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Current Analytical Chemistry

Editor-in-Chief

ISSN (Print): 1573-4110
ISSN (Online): 1875-6727

Review Article

MALDI MS Analysis to Investigate the Lipid Composition of Sperm

Author(s): Kathrin M. Engel, Ulrike Jakop, Karin Müller, Sonja Grunewald, Uwe Paasch and Jürgen Schiller*

Volume 16, Issue 1, 2020

Page: [79 - 91] Pages: 13

DOI: 10.2174/1573411014666181030123256

Price: $65

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Abstract

Background: The sperm plasma membrane meets the requirements of sperm transit through the female genital tract and subsequent fertilization. Commonly, the (phospho)lipid composition of sperm is characterized by tremendous amounts of highly unsaturated fatty acyl residues such as docosahexaenoic and docosapentaenoic acid. While human sperm contain almost exclusively diacyl lipids, many animal sperm additionally contain significant amounts of ether lipids such as alkylacyl- and alkenyl-acyl lipids (plasmalogens).

Hypothesis/Objective: It is suggested that deviations from the typical lipid composition are indicative of pathological changes. Therefore, simple methods to elucidate the sperm lipid composition are essential.

Method: Matrix-assisted laser desorption and ionization (MALDI) mass spectrometry (MS) is a fast and simple method. Since the selection of the most suitable matrix is a crucial step in MALDI MS, this topic will be highlighted. It will also be shown that MALDI MS can be easily combined with thin-layer chromatography to overcome ion suppression effects.

Results: The lipid composition of sperm from different species can be elucidated by MALDI MS. However, different matrix compounds have to be used to record positive and negative ion mass spectra. Since some sperm (glyco)lipids are characterized by the presence of sulfate residues which suppress the detection of less acidic lipids in the negative ion mode, previous separation is often necessary. It will be also emphasized that plasmalogens can be easily identified by either enzymatic digestion or treatment with acids.

Conclusion: MALDI MS is a reliable method to obtain sperm lipid fingerprints in a simple and convenient way.

Keywords: Lipid oxidation, MALDI, mass spectrometry, phospholipids, sperm, TLC.

