Advanced High-Coverage Targeted Metabolomics Method (SWATHtoMRM) for Exploring the Relationship of Follicular Fluid Components with Age

Author(s): Jingyan Song, Tianqi Wang, Jiayin Guo, Ying Guo, Xiaoming Wang, Yi Yang, Kaiyue Xu, Yuanhong Sa, Lihua Yuan, Huaying Jiang, Zhengao Sun*.

Journal Name: Current Pharmaceutical Analysis

Volume 16 , Issue 3 , 2020

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Graphical Abstract:


Abstract:

Background: The complexity of follicular fluid metabolome presents a huge challenge for qualitative and quantitative metabolite profiling and discovery of the comprehensive biomarkers.

Objective: In order to address this challenge, novel SWATHtoMRM metabolomics method was used for providing broad coverage and excellent quantitative capability to discover the human follicular fluid metabolites related to age and evaluate their relationship with pregnancy outcome and oocyte senescence.

Methods: The patients were divided into four groups according to age, including group A (28 cases, 21- 27 years old), group B (42 cases, 28-34 years old), group C (31 cases, 35-41 years old), and group D (24 cases, 42-48 years old). Follicular fluid samples from 125 IVF patients were analyzed. The differential ions among the four groups were identified by principal components analysis according to accurate mass, isotope ratio, and tandem mass spectroscopic spectra. Then, the differential metabolic pathways were further identified by a KEGG cluster analysis.

Results: A total of 18 metabolites in the follicular fluid differed among the four groups, including amino acids, lipids, hormones, and vitamins. A total of 15 metabolites, including 6-oxohexanoate, phenylalanine, proline, hexadecanoic acid, linoleate, arachidonate, oleic acid, docosahexaenoic acid, LysoPC(16:1), LysoPC(20:5), LysoPC (20:3), 25-hydroxyvitamin D3, 5-dehydroepisterol, 27- hydroxycholesterol, and 5beta-cholestane-3alpha,7alpha,12alpha,23,25-pentol, were down-regulated with age and 3 metabolites, including LysoPC(18:3), LysoPC(18:1), and 13,14-dihydroretinol, were upregulated with age.

Conclusion: Our study provides useful information for revealing the relationship between age and female reproductive capability.

Keywords: Follicular fluid, metabolomics, age, reproductive function, SWATH to MRM, UPLC-QTOF.

