Progress in tumor vascular normalization for anticancer therapy: challenges and perspectives

Bingxue Shang, Zhifei Cao, Quansheng Zhou

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Front. Med. ›› 2012, Vol. 6 ›› Issue (1) : 67-78. DOI: 10.1007/s11684-012-0176-8
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Progress in tumor vascular normalization for anticancer therapy: challenges and perspectives

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Abstract

Antitumor angiogenic therapy has been shown promising in the treatment of several advanced cancers since the approval of the first antiangiogenic drug Avastin in 2004. Although the current antiangiogenic drugs reduce the density of tumor blood vessels and result in tumor shrinkage at the early stage of treatment, recent studies have shown that antiangiogenic therapy has transient and insufficient efficacy, resulting in tumor recurrence in patients after several months of treatment. Blockage of blood and oxygen supplies creates a hypoxic and acidic microenvironment in the tumor tissues, which fosters tumor cells to become more aggressive and metastatic. In 2001, Jain proposed tumor vascular normalization as an alternative approach to treating cancers based on the pioneering work on tumor blood vessels by several other researchers. At present, normalizing the disorganized tumor vasculature, rather than disrupting or blocking them, has emerged as a new option for anticancer therapy. Preclinical and clinical data have shown that tumor vascular normalization using monoclonal antibodies, proteins, peptides, small molecules, and pericytes resulted in decreased tumor size and reduced metastasis. However, current tumor vascular normalizing drugs display moderate anticancer efficacy. Accumulated data have shown that a variety of vasculogenic/angiogenic tumor cells and genes play important roles in tumor neovascularization, growth, and metastasis. Therefore, multiple-targeting of vasculogenic tumor cells and genes may improve the efficacy of tumor vascular normalization. To this end, the combination of antiangiogenic drugs with tumor vascular normalizing therapeutics, as well as the integration of Western medicine with traditional Chinese medicine, may provide a good opportunity for discovering novel tumor vascular normalizing drugs for an effective anticancer therapy.

Keywords

angiogenesis / vasculogenesis / neovascularization / tumor / vasculature / normalization / traditional Chinese medicine

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Bingxue Shang, Zhifei Cao, Quansheng Zhou. Progress in tumor vascular normalization for anticancer therapy: challenges and perspectives. Front Med, 2012, 6(1): 67‒78 https://doi.org/10.1007/s11684-012-0176-8

References

[1]
Ebos JM, Kerbel RS. Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat Rev Clin Oncol 2011; 8(4): 210-221
CrossRef Pubmed Google scholar
[2]
Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285(21): 1182-1186
CrossRef Pubmed Google scholar
[3]
Heath VL, Bicknell R. Anticancer strategies involving the vasculature. Nat Rev Clin Oncol 2009; 6(7): 395-404
CrossRef Pubmed Google scholar
[4]
Ribatti D. Endogenous inhibitors of angiogenesis: a historical review. Leuk Res 2009; 33(5): 638-644
