Investigations into Tumor Angiogenesis
Angiogenesis (the recruitment and formation of new blood vessels) plays a fundamental role in vessel development in the embryo and placenta during pregnancy. In adults, it is confined mainly to the menstrual cycle and wound healing, and its occurrence otherwise often heralds pathologic states such as tumor development, atherosclerosis, endometriosis, ischemic injury, or macular degeneration. The late Dr. Judah Folkman, founder of the tumor angiogenesis field, demonstrated that tumors cannot grow beyond a minimal size without recruiting new blood vessels. His suggestion that inhibition of such tumor angiogenesis may be an effective and novel means to target tumors has led to a paradigm shift in cancer care.
Hundreds of clinical trials worldwide are now testing anti-angiogenic therapeutic strategies. Considerable basic and translational angiogenesis research is being conducted at our Center of Cancer Systems Biology. A sizable number of members of our team had tight research collaborations or trained under Judah Folkman. Among these are Lynn Hlatky, Philip Hahnfeldt, Amir Abdollahi, Giannoula Klement, Nava Almog, Clare Lamont, Abdo Abouslaybi, and Kashi Javaherian. Many of the angiogenic initiatives our researchers designed jointly with Dr. Folkman continue at the Center, dovetailing with our Center's two primary mandates: to investigate how intercellular interactions and tumor microenvironment modify tumor evolution, and to develop predictive quantitative models of carcinogenesis and metastasis. To pursue these, the Center's team of investigators merge several distinct backgrounds in tumor angiogenesis. These include: i) quantitative and experimental investigations into "metronomic" (low, uniform) dosing as an anti-angiogenic, optimum-maintenance therapy (Philip Hahnfeldt, Giannoula Klement); ii) computational modeling of tumor angiogenic carrying capacity and its influence on tumor progression, including the induction of oscillatory behavior and dormancy (Lynn Hlatky, Philip Hahnfeldt); iii) the molecular determinants of angiogenic signaling in tumor dormancy (Nava Almog, Amir Abdollahi); iv) the role of platelets in tumor angiogenesis and in other pathologic processes (Giannoula Klement, Abdo Abouslaybi); v) pan-genomic implications of the angiogenic switch (Amir Abdollahi, Lynn Hlatky, Philip Hahnfeldt); vi) studies of radiation quality effect on the ability of the host to support tumor angiogenesis (Clare Lamont, with Swati Girdhani,); vii) studies of the broader role of angiogenesis in radiation oncology (Lynn Hlatky, Amir Abdollahi) and viii) the study of intrinsic inhibitors of angiogenesis (Kashi Javaherian, Amir Abdollahi).
A strong body of work on the topic of tumor angiogenesis has been published on the topic by researchers currently at CCSB:
- Almog N, Klement G. Platelet Proteome and Tumor Dormancy: Can Platelets Content Serve as Predictive Biomarkers for Exit of Tumors from Dormancy? Cancers 2010, 2: 842-858.
- Almog N. Molecular mechanisms underlying tumor dormancy. Cancer Lett. 2010.
- Almog N, Ma L, Raychowdhury R, Schwager C, Erber R, Short S, Hlatky L, Vajkoczy P, Huber PE, Folkman J and Abdollahi A. Transcriptional switch of dormant tumors to fast-growing angiogenic phenotype. Cancer Res 69 (2009) 836-44.
- Klement GL, Yip TT, Cassiola F, Kikuchi L, Cervi D, Podust V, Italiano JE, Wheatley E, Abou-Slaybi A, Bender E, Almog N, Kieran MW and Folkman J. Platelets actively sequester angiogenesis regulators. Blood 113 (2009) 2835-42.
- Lee TY, Muschal S, Pravda EA, Folkman J, Abdollahi A and Javaherian K. Angiostatin regulates the expression of antiangiogenic and proapoptotic pathways via targeted inhibition of mitochondrial proteins. Blood 114 (2009) 1987-98.
- Cervi D, Yip TT, Bhattacharya N, Podust VN, Peterson J, Abou-Slaybi A, Naumov GN, Bender E, Almog N, Italiano Jr. JE, Folkman J and Klement GL. Platelet-associated PF-4 as a biomarker of early tumor growth. Blood 111 (2008) 1201-7.
- Lee TY, Tjin Tham Sjin RM, Movahedi S, Ahmed B, Pravda EA, Lo KM, Gillies SD, Folkman J and Javaherian K. Linking antibody Fc domain to endostatin significantly improves endostatin half-life and efficacy. Clin Cancer Res 14 (2008) 1487-93.
- Abdollahi A, Schwager C, Kleeff J, Esposito I, Domhan S, Peschke P, Hauser K, Hahnfeldt P, Hlatky L, Debus J, Peters JM, Friess H, Folkman J and Huber PE. Transcriptional network governing the angiogenic switch in human pancreatic cancer. Proc Natl Acad Sci USA 104 (2007) 12890-5.
