Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2021

Open Access 01-12-2021 | Research

High-coverage targeted lipidomics revealed dramatic lipid compositional changes in asthenozoospermic spermatozoa and inverse correlation of ganglioside GM3 with sperm motility

Authors: Shuqiang Chen, Ming Wang, Li Li, Jun Wang, Xuhui Ma, Hengde Zhang, Yang Cai, Bin Kang, Jianlei Huang, Bo Li

Published in: Reproductive Biology and Endocrinology | Issue 1/2021

Login to get access

Abstract

Background

It has been previously demonstrated that cholesterol content and cholesterol/phospholipid ratio were significantly higher in asthenozoospermia and oligoasthenoteratozoospermia. The majority of published studies have investigated the fatty acid composition of phospholipids rather than lipids themselves. This study evaluated the lipid composition of asthenozoospermic and normozoospermic spermatozoa, and identified the exact lipid species that correlated with sperm motility.

Methods

A total of 12 infertile asthenozoospermia patients and 12 normozoospermia subjects with normal sperm motility values were tested for semen volume, sperm concentration, count, motility, vitality and morphology. High-coverage targeted lipidomics with 25 individual lipid classes was performed to analyze the sperm lipid components and establish the exact lipid species that correlated with sperm motility.

Results

A total of 25 individual lipid classes and 479 lipid molecular species were identified and quantified. Asthenozoospermic spermatozoa showed an increase in the level of four lipid classes, including Cho, PE, LPI and GM3. A total of 48 lipid molecular species were significantly altered between normozoospermic and asthenozoospermic spermatozoa. Furthermore, the levels of total GM3 and six GM3 molecular species, which were altered in normozoospermic spermatozoa versus asthenozoospermic spermatozoa, were inversely correlated with sperm progressive and total motility.

Conclusions

Several unique lipid classes and lipid molecular species were significantly altered between asthenozoospermic and normozoospermic spermatozoa, revealing new possibilities for further mechanistic pursuits and highlighting the development needs of culture medium formulations to improve sperm motility.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bolla JR, Agasid MT, Mehmood S, Robinson CV. Membrane Protein-Lipid Interactions Probed Using Mass Spectrometry. Annu Rev Biochem. 2019;88:85–111.CrossRef Bolla JR, Agasid MT, Mehmood S, Robinson CV. Membrane Protein-Lipid Interactions Probed Using Mass Spectrometry. Annu Rev Biochem. 2019;88:85–111.CrossRef
2.
go back to reference Schuhmacher M, Grasskamp AT, Barahtjan P, Wagner N, Lombardot B, Schuhmacher JS, Sala P, Lohmann A, Henry I, Shevchenko A, et al. Live-cell lipid biochemistry reveals a role of diacylglycerol side-chain composition for cellular lipid dynamics and protein affinities. Proc Natl Acad Sci U S A. 2020;117:7729–38.CrossRef Schuhmacher M, Grasskamp AT, Barahtjan P, Wagner N, Lombardot B, Schuhmacher JS, Sala P, Lohmann A, Henry I, Shevchenko A, et al. Live-cell lipid biochemistry reveals a role of diacylglycerol side-chain composition for cellular lipid dynamics and protein affinities. Proc Natl Acad Sci U S A. 2020;117:7729–38.CrossRef
3.
go back to reference Grouleff J, Irudayam SJ, Skeby KK, Schiott B. The influence of cholesterol on membrane protein structure, function, and dynamics studied by molecular dynamics simulations. Biochim Biophys Acta. 2015;1848:1783–95.CrossRef Grouleff J, Irudayam SJ, Skeby KK, Schiott B. The influence of cholesterol on membrane protein structure, function, and dynamics studied by molecular dynamics simulations. Biochim Biophys Acta. 2015;1848:1783–95.CrossRef
4.
go back to reference Casares D, Escriba PV, Rossello CA. Membrane Lipid Composition: Effect on Membrane and Organelle Structure, Function and Compartmentalization and Therapeutic Avenues. Int J Mol Sci. 2019;20:2167. Casares D, Escriba PV, Rossello CA. Membrane Lipid Composition: Effect on Membrane and Organelle Structure, Function and Compartmentalization and Therapeutic Avenues. Int J Mol Sci. 2019;20:2167.
5.
go back to reference Nielson JR, Rutter JP. Lipid-mediated signals that regulate mitochondrial biology. J Biol Chem. 2018;293:7517–21.CrossRef Nielson JR, Rutter JP. Lipid-mediated signals that regulate mitochondrial biology. J Biol Chem. 2018;293:7517–21.CrossRef
6.
go back to reference 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;2:246–256. 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;2:246–256.
7.
go back to reference Salvolini E, Buldreghini E, Lucarini G, Vignini A, Lenzi A, Di Primio R, Balercia G. Involvement of sperm plasma membrane and cytoskeletal proteins in human male infertility. Fertil Steril 2013;99:697–704. Salvolini E, Buldreghini E, Lucarini G, Vignini A, Lenzi A, Di Primio R, Balercia G. Involvement of sperm plasma membrane and cytoskeletal proteins in human male infertility. Fertil Steril 2013;99:697–704.
8.
go back to reference Lucio CF, Brito MM, Angrimani D, Belaz K, Morais D, Zampieri D, Losano J, Assumpcao M, Nichi M, Eberlin MN, Vannucchi CI. Lipid composition of the canine sperm plasma membrane as markers of sperm motility. Reprod Domest Anim. 2017;52(Suppl 2):208–13.CrossRef Lucio CF, Brito MM, Angrimani D, Belaz K, Morais D, Zampieri D, Losano J, Assumpcao M, Nichi M, Eberlin MN, Vannucchi CI. Lipid composition of the canine sperm plasma membrane as markers of sperm motility. Reprod Domest Anim. 2017;52(Suppl 2):208–13.CrossRef
9.
