Galectin-3 interferes with tissue repair and promotes cardiac dysfunction and comorbidities in a genetic heart failure model.
Cell proliferation
Failing heart
Galectins
Macrophage–fibroblast cross-talk
Pro-fibrotic response
Journal
Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402
Informations de publication
Date de publication:
19 Apr 2022
19 Apr 2022
Historique:
received:
29
11
2021
accepted:
21
03
2022
revised:
14
03
2022
entrez:
20
4
2022
pubmed:
21
4
2022
medline:
22
4
2022
Statut:
epublish
Résumé
Galectin-3, a biomarker for heart failure (HF), has been associated with myocardial fibrosis. However, its causal involvement in HF pathogenesis has been questioned in certain models of cardiac injury-induced HF. To address this, we used desmin-deficient mice (des
Identifiants
pubmed: 35441327
doi: 10.1007/s00018-022-04266-6
pii: 10.1007/s00018-022-04266-6
doi:
Substances chimiques
Desmin
0
Galectin 3
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
250Subventions
Organisme : General Secretariat for Research and Technology
ID : Synergasia ESPA 09SYN-21-965
Organisme : Hellenic Cardiological Society
ID : 2010-13/151
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
de Boer RA, De Keulenaer G, Bauersachs J, Brutsaert D, Cleland JG, Diez J, Du XJ, Ford P, Heinzel FR, Lipson KE, McDonagh T, Lopez-Andres N, Lunde IG, Lyon AR, Pollesello P, Prasad SK, Tocchetti CG, Mayr M, Sluijter JPG, Thum T, Tschöpe C, Zannad F, Zimmermann WH, Ruschitzka F, Filippatos G, Lindsey ML, Maack C, Heymans S (2019) Towards better definition, quantification and treatment of fibrosis in heart failure. A scientific roadmap by the Committee of Translational Research of the Heart Failure Association (HFA) of the European Society of Cardiology. Eur J Heart Fail 21:272–285
doi: 10.1002/ejhf.1406
Psarras S, Beis D, Nikouli S, Tsikitis M, Capetanaki Y (2019) Three in a Box: understanding cardiomyocyte, fibroblast, and innate immune cell interactions to orchestrate cardiac repair processes. Front Cardiovasc Med 6:1–23. https://doi.org/10.3389/fcvm.2019.00032
doi: 10.3389/fcvm.2019.00032
Ivey MJ, Kuwabara JT, Pai JT, Moore RE, Sun Z, Tallquist MD (2018) Resident fibroblast expansion during cardiac growth and remodeling. J Mol Cell Cardiol 114:161–174. https://doi.org/10.1016/j.yjmcc.2017.11.012
doi: 10.1016/j.yjmcc.2017.11.012
pubmed: 29158033
Prabhu SD, Frangogiannis NG (2016) The biological basis for cardiac repair after myocardial infarction. Circ Res 119:91–112. https://doi.org/10.1161/CIRCRESAHA.116.303577
doi: 10.1161/CIRCRESAHA.116.303577
pubmed: 27340270
pmcid: 4922528
Henderson NC, Rieder F, Wynn TA (2020) Fibrosis: from mechanisms to medicines. Nature 587:555–566. https://doi.org/10.1038/s41586-020-2938-9
doi: 10.1038/s41586-020-2938-9
pubmed: 33239795
pmcid: 8034822
Triposkiadis F, Giamouzis G, Parissis J, Starling RC, Boudoulas H, Skoularigis J, Butler J, Filippatos G (2016) Reframing the association and significance of co-morbidities in heart failure. Eur J Heart Fail 18:744–758. https://doi.org/10.1002/ejhf.600
doi: 10.1002/ejhf.600
pubmed: 27358242
Sciacchitano S, Lavra L, Morgante A, Ulivieri A, Magi F, De Francesco GP, Bellotti C, Salehi LB, Ricci A (2018) Galectin-3: one molecule for an alphabet of diseases, from A to Z. Int J Mol Sci. https://doi.org/10.3390/ijms19020379
