Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms.

We hypothesized that endothelial progenitor cells derived from individuals with diabetes would exhibit functional defects including inability to respond to hypoxia and altered paracrine/autocrine function that would impair the angiogenic potential of these cells. Circulating mononuclear cells isolat...

Full description

Saved in:
Bibliographic Details
Main Authors: Yagna P R Jarajapu, Sugata Hazra, Mark Segal, Sergio Li Calzi, Chandra Jadhao, Kevin Qian, Sayak K Mitter, Mohan K Raizada, Michael E Boulton, Maria B Grant
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0093965&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850026369101070336
author Yagna P R Jarajapu
Sugata Hazra
Mark Segal
Sergio Li Calzi
Chandra Jadhao
Kevin Qian
Sayak K Mitter
Mohan K Raizada
Michael E Boulton
Maria B Grant
author_facet Yagna P R Jarajapu
Sugata Hazra
Mark Segal
Sergio Li Calzi
Chandra Jadhao
Kevin Qian
Sayak K Mitter
Mohan K Raizada
Michael E Boulton
Maria B Grant
author_sort Yagna P R Jarajapu
collection DOAJ
description We hypothesized that endothelial progenitor cells derived from individuals with diabetes would exhibit functional defects including inability to respond to hypoxia and altered paracrine/autocrine function that would impair the angiogenic potential of these cells. Circulating mononuclear cells isolated from diabetic (n = 69) and nondiabetic (n = 46) individuals were used to grow endothelial colony forming cells (ECFC), early endothelial progenitor cells (eEPCs) and isolate CD34+ cells. ECFCs and eEPCs were established from only 15% of the diabetic individuals tested thus directing our main effort toward examination of CD34+ cells. CD34+ cells were plated in basal medium to obtain cell-free conditioned medium (CM). In CM derived from CD34+ cells of diabetic individuals (diabetic-CM), the levels of stem cell factor, hepatocyte growth factor, and thrombopoietin were lower, and IL-1β and tumor necrosis factor (TNFα) levels were higher than CM derived from nondiabetic individuals (nondiabetic-CM). Hypoxia did not upregulate HIF1α in CD34+ cells of diabetic origin. Migration and proliferation of nondiabetic CD34+ cells toward diabetic-CM were lower compared to nondiabetic-CM. Attenuation of pressure-induced constriction, potentiation of bradykinin relaxation, and generation of cGMP and cAMP in arterioles were observed with nondiabetic-CM, but not with diabetic-CM. Diabetic-CM failed to induce endothelial tube formation from vascular tissue. These results suggest that diabetic subjects with microvascular complications exhibit severely limited capacity to generate ex-vivo expanded endothelial progenitor populations and that the vasoreparative dysfunction observed in diabetic CD34+ cells is due to impaired autocrine/paracrine function and reduced sensitivity to hypoxia.
format Article
id doaj-art-e7f09b25d3ea4ccbb11862b45c54bae8
institution DOAJ
issn 1932-6203
language English
publishDate 2014-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-e7f09b25d3ea4ccbb11862b45c54bae82025-08-20T03:00:35ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0194e9396510.1371/journal.pone.0093965Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms.Yagna P R JarajapuSugata HazraMark SegalSergio Li CalziChandra JadhaoKevin QianSayak K MitterMohan K RaizadaMichael E BoultonMaria B GrantWe hypothesized that endothelial progenitor cells derived from individuals with diabetes would exhibit functional defects including inability to respond to hypoxia and altered paracrine/autocrine function that would impair the angiogenic potential of these cells. Circulating mononuclear cells isolated from diabetic (n = 69) and nondiabetic (n = 46) individuals were used to grow endothelial colony forming cells (ECFC), early endothelial progenitor cells (eEPCs) and isolate CD34+ cells. ECFCs and eEPCs were established from only 15% of the diabetic individuals tested thus directing our main effort toward examination of CD34+ cells. CD34+ cells were plated in basal medium to obtain cell-free conditioned medium (CM). In CM derived from CD34+ cells of diabetic individuals (diabetic-CM), the levels of stem cell factor, hepatocyte growth factor, and thrombopoietin were lower, and IL-1β and tumor necrosis factor (TNFα) levels were higher than CM derived from nondiabetic individuals (nondiabetic-CM). Hypoxia did not upregulate HIF1α in CD34+ cells of diabetic origin. Migration and proliferation of nondiabetic CD34+ cells toward diabetic-CM were lower compared to nondiabetic-CM. Attenuation of pressure-induced constriction, potentiation of bradykinin relaxation, and generation of cGMP and cAMP in arterioles were observed with nondiabetic-CM, but not with diabetic-CM. Diabetic-CM failed to induce endothelial tube formation from vascular tissue. These results suggest that diabetic subjects with microvascular complications exhibit severely limited capacity to generate ex-vivo expanded endothelial progenitor populations and that the vasoreparative dysfunction observed in diabetic CD34+ cells is due to impaired autocrine/paracrine function and reduced sensitivity to hypoxia.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0093965&type=printable
spellingShingle Yagna P R Jarajapu
Sugata Hazra
Mark Segal
Sergio Li Calzi
Chandra Jadhao
Kevin Qian
Sayak K Mitter
Mohan K Raizada
Michael E Boulton
Maria B Grant
Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms.
PLoS ONE
title Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms.
title_full Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms.
title_fullStr Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms.
title_full_unstemmed Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms.
title_short Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms.
title_sort vasoreparative dysfunction of cd34 cells in diabetic individuals involves hypoxic desensitization and impaired autocrine paracrine mechanisms
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0093965&type=printable
work_keys_str_mv AT yagnaprjarajapu vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT sugatahazra vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT marksegal vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT sergiolicalzi vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT chandrajadhao vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT kevinqian vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT sayakkmitter vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT mohankraizada vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT michaeleboulton vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms
AT mariabgrant vasoreparativedysfunctionofcd34cellsindiabeticindividualsinvolveshypoxicdesensitizationandimpairedautocrineparacrinemechanisms