Different concentrations of kaempferol distinctly modulate murine embryonic stem cell function

Food and Chemical Toxicology

Volumn 87, Issue , 2016, Pages 148-156

  Correia, Marcelo ^a,b   Rodrigues, Ana S ^a,b,c   Perestrelo, Tânia ^a,b   Pereira, Sandro L ^a,b,c   Ribeiro, Marcelo F ^a,c   Sousa, Maria I ^a,c   Ramalho Santos, João ^a,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Apoptosis; Kaempferol; Mitochondria; ROS; Stem cell

Indexed keywords

KAEMPFEROL; OCTAMER TRANSCRIPTION FACTOR 4; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NANOG; BIOLOGICAL MARKER; KAEMPFEROL DERIVATIVE; SUPEROXIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL GROWTH; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYONIC STEM CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; ANIMAL; CELL CYCLE; CELL LINE; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; NECROSIS;

ANIMALS; APOPTOSIS; BIOMARKERS; CELL CYCLE; CELL LINE; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; KAEMPFEROLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; NECROSIS; SUPEROXIDES;

EID: 84949934778     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2015.12.011     Document Type: Article

References (45)

1. Barros L., Duenas M., Carvalho A.M., Ferreira I.C., Santos-Buelga C. Characterization of phenolic compounds in flowers of wild medicinal plants from Northeastern Portugal. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 2012, 50:1576-1582.
2. Bestwick C.S., Milne L., Duthie S.J. Kaempferol induced inhibition of HL-60 cell growth results from a heterogeneous response, dominated by cell cycle alterations. Chem. Biol. Interact. 2007, 170:76-85.
3. Bestwick C.S., Milne L., Pirie L., Duthie S.J. The effect of short-term kaempferol exposure on reactive oxygen levels and integrity of human (HL-60) leukaemic cells. Biochim. Biophys. Acta 2005, 1740:340-349.
4. Calderon-Montano J.M., Burgos-Moron E., Perez-Guerrero C., Lopez-Lazaro M. A review on the dietary flavonoid kaempferol. Mini Rev. Med. Chem. 2011, 11:298-344.
5. Chen A.Y., Chen Y.C. A review of the dietary flavonoid, kaempferol on human health and cancer chemoprevention. Food Chem. 2013, 138:2099-2107.
6. Chen X., Xu H., Yuan P., Fang F., Huss M., Vega V.B., Wong E., Orlov Y.L., Zhang W., Jiang J., Loh Y.H., Yeo H.C., Yeo Z.X., Narang V., Govindarajan K.R., Leong B., Shahab A., Ruan Y., Bourque G., Sung W.K., Clarke N.D., Wei C.L., Ng H.H. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117.
7. Choi E.M. Kaempferol protects MC3T3-E1 cells through antioxidant effect and regulation of mitochondrial function. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 2011, 49:1800-1805.
8. Correia M., Sousa M.I., Rodrigues A.S., Perestrelo T., Pereira S.L., Ribeiro M.F., Ramalho-Santos J. Potential impact of food supplements on the growth of mouse embryonic stem cells. Data in Brief 2015, (submitted for publication).
9. Crespo I., Garcia-Mediavilla M.V., Almar M., Gonzalez P., Tunon M.J., Sanchez-Campos S., Gonzalez-Gallego J. Differential effects of dietary flavonoids on reactive oxygen and nitrogen species generation and changes in antioxidant enzyme expression induced by proinflammatory cytokines in Chang liver cells. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 2008, 46:1555-1569.
10. Dang Q., Song W., Xu D., Ma Y., Li F., Zeng J., Zhu G., Wang X., Chang L.S., He D., Li L. Kaempferol suppresses bladder cancer tumor growth by inhibiting cell proliferation and inducing apoptosis. Mol. Carcinog. 2014.
11. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-156.
12. Folmes C.D., Nelson T.J., Martinez-Fernandez A., Arrell D.K., Lindor J.Z., Dzeja P.P., Ikeda Y., Perez-Terzic C., Terzic A. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab. 2011, 14:264-271.
13. Huang W.W., Chiu Y.J., Fan M.J., Lu H.F., Yeh H.F., Li K.H., Chen P.Y., Chung J.G., Yang J.S. Kaempferol induced apoptosis via endoplasmic reticulum stress and mitochondria-dependent pathway in human osteosarcoma U-2 OS cells. Mol. Nutr. Food Res. 2010, 54:1585-1595.
14. Jeong J.C., Kim M.S., Kim T.H., Kim Y.K. Kaempferol induces cell death through ERK and Akt-dependent down-regulation of XIAP and survivin in human glioma cells. Neurochem. Res. 2009, 34:991-1001.
15. Kandaswami C., Lee L.T., Lee P.P., Hwang J.J., Ke F.C., Huang Y.T., Lee M.T. The antitumor activities of flavonoids. vivo 2005, 19:895-909.
16. Kang G.Y., Lee E.R., Kim J.H., Jung J.W., Lim J., Kim S.K., Cho S.G., Kim K.P. Downregulation of PLK-1 expression in kaempferol-induced apoptosis of MCF-7 cells. Eur. J. Pharmacol. 2009, 611:17-21.
17. Lee E.R., Kang Y.J., Kim J.H., Lee H.T., Cho S.G. Modulation of apoptosis in HaCaT keratinocytes via differential regulation of ERK signaling pathway by flavonoids. J. Biol. Chem. 2005, 280:31498-31507.
18. Lee H.S., Cho H.J., Yu R., Lee K.W., Chun H.S., Park J.H. Mechanisms underlying apoptosis-inducing effects of Kaempferol in HT-29 human colon cancer cells. Int. J. Mol. Sci. 2014, 15:2722-2737.
19. Li W., Du B., Wang T., Wang S., Zhang J. Kaempferol induces apoptosis in human HCT116 colon cancer cells via the Ataxia-Telangiectasia Mutated-p53 pathway with the involvement of p53 upregulated modulator of apoptosis. Chem. Biol. Interact. 2009, 177:121-127.
20. Marfe G., Tafani M., Indelicato M., Sinibaldi-Salimei P., Reali V., Pucci B., Fini M., Russo M.A. Kaempferol induces apoptosis in two different cell lines via Akt inactivation, Bax and SIRT3 activation, and mitochondrial dysfunction. J. Cell. Biochem. 2009, 106:643-650.
21. Martin G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:7634-7638.
22. Miean K.H., Mohamed S. Flavonoid (myricetin, quercetin, kaempferol, luteolin, and apigenin) content of edible tropical plants. J. Agric. Food Chem. 2001, 49:3106-3112.
23. Nguyen T.T., Tran E., Ong C.K., Lee S.K., Do P.T., Huynh T.T., Nguyen T.H., Lee J.J., Tan Y., Ong C.S., Huynh H. Kaempferol-induced growth inhibition and apoptosis in A549 lung cancer cells is mediated by activation of MEK-MAPK. J. Cell. Physiol. 2003, 197:110-121.
24. Pereira S.L., Graos M., Rodrigues A.S., Anjo S.I., Carvalho R.A., Oliveira P.J., Arenas E., Ramalho-Santos J. Inhibition of mitochondrial complex III blocks neuronal differentiation and maintains embryonic stem cell pluripotency. PLoS One 2013, 8:e82095.
25. Pereira S.L., Rodrigues A.S., Sousa M.I., Correia M., Perestrelo T., Ramalho-Santos J. From gametogenesis and stem cells to cancer: common metabolic themes. Hum. Reprod. Update 2014, 20:924-943.
26. Rodrigues A.S., Correia M., Gomes A., Pereira S.L., Perestrelo T., Sousa M.I., Ramalho-Santos J. Dichloroacetate, the Pyruvate Dehydrogenase complex and the Modulation of mESC pluripotency. PLoS One 2015, 10:e0131663.
27. Rodrigues A.S., Pereira S.L., Correia M., Gomes A., Perestrelo T., Ramalho-Santos J. Differentiate or Die: 3-Bromopyruvate and pluripotency in mouse embryonic stem cells. PLoS One 2015, 10:e0135617.
28. Sak K. Cytotoxicity of dietary flavonoids on different human cancer types. Pharmacogn. Rev. 2014, 8:122-146.
29. Sak K., Everaus H. Role of flavonoids in future anticancer therapy by eliminating the cancer stem cells. Curr. Stem Cell Res. Ther. 2015, 10:271-282.
30. Sharma V., Joseph C., Ghosh S., Agarwal A., Mishra M.K., Sen E. Kaempferol induces apoptosis in glioblastoma cells through oxidative stress. Mol. Cancer Ther. 2007, 6:2544-2553.
31. Smith A.G., Heath J.K., Donaldson D.D., Wong G.G., Moreau J., Stahl M., Rogers D. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 1988, 336:688-690.
32. Sousa M.I., Rodrigues A.S., Pereira S., Perestrelo T., Correia M., Ramalho-Santos J. Mitochondrial mechanisms of metabolic reprogramming in proliferating cells. Curr. Med. Chem. 2015.
33. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
34. Toh J.Y., Tan V.M., Lim P.C., Lim S.T., Chong M.F. Flavonoids from fruit and vegetables: a focus on cardiovascular risk factors. Curr. Atheroscler. Rep. 2013, 15:368.
35. Trivedi R., Kumar S., Kumar A., Siddiqui J.A., Swarnkar G., Gupta V., Kendurker A., Dwivedi A.K., Romero J.R., Chattopadhyay N. Kaempferol has osteogenic effect in ovariectomized adult Sprague-Dawley rats. Mol. Cell. Endocrinol. 2008, 289:85-93.
36. Varum S., Rodrigues A.S., Moura M.B., Momcilovic O., Easley C.A.t, Ramalho-Santos J., Van Houten B., Schatten G. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 2011, 6:e20914.
37. Vega-Naredo I., Loureiro R., Mesquita K.A., Barbosa I.A., Tavares L.C., Branco A.F., Erickson J.R., Holy J., Perkins E.L., Carvalho R.A., Oliveira P.J. Mitochondrial metabolism directs stemness and differentiation in P19 embryonal carcinoma stem cells. Cell Death Differ. 2014, 21:1560-1574.
38. Ware C.B., Nelson A.M., Mecham B., Hesson J., Zhou W., Jonlin E.C., Jimenez-Caliani A.J., Deng X., Cavanaugh C., Cook S., Tesar P.J., Okada J., Margaretha L., Sperber H., Choi M., Blau C.A., Treuting P.M., Hawkins R.D., Cirulli V., Ruohola-Baker H. Derivation of naive human embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:4484-4489.
39. Weseler A.R., Ruijters E.J., Drittij-Reijnders M.J., Reesink K.D., Haenen G.R., Bast A. Pleiotropic benefit of monomeric and oligomeric flavanols on vascular health-a randomized controlled clinical pilot study. PLoS One 2011, 6:e28460.
40. Williams R.L., Hilton D.J., Pease S., Willson T.A., Stewart C.L., Gearing D.P., Wagner E.F., Metcalf D., Nicola N.A., Gough N.M. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 1988, 336:684-687.
41. Yans A., Shahamati S.Z., Maghsoudi A.H., Maghsoudi N. Digitoflavone provokes mitochondrial biogenesis in PC12 cells: a protective approach to oxidative stress. Pharm. Biol. 2015, 1-8.
42. Yao L.H., Jiang Y.M., Shi J., Tomas-Barberan F.A., Datta N., Singanusong R., Chen S.S. Flavonoids in food and their health benefits. Plant Foods Hum. Nutr. 2004, 59:113-122.
43. Ying Q.L., Nichols J., Chambers I., Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 2003, 115:281-292.
44. Zhang Y., Wang D., Yang L., Zhou D., Zhang J. Purification and characterization of flavonoids from the leaves of Zanthoxylum bungeanum and correlation between their structure and antioxidant activity. PLoS One 2014, 9:e105725.
45. Zhou W., Choi M., Margineantu D., Margaretha L., Hesson J., Cavanaugh C., Blau C.A., Horwitz M.S., Hockenbery D., Ware C., Ruohola-Baker H. HIF1alpha induced switch from bivalent to exclusively glycolytic metabolism during ESC-to-EpiSC/hESC transition. EMBO J. 2012, 31:2103-2116.