A conserved complex lipid signature marks human muscle aging and responds to short-term exercise

Georges E. Janssens; Marte Molenaars; Katharina Herzog; Lotte Grevendonk; Carlijn M. E. Remie; Martin A. T. Vervaart; Hyung L. Elfrink; Eric J. M. Wever; Bauke V. Schomakers; Simone W. Denis; Hans R. Waterham; Mia L. Pras-Raves; Michel van Weeghel; Antoine H. C. van Kampen; Alessandra Tammaro; Loes M. Butter; Sanne van der Rijt; Sandrine Florquin; Aldo Jongejan; Perry D. Moerland; Joris Hoeks; Patrick Schrauwen; Frederic M. Vaz; Riekelt H. Houtkooper

doi:10.1038/s43587-024-00595-2

A conserved complex lipid signature marks human muscle aging and responds to short-term exercise

Georges E. Janssens^*, Marte Molenaars, Katharina Herzog, Lotte Grevendonk, Carlijn M. E. Remie, Martin A. T. Vervaart, Hyung L. Elfrink, Eric J. M. Wever, Bauke V. Schomakers, Simone W. Denis, Hans R. Waterham, Mia L. Pras-Raves, Michel van Weeghel, Antoine H. C. van Kampen, Alessandra Tammaro, Loes M. Butter, Sanne van der Rijt, Sandrine Florquin, Aldo Jongejan, Perry D. MoerlandJoris Hoeks, Patrick Schrauwen, Frederic M. Vaz^*, Riekelt H. Houtkooper^*

^*Corresponding author for this work

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

Abstract

Studies in preclinical models suggest that complex lipids, such as phospholipids, play a role in the regulation of longevity. However, identification of universally conserved complex lipid changes that occur during aging, and how these respond to interventions, is lacking. Here, to comprehensively map how complex lipids change during aging, we profiled ten tissues in young versus aged mice using a lipidomics platform. Strikingly, from >1,200 unique lipids, we found a tissue-wide accumulation of bis(monoacylglycero)phosphate (BMP) during mouse aging. To investigate translational value, we assessed muscle tissue of young and older people, and found a similar marked BMP accumulation in the human aging lipidome. Furthermore, we found that a healthy-aging intervention consisting of moderate-to-vigorous exercise was able to lower BMP levels in postmenopausal female research participants. Our work implicates complex lipid biology as central to aging, identifying a conserved aging lipid signature of BMP accumulation that is modifiable upon a short-term healthy-aging intervention.

Original language	English
Number of pages	21
Journal	Nature aging
Issue number	5
DOIs	https://doi.org/10.1038/s43587-024-00595-2
Publication status	E-pub ahead of print - 1 Apr 2024

Keywords

MASS-SPECTROMETRY
BIS(MONOACYLGLYCERO)PHOSPHATE
CARDIOLIPIN
LONGEVITY
PHOSPHATIDYLGLYCEROL
PATHWAY
STORAGE

Access to Document

10.1038/s43587-024-00595-2

Cite this

Janssens, G. E., Molenaars, M., Herzog, K., Grevendonk, L., Remie, C. M. E., Vervaart, M. A. T., Elfrink, H. L., Wever, E. J. M., Schomakers, B. V., Denis, S. W., Waterham, H. R., Pras-Raves, M. L., van Weeghel, M., van Kampen, A. H. C., Tammaro, A., Butter, L. M., van der Rijt, S., Florquin, S., Jongejan, A., ... Houtkooper, R. H. (2024). A conserved complex lipid signature marks human muscle aging and responds to short-term exercise. Nature aging, (5). Advance online publication. https://doi.org/10.1038/s43587-024-00595-2

@article{3956786fc5e446b5a08592236ad46d4a,

title = "A conserved complex lipid signature marks human muscle aging and responds to short-term exercise",

abstract = "Studies in preclinical models suggest that complex lipids, such as phospholipids, play a role in the regulation of longevity. However, identification of universally conserved complex lipid changes that occur during aging, and how these respond to interventions, is lacking. Here, to comprehensively map how complex lipids change during aging, we profiled ten tissues in young versus aged mice using a lipidomics platform. Strikingly, from >1,200 unique lipids, we found a tissue-wide accumulation of bis(monoacylglycero)phosphate (BMP) during mouse aging. To investigate translational value, we assessed muscle tissue of young and older people, and found a similar marked BMP accumulation in the human aging lipidome. Furthermore, we found that a healthy-aging intervention consisting of moderate-to-vigorous exercise was able to lower BMP levels in postmenopausal female research participants. Our work implicates complex lipid biology as central to aging, identifying a conserved aging lipid signature of BMP accumulation that is modifiable upon a short-term healthy-aging intervention.",

keywords = "MASS-SPECTROMETRY, BIS(MONOACYLGLYCERO)PHOSPHATE, CARDIOLIPIN, LONGEVITY, PHOSPHATIDYLGLYCEROL, PATHWAY, STORAGE",

