Reduced endothelial progenitor cell number and function in inflammatory bowel disease: A possible link to the pathogenesis

American Journal of Gastroenterology

Volumn 104, Issue 10, 2009, Pages 2500-2507

  Garolla, Andrea ^a   Dinc, Renata ^a   Checchin, Davide ^a   Biagioli, Andrea ^a   De Toni, Luca ^a   Nicoletti, Valentina ^a   Scarpa, Marco ^b   Bolzonello, Elisa ^a,c   Sturniolo, Giacomo Carlo ^a   Foresta, Carlo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; CHEMOKINE RECEPTOR CXCR4; FOLLITROPIN; LUTEINIZING HORMONE; MESALAZINE; TESTOSTERONE; CXCR4 PROTEIN, HUMAN;

ADULT; ANTIGEN DETECTION; ANTIGEN EXPRESSION; APOPTOSIS; ARTERY BLOOD FLOW; ARTERY DILATATION; ARTICLE; BRACHIAL ARTERY; CELL COUNT; CELL FUNCTION; COLONY FORMING UNIT; CONTROLLED STUDY; CROHN DISEASE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENDOTHELIUM PROGENITOR CELL; FOLLITROPIN BLOOD LEVEL; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IN VITRO STUDY; LUTEINIZING HORMONE BLOOD LEVEL; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; STEM CELL; TESTOSTERONE BLOOD LEVEL; ULCERATIVE COLITIS; ANALYSIS OF VARIANCE; BLOOD FLOW VELOCITY; CASE CONTROL STUDY; ENTERITIS; FLOW CYTOMETRY; METABOLISM; NONPARAMETRIC TEST; PATHOLOGY; PHYSIOLOGY; RISK FACTOR;

ADULT; ANALYSIS OF VARIANCE; APOPTOSIS; BLOOD FLOW VELOCITY; BRACHIAL ARTERY; CASE-CONTROL STUDIES; CELL COUNT; ENDOTHELIAL CELLS; FLOW CYTOMETRY; FOLLICLE STIMULATING HORMONE; HUMANS; INFLAMMATORY BOWEL DISEASES; LUTEINIZING HORMONE; MALE; RECEPTORS, CXCR4; RISK FACTORS; STATISTICS, NONPARAMETRIC; STEM CELLS; TESTOSTERONE;

EID: 70350513001     PISSN: 00029270     EISSN: 15720241     Source Type: Journal    
DOI: 10.1038/ajg.2009.332     Document Type: Article

References (65)

