help button home button Endocrine Society JCEM
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS

This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Li, X. F.
Right arrow Articles by Smith, S. K.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Li, X. F.
Right arrow Articles by Smith, S. K.
The Journal of Clinical Endocrinology & Metabolism Vol. 86, No. 4 1823-1834
Copyright © 2001 by The Endocrine Society


Original Studies

Angiogenic Growth Factor Messenger Ribonucleic Acids in Uterine Natural Killer Cells1

Xiao Feng Li, D. Stephen Charnock-Jones, Eko Zhang, Susan Hiby, Shazia Malik, Kate Day, Diane Licence, J. Mark Bowen, Lucy Gardner, Ashley King2, Yung Wai Loke and Stephen K. Smith

Reproductive Molecular Research Group (X.F.L., D.S.C.-J., E.Z., S.M., K.D., D.L., S.K.S.), Research Group in Human Reproductive Immunobiology (S.H., J.M.B., L.G., A.K., Y.W.L.), and Department of Obstetrics and Gynecology, Rosie Hospital (X.F.L., D.S.C.-J., E.Z., S.M., K.D., D.L., S.K.S.), Cambridge, United Kingdom CB2 2SW; and Department of Pathology, University of Cambridge (S.H., J.M.B., L.G., A.K., Y.W.L.), Cambridge, United Kingdom CB2 1QJ

Address all correspondence and requests for reprints to: Prof. S. K. Smith, Department of Obstetrics and Gynecology, The Rosie Hospital, Robinson Way, Cambridge, United Kingdom CB2 2SW. E-mail: sks1000{at}cam.ac.uk

Angiogenesis is essential for endometrial growth and repair, and disruption of this process may lead to common disorders of women, including menorrhagia and endometriosis. In pregnancy, failure of the endometrial spiral arterioles to undergo remodeling leads to preeclampsia. Here we report that in addition to vascular endothelial growth factor A (VEGF-A), human endometrium expresses messenger ribonucleic acids (mRNAs) encoding VEGF-C, placenta growth factor (PlGF), the angiopoietins, angiopoietin 1 (Ang1) and Ang2, and the receptors VEGFR-3 (Flt-4), Tie 1, and Tie 2. Levels of VEGF-C, PlGF, and Tie 2 changed during the menstrual cycle. Intense hybridization for VEGF-C and PlGF mRNAs was found in uterine nature killer cells in secretory phase endometrium and for Ang2 mRNA in the same cells in the late secretory phase. Interleukin-2 (IL-2) and IL-15 up-regulated VEGF-C, but not PlGF or Ang2, mRNA levels in isolated NK cells. Conditioned medium from decidual NK cells did not induce human umbilical vein endothelial cell apoptosis. These results indicate that human endometrium expresses a wide range of angiogenic growth factors and that uterine nature killer cells may play an important role in the abnormal endometrial angiogenesis that underlies a range of disorders affecting women.




This article has been cited by other articles:


Home page
Physiol. Rev.Home page
C. Clapp, S. Thebault, M. C. Jeziorski, and G. Martinez De La Escalera
Peptide Hormone Regulation of Angiogenesis
Physiol Rev, October 1, 2009; 89(4): 1177 - 1215.
[Abstract] [Full Text] [PDF]


Home page
Biol. Reprod.Home page
T. V. Mallidi, L. E. Craig, S. R. Schloemann, and J. K. Riley
Murine Endometrial and Decidual NK1.1+ Natural Killer Cells Display a B220+CD11c+ Cell Surface Phenotype
Biol Reprod, August 1, 2009; 81(2): 310 - 318.
[Abstract] [Full Text] [PDF]


Home page
ReproductionHome page
P. J Williams, J. N Bulmer, R. F Searle, B. A Innes, and S. C Robson
Altered decidual leucocyte populations in the placental bed in pre-eclampsia and foetal growth restriction: a comparison with late normal pregnancy
Reproduction, July 1, 2009; 138(1): 177 - 184.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Physiol. Cell Physiol.Home page
W. J. Pearce
Multifunctional angiogenic factors: add GnRH to the list. Focus on "Gonadotropin-releasing hormone-regulated chemokine expression in human placentation"
Am J Physiol Cell Physiol, July 1, 2009; 297(1): C4 - C5.
[Full Text] [PDF]


