Concise review: Diabetes, the bone marrow niche, and impaired vascular regeneration

Stem Cells Translational Medicine

Volumn 3, Issue 8, 2014, Pages 949-957

  Fadini, Gian Paolo ^a,b   Ferraro, Francesca ^c,d   Quaini, Federico ^e   Asahara, Takayuki ^f   Madeddu, Paolo ^g  

^a UNIVERSITY OF PADOVA   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c PENNSYLVANIA HOSPITAL   (United States)

^d FOX CHASE CANCER CENTER   (United States)

^e UNIVERSITY OF PARMA   (Italy)

^f TOKAI UNIVERSITY   (Japan)

^g UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Complications; Regeneration; Stem cells

Indexed keywords

CD146 ANTIGEN; CD34 ANTIGEN; DECAPENTAPLEGIC PROTEIN; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE COLONY STIMULATING FACTOR RECEPTOR; HERMES ANTIGEN; SIALOADHESIN; STEM CELL FACTOR; STROMAL CELL DERIVED FACTOR 1; STROMAL CELL DERIVED FACTOR 1ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ADULTHOOD; ARTICLE; BONE MARROW DEPRESSION; BONE MARROW DISEASE; CYTOSKELETON; DIABETES MELLITUS; DIABETIC MICROANGIOPATHY; ENDOTHELIAL PROGENITOR CELL; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HISTOPATHOLOGY; HOMEOSTASIS; HUMAN; HYPERGLYCEMIA; MULTIPLE ORGAN FAILURE; NEUROPATHY; PHENOTYPE; STEM CELL MOBILIZATION; SYMPATHETIC TONE; VASCULAR DISEASE;

COMPLICATIONS; REGENERATION; STEM CELLS;

ANIMALS; BLOOD GLUCOSE; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; DIABETIC ANGIOPATHIES; DIABETIC NEUROPATHIES; ENDOTHELIAL CELLS; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; NEURAL STEM CELLS; STEM CELL NICHE; STEM CELLS;

EID: 84905509926     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2014-0052     Document Type: Article

References (75)

