmacol Exp Ther 2002;301:402-409. (Pubitemid 34429948)
9. Hill EP, Longo LD: Dynamics of maternal-fetal nutrient transfer. Fed Proc 1980;39:239-244. (Pubitemid 10097778)
10. Younes MA, Besch NF, Besch PK: Estradiol and progesterone binding in human term placental cytosol. Am J Obstet Gynecol 1981;141:170-174. (Pubitemid 11018286)
11. Leiser R, Kaufmann P: Placental structure: in a comparative aspect. Exp Clin Endocrinol 1994;102:122-134. (Pubitemid 24235550)
12. Malassine A: Morphological variability and placental function. Gynecol Obstet Fertil 2001;29:489-496. (Pubitemid 32844695)
13. Boyd JD, Hamilton WJ: Electron microscopic observations on the cytotrophoblast contribution to the syncytium in the human placenta. J Anat 1966;100:535-548.
14. Aplin JD: Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 1991;99( Pt 4):681-692.
15. Cross JC, Werb Z, Fisher SJ: Implantation and the placenta: key pieces of the development puzzle. Science 1994;266:15081518.
16. Rote NS, Chakrabarti S, Stetzer BP: The role of human endogenous retroviruses in trophoblast differentiation and placental development. Placenta 2004;25:673-683. (Pubitemid 39185944)
17. Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF 3rd: Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 1986;118:1567-1582. (Pubitemid 16078536)
18. Morrish DW, Bhardwaj D, Dabbagh LK, Marusyk H, Siy O: Epidermal growth factor induces differentiation and secretion of human chorionic gonadotropin and placental lactogen in normal placenta. J Clin Endocrinol Metab 1987;65:1282-1290. (Pubitemid 18026872)
19. Strauss JF 3rd, Kido S, Sayegh R, Sakuragi N, Gafvels ME: The cAMP signalling system and human trophoblast function. Placenta 1992;13:389-403.
20. Midgley AR, Pierce GB Jr, Deneau GA, Gosling JR: Morphogenesis of syncytiotrophoblast in vivo: an autoradiographic demonstration. Science 1963;141:349-350.
21. Daoud G, Amyot M, Rassart E, et al.: ERK1/2 and p38 regulate trophoblasts differentiation in human term placenta. J Physiol 2005;566:409-423. (Pubitemid 41030549)
22. Kyriakis JM, Avruch J: Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001;81:807-869. (Pubitemid 32267078)
23. Whitley GSJ: Production of human trophoblast cell lines. In: Placenta and Trophoblast: Methods and Protocols, Vol. 1. Soares MJ, Hunt JS (eds). Totowa, New Jersey, Humana Press, 2006, pp. 219-228.
24. Fisher SJ, Cui TY, Zhang L, et al.: Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 1989;109:891-902. (Pubitemid 19197046)
25. Liu F, Soares MJ, Audus KL: Permeability properties of monolayers of the human trophoblast cell line BeWo. Am J Physiol 1997;273:C1596-1604.
26. Al-Nasiry S, Spitz B, Hanssens M, Luyten C, Pijnenborg R: Differential effects of inducers of syncytialization and apoptosis on BeWo and JEG-3 choriocarcinoma cells. Hum Reprod 2006;21:193-201. (Pubitemid 41794311)
27. Dalton P, Christian HC, Redman CW, Sargent IL, Boyd CA: Differential effect of cross-linking the CD98 heavy chain on fusion and amino acid transport in the human placental trophoblast (BeWo) cell line. Biochim Biophys Acta 2007;1768:401-410. (Pubitemid 46275594)
28. Taylor RN, Newman ED, Chen SA: Forskolin and methotrexate induce an intermediate trophoblast phenotype in cultured human choriocarcinoma cells. Am J Obstet Gynecol 1991;164: 204-210.
29. Wice B, Menton D, Geuze H, Schwartz AL: Modulators of cyclic AMP metabolism induce syncytiotrophoblast formation in vitro. Exp Cell Res 1990;186:306-316.
30. Kudo Y, Boyd CA, Millo J, Sargent IL, Redman CW: Manipulation of CD98 expression affects both trophoblast cell fusion and amino acid transport activity during syncytialization of human placental BeWo cells. J Physiol 2003;550:3-9. (Pubitemid 36869265)
31. Hamel A, Mergler D, Takser L, Simoneau L, Lafond J: Effects of low concentrations of organochlorine compounds in women on calcium transfer in human placental syncytiotrophoblast. Toxicol Sci 2003;76:182-189. (Pubitemid 37361897)
32. Plessow D, Waldschlager J, Richter DU, et al.: Effects of phytoestrogens on the trophoblast tumour cell lines BeWo and Jeg3. Anticancer Res 2003;23:1081-1086. (Pubitemid 36750922)
33. Lafond J, Hamel A, Takser L, Vaillancourt C, Mergler D: Low environmental contamination by lead in pregnant women: effect on calcium transfer in human placental syncytiotrophoblasts. J Toxicol Environ Health A 2004;67:1069-1079. (Pubitemid 40990836)
34. Meissner U, Spranger R, Lehner M, et al.: Hypoxia-induced leptin production in human trophoblasts does not protect from apoptosis. Eur J Endocrinol 2005;153:455-461. (Pubitemid 41410502)
35. Bechi N, Ietta F, Romagnoli R, et al.: Estrogen-like response to p-nonylphenol in human first trimester placenta and BeWo choriocarcinoma cells. Toxicol Sci 2006;93:75-81. (Pubitemid 44288251)
36. Ampasavate C, Chandorkar GA, Vande Velde DG, Stobaugh JF, Audus KL: Transport and metabolism of opioid peptides across BeWo cells, an in vitro model of the placental barrier. Int J Pharm 2002;233:85-98. (Pubitemid 34230421)
37. Ono M, Ueno M, Masuoka C, Ikeda T, Nohara T: Iridoid glucosides from the fruit of Genipa americana. Chem Pharm Bull (Tokyo) 2005;53:1342-1344. (Pubitemid 41425637)
38. Ono M, Ishimatsu N, Masuoka C, et al.: Three new monoterpenoids from the fruit of Genipa americana. Chem Pharm Bull (Tokyo) 2007;55:632-634. (Pubitemid 46570845)
39. Djerassi C, Gray JD, Kingl FA: Naturally occurring oxygen heteroycles. IX. Isolation and characterization of genipin. J Org Chem 1960;25:2174-2177.
40. Guarnaccia R, Madyastha KM, Tegtmeyer E, Coscia CJ: Geniposidic acid, an iridoid glucoside from Genipa americana. Tetrahedron Lett 1972;50:5125-5127.
41. Yamano T, Tsujimoto Y, Noda T, et al.: Hepatotoxicity of geniposide in rats. Food Chem Toxicol 1990;28:515-519. (Pubitemid 20329379)
42. Matos F (ed): Introdução à Fitoquímica Experimental. Fortaleza, Brazil, Editora da UFC, 1997, p. 141.
43. Heazell AE, Taylor NN, Greenwood SL, Baker PN, Crocker IP: Does altered oxygenation or reactive oxygen species alter cell turnover of BeWo choriocarcinoma cells? Reprod Biomed Online 2009;18:111-119.
44. Yoshimura A, Yoshida T, Seguchi T, et al.: Low binding capacity and altered O-linked glycosylation of low density lipoprotein receptor in a monensin-resistant mutant of Chinese hamster ovary cells. J Biol Chem 1987;262:13299-13308.
45. Reyes-Chilpa R, Rivera J, Oropeza M, et al.: Methanol extracts of Hamelia patens containing oxindole alkaloids relax KClinduced contraction in rat myometrium. Biol Pharm Bull 2004; 27:1617-1620. (Pubitemid 41701650)
46. Figueiredo RW, Maia GA, Holanda LFF, Monteiro JCS: Caracteri s̀ticas químicas e físicas do jenipapo. Pesquisa Agropecua r̀ia Brasileira 1986;21:421-428.
47. Silva AP, Lima CLC, Vieites RL: Caracterisação quimica e fisica do jenipapo (Genipa americana) armazenado. Scientia Agrícola 1998;55:29-34.
48. Wentworth JM, Agostini M, Love J, Schwabe JW, Chatterjee VK: St John's wort, a herbal antidepressant, activates the steroid X receptor. J Endocrinol 2000;166:R11-16.
49. Krishtal O, Lozovaya N, Fisunov A, et al.: Modulation of ion channels in rat neurons by the constituents of Hypericum perforatum. Pharmacopsychiatry 2001;34:S74-S82.
