152
Views
0
CrossRef citations to date
0
Altmetric
Review

The sweet side of wound healing: galectins as promising therapeutic targets in hemostasis, inflammation, proliferation, and maturation/remodeling

, , &
Pages 41-53 | Received 28 Sep 2022, Accepted 29 Jan 2023, Published online: 09 Feb 2023

References

  • Gabius HJ, Andre S, Jimenez-Barbero J, et al. From lectin structure to functional glycomics: principles of the sugar code. Trends Biochem Sci. 2011 Jun;36(6):298–313
  • Solis D, Bovin NV, Davis AP, et al. A guide into glycosciences: how chemistry, biochemistry and biology cooperate to crack the sugar code. Biochim Biophys Acta. 2015 Jan;1850(1):186–235
  • Gabius HJ, Kaltner H, Kopitz J, et al. The glycobiology of the CD system: a dictionary for translating marker designations into glycan/lectin structure and function. Trends Biochem Sci. 2015 Jul;40(7):360–376
  • Gal P, Varinska L, Faber L, et al. How signaling molecules regulate tumor microenvironment: parallels to wound repair. Molecules. 2017 Oct 26;22:11.
  • Villalobo A, Nogales-Gonzalez A, Gabius HJ. A guide to signaling pathways connecting protein-glycan interaction with the emerging versatile effector functionality of mammalian lectins. Trends Glycosci Glyc. 2006 Jan;18(99):1–37.
  • Cummings RD. Stuck on sugars - how carbohydrates regulate cell adhesion, recognition, and signaling. Glycoconj J. 2019 Aug;36(4):241–257.
  • Vidinsky B, Gal P, Toporcer T, et al. Histological study of the first seven days of skin wound healing in rats. Acta Vet Brno. 2006 Jun;75(2):197–+
  • Gal P, Kilik R, Mokry M, et al. Simple method of open skin wound healing model in corticosteroid-treated and diabetic rats: standardization of semi-quantitative and quantitative histological assessments. Vet Med-Czech. 2008 Dec;53(12):652–659
  • Rüdiger H, Gabius HJ. The sugar code. Fundamentals of glycosciences. In: Gabius HJ, editor. The history of lectinology. Weinheim Germany: Wiley-VCH; 2009. p. 261–268.
  • Garcia Caballero G, Kaltner H, Kutzner TJ, et al. How galectins have become multifunctional proteins. Histol Histopathol. 2020 Jun;35(6):509–539
  • Schedlbauer A, Gilles U, Ludwig AK, et al. Characterizing ligand-induced conformational changes in clinically relevant galectin-1 by H(N)/H2O (D2O) exchange. Biochimie. 2021 Aug;187:48–56.
  • He LZ, Andre S, Siebert HC, et al. Detection of ligand- and solvent-induced shape alterations of cell-growth-regulatory human lectin galectin-1 in solution by small angle neutron and x-ray scattering. Biophys J. 2003 Jul;85(1):511–524
  • Gendronneau G, Sidhu SS, Delacour D, et al. Galectin-7 in the control of epidermal homeostasis after injury. Mol Biol Cell. 2008 Dec;19(12):5541–5549
  • Paclik D, Lohse K, Wiedenmann B, et al. Galectin-2 and −4, but not galectin-1, promote intestinal epithelial wound healing in vitro through a TGF-beta-independent mechanism. Inflamm Bowel Dis. 2008 Oct;14(10):1366–1372
  • Cooper DN. Galectinomics: finding themes in complexity. Biochim Biophys Acta. 2002 Sep 19;1572(2–3):209–231.
  • Gabius HJ. Animal lectins. Eur J Biochem. 1997 Feb 1;243(3):543–576.
  • Ahmad N, Gabius HJ, Andre S, et al. Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J Biol Chem. 2004 Mar 19;279(12):10841–10847.
  • Chiu YP, Sun YC, Qiu DC, et al. Liquid-liquid phase separation and extracellular multivalent interactions in the tale of galectin-3. Nat Commun. 2020 Mar 6;11(1):1229.
  • HJ G, JC M, Kopitz J, et al. Sweet complementarity: the functional pairing of glycans with lectins. Cell Mol Life Sci. 2016 May;73(10):1989–2016
  • Fischer C, Sanchez-Ruderisch H, Welzel M, et al. Galectin-1 interacts with the {alpha}5{beta}1 fibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J Biol Chem. 2005 Nov 4;280(44):37266–37277.