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[1]
Carlsen, E.; Giwercman, A.; Keiding, N.; Skakkebaek, N.E. Evidence for decreasing quality of semen during past 50 years. BMJ, 1992, 305(6854), 609-613.
[http://dx.doi.org/10.1136/bmj.305.6854.609] [PMID: 1393072]
[2]
Merzenich, H.; Zeeb, H.; Blettner, M. Decreasing sperm quality: a global problem? BMC Public Health, 2010, 10, 24.
[http://dx.doi.org/10.1186/1471-2458-10-24] [PMID: 20085639]
[3]
Wathes, D.C.; Abayasekara, D.R.; Aitken, R.J. Polyunsaturated fatty acids in male and female reproduction. Biol. Reprod., 2007, 77(2), 190-201.
[http://dx.doi.org/10.1095/biolreprod.107.060558] [PMID: 17442851]
[4]
Nolan, J.P.; Hammerstedt, R.H. Regulation of membrane stability and the acrosome reaction in mammalian sperm. FASEB J., 1997, 11(8), 670-682.
[http://dx.doi.org/10.1096/fasebj.11.8.9240968] [PMID: 9240968]
[5]
Honke, K.; Zhang, Y.; Cheng, X.; Kotani, N.; Taniguchi, N. Biological roles of sulfoglycolipids and pathophysiology of their deficiency. Glycoconj. J., 2004, 21(1-2), 59-62.
[http://dx.doi.org/10.1023/B:GLYC.0000043749.06556.3d] [PMID: 15467400]
[6]
Teuber, K.; Schiller, J.; Jakop, U.; Lüpold, S.; Orledge, J.M.; Blount, J.D.; Royle, N.J.; Hoodless, A.; Müller, K. MALDI-TOF mass spectrometry as a simple tool to determine the phospholipid/glycolipid composition of sperm: pheasant spermatozoa as one selected example. Anim. Reprod. Sci., 2011, 123(3-4), 270-278.
[http://dx.doi.org/10.1016/j.anireprosci.2011.01.009] [PMID: 21295419]
[7]
Lenzi, A.; Picardo, M.; Gandini, L.; Dondero, F. Lipids of the sperm plasma membrane: from polyunsaturated fatty acids considered as markers of sperm function to possible scavenger therapy. Hum. Reprod. Update, 1996, 2(3), 246-256.
[http://dx.doi.org/10.1093/humupd/2.3.246] [PMID: 9079417]
[8]
Christie, W.W.; Han, X. Lipid Analysis - Isolation, Separation, Identification and Lipidomic Analysis; 4th ed.; The Oily Press: Bridgwater, 2010.
[9]
Schlame, M.; Ren, M.; Xu, Y.; Greenberg, M.L.; Haller, I. Molecular symmetry in mitochondrial cardiolipins. Chem. Phys. Lipids, 2005, 138(1-2), 38-49.
[http://dx.doi.org/10.1016/j.chemphyslip.2005.08.002] [PMID: 16226238]
[10]
Eibisch, M.; Zellmer, S.; Gebhardt, R.; Süss, R.; Fuchs, B.; Schiller, J. Phosphatidylcholine dimers can be easily misinterpreted as cardiolipins in complex lipid mixtures: a matrix-assisted laser desorption/ionization time-of-flight mass spectrometric study of lipids from hepatocytes. Rapid Commun. Mass Spectrom., 2011, 25(18), 2619-2626.
[http://dx.doi.org/10.1002/rcm.5161] [PMID: 23657956]
[11]
Harayama, T.; Riezman, H. Understanding the diversity of membrane lipid composition. Nat. Rev. Mol. Cell Biol., 2018, 19(5), 281-296.
[http://dx.doi.org/10.1038/nrm.2017.138] [PMID: 29410529]
[12]
Lydic, T.A.; Goo, Y.H. Lipidomics unveils the complexity of the lipidome in metabolic diseases. Clin. Transl. Med., 2018, 7(1), 4.
[http://dx.doi.org/10.1186/s40169-018-0182-9] [PMID: 29374337]
[13]
Fuchs, B.; Bresler, K.; Schiller, J. Oxidative changes of lipids monitored by MALDI MS. Chem. Phys. Lipids, 2011, 164(8), 782-795.
[http://dx.doi.org/10.1016/j.chemphyslip.2011.09.006] [PMID: 21964445]
[14]
Fuchs, B.; Müller, K.; Paasch, U.; Schiller, J. Lysophospholipids: potential markers of diseases and infertility? Mini Rev. Med. Chem., 2012, 12(1), 74-86.
[http://dx.doi.org/10.2174/138955712798868931] [PMID: 22070693]