CrossRef Pubmed Google scholar
[5]
Ribatti D. The discovery of antiangiogenic molecules: a historical review. Curr Pharm Des 2009; 15(4): 345-352
CrossRef Pubmed Google scholar
[6]
Van Cutsem E, Lambrechts D, Prenen H, Jain RK, Carmeliet P. Lessons from the adjuvant bevacizumab trial on colon cancer: what next? J Clin Oncol 2011; 29(1): 1-4
CrossRef Pubmed Google scholar
[7]
Miles D, Harbeck N, Escudier B, Hurwitz H, Saltz L, Van Cutsem E, Cassidy J, Mueller B, Sirzén F. Disease course patterns after discontinuation of bevacizumab: pooled analysis of randomized phase III trials. J Clin Oncol 2011; 29(1): 83-88
CrossRef Pubmed Google scholar
[8]
Otrock ZK, Hatoum HA, Awada AH, Ishak RS, Shamseddine AI. Hypoxia-inducible factor in cancer angiogenesis: structure, regulation and clinical perspectives. Crit Rev Oncol Hematol 2009; 70(2): 93-102
CrossRef Pubmed Google scholar
[9]
Osinsky S, Zavelevich M, Vaupel P. Tumor hypoxia and malignant progression. Exp Oncol 2009; 31(2): 80-86
Pubmed
[10]
Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med 2001; 7(9): 987-989
CrossRef Pubmed Google scholar
[11]
Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005; 307(5706): 58-62
CrossRef Pubmed Google scholar
[12]
Carmeliet P, Jain RK. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov 2011; 10(6): 417-427
CrossRef Pubmed Google scholar
[13]
Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, Jain RK. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 2011; 91(3): 1071-1121
CrossRef Pubmed Google scholar
[14]
Sato Y. Persistent vascular normalization as an alternative goal of anti-angiogenic cancer therapy. Cancer Sci 2011; 102(7): 1253-1256
CrossRef Pubmed Google scholar
[15]
Fukumura D, Jain RK. Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc Res 2007; 74(2-3): 72-84
CrossRef Pubmed Google scholar
[16]
Hess AR, Margaryan NV, Seftor EA, Hendrix MJ. Deciphering the signaling events that promote melanoma tumor cell vasculogenic mimicry and their link to embryonic vasculogenesis: role of the Eph receptors. Dev Dyn 2007; 236(12): 3283-3296
CrossRef Pubmed Google scholar
[17]
Kučera T, Lammert E. Ancestral vascular tube formation and its adoption by tumors. Biol Chem 2009; 390(10): 985-994
CrossRef Pubmed Google scholar
[18]
Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011; 473(7347): 298-307
CrossRef Pubmed Google scholar
[19]
Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011; 146(6): 873-887
CrossRef Pubmed Google scholar
[20]
Shen R, Ye Y, Chen L, Yan Q, Barsky SH, Gao JX. Precancerous stem cells can serve as tumor vasculogenic progenitors. PLoS One, 2008; 3(2): e1652
[21]
Menakuru SR, Brown NJ, Staton CA, Reed MW. Angiogenesis in pre-malignant conditions. Br J Cancer 2008; 99(12): 1961-1966
CrossRef Pubmed Google scholar
[22]
Hong D, Gupta R, Ancliff P, Atzberger A, Brown J, Soneji S, Green J, Colman S, Piacibello W, Buckle V, Tsuzuki S, Greaves M, Enver T. Initiating and cancer-propagating cells in TEL-AML1-associated childhood leukemia. Science 2008; 319(5861): 336-339
CrossRef Pubmed Google scholar
[23]
Hill RP, Marie-Egyptienne DT, Hedley DW. Cancer stem cells, hypoxia and metastasis. Semin Radiat Oncol 2009; 19(2): 106-111
CrossRef Pubmed Google scholar
