The N-terminal RASSF family: A new group of Ras-association-domain-containing proteins, with emerging links to cancer formation

Biochemical Journal

Volumn 425, Issue 2, 2010, Pages 303-311

  Sherwood, Victoria ^a,b   Recino, Asha ^a   Jeffries, Alex ^a   Ward, Andrew ^a   Chalmers, Andrew D ^a  

^a University of Bath   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

Author keywords

N terminal Ras association domain family (RASSF7 10); Tumour suppressor; Ubiquitin fold

Indexed keywords

BIOLOGICAL PROCESS; DOMAIN-CONTAINING PROTEINS; MICROTUBULE STABILITY; N-TERMINALS; NEW MEMBERS; PROMOTER METHYLATION; TUMOUR SUPPRESSOR; UBIQUITIN; VESICLE TRAFFICKING;

CELL DEATH; TUMORS;

PROTEINS;

GUANOSINE TRIPHOSPHATASE; PROTEIN P53; RAS ASSOCIATION DOMAIN FAMILY PROTEIN; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 10; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 7; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 8; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 9; RAS PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ACUTE LYMPHOCYTIC LEUKEMIA; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; APOPTOSIS; CANCER GROWTH; CANCER RISK; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL PROLIFERATION; CHILDHOOD LEUKEMIA; CHROMOSOME 3P; DOWN REGULATION; ENDOMETRIUM CARCINOMA; GERM CELL TUMOR; HUMAN; HYPOXIA; LUNG ADENOCARCINOMA; MICROTUBULE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CARCINOMA; PANCREAS ADENOCARCINOMA; PANCREAS ISLET CELL TUMOR; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; TUMOR SUPPRESSOR GENE; UPREGULATION;

CELL PHYSIOLOGICAL PHENOMENA; HUMANS; NEOPLASMS; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 73849132617     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20091318     Document Type: Review

References (106)

