Skip to main content
SpringerLink
Log in

Cooperative Interactions Between Integrins and Growth Factor Signaling in Pathological Angiogenesis

  • Chapter
  • First Online:
The Tumor Microenvironment

Part of the book series: Cancer Drug Discovery and Development ((CDD&D))

  • 2836 Accesses

Abstract

As with most complex biological processes, angiogenesis requires the integration of a number of molecular signaling networks to coordinate multiple cues from both the extracellular tissue microenvironment as well as the cell’s interior. Thus an important area of angiogenesis investigation involves understanding the mechanisms that facilitate cooperation between multiple receptor–ligand signaling pathways. Two crucial networks that play active role in angiogenesis include growth factor/growth factor receptors and extracellular matrix/integrin receptor signaling systems. Emerging evidence suggests that these two important signaling systems depend in large part on each other, and function cooperatively to control new blood vessel development. Given the tissue-specific variations in the expression of components within each of these systems, significant challenges exist in order to exploit these signaling pathways for clinical intervention. A more detailed understanding of how the molecular components of these two signaling systems communicate with each other to direct and coordinate downstream effector functions may lead to optimized anti-angiogenic strategies to control malignant tumor progression. In this regard, we will discuss the multiple ways by which growth factor and integrin signaling pathways function cooperatively to regulate pathological angiogenesis within the context of the tissue microenvironment.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aidoudi S, Bujakowska K, Kieffer N et al (2008) The CXC-chemokine CXCL4 interacts with integrins implicated in angiogenesis. PLoS One. doi:10.137/journal.pone.0002657

    Google Scholar 

  • Akalu A, Cretu A, Brooks PC (2005) Targeting integrins for the control of tumor angiogenesis. Expert Opin Investig Drugs 14:1475–1486

    Article  PubMed  CAS  Google Scholar 

  • Alavi AS, Acevedo L, Min W et al (2007) Chemoresistance of endothelial cells induced by basic fibroblast growth factor depends on Raf-1-mediated inhibition of the proapoptotic kinase, ASK1. Cancer Res 67:2766–7272

    Article  PubMed  CAS  Google Scholar 

  • Alavi A, Hood JD, Frausto R et al (2003) Role of Raf in vascular protection from distinct apoptotic stimuli. Science 301:94–96

    Article  PubMed  CAS  Google Scholar 

  • Astrof S, Hynes RO (2009) Fibronectins in vascular morphogenesis. Angiogenesis 12:165–175

    Article  PubMed  CAS  Google Scholar 

  • Avraamides CJ, Garmy-Susini B, Varner JA (2008) Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer 8:604–617

    Article  PubMed  CAS  Google Scholar 

  • Bader BL, Rayburn H, Crowley D et al (1998) Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all alpha v integrins. Cell 95:507–519

    Article  PubMed  CAS  Google Scholar 

  • Borges E, Jan Y, Ruoslahti E (2000) Platelet-derived growth factor beta and vascular endothelial growth factor receptor 2 bind to beta 3 integrin through its extracellular domain. J Biol Chem 275:39867–39873

    Article  PubMed  CAS  Google Scholar 

  • Brooks PC, Clark RA, Cheresh DA (1994) Requirement of vascular integrin αvβ3 for angiogenesis. Science 264:569–571

    Article  PubMed  CAS  Google Scholar 

  • Burri PH, Hlushchuk R, Djonov V (2004) Intussuceptive angiogenesis: its emergence, its characteristics, and its significance. Dev Dyn 231:474–488

    Article  PubMed  Google Scholar 

  • Carbonell WS, Ansorge O, Sibson N et al (2009) The vascular basement membrane as “soil” in brain metastasis. PLoS One 4:1–14

    Article  Google Scholar 

  • Cascone I, Napione L, Maniero F et al (2005) Stable interaction between alpha 5 beta 1 integrin and Tie2 tyrosine kinase receptor regulates endothelial cell response to Ang-1. J Cell Biol 170:993–1004

    Article  PubMed  CAS  Google Scholar 

  • Cavallaro U, Tenan M, Castelli V et al (2001) Response of bovine endothelial cells to FGF-2 and VEGF is dependent on their site of origin: relevance to the regulation of angiogenesis. J Cell Biochem 82:619–633

