Tumour vascularization: sprouting angiogenesis and beyond.
Tumour angiogenesis is a fast growing domain in tumour biology. Many growth factors and mechanisms have been unravelled. For almost 30 years, the sprouting of new vessels out of existing ones was considered as an exclusive way of tumour vascularisation. However, over the last years several additional mechanisms have been identified. With the discovery of the contribution of intussusceptive angiogenesis, recruitment of endothelial progenitor cells, vessel co-option, vasculogenic mimicry and lymphangiogenesis to tumour growth, anti-tumour targeting strategies will be more complex than initially thought. This review highlights these processes and intervention as a potential application in cancer therapy. It is concluded that future anti-vascular therapies might be most beneficial when based on multimodal anti-angiogenic, anti-vasculogenic mimicry and anti-lymphangiogenic strategies.
Hillen
Femke
F
Angiogenesis Laboratory, Research Institute for Growth and Development (GROW), Department of Pathology, Maastricht University & University Hospital Maastricht, P.O. Box 5800, 6202, AZ Maastricht, The Netherlands.
Griffioen
Arjan W
AW
D000818:Animals; D042783:Endothelial Cells / Q000166:cytology; D006801:Humans; D008200:Lymphangiectasis; D009369:Neoplasms / Q000098:blood supply*; D009389:Neovascularization, Pathologic / Q000209:etiology*; D013234:Stem Cells / Q000502:physiology; D042461:Vascular Endothelial Growth Factor A / Q000502:physiology
D042461:Vascular Endothelial Growth Factor A
Am J Pathol. 2001 Apr;158(4):1279-88
11290546
Arch Dermatol. 2001 Apr;137(4):471-4
11295928
Nat Med. 2001 May;7(5):575-83
11329059
Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):8018-23
11416160
Ann N Y Acad Sci. 2001 Jun;938:36-45; discussion 45-7
11458524
Cancer Res. 2001 Sep 1;61(17):6322-7
11522618
EMBO J. 2001 Sep 3;20(17):4762-73
11532940
Cancer Res. 2001 Sep 15;61(18):6624-8
11559524
Nat Med. 2001 Nov;7(11):1194-201
11689883
N Engl J Med. 2004 Jul 15;351(3):250-9
15254283
Ann Surg. 2004 Aug;240(2):306-12
15273556
Proc Natl Acad Sci U S A. 2004 Aug 10;101(32):11658-63
15289610
Blood. 2004 Sep 15;104(6):1769-77
15187022
Blood. 2004 Oct 1;104(7):2084-6
15191949
J Natl Cancer Inst. 2004 Oct 6;96(19):1473-7
15467037
Dev Dyn. 2004 Nov;231(3):474-88
15376313
Trends Genet. 2004 Nov;20(11):563-9
15475116
Cancer Cell. 2004 Oct;6(4):333-45
15488757
Circulation. 2004 Oct 26;110(17):2673-7
15313945
Anat Rec. 1986 Oct;216(2):154-64
3777448
Cell. 1989 Feb 10;56(3):345-55
2464438
Endocrinology. 1991 Aug;129(2):896-900
1855480
J Natl Cancer Inst. 1993 Jan 20;85(2):121-31
8418301
Ophthalmology. 1993 Sep;100(9):1389-98
8371929
Anat Embryol (Berl). 1993 Feb;187(2):121-30
8238959
Cell. 1994 Oct 21;79(2):315-28
7525077
J Neurosurg. 1994 Dec;81(6):902-9
7525899
J Natl Cancer Inst. 1995 Feb 15;87(4):304-9
7707422
Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3566-70
7724599
J Exp Med. 1995 Jul 1;182(1):219-31
7790818
J Exp Med. 1995 Nov 1;182(5):1337-43
7595204
Nat Med. 1995 Feb;1(2):149-53
7585012