1. Seshasai SR, Kaptoge S, Thompson A et al. Diabetes mellitus, fasting glucose, and risk of cause-specific death. N Engl J Med 2011;364: 829-841.
2. Brownlee M. The pathobiology of diabetic complications: A unifying mechanism. Diabetes 2005;54:1615-1625.
3. Asahara T, Murohara T, Sullivan A et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-967.
4. Fadini GP, Avogaro A. It is all in the blood: The multifaceted contribution of circulating progenitor cells in diabetic complications. Exp Diabetes Res 2012;2012:742976.
5. Fadini GP. An underlying principle for the study of circulating progenitor cells in diabetes and its complications. Diabetologia 2008;51: 1091-1094.
6. Fadini GP. A reappraisal on the role of circulating (progenitor) cells in the pathobiology of diabetic complications. Diabetologia 2014; 57:4-15.
7. Lo Celso C, Fleming HE, Wu JW et al. Liveanimal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 2009;457:92-96.
8. Haylock DN, Williams B, JohnstonHMet al. Hemopoietic stem cells with higher hemopoietic potential reside at the bone marrow endosteum. STEM CELLS 2007;25:1062-1069.
9. Köhler A, Schmithorst V, Filippi MD et al. Altered cellular dynamics and endosteal location of aged early hematopoietic progenitor cells revealed by time-lapse intravital imaging in long bones. Blood 2009;114:290-298.
10. Arai F, Hirao A, Ohmura M et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004;118:149-161.
11. 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.
12. Taichman RS, Reilly MJ, Emerson SG. Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood 1996;87:518-524.
13. Semerad CL, Christopher MJ, Liu F et al. G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 2005;106:3020-3027.
14. Christopher MJ, Rao M, Liu F et al. Expression of the G-CSF receptor in monocytic cells is sufficient to mediate hematopoietic progenitor mobilization by G-CSF in mice. J Exp Med 2011; 208:251-260.
15. Winkler IG, Sims NA, Pettit AR et al. Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 2010;116:4815-4828.
16. Chow A, Lucas D, Hidalgo A et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med 2011;208:261-271.
17. Li W, Johnson SA, Shelley WC et al. Hematopoietic stem cell repopulating ability can be maintained in vitro by some primary endothelial cells. Exp Hematol 2004;32:1226-1237.
18. Ding L, Saunders TL, Enikolopov G et al. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012;481: 457-462.
19. Sipkins DA, Wei X, Wu J W et al. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 2005;435:969-973.
20. Narayan K, Juneja S, Garcia C. Effects of 5- fluorouracil or total-body irradiation on murine bone marrow microvasculature. Exp Hematol 1994;22:142-148.
21. Winkler IG, Barbier V, Wadley R et al. Positioning of bone marrow hematopoietic and stromal cells relative to blood flow in vivo: Serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches. Blood 2010; 116:375-385.
22. Sacchetti P, Sousa KM, Hall AC et al. Liver X receptors and oxysterols promote ventral midbrain neurogenesis in vivo and in human embryonic stem cells. Cell Stem Cell 2009;5: 409-419.
23. Sugiyama T, Kohara H, Noda M et al. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006;25:977-988.
24. Omatsu Y, Sugiyama T, Kohara H et al. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 2010;33:387-399.
25. Méndez-Ferrer S, Michurina TV, Ferraro F et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010;466:829-834.
26. Mvndez-Ferrer S, Lucas D, Battista M et al. Haematopoietic stem cell release is regulated by circadian oscillations. Nature 2008; 452:442-447.
27. Lucas D, Battista M, Shi PA et al. Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell 2008;3:364-366.
28. Spiegel A, Shivtiel S, Kalinkovich A et al. Catecholaminergic neurotransmitters regulate migration and repopulation of immature human CD34+ cells through Wnt signaling. Nat Immunol 2007;8:1123-1131.
29. Zhang J, Niu C, Ye L et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003;425:836-841.
30. Oikawa A, Siragusa M, Quaini F et al. Diabetes mellitus induces bone marrow microangiopathy. Arterioscler Thromb Vasc Biol 2010; 30:498-508.
31. Hazra S, Jarajapu YP, Stepps V et al. Longterm type 1 diabetes influences haematopoietic stem cells by reducing vascular repair potential and increasing inflammatory monocyte generation in a murine model. Diabetologia 2013;56: 644-653.
32. Mangialardi G, Katare R, Oikawa A et al. Diabetes causes bone marrow endothelial barrier dysfunction by activation of the RhoARho- associated kinase signaling pathway. Arterioscler Thromb Vasc Biol 2013;33:555-564.
33. Fadini GP, Albiero M, Seeger F et al. Stem cell compartmentalization in diabetes and high cardiovascular risk reveals the role of DPP-4 in diabetic stem cell mobilopathy. Basic Res Cardiol 2013;108:313.
34. Spinetti G, Cordella D, Fortunato O et al. Global remodeling of the vascular stem cell niche in bone marrow of diabetic patients: Implication of the microRNA-155/FOXO3a signaling pathway. Circ Res 2013;112:510-522.
35. Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res 2007;100:174-190.
36. Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 2007;100:158-173.
37. Busik JV, Tikhonenko M, Bhatwadekar A et al. Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock. J Exp Med 2009;206:2897-2906.
38. Albiero M, Poncina N, Tjwa M et al. Diabetes causes bone marrow autonomic neuropathy and impairs stem cell mobilization via dysregulated p66Shc and Sirt1. Diabetes 2014; 63:1353-1365.
39. Naveiras O, Nardi V, Wenzel PL et al. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 2009;460:259-263.
40. Fadini GP, Sartore S, Schiavon M et al. Diabetes impairs progenitor cell mobilisation after hindlimb ischaemia-reperfusion injury in rats. Diabetologia 2006;49:3075-3084.
