Identification of the Leukemia inhibitory factor cell targets within the rat testis

Biology of Reproduction

Volumn 72, Issue 3, 2005, Pages 602-611

  Dorval Coiffec, Isabelle ^a   Delcros, Jean Guy ^a   Hakovirta, Harri ^b   Toppari, Jorma ^b   Jégou, Bernard ^a   Piquet Pellorce, Claire ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

Cytokines; Meiosis; Spermatogenesis; Testis

Indexed keywords

ISOPROTEIN; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR; THYMIDINE; TRITIUM;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BIOTINYLATION; CARBOXY TERMINAL SEQUENCE; CELL POPULATION; COITUS; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; GERM CELL; IMMUNOREACTIVITY; MALE; MEIOSIS; MICRODISSECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURIFICATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; SEQUENCE ANALYSIS; SOMATIC CELL; SPERMATOGENESIS; SPERMATOGONIUM; TARGET CELL; TESTIS; TESTIS CELL; WESTERN BLOTTING;

ANIMALS; GERM CELLS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR ALPHA SUBUNIT; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CYTOKINE; RECEPTORS, OSM-LIF; SPERMATOGENESIS; SPERMATOGONIA; TESTIS; TISSUE DISTRIBUTION;

ANIMALIA; MYOIDEA; TRITIUM;

EID: 14044266903     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.034892     Document Type: Article

References (68)

