Lis1, the Drosophila homolog of a human lissencephaly disease gene, is required for germline cell division and oocyte differentiation

Development

Volumn 126, Issue 20, 1999, Pages 4477-4488

  Liu, Zhao ^a   Xie, Ting ^b   Steward, Ruth ^a  

^a RUTGERS UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Cell division; Cyst; Cytoskeleton; Drosophila; Fusome; Germline; LIS1; Lissencephaly

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE;

AGYRIA; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CELL MIGRATION; CYTOSKELETON; DROSOPHILA; GENE; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BRAIN; CELL DIFFERENTIATION; CELL DIVISION; CELL MOVEMENT; CLONING, MOLECULAR; DNA PRIMERS; DROSOPHILA; DROSOPHILA PROTEINS; DYNEIN ATPASE; FEMALE; GENES, INSECT; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR MOTOR PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; OOCYTES; PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY;

ASPERGILLUS; EMERICELLA NIDULANS; HEXAPODA;

EID: 0032693534     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Albrecht, U., Abu-Issa, R., Ratz, B., Hattori, M., Aoki, J., Arai, H., Inoue, K. and Eichele, G. (1996). Platelet-activating factor acetylhydrolase expression and activity suggest a link between neuronal migration and platelet-activating factor. Dev. Biol. 180, 579-593.
2. Ashburner, M. (1989). Drosophila A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
3. Beckwith, S. M., Roghi, C. H., Liu, B. and Ronald Morris, N. (1998). The "8-kD" cytoplasmic dynein light chain is required for nuclear migration and for dynein heavy chain localization in Aspergillus nidulans. J. Cell Biol. 143, 1239-1247.
4. Bito, H., Nakamura, M., Honda, Z., Izumi, T., Iwatsubo, T., Seyama, Y., Ogura, A., Kudo, Y. and Shimizu, T. (1992). Platelet-activating factor (PAF) receptor in rat brain: PAF mobilizes intracellular Ca2+ in hippocampal neurons. Neuron 9, 285-294.
5. Brown, N. H. and Kafatos, F. C. (1988). Functional cDNA libraries from Drosophila embryos. J. Mol. Biol. 203, 425-437.
6. Chou, T. B., Noll, E. and Perrimon, N. (1993). Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras. Development 119, 1359-1369.
7. Chou, T. B. and Perrimon, N. (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679.
8. de Cuevas, M., Lee, J. K. and Spradling, A. C. (1996). alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122, 3959-3968.
9. de Cuevas, M. and Spradling, A. C. (1998). Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125, 2781-2789.
10. Deng, W. and Lin, H. (1997). Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev. Biol. 189, 79-94.
11. des Portes, V., Pinard, J. M., Billuart, P., Vinet, M. C., Koulakoff, A., Carrie, A., Gelot, A., Dupuis, E., Motte, J., Berwald-Netter, Y. et al. (1998). A novel CNS gene required for neuronal migration and involved in X- linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92, 51-61.
12. Dieker, H. (1967). [Studies on the genetics of particularly regular high alpha-waves in human EEG]. Humangenetik 4, 189-216.
13. Dobyns, W. B. (1989). The neurogenetics of lissencephaly. Neurol. Clin. 7, 89-105.
14. Geiser, J. R., Schott, E. J., Kingsbury, T. J., Cole, N. B., Totis, L. J., Bhattacharyya, G., He, L. and Hoyt, M. A. (1997). Saccharomyces cerevisiae genes required in the absence of the CIN8-encoded spindle motor act in functionally diverse mitotic pathways. Mol. Biol. Cell. 8, 1035-1050.
15. Gleeson, J. G., Allen, K. M., Fox, J. W., Lamperti, E. D., Berkovic, S., Scheffer, I., Cooper, E. C., Dobyns, W. B., Minnerath, S. R., Ross, M. E. et al. (1998). Doublecortin, a brain-specific gene mutated in human X- linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92, 63-72.
16. Golic, K. G. and Lindquist, S. (1989). The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499-509.
17. Hattori, M., Adachi, H., Tsujimoto, M., Arai, H. and Inoue, K. (1994). Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase [corrected] [published erratum appears in Nature 1994 Aug 4;370(6488):391]. Nature 370, 216-218.
18. Hirotsune, S., Fleck, M. W., Gambello, M. J., Bix, G. J., Chen, A., Clark, G. D., Ledbetter, D. H., McBain, C. J. and Wynshaw-Boris, A. (1998). Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat. Genet. 19, 333-339.
19. Ho, Y. S., Swenson, L., Derewenda, U., Serre, L., Wei, Y., Dauter, Z., Hattori, M., Adachi, T., Aoki, J., Arai, H. et al. (1997) Brain acetylhydrolase that inactivates platelet-activating factor is a G-protein-like trimer. Nature 385, 89-93.
20. Holleran, E. A., Tokito, M. K., Karki, S. and Holzbaur, E. L. (1996). Centractin (ARP1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles. J. Cell Biol. 135, 1815-1829.
21. Kornecki, E. and Ehrlich, Y. H. (1988). Neuroregulatory and neuropathological actions of the ether-phospholipid platelet-activating factor. Science 240, 1792-1794.
22. Lewis, E. B. and Bacher, F. (1968). Method of feeding ethyl methane sulfonate (EMS) to Drosophila males. Dros. Inf. Serv. 43, 193.
23. Lin, H. and Spradling, A. C. (1995). Fusome asymmetry and oocyte determination in Drosophila. Dev. Genet. 16, 6-12.
24. Lin, H. and Spradling, A. C. (1997). A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124, 2463-2476.
25. Lin, H., Yue, L. and Spradling, A. C. (1994). The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120, 947-956.
26. Lo Nigro, C., Chong, C. S., Smith, A. C., Dobyns, W. B., Carrozzo, R. and Ledbetter, D. H. (1997). Point mutations and an intragenic deletion in LIS1, the lissencephaly causative gene in isolated lissencephaly sequence and Miller-Dieker syndrome. Hum. Mol. Genet. 6, 157-164.
27. Marcheselli, V. L. and Bazan, N. G. (1994). Platelet-activating factor is a messenger in the electroconvulsive shock-induced transcriptional activation of c-fos and zif-268 in hippocampus. J. Neurosci. Res. 37, 54-61.
28. McGrail, M., Gepner, J., Silvanovich, A., Ludmann, S., Serr, M. and Hays, T. S. (1995). Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex. J. Cell Biol. 131, 411-425.
29. McGrail, M. and Hays, T. S. (1997). The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124, 2409-2419.
30. McKearin, D. (1997). The Drosophila fusome, organelle biogenesis and germ cell differentiation: if you build it. BioEssays 19, 147-152.
31. McKearin, D. and Ohlstein, B. (1995). A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 121, 2937-2947.
32. Miller, J. Q. (1963). Lissencephaly in 2 siblings. Neurology 13, 841-850.
33. Mizuguchi, M., Takashima, S., Kakita, A., Yamada, M. and Ikeda, K. (1995). Lissencephaly gene product. Localization in the central nervous system and loss of immunoreactivity in Miller-Dieker syndrome. Am. J. Pathol. 147, 1142-1151.
34. Morris, N. R., Efimov, V. P. and Xiang, X. (1998a). Nuclear migration, nucleokinesis and lissencephaly. Trends Cell Biol. 8, 467-470.
35. Morris, S. M., Albrecht, U., Reiner, O., Eichele, G. and Yu-Lee, L. (1998b). The lissencephaly gene product Lis1, a protein involved in neuronal migration, interacts with a nuclear movement protein. NudC. Curr. Biol. 8, 603-606.
36. Neer, E. J., Schmidt, C. J. and Smith, T. (1993). LIS is more [news]. Nat. Genet. 5, 3-4.
37. Osmani, A. H., Osmani, S. A. and Morris, N. R. (1990). The molecular cloning and identification of a gene product specifically required for nuclear movement in Aspergillus nidulans. J. Cell Biol. 111, 543-551.
38. Pirrotta, V. (1988). Vectors for P-mediated transformation in Drosophila. In Vectors, a Survey of Molecular Cloning Vectors and their Uses, (ed. R. L. Rodriguez, and D. T. Denhardt), pp. 437-456. Boston: Butterworths.
39. Plamann, M., Minke, P. F., Tinsley, J. H. and Bruno, K. S. (1994). Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127, 139-149.
40. Reiner, O., Carrozzo, R., Shen, Y., Wehnert, M., Faustinella, F., Dobyns, W. B., Caskey, C. T. and Ledbetter, D. H. (1993). Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364, 717-721.
41. Robb, M. J., Wilson, M. A. and Vierula, P. J. (1995). A fungal actin-related protein involved in nuclear migration. Mol. Gen. Genet. 247, 583-590.
42. Robinson, D. N., Cant, K. and Cooley, L. (1994). Morphogenesis of Drosophila ovarian ring canals. Development 120, 2015-2025.
43. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory. New York: Cold Spring Harbor Laboratory Press.
44. Sapir, T., Elbaum, M. and Reiner, O. (1997). Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. EMBO J. 16, 6977-6984.
45. Saxton, W. M., Hicks, J., Goldstein, L. S. and Raff, E. C. (1991). Kinesin heavy chain is essential for viability and neuromuscular functions in Drosophila, but mutants show no defects in mitosis. Cell 64, 1093-1102.
46. Spradling, A. C. (1993). Developmental genetics of oogenesis. In The Development of Drosophila melanogaster. (ed. M. Bate and A. Martinez-Arias), pp. 1-70. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
47. Spradling, A. C. and Rubin, G. M. (1982). Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341-347.
48. Stroumbakis, N. D., Li, Z. and Tolias, P. P. (1994). RNA- and single-stranded DNA-binding (SSB) proteins expressed during Drosophila melanogaster oogenesis: a homolog of bacterial and eukaryotic mitochondrial SSBs. Gene 143, 171-177.
49. Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81-85.
50. Theurkauf, W. E., Alberts, B. M., Jan, Y. N. and Jongens, T. A. (1993) A central role for microtubules in the differentiation of Drosophila oocytes. Development 118, 1169-1180.
51. Tinsley, J. H., Minke, P. F., Bruno, K. S. and Plamann, M. (1996). p150glued, the largest subunit of the dynactin complex, is nonessential in Neurospora but required for nuclear distribution. Mol. Biol. Cell 7, 731-742.
52. Vallari, D. S., Record, M. and Snyder, F. (1990). Conversion of alkylacetylglycerol to platelet-activating factor in HL-60 cells and subcellular localization of the mediator. Arch. Biochem. Biophys. 276, 538-545.
53. Venable, M. E., Zimmerman, G. A., McIntyre, T. M. and Prescott, S. M. (1993). Platelet-activating factor: a phospholipid autacoid with diverse actions. J. Lipid Res. 34, 691-702.
54. Wang, D. S., Shaw, R., Hattori, M., Arai, H., Inoue, K. and Shaw, G. (1995). Binding of pleckstrin homology domains to WD40/beta-transducin repeat containing segments of the protein product of the Lis-1 gene. Biochem. Biophys. Res. Commun. 209, 622-629.
55. Willins, D. A., Liu, B., Xiang, X. and Morris, N. R. (1997). Mutations in the heavy chain of cytoplasmic dynein suppress the nudF nuclear migration mutation of Aspergillus nidulans. Mol. Gen. Genet. 255, 194-200.
56. Xiang, X., Beckwith, S. M. and Morris, N. R. (1994). Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 91, 2100-2104.
57. Xiang, X., Osmani, A. H., Osmani, S. A., Xin, M. and Morris, N. R. (1995) NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell 6, 297-310.
58. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
59. Yue, L. and Spradling, A. C. (1992). hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev. 6, 2443-2454.
60. Zaccai, M. and Lipshitz, H. D. (1996). Differential distributions of two adducin-like protein isoforms in the Drosophila ovary and early embryo. Zygote 4, 159-166.