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pmid:33806494

Calendula officinalis Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes.

Maria Doligalska · Kinga Jóźwicka · Ludmiła Szewczak · Julita Nowakowska · Klaudia Brodaczewska · Katarzyna Goździk · Cezary Pączkowski · Anna Szakiel

Pathogens (Basel, Switzerland) · 2021 doi:10.3390/pathogens10030296

Paper

complete

Experiment

partial

Data

partial

Analysis

absent

Execution

absent

Execution evidence has not yet been added to this .science file. Explore its methods, data and open questions to plan the next step.
Record details sci_version · id · kind · revision · content_hash · schema · created_at · updated_at · generator
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2026-11-01T15:41:31Z
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paper object · 10 fields
state
complete
title
Calendula officinalis Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes.
doi
10.3390/pathogens10030296
pmid
33806494
authors array · 8 items
[0]
Maria Doligalska
[1]
Kinga Jóźwicka
[2]
Ludmiła Szewczak
[3]
Julita Nowakowska
[4]
Klaudia Brodaczewska
[5]
Katarzyna Goździk
[6]
Cezary Pączkowski
[7]
Anna Szakiel
journal
Pathogens (Basel, Switzerland)
year
2021
abstract
The influence of triterpenoid saponins on subcellular morphological changes in the cells of parasitic nematodes remains poorly understood. Our study examines the effect of oleanolic acid glucuronides from marigold (Calendula officinalis) on the possible modification of immunogenic proteins from infective Heligmosomoides polygyrus bakeri larvae (L3). Our findings indicate that the triterpenoid saponins alter the subcellular morphology of the larvae and prevent recognition of nematode-specific proteins by rabbit immune-IgG. TEM ultrastructure and HPLC analysis showed that microtubule and cytoskeleton fibres were fragmented by saponin treatment. MASCOT bioinformatic analysis revealed that in larvae exposed to saponins, the immune epitopes of their proteins altered. Several mitochondrial and cytoskeleton proteins involved in signalling and cellular processes were downregulated or degraded. As possible candidates, the following set of recognised proteins may play a key role in the immunogenicity of larvae: beta-tubulin isotype, alpha-tubulin, myosin, paramyosin isoform-1, actin, disorganized muscle protein-1, ATP-synthase, beta subunit, carboxyl transferase domain protein, glutamate dehydrogenase, enolase (phosphopyruvate hydratase), fructose-bisphosphate aldolase 2, tropomyosin, arginine kinase or putative chaperone protein DnaK, and galactoside-binding lectin. Data are available via ProteomeXchange with identifier PXD024205.
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claim-data-access
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All data generated and analysed during these studies are included in this published article and in the Supplementary information files. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD024205 and 10.6019/PXD024205 [78].
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methodological
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sections[24] "Data Availability Statement" paragraph 2
quote
All data generated and analysed during these studies are included in this published article and in the Supplementary information files. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD024205 and 10.6019/PXD024205 [78].
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Read the published estimate from the source