1. Takai, Y., Sasaki, T. and Matozaki, T. (2001) Small GTP-binding proteins. Physiol. Rev. 81, 153-208
2. Cully, M. and Downward, J. (2008) SnapShot: Ras Signaling. Cell 133, 1292-1292.e1
3. Hancock, J. F. and Parton, R. G. (2005) Ras plasma membrane signalling platforms. Biochem. J. 389, 1-11
4. Tanaka, T. and Rabbitts, T. H. (2008) Interfering with protein-protein interactions: potential for cancer therapy. Cell Cycle 7, 1569-1574
5. Sherwood, V., Manbodh, R., Sheppard, C. and Chalmers, A. D. (2008) RASSF7 is a member of a new family of Ras association domain-containing proteins and is required for completing mitosis. Mol. Biol. Cell 19, 1772-1782
6. Avruch, J., Xavier, R., Bardeesy, N., Zhang, X. F., Praskova, M., Zhou, D. and Xia, F. (2009) Rassf family of tumor suppressor polypeptides. J. Biol. Chem. 284, 11001-11005
7. Richter, A. M., Pfeifer, G. P. and Dammann, R. H. (2009) The RASSF proteins in cancer; from epigenetic silencing to functional characterization. Biochim. Biophys. Acta 1796, 114-128
8. van der Weyden, L. and Adams, D. J. (2007) The Ras-association domain family (RASSF) members and their role in human tumourigenesis. Biochim. Biophys. Acta 1776, 58-85
9. Dammann, R., Schagdarsurengin, U., Seidel, C., Strunnikova, M., Rastetter, M., Baier, K. and Pfeifer, G. P. (2005) The tumor suppressor RASSF1A in human carcinogenesis: an update. Histol. Histopathol. 20, 645-663
10. Donninger, H., Vos, M. D. and Clark, G. J. (2007) The RASSF1A tumor suppressor. J. Cell. Sci. 120, 3163-3172
11. Hesson, L. B., Cooper, W. N. and Latif, F. (2007) The role of RASSF1A methylation in cancer. Dis. Markers 23, 73-87
12. Ponting, C. P. and Benjamin, D. R. (1996) A novel family of Ras-binding domains. Trends Biochem. Sci. 21, 422-425
13. Wohlgemuth, S., Kiel, C., Kramer, A., Serrano, L., Wittinghofer, F. and Herrmann, C. (2005) Recognizing and defining true Ras binding domains I: biochemical analysis. J. Mol. Biol. 348, 741-758
14. Rodriguez-Viciana, P., Sabatier, C. and McCormick, F. (2004) Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Mol. Cell. Biol. 24, 4943-4954
15. Kalhammer, G., Bahler, M., Schmitz, F., Jockel, J. and Block, C. (1997) Ras-binding domains: predicting function versus folding. FEBS Lett. 414, 599-602
16. Herrmann, C. (2003) Ras-effector interactions: after one decade. Curr. Opin. Struct. Biol. 13, 122-129
17. Scheel, H. and Hofmann, K. (2003) A novel interaction motif, SARAH, connects three classes of tumor suppressor. Curr. Biol. 13, R899-R900
18. Hwang, E., Ryu, K. S., Paakkonen, K., Guntert, P., Cheong, H. K., Lim, D. S., Lee, J. O., Jeon, Y. H. and Cheong, C. (2007) Structural insight into dimeric interaction of the SARAH domains from Mst1 and RASSF family proteins in the apoptosis pathway. Proc. Natl. Acad. Sci. U.S.A. 104, 9236-9241
19. Harjes, E., Harjes, S., Wohlgemuth, S., Muller, K. H., Krieger, E., Herrmann, C. and Bayer, P. (2006) GTP-Ras disrupts the intramolecular complex of C1 and RA domains of Nore1. Structure 14, 881-888
20. Grigoryan, G. and Keating, A. E. (2008) Structural specificity in coiled-coil interactions. Curr. Opin. Struct. Biol. 18, 477-483
21. Weitzel, J. N., Kasperczyk, A., Mohan, C. and Krontiris, T. G. (1992) The HRAS1 gene cluster: two upstream regions recognizing transcripts and a third encoding a gene with a leucine zipper domain. Genomics 14, 309-319
22. Falvella, F. S., Manenti, G., Spinola, M., Pignatiello, C., Conti, B., Pastorino, U. and Dragani, T. A. (2006) Identification of RASSF8 as a candidate lung tumor suppressor gene. Oncogene 25, 3934-3938
23. Polesello, C., Huelsmann, S., Brown, N. H. and Tapon, N. (2006) The Drosophila RASSF homolog antagonizes the hippo pathway. Curr. Biol. 16, 2459-2465
24. Khokhlatchev, A., Rabizadeh, S., Xavier, R., Nedwidek, M., Chen, T., Zhang, X. F., Seed, B. and Avruch, J. (2002) Identification of a novel Ras-regulated proapoptotic pathway. Curr. Biol. 12, 253-265
25. Dammann, R., Li, C., Yoon, J. H., Chin, P. L., Bates, S. and Pfeifer, G. P. (2000) Epigenetic inactivation of a RAS association domain family protein from the lung tumour suppressor locus 3p21.3. Nat. Genet. 25, 315-319
26. Lerman, M. I. and Minna, J. D. (2000) The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: identification and evaluation of the resident candidate tumor suppressor genes. The International Lung Cancer Chromosome 3p21.3 Tumor Suppressor Gene Consortium. Cancer Res. 60, 6116-6133
27. Agathanggelou, A., Honorio, S., Macartney, D. P., Martinez, A., Dallol, A., Rader, J., Fullwood, P., Chauhan, A., Walker, R., Shaw, J. A. et al. (2001) Methylation associated inactivation of RASSF1A from region 3p21.3 in lung, breast and ovarian tumours. Oncogene 20, 1509-1518
28. van der Weyden, L., Tachibana, K. K., Gonzalez, M. A., Adams, D. J., Ng, B. L., Petty, R., Venkitaraman, A. R., Arends, M. J. and Bradley, A. (2005) The RASSF1A isoform of RASSF1 promotes microtubule stability and suppresses tumorigenesis. Mol. Cell. Biol. 25, 8356-8367
29. Tommasi, S., Dammann, R., Zhang, Z., Wang, Y., Liu, L., Tsark, W. M., Wilczynski, S. P., Li, J., You, M. and Pfeifer, G. P. (2005) Tumor susceptibility of Rassf1a knockout mice. Cancer Res. 65, 92-98
30. Praskova, M., Khoklatchev, A., Ortiz-Vega, S. and Avruch, J. (2004) Regulation of the MST1 kinase by autophosphorylation, by the growth inhibitory proteins, RASSF1 and NORE1, and by Ras. Biochem. J. 381, 453-462
31. Cooper, W. N., Hesson, L. B., Matallanas, D., Dallol, A., von Kriegsheim, A., Ward, R., Kolch, W. and Latif, F. (2009) RASSF2 associates with and stabilizes the proapoptotic kinase MST2. Oncogene 28, 2988-2998
32. Harvey, K. and Tapon, N. (2007) The Salvador-Warts-Hippo pathway: an emerging tumour-suppressor network. Nat. Rev. Cancer 7, 182-191
33. Saucedo, L. J. and Edgar, B. A. (2007) Filling out the Hippo pathway. Nat. Rev. Mol. Cell. Biol. 8, 613-621
34. Matallanas, D., Romano, D., Yee, K., Meissl, K., Kucerova, L., Piazzolla, D., Baccarini, M., Vass, J. K., Kolch, W. and O'Neill, E. (2007) RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein. Mol. Cell. 27, 962-975
35. Vichalkovski, A., Gresko, E., Cornils, H., Hergovich, A., Schmitz, D. and Hemmings, B. A. (2008) NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. Curr. Biol. 18, 1889-1895
36. Baksh, S., Tommasi, S., Fenton, S., Yu, V. C., Martins, L. M., Pfeifer, G. P., Latif, F., Downward, J. and Neel, B. G. (2005) The tumor suppressor RASSF1A and MAP-1 link death receptor signaling to Bax conformational change and cell death. Mol. Cell. 18, 637-650
37. Vos, M. D., Dallol, A., Eckfeld, K., Allen, N. P., Donninger, H., Hesson, L. B., Calvisi, D., Latif, F. and Clark, G. J. (2006) The RASSF1A tumor suppressor activates Bax via MOAP-1. J. Biol. Chem. 281, 4557-4563
38. Allen, N. P., Donninger, H., Vos, M. D., Eckfeld, K., Hesson, L., Gordon, L., Birrer, M. J., Latif, F. and Clark, G. J. (2007) RASSF6 is a novel member of the RASSF family of tumor suppressors. Oncogene 26, 6203-6211
39. Foley, C. J., Freedman, H., Choo, S. L., Onyskiw, C., Fu, N. Y., Yu, V. C., Tuszynski, J., Pratt, J. C. and Baksh, S. (2008) Dynamics of RASSF1A/ MOAP-1 association with death receptors. Mol. Cell. Biol. 28, 4520-4535
40. Shivakumar, L., Minna, J., Sakamaki, T., Pestell, R. and White, M. A. (2002) The RASSF1A tumor suppressor blocks cell cycle progression and inhibits cyclin D1 accumulation. Mol. Cell. Biol. 22, 4309-4318
41. Liu, L., Tommasi, S., Lee, D. H., Dammann, R. and Pfeifer, G. P. (2003) Control of microtubule stability by the RASSF1A tumor suppressor. Oncogene 22, 8125-8136
