DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Extracellular matrix and growth factor engineering for controlled angiogenesis in regenerative medicine

Abstract

In this study, blood vessel growth plays a key role in regenerative medicine, both to restore blood supply to ischemic tissues and to ensure rapid vascularization of clinical-size tissue-engineered grafts. For example, vascular endothelial growth factor (VEGF) is the master regulator of physiological blood vessel growth and is one of the main molecular targets of therapeutic angiogenesis approaches. However, angiogenesis is a complex process and there is a need to develop rational therapeutic strategies based on a firm understanding of basic vascular biology principles, as evidenced by the disappointing results of initial clinical trials of angiogenic factor delivery. In particular, the spatial localization of angiogenic signals in the extracellular matrix (ECM) is crucial to ensure the proper assembly and maturation of new vascular structures. Here, we discuss the therapeutic implications of matrix interactions of angiogenic factors, with a special emphasis on VEGF, as well as provide an overview of current approaches, based on protein and biomaterial engineering that mimic the regulatory functions of ECM to optimize the signaling microenvironment of vascular growth factors.

Authors:
 [1];  [2];  [2];  [2];  [3];  [2];  [3];  [4];  [4];  [2];  [5];  [2]
  1. Osaka Univ., Osaka (Japan)
  2. Basel Univ., Basel (Switzerland); Basel Univ. Hospital, Basel (Switzerland)
  3. Basel Univ. Hospital, Basel (Switzerland)
  4. Ecole Polytechnique Federale de Lausanne (EPFL), Lausanne (Switzerland)
  5. Ecole Polytechnique Federale de Lausanne (EPFL), Lausanne (Switzerland); Univ. of Chicago, Chicago, IL (United States); Argonne National Lab., Argonne, IL (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1225190
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Bioengineering and Biotechnology
Additional Journal Information:
Journal Volume: 3; Journal Issue: 3; Journal ID: ISSN 2296-4185
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; angiogenesis; growth factors; extracellular matrix; fibrin; protein engineering

Citation Formats

Martino, Mikael M., Brkic, Sime, Bovo, Emmanuela, Burger, Maximilian, Schaefer, Dirk J., Wolff, Thomas, Gurke, Lorenz, Briquez, Priscilla S., Larsson, Hans M., Gianni-Barrera, Roberto, Hubbell, Jeffrey A., and Banfi, Andrea. Extracellular matrix and growth factor engineering for controlled angiogenesis in regenerative medicine. United States: N. p., 2015. Web. doi:10.3389/fbioe.2015.00045.
Martino, Mikael M., Brkic, Sime, Bovo, Emmanuela, Burger, Maximilian, Schaefer, Dirk J., Wolff, Thomas, Gurke, Lorenz, Briquez, Priscilla S., Larsson, Hans M., Gianni-Barrera, Roberto, Hubbell, Jeffrey A., & Banfi, Andrea. Extracellular matrix and growth factor engineering for controlled angiogenesis in regenerative medicine. United States. https://doi.org/10.3389/fbioe.2015.00045
Martino, Mikael M., Brkic, Sime, Bovo, Emmanuela, Burger, Maximilian, Schaefer, Dirk J., Wolff, Thomas, Gurke, Lorenz, Briquez, Priscilla S., Larsson, Hans M., Gianni-Barrera, Roberto, Hubbell, Jeffrey A., and Banfi, Andrea. Wed . "Extracellular matrix and growth factor engineering for controlled angiogenesis in regenerative medicine". United States. https://doi.org/10.3389/fbioe.2015.00045. https://www.osti.gov/servlets/purl/1225190.
@article{osti_1225190,
title = {Extracellular matrix and growth factor engineering for controlled angiogenesis in regenerative medicine},
author = {Martino, Mikael M. and Brkic, Sime and Bovo, Emmanuela and Burger, Maximilian and Schaefer, Dirk J. and Wolff, Thomas and Gurke, Lorenz and Briquez, Priscilla S. and Larsson, Hans M. and Gianni-Barrera, Roberto and Hubbell, Jeffrey A. and Banfi, Andrea},
abstractNote = {In this study, blood vessel growth plays a key role in regenerative medicine, both to restore blood supply to ischemic tissues and to ensure rapid vascularization of clinical-size tissue-engineered grafts. For example, vascular endothelial growth factor (VEGF) is the master regulator of physiological blood vessel growth and is one of the main molecular targets of therapeutic angiogenesis approaches. However, angiogenesis is a complex process and there is a need to develop rational therapeutic strategies based on a firm understanding of basic vascular biology principles, as evidenced by the disappointing results of initial clinical trials of angiogenic factor delivery. In particular, the spatial localization of angiogenic signals in the extracellular matrix (ECM) is crucial to ensure the proper assembly and maturation of new vascular structures. Here, we discuss the therapeutic implications of matrix interactions of angiogenic factors, with a special emphasis on VEGF, as well as provide an overview of current approaches, based on protein and biomaterial engineering that mimic the regulatory functions of ECM to optimize the signaling microenvironment of vascular growth factors.},
doi = {10.3389/fbioe.2015.00045},
journal = {Frontiers in Bioengineering and Biotechnology},
number = 3,
volume = 3,
place = {United States},
year = {Wed Apr 01 00:00:00 EDT 2015},
month = {Wed Apr 01 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 127 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Tenascin C Promiscuously Binds Growth Factors via Its Fifth Fibronectin Type III-Like Domain
journal, April 2013


