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 the Center of Cancer Systems Biology. A sizable number of members of our team had tight research collaborations with or trained under Dr. Folkman. Among these are Lynn Hlatky, Philip Hahnfeldt, Amir Abdollahi, Giannoula Klement, Nava Almog, Clare Lamont, Abdo Abou-Slaybi, and Kashi Javaherian. Many of the angiogenic initiatives our researchers designed jointly with Dr. Folkman continue at the CCSB, 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 CCSB'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 (Hahnfeldt, Klement) |
| ii. | computational modeling of tumor angiogenic carrying capacity and its influence on tumor progression, including the induction of oscillatory behavior and dormancy (Hlatky, Hahnfeldt) |
| iii. | the molecular determinants of angiogenic signaling in tumor dormancy (Almog, Abdollahi) |
| iv. | the role of platelets in tumor angiogenesis and in other pathologic processes (Klement, Abou-Slaybi) |
| v. | pan-genomic implications of the angiogenic switch (Abdollahi, Hlatky, Hahnfeldt) |
| vi. | studies of radiation quality effect on the ability of the host to support tumor angiogenesis (Lamont – with Girdhani) |
| vii. | studies of the broader role of angiogenesis in radiation oncology (Hlatky, Abdollahi) |
| viii. | the study of intrinsic inhibitors of angiogenesis (Javaherian, Abdollahi). |
Publications:
A strong body of work on the topic of tumor angiogenesis has been published by researchers currently at the CCSB:
- Lignet F, Benzekry S, Wilson S, Billy F, Saut O, Tod M, You B, Adda Berkane A, Kassour S, Wei MX, Grenier E, Ribba B. Theoretical investigation of the efficacy of antiangiogenic drugs combined to chemotherapy in xenografted mice. J Theor Biol 320: 86-99, 2013. Epub 2012 Dec 21.
- Kareva I. Biological Stoichiometry in Tumor Micro-environments. PLoS One 8(1): e51844, 2013. Epub 2013 Jan 22.
- Almog N. Genes and Regulatory Pathways Involved in Persistence of Dormant Micro-tumors. Adv Exp Med Biol 734: 3-17, 2013. (also in Systems Biology of Tumor Dormancy. Enderling H, Almog N, Hlatky L, editors. New York: Springer; c2013. XVIII, 291p.)
- Hahnfeldt P. The host support niche as a control point for tumor dormancy: implications for tumor development and beyond. Adv Exp Med Biol 734: 19-35, 2013. (also in Systems Biology of Tumor Dormancy. Enderling H, Almog N, Hlatky L, editors. New York: Springer; c2013. XVIII, 291p.)
- Mayer EL, Isakoff SJ, Klement G, Downing SR, Chen WY, Hannagan K, Gelman R, Winer EP, Burstein HJ. Combination antiangiogenic therapy in advanced breast cancer: a phase 1 trial of vandetanib, a VEGFR inhibitor, and metronomic chemotherapy, with correlative platelet proteomics. Breast Cancer Res Treat 136(1): 169-78, 2012.
- Palladino M, Gatto I, Neri V, Stigliano E, Smith RC, Pola E, Straino S, Gaetani E, Capogrossi M, Leone G, Hlatky L, Pola R. Combined therapy with sonic hedgehog gene transfer and bone marrow-derived endothelial progenitor cells enhances angiogenesis and myogenesis in the ischemic skeletal muscle. J Vasc Res 49(5): 425-31, 2012. Epub 2012 Jun 22.
- Peterson JE, Zurakowski D, Italiano JE Jr, Michel LV, Connors S, Oenick M, D'Amato RJ, Klement GL, Folkman J. VEGF, PF4 and PDGF are elevated in platelets of colorectal cancer patients. Angiogenesis 15(2): 265-73, 2012. Epub 2012 Mar 9.
- Enderling H, Hahnfeldt P, Hlatky L, Almog N. Systems biology of tumor dormancy: linking biology and mathematics on multiple scales to improve cancer therapy. Cancer Res 72(9): 2172-5, 2012. Epub 2012 Mar 13.
- Benzekry S. Mathematical and numerical analysis of a model for anti-angiogenic therapy in metastatic cancers. Esaim Math Model Numer Anal 46(2): 207-37, 2012. Epub 2011 Oct 6.
- Benzekry S. Passing to the limit 2D-1D in a model for metastatic growth. J Biol Dyn 6 Suppl 1: 19-30, 2012. Epub 2011 Jun 24.
- Benzekry S, André N, Benabdallah A, Ciccolini J, Faivre C, Hubert F, Barbolosi D. Modeling the impact of anticancer agents on metastatic spreading. Math Model Natl Phenom 7(1): 306-36, 2012. Epub 2012 Jan 25.
- Benzekry S, Chapuisat G, Ciccolini J, Erlinger A, Hubert F. A new mathematical model for optimizing the combination between antiangiogenic and cytotoxic drugs in oncology / Un nouveau modèle mathématique pour l'optimisation des combinaisons antiangiogéniques/cytotoxiques en cancérologie. Comptes Rendus Mathematique 350(1-2): 23-8, 2012. Epub 2011 Dec 16.
- Palladino M, Gatto I, Neri V, Straino S, Silver M, Tritarelli A, Piccioni A, Smith RC, Gaetani E, Losordo DW, Crea F, Capogrossi M, Pola R. Pleiotropic beneficial effects of sonic hedgehog gene therapy in an experimental model of peripheral limb ischemia. Mol Ther 19(4): 658-66, 2011. Epub 2011 Jan 11.
- Benzekry S. Mathematical analysis of a two-dimensional population model of metastatic growth including angiogenesis. J Evol Equ 11(1): 187-213, 2011. Epub 2010 Dec 23.
- Almog N. Molecular mechanisms underlying tumor dormancy. Cancer Lett 294(2): 139-46, 2010. Epub 2010 Apr 2.
- Almog N, Klement G. Platelet Proteome and Tumor Dormancy: Can Platelets Content Serve as Predictive Biomarkers for Exit of Tumors from Dormancy? Cancers 2(2): 842-58, 2010.
- Fainaru O, Almog N, Nakai K, Montoya-Zavala M, Abdollahi A, D'Amato R, Ingber D. Immature dendritic cells promote angiogenesis and tumor growth. FASEB J 24(5): 1411-8, 2010.
- Lee TY, Muschal S, Pravda EA, Folkman J, Abdollahi A, Javaherian K. Angiostatin regulates the expression of antiangiogenic and proapoptotic pathways via targeted inhibition of mitochondrial proteins. Blood 114(9): 1987-98, 2009. Epub 2009 May 22.
- Straface G, Aprahamian T, Flex A, Gaetani E, Biscetti F, Smith RC, Pecorini G, Pola E, Angelini F, Stigliano E, Castellot JJ Jr, Losordo DW, Pola R. Sonic hedgehog regulates angiogenesis and myogenesis during post-natal skeletal muscle regeneration. J Cell Mol Med 13(8B): 2424-35, 2009. Epub 2008 Jul 26.
- Peterson JE, Zurakowski D, Italiano JE Jr, Michel LV, Fox L, Klement GL, Folkman J. Normal ranges of angiogenesis regulatory proteins in human platelets. A J Hematol 85(7): 487-93, 2010.
- 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, Folkman J. Platelets actively sequester angiogenesis regulators. Blood 113(12): 2835-42, 2009. Epub 2008 Nov 25.
- Almog N, Ma L, Raychowdhury R, Schwager C, Erber R, Short S, Hlatky L, Vajkoczy P, Huber PE, Folkman J, Abdollahi A. Transcriptional switch of dormant tumors to fast-growing angiogenic phenotype. Cancer Res 69(3): 836-44, 2009. Epub 2009 Jan 27.
- Biscetti F, Gaetani E, Flex A, Straface G, Pecorini G, Angelini F, Stigliano E, Aprahamian T, Smith RC, Castellot JJ, Pola R. Peroxisome proliferator-activated receptor alpha is crucial for iloprost-induced in vivo angiogenesis and vascular endothelial growth factor upregulation. J Vasc Res 46(2): 103-8, 2009. Epub 2008 Jul 10.