doi: 10.3390/ijms19020379
pubmed: 29393868
pmcid: 5855667
Lok DJ, Lok SI, Bruggink-André De La Porte PW, Badings E, Lipsic E, Van Wijngaarden J, De Boer RA, Van Veldhuisen DJ, Van Der Meer P (2013) Galectin-3 is an independent marker for ventricular remodeling and mortality in patients with chronic heart failure. Clin Res Cardiol 102:103–110. https://doi.org/10.1007/s00392-012-0500-y
doi: 10.1007/s00392-012-0500-y
pubmed: 22886030
Suthahar N, Meijers WC, Silljé HHW, Ho JE, Liu FT, de Boer RA (2018) Galectin-3 activation and inhibition in heart failure and cardiovascular disease: an update. Theranostics 8:593–609
doi: 10.7150/thno.22196
González GE, Rhaleb N-E, D’Ambrosio MA, Nakagawa P, Liao T-D, Peterson EL, Leung P, Dai X, Janic B, Liu Y, Yang X, Carretero OA, Ambrosio MAD, Nakagawa P, Liao T-D, Peterson EL, Leung P, Dai X, Janic B, Liu Y, Yang X, Carretero OA, Ge G, Rhaleb N-E, Ma DA, Nakagawa P, Liao T-D, El P, Leung P, Dai X, Janic B, Liu Y, Yang X, Oa C (2016) Cardiac-deleterious role of galectin-3 in chronic angiotensin II-induced hypertension. Am J Physiol Circ Physiol 311:H1287-1296. https://doi.org/10.1152/ajpheart.00096.2016
doi: 10.1152/ajpheart.00096.2016
Yu L, Ruifrok WPT, Meissner M, Bos EM, Van Goor H, Sanjabi B, Van Der Harst P, Pitt B, Goldstein IJ, Koerts JA, Van Veldhuisen DJ, Bank RA, Van Gilst WH, Silljé HHW, De Boer RA (2013) Genetic and pharmacological inhibition of galectin-3 prevents cardiac remodeling by interfering with myocardial fibrogenesis. Circ Hear Fail 6:107–117. https://doi.org/10.1161/CIRCHEARTFAILURE.112.971168
doi: 10.1161/CIRCHEARTFAILURE.112.971168
Nguyen MN, Su Y, Kiriazis H, Yang Y, Gao XM, McMullen JR, Dart AM, Du XJ (2018) Upregulated galectin-3 is not a critical disease mediator of cardiomyopathy induced by β2-adrenoceptor overexpression. Am J Physiol Hear Circ Physiol 314:H1169–H1178. https://doi.org/10.1152/ajpheart.00337.2017
doi: 10.1152/ajpheart.00337.2017
Frunza O, Russo I, Saxena A, Shinde AV, Humeres C, Hanif W, Rai V, Su Y, Frangogiannis NG (2016) Myocardial galectin-3 expression is associated with remodeling of the pressure-overloaded heart and may delay the hypertrophic response without affecting survival, dysfunction, and cardiac fibrosis. Am J Pathol 186:1114–1127. https://doi.org/10.1016/j.ajpath.2015.12.017
doi: 10.1016/j.ajpath.2015.12.017
pubmed: 26948424
pmcid: 4861760
Diokmetzidou A, Soumaka E, Kloukina I, Tsikitis M, Makridakis M, Varela A, Davos CH, Georgopoulos S, Anesti V, Vlahou A, Capetanaki Y (2016) Desmin and αB-crystallin interplay in the maintenance of mitochondrial homeostasis and cardiomyocyte survival. J Cell Sci 129:3705–3720. https://doi.org/10.1242/jcs.192203
doi: 10.1242/jcs.192203
pubmed: 27566162
pmcid: 5087667
Psarras S, Mavroidis M, Sanoudou D, Davos CH, Xanthou G, Varela AE, Panoutsakopoulou V, Capetanaki Y (2012) Regulation of adverse remodelling by osteopontin in a genetic heart failure model. Eur Heart J 33:1954–1963. https://doi.org/10.1093/eurheartj/ehr119
doi: 10.1093/eurheartj/ehr119
pubmed: 21525025
Mavroidis M, Davos CH, Psarras S, Varela A, Athanasiadis NC, Katsimpoulas M, Kostavasili I, Maasch C, Vater A, van Tintelen JP, Capetanaki Y (2015) Complement system modulation as a target for treatment of arrhythmogenic cardiomyopathy. Basic Res Cardiol 110:27. https://doi.org/10.1007/s00395-015-0485-6