1. Dym M. The male reproductive system. In: Weiss L, (ed.), Histology: Cell and Tissue Biology. New York: Elsevier Biomedical; 1983:1000-1053.
2. de Kretser DM, Loveland KL, Meinhardt A, Simorangkir D, Wreford N. Spermatogenesis. Hum Reprod 1998; 13(Suppl 1):1-8.
3. Piquet-Pellorce C, Dorval I, Jegou B. Paracrine control of spermatogenetic stem cells: example of the leukemia inhibitory factor [in French]. Contracept Fertil Sex 1997; 25:565-568.
4. Weinbauer GF, Wessels J. 'Paracrine' control of spermatogenesis. Andrologia 1999; 31:249-262.
5. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem J 1998; 334(Pt 2):297-314.
6. Elson GC, Lelievre E, Guillet C, Chevalier S, Plun-Favreau H, Froger J, Suard I, de Coignac AB, Delneste Y, Bonnefoy JY, Gauchat JF, Gascan H. CLF associates with CLC to form a functional heteromeric ligand for the CNTF receptor complex. Nat Neurosci 2000; 3:867-872.
7. Murakami M, Kamimura D, Hirano T. New IL-6 (gp130) family cytokine members, CLC/NNT1/BSF3 and IL-27. Growth Factors 2004; 22:75-77.
8. Yoshida K, Taga T, Saito M, Suematsu S, Kumanogoh A, Tanaka T, Fujiwara H, Hirata M, Yamagami T, Nakahata T, Hirabayashi T, Yoneda Y, Tanaka K, Wang WZ, Mori C, Shiota K, Yoshida N, Kishimoto T. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci U S A 1996; 93:407-411.
9. Ware CB, Horowitz MC, Renshaw BR, Hunt JS, Liggitt D, Koblar SA, Gliniak BC, McKenna HJ, Papayannopoulou T, Thoma B. Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 1995; 121:1283-1299.
10. Li M, Sendtner M, Smith A. Essential function of LIF receptor in motor neurons. Nature 1995; 378:724-727.
11. Kawashima I, Takiguchi Y. Interleukin-11: a novel stroma-derived cytokine. Prog Growth Factor Res 1992; 4:191-206.
12. Ernst M, Inglese M, Waring P, Campbell IK, Bao S, Clay FJ, Alexander WS, Wicks IP, Tarlinton DM, Novak U, Heath JK, Dunn AR. Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J Exp Med 2001; 194:189-203.
13. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992; 359:76-79.
14. Robb L, Li R, Hartley L, Nandurkar HH, Koentgen F, Begley CG. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat Med 1998; 4:303-308.
15. Bilinski P, Roopenian D, Gossler A. Maternal IL-11Ralpha function is required for normal decidua and fetoplacental development in mice. Genes Dev 1998; 12:2234-2243.
16. Song H, Lim H, Das SK, Paria BC, Dey SK. Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol Endocrinol 2000; 14:1147-1161.
17. Du X, Everett ET, Wang G, Lee WH, Yang Z, Williams DA. Murine interleukin-11 (IL-11) is expressed at high levels in the hippocampus and expression is developmentally regulated in the testis. J Cell Physiol 1996; 168:362-372.
18. de Miguel MP, de Boer-Brouwer M, de Rooij DG, Paniagua R, van Dissel-Emiliani FM. Ontogeny and localization of an oncostatin M-like protein in the rat testis: its possible role at the start of spermatogenesis. Cell Growth Differ 1997; 8:611-618.
19. Syed V, Gerard N, Kaipia A, Bardin CW, Parvinen M, Jegou B. Identification, ontogeny, and regulation of an interleukin-6-like factor in the rat seminiferous tubule. Endocrinology 1993; 132:293-299.
20. Okuda Y, Morris PL. Identification of interleukin-6 receptor (IL-6R) mRNA in isolated Sertoli and Leydig cells: regulation by gonadotropin and interleukins in vitro. Endocrine 1994; 2:1163-1168.
21. Piquet-Pellorce C, Dorval-Coiffec I, Pham MD, Jegou B. Leukemia inhibitory factor expression and regulation within the testis. Endocrinology 2000; 141:1136-1141.
22. Hilton DJ, Gough NM. Leukemia inhibitory factor: a biological perspective. J Cell Biochem 1991; 46:21-26.
23. Shen MM, Skoda RC, Cardiff RD, Campos-Torres J, Leder P, Ornitz DM. Expression of LIF in transgenic mice results in altered thymic epithelium and apparent interconversion of thymic and lymph node morphologies. EMBO J 1994; 13:1375-1385.
24. Yano H, Readhead C, Nakashima M, Ren SG, Melmed S. Pituitary-directed leukemia inhibitory factor transgene causes Cushing's syndrome: neuro-immune-endocrine modulation of pituitary development. Mol Endocrinol 1998; 12:1708-1720.
25. Molyneaux KA, Schaible K, Wylie C. GP130, the shared receptor for the LIF/IL6 cytokine family in the mouse, is not required for early germ cell differentiation, but is required cell-autonomously in oocytes for ovulation. Development 2003; 130:4287-4294.