Surgery. 1996 Mar;119(3):333-9
8619189
Microvasc Res. 1996 Mar;51(2):260-72
8778579
Cell. 1996 Dec 27;87(7):1161-9
8980223
Cell. 1997 Jan 24;88(2):277-85
9008168
Science. 1997 Feb 14;275(5302):964-7
9020076
Am J Pathol. 1997 Dec;151(6):1523-30
9403702
Mol Cancer Ther. 2002 Nov;1(13):1173-9
12479698
Med Res Rev. 2003 Mar;23(2):117-45
12500286
Clin Cancer Res. 2003 Jan;9(1):377-82
12538491
J Immunol. 2003 Mar 15;170(6):3369-76
12626597
Cancer Biol Ther. 2003 May-Jun;2(3):255-6
12878859
Science. 2003 Jul 25;301(5632):452-4
12881543
Cancer Cell. 2003 Jul;4(1):19-29
12892710
Cancer Lett. 2003 Jul 30;198(1):83-8
12893434
J Clin Oncol. 2005 Sep 20;23(27):6533-9
16116151
Br J Cancer. 2005 Sep 19;93(6):688-93
16136051
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15593-8
16230630
Cancer Res. 2005 Nov 1;65(21):9851-60
16267008
Cancer Res. 2005 Nov 15;65(22):10164-9
16288000
Cancer Cell. 2005 Dec;8(6):443-54
16338658
Nature. 2005 Dec 15;438(7070):932-6
16355210
Nature. 2005 Dec 15;438(7070):946-53
16355212
Nature. 2005 Dec 15;438(7070):967-74
16355214
Cancer Res. 2005 Dec 15;65(24):11520-8
16357161
Eur J Cancer. 2006 Feb;42(3):357-62
16377180
Anticancer Res. 2006 Jan-Feb;26(1A):59-69
16475680
N Engl J Med. 2006 Mar 2;354(9):980-2; discussion 980-2
16510760
N Engl J Med. 2006 Mar 2;354(9):980-2; discussion 980-2
16514715
Br J Cancer. 2006 May 22;94(10):1355-60
16641900
Cancer Res. 2006 Jun 1;66(11):5696-706
16740707
Trends Cell Biol. 2006 Jun;16(6):293-300
16697642
Nat Med. 2006 Aug;12(8):925-32
16892036
J Pathol. 2001 Dec;195(5):537-42
11745688
Cancer Res. 2002 Jan 15;62(2):560-6
11809710
Nat Immunol. 2002 Feb;3(2):143-50
11812991
Prostate. 2002 Feb 15;50(3):189-201
11813211
Science. 2002 Feb 22;295(5559):1526-8
11859195
Cancer Res. 2002 Mar 15;62(6):1847-53
11912164
Invest Ophthalmol Vis Sci. 2002 Apr;43(4):912-8
11923228
Genes Dev. 2002 Apr 1;16(7):773-83
11937485
Trends Cardiovasc Med. 2002 Apr;12(3):128-34
12007738
Cell. 2002 May 31;109(5):625-37
12062105
J Pathol. 2002 Jul;197(3):355-62
12115882
Nat Med. 2002 Aug;8(8):841-9
12091880
Nat Rev Cancer. 2002 Aug;2(8):573-83
12154350
Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11399-404
12177446
Dev Dyn. 2002 Aug;224(4):391-402
12203731
Dev Cell. 2002 Sep;3(3):411-23
12361603
Development. 2002 Oct;129(20):4797-806
12361971
Am J Pathol. 2002 Oct;161(4):1235-46
12368197
Oncogene. 2002 Oct 10;21(46):7011-26
12370823
J Histochem Cytochem. 2002 Nov;50(11):1555-62
12417622
J Exp Med. 2002 Dec 2;196(11):1497-506
12461084
Cancer Res. 2003 Sep 1;63(17):5381-9
14500372
Ann Rheum Dis. 2003 Nov;62 Suppl 2:ii60-7
14532152
J Cell Biol. 2003 Oct 27;163(2):209-13
14581448
Cancer Cell. 2003 Oct;4(4):277-89
14585355
Nat Med. 2003 Nov;9(11):1370-6
14556003
J Biol Chem. 2000 Jul 14;275(28):21340-8
10766752
Blood. 2000 Jul 1;96(1):176-81
10891448
Nature. 2000 Aug 17;406(6797):747-52
10963602
Nature. 2000 Sep 14;407(6801):249-57
11001068
Nat Cell Biol. 2000 Oct;2(10):737-44
11025665
Clin Cancer Res. 2000 Nov;6(11):4442-8
11106265
Microsc Res Tech. 2001 Jan 15;52(2):182-9
11169866
Nat Med. 2001 Feb;7(2):186-91
11175849
