Maternal Leukemia Inhibitory Factor (LIF) promotes fetal neurogenesis via a LIF-ACTH-LIF signaling relay pathway

Endocrinology

Volumn 151, Issue 4, 2010, Pages 1853-1862

  Simamura, Eriko ^a   Shimada, Hiroki ^a   Higashi, Nobuaki ^a   Uchishiba, Maimi ^a   Otani, Hiroki ^b   Hatta, Toshihisa ^a  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

^b SHIMANE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN; GLYCOPROTEIN; GLYCOPROTEIN 130; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL PROLIFERATION; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; CORTICOTROPIN RELEASE; FEMALE; FETUS; FETUS DEVELOPMENT; GESTATION PERIOD; MOTHER FETUS RELATIONSHIP; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STEM CELL; SYNCYTIOTROPHOBLAST;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; CELL LINE; CELLS, CULTURED; CYTOKINE RECEPTOR GP130; ENZYME-LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTES; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNOHISTOCHEMISTRY; LEUKEMIA INHIBITORY FACTOR; MATERNAL-FETAL EXCHANGE; NEUROGENESIS; PITUITARY GLAND; PITUITARY-ADRENAL SYSTEM; PLACENTA; PREGNANCY; PRO-OPIOMELANOCORTIN; RATS; RATS, WISTAR; RECEPTORS, OSM-LIF; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS; TROPHOBLASTS;

EID: 77950235518     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-0985     Document Type: Article

References (51)

