Measurements of CD34+/CD45-dim stem cells predict healing of diabetic neuropathic wounds

Diabetes

Volumn 65, Issue 2, 2016, Pages 486-497

  Thom, Stephen R ^a   Hampton, Michelle ^b   Troiano, Michael A ^c   Mirza, Ziad ^d   Malay, D Scot ^c   Shannon, Steven ^c   Jennato, Nathan B ^c   Donohue, Cornelius M ^e   Hoffstad, Ole ^f   Woltereck, Diana ^d   Yang, Ming ^a   Yu, Kevin ^a   Bhopale, Veena M ^a   Kovtun, Svitlana ^a   Margolis, David J ^b,f  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c PENN PRESBYTERIAN MEDICAL CENTER   (United States)

^d GREATER BALTIMORE MEDICAL CENTER   (United States)

^e Roxborough Memorial Hospital   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CD45 ANTIGEN; HYPOXIA INDUCIBLE FACTOR; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DEBRIDEMENT; DIABETIC NEUROPATHY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE; FOLLOW UP; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PATIENT CARE; PRIORITY JOURNAL; STEM CELL; TREATMENT DURATION; WOUND CARE; WOUND HEALING; ADULT STEM CELL; BLOOD; DIABETIC FOOT; MIDDLE AGED; PREDICTIVE VALUE; STATISTICAL MODEL; TIME FACTOR;

ADULT STEM CELLS; ANTIGENS, CD34; ANTIGENS, CD45; DIABETIC FOOT; DIABETIC NEUROPATHIES; FEMALE; FLOW CYTOMETRY; HUMANS; LOGISTIC MODELS; MALE; MIDDLE AGED; PREDICTIVE VALUE OF TESTS; TIME FACTORS; WOUND HEALING;

EID: 84962431725     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-0517     Document Type: Article

References (54)

1. 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
2. Tepper OM, Carr J, Allen RJ Jr, et al. Decreased circulating progenitor cell number and failed mechanisms of stromal cell-derived factor-1alpha mediated bone marrow mobilization impair diabetic tissue repair. Diabetes 2010; 59: 1974-1983
3. Barcelos LS, Duplaa C, Kränkel N, et al. Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of an-giogenesis and activation of Wnt signaling. Circ Res 2009; 104: 1095-1102
4. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004; 27: 1047-1053
5. Bartus CL, Margolis DJ. Reducing the incidence of foot ulceration and amputation in diabetes. Curr Diab Rep 2004; 4: 413-418
6. Margolis DJ, Gelfand JM, Hoffstad O, Berlin JA. Surrogate end points for the treatment of diabetic neuropathic foot ulcers. Diabetes Care 2003; 26: 1696-1700
7. Albiero M, Avogaro A, Fadini GP. Restoring stem cell mobilization to promote vascular repair in diabetes. Vascul Pharmacol 2013; 58: 253-258
8. Fukaya E, Margolis DJ, Miller CJ, Milovanova TN, Papadopoulos M, Thom SR. Endothelial progenitor cell mobilization following acute wound injury. Wound Repair Regen 2013; 21: 907-908
9. 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
10. Rehman J, Li J, Parvathaneni L, et al. Exercise acutely increases circulating endothelial progenitor cells and monocyte-/macrophage-derived angiogenic cells. J Am Coll Cardiol 2004; 43: 2314-2318
11. Thom SR, Bhopale VM, Velazquez OC, Goldstein LJ, Thom LH, Buerk DG. Stem cell mobilization by hyperbaric oxygen. Am J Physiol Heart Circ Physiol 2006; 290:H1378-H1386
12. Goldstein LJ, Gallagher KA, Bauer SM, et al. Endothelial progenitor cell release into circulation is triggered by hyperoxia-induced increases in bone marrow nitric oxide. Stem Cells 2006; 24: 2309-2318
13. Gallagher KA, Liu ZJ, Xiao M, et al. Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1 alpha. J Clin Invest 2007; 117: 1249-1259
14. Milovanova TN, Bhopale VM, Sorokina EM, et al. Lactate stimulates vasculogenic stem cells via the thioredoxin system and engages an autocrine activation loop involving hypoxia-inducible factor 1. Mol Cell Biol 2008; 28: 6248-6261
15. Thom SR, Milovanova TN, Yang M, et al. Vasculogenic stem cell mobilization and wound recruitment in diabetic patients: increased cell number and intracellular regulatory protein content associated with hyperbaric oxygen therapy. Wound Repair Regen 2011; 19: 149-161
16. Galiano RD, Tepper OM, Pelo CR, et al. Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am J Pathol 2004; 164: 1935-1947
17. Kirana S, Stratmann B, Prante C, et al. Autologous stem cell therapy in the treatment of limb ischaemia induced chronic tissue ulcers of diabetic foot patients. Int J Clin Pract 2012; 66: 384-393
18. Seo SG, Yeo JH, Kim JIH, Kim J-B, Cho T-J, Lee DY. Negative-pressure wound therapy induces endothelial progenitor cell mobilization in diabetic patients with foot infection or skin defects. Exp Mol Med 2013; 45:e62
19. Heyboer M 3rd, Milovanova TN, Wojcik S, et al. CD34+/CD45-dim stem cell mobilization by hyperbaric oxygen - changes with oxygen dosage. Stem Cell Res (Amst) 2014; 12: 638-645
20. Liao YF, Chen LL, Zeng TS, et al. Number of circulating endothelial progenitor cells as a marker of vascular endothelial function for type 2 diabetes. Vasc Med 2010; 15: 279-285
21. Liang C, Ren Y, Tan H, et al. Rosiglitazone via upregulation of Akt/eNOS pathways attenuates dysfunction of endothelial progenitor cells, induced by advanced glycation end products. Br J Pharmacol 2009; 158: 1865-1873
22. 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
23. Lapidot T, Petit I. Current understanding of stem cell mobilization: the roles of chemokines, proteolytic enzymes, adhesion molecules, cytokines, and stromal cells. Exp Hematol 2002; 30: 973-981
24. Fernández A, De Arriba F, Rivera J, Heras I, Vicente V, Lozano ML. Successful mobilization of hematopoietic peripheral blood progenitor cells with paclitaxel-based chemotherapy as initial or salvage regimen in patients with hematologic malignancies. Haematologica 2008; 93: 1436-1438
25. Sorrentino SA, Doerries C, Manes C, et al. Nebivolol exerts beneficial effects on endothelial function, early endothelial progenitor cells, myocardial neo-vascularization, and left ventricular dysfunction early after myocardial infarction beyond conventional β1-blockade. J Am Coll Cardiol 2011; 57: 601-611
26. Chen LL, Liao YF, Zeng TS, Yu F, Li HQ, Feng Y. Effects of metformin plus gliclazide compared with metformin alone on circulating endothelial progenitor cell in type 2 diabetic patients. Endocrine 2010; 38: 266-275
27. Margolis DJ, Hoffstad O, Thom S, et al. The differential effect of angiotensin-converting enzyme inhibitors and angiotensin receptor blockers with respect to foot ulcer and limb amputation in those with diabetes. Wound Repair Regen 2010; 18: 445-451
28. Guo S, Cheng Y, Ma Y, Yang X. Endothelial progenitor cells derived from CD34+ cells form cooperative vascular networks. Cell Physiol Biochem 2010; 26: 679-688
29. Zou H-X, Jia J, Zhang WF, Sun ZJ, Zhao YF. Propranolol inhibits endothelial progenitor cell homing: a possible treatment mechanism of infantile hemangioma. Cardiovasc Pathol 2013; 22: 203-210
30. Xu H, Yang YJ, Yang T, Qian HY. Statins and stem cell modulation. Ageing Res Rev 2013; 12: 1-7
31. Hristov M, Fach C, Becker C, et al. Reduced numbers of circulating endothelial progenitor cells in patients with coronary artery disease associated with long-term statin treatment. Atherosclerosis 2007; 192: 413-420
32. Fuchs M, Scheid C, Schulz A, Diehl V, Söhngen D. Trimethoprim/sulfamethoxazole prophylaxis impairs function of mobilised autologous peripheral blood stem cells. Bone Marrow Transplant 2000; 26: 815-816
33. Tecilazich F, Dinh T, Pradhan-Nabzdyk L, et al. Role of endothelial progenitor cells and inflammatory cytokines in healing of diabetic foot ulcers. PLoS One 2013; 8:e83314
34. Milovanova TN, Bhopale VM, Sorokina EM, et al. Hyperbaric oxygen stimulates vasculogenic stem cell growth and differentiation in vivo. J Appl Physiol (1985) 2009; 106: 711-728
35. Quiroz FG, Posada OM, Gallego-Perez D, et al. Housekeeping gene stability influences the quantification of osteogenic markers during stem cell differentiation to the osteogenic lineage. Cytotechnology 2010; 62: 109-120
36. Li X, Yang Q, Bai J, Xuan Y, Wang Y. Identification of appropriate reference genes for human mesenchymal stem cell analysis by quantitative real-time PCR. Biotechnol Lett 2015; 37: 67-73
37. Mindaye ST, Ra M, Lo Surdo JL, Bauer SR, Alterman MA. Global proteomic signature of undifferentiated human bone marrow stromal cells: evidence for donor-to-donor proteome heterogeneity. Stem Cell Res (Amst) 2013; 11: 793-805
38. Momcilovic O, Knobloch L, Fornsaglio J, Varum S, Easley C, Schatten G. DNA damage responses in human induced pluripotent stem cells and embryonic stem cells. PLoS One 2010; 5:e13410
39. Yoshitake H, Takeda Y, Nitto T, Sendo F. Cross-linking of GPI-80, a possible regulatory molecule of cell adhesion, induces up-regulation of CD11b/CD18 expression on neutrophil surfaces and shedding of L-selectin. J Leukoc Biol 2002; 71: 205-211
40. Maynard MA, Evans AJ, Shi W, Kim WY, Liu F-F, Ohh M. Dominant-negative HIF-3 alpha 4 suppresses VHL-null renal cell carcinoma progression. Cell Cycle 2007; 6: 2810-2816
41. Wang V, Davis DA, Haque M, Huang LE, Yarchoan R. Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res 2005; 65: 3299-3306
42. Pober JS Just the FACS or stalking the elusive circulating endothelial progenitor cell. Arterioscler Thromb Vasc Biol 2012; 32: 837-838
43. Belch JJ, Topol EJ, Agnelli G, et al.; Prevention of Atherothrombotic Disease Network. Critical issues in peripheral arterial disease detection and management: a call to action. Arch Intern Med 2003; 163: 884-892
44. Tung JW, Heydari K, Tirouvanziam R, et al. Modern flow cytometry: a practical approach. Clin Lab Med 2007; 27: 453-468, v
45. Porichis F, Hart MG, Griesbeck M, et al. High-throughput detection of miRNAs and gene-specific mRNA at the single-cell level by flow cytometry. Nat Commun 2014; 5: 5641
46. Laing AJ, Dillon JP, Condon ET, et al. Mobilization of endothelial precursor cells: systemic vascular response to musculoskeletal trauma. J Orthop Res 2007; 25: 44-50
47. Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA. Diabetic neuropathic foot ulcers: the association of wound size, wound duration, and wound grade on healing. Diabetes Care 2002; 25: 1835-1839
48. Howangyin KY, Silvestre JS. Diabetes mellitus and ischemic diseases: molecular mechanisms of vascular repair dysfunction. Arterioscler Thromb Vasc Biol 2014; 34: 1126-1135
49. Yiu KH, Tse HF. Specific role of impaired glucose metabolism and diabetes mellitus in endothelial progenitor cell characteristics and function. Arterioscler Thromb Vasc Biol 2014; 34: 1136-1143
50. Gao W, Ferguson G, Connell P, et al. Glucose attenuates hypoxia-induced changes in endothelial cell growth by inhibiting HIF-1α expression. Diab Vasc Dis Res 2014; 11: 270-280
51. Maxwell PH, Wiesener MS, Chang GW, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399: 271-275
52. Yoo PS, Mulkeen AL, Cha CH. Post-transcriptional regulation of vascular endothelial growth factor: implications for tumor angiogenesis. World J Gastroenterol 2006; 12: 4937-4942
53. Al-Souhibani N, Al-Ghamdi M, Al-Ahmadi W, Khabar KSA Posttranscriptional control of the chemokine receptor CXCR4 expression in cancer cells. Carcinogenesis 2014; 35: 1983-1992
54. Lebrun E, Tomic-Canic M, Kirsner RS. The role of surgical debridement in healing of diabetic foot ulcers. Wound Repair Regen 2010; 18: 433-438