The kinesin KIF17b and RNA-binding protein TB-RBP transport specific cAMP-responsive element modulator-regulated mRNAs in male germ cells

被引:64
作者
Chennathukuzhi, V
Morales, CR
El-Alfy, M
Hecht, NB
机构
[1] Univ Penn, Sch Med, Ctr Res Reprod & Womens Hlth, Philadelphia, PA 19104 USA
[2] McGill Univ, Dept Anat & Cell Biol, Montreal, PQ H3A 2T5, Canada
[3] CHU Laval, Montreal, PQ G1V 4G2, Canada
关键词
D O I
10.1073/pnas.2536695100
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Testis brain RNA-binding protein (TB-RBP), the mouse orthologue of the human protein Translin, is a widely expressed and highly conserved protein with proposed functions in chromosomal translocations, mitotic cell division, and mRNA transport, stabilization, and storage. Targeted inactivation of TB-RBP leads to abnormalities in fertility and behavior. A testis-enriched kinesin KIF17b coimmunoprecipitates with TB-RBP in a RNA-protein complex containing specific cAMP-responsive element modulator (CREM)regulated mRNAs. The specificity of this interaction is confirmed by in vivo RNA-protein crosslinking and transfections of hippocampal neurons. Combining in situ hybridization and immunohistochemistry at the electron microscope level, a temporally sequential dissociation of KIF17b and TB-RBP from specific mRNAs is detected with TB-RBP release coincident with the time of mRNA translation, indicating a separation of the processes of transport and translation. We conclude that KIF17b serves as a molecular motor component of a TB-RBP-mouse ribonucleoprotein complex transporting a group of specific CREM-regulated mRNAs in mammalian male postmeiotic germ cells. Because KIF17b has been reported to control CREM-dependent transcription in male germ cells by regulating the intracellular location of the transcriptional coactivator activator of CREM in testis, this indicates that one kinesin links the processes of transcription and transport of specific mRNAs in mammalian male germ cells.
引用
收藏
页码:15566 / 15571
页数:6
相关论文
共 32 条
[1]   A NOVEL GENE, TRANSLIN, ENCODES A RECOMBINATION HOTSPOT BINDING-PROTEIN ASSOCIATED WITH CHROMOSOMAL TRANSLOCATIONS [J].
AOKI, K ;
SUZUKI, K ;
SUGANO, T ;
TASAKA, T ;
NAKAHARA, K ;
KUGE, O ;
OMORI, A ;
KASAI, M .
NATURE GENETICS, 1995, 10 (02) :167-174
[2]   Severe impairment of spermatogenesis in mice lacking the CREM gene [J].
Blendy, JA ;
Kaestner, KH ;
Weinbauer, GF ;
Nieschlag, E ;
Schutz, G .
NATURE, 1996, 380 (6570) :162-165
[3]   A ROLE FOR TRANSCRIPTION AND FRGY2 IN MASKING MATERNAL MESSENGER-RNA WITHIN XENOPUS-OOCYTES [J].
BOUVET, P ;
WOLFFE, AP .
CELL, 1994, 77 (06) :931-941
[4]   GENETICALLY HAPLOID SPERMATIDS ARE PHENOTYPICALLY DIPLOID [J].
BRAUN, RE ;
BEHRINGER, RR ;
PESCHON, JJ ;
BRINSTER, RL ;
PALMITER, RD .
NATURE, 1989, 337 (6205) :373-376
[5]   OPTIMIZED SURVIVAL OF HIPPOCAMPAL-NEURONS IN B27-SUPPLEMENTED NEUROBASAL(TM), A NEW SERUM-FREE MEDIUM COMBINATION [J].
BREWER, GJ ;
TORRICELLI, JR ;
EVEGE, EK ;
PRICE, PJ .
JOURNAL OF NEUROSCIENCE RESEARCH, 1993, 35 (05) :567-576
[6]   PROTAMINE TRANSCRIPT SHARING AMONG POSTMEIOTIC SPERMATIDS [J].
CALDWELL, KA ;
HANDEL, MA .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1991, 88 (06) :2407-2411
[7]   Mice deficient for testis-brain RNA-binding protein exhibit a coordinate loss of TRAX, reduced fertility, altered gene expression in the brain, and behavioral changes [J].
Chennathukuzhi, V ;
Stein, JM ;
Abel, T ;
Donlon, S ;
Yang, SC ;
Miller, JP ;
Allman, DM ;
Simmons, RA ;
Hecht, NB .
MOLECULAR AND CELLULAR BIOLOGY, 2003, 23 (18) :6419-6434
[8]   Trax (Translin-associated factor X), a primarily cytoplasmic protein, inhibits the binding of TB-RBP (Translin) to RNA [J].
Chennathukuzhi, VM ;
Kurihara, Y ;
Bray, JD ;
Hecht, NB .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2001, 276 (16) :13256-13263
[9]   miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis [J].
Deng, W ;
Lin, HF .
DEVELOPMENTAL CELL, 2002, 2 (06) :819-830
[10]   CELL-SPECIFIC PROTEINS INTERACT WITH THE 3' UNTRANSLATED REGIONS OF PRM-1 AND PRM-2 MESSENGER-RNA [J].
FAJARDO, MA ;
BUTNER, KA ;
LEE, K ;
BRAUN, RE .
DEVELOPMENTAL BIOLOGY, 1994, 166 (02) :643-653