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Published in: Angiogenesis 2/2009

01-06-2009 | Original Paper

Vasculogenesis in infantile hemangioma

Authors: Elisa Boscolo, Joyce Bischoff

Published in: Angiogenesis | Issue 2/2009

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Abstract

Infantile hemangioma is a vascular tumor that occurs in 5–10% of infants of European descent. A defining feature of infantile hemangioma is the dramatic growth and development into a disorganized mass of blood vessels. Subsequently, a slow spontaneous involution begins around 1 year of age and continues for 4–6 years. The growth and involution of infantile hemangioma is very different from other vascular tumors and vascular malformations, which do not regress and can occur at any time during childhood or adult life. Much has been learned from careful study of the tissue morphology and gene expression patterns during the life-cycle of hemangioma. Tissue explants and tumor-derived cell populations have provided further insight to unravel the cellular and molecular basis of infantile hemangioma. A multipotent progenitor cell capable of de novo blood vessel formation has been isolated from infantile hemangioma, which suggests that this common tumor of infancy, long considered to be a model for pathologic angiogenesis, may also represent pathologic vasculogenesis. Whether viewed as angiogenesis or vasculogenesis, infantile hemangioma represents a vascular perturbation during a critical period of post-natal growth, and as such provides a unique opportunity to decipher mechanisms of human vascular development.
Literature
1.
2.
3.
go back to reference Haggstrom AN, Drolet BA, Baselga E, Chamlin SL, Garzon MC, Horii KA, Lucky AW, Mancini AJ, Metry DW, Newell B et al (2007) Prospective study of infantile hemangiomas: demographic, prenatal, and perinatal characteristics. J Pediatr 150:291–294PubMedCrossRef Haggstrom AN, Drolet BA, Baselga E, Chamlin SL, Garzon MC, Horii KA, Lucky AW, Mancini AJ, Metry DW, Newell B et al (2007) Prospective study of infantile hemangiomas: demographic, prenatal, and perinatal characteristics. J Pediatr 150:291–294PubMedCrossRef
4.
go back to reference Frieden IJ, Haggstrom AN, Drolet BA, Mancini AJ, Friedlander SF, Boon L, Chamlin SL, Baselga E, Garzon MC, Nopper AJ et al (2005) Infantile hemangiomas: current knowledge, future directions. In: Proceedings of a research workshop on infantile hemangiomas, April 7–9, 2005, Bethesda. Pediatr Dermatol 22:383–406 Frieden IJ, Haggstrom AN, Drolet BA, Mancini AJ, Friedlander SF, Boon L, Chamlin SL, Baselga E, Garzon MC, Nopper AJ et al (2005) Infantile hemangiomas: current knowledge, future directions. In: Proceedings of a research workshop on infantile hemangiomas, April 7–9, 2005, Bethesda. Pediatr Dermatol 22:383–406
5.
go back to reference Metry DW, Haggstrom AN, Drolet BA, Baselga E, Chamlin S, Garzon M, Horii K, Lucky A, Mancini AJ, Newell B et al (2006) A prospective study of PHACE syndrome in infantile hemangiomas: demographic features, clinical findings, and complications. Am J Med Genet A 140:975–986PubMed Metry DW, Haggstrom AN, Drolet BA, Baselga E, Chamlin S, Garzon M, Horii K, Lucky A, Mancini AJ, Newell B et al (2006) A prospective study of PHACE syndrome in infantile hemangiomas: demographic features, clinical findings, and complications. Am J Med Genet A 140:975–986PubMed
6.
go back to reference Huang SA, Tu HM, Harney JW, Venihaki M, Butte AJ, Kozakewich HP, Fishman SJ, Larsen PR (2000) Severe hypothyroidism caused by type 3 iodothyronine deiodinase in infantile hemangiomas. N Engl J Med 343:185–189PubMedCrossRef Huang SA, Tu HM, Harney JW, Venihaki M, Butte AJ, Kozakewich HP, Fishman SJ, Larsen PR (2000) Severe hypothyroidism caused by type 3 iodothyronine deiodinase in infantile hemangiomas. N Engl J Med 343:185–189PubMedCrossRef
7.
go back to reference Boon LM, MacDonald DM, Mulliken JB (1999) Complications of systemic corticosteroid therapy for problematic hemangioma. Plast Reconstr Surg 104:1616–1623PubMedCrossRef Boon LM, MacDonald DM, Mulliken JB (1999) Complications of systemic corticosteroid therapy for problematic hemangioma. Plast Reconstr Surg 104:1616–1623PubMedCrossRef
8.
go back to reference Enjolras O, Breviere GM, Roger G, Tovi M, Pellegrino B, Varotti E, Soupre V, Picard A, Leverger G (2004) Vincristine treatment for function- and life-threatening infantile hemangioma. Arch Pediatr 11:99–107PubMedCrossRef Enjolras O, Breviere GM, Roger G, Tovi M, Pellegrino B, Varotti E, Soupre V, Picard A, Leverger G (2004) Vincristine treatment for function- and life-threatening infantile hemangioma. Arch Pediatr 11:99–107PubMedCrossRef
9.
go back to reference Fawcett SL, Grant I, Hall PN, Kelsall AW, Nicholson JC (2004) Vincristine as a treatment for a large haemangioma threatening vital functions. Br J Plast Surg 57:168–171PubMedCrossRef Fawcett SL, Grant I, Hall PN, Kelsall AW, Nicholson JC (2004) Vincristine as a treatment for a large haemangioma threatening vital functions. Br J Plast Surg 57:168–171PubMedCrossRef
10.
go back to reference Ezekowitz RA, Mulliken JB, Folkman J (1992) Interferon alfa-2a therapy for life-threatening hemangiomas of infancy. N Engl J Med 326:1456–1463PubMed Ezekowitz RA, Mulliken JB, Folkman J (1992) Interferon alfa-2a therapy for life-threatening hemangiomas of infancy. N Engl J Med 326:1456–1463PubMed
11.
go back to reference Chang E, Boyd A, Nelson CC, Crowley D, Law T, Keough KM, Folkman J, Ezekowitz RA, Castle VP (1997) Successful treatment of infantile hemangiomas with interferon-alpha-2b. J Pediatr Hematol Oncol 19:237–244PubMedCrossRef Chang E, Boyd A, Nelson CC, Crowley D, Law T, Keough KM, Folkman J, Ezekowitz RA, Castle VP (1997) Successful treatment of infantile hemangiomas with interferon-alpha-2b. J Pediatr Hematol Oncol 19:237–244PubMedCrossRef
12.
go back to reference Barlow CF, Priebe CJ, Mulliken JB, Barnes PD, Mac Donald D, Folkman J, Ezekowitz RA (1998) Spastic diplegia as a complication of interferon Alfa-2a treatment of hemangiomas of infancy. J Pediatr 132:527–530PubMedCrossRef Barlow CF, Priebe CJ, Mulliken JB, Barnes PD, Mac Donald D, Folkman J, Ezekowitz RA (1998) Spastic diplegia as a complication of interferon Alfa-2a treatment of hemangiomas of infancy. J Pediatr 132:527–530PubMedCrossRef
13.
go back to reference Greinwald JH Jr, Burke DK, Bonthius DJ, Bauman NM, Smith RJ (1999) An update on the treatment of hemangiomas in children with interferon alfa-2a. Arch Otolaryngol Head Neck Surg 125:21–27PubMed Greinwald JH Jr, Burke DK, Bonthius DJ, Bauman NM, Smith RJ (1999) An update on the treatment of hemangiomas in children with interferon alfa-2a. Arch Otolaryngol Head Neck Surg 125:21–27PubMed
14.
go back to reference Leaute-Labreze C, Dumas de la Roque E, Hubiche T, Boralevi F, Thambo JB, Taieb A (2008) Propranolol for severe hemangiomas of infancy. N Engl J Med 358:2649–2651PubMedCrossRef Leaute-Labreze C, Dumas de la Roque E, Hubiche T, Boralevi F, Thambo JB, Taieb A (2008) Propranolol for severe hemangiomas of infancy. N Engl J Med 358:2649–2651PubMedCrossRef
15.
go back to reference Chang LC, Haggstrom AN, Drolet BA, Baselga E, Chamlin SL, Garzon MC, Horii KA, Lucky AW, Mancini AJ, Metry DW et al (2008) Growth characteristics of infantile hemangiomas: implications for management. Pediatrics 122:360–367PubMedCrossRef Chang LC, Haggstrom AN, Drolet BA, Baselga E, Chamlin SL, Garzon MC, Horii KA, Lucky AW, Mancini AJ, Metry DW et al (2008) Growth characteristics of infantile hemangiomas: implications for management. Pediatrics 122:360–367PubMedCrossRef
16.
go back to reference Mancini AJ, Smoller BR (1996) Proliferation and apoptosis within juvenile capillary hemangiomas. Am J Dermatopathol 18:505–514PubMedCrossRef Mancini AJ, Smoller BR (1996) Proliferation and apoptosis within juvenile capillary hemangiomas. Am J Dermatopathol 18:505–514PubMedCrossRef
17.
