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MiR-126 Contributes to Human Umbilical Cord Blood Cell-Induced Neurorestorative Effects After Stroke in Type-2 Diabetic Mice

Chen, Jieli, Ning, Ruizhuo, Zacharek, Alex, Cui, Chengcheng, Cui, Xu, Yan, Tao, Venkat, Poornima, Zhang, Yi, Chopp, Michael·2016·Stem Cells

Abstract

Diabetes mellitus (DM) is a high risk factor for stroke and leads to more severe vascular and white-matter injury than stroke in non-DM. We tested the neurorestorative effects of delayed human umbilical cord blood cell (HUCBC) treatment of stroke in type-2 diabetes (T2DM). db/db-T2DM and db/+-non-DM mice were subjected to distal middle cerebral artery occlusion (dMCAo) and were treated 3 days after dMCAo with: (a) non-DM + Phosphate buffered saline (PBS); (b) T2DM + PBS; (c) T2DM + naïve-HUCBC; (d) T2DM + miR-126−/−HUCBC. Functional evaluation, vascular and white-matter changes, neuroinflammation, and miR-126 effects were measured in vivo and in vitro. T2DM mice exhibited significantly decreased serum and brain tissue miR-126 expression compared with non-DM mice. T2DM+HUCBC mice exhibited increased miR-126 expression, increased tight junction protein expression, axon/myelin, vascular density, and M2-macrophage polarization. However, decreased blood-brain barrier leakage, brain hemorrhage, and miR-126 targeted gene vascular cell adhesion molecule-1 and monocyte chemotactic protein 1 expression in the ischemic brain as well as improved functional outcome were present in HUCBC-treated T2DM mice compared with control T2DM mice. MiR-126−/−HUCBC-treatment abolished the benefits of naïve-HUCBC-treatment in T2DM stroke mice. In vitro, knock-in of miR-126 in primary cultured brain endothelial cells (BECs) or treatment of BECs with naïve-HUCBCs significantly increased capillary-like tube formation, and increased axonal outgrowth in primary cultured cortical neurons; whereas treatment of BECs or cortical neurons with miR-126−/−HUCBC attenuated HUCBC-treatment-induced capillary tube formation and axonal outgrowth. Our data suggest delayed HUCBC-treatment of stroke increases vascular/white-matter remodeling and anti-inflammatory effects; MiR-126 may contribute to HUCBC-induced neurorestorative effects in T2DM mice.

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Research works printed but not linked: 55