- Pietramaggiori G, Scherer SS, Cervi D, Klement G, Orgill DP. TUmors stimulate platelet delivery of angiogenic factors in vivo: an unexpected benefit. Am J Pathol 173(6): 1609-16, 2008.
- Biscetti F, Pola R. Endothelial progenitor cells and angiogenesis join the PPARty. Circ Res 103(1): 7-9, 2008.
- Biscetti F, Gaetani E, Flex A, Aprahamian T, Hopkins T, Straface G, Pecorini G, Stigliano E, Smith RC, Angelini F, Castellot JJ Jr, Pola R. Selective activation of peroxisome proliferator-activated receptor (PPAR)alpha and PPAR gamma induces neoangiogenesis through a vascular endothelial growth factor-dependent mechanism. Diabetes 57(5): 1394-404, 2008.
- Lee TY, Tjin Tham Sjin RM, Movahedi S, Ahmed B, Pravda EA, Lo KM, Gillies SD, Folkman J, Javaherian K. Linking antibody Fc domain to endostatin significantly improves endostatin half-life and efficacy. Clin Cancer Res 14(5): 1487-93, 2008.
- Italiano JE Jr, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, Ryeom S, Folkman J, Klement GL. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 111(3): 1227-33, 2008. Epub 2007 Oct 25.
- Cervi D, Yip TT, Bhattacharya N, Podust VN, Peterson J, Abou-Slaybi A, Naumov GN, Bender E, Almog N, Italiano Jr. JE, Folkman J, Klement GL. Platelet-associated PF-4 as a biomarker of early tumor growth. Blood 111(3): 1201-7, 2008. Epub 2007 Oct 3.
- 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, Huber PE. Transcriptional network governing the angiogenic switch in human pancreatic cancer. Proc Natl Acad Sci U S A 104(31): 12890-5, 2007. Epub 2007 Jul 24.
- 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, Losordo DW. Tumor necrosis factor-alpha receptor p75 is required in ischemia-induced neovascularization. Circulation 115(6): 752-62, 2007. Epub 2007 Jan 29.
- 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, Losordo DW. Cell cycle regulator E2F1 modulates angiogenesis via p53-dependent transcriptional control of VEGF. Proc Natl Acad Sci U S A 103(29): 11015-20, 2006. Epub 2006 Jul 11.
- Danese S, Sans M, de la Motte C, Graziani C, West G, Phillips MH, Pola R, Rutella S, Willis J, Gasbarrini A, Fiocchi C. Angiogenesis as a novel component of inflammatory bowel disease pathogenesis. Gastroenterology 130(7): 2060-73, 2006.
- Tjin Tham Sjin RM, Naspinski J, Birsner AE, Li C, Chan R, Lo KM, Gillies S, Zurakowski D, Folkman J, Samulski J, Javaherian K. Endostatin therapy reveals a U-shaped curve for antitumor activity. Cancer Gene Ther 13(6): 619-27, 2006.
- Clamp A, Blackhall FH, Henrioud A, Jayson GC, Javaherian K, Esko J, Gallagher JT, Merry CL. The morphogenic properties of oligomeric endostatin are dependent on cell surface heparan sulfate. J Biol Chem 281(21): 14813-22, 2006. Epub 2006 Feb 15.
- Almog N, Henke V, Flores L, Hlatky L, Kung AL, Wright RD, Berger R, Hutchinson L, Naumov GN, Bender E, Akslen LA, Achilles EG, Folkman J. Prolonged dormancy of human liposarcoma is associated with impaired tumor angiogenesis. FASEB J 20(7): 947-9, 2006. Epub 2006 Apr 25.
- Becker CM, Sampson DA, Short SM, Javaherian K, Folkman J, D'Amato RJ. Short synthetic endostatin peptides inhibit endothelial migration in vitro and endometriosis in a mouse model. Fertil Steril 85(1): 71-7, 2006.
- 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(11): 573-81, 2005.
- Zeng X, Chen J, Miller YI, Javaherian K, Moulton KS. Endostatin binds biglycan and LDL and interferes with LDL retention to the subendothelial matrix during atherosclerosis. J Lipid Res 46(9): 1849-59, 2005. Epub 2005 Jul 1.