    Article  PubMed  CAS  Google Scholar 

  • Chen CC, Chen N, Lau LF (2001) The angiogenic factors Cyr61 and connective tissue growth factor induces adhesive signaling in primary human skin fibroblasts. J Biol Chem 276:10443–10452

    Article  PubMed  CAS  Google Scholar 

  • Chung ES, Chauhan SK, Jin Y et al (2009) Contribution of macrophages to angiogenesis induced by vascular endothelial growth factor receptor-3-specific ligands. Am J Pathol 175:1984–1992

    Article  PubMed  Google Scholar 

  • Chang J, Bachelder RE, Lipscomb EA et al (2002) Integrin (alpha 6 beta 4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cell. J Cell Biol 158:165–174

    Article  Google Scholar 

  • Clark RA (2008) Synergistic signaling from extracellular matrix-growth factor complexes. J Invest Dermatol 128:1354–1355

    Article  PubMed  CAS  Google Scholar 

  • Clemmons DR, Maile LA (2005) Interaction between insulin-like growth factor-I receptor and alpha V beta 3 integrin linked signaling pathways: cellular responses to changes in multiple signaling inputs. Mol Endocrinol 19:1–11

    Article  PubMed  CAS  Google Scholar 

  • Colmone A, Sipkins DA (2008) Beyond angiogenesis: the role of endothelium in the bone marrow vascular niche. Transl Res 151:1–9

    Article  PubMed  CAS  Google Scholar 

  • Contois C, Akalu A, Brooks PC (2009) Integrins as functional hubs in the regulation of pathological angiogenesis. Semin Cancer Biol 19:318–328

    Article  PubMed  CAS  Google Scholar 

  • Delcommenne M, Streuli CH (1995) Control of integrin expression by extracellular matrix. J Biol Chem 270:26794–26801

    Article  PubMed  CAS  Google Scholar 

  • Ebos JM, Lee CR, Kerbel RS (2009) Tumor and host-mediated pathways of resistance and disease progression in response to antiangiogenic therapy. Clin Cancer Res 15:5020–5025

    Article  PubMed  CAS  Google Scholar 

  • Eliceiri BP, Paul R, Schwartzberg PL et al (1999) selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 4:915–924

    Article  PubMed  CAS  Google Scholar 

  • Eliceiri BP, Puente XS, Hood JD et al (2002) Src-mediated coupling of focal adhesion kinase to integrin αvβ5 in vascular endothelial growth factor signaling. J Cell Biol 157:149–159

    Article  PubMed  CAS  Google Scholar 

  • Elsegood CL, Zhuo Y, Wesolowski GA et al (2006) M-CSF induces the stable interaction of cFms with alpha v beta 3 integrin in osteoclasts. Int J Biochem Cell Biol 38:1518–1529

    Article  PubMed  CAS  Google Scholar 

  • Engelman JA (2009) Targeting PI3K signaling in cancer: opportunities, challenges and limitations. Nat Rev 9:550–562

    Article  CAS  Google Scholar 

  • Falcioni R, Antonini A, Nisticò P et al (1997) Alpha 6 beta 4 and alpha 6 beta 1 integrins associate with ErbB-2 in human carcinoma cell lines. Exp Cell Res 236:76–85

    Article  PubMed  CAS  Google Scholar 

  • Feng X, Clark AF, Galanakis D et al (1999) Fibrin and collagen differentially regulate human dermal microvascular endothelial cell integrins: stabilization of αv/β3 mRNA by fibrin. J Invest Dermatol 113:913–919

    Article  PubMed  CAS  Google Scholar 

  • Fernado NT, Koch M, Rothrock C et al (2008) Tumor escape from endogenous, extracellular matrix-associated angiogenesis inhibitors by up-regulation of multiple proangiogenic factors. Clin Cancer Res 14:1529–1539

    Article  Google Scholar 

  • Fischer C, Schneider M, Carmeliet P (2006) Principles and therapeutic implications of angiogenesis, vasculogenesis and arteriogenesis. Hand Exp Pharmacol 176:157–212

    Article  CAS  Google Scholar 

  • Folkman J (2007) Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 6:273–286

    Article  PubMed  CAS  Google Scholar 

  • Fornaro M, Plescia J, Chheang S et al (2003) Fibronectin protects prostate cancer cells from tumor necrosis factor-α-induced apoptosis via the AKT/Survivin pathway. J Biol Chem 278:50402–50411

