Spatial segmentation and metabolite annotation involved in sperm maturation in the rat epididymis by MALDI imaging mass spectrometry.


Journal

Journal of mass spectrometry : JMS
ISSN: 1096-9888
Titre abrégé: J Mass Spectrom
Pays: England
ID NLM: 9504818

Informations de publication

Date de publication:
Dec 2020
Historique:
received: 10 10 2019
revised: 19 07 2020
accepted: 21 07 2020
entrez: 12 10 2020
pubmed: 13 10 2020
medline: 28 8 2021
Statut: ppublish

Résumé

Spermatozoa acquire their fertilizing capacity during a complex maturation process that occurs in the epididymis. This process involves a substantial molecular remodeling at the surface of the gamete. Epididymis is divided into three regions (the caput, corpus, and cauda) or into 19 intraregional segments based on histology. Most studies carried out on epididymal maturation have been performed on sperm samples or tissue extracts. Here, we used MALDI imaging mass spectrometry in the positive and negative ion modes combined with spatial segmentation and automated metabolite annotation to study the precise localization of metabolites directly in the rat epididymis. The spatial segmentation revealed that the rat epididymis could be divided into several molecular clusters different from the 19 intraregional segments. The discriminative m/z values that contributed the most to each molecular cluster were then annotated and corresponded mainly to phosphatidylcholines, sphingolipids, glycerophosphates, triacylglycerols, plasmalogens, phosphatidylethanolamines, and lysophosphatidylcholines. A substantial remodeling of lipid composition during epididymal maturation was observed. It was characterized in particular by an increase in the number of sphingolipids and plasmalogens and a decrease in the proportion of triacylglycerols annotated from caput to cauda. Ion images reveal that molecules belonging to the same family can have very different localizations along the epididymis. For some of them, annotation was confirmed by on-tissue MS/MS experiments. A 3D model of the epididymis head was reconstructed from 61 sections analyzed with a lateral resolution of 50 μm and can be used to obtain information on the localization of a given analyte in the whole volume of the tissue.

Identifiants

pubmed: 33043525
doi: 10.1002/jms.4633
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e4633

Subventions

Organisme : Biogenouest
Organisme : Conseil Regional de Bretagne
Organisme : Infrastructures en Biologie Sante et Agronomie (IBiSA)
Organisme : and Conseil Régional de Bretagne
Organisme : Biogenouest, Infrastructures en Biologie Santé et Agronomie (IBiSA)

Informations de copyright

© 2020 John Wiley & Sons, Ltd.

