Trauma-hemorrhagic shock induces a CD36-dependent RBC endothelial-adhesive phenotype

Edwin A. Deitch, Michael Condon, Eleonora Feketeova, George W. Machiedo, Leonard Mason, Ghia M. Vinluan, Vamsi Alli, Matthew D. Neal, Jacquelyn N. Tomaio, Jordan E. Fishman, Walter N. Durán, Zoltan Spolarics

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

OBJECTIVE:: Microvascular dysfunction is a key element in the development of the multiple organ dysfunction syndrome. Although the mechanisms for this response are unclear, RBC adhesion to endothelium may initiate intravascular occlusion leading to ischemic tissue injury. Thus, we tested the hypothesis that trauma-hemorrhage induces RBC-endothelial cell adhesion. DESIGN:: Prospective in vivo and in vitro animal study and analysis of patient blood samples. SETTING:: University research laboratory and hospital emergency and trauma units. INTERVENTION:: We initially assayed RBC adhesion to endothelial cells in vitro using RBCs obtained from rats subjected to trauma-hemorrhagic shock or sham shock as well as from severely injured trauma patients. Subsequently, we measured the role of putative RBCs and endothelial cell receptors in the increased RBC-endothelial cell adhesive response. MAIN RESULTS:: In both rats and humans, trauma-hemorrhagic shock increased RBC adhesion to endothelium as well as increasing several putative RBC surface adhesion molecules including CD36. The critical factor leading to RBC-endothelial cell adhesion was increased surface RBC CD36 expression. Adhesion of trauma-hemorrhagic shock RBCs was mediated, at least in part, by the binding of RBC CD36 to its cognate endothelial receptors (αVβ3 and VCAM-1). Gut-derived factors carried in the intestinal lymphatics triggered these trauma-hemorrhagic shock-induced RBC changes because 1) preventing trauma-hemorrhagic shock intestinal lymph from reaching the systemic circulation abrogated the RBC effects, 2) in vitro incubation of naïve whole blood with trauma-hemorrhagic shock lymph replicated the in vivo trauma-hemorrhagic shock-induced RBC changes while 3) injection of trauma-hemorrhagic shock lymph into naïve animals recreated the RBC changes observed after actual trauma-hemorrhagic shock. CONCLUSIONS:: 1) Trauma-hemorrhagic shock induces rapid RBC adhesion to endothelial cells in patients and animals. 2) Increased RBC CD36 expression characterizes the RBC-adhesive phenotype. 3) The RBC phenotypic and functional changes were induced by gut-derived humoral factors. These novel findings may explain the microvascular dysfunction occurring after trauma-hemorrhagic shock, sepsis, and other stress states..

Original languageEnglish (US)
JournalCritical care medicine
Volume42
Issue number3
DOIs
StatePublished - Mar 1 2014

Fingerprint

Hemorrhagic Shock
Adhesives
Phenotype
Wounds and Injuries
Endothelial Cells
Lymph
proctolin
Cell Adhesion
Endothelium
Hospital Units
Multiple Organ Failure
Vascular Cell Adhesion Molecule-1
Trauma Centers
Hospital Emergency Service
Shock
Sepsis

