C. quinoa and S. hispanica L. Seeds Provide Immunonutritional Agonists to Selectively Polarize Macrophages
Abstract
:1. Introduction
2. Material and Methods
2.1. Cell Culture
2.2. Isolation of Protease Inhibitors (PPIs) and Cell Culture Treatments
2.3. FACS Analysis for TLR4 Expression and Macrophage Phenotypic Differentiation
2.4. Cell ‘Mito’ Stress Test Assay
2.5. Measurement of Lysosomal (Neutral Red Assay) and Mitochondrial Enzyme (Test MTT) Activities
2.6. Phospholipid Assay
2.7. Relative Gene Expression Analyses
2.8. Cell Cultures Total Protein Extraction
2.9. In-Gel Digestion
2.10. Reverse Phase-Liquid Chromatography RP-LC-MS/MS Analysis
2.11. Statistical Analysis
3. Results and Discussion
3.1. Protein Patterns
3.2. Macrophage Polarization
3.3. Immunonutritonal Changes
3.4. Phenotypic Changes
4. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Nº (#) | Protein a (Accession) | Mr | pI | Mean Fold Difference b | pc | |
---|---|---|---|---|---|---|
C. quinoa | S. hispanica L. | |||||
1 | Heat shock protein HSP 90-beta (P08238) | 83.2 | 5.03 | 1.23 ± 0.28 | 0.89 ± 0.28 | 0.103 |
2 | Pyruvate kinase (P14618) | 57.9 | 7.84 | 0.13 ± 0.03 * | 0.11 ± 0.03 * | 0.446 |
3 | Malate dehydrogenase (P40926) | 35.5 | 8.68 | 1.92 ± 0.44 * | 1.66 ± 0.53 | 0.444 |
4 | Polyubiquitin-C (P0CG48) | 77.0 | 7.66 | 1.34 ± 0.31 | 1.16 ± 0.37 | 0.445 |
5 | Transitional endoplasmic reticulum ATPase (P55072) | 89.3 | 5.26 | 1.40 ± 0.32 | 1.22 ± 0.39 | 0.443 |
6 | T-complex protein 1 subunit zeta (P40227) | 58.0 | 6.68 | 0.24 ± 0.05 * | 0.21 ± 0.07 * | 0.446 |
7 | Protein disulfide-isomerase (P07237) | 57.1 | 4.87 | 1.30 ± 0.30 | 0.97 ± 0.31 | 0.124 |
8 | Peptidyl-prolyl cis-trans isomerase A (P62937) | 18.0 | 7.81 | 1.71 ± 0.38 | 1.25 ± 0.40 | 0.124 |
9 | 6-phosphogluconate dehydrogenase (P52209-2) | 51.8 | 7.44 | 1.61 ± 0.38 | 1.46 ± 0.46 | 0.445 |
10 | Ras-related protein Rab-7a (P51149) | 23.5 | 6.70 | 0.96 ± 0.22 | 0.62 ± 0.20 | 0.037 |
11 | Aldehyde dehydrogenase (P05091-2) | 51.0 | 6.20 | 0.28 ± 0.06 * | 0.97 ± 0.31 | 0.001 |
12 | D-3-phosphoglycerate dehydrogenase (O43175) | 56.6 | 6.71 | 1.68 ± 0.38 | 1.45 ± 0.47 | 0.445 |
13 | L-lactate dehydrogenase B chain (P07195) | 36.6 | 6.05 | 1.96 ± 0.45 * | 0.97 ± 0.31 | 0.004 |
14 | Sodium/potassium-transporting ATPase (P05023-3) | 109.5 | 5.31 | 1.68 ± 0.38 | 0.36 ± 0.11 * | 0.001 |
15 | Fructose-bisphosphate aldolase A (P04075) | 39.4 | 8.09 | 0.72 ± 0.16 | 1.45 ± 0.45 | 0.010 |
