Changes in the lipid profile of hamster liver after Schistosoma mansoni infection, characterized by mass spectrometry imaging and LC-MS/MS analysis.
AP-SMALDI
Granuloma
Host-parasite interaction
Infection
Mass spectrometry imaging
Parasites
Schistosoma mansoni
Schistosomiasis
Journal
Analytical and bioanalytical chemistry
ISSN: 1618-2650
Titre abrégé: Anal Bioanal Chem
Pays: Germany
ID NLM: 101134327
Informations de publication
Date de publication:
May 2022
May 2022
Historique:
received:
14
10
2021
accepted:
03
03
2022
revised:
18
01
2022
pubmed:
24
3
2022
medline:
27
4
2022
entrez:
23
3
2022
Statut:
ppublish
Résumé
Schistosomiasis, caused by the human parasite Schistosoma mansoni, is one of the WHO-listed neglected tropical diseases (NTDs), and it has severe impact on morbidity and mortality, especially in Africa. Not only the adult worms but also their eggs are responsible for health problems. Up to 50% of the eggs produced by the female worms are not excreted with the feces but are trapped in the host tissue, such as the liver, where they provoke immune responses and a change in the lipid profile. We built up a database with 372 infection markers found in livers of S. mansoni-infected hamsters, using LC-MS/MS for identification, followed by statistical analysis. Most of them belong to the lipid classes of phosphatidylcholines (PCs), phosphatidylethanolamines (PEs), and triglycerides (TGs). We assigned some of these markers to specific anatomical structures by applying high-resolution MALDI MSI to cryosections of hamster liver and generating ion images based on the marker list from the LC-MS/MS experiments. Furthermore, enrichment and depletion of several markers were visualized.
Identifiants
pubmed: 35320368
doi: 10.1007/s00216-022-04006-6
pii: 10.1007/s00216-022-04006-6
pmc: PMC9035427
doi:
Substances chimiques
Lipids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3653-3665Subventions
Organisme : Hessisches Ministerium für Wissenschaft und Kunst
ID : LOEWE Center DRUID
Organisme : Deutsche Forschungsgemeinschaft
ID : INST 162/500-1 FUGG
Organisme : Deutsche Forschungsgemeinschaft
ID : RO3714/4-1
Organisme : Deutsche Forschungsgemeinschaft
ID : Sp314/13-1
Informations de copyright
© 2022. The Author(s).
Références
Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet. 2006;368(9541):1106–18.
pubmed: 16997665
doi: 10.1016/S0140-6736(06)69440-3
World Health Organization. Integrating neglected tropical diseases into global health and development: fourth WHO report on neglected tropical diseases. 2017.
World Health Organization. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. 2002.
Vale N, Gouveia MJ, Rinaldi G, Brindley PJ, Gartner F, da Costa JMC. Praziquantel for schistosomiasis: single-drug metabolism revisited, mode of action, and resistance. Antimicrob Agents Ch. 2017;61(5):16.
doi: 10.1128/AAC.02582-16
Caffrey CR. Chemotherapy of schistosomiasis: present and future. Curr Opin Chem Biol. 2007;11(4):433–9.
pubmed: 17652008
doi: 10.1016/j.cbpa.2007.05.031
Schramm G, Hamilton JV, Balog CIA, Wuhrer M, Gronow A, Beckmann S, Wippersteg V, Grevelding CG, Goldmann T, Weber E, Brattig NW, Deelder AM, Dunne DW, Hokke CH, Haas H, Doenhoff MJ. Molecular characterisation of kappa-5, a major antigenic glycoprotein from Schistosoma mansoni eggs. Mol Biochem Parasit. 2009;166(1):4–14.
doi: 10.1016/j.molbiopara.2009.02.003
Hams E, Aviello G, Fallon PG. The Schistosoma granuloma: friend or foe? Front Immunol. 2013;4:8.
