HR-MAS NMR spectroscopy of reconstructed human epidermis: Potential for the in situ investigation of the chemical interactions between skin allergens and nucleophilic amino acids

Chemical Research in Toxicology

Volumn 26, Issue 1, 2013, Pages 136-145

  Elbayed, Karim ^a   Berl, Valérie ^a   Debeuckelaere, Camille ^a   Moussallieh, François Marie ^a,b   Piotto, Martial ^c   Namer, Izzie Jacques ^a,b   Lepoittevin, Jean Pierre ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^c Bruker Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; AMINO ACID; CYSTEINE; HISTIDINE; HUMAN SERUM ALBUMIN; METHIONINE;

ARTICLE; CHEMICAL INTERACTION; EPIDERMIS; HIGH RESOLUTION MAGIC ANGLE SPINNING; HUMAN; IMMUNE SYSTEM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOPHILICITY; PHENOTYPE; STEREOCHEMISTRY;

ALKANESULFONATES; ALLERGENS; AMINO ACIDS; CARBON ISOTOPES; CELL CULTURE TECHNIQUES; CELL LINE; CYSTEINE; EPIDERMIS; HISTIDINE; HUMANS; METHIONINE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SERUM ALBUMIN;

EID: 84872588615     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300428u     Document Type: Article

References (71)

1. Lowe, I. J. (1959) Free induction decays of rotating solids Phys. Rev. Lett. 2, 285-287
2. Andrew, E. R., Bradbury, A., and Eades, R. G. (1959) Removal of dipolar broadening of nuclear magnetic resonance spectra of solids by specimen rotation Nature 183, 1802-1803
3. Lippens, G., Bourdonneau, M., Dhalluin, C., Warrass, R., Richert, T., Seetharaman, C., Boutillon, C., and Piotto, M. (1999) Study of compounds attached to solid supports using high resolution magic angle spinning NMR Curr. Org. Chem. 3, 147-169
4. Cheng, L. L., Lean, C. L., Bogdanova, A., Wright, S. C., Jr, Ackerman, J. L., Brady, T. J., and Garrido, L. (1996) Enhanced resolution of proton NMR spectra of malignant lymph nodes using magic-angle spinning Magn. Reson. Med. 36, 653-658
5. Cheng, L. L., Ma, M. J., Becerra, L., Ptak, T., Tracey, I., Lackner, A., and Gonzàlez, R. G. (1997) Quantitative neuropathology by high resolution magic angle spinning proton magnetic resonance spectroscopy Proc. Natl. Acad. Sci. U.S.A. 94, 6408-6413
6. Bathen, T. F., Sitter, B., Sjøbakk, T. E., Tessem, M. B., and Gribbestad, I. S. (2010) Magnetic resonance metabolomics of intact tissue: a biotechnological tool in cancer diagnostics and treatment evaluation Cancer Res. 70, 6692-6696
7. Martínez-Bisbal, M. C., Martí-Bonmatí, L., Piquer, J., Revert, A., Ferrer, P., Llácer, J. L., Piotto, M., Assemat, O., and Celda, B. (2004) 1H and 13C HR-MAS spectroscopy of intact biopsy samples ex vivo and in vivo 1H MRS study of human high grade gliomas NMR Biomed. 17, 191-205
8. Cheng, L. L., Anthony, D. C., Comite, A. R., Black, P. M., Tzika, A. A., and Gonzalez, R. G. (2000) Quantification of microheterogeneity in glioblastoma multiforme with ex vivo high-resolution magic-angle spinning (HRMAS) proton magnetic resonance spectroscopy Neuro-Oncol. 2, 87-95
9. Tzika, A. A., Cheng, L. L., Goumnerova, L., Madsen, J. R., Zurakowski, D., Astrakas, L. G., Zarifi, M. K., Michael Scott, R., Anthony, D. C., Gilberto Gonzalez, R., and Black, P. M. (2002) Biochemical characterization of pediatric brain tumors by using in vivo and ex vivo magnetic resonance spectroscopy J. Neurosurg. 96, 1023-1031
10. Erb, G., Elbayed, K., Piotto, M., Raya, J., Neuville, A., Mohr, M., Maitrot, D., Kehrli, P., and Namer, I. (2008) Toward improved grading of malignancy in oligodendrogliomas using metabolomics. J Magn. Reson. Med. 59, 959-965
11. Gribbestad, I. S., Sitter, B., Lundgren, S., Krane, J., and Axelson, D. (1999) Metabolite composition in breast tumors examined by proton nuclear magnetic resonance spectroscopy Anticancer Res. 19, 1737-1746
12. Moccia, M., Pellecchia, M. T., Erro, R., Zingone, F., Marelli, S., Barone, D. G., Ciacci, C., Strambi, L. F., and Barone, P. (2010) Restless legs syndrome is a common feature of adult celiac disease Mov. Disord. 25, 877-881