  • JC M, Romero A, FA H, et al. Lectins: a primer for histochemists and cell biologists. Histochem Cell Biol. 2017 Feb;147(2):199–222
  • Reinke JM, Sorg H. Wound repair and regeneration. Eur Surg Res. 2012;49(1):35–43.
  • Berndt MC, Metharom P, Andrews RK. Primary haemostasis: newer insights. Haemophilia. 2014 May;20(Suppl 4):15–22.
  • Ni H, Denis CV, Subbarao S, et al. Persistence of platelet thrombus formation in arterioles of mice lacking both von Willebrand factor and fibrinogen. J Clin Invest. 2000 Aug;106(3):385–392
  • Romaniuk MA, Tribulatti MV, Cattaneo V, et al. Human platelets express and are activated by galectin-8. Biochem J. 2010 Dec 15;432(3):535–547.
  • Schattner M. Platelets and galectins. Ann Transl Med. 2014 Sep;2(9):85.
  • Shattil SJ, Kim C, Ginsberg MH. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol. 2010 Apr;11(4):288–300.
  • Pacienza N, Pozner RG, Bianco GA, et al. The immunoregulatory glycan-binding protein galectin-1 triggers human platelet activation. FASEB J. 2008;22(4):1113–1123.
  • O’Sullivan JM, Jenkins PV, Rawley O, et al. Galectin-1 and galectin-3 constitute novel-binding partners for factor VIII. Arterioscler Thromb Vasc Biol. 2016;36(5):855–863
  • Ellis S, Lin EJ, Tartar D. Immunology of wound healing. Curr Dermatol Rep. 2018;7(4):350–358.
  • Wilgus TA. Inflammation as an orchestrator of cutaneous scar formation: a review of the literature. Plast Aesthet Res. 2020;7:54.
  • Landen NX, Li D, Stahle M. Transition from inflammation to proliferation: a critical step during wound healing. Cell Mol Life Sci. 2016 Oct;73(20):3861–3885.
  • de Oliveira S, Rosowski EE, Huttenlocher A. Neutrophil migration in infection and wound repair: going forward in reverse. Nat Rev Immunol. 2016 May 27;16(6):378–391.
  • Nieminen J, St-Pierre C, Sato S. Galectin-3 interacts with naive and primed neutrophils, inducing innate immune responses. J Leukoc Biol. 2005 Nov;78(5):1127–1135.
  • Almkvist J, Dahlgren C, Leffler H, et al. Activation of the neutrophil nicotinamide adenine dinucleotide phosphate oxidase by galectin-1. J Immunol. 2002 Apr 15;168(8):4034–4041.
  • Nishi N, Shoji H, Seki M, et al. Galectin-8 modulates neutrophil function via interaction with integrin alphaM. Glycobiology. 2003 Nov;13(11):755–763
  • Vega-Carrascal I, Bergin DA, McElvaney OJ, et al. Galectin-9 signaling through TIM-3 is involved in neutrophil-mediated Gram-negative bacterial killing: an effect abrogated within the cystic fibrosis lung. J Immunol. 2014 Mar 1;192(5):2418–2431.
  • Yamaoka A, Kuwabara I, Frigeri LG, et al. A human lectin, galectin-3 (epsilon bp/Mac-2), stimulates superoxide production by neutrophils. J Immunol. 1995 Apr 1;154(7):3479–3487.
  • Stowell SR, Karmakar S, Arthur CM, et al. Galectin-1 induces reversible phosphatidylserine exposure at the plasma membrane. Mol Biol Cell. 2009 Mar;20(5):1408–1418
  • Stowell SR, Karmakar S, Stowell CJ, et al. Human galectin-1, −2, and −4 induce surface exposure of phosphatidylserine in activated human neutrophils but not in activated T cells. Blood. 2007 Jan 1;109(1):219–227.
  • Law HL, Wright RD, Iqbal AJ, et al. A pro-resolving role for galectin-1 in acute inflammation. Front Pharmacol. 2020;11:274.
  • Fernandez GC, Ilarregui JM, Rubel CJ, et al. Galectin-3 and soluble fibrinogen act in concert to modulate neutrophil activation and survival: involvement of alternative MAPK pathways. Glycobiology. 2005 May;15(5):519–527
  • Karlsson A, Christenson K, Matlak M, et al. Galectin-3 functions as an opsonin and enhances the macrophage clearance of apoptotic neutrophils. Glycobiology. 2009 Jan;19(1):16–20.