go back to reference Rivera-Egea R, Garrido N, Sota N, Meseguer M, Remohi J, Dominguez F. Sperm lipidic profiles differ significantly between ejaculates resulting in pregnancy or not following intracytoplasmic sperm injection. J Assist Reprod Genet. 2018;35:1973–85.CrossRef Rivera-Egea R, Garrido N, Sota N, Meseguer M, Remohi J, Dominguez F. Sperm lipidic profiles differ significantly between ejaculates resulting in pregnancy or not following intracytoplasmic sperm injection. J Assist Reprod Genet. 2018;35:1973–85.CrossRef
10.
go back to reference Andersen JM, Ronning PO, Herning H, Bekken SD, Haugen TB, Witczak O. Fatty acid composition of spermatozoa is associated with BMI and with semen quality. Andrology 2016;4:857–865. Andersen JM, Ronning PO, Herning H, Bekken SD, Haugen TB, Witczak O. Fatty acid composition of spermatozoa is associated with BMI and with semen quality. Andrology 2016;4:857–865.
11.
go back to reference Aksoy Y, Aksoy H, Altinkaynak K, Aydin HR, Ozkan A. Sperm fatty acid composition in subfertile men. Prostaglandins Leukot Essent Fatty Acids 2006;75:75–79. Aksoy Y, Aksoy H, Altinkaynak K, Aydin HR, Ozkan A. Sperm fatty acid composition in subfertile men. Prostaglandins Leukot Essent Fatty Acids 2006;75:75–79.
12.
go back to reference Garolla A, Sabovic I, Tescari S, De Toni L, Menegazzo M, Cosci I, De Filippis V, Giarola M, Foresta C. Impaired sperm function in infertile men relies on the membrane sterol pattern. Andrology 2018;6:325–334. Garolla A, Sabovic I, Tescari S, De Toni L, Menegazzo M, Cosci I, De Filippis V, Giarola M, Foresta C. Impaired sperm function in infertile men relies on the membrane sterol pattern. Andrology 2018;6:325–334.
13.
go back to reference Choy JT, Eisenberg ML. Male infertility as a window to health. Fertil Steril 2018, 110:810–814. Choy JT, Eisenberg ML. Male infertility as a window to health. Fertil Steril 2018, 110:810–814.
14.
go back to reference 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;69:403–17. 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;69:403–17.
15.
go back to reference Shahrokhi SZ, Salehi P, Alyasin A, Taghiyar S, Deemeh MR. Asthenozoospermia: Cellular and molecular contributing factors and treatment strategies. Andrologia 2020;52:e13463. Shahrokhi SZ, Salehi P, Alyasin A, Taghiyar S, Deemeh MR. Asthenozoospermia: Cellular and molecular contributing factors and treatment strategies. Andrologia 2020;52:e13463.
16.
go back to reference Zerbinati C, Caponecchia L, Rago R, Leoncini E, Bottaccioli AG, Ciacciarelli M, Pacelli A, Salacone P, Sebastianelli A, Pastore A, et al: Fatty acids profiling reveals potential candidate markers of semen quality. Andrology 2016;4:1094–1101. Zerbinati C, Caponecchia L, Rago R, Leoncini E, Bottaccioli AG, Ciacciarelli M, Pacelli A, Salacone P, Sebastianelli A, Pastore A, et al: Fatty acids profiling reveals potential candidate markers of semen quality. Andrology 2016;4:1094–1101.
17.
go back to reference Tavilani H, Doosti M, Nourmohammadi I, Mahjub H, Vaisiraygani A, Salimi S, Hosseinipanah SM. Lipid composition of spermatozoa in normozoospermic and asthenozoospermic males. Prostaglandins Leukot Essent Fatty Acids 2007;77:45–50. Tavilani H, Doosti M, Nourmohammadi I, Mahjub H, Vaisiraygani A, Salimi S, Hosseinipanah SM. Lipid composition of spermatozoa in normozoospermic and asthenozoospermic males. Prostaglandins Leukot Essent Fatty Acids 2007;77:45–50.
18.
go back to reference Wenk MR. Lipidomics: new tools and applications. Cell 2010;143:888–895. Wenk MR. Lipidomics: new tools and applications. Cell 2010;143:888–895.
19.
go back to reference Wang R, Li B, Lam SM, Shui G. Integration of lipidomics and metabolomics for in-depth understanding of cellular mechanism and disease progression. J Genet Genomics. 2020;47:69–83.CrossRef Wang R, Li B, Lam SM, Shui G. Integration of lipidomics and metabolomics for in-depth understanding of cellular mechanism and disease progression. J Genet Genomics. 2020;47:69–83.CrossRef
20.