- Kishore R, Qin G, Luedemann C, Bord E, Hanley A, Silver M, Gavin M, Yoon YS, Goukassian D, Losordo DW. The cytoskeletal protein ezrin regulates EC proliferation and angiogenesis via TNF-alpha-induced transcriptional repression of cyclin A. J Clin Invest 115(8): 1785-96, 2005. Epub 2005 Jun 16.
- Abdollahi A, Hlatky L, Huber PE. Endostatin: the logic of antiangiogenic therapy. Drug Resist Updat 8(1-2): 59-74, 2005. Epub 2005 Apr 7.
- Bosch-Marcé M, Pola R, Wecker AB, Silver M, Weber A, Luedemann C, Curry C, Murayama T, Kearney M, Yoon YS, Malinow MR, Asahara T, Isner JM, Losordo DW. Hyperhomocyst(e)inemia impairs angiogenesis in a murine model of limb ischemia. Vasc Med 10(1): 15-22, 2005.
- Pola R, Aprahamian TR, Bosch-Marcé M, Curry C, Gaetani E, Flex A, Smith RC, Isner JM, Losordo DW. Age-dependent VEGF expression and intraneural neovascularization during regeneration of peripheral nerves. Neurobiol Aging 25(10):1361-8, 2004.
- Abdollahi A, Hahnfeldt P, Maercker C, Grone HJ, Debus J, Ansorge W, Folkman J, Hlatky L, Huber PE. Endostatin's antiangiogenic signaling network. Mol Cell 13(5): 649-63, 2004.
- Pola R, Gaetani E, Flex A, Aprahamian TR, Bosch-Marcé M, Losordo DW, Smith RC, Pola P. Comparative analysis of the in vivo angiogenic properties of stable prostacyclin analogs: a possible role for peroxisome proliferator-activated receptors. J Mol Cell Cardiol 36(3): 363-70, 2004.
- 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, Huber PE. Combined therapy with direct and indirect angiogenesis inhibition results in enhanced antiangiogenic and antitumor effects. Cancer Res 63(24): 8890-8, 2003.
- Pola R, Gaetani E, Flex A, Aprahamian T, Proia AS, Bosch-Marcé M, Smith RC, Pola P. Peripheral nerve ischemia: apolipoprotein E deficiency results in impaired functional recovery and reduction of associated intraneural angiogenic response. Exp Neurol 184(1): 264-73, 2003.
- Blackhall FH, Merry CL, Lyon M, Jayson GC, Folkman J, Javaherian K, Gallagher JT. Binding of endostatin to endothelial heparan sulphate shows a differential requirement for specific sulphates. Biochem J 375(Pt 1): 131-9, 2003.
- Pola R, Ling LE, Aprahamian TR, Barban E, Bosch-Marce M, Curry C, Corbley M, Kearney M, Isner JM, Losordo DW. Postnatal recapitulation of embryonic hedgehog pathway in response to skeletal muscle ischemia. Circulation 108(4): 479-85, 2003. Epub 2003 Jul 14.
- 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(13): 3755-63, 2003.
- Moulton KS, Vakili K, Zurakowski D, Soliman M, Butterfield C, Sylvin E, Lo KM, Gillies S, Javaherian K, Folkman J. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci U S A 100(8): 4736-41, 2003. Epub 2003 Apr 7.
- Hahnfeldt P, Folkman J, Hlatky L. Minimizing long-term tumor burden: the logic for metronomic chemotherapeutic dosing and its antiangiogenic basis. J Theor Biol 220(4): 545-54, 2003.
- Javaherian K, Park SY, Pickl WF, LaMontagne KR, Sjin RT, Gillies S, Lo KM. Laminin modulates morphogenic properties of the collagen XVIII endostatin domain. J Biol Chem 277(47): 45211-8, 2002. Epub 2002 Sep 16.
- 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, Kaipainen A. PPARgamma ligands inhibit primary tumor growth and metastasis by inhibiting angiogenesis. J Clin Invest 110(7): 923-32, 2002.
- Ambati BK, Joussen AM, Ambati J, Moromizato Y, Guha C, Javaherian K, Gillies S, O'Reilly MS, Adamis AP. Angiostatin inhibits and regresses corneal neovascularization. Arch Ophthalmol 120(8): 1063-8, 2002.
