Asymmetric cell division during animal development (original) (raw)

References

1. Horvitz, H. R. & Herskowitz, I. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68, 237–255 (1992).
   Article CAS PubMed Google Scholar
2. Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64–119 ( 1983).
   CAS PubMed Google Scholar
3. Guo, S. & Kemphues, K. J. Molecular genetics of asymmetric cleavage in the early Caenorhabditis elegans embryo. Curr. Opin. Genet. Dev. 6, 408–415 (1996).
   CAS PubMed Google Scholar
4. Kemphues, K. PARsing embryonic polarity. Cell 101, 345 –348 (2000).
   CAS PubMed Google Scholar
5. Rose, L. S. & Kemphues, K. J. Early patterning of the C. elegans embryo. Annu. Rev. Genet. 32, 521–545 (1998).
   CAS PubMed Google Scholar
6. Schubert, C. M., Lin, R., de Vries, C. J., Plasterk, R. H. & Priess, J. R. MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Mol. Cell 5, 671–682 (2000).
   CAS PubMed Google Scholar
7. Kemphues, K. J., Priess, J. R., Morton, D. G. & Cheng, N. S. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311– 320 (1988).This report describes the identification of PAR genes, which turned out to be a conserved machinery for orientating asymmetric cell division.
   CAS PubMed Google Scholar
8. Etemad-Moghadam, B., Guo, S. & Kemphues, K. J. Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos . Cell 83, 743–752 (1995).
   CAS PubMed Google Scholar
9. Hung, T. J. & Kemphues, K. J. PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos . Development 126, 127– 135 (1999).
   CAS PubMed Google Scholar
10. Tabuse, Y. et al. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125, 3607–3614 ( 1998).
    CAS PubMed Google Scholar
11. Watts, J. L. et al. par-6, a gene involved in the establishment of asymmetry in early C. elegans embryos, mediates the asymmetric localization of PAR-3. Development 122, 3133– 3140 (1996).
    CAS PubMed Google Scholar
12. Cheng, N. N., Kirby, C. M. & Kemphues, K. J. Control of cleavage spindle orientation in Caenorhabditis elegans: the role of the genes par-2 and par-3. Genetics 139, 549–559 ( 1995).
    CAS PubMed PubMed Central Google Scholar
13. Boyd, L., Guo, S., Levitan, D., Stinchcomb, D. T. & Kemphues, K. J. PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos . Development 122, 3075– 3084 (1996).
    CAS PubMed Google Scholar
14. Guo, S. & Kemphues, K. J. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611–620 (1995). This report describes the cloning of PAR-1, the first asymmetrically segregating protein in C. elegans.
    CAS PubMed Google Scholar
15. Hirata, J., Nakagoshi, H., Nabeshima, Y. & Matsuzaki, F. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 377, 627– 630 (1995).
    CAS PubMed Google Scholar
16. Knoblich, J. A., Jan, L. Y. & Jan, Y. N. Asymmetric segregation of Numb and Prospero during cell division. Nature 377, 624– 627 (1995).
    CAS PubMed Google Scholar
17. Spana, E. P. & Doe, C. Q. The Prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121, 3187– 3195 (1995).
    CAS PubMed Google Scholar
18. Li, P., Yang, X., Wasser, M., Cai, Y. & Chia, W. Inscuteable and Staufen mediate asymmetric localization and segregation of Prospero RNA during Drosophila neuroblast cell divisions. Cell 90, 437–447 ( 1997).
    CAS PubMed Google Scholar
19. Broadus, J., Fuerstenberg, S. & Doe, C. Q. Staufen-dependent localization of Prospero mRNA contributes to neuroblast daughter-cell fate. Nature 391, 792–795 (1998).
    CAS PubMed Google Scholar
20. Schuldt, A. J. et al. Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 12, 1847–1857 (1998).
    CAS PubMed PubMed Central Google Scholar
21. Shen, C. P., Jan, L. Y. & Jan, Y. N. Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell 90, 449–458 (1997).
    Article CAS PubMed Google Scholar
22. Ikeshima-Kataoka, H., Skeath, J. B., Nabeshima, Y., Doe, C. Q. & Matsuzaki, F. Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature 390, 625–629 ( 1997).