  • Auvynet C, Moreno S, Melchy E, et al. Galectin-1 promotes human neutrophil migration. Glycobiology. 2013 Jan;23(1):32–42
  • Gil CD, La M, Perretti M, et al. Interaction of human neutrophils with endothelial cells regulates the expression of endogenous proteins annexin 1, galectin-1 and galectin-3. Cell Biol Int. 2006 Apr;30(4):338–344
  • Hirao H, Uchida Y, Kadono K, et al. The protective function of galectin-9 in liver ischemia and reperfusion injury in mice. Liver Transpl. 2015 Jul;21(7):969–981
  • Farnworth SL, Henderson NC, Mackinnon AC, et al. Galectin-3 reduces the severity of pneumococcal pneumonia by augmenting neutrophil function. Am J Pathol. 2008 Feb;172(2):395–405
  • Rostoker R, Yaseen H, Schif-Zuck S, et al. Galectin-1 induces 12/15-lipoxygenase expression in murine macrophages and favors their conversion toward a pro-resolving phenotype. Prostaglandins Other Lipid Mediat. 2013 Dec;107:85–94.
  • Lv R, Bao Q, Li Y. Regulation of M1type and M2type macrophage polarization in RAW264.7 cells by Galectin9. Mol Med Rep. 2017 Dec;16(6):9111–9119.
  • Li Y, Komai-Koma M, Gilchrist DS, et al. Galectin-3 is a negative regulator of lipopolysaccharide-mediated inflammation. J Iimmunol. 2008 Aug 15;181(4):2781–2789.
  • Yildirim C, Vogel DY, Hollander MR, et al. Galectin-2 induces a proinflammatory, anti-arteriogenic phenotype in monocytes and macrophages. Plos One. 2015;10(4):e0124347
  • Hong SH, Shin JS, Chung H, et al. Galectin-4 Interaction with CD14 triggers the differentiation of monocytes into macrophage-like cells via the MAPK signaling pathway. Immune Netw. 2019 Jun;19(3):e17
  • Rabinovich GA, Sotomayor CE, Riera CM, et al. Evidence of a role for galectin-1 in acute inflammation. Eur J Immunol. 2000 May;30(5):1331–1339
  • Correa SG, Sotomayor CE, Aoki MP, et al. Opposite effects of galectin-1 on alternative metabolic pathways of L-arginine in resident, inflammatory, and activated macrophages. Glycobiology. 2003 Feb;13(2):119–128
  • Barrionuevo P, Beigier-Bompadre M, Ilarregui JM, et al. A novel function for galectin-1 at the crossroad of innate and adaptive immunity: galectin-1 regulates monocyte/macrophage physiology through a nonapoptotic ERK-Dependent pathway. J Iimmunol. 2007 Jan 1;178(1):436–445.
  • Malik RK, Ghurye RR, Lawrence-Watt DJ, et al. Galectin-1 stimulates monocyte chemotaxis via the p44/42 MAP kinase pathway and a pertussis toxin-sensitive pathway. Glycobiology. 2009 Dec;19(12):1402–1407
  • Sano H, Hsu DK, Yu L, et al. Human galectin-3 is a novel chemoattractant for monocytes and macrophages. J Immunol. 2000 Aug 15;165(4):2156–2164.
  • Jia W, Kidoya H, Yamakawa D, et al. Galectin-3 accelerates M2 macrophage infiltration and angiogenesis in tumors. Am J Pathol. 2013 May;182(5):1821–1831
  • Paclik D, Werner L, Guckelberger O, et al. Galectins distinctively regulate central monocyte and macrophage function. Cell Immunol. 2011;271(1):97–103
  • Kashio Y, Nakamura K, Abedin MJ, et al. Galectin-9 induces apoptosis through the calcium-calpain-caspase-1 pathway. J Immunol. 2003 Apr 1;170(7):3631–3636.
  • Coma M, Frohlichova L, Urban L, et al. Molecular changes underlying hypertrophic scarring following burns involve specific deregulations at all wound healing stages (inflammation, proliferation and maturation). Int J Mol Sci. 2021 Jan 18;22:2.
  • Liu FT, Rabinovich GA. Galectins: regulators of acute and chronic inflammation. Ann N Y Acad Sci. 2010 Jan;1183:158–182.
  • Stowell SR, Qian Y, Karmakar S, et al. Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J Immunol. 2008 Mar 1;180(5):3091–3102.
