Temporal RAGE Over-Expression Disrupts Lung Development by Modulating Apoptotic Signaling

Receptors for advanced glycation end products (RAGE) are multiligand cell surface receptors found most abundantly in lung tissue. This study sought to evaluate the role of RAGE in lung development by using a transgenic (TG) mouse model that spatially and temporally controlled RAGE overexpression. Hi...

Full description

Saved in:
Bibliographic Details
Main Authors: Derek M. Clarke, Madison N. Kirkham, Logan B. Beck, Carrleigh Campbell, Hayden Alcorn, Benjamin T. Bikman, Juan A. Arroyo, Paul R. Reynolds
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Current Issues in Molecular Biology
Subjects:
Online Access:https://www.mdpi.com/1467-3045/46/12/867
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850050854576455680
author Derek M. Clarke
Madison N. Kirkham
Logan B. Beck
Carrleigh Campbell
Hayden Alcorn
Benjamin T. Bikman
Juan A. Arroyo
Paul R. Reynolds
author_facet Derek M. Clarke
Madison N. Kirkham
Logan B. Beck
Carrleigh Campbell
Hayden Alcorn
Benjamin T. Bikman
Juan A. Arroyo
Paul R. Reynolds
author_sort Derek M. Clarke
collection DOAJ
description Receptors for advanced glycation end products (RAGE) are multiligand cell surface receptors found most abundantly in lung tissue. This study sought to evaluate the role of RAGE in lung development by using a transgenic (TG) mouse model that spatially and temporally controlled RAGE overexpression. Histological imaging revealed that RAGE upregulation from embryonic day (E) 15.5 to E18.5 led to a thickened alveolar parenchyma and reduced alveolar surface area, while RAGE overexpression from E0 to E18.5 caused a significant loss of tissue and decreased architecture. Mitochondrial dysfunction was a hallmark of RAGE-mediated disruption, with decreased levels of anti-apoptotic BCL-W and elevated pro-apoptotic BID, SMAC, and HTRA2, indicating compromised mitochondrial integrity and increased intrinsic apoptotic activity. Extrinsic apoptotic signaling was similarly dysregulated, as evidenced by the increased expression of TNFRSF21, Fas/FasL, and Trail R2 in E0-18.5 RAGE TG mice. Additionally, reductions in IGFBP-3 and IGFBP-4, coupled with elevated p53 and decreased p27 expression, highlighted disruptions in the cell survival and cycle regulatory pathways. Despite the compensatory upregulation of inhibitors of apoptosis proteins (cIAP-2, XIAP, and Survivin), tissue loss and structural damage persisted. These findings underscore RAGE’s role as a pivotal modulator of lung development. Specifically, the timing of RAGE upregulation significantly impacts lung development by influencing pathways that cause distinct histological phenotypes. This research may foreshadow how RAGE signaling plausibly contributes to developmental lung diseases.
format Article
id doaj-art-e4fd78c526444980879100bbd4daf75d
institution DOAJ
issn 1467-3037
1467-3045
language English
publishDate 2024-12-01
publisher MDPI AG
record_format Article
series Current Issues in Molecular Biology
spelling doaj-art-e4fd78c526444980879100bbd4daf75d2025-08-20T02:53:19ZengMDPI AGCurrent Issues in Molecular Biology1467-30371467-30452024-12-014612144531446310.3390/cimb46120867Temporal RAGE Over-Expression Disrupts Lung Development by Modulating Apoptotic SignalingDerek M. Clarke0Madison N. Kirkham1Logan B. Beck2Carrleigh Campbell3Hayden Alcorn4Benjamin T. Bikman5Juan A. Arroyo6Paul R. Reynolds7Department of Cell Biology and Physiology, Brigham Young University, 3054 Life Sciences Building, Provo, UT 84602, USADepartment of Cell Biology and Physiology, Brigham Young University, 3054 Life Sciences Building, Provo, UT 84602, USADepartment of Cell Biology and Physiology, Brigham Young University, 3054 Life Sciences Building, Provo, UT 84602, USADepartment of Cell Biology and Physiology, Brigham Young University, 3054 Life Sciences Building, Provo, UT 84602, USADepartment of Cell Biology and Physiology, Brigham