Asymmetric cell division: Lessons from flies and worms

Current Opinion in Genetics and Development

Volumn 8, Issue 4, 1998, Pages 392-399

  Lu, Bingwei ^a   Jan, Lily Y ^a   Jan, Yuh Nung ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN;

CAENORHABDITIS ELEGANS; CELL DIVISION; CYTOSKELETON; DEVELOPMENTAL BIOLOGY; DROSOPHILA; MITOSIS SPINDLE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS;

EID: 0031663771     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(98)80108-1     Document Type: Article

References (59)

1. Horvitz HR, Herskowitz I: Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 1992, 68:237-255.
2. Guo S, Kemphues KJ: Molecular genetics of asymmetric cleavage in the early Caenorhabditis elegans embryo. Curr Opin Genet Dev 1996, 6:408-415.
3. Doe CQ: Asymmetric cell division and neurogenesis. Curr Opin Genet Dev 1996, 6:562-566.
4. Knoblich JA: Mechanisms of asymmetric cell division during animal development. Curr Opin Cell Biol 1997, 9:833-841.
5. Kemphues KJ, Strome S: Fertilization and establishment of polarity in the embryo. In C. elegans II. Edited by Riddle DL, Blumenthal T, Meyer BJ, Priess JR. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1997:335-359.
6. Schagat T, Lin H: Neuroblasts: a model for the asymmetric division of stem cells. Trends Genet 1997, 13:33-39.
7. Jan YN, Jan LY: Asymmetric cell division. Nature 1998, 392:775-778.
8. Uemura T, Shepherd S, Ackerman L, Jan LY, Jan YN: numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 1989, 58:349-360.
9. Rhyu MS, Jan LY, Jan YN: Asymmetric distribution of Numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 1994, 76:477-491.
10. Knoblich JA, Jan LY, Jan YN: Asymmetric segregation of Numb and Prospero during cell division. Nature 1995, 377:624-627.
11. Spana EP, Kopczynski C, Goodman CS, Doe CQ: Asymmetric localization of Numb autonomously determines sibling neuron identity in Drosophila CNS. Development 1995, 121:3489-3494.
12. •].
13. •] together demonstrate that in addition to their functions in controlling asymmetric neural precursor divisions in the Drosophila CNS and PNS, Inscuteable and Numb are also required for the asymmetric muscle precursor divisions during myogenesis. Similar to the situation in the nervous system, Numb is preferentially segregated to one of the two daughter cells to distinguish sibling cell fates and Inscuteable is required for the asymmetric localization of Numb. Thus, Inscuteable and Numb function in asymmetric divisions of several different types of precursors.
14. Quo M, Jan LY, Jan YN: Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 1996, 17:27-41.
15. Spana EP, Doe CQ: Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 1996, 17:21-26.
16. Frise E, Knoblich JA, Younger-Shepherd S, Jan LY, Jan YN: The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc Natl Acad Sci USA 1996, 93:11925-11932.
17. Wang S, Younger-Shepherd S, Jan LY, Jan YN: Only a subset of the binary cell fate decisions mediated by Numb/Notch signaling in Drosophila sensory organ lineage requires Suppressor of Hairless. Development 1998, 124:4435-4446. This paper shows that in the sensory organ lineage, Numb/Notch signaling is transduced differently in the IIa and IIb lineages. Suppressor of Hairless is required in the cell fate decision of the IIa (hair/socket) but not the IIb (neuron/sheath) lineage. Moreover, an immunofluorescence study shows that Numb is localized asymmetrically in all three divisions of the SOP lineage.
18. •].
19. •] show that Sanpodo acts downstream of Numb in the Numb/Notch signaling pathway to control sibling cell fates. The homology between Sanpodo and Tropomodulin, an actin/tropomyosin associated protein, suggests that the Numb/Notch signaling pathway may control cell fates through regulating the cytoskeleton. The function of Numb in specifying GMC daughter cell fates was demonstrated for the first time.
20. Vaessin H, Grell E, Wolff E, Bier E, Jan LY, Jan YN: prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 1991, 67:942-953.
