Digital Spatial Profiling Identifies Distinct Molecular Signatures of Vascular Lesions in Pulmonary Arterial Hypertension

Rubin M. Tuder, Aneta Gandjeva, Sarah Williams, Sushil Kumar, Vitaly O. Kheyfets, Kyle Matthew Hatton-Jones, Jacqueline R. Starr, Jeong Yun, Jason Hong, Nicholas R. West, Kurt R. Stenmark
University of Colorado Anschutz Medical Campus School of Medicine. University of Colorado. Griffith University. Brigham and Women’s Hospital and Harvard Medical School. University of California, Los Angeles.
United States and Australia

American Journal of Respiratory and Critical Care Medicine
Am J Respir Crit Care Med 2024;
DOI: 10.1164/rccm.202307-1310OC

Abstract
Rationale: Idiopathic Pulmonary Arterial Hypertension (IPAH) is characterized by extensive pulmonary vascular remodeling due to plexiform and obliterative lesions, media hypertrophy, inflammatory cell infiltration, and alterations of the adventitia.
Objective: Test the hypothesis that microscopic IPAH vascular lesions express unique molecular profiles, which collectively are different from control pulmonary arteries.
Methods: We used digital spatial transcriptomics to profile the genome-wide differential transcriptomic signature of key pathological lesions (plexiform, obliterative, intima+media hypertrophy, and adventitia) in IPAH lungs (n= 11) and compared these data to the intima+media and adventitia of control pulmonary artery (n=5).
Results: We detected 8273 transcripts in the IPAH lesions and control lung pulmonary arteries. Plexiform lesions and IPAH adventitia exhibited the greatest number of differentially expressed genes when compared with intima-media hypertrophy and obliterative lesions. Plexiform lesions in IPAH showed enrichment for (i) genes associated with TGFβ-signaling and (ii) mutated genes affecting the extracellular matrix and endothelial-mesenchymal transformation. Plexiform lesions and IPAH adventitia showed upregulation of genes involved in immune and interferon signaling, coagulation, and complement pathways. Cellular deconvolution indicated variability in the number of vascular and inflammatory cells between IPAH lesions, which underlies the differential transcript profiling.
Conclusions: IPAH lesions express unique molecular transcript profiles enriched for pathways involving pathogenetic pathways, including genetic disease drivers, innate and acquired immunity, hypoxia sensing, and angiogenesis signaling. These data provide a rich molecular-structural framework in IPAH vascular lesions that inform novel biomarkers and therapeutic targets in this highly morbid disease.

Category
Class I. Idiopathic Pulmonary Hypertension
Genetic Factors Associated with Pulmonary Vascular Disease
Pulmonary Vascular Pathology
Vascular Cell Biology and Mechanisms of Pulmonary Vascular Disease

Age Focus: Pediatric Pulmonary Vascular Disease or Adult Pulmonary Vascular Disease

Fresh or Filed Publication: Fresh (PHresh). Less than 1-2 years since publication

Article Access
Free PDF File or Full Text Article Available Through PubMed or DOI: No

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