2017 ; Vol.27-4: 668~677
|Author||Hee-Jung Choi, Tae-Wook Chung, Mi-Ju Park, Hyung Sik Kim, Sooseong You, Myeong Soo Lee, Bo Sun Joo, Kyu Sup Lee, Keuk-Jun Kim, Gabbine Wee, Choong-Yong Kim, Cheorl-Ho Kim, Ki-Tae Ha|
|Place of duty||School of Korean Medicine and Healthy Aging Korean Medicine Research Center, Pusan National University, Yangsan 50612, Republic of Korea|
|Title||Benzoic Acid Enhances Embryo Implantation through LIF-Dependent Expression of Integrin αVβ3 and αVβ5|
J. Microbiol. Biotechnol.2017 ;
|Abstract||Embryo implantation is the crucial step for a successful pregnancy. Diverse factors, including
adhesion molecules, growth factors, and cytokines are important for embryo implantation
through improving endometrial receptivity. Benzoic acid (BA), a component of various plants,
has been shown to have antifungal and antioxidant effects. However, the effect of BA on
embryo implantation remains unknown. Here, we showed the contribution of BA for the
enhancement of endometrial receptivity through the leukemia inhibitory factor (LIF)-
dependent increase of integrin αV, β3, and β5 expression. Furthermore, in vivo study using a
mifepristone-induced implantation failure model showed that BA definitely improves the
numbers of implantation embryos. Taken together, we suggest that BA has a novel function
for embryo implantation through the up-regulation of LIF-mediated integrins, and may be a
candidate for therapeutic medicine to increase the pregnancy rate.|
|Key_word||Benzoic acid, leukemia inhibitory factor, integrin, adhesion, endometrial receptivity, implantation|
Diedrich K, Fauser BC, Devroey P, Griesinger G. 2007. The role of the endometrium and embryo in human implantation. Hum. Reprod. Update 13: 365-377.
Horne AW, White JO, Lalani EN. 2000. The endometrium and embryo implantation. A receptive endometrium depends on more than hormonal influences. BMJ 321: 1301-1302.
Koot YE, Macklon NS. 2013. Embryo implantation: biology, evaluation, and enhancement. Curr. Opin. Obstet. Gynecol. 25: 274-279.
D imitriadis E, Menkhorst E, Salamonsen LA, Paiva P. 2010. Review: LIF and IL11 in trophoblast-endometrial interactions during the establishment of pregnancy. Placenta 31 Suppl:S99-S104.
Cu llinan EB, Abbondanzo SJ, Anderson PS, Pollard JW, Lessey BA, Stewart CL. 1996. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation. Proc. Natl. Acad. Sci. USA 93: 3115-3120.
Ag hajanova L. 2010. Update on the role of leukemia inhibitory factor in assisted reproduction. Curr. Opin. Obstet. Gynecol. 22:213-219.
Wu M , Yin Y, Z hao M, Hu L, C hen Q. 2013. The l ow expression of leukemia inhibitory factor in endometrium:possible relevant to unexplained infertility with multiple implantation failures. Cytokine 62: 334-339.
St eck T, Giess R, Suetterlin MW, Bolland M, Wiest S, Poehls UG, Dietl J. 2004. Leukaemia inhibitory factor (LIF) gene mutations in women with unexplained infertility and recurrent failure of implantation after IVF and embryo transfer. Eur. J. Obstet. Gynecol. Reprod. Biol. 112: 69-73.
Ter akawa J, Wakitani S, Sugiyama M, Inoue N, Ohmori Y, Kiso Y, et al. 2011. Embryo implantation is blocked by intraperitoneal injection with anti-LIF antibody in mice. J. Reprod. Dev. 57: 700-707.
Me nkhorst E, Zhang JG, Sims NA, Morgan PO, Soo P, Poulton IJ, et al. 2011. Vaginally administered PEGylated LIF antagonist blocked embryo implantation and eliminated non-target effects on bone in mice. PLoS One 6: e19665.
As chenbach LC, Hester KE, McCann NC, Zhang JG, Dimitriadis E, Duffy DM. 2013. The LIF receptor antagonist PEGLA is effectively delivered to the uterine endometrium and blocks LIF activity in cynomolgus monkeys. Contraception 87: 813-823.
Wh ite CA, Zhang JG, Salamonsen LA, Baca M, Fairlie WD, Metcalf D, et al. 2007. Blocking LIF a ction in the u terus by using a PEGylated antagonist prevents implantation: a nonhormonal contraceptive strategy. Proc. Natl. Acad. Sci. USA 104: 19357-19362.