    Article  PubMed  CAS  Google Scholar 

  • Friedlander M, Brooks PC, Shaffer RW et al (1995) Definition of two angiogenic pathways by distinct alpha v integrins. Science 270:1500–1502

    Article  PubMed  CAS  Google Scholar 

  • Ghosh K, Thodeti CK, Dudley AC et al (2008) Tumor-derived endothelial cells exhibit aberrant Rho-mediated mechanosensing and abnormal angiogenesis in vitro. Proc Natl Acad Sci U S A 105:11305–11310

    Article  PubMed  CAS  Google Scholar 

  • Greenberg JI, Shields DJ, Barillas SG et al (2008) A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 456:809–813

    Article  PubMed  CAS  Google Scholar 

  • Guo P, Xu L, Pan S et al (2001) Vascular endothelial growth factor isoforms display distinct activities in promoting tumor angiogenesis at different anatomic sites. Cancer Res 61:8569–8577

    PubMed  CAS  Google Scholar 

  • Hida K, Klagsbrun M (2005) A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities. Cancer Res 65:2507–2510

    Article  PubMed  CAS  Google Scholar 

  • Hlushchuk R, Riesterer O, Baum O et al (2008) Tumor recovery by angiogenic switch from sprouting to intussuceptive angiogenesis after treatment with PTK787/ZK222584 or ionizing radiation. Am J Pathol 173:1173–1185

    Article  PubMed  CAS  Google Scholar 

  • Hodivala-Dilke KM, Reynolds AR, Reynolds LE (2003) Integrins in angiogenesis: multitalented molecules in a balancing act. Cell Tissue Res 314:131–144

    Article  PubMed  CAS  Google Scholar 

  • Hood JD, Frausto R, Kiosses WB et al (2003) Differential αv integrin-mediated Ras-ERK signaling during two pathways of angiogenesis. J Cell Biol 162:933–943

    Article  PubMed  CAS  Google Scholar 

  • Huang SC, Fraenkel E (2009) Integrating proteomic, transcriptional, and interactome data reveals hidden components of signaling and regulatory networks. Sci Signal 2:1–10

    Google Scholar 

  • Hutchings H, Ortega N, Plouët J (2003) Extracellular matrix-bound vascular endothelial growth factor promotes endothelial cell adhesion, migration, and survival through integrin ligation. FASEB J 11:1520–1532

    Google Scholar 

  • Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326:1216–1219

    Article  PubMed  CAS  Google Scholar 

  • Ivaska J, Heino J (2010) Interplay between cell adhesion and growth factor receptors: from plasma membranes to the endosomes. Cell Tissue Res 339:111–120

    Article  PubMed  CAS  Google Scholar 

  • Jendraschak E, Kaminski WE, Kiefl R et al (1998) IGF-1, PDGF and CD18 are adhesive responsive genes: regulation during monocyte differentiation. Biochim Biophys Acta 1396:320–335

    Article  PubMed  CAS  Google Scholar 

  • Kilarski WW, Samolov B, Petersson L et al (2009) Biomechanical regulation of blood vessel growth during tissue vascularization. Nat Med 15:657–664

    Article  PubMed  CAS  Google Scholar 

  • Kim KK, Wei Y, Szekeres C et al (2009) Epithelial cell α3β1 integrin links β-catenin and smad signaling to promote myofibroblast formation and pulmonary fibrosis. J Clin Invest 119: 213–224

    PubMed  CAS  Google Scholar 

  • Klement GL, Yip TT, Cassiola F et al (2008) Platelets actively sequester angiogenesis regulators. Blood 5:125–135

    Google Scholar 

  • Kubota Y, Takubo K, Shimizu T et al (2009) M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J Exp Med 206:1089–1102

    Article  PubMed  CAS  Google Scholar 

  • Lazova R, Rothberg G, Rimm D et al (2009) The semaphoring 7A receptor plexin C1 is lost during melanoma metastasis. Am J Dermatopathol 31:177–181

    Article  PubMed  Google Scholar 

  • Lorger M, Krueger JS, O’Neal M et al (2009) Activation of tumor cell integrin αvβ3 controls angiogenesis and metastatic growth in the brain. Proc Natl Acad Sci U S A 106:10666–10671

