Interfacial reactions of ozone with surfactant protein B in a model lung surfactant system

Hugh I. Kim, Hyungjun Kim, Young Shik Shin, Luther W. Beegle, Seung Soon Jang, Evan L. Neidholdt, William A. Goddard, James R. Heath, Isik Kanik, J. L. Beauchamp

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

Oxidative stresses from irritants such as hydrogen peroxide and ozone (O3) can cause dysfunction of the pulmonary surfactant (PS) layer in the human lung, resulting in chronic diseases of the respiratory tract. For identification of structural changes of pulmonary surfactant protein B (SP-B) due to the heterogeneous reaction with O3, field-induced droplet ionization (FIDI) mass spectrometry has been utilized. FIDI is a soft ionization method in which ions are extracted from the surface of microliter-volume droplets. We report structurally specific oxidative changes of SP-B 1-25 (a shortened version of human SP-B) at the air-liquid interface. We also present studies of the interfacial oxidation of SP-B1-25 in a nonionizable 1-palmitoyl-2-oleoyl-sn-glycerol (POG) surfactant layer as a model PS system, where competitive oxidation of the two components is observed. Our results indicate that the heterogeneous reaction of SP-B1-25 at the interface is quite different from that in the solution phase. In comparison with the nearly complete homogeneous oxidation of SP-B1-25, only a subset of the amino acids known to react with ozone are oxidized by direct ozonolysis in the hydrophobic interfacial environment, both with and without the lipid surfactant layer. Combining these experimental observations with the results of molecular dynamics simulations provides an improved understanding of the interfacial structure and chemistry of a model lung surfactant system subjected to oxidative stress.

Original languageEnglish
Pages (from-to)2254-2263
Number of pages10
JournalJournal of the American Chemical Society
Volume132
Issue number7
DOIs
Publication statusPublished - 2010 Mar 3
Externally publishedYes

Fingerprint

Ozone
Surface chemistry
Surface-Active Agents
Surface active agents
Proteins
Lung
Ionization
Pulmonary Surfactants
Oxidative stress
Oxidation
Oxidative Stress
Pulmonary Surfactant-Associated Proteins
Irritants
Molecular Dynamics Simulation
Respiratory System
Hydrogen Peroxide
Mass spectrometry
Molecular dynamics
Mass Spectrometry
Chronic Disease

ASJC Scopus subject areas

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

Kim, H. I., Kim, H., Shin, Y. S., Beegle, L. W., Jang, S. S., Neidholdt, E. L., ... Beauchamp, J. L. (2010). Interfacial reactions of ozone with surfactant protein B in a model lung surfactant system. Journal of the American Chemical Society, 132(7), 2254-2263. https://doi.org/10.1021/ja908477w

Interfacial reactions of ozone with surfactant protein B in a model lung surfactant system. / Kim, Hugh I.; Kim, Hyungjun; Shin, Young Shik; Beegle, Luther W.; Jang, Seung Soon; Neidholdt, Evan L.; Goddard, William A.; Heath, James R.; Kanik, Isik; Beauchamp, J. L.

In: Journal of the American Chemical Society, Vol. 132, No. 7, 03.03.2010, p. 2254-2263.

Research output: Contribution to journalArticle

Kim, HI, Kim, H, Shin, YS, Beegle, LW, Jang, SS, Neidholdt, EL, Goddard, WA, Heath, JR, Kanik, I & Beauchamp, JL 2010, 'Interfacial reactions of ozone with surfactant protein B in a model lung surfactant system', Journal of the American Chemical Society, vol. 132, no. 7, pp. 2254-2263. https://doi.org/10.1021/ja908477w
Kim, Hugh I. ; Kim, Hyungjun ; Shin, Young Shik ; Beegle, Luther W. ; Jang, Seung Soon ; Neidholdt, Evan L. ; Goddard, William A. ; Heath, James R. ; Kanik, Isik ; Beauchamp, J. L. / Interfacial reactions of ozone with surfactant protein B in a model lung surfactant system. In: Journal of the American Chemical Society. 2010 ; Vol. 132, No. 7. pp. 2254-2263.
@article{c80c9a7c0a394f5ab5b4a287d09088f4,
title = "Interfacial reactions of ozone with surfactant protein B in a model lung surfactant system",
abstract = "Oxidative stresses from irritants such as hydrogen peroxide and ozone (O3) can cause dysfunction of the pulmonary surfactant (PS) layer in the human lung, resulting in chronic diseases of the respiratory tract. For identification of structural changes of pulmonary surfactant protein B (SP-B) due to the heterogeneous reaction with O3, field-induced droplet ionization (FIDI) mass spectrometry has been utilized. FIDI is a soft ionization method in which ions are extracted from the surface of microliter-volume droplets. We report structurally specific oxidative changes of SP-B 1-25 (a shortened version of human SP-B) at the air-liquid interface. We also present studies of the interfacial oxidation of SP-B1-25 in a nonionizable 1-palmitoyl-2-oleoyl-sn-glycerol (POG) surfactant layer as a model PS system, where competitive oxidation of the two components is observed. Our results indicate that the heterogeneous reaction of SP-B1-25 at the interface is quite different from that in the solution phase. In comparison with the nearly complete homogeneous oxidation of SP-B1-25, only a subset of the amino acids known to react with ozone are oxidized by direct ozonolysis in the hydrophobic interfacial environment, both with and without the lipid surfactant layer. Combining these experimental observations with the results of molecular dynamics simulations provides an improved understanding of the interfacial structure and chemistry of a model lung surfactant system subjected to oxidative stress.",
author = "Kim, {Hugh I.} and Hyungjun Kim and Shin, {Young Shik} and Beegle, {Luther W.} and Jang, {Seung Soon} and Neidholdt, {Evan L.} and Goddard, {William A.} and Heath, {James R.} and Isik Kanik and Beauchamp, {J. L.}",
year = "2010",
month = "3",
day = "3",
doi = "10.1021/ja908477w",
language = "English",
volume = "132",
pages = "2254--2263",
journal = "Journal of the American Chemical Society",
issn = "0002-7863",
publisher = "American Chemical Society",
number = "7",

