Glyphosate-induced stiffening of HaCaT keratinocytes, a Peak Force Tapping study on living cells

Journal of Structural Biology

Volumn 178, Issue 1, 2012, Pages 1-7

  Heu, Celine ^a   Berquand, Alexandre ^b   Elie Caille, Celine ^a   Nicod, Laurence ^a  

^a UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^b BRUKER DALTONIK GMBH   (Germany)

Author keywords

Atomic force microscopy; Cytoskeleton; Glyphosate cytotoxicity; Keratinocyte; Sneddon model; Young's modulus

Indexed keywords

GLYPHOSATE;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL LINE; CELL MEMBRANE; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; CYTOTOXICITY; HUMAN; IC 50; KERATINOCYTE; PEAK FORCE TAPPING; PRIORITY JOURNAL;

CELL LINE; CELL MEMBRANE; CYTOSKELETON; EPIDERMIS; GLYCINE; HUMANS; KERATINOCYTES; MICROSCOPY, ATOMIC FORCE; QUERCETIN;

EID: 84859432338     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2012.02.007     Document Type: Article

References (71)

1. Adamcik J., Berquand A., Mezzenga R. Single-step direct measurement of amyloid fibrils stiffness by peak force quantitative nanomechanical atomic force microscopy. Applied Physics Letters 2011, 98. 10.1063/1.3589369.
2. Alcocer F., Whitley D., Salazar-Gonzalez J.F., Jordan W.D., Sellers M.T., et al. Quercetin inhibits human vascular smooth muscle cell proliferation and migration. Surgery 2002, 131:198-204.
3. Alonso J.L., Goldmann W.H. Feeling the forces: atomic force microscopy in cell biology. Life Sciences 2003, 72:2553-2560.
4. Amerio P., Motta A., Toto P., Pour S.M., Pajand R., et al. Skin toxicity from glyphosate surfactant formulation. Clinical Toxicology 2004, 42:317-319.
5. Belikov S., Erina E., Huang L., Su C., Prater C., et al. Parametrization of atomic force microscopy tip shape models for quantitative nanomechanical measurements. Journal of Vacuum Science and Technology B 2009, 984:1852-1860.
6. Benachour N., Sipahutar H., Moslemi S., Gasnier C., Travert C., et al. Time- and dose-dependent effects of roundup on human embryonic and placental cells. Archives of Environmental Contamination and Toxicology 2007, 53:126-133.
7. Berdyyeva T.K., Woodworth C.D., Sokolov I. Human epithelial cells increase their rigidity with aging in vitro: direct measurements. Physical Medicine and Biology 2005, 50:81-92.
8. Berquand A., Roduit C., Kasas S., Holloschi A., Ponce L., et al. Atomic force microscopy imaging of living cells. Microscopy Today 2010, 18:8-14.
9. Berquand A., Roduit C., Kasas S., Holloschi A., Ponce L., et al. Atomic force microscopy imaging of living cells. Microscopy Today 2011, (December issue).
10. Binnig G., Quate C.F., Gerber C. Atomic force microscope. Physical Review Letters 1986, 56:930-933.
11. Birukova A.A., Arce F.T., Moldobaeva N., Dudek S.M., Garcia J.G.N., et al. Endothelial permeability is controlled by spatially defined cytoskeletal mechanics: atomic force microscopy force mapping of pulmonary endothelial monolayer. Nanomedicine: Nanotechnology, Biology and Medicine 2009, 5:30-41.
12. Bolognesi C., Carrasquilla G., Volpi S., Solomon K.R., Marshall E.J.P. Biomonitoring of genotoxic risk in agricultural workers from five Colombian regions: association to occupational exposure to glyphosate. Journal of Toxicology and Environmental Health, Part A 2009, 72:986-997.
13. Boukamp P., Petrussevska R.T., Breitkreutz D., Hornung J., Markham A., et al. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. The Journal of Cell Biology 1988, 106:761-771.