Références

Cornwall GA. New insights into epididymal biology and function. Hum Reprod Update. 2009;15:213-227.
Dacheux JL, Dacheux F. New insights into epididymal function in relation to sperm maturation. Reproduction. 2014;147(2):R27-R42.
Jones R. Plasma membrane structure and remodelling during sperm maturation in the epididymis. J Reprod Fertil Suppl. 1998;53:73-84.
Kirchhoff C, Pera I, Derr P, Yeung CH, Cooper T. The molecular biology of the sperm surface. Post-testicular membrane remodelling. Adv Exp Med Biol. 1997;424:221-232.
Cleland K. The structure and function of the epididymis. 1. The histology of the rat epididymis. Aust J Zool. 1957;5(3):223-246.
Robaire B, Hermo L. Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: Knobil E, Neil J, eds. The Physiology of Reproduction. New York: Raven Press; 1988:1000-1080.
Kirchhoff C. Gene expression in the epididymis. Int Rev Cytol. 1999;188:133-202.
Turner TT, Bomgardner D, Jacobs JP, Nguyen QA. Association of segmentation of the epididymal interstitium with segmented tubule function in rats and mice. Reproduction. 2003;125(6):871-878.
Jelinsky SA, Turner TT, Bang HJ, et al. The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol Reprod. 2007;76(4):561-570.
Jervis KM, Robaire B. Dynamic changes in gene expression along the rat epididymis. Biol Reprod. 2001;65(3):696-703.
Guyonnet B, Dacheux F, Dacheux J-L, Gatti J-L. The epididymal transcriptome and proteome provide some insights into new epididymal regulations. J Androl. 2011;32(6):651-664.
Gervasi MG, Visconti PE. Molecular changes and signaling events occurring in spermatozoa during epididymal maturation. Andrology. 2017;5(2):204-218.
Yuan H, Liu A, Zhang L, et al. Proteomic profiling of regionalized proteins in rat epididymis indicates consistency between specialized distribution and protein functions. J Proteome Res. 2006;5(2):299-307.
Hu S-G, Liang A-J, Yao G-X, et al. The dynamic metabolomic changes throughout mouse epididymal lumen fluid potentially contribute to sperm maturation. Andrology. 2018;6(1):247-255.
Kim N, Nakamura H, Masaki H, Kumasawa K, Hirano K-I, Kimura T. Effect of lipid metabolism on male fertility. Biochem Biophys Res Commun. 2017;485(3):686-692.
Haidl G, Opper C. Changes in lipids and membrane anisotropy in human spermatozoa during epididymal maturation. Hum Reprod. 1997;12(12):2720-2723.
Pyttel S, Nimptsch A, Böttger J, et al. Changes of murine sperm phospholipid composition during epididymal maturation determined by MALDI-TOF mass spectrometry. Theriogenology. 2014;82(3):396-402.
Sato H, Taketomi Y, Isogai Y, et al. Group III secreted phospholipase A2 regulates epididymal sperm maturation and fertility in mice. J Clin Invest. 2010;120(5):1400-1414.
Rejraji H, Sion B, Prensier G, et al. Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod. 2006;74(6):1104-1113.
Lagarrigue M, Lavigne R, Guevel B, Com E, Chaurand P, Pineau C. Matrix-assisted laser desorption/ionization imaging mass spectrometry: a promising technique for reproductive research. Biol Reprod. 2012;86(3):1-11, 74.
Chaurand P, Fouchecourt S, DaGue BB, et al. Profiling and imaging proteins in the mouse epididymis by imaging mass spectrometry. Proteomics. 2003;3(11):2221-2239.
Ryan DJ, Nei D, Prentice BM, Rose KL, Caprioli RM, Spraggins JM. Protein identification in imaging mass spectrometry through spatially targeted liquid micro-extractions. Rapid Commun Mass Spectrom. 2018;32(5):442-450.
Crecelius AC, Schubert US, von Eggeling F. MALDI mass spectrometric imaging meets “omics”: recent advances in the fruitful marriage. Analyst. 2015;140(17):5806-5820.
Palmer A, Phapale P, Chernyavsky I, et al. FDR-controlled metabolite annotation for high-resolution imaging mass spectrometry. Nat Methods. 2017;14(1):57-60.
Crecelius AC, Cornett DS, Caprioli RM, Williams B, Dawant BM, Bodenheimer B. Three-dimensional visualization of protein expression in mouse brain structures using imaging mass spectrometry. J Am Soc Mass Spectrom. 2005;16(7):1093-1099.
Andersson M, Groseclose MR, Deutch AY, Caprioli RM. Imaging mass spectrometry of proteins and peptides: 3D volume reconstruction. Nat Methods. 2008;5(1):101-108.
Seeley EH, Caprioli RM. 3D imaging by mass spectrometry: a new frontier. Anal Chem. 2012;84(5):2105-2110.
Palmer AD, Alexandrov T. Serial 3D imaging mass spectrometry at its tipping point. Anal Chem. 2015;87(8):4055-4062.
Oetjen J, Veselkov K, Watrous J, et al. Benchmark datasets for 3D MALDI- and DESI-imaging mass spectrometry. Gigascience. 2015;4(1):1-7, 20.
Jones EE, Quiason C, Dale S, Shahidi-Latham SK. Feasibility assessment of a MALDI FTICR imaging approach for the 3D reconstruction of a mouse lung. J Am Soc Mass Spectrom. 2017;28(8):1709-1715.
Alexandrov T, Kobarg JH. Efficient spatial segmentation of large imaging mass spectrometry datasets with spatially aware clustering. Bioinformatics. 2011;27(13):i230-i238.
Klein O, Strohschein K, Nebrich G, et al. MALDI imaging mass spectrometry: discrimination of pathophysiological regions in traumatized skeletal muscle by characteristic peptide signatures. Proteomics. 2014;14(20):2249-2260.
Deininger SO, Ebert MP, Futterer A, Gerhard M, Rocken C. MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers. J Proteome Res. 2008;7(12):5230-5236.
Trede D, Schiffler S, Becker M, et al. Exploring three-dimensional matrix-assisted laser desorption/ionization imaging mass spectrometry data: three-dimensional spatial segmentation of mouse kidney. Anal Chem. 2012;84(14):6079-6087.
Rauser S, Marquardt C, Balluff B, et al. Classification of HER2 receptor status in breast cancer tissues by MALDI imaging mass spectrometry. J Proteome Res. 2010;9(4):1854-1863.
Lotz JM, Hoffmann F, Lotz J, et al. Integration of 3D multimodal imaging data of a head and neck cancer and advanced feature recognition. Biochim Biophys Acta Proteins Proteomics. 2017;1865(7):946-956.
Cornett DS, Reyzer ML, Chaurand P, Caprioli RM. MALDI imaging mass spectrometry: molecular snapshots of biochemical systems. Nat Methods. 2007;4(10):828-833.
De Grava Kempinas W, Klinefelter GR. Interpreting histopathology in the epididymis. Spermatogenesis. 2014;4(2):e979114.
Fuchs B, Jakop U, Göritz F, et al. MALDI-TOF “fingerprint” phospholipid mass spectra allow the differentiation between ruminantia and feloideae spermatozoa. Theriogenology. 2009;71(4):568-575.
Busik JV, Reid GE, Lydic TA. Global analysis of retina lipids by complementary precursor ion and neutral loss mode tandem mass spectrometry. Methods Mol Biol. 2009;579:33-70.
Fuchs B, Muller K, Paasch U, Schiller J. Lysophospholipids: potential markers of diseases and infertility? Mini Rev Med Chem. 2012;12(1):74-86.
Cross NL. Sphingomyelin modulates capacitation of human sperm in vitro. Biol Reprod. 2000;63(4):1129-1134.
Masaki H, Kim N, Nakamura H, et al. Long-chain fatty acid triglyceride (TG) metabolism disorder impairs male fertility: a study using adipose triglyceride lipase deficient mice. Mol Hum Reprod. 2017;23(7):452-460.
Alvarez JG, Storey BT, Hemling ML, Grob RL. High-resolution proton nuclear magnetic resonance characterization of seminolipid from bovine spermatozoa. J Lipid Res. 1990;31:1073-1081.
Attar M, Kates M, Bou Khalil M, Carrier D, Wong PT, Tanphaichitr N. A Fourier-transform infrared study of the interaction between germ-cell specific sulfogalactosylglycerolipid and dimyristoylglycerophosphocholine. Chem Phys Lipids. 2000;106(2):101-114.
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;10:1-12, 1344.
Tanphaichitr N, Kongmanas K, Faull KF, et al. Properties, metabolism and roles of sulfogalactosylglycerolipid in male reproduction. Prog Lipid Res. 2018;72:18-41.
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.
Leopold J, Popkova Y, Engel KM, Schiller J. Recent developments of useful MALDI matrices for the mass spectrometric characterization of lipids. Biomolecules. 2018;8(4):1-25, 173.