doi: 10.1007/s00395-015-0485-6
pubmed: 25851234
Milner DJ, Taffet GE, Wang X, Pham T, Tamura T, Hartley C, Gerdes MA, Capetanaki Y (1999) The absence of desmin leads to cardiomyocyte hypertrophy and cardiac dilation with compromised systolic function. J Mol Cell Cardiol 31:2063–2076. https://doi.org/10.1006/jmcc.1999.1037
doi: 10.1006/jmcc.1999.1037
pubmed: 10591032
Colnot C, Fowlis D, Ripoche MA, Bouchaert I, Poirier F (1998) Embryonic implantation in galectin 1/galectin 3 double mutant mice. Dev Dyn 211:306–313. https://doi.org/10.1002/(SICI)1097-0177(199804)211:4%3c306::AID-AJA2%3e3.0.CO;2-L
doi: 10.1002/(SICI)1097-0177(199804)211:4<306::AID-AJA2>3.0.CO;2-L
pubmed: 9566950
Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y (1996) Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol 134:1255–1270. https://doi.org/10.1083/jcb.134.5.1255
doi: 10.1083/jcb.134.5.1255
pubmed: 8794866
Apostolou E, Stavropoulos A, Sountoulidis A, Xirakia C, Giaglis S, Protopapadakis E, Ritis K, Mentzelopoulos S, Pasternack A, Foster M, Ritvos O, Tzelepis GE, Andreakos E, Sideras P (2012) Activin-A overexpression in the murine lung causes pathology that simulates acute respiratory distress syndrome. Am J Respir Crit Care Med 185:382–391. https://doi.org/10.1164/rccm.201105-0784OC
doi: 10.1164/rccm.201105-0784OC
pubmed: 22161160
Bossios A, Psarras S, Gourgiotis D, Skevaki CLCL, Constantopoulos AGAGAG, Saxoni-Papageorgiou P, Papadopoulos NGNGNG (2005) Rhinovirus infection induces cytotoxicity and delays wound healing in bronchial epithelial cells. Respir Res 6:1–11. https://doi.org/10.1186/1465-9921-6-114
doi: 10.1186/1465-9921-6-114
Pratsinis H, Kletsas D, Melliou E, Chinou I (2010) Antiproliferative activity of Greek propolis. J Med Food 13:286–290
doi: 10.1089/jmf.2009.0071
Darzynkiewicz Z, Halicka H, Zhao H (2010) Analysis of cellular DNA content by flow and laser scanning cytometry. Adv Exp Med Biol 676:137–147
doi: 10.1007/978-1-4419-6199-0_9
Liakou E, Mavrogonatou E, Pratsinis H, Rizou S, Evangelou K, Panagiotou PN, Karamanos NK, Gorgoulis VG, Kletsas D (2016) Ionizing radiation-mediated premature senescence and paracrine interactions with cancer cells enhance the expression of syndecan 1 in human breast stromal fibroblasts: The role of TGF-β. Aging (Albany NY) 8:1650–1669. https://doi.org/10.18632/aging.100989
doi: 10.18632/aging.100989
Johannes L, Jacob R, Leffler H (2018) Galectins at a glance. J Cell Sci 131:1–9. https://doi.org/10.1242/jcs.208884
doi: 10.1242/jcs.208884
Liu YH, D’Ambrosio M, Liao TD, Peng H, Rhaleb NE, Sharma U, Andre S, Gabius HJ, Carretero OA (2009) N-acetyl-seryl-aspartyl-lysyl-proline prevents cardiac remodeling and dysfunction induced by galectin-3, a mammalian adhesion/growth-regulatory lectin. Am J Physiol Hear Circ Physiol 296:H404–H412. https://doi.org/10.1152/ajpheart.00747.2008
doi: 10.1152/ajpheart.00747.2008
Piek A, de Boer RA, Silljé HHW (2016) The fibrosis-cell death axis in heart failure. Heart Fail Rev 21:199–211. https://doi.org/10.1007/s10741-016-9536-9
doi: 10.1007/s10741-016-9536-9
pubmed: 26883434
pmcid: 4762920
Li X, Tang X, Lu J, Yuan S (2018) Therapeutic inhibition of Galectin-3 improves cardiomyocyte apoptosis and survival during heart failure. Mol Med Rep 17:4106–4112. https://doi.org/10.3892/mmr.2017.8323
