NDK-1, the homolog of NM23-H1/H2 regulates cell migration and apoptotic engulfment in C. elegans

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Fancsalszky, Luca ^a   Monostori, Eszter ^a   Farkas, Zsolt ^a   Pourkarimi, Ehsan ^a,d   Masoudi, Neda ^a,e   Hargitai, Balázs ^a   Bosnar, Maja Herak ^b   Deželjin, Martina ^b   Zsákai, Annamária ^a   Vellai, Tibor ^a   Mehta, Anil ^c   Takács Vellai, Krisztina ^a  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b RUDER BO KOVI INSTITUTE   (Croatia)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; DYNAMIN I; GREEN FLUORESCENT PROTEIN; INTEGRIN; NUCLEOSIDE DIPHOSPHATE KINASE; NUCLEOSIDE DIPHOSPHATE KINASE 1; NUCLEOSIDE DIPHOSPHATE KINASE A; NUCLEOSIDE DIPHOSPHATE KINASE NM23 H2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CELL MIGRATION; CONTROLLED STUDY; DISTAL TIP CELL; ENZYME ACTIVITY; EPISTASIS; GERM CELL; GONADAL SHEATH CELL; LOSS OF FUNCTION MUTATION; NDK 1 GENE; NONHUMAN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; CELL MOVEMENT; CYTOSKELETAL PROTEINS; EMBRYO, NONMAMMALIAN; GENES, LETHAL; HUMANS; MUTATION; NM23 NUCLEOSIDE DIPHOSPHATE KINASES; PHENOTYPE; RAC GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 84899109859     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092687     Document Type: Article

References (52)

1. Marino N, Marshall JC, Steeg PS (2011) Protein-protein interactions: a mechanism regulating the anti-metastatic properties of Nm23-H1. Naunyn Schmiedebergs Arch Pharmacol 384: 351-62.
2. Desvignes T, Pontarotti P, Fauvel C, Bobe J (2009) Nme protein family evolutionary history, a vertebrate perspective. BMC Evol Biol 9: 256.
3. Besant PG, Tan E, Attwood PV (2003) Mammalian protein histidine kinases. Int J Biochem Cell Biol 35: 297-309. (Pubitemid 36084451)
4. Steeg PS, Palmieri D, Ouatas T, Salerno M (2003) Histidine kinases and histidine phosphorylated proteins in mammalian cell biology, signal transduction and cancer. Cancer Lett 190: 1-12. (Pubitemid 36106550)
5. Ma D, McCorkle JR, Kaetzel DM (2004) The metastasis suppressor NM23-H1 possesses 3′-5′ exonuclease activity. J Biol Chem 279: 18073-84. (Pubitemid 38560577)
6. Zhang Q, McCorkle JR, Novak M, Yang M, Kaetzel DM (2011) Metastasis suppressor function of NM23-H1 requires its 3′-5′ exonuclease activity. Int J Cancer 128: 40-50.
7. Fan Z, Beresford PJ, Oh DY, Zhang D, Lieberman J (2003) Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor. Cell 112: 659-72. (Pubitemid 36331778)
8. Postel EH, Weiss VH, Beneken J, Kirtane A (1996) Mutational analysis of NM23-H2/NDP kinase identifies the structural domains critical to recognition of a c-myc regulatory element. Proc Natl Acad Sci USA 93: 6892-7. (Pubitemid 26243470)
9. Nallamothu G, Dammai V, Hsu T (2009) Developmental function of Nm23/awd: a mediator of endocytosis. Mol Cell Biochem 329: 35-44.
10. Annesley SJ, Bago R, Bosnar MH, Filic V, Marinović M, et al. (2011) Dictyostelium discoideum nucleoside diphosphate kinase C plays a negative regulatory role in phagocytosis, macropinocytosis and exocytosis. PLoS One. 6: e26024.