1. Hatoum OA, Binion DG, Otterson MF et al. Acquired microvascular dysfunction in inflammatory bowel disease: loss of nitric oxide-mediated vasodilation. Gastroenterology 2003; 125:58-69
2. Hatoum OA, Gauthier KM, Binion DG et al. Novel mechanism of vasodilation in inflammatory bowel disease. Arterioscler Thromb Vasc Biol 2005; 25:2355-2361
3. Palatka K, Serfozo Z, Vereb Z et al. Effect of IBD sera on expression of inducible and endothelial nitric oxide synthase in human umbilical vein endothelial cells. World J Gastroenterol 2006; 12:1730-1738
4. Majno G. Chronic inflammation: links with angiogenesis and wound healing. Am J Pathol 1998; 153:1035-1039
5. Bagli E, Xagorari A, Papetropoulos A et al. Angiogenesis in inflammation. Autoimmun Rev 2004; 3 (Suppl 1):S26
6. Papa A, Santoliquido A, Danese S et al. Increased carotid intima-media thickness in patients with inflammatory bowel disease. Aliment Pharmacolther 2005; 22:839-846
7. Kocaman O, Sahin T, Aygun C et al. Endothelial dysfunction in patients with ulcerative colitis. Inflamm Bowel Dis 2006; 12:166-171
8. Nuutinen H, Reunanen M, Farkkila M et al. Association of ulcerative colitis and ischemic heart disease. Gastroenterology 1995; 108:A886
9. Nuutinen H, Reunanem M, Farkkila M et al. Association of Crohn's disease and ischemic heart disease. Gastroenterology 1996; 110:A981
10. Mutlu B, Ermeydan CM, Enc F et al. Acute myocardial infarction in a young woman with severe ulcerative colitis. Int J Cardiol 2002; 83:183-185
11. Grip O, Svensson PJ, Lindgren S. Inflammatory bowel disease promotes venous thrombosis earlier in life. Scand J Gastroenterol 2000; 35:619-623
12. Bernstein CN, Blanchard JF, Houston DS et al. The incidence of deep venous thrombosis and pulmonary embolism among patients with inflammatory bowel disease: a population-based cohort study. Thromb Haemost 2001; 85:430-434
13. Novacek G, Haumer M, Schima W et al. Aortic mural thrombi in patients with inflammatory bowel disease: report of two cases and review of the literature. Inflamm Bowel Dis 2004; 10:430-435
14. Miehsler W, Reinisch W, Valic E et al. Is inflammatory bowel disease an independent and disease specific risk factor for thromboembolism? Gut 2004; 53:542-548
15. Asahara T, Isner JM. Endothelial progenitor cells for vascular regeneration. J Hematother Stem Cell Res 2002; 11:171-178
16. Dimmeler S, Zeiher AM. Vascular repair by circulating endothelial progenitor cells: the missing link in atherosclerosis? J Mol Med 2004; 82:671-677
17. Garmy-Susini B, Varner JA. Circulating endothelial progenitor cells. Br J Cancer 2005; 93:855-888
18. Asahara T, Murohara T, Sullivan A et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275:964-967
19. Werner N, Kosiol S, Schiegl T et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005; 353:999-1007 (Pubitemid 41262334)
20. Loomans CJ, de Koning EJ, Staal FJ et al. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 2004; 53:195-199
21. Foresta C, Caretta N, Lana A et al. Circulating endothelial progenitor cells in subjects with rectile dysfunction. Int J Impot Res 2005; 17:288-290
22. Hill JM, Zalos G, Halcox JP et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 2003; 348:593-600
23. Vasa M, Fichtlscherer S, Aicher A et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 2001; 89:E1-7
24. Liew A, Barry F, O'Brien T. Endothelial progenitor cells: diagnostic and therapeutic considerations. Bioessays 2006; 28:261-270
25. Werner N, Nickenig G. Influence of cardiovascular risk factors on endothelial progenitor cells: limitations for therapy? Arterioscler Thromb Vasc Biol 2006; 26:257-266
26. Verma S, Anderson TJ. Fundamentals of endothelial function for the clinical cardiologist. Circulation 2002; 105:546-549 (Pubitemid 34123425)
27. Masuda J, Mitsuyama K, Yamasaki H et al. Depletion of endothelial progenitor cells in the peripheral blood of patients with ulcerative colitis. Int J Mol Med 2007; 19:221-228
28. Haubitz M, Woywodt A. Circulating endothelial cells and vasculitis. Intern Med 2004; 43:660-667
29. Shintani S, Murohara T, Ikeda H et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 2001; 103:2776-2779
30. Nakatani K, Takeshita S, Tsujimoto H et al. Circulating endothelial cells in Kawasaki disease. Clin Exp Immunol 2003; 13:536-540
31. Iwaguro H, Yamaguchi J, Kalka C et al. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 2002; 105:732-738
32. Plate KH, Breier G, Weich HA et al. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992; 359:845-848
33. Di Sabatino A, Ciccocioppo R, Armellini E et al. bFGF and VEGF correlate respectively with bowel wall thickness andintramural blood flow in Crohn's disease. Inflamm Bowel Dis 2004; 10:573-577
34. Kanazawa S, Tsunoda T, Onuma E et al. VEGF, basic-FGF and TGF-beta in Crohn's disease and ulcerative colitis: a novel mechanism of chronic intestinal inflammation. Am J Gastroenterol 2001; 96:822-828
35. Ferrante M, Pierik M, Henckaerts L et al. The role of vascular endothelial growth factor (VEGF) in inflammatory bowel disease. Inflamm Bowel Dis 2006; 12:870-878