go back to reference Smoller BR, Apfelberg DB (1993) Infantile (juvenile) capillary hemangioma: a tumor of heterogeneous cellular elements. J Cutan Pathol 20:330–336PubMedCrossRef Smoller BR, Apfelberg DB (1993) Infantile (juvenile) capillary hemangioma: a tumor of heterogeneous cellular elements. J Cutan Pathol 20:330–336PubMedCrossRef
18.
go back to reference 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 93:2357–2364PubMedCrossRef 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 93:2357–2364PubMedCrossRef
19.
go back to reference Chang J, Most D, Bresnick S, Mehrara B, Steinbrech DS, Reinisch J, Longaker MT, Turk AE (1999) Proliferative hemangiomas: analysis of cytokine gene expression and angiogenesis. Plast Reconstr Surg 103:1–9 (discussion 10)PubMedCrossRef Chang J, Most D, Bresnick S, Mehrara B, Steinbrech DS, Reinisch J, Longaker MT, Turk AE (1999) Proliferative hemangiomas: analysis of cytokine gene expression and angiogenesis. Plast Reconstr Surg 103:1–9 (discussion 10)PubMedCrossRef
20.
go back to reference Picard A, Boscolo E, Khan ZA, Bartch TC, Mulliken JB, Vazquez MP, Bischoff J (2008) IGF-2 and FLT-1/VEGF-R1 mRNA levels reveal distinctions and similarities between congenital and common infantile hemangioma. Pediatr Res 63:263–267PubMedCrossRef Picard A, Boscolo E, Khan ZA, Bartch TC, Mulliken JB, Vazquez MP, Bischoff J (2008) IGF-2 and FLT-1/VEGF-R1 mRNA levels reveal distinctions and similarities between congenital and common infantile hemangioma. Pediatr Res 63:263–267PubMedCrossRef
21.
go back to reference 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 hemangioma-derived endothelial cells. Am J Pathol 159:2271–2280PubMed 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 hemangioma-derived endothelial cells. Am J Pathol 159:2271–2280PubMed
22.
go back to reference Yu Y, Flint AF, Mulliken JB, Wu JK, Bischoff J (2004) Endothelial progenitor cells in infantile hemangioma. Blood 103:1373–1375PubMedCrossRef Yu Y, Flint AF, Mulliken JB, Wu JK, Bischoff J (2004) Endothelial progenitor cells in infantile hemangioma. Blood 103:1373–1375PubMedCrossRef
23.
go back to reference North PE, Waner M, Mizeracki A, Mrak RE, Nicholas R, Kincannon J, Suen JY, Mihm MC Jr (2001) A unique microvascular phenotype shared by juvenile hemangiomas and human placenta. Arch Dermatol 137:559–570PubMed North PE, Waner M, Mizeracki A, Mrak RE, Nicholas R, Kincannon J, Suen JY, Mihm MC Jr (2001) A unique microvascular phenotype shared by juvenile hemangiomas and human placenta. Arch Dermatol 137:559–570PubMed
24.
go back to reference Barnes CM, Huang S, Kaipainen A, Sanoudou D, Chen EJ, Eichler GS, Guo Y, Yu Y, Ingber DE, Mulliken JB et al (2005) Evidence by molecular profiling for a placental origin of infantile hemangioma. Proc Natl Acad Sci USA 102:19097–19102PubMedCrossRef Barnes CM, Huang S, Kaipainen A, Sanoudou D, Chen EJ, Eichler GS, Guo Y, Yu Y, Ingber DE, Mulliken JB et al (2005) Evidence by molecular profiling for a placental origin of infantile hemangioma. Proc Natl Acad Sci USA 102:19097–19102PubMedCrossRef
25.
go back to reference Barnes CM, Christison-Lagay EA, Folkman J (2007) The placenta theory and the origin of infantile hemangioma. Lymphat Res Biol 5:245–255PubMedCrossRef Barnes CM, Christison-Lagay EA, Folkman J (2007) The placenta theory and the origin of infantile hemangioma. Lymphat Res Biol 5:245–255PubMedCrossRef
26.
go back to reference Chang EI, Chang EI, Thangarajah H, Hamou C, Gurtner GC (2007) Hypoxia, hormones, and endothelial progenitor cells in hemangioma. Lymphat Res Biol 5:237–243PubMedCrossRef Chang EI, Chang EI, Thangarajah H, Hamou C, Gurtner GC (2007) Hypoxia, hormones, and endothelial progenitor cells in hemangioma. Lymphat Res Biol 5:237–243PubMedCrossRef
27.
go back to reference Pittman KM, Losken HW, Kleinman ME, Marcus JR, Blei F, Gurtner GC, Marchuk DA (2006) No evidence for maternal-fetal microchimerism in infantile hemangioma: a molecular genetic investigation. J Invest Dermatol 126:2533–2538PubMedCrossRef Pittman KM, Losken HW, Kleinman ME, Marcus JR, Blei F, Gurtner GC, Marchuk DA (2006) No evidence for maternal-fetal microchimerism in infantile hemangioma: a molecular genetic investigation. J Invest Dermatol 126:2533–2538PubMedCrossRef
28.