  • Motran CC, Molinder KM, Liu SD, et al. Galectin-1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function. Eur J Immunol. 2008 Nov;38(11):3015–3027
  • Rabinovich GA, Ramhorst RE, Rubinstein N, et al. Induction of allogenic T-cell hyporesponsiveness by galectin-1-mediated apoptotic and non-apoptotic mechanisms. Cell Death Differ. 2002 Jun;9(6):661–670
  • Norling LV, Sampaio AL, Cooper D, et al. Inhibitory control of endothelial galectin-1 on in vitro and in vivo lymphocyte trafficking. Faseb J. 2008 Mar;22(3):682–690
  • Rabinovich GA, Ariel A, Hershkoviz R, et al. Specific inhibition of T-cell adhesion to extracellular matrix and proinflammatory cytokine secretion by human recombinant galectin-1. Immunology. 1999 May;97(1):100–106
  • Luo Z, Ji Y, Tian D, et al. Galectin-7 promotes proliferation and Th1/2 cells polarization toward Th1 in activated CD4+ T cells by inhibiting The TGFbeta/Smad3 pathway. Mol Immunol. 2018 Sep;101:80–85.
  • Gooden MJ, Wiersma VR, Samplonius DF, et al. Galectin-9 activates and expands human T-helper 1 cells. Plos One. 2013;8(5):e65616
  • Lhuillier C, Barjon C, Niki T, et al. Impact of Exogenous Galectin-9 on Human T Cells: contribution of the t cell receptor complex to antigen-independent activation but not to apoptosis induction. J Biol Chem. 2015 Jul 3;290(27):16797–16811.
  • Zhu C, Anderson AC, Schubart A, et al. The tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol. 2005 Dec;6(12):1245–1252
  • Norambuena A, Metz C, Vicuna L, et al. Galectin-8 induces apoptosis in Jurkat T cells by phosphatidic acid-mediated ERK1/2 activation supported by protein kinase A down-regulation. J Biol Chem. 2009 May 8;284(19):12670–12679.
  • Toscano MA, Bianco GA, Ilarregui JM, et al. Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat Immunol. 2007 Aug 8;8:825–834.
  • Stillman BN, Hsu DK, Pang M, et al. Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol. 2006 Jan 15;176(2):778–789.
  • Nosbaum A, Prevel N, Truong HA, et al. Cutting edge: regulatory T cells facilitate cutaneous wound healing. J Immunol. 2016 Mar 1;196(5):2010–2014.
  • Haertel E, Joshi N, Hiebert P, et al. Regulatory T cells are required for normal and activin-promoted wound repair in mice. Eur J Immunol. 2018 Jun;48(6):1001–1013.
  • Hou XX, Wang XQ, Zhou WJ, et al. Regulatory T cells induce polarization of pro-repair macrophages by secreting sFGL2 into the endometriotic milieu. Commun Biol. 2021 Apr 23;4(1):499.
  • Boothby IC, Cohen JN, Rosenblum MD. Regulatory T cells in skin injury: at the crossroads of tolerance and tissue repair. Sci Immunol. 2020 May 1;5(47):eaaz9631.
  • Garin MI, Chu CC, Golshayan D, et al. Galectin-1: a key effector of regulation mediated by CD4+CD25+ T cells. Blood. 2007 Mar 1;109(5):2058–2065.
  • Fermino ML, Dias FC, Lopes CD, et al. Galectin-3 negatively regulates the frequency and function of CD4(+) CD25(+) Foxp3(+) regulatory T cells and influences the course of Leishmania major infection. Eur J Immunol. 2013 Jul;43(7):1806–1817
  • Wu C, Thalhamer T, Franca RF, et al. Galectin-9-CD44 interaction enhances stability and function of adaptive regulatory T cells. Immunity. 2014 Aug 21;41(2):270–282.
  • Xie RD, Xu LZ, Yang LT, et al. Galectin-1 inhibits oral-intestinal allergy syndrome. Oncotarget. 2017 Feb 21;8(8):13214–13222.
  • Chen HY, Sharma BB, Yu L, et al. Role of galectin-3 in mast cell functions: galectin-3-deficient mast cells exhibit impaired mediator release and defective JNK expression. J Immunol. 2006 Oct 15;177(8):4991–4997.
  • Suzuki Y, Inoue T, Yoshimaru T, et al. Galectin-3 but not galectin-1 induces mast cell death by oxidative stress and mitochondrial permeability transition. Biochim Biophys Acta. 2008 May;1783(5):924–934
  • Kojima R, Ohno T, Iikura M, et al. Galectin-9 enhances cytokine secretion, but suppresses survival and degranulation, in human mast cell line. Plos One. 2014;9(1):e86106
  • Vinish M, Cui W, Stafford E, et al. Dendritic cells modulate burn wound healing by enhancing early proliferation. Wound Repair Regen. 2016 Jan-Feb;24(1):6–13
  • Fulcher JA, Hashimi ST, Levroney EL, et al. Galectin-1-matured human monocyte-derived dendritic cells have enhanced migration through extracellular matrix. J Immunol. 2006 Jul 1;177(1):216–226.