42. Song, M. S., Song, S. J., Ayad, N. G., Chang, J. S., Lee, J. H., Hong, H. K., Lee, H., Choi, N., Kim, J., Kim, H., Kim, J. W., Choi, E. J., Kirschner, M. W. and Lim, D. S. (2004) The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex. Nat. Cell Biol. 6, 129-137
43. Rong, R., Jin, W., Zhang, J., Sheikh, M. S. and Huang, Y. (2004) Tumor suppressor RASSF1A is a microtubule-binding protein that stabilizes microtubules and induces G2/M arrest. Oncogene 23, 8216-8230
44. Whang, Y. M., Kim, Y. H., Kim, J. S. and Yoo, Y. D. (2005) RASSF1A suppresses the c-Jun-NH2-kinase pathway and inhibits cell cycle progression. Cancer Res. 65, 3682-3690
45. Deng, Z. H., Wen, J. F., Li, J. H., Xiao, D. S. and Zhou, J. H. (2008) Activator protein-1 involved in growth inhibition by RASSF1A gene in the human gastric carcinoma cell line SGC7901. World J. Gastroenterol. 14, 1437-1443
46. Thaler, S., Hahnel, P. S., Schad, A., Dammann, R. and Schuler, M. (2009) RASSF1A mediates p21Cip1/Waf1-dependent cell cycle arrest and senescence through modulation of the Raf-MEK-ERK pathway and inhibition of Akt. Cancer Res. 69, 1748-1757
47. Song, M. S., Song, S. J., Kim, S. Y., Oh, H. J. and Lim, D. S. (2008) The tumour suppressor RASSF1A promotes MDM2 self-ubiquitination by disrupting the MDM2-DAXX-HAUSP complex. EMBO J. 27, 1863-1874
48. Ahmed-Choudhury, J., Agathanggelou, A., Fenton, S. L., Ricketts, C., Clark, G. J., Maher, E. R. and Latif, F. (2005) Transcriptional regulation of cyclin A2 by RASSF1A through the enhanced binding of p120E4F to the cyclin A2 promoter. Cancer Res. 65, 2690-2697
49. Fenton, S. L., Dallol, A., Agathanggelou, A., Hesson, L., Ahmed-Choudhury, J., Baksh, S., Sardet, C., Dammann, R., Minna, J. D., Downward, J. et al. (2004) Identification of the E1A-regulated transcription factor p120 E4F as an interacting partner of the RASSF1A candidate tumor suppressor gene. Cancer Res. 64, 102-107
50. Dallol, A., Agathanggelou, A., Fenton, S. L., Ahmed-Choudhury, J., Hesson, L., Vos, M. D., Clark, G. J., Downward, J., Maher, E. R. and Latif, F. (2004) RASSF1A interacts with microtubule-associated proteins and modulates microtubule dynamics. Cancer Res. 64, 4112-4116
51. Vos, M. D., Martinez, A., Elam, C., Dallol, A., Taylor, B. J., Latif, F. and Clark, G. J. (2004) A role for the RASSF1A tumor suppressor in the regulation of tubulin polymerization and genomic stability. Cancer Res. 64, 4244-4250
52. Song, M. S., Chang, J. S., Song, S. J., Yang, T. H., Lee, H. and Lim, D. S. (2005) The centrosomal protein RAS association domain family protein 1A (RASSF1A)-binding protein 1 regulates mitotic progression by recruiting RASSF1A to spindle poles. J. Biol. Chem. 280, 3920-3927
53. Guo, C., Tommasi, S., Liu, L., Yee, J. K., Dammann, R. and Pfeifer, G. P. (2007) RASSF1A is part of a complex similar to the Drosophila Hippo/Salvador/Lats tumor-suppressor network. Curr. Biol. 17, 700-705
54. Song, M. S. and Lim, D. S. (2004) Control of APC-Cdc20 by the tumor suppressor RASSF1A. Cell Cycle 3, 574-576
55. Liu, L., Baier, K., Dammann, R. and Pfeifer, G. P. (2007) The tumor suppressor RASSF1A does not interact with Cdc20, an activator of the anaphase-promoting complex. Cell Cycle 6, 1663-1665
56. Rong, R., Jiang, L. Y., Sheikh, M. S. and Huang, Y. (2007) Mitotic kinase Aurora-A phosphorylates RASSF1A and modulates RASSF1A-mediated microtubule interaction and M-phase cell cycle regulation. Oncogene 26, 7700-7708
57. Liu, L., Guo, C., Dammann, R., Tommasi, S. and Pfeifer, G. P. (2008) RASSF1A interacts with and activates the mitotic kinase Aurora-A. Oncogene 27, 6175-6186
58. Dallol, A., Hesson, L. B., Matallanas, D., Cooper, W. N., O'Neill, E., Maher, E. R., Kolch, W. and Latif, F. (2009) RAN GTPase is a RASSF1A effector involved in controlling microtubule organization. Curr. Biol. 19, 1227-1232
