Address

Institut Interdisciplinaire de Recherche de Grenoble (IRIG)
SYstèmes Moléculaires et nanoMatériaux pour l’Energie et la Santé (SyMMES)
Chimie Interface Biologie pour l’Environnement, la Santé et la Toxicologie (CIBEST)
CEA-Grenoble
17 avenue des Martyr
38054 Grenoble cedex 09

Research interests

Toxicity and ecotoxicity of nanomaterials.

Research in our lab is focused on DNA damage and repair, from damage recognition, development of analytical techniques to detect and quantify them with the highest sensitivity and selectivity, to genotoxicity assessment. In this context, my main research interest is engineered nanomaterial (ENM) toxicity and ecotoxicity.

The effects of ENM are assessed on in vitro models: lung, liver, kidney cells lines, intestinal models (mono- and co-culture systems, representative of the ileum epithelium and Peyer’s patches), skin models (primary keratinocytes from human donors or whole human skin assays).

More specifically, toxicological studies are focused on the impact of nanomaterials on DNA (genotoxicity) and DNA repair systems, which are linked to oxidative stress and inflammation assessment. A multidisciplinary approach is used, going from classical toxicity testing (cytotoxicity; genotoxicity: comet assay, micronucleus assay, HPLC-MS/MS, gamma-H2AX or 53BP1 immunostaining etc.; molecular approaches: RT-qPCR, western blot, ELISA etc.) to medium-scale and high-content analysis (HCA, Cell Insight) and -omics approaches (transcriptomics, proteomics) coupled to state-of-the-art microscopy techniques (TEM, STEM, µXRF on synchrotrons, µPIXE on nuclear microprobes). The physico-chemistry and fate of nanomaterials are characterized (dynamic light scattering, X-ray diffraction, X-ray absorption spectroscopy, Raman spectroscopy etc.).

Topics

• Towards safer-by-design quantum dots. In collaboration with chemists from CEA/SyMMES/STEP, and in the frame of the LabEx SERENADE,we design and assess the toxicity of new quantum dot formulations, with different chemical composition, core-shell structure, surface chemistry, focusing on low-toxicity and earth-abundant chemical elements.
• Toxicity of particulate food additives on intestinal models. E171 and E551, i.e. TiO₂ and SiO₂, respectively, are authorized additives that are used in a wide range of food products. We focus on the assessment of their potential translocation through the gastro-intestinal tract and on their toxicity in intestinal models, either healthy or with genetic susceptibility to inflammatory bowel disease.
• Toxicity of biomaterials and nanomedicines. In the frame of the BIORIMA (H2020) project, the toxicity of bionanomaterials and nanomedicines is evaluated.
• Genotoxicity of metal oxide nanoparticles using realistic exposure scenario, especially via the inhalation route: chronic exposure, air-liquid exposure (coll. KIT, Germany).

Funding

H2020 (BIORIMA, 2017-2021; COST Action hCOMET CA15132); FP7 (NanoMile, 2013-2017; NanoLINEN, 2010-2012); ANR (PAIPITO, 2017-2020; NEUTRINOS, 2017-2020, ANTIDOTE, 2017-2020; Signanotox, 2007-2010); ANSES (Silimmun, 2015-2018; Nanogut, 2013-2016; Innimmunotox, 2011-2014 and NanoPIST, 2008-2011); Plan Cancer (SiFoodCan, 2016-2019); Labex SERENADE (2012-2020); INERIS/MEEDDM (NanoTrans, 2009-2012); C’nano Ile de France (PLUTON and NanoDIG, 2010-2012); CEA/Toxicology and Nanoscience programs (Plantura, 2013-2016; Bamaco, 2013-2016; Nanostress, 2012-2014; Transrad, 2011-2012; NanoBioMet, Transrad, BiotUrBacium, 2010-2011).


