A new function for transferrin expressed in testes;Une nouvelle fonction pour la transferrine exprimée par le testicule

Andrologie

Volumn 19, Issue 2, 2009, Pages 81-89

  Fumel, B ^a   Sow, A ^b   Fouchecourt S ^c   Guillou, F ^d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d Haras Nationaux   (France)

Author keywords

Phagocytosis; Residual bodies; Sertoli cells; Testis; Transferrin

Indexed keywords

EID: 67949115627     PISSN: 11662654     EISSN: 17605377     Source Type: Journal    
DOI: 10.1007/s12610-009-0013-3     Document Type: Review

References (76)

1. M.K. Skinner W.L. Cosand M.D. Griswold 1984 Purification and characterization of testicular transferrin secreted by rat Sertoli cells Biochem J 218 2 313 320
2. H. Fuse M. Okomura T. Kazama T. Katayama 1994 Correlation of seminal plasma transferrin concentration and hypoosmotic swelling of the sperm Arch Androl 32 2 95 100
3. C. Sueldo R.P. Marrs T. Berger 1984 Correlation of semen transferrin concentration and sperm fertilizing capacity Am J Obstet Gynecol 150 528 531
4. C. Barthelemy B. Khalfoun J.M. Guillaumin 1988 Seminal fluid transferrin as an index of gonadal function in men J Reprod Fertil 82 1 113 118
5. A. Ber N. Vardinon L. Yogev 1990 Transferrin in seminal plasma and in serum of men: its correlation with sperm quality and hormonal status Hum Reprod 5 3 294 297
6. R.R. Gilmont P.L. Senger S.R. Sylvester M.D. Griswold 1990 Seminal transferrin and spermatogenic capability in bull Biol Reprod 43 1 151 157
7. R.N. Bharshankar J.R. Bharshankar 2000 Relationship of seminal plasma transferrin with seminal parameters in male infertility Indian J Physiol Pharmacol 44 4 456 460
8. K.I. Yoshida Y. Nakame Y. Uchijima 1988 Seminal plasma transferrin concentration in normozoospermic fertile men and oligozoospermic men associated with varicocele Int J Fertil 33 6 432 436
9. S. Hugly M. Griswold 1987 Regulation of levels of specific Sertoli cell mRNAs by vitamin A Dev Biol 121 2 316 324
10. A. Zalata T. Hafez F. Schoonjans F. Comhaire 1996 The possible meaning of transferrin and its soluble receptors in seminal plasma as markers of the seminiferous epithelium Hum Reprod 11 4 761 764
11. S.E. Bernstein 1987 Hereditary hypotransferrinemia with hemosiderosis, a murine disorder resembling human atransferrinemia J Lab Clin Med 110 6 690 705
12. B. Gorinski C. Horsburgh P.E. Lindsey 1979 Evidence for the bilobal nature of differic rabbit plasma transferrin Nature 281 5727 157 158
13. S. Heaphy J. Williams 1982 The preparation and partial characterization of N-terminal and C-terminal: iron-binding fragments from rabbit serum transferrin Biochem J 205 3 611 617
14. P. Aisen A. Leibman J. Zweier 1978 Stoichiometric and site characteristics of the binding of iron to human transferrin J Biol Chem 253 6 1930 1937
15. E.H. Morgan 1969 Factors affecting the synthesis of transferrin by rat tissue slices J Biol Chem 244 15 4193 4199
16. R.R. Meehan D.P. Barlow R.E. Hill 1984 Pattern of serum protein gene expression in mouse visceral yolk sac and fetal liver EMBO J 3 8 1881 1885
17. R. Cassia L. Besnard L. Fiette 1997 Transferrin is an early marker of hepatic differentiation, and its expression correlates with the postnatal development of oligodendrocytes in mice J Neurosci Res 50 3 421 432
18. G.C. Yeoh E.H. Morgan 1974 Albumin and transferrin synthesis during development in the rat Biochem J 144 2 215 224
19. M.J. Levin D. Tuil G. Uzan 1984 Expression of the transferrin gene during development of non-hepatic tissues: high-level of transferrin mRNA in fetal muscle and adult brain Biochem Biophys Res Commun 122 1 212 217
20. B. Bloch T. Popovici S. Chouham 1987 Transferrin gene expression in choroid plexus of the adult rat brain Brain Res Bull 18 4 573 576
21. M.G. Yefimova J.C. Jeanny X. Guillonneau 2000 Iron, ferritin, transferrin and transferrin receptor in the adult rat retina Invest Ophtalmol Vis Sci 41 8 2343 2351
22. E.Y. Lee M.H. Barcellos-Hoff L.H. Chen 1987 Transferrin is a major mouse milk protein and is synthesized by mammary epithelial cells In Vitro Cell Dev Biol 23 3 221 226
23. J.I. Huggenvik R.L. Idzerda L. Haywood 1987 Transferrin messenger ribonucleic acid molecular cloning and hormonal regulation in rat Sertoli cells Endocrinology 120 1 332 340
24. S. Migrenne C. Racine F. Guillou R. Habert 2003 Pituitary hormones inhibit the function and differentiation of fetal Sertoli cells Endocrinology 144 6 2617 2622
25. C.T. Anthony M. Rosselli M.K. Skinner 1991 Actions of the testicular paracrine factor (P-Mod-S) on Sertoli cell transferrin secretion throughout pubertal development Endocrinology 129 1 353 360
26. S. Suire I. Fontaine F. Guillou 1997 Transferrin gene expression and secretion in rat Sertoli cells Mol Reprod Dev 48 2 168 175
27. C. Morales S. Hugly M.D. Griswold 1987 Stage-dependent levels of specific mRNA transcripts in Sertoli cells Biol Reprod 36 4 1035 1046
28. C. Lecureuil C. Staub S. Fouchécourt 2007 Transferrin overexpression alters testicular function in aged mice Mol Reprod Dev 74 2 197 206
29. M.K. Skinner M.D. Griswold 1982 Secretion of testicular transferrin by cultured Sertoli cells is regulated by hormones and retinoids Biol Reprod 27 1 211 221
30. S. Suire I. Fontaine F. Guillou 1995 Follicle-stimulating hormone (FSH) stimulates transferrin gene transcription in rat Sertoli cells: cis and trans-acting elements involved in FSH action via cyclic adenosine 3-5-monophosphate on the transferrin gene Mol Endocrinol 9 6 756 766
31. P. Foucault S. Carreau W. Kuczynski 1992 Human Sertoli cells in vitro. Lactate, estradiol-17 beta and transferrin production J Androl 13 5 361 367
32. M. Huleihel D. Zeyse E. Lunenfeld 2002 Induction of transferrin secretion in murine Sertoli cells by FSH and IL-1: the possibility of different mechanism(s) of regulation Am J Reprod Immunol 47 2 112 117
33. C. Monet-Kuntz F. Guillou I. Fontaine Y. Combarnous 1992 Purification of ovine transferrin and study of the hormonal control of its secretion in enriched cultures of ovine Sertoli cells J Reprod Fertil 94 1 189 201
34. S. Suire M.C. Maurel F. Guillou 1996 Follitropin action on the transferrin gene in Sertoli cells is mediated by cAMP-responsive-element- binding-protein and antagonized by chicken ovalbumin-upstream-promoter- transcription factor Eur J Biochem 239 1 52 60
35. S. Hugly K. Roberts M.D. Griswold 1988 Transferrin and sulphated glycoprotein-2 messenger ribonucleic acid levels in the testis and isolated Sertoli cells of hypophysectomized rats Endocrinology 122 4 1390 1396
36. N. Itoh A. Nanbu H. Tachiki 1994 Restoration of testicular transferrin, insulin-like growth factor-1 (IGF-1), and spermatogenesis by exogenously administered purified FSH and testosterone in medically hypophysectomized rats Arch Androl 33 3 169 177
37. F. Sigillo F. Guillou I. Fontaine 1999 In vitro regulation of rat Sertoli cell transferrin expression by tumor necrosis factor alpha and retinoic acid Mol Cell Endocrinol 148 1-2 163 170
