Consensus guidelines for the use and interpretation of angiogenesis assays

Patrycja Nowak-Sliwinska; Kari Alitalo; Elizabeth Allen; Andrey Anisimov; Alfred C. Aplin; Robert Auerbach; Hellmut G. Augustin; David O. Bates; Judy R. van Beijnum; R. Hugh F. Bender; Gabriele Bergers; Andreas Bikfalvi; Joyce Bischoff; Barbara C. Böck; Peter C. Brooks; Federico Bussolino; Bertan Cakir; Peter Carmeliet; Daniel Castranova; Anca M. Cimpean; Ondine Cleaver; George Coukos; George E. Davis; Michele De Palma; Anna Dimberg; Ruud P.M. Dings; Valentin Djonov; Andrew C. Dudley; Neil P. Dufton; Sarah Maria Fendt; Napoleone Ferrara; Marcus Fruttiger; Dai Fukumura; Bart Ghesquière; Yan Gong; Robert J. Griffin; Adrian L. Harris; Christopher C.W. Hughes; Nan W. Hultgren; M. Luisa Iruela-Arispe; Melita Irving; Rakesh K. Jain; Raghu Kalluri; Joanna Kalucka; Robert S. Kerbel; Jan Kitajewski; Ingeborg Klaassen; Hynda K. Kleinmann; Pieter Koolwijk; Elisabeth Kuczynski; Brenda R. Kwak; Koen Marien; Juan M. Melero-Martin; Lance L. Munn; Roberto F. Nicosia; Agnes Noel; Jussi Nurro; Anna Karin Olsson; Tatiana V. Petrova; Kristian Pietras; Roberto Pili; Jeffrey W. Pollard; Mark J. Post; Paul H.A. Quax; Gabriel A. Rabinovich; Marius Raica; Anna M. Randi; Domenico Ribatti; Curzio Ruegg; Reinier O. Schlingemann; Stefan Schulte-Merker; Lois E.H. Smith; Jonathan W. Song; Steven A. Stacker; Jimmy Stalin; Amber N. Stratman; Maureen Van de Velde; Victor W.M. van Hinsbergh; Peter B. Vermeulen; Johannes Waltenberger; Brant M. Weinstein; Hong Xin; Bahar Yetkin-Arik; Seppo Yla-Herttuala; Mervin C. Yoder; Arjan W. Griffioen

doi:10.1007/s10456-018-9613-x

Consensus guidelines for the use and interpretation of angiogenesis assays

Patrycja Nowak-Sliwinska, Kari Alitalo, Elizabeth Allen, Andrey Anisimov, Alfred C. Aplin, Robert Auerbach, Hellmut G. Augustin, David O. Bates, Judy R. van Beijnum, R. Hugh F. Bender, Gabriele Bergers, Andreas Bikfalvi, Joyce Bischoff, Barbara C. Böck, Peter C. Brooks, Federico Bussolino, Bertan Cakir, Peter Carmeliet, Daniel Castranova, Anca M. CimpeanOndine Cleaver, George Coukos, George E. Davis, Michele De Palma, Anna Dimberg, Ruud P.M. Dings, Valentin Djonov, Andrew C. Dudley, Neil P. Dufton, Sarah Maria Fendt, Napoleone Ferrara, Marcus Fruttiger, Dai Fukumura, Bart Ghesquière, Yan Gong, Robert J. Griffin, Adrian L. Harris, Christopher C.W. Hughes, Nan W. Hultgren, M. Luisa Iruela-Arispe, Melita Irving, Rakesh K. Jain, Raghu Kalluri, Joanna Kalucka, Robert S. Kerbel, Jan Kitajewski, Ingeborg Klaassen, Hynda K. Kleinmann, Pieter Koolwijk, Elisabeth Kuczynski, Brenda R. Kwak, Koen Marien, Juan M. Melero-Martin, Lance L. Munn, Roberto F. Nicosia, Agnes Noel, Jussi Nurro, Anna Karin Olsson, Tatiana V. Petrova, Kristian Pietras, Roberto Pili, Jeffrey W. Pollard, Mark J. Post, Paul H.A. Quax, Gabriel A. Rabinovich, Marius Raica, Anna M. Randi, Domenico Ribatti, Curzio Ruegg, Reinier O. Schlingemann, Stefan Schulte-Merker, Lois E.H. Smith, Jonathan W. Song, Steven A. Stacker, Jimmy Stalin, Amber N. Stratman, Maureen Van de Velde, Victor W.M. van Hinsbergh, Peter B. Vermeulen, Johannes Waltenberger, Brant M. Weinstein, Hong Xin, Bahar Yetkin-Arik, Seppo Yla-Herttuala, Mervin C. Yoder, Arjan W. Griffioen

