Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
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Decorin: a multifunctional proteoglycan involved in oocyte maturation and trophoblast migration

  • Park, Beom Seok (Department of Biomedical Laboratory Science, College of Health Science, Eulji University) ;
  • Lee, Jaewang (Department of Biomedical Laboratory Science, College of Health Science, Eulji University) ;
  • Jun, Jin Hyun (Department of Biomedical Laboratory Science, College of Health Science, Eulji University)
  • Received : 2021.11.04
  • Accepted : 2021.11.15
  • Published : 2021.12.31
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Abstract

Decorin (DCN) is a proteoglycan belonging to the small leucine-rich proteoglycan family. It is composed of a protein core containing leucine repeats with a glycosaminoglycan chain consisting of either chondroitin sulfate or dermatan sulfate. DCN is a structural component of connective tissues that can bind to type I collagen. It plays a role in the assembly of the extracellular matrix (ECM), and it is related to fibrillogenesis. It can interact with fibronectin, thrombospondin, complement component C1, transforming growth factor (TGF), and epidermal growth factor receptor. Normal DCN expression regulates a wide range of cellular processes, including proliferation, migration, apoptosis, and autophagy, through interactions with various molecules. However, its aberrant expression is associated with oocyte maturation, oocyte quality, and poor extravillous trophoblast invasion of the uterus, which underlies the occurrence of preeclampsia and intrauterine growth restriction. Spatiotemporal hormonal control of successful pregnancy should regulate the concentration and activity of specific proteins such as proteoglycan participating in the ECM remodeling of trophoblastic and uterine cells in fetal membranes and uterus. At the human feto-maternal interface, TGF-β and DCN play crucial roles in the regulation of trophoblast invasion of the uterus. This review summarizes the role of the proteoglycan DCN as an important and multifunctional molecule in the physiological regulation of oocyte maturation and trophoblast migration. This review also shows that recombinant DCN proteins might be useful for substantiating diverse functions in both animal and in vitro models of oogenesis and implantation.

Keywords

Acknowledgement

We thank Ho min Kim (from the IBS and KAIST) for his help with protein expression.