Home page
Biol. Reprod.Home page
G. Zimmermann, W. Ackermann, and H. Alexander
Epithelial Human Chorionic Gonadotropin Is Expressed and Produced in Human Secretory Endometrium During the Normal Menstrual Cycle
Biol Reprod, May 1, 2009; 80(5): 1053 - 1065.
[Abstract] [Full Text] [PDF]


Home page
J. Immunol.Home page
S. S. Kalkunte, T. F. Mselle, W. E. Norris, C. R. Wira, C. L. Sentman, and S. Sharma
Vascular Endothelial Growth Factor C Facilitates Immune Tolerance and Endovascular Activity of Human Uterine NK Cells at the Maternal-Fetal Interface
J. Immunol., April 1, 2009; 182(7): 4085 - 4092.
[Abstract] [Full Text] [PDF]


Home page
J. Leukoc. Biol.Home page
K. Kitaya and T. Yasuo
Dermatan sulfate proteoglycan biglycan as a potential selectin L/CD44 ligand involved in selective recruitment of peripheral blood CD16(-) natural killer cells into human endometrium
J. Leukoc. Biol., March 1, 2009; 85(3): 391 - 400.
[Abstract] [Full Text] [PDF]


Home page
Hum ReprodHome page
S. Quenby, H. Nik, B. Innes, G. Lash, M. Turner, J. Drury, and J. Bulmer
Uterine natural killer cells and angiogenesis in recurrent reproductive failure
Hum. Reprod., January 1, 2009; 24(1): 45 - 54.
[Abstract] [Full Text] [PDF]


Home page
Mol Hum ReprodHome page
A. Germeyer, A. M. Sharkey, M. Prasadajudio, R. Sherwin, A. Moffett, K. Bieback, S. Clausmeyer, L. Masters, R. M. Popovici, A. P. Hess, et al.
Paracrine effects of uterine leucocytes on gene expression of human uterine stromal fibroblasts
Mol. Hum. Reprod., January 1, 2009; 15(1): 39 - 48.
[Abstract] [Full Text] [PDF]


Home page
EndocrinologyHome page
G. W. Aberdeen, S. J. Wiegand, T. W. Bonagura Jr., G. J. Pepe, and E. D. Albrecht
Vascular Endothelial Growth Factor Mediates the Estrogen-Induced Breakdown of Tight Junctions between and Increase in Proliferation of Microvessel Endothelial Cells in the Baboon Endometrium
Endocrinology, December 1, 2008; 149(12): 6076 - 6083.
[Abstract] [Full Text] [PDF]


Home page
Reproductive SciencesHome page
M. Plaisier, E. Streefland, P. Koolwijk, V.W.M. van Hinsbergh, F.M. Helmerhorst, and J.J.H.M. Erwich
Angiogenic Growth Factors and Their Receptors in First-Trimester Human Decidua of Pregnancies Further Complicated By Preeclampsia or Fetal Growth Restriction
Reproductive Sciences, September 1, 2008; 15(7): 720 - 726.
[Abstract] [PDF]


Home page
Int ImmunolHome page
H. Amsalem, A. Gaiger, S. Mizrahi, S. Yagel, and J. Rachmilewitz
Characterization of a lymphocyte subset displaying a unique regulatory activity in human decidua
Int. Immunol., September 1, 2008; 20(9): 1147 - 1154.
[Abstract] [Full Text] [PDF]


Home page
Biol. Reprod.Home page
J. Zhang, H. Dong, B. Wang, S. Zhu, and B. A. Croy
Dynamic Changes Occur in Patterns of Endometrial EFNB2/EPHB4 Expression During the Period of Spiral Arterial Modification in Mice
Biol Reprod, September 1, 2008; 79(3): 450 - 458.
[Abstract] [Full Text] [PDF]


Home page
J. Immunol.Home page
A. M. Sharkey, L. Gardner, S. Hiby, L. Farrell, R. Apps, L. Masters, J. Goodridge, L. Lathbury, C. A. Stewart, S. Verma, et al.
Killer Ig-Like Receptor Expression in Uterine NK Cells Is Biased toward Recognition of HLA-C and Alters with Gestational Age
J. Immunol., July 1, 2008; 181(1): 39 - 46.
[Abstract] [Full Text] [PDF]


Home page
Mol Hum ReprodHome page
C. Y. Tan, J. F.V. Ho, Y. S. Chong, A. Loganath, Y. H. Chan, J. Ravichandran, C. G. Lee, and S. S. Chong
Paternal contribution of HLA-G*0106 significantly increases risk for pre-eclampsia in multigravid pregnancies
Mol. Hum. Reprod., May 1, 2008; 14(5): 317 - 324.
[Abstract] [Full Text] [PDF]