Auteurs

Mélanie Lagarrigue (M)

Univ Rennes, Inserm, EHESP, Irset (Institut de recherche en santé, environnement et travail), UMR_S 1085, Rennes Cedex, F-35042, France.
Protim, Univ Rennes, Rennes Cedex, F-35042, France.

Régis Lavigne (R)

Univ Rennes, Inserm, EHESP, Irset (Institut de recherche en santé, environnement et travail), UMR_S 1085, Rennes Cedex, F-35042, France.
Protim, Univ Rennes, Rennes Cedex, F-35042, France.

Blandine Guével (B)

Univ Rennes, Inserm, EHESP, Irset (Institut de recherche en santé, environnement et travail), UMR_S 1085, Rennes Cedex, F-35042, France.
Protim, Univ Rennes, Rennes Cedex, F-35042, France.

Andrew Palmer (A)

Structural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany.

Karine Rondel (K)

Univ Rennes, Inserm, EHESP, Irset (Institut de recherche en santé, environnement et travail), UMR_S 1085, Rennes Cedex, F-35042, France.
Protim, Univ Rennes, Rennes Cedex, F-35042, France.

Jan H Kobarg (JH)

Bruker Daltonik/SCiLS GmbH, Bremen, Germany.

Dennis Trede (D)

Bruker Daltonik/SCiLS GmbH, Bremen, Germany.

Charles Pineau (C)

Univ Rennes, Inserm, EHESP, Irset (Institut de recherche en santé, environnement et travail), UMR_S 1085, Rennes Cedex, F-35042, France.
Protim, Univ Rennes, Rennes Cedex, F-35042, France.

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