Identification and consequences of galectin-3 expression in pituitary tumors

Molecular and Cellular Endocrinology

Volumn 326, Issue 1-2, 2010, Pages 8-14

  Righi, A ^a,b   Jin, L ^a   Zhang, S ^a   Stilling, G ^a   Scheithauer, B W ^a   Kovacs, K ^c   Lloyd, R V ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF TURIN   (Italy)

^c ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

ACTH adenoma; Folliculo stellate cells; Galectin 3; Pituitary; PRL adenoma; Tumor

Indexed keywords

GALECTIN 3; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA1;

CANCER GROWTH; CANCER INVASION; CARCINOGENESIS; CELL CYCLE REGULATION; CYTOSKELETON; GENE FUNCTION; GENE OVEREXPRESSION; HUMAN; HYPOPHYSIS TUMOR; METASTASIS POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; APOPTOSIS; CARCINOMA; CORE BINDING FACTOR ALPHA 1 SUBUNIT; CORE BINDING FACTOR ALPHA 2 SUBUNIT; GALECTIN 3; HUMANS; METHYLATION; MICE; PITUITARY GLAND; PITUITARY NEOPLASMS;

EID: 77955427083     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.04.026     Document Type: Review

References (94)

1. Ahmad N., Gabius H.J., Sabesan S., Oscarson S., Brewer C.F. Thermodynamic binding studies of bivalent oligosaccharides to galectin-1, galectin-3, and the carbohydrate recognition domain of galectin-3. Glycobiology 2004, 14(9):817-825.
2. Akahani S., Nangia-Makker P., Inohara H., Kim H.R., Raz A. Galectin-3: a novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res. 1997, 57(23):5272-5276.
3. Amado M., Almeida R., Schwientek T., Clausen H. Identification and characterization of large galactosyl-transferase gene families: galactosyltransferases for all functions. Biochem. Biophys. Acta 1999, 1473(1):35-53.
4. Arar C., Gaudin J.C., Capron L., Legrand A. Galectin-3 gene (LGALS3) expression in experimental atherosclerosis and cultured smooth muscle cells. FEBS Lett. 1998, 430(3):307-311.
5. Barnes G.L., Hebert K.E., Kamal M., Javed A., Einhorn T.A., Lian J.B., et al. Fidelity of Runx2 activity in breast cancer cells is required for the generation of metastases associated osteolytic disease. Cancer Res. 2004, 64(13):4506-4513.
6. Bao Q., Hughes R.C. Galectin-3 expression and effects on cyst enlargement and tubulogenesis in kidney epithelial MDCK cells cultured in three-dimensional matrices in vitro. J. Cell Sci. 1995, 108(Pt 8):2791-2800.
7. Barondes S.H., Castronovo V., Cooper D.N., Cummings R.D., Drickamer K., Feizi T., et al. Galectins: a family of animal β-galactoside-binding lectins. Cell 1994, 76(4):597-598.
8. Bartolazzi A., Orlandi F., Saggiorato E., Volante M., Arecco F., Rossetto R., et al. Galectin-3-expression analysis in the surgical selection of follicular thyroid nodules with indeterminate fine-needle aspiration cytology: a prospective multicentre study. Lancet Oncol. 2008, 9(6):543-549.
9. Bergero N., De Pompa R., Sacerdote C., Gasparri G., Volante M., Bussolati G., et al. Galectin-3 expression in parathyroid carcinoma: immunohistochemical study of 26 cases. Hum. Pathol. 2005, 36(8):908-914.
10. Bresalier R.S., Mazurek N., Sternberg L.R., Byrd J.C., Yunker C.K., Nangia-Makker P., et al. Metastasis of human colon cancer is altered by modifying expression of the beta-galactoside-binding protein galectin-3. Gastroenterology 1998, 115(2):287-296.
