A switch in Notch gene expression parallels stem cell to endothelial transition in infantile hemangioma

Angiogenesis

Volumn 13, Issue 1, 2010, Pages 15-23

  Wu, June K ^a   Adepoju, Omotinuwe ^a   De Silva, Dinuka ^a   Baribault, Keith ^a   Boscolo, Elisa ^b   Bischoff, Joyce ^b   Kitajewski, Jan ^a  

^a College of Physicians and Surgeons ^*  (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Endothelial cell; Infantile hemangioma; Notch gene expression; Stem cell

Indexed keywords

CD31 ANTIGEN; JAGGED1; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH3 RECEPTOR; NOTCH4 RECEPTOR;

ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM; GENE EXPRESSION; GENE FUNCTION; HEMANGIOMA; HUMAN; HUMAN CELL; INFANTILE HEMANGIOMA; MULTIGENE FAMILY; PLACENTA; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SKIN; STEM CELL;

ANTIGENS, CD31; CALCIUM-BINDING PROTEINS; CELL PROLIFERATION; CELL SEPARATION; ENDOTHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEMANGIOMA; HUMANS; INFANT; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; PLACENTA; PREGNANCY; PROTEIN TRANSPORT; RECEPTORS, NOTCH; RNA, MESSENGER; SKIN; STEM CELLS;

EID: 77950691904     PISSN: 09696970     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10456-009-9161-5     Document Type: Article

References (35)

