Browse > Article
http://dx.doi.org/10.5653/cerm.2017.44.2.63

N-glycoproteomic analysis of human follicular fluid during natural and stimulated cycles in patients undergoing in vitro fertilization  

Lim, Hee-Joung (Forensic Science R&D Lab, Police Science Institute)
Seok, Ae Eun (Laboratory of Signal Transduction and Disease Biomarker Discovery, Department of Senior Healthcare, BK21 Plus Program, Graduate School, Eulji University)
Han, Jiyou (Department of Biological Sciences, Laboratory of Stem Cell Research and Biotechnology, Hyupsung University)
Lee, Jiyeong (Department of Biomedical Laboratory Science, College of Health Sciences, Eulji University)
Lee, Sungeun (Research Institute of DONGDEOK Pharmaceutical)
Kang, Hee-Gyoo (Laboratory of Signal Transduction and Disease Biomarker Discovery, Department of Senior Healthcare, BK21 Plus Program, Graduate School, Eulji University)
Cha, Byung Heun (Department of Biomedical Laboratory Science, College of Health Sciences, Eulji University)
Yang, Yunseok (Department of Obstetrics and Gynecology, Eulji University Hospital)
Publication Information
Clinical and Experimental Reproductive Medicine / v.44, no.2, 2017 , pp. 63-72 More about this Journal
Abstract
Objective: Hyperstimulation methods are broadly used for in vitro fertilization (IVF) in patients with infertility; however, the side effects associated with these therapies, such as ovarian hyperstimulation syndrome (OHSS), have not been well studied. N-glycoproteomes are subproteomes used for the remote sensing of ovarian stimulation in follicular growth. Glycoproteomic variation in human follicular fluid (hFF) has not been evaluated. In this study, we aimed to identify and quantify the glycoproteomes and N-glycoproteins (N-GPs) in natural and stimulated hFF using label-free nano-liquid chromatography/electrospray ionization-quad time-of-flight mass spectrometry. Methods: For profiling of the total proteome and glycoproteome, pooled protein samples from natural and stimulated hFF samples were selectively isolated using hydrazide chemistry to obtain the total proteomes and glycoproteomes. N-GPs were validated by the consensus sequence N-X-S/T (92.2% specificity for the N-glycomotif at p<0.05). All data were compared between natural versus hyperstimulated hFF samples. Results: We detected 41 and 44 N-GPs in the natural and stimulated hFF samples, respectively. Importantly, we identified 11 N-GPs with greater than two-fold upregulation in stimulated hFF samples compared to natural hFF samples. We also validated the novel N-GPs thyroxine-binding globulin, vitamin D-binding protein, and complement proteins C3 and C9. Conclusion: We identified and classified N-GPs in hFF to improve our understanding of follicular physiology in patients requiring assisted reproduction. Our results provided important insights into the prevention of hyperstimulation side effects, such as OHSS.
Keywords
Fertilization in vitro; Human follicular fluid; Hyper stimulation; N-glycoprotein; Natural cycle; Proteomics;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Ducolomb Y, Gonzalez-Marquez H, Fierro R, Jimenez I, Casas E, Flores D, et al. Effect of porcine follicular fluid proteins and peptides on oocyte maturation and their subsequent effect on in vitro fertilization. Theriogenology 2013;79:896-904.   DOI
2 Estes SJ, Ye B, Qiu W, Cramer D, Hornstein MD, Missmer SA. A proteomic analysis of IVF follicular fluid in women   DOI
3 Ferrero S, Gillott DJ, Remorgida V, Anserini P, Ragni N, Grudzinskas JG. Proteomic analysis of peritoneal fluid in fertile and infertile women with endometriosis. J Reprod Med 2009;54:32-40.