59. Dallol, A., Agathanggelou, A., Tommasi, S., Pfeifer, G. P., Maher, E. R. and Latif, F. (2005) Involvement of the RASSF1A tumor suppressor gene in controlling cell migration. Cancer Res. 65, 7653-7659
60. Moshnikova, A., Frye, J., Shay, J. W., Minna, J. D. and Khokhlatchev, A. V. (2006) The growth and tumor suppressor NORE1A is a cytoskeletal protein that suppresses growth by inhibition of the ERK pathway. J. Biol. Chem. 281, 8143-8152
61. Calvisi, D. F., Donninger, H., Vos, M. D., Birrer, M. J., Gordon, L., Leaner, V. and Clark, G. J. (2009) NORE1A tumor suppressor candidate modulates p21CIP1 via p53. Cancer Res. 69, 4629-4637
62. Vavvas, D., Li, X., Avruch, J. and Zhang, X. F. (1998) Identification of Nore1 as a potential Ras effector. J. Biol. Chem. 273, 5439-5442
63. Stieglitz, B., Bee, C., Schwarz, D., Yildiz, O., Moshnikova, A., Khokhlatchev, A. and Herrmann, C. (2008) Novel type of Ras effector interaction established between tumour suppressor NORE1A and Ras switch II. EMBO J. 27, 1995-2005
64. Kinashi, T. (2007) Integrin regulation of lymphocyte trafficking: lessons from structural and signaling studies. Adv. Immunol. 93, 185-227
65. Vos, M. D. and Clark, G. J. (2005) RASSF FAMILY Proteins and Ras transformation. Methods Enzymol. 407, 311-322
66. Ortiz-Vega, S., Khokhlatchev, A., Nedwidek, M., Zhang, X. F., Dammann, R., Pfeifer, G. P. and Avruch, J. (2002) The putative tumor suppressor RASSF1A homodimerizes and heterodimerizes with the Ras-GTP binding protein Nore1. Oncogene 21, 1381-1390
67. Calvisi, D. F., Ladu, S., Gorden, A., Farina, M., Conner, E. A., Lee, J. S., Factor, V. M. and Thorgeirsson, S. S. (2006) Ubiquitous activation of Ras and Jak/Stat pathways in human HCC. Gastroenterology 130 1117-1128
68. Krontiris, T. G., Devlin, B., Karp, D. D., Robert, N. J. and Risch, N. (1993) An association between the risk of cancer and mutations in the HRAS1 minisatellite locus. N. Engl. J. Med. 329, 517-523
69. Krontiris, T. G., DiMartino, N. A., Colb, M. and Parkinson, D. R. (1985) Unique allelic restriction fragments of the human Ha-ras locus in leukocyte and tumour DNAs of cancer patients. Nature 313, 369-374
70. Weitzel, J. N., Ding, S., Larson, G. P., Nelson, R. A., Goodman, A., Grendys, E. C., Ball, H. G. and Krontiris, T. G. (2000) The HRAS1 minisatellite locus and risk of ovarian cancer. Cancer Res. 60, 259-261
71. Firgaira, F. A., Seshadri, R., McEvoy, C. R., Dite, G. S., Giles, G. G., McCredie, M. R., Southey, M. C., Venter, D. J. and Hopper, J. L. (1999) HRAS1 rare minisatellite alleles and breast cancer in Australian women under age forty years. J. Natl. Cancer Inst. 91, 2107-2111
72. Tamimi, R. M., Hankinson, S. E., Ding, S., Gagalang, V., Larson, G. P., Spiegelman, D., Colditz, G. A., Krontiris, T. G. and Hunter, D. J. (2003) The HRAS1 variable number of tandem repeats and risk of breast cancer. Cancer Epidemiol. Biomarkers Prev. 12, 1528-1530
73. Brandt, R., Grutzmann, R., Bauer, A., Jesnowski, R., Ringel, J., Lohr, M., Pilarsky, C. and Hoheisel, J. D. (2004) DNA microarray analysis of pancreatic malignancies. Pancreatology 4, 587-597
74. Friess, H., Ding, J., Kleeff, J., Fenkell, L., Rosinski, J. A., Guweidhi, A., Reidhaar-Olson, J. F., Korc, M., Hammer, J. and Buchler, M. W. (2003) Microarray-based identification of differentially expressed growth- and metastasis-associated genes in pancreatic cancer. Cell. Mol. Life Sci. 60, 1180-1199
75. Logsdon, C. D., Simeone, D. M., Binkley, C., Arumugam, T., Greenson, J. K., Giordano, T. J., Misek, D. E., Kuick, R. and Hanash, S. (2003) Molecular profiling of pancreatic adenocarcinoma and chronic pancreatitis identifies multiple genes differentially regulated in pancreatic cancer. Cancer Res. 63, 2649-2657