doi: 10.3389/fimmu.2013.00089
Vella AT, Hulsebosch MD, Pearce EJ. Schistosoma-mansoni eggs induce antigen-responsive CD44-HI T-helper 2-cells and IL-4-secreting CD44-LO cells – Potential for T-helper 2 subset differentiation is evident at the precursor level. J Immunol. 1992;149(5):1714–22.
pubmed: 1387150
Adams DO. Granulomatous inflammatory response. Am J Pathol. 1976;84(1):164–91.
pubmed: 937513
pmcid: 2032357
Weinstock JV, Boros DL. Organ-dependent differences in composition and function observed in hepatic and intenstinal granulomas isolated from mice with schistosomiasis mansoni. J Immunol. 1983;130(1):418–22.
pubmed: 6600190
Wilson JL, Mayr HK, Weichhart T. Metabolic programming of macrophages: implications in the pathogenesis of granulomatous disease. Front Immunol. 2019;10:22.
doi: 10.3389/fimmu.2019.00022
Doenhoff MJ, Stanley RG, Griffiths K, Jackson CL. An anti-atherogenic effect of Schistosoma mansoni infections in mice associated with a parasite-induced lowering of blood total cholesterol. Parasitology. 2002;125:415–21.
pubmed: 12458825
doi: 10.1017/S0031182002002275
Da Silva FL, Del-Rei RP, Fraga DBM, Leony LM, de Souza A, Santos FLN. Alterations in the lipid profiles and circulating liver enzymes in individuals infected by Schistosoma mansoni. Rev Soc Bras Med. 2018;51(6):795–801.
doi: 10.1590/0037-8682-0113-2018
Anthony B, Mathieson W, de Castro-Borges W, Allen J. Schistosoma mansoni: egg-induced downregulation of hepatic stellate cell activation and fibrogenesis. Exp Parasitol. 2010;124(4):409–20.
pubmed: 20045695
doi: 10.1016/j.exppara.2009.12.009
Stanley RG, Jackson CL, Griffiths K, Doenhoff MJ. Effects of Schistosoma mansoni worms and eggs on circulating cholesterol and liver lipids in mice. Atherosclerosis. 2009;207(1):131–8.
pubmed: 19464685
doi: 10.1016/j.atherosclerosis.2009.04.037
Rustam YH, Reid GE. Analytical challenges and recent advances in mass spectrometry based lipidomics. Anal Chem. 2018;90(1):374–97.
pubmed: 29166560
doi: 10.1021/acs.analchem.7b04836
Li F, Qin XZ, Chen HQ, Qiu L, Guo YM, Liu H, Chen G, Song G, Wang X, Li F, Guo S, Wang B, Li Z. Lipid profiling for early diagnosis and progression of colorectal cancer using direct-infusion electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Rapid Commun Mass Spectrom. 2013;27(1):24–34.
pubmed: 23239314
doi: 10.1002/rcm.6420
Waldchen F, Mohr F, Wagner AH, Heiles S. Multifunctional reactive MALDI matrix enabling high-lateral resolution dual polarity ms imaging and lipid C=C position-resolved MS2 imaging. Anal Chem. 2020;92(20):14130–8.
pubmed: 32924439
doi: 10.1021/acs.analchem.0c03150
Surma MA, Herzog R, Vasilj A, Klose C, Christinat N, Morin-Rivron D, Simons K, Masoodi M, Sampaio JL. An automated shotgun lipidomics platform for high throughput, comprehensive, and quantitative analysis of blood plasma intact lipids. Eur J Lipid Sci Tech. 2015;117(10):1540–9.
doi: 10.1002/ejlt.201500145
Kadesch P, Quack T, Gerbig S, Grevelding CG, Spengler B. Tissue- and sex-specific lipidomic analysis of Schistosoma mansoni using high-resolution atmospheric pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging. Plos Neglect Trop D. 2020;14(5):17.
doi: 10.1371/journal.pntd.0008145
Giera M, Kaisar MMM, Derks RJE, Steenvoorden E, Kruize YCM, Hokke CH, Yazdanbakhsh M, Evert B. The Schistosoma mansoni lipidome: leads for immunomodulation. Anal Chim Acta. 2018;1037:107–18.
pubmed: 30292284
doi: 10.1016/j.aca.2017.11.058
Yang XY, Ding WM, Qian XY, Jiang PF, Chen QQ, Zhang X, Lu Y, Wu J, Sun F, Pan Z, Li X, Pan W. Schistosoma japonicum infection leads to the reprogramming of glucose and lipid metabolism in the colon of mice. Front Vet Sci. 2021;8:10.