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The claim, method and evidence span published with the source article.
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PMC7999767
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H. polygyrus bakeri L3 proteins identified by hyperimmune rabbit serum, which were deactivated by C.officinalis GlcOAUA.
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2.4. LC-MS/MS Identification of Antigenic Proteins of L3 H. polygyrus bakeri
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Table 1
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H. polygyrus bakeri L3 proteins identified by hyperimmune rabbit serum, which were deactivated by C.officinalis GlcOAUA.
rows array · 26 items
[0] array · 12 items
[0]
Band (kDa)
[1]
Accession (Gi Number)
[2]
Protein Name
[3]
Species
[4]
Score
[5]
Mass (kDa)
[6]
emPAI
[7]
Coverage %
[8]
Number of Significant Peptide Matches
[9]
Uniprot ID
[10]
Description
[11]
Length (aa)
[1] array · 12 items
[0]
1 and 2 (50.8-49.1)
[1]
gi|568290660
[2]
ATP synthase F1, beta subunit
[3]
Necator americanus
[4]
1325
[5]
58,151
[6]
1.57
[7]
0.45
[8]
28
[9]
XP_013300832.1
[10]
ATP synthase subunit beta, mitochondrial
[11]
541
[2] array · 12 items
[0]
[1]
gi|160415837
[2]
Beta-tubulin isotype 1
[3]
Cylicocyclus nassatus
[4]
671
[5]
50,444
[6]
0.95
[7]
0.27
[8]
14
[9]
ABX39216.1
[10]
Beta-tubulin isotype 1
[11]
448
[3] array · 12 items
[0]
[1]
gi|560120094
[2]
Myosin and Myosin head and Myosin tail domain containing protein
[3]
Haemonchus contortus
[4]
644
[5]
226,702
[6]
0.28
[7]
0.09
[8]
15
[9]
CDJ95285.1
[10]
Myosin head
[11]
1963
[4] array · 12 items
[0]
[1]
gi|47606682
[2]
Paramyosin isoform 1
[3]
Dictyocaulus viviparus
[4]
620
[5]
100,878
[6]
0.65
[7]
0.22
[8]
13
[9]
AAT36324.1
[10]
CRE-UNC-15 protein
[11]
876
[5] array · 12 items
[0]
[1]
gi|597882604
[2]
Hypothetical protein Y032_0003g1332
[3]
Ancylostoma ceylanicum
[4]
492
[5]
50,904
[6]
0.79
[7]
0.3
[8]
9
[9]
EYC31965.1
[10]
V-type ATPase, B subunit
[11]
458
[6] array · 12 items
[0]
[1]
gi|371486394
[2]
Alpha tubulin
[3]
Ostertagia ostertagi
[4]
465
[5]
5053
[6]
0.79
[7]
0.24
[8]
11
[9]
AEX31242.1
[10]
Tubulin/FtsZ family, GTPase domain protein
[11]
446
[7] array · 12 items
[0]
[1]
gi|568269548
[2]
Carboxyl transferase domain protein
[3]
Necator americanus
[4]
321
[5]
58,645
[6]
0.24
[7]
0.11
[8]
6
[9]
ETN70891
[10]
Carboxyl transferase domain protein
[11]
535
[8] array · 12 items
[0]
[1]
gi|9438176
[2]
Heat shock 70 protein
[3]
Parastrongyloides trichosuri
[4]
318
[5]
70,452
[6]
0.35
[7]
0.17
[8]
6
[9]
AAF87583.1
[10]
Heat shock protein 70
[11]
644
[9] array · 12 items
[0]
[1]
gi|162280611
[2]
Actin variant 1
[3]
Dictyocaulus viviparus
[4]
274
[5]
42,129
[6]
0.65
[7]
0.29
[8]
5
[9]
ABX82966.1
[10]
Actin
[11]
376
[10] array · 12 items
[0]
[1]
gi|253721983
[2]
Glutamate dehydrogenase, partial
[3]
Haemonchus contortus
[4]
210
[5]
59,444
[6]
0.33
[7]
0.09
[8]
5
[9]
ACT34055.1
[10]
Glutamate dehydrogenase
[11]
532
[11] array · 12 items
[0]
3 (42.7)
[1]
gi|162280611
[2]
Actin variant 1
[3]
Dictyocaulus viviparus
[4]
2471
[5]
42,129
[6]
2.31
[7]
0.46
[8]
57
[9]
ABX82966.1
[10]
Actin
[11]
376
[12] array · 12 items
[0]
[1]
gi|560127002
[2]
Lipoma HMGIC fusion partner protein and Heat shock protein 70 domain containing protein
[3]
Haemonchus contortus
[4]
771
[5]
9216
[6]
0.66
[7]
0.19
[8]
17
[9]
CDJ88360.1
[10]
Putative chaperone protein DnaK
[11]
829
[13] array · 12 items
[0]
