Article: Circulating CD133 +VEGFR2 + and CD34 +VEGFR2 + cells and arterial function in patients with beta-thalassaemia major

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TitleCirculating CD133 +VEGFR2 + and CD34 +VEGFR2 + cells and arterial function in patients with beta-thalassaemia major
AuthorsCheung, YF1
Chan, S1
Yang, M1
Ye, JY1
Ha, SY1
Wong, SJ1
Chan, GCF1
KeywordsMedicine & Public Health
Hematology
Oncology
Issue Date2011
PublisherSpringer Berlin / Heidelberg
CitationAnnals of Hematology, 2011, v. 91, n. 3, p. 345-352 [How to Cite?]
DOI: http://dx.doi.org/10.1007/s00277-011-1302-4
AbstractArterial dysfunction has been documented in patients with beta-thalassaemia major. This study aimed to determine the quantity and proliferative capacity of circulating CD133+VEGFR2+ and CD34+VEGFR2+ cells in patients with beta-thalassaemia major and those after haematopoietic stem cell transplantation (HSCT), and their relationships with arterial function. Brachial arterial flow-mediated dilation (FMD), carotid arterial stiffness, the quantity of these circulating cells and their number of colony-forming units (CFUs) were determined in 17 transfusion-dependent thalassaemia patients, 14 patients after HSCT and 11 controls. Compared with controls, both patient groups had significantly lower FMD and greater arterial stiffness. Despite having increased CD133+VEGFR2+ and CD34+VEGFR2+ cells, transfusion-dependent patients had significantly reduced CFUs compared with controls (p = 0.002). There was a trend of increasing CFUs across the three groups with decreasing iron load (p = 0.011). The CFUs correlated with brachial FMD (p = 0.029) and arterial stiffness (p = 0.02), but not with serum ferritin level. Multiple linear regression showed that CFU was a significant determinant of FMD (p = 0.043) and arterial stiffness (p = 0.02) after adjustment of age, sex, body mass index, blood pressure and serum ferritin level. In conclusion, arterial dysfunction found in patients with beta-thalassaemia major before and after HSCT may be related to impaired proliferation of CD133+VEGFR2+ and CD34+VEGFR2+ cells. © 2011 The Author(s).
ISSN0939-5555
2011 Impact Factor: 2.615
2011 SCImago Journal Rankings: 0.306
DOIhttp://dx.doi.org/10.1007/s00277-011-1302-4
ISI Accession Number IDWOS:000300280900004
Funding AgencyGrant Number
Children's Thalassaemia Foundation
Funding Information:

The authors are grateful to the Children's Thalassaemia Foundation for funding this work

PubMed Central IDPMC3274669
ReferencesCheung YF, Chan GC, Ha SY (2002) Arterial stiffness and endothelial function in patients with beta-thalassemia major. Circulation 106:2561–2566. doi: 10.1161/01.CIR.0000037225.92759.A7

Gedikli O, Altinbas A, Orucoglu A, Dogan A, Ozaydin M, Aslan SM, Acar G, Canatan D (2007) Elastic properties of the ascending aorta in patients with beta-thalassemia major. Echocardiography 24:830–836. doi: 10.1111/j.1540-8175.2007.00486.x

Ulger Z, Aydinok Y, Gurses D, Levent E, Ozyurek AR (2006) Stiffness of the abdominal aorta in beta-thalassemia major patients related with body iron load. J Pediatr Hematol Oncol 28:647–652. doi: 10.1097/01.mph.0000212987.18694.5a

Cheung YF, Ha SY, Chan GC (2005) Ventriculo-vascular interactions in patients with beta thalassaemia major. Heart 91:769–773. doi: 10.1136/hrt.2003.032110

Cheung YF, Chow PC, Chan GC, Ha SY (2006) Carotid intima–media thickness is increased and related to arterial stiffening in patients with beta-thalassaemia major. Br J Haematol 135:732–734. doi: 10.1111/j.1365-2141.2006.06349.x