41. Fadini GP, Avogaro A. Dipeptidyl peptidase-4 inhibition and vascular repair by mobilization of endogenous stem cells in diabetes and beyond. Atherosclerosis 2013;229: 23-29.
42. Fadini GP, Albiero M, Vigili de Kreutzenberg S et al. Diabetes impairs stem cell and proangiogenic cell mobilization in humans. Diabetes Care 2013;36:943-949.
43. Fadini GP, Avogaro A. Diabetes impairs mobilization of stem cells for the treatment of cardiovascular disease: A meta-regression analysis. Int J Cardiol 2013;168:892-897.
44. Ling L, Shen Y, Wang K et al. Worseclinical outcomes in acute myocardial infarction patients with type 2 diabetes mellitus: Relevance to impaired endothelial progenitor cells mobilization. PLoS One 2012;7:e50739.
45. DiPersio JF. Diabetic stem-cell "mobilopathy" N Engl J Med 2011;365:2536-2538.
46. Orlandi A, Chavakis E, Seeger F et al. Long-term diabetes impairs repopulation of hematopoietic progenitor cells and dysregulates the cytokine expression in the bone marrow microenvironment in mice. Basic Res Cardiol 2010; 105:703-712.
47. Chiba H, Ataka K, Iba K et al. Diabetes impairs the interactions between long-term hematopoietic stem cells and osteopontinpositive cells in the endosteal niche of mouse bone marrow. Am J Physiol Cell Physiol 2013; 305:C693-C703.
48. Christopherson KW 2nd., Cooper S, Broxmeyer HE. Cell surface peptidase CD26/DPPIV mediates G-CSF mobilization of mouse progenitor cells. Blood 2003;101:4680-4686.
49. Westerweel PE, Teraa M, Rafii S et al. Impaired endothelial progenitor cell mobilization and dysfunctional bone marrow stroma in diabetes mellitus. PLoS One 2013;8:e60357.
50. Fadini GP, de Kreutzenberg SV, Boscaro E et al. An unbalanced monocyte polarisation in peripheral blood and bone marrow of patients with type 2 diabetes has an impact on microangiopathy. Diabetologia 2013;56:1856-1866.
51. Nagareddy PR, Murphy AJ, Stirzaker RA et al. Hyperglycemia promotes myelopoiesis and impairs the resolution of atherosclerosis. Cell Metab 2013;17:695-708.
52. Hoggatt J, Mohammad KS, Singh P et al. Differential stem- and progenitor-cell trafficking by prostaglandin E2. Nature 2013;495: 365-369.
53. 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.
54. Fadini GP, Losordo D, Dimmeler S. Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 2012;110:624-637.
55. Dieterlen-Lièvre F, Jaffredo T. Decoding the hemogenic endothelium in mammals. Cell Stem Cell 2009;4:189-190.
56. Timmermans F, Plum J, Yvder MC et al. Endothelial progenitor cells: Identity defined? J Cell Mol Med 2009;13:87-102.
57. Masuda H, Alev C, Akimaru H et al. Methodological development of a clonogenic assay to determine endothelial progenitor cell potential. Circ Res 2011;109:20-37.
58. Bailey AS, Willenbring H, Jiang S et al. Myeloid lineage progenitors give rise to vascular endothelium. Proc Natl Acad Sci USA 2006; 103:13156-13161.
59. Mantovani A, Garlanda C, Locati M. Macrophage diversity and polarization in atherosclerosis: A question of balance. Arterioscler Thromb Vasc Biol 2009;29:1419-1423.
60. Jetten N, Verbruggen S, Gijbels MJ et al. Anti-inflammatory M2, but not pro-inflammatory M1macrophages promote angiogenesis in vivo. Angiogenesis 2014;17:109-118.
61. Dutta P, Courties G, Wei Y et al. Myocardial infarction accelerates atherosclerosis. Nature 2012;487:325-329.
62. Borissoff JI, Joosen IA, Versteylen MO et al. Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol 2013;33:2032-2040.
63. Abaci A, Ǒguzhan A, Kahraman S et al. Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 1999;99: 2239-2242.
64. Avogaro A, Albiero M, Menegazzo L et al. Endothelial dysfunction in diabetes: The role of reparatory mechanisms. Diabetes Care 2011;34 (Suppl 2):S285-S290.
65. Schatteman GC, Hanlon HD, Jiao C et al. Blood-derived angioblasts accelerate bloodflow restoration in diabetic mice. J Clin Invest 2000;106:571-578.
66. Tepper OM, Galiano RD, Capla JM et al. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 2002;106:2781-2786.
67. Tepper OM, Capla JM, Galiano RD et al. Adult vasculogenesis occurs through in situ recruitment, proliferation, and tubulization of circulating bone marrow-derived cells. Blood 2005;105:1068-1077.
68. Bento CF, Pereira P. Regulation of hypoxia-inducible factor 1 and the loss of the cellular response to hypoxia in diabetes. Diabetologia 2011;54:1946-1956.
69. Albiero M, Menegazzo L, Boscaro E et al. Defective recruitment, survival and proliferation of bone marrow-derived progenitor cells at sites of delayed diabetic wound healing in mice. Diabetologia 2011;54:945-953.
70. Asahara T, Kawamoto A, Masuda H. Concise review: Circulating endothelial progenitor cells for vascular medicine. STEM CELLS 2011; 29:1650-1655.
71. Clifford DM, Fisher SA, Brunskill SJ et al. Stem cell treatment for acute myocardial infarction. Cochrane Database Syst Rev 2012;2: CD006536.
72. Fadini GP, Agostini C, Avogaro A. Autologous stem cell therapy for peripheral arterial disease meta-analysis and systematic review of the literature. Atherosclerosis 2010;209: 10-17.
73. Tanaka R, Masuda H, Kato S et al. Autologous G-CSFmobilized peripheral blood CD34(+) cell therapy for diabetic patients with chronic non-healing ulcer. Cell Transplant 2012;168: 892-897.
74. Tanaka R, Vaynrub M, Masuda H et al. Quality-control culture system restores diabetic endothelial progenitor cell vasculogenesis and accelerates wound closure. Diabetes 2013;62: 3207-3217.
75. Fadini GP, de Kreutzenberg SV, Mariano V et al. Optimized glycaemic control achieved with add-on basal insulin therapy improves indexes of endothelial damage and regeneration in type 2 diabetic patients with macroangiopathy: A randomized crossover trial comparing detemir versus glargine. Diabetes Obes Metab 2011;13:718-725