Expression of the vascular endothelial growth factor-receptor system in the porcine endometrium throughout the estrous cycle and early pregnancy

Molecular Reproduction and Development

Volumn 75, Issue 2, 2008, Pages 362-372

  Kaczmarek, Monika M ^a   Waclawik, Agnieszka ^a   Blitek, Agnieszka ^a   Kowalczyk, Anna E ^a   Schams, Dieter ^b   Ziecik, Adam J ^a  

^a INSTITUTE OF ANIMAL REPRODUCTION AND FOOD RESEARCH   (Poland)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Angiogenesis; Endometrium; Pig; VEGF; VEGFR 1; VEGFR 2

Indexed keywords

MESSENGER RNA; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ARTICLE; CONTROLLED STUDY; ENDOMETRIUM CELL; EPITHELIUM CELL; ESTRUS CYCLE; FEMALE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION REGULATION; HUMAN; IMMUNOHISTOCHEMISTRY; NUCLEOTIDE SEQUENCE; OVULATION; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SWINE; WESTERN BLOTTING;

ACTINS; ANIMALS; ENDOMETRIUM; ESTRUS; FEMALE; GENE EXPRESSION REGULATION; PREGNANCY; PREGNANCY, ANIMAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SWINE; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

ANIMALIA; SUIDAE; SUS;

EID: 37849025186     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20815     Document Type: Article

References (56)