    Article CAS PubMed Google Scholar
23. Rhyu, M. S., Jan, L. Y. & Jan, Y. N. Asymmetric distribution of Numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells . Cell 76, 477–491 (1994). The first report describing an asymmetrically segregating determinant during somatic cell division.
    CAS PubMed Google Scholar
24. Lu, B., Rothenberg, M., Jan, L. Y. & Jan, Y. N. Partner of Numb colocalizes with Numb during mitosis and directs Numb asymmetric localization in Drosophila neural and muscle progenitors. Cell 95, 225–235 ( 1998).
    CAS PubMed Google Scholar
25. Vaessin, H. et al. prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 67, 941– 953 (1991).
    CAS PubMed Google Scholar
26. Doe, C. Q., Chu-LaGraff, Q., Wright, D. M. & Scott, M. P. The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 65, 451– 464 (1991).
    CAS PubMed Google Scholar
27. Uemura, T., Shepherd, S., Ackerman, L., Jan, L. Y. & Jan, Y. N. numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58, 349–360 ( 1989).
    CAS PubMed Google Scholar
28. Carmena, A., Murugasu-Oei, B., Menon, D., Jimenez, F. & Chia, W. Inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev. 12, 304–315 ( 1998).
    CAS PubMed PubMed Central Google Scholar
29. Buescher, M. et al. Binary sibling neuronal cell fate decisions in the Drosophila embryonic central nervous system are nonstochastic and require inscuteable -mediated asymmetry of ganglion mother cells. Genes Dev. 12, 1858–1870 (1998).
    CAS PubMed PubMed Central Google Scholar
30. Ruiz Gomez, M. & Bate, M. Segregation of myogenic lineages in Drosophila requires numb. Development 124, 4857–4866 ( 1997).
    CAS PubMed Google Scholar
31. Park, M., Yaich, L. E. & Bodmer, R. Mesodermal cell fate decisions in Drosophila are under the control of the lineage genes numb, notch, and sanpodo. Mech. Dev. 75, 117– 126 (1998).
    CAS PubMed Google Scholar
32. Spana, E. P., Kopczynski, C., Goodman, C. S. & Doe, C. Q. Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS. Development 121, 3489–3494 (1995).
    CAS PubMed Google Scholar
33. Guo, M., Jan, L. Y. & Jan, Y. N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17, 27–41 (1996).
    PubMed Google Scholar
34. Frise, E., Knoblich, J. A., Younger-Shepherd, S., Jan, L. Y. & Jan, Y. N. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell–cell interaction in sensory organ lineage. Proc. Natl Acad. Sci. USA 93, 11925–11932 (1996).
    CAS PubMed PubMed Central Google Scholar
35. Kraut, R., Chia, W., Jan, L. Y., Jan, Y. N. & Knoblich, J. A. Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 383, 50–55 (1996). Describes the first protein that couples determinant segregation to spindle orientation and seems to establish the axis of polarity.
    CAS PubMed Google Scholar
36. Kraut, R. & Campos-Ortega, J. A. inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adaptor protein. Dev. Biol. 174, 65– 81 (1996).
    CAS PubMed Google Scholar
37. Kaltschmidt, J. A., Davidson, C. M., Brown, N. H. & Brand, A. H. Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nature Cell Biol. 2, 7–12 (2000). [PubMed]
    CAS PubMed Google Scholar
38. Schober, M., Schaefer, M. & Knoblich, J. A. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 402, 548–551 (1999).
    CAS PubMed Google Scholar
39. Wodarz, A., Ramrath, A., Kuchinke, U. & Knust, E. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402, 544– 547 (1999). References 38 and 39 reveal a potential mechanism that orients asymmetric cell division along one of the body axis, in this case the apical–basal axis.
    CAS PubMed Google Scholar
40. Kuchinke, U., Grawe, F. & Knust, E. Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Curr. Biol. 8, 1357–1365 (1998).
    CAS PubMed Google Scholar
41. Muller, H. A. & Wieschaus, E. armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila . J. Cell Biol. 134, 149– 163 (1996).
