Evolution and function of the uterine serpins (SERPINA14)

American Journal of Reproductive Immunology

Volumn 64, Issue 4, 2010, Pages 265-274

  Padua, Maria B ^a   Hansen, Peter J ^b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Immunoregulation; Pregnancy; Progesterone; Uterine milk proteins; Uterine serpin

Indexed keywords

PROGESTERONE; SERINE PROTEINASE INHIBITOR; UTEROFERRIN;

ALLOGRAFT; BOVIDS; CARNIVORE; CELL FUNCTION; DOLPHIN; ENDOMETRIUM; ENZYME INHIBITION; FEMALE; GENE DUPLICATION; GENETIC VARIABILITY; GOAT; GRAFT REJECTION; HORSE; HUMAN; IMMUNOREGULATION; IRON TRANSPORT; LYMPHOCYTE PROLIFERATION; MOLECULAR EVOLUTION; NATURAL KILLER CELL; NONHUMAN; PHYLOGENY; PREGNANCY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SWINE;

ANIMALS; ANIMALS, DOMESTIC; ENDOMETRIUM; EVOLUTION, MOLECULAR; FEMALE; FETUS; GENE EXPRESSION REGULATION; MAMMALS; PLACENTA; PREGNANCY; PREGNANCY, ANIMAL; PROGESTERONE; SERINE PROTEINASE INHIBITORS; SERPINS; UTERUS;

EID: 77956256441     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2010.00901.x     Document Type: Review

References (63)