11. Cai W.Y., Alexander J.M., Hedley-Whyte E.T., Scheithauer B.W., Jameson J.L., et al. Ras mutations in human prolactinomas and pituitary carcinomas. J. Clin. Endocrinol. Metab. 1994, 78(1):89-93.
12. Cameron E.R., Neil J.C. The Runx genes: lineage-specific oncogenes and tumor suppressors. Oncogene 2004, 23(24):4308-4314.
13. Cerra R.F., Gitt M.A., Barondes S.H. Three soluble rat beta galactoside binding lectins. J. Biol. Chem. 1985, 260(19):10474-10477.
14. Costessi A., Pines A., D'Andrea P., Romanello M., Damante G., Cesaratto L., et al. Extracellular nucleotides activate Runx2 in the osteoblast-like HOBIT cell line: a possible molecular link between mechanical stress and osteoblasts' response. Bone 2005, 36(3):418-432.
15. Danguy A., Camby I., Kiss R. Galectins and cancer. Biochim. Biophys. Acta 2002, 1572(2-3):285-293.
16. Davidson P.J., Li S.Y., Lohse A.G., Vandergaast R., Verde E., Pearson A., et al. Transport of galectin-3 between the nucleus and cytoplasm. I. Conditions and signals for nuclear import. Glycobiology 2006, 16(7):602-611.
17. Ducy P., Schinke T., Karsenty G. The osteoblast: a sophisticated fibroblast under central surveillance. Science 2000, 289(5484):1501-1504.
18. Durst K.L., Hiebert S.W. Role of RUNX family members in transcriptional repression and gene silencing. Oncogene 2004, 23(24):4220-4224.
19. Ezzat S., Mader R., Fischer S., Yu S., Ackerley C., Asa S.L. An essential role for the hematopoietic transcription factor Ikaros in hypothalamic-pituitary-mediated somatic growth. Proc. Natl. Acad. Sci. U.S.A. 2006, 103(7):2214-2219.
20. Ezzat S., Asa S.L. Mechanisms of disease: the pathogenesis of pituitary tumors. Nat. Clin. Pract. Endocrinol. Metab. 2006, 2(4):220-230.
21. Ezzat S., Yu S., Asa S.L. Ikaros isoforms in human pituitary tumors: distinct localization, histone acetylation, and activation of the 5_fibroblast growth factor receptor-4 promoter. Am. J. Pathol. 2003, 163(3):1177-1184.
22. Ezzat S., Yu S., Asa S.L. The zinc finger Ikaros transcription factor regulates pituitary growth hormone and prolactin gene expression through distinct effects on chromatin accessibility. Mol. Endocrinol. 2005, 19(4):1004-1111.
23. Ezzat S., Zhu X., Loeper S., Fischer S., Asa S.L. Tumor-derived Ikaros 6 acetylates the Bcl-XL promoter to up-regulate a survival signal in pituitary cells. Mol. Endocrinol. 2006, 20(11):2976-2986.
24. Farrell W.E., Clayton R.N. Epigenetic change in pituitary tumorigenesis. Endocr. Relat. Cancer 2003, 10(2):323-330.
25. Fero M.L., Rivkin M., Tasch M., Porter P., Carow C.E., Firpo E., et al. A syndrome of multi-organ hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27kip1-deficient mice. Cell 1996, 85(5):733-744.
26. Gicquel C., LeBouc Y., Luton J.-P., Girad F., Bertagna X. Monoclonality of corticotroph macroadenomas in Cushing's disease. J. Clin. Endocrinol. Metab. 1992, 75(2):472-475.
27. Goetz J.G. Bidirectional control of the inner dynamics of focal adhesions promotes cell migration. Cell Adhes. Migr. 2009, 3(2):185-190.
28. Hirabayashi J., Kasai K. The family of metazoan metal-independent beta-galactoside-binding lectins: structure, function and molecular evolution. Glycobiology 1993, 3(4):297-304.