38. S.D. Holmes L.I. Lipshultz R.G. Smith 1984 Regulation of transferrin secretion by human Sertoli cells cultured in the presence or absence of human peritubular cells J Clin Endocrinol Metab 59 6 1058 1062
39. S. Storch B. Kübler S. Höning 2001 Transferrin binds insulin-like growth factors and affects binding properties of insulin-like growth factor binding protein-3 FEBS Lett 509 3 395 398
40. C. Le Roy H. Lejeune F. Chuzel 1999 Autocrine regulation of Leydig cell differentiated functions by insulin-like growth factor I and transforming growth factor beta J Steroid Biochem Mol Biol 69 1-6 379 384
41. K.P. Roberts C.A. AWoniyi R. Santulli B.R. Zirkin 1991 Regulation of Sertoli cell transferrin and sulphated glycoprotein-2 messenger ribonucleic acid levels during the restoration of spermatogenesis in the adult hypophysectomized rat Endocrinology 129 6 3417 3423
42. B. Le Magueresse C. Pineau F. Guillou B. Jégou 1988 Influence of germ cells upon transferrin secretion by rat Sertoli cells in vitro J Endocrinol 118 3 R13 R16
43. B.J. Stallard M.D. Griswold 1990 Germ cell regulation of Sertoli cell transferrin mRNA levels Mol Endocrinol 4 3 393 401
44. J.N. Norton M.K. Skinner 1992 Regulation of Sertoli cell differentiation by the testicular paracrine factor PModS: potential role of immediate-early genes Mol Endocrinol 6 12 2018 2026
45. P.D. Whaley J. Chaudhary A. Cupp M.K. Skinner 1995 Role of specific response elements of the c-fos promoter and involvement of intermediate transcription factor(s) in the induction of Sertoli cell differentiation (transferrin promoter activation) by the testicular paracrine factor PModS Endocrinology 136 7 3046 3053
46. J.P. De Winter H.M. Vanderstichele G. Verhoeven 1994 Peritubular myoid cells from immature rat testes secrete activin-A and express activin receptor type II in vitro Endocrinology 135 2 759 767
47. M. Onoda C.A. Suarez-Quian 1994 Modulation of transferrin secretion by epidermal growth factor in immature rat Sertoli cells in vitro J Reprod Fertil 100 2 541 550
48. E. Hoeben L. Deboel L. Rombauts 1994 Different cells and cell lines produce factors that modulate Sertoli cell function Mol Cell Endocrinol 101 1-2 263 275
49. F.R. Boockfor L.K. Schwarz 1991 Effects of interleukin-6, interleukin-2, and tumor necrosis factor alpha on transferrin release from Sertoli cells in culture Endocrinology 129 1 256 262
50. E. Hoeben J. Van Damme W. Put 1996 Cytokines derived from activated human mononuclear cells markedly stimulate transferrin secretion by cultured Sertoli cells Endocrinology 137 2 514 521
51. S.D. Holmes L.R. Bucci L.I. Lipshultz R.G. Smith 1983 Transferrin binds specifically to pachytene spermatocytes Endocrinology 113 5 1916 1918
52. S.R. Sylvester M.D. Griswold 1984 Localization of transferrin and transferrin receptors in rat testes Biol Reprod 31 1 195 203
53. R.G. Petrie Jr C.R. Morales 1992 Receptor-mediated endocytosis of testicular transferrin by germinal cells of the rat testis Cell Tissue Res 267 1 45 55
54. P.J. Wauben-Penris G.J. Strous H.A. van der Donk 1988 Kinetics of transferrin endocytosis and iron uptake by intact isolated rat seminiferous tubules and Sertoli cells in culture Biol Reprod 38 4 853 861
55. N. Jabado F. Cannone-Hergaux S. Gruenheid 2002 Iron transporter Nramp2/DMT-1 is associated with the membrane of phagosomes in macrophages and Sertoli cells Blood 100 7 2617 2622
56. H.J. Merker J. Vormann T. Günther 1996 Iron-induced injury of rat testis Andrologia 28 5 267 273