Home page
Mol Hum ReprodHome page
M. Plaisier, P. Koolwijk, F. Willems, F. M. Helmerhorst, and V. W.M. van Hinsbergh
Pericellular-acting proteases in human first trimester decidua
Mol. Hum. Reprod., January 1, 2008; 14(1): 41 - 51.
[Abstract] [Full Text] [PDF]


Home page
DiabetesHome page
S. D. Burke, H. Dong, A. D. Hazan, and B. A. Croy
Aberrant Endometrial Features of Pregnancy in Diabetic NOD Mice
Diabetes, December 1, 2007; 56(12): 2919 - 2926.
[Abstract] [Full Text] [PDF]


Home page
EndocrinologyHome page
J. E. Girling, F. L. Lederman, L. M. Walter, and P. A. W. Rogers
Progesterone, But Not Estrogen, Stimulates Vessel Maturation in the Mouse Endometrium
Endocrinology, November 1, 2007; 148(11): 5433 - 5441.
[Abstract] [Full Text] [PDF]


Home page
J. Leukoc. Biol.Home page
C. Tayade, Y. Fang, D. Hilchie, and B. A. Croy
Lymphocyte contributions to altered endometrial angiogenesis during early and midgestation fetal loss
J. Leukoc. Biol., October 1, 2007; 82(4): 877 - 886.
[Abstract] [Full Text] [PDF]


Home page
Hum ReprodHome page
J. Gilabert-Estelles, L.A. Ramon, F. Espana, J. Gilabert, V. Vila, E. Reganon, R. Castello, M. Chirivella, and A. Estelles
Expression of angiogenic factors in endometriosis: relationship to fibrinolytic and metalloproteinase systems
Hum. Reprod., August 1, 2007; 22(8): 2120 - 2127.
[Abstract] [Full Text] [PDF]


Home page
J. Immunol.Home page
C. Tayade, D. Hilchie, H. He, Y. Fang, L. Moons, P. Carmeliet, R. A. Foster, and B. A. Croy
Genetic Deletion of Placenta Growth Factor in Mice Alters Uterine NK Cells
J. Immunol., April 1, 2007; 178(7): 4267 - 4275.
[Abstract] [Full Text] [PDF]


Home page
Mol Hum ReprodHome page
A. van der Meer, H.G.M. Lukassen, B. van Cranenbroek, E.H. Weiss, D.D.M. Braat, M.J. van Lierop, and I. Joosten
Soluble HLA-G promotes Th1-type cytokine production by cytokine-activated uterine and peripheral natural killer cells
Mol. Hum. Reprod., February 1, 2007; 13(2): 123 - 133.
[Abstract] [Full Text] [PDF]


Home page
FASEB J.Home page
G. E. Lash, H. A. Otun, B. A. Innes, M. Kirkley, L. De Oliveira, R. F. Searle, S. C. Robson, and J. N. Bulmer
Interferon-{gamma} inhibits extravillous trophoblast cell invasion by a mechanism that involves both changes in apoptosis and protease levels
FASEB J, December 1, 2006; 20(14): 2512 - 2518.
[Abstract] [Full Text] [PDF]


Home page
J. Leukoc. Biol.Home page
G. E. Lash, B. Schiessl, M. Kirkley, B. A. Innes, A. Cooper, R. F. Searle, S. C. Robson, and J. N. Bulmer
Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy
J. Leukoc. Biol., September 1, 2006; 80(3): 572 - 580.
[Abstract] [Full Text] [PDF]


Home page
Endocr. Rev.Home page
H. N. Jabbour, R. W. Kelly, H. M. Fraser, and H. O. D. Critchley
Endocrine Regulation of Menstruation
Endocr. Rev., February 1, 2006; 27(1): 17 - 46.
[Abstract] [Full Text] [PDF]


Home page
ReproductionHome page
F Arcuri, M Cintorino, A Carducci, S Papa, M G Riparbelli, S Mangioni, A M Di Blasio, P Tosi, and P Vigano
Human decidual natural killer cells as a source and target of macrophage migration inhibitory factor
Reproduction, January 1, 2006; 131(1): 175 - 182.
[Abstract] [Full Text] [PDF]


Home page
J. Immunol.Home page
C. Tayade, G. P. Black, Y. Fang, and B. A. Croy
Differential Gene Expression in Endometrium, Endometrial Lymphocytes, and Trophoblasts during Successful and Abortive Embryo Implantation
J. Immunol., January 1, 2006; 176(1): 148 - 156.
[Abstract] [Full Text] [PDF]


Home page
J. Leukoc. Biol.Home page
C. Tayade, Y. Fang, G. P. Black, P. VA Jr, A. Erlebacher, and B. A. Croy
Differential transcription of Eomes and T-bet during maturation of mouse uterine natural killer cells
J. Leukoc. Biol., December 1, 2005; 78(6): 1347 - 1355.
[Abstract] [Full Text] [PDF]


Home page
Mol Hum ReprodHome page
N. R. Nayak, C. J. Kuo, T. A. Desai, S. J. Wiegand, B. L. Lasley, L. C. Giudice, and R. M. Brenner
Expression, localization and hormonal control of angiopoietin-1 in the rhesus macaque endometrium: potential role in spiral artery growth
Mol. Hum. Reprod., November 1, 2005; 11(11): 791 - 799.
[Abstract] [Full Text] [PDF]


Home page
FASEB J.Home page
J. S. Hunt, M. G. Petroff, R. H. McIntire, and C. Ober
HLA-G and immune tolerance in pregnancy
FASEB J, May 1, 2005; 19(7): 681 - 693.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
K. Kitaya, T. Yamaguchi, and H. Honjo
Central Role of Interleukin-15 in Postovulatory Recruitment of Peripheral Blood CD16(-) Natural Killer Cells into Human Endometrium
J. Clin. Endocrinol. Metab., May 1, 2005; 90(5): 2932 - 2940.
[Abstract] [Full Text] [PDF]


Home page
Mol Hum ReprodHome page
A. P. Ponnampalam, G. C. Weston, A. C. Trajstman, B. Susil, and P. A.W. Rogers
Molecular classification of human endometrial cycle stages by transcriptional profiling
Mol. Hum. Reprod., December 1, 2004; 10(12): 879 - 893.
[Abstract] [Full Text] [PDF]


Home page
Hum ReprodHome page
C.S. Witt, J. Goodridge, M.G. Gerbase-DeLima, S. Daher, and F.T. Christiansen
Maternal KIR repertoire is not associated with recurrent spontaneous abortion
Hum. Reprod., November 1, 2004; 19(11): 2653 - 2657.
[Abstract] [Full Text] [PDF]


Home page
Hum ReprodHome page
C. Print, R. Valtola, A. Evans, K. Lessan, S. Malik, and S. Smith
Soluble factors from human endometrium promote angiogenesis and regulate the endothelial cell transcriptome
Hum. Reprod., October 1, 2004; 19(10): 2356 - 2366.
[Abstract] [Full Text] [PDF]


Home page
Mol Hum ReprodHome page
H.G.M. Lukassen, I. Joosten, B. van Cranenbroek, M.J.C. van Lierop, J. Bulten, D.D.M. Braat, and A. van der Meer
Hormonal stimulation for IVF treatment positively affects the CD56bright/CD56dim NK cell ratio of the endometrium during the window of implantation
Mol. Hum. Reprod., July 1, 2004; 10(7): 513 - 520.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Pathol.Home page
G. Krikun, D. Sakkas, F. Schatz, L. Buchwalder, D. Hylton, C. Tang, and C. J. Lockwood
Endometrial Angiopoietin Expression and Modulation by Thrombin and Steroid Hormones: A Mechanism for Abnormal Angiogenesis Following Long-Term Progestin-Only Contraception
Am. J. Pathol., June 1, 2004; 164(6): 2101 - 2107.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
S. Battersby, H. O. D. Critchley, K. Morgan, R. P. Millar, and H. N. Jabbour
Expression and Regulation of the Prokineticins (Endocrine Gland-Derived Vascular Endothelial Growth Factor and Bv8) and Their Receptors in the Human Endometrium across the Menstrual Cycle
J. Clin. Endocrinol. Metab., May 1, 2004; 89(5): 2463 - 2469.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
K. Kitaya, T. Nakayama, N. Daikoku, S. Fushiki, and H. Honjo
Spatial and Temporal Expression of Ligands for CXCR3 and CXCR4 in Human Endometrium
J. Clin. Endocrinol. Metab., May 1, 2004; 89(5): 2470 - 2476.
[Abstract] [Full Text] [PDF]