- Goukassian DA, Qin G, Dolan C, Murayama T, Silver M, Curry C, Eaton E, Luedemann C, Ma H, Asahara T, Zak V, Mehta S, Burg A, Thorne T, Kishore R and Losordo DW. Tumor necrosis factor-alpha receptor p75 is required in ischemia-induced neovascularization. Circulation 115 (2007) 752-62.
- Almog N, Henke V, Flores L, Hlatky L, Kung AL, Wright RD, Berger R, Hutchinson L, Naumov GN, Bender E, Akslen LA, Achilles EG and Folkman J. Prolonged dormancy of human liposarcoma is associated with impaired tumor angiogenesis. FASEB J 20 (2006) 947-9.
- Becker CM, Sampson DA, Short SM, Javaherian K, Folkman J and D'Amato RJ. Short synthetic endostatin peptides inhibit endothelial migration in vitro and endometriosis in a mouse model. Fertil Steril 85 (2006) 71-7.
- Clamp A, Blackhall FH, Henrioud A, Jayson GC, Javaherian K, Esko J, Gallagher JT and Merry CL. The morphogenic properties of oligomeric endostatin are dependent on cell surface heparan sulfate. J Biol Chem 281 (2006) 14813-22.
- Tjin Tham Sjin RM, Naspinski J, Birsner AE, Li C, Chan R, Lo KM, Gillies S, Zurakowski D, Folkman J, Samulski J and Javaherian K. Endostatin therapy reveals a U-shaped curve for antitumor activity. Cancer Gene Ther 13 (2006) 619-27.
- Qin G, Kishore R, Dolan CM, Silver M, Wecker A, Luedemann CN, Thorne T, Hanley A, Curry C, Heyd L, Dinesh D, Kearney M, Martelli F, Murayama T, Goukassian DA, Zhu Y and Losordo DW. Cell cycle regulator E2F1 modulates angiogenesis via p53-dependent transcriptional control of VEGF. Proc Natl Acad Sci USA 103 (2006) 11015-20.
- Abdollahi A, Hlatky L and Huber PE. Endostatin: the logic of antiangiogenic therapy. Drug Resist Updat. 8 (2005) 59-74.
- Zeng X, Chen J, Miller YI, Javaherian K and Moulton KS. Endostatin binds biglycan and LDL and interferes with LDL retention to the subendothelial matrix during atherosclerosis. J Lipid Res 46 (2005) 1849-59.
- Kieran MW, Turner CD, Rubin JB, Chi SN, Zimmerman MA, Chordas C, Klement G, Laforme A, Gordon A, Thomas A, Neuberg D, Browder T and Folkman J. A feasibility trial of antiangiogenic (metronomic) chemotherapy in pediatric patients with recurrent or progressive cancer. J Pediatr Hematol Oncol 27 (2005) 573-81.
- Kishore R, Qin G, Luedemann C, Bord E, Hanley A, Silver M, Gavin M, Yoon YS, Goukassian D and Losordo DW. The cytoskeletal protein ezrin regulates EC proliferation and angiogenesis via TNF-alpha-induced transcriptional repression of cyclin A. J Clin Invest 115 (2005) 1785-96.
- Abdollahi A, Hahnfeldt P, Maercker C, Grone HJ, Debus J, Ansorge W, Folkman J, Hlatky L and Huber PE. Endostatin's antiangiogenic signaling network. Mol Cell 13 (2004) 649-63.
- Hahnfeldt P, Folkman J and Hlatky L. Minimizing long-term tumor burden: the logic for metronomic chemotherapeutic dosing and its antiangiogenic basis. J Theor. Biol. 220 (2003) 545-54.
- Blackhall FH, Merry CL, Lyon M, Jayson GC, Folkman J, Javaherian K and Gallagher JT. Binding of endostatin to endothelial heparan sulphate shows a differential requirement for specific sulphates. Biochem J 375 (2003) 131-9.
- Moulton KS, Vakili K, Zurakowski D, Soliman M, Butterfield C, Sylvin E, Lo KM, Gillies S, Javaherian K and Folkman J. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci USA 100 (2003) 4736-41.
- Abdollahi A, Lipson KE, Sckell A, Zieher H, Klenke F, Poerschke D, Roth A, Han X, Krix M, Bischof M, Hahnfeldt P, Grone HJ, Debus J, Hlatky L and Huber PE. Combined therapy with direct and indirect angiogenesis inhibition results in enhanced antiangiogenic and antitumor effects. Cancer Res 63 (2003) 8890-8.
- Abdollahi A, Lipson KE, Han X, Krempien R, Trinh T, Weber KJ, Hahnfeldt P, Hlatky L, Debus J, Howlett AR, Huber PE. SU5416 and SU6668 attenuate the angiogenic effects of radiation-induced tumor cell growth factor production and amplify the direct anti-endothelial action of radiation in vitro. Cancer Res 63 (2003) 3755-63.
