Seminal lipid profiling and antioxidant capacity: A species comparison.
Abstract: On their way to the oocyte, sperm cells are subjected to oxidative stress, which may trigger the oxidation of phospholipids (PL). Applying MALDI-TOF MS, HPTLC and ESI-IT MS, we comparatively analyzed the PL compositions of semen and blood of species differing in their reproductive systems and types of nutrition (bull, boar, stallion, lion and man) with regard to the sensitivity to oxidation as well as the accumulation of harmful lyso-PL (LPL), transient products of lipid oxidation. In addition, the protective capacity of seminal fluid (SF) was also examined. The PL composition of erythrocytes and blood plasma is similar across the species, while pronounced differences exist for sperm and SF. Since the blood function is largely conserved across mammalian species, but the reproductive systems may vary in many aspects, the obtained results suggest that the PL composition is not determined by the type of nutrition, but by the relatedness of species and by functional requirements of cell membranes such as fluidity. Sperm motion and fertilization of oocytes require a rather flexible membrane, which is accomplished by significant moieties of unsaturated fatty acyl residues in sperm lipids of most species, but implies a higher risk of oxidation. Due to a high content of plasmalogens (alkenyl ether lipids), bull sperm are most susceptible to oxidation. Our data indicate that bull sperm possess the most effective protective power in SF. Obviously, a co-evolution of PL composition and protective mechanisms has occurred in semen and is related to the reproductive characteristics. Although the protective capacity in human SF seems well developed, we recorded the most pronounced individual contaminations with LPL in human semen. Probably, massive oxidative challenges related to lifestyle factors interfere with natural conditions.
Publication Date: 2022-03-08 PubMed ID: 35259184PubMed Central: PMC8903242DOI: 10.1371/journal.pone.0264675Google Scholar: Lookup
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- Journal Article
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Summary
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This research investigates how sperm cells, on their journey to the egg, are impacted by oxidative stress potentially leading to the oxidation of phospholipids. The study compares the sperm and blood of different species (bull, boar, stallion, lion and man) in relation to their sensitivity to oxidation, the accumulation of harmful lyso-PL, and the protective capacity of the seminal fluid. The results suggest that the phospholipid composition is determined by the relatedness of species and the functional requirements of cell membranes, not diet, and has evolved to protect against oxidation in tandem with reproductive characteristics.
Research Methodology
- Applying Matrix-assisted Laser Desorption/Ionization-Time Of Flight Mass Spectrometry (MALDI-TOF MS), High-Performance Thin-Layer Chromatography (HPTLC) and ElectroSpray Ionization – Ion Trap Mass Spectrometry (ESI-IT MS), the research team analyzed the phospholipid (PL) components of semen and blood samples taken from various species (bull, boar, stallion, lion and man).
- These species were chosen due to differences in their reproductive systems and diets.
- The team was particularly interested in studying the sensitivity of these samples to oxidation and the accumulation of harmful lyso-PL, which are transient products of lipid oxidation.
Investigating Seminal Fluid’s Protective Capacity
- In addition to examining the phospholipid composition of semen and blood, the protective capacity of seminal fluid (SF) against oxidation was also analysed.
Findings on Phospholipid (PL) Composition
- The research found that while the PL composition of red blood cells and blood plasma was similar across the studied species, there were pronounced differences in the PL compositions of sperm and seminal fluid.
Significance of Phospholipid Composition
- Given that blood function is largely the same across mammalian species, while reproductive systems can vary greatly, this suggests that PL composition is more likely determined by species relatedness and particular functional needs of cell membranes (such as fluidity) rather than diet.
- For instance, more fluid membranes, which are vital for sperm motility and egg fertilization, are achieved through increased amounts of unsaturated fatty acyl residues in sperm lipids; however, this also implies higher susceptibility to oxidation.
Specific Findings in Different Species
- It was found that bull sperm, which contain a high content of plasmalogens (a type of alkenyl ether lipid), are most susceptible to oxidation. However, the study also found that bull sperm seem to possess the most effective antioxidative mechanisms in their seminal fluid.
- This suggests that there is a co-evolution of PL compositions and antioxidative mechanisms in semen related to specific reproductive characteristics of each species.