Curriculum

2014: HDR, école doctorale de chimie et des sciences du vivant (EDCSV), Grenoble, "Impact of uranium and nanoparticles on human and environmental models".
2010-today: researcher, CEA Grenoble, Laboratoire Lésions des Acides Nucléiques (Nucleic acid lesions laboratory, LAN). Toxicity and ecotoxicity of nanoparticles and carbon nanotubes.
2004-2010: researcher, CEA Saclay, Laboratoire Pierre Süe (LPS) then Laboratoire Structure et Dynamique par Résonance Magnétique (LSDRM). Toxicity and ecotoxicity of uranium, metal oxide nanoparticles and carbon nanotubes.
2002-2004: post-doctoral position, Laboratoire Pierre Süe, CEA Saclay. Nephrotoxicity of uranium.
1998-2002: Ph.D. thesis; CNRS-Aventis Pharma. Synthesis and optimization of lipidic vectors (cationic lipids, formulated as micelles or liposomes) for gene delivery; in vitro testing.
1998: AgroParisTech, specialization in analytical chemistry; Master “Physico-chemistry and quality of bioproducts”.

Supervision

Post-doc
Ana Peropadre (Feb. 2019-Aug. 2020)
Eline Bartolami (Feb. 2019-May 2020)
Marie-Edith Arnal (Sep. 2018-March 2020)
Céline Tisseyre (June 2017-Dec. 2018)
Adeline Tarantini (Dec. 2014-Dec. 2016)
Laure Bobyk (Janv. 2014-July 2015)
Lucie Armand (Nov. 2012-Nov. 2014)
Emilie Brun (Oct. 2009-Sept. 2011)
Mary-Line Jugan (Oct. 2008-Juill. 2010)
Sabrina Barillet (Nov. 2007-Mai 2009)

Ph.D.
Fanny Dussert (Nov. 2017-Nov. 2020)
Marie Dorier (Nov. 2013-Nov. 2016)
Mathilde Biola (Oct. 2012-Jan. 2016)
Camille Larue (Oct. 2008-sept. 2011)
Julien Laurette (Oct. 2007-sept. 2010)
Angélique Simon-Deckers (Oct. 2005-sept. 2008)

Publications

2019
K.-D. Wegner, F. Dussert, D. Truffier-Boutry, A. Benayad, D. Beal, L. Mattera, W.-L. Ling, M. Carrière, P. Reiss. Influence of the core/shell structure of indium phosphide based quantum dots on their photostability and cytotoxicity. Frontiers in chemistry, 2019.

A. Tarantini, K.-D. Wegner, F. Dussert, G. Sarret, D. Beal, L. Mattera, C. Lincheneau, O. Proux, D. Truffier-Boutry, C. Moriscot, B. Gallet, P.-H. Jouneau, P. Reiss, M. Carrière. Physicochemical alterations and toxicity of InP alloyed quantum dots aged in environmental conditions: A safer by design evaluation. Nanoimpact, 14: 100168, 2019.

K.-D. Wegner, S. Pouget, W.-L. Ling, M. Carrière and P. Reiss. Gallium – a versatile element for tuning the photoluminescence properties of InP quantum dots. ChemCom, 55(11): 1663-1666, 2019.

F. Fus, Y. Yang, HZ Shirley Lee, S. Top, M. Carriere, A. Bouron, A. Pacureanu, JC da Silva, M. Salmain, A. Vessières, P. Cloetens, G. Jaouen, S. Bohic. Intracellular localization of an osmocenyl-tamoxifen derivative in breast cancer cells revealed by synchrotron radiation X-ray fluorescence imaging. Angewandte Chemie, 58(11): 3461-3465, 2019.

B. Dalzon, M. Guidetti, D. Testemale, S. Reymond, O. Proux, J. Vollaire, V. Collin-Faure, I. Testard, D. Fenel, G. Schoehn, J. Arnaud, M. Carrière, V. Josserand, T. Rabilloud, C. Aude-Garcia. Utility of macrophages in an antitumor strategy based on the vectorization of iron oxide nanoparticles. Nanoscale, 11(19): 9341-9352, 2019.

2018
M. Dorier, D. Béal, C. Marie-Desvergne, M. Dubosson, F. Barreau, E. Houdeau, N. Herlin-Boime, T. Rabilloud, M. Carrière. The food additive E171 and titanium dioxide nanoparticles indirectly alter the homeostasis of the human intestinal epithelial cells, in vitro. Env. Sci.: Nano, 6, 1549-1561, 2019.

MJ. Bessa, F. Brandao, MM. Querido, C. Costa, C. Costa Pereira, V. Valdiglesias, B. Laffon, M. Carrière, JP. Teixeira, S. Fraga. Optimization of the harvesting and freezing conditions of human cell lines for DNA damage analysis by the alkaline comet assay. Mutat. Res., 2018.