1. Louis EJ. Making the most of redundancy. Nature 2007, 449:673-674.
2. Moffatt J, Bazer FW, Hansen PJ, Chun PW, Roberts RM. Purification, secretion and immunocytochemical localization of the uterine milk proteins, major progesterone-induced proteins in uterine secretions of the sheep. Biol Reprod 1987, 36:419-430.
3. Baumbach GA, Ketcham CM, Richardson DE, Bazer FW, Roberts RM. Isolation and characterization of a high molecular weight stable pink form of uteroferrin from uterine secretions and allantoic fluid of pigs. J Biol Chem 1986, 261:12869-12878.
4. Leslie MV, Hansen PJ, Newton GR. Uterine secretions of the cow contain proteins that are immunochemically related to the major progesterone-induced proteins of the sheep uterus. Domest Anim Endocrinol 1990, 7:517-526.
5. Roberts RM, Bazer FW. The functions of uterine secretions. J Reprod Fertil 1988, 82:875-892.
6. Ing NH, Roberts RM. The major progesterone-induced proteins secreted into the sheep uterus are members of the serpin superfamily of protease inhibitors. J Biol Chem 1989, 264:3372-3379.
7. Malathy PV, Imakawa K, Simmen RC, Roberts RM. Molecular cloning of the uteroferrin-associated protein, a major progesterone-induced serpin secreted by the porcine uterus, and expression of its mRNA during pregnancy. Mol Endocrinol 1990, 4:428-440.
8. Mathialagan N, Hansen TR. Pepsin-inhibitory activity of uterine serpins. Proc Natl Acad Sci USA 1996, 93:13653-13658.
9. Irving JA, Pike RN, Lesk AM, Whisstock JC. Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res 2000, 10:1845-1864.
10. Tekin ş, Padua MB, Newton GR, Hansen PJ. Identification and cloning of caprine uterine serpin. Mol Reprod Dev 2005, 70:262-270.
11. Padua MB, Kowaslki AA, Cañas MY, Hansen PJ. The molecular phylogeny of uterine serpins and its relationship to evolution of placentation. FASEB J 2010, 24:526-537.
12. Peltier MR, Raley LC, Liberles DA, Benner SA, Hansen PJ. Evolutionary history of the uterine serpins. J Exp Zool 2000, 288:165-174.
13. Ragg H, Lokot T, Kamp PB, Atchley WR, Dress A. Vertebrate serpins: construction of a conflict-free phylogeny by combining exon-intron and diagnostic site analyses. Mol Biol Evol 2001, 18:577-584.
14. Padua MB, Hansen PJ. Changes in expression of cell-cycle-related genes in PC-3 prostate cancer cells caused by ovine uterine serpin. J Cell Biochem 2009, 107:1182-1188.
15. Ulbrich SE, Frohlich T, Schulke K, Englberger E, Waldschmitt N, Arnold GJ, Reichenbach HD, Reichenbach M, Wolf E, Meyer HHD, Bauersachs S. Evidence for estrogen-dependent uterine serpin (SERPINA14) expression during estrus in the bovine endometrial glandular epithelium and lumen. Biol Reprod 2009, 81:795-805.
16. Vogel P. The current molecular phylogeny of eutherian mammals challenges previous interpretations of placental evolution. Placenta 2005, 26:591-596.
17. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
18. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
19. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992, 8:275-282.
20. Strimmer K, von Haeseler A. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 1996, 13:964-969.
21. Schmidt HA, Strimmer K, Vingron M, von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002, 18:502-504.
22. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
23. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 2003, 31:3497-3500.
24. Montgelard C, Catzeflis FM, Douzery E. Phylogenetic relationships of artiodactyls and cetaceans as deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences. J Mol Evol 1997, 14:550-559.
25. Hungtinton JA. Shape-shifting serpins-advantages of a mobile mechanism. Trends Biochem Sci 2006, 31:427-435.
26. Whisstock JC, Bottomley SP. Molecular gymnastics: serpin structure folding and misfolding. Curr Opin Struct Biol 2006, 16:761-768.
27. Liu WJ, Hansen PJ. Progesterone-induced secretion of dipeptidyl peptidase-IV (cell differentiation antigen 26) by the uterine endometrium of the ewe and cow that costimulates lymphocyte proliferation. Endocrinology 1995, 136:779-787.
28. Potempa J, Korzus E, Travis J. The serpin superfamily of proteinase inhibitors: structure, function and regulation. J Biol Chem 1994, 269:15957-15960.
29. Peltier MR, Grant TR, Hansen PJ. Distinct physical and structural properties of the ovine uterine serpin. Biochim Biophys Acta 2000, 1479:37-51.
30. Leslie MV, Hansen PJ. Progesterone-regulated secretion of the serpin-like proteins of the ovine and bovine uterus. Steroids 1991, 56:589-597.
31. Stewart MD, Johnson GA, Gray CA, Burghardt RC, Schuler LA, Joyce MM, Bazer FW, Spencer TE. Prolactin receptor and uterine milk protein expression in the ovine endometrium during the estrous cycle and pregnancy. Biol Reprod 2000, 62:1779-1789.
32. Ing NH, Francis H, McDonnell JJ, Amann JF, Roberts RM. Progesterone induction of the uterine milk proteins: major secretory proteins of sheep endometrium. Biol Reprod 1989, 41:643-654.
33. Stephenson DC, Leslie MV, Low BG, Newton GR, Hansen PJ, Bazer FW. Secretion of the major progesterone-induced proteins of the sheep uterus by caruncular and intercaruncular endometrium of the pregnant ewe from days 20-140 of gestation. Domest Anim Endocrinol 1989, 6:349-362.
34. Gray CA, Stewart MD, Johnson GA, Spencer TE. Postpartum uterine involution in sheep in endometrial gene expression. Reproduction 2003, 125:185-198.
