Flow-based imaging uncovers divergent monocyte recruitment dynamics in diabetes- and TNF-α–driven vascular inflammation

D. Semo (Münster)1, X. Liang (Münster)1, M. Schwietzer (Münster)1, W. Wang (Münster)1, X. Hu (Münster)1, M. Dorenkamp (Münster)1, P. Poorana Priya (Madurai)2, J. M. Manogaran (London)3, F. C. Vincent (Kaiserslautern)4, H. Reinecke (Münster)1, R. Gofrey (Münster)1
1Universitätsklinikum Münster Klinik für Kardiologie I: Koronare Herzkrankheit, Herzinsuffizienz und Angiologie Münster, Deutschland; 2Pathologisches Institut, Velammal Medical College Hospital and Research Institute Madurai, Indien; 3Hillingdon Hospital London, Großbritannien; 4Institut für Biologie University of Maryland Global Campus Europe (UMGC-Europe) Kaiserslautern, Deutschland

Background/Purpose:
Monocyte-endothelial interactions drive acute inflammation and chronic vascular disease in type 2 diabetes mellitus (T2DM). However, it remains unclear whether molecular pathways involved in TNF-α-induced and diabetes-associated monocyte trafficking are similar or divergent. Therefore, the aim of this study is to explore potential divergences. 

Methods:
We utilized a physiological flow-based imaging system under controlled shear stress to quantifyCD14⁺ monocyte adhesion, transendothelial migration (TEM), and abluminal residence on human umbilical vein endothelial cell (HUVEC) monolayers after activation of those cells by either TNF- α or serum obtained from T2DM patients.

Results:
Both stimuli resulted in similar initial monocyte adhesion (40 adherent cells by 3 minutes within view field). On the other hand, TEM efficiencies  were quite variable. TNF-α stimulation promoted TEM (18% by 5 min post initiation) whereas T2DM conditions showed severely impaired TEM (~5% at 5 min post initiation).

Moreover, monocytes under T2DM conditions were retained abluminally longer than TNF- α (median 85 min vs. 25 min; p < 0.0001). This prolonged retention phenotype was mimicked by exposing endothelial cells to hyperglycemia.

To elucidate the underlying molecular mechanisms, we performed a comparative RNA-sequencing analysis of T2DM-stimulated (GSE92724) and TNF- α stimulated (GSE134489) endothelial cells. Analysis revealed a near-zero transcriptional correlation (r = 0.018), indicating highly divergent genomic responses. TNF- α stimulation resulted in a coordinate, NF-KB–dependent upregulation of VCAM1, ICAM1, E-selectin, and key junctional molecules, leading to organized junctional remodeling. Conversely, T2DM conditions led to a VCAM1-biased adhesion pattern with ICAM1 downregulation (0.61-fold), claudin suppression, and junctional disorganization.

KEGG pathway mapping further confirmed that TNF- α promotes coordinated endothelial–leukocyte integrin co-activation, whereas T2DM causes discordant  junctional loss. Subsequent qPCR validation showed selective upregulation of RAGE and JAM-3 under T2DM conditions—consistent with AGE-RAGE signaling and JAM-3–MAC-1-mediated monocyte trapping—in the absence of classical NF-KB activation.

Conclusion:
We could show  different patterns of monocytic adhesion and TEM  in T2DM compared to TNF-α. TNF-α stimulates leukocyte recruitment while T2DM induces  a leukocytic retention by VCAM-1 biased adhesion, junctional disorganization and impaired reverse transendothelial migration. The present  study identifies the AGE-RAGE axis and JAM-3–MAC-1 interactions as distinct, promising therapeutic targets for mitigation of  diabetic vascular inflammation.