go back to reference Regnier S, Dupin N, Le Danff C, Wassef M, Enjolras O, Aractingi S (2007) Endothelial cells in infantile haemangiomas originate from the child and not from the mother (a fluorescence in situ hybridization-based study). Br J Dermatol 157:158–160PubMedCrossRef Regnier S, Dupin N, Le Danff C, Wassef M, Enjolras O, Aractingi S (2007) Endothelial cells in infantile haemangiomas originate from the child and not from the mother (a fluorescence in situ hybridization-based study). Br J Dermatol 157:158–160PubMedCrossRef
29.
go back to reference Bauland CG, van Steensel MA, Steijlen PM, Rieu PN, Spauwen PH (2006) The pathogenesis of hemangiomas: a review. Plast Reconstr Surg 117:29e–35ePubMedCrossRef Bauland CG, van Steensel MA, Steijlen PM, Rieu PN, Spauwen PH (2006) The pathogenesis of hemangiomas: a review. Plast Reconstr Surg 117:29e–35ePubMedCrossRef
30.
go back to reference Pack GT, Miller TR (1950) Hemangiomas; classification, diagnosis and treatment. Angiology 1:405–426PubMedCrossRef Pack GT, Miller TR (1950) Hemangiomas; classification, diagnosis and treatment. Angiology 1:405–426PubMedCrossRef
31.
go back to reference Virchow R (1863) Die Krankhaften Geschwulste. August Hirschwald, Berlin Virchow R (1863) Die Krankhaften Geschwulste. August Hirschwald, Berlin
32.
go back to reference Pack G (1950) Hemangiomas, classification, diagnosis, and treatment. Angiology 1:40CrossRef Pack G (1950) Hemangiomas, classification, diagnosis, and treatment. Angiology 1:40CrossRef
33.
go back to reference Malan E (1974) Vascular Malformations (Angiodysplasias). Carlo Erba Foundation, Milan, p 4 Malan E (1974) Vascular Malformations (Angiodysplasias). Carlo Erba Foundation, Milan, p 4
34.
go back to reference Mulliken JB, Zetter BR, Folkman J (1982) In vitro characteristics of endothelium from hemangiomas and vascular malformations. Surgery 92:348–353PubMed Mulliken JB, Zetter BR, Folkman J (1982) In vitro characteristics of endothelium from hemangiomas and vascular malformations. Surgery 92:348–353PubMed
35.
go back to reference Dosanjh A, Chang J, Bresnick S, Zhou L, Reinisch J, Longaker M, Karasek M (2000) In vitro characteristics of neonatal hemangioma endothelial cells: similarities and differences between normal neonatal and fetal endothelial cells. J Cutan Pathol 27:441–450PubMedCrossRef Dosanjh A, Chang J, Bresnick S, Zhou L, Reinisch J, Longaker M, Karasek M (2000) In vitro characteristics of neonatal hemangioma endothelial cells: similarities and differences between normal neonatal and fetal endothelial cells. J Cutan Pathol 27:441–450PubMedCrossRef
36.
go back to reference 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 107:745–752PubMedCrossRef 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 107:745–752PubMedCrossRef
37.
go back to reference Dadras SS, North PE, Bertoncini J, Mihm MC, Detmar M (2004) Infantile hemangiomas are arrested in an early developmental vascular differentiation state. Mod Pathol 17:1068–1079PubMedCrossRef Dadras SS, North PE, Bertoncini J, Mihm MC, Detmar M (2004) Infantile hemangiomas are arrested in an early developmental vascular differentiation state. Mod Pathol 17:1068–1079PubMedCrossRef
38.
go back to reference 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 33:295–303PubMedCrossRef 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 33:295–303PubMedCrossRef
39.
go back to reference Khan ZA, Melero-Martin JM, 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 108:915–921PubMedCrossRef Khan ZA, Melero-Martin JM, 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 108:915–921PubMedCrossRef
40.
go back to reference O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88:277–285PubMedCrossRef O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88:277–285PubMedCrossRef
41.
go back to reference Kleinman ME, Tepper OM, Capla JM, Bhatt KA, Ceradini DJ, Galiano RD, Blei F, Levine JP, Gurtner GC (2003) Increased circulating AC133+ CD34+ endothelial progenitor cells in children with hemangioma. Lymphat Res Biol 1:301–307PubMedCrossRef Kleinman ME, Tepper OM, Capla JM, Bhatt KA, Ceradini DJ, Galiano RD, Blei F, Levine JP, Gurtner GC (2003) Increased circulating AC133+ CD34+ endothelial progenitor cells in children with hemangioma. Lymphat Res Biol 1:301–307PubMedCrossRef
42.