Nat Med. 2001 Feb;7(2):192-8
11175850
Cancer Res. 2001 Mar 1;61(5):1786-90
11280723
Am J Hematol. 2001 May;67(1):51-3
11279658
Mol Cancer Ther. 2006 Dec;5(12):3078-84
17172410
Cancer Metastasis Rev. 2006 Dec;25(4):677-94
17160713
Circ Res. 2007 Feb 2;100(2):204-12
17218606
Breast Cancer Res. 2006;8(6):R69
17156488
Biochem Biophys Res Commun. 2007 Mar 30;355(1):1-5
17276388
Cancer Lett. 2007 May 8;249(2):188-97
16997457
Oncogene. 2007 Jun 14;26(28):4158-70
17173062
Cancer Lett. 2007 Aug 28;254(1):128-36
17442484
Eye (Lond). 2008 Jul;22(7):948-52
17363922
Nat Med. 2003 Jun;9(6):669-76
12778165
Nat Med. 2003 Jun;9(6):685-93
12778167
Nat Rev Cancer. 2003 Jun;3(6):411-21
12778131
Cancer Res. 2003 Jun 1;63(11):2812-9
12782586
Cancer Res. 2003 Jun 15;63(12):3403-12
12810677
J Exp Med. 2003 Jun 16;197(12):1755-65
12810693
J Cell Biol. 2003 Jun 23;161(6):1163-77
12810700
Brain Pathol. 2003 Oct;13(4):582-97
14655762
Nat Immunol. 2004 Jan;5(1):74-80
14634646
Chin Med J (Engl). 2004 Jan;117(1):94-8
14733782
N Engl J Med. 2004 Jun 3;350(23):2335-42
15175435
Trends Immunol. 2004 Jul;25(7):387-95
15207507
J Biol Chem. 1998 Mar 20;273(12):6599-602
9506953
Histochem Cell Biol. 1998 Apr;109(4):349-57
9562384
Am J Pathol. 1999 Feb;154(2):385-94
10027397
J Cell Biol. 1999 Feb 22;144(4):789-801
10037799
Nature. 1999 Oct 14;401(6754):670-7
10537105
Science. 1999 Dec 24;286(5449):2511-4
10617467
J Clin Invest. 2000 Jan;105(1):71-7
10619863
Cell. 2000 Jan 7;100(1):57-70
10647931
Carcinogenesis. 2000 Mar;21(3):505-15
10688871
Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3422-7
10725398
Blood. 2000 May 15;95(10):3106-12
10807776
Nat Med. 1999 Apr;5(4):434-8
10202935
Science. 1999 Jun 18;284(5422):1994-8
10373119
EMBO J. 1999 Jul 15;18(14):3964-72
10406801
Circ Res. 1999 Aug 6;85(3):221-8
10436164
Am J Pathol. 1999 Sep;155(3):739-52
10487832
J Clin Invest. 2004 Nov;114(9):1260-71
15520858
Drug Resist Updat. 2004 Aug-Oct;7(4-5):289-300
15533766
Int J Oncol. 2004 Dec;25(6):1609-14
15547697
Cancer Res. 2004 Nov 15;64(22):8249-55
15548691
Nat Rev Cancer. 2004 Dec;4(12):978-87
15573119
Science. 2005 Jan 7;307(5706):58-62
15637262
Cancer Cell. 2005 Jan;7(1):101-11
15652753
Cardiovasc Res. 2005 Feb 15;65(3):639-48
15664390
Mol Cell Biol. 2005 Mar;25(6):2441-9
15743836
Nat Med. 2005 Mar;11(3):261-2
15723071
J Clin Oncol. 2005 Mar 20;23(9):2078-93
15774796
Cytokine Growth Factor Rev. 2005 Apr;16(2):159-78
15863032
Blood. 2005 Jun 1;105(11):4321-9
15632204
Blood. 2005 Jun 15;105(12):4649-56
15705793
Oncol Rep. 2005 Jul;14(1):81-4
15944771
J Histochem Cytochem. 2005 Aug;53(8):997-1002
15923371
EMBO J. 2005 Aug 17;24(16):2885-95
16052207
Blood. 2005 Sep 1;106(5):1525-31
15905185
J Immunol. 2005 Sep 1;175(5):2890-9
16116175
Circ Res. 2005 Sep 16;97(6):512-23
16166562
FASEB J. 2002 Dec;16(14):1985-7
12397087
Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16069-74
12446836
Oncol Rep. 2006 Oct;16(4):693-8
16969481
Endocr Rev. 1997 Feb;18(1):4-25
9034784
Science. 1997 Jul 4;277(5322):55-60
9204896
Nat Med. 1997 Aug;3(8):887-93
9256280
Am J Pathol. 1997 Nov;151(5):1417-23
9358768