  1. Mast, 1995, Hypertension and diabetes mellitus as determinants of multiple lacunar infarcts, Stroke, 26, 30, 10.1161/01.STR.26.1.30 · DOI
  2. Li, 1998, Hyperglycemia-exaggerated ischemic brain damage following 30 min of middle cerebral artery occlusion is not due to capillary obstruction, Brain Res, 804, 36, 10.1016/S0006-8993(98)00651-9 · DOI
  3. Capes, 2001, Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: A systematic overview, Stroke, 32, 2426, 10.1161/hs1001.096194 · DOI · Paper page
  4. Ye, 2011, Niaspan reduces high-mobility group box 1/receptor for advanced glycation endproducts after stroke in type-1 diabetic rats, Neuroscience, 190, 339, 10.1016/j.neuroscience.2011.06.004 · DOI
  5. Chen, 2011, White matter damage and the effect of matrix metalloproteinases in type 2 diabetic mice after stroke, Stroke, 42, 445, 10.1161/STROKEAHA.110.596486 · DOI
  6. Savitz, 2011, Stem cell therapy as an emerging paradigm for stroke (STEPS) II, Stroke, 42, 825, 10.1161/STROKEAHA.110.601914 · DOI
  7. Fagan, 1998, Cost-effectiveness of tissue plasminogen activator for acute ischemic stroke. NINDS rt-PA Stroke Study Group, Neurology, 50, 883, 10.1212/WNL.50.4.883 · DOI
  8. Armstead, 2010, Signaling, delivery and age as emerging issues in the benefit/risk ratio outcome of tPA For treatment of CNS ischemic disorders, J Neurochem, 113, 303, 10.1111/j.1471-4159.2010.06613.x · DOI
  9. Grotta, 2008, Stroke program review group: An interim report, Stroke, 39, 1364, 10.1161/STROKEAHA.107.510776 · DOI
  10. Neuhoff, 2007, Proliferation, differentiation, and cytokine secretion of human umbilical cord blood-derived mononuclear cells in vitro, Exp Hematol, 35, 1119, 10.1016/j.exphem.2007.03.019 · DOI
  11. Chen, 2001, Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats, Stroke, 32, 2682, 10.1161/hs1101.098367 · DOI
  12. Yan, 2014, HUCBCs increase angiopoietin 1 and induce neurorestorative effects after stroke in T1DM rats, CNS Neurosci Ther, 20, 935, 10.1111/cns.12307 · DOI
  13. Papadopoulos, 1987, Recombinant human tissue-type plasminogen activator therapy in acute thromboembolic stroke, J Neurosurg, 67, 394, 10.3171/jns.1987.67.3.0394 · DOI
  14. Fan, 2012, A rat model of studying tissue-type plasminogen activator thrombolysis in ischemic stroke with diabetes, Stroke, 43, 567, 10.1161/STROKEAHA.111.635250 · DOI
  15. Chen, 2011, Adverse effects of bone marrow stromal cell treatment of stroke in diabetic rats, Stroke, 42, 3551, 10.1161/STROKEAHA.111.627174 · DOI · Paper page
  16. Rosenzweig, 2013, Age-dependent exacerbation of white matter stroke outcomes: A role for oxidative damage and inflammatory mediators, Stroke, 44, 2579, 10.1161/STROKEAHA.113.001796 · DOI
  17. Zampetaki, 2010, Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes, Circ Res, 107, 810, 10.1161/CIRCRESAHA.110.226357 · DOI · Paper page
  18. Freilich, 2013, Integrated expression profiles of mRNA and miRNA in polarized primary murine microglia, PLoS One, 8, e79416, 10.1371/journal.pone.0079416 · DOI · Paper page
  19. Bai, 2009, Ectopic expression of angiopoietin-1 promotes neuronal differentiation in neural progenitor cells through the Akt pathway, Biochem Biophys Res Commun, 378, 296, 10.1016/j.bbrc.2008.11.052 · DOI
  20. Mocharla, 2013, AngiomiR-126 expression and secretion from circulating CD34(+) and CD14(+) PBMCs: Role for proangiogenic effects and alterations in type 2 diabetics, Blood, 121, 226, 10.1182/blood-2012-01-407106 · DOI
  21. Kuraoka, 2009, Direct experimental occlusion of the distal middle cerebral artery induces high reproducibility of brain ischemia in mice, Exp Anim, 58, 19, 10.1538/expanim.58.19 · DOI
  22. Harris, 2008, MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1, Proc Natl Acad Sci USA, 105, 1516, 10.1073/pnas.0707493105 · DOI
  23. Cui, 2015, Deficiency of brain ATP-binding cassette transporter A-1 exacerbates blood-brain barrier and white matter damage after stroke, Stroke, 46, 827, 10.1161/STROKEAHA.114.007145 · DOI
  24. Farr, 2002, Quantitative and qualitative impairments in skilled reaching in the mouse (Mus musculus) after a focal motor cortex stroke, Stroke, 33, 1869, 10.1161/01.STR.0000020714.48349.4E · DOI
  25. Swanson, 1990, A semiautomated method for measuring brain infarct volume, J Cereb Blood Flow Metab, 10, 290, 10.1038/jcbfm.1990.47 · DOI
  26. Zacharek, 2009, Simvastatin increases notch signaling activity and promotes arteriogenesis after stroke, Stroke, 40, 254, 10.1161/STROKEAHA.108.524116 · DOI · Paper page
  27. Zacharek, 2006, Nitric oxide regulates Angiopoietin1/Tie2 expression after stroke, Neurosci Lett, 404, 28, 10.1016/j.neulet.2006.05.027 · DOI
  28. Chen, 2009, Increasing Ang1/Tie2 expression by simvastatin treatment induces vascular stabilization and neuroblast migration after stroke, J Cell Mol Med, 13, 1348, 10.1111/j.1582-4934.2008.00380.x · DOI
  29. Chen, 2007, Niaspan increases angiogenesis and improves functional recovery after stroke, Ann Neurol, 62, 49, 10.1002/ana.21160 · DOI · Paper page