go back to reference Ozerdem U, Grako KA, Dahlin-Huppe K, Monosov E, Stallcup WB (2001) NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev Dyn 222:218–227PubMedCrossRef Ozerdem U, Grako KA, Dahlin-Huppe K, Monosov E, Stallcup WB (2001) NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev Dyn 222:218–227PubMedCrossRef
43.
go back to reference Tigges U, Hyer EG, Scharf J, Stallcup WB (2008) FGF2-dependent neovascularization of subcutaneous Matrigel plugs is initiated by bone marrow-derived pericytes and macrophages. Development 135:523–532PubMedCrossRef Tigges U, Hyer EG, Scharf J, Stallcup WB (2008) FGF2-dependent neovascularization of subcutaneous Matrigel plugs is initiated by bone marrow-derived pericytes and macrophages. Development 135:523–532PubMedCrossRef
44.
go back to reference Li Q, Yu Y, Bischoff J, Mulliken JB, Olsen BR (2003) Differential expression of CD146 in tissues and endothelial cells derived from infantile haemangioma and normal human skin. J Pathol 201:296–302PubMedCrossRef Li Q, Yu Y, Bischoff J, Mulliken JB, Olsen BR (2003) Differential expression of CD146 in tissues and endothelial cells derived from infantile haemangioma and normal human skin. J Pathol 201:296–302PubMedCrossRef
45.
go back to reference Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313PubMedCrossRef Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313PubMedCrossRef
46.
go back to reference Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD, Graff JM (2008) White fat progenitor cells reside in the adipose vasculature. Science 322:583–586PubMedCrossRef Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD, Graff JM (2008) White fat progenitor cells reside in the adipose vasculature. Science 322:583–586PubMedCrossRef
47.
go back to reference Khan ZA, Boscolo E, Picard A, Psutka S, Melero-Martin JM, Bartch TC, Mulliken JB, Bischoff J (2008) Multipotential stem cells recapitulate human infantile hemangioma in immunodeficient mice. J Clin Invest 118:2592–2599PubMed Khan ZA, Boscolo E, Picard A, Psutka S, Melero-Martin JM, Bartch TC, Mulliken JB, Bischoff J (2008) Multipotential stem cells recapitulate human infantile hemangioma in immunodeficient mice. J Clin Invest 118:2592–2599PubMed
48.
go back to reference 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 99:7455–7460PubMedCrossRef 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 99:7455–7460PubMedCrossRef
49.
go back to reference North PE, Waner M, Mizeracki A, Mihm MC Jr (2000) GLUT1: a newly discovered immunohistochemical marker for juvenile hemangiomas. Hum Pathol 31:11–22PubMedCrossRef North PE, Waner M, Mizeracki A, Mihm MC Jr (2000) GLUT1: a newly discovered immunohistochemical marker for juvenile hemangiomas. Hum Pathol 31:11–22PubMedCrossRef
50.
go back to reference Melero-Martin JM, De Obaldia ME, Kang SY, Khan ZA, Yuan L, Oettgen P, Bischoff J (2008) Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 103:194–202PubMedCrossRef Melero-Martin JM, De Obaldia ME, Kang SY, Khan ZA, Yuan L, Oettgen P, Bischoff J (2008) Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 103:194–202PubMedCrossRef
51.
52.
go back to reference Au P, Tam J, Fukumura D, Jain RK (2008) Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111:4551–4558PubMedCrossRef Au P, Tam J, Fukumura D, Jain RK (2008) Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111:4551–4558PubMedCrossRef
53.
go back to reference Tan ST, Wallis RA, He Y, Davis PF (2004) Mast cells and hemangioma. Plast Reconstr Surg 113:999–1011PubMedCrossRef Tan ST, Wallis RA, He Y, Davis PF (2004) Mast cells and hemangioma. Plast Reconstr Surg 113:999–1011PubMedCrossRef
54.
go back to reference Pasyk KA, Cherry GW, Grabb WC, Sasaki GH (1984) Quantitative evaluation of mast cells in cellularly dynamic and adynamic vascular malformations. Plast Reconstr Surg 73:69–77PubMedCrossRef Pasyk KA, Cherry GW, Grabb WC, Sasaki GH (1984) Quantitative evaluation of mast cells in cellularly dynamic and adynamic vascular malformations. Plast Reconstr Surg 73:69–77PubMedCrossRef
55.
