VEGFR-3 neutralization inhibits ovarian lymphangiogenesis, follicle maturation, and murine pregnancy

American Journal of Pathology

Volumn 183, Issue 5, 2013, Pages 1596-1607

  Rutkowski, Joseph M ^a   Ihm, Jong Eun ^a   Lee, Seung Tae ^a   Kilarski, Witold W ^a   Greenwood, Veronique I ^a   Pasquier, Miriella C ^a   Quazzola, Alexandra ^b   Trono, Didier ^b   Hubbell, Jeffrey A ^a   Swartz, Melody A ^a  

^a Laboratory of Computational Systems Biology Institute of Bioengineering School of Life Sciences   (Switzerland)

^b EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MF4 31C1; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLASTOCYST; CELL DENSITY; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS; FETUS GROWTH; HORMONE SYNTHESIS; LIPID STORAGE; LYMPHANGIOGENESIS; MACROPHAGE; MOUSE; NONHUMAN; OOCYTE; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; OVULATION; PREGNANCY; PREGNANCY DISORDER; PRIORITY JOURNAL; SPONTANEOUS ABORTION;

ABORTION, SPONTANEOUS; ANIMALS; ANTIBODIES, BLOCKING; ANTIBODIES, NEUTRALIZING; APOPTOSIS; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION; FETAL DEVELOPMENT; LIPID METABOLISM; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MACROPHAGES; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; NEUTRALIZATION TESTS; OVARIAN FOLLICLE; PREGNANCY; PREGNANCY OUTCOME; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84886703519     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.07.031     Document Type: Article

References (76)

1. I. Choi, S. Lee, and Y.K. Hong The new era of the lymphatic system: no longer secondary to the blood vascular system Cold Spring Harb Perspect Med 2 2012 a006445
2. H.M. Brown, K.R. Dunning, R.L. Robker, M. Pritchard, and D.L. Russell Requirement for ADAMTS-1 in extracellular matrix remodeling during ovarian folliculogenesis and lymphangiogenesis Dev Biol 300 2006 699 709
3. H.M. Brown, R.L. Robker, and D.L. Russell Development and hormonal regulation of the ovarian lymphatic vasculature Endocrinology 151 2010 5446 5455
4. F. Gaytán, E. Tarradas, C. Bellido, C. Morales, and J.E. Sánchez-Criado Prostaglandin E(1) inhibits abnormal follicle rupture and restores ovulation in indomethacin-treated rats Biol Reprod 67 2002 1140 1147
5. T. Svingen, M. François, D. Wilhelm, and P. Koopman Three-dimensional imaging of Prox1-EGFP transgenic mouse gonads reveals divergent modes of lymphangiogenesis in the testis and ovary PLoS One 7 2012 e52620
6. H.M. Fraser Regulation of the ovarian follicular vasculature Reprod Biol Endocrinol 4 2006 18
7. M.M. Kaczmarek, D. Schams, and A.J. Ziecik Role of vascular endothelial growth factor in ovarian physiology-an overview Reprod Biol 5 2005 111 136
8. S.A. Pauli, H. Tang, J. Wang, P. Bohlen, R. Posser, T. Hartman, M.V. Sauer, J. Kitajewski, and R.C. Zimmermann The vascular endothelial growth factor (VEGF)/VEGF receptor 2 pathway is critical for blood vessel survival in corpora lutea of pregnancy in the rodent Endocrinology 146 2005 1301 1311
9. M. Skobe, L.M. Hamberg, T. Hawighorst, M. Schirner, G.L. Wolf, K. Alitalo, and M. Detmar Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma Am J Pathol 159 2001 893 903
10. N. Ferrara Vascular endothelial growth factor: basic science and clinical progress Endocr Rev 25 2004 581 611
