Abstract
RECK (reversion-inducing cysteine-rich protein with Kazal motifs) is a membrane-anchored glycoprotein which regulates MMP2 and MMP9 activity and has been proposed to play a role in embryo implantation while misexpression of RECK has been associated with a variety of carcinomas. Unfortunately, understanding on the steroidal regulation of uterine RECK is lacking. To address this gap in our knowledge, we examined steroidal regulation and cellular expression of Reck mRNA and protein within the mouse uterus in vivo. Uterine Reck mRNA and protein were decreased by estrogen, while progesterone alone had no effect. The estrogen-induced down regulation could be partially blocked by progesterone. RECK was localized primarily to luminal and glandular epithelial cells and the level of expression was regulated in a similar fashion as in whole tissue by the steroids. Knock-down of endogenous RECK in human endometrial epithelial and stromal cells resulted in a significant increase in active MMP9 expression but not that of pro-MMP9 or MMP2. These studies demonstrate that RECK expression in the mouse uterus is steroidally regulated and that within endometrial epithelial and stromal cells, RECK regulates MMP9, but not MMP2 activity.
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T.E. Curry Jr., K.G. Osteen, Endo. Rev. 24, 428–465 (2003)
P.B. Cornet, C. Galant, Y. Eeckhout, P.J. Courtoy, E. Marbaix, P. Henriet, J. Clin. Endocrinol. Metab. 90, 1001–1011 (2005)
C. Galant, M. Berliere, D. Dubois, J.C. Verougstraete, A. Charles, P. Lemoine, I. Kokorine, Y. Eeckhout, P.J. Courtoy, E. Marbaix, Am. J. Pathol. 165, 83–94 (2004)
M. Hickey, J. Higham, M. Sullivan, L. Miles, I.S. Fraser, Fertil. Steril. 75, 288–296 (2001)
A.J. Vincent, N. Malakooti, J. Zhang, P.A. Rogers, B. Affandi, L.A. Salamonsen, Hum. Reprod. 14, 807–815 (1999)
H.W. Chung, J.Y. Lee, H.S. Moon, S.E. Hur, M.H. Park, Y. Wen, M.L. Polan, Fertil. Steril. 78, 787–795 (2001)
T. Collette, C. Bellehumeur, R. Kats, R. Maheux, J. Mailloux, M. Villeneuve, A. Akoum, Hum. Reprod. 19, 1257–1264 (2004)
T. Collette, R. Maheux, J. Mailloux, A. Akoum, Hum. Reprod. 21, 3059–3067 (2006)
J. Szamatowicz, P. Laudanski, I. Tomaszewska, Hum. Reprod. 17, 284–288 (2002)
N. Inagaki, C. Stern, J. McBain, A. Lopata, L. Kornman, D. Wilkinson, Hum. Reprod. 18, 608–615 (2003)
N. Inagaki, L. Ung, T. Otani, D. Wilkinson, A. Lopata, Eur. J. Obstet. Gynecol. Reprod. 111, 197–203 (2003)
K. Aglund, M. Rauvala, U. Puistola, T. Angstrom, T. Turpeenniemi-Hujanen, B. Zackrission, U. Stendahl, Gynecol. Oncol. 94, 699–704 (2004)
L.A. DiNezza, A. Misajon, J. Zhang, T. Jobling, M.A. Quinn, A.G. Ostor, G. Nie, A. Lopata, L.A. Salamonsen, Cancer 94, 1466–1475 (2002)
N. Karahan, M. Güney, S. Baspinar, B. Oral, N. Kapucuoglu, T. Mungan, Eur. J. Gynaecol. Oncol. 28, 184–188 (2007)
A. Lopata, F. Agresta, M.A. Quinn, C. Smith, A.G. Ostor, L.A. Salamonsen, Gynecol. Oncol. 90, 318–324 (2003)
Y. Soini, E. Alarakkola, H. Autio-Harmainen, Hum. Pathol. 28, 220–226 (1997)
J.E. Fata, A.T. Ho, K.J. Leco, R.A. Moorehead, R. Khokha, Cell. Mol. Life Sci. 57, 77–95 (2000)
D.E. Gomez, D.F. Alonso, H. Yoshiji, U.P. Thorgeirsson, Eur. J. Cell Biol. 74, 111–122 (1997)
K.J. Leco, S.S. Apte, G.T. Taniguchi, S.P. Hawkes, R. Khokha, G.A. Schultz, D.R. Edwards, FEBS Lett. 401, 213–217 (1997)
W.B. Nothnick, Biol. Reprod. 63, 905–912 (2000)
J. Zhang, L.A. Salamonsen, Mol. Hum. Reprod. 3, 735–741 (1997)
A.L. Hampton, L.A. Salamonsen, J. Endocrinol. 141, R1–R3 (1994)
T. Higuchi, H. Kanzaki, H. Nakayama, M. Fujimoto, H. Hatayama, K. Kojima, M. Iwai, T. Mori, J. Fujita, Endocrinology 136, 4973–4981 (1995)
W. Rodgers, L.M. Matrisian, L.C. Giudice, B. Dsupin, P. Cannon, C. Svitek, F. Gorstein, K.G. Osteen, J. Clin. Invest. 94, 946–953 (1994)
R.M. Brenner, L. Rudolph, L. Matrisian, O.D. Slayden, Hum. Reprod. 11, 150–164 (1996)
L.A. Rudolph-Owen, O.D. Slayden, L.M. Matrisian, R.M. Brenner, Biol. Reprod. 59, 1349–1359 (1998)
L.A. Salamonsen, A.R. Butt, F.R. Hammond, S. Garcia, J. Zhang, J. Clin. Endocrinol. Metab. 82, 1409–1415 (1997)
C. Takahashi, Z. Sheng, T.P. Horan, H. Kitayama, M. Maki, K. Hitomi, Y. Kitaura, S. Takai, R.M. Sasahara, A. Horimoto, Y. Ikawa, B.J. Ratzkin, T. Arakawa, M. Noda, Proc. Natl. Acad. Sci. USA 95, 13221–13226 (1998)
J. Oh, R. Takahashi, S. Kondo, A. Mizoguchi, E. Adachi, R.M. Sasahara, S. Nishimura, Y. Imamura, H. Kitayama, D.B. Alexander, C. Ide, T.P. Horan, T. Arakawa, H. Yoshida, S. Nishikawa, Y. Itoh, M. Seiki, S. Itohara, C. Takahashi, M. Noda, Cell 107, 789–800 (2001)
M. Noda, C. Takahashi, Cancer Sci. 98, 1659–1665 (2007)
M. Noda, J. Oh, R. Takahashi, S. Kondo, H. Kitayama, C. Takahashi, Cancer Metastasis Rev. 22, 167–175 (2003)
R.K. Nuttall, C.L. Sampieri, C.J. Pennington, S.E. Gill, G.A. Schultz, D.R. Edwards, FEBS Lett. 563, 129–134 (2004)
S.J. Hu, G. Ren, J.L. Liu, Z.A. Zhao, Y.S. Yu, R.W. Su, X.H. Ma, H. Ni, W. Lei, Z.M. Yang, J. Biol. Chem. 283, 473–484 (2008)
E.P. Chandana, Y. Maeda, A. Ueda, H. Kiyonari, N. Oshima, M. Yamamoto, S. Kondo, J. Oh, R. Takahashi, Y. Yoshida, S. Kawashima, D.B. Alexander, H. Kitayama, C. Takahashi, Y. Tabata, T. Matsuzaki, M. Noda, BMC Dev. Biol. 10, 84 (2010)
X. Zhang, E. Hoang, W.B. Nothnick, Mol. Reprod. Dev. 76, 160–172 (2009)
W.B. Nothnick, C. Healy, X. Hong, Endocrine 37, 265–273 (2010)
D.A. Kniss, P.D. Zimmeran, C.L. Garver, R.H. Fertel, Am. J. Obstet. Gynecol. 177, 559–567 (1997)
G. Krikun, G. Mor, A. Alvero, S. Guller, F. Schatz, E. Sapi, M. Rahman, R. Caze, M. Qumsiyeh, C.J. Lockwood, Endocrinology 145, 2291–2296 (2004)
H. Kumamoto, K. Ooya, J. Oral Pathol. Med. 35, 345–351 (2006)
S. Takagi, T. Kitamura, Y. Hosaka, T. Ohsaki, D. Bosnakovsi, T. Kadosawa, M. Okumura, T. Fujinaga, J. Vet. Med. Sci. 67, 385–391 (2005)
M. Echizenya, S. Kondo, R. Takahashi, J. Oh, S. Kawashima, H. Kitayama, C. Takahashi, M. Noda, Oncogene 24, 5850–5857 (2005)
B. Welm, J. Mott, Z. Werb, Curr. Biol. 12, R209–R211 (2002)
S. Kawashima, Y. Imamura, E.P. Chandana, T. Noda, R. Takahashi, E. Adachi, C. Takahashi, M. Noda, J. Neurochem. 104, 376–385 (2008)
T. Accorsi-Mendonca, K.B. Paiva, W.F. Zambuzi, T.M. Cestari, V.S. Lara, M.C. Sogayar, R. Taga, J.M. Granjeiro, J. Mol. Histol. 39, 201–208 (2008)
S. Kondo, C. Shukunami, Y. Morioka, N. Matsumoto, R. Takahashi, J. Oh, T. Atsumi, A. Umezawa, A. Kudo, H. Kitayama, Y. Hiraki, M. Noda, J. Cell Sci. 120, 849–857 (2007)
J. Guo, L. Zou, J. Huazhong Univ. Sci. Technol. Med. Sci. 26, 738–740 (2006)
T. Muraguchi, Y. Takegami, T. Ohtsuka, S. Kitajima, E.P.S. Chandana, A. Omura, T. Miki, R. Takahashi, N. Matsumoto, A. Ludwig, M. Noda, C. Takahashi, Nat. Neurosci. 10, 838–845 (2007)
K. Furumoto, S. Arii, A. Mori, H. Furuyama, M.J. Gorrin Rivas, T. Nakao, N. Isobe, T. Murata, C. Takahashi, M. Noda, M. Imamura, Hepatology 33, 189–195 (2001)
T. Masui, R. Doi, T. Koshiba, K. Fujimoto, S. Tsuji, S. Nakajima, M. Koizumi, E. Toyoda, S. Tulachan, D. Ito, K. Kami, T. Mori, M. Wada, M. Noda, M. Imamura, Clin. Cancer Res. 9, 1779–1784 (2003)
P.N. Span, C.G. Sweep, P. Manders, L.V. Beex, D. Leppert, R.L. Lindberg, Cancer 97, 2710–2715 (2003)
N. Takemoto, M. Tada, Y. Hida, T. Asano, S. Cheng, T. Kuramae, J. Hamada, M. Miyamoto, S. Kondo, T. Moriuchi, Lung Cancer 58, 376–383 (2007)
C.Y. Cho, J.H. Wang, H.C. Chang, C.K. Chang, W.C. Hung, J. Cell. Physiol. 213, 65–69 (2007)
T. Takeuchi, M. Hisanaga, M. Nagao, N. Ikeda, H. Fujii, F. Koyama, T. Mukogawa, H. Matsumoto, S. Kondo, C. Takahashi, M. Noda, Y. Nakajima, Clin. Cancer Res. 10, 5572–5579 (2004)
M.F. van der Jagt, F.C. Sweep, E.T. Waas, T. Hendriks, T.J. Ruers, A.H. Merry, T. Wobbes, P.N. Span, Cancer Lett. 237, 289–297 (2006)
S.L. Li, D.L. Gao, Z.H. Zhao, Z.W. Liu, Q.M. Zhao, J.X. Yu, K.S. Chen, Y.H. Zhang, World J. Gastroenterol. 13, 6076–6081 (2007)
F. Ohl, M. Jung, C. Xu, C. Stephan, A. Rabien, M. Burkhardt, A. Nitsche, G. Kristiansen, S.A. Loening, A. Radonic, K. Jung, J. Mol. Med. 83, 1014–1024 (2005)
A. Rabien, M. Burkhardt, M. Jung, F. Fritzsche, M. Ringsdorf, H. Schicktanz, S.A. Loening, G. Kristiansen, K. Jung, Eur. Urol. 51, 1259–1266 (2007)
A.C. Riddick, C.J. Shukla, C.J. Pennington, R. Bass, R.K. Nuttall, A. Hogan, K.K. Sethia, V. Ellis, A.T. Collins, N.J. Maitland, R.Y. Ball, D.R. Edwards, Br. J. Cancer 92, 2171–2180 (2005)
Y. Li, Y. Zhang, Q. Zheng, J. Huazhong Univ. Sci. Technol. Med. Sci. 25, 552–554 (2005)
S.Y. Song, H.J. Son, E. Nam, J.C. Rhee, C. Park, Eur. J. Cancer 42, 101–108 (2006)
H.G. Kang, H.S. Kim, K.J. Kim, J.H. Oh, M.R. Lee, S.M. Seol, I. Han, J. Orthop. Res. 25, 696–702 (2007)
M. Okamura, A. Unami, M. Moto, M. Muguruma, T. Ito, M. Jin, Y. Oishi, Y. Kashida, K. Mitsumori, Cancer Lett. 245, 321–330 (2007)
S. Simizu, S. Takagi, Y. Tamura, H. Osada, Cancer Res. 65, 7455–7461 (2005)
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Zhang, X., Healy, C. & Nothnick, W.B. Estrogen suppresses expression of the matrix metalloproteinase inhibitor reversion-inducing cysteine-rich protein with Kazal motifs (RECK) within the mouse uterus. Endocrine 42, 97–106 (2012). https://doi.org/10.1007/s12020-012-9614-2
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DOI: https://doi.org/10.1007/s12020-012-9614-2