Hahalis G, Kremastinos DT, Terzis G, Kalogeropoulos AP, Chrysanthopoulou A, Karakantza M, Kourakli A, Adamopoulos S, Tselepis AD, Grapsas N, Siablis D, Zoumbos NC, Alexopoulos D (2008) Global vasomotor dysfunction and accelerated vascular aging in beta-thalassemia major. Atherosclerosis 198:448–457. doi: 10.1016/j.atherosclerosis.2007.09.030

Kyriakou DS, Alexandrakis MG, Kyriakou ES, Liapi D, Kourelis TV, Passam F, Papadakis A (2001) Activated peripheral blood and endothelial cells in thalassemia patients. Ann Hematol 80:577–583. doi: 10.1007/s002770100355

Rosenzwieg A (2005) Circulation endothelial progenitors—cells as biomarkers. N Engl J Med 353:1055–1056. doi: 10.1056/NEJMe058134

Heiss C, Keymel S, Niesler U, Ziemann J, Kelm M, Kalka C (2005) Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol 45:1441–1448. doi: 10.1016/j.jacc.2004.12.074

Livrea MA, Tesoriere L, Pintaudi AM, Calabrese A, Maggio A, Freisleben HJ, D’Arpa D, D’Anna R, Bongiorno A (1996) Oxidative stress and antioxidant status in beta-thalassemia major: iron overload and depletion of lipid-soluble antioxidants. Blood 88:3608–3614

Day SM, Duquaine D, Mundada LV, Menon RG, Khan BV, Rajagopalan S, Fay WP (2003) Chronic iron administration increases vascular oxidative stress and accelerates arterial thrombosis. Circulation 107:2601–2606

Imanishi T, Hano T, Nishio I (2005) Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens 23:97–104. doi: 10.1097/00004872-200501000-00018

Yoder MC, Ingram DA (2009) The definition of EPCs and other bone marrow cells contributing to neoangiogenesis and tumor growth: is there common ground for understanding the roles of numerous marrow-derived cells in the neoangiogenic process? Biochim Biophys Acta 1796:50–54

Yoder MC (2010) Is endothelium the origin of endothelial progenitor cells? Arterioscler Thromb Vasc Biol 30:1094–1103. doi: 10.1161/ATVBAHA.109.191635

Timmermans F, Plum J, Yöder MC, Ingram DA, Vandekerckhove B, Case J (2009) Endothelial progenitor cells: identity defined? J Cell Mol Med 13:87–102. doi: 10.1111/j.1582-4934.2008.00598.x

Fadini GP, Miorin M, Facco M, Bonamico S, Baesso I, Grego F, Menegolo M, de Kreutzenberg SV, Tiengo A, Agostini C, Avogaro A (2005) Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. J Am Coll Cardiol 45:1449–1457. doi: 10.1016/j.jacc.2004.11.067

Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T (2003) Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348:593–600. doi: 10.1056/NEJMoa022287

Fadini GP, Coracina A, Baesso I, Agostini C, Tiengo A, Avogaro A, de Kreutzenberg SV (2006) Peripheral blood CD34+KDR+ endothelial progenitor cells are determinants of subclinical atherosclerosis in a middle-aged general population. Stroke 37:2277–2282. doi: 10.1161/01.STR.0000236064.19293.79

Kunz GA, Liang G, Cuculi F, Gregg D, Vata KC, Shaw LK, Goldschmidt-Clermont PJ, Dong C, Taylor DA, Peterson ED (2006) Circulating endothelial progenitor cells predict coronary artery disease severity. Am Heart J 152:190–195. doi: 10.1016/j.ahj.2006.02.001

Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G (2005) Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 353:999–1007. doi: 10.1056/NEJMoa043814

Aggeli C, Antoniades C, Cosma C, Chrysohoou C, Tousoulis D, Ladis V, Karageorga M, Pitsavos C, Stefanadis C (2005) Endothelial dysfunction and inflammatory process in transfusion-dependent patients with beta-thalassemia major. Int J Cardiol 105:80–84. doi: 10.1016/j.ijcard.2004.12.025