14. Butt H.-J., Cappella B., Kappl M. Force measurements with the atomic force microscope: technique, interpretation and applications. Surface Science Reports 2005, 59:1-152.
15. Chouinard J.A., Grenier G., Khalil A., Vermette P. Oxidized-LDL induce morphological changes and increase stiffness of endothelial cells. Experimental Cell Research 2008, 314:3007-3016.
16. Clausen-Schaumann H., Seitz M., Krautbauer R., Gaub H.E. Force spectroscopy with single bio-molecules. Current Opinion in Chemical Biology 2000, 4:524-530.
17. Cross S.E., Jin Y.-S., Rao J., Gimzewski J.K. Nanomechanical analysis of cells from cancer patients. Nature Nanotechnology 2007, 2:780-783.
18. De Roos A.J., Zahm S.H., Cantor K.P., Weisenburger D.D., Holmes F.F., et al. Integrative assessment of multiple pesticides as risk factors for non-Hodgkin's lymphoma among men. Occupational and Environmental Medicine 2003, 60:e11.
19. Derjaguin B.V., Muller V.M., Toporov Y.P. Effect of contact deformations on the adhesion of particles. Journal of Colloid and Interface Science 1975, 53:314-326.
20. Domke J., Radmacher M. Measuring the elastic properties of thin polymer films with the AFM. Langmuir 1998, 14:3320-3325.
21. Dorobantu L.S., Gray M.R. Application of atomic force microscopy in bacterial research. Scanning 2010, 32:74-96.
22. Elie-Caille C., Heu C., Guyon C., Nicod L. Morphological damages of a glyphosate-treated human keratinocyte cell line revealed by a micro- to nanoscale microscopic investigation. Cell Biology and Toxicology 2010, 26:331-339.
23. Fierro F.A., Taubenberger A., Puech P.-H., Ehninger G., Bornhauser M., Muller D.J., Illmer T. BCR/ABL expression of myeloid progenitors increases β1-integrin mediated adhesion to stromal cells. Journal of Molecular Biology 2008, 377:1082-1093.
24. Florin E., Moy V., Gaub H. Adhesion forces between individual ligand-receptor pairs. Science 1994, 264:415-417.
25. Fung C.K.M., Seiffert-Sinha K., Lai K.W.C., Yang R., Panyard D., et al. Investigation of human keratinocyte cell adhesion using atomic force microscopy. Nanomedicine: Nanotechnology, Biology and Medicine 2010, 6:191-200.
26. Gehin A., Guyon C., Nicod L. Glyphosate-induced antioxidant imbalance in HaCaT: the protective effect of vitamins C and E. Environmental Toxicology and Pharmacology 2006, 22:27-34.
27. Gehin A., Guillaume Y.C., Millet J., Guyon C., Nicod L. Vitamins C and E reverse effect of herbicide-induced toxicity on human epidermal cells HaCaT: a biochemometric approach. International Journal of Pharmaceutics 2005, 288:219-226.
28. George J., Prasad S., Mahmood Z., Shukla Y. Studies on glyphosate-induced carcinogenicity in mouse skin: a proteomic approach. Journal of Proteomics 2010, 73:951-964.
29. Gilbert Y., Deghorain M., Wang L., Xu B., Pollheimer P.D., Gruber H.J., Errington J., Hallet B., Haulot X., Verbelen C., Hols P., Dufrêne Y.F. Single-molecule force spectroscopy and imaging of the vancomycin/d-Ala-d-Ala interaction. Nano Letters 2007, 7:796-801.
30. Gunning A.P., Chambers S., Pin C., Man A.L., Morris V.J., et al. Mapping specific adhesive interactions on living human intestinal epithelial cells with atomic force microscopy. FASEB J. 2008, 22:2331-2339.
31. Hamon L., Pastré D., Dupaigne P., Breton C.L., Cam E.L., et al. High-resolution AFM imaging of single-stranded DNA-binding (SSB) protein-DNA complexes. Nucleic Acids Research 2007, 35:e58.
32. Hertz J. Für reine und angewandte Mathematik 1881, 92:156-171.
