Hypermethylated in cancer 1 (HIC1) recruits polycomb repressive complex 2 (PRC2) to a subset of its target genes through interaction with human polycomb-like (hPCL) proteins

Journal of Biological Chemistry

Volumn 287, Issue 13, 2012, Pages 10509-10524

  Boulay, Gaylor ^a   Dubuissez, Marion ^a   Van Rechem, Capucine ^a,d   Forget, Antoine ^b   Helin, Kristian ^c   Ayrault, Olivier ^b   Leprince, Dominique ^a  

^a UNIV LILLE   (France)

^b INSERM U1005   (France)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURVIVAL; COREPRESSORS; DNA BINDING; GROWTH CONTROL; HUMAN CANCER; IN-VIVO; N-TERMINALS; PARALOGS; PARTIAL DISPLACEMENT; POLYCOMB; STABLE COMPLEXES; STRESS RESPONSE; TARGET GENES; TRANSCRIPTIONAL REPRESSORS; TUMOR SUPPRESSOR GENES; YEAST TWO HYBRID; ZINC FINGER;

DIAGNOSIS; GENES; MAMMALS; TRANSCRIPTION FACTORS;

DISEASES;

CORE PROTEIN; DNA HYBRID; DROSOPHILA PROTEIN; EMBRYONIC ECTODERM DEVELOPMENT PROTEIN; PHD FINGER PROTEIN 1; POLYCOMB GROUP PROTEIN; POLYCOMB LIKE 3L PROTEIN; POLYCOMB LIKE 3S PROTEIN; PROTEIN P53; PROTEIN SUZ12; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN C2H2;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; ATOH1 GENE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA BINDING; DNA PROTEIN COMPLEX; DNA SEQUENCE; EMBRYO; EPIGENETICS; FEMALE; GENE; GENE DELETION; GENE INTERACTION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; GENETIC ASSOCIATION; GENETIC SCREENING; GROWTH REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYBRID GENE; HYPERMETHYLATED IN CANCER 1 GENE; IN VIVO STUDY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; POLYCOMB REPRESSIVE COMPLEX 2 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARRIER PROTEINS; CEREBELLUM; DNA-BINDING PROTEINS; FEMALE; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; NUCLEAR PROTEINS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; ZINC FINGERS;

MAMMALIA; MUS;

EID: 84858969865     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.320234     Document Type: Article

References (73)