go back to reference Lam SM, Tian H, Shui G. Lipidomics, en route to accurate quantitation. Biochim Biophys Acta Mol Cell Biol Lipids. 2017;1862:752–61. Lam SM, Tian H, Shui G. Lipidomics, en route to accurate quantitation. Biochim Biophys Acta Mol Cell Biol Lipids. 2017;1862:752–61.
21.
go back to reference Lam SM, Wang Z, Li B, Shui G. High-coverage lipidomics for functional lipid and pathway analyses. Anal Chim Acta. 2021;1147:199–210.CrossRef Lam SM, Wang Z, Li B, Shui G. High-coverage lipidomics for functional lipid and pathway analyses. Anal Chim Acta. 2021;1147:199–210.CrossRef
22.
go back to reference Evans HC, Dinh TTN, Hardcastle ML, Gilmore AA, Ugur MR, Hitit M, Jousan FD, Nicodemus MC, Memili E. Advancing Semen Evaluation Using Lipidomics. Front Vet Sci. 2021;8:601794.CrossRef Evans HC, Dinh TTN, Hardcastle ML, Gilmore AA, Ugur MR, Hitit M, Jousan FD, Nicodemus MC, Memili E. Advancing Semen Evaluation Using Lipidomics. Front Vet Sci. 2021;8:601794.CrossRef
23.
go back to reference Lee HC, Yokomizo T. Applications of mass spectrometry-based targeted and non-targeted lipidomics. Biochem Biophys Res Commun. 2018;504:576–81.CrossRef Lee HC, Yokomizo T. Applications of mass spectrometry-based targeted and non-targeted lipidomics. Biochem Biophys Res Commun. 2018;504:576–81.CrossRef
24.
go back to reference Lam SM, Tong L, Duan X, Petznick A, Wenk MR, Shui G. Extensive characterization of human tear fluid collected using different techniques unravels the presence of novel lipid amphiphiles. J Lipid Res. 2014;55:289–98.CrossRef Lam SM, Tong L, Duan X, Petznick A, Wenk MR, Shui G. Extensive characterization of human tear fluid collected using different techniques unravels the presence of novel lipid amphiphiles. J Lipid Res. 2014;55:289–98.CrossRef
25.
go back to reference Song JW, Lam SM, Fan X, Cao WJ, Wang SY, Tian H, Chua GH, Zhang C, Meng FP, Xu Z, et al. Omics-Driven Systems Interrogation of Metabolic Dysregulation in COVID-19 Pathogenesis. Cell Metab. 2020;32:188–202. e185. Song JW, Lam SM, Fan X, Cao WJ, Wang SY, Tian H, Chua GH, Zhang C, Meng FP, Xu Z, et al. Omics-Driven Systems Interrogation of Metabolic Dysregulation in COVID-19 Pathogenesis. Cell Metab. 2020;32:188–202. e185.
26.
go back to reference World Medical A. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 2013;310:2191–2194. World Medical A. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 2013;310:2191–2194.
27.
go back to reference Cao X, Wei R, Zhang X, Zhou J, Lou J, Cui Y. Impact of human papillomavirus infection in semen on sperm progressive motility in infertile men: a systematic review and meta-analysis. Reprod Biol Endocrinol 2020, 18:38. Cao X, Wei R, Zhang X, Zhou J, Lou J, Cui Y. Impact of human papillomavirus infection in semen on sperm progressive motility in infertile men: a systematic review and meta-analysis. Reprod Biol Endocrinol 2020, 18:38.
28.
go back to reference Banyra O, Nikitin O, Ventskivska I: Acute epididymo-orchitis: relevance of local classification and partner’s follow-up. Cent European J Urol 2019;72:324–329. Banyra O, Nikitin O, Ventskivska I: Acute epididymo-orchitis: relevance of local classification and partner’s follow-up. Cent European J Urol 2019;72:324–329.
29.
go back to reference Pereira R, Sa R, Barros A, Sousa M. Major regulatory mechanisms involved in sperm motility. Asian J Androl. 2017;19:5–14.PubMed Pereira R, Sa R, Barros A, Sousa M. Major regulatory mechanisms involved in sperm motility. Asian J Androl. 2017;19:5–14.PubMed
30.
go back to reference Ahammad MU, Jarrell ZR, Benson AP. Sperm Collection of Differential Quality Using Density Gradient Centrifugation. J Vis Exp. 2018;141:e58833. Ahammad MU, Jarrell ZR, Benson AP. Sperm Collection of Differential Quality Using Density Gradient Centrifugation. J Vis Exp. 2018;141:e58833.
31.
