Halting the vicious cycle within the multiple myeloma ecosystem: blocking JAM-A on bone marrow endothelial cells restores angiogenic homeostasis and suppresses tumor progression

Haematologica. 2021 Jul 1;106(7):1943-1956. doi: 10.3324/haematol.2019.239913.

Abstract

Interactions of malignant multiple myeloma (MM) plasma cells (MM-cells) with the microenvironment control MM-cell growth, survival, drug-resistance and dissemination. As in MM microvascular density increases in the bone marrow (BM), we investigated whether BM MM endothelial cells (MMECs) control disease progression via the junctional adhesion molecule A (JAM-A). Membrane and cytoplasmic JAM-A levels were upregulated in MMECs in 111 newly diagnosed (NDMM) and 201 relapsed-refractory (RRMM) patients compared to monoclonal gammopathy of undetermined significance (MGUS) and healthy controls. Elevated membrane expression of JAM-A on MMECs predicted poor clinical outcome. Mechanistically, addition of recombinant JAM-A to MMECs increased angiogenesis whereas its inhibition impaired angiogenesis and MM growth in 2D and 3D in vitro cell culture and chorioallantoic membrane-assays. To corroborate these findings, we treated MM bearing mice with JAM-A blocking mAb and demonstrated impaired MM progression corresponding to decreased MM-related vascularity. These findings support JAM-A as an important mediator of MM progression through facilitating MM-associated angiogenesis. Collectively, elevated JAM-A expression on bone marrow endothelial cells is an independent prognostic factor for patient survival in both NDMM and RRMM. Blocking JAM-A restricts angiogenesis in vitro, in embrio and in vivo and represents a suitable druggable molecule to halt neoangiogenesis and MM progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow
  • Ecosystem
  • Endothelial Cells
  • Homeostasis
  • Humans
  • Junctional Adhesion Molecule A*
  • Mice
  • Multiple Myeloma* / drug therapy
  • Tumor Microenvironment

Substances

  • Junctional Adhesion Molecule A

Grants and funding

FundingThis work was supported by the Bayerische Forschungsstiftung consortium FortiTher (WP2TP3), the Deutsche Forschungsgemeinschaft mBone consortium (2084/1, 401253051), by the Italian Association for Cancer Research (AIRC) through an Investigator Grant (n. 20441 to VR), by the GLOBALDOC Project - CUP H96J17000160002 approved with A.D. n. 9 from Puglia Region, financed under the Action Plan for Cohesion approved with Commission decision C (2016) 1417 to AGS. This research project was supported in part by the Apulian Regional Project “Medicina di Precisione” to AGS. AR was supported by the Wilhelm Sander-Stiftung (grant n. 2014.903.1).