Regulation of antigen-specific T cell infiltration and spatial architecture in multiple myeloma and premalignancy
Open accessAbstract
Entry of antigen-specific T cells into human tumors is critical for immunotherapy, but the underlying mechanisms are poorly understood. Here, we combined high-dimensional spatial analyses with in vitro and in vivo modeling to study the mechanisms underlying immune infiltration in human multiple myeloma (MM) and its precursor monoclonal gammopathy of undetermined significance (MGUS). Clustered tumor growth was a feature of MM but not MGUS biopsies, and this growth pattern was reproduced in humanized mouse models. MM biopsies exhibited intralesional as well as spatial heterogeneity, with coexistence of T cell-rich and T cell-sparse regions and the presence of areas of T cell exclusion. In vitro studies demonstrated that T cell entry into MM clusters was regulated by agonistic signals and CD2-CD58 interactions. Upon adoptive transfer, antigen-specific T cells localized to the tumor site but required in situ DC-mediated antigen presentation for tumor entry. C-type lectin domain family 9 member A-positive (CLEC9A+) DCs appeared to mark portals of entry for gradients of T cell infiltration in MM biopsies, and their proximity to T cell factor 1-positive (TCF1+) T cells correlated with disease state and risk status. These data illustrate a role for tumor-associated DCs and in situ activation in promoting the infiltration of antigen-specific T cells in MM and provide insights into spatial alterations in tumor/immune cells with malignant evolution.
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Several patterns of immune dysregulation have been reported in MGUS and SMM using single cell RNA sequencing.
“Several patterns of dysregulation have been reported using single cell RNA sequencing.82,83,91-93”
From Evolution of Multiple Myeloma from a Genomic Perspective (2026) · cites this paper as [92]
The Results section, “Immune composition in MGUS, SMM, and MM” (page unavailable), reports differences in immune-cell composition across these conditions. But the paper says it studied the biopsies using multiplex immunofluorescence; its Methods also describe digital spatial profiling, not single-cell RNA sequencing. The claimed method is therefore unsupported for this source. (LLM, conf=0.86)
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- Authors
- Robinson, M. H., Villa, N. Y., Jaye, D. L., Nooka, A. K., Duffy, A., McCachren, S. S., Manalo, J., Switchenko, J. M., Barnes, S., Potdar, S., Azeem, M. I., Horvat, A. A., Parihar, V. C., Gong, J., Liang, Y., Smith, G. H., Gupta, V. A., Boise, L. H., Kaufman, J. L., Hofmeister, C. C., Joseph, N. S., Lonial, S., Dhodapkar, K. M., & Dhodapkar, M. V.
- Affiliations
- Emory University (US)
- Nanostring Technologies (United States) (US)
- Corresponding author
- Dhodapkar, Madhav V.
- ORCID
- Robinson, M. Hope
- Villa, Nancy Y.
- Jaye, David L.
- Nooka, Ajay K.
- Duffy, Alyssa
- McCachren, Samuel S.
- Switchenko, Jeffrey M.
- Potdar, Sayalee
- Azeem, Maryam I.
- Parihar, Vaunita C.
- Gong, Jingjing
- Liang, Yan
- Smith, Geoffrey H.
- Gupta, Vikas A.
- Boise, Lawrence H.
- Kaufman, Jonathan L.
- Hofmeister, Craig C.
- Joseph, Nisha S.
- Lonial, Sagar
- Dhodapkar, Kavita M.
- Dhodapkar, Madhav V.
- Venue
- Journal of Clinical Investigation
- Published
- 2023-08-01
- Volume
- 133
- Issue
- 15
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC10378152
- OpenAlex
- W4385410340
- Cited by
- 48
- References
- 37
- Citations by year
- 2026: 11 · 2025: 20 · 2024: 15 · 2023: 2
- FWCI
- 9.92
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal of Clinical Investigation (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- NCI (CA197603)
- Topics
- Health Sciences › Medicine › Hematology › Multiple Myeloma Research and Treatments
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- multiple myeloma, monoclonal gammopathy of undetermined significance, tumor immune microenvironment, spatial heterogeneity, T-cell exclusion, tumor-associated dendritic cells, CLEC9A, TCF1, antigen presentation, tumor clusters, humanized mice, adoptive T cell therapy
- MeSH terms
- Animals, Dendritic Cells, Humans, Immunotherapy, Multiple Myeloma, Precancerous Conditions, T-Lymphocytes, Antigen Presentation, Mice
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