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Ethanolic extract of Salvia officinalis alter vascular endothelial growth factor gene expression and its receptors in the mouse endometrium at preimplantation

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Abstract

Salvia officinalis contains steroid and isoflavonoid coumestrol, daidzein, and genistein which are considered as phytoestrogens. Isoflavones are alternatives to hormone replacement treatment. No studies have been conducted on the effect of S. officinalis extraction on endometrial angiogenesis yet. The adult female mice in the test group received an ethanolic extract of the S. officinalis (100 mg/kg) once a day for 14 days then pseudopregnancy was induced. Uterine horns were removed for molecular and histological assessment in each group. Motic image software was used to assess the quantitative vascular parameters, and real-time PCR was done to determine vascular gene expression in the endometrium. Data analysis on gene expression showed a decrease in rate of vascular endothelial growth factor (VEGF) gene expression (1.559). VEGF receptor gene expression is accompanied by an increase in the rate of kinase insert domain protein receptor (KDR) gene expression (2.504) and FMS-like tyrosine kinase 1 (FLT1) gene expression (0.606). Although there was no significant difference in vascular density between control and test groups, a significant difference (p ≤ 0.05) was evident in the intravascular area between control and test groups at preimplantation time. It is concluded that S. officinalis may affect on implantation media because decidual angiogenesis has a main role in the maintenance of pregnancy at implantation time.

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References

  • Alarcon-Aguilar FJ, Roman-Ramos R, Flores-Saenz JL, Aguirre-Garcia F (2002) Investigation on the hypoglycaemic effects of extracts of four Mexican medicinal plants in normal and alloxan diabetic mice. Phytother Res 16:383–386

    Article  CAS  PubMed  Google Scholar 

  • Baricevic D, Sosa S, Della LR, Tubaro A, Simonovska B, Krasna A, Zupancic A (2001) Topical anti-inflammatory activity of Salvia officinalis L. leaves: the relevance of ursolic acid. J Ethnopharmacol 75:125–132

    Article  CAS  PubMed  Google Scholar 

  • Cha J, Sun X, Dey SK (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat Med 6:1754–1767

    Article  Google Scholar 

  • Chakraborty I, Das SK, Dey S (1995) Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation. J Endocrinol 147:339–352

    Article  CAS  PubMed  Google Scholar 

  • Ciotta L, Stracquadanio M, Pagano I, And A, Valenti O, Roccasalva L (2012) Clinical effects of treatment with phytoestrogens in postmenopausal women. Minerva Ginecol 64:15–22

    CAS  PubMed  Google Scholar 

  • De Leo V, Lanzetta D, Cazzavacca R, Morgante G (1998) Treatment of neurovegetative menopausal symptoms with a phytotherapeutic agent. Minerva Ginecol 50:207–211

    PubMed  Google Scholar 

  • Dinga M, Yea T-X, Zhaoa G-R, Yuana Y-J, Guo Z-X (2005) Aqueous extract of Salvia miltiorrhiza attenuates increased endothelial permeability induced by tumor necrosis factor-α. Int Immunopharmacol 5:1641–1651

    Article  Google Scholar 

  • Dosiou C, Giudice LC (2005) Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 26:44–62

    Article  CAS  PubMed  Google Scholar 

  • Douglas NC, Tang H, Gomez R, Pytowski B, Hicklin DJ, Sauer CM et al (2009) Vascular endothelial growth factor receptor 2 (VEGFR-2) functions to promote uterine decidual angiogenesis during early pregnancy in the mouse. Endocrinology 6:3845–3854

    Article  Google Scholar 

  • Fest S, Aldo PB, Abrahams VM, Visintin I, Alvero A, Chen R et al (2007) Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy. Am J Reprod Immunol 6:55–66

    Article  Google Scholar 

  • Gille H, Kowalski J, Li B, LeCouter J, Moffat B, Zioncheck TF et al (2001) Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J Biol Chem 276:3222–3230

    Article  CAS  PubMed  Google Scholar 

  • Hervé MAJ, Meduri G, Petit FG, Domet TS, Lazennec G, Mourah S et al (2006) Regulation of the vascular endothelial growth factor (VEGF) receptor KDR-1/KDR by estradiol through VEGF in uterus. J Endocrinol 188:91–99

    Article  PubMed  Google Scholar 

  • Heryanto B, Girling JE, Rogers PA (2004) Intravascular neutrophils partially mediate the endometrial endothelial cell proliferative response to oestrogen in ovariectomised mice. Reproduction 127:613–620

    Article  CAS  PubMed  Google Scholar 

  • Hohmann J, Zupko I, Redei D, Csanyi M, Falkay G, Mathe I et al (1999) Protective effects of the aerial parts of Salvia officinalis, Melissa officinalis, and Lavandula angustifolia and their constituents against enzyme-dependent and enzyme-independent lipid peroxidation. Planta Med 65:576–578

    Article  CAS  PubMed  Google Scholar 

  • Islam MW, Tariq M, Ageel AM, al-Said MS, al-Yhya AM (1991) Effect of Salvia haematodes on sexual behavior of male rats. J Ethnopharmacol 33:67–7