  • Hsu DK, Chernyavsky AI, Chen HY, et al. Endogenous galectin-3 is localized in membrane lipid rafts and regulates migration of dendritic cells. J Invest Dermatol. 2009 Mar;129(3):573–583
  • Hsu YL, Wang MY, Ho LJ, et al. Up-regulation of galectin-9 induces cell migration in human dendritic cells infected with dengue virus. J Cell Mol Med. 2015 May;19(5):1065–1076
  • Dai SY, Nakagawa R, Itoh A, et al. Galectin-9 induces maturation of human monocyte-derived dendritic cells. J Immunol. 2005 Sep 1;175(5):2974–2981.
  • Chen SS, Sun LW, Brickner H, et al. Downregulating galectin-3 inhibits proinflammatory cytokine production by human monocyte-derived dendritic cells via RNA interference. Cell Immunol. 2015 Mar;294(1):44–53
  • Wu SY, Yu JS, Liu FT, et al. Galectin-3 negatively regulates dendritic cell production of IL-23/IL-17-axis cytokines in infection by histoplasma capsulatum. J Iimmunol. 2013 Apr 1;190(7):3427–3437.
  • Cortegano I, Del Pozo V, Cardaba B, et al. Galectin-3 down-regulates IL-5 gene expression on different cell types. J Immunol. 1998 Jul 1;161(1):385–389.
  • Rao SP, Wang Z, Zuberi RI, et al. Galectin-3 functions as an adhesion molecule to support eosinophil rolling and adhesion under conditions of flow. J Immunol. 2007 Dec 1;179(11):7800–7807.
  • Asakura H, Kashio Y, Nakamura K, et al. Selective eosinophil adhesion to fibroblast via IFN-gamma-induced galectin-9. J Immunol. 2002 Nov 15;169(10):5912–5918.
  • Wokalek H, Ruh H. Time course of wound healing. J Biomater Appl. 1991 Apr;5(4):337–362.
  • Tracy LE, Minasian RA, Caterson EJ. Extracellular matrix and dermal fibroblast function in the healing wound. Adv Wound Care (New Rochelle). 2016 Mar 1;5(3):119–136.
  • Chitturi RT, Balasubramaniam AM, Parameswar RA, et al. The role of myofibroblasts in wound healing, contraction and its clinical implications in cleft palate repair. J Int Oral Health. 2015 Mar;7(3):75–80.
  • Li B, Wang JH. Fibroblasts and myofibroblasts in wound healing: force generation and measurement. J Tissue Viability. 2011 Nov;20(4):108–120.
  • Pastar I, Stojadinovic O, Yin NC, et al. Epithelialization in wound healing: a comprehensive review. Adv Wound Care (New Rochelle). 2014 Jul 1;3(7):445–464.
  • Eelen G, Treps L, Li X, et al. Basic and therapeutic aspects of angiogenesis updated. Circ Res. 2020 Jul 3;127(2):310–329.
  • Dvorankova B, Szabo P, Lacina L, et al., Human galectins induce conversion of dermal fibroblasts into myofibroblasts and production of extracellular matrix: potential application in tissue engineering and wound repair. Cells Tissues Organs. 2011. 194(6): 469–480.
  • Lin YT, Chen JS, Wu MH, et al. Galectin-1 accelerates wound healing by regulating the neuropilin-1/Smad3/NOX4 pathway and ROS production in myofibroblasts. J Invest Dermatol. 2015 Jan;135(1):258–268.
  • Fan SM, Tsai CF, Yen CM, et al. Inducing hair follicle neogenesis with secreted proteins enriched in embryonic skin. Biomaterials. 2018 Jun;167:121–131.
  • Cao Z, Said N, Amin S, et al. Galectins-3 and −7, but not galectin-1, play a role in re-epithelialization of wounds. J Biol Chem. 2002 Nov 1;277(44):42299–42305.
