Active hair growth (anagen) is associated with angiogenesis

Journal of Investigative Dermatology

Volumn 114, Issue 5, 2000, Pages 909-916

  Mecklenburg, Lars ^d   Tobin, Desmond J ^d   Müller Röver, Sven ^a   Handjiski, Bori ^b   Wendt, Gunnar ^d   Peters, Eva M J ^d   Pohl, Susanne ^d   Moll, Ingrid ^d   Paus, Ralf ^c  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d NONE

Author keywords

C57BL 6; PECAM 1; Skin; TNP 470

Indexed keywords

ANGIOGENESIS INHIBITOR; FUMAGILLOL CHLOROACETYLCARBAMATE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HAIR GROWTH; MORPHOMETRICS; MOUSE; NONHUMAN; PERFUSION; PRIORITY JOURNAL; QUANTITATIVE DIAGNOSIS; SKIN BLOOD FLOW;

EID: 0034023353     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.2000.00954.x     Document Type: Article

References (69)

1. Albelda SM, Muller WA, Buck CA, Newman PJ: Molecular and cellular properties of PECAM-1 (endoCAM/CD31): a novel vascular cell-cell adhesion molecule. J Cell Biol 114:1059-1068, 1991
2. Antoine N, Daukandt M, Heinen M, Simar LJ, Castronovo V: In vitro and in vivo stimulation of the murine immune system by AGM-1470, a potent angiogenesis inhibitor. Am J Pathol 148:393-398, 1996
3. Arnold F, West DC: Angiogenesis in wound healing. Pharmac Ther 52:407-422, 1991
4. Auerbach R, Auerbach W, Polakowski I: Assays for angiogenesis: a review. Pharmac Ther 51:1-11, 1991
5. Botchkarev VA, Eichmüller S, Peters EMJ, Pietsch P, Johansson O, Maurer M, Paus R: A simple fluorescent technique for co-visualization of mast cells and nerve fibres reveals selectivity and hair cycle-dependent changes in mast cell-nerve fibre contacts in skin. Arch Dermatol Res 289:292-303, 1997
6. Botchkarev VA, Welker P, Albers KM, et al: A new role for neurotrophine-3: Involvement in the regulation of hair follicle regression (catagen). Am J Pathol 153:785-799, 1998
7. Botchkarev VA, Botchkareva NV, Welker P, et al: A new role for neurotrophins: involvement of brain-derived neurotrophic factor and neurotrophin-4 in hair cycle control. FASEB J 13:395-410, 1999
8. Braverman IM: The cutaneous microcirculation: ultrastructure and microanatomical organization. Microcirculation 4:329-340, 1997
9. Braverman IM: Cutaneous microvasculature. In: Freedberg IM, Eisen AZ, Wolff K, et al, eds. Fitzpatrick's Dermatology in General Medicine. New York: McGraw-Hill, 1999, pp 299-320
10. Bujan J, Gimeno MJ, Prieto A, Pascual G, Bellon JM, Alvarez-Mon M: Modulation of PECAM-1 (CD31) expression in human endothelial cells: effect of IFNgamma and IL-10. J Vasc Res 36:106-113, 1999
11. Castronovo V, Belotti D: TNP-470 (AGM-1470): Mechanisms of action and early clinical development. Eur J Cancer 32A:2520-2527, 1996
12. Chase HB, Montagna W, Malone JD: Changes in the skin in relation to the hair growth cycle. Anat Rec 116:75-82, 1953
13. Christenson LK, Stouffer RL: Proliferation of microvascular endothelial cells in the primate corpus luteum during the menstrual cycle and simulated early pregnancy. Endocrinology 137:367-374, 1996
14. Couffinhal T, Silver M, Zheng LP, Kearney M, Witzenbichler B, Isner JM: Mouse model of angiogenesis. Am J Pathol 152:1667-1679, 1998
15. Creamer D, Allen MH, Sousa A, Poston R, Barker JN: Localization of endothelial proliferation and microvascular expansion in active plaque psoriasis. Br J Dermatol 136:859-865, 1997
16. Detmar M: Molecular regulation of angiogenesis in the skin. J Invest Dermatol 106:207-208, 1996
17. Detmar M, Brown LF, Claffey KP, et al: Overexpression of vascular permeability factor/ vascular endothelial growth factor and its receptors in psoriasis. J Exp Med 180:1141-1146, 1994
18. Detmar M, Brown LF, Schön MP, et al: Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J Invest Dermatol 111:1-6, 1998
19. Dhanabal M, Ramchandran R, Volk R, et al: Endostatin: yeast production, mutants, and antitumor effect in renal cell carcinoma. Cancer Res 59:189-197, 1999
20. Durward A, Rudall KM. The vascularity and patterns of growth of hair follicles. In: Montagna W, Ellis RA, eds. The Biology of Hair Growth. New York: Academic Press, 1958, pp 189-218
