Dynamic expression of calcium-regulatory molecules, TRPV6 and S100g, in the uterine endometrium during pregnancy in pigs

Biology of Reproduction

Volumn 81, Issue 6, 2009, Pages 1122-1130

  Choi, Yohan ^a   Seo, Heewon ^a   Kim, Mingoo ^a   Ka, Hakhyun ^a  

^a Yonsei University Wonju   (South Korea)

Author keywords

Calcium; Female reproductive tract; Implantation; Pig; S100G; Steroid hormones; TRPV6; Uterus

Indexed keywords

CALCIUM ION; ESTROGEN; MESSENGER RNA; PROGESTERONE; PROTEIN S 100; PROTEIN S 100 G; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 6; CALBINDIN; CALCIUM; ESTRADIOL; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CHORION; CONCEPTUS; CONTROLLED STUDY; EMBRYO; ENDOMETRIUM; EPITHELIUM CELL; ESTRUS CYCLE; EXPERIMENTAL PIG; FEMALE; NIDATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; ANALYSIS OF VARIANCE; ANIMAL; BREEDING; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GESTATIONAL AGE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; ORGAN CULTURE TECHNIQUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SWINE; WESTERN BLOTTING;

SUIDAE;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CALCIUM; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; EMBRYO IMPLANTATION; ENDOMETRIUM; EPITHELIAL CELLS; ESTRADIOL; ESTROUS CYCLE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ORGAN CULTURE TECHNIQUES; PREGNANCY; PREGNANCY, ANIMAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SWINE; TRPV CATION CHANNELS;

EID: 73949142428     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.076703     Document Type: Article

References (48)

