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

Zsolt Farkas, Metka Petric, Xianghua Liu, Floriane Herit, Éva Rajnavölgyi, Zsuzsa Szondy, Zsófia Budai, Tamás I. Orbán, Sára Sándor, Anil Mehta, Zsuzsa Bajtay, Tibor Kovács, Sung Yun Jung, Muhammed Afaq Shakir, Jun Qin, Zheng Zhou, Florence Niedergang, Mathieu Boissan, Krisztina Takács-Vellai

    Research output: Contribution to journalArticle

    Abstract

    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.

    Original languageEnglish
    Pages (from-to)11606-11614
    Number of pages9
    JournalFASEB Journal
    Volume33
    Issue number10
    Early online date17 Jul 2019
    DOIs
    Publication statusPublished - 1 Oct 2019

    Fingerprint

    Dynamin I
    Nucleoside-Diphosphate Kinase
    Phagocytosis
    Phagosomes
    Protein Isoforms
    Macrophages
    Actins
    Clone Cells
    Dynamins
    Caenorhabditis elegans
    Pathogens
    Thymocytes
    Cadaver
    Mass spectrometry
    Ligation
    Microscopy
    Assays
    Mass Spectrometry
    Microscopic examination
    Bone

    Keywords

    • metastasis inhibitor
    • apoptotic clearance
    • phagosome formation
    • phagosome maturation
    • actin cup

    Cite this

    Farkas, Z., Petric, M., Liu, X., Herit, F., Rajnavölgyi, É., Szondy, Z., ... Takács-Vellai, K. (2019). The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin. FASEB Journal, 33(10), 11606-11614. https://doi.org/10.1096/fj.201900220R
    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. In: FASEB Journal. 2019 ; Vol. 33, No. 10. pp. 11606-11614.
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    abstract = "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., Rajnav{\"o}lgyi, {\'E}., Szondy, Z., Budai, Z., Orb{\'a}n, T. I., S{\'a}ndor, S., Mehta, A., Bajtay, Z., Kov{\'a}cs, T., Jung, S. Y., Afaq Shakir, M., Qin, J., Zhou, Z., Niedergang, F., Boissan, M., Tak{\'a}cs-Vellai, K. The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/dynamin.",
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    author = "Zsolt Farkas and Metka Petric and Xianghua Liu and Floriane Herit and {\'E}va Rajnav{\"o}lgyi and Zsuzsa Szondy and Zs{\'o}fia Budai and Orb{\'a}n, {Tam{\'a}s I.} and S{\'a}ra S{\'a}ndor and Anil Mehta and Zsuzsa Bajtay and Tibor Kov{\'a}cs and Jung, {Sung Yun} and {Afaq Shakir}, Muhammed and Jun Qin and Zheng Zhou and Florence Niedergang and Mathieu Boissan and Krisztina Tak{\'a}cs-Vellai",
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    language = "English",
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    Farkas, Z, Petric, M, Liu, X, Herit, F, Rajnavölgyi, É, Szondy, Z, Budai, Z, Orbán, TI, Sándor, S, Mehta, A, Bajtay, Z, Kovács, T, Jung, SY, Afaq Shakir, M, Qin, J, Zhou, Z, Niedergang, F, Boissan, M & Takács-Vellai, K 2019, 'The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin', FASEB Journal, vol. 33, no. 10, pp. 11606-11614. https://doi.org/10.1096/fj.201900220R

    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.

    In: FASEB Journal, Vol. 33, No. 10, 01.10.2019, p. 11606-11614.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin

    AU - Farkas, Zsolt

    AU - Petric, Metka

    AU - Liu, Xianghua

    AU - Herit, Floriane

    AU - Rajnavölgyi, Éva

    AU - Szondy, Zsuzsa

    AU - Budai, Zsófia

    AU - Orbán, Tamás I.

    AU - Sándor, Sára

    AU - Mehta, Anil

    AU - Bajtay, Zsuzsa

    AU - Kovács, Tibor

    AU - Jung, Sung Yun

    AU - Afaq Shakir, Muhammed

    AU - Qin, Jun

    AU - Zhou, Zheng

    AU - Niedergang, Florence

    AU - Boissan, Mathieu

    AU - Takács-Vellai, Krisztina

    PY - 2019/10/1

    Y1 - 2019/10/1

    N2 - 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.

    AB - 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.

    KW - metastasis inhibitor

    KW - apoptotic clearance

    KW - phagosome formation

    KW - phagosome maturation

    KW - actin cup

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    DO - 10.1096/fj.201900220R

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    Farkas Z, Petric M, Liu X, Herit F, Rajnavölgyi É, Szondy Z et al. The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin. FASEB Journal. 2019 Oct 1;33(10):11606-11614. https://doi.org/10.1096/fj.201900220R