  • Liu W, Hsu DK, Chen HY, et al. Galectin-3 regulates intracellular trafficking of EGFR through Alix and promotes keratinocyte migration. J Invest Dermatol. 2012 Dec;132(12):2828–2837
  • Pepe D, Elliott CG, Forbes TL, et al. Detection of galectin-3 and localization of advanced glycation end products (AGE) in human chronic skin wounds. Histol Histopathol. 2014 Feb;29(2):251–258
  • Cho SB, Kim JS, Zheng Z, et al. Decreased tissue and serum expression of galectin-7 in patients with hypertrophic scars. Acta Derm Venereol. 2013 Nov;93(6):669–673
  • Saigusa R, Yamashita T, Miura S, et al. A potential contribution of decreased galectin-7 expression in stratified epithelia to the development of cutaneous and oesophageal manifestations in systemic sclerosis. Exp Dermatol. 2019 May;28(5):536–542
  • Gendronneau G, Sanii S, Dang T, et al. Overexpression of galectin-7 in mouse epidermis leads to loss of cell junctions and defective skin repair. Plos One. 2015;10(3):e0119031
  • Hinz B. The role of myofibroblasts in wound healing. Curr Res Transl Med. 2016 Oct - Dec;64(4):171–177.
  • Vorstandlechner V, Laggner M, Kalinina P, et al. Deciphering the functional heterogeneity of skin fibroblasts using single-cell RNA sequencing. FASEB J. 2020 Mar;34(3):3677–3692
  • Evans RA, Tian YC, Steadman R, et al. TGF-beta1-mediated fibroblast-myofibroblast terminal differentiation-the role of Smad proteins. Exp Cell Res. 2003 Jan 15;282(2):90–100.
  • Kirkpatrick LD, Shupp JW, Smith RD, et al. Galectin-1 production is elevated in hypertrophic scar. Wound Repair Regen. 2021 Jan;29(1):117–128
  • Klingberg F, Hinz B, White ES. The myofibroblast matrix: implications for tissue repair and fibrosis. J Pathol. 2013 Jan;229(2):298–309.
  • Lian N, Li T. Growth factor pathways in hypertrophic scars: molecular pathogenesis and therapeutic implications. Biomed Pharmacother. 2016 Dec;84:42–50.
  • He J, Li X, Luo H, et al. Galectin-3 mediates the pulmonary arterial hypertension–induced right ventricular remodeling through interacting with NADPH oxidase 4. J Am Soc Hypertens. 2017 May;11(5):275–289 e2
  • Luo H, Liu B, Zhao L, et al. Galectin-3 mediates pulmonary vascular remodeling in hypoxia-induced pulmonary arterial hypertension. J Am Soc Hypertens. 2017 Oct;11(10):673–683 e3
  • Gal P, Vasilenko T, Kovac I, et al. Human galectin3: molecular switch of gene expression in dermal fibroblasts in vitro and of skin collagen organization in open wounds and tensile strength in incisions in vivo. Mol Med Rep. 2021 Feb;23(2):99.
  • Huang CY, Hsieh PL, Ng MY, et al. Galectin-7 promotes proliferation and wound healing capacities in periodontal ligament fibroblasts by activating ERK signaling. J Formos Med Assoc. 2021 Aug;121(5):1008–1011.
  • Zhao Y, Zhao S, Li H, et al. Expression of galectin-7 in vulvar lichen sclerosus and its effect on dermal fibroblasts. Oncol Lett. 2018 Aug;16(2):2559–2564
  • Smith PC, Metz C, de la Pena A, et al. Galectin-8 mediates fibrogenesis induced by cyclosporine in human gingival fibroblasts. J Periodontal Res. 2020 Oct;55(5):724–733
  • Mahabeleshwar GH, Feng W, Reddy K, et al. Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ Res. 2007 Sep 14;101(6):570–580.
  • Goel HL, Mercurio AM. Enhancing integrin function by VEGF/neuropilin signaling: implications for tumor biology. Cell Adh Migr. 2012 Nov-Dec;6(6):554–560.
  • Shimizu A, Zankov DP, Kurokawa-Seo M, et al. Vascular endothelial growth factor-a exerts diverse cellular effects via small g proteins, rho and rap. Int J Mol Sci. 2018 16 Apr; 19(4)
  • Barleon B, Sozzani S, Zhou D, et al. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood. 1996 Apr 15;87(8):3336–3343.
  • Hsieh SH, Ying NW, Wu MH, et al. Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene. 2008 Jun 12;27(26):3746–3753.
  • van Beijnum JR, Thijssen VL, Lappchen T, et al. A key role for galectin-1 in sprouting angiogenesis revealed by novel rationally designed antibodies. Int J Cancer. 2016 Aug 15;139(4):824–835.