13. Cheng, L. L., Wu, C.-L., Smith, M. R., and Gonzalez, R. G. (2001) Non-destructive quantitation of spermine in human prostate tissue samples using HRMAS 1H NMR spectroscopy at 9.4 T FEBS Lett. 494, 112-116
14. Swindle, P., Ramadan, S., Stanwell, P., McCredie, S., Russell, P., and Mountford, C. (2008) Proton magnetic resonance spectroscopy of the central, transition and peripheral zones of the prostate: assignments and correlation with histopathology Magn. Reson. Mater. 21, 423-434
15. Van Asten, J. J. A., Cuijpers, V., Hulsbergen-Van De Kaa, C., Soede-Huijbregts, C., Witjes, J. A., Verhofstad, A., and Heerschap, A. (2008) High resolution magic angle spinning NMR spectroscopy for metabolic assessment of cancer presence and Gleason score in human prostate needle biopsies Magn. Reson. Mater. 21, 435-442
16. 1H-high-resolution magic angle spinning (HRMAS) NMR spectroscopy J. Pediatr. Blood Cancer 56 (1) 24-34
17. Moka, D., Vorreuther, R., Schicha, H., Spraul, M., Humpfer, E., Lipinski, M., Foxall, P. J. D., Nicholson, J. K., and Lindon, J. C. (1997) Magic angle spinning proton magnetic resonance spectroscopic analysis of intact kidney sample tissues Anal. Commun. 34, 107-109
18. Tate, A. R., Foxall, P. J. D., Holmes, E., Moka, D., Spraul, M., Nicholson, J. K., and Lindon, J. C. (2000) Distinction between normal and renal cell carcinoma kidney cortical biopsy samples using pattern recognition of (1)H magic angle spinning (MAS) NMR spectra NMR Biomed. 13, 64-71
19. Mahon, M. M., Cox, I. J., Dina, R., Soutter, W. P., McIndoe, G. A., Williams, A. D., and DeSouza, N. M. (2004) 1)H magnetic resonance spectroscopy of preinvasive and invasive cervical cancer: in vivo-ex vivo profiles and effect of tumor load J. Magn. Reson. Imaging 19, 356-364
20. Mountford, C. E., Delikatny, E. J., Dyne, M., Holmes, K. T., Mackinnon, W. B., Ford, R., Hunter, J. C., Truskett, I. D., and Russell, P. (1990) Uterine cervical punch biopsy specimens can be analyzed by 1H MRS Magn. Reson. Med. 13, 324-331
21. Dave, U., Taylor-Robinson, S. D., Walker, M. M., Mahon, M., Puri, B. K., Thursz, M. R., Desouza, N. M., and Cox, I. J. (2004) In vitro 1H-magnetic resonance spectroscopy of Barrett's esophageal mucosa using magic angle spinning techniques Eur. J. Gastroenterol. Hepatol. 16, 1199-1205
22. Namer, I. J., Ben Sellem, D., Elbayed, K., Neuville, A., Moussallieh, F.-M., Lang-Averous, G., Piotto, M., and Bellocq, J.-P. (2011) Metabolomic characterization of ovarian epithelial carcinomas by HRMAS-NMR spectroscopy J. Oncol. 10.1155/2011/174019
23. Piotto, M., Moussallieh, F. M., Dillmann, B., Imperiale, A., Neuville, A., Brigand, C., Bellocq, J. P., Elbayed, K., and Namer, I. J. (2009) Metabolic characterization of primary human colorectal cancers using high resolution magic angle spinning H-1 magnetic resonance spectroscopy Metabolomics 5, 292-301
24. Chan, E. C. Y., Koh, P. K., Mal, M., Cheah, P. Y., Eu, K. W., Backshall, A., Cavill, R., Nicholson, J. K., and Keun, H. C. (2009) Metabolic profiling of human colorectal cancer using high-resolution magic angle spinning nuclear magnetic resonance (HR-MAS NMR) spectroscopy and gas chromatography mass spectrometry (GC/MS) J. Proteome Res. 8, 352-361
25. Benahmed, M. A., Santelmo, N., Elbayed, K., Frossard, N., Noll, E., Canuet, M., Pottecher, J., Diemunsch, P., Piotto, M., Massard, G., and Namer, I. J. (2011) The assessment of the quality of the graft in an animal model for lung transplantation using the metabolomics (1) H high-resolution magic angle spinning NMR spectroscopy Magn. Reson. Med. 68, 1026-1038
26. 1H high resolution magic angle spinning nuclear magnetic resonance: a case report J. Med. Case Rep. 6, 22
27. Landsteiner, K. and Jacobs, J. (1936) Studies on the sensitization of animals with simple chemical compounds J. Exp. Med. 64, 625-629
28. Lepoittevin, J.-P. (2011) Molecular Aspects in Allergic and Irritant Contact Dermatitis, in Contact Dermatitis (Duus Johansen, J., Frosch., P. J., and Lepoittevin, J.-P., Eds.) 5 th ed., pp 91-110, Springer-Verlag, Berlin.