Koestler M, Kirsch D, Hester A, Leisner A, Guenther S, Spengler B. A high-resolution scanning microprobe matrix-assisted laser desorption/ionization ion source for imaging analysis on an ion trap/Fourier transform ion cyclotron resonance mass spectrometer. Rapid Commun Mass Sp. 2008;22(20):3275–85.
doi: 10.1002/rcm.3733
Mokosch AS, Gerbig S, Grevelding CG, Haeberlein S, Spengler B. High-resolution AP-SMALDI MSI as a tool for drug imaging in Schistosoma mansoni. Anal Bioanal Chem. 2021;413(10):2755–66.
pubmed: 33723627
pmcid: 8007518
doi: 10.1007/s00216-021-03230-w
Xu YZ, Dresden MH. Schistosoma mansoni – Egg morphology and hatchability. J Parasitol. 1989;75(3):481–3.
pubmed: 2723933
doi: 10.2307/3282615
Grevelding CG. Genomic instability in Schistosoma mansoni. Mol Biochem Parasit. 1999;101(1–2):207–16.
doi: 10.1016/S0166-6851(99)00078-X
Roderfeld M, Padem S, Lichtenberger J, Quack T, Weiskirchen R, Longerich T, Schramm G, Churin Y, Irungbam K, Tschuschner A, Windhorst A, Grevelding CG, Roeb E. Schistosoma mansoniEgg-Secreted Antigens Activate Hepatocellular Carcinoma-Associated Transcription Factors c-Jun and STAT3 in Hamster and Human Hepatocytes. Hepatology. 2020;72(2):626–41.
pubmed: 30053321
doi: 10.1002/hep.30192
Weglage J, Wolters F, Hehr L, Lichtenberger J, Wulz C, Hempel F, Baier A, Quack T, Köhler K, Longerich T, Schramm G, Irungbam K, Mueller H, von Buelow V, TschuschnerA, Odenthal M, Drebber U, el Arousy M, Ramalho LNZ, Bankov K, Wild P, Pons-Kühnemann J, Tschammer J, Grevelding CG, Roeb E, Roderfeld M. Schistosoma mansoni eggs induce Wnt/beta-catenin signaling and activate the protooncogene c-Jun in human and hamster colon. Sci Rep. 2020;10(1):14.
Lu ZG, Sessler F, Holroyd N, Hahnel S, Quack T, Berriman M, Grevelding CG. Schistosome sex matters: a deep view into gonad-specific and pairing-dependent transcriptomes reveals a complex gender interplay. Sci Rep. 2016;6:14.
doi: 10.1038/s41598-016-0009-0
Lillie RD, Ashburn LL. Supersaturated solutions of fat stains in dilute isopropanol for demonstration of acute fatty degeneration not shown by Herxheimer’s technique. Arch Pathol. 1943;36:432–40.
Bouschen W, Schulz O, Eikel D, Spengler B. Matrix vapor deposition/recrystallization and dedicated spray preparation for high-resolution scanning microprobe matrix-assisted laser desorption/ionization imaging mass spectrometry (SMALDI-MS) of tissue and single cells. Rapid Commun Mass Spectrom. 2010;24(3):355–64.
pubmed: 20049881
doi: 10.1002/rcm.4401
Breitkopf SB, Taveira MD, Yuan M, Wuif GM, Asara JM. Serial-omics of P53-/-, Brca1-/- mouse breast tumor and normal mammary gland. Sci Rep. 2017;7:17.