Cancer Biology

Research output: Contribution to journal › Review article › peer-review

427 Scopus citations

Abstract

The formation of new blood vessels, or angiogenesis, is a complex process that plays important roles in growth and development, tissue and organ regeneration, as well as numerous pathological conditions. Angiogenesis undergoes multiple discrete steps that can be individually evaluated and quantified by a large number of bioassays. These independent assessments hold advantages but also have limitations. This article describes in vivo, ex vivo, and in vitro bioassays that are available for the evaluation of angiogenesis and highlights critical aspects that are relevant for their execution and proper interpretation. As such, this collaborative work is the first edition of consensus guidelines on angiogenesis bioassays to serve for current and future reference.

Original language	English (US)
Pages (from-to)	425-532
Number of pages	108
Journal	Angiogenesis
Volume	21
Issue number	3
DOIs	https://doi.org/10.1007/s10456-018-9613-x
State	Published - Aug 1 2018

Keywords

Angiogenesis
Aortic ring
Chorioallantoic membrane (CAM)
Corneal angiogenesis
Endothelial cell migration
Hindlimb ischemia
Intussusceptive angiogenesis
Microfluidic
Myocardial angiogenesis
Myocardial angiogenesis
Plug assay
Proliferation
Recombinant proteins
Retinal vasculature
Tip cells
Vascular network
Vessel co-option
Zebrafish

ASJC Scopus subject areas

Physiology
Clinical Biochemistry
Cancer Research

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10.1007/s10456-018-9613-x

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Nowak-Sliwinska, P., Alitalo, K., Allen, E., Anisimov, A., Aplin, A. C., Auerbach, R., Augustin, H. G., Bates, D. O., van Beijnum, J. R., Bender, R. H. F., Bergers, G., Bikfalvi, A., Bischoff, J., Böck, B. C., Brooks, P. C., Bussolino, F., Cakir, B., Carmeliet, P., Castranova, D., ... Griffioen, A. W. (2018). Consensus guidelines for the use and interpretation of angiogenesis assays. Angiogenesis, 21(3), 425-532. https://doi.org/10.1007/s10456-018-9613-x

Nowak-Sliwinska, P, Alitalo, K, Allen, E, Anisimov, A, Aplin, AC, Auerbach, R, Augustin, HG, Bates, DO, van Beijnum, JR, Bender, RHF, Bergers, G, Bikfalvi, A, Bischoff, J, Böck, BC, Brooks, PC, Bussolino, F, Cakir, B, Carmeliet, P, Castranova, D, Cimpean, AM, Cleaver, O, Coukos, G, Davis, GE, De Palma, M, Dimberg, A, Dings, RPM, Djonov, V, Dudley, AC, Dufton, NP, Fendt, SM, Ferrara, N, Fruttiger, M, Fukumura, D, Ghesquière, B, Gong, Y, Griffin, RJ, Harris, AL, Hughes, CCW, Hultgren, NW, Iruela-Arispe, ML, Irving, M, Jain, RK, Kalluri, R, Kalucka, J, Kerbel, RS, Kitajewski, J, Klaassen, I, Kleinmann, HK, Koolwijk, P, Kuczynski, E, Kwak, BR, Marien, K, Melero-Martin, JM, Munn, LL, Nicosia, RF, Noel, A, Nurro, J, Olsson, AK, Petrova, TV, Pietras, K, Pili, R, Pollard, JW, Post, MJ, Quax, PHA, Rabinovich, GA, Raica, M, Randi, AM, Ribatti, D, Ruegg, C, Schlingemann, RO, Schulte-Merker, S, Smith, LEH, Song, JW, Stacker, SA, Stalin, J, Stratman, AN, Van de Velde, M, van Hinsbergh, VWM, Vermeulen, PB, Waltenberger, J, Weinstein, BM, Xin, H, Yetkin-Arik, B, Yla-Herttuala, S, Yoder, MC & Griffioen, AW 2018, 'Consensus guidelines for the use and interpretation of angiogenesis assays', Angiogenesis, vol. 21, no. 3, pp. 425-532. https://doi.org/10.1007/s10456-018-9613-x

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title = "Consensus guidelines for the use and interpretation of angiogenesis assays",

abstract = "The formation of new blood vessels, or angiogenesis, is a complex process that plays important roles in growth and development, tissue and organ regeneration, as well as numerous pathological conditions. Angiogenesis undergoes multiple discrete steps that can be individually evaluated and quantified by a large number of bioassays. These independent assessments hold advantages but also have limitations. This article describes in vivo, ex vivo, and in vitro bioassays that are available for the evaluation of angiogenesis and highlights critical aspects that are relevant for their execution and proper interpretation. As such, this collaborative work is the first edition of consensus guidelines on angiogenesis bioassays to serve for current and future reference.",

keywords = "Angiogenesis, Aortic ring, Chorioallantoic membrane (CAM), Corneal angiogenesis, Endothelial cell migration, Hindlimb ischemia, Intussusceptive angiogenesis, Microfluidic, Myocardial angiogenesis, Myocardial angiogenesis, Plug assay, Proliferation, Recombinant proteins, Retinal vasculature, Tip cells, Vascular network, Vessel co-option, Zebrafish",

author = "Patrycja Nowak-Sliwinska and Kari Alitalo and Elizabeth Allen and Andrey Anisimov and Aplin, {Alfred C.} and Robert Auerbach and Augustin, {Hellmut G.} and Bates, {David O.} and {van Beijnum}, {Judy R.} and Bender, {R. Hugh F.} and Gabriele Bergers and Andreas Bikfalvi and Joyce Bischoff and B{\"o}ck, {Barbara C.} and Brooks, {Peter C.} and Federico Bussolino and Bertan Cakir and Peter Carmeliet and Daniel Castranova and Cimpean, {Anca M.} and Ondine Cleaver and George Coukos and Davis, {George E.} and {De Palma}, Michele and Anna Dimberg and Dings, {Ruud P.M.} and Valentin Djonov and Dudley, {Andrew C.} and Dufton, {Neil P.} and Fendt, {Sarah Maria} and Napoleone Ferrara and Marcus Fruttiger and Dai Fukumura and Bart Ghesqui{\`e}re and Yan Gong and Griffin, {Robert J.} and Harris, {Adrian L.} and Hughes, {Christopher C.W.} and Hultgren, {Nan W.} and Iruela-Arispe, {M. Luisa} and Melita Irving and Jain, {Rakesh K.} and Raghu Kalluri and Joanna Kalucka and Kerbel, {Robert S.} and Jan Kitajewski and Ingeborg Klaassen and Kleinmann, {Hynda K.} and Pieter Koolwijk and Elisabeth Kuczynski and Kwak, {Brenda R.} and Koen Marien and Melero-Martin, {Juan M.} and Munn, {Lance L.} and Nicosia, {Roberto F.} and Agnes Noel and Jussi Nurro and Olsson, {Anna Karin} and Petrova, {Tatiana V.} and Kristian Pietras and Roberto Pili and Pollard, {Jeffrey W.} and Post, {Mark J.} and Quax, {Paul H.A.} and Rabinovich, {Gabriel A.} and Marius Raica and Randi, {Anna M.} and Domenico Ribatti and Curzio Ruegg and Schlingemann, {Reinier O.} and Stefan Schulte-Merker and Smith, {Lois E.H.} and Song, {Jonathan W.} and Stacker, {Steven A.} and Jimmy Stalin and Stratman, {Amber N.} and {Van de Velde}, Maureen and {van Hinsbergh}, {Victor W.M.} and Vermeulen, {Peter B.} and Johannes Waltenberger and Weinstein, {Brant M.} and Hong Xin and Bahar Yetkin-Arik and Seppo Yla-Herttuala and Yoder, {Mervin C.} and Griffioen, {Arjan W.}",

note = "Publisher Copyright: {\textcopyright} 2018, The Author(s).",

year = "2018",

month = aug,

day = "1",

doi = "10.1007/s10456-018-9613-x",

language = "English (US)",

volume = "21",

pages = "425--532",

journal = "Angiogenesis",

issn = "0969-6970",

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TY - JOUR

T1 - Consensus guidelines for the use and interpretation of angiogenesis assays

AU - Nowak-Sliwinska, Patrycja

AU - Alitalo, Kari

AU - Allen, Elizabeth

AU - Anisimov, Andrey

AU - Aplin, Alfred C.

AU - Auerbach, Robert

AU - Augustin, Hellmut G.

AU - Bates, David O.

AU - van Beijnum, Judy R.

AU - Bender, R. Hugh F.

AU - Bergers, Gabriele

AU - Bikfalvi, Andreas

AU - Bischoff, Joyce

AU - Böck, Barbara C.

AU - Brooks, Peter C.

AU - Bussolino, Federico

AU - Cakir, Bertan

AU - Carmeliet, Peter

AU - Castranova, Daniel

AU - Cimpean, Anca M.

AU - Cleaver, Ondine

AU - Coukos, George

AU - Davis, George E.