L essey BA, Damjanovich L, Coutifaris C, Castelbaum A, Albelda SM, Buck CA. 1992. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J. Clin. Invest. 90: 188-195.
Lessey BA. 1998. Endometrial integrins and the establishment of uterine receptivity. Hum. Reprod. 13 Suppl 3: 247-258; discussion 259-261.
L essey BA, Castelbaum AJ, Sawin SW, Sun JH. 1995. Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil. Steril. 63: 535-542.
Nair B. 2001. Final report on the safety assessment of benzyl alcohol, benzoic acid, and sodium benzoate. Int. J. Toxicol. 20 Suppl 3: 23-50.
L ondon RE, Gabel SA. 1988. A deuterium surface coil NMR study of the metabolism of D-methionine in the liver of the anesthetized rat. Biochemistry 27: 7864-7869.
Oya nagi K, Kuniya Y, Nagao M, Tsuchiyama A, Nakao T. 1987. Cytotoxicities of sodium benzoate in primary culture of hepatocytes from adult rat liver. Tohoku J. Exp. Med. 152:47-51.
Przybyszewski WM, Malec J. 1982. Protection against hydroxyurea-induced cytotoxic effects in L5178Y cells by free radical scavengers. Cancer Lett. 17: 223-228.
Cerv antes A, Pinedo HM, Lankelma J, Schuurhuis GJ. 1988. The role of oxygen-derived free radicals in the cytotoxicity of doxorubicin in multidrug resistant and sensitive human ovarian cancer cells. Cancer Lett. 41: 169-177.
Su thanthiran M, Solomon SD, Williams PS, Rubin AL, Novogrodsky A, Stenzel KH. 1984. Hydroxyl radical scavengers inhibit human natural killer cell activity. Nature 307: 276-278.
Cheu ng K, Archibald AC, Robinson MF. 1984. Luminoldependent chemiluminescence produced by neutrophils stimulated by immune complexes. Aust. J. Exp. Biol. Med. Sci. 62: 403-419.
Walker PD, Shah SV. 1988. Evidence suggesting a role for hydroxyl radical in gentamicin-induced acute renal failure in rats. J. Clin. Invest. 81: 334-341.
Evangelista S, Meli A. 1985. Influence of antioxidants and radical scavengers on ethanol-induced gastric ulcers in the rat. Gen. Pharmacol. 16: 285-286.
Chu ng TW, Kim SJ, Choi HJ, Song KH, Jin UH, Yu DY, et al. 2014. Hepatitis B virus X protein specially regulates the sialyl Lewis A synthesis among glycosylation events for metastasis. Mol. Cancer 13: 222.
Ki m EY, Choi HJ, Chung TW, Jang SB, Kim K, Ha KT. 2015. Expression and efficient one-step chromatographic purification of a soluble antagonist for human leukemia inhibitory factor receptor in Escherichia coli. J. Microbiol. Biotechnol. 25: 1307-1314.
Ch oi HJ, Chung TW, Park MJ, Lee KS, Yoon Y, Kim HS, et al. 2016. Paeonia lactiflora enhances the adhesion of trophoblast to the endometrium via induction of leukemia inhibitory factor expression. PLoS One 11: e0148232.
Brown JK, Shaw JL, Critchley HO, Horne AW. 2012. Human fallopian tube epithelium constitutively expresses integrin endometrial receptivity markers: no evidence for a tubal implantation window. Mol. Hum. Reprod. 18: 111-120.
Kn udtson JF, Tekmal RR, Santos MT, Binkley PA, Krishnegowda N, Valente P, Schenken RS. 2015. Impaired development of early endometriotic lesions in CD44 knockout mice. Reprod. Sci. 23: 87-91.
Zh ang Y, Liu S, Liu Y, Wang Z, Wang X, Yan Q. 2009. Overexpression of fucosyltransferase VII (FUT7) promotes embryo adhesion and implantation. Fertil. Steril. 91: 908-914.
Chen JR, Cheng JG, Shatzer T, Sewell L, Hernandez L, Stewart CL. 2000. Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 141: 4365-4372.
L iang XH, Deng WB, Li M, Zhao ZA, Wang TS, Feng XH, et al. 2014. Egr1 protein acts downstream of estrogen-leukemia inhibitory factor (LIF)-STAT3 pathway and plays a role during implantation through targeting Wnt4. J. Biol. Chem. 289: 23534-23545.