Induction of Aberrant Vascular Growth, But Not of Normal Angiogenesis, by Cell-Based Expression of Different Doses of Human and Mouse VEGF Is Species-Dependent
journal, February 2013

  • Mujagic, Edin; Gianni-Barrera, Roberto; Trani, Marianna
  • Human Gene Therapy Methods, Vol. 24, Issue 1
  • DOI: 10.1089/hgtb.2012.197

Update on therapeutic vascularization strategies
journal, January 2009


VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia
journal, June 2003

  • Gerhardt, Holger; Golding, Matthew; Fruttiger, Marcus
  • The Journal of Cell Biology, Vol. 161, Issue 6
  • DOI: 10.1083/jcb.200302047

Gene Therapy for Ischemic Cardiovascular Diseases: Some Lessons Learned from the First Clinical Trials
journal, November 2004

  • Ylä-Herttuala, Seppo; Markkanen, Johanna E.; Rissanen, Tuomas T.
  • Trends in Cardiovascular Medicine, Vol. 14, Issue 8
  • DOI: 10.1016/j.tcm.2004.09.001

Polymers for pro- and anti-angiogenic therapy
journal, April 2007


Growth factor delivery-based tissue engineering: general approaches and a review of recent developments
journal, June 2010

  • Lee, Kangwon; Silva, Eduardo A.; Mooney, David J.
  • Journal of The Royal Society Interface, Vol. 8, Issue 55
  • DOI: 10.1098/rsif.2010.0223

The shunt problem: control of functional shunting in normal and tumour vasculature
journal, July 2010

  • Pries, Axel R.; Höpfner, Michael; le Noble, Ferdinand
  • Nature Reviews Cancer, Vol. 10, Issue 8
  • DOI: 10.1038/nrc2895

The role of actively released fibrin-conjugated VEGF for VEGF receptor 2 gene activation and the enhancement of angiogenesis
journal, April 2008


Therapeutic angiogenesis for critical limb ischaemia
journal, May 2013


Strategic Directions in Tissue Engineering
journal, December 2007

  • Johnson, Peter C.; Mikos, Antonios G.; Fisher, John P.
  • Tissue Engineering, Vol. 13, Issue 12
  • DOI: 10.1089/ten.2007.0335

The well-tempered vessel
journal, May 2001

  • Blau, Helen M.; Banfi, Andrea
  • Nature Medicine, Vol. 7, Issue 5
  • DOI: 10.1038/87850

FACS-purified myoblasts producing controlled VEGF levels induce safe and stable angiogenesis in chronic hind limb ischemia
journal, December 2011


VEGF gene therapy: stimulating angiogenesis or angioma-genesis?
journal, October 2000

  • Carmeliet, Peter
  • Nature Medicine, Vol. 6, Issue 10
  • DOI: 10.1038/80430

Increased angiogenesis and blood vessel maturation in acellular collagen–heparin scaffolds containing both FGF2 and VEGF
journal, February 2007


Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction
journal, July 2007


Critical role of microenvironmental factors in angiogenesis
journal, May 2005

  • Banfi, Andrea; von Degenfeld, Georges; Blau, Helen M.
  • Current Atherosclerosis Reports, Vol. 7, Issue 3
  • DOI: 10.1007/s11883-005-0011-7

Adipose tissue-derived progenitors for engineering osteogenic and vasculogenic grafts
journal, July 2010

  • Scherberich, Arnaud; Müller, Andreas M.; Schäfer, Dirk J.
  • Journal of Cellular Physiology, Vol. 225, Issue 2
  • DOI: 10.1002/jcp.22313

The Extracellular Matrix: Not Just Pretty Fibrils
journal, November 2009


Vascularization in Tissue Engineering
book, October 2020


Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II)
journal, January 2007


Growth factor binding to the pericellular matrix and its importance in tissue engineering☆
journal, November 2007


The 12th–14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain
journal, December 2010

  • Martino, Mikaël M.; Hubbell, Jeffrey A.
  • The FASEB Journal, Vol. 24, Issue 12
  • DOI: 10.1096/fj.09-151282

Cell-Demanded Liberation of VEGF 121 From Fibrin Implants Induces Local and Controlled Blood Vessel Growth
journal, April 2004


The 12th–14th type III repeats of fibronectin function as a highly promiscuous growth factor‐binding domain
journal, July 2010

  • Martino, Mikaël M.; Hubbell, Jeffrey A.
  • The FASEB Journal, Vol. 24, Issue 12
  • DOI: 10.1096/fj.09.151282

New aspects in vascular gene therapy
journal, April 2010


Basic and Therapeutic Aspects of Angiogenesis
journal, September 2011


Vascularization in tissue engineering
journal, August 2008

  • Rouwkema, Jeroen; Rivron, Nicolas C.; van Blitterswijk, Clemens A.
  • Trends in Biotechnology, Vol. 26, Issue 8
  • DOI: 10.1016/j.tibtech.2008.04.009

Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering
text, January 2007


Long-lasting fibrin matrices ensure stable and functional angiogenesis by highly tunable, sustained delivery of recombinant VEGF164
journal, April 2014

  • Sacchi, V.; Mittermayr, R.; Hartinger, J.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 19
  • DOI: 10.1073/pnas.1404605111

Integrin regulation of growth factor receptors
journal, April 2002

  • Yamada, Kenneth M.; Even-Ram, Sharona
  • Nature Cell Biology, Vol. 4, Issue 4
  • DOI: 10.1038/ncb0402-e75

Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor
journal, February 2011

  • Kim, Soo-Hyun; Turnbull, Jeremy; Guimond, Scott
  • Journal of Endocrinology, Vol. 209, Issue 2
  • DOI: 10.1530/JOE-10-0377

VEGF Gene Delivery to Muscle
journal, November 1998


Long-lasting fibrin matrices ensure stable and functional angiogenesis by highly tunable, sustained delivery of recombinant VEGF164
text, January 2014

  • Sacchi, Veronica; Mittermayr, Rainer; Hartinger, Joachim
  • National Academy of Sciences
  • DOI: 10.5167/uzh-96009

Inducible adeno-associated virus vectors promote functional angiogenesis in adult organisms via regulated vascular endothelial growth factor expression
journal, May 2009

  • Tafuro, Sabrina; Ayuso, Eduard; Zacchigna, Serena
  • Cardiovascular Research, Vol. 83, Issue 4
  • DOI: 10.1093/cvr/cvp152

Long-lasting fibrin matrices ensure stable and functional angiogenesis by highly tunable, sustained delivery of recombinant VEGF164
text, January 2014

  • Sacchi, Veronica; Mittermayr, Rainer; Hartinger, Joachim
  • National Academy of Sciences
  • DOI: 10.5451/unibas-ep61122

Controlled Angiogenesis in the Heart by Cell-Based Expression of Specific Vascular Endothelial Growth Factor Levels
journal, October 2012

  • Melly, Ludovic F.; Marsano, Anna; Frobert, Aurelien
  • Human Gene Therapy Methods, Vol. 23, Issue 5
  • DOI: 10.1089/hgtb.2012.032

Microenvironmental VEGF distribution is critical for stable and functional vessel growth in ischemia
journal, December 2006

  • von Degenfeld, Georges; Banfi, Andrea; Springer, Matthew L.
  • The FASEB Journal, Vol. 20, Issue 14
  • DOI: 10.1096/fj.06-6568fje

Enhancing microvascular formation and vessel maturation through temporal control over multiple pro-angiogenic and pro-maturation factors
journal, December 2013


Heart Disease and Stroke Statistics—2013 Update: A Report From the American Heart Association
journal, January 2013


Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix
journal, March 2013

  • Martino, M. M.; Briquez, P. S.; Ranga, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 12
  • DOI: 10.1073/pnas.1221602110

Polymeric system for dual growth factor delivery
journal, November 2001

  • Richardson, Thomas P.; Peters, Martin C.; Ennett, Alessandra B.
  • Nature Biotechnology, Vol. 19, Issue 11, p. 1029-1034
  • DOI: 10.1038/nbt1101-1029

Therapeutic angiogenesis due to balanced single-vector delivery of VEGF and PDGF-BB
journal, June 2012

  • Banfi, Andrea; von Degenfeld, Georges; Gianni-Barrera, Roberto
  • The FASEB Journal, Vol. 26, Issue 6
  • DOI: 10.1096/fj.11-197400