4 Jarkovska K, Martinkova J, Liskova L, Halada P, Moos J, Rezabek K, et al. Proteome mining of human follicular fluid reveals a crucial role of complement cascade and key biological pathways in women undergoing in vitro fertilization. J Proteome Res 2010;9: 1289-301.   DOI
5 Georgiou AS, Sostaric E, Wong CH, Snijders AP, Wright PC, Moore HD, et al. Gametes alter the oviductal secretory proteome. Mol Cell Proteomics 2005;4:1785-96.   DOI
6 Curry TE Jr, Dean DD, Sanders SL, Pedigo NG, Jones PB. The role of ovarian proteases and their inhibitors in ovulation. Steroids 1989;54:501-21.   DOI
7 Yokota K, Hirano T, Urata N, Yamauchi N, Hattori MA. Upregulation of P-glycoprotein activity in porcine oocytes and granulosa cells during in vitro maturation. J Reprod Dev 2011;57:322-6.   DOI
8 Clark GF. Functional glycosylation in the human and mammalian uterus. Fertil Res Pract 2015;1:17.   DOI
9 Daikoku T, Tranguch S, Friedman DB, Das SK, Smith DF, Dey SK. Proteomic analysis identifies immunophilin FK506 binding protein 4 (FKBP52) as a downstream target of Hoxa10 in the periimplantation mouse uterus. Mol Endocrinol 2005;19:683-97.   DOI
10 Aitken RJ, Nixon B, Lin M, Koppers AJ, Lee YH, Baker MA. Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl 2007;9:554-64.   DOI
11 Peddinti D, Nanduri B, Kaya A, Feugang JM, Burgess SC, Memili E. Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Syst Biol 2008;2:19.   DOI
12 Yoon SJ, Rahman MS, Kwon WS, Ryu DY, Park YJ, Pang MG. Proteomic identification of cryostress in epididymal spermatozoa. J Anim Sci Biotechnol 2016;7:67.   DOI
13 Bedaiwy M, Shahin AY, AbulHassan AM, Goldberg JM, Sharma RK, Agarwal A, et al. Differential expression of follicular fluid cytokines: relationship to subsequent pregnancy in IVF cycles. Reprod Biomed Online 2007;15:321-5.   DOI
14 Spitzer D, Murach KF, Lottspeich F, Staudach A, Illmensee K. Different protein patterns derived from follicular fluid of mature and immature human follicles. Hum Reprod 1996;11:798-807.   DOI
15 Anderson NL, Anderson NG. Proteome and proteomics: new technologies, new concepts, and new words. Electrophoresis 1998;19:1853-61.   DOI
16 Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics 2002;1:845-67.   DOI
17 Hanrieder J, Nyakas A, Naessen T, Bergquist J. Proteomic analysis of human follicular fluid using an alternative bottom-up approach. J Proteome Res 2008;7:443-9.   DOI
18 Wujek P, Kida E, Walus M, Wisniewski KE, Golabek AA. N-glycosylation is crucial for folding, trafficking, and stability of human tripeptidyl- peptidase I. J Biol Chem 2004;279:12827-39.   DOI
19 Lee HC, Lee SW, Lee KW, Lee SW, Cha KY, Kim KH, et al. Identification of new proteins in follicular fluid from mature human follicles by direct sample rehydration method of two-dimensional polyacrylamide gel electrophoresis. J Korean Med Sci 2005;20: 456-60.   DOI
20 Hughes SC, Mason HD, Franks S, Holly JM. The insulin-like growth factors (IGFs) in follicular fluid are predominantly bound in the ternary complex. J Endocrinol 1997;155:R1-4.   DOI
21 Schweigert FJ, Gericke B, Wolfram W, Kaisers U, Dudenhausen JW. Peptide and protein profiles in serum and follicular fluid of women undergoing IVF. Hum Reprod 2006;21:2960-8.   DOI
22 Ceciliani F, Giordano A, Spagnolo V. The systemic reaction during inflammation: the acute-phase proteins. Protein Pept Lett 2002; 9:211-23.   DOI
23 de Boer JP, Creasey AA, Chang A, Abbink JJ, Roem D, Eerenberg AJ, et al. Alpha-2-macroglobulin functions as an inhibitor of fibrinolytic, clotting, and neutrophilic proteinases in sepsis: studies using a baboon model. Infect Immun 1993;61:5035-43.
