Direct determination of oligomeric organization of integral membrane proteins and lipids from intact customizable bilayer

Aniruddha Panda; Fabian Giska; Anna L. Duncan; Alexander J. Welch; Caroline Brown; Rachel McAllister; Parameswaran Hariharan; Jean N.D. Goder; Jeff Coleman; Sathish Ramakrishnan; Frédéric Pincet; Lan Guan; Shyam Krishnakumar; James E. Rothman; Kallol Gupta

doi:10.1038/s41592-023-01864-5

Direct determination of oligomeric organization of integral membrane proteins and lipids from intact customizable bilayer

Aniruddha Panda, Fabian Giska, Anna L. Duncan, Alexander J. Welch, Caroline Brown, Rachel McAllister, Parameswaran Hariharan, Jean N.D. Goder, Jeff Coleman, Sathish Ramakrishnan, Frédéric Pincet, Lan Guan, Shyam Krishnakumar, James E. Rothman, Kallol Gupta^*

^*Corresponding author af dette arbejde

Institut for Kemi

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

18 Citationer (Scopus)

Abstract

Hierarchical organization of integral membrane proteins (IMP) and lipids at the membrane is essential for regulating myriad downstream signaling. A quantitative understanding of these processes requires both detections of oligomeric organization of IMPs and lipids directly from intact membranes and determination of key membrane components and properties that regulate them. Addressing this, we have developed a platform that enables native mass spectrometry (nMS) analysis of IMP–lipid complexes directly from intact and customizable lipid membranes. Both the lipid composition and membrane properties (such as curvature, tension, and fluidity) of these bilayers can be precisely customized to a target membrane. Subsequent direct nMS analysis of these intact proteolipid vesicles can yield the oligomeric states of the embedded IMPs, identify bound lipids, and determine the membrane properties that can regulate the observed IMP–lipid organization. Applying this method, we show how lipid binding regulates neurotransmitter release and how membrane composition regulates the functional oligomeric state of a transporter.

Originalsprog	Engelsk
Tidsskrift	Nature Methods
Vol/bind	20
Nummer	6
Sider (fra-til)	891-897
Antal sider	7
ISSN	1548-7091
DOI	https://doi.org/10.1038/s41592-023-01864-5
Status	Udgivet - jun. 2023

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10.1038/s41592-023-01864-5

https://pmc.ncbi.nlm.nih.gov/articles/PMC10932606/pdf/nihms-1972575.pdf

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Panda, A., Giska, F., Duncan, A. L., Welch, A. J., Brown, C., McAllister, R., Hariharan, P., Goder, J. N. D., Coleman, J., Ramakrishnan, S., Pincet, F., Guan, L., Krishnakumar, S., Rothman, J. E., & Gupta, K. (2023). Direct determination of oligomeric organization of integral membrane proteins and lipids from intact customizable bilayer. Nature Methods, 20(6), 891-897. https://doi.org/10.1038/s41592-023-01864-5

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title = "Direct determination of oligomeric organization of integral membrane proteins and lipids from intact customizable bilayer",

abstract = "Hierarchical organization of integral membrane proteins (IMP) and lipids at the membrane is essential for regulating myriad downstream signaling. A quantitative understanding of these processes requires both detections of oligomeric organization of IMPs and lipids directly from intact membranes and determination of key membrane components and properties that regulate them. Addressing this, we have developed a platform that enables native mass spectrometry (nMS) analysis of IMP–lipid complexes directly from intact and customizable lipid membranes. Both the lipid composition and membrane properties (such as curvature, tension, and fluidity) of these bilayers can be precisely customized to a target membrane. Subsequent direct nMS analysis of these intact proteolipid vesicles can yield the oligomeric states of the embedded IMPs, identify bound lipids, and determine the membrane properties that can regulate the observed IMP–lipid organization. Applying this method, we show how lipid binding regulates neurotransmitter release and how membrane composition regulates the functional oligomeric state of a transporter.",

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author = "Aniruddha Panda and Fabian Giska and Duncan, {Anna L.} and Welch, {Alexander J.} and Caroline Brown and Rachel McAllister and Parameswaran Hariharan and Goder, {Jean N.D.} and Jeff Coleman and Sathish Ramakrishnan and Fr{\'e}d{\'e}ric Pincet and Lan Guan and Shyam Krishnakumar and Rothman, {James E.} and Kallol Gupta",

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Panda, A, Giska, F, Duncan, AL, Welch, AJ, Brown, C, McAllister, R, Hariharan, P, Goder, JND, Coleman, J, Ramakrishnan, S, Pincet, F, Guan, L, Krishnakumar, S, Rothman, JE & Gupta, K 2023, 'Direct determination of oligomeric organization of integral membrane proteins and lipids from intact customizable bilayer', Nature Methods, bind 20, nr. 6, s. 891-897. https://doi.org/10.1038/s41592-023-01864-5

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AU - Brown, Caroline

AU - McAllister, Rachel

AU - Hariharan, Parameswaran

AU - Goder, Jean N.D.

AU - Coleman, Jeff

AU - Ramakrishnan, Sathish

AU - Pincet, Frédéric

AU - Guan, Lan

AU - Krishnakumar, Shyam

AU - Rothman, James E.

AU - Gupta, Kallol

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N2 - Hierarchical organization of integral membrane proteins (IMP) and lipids at the membrane is essential for regulating myriad downstream signaling. A quantitative understanding of these processes requires both detections of oligomeric organization of IMPs and lipids directly from intact membranes and determination of key membrane components and properties that regulate them. Addressing this, we have developed a platform that enables native mass spectrometry (nMS) analysis of IMP–lipid complexes directly from intact and customizable lipid membranes. Both the lipid composition and membrane properties (such as curvature, tension, and fluidity) of these bilayers can be precisely customized to a target membrane. Subsequent direct nMS analysis of these intact proteolipid vesicles can yield the oligomeric states of the embedded IMPs, identify bound lipids, and determine the membrane properties that can regulate the observed IMP–lipid organization. Applying this method, we show how lipid binding regulates neurotransmitter release and how membrane composition regulates the functional oligomeric state of a transporter.

AB - Hierarchical organization of integral membrane proteins (IMP) and lipids at the membrane is essential for regulating myriad downstream signaling. A quantitative understanding of these processes requires both detections of oligomeric organization of IMPs and lipids directly from intact membranes and determination of key membrane components and properties that regulate them. Addressing this, we have developed a platform that enables native mass spectrometry (nMS) analysis of IMP–lipid complexes directly from intact and customizable lipid membranes. Both the lipid composition and membrane properties (such as curvature, tension, and fluidity) of these bilayers can be precisely customized to a target membrane. Subsequent direct nMS analysis of these intact proteolipid vesicles can yield the oligomeric states of the embedded IMPs, identify bound lipids, and determine the membrane properties that can regulate the observed IMP–lipid organization. Applying this method, we show how lipid binding regulates neurotransmitter release and how membrane composition regulates the functional oligomeric state of a transporter.

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Direct determination of oligomeric organization of integral membrane proteins and lipids from intact customizable bilayer

Abstract

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