Possible involvement of IFNT in lymphangiogenesis in the corpus luteum during the maternal recognition period in the cow

Reproduction

Volumn 142, Issue 6, 2011, Pages 879-892

  Nitta, Akane ^a   Shirasuna, Koumei ^a   Haneda, Shingo ^a   Matsui, Motozumi ^a   Shimizu, Takashi ^a   Matsuyama, Shuichi ^b   Kimura, Koji ^b   Bollwein, Heinrich ^c   Miyamoto, Akio ^a  

^a OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF LIVESTOCK AND GRASSLAND SCIENCE   (Japan)

^c UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID; LYMPHATIC ENDOTHELIAL HYALURONAN RECEPTOR 1; MESSENGER RNA; PODOPLANIN; PROTEIN P16; PROTEIN P40; TAU INTERFERON; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 3;

ANIMAL EXPERIMENT; ARTICLE; CELL STIMULATION; CONCEPTION; CONTROLLED STUDY; CORPUS LUTEUM; ESTRUS CYCLE; FEMALE; FIRST TRIMESTER PREGNANCY; IMMUNE FUNCTION TEST; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LYMPH VESSEL; LYMPHANGIOGENESIS; MATERNAL RECOGNITION PERIOD; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; WESTERN BLOTTING;

ANIMALS; CATTLE; CELL PROLIFERATION; CORPUS LUTEUM; ENDOTHELIAL CELLS; ESTROUS CYCLE; FEMALE; INTERFERON TYPE I; INTERFERON-ALPHA; LYMPHANGIOGENESIS; PREGNANCY; PREGNANCY PROTEINS; PREGNANCY, ANIMAL; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 82355181589     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-11-0157     Document Type: Article

References (86)

1. Andersen DH 1926 Lymphatic and blood vessels of the ovary of the sow. Contributions to Embryology 88 107-124.
2. Asselin E, Johnson GA, Spencer TE & Bazer FW 2001 Monocyte chemotactic protein-1 and -2 messenger ribonucleic acids in the ovine uterus: regulation by pregnancy, progesterone, and interferon-tau. Biology of Reproduction 64 992-1000. (doi:10.1095/biolreprod64.3.992)
3. Baldwin ME, Halford MM, Roufail S, Williams RA, Hibbs ML, Grail D, Kubo H, Stacker SA & Achen MG 2005 Vascular endothelial growth factor D is dispensable for development of the lymphatic system. Molecular and Cellular Biology 25 2441-2449. (doi:10.1128/MCB.25.6. 2441-2449.2005)
4. Baluk P, Tammela T, Ator E, Lyubynska N, Achen MG, Hicklin DJ, Jeltsch M, Petrova TV, Pytowski B, Stacker SA et al. 2005 Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. Journal of Clinical Investigation 115 247-257. (doi:10.1172/JCI22037)
5. Banerji S, Ni J, Wang SX, Clasper S, Su J, Tammi R, Jones M & Jackson DG 1999 LYVE-1, a new homologue of the CD44 glycoprotein, is a lymphspecific receptor for hyaluronan. Journal of Cell Biology 144 789-801. (doi:10.1083/jcb.144.4.789)
6. Beindorff N, Nagai K, Shirasuna K, Herzog K, Hoeffmann K, Sasaki M, Bollwein H & Miyamoto A 2010 Vascular changes in the corpus luteum during early pregnancy in the cow. Journal of Reproduction and Development 56 263-270. (doi:10.1262/jrd.09-150K)
7. Berisha B, Schams D, Kosmann M, Amselgruber W & Einspanier R 2000 Expression and tissue concentration of vascular endothelial growth factor, its receptors, and localization in the bovine corpus luteum during estrous cycle and pregnancy. Biology of Reproduction 63 1106-1114. (doi:10.1095/biolreprod63.4. 1106)
8. Bott RC, Ashley RL, Henkes LE, Antoniazzi AQ, Bruemmer JE, Niswender GD, Bazer FW, Spencer TE, Smirnova NP, Anthony RV et al. 2010 Uterine vein infusion of interferon tau (IFNT) extends luteal life span in ewes. Biology of Reproduction 82 725-735. (doi:10.1095/ biolreprod.109.079467)
9. Brannstrom M, Giesecke L, Moore IC, van den Heuvel CJ & Robertson SA 1994 Leukocyte subpopulations in the rat corpus luteum during pregnancy and pseudopregnancy. Biology of Reproduction 50 1161-1167. (doi:10.1095/ biolreprod50.5.1161)
10. Breiteneder-Geleff S, Soleiman A, Kowalski H, Horvat R, Amann G, Kriehuber E, Diem K, Weninger W, Tschachler E, Alitalo K et al. 1999 Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. American Journal of Pathology 154 385-394. (doi:10. 1016/S0002-9440(10)65285-6)
11. Chen Y, Green JA, Antoniou E, Ealy AD, Mathialagan N, Walker AM, Avalle MP, Rosenfeld CS, Hearne LB & Roberts RM 2006 Effect of interferon-tau administration on endometrium of nonpregnant ewes: a comparison with pregnant ewes. Endocrinology 147 2127-2137. (doi:10.1210/en.2005-1310)
12. Choi Y, Johnson GA, Burghardt RC, Berghman LR, Joyce MM, Taylor KM, Stewart MD, Bazer FW & Spencer TE 2001 Interferon regulatory factortwo restricts expression of interferon-stimulated genes to the endometrial stroma and glandular epithelium of the ovine uterus. Biology of Reproduction 65 1038-1049. (doi:10.1095/biolreprod65.4.1038)
13. Chomczynski P & Sacchi N 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162 156-159. (doi:10.1016/0003-2697(87) 90021-2)
14. Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Radziejewski C, D'Amore PA, Dana MR, Wiegand SJ & Streilein JW 2004 VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. Journal of Clinical Investigation 113 1040-1050. (doi:10.1172/JCI20465)
15. Czeizel E & Palkovich I 1962 Study of the interual lymphatic vessels of the ovary by experimental lymph stasis. Anatomischer Anzeiger 111 413-425.
16. Farin CE, Imakawa K, Hansen TR, McDonnell JJ, Murphy CN, Farin PW & Roberts RM 1990 Expression of trophoblastic interferon genes in sheep and cattle. Biology of Reproduction 43 210-218. (doi:10.1095/ biolreprod43.2.210)
17. Fleming JG, Spencer TE, Safe SH & Bazer FW 2006 Estrogen regulates transcription of the ovine oxytocin receptor gene through GC-rich SP1 promoter elements. Endocrinology 147 899-911. (doi:10.1210/en.2005-1120)
18. Fraser HM, Dickson SE, Lunn SF, Wulff C, Morris KD, Carroll VA & Bicknell R 2000 Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology 141 995-1000. (doi:10.1210/en.141.3.995)
19. Gifford CA, Racicot K, Clark DS, Austin KJ, Hansen TR, Lucy MC, Davies CJ & Ott TL 2007 Regulation of interferon-stimulated genes in peripheral blood leukocytes in pregnant and bred, nonpregnant dairy cows. Journal of Dairy Science 90 274-280. (doi:10.3168/jds.S0022-0302 (07)72628-0)
20. Girsh E, Wang W, Mamluk R, Arditi F, Friedman A, Milvae RA & Meidan R 1996 Regulation of endothelin-1 expression in the bovine corpus luteum: elevation by prostaglandin F2 alpha. Endocrinology 137 5191-5196. (doi:10.1210/en.137.12.5191)
21. Green MP, Spate LD, Bixby JA, Ealy AD & Roberts RM 2005 A comparison of the anti-luteolytic activities of recombinant ovine interferon-alpha and -tau in sheep. Biology of Reproduction 73 1087-1093. (doi:10.1095/ biolreprod.105.043406)
22. Han H, Austin KJ, Rempel LA & Hansen TR 2006 Low blood ISG15 mRNA and progesterone levels are predictive of non-pregnant dairy cows. Journal of Endocrinology 191 505-512. (doi:10.1677/joe.1.07015)
23. Hansen TR, Austin KJ & Johnson GA 1997 Transient ubiquitin cross-reactive protein gene expression in the bovine endometrium. Endocrinology 138 5079-5082. (doi:10.1210/en.138.11.5079)
24. Hansen TR, Austin KJ, Perry DJ, Pru JK, Teixeira MG & Johnson GA 1999 Mechanism of action of interferon-tau in the uterus during early pregnancy. Journal of Reproduction and Fertility. Supplement 54 329-339.
25. Hansen TR, Henkes LE, Ashley RL, Bott RC, Antoniazzi AQ & Han H 2010 Endocrine actions of interferon-tau in ruminants. Society of Reproduction and Fertility Supplement 67 325-340. (doi:10.5661/RDR-VII-325)
26. Imakawa K, Anthony RV, Kazemi M, Marotti KR, Polites HG & Roberts RM 1987 Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm. Nature 330 377-379. (doi:10.1038/ 330377a0)
27. Iwata C, Kano MR, Komuro A, Oka M, Kiyono K, Johansson E, Morishita Y, Yashiro M, Hirakawa K, Kaminishi M et al. 2007 Inhibition of cyclooxygenase-2 suppresses lymph node metastasis via reduction of lymphangiogenesis. Cancer Research 67 10181-10189. (doi:10.1158/ 0008-5472.CAN-07-2366)
28. Jiemtaweeboon S, Shirasuna K, Nitta A, Kobayashi A, Schuberth HJ, Shimizu T & Miyamoto A 2011 Evidence that polymorphonuclear neutrophils infiltrate into the developing corpus luteum and promote angiogenesis with interleukin-8 in the cow. Reproductive Biology and Endocrinology 9 79. (doi:10.1186/1477-7827-9- 79)
29. Johnson GA, Austin KJ, Van Kirk EA & Hansen TR 1998 Pregnancy and interferon-tau induce conjugation of bovine ubiquitin cross-reactive protein to cytosolic uterine proteins. Biology of Reproduction 58 898-904. (doi:10.1095/biolreprod58.4.898)
30. Johnson GA, Spencer TE, Hansen TR, Austin KJ, Burghardt RC & Bazer FW 1999 Expression of the interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus. Biology of Reproduction 61 312-318. (doi:10.1095/biolreprod61.1.312)
31. Joukov V, Sorsa T, Kumar V, Jeltsch M, Claesson-Welsh L, Cao Y, Saksela O, Kalkkinen N & Alitalo K 1997 Proteolytic processing regulates receptor specificity and activity of VEGFC. EMBO Journal 16 3898-3911. (doi:10. 1093/emboj/16.13.3898)
32. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H et al. 2004 Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nature Immunology 5 74-80. (doi:10. 1038/ni1013)
33. Klipper E, Gilboa T, Levy N, Kisliouk T, Spanel-Borowski K & Meidan R 2004 Characterization of endothelin-1 and nitric oxide generating systems in corpus luteum-derived endothelial cells. Reproduction 128 463-473. (doi:10.1530/rep.1.00271)
34. Kubo H, Cao R, Brakenhielm E, Makinen T, Cao Y & Alitalo K 2002 Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. PNAS 99 8868-8873. (doi:10.1073/pnas.062040199)
35. Leak LV, Yu ZX, Jones M & Ferrans VJ 1999 Characterization of a transformed ovine lymphatic endothelial cell line. Microcirculation 6 63-73. (doi:10.1111/j.1549-8719.1999.tb00088.x)
36. Lei ZM, Chegini N & Rao CV 1991 Quantitative cell composition of human and bovine corpora lutea from various reproductive states. Biology of Reproduction 44 1148-1156. (doi:10.1095/biolreprod44.6. 1148)
37. Li J & Roberts RM 1994 Interferon-tau and interferon-alpha interact with the same receptors in bovine endometrium. Use of a readily iodinatable form of recombinant interferon-tau for binding studies. Journal of Biological Chemistry 269 13544-13550.
38. Maliba R, Brkovic A, Neagoe PE, Villeneuve LR & Sirois MG 2008 Angiopoietin-mediated endothelial P-selectin translocation: cell signaling mechanisms. Journal of Leukocyte Biology 83 352-360. (doi:10. 1189/jlb.0107056)
39. Meyer MD, Hansen PJ, Thatcher WW, Drost M, Badinga L, Roberts RM, Li J, Ott TL & Bazer FW 1995 Extension of corpus luteum lifespan and reduction of uterine secretion of prostaglandin F2 alpha of cows in response to recombinant interferon-tau. Journal of Dairy Science 78 1921-1931. (doi:10.3168/jds.S0022- 0302(95)76817-5)
40. Millauer B, Wizigmann-Voos S, Schnurch H, Martinez R, Moller NP, Risau W & Ullrich A 1993 High affinity VEGF binding and developmental expression suggest Flk-1 as amajor regulator of vasculogenesis and angiogenesis. Cell 72 835-846. (doi:10.1016/0092-8674(93) 90573-9)
41. Miyamoto A & Schams D 1991 Oxytocin stimulates progesterone release from microdialyzed bovine corpus luteum in vitro. Biology of Reproduction 44 1163-1170. (doi:10.1095/biolreprod44.6.1163)
42. Miyamoto A, Shirasuna K & Sasahara K 2009 Local regulation of corpus luteum development and regression in the cow: impact of angiogenic and vasoactive factors. Domestic Animal Endocrinology 37 159-169. (doi:10.1016/j.domaniend.2009.04.005)
43. Miyamoto A, Shirasuna K, Shimizu S, Bollwein H & Schams D 2010 Regulation of corpus luteum development and maintenance: specific roles of angiogenesis and action of prostaglandin F2 alpha. Society of Reproduction and Fertility Supplement 67 289-304.
44. Morris B & Sass M 1966 The formation of lymph in the ovary. Proceedings of the Royal Society of London. Series B, Biological Sciences 164 577-591. (doi:10.1098/rspb.1966.0049)
45. Murata K 1976 Fine distribution of lympha vessels within the ovaries. Journal of Tokyo Medical College 34 425-437.
46. Nagaoka K, Sakai A, Nojima H, Suda Y, Yokomizo Y, Imakawa K, Sakai S & Christenson RK 2003 A chemokine, interferon (IFN)-gamma-inducible protein 10 kDa, is stimulated by IFN-tau and recruits immune cells in the ovine endometrium. Biology of Reproduction 68 1413-1421. (doi:10. 1095/biolreprod.102. 008912)
47. Nguyen VP, Chen SH, Trinh J, Kim H, Coomber BL & Dumont DJ 2007 Differential response of lymphatic, venous and arterial endothelial cells to angiopoietin-1 and angiopoietin-2. BMC Cell Biology 8 10. (doi:10. 1186/1471-2121-8-10)
48. Oliveira JF, Henkes LE, Ashley RL, Purcell SH, Smirnova NP, Veeramachaneni DN, Anthony RV & Hansen TR 2008 Expression of interferon (IFN)-stimulated genes in extrauterine tissues during early pregnancy in sheep is the consequence of endocrine IFN-tau release from the uterine vein. Endocrinology 149 1252-1259. (doi:10.1210/en.2007-0863)
49. O'Shea JD, Rodgers RJ & D'Occhio MJ 1989 Cellular composition of the cyclic corpus luteum of the cow. Journal of Reproduction and Fertility 85 483-487. (doi:10.1530/jrf.0.0850483)
50. Otsuki Y, Magari S & Sugimoto O 1987 Fine structure and morphometric analysis of lymphatic capillaries in the developing corpus luteum of the rabbit. Lymphology 20 64-72. (Pubitemid 17103732)
51. Penny LA 2000 Monocyte chemoattractant protein 1 in luteolysis. Reviews of Reproduction 5 63-66. (doi:10.1530/ror.0.0050063)
52. Podgrabinska S, Braun P, Velasco P, Kloos B, Pepper MS & Skobe M 2002 Molecular characterization of lymphatic endothelial cells. PNAS 99 16069-16074. (doi:10.1073/pnas.242401399)
53. Prevo R, Banerji S, Ferguson DJ, Clasper S & Jackson DG 2001 Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium. Journal of Biological Chemistry 276 19420-19430. (doi:10. 1074/jbc.M011004200)
54. Reibiger I & Spanel-Borowski K 2000 Difference in localization of eosinophils and mast cells in the bovine ovary. Journal of Reproduction and Fertility 118 243-249. (doi:10.1530/reprod/118.2.243)
55. Roberts RM, Cross JC & Leaman DW 1992 Interferons as hormones of pregnancy. Endocrine Reviews 13 432-452. (doi:10.1210/edrv-13-3-432)
56. Roberts RM, Xie S & Mathialagan N 1996 Maternal recognition of pregnancy. Biology of Reproduction 54 294-302. (doi:10.1095/biolreprod54.2.294)
57. Robinson RS, Woad KJ, Hammond AJ, Laird M, Hunter MG & Mann GE 2009 Angiogenesis and vascular function in the ovary. Reproduction 138 869-881. (doi:10.1530/REP-09-0283)
58. Schams D & Berisha B 2004 Regulation of corpus luteum function in cattle - an overview. Reproduction in Domestic Animals 39 241-251. (doi:10. 1111/j.1439-0531.2004.00509.x)
59. Schams D, Stefanie S, Heinrich HDM & Bajram B 2009 Expression of lymphangiogenic factors in bovine corpus luteum during estrous cycle, pregnancy, and induced luteolysis. Biology of Reproduction 81 (Meeting Abstracts) 514.
60. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML & Schuh AC 1995 Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376 62-66. (doi:10.1038/376062a0)
61. Shirasuna K, Watanabe S, Asahi T, Wijayagunawardane MP, Sasahara K, Jiang C, Matsui M, Sasaki M, Shimizu T, Davis JS et al. 2008 Prostaglandin F2alpha increases endothelial nitric oxide synthase in the periphery of the bovine corpus luteum: the possible regulation of blood flow at an early stage of luteolysis. Reproduction 135 527-539. (doi:10.1530/REP-07-0496)
62. Shirasuna K, Asahi T, Sasaki M, Shimizu T & Miyamoto A 2009 Distribution of arteriolovenous vessels, capillaries and eNOS expression in the bovine corpus luteum during the estrous cycle: a possible implication of different sensitivity by luteal phase to PGF(2 alpha) in the increase of luteal blood flow. Journal of Reproduction and Development 56 124-130. (doi:10.1262/jrd.09-106O)
63. Skarzynski DJ, Miyamoto Y & Okuda K 2000 Production of prostaglandin F(2alpha) by cultured bovine endometrial cells in response to tumor necrosis factor alpha: cell type specificity and intracellular mechanisms. Biology of Reproduction 62 1116-1120. (doi:10.1095/biolreprod62.5. 1116)
64. Spanel-Borowski K 1991 Diversity of ultrastructure in different phenotypes of cultured microvessel endothelial cells isolated from bovine corpus luteum. Cell and Tissue Research 266 37-49. (doi:10.1007/ BF00678709)
65. Spencer TE & Bazer FW 1996 Ovine interferon tau suppresses transcription of the estrogen receptor and oxytocin receptor genes in the ovine endometrium. Endocrinology 137 1144-1147. (doi:10.1210/en.137.3. 1144)
66. Spencer TE, Becker WC, George P, Mirando MA, Ogle TF & Bazer FW 1995 Ovine interferon-tau inhibits estrogen receptor up-regulation and estrogen-induced luteolysis in cyclic ewes. Endocrinology 136 4932-4944. (doi:10.1210/en.136.11.4932)
67. Spencer TE, Stagg AG, Ott TL, Johnson GA, Ramsey WS & Bazer FW 1999 Differential effects of intrauterine and subcutaneous administration of recombinant ovine interferon tau on the endometrium of cyclic ewes. Biology of Reproduction 61 464-470. (doi:10.1095/biolreprod61.2.464)
68. Spencer TE, Burghardt RC, Johnson GA & Bazer FW 2004 Conceptus signals for establishment and maintenance of pregnancy. Animal Reproduction Science 82-83 537-550. (doi:10.1016/j.anireprosci. 2004.04.014)
69. Staggs KL, Austin KJ, Johnson GA, Teixeira MG, Talbott CT, Dooley VA & Hansen TR 1998 Complex induction of bovine uterine proteins by interferon-tau. Biology of Reproduction 59 293-297. (doi:10.1095/ biolreprod59.2.293)
70. Standaert FE, Zamora CS & Chew BP 1991 Quantitative and qualitative changes in blood leukocytes in the porcine ovary. American Journal of Reproductive Immunology 25 163-168.