Specific VEGF sequestering and release using peptide-functionalized hydrogel microspheres
journal, April 2012


Extracellular Matrix and Cytokines: A Functional Unit
journal, January 2000

  • Schönherr, Elke; Hausser, Heinz-JüRgen
  • Developmental Immunology, Vol. 7, Issue 2-4
  • DOI: 10.1155/2000/31748

Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering
journal, September 2007


Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis
journal, February 2004

  • Ozawa, Clare R.; Banfi, Andrea; Glazer, Nicole L.
  • Journal of Clinical Investigation, Vol. 113, Issue 4
  • DOI: 10.1172/jci200418420

Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors
journal, December 2009

  • Borselli, Cristina; Storrie, Hannah; Benesch-Lee, Frank
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 8
  • DOI: 10.1073/pnas.0903875106

Engineering the Growth Factor Microenvironment with Fibronectin Domains to Promote Wound and Bone Tissue Healing
journal, September 2011


Agent-based simulation of notch-mediated tip cell selection in angiogenic sprout initialisation
journal, January 2008

  • Bentley, Katie; Gerhardt, Holger; Bates, Paul A.
  • Journal of Theoretical Biology, Vol. 250, Issue 1
  • DOI: 10.1016/j.jtbi.2007.09.015

Positional Control of Cell Fate Through Joint Integrin/Receptor Protein Kinase Signaling
journal, November 2003


Vasculogenic bio-synthetic hydrogel for enhancement of pancreatic islet engraftment and function in type 1 diabetes
journal, June 2013


Heterogeneity of the Angiogenic Response Induced in Different Normal Adult Tissues by Vascular Permeability Factor/Vascular Endothelial Growth Factor
journal, January 2000

  • Pettersson, Anna; Nagy, Janice A.; Brown, Lawrence F.
  • Laboratory Investigation, Vol. 80, Issue 1
  • DOI: 10.1038/labinvest.3780013

Cell-demanded release of VEGF from synthetic, biointeractive cell ingrowth matrices for vascularized tissue growth
journal, December 2003

  • Zisch, Andreas H.; Lutolf, Matthias P.; Ehrbar, Martin
  • The FASEB Journal, Vol. 17, Issue 15
  • DOI: 10.1096/fj.02-1041fje

Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall
journal, August 2003


Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy.
text, January 2002

  • Dor, Yuval; Djonov, Valentin Georgiev; Abramovitch, Rinat
  • EMBO Press
  • DOI: 10.48350/149304

VEGF gene therapy: therapeutic angiogenesis in the clinic and beyond
journal, March 2012


Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele
journal, April 1996

  • Carmeliet, Peter; Ferreira, Valérie; Breier, Georg
  • Nature, Vol. 380, Issue 6573
  • DOI: 10.1038/380435a0

Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis
journal, January 2007

  • Hellström, Mats; Phng, Li-Kun; Hofmann, Jennifer J.
  • Nature, Vol. 445, Issue 7129
  • DOI: 10.1038/nature05571

Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene
journal, April 1996

  • Ferrara, Napoleone; Carver-Moore, Karen; Chen, Helen
  • Nature, Vol. 380, Issue 6573
  • DOI: 10.1038/380439a0

Growth Factors Engineered for Super-Affinity to the Extracellular Matrix Enhance Tissue Healing
journal, February 2014


Therapeutic angiogenesis: controlled delivery of angiogenic factors
journal, June 2012

  • Chu, Hunghao; Wang, Yadong
  • Therapeutic Delivery, Vol. 3, Issue 6
  • DOI: 10.4155/tde.12.50

Vitronectin: Growth Factor Complexes Hold Potential as a Wound Therapy Approach
journal, June 2008

  • Upton, Zee; Cuttle, Leila; Noble, Anthony
  • Journal of Investigative Dermatology, Vol. 128, Issue 6
  • DOI: 10.1038/sj.jid.5701148

Long-term VEGF-A expression promotes aberrant angiogenesis and fibrosis in skeletal muscle
journal, May 2011

  • Karvinen, H.; Pasanen, E.; Rissanen, T. T.
  • Gene Therapy, Vol. 18, Issue 12
  • DOI: 10.1038/gt.2011.66

The promotion of endothelial cell attachment and spreading using FNIII10 fused to VEGF-A165
journal, August 2013


Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression
journal, September 2000


Critical role of microenvironmental factors in angiogenesis
journal, May 2005

  • Banfi, Andrea; von Degenfeld, Georges; Blau, Helen M.
  • Current Atherosclerosis Reports, Vol. 7, Issue 3
  • DOI: 10.1007/s11883-005-0011-7

Growth factor binding to the pericellular matrix and its importance in tissue engineering☆
journal, November 2007


Increased angiogenesis and blood vessel maturation in acellular collagen–heparin scaffolds containing both FGF2 and VEGF
journal, February 2007


Polymers for pro- and anti-angiogenic therapy
journal, April 2007


Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering
journal, September 2007


Specific VEGF sequestering and release using peptide-functionalized hydrogel microspheres
journal, April 2012


Vasculogenic bio-synthetic hydrogel for enhancement of pancreatic islet engraftment and function in type 1 diabetes
journal, June 2013


The promotion of endothelial cell attachment and spreading using FNIII10 fused to VEGF-A165
journal, August 2013


Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction
journal, July 2007


Basic and Therapeutic Aspects of Angiogenesis
journal, September 2011


New aspects in vascular gene therapy
journal, April 2010


Agent-based simulation of notch-mediated tip cell selection in angiogenic sprout initialisation
journal, January 2008

  • Bentley, Katie; Gerhardt, Holger; Bates, Paul A.
  • Journal of Theoretical Biology, Vol. 250, Issue 1
  • DOI: 10.1016/j.jtbi.2007.09.015

Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II)
journal, January 2007


Gene Therapy for Ischemic Cardiovascular Diseases: Some Lessons Learned from the First Clinical Trials
journal, November 2004

  • Ylä-Herttuala, Seppo; Markkanen, Johanna E.; Rissanen, Tuomas T.
  • Trends in Cardiovascular Medicine, Vol. 14, Issue 8
  • DOI: 10.1016/j.tcm.2004.09.001

Vascularization in tissue engineering
journal, August 2008

  • Rouwkema, Jeroen; Rivron, Nicolas C.; van Blitterswijk, Clemens A.
  • Trends in Biotechnology, Vol. 26, Issue 8
  • DOI: 10.1016/j.tibtech.2008.04.009

Glomeruloid Microvascular Proliferation Follows Adenoviral Vascular Permeability Factor/Vascular Endothelial Growth Factor-164 Gene Delivery
journal, March 2001

  • Sundberg, Christian; Nagy, Janice A.; Brown, Lawrence F.
  • The American Journal of Pathology, Vol. 158, Issue 3
  • DOI: 10.1016/s0002-9440(10)64062-x

Clinical evidence of angiogenesis after arterial gene transfer of phVEGF165 in patient with ischaemic limb
journal, August 1996


Interactions between growth factor receptors and adhesion molecules: breaking the rules
journal, October 2003


Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene
journal, April 1996

  • Ferrara, Napoleone; Carver-Moore, Karen; Chen, Helen
  • Nature, Vol. 380, Issue 6573
  • DOI: 10.1038/380439a0

VEGF gene therapy: stimulating angiogenesis or angioma-genesis?
journal, October 2000

  • Carmeliet, Peter
  • Nature Medicine, Vol. 6, Issue 10
  • DOI: 10.1038/80430

The well-tempered vessel
journal, May 2001

  • Blau, Helen M.; Banfi, Andrea
  • Nature Medicine, Vol. 7, Issue 5
  • DOI: 10.1038/87850

Long-term VEGF-A expression promotes aberrant angiogenesis and fibrosis in skeletal muscle
journal, May 2011

  • Karvinen, H.; Pasanen, E.; Rissanen, T. T.
  • Gene Therapy, Vol. 18, Issue 12
  • DOI: 10.1038/gt.2011.66

VEGF gene therapy: therapeutic angiogenesis in the clinic and beyond
journal, March 2012


Heterogeneity of the Angiogenic Response Induced in Different Normal Adult Tissues by Vascular Permeability Factor/Vascular Endothelial Growth Factor
journal, January 2000

  • Pettersson, Anna; Nagy, Janice A.; Brown, Lawrence F.
  • Laboratory Investigation, Vol. 80, Issue 1
  • DOI: 10.1038/labinvest.3780013

Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis
journal, January 2007

  • Hellström, Mats; Phng, Li-Kun; Hofmann, Jennifer J.
  • Nature, Vol. 445, Issue 7129
  • DOI: 10.1038/nature05571

Integrin regulation of growth factor receptors
journal, April 2002

  • Yamada, Kenneth M.; Even-Ram, Sharona
  • Nature Cell Biology, Vol. 4, Issue 4
  • DOI: 10.1038/ncb0402-e75

The shunt problem: control of functional shunting in normal and tumour vasculature
journal, July 2010

  • Pries, Axel R.; Höpfner, Michael; le Noble, Ferdinand
  • Nature Reviews Cancer, Vol. 10, Issue 8
  • DOI: 10.1038/nrc2895

Therapeutic angiogenesis for critical limb ischaemia
journal, May 2013


Vitronectin: Growth Factor Complexes Hold Potential as a Wound Therapy Approach
journal, June 2008

  • Upton, Zee; Cuttle, Leila; Noble, Anthony
  • Journal of Investigative Dermatology, Vol. 128, Issue 6
  • DOI: 10.1038/sj.jid.5701148

Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors
journal, December 2009

  • Borselli, Cristina; Storrie, Hannah; Benesch-Lee, Frank
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 8
  • DOI: 10.1073/pnas.0903875106

Heparin-binding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix
journal, March 2013

  • Martino, M. M.; Briquez, P. S.; Ranga, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 12
  • DOI: 10.1073/pnas.1221602110

Induction of Aberrant Vascular Growth, But Not of Normal Angiogenesis, by Cell-Based Expression of Different Doses of Human and Mouse VEGF Is Species-Dependent
journal, February 2013

  • Mujagic, Edin; Gianni-Barrera, Roberto; Trani, Marianna
  • Human Gene Therapy Methods, Vol. 24, Issue 1
  • DOI: 10.1089/hgtb.2012.197

Strategic Directions in Tissue Engineering
journal, December 2007

  • Johnson, Peter C.; Mikos, Antonios G.; Fisher, John P.
  • Tissue Engineering, Vol. 13, Issue 12
  • DOI: 10.1089/ten.2007.0335

Local Delivery of VEGF and SDF Enhances Endothelial Progenitor Cell Recruitment and Resultant Recovery from Ischemia
journal, April 2015

  • Anderson, Erin M.; Kwee, Brian J.; Lewin, Sarah A.
  • Tissue Engineering Part A, Vol. 21, Issue 7-8
  • DOI: 10.1089/ten.tea.2014.0508

Inducible adeno-associated virus vectors promote functional angiogenesis in adult organisms via regulated vascular endothelial growth factor expression
journal, May 2009

  • Tafuro, Sabrina; Ayuso, Eduard; Zacchigna, Serena
  • Cardiovascular Research, Vol. 83, Issue 4
  • DOI: 10.1093/cvr/cvp152

Cell-demanded release of VEGF from synthetic, biointeractive cell ingrowth matrices for vascularized tissue growth
journal, December 2003

  • Zisch, Andreas H.; Lutolf, Matthias P.; Ehrbar, Martin
  • The FASEB Journal, Vol. 17, Issue 15
  • DOI: 10.1096/fj.02-1041fje

Microenvironmental VEGF distribution is critical for stable and functional vessel growth in ischemia
journal, December 2006

  • von Degenfeld, Georges; Banfi, Andrea; Springer, Matthew L.
  • The FASEB Journal, Vol. 20, Issue 14
  • DOI: 10.1096/fj.06-6568fje

The 12th–14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain
journal, December 2010

  • Martino, Mikaël M.; Hubbell, Jeffrey A.
  • The FASEB Journal, Vol. 24, Issue 12
  • DOI: 10.1096/fj.09-151282

Therapeutic angiogenesis due to balanced single-vector delivery of VEGF and PDGF-BB
journal, June 2012

  • Banfi, Andrea; von Degenfeld, Georges; Gianni-Barrera, Roberto
  • The FASEB Journal, Vol. 26, Issue 6
  • DOI: 10.1096/fj.11-197400

Growth factor delivery-based tissue engineering: general approaches and a review of recent developments
journal, June 2010

  • Lee, Kangwon; Silva, Eduardo A.; Mooney, David J.
  • Journal of The Royal Society Interface, Vol. 8, Issue 55
  • DOI: 10.1098/rsif.2010.0223

Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall
journal, August 2003


Release of basic fibroblast growth factor from a crosslinked glycosaminoglycan hydrogel promotes wound healing
journal, March 2007


Interactions between extracellular matrix and growth factors in wound healing
journal, March 2009


The Extracellular Matrix: Not Just Pretty Fibrils
journal, November 2009


Growth Factors Engineered for Super-Affinity to the Extracellular Matrix Enhance Tissue Healing
journal, February 2014


Positional Control of Cell Fate Through Joint Integrin/Receptor Protein Kinase Signaling
journal, November 2003


Extracellular Matrix and Cytokines: A Functional Unit
journal, January 2000

  • Schönherr, Elke; Hausser, Heinz-JüRgen
  • Developmental Immunology, Vol. 7, Issue 2-4
  • DOI: 10.1155/2000/31748

VEGF Gene Delivery to Myocardium: Deleterious Effects of Unregulated Expression
journal, August 2000

  • Lee, Randall J.; Springer, Matthew L.; Blanco-Bose, William E.
  • Circulation, Vol. 102, Issue 8
  • DOI: 10.1161/01.cir.102.8.898