16 | Annexin A5 (P08758) | 35.9 | 5.05 | 2.01 ± 0.46 * | 2.04 ± 0.65 | 0.932 |
17 | Voltage-dependent anion-selective channel (P45880-2) | 30.4 | 7.20 | 1.34 ± 0.31 | 1.16 ± 0.38 | 0.445 |
18 | L-lactate dehydrogenase A chain (P00338) | 36.7 | 8.27 | 1.34 ± 0.31 | 0.87 ± 0.28 | 0.037 |
19 | Macrophage-capping protein (P40121-2) | 36.8 | 7.20 | 1.67 ± 0.38 | 1.45 ± 0.46 | 0.446 |
20 | Dolichyl-diphosphooligosaccharide-glycosyltransferase (P39656-3) | 49.0 | 6.86 | 0.33 ± 0.88 * | 0.29 ± 0.09 * | 0.446 |
21 | Nucleoside diphosphate kinase A (P15531) | 17.1 | 6.19 | 1.68 ± 0.27 | 1.45 ± 0.46 | 0.445 |
22 | T-complex protein 1 subunit delta (P50991) | 57.9 | 7.83 | 1.20 ± 0.27 | 0.21 ± 0.07 * | 0.001 |
23 | Ubiquitin-like modifier-activating enzyme 1 (P22314-2) | 113.7 | 5.60 | 0.67 ± 0.15 | 0.58 ± 0.17 | 0.446 |
24 | Serine hydroxymethyl-transferase (P34897-3) | 53.4 | 8.15 | 1.70 ± 0.38 | 1.42 ± 0.32 | 0.445 |
25 | Malate dehydrogenase (P40925-2) | 27.0 | 9.11 | 1.67 ± 0.38 | 1.54 ± 0.41 | 0.446 |
26 | Serine/threonine kinase receptor-associated protein (Q9Y3F4) | 38.4 | 5.12 | 0.42 ± 0.10 * | 0.36 ± 0.11 * | 0.446 |
27 | Glucose-6-phosphate isomerase (P06744) | 63.1 | 8.32 | 1.22 ± 0.25 | 0.97 ± 0.13 | 0.446 |
28 | T-complex protein 1 subunit α (P17987) | 60.3 | 6.11 | 1.12 ± 0.19 | 0.48 ± 0.15 * | 0.001 |
29 | Chloride intracellular channel protein 1 (O00299) | 26.9 | 5.17 | 1.86 ± 0.34 | 1.39 ± 0.43 | 0.446 |
30 | Nascent polypeptide-associated complex subunit α (Q13765) | 23.4 | 4.56 | 1.12 ± 0.25 | 0.49 ± 0.15 * | 0.002 |
31 | Rho GDP-dissociation inhibitor 1 (P52565) | 23.2 | 5.11 | 2.51 ± 0.57 * | 1.54 ± 0.62 | 0.013 |
32 | Glucose-6-phosphate 1-dehydrogenase (P11413) | 59.2 | 6.84 | 1.00 ± 0.23 | 0.87 ± 0.27 | 0.446 |
33 | Glyceraldehyde-3-phosphate dehydrogenase (P04406) | 36.0 | 8.46 | 0.56 ± 0.13 * | 0.48 ± 0.15 * | 0.446 |
34 | Dihydrolipoyl dehydrogenase (P09622-2) | 43.6 | 7.03 | 1.67 ± 0.38 | 0.72 ± 0.23 | 0.002 |
35 | Ras-related protein Rab-10 (P61026) | 22.5 | 8.38 | 1.68 ± 0.38 | 0.97 ± 0.26 | 0.013 |
36 | V-type proton ATPase catalytic subunit A (P38606-2) | 64.7 | 5.66 | 1.12 ± 0.25 | 0.51 ± 0.15 * | 0.002 |
37 | Poly(rC)-binding protein 1 (Q15365) | 37.5 | 7.09 | 2.24 ± 0.51 * | 1.45 ± 0.46 | 0.037 |
38 | Voltage-dependent anion-selective channel protein 1 (P21796) | 30.8 | 8.54 | 1.26 ± 0.29 | 0.36 ± 0.11 * | 0.001 |
