Metastasis suppressor NM23-H1 promotes repair of UV-induced DNA damage and suppresses UV-induced melanomagenesis

Cancer Research

Volumn 72, Issue 1, 2012, Pages 133-143

  Jarrett, Stuart G ^a   Novak, Marian ^a   Dabernat, Sandrine ^b   Daniel, Jean Yves ^b   Mellon, Isabel ^a   Zhang, Qingbei ^a   Harris, Nathan ^a   Ciesielski, Michael J ^c   Fenstermaker, Robert A ^c   Kovacic, Diane ^d   Slominski, Andrzej ^d   Kaetzel, David M ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA POLYMERASE; NUCLEOSIDE DIPHOSPHATE KINASE; NUCLEOSIDE DIPHOSPHATE KINASE A; PHOSPHODIESTERASE I; SPLEEN EXONUCLEASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CANCER INVASION; CELL NUCLEUS; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; EMBRYO; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME DEFICIENCY; EXCISION REPAIR; GENE MUTATION; HEMIZYGOTE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MELANOCYTE; MELANOMA; MELANOMA CELL; METASTASIS INHIBITION; MOUSE; MUTAGENESIS; NM23 M1 GENE; NM23 M2 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; RADIATION CARCINOGENESIS; SUPPRESSOR GENE; TRANSGENIC MOUSE; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION; ULTRAVIOLET C RADIATION; ULTRAVIOLET RADIATION;

ANIMALS; CELL LINE, TUMOR; DNA DAMAGE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MUTATION; NEOPLASMS, RADIATION-INDUCED; NM23 NUCLEOSIDE DIPHOSPHATE KINASES; ULTRAVIOLET RAYS;

EID: 84855378399     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-1795     Document Type: Article

References (50)

1. Rinker-Schaeffer CW, O'Keefe JP, Welch DR, Theodorescu D. Metastasis suppressor proteins: discovery, molecular mechanisms, and clinical application. Clin Cancer Res 2006;12:3882-9. (Pubitemid 44078070)
2. Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med 2006;12:895-904. (Pubitemid 44175140)
3. Steeg PS, Bevilacqua G, Pozzatti R, Liotta LA, Sobel ME. Altered expression of NM23, a gene associated with low tumor metastatic potential, during adenovirus 2 Ela inhibition of experimental metastasis. Cancer Res 1988;48:6550-4.
4. Leone A, Flatow U, VanHoutte K, Steeg PS. Transfection of human nm23-H1 into the human MDA-MB-435 breast carcinoma cell line: effects on tumor metastatic potential, colonization and enzymatic activity. Oncogene 1993;8:2325-33. (Pubitemid 23252360)
5. Leone A, Flatow U, King CR, Sandeen MA, Margulies IM, Liotta LA, et al. Reduced tumor incidence, metastatic potential, and cytokine responsiveness of nm23-transfected melanoma cells. Cell 1991;65: 25-35. (Pubitemid 121001210)
6. Ferrari D, Lombardi M, Ricci R, Michiara M, Santini M, De Panfilis G. Dermatopathological indicators of poor melanoma prognosis are significantly inversely correlated with the expression of NM23 protein in primary cutaneous melanoma. J Cutan Pathol 2007;34:705-12. (Pubitemid 47256248)
7. Florenes VA, Aamdal S, Myklebost O, Maelandsmo GM, Bruland OS, Fodstad O. Levels of nm23 messenger RNA in metastatic malignant melanomas: inverse correlation to disease progression. Cancer Res 1992;52:6088-91.
8. Caligo MA, Grammatico P, Cipollini G, Varesco L, Del Porto G, Bevilacqua G. A low NM23.H1 gene expression identifying high malignancy human melanomas. Melanoma Res 1994;4:179-84. (Pubitemid 24208278)
9. Agarwal RP, Robison B, Parks RE Jr. Nucleoside diphosphokinase from human erythrocytes. Methods Enzymol 1978;51:376-86.
10. Freije JM, Blay P, MacDonald NJ, ManrowRE, Steeg PS. Site-directed mutation of Nm23-H1. Mutations lacking motility suppressive capacity upon transfection are deficient in histidine-dependent protein phosphotransferase pathways in vitro. J Biol Chem 1997;272:5525-32. (Pubitemid 27102375)
11. Steeg PS, Palmieri D, Ouatas T, Salerno M. Histidine kinases and histidine phosphorylated proteins in mammalian cell biology, signal transduction and cancer. Cancer Lett 2003;190:1-12. (Pubitemid 36106550)
12. Postel EH. Cleavage of DNA by human NM23-H2/nucleoside diphosphate kinase involves formation of a covalent protein-DNA complex. J Biol Chem 1999;274:22821-9.
13. Postel EH, Abramczyk BM, Levit MN, Kyin S. Catalysis of DNA cleavage and nucleoside triphosphate synthesis by NM23-H2/NDP kinase share an active site that implies a DNA repair function. Proc Natl Acad Sci U SA 2000;97:14194-9. (Pubitemid 32016553)
14. Ma D, McCorkle JR, Kaetzel DM.The metastasis suppressor NM23-H1 possesses 3′-5′ exonuclease activity. J Biol Chem 2004;279: 18073-84. (Pubitemid 38560577)
15. Shevelev IV, Hubscher U. The 3′ 5′ exonucleases. Nat Rev Mol Cell Biol 2002;3:364-76.
16. Yang M, Jarrett SG, Craven R, Kaetzel DM. YNK1, the yeast homolog of human metastasis suppressor NM23, is required for repair of UV radiation- and etoposide-induced DNA damage. Mutat Res 2009;660: 74-8.
17. Zhang Q, McCorkle JR, Novak M, Yang M, Kaetzel DM. Metastasis suppressor function of NM23-H1 requires its 3′;-5′ exonuclease activity. Int J Cancer 2010;128:40-50.
18. Herlyn M, Thurin J, Balaban G, Bennicelli JL, Herlyn D, Elder DE, et al. Characteristics of cultured human melanocytes isolated from different stages of tumor progression. Cancer Res 1985;45:5670-6. (Pubitemid 16218571)
19. Herlyn M, Balaban G, Bennicelli J, Guerry Dt, Halaban R, Herlyn D, et al. Primary melanoma cells of the vertical growth phase: similarities to metastatic cells. J Natl Cancer Inst 1985;74:283-9. (Pubitemid 15112114)
20. Arnaud-Dabernat S, Bourbon PM, Dierich A, Le Meur M, Daniel JY. Knockout mice as model systems for studying nm23/NDP kinase gene functions. Application to the nm23-M1 gene. J Bioenerg Biomembr 2003;35:19-30. (Pubitemid 36667577)
21. Postel EH, Wohlman I, Zou X, Juan T, Sun N, D'Agostin D, et al. Targeted deletion of Nm23/nucleoside diphosphate kinase A and B reveals their requirement for definitive erythropoiesis in the mouse embryo. Dev Dyn 2009;238:775-87.
22. Scott TL, Wakamatsu K, Ito S, D'Orazio JA. Purification and growth of melanocortin 1 receptor (Mc1r)- defective primary murine melanocytes is dependent on stem cell factor (SFC) from keratinocyte-conditioned media. In Vitro Cell Dev Biol Anim 2009;45:577-83.
23. Ayala-Torres S, Chen Y, Svoboda T, Rosenblatt J, Van Houten B. Analysis of gene-specific DNA damage and repair using quantitative polymerase chain reaction. Methods 2000;22:135-47. (Pubitemid 32896718)
24. Ford JM, Hanawalt PC. Expression of wild-type p53 is required for efficient global genomic nucleotide excision repair in UV-irradiated human fibroblasts. J Biol Chem 1997;272:28073-80. (Pubitemid 27473616)
25. Wulff BC, Schick JS, Thomas-Ahner JM, Kusewitt DF, Yarosh DB, Oberyszyn TM. Topical treatment with OGG1 enzyme affects UVBinduced skin carcinogenesis. Photochem Photobiol 2008;84:317-21. (Pubitemid 351421383)
26. Mone MJ, Volker M, Nikaido O, Mullenders LH, van Zeeland AA, Verschure PJ, et al. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep 2001;2:1013-7. (Pubitemid 33130608)
27. Glaab WE, Tindall KR. Mutation rate at the hprt locus in human cancer cell lines with specific mismatch repair-gene defects. Carcinogenesis 1997;18:1-8. (Pubitemid 28134609)
28. Glaab WE, Risinger JI, Umar A, Barrett JC, Kunkel TA, Tindall KR. Cellular resistance and hypermutability in mismatch repair-deficient human cancer cell lines following treatment with methyl methanesulfonate. Mutat Res 1998;398:197-207. (Pubitemid 28225038)
29. Tomayko MM, Reynolds CP. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 1989; 24:148-54. (Pubitemid 19163397)
30. Hanawalt PC, Ford JM, Lloyd DR. Functional characterization of global genomic DNA repair and its implications for cancer. Mutat Res 2003;544:107-14. (Pubitemid 37487654)
31. Rossman TG, Goncharova EI, Nadas A. Modeling and measurement of the spontaneous mutation rate in mammalian cells. Mutat Res 1995; 328:21-30.
32. Kath R, Jambrosic JA, Holland L, Rodeck U, Herlyn M. Development of invasive and growth factor-independent cell variants from primary human melanomas. Cancer Res 1991;51:2205-11.
33. Noonan FP, Otsuka T, Bang S, Anver MR, Merlino G. Accelerated ultraviolet radiation-induced carcinogenesis in hepatocyte growth factor/scatter factor transgenic mice. Cancer Res 2000;60:3738-43. (Pubitemid 32204561)
34. Nordman J, Wright A. The relationship between dNTP pool levels and mutagenesis in an Escherichia coli NDP kinase mutant. Proc Natl Acad Sci USA 2008;105:10197-202.
35. Lu Q, Zhang X, Almaula N, Mathews CK, Inouye M. The gene for nucleoside diphosphate kinase functions as a mutator gene in Escherichia coli. J Mol Biol 1995;254:337-41. (Pubitemid 26001773)
36. Shuck SC, Short EA, Turchi JJ. Eukaryotic nucleotide excision repair: from understanding mechanisms to influencing biology. Cell Res 2008;18:64-72.
37. Zhang ZM, Yang XQ, Wang D, Wang G, Yang ZZ, Qing Y, et al. Nm23- H1 protein binds to APE1 at AP sites and stimulates AP endonuclease activity following ionizing radiation of the human lung cancer A549 cells. Cell Biochem. Biophys 2011;61:561-72.
38. Yoon JH, Singh P, Lee DH, Qiu J, Cai S, O'Connor TR, et al. Characterization of the 3′ → 5′ exonuclease activity found in human nucleoside diphosphate kinase 1 (NDK1) and several of its homologues. Biochemistry 2005;44:15774-86. (Pubitemid 41746909)
39. Murthy S, Reddy GP. Replitase: complete machinery for DNA synthesis. J Cell Physiol 2006;209:711-7. (Pubitemid 44665692)
40. Kim J, Wheeler LJ, Shen R, Mathews CK. Protein-DNA interactions in the T4 dNTP synthetase complex dependent on gene 32 singlestranded DNA-binding protein. Mol Microbiol 2005;55:1502-14. (Pubitemid 40342075)
41. Shen R, Olcott MC, Kim J, Rajagopal I, Mathews CK. Escherichia coli nucleoside diphosphate kinase interactions with T4 phage proteins of deoxyribonucleotide synthesis and possible regulatory functions. J Biol Chem 2004;279:32225-32. (Pubitemid 39014671)
42. Kimura T, Takeda S, Sagiya Y, Gotoh M, Nakamura Y, Arakawa H. Impaired function of p53R2 in Rrm2b-null mice causes severe renal failure through attenuation of dNTP pools. Nat Genet 2003;34:440-5. (Pubitemid 36935338)
43. Kunos CA, Colussi VC, Pink J, Radivoyevitch T, Oleinick NL. Radiosensitization of human cervical cancer cells by inhibiting ribonucleotide reductase: enhanced radiation response at low-dose rates. Int J Radiat Oncol 2011;80:1198-204.
44. Chen YL, Eriksson S, Chang ZF. Regulation and functional contribution of thymidine kinase 1 in repair of DNA damage. J Biol Chem 2010; 285:27327-35.
45. Niida H, Katsuno Y, Sengoku M, Shimada M, Yukawa M, Ikura M, et al. Essential role of Tip60-dependent recruitment of ribonucleotide reductase at DNA damage sites in DNA repair during G1 phase. Genes Dev 2010;24:333-8.
46. Koberle B, Roginskaya V, Wood RD. XPA protein as a limiting factor for nucleotide excision repair and UV sensitivity in human cells. DNA Repair 2006;5:641-8.
47. Emmert S, Kobayashi N, Khan SG, Kraemer KH. The xeroderma pigmentosum group C gene leads to selective repair of cyclobutane pyrimidine dimers rather than 6-4 photoproducts. Proc Natl Acad SciU S A 2000;97:2151-56. (Pubitemid 30134037)
48. Yang G, Curley D, Bosenberg MW, Tsao H. Loss of xeroderma pigmentosum C (Xpc) enhances melanoma photocarcinogenesis in Ink4a-Arf-deficient mice. Cancer Res 2007;67:5649-57. (Pubitemid 46984996)
49. van Schanke A, van Venrooij GM, Jongsma MJ, Banus HA, Mullenders LH, van Kranen HJ, et al. Induction of nevi and skin tumors in Ink4a/Arf Xpa knockout mice by neonatal, intermittent, or chronic UVB exposures. Cancer Res 2006;66:2608-15.
50. Boissan M, Wendum D, Arnaud-Dabernat S, Munier A, Debray M, Lascu I, et al. Increased lung metastasis in transgenic NM23-Null/SV40 mice with hepatocellular carcinoma. J Natl Cancer Inst 2005;97: 836-45. (Pubitemid 40909126)