1. Clapham DE. Calcium signaling. Cell 2007; 131:1047-1058.
2. Whitaker M. Calcium at fertilization and in early development. Physiol Rev 2006; 86:25-88.
3. Tinel H, Denker HW, Thie M. Calcium influx in human uterine epithelial RL95-2 cells triggers adhesiveness for trophoblast-like cells: model studies on signalling events during embryo implantation. Mol Hum Reprod 2000; 6:1119-1130.
4. Zhu LJ, Bagchi MK, Bagchi IC. Attenuation of calcitonin gene expression in pregnant rat uterus leads to a block in embryonic implantation. Endocrinology 1998; 139:330-339.
5. Luu KC, Nie GY, Salamonsen LA. Endometrial calbindins are critical for embryo implantation: evidence from in vivo use of morpholino antisense oligonucleotides. Proc Nad Acad Sci U S A 2004; 101:8028-8033.
6. Geisert RD, Renegar RH, Thatcher WW, Roberts RM, Bazer FW. Establishment of pregnancy in the pig, I: interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biol Reprod 1982; 27:925-939.
7. 2+ reabsorption in the distal nephron. Annu Rev Physiol 2002; 64:529-549.
8. 2+ channels ECaC1 and ECaC2 (TRPV5 and TRPV6): role of the intracellular loop located between transmembrane segments 2 and 3. J Biol Chem 2002; 277:30852-30858.
9. Vennekens R, Hoenderop JG, Prenen J, Stuiver M, Willems PH, Droogmans G, Nilius B, Bindels RJ. Permeation and gating properties of the novel epithehal Ca(2+) channel. J Biol Chem 2000; 275:3963-3969.
10. Hoenderop JG, Nilius B, Bindels RJ. Calcium absorption across epithelia. Physiol Rev 2005; 85:373-422.
11. Lee GS, Jeung EB. Uterine TRPV6 expression during the estrous cycle and pregnancy in a mouse model. Am J Physiol Endocrinol Metab 2007; 293:E132-E138.
12. + ATPase 1b during rat estrous cycle. Am J Physiol Endocrinol Metab 2006; 291:E234-E241.
13. Ka H, Seo H, Kim M, Choi Y, Lee CK. Identification of differentially expressed genes in the uterine endometrium on day 12 of the estrous cycle and pregnancy in pigs. Mol Reprod Dev 2009; 76:75-84.
14. den Dekker E, Hoenderop JG, Nilius B, Bindels RJ. The epithelial calcium channels, TRPV5 & TRPV6: from identification towards regulation. Cell Calcium 2003; 33:497-507.
15. Tatsumi K, Higuchi T, Fujiwara H, Nakayama T, Itoh K, Mori T, Fujii S, Fujita J. Expression of calcium binding protein D-9k messenger RNA in the mouse uterine endometrium during implantation. Mol Hum Reprod 1999; 5:153-161.
16. Warembourg M, Perret C, Thomasset M. Analysis and in situ detection of cholecalcin messenger RNA (9000 Mr CaBP) in the uterus of the pregnant rat. Cell Tissue Res 1987; 247:51-57.
17. Krisinger J, Jeung EB, Simmen RC, Leung PC. Porcine calbindin-D9k gene: expression in endometrium, myometrium, and placenta in the absence of a functional estrogen response element in intron A. Biol Reprod 1995; 52:115-123.
18. Nie GY, Li Y, Wang J, Minoura H, Findlay JK, Salamonsen LA. Complex regulation of calcium-binding protein D9k (calbindin-D(9k)) in the mouse uterus during early pregnancy and at the site of embryo implantation. Biol Reprod 2000; 62:27-36.
19. Choi KC, Jeung EB. Molecular mechanism of regulation of the calcium-binding protein calbindin-D9k, and its physiological role(s) in mammals: a review of current research. J Cell Mol Med 2008; 12:409-420.
20. Yun SM, Choi KC, Kim IH, An BS, Lee GS, Hong EJ, Oh GT, Jeung EB. Dominant expression of porcine Calbindin-D9k in the uterus during a luteal phase. Mol Reprod Dev 2004; 67:251-256.
21. Jaeger LA, Johnson GA, Ka H, Garlow JG, Burghardt RC, Spencer TE, Bazer FW. Functional analysis of autocrine and paracrine signalling at the uterine-conceptus interface in pigs. Reprod Suppl 2001; 58:191-207.
22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25:402-408.
23. Ka H, Jaeger LA, Johnson GA, Spencer TE, Bazer FW. Keratinocyte growth factor is up-regulated by estrogen in the porcine uterine endometrium and functions in trophectoderm cell proliferation and differentiation. Endocrinology 2001; 142:2303-2310.
24. Braissant O, Wahli W. A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1998; 1:10-16.
25. Bianco SD, Peng JB, Takanaga H, Suzuki Y, Crescenzi A, Kos CH, Zhuang L, Freeman MR, Gouveia CH, Wu J, Luo H, Mauro T, et al. Marked disturbance of calcium homeostasis in mice with targeted disruption of the Trpv6 calcium channel gene. J Bone Miner Res 2007; 22:274-285.