33. Hsieh C.H., Lin Y.H., Lin S., Tsai-Wu J.J., Herbert Wu C.H., et al. Surface ultrastructure and mechanical property of human chondrocyte revealed by atomic force microscopy. Osteoarthritis and Cartilage 2008, 16:480-488.
34. Kimura S., Warabi E., Yanagawa T., Ma D., Itoh K., et al. Essential role of Nrf2 in keratinocyte protection from UVA by quercetin. Biochemical and Biophysical Research Communications 2009, 387:109-114.
35. Kook D., Wolf A.H., Yu A.L., Neubauer A.S., Priglinger S.G., et al. The protective effect of quercetin against oxidative stress in the human RPE in vitro. Investigative Ophthalmology & Visual Science 2008, 49:1712-1720.
36. Kumar S., Weaver V. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer and Metastasis Reviews 2009, 28:113-127.
37. Laurent V.M., Kasas S., Yersin A., Schäffer T.E., Catsicas S., et al. Gradient of rigidity in the lamellipodia of migrating cells revealed by atomic force microscopy. Biophysical Journal 2005, 89:667-675.
38. Li F., Redick S.D., Erickson H.P., Moy V.T. Force measurements of the α5β1 integrin-fibronectin interaction. Biophysical Journal 2003, 84:1252-1262.
39. Li Q.S., Lee G.Y.H., Ong C.N., Lim C.T. AFM indentation study of breast cancer cells. Biochemical and Biophysical Research Communications 2008, 374:609-613.
40. Lieber S.C., Aubry N., Pain J., Diaz G., Kim S.-J., et al. Aging increases stiffness of cardiac myocytes measured by atomic force microscopy nanoindentation. American Journal of Physiology - Heart and Circulatory Physiology 2004, 287:H645-H651.
41. Lulevich V., Yang H.-y., Rivkah Isseroff R., Liu G.-y. Single cell mechanics of keratinocyte cells. Ultramicroscopy 2010, 110:1435-1442.
42. Magin T.M., Vijayaraj P., Leube R.E. Structural and regulatory functions of keratins. Experimental Cell Research 2007, 313:2021-2032.
43. Marc J., Mulner-Lorillon O., Boulben S., Hureau D., Durand G., et al. Pesticide roundup provokes cell division dysfunction at the level of CDK1/cyclin B activation. Chemical Research in Toxicology 2002, 15:326-331.
44. Müller D.J., Dufrene Y.F. Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nature Nanotechnology 2008, 3:261-269.
45. Nagami H., Nishigaki Y., Matsushima S., Matsushita T., Asanuma S., et al. Hospital-based survey of pesticide poisoning in Japan, 1998-2002 2005, Hamilton Hardy, Attleboro, MA, Etats Unis.
46. Nielsen J., Nielsen F., Sørensen J. Defense against dermal exposures is only skin deep: significantly increased penetration through slightly damaged skin. Archives of Dermatological Research 2007, 299:423-431.
47. Ossola B., Kääriäinen T.M., Raasmaja A., Männistö P.T. Time-dependent protective and harmful effects of quercetin on 6-OHDA-induced toxicity in neuronal SH-SY5Y cells. Toxicology 2008, 250:1-8.
48. Paganelli A., Gnazzo V., Acosta H., López S.L., Carrasco A.s.E. Glyphosate-based herbicides produce teratogenic effects on vertebrates by impairing retinoic acid signaling. Chemical Research in Toxicology 2010, 23:1586-1595.
49. Pellegrin S., Mellor H. Actin stress fibres. Journal of Cell Science 2007, 120:3491-3499.
50. Pellegrino M., Furmaniak-Kazmierczak E., LeBlanc J.C., Cho T., Cao K., et al. The apolipoprotein(a) component of lipoprotein(a) stimulates actin stress fiber formation and loss of cell-cell contact in cultured endothelial cells. Journal of Biological Chemistry 2004, 279:6526-6533.
51. Penagos H., Ruepert C., Partanen T., Wesseling C. Pesticide patch test series for the assessment of allergic contact dermatitis among banana plantation workers in panama. Dermatitis 2004, 15(3):137-145.