N. Fernandez-Bertolez, C. Costa, MJ. Bessa, M. Park, M. Carrière, F. Dussert, JP. Teixeira, E. Pasaro, B. Laffon, V. Valdiglesias. Assessment of oxidative damage induced by iron oxide nanoparticles on different nervous system cells. Mutat. Res., 2019.

M. Dorier, C. Tisseyre, F. Dussert, D. Beal, M.-E. Arnal, T. Douki, V. Valdiglesias, B. Laffon, S. Fraga, F. Brandao, N. Herlin-Boime, F. Barreau, T. Rabilloud, M. Carrière. Toxicological impact of acute exposure to E171 food additive and TiO₂ nanoparticles on a co-culture of Caco-2 and HT29-MTX intestinal cells. Mutat. Res., 2019.

C. Larue, C. Baratange, D. Vantelon, H. Khodja, S. Surblé, A. Elger, M. Carrière. Influence of soil type on TiO₂ nanoparticle fate in an agro-ecosystem. Sci. Total Env., 630: 609-617, 2018.

2017
M. Dorier, D. Béal, C. Marie-Desvergne, M. Dubosson, F. Barreau, E. Houdeau, N. Herlin-Boime, M. Carrière. Continuous in vitro exposure of intestinal epithelial cells to E171 food additive causes oxidative stress, inducing oxidation of DNA bases but no endoplasmic reticulum stress. Nanotoxicology, 11(6): 751-761, 2017.

JY. Bottero, J. Rose, C. de Garidel, A. Masion, T. Deutsch, G. Brochard, M. Carrière, N. Gontard, H. Wortham, T. Rabilloud, B. Salles, M. Dubosson, B. Cathala, D. Boutry, E. Erekovsky, C. Auplat, L. Charlet, T. Heulin, E. Frejafon and S. Lanone. SERENADE: Safer and eco-design research and education applied to nanomaterial development, the new generation of materials safer by design. Env. Sci.: Nano, 24, 526-538, 2017.

Kaur I., Ellis LJ. Romer I., Tantra R., Carrière M., Allard S., Mayne-L’hermite M., Minelli C., Unger W., Potthoff A., Rades S., Valsami-Jones E. Dispersion of nanomaterials in aqueous media: Towards protocol optimization. J. Vis. Exp. 130, 2017.

B. Dalzon, C. Aude-Garcia, V. Collin-Faure, H. Diemer, D. Béal, F. Dussert, D. Fenel, G. Schoehn, S. Cianférani, M. Carrière, T. Rabilloud. Differential proteomics highlights macrophage-specific responses to amorphous silica nanoparticles. Nanoscale 9(27): 9641-9658, 2017

A. Pradas del Real, V. Vidal, M. Carrière, H. Castillo-Michel, C. Levard, P. Chaurand, G. Sarret. Silver nanoparticles and wheat roots: A complex interplay. Environ. Sci. Technol. 51(10): 5774-5782, 2017.

S. Bettini, E. Boutet-Robinet, C. Cartier, C. Comera, E. Gaultier, J. Dupuy, N. Naud, S. Taché, P. Grysan, S. Reguer, N. Thieriet, M. Réfrégier, D. Thiaudière, J.-P. Cravedi, M Carrière, J.-N. Audinot, F. Pierre, L. Guzylack-Piriou, E. Houdeau. Food-grade TiO₂ impairs intestinal immune homeostasis, initiates preneoplasic lesions and promotes aberrant crypt development in the rat colon. Sci. Rep., 7: 40373, 2017.

M. Carrière, S. Sauvaigo, T. Douki, JL. Ravanat. Impact of nanoparticles on DNA repair: Current knowledge and future perspectives. Mutagenesis, 32(1): 203-213, 2017.

M. Biola-Clier, D. Beal, S. Caillat, S. Libert L. Armand, N. Herlin-Boime, S. Sauvaigo, T. Douki, M. Carrière. Comparison of the DNA damage response of BEAS-2B and A549 cells exposed to titanium dioxide nanoparticles. Mutagenesis, 32(1): 161-172, 2017.

2016
G. Veronesi, A. Deniaud, T. Gallon, P.-H. Jouneau, J. Villanova, P. Delangle, M. Carrière, I. Kieffer, P. Charbonnier, E. Mintz, I. Michaud-Soret. Visualization, quantification and coordination of Ag⁺ ions released from silver nanoparticles in hepatocytes. Nanoscale, 8(38): 17012-17021, 2016.

G. Klein, C. Mathé, M. Biola-Clier, S. Devineau, E. Douineau, E. Hatem, L. Marichal, B. Alonso, J.-C. Gaillard, G. Laniel, J. Armengaud, M. Carrière, S. Chédin, Y. Boulard, S. Pin, J.-P. Renault, J.-C. Aude, J. Labarre. RNA binding proteins are a major target of silica nanoparticles in cell extracts. Nanotoxicology, 10(10): 1555-1564, 2016.

P. Reiss, M. Carrière, C. Lincheneau, L Vaure, S. Tamang. Syntheis of semiconductor nanocrystals, focusing on nontoxic and earth-abundant materials. Chem. Rev., 116(18): 10731-819, 2016.

A. Pradas del Real, H. Castillo-Michel, R. Kaegi, B. Sinnet, V. Magnin, N. Findling, J. Villanova, M. Carrière, C. Santaella, A. Fernandez-Martinez, C. Levard, G. Sarret. Fate of Ag-NPs in sewage sludge after application on agricultural soils. Environmental Science and Technology, 50(4): 1759-68, 2016.

L. Armand, A. Tarantini, D. Beal, M. Biola-Clier, L. Bobyk, S. Sorieul, K. Pernet-Gallay, C. Desvergne, I. Lynch, N. Herlin-Boime, M. Carrière. Long-term exposure of A549 cells to titanium dioxide nanoparticles induces DNA damage and sensitizes cells towards genotoxic agents. Nanotoxicology, 10(7): 913-23, 2016.

C. Aude-Garcia, B. Dalzon, JL. Ravanat, V. Collin-Faure, H. Diemer, JM Strub, S. Cianferani, A Van Dorsselaer, M. Carrière and T. Rabilloud. A combined proteomic and targeted analysis unravels new toxic mechanisms for zinc oxide nanoparticles in macrophages. J. Proteomics, 134: 174-185, 2016.

L. Armand, M. Biola-Clier, L. Bobyk, V. Collin-Faure, H. Diemer, S. Cianferani, A. Van Dorsselaer, N. Herlin-Boime, T. Rabilloud and M. Carrière. Molecular responses of alveolar epithelial A549 cells to chronic exposure to titanium dioxide nanoparticles: A proteomic view. J Proteomics, 134: 163-173, 2016.

C. Aude-Garcia, V. Collin-Faure, G. Mure, K. Pernet-Gallay, P.-H. Jouneau, S. Sorieul, A. Gerdil, N. Herlin-Boime, M. Carrière and T. Rabilloud. Different in vitro exposure regimens of murine primary macrophages to silver nanoparticles induce different fate of nanoparticles and different toxicological and functional consequences. Nanotoxicology, 10(5): 586-96, 2016.

2015
G. Veronesi, T. Gallon, A. Deniaud, B. Boff, C. Gateau, C. Lebrun, C. Vidaud, F. Rollin-Genetet, M. Carrière, I. Kieffer, E. Mintz, P. Delangle, I. Michaud-Soret. XAS investigation of Silver(I) coordination in Copper(I) biological binding sites. Inorg Chem, 54(24): 11688-96, 2015.

S. Leulmi, X. Chauchet, M. Morcrette, G. Ortiz, H. Joisten, P. Sabon, T. Livache, Y. Hou, M. Carrière, S. Lequien, B. Dieny. Triggering the apoptosis of targeted human renal cells by the vibration of anisotropic magnetic particles attached to the cell membrane. Nanoscale, 7(38): 15904-14, 2015.

F. Taupin, M. Flaenders, R. Delorme, T. Brochard, JF. Mayol, J. Arnaud, P. Perriat, L. Sancey, F. Lux, RF. Barth, M. Carrière, JL. Ravanat, H. Elleaume. Gadolinium nanoparticles and contrast agent as radiation sensitizers. Phys Med Biol, 60(11): 4449-64, 2015.

M. Dorier, E. Brun, G. Veronesi, F. Barreau, K. Pernet-Gallay, C. Desvergne, T. Rabilloud, C. Carapito, N. Herlin-Boime, M. Carrière. Impact of anatase and rutile titanium dioxide nanoparticles on uptake carriers and efflux pumps in Caco-2 gut epithelial cells. Nanoscale, 7(16): 7352-60, 2015.