Limsuwan A, Tubtom D, Pakakasama S, Chaunsumrit A (2009) Comparison of vascular complications between conventional treatment and bone marrow transplantation for children with beta-thalassemia disease. Pediatr Cardiol 30:777–780. doi: 10.1007/s00246-009-9436-z

de Witte T (2008) The role of iron in patients after bone marrow transplantation. Blood Rev 22(Suppl 2):S22–S28. doi: 10.1016/S0268-960X(08)70005-5

Evens AM, Mehta J, Gordon LI (2004) Rust and corrosion in hematopoietic stem cell transplantation: the problem of iron and oxidative stress. Bone Marrow Transplant 34:561–571. doi: 10.1038/sj.bmt.1704591

Rodriguez-Crespo I, Nishida CR, Knudsen GM, de Montellano PR (1999) Mutation of the five conserved histidines in the endothelial nitric-oxide synthase hemoprotein domain. No evidence for a non-heme metal requirement for catalysis. J Biol Chem 274:21617–21624. doi: 10.1074/jbc.274.31.21617

Smith JB, Selak MA, Dangelmaier C, Daniel JL (1992) Cytosolic calcium as a second messenger for collagen-induced platelet responses. Biochem J 288(Pt 3):925–929

Butthep P, Khuhapinant A, Bunyaratvej A, Fucharoen S, Kitaguchi H, Funahara Y (1997) Thalassemic serum inhibits endothelial cell mitosis in vitro. Southeast Asian J Trop Med Public Health 28(Suppl 3):155–160

Banjerdpongchai R, Wilairat P, Fucharoen S, Bunyaratvej A (1997) Morphological alterations and apoptosis of endothelial cells induced by thalassemic serum in vitro. Southeast Asian J Trop Med Public Health 28(Suppl 3):149–154

Leone AM, Valgimigli M, Giannico MB, Zaccone V, Perfetti M, D’Amario D, Rebuzzi AG, Crea F (2009) From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells. Eur Heart J 30:890–899. doi: 10.1093/eurheartj/ehp078

Chaisiripoomkere W, Jootar S, Chanjarunee S, Ungkanont A (1999) Serum erythropoietin levels in thalassemia major and intermedia. Southeast Asian J Trop Med Public Health 30:786–788

Heeschen C, Aicher A, Lehmann R, Fichtlscherer S, Vasa M, Urbich C, Mildner-Rihm C, Martin H, Zeiher AM, Dimmeler S (2003) Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 102:1340–1346. doi: 10.1182/blood-2003-01-0223

Bahlmann FH, De Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, Boehm SM, Menne J, Haller H, Fliser D (2004) Erythropoietin regulates endothelial progenitor cells. Blood 103:921–926. doi: 10.1182/blood-2003-04-1284

Anning PB, Chen Y, Lamb NJ, Mumby S, Quinlan GJ, Evans TW, Gutteridge JM (1999) Iron overload upregulates haem oxygenase 1 in the lung more rapidly than in other tissues. FEBS Lett 447:111–114. doi: 10.1016/S0014-5793(99)00250-1

Wu BJ, Midwinter RG, Cassano C, Beck K, Wang Y, Changsiri D, Gamble JR, Stocker R (2009) Heme oxygenase-1 increases endothelial progenitor cells. Arterioscler Thromb Vasc Biol 29:1537–1542. doi: 10.1161/ATVBAHA.109.184713

Shantsila E, Watson T, Tse HF, Lip GY (2007) Endothelial colony forming units: are they a reliable marker of endothelial progenitor cell numbers? Ann Med 39:474–479. doi: 10.1080/07853890701329283

Tura O, Barclay GR, Roddie H, Davies J, Turner ML (2007) Absence of a relationship between immunophenotypic and colony enumeration analysis of endothelial progenitor cells in clinical haematopoietic cell sources. J Transl Med 5:37. doi: 10.1186/1479-5876-5-37

Stakos DA, Tavridou A, Margaritis D, Tziakas DN, Kotsianidis I, Chalikias GK, Tsatalas K, Bourikas G, Manolopoulos VG, Boudoulas H (2009) Oxidised low-density lipoprotein and arterial function in beta-thalassemia major. Eur J Haematol 82:477–483. doi: 10.1111/j.1600-0609.2009.01236.x