doi: 10.3892/mmr.2017.8323
pubmed: 29286090
Maria DX, Asensio-lopez DELC, Dx S, Fernandez J, Palacio DEL, del Asensio-Lopez MC, Lax A, Fernandez del Palacio MJ, Sassi Y, Hajjar RJ, Pascual-Figal DA (2018) Pharmacological inhibition of the mitochondrial NADPH oxidase 4/PKCα/Gal-3 pathway reduces left ventricular fibrosis following myocardial infarction. Transl Res 199:4–23. https://doi.org/10.1016/j.trsl.2018.04.004
doi: 10.1016/j.trsl.2018.04.004
Bajpai G, Bredemeyer AAL, Li WW, Zaitsev K, Koenig ALAL, Lokshina II, Mohan J, Ivey B, Hsiao HMH, Weinheimer CC, Kovacs A, Epelman S, Artyomov MM, Kreisel D, Lavine KJK (2019) Tissue resident CCR2- and CCR2+ cardiac macrophages differentially orchestrate monocyte recruitment and fate specification following myocardial injury. Circ Res 124:263–278. https://doi.org/10.1161/CIRCRESAHA.118.314028
doi: 10.1161/CIRCRESAHA.118.314028
pubmed: 30582448
pmcid: 6626616
Schlüter K-D, Schulz R, Schreckenberg R (2015) Arginase induction and activation during ischemia and reperfusion and functional consequences for the heart. Front Physiol 6:1–8. https://doi.org/10.3389/fphys.2015.00065
doi: 10.3389/fphys.2015.00065
Riehle C, Bauersachs J (2019) Small animal models of heart failure. Cardiovasc Res 115:1838–1849. https://doi.org/10.1093/cvr/cvz161
doi: 10.1093/cvr/cvz161
pubmed: 31243437
pmcid: 6803815
Wu CK, Su MY, Lee JK, Chiang FT, Hwang JJ, Lin JL, Chen JJ, Liu FT, Tsai CT (2015) Galectin-3 level and the severity of cardiac diastolic dysfunction using cellular and animal models and clinical indices. Sci Rep 5:1–10. https://doi.org/10.1038/srep17007
doi: 10.1038/srep17007
Sonkawade S, Pokharel S, Karthikeyan B, Kim M, Xu S, Kc K, Sexton S, Catalfamo K, Spernyak J, Sharma UC (2021) Small endogeneous peptide mitigates myocardial remodeling in a mouse model of cardioselective galectin-3 overexpression. Circ Hear Fail 14:e008510
Cassaglia P, Penas F, Betazza C, Fontana Estevez F, Miksztowicz V, Martínez Naya N, Llamosas MC, Noli Truant S, Wilensky L, Volberg V, Cevey ÁC, Touceda V, Cicale E, Berg G, Fernández M, Goren N, Morales C, González GE (2020) Genetic deletion of galectin-3 alters the temporal evolution of macrophage infiltration and healing affecting the cardiac remodeling and function after myocardial infarction in mice. Am J Pathol 190:1789–1800. https://doi.org/10.1016/j.ajpath.2020.05.010
doi: 10.1016/j.ajpath.2020.05.010
pubmed: 32473918
Mackinnon AC, Farnworth SL, Hodkinson PS, Henderson NC, Atkinson KM, Leffler H, Nilsson UJ, Haslett C, Forbes SJ, Sethi T (2008) Regulation of alternative macrophage activation by galectin-3. J Immunol 180:20–22
doi: 10.4049/jimmunol.180.4.2650
Nahrendorf M, Swirski FK (2016) Abandoning M1/M2 for a network model of macrophage function. Circ Res 119:414–417. https://doi.org/10.1161/CIRCRESAHA.116.309194
doi: 10.1161/CIRCRESAHA.116.309194
pubmed: 27458196
pmcid: 4965179
Walter W, Alonso-Herranz L, Trappetti V, Crespo I, Ibberson M, Cedenilla M, Karaszewska A, Núñez V, Xenarios I, Arroyo AG, Sánchez-Cabo F, Ricote M (2018) Deciphering the dynamic transcriptional and post-transcriptional networks of macrophages in the healthy heart and after myocardial injury. Cell Rep 23:622–636. https://doi.org/10.1016/j.celrep.2018.03.029
doi: 10.1016/j.celrep.2018.03.029
pubmed: 29642017