24 Tse JY, Chiu PC, Lee KF, Seppala M, Koistinen H, Koistinen R, et al. The synthesis and fate of glycodelin in human ovary during folliculogenesis. Mol Hum Reprod 2002;8:142-8.   DOI
25 Agrawal R, Sladkevicius P, Engmann L, Conway GS, Payne NN, Bekis J, et al. Serum vascular endothelial growth factor concentrations and ovarian stromal blood flow are increased in women with polycystic ovaries. Hum Reprod 1998;13:651-5.   DOI
26 Bora NS, Kaliappan S, Jha P, Xu Q, Sohn JH, Dhaulakhandi DB, et al. Complement activation via alternative pathway is critical in the development of laser-induced choroidal neovascularization: role of factor B and factor H. J Immunol 2006;177:1872-8.   DOI
27 Girardi G, Yarilin D, Thurman JM, Holers VM, Salmon JE. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med 2006;203:2165-75.   DOI
28 Nozaki M, Raisler BJ, Sakurai E, Sarma JV, Barnum SR, Lambris JD, et al. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci U S A 2006;103: 2328-33.   DOI
29 Dai G, Lu G. Different protein expression patterns associated with polycystic ovary syndrome in human follicular fluid during controlled ovarian hyperstimulation. Reprod Fertil Dev 2012;24: 893-904.   DOI
30 Das T, Chattopadhyay R, Ghosh S, Goswami S, Chattopadhyay D, Chakravarty B, et al. Role of an estrogen-upregulated 64.0-kDa uterine fluid glycoprotein in improving fertility in women. Fertil Steril 2007;87:343-50.   DOI
31 Kim YS, Kim MS, Lee SH, Choi BC, Lim JM, Cha KY, et al. Proteomic analysis of recurrent spontaneous abortion: identification of an inadequately expressed set of proteins in human follicular fluid. Proteomics 2006;6:3445-54.   DOI
32 Larsen MR, Jensen SS, Jakobsen LA, Heegaard NH. Exploring the sialiome using titanium dioxide chromatography and mass spectrometry. Mol Cell Proteomics 2007;6:1778-87.   DOI
33 Jarkovska K, Kupcova Skalnikova H, Halada P, Hrabakova R, Moos J, Rezabek K, et al. Development of ovarian hyperstimulation syndrome: interrogation of key proteins and biological processes in human follicular fluid of women undergoing in vitro fertilization. Mol Hum Reprod 2011;17:679-92.   DOI
34 Wu R, Van der Hoek KH, Ryan NK, Norman RJ, Robker RL. Macrophage contributions to ovarian function. Hum Reprod Update 2004;10:119-33.   DOI
35 Kruger AJ, Yang C, Tam SW, Hinerfeld D, Evans JE, Green KM, et al. Haptoglobin as an early serum biomarker of virus-induced autoimmune type 1 diabetes in biobreeding diabetes resistant and LEW1.WR1 rats. Exp Biol Med (Maywood) 2010;235:1328-37.   DOI
36 Wollscheid B, Bausch-Fluck D, Henderson C, O'Brien R, Bibel M, Schiess R, et al. Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat Biotechnol 2009;27:378-86.   DOI
37 Echan LA, Tang HY, Ali-Khan N, Lee K, Speicher DW. Depletion of multiple high-abundance proteins improves protein profiling capacities of human serum and plasma. Proteomics 2005;5: 3292-303.   DOI
38 Fortune JE. Ovarian follicular growth and development in mammals. Biol Reprod 1994;50:225-32.   DOI
39 Nayudu PL, Lopata A, Jones GM, Gook DA, Bourne HM, Sheather SJ, et al. An analysis of human oocytes and follicles from stimulated cycles: oocyte morphology and associated follicular fluid characteristics. Hum Reprod 1989;4:558-67.   DOI
40 Kuo MW, Wang CH, Wu HC, Chang SJ, Chuang YJ. Soluble THSD7A is an N-glycoprotein that promotes endothelial cell migration and tube formation in angiogenesis. PLoS One 2011;6: e29000.   DOI
41 Tahboub R, Arafah BM. Sex steroids and the thyroid. Best Pract Res Clin Endocrinol Metab 2009;23:769-80.   DOI
42 Poppe K, Velkeniers B, Glinoer D. The role of thyroid autoimmunity in fertility and pregnancy. Nat Clin Pract Endocrinol Metab 2008;4:394-405.   DOI
43 Stuckey BG, Yeap D, Turner SR. Thyroxine replacement during super-ovulation for in vitro fertilization: a potential gap in management? Fertil Steril 2010;93:2414.e1-3.