1. Akins EL, Morrissette MC. 1968. Gross ovarian changes during estrous cycle of swine. Am J Vet Res 29:1953-1957.
2. Anthony FW, Wheeler T, Elcock CL, Pickett M, Thomas EJ. 1994. Short report: Identification of a specific pattern of vascular endothelial growth factor mRNA expression in human placenta and cultured placental fibroblasts. Placenta 15:55-561.
3. Barboni B, Turriani M, Galeati G, Spinaci M, Bacci ML, Forni M, Mattioli M. 2000. Vascular endothelial growth factor production in growing pig antral follicles. Biol Reprod 63:858-864.
4. Bazer FW, Geisert RD, Thatcher WW, Roberts RM. 1982. The establishment and maintenance of pregnancy. In: Cole DJA, Foxcroft GR, editors. Control of pig reproduction. London: Butterworth Scientific. pp 227-253.
5. Bornes S, Boulard M, Hieblot C, Zanibellato C, Iacovoni JS, Prats H, Touriol C. 2004. Control of the vascular endothelial growth factor internal ribosome entry site (IRES) activity and translation initiation by alternatively spliced coding sequences. J Biol Chem 279:18717-18726.
6. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
7. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
8. Celia G, Osol G. 2005. Uterine venous permeability in the rat is altered in response to pregnancy, vascular endothelial growth factor, and venous constriction. Endothelium 12:81-88.
9. Charnock-Jones DS, Sharkey AM, Rajput-Williams J, Burch D, Schofield JP, Fountain SA, Boocock CA, Smith SK. 1993. Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol Reprod 48:1120-1128.
10. Charnock-Jones DS, Clark DE, Licence D, Day K, Wooding FB, Smith SK. 2001. Distribution of vascular endothelial growth factor (VEGF) and its binding sites at the maternal-fetal interface during gestation in pigs. Reproduction 122:753-760.
11. Cheung CY, Singh M, Ebaugh MJ, Brace RA. 1995. Vascular endothelial growth factor gene expression in ovine placenta and fetal membranes. Am J Obstet Gynecol 173:753-759.
12. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
13. Christenson RK, Farley DB, Anderson LH, Ford SP. 1994. Luteal maintenance during early pregnancy in the pig: Role for prostaglandin E2. Prostaglandins 47:61-75.
14. Clark JH, Markaveich BM. 1988. Actions of ovarian steroids. In: Knobil E, Neill J, editors. The physiology of reproduction. New York: Raven Press. pp 675-724.
15. Clauss M, Weich H, Breier G, Knies U, Rockl W, Waltenberger J, Risau W. 1996. The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem 271:17629-17634.
16. Cullinan-Bove K, Koos RD. 1993. Vascular endothelial growth factor/vascular permeability factor expression in the rat uterus: Rapid stimulation by estrogen correlates with estrogen-induced increases in uterine capillary permeability and growth. Endocrinology 133:829-837.
17. Das SK, Chakraborty I, Wang J, Dey SK, Hoffman LH. 1997. Expression of vascular endothelial growth factor (VEGF) and VEGF-receptor messenger ribonucleic acids in the peri-implantation rabbit uterus. Biol Reprod 56:1390-1399.
18. Dickson WM, Bosc MJ, Du Mesnil du Buisson F, Locatelli A. 1969. The use of an indicator diffusion procedure to measure the uterine blood flow in sows during the estrous cycle and pregnancy. Biol Reprod 1:295-301.
19. Ferrara N, Houck KA, Jakeman LB, Winer J, Leung DW. 1991. The vascular endothelial growth factor family of polypeptides. J Cell Biochem 47:211-218.
20. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.
21. Ferrara N, Chen H, Davis-Smyth T, Gerber HP, Nguyen TN, Peers D, Chisholm V, Hillan KJ, Schwall RH. 1998. Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat Med 4:336-340.
22. Ferrara N, Gerber HP, LeCouter J. 2003. The biology of VEGF and its receptors. Nat Med 9:669-676.
23. Fong GH, Rossant J, Gertsenstein M, Breitman ML. 1995. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66-70.
24. Ford SP, Christenson RK. 1979. Blood flow to uteri of sows during the estrous cycle and early pregnancy: Local effect of the conceptus on the uterine blood supply. Biol Reprod 21:617-624.
25. Ford SP. 1982. Control of uterine and ovarian blood flow throughout the estrous cycle and pregnancy of ewes, sows and cows. J Anim Sci 55:32-42.
26. Gargett CE, Rogers PA. 2001. Human endometrial angiogenesis. Reproduction 121:181-186.
27. Geisert RD, Renegar RH, Thatcher WW, Roberts RM, Bazer FW. 1982. Establishment of pregnancy in the pig. I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biol Reprod 27:925-939.
28. Geisert RD, Brenner RM, Moffatt RJ, Harney JP, Yellin T, Bazer FW. 1993. Changes in oestrogen receptor protein, mRNA expression and localization in the endometrium of cyclic and pregnant gilts. Reprod Fertil Dev 5:247-260.
29. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M, Ferrara N. 1999. VEGF is required for growth and survival in neonatal mice. Development 126:1149-1159.
30. Halder JB, Zhao X, Soker S, Paria BC, Klagsbrun M, Das SK, Dey SK. 2000. Differential expression of VEGF isofbrms and VEGF(164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF(164) in vascular permeability and angiogenesis during implantation. Genesis 26:213-224.