Adler M, Mayo A, Zhou X, Franklin RA, Meizlish ML, Medzhitov R, Kallenberger SM, Alon U (2020) Principles of cell circuits for tissue repair and fibrosis. iScience 23:100841. https://doi.org/10.1016/j.isci.2020.100841
doi: 10.1016/j.isci.2020.100841
pubmed: 32058955
pmcid: 7005469
Wu R, Ma F, Tosevska A, Farrell C, Pellegrini M, Deb A (2020) Cardiac fibroblast proliferation rates and collagen expression mature early and are unaltered with advancing age. JCI Insight. https://doi.org/10.1172/jci.insight.140628
doi: 10.1172/jci.insight.140628
pubmed: 33290278
pmcid: 7819745
Bujak M, Kweon HJ, Chatila K, Li N, Taffet G, Frangogiannis NG (2008) Aging-Related defects are associated with adverse cardiac remodeling in a mouse model of reperfused myocardial infarction. J Am Coll Cardiol 51:1384–1392. https://doi.org/10.1016/j.jacc.2008.01.011
doi: 10.1016/j.jacc.2008.01.011
pubmed: 18387441
pmcid: 3348616
Zhu F, Li Y, Zhang J, Piao C, Liu T, Li HH, Du J (2013) Senescent cardiac fibroblast is critical for cardiac fibrosis after myocardial infarction. PLoS One 8:1–12. https://doi.org/10.1371/journal.pone.0074535
doi: 10.1371/journal.pone.0074535
Ibarrola J, Sádaba R, Garcia-Peña A, Arrieta V, Martinez-Martinez E, Alvarez V, Fernández-Celis A, Gainza A, Santamaría E, Fernández-Irigoyen J, Cachofeiro V, Fay R, Rossignol P, López-Andrés N (2018) A role for fumarate hydratase in mediating oxidative effects of galectin-3 in human cardiac fibroblasts. Int J Cardiol 258:217–223. https://doi.org/10.1016/j.ijcard.2017.12.103
doi: 10.1016/j.ijcard.2017.12.103
pubmed: 29544935
de Souza BSF, Silva DN, Carvalho RH, de Sampaio GLA, Paredes BD, Aragão França L, Azevedo CM, Vasconcelos JF, Meira CS, Neto PC, Macambira SG, da Silva KN, Allahdadi KJ, Tavora F, de Souza Neto JD, dos Santos RR, Soares MBP (2017) Association of cardiac galectin-3 expression, myocarditis, and fibrosis in chronic chagas disease cardiomyopathy. Am J Pathol 187:1134–1146. https://doi.org/10.1016/j.ajpath.2017.01.016
doi: 10.1016/j.ajpath.2017.01.016
pubmed: 28322201
González GE, Cassaglia P, Noli Truant S, Fernández MM, Wilensky L, Volberg V, Malchiodi EL, Morales C, Gelpi RJ (2014) Galectin-3 is essential for early wound healing and ventricular remodeling after myocardial infarction in mice. Int J Cardiol 176:1423–1425. https://doi.org/10.1016/j.ijcard.2014.08.011
doi: 10.1016/j.ijcard.2014.08.011
pubmed: 25150483
Shirakawa K, Endo J, Kataoka M, Katsumata Y, Yoshida N, Yamamoto T, Isobe S, Moriyama H, Goto S, Kitakata H, Hiraide T, Fukuda K, Sano M (2018) IL (interleukin)-10-STAT3-galectin-3 axis is essential for osteopontin-producing reparative macrophage polarization after myocardial infarction. Circulation 138:2021–2035. https://doi.org/10.1161/CIRCULATIONAHA.118.035047
doi: 10.1161/CIRCULATIONAHA.118.035047
pubmed: 29967195
Shardonofsky FR, Capetanaki Y, Boriek AM (2006) Desmin modulates lung elastic recoil and airway responsiveness. Am J Physiol Lung Cell Mol Physiol 290:890–896. https://doi.org/10.1152/ajplung.00397.2005
doi: 10.1152/ajplung.00397.2005
Mohamed JS, Hajira A, Li Z, Paulin D, Boriek AM (2011) Desmin regulates airway smooth muscle hypertrophy through early growth-responsive protein-1 and microRNA-26a. J Biol Chem 286:43394–43404. https://doi.org/10.1074/jbc.M111.235127
doi: 10.1074/jbc.M111.235127
pubmed: 21903578
pmcid: 3234798
