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Development, Vol 120, Issue 5 1071-1083, Copyright © 1994 by Company of Biologists

JOURNAL ARTICLES

Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation

SK Das, XN Wang, BC Paria, D Damm, JA Abraham, M Klagsbrun, GK Andrews and SK Dey
Department of Physiology, Ralph L. Smith Research Center, University of Kansas Medical Center, Kansas City 66160-7338.

Heparin-binding EGF-like growth factor (HB-EGF) is a newly discovered member of the EGF family of growth factors. HB-EGF can bind to two loci on cell surfaces, heparan sulphate proteoglycans and EGF-receptor (EGF-R), and either one or both of these interactions could play a role in cell-cell interactions. In the rodent, increased endometrial vascular permeability at the site of blastocyst apposition is considered to be an earliest discernible prerequisite event in the process of implantation and this event coincides with the initial attachment reaction between the blastocyst trophectoderm and uterine luminal epithelium. This investigation demonstrates that the HB-EGF gene is expressed in the mouse uterine luminal epithelium surrounding the blastocyst 6-7 hours before the attachment reaction that occurs at 2200-2300 hours on day 4 of pregnancy. It was further demonstrated that this gene is not expressed in the luminal epithelium at the site of the blastocyst apposition during the progesterone-maintained delayed implantation, but is readily induced in the luminal epithelium surrounding an activated blastocyst after termination of the delay by an estrogen injection. In vitro studies showed that HB-EGF induced blastocyst EGF-R autophosphorylation, and promoted blastocyst growth, zona-hatching and trophoblast outgrowth. These results suggest possible interactions between the uterine HB-EGF and blastocyst EGF-R very early in the process of implantation, earlier than any other embryo-uterine interactions defined to date at the molecular level.
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K. Chobotova, M.-E. Muchmore, J. Carver, H.-J Yoo, S. Manek, W. J. Gullick, D. H. Barlow, and H. J. Mardon
The Mitogenic Potential of Heparin-Binding Epidermal Growth Factor in the Human Endometrium Is Mediated by the Epidermal Growth Factor Receptor and Is Modulated by Tumor Necrosis Factor-{alpha}
J. Clin. Endocrinol. Metab., December 1, 2002; 87(12): 5769 - 5777.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
A. Hicks, R. Potula, Y. J. Sui, F. Villinger, D. Pinson, I. Adany, Z. Li, C. Long, P. Cheney, J. Marcario, et al.
Neuropathogenesis of Lentiviral Infection in Macaques : Roles of CXCR4 and CCR5 Viruses and Interleukin-4 in Enhancing Monocyte Chemoattractant Protein-1 Production in Macrophages
Am. J. Pathol., September 1, 2002; 161(3): 813 - 822.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
X. Wang, H. Wang, H. Matsumoto, S. K. Roy, S. K. Das, and B. C. Paria
Dual source and target of heparin-binding EGF-like growth factor during the onset of implantation in the hamster
Development, September 1, 2002; 129(17): 4125 - 4134.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
H. Ni, T. Sun, N.-Z. Ding, X.-H. Ma, and Z.-M. Yang
Differential Expression of Microsomal Prostaglandin E Synthase at Implantation Sites and in Decidual Cells of Mouse Uterus
Biol Reprod, July 1, 2002; 67(1): 351 - 358.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
P. Yang, A. Kriatchko, and S. K. Roy
Expression of ER-{alpha} and ER-{beta} in the Hamster Ovary: Differential Regulation by Gonadotropins and Ovarian Steroid Hormones
Endocrinology, June 1, 2002; 143(6): 2385 - 2398.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
D. Nadano, K. Sugihara, B. C. Paria, S. Saburi, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, J. Nakayama, and M. N. Fukuda
Significant Differences Between Mouse and Human Trophinins Are Revealed by Their Expression Patterns and Targeted Disruption of Mouse Trophinin Gene
Biol Reprod, February 1, 2002; 66(2): 313 - 321.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Reese, S. K. Das, B. C. Paria, H. Lim, H. Song, H. Matsumoto, K. L. Knudtson, R. N. DuBois, and S. K. Dey
Global Gene Expression Analysis to Identify Molecular Markers of Uterine Receptivity and Embryo Implantation
J. Biol. Chem., November 16, 2001; 276(47): 44137 - 44145.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
E. R. Norwitz, D. J. Schust, and S. J. Fisher
Implantation and the Survival of Early Pregnancy
N. Engl. J. Med., November 8, 2001; 345(19): 1400 - 1408.
[Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
K. B. C. Apparao, M. J. Murray, M. A. Fritz, W. R. Meyer, A. F. Chambers, P. R. Truong, and B. A. Lessey
Osteopontin and Its Receptor {alpha}v{beta}3 Integrin Are Coexpressed in the Human Endometrium during the Menstrual Cycle But Regulated Differentially
J. Clin. Endocrinol. Metab., October 1, 2001; 86(10): 4991 - 5000.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
R. E. Leach, R. Khalifa, D. R. Armant, A. Brudney, S. K. Das, S. K. Dey, and A. T. Fazleabas
Heparin-Binding EGF-Like Growth Factor Modulation by Antiprogestin and CG in the Baboon (Papio anubis)
J. Clin. Endocrinol. Metab., September 1, 2001; 86(9): 4520 - 4528.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. Reese, X. Zhao, W.-G. Ma, N. Brown, T. J. Maziasz, and S. K. Dey
Comparative Analysis of Pharmacologic and/or Genetic Disruption of Cyclooxygenase-1 and Cyclooxygenase-2 Function in Female Reproduction in Mice
Endocrinology, July 1, 2001; 142(7): 3198 - 3206.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
J. Julian, S. K. Das, S. K. Dey, D. Baraniak, V.-T. Ta, and D. D. Carson
Expression of Heparin/Heparan Sulfate Interacting Protein/Ribosomal Protein L29 During the Estrous Cycle and Early Pregnancy in the Mouse
Biol Reprod, April 1, 2001; 64(4): 1165 - 1175.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
B. C. Paria, W.-g. Ma, J. Tan, S. Raja, S. K. Das, S. K. Dey, and B. L. M. Hogan
Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors
PNAS, January 30, 2001; 98(3): 1047 - 1052.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. R. Chen, J.-G. Cheng, T. Shatzer, L. Sewell, L. Hernandez, and C. L. Stewart
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, December 1, 2000; 141(12): 4365 - 4372.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
N. Suzuki, D. Nadano, B. C. Paria, S. Kupriyanov, K. Sugihara, and M. N. Fukuda
Trophinin Expression in the Mouse Uterus Coincides with Implantation and Is Hormonally Regulated But Not Induced by Implanting Blastocysts
Endocrinology, November 1, 2000; 141(11): 4247 - 4254.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
H. Song, H. Lim, S. K. Das, B. C. Paria, and S. K. Dey
Dysregulation of EGF Family of Growth Factors and COX-2 in the Uterus during the Preattachment and Attachment Reactions of the Blastocyst with the Luminal Epithelium Correlates with Implantation Failure in LIF- Deficient Mice
Mol. Endocrinol., August 1, 2000; 14(8): 1147 - 1161.
[Abstract] [Full Text]

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 Am. J. Physiol. Renal Physiol.Home page
B. Robert, X. Zhao, and D. R. Abrahamson
Coexpression of neuropilin-1, Flk1, and VEGF164 in developing and mature mouse kidney glomeruli
Am J Physiol Renal Physiol, August 1, 2000; 279(2): F275 - F282.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
C. Passavant, X. Zhao, S.K. Das, S.K. Dey, and R.A. Mead
Changes in Uterine Expression of Leukemia Inhibitory Factor Receptor Gene During Pregnancy and Its Up-Regulation by Prolactin in the Western Spotted Skunk
Biol Reprod, July 1, 2000; 63(1): 301 - 307.
[Abstract] [Full Text]

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 EndocrinologyHome page
J. Reese, N. Binart, N. Brown, W.-g. Ma, B. C. Paria, S. K. Das, P. A. Kelly, and S. K. Dey
Implantation and Decidualization Defects in Prolactin Receptor (PRLR)-Deficient Mice Are Mediated by Ovarian But Not Uterine PRLR
Endocrinology, May 1, 2000; 141(5): 1872 - 1881.
[Abstract] [Full Text] [PDF]

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 Genes Dev.Home page
C. Brisken, A. Heineman, T. Chavarria, B. Elenbaas, J. Tan, S. K. Dey, J. A. McMahon, A. P. McMahon, and R. A. Weinberg
Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling
Genes & Dev., March 15, 2000; 14(6): 650 - 654.
[Abstract] [Full Text]

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 Mol Hum ReprodHome page
K. R. Park, T. Inoue, M. Ueda, T. Hirano, T. Higuchi, M. Maeda, I. Konishi, H. Fujiwara, and S. Fujii
CD9 is expressed on human endometrial epithelial cells in association with integrins {alpha}6, {alpha}3 and {beta}1
Mol. Hum. Reprod., March 1, 2000; 6(3): 252 - 257.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
R. K. Nuttall and T. G. Kennedy
Epidermal Growth Factor and Basic Fibroblast Growth Factor Increase the Production of Matrix Metalloproteinases during in Vitro Decidualization of Rat Endometrial Stromal Cells
Endocrinology, February 1, 2000; 141(2): 629 - 636.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
X Zhao, W Ma, S. Das, S. Dey, and B. Paria
Blastocyst H(2) receptor is the target for uterine histamine in implantation in the mouse
Development, January 6, 2000; 127(12): 2643 - 2651.
[Abstract] [PDF]

