The RNA-Binding Protein Rrm4 is Essential for Efficient Secretion of Endochitinase Cts1

Koepke, Janine; Kaffarnik, Florian; Haag, Carl; Zarnack, Kathi; Luscombe, Nicholas M.; König, Julian; Ule, Jernej; Kellner, Ronny; Begerow, Dominik; Feldbrügge, Michael

doi:10.1074/mcp.m111.011213

Cited by 49 publications

(83 citation statements)

References 88 publications

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“…mRNA molecules are attached to endosomes and thus hitchhike these organelles (12). Most interestingly, the transport mechanism appears to be required for the proper localization of several mitochondrial proteins (13). This suggests transient association of kinesin-3 with mitochondria for delivery of mRNA encoding mitochondrial proteins.…”

Section: Discussionmentioning

confidence: 99%

“…Recent data obtained from U. maydis may explain the somewhat contradictory results. It was shown recently that Kin3 of U. maydis is involved in mRNA transport (11,13). mRNA molecules are attached to endosomes and thus hitchhike these organelles (12).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, deletion of the RNA-binding protein Rrm4 resulted in changes of the expression pattern of many genes. Among 5 identified mRNAs, three of them encode mitochondrial proteins, suggesting delivery of such mRNAs toward mitochondria (13). Koepke et al suggested that mitochondrial protein import depends on proper mRNA localization.…”

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confidence: 99%

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Neurospora crassa NKIN2, a Kinesin-3 Motor, Transports Early Endosomes and Is Required for Polarized Growth

et al. 2013

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bBiological motors are molecular nanomachines, which convert chemical energy into mechanical forces. The combination of mechanoenzymes with structural components, such as the cytoskeleton, enables eukaryotic cells to overcome entropy, generate molecular gradients, and establish polarity. Hyphae of filamentous fungi are among the most polarized cells, and polarity defects are most obvious. Here, we studied the role of the kinesin-3 motor, NKIN2, in Neurospora crassa. We found that NKIN2 localizes as fast-moving spots in the cytoplasm of mature hyphae. To test whether the spots represented early endosomes, the Rab5 GTPase YPT52 was used as an endosomal marker. NKIN2 colocalized with YPT52. Deletion of nkin2 caused strongly reduced endosomal movement. Combined, these results confirm the involvement of NKIN2 in early endosome transport. Introduction of a rigor mutation into NKIN2 labeled with green fluorescent protein (GFP) resulted in decoration of microtubules. Interestingly, NKIN2rigor was associated with a subpopulation of microtubules, as had been shown earlier for the Aspergillus nidulans orthologue UncA. Other kinesins did not show this specificity.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Neurospora crassa NKIN2, a Kinesin-3 Motor, Transports Early Endosomes and Is Required for Polarized Growth

et al. 2013

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“…Thus, the RNA-binding domain is functionally important, and Rrm4 does not hitchhike on transported mRNAs, but is an integral part of the transport unit (König et al, 2009). According to current views, microtubule-dependent transport of mRNPs is important for determination of the subcellular localisation of targets such as the small G protein Rho3 at retraction septa, as well as crucial for efficient secretion of the endochitinase Cts1 (König et al, 2009;Zarnack and Feldbrügge, 2010;Koepke et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes

Baumann

Pohlmann

Jungbluth

et al. 2012

Journal of Cell Science

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145

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SummaryLong-distance transport of mRNAs is important in determining polarity in eukaryotes. Molecular motors shuttle large ribonucleoprotein complexes (mRNPs) containing RNA-binding proteins and associated factors along microtubules. However, precise mechanisms including the interplay of molecular motors and a potential connection to membrane trafficking remain elusive. Here, we solve the motor composition of transported mRNPs containing the RNA-binding protein Rrm4 of the pathogen Ustilago maydis. The underlying transport process determines the axis of polarity in infectious filaments. Plus-end-directed Kin3, a kinesin-3 type motor, mediates anterograde transport of mRNPs and is also present in transport units moving retrogradely. Split dynein Dyn1-Dyn2 functions in retrograde movement of mRNPs. Plus-end-directed conventional kinesin Kin1 is indirectly involved by transporting minus-end-directed dynein back to plus ends. Importantly, we additionally demonstrate that Rrm4-containing mRNPs colocalise with the t-SNARE Yup1 on shuttling endosomes and that functional endosomes are essential for mRNP movement. Either loss of Kin3 or removal of its lipidbinding pleckstrin-homology domain abolishes Rrm4-dependent movement without preventing colocalisation of Rrm4 and Yup1-positive endosomes. In summary, we uncovered the combination of motors required for mRNP shuttling along microtubules. Furthermore, intimately linked co-transport of endosomes and mRNPs suggests vesicle hitchhiking as mode of mRNP transport.

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“…In such rapidly elongating filaments, long-distance transport, including endosomal RNA transport, becomes important (13,17). Previous studies on the RNA-binding protein Rrm4 identified the chitinase Cts1 as a potential target of active mRNA transport (18). Interestingly, Cts1 is unconventionally secreted (19).…”

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confidence: 99%

Chitinases Are Essential for Cell Separation in Ustilago maydis

et al. 2015

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Chitin is an essential component of the fungal cell wall, providing rigidity and stability. Its degradation is mediated by chitinases and supposedly ensures the dynamic plasticity of the cell wall during growth and morphogenesis. Hence, chitinases should be particularly important for fungi with dramatic morphological changes, such as Ustilago maydis. This smut fungus switches from yeast to filamentous growth for plant infection, proliferates as a mycelium in planta, and forms teliospores for spreading. Here, we investigate the contribution of its four chitinolytic enzymes to the different morphological changes during the complete life cycle in a comprehensive study of deletion strains combined with biochemical and cell biological approaches. Interestingly, two chitinases act redundantly in cell separation during yeast growth. They mediate the degradation of remnant chitin in the fragmentation zone between mother and daughter cell. In contrast, even the complete lack of chitinolytic activity does not affect formation of the infectious filament, infection, biotrophic growth, or teliospore germination. Thus, unexpectedly we can exclude a major role for chitinolytic enzymes in morphogenesis or pathogenicity of U. maydis. Nevertheless, redundant activity of even two chitinases is essential for cell separation during saprophytic growth, possibly to improve nutrient access or spreading of yeast cells by wind or rain.

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The RNA-Binding Protein Rrm4 is Essential for Efficient Secretion of Endochitinase Cts1

Cited by 49 publications

References 88 publications

Neurospora crassa NKIN2, a Kinesin-3 Motor, Transports Early Endosomes and Is Required for Polarized Growth

Neurospora crassa NKIN2, a Kinesin-3 Motor, Transports Early Endosomes and Is Required for Polarized Growth

Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes

Chitinases Are Essential for Cell Separation in Ustilago maydis

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