Basic biological roles of galectins in tissue repair and tumor growth

1. Ashcroft GS, et al. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest 2003; 111: 1309–1318.

2. Korkaya H, et al. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J Clin Invest 2011; 121: 3804–3809.

3. Scatena R, et al. Cancer stem cells: the development of new cancer therapeutics. Expert Opin Biol Ther 2011; 11: 875–892.

4. Motlík J, et al. Porcine epidermal stem cells as a biomedical model for wound healing and normal/malignant epithelial cell propagation. Theriogenology 2007; 67: 105–111.

5. Strnad H, et al. Head and neck squamous cancer stromal fibroblasts produce growth factors influencing phenotype of normal human keratinocytes. Histochem Cell Biol 2010; 133: 201–211.

6. Plzák J, et al. Epithelial-stromal interaction in squamous cell epithelium-derived tumors: an important new player in the control of tumor biological properties. Anticancer Res 2010; 30: 455–462.

7. Dvořánková B, 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: 469–480.

8. Valach J, et al. Smooth muscle actin-expressing stromal fibroblasts in head and neck squamous cell carcinoma: increased expression of galectin-1 and induction of poor prognosis factors. Int J Cancer 2012; 131: 2499–2508.

9. Gendronneau G, et al. Galectin-7 in the control of epidermal homeostasis after injury. Mol Biol Cell 2008; 19: 5541–5549.

10. Teichberg A, et al. beta-D-galactoside binding protein from electric organ tissue of Electrophorus electricus. Proc Natl Acad Sci USA 1975 72: 1383–1387.

11. Leffler H, et al. Introduction to galectins. Glycoconj J 2004; 19: 433–440.

12. Hirabayashi J, et al. The family of metazoan metal-independent beta-galactoside-binding lectins: Structure, functions and molecular evolution. Glycobiology 1993; 3: 297–304.

13. Cummings RD, et al. Galectins. Essentials of Glycobiology. 2nd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2009. Chapter 33.

14. Hsu DK, et al. Regeneration of cellular homeostasis by galectins. Glycoconj J 2004; 19: 507–515.

15. Liu FT, et al. Intracellular functions of galectins. Biochem Biophys Acta 2002; 1572: 263–273.

16. Hughe RC, et al. Galectins as modulators of cell adhesion. Biochemie 2001; 83: 667–676.

17. Sano H, et al. Human galectin-3 is a novel chemoattractant for monocytes and macrophages. J Immunol 2000; 165: 2156–2164.

18. Hsu DK, et al. Galectins in apoptosis. Methods Enzymol 2006; 417: 256–273.

19. Sato S, et al. Seeing strangers or annoucing „danger“: Galectin-3 in two models of innate imunity. Glycoconj J 2004; 19: 583–591.

20. Van den Brule F, et al. Expression of galectins in cancer. Glycoconj J 2004; 19: 537–542.

21. Yang RY, et al. Galectins: structure, function and therapeutic potential. Expert Rev Mol Med 2008; 10: e17.

22. Camby I, et al. Galectin-1: a small protein with major functions. Glycobiology 2006; 16: 137–157.

23. Thijssen VL, et al. Galectins in the tumor endothelium: opportunities for combined cancer therapy. Blood 2007; 110: 2819–2827.

24. Thijssen VL, et al. Tumor cells secrete galectin-1 to enhance endothelial cell activity. Cancer Res 2010 70: 6216–6224.

25. Klíma J, et al. Differential regulation of galectin expression/ reactivity during wound healing in porcine skin and in cultures of epidermal cells with functional impact on migration. Physiol Res 2009; 58: 873–884.

26. Gál P, et al. Open wound healing in vivo: monitoring binding and presence of adhesion/growth-regulatory galectins in rat skin during the course of complete re-epithelialization. Acta Histochem Cytochem 2011 44: 191–199.