- Browder T, Folkman J, Hahnfeldt P, Heymach J, Hlatky L, Kieran M, Rogers MS. Antiangiogenic therapy and p53. Science 297(5581): 471, 2002.
- Hlatky L, Hahnfeldt P, Folkman J. Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J Natl Cancer Inst 94(12): 883-93, 2002.
- Goukassian D, Díez-Juan A, Asahara T, Schratzberger P, Silver M, Murayama T, Isner JM, Andrés V. Overexpression of p27(Kip1) by doxycycline-regulated adenoviral vectors inhibits endothelial cell proliferation and migration and impairs angiogenesis. FASEB J 15(11): 1877-85, 2011.
- Pola R, Ling LE, Silver M, Corbley MJ, Kearney M, Blake Pepinsky R, Shapiro R, Taylor FR, Baker DP, Asahara T, Isner JM. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat Med 7(6): 706-11, 2001.
- Sachs RK, Hlatky LR, Hahnfeldt P. Simple ODE models of tumor growth and anti-angiogenic or radiation treatment. Math Comp Modeling 33(12-13): 1297-305, 2001.
- Kuo CJ, LaMontagne KR Jr, Garcia-Cardeña G, Ackley BD, Kalman D, Park S, Christofferson R, Kamihara J, Ding YH, Lo KM, Gillies S, Folkman J, Mulligan RC, Javaherian K. Oligomerization-dependent regulation of motility and morphogenesis by the collagen XVIII NC1/endostatin domain. J Cell Biol 152(6): 1233-46, 2001.
- Beecken WD, Fernandez A, Joussen AM, Achilles EG, Flynn E, Lo KM, Gillies SD, Javaherian K, Folkman J, Shing Y. Effect of antiangiogenic therapy on slowly growing, poorly vascularized tumors in mice. J Natl Cancer Inst 93(5): 382-7, 2001.
- Rak J, Yu JL, Klement G, Kerbel RS. Oncogenes and angiogenesis: signaling three-dimensional tumor growth. J Investig Dermatol Symp Proc 5(1): 24-33, 2000.
- Folkman J, Hahnfeldt P, Hlatky L. Cancer: looking outside the genome. Nat Rev Mol Cell Biol 1(1): 76-9, 2000.
- Kerbel RS, Viloria-Petit A, Klement G, Rak J. ‘Accidental’ anti-angiogenic drugs. anti-oncogene directed signal transduction inhibitors and conventional chemotherapeutic agents as examples. Eur J Cancer 36(10): 1248-57, 2000.
- Rak J, Klement G. Impact of oncogenes and tumor suppressor genes on deregulation of hemostasis and angiogenesis in cancer. Cancer Metastasis Rev 1(1-2): 93-6, 2000.
- Klement G, Baruchel S, Rak J, Man S, Clark K, Hicklin DJ, Bohlen P, Kerbel RS. Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J Clin Invest 105(8): R15-24, 2000.
- Hahnfeldt P, Panigrahy D, Folkman J, Hlatky L. Tumor development under angiogenic signaling: a dynamical theory of tumor growth, treatment response, and postvascular dormancy. Cancer Res 59(19): 4770-5, 1999.
- Bergers G, Javaherian K, Lo KM, Folkman J, Hanahan D. Effects of angiogenesis inhibitors on multistage carcinogenesis in mice. Science 284(5415): 808-12, 1999.
- Ding YH, Javaherian K, Lo KM, Chopra R, Boehm T, Lanciotti J, Harris BA, Li Y, Shapiro R, Hohenester E, Timpl R, Folkman J, Wiley DC. Zinc-dependent dimers observed in crystals of human endostatin. Proc Natl Acad Sci U S A 95(18): 10443-8, 1998.
- 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.
- Hlatky L, Hahnfeldt P, Tsionou C, Coleman CN. Vascular endothelial growth factor: environmental controls and effects in angiogenesis. Br J Cancer Suppl 27: S151-6, 1996.
- Hlatky L, Tsionou C, Hahnfeldt P, Coleman CN. Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res 54(23): 6083-6, 1994.