High Dimensional Immune Profiling of Smoldering Multiple Myeloma Distinguishes Distinct Tumor Microenvironments
Multiple myeloma (MM) is a malignancy of plasma cells that arises from premalignant Monoclonal Gammopathy of Undetermined Significance (MGUS) and often progresses through an asymptomatic Smoldering (SMM) phase. Understanding the interactions between abnormal clonal plasma cells and the tumor microen...
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| Published in | Clinical lymphoma, myeloma and leukemia Vol. 22; no. 11; pp. 853 - 862 |
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| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Elsevier Inc
01.11.2022
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| Abstract | Multiple myeloma (MM) is a malignancy of plasma cells that arises from premalignant Monoclonal Gammopathy of Undetermined Significance (MGUS) and often progresses through an asymptomatic Smoldering (SMM) phase. Understanding the interactions between abnormal clonal plasma cells and the tumor microenvironment (TME) in the early disease states (MGUS, SMM) may inform risk assessment and therapy.
We performed high dimensional immunologic analysis of bone marrow specimens from 73 subjects with SMM by mass cytometry and T cell receptor sequencing of CD138-depleted bone marrow (BM) mononuclear cells, and proteomics and seromic profiling of BM plasma. Analysis of individual assay data identified self-organizing subgroups of SMM patients. We then applied novel bioinformatic methods to integrate data from pairs, trios, and quartets of assays.
Mass cytometry, TCRSeq and proteomics identified three taxa (sing. taxon) of subjects that shared common characteristics across all three assays. Differential levels of BM plasma pleiotropin (PTN) and BM T cells and their productive clonality emerged as strong distinguishing factors among these taxa.
These results suggest that the continuum from MGUS to MM does not consist of a single pathway in the TME, and that complex interactions between myeloma cells and the TME may ultimately determine progression and inform clinical management.
Smoldering multiple myeloma is a heterogeneous condition with continuous risk for progression to active disease. Integrated analysis of high dimensional immune profiling data identifies 3 distinct groups in a smoldering myeloma cohort. Each immunophenotypic group has features that suggest functional states in the bone marrow microenvironment that may contribute to stability or progression. |
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| AbstractList | Multiple myeloma (MM) is a malignancy of plasma cells that arises from premalignant Monoclonal Gammopathy of Undetermined Significance (MGUS) and often progresses through an asymptomatic Smoldering (SMM) phase. Understanding the interactions between abnormal clonal plasma cells and the tumor microenvironment (TME) in the early disease states (MGUS, SMM) may inform risk assessment and therapy.
We performed high dimensional immunologic analysis of bone marrow specimens from 73 subjects with SMM by mass cytometry and T cell receptor sequencing of CD138-depleted bone marrow (BM) mononuclear cells, and proteomics and seromic profiling of BM plasma. Analysis of individual assay data identified self-organizing subgroups of SMM patients. We then applied novel bioinformatic methods to integrate data from pairs, trios, and quartets of assays.
Mass cytometry, TCRSeq and proteomics identified three taxa (sing. taxon) of subjects that shared common characteristics across all three assays. Differential levels of BM plasma pleiotropin (PTN) and BM T cells and their productive clonality emerged as strong distinguishing factors among these taxa.
These results suggest that the continuum from MGUS to MM does not consist of a single pathway in the TME, and that complex interactions between myeloma cells and the TME may ultimately determine progression and inform clinical management.
Smoldering multiple myeloma is a heterogeneous condition with continuous risk for progression to active disease. Integrated analysis of high dimensional immune profiling data identifies 3 distinct groups in a smoldering myeloma cohort. Each immunophenotypic group has features that suggest functional states in the bone marrow microenvironment that may contribute to stability or progression. Multiple myeloma (MM) is a malignancy of plasma cells that arises from premalignant Monoclonal Gammopathy of Undetermined Significance (MGUS) and often progresses through an asymptomatic Smoldering (SMM) phase. Understanding the interactions between abnormal clonal plasma cells and the tumor microenvironment (TME) in the early disease states (MGUS, SMM) may inform risk assessment and therapy.BACKGROUNDMultiple myeloma (MM) is a malignancy of plasma cells that arises from premalignant Monoclonal Gammopathy of Undetermined Significance (MGUS) and often progresses through an asymptomatic Smoldering (SMM) phase. Understanding the interactions between abnormal clonal plasma cells and the tumor microenvironment (TME) in the early disease states (MGUS, SMM) may inform risk assessment and therapy.We performed high dimensional immunologic analysis of bone marrow specimens from 73 subjects with SMM by mass cytometry and T cell receptor sequencing of CD138-depleted bone marrow (BM) mononuclear cells, and proteomics and seromic profiling of BM plasma. Analysis of individual assay data identified self-organizing subgroups of SMM patients. We then applied novel bioinformatic methods to integrate data from pairs, trios, and quartets of assays.PATIENTS AND METHODSWe performed high dimensional immunologic analysis of bone marrow specimens from 73 subjects with SMM by mass cytometry and T cell receptor sequencing of CD138-depleted bone marrow (BM) mononuclear cells, and proteomics and seromic profiling of BM plasma. Analysis of individual assay data identified self-organizing subgroups of SMM patients. We then applied novel bioinformatic methods to integrate data from pairs, trios, and quartets of assays.Mass cytometry, TCRSeq and proteomics identified three taxa (sing. taxon) of subjects that shared common characteristics across all three assays. Differential levels of BM plasma pleiotropin (PTN) and BM T cells and their productive clonality emerged as strong distinguishing factors among these taxa.RESULTSMass cytometry, TCRSeq and proteomics identified three taxa (sing. taxon) of subjects that shared common characteristics across all three assays. Differential levels of BM plasma pleiotropin (PTN) and BM T cells and their productive clonality emerged as strong distinguishing factors among these taxa.These results suggest that the continuum from MGUS to MM does not consist of a single pathway in the TME, and that complex interactions between myeloma cells and the TME may ultimately determine progression and inform clinical management.CONCLUSIONThese results suggest that the continuum from MGUS to MM does not consist of a single pathway in the TME, and that complex interactions between myeloma cells and the TME may ultimately determine progression and inform clinical management. |
| Author | Auclair, Daniel Yesil, Jen Gnjatic, Sacha Cho, Hearn Jay Parekh, Samir Perumal, Deepak Adams, Homer Kim-Schulze, Seunghee Fernandez, Nicolas Rahman, Adeeb |
| Author_xml | – sequence: 1 givenname: Nicolas surname: Fernandez fullname: Fernandez, Nicolas organization: Precision Immunology Institute – sequence: 2 givenname: Deepak surname: Perumal fullname: Perumal, Deepak organization: Tisch Cancer Institute – sequence: 3 givenname: Adeeb surname: Rahman fullname: Rahman, Adeeb organization: Human Immune Monitoring Center – sequence: 4 givenname: Seunghee surname: Kim-Schulze fullname: Kim-Schulze, Seunghee organization: Human Immune Monitoring Center – sequence: 5 givenname: Jen surname: Yesil fullname: Yesil, Jen organization: Multiple Myeloma Research Foundation, Norwalk, CT – sequence: 6 givenname: Daniel orcidid: 0000-0001-5151-3058 surname: Auclair fullname: Auclair, Daniel organization: Multiple Myeloma Research Foundation, Norwalk, CT – sequence: 7 givenname: Homer orcidid: 0000-0003-0506-4591 surname: Adams fullname: Adams, Homer organization: Janssen Research & Development, LLC, Spring House, PA – sequence: 8 givenname: Samir surname: Parekh fullname: Parekh, Samir organization: Precision Immunology Institute – sequence: 9 givenname: Sacha surname: Gnjatic fullname: Gnjatic, Sacha organization: Precision Immunology Institute – sequence: 10 givenname: Hearn Jay orcidid: 0000-0003-4481-5757 surname: Cho fullname: Cho, Hearn Jay email: hearn.jay.cho@mssm.edu organization: Precision Immunology Institute |
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| CitedBy_id | crossref_primary_10_1016_j_ymgme_2025_109074 crossref_primary_10_3390_diagnostics13142328 crossref_primary_10_3389_fcell_2024_1359084 crossref_primary_10_3390_curroncol30070455 crossref_primary_10_3390_cells14060430 |
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