Cationic nanoparticles induce nanoscale disruption in living cell plasma membranes

Jiumei Chen, Jessica A. Hessler, Krishna Putchakayala, Brian K. Panama, Damian P. Khan, Seungpyo Hong, Douglas G. Mullen, Stassi C. DiMaggio, Abhigyan Som, Gregory N. Tew, Anatoli N. Lopatin, James R. Baker, Mark M Banaszak Holl, Bradford G. Orr

Research output: Contribution to journalArticle

152 Citations (Scopus)

Abstract

It has long been recognized that cationic nanoparticles induce cell membrane permeability. Recently, it has been found that cationic nanoparticles induce the formation and/or growth of nanoscale holes in supported lipid bilayers. In this paper, we show that noncytotoxic concentrations of cationic nanoparticles induce 30-2000 pA currents in 293A (human embryonic kidney) and KB (human epidermoid carcinoma) cells, consistent with a nanoscale defect such as a single hole or group of holes in the cell membrane ranging from 1 to 350 nm2 in total area. Other forms of nanoscale defects, including the nanoparticle porating agents adsorbing onto or intercalating into the lipid bilayer, are also consistent; although the size of the defect must increase to account for any reduction in ion conduction, as compared to a water channel. An individual defect forming event takes 1-100 ms, while membrane resealing may occur over tens of seconds. Patch-clamp data provide direct evidence for the formation of nanoscale defects in living cell membranes. The cationic polymer data are compared and contrasted with patch-clamp data obtained for an amphiphilic phenylene ethynylene antimicrobial oligomer (AMO-3), a small molecule that is proposed to make well-defined 3.4 nm holes in lipid bilayers. Here, we observe data that are consistent with AMO-3 making ∼ 3 nm holes in living cell membranes.

Original languageEnglish
Pages (from-to)11179-11185
Number of pages7
JournalJournal of Physical Chemistry B
Volume113
Issue number32
DOIs
Publication statusPublished - 2009 Aug 13

Fingerprint

Cell membranes
Lipid bilayers
Nanoparticles
membranes
nanoparticles
Defects
defects
lipids
clamps
Clamping devices
Aquaporins
kidneys
oligomers
Oligomers
permeability
Polymers
cancer
Ions
Membranes
conduction

All Science Journal Classification (ASJC) codes

  • Physical and Theoretical Chemistry
  • Materials Chemistry
  • Surfaces, Coatings and Films

Cite this

Chen, J., Hessler, J. A., Putchakayala, K., Panama, B. K., Khan, D. P., Hong, S., ... Orr, B. G. (2009). Cationic nanoparticles induce nanoscale disruption in living cell plasma membranes. Journal of Physical Chemistry B, 113(32), 11179-11185. https://doi.org/10.1021/jp9033936
Chen, Jiumei ; Hessler, Jessica A. ; Putchakayala, Krishna ; Panama, Brian K. ; Khan, Damian P. ; Hong, Seungpyo ; Mullen, Douglas G. ; DiMaggio, Stassi C. ; Som, Abhigyan ; Tew, Gregory N. ; Lopatin, Anatoli N. ; Baker, James R. ; Holl, Mark M Banaszak ; Orr, Bradford G. / Cationic nanoparticles induce nanoscale disruption in living cell plasma membranes. In: Journal of Physical Chemistry B. 2009 ; Vol. 113, No. 32. pp. 11179-11185.
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Chen, J, Hessler, JA, Putchakayala, K, Panama, BK, Khan, DP, Hong, S, Mullen, DG, DiMaggio, SC, Som, A, Tew, GN, Lopatin, AN, Baker, JR, Holl, MMB & Orr, BG 2009, 'Cationic nanoparticles induce nanoscale disruption in living cell plasma membranes', Journal of Physical Chemistry B, vol. 113, no. 32, pp. 11179-11185. https://doi.org/10.1021/jp9033936

Cationic nanoparticles induce nanoscale disruption in living cell plasma membranes. / Chen, Jiumei; Hessler, Jessica A.; Putchakayala, Krishna; Panama, Brian K.; Khan, Damian P.; Hong, Seungpyo; Mullen, Douglas G.; DiMaggio, Stassi C.; Som, Abhigyan; Tew, Gregory N.; Lopatin, Anatoli N.; Baker, James R.; Holl, Mark M Banaszak; Orr, Bradford G.

In: Journal of Physical Chemistry B, Vol. 113, No. 32, 13.08.2009, p. 11179-11185.

Research output: Contribution to journalArticle

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T1 - Cationic nanoparticles induce nanoscale disruption in living cell plasma membranes

AU - Chen, Jiumei

AU - Hessler, Jessica A.

AU - Putchakayala, Krishna

AU - Panama, Brian K.

AU - Khan, Damian P.

AU - Hong, Seungpyo

AU - Mullen, Douglas G.

AU - DiMaggio, Stassi C.

AU - Som, Abhigyan

AU - Tew, Gregory N.

AU - Lopatin, Anatoli N.

AU - Baker, James R.

AU - Holl, Mark M Banaszak

AU - Orr, Bradford G.

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N2 - It has long been recognized that cationic nanoparticles induce cell membrane permeability. Recently, it has been found that cationic nanoparticles induce the formation and/or growth of nanoscale holes in supported lipid bilayers. In this paper, we show that noncytotoxic concentrations of cationic nanoparticles induce 30-2000 pA currents in 293A (human embryonic kidney) and KB (human epidermoid carcinoma) cells, consistent with a nanoscale defect such as a single hole or group of holes in the cell membrane ranging from 1 to 350 nm2 in total area. Other forms of nanoscale defects, including the nanoparticle porating agents adsorbing onto or intercalating into the lipid bilayer, are also consistent; although the size of the defect must increase to account for any reduction in ion conduction, as compared to a water channel. An individual defect forming event takes 1-100 ms, while membrane resealing may occur over tens of seconds. Patch-clamp data provide direct evidence for the formation of nanoscale defects in living cell membranes. The cationic polymer data are compared and contrasted with patch-clamp data obtained for an amphiphilic phenylene ethynylene antimicrobial oligomer (AMO-3), a small molecule that is proposed to make well-defined 3.4 nm holes in lipid bilayers. Here, we observe data that are consistent with AMO-3 making ∼ 3 nm holes in living cell membranes.

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