go back to reference Shui G, Stebbins JW, Lam BD, Cheong WF, Lam SM, Gregoire F, Kusonoki J, Wenk MR. Comparative plasma lipidome between human and cynomolgus monkey: are plasma polar lipids good biomarkers for diabetic monkeys? PLoS One. 2011;6:e19731.CrossRef Shui G, Stebbins JW, Lam BD, Cheong WF, Lam SM, Gregoire F, Kusonoki J, Wenk MR. Comparative plasma lipidome between human and cynomolgus monkey: are plasma polar lipids good biomarkers for diabetic monkeys? PLoS One. 2011;6:e19731.CrossRef
32.
go back to reference Lam SM, Wang Y, Duan X, Wenk MR, Kalaria RN, Chen CP, Lai MK, Shui G. Brain lipidomes of subcortical ischemic vascular dementia and mixed dementia. Neurobiol Aging 2014;35:2369–2381. Lam SM, Wang Y, Duan X, Wenk MR, Kalaria RN, Chen CP, Lai MK, Shui G. Brain lipidomes of subcortical ischemic vascular dementia and mixed dementia. Neurobiol Aging 2014;35:2369–2381.
33.
go back to reference Shui G, Guan XL, Low CP, Chua GH, Goh JS, Yang H, Wenk MR. Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry: application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol Biosyst 2010, 6:1008–1017. Shui G, Guan XL, Low CP, Chua GH, Goh JS, Yang H, Wenk MR. Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry: application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol Biosyst 2010, 6:1008–1017.
34.
go back to reference Wang W, Xin J, Yang X, Lam SM, Shui G, Wang Y, Huang X: Lipid-gene regulatory network reveals coregulations of triacylglycerol with phosphatidylinositol/lysophosphatidylinositol and with hexosyl-ceramide. Biochim Biophys Acta Mol Cell Biol Lipids 2019, 1864:168–180. Wang W, Xin J, Yang X, Lam SM, Shui G, Wang Y, Huang X: Lipid-gene regulatory network reveals coregulations of triacylglycerol with phosphatidylinositol/lysophosphatidylinositol and with hexosyl-ceramide. Biochim Biophys Acta Mol Cell Biol Lipids 2019, 1864:168–180.
35.
go back to reference Chicco AJ, Sparagna GC. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol. 2007;292:C33–44.CrossRef Chicco AJ, Sparagna GC. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol. 2007;292:C33–44.CrossRef
36.
go back to reference Julienne CM, Tardieu M, Chevalier S, Pinault M, Bougnoux P, Labarthe F, Couet C, Servais S, Dumas JF. Cardiolipin content is involved in liver mitochondrial energy wasting associated with cancer-induced cachexia without the involvement of adenine nucleotide translocase. Biochim Biophys Acta. 2014;1842:726–33.CrossRef Julienne CM, Tardieu M, Chevalier S, Pinault M, Bougnoux P, Labarthe F, Couet C, Servais S, Dumas JF. Cardiolipin content is involved in liver mitochondrial energy wasting associated with cancer-induced cachexia without the involvement of adenine nucleotide translocase. Biochim Biophys Acta. 2014;1842:726–33.CrossRef
37.
go back to reference Zheng C, Terreni M, Sollogoub M, Zhang Y. Ganglioside GM3 and Its Role in Cancer. Curr Med Chem. 2019;26:2933–47.CrossRef Zheng C, Terreni M, Sollogoub M, Zhang Y. Ganglioside GM3 and Its Role in Cancer. Curr Med Chem. 2019;26:2933–47.CrossRef
38.
go back to reference Craig LB, Brush RS, Sullivan MT, Zavy MT, Agbaga MP, Anderson RE. Decreased very long chain polyunsaturated fatty acids in sperm correlates with sperm quantity and quality. J Assist Reprod Genet 2019, 36:1379–1385. Craig LB, Brush RS, Sullivan MT, Zavy MT, Agbaga MP, Anderson RE. Decreased very long chain polyunsaturated fatty acids in sperm correlates with sperm quantity and quality. J Assist Reprod Genet 2019, 36:1379–1385.
39.
go back to reference Lopalco P, Vitale R, Cho YS, 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. Lopalco P, Vitale R, Cho YS, 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.
40.
go back to reference Cohen R, Buttke DE, Asano A, Mukai C, Nelson JL, Ren D, Miller RJ, Cohen-Kutner M, Atlas D, Travis AJ. Lipid modulation of calcium flux through CaV2.3 regulates acrosome exocytosis and fertilization. Dev Cell 2014;28:310–321. Cohen R, Buttke DE, Asano A, Mukai C, Nelson JL, Ren D, Miller RJ, Cohen-Kutner M, Atlas D, Travis AJ. Lipid modulation of calcium flux through CaV2.3 regulates acrosome exocytosis and fertilization. Dev Cell 2014;28:310–321.