29. Lepoittevin, J.-P. and Leblond, I. (1997) Hapten-protein-T cell receptor interactions Eur. J. Dermatol. 7, 151-154
30. Meschkat, E., Barratt, M. D., and Lepoittevin, J. P. (2001) Studies of the chemical selectivity of hapten, reactivity, and skin sensitization potency. 1. Synthesis and studies on the reactivity toward model nucleophiles of the (13)C-labeled skin sensitizers hex-1-ene- and hexane-1,3-sultones Chem. Res. Toxicol. 14, 110-117
31. Alvarez-Sanchez, R., Basketter, D. A., Pease, C., and Lepoittevin, J. P. (2003) Studies of chemical selectivity of hapten, reactivity, and skin sensitization potency. 3. Synthesis and studies on the reactivity toward model nucleophiles of the 13C-labeled skin sensitizers, 5-chloro-2-methylisothiazol-3- one (MCI) and 2-methylisothiazol-3-one (MI) Chem. Res. Toxicol. 16, 627-636
32. Eilstein, J., Giménez-Arnau, E., Duché, D., Rousset, F., and Lepoittevin, J.-P. (2006) Synthesis and reactivity toward nucleophilic amino acids of 2,5-[13C]-dimethyl-p-benzoquinonediimine Chem. Res. Toxicol. 19, 1248-1256
33. Baker, A., Zidek, L., Wiesler, D., Chmelik, J., Pagel, M., and Novotny, M. V. (1998) Reaction of N-acetylglycyllysine methyl ester with 2-alkenals: an alternative model for covalent modification of proteins Chem. Res. Toxicol. 11, 730-740
34. Alvarez-Sanchez, R., Divkovic, M., Basketter, D. A., Pease, C., Panico, M., Dell, A., Morris, H., and Lepoittevin, J. P. (2004) Effect of glutathione on the covalent binding of the 13C-labeled skin sensitizer 5-chloro-2- methylisothiazol-3-one to human serum albumin: identification of adducts by nuclear magnetic resonance, matrix-assisted laser desorption/ionization mass spectrometry, and nanoelectrospray tandem mass spectrometry Chem. Res. Toxicol. 17, 1280-1288
35. Redeby, T., Nilsson, U., Altamore, T. M., Ilag, L., Ambrosi, A., Broo, K., Börje, A., and Karlberg, A.-T. (2010) Specific adducts formed through a radical reaction between peptides and contact allergenic hydroperoxides Chem. Res. Toxicol. 23, 203-210
36. Divkovic, M., Pease, C. K., Gerberick, G. F., and Basketter, D. A. (2005) Hapten-protein binding: from theory to practical application in the in vitro prediction of skin sensitization Contact Dermatitis 53, 189-200
37. Rosdy, M. and Clauss, L. C. (1990) Terminal epidermal differentiation of human keratinocytes grown in chemically defined medium on inert filter substrates at the air-liquid interface J. Invest. Dermatol. 95, 409-414
38. Ponec, M. (1995) Reconstructed human epidermis in vitro: an alternative to animal testing ATLA 23, 97-110
39. Bernard, F.-X., Barrault, C., Deguercy, A., De Wever, B., and Rosdy, M. (2000) Expression of type 1 5alpha-reductase and metabolism of testosterone in reconstructed human epidermis (SkinEthic®): a new model for screening skin-targeted androgen modulators Int. J. Cosmetic Sci. 22, 397-407
40. Gysler, A., Kleuser, B., Sippl, W., Lange, K., Korting, H. C., Höltje, H.-D., and Schäfer-Korting, M. (1999) Skin penetration and metabolism of topical glucocorticoids in reconstructed epidermis and in excised human skin Pharm. Res. 16, 1386-1391
41. De Brugerolle de Fraisinette, A., Picarles, V., Chibout, S., Kolopp, M., Medina, J., Burtin, P., Ebelin, M.-E., Osborne, S., Mayer, F. K., Spake, A., Rosdy, M., De Wever, B., Ettlin, R. A., and Cordier, A. (1999) Predictivity of an in vitro model for acute and chronic skin irritation (SkinEthic) applied to the testing of topical vehicles Cell Biol. Toxicol. 15, 121-135
42. Tornier, C., Rosdy, M., and Maibach, H. I. (2006) In vitro skin irritation testing on reconstituted human epidermis: reproducibility for 50 chemicals tested with two protocols Toxicol. in Vitro 20, 401-416
43. Coquette, A., Berna, N., Vandenbosch, A., Rosdy, M., and Poumay, Y. (1999) Differential expression and release of cytokines by an in vitro reconstructed human epidermis following exposure to skin irritant and sensitizing chemicals Toxicol. in Vitro 13, 867-877
44. Alépée, N., Tornier, C., Robert, C., Amsellem, C., Roux, M.-H., Doucet, O., Pachot, J., Méloni, M., and de Brugerolle de Fraissinette, A. (2010) A catch-up validation study on reconstructed human epidermis (SkinEthic RHE) for full replacement of the Draize skin irritation test Toxicol. in Vitro 24, 257-266
45. 13C methyl alkanesulfonates: new lipophilic methylating agents for the identification of nucleophilic amino acids of proteins by NMR Tetrahedron Lett. 33, 3875-3878
46. Roberts, D. W., Goodwin, B. F. J., and Basketter, D. (1988) Methyl groups as antigenic determinants in skin sensitisation Contact Dermatitis 18, 219-225
47. Fraginals, R., Lepoittevin, J.-P., and Benezra, C. (1990) Sensitizing capacity of three methyl alkanesulphonates: a murine in vivo and in vitro model of allergic contact dermatitis Arch. Dermatol. Res. 282, 455-458
48. Piotto, M., Moussallieh, F. M., Imperiale, A., Detour, J., Bellocq, J. P., Namer, I. J., and Elbayed, K. (2012) In Methodologies in Metabolics (Lutz, N., Sweedler, J. V., and Wevers, R. A., Eds.) Cambridge University Press: Cambridge, U.K.
49. Piotto, M., Elbayed, K., Wieruszeski, J. M., and Lippens, G. (2005) Practical aspects of shimming a high resolution magic angle spinning probe J. Magn. Reson. 173, 84-89
50. Carr, H. Y. and Purcell, E. M. (1954) Effects of diffusion on free precession in nuclear magnetic resonance experiments Phys. Rev. 94, 630-638
51. Elbayed, K., Dillmann, B., Raya, J., Piotto, M., and Engelke, F. (2005) Field modulation effects induced by sample spinning: application to high-resolution magic angle spinning NMR Adv. Magn. Reson. 174, 2-26
52. 1 inhomogeneities J. Magn. Reson. 149, 114-118
53. Wider, G. and Dreier, L. (2006) Measuring protein concentrations by NMR spectroscopy J. Am. Chem. Soc. 128, 2571-2576
54. Shaka, A. J., Lee, C. J., and Pines, A. (1988) Iterative schemes for bilinear operators: application to spin decoupling J. Magn. Reson. 77, 274-293
55. Davis, A. L., Keeler, J., Laue, E. D., and Moskau, D. (1992) Experiments for recording pure-adsorption heteronuclear correlation spectra using pulsed field gradients J. Magn. Reson. 98, 207-216
56. Willker, W., Leibfritz, D., Kerssebaum, R., and Bermel, W. (1993) Gradient selection in inverse heteronuclear correlation spectroscopy Magn. Reson. Chem. 31, 287-292
57. Detour, J., Elbayed, K., Piotto, M., Moussallieh, F. M., Nehlig, A., and Namer, I. J. (2011) Ultrafast in vivo microwave irradiation for enhanced metabolic stability of brain biopsy samples during HRMAS NMR analysis J. Neurosci. Methods 201, 89-97