Human Studies of Angiogenic Gene Therapy
journal, October 2009


The “Heart Disease and Stroke Statistics—2013 Update” and the Need for a National Cardiovascular Surveillance System
journal, January 2013


Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis
journal, February 2004

  • Ozawa, Clare R.; Banfi, Andrea; Glazer, Nicole L.
  • Journal of Clinical Investigation, Vol. 113, Issue 4
  • DOI: 10.1172/jci18420

Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression
journal, September 2000


Tenascin C Promiscuously Binds Growth Factors via Its Fifth Fibronectin Type III-Like Domain
journal, April 2013


Update on therapeutic vascularization strategies
journal, January 2009


Long-lasting fibrin matrices ensure stable and functional angiogenesis by highly tunable, sustained delivery of recombinant VEGF164
text, January 2014

  • Sacchi, Veronica; Mittermayr, Rainer; Hartinger, Joachim
  • National Academy of Sciences
  • DOI: 10.5451/unibas-ep61122

Works referencing / citing this record:

3D Cardiac Cell Culture: A Critical Review of Current Technologies and Applications
journal, June 2019


Therapeutic vascularization in regenerative medicine
journal, April 2020

  • Gianni‐Barrera, Roberto; Di Maggio, Nunzia; Melly, Ludovic
  • STEM CELLS Translational Medicine, Vol. 9, Issue 4
  • DOI: 10.1002/sctm.19-0319

TGF-β1/CD105 signaling controls vascular network formation within growth factor sequestering hyaluronic acid hydrogels
journal, March 2018


It Takes Two to Tang: Coupling of Angiogenesis and Osteogenesis for Bone Regeneration
text, January 2017


EphrinB2/EphB4 signaling regulates non-sprouting angiogenesis by VEGF
text, January 2018


4D Biomaterials for Light‐Guided Angiogenesis
collection, January 2018

  • Farrukh, Aleeza; Paez, Julieta I.; Del Campo Bécares, Aránzazu
  • Universität des Saarlandes
  • DOI: 10.22028/d291-29506

Rational Design of Prevascularized Large 3D Tissue Constructs Using Computational Simulations and Biofabrication of Geometrically Controlled Microvessels
journal, May 2016

  • Arrigoni, Chiara; Bongio, Matilde; Talò, Giuseppe
  • Advanced Healthcare Materials, Vol. 5, Issue 13
  • DOI: 10.1002/adhm.201500958

A sulfonated reversible thermal gel for the spatiotemporal control of VEGF delivery to promote therapeutic angiogenesis: Sulfonated reversible thermal gel for control of VEGF delivery
journal, September 2018

  • Lee, David J.; Rocker, Adam J.; Bardill, James R.
  • Journal of Biomedical Materials Research Part A, Vol. 106, Issue 12
  • DOI: 10.1002/jbm.a.36496

In vitro selection technologies to enhance biomaterial functionality
journal, May 2016

  • Rosch, Jonah C.; Hollmann, Emma K.; Lippmann, Ethan S.
  • Experimental Biology and Medicine, Vol. 241, Issue 9
  • DOI: 10.1177/1535370216647182

Cellularizing hydrogel-based scaffolds to repair bone tissue: How to create a physiologically relevant micro-environment?
journal, December 2016

  • Maisani, Mathieu; Pezzoli, Daniele; Chassande, Olivier
  • Journal of Tissue Engineering, Vol. 8
  • DOI: 10.1177/2041731417712073

Biofabrication strategies for creating microvascular complexity
journal, April 2019

  • Morss Clyne, Alisa; Swaminathan, Swathi; Díaz Lantada, Andrés
  • Biofabrication, Vol. 11, Issue 3
  • DOI: 10.1088/1758-5090/ab0621

Tethering QK peptide to enhance angiogenesis in elastin-like recombinamer (ELR) hydrogels
journal, February 2019

  • Flora, Tatjana; de Torre, I. González; Alonso, M.
  • Journal of Materials Science: Materials in Medicine, Vol. 30, Issue 2
  • DOI: 10.1007/s10856-019-6232-z

State-of-the-Art Strategies for the Vascularization of Three-Dimensional Engineered Organs
journal, June 2019

  • Min, Sangil; Ko, In Kap; Yoo, James J.
  • Vascular Specialist International, Vol. 35, Issue 2
  • DOI: 10.5758/vsi.2019.35.2.77

Design principles for therapeutic angiogenic materials
journal, January 2016

  • Briquez, Priscilla S.; Clegg, Lindsay E.; Martino, Mikaël M.
  • Nature Reviews Materials, Vol. 1, Issue 1
  • DOI: 10.1038/natrevmats.2015.6