[24]
Zhao Y, Dong J, Huang Q, Lou M, Wang A, Lan Q. Endothelial cell transdifferentiation of human glioma stem progenitor cells in vitro. Brain Res Bull 2010; 82(5-6): 308-312
CrossRef Pubmed Google scholar
[25]
Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C, Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010; 468(7325): 829-833
CrossRef Pubmed Google scholar
[26]
Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, Maira G, Parati EA, Stassi G, Larocca LM, De Maria R. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010; 468(7325): 824-828
CrossRef Pubmed Google scholar
[27]
Soda Y, Marumoto T, Friedmann-Morvinski D, Soda M, Liu F, Michiue H, Pastorino S, Yang M, Hoffman RM, Kesari S, Verma IM. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc Natl Acad Sci USA 2011; 108(11): 4274-4280
CrossRef Pubmed Google scholar
[28]
Chiao MT, Yang YC, Cheng WY, Shen CC, Ko JL. CD133+ glioblastoma stem-like cells induce vascular mimicry in vivo. Curr Neurovasc Res 2011; 8(3): 210-219
CrossRef Pubmed Google scholar
[29]
Ping YF, Bian XW. Consice review: contribution of cancer stem cells to neovascularization. Stem Cells 2011; 29(6): 888-894
CrossRef Pubmed Google scholar
[30]
Ahn GO, Brown JM. Role of endothelial progenitors and other bone marrow-derived cells in the development of the tumor vasculature. Angiogenesis 2009; 12(2): 159-164
CrossRef Pubmed Google scholar
[31]
Ria R, Piccoli C, Cirulli T, Falzetti F, Mangialardi G, Guidolin D, Tabilio A, Di Renzo N, Guarini A, Ribatti D, Dammacco F, Vacca A. Endothelial differentiation of hematopoietic stem and progenitor cells from patients with multiple myeloma. Clin Cancer Res 2008; 14(6): 1678-1685
CrossRef Pubmed Google scholar
[32]
Vacca A, Ribatti D. Bone marrow angiogenesis in multiple myeloma. Leukemia 2006; 20(2): 193-199
CrossRef Pubmed Google scholar
[33]
Chen H, Campbell RA, Chang Y, Li M, Wang CS, Li J, Sanchez E, Share M, Steinberg J, Berenson A, Shalitin D, Zeng Z, Gui D, Perez-Pinera P, Berenson RJ, Said J, Bonavida B, Deuel TF, Berenson JR. Pleiotrophin produced by multiple myeloma induces transdifferentiation of monocytes into vascular endothelial cells: a novel mechanism of tumor-induced vasculogenesis. Blood 2009; 113(9): 1992-2002
CrossRef Pubmed Google scholar
[34]
Scavelli C, Nico B, Cirulli T, Ria R, Di Pietro G, Mangieri D, Bacigalupo A, Mangialardi G, Coluccia AM, Caravita T, Molica S, Ribatti D, Dammacco F, Vacca A. Vasculogenic mimicry by bone marrow macrophages in patients with multiple myeloma. Oncogene 2008; 27(5): 663-674
CrossRef Pubmed Google scholar
[35]
Maltby S, Khazaie K, McNagny KM. Mast cells in tumor growth: angiogenesis, tissue remodelling and immune-modulation. Biochim Biophys Acta 2009; 1796(1): 19-26
Pubmed
[36]
Ball SG, Shuttleworth CA, Kielty CM. Mesenchymal stem cells and neovascularization: role of platelet-derived growth factor receptors. J Cell Mol Med 2007; 11(5): 1012-1030
CrossRef Pubmed Google scholar
[37]
Chen MY, Lie PC, Li ZL, Wei X. Endothelial differentiation of Wharton’s jelly-derived mesenchymal stem cells in comparison with bone marrow-derived mesenchymal stem cells. Exp Hematol 2009; 37(5): 629-640
CrossRef Pubmed Google scholar
[38]
Siveen KS, Kuttan G. Role of macrophages in tumour progression. Immunol Lett 2009; 123(2): 97-102
CrossRef Pubmed Google scholar
[39]
Coffelt SB, Hughes R, Lewis CE. Tumor-associated macrophages: effectors of angiogenesis and tumor progression. Biochim Biophys Acta 2009; 1796(1): 11-18
Pubmed
[40]
Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe’er J, Trent JM, Meltzer PS, Hendrix MJ. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999; 155(3): 739-752
CrossRef Pubmed Google scholar
[41]
Folberg R, Hendrix MJ, Maniotis AJ. Vasculogenic mimicry and tumor angiogenesis. Am J Pathol 2000; 156(2): 361-381
CrossRef Pubmed Google scholar
[42]
Seftor RE, Seftor EA, Koshikawa N, Meltzer PS, Gardner LM, Bilban M, Stetler-Stevenson WG, Quaranta V, Hendrix MJ. Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res 2001; 61(17): 6322-6327
Pubmed
[43]
Sood AK, Fletcher MS, Zahn CM, Gruman LM, Coffin JE, Seftor EA, Hendrix MJ. The clinical significance of tumor cell-lined vasculature in ovarian carcinoma: implications for anti-vasculogenic therapy. Cancer Biol Ther 2002; 1(6): 661-664
Pubmed
[44]
Hendrix MJ, Seftor EA, Hess AR, Seftor RE. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat Rev Cancer 2003; 3(6): 411-421
CrossRef Pubmed Google scholar
[45]
Folberg R, Maniotis AJ. Vasculogenic mimicry. APMIS 2004; 112(7-8): 508-525
CrossRef Pubmed Google scholar
[46]
Zhang S, Zhang D, Sun B. Vasculogenic mimicry: current status and future prospects. Cancer Lett 2007; 254(2): 157-164
CrossRef Pubmed Google scholar
[47]
Rak J, Milsom C, Yu J. Vascular determinants of cancer stem cell dormancy—do age and coagulation system play a role? APMIS 2008; 116(7-8): 660-676
CrossRef Pubmed Google scholar
[48]
Begg AC, Stewart FA, Vens C. Strategies to improve radiotherapy with targeted drugs. Nat Rev Cancer 2011;11(4):239-253
CrossRef Pubmed Google scholar
[49]
Chiarugi V, Magnelli L, Cinelli M, Ruggiero M. Oncogenes, p53, and tumor angiogenesis. J Cancer Res Clin Oncol 1998; 124(9): 523-525
CrossRef Pubmed Google scholar
[50]
Giri D, Ittmann M. Inactivation of the PTEN tumor suppressor gene is associated with increased angiogenesis in clinically localized prostate carcinoma. Hum Pathol 1999; 30(4): 419-424
CrossRef Pubmed Google scholar
[51]
Bohonowych JE,Gopal U, Isaacs JS. Hsp90 as a gatekeeper of tumor angiogenesis: clinical promise and potential pitfalls. J Oncol 2010; 2010: 412985
[52]
Gao JX. Cancer stem cells: the lessons from pre-cancerous stem cells. J Cell Mol Med 2008; 12(1): 67-96
CrossRef Pubmed Google scholar
[53]
Midulla M, Verma R, Pignatelli M, Ritter MA, Courtenay-Luck NS, George AJ. Source of oncofetal ED-B-containing fibronectin: implications of production by both tumor and endothelial cells. Cancer Res 2000; 60(1): 164-169
Pubmed
[54]
Ye Y, Yin DT, Chen L, Zhou Q, Shen R, He G, Yan Q, Tong Z, Issekutz AC, Shapiro CL, Barsky SH, Lin H, Li JJ, Gao JX. Identification of Piwil2-like (PL2L) proteins that promote tumorigenesis. PLoS ONE 2010; 5(10): e13406
CrossRef Pubmed Google scholar
[55]
Oike Y, Ito Y, Hamada K, Zhang XQ, Miyata K, Arai F, Inada T, Araki K, Nakagata N, Takeya M, Kisanuki YY, Yanagisawa M, Gale NW, Suda T. Regulation of vasculogenesis and angiogenesis by EphB/ephrin-B2 signaling between endothelial cells and surrounding mesenchymal cells. Blood 2002; 100(4): 1326-1333
Pubmed
[56]
Djokovic D, Trindade A, Gigante J, Badenes M, Silva L, Liu R, Li X, Gong M, Krasnoperov V, Gill PS, Duarte A. Combination of Dll4/Notch and Ephrin-B2/EphB4 targeted therapy is highly effective in disrupting tumor angiogenesis. BMC Cancer 2010; 10(1): 641-652
CrossRef Pubmed Google scholar
[57]
McColgan P, Sharma P. Polymorphisms of matrix metalloproteinases 1, 2, 3 and 9 and susceptibility to lung, breast and colorectal cancer in over 30,000 subjects. Int J Cancer 2009; 125(6): 1473-1478
CrossRef Pubmed Google scholar
[58]
Taveau JC, Dubois M, Le Bihan O, Trépout S, Almagro S, Hewat E, Durmort C, Heyraud S, Gulino-Debrac D, Lambert O. Structure of artificial and natural VE-cadherin-based adherens junctions. Biochem Soc Trans 2008; 36(2): 189-193
CrossRef Pubmed Google scholar
[59]
Sun Q, Zhou H, Binmadi NO, Basile JR. Hypoxia-inducible factor-1-mediated regulation of semaphorin 4D affects tumor growth and vascularity. J Biol Chem 2009; 284(46): 32066-32074
CrossRef Pubmed Google scholar
[60]
Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996; 87(7): 1171-1180
CrossRef Pubmed Google scholar
[61]
Suri C, McClain J, Thurston G, McDonald DM, Zhou H, Oldmixon EH, Sato TN, Yancopoulos GD. Increased vascularization in mice overexpressing angiopoietin-1. Science 1998; 282(5388): 468-471
CrossRef Pubmed Google scholar
[62]
Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, McDonald DM. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 1999; 286(5449): 2511-2514
CrossRef Pubmed Google scholar
[63]
Hayes AJ, Huang WQ, Yu J, Maisonpierre PC, Liu A, Kern FG, Lippman ME, McLeskey SW, Li LY. Expression and function of angiopoietin-1 in breast cancer. Br J Cancer 2000; 83(9): 1154-1160
CrossRef Pubmed Google scholar
[64]
Willett CG, Boucher Y, di Tomaso E, Duda DG, Munn LL, Tong RT, Chung DC, Sahani DV, Kalva SP, Kozin SV, Mino M, Cohen KS, Scadden DT, Hartford AC, Fischman AJ, Clark JW, Ryan DP, Zhu AX, Blaszkowsky LS, Chen HX, Shellito PC, Lauwers GY, Jain RK. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 2004; 10(2): 145-147
CrossRef Pubmed Google scholar
[65]
Ferrara N, Hillan KJ, Novotny W. Bevacizumab (Avastin), a humanized anti-VEGF monoclonal antibody for cancer therapy. Biochem Biophys Res Commun 2005; 333(2): 328-335
CrossRef Pubmed Google scholar
[66]
Jain RK, Duda DG, Willett CG, Sahani DV, Zhu AX, Loeffler JS, Batchelor TT, Sorensen AG. Biomarkers of response and resistance to antiangiogenic therapy. Nat Rev Clin Oncol 2009; 6(6): 327-338
CrossRef Pubmed Google scholar
[67]
Greenberg JI, Cheresh DA. VEGF as an inhibitor of tumor vessel maturation: implications for cancer therapy. Expert Opin Biol Ther 2009; 9(11): 1347-1356
CrossRef Pubmed Google scholar
[68]
Tong RT, Boucher Y, Kozin SV, Winkler F, Hicklin DJ, Jain RK. Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res 2004; 64(11): 3731-3736
CrossRef Pubmed Google scholar
[69]
Winkler F, Kozin SV, Tong RT, Chae SS, Booth MF, Garkavtsev I, Xu L, Hicklin DJ, Fukumura D, di Tomaso E, Munn LL, Jain RK. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 2004; 6(6): 553-563
Pubmed
[70]
Ladroue C, Carcenac R, Leporrier M, Gad S, Le Hello C, Galateau-Salle F, Feunteun J, Pouysségur J, Richard S, Gardie B. PHD2 mutation and congenital erythrocytosis with paraganglioma. N Engl J Med 2008; 359(25): 2685-2692
CrossRef Pubmed Google scholar
[71]
Mazzone M, Dettori D, Leite de Oliveira R, Loges S, Schmidt T, Jonckx B, Tian YM, Lanahan AA, Pollard P, Ruiz de Almodovar C, De Smet F, Vinckier S, Aragonés J, Debackere K, Luttun A, Wyns S, Jordan B, Pisacane A, Gallez B, Lampugnani MG, Dejana E, Simons M, Ratcliffe P, Maxwell P, Carmeliet P. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009; 136(5): 839-851
CrossRef Pubmed Google scholar
[72]
Kim JW, Johnson RS. You don’t need a PHD to grow a tumor. Dev Cell 2009; 16(6): 781-782
CrossRef Pubmed Google scholar
[73]
Choi HJ, Song BJ, Gong YD, Gwak WJ, Soh Y. Rapid degradation of hypoxia-inducible factor-1alpha by KRH102053, a new activator of prolyl hydroxylase 2. Br J Pharmacol 2008; 154(1): 114-125
CrossRef Pubmed Google scholar
[74]
Nepal M, Gong YD, Park YR, Soh Y. An activator of PHD2, KRH102140, decreases angiogenesis via inhibition of HIF-1α. Cell Biochem Funct 2011; 29(2): 126-134
CrossRef Pubmed Google scholar
[75]
Vestweber D. VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Thromb Vasc Biol 2008; 28(2): 223-232
CrossRef Pubmed Google scholar
[76]
Gavard J. Breaking the VE-cadherin bonds. FEBS Lett 2009; 583(1): 1-6
CrossRef Pubmed Google scholar
[77]
Dejana E, Orsenigo F, Lampugnani MG. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci 2008; 121(13): 2115-2122
CrossRef Pubmed Google scholar
[78]
Zhang LZ, Mei J, Qian ZK, Cai XS, Jiang Y, Huang WD. The role of VE-cadherin in osteosarcoma cells. Pathol Oncol Res 2010; 16(1): 111-117
CrossRef Pubmed Google scholar
[79]
Cavallaro U, Liebner S, Dejana E. Endothelial cadherins and tumor angiogenesis. Exp Cell Res 2006; 312(5): 659-667
CrossRef Pubmed Google scholar
[80]
Labelle M, Schnittler HJ, Aust DE, Friedrich K, Baretton G, Vestweber D, Breier G. Vascular endothelial cadherin promotes breast cancer progression via transforming growth factor beta signaling. Cancer Res 2008; 68(5): 1388-1397
CrossRef Pubmed Google scholar
[81]
Otani A, Slike BM, Dorrell MI, Hood J, Kinder K, Ewalt KL, Cheresh D, Schimmel P, Friedlander M. A fragment of human TrpRS as a potent antagonist of ocular angiogenesis. Proc Natl Acad Sci USA 2002; 99(1): 178-183
CrossRef Pubmed Google scholar
[82]
Banin E, Dorrell MI, Aguilar E, Ritter MR, Aderman CM, Smith AC, Friedlander J, Friedlander M. T2-TrpRS inhibits preretinal neovascularization and enhances physiological vascular regrowth in OIR as assessed by a new method of quantification. Invest Ophthalmol Vis Sci 2006; 47(5): 2125-2134
CrossRef Pubmed Google scholar
[83]
Zhou Q, Kiosses WB, Liu J, Schimmel P. Tumor endothelial cell tube formation model for determining anti-angiogenic activity of a tRNA synthetase cytokine. Methods 2008; 44(2): 190-195
CrossRef Pubmed Google scholar
[84]
Zhou Q, Kapoor M, Guo M, Belani R, Xu X, Kiosses WB, Hanan M, Park C, Armour E, Do MH, Nangle LA, Schimmel P, Yang XL. Orthogonal use of a human tRNA synthetase active site to achieve multifunctionality. Nat Struct Mol Biol 2010; 17(1): 57-61
CrossRef Pubmed Google scholar
[85]
