Cargando…

The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin

Phagocytosis of various targets, such as apoptotic cells or opsonized pathogens, by macrophages is coordinated by a complex signaling network initiated by distinct phagocytic receptors. Despite the different initial signaling pathways, each pathway ends up regulating the actin cytoskeletal network,...

Descripción completa

Detalles Bibliográficos
Autores principales: Farkas, Zsolt, Petric, Metka, Liu, Xianghua, Herit, Floriane, Rajnavölgyi, Éva, Szondy, Zsuzsa, Budai, Zsófia, Orbán, Tamás I., Sándor, Sára, Mehta, Anil, Bajtay, Zsuzsa, Kovács, Tibor, Jung, Sung Yun, Afaq Shakir, Muhammed, Qin, Jun, Zhou, Zheng, Niedergang, Florence, Boissan, Mathieu, Takács-Vellai, Krisztina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Federation of American Societies for Experimental Biology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6819981/
https://www.ncbi.nlm.nih.gov/pubmed/31242766
http://dx.doi.org/10.1096/fj.201900220R
_version_ 1783463852689588224
author Farkas, Zsolt
Petric, Metka
Liu, Xianghua
Herit, Floriane
Rajnavölgyi, Éva
Szondy, Zsuzsa
Budai, Zsófia
Orbán, Tamás I.
Sándor, Sára
Mehta, Anil
Bajtay, Zsuzsa
Kovács, Tibor
Jung, Sung Yun
Afaq Shakir, Muhammed
Qin, Jun
Zhou, Zheng
Niedergang, Florence
Boissan, Mathieu
Takács-Vellai, Krisztina
author_facet Farkas, Zsolt
Petric, Metka
Liu, Xianghua
Herit, Floriane
Rajnavölgyi, Éva
Szondy, Zsuzsa
Budai, Zsófia
Orbán, Tamás I.
Sándor, Sára
Mehta, Anil
Bajtay, Zsuzsa
Kovács, Tibor
Jung, Sung Yun
Afaq Shakir, Muhammed
Qin, Jun
Zhou, Zheng
Niedergang, Florence
Boissan, Mathieu
Takács-Vellai, Krisztina
author_sort Farkas, Zsolt
collection PubMed
description Phagocytosis of various targets, such as apoptotic cells or opsonized pathogens, by macrophages is coordinated by a complex signaling network initiated by distinct phagocytic receptors. Despite the different initial signaling pathways, each pathway ends up regulating the actin cytoskeletal network, phagosome formation and closure, and phagosome maturation leading to degradation of the engulfed particle. Herein, we describe a new phagocytic function for the nucleoside diphosphate kinase 1 (NDK-1), the nematode counterpart of the first identified metastasis inhibitor NM23-H1 (nonmetastatic clone number 23) nonmetastatic clone number 23 or nonmetastatic isoform 1 (NME1). We reveal by coimmunoprecipitation, Duolink proximity ligation assay, and mass spectrometry that NDK-1/NME1 works in a complex with DYN-1/Dynamin (Caenorhabditis elegans/human homolog proteins), which is essential for engulfment and phagosome maturation. Time-lapse microscopy shows that NDK-1 is expressed on phagosomal surfaces during cell corpse clearance in the same time window as DYN-1. Silencing of NM23-M1 in mouse bone marrow–derived macrophages resulted in decreased phagocytosis of apoptotic thymocytes. In human macrophages, NM23-H1 and Dynamin are corecruited at sites of phagosome formation in F-actin–rich cups. In addition, NM23-H1 was required for efficient phagocytosis. Together, our data demonstrate that NDK-1/NME1 is an evolutionarily conserved element of successful phagocytosis.—Farkas, Z., Petric, M., Liu, X., Herit, F., Rajnavölgyi, É., Szondy, Z., Budai, Z., Orbán, T. I., Sándor, S., Mehta, A., Bajtay, Z., Kovács, T., Jung, S. Y., Afaq Shakir, M., Qin, J., Zhou, Z., Niedergang, F., Boissan, M., Takács-Vellai, K. The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/dynamin.
format Online
Article
Text
id pubmed-6819981
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Federation of American Societies for Experimental Biology
record_format MEDLINE/PubMed
spelling pubmed-68199812019-11-04 The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin Farkas, Zsolt Petric, Metka Liu, Xianghua Herit, Floriane Rajnavölgyi, Éva Szondy, Zsuzsa Budai, Zsófia Orbán, Tamás I. Sándor, Sára Mehta, Anil Bajtay, Zsuzsa Kovács, Tibor Jung, Sung Yun Afaq Shakir, Muhammed Qin, Jun Zhou, Zheng Niedergang, Florence Boissan, Mathieu Takács-Vellai, Krisztina FASEB J Research Phagocytosis of various targets, such as apoptotic cells or opsonized pathogens, by macrophages is coordinated by a complex signaling network initiated by distinct phagocytic receptors. Despite the different initial signaling pathways, each pathway ends up regulating the actin cytoskeletal network, phagosome formation and closure, and phagosome maturation leading to degradation of the engulfed particle. Herein, we describe a new phagocytic function for the nucleoside diphosphate kinase 1 (NDK-1), the nematode counterpart of the first identified metastasis inhibitor NM23-H1 (nonmetastatic clone number 23) nonmetastatic clone number 23 or nonmetastatic isoform 1 (NME1). We reveal by coimmunoprecipitation, Duolink proximity ligation assay, and mass spectrometry that NDK-1/NME1 works in a complex with DYN-1/Dynamin (Caenorhabditis elegans/human homolog proteins), which is essential for engulfment and phagosome maturation. Time-lapse microscopy shows that NDK-1 is expressed on phagosomal surfaces during cell corpse clearance in the same time window as DYN-1. Silencing of NM23-M1 in mouse bone marrow–derived macrophages resulted in decreased phagocytosis of apoptotic thymocytes. In human macrophages, NM23-H1 and Dynamin are corecruited at sites of phagosome formation in F-actin–rich cups. In addition, NM23-H1 was required for efficient phagocytosis. Together, our data demonstrate that NDK-1/NME1 is an evolutionarily conserved element of successful phagocytosis.