  • Thijssen VL, Postel R, Brandwijk RJ, et al. Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci U S A. 2006 Oct 24;103(43):15975–15980.
  • Thijssen VL. Galectins in endothelial cell biology and angiogenesis: the basics. Biomolecules. 2021 Sep 20;11(9):1386.
  • Jouve N, Despoix N, Espeli M, et al. The involvement of CD146 and its novel ligand Galectin-1 in apoptotic regulation of endothelial cells. J Biol Chem. 2013 Jan 25;288(4):2571–2579.
  • Markowska AI, Liu FT, Panjwani N. Galectin-3 is an important mediator of VEGF- and bFGF-mediated angiogenic response. J Exp Med. 2010 Aug 30;207(9):1981–1993.
  • Markowska AI, Jefferies KC, Panjwani N. Galectin-3 protein modulates cell surface expression and activation of vascular endothelial growth factor receptor 2 in human endothelial cells. J Biol Chem. 2011 Aug 26;286(34):29913–29921.
  • D’Haene N, Sauvage S, Maris C, et al. VEGFR1 and VEGFR2 involvement in extracellular galectin-1- and galectin-3-induced angiogenesis. Plos One. 2013;8(6):e67029
  • Dos Santos SN, Sheldon H, Pereira JX, et al. Galectin-3 acts as an angiogenic switch to induce tumor angiogenesis via Jagged-1/Notch activation. Oncotarget. 2017 Jul 25;8(30):49484–49501.
  • Zhang L, Li YM, Zeng XX, et al. Galectin-3- mediated transdifferentiation of pulmonary artery endothelial cells contributes to hypoxic pulmonary vascular remodeling. Cell Physiol Biochem. 2018;51(2):763–777
  • Sedlar A, Travnickova M, Bojarova P, et al. Interaction between galectin-3 and integrins mediates cell-matrix adhesion in endothelial cells and mesenchymal stem cells. Int J Mol Sci. 2021 May 13;22:10.
  • Fukushi J, Makagiansar IT, Stallcup WB. NG2 proteoglycan promotes endothelial cell motility and angiogenesis via engagement of galectin-3 and alpha3beta1 integrin. Mol Biol Cell. 2004 Aug;15(8):3580–3590.
  • Walker JT, Elliott CG, Forbes TL, et al. Genetic deletion of galectin-3 does not impair full-thickness excisional skin healing. J Invest Dermatol. 2016 May;136(5):1042–1050.
  • Cueni LN, Detmar M. Galectin-8 interacts with podoplanin and modulates lymphatic endothelial cell functions. Exp Cell Res. 2009 Jun 10;315(10):1715–1723.
  • Varinska L, Faber L, Petrovova E, et al. Galectin-8 favors VEGF-induced angiogenesis: in vitro study in human umbilical vein endothelial cells and in vivo study in chick chorioallantoic membrane. Anticancer Res. 2020 Jun;40(6):3191–3201
  • Zamorano P, Koning T, Oyanadel C, et al. Galectin-8 induces endothelial hyperpermeability through the eNOS pathway involving S-nitrosylation-mediated adherens junction disassembly. Carcinogenesis. 2019 Feb;40(2):313–323
  • Aanhane E, Schulkens IA, Heusschen R, et al. Different angioregulatory activity of monovalent galectin-9 isoforms. Angiogenesis. 2018 Aug;21(3):545–555
  • Koshizuka S, Kanazawa K, Kobayashi N, et al. The beneficial effects of recombinant human insulin-like growth factor-I (IGF-I) on wound healing in severely wounded senescent mice. Surg Today. 1997;27(10):946–952
  • Tortelli F, Pisano M, Briquez PS, et al. Fibronectin binding modulates CXCL11 activity and facilitates wound healing. PLoS One. 2013;8(10):e79610
  • Sugiyama K, Ishii G, Ochiai A, et al. Improvement of the breaking strength of wound by combined treatment with recombinant human G-CSF, recombinant human M-CSF, and a TGF-beta1 receptor kinase inhibitor in rat skin. Cancer Sci. 2008 May;99(5):1021–1028
  • Filer A, Bik M, Parsonage GN, et al. Galectin 3 induces a distinctive pattern of cytokine and chemokine production in rheumatoid synovial fibroblasts via selective signaling pathways. Arthritis Rheum. 2009 Jun;60(6):1604–1614
  • Toegel S, Weinmann D, Andre S, et al. Galectin-1 couples glycobiology to inflammation in osteoarthritis through the activation of an NF-kappaB-regulated gene network. J Immunol. 2016 Feb 15;196(4):1910–1921.