39 | T-complex protein 1 subunit ε (P48643-2) | 49.5 | 6.19 | 1.55 ± 0.09 | 0.42 ± 0.12 * | 0.001 |
40 | Peptidyl-prolyl cis-trans isomerase FKBP4 (Q02790) | 51.8 | 5.43 | 0.42 ± 0.10 * | 0.38 ± 0.13 * | 0.446 |
41 | Ras-related protein Rab-1A (P62820) | 22.7 | 6.21 | 0.56 ± 0.13 * | 0.97 ± 0.31 | 0.025 |
42 | T-complex protein 1 subunit eta(Q99832-3) | 54.8 | 7.68 | 1.68 ± 0.38 | 0.49 ± 0.14 * | 0.001 |
43 | Ras-related protein Rab-2A (P61019-2) | 20.8 | 6.11 | 1.67 ± 0.38 | 0.72 ± 0.23 | 0.002 |
44 | Isocitrate dehydrogenase [NADP] cytoplasmic (O75874) | 46.6 | 7.01 | 1.51 ± 0.33 | 1.42 ± 0.08 | 0.446 |
45 | Isocitrate dehydrogenase [NADP], mitochondrial (P48735-2) | 45.2 | 7.75 | 2.51 ± 0.57 * | 0.72 ± 0.32 | 0.001 |
46 | Fermitin family homolog 3 (Q86UX7-2) | 75.4 | 6.77 | 0.56 ± 0.13 * | 0.48 ± 0.13 * | 0.446 |
47 | Dolichyl-diphosphooligosaccharide--protein glycosyltransferase subunit 2 (P04844-2) | 67.7 | 6.06 | 0.84 ± 0.19 | 0.79 ± 0.23 | 0.446 |
48 | Receptor of activated protein C kinase 1 (P63244) | 35.1 | 7.69 | 3.35 ± 0.77 * | 1.56 ± 0.46 | 0.001 |
49 | Ceruloplasmin (P00450) | 122.1 | 5.72 | 2.51 ± 0.57 * | 2.18 ± 0.70 | 0.446 |
50 | Hypoxia up-regulated protein 1 (Q9Y4L1) | 111.3 | 5.22 | 0.84 ± 0.19 | 0.76 ± 0.32 | 0.446 |
51 | SRP55-3 of Serine/arginine-rich splicing factor 6 (Q13247-3) | 38.4 | 11.00 | 1.67 ± 0.38 | 0.87 ± 0.41 | 0.002 |
52 | High mobility group protein B1 (P09429) | 24.9 | 5.74 | 0.84 ± 0.19 | 0.69 ± 0.17 | 0.446 |
53 | Cell division control protein 42 homolog (P60953) | 21.2 | 6.55 | 0.91 ± 0.12 | 1.67 ± 0.26 | 0.025 |
54 | Ran GTPase-activating protein 1 (P46060) | 63.5 | 4.68 | 1.69 ± 0.28 | 0.72 ± 0.17 | 0.002 |
55 | NADPH-cytochrome P450 reductase (P16435) | 76.6 | 5.58 | 1.75 ± 0.42 | 0.81 ± 0.22 | 0.002 |
56 | Glutamate dehydrogenase 1 (P00367-3) | 46.5 | 7.08 | 0.84 ± 0.19 | 0.76 ± 0.21 | 0.446 |
57 | Ras GTPase-activating-like protein IQGAP1 (P46940) | 189.1 | 6.48 | 0.84 ± 0.19 | 0.79 ± 0.18 | 0.446 |
58 | Proliferation-associated protein 2G4 (Q9UQ80-2) | 38.0 | 7.53 | 1.26 ± 0.29 | 0.54 ± 0.17 | 0.001 |
59 | Protein disulfide-isomerase A3 (P30101) | 56.7 | 6.35 | 1.33 ± 0.19 | 0.47 ± 0.09 | 0.001 |
60 | GTP-binding nuclear protein Ran (P62826) | 24.4 | 7.49 | 2.24 ± 0.51 * | 1.94 ± 0.62 | 0.445 |
61 | Calnexin (P27824) | 67.5 | 4.60 | 0.89 ± 0.19 | 0.76 ± 0.32 | 0.446 |
62 | Serine/threonine-protein phosphatase 2A 55 kDa regulatory subunit B (P63151) | 51.7 | 6.20 | 0.85 ± 0.16 | 1.45 ± 0.34 | 0.025 |