21. Doe CQ, Chu-LaGraff Q, Wright DM, Scott MP: The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 1991, 65:451-465.
22. Matsuzaki F, Koizumi K, Hama C, Yoshioka T, Nabeshima Y: Cloning of the Drosophila prospero gene and its expression in ganglion mother cells. Biochem Biophys Res Comm 1992, 182:1326-1332.
23. Spana EP, Doe CQ: The Prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 1995, 121:3187-3195.
24. Hirata J, Nakagoshi H, Nabeshima Y, Matsuzaki F: Asymmetric segregation of a hemeoprotein, Prospero, during cell divisions in neural and endodermal development. Nature 1995, 377:627-630.
25. ••].
26. ••] describe the asymmetric localization of prospero RNA in Drosophila neuroblasts. The observation of prospero RNA localization prompted the authors to investigate the role of Stauten in the process. Stauten is expressed in neuroblasts and is asymmetrically localized during mitosis, colocalizing with Prospero protein and RNA. In staufen mutants, prospero RNA is not localized but the protein is still localized. Moreover, Stauten physically interacts with Inscuteable and binds prospero RNA 3′-UTR and serves to link prospero RNA to Inscuteable.
27. Kraut R, Campos-Ortega JA: inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adapter protein. Dev Biol 1996, 174:65-81.
28. Kraut R, Chia W, Jan LY, Jan YN, Knoblich JA: Role of inscuteable in orienting asymmetric cell division in Drosophila. Nature 1996, 383:50-55.
29. ••].
30. ••] identified Miranda as a Prospero-interacting protein in yeast two-hybrid screens using the Prospero localization domain as a bait. Miranda is expressed in cell types where asymmetric Prospero localization takes place. Moreover, Miranda protein itself is asymmetrically localized, coinciding with Prospero localization. In miranda mutant embryos Prospero is delocalized. These studies therefore identify an important component of the cellular machinery that localizes Prospero and provide a new starting point to identify more upstream components of the localization pathway.
31. Shen C-P, Knoblich, JA, Chan Y-M, Jiang M-M, Jan LY, Jan YN: Miranda as a multidomain adapter linking apically localized Inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila. Genes Dev 1998, 12:1847-1857. This paper shows that Miranda is an adapter molecule not merely dedicated to Prospero localization - it also interacts with Staufen and is required for Staufen localization. Structure-function analysis of Miranda identified an amino-terminal domain in Miranda responsible for its asymmetric localization and interaction with Inscuteable. Miranda may therefore provide a physical link between apically located Inscuteable and basally localized Prospero and Staufen.
32. Vinson CR, Conover S, Adler PN: A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 1989, 338:263-264.
33. Adler PN: The genetic control of tissue polarity in Drosophila. Bioessays 1992, 14:735-741.
34. Gho M, Schweisguth F: Frizzled signaling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature 1998, in press. This paper provides the first evidence that the asymmetric SOP divisions in the bristle lineage in Drosophila follows planar A-P polarity and that the Frizzled signaling pathway is involved in orienting the first division axis and the positioning of Numb crescents. It is also shown that the axes of the second divisions are controlled by mechanisms independent of Frizzled signaling.
35. Hill DP, Strome S: Brief cytochalasin-induced disruption of microfilaments during a critical interval in 1-cell C. elegans embryos alters the partitioning of developmental instructions to the 2-cell embryo. Development 1990, 108:159-172.
36. •].
37. •] show that treatment with Latrunculin, a potent inhibitor of microfilament polymerization, results in the absence of asymmetric protein localization in both Drosophila embryos and in vitro cultured cells. These studies demonstrate that, as in other systems, the actin cytoskeleton is important in establishing cellular polarity.
38. Mello CC, Schubert C, Draper B, Zhang W, Lobel R, Priess JR: The PIE-1 protein and germline specification in C. elegans embryos. Nature 1996, 382:710-712.