[1]
gi|301015486
[2]
Enolase
[3]
Haemonchus contortus
[4]
497
[5]
47,273
[6]
1.04
[7]
0.3
[8]
9
[9]
ADK47524.1
[10]
Phosphopyruvate hydratase
[11]
434
[14] array · 12 items
[0]
[1]
gi|597877220
[2]
Hypothetical protein Y032_0010g849
[3]
Ancylostoma ceylanicum
[4]
374
[5]
62,832
[6]
0.6
[7]
0.11
[8]
9
[9]
EYC26588.1
[10]
Protein unc-87
[11]
558
[15] array · 12 items
[0]
[1]
gi|47606682
[2]
Paramyosin isoform 1
[3]
Dictyocaulus viviparus
[4]
310
[5]
100,878
[6]
0.18
[7]
0.07
[8]
6
[9]
AAT36324.1
[10]
CRE-UNC-15 protein
[11]
876
[16] array · 12 items
[0]
[1]
gi|157326537
[2]
Tropomyosin
[3]
Heigmosomoides polygyrus
[4]
291
[5]
3313
[6]
1.14
[7]
0.18
[8]
6
[9]
ABV44405.1
[10]
Tropomyosin
[11]
284
[17] array · 12 items
[0]
[1]
gi|568290660
[2]
ATP synthase F1, beta subunit
[3]
Necator americanus
[4]
217
[5]
58,151
[6]
0.34
[7]
0.19
[8]
4
[9]
XP_013300832.1
[10]
ATP synthase subunit beta, mitochondrial
[11]
541
[18] array · 12 items
[0]
4 (40.7)
[1]
gi|325516326
[2]
Disorganized muscle protein 1
[3]
Haemonchus contortus
[4]
414
[5]
35,825
[6]
0.26
[7]
0.14
[8]
5
[9]
ADZ24723.1
[10]
Disorganized muscle protein 1
[11]
321
[19] array · 12 items
[0]
[1]
gi|162280611
[2]
Actin variant 1
[3]
Dictyocaulus viviparus
[4]
411
[5]
42,129
[6]
0.82
[7]
0.37
[8]
10
[9]
ABX82966.1
[10]
Actin
[11]
376
[20] array · 12 items
[0]
[1]
gi|560124746
[2]
Galectin domain containing protein
[3]
Haemonchus contortus
[4]
333
[5]
40,642
[6]
0.23
[7]
0.1
[8]
9
[9]
CDJ90629.1
[10]
Galactoside-binding lectin
[11]
356
[21] array · 12 items
[0]
[1]
gi|541045947
[2]
Fructose-bisphosphate aldolase 2
[3]
Ascaris suum
[4]
316
[5]
45,469
[6]
0.1
[7]
0.06
[8]
6
[9]
ADY45824.1
[10]
Fructose-bisphosphate aldolase class-I
[11]
417
[22] array · 12 items
[0]
[1]
gi|597874384
[2]
Hypothetical protein Y032_0015g2816
[3]
Ancylostoma ceylanicum
[4]
295
[5]
40,719
[6]
0.36
[7]
0.11
[8]
7
[9]
EYC23757.1
[10]
Arginine kinase
[11]
359
[23] array · 12 items
[0]
[1]
gi|568290660
[2]
ATP synthase F1, beta subunit
[3]
Necator americanus
[4]
255
[5]
58,151
[6]
0.55
[7]
0.24
[8]
6
[9]
XP_013300832.1
[10]
ATP synthase subunit beta, mitochondrial
[11]
541
[24] array · 12 items
[0]
[1]
gi|157381686
[2]
Heat shock protein 70
[3]
Angiostrongylus vasorum
[4]
253
[5]
5614
[6]
0.35
[7]
0.13
[8]
5
[9]
ABV46675.1
[10]
Putative chaperone protein DnaK
[11]
507
[25] array · 12 items
[0]
[1]
gi|597834320
[2]
Hypothetical protein Y032_0324g2520
[3]
Ancylostoma ceylanicum
[4]
228
[5]
30,314
[6]
0.15
[7]
0.09
[8]
4
[9]
EYB84003.1
[10]
Fructose-bisphosphate aldolase class-I
[11]
282
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224
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All data generated and analysed during these studies are included in this published article and in the Supplementary information files. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD024205 and 10.6019/PXD024205 [78].
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Complete file 
{"sci_version": "1.0", "schema": "https://corpus.bntrg.co.uk/sci/1.0/sci.schema.json", "id": "pmid:33806494", "kind": "science-record", "revision": 3, "content_hash": "sha256:4175c22603a5234e32d1b60e35e544e60022ce91d14aed8f0f40834c1f534b4f", "created_at": "2026-11-01T15:41:31Z", "updated_at": "2026-11-01T18:55:02Z", "generator": {"name": "corpus-assay-engine", "run_id": "reading-sci-2026-11-01"}, "paper": {"state": "complete", "title": "Calendula officinalis Triterpenoid Saponins Impact the Immune Recognition of Proteins in Parasitic Nematodes.", "doi": "10.3390/pathogens10030296", "pmid": "33806494", "authors": ["Maria Doligalska", "Kinga Jóźwicka", "Ludmiła Szewczak", "Julita Nowakowska", "Klaudia Brodaczewska", "Katarzyna Goździk", "Cezary Pączkowski", "Anna Szakiel"], "journal": "Pathogens (Basel, Switzerland)", "year": 2021, "abstract": "The influence of triterpenoid saponins on subcellular morphological changes in the cells of parasitic nematodes remains poorly understood. Our study examines the effect of oleanolic acid glucuronides from marigold (Calendula officinalis) on the possible modification of immunogenic proteins from infective Heligmosomoides polygyrus bakeri larvae (L3). Our findings indicate that the triterpenoid saponins alter the subcellular morphology of the larvae and prevent recognition of nematode-specific proteins by rabbit immune-IgG. TEM ultrastructure and HPLC analysis showed that microtubule and cytoskeleton fibres were fragmented by saponin treatment. MASCOT bioinformatic analysis revealed that in larvae exposed to saponins, the immune epitopes of their proteins altered. Several mitochondrial and cytoskeleton proteins involved in signalling and cellular processes were downregulated or degraded. As possible candidates, the following set of recognised proteins may play a key role in the immunogenicity of larvae: beta-tubulin isotype, alpha-tubulin, myosin, paramyosin isoform-1, actin, disorganized muscle protein-1, ATP-synthase, beta subunit, carboxyl transferase domain protein, glutamate dehydrogenase, enolase (phosphopyruvate hydratase), fructose-bisphosphate aldolase 2, tropomyosin, arginine kinase or putative chaperone protein DnaK, and galactoside-binding lectin. Data are available via ProteomeXchange with identifier PXD024205.", "claims": [{"id": "claim-data-access", "statement": "All data generated and analysed during these studies are included in this published article and in the Supplementary information files. 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This lane did not download the dataset or read its licence.", "duration_hours": null, "parameters": {}, "inputs": [], "outputs": ["the source data with its repository provenance"], "instruments": [], "reagents": []}, {"id": "run_analysis", "order": 3, "name": "Run the published analysis", "kind": "analysis", "state": "complete", "blocked_on": null, "description": "Apply the paper's statistical method to the resolved series and compare the result with the published target.", "duration_hours": null, "parameters": {}, "inputs": [], "outputs": ["the replicated result and its comparison"], "instruments": [], "reagents": []}], "materials": [], "instruments": [], "reagents": [], "conditions": {}, "gaps": ["step:obtain_source_data blocked on data:accession_absent"]}, "data": {"state": "partial", "assets": [{"id": "source:pmid:33806494", "role": "manuscript", "format": "xml", "media_type": "application/xml", "uri": "https://doi.org/10.3390/pathogens10030296", "sha256": "sha256:d074432912b92ff4cb3a5d7a807dab72c4beb9763d165a13b3d944fae47aa420", "bytes": 65075, "access": "open", "state": "resolved", "reader": null, "reader_status": "reader_required", "identifier": "10.3390/pathogens10030296", "version": null, "note": "Full article fetched from PMC; the checksum covers the rendered section body, not the original XML bytes.", "structure": {"pmcid": "PMC7999767", "source": "europe_pmc_fulltext", "coverage": "whole_body", "text_hash_scope": "rendered_section_body"}}, {"id": "asset:table:pmid:33806494:1", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:ad92997da9240c18a6a6484f62696662a70b329fdf96c0cfdbcc1b67137f9a41", "bytes": 