Combined Quantitative (Phospho)proteomics and Mass Spectrometry Imaging Reveal Temporal and Spatial Protein Changes in Human Intestinal Ischemia–Reperfusion (2024)

Kip, A. M., Valverde, J. M., Altelaar, M., Heeren, R. M. A., Hundscheid, I. H. R., Dejong, C. H. C., Olde Damink, S. W. M., Balluff, B., & Lenaerts, K. (2022). Combined Quantitative (Phospho)proteomics and Mass Spectrometry Imaging Reveal Temporal and Spatial Protein Changes in Human Intestinal Ischemia–Reperfusion. Journal of Proteome Research, 21(1), 49-66. https://doi.org/10.1021/acs.jproteome.1c00447

Kip, Anna M. ; Valverde, Juan Manuel ; Altelaar, Maarten et al. / Combined Quantitative (Phospho)proteomics and Mass Spectrometry Imaging Reveal Temporal and Spatial Protein Changes in Human Intestinal Ischemia–Reperfusion. In: Journal of Proteome Research. 2022 ; Vol. 21, No. 1. pp. 49-66.

@article{feb63612a0f94edfb604f6165d0934c4,

title = "Combined Quantitative (Phospho)proteomics and Mass Spectrometry Imaging Reveal Temporal and Spatial Protein Changes in Human Intestinal Ischemia–Reperfusion",

abstract = "Intestinal ischemia–reperfusion (IR) injury is a severe clinical condition, and unraveling its pathophysiology is crucial to improve therapeutic strategies and reduce the high morbidity and mortality rates. Here, we studied the dynamic proteome and phosphoproteome in the human intestine during ischemia and reperfusion, using liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis to gain quantitative information of thousands of proteins and phosphorylation sites, as well as mass spectrometry imaging (MSI) to obtain spatial information. We identified a significant decrease in abundance of proteins related to intestinal absorption, microvillus, and cell junction, whereas proteins involved in innate immunity, in particular the complement cascade, and extracellular matrix organization increased in abundance after IR. Differentially phosphorylated proteins were involved in RNA splicing events and cytoskeletal and cell junction organization. In addition, our analysis points to mitogen-activated protein kinase (MAPK) and cyclin-dependent kinase (CDK) families to be active kinases during IR. Finally, matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF) MSI presented peptide alterations in abundance and distribution, which resulted, in combination with Fourier-transform ion cyclotron resonance (FTICR) MSI and LC-MS/MS, in the annotation of proteins related to RNA splicing, the complement cascade, and extracellular matrix organization. This study expanded our understanding of the molecular changes that occur during IR in the human intestine and highlights the value of the complementary use of different MS-based methodologies.",

keywords = "human intestinal ischemia−reperfusion, mass spectrometry imaging, phosphoproteomics, proteomics, spatiotemporal data",

author = "Kip, {Anna M.} and Valverde, {Juan Manuel} and Maarten Altelaar and Heeren, {Ron M.A.} and Hundscheid, {Inca H.R.} and Dejong, {Cornelis H.C.} and {Olde Damink}, {Steven W.M.} and Benjamin Balluff and Kaatje Lenaerts",

note = "Funding Information: This work was funded by NUTRIM, Maastricht University (NUTRIM Graduate Program grant to A.M.K.), NWO (Aspasia grant 015.010.046 to K.L.), NWO (project 184.034.019), and was part of the Netherlands X-omics Initiative. J.M.V. was supported by scholarships from the Ministry of Science and Technology of Costa Rica (MICITT) and the University of Costa Rica (UCR). We thank the surgical team of Maastricht UMC+ for their excellent surgical assistance. Table of Contents graphic was created with BioRender.com. Publisher Copyright: {\textcopyright} 2021 The Authors. Published by American Chemical Society",

year = "2022",

month = jan,

day = "7",

doi = "10.1021/acs.jproteome.1c00447",

language = "English",

volume = "21",

pages = "49--66",

journal = "Journal of Proteome Research",

issn = "1535-3893",

publisher = "American Chemical Society",

number = "1",

}

Kip, AM, Valverde, JM, Altelaar, M, Heeren, RMA, Hundscheid, IHR, Dejong, CHC, Olde Damink, SWM, Balluff, B & Lenaerts, K 2022, 'Combined Quantitative (Phospho)proteomics and Mass Spectrometry Imaging Reveal Temporal and Spatial Protein Changes in Human Intestinal Ischemia–Reperfusion', Journal of Proteome Research, vol. 21, no. 1, pp. 49-66. https://doi.org/10.1021/acs.jproteome.1c00447

Combined Quantitative (Phospho)proteomics and Mass Spectrometry Imaging Reveal Temporal and Spatial Protein Changes in Human Intestinal Ischemia–Reperfusion. / Kip, Anna M.; Valverde, Juan Manuel; Altelaar, Maarten et al.
In: Journal of Proteome Research, Vol. 21, No. 1, 07.01.2022, p. 49-66.

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

TY - JOUR

T1 - Combined Quantitative (Phospho)proteomics and Mass Spectrometry Imaging Reveal Temporal and Spatial Protein Changes in Human Intestinal Ischemia–Reperfusion

AU - Kip, Anna M.

AU - Valverde, Juan Manuel

AU - Altelaar, Maarten

AU - Heeren, Ron M.A.

AU - Hundscheid, Inca H.R.

AU - Dejong, Cornelis H.C.

AU - Olde Damink, Steven W.M.

AU - Balluff, Benjamin

AU - Lenaerts, Kaatje

N1 - Funding Information:This work was funded by NUTRIM, Maastricht University (NUTRIM Graduate Program grant to A.M.K.), NWO (Aspasia grant 015.010.046 to K.L.), NWO (project 184.034.019), and was part of the Netherlands X-omics Initiative. J.M.V. was supported by scholarships from the Ministry of Science and Technology of Costa Rica (MICITT) and the University of Costa Rica (UCR). We thank the surgical team of Maastricht UMC+ for their excellent surgical assistance. Table of Contents graphic was created with BioRender.com.Publisher Copyright:© 2021 The Authors. Published by American Chemical Society

PY - 2022/1/7

Y1 - 2022/1/7

N2 - Intestinal ischemia–reperfusion (IR) injury is a severe clinical condition, and unraveling its pathophysiology is crucial to improve therapeutic strategies and reduce the high morbidity and mortality rates. Here, we studied the dynamic proteome and phosphoproteome in the human intestine during ischemia and reperfusion, using liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis to gain quantitative information of thousands of proteins and phosphorylation sites, as well as mass spectrometry imaging (MSI) to obtain spatial information. We identified a significant decrease in abundance of proteins related to intestinal absorption, microvillus, and cell junction, whereas proteins involved in innate immunity, in particular the complement cascade, and extracellular matrix organization increased in abundance after IR. Differentially phosphorylated proteins were involved in RNA splicing events and cytoskeletal and cell junction organization. In addition, our analysis points to mitogen-activated protein kinase (MAPK) and cyclin-dependent kinase (CDK) families to be active kinases during IR. Finally, matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF) MSI presented peptide alterations in abundance and distribution, which resulted, in combination with Fourier-transform ion cyclotron resonance (FTICR) MSI and LC-MS/MS, in the annotation of proteins related to RNA splicing, the complement cascade, and extracellular matrix organization. This study expanded our understanding of the molecular changes that occur during IR in the human intestine and highlights the value of the complementary use of different MS-based methodologies.

AB - Intestinal ischemia–reperfusion (IR) injury is a severe clinical condition, and unraveling its pathophysiology is crucial to improve therapeutic strategies and reduce the high morbidity and mortality rates. Here, we studied the dynamic proteome and phosphoproteome in the human intestine during ischemia and reperfusion, using liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis to gain quantitative information of thousands of proteins and phosphorylation sites, as well as mass spectrometry imaging (MSI) to obtain spatial information. We identified a significant decrease in abundance of proteins related to intestinal absorption, microvillus, and cell junction, whereas proteins involved in innate immunity, in particular the complement cascade, and extracellular matrix organization increased in abundance after IR. Differentially phosphorylated proteins were involved in RNA splicing events and cytoskeletal and cell junction organization. In addition, our analysis points to mitogen-activated protein kinase (MAPK) and cyclin-dependent kinase (CDK) families to be active kinases during IR. Finally, matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF) MSI presented peptide alterations in abundance and distribution, which resulted, in combination with Fourier-transform ion cyclotron resonance (FTICR) MSI and LC-MS/MS, in the annotation of proteins related to RNA splicing, the complement cascade, and extracellular matrix organization. This study expanded our understanding of the molecular changes that occur during IR in the human intestine and highlights the value of the complementary use of different MS-based methodologies.

KW - human intestinal ischemia−reperfusion

KW - mass spectrometry imaging

KW - phosphoproteomics

KW - proteomics

KW - spatiotemporal data

UR - http://www.scopus.com/inward/record.url?scp=85121258952&partnerID=8YFLogxK

U2 - 10.1021/acs.jproteome.1c00447

DO - 10.1021/acs.jproteome.1c00447

M3 - Article

C2 - 34874173

AN - SCOPUS:85121258952

SN - 1535-3893

VL - 21

SP - 49

EP - 66

JO - Journal of Proteome Research

JF - Journal of Proteome Research

IS - 1

ER -

Kip AM, Valverde JM, Altelaar M, Heeren RMA, Hundscheid IHR, Dejong CHC et al. Combined Quantitative (Phospho)proteomics and Mass Spectrometry Imaging Reveal Temporal and Spatial Protein Changes in Human Intestinal Ischemia–Reperfusion. Journal of Proteome Research. 2022 Jan 7;21(1):49-66. doi: 10.1021/acs.jproteome.1c00447