LGN/mInsc and LGN/NuMA Complex Structures Suggest Distinct Functions in Asymmetric Cell Division for the Par3/mInsc/LGN and Gαi/LGN/NuMA Pathways

Molecular Cell

Volumn 43, Issue 3, 2011, Pages 418-431

  Zhu, Jinwei ^a,b   Wen, Wenyu ^a   Zheng, Zhen ^c   Shang, Yuan ^b   Wei, Zhiyi ^b   Xiao, Zhuoni ^c   Pan, Zhu ^a   Du, Quansheng ^c   Wang, Wenning ^a   Zhang, Mingjie ^a,b  

^a FUDAN UNIVERSITY   (China)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; GLYCINE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; LEUCINE; NUCLEAR PROTEIN; PROTEIN MLNSC; PROTEIN NUMA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOCHEMISTRY; CELL DIVISION; CELL POLARITY; CONTROLLED STUDY; CYTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; INVERTEBRATE; MITOSIS SPINDLE; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STRUCTURE;

INVERTEBRATA;

EID: 79960913555     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.07.011     Document Type: Article

References (47)

1. Bowman S.K., Neumüller R.A., Novatchkova M., Du Q., Knoblich J.A. The Drosophila NuMA Homolog Mud regulates spindle orientation in asymmetric cell division. Dev. Cell 2006, 10:731-742.
2. Bryant D.M., Datta A., Rodríguez-Fraticelli A.E., Peränen J., Martín-Belmonte F., Mostov K.E. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 2010, 12:1035-1045.
3. Cowan C.R., Hyman A.A. Asymmetric cell division in C. elegans: cortical polarity and spindle positioning. Annu. Rev. Cell Dev. Biol. 2004, 20:427-453.
4. Das A.K., Cohen P.W., Barford D. The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 1998, 17:1192-1199.
5. Du Q., Macara I.G. Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell 2004, 119:503-516.
6. Du Q., Stukenberg P.T., Macara I.G. A mammalian Partner of inscuteable binds NuMA and regulates mitotic spindle organization. Nat. Cell Biol. 2001, 3:1069-1075.
7. Du Q., Taylor L., Compton D.A., Macara I.G. LGN blocks the ability of NuMA to bind and stabilize microtubules. A mechanism for mitotic spindle assembly regulation. Curr. Biol. 2002, 12:1928-1933.
8. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
9. Gönczy P. Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell Biol. 2008, 9:355-366.
10. Hao Y., Du Q.S., Chen X.Y., Zheng Z., Balsbaugh J.L., Maitra S., Shabanowitz J., Hunt D.F., Macara I.G. Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical Pins. Curr. Biol. 2010, 20:1809-1818.
11. Horvitz H.R., Herskowitz I. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 1992, 68:237-255.
12. Izumi Y., Ohta N., Itoh-Furuya A., Fuse N., Matsuzaki F. Differential functions of G protein and Baz-aPKC signaling pathways in Drosophila neuroblast asymmetric division. J. Cell Biol. 2004, 164:729-738.
13. Izumi Y., Ohta N., Hisata K., Raabe T., Matsuzaki F. Drosophila Pins-binding protein Mud regulates spindle-polarity coupling and centrosome organization. Nat. Cell Biol. 2006, 8:586-593.
14. Jínek M., Rehwinkel J., Lazarus B.D., Izaurralde E., Hanover J.A., Conti E. The superhelical TPR-repeat domain of O-linked GlcNAc transferase exhibits structural similarities to importin alpha. Nat. Struct. Mol. Biol. 2004, 11:1001-1007.
15. Johnston C.A., Hirono K., Prehoda K.E., Doe C.Q. Identification of an Aurora-A/PinsLINKER/Dlg spindle orientation pathway using induced cell polarity in S2 cells. Cell 2009, 138:1150-1163.
16. Knoblich J.A. Mechanisms of asymmetric stem cell division. Cell 2008, 132:583-597.
17. Konno D., Shioi G., Shitamukai A., Mori A., Kiyonari H., Miyata T., Matsuzaki F. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 2008, 10:93-101.
18. Kraut R., Campos-Ortega J.A. inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adaptor protein. Dev. Biol. 1996, 174:65-81.
19. Kraut R., Chia W., Jan L.Y., Jan Y.N., Knoblich J.A. Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 1996, 383:50-55.
20. Kuchinke U., Grawe F., Knust E. Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Curr. Biol. 1998, 8:1357-1365.
21. Lin H. The stem-cell niche theory: lessons from flies. Nat. Rev. Genet. 2002, 3:931-940.
22. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 441:1068-1074.
23. Morrison S.J., Spradling A.C. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008, 132:598-611.
24. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 1997, 53:240-255.
25. Neumüller R.A., Knoblich J.A. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 2009, 23:2675-2699.
26. Nipper R.W., Siller K.H., Smith N.R., Doe C.Q., Prehoda K.E. Galphai generates multiple Pins activation states to link cortical polarity and spindle orientation in Drosophila neuroblasts. Proc. Natl. Acad. Sci. USA 2007, 104:14306-14311.
27. Parmentier M.L., Woods D., Greig S., Phan P.G., Radovic A., Bryant P., O'Kane C.J. Rapsynoid/partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J. Neurosci. 2000, 20:RC84.
28. Petronczki M., Knoblich J.A. DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nat. Cell Biol. 2001, 3:43-49.
29. Poulson N.D., Lechler T. Robust control of mitotic spindle orientation in the developing epidermis. J. Cell Biol. 2010, 191:915-922.
30. Roh M.H., Fan S., Liu C.J., Margolis B. The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells. J. Cell Sci. 2003, 116:2895-2906.
31. Schaefer M., Shevchenko A., Shevchenko A., Knoblich J.A. A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr. Biol. 2000, 10:353-362.
32. Schaefer M., Petronczki M., Dorner D., Forte M., Knoblich J.A. Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 2001, 107:183-194.
33. Scheufler C., Brinker A., Bourenkov G., Pegoraro S., Moroder L., Bartunik H., Hartl F.U., Moarefi I. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 2000, 101:199-210.
34. Schober M., Schaefer M., Knoblich J.A. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 1999, 402:548-551.
35. Sheldrick G.M. A short history of SHELX. Acta Crystallogr. A 2008, 64:112-122.
36. Siegrist S.E., Doe C.Q. Microtubule-induced Pins/Galphai cortical polarity in Drosophila neuroblasts. Cell 2005, 123:1323-1335.
37. Siegrist S.E., Doe C.Q. Extrinsic cues orient the cell division axis in Drosophila embryonic neuroblasts. Development 2006, 133:529-536.
38. Siller K.H., Doe C.Q. Spindle orientation during asymmetric cell division. Nat. Cell Biol. 2009, 11:365-374.
39. Siller K.H., Cabernard C., Doe C.Q. The NuMA-related Mud protein binds Pins and regulates spindle orientation in Drosophila neuroblasts. Nat. Cell Biol. 2006, 8:594-600.
40. Wang J., Dye B.T., Rajashankar K.R., Kurinov I., Schulman B.A. Insights into anaphase promoting complex TPR subdomain assembly from a CDC26-APC6 structure. Nat. Struct. Mol. Biol. 2009, 16:987-989.
41. Williams S.E., Beronja S., Pasolli H.A., Fuchs E. Asymmetric cell divisions promote Notch-dependent epidermal differentiation. Nature 2011, 470:353-358.
42. Wodarz A., Ramrath A., Kuchinke U., Knust E. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 1999, 402:544-547.
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. 2000, 150:1361-1374.
44. 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 2000, 100:399-409.
45. Zhang Z., Kulkarni K., Hanrahan S.J., Thompson A.J., Barford D. The APC/C subunit Cdc16/Cut9 is a contiguous tetratricopeptide repeat superhelix with a homo-dimer interface similar to Cdc27. EMBO J. 2010, 29:3733-3744.
46. Zheng Z., Zhu H., Wan Q., Liu J., Xiao Z., Siderovski D.P., Du Q. LGN regulates mitotic spindle orientation during epithelial morphogenesis. J. Cell Biol. 2010, 189:275-288.
47. Zigman M., Cayouette M., Charalambous C., Schleiffer A., Hoeller O., Dunican D., McCudden C.R., Firnberg N., Barres B.A., Siderovski D.P., Knoblich J.A. Mammalian inscuteable regulates spindle orientation and cell fate in the developing retina. Neuron 2005, 48:539-545.