[1]
Chen, J.; Chen, X.H. Kong, Wei. Comparison of three different controlled ovarian hyper stimulation protocols on IVF outcome in patients with different antral follicles number; Progress in Obstetrics & Gynecology, 2013.
[2]
Sun, Z.G.; Wu, H.C.; Lian, F.; Zhang, X.X.; Pang, C.H.; Guo, Y.; Song, J.Y.; Wang, A.J.; Shi, L.; Han, L.T. Human follicular fluid metabolomics study of follicular development and oocyte quality. Chromatographia, 2017, 80, 901-909.
[http://dx.doi.org/10.1007/s10337-017-3290-6]
[3]
Csemiczky, G.; Wramsby, H.; Johannisson, E.; Landgren, B.M. Importance of endometrial quality in women with tubal infertility during a natural menstrual cycle for the outcome of IVF treatment. J. Assist. Reprod. Genet., 1998, 15(2), 55-61.
[http://dx.doi.org/10.1007/BF02766825] [PMID: 9513841]
[4]
Dagan, W.; Kulvinder, K.; Jamie, G.; Michael, G.; Jenny, C.T.; Elpida, F.; Santiago, M. Clinical utilization of a rapid low-pass whole genome sequencing technique for the diagnosis of aneuploidy in human embryos prior to implantation. 2014, 51, 553-562.
[5]
Chen, Y.; Huang, W.X. Clinical study on pregnant women with IgA nephropathy in a hospital in recent 10 years. Chinese Journal of Woman and Child Health Research, 2017, 6, 741-743.
[6]
Want, E.J.; Wilson, I.D.; Gika, H.; Theodoridis, G.; Plumb, R.S.; Shockcor, J.; Holmes, E.; Nicholson, J.K. Global metabolic profiling procedures for urine using UPLC-MS. Nat. Protoc., 2010, 5(6), 1005-1018.
[http://dx.doi.org/10.1038/nprot.2010.50] [PMID: 20448546]
[7]
Siddiqui, M.R.; Alothman, Z.A.; Rahman, N. Analytical techniques in pharmaceutical analysis: A review. Arab. J. Chem., 2017, 10, 1409-1421.
[http://dx.doi.org/10.1016/j.arabjc.2013.04.016]
[8]
Alothman, Z.A.; Rahman, N.; Siddiqui, M.R. Review on pharmaceutical impurities stability studies and degradation products. Rev. Adv. Sci. Eng., 2013, 2, 155-166.
[http://dx.doi.org/10.1166/rase.2013.1039]
[9]
Patti, G.J.; Yanes, O.; Siuzdak, G. Innovation: Metabolomics: the apogee of the omics trilogy. Nat. Rev. Mol. Cell Biol., 2012, 13(4), 263-269.
[http://dx.doi.org/10.1038/nrm3314] [PMID: 22436749]
[10]
Cajka, T.; Fiehn, O. Toward merging untargeted and target methods in mass spectrometry-based metabolomics and lipidomics. Anal. Chem., 2016, 88(1), 524-545.
[http://dx.doi.org/10.1021/acs.analchem.5b04491] [PMID: 26637011]
[11]
Tanaka, T.; Tsutsui, H.; Hirano, K.; Koike, T.; Tokumura, A.; Satouchi, K. Quantitative analysis of lysophosphatidic acid by time-of-flight mass spectrometry using a phosphate-capture molecule. J. Lipid Res., 2004, 45(11), 2145-2150.
[http://dx.doi.org/10.1194/jlr.D400010-JLR200] [PMID: 15314093]
[12]
Kushnir, M.M.; Rockwood, A.L.; Bergquist, J. Liquid chromatography-tandem mass spectrometry applications in endocrinology. Mass Spectrom. Rev., 2010, 29(3), 480-502.
[http://dx.doi.org/10.1002/mas.20264] [PMID: 19708015]
[13]
Sun, Y.; Jia, P.; Yuan, L.; Liu, Y.; Zhang, Z.; Du, Y.; Zhang, L. Investigating the in vitro stereoselective metabolism of m-nisoldipine enantiomers: characterization of metabolites and cytochrome P450 isoforms involved. Biomed. Chromatogr., 2015, 29(12), 1893-1900.
[http://dx.doi.org/10.1002/bmc.3512] [PMID: 25994315]
[14]
Liu, M.; Zhao, S.; Wang, Z.; Wang, Y.; Liu, T.; Li, S.; Wang, C.; Wang, H.; Tu, P. Identification of metabolites of deoxyschizandrin in rats by UPLC-Q-TOF-MS/MS based on multiple mass defect filter data acquisition and multiple data processing techniques. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2014, 949-950, 115-126.