  30. Taylor, 2005, A microfluidic culture platform for CNS axonal injury, regeneration and transport, Nat Methods, 2, 599, 10.1038/nmeth777 · DOI
  31. Ueno, 2012, Axonal outgrowth and dendritic plasticity in the cortical peri-infarct area after experimental stroke, Stroke, 43, 2221, 10.1161/STROKEAHA.111.646224 · DOI
  32. Aurrand-Lions, 2002, Junctional adhesion molecules and interendothelial junctions, Cells Tissues Organs, 172, 152, 10.1159/000066967 · DOI
  33. Bazzoni, 2004, Endothelial cell-to-cell junctions: Molecular organization and role in vascular homeostasis, Physiol Rev, 84, 869, 10.1152/physrev.00035.2003 · DOI
  34. Alexander, 2002, Extracellular matrix, junctional integrity and matrix metalloproteinase interactions in endothelial permeability regulation, J Anat, 200, 561, 10.1046/j.1469-7580.2002.00057.x · DOI
  35. Taguchi, 2004, Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model, J Clin Invest, 114, 330, 10.1172/JCI200420622 · DOI
  36. Martini, 2007, Hyperglycemia in acute ischemic stroke: A vascular perspective, J Cereb Blood Flow Metab, 27, 435, 10.1038/sj.jcbfm.9600355 · DOI
  37. Cui, 2011, Angiopoietin/Tie2 pathway mediates type 2 diabetes induced vascular damage after cerebral stroke, Neurobiol Dis, 43, 285, 10.1016/j.nbd.2011.04.005 · DOI
  38. S Roriz-Filho, 2009, (Pre)diabetes, brain aging, and cognition, Biochim Biophys Acta, 1792, 432, 10.1016/j.bbadis.2008.12.003 · DOI
  39. Shi, 2010, A long-term observation of olfactory ensheathing cells transplantation to repair white matter and functional recovery in a focal ischemia model in rat, Brain Res, 1317, 257, 10.1016/j.brainres.2009.12.061 · DOI
  40. Hall, 2009, Human umbilical cord blood cells directly suppress ischemic oligodendrocyte cell death, J Neurosci Res, 87, 333, 10.1002/jnr.21857 · DOI
  41. Parsa, 2012, Adoptive transfer of immunomodulatory M2 macrophages prevents type 1 diabetes in NOD mice, Diabetes, 61, 2881, 10.2337/db11-1635 · DOI
  42. Ma, 2015, Adoptive transfer of M2 macrophages promotes locomotor recovery in adult rats after spinal cord injury, Brain Behav Immun, 45, 157, 10.1016/j.bbi.2014.11.007 · DOI
  43. Brifault, 2015, Delayed pituitary adenylate cyclase-activating polypeptide delivery after brain stroke improves functional recovery by inducing m2 microglia/macrophage polarization, Stroke, 46, 520, 10.1161/STROKEAHA.114.006864 · DOI
  44. Wang, 2013, Microglia/macrophage polarization dynamics in white matter after traumatic brain injury, J Cereb Blood Flow Metab, 33, 1864, 10.1038/jcbfm.2013.146 · DOI · Paper page
  45. Sozmen, 2009, A white matter stroke model in the mouse: Axonal damage, progenitor responses and MRI correlates, J Neurosci Methods, 180, 261, 10.1016/j.jneumeth.2009.03.017 · DOI
  46. Meng, 2012, Downregulation of microRNA-126 in endothelial progenitor cells from diabetes patients, impairs their functional properties, via target gene Spred-1, J Mol Cell Cardiol, 53, 64, 10.1016/j.yjmcc.2012.04.003 · DOI
  47. Wang, 2008, The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis, Dev Cell, 15, 261, 10.1016/j.devcel.2008.07.002 · DOI · Paper page
  48. Fish, 2008, miR-126 regulates angiogenic signaling and vascular integrity, Dev Cell, 15, 272, 10.1016/j.devcel.2008.07.008 · DOI · Paper page
  49. Regazzi, 2010, Diabetes mellitus reveals its micro-signature, Circ Res, 107, 686, 10.1161/CIRCRESAHA.110.228841 · DOI
  50. Huang, 2013, Mesenchymal stem cells modified with miR-126 release angiogenic factors and activate Notch ligand Delta-like-4, enhancing ischemic angiogenesis and cell survival, Int J Mol Med, 31, 484, 10.3892/ijmm.2012.1200 · DOI
  51. Liu, 2013, MicroRNAs in immune response and macrophage polarization, Arterioscler Thromb Vasc Biol, 33, 170, 10.1161/ATVBAHA.112.300068 · DOI
  52. Zhang, 2013, miR-126 and miR-126* repress recruitment of mesenchymal stem cells and inflammatory monocytes to inhibit breast cancer metastasis, Nat Cell Biol, 15, 284, 10.1038/ncb2690 · DOI
  53. Arner, 2012, Adipose tissue microRNAs as regulators of CCL2 production in human obesity, Diabetes, 61, 1986, 10.2337/db11-1508 · DOI
  54. Shechter, 2013, Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus, Immunity, 38, 555, 10.1016/j.immuni.2013.02.012 · DOI · Paper page
  55. Sun, 2012, IRF-1 and miRNA126 modulate VCAM-1 expression in response to a high-fat meal, Circ Res, 111, 1054, 10.1161/CIRCRESAHA.112.270314 · DOI

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Metadata

Authors
Chen, J., Ning, R., Zacharek, A., Cui, C., Cui, X., Yan, T., Venkat, P., Zhang, Y., & Chopp, M.
Affiliations
Department of Neurology, Henry Ford Hospital, Detroit, Michigan, USA
Venue
Stem Cells
Published
2016-01-01
Volume
34
Issue
1
Pages
102-113
ISSN
  • 1066-5099
  • 1549-4918
Cited by
58
References
5
Language
en
Funders
  • National Institute on Aging (R01 AG031811, R01 AG 037506)
  • National Institute of Neurological Disorders and Stroke (R01 NS083078-01A1, R01 NS092917-01, R41 NS080329-01A1)
  • American Heart Association (14GRNT20460026, 12SDG9300009)

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