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 DevelopmentHome page
J Wang, L Mayernik, J. Schultz, and D. Armant
Acceleration of trophoblast differentiation by heparin-binding EGF-like growth factor is dependent on the stage-specific activation of calcium influx by ErbB receptors in developing mouse blastocysts
Development, January 1, 2000; 127(1): 33 - 44.
[Abstract] [PDF]

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 EndocrinologyHome page
J. Tan, B. C. Paria, S. K. Dey, and S. K. Das
Differential Uterine Expression of Estrogen and Progesterone Receptors Correlates with Uterine Preparation for Implantation and Decidualization in the Mouse
Endocrinology, November 1, 1999; 140(11): 5310 - 5321.
[Abstract] [Full Text]

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 BloodHome page
F. Vinante, M. Marchi, A. Rigo, P. Scapini, G. Pizzolo, and M. A. Cassatella
Granulocyte-Macrophage Colony-Stimulating Factor Induces Expression of Heparin-Binding Epidermal Growth Factor-Like Growth Factor/Diphtheria Toxin Receptor and Sensitivity to Diphtheria Toxin in Human Neutrophils
Blood, November 1, 1999; 94(9): 3169 - 3177.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
R. E. Leach, R. Khalifa, N. D. Ramirez, S. K. Das, J. Wang, S. K. Dey, R. Romero, and D. R. Armant
Multiple Roles for Heparin-Binding Epidermal Growth Factor-Like Growth Factor Are Suggested by Its Cell-Specific Expression during the Human Endometrial Cycle and Early Placentation
J. Clin. Endocrinol. Metab., September 1, 1999; 84(9): 3355 - 3363.
[Abstract] [Full Text]

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 Mol Hum ReprodHome page
Y. Gui, J. Zhang, L. Yuan, and B. A. Lessey
Regulation of HOXA-10 and its expression in normal and abnormal endometrium
Mol. Hum. Reprod., September 1, 1999; 5(9): 866 - 873.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
F. Raga, E. M. Casañ, J. Kruessel, Y. Wen, F. Bonilla-Musoles, and M. L. Polan
The Role of Gonadotropin-Releasing Hormone in Murine Preimplantation Embryonic Development
Endocrinology, August 1, 1999; 140(8): 3705 - 3712.
[Abstract] [Full Text]

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 Genes Dev.Home page
H. Lim, R. A. Gupta, W.-g. Ma, B. C. Paria, D. E. Moller, J. D. Morrow, R. N. DuBois, J. M. Trzaskos, and S. K. Dey
Cyclo-oxygenase-2-derived prostacyclin mediates embryo implantation in the mouse via PPARdelta
Genes & Dev., June 15, 1999; 13(12): 1561 - 1574.
[Abstract] [Full Text]

Home page
 Mol. Endocrinol.Home page
H. Lim, L. Ma, W.-g. Ma, R. L. Maas, and S. K. Dey
Hoxa-10 Regulates Uterine Stromal Cell Responsiveness to Progesterone during Implantation and Decidualization in the Mouse
Mol. Endocrinol., June 1, 1999; 13(6): 1005 - 1017.
[Abstract] [Full Text]

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 EndocrinologyHome page
J. J. Kim, J. Wang, C. Bambra, S. K. Das, S. K. Dey, and A. T. Fazleabas
Expression of Cyclooxygenase-1 and -2 in the Baboon Endometrium during the Menstrual Cycle and Pregnancy
Endocrinology, June 1, 1999; 140(6): 2672 - 2678.
[Abstract] [Full Text]

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 EndocrinologyHome page
B. C. Paria, J. Tan, D. B. Lubahn, S. K. Dey, and S. K. Das
Uterine Decidual Response Occurs in Estrogen Receptor-{alpha}-Deficient Mice
Endocrinology, June 1, 1999; 140(6): 2704 - 2710.
[Abstract] [Full Text]

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 Mol Hum ReprodHome page
T.L. Purcell, R. Given, K Chwalisz, and R.E. Garfield
Nitric oxide synthase distribution during implantation in the mouse
Mol. Hum. Reprod., May 1, 1999; 5(5): 467 - 475.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
B.C. Paria, X. Zhao, J. Wang, S.K. Das, and S.K. Dey
Fatty-Acid Amide Hydrolase Is Expressed in the Mouse Uterus and Embryo during the Periimplantation Period
Biol Reprod, May 1, 1999; 60(5): 1151 - 1157.
[Abstract] [Full Text]


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