doi: 10.1038/s41598-017-15132-y
Garikapati V, Colasante C, Baumgart-Vogt E, Spengler B. Sequential lipidomic, metabolomic and proteomic analyses of serum, liver and heart tissue specimens from peroxisomal biogenesis factor 11α knockout mice. Anal Bioanal Chem. 2022;414:2235–50.
pubmed: 35083512
pmcid: 8821073
doi: 10.1007/s00216-021-03860-0
Koelmel JP, Kroeger NM, Ulmer CZ, Bowden JA, Patterson RE, Cochran JA, Beecher CWW, Garrett TJ, Yost RA. LipidMatch: an automated workflow for rule-based lipid identification using untargeted high-resolution tandem mass spectrometry data. BMC Bioinformatics. 2017;18:11.
doi: 10.1186/s12859-017-1744-3
Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Meth. 2016;13(9):731–40.
doi: 10.1038/nmeth.3901
Chong J, Soufan O, Li C, Caraus I, Li SZ, Bourque G, Wishart DS, Xia J. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res. 2018;46(W1):W486-W94.
Paschke C, Leisner A, Hester A, Maass K, Guenther S, Bouschen W, Spengler B. Mirion-A Software Package for Automatic Processing of Mass Spectrometric Images. J Am Soc Mass Spectr. 2013;24(8):1296–306.
doi: 10.1007/s13361-013-0667-0
Girgis NM, Gundra UM, Ward LN, Cabrera M, Frevert U, Loke P. Ly6C(high) monocytes become alternatively activated macrophages in schistosome granulomas with help from CD4+ cells. Plos Pathog. 2014;10(6):13.
doi: 10.1371/journal.ppat.1004080
Shaw MK. Schistosoma-mansonii – Vitelline gland development in females from single sex infections. J Helminthol. 1987;61(3):253–9.
pubmed: 3117875
doi: 10.1017/S0022149X00010117
Mone H, Boissier J. Sexual biology of schistosomes. Adv Parasit. 2004;57(57):89–189.
doi: 10.1016/S0065-308X(04)57002-1
El Ridi R, Tallima H, Salah M, Aboueldahab M, Fahmy OM, Al-Halbosiy MF, Mahmoud SS. Efficacy and mechanism of action of arachidonic acid in the treatment of hamsters infected with Schistosoma mansoni or Schistosoma haematobium. Int J Antimicrob Ag. 2012;39(3):232–9.
doi: 10.1016/j.ijantimicag.2011.08.019
Standen OD. The relationship of sex in Schistosoma-mansoni to migration within the hepatic portal system of experimentally infected mice. Ann Trop Med Parasit. 1953;47(2):139–45.
pubmed: 13080976
doi: 10.1080/00034983.1953.11685555
Bexkens ML, Mebius MM, Houweling M, Brouwers JF, Tielens AGM, van Hellemond JJ. Schistosoma mansoni does not and cannot oxidise fatty acids, but these are used for biosynthetic purposes instead. Int J Parasitol. 2019;49(8):647–56.
pubmed: 31170410
doi: 10.1016/j.ijpara.2019.03.005
Colley DG, Bustinduy AL, Secor E, King CH. Human schistosomiasis. Lancet. 2014;383(9936):2253–64.
pubmed: 24698483
pmcid: 4672382
doi: 10.1016/S0140-6736(13)61949-2
Brouwers J, Van Hellemond JJ, van Golde LMG, Tielens AGM. Ether lipids and their possible physiological function in adult Schistosoma mansoni. Mol Biochem Parasit. 1998;96(1–2):49–58.
doi: 10.1016/S0166-6851(98)00103-0
Jokiranta TS, Jokipii L, Meri S. Complement resistance of parasites. Scand J Immunol. 1995;42(1):9–20.
pubmed: 7631149
doi: 10.1111/j.1365-3083.1995.tb03620.x
Fishelson Z. Novel mechanisms of immune evasion by schistosoma-mansoni. Mem I Oswaldo Cruz. 1995;90(2):289–92.
doi: 10.1590/S0074-02761995000200029