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

Zsolt Farkas, Metka Petric, Xianghua Liu, Floriane Herit, E. Rajnavolgyi, Z. Szondy, Zsófia Budai, Tamás I. Orbán, Sára Sándor, Anil Mehta, Z. Bajtay, Tibor Kovács, Sung Yun Jung, Muhammed Afaq Shakir, Jun Qin, Zheng Zhou, Florence Niedergang, Mathieu Boissan, K. 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 : official publication of the Federation of American Societies for Experimental Biology
Volume33
Issue number10
DOIs
Publication statusPublished - Oct 1 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

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

ASJC Scopus subject areas

  • Biotechnology
  • Biochemistry
  • Molecular Biology
  • Genetics

Cite this

The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin. / Farkas, Zsolt; Petric, Metka; Liu, Xianghua; Herit, Floriane; Rajnavolgyi, E.; Szondy, Z.; Budai, Zsófia; Orbán, Tamás I.; Sándor, Sára; Mehta, Anil; Bajtay, Z.; Kovács, Tibor; Jung, Sung Yun; Afaq Shakir, Muhammed; Qin, Jun; Zhou, Zheng; Niedergang, Florence; Boissan, Mathieu; Takács-Vellai, K.

In: FASEB journal : official publication of the Federation of American Societies for Experimental Biology, Vol. 33, No. 10, 01.10.2019, p. 11606-11614.

Research output: Contribution to journalArticle

Farkas, Z, Petric, M, Liu, X, Herit, F, Rajnavolgyi, E, 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 : official publication of the Federation of American Societies for Experimental Biology, vol. 33, no. 10, pp. 11606-11614. https://doi.org/10.1096/fj.201900220R
Farkas, Zsolt ; Petric, Metka ; Liu, Xianghua ; Herit, Floriane ; Rajnavolgyi, E. ; Szondy, Z. ; Budai, Zsófia ; Orbán, Tamás I. ; Sándor, Sára ; Mehta, Anil ; Bajtay, Z. ; Kovács, Tibor ; Jung, Sung Yun ; Afaq Shakir, Muhammed ; Qin, Jun ; Zhou, Zheng ; Niedergang, Florence ; Boissan, Mathieu ; Takács-Vellai, K. / The nucleoside diphosphate kinase NDK-1/NME1 promotes phagocytosis in concert with DYN-1/Dynamin. In: FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2019 ; Vol. 33, No. 10. pp. 11606-11614.
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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 - Rajnavolgyi, E.

AU - Szondy, Z.

AU - Budai, Zsófia

AU - Orbán, Tamás I.

AU - Sándor, Sára

AU - Mehta, Anil

AU - Bajtay, Z.

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, K.

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 - actin cup

KW - apoptotic clearance

KW - metastasis inhibitor

KW - phagosome formation

KW - phagosome maturation

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