All Science Journal Classification (ASJC) codes

  • Critical Care and Intensive Care Medicine

Cite this

Deitch, E. A., Condon, M., Feketeova, E., Machiedo, G. W., Mason, L., Vinluan, G. M., ... Spolarics, Z. (2014). Trauma-hemorrhagic shock induces a CD36-dependent RBC endothelial-adhesive phenotype. Critical care medicine, 42(3). https://doi.org/10.1097/CCM.0000000000000119
Deitch, Edwin A. ; Condon, Michael ; Feketeova, Eleonora ; Machiedo, George W. ; Mason, Leonard ; Vinluan, Ghia M. ; Alli, Vamsi ; Neal, Matthew D. ; Tomaio, Jacquelyn N. ; Fishman, Jordan E. ; Durán, Walter N. ; Spolarics, Zoltan. / Trauma-hemorrhagic shock induces a CD36-dependent RBC endothelial-adhesive phenotype. In: Critical care medicine. 2014 ; Vol. 42, No. 3.
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abstract = "OBJECTIVE:: Microvascular dysfunction is a key element in the development of the multiple organ dysfunction syndrome. Although the mechanisms for this response are unclear, RBC adhesion to endothelium may initiate intravascular occlusion leading to ischemic tissue injury. Thus, we tested the hypothesis that trauma-hemorrhage induces RBC-endothelial cell adhesion. DESIGN:: Prospective in vivo and in vitro animal study and analysis of patient blood samples. SETTING:: University research laboratory and hospital emergency and trauma units. INTERVENTION:: We initially assayed RBC adhesion to endothelial cells in vitro using RBCs obtained from rats subjected to trauma-hemorrhagic shock or sham shock as well as from severely injured trauma patients. Subsequently, we measured the role of putative RBCs and endothelial cell receptors in the increased RBC-endothelial cell adhesive response. MAIN RESULTS:: In both rats and humans, trauma-hemorrhagic shock increased RBC adhesion to endothelium as well as increasing several putative RBC surface adhesion molecules including CD36. The critical factor leading to RBC-endothelial cell adhesion was increased surface RBC CD36 expression. Adhesion of trauma-hemorrhagic shock RBCs was mediated, at least in part, by the binding of RBC CD36 to its cognate endothelial receptors (αVβ3 and VCAM-1). Gut-derived factors carried in the intestinal lymphatics triggered these trauma-hemorrhagic shock-induced RBC changes because 1) preventing trauma-hemorrhagic shock intestinal lymph from reaching the systemic circulation abrogated the RBC effects, 2) in vitro incubation of na{\"i}ve whole blood with trauma-hemorrhagic shock lymph replicated the in vivo trauma-hemorrhagic shock-induced RBC changes while 3) injection of trauma-hemorrhagic shock lymph into na{\"i}ve animals recreated the RBC changes observed after actual trauma-hemorrhagic shock. CONCLUSIONS:: 1) Trauma-hemorrhagic shock induces rapid RBC adhesion to endothelial cells in patients and animals. 2) Increased RBC CD36 expression characterizes the RBC-adhesive phenotype. 3) The RBC phenotypic and functional changes were induced by gut-derived humoral factors. These novel findings may explain the microvascular dysfunction occurring after trauma-hemorrhagic shock, sepsis, and other stress states..",
author = "Deitch, {Edwin A.} and Michael Condon and Eleonora Feketeova and Machiedo, {George W.} and Leonard Mason and Vinluan, {Ghia M.} and Vamsi Alli and Neal, {Matthew D.} and Tomaio, {Jacquelyn N.} and Fishman, {Jordan E.} and Dur{\'a}n, {Walter N.} and Zoltan Spolarics",
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Deitch, EA, Condon, M, Feketeova, E, Machiedo, GW, Mason, L, Vinluan, GM, Alli, V, Neal, MD, Tomaio, JN, Fishman, JE, Durán, WN & Spolarics, Z 2014, 'Trauma-hemorrhagic shock induces a CD36-dependent RBC endothelial-adhesive phenotype', Critical care medicine, vol. 42, no. 3. https://doi.org/10.1097/CCM.0000000000000119

Trauma-hemorrhagic shock induces a CD36-dependent RBC endothelial-adhesive phenotype. / Deitch, Edwin A.; Condon, Michael; Feketeova, Eleonora; Machiedo, George W.; Mason, Leonard; Vinluan, Ghia M.; Alli, Vamsi; Neal, Matthew D.; Tomaio, Jacquelyn N.; Fishman, Jordan E.; Durán, Walter N.; Spolarics, Zoltan.

In: Critical care medicine, Vol. 42, No. 3, 01.03.2014.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Trauma-hemorrhagic shock induces a CD36-dependent RBC endothelial-adhesive phenotype

AU - Deitch, Edwin A.

AU - Condon, Michael

AU - Feketeova, Eleonora

AU - Machiedo, George W.

AU - Mason, Leonard

AU - Vinluan, Ghia M.

AU - Alli, Vamsi

AU - Neal, Matthew D.

AU - Tomaio, Jacquelyn N.

AU - Fishman, Jordan E.

AU - Durán, Walter N.