63 | Apoptosis-inducing factor 1 (O95831-3) | 66.3 | 8.94 | 0.56 ± 0.13 * | 0.48 ± 0.15 * | 0.446 |
64 | Phosphoglycerate kinase 1 (P00558) | 44.6 | 8.10 | 1.92 ± 0.44 * | 1.64 ± 0.36 | 0.148 |
65 | Phosphoglycerate mutase 1 (P18669) | 28.8 | 7.18 | 1.81 ± 0.38 | 1.25 ± 0.40 | 0.124 |
66 | 40S ribosomal protein S3 (P23396) | 26.7 | 9.66 | 1.66 ± 0.28 | 1.13 ± 0.36 | 0.050 |
67 | Rab GDP dissociation inhibitor β (P50395) | 50.6 | 6.47 | 0.42 ± 0.10 * | 0.36 ± 0.11 * | 0.446 |
68 | T-complex protein 1 subunit γ (P49368) | 60.5 | 6.49 | 0.21 ± 0.05 * | 1.09 ± 0.35 | 0.001 |
69 | T-complex protein 1 subunit τ (P50990-3) | 51.6 | 5.24 | 1.12 ± 0.25 | 0.48 ± 0.16 * | 0.001 |
70 | Serine/threonine-protein phosphatase PP1-α (P62136) | 37.5 | 6.33 | 1.00 ± 0.23 | 0.29 ± 0.09 * | 0.002 |
71 | T-complex protein 1 subunit β (P78371-2) | 52.7 | 6.44 | 2.10 ± 0.48 * | 1.56 ± 0.36 | 0.066 |
72 | Serine/threonine-protein phosphatase PP1-γ (P36873) | 37.0 | 6.54 | 1.26 ± 0.29 | 0.37 ± 0.10 * | 0.001 |
73 | Peroxiredoxin-1 (Q06830) | 22.1 | 8.13 | 1.20 ± 0.27 | 0.83 ± 0.26 | 0.066 |
74 | Sarcoplasmic/endoplasmic reticulum calcium ATPase 2 (P16615-2) | 109.6 | 5.36 | 1.12 ± 0.25 | 0.65 ± 0.18 * | 0.002 |
75 | Plasminogen activator inhibitor 1 RNA-binding protein (Q8NC51-4) | 42.4 | 8.44 | 1.67 ± 0.38 | 1.74 ± 0.42 | 0.446 |
76 | Proliferating cell nuclear antigen (P12004) | 28.8 | 4.69 | 0.84 ± 0.19 | 0.72 ± 0.23 | 0.446 |
77 | Proteasome subunit beta type-5 (P28074) | 28.5 | 6.92 | 0.42 ± 0.10 * | 0.18 ± 0.05 * | 0.002 |
78 | Splicing factor, proline- and glutamine-rich (P23246) | 76.1 | 9.44 | 1.12 ± 0.25 | 1.78 ± 0.52 | 0.190 |
79 | Protein disulfide-isomerase A4 (P13667) | 72.9 | 5.07 | 1.68 ± 0.38 | 0.97 ± 0.26 | 0.013 |
80 | Nucleosome assembly protein 1-like 1 (P55209-2) | 42.7 | 4.55 | 0.56 ± 0.13 * | 0.84 ± 0.16 * | 0.446 |
81 | Ubiquitin-conjugating enzyme E2 N (P61088) | 17.1 | 6.57 | 0.84 ± 0.19 | 0.72 ± 0.23 | 0.446 |
82 | Calcyclin-binding protein (Q9HB71) | 26.2 | 8.25 | 0.96 ± 0.15 | 0.87 ± 0.32 | 0.446 |
83 | SRP40-4 of Serine/arginine-rich splicing factor 5 (Q13243-3) | 30.8 | 11.66 | 0.81 ± 0.14 | 0.76 ± 0.13 | 0.446 |
84 | Prostaglandin E synthase 3 (Q15185-3) | 14.9 | 4.77 | 0.80 ± 0.05 | 0.81 ± 0.09 | 0.446 |
85 | V-type proton ATPase subunit C1 (P21283) | 43.9 | 7.46 | 0.88 ± 0.19 | 0.72 ± 0.06 | 0.446 |