29. Ho M.K., Springer T.A. Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies. J. Immunol. 1982, 128(3):1221-1228.
30. Hrdlickova-Cela E., Plzak J., Smetana K., Melkova Z., Kaltner H., Filipec M., et al. Detection of galectin-3 in tear fluid at disease states and immunohistochemical and lectin histochemical analysis in human corneal and conjunctival epithelium. Br. J. Ophthalmol. 2001, 85(11):1336-1340.
31. Huflejt M.E., Turck C.W., Lindstedt R., Barondes S.H., Leffler H. L-29, a soluble lactose-binding lectin, is phosphorylated on serine 6 and serine 12 in vivo and by casein kinase I. J. Biol. Chem. 1993, 268(35):26712-26718.
32. Inoue K., Ozaki S., Shiga T., Ito K., Masuda T., Okado N., et al. Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. Nat. Neurosci. 2002, 5(10):946-954.
33. Jin L., Qian X., Kulig E., Sanno N., Scheithauer B.W., Kovacs K., et al. Transforming growth factor-β, transforming growth factor-β receptor II and p27kip1 expression in nontumorous and neoplastic human pituitaries. Am. J. Pathol. 1997, 151(2):509-519.
34. Jin L., Riss D., Ruebel K., Kajita S., Scheithauer B.W., Horvath E., et al. Galectin-3 expression in functioning and silent ACTH-producing adenomas. Endocr. Pathol. 2005, 16(2):107-114.
35. Jin L., Kulig E.J., Qian X., Scheithauer B.W., Eberhardt N.L., Lloyd R.V. A human pituitary adenoma cell line proliferates and maintains some differentiated functions following expression of SV40 large T-antigen. Endocr. Pathol. 1998, 9(2):169-184.
36. Kadrofske M.M., Openo K.P., Wang J.L. The human LGALS3 (galectin-3) gene: determination of the gene structure and functional characterization of the promoter. Arch. Biochem. Biophys. 1998, 349(1):7-20.
37. Karga H.J., Alexander J.M., Hedley-Whyte E.T., Klibanski A., Jameson J.L. Ras mutations in human pituitary tumors. J. Clin. Endocrinol. Metab. 1992, 74(4):914-919.
38. Kasper M., Hughes R.C. Immunocytochemical evidence for a modulation of galectin 3 (Mac-2), a carbohydrate binding protein, in pulmonary fibrosis. J. Pathol. 1996, 179(3):309-316.
39. Kim H.R., Lin H.M., Biliran H., Raz A. Cell cycle arrest and inhibition of anoikis by galectin-3 in human breast epithelial cells. Cancer Res. 1999, 59(16):4148-4154.
40. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89(5):755-764.
41. Kramer M.W., Kuczyk M.A., Hennenlotter J., Serth J., Schilling D., Stenzl A., et al. Decreased expression of galectin-3 predicts tumour recurrence in pTa bladder cancer. Oncol. Rep. 2008, 20(6):1403-1408.
42. Lefranc F., Chevalier C., Vinchon M., Dhellemmes P., Schüring M.P., Kaltner H., et al. Characterization of the levels of expression of retinoic acid receptors, galectin-3, macrophage migration inhibiting factor, and p53 in 51 adamantinomatous craniopharyngiomas. J. Neurosurg. 2003, 98(1):145-153.
43. Li S.Y., Davidson P.J., Lin N.Y., Patterson R.J., Wang J.L., Arnoys E.J. Transport of galectin-3 between the nucleus and cytoplasm. II. Identification of the signal for nuclear export. Glycobiology 2006, 16(7):612-622.
44. Lin H.M., Moon B.K., Yu F., Kim H.R. Galectin-3 mediates genistein-induced G2/M arrest and inhibits apoptosis. Carcinogenesis 2000, 21(11):1941-1945.
45. Liu F.T., Rabinovich G.A. Galectins as modulators of tumour progression. Nat. Rev. Cancer 2005, 5(1):29-41.
46. Liu F.T. Regulatory roles of galectins in the immune response. Int. Arch. Allergy Immunol. 2005, 136(4):385-400.
47. Liu F.T., Orida N. Synthesis of surface immunoglobulin E receptor in Xenopus oocytes by translation of mRNA from rat basophilic leukemia cells. J. Biol. Chem. 1984, 259(17):10649-10652.
48. Lloyd R.V. Molecular pathology of pituitary adenomas. J. Neurooncol. 2001, 54(2):111-119.
49. Lotan R., Belloni P.N., Tressler R.J., Lotan D., Xu X.C., Nicolson G.L. Expression of galectins on microvessel endothelial cells and their involvement in tumour cell adhesion. Glycoconj. J. 1994, 11(5):462-468.
50. Matarrese P., Tinari N., Semeraro M.L., Natoli C., Iacobelli S., Malorni W. Galectin-3 overexpression protects from cell damage and death by influencing mitochondrial homeostasis. FEBS Lett. 2000, 473(3):311-315.
51. Matsuda Y., Yamagiwa Y., Fukushima K., Ueno Y., Shimosegawa T. Expression of galectin-3 involved in prognosis of patients with hepatocellular carcinoma. Hepatol. Res. 2008, 38(11):1098-1111.
52. Mazurek N., Conklin J., Byrd J.C., Raz A., Bresalier R.S. Phosphorylation of the h-galactoside-binding protein galectin-3 modulates binding to its ligands. J. Biol. Chem. 2000, 275(46):36311-36315.
53. Mazurek N., Sun Y.J., Price J.E., Ramdas L., Schober W., Nangia-Makker P., et al. Phosphorylation of galectin-3 contributes to malignant transformation of human epithelial cells via modulation of unique sets of genes. Cancer Res. 2005, 65(23):10767-10775.
54. Moisan S., Demers M., Mercier J., Magnaldo T., Potworowski E.F., St-Pierre Y. Upregulation of galectin-7 in murine lymphoma cells is associated with progression toward an aggressive phenotype. Leukemia 2003, 17(4):751-759.
55. Nangia-Makker P., Balan V., Raz A. Regulation of tumor progression by extracellular galectin-3. Cancer Microenviron. 2008, 1(1):43-51.
56. Niida S., Amizuka N., Hara F., Ozawa H., Kodama H. Expression of Mac-2 antigen in the preosteoclast and osteoclast identified in the op/op mouse injected with macrophage colony-stimulating factor. J. Bone Miner. Res. 1994, 9(6):873-881.
57. Ochieng J., Furtak V., Lukyanov P. Extracellular functions of galectin-3. Glycoconj. J. 2004, 19(7-9):527-535.
58. Okada K., Shimura T., Suehiro T., Mochiki E., Kuwano H. Reduced galectin-3 expression is an indicator of unfavorable prognosis in gastric cancer. Anticancer Res. 2006, 26(2B):1369-1376.
59. Pernicone P.J., Scheithauer B.W., Sebo T.J., Kovacs K.T., Horvath E., Young W.F., et al. Pituitary carcinoma: a clinicopathologic study of 15 cases. Cancer 1997, 79(4):804-812.
60. Qian X., Jin L., Grande J.P., Lloyd R.V. Transforming growth factor-beta and p27 expression in pituitary cells. Endocrinology 1996, 137(7):3051-3060.
61. Quereda V., Malumbres M. Cell cycle control of pituitary development and disease. J. Mol. Endocrinol. 2009, 42(2):75-86.
62. Raimond J., Zimonjic D.B., Mignon C., Mattei M., Popescu N.C., Monsigny M., et al. Mapping of the galectin-3 gene (LGALS3) to human chromosome 14 at region 14q21-22. Mamm. Genome 1997, 8(9):706-707.
63. Raz A., Meromsky L., Zvibel I., Lotan R. Transformation-related changes in the expression of endogenous cell lectins. Int. J. Cancer 1987, 39(3):353-360.
64. Reichert F., Saada A., Rotshenker S. Peripheral nerve injury induces Schwann cells to express two macrophage phenotypes: phagocytosis and the galactose-specific lectin MAC-2. J. Neurosci. 1994, 14(5 Pt 2):3231-3245.
65. Riss D., Jin L., Qian X., Bayliss J., Scheithauer B.W., Young W.F., et al. Differential expression of galectin-3 in pituitary tumors. Cancer Res. 2003, 63(May (9)):2251-2255.
66. Rodriguez F.J., Scheithauer B.W., Roncaroli F., Silva A.I., Kovacs K., Brat D.J., et al. Galectin-3 expression is ubiquitous in tumors of the sellar region, nervous system, and mimics: an immunohistochemical and RT-PCR study. Am. J. Surg. Pathol. 2008, 32(9):1344-1352.
67. Roff C.F., Wang J.L. Endogenous lectins from cultured cells. Isolation and characterization of carbohydrate-binding proteins from 3T3 fibroblasts. J. Biol. Chem. 1983, 258(17):10657-10663.
68. Roncaroli F., Scheithauer B.W., Cenacchi G., Horvath E., Kovacs K., Lloyd R.V., et al. 'Spindle cell oncocytoma' of the adenohypophysis: a tumor of folliculostellate cells?. Am. J. Surg. Pathol. 2002, 26(8):1048-1055.
69. Ruebel K.H., Jin L., Qian X., Scheithauer B.W., Kovacs K., Nakamura N., et al. Effects of DNA methylation on galectin-3 expression in pituitary tumors. Cancer Res. 2005, 65(February (4)):1136-1140.
70. Ruebel K.H., Leontovich A.A., Jin L., Stilling G.A., Zhang H., Qian X., et al. Patterns of gene expression in pituitary carcinomas and adenomas analyzed by high-density oligonucleotide arrays, reverse transcriptase-quantitative PCR, and protein expression. Endocrine 2006, 29(3):435-444.
71. Ruebel K.H., Leontovich A.A., Tanizaki Y., Jin L., Stilling G.A., Zhang S., et al. Effects of TGFbeta1 on gene expression in the HP75 human pituitary tumor cell line identified by gene expression profiling. Endocrine 2008, 33(1):62-76.
72. Schaffert C., Pour P.M., Chaney W.G. Localization of galectin-3 in normal and diseased pancreatic tissue. Int. J. Pancreatol. 1998, 23(1):1-9.
73. Scheithauer B.W., Kurtkaya-Yapicier O., Kovacs K.T., Young W.F., Lloyd R.V. Pituitary carcinoma: a clinicopathological review. Neurosurgery 2005, 56(5):1066-1074.
74. Schulte H.M., Oldfield E.H., Allolio B., Katz D.A., Berkman R.A., Ali I.U. Clonal composition of pituitary adenomas in patients with Cushing's disease: determination by X-chromosome inactivation analysis. J. Clin. Endocrinol. Metab. 1991, 73(6):1302-1308.
75. Shekhar M.P., Nangia-Makker P., Tait L., Miller F., Raz A. Alterations in galectin-3 expression and distribution correlate with breast cancer progression: functional analysis of galectin-3 in breast epithelial-endothelial interactions. Am. J. Pathol. 2004, 165(6):1931-1941.
76. Shimonishi T., Miyazaki K., Kono N., Sabit H., Tuneyama K., Harada K., et al. Expression of endogenous galectin-1 and galectin-3 in intrahepatic cholangiocarcinoma. Hum. Pathol. 2001, 32(3):302-310.
77. Shimura T., Takenaka Y., Tsutsumi S., Hogan V., Kikuchi A., Raz A. Galectin-3 a novel binding partner of catenin. Cancer Res. 2004, 64(18):6363-6367.
78. Shimura T., Takenaka Y., Fukumori T., Tsutsumi S., Okada K., Hogan V., et al. Implication of galectin-3 in Wnt signaling. Cancer Res. 2005, 65(9):3535-3537.
79. Sparrow C.P., Leffler H., Barondes S.H. Multiple soluble b-galactoside binding lectins from human lung. J. Biol. Chem. 1987, 262(16):7383-7390.
80. Stock M., Schafer H., Stricker S., Gross G., Mundlos S., Otto F. Expression of galectin-3 in skeletal tissues is controlled by Runx2. J. Biol. Chem. 2003, 278(19):17360-17367.
81. Takenaka Y., Fukumori T., Yoshii T., Oka N., Inohara H., Kim H.R., et al. Nuclear export of phosphorylated galectin-3 regulates its antiapoptotic activity in response to chemotherapeutic drugs. Mol. Cell. Biol. 2004, 24(1):4395-4406.
82. Teymoortash A., Pientka A., Schrader C., Tiemann M., Werner J.A. Expression of galectin-3 in adenoid cystic carcinoma of the head and neck and its relationship with distant metastasis. J. Cancer Res. Clin. Oncol. 2006, 132(1):51-56.
83. Thodou E., Argyrakos T., Kontogeorgos G. Galectin-3 as a marker distinguishing functioning from silent corticotroph adenomas. Hormones 2007, 6(3):227-232.
84. Tsuboi K., Shimura T., Masuda N., Ide M., Tsutsumi S., Yamaguchi S., et al. Galectin-3 expression in colorectal cancer: relation to invasion and metastasis. Anticancer Res. 2007, 27(4B):2289-2296.
85. Van den Brule F., Califice S., Castronovo V. Expression of galectins in cancer: a critical review. Glycoconj. J. 2004, 19(7-9):537-542.
86. Villa-Verde D.M., Silva-Monteiro E., Jasiulionis M.G., Farias-De-Oliveira D.A., Brentani R.R., Savino W., et al. Galectin-3 modulates carbohydrate-dependent thymocyte interactions with the thymic microenvironment. Eur. J. Immunol. 2002, 32(5):434-1444.
87. Vladimirova V., Waha A., Luckerath K., Pesheva P., Probstmeier R. Runx2 is expressed in human glioma cells and mediates the expression of galectin-3. J. Neurosci. Res. 2008, 86(11):450-461.
88. Wang Y., Nangia-Makker P., Tait L., Balan V., Hogan V., Pienta K.J., et al. Regulation of prostate cancer progression by galectin-3. Am. J. Pathol. 2009, 174(4):1515-1523.
89. Wollenberg A., de la Salle H., Hanau D., Liu F.T., Bieber T. Human keratinocytes release the endogenous beta-galactoside-binding soluble lectin immunoglobulin E (IgE-binding protein) which binds to Langerhans cells where it modulates their binding capacity for IgE glycoforms. J. Exp. Med. 1993, 178(3):777-785.
90. Woo H.J., Shaw L.M., Messier J.M., Mercurio A.M. The major non integrin laminin binding protein of macrophages is identical to carbohydrate binding protein 35 (Mac-2). J. Biol. Chem. 1990, 265(13):7097-7099.
91. Xu X.-C., El-Naggar A.K., Lotan R. Differential expression of galectin-1 and galectin-3 in thyroid tumors. Potential diagnostic implications. Am. J. Pathol. 1995, 147(3):815-822.
92. Yang R.Y., Hsu D.K., Liu F.T. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc. Natl. Acad. Sci. U.S.A. 1996, 93(13):6737-6742.
93. Yoshii T., Fukumori T., Honjo Y., Inohara H., Kim H.R., Raz A. Galectin-3 phosphorylation is required for its anti-apoptotic function and cell cycle arrest. J. Biol. Chem. 2002, 277(9):6852-6857.
94. Zhang H.Y., Jin L., Stilling G.A., Ruebel K.H., Coonse K., Tanizaki Y., et al. RUNX1 and RUNX2 upregulate galectin-3 expression in human pituitary tumors. Endocrine 2009, 35(1):101-111.