26. Bazer FW, Ott TL, Spencer TE. Endocrinology of the transition from recurring estrous cycles to establishment of pregnancy in subprimate mammals. In: Bazer FW (ed.). The Endocrinology of Pregnancy. Totowa, NJ: Humana Press; 2998:1-34.
27. White FJ, Ross JW, Joyce MM, Geisert RD, Burghardt RC, Johnson GA. Steroid regulation of cell specific secreted phosphoprotein 1 (osteopontin) expression in the pregnant porcine uterus. Biol Reprod 2005; 73:1294-1301.
28. Seo H, Kim M, Choi Y, Lee CK, Ka H. Analysis of lysophosphatidic acid (LPA) receptor and LPA-induced endometrial prostaglandin-endoperoxide synthase 2 expression in the porcine uterus. Endocrinology 2008; 149: 6166-6175.
29. Joyce MM, Burghardt RC, Geisert RD, Burghardt JR, Hooper RN, Ross JW, Ashworth MD, Johnson GA. Pig conceptuses secrete estrogen and interferons to differentially regulate uterine STAT1 in a temporal and cell type-specific manner. Endocrinology 2007; 148:4420-4431.
30. Basha SM, Bazer FW, Geisert RD, Roberts RM. Progesterone-induced uterine secretions in pigs: recovery from pseudopregnant and unilaterally pregnant gilts. J Anim Sci 1980; 50:113-123.
31. Fazleabas AT, Bazer FW, Roberts RM. Purification and properties of a progesterone-induced plasmin/trypsin inhibitor from uterine secretions of pigs and its immunocytochemical localization in the pregnant uterus. J Biol Chem 1982; 257:6886-6897.
32. Adams KL, Bazer FW, Roberts RM. Progesterone-induced secretion of a retinol-binding protein in the pig uterus. J Reprod Fertil 1981; 62:39-47.
33. Ka H, Al-Ramadan S, Erikson DW, Johnson GA, Burghardt RC, Spencer TE, Jaeger LA, Bazer FW. Regulation of expression of fibroblast growth factor 7 in the pig uterus by progesterone and estradiol. Biol Reprod 2007; 77:172-180.
34. Geisert RD, Brenner RM, Moffatt RJ, Harney JP, Yellin T, Bazer FW. Changes in oestrogen receptor protein, mRNA expression and localization in the endometrium of cyclic and pregnant gilts. Reprod Fertil 1993; 5: 247-260.
35. Geisert RD, Pratt TN, Bazer FW, Mayes JS, Watson GH. Immunocytochemical localization and changes in endometrial progestin receptor protein during the porcine oestrous cycle and early pregnancy. Reprod Fertil Dev 1994; 6:749-760.
36. Fischer HE, Bazer FW, Fields MJ. Steroid metabolism by endometrial and conceptus tissues during early pregnancy and pseudopregnancy in gilts. J Reprod Fertil 1985; 75:69-78.
37. Robertson HA, King GJ. Plasma concentrations of progesterone, oestrone, oestradiol-17beta and of oestrone sulphate in the pig at implantation, during pregnancy and at parturition. J Reprod Fertil 1974; 40:133-141.
38. Knight JW, Bazer FW, Thatcher WW, Franke DE, Wallace HD. Conceptus development in intact and unilaterally hysterectomized-ovariectomized gilts: interrelations among hormonal status, placental development, fetal fluids and fetal growth. J Anim Sci 1977; 44:620-637.
39. Bazer FW, Slayden OD. Progesterone-induced gene expression in uterine epithelia: a myth perpetuated by conventional wisdom. Biol Reprod 2008; 79:1008-1009.
40. Mathieu CL, Burnett SH, Mills SE, Overpeck JG, Bruns DE, Bruns ME. Gestational changes in calbindin-D9k in rat uterus, yolk sac, and placenta: implications for maternal-fetal calcium transport and uterine muscle function. Proc Natl Acad Sci U S A 1989; 86:3433-3437.
41. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003; 4:517-529.
42. Geisert RD, Thatcher WW, Roberts RM, Bazer FW. Establishment of pregnancy in the pig: III. Endometrial secretory response to estradiol valerate administered on day 11 of the estrous cycle. Biol Reprod 1982; 27:957-965.
43. Burghardt RC, Bowen JA, Newton GR, Bazer FW. Extracellular matrix and the implantation cascade in pigs. J Reprod Fertil Suppl 1997; 52:151-164.
44. Leitinger B, McDowall A, Stanley P, Hogg N. The regulation of integrin function by Ca(2+). Biochim Biophys Acta 2000; 1498:91-98.
45. Roberts RM, Bazer FW. The functions of uterine secretions. J Reprod Fertil 1988; 82:875-892.
46. Spencer TE, Bazer FW. Uterine and placental factors regulating conceptus growth in domestic animals. J Anim Sci 2004; 82(E-suppl):E4-E13.
47. Garlow JE, Ka H, Johnson GA, Burghardt RC, Jaeger LA, Bazer FW. Analysis of osteopontin at the maternal-placental interface in pigs. Biol Reprod 2002; 66:718-725.
48. Ryan PL, Baum DL, Lenhart JA, Ohleth KM, BagneU CA. Expression of uterine and cervical epithelial Cadherin during relaxin-induced growth in pigs. Reproduction 2001; 122:929-937.