—Farkas, Z., Petric, M., Liu, X., Herit, F., Rajnavölgyi, É., Szondy, Z., Budai, Z., Orbán, T. I., Sándor, S., Mehta, A., Bajtay, Z., Kovács, T., Jung, S. Y., Afaq Shakir, M., Qin, J., Zhou, Z., Niedergang, F., Boissan, M., Takács-Vellai, K. The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/dynamin. Federation of American Societies for Experimental Biology 2019-10 2019-07-17 /pmc/articles/PMC6819981/ /pubmed/31242766 http://dx.doi.org/10.1096/fj.201900220R Text en © FASEB http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Farkas, Zsolt
Petric, Metka
Liu, Xianghua
Herit, Floriane
Rajnavölgyi, Éva
Szondy, Zsuzsa
Budai, Zsófia
Orbán, Tamás I.
Sándor, Sára
Mehta, Anil
Bajtay, Zsuzsa
Kovács, Tibor
Jung, Sung Yun
Afaq Shakir, Muhammed
Qin, Jun
Zhou, Zheng
Niedergang, Florence
Boissan, Mathieu
Takács-Vellai, Krisztina
The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin
title The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin
title_full The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin
title_fullStr The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin
title_full_unstemmed The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin
title_short The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin
title_sort nucleoside diphosphate kinase ndk-1/nme1 promotes phagocytosis in concert with dyn-1/dynamin
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6819981/
https://www.ncbi.nlm.nih.gov/pubmed/31242766
http://dx.doi.org/10.1096/fj.201900220R
work_keys_str_mv AT farkaszsolt thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT petricmetka thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT liuxianghua thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT heritfloriane thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT rajnavolgyieva thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT szondyzsuzsa thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT budaizsofia thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT orbantamasi thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT sandorsara thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT mehtaanil thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT bajtayzsuzsa thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT kovacstibor thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT jungsungyun thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT afaqshakirmuhammed thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT qinjun thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT zhouzheng thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT niedergangflorence thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT boissanmathieu thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT takacsvellaikrisztina thenucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT farkaszsolt nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT petricmetka nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT liuxianghua nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT heritfloriane nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT rajnavolgyieva nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT szondyzsuzsa nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT budaizsofia nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT orbantamasi nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT sandorsara nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT mehtaanil nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT bajtayzsuzsa nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT kovacstibor nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT jungsungyun nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT afaqshakirmuhammed nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT qinjun nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT zhouzheng nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT niedergangflorence nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT boissanmathieu nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin
AT takacsvellaikrisztina nucleosidediphosphatekinasendk1nme1promotesphagocytosisinconcertwithdyn1dynamin