go back to reference Ritter MR, Reinisch J, Friedlander SF, Friedlander M (2006) Myeloid cells in infantile hemangioma. Am J Pathol 168:621–628PubMedCrossRef Ritter MR, Reinisch J, Friedlander SF, Friedlander M (2006) Myeloid cells in infantile hemangioma. Am J Pathol 168:621–628PubMedCrossRef
56.
go back to reference Nguyen VA, Furhapter C, Romani N, Weber F, Sepp N (2004) Infantile hemangioma is a proliferation of beta 4-negative endothelial cells adjacent to HLA-DR-positive cells with dendritic cell morphology. Hum Pathol 35:739–744PubMedCrossRef Nguyen VA, Furhapter C, Romani N, Weber F, Sepp N (2004) Infantile hemangioma is a proliferation of beta 4-negative endothelial cells adjacent to HLA-DR-positive cells with dendritic cell morphology. Hum Pathol 35:739–744PubMedCrossRef
57.
go back to reference Jang YC, Isik FF, Gibran NS (2000) Nerve distribution in hemangiomas depends on the proliferative state of the microvasculature. J Surg Res 93:144–148PubMedCrossRef Jang YC, Isik FF, Gibran NS (2000) Nerve distribution in hemangiomas depends on the proliferative state of the microvasculature. J Surg Res 93:144–148PubMedCrossRef
58.
go back to reference Berard M, Sordello S, Ortega N, Carrier JL, Peyri N, Wassef M, Bertrand N, Enjolras O, Drouet L, Plouet J (1997) Vascular endothelial growth factor confers a growth advantage in vitro and in vivo to stromal cells cultured from neonatal hemangiomas. Am J Pathol 150:1315–1326PubMed Berard M, Sordello S, Ortega N, Carrier JL, Peyri N, Wassef M, Bertrand N, Enjolras O, Drouet L, Plouet J (1997) Vascular endothelial growth factor confers a growth advantage in vitro and in vivo to stromal cells cultured from neonatal hemangiomas. Am J Pathol 150:1315–1326PubMed
59.
go back to reference 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 14:1236–1246PubMedCrossRef 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 14:1236–1246PubMedCrossRef
60.
go back to reference Zhang L, Lin X, Wang W, Zhuang X, Dong J, Qi Z, Hu Q (2005) Circulating level of vascular endothelial growth factor in differentiating hemangioma from vascular malformation patients. Plast Reconstr Surg 116:200–204PubMedCrossRef Zhang L, Lin X, Wang W, Zhuang X, Dong J, Qi Z, Hu Q (2005) Circulating level of vascular endothelial growth factor in differentiating hemangioma from vascular malformation patients. Plast Reconstr Surg 116:200–204PubMedCrossRef
61.
go back to reference Fong GH, Rossant J, Gertsenstein M, Breitman ML (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66–70PubMedCrossRef Fong GH, Rossant J, Gertsenstein M, Breitman ML (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66–70PubMedCrossRef
62.
go back to reference Blei F, Walter J, Orlow SJ, Marchuk DA (1998) Familial segregation of hemangiomas and vascular malformations as an autosomal dominant trait. Arch Dermatol 134:718–722PubMedCrossRef Blei F, Walter J, Orlow SJ, Marchuk DA (1998) Familial segregation of hemangiomas and vascular malformations as an autosomal dominant trait. Arch Dermatol 134:718–722PubMedCrossRef
63.
go back to reference Walter JW, Blei F, Anderson JL, Orlow SJ, Speer MC, Marchuk DA (1999) Genetic mapping of a novel familial form of infantile hemangioma. Am J Med Genet 82:77–83PubMedCrossRef Walter JW, Blei F, Anderson JL, Orlow SJ, Speer MC, Marchuk DA (1999) Genetic mapping of a novel familial form of infantile hemangioma. Am J Med Genet 82:77–83PubMedCrossRef
64.
go back to reference Pramanik K, Chun CZ, Garnaas MK, Samant GV, Li K, Horswill MA, North PE, Ramchandran R (2009) Dusp-5 and Snrk-1 coordinately function during vascular development and disease. Blood 113:1184–1191PubMedCrossRef Pramanik K, Chun CZ, Garnaas MK, Samant GV, Li K, Horswill MA, North PE, Ramchandran R (2009) Dusp-5 and Snrk-1 coordinately function during vascular development and disease. Blood 113:1184–1191PubMedCrossRef
65.
go back to reference Qian F, Zhen F, Ong C, Jin SW, Meng Soo H, Stainier DY, Lin S, Peng J, Wen Z (2005) Microarray analysis of zebrafish cloche mutant using amplified cDNA and identification of potential downstream target genes. Dev Dyn 233:1163–1172PubMedCrossRef Qian F, Zhen F, Ong C, Jin SW, Meng Soo H, Stainier DY, Lin S, Peng J, Wen Z (2005) Microarray analysis of zebrafish cloche mutant using amplified cDNA and identification of potential downstream target genes. Dev Dyn 233:1163–1172PubMedCrossRef
66.
