Insights into the biology and prevention of tumor metastasis provided by the Nm23 metastasis suppressor gene

Cancer and Metastasis Reviews

Volumn 31, Issue 3-4, 2012, Pages 593-603

  Marino, Natascia ^a   Nakayama, Joji ^a   Collins, Joshua W ^a   Steeg, Patricia S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Histidine protein kinase; Metastasis; Metastasis suppressor; NDPK; Nm23; NME; Therapeutics

Indexed keywords

ABSINTHOL; ACETYLSALICYLIC ACID; AMENTOFLAVONE; CARNOSINE; GAMMA LINOLENIC ACID; INDOMETACIN; LYSOPHOSPHATIDYLCHOLINE; MEDROXYPROGESTERONE ACETATE; NUCLEOSIDE DIPHOSPHATE KINASE; NUCLEOSIDE DIPHOSPHATE KINASE A; NUCLEOSIDE DIPHOSPHATE KINASE NM23; PHOSPHODIESTERASE I; PROTEIN HISTIDINE KINASE; RETINOIC ACID; SPLEEN EXONUCLEASE; VITAMIN D DERIVATIVE;

AGARICUS BLAZEI; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER CELL; CANCER GENE THERAPY; CANCER INHIBITION; COLON CARCINOMA; DOWN REGULATION; ENZYME ACTIVITY; GENE CONTROL; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; IN VIVO STUDY; MELANOMA; METASTASIS; MOLECULAR BIOLOGY; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN UNFOLDING; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; UPREGULATION;

ANIMALS; GENES, TUMOR SUPPRESSOR; HUMANS; MICE; MICE, TRANSGENIC; NEOPLASM METASTASIS; NM23 NUCLEOSIDE DIPHOSPHATE KINASES; RECEPTORS, LYSOPHOSPHATIDIC ACID; TRANSFECTION;

EID: 84867996816     PISSN: 01677659     EISSN: 15737233     Source Type: Journal    
DOI: 10.1007/s10555-012-9374-8     Document Type: Article

References (128)

1. Steeg, P. S.; et al. (1988). Altered expression of NM23, a gene associated with low tumor metastatic potential, during adenovirus 2 Ela inhibition of experimental metastasis. Cancer Research, 48(22), 6550-6554.
2. Dearolf, C. R.; Hersperger, E.; & Shearn, A. (1988). Developmental consequences of awdb3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Developmental Biology, 129(1), 159-168.
3. Dearolf, C. R.; et al. (1988). Molecular consequences of awdb3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Developmental Biology, 129(1), 169-178.
4. Lacombe, M. L.; et al. (2000). The human Nm23/nucleoside diphosphate kinases. Journal of Bioenergetics and Biomembranes, 32(3), 247-258.
5. Steeg, P. S.; Zollo, M.; & Wieland, T. (2011). A critical evaluation of biochemical activities reported for the nucleoside diphosphate kinase/Nm23/Awd family proteins: opportunities and missteps in understanding their biological functions. Naunyn-Schmiedeberg's Archives of Pharmacology, 384(4-5), 331-339.
6. Berg, P.; & Joklik, W. K. (1953). Transphosphorylation between nucleoside polyphosphates. Nature, 172(4387), 1008-1009.
7. Krebs, H. A.; & Hems, R. (1953). Some reactions of adenosine and inosine phosphates in animal tissues. Biochimica et Biophysica Acta, 12(1-2), 172-180.
8. Wallet, V.; et al. (1990). Dictyostelium nucleoside diphosphate kinase highly homologous to Nm23 and Awd proteins involved in mammalian tumor metastasis and Drosophila development. Journal of the National Cancer Institute, 82(14), 1199-1202.
9. Hippe, H. J.; et al. (2003). Activation of heterotrimeric G proteins by a high energy phosphate transfer via nucleoside diphosphate kinase (NDPK) B and Gbeta subunits. Specific activation of Gsalpha by an NDPK B.Gbetagamma complex in H10 cells. Journal of Biological Chemistry, 278(9), 7227-7233.
10. Lu, Q.; et al. (1995). The gene for nucleoside diphosphate kinase functions as a mutator gene in Escherichia coli. Journal of Molecular Biology, 254(3), 337-341.
11. Hartsough, M. T.; et al. (2002). Nm23-H1 metastasis suppressor phosphorylation of kinase suppressor of Ras via a histidine protein kinase pathway. Journal of Biological Chemistry, 277(35), 32389-32399.