    Article  PubMed  CAS  Google Scholar 

  • MacDonald TJ, Stewart CF, Kocak M et al (2008) Phase I clinical trial of cilengitide in children with refractory brain tumors: pediatric brain tumor consortium study PBTC-012. J Clin Oncol 26: 919–924

    Article  PubMed  CAS  Google Scholar 

  • Madri JA, Pratt BM, Tucker AM (1988) Phenotypic modulation of endothelial cells by transforming growth factor-β depends upon the composition and organization of the extracellular matrix. J Cell Biol 106:1375–1384

    Article  PubMed  CAS  Google Scholar 

  • Mikkelsen T, Brodie C, Finniss S et al (2009) Radiation sensitization of glioblastoma by cilengitide has unanticipated schedule-dependency. Int J Cancer 124:2719–2727

    Article  PubMed  CAS  Google Scholar 

  • Magnon C, Galaup A, Mullan B et al (2005) Canstatin acts on endothelial and tumor cells via mitochondrial damage initiated through interaction with alpha v beta 3 and alpha v beta 5 integrins. Cancer Res 65:4353–4361

    Article  PubMed  CAS  Google Scholar 

  • Mahabeleshwar GH, Feng W, Phillips DR et al (2006) Integrin signaling is critical for pathological angiogenesis. J Exp Med 203:2495–2507

    Article  PubMed  CAS  Google Scholar 

  • Mahabeleshwar GH, Feng W, Reddy K et al (2007) Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ Res 101:570–580

    Article  PubMed  CAS  Google Scholar 

  • Mattila E, Auvinen K, Salmi M et al (2008) The protein tyrosine phosphatase TCPTP controls VEGFR2 signaling. J Cell Sci 121:3570–3580

    Article  PubMed  CAS  Google Scholar 

  • Mattila E, Pellinen T, Nevo J et al (2004) Negative regulation of EGFR signaling through integrin-a1β1-mediated activation of protein tyrosine phosphatase TCPTP. Nat Cell Biol 7:78–85

    Article  PubMed  Google Scholar 

  • Mikelis C, Sfaelou E, Koutsioumpa M et al (2009) Integrin αvβ3 is a pleiotrophin receptor required for pleiotrophin-induced endothelial cell migration through receptor protein tyrosine phosphatase β/ζ. FASEB J 23:1459–1469

    Article  PubMed  CAS  Google Scholar 

  • Mittola S, Brenchio B, Piccinini M et al (2006) Type I collagen limits VEGFR-2 signaling by SHP2 protein-tyrosine phosphatase-dependent mechanism. Circ Res 98:45–54

    Article  Google Scholar 

  • Mori S, Wu CY, Yamaji S et al (2008) Direct binding of integrin αvβ3 to FGF1 plays a role in FGF1 signaling. J Biol Chem 283:18066–18075

    Article  PubMed  CAS  Google Scholar 

  • Mousa SA, Lorelli W, Campochiaro (1999) Role of hypoxia and extracellular matrix-integrin binding in the modulation of angiogenic growth factors secretion by retinal pigmented epithelial cells. J Cell Biochem 74:135–143

    Google Scholar 

  • Munger JS, Harpel JG, Giancotti FG et al (1998) Interactions between growth factors and integrins: latent forms of transforming growth factor-β are ligands for integrin αvβ1. Mol Biol Cell 9:2627–2638

    PubMed  CAS  Google Scholar 

  • Murdoch C, Muthana M, Coffelt SB et al (2008) The role of myeloid cells in the promotion of tumor angiogenesis. Nat Rev Cancer 8:618–631

    Article  PubMed  CAS  Google Scholar 

  • Petitclerc E, Boutaud A, Prestayko A et al (2000) New functions for non-collagenous domains of human collagen type IV: novel integrin ligands inhibiting angiogenesis and tumor growth in vv. J Biol Chem 275:8051–8061

    Article  PubMed  CAS  Google Scholar 

  • Puigvert JC, Huveneers S, Fredriksson L (2009) Cross-talk between integrins and oncogenes modulates chemosensitivity. Mol Pharmacol 75:947–955

    Article  PubMed  CAS  Google Scholar 

  • Rahman S, Patel Y, Murray J et al (2005) Novel hepatocyte growth factor (HGF) binding domains on fibronectin and vitronectin coordinate a distinct and amplified Met-integrin induced signaling pathway in endothelial cells. BMC Cell Biol 6:8–14