    CAS PubMed Google Scholar
42. Petronczki, M. & Knoblich, J. A. DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila . Nature Cell Biol. 3, 43– 49 (2001).
    CAS PubMed Google Scholar
43. Wodarz, A., Ramrath, A., Grimm, A. & Knust, E. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150, 1361–1374 (2000).
    CAS PubMed PubMed Central Google Scholar
44. Fuerstenberg, S., Peng, C. Y., Alvarez-Ortiz, P., Hor, T. & Doe, C. Q. Identification of Miranda protein domains regulating asymmetric cortical localization, cargo binding, and cortical release. Mol. Cell. Neurosci. 12, 325– 339 (1998).
    CAS PubMed Google Scholar
45. Joberty, G., Petersen, C., Gao, L. & Macara, I. G. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nature Cell Biol. 2, 531–539 (2000). [PubMed]
    CAS PubMed Google Scholar
46. Johansson, A., Driessens, M. & Aspenstrom, P. The mammalian homologue of the Caenorhabditis elegans polarity protein PAR-6 is a binding partner for the Rho GTPases Cdc42 and Rac1. J. Cell Sci. 113, 3267– 3275 (2000).
    CAS PubMed Google Scholar
47. Lin, D. et al. A mammalian PAR-3–PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nature Cell Biol. 2, 540–547 (2000). [PubMed]
    CAS PubMed Google Scholar
48. Qiu, R. G., Abo, A. & Martin, G. S. A human homolog of the C. elegans polarity determinant Par-6 links Rac and Cdc42 to PKCζ signaling and cell transformationM . Curr. Biol. 10, 697–707 (2000).
    CAS PubMed Google Scholar
49. Brazil, D. B. & Hemmings, B. A. Cell polarity: Scaffold proteins par excellence. Curr. Biol. 10, R592– R594 (2000).
    CAS PubMed Google Scholar
50. Izumi, Y. et al. An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J. Cell Biol. 143, 95–106 (1998).
    CAS PubMed PubMed Central Google Scholar
51. Jantsch-Plunger, V. et al. CYK-4. A rho family GTPase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 149, 1391–1404 (2000).
    CAS PubMed PubMed Central Google Scholar
52. Goldstein, B. Cell contacts orient some cell division axes in the Caenorhabditis elegans embryo. J. Cell Biol. 129, 1071– 1080 (1995).
    CAS PubMed Google Scholar
53. Thorpe, C. J., Schlesinger, A., Carter, J. C. & Bowerman, B. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 90, 695– 705 (1997).
    CAS PubMed Google Scholar
54. Schlesinger, A., Shelton, C. A., Maloof, J. N., Meneghini, M. & Bowerman, B. Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev. 13, 2028–2038 ( 1999).
    CAS PubMed PubMed Central Google Scholar
55. Gho, M. & Schweisguth, F. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila . Nature 393, 178–181 (1998). This report describes a connection between asymmetric cell division and planar polarity and shows the function of Frizzled in establishing this connection.
    CAS PubMed Google Scholar
56. Roegiers, F., Younger-Shepherd, S., Jan, L. Y. & Jan, Y. N. The sensory organ precursor cell lineage in Drosophila contains two types of asymmetric divisions. Nature Cell Biol. 3, 58–67 (2001).
    CAS PubMed Google Scholar
57. Bray, S. Planar polarity: out of joint? Curr. Biol. 10, R155–R158 (2000).
    CAS PubMed Google Scholar
58. Shulman, J. M., Perrimon, N. & Axelrod, J. D. Frizzled signaling and the developmental control of cell polarity. Trends Genet. 14, 452– 458 (1998).
    CAS PubMed Google Scholar
59. Vinson, C. R., Conover, S. & Adler, P. N. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338, 263–264 ( 1989).
    CAS PubMed Google Scholar
60. Strutt, D. I., Weber, U. & Mlodzik, M. The role of RhoA in tissue polarity and Frizzled signalling . Nature 387, 292–295 (1997).
    CAS PubMed Google Scholar
61. Rulifson, E. J., Wu, C. H. & Nusse, R. Pathway specificity by the bifunctional receptor frizzled is determined by affinity for wingless. Mol. Cell 6 , 117–126 (2000).