50. Kim JK, So H, Youn MJ, et al.: Hibiscus sabdariffa L. water extract inhibits the adipocyte differentiation through the PI3-K and MAPK pathway. J Ethnopharmacol 2007;114:260-267. (Pubitemid 47539832)
51. Jin UH, Kim DI, Lee TK, et al.: Herbal formulation, Yukmijihang- tang-Jahage, regulates bone resorption by inhibition of phosphorylation mediated by tyrosine kinase Src and cyclooxygenase expression. J Ethnopharmacol 2006;106:333-343.
52. Peeyush L, Khoo N, Guimond M-J, Chakraborty C: Control mechanisms in human trophoblast proliferation and invasiveness: their derangement during trophoblastic tumor progression-a review. Trophoblast Res 1999;13:119-136.
53. Keryer G, Alsat E, Tasken K, Evain-Brion D: Cyclic AMPdependent protein kinases and human trophoblast cell differentiation in vitro. J Cell Sci 1998;111(Pt 7):995-1004. (Pubitemid 28196082)
54. Forbes K, Westwood M, Baker PN, Aplin JD: Insulin-like growth factor I and II regulate the life cycle of trophoblast in the developing human placenta. Am J Physiol Cell Physiol 2008;294: C1313-1322.
55. Ehses JA, Casilla VR, Doty T, et al.: Glucose-dependent insulinotropic polypeptide promotes beta-(INS-1) cell survival via cyclic adenosine monophosphate-mediated caspase-3 inhibition and regulation of p38 mitogen-activated protein kinase. Endocrinology 2003;144:4433-4445. (Pubitemid 37204843)
56. Fang Y, Olah ME: Cyclic AMP-dependent, protein kinase Aindependent activation of extracellular signal-regulated kinase 1/2 following adenosine receptor stimulation in human umbilical vein endothelial cells: role of exchange protein activated by cAMP 1 (Epac1). J Pharmacol Exp Ther 2007;322:1189-1200. (Pubitemid 47295788)
57. Lee JC, Laydon JT, McDonnell PC, et al.: A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 1994;372:739-746.
58. Cuenda A, Rouse J, Doza YN, et al.: SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 1995;364:229-233.
59. Lali FV, Hunt AE, Turner SJ, Foxwell BM: The pyridinyl imidazole inhibitor SB203580 blocks phosphoinositide-dependent protein kinase activity, protein kinase B phosphorylation, and retinoblastoma hyperphosphorylation in interleukin-2-stimulated T cells independently of p38 mitogen-activated protein kinase. J Biol Chem 2000;275:7395-7402. (Pubitemid 30146294)
60. Rubinfield R: The ERK cascade as a prototype of MAPK signaling pathways. In: MAP Kinase Signaling Protocols, Vol. 250. Segar R (ed), Totowa, New Jersey, Humana Press, 2004, pp. 1-49.
61. Sharma GD, He J, Bazan HE: p38 and ERK1/2 coordinate cellular migration and proliferation in epithelial wound healing: evidence of cross-talk activation between MAP kinase cascades. J Biol Chem 2003;278:21989-21997. (Pubitemid 36792607)
62. Kuo WH, Chou FP, Young SC, Chang YC, Wang CJ: Geniposide activates GSH S-transferase by the induction of GST M1 and GST M2 subunits involving the transcription and phosphorylation of MEK-1 signaling in rat hepatocytes. Toxicol Appl Pharmacol 2005;208:155-162.
63. Moon DO, Lee KJ, Choi YH, Kim GY: Beta-sitosterol-inducedapoptosis is mediated by the activation of ERK and the downregulation of Akt in MCA-102 murine fibrosarcoma cells. Int Immunopharmacol 2007;7:1044-1053. (Pubitemid 46900910)
64. Cos P, Vlietinck AJ, Berghe DV, Maes L: Anti-infective potential of natural products: how to develop a stronger in vitro 'proof-of-concept'. J Ethnopharmacol 2006;106:290-302. (Pubitemid 43949328)
65. Alsat E, Malassiné A, Tarrade A, Merviel P, É vain-Brion D: Le cytotrophoblaste humain, un casse-tête pour le biologiste. Mé- decine/Sciences 1999;15:1236-1243. (Pubitemid 129787076)