Jaggi JS, Henke E, Seshan SV, Kappel BJ, Chattopadhyay D, May C, McDevitt MR, Nolan D, Mittal V, Benezra R, Scheinberg DA. Selective alpha-particle mediated depletion of tumor vasculature with vascular normalization. PLoS ONE 2007; 2(3): e267
CrossRef Pubmed Google scholar
[86]
Rolny C, Mazzone M, Tugues S, Laoui D, Johansson I, Coulon C, Squadrito ML, Segura I, Li X, Knevels E, Costa S, Vinckier S, Dresselaer T, Åkerud P, De Mol M, Salomäki H, Phillipson M, Wyns S, Larsson E, Buysschaert I, Botling J, Himmelreich U, Van Ginderachter JA, De Palma M, Dewerchin M, Claesson-Welsh L, Carmeliet P. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 2011; 19(1): 31-44
CrossRef Pubmed Google scholar
[87]
Wang L, Zhou GB, Liu P, Song JH, Liang Y, Yan XJ, Xu F, Wang BS, Mao JH, Shen ZX, Chen SJ, Chen Z. Dissection of mechanisms of Chinese medicinal formula Realgar-Indigo naturalis as an effective treatment for promyelocytic leukemia. Proc Natl Acad Sci USA 2008; 105(12): 4826-4831
CrossRef Pubmed Google scholar
[88]
Xiong L, Tian SX. A concept of regulating tumor microenvironment immune and normalizing angiogenesis by Chinese medicine drug therapy for supporting zheng-qi to prop up root. Chin J Integr Traidt West Med (Zhongguo Zhong Xi Yi Jie He Za Zhi) 2010; 30(2): 201-204 (in Chinese)
Pubmed
[89]
Pang X, Yi Z, Zhang J, Lu B, Sung B, Qu W, Aggarwal BB, Liu M. Celastrol suppresses angiogenesis-mediated tumor growth through inhibition of AKT/mammalian target of rapamycin pathway. Cancer Res 2010; 70(5): 1951-1959
CrossRef Pubmed Google scholar
[90]
Pang X, Yi T, Yi Z, Cho SG, Qu W, Pinkaew D, Fujise K, Liu M. Morelloflavone, a biflavonoid, inhibits tumor angiogenesis by targeting rho GTPases and extracellular signal-regulated kinase signaling pathways. Cancer Res 2009; 69(2): 518-525
CrossRef Pubmed Google scholar
[91]
Qiang L, Yang Y, You QD, Ma YJ, Yang L, Nie FF, Gu HY, Zhao L, Lu N, Qi Q, Liu W, Wang XT, Guo QL. Inhibition of glioblastoma growth and angiogenesis by gambogic acid: an in vitro and in vivo study. Biochem Pharmacol 2008; 75(5): 1083-1092
CrossRef Pubmed Google scholar
[92]
Pang X, Yi Z, Zhang X, Sung B, Qu W, Lian X, Aggarwal BB, Liu M. Acetyl-11-keto-beta-boswellic acid inhibits prostate tumor growth by suppressing vascular endothelial growth factor receptor 2-mediated angiogenesis. Cancer Res 2009; 69(14): 5893-5900
CrossRef Pubmed Google scholar
[93]
Park B, Sung B, Yadav VR, Cho SG, Liu M, Aggarwal BB. Acetyl-11-keto-β-boswellic acid suppresses invasion of pancreatic cancer cells through the downregulation of CXCR4 chemokine receptor expression. Int J Cancer 2011; 129(1): 23-33
CrossRef Pubmed Google scholar
[94]
Pang X, Zhang L, Lai L, Chen J, Wu Y, Yi Z, Zhang J, Qu W, Aggarwal BB, Liu M. 1′-Acetoxychavicol acetate suppresses angiogenesis-mediated human prostate tumor growth by targeting VEGF-mediated Src-FAK-Rho GTPase-signaling pathway. Carcinogenesis 2011; 32(6): 904-912
CrossRef Pubmed Google scholar
[95]
Kuang L, Wang L, Wang Q, Zhao Q, Du B, Li D, Luo J, Liu M, Hou A, Qian M. Cudratricusxanthone G inhibits human colorectal carcinoma cell invasion by MMP-2 down-regulation through suppressing activator protein-1 activity. Biochem Pharmacol 2011; 81(10): 1192-1200
CrossRef Pubmed Google scholar
[96]
Liu XD, Fan RF, Zhang Y, Yang HZ, Fang ZG, Guan WB, Lin DJ, Xiao RZ, Huang RW, Huang HQ, Liu PQ, Liu JJ. Down-regulation of telomerase activity and activation of caspase-3 are responsible for tanshinone I-induced apoptosis in monocyte leukemia cells in vitro. Int J Mol Sci 2010; 11(6): 2267-2280
CrossRef Pubmed Google scholar
[97]
Wu Y, Fan Q, Lu N, Tao L, Gao Y, Qi Q, Guo Q. Breviscapine-induced apoptosis of human hepatocellular carcinoma cell line HepG2 was involved in its antitumor activity. Phytother Res 2010; 24(8): 1188-1194
Pubmed
[98]
Lin J, Wei L, Xu W, Hong Z, Liu X, Peng J. Effect of Hedyotis diffusa Willd extract on tumor angiogenesis. Mol Med Report 2011; 4(6): 1283-1288
Pubmed
[99]
You J. Study on the tumor microenvironment and tumor vascular normalization in integrative treatment of tumor by Chinese medicine and western medicine.Chin J Integr Traidt West Med (Zhongguo Zhong Xi Yi Jie He Za Zhi) 2011; 31(8): 1127-1131 (in Chinese)
Pubmed
[100]
Hida K, Hida Y, Amin DN, Flint AF, Panigrahy D, Morton CC, Klagsbrun M. Tumor-associated endothelial cells with cytogenetic abnormalities. Cancer Res 2004; 64(22): 8249-8255
CrossRef Pubmed Google scholar
[101]
Tian S, Hayes AJ, Metheny-Barlow LJ, Li LY. Stabilization of breast cancer xenograft tumour neovasculature by angiopoietin-1. Br J Cancer 2002; 86(4): 645-651
CrossRef Pubmed Google scholar
[102]
Metheny-Barlow LJ, Li LY. The enigmatic role of angiopoietin-1 in tumor angiogenesis. Cell Res 2003; 13(5): 309-317
CrossRef Pubmed Google scholar
[103]
Inai T, Mancuso M, Hashizume H, Baffert F, Haskell A, Baluk P, Hu-Lowe DD, Shalinsky DR, Thurston G, Yancopoulos GD, McDonald DM. Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol 2004; 165(1): 35-52
CrossRef Pubmed Google scholar
[104]
Coulon C, Georgiadou M, Roncal C, De Bock K, Langenberg T, Carmeliet P. From vessel sprouting to normalization: role of the prolyl hydroxylase domain protein/hypoxia-inducible factor oxygen-sensing machinery. Arterioscler Thromb Vasc Biol 2010; 30(12): 2331-2336
CrossRef Pubmed Google scholar
[105]
Sorensen AG, Batchelor TT, Zhang WT, Chen PJ, Yeo P, Wang M, Jennings D, Wen PY, Lahdenranta J, Ancukiewicz M, di Tomaso E, Duda DG, Jain RK. A “vascular normalization index” as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res 2009; 69(13): 5296-5300
CrossRef Pubmed Google scholar
[106]
Zhang Q, Bindokas V, Shen J, Fan H, Hoffman RM, Xing HR. Time-course imaging of therapeutic functional tumor vascular normalization by antiangiogenic agents. Mol Cancer Ther 2011; 10(7): 1173-1184
CrossRef Pubmed Google scholar
[107]
Hormigo A, Gutin PH, Rafii S. Tracking normalization of brain tumor vasculature by magnetic imaging and proangiogenic biomarkers. Cancer Cell 2007; 11(1): 6-8
CrossRef Pubmed Google scholar

Acknowledgements

This study was supported by grants from the National Natural Science Foundation of China (Grant No.30971138), the Science Foundation of Suzhou City (No. SWG0904 and No. SS201004), a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and a Special National Strategic Leader Project of China (No. XDA01040200).

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2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
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