Diabetes impairs mobilization of mouse bone marrow-derived Lin-/VEGF-R2+ progenitor cells

Blood Cells, Molecules, and Diseases

Volumn 51, Issue 3, 2013, Pages 163-173

  Barthelmes, D ^a   Irhimeh, M R ^a   Gillies, M C ^a   Karimipour, M ^a   Zhou, M ^a   Zhu, L ^a   Shen, W Y ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Diabetes; Diabetic retinopathy; Endothelial progenitor cells; Erythropoietin; Granulocyte colony stimulating factor; Stem cell mobilization

Indexed keywords

ERYTHROPOIETIN; GRANULOCYTE COLONY STIMULATING FACTOR; STREPTOZOCIN; TETRAHYDROBIOPTERIN; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ARTICLE; BONE MARROW; CELL ISOLATION; CELL MIGRATION; CELL STRUCTURE; COLONY FORMATION; CONTROLLED STUDY; CULTURE MEDIUM; DIABETES MELLITUS; DIABETIC RETINOPATHY; ENDOTHELIAL PROGENITOR CELL; GRANULOCYTE; HYPERGLYCEMIA; IN VITRO STUDY; INTRAPERITONEAL DRUG ADMINISTRATION; MOUSE; MOUSE STRAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STREPTOZOCIN DIABETES; TISSUE REPAIR;

MUS;

ARVO; ASSOCIATION FOR RESEARCH IN VISION AND OPHTHALMOLOGY; AUSTRALIAN NATIONAL HEALTH AND MEDICAL RESEARCH COUNCIL; BH4; BIOTINYLATED ULEX EUROPAEUS AGGLUTININ I; BLOOD-RETINAL BARRIER; BM; BONE MARROW; BRB; CNTX; CONTROL MICE TREATED WITH THE DRUG COCKTAIL; CONTROL MICE WITHOUT DRUG COCKTAIL TREATMENT; CTX; DIABETES; DIABETIC MICE TREATED WITH THE DRUG COCKTAIL; DIABETIC MICE WITHOUT DRUG COCKTAIL TREATMENT; DIABETIC RETINOPATHY; DNTX; DTX; ENDOTHELIAL PROGENITOR CELLS; EPCS; EPO; ERYTHROPOIETIN; FFA; FUNDUS FLUORESCEIN ANGIOGRAPHY; G-CSF; GRANULOCYTE COLONY-STIMULATING FACTOR; HEMATOPOIETIC LINEAGE MARKERS; I.P; INTRAPERITONEAL; LIN; NHMRC; PB; PERIPHERAL BLOOD; SD; SDF-1; STANDARD DEVIATION; STEM CELL MOBILIZATION; STREPTOZOTOCIN; STROMAL DERIVED FACTOR-1; STZ; TETRAHYDROBIOPTERIN; UEA-I; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR 2; VEGF; VEGF-R2; WBCS; WHITE BLOOD CELLS;

ANIMALS; BLOOD GLUCOSE; BLOOD-RETINAL BARRIER; BODY WEIGHT; BONE MARROW CELLS; DIABETES MELLITUS, EXPERIMENTAL; ERYTHROCYTE INDICES; HEMATOPOIETIC STEM CELL MOBILIZATION; IMMUNOPHENOTYPING; MALE; MICE; PHENOTYPE; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84881026181     PISSN: 10799796     EISSN: 10960961     Source Type: Journal    
DOI: 10.1016/j.bcmd.2013.05.002     Document Type: Article

References (66)

1. Alberti K.G., Zimmet P.Z. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet. Med. 1998, 15:539-553.
2. Danaei G., Friedman A.B., Oza S., Murray C.J., Ezzati M. Diabetes prevalence and diagnosis in US states: analysis of health surveys. Popul. Health Metrics 2009, 7:16.
3. Crofford O.B. Diabetes control and complications. Annu. Rev. Med. 1995, 46:267-279.
4. Fong D.S., Aiello L.P., Ferris F.L., Klein R. Diabetic retinopathy. Diabetes Care 2004, 27:2540-2553.
5. Waltenberger J. Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications. Cardiovasc. Res. 2001, 49:554-560.
6. Asahara T., Murohara T., Sullivan A., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997, 275:964-967.
7. Asahara T., Masuda H., Takahashi T., et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 1999, 85:221-228.
8. Tepper O.M., Galiano R.D., Capla J.M., et al. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 2002, 106:2781-2786.
9. Sekiguchi H., Ii M., Losordo D.W. The relative potency and safety of endothelial progenitor cells and unselected mononuclear cells for recovery from myocardial infarction and ischemia. J. Cell. Physiol. 2009, 219:235-242.
10. Tateishi-Yuyama E., Matsubara H., Murohara T., et al. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 2002, 360:427-435.
11. Jung K.H., Roh J.K. Circulating endothelial progenitor cells in cerebrovascular disease. J. Clin. Neurol. 2008, 4:139-147.
12. Shi Q., Rafii S., Wu M.H., et al. Evidence for circulating bone marrow-derived endothelial cells. Blood 1998, 92:362-367.
13. Ingram D.A., Mead L.E., Moore D.B., et al. Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 2005, 105:2783-2786.
14. Urao N., Okigaki M., Yamada H., et al. Erythropoietin-mobilized endothelial progenitors enhance reendothelialization via Akt-endothelial nitric oxide synthase activation and prevent neointimal hyperplasia. Circ. Res. 2006, 98:1405-1413.
15. Heeschen C., Aicher A., Lehmann R., et al. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 2003, 102:1340-1346.
16. Fadini G.P., Sartore S., Schiavon M., et al. Diabetes impairs progenitor cell mobilisation after hindlimb ischaemia-reperfusion injury in rats. Diabetologia 2006, 49:3075-3084.
17. Thum T., Fraccarollo D., Schultheiss M., et al. Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 2007, 56:666-674.
18. Stroes E., Kastelein J., Cosentino F., et al. Tetrahydrobiopterin restores endothelial function in hypercholesterolemia. J. Clin. Invest. 1997, 99:41-46.
19. Friedrich E.B., Walenta K., Scharlau J., Nickenig G., Werner N. CD34-/CD133+/VEGFR-2+ endothelial progenitor cell subpopulation with potent vasoregenerative capacities. Circ. Res. 2006, 98:e20-e25.
20. Critser P.J., Voytik-Harbin S.L., Yoder M.C. Isolating and defining cells to engineer human blood vessels. Cell Prolif. 2011, 44(Suppl. 1):15-21.
21. Medina R., O'Neill C.L., Humphreys M.W., Gardiner T.A., Stitt A.W. Outgrowth endothelial cells: characterisation and their potential for reversing ischaemic retinopathy. Invest. Ophthalmol. Vis. Sci. 2010, 51:5906-5913.
22. Barber C.L., Iruela-Arispe M.L. The ever-elusive endothelial progenitor cell: identities, functions and clinical implications. Pediatr. Res. 2006, 59:26R-32R.
23. Hirschi K.K., Ingram D.A., Yoder M.C. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1584-1595.
24. Rafii S., Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. 2003, 9:702-712.
25. Case J., Mead L.E., Bessler W.K., et al. Human CD34(+)AC133(+)VEGFR-2(+) cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp. Hematol. 2007, 35:1109-1118.
26. Murasawa S., Asahara T. Endothelial progenitor cells for vasculogenesis. Physiology (Bethesda) 2005, 20:36-42.
27. Ingram D.A., Mead L.E., Tanaka H., et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 2004, 104:2752-2760.
28. Mund J.A., Estes M.L., Yoder M.C., Ingram D.A., Case J. Flow cytometric identification and functional characterization of immature and mature circulating endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2012, 32:1045-1053.
29. Rerup C.C. Drugs producing diabetes through damage of the insulin secreting cells. Pharmacol. Rev. 1970, 22:485-518.
30. Shen W., Li S., Chung S.H., Gillies M.C. Retinal vascular changes after glial disruption in rats. J. Neurosci. Res. 2010, 88:1485-1499.
31. Antonetti D.A., Barber A.J., Khin S., et al. Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content: vascular endothelial growth factor decreases occludin in retinal endothelial cells. Penn State Retina Research Group. Diabetes 1998, 47:1953-1959.
32. Ishida S., Usui T., Yamashiro K., et al. VEGF164 is proinflammatory in the diabetic retina. Invest. Ophthalmol. Vis. Sci. 2003, 44:2155-2162.
33. Barber A.J., Antonetti D.A., Gardner T.W. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes. The Penn State Retina Research Group. Invest. Ophthalmol. Vis. Sci. 2000, 41:3561-3568.
34. Barber A.J., Antonetti D.A., Kern T.S., et al. The Ins2Akita mouse as a model of early retinal complications in diabetes. Invest. Ophthalmol. Vis. Sci. 2005, 46:2210-2218.
35. Feit-Leichman R.A., Kinouchi R., Takeda M., et al. Vascular damage in a mouse model of diabetic retinopathy: relation to neuronal and glial changes. Invest. Ophthalmol. Vis. Sci. 2005, 46:4281-4287.
36. Ribatti D., Presta M., Vacca A., et al. Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood 1999, 93:2627-2636.
37. Mahmud D.L., G-Amlak M., Deb D.K., et al. Phosphorylation of forkhead transcription factors by erythropoietin and stem cell factor prevents acetylation and their interaction with coactivator p300 in erythroid progenitor cells. Oncogene 2002, 21:1556-1562.
38. Hirata A., Minamino T., Asanuma H., et al. Erythropoietin enhances neovascularization of ischemic myocardium and improves left ventricular dysfunction after myocardial infarction in dogs. J. Am. Coll. Cardiol. 2006, 48:176-184.
39. McVicar C.M., Colhoun L.M., Abrahams J.L., et al. Differential modulation of angiogenesis by erythropoiesis-stimulating agents in a mouse model of ischaemic retinopathy. PLoS One 2010, 5:e11870.
40. Ohki Y., Heissig B., Sato Y., et al. Granulocyte colony-stimulating factor promotes neovascularization by releasing vascular endothelial growth factor from neutrophils. FASEB J. 2005, 19:2005-2007.
41. Asahara T., Takahashi T., Masuda H., et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 1999, 18:3964-3972.
42. Hattori K., Dias S., Heissig B., et al. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J. Exp. Med. 2001, 193:1005-1014.
43. Yoshioka T., Takahashi M., Shiba Y., et al. Granulocyte colony-stimulating factor (G-CSF) accelerates reendothelialization and reduces neointimal formation after vascular injury in mice. Cardiovasc. Res. 2006, 70:61-69.
44. Takahashi T., Kalka C., Masuda H., et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat. Med. 1999, 5:434-438.
45. Tiefenbacher C.P. Tetrahydrobiopterin: a critical cofactor for eNOS and a strategy in the treatment of endothelial dysfunction?. Am. J. Physiol. Heart Circ. Physiol. 2001, 280:H2484-H2488.
46. He T., Smith L.A., Lu T., Joyner M.J., Katusic Z.S. Activation of peroxisome proliferator-activated receptor-{delta} enhances regenerative capacity of human endothelial progenitor cells by stimulating biosynthesis of tetrahydrobiopterin. Hypertension 2011, 58:287-294.
47. Heissig B., Hattori K., Dias S., et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002, 109:625-637.
48. Moore M.A., Hattori K., Heissig B., et al. Mobilization of endothelial and hematopoietic stem and progenitor cells by adenovector-mediated elevation of serum levels of SDF-1, VEGF, and angiopoietin-1. Ann. N. Y. Acad. Sci. 2001, 938:36-45. (discussion 45-7).
49. Irhimeh M.R., Fitton J.H., Lowenthal R.M. Fucoidan ingestion increases the expression of CXCR4 on human CD34+ cells. Exp. Hematol. 2007, 35:989-994.
50. Kim J.H., Yu Y.S., Min B.H., Kim K.W. Protective effect of clusterin on blood-retinal barrier breakdown in diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 2010, 51:1659-1665.
51. Su E.N., Alder V.A., Yu D.Y., et al. Continued progression of retinopathy despite spontaneous recovery to normoglycemia in a long-term study of streptozotocin-induced diabetes in rats. Graefes Arch. Clin. Exp. Ophthalmol. 2000, 238:163-173.
52. Klein R., Klein B.E., Moss S.E., Davis M.D., DeMets D.L. The Wisconsin epidemiologic study of diabetic retinopathy. II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30years. Arch. Ophthalmol. 1984, 102:520-526.
53. Fadini G.P., Miorin M., Facco M., et al. Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. J. Am. Coll. Cardiol. 2005, 45:1449-1457.
54. Schmidt-Lucke C., Rossig L., Fichtlscherer S., et al. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 2005, 111:2981-2987.
55. Werner N., Kosiol S., Schiegl T., et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N. Engl. J. Med. 2005, 353:999-1007.
56. Brunner S., Schernthaner G.H., Satler M., et al. Correlation of different circulating endothelial progenitor cells to stages of diabetic retinopathy: first in vivo data. Invest. Ophthalmol. Vis. Sci. 2009, 50:392-398.
57. Lee I.G., Chae S.L., Kim J.C. Involvement of circulating endothelial progenitor cells and vasculogenic factors in the pathogenesis of diabetic retinopathy. Eye 2006, 20:546-552.
58. Loomans C.J., de Koning E.J., Staal F.J., et al. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 2004, 53:195-199.
59. Schatteman G.C., Hanlon H.D., Jiao C., Dodds S.G., Christy B.A. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J. Clin. Invest. 2000, 106:571-578.
60. Nathan D.M., Zinman B., Cleary P.A., et al. Modern-day clinical course of type 1 diabetes mellitus after 30years' duration: the diabetes control and complications trial/epidemiology of diabetes interventions and complications and Pittsburgh epidemiology of diabetes complications experience (1983-2005). Arch. Intern. Med. 2009, 169:1307-1316.
61. Fadini G.P., Boscaro E., de Kreutzenberg S., et al. Time course and mechanisms of circulating progenitor cell reduction in the natural history of type 2 diabetes. Diabetes Care 2010, 33:1097-1102.
62. Negrean M., Stirban A., Stratmann B., et al. Effects of low- and high-advanced glycation endproduct meals on macro- and microvascular endothelial function and oxidative stress in patients with type 2 diabetes mellitus. Am. J. Clin. Nutr. 2007, 85:1236-1243.
63. Chen Q., Dong L., Wang L., Kang L., Xu B. Advanced glycation end products impair function of late endothelial progenitor cells through effects on protein kinase Akt and cyclooxygenase-2. Biochem. Biophys. Res. Commun. 2009, 381:192-197.
64. Ferraro F., Lymperi S., Mendez-Ferrer S., et al. Diabetes impairs hematopoietic stem cell mobilization by altering niche function. Sci. Transl. Med. 2011, 3. (104ra101).
65. Fadini G.P., Albiero M., Vigili de Kreutzenberg S., et al. Diabetes impairs stem cell and proangiogenic cell mobilization in humans. Diabetes Care 2013, 36:943-949.
66. Murata T., Nakagawa K., Khalil A., et al. The relation between expression of vascular endothelial growth factor and breakdown of the blood-retinal barrier in diabetic rat retinas. Lab. Invest. 1996, 74:819-825.