76. Lowe, A. W., Olsen, M., Hao, Y., Lee, S. P., Taek Lee, K., Chen, X., van de Rijn, M. and Brown, P. O. (2007) Gene expression patterns in pancreatic tumors, cells and tissues. PLoS ONE 2, e323
77. Mutter, G. L., Baak, J. P., Fitzgerald, J. T., Gray, R., Neuberg, D., Kust, G. A., Gentleman, R., Gullans, S. R., Wei, L. J. and Wilcox, M. (2001) Global expression changes of constitutive and hormonally regulated genes during endometrial neoplastic transformation. Gynecol. Oncol. 83, 177-185
78. Tan, D. S., Lambros, M. B., Rayter, S., Natrajan, R., Vatcheva, R., Gao, Q., Marchio, C., Geyer, F. C., Savage, K., Parry, S. et al. (2009) PPM1D is a potential therapeutic target in ovarian clear cell carcinomas. Clin. Cancer Res. 15, 2269-2280
79. Kenneth, N. S. and Rocha, S. (2008) Regulation of gene expression by hypoxia. Biochem. J. 414, 19-29
80. Camps, C., Buffa, F. M., Colella, S., Moore, J., Sotiriou, C., Sheldon, H., Harris, A. L., Gleadle, J. M. and Ragoussis, J. (2008) hsa-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin. Cancer Res. 14, 1340-1348
81. Liang, G. P., Su, Y. Y., Chen, J., Yang, Z. C., Liu, Y. S. and Luo, X. D. (2009) Analysis of the early adaptive response of endothelial cells to hypoxia via a long serial analysis of gene expression. Biochem. Biophys. Res. Commun. 384, 415-419
82. Welcsh, P. L., Lee, M. K., Gonzalez-Hernandez, R. M., Black, D. J., Mahadevappa, M., Swisher, E. M., Warrington, J. A. and King, M. C. (2002) BRCA1 transcriptionally regulates genes involved in breast tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 99, 7560-7565
83. Hitomi, J., Christofferson, D. E., Ng, A., Yao, J., Degterev, A., Xavier, R. J. and Yuan, J. (2008) Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135, 1311-1323
84. Chalmers, A. D., Lachani, K., Shin, Y., Sherwood, V., Cho, K. W. and Papalopulu, N. (2006) Grainyhead-like 3, a transcription factor identified in a microarray screen, promotes the specification of the superficial layer of the embryonic epidermis. Mech. Dev. 123, 702-718
85. Goshima, G., Wollman, R., Goodwin, S. S., Zhang, N., Scholey, J. M., Vale, R. D. and Stuurman, N. (2007) Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417-421
86. Morris, J. A., Kandpal, G., Ma, L. and Austin, C. P. (2003) DISC1 (disrupted-in-schizophrenia 1) is a centrosome-associated protein that interacts with MAP1A, MIPT3, ATF4/5 and NUDEL: regulation and loss of interaction with mutation. Hum. Mol. Genet. 12, 1591-1608
87. Tsang, H. T., Connell, J. W., Brown, S. E., Thompson, A., Reid, E. and Sanderson, C. M. (2006) A systematic analysis of human CHMP protein interactions: additional MIT domain-containing proteins bind to multiple components of the human ESCRT III complex. Genomics 88, 333-346
88. Debeer, P., Schoenmakers, E. F., Thoelen, R., Holvoet, M., Kuittinen, T., Fabry, G., Fryns, J. P., Goodman, F. R. and Van de Ven, W. J. (2000) Physical map of a 1.5 mb region on 12p11.2 harbouring a synpolydactyly associated chromosomal breakpoint. Eur. J. Hum. Genet. 8, 561-570
89. Debeer, P., Schoenmakers, E. F., Twal, W. O., Argraves, W. S., De Smet, L., Fryns, J. P. and Van De Ven, W. J. (2002) The fibulin-1 gene (FBLN1) is disrupted in a t(12;22) associated with a complex type of synpolydactyly. J. Med. Genet. 39, 98-104
90. Gariboldi, M., Manenti, G., Canzian, F., Falvella, F. S., Radice, M. T., Pierotti, M. A., Della Porta, G., Binelli, G. and Dragani, T. A. (1993) A major susceptibility locus to murine lung carcinogenesis maps on chromosome 6. Nat. Genet. 3, 132-136
91. To, M. D., Perez-Losada, J., Mao, J. H., Hsu, J., Jacks, T. and Balmain, A. (2006) A functional switch from lung cancer resistance to susceptibility at the Pas1 locus in Kras2LA2 mice. Nat. Genet. 38, 926-930