References

  1. Iozzo RV, Schaefer L. Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol 2015;42:11-55. https://doi.org/10.1016/j.matbio.2015.02.003
  2. Scott PG, McEwan PA, Dodd CM, Bergmann EM, Bishop PN, Bella J. Crystal structure of the dimeric protein core of decorin, the archetypal small leucine-rich repeat proteoglycan. Proc Natl Acad Sci U S A 2004;101:15633-8. https://doi.org/10.1073/pnas.0402976101
  3. Park BS, Lee JO. Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp Mol Med 2013;45:e66. https://doi.org/10.1038/emm.2013.97
  4. Halari CD, Zheng M, Lala PK. Roles of two small leucine-rich proteoglycans decorin and biglycan in pregnancy and pregnancy-associated diseases. Int J Mol Sci 2021;22:10584. https://doi.org/10.3390/ijms221910584
  5. Kajava AV. Structural diversity of leucine-rich repeat proteins. J Mol Biol 1998;277:519-27. https://doi.org/10.1006/jmbi.1998.1643
  6. Jin MS, Lee JO. Application of hybrid LRR technique to protein crystallization. BMB Rep 2008;41:353-7. https://doi.org/10.5483/BMBRep.2008.41.5.353
  7. Park BS, Won SY, Lee DS, Kim HM. Human leucine-rich-alpha-2-glycoprotein1: purification, crystallization, and X-ray crystallographic analysis. Biodesign 2020;8:60-3. https://doi.org/10.34184/kssb.2020.8.3.60
  8. Franczyk M, Wawrzykowski J, Kankofer M. Preliminary results of the placental decorin profile in bovine pregnancy and parturition. Glycoconj J 2018;35:461-5. https://doi.org/10.1007/s10719-018-9834-7
  9. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 1997;136:729-43. https://doi.org/10.1083/jcb.136.3.729
  10. Wang Y, Zhang H, Zhang Y, Li X, Hu X, Wang X. Decorin promotes apoptosis and autophagy via suppressing c-Met in HTR-8 trophoblasts. Reproduction 2020;159:669-77. https://doi.org/10.1530/REP-19-0458
  11. Jamiol M, Wawrzykowski J, Kankofer M. The influence of progesterone and prostaglandin F2α on decorin and the adhesion of caruncular epithelial cells of bovine placenta at early-mid pregnancy-Part II. Reprod Domest Anim 2021;56:1040-9. https://doi.org/10.1111/rda.13948
  12. Ricciardelli C, Rodgers RJ. Extracellular matrix of ovarian tumors. Semin Reprod Med 2006;24:270-82. https://doi.org/10.1055/s-2006-948556
  13. Grisaru D, Hauspy J, Prasad M, Albert M, Murphy KJ, Covens A, et al. Microarray expression identification of differentially expressed genes in serous epithelial ovarian cancer compared with bulk normal ovarian tissue and ovarian surface scrapings. Oncol Rep 2007;18:1347-56.
  14. Santra M, Reed CC, Iozzo RV. Decorin binds to a narrow region of the epidermal growth factor (EGF) receptor, partially overlapping but distinct from the EGF-binding epitope. J Biol Chem 2002;277:35671-81. https://doi.org/10.1074/jbc.M205317200
  15. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004;303:682-4. https://doi.org/10.1126/science.1092463
  16. Ben-Ami I, Freimann S, Armon L, Dantes A, Strassburger D, Friedler S, et al. PGE2 up-regulates EGF-like growth factor biosynthesis in human granulosa cells: new insights into the coordination between PGE2 and LH in ovulation. Mol Hum Reprod 2006;12:593-9. https://doi.org/10.1093/molehr/gal068
  17. Iozzo RV, Schaefer L. Proteoglycans in health and disease: novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans. FEBS J 2010;277:3864-75. https://doi.org/10.1111/j.1742-4658.2010.07797.x
  18. Csordas G, Santra M, Reed CC, Eichstetter I, McQuillan DJ, Gross D, et al. Sustained down-regulation of the epidermal growth factor receptor by decorin: a mechanism for controlling tumor growth in vivo. J Biol Chem 2000;275:32879-87. https://doi.org/10.1074/jbc.M005609200
  19. Zhu JX, Goldoni S, Bix G, Owens RT, McQuillan DJ, Reed CC, et al. Decorin evokes protracted internalization and degradation of the epidermal growth factor receptor via caveolar endocytosis. J Biol Chem 2005;280:32468-79. https://doi.org/10.1074/jbc.M503833200
  20. Adam M, Schwarzer JU, Kohn FM, Strauss L, Poutanen M, Mayerhofer A. Mast cell tryptase stimulates production of decorin by human testicular peritubular cells: possible role of decorin in male infertility by interfering with growth factor signaling. Hum Reprod 2011;26:2613-25. https://doi.org/10.1093/humrep/der245