11. M. Shibuya Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis J Biochem Mol Biol 39 2006 469 478
12. K. Iijima, J.Y. Jiang, T. Shimizu, H. Sasada, and E. Sato Acceleration of follicular development by administration of vascular endothelial growth factor in cycling female rats J Reprod Dev 51 2005 161 168
13. R. Gómez, C. Simón, J. Remohí, and A. Pellicer Vascular endothelial growth factor receptor-2 activation induces vascular permeability in hyperstimulated rats, and this effect is prevented by receptor blockade Endocrinology 143 2002 4339 4348
14. T.M. Hazzard, R.M. Rohan, T.A. Molskness, J.W. Fanton, R.J. D'Amato, and R.L. Stouffer Injection of antiangiogenic agents into the macaque preovulatory follicle: disruption of corpus luteum development and function Endocrine 17 2002 199 206
15. R.C. Zimmermann, T. Hartman, P. Bohlen, M.V. Sauer, and J. Kitajewski Preovulatory treatment of mice with anti-VEGF receptor 2 antibody inhibits angiogenesis in corpora lutea Microvasc Res 62 2001 15 25
16. R.C. Zimmermann, T. Hartman, S. Kavic, S.A. Pauli, P. Bohlen, M.V. Sauer, and J. Kitajewski Vascular endothelial growth factor receptor 2-mediated angiogenesis is essential for gonadotropin-dependent follicle development J Clin Invest 112 2003 659 669
17. R.L. Stouffer, F. Xu, and D.M. Duffy Molecular control of ovulation and luteinization in the primate follicle Front Biosci 12 2007 297 307
18. N.C. Douglas, H. Tang, R. Gomez, B. Pytowski, D.J. Hicklin, C.M. Sauer, J. Kitajewski, M.V. Sauer, and R.C. Zimmermann Vascular endothelial growth factor receptor 2 (VEGFR-2) functions to promote uterine decidual angiogenesis during early pregnancy in the mouse Endocrinology 150 2009 3845 3854
19. R.H. Adams, and K. Alitalo Molecular regulation of angiogenesis and lymphangiogenesis Nat Rev Mol Cell Biol 8 2007 464 478
20. C. Norrmén, T. Tammela, T.V. Petrova, and K. Alitalo Biological basis of therapeutic lymphangiogenesis [Erratum appeared in Circulation 2011, 124:e901-e903] Circulation 123 2011 1335 1351
21. J. Goldman, J.M. Rutkowski, J.D. Shields, M.C. Pasquier, Y. Cui, H.G. Schmokel, S. Willey, D.J. Hicklin, B. Pytowski, and M.A. Swartz Cooperative and redundant roles of VEGFR-2 and VEGFR-3 signaling in adult lymphangiogenesis [Erratum appeared in FASEB J 2007, 21:1942] FASEB J 21 2007 1003 1012
22. B. Pytowski, J. Goldman, K. Persaud, Y. Wu, L. Witte, D.J. Hicklin, M. Skobe, K.C. Boardman, and M.A. Swartz Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody J Natl Cancer Inst 97 2005 14 21
23. T. Tammela, B. Enholm, K. Alitalo, and K. Paavonen The biology of vascular endothelial growth factors Cardiovasc Res 65 2005 550 563
24. S. Ichikawa, S. Uchino, and Y. Hirata Lymphatic and blood vasculature of the forming corpus luteum Lymphology 20 1987 73 83
25. Y. Otsuki, S. Magari, and O. Sugimoto Lymphatic capillaries in rabbit ovaries during ovulation: an ultrastructural study Lymphology 19 1986 55 64
26. Y. Otsuki, S. Magari, and O. Sugimoto Fine structure and morphometric analysis of lymphatic capillaries in the developing corpus luteum of the rabbit Lymphology 20 1987 64 72
27. I. Demeestere, A. Delbaere, C. Gervy, M. Van Den Bergh, F. Devreker, and Y. Englert Effect of preantral follicle isolation technique on in-vitro follicular growth, oocyte maturation and embryo development in mice Hum Reprod 17 2002 2152 2159
28. J. Liu, J. Van Der Elst, R. Van Den Broecke, F. Dumortier, and M. Dhont Maturation of mouse primordial follicles by combination of grafting and in vitro culture Biol Reprod 62 2000 1218 1223
29. G.A. Thouas, N.A. Korfiatis, A.J. French, G.M. Jones, and A.O. Trounson Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts Reprod Biomed Online 3 2001 25 29
30. T. Inai, M. Mancuso, H. Hashizume, F. Baffert, A. Haskell, P. Baluk, D.D. Hu-Lowe, D.R. Shalinsky, G. Thurston, G.D. Yancopoulos, and D.M. McDonald Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts Am J Pathol 165 2004 35 52
31. T.A. Partanen, and K. Paavonen Lymphatic versus blood vascular endothelial growth factors and receptors in humans Microsc Res Tech 55 2001 108 121
32. A.N. Witmer, B.C. van Blijswijk, J. Dai, P. Hofman, T.A. Partanen, G.F. Vrensen, and R.O. Schlingemann VEGFR-3 in adult angiogenesis J Pathol 195 2001 490 497
33. P. Laakkonen, M. Waltari, T. Holopainen, T. Takahashi, B. Pytowski, P. Steiner, D. Hicklin, K. Persaud, J.R. Tonra, L. Witte, and K. Alitalo Vascular endothelial growth factor receptor 3 is involved in tumor angiogenesis and growth Cancer Res 67 2007 593 599
34. N. Roberts, B. Kloos, M. Cassella, S. Podgrabinska, K. Persaud, Y. Wu, B. Pytowski, and M. Skobe Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2 Cancer Res 66 2006 2650 2657
35. L.P. Reynolds, A.T. Grazul-Bilska, and D.A. Redmer Angiogenesis in the corpus luteum Endocrine 12 2000 1 9
36. T. Tammela, G. Zarkada, E. Wallgard, A. Murtomäki, S. Suchting, M. Wirzenius, M. Waltari, M. Hellström, T. Schomber, R. Peltonen, C. Freitas, A. Duarte, H. Isoniemi, P. Laakkonen, G. Christofori, S. Ylä-Herttuala, M. Shibuya, B. Pytowski, A. Eichmann, C. Betsholtz, and K. Alitalo Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation Nature 454 2008 656 660
37. J.L. Pate, and P. Landis Keyes Immune cells in the corpus luteum: friends or foes? Reproduction 122 2001 665 676
38. M.P. Hedger, J.X. Qin, D.M. Robertson, and D.M. de Kretser Intragonadal regulation of immune system functions Reprod Fertil Dev 2 1990 263 280
39. T. Shakil, and S.A. Whitehead Inhibitory action of peritoneal macrophages on progesterone secretion from co-cultured rat granulosa cells Biol Reprod 50 1994 1183 1189
40. S.G. Rockson Update on the biology and treatment of lymphedema Curr Treat Options Cardiovasc Med 14 2012 184 192
41. J.M. Rutkowski, C.E. Markhus, C.C. Gyenge, K. Alitalo, H. Wiig, and M.A. Swartz Dermal collagen and lipid deposition correlate with tissue swelling and hydraulic conductivity in murine primary lymphedema Am J Pathol 176 2010 1122 1129
42. J.M. Rutkowski, M. Moya, J. Johannes, J. Goldman, and M.A. Swartz Secondary lymphedema in the mouse tail: Lymphatic hyperplasia, VEGF-C upregulation, and the protective role of MMP-9 Microvasc Res 72 2006 161 171
43. D. Skarzyński, J. Młynarczuk, and J. Kotwica Involvement of high-density lipoprotein in stimulatory effect of hormones supporting function of the bovine corpus luteum Acta Vet Hung 51 2003 111 120