[15]
Liebisch, G.; Vizcaíno, J.A.; Köfeler, H.; Trötzmüller, M.; Griffiths, W.J.; Schmitz, G.; Spener, F.; Wakelam, M.J. Shorthand notation for lipid structures derived from mass spectrometry. J. Lipid Res., 2013, 54(6), 1523-1530.
[http://dx.doi.org/10.1194/jlr.M033506] [PMID: 23549332]
[16]
Braverman, N.E.; Moser, A.B. Functions of plasmalogen lipids in health and disease. Biochim. Biophys. Acta, 2012, 1822(9), 1442-1452.
[http://dx.doi.org/10.1016/j.bbadis.2012.05.008] [PMID: 22627108]
[17]
Schiller, J.; Müller, M.; Fuchs, B.; Arnold, K.; Huster, D. 31P NMR spectroscopy of phospholipids: from micelles to membranes. Curr. Anal. Chem., 2007, 3(4), 283-301.
[http://dx.doi.org/10.2174/157341107782109635]
[18]
Wallner, S.; Schmitz, G. Plasmalogens the neglected regulatory and scavenging lipid species. Chem. Phys. Lipids, 2011, 164(6), 573-589.
[http://dx.doi.org/10.1016/j.chemphyslip.2011.06.008] [PMID: 21723266]
[19]
Rouser, G.; Fkeischer, S.; Yamamoto, A. Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids, 1970, 5(5), 494-496.
[http://dx.doi.org/10.1007/BF02531316] [PMID: 5483450]
[20]
Pesce, M.A.; Bodourian, S.H. Interference with the enzymic measurement of cholesterol in serum by use of five reagent kits. Clin. Chem., 1977, 23(4), 757-760.
[PMID: 844175]
[21]
Fuchs, B.; Süss, R.; Teuber, K.; Eibisch, M.; Schiller, J. Lipid analysis by thin-layer chromatography--a review of the current state. J. Chromatogr. A, 2011, 1218(19), 2754-2774.
[http://dx.doi.org/10.1016/j.chroma.2010.11.066] [PMID: 21167493]
[22]
Kuksis, A.; Myher, J.J. Gas chromatographic analysis of plasma lipids. Adv. Chromatogr., 1989, 28, 267-332.
[PMID: 2646858]
[23]
Giles, C.; Takechi, R.; Lam, V.; Dhaliwal, S.S.; Mamo, J.C.L. Contemporary lipidomic analytics: opportunities and pitfalls. Prog. Lipid Res., 2018, 71, 86-100.
[http://dx.doi.org/10.1016/j.plipres.2018.06.003] [PMID: 29959947]
[24]
Lee, H.C.; Yokomizo, T. Applications of mass spectrometry-based targeted and non-targeted lipidomics. Biochem. Biophys. Res. Commun., 2018, 504(3), 576-581.
[http://dx.doi.org/10.1016/j.bbrc.2018.03.081] [PMID: 29534960]
[25]
Fuchs, B.; Süss, R.; Schiller, J. An update of MALDI-TOF mass spectrometry in lipid research. Prog. Lipid Res., 2010, 49(4), 450-475.
[http://dx.doi.org/10.1016/j.plipres.2010.07.001] [PMID: 20643161]
[26]
Jaskolla, T.W.; Karas, M. Compelling evidence for Lucky Survivor and gas phase protonation: the unified MALDI analyte protonation mechanism. J. Am. Soc. Mass Spectrom., 2011, 22(6), 976-988.
[http://dx.doi.org/10.1007/s13361-011-0093-0] [PMID: 21953039]
[27]
Hillenkamp, F.; Peter-Katalinić, J. MALDI MS - a practical guide to instrumentation, methods and application, 2nd ed; Wiley-VCH: Weinheim, 2007.
[http://dx.doi.org/10.1002/9783527610464]
[28]
Jurowski, K.; Kochan, K.; Walczak, J.; Barańska, M.; Piekoszewski, W.; Buszewski, B. Analytical techniques in lipidomics: state of the art. Crit. Rev. Anal. Chem., 2017, 47(5), 418-437.
[http://dx.doi.org/10.1080/10408347.2017.1310613] [PMID: 28340309]
[29]
Tholey, A.; Heinzle, E. Ionic (liquid) matrices for matrix-assisted laser desorption/ionization mass spectrometry-applications and perspectives. Anal. Bioanal. Chem., 2006, 386(1), 24-37.
[http://dx.doi.org/10.1007/s00216-006-0600-5] [PMID: 16830111]
[30]