26. Smith AG, Heath JK, Donaldson DD, Wong GG, Moreau J, Stahl M, Rogers D. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 1988; 336:688-690.
27. De Miguel MP, De Boer-Brouwer M, Paniagua R, van den Hurk R, De Rooij DG, Van Dissel-Emiliani FM. Leukemia inhibitory factor and ciliary neurotropic factor promote the survival of Sertoli cells and gonocytes in coculture system. Endocrinology 1996; 137:1885-1893.
28. Godin I, Deed R, Cooke J, Zsebo K, Dexter M, Wylie CC. Effects of the steel gene product on mouse primordial germ cells in culture. Nature 1991; 352:807-809.
29. Matsui Y, Toksoz D, Nishikawa S, Williams D, Zsebo K, Hogan BL. Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature 1991; 353:750-752.
30. Pesce M, Farrace MG, Piacentini M, Dolci S, De Felici M. Stem cell factor and leukemia inhibitory factor promote primordial germ cell survival by suppressing programmed cell death (apoptosis). Development 1993; 118:1089-1094.
31. Cheng L, Gearing DP, White LS, Compton DL, Schooley K, Donovan PJ. Role of leukemia inhibitory factor and its receptor in mouse primordial germ cell growth. Development 1994; 120:3145-3153.
32. Koshimizu U, Taga T, Watanabe M, Saito M, Shirayoshi Y, Kishimoto T, Nakatsuji N. Functional requirement of gp130-mediated signaling for growth and survival of mouse primordial germ cells in vitro and derivation of embryonic germ (EG) cells. Development 1996;122:1235-1242.
33. Bayne K. Revised Guide for the Care and Use of Laboratory Animals available. American Physiological Society. Physiologist 1996;39:199, 208-211.
34. Rathjen PD, Toth S, Willis A, Heath JK, Smith AG. Differentiation inhibiting activity is produced in matrix-associated and diffusible forms that are generated by alternate promoter usage. Cell 1990; 62:1105-1114.
35. Skinner MK, Fritz IB. Testicular peritubular cells secrete a protein under androgen control that modulates Sertoli cell functions. Proc Natl Acad Sci U S A 1985; 82:114-118.
36. Toebosch AM, Robertson DM, Trapman J, Klaassen P, de Paus RA, de Jong FH, Grootegoed JA. Effects of FSH and IGF-I on immature rat Sertoli cells: inhibin alpha- and beta-subunit mRNA levels and inhibin secretion. Mol Cell Endocrinol 1988; 55:101-105.
37. Palombi F, Di Carlo C. Alkaline phosphatase is a marker for myoid cells in cultures of rat peritubular and tubular tissue. Biol Reprod 1988; 39:1101-1109.
38. Klinefelter GR, Hall PF, Ewing LL. Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multistep procedure. Biol Reprod 1987; 36:769-783.
39. Li HE, Hedger MP, Clements JA, Risbridger GP. Localization of immunoreactive beta-endorphin and adrenocorticotropic hormone and pro-opiomelanocortin mRNA to rat testicular interstitial tissue macrophages. Biol Reprod 1991; 45:282-289.
40. Hutson JC. Changes in the concentration and size of testicular macrophages during development. Biol Reprod 1990; 43:885-890.
41. Labrie F, Simard J, Luu-The V, Pelletier G, Belanger A, Lachance Y, Zhao HF, Labrie C, Breton N, de Launoit Y, et al. Structure and tissue-specific expression of 3 beta-hydroxysteroid dehydrogenase/5-ene-4-ene isomerase genes in human and rat classical and peripheral steroidogenic tissues. J Steroid Biochem Mol Biol 1992; 41:421-435.
42. Meistrich ML, Longtin J, Brock WA, Grimes SR Jr, Mace ML. Purification of rat spermatogenic cells and preliminary biochemical analysis of these cells. Biol Reprod 1981; 25:1065-1077.
43. Pineau C, Syed V, Bardin CW, Jegou B, Cheng CY. Germ cell-conditioned medium contains multiple factors that modulate the secretion of testins, clusterin, and transferrin by Sertoli cells. J Androl 1993; 14:87-98.
44. Bellve AR, Millette CF, Bhatnagar YM, O'Brien DA. Dissociation of the mouse testis and characterization of isolated spermatogenic cells. J Histochem Cytochem 1977; 25:480-494.
45. Dym M, Jia MC, Dirami G, Price JM, Rabin SJ, Mocchetti I, Ravindranath N. Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Biol Reprod 1995; 52:8-19.
46. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual, 2nd ed. New York: Cold Spring Harbor Laboratory Press; 1989.
