A novel function for the Rab5 effector Rabenosyn-5 in planar cell polarity

被引:34
|
作者
Mottola, Giovanna [1 ,2 ]
Classen, Anne-Kathrin [1 ]
Gonzalez-Gaitan, Marcos [1 ,3 ,4 ]
Eaton, Suzanne [1 ]
Zerial, Marino [1 ]
机构
[1] Max Planck Inst Mol Cell Biol & Genet, D-01307 Dresden, Germany
[2] Univ Naples Federico 2, Dipartimento Biochim & Biotecnol Med, I-80131 Naples, Italy
[3] Univ Geneva, Dept Biochem, CH-1211 Geneva, Switzerland
[4] Univ Geneva, Dept Mol Biol, CH-1211 Geneva, Switzerland
来源
DEVELOPMENT | 2010年 / 137卷 / 14期
关键词
Drosophila; Endocytosis; Planar cell polarity; Wing; 7-PASS TRANSMEMBRANE CADHERIN; ENDOCYTIC PATHWAY; ASYMMETRIC LOCALIZATION; DROSOPHILA-MELANOGASTER; CAENORHABDITIS-ELEGANS; GRADIENT FORMATION; TISSUE POLARITY; EARLY ENDOSOMES; PROTEIN; MEMBRANE;
D O I
10.1242/dev.048413
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
In addition to apicobasal polarization, some epithelia also display polarity within the plane of the epithelium. To what extent polarized endocytosis plays a role in the establishment and maintenance of planar cell polarity (PCP) is at present unclear. Here, we investigated the role of Rabenosyn-5 (Rbsn-5), an evolutionarily conserved effector of the small GTPase Rab5, in the development of Drosophila wing epithelium. We found that Rbsn-5 regulates endocytosis at the apical side of the wing epithelium and, surprisingly, further uncovered a novel function of this protein in PCP. At early stages of pupal wing development, the PCP protein Fmi redistributes between the cortex and Rab5- and Rbsn-5-positive early endosomes. During planar polarization, Rbsn-5 is recruited at the apical cell boundaries and redistributes along the proximodistal axis in an Fmi-dependent manner. At pre-hair formation, Rbsn-5 accumulates at the bottom of emerging hairs. Loss of Rbsn-5 causes intracellular accumulation of Fmi and typical PCP alterations such as defects in cell packing, in the polarized distribution of PCP proteins, and in hair orientation and formation. Our results suggest that establishment of planar polarity requires the activity of Rbsn-5 in regulating both the endocytic trafficking of Fmi at the apical cell boundaries and hair morphology.
引用
收藏
页码:2353 / 2364
页数:12
相关论文
共 50 条
  • [31] The Rab5 effector Rabaptin-5 and its isoform Rabaptin-5δ differ in their ability to interact with the small GTPase Rab4
    Korobko, E
    Kiselev, S
    Olsnes, S
    Stenmark, H
    Korobko, I
    FEBS JOURNAL, 2005, 272 (01) : 37 - 46
  • [32] INTERACTIONS OF RAB5 WITH CYTOSOLIC PROTEINS
    KURZCHALIA, TV
    GORVEL, JP
    DUPREE, P
    PARTON, R
    KELLNER, R
    HOUTHAEVE, T
    GRUENBERG, J
    SIMONS, K
    JOURNAL OF BIOLOGICAL CHEMISTRY, 1992, 267 (26) : 18419 - 18423
  • [33] Kinetic timing: A novel mechanism that improves the timer function of Rab5 GTPase in endosome fusion
    Li, GP
    Qian, H
    MOLECULAR BIOLOGY OF THE CELL, 2001, 12 : 216A - 216A
  • [34] Dimerization of small GTPase Rab5
    Daitoku, H
    Isida, J
    Fujiwara, K
    Nakajima, T
    Fukamizu, A
    INTERNATIONAL JOURNAL OF MOLECULAR MEDICINE, 2001, 8 (04) : 397 - 404
  • [35] The Rab5 effector EEA1 interacts directly with syntaxin-6
    Simonsen, A
    Gaullier, JM
    D'Arrigo, A
    Stenmark, H
    JOURNAL OF BIOLOGICAL CHEMISTRY, 1999, 274 (41) : 28857 - 28860
  • [36] Rab5 and its effector FHF contribute to neuronal polarity through dynein-dependent retrieval of somatodendritic proteins from the axon
    Guo, Xiaoli
    Farias, Ginny G.
    Mattera, Rafael
    Bonifacino, Juan S.
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2016, 113 (36) : E5318 - E5327
  • [37] Coordination of the Rab5 Cycle on Macropinosomes
    Feliciano, William D.
    Yoshida, Sei
    Straight, Samuel W.
    Swanson, Joel A.
    TRAFFIC, 2011, 12 (12) : 1911 - 1922
  • [38] Conserved role for RAB5 in mitosis
    Rachel David
    Nature Reviews Molecular Cell Biology, 2012, 13 (1) : 5 - 5
  • [39] Rabenosyn-5 and EHD1 interact and sequentially regulate protein recycling to the plasma membrane
    Naslavsky, N
    Boehm, M
    Backlund, PS
    Caplan, S
    MOLECULAR BIOLOGY OF THE CELL, 2004, 15 (05) : 2410 - 2422
  • [40] rabip4′ is an effector of rab5 and rab4 and regulates transport through early endosomes
    Fouraux, MA
    Deneka, M
    Ivan, V
    van der Heijden, A
    Raymackers, J
    van Suylekom, D
    van Venrooij, WJ
    van der Sluijs, P
    Pruijn, GJM
    MOLECULAR BIOLOGY OF THE CELL, 2004, 15 (02) : 611 - 624