27. Rabinovich GA, et al. Specific inhibition of T cell adhesion to extracellular matrix a proinflammatory cytokine secretion by human recombinant galectin-1. Imunology 1999; 97: 100–106.

28. Van der Leij J, et al. Dimeric galectin-1 induces IL-10 production in T-lymphocytes, an important tool in the regulation of the immune response. J Pathol 2004; 204: 511–518.

29. Rabinovich GA, et al. Recombinant galectin-1 and its genetic delivery suppress collagen-induced via T cell apoptosis. J Exp Med 1999; 190: 385–398.

30. Santucci L, et al. Galectin-1 suppresses experimental collitis in mice. Gastroenterology 2003; 124: 1381–1394.

31. Wang L, et al. Galectin-1 and galectin-3 in chronic pancreatitis. Lab Invest 2000; 80: 1233–1241.

32. Adams L, et al. Biphasic modulation of cell growth by recombinant human galectin-1. Biochim Biophys Acta 1996; 1312: 137–144.

33. André S, et al. Tumor suppressor p16INK4a-modulator of glycomic profile and galectin-1 expression to increase susceptibility to carbohydrate-dependent induction of anoikis in pancreatic carcinoma cells. FEBS J 2007; 274: 3233–3256.

34. Rabien A, et al. Tumor suppressor p16INK4a controls oncogenic K-Ras function in human pancreatic cancer cells. Cancer Sci 2012; 103: 169–175.

35. Miura T, et al. Galectin-1beta, a natural monomeric form of galectin-1 lacking its six amino- terminal residues promotes axonal regeneration but not cell death. Cell Death Differ 2004; 11: 1076–1083.

36. Saussez S, et al. Increased expression and altered intracellular distribution of adhesion/growth-regulatory lectins galectins-1 and -7 during tumour progression in hypopharyngeal and laryngeal squamous cell carcinomas. Histopathology 2008; 52: 483–493.

37. Saussez S, et al. Adhesion/growth-regulatory tissue lectin galectin-1 in relation to angiogenesis/lymphocyte infiltration and prognostic relevance of stromal up-regulation in laryngeal carcinomas. Anticancer Res 2009; 29: 59–65.

38. Hsieh SH, et al. Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene. 2008; 27: 3746–3753.

39. D’Haene N, et al. VEGFR1 and VEGFR2 involvement in extracellular galectin-1- and galectin-3-induced angiogenesis. PLoS One 2013; 8: e67029.

40. Ito K, et al. Thiodigalactoside inhibits murine cancers by concurrently blocking effects of galectin-1 on immune dysregulation, angiogenesis and protection against oxidative stress. Angiogenesis 2011 14: 293–307.

41. Thijssen VL, et al. The galectin profile of the endothelium: altered expression and localization in activated and tumor endothelial cells. Am J Pathol. 2008; 172: 545–553.

42. Clausse N, et al. Galectin-1 expression in prostate tumor-associated capillary endothelial cells is increased by prostate carcinoma cells and modulates heterotypic cell-cell adhesion. Angiogenesis 1999; 3: 317–325.

43. Laderach DJ et al. A unique galectin signature in human prostate cancer progression suggests galectin-1 as a key target for treatment of advanced disease. Cancer Res 2013; 73: 86–96.

44. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005; 5: 263–274.

45. Smetana K, et al. Phylogeny, regeneration, ageing and cancer: role of microenvironment and possibility of its therapeutic manipulation. Folia Biol (Praha) 2012; 59: 207–216.

46. Paclik D, et al. Galectin-2 induces apoptosis of lamina propria T- lymphocytes and a meliorates acute and chronic experimental colitis in mice. J Mol Med (Berl) 2008; 86: 1395–1406.

47. Paclik D, et al. Galectin-2 and -4, but not galectin-1, promote intestinal epithelial wound healing in vitro through a TGF-β-independent mechanism. Inflamm Bowel Dis 2008; 14: 1366–1372.