57. R.L. Idzerda H. Huebers C.A. Finch G.S. McKnight 1986 Rat transferrin gene expression: tissue-specific regulation by iron deficiency Proc Natl Acad Sci USA 83 11 3723 3727
58. M.G. Yefimova A. Sow I. Fontaine 2008 Dimeric transferrin inhibits phagocytosis of residual bodies by testicular rat Sertoli cells Biol Reprod 78 4 697 704
59. V.A. Fadok D.L. Bratton S.C. Frasch 1998 The role of phosphatidylserine in recognition of apoptotic cells by phagocytes Cell Death Differ 5 7 551 562
60. Y. Kawasaki A. Nakagawa Nagaosa 2002 Phosphatidylserine binding of class B scavenger receptor type I, a phagocytosis receptor of testicular Sertoli cells J Biol Chem 277 30 27559 27566
61. A. Shiratsuchi Y. Kawasaki M. Ykemoto 1999 Role of class B scavenger receptor type I in phagocytosis of apoptotic rat spermatogenic cells by Sertoli cells J Biol Chem 274 9 5901 5908
62. I. Gillot C. Jehl-Pietri P. Gounon 2005 Germ cells and fatty acids induce translocation of CD36 scavenger receptor to the plasma membrane of Sertoli cells Cell Sci 118 14 3027 3035
63. H. Wang Y. Chen Y. Ge 2005 Immunoexpression of Tyro 3 family receptors Tyro3, Axl and Mer, and their ligand Gas6 in postnatal developing mouse testis J Histochem Cytochem 53 11 1355 1364
64. T. Nakano Y. Ishimoto J. Kishino 1997 Cell adhesion to phosphatidylserine mediated by a product of growth arrestspecific gene 6 J Biol Chem 272 47 29411 29414
65. O. Benzakour A. Gely R. Lara V. Coronas 2007 Fonctions nouvelles de Gas6 et de la protéine S: facteurs vitamine K-dépendants et ligands des récepteurs tyrosine-kinase de la famille TAM Med Sci (Paris) 23 10 826 833
66. R.S. Scott E.J. McMahon S.M. Pop 2001 Phagocytosis and clearance of apoptotic cells is mediated by Mer Nature 411 6834 207 211
67. J.C. Todt B. Hu J.L. Curtis 2004 The receptor tyrosine-kinase Mertk activates phospholipase C-gamma2 during recognition of apoptotic thymocytes by murine macrophages J Leukoc Biol 75 4 705 713
68. H. Sakamoto N. Sakamoto M. Oryu 1997 A novel function of transferrin as a constituent of macromolecular activators of phagocytosis from platelets and their precursors Biochem Biophys Res Commun 230 2 270 274
69. Q. Lu M. Gore Q. Zhang 1999 Tyro3 family receptors are essential regulators of mammalian spermatogenesis Nature 398 6729 723 728
70. H. Kenis H. van Genderen N.M. Deckers 2006 Annexin A5 inhibits engulfment through internalization of PS-expressing cell membrane patches Exp Cell Res 312 6 719 726
71. C. Pineau B. Le Magueresse J.L. Courtens B. Jégou 1991 Study in vitro of the phagocytic function of Sertoli cells in the rat Cell Tissue Res 264 3 589 598
72. M.M. Garza L.K. Schwarz J.M. Bonner F.R. Boockfor 1991 Sertoli cell function varies along the seminiferous tubule: the proportion and response of transferrin secretors differ between stage-associated tubule segments Endocrinology 128 4 1869 1874
73. C. Morales S. Hugly M.D. Griswold 1987 Stage-dependent levels of specific mRNA transcripts in Sertoli cells Biol Reprod 36 4 1035 1046
74. C.R. Morales A.A. Alcinar N.B. Hecht M.D. Griswold 1989 Specific mRNAs in Sertoli and germinal cells of testes from stage synchronized rats Mol Endocrinol 3 4 725 733
75. W.W. Wright M. Parviven Musto 1983 Identification of stage-specific proteins synthesized by rat seminiferous tubules Biol Reprod 29 1 257 270
76. Y. Maeda A. Shiratsuchi M. Namiki Y. Nakanishi 2002 Inhibition of sperm production in mice by annexin V microinjected into seminiferous tubules: possible etiology of phagocytic clearance of apoptotic spermatogenic cells and male fertility Cell Death Differ 9 7 742 749