11. Nallamothu G, Woolworth JA, Dammai V, Hsu T (2008) awd, the homolog of metastasis suppressor gene Nm23, regulates Drosophila epithelial cell invasion. Mol Cell Biol 28: 1964-73. (Pubitemid 351342627)
12. Dammai V, Adryan B, Lavenburg KR, Hsu T (2003) Drosophila awd, the homolog of human nm23, regulates FGF receptor levels and functions synergistically with shi/dynamin during tracheal development. Genes & Dev 17: 2812-2824. (Pubitemid 37463290)
13. Baillat G, Gaillard S, Castets F, Monneron A (2002) Interactions of phocein with nucleoside-diphosphate kinase, Eps15, and Dynamin I. J Biol Chem 277: 18961-6. (Pubitemid 34952457)
14. Blelloch R, Newman C, Kimble J (1999) Control of cell migration during Caenorhabditis elegans development. Curr Opin Cell Biol 11: 608-13. (Pubitemid 29460403)
15. Montell DJ (1999) The genetics of cell migration in Drosophila melanogaster and Caenorhabditis elegans development. Development 126: 3035-46.
16. Lehmann R (2001) Cell migration in invertebrates: clues from border and distal tip cells. Curr Opin Genet Dev 11: 457-63.
17. Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126: 1011-1022. (Pubitemid 29142008)
18. Gartner A, Boag PR, Blackwell TK (2008) Germline Survival and Apoptosis. WormBook.
19. Wu YC, Horvitz HR (1998) C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392: 501-4.
20. Reddien PW, Horvitz HR (2000) CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans . Nat Cell Biol 2: 131-6.
21. Meighan CM, Schwarzbauer JE (2007) Control of C. elegans hermaphrodite gonad size and shape by vab-3/Pax6-mediated regulation of integrin receptors. Genes Dev 21: 1615-20. (Pubitemid 47026366)
22. Hurwitz ME, Vanderzalm PJ, Bloom L, Goldman J, Garriga G, et al. (2009) Abl kinase inhibits the engulfment of apoptotic cells in Caenorhabditis elegans. PLoS Biol 7: e99.
23. Hsu TY, Wu YC (2010) Engulfment of apoptotic cells in C. elegans is mediated by integrin a/SRC signaling. Curr Biol 20: 477-86.
24. Mangahas PM, Zhou Z (2005) Clearance of apoptotic cells in Caenorhabditis elegans . Semin Cell Dev Biol 16: 295-306. (Pubitemid 40432130)
25. Masoudi N, Fancsalszky L, Pourkarimi E, Vellai T, Alexa A, et al. (2013) The NM23-H1/H2 homolog NDK-1 is required for full activation of Ras signaling in C. elegans. Development 140: 3486-95.
26. Boissan M, De Wever O, Lizarraga F, Wendum D, Poincloux R, et al. (2010) Implication of metastasis suppressor NM23-H1 in maintaining adherens junctions and limiting the invasive potential of human cancer cells. Cancer Res 70: 7710-22.
27. Perina D, Bosnar MH, Bago R, Mikoč A, Harcet M, et al. (2011) Sponge non-metastatic Group I Nme gene/protein - structure and function is conserved from sponges to humans. BMC Evol Biol 11: 87.
28. Fournier HN, Albiges-Rizo C, Block MR (2003) New insights into Nm23 control of cell adhesion and migration. J Bioenerg Biomembr 35: 81-87. (Pubitemid 36667584)
29. Miyamoto M, Iwashita S, Yamaguchi S, Ono Y (2009) Role of nm23 in the regulation of cell shape and migration via Rho family GTPase signals. Mol Cell Biochem 329: 175-9.
30. She S, Xu B, He M, Lan X, Wang Q (2010) Nm23-H1 suppresses hepatocarcinoma cell adhesion and migration on fibronectin by modulating glycosylation of integrin beta1. J Exp Clin Cancer Res 29: 93.
31. Lee M, Cram EJ, Shen B, Schwarzbauer JE (2001) Roles for bpat-3 integrins in development and function of Caenorhabditis elegans muscles and gonads. J Biol Chem 276: 36404-10.
