Cathepsin B, cathepsin L, and cystatin C in the porcine uterus and placenta: Potential roles in endometrial/placental remodeling and in fluid-phase transport of proteins secreted by uterine epithelia across placental areolae

Biology of Reproduction

Volumn 82, Issue 5, 2010, Pages 854-864

  Song, Gwonhwa ^c   Bailey, Daniel W ^a,b   Dunlap, Kathrin A ^a,b   Burghardt, Robert C ^a,b   Spencer, Thomas E ^a   Bazer, Fuller W ^a,c   Johnson, Greg A ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c Seoul National University   (South Korea)

Author keywords

Cathepsins; Cystatins; Estradiol; Gene regulation; Pig; Placenta; Progesterone; Proteases; Uterus

Indexed keywords

CATHEPSIN B; CATHEPSIN L; CYSTATIN C; ESTRADIOL; ESTROGEN; MESSENGER RNA; PROGESTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHORION; CONTROLLED STUDY; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; GILT (SWINE); HORMONAL REGULATION; IN SITU HYBRIDIZATION; LIQUID; NONHUMAN; PLACENTAL TRANSFER; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN TRANSPORT; TISSUE DISTRIBUTION;

ANIMALS; ANIMALS, NEWBORN; CATHEPSIN B; CATHEPSIN L; CYSTATIN C; ENDOMETRIUM; ENTEROCYTES; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; MATERNAL-FETAL EXCHANGE; PLACENTA; PREGNANCY; PROGESTERONE; PROTEIN TRANSPORT; RNA, MESSENGER; SWINE; TISSUE DISTRIBUTION;

SUIDAE; SUS;

EID: 77953827615     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.080929     Document Type: Article

References (55)