O’Rourke, M.B.; Djordjevic, S.P.; Padula, M.P. The quest for improved reproducibility in MALDI mass spectrometry. Mass Spectrom. Rev., 2018, 37(2), 217-228.
[http://dx.doi.org/10.1002/mas.21515] [PMID: 27420733]
[31]
Schiller, J.; Arnhold, J.; Benard, S.; Müller, M.; Reichl, S.; Arnold, K. Lipid analysis by matrix-assisted laser desorption and ionization mass spectrometry: A methodological approach. Anal. Biochem., 1999, 267(1), 46-56.
[http://dx.doi.org/10.1006/abio.1998.3001] [PMID: 9918654]
[32]
Griffiths, R.L.; Bunch, J. A survey of useful salt additives in matrix-assisted laser desorption/ionization mass spectrometry and tandem mass spectrometry of lipids: introducing nitrates for improved analysis. Rapid Commun. Mass Spectrom., 2012, 26(13), 1557-1566.
[http://dx.doi.org/10.1002/rcm.6258] [PMID: 22638973]
[33]
Fuchs, B.; Schiller, J. Recent developments of useful MALDI matrices for the mass spectrometric characterization of apolar compounds. Curr. Org. Chem., 2009, 13(16), 1664-1681.
[http://dx.doi.org/10.2174/138527209789578108]
[34]
Teuber, K.; Schiller, J.; Fuchs, B.; Karas, M.; Jaskolla, T.W. Significant sensitivity improvements by matrix optimization: a MALDI-TOF mass spectrometric study of lipids from hen egg yolk. Chem. Phys. Lipids, 2010, 163(6), 552-560.
[http://dx.doi.org/10.1016/j.chemphyslip.2010.04.005] [PMID: 20420816]
[35]
Eibisch, M.; Fuchs, B.; Schiller, J.; Süß, R.; Teuber, K. Analysis of phospholipid mixtures from biological tissues by matrix-assisted laser desorption and ionization time-of-flight mass spectrometry (MALDI-TOF MS): a laboratory experiment. J. Chem. Educ., 2011, 88(4), 503-507.
[http://dx.doi.org/10.1021/ed1004905]
[36]
Huang, C.; Li, B.; Xu, K.; Liu, D.; Hu, J.; Yang, Y.; Nie, H.; Fan, L.; Zhu, W. Decline in semen quality among 30,636 young Chinese men from 2001 to 2015. Fertil. Steril., 2017, 107(1), 83-88.e2.
[http://dx.doi.org/10.1016/j.fertnstert.2016.09.035] [PMID: 27793371]
[37]
Sengupta, P.; Nwagha, U.; Dutta, S.; Krajewska-Kulak, E.; Izuka, E. Evidence for decreasing sperm count in African population from 1965 to 2015. Afr. Health Sci., 2017, 17(2), 418-427.
[http://dx.doi.org/10.4314/ahs.v17i2.16] [PMID: 29062337]
[38]
Gabrielsen, J.S.; Tanrikut, C. Chronic exposures and male fertility: the impacts of environment, diet, and drug use on spermatogenesis. Andrology, 2016, 4(4), 648-661.
[http://dx.doi.org/10.1111/andr.12198] [PMID: 27230702]
[39]
Schiller, J.; Arnhold, J.; Glander, H-J.; Arnold, K. Lipid analysis of human spermatozoa and seminal plasma by MALDI-TOF mass spectrometry and NMR spectroscopy - effects of freezing and thawing. Chem. Phys. Lipids, 2000, 106(2), 145-156.
[http://dx.doi.org/10.1016/S0009-3084(00)00148-1] [PMID: 10930566]
[40]
Aksoy, Y.; Aksoy, H.; Altinkaynak, K.; Aydin, H.R.; Ozkan, A. Sperm fatty acid composition in subfertile men. Prostaglandins Leukot. Essent. Fatty Acids, 2006, 75(2), 75-79.
[http://dx.doi.org/10.1016/j.plefa.2006.06.002] [PMID: 16893631]
[41]
Brezina, P.R.; Kutteh, W.H.; Bailey, A.P.; Ding, J.; Ke, R.W.; Klosky, J.L. Fertility preservation in the age of assisted reproductive technologies. Obstet. Gynecol. Clin. North Am., 2015, 42(1), 39-54.
[http://dx.doi.org/10.1016/j.ogc.2014.09.004] [PMID: 25681839]
[42]
Glander, H-J.; Schiller, J.; Süss, R.; Paasch, U.; Grunewald, S.; Arnhold, J. Deterioration of spermatozoal plasma membrane is associated with an increase of sperm lyso-phosphatidylcholines. Andrologia, 2002, 34(6), 360-366.