52. Pittenger, B., Erina, N., Su, C., 2010. Quantitative Mechanical Property Mapping at the Nanoscale with PeakForce QNM. Bruker Application Note #128.
53. Pletikapic, G., Berquand, A., Misic T., Svetlicic, V., in press. Quantitative nanochemical mapping of marine diatom in sea water using PeakForce Tapping AFM. Journal of Phycology.
54. Prasad S.S., Madhulika S., Yogeshwer S. Clastogenic effects of glyphosate in bone marrow cells of Swiss albino mice. Journal of Toxicology 2009.
55. Proksch E., Brandner J.M., Jensen J.-M. The skin: an indispensable barrier. Experimental Dermatology 2008, 17:1063-1072.
56. Reich A., Lehmann B., Meurer M., Muller D.J. Structural alterations provoked by narrow-band ultraviolet B in immortalized keratinocytes: assessment by atomic force microscopy. Experimental Dermatology 2007, 16:1007-1015.
57. Reich A., Meurer M., Viehweg A., Muller D.J. Narrow-band UVB-induced externalization of selected nuclear antigens in keratinocytes: implications for Lupus Erythematosus pathogenesis†. Photochemistry and Photobiology 2009, 85:1-7.
58. Rico F., Chu C., Moy V.T. Force-clamp measurements of receptor-ligand interactions. Methods in Molecular Biology 2011, 736:331-353.
59. Rotsch C., Radmacher M. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophysical Journal 2000, 78:520-535.
60. Shih C.M., Lin H., Liang Y.C., Lee W.S., Bi W.F., et al. Concentration-dependent differential effects of quercetin on rat aortic smooth muscle cells. European Journal of Pharmacology 2004, 496:41-48.
61. Sneddon I.N. The relation between load and penetration in the axisymmetric bossiness problem for a punch of arbitrary profile. International Journal of Engineering Science 1965, 3:47-57.
62. Starodubtseva M.N. Mechanical properties of cells and ageing. Ageing Research Reviews 2011, 10:16-25.
63. Stewart M.P., Toyoda Y., Hyman A.A., Muller D.J. Force probing cell shape changes to molecular resolution. Trends in Biochemical Sciences 2011, 36:444-450.
64. Stolz M., Gottardi R., Raiteri R., Miot S., Martin I., Imer R., Staufer U., Raducanu A., Duggelin M., Baschong W., Daniels A.U., Friederich N.F., Aszodi A., Aebi U. Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy. Nature Nanotechnology 2009, 4:186-192.
65. Suresh S. Biomechanics and biophysics of cancer cells. Acta Biomaterialia 2007, 3:413-438.
66. Suresh S., Spatz J., Mills J.P., Micoulet A., Dao M., et al. Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. Acta Biomaterialia 2005, 1:15-30.
67. Touhami A., Nysten B., Dufrêne Y.F. Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy. Langmuir 2003, 19:4539-4543.
68. Trickey W.R., Baaijens F.P.T., Laursen T.A., Alexopoulos L.G., Guilak F. Determination of the Poisson's ratio of the cell: recovery properties of chondrocytes after release from complete micropipette aspiration. Journal of Biomechanics 2006, 39:78-87.
69. 2 induced early cell apoptosis and mitochondrial damage to normal human kératinocytes. Chinese Medical Journal 2010, 123(5):532-536.
70. Williams G.M., Kroes R., Munro I.C. Safety evaluation and risk assessment of the herbicide roundup and its active ingredient, glyphosate, for humans. Regulatory Toxicology and Pharmacology 2000, 31:117-165.
71. Zhong Q., Inniss D., Kjoller K., Elings V.B. Fractured polymer/silica fiber surface studied by tapping mode atomic force microscopy. Surface Science Letters 1993, 290:L688-L692.