86 | Heat shock protein HSP 90-α (P07900) | 84.6 | 5.02 | 1.32 ± 0.30 | 0.99 ± 0.32 | 0.135 |
87 | RuvB-like 1 (Q9Y265) | 42.1 | 6.38 | 0.56 ± 0.13 * | 0.48 ± 0.15 * | 0.446 |
88 | Phospholipase A-2-activating protein (Q9Y263) | 50.2 | 6.42 | 1.67 ± 0.38 | 1.75 ± 0.27 | 0.446 |
89 | Ras-related protein Rab-14 (P61106) | 87.1 | 6.37 | 5.03 ± 1.15 * | 2.91 ± 0.39 * | 0.013 |
90 | Prolyl endopeptidase (P48147) | 23.9 | 6.21 | 1.75 ± 0.31 | 1.45 ± 0.44 | 0.446 |
91 | V-type proton ATPase subunit B (P21281) | 80.6 | 5.86 | 1.67 ± 0.42 | 1.42 ± 0.12 | 0.446 |
92 | Ras-related protein Rab-6A (P20340) | 56.5 | 5.81 | 1.57 ± 0.38 | 1.45 ± 0.08 | 0.446 |
93 | Dolichyl-diphosphooligosaccharide-protein glycosyltransferase subunit 1 (P04843) | 23.6 | 5.54 | 1.37 ± 0.36 | 2.87 ± 0.64 * | 0.025 |
94 | Mitochondrial import receptor subunit TOM40 homolog (O96008-2) | 68.5 | 6.38 | 3.35 ± 0.76 * | 1.28 ± 0.24 | 0.002 |
95 | Ras-related protein Rab-11B (Q15907) | 34.4 | 7.24 | 1.71 ± 0.38 | 1.54 ± 0.46 | 0.446 |
96 | Serine/arginine-rich splicing factor 1 (Q07955) | 24.5 | 5.94 | 1.69 ± 0.23 | 1.72 ± 0.31 | 0.446 |
97 | Inter-α-trypsin inhibitor heavy chain H2 (P19823) | 27.7 | 10.35 | 1.66 ± 0.35 | 2.91 ± 0.93 * | 0.025 |
98 | Ras GTPase-activating protein-binding protein 1 (Q13283) | 106.3 | 6.85 | 1.59 ± 0.37 | 1.33 ± 0.46 | 0.446 |
99 | Clathrin heavy chain 1 (Q00610-2) | 187.8 | 5.69 | 1.68 ± 0.38 | 0.29 ± 0.09 * | 0.001 |
100 | Proteasome subunit beta type-4 (P28070) | 29.2 | 5.97 | 0.84 ± 0.19 | 0.72 ± 0.23 | 0.446 |
101 | Guanine nucleotide-binding protein G ‘α’ (P04899) | 40.5 | 5.54 | 1.76 ± 0.26 * | 1.45 ± 0.31 | 0.013 |
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Srdić, M.; Ovčina, I.; Fotschki, B.; Haros, C.M.; Laparra Llopis, J.M. C. quinoa and S. hispanica L. Seeds Provide Immunonutritional Agonists to Selectively Polarize Macrophages. Cells 2020, 9, 593. https://doi.org/10.3390/cells9030593
Srdić M, Ovčina I, Fotschki B, Haros CM, Laparra Llopis JM. C. quinoa and S. hispanica L. Seeds Provide Immunonutritional Agonists to Selectively Polarize Macrophages. Cells. 2020; 9(3):593. https://doi.org/10.3390/cells9030593
Chicago/Turabian StyleSrdić, Maša, Ivana Ovčina, Bartosz Fotschki, Claudia Monika Haros, and Jose Moises Laparra Llopis. 2020. "C. quinoa and S. hispanica L. Seeds Provide Immunonutritional Agonists to Selectively Polarize Macrophages" Cells 9, no. 3: 593. https://doi.org/10.3390/cells9030593