AU - De Palma, Michele

AU - Dimberg, Anna

AU - Dings, Ruud P.M.

AU - Djonov, Valentin

AU - Dudley, Andrew C.

AU - Dufton, Neil P.

AU - Fendt, Sarah Maria

AU - Ferrara, Napoleone

AU - Fruttiger, Marcus

AU - Fukumura, Dai

AU - Ghesquière, Bart

AU - Gong, Yan

AU - Griffin, Robert J.

AU - Harris, Adrian L.

AU - Hughes, Christopher C.W.

AU - Hultgren, Nan W.

AU - Iruela-Arispe, M. Luisa

AU - Irving, Melita

AU - Jain, Rakesh K.

AU - Kalluri, Raghu

AU - Kalucka, Joanna

AU - Kerbel, Robert S.

AU - Kitajewski, Jan

AU - Klaassen, Ingeborg

AU - Kleinmann, Hynda K.

AU - Koolwijk, Pieter

AU - Kuczynski, Elisabeth

AU - Kwak, Brenda R.

AU - Marien, Koen

AU - Melero-Martin, Juan M.

AU - Munn, Lance L.

AU - Nicosia, Roberto F.

AU - Noel, Agnes

AU - Nurro, Jussi

AU - Olsson, Anna Karin

AU - Petrova, Tatiana V.

AU - Pietras, Kristian

AU - Pili, Roberto

AU - Pollard, Jeffrey W.

AU - Post, Mark J.

AU - Quax, Paul H.A.

AU - Rabinovich, Gabriel A.

AU - Raica, Marius

AU - Randi, Anna M.

AU - Ribatti, Domenico

AU - Ruegg, Curzio

AU - Schlingemann, Reinier O.

AU - Schulte-Merker, Stefan

AU - Smith, Lois E.H.

AU - Song, Jonathan W.

AU - Stacker, Steven A.

AU - Stalin, Jimmy

AU - Stratman, Amber N.

AU - Van de Velde, Maureen

AU - van Hinsbergh, Victor W.M.

AU - Vermeulen, Peter B.

AU - Waltenberger, Johannes

AU - Weinstein, Brant M.

AU - Xin, Hong

AU - Yetkin-Arik, Bahar

AU - Yla-Herttuala, Seppo

AU - Yoder, Mervin C.

AU - Griffioen, Arjan W.

PY - 2018/8/1

Y1 - 2018/8/1

N2 - The formation of new blood vessels, or angiogenesis, is a complex process that plays important roles in growth and development, tissue and organ regeneration, as well as numerous pathological conditions. Angiogenesis undergoes multiple discrete steps that can be individually evaluated and quantified by a large number of bioassays. These independent assessments hold advantages but also have limitations. This article describes in vivo, ex vivo, and in vitro bioassays that are available for the evaluation of angiogenesis and highlights critical aspects that are relevant for their execution and proper interpretation. As such, this collaborative work is the first edition of consensus guidelines on angiogenesis bioassays to serve for current and future reference.

AB - The formation of new blood vessels, or angiogenesis, is a complex process that plays important roles in growth and development, tissue and organ regeneration, as well as numerous pathological conditions. Angiogenesis undergoes multiple discrete steps that can be individually evaluated and quantified by a large number of bioassays. These independent assessments hold advantages but also have limitations. This article describes in vivo, ex vivo, and in vitro bioassays that are available for the evaluation of angiogenesis and highlights critical aspects that are relevant for their execution and proper interpretation. As such, this collaborative work is the first edition of consensus guidelines on angiogenesis bioassays to serve for current and future reference.

KW - Angiogenesis

KW - Aortic ring

KW - Chorioallantoic membrane (CAM)

KW - Corneal angiogenesis

KW - Endothelial cell migration

KW - Hindlimb ischemia

KW - Intussusceptive angiogenesis

KW - Microfluidic

KW - Myocardial angiogenesis

KW - Plug assay

KW - Proliferation

KW - Recombinant proteins

KW - Retinal vasculature

KW - Tip cells

KW - Vascular network

KW - Vessel co-option

KW - Zebrafish

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UR - http://www.scopus.com/inward/citedby.url?scp=85046903965&partnerID=8YFLogxK

U2 - 10.1007/s10456-018-9613-x

DO - 10.1007/s10456-018-9613-x

M3 - Review article

C2 - 29766399

AN - SCOPUS:85046903965

SN - 0969-6970

VL - 21

SP - 425

EP - 532

JO - Angiogenesis

JF - Angiogenesis

IS - 3

ER -

Consensus guidelines for the use and interpretation of angiogenesis assays

Abstract

Keywords

ASJC Scopus subject areas

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