44. J.D. Veldhuis Follicle-stimulating hormone regulates low density lipoprotein metabolism by swine granulosa cells Endocrinology 123 1988 1660 1667
45. A. Rolaki, P. Drakakis, S. Millingos, D. Loutradis, and A. Makrigiannakis Novel trends in follicular development, atresia and corpus luteum regression: a role for apoptosis Reprod Biomed Online 11 2005 93 103
46. M.R. Nourani, Y. Owada, N. Kitanaka, H. Sakagami, H. Hoshi, H. Iwasa, F. Spener, and H. Kondo Occurrence of immunoreactivity for adipocyte-type fatty acid binding protein in degenerating granulosa cells in atretic antral follicles of mouse ovary J Mol Histol 36 2005 491 497
47. P. Chen, C. Li, S. Lang, G. Zhu, A. Reheman, C.M. Spring, J. Freedman, and H. Ni Animal model of fetal and neonatal immune thrombocytopenia: role of neonatal Fc receptor in the pathogenesis and therapy Blood 116 2010 3660 3668
48. T. Krzymowski, and S. Stefanczyk-Krzymowska Local retrograde and destination transfer of physiological regulators as an important regulatory system and its role. Facts and hypothesis J Physiol Pharmacol 63 2012 3 16
49. C. Bellini, M. Rutigliani, F. Boccardo, C. Campisi, T. Bellini, E. Bonioli, and E. Fulcheri Are there lymphatic vessels in the placenta? Lymphology 45 2012 34 36
50. E. Castro, W. Tony Parks, and C. Galambos Neither normal nor diseased placentas contain lymphatic vessels Placenta 32 2011 310 316
51. J.F. Donoghue, C.J. McGavigan, F.L. Lederman, L.M. Cann, L. Fu, E. Dimitriadis, J.E. Girling, and P.A. Rogers Dilated thin-walled blood and lymphatic vessels in human endometrium: a potential role for VEGF-D in progestin-induced break-through bleeding PLoS One 7 2012 e30916
52. M. Volchek, J.E. Girling, G.E. Lash, L. Cann, B. Kumar, S.C. Robson, J.N. Bulmer, and P.A. Rogers Lymphatics in the human endometrium disappear during decidualization Hum Reprod 25 2010 2455 2464
53. C. Dunk, and A. Ahmed Expression of VEGF-C and activation of its receptors VEGFR-2 and VEGFR-3 in trophoblast Histol Histopathol 16 2001 359 375
54. B. Vollmar, M.W. Laschke, R. Rohan, J. Koenig, and M.D. Menger In vivo imaging of physiological angiogenesis from immature to preovulatory ovarian follicles Am J Pathol 159 2001 1661 1670
55. T.J. Acosta, and A. Miyamoto Vascular control of ovarian function: ovulation, corpus luteum formation and regression Anim Reprod Sci 82-83 2004 127 140
56. D.A. Magoffin Ovarian theca cell Int J Biochem Cell Biol 37 2005 1344 1349
57. H.N. Jabbour, R.W. Kelly, H.M. Fraser, and H.O. Critchley Endocrine regulation of menstruation Endocr Rev 27 2006 17 46
58. A. Nitta, K. Shirasuna, S. Haneda, M. Matsui, T. Shimizu, S. Matsuyama, K. Kimura, H. Bollwein, and A. Miyamoto Possible involvement of IFNT in lymphangiogenesis in the corpus luteum during the maternal recognition period in the cow Reproduction 142 2011 879 892
59. F. Xu, and R.L. Stouffer Existence of the lymphatic system in the primate corpus luteum Lymphat Res Biol 7 2009 159 168
60. S. Stefańczyk-Krzymowska, and T. Krzymowski Local adjustment of blood and lymph circulation in the hormonal regulation of reproduction in female pigs-facts, conclusions and suggestions for future research Reprod Biol 2 2002 115 132
61. S. Stefanczyk-Krzymowska, J. Chlopek, W. Grzegorzewski, and M. Radomski Local transfer of prostaglandin E2 into the ovary and its retrograde transfer into the uterus in early pregnant sows Exp Physiol 90 2005 807 814
62. A.E. Drummond, and J.K. Findlay The role of estrogen in folliculogenesis Mol Cell Endocrinol 151 1999 57 64
63. T. Krzymowski, and S. Stefańczyk-Krzymowska The role of the endometrium in endocrine regulation of the animal oestrous cycle Reprod Domest Anim 43 2008 80 91
64. F.C. Battaglia Clinical studies linking fetal velocimetry, blood flow and placental transport in pregnancies complicated by intrauterine growth retardation (IUGR) Trans Am Clin Climatol Assoc 114 2003 305 313
65. M. Gilbert, and A. Leturque Fetal weight and its relationship to placental blood flow and placental weight in experimental intrauterine growth retardation in the rat J Dev Physiol 4 1982 237 246
66. L.H. Khan, C.R. Rosenfeld, X.T. Liu, and R.R. Magness Regulation of the cGMP-cPKG pathway and large-conductance Ca2+-activated K+ channels in uterine arteries during the ovine ovarian cycle Am J Physiol Endocrinol Metab 298 2010 E222 E228
67. D. Nagar, X.T. Liu, and C.R. Rosenfeld Estrogen regulates {beta}1-subunit expression in Ca(2+)-activated K(+) channels in arteries from reproductive tissues Am J Physiol Heart Circ Physiol 289 2005 H1417 H1427
68. L.L. Espey, and H. Lipner Measurements of intrafollicular pressures in the rabbit ovary Am J Physiol 205 1963 1067 1072
69. J.W. Breslin, N. Gaudreault, K.D. Watson, R. Reynoso, S.Y. Yuan, and M.H. Wu Vascular endothelial growth factor-C stimulates the lymphatic pump by a VEGF receptor-3-dependent mechanism Am J Physiol Heart Circ Physiol 293 2007 H709 H718
70. D. Pietrowski, L. Szabo, M. Sator, A. Just, and C. Egarter Ovarian hyperstimulation syndrome is correlated with a reduction of soluble VEGF receptor protein level and a higher amount of VEGF-A Hum Reprod 27 2012 196 199
71. M. Hsieh, D. Boerboom, M. Shimada, Y. Lo, A.F. Parlow, U.F. Luhmann, W. Berger, and J.S. Richards Mice null for Frizzled4 (Fzd4-/-) are infertile and exhibit impaired corpora lutea formation and function Biol Reprod 73 2005 1135 1146
72. M.J. Karkkainen, A. Saaristo, L. Jussila, K.A. Karila, E.C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M.I. Kettunen, S. Yla-Herttuala, D.N. Finegold, R.E. Ferrell, and K. Alitalo A model for gene therapy of human hereditary lymphedema Proc Natl Acad Sci USA 98 2001 12677 12682
73. T. Mäkinen, L. Jussila, T. Veikkola, T. Karpanen, M.I. Kettunen, K.J. Pulkkanen, R. Kauppinen, D.G. Jackson, H. Kubo, S. Nishikawa, S. Ylä-Herttuala, and K. Alitalo Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3 Nat Med 7 2001 199 205
74. M.G. Achen, G.B. Mann, and S.A. Stacker Targeting lymphangiogenesis to prevent tumour metastasis Br J Cancer 94 2006 1355 1360
75. A. Szuba, M. Skobe, M.J. Karkkainen, W.S. Shin, D.P. Beynet, N.B. Rockson, N. Dakhil, S. Spilman, M.L. Goris, H.W. Strauss, T. Quertermous, K. Alitalo, and S.G. Rockson Therapeutic lymphangiogenesis with human recombinant VEGF-C FASEB J 16 2002 1985 1987
76. Y.S. Yoon, T. Murayama, E. Gravereaux, T. Tkebuchava, M. Silver, C. Curry, A. Wecker, R. Kirchmair, C.S. Hu, M. Kearney, A. Ashare, D.G. Jackson, H. Kubo, J.M. Isner, and D.W. Losordo VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema J Clin Invest 111 2003 717 725