Abstract P3020: A prognostic molecular signature of hepatic steatosis is spatially heterogeneous and dynamic in human liver

A Andrew Perry (Vanderbilt University Medical Center, Nashville, TN (L.K.S., A.P., P.L., Q.S., S.Z., K.A., E.R.G., R.V.S.).) N Niran Hadad (Translational Genomics Research Institute, Phoenix, Arizona, United States) E Emeli Chatterjee (Massachusetts General Hospital, Boston, Massachusetts, United States) M Maria Jimenez Ramos (Institute for Regeneration and Repair, University of Edinburgh, Edinburgh, United Kingdom) E Eric Farber-Eger R Rashedeh Roshani L Lindsey Stolze (Vanderbilt University Medical Cente, Nashville, Tennessee, United States) M Michael Betti (Vanderbilt University Medical Center, Nashville, Tennessee, United States) S Shilin Zhao (Department of Biostatistics, Vanderbilt University Medical Center) S Shi Huang (Faculty of Dentistry, University of Hong Kong) L Liesbet Martens T Timothy Kendall (Institute for Regeneration and Repair, University of Edinburgh, Edinburgh, United Kingdom) T Tinne Thone (Ghent University, Ghent, Belgium) K Kaushik Amancherla S Samuel Bailin (Vanderbilt University Medical Cente, Nashville, Tennessee, United States) C Curtis Gabriel (Vanderbilt University, Nashville, Tennessee, United States) J John Koethe (Vanderbilt University Medical Cente, Nashville, Tennessee, United States) J John Carr (Vanderbilt University, Nashville, Tennessee, United States) J James Terry (Vanderbilt Univ Medical Center, Nashville, Tennessee, United States) N Nataraja Sarma Vaitinadin (Vanderbilt University Medical Center, Nashville, Tennessee, United States) J Jane Freedman (Vanderbilt University, Nashville, Tennessee, United States) K Kahraman Tanriverdi (Vanderbilt University Medical Cente, Nashville, Tennessee, United States) E Eric Alsop (TGen, Phoenix, Arizona, United States) K Kendall Van Keuren-Jensen J John Sauld (Emulate Inc, Boston, Massachusetts, United States) G Gautam Mahajan (Emulate Inc, Boston, Massachusetts, United States) S Sadiya Khan (Northwestern University, Chicago, Illinois, United States) L Laura Colangelo (Northwestern University, Chicago, Illinois, United States) M Matthew Nayor S Susan Fisher-hoch (UT HOUSTON SCHOOL OF PUBLIC HEALTH, Brownsville, Texas, United States) J Joseph B McCormick (The University of Texas Health, Brownsville, Texas, United States) K Kari North (UNIV OF TX HEALTH SCI CTR HOUSTON, Houston, Texas, United States) J Jennifer Below (Vanderbilt University Medical Center, Nashville, Tennessee, United States) Q Quinn Wells (VANDERBILT UNIVERSITY, Nashville, Tennessee, United States) D Dale Abel (University of California - Los Angeles, Los Angeles, California, United States) R Ravi Kalhan (Northwestern University, Oak Park, Illinois, United States) C Charlotte Scott (Ghent University, Ghent, Belgium) M Martin Guilliams E Eric Gamazon J Jonathan Fallowfield (Institute for Regeneration and Repair, University of Edinburgh, Edinburgh, United Kingdom) N Nicholas Banovich (Translational Genomics Research Institute, Phoenix, Arizona, United States) S Saumya Das R Ravi Shah

Abstract

Introduction: The prevalence of hepatic steatosis—a central and early phenotype in multi-system metabolic dysfunction—is increasing in parallel with the obesity pandemic, calling for novel approaches for prevention and treatment. Hypothesis: We hypothesized that the circulating proteome may reflect cell specific mechanisms of hepatic steatosis. Methods: Using multi-modality hepatic imaging and broad circulating proteomics in approximately 5,000 individuals across 3 diverse cohorts (CARDIA, Cameron County Hispanic Cohort, UK Biobank), we identified proteins implicated in the progression of hepatic steatosis. We tested for a relationship with these proteomic markers of hepatic steatosis with metabolic-related clinical outcomes in UK Biobank. We translated these findings from the circulating proteome to several tissue-based datasets including bulk RNA sequencing, single-cell RNA sequencing, and spatial transcriptomics. To further prove the hepatocyte origin of prioritized proteins, we used a humanized “liver-on-a-chip” model. Results: We observed proteins implicated in the progression of hepatic steatosis—such as those related to central carbon and amino acid metabolism, hepatocyte regeneration, inflammation, fibrosis, insulin sensitivity—are largely encoded by genes enriched at the transcriptional level in human liver. Circulating multi-protein signatures of hepatic steatosis were strongly associated with a fatty liver disease phenotype and multi-system metabolic outcomes in >26,000 free-living individuals. Moreover, we observed increased activity of transcripts encoding proteins prioritized in clinical studies spatially in areas of steatosis via spatial transcriptomics in human liver, with several top candidates dynamic during progression of steatosis in human liver. Finally, using a humanized “liver-on-a-chip” model, we induced hepatic steatosis, confirming cell-specific expression of targets implicated across tissue and clinical studies at a transcriptional and proteomic level. Conclusions: These results underscore the utility of a unified approach that combines human studies, multi-omics, and dynamic tissue-on-a-chip experiments to identify a prognostic, functional, dynamic “liquid biopsy” of human liver, with relevance for clinical biomarker discovery and mechanistic research applications.