41.
go back to reference Saez F, Whitfield M, Drevet JR. Impairment of sperm maturation and capacitation due to diet-dependent cholesterol overload. Andrology 2019;7:654–661. Saez F, Whitfield M, Drevet JR. Impairment of sperm maturation and capacitation due to diet-dependent cholesterol overload. Andrology 2019;7:654–661.
42.
go back to reference Lipina C, Hundal HS. Ganglioside GM3 as a gatekeeper of obesity-associated insulin resistance: Evidence and mechanisms. FEBS Lett 2015;589:3221–3227. Lipina C, Hundal HS. Ganglioside GM3 as a gatekeeper of obesity-associated insulin resistance: Evidence and mechanisms. FEBS Lett 2015;589:3221–3227.
43.
go back to reference Cardona C, Neri QV, Simpson AJ, Moody MA, Ostermeier GC, Seaman EK, Paniza T, Rosenwaks Z, Palermo GD, Travis AJ. Localization patterns of the ganglioside GM1 in human sperm are indicative of male fertility and independent of traditional semen measures. Mol Reprod Dev. 2017;84:423–35.CrossRef Cardona C, Neri QV, Simpson AJ, Moody MA, Ostermeier GC, Seaman EK, Paniza T, Rosenwaks Z, Palermo GD, Travis AJ. Localization patterns of the ganglioside GM1 in human sperm are indicative of male fertility and independent of traditional semen measures. Mol Reprod Dev. 2017;84:423–35.CrossRef
44.
go back to reference Hwang SU, Jeon Y, Yoon JD, Cai L, Kim E, Yoo H, Kim KJ, Park KM, Jin M, Kim H, Hyun SH. Effect of ganglioside GT1b on the in vitro maturation of porcine oocytes and embryonic development. J Reprod Dev. 2015;61:549–57.CrossRef Hwang SU, Jeon Y, Yoon JD, Cai L, Kim E, Yoo H, Kim KJ, Park KM, Jin M, Kim H, Hyun SH. Effect of ganglioside GT1b on the in vitro maturation of porcine oocytes and embryonic development. J Reprod Dev. 2015;61:549–57.CrossRef
45.
go back to reference Zhuo D, Guan F. Ganglioside GM1 promotes contact inhibition of growth by regulating the localization of epidermal growth factor receptor from glycosphingolipid-enriched microdomain to caveolae. Cell Prolif. 2019;52:e12639. Zhuo D, Guan F. Ganglioside GM1 promotes contact inhibition of growth by regulating the localization of epidermal growth factor receptor from glycosphingolipid-enriched microdomain to caveolae. Cell Prolif. 2019;52:e12639.
46.
go back to reference Prokazova NV, Samovilova NN, Gracheva EV, Golovanova NK. Ganglioside GM3 and its biological functions. Biochemistry (Mosc) 2009;74:235–249. Prokazova NV, Samovilova NN, Gracheva EV, Golovanova NK. Ganglioside GM3 and its biological functions. Biochemistry (Mosc) 2009;74:235–249.
47.
go back to reference Miranda PV, Allaire A, Sosnik J, Visconti PE. Localization of low-density detergent-resistant membrane proteins in intact and acrosome-reacted mouse sperm. Biol Reprod. 2009;80:897–904. Miranda PV, Allaire A, Sosnik J, Visconti PE. Localization of low-density detergent-resistant membrane proteins in intact and acrosome-reacted mouse sperm. Biol Reprod. 2009;80:897–904.
48.
go back to reference Bushway AA, Clegg ED, Keenan TW. Composition and synthesis of gangliosides in bovine testis, sperm and seminal plasma. Biol Reprod. 1977;17:432–442. Bushway AA, Clegg ED, Keenan TW. Composition and synthesis of gangliosides in bovine testis, sperm and seminal plasma. Biol Reprod. 1977;17:432–442.
49.
go back to reference Gore PJ, Singh SP, Brooks DE. Composition of gangliosides from ovine testis and spermatozoa. Biochim Biophys Acta. 1986;876:36–47.CrossRef Gore PJ, Singh SP, Brooks DE. Composition of gangliosides from ovine testis and spermatozoa. Biochim Biophys Acta. 1986;876:36–47.CrossRef
50.
