Hexane extract of aged black garlic reduces cell proliferation and attenuates the expression of ICAM-1 and VCAM‑1 in TNF-α-activated human endometrial stromal cells

Kim,Ki-Hyung; Park,Jin  Kyeong; Choi,Young-Whan; Kim,Youn-Han; Lee,Eun  Na; Lee,Ja-Rang; Kim,Heui-Soo; Baek,Sun-Yong; Kim,Bong-Seon; Lee,Kyu-Sup; Yoon,Sik

doi:10.3892/ijmm.2013.1362

Hexane extract of aged black garlic reduces cell proliferation and attenuates the expression of ICAM-1 and VCAM‑1 in TNF-α-activated human endometrial stromal cells

Authors:
- Ki-Hyung Kim
- Jin Kyeong Park
- Young-Whan Choi
- Youn-Han Kim
- Eun Na Lee
- Ja-Rang Lee
- Heui-Soo Kim
- Sun-Yong Baek
- Bong-Seon Kim
- Kyu-Sup Lee
- Sik Yoon
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Affiliations: Department of Obstetrics and Gynecology, Pusan National University School of Medicine, Busan 602-739, Republic of Korea, Department of Anatomy, Pusan National University School of Medicine, Yangsan 626-870, Republic of Korea, Department of Horticultural Bioscience, College of Natural Resources and Life Science, Pusan National University, Miryang 627-706, Republic of Korea, Department of Biological Sciences, College of Natural Sciences, Pusan National University, Busan 609-735, Republic of Korea
Published online on: April 25, 2013 https://doi.org/10.3892/ijmm.2013.1362
Pages: 67-78

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Abstract

Increasing evidence indicates the potentially crucial roles of intercellular adhesion molecule-1 (ICAM-1) and vascular cell adhesion molecule-1 (VCAM-1) in the pathological process underlying endometriosis. The present study aimed to investigate the effects of a hexane extract of aged black garlic (HEABG) on the proliferation and expression of ICAM-1 and VCAM-1 in tumor necrosis factor-α (TNF-α)-activated human endometrial stromal cells (HESCs) isolated from patients with endometriosis. HESCs were isolated from endometriotic tissues obtained from women with advanced endometriosis who underwent laparoscopic surgery for ovarian endometrioma (n=18). Cell proliferation and cell cycle analysis were assessed by WST-1 assay and flow cytometry, respectively. The expression of ICAM-1 and VCAM-1 was measured by flow cytometry, immunofluorescence staining, immunoblotting and quantitative reverse transcriptase-PCR. The secretion of interleukin-6 (IL-6) was determined by enzyme-linked immunosorbent assay (ELISA). The activation of nuclear factor-κB (NF-κB) and activator protein-1 (AP-1) was detected by electrophoretic mobility shift assay (EMSA) and the activation of c-Jun N-terminal kinase (JNK), extracellular signal-regulated kinase (ERK) and p38 MAPK was analyzed by immunoblotting. Cell proliferation and cell cycle progression were significantly suppressed by HEABG in the TNF-α-induced HESCs through the inhibition of the ERK and JNK signaling pathways. Remarkably, the treatment of the HESCs with HEABG potently suppressed the TNF-α-induced ICAM-1 and VCAM-1 transcript and protein expression by inhibiting the activation of NF-κB and AP-1 transcription factors. Our results suggest that HEABG may be effective in the prevention and treatment of endometriosis in humans.

