Circadian organization of lipid landscape is perturbed in type 2 diabetic patients

Flore Sinturel; Simona Chera; Marie-Claude Brulhart-Meynet; Jonathan Paz Montoya; Dirk Jan Stenvers; Peter H. Bisschop; Andries Kalsbeek; Idris Guessous; François R. Jornayvaz; Jacques Philippe; Steven A. Brown; Giovanni D'Angelo; Howard Riezman; Charna Dibner

doi:https://doi.org/10.1016/j.xcrm.2023.101299

Circadian organization of lipid landscape is perturbed in type 2 diabetic patients

Flore Sinturel, Simona Chera, Marie-Claude Brulhart-Meynet, Jonathan Paz Montoya, Dirk Jan Stenvers, Peter H. Bisschop, Andries Kalsbeek, Idris Guessous, François R. Jornayvaz, Jacques Philippe, Steven A. Brown, Giovanni D'Angelo, Howard Riezman, Charna Dibner

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

Abstract

Lipid homeostasis in humans follows a diurnal pattern in muscle and pancreatic islets, altered upon metabolic dysregulation. We employ tandem and liquid-chromatography mass spectrometry to investigate daily regulation of lipid metabolism in subcutaneous white adipose tissue (SAT) and serum of type 2 diabetic (T2D) and non-diabetic (ND) human volunteers (n = 12). Around 8% of ≈440 lipid metabolites exhibit diurnal rhythmicity in serum and SAT from ND and T2D subjects. The spectrum of rhythmic lipids differs between ND and T2D individuals, with the most substantial changes observed early morning, as confirmed by lipidomics in an independent cohort of ND and T2D subjects (n = 32) conducted at a single morning time point. Strikingly, metabolites identified as daily rhythmic in both serum and SAT from T2D subjects exhibit phase differences. Our study reveals massive temporal and tissue-specific alterations of human lipid homeostasis in T2D, providing essential clues for the development of lipid biomarkers in a temporal manner.

Original language	English
Article number	101299
Journal	Cell Reports Medicine
Volume	4
Issue number	12
DOIs	https://doi.org/10.1016/j.xcrm.2023.101299
Publication status	Published - 19 Dec 2023

Keywords

1-deoxyceramides
DAGs
TAGs
glycerophosphopholipids
human circadian system
lipidomics
serum
sphingolipids
subcutaneous white adipose tissue
type 2 diabetes

Access to Document

https://doi.org/10.1016/j.xcrm.2023.101299

Cite this

Sinturel, F., Chera, S., Brulhart-Meynet, M.-C., Montoya, J. P., Stenvers, D. J., Bisschop, P. H., Kalsbeek, A., Guessous, I., Jornayvaz, F. R., Philippe, J., Brown, S. A., D'Angelo, G., Riezman, H., & Dibner, C. (2023). Circadian organization of lipid landscape is perturbed in type 2 diabetic patients. Cell Reports Medicine, 4(12), Article 101299. https://doi.org/10.1016/j.xcrm.2023.101299

@article{5692f9ad870a434aa283d4f7662eddad,

title = "Circadian organization of lipid landscape is perturbed in type 2 diabetic patients",

abstract = "Lipid homeostasis in humans follows a diurnal pattern in muscle and pancreatic islets, altered upon metabolic dysregulation. We employ tandem and liquid-chromatography mass spectrometry to investigate daily regulation of lipid metabolism in subcutaneous white adipose tissue (SAT) and serum of type 2 diabetic (T2D) and non-diabetic (ND) human volunteers (n = 12). Around 8% of ≈440 lipid metabolites exhibit diurnal rhythmicity in serum and SAT from ND and T2D subjects. The spectrum of rhythmic lipids differs between ND and T2D individuals, with the most substantial changes observed early morning, as confirmed by lipidomics in an independent cohort of ND and T2D subjects (n = 32) conducted at a single morning time point. Strikingly, metabolites identified as daily rhythmic in both serum and SAT from T2D subjects exhibit phase differences. Our study reveals massive temporal and tissue-specific alterations of human lipid homeostasis in T2D, providing essential clues for the development of lipid biomarkers in a temporal manner.",

keywords = "1-deoxyceramides, DAGs, TAGs, glycerophosphopholipids, human circadian system, lipidomics, serum, sphingolipids, subcutaneous white adipose tissue, type 2 diabetes",

author = "Flore Sinturel and Simona Chera and Marie-Claude Brulhart-Meynet and Montoya, {Jonathan Paz} and Stenvers, {Dirk Jan} and Bisschop, {Peter H.} and Andries Kalsbeek and Idris Guessous and Jornayvaz, {Fran{\c c}ois R.} and Jacques Philippe and Brown, {Steven A.} and Giovanni D'Angelo and Howard Riezman and Charna Dibner",