32. Lee M, Shen B, Schwarzbauer JE, Ahn J, Kwon J (2005) Connections between integrins and Rac GTPase pathways control gonad formation and function in C. elegans. Biochim Biophys Acta. 1723: 248-55. (Pubitemid 40744693)
33. Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56: 110-156. (Pubitemid 8049332)
34. Sulston JE, Schierenberg E, White JG, Thomson N (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100: 64-119.
35. Lundquist EA, Reddien PW, Hartwieg E, Horvitz HR, Bargmann CI (2001) Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 128: 4475-88. (Pubitemid 33130428)
36. Yu X, Odera S, Chuang CH, Lu N, Zhou Z (2006) C. elegans Dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev Cell 10: 743-57. (Pubitemid 43779115)
37. Woolworth JA, Nallamothu G, Hsu T (2009) The Drosophila metastasis suppressor gene Nm23 homolog, awd, regulates epithelial integrity during oogenesis. Mol Cell Biol 29: 4679-90.
38. Cram EJ, Shang H, Schwarzbauer JE (2006) A systematic RNA interference screen reveals a cell migration gene network in C. elegans . J Cell Sci 119: 4811-8. (Pubitemid 46017794)
39. Venturelli D, Martinez R, Melotti P, Casella I, Peschle C, et al. (1995) Overexpression of DR-nm23, a protein encoded by a member of the nm23 gene family, inhibits granulocyte differentiation and induces apoptosis in 32Dc13 myeloid cells. Proc Natl Acad Sci USA 92: 7435-9.
40. Volm M, Mattern J, Koomägi R (1998) Association between nm23-H1 expression, proliferation and apoptosis in non-small cell lung carcinomas. Clin Exp Metastasis 16: 595-602. (Pubitemid 29044582)
41. Negroni A, Venturelli D, Tanno B, Amendola R, Ransac S, et al. (2000) Neuroblastoma specific effects of DR-nm23 and its mutant forms on differentiation and apoptosis. Cell Death Differ 7: 843-50.
42. Kang Y, Lee DC, Han J, Yoon S, Won M, et al. (2007) NM23-H2 involves in negative regulation of Diva and Bcl2L10 in apoptosis signaling. Biochem Biophys Res Commun 359: 76-82. (Pubitemid 46836672)
43. Choudhuri T, Murakami M, Kaul R, Sahu SK, Mohanty S, et al. (2010) Nm23-H1 can induce cell cycle arrest and apoptosis in B cells. Cancer Biol Ther 9: 1065-78.
44. Krishnan KS, Rikhy R, Rao S, Shivalkar M, Mosko M, et al. (2001) Nucleoside diphosphate kinase, a source of GTP, is required for dynamin-dependent synaptic vesicle recycling. Neuron 30: 197-210. (Pubitemid 32441687)
45. Kinchen JM, Cabello J, Klingele D, Wong K, Feichtinger R, et al. (2005) Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans. Nature 434: 93-9. (Pubitemid 40349391)
46. Shen Q, He B, Lu N, Conradt B, Grant BD, et al. (2013) Phagocytic receptor signaling regulates clathrin and epsin-mediated cytoskeletal remodeling during apoptotic cell engulfment in C. elegans. Development 140: 3230-43.
47. Sun J, Wang X, Lau A, Liao TY, Bucci C, et al. (2010) Mycobacterial nucleoside diphosphate kinase blocks phagosome maturation in murine RAW 264.7 macrophages. PLoS One 5: e8769.
48. Elliott MR, Ravichandran KS (2010) Clearance of apoptotic cells: implications in health and disease. J Cell Biol 189: 1059-1070.
49. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 2011 144: 646-74.
50. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
51. Timmons L (2006) Construction of plasmids for RNA interference and in vitro transcription of double-stranded RNA. Methods Mol Biol 351: 109-17.
52. Palmieri D, Halverson DO, Ouatas J, Horak CE, Salerno M, et al. (2005) Medroxyprogesterone acetate elevation of Nm23-H1 metastasis suppressor expression in hormone receptor-negative breast cancer. J Natl Cancer Inst 97: 632-42. (Pubitemid 40812627)