Cultured cell‐derived extracellular matrices to enhance the osteogenic differentiation and angiogenic properties of human mesenchymal stem/stromal cells
journal, July 2019

  • Carvalho, Marta S.; Silva, João C.; Cabral, Joaquim M. S.
  • Journal of Tissue Engineering and Regenerative Medicine, Vol. 13, Issue 9
  • DOI: 10.1002/term.2907

EphrinB2/EphB4 signaling regulates non‐sprouting angiogenesis by VEGF
journal, April 2018


Prevascularized bladder acellular matrix hydrogel/silk fibroin composite scaffolds promote the regeneration of urethra in a rabbit model
journal, October 2018


It Takes Two to Tango: Coupling of Angiogenesis and Osteogenesis for Bone Regeneration
journal, November 2017

  • Grosso, Andrea; Burger, Maximilian G.; Lunger, Alexander
  • Frontiers in Bioengineering and Biotechnology, Vol. 5
  • DOI: 10.3389/fbioe.2017.00068

Angiogenesis-promoted bone repair with silicate-shelled hydrogel fiber scaffolds
journal, January 2019

  • Dashnyam, Khandmaa; Buitrago, Jennifer O.; Bold, Tsendmaa
  • Biomaterials Science, Vol. 7, Issue 12
  • DOI: 10.1039/c9bm01103j

Growth factors with enhanced syndecan binding generate tonic signalling and promote tissue healing
journal, November 2019

  • Mochizuki, Mayumi; Güç, Esra; Park, Anthony J.
  • Nature Biomedical Engineering, Vol. 4, Issue 4
  • DOI: 10.1038/s41551-019-0469-1

Halfway between 2D and Animal Models: Are 3D Cultures the Ideal Tool to Study Cancer-Microenvironment Interactions?
journal, January 2018

  • Hoarau-Véchot, Jessica; Rafii, Arash; Touboul, Cyril
  • International Journal of Molecular Sciences, Vol. 19, Issue 1
  • DOI: 10.3390/ijms19010181

Mechanical Interaction Between Cells Facilitates Molecular Transport
text, January 2019


Mechanical Interaction between Cells Facilitates Molecular Transport
journal, November 2019


Gellan Gum Hydrogels with Enzyme-Sensitive Biodegradation and Endothelial Cell Biorecognition Sites
journal, February 2018

  • da Silva, Lucília P.; Jha, Amit K.; Correlo, Vitor M.
  • Advanced Healthcare Materials, Vol. 7, Issue 5
  • DOI: 10.1002/adhm.201700686

4D Biomaterials for Light‐Guided Angiogenesis
journal, December 2018

  • Farrukh, Aleeza; Paez, Julieta I.; del Campo, Aránzazu
  • Advanced Functional Materials, Vol. 29, Issue 6
  • DOI: 10.1002/adfm.201807734

Cellularizing hydrogel-based scaffolds to repair bone tissue: How to create a physiologically relevant micro-environment?
journal, December 2016

  • Maisani, Mathieu; Pezzoli, Daniele; Chassande, Olivier
  • Journal of Tissue Engineering, Vol. 8
  • DOI: 10.1177/2041731417712073

TGF-β1/CD105 signaling controls vascular network formation within growth factor sequestering hyaluronic acid hydrogels
journal, March 2018


EphrinB2/EphB4 signaling regulates non‐sprouting angiogenesis by VEGF
journal, April 2018


Learning from Mother Nature: Innovative Tools to Boost Endogenous Repair of Critical or Difficult-to-Heal Large Tissue Defects
journal, April 2017

  • Cancedda, Ranieri; Bollini, Sveva; Descalzi, Fiorella
  • Frontiers in Bioengineering and Biotechnology, Vol. 5
  • DOI: 10.3389/fbioe.2017.00028

Halfway between 2D and Animal Models: Are 3D Cultures the Ideal Tool to Study Cancer-Microenvironment Interactions?
journal, January 2018

  • Hoarau-Véchot, Jessica; Rafii, Arash; Touboul, Cyril
  • International Journal of Molecular Sciences, Vol. 19, Issue 1
  • DOI: 10.3390/ijms19010181

State-of-the-Art Strategies for the Vascularization of Three-Dimensional Engineered Organs
journal, June 2019

  • Min, Sangil; Ko, In Kap; Yoo, James J.
  • Vascular Specialist International, Vol. 35, Issue 2
  • DOI: 10.5758/vsi.2019.35.2.77

Preparation and characteristics of gelatin sponges crosslinked by microbial transglutaminase
journal, August 2017