1. Ratajczak J, Machaliński B, Marlicz W, Halasa M, Ratajczak MZ 1997 Influence of leukemia inhibitory factor (LIF) on the survival, proliferation and differentiation of human erythroid progenitor cells. In vitro studies under serum free conditions. Folia Histochem Cytobiol 35:63-68
2. Metcalf D 1997 Murine hematopoietic stem cells committed to macrophage/dendritic cell formation: stimulation by Flk2-ligand with enhancement by regulators using the gp130 receptor chain. Proc Natl Acad Sci USA 94:11552-11556
3. Oshima K, Teo DT, Senn P, Starlinger V, Heller S 2007 LIF promotes neurogenesis and maintains neural precursors in cell populations derived from spiral ganglion stem cells. BMC Dev Biol 7:112
4. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T 1999 Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284:479-482
5. Nakashima K, Wiese S, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Yoshida K, Kishimoto T, Sendtner M, Taga T 1999 Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. J Neurosci 19:5429-5434
6. Bauer S 2009 Cytokine control of adult neural stem cells. Ann NY Acad Sci 1153:48-56
7. Hsu YC, Lee DC, Chiu IM 2007 Neural stem cells, neural progenitors, and neurotrophic factors. Cell Transplant 16:133-150
8. Hatta T, Moriyama K, Nakashima K, Taga T, Otani H 2002 The role of gp130 in cerebral cortical development: in vivo functional analysis in a mouse exo utero system. J Neurosci 22:5516-5524
9. Kaufman MK 1992 The atlas of mouse development. London: Academic Press
10. Angevine Jr JB, Sidman RL 1961 Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766-768
11. Hatta T, Matsumoto A, Ono A, Udagawa J, Nimura M, Hashimoto R, Otani H 2006 Quantitative analyses of leukemia inhibitory factor in the cerebrospinal fluid in mouse embryos. Neuroreport 17:1863-1866
12. Altman J, Bayer AS 1995 Atlas of prenatal rat brain development. Boca Raton, FL: CRC Press
13. Gasser UE, Hatten ME 1990 Neuron-glia interactions of rat hippocampal cells in vitro: glial-guided neuronal migration and neuronal regulation of glial differentiation. J Neurosci 10:1276-1285
14. Nimura M, Udagawa J, Hatta T, Hashimoto R, Otani H 2006 Spatial and temporal patterns of expression of melanocortin type 2 and 5 receptors in the fetal mouse tissues and organs. Anat Embryol (Berl) 211:109-117
15. Assali NS, Hamermesz J 1954 Adrenocorticotropic substances from human placenta. Endocrinology 55:561-567
16. Jansen PM, de Jong IW, Hart M, Kim KJ, Aarden LA, Hinshaw LB, Taylor Jr FB, Hack CE 1996 Release of leukemia inhibitory factor in primate sepsis. Analysis of the role of TNF-α. J Immunol 156:4401-4407
17. Couly GF, Le Douarin NM 1985 Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol 110:422-439
18. Nemeskéri A, Sétáló G, Halász B 1988 Ontogenesis of the three parts of the fetal rat adenohypophysis. A detailed immunohistochemical analysis. Neuroendocrinology 48:534-543
19. René F, Hindelang C, Vuillez P, Plante M, Klein MJ, Félix JM, Stoeckel ME 1993 Morphofunctional aspects of melanotrophic cells developing in situ and in vitro. Ann NY Acad Sci 680:89-110
20. Pintar JE, Lugo DI 1987 Proopiomelanocortin gene expression, prohormone processing, and secretion during rat pituitary development. Ann NY Acad Sci 512:318-327
21. Lugo DI, Roberts JL, Pintar JE 1989 Analysis of proopiomelanocortin gene expression during prenatal development of the rat pituitary gland. Mol Endocrinol 3:1313-1324
22. Jailer JW, Knowlton AI 1950 Simulated adreno-cortical activity during pregnancy in an Addisonian patient. J Clin Invest 29:1430-1436
23. Raffin-Sanson ML, de Keyzer Y, Bertagna X 2003 Proopiomelanocortin, a polypeptide precursor with multiple functions: from physiology to pathological conditions. Eur J Endocrinol 149:79-90
24. Beloosesky R, Gayle DA, Amidi F, Ahanya SN, Desai M, Ross MG 2006 Ontogenic expression of putative feeding peptides in the rat fetal brain and placenta. Nutr Neurosci 9:33-40
25. Waddell BJ, Burton PJ 1993 Release of bioactive ACTH by perifused human placenta at early and late gestation. J Endocrinol 136:345-353
26. Kojima K, Kanzaki H, Iwai M, Hatayama H, Fujimoto M, Narukawa S, Higuchi T, Kaneko Y, Mori T, Fujita J 1995 Expression of leukaemia inhibitory factor (LIF) receptor in human placenta: a possible role for LIF in the growth and differentiation of trophoblasts. Hum Reprod 10:1907-1911
27. Yang ZM, Le SP, Chen DB, Yasukawa K, Harper MJ 1995 Expression patterns of leukaemia inhibitory factor receptor (LIFR) and the gp130 receptor component in rabbit uterus during early pregnancy. J Reprod Fertil 103:249-255
28. Sawai K, Matsuzaki N, Kameda T, Hashimoto K, Okada T, Shimoya K, Nobunaga T, Taga T, Kishimoto T, Saji F 1995 Leukemia inhibitory factor produced at the fetomaternal interface stimulates chorionic gonadotropin production: its possible implication during pregnancy, including implantation period. J Clin Endocrinol Metab 80:1449-1456
29. Takahashi Y, Carpino N, Cross JC, Torres M, Parganas E, Ihle JN 2003 SOCS3: an essential regulator of LIF receptor signaling in trophoblast giant cell differentiation. EMBO J 22:372-384
30. Ray DW, Ren SG, Melmed S 1996 Leukemia inhibitory factor (LIF) stimulates proopiomelanocortin (POMC) expression in a corticotroph cell line. Role of STAT pathway. J Clin Invest 97:1852-1859
31. Akita S, Webster J, Ren SG, Takino H, Said J, Zand O, Melmed S 1995 Human and murine pituitary expression of leukemia inhibitory factor. Novel intrapituitary regulation of adrenocorticotropin hormone synthesis and secretion. J Clin Invest 95:1288-1298
32. Stickrod G 1981 In utero injection of rat fetuses. Physiol Behav 27:557-558
33. West MJ, Slomianka L, Gundersen HJ 1991 Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497
34. Faria TN, Soares MJ 1991 Trophoblast cell differentiation: establishment, characterization, and modulation of a rat trophoblast cell line expressing members of the placental prolactin family. Endocrinology 129:2895-2906
35. Soares MJ, Hunt JS 2005 Placenta and trophoblast-methods and protocols. Totowa, NJ: Humana Press
36. Hilton DJ, Nicola NA, Waring PM, Metcalf D 1991 Clearance and fate of leukemia-inhibitory factor (LIF) after injection into mice. J Cell Physiol 148:430-439
37. Faria TN, Ogren L, Talamantes F, Linzer DI, Soares MJ 1991 Localization of placental lactogen-I in trophoblast giant cells of the mouse placenta. Biol Reprod 44:327-331
38. Petraglia F, Sawchenko PE, Rivier J, Vale W 1987 Evidence for local stimulation of ACTH secretion by corticotropin-releasing factor in human placenta. Nature 328:717-719
39. Pitard V, Lorgeot V, Taupin JL, Aubard Y, Praloran V, Moreau JF 1998 The presence in human serum of a circulating soluble leukemia inhibitory factor receptor (sgp190) and its evolution during pregnancy. Eur Cytokine Netw 9:599-605
40. Shimon I, Yan X, Ray DW, Melmed S 1997 Cytokine-dependent gp130 receptor subunit regulates human fetal pituitary adrenocorticotropin hormone and growth hormone secretion. J Clin Invest 100:357-363
41. Aikawa J, Ikeda-Naiki S, Ohgane J, Min KS, Imamura T, Sasai K, Shiota K, Ogawa T 1997 Molecular cloning of rat leukemia inhibitory factor receptor α-chain gene and its expression during pregnancy. Biochim Biophys Acta 1353:266-276
42. Chambers I, Cozens A, Broadbent J, Robertson M, Lee M, Li M, Smith A 1997 Structure of the mouse leukaemia inhibitory factor receptor gene: regulated expression of mRNA encoding a soluble receptor isoform from an alternative 5′ untranslated region. Biochem J 328(Pt 3):879-888
43. Ni H, Ding NZ, Harper MJ, Yang ZM 2002 Expression of leukemia inhibitory factor receptor and gp130 in mouse uterus during early pregnancy. Mol Reprod Dev 63:143-150
44. Li R, Hartley L, Robb L 2001 Cloning of rat interleukin 11 and interleukin 11 receptor α chain and analysis of their expression in rat uterus in the peri-implantation period. Reproduction 122:593-600
45. bright natural killer cells in the human early pregnancy decidua. Int Immunol 5:559-563
46. Auernhammer CJ, Chesnokova V, Bousquet C, Melmed S 1998 Pituitary corticotroph SOCS-3: novel intracellular regulation of leukemia-inhibitory factor-mediated proopiomelanocortin gene expression and adrenocorticotropin secretion. Mol Endocrinol 12:954-961
47. Starr R, Willson TA, Viney EM, Murray LJ, Rayner JR, Jenkins BJ, Gonda TJ, Alexander WS, Metcalf D, Nicola NA, Hilton DJ 1997 A family of cytokine-inducible inhibitors of signalling. Nature 387:917-921
48. Kurek JB, Austin L, Cheema SS, Bartlett PF, Murphy M 1996 Upregulation of leukaemia inhibitory factor and interleukin-6 in transected sciatic nerve and muscle following denervation. Neuromuscul Disord 6:105-114
49. Lagneaux L, Delforge A, Snoeck R, Bosmans E, Moreau JF, Taupin JL, De Clercq E, Stryckmans P, Bron D 1996 Human cytomegalovirus increases constitutive production of interleukin-6 and leukemia inhibitory factor by bone marrow stromal cells. Blood 87:59-66
50. Larroque B, Ancel PY, Marret S, Marchand L, André M, Arnaud C, Pierrat V, Rozé JC, Messer J, Thiriez G, Burguet A, Picaud JC, Bréart G, Kaminski M 2008 Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet 371:813-820
51. Mueller BR, Bale TL 2008 Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28: 9055-9065