G. Veronesi, C. Aude-Garcia, I. Kieffer, T. Gallon, P. Delangle, N. Herlin-Boime, T. Rabilloud and M. Carrière. Exposure-dependent Ag+ release from silver nanoparticles and its complexation in AgS₂ sites in primary murine macrophages. Nanoscale, 7(16): 7323-30, 2015.

S. Triboulet, C. Aude-Garcia, L. Armand, V. Collin-Faure, M. Chevallet, H. Diemer, A. Gerdil, F. Proamer, J.-M. Strub, A. Habert, N. Herlin, A. Van Dorsselaer, M. Carrière, T. Rabilloud. Comparative proteomic analysis of the molecular responses of mouse macrophages to titanium dioxide and copper oxide nanoparticles unravels some toxic mechanisms for copper oxide nanoparticles in macrophages. Plos One, 10(4): e0124496, 2015.

2014
E. Brun, G. Veronesi, F. Barreau, C. Chanéac, B. Fayard, S. Sorieul, A. Mabondzo, N. Herlin-Boime, M. Carrière. Titanium dioxide nanoparticle translocation through ex vivo, in vivo and in vitro gut models: Identification of the more relevant in vitro model and markers of gut impact. Particle Fibre Toxicology, 11: 13, 2014

S. Triboulet, C. Aude-Garcia, L. Armand, V. Collin-Faure, H. Diemer, F. Proamer, J.-M. Strub, D. Hanau, M. Carrière, A. Van Dorsselaer and T. Rabilloud. Analysis of cellular responses of macrophages to zinc ions and zinc oxide nanoparticles: A combined targeted and proteomic approach.. Nanoscale, 6(11): 6102-14, 2014.

A. Khemiri, M. Carrière, N. Bremond, M.A. Ben Mlouka, L. Coquet, I. Llorens, V. Chapon, P. Cosette, C. Berthomieu. Escherichia coli response to uranyl exposure at low pH and associated protein regulations. PLoS One, 9(2):e89863, 2014.

K. Becker, S. Schroecksnadel, S. Geisler, M. Carrière, J. M. Gostner, H. Schennach, N. Herlin, Dietmar Fuchs. TiO₂ nanoparticles and bulk material stimulate human peripheral blood mononuclear cells. Food Chem Toxicol, 65: 63-69, 2014.

C. Larue, H. Castillo-Michel, S. Sobanska, L. Cecillon, S. Bureau, C. Dumat, V. Barthes, L. Ouerdane, M. Carrière, G. Sarret. Foliar exposure of the crop Lactuca sativa to silver nanoparticles: Evidence for internalization and changes in Ag speciation. J Haz Mat, 264: 98-106, 2014.

M. Carrière, S. Pigeot-Rémy, A. Casanova, J.-C. Lazzaroni, C. Guillard, N. Herlin-Boime. Impact of titanium dioxide nanoparticle dispersion state and dispersion method on their toxicity towards A549 lung cells and Escherichia coli bacteria. J Translat. Toxicol., 1(1): 10-20, 2014.

2013
S. Triboulet, C. Aude-Garcia, M. Carrière, H. Diemer, F. Proamer, A. Habert, M. Chevalet, V. Collin-Faure, J.-M. Strub, D. Hanau, A. Van Dorsselaer, N. Herlin-Boime and T. Rabilloud. Molecular response of mouse macrophages to copper and copper oxide nanoparticles inferred from proteomic analyses. Mol Cell Proteomics, 12(11): 3108-22, 2013.

L. Rémy, M. Carrière, A. Derret-Bobillot, C. Martini, M. Sanguinetti, E. Borézée-Durant. The Staphylococcus aureus Opp1 ABC-transporter imports nickel and cobalt in zinc-depleted conditions and contributes to virulence. Molecular Microbiology, 87(4): 730-43, 2013.

2012
I. Llorens, G. Untereiner, D. Jaillard, B. Gouget, V. Chapon, M. Carrière. Uranium interaction with three multi-resistant environmental bacteria: Cupriavidus metallidurans CH34, Deinococcus radiodurans R1 and Rhodopseudomonas palustris. PLoS One, 7(12), 2012.

