Analysis of neuronal and glial phenotypes in brains of mice deficient in leukemia inhibitory factor

Journal of Neurobiology

Volumn 36, Issue 4, 1998, Pages 509-524

  Bugga, Lakshmi ^a   Gadient, Reto A ^a   Kwan, Karen ^a,c   Stewart, Colin L ^b,d   Patterson, Paul H ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b HOFFMANN LA ROCHE INC   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

CNTF; Cytokine; Gp130; IL 6; LIF; Sexual dimorphism

Indexed keywords

ACETYLCHOLINESTERASE; CALBINDIN; CALCITONIN; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; CHOLINERGIC RECEPTOR; PARVALBUMIN; PROTEIN S 100; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL CULTURE; GENOTYPE; HIPPOCAMPUS; HISTOLOGY; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NIDATION; NONHUMAN; OLIGODENDROGLIA; PERINATAL DEATH; PHENOTYPE; PRIORITY JOURNAL; SEX DIFFERENCE; STATISTICAL ANALYSIS;

EID: 0031695876     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1097-4695(19980915)36:4<509::aid-neu5>3.0.co;2-%23     Document Type: Article

References (86)

1. AKITA, S., MALKIN, J., and MELMED, S. (1996). Disrupted murine leukemia inhibitory factor (LIF) gene attenuates adrenocorticotropic hormone (ACTH) secretion. Endocrinology 137:3140-3143.
2. 2+ currents. Glia 17:181-194.
3. ALOISI, F., ROSA, S., TEST, U., BONSI, P., RUSSON, G., PESCHLE, C., and LEVI, G. (1994). Regulation of leukemia inhibitory factor synthesis in cultured human astrocytes. J. Immunol. 152:5022-5031.
4. BAMBER, B. A., MASTERS, B. A., HOYLE, G. W., BRINSTER, R. L., and PALMITER, R. D. (1994). Leukemia inhibitory factor induces neurotransmitter switching in transgenic mice. Proc. Natl. Acad. Sci. USA 91:7839-7843.
5. BANNER, L. R., MOAYERI, N. N., and PATTERSON, P. H. (1997). Leukemia inhibitory factor is expressed in astrocytes following cortical injury. Exp. Neurol. 147: 1-9.
6. BANNER, L. R., and PATTERSON, P. H. (1994). Major changes in the expression of the mRNAs for CDF/LIF and its receptor after injury to adult peripheral nerves and ganglia. Proc. Natl. Acad. Sci. USA 91:7109-7113.
7. BARRES, B. A., BURNE, J. F., HOLTMANN, B., THOENEN, H., SENDTNER, M., and RAFF, M. C. (1996). Ciliary neurotrophic factor enhances the rate of oligodendrocyte generation. Mol. Cell. Neurosci. 8:146-156.
8. BENVENISTE, E. N. (1992). Cytokines: influence on glial cell gene expression and function. Chem. Immunol. 52:106-153.
9. BIANCHI, R., VERZINI, M., GARBUGLIA, M., GIAMBANCO, I., and DONATO, R. (1994). Mechanism of S100 protein-dependent inhibition of glial fibrillary acidic protein (GFAP) polymerization. Biochim. Biophys. Acta 1223:354-360.
10. CAMMER, W., ZHANG, H., and CAMMER, M. (1993). Glial cell abnormalities in the CNS of the carbonic anhydrase II deficient mutant mouse. J. Neurobiol. Sci. 118:1-9.
11. CHEEMA, S. S., RICHARDS, L. J., MURPHY, M., and BARTLETT, P. F. (1994). Leukaemia inhibitory factor rescues motoneurones from axotomy-induced cell death. Neuroreport 5:989-992.
12. CHENG, J. G., and PATTERSON, P. H. (1997). LIF is an autocrine factor for sympathetic neurons. Mol. Cell. Neurosci. 9:372-380.
13. CORNESS, J., SHI, T.-J., Xu, Z.-Q., BRULET, P., and HOKFELT, T. (1996). Influence of leukemia inhibitory factor on galanin/GMAP and neuropeptide Y expression in mouse primary sensory neurons after axotomy. Exp. Brain Res. 112:79-88.
14. CURTIS, R., SCHERER, S., SOMOGYI, R., ADRYAN, K. M., IP, N. Y., ZHU, Y., LINDSAY, R. M., and DISTEFANO, P. S. (1994). Retrograde axonal transport of LIF is increased by peripheral nerve injury: correlation with increased LIF expression in distal nerve. Neuron 12:191-204.
15. DECHIARA, T. M., VEJSADA, R., POUEYMIROU, W. T., ACHESON, A., SURI, C., CONOVER, J. C., FRIEDMAN, B., McCLAIN, J., PAN, L., STAHL, N., IP, N. Y., KATO, A., and YANCOPOULOS, G. D. (1995). Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth. Cell 83:313-322.
16. DOUPE, A. J., and PATTERSON, P. H. (1982). Glucocorticoids and the developing nervous system. In: D. Ganten and D. Pfaff, (Eds.) Current Topics in Neuroendocrinology. Springer-Verlag, New York, pp. 23-43.
17. ENG, L. F., and GHIRNIKAR, R. S. (1994). GFAP and astrogliosis. Brain Pathol. 4:229-237.
18. ESCARY, J. L., PERREAU, J., DUMENIL, D., EZINE, S., and BRULET, P. (1993). Leukemia inhibitory factor is necessary for maintenance of hematopoietic stem cells and thymocyte stimulation. Nature 363:361-364.
19. FAN, G. P., and KATZ, D. M. (1993). Non-neuronal cells inhibit catecholaminergic differentiation of primary sensory neurons: role of leukemia inhibitory factor. Development 118:83-93.
20. FANN, M. J., and PATTERSON, P. H. (1994). Depolarization differentially regulates the effects of bone morphogenetic protein (BMP)-2, BMP-6 and activin A on sympathetic neuronal phenotype. J. Neurochem. 63:2074-2079.
21. FUKADA, K. (1980). Hormonal control of neurotransmitter choice in sympathetic neurone cultures. Nature 287:553-555.
22. FUKADA, K. (1985). Purification and partial characterization of a cholinergic neuronal differentiation factor. Proc. Natl. Acad. Sci. USA 82:8795-8799.
23. GARCIA-SEGURA, L.-M., CHOWEN, J. A., DUENAS, M., PARDUCZ, A., and NAFTOLIN, F. (1996). Gonadal steroids and astroglial plasticity. Cell. Mol. Neurobiol. 16:225-237.
24. GARD, A. L., BURRELL, M. R., PFEIFFER, S. E., RUDGE, J. S., and WILLIAMS, W. C. II. (1995). Astroglial control of oligodendrocyte survival mediated by PDGF and leukemia inhibitory factor-like protein. Development 121:2187-2191.
25. GARY, K. A., and CHRONWALL, B. M. (1995). Regulation of GFAP expression in glial-like cells of the rat pituitary intermediate lobe by lactation, salt-loading, and adrenalectomy. Glia 13:272-282.
26. GEARING, D. P. (1993). The leukemia inhibitory factor and its receptor. Adv. Immunol. 53:31-58.
27. GINOVART, N., MARCEL, D., BEZIN, L., GAGNE, C., PUJOL, J. F., and WEISSMANN, D. (1996). Tyrosine hydroxylase expression within Balb/C and C57Black/6 mouse locus coeruleus. II. Quantitative study of the enzyme level. Brain Res. 719:45-55.
28. HENDRY, I. A., MURPHY, M., HILTON, D. J., NICOLA, N. A., and BARTLETT, P. F. (1992). Binding and retrograde transport of leukemia inhibitory factor by the sensory nervous system. J. Neurosci. 12:3427-3434.
29. Hsu, L. W., and HEATH, J. K. ( 1994). Identification of two elements involved in regulating expression of the murine leukaemia inhibitory factor gene. Biochem. J. 302:103-110.
30. HUGHES, R. A., SENDTNER, M., and THOENEN, H. (1993). Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J. Neurosci. Res. 36:663-671.
31. INAGAKI, M., NAKAMURA, Y., TAKEDA, M., NISHIMURA, T., and INAGAKI, N. (1994). Glial fibrillary acidic protein: dynamic property and regulation by phosphorylation. Brain Pathol. 4:239-243.
32. JONES, K. J., KINDERMAN, N. B., and OBLINGER, M. M. (1997). Alterations in glial fibrillary acidic protein (GFAP) mRNA levels in the hamster facial motor nucleus: effects of axotomy and testosterone. Neurochem. Res. 22:1359-1366.
33. KAHN, M. A., and DE VELLIS, J. (1994). Regulation of an oligodendrocyte progenitor cell line by the interleukin-6 family of cytokines. Glia 12:87-98.
34. KAHN, M. A., ELLISON, J. A., CHANG, R. P., SPEIGHT, G. J., and DE VELLIS, J. (1997). CNTF induces GFAP in a S-100 brain cell population: the pattern of CNTF-aR suggests an indirect mode of action. Dev. Brain Res. 98:221-233.
35. KAPRIELIAN, Z., and PATTERSON, P. H. (1993). Surface and cytoskeletal markers of rostrocaudal position in the mammalian nervous system. J. Neurosci. 13:2495-2508.
36. KATO, A. C., and LINDSAY, R. M. (1994). Overlapping and additive effects of neurotrophins and CNTF on cultured human spinal cord neurons. Exp. Neurol. 130:196-201.
37. KESSLER, J. A., LUDLAM, W. H., FREIDIN, M. M., HALL, D. H., MICHAELSON, M. D., SPRAY, D. C., DOUGHERTY, M., and BATTER, D. K. (1993). Cytokine-induced programmed death of cultured sympathetic neurons. Neuron 11:1123-1132.
38. KOTZBAUER, P. T., LAMPE, P. A., ESTUS, S., MILBRANDT, J., and JOHNSON, E. M. J. (1994). Postnatal development of survival responsiveness in rat sympathetic neurons to leukemia inhibitory factor and ciliary neurotrophic factor. Neuron 12:763-773.
39. LAPING, N. J., TETER, B., NICHOLS, N. R., ROZOVSKY, I., and FINCH, C. E. (1994). Glial fibrillary acidic protein: regulation by hormones, cytokines, and growth factors. Brain Pathol. 1:259-275.
40. LE Roux, P. D., and REH, T. A. (1994). Astroglia demonstrate regional differences in their ability to maintain primary dendritic outgrowth from mouse cortical neurons in vitro. J. Neurobiol. 27:97-112.
41. LEMKE, R., GADIENT, R. A., PATTERSON, P. H., BIGL, V., and SCHLIEBS, R. (1997). Leukemia inhibitory factor (LIF) mRNA-expressing neuronal subpopulations in adult rat forebrain. Neurosci. Lett. 229:69-71.
42. LEMKE, R., GADIENT, R. A., SCHLIEBS, R., BIGL, V., and PATTERSON, P. H. (1996). Neuronal expression of leukemia inhibitory factor (LIF) in the rat brain. Neurosci. Lett. 215:205-208.
43. LEVISON, S. W., and GOLDMAN, J. E. (1993). Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10:201-212.
44. LI, M., SENDTNER, M., and SMITH, A. (1995). Essential function of LIF receptor in motor neurons. Nature 378:724-727.
45. LUDLAM, W. H., ZANG, Z., MCCARSON, K. E., KRAUSE, J. E., SPRAY, D. C., and KESSLER, J. A. (1994). mRNAs encoding muscarinic and substance P receptors in cultured sympathetic neurons are differentially regulated by LIF or CNTF. Dev. Biol. 164:528-539.
46. MARTINOU, J., MARTTNOU, I., and KATO, A. C. (1992). Cholinergic differentiation factor (CDF/LIF) promotes survival of isolated rat embryonic motoneurons in vitro. Neuron 8:737-744.
47. MASU, Y., WOLF, E., HOLTMANN, B., SENDTNER, M., BREM, G., and THOENEN, H. (1993). Disruption of the CNTF gene results in motor neuron degeneration. Nature 365:27-32.
48. MAYER, M., BHAKOO, K., and NOBLE, M. (1994). Ciliary neurotrophic factor and leukemia inhibitory factor promote the generation, maturation and survival of oligodendrocytes in vitro. Development 120:143-153.
49. MCLENNAN, I. S., HILL, C. E., and HENDRY, I. A. (1980). Glucocorticoids modulate transmitter choice in developing superior cervical ganglion. Nature 283:206-207.
50. MERRILL, J. E., and BENVENISTE, E. N. (1996). Cytokines in inflammatory brain lesions: helpful and harmful. Trends Neurosci. 19:331-337.
51. MURPHY, M., REID, K., BROWN, M. A., and BARTLETT, P. F. (1993). Involvement of leukemia inhibitory factor and nerve growth factor in the development of dorsal root ganglion neurons. Development 117:1173-1182.
52. MURPHY, M., REID, K., HILTON, D. J., and BARTLETT, P. F. (1991). Generation of sensory neurons is stimulated by leukemia inhibitory factor. Proc. Natl. Acad. Sci. USA 88:3498-3501.
53. MURPHY, G. M. J., SONG, Y., ONG, E., LEE, Y. L., SCHMIDT, K. G., BOCCHINI, V., and ENG, L. F. (1995). Leukemia inhibitory factor mRNA is expressed in cortical astrocyte cultures but not in an immortalized microglial cell line. Neurosci. Lett. 184:48-51.
54. NAKAGAITO, Y., YOSHIDA, T., SATOH, M., and TAKEUCHI, M. (1995). Effects of leukemia inhibitory factor on the differentiation of astrocyte progenitor cells from embryonic mouse cerebral hemispheres. Dev. Brain Res. 87:220-223.
55. NAWA, H., and SAH, D. (1990). Different biological activities in conditioned media control the expression of a variety of neuropeptides in cultured sympathetic neurons. Neuron 4:279-287.
56. NAWA, H., YAMAMORI, T., LE, T., and PATTERSON, P. (1990). Generation of neuronal diversity: analogies and homologies with hematopoiesis. Cold Spring Harbor Symp. Quant. Biol. 55:247-253.
57. NAWA, H., NAKANISHI, S., and PATTERSON, P. (1991). Recombinant cholinergic differentiation factor (leukemia inhibitory factor) regulates sympathetic neuron phenotype by alterations in the size and amounts of neuropeptide mRNAs. J. Neurochem. 56:2147-2150.
58. NISHIYAMA, K., COLLODI, P., and BARNES, D. (1993). Regulation of glial fibrillary acidic protein in serumfree mouse embryo (SFME) cells by leukemia factor and related peptides. Neurosci. Lett. 163:114-116.
59. PATTERSON. P. H. (1994). Leukemia inhibitory factor, a cytokine at the interface between neurobiology and immunology. Proc. Natl. Acad. Sci. USA 91:7833-7835.
60. PATTERSON, P. H., Kou, S.-Y., SUGIURA, S., LAHAV, R., and BANNER, L. R. (1997). LIF coordinates neuronal and inflammatory responses to nerve injury. Soc. Neurosci. Abstr. 23:393.33.
61. PROCHIANTZ, A. (1995). Neuronal polarity: giving neurons heads and tails. Neuron 15:743-746.
62. QIAN, J., BULL, M. S., and LEVITT, P. (1992). Targetderived astroglia regulate axonal outgrowth in a region-specific manner. Dev. Biol. 149:278-294.
63. QIU, L., BERND, P., and FUKADA, K. (1994). Cholinergic neuronal differentiation factor (CDF) leukemia inhibitory factor (LIF) binds to specific regions of the developing nervous system in vivo. Dev. Biol. 163:516-520.
64. RAO, M. S., PATTERSON, P. H., and LANDIS, S. C. (1992). Multiple cholinergic differentiation factors are present in footpad extracts-comparison with known cholinergic factors. Development 116:731-744.
65. RAO, M. S., SUN, Y., ESCARY, J. L., PERREAU, J., TRESSER, S., PATTERSON, P. H., ZIGMOND, R. E., BRULET, P., and LANDIS, S. C. (1993). Leukemia inhibitory factor mediates an injury response but not a target-directed developmental transmitter switch in sympathetic neurons. Neuron 11:1175-1185.
66. RICHARDS, L. J., KILPATRICK, T. J., DUTTON, R., TAN, S.-S., GEARING, D. P., BARTLETT, P. F., and MURPHY, M. (1996). Leukaemia inhibitory factor or related factors promote the differentiation of neuronal and astrocytic precursors within the developing murine spinal cord. Eur. J. Neurosci. 8:291-299.
67. ROHRER, H. (1992). Cholinergic neuronal differentiation factors: evidence for the presence of both CNTF-like and non-CNTF-like factors in developing rat footpad. Development 114:689-698.
68. ROUSSELET, A., AUTILLO-TOUATI, A., ARAUD, D., and PROCHIANTZ, A. (1990). In vitro regulation of neuronal morphogenesis and polarity by astrocyte-derived factors. Dev. Biol. 137:33-45.
69. RUDGE, J. S., EATON, M. J., MATHER, P., LINDSAY, R. M., and WHITTEMORE, S. R. (1996). CNTF induces raphe neuronal precursors to switch from a serotonergic to a cholinergic phenotype in vitro. Mol. Cell. Neurosci. 7:204-221.
70. SENDTNER, M., GOTZ, R., HOLTMANN, B., ESCARY, J.-L., MASU, Y., CARROLL, P., WOLF, E., BREM, G., BRULET, P., and THOENEN, H. (1996). Cryptic physiological trophic support of motoneurons by LIF revealed by double gene targeting of CNTF and LIF. Curr. Biol. 6:686-694.