Home page
ReproductionHome page
B Heryanto, J E Girling, and P A W Rogers
Intravascular neutrophils partially mediate the endometrial endothelial cell proliferative response to oestrogen in ovariectomised mice
Reproduction, May 1, 2004; 127(5): 613 - 620.
[Abstract] [Full Text] [PDF]


Home page
Hum ReprodHome page
N. Suzumori, M. Sugiura-Ogasawara, K. Katano, and K. Suzumori
Women with endometriosis have increased levels of placental growth factor in the peritoneal fluid compared with women with cystadenomas
Hum. Reprod., December 1, 2003; 18(12): 2595 - 2598.
[Abstract] [Full Text] [PDF]


Home page
Mol Hum ReprodHome page
J. Hirchenhain, I. Huse, A. Hess, P. Bielfeld, F. De Bruyne, and J. S. Krussel
Differential expression of angiopoietins 1 and 2 and their receptor Tie-2 in human endometrium
Mol. Hum. Reprod., November 1, 2003; 9(11): 663 - 669.
[Abstract] [Full Text] [PDF]


Home page
J. Immunol.Home page
S. Chantakru, W.-C. Wang, M. van den Heuvel, S. Bashar, A. Simpson, Q. Chen, B. A. Croy, and S. S. Evans
Coordinate Regulation of Lymphocyte-Endothelial Interactions by Pregnancy-Associated Hormones
J. Immunol., October 15, 2003; 171(8): 4011 - 4019.
[Abstract] [Full Text] [PDF]


Home page
J. Immunol.Home page
A. A. Ashkar, G. P. Black, Q. Wei, H. He, L. Liang, J. R. Head, and B. A. Croy
Assessment of Requirements for IL-15 and IFN Regulatory Factors in Uterine NK Cell Differentiation and Function During Pregnancy
J. Immunol., September 15, 2003; 171(6): 2937 - 2944.
[Abstract] [Full Text] [PDF]


Home page
Reproductive SciencesHome page
D. S. Torry, D. Mukherjea, J. Arroyo, and R. J. Torry
Expression and Function of Placenta Growth Factor: Implications for Abnormal Placentation
Reproductive Sciences, May 1, 2003; 10(4): 178 - 188.
[Abstract] [PDF]


Home page
Hum ReprodHome page
A. Arici, I. Matalliotakis, A. Goumenou, G. Koumantakis, S. Vassiliadis, B. Selam, and N. G. Mahutte
Increased levels of interleukin-15 in the peritoneal fluid of women with endometriosis: inverse correlation with stage and depth of invasion
Hum. Reprod., February 1, 2003; 18(2): 429 - 432.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
T. A. Henderson, P. T. K. Saunders, A. Moffett-King, N. P. Groome, and H. O. D. Critchley
Steroid Receptor Expression in Uterine Natural Killer Cells
J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 440 - 449.
[Abstract] [Full Text] [PDF]


Home page
EndocrinologyHome page
L. C. Kao, S. Tulac, S. Lobo, B. Imani, J. P. Yang, A. Germeyer, K. Osteen, R. N. Taylor, B. A. Lessey, and L. C. Giudice
Global Gene Profiling in Human Endometrium during the Window of Implantation
Endocrinology, June 1, 2002; 143(6): 2119 - 2138.
[Abstract] [Full Text] [PDF]


Home page
J. Clin. Endocrinol. Metab.Home page
O. Gubbay, H. O. D. Critchley, J. M. Bowen, A. King, and H. N. Jabbour
Prolactin Induces ERK Phosphorylation in Epithelial and CD56+ Natural Killer Cells of the Human Endometrium
J. Clin. Endocrinol. Metab., May 1, 2002; 87(5): 2329 - 2335.
[Abstract] [Full Text] [PDF]


Home page
Hum ReprodHome page
L. S. Gambino, N. G. Wreford, J. F. Bertram, P. Dockery, F. Lederman, and P. A.W. Rogers
Angiogenesis occurs by vessel elongation in proliferative phase human endometrium
Hum. Reprod., May 1, 2002; 17(5): 1199 - 1206.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Pathol.Home page
P. Hewett, S. Nijjar, M. Shams, S. Morgan, J. Gupta, and A. Ahmed
Down-Regulation of Angiopoietin-1 Expression in Menorrhagia
Am. J. Pathol., March 1, 2002; 160(3): 773 - 780.
[Abstract] [Full Text] [PDF]




HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals
Copyright © 2001 by The Endocrine Society