go back to reference Sumanas S, Jorniak T, Lin S (2005) Identification of novel vascular endothelial-specific genes by the microarray analysis of the zebrafish cloche mutants. Blood 106:534–541PubMedCrossRef Sumanas S, Jorniak T, Lin S (2005) Identification of novel vascular endothelial-specific genes by the microarray analysis of the zebrafish cloche mutants. Blood 106:534–541PubMedCrossRef
67.
go back to reference St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, Lal A, Riggins GJ, Lengauer C, Vogelstein B et al (2000) Genes expressed in human tumor endothelium. Science 289:1197–1202PubMedCrossRef St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, Lal A, Riggins GJ, Lengauer C, Vogelstein B et al (2000) Genes expressed in human tumor endothelium. Science 289:1197–1202PubMedCrossRef
68.
go back to reference Arbiser JL, Weiss SW, Arbiser ZK, Bravo F, Govindajaran B, Caceres-Rios H, Cotsonis G, Recavarren S, Swerlick RA, Cohen C (2001) Differential expression of active mitogen-activated protein kinase in cutaneous endothelial neoplasms: implications for biologic behavior and response to therapy. J Am Acad Dermatol 44:193–197PubMedCrossRef Arbiser JL, Weiss SW, Arbiser ZK, Bravo F, Govindajaran B, Caceres-Rios H, Cotsonis G, Recavarren S, Swerlick RA, Cohen C (2001) Differential expression of active mitogen-activated protein kinase in cutaneous endothelial neoplasms: implications for biologic behavior and response to therapy. J Am Acad Dermatol 44:193–197PubMedCrossRef
69.
go back to reference Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD (1996) Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171–1180PubMedCrossRef Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD (1996) Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171–1180PubMedCrossRef
70.
go back to reference Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N et al (1997) Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277:55–60PubMedCrossRef Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N et al (1997) Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277:55–60PubMedCrossRef
71.
go back to reference Hawighorst T, Skobe M, Streit M, Hong YK, Velasco P, Brown LF, Riccardi L, Lange-Asschenfeldt B, Detmar M (2002) Activation of the tie2 receptor by angiopoietin-1 enhances tumor vessel maturation and impairs squamous cell carcinoma growth. Am J Pathol 160:1381–1392PubMed Hawighorst T, Skobe M, Streit M, Hong YK, Velasco P, Brown LF, Riccardi L, Lange-Asschenfeldt B, Detmar M (2002) Activation of the tie2 receptor by angiopoietin-1 enhances tumor vessel maturation and impairs squamous cell carcinoma growth. Am J Pathol 160:1381–1392PubMed
72.
go back to reference Stoeltzing O, Ahmad SA, Liu W, McCarty MF, Parikh AA, Fan F, Reinmuth N, Bucana CD, Ellis LM (2002) Angiopoietin-1 inhibits tumour growth and ascites formation in a murine model of peritoneal carcinomatosis. Br J Cancer 87:1182–1187PubMedCrossRef Stoeltzing O, Ahmad SA, Liu W, McCarty MF, Parikh AA, Fan F, Reinmuth N, Bucana CD, Ellis LM (2002) Angiopoietin-1 inhibits tumour growth and ascites formation in a murine model of peritoneal carcinomatosis. Br J Cancer 87:1182–1187PubMedCrossRef
73.
go back to reference Feng Y, vom Hagen F, Pfister F, Djokic S, Hoffmann S, Back W, Wagner P, Lin J, Deutsch U, Hammes HP (2007) Impaired pericyte recruitment and abnormal retinal angiogenesis as a result of angiopoietin-2 overexpression. Thromb Haemost 97:99–108PubMed Feng Y, vom Hagen F, Pfister F, Djokic S, Hoffmann S, Back W, Wagner P, Lin J, Deutsch U, Hammes HP (2007) Impaired pericyte recruitment and abnormal retinal angiogenesis as a result of angiopoietin-2 overexpression. Thromb Haemost 97:99–108PubMed
74.
go back to reference Perry BN, Govindarajan B, Bhandarkar SS, Knaus UG, Valo M, Sturk C, Carrillo CO, Sohn A, Cerimele F, Dumont D et al (2006) Pharmacologic blockade of angiopoietin-2 is efficacious against model hemangiomas in mice. J Invest Dermatol 126:2316–2322PubMedCrossRef Perry BN, Govindarajan B, Bhandarkar SS, Knaus UG, Valo M, Sturk C, Carrillo CO, Sohn A, Cerimele F, Dumont D et al (2006) Pharmacologic blockade of angiopoietin-2 is efficacious against model hemangiomas in mice. J Invest Dermatol 126:2316–2322PubMedCrossRef
75.