71. SHADIACK, A. M., HART, R. P., CARLSON, C. D., and JONAKAIT, G. M. (1993). Interleukin-1 induces substance P in sympathetic ganglia through the induction of leukemia inhibitory factor (LIF). J. Neurosci. 13:2601-2609.
72. STEWART, C. L., KASPAR, P., BRUNET, L. J., BHATT, H., GADI, I., KONTGEN, F., and ABBONDANZO, S. J. (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359:76-79.
73. SUN, Y., LANDIS, S. C., and ZIGMOND, R. E. (1996). Signals triggering the induction of leukemia inhibitory factor in sympathetic superior cervical ganglia and their nerve trunks after axonal injury. Mol Cell. Neurosci. 7:152-163.
74. SUN, Y., RAO, M., ZIGMOND, R. E., and LANDIS, S. C. (1994). Regulation of vasoactive intestinal peptide expression in sympathetic neurons in culture and after axotomy: the role of cholinergic differentiation factor/ leukemia inhibitory factor. J. Neurobiol. 25:415-430.
75. SUN. Y., and ZIGMOND, R. E. (1996a). Leukaemia inhibitory factor induced in the sciatic nerve after axotomy is involved in the induction of galanin in sensory neurons. Eur. J. Neurosci. 8:2213-2220.
76. SUN, Y., and ZIGMOND, R. E. (1996b). Involvement of leukemia inhibitory factor in the increases in galanin and vasoactive intestinal peptide mRNA and the decreases in neuropeptide Y and tyrosine hydroxylase mRNA in sympathetic neurons after axotomy. J. Neurochem. 67:1751-1760.
77. THALER, C. D., SUHR, L., IP, N., and KATZ, D. M. (1994). Leukemia inhibitory factor and neurotrophins support overlapping populations of rat nodose sensory neurons in culture. Dev. Biol. 161:338-344.
78. URE, D. R., and CAMPENOT, R. B. (1994). Leukemia inhibitory factor and nerve growth factor are retrogradely transported and processed by cultured rat sympathetic neurons. Dev. Biol. 162:339-347.
79. VEJSADA, R., SAGOT, Y., and KATO, A. C. (1995). Quantitative comparison of the transient rescue effects of neurotrophic factors on axotomized motoneurons in vivo. Eur. J. Neurosci. 7:108-115.
80. WARE, C. B., HOROWITZ, M. C., RENSHAW, B. R., HUNT, J. S., LIGGITT, D., KOBLAR, S. A., FLINIAK, B. C., MCKENNA, H. J., PAPAYANNOPOULOU, T., THOMA, B., CHENG, L., DONOVAN, P., PESCHON, J. J., BARTLETT, P. F., WILLIS, C. R., WRIGHT, B. D., CARPENTER, M. K., DAVIDSON, B. L., and GEARING, D. P. (1995). Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 121:1283-1299.
81. WESSELINGH, S. L., GOUGH, N. M., FINLAY-JONES, J. J., and Mc DONALD, P. J. (1990). Detection of cytokine mRNA in astrocyte cultures using the polymerase chain reaction. Lymphokine Res. 9:177-185.
82. WESTERGAARD, N., FOSMARK, H., and SCHOUSBOE, A. (1991). Metabolism and release of glutamate in cerebellar granule cells cocultured with astrocytes from cerebellum or cerebral cortex. J. Neurochem. 56: 59-66.
83. YAMAKUNI, H., MINAMI, M., and SATOH, M. (1996). Localization of mRNA for leukemia inhibitory factor receptor in the adult rat brain. J. Neuroimmunol. 70:45-53.
84. YAMAMORI, T. (1991). Localization of cholinergic differentiation factor/leukemia inhibitory factor mRNA in the rat brain and peripheral tissues. Proc. Natl. Acad. Sci. USA 88:7298-7302.
85. YAMAMORI, T., FUKADA, K., AEBERSOLD, R., KORSCHING, S., FANN, M.-J., and PATTERSON, P. H. (1989). The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science 246:1412-1416.
86. YOSHIDA, T., SATOH, M., NAKAGAITO, Y., KUNO, H., and TAKEUCHI, M. (1993). Cytokines affecting survival and differentiation of an astrocyte progenitor cell line. Dev. Brain Res. 76:147-150.