AU - Spolarics, Zoltan

PY - 2014/3/1

Y1 - 2014/3/1

N2 - OBJECTIVE:: Microvascular dysfunction is a key element in the development of the multiple organ dysfunction syndrome. Although the mechanisms for this response are unclear, RBC adhesion to endothelium may initiate intravascular occlusion leading to ischemic tissue injury. Thus, we tested the hypothesis that trauma-hemorrhage induces RBC-endothelial cell adhesion. DESIGN:: Prospective in vivo and in vitro animal study and analysis of patient blood samples. SETTING:: University research laboratory and hospital emergency and trauma units. INTERVENTION:: We initially assayed RBC adhesion to endothelial cells in vitro using RBCs obtained from rats subjected to trauma-hemorrhagic shock or sham shock as well as from severely injured trauma patients. Subsequently, we measured the role of putative RBCs and endothelial cell receptors in the increased RBC-endothelial cell adhesive response. MAIN RESULTS:: In both rats and humans, trauma-hemorrhagic shock increased RBC adhesion to endothelium as well as increasing several putative RBC surface adhesion molecules including CD36. The critical factor leading to RBC-endothelial cell adhesion was increased surface RBC CD36 expression. Adhesion of trauma-hemorrhagic shock RBCs was mediated, at least in part, by the binding of RBC CD36 to its cognate endothelial receptors (αVβ3 and VCAM-1). Gut-derived factors carried in the intestinal lymphatics triggered these trauma-hemorrhagic shock-induced RBC changes because 1) preventing trauma-hemorrhagic shock intestinal lymph from reaching the systemic circulation abrogated the RBC effects, 2) in vitro incubation of naïve whole blood with trauma-hemorrhagic shock lymph replicated the in vivo trauma-hemorrhagic shock-induced RBC changes while 3) injection of trauma-hemorrhagic shock lymph into naïve animals recreated the RBC changes observed after actual trauma-hemorrhagic shock. CONCLUSIONS:: 1) Trauma-hemorrhagic shock induces rapid RBC adhesion to endothelial cells in patients and animals. 2) Increased RBC CD36 expression characterizes the RBC-adhesive phenotype. 3) The RBC phenotypic and functional changes were induced by gut-derived humoral factors. These novel findings may explain the microvascular dysfunction occurring after trauma-hemorrhagic shock, sepsis, and other stress states..

AB - OBJECTIVE:: Microvascular dysfunction is a key element in the development of the multiple organ dysfunction syndrome. Although the mechanisms for this response are unclear, RBC adhesion to endothelium may initiate intravascular occlusion leading to ischemic tissue injury. Thus, we tested the hypothesis that trauma-hemorrhage induces RBC-endothelial cell adhesion. DESIGN:: Prospective in vivo and in vitro animal study and analysis of patient blood samples. SETTING:: University research laboratory and hospital emergency and trauma units. INTERVENTION:: We initially assayed RBC adhesion to endothelial cells in vitro using RBCs obtained from rats subjected to trauma-hemorrhagic shock or sham shock as well as from severely injured trauma patients. Subsequently, we measured the role of putative RBCs and endothelial cell receptors in the increased RBC-endothelial cell adhesive response. MAIN RESULTS:: In both rats and humans, trauma-hemorrhagic shock increased RBC adhesion to endothelium as well as increasing several putative RBC surface adhesion molecules including CD36. The critical factor leading to RBC-endothelial cell adhesion was increased surface RBC CD36 expression. Adhesion of trauma-hemorrhagic shock RBCs was mediated, at least in part, by the binding of RBC CD36 to its cognate endothelial receptors (αVβ3 and VCAM-1). Gut-derived factors carried in the intestinal lymphatics triggered these trauma-hemorrhagic shock-induced RBC changes because 1) preventing trauma-hemorrhagic shock intestinal lymph from reaching the systemic circulation abrogated the RBC effects, 2) in vitro incubation of naïve whole blood with trauma-hemorrhagic shock lymph replicated the in vivo trauma-hemorrhagic shock-induced RBC changes while 3) injection of trauma-hemorrhagic shock lymph into naïve animals recreated the RBC changes observed after actual trauma-hemorrhagic shock. CONCLUSIONS:: 1) Trauma-hemorrhagic shock induces rapid RBC adhesion to endothelial cells in patients and animals. 2) Increased RBC CD36 expression characterizes the RBC-adhesive phenotype. 3) The RBC phenotypic and functional changes were induced by gut-derived humoral factors. These novel findings may explain the microvascular dysfunction occurring after trauma-hemorrhagic shock, sepsis, and other stress states..

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