48. Dvořánková B, et al. Human galectin-2: nuclear presence in vitro and its modulation by quiescence/stress factors. Histol Histopathol 2008; 23: 167–168.

49. Magnaldo T, et al. Galectin-7, a marker of all types of stratified epithelia. Differentiation 1998; 63: 159–168.

50. Saussez S, et al. Galectin-7. Cell Mol Life Sci 2006; 63: 686–697.

51. Cao Z, et al. Galectin-7 as a potential mediator of corneal epitelial cell migration. Arch Ophthalmol 2003; 121: 82–86.

52. Sato M, et al. Quantification of galectin-7 and its localization in adult mouse tissues. J Biochem 2002; 131: 255–260.

53. Polyak K, et al. A Model for p53 – induced apoptosis. Nature 1997; 389: 300–305.

54. Čada Z, et al. Galectin-7: will the lectin’s activity establish clinical correlations in head and neck squamous cell and basal cell carcinomas? Histol Histopathol 2009; 21: 44–48.

55. Barrés C, et al. Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood 2010; 115: 696–705.

56. Rapoport EM, et al. Mammalian galectins: structure, carbohydrate specifity, and functions. Biochemistry 2008; 73: 393–405.

57. Boronkai A, et al. Potentiation of paclitaxel- induced apoptosis by galectin-13 overexpression via activation of Ask-1-p38-MAP kinase and JNK/SAPK pathways and suppression of Akt and ERK ½ activation in U-937 human macrophage cells. J Cell Biology 2009; 89: 753–763.

58. Young AR, et al. Functional charakterization of an eosinophil – specific galectin, ovine galectin-14. Glycoconj J 2009; 26: 423–432.

59. Gray CA, et al. Discovery and charakterization of an epithelial specific galectin in the endometrium that forms crystals in the trophectoderm. Proc Natl Acad Sci USA 2004; 101: 7982–7987.

60. Grendel T, et al. Early stages of trachea healing process: (immuno/lectin) histochemical monitoring of selected markers and adhesion/growth-regulatory endogenous lectins. Folia Biol (Praha) 2012; 58: 135–143.

61. Cao Z, et al. Galectins-3 and -7, but not galectin-1, play a role in re-epitelialization of wounds. J Biol Chem 2002; 277: 42299–42305.

62. Maeda N, et al. Stimulation of proliferation of rat hepatic stellare cells by galectin-1 and -3 through different intracellular signalling pathways. J Biol Chem 2003; 278: 18938–18944.

63. Matarrese P, et al. Galectin-3 overexpression protects from apoptosis by improving cell adhesion properties. Int J Cancer 2000; 85: 545–554.

64. Henderson NC, et al. Galectin-3 regulates myofibroblasts activation and hepatic fibrosis. Proc Natl Acad Sci USA 2006; 103: 5060–5065.

65. Henderson NC, et al. Galectin-3 expression and secretion links macrophages to the promotion of renal fibrosis. Am J Pathol 2008; 172: 288–298.

66. de Boer RA, et al. Galectin-3: a novel mediator of heart failure development and progression. Eur J Heart Fail 2009; 11: 811–817.

67. Kasper M, et al. Immunohistochemical evidence for the occurence of similar epitelial phenotypes during lung development and radiation-induced fibrogenesis. Int J Radiat Biol 2000; 76: 493–501.

68. Zuberi RI, et al. Activation of rat basophillic leukemia cells by epsilon BP, an IgE- binding endogenous lectin. Cell Immunol 1994; 156: 1–12.

69. Sano H, et al. Critical role of galectin-3 in phagocytosis by macrophages. J Clin Invest 2003; 112: 389–397.

70. Almkvist J, et al. Activation of the neutrophil nicotinamide adenine dinucleotide phosphate oxidaze by galectin-1. J Immunol 2002; 168: 4034–4041.