1. Frieden IJ, Haggstrom AN, Drolet BA, Mancini AJ, Friedlander SF, Boon L, Chamlin SL, Baselga E, Garzon MC, Nopper AJ, Siegel DH, Mathes EW, Goddard DS, Bischoff J, North PE, Esterly NB (2005) Infantile hemangiomas: current knowledge, future directions. Proceedings of a research workshop on infantile hemangiomas, April 7-9, Bethesda, Maryland, USA. Pediatr Dermatol 22:383-406
2. Mulliken JB, Fishman SJ, Burrows PE (2000) Vascular anomalies. Curr Probl Surg 37:517-584
3. Mulliken JB, Glowacki J (1982) Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg 69:412-422 (Pubitemid 12191292)
4. North PE, Waner M, Mizeracki A, Mihm MC Jr (2000) GLUT1: a newly discovered immunohistochemical marker for juvenile hemangiomas. Hum Pathol 31:11-22 (Pubitemid 30054381)
5. North PE, Waner M, Brodsky MC (2002) Are infantile hemangiomas of placental origin? Ophthalmology 109:633-634 (Pubitemid 34270116)
6. Barnes CM, Christison-Lagay EA, Folkman J (2007) The placenta theory and the origin of infantile hemangioma. Lymphat Res Biol 5:245-255
7. Barnes CM, Huang S, Kaipainen A, Sanoudou D, Chen EJ, Eichler GS, Guo Y, Yu Y, Ingber DE, Mulliken JB, Beggs AH, Folkman J, Fishman SJ (2005) Evidence by molecular profiling for a placental origin of infantile hemangioma. Proc Natl Acad Sci USA 102:19097-19102 (Pubitemid 43049572)
8. Kraling BM, Razon MJ, Boon LM, Zurakowski D, Seachord C, Darveau RP, Mulliken JB, Corless CL, Bischoff J (1996) E-selectin is present in proliferating endothelial cells in human hemangiomas. Am J Pathol 148:1181-1191 (Pubitemid 26108255)
9. Takahashi K, Mulliken JB, Kozakewich HP, Rogers RA, Folkman J, Ezekowitz RA (1994) Cellular markers that distinguish the phases of hemangioma during infancy and childhood. J Clin Invest 93:2357-2364 (Pubitemid 24177146)
10. Ritter MR, Moreno SK, Dorrell MI, Rubens J, Ney J, Friedlander DF, Bergman J, Cunningham BB, Eichenfield L, Reinisch J, Cohen S, Veccione T, Holmes R, Friedlander SF, Friedlander M (2003) Identifying potential regulators of infantile hemangioma progression through large-scale expression analysis: a possible role for the immune system and indoleamine 2, 3 dioxygenase (IDO) during involution. Lymphat Res Biol 1:291-299
11. Ritter MR, Dorrell MI, Edmonds J, Friedlander SF, Friedlander M (2002) Insulin-like growth factor 2 and potential regulators of hemangioma growth and involution identified by large-scale expression analysis. Proc Natl Acad Sci USA 99:7455-7460 (Pubitemid 34568712)
12. Calicchio ML, Collins T, Kozakewich HP (2009) Identification of signaling systems in proliferating and involuting phase infantile hemangiomas by genome-wide transcriptional profiling. Am J Pathol 174:1638-1649
13. Bischoff J (2002) Monoclonal expansion of endothelial cells in hemangioma: an intrinsic defect with extrinsic consequences? Trends Cardiovasc Med 12:220-224 (Pubitemid 34823632)
14. Boye E, Yu Y, Paranya G, Mulliken JB, Olsen BR, Bischoff J (2001) Clonality and altered behavior of endothelial cells from hemangiomas. J Clin Invest 107:745-752 (Pubitemid 32225360)
15. Walter JW, North PE, Waner M, Mizeracki A, Blei F, Walker JW, Reinisch JF, Marchuk DA (2002) Somatic mutation of vascular endothelial growth factor receptors in juvenile hemangioma. Genes Chromosomes Cancer 33:295-303 (Pubitemid 34130936)
16. Yu Y, Varughese J, Brown LF, Mulliken JB, Bischoff J (2001) Increased Tie2 expression, enhanced response to angiopoietin-1, and dysregulated angiopoietin-2 expression in hemangiomaderived endothelial cells. Am J Pathol 159:2271-2280 (Pubitemid 33104280)
17. Jinnin M, Medici D, Park L, Limaye N, Liu Y, Boscolo E, Bischoff J, Vikkula M, Boye E, Olsen BR (2008) Suppressed NFAT-dependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma. Nat Med 14:1236-1246
18. Yu Y, Flint AF, Mulliken JB, Wu J.K., Bischoff J (2004) Endothelial progenitor cells in infantile hemangioma. Blood 103: 1373-1375 (Pubitemid 38168651)
19. Kleinman ME, Blei F, Gurtner GC (2005) Circulating endothelial progenitor cells and vascular anomalies. Lymphat Res Biol 3: 234-239 (Pubitemid 43115792)
20. Khan ZA, Melero-Martin J.M., Wu X, Paruchuri S, Boscolo E, Mulliken JB, Bischoff J (2006) Endothelial progenitor cells from infantile hemangioma and umbilical cord blood display unique cellular responses to endostatin. Blood 108:915-921 (Pubitemid 44154625)
21. Khan ZA, Boscolo E, Picard A, Psutka S, Melero-Martin J.M., Bartch TC, Mulliken JB, Bischoff J (2008) Multipotential stem cells recapitulate human infantile hemangioma in immunodeficient mice. J Clin Invest 118(7):2592-2599 (Pubitemid 351949786)
22. Shawber CJ, Das I, Francisco E, Kitajewski J (2003) Notch signaling in primary endothelial cells. AnnNYAcad Sci 995:162-170 (Pubitemid 36706623)
23. Shawber CJ, Kitajewski J (2004) Notch function in the vasculature: insights from zebrafish, mouse and man. Bioessays 26: 225-234 (Pubitemid 38325664)
24. Zhang G, Zhou J, Fan Q, Zheng Z, Zhang F, Liu X, Hu S (2008) Arterial-venous endothelial cell fate is related to vascular endothelial growth factor and Notch status during human bone mesenchymal stem cell differentiation. FEBS Lett 582:2957-2964
25. Patel NS, Li JL, Generali D, Poulsom R, Cranston DW, Harris AL (2005) Up-regulation of delta-like 4 ligand in human tumor vasculature and the role of basal expression in endothelial cell function. Cancer Res 65:8690-8697 (Pubitemid 41377356)
26. Dufraine J, Funahashi Y, Kitajewski J (2008) Notch signaling regulates tumor angiogenesis by diverse mechanisms. Oncogene 27:5132-5137
27. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I, Singh M, Chien M, Tan C, Hongo JA, de Sauvage F, Plowman G, Yan M (2006) Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444:1083-1087 (Pubitemid 46018529)
28. Funahashi Y, Hernandez SL, Das I, Ahn A, Huang J, Vorontchikhina M, Sharma A, Kanamaru E, Borisenko V, Desilva DM, Suzuki A, Wang X, Shawber CJ, Kandel JJ, Yamashiro DJ, Kitajewski J (2008)Anotch1 ectodomain construct inhibits endothelial notch signaling, tumor growth, and angiogenesis. Cancer Res 68: 4727-4735
29. Williams CK, Li JL, Murga M, Harris AL, Tosato G (2006) Up-regulation of the Notch ligand Delta-like 4 inhibits VEGFinduced endothelial cell function. Blood 107:931-939 (Pubitemid 43156289)
30. Shawber CJ, Funahashi Y, Francisco E, Vorontchikhina M, Kitamura Y, Stowell SA, Borisenko V, Feirt N, Podgrabinska S, Shiraishi K, Chawengsaksophak K, Rossant J, Accili D, Skobe M, Kitajewski J (2007) Notch alters VEGF responsiveness in human and murine endothelial cells by direct regulation of VEGFR-3 expression. J Clin Invest 117:3369-3382 (Pubitemid 350096993)
31. Wu J.K., Kitajewski J.K. (2009) A potential role for Notch signaling in the pathogenesis and regulation of hemangiomas. J Craniofac Surg 20(1):698-702
32. Joutel A, Andreux F, Gaulis S, Domenga V, Cecillon M, Battail N, Piga N, Chapon F, Godfrain C, Tournier-Lasserve E (2000) The ectodomain of the Notch3 receptor accumulates within the cerebrovasculature of CADASIL patients. J Clin Invest 105: 597-605 (Pubitemid 30146506)
33. Doi H, Iso T, Shiba Y, Sato H, Yamazaki M, Oyama Y, Akiyama H, Tanaka T, Tomita T, Arai M, Takahashi M, Ikeda U, Kurabayashi M (2009) Notch signaling regulates the differentiation of bone marrow-derived cells into smooth muscle-like cells during arterial lesion formation. Biochem Biophys Res Commun 381: 654-659
34. Benedito R, Roca C, Sorensen I, Adams S, Gossler A, Fruttiger M, Adams RH (2009) The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137:1124-1135
35. Liu H, Kennard S, Lilly B (2009) NOTCH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1. Circ Res 104:466-475