G. Veronesi, E. Brun, B. Fayard, M. Cotte, M. Carrière. Structural properties of rutile TiO₂ nanoparticles accumulated in a model of gastrointestinal epithelium elucidated by micro-beam X-ray Absorption Fine Structure spectroscopy. Applied Physics Letters, 100(21), 2012.

M.-L. Jugan, S. Barillet, A. Simon-Deckers, N. Herlin, S. Sauvaigo, T. Douki and M. Carrière. Titanium sidoxide nanoparticles induce genotoxic effects and impair DNA repair activity in vitro. Nanotoxicology, 6: 501-513, 2012.

C. Larue, M. Pinault, B. Czarny, D. Georgin, D. Jaillard, N. Bendiab, M. Mayne-L’Hermite, F. Taran, V. Dive, M. Carrière. Quantitative evaluation of multi-walled carbon nanotubes uptake in wheat and rapeseed. Journal of Hazardous Material, 228: 155-163, 2012.

C. Larue, J. Laurette, N. Herlin-Boime, H. Khodja, B. Fayard, A.M. Flank, F. Brisset, M. Carrière. Accumulation, translocation and impact of TiO₂ nanoparticles in wheat (Triticum aestivum spp.). Science of the total environment, 197-208, 2012.

C. Larue, G. Veronesi, A.M. Flank, S. Surblé, N. Herlin-Boime, M. Carrière. Comparative uptake and impact of TiO₂ nanoparticles in wheat and rapeseed. Journal of Toxicology and Environmental Health A, 75(13-15): 722-734, 2012.

E. Brun, M. Carrière, A. Mabondzo. In vitro evidence of dysregulation of blood-brain barrier function after acute and repeated/long-term exposure to TiO₂ nanoparticles. Biomaterials, 33(3): 886-896, 2012.

J. Laurette, C. Larue, I. Llorens, D. Jaillard, PH. Jouneau, J. Bourguignon and M. Carrière. Speciation of uranium in plants upon root accumulation and root-to-shoot translocation: A XAS and TEM study. Environmental and experimental botany, 77: 87-95, 2012.

J. Laurette, C. Larue, C. Mariet, F. Brisset, H. Khodja, J. Bourguignon and M. Carrière. Influence of uranium speciation on its accumulation and translocation in three plant species: oilseed rape, sunflower and wheat. Environmental and experimental botany, 77: 96-107, 2012.

2011
M.-L. Jugan, S. Barillet, A. Simon-Deckers, S. Sauvaigo, T. Douki, N. Herlin and M. Carrière. Cytotoxic and genotoxic impact of TiO₂ nanoparticles on A549 cells. Journal of biomedical nanotechnology, 7(1), 22-23, 2011.

A. Casanova, M. Carrière, and N. Herlin-Boime. Dispersion of Aeroxil P25 TiO₂ nanoparticles in media of biological interest for the culture of eukaryotic cells. Journal of biomedical nanotechnology, 7(1), 24-25, 2011.

L. Mondani, K. Benzerara, M. Carrière, R. Christen, Y. Mamindy-Pajany, L. Février, N. Marmier, W. Achouak, P. Nardoux, C. Berthomieu, V. Chapon. Influence of uranium on bacterial communities: Comparison of natural uranium-rich soils with control. PLoS One, 6(10), 2011.

C. Boutin, A. Stopin, F. Lenda, T. Brotin, J.-P. Dutasta, N. Jamin, A. Sanson, Y. Boulard, F. Leteurtre, G. Huber, A. Bogaert-Buchmann, N. Tassali, H. Desvaux, M. Carrière and P. Berthault. Cell uptake of a biosensor detected by hyperpolarized 123Xe NMR: the transferrin case. Bioorganic and Medicinal Chemistry, 19: 4135-4143, 2011.

C. Boutin, H. Desvaux, M. Carrière, F. Leteurtre, N. Jamin, Y. Boulard and P. Berthault. Hyperpolarized 129Xe NMR signature of living biological cells. NMR in biomedecine, 24: 1-7, 2011.

C. Cavazza, L. Martin, E. Laffly, H. Lebrette, M. V. Cherrier, P. Richaud, M. Carrière and J. C. Fontecilla-Camps. Histidine 416 of the periplasmic binding protein NikA is essential for nickel uptake in Escherichia coli. FEBS Letters, 585(4), 2011.