Article Details

Journal Circulation
Volume / Issue Vol. 151, Issue Suppl_1
Published March 11, 2025
ISSN 0009-7322
Publisher Lippincott Williams & Wilkins

Journal Info

Circulation

Lippincott Williams & Wilkins

ISSN: 0009-7322 Health Sciences

Authors (43)

A

Andrew Perry

Vanderbilt University Medical Center, Nashville, TN (L.K.S., A.P., P.L., Q.S., S.Z., K.A., E.R.G., R.V.S.).

N

Niran Hadad

Translational Genomics Research Institute, Phoenix, Arizona, United States

E

Emeli Chatterjee

Massachusetts General Hospital, Boston, Massachusetts, United States

M

Maria Jimenez Ramos

Institute for Regeneration and Repair, University of Edinburgh, Edinburgh, United Kingdom

E

Eric Farber-Eger

R

Rashedeh Roshani

L

Lindsey Stolze

Vanderbilt University Medical Cente, Nashville, Tennessee, United States

M

Michael Betti

Vanderbilt University Medical Center, Nashville, Tennessee, United States

S

Shilin Zhao

Department of Biostatistics, Vanderbilt University Medical Center

S

Shi Huang

Faculty of Dentistry, University of Hong Kong

L

Liesbet Martens

T

Timothy Kendall

Institute for Regeneration and Repair, University of Edinburgh, Edinburgh, United Kingdom

T

Tinne Thone

Ghent University, Ghent, Belgium

K

Kaushik Amancherla

S

Samuel Bailin

Vanderbilt University Medical Cente, Nashville, Tennessee, United States

C

Curtis Gabriel

Vanderbilt University, Nashville, Tennessee, United States

J

John Koethe

Vanderbilt University Medical Cente, Nashville, Tennessee, United States

J

John Carr

Vanderbilt University, Nashville, Tennessee, United States

J

James Terry

Vanderbilt Univ Medical Center, Nashville, Tennessee, United States

N

Nataraja Sarma Vaitinadin

Vanderbilt University Medical Center, Nashville, Tennessee, United States

J

Jane Freedman

Vanderbilt University, Nashville, Tennessee, United States

K

Kahraman Tanriverdi

Vanderbilt University Medical Cente, Nashville, Tennessee, United States

E

Eric Alsop

TGen, Phoenix, Arizona, United States

K

Kendall Van Keuren-Jensen

J

John Sauld

Emulate Inc, Boston, Massachusetts, United States

G

Gautam Mahajan

Emulate Inc, Boston, Massachusetts, United States

S

Sadiya Khan

Northwestern University, Chicago, Illinois, United States

L

Laura Colangelo

Northwestern University, Chicago, Illinois, United States

M

Matthew Nayor

S

Susan Fisher-hoch

UT HOUSTON SCHOOL OF PUBLIC HEALTH, Brownsville, Texas, United States

J

Joseph B McCormick

The University of Texas Health, Brownsville, Texas, United States

K

Kari North

UNIV OF TX HEALTH SCI CTR HOUSTON, Houston, Texas, United States

J

Jennifer Below

Vanderbilt University Medical Center, Nashville, Tennessee, United States

Q

Quinn Wells

VANDERBILT UNIVERSITY, Nashville, Tennessee, United States

D

Dale Abel

University of California - Los Angeles, Los Angeles, California, United States

R

Ravi Kalhan

Northwestern University, Oak Park, Illinois, United States

C

Charlotte Scott

Ghent University, Ghent, Belgium

M

Martin Guilliams

E

Eric Gamazon

J

Jonathan Fallowfield

Institute for Regeneration and Repair, University of Edinburgh, Edinburgh, United Kingdom

N

Nicholas Banovich

Translational Genomics Research Institute, Phoenix, Arizona, United States

S

Saumya Das

R

Ravi Shah