12. Steeg, P. S.; Horak, C. E.; & Miller, K. D. (2008). Clinical-translational approaches to the Nm23-H1 metastasis suppressor. Clinical Cancer Research, 14(16), 5006-5012.
13. Steeg, P. S.; et al. (2003). Histidine kinases and histidine phosphorylated proteins in mammalian cell biology, signal transduction and cancer. Cancer Letters, 190(1), 1-12.
14. Ma, D.; McCorkle, J. R.; & Kaetzel, D. M. (2004). The metastasis suppressor NM23-H1 possesses 3′-5′ exonuclease activity. Journal of Biological Chemistry, 279(17), 18073-18084.
15. Zhang, Q.; et al. (2011). Metastasis suppressor function of NM23-H1 requires its 3′-5′ exonuclease activity. International Journal of Cancer, 128(1), 40-50.
16. Jarrett, S. G.; et al. (2012). Metastasis suppressor NM23-H1 promotes repair of UV-induced DNA damage and suppresses UV-induced melanomagenesis. Cancer Research, 72(1), 133-143.
17. Garzia, L.; et al. (2008). Phosphorylation of nm23-H1 by CKI induces its complex formation with h-prune and promotes cell motility. Oncogene, 27(13), 1853-1864.
18. Reymond, A.; et al. (1999). Evidence for interaction between human PRUNE and nm23-H1 NDPKinase. Oncogene, 18(51), 7244-7252.
19. Kaul, R.; et al. (2007). Epstein-Barr virus latent nuclear antigens can induce metastasis in a nude mouse model. Journal of Virology, 81(19), 10352-10361.
20. Subramanian, C.; Cotter, M. A.; 2nd, & Robertson, E. S. (2001). Epstein-Barr virus nuclear protein EBNA-3C interacts with the human metastatic suppressor Nm23-H1: a molecular link to cancer metastasis. Nature Medicine, 7(3), 350-355.
21. Horak, C. E.; et al. (2007). Nm23-H1 suppresses tumor cell motility by down-regulating the lysophosphatidic acid receptor EDG2. Cancer Research, 67(15), 7238-7246.
22. Horak, C. E.; et al. (2007). Nm23-H1 suppresses metastasis by inhibiting expression of the lysophosphatidic acid receptor EDG2. Cancer Research, 67(24), 11751-11759.
23. Jean-Claude A. Marshall JC. A.; J Collins J.W.; Nakayama J.; Horak H.E.; Liewehr D.J.; et al. (2012). Inhibition of LPA1/EDG2 Induces Metastatic Dormancy in Breast Cancer. JNCI, In press
24. Lee, M. J.; et al. (2011). Pro-oncogenic potential of NM23-H2 in hepatocellular carcinoma. Experimental & Molecular Medicine, 44(3): 214-224
25. Miyazaki, H.; et al. (1999). Overexpression of nm23-H2/NDP kinase B in a human oral squamous cell carcinoma cell line results in reduced metastasis, differentiated phenotype in the metastatic site, and growth factor-independent proliferative activity in culture. Clinical Cancer Research, 5(12), 4301-4307.
26. Boissan, M.; et al. (2010). Implication of metastasis suppressor NM23-H1 in maintaining adherens junctions and limiting the invasive potential of human cancer cells. Cancer Research, 70(19), 7710-7722.
27. Arnaud-Dabernat, S.; et al. (2003). Knockout mice as model systems for studying nm23/NDP kinase gene functions. Application to the nm23-M1 gene. Journal of Bioenergetics and Biomembranes, 35(1), 19-30.
28. Boissan, M.; et al. (2005). Increased lung metastasis in transgenic NM23-Null/SV40 mice with hepatocellular carcinoma. Journal of the National Cancer Institute, 97(11), 836-845.
29. Postel, E. H.; et al. (2009). Targeted deletion of Nm23/nucleoside diphosphate kinase A and B reveals their requirement for definitive erythropoiesis in the mouse embryo. Developmental Dynamics, 238(3), 775-787.
30. Hippe, H. J.; et al. (2009). The interaction of nucleoside diphosphate kinase B with Gbetagamma dimers controls heterotrimeric G protein function. Proceedings of the National Academy of Sciences of the United States of America, 106(38), 16269-16274.
31. Hippe, H. J.; et al. (2011). Nucleoside diphosphate kinase B is required for the formation of heterotrimeric G protein containing caveolae. Naunyn-Schmiedeberg's Archives of Pharmacology, 384(4-5), 461-472.
32. Di, L.; et al. (2010). Nucleoside diphosphate kinase B knock-out mice have impaired activation of the K+ channel KCa3.1, resulting in defective T cell activation. Journal of Biological Chemistry, 285(50), 38765-38771.
33. Sirotkovic-Skerlev, M.; et al. (2005). Expression of c-myc, erbB-2, p53 and nm23-H1 gene product in benign and malignant breast lesions: coexpression and correlation with clinicopathologic parameters. Experimental and Molecular Pathology, 79(1), 42-50.
34. Muller, W.; et al. (1998). Expression of nm23 in gastric carcinoma: association with tumor progression and poor prognosis. Cancer, 83(12), 2481-2487.
35. Kapitanovic, S.; et al. (2004). nm23-H1 expression and loss of heterozygosity in colon adenocarcinoma. Journal of Clinical Pathology, 57(12), 1312-1318.
36. Kumar Dhar, D.; et al. (1999). nm23 in the primary and metastatic sites of gastric carcinoma. Relation to AFP-producing carcinoma. Oncology, 56(2), 122-128.
37. Betke, H.; et al. (1998). The role of nm23 in melanoma progression and its prognostic significance. Polish Journal of Pathology, 49(2), 93-96.
38. Guan-Zhen, Y.; et al. (2007). Reduced protein expression of metastasis-related genes (nm23, KISS1, KAI1 and p53) in lymph node and liver metastases of gastric cancer. International Journal of Experimental Pathology, 88(3), 175-183.
39. Takes, R. P.; et al. (2001). Expression of genetic markers in lymph node metastases compared with their primary tumours in head and neck cancer. The Journal of Pathology, 194(3), 298-302.
40. Ohta, Y.; et al. (2000). Increased vascular endothelial growth factor and vascular endothelial growth factor-c and decreased nm23 expression associated with microdissemination in the lymph nodes in stage I non-small cell lung cancer. The Journal of Thoracic and Cardiovascular Surgery, 119(4 Pt 1), 804-813.
41. Sarac, E.; et al. (1998). nm23 expression in carcinoma of the uterine cervix. European Journal of Gynaecological Oncology, 19(3), 312-315.
42. Terasaki-Fukuzawa, Y.; et al. (2002). Decreased nm23 expression, but not Ki-67 labeling index, is significantly correlated with lymph node metastasis of breast invasive ductal carcinoma. International Journal of Molecular Medicine, 9(1), 25-29.
43. Leone, A.; et al. (1993). Evidence for nm23 RNA overexpression, DNA amplification and mutation in aggressive childhood neuroblastomas. Oncogene, 8(4), 855-865.
44. Oda, Y.; et al. (2000). Comparison of histological changes and changes in nm23 and c-MET expression between primary and metastatic sites in osteosarcoma: a clinicopathologic and immunohistochemical study. Human Pathology, 31(6), 709-716.
45. Niitsu, N.; et al. (2001). Serum nm23-H1 protein as a prognostic factor in aggressive non-Hodgkin lymphoma. Blood, 97(5), 1202-1210.
46. Okabe-Kado, J.; et al. (1995). Inhibitory action of nm23 proteins on induction of erythroid differentiation of human leukemia cells. Biochimica et Biophysica Acta, 1267(2-3), 101-106.
47. Okabe-Kado, J. (2002). Serum nm23-H1 protein as a prognostic factor in hematological malignancies. Leukemia & Lymphoma, 43(4), 859-867.
48. Anzinger, J.; et al. (2001). Secretion of a nucleoside diphosphate kinase (Nm23-H2) by cells from human breast, colon, pancreas and lung tumors. Proceedings of the Western Pharmacology Society, 44, 61-63.
49. Niitsu, N.; et al. (2000). Plasma levels of the differentiation inhibitory factor nm23-H1 protein and their clinical implications in acute myelogenous leukemia. Blood, 96(3), 1080-1086.
50. Okabe-Kado, J.; et al. (2009). Extracellular NM23-H1 protein inhibits the survival of primary cultured normal human peripheral blood mononuclear cells and activates the cytokine production. International Journal of Hematology, 90(2), 143-152.