[http://dx.doi.org/10.1046/j.1439-0272.2002.00508.x] [PMID: 12472619]
[43]
Demchenko, A.P. Beyond annexin V: fluorescence response of cellular membranes to apoptosis. Cytotechnology, 2013, 65(2), 157-172.
[http://dx.doi.org/10.1007/s10616-012-9481-y] [PMID: 22797774]
[44]
Said, T.M.; Agarwal, A.; Grunewald, S.; Rasch, M.; Glander, H.J.; Paasch, U. Evaluation of sperm recovery following annexin V magnetic-activated cell sorting separation. Reprod. Biomed. Online, 2006, 13(3), 336-339.
[http://dx.doi.org/10.1016/S1472-6483(10)61437-X] [PMID: 16984761]
[45]
Aitken, R.J.; Jones, K.T.; Robertson, S.A. Reactive oxygen species and sperm function--in sickness and in health. J. Androl., 2012, 33(6), 1096-1106.
[http://dx.doi.org/10.2164/jandrol.112.016535] [PMID: 22879525]
[46]
Griveau, J.F.; Dumont, E.; Renard, P.; Callegari, J.P.; Le Lannou, D. Reactive oxygen species, lipid peroxidation and enzymatic defence systems in human spermatozoa. J. Reprod. Fertil., 1995, 103(1), 17-26.
[http://dx.doi.org/10.1530/jrf.0.1030017] [PMID: 7707295]
[47]
Wolff, H. The biologic significance of white blood cells in semen. Fertil. Steril., 1995, 63(6), 1143-1157.
[http://dx.doi.org/10.1016/S0015-0282(16)57588-8] [PMID: 7750580]
[48]
Lessig, J.; Gey, C.; Schiller, J.; Süss, R.; Paasch, U.; Grunewald, S.; Glander, H.J.; Arnhold, J. Hypochlorous acid-induced stress on human spermatozoa. A model for inflammation in the male genital tract. Chem. Phys. Lipids, 2005, 135(2), 201-211.
[http://dx.doi.org/10.1016/j.chemphyslip.2005.02.015] [PMID: 15885680]
[49]
Lessig, J.; Glander, H-J.; Schiller, J.; Petković, M.; Paasch, U.; Arnhold, J. Destabilization of the acrosome results in release of phospholipase A2 from human spermatozoa and subsequent formation of lysophospholipids. Andrologia, 2006, 38(2), 69-75.
[http://dx.doi.org/10.1111/j.1439-0272.2006.00713.x] [PMID: 16529578]
[50]
Pyttel, S.; Zschörnig, K.; Nimptsch, A.; Paasch, U.; Schiller, J. Enhanced lysophosphatidylcholine and sphingomyelin contents are characteristic of spermatozoa from obese men-A MALDI mass spectrometric study. Chem. Phys. Lipids, 2012, 165(8), 861-865.
[http://dx.doi.org/10.1016/j.chemphyslip.2012.11.001] [PMID: 23146833]
[51]
Camargo, M.; Intasqui, P.; de Lima, C.B.; Montani, D.A.; Nichi, M.; Pilau, E.J.; Gozzo, F.C.; Lo Turco, E.G.; Bertolla, R.P. Maldi-tof fingerprinting of seminal plasma lipids in the study of human male infertility. Lipids, 2014, 49(9), 943-956.
[http://dx.doi.org/10.1007/s11745-014-3922-7] [PMID: 24934590]
[52]
Esmaeili, V.; Shahverdi, A.H.; Moghadasian, M.H.; Alizadeh, A.R. Dietary fatty acids affect semen quality: a review. Andrology, 2015, 3(3), 450-461.
[http://dx.doi.org/10.1111/andr.12024] [PMID: 25951427]
[53]
Vireque, A.A.; Tata, A.; Silva, O.F.; LoTurco, E.G.; Azzolini, A.; Ferreira, C.R.; Dantas, M.H.; Ferriani, R.A.; Reis, R.M. Effects of n-6 and n-3 polyunsaturated acid-rich soybean phosphatidylcholine on membrane lipid profile and cryotolerance of human sperm. Fertil. Steril., 2016, 106(2), 273-283.e6.
[http://dx.doi.org/10.1016/j.fertnstert.2016.03.044] [PMID: 27105718]
[54]
Pini, T.; Leahy, T.; de Graaf, S.P. Sublethal sperm freezing damage: Manifestations and solutions. Theriogenology, 2018, 118, 172-181.
[http://dx.doi.org/10.1016/j.theriogenology.2018.06.006] [PMID: 29913422]
[55]