go back to reference Mack SR, Zaneveld LJ, Peterson RN, Hunt W, Russell LD. Characterization of human sperm plasma membrane: glycolipids and polypeptides. J Exp Zool. 1987;243:339–346. Mack SR, Zaneveld LJ, Peterson RN, Hunt W, Russell LD. Characterization of human sperm plasma membrane: glycolipids and polypeptides. J Exp Zool. 1987;243:339–346.
51.
go back to reference Watanabe H, Takeda R, Hirota K, Kondoh G. Lipid raft dynamics linked to sperm competency for fertilization in mice. Genes Cells 2017;22:493–500. Watanabe H, Takeda R, Hirota K, Kondoh G. Lipid raft dynamics linked to sperm competency for fertilization in mice. Genes Cells 2017;22:493–500.
52.
go back to reference Kim BH, Ju WS, Kim JS, Kim SU, Park SJ, Ward SM, Lyu JH, Choo YK. Effects of Gangliosides on Spermatozoa, Oocytes, and Preimplantation Embryos. Int J Mol Sci. 2019;21:106. Kim BH, Ju WS, Kim JS, Kim SU, Park SJ, Ward SM, Lyu JH, Choo YK. Effects of Gangliosides on Spermatozoa, Oocytes, and Preimplantation Embryos. Int J Mol Sci. 2019;21:106.
53.
go back to reference Park HJ, Chae SK, Kim JW, Yang SG, Jung JM, Kim MJ, Wee G, Lee DS, Kim SU, Koo DB. Ganglioside GM3 induces cumulus cell apoptosis through inhibition of epidermal growth factor receptor-mediated PI3K/AKT signaling pathways during in vitro maturation of pig oocytes. Mol Reprod Dev. 2017;84:702–11.CrossRef Park HJ, Chae SK, Kim JW, Yang SG, Jung JM, Kim MJ, Wee G, Lee DS, Kim SU, Koo DB. Ganglioside GM3 induces cumulus cell apoptosis through inhibition of epidermal growth factor receptor-mediated PI3K/AKT signaling pathways during in vitro maturation of pig oocytes. Mol Reprod Dev. 2017;84:702–11.CrossRef
54.
go back to reference Tsutsumi O, Kurachi H, Oka T. A physiological role of epidermal growth factor in male reproductive function. Science 1986;233:975–977. Tsutsumi O, Kurachi H, Oka T. A physiological role of epidermal growth factor in male reproductive function. Science 1986;233:975–977.
55.
go back to reference Abe K, Eto K, Abe S. Epidermal growth factor mediates spermatogonial proliferation in newt testis. Reprod Biol Endocrinol. 2008;6:7.CrossRef Abe K, Eto K, Abe S. Epidermal growth factor mediates spermatogonial proliferation in newt testis. Reprod Biol Endocrinol. 2008;6:7.CrossRef
56.
go back to reference Furuya S, Endo Y, Oba M, Suzuki S, Nozawa S. Effect of epidermal growth factor on human sperm capacitation. Fertil Steril. 1993;60:905–910. Furuya S, Endo Y, Oba M, Suzuki S, Nozawa S. Effect of epidermal growth factor on human sperm capacitation. Fertil Steril. 1993;60:905–910.
57.
go back to reference Spalekova E, Makarevich AV, Lukac N. Ram Sperm Motility Parameters under The Influence of Epidermal Growth Factor. Vet Med Int. 2011;2011:642931.CrossRef Spalekova E, Makarevich AV, Lukac N. Ram Sperm Motility Parameters under The Influence of Epidermal Growth Factor. Vet Med Int. 2011;2011:642931.CrossRef
58.
go back to reference Ferreira G, Costa C, Bassaizteguy V, Santos M, Cardozo R, Montes J, Settineri R, Nicolson GL. Incubation of human sperm with micelles made from glycerophospholipid mixtures increases sperm motility and resistance to oxidative stress. PLoS One 2018;13:e0197897. Ferreira G, Costa C, Bassaizteguy V, Santos M, Cardozo R, Montes J, Settineri R, Nicolson GL. Incubation of human sperm with micelles made from glycerophospholipid mixtures increases sperm motility and resistance to oxidative stress. PLoS One 2018;13:e0197897.
Metadata
Title
High-coverage targeted lipidomics revealed dramatic lipid compositional changes in asthenozoospermic spermatozoa and inverse correlation of ganglioside GM3 with sperm motility
Authors
Shuqiang Chen
Ming Wang
Li Li
Jun Wang
Xuhui Ma
Hengde Zhang
Yang Cai
Bin Kang
Jianlei Huang
Bo Li
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2021
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-021-00792-3

Other articles of this Issue 1/2021

Reproductive Biology and Endocrinology 1/2021 Go to the issue