71. Kuwabara I, et al. Galectin-3 promotes adhesion of human neutrophils to laminin. J Immunol 1996; 156: 3939–3944.

72. Sato S, et al. Role of galectin-3 as an adhesion molecule for neutrophil extravasation during streptococal pneumonia. J Immunol 2002; 168: 1813–1822.

73. Fernández GC, et al. Galectin-3 and soluble fibrinogen act in concert to modulate neutrophil activation and survival. Involvement of alternative MAPK-pathways. Glycobiology 2005; 15: 519–527.

74. Yang RY, et al. Expression of galectin-3 modulates T-cells grouth and apoptosis. Proc Nath Acad Sci USA 1996; 93: 6737–6742.

75. Fukumori T, et al. CD29 and CD7 mediate galectin-3-induced type II T-cell apoptosis. Cancer Res 2003; 63: 8302–8311.

76. Markowska AI, et al. Galectin-3 is an important mediator of VEGF- and bFGF-mediated angiogenic response. J Exp Med 2010; 207: 1981–1993.

77. Nangia-Makker P, et al. Galectin-3 induces endothelial cell morphogenesis and angiogenesis. Am J Pathol 2000; 156: 899–909.

78. van der Velde AR, at al. Prognostic value of changes in galectin-3 levels over time in patients with heart failure: data from CORONA and COACH. Circ Heart Fail 2013; 6: 219–226.

79. Motiwala SR, et al. Serial measurement of galectin-3 in patients with chronic heart failure: results from the ProBNP Outpatient Tailored Chronic Heart Failure Therapy (PROTECT) study. Eur J Heart Fail. 2013; 15: 1157–1163.

80. Luecke N, et al. Secreted proteome of the murine multipotent hematopoietic progenitor cell line DKmix. Rapid Commun Mass Spectrom 2010; 24: 561–570.

81. Hrynchysyn N, et al. Galectin-3: a new biomarker for the diagnosis, analysis and prognosis of acute and chronic heart failure. Arch Cardiovasc Dis 2013; 106: 541–546.

82. Huflejt ME, et al. Galectin-4 in normal tissues and cancer. Glycoconj J 2003; 20: 247–255.

83. Rapoport EM, et al. Mammalian galectins: structure, carbohydrate specificity, and functions. Biochemistry (Mosc) 2008; 73: 393–405.

84. Hadari YR, et al. Galectin-8 binding to integrins inhibits cell adhesion and induces apoptosis. J Cell Sci 2000; 113: 2385–2397.

85. Nishi N, et al. Galectin-8 modulates neutrophil function via interaction with integrin alphaM. Glycobiology 2003; 13: 755–763.

86. Matsumoto R, et al. Biological activities of ecalectin: a novel eosinophil-activating factor. J Immunol 2002; 168: 1961–1967.

87. Rabinovich GA, et al. Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease. Parasite Immunology 2005; 27: 103–114.

88. Kageshita T, et al. Possible role of galectin-9 in cell aggregation and apoptosis of human melanoma cell lines and its clinical significance. Int J Cancer 2002; 99: 809–816.

89. Delgado VM, et al. Modulation of endothelial cell migration and angiogenesis: a novel function for the „tandem-repeat“ lectin galectin-8. FASEB J 2011; 25: 242–254.

90. Fík Z, et al. Loss of adhesion/growth-regulatory galectin-9 from squamous cell epithelium in head and neck carcinomas. J Oral Pathol Med 2013; 42: 166–173.

91. Hotta K, et al. Galectin-12, an adipose- expressed galectin- like molecule possessing apoptosis-inducing activity. J Biol Chem 2001; 276: 34089–34097.

92. Dvorak HF, et al. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986; 315: 1650–1659.

93. Kolar M, et al. Upregulation of IL-6, IL-8 and CXCL-1 production in dermal fibroblasts by normal/malignant epithelial cells in vitro: Immunohistochemical and transcriptomic analyses. Biol Cell 2012; 104: 738–751.