71. Teixeira MG, Austin KJ, Perry DJ, Dooley VD, Johnson GA, Francis BR & Hansen TR 1997 Bovine granulocyte chemotactic protein-2 is secreted by the endometrium in response to interferon-tau (IFN-tau). Endocrine 6 31-37. (doi:10.1007/BF02738799)
72. Wang Y & Oliver G 2010 Current views on the function of the lymphatic vasculature in health and disease. Genes and Development 24 2115-2126. (doi:10.1101/gad.1955910)
73. Watanabe S, Shirasuna K, Matsui M, Yamamoto D, Berisha B, Schams D & Miyamoto A 2006 Effect of intraluteal injection of endothelin type A receptor antagonist on PGF2alpha-induced luteolysis in the cow. Journal of Reproduction and Development 52 551-559. (doi:10.1262/ jrd.18018)
74. Wilting J, Eichmann A & Christ B 1997 Expression of the avian VEGF receptor homologues Quek1 and Quek2 in blood-vascular and lymphatic endothelial and non-endothelial cells during quail embryonic development. Cell and Tissue Research 288 207-223. (doi:10.1007/ s004410050807)
75. Woad KJ, Hammond AJ, Hunter M, Mann GE, Hunter MG & Robinson RS 2009 FGF2 is crucial for the development of bovine luteal endothelial networks in vitro. Reproduction 138 581-588. (doi:10.1530/REP-09-0030)
76. Wulff C, Wilson H, Rudge JS, Wiegand SJ, Lunn SF & Fraser HM 2001 Luteal angiogenesis: prevention and intervention by treatment with vascular endothelial growth factor trap(A40). Journal of Clinical Endocrinology and Metabolism 86 3377-3386. (doi:10.1210/jc.86.7. 3377)
77. Xu F & Stouffer RL 2009a Existence of the lymphatic system in the primate corpus luteum. Lymphatic Research and Biology 7 159-168. (doi:10. 1089/lrb.2009.0009)
78. Xu F & Stouffer RL 2009b Local delivery of an anti-lymphangiogenic agent supresses ovulation in the monkey. Biology of Reproduction 81 ABSTRACT 516. (doi:10.1095/biolreprod.108.074732)
79. Yamada Y, Nezu J, Shimane M & Hirata Y 1997 Molecular cloning of a novel vascular endothelial growth factor, VEGFD. Genomics 42 483-488. (doi:10.1006/geno.1997.4774)
80. Yamashita H, Kamada D, Shirasuna K, Matsui M, Shimizu T, Kida K, Berisha B, Schams D & Miyamoto A 2008 Effect of local neutralization of basic fibroblast growth factor or vascular endothelial growth factor by a specific antibody on the development of the corpus luteum in the cow. Molecular Reproduction and Development 75 1449-1456. (doi:10.1002/mrd.20878)
81. Yang L, Wang XL, Wan PC, Zhang LY, Wu Y, Tang DW & Zeng SM 2010 Upregulation of expression of interferon-stimulated gene 15 in the bovine corpus luteum during early pregnancy. Journal of Dairy Science 93 1000-1011. (doi:10.3168/jds.2009-2529)
82. Yasuda M, Shimizu S, Tokuyama S, Watanabe T, Kiuchi Y & Yamamoto T 2000 A novel effect of polymorphonuclear leukocytes in the facilitation of angiogenesis. Life Sciences 66 2113-2121. (doi:10.1016/S0024- 3205(00)00537-3)
83. Zarco L, Stabenfeldt GH, Basu S, Bradford GE & Kindahl H 1988a Modification of prostaglandin F-2 alpha synthesis and release in the ewe during the initial establishment of pregnancy. Journal of Reproduction and Fertility 83 527-536. (doi:10.1530/jrf.0.0830527)
84. Zarco L, Stabenfeldt GH, Quirke JF, Kindahl H & Bradford GE 1988b Release of prostaglandin F-2 alpha and the timing of events associated with luteolysis in ewes with oestrous cycles of different lengths. Journal of Reproduction and Fertility 83 517-526. (doi:10.1530/jrf.0. 0830517)
85. Zeng Y, Opeskin K, Goad J & Williams ED 2006 Tumor-induced activation of lymphatic endothelial cells via vascular endothelial growth factor receptor-2 is critical for prostate cancer lymphatic metastasis. Cancer Research 66 9566-9575. (doi:10.1158/0008-5472. CAN-06-1488)
86. Zheng J, Redmer DA & Reynolds LP 1993 Vascular development and heparin-binding growth factors in the bovine corpus luteum at several stages of the estrous cycle. Biology of Reproduction 49 1177-1189. (doi:10.1095/ biolreprod49.6.1177)