    Article  PubMed  Google Scholar 

  • Rapisarda A, Melillo G (2009) Role of hypoxic tumor microenvironment in the resistance to anti-angiogenic therapies. Drug Resist Updat 12:74–80

    Article  PubMed  CAS  Google Scholar 

  • Retta SF, Cassara G, D’Amato M et al (2001) Cross talk between β1 and αv integrins: β1 affects β3 mRNA stability. Mol Biol Cell 12:3126–3138

    PubMed  CAS  Google Scholar 

  • Reynolds AR, Reynolds LE, Nagel TE et al (2004) Elevated Flk1 (vascular endothelial growth factor receptor 2) signaling mediates enhanced angiogenesis in β3-integrin-deficient mice. Cancer Res 64:8643–8650

    Article  PubMed  CAS  Google Scholar 

  • Reynolds LE, Conti FJ, Lucas M et al (2005) Accelerated re-epithelialization in β3-integrin-deficient mice is associated with enhanced TGF-β1 signaling. Nat Med 11:167–174

    Article  PubMed  CAS  Google Scholar 

  • Reynolds LE, Wyder L, Lively JC et al (2002) Enhanced pathological angiogenesis in mice lacking β3 integrin or β3 and β5 integrins. Nat Med 8:27–34

    Article  PubMed  CAS  Google Scholar 

  • Ricono JM, Huang M, Barnes LA et al (2009) Specific cross talk between epidermal growth factor receptor and integrin αvβ5 promotes carcinoma cell invasion and metastasis. Cancer Res 69:1383–1391

    Article  PubMed  CAS  Google Scholar 

  • Sahni A, Sahni SK, Francis CW (2005) Endothelial cell activation by IL-1β in the presence of fibrinogen requires αvβ3. Arterioscler Thromb Vasc Biol 25:2222–2227

    Article  PubMed  CAS  Google Scholar 

  • Sasaki T, Timpl R (2001) Domain IVa of laminin α5 chain is cell-adhesive and binds β1 and αvβ3 integrins through Arg-Gly-Asp. FEBS Lett 509:181–185

    Article  PubMed  CAS  Google Scholar 

  • Scaffidi AK, Petrovic N, Moddley YP et al (2004) αvβ3 integrin interacts with the transforming growth factor β (TGFβ) type II receptor to potentiate the proliferative effects of TGFβ1 in living human lung fibroblasts. J Biol Chem 279:37726–37733

    Article  PubMed  CAS  Google Scholar 

  • Schneller M, Vuori K, Ruoslahti E (1997) Alpha v beta 3 integrin associates with activated insulin and PDGFbeta receptors and potentiates the biological activity of PDGF. EMBO J 16:5600–56007

    Article  PubMed  CAS  Google Scholar 

  • Schultz GS, Wysocki A (2009) Interactions between extracellular matrix and growth factors in wound healing. Wound Rep Reg 17:153–162

    Article  Google Scholar 

  • Shaw RJ, Doherty DE, Ritter AG et al (1990) Adherence-dependent increase in human monocyte PDGF(B) mRNA is associated with increase in c-fos, c-jun, and EGR2 mRNA. J Cell Biol 111:2139–2148

    Article  PubMed  CAS  Google Scholar 

  • Shim SW, Ho IA, Wong PE (2007) Angiopoietin: a TIE(d) balance in tumor angiogenesis. Mol Cancer Res 5:655–665

    Article  PubMed  CAS  Google Scholar 

  • Soldi R, Mitola S, Strasly M (1999) Role of alpha v beta 3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J 8:882–892

    Article  Google Scholar 

  • Somanath PR, Ciocea A, Byzova TV (2008) Integrin and growth factor receptor alliance in angiogenesis. Cell Biochem Biophys doi:10.1007/s12013-008-9040-5

    Google Scholar 

  • St Croix B, Rago C, Velculescu V et al (2000) Gene expressed in human endothelium. Science 289:1197–1202

    Article  PubMed  CAS  Google Scholar 

  • Staniszewska I, Sariyer IK, Lecht S et al (2008) Integrin alpha9 beta1 is a receptor for nerve growth factor and other neurotrophins. J Cell Sci 121:504–513

