Molecular insight into the interplay among heterogeneous plasmacytes and microenvironment cells and their clinical relevance in myeloma

L Lu Jiang (School of Flexible Electronics (Future Technologies), Key Laboratory of Flexible Electronics, and Institute of Advanced Materials, Nanjing Tech University, 30 South Puzhu Road, Nanjing 211816, P. R. China) C Cheng-Lin Liu (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine) Y Yu-Liang Zhang (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine) N Niu Qiao (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine) J Jian-Feng Li (Xiamen University , , ,) S Shuang-Shuang Yang (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine) X Xiao-Zhong Shen (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine) M Meng-Ping Chen (Department of Hematology, Renji Hospital, Shanghai Jiao Tong University School of Medicine) S Sheng-Yue Wang (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine) T Ting Wu (Children’s Hospital, Zhejiang University School of Medicine) B Bing Chen S Shu-Ting Yu (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine) F Fang-Ying Jiang (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine) S Shuai Wang Y Yuan-Fang Liu (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine) Y Yan Wang Y Yi Tao (Guangdong Provincial Engineering Research Center for Urban Water Recycling and Environmental Safety, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong, China.) Z Zhu Chen (Key Laboratory of Biomedical Polymers of Ministry of Education, Department of Chemistry, Department of Cardiology, Zhongnan Hospital) J Jian-Qing Mi (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine) J Jian Hou J Jie Xu S Sai-Juan Chen (Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine)

Abstract

Multiple myeloma (MM) develops with the acquisition of genetic abnormalities in plasmacytes and changes in microenvironment cells (MECs). Despite the progress in understanding MM disease mechanism through omics studies, the genomic/transcriptomic profiling remains limited in Chinese MM patients. Here, we collected 277 newly diagnosed MM (NDMM) patients in the Shanghai MM Omics (SMMO) project. Analysis of 267 cases with whole-genome/whole-exome sequencing and RNA sequencing (RNA-seq) identified three genetic groups (MY, HRD, and MS/CD). Using single-cell RNA sequencing (scRNA-seq), we investigated 59 NDMM subjects from SMMO, 20 relapsed cases from public database and 30 normal controls. Eight subpopulations of plasmacytes from NDMM (mSP1–mSP8) were defined, each showing unique signatures while forming a differentiation trajectory. The mSP2 is worth noting due to its high proliferative property. Regarding MECs, we found T cell subsets including T-helpers, Tregs, and cytotoxic T cells all in dysfunctional status and increased myeloid-derived suppressor cells such as macrophages mainly in M2 polarization, both constituting a milieu in favor of MM cell growth and immune escape. Furthermore, we scrutinized the crosstalk between MM cells and MECs and that among distinct MECs. A dynamic, comprehensive MM pathogenesis network was revealed, with a number of ligand–receptor pairs. Importantly, the mSP2 signature can be projected to the MM cell RNA-seq data of 235 patients to generate a Score100 with prognostic value in SMMO. Via multivariate analysis of the International Staging System, Consensus Genomic Staging, and Score100, we propose a practical MM stratification model for evaluating aggressive myeloma.

Article Details

Volume / Issue Vol. 123, Issue 21
Published May 26, 2026
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (22)

L

Lu Jiang

School of Flexible Electronics (Future Technologies), Key Laboratory of Flexible Electronics, and Institute of Advanced Materials, Nanjing Tech University, 30 South Puzhu Road, Nanjing 211816, P. R. China

C

Cheng-Lin Liu

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine

Y

Yu-Liang Zhang

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine

N

Niu Qiao

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine

J

Jian-Feng Li

Xiamen University , , ,

S

Shuang-Shuang Yang

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine

X

Xiao-Zhong Shen

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine

M

Meng-Ping Chen

Department of Hematology, Renji Hospital, Shanghai Jiao Tong University School of Medicine

S

Sheng-Yue Wang

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine

T

Ting Wu

Children’s Hospital, Zhejiang University School of Medicine

B

Bing Chen

S

Shu-Ting Yu

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine

F

Fang-Ying Jiang

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Center for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine

S

Shuai Wang

Y

Yuan-Fang Liu

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine

Y

Yan Wang

Y

Yi Tao

Guangdong Provincial Engineering Research Center for Urban Water Recycling and Environmental Safety, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong, China.

Z

Zhu Chen

Key Laboratory of Biomedical Polymers of Ministry of Education, Department of Chemistry, Department of Cardiology, Zhongnan Hospital

J

Jian-Qing Mi

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine

J

Jian Hou

J

Jie Xu

S

Sai-Juan Chen

Shanghai Institute of Hematology, State Key Laboratory of Medical Genomics, National Research Centre for Translational Medicine at Shanghai, Research Unit of Hematologic Malignancies Genomics and Translational Research of Chinese Academy of Medical Sciences, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine