Regulated expression and ultrastructural localization of galectin-1, a proapoptotic β-galactoside-binding lectin, during spermatogenesis in rat testis

Biology of Reproduction

Volumn 68, Issue 1, 2003, Pages 51-59

  Dettin, Luis ^a   Rubinstein, Natalia ^b   Aoki, Agustin ^a   Rabinovich, Gabriel A ^b   Maldonado, Cristina A ^a,c  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

Author keywords

Apoptosis; Immunology; Sertoli cells; Spermatogenesis

Indexed keywords

ANTIBODY; CARBOHYDRATE BINDING PROTEIN; GALAPTIN; GALECTIN 1;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELL DIFFERENTIATION; CELL SPREADING; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CHRONIC INFLAMMATION; CONTROLLED STUDY; ENZYME BINDING; EPIDIDYMIS; GERM CELL; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; LECTIN BINDING; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATID; SPERMATOGENESIS; T LYMPHOCYTE ACTIVATION; TESTIS DEVELOPMENT; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; EPIDIDYMIS; GALACTOSIDES; GALECTIN 1; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, IMMUNOELECTRON; RATS; RATS, WISTAR; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

ANIMALIA;

EID: 0037230314     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.102.006361     Document Type: Article

References (52)

1. Barondes SH, Castronovo V, Cooper DNW, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K, Leffler H, Liu E, Lotan R, Mercurio AM, Monsigni M, Pillai S, Poirier F, Raz A, Rigby PWJ, Rini JM, Wang JL. Galectins: A family of animal galactoside-binding lectins. Cell 1994; 76:597-598.
2. Rabinovich GA, Baum LG, Tinari N, Paganelli R, Natoli C, Liu F-T, lacobelli S. Galectins and their ligands: Amplifiers, silencers or tuners of the inflammatory response. Trends Immunol 2002; 23:313-320.
3. Liu F-T. Galectins: A new family of regulators of inflammation. Clin Immunol 2000; 97:79-88.
4. Rabinovich GA, Rubinstein N, Fainboim L. Unlocking the secrets of galectins: A challenge at the frontiers of glycoimmunology. J Leukoc Biol 2002; 71:741-752.
5. Baum LG, Pang M, Perillo NL, Wu T, Delegaene A, Uittenbogaart CH, Fukuda M, Seilhamer JJ. Human thymic epithelial cells express an endogenous lectin, galectin-1, which binds to core 2 O-glycans on thymocytes and T lymphoblastoid cells. J Exp Med 1995; 181:877-887.
6. Rabinovich GA, Castagna LF, Landa CA, Riera CM, Sotomayor CE. Regulated expression of a 16-kDa galectin-like protein in activated rat macrophages. J Leukoc Biol 1996; 59:363-370.
7. Rabinovich GA, Iglesias MM, Modesti NM, Castagna LF, Todel CW, Riera CM, Sotomayor CE. Activated rat macrophages produce a galectin-1-like protein that induces apoptosis of activated T-cells: A biochemical and functional characterization. J Immunol 1998; 160:4831-4840.
8. Zúñiga El, Gruppi A, Hirabayashi J, Kasai KI, Rabinovich GA. Regulated expression and effect of galectin-1 on Trypanosoma cruzi-infected macrophages: Modulation of microbicidal activity and survival. Infect Immun 2001; 69:6804-6812.
9. Blaser C, Kaufmann M, Muller C, Zimmermann C, Wells V, Mallucci L, Pircher H. β-galactoside-binding protein secreted by activated T cells inhibits antigen-induced proliferation of T cells. Eur J Immunol 1998; 28:2311-2319.
10. Zúñiga E, Rabinovich GA, Iglesias MM, Gruppi A. Regulated expression of galectin-1 during B-cell activation and implications for T-cell apoptosis. J Leukoc Biol 2001; 70:73-79.
11. Maldonado CA, Castagna LE, Rabinovich GA, Landa CA. Immunocytochemical study of the distribution of a 16-kDa galectin in the chicken retina. Invest Ophthalmol Vis Sci 1999; 40:2971-2977.
12. Perillo NL, Pace KE, Seihamer JJ, Baum LG. Apoptosis of T-cells mediated by galectin-1. Nature 1995; 378:736-739.
13. Vespa GN, Lewis LA, Kozak KR, Moran M, Nguyen JT, Baum LG, Miceli MC. Galectin-1 specifically modulates TCR signals to enhance TCR apoptosis but inhibit IL-2 production and proliferation. J Immunol 1999; 162:799-806.
14. Rabinovich GA, Alonso CR, Sotomayor CE, Durand S, Bocco JL, Riera CM. Molecular mechanisms implicated in galectin-1-induced apoptosis: Activation of the AP-1 transcription factor and down-regulation of Bcl-2. Cell Death Differ 2000; 7:747-753.
15. Rabinovich GA, Ariel A, Hershkoviz R, Hirabayashi J, Kasai KI, Lider O. Specific inhibition of T-cell adhesion to extracellular matrix and proinflammatory cytokine secretion by human recombinant galectin-1. Immunology 1999; 97:100-106.
16. Rabinovich GA, Daly G, Dreja H, Tailor H, Riera CM, Hirabayashi J, Chernajovsky Y. Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis. J Exp Med 1999; 190:385-397.
17. Santucci EL, Fiorucci S, Cammilleri F, Servillo G, Federici B, Morelli A. Galectin-1 exerts immunomodulatory and protective effects on concanavalin-A-induced hepatitis in mice. Hepatology 2000; 31:399-407.
18. Rabinovich GA, Sotomayor CE, Riera CM, Bianco ID, Correa SG. Evidence of a role for galectin-1 in acute inflammation. Eur J Immunol 2000; 30:1331-1339.
19. Filippini A, Riccioli A, Padula F, Lauretti P, D'Alessio A, De Cesaris P, Gandini L, Lenzi A. Ziparo E. Control and impairment of immune privilege in the testis and in semen. Hum Reprod Update 2001; 7: 444-449.
20. Ferguson TA, Griffith TS. A vision of cell death: Insights into immune privilege. Immunol Rev 1997; 156:167-184.
21. Pöllänen P, von Euler M, Sainio-Pollanen S, Jahnukainen K, Hakovirta H, Soder O, Parvinen M. Immunosuppressive activity in the rat seminiferous tubules. J Reprod Immunol 1992; 22:117-126.
22. Pöllänen P, von Euler M, Jahnukainen K, Saari T, Parvinen M, Sainio-Pöllänen S, Soder O. Role of transforming growth factor β in testicular immunosuppression. J Reprod Immunol 1993; 24:123-137.
23. Selawry HP, Koth M, Herrod HG, Lu ZN. Production of a factor, or factors, suppressing IL-2 production and T-cell proliferation by Sertoli cell-enriched preparations. A potential role for islet transplantation in an immunologically privileged site. Transplantation 1991; 52:846-85.
24. De Cesaris P, Filippini A, Setchel BP. Immunosuppressive molecules produced by Sertoli cells cultured in vitro: Biological effects on lymphocytes. Biochem Biophys Res Commun 1992; 186:1639-1646.
25. Bellgrau D, Gold D, Selawry H, Moore J, Franzusoff A, Duke RC. A role for CD95 ligand in preventing graft rejection. Nature 1995; 377:630-632.
26. Lee J, Richburg JH, Younkin SC, Boekelheide K. The Fas system is a key regulator of germ cells apoptosis in the testis. Endocrinology 1997; 138:2081-2088.
27. Pentikainen V, Erkkila K, Dunkel L. Fas regulates germ cell apoptosis in the human testis in vitro. Am J Physiol 1999; 276:E310-E316.
28. Green DR, Ferguson TA. The role of Fas ligand in immune privilege. Nat Rev Mol Cell Biol 2001; 2:917-924.
29. Phillips B, Knisley K, Weitlauf KD, Dorsett J, Lee V, Weitlauf H, Differential expression of two β-galactoside-binding lectins in the reproductive tracts of pregnant mice. Biol Reprod 1996; 55:548-558.
30. Wollina U, Schreiber G, Gorning M, Feldrappe S, Burchert M, Gabius HJ, Sertoli cell expression of galectin-1 and -3 and accessible binding sites in normal human testis and Sertoli cell-only syndrome. Histol Histopathol 1999; 14:779-784.
31. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-684.
32. Frens G, Controlled nucleation of the regulation of the particle size in monodisperse gold solution. Nat Phys Sci 1973; 241:20-22.
33. Leblond CP, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci 1952; 55:548-573.
34. Poirier F, Robertson EJ. Normal development of mice carrying a null mutation in the gene encoding the L-14 S-type lectin. Development 1993; 119:1229-1236.
35. Rabinovich GA, Rubinstein N, Matar P, Rozados V, Gervasoni S, Scharovsky OG. The antimetastatic effect of a single low dose of cyclophosphamide involves modulation of galectin-1 and Bcl-2 expression. Cancer Immunol Immunother 2002; 50:597-603.
36. Griswold MD. The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol 1998; 9:411-416.
37. Skinner MK. Secretion of growth factors and other regulatory factors. In: Russell LD, Griswold MD (eds.), The Sertoli Cell, Vol. 1, 1st Ed. Clearwater, FL: Cache River Press; 1993:237-248.
38. Parvinen M. Cyclic function of Sertoli cells. In: Russell LD, Griswold MD (eds.), The Sertoli Cell, Vol. 1, 1st Ed. Clearwater, FL: Cache River Press; 1993:349-364.
39. Griswold MD. Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 1995; 52:211-216.
40. Linder CC, Heckert LL, Roberts KP, Kim KH, Griswold MD. Expression of receptors during the cycle of the seminiferous epithelium. Ann N Y Acad Sci 1991; 637:313-321
41. Timmons PM, Righby PWJ, Poirier E The murine seminiferous epithelial cycle is prefigured in the Sertoli cells of the embryonic testis. Development 2002; 129:635-647
42. Turek PH, Malkowicz SB, Tomaszewski JE, Wein AJ, Peehl D. The role of Sertoli cells in active immunosuppression in the human testis. Br J Urol 1996; 77:891-895,
43. Pöllänen P, von Euler M, Soder O. Testicular immunoregulatory factors. J Reprod Immunol 1990; 18:51-76.
44. Hedeger MP, Meinhardt A. Local regulation of T-cell numbers and lymphocyte-inhibiting activity in the interstitial tissue of the adult rat testis. J Reprod Immunol 2000; 48:69-80.
45. Yin Y, Stahl BC, De Wolf WC, Morgentaler A. p53-mediated germ cell quality control in spermatogenesis. Dev Biol 1998; 204:165-171.
46. Akama TO, Nakagawa H, Sugihara K, Narisawa S, Ohyama C, Nishimura S, O'Brien DA, Moremen KW, Millan JL, Fukuda MN. Germ cell survival through carbohydrate-mediated interaction with Sertoli cells. Science 2002; 295:124-127,
47. Jegou B, Spermatids are regulators of Sertoli cell function. Ann N Y Acad Sci 1991; 637:340-353.
48. Cavicchia JC, Sacerdote FL. Correlation between blood-testis barrier development and onset of the first spermatogenic wave in normal and in busulfan-treated rats: A lanthanum and freeze-fracture study. Anat Rec 1991; 230:361-8.
49. Topfer-Petersen E. Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum Reprod Update 1999; 5:314-329.
50. Sylvester SR, Skinner MK, Griswold MD. A sulfated glycoprotein synthesized by Sertoli cells and by epididymal cells is a component of the sperm membrane. Biol Reprod 1984; 31:1087-1101.
51. Cooper DNW, Barondes SH. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol 1990; 110:1681-1691.
52. Poirier F, Robertson EJ. Normal development of mice carrying a null mutation in the gene encoding the L-14 S-type lectin. Development 1993; 119:1229-1236.