Higham A, Quinn AM, Cançado JED, Singh D (2019) The pathology of small airways disease in COPD: historical aspects and future directions. Respir Res 20:1–11. https://doi.org/10.1186/s12931-019-1017-y
doi: 10.1186/s12931-019-1017-y
Pilette C, Colinet B, Kiss R, André S, Kaltner H, Gabius HJ, Delos M, Vaerman JP, Decramer M, Sibille Y (2007) Increased galectin-3 expression and intra-epithelial neutrophils in small airways in severe COPD. Eur Respir J 29:914–922. https://doi.org/10.1183/09031936.00073005
doi: 10.1183/09031936.00073005
pubmed: 17251233
Markowska AI, Liu F-T, Panjwani N (2010) Galectin-3 is an important mediator of VEGF- and bFGF-mediated angiogenic response. J Exp Med 207:1981–1993. https://doi.org/10.1084/jem.20090121
doi: 10.1084/jem.20090121
pubmed: 20713592
pmcid: 2931172
Cahill TJ, Choudhury RP, Riley PR (2017) Heart regeneration and repair after myocardial infarction: translational opportunities for novel therapeutics. Nat Rev Drug Discov 16:699–717. https://doi.org/10.1038/nrd.2017.106
doi: 10.1038/nrd.2017.106
pubmed: 28729726
Dick SA, Epelman S (2016) Chronic heart failure and inflammation. Circ Res 119:159–176. https://doi.org/10.1161/CIRCRESAHA.116.308030
doi: 10.1161/CIRCRESAHA.116.308030
pubmed: 27340274
Dings RPM, Miller MC, Griffin RJ, Mayo KH (2018) Galectins as molecular targets for therapeutic intervention. Int J Mol Sci 19:1–22. https://doi.org/10.3390/ijms19030905
doi: 10.3390/ijms19030905
Seropian IM, Cerliani JP, Toldo S, Van Tassell BW, Ilarregui JM, González GE, Matoso M, Salloum FN, Melchior R, Gelpi RJ, Stupirski JC, Benatar A, Gómez KA, Morales C, Abbate A, Rabinovich GA (2013) Galectin-1 controls cardiac inflammation and ventricular remodeling during acute myocardial infarction. Am J Pathol 182:29–40. https://doi.org/10.1016/j.ajpath.2012.09.022
doi: 10.1016/j.ajpath.2012.09.022
pubmed: 23142379
pmcid: 5691326
McWhorter FY, Wang T, Nguyen P, Chung T, Liu WF (2013) Modulation of macrophage phenotype by cell shape. Proc Natl Acad Sci USA 110:17253–17258. https://doi.org/10.1073/pnas.1308887110
doi: 10.1073/pnas.1308887110
pubmed: 24101477
pmcid: 3808615
Ibarrola J, Matilla L, Martínez-Martínez E, Gueret A, Fernández-Celis A, Henry JP, Nicol L, Jaisser F, Mulder P, Ouvrard-Pascaud A, López-Andrés N (2019) Myocardial injury after ischemia/reperfusion is attenuated by pharmacological galectin-3 inhibition. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-46119-6
doi: 10.1038/s41598-019-46119-6
Miller M, Ludwig A, Wichapong K, Kaltner H, Kopitz J, Gabius H, Mayo K (2018) Adhesion/growth-regulatory galectins tested in combination: evidence for formation of hybrids as heterodimers. Biochem J 475:1003–1018. https://doi.org/10.1042/BCJ20170658
doi: 10.1042/BCJ20170658
pubmed: 29321242
D’Haene N, Sauvage S, Maris C, Adanja I, Le Mercier M, Decaestecker C, Baum L, Salmon I (2013) VEGFR1 and VEGFR2 involvement in extracellular galectin-1- and galectin-3-induced angiogenesis. PLoS One 8:e67029. https://doi.org/10.1371/journal.pone.0067029
doi: 10.1371/journal.pone.0067029
pubmed: 23799140
pmcid: 3684579
von Hundelshausen P, Wichapong K, Gabius HJ, Mayo KH (2021) The marriage of chemokines and galectins as functional heterodimers. Cell Mol Life Sci 78:8073–8095. https://doi.org/10.1007/s00018-021-04010-6
doi: 10.1007/s00018-021-04010-6