Loss of Phospholipid Membrane Integrity Induced by Two-Dimensional Nanomaterials

Ines Zucker; Jay Werber; Zachary S. Fishman; Sara M. Hashmi; Uri R. Gabinet; Xinglin Lu; Chinedum O. Osuji; Lisa D. Pfefferle; Menachem Elimelech

doi:10.1021/acs.estlett.7b00358

Loss of Phospholipid Membrane Integrity Induced by Two-Dimensional Nanomaterials

Ines Zucker, Jay Werber, Zachary S. Fishman, Sara M. Hashmi, Uri R. Gabinet, Xinglin Lu, Chinedum O. Osuji, Lisa D. Pfefferle, Menachem Elimelech

Chemistry (Twin Cities)

Research output: Contribution to journal › Article › peer-review

38 Scopus citations

Abstract

The interaction of two-dimensional (2D) nanomaterials with biological membranes has important implications for ecotoxicity and human health. In this study, we use a dye-leakage assay to quantitatively assess the disruption of a model phospholipid bilayer membrane (i.e., lipid vesicles) by five emerging 2D nanomaterials: graphene oxide (GO), reduced graphene oxide (rGO), molybdenum disulfide (MoS₂), copper oxide (CuO), and iron oxide (α-Fe₂O₃). Leakage of dye from the vesicle inner solution, which indicates loss of membrane integrity, was observed for GO, rGO, and MoS₂ nanosheets but not for CuO and α-Fe₂O₃, implying that 2D morphology by itself is not sufficient to cause loss of membrane integrity. Mixing GO and rGO with lipid vesicles induced aggregation, whereas enhanced stability (dispersion) was observed with MoS₂ nanosheets, suggesting different aggregation mechanisms for the 2D nanomaterials upon interaction with lipid bilayers. No loss of membrane integrity was observed under strong oxidative conditions, indicating that nanosheet-driven membrane disruption stemmed from a physical mechanism rather than chemical oxidation. For GO, the most disruptive nanomaterial, we show that the extent of membrane integrity loss was dependent on total surface area, not edge length, which is consistent with a lipid-extraction mechanism and inconsistent with a piercing mechanism.

Original language	English (US)
Pages (from-to)	404-409
Number of pages	6
Journal	Environmental Science and Technology Letters
Volume	4
Issue number	10
DOIs	https://doi.org/10.1021/acs.estlett.7b00358
State	Published - Oct 10 2017

Bibliographical note

Funding Information:
The authors acknowledge the support received from the National Science Foundation through the Engineering Recearch Center for Nanotechnology Enabled Water Treatment (ERC-1449500). We also acknowledge the YIBS Postdoctoral Fellowship and Tel Aviv University Presidential Postdoctoral Fellowship awarded to I.Z. Z.F. and L.P. acknowledge support from the Army Research Laboratory (QRO grant #64935, Agreement W911NF1410564). Facilities use was supported by the Facility for Light Scattering and YINQE with great help from Dr. Michael Rooks. The authors thank Gilad Kaufman, Camrynn Fausey, and Ben Zucker for their advice and help with data analysis.

Publisher Copyright:
© 2017 American Chemical Society.

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title = "Loss of Phospholipid Membrane Integrity Induced by Two-Dimensional Nanomaterials",

abstract = "The interaction of two-dimensional (2D) nanomaterials with biological membranes has important implications for ecotoxicity and human health. In this study, we use a dye-leakage assay to quantitatively assess the disruption of a model phospholipid bilayer membrane (i.e., lipid vesicles) by five emerging 2D nanomaterials: graphene oxide (GO), reduced graphene oxide (rGO), molybdenum disulfide (MoS2), copper oxide (CuO), and iron oxide (α-Fe2O3). Leakage of dye from the vesicle inner solution, which indicates loss of membrane integrity, was observed for GO, rGO, and MoS2 nanosheets but not for CuO and α-Fe2O3, implying that 2D morphology by itself is not sufficient to cause loss of membrane integrity. Mixing GO and rGO with lipid vesicles induced aggregation, whereas enhanced stability (dispersion) was observed with MoS2 nanosheets, suggesting different aggregation mechanisms for the 2D nanomaterials upon interaction with lipid bilayers. No loss of membrane integrity was observed under strong oxidative conditions, indicating that nanosheet-driven membrane disruption stemmed from a physical mechanism rather than chemical oxidation. For GO, the most disruptive nanomaterial, we show that the extent of membrane integrity loss was dependent on total surface area, not edge length, which is consistent with a lipid-extraction mechanism and inconsistent with a piercing mechanism.",

author = "Ines Zucker and Jay Werber and Fishman, {Zachary S.} and Hashmi, {Sara M.} and Gabinet, {Uri R.} and Xinglin Lu and Osuji, {Chinedum O.} and Pfefferle, {Lisa D.} and Menachem Elimelech",

note = "Funding Information: The authors acknowledge the support received from the National Science Foundation through the Engineering Recearch Center for Nanotechnology Enabled Water Treatment (ERC-1449500). We also acknowledge the YIBS Postdoctoral Fellowship and Tel Aviv University Presidential Postdoctoral Fellowship awarded to I.Z. Z.F. and L.P. acknowledge support from the Army Research Laboratory (QRO grant #64935, Agreement W911NF1410564). Facilities use was supported by the Facility for Light Scattering and YINQE with great help from Dr. Michael Rooks. The authors thank Gilad Kaufman, Camrynn Fausey, and Ben Zucker for their advice and help with data analysis. Publisher Copyright: {\textcopyright} 2017 American Chemical Society.",

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AU - Werber, Jay

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AU - Gabinet, Uri R.

AU - Lu, Xinglin

AU - Osuji, Chinedum O.

AU - Pfefferle, Lisa D.

AU - Elimelech, Menachem

N1 - Funding Information: The authors acknowledge the support received from the National Science Foundation through the Engineering Recearch Center for Nanotechnology Enabled Water Treatment (ERC-1449500). We also acknowledge the YIBS Postdoctoral Fellowship and Tel Aviv University Presidential Postdoctoral Fellowship awarded to I.Z. Z.F. and L.P. acknowledge support from the Army Research Laboratory (QRO grant #64935, Agreement W911NF1410564). Facilities use was supported by the Facility for Light Scattering and YINQE with great help from Dr. Michael Rooks. The authors thank Gilad Kaufman, Camrynn Fausey, and Ben Zucker for their advice and help with data analysis. Publisher Copyright: © 2017 American Chemical Society.

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N2 - The interaction of two-dimensional (2D) nanomaterials with biological membranes has important implications for ecotoxicity and human health. In this study, we use a dye-leakage assay to quantitatively assess the disruption of a model phospholipid bilayer membrane (i.e., lipid vesicles) by five emerging 2D nanomaterials: graphene oxide (GO), reduced graphene oxide (rGO), molybdenum disulfide (MoS2), copper oxide (CuO), and iron oxide (α-Fe2O3). Leakage of dye from the vesicle inner solution, which indicates loss of membrane integrity, was observed for GO, rGO, and MoS2 nanosheets but not for CuO and α-Fe2O3, implying that 2D morphology by itself is not sufficient to cause loss of membrane integrity. Mixing GO and rGO with lipid vesicles induced aggregation, whereas enhanced stability (dispersion) was observed with MoS2 nanosheets, suggesting different aggregation mechanisms for the 2D nanomaterials upon interaction with lipid bilayers. No loss of membrane integrity was observed under strong oxidative conditions, indicating that nanosheet-driven membrane disruption stemmed from a physical mechanism rather than chemical oxidation. For GO, the most disruptive nanomaterial, we show that the extent of membrane integrity loss was dependent on total surface area, not edge length, which is consistent with a lipid-extraction mechanism and inconsistent with a piercing mechanism.

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Loss of Phospholipid Membrane Integrity Induced by Two-Dimensional Nanomaterials

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