39. Guedes S, Priess JR: The C. elegans MEX-1 protein is present in germline blastomeres and is a P-granule component. Development 1997, 124:731-739.
40. Hunter CP, Kenyon C: Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 1996, 87:217-226.
41. Draper BW, Mello CC, Bowerman B, Hardin J, Priess JR: MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 1996, 87:205-216.
42. Lin R, Hill RJ, Priess JR: POP-1 and anterior-posterior fate decisions in C. elegans embryos. Cell 1998, 92:229-239. The authors demonstrate that POP-1 is present at unequal levels between the two daughters of multiple anterior-posterior divisions in early C. elegans embryos and that this POP-1 asymmetry is required to specify daughter cell fates. Loss of POP-1 causes both daughters to acquire posterior cell fates whereas equal segregation of POP-1 caused by mutations in the Wnt signaling pathway leads to posterior→anterior cell-fate transformations. POP-1 therefore functions in a general mechanism to distinguish binary cell fates.
43. Kaletta T, Schnabel H, Schnabel R: Binary specification of the embryonic lineage in Caenorhabditis elegans. Nature 1997, 390:294-298.
44. Seydoux G, Mello CC, Pettitt J, Wood WB, Priess JR, Fire A: Repression of gene expression in the embryonic germ lineage of C. elegans. Nature 1996, 382:713-716.
45. Kemphues KJ, Priess JR, Morton DG, Cheng N: Identification of genes for cytoplasmic localization in early C. elegans embryo. Cell 1988, 52:311-320.
46. Guo S, Kemphues KJ: par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 1995, 81:611-620.
47. Boyd L, Guo S, Levitan D, Stinchcomb D, Kemphues KJ: PAR-2 is asymmetrically distributed and promotes association of P- granules and PAR-1 with the cortex in C. elegans embryos. Development 1996, 122:3075-3084.
48. Etemad-Moghadam B, Guo S, Kemphues KJ: Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 1995, 83:743-752.
49. Crittenden SL, Rudel D, Binder J, Evans TC, Kimble J: Genes required for GLP-1 asymmetry in the early Caenorhabditis elegans embryo. Dev Biol 1997, 181:36-46.
50. Bowerman B, Ingram MK, Hunter CP: The maternal par genes and the segregation of cell fate specification activities in early Caenorhabiditis elegans embryos. Development 1997, 124:3815-3826.
51. Drewes G, Ebneth A, Preuss A, Mandelkow EM, Mandelkow E: MARK, a novel family of protein kinases that phosphorylate microtuble-associated proteins and trigger microtuble disruption. Cell 1997, 89:297-308.
52. Goldstein B: Cell contacts orient some division axes in the Canorhabditis elegans embryo. J Cell Biol 1995, 129:1071-1080.
53. Goldstein B: An analysis of the response to gut induction in the C. elegans embryo. Development 1995, 121:1227-1236.
54. ••].
55. ••] isolated the mom mutants. The mom genes encode components of the Wnt signaling pathway, suggesting that during P2-EMS interaction, a signal from P2 activates the Wnt signaling pathway which then regulates POP-1 levels between the two daughters of EMS and the spindle orientation of EMS division. By taking advantage of the C. elegans genome project and a powerful RNA-mediated interference assay, the authors showed that other components of the Wnt pathway - such as an APC-related gene and an armadillo/β-catenin homolog - are also required for E and MS cell-fate decision.
56. Zhong W, Feder JN, Jiang MM, Jan LY, Jan YN: Asymmetric localization of a mammalian Numb homolog during mouse cortical neurogenesis. Neuron 1996, 17:43-53.
57. Verdi JM, Schmandt R, Bashirullah A, Jacob S, Salvino R, Craig CG, Program AE, Lipshitz HD, McGlade CJ: Mammalian NUMB is an evolutionary conserved signaling adapter protein that specifies cell fate. Curr Biol 1996, 6:1134-1145.
58. Zhong W, Jiang MM, Weinmaster G, Jan LY, Jan YN: Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 1997, 124:1887-1897.
59. Bohm H, Brinkmann V, Drab M, Henske A, Kurzchalia TV: Mammalian homologues of C. elegans PAR-1 are asymmetrically localized in epithelial cells and may influence their polarity. Curr Biol 1997, 7:603-606.