- Despite the apparent efficacy of antioxidative mechanisms in human seminal fluid, the most pronounced individual contaminations with harmful lyso-PL were found in human semen samples. This could be due to high oxidative stress from lifestyle-related factors.
Cite This Article
APA
Jakop U, Müller K, Müller P, Neuhauser S, Callealta Rodríguez I, Grunewald S, Schiller J, Engel KM.
(2022).
Seminal lipid profiling and antioxidant capacity: A species comparison.
PLoS One, 17(3), e0264675.
https://doi.org/10.1371/journal.pone.0264675 Publication
Researcher Affiliations
- Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany.
- Institute for Reproduction of Farm Animals Schönow e. V., Bernau, Germany.
- Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany.
- Department of Biology, Humboldt-Universität zu Berlin, Berlin, Germany.
- Free University Berlin, Equine Clinic, Bad Saarow, Germany.
- Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa.
- Department of Dermatology, Training Center of the European Academy of Andrology, University of Leipzig, Leipzig, Germany.
- Department of Dermatology, Training Center of the European Academy of Andrology, University of Leipzig, Leipzig, Germany.
- Department of Dermatology, Training Center of the European Academy of Andrology, University of Leipzig, Leipzig, Germany.
- Faculty of Medicine, Institute for Medical Physics and Biophysics, Leipzig University, Leipzig, Germany.
MeSH Terms
- Animals
- Antioxidants / metabolism
- Cattle
- Cell Membrane / metabolism
- Horses
- Humans
- Male
- Mammals / metabolism
- Oxidative Stress
- Phospholipids / metabolism
- Semen / metabolism
- Spermatozoa / metabolism
- Swine
Conflict of Interest Statement
The authors have declared that no competing interests exist.
References
This article includes 50 references
- Dean JM, Lodhi IJ. Structural and functional roles of ether lipids.. Protein Cell 2018 Feb;9(2):196-206.
- 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 Nov;126(1):85-94.
- Lessig J, Gey C, Süss R, Schiller J, Glander HJ, 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 Feb;137(2):265-77.
- 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 Aug;405(21):6675-82.
- Ernst AM, Contreras FX, Brügger B, Wieland F. Determinants of specificity at the protein-lipid interface in membranes.. FEBS Lett 2010 May 3;584(9):1713-20.
- Nicolson GL. The Fluid-Mosaic Model of Membrane Structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years.. Biochim Biophys Acta 2014 Jun;1838(6):1451-66.
- Nagata M. Inflammatory cells and oxygen radicals.. Curr Drug Targets Inflamm Allergy 2005 Aug;4(4):503-4.
- García-Rincón J, Darszon A, Beltrán C. Speract, a sea urchin egg peptide that regulates sperm motility, also stimulates sperm mitochondrial metabolism.. Biochim Biophys Acta 2016 Apr;1857(4):415-26.
- Nowicka-Bauer K, Lepczynski A, Ozgo M, Kamieniczna M, Fraczek M, Stanski L, Olszewska M, Malcher A, Skrzypczak W, Kurpisz MK. Sperm mitochondrial dysfunction and oxidative stress as possible reasons for isolated asthenozoospermia.. J Physiol Pharmacol 2018 Jun;69(3).
- du Plessis SS, Agarwal A, Mohanty G, van der Linde M. Oxidative phosphorylation versus glycolysis: what fuel do spermatozoa use?. Asian J Androl 2015 Mar-Apr;17(2):230-5.
- Iizuka-Hishikawa Y, Hishikawa D, Sasaki J, Takubo K, Goto M, Nagata K, Nakanishi H, Shindou H, Okamura T, Ito C, Toshimori K, Sasaki T, Shimizu T. Lysophosphatidic acid acyltransferase 3 tunes the membrane status of germ cells by incorporating docosahexaenoic acid during spermatogenesis.. J Biol Chem 2017 Jul 21;292(29):12065-12076.
- García BM, Fernández LG, Ferrusola CO, Salazar-Sandoval C, Rodríguez AM, Martinez HR, Tapia JA, Morcuende D, Peña FJ. Membrane lipids of the stallion spermatozoon in relation to sperm quality and susceptibility to lipid peroxidation.. Reprod Domest Anim 2011 Feb;46(1):141-8.