    CAS PubMed Google Scholar
62. Lu, B., Usui, T., Uemura, T., Jan, L. & Jan, Y. N. Flamingo controls the planar polarity of sensory bristles and asymmetric division of sensory organ precursors in Drosophila. Curr. Biol. 9, 1247–1250 (1999).
    CAS PubMed Google Scholar
63. Bellaiche, Y., Gho, M., Kaltschmidt, J. A., Brand, A. H. & Schweisguth, F. Frizzled regulates the localisation of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nature Cell Biol. 3, 50– 57 (2001).
    CAS PubMed Google Scholar
64. Gotta, M. & Ahringer, J. Distinct roles for Gα and Gβγ in regulating spindle position and orientation in early C. elegans embryos. Nature Cell Biol. (in the press).
65. Zwaal, R. R. et al. G proteins are required for spatial orientation of early cell cleavages in C. elegans embryos. Cell 86, 619–629 (1996).
    CAS PubMed Google Scholar
66. Sheldahl, L. C., Park, M., Malbon, C. C. & Moon, R. T. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner. Curr. Biol. 9, 695– 698 (1999).
    CAS PubMed Google Scholar
67. Schaefer, M., Shevchenko, A. & Knoblich, J. A. A protein complex containing inscuteable and the Gα-binding protein Pins orients asymmetric cell divisions in Drosophila . Curr. Biol. 10, 353– 362 (2000).
    CAS PubMed Google Scholar
68. Yu, F., Morin, X., Cai, Y., Yang, X. & Chia, W. Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell 100, 399–409 ( 2000).
    CAS PubMed Google Scholar
69. Parmentier, M. L. et al. Rapsynoid/Partner of Inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J. Neurosci. (Online) 20, RC84 (2000).
70. Siderovski, D. P., Diverse-Pierluissi, M. & De Vries, L. The GoLoco motif: a Gαi/o binding motif and potential guanine-nucleotide exchange factor. Trends Biochem. Sci. 24, 340–341 (1999).
    CAS PubMed Google Scholar
71. Takesono, A. et al. Receptor-independent activators of heterotrimeric G-protein signaling pathways. J. Biol. Chem. 274, 33202–33205 (1999).
    CAS PubMed Google Scholar
72. Parent, C. A., Blacklock, B. J., Froehlich, W. M., Murphy, D. B. & Devreotes, P. N. G protein signaling events are activated at the leading edge of chemotactic cells. Cell 95, 81–91 (1998).
    CAS PubMed Google Scholar
73. Chant, J. Cell polarity in yeast. Annu. Rev. Cell. Dev. Biol. 15, 365–391 (1999).
    CAS PubMed Google Scholar
74. Nern, A. & Arkowitz, R. A. A Cdc24p–Far1p–Gβγ protein complex required for yeast orientation during mating. J. Cell Biol. 144, 1187–1202 (1999).
    CAS PubMed PubMed Central Google Scholar
75. Mello, C. C. et al. The PIE-1 protein and germline specification in C. elegans embryos. Nature 382, 710– 712 (1996).
    CAS PubMed Google Scholar
76. Seydoux, G. et al. Repression of gene expression in the embryonic germ lineage of C. elegans. Nature 382, 713– 716 (1996).
    CAS PubMed Google Scholar
77. Reese, K. J., Dunn, M. A., Waddle, J. A. & Seydoux, G. Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Mol. Cell 6, 445–455 ( 2000).
    CAS PubMed Google Scholar
78. Lu, B., Ackerman, L., Jan, L. Y. & Jan, Y. N. Modes of protein movement that lead to the asymmetric localization of partner of Numb during Drosophila neuroblast division. Mol. Cell 4, 883–891 (1999).
    CAS PubMed Google Scholar
79. Peng, C.-Y., Manning, L., Albertson, R. & Doe, C. Q. The tumour suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 408, 596–600 (2000).
    CAS PubMed Google Scholar
80. Ohshiro, T., Yagami, T., Zhang, C. & Matsuzaki, F. Role of cortical tumour suppressor proteins in asymmetric division of Drosophila neuroblast . Nature 408, 593–596 (2000). References 79 and 80 describe the first genes that are required for basal, but not apical, protein localization in Drosophila neuroblasts, suggesting that they are components of the transport machinery.