Case J, Ingram DA, Haneline LS (2008) Oxidative stress impairs endothelial progenitor cell function. Antioxid Redox Signal 10:1895–1907. doi: 10.1089/ars.2008.2118

He T, Peterson TE, Holmuhamedov EL, Terzic A, Caplice NM, Oberley LW, Katusic ZS (2004) Human endothelial progenitor cells tolerate oxidative stress due to intrinsically high expression of manganese superoxide dismutase. Arterioscler Thromb Vasc Biol 24:2021–2027. doi: 10.1161/01.ATV.0000142810.27849.8f

Hoetzer GL, Van Guilder GP, Irmiger HM, Keith RS, Stauffer BL, DeSouza CA (2007) Aging, exercise, and endothelial progenitor cell clonogenic and migratory capacity in men. J Appl Physiol 102:847–852. doi: 10.1152/japplphysiol.01183.2006

Celermajer DS, Sorensen KE, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Deanfield JE (1994) Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 24:471–476. doi: 10.1016/0735-1097(94)90305-0
DC Field
Value
dc.contributor.authorCheung, YF
dc.contributor.authorChan, S
dc.contributor.authorYang, M
dc.contributor.authorYe, JY
dc.contributor.authorHa, SY
dc.contributor.authorWong, SJ
dc.contributor.authorChan, GCF
dc.date.accessioned2012-02-21T05:42:57Z
dc.date.available2012-02-21T05:42:57Z
dc.date.issued2011
dc.description.abstractArterial dysfunction has been documented in patients with beta-thalassaemia major. This study aimed to determine the quantity and proliferative capacity of circulating CD133+VEGFR2+ and CD34+VEGFR2+ cells in patients with beta-thalassaemia major and those after haematopoietic stem cell transplantation (HSCT), and their relationships with arterial function. Brachial arterial flow-mediated dilation (FMD), carotid arterial stiffness, the quantity of these circulating cells and their number of colony-forming units (CFUs) were determined in 17 transfusion-dependent thalassaemia patients, 14 patients after HSCT and 11 controls. Compared with controls, both patient groups had significantly lower FMD and greater arterial stiffness. Despite having increased CD133+VEGFR2+ and CD34+VEGFR2+ cells, transfusion-dependent patients had significantly reduced CFUs compared with controls (p = 0.002). There was a trend of increasing CFUs across the three groups with decreasing iron load (p = 0.011). The CFUs correlated with brachial FMD (p = 0.029) and arterial stiffness (p = 0.02), but not with serum ferritin level. Multiple linear regression showed that CFU was a significant determinant of FMD (p = 0.043) and arterial stiffness (p = 0.02) after adjustment of age, sex, body mass index, blood pressure and serum ferritin level. In conclusion, arterial dysfunction found in patients with beta-thalassaemia major before and after HSCT may be related to impaired proliferation of CD133+VEGFR2+ and CD34+VEGFR2+ cells. © 2011 The Author(s).
dc.description.naturepublished_or_final_version
dc.description.otherSpringer Open Choice, 21 Feb 2012
dc.identifier.citationAnnals of Hematology, 2011, v. 91, n. 3, p. 345-352 [How to Cite?]
DOI: http://dx.doi.org/10.1007/s00277-011-1302-4
dc.identifier.citeulike9631716
dc.identifier.doihttp://dx.doi.org/10.1007/s00277-011-1302-4
dc.identifier.eissn1432-0584
dc.identifier.epage352
dc.identifier.hkuros191927
dc.identifier.hkuros198730
dc.identifier.isiWOS:000300280900004
Funding AgencyGrant Number
Children's Thalassaemia Foundation
Funding Information:

The authors are grateful to the Children's Thalassaemia Foundation for funding this work

dc.identifier.issn0939-5555
2011 Impact Factor: 2.615
2011 SCImago Journal Rankings: 0.306
dc.identifier.issue3
dc.identifier.openurl
dc.identifier.pmcidPMC3274669
dc.identifier.pmid21808992
dc.identifier.scopuseid_2-s2.0-84857363739
dc.identifier.spage345
dc.identifier.urihttp://hdl.handle.net/10722/144928
dc.identifier.volume91
dc.languageEng
dc.publisherSpringer Berlin / Heidelberg
dc.relation.ispartofAnnals of Hematology
dc.relation.referencesCheung YF, Chan GC, Ha SY (2002) Arterial stiffness and endothelial function in patients with beta-thalassemia major. Circulation 106:2561–2566. doi: 10.1161/01.CIR.0000037225.92759.A7
dc.relation.referencesGedikli O, Altinbas A, Orucoglu A, Dogan A, Ozaydin M, Aslan SM, Acar G, Canatan D (2007) Elastic properties of the ascending aorta in patients with beta-thalassemia major. Echocardiography 24:830–836. doi: 10.1111/j.1540-8175.2007.00486.x
dc.relation.referencesUlger Z, Aydinok Y, Gurses D, Levent E, Ozyurek AR (2006) Stiffness of the abdominal aorta in beta-thalassemia major patients related with body iron load. J Pediatr Hematol Oncol 28:647–652. doi: 10.1097/01.mph.0000212987.18694.5a
dc.relation.referencesCheung YF, Ha SY, Chan GC (2005) Ventriculo-vascular interactions in patients with beta thalassaemia major. Heart 91:769–773. doi: 10.1136/hrt.2003.032110
dc.relation.referencesCheung YF, Chow PC, Chan GC, Ha SY (2006) Carotid intima–media thickness is increased and related to arterial stiffening in patients with beta-thalassaemia major. Br J Haematol 135:732–734. doi: 10.1111/j.1365-2141.2006.06349.x
dc.relation.referencesHahalis G, Kremastinos DT, Terzis G, Kalogeropoulos AP, Chrysanthopoulou A, Karakantza M, Kourakli A, Adamopoulos S, Tselepis AD, Grapsas N, Siablis D, Zoumbos NC, Alexopoulos D (2008) Global vasomotor dysfunction and accelerated vascular aging in beta-thalassemia major. Atherosclerosis 198:448–457. doi: 10.1016/j.atherosclerosis.2007.09.030
dc.relation.referencesKyriakou DS, Alexandrakis MG, Kyriakou ES, Liapi D, Kourelis TV, Passam F, Papadakis A (2001) Activated peripheral blood and endothelial cells in thalassemia patients. Ann Hematol 80:577–583. doi: 10.1007/s002770100355
dc.relation.referencesRosenzwieg A (2005) Circulation endothelial progenitors—cells as biomarkers. N Engl J Med 353:1055–1056. doi: 10.1056/NEJMe058134
dc.relation.referencesHeiss C, Keymel S, Niesler U, Ziemann J, Kelm M, Kalka C (2005) Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol 45:1441–1448. doi: 10.1016/j.jacc.2004.12.074
dc.relation.referencesLivrea MA, Tesoriere L, Pintaudi AM, Calabrese A, Maggio A, Freisleben HJ, D’Arpa D, D’Anna R, Bongiorno A (1996) Oxidative stress and antioxidant status in beta-thalassemia major: iron overload and depletion of lipid-soluble antioxidants. Blood 88:3608–3614
dc.relation.referencesDay SM, Duquaine D, Mundada LV, Menon RG, Khan BV, Rajagopalan S, Fay WP (2003) Chronic iron administration increases vascular oxidative stress and accelerates arterial thrombosis. Circulation 107:2601–2606
dc.relation.referencesImanishi T, Hano T, Nishio I (2005) Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens 23:97–104. doi: 10.1097/00004872-200501000-00018
dc.relation.referencesYoder MC, Ingram DA (2009) The definition of EPCs and other bone marrow cells contributing to neoangiogenesis and tumor growth: is there common ground for understanding the roles of numerous marrow-derived cells in the neoangiogenic process? Biochim Biophys Acta 1796:50–54