21. Eichmüller S, Stevenson PA, Paus R: A new method for double immunolabeling with primary antibodies from identical species. J Immunol Methods 190:255-265, 1996
22. Eichmüller S, van der Veen C, Moll I, Hermes B, Hofmann U, Müller-Röver S, Paus R: Clusters of perifollicular macrophages in normal murine skin: physiological degeneration of selected hair follicles by programmed organ deletion. J Histochem Cytochem 46:361-370, 1998
23. Ellis R, Moretti G: Vascular patterns associated with catagen hair follicles in the human scalp. Ann NY Acad Sci 83:448-457, 1959
24. Folkman J: What is the role of angiogenesis in metastasis from cutaneous melanoma? Eur J Cancer Clin Oncol 23:361-363, 1987
25. Folkman J: What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 82:4-6, 1990
26. Folkman J: Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med 1:27-31, 1995
27. Folkman J: Tumor angiogenesis and tissue factor. Nature Med 2:167-168, 1996
28. Folkman J, Shing Y: Angiogenesis. J Biol Chem 267:10931-10934, 1992
29. Forbes PD. Vascular supply of the skin and hair in swine. In: Montagna W, Dobson RL, eds. Advances in Biology of Skin, Vol IX, Hair Growth. Oxford: Pergamon Press, 1967, pp 419-432
30. Gariano RF, Iruela-Arispe ML, Sage EH, Hendrickson AE: Immunohistochemical characterization of developing and mature retinal blood vessels. Invest Ophthalmol Vis Sci 37:93-103, 1996
31. Gerdes J, Scholzen T, Gerlach C, Kubbutat MHG, Zentgraf H: Assessment of cell proliferation in murine tissues with a polyclonal antiserum against the murine Ki-67 protein. Eur Cell Biol 72 (Suppl. 43):88, 1997
32. Gille J, Khalik M, Konig V, Kaufmann R: Hepatocyte growth factor/scatter factor (HGF/SF) induces vascular permeability factor (VPF/VEGF) expression by cultured keratinocytes. J Invest Dermatol 111:1160-1165, 1998
33. Goldman CK, Tsai JC, Soroceanu L, Gillespie GY: Loss of vascular endothelial growth factor in human alopecia hair follicles. J Invest Dermatol 104:18S-20S, 1995
34. Handjiski B, Eichmüller S, Hofmann U, Czarnetzki BM, Paus R: Alkaline phosphatase activity during the murine hair cycle. Br J Dermatol 131:303-310, 1994
35. Horak ER, Leek R, Klenk N, et al: Angiogenesis, assessed by platelet/endothelial cell adhesion molecule antibodies, as indicator of node metastases and survival in breast cancer. Lancet 340:1120-1124, 1992
36. Hudlická O, Brown MD, Egginton S. Angiogenesis: basic concepts and methodology. In: Halliday A, Hunt BJ, Poston L, Schachter M: eds. An Introduction to Vascular Biology Cambridge: Cambridge University Press, 1998:pp 3-19
37. Ingber D, Fujita T, Kishimoto S, et al: Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature 348:1757-1763, 1990
38. Karnovsky MJ: Formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137-138, 1965
39. Kozlowska U, Blume-Peytavi U, Kodelja V, et al: Expression of vascular endothelial growth factor (VEGF) in various compartments of the human hair follicle. Arch Dermatol Res 290:661-668, 1998
40. Lachgar S, Moukadiri H, Jonca F, et al: Vascular endothelial growth factor is an autocrine growth factor for hair dermal papilla cells. J Invest Dermatol 106:17-23, 1996
41. Lachgar S, Charveron M, Gall Y, Bonafe JL: Minoxidil upregulates the expression of vascular endothelial growth factor in human hair dermal papilla cells. Br J Dermatol 138:407-411, 1998
42. Li L, Paus R, Margolis LB, Hoffman RM: Hair growth in vitro from histocultured skin. In Vitro Cell Dev Biol 28A:479-481, 1992
43. Lindner G, Menrad A, Gherardi E, et al: Involvement of hepatocyte growth factor/ scatter factor and Met receptor signaling in hair follicle morphogenesis and cycling. FASEB J 14:319-332, 2000
44. Matsumoto M, Nishinakagawa H, Kurohmaru M, Hayashi Y, Otsuka J: Pregnancy affects the microvasculature of the mammalian gland in mice. J Vet Med Sci 54:937-943, 1992
45. Montagna W, Parakkal PF: The Structure and Function of Skin New York, Academic Press, 1974:pp 142-156
46. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z: Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13:9-22, 1999