- Hlatky L, Hahnfeldt P and Folkman J. Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J Natl Cancer Inst 94 (2002) 883-93.
- Browder T, Folkman J, Hahnfeldt P, Heymach J, Hlatky L, Kieran M and Rogers MS. Antiangiogenic therapy and p53. Science 297 (2002) 471.
- Ambati BK, Joussen AM, Ambati J, Moromizato Y, Guha C, Javaherian K, Gillies S, O'Reilly MS and Adamis AP. Angiostatin inhibits and regresses corneal neovascularization. Arch Ophthalmol 120 (2002) 1063-8.
- Javaherian K, Park SY, Pickl WF, LaMontagne KR, Sjin RT, Gillies S and Lo KM. Laminin modulates morphogenic properties of the collagen XVIII endostatin domain. J Biol Chem 277 (2002) 45211-8.
- Panigrahy D, Singer S, Shen LQ, Butterfield CE, Freedman DA, Chen EJ, Moses MA, Kilroy S, Duensing S, Fletcher C, Fletcher JA, Hlatky L, Hahnfeldt P, Folkman J and Kaipainen A. PPARgamma ligands inhibit primary tumor growth and metastasis by inhibiting angiogenesis. J Clin Invest 110 (2002) 923-32.
- Sachs RK, Hlatky LR and Hahnfeldt P. Simple ODE models of tumor growth and anti-angiogenic or radiation treatment. Math Comp Modeling 33 (2001) 1297-305.
- Beecken WD, Fernandez A, Joussen AM, Achilles EG, Flynn E, Lo KM, Gillies SD, Javaherian K, Folkman J and Shing Y. Effect of antiangiogenic therapy on slowly growing, poorly vascularized tumors in mice. J Natl Cancer Inst 93 (2001) 382-7.
- Kuo CJ, LaMontagne Jr. KR, Garcia-Cardena G, Ackley BD, Kalman D, Park S, Christofferson R, Kamihara J, Ding YH, Lo KM, Gillies S, Folkman J, Mulligan RC and Javaherian K. Oligomerization-dependent regulation of motility and morphogenesis by the collagen XVIII NC1/endostatin domain. J Cell Biol 152 (2001) 1233-46.
- Goukassian D, Diez-Juan A, Asahara T, Schratzberger P, Silver M, Murayama T, Isner JM and Andres V. Overexpression of p27(Kip1) by doxycycline-regulated adenoviral vectors inhibits endothelial cell proliferation and migration and impairs angiogenesis. FASEB J 15 (2001) 1877-85.
- Folkman J, Hahnfeldt P and Hlatky L. Cancer: looking outside the genome. Nat Rev Mol Cell Biol 1 (2000) 76-9.
- Kerbel RS, Viloria-Petit A, Klement G and Rak J. 'Accidental' anti-angiogenic drugs. anti-oncogene directed signal transduction inhibitors and conventional chemotherapeutic agents as examples. Eur J Cancer 36 (2000) 1248-57.
- Klement G, Baruchel S, Rak J, Man S, Clark K, Hicklin DJ, Bohlen P and Kerbel RS. Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J Clin Invest 105 (2000) R15-24.
- Rak J and Klement G. Impact of oncogenes and tumor suppressor genes on deregulation of hemostasis and angiogenesis in cancer. Cancer Metastasis Rev 19 (2000) 93-6.
- Rak J, Yu JL, Klement G and Kerbel RS. Oncogenes and angiogenesis: signaling three-dimensional tumor growth. J Investig Dermatol Symp Proc 5 (2000) 24-33.
- Hahnfeldt P, Panigrahy D, Folkman J and Hlatky L. Tumor development under angiogenic signaling: a dynamical theory of tumor growth, treatment response, and postvascular dormancy. Cancer Res 59 (1999) 4770-5.
- Bergers G, Javaherian K, Lo KM, Folkman J and Hanahan D. Effects of angiogenesis inhibitors on multistage carcinogenesis in mice. Science 284 (1999) 808-12.
- Folkman J, Hahnfeldt P, Hlatky L. The logic of anti-angiogenic gene therapy. In: Friedmann T, editor. The Development of Gene Therapy, Ch. III. Target Tissues and Target Diseases - Cancer. New York: Cold Spring Harbor Laboratory Press (1998) p1-17.
- Ding YH, Javaherian K, Lo KM, Chopra R, Boehm T, Lanciotti J, Harris BA, Li Y, Shapiro R, Hohenester E, Timpl R, Folkman J and Wiley DC. Zinc-dependent dimers observed in crystals of human endostatin. Proc Natl Acad Sci USA 95 (1998) 10443-8.
- Hlatky L, Hahnfeldt P, Tsionou C and Coleman CN. Vascular endothelial growth factor: environmental controls and effects in angiogenesis. Br J Cancer Suppl 27 (1996) S151-6.
- Hlatky L, Tsionou C, Hahnfeldt P and Coleman CN. Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res 54 (1994) 6083-6.