dc.relation.referencesYoder MC (2010) Is endothelium the origin of endothelial progenitor cells? Arterioscler Thromb Vasc Biol 30:1094–1103. doi: 10.1161/ATVBAHA.109.191635
dc.relation.referencesTimmermans F, Plum J, Yöder MC, Ingram DA, Vandekerckhove B, Case J (2009) Endothelial progenitor cells: identity defined? J Cell Mol Med 13:87–102. doi: 10.1111/j.1582-4934.2008.00598.x
dc.relation.referencesFadini GP, Miorin M, Facco M, Bonamico S, Baesso I, Grego F, Menegolo M, de Kreutzenberg SV, Tiengo A, Agostini C, Avogaro A (2005) Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. J Am Coll Cardiol 45:1449–1457. doi: 10.1016/j.jacc.2004.11.067
dc.relation.referencesHill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T (2003) Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348:593–600. doi: 10.1056/NEJMoa022287
dc.relation.referencesFadini GP, Coracina A, Baesso I, Agostini C, Tiengo A, Avogaro A, de Kreutzenberg SV (2006) Peripheral blood CD34+KDR+ endothelial progenitor cells are determinants of subclinical atherosclerosis in a middle-aged general population. Stroke 37:2277–2282. doi: 10.1161/01.STR.0000236064.19293.79
dc.relation.referencesKunz GA, Liang G, Cuculi F, Gregg D, Vata KC, Shaw LK, Goldschmidt-Clermont PJ, Dong C, Taylor DA, Peterson ED (2006) Circulating endothelial progenitor cells predict coronary artery disease severity. Am Heart J 152:190–195. doi: 10.1016/j.ahj.2006.02.001
dc.relation.referencesWerner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G (2005) Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 353:999–1007. doi: 10.1056/NEJMoa043814
dc.relation.referencesAggeli C, Antoniades C, Cosma C, Chrysohoou C, Tousoulis D, Ladis V, Karageorga M, Pitsavos C, Stefanadis C (2005) Endothelial dysfunction and inflammatory process in transfusion-dependent patients with beta-thalassemia major. Int J Cardiol 105:80–84. doi: 10.1016/j.ijcard.2004.12.025
dc.relation.referencesLimsuwan A, Tubtom D, Pakakasama S, Chaunsumrit A (2009) Comparison of vascular complications between conventional treatment and bone marrow transplantation for children with beta-thalassemia disease. Pediatr Cardiol 30:777–780. doi: 10.1007/s00246-009-9436-z
dc.relation.referencesde Witte T (2008) The role of iron in patients after bone marrow transplantation. Blood Rev 22(Suppl 2):S22–S28. doi: 10.1016/S0268-960X(08)70005-5
dc.relation.referencesEvens AM, Mehta J, Gordon LI (2004) Rust and corrosion in hematopoietic stem cell transplantation: the problem of iron and oxidative stress. Bone Marrow Transplant 34:561–571. doi: 10.1038/sj.bmt.1704591
dc.relation.referencesRodriguez-Crespo I, Nishida CR, Knudsen GM, de Montellano PR (1999) Mutation of the five conserved histidines in the endothelial nitric-oxide synthase hemoprotein domain. No evidence for a non-heme metal requirement for catalysis. J Biol Chem 274:21617–21624. doi: 10.1074/jbc.274.31.21617
dc.relation.referencesSmith JB, Selak MA, Dangelmaier C, Daniel JL (1992) Cytosolic calcium as a second messenger for collagen-induced platelet responses. Biochem J 288(Pt 3):925–929
dc.relation.referencesButthep P, Khuhapinant A, Bunyaratvej A, Fucharoen S, Kitaguchi H, Funahara Y (1997) Thalassemic serum inhibits endothelial cell mitosis in vitro. Southeast Asian J Trop Med Public Health 28(Suppl 3):155–160
dc.relation.referencesBanjerdpongchai R, Wilairat P, Fucharoen S, Bunyaratvej A (1997) Morphological alterations and apoptosis of endothelial cells induced by thalassemic serum in vitro. Southeast Asian J Trop Med Public Health 28(Suppl 3):149–154
dc.relation.referencesLeone AM, Valgimigli M, Giannico MB, Zaccone V, Perfetti M, D’Amario D, Rebuzzi AG, Crea F (2009) From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells. Eur Heart J 30:890–899. doi: 10.1093/eurheartj/ehp078
dc.relation.referencesChaisiripoomkere W, Jootar S, Chanjarunee S, Ungkanont A (1999) Serum erythropoietin levels in thalassemia major and intermedia. Southeast Asian J Trop Med Public Health 30:786–788
dc.relation.referencesHeeschen C, Aicher A, Lehmann R, Fichtlscherer S, Vasa M, Urbich C, Mildner-Rihm C, Martin H, Zeiher AM, Dimmeler S (2003) Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 102:1340–1346. doi: 10.1182/blood-2003-01-0223
dc.relation.referencesBahlmann FH, De Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, Boehm SM, Menne J, Haller H, Fliser D (2004) Erythropoietin regulates endothelial progenitor cells. Blood 103:921–926. doi: 10.1182/blood-2003-04-1284
dc.relation.referencesAnning PB, Chen Y, Lamb NJ, Mumby S, Quinlan GJ, Evans TW, Gutteridge JM (1999) Iron overload upregulates haem oxygenase 1 in the lung more rapidly than in other tissues. FEBS Lett 447:111–114. doi: 10.1016/S0014-5793(99)00250-1
dc.relation.referencesWu BJ, Midwinter RG, Cassano C, Beck K, Wang Y, Changsiri D, Gamble JR, Stocker R (2009) Heme oxygenase-1 increases endothelial progenitor cells. Arterioscler Thromb Vasc Biol 29:1537–1542. doi: 10.1161/ATVBAHA.109.184713
dc.relation.referencesShantsila E, Watson T, Tse HF, Lip GY (2007) Endothelial colony forming units: are they a reliable marker of endothelial progenitor cell numbers? Ann Med 39:474–479. doi: 10.1080/07853890701329283
dc.relation.referencesTura O, Barclay GR, Roddie H, Davies J, Turner ML (2007) Absence of a relationship between immunophenotypic and colony enumeration analysis of endothelial progenitor cells in clinical haematopoietic cell sources. J Transl Med 5:37. doi: 10.1186/1479-5876-5-37
dc.relation.referencesStakos DA, Tavridou A, Margaritis D, Tziakas DN, Kotsianidis I, Chalikias GK, Tsatalas K, Bourikas G, Manolopoulos VG, Boudoulas H (2009) Oxidised low-density lipoprotein and arterial function in beta-thalassemia major. Eur J Haematol 82:477–483. doi: 10.1111/j.1600-0609.2009.01236.x
dc.relation.referencesCase J, Ingram DA, Haneline LS (2008) Oxidative stress impairs endothelial progenitor cell function. Antioxid Redox Signal 10:1895–1907. doi: 10.1089/ars.2008.2118
dc.relation.referencesHe T, Peterson TE, Holmuhamedov EL, Terzic A, Caplice NM, Oberley LW, Katusic ZS (2004) Human endothelial progenitor cells tolerate oxidative stress due to intrinsically high expression of manganese superoxide dismutase. Arterioscler Thromb Vasc Biol 24:2021–2027. doi: 10.1161/01.ATV.0000142810.27849.8f
dc.relation.referencesHoetzer GL, Van Guilder GP, Irmiger HM, Keith RS, Stauffer BL, DeSouza CA (2007) Aging, exercise, and endothelial progenitor cell clonogenic and migratory capacity in men. J Appl Physiol 102:847–852. doi: 10.1152/japplphysiol.01183.2006
dc.relation.referencesCelermajer DS, Sorensen KE, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Deanfield JE (1994) Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 24:471–476. doi: 10.1016/0735-1097(94)90305-0
dc.rightsThe Author(s)
dc.rightsCreative Commons: Attribution 3.0 Hong Kong License
dc.subjectMedicine & Public Health
dc.subjectHematology
dc.subjectOncology
dc.titleCirculating CD133 +VEGFR2 + and CD34 +VEGFR2 + cells and arterial function in patients with beta-thalassaemia major
dc.typeArticle
Author Affiliations
  1. The University of Hong Kong