35. Padua MB, Tekin ş, Spencer TE, Hansen PJ. Actions of progesterone on uterine immunosuppression and endometrial gland development in the uterine gland knockout (UGKO) ewe. Mol Reprod Dev 2005, 71:347-357.
36. Spencer TE, Gray A, Johnson GA, Taylor KM, Gertler A, Gootwine E, Ott TL, Bazer FW. Effects of recombinant ovine interferon tau, placental lactogen, and growth hormone on the ovine uterus. Biol Reprod 1999, 61:1409-1418.
37. Noel S, Herman A, Johnson GA, Gray CA, Stewart MD, Bazer FW, Gertler A, Spencer TE. Ovine placental lactogen specifically binds to endometrial glands to the ovine uterus. Biol Reprod 2003, 68:772-780.
38. Bauersachs S, Ulbrich SE, Gross K, Schmidt SEM, Meyer HHD, Einspanier R, Wenigerkind H, Vermehren M, Blum H, Sinowatz F, Wolf E. Gene expression profiling of bovine endometrium during the oestrus cycle: detection of molecular pathways involved in functional changes. J Mol Endocrinol 2005, 34:889-908.
39. Khatib H, Schutzkus V, Chang YM, Rosa GJM. Pattern of expression of the uterine milk protein gene and its association with productive life in cattle. J Dairy Sci 2006, 90:2427-2433.
40. Hansen PJ, Bazer FW, Segerson EC. Skin graft survival in the uterine lumen of ewes treated with progesterone. Am J Reprod Immunol Microbiol 1986, 12:48-54.
41. Hansen PJ. Regulation of uterine immune function by progesterone-lessons from the sheep. J Reprod Immunol 1998, 40:63-79.
42. Segerson EC, Moffatt RJ, Bazer FW, Roberts MR. Suppression of phytohemagglutinin-stimulated lymphocyte blastogenesis by ovine uterine milk protein. Biol Reprod 1984, 30:1175-1186.
43. Hansen PJ, Segerson EC, Bazer FW. Characterization of immunosuppressive substances in the basic protein fraction of uterine secretions of pregnant ewes. Biol Reprod 1987, 36:393-403.
44. Stephenson DC, Hansen PJ, Newton GR, Bazer FW, Low BG. Inhibition of lymphocyte proliferation by uterine fluid from the pregnant ewe. Biol Reprod 1989, 41:1063-1075.
45. Skopets B, Hansen PJ. Identification of the predominant proteins in uterine fluids of unilaterally pregnant ewes that inhibit lymphocyte proliferation. Biol Reprod 1993, 49:997-1007.
46. Skopets B, Liu WJ, Hansen PJ. Effects of endometrial serpin-like proteins on immune responses in sheep. Am J Reprod Immunol 1995, 33:86-93.
47. Padua MB, Hansen PJ. Regulation of DNA synthesis and the cell cycle in human prostate cancer cells and lymphocytes by ovine uterine serpin. BMC Cell Biol 2008, 9:5.
48. Liu WJ, Hansen PJ. Effect of the progesterone-induced serpin-like proteins of the sheep endometrium on natural-killer cell activity in sheep and mice. Biol Reprod 1993, 49:1008-1014.
49. Tekin ş, Hansen PJ. Natural-killer like cells in the sheep: functional characterization and regulation by pregnancy-associated proteins. Exp Biol Med 2002, 227:803-811.
50. Tekin ş, Padua MB, Brad AM, Hansen PJ. Antiproliferative actions of ovine uterine serpin. Am J Reprod Immunol 2005, 53:136-143.
51. Tekin ş, Padua MB, Brad AM, Rhodes ML, Hansen PJ. Expression and properties of recombinant ovine uterine serpin. Exp Biol Med (Maywood) 2006, 231:1313-1322.
52. Liu WJ, Peltier MR, Hansen PJ. Binding of ovine uterine serpin to lymphocytes. Am J Reprod Immunol 1999, 41:428-432.
53. Peltier MR, Liu WJ, Hansen PJ. Regulation of lymphocyte proliferation by uterine serpin: interleukin-2 mRNA production, CD25 expression and responsiveness to interleukin-2. Exp Biol Med 1999, 223:75-81.
54. Newton GR, Hansen PJ, Bazer FW, Leslie MV, Stephenson DC, Low BG. Presence of major progesterone-induced proteins of the sheep endometrium in fetal fluids. Biol Reprod 1989, 40:417-424.
55. McFarlane JR, Foulds LM, O'Connor AE, Phillips DJ, Jenkin G, Hearn MTW, Kretser DM. Uterine milk protein, a novel activin-binding protein, is present in ovine allantoic fluid. Endocrinology 1999, 140:4745-4752.
56. Murray MK, Malathy PV, Bazer FW, Roberts RM. Structural relationship, biosynthesis, and immunocytochemical localization of uteroferrin-associated basic glycoproteins. J Biol Chem 1989, 264:4143-4150.
57. Xie S, Low BG, Nagel RJ, Kramer KK, Anthony RV, Zoli AP, Beckers JF, Roberts RM. Identification of the major pregnancy-specific antigens of cattle and sheep as inactive members of the aspartic proteinase family. Proc Natl Acad Sci USA 1991, 88:10247-10251.
58. Green JA, Xie S, Roberts RM. Pepsin-related molecules secreted by trophoblast. Rev Reprod 1998, 3:62-69.
59. Hansen PJ, Newton GR. Binding of immunoglobulins to the major progesterone-induced proteins secreted by the sheep uterus. Arch Biochem Biophys 1988, 260:208-217.
60. Buhi WC, Ducsay CA, Bazer FW, Roberts RM. Iron transfer between the purple phosphatase uteroferrin and transferring and its possible role in iron metabolism of the fetal pig. J Biol Chem 1982, 257:1712-1723.
61. Chen TT, Bazer FW, Gebhardt BM, Roberts RM. Uterine secretion in mammals: synthesis and placental transport of a purple acid phosphatase in pigs. Biol Reprod 1975, 13:304-313.
62. Ducsay CA, Buhi WC, Bazer FW, Roberts RM. Role of uteroferrin in iron transport and macromolecular uptake by allantoic epithelium of the porcine conceptus. Biol Reprod 1982, 26:729-743.
63. Renegar RH, Bazer FW, Roberts RM. Placental transport and distribution of uteroferrin in the fetal pig. Biol Reprod 1982, 27:1247-1260.