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1.	Sampson JA: The development of the implantation theory for the origin of peritoneal endometriosis. Am J Obstet Gynecol. 40:549–557. 1940.
2.	Paul Dmowski W and Braun DP: Immunology of endometriosis. Best Pract Res Clin Obstet Gynaecol. 18:245–263. 2004.
3.	Olovsson M: Immunological aspects of endometriosis: an update. Am J Reprod Immunol. 66(Suppl 1): 101–104. 2011. View Article : Google Scholar
4.	Mousa SA: Cell adhesion molecules: potential therapeutic and diagnostic implications. Mol Biotechnol. 38:33–40. 2008. View Article : Google Scholar : PubMed/NCBI
5.	Wu TC: The role of vascular cell adhesion molecule-1 in tumor immune evasion. Cancer Res. 67:6003–6006. 2007. View Article : Google Scholar : PubMed/NCBI
6.	Somigliana E, Viganò P, Gaffuri B, Guarneri D, Busacca M and Vignali M: Human endometrial stromal cells as a source of soluble intercellular adhesion molecule (ICAM)-1 molecules. Hum Reprod. 11:1190–1194. 1996.PubMed/NCBI
7.	Tabibzadeh SS and Poubouridis D: Expression of leukocyte adhesion molecules in human endometrium. Am J Clin Pathol. 93:183–189. 1990.PubMed/NCBI
8.	Viganó P, Pardi R, Magri B, Busacca M, Di Blasio AM and Vignali M: Expression of intercellular adhesion molecule-1 (ICAM-1) on cultured human endometrial stromal cells and its role in the interaction with natural killers. Am J Reprod Immunol. 32:139–145. 1994.PubMed/NCBI
9.	Viganò P, Gaffuri B, Somigliana E, Busacca M, Di Blasio AM and Vignali M: Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture. Mol Hum Reprod. 4:1150–1156. 1998.PubMed/NCBI
10.	Wu MH, Yang BC, Lee YC, Wu PL and Hsu CC: The differential expression of intercellular adhesion molecule-1 and regulation by interferon-gamma during the pathogenesis of endometriosis. Am J Reprod Immunol. 51:373–380. 2004. View Article : Google Scholar : PubMed/NCBI
11.	Defrère S, Donnez J, Moulin P, Befahy P, Gonzalez-Ramos R, Lousse JC and Van Langendonckt A: Expression of intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in human endometrial stromal and epithelial cells is regulated by interferon-gamma but not iron. Gynecol Obstet Invest. 65:145–154. 2008.PubMed/NCBI
12.	Braun DP, Ding J and Dmowski WP: Peritoneal fluid-mediated enhancement of eutopic and ectopic endometrial cell proliferation is dependent on tumor necrosis factor-alpha in women with endometriosis. Fertil Steril. 78:727–732. 2002. View Article : Google Scholar : PubMed/NCBI
13.	González-Ramos R, Van Langendonckt A, Defrère S, Lousse JC, Colette S, Devoto L and Donnez J: Involvement of the nuclear factor-κB pathway in the pathogenesis of endometriosis. Fertil Steril. 94:1985–1994. 2010.
14.	Yamauchi N, Harada T, Taniguchi F, Yoshida S, Iwabe T and Terakawa N: Tumor necrosis factor-alpha induced the release of interleukin-6 from endometriotic stromal cells by the nuclear factor-kappaB and mitogen-activated protein kinase pathways. Fertil Steril. 82(Suppl 3): 1023–1028. 2004. View Article : Google Scholar
15.	Okamoto H, Cujec TP, Yamanaka H and Kamatani N: Molecular aspects of rheumatoid arthritis: role of transcription factors. FEBS J. 275:4463–4470. 2008. View Article : Google Scholar : PubMed/NCBI
16.	Pittler MH and Ernst E: Clinical effectiveness of garlic (Allium sativum). Mol Nutr Food Res. 51:1382–1385. 2007. View Article : Google Scholar : PubMed/NCBI
17.	Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 67:817–821. 1997. View Article : Google Scholar : PubMed/NCBI
18.	Pino M, Galleguillos C, Torres M, Sovino H, Fuentes A, Boric MA and Johnson MC: Association between MMP1 and MMP9 activities and ICAM-1 cleavage induced by tumor necrosis factor in stromal cell cultures from eutopic endometria of women with endometriosis. Reproduction. 138:837–847. 2009. View Article : Google Scholar : PubMed/NCBI
19.	Prefumo F, Semino C, Melioli G and Venturini PL: A defective expression of ICAM-1 (CD54) on secretory endometrial cells is associated with endometriosis. Immunol Lett. 80:49–53. 2002. View Article : Google Scholar : PubMed/NCBI
20.	Kyama CM, Overbergh L, Mihalyi A, Meuleman C, Mwenda JM, Mathieu C and D’Hooghe TM: Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis. Fertil Steril. 89:301–310. 2008. View Article : Google Scholar : PubMed/NCBI
21.	Sikora J, Mielczarek-Palacz A and Kondera-Anasz Z: Role of natural killer cell activity in the pathogenesis of endometriosis. Curr Med Chem. 18:200–208. 2011. View Article : Google Scholar : PubMed/NCBI
22.	Viganò P, Somigliana E, Gaffuri B, Santorsola R, Busacca M and Vignali M: Endometrial release of soluble intercellular adhesion molecule 1 and endometriosis: relationship to the extent of the disease. Obstet Gynecol. 95:115–118. 2000.PubMed/NCBI
23.	De Placido G, Alviggi C, Di Palma G, Carravetta C, Matarese G, Landino G and Racioppi L: Serum concentrations of soluble human leukocyte class I antigens and of the soluble intercellular adhesion molecule-1 in endometriosis: relationship with stage and non-pigmented peritoneal lesions. Hum Reprod. 13:3206–3210. 1998.
24.	González-Ramos R, Van Langendonckt A, Defrère S, Lousse JC, Mettlen M, Guillet A and Donnez J: Agents blocking the nuclear factor-kappaB pathway are effective inhibitors of endometriosis in an in vivo experimental model. Gynecol Obstet Invest. 65:174–186. 2008.PubMed/NCBI
25.	Nasu K, Nishida M, Ueda T, Yuge A, Takai N and Narahara H: Application of the nuclear factor-kappaB inhibitor BAY 11-7085 for the treatment of endometriosis: an in vitro study. Am J Physiol Endocrinol Metab. 293:E16–E23. 2007. View Article : Google Scholar : PubMed/NCBI
26.	Zhang W and Liu HT: MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 12:9–18. 2002. View Article : Google Scholar : PubMed/NCBI
27.	Wu MH, Wang CA, Lin CC, Chen LC, Chang WC and Tsai SJ: Distinct regulation of cyclooxygenase-2 by interleukin-1beta in normal and endometriotic stromal cells. J Clin Endocrinol Metab. 90:286–295. 2005. View Article : Google Scholar : PubMed/NCBI
28.	Hirota Y, Osuga Y, Hirata T, Harada M, Morimoto C, Yoshino O, Koga K, Yano T, Tsutsumi O and Taketani Y: Activation of protease-activated receptor 2 stimulates proliferation and inter-leukin (IL)-6 and IL-8 secretion of endometriotic stromal cells. Hum Reprod. 20:3547–3553. 2005. View Article : Google Scholar : PubMed/NCBI
29.	Yotova IY, Quan P, Leditznig N, Beer U, Wenzl R and Tschugguel W: Abnormal activation of Ras/Raf/MAPK and RhoA/ROCKII signalling pathways in eutopic endometrial stromal cells of patients with endometriosis. Hum Reprod. 26:885–897. 2011. View Article : Google Scholar : PubMed/NCBI