[http://dx.doi.org/10.1016/j.jchromb.2013.12.022] [PMID: 24487041]
[15]
Xie, W.W.; Jin, Y.R.; Hou, L.D.; Ma, Y.H.; Xu, H.J.; Zhang, K.R.; Zhang, L.T.; Du, Y.F. A practical strategy for the characterization of ponicidin metabolites in vivo and in vitro by UHPLC-Q-TOF-MS based on nontargeted SWATH data acquisition. J. of Pharm. and Biomed. Anal., 2017, 145, 865-878.
[16]
Zhou, J.; Yin, Y. Strategies for large-scale targeted metabolomics quantification by liquid chromatography-mass spectrometry. Analyst (Lond.), 2016, 141, 6362-6373.
[17]
Griffiths, W.J.; Koal, T.; Wang, Y.; Kohl, M.; Enot, D.P.; Deigner, H.P. Targeted metabolomics for biomarker discovery. Angew. Chem. Int. Ed. Engl., 2010, 49(32), 5426-5445.
[http://dx.doi.org/10.1002/anie.200905579] [PMID: 20629054]
[18]
Lacorte, S.; Fernandez-Alba, A.R. Time of flight mass spectrometry applied to the liquid chromatographic analysis of pesticides in water and food. Mass Spectrom. Rev., 2006, 25(6), 866-880.
[http://dx.doi.org/10.1002/mas.20094] [PMID: 16752429]
[19]
Carrel, D.; Hamon, M.; Darmon, M. Role of the C-terminal di-leucine motif of 5-HT1A and 5-HT1B serotonin receptors in plasma membrane targeting. J. Cell Sci., 2006, 119(Pt 20), 4276-4284.
[http://dx.doi.org/10.1242/jcs.03189] [PMID: 17003106]
[20]
Díaz-Bello, B.; Rangel-García, C.I.; Salvador, C.; Carrisoza-Gaytán, R.; Escobar, L.I. The polarization of the G-protein activated potassium channel GIRK5 to the vegetal pole of Xenopus laevis oocytes is driven by a di-leucine motif. PLoS One, 2013, 8(5) e64096
[http://dx.doi.org/10.1371/journal.pone.0064096] [PMID: 23717539]
[21]
Pacella, L.; Zander-Fox, D.L.; Armstrong, D.T.; Lane, M. Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment. Fertil. Steril., 2012, 98(4), 986-94.e1, 2.
[http://dx.doi.org/10.1016/j.fertnstert.2012.06.025] [PMID: 22818290]
[22]
Westendorf, J.M.; Rao, P.N.; Gerace, L. Cloning of cDNAs for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated epitope. Proc. Natl. Acad. Sci. USA, 1994, 91(2), 714-718.
[http://dx.doi.org/10.1073/pnas.91.2.714] [PMID: 8290587]
[23]
Aardema, H.; Vos, P.L.A.M.; Lolicato, F.; Roelen, B.A.J.; Knijn, H.M.; Vaandrager, A.B.; Helms, J.B.; Gadella, B.M. Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol. Reprod., 2011, 85(1), 62-69.
[http://dx.doi.org/10.1095/biolreprod.110.088815] [PMID: 21311036]
[24]
Siriwardhana, N.; Kalupahana, N.S.; Moustaid-Moussa, N. Health benefits of n-3 polyunsaturated fatty acids: eicosapentaenoic acid and docosahexaenoic acid. Adv. Food Nutr. Res., 2012, 65, 211-222.
[http://dx.doi.org/10.1016/B978-0-12-416003-3.00013-5] [PMID: 22361189]
[25]
Hashidateyoshida, T.; Harayama, T.; Hishikawa, D.; Morimoto, R.; Hamano, F.; Shimizu, T. Fatty acid remodeling by LPCAT3 enriches arachidonate in phospholipid membranes and regulates triglyceride transport 2015, 4 e06328
[26]
Kakisaka, K.; Cazanave, S.C.; Fingas, C.D.; Guicciardi, M.E.; Bronk, S.F.; Werneburg, N.W.; Mott, J.L.; Gores, G.J. Mechanisms of lysophosphatidylcholine-induced hepatocyte lipoapoptosis. Am. J. Physiol. Gastrointest. Liver Physiol., 2012, 302(1), G77-G84.
[http://dx.doi.org/10.1152/ajpgi.00301.2011] [PMID: 21995961]
[27]
Akazawa, Y.; Cazanave, S.; Mott, J.L.; Elmi, N.; Bronk, S.F.; Kohno, S.; Charlton, M.R.; Gores, G.J. Palmitoleate attenuates palmitate-induced Bim and PUMA up-regulation and hepatocyte lipoapoptosis. J. Hepatol., 2010, 52(4), 586-593.
[http://dx.doi.org/10.1016/j.jhep.2010.01.003] [PMID: 20206402]
[28]
Ibrahim, S.H.; Gores, G.J. Who pulls the trigger: JNK activation in liver lipotoxicity? J. Hepatol., 2012, 56(1), 17-19.
[http://dx.doi.org/10.1016/j.jhep.2011.04.017] [PMID: 21703172]
[29]
Georges, A.; L’Hôte, D.; Todeschini, A.L.; Auguste, A.; Legois, B.; Zider, A.; Veitia, R.A. The transcription factor FOXL2 mobilizes estrogen signaling to maintain the identity of ovarian granulosa cells. eLife, 2014, 3, 3.
[http://dx.doi.org/10.7554/eLife.04207] [PMID: 25369636]
[30]
Yenuganti, V.R.; Vanselow, J. Oleic acid induces down-regulation of the granulosa cell identity marker FOXL2, and up-regulation of the Sertoli cell marker SOX9 in bovine granulosa cells. Reprod. Biol. Endocrinol., 2017, 15(1), 57.
[http://dx.doi.org/10.1186/s12958-017-0276-z] [PMID: 28747195]
[31]
Elis, S.; Oseikria, M.; Vitorino, C.A.; Bertevello, P.S.; Corbin, E.; Teixeira-Gomes, A.P.; Lecardonnel, J.; Archilla, C.; Duranthon, V.; Labas, V.; Uzbekova, S. Docosahexaenoic acid mechanisms of action on the bovine oocyte-cumulus complex. J. Ovarian Res., 2017, 10, 74.
[32]
Boruszewska, D.; Sinderewicz, E.; Kowalczyk-Zieba, I.; Grycmacher, K.; Woclawek-Potocka, I. The effect of lysophosphatidic acid during in vitro maturation of bovine cumulus-oocyte complexes: cumulus expansion, glucose metabolism and expression of genes involved in the ovulatory cascade, oocyte and blastocyst competence. Reprod. Biol. Endocrinol., 2015, 13, 44.
[33]
Doignon, F.; Laquel, P.; Testet, E.; Tuphile, K.; Fouillen, L.; Bessoule, J.J. Requirement of phosphoinositides containing stearic acid to control cell polarity. Mol. Cell. Biol., 2015, 36(5), 765-780.
[http://dx.doi.org/10.1128/MCB.00843-15] [PMID: 26711260]
[34]
Chattopadhyay, A.; Navab, M.; Hough, G.; Grijalva, V.; Mukherjee, P.; Fogelman, H.R.; Hwang, L.H.; Faull, K.F.; Lusis, A.J.; Reddy, S.T.; Fogelman, A.M. Tg6F ameliorates the increase in oxidized phospholipids in the jejunum of mice fed unsaturated LysoPC or WD. J. Lipid Res., 2016, 57(5), 832-847.
[http://dx.doi.org/10.1194/jlr.M064352] [PMID: 26965826]
[35]
Hossein Rashidi, B.; Hormoz, B.; Shahrokh Tehraninejad, E.; Shariat, M.; Mahdavi, A. Testosterone and dehydroepiandrosterone sulphate levels and IVF/ICSI results. Gynecol. Endocrinol., 2009, 25(3), 194-198.
[http://dx.doi.org/10.1080/09513590802582644] [PMID: 19347710]
[36]
Lasley, B.L.; Crawford, S.L.; Laughlin, G.A.; Santoro, N.; McConnell, D.S.; Crandall, C.; Greendale, G.A.; Polotsky, A.J.; Vuga, M. Circulating dehydroepiandrosterone sulfate levels in women who underwent bilateral salpingo-oophorectomy during the menopausal transition. Menopause, 2011, 18(5), 494-498.
[http://dx.doi.org/10.1097/gme.0b013e3181fb53fc] [PMID: 21178790]
[37]
Chimote, N.M.; Nath, N.M.; Chimote, N.N.; Chimote, B.N. Follicular fluid dehydroepiandrosterone sulfate is a credible marker of oocyte maturity and pregnancy outcome in conventional in vitro fertilization cycles. J. Hum. Reprod. Sci., 2015, 8(4), 209-213.
[http://dx.doi.org/10.4103/0974-1208.170397] [PMID: 26751787]
[38]
Barad, D.; Gleicher, N. Effect of dehydroepiandrosterone on oocyte and embryo yields, embryo grade and cell number in IVF. Hum. Reprod., 2006, 21(11), 2845-2849.