  • Weinmann D, Schlangen K, Andre S, et al. Galectin-3 induces a pro-degradative/inflammatory gene signature in human chondrocytes, teaming up with galectin-1 in osteoarthritis pathogenesis. Sci Rep. 2016 Dec 16;6:39112.
  • Ochieng J, Fridman R, Nangia-Makker P, et al. Galectin-3 is a novel substrate for human matrix metalloproteinases-2 and −9. Biochemistry. 1994 Nov 29;33(47):14109–14114.
  • Sundqvist M, Welin A, Elmwall J, et al. Galectin-3 type-C self-association on neutrophil surfaces; The carbohydrate recognition domain regulates cell function. J Leukoc Biol. 2018 Feb;103(2):341–353
  • Kim MH, Wu WH, Choi JH, et al. Galectin-1 from conditioned medium of three-dimensional culture of adipose-derived stem cells accelerates migration and proliferation of human keratinocytes and fibroblasts. Wound Repair Regen. 2018 Dec;26(Suppl 1):S9–S18
  • Begley CG, Ellis LM. Drug development: raise standards for preclinical cancer research. Nature. 2012 Mar 28;483(7391):531–533.
  • Gan HK, You B, Pond GR, et al. Assumptions of expected benefits in randomized phase iii trials evaluating systemic treatments for cancer. J Natl Cancer I. 2012 Apr;104(8):590–598
  • Henderson NC, Mackinnon AC, Farnworth SL, et al. Galectin-3 regulates myofibroblast activation and hepatic fibrosis. Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):5060–5065.
  • Wang L, Friess H, Zhu Z, et al. Galectin-1 and galectin-3 in chronic pancreatitis. Lab Invest. 2000 Aug;80(8):1233–1241
  • Henderson NC, Mackinnon AC, Farnworth SL, et al. Galectin-3 expression and secretion links macrophages to the promotion of renal fibrosis. Am J Pathol. 2008 Feb;172(2):288–298
  • Gittens BR, Bodkin JV, Nourshargh S, et al. Galectin-3: a positive regulator of leukocyte recruitment in the inflamed microcirculation. J Immunol. 2017 Jun 1;198(11):4458–4469.
  • Stowell SR, Arthur CM, Mehta P, et al. Galectin-1, −2, and −3 exhibit differential recognition of sialylated glycans and blood group antigens. J Biol Chem. 2008 Apr 11;283(15):10109–10123.
  • Su EW, Bi S, Kane LP. Galectin-9 regulates T helper cell function independently of Tim-3. Glycobiology. 2011 Oct;21(10):1258–1265.
  • Kopitz J, von Reitzenstein C, Andre S, et al. Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of galectin-1 and functional divergence from galectin-3. J Biol Chem. 2001 Sep 21;276(38):35917–35923.
  • Kopitz J, Xiao Q, Ludwig AK, et al. Reaction of a programmable glycan presentation of glycodendrimersomes and cells with engineered human lectins to show the sugar functionality of the cell surface. Angew Chem Int Ed Engl. 2017 Nov 13;56(46):14677–14681.
  • Ludwig AK, Michalak M, Xiao Q, et al. Design-functionality relationships for adhesion/growth-regulatory galectins. Proc Natl Acad Sci U S A. 2019 Feb 19;116(8):2837–2842.
  • Tasumi S, Vasta GR. A galectin of unique domain organization from hemocytes of the Eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus. J Immunol. 2007 Sep 1;179(5):3086–3098.
  • Vasta GR, Feng C, Bianchet MA, et al. Structural, functional, and evolutionary aspects of galectins in aquatic mollusks: from a sweet tooth to the Trojan horse. Fish Shellfish Immunol. 2015 Sep;46(1):94–106
  • Antonopoulos A, North SJ, Haslam SM, et al. Glycosylation of mouse and human immune cells: insights emerging from N-glycomics analyses. Biochem Soc Trans. 2011 Oct;39(5):1334–1340
  • Amano M, Hashimoto R, Nishimura SI. Effects of single genetic damage in carbohydrate-recognizing proteins in mouse serum N-glycan profile revealed by simple glycotyping analysis. Chembiochem. 2012 Feb 13;13(3):451–464.
  • Smetana K, Andre S, Kaltner H, et al. Context-dependent multifunctionality of galectin-1: a challenge for defining the lectin as therapeutic target. Expert Opin Ther Tar. 2013 Apr;17(4):379–392

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.