Effects of silver nanoparticles and ions on a co-culture model for the gastrointestinal epithelium

Georgantzopoulou, Anastasia; Serchi, Tommaso; Cambier, Sébastien; Leclercq, Céline C.; Renaut, Jenny; Shao, Jia; Kruszewski, Marcin; Lentzen, Esther; Grysan, Patrick; Eswara, Santhana; Audinot, Jean-Nicolas; Contal, Servane; Ziebel, Johanna; Guignard, Cédric; Hoffmann, Lucien; Murk, AlberTinka J.; Gutleb, Arno C.

doi:10.1186/s12989-016-0117-9

Particle and Fibre Toxicology

Table 2 Proteins with altered abundance. The cells in co-culture were exposed to the non-toxic concentration of 1 mg/L of Ag 20 nm NPs, Ag 200 nm NPs or AgNO₃ ^a)

From: Effects of silver nanoparticles and ions on a co-culture model for the gastrointestinal epithelium

Spot N°	Protein name	UniProt Ac. N°	UniProt ID	NCBI GI	Cov. %	MOWSE Score	p-value	Queries matched	Mr (Da)	pI (pH)	AgNO₃ vs Control		Ag 20nm vs Control		Ag 200nm vs Control
Spot N°	Protein name	UniProt Ac. N°	UniProt ID	NCBI GI	Cov. %	MOWSE Score	p-value	Queries matched	Mr (Da)	pI (pH)	Fold Change	t-test	Fold Change	t-test	Fold Change	t-test
	Cytoskeleton-associated proteins
260	villin-1	P09327	VILI_HUMAN	194394237	40%	153	2.7e-010	40	93093	5.99	−1.13	0.351	−1.03	0.792	1.55	0.047
701	keratin, type II cytoskeletal 8	P05787	K2C8_HUMAN	4504919	64%	274	2.2e-022	38	53671	5.52	−1.29	0.451	2.05	0.026	−1.97	0.12
800	keratin, type II cytoskeletal 8	P05787	K2C8_HUMAN	4504919	67%	345	1.7e-029	43	53671	5.52	1.13	0.468	1.7	0.002	1.16	0.18
1083	keratin, type II cytoskeletal 8	P05787	K2C8_HUMAN	4504919	59%	412	3.4e-036	44	53671	5.52	3.1	0.001	1.59	0.022	1.1	0.598
841	cytokeratin 18 (424 AA)	P05783	K1C18_HUMAN	30311	77%	387	1.1e-033	46	47305	5.27	1.1	0.502	1.49	0.029	1.02	0.802
263	gelsolin isoform a precursor	B7Z9A0	B7Z9A0_HUMAN	221045118	35%	130	5.4e-008	34	83451	5.58	−1.1	0.751	1.77	0.033	1.33	0.218
984	actin, cytoplasmic 1	P60709	ACTB_HUMAN	14250401	72%	527	1.1e-047	38	41321	5.56	−1.1	0.114	−1.74	0.004	−1.05	0.282
993	actin, cytoplasmic 1	Q53G99	Q53G99_HUMAN	62897625	85%	642	3.4e-059	42	42080	5.37	−1.22	0.083	−1.94	0.001	−1.1	0.319
683	tubulin alpha-1B chain	P68363	TBA1B_HUMAN	119578453	60%	317	1.1e-026	30	46797	4.96	−2.16	0.009	−1.55	0.077	1.07	0.815
713	tubulin, beta 2C, isoform CRA_b	Q8N6N5	Q8N6N5_HUMAN	119608775	55%	272	3.4e-022	38	49250	4.88	−3.8	0.003	−1.22	0.331	1.32	0.267
538	dihydropyrimidinase-related protein 2	Q16555	DPYL2_HUMAN	4503377	62%	347	1.1e-029	40	62711	5.95	−1.62	0.052	1.44	0.08	1.44	0.117
	Oxidative stress-associated proteins
1492	peroxiredoxin-6	P30041	PRDX6_HUMAN	4758638	89%	718	8.6e-067	46	25133	6.00	−1.45	0.005	−1.25	0.036	−1.33	0.032
627	protein disulfide-isomerase A3	P30101	PDIA3_HUMAN	220702506	58%	271	4.3e-022	38	55328	5.61	1.1	0.383	2.01	0.004	1.38	0.038
629	protein disulfide-isomerase A3	P30101	PDIA3_HUMAN	220702506	64%	795	1.7e-074	43	54541	5.61	1.34	0.18	2.63	0.007	1.42	0.106
635	protein disulfide-isomerase A3	P30101	PDIA3_HUMAN	220702506	63%	645	1.7e-059	44	54541	5.61	1.32	0.146	2.53	0.003	1.22	0.2
655	protein disulfide isomerase family A, member 3, isoform CRA_a	B3KQT9	B3KQT9_HUMAN	119597640	40%	81	0.0039	21	54454	6.78	1.69	0.043	1.1	0.247	−1.06	0.514
765	protein disulfide-isomerase A6	Q15084	PDIA6_HUMAN	1710248	63%	419	6.8e-037	38	46512	4.95	1.32	0.118	1.52	0.04	−1.11	0.618
769	protein disulfide-isomerase A6	Q15084	PDIA6_HUMAN	1710248	63%	467	1.1e-041	43	46512	4.95	1.25	0.104	1.53	0.02	1.05	0.757
767	glutathione synthetase	P48637	GSHB_HUMAN	4504169	70%	580	5.4e-053	50	52523	5.67	−1.08	0.367	1.48	9E-04	1.01	0.79
	Apoptosis-associated proteins
1203	annexin A4	P09525	ANXA4_HUMAN	1703319	73%	453	2.7e-040	39	36088	5.84	−1.27	0.021	−1.54	0.01	−1.04	0.703
1208	annexin A4	P09525	ANXA4_HUMAN	1703319	69%	346	1.4e-029	37	36088	5.84	−1.16	0.434	−1.1	0.611	1.88	0.009
1226	annexin A4	P09525	ANXA4_HUMAN	1703319	73%	731	4.3e-068	42	36088	5.84	−1.24	0.119	−1.63	0.006	−1.06	0.676
1769	histidine triad nucleotide-binding protein 1	P49773	HINT1_HUMAN	227968190	94%	105	1.7e-005	18	13887	6.24	1.16	0.224	1.36	0.013	1.24	0.037
1773	programmed cell death protein 5	O14737	PDCD5_HUMAN	159163907	84%	217	1.1e-016	22	12911	9.85	1.72	0.011	1.03	0.896	−1.45	0.115
	Stress-associated proteins
408	heat shock cognate 71 kDa protein isoform 2	Q53HF2	Q53HF2_HUMAN	24234686	57%	419	6.8e-037	39	53598	5.62	−1.03	0.896	1.55	0.023	−1.04	0.845
414	heat shock 70 kDa protein 1A/1B	P08107	HSP71_HUMAN	147744565	62%	248	8.6e-020	33	70294	5.48	1.46	0.016	1.57	0.017	1.1	0.493
429	heat shock 70 kDa protein 1A/1B	P08107	HSP71_HUMAN	147744565	56%	515	1.7e-046	45	70294	5.48	1.33	0.01	1.61	3E-04	1.28	0.269
438	heat shock 70 kDa protein 1A/1B	P08107	HSP71_HUMAN	147744565	51%	203	2.7e-015	31	70294	5.48	1.54	0.034	2.04	0.021	1.04	0.913
573	60 kDa heat shock protein, mitochondrial	P10809	CH60_HUMAN	31542947	53%	357	1.1e-030	43	61187	5.70	−1.03	0.884	1.74	0.029	−1.22	0.44
576	60 kDa heat shock protein, mitochondrial	P10809	CH60_HUMAN	31542947	45%	138	8.6e-009	30	61187	5.70	−1	0.86	1.75	0.004	−1.15	0.356
577	60 kDa heat shock protein, mitochondrial	P10809	CH60_HUMAN	31542947	57%	641	4.3e-059	47	61187	5.70	−1.04	0.889	1.85	0.048	−1.21	0.577
578	60 kDa heat shock protein, mitochondrial	P10809	CH60_HUMAN	31542947	72%	684	2.2e-063	49	61187	5.70	−1.04	0.869	1.66	0.067	−1.26	0.469
473	stress-induced-phosphoprotein 1	P31948	STIP1_HUMAN	5803181	54%	131	4.3e-008	29	68721	7.81	1.05	0.57	2.02	0.002	1.37	0.012
479	stress-induced-phosphoprotein 1	P31948	STIP1_HUMAN	5803181	58%	122	3.4e-007	28	68721	7.81	1.08	0.404	2.03	0.003	1.29	0.032
	Metabolism-associated proteins
625	liver carboxylesterase 1	P23141	EST1_HUMAN	30749518	45%	133	2.7e-008	38	60692	6.06	−1.06	0.869	−1.91	0.028	−1.18	0.488
631	liver carboxylesterase 1	P23141	EST1_HUMAN	30749518	51%	109	6.8e-006	31	60692	6.06	−1.13	0.732	−2.59	0.017	−1.48	0.191
1543	glutathione S-transferase P	P09211	GSTP1_HUMAN	4504183	75%	716	1.4e-066	29	23569	5.43	−1.14	0.435	−1.95	0.008	−1.29	0.19
1569	glutathione S-transferase P	P09211	GSTP1_HUMAN	4504183	75%	681	4.3e-063	26	23569	5.43	−1.03	0.791	−1.68	0.008	−1.17	0.266
1866	fatty acid binding protein	P07148	FABPL_HUMAN	182356	91%	408	8.6e-036	21	14226	6.60	1.26	0.195	1.88	0.008	−1.07	0.706
1177	inorganic pyrophosphatase	Q15181	IPYR_HUMAN	11056044	77%	234	2.2e-018	29	33095	5.54	−1.16	0.332	1.41	0.05	1.2	0.366
1199	inorganic pyrophosphatase	Q15181	IPYR_HUMAN	11056044	68%	169	6.8e-012	25	33095	5.54	−1.03	0.975	1.91	0.031	1.26	0.309
1045	sialic acid synthase	Q9NR45	SIAS_HUMAN	12056473	76%	397	1.1e-034	39	40738	6.29	−1.15	0.548	1.58	0.046	1.37	0.109
1133	pyridoxal kinase	O00764	PDXK_HUMAN	119629883	45%	123	2.7e-007	24	42931	7.59	−1.06	0.702	−1.7	0.008	1.01	0.988
1320	purine nucleoside phosphorylase	P00491	PNPH_HUMAN	157168362	73%	244	2.2e-019	29	32758	6.71	−1.25	0.249	−2.03	0.028	−1.18	0.405
941	aspartate aminotransferase, cytoplasmic	P17174	AATC_HUMAN	4504067	72%	298	8.6e-025	39	46447	6.52	1.85	0.039	1.03	0.966	1.11	0.632
1938	polyubiquitin-C	F5H7Y5	F5H7Y5_HUMAN	228311825	80%	556	1.4e-050	24	17081	6.22	1.36	0.016	1.09	0.514	−1.19	0.268
185	elongation factor 2	P13639	EF2_HUMAN	4503483	37%	197	1.1e-014	38	96246	6.41	1.24	0.164	−1.82	0.021	1.15	0.595
200	elongation factor 2	P13639	EF2_HUMAN	4503483	46%	258	8.6e-021	45	96246	6.41	−1.15	0.164	−1.67	0.009	1.21	0.646
1734	peptidyl-prolyl cis-trans isomerase A	P62937	PPIA_HUMAN	1633054	93%	443	2.7e-039	23	18098	7.82	1.78	0.05	−1.48	0.037	−1.27	0.125
994	leukocyte elastase inhibitor	P30740	ILEU_HUMAN	13489087	56%	563	2.7e-051	39	42829	5.90	−1.65	0.003	−2	0.001	−1.25	0.147
1007	leukocyte elastase inhibitor	P30740	ILEU_HUMAN	13489087	52%	266	1.4e-021	27	42829	5.90	−1.65	0.02	−1.75	0.009	−1.39	0.151
1020	leukocyte elastase inhibitor	P30740	ILEU_HUMAN	13489087	56%	662	3.4e-061	39	42829	5.90	−1.22	0.024	−1.32	0.005	1.11	0.021
703	retinal dehydrogenase 1	P00352	AL1A1_HUMAN	21361176	52%	318	8.6e-027	45	55454	6.30	−1.28	0.064	−1.62	0.01	1.19	0.18
815	alpha-enolase	P06733	ENOA_HUMAN	203282367	78%	531	4.3e-048	48	47350	6.99	1.07	0.614	1.92	0.008	1.12	0.479
816	alpha-enolase	P06733	ENOA_HUMAN	203282367	80%	383	2.7e-033	45	47350	6.99	−1.03	0.803	1.54	0.008	1.05	0.737
1426	triosephosphate isomerase isoform 1	P60174	TPIS_HUMAN	4507645	97%	631	4.3e-058	51	26938	6.45	1.13	0.515	1.95	0.025	1.09	0.582
1443	triosephosphate isomerase isoform 1	P60174	TPIS_HUMAN	4507645	94%	830	5.4e-078	53	26938	6.45	−1.02	0.946	1.92	0.049	1.18	0.501
1461	triosephosphate isomerase isoform 1	P60174	TPIS_HUMAN	66360365	55%	171	4.3e-012	26	26938	6.45	−1.56	0.033	−1.08	0.667	−1.13	0.494
1008	fructose-bisphosphate aldolase C	P09972	ALDOC_HUMAN	61680382	61%	138	8.6e-009	23	37940	6.67	−1.23	0.047	−1.07	0.334	1.35	0.003
	Others
1357	chloride intracellular channel protein 1	O00299	CLIC1_HUMAN	14251209	81%	322	3.4e-027	31	27248	5.09	1.2	0.107	−1.55	0.009	−1.2	0.064
1370	chloride intracellular channel protein 1	O00299	CLIC1_HUMAN	14251209	75%	506	1.4e-045	38	27248	5.09	−1.04	0.808	−1.65	0.013	−1.22	0.213

^a)The spot number; protein name; UniProt accession number; UniProt ID; NCBI accession number; sequence coverage; MOWSE score; p-value relative to the MASCOT identification; number of queries matched; theoretical molecular weight (expressed in Da) and isoelectric point (expressed in pH units); the fold change and relative t-test value for co-cultures treated with AgNO₃, Ag 20 nm NPs and Ag 200 nm NPs, respectively, are reported for each protein. Italics = protein is more abundant; Bold = protein is less abundant.

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