44 Lee S, Kang DW, Hudgins-Spivey S, Krust A, Lee EY, Koo Y, et al. Theca-specific estrogen receptor-alpha knockout mice lose fertility prematurely. Endocrinology 2009;150:3855-62.   DOI
45 Schepeler T, Mansilla F, Christensen LL, Orntoft TF, Andersen CL. Clusterin expression can be modulated by changes in TCF1-mediated Wnt signaling. J Mol Signal 2007;2:6.   DOI
46 Cooke NE, David EV. Serum vitamin D-binding protein is a third member of the albumin and alpha fetoprotein gene family. J Clin Invest 1985;76:2420-4.   DOI
47 Nielsen HK, Brixen K, Bouillon R, Mosekilde L. Changes in biochemical markers of osteoblastic activity during the menstrual cycle. J Clin Endocrinol Metab 1990;70:1431-7.   DOI
48 Kushner I. The acute phase response: an overview. Methods Enzymol 1988;163:373-83.
49 Orvieto R, Zagatsky I, Yulzari-Roll V, La Marca A, Fisch B. Substituting human chorionic gonadotropin by gonadotropin-releasing hormone agonist to trigger final follicular maturation, during controlled ovarian hyperstimulation, results in less systemic inflammation. Gynecol Endocrinol 2006;22:437-40.   DOI
50 Orvieto R. Controlled ovarian hyperstimulation: an inflammatory state. J Soc Gynecol Investig 2004;11:424-6.   DOI
51 Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P. Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod Biol Endocrinol 2009;7:40.   DOI
52 Ferrara N. Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am J Physiol Cell Physiol 2001;280:C1358-66.   DOI
53 Fukuda R, Hirota K, Fan F, Jung YD, Ellis LM, Semenza GL. Insulinlike growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J Biol Chem 2002;277:38205-11.   DOI
54 MacDougall MJ, Tan SL, Balen A, Jacobs HS. A controlled study comparing patients with and without polycystic ovaries undergoing in-vitro fertilization. Hum Reprod 1993;8:233-7.   DOI
55 Nelson SM, Lawlor DA. Predicting live birth, preterm delivery, and low birth weight in infants born from in vitro fertilisation: a prospective study of 144,018 treatment cycles. PLoS Med 2011; 8:e1000386.   DOI
56 Dumesic DA, Meldrum DR, Katz-Jaffe MG, Krisher RL, Schoolcraft WB. Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil Steril 2015;103:303-16.   DOI
57 Schenker JG, Weinstein D. Ovarian hyperstimulation syndrome: a current survey. Fertil Steril 1978;30:255-68.   DOI
58 Angelucci S, Ciavardelli D, Di Giuseppe F, Eleuterio E, Sulpizio M, Tiboni GM, et al. Proteome analysis of human follicular fluid. Biochim Biophys Acta 2006;1764:1775-85.   DOI
59 Atiomo W, Khalid S, Parameshweran S, Houda M, Layfield R. Proteomic biomarkers for the diagnosis and risk stratification of polycystic ovary syndrome: a systematic review. BJOG 2009;116: 137-43.   DOI