    CAS PubMed Google Scholar
81. Woods, D. F., Hough, C., Peel, D., Callaini, G. & Bryant, P. J. Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J. Cell Biol. 134, 1469–1482 (1996).
    CAS PubMed Google Scholar
82. Bilder, D., Li, M. & Perrimon, N. Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289, 113–116 (2000).
    CAS PubMed Google Scholar
83. Strand, D., Raska, I. & Mechler, B. M. The Drosophila lethal(2)giant larvae tumor suppressor protein is a component of the cytoskeleton. J. Cell Biol. 127, 1345–1360 ( 1994).
    CAS PubMed Google Scholar
84. Woods, D. F. & Bryant, P. J. The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451– 464 (1991).
    CAS PubMed Google Scholar
85. Strand, D. et al. The Drosophila lethal(2)giant larvae tumor suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J. Cell Biol. 127, 1361– 1373 (1994).
    CAS PubMed Google Scholar
86. De Lorenzo, C., Mechler, B. M. & Bryant, P. J. What is Drosophila telling us about cancer? Cancer Metastasis Rev. 18, 295– 311 (1999).
    CAS PubMed Google Scholar
87. Kagami, M., Toh-e, A. & Matsui, Y. Sro7p, a Saccharomyces cerevisiae counterpart of the tumor suppressor l(2)gl protein, is related to myosins in function. Genetics 149, 1717–1727 (1998).
    CAS PubMed PubMed Central Google Scholar
88. Qian, X., Goderie, S. K., Shen, Q., Stern, J. H. & Temple, S. Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125, 3143–3152 (1998).
    CAS PubMed Google Scholar
89. Chenn, A. & McConnell, S. K. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis . Cell 82, 631–641 (1995).
    CAS PubMed Google Scholar
90. Zhong, W., Feder, J. N., Jiang, M. M., Jan, L. Y. & Jan, Y. N. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17, 43–53 (1996).
    CAS PubMed Google Scholar
91. Wakamatsu, Y., Maynard, T. M., Jones, S. U. & Weston, J. A. NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 23, 71–81 ( 1999).
    CAS PubMed Google Scholar
92. Zhong, W. et al. Mouse numb is an essential gene involved in cortical neurogenesis . Proc. Natl Acad. Sci. USA 97, 6844– 6849 (2000).
    CAS PubMed PubMed Central Google Scholar
93. Johansson, C. B. et al. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96, 25– 34 (1999).
    CAS PubMed Google Scholar
94. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703–716 (1999).
    CAS PubMed Google Scholar
95. Hyman, A. A. Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position. J. Cell Biol. 109, 1185–1193 ( 1989). Laser ablation of microtubules reveals a mechanism for orientation of mitotic spindles: astral microtubules attach to a cortical site and pull the spindle towards the site.
    CAS PubMed Google Scholar
96. Shulman, J. M., Benton, R. & St Johnston, D. The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101, 377– 388 (2000).
    CAS PubMed Google Scholar
97. Bohm, H., Brinkmann, V., Drab, M., Henske, A. & Kurzchalia, T. V. Mammalian homologues of C. elegans PAR-1 are asymmetrically localized in epithelial cells and may influence their polarity . Curr. Biol. 7, 603–606 (1997).
    CAS PubMed Google Scholar
98. Levitan, D. J., Boyd, L., Mello, C. C., Kemphues, K. J. & Stinchcomb, D. T. par-2, a gene required for blastomere asymmetry in Caenorhabditis elegans, encodes zinc-finger and ATP-binding motifs . Proc. Natl Acad. Sci. USA 91, 6108– 6112 (1994).
    CAS PubMed PubMed Central Google Scholar
99. Burglin, T. R. A Caenorhabditis elegans prospero homologue defines a novel domain . Trends Biochem. Sci. 19, 70– 71 (1994).
    CAS PubMed Google Scholar
100. Oliver, G. et al. Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech. Dev. 44, 3– 16 (1993).
     CAS PubMed Google Scholar

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