31. Henricks DM, Guthrie HD, Handlin DL. 1972. Plasma estrogen, progesterone and luteinizing hormone levels during the estrous cycle in pigs. Biol Reprod 6:210-218.
32. Horowitz JR, Rivard A, van der Zee R, Hariawala M, Sheriff DD, Esakof DD, Chaudhry GM, Symes JF, Isner J. 1997. Vascular endothelial growth factor produces nitric oxide-dependent hypotension: Evidence for a maintenance role in quiescent adult endothelium. Arterioscler Thromb Vasc Biol 17:2793-2800.
33. Hyder SM, Chiappetta C, Murthy L, Stancel GM. 1997. Selective inhibition of estrogen-regulated gene expression in vivo by the pure antiestrogen ICI 182,78. Cancer Res 57:2547-2549.
34. Kaczmarek MM, Kowalczyk AE, Waclawik A, Schams D, Ziecik AJ. 2007. Expression of vascular endothelial growth factor and its receptors in the porcine corpus luteum during the estrous cycle and early pregnancy. Mol Reprod Dev 74:730-739.
35. Kaeoket K, Persson E, Dalin AM. 2002. Corrigendum to "The sow endometrium at different stages of the oestrus cycle: Studies on morphological changes and infiltration by cells of the immune system". Anim Reprod Sci 73:89-107.
36. Ku DD, Zaleski JK, Liu S, Brock T. 1993. Vascular endothelial growth factor induces EDRF-dependent relaxation of coronary arteries. Am J Physiol 265:H586-H592.
37. Lei J, Jiang A, Pei D. 1998. Identification and characterization of a new splicing variant of vascular endothelial growth factor: VE GF183. Biochim Biophys Acta 1443:400-406.
38. Leiser R, Zimmermann W, Sidler X, Christen A. 1988. Normal cyclical morphology of the endometrium and ovary of swine. Tierärztl Prax 16:261-280.
39. Magness RR, Christenson RK, Ford S. 1983. Ovarian blood flow throughout the estrous cycle and early pregnancy in sows. Biol Reprod 28:1090-1096.
40. Nayak NR, Brenner RM. 2002. Vascular proliferation and vascular endothelial growth factor expression in the rhesus macaque endometrium. J Clin Endocrinol Metab 87:1845-1855.
41. Park JE, Chen HH, Winer J, Houck KA, Ferrara N. 1994. Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J Biol Chem 269:25646-25654.
42. Rabbani ML, Rogers PA. 2001. Role of vascular endothelial growth factor in endometrial vascular events before implantation in rats. Reproduction 122:85-90.
43. Rowe AJ, Wulff C, Fraser HM. 2003. Localization of mRNA for vascular endothelial growth factor (VEGF), angiopoietins and their receptors during the peri-implantation period and early pregnancy in marmosets (Callithrix jacchus). Reproduction 126:227-238.
44. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: A laboratory manual 2nd ed. New York: Cold Spring Harbor Laboratory Press.
45. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. 1983. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219:983-985.
46. 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.
47. Sharma HS, Tang ZH, Gho BC, Verdouw PD. 1995. Nucleotide sequence and expression of the porcine vascular endothelial growth factor. Biochim Biophys Acta 1260:235-238.
48. Shifren JL, Tseng JF, Zaloudek CJ, Ryan IP, Meng YG, Ferrara N, Jaffe RB, Taylor RN. 1996. Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: Implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. J Clin Endocrinol Metab 81:3112-3118.
49. Spagnuolo-Weaver M, Fuerst R, Campbell ST, Meehan BM, McNeilly F, Adair B, Allan G. 1999. A fluorimeter-based RT-PCR method for the detection and quantitation of porcine cytokines. J Immunol Methods 230:19-27.
50. Sugino N, Kashida S, Karube-Harada A, Takiguchi S, Kato H. 2002. Expression of vascular endothelial growth factor (VEGF) and its receptors in human endometrium throughout the menstrual cycle and in early pregnancy. Reproduction 123:379-387.
51. Tischer E, Mitchell R, Hartman T, Silva M, Gospodarowicz D, Fiddes JC, Abraham JA. 1991. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem 266:11947-11954.
52. Vonnahme KA, Wilson ME, Ford SP. 2001. Relationship between placental vascular endothelial growth factor expression and placental/endometrial vascularity in the pig. Biol Reprod 64:1821-1825.
53. Wei P, Chen XL, Song XX, Han CS, Liu YX. 2004. VEGF, bFGF, and their receptors in the endometrium of rhesus monkey during menstrual cycle and early pregnancy. Mol Reprod Dev 68:456-462.
54. Welter H, Wollenhaupt K, Tiemann U, Einspanier R. 2003. Regulation of the VEGF-system in the endometrium during steroid-replacement and early pregnancy of pigs. Exp Clin Endocrinol Diabetes 111:33-40.
55. Winther H, Ahmed A, Dantzer V. 1999. Immunohistochemical localization of vascular endothelial growth factor (VEGF) and its two specific receptors, Flt-1 and KDR, in the porcine placenta and non-pregnant uterus. Placenta 20:35-43.
56. Wulff C, Wilson H, Dickson SE, Wiegand SJ, Fraser HM. 2002. Hemochorial placentation in the primate: Expression of vascular endothelial growth factor, angiopoietins, and their receptors throughout pregnancy. Biol Reprod 66:802-812.