note = "Funding Information: This work was supported by grant 310030_184708/1 , the Vontobel Foundation, the Novartis Consumer Health Foundation , EFSD/Novo Nordisk Programme for Diabetes Research in Europe, Swiss Life Foundation, the Olga Mayenfisch Foundation , the Fondation pour l'innovation sur le cancer et la biologie , Ligue Pulmonaire Genevoise, Swiss Cancer League, Velux Foundation , Leenaards Foundation , ISREC Foundation , and the Gertrude von Meissner Foundation (C.D.); by Young Independent Investigator Grant SGED/SSED and Swiss Life Foundation (F.S.); by the Research Council of Norway 314397 (S.C.); and by ZonMW Agiko stipend 92003592 (D.J.S.). Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

month = dec,

day = "19",

doi = "https://doi.org/10.1016/j.xcrm.2023.101299",

language = "English",

volume = "4",

journal = "Cell Reports Medicine",

issn = "2666-3791",

publisher = "Cell Press",

number = "12",

}

TY - JOUR

T1 - Circadian organization of lipid landscape is perturbed in type 2 diabetic patients

AU - Sinturel, Flore

AU - Chera, Simona

AU - Brulhart-Meynet, Marie-Claude

AU - Montoya, Jonathan Paz

AU - Stenvers, Dirk Jan

AU - Bisschop, Peter H.

AU - Kalsbeek, Andries

AU - Guessous, Idris

AU - Jornayvaz, François R.

AU - Philippe, Jacques

AU - Brown, Steven A.

AU - D'Angelo, Giovanni

AU - Riezman, Howard

AU - Dibner, Charna

N1 - Funding Information: This work was supported by grant 310030_184708/1 , the Vontobel Foundation, the Novartis Consumer Health Foundation , EFSD/Novo Nordisk Programme for Diabetes Research in Europe, Swiss Life Foundation, the Olga Mayenfisch Foundation , the Fondation pour l'innovation sur le cancer et la biologie , Ligue Pulmonaire Genevoise, Swiss Cancer League, Velux Foundation , Leenaards Foundation , ISREC Foundation , and the Gertrude von Meissner Foundation (C.D.); by Young Independent Investigator Grant SGED/SSED and Swiss Life Foundation (F.S.); by the Research Council of Norway 314397 (S.C.); and by ZonMW Agiko stipend 92003592 (D.J.S.). Publisher Copyright: © 2023 The Author(s)

PY - 2023/12/19

Y1 - 2023/12/19

N2 - Lipid homeostasis in humans follows a diurnal pattern in muscle and pancreatic islets, altered upon metabolic dysregulation. We employ tandem and liquid-chromatography mass spectrometry to investigate daily regulation of lipid metabolism in subcutaneous white adipose tissue (SAT) and serum of type 2 diabetic (T2D) and non-diabetic (ND) human volunteers (n = 12). Around 8% of ≈440 lipid metabolites exhibit diurnal rhythmicity in serum and SAT from ND and T2D subjects. The spectrum of rhythmic lipids differs between ND and T2D individuals, with the most substantial changes observed early morning, as confirmed by lipidomics in an independent cohort of ND and T2D subjects (n = 32) conducted at a single morning time point. Strikingly, metabolites identified as daily rhythmic in both serum and SAT from T2D subjects exhibit phase differences. Our study reveals massive temporal and tissue-specific alterations of human lipid homeostasis in T2D, providing essential clues for the development of lipid biomarkers in a temporal manner.

AB - Lipid homeostasis in humans follows a diurnal pattern in muscle and pancreatic islets, altered upon metabolic dysregulation. We employ tandem and liquid-chromatography mass spectrometry to investigate daily regulation of lipid metabolism in subcutaneous white adipose tissue (SAT) and serum of type 2 diabetic (T2D) and non-diabetic (ND) human volunteers (n = 12). Around 8% of ≈440 lipid metabolites exhibit diurnal rhythmicity in serum and SAT from ND and T2D subjects. The spectrum of rhythmic lipids differs between ND and T2D individuals, with the most substantial changes observed early morning, as confirmed by lipidomics in an independent cohort of ND and T2D subjects (n = 32) conducted at a single morning time point. Strikingly, metabolites identified as daily rhythmic in both serum and SAT from T2D subjects exhibit phase differences. Our study reveals massive temporal and tissue-specific alterations of human lipid homeostasis in T2D, providing essential clues for the development of lipid biomarkers in a temporal manner.

KW - 1-deoxyceramides

KW - DAGs

KW - TAGs

KW - glycerophosphopholipids

KW - human circadian system

KW - lipidomics

KW - serum

KW - sphingolipids

KW - subcutaneous white adipose tissue

KW - type 2 diabetes

UR - http://www.scopus.com/inward/record.url?scp=85180072351&partnerID=8YFLogxK

U2 - https://doi.org/10.1016/j.xcrm.2023.101299

DO - https://doi.org/10.1016/j.xcrm.2023.101299

M3 - Article

C2 - 38016481

SN - 2666-3791

VL - 4

JO - Cell Reports Medicine

JF - Cell Reports Medicine

IS - 12

M1 - 101299

ER -

Circadian organization of lipid landscape is perturbed in type 2 diabetic patients

Abstract

Keywords

Access to Document

Other files and links

Cite this