47. Aikawa J, Ikeda-Naiki S, Ohgane J, Min KS, Imamura T, Sasai K, Shiota K, Ogawa T. Molecular cloning of rat leukemia inhibitory factor receptor alpha-chain gene and its expression during pregnancy. Biochim Biophys Acta 1997; 1353:266-276.
48. Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S, Kunisada T, Fujimoto T. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 1991; 113:689-699.
49. Cuevas EC, Bateman AC, Wilkins BS, Johnson PA, Williams JH, Lee AH, Jones DB, Wright DH. Microwave antigen retrieval in immunocytochemistry: a study of 80 antibodies. J Clin Pathol 1994; 47:448-452.
50. Parvinen M, Soder O, Mali P, Froysa B, Ritzen EM. In vitro stimulation of stage-specific deoxyribonucleic acid synthesis in rat seminiferous tubule segments by interleukin-1 alpha. Endocrinology 1991; 129:1614-1620.
51. Parvinen M, Vanha-Perttula T. Identification and enzyme quantitation of the stages of the seminiferous epithelial wave in the rat. Anat Rec 1972; 174:435-449.
52. Moreau JF, Bonneville M, Godard A, Gascan H, Gruart V, Moore MA, Soulillou JP. Characterization of a factor produced by human T cell clones exhibiting eosinophil-activating and burst-promoting activities. J Immunol 1987; 138(11):3844-3849.
53. Toppari J, Parvinen M. In vitro differentiation of rat seminiferous tubular segments from defined stages of the epithelial cycle morphologic and immunolocalization analysis. J Androl 1985; 6:334-343.
54. Hakovirta H, Yan W, Kaleva M, Zhang F, Vanttinen K, Morris PL, Soder M, Parvinen M, Toppari J. Function of stem cell factor as a survival factor of spermatogonia and localization of messenger ribonucleic acid in the rat seminiferous epithelium. Endocrinology 1999; 140:1492-1498.
55. Jenab S, Morris PL. Testicular leukemia inhibitory factor (LIF) and LIF receptor mediate phosphorylation of signal transducers and activators of transcription (STAT)-3 and STAT-1 and induce c-fos transcription and activator protein-1 activation in rat Sertoli but not germ cells. Endocrinology 1998; 139:1883-1890.
56. Mauduit C, Goddard I, Besset V, Tabone E, Rey C, Gasnier F, Dacheux F, Benahmed M. Leukemia inhibitory factor antagonizes gonadotropin induced-testosterone synthesis in cultured porcine leydig cells: sites of action. Endocrinology 2001; 142:2509-2520.
57. de Rooij DG. Stem cells in the testis. Int J Exp Pathol 1998; 79:67-80.
58. Rossi P, Sette C, Dolci S, Geremia R. Role of c-kit in mammalian spermatogenesis. J Endocrinol Invest 2000; 23:609-615.
59. Albanesi C, Geremia R, Giorgio M, Dolci S, Sette C, Rossi P. A cell-and developmental stage-specific promoter drives the expression of a truncated c-kit protein during mouse spermatid elongation. Development 1996; 122:1291-1302.
60. Orth JM, Jester WF Jr, Qiu J. Gonocytes in testes of neonatal rats express the c-kit gene. Mol Reprod Dev 1996; 45:123-131.
61. Bugga L, Gadient RA, Kwan K, Stewart CL, Patterson PH. Analysis of neuronal and glial phenotypes in brains of mice deficient in leukemia inhibitory factor. J Neurobiol 1998; 36:509-524.
62. Bamberger AM, Schulte HM, Wullbrand A, Jung R, Beil FU, Bamberger CM. Expression of leukemia inhibitory factor (LIF) and LIF receptor (LIF-R) in the human adrenal cortex: implications for steroidogenesis. Mol Cell Endocrinol 2000; 162:145-149.
63. Jégou B, Pineau C, Dupaix A. Paracrine control of testis function. In: Wang C (ed.), Male Reproductive Function, vol. 5. Norwell, MA: Kluwer Academic Press; 1999:41-63.
64. Balkwill F. Cytokine amplification and inhibition of immune and inflammatory responses. J Viral Hepat 1997; 4(Suppl 2):6-15.
65. Masu Y, Wolf E, Holtmann B, Sendtner M, Brem G, Thoenen H. Disruption of the CNTF gene results in motor neuron degeneration. Nature 1993; 365:27-32.
66. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, Zinkernagel R, Bluethmann H, Kohler G. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994; 368:339-342.
67. Sendtner M, Gotz R, Holtmann B, Thoenen H. Endogenous ciliary neurotrophic factor is a lesion factor for axotomized motoneurons in adult mice. J Neurosci 1997; 17:6999-7006.
68. Oppenheim RW, Wiese S, Prevette D, Armanini M, Wang S, Houenou LJ, Holtmann B, Gotz R, Pennica D, Sendtner M. Cardiotrophin-1, a muscle-derived cytokine, is required for the survival of subpopulations of developing motoneurons. J Neurosci 2001; 21:1283-1291.