1. Enders AC. Comparative placental structure. Adv Drug Deliv Rev 1999; 38:3-15.
2. Aplin JD, Kimber SJ. Trophoblast-uterine interactions at implantation. Reprod Biol Endocrinol 2004; 2:48-59.
3. Burghardt RC, Johnson GA, Jaeger LA, Ka H, Garlow JE, Spencer TE, Bazer FW. Integrins and extracellular matrix proteins at the maternal-fetal interface in domestic animals. Cells Tissues Organs 2002; 172:202-217.
4. Johnson GA, Bazer FW, Jaeger LA, Ka H, Garlow JE, Pfarrer C, Spencer TE, Burghardt RC. Muc-1, integrin, and osteopontin expression during the implantation cascade in sheep. Biol Reprod 2001; 65:820-828. (Pubitemid 32777369)
5. Lessey BA, Castelbaum AJ. Integrins and implantation in the human. Rev Endocr Metab Disord 2002; 3:107-117.
6. Enders AC, Carter AM. What can comparative studies of placental structure tell us? A review. Placenta 2004; 25(suppl 1):S3-S9.
7. Salamonsen LA, Nie G. Proteases at the endometrial-trophoblast interface: their role in implantation. Rev Endocr Metab Disord 2002; 3:133-143.
8. Bjorkman N. Fine structure of the fetal-maternal area of exchange in the epitheliochorial and endotheliochorial types of placentation. Acta Anat Suppl (Basel) 1973; 61(suppl):1-22.
9. Renegar RH, Bazer FW, Roberts RM. Placental transport and distribution of uteroferrin in the fetal pig. Biol Reprod 1982; 27:1247-1260.
10. Dantzer V, Leiser R. Microvascularization of regular and irregular areolae of the areola-gland submunit of the porcine placenta: structural and functional aspects. Anat Embryol (Berl) 1993; 188:257-267. (Pubitemid 23287131)
11. Knight JW, Bazer FW, Thatcher WW, Franke DE, Wallace D. 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.
12. Bazer FW, Roberts RM. Biochemical aspects of conceptus-endometrial interactions. J Exp Zool 1983; 228:373-383.
13. Salamonsen LA. Role of proteases in implantation. Rev Reprod 1999; 4: 11-22.
14. Afonso S, Romagnano L, Babiarz B. The expression and function of cystatin C and cathepsin B and cathepsin L during mouse embryo implantation and placentation. Development 1997; 124:3415-3425. (Pubitemid 27440456)
15. Song G, Spencer TE, Bazer FW. Cathepsins in the ovine uterus: regulation by pregnancy, progesterone, and interferon tau. Endocrinology 2005; 146: 4825-4833.
16. Song G, Spencer TE, Bazer FW. Progesterone and interferon-tau regulate cystatin C in the endometrium. Endocrinology 2006; 147:3478-3483.
17. Song G, Bazer FW, Spencer TE. Differential expression of cathepsins and cystatin C in ovine uteroplacental tissues. Placenta 2007; 28:1091-1098.
18. Ren WP, Sloane F. Cathepsins D and B in breast cancer. Cancer Treat Res 1996; 83:325-352.
19. Kirschke H, Barrett AJ, Rawlings ND. Lysosomal Cysteine Proteases. Oxford: Oxford University Press; 1998.
20. Kirschke H, Shaw E. Rapid interaction of cathepsin L by Z-Phe-PheCHN12 and Z-Phe-AlaCHN2. Biochem Biophys Res Commun 1981; 101:454-458.
21. Kirschke H, Kembhavi AA, Bohley P, Barrett AJ. Action of rat liver cathepsin L on collagen and other substrates. Biochem J 1982; 201:367-372. (Pubitemid 12160167)
22. Mason RW, Johnson DA, Barrett AJ, Chapman HA. Elastinolytic activity of human cathepsin L. Biochem J 1986; 233:925-927.
23. Lah TT, Buck MR, Honn KV, Crissman JD, Rao NC, Liotta LA, Sloane BF. Degradation of laminin by human tumor cathepsin B. Clin Exp Metastasis 1989; 7:461-468.
24. Guinec N, Dalet-Fumeron V, Pagano M. "In vitro" study of basement membrane degradation by the cysteine proteases, cathepsins B, B-like and L. Digestion of collagen IV, laminin, fibronectin, and release of gelatinase activities from basement membrane fibronectin. Biol Chem Hoppe Seyler 1993; 374:1135-1146.
25. Hall A, Hakansson K, Mason RW, Abrahamson M. Structural basis for the biological specificity of cystatin C. Identification of leucine 9 in the Nterminal binding region as a selectivity-conferring residue in the inhibition of mammalian cysteine peptidases. J Biol Chem 1995; 270:5115-5121.
26. Murphy G, Ward R, Gavrilovic J, Atdinson S. Physiological mechanisms for metalloprotease activation. Matrix 1992; 1:224-230.
27. Goretzski L, Schmitt M, Mann K, Calvete J, Chucholowski N, Kramer M, Gunzler W, Janicke F, Graeff H. Effective activation of the proenzyme form of the urokinase-type plasminogen activator (pro-uPA) by the cysteine protease cathepsin L. FEBS Lett 1992; 297:112-118.
28. Kirschke H, Barrett AJ, Rawlings ND. Proteases 1: lysosomal cysteine proteases. Protein Profile 1995; 2:1581-1643.
29. Verhage HG, Boomsma RA, Mavrogianis PA, Li W, Fazleabas AT, Jaffe RC. Immunological characterization and immunohistochemical localization of a progesterone-dependent cat endometrial secretory protein. Biol Reprod 1989; 41:347-354.
30. Li WG, Jaffe RC, Fazleabas AT, Verhage HG. Progesterone-dependent cathepsin L proteolytic activity in cat uterine flushings. Biol Reprod 1991; 44:625-631.
31. Jokimaa V, Oksjoki S, Kujari H, Vuorio E, Anttila L. Expression patterns of cathepsins B, H, K, L and S in the human endometrium. Mol Hum Reprod 2001; 7:73-78.
32. Nakanishi T, Ozaki Y, Blomgren K, Tateyama H, Sugiura-Ogasawara M, Suzumori K. Role of cathepsins and cystatins in patients with recurrent miscarriage. Mol Hum Reprod 2005; 11:351-355.
33. Bazer FW, Thatcher WW. Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2a by the uterine endometrium. Prostaglandins 1977; 14: 397-400.
34. Frank M, Bazer FW, Thatcher WW, Wilcox CJ. A study of prostaglandin F2alpha as the luteolysin in swine: III. Effects of estradiol valerate on prostaglandin F, progestins, estrone and estradiol concentrations in the utero-ovarian vein of nonpregnant gilts. Prostaglandins 1977; 14:1183-1196.
35. Ziecik AJ, Waclawik A, Bogacki M. Conceptus signals for establishment and maintenance of pregnancy in pigs-lipid signaling system. Exp Clin Endocrinol Diabetes 2008; 116:443-449.
36. Geisert RD, Blair RM, Pratt T, Zavy MT. Characterization and proteolytic activity of a cathepsin L-like polypeptide in endometrium and uterine flushings of cycling, pregnant and steroid-treated ovariectomized gilts. Reprod Fertil Dev 1997; 9:395-402. (Pubitemid 27502142)
37. Jensen AR, Elnif J, Burrin DG, Sangild PT. Development of intestinal immunoglobulin absorption and enzyme activities in neonatal pigs is diet dependent. J Nutr 2001; 131:3259-3265. (Pubitemid 33136146)
38. Osenkowski P, Toth M, Fridman R. Processing, shedding, and endocytosis of membrane type 1-matrix metalloprotease (MT1-MMP). J Cell Physiol 2004; 200:2-10.
39. Song G, Dunlap KA, Kim J, Bailey DW, Spencer TE, Burghardt RC, Johnson GA, Bazer FW. Stanniocalcin 1 is a luminal epithelial marker for implantation in pigs regulated by progesterone and estrogen. Endocrinology 2009; 150:936-945.
40. Spencer TE, Ing NH, Ott TL, Mayes JS, Becker WC, Watson GH, Mirando MA, Bazer FW. Intrauterine injection of ovine interferon-tau alters oestrogen receptor and oxytocin receptor expression in the endometrium of cyclic ewes. J Mol Endocrinol 1995; 15:203-220.
41. Johnson GA, Spencer TE, Burghardt RC, Bazer FW. Ovine osteopontin: I. Cloning and expression of mRNA in the uterus during the periimplantation period. Biol Reprod 1999; 61:884-891.
42. Baker K, Qiao SW, Kuo T, Kobayashi K, Yoshida M, Lencer WI, Blumberg RS. Immune and non-immune functions of the (not so) neonatal Fc receptor, FcRn. Semin Immunopathol 2009; 31:223-236.
43. Salmon H, Berri M, Gerdts V, Meurens F. Humoral and cellular factors of maternal immunity in swine. Dev Comp Immunol 2009; 33:384-393.
44. Kukor Z, Mayerle J, Kruger B, Toth M, Steed PM, Halangk W, Lerch MM, Sahin-Toth M. Presence of cathepsin B in the human pancreatic secretory pathway and its role in trypsinogen activation during hereditary pancreatitis. J Biol Chem 2002; 277:21389-21396.
45. Jutras I, Reudelhuber TL. Prorenin processing by cathepsin B in vitro and in transfected cells. FEBS Lett 1999; 443:48-52.
46. Yasothornsrikul S, Greenbaum D, Medzihradszky KF, Toneff T, Bundey R, Miller R, Schilling B, Petermann I, Dehnert J, Logvinova A, Goldsmith P, Neveu JM, et al. Cathepsin L in secretory vesicles functions as a prohormone- processing enzyme for production of the enkephalin neuropeptide neurotransmitter. Proc Natl Acad Sci U S A 2003; 100: 9590-9595.
47. Funkelstein L, Toneff T, Hwang SR, Reinhekel T, Peters C, Hook V. Cathepsin L participates in the production of neuropeptide Y in secretory vesicles, demonstrated by protease gene knockout and expression. J Neurochem 2008; 106:384-391.
48. Biswas N, Rodriguez-Flores JL, Courel M, Gayen JR, Baingankar SM, Mahata M, Torpey JW, Taupenot L, O'Connor DT, Mahata SK. Cathepsin L co-localizes with chromogranin A in chromaffin vesicles to generate active peptides. Endocrinology 2009; 150:3547-3557.
49. Dempsey FW, Wislocki B, Amoroso EC. Electron microscopy of the pig's placenta, with especial reference to the cell membranes of the endometrium and chorion. Am J Anat 1955; 91:65-101.
50. Ducsay CA, Buhi WC, Bazer FW, Roberts RM, Combs GE. Role of uteroferrin in placental iron transport: effect of maternal iron treatment on fetal iron and uteroferrin content and neonatal hemoglobin. J Anim Sci 1984; 62:1303-1308.
51. Roberts RM, Raub TJ, Bazer FW. Role of uteroferrin in transplacental iron transport in the pig. Fed Proc 1986; 45:2513-2518. (Pubitemid 16020688)
52. Bazer FW, Worthington-White D, Fliss MFV, Gross S. Uteroferrin: a progesterone-induced hematopoietic growth factor of uterine origin. J Exp Hematol 1991; 19:910-915.
53. Bazer FW. Allantoic fluid: regulation of volume and composition. In: Brace RA (ed.), Fetal and Neonatal Body Fluids. Cornell: Perinatology Press; 1989:135-157.
54. Leary L Jr, Lecce JG. The preferential transport of immunoglobulin G by the small intestine of the neonatal piglet. J Nutr 1979; 109:458-466.
55. Butler JE, Sun J, Wertz N, Sinkora M. Antibody repertoire development in swine. Dev Comp Immunol 2006; 30:199-221.