Hu W, Feng Z, Teresky AK, Levine AJ. 2007. p53 regulates maternal reproduction through LIF. Nature 450: 721-724.
L ubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. 1993. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. USA 90: 11162-11166.
v on Grothusen C, Lalitkumar S, Boggavarapu NR, GemzellDanielsson K, Lalitkumar PG. 2014. Recent advances in understanding endometrial receptivity: molecular basis and clinical applications. Am. J. Reprod. Immunol. 72: 148-157.
Makker A, Singh MM. 2006. Endometrial receptivity: clinical assessment in relation to fertility, infertility, and antifertility. Med. Res. Rev. 26: 699-746.
Mains L, Van Voorhis BJ. 2010. Optimizing the technique of embryo transfer. Fertil. Steril. 94: 785-790.
Zh ang YM, Zhang YY, Bulbul A, Shan X, Wang XQ, Yan Q. 2015. Baicalin promotes embryo adhesion and implantation by upregulating fucosyltransferase IV (FUT4) via Wnt/betacatenin signaling pathway. FEBS Lett. 589: 1225-1233.
Zhao M, Chang C, Liu Z, Chen LM, Chen Q. 2010. Treatment with low-dose aspirin increased the level LIF and integrin beta3 expression in mice during the implantation window. Placenta 31: 1101-1105.
Chu ng TW, Park MJ, Kim HS, Choi HJ, Ha KT. 2016. Integrin αVβ3 and αVβ5 are required for leukemia inhibitory factor-mediated the adhesion of trophoblast cells to the endometrial cells. Biochem. Biophys. Res. Commun. 469: 936-940.
Agca C, Gubler A, Traber G, Beck C, Imsand C, Ail D, et al. 2013. p38 MAPK signaling acts upstream of LIF-dependent neuroprotection during photoreceptor degeneration. Cell Death Dis. 4: e785.
Fan Z, Bau B, Yang H, Aigner T. 2004. IL-1beta induction of IL-6 and LIF in normal articular human chondrocytes involves the ERK, p38 and NFkappaB signaling pathways. Cytokine 28: 17-24.
Car ino C, Olawaiye AB, Cherfils S, Serikawa T, Lynch MP, Rueda BR, Gonzalez RR. 2008. Leptin regulation of proangiogenic molecules in benign and cancerous endometrial cells. Int. J. Cancer 123: 2782-2790.
Wu GS. 2004. The functional interactions between the p53 and MAPK signaling pathways. Cancer Biol. Ther. 3: 156-161.
Schneider G, Kramer OH. 2011. NFkappaB/p53 crosstalk a promising new therapeutic target. Biochim. Biophys. Acta 1815: 90-103.
Abraham AG, O’Neill E. 2014. PI3K/Akt-mediated regulation of p53 in cancer. Biochem. Soc. Trans. 42: 798-803.
F eng Z, Zhang C, Kang HJ, Sun Y, Wang H, Naqvi A, et al. 2011. Regulation of female reproduction by p53 and its family members. FASEB J. 25: 2245-2255.
Yang ZM, Chen DB, Le SP, Harper MJ. 1996. Differential hormonal regulation of leukemia inhibitory factor (LIF) in rabbit and mouse uterus. Mol. Reprod. Dev. 43: 470-476.
Arici A, Engin O, Attar E, Olive DL. 1995. Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in human endometrium. J. Clin. Endocrinol. Metab. 80: 1908-1915.
Aghajanova L. 2004. Leukemia inhibitory factor and human embryo implantation. Ann. NY Acad. Sci. 1034: 176-183.
Danielsson KG, Swahn ML, Bygdeman M. 1997. The effect of various doses of mifepristone on endometrial leukaemia inhibitory factor expression in the midluteal phase - an immunohistochemical study. Hum. Reprod. 12: 1293-1297.
L alitkumar PG, Lalitkumar S, Meng CX, Stavreus-Evers A, Hambiliki F, Bentin-Ley U, Gemzell-Danielsson K. 2007. Mifepristone, but not levonorgestrel, inhibits human blastocyst attachment to an in vitro endometrial three-dimensional cell culture model. Hum. Reprod. 22: 3031-3037.
Hazan R, Levine A, Abeliovich H. 2004. Benzoic acid, a weak organic acid food preservative, exerts specific effects on intracellular membrane trafficking pathways in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 70: 4449-4457.