58. Martínez-Granados, B., Monleón, D., Martínez-Bisbal, M. C., Rodrigo, J. M., del Olmo, J., Lluch, P., Ferrández, A., Martí-Bonmati, L., and Celda, B. (2006) Metabolite identification in human liver needle biopsies by high-resolution magic angle spinning 1H NMR spectroscopy NMR Biomed. 19, 90-100
59. Janeke, G., Siefken, W., Carstensen, S., Springmann, G., Bleck, O., Steinhart, H., Höger, P., Wittern, K.-P., Wenck, H., Stäb, F., Sauermann, G., Schreiner, V., and Doering, T. (2003) Role of taurine accumulation in keratinocyte hydration J. Invest. Dermatol. 121, 354-361
60. Silva, D. L. P., Thiago, S. B., Pessoîa, F. A., Mrestani, Y., Rüttinger, H. H., Wohlrab, J., and Neubert, R. H. H. (2008) Penetration profile of taurine in the human skin and its distribution in skin layers Pharm. Res. 25, 1846-1850
61. Lazariev, A., Allouche, A.-R., Aubert-Frécon, M., Fauvelle, F., Piotto, M., Elbayed, K., Namer, I.-J., van Ormondt, D., and Graveron-Demilly, D. (2011) Optimization of metabolite basis sets prior to quantitation in magnetic resonance spectroscopy: an approach based on quantum mechanics Meas. Sci. Technol. 22, 114020
62. Ponec, M., Boelsma, E., Weerheim, A., Mulder, A., Bouwstra, J., and Mommaas, M. (2000) Lipid and ultrastructural characterization of reconstructed skin models Int. J. Pharm. 203, 211-225
63. 323-336 Lett. Pept. Sci. 4/5/6, 467-472
64. Gerberick, G. F., Aleksic, M., Basketter, D. A., Casati, S., Karlberg, A.-T., Kern, P., Kimber, I., Lepoittevin, J.-P., Natsch, A., Ovigne, J.-M., Rovida, C., Sakagushi, H., and Schultz, T. (2008) Chemical reactivity measurement and the predictive identification of skin sensitisers ATLA 36, 215-242
65. Kato, H., Okamoto, M., Yamashita, K., Nakamura, Y., Fukumori, Y., Nakai, K., and Kaneko, H. (2003) (2003) Peptide-binding assessment using mass spectrometry as a new screening method for skin sensitization J. Toxicol. Sci. 28, 19-24
66. Schultz, T. W., Yarbrough, J. W., and Johnson, E. L. (2005) Structure-activity relationships for reactivity of carbonyl-containing compounds with glutathione SAR QSAR Environ. Res. 16, 313-322
67. Aptula, A. O., Patlewicz, G., Roberts, D. W., and Schultz, T. W. (2006) Non-enzymatic glutathione reactivity and in vitro toxicity: a non-animal approach to skin sensitization Toxicol. in Vitro 20, 239-247
68. Gerberick, G. F., Vassallo, J. D., Bailey, R. E., Chaney, J. G., Morrall, S. W., and Lepoittevin, J.-P. (2004) Development of a peptide reactivity assay for screening contact allergens Toxicol. Sci. 81, 332-343
69. Gerberick, G. F., Vassallo, J. D., Foertsch, L. M., Price, B. B., Chaney, J. G., and Lepoittevin, J.-P. (2007) Quantification of chemical peptide reactivity for screening contact allergens: a classification tree model approach Toxicol. Sci. 97, 417-427
70. Natsch, A. and Gfeller, H. (2008) LC-MS-based characterization of the peptide reactivity of chemicals to improve the in vitro prediction of the skin sensitization potential Toxicol. Sci. 106, 464-478
71. Kimber, I., Basketter, D. A., Butler, M., Gamer, A., Garrigue, J.-L., Gerberick, G. F., Newsome, C., Steiling, W., and Vohr, H. W. (2003) Classification of contact allergens according to potency: proposals Food Chem. Toxicol. 41, 1799-1809