51. Lilly, A. J.; et al. (2011). Nm23-h1 indirectly promotes the survival of acute myeloid leukemia blast cells by binding to more mature components of the leukemic clone. Cancer Research, 71(3), 1177-1186.
52. Ouatas, T.; Halverson, D.; & Steeg, P. S. (2003). Dexamethasone and medroxyprogesterone acetate elevate Nm23-H1 metastasis suppressor gene expression in metastatic human breast carcinoma cells: new uses for old compounds. Clinical Cancer Research, 9(10 Pt 1), 3763-3772.
53. Palmieri, D.; et al. (2005). Medroxyprogesterone acetate elevation of Nm23-H1 metastasis suppressor expression in hormone receptor-negative breast cancer. Journal of the National Cancer Institute, 97(9), 632-642.
54. Siveen, K. S.; & Kuttan, G. (2011). Thujone inhibits lung metastasis induced by B16F-10 melanoma cells in C57BL/6 mice. Canadian Journal of Physiology and Pharmacology, 89(10), 691-703.
55. Niu, Y. C.; et al. (2009). A low molecular weight polysaccharide isolated from Agaricus blazei Murill (LMPAB) exhibits its anti-metastatic effect by down-regulating metalloproteinase-9 and up-regulating Nm23-H1. The American Journal of Chinese Medicine, 37(5), 909-921.
56. Guruvayoorappan, C.; & Kuttan, G. (2008). Amentoflavone inhibits experimental tumor metastasis through a regulatory mechanism involving MMP-2, MMP-9, prolyl hydroxylase, lysyl oxidase, VEGF, ERK-1, ERK-2, STAT-1, NM23 and cytokines in lung tissues of C57BL/6 mice. Immunopharmacology and Immunotoxicology, 30(4), 711-727.
57. Li, J.; et al. (2006). Inhibition of ovarian cancer metastasis by adeno-associated virus-mediated gene transfer of nm23H1 in an orthotopic implantation model. Cancer Gene Therapy, 13(3), 266-272.
58. Xiang, J. J.; et al. (2003). IONP-PLL: a novel non-viral vector for efficient gene delivery. The Journal of Gene Medicine, 5(9), 803-817.
59. Li, Z.; et al. (2009). Nanoparticle delivery of anti-metastatic NM23-H1 gene improves chemotherapy in a mouse tumor model. Cancer Gene Therapy, 16(5), 423-429.
60. Lim, J.; et al. (2011). Cell-permeable NM23 blocks the maintenance and progression of established pulmonary metastasis. Cancer Research, 71(23), 7216-7225.
61. Choi, J. W.; et al. (2010). LPA receptors: subtypes and biological actions. Annual Review of Pharmacology and Toxicology, 50, 157-186.
62. Ishii, I.; et al. (2004). Lysophospholipid receptors: signaling and biology. Annual Review of Biochemistry, 73, 321-354.
63. Mills, G. B.; & Moolenaar, W. H. (2003). The emerging role of lysophosphatidic acid in cancer. Nature Reviews. Cancer, 3(8), 582-591.
64. Aguirre-Ghiso, J. A.; et al. (2003). ERK(MAPK) activity as a determinant of tumor growth and dormancy; regulation by p38(SAPK). Cancer Research, 63(7), 1684-1695.
65. Aguirre-Ghiso, J. A. (2007). Models, mechanisms and clinical evidence for cancer dormancy. Nature Reviews. Cancer, 7(11), 834-846.
66. Aguirre-Ghiso, J. A.; Ossowski, L.; & Rosenbaum, S. K. (2004). Green fluorescent protein tagging of extracellular signal-regulated kinase and p38 pathways reveals novel dynamics of pathway activation during primary and metastatic growth. Cancer Research, 64(20), 7336-7345.
67. Sosa, M. S.; et al. (2011). ERK1/2 and p38alpha/beta signaling in tumor cell quiescence: opportunities to control dormant residual disease. Clinical Cancer Research, 17(18), 5850-5857.
68. Otsuki, Y.; et al. (2001). Tumor metastasis suppressor nm23H1 regulates Rac1 GTPase by interaction with Tiam1. Proceedings of the National Academy of Sciences of the United States of America, 98(8), 4385-4390.
69. Kim, S. H.; & Kim, J. (2006). Reduction of invasion in human fibrosarcoma cells by ribosomal protein S3 in conjunction with Nm23-H1 and ERK. Biochimica et Biophysica Acta, 1763(8), 823-832.
70. Iwashita, S.; et al. (2004). Lbc proto-oncogene product binds to and could be negatively regulated by metastasis suppressor nm23-H2. Biochemical and Biophysical Research Communications, 320(4), 1063-1068.
71. Zhu, J.; et al. (1999). Interaction of the Ras-related protein associated with diabetes rad and the putative tumor metastasis suppressor NM23 provides a novel mechanism of GTPase regulation. Proceedings of the National Academy of Sciences of the United States of America, 96(26), 14911-14918.
72. Murakami, M.; et al. (2008). The suppressor of metastasis Nm23-H1 interacts with the Cdc42 Rho family member and the pleckstrin homology domain of oncoprotein Dbl-1 to suppress cell migration. Cancer Biology & Therapy, 7(5), 677-688.
73. Palacios, F.; et al. (2002). ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nature Cell Biology, 4(12), 929-936.
74. Seong, H. A.; Jung, H.; & Ha, H. (2007). NM23-H1 tumor suppressor physically interacts with serine-threonine kinase receptor-associated protein, a transforming growth factor-beta (TGF-beta) receptor-interacting protein, and negatively regulates TGF-beta signaling. Journal of Biological Chemistry, 282(16), 12075-12096.
75. Curtis, C. D.; et al. (2007). Interaction of the tumor metastasis suppressor nonmetastatic protein 23 homologue H1 and estrogen receptor alpha alters estrogen-responsive gene expression. Cancer Research, 67(21), 10600-10607.
76. Rayner, K.; et al. (2008). Discovery of NM23-H2 as an estrogen receptor beta-associated protein: role in estrogen-induced gene transcription and cell migration. The Journal of Steroid Biochemistry and Molecular Biology, 108(1-2), 72-81.
77. Paravicini, G.; et al. (1996). The metastasis suppressor candidate nucleotide diphosphate kinase NM23 specifically interacts with members of the ROR/RZR nuclear orphan receptor subfamily. Biochemical and Biophysical Research Communications, 227(1), 82-87.
78. Zheng, L.; Roeder, R. G.; & Luo, Y. (2003). S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell, 114(2), 255-266.
79. Fan, Z.; et al. (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(5), 659-672.
80. Otero, A. S. (2000). NM23/nucleoside diphosphate kinase and signal transduction. Journal of Bioenergetics and Biomembranes, 32(3), 269-275.
81. Pinon, V. P.; et al. (1999). Cytoskeletal association of the A and B nucleoside diphosphate kinases of interphasic but not mitotic human carcinoma cell lines: specific nuclear localization of the B subunit. Experimental Cell Research, 246(2), 355-367.
82. Fournier, H. N.; et al. (2002). Integrin cytoplasmic domain-associated protein 1alpha (ICAP-1alpha) interacts directly with the metastasis suppressor nm23-H2, and both proteins are targeted to newly formed cell adhesion sites upon integrin engagement. Journal of Biological Chemistry, 277(23), 20895-20902.
83. Aktary, Z.; et al. (2010). Plakoglobin interacts with and increases the protein levels of metastasis suppressor Nm23-H2 and regulates the expression of Nm23-H1. Oncogene, 29(14), 2118-2129.
84. D'Angelo, A.; et al. (2004). Prune cAMP phosphodiesterase binds nm23-H1 and promotes cancer metastasis. Cancer Cell, 5(2), 137-149.
85. Polanski, R.; et al. (2011). MDM2 interacts with NME2 (non-metastatic cells 2, protein) and suppresses the ability of NME2 to negatively regulate cell motility. Carcinogenesis, 32(8), 1133-1142.
86. Mileo, A. M.; et al. (2006). Multiple interference of the human papillomavirus-16 E7 oncoprotein with the functional role of the metastasis suppressor Nm23-H1 protein. Journal of Bioenergetics and Biomembranes, 38(3-4), 215-225.
87. Engel, M.; et al. (1998). Glyceraldehyde-3-phosphate dehydrogenase and Nm23-H1/nucleoside diphosphate kinase A. Two old enzymes combine for the novel Nm23 protein phosphotransferase function. Journal of Biological Chemistry, 273(32), 20058-20065.
88. Du, J.; & Hannon, G. J. (2002). The centrosomal kinase Aurora-A/STK15 interacts with a putative tumor suppressor NM23-H1. Nucleic Acids Research, 30(24), 5465-5475.
89. Leone, A.; et al. (1993). 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, 8(9), 2325-2333.
90. Bhujwalla, Z. M.; et al. (1999). Nm23-transfected MDA-MB-435 human breast carcinoma cells form tumors with altered phospholipid metabolism and pH: a 31P nuclear magnetic resonance study in vivo and in vitro. Magnetic Resonance in Medicine, 41(5), 897-903.
91. Russell, R. L.; et al. (1998). Relationship of nm23 to proteolytic factors, proliferation and motility in breast cancer tissues and cell lines. British Journal of Cancer, 78(6), 710-717.
92. Fukuda, M.; et al. (1996). Decreased expression of nucleoside diphosphate kinase alpha isoform, an nm23-H2 gene homolog, is associated with metastatic potential of rat mammary-adenocarcinoma cells. International Journal of Cancer, 65(4), 531-537.
93. Leone, A.; et al. (1991). Reduced tumor incidence, metastatic potential, and cytokine responsiveness of nm23-transfected melanoma cells. Cell, 65(1), 25-35.
94. Baba, H.; et al. (1995). Two isotypes of murine nm23/nucleoside diphosphate kinase, nm23-M1 and nm23-M2, are involved in metastatic suppression of a murine melanoma line. Cancer Research, 55(9), 1977-1981.
95. Parhar, R. S.; et al. (1995). Effects of cytokine-mediated modulation of nm23 expression on the invasion and metastatic behavior of B16F10 melanoma cells. International Journal of Cancer, 60(2), 204-210.
96. Miele, M. E.; et al. (1997). Suppression of human melanoma metastasis following introduction of chromosome 6 is independent of NME1 (Nm23). Clinical & Experimental Metastasis, 15(3), 259-265.
97. Tagashira, H.; et al. (1998). Reduced metastatic potential and c-myc overexpression of colon adenocarcinoma cells (Colon 26 line) transfected with nm23-R2/rat nucleoside diphosphate kinase alpha isoform. International Journal of Molecular Medicine, 2(1), 65-68.
98. Suzuki, E.; et al. (2004). nm23-H1 reduces in vitro cell migration and the liver metastatic potential of colon cancer cells by regulating myosin light chain phosphorylation. International Journal of Cancer, 108(2), 207-211.
99. Bevilacqua, G.; et al. (1989). Association of low nm23 RNA levels in human primary infiltrating ductal breast carcinomas with lymph node involvement and other histopathological indicators of high metastatic potential. Cancer Research, 49(18), 5185-5190.
100. Hennessy, C.; et al. (1991). Expression of the antimetastatic gene nm23 in human breast cancer: an association with good prognosis. Journal of the National Cancer Institute, 83(4), 281-285.
101. Charpin, C.; et al. (1998). Prognostic significance of Nm23/NDPK expression in breast carcinoma, assessed on 10-year follow-up by automated and quantitative immunocytochemical assays. The Journal of Pathology, 184(4), 401-407.
102. Dong, S. W.; et al. (2011). Expression patterns of ER, HER2, and NM23-H1 in breast cancer patients with different menopausal status: correlations with metastasis. Molecular Diagnosis & Therapy, 15(4), 211-219.
103. Heimann, R.; Ferguson, D. J.; & Hellman, S. (1998). The relationship between nm23, angiogenesis, and the metastatic proclivity of node-negative breast cancer. Cancer Research, 58(13), 2766-2771.
104. Tokunaga, Y.; et al. (1993). Reduced expression of nm23-H1, but not of nm23-H2, is concordant with the frequency of lymph-node metastasis of human breast cancer. International Journal of Cancer, 55(1), 66-71.
105. Royds, J. A.; et al. (1993). Nm23 protein expression in ductal in situ and invasive human breast carcinoma. Journal of the National Cancer Institute, 85(9), 727-731.
106. Bal, A.; et al. (2008). Expression of nm23 in the spectrum of pre-invasive, invasive and metastatic breast lesions. Diagnostic Pathology, 3, 23.
107. Ferrari, D.; et al. (2007). Dermatopathological indicators of poor melanoma prognosis are significantly inversely correlated with the expression of NM23 protein in primary cutaneous melanoma. Journal of Cutaneous Pathology, 34(9), 705-712.
108. McDermott, N. C.; et al. (2000). Immunohistochemical expression of nm23 in primary invasive malignant melanoma is predictive of survival outcome. The Journal of Pathology, 190(2), 157-162.
109. Sarris, M.; et al. (2004). Cytoplasmic expression of nm23 predicts the potential for cerebral metastasis in patients with primary cutaneous melanoma. Melanoma Research, 14(1), 23-27.
110. Dome, B.; Somlai, B.; & Timar, J. (2000). The loss of NM23 protein in malignant melanoma predicts lymphatic spread without affecting survival. Anticancer Research, 20(5C), 3971-3974.
111. Pacifico, M. D.; et al. (2005). nm23 as a prognostic marker in primary cutaneous melanoma: evaluation using tissue microarray in a patient group with long-term follow-up. Melanoma Research, 15(5), 435-440.
112. Andolfo, I.; et al. (2011). Correlation of NM23-H1 cytoplasmic expression with metastatic stage in human prostate cancer tissue. Naunyn-Schmiedeberg's Archives of Pharmacology, 384(4-5), 489-498.
113. Mandai, M.; et al. (1994). Expression of metastasis-related nm23-H1 and nm23-H2 genes in ovarian carcinomas: correlation with clinicopathology, EGFR, c-erbB-2, and c-erbB-3 genes, and sex steroid receptor expression. Cancer Research, 54(7), 1825-1830.
114. Hsu, N. Y.; et al. (1999). Expression of nm23 in the primary tumor and the metastatic regional lymph nodes of patients with gastric cardiac cancer. Clinical Cancer Research, 5(7), 1752-1757.
115. Yamaguchi, A.; et al. (1994). Expression of human nm23-H1 and nm23-H2 proteins in hepatocellular carcinoma. Cancer, 73(9), 2280-2284.
116. Guo, H.; et al. (2010). Prognostic significance of co-expression of nm23 and p57 protein in hepatocellular carcinoma. Hepatology Research, 40(11), 1107-1116.
117. An, R.; et al. (2010). Expressions of nucleoside diphosphate kinase (nm23) in tumor tissues are related with metastasis and length of survival of patients with hepatocellular carcinoma. Biomedical and Environmental Sciences, 23(4), 267-272.
118. Hsu, N. Y.; et al. (2007). Prognostic significance of expression of nm23-H1 and focal adhesion kinase in non-small cell lung cancer. Oncology Reports, 18(1), 81-85.
119. Goncharuk, V. N.; et al. (2004). Co-downregulation of PTEN, KAI-1, and nm23-H1 tumor/metastasis suppressor proteins in non-small cell lung cancer. Annals of Diagnostic Pathology, 8(1), 6-16.
120. Ohta, Y.; et al. (2001). The predictive value of vascular endothelial growth factor and nm23 for the diagnosis of occult metastasis in non-small cell lung cancer. Japanese Journal of Cancer Research, 92(3), 361-366.
121. Wang, Y. F.; et al. (2004). Prognostic significance of nm23-H1 expression in oral squamous cell carcinoma. British Journal of Cancer, 90(11), 2186-2193.
122. Engel, M.; et al. (1993). High levels of nm23-H1 and nm23-H2 messenger RNA in human squamous-cell lung carcinoma are associated with poor differentiation and advanced tumor stages. International Journal of Cancer, 55(3), 375-379.
123. Yokoyama, A.; et al. (1996). Differentiation inhibitory factor nm23 as a new prognostic factor in acute monocytic leukemia. Blood, 88(9), 3555-3561.
124. Niitsu, N.; et al. (2003). Expression of nm23-H1 is associated with poor prognosis in peripheral T-cell lymphoma. British Journal of Haematology, 123(4), 621-630.
125. Niitsu, N.; Nakamine, H.; & Okamoto, M. (2011). Expression of nm23-H1 is associated with poor prognosis in peripheral T-cell lymphoma, not otherwise specified. Clinical Cancer Research, 17(9), 2893-2899.
126. Niitsu, N.; et al. (2004). Clinical significance of intracytoplasmic nm23-H1 expression in diffuse large B-cell lymphoma. Clinical Cancer Research, 10(7), 2482-2490.
127. Niitsu, N.; et al. (2008). A clinicopathological study of nm23-H1 expression in classical Hodgkin's lymphoma. Annals of Oncology, 19(11), 1941-1946.
128. Ferenc, T.; et al. (2004). Analysis of nm23-H1 protein immunoreactivity in follicular thyroid tumors. Polish Journal of Pathology, 55(4), 149-153.