47. Ohsawa M, Naka N, Tomita Y, Kawamori D, Aozasa K: Use of immunohistochemical procedures in diagnosing angiosarcoma. Evaluation of 98 cases. Cancer 75:2867-2874, 1995
48. O'Reilly MS, Holmgren L, Shing Y, et al: Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79:315-328, 1994
49. Paus R, Cotsarelis G: The biology of hair follicles. N Engl J Med 341:491-497, 1999
50. Paus R, Stenn KS, Link RE: Telogen skin contains an inhibitor of hair growth. Br J Dermatol 122:777-784, 1990
51. Paus R, Maurer M, Slominski A, Czarnetzki BM: Mast cell involvement in murine hair growth. Dev Biol 163:230-249, 1994
52. Paus R, Foitzik K, Welker P, Bulfone-Paus S, Eichmüller S: Transforming growth factor-β receptor type I and type II expression during murine hair follicle development and cycling. J Invest Dermatol 109:518-526, 1997
53. Paus R, van der Veen C, Eichmüller S, Kopp T, Hagen E, Müller-Röver S, Hofmann U: Generation and cyclic remodelling of the hair follicle immune system in mice. J Invest Dermatol 111:7-18, 1998
54. Paus R, Müller-Röver S, Van der Veen C, et al: A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis. J Invest Dermatol 113:523-532, 1999
55. Seghezzi G, Patel S, Ren CJ, et al: Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angtogenesis. J Cell Biol 141:1659-1673, 1998
56. Sholley MM, Cotran RS: Endothelial DNA synthesis in the microvasculature of rat skin during the hair growth cycle. Am J Anat 147:243-254, 1976
57. Slominski A, Paus R: Melanogenesis is coupled to murine anagen: toward new concepts for the role of melanocytes and the regulation of melanogenesis in hair growth. J Invest Dermatol 101:90S-97S, 1993
58. Slominski A, Paus R, Costantino R: Differential expression and activity of melanogenesis-related proteins during induced hair growth in mice. J Invest Dermatol 96:172-179, 1991
59. Slominski A, Paus R, Plonka P, Handjiski B, Maurer M, Chakraborty A, Mihm C: Pharmacological disruption of hair follicle pigmentation by cyclophosphamide as a model for studying the melanocyte response to and recovery from cytotoxic drug damage in situ. J Invest Dermatol 106:1203-1211, 1996
60. Stenn MD, Fernandez LA, Tirell SJ: The angiogenic properties of the rat vibrissa hair follicle associate with the bulb. J Invest Dermatol 90:409-411, 1988
61. Suri C, McClain J, Thurston G, et al: Increased vascularization in mice overexpressing angiopoietin-1. Science 282:468-471, 1998
62. Tobin DJ, Fenton DA, Kendall MD: Cell degeneration in alopecia areata. Am J Dermatol 13:248-256, 1991
63. Tobin DJ, Hageb E, Botchkarev VA, Paus R: Do hair bulb melanocytes undergo apoptosis during hair follicle regression (catagen)? J Invest Dermatol 111:941-947, 1998
64. Vartanian RK, Weidner N: Correlation of intratumoral endothelial cell proliferation with microvessel density (tumor angiogenesis) and tumor cell proliferation in breast carcinoma. Am J Pathol 144:1188-1194, 1994
65. Vermeulen PB, Verhoeven D, Hubens G, et al: Microvessel density, endothelial cell proliferation and tumour cell proliferation in human colorectal adenocarcinomas. Ann Oncol 6:59-64, 1995
66. Vermeulen PB, Dirix LY, Libura J, Vanhoolst IF, Van Marck E, Van Oosterom AT: Correlation of the fractions of proliferating tumor and endothelial cells in breast and colorectal adenocarcinoma is independent of tumor histiotype and microvessel density. Microvascular Res 54:88-92, 1997
67. Wang D, Huang HJ, Kazlauskas A, Cavenee WK: Induction of vascular endothelial growth factor expression in endothelial cells by platelet-derived growth factor through the activation of phosphatidylinositol 3-kinase. Cancer Res 59:1464-1472, 1999
68. Wojta J, Kaun C, Breuss JM, et al: Hepatocyte growth factor increases expression of vascular endothelial growth factor and plasminogen activator inhibitor-1 in human keratinocytes and the vascular endothelial growth factor receptor flk-1 in human endothelial cells. Lab Invest 79:427-438, 1999
69. Wong J, Wang N, Miller JW, Schuman JS: Modulation of human fibroblast activity by selected angiogenesis inhibitors. Exp Eye Res 58:439-451, 1994