[http://dx.doi.org/10.1093/humrep/del254] [PMID: 16997936]
[39]
Tartagni, M.; Cicinelli, M.V.; Baldini, D.; Tartagni, M.V.; Alrasheed, H.; DeSalvia, M.A.; Loverro, G.; Montagnani, M. Dehydroepiandrosterone decreases the age-related decline of the in vitro fertilization outcome in women younger than 40 years old. Reprod. Biol. Endocrinol., 2015, 13, 18.
[http://dx.doi.org/10.1186/s12958-015-0014-3] [PMID: 25884390]
[40]
Kumar, A.N.; Naidu, J.N.; Satyanarayana, U.; Anitha, M.; Ramalingam, K. Association of insulin resistance and serum 25-OH vitamin D in Indian women with polycystic ovary syndrome. International Journal of Clinical Biochemistry and Research, 2015, 2, 22-26.
[41]
Thomson, R.L.; Spedding, S.; Buckley, J.D. Vitamin D in the aetiology and management of polycystic ovary syndrome. Clin. Endocrinol. (Oxf.), 2012, 77(3), 343-350.
[http://dx.doi.org/10.1111/j.1365-2265.2012.04434.x] [PMID: 22574874]
[42]
Dicken, C.L.; Israel, D.D.; Davis, J.B.; Sun, Y.; Shu, J.; Hardin, J.; Neal-Perry, G. Peripubertal vitamin D(3) deficiency delays puberty and disrupts the estrous cycle in adult female mice. Biol. Reprod., 2012, 87(2), 51.
[http://dx.doi.org/10.1095/biolreprod.111.096511] [PMID: 22572998]
[43]
Kebapcilar, A.G.; Kulaksizoglu, M.; Kebapcilar, L.; Gonen, M.S.; Unlü, A.; Topcu, A.; Demirci, F.; Taner, C.E. Is there a link between premature ovarian failure and serum concentrations of vitamin D, zinc, and copper? Menopause, 2013, 20(1), 94-99.
[http://dx.doi.org/10.1097/gme.0b013e31826015ca] [PMID: 22968257]
[44]
Zhu, J.; Lin, F.H.; Zhang, J.; Lin, J.; Li, H.; Li, Y.W.; Tan, X.W.; Tan, J.H. The signaling pathways by which the Fas/FasL system accelerates oocyte aging. Aging (Albany NY), 2016, 8(2), 291-303.
[http://dx.doi.org/10.18632/aging.100893] [PMID: 26869336]
[45]
Moise, A.R.; Isken, A.; Domínguez, M.; de Lera, A.R.; von Lintig, J.; Palczewski, K. Specificity of zebrafish retinol saturase: formation of all-trans-13,14-dihydroretinol and all-trans-7,8- dihydroretinol. Biochemistry, 2007, 46(7), 1811-1820.
[http://dx.doi.org/10.1021/bi062147u] [PMID: 17253779]
[46]
Umetani, M.; Ghosh, P.; Ishikawa, T.; Umetani, J.; Ahmed, M.; Mineo, C.; Shaul, P.W. The cholesterol metabolite 27-hydroxycholesterol promotes atherosclerosis via proinflammatory processes mediated by estrogen receptor alpha. Cell Metab., 2014, 20(1), 172-182.
[http://dx.doi.org/10.1016/j.cmet.2014.05.013] [PMID: 24954418]
[47]
Burkard, I.; von Eckardstein, A.; Waeber, G.; Vollenweider, P.; Rentsch, K.M. Lipoprotein distribution and biological variation of 24S- and 27-hydroxycholesterol in healthy volunteers. Atherosclerosis, 2007, 194(1), 71-78.
[http://dx.doi.org/10.1016/j.atherosclerosis.2006.09.026] [PMID: 17107679]
[48]
Sauer, M.V.; Sauer, M.D. Reproduction at an advanced maternal age and maternal health. Fertil. Steril., 2015, 103(5), 1136-1143.
[http://dx.doi.org/10.1016/j.fertnstert.2015.03.004] [PMID: 25934599]
[49]
Crawford, N.M.; Steiner, A.Z. Age-related infertility. Obstet. Gynecol. Clin. North Am., 2015, 42(1), 15-25.
[http://dx.doi.org/10.1016/j.ogc.2014.09.005] [PMID: 25681837]


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VOLUME: 16
ISSUE: 3
Year: 2020
Page: [291 - 302]
Pages: 12
DOI: 10.2174/1573412915666190218155820
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