Svetlichnyy, V.; Müller, P.; Pomorski, T.G.; Schulze, M.; Schiller, J.; Müller, K. Metabolic incorporation of unsaturated fatty acids into boar spermatozoa lipids and de novo formation of diacylglycerols. Chem. Phys. Lipids, 2014, 177, 41-50.
[http://dx.doi.org/10.1016/j.chemphyslip.2013.11.001] [PMID: 24252640]
[56]
Pyttel, S.; Nimptsch, A.; Böttger, J.; Zschörnig, K.; Jakop, U.; Wegener, J.; Müller, K.; Paasch, U.; Schiller, J. Changes of murine sperm phospholipid composition during epididymal maturation determined by MALDI-TOF mass spectrometry. Theriogenology, 2014, 82(3), 396-402.
[http://dx.doi.org/10.1016/j.theriogenology.2014.04.017] [PMID: 24877723]
[57]
Goto-Inoue, N.; Hayasaka, T.; Zaima, N.; Setou, M. The specific localization of seminolipid molecular species on mouse testis during testicular maturation revealed by imaging mass spectrometry. Glycobiology, 2009, 19(9), 950-957.
[http://dx.doi.org/10.1093/glycob/cwp089] [PMID: 19542524]
[58]
Lopalco, P.; Vitale, R.; Cho, Y.S.; Totaro, P.; Corcelli, A.; Lobasso, S. Alteration of cholesterol sulfate/seminolipid ratio in semen lipid profile of men with oligoasthenozoospermia. Front. Physiol., 2019, 10, 1344.
[59]
Zhang, Y.; Hayashi, Y.; Cheng, X.; Watanabe, T.; Wang, X.; Taniguchi, N.; Honke, K. Testis-specific sulfoglycolipid, seminolipid, is essential for germ cell function in spermatogenesis. Glycobiology, 2005, 15(6), 649-654.
[http://dx.doi.org/10.1093/glycob/cwi043] [PMID: 15659616]
[60]
Zaima, N.; Kinoshita, S.; Hieda, N.; Kugo, H.; Narisawa, K.; Yamamoto, A.; Yanagimoto, K.; Moriyama, T. Effect of dietary fish oil on mouse testosterone level and the distribution of eicosapentaenoic acid-containing phosphatidylcholine in testicular interstitium. Biochem. Biophys. Rep., 2016, 7, 259-265.
[http://dx.doi.org/10.1016/j.bbrep.2016.06.014] [PMID: 28955915]
[61]
Lessig, J.; Gey, C.; Süss, R.; Schiller, J.; Glander, H-J.; Arnhold, J. Analysis of the lipid composition of human and boar spermatozoa by MALDI-TOF mass spectrometry, thin layer chromatography and 31P NMR spectroscopy. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2004, 137(2), 265-277.
[http://dx.doi.org/10.1016/j.cbpc.2003.12.001] [PMID: 14990223]
[62]
Lessig, J.; Fuchs, B. HOCl-mediated glycerophosphocholine and glycerophosphoethanolamine generation from plasmalogens in phospholipid mixtures. Lipids, 2010, 45(1), 37-51.
[http://dx.doi.org/10.1007/s11745-009-3365-8] [PMID: 19937395]
[63]
Nimptsch, A.; Fuchs, B.; Süß, R.; Zschörnig, K.; Jakop, U.; Göritz, F.; Schiller, J.; Müller, K. A simple method to identify ether lipids in spermatozoa samples by MALDI-TOF mass spectrometry. Anal. Bioanal. Chem., 2013, 405(21), 6675-6682.
[http://dx.doi.org/10.1007/s00216-013-7147-z] [PMID: 23812881]
[64]
Schiller, J.; Müller, K.; Süss, R.; Arnhold, J.; Gey, C.; Herrmann, A.; Lessig, J.; Arnold, K.; Müller, P. Analysis of the lipid composition of bull spermatozoa by MALDI-TOF mass spectrometry--a cautionary note. Chem. Phys. Lipids, 2003, 126(1), 85-94.
[http://dx.doi.org/10.1016/S0009-3084(03)00097-5] [PMID: 14580713]
[65]
Blank, M.L.; Cress, E.A.; Piantadosi, C.; Snyder, F. A method for the quantitative determination of glycerolipids containing O-alkyl and O-alk-1-enyl moieties. Biochim. Biophys. Acta, 1975, 380(2), 208-218.
[http://dx.doi.org/10.1016/0005-2760(75)90007-7] [PMID: 164236]
[66]