}

TY - JOUR

T1 - Interfacial reactions of ozone with surfactant protein B in a model lung surfactant system

AU - Kim, Hugh I.

AU - Kim, Hyungjun

AU - Shin, Young Shik

AU - Beegle, Luther W.

AU - Jang, Seung Soon

AU - Neidholdt, Evan L.

AU - Goddard, William A.

AU - Heath, James R.

AU - Kanik, Isik

AU - Beauchamp, J. L.

PY - 2010/3/3

Y1 - 2010/3/3

N2 - Oxidative stresses from irritants such as hydrogen peroxide and ozone (O3) can cause dysfunction of the pulmonary surfactant (PS) layer in the human lung, resulting in chronic diseases of the respiratory tract. For identification of structural changes of pulmonary surfactant protein B (SP-B) due to the heterogeneous reaction with O3, field-induced droplet ionization (FIDI) mass spectrometry has been utilized. FIDI is a soft ionization method in which ions are extracted from the surface of microliter-volume droplets. We report structurally specific oxidative changes of SP-B 1-25 (a shortened version of human SP-B) at the air-liquid interface. We also present studies of the interfacial oxidation of SP-B1-25 in a nonionizable 1-palmitoyl-2-oleoyl-sn-glycerol (POG) surfactant layer as a model PS system, where competitive oxidation of the two components is observed. Our results indicate that the heterogeneous reaction of SP-B1-25 at the interface is quite different from that in the solution phase. In comparison with the nearly complete homogeneous oxidation of SP-B1-25, only a subset of the amino acids known to react with ozone are oxidized by direct ozonolysis in the hydrophobic interfacial environment, both with and without the lipid surfactant layer. Combining these experimental observations with the results of molecular dynamics simulations provides an improved understanding of the interfacial structure and chemistry of a model lung surfactant system subjected to oxidative stress.

AB - Oxidative stresses from irritants such as hydrogen peroxide and ozone (O3) can cause dysfunction of the pulmonary surfactant (PS) layer in the human lung, resulting in chronic diseases of the respiratory tract. For identification of structural changes of pulmonary surfactant protein B (SP-B) due to the heterogeneous reaction with O3, field-induced droplet ionization (FIDI) mass spectrometry has been utilized. FIDI is a soft ionization method in which ions are extracted from the surface of microliter-volume droplets. We report structurally specific oxidative changes of SP-B 1-25 (a shortened version of human SP-B) at the air-liquid interface. We also present studies of the interfacial oxidation of SP-B1-25 in a nonionizable 1-palmitoyl-2-oleoyl-sn-glycerol (POG) surfactant layer as a model PS system, where competitive oxidation of the two components is observed. Our results indicate that the heterogeneous reaction of SP-B1-25 at the interface is quite different from that in the solution phase. In comparison with the nearly complete homogeneous oxidation of SP-B1-25, only a subset of the amino acids known to react with ozone are oxidized by direct ozonolysis in the hydrophobic interfacial environment, both with and without the lipid surfactant layer. Combining these experimental observations with the results of molecular dynamics simulations provides an improved understanding of the interfacial structure and chemistry of a model lung surfactant system subjected to oxidative stress.

UR - http://www.scopus.com/inward/record.url?scp=77749242844&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77749242844&partnerID=8YFLogxK

U2 - 10.1021/ja908477w

DO - 10.1021/ja908477w

M3 - Article

VL - 132

SP - 2254

EP - 2263

JO - Journal of the American Chemical Society

JF - Journal of the American Chemical Society

SN - 0002-7863

IS - 7

ER -