92. Manenti, G., De Gregorio, L., Pilotti, S., Falvella, F. S., Incarbone, M., Ravagnani, F., Pierotti, M. A. and Dragani, T. A. (1997) Association of chromosome 12p genetic polymorphisms with lung adenocarcinoma risk and prognosis. Carcinogenesis 18, 1917-1920
93. Yanagitani, N., Kohno, T., Sunaga, N., Kunitoh, H., Tamura, T., Tsuchiya, S., Saito, R. and Yokota, J. (2002) Localization of a human lung adenocarcinoma susceptibility locus, possibly syntenic to the mouse Pas1 locus, in the vicinity of the D12S1034 locus on chromosome 12p11.2-p12.1. Carcinogenesis 23, 1177-1183
94. Falvella, F. S., Spinola, M., Manenti, G., Conti, B., Pastorino, U., Skaug, V., Haugen, A. and Dragani, T. A. (2007) Common polymorphisms in D12S1034 flanking genes RASSF8 and BHLHB3 are not associated with lung adenocarcinoma risk. Lung Cancer 56, 1-7
95. Korkola, J. E., Houldsworth, J., Chadalavada, R. S., Olshen, A. B., Dobrzynski, D., Reuter, V. E., Bosl, G. J. and Chaganti, R. S. (2006) Down-regulation of stem cell genes, including those in a 200-kb gene cluster at 12p13.31, is associated with in vivo differentiation of human male germ cell tumors. Cancer Res. 66, 820-827
96. Weiser, K. C., Liu, B., Hansen, G. M., Skapura, D., Hentges, K. E., Yarlagadda, S., Morse Iii, H. C. and Justice, M. J. (2007) Retroviral insertions in the VISION database identify molecular pathways in mouse lymphoid leukemia and lymphoma. Mamm. Genome 18, 709-722
97. Eckfeldt, C. E., Mendenhall, E. M., Flynn, C. M., Wang, T. F., Pickart, M. A., Grindle, S. M., Ekker, S. C. and Verfaillie, C. M. (2005) Functional analysis of human hematopoietic stem cell gene expression using zebrafish. PLoS Biol. 3, e254
98. Jin, J., Smith, F. D., Stark, C., Wells, C. D., Fawcett, J. P., Kulkarni, S., Metalnikov, P., O'Donnell, P., Taylor, P., Taylor, L. et al. (2004) Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 14, 1436-1450
99. Rual, J. F., Venkatesan, K., Hao, T., Hirozane-Kishikawa, T., Dricot, A., Li, N., Berriz, G. F., Gibbons, F. D., Dreze, M., Ayivi-Guedehoussou, N. et al. (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437, 1173-1178
100. Alam, M. R., Caldwell, B. D., Johnson, R. C., Darlington, D. N., Mains, R. E. and Eipper, B. A. (1996) Novel proteins that interact with the COOH-terminal cytosolic routing determinants of an integral membrane peptide-processing enzyme. J. Biol. Chem. 271, 28636-28640
101. Prigge, S. T., Mains, R. E., Eipper, B. A. and Amzel, L. M. (2000) New insights into copper monooxygenases and peptide amidation: structure, mechanism and function. Cell. Mol. Life Sci. 57, 1236-1259
102. Chen, L., Johnson, R. C. and Milgram, S. L. (1998) P-CIP1, a novel protein that interacts with the cytosolic domain of peptidylglycine alpha-amidating monooxygenase, is associated with endosomes. J. Biol. Chem. 273, 33524-33532
103. Rajagopal, C., Stone, K. L., Francone, V. P., Mains, R. E. and Eipper, B. A. (2009) Secretory granule to the nucleus: role of a multiply phosphorylated intrinsically unstructured domain, J. Biol. Chem. 18, 25723-25734
104. Hesson, L. B., Dunwell, T. L., Cooper, W. N., Catchpoole, D., Brini, A. T., Chiaramonte, R., Griffiths, M., Chalmers, A. D., Maher, E. R. and Latif, F. (2009) The novel RASSF6 and RASSF10 candidate tumour suppressor genes are frequently epigenetically inactivated in childhood leukaemias. Mol. Cancer 8, 42
105. Reeves, N. and Posakony, J. W. (2005) Genetic programs activated by proneural proteins in the developing Drosophila PNS. Dev. Cell. 8, 413-425
106. Nybakken, K., Vokes, S. A., Lin, T. Y., McMahon, A. P. and Perrimon, N. (2005) A genome-wide RNA interference screen in Drosophila melanogaster cells for new components of the Hh signaling pathway. Nat. Genet. 37, 1323-1332