    Article  PubMed  CAS  Google Scholar 

  • Streuli CH, Akhtar N (2009) Signal cooperation between integrins and other receptor systems. Biochem J 418:491–506

    Article  PubMed  CAS  Google Scholar 

  • Sudhakar A, Boosani C S (2008) Inhibition of tumor angiogenesis by tumstatin: insights into signaling mechanisms and implications in cancer regression. Pharm Res 25:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Toge H, Inagaki T, Kojimoto Y et al (2009) Angiogenesis in renal cell carcinoma: the role of tumor-associated macrophages. Int J Urol 16: 801–807

    Article  PubMed  CAS  Google Scholar 

  • Toledo MS, Suzuki E, Handa K et al (2005) Effect of ganglioside and tetraspanins in microdomains on interaction of integrins with fibroblast growth factor receptor. J Biol Chem 280:16227–16234

    Article  PubMed  CAS  Google Scholar 

  • Virrey JJ, Guan S, Li W et al (2008) Increased survivin expression confers chemoresistance to tumor-associated endothelial cells. Am J Pathol 173:575–585

    Article  PubMed  CAS  Google Scholar 

  • Vlahakis N, Young BA, Atakilit A et al (2007) Integrin α9β1 directly binds vascular endothelial growth factor (VEGF)-A and contributes to VEGF-A-induced angiogenesis. J Biol Chem 282:15187–15196

    Article  PubMed  CAS  Google Scholar 

  • Wagner EF, Nebreda AR (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev 9:537–549

    Article  CAS  Google Scholar 

  • Walker JL, Fournier AK, Assoian RK (2005) Regulation of growth factor signaling and cell cycle progression by cell adhesion and adhesion-dependent changes in cell tension. Cyt Growth Factor Rev 16:395–405

    Article  CAS  Google Scholar 

  • Wegener KL, Campbell ID (2008) Transmembrane and cytoplasmic domains in integrin activation and protein–protein interactions. Mol Membr Biol 25:76–87

    Article  Google Scholar 

  • Wickström SA, Alitalo K, Keski-Oja J et al (2004) An endostatin-derived peptide interacts with integrins and regulates actin cytoskeleton and migration of endothelial cells. J Biol Chem 279:20178–20185

    Article  PubMed  Google Scholar 

  • Wipff PJ, Hinz B (2008) Integrins and activation of latent transforming growth factor β1 – an intimate relationship. Eur J Cell Biol 87:601–615

    Article  PubMed  CAS  Google Scholar 

  • Woodal BP, Nyström A, Iozzo RA et al (2008) Integrin alpha 2 beta 1 is the required receptor for endorepellin angiostatic activity. J Biol Chem 283:2335–2343

    Article  Google Scholar 

  • Yan W, Bentley B, Shao R (2008) Distinct angiogenic mediators are required for basic fibroblast growth factor- and vascular endothelial growth factor-induced angiogenesis: the role of cytoplasmic tyrosine kinase c-Abl in tumor angiogenesis. Mol Biol Cell 19:2278–2288

    Article  PubMed  CAS  Google Scholar 

  • Zaidel-Bar R, Itzkovitz S, Ma’ayan A et al (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 9:858–867

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by grant 2ROICA91645 to PCB and grant P20RR15555 to Robert Friesel and subproject to PCB. We would like to apologize to all those investigators whose important work was not discussed due to space limitations.

Author information

Authors and Affiliations

  1. Maine Medical Center Research Institute, Center for Molecular Medicine, 81 Research Drive, Scarborough, ME, USA

    Peter C. Brooks

Authors
  1. Jennifer Roth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric Tweedie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter C. Brooks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter C. Brooks .

Editor information

Editors and Affiliations

  1. Genzyme Corporation, Mountain Rd. 1, Framingham, 01701-9322, Massachusetts, USA

    Rebecca G. Bagley

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Roth, J., Tweedie, E., Brooks, P.C. (2010). Cooperative Interactions Between Integrins and Growth Factor Signaling in Pathological Angiogenesis. In: Bagley, R. (eds) The Tumor Microenvironment. Cancer Drug Discovery and Development. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-6615-5_29

Download citation

  • DOI: https://doi.org/10.1007/978-1-4419-6615-5_29

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4419-6614-8

  • Online ISBN: 978-1-4419-6615-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation