E-selectin mediates stem cell adhesion and formation of blood vessels in a murine model of infantile hemangioma

American Journal of Pathology

Volumn 181, Issue 6, 2012, Pages 2239-2247

  Smadja, David M ^a,b   Mulliken, John B ^a,c   Bischoff, Joyce ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ARTICLE; CAPILLARY HEMANGIOMA; CELL ADHESION; CELL ISOLATION; CELL MIGRATION; CELL PROLIFERATION; CHILD; ENDOTHELIUM CELL; FEMALE; HEMANGIOMA STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INFANT; MALE; MOUSE; NONHUMAN; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; ANTIBODIES, BLOCKING; ANTIBODIES, MONOCLONAL; BLOOD VESSELS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELL SEPARATION; CHILD, PRESCHOOL; DISEASE MODELS, ANIMAL; E-SELECTIN; ENDOTHELIAL CELLS; FEMALE; HEMANGIOMA, CAPILLARY; HUMANS; INFANT; MALE; MICE; MICE, NUDE; NEOPLASTIC SYNDROMES, HEREDITARY; NEOVASCULARIZATION, PHYSIOLOGIC; RECOMBINANT PROTEINS; STEM CELLS;

EID: 84869167214     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.08.030     Document Type: Article

References (52)

1. J.B. Mulliken, S.J. Fishman, P.E. Burrows Vascular anomalies Curr Probl Surg 37 2000 517 584
2. E. Boye, Y. Yu, G. Paranya, J.B. Mulliken, B.R. Olsen, J. Bischoff Clonality and altered behavior of endothelial cells from hemangiomas J Clin Invest 107 2001 745 752
3. J.W. Walter, P.E. North, M. Waner, A. Mizeracki, F. Blei, J.W. Walker, J.F. Reinisch, D.A. Marchuk Somatic mutation of vascular endothelial growth factor receptors in juvenile hemangioma Genes Chromosomes Cancer 33 2002 295 303
4. Q. Li, Y. Yu, J. Bischoff, J.B. Mulliken, B.R. Olsen Differential expression of CD146 in tissues and endothelial cells derived from infantile haemangioma and normal human skin J Pathol 201 2003 296 302
5. M. Jinnin, D. Medici, L. Park, N. Limaye, Y. Liu, E. Boscolo, J. Bischoff, M. Vikkula, E. Boye, B.R. Olsen Suppressed NFAT-dependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma Nat Med 14 2008 1236 1246
6. C.M. Barnes, S. Huang, A. Kaipainen, D. Sanoudou, E.J. Chen, G.S. Eichler, Y. Guo, Y. Yu, D.E. Ingber, J.B. Mulliken, A.H. Beggs, J. Folkman, S.J. Fishman Evidence by molecular profiling for a placental origin of infantile hemangioma Proc Natl Acad Sci USA 102 2005 19097 19102
7. P.E. North, M. Waner, A. Mizeracki, R.E. Mrak, R. Nicholas, J. Kincannon, J.Y. Suen, M.C. Mihm Jr. A unique microvascular phenotype shared by juvenile hemangiomas and human placenta Arch Dermatol 137 2001 559 570
8. M.L. Calicchio, T. Collins, H.P. Kozakewich Identification of signaling systems in proliferating and involuting phase infantile hemangiomas by genome-wide transcriptional profiling Am J Pathol 174 2009 1638 1649
9. M.E. Kleinman, M.R. Greives, S.S. Churgin, K.M. Blechman, E.I. Chang, D.J. Ceradini, O.M. Tepper, G.C. Gurtner Hypoxia-induced mediators of stem/progenitor cell trafficking are increased in children with hemangioma Arterioscler Thromb Vasc Biol 27 2007 2664 2670
10. M.E. Kleinman, O.M. Tepper, J.M. Capla, K.A. Bhatt, D.J. Ceradini, R.D. Galiano, F. Blei, J.P. Levine, G.C. Gurtner Increased circulating AC133+ CD34+ endothelial progenitor cells in children with hemangioma Lymphat Res Biol 1 2003 301 307
11. M.R. Ritter, J. Reinisch, S.F. Friedlander, M. Friedlander Myeloid cells in infantile hemangioma Am J Pathol 168 2006 621 628
12. Z.A. Khan, E. Boscolo, A. Picard, S. Psutka, J.M. Melero-Martin, T.C. Bartch, J.B. Mulliken, J. Bischoff Multipotential stem cells recapitulate human infantile hemangioma in immunodeficient mice J Clin Invest 118 2008 2592 2599
13. S. Greenberger, E. Boscolo, I. Adini, J.B. Mulliken, J. Bischoff Corticosteroid suppression of VEGF-A in infantile hemangioma-derived stem cells N Engl J Med 362 2010 1005 1013
14. B.M. Kraling, M.J. Razon, L.M. Boon, D. Zurakowski, C. Seachord, R.P. Darveau, J.B. Mulliken, C.L. Corless, J. Bischoff E-selectin is present in proliferating endothelial cells in human hemangiomas Am J Pathol 148 1996 1181 1191
15. V. Verkarre, N. Patey-Mariaud de Serre, R. Vazeux, D. Teillac-Hamel, B. Chretien-Marquet, C. Le Bihan, M. Leborgne, S. Fraitag, N. Brousse ICAM-3 and E-selectin endothelial cell expression differentiate two phases of angiogenesis in infantile hemangiomas J Cutan Pathol 26 1999 17 24
16. S. Greenberger, I. Adini, E. Boscolo, J.B. Mulliken, J. Bischoff Targeting NF-kappaB in infantile hemangioma-derived stem cells reduces VEGF-A expression Angiogenesis 13 2010 327 335
17. E. Boscolo, J.B. Mulliken, J. Bischoff VEGFR-1 mediates endothelial differentiation and formation of blood vessels in a murine model of infantile hemangioma Am J Pathol 179 2011 2266 2277
18. E. Boscolo, C.L. Stewart, S. Greenberger, J.K. Wu, J.T. Durham, I.M. Herman, J.B. Mulliken, J. Kitajewski, J. Bischoff JAGGED1 signaling regulates hemangioma stem cell-to-pericyte/vascular smooth muscle cell differentiation Arterioscler Thromb Vasc Biol 31 2011 2181 2192
19. Z.A. Khan, J.M. Melero-Martin, X. Wu, S. Paruchuri, E. Boscolo, J.B. Mulliken, J. Bischoff Endothelial progenitor cells from infantile hemangioma and umbilical cord blood display unique cellular responses to endostatin Blood 108 2006 915 921
20. J.M. Melero-Martin, M.E. De Obaldia, S.Y. Kang, Z.A. Khan, L. Yuan, P. Oettgen, J. Bischoff Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells Circ Res 103 2008 194 202
21. J.M. Melero-Martin, Z.A. Khan, A. Picard, X. Wu, S. Paruchuri, J. Bischoff In vivo vasculogenic potential of human blood-derived endothelial progenitor cells Blood 109 2007 4761 4768
22. K.T. Kang, P. Allen, J. Bischoff Bioengineered human vascular networks transplanted into secondary mice reconnect with the host vasculature and re-establish perfusion Blood 118 2011 6718 6721
23. S. SenBanerjee, Z. Lin, G.B. Atkins, D.M. Greif, R.M. Rao, A. Kumar, M.W. Feinberg, Z. Chen, D.I. Simon, F.W. Luscinskas, T.M. Michel, M.A. Gimbrone Jr., G. Garcia-Cardena, M.K. Jain KLF2 is a novel transcriptional regulator of endothelial proinflammatory activation J Exp Med 199 2004 1305 1315
24. Z.J. Liu, R. Tian, Y. Li, W. An, Y. Zhuge, A.S. Livingstone, O.C. Velazquez Inhibition of tumor angiogenesis and melanoma growth by targeting vascular E-selectin Ann Surg 254 2011 450 456 discussion 456-457
25. S.R. Barthel, G.K. Wiese, J. Cho, M.J. Opperman, D.L. Hays, J. Siddiqui, K.J. Pienta, B. Furie, C.J. Dimitroff Alpha 1,3 fucosyltransferases are master regulators of prostate cancer cell trafficking Proc Natl Acad Sci USA 106 2009 19491 19496
26. S. Hiratsuka, S. Goel, W.S. Kamoun, Y. Maru, D. Fukumura, D.G. Duda, R.K. Jain Endothelial focal adhesion kinase mediates cancer cell homing to discrete regions of the lungs via E-selectin up-regulation Proc Natl Acad Sci USA 108 2011 3725 3730
27. S.P. Thankamony, R. Sackstein Enforced hematopoietic cell E- and L-selectin ligand (HCELL) expression primes transendothelial migration of human mesenchymal stem cells Proc Natl Acad Sci USA 108 2011 2258 2263
28. I.Y. Oh, C.H. Yoon, J. Hur, J.H. Kim, T.Y. Kim, C.S. Lee, K.W. Park, I.H. Chae, B.H. Oh, Y.B. Park, H.S. Kim Involvement of E-selectin in recruitment of endothelial progenitor cells and angiogenesis in ischemic muscle Blood 110 2007 3891 3899
29. D.M. Smadja, I. Bieche, G. Uzan, H. Bompais, L. Muller, C. Boisson-Vidal, M. Vidaud, M. Aiach, P. Gaussem PAR-1 activation on human late endothelial progenitor cells enhances angiogenesis in vitro with upregulation of the SDF-1/CXCR4 system Arterioscler Thromb Vasc Biol 25 2005 2321 2327
30. P.S. Frenette, T.N. Mayadas, H. Rayburn, R.O. Hynes, D.D. Wagner Susceptibility to infection and altered hematopoiesis in mice deficient in both P- and E-selectins Cell 84 1996 563 574
31. A.J. Naiyer, D.Y. Jo, J. Ahn, R. Mohle, M. Peichev, G. Lam, R.L. Silverstein, M.A. Moore, S. Rafii Stromal derived factor-1-induced chemokinesis of cord blood CD34(+) cells (long-term culture-initiating cells) through endothelial cells is mediated by E-selectin Blood 94 1999 4011 4019
32. C.J. Dimitroff, J.Y. Lee, S. Rafii, R.C. Fuhlbrigge, R. Sackstein CD44 is a major E-selectin ligand on human hematopoietic progenitor cells J Cell Biol 153 2001 1277 1286
33. A. Hidalgo, L.A. Weiss, P.S. Frenette Functional selectin ligands mediating human CD34(+) cell interactions with bone marrow endothelium are enhanced postnatally J Clin Invest 110 2002 559 569
34. A.W. Greenberg, W.G. Kerr, D.A. Hammer Relationship between selectin-mediated rolling of hematopoietic stem and progenitor cells and progression in hematopoietic development Blood 95 2000 478 486
35. M.P. Bevilacqua, S. Stengelin, M.A. Gimbrone Jr., B. Seed Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins Science 243 1989 1160 1165
36. U. Schindler, V.R. Baichwal Three NF-kappa B binding sites in the human E-selectin gene required for maximal tumor necrosis factor alpha-induced expression Mol Cell Biol 14 1994 5820 5831
37. G. Tabatabai, C. Herrmann, G. von Kurthy, M. Mittelbronn, S. Grau, B. Frank, R. Mohle, M. Weller, W. Wick VEGF-dependent induction of CD62E on endothelial cells mediates glioma tropism of adult haematopoietic progenitor cells Brain 131 2008 2579 2595
38. Y. Nishiwaki, M. Yoshida, H. Iwaguro, H. Masuda, N. Nitta, T. Asahara, M. Isobe Endothelial E-selectin potentiates neovascularization via endothelial progenitor cell-dependent and -independent mechanisms Arterioscler Thromb Vasc Biol 27 2007 512 518
39. A.E. Koch, M.M. Halloran, C.J. Haskell, M.R. Shah, P.J. Polverini Angiogenesis mediated by soluble forms of E-selectin and vascular cell adhesion molecule-1 Nature 376 1995 517 519
40. P. Kumar, M.A. Amin, L.A. Harlow, P.J. Polverini, A.E. Koch Src and phosphatidylinositol 3-kinase mediate soluble E-selectin-induced angiogenesis Blood 101 2003 3960 3968
41. Y. Yu, A.F. Flint, J.B. Mulliken, J.K. Wu, J. Bischoff Endothelial progenitor cells in infantile hemangioma Blood 103 2004 1373 1375
42. M.R. Ritter, M.I. Dorrell, J. Edmonds, S.F. Friedlander, M. Friedlander Insulin-like growth factor 2 and potential regulators of hemangioma growth and involution identified by large-scale expression analysis Proc Natl Acad Sci USA 99 2002 7455 7460
43. D. Wong, K. Dorovini-Zis Regualtion by cytokines and lipopolysaccharide of E-selectin expression by human brain microvessel endothelial cells in primary culture J Neuropathol Exp Neurol 55 1996 225 235
44. K.M. Schweitzer, A.M. Drager, P. van der Valk, S.F. Thijsen, A. Zevenbergen, A.P. Theijsmeijer, C.E. van der Schoot, M.M. Langenhuijsen Constitutive expression of E-selectin and vascular cell adhesion molecule-1 on endothelial cells of hematopoietic tissues Am J Pathol 148 1996 165 175
45. M.E. Gerritsen, C.P. Shen, M.C. McHugh, W.J. Atkinson, J.M. Kiely, D.S. Milstone, F.W. Luscinskas, M.A. Gimbrone Jr. Activation-dependent isolation and culture of murine pulmonary microvascular endothelium Microcirculation 2 1995 151 163
46. A.T. Hooper, J.M. Butler, D.J. Nolan, A. Kranz, K. Iida, M. Kobayashi, H.G. Kopp, K. Shido, I. Petit, K. Yanger, D. James, L. Witte, Z. Zhu, Y. Wu, B. Pytowski, Z. Rosenwaks, V. Mittal, T.N. Sato, S. Rafii Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells Cell Stem Cell 4 2009 263 274
47. J.M. Butler, D.J. Nolan, E.L. Vertes, B. Varnum-Finney, H. Kobayashi, A.T. Hooper, M. Seandel, K. Shido, I.A. White, M. Kobayashi, L. Witte, C. May, C. Shawber, Y. Kimura, J. Kitajewski, Z. Rosenwaks, I.D. Bernstein, S. Rafii Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells Cell Stem Cell 6 2010 251 264
48. H. Kobayashi, J.M. Butler, R. O'Donnell, M. Kobayashi, B.S. Ding, B. Bonner, V.K. Chiu, D.J. Nolan, K. Shido, L. Benjamin, S. Rafii Angiocrine factors from Akt-activated endothelial cells balance self-renewal and differentiation of haematopoietic stem cells Nat Cell Biol 12 2010 1046 1056
49. M. Seandel, J.M. Butler, H. Kobayashi, A.T. Hooper, I.A. White, F. Zhang, E.L. Vertes, M. Kobayashi, Y. Zhang, S.V. Shmelkov, N.R. Hackett, S. Rabbany, J.L. Boyer, S. Rafii Generation of a functional and durable vascular niche by the adenoviral E4ORF1 gene Proc Natl Acad Sci USA 105 2008 19288 19293
50. G. Curradi, M.S. Walters, B.S. Ding, S. Rafii, N.R. Hackett, R.G. Crystal Airway basal cell vascular endothelial growth factor-mediated cross-talk regulates endothelial cell-dependent growth support of human airway basal cells Cell Mol Life Sci 69 2012 2217 2231
51. B.S. Ding, D.J. Nolan, J.M. Butler, D. James, A.O. Babazadeh, Z. Rosenwaks, V. Mittal, H. Kobayashi, K. Shido, D. Lyden, T.N. Sato, S.Y. Rabbany, S. Rafii Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration Nature 468 2010 310 315
52. B.S. Ding, D.J. Nolan, P. Guo, A.O. Babazadeh, Z. Cao, Z. Rosenwaks, R.G. Crystal, M. Simons, T.N. Sato, S. Worgall, K. Shido, S.Y. Rabbany, S. Rafii Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization Cell 147 2011 539 553