- Wathes DC, Abayasekara DR, Aitken RJ. Polyunsaturated fatty acids in male and female reproduction.. Biol Reprod 2007 Aug;77(2):190-201.
- Broniec A, Klosinski R, Pawlak A, Wrona-Krol M, Thompson D, Sarna T. Interactions of plasmalogens and their diacyl analogs with singlet oxygen in selected model systems.. Free Radic Biol Med 2011 Apr 1;50(7):892-8.
- Alvarez JG, Storey BT. Differential incorporation of fatty acids into and peroxidative loss of fatty acids from phospholipids of human spermatozoa.. Mol Reprod Dev 1995 Nov;42(3):334-46.
- Arnhold J, Osipov AN, Spalteholz H, Panasenko OM, Schiller J. Formation of lysophospholipids from unsaturated phosphatidylcholines under the influence of hypochlorous acid.. Biochim Biophys Acta 2002 Aug 15;1572(1):91-100.
- 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 Dec;165(8):861-5.
- Saez F, Drevet JR. Dietary Cholesterol and Lipid Overload: Impact on Male Fertility.. Oxid Med Cell Longev 2019;2019:4521786.
- Samanta L, Parida R, Dias TR, Agarwal A. The enigmatic seminal plasma: a proteomics insight from ejaculation to fertilization.. Reprod Biol Endocrinol 2018 Apr 28;16(1):41.
- Bromfield JJ. Seminal fluid and reproduction: much more than previously thought.. J Assist Reprod Genet 2014 Jun;31(6):627-36.
- Lueders I, Luther I, Scheepers G, van der Horst G. Improved semen collection method for wild felids: urethral catheterization yields high sperm quality in African lions (Panthera leo).. Theriogenology 2012 Aug;78(3):696-701.
- World Health Organization. WHO laboratory manual for the examination and processing of human semen. Geneva: World Health Organization; 2010.
- Nimptsch A, Pyttel S, Paasch U, Mohr C, Heinrich JM, Schiller J. A MALDI MS investigation of the lysophosphatidylcholine/phosphatidylcholine ratio in human spermatozoa and erythrocytes as a useful fertility marker.. Lipids 2014 Mar;49(3):287-93.
- BLIGH EG, DYER WJ. A rapid method of total lipid extraction and purification.. Can J Biochem Physiol 1959 Aug;37(8):911-7.
- Fellmann P, Zachowski A, Devaux PF. Synthesis and use of spin-labeled lipids for studies of the transmembrane movement of phospholipids.. Methods Mol Biol 1994;27:161-75.
- Morrot G, Hervé P, Zachowski A, Fellmann P, Devaux PF. Aminophospholipid translocase of human erythrocytes: phospholipid substrate specificity and effect of cholesterol.. Biochemistry 1989 Apr 18;28(8):3456-62.
- 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 Feb 1;267(1):46-56.
- Petkovic M, Schiller J, Müller M, Benard S, Reichl S, Arnold K, Arnhold J. Detection of individual phospholipids in lipid mixtures by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry: phosphatidylcholine prevents the detection of further species.. Anal Biochem 2001 Feb 15;289(2):202-16.
- Liebisch G, Fahy E, Aoki J, Dennis EA, Durand T, Ejsing CS, Fedorova M, Feussner I, Griffiths WJ, Köfeler H, Merrill AH Jr, Murphy RC, O'Donnell VB, Oskolkova O, Subramaniam S, Wakelam MJO, Spener F. Update on LIPID MAPS classification, nomenclature, and shorthand notation for MS-derived lipid structures.. J Lipid Res 2020 Dec;61(12):1539-1555.
- Furland NE, Oresti GM, Antollini SS, Venturino A, Maldonado EN, Aveldaño MI. Very long-chain polyunsaturated fatty acids are the major acyl groups of sphingomyelins and ceramides in the head of mammalian spermatozoa.. J Biol Chem 2007 Jun 22;282(25):18151-18161.
- Cummins JM, Woodall PF. On mammalian sperm dimensions.. J Reprod Fertil 1985 Sep;75(1):153-75.
- 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 Mar 1;71(4):568-75.
- Esmaeili V, Shahverdi AH, Moghadasian MH, Alizadeh AR. Dietary fatty acids affect semen quality: a review.. Andrology 2015 May;3(3):450-61.
- Castellano CA, Audet I, Bailey JL, Chouinard PY, Laforest JP, Matte JJ. Effect of dietary n-3 fatty acids (fish oils) on boar reproduction and semen quality.. J Anim Sci 2010 Jul;88(7):2346-55.
- Speake BK, Surai PF, Rooke JA, Vriese SD, Christophe AB. Regulation of avian and mammalian sperm production by dietary fatty acids. 2003; In: De Vriese SR, Christophe AB, editors. Male Fertility and Lipid Metabolism. Champaign: AOCS Press; 2003. pp. 96–117.
- Svetlichnyy V, Müller P, Pomorski TG, 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 Jan;177:41-50.
- Klinovska K, Sebkova N, Dvorakova-Hortova K. Sperm-egg fusion: a molecular enigma of mammalian reproduction.. Int J Mol Sci 2014 Jun 13;15(6):10652-68.
- Müller K, Pomorski T, Müller P, Zachowski A, Herrmann A. Protein-dependent translocation of aminophospholipids and asymmetric transbilayer distribution of phospholipids in the plasma membrane of ram sperm cells.. Biochemistry 1994 Aug 23;33(33):9968-74.
- Robinson BS, Johnson DW, Poulos A. Novel molecular species of sphingomyelin containing 2-hydroxylated polyenoic very-long-chain fatty acids in mammalian testes and spermatozoa.. J Biol Chem 1992 Jan 25;267(3):1746-51.
- Fuchs B, Schiller J. MALDI-TOF MS analysis of lipids from cells, tissues and body fluids.. Subcell Biochem 2008;49:541-65.
- Aitken RJ. Impact of oxidative stress on male and female germ cells: implications for fertility.. Reproduction 2020 Apr;159(4):R189-R201.
- Fuchs B, Muller K, Paasch U, Schiller J. Lysophospholipids: potential markers of diseases and infertility?. Mini Rev Med Chem 2012 Jan;12(1):74-86.
- Brien M, Larose J, Greffard K, Julien P, Bilodeau JF. Increased placental phospholipase A(2) gene expression and free F(2)-isoprostane levels in response to oxidative stress in preeclampsia.. Placenta 2017 Jul;55:54-62.
- Lessig J, Fuchs B. Plasmalogens in biological systems: their role in oxidative processes in biological membranes, their contribution to pathological processes and aging and plasmalogen analysis.. Curr Med Chem 2009;16(16):2021-41.
- Ulrich K, Jakob U. The role of thiols in antioxidant systems.. Free Radic Biol Med 2019 Aug 20;140:14-27.
- Plante G, Prud'homme B, Fan J, Lafleur M, Manjunath P. Evolution and function of mammalian binder of sperm proteins.. Cell Tissue Res 2016 Jan;363(1):105-127.
- Suarez SS, Pacey AA. Sperm transport in the female reproductive tract.. Hum Reprod Update 2006 Jan-Feb;12(1):23-37.
- Rickard JP, de Graaf SP. Sperm surface changes and their consequences for sperm transit through the female reproductive tract.. Theriogenology 2020 Jul 1;150:96-105.
- Rickard JP, Pool KR, Druart X, de Graaf SP. The fate of spermatozoa in the female reproductive tract: A comparative review.. Theriogenology 2019 Oct 1;137:104-112.
- García-Vázquez FA, Gadea J, Matás C, Holt WV. Importance of sperm morphology during sperm transport and fertilization in mammals.. Asian J Androl 2016 Nov-Dec;18(6):844-850.
Citations
This article has been cited 2 times.- Horta Remedios M, Liang W, González LN, Li V, Da Ros VG, Cohen DJ, Zaremberg V. Ether lipids and a peroxisomal riddle in sperm.. Front Cell Dev Biol 2023;11:1166232.
- Li W, Mi S, Zhang J, Liu X, Chen S, Liu S, Feng X, Tang Y, Li Y, Liu L, Fang L, Zhang S, Yu Y. Integrating sperm cell transcriptome and seminal plasma metabolome to analyze the molecular regulatory mechanism of sperm motility in Holstein stud bulls.. J Anim Sci 2023 Jan 3;101.
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