go back to reference Sun JF, Phung T, Shiojima I, Felske T, Upalakalin JN, Feng D, Kornaga T, Dor T, Dvorak AM, Walsh K et al (2005) Microvascular patterning is controlled by fine-tuning the Akt signal. Proc Natl Acad Sci USA 102:128–133PubMedCrossRef Sun JF, Phung T, Shiojima I, Felske T, Upalakalin JN, Feng D, Kornaga T, Dor T, Dvorak AM, Walsh K et al (2005) Microvascular patterning is controlled by fine-tuning the Akt signal. Proc Natl Acad Sci USA 102:128–133PubMedCrossRef
76.
go back to reference Phung TL, Ziv K, Dabydeen D, Eyiah-Mensah G, Riveros M, Perruzzi C, Sun J, Monahan-Earley RA, Shiojima I, Nagy JA et al (2006) Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10:159–170PubMedCrossRef Phung TL, Ziv K, Dabydeen D, Eyiah-Mensah G, Riveros M, Perruzzi C, Sun J, Monahan-Earley RA, Shiojima I, Nagy JA et al (2006) Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10:159–170PubMedCrossRef
77.
go back to reference Kleinman ME, Greives MR, Churgin SS, Blechman KM, Chang EI, Ceradini DJ, Tepper OM, Gurtner GC (2007) Hypoxia-induced mediators of stem/progenitor cell trafficking are increased in children with hemangioma. Arterioscler Thromb Vasc Biol 27:2664–2670PubMedCrossRef Kleinman ME, Greives MR, Churgin SS, Blechman KM, Chang EI, Ceradini DJ, Tepper OM, Gurtner GC (2007) Hypoxia-induced mediators of stem/progenitor cell trafficking are increased in children with hemangioma. Arterioscler Thromb Vasc Biol 27:2664–2670PubMedCrossRef
78.
go back to reference Isik FF, Rand RP, Gruss JS, Benjamin D, Alpers CE (1996) Monocyte chemoattractant protein-1 mRNA expression in hemangiomas and vascular malformations. J Surg Res 61:71–76PubMedCrossRef Isik FF, Rand RP, Gruss JS, Benjamin D, Alpers CE (1996) Monocyte chemoattractant protein-1 mRNA expression in hemangiomas and vascular malformations. J Surg Res 61:71–76PubMedCrossRef
79.
go back to reference 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 148:1181–1191PubMed 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 148:1181–1191PubMed
80.
go back to reference Oh IY, Yoon CH, Hur J, Kim JH, Kim TY, Lee CS, Park KW, Chae IH, Oh BH, Park YB et al (2007) Involvement of E-selectin in recruitment of endothelial progenitor cells and angiogenesis in ischemic muscle. Blood 110:3891–3899PubMedCrossRef Oh IY, Yoon CH, Hur J, Kim JH, Kim TY, Lee CS, Park KW, Chae IH, Oh BH, Park YB et al (2007) Involvement of E-selectin in recruitment of endothelial progenitor cells and angiogenesis in ischemic muscle. Blood 110:3891–3899PubMedCrossRef
81.
go back to reference Gainers ME, Descheny L, Barthel SR, Liu L, Wurbel MA, Dimitroff CJ (2007) Skin-homing receptors on effector leukocytes are differentially sensitive to glyco-metabolic antagonism in allergic contact dermatitis. J Immunol 179:8509–8518PubMed Gainers ME, Descheny L, Barthel SR, Liu L, Wurbel MA, Dimitroff CJ (2007) Skin-homing receptors on effector leukocytes are differentially sensitive to glyco-metabolic antagonism in allergic contact dermatitis. J Immunol 179:8509–8518PubMed
82.
go back to reference Hidalgo A, Weiss LA, Frenette PS (2002) Functional selectin ligands mediating human CD34(+) cell interactions with bone marrow endothelium are enhanced postnatally. J Clin Invest 110:559–569PubMed Hidalgo A, Weiss LA, Frenette PS (2002) Functional selectin ligands mediating human CD34(+) cell interactions with bone marrow endothelium are enhanced postnatally. J Clin Invest 110:559–569PubMed
Metadata
Title
Vasculogenesis in infantile hemangioma
Authors
Elisa Boscolo
Joyce Bischoff
Publication date
01-06-2009
Publisher
Springer Netherlands
Published in
Angiogenesis / Issue 2/2009
Print ISSN: 0969-6970
Electronic ISSN: 1573-7209
DOI
https://doi.org/10.1007/s10456-009-9148-2

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