Altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and SCID-hu mice

In myeloma, the bone marrow (BM) stroma mediates tumor growth directly and indirectly through the alteration of BM niches. The mesenchymal and endothelial cell subsets altered in the interstitial BM and focal lesions (FLs) of patients newly diagnosed with myeloma, as well as in the myelomasupportiv...

Full description

Saved in:
Bibliographic Details
Main Authors: Wen Ling, Maurizio Zangari, Frits van Rhee, Bart Barlogie, Shmuel Yaccoby
Format: Article
Language:English
Published: Ferrata Storti Foundation 2025-06-01
Series:Haematologica
Online Access:https://haematologica.org/article/view/12110
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850129987962667008
author Wen Ling
Maurizio Zangari
Frits van Rhee
Bart Barlogie
Shmuel Yaccoby
author_facet Wen Ling
Maurizio Zangari
Frits van Rhee
Bart Barlogie
Shmuel Yaccoby
author_sort Wen Ling
collection DOAJ
description In myeloma, the bone marrow (BM) stroma mediates tumor growth directly and indirectly through the alteration of BM niches. The mesenchymal and endothelial cell subsets altered in the interstitial BM and focal lesions (FLs) of patients newly diagnosed with myeloma, as well as in the myelomasupportive human bone of the SCID-hu mouse model, were identified using single-cell atlases and gene expression profiling. The mesenchymal compartment showed enriched cells reflecting matrix cancer-associated fibroblasts (CAFs) and vascular CAFs/pericytes in FLs compared to interstitial BM and in myeloma interstitial BM compared to healthy donors. Patients with myeloma possessed inflammatory mesenchymal stem cell (MSC) subsets that expressed genes resembling various CAFs, including antigen-presenting CAFs and genes composing the diagnostic three-gene MSCs score for myeloma. The vascular compartment in FLs showed reduced expression of genes representing specialized bone remodeling endothelial cells and upregulation of genes reflecting angiogenic endothelial cells. We identified stroma factor-expressing CYR61/CCN1+ myeloid cells that were detected in myeloma but not in donors’ bones. CYR61/CCN1+ myeloid cells co-expressed CD14, and their numbers were lower in the interstitial BM of patients with high-risk versus low-risk disease, and rare in FLs. These cells were enriched in the BM aspirate lipid layer. The SCID-hu model showed changes in mesenchymal and endothelial cell subsets resembling clinical FLs, except for inflammatory mesenchymal cells, which were present in the model but suppressed in FLs. Overall, this study provides a comprehensive assessment of the altered stroma in myeloma and identifies previously unappreciated microenvironmental cell subsets.
format Article
id doaj-art-75dd9cbcb51d4885bc105cfe3e0359e3
institution OA Journals
issn 0390-6078
1592-8721
language English
publishDate 2025-06-01
publisher Ferrata Storti Foundation
record_format Article
series Haematologica
spelling doaj-art-75dd9cbcb51d4885bc105cfe3e0359e32025-08-20T02:32:48ZengFerrata Storti FoundationHaematologica0390-60781592-87212025-06-01999110.3324/haematol.2025.287717Altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and SCID-hu miceWen Ling0Maurizio Zangari1Frits van Rhee2Bart Barlogie3Shmuel Yaccoby4Myeloma Center, Department of Internal Medicine, Winthrop P. Rockefeller Cancer Institute, University of Arkansas for Medical Sciences, Little Rock, ARMyeloma Center, Department of Internal Medicine, Winthrop P. Rockefeller Cancer Institute, University of Arkansas for Medical Sciences, Little Rock, ARMyeloma Center, Department of Internal Medicine, Winthrop P. Rockefeller Cancer Institute, University of Arkansas for Medical Sciences, Little Rock, ARMyeloma Center, Department of Internal Medicine, Winthrop P. Rockefeller Cancer Institute, University of Arkansas for Medical Sciences, Little Rock, ARMyeloma Center, Department of Internal Medicine, Winthrop P. Rockefeller Cancer Institute, University of Arkansas for Medical Sciences, Little Rock, AR In myeloma, the bone marrow (BM) stroma mediates tumor growth directly and indirectly through the alteration of BM niches. The mesenchymal and endothelial cell subsets altered in the interstitial BM and focal lesions (FLs) of patients newly diagnosed with myeloma, as well as in the myelomasupportive human bone of the SCID-hu mouse model, were identified using single-cell atlases and gene expression profiling. The mesenchymal compartment showed enriched cells reflecting matrix cancer-associated fibroblasts (CAFs) and vascular CAFs/pericytes in FLs compared to interstitial BM and in myeloma interstitial BM compared to healthy donors. Patients with myeloma possessed inflammatory mesenchymal stem cell (MSC) subsets that expressed genes resembling various CAFs, including antigen-presenting CAFs and genes composing the diagnostic three-gene MSCs score for myeloma. The vascular compartment in FLs showed reduced expression of genes representing specialized bone remodeling endothelial cells and upregulation of genes reflecting angiogenic endothelial cells. We identified stroma factor-expressing CYR61/CCN1+ myeloid cells that were detected in myeloma but not in donors’ bones. CYR61/CCN1+ myeloid cells co-expressed CD14, and their numbers were lower in the interstitial BM of patients with high-risk versus low-risk disease, and rare in FLs. These cells were enriched in the BM aspirate lipid layer. The SCID-hu model showed changes in mesenchymal and endothelial cell subsets resembling clinical FLs, except for inflammatory mesenchymal cells, which were present in the model but suppressed in FLs. Overall, this study provides a comprehensive assessment of the altered stroma in myeloma and identifies previously unappreciated microenvironmental cell subsets. https://haematologica.org/article/view/12110
spellingShingle Wen Ling
Maurizio Zangari
Frits van Rhee
Bart Barlogie
Shmuel Yaccoby
Altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and SCID-hu mice
Haematologica
title Altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and SCID-hu mice
title_full Altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and SCID-hu mice
title_fullStr Altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and SCID-hu mice
title_full_unstemmed Altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and SCID-hu mice
title_short Altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and SCID-hu mice
title_sort altered mesenchymal and endothelial subsets in interstitial bone marrow and focal lesions in myeloma patients and scid hu mice
url https://haematologica.org/article/view/12110
work_keys_str_mv AT wenling alteredmesenchymalandendothelialsubsetsininterstitialbonemarrowandfocallesionsinmyelomapatientsandscidhumice
AT mauriziozangari alteredmesenchymalandendothelialsubsetsininterstitialbonemarrowandfocallesionsinmyelomapatientsandscidhumice
AT fritsvanrhee alteredmesenchymalandendothelialsubsetsininterstitialbonemarrowandfocallesionsinmyelomapatientsandscidhumice
AT bartbarlogie alteredmesenchymalandendothelialsubsetsininterstitialbonemarrowandfocallesionsinmyelomapatientsandscidhumice
AT shmuelyaccoby alteredmesenchymalandendothelialsubsetsininterstitialbonemarrowandfocallesionsinmyelomapatientsandscidhumice