Young University, 3054 Life Sciences Building, Provo, UT 84602, USADepartment of Cell Biology and Physiology, Brigham Young University, 3054 Life Sciences Building, Provo, UT 84602, USADepartment of Cell Biology and Physiology, Brigham Young University, 3054 Life Sciences Building, Provo, UT 84602, USADepartment of Cell Biology and Physiology, Brigham Young University, 3054 Life Sciences Building, Provo, UT 84602, USAReceptors for advanced glycation end products (RAGE) are multiligand cell surface receptors found most abundantly in lung tissue. This study sought to evaluate the role of RAGE in lung development by using a transgenic (TG) mouse model that spatially and temporally controlled RAGE overexpression. Histological imaging revealed that RAGE upregulation from embryonic day (E) 15.5 to E18.5 led to a thickened alveolar parenchyma and reduced alveolar surface area, while RAGE overexpression from E0 to E18.5 caused a significant loss of tissue and decreased architecture. Mitochondrial dysfunction was a hallmark of RAGE-mediated disruption, with decreased levels of anti-apoptotic BCL-W and elevated pro-apoptotic BID, SMAC, and HTRA2, indicating compromised mitochondrial integrity and increased intrinsic apoptotic activity. Extrinsic apoptotic signaling was similarly dysregulated, as evidenced by the increased expression of TNFRSF21, Fas/FasL, and Trail R2 in E0-18.5 RAGE TG mice. Additionally, reductions in IGFBP-3 and IGFBP-4, coupled with elevated p53 and decreased p27 expression, highlighted disruptions in the cell survival and cycle regulatory pathways. Despite the compensatory upregulation of inhibitors of apoptosis proteins (cIAP-2, XIAP, and Survivin), tissue loss and structural damage persisted. These findings underscore RAGE’s role as a pivotal modulator of lung development. Specifically, the timing of RAGE upregulation significantly impacts lung development by influencing pathways that cause distinct histological phenotypes. This research may foreshadow how RAGE signaling plausibly contributes to developmental lung diseases.https://www.mdpi.com/1467-3045/46/12/867RAGElungembryotransgenicapoptosis
spellingShingle Derek M. Clarke
Madison N. Kirkham
Logan B. Beck
Carrleigh Campbell
Hayden Alcorn
Benjamin T. Bikman
Juan A. Arroyo
Paul R. Reynolds
Temporal RAGE Over-Expression Disrupts Lung Development by Modulating Apoptotic Signaling
Current Issues in Molecular Biology
RAGE
lung
embryo
transgenic
apoptosis
title Temporal RAGE Over-Expression Disrupts Lung Development by Modulating Apoptotic Signaling
title_full Temporal RAGE Over-Expression Disrupts Lung Development by Modulating Apoptotic Signaling
title_fullStr Temporal RAGE Over-Expression Disrupts Lung Development by Modulating Apoptotic Signaling
title_full_unstemmed Temporal RAGE Over-Expression Disrupts Lung Development by Modulating Apoptotic Signaling
title_short Temporal RAGE Over-Expression Disrupts Lung Development by Modulating Apoptotic Signaling
title_sort temporal rage over expression disrupts lung development by modulating apoptotic signaling
topic RAGE
lung
embryo
transgenic
apoptosis
url https://www.mdpi.com/1467-3045/46/12/867
work_keys_str_mv AT derekmclarke temporalrageoverexpressiondisruptslungdevelopmentbymodulatingapoptoticsignaling
AT madisonnkirkham temporalrageoverexpressiondisruptslungdevelopmentbymodulatingapoptoticsignaling
AT loganbbeck temporalrageoverexpressiondisruptslungdevelopmentbymodulatingapoptoticsignaling
AT carrleighcampbell temporalrageoverexpressiondisruptslungdevelopmentbymodulatingapoptoticsignaling
AT haydenalcorn temporalrageoverexpressiondisruptslungdevelopmentbymodulatingapoptoticsignaling
AT benjamintbikman temporalrageoverexpressiondisruptslungdevelopmentbymodulatingapoptoticsignaling
AT juanaarroyo temporalrageoverexpressiondisruptslungdevelopmentbymodulatingapoptoticsignaling
AT paulrreynolds temporalrageoverexpressiondisruptslungdevelopmentbymodulatingapoptoticsignaling