author = "Janssens, {Georges E.} and Marte Molenaars and Katharina Herzog and Lotte Grevendonk and Remie, {Carlijn M. E.} and Vervaart, {Martin A. T.} and Elfrink, {Hyung L.} and Wever, {Eric J. M.} and Schomakers, {Bauke V.} and Denis, {Simone W.} and Waterham, {Hans R.} and Pras-Raves, {Mia L.} and {van Weeghel}, Michel and {van Kampen}, {Antoine H. C.} and Alessandra Tammaro and Butter, {Loes M.} and {van der Rijt}, Sanne and Sandrine Florquin and Aldo Jongejan and Moerland, {Perry D.} and Joris Hoeks and Patrick Schrauwen and Vaz, {Frederic M.} and Houtkooper, {Riekelt H.}",

year = "2024",

month = apr,

day = "1",

doi = "10.1038/s43587-024-00595-2",

language = "English",

journal = "Nature aging",

issn = "2662-8465",

publisher = "Nature Publishing Group",

number = "5",

}

Janssens, GE, Molenaars, M, Herzog, K, Grevendonk, L, Remie, CME, Vervaart, MAT, Elfrink, HL, Wever, EJM, Schomakers, BV, Denis, SW, Waterham, HR, Pras-Raves, ML, van Weeghel, M, van Kampen, AHC, Tammaro, A, Butter, LM, van der Rijt, S, Florquin, S, Jongejan, A, Moerland, PD, Hoeks, J , Schrauwen, P, Vaz, FM & Houtkooper, RH 2024, 'A conserved complex lipid signature marks human muscle aging and responds to short-term exercise', Nature aging, no. 5. https://doi.org/10.1038/s43587-024-00595-2

TY - JOUR

T1 - A conserved complex lipid signature marks human muscle aging and responds to short-term exercise

AU - Janssens, Georges E.

AU - Molenaars, Marte

AU - Herzog, Katharina

AU - Grevendonk, Lotte

AU - Remie, Carlijn M. E.

AU - Vervaart, Martin A. T.

AU - Elfrink, Hyung L.

AU - Wever, Eric J. M.

AU - Schomakers, Bauke V.

AU - Denis, Simone W.

AU - Waterham, Hans R.

AU - Pras-Raves, Mia L.

AU - van Weeghel, Michel

AU - van Kampen, Antoine H. C.

AU - Tammaro, Alessandra

AU - Butter, Loes M.

AU - van der Rijt, Sanne

AU - Florquin, Sandrine

AU - Jongejan, Aldo

AU - Moerland, Perry D.

AU - Hoeks, Joris

AU - Schrauwen, Patrick

AU - Vaz, Frederic M.

AU - Houtkooper, Riekelt H.

PY - 2024/4/1

Y1 - 2024/4/1

N2 - Studies in preclinical models suggest that complex lipids, such as phospholipids, play a role in the regulation of longevity. However, identification of universally conserved complex lipid changes that occur during aging, and how these respond to interventions, is lacking. Here, to comprehensively map how complex lipids change during aging, we profiled ten tissues in young versus aged mice using a lipidomics platform. Strikingly, from >1,200 unique lipids, we found a tissue-wide accumulation of bis(monoacylglycero)phosphate (BMP) during mouse aging. To investigate translational value, we assessed muscle tissue of young and older people, and found a similar marked BMP accumulation in the human aging lipidome. Furthermore, we found that a healthy-aging intervention consisting of moderate-to-vigorous exercise was able to lower BMP levels in postmenopausal female research participants. Our work implicates complex lipid biology as central to aging, identifying a conserved aging lipid signature of BMP accumulation that is modifiable upon a short-term healthy-aging intervention.

AB - Studies in preclinical models suggest that complex lipids, such as phospholipids, play a role in the regulation of longevity. However, identification of universally conserved complex lipid changes that occur during aging, and how these respond to interventions, is lacking. Here, to comprehensively map how complex lipids change during aging, we profiled ten tissues in young versus aged mice using a lipidomics platform. Strikingly, from >1,200 unique lipids, we found a tissue-wide accumulation of bis(monoacylglycero)phosphate (BMP) during mouse aging. To investigate translational value, we assessed muscle tissue of young and older people, and found a similar marked BMP accumulation in the human aging lipidome. Furthermore, we found that a healthy-aging intervention consisting of moderate-to-vigorous exercise was able to lower BMP levels in postmenopausal female research participants. Our work implicates complex lipid biology as central to aging, identifying a conserved aging lipid signature of BMP accumulation that is modifiable upon a short-term healthy-aging intervention.

KW - MASS-SPECTROMETRY

KW - BIS(MONOACYLGLYCERO)PHOSPHATE

KW - CARDIOLIPIN

KW - LONGEVITY

KW - PHOSPHATIDYLGLYCEROL

KW - PATHWAY

KW - STORAGE

U2 - 10.1038/s43587-024-00595-2

DO - 10.1038/s43587-024-00595-2

M3 - Article

SN - 2662-8465

JO - Nature aging

JF - Nature aging

IS - 5

ER -

A conserved complex lipid signature marks human muscle aging and responds to short-term exercise

Abstract

Keywords

Access to Document

Fingerprint

Cite this