4389, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[6]/table-wrap[1]#pathogens-10-00296-t001", "version": null, "note": "H. polygyrus bakeri L3 proteins identified by hyperimmune rabbit serum, which were deactivated by C.officinalis GlcOAUA.", "structure": {"pmcid": "PMC7999767", "section_index": 6, "section_title": "2.4. LC-MS/MS Identification of Antigenic Proteins of L3 H. polygyrus bakeri", "row_count": 26, "column_count": 12}, "table": {"label": "Table 1", "caption": "H. polygyrus bakeri L3 proteins identified by hyperimmune rabbit serum, which were deactivated by C.officinalis GlcOAUA.", "rows": [["Band (kDa)", "Accession (Gi Number)", "Protein Name", "Species", "Score", "Mass (kDa)", "emPAI", "Coverage %", "Number of Significant Peptide Matches", "Uniprot ID", "Description", "Length (aa)"], ["1 and 2 (50.8-49.1)", "gi|568290660", "ATP synthase F1, beta subunit", "Necator americanus", "1325", "58,151", "1.57", "0.45", "28", "XP_013300832.1", "ATP synthase subunit beta, mitochondrial", "541"], ["", "gi|160415837", "Beta-tubulin isotype 1", "Cylicocyclus nassatus", "671", "50,444", "0.95", "0.27", "14", "ABX39216.1", "Beta-tubulin isotype 1", "448"], ["", "gi|560120094", "Myosin and Myosin head and Myosin tail domain containing protein", "Haemonchus contortus", "644", "226,702", "0.28", "0.09", "15", "CDJ95285.1", "Myosin head", "1963"], ["", "gi|47606682", "Paramyosin isoform 1", "Dictyocaulus viviparus", "620", "100,878", "0.65", "0.22", "13", "AAT36324.1", "CRE-UNC-15 protein", "876"], ["", "gi|597882604", "Hypothetical protein Y032_0003g1332", "Ancylostoma ceylanicum", "492", "50,904", "0.79", "0.3", "9", "EYC31965.1", "V-type ATPase, B subunit", "458"], ["", "gi|371486394", "Alpha tubulin", "Ostertagia ostertagi", "465", "5053", "0.79", "0.24", "11", "AEX31242.1", "Tubulin/FtsZ family, GTPase domain protein", "446"], ["", "gi|568269548", "Carboxyl transferase domain protein", "Necator americanus", "321", "58,645", "0.24", "0.11", "6", "ETN70891", "Carboxyl transferase domain protein", "535"], ["", "gi|9438176", "Heat shock 70 protein", "Parastrongyloides trichosuri", "318", "70,452", "0.35", "0.17", "6", "AAF87583.1", "Heat shock protein 70", "644"], ["", "gi|162280611", "Actin variant 1", "Dictyocaulus viviparus", "274", "42,129", "0.65", "0.29", "5", "ABX82966.1", "Actin", "376"], ["", "gi|253721983", "Glutamate dehydrogenase, partial", "Haemonchus contortus", "210", "59,444", "0.33", "0.09", "5", "ACT34055.1", "Glutamate dehydrogenase", "532"], ["3 (42.7)", "gi|162280611", "Actin variant 1", "Dictyocaulus viviparus", "2471", "42,129", "2.31", "0.46", "57", "ABX82966.1", "Actin", "376"], ["", "gi|560127002", "Lipoma HMGIC fusion partner protein and Heat shock protein 70 domain containing protein", "Haemonchus contortus", "771", "9216", "0.66", "0.19", "17", "CDJ88360.1", "Putative chaperone protein DnaK", "829"], ["", "gi|301015486", "Enolase", "Haemonchus contortus", "497", "47,273", "1.04", "0.3", "9", "ADK47524.1", "Phosphopyruvate hydratase", "434"], ["", "gi|597877220", "Hypothetical protein Y032_0010g849", "Ancylostoma ceylanicum", "374", "62,832", "0.6", "0.11", "9", "EYC26588.1", "Protein unc-87", "558"], ["", "gi|47606682", "Paramyosin isoform 1", "Dictyocaulus viviparus", "310", "100,878", "0.18", "0.07", "6", "AAT36324.1", "CRE-UNC-15 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