  21. Iozzo RV, Moscatello DK, McQuillan DJ, Eichstetter I. Decorin is a biological ligand for the epidermal growth factor receptor. J Biol Chem 1999;274:4489-92. https://doi.org/10.1074/jbc.274.8.4489
  22. Ben-Ami I, Freimann S, Armon L, Dantes A, Ron-El R, Amsterdam A. Novel function of ovarian growth factors: combined studies by DNA microarray, biochemical and physiological approaches. Mol Hum Reprod 2006;12:413-9. https://doi.org/10.1093/molehr/gal045
  23. Yu Y, Yan J, Li M, Yan L, Zhao Y, Lian Y, et al. Effects of combined epidermal growth factor, brain-derived neurotrophic factor and insulin-like growth factor-1 on human oocyte maturation and early fertilized and cloned embryo development. Hum Reprod 2012;27:2146-59. https://doi.org/10.1093/humrep/des099
  24. Adam M, Saller S, Strobl S, Hennebold JD, Dissen GA, Ojeda SR, et al. Decorin is a part of the ovarian extracellular matrix in primates and may act as a signaling molecule. Hum Reprod 2012;27:3249-58. https://doi.org/10.1093/humrep/des297
  25. Peng JY, Gao KX, Xin HY, Han P, Zhu GQ, Cao BY. Molecular cloning, expression analysis, and function of decorin in goat ovarian granulosa cells. Domest Anim Endocrinol 2016;57:108-16. https://doi.org/10.1016/j.domaniend.2016.05.006
  26. Kedem A, Ulanenko-Shenkar K, Yung Y, Yerushalmi GM, Maman E, Hourvitz A. Elucidating Decorin's role in the preovulatory follicle. J Ovarian Res 2020;13:15. https://doi.org/10.1186/s13048-020-0612-3
  27. Richards H, Murley C, Poat JA, Munday KA. Proceedings: studies on levels of angiotensin II in the circulation of the rat. J Endocrinol 1976;68:11-2.
  28. Maman E, Yung Y, Kedem A, Yerushalmi GM, Konopnicki S, Cohen B, et al. High expression of luteinizing hormone receptors messenger RNA by human cumulus granulosa cells is in correlation with decreased fertilization. Fertil Steril 2012;97:592-8. https://doi.org/10.1016/j.fertnstert.2011.12.027
  29. Yung Y, Aviel-Ronen S, Maman E, Rubinstein N, Avivi C, Orvieto R, et al. Localization of luteinizing hormone receptor protein in the human ovary. Mol Hum Reprod 2014;20:844-9. https://doi.org/10.1093/molehr/gau041
  30. Sawada Y, Sato T, Saito C, Ozawa F, Ozaki Y, Sugiura-Ogasawara M. Clinical utility of decorin in follicular fluid as a biomarker of oocyte potential. Reprod Biol 2018;18:33-9. https://doi.org/10.1016/j.repbio.2017.12.001
  31. Wu Z, Aron AW, Macksoud EE, Iozzo RV, Hai CM, Lechner BE. Uterine dysfunction in biglycan and decorin deficient mice leads to dystocia during parturition. PLoS One 2012;7:e29627. https://doi.org/10.1371/journal.pone.0029627
  32. Lysiak JJ, Hunt J, Pringle GA, Lala PK. Localization of transforming growth factor beta and its natural inhibitor decorin in the human placenta and decidua throughout gestation. Placenta 1995;16:221-31. https://doi.org/10.1016/0143-4004(95)90110-8
  33. Xu G, Guimond MJ, Chakraborty C, Lala PK. Control of proliferation, migration, and invasiveness of human extravillous trophoblast by decorin, a decidual product. Biol Reprod 2002;67:681-9. https://doi.org/10.1095/biolreprod67.2.681
  34. Gellersen B, Briese J, Oberndorfer M, Redlin K, Samalecos A, Richter DU, et al. Expression of the metastasis suppressor KAI1 in decidual cells at the human maternal-fetal interface: regulation and functional implications. Am J Pathol 2007;170:126-39. https://doi.org/10.2353/ajpath.2007.060175
  35. Nandi P, Siddiqui MF, Lala PK. Restraint of trophoblast invasion of the uterus by decorin: role in pre-eclampsia. Am J Reprod Immunol 2016;75:351-60. https://doi.org/10.1111/aji.12449
  36. Siddiqui MF, Nandi P, Girish GV, Nygard K, Eastabrook G, de Vrijer B, et al. Decorin over-expression by decidual cells in preeclampsia: a potential blood biomarker. Am J Obstet Gynecol 2016;215:361. e1-361.e15.
  37. Halari CD, Nandi P, Jeyarajah MJ, Renaud SJ, Lala PK. Decorin production by the human decidua: role in decidual cell maturation. Mol Hum Reprod 2020;26:784-96. https://doi.org/10.1093/molehr/gaaa058