Teuber, K.; Fedorova, M.; Hoffmann, R.; Schiller, J. Dinitrophenylhydrazine as a new matrix to analyze oxidized phospholipids by MALDI-TOF mass spectrometry. Anal. Lett., 2012, 45, 968-976.
[http://dx.doi.org/10.1080/00032719.2012.670785]
[67]
Dannenberger, D.; Lorenz, S.; Nuernberg, G.; Scollan, N.; Ender, K.; Nuernberg, K. Analysis of fatty aldehyde composition, including 12-methyltridecanal, in plasmalogens from longissimus muscle of concentrate- and pasture-fed bulls. J. Agric. Food Chem., 2006, 54(1), 182-188.
[http://dx.doi.org/10.1021/jf051596i] [PMID: 16390197]
[68]
Schmid, H.H.; Bandi, P.C.; Su, K.L. Analysis and quantification of ether lipids by chromatographic methods. J. Chromatogr. Sci., 1975, 13(10), 478-486.
[http://dx.doi.org/10.1093/chromsci/13.10.478] [PMID: 241757]
[69]
Fuchs, B.; Müller, K.; Göritz, F.; Blottner, S.; Schiller, J. Characteristic oxidation products of choline plasmalogens are detectable in cattle and roe deer spermatozoa by MALDI-TOF mass spectrometry. Lipids, 2007, 42(11), 991-998.
[http://dx.doi.org/10.1007/s11745-007-3108-7] [PMID: 17717713]
[70]
Sieme, H.; Oldenhof, H.; Wolkers, W.F. Mode of action of cryoprotectants for sperm preservation. Anim. Reprod. Sci., 2016, 169, 2-5.
[http://dx.doi.org/10.1016/j.anireprosci.2016.02.004] [PMID: 26936658]
[71]
Engel, K.M.; Schiller, J.; Müller, K.; Dannenberger, D.; Jakop, U. The phospholipid composition of kangaroo spermatozoa verified by mass spectrometric lipid analysis. Lipids, 2017, 52(10), 857-869.
[http://dx.doi.org/10.1007/s11745-017-4283-9] [PMID: 28801719]
[72]
Cabrera, T.; Ramires-Neto, C.; Belaz, K.R.A.; Freitas-Dell’aqua, C.P.; Zampieri, D.; Tata, A.; Eberlin, M.N.; Alvarenga, M.A.; Souza, F.F. Influence of spermatozoal lipidomic profile on the cryoresistance of frozen spermatozoa from stallions. Theriogenology, 2018, 108, 161-166.
[http://dx.doi.org/10.1016/j.theriogenology.2017.11.025] [PMID: 29223009]
[73]
Fuchs, B.; Jakop, U.; Göritz, F.; Hermes, R.; Hildebrandt, T.; Schiller, J.; Müller, K. MALDI-TOF “fingerprint” phospholipid mass spectra allow the differentiation between ruminantia and feloideae spermatozoa. Theriogenology, 2009, 71(4), 568-575.
[http://dx.doi.org/10.1016/j.theriogenology.2008.08.023] [PMID: 18950847]
[74]
Braga, L.T., Jr; Bravo, N.; Belaz, K.; Zampieri, D.; Eberlin, M.N.; Conforti, V.A. Lipid profiles of canine spermatozoa as revealed via matrix-assisted laser desorption/ionization mass spectrometry. Reprod. Domest. Anim., 2016, 51(6), 1055-1058.
[http://dx.doi.org/10.1111/rda.12792] [PMID: 27645126]
[75]
Lucio, C.F.; Brito, M.M.; Angrimani, D.; Belaz, K.; Morais, D.; Zampieri, D.; Losano, J.; Assumpção, M.; Nichi, M.; Eberlin, M.N.; Vannucchi, C.I. Lipid composition of the canine sperm plasma membrane as markers of sperm motility. Reprod. Domest. Anim., 2017, 52(Suppl. 2), 208-213.
[http://dx.doi.org/10.1111/rda.12860] [PMID: 27807900]
[76]
Collins, A.M.; Williams, V.; Evans, J.D. Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Insect Mol. Biol., 2004, 13(2), 141-146.
[http://dx.doi.org/10.1111/j.0962-1075.2004.00469.x] [PMID: 15056361]
[77]
Wegener, J.; Zschörnig, K.; Onischke, K.; Fuchs, B.; Schiller, J.; Müller, K. Conservation of honey bee (Apis mellifera) sperm phospholipids during storage in the bee queen--a TLC/MALDI-TOF MS study. Exp. Gerontol., 2013, 48(2), 213-222.
[http://dx.doi.org/10.1016/j.exger.2012.12.009] [PMID: 23279974]

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