    Article  CAS  PubMed  Google Scholar 

  • Jedinák A, Mucková M, Kost'álová D, Maliar T, Masterova I (2006) Antiprotease and anti-metastatic activity of ursolic acid isolated from Salvia officinalis. Z Naturforsch C 61:777–782

    Article  PubMed  Google Scholar 

  • Liu YX, Gao F, Wei P, Chen XL, Gao HJ, Zou RJ, Siao LJ, Xu FH, Feng Q, Liu K, Hu ZY (2005) Involvement of molecules related to angiogenesis, proteolysis and apoptosis in implantation in rhesus monkey and mouse. Contraception 71:249–262

    Article  PubMed  Google Scholar 

  • Lu Y, Foo LY (2000) Flavonoid and phenolic glycosides from Salvia officinalis. Phytochemistry 55:263–267

    Article  PubMed  Google Scholar 

  • Miller L, Hunt JS (1996) Sex steroid hormones and macrophage function. Life Sci 59:1–14

    Article  CAS  PubMed  Google Scholar 

  • Navot D, Margalioth EJ, Laufer N, Birkenfeld A, Relou A, Rosler A et al (1987) Direct correlation between plasma renin activity and severity of the ovarian hyperstimulation syndrome. Fertil Steril 48:57–61

    Article  CAS  PubMed  Google Scholar 

  • Okada H, Tsutsumi A, Imai M, Nakajima T, Yasuda K, Kanzaki H (2010) Estrogen and selective estrogen receptor modulators regulate vascular endothelial growth factor and soluble vascular endothelial growth factor receptor in human endometrial stromal cells. Fertil Steril 93:2680–2686

    Article  CAS  PubMed  Google Scholar 

  • Plaks V, Birnberg T, Berkutzki T, Sela S, BenYashar A, Kalchenko V et al (2008) Uterine DCs are crucial for decidua formation during embryo implantation in mice. J Clin Invest 118:3954–3965

    CAS  PubMed  PubMed Central  Google Scholar 

  • Plank MJ, Sleeman BD (2003) A reinforced random walk model of tumour angiogenesis and anti‐angiogenic strategies. Math Med Biol 20:135–181

    Article  CAS  PubMed  Google Scholar 

  • Rabbani ML, Rogers PA (2001) Role of vascular endothelial growth factor in endometrial vascular events before implantation in rats. Reproduction 6:85–90

    Article  Google Scholar 

  • Rockwell LC, Pillai S, Olson CE, Koos RD (2002) Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents. Biol Reprod 6:1804–1810

    Article  Google Scholar 

  • Senger DR, Connolly DT, Van de Water L, Feder J, Dvorak HF (1990) Purification and NH2-terminal amino acid sequence of guinea pig tumor-secreted vascular permeability factor. Cancer Res 50:1774–1778

    CAS  PubMed  Google Scholar 

  • Sengupta J, Lalitkumar PG, Najwa AR, Charnock-Jones DS, Evans AL, Sharkey AM et al (2007) Immunoneutralization of vascular endothelial growth factor inhibits pregnancy establishment in the rhesus monkey (Macacamulatta). Reproduction 6:1199–1211

    Article  Google Scholar 

  • Shifren JL, Tseng JF, Zaloudek CJ, Ryan IP, Meng YG, Ferrara N, Jaffe RB, Taylor RN (1996) Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. J Clin Endocrinol Metab 81:3112–3118

    CAS  PubMed  Google Scholar 

  • Walker JB, Sytsma KJ, Treutlein J, Wink M (2004) Salvia (Lamiaceae) is not monophyletic: implications for the systematics, radiation, and ecological specializations of Salvia and tribe Mentheae. Am J Bot 91:1115–1125

    Article  PubMed  Google Scholar 

  • Wickström SA, Alitalo K, Keski-Oja J (2004) An endostatin-derived peptide interacts with integrins and regulates actin cytoskeleton and migration of endothelial cells. J Biol Chem 279:20178–20185

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Razi herbal medicines research center of Lorestan University of Medical Sciences.

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Authors and Affiliations

  1. Razi Herbal Medicines Research Center, Lorestan University of Medical Sciences, Khorramabad, Iran

    Nasim Beigi Boroujeni

  2. Department of Biochemistry, Payame Noor University of Tehran, Tehran, Iran

    Masoud Beigi Boroujeni & Afsaneh Shafiei

  3. Department of Anatomical Sciences, Lorestan University of Medical Sciences, Khorramabad, Iran

    Mohammadreza Gholami

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  1. Nasim Beigi Boroujeni
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  2. Masoud Beigi Boroujeni
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Correspondence to Nasim Beigi Boroujeni.

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Beigi Boroujeni, N., Beigi Boroujeni, M., Gholami, M. et al. Ethanolic extract of Salvia officinalis alter vascular endothelial growth factor gene expression and its receptors in the mouse endometrium at preimplantation. Comp Clin Pathol 25, 125–129 (2016). https://doi.org/10.1007/s00580-015-2152-6

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  • DOI: https://doi.org/10.1007/s00580-015-2152-6

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