Growth factors/chemokines in diabetic vitreous and aqueous alter the function of bone marrow-derived progenitor (CD34⁺) cells in humans

Am J Physiol Endocrinol Metab. 2014 Oct 15;307(8):E695-702. doi: 10.1152/ajpendo.00253.2014. Epub 2014 Aug 26.

Abstract

Ocular ischemic microenvironment plays a critical role in the progression of diabetic retinopathy (DR). In this study, we investigated the effect of vitreous and aqueous obtained from proliferative DR patients on the function of CD34⁺ cells derived from healthy humans. Human CD34⁺ cells were incubated with vitreous or aqueous of subjects with PDR. After incubation, cell migration of CD34⁺ was evaluated with CXCL12. Intracellular levels of nitric oxide (NO) were measured with DAF-FM. Tube formation assay was used to evaluate the effect of treated CD34⁺ cells on in vitro angiogenesis. Angiogenic protein array and mass spectrometry (MS) were performed to ascertain the factors secreted by healthy nondiabetic CD34⁺ cells exposed to diabetic vitreous or aqueous. PDR vitreous/aqueous reduced migration of CD34⁺ cells (672.45 ± 42.1/736.75 ± 101.7 AFU; P < 0.01) and attenuated intracellular NO levels (182 ± 1.4/184.5 ± 6.3 AFU, P = 0.002). Pretreatment with PDR vitreous suppressed tube formation of human retinal endothelial cells (64 ± 1.6 vs. 80 ± 2.5). CD34⁺ exposed to PDR vitreous resulted in the increased expression of CXCL4 and serpin F1, whereas CD34⁺ exposed to PDR aqueous showed increased expression of CXCL4, serpin F1, and endothelin-1 (ET-1). MS analysis of CD34⁺ (exposed to PDR vitreous) expressed J56 gene segment, isoform 2 of SPARC-related modular calcium-binding protein 2, isoform 1 of uncharacterized protein c1 orf167, integrin α-M, and 40s ribosomal protein s21. Exposure of healthy nondiabetic CD34⁺ cells to PDR vitreous and aqueous resulted in decreased migration, reduced generation of NO, and altered paracrine secretory function. Our results suggest that the contribution of CD34⁺ cells to the aberrant neovascularization observed in PDR is driven more by the proangiogenic effects of the retinal cells rather than the influence of the vitreous.

Keywords: CD34+; aqueous; progenitor cells; proliferative diabetic retinopathy; vitreous.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Adult Stem Cells / cytology
  • Adult Stem Cells / immunology
  • Adult Stem Cells / metabolism
  • Adult Stem Cells / pathology
  • Aged
  • Antigens, CD34 / metabolism
  • Aqueous Humor / immunology
  • Aqueous Humor / metabolism*
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / metabolism
  • Bone Marrow Cells / pathology
  • Cells, Cultured
  • Chemotaxis
  • Diabetic Retinopathy / immunology
  • Diabetic Retinopathy / metabolism*
  • Diabetic Retinopathy / pathology
  • Endothelin-1 / agonists
  • Endothelin-1 / chemistry
  • Endothelin-1 / metabolism*
  • Eye Proteins / agonists
  • Eye Proteins / chemistry
  • Eye Proteins / metabolism*
  • Humans
  • Middle Aged
  • Neovascularization, Pathologic / immunology
  • Neovascularization, Pathologic / metabolism
  • Neovascularization, Pathologic / pathology
  • Nerve Growth Factors / agonists
  • Nerve Growth Factors / chemistry
  • Nerve Growth Factors / metabolism*
  • Nitric Oxide / metabolism
  • Peptide Mapping
  • Platelet Factor 4 / agonists
  • Platelet Factor 4 / chemistry
  • Platelet Factor 4 / metabolism*
  • Retina / immunology
  • Retina / metabolism
  • Retina / pathology
  • Serpins / agonists
  • Serpins / chemistry
  • Serpins / metabolism*
  • Vitreoretinopathy, Proliferative / immunology
  • Vitreoretinopathy, Proliferative / metabolism*
  • Vitreoretinopathy, Proliferative / pathology
  • Vitreous Body / immunology
  • Vitreous Body / metabolism*

Substances

  • Antigens, CD34
  • Endothelin-1
  • Eye Proteins
  • Nerve Growth Factors
  • PF4V1 protein, human
  • Serpins
  • pigment epithelium-derived factor
  • Nitric Oxide
  • Platelet Factor 4