36. Lima e Silva R, Shen J, Hackett SF et al. The SDF-1/CXCR4 ligand/receptor pair is an important contributor to several types of ocular neovascularization. FASEB J 2007; 21:3219-3230 (Pubitemid 47565540)
37. Velazquez OC. Angiogenesis and vasculogenesis: inducing the growth of new blood vessels and wound healing by stimulation of bone marrow-derived progenitor cell mobilization and homing. J Vasc Surg 2007; 45:A39-47
38. Ma Q, Jones D, Springer TA. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 1999; 10:463-471
39. Majka M, Ratajczak J, Kowalska MA et al. Binding of stromal derived factor-1alpha (SDF-1alpha) to CXCR4 chemokine receptor in normal human megakaryoblasts but not in platelets induces phosphorylation of mitogen-activated protein kinase p42/44 (MAPK), ELK-1 transcription factor and serine/threonine kinase AKT. Eur J Haematol 2000; 64:164-172
40. Foresta C, Caretta N, Lana A et al. Reduced number of circulating endothelial progenitor cells in hypogonadal men. J Clin Endocrinol Metab 2006; 91:4599-4602
41. Szathmari M, Vasarhelyi B, Treszl A et al. Association of dehydroepiandrosterone sulfate and testosterone deficiency with bone turnover in men with inflammatory bowel disease. Int J Colorectal Dis 2002; 17:63-66
42. Foresta C, Zuccarello D, Biagioli A et al. Oestrogen stimulates endothelial progenitor cells via oestrogen receptor-alpha. Clin Endocrinol 2007; 67:520-525
43. Kusuyama T, Omura T, Nishiya D et al. The Effects of HMG-CoA reductase inhibitor on vascular progenitor cells. J Pharmacol Sci 2006; 101:344-349 (Pubitemid 44285183)
44. Urbich C, Dimmeler S. Risk factors for coronary artery disease, circulating endothelial progenitor cells, and the role of HMG-CoA reductase inhibitors. Kidney Int 2005; 67:1672-1676
45. Ablin JN, Boguslavski V, Aloush V et al. Effect of anti-TNFalpha treatment on circulating endothelial progenitor cells (EPCs) in rheumatoid arthritis. Life Sci 2006; 79:2364-2369
46. Foresta C, Ferlin A, De Toni L et al. Circulating endothelial progenitor cells and endothelial function after chronic tadalafil treatment in subjects with rectile dysfunction. Int J Impot Res 2006; 18:484-488
47. Foresta C, Caretta N, Lana A et al. Relationship between vascular damage degrees and endothelial progenitor cells in patients with rectile dysfunction: Effect of vardenafil administration and pde5 expression in the bone marrow. Eur Urol 2007; 51:1411-1417
48. Kane SV, Sandborn WJ, Rufo PA et al. Fecal lactoferrin is a sensitive and specific marker in identifying intestinal inflammation. Am J Gastroenterol 2003; 98:1309-1314
49. Scheubel RJ, Silber RE, Kuss O et al. Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass graft ing. J Am Coll Cardiol 2003; 42:2073-2080
50. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995; 1:27-31
51. Timeus F, Crescenzio N, Doria A et al. Flow cytometric evaluation of circulating CD34+ cell counts and apoptotic rate in children with acquired aplastic anemia and myelodysplasia. Exp Hematol 2005; 33:597-604
52. Schwartzenberg S, Deutsch V, Maysel-Auslender S et al. Circulating apoptotic progenitor cells: a novel biomarker in patients with acute coronary syndromes. Arterioscler Thromb Vasc Biol 2007; 27:e27-31
53. Koopman G, Reutelingsperger CP, Kuijten GA et al. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 1994; 84:1415-1420
54. Martin SJ, Reutelingsperger CP, McGahon AJ et al. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 1995; 182:1545-1556
55. Corretti MC, Anderson TJ, Benjamin EJ et al. International Brachial Artery Reactivity Task Force. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002; 39:257-265
56. Furness SG, McNagny K. Beyond mere markers: functions for CD34 family of sialomucins in hematopoiesis. Immunol Res 2006; 34:13-32
57. Goussetis E, Theodosaki M, Paterakis G et al. A functional hierarchy among the CD34+ hematopoietic cells based on in vitro proliferative and differentiative potential of AC133+CD34(bright) and AC133(dim/)-CD34+ human cord blood cells. J Hematother Stem Cell Res 2000; 9:827-840
58. Peichev M, Naiyer AJ, Pereira D et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000; 95:952-958
59. Moore MA, 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; 938:36-47
60. Suriano R, Chaudhuri D, Johnson RS et al. 17Beta-estradiol mobilizes bone marrow-derived endothelial progenitor cells to tumors. Cancer Res 2008; 68:6038-6042
61. van Hinsbergh VW, Koolwijk P. Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovasc Res 2008; 78:203-212
62. 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 (Pubitemid 29335849)
63. Aicher A, Heeschen C, Mildner-Rihm C et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 2003; 9:1370-1376
64. Kollet O, Petit I, Kahn J et al. Human CD34(+)CXCR4( ? ) sorted cells harbor intracellular CXCR4, which can be functionally expressed and provide NOD/SCID repopulation. Blood 2002; 100:2778-2786
65. Stellos K, Langer H, Daub K et al. Platelet-derived stromal cellderived factor-1 regulates adhesion and promotes differentiation of human CD34+ cells to endothelial progenitor cells. Circulation 2008; 117:206-15.