1. Sauvageau, M., and Sauvageau, G. (2010) Polycomb group proteins. Multifaceted regulators of somatic stem cells and cancer. Cell Stem Cell 7,299-313
2. Morey, L., and Helin, K. (2010) Polycomb group protein-mediated repression of transcription. Trends Biochem. Sci. 35, 323-332
3. Margueron, R., and Reinberg, D. (2011) The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349
4. Pasini, D., Cloos, P. A., Walfridsson, J., Olsson, L., Bukowski, J. P., Johansen, J. V., Bak, M., Tommerup, N., Rappsilber, J., and Helin, K. (2010) JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464, 306-310
5. Li, G., Margueron, R., Ku, M., Chambon, P., Bernstein, B. E., and Reinberg, D. (2010) Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 24, 368-380
6. Tie, F., Prasad-Sinha, J., Birve, A., Rasmuson-Lestander, A., and Harte, P. J. (2003) A 1-megadalton ESC/E(Z) complex from Drosophila that contains Polycomb-like and RPD3. Mol. Cell. Biol. 23, 3352-3362 (Pubitemid 36459246)
7. Coulson, M., Robert, S., Eyre, H. J., and Saint, R. (1998) The identification and localization of a human gene with sequence similarity to Polycomblike of Drosophila melanogaster. Genomics 48, 381-383 (Pubitemid 28180741)
8. Walker, E., Chang, W. Y., Hunkapiller, J., Cagney, G., Garcha, K., Torchia, J., Krogan, N. J., Reiter, J. F., and Stanford, W. L. (2010) Polycomb-like 2 associates with PRC2 and regulates transcriptional networks during mouse embryonic stem cell self-renewal and differentiation. Cell Stem Cell 6, 153-166
9. Wang, S., Robertson, G. P., and Zhu, J. (2004) A novel human homologue of Drosophila Polycomb-like gene is up-regulated in multiple cancers. Gene 343, 69-78 (Pubitemid 39551030)
10. Boulay, G., Rosnoblet, C., Guérardel, C., Angrand, P. O., and Leprince, D. (2011) Functional characterization of human Polycomb-like 3 isoforms identifies them as components of distinct EZH2 protein complexes. Biochem. J. 434, 333-342
11. Nekrasov, M., Klymenko, T., Fraterman, S., Papp, B., Oktaba, K., Köcher, T., Cohen, A., Stunnenberg, H. G., Wilm, M., and Müller, J. (2007) Pcl-PRC2 is needed to generate high levels of H3K27 trimethylation at Polycomb target genes. EMBO J. 26, 4078-4088 (Pubitemid 47462096)
12. Sarma, K., Margueron, R., Ivanov, A., Pirrotta, V., and Reinberg, D. (2008) Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol. Cell. Biol. 28, 2718-2731 (Pubitemid 351542370)
13. Cao, R., Wang, H., He, J., Erdjument-Bromage, H., Tempst, P., and Zhang, Y. (2008) Role of hPHF1 in H3K27 methylation and Hox gene silencing. Mol. Cell. Biol. 28, 1862-1872
14. Savla, U., Benes, J., Zhang, J., and Jones, R. S. (2008) Recruitment of Drosophila Polycomb group proteins by Polycomb-like, a component of a novel protein complex in larvae. Development 135, 813-817 (Pubitemid 351524135)
15. Casanova, M., Preissner, T., Cerase, A., Poot, R., Yamada, D., Li, X., Appanah, R., Bezstarosti, K., Demmers, J., Koseki, H., and Brockdorff, N. (2011) Polycomb-like 2 facilitates the recruitment of PRC2 Polycomb group complexes to the inactive X chromosome and to target loci in embryonic stem cells. Development 138, 1471-1482
16. Wales, M. M., Biel, M. A., el Deiry, W., Nelkin, B. D., Issa, J. P., Cavenee, W. K., Kuerbitz, S. J., and Baylin, S. B. (1995) p53 activates expression of HIC-1, a new candidate tumor suppressor gene on 17p13.3. Nat. Med. 1, 570-577
17. Fleuriel, C., Touka, M., Boulay, G., Guérardel, C., Rood, B. R., and Leprince, D. (2009) HIC1 (hypermethylated in cancer 1) epigenetic silencing in tumors. Int. J. Biochem. Cell Biol. 41, 26-33
18. Chen, W. Y., Zeng, X., Carter, M. G., Morrell, C. N., Chiu Yen, R. W., Esteller, M., Watkins, D. N., Herman, J. G., Mankowski, J. L., and Baylin, S. B. (2003) Heterozygous disruption of Hic1 predisposes mice to a gender- dependent spectrum of malignant tumors. Nat. Genet. 33, 197-202 (Pubitemid 36177074)
19. Chen, W., Cooper, T. K., Zahnow, C. A., Overholtzer, M., Zhao, Z., Ladanyi, M., Karp, J. E., Gokgoz, N., Wunder, J. S., Andrulis, I. L., Levine, A. J., Mankowski, J. L., and Baylin, S. B. (2004) Epigenetic and genetic loss of Hic1 function accentuates the role of p53 in tumorigenesis. Cancer Cell 6, 387-398 (Pubitemid 39361439)
20. Chen, W. Y., Wang, D. H., Yen, R. C., Luo, J., Gu, W., and Baylin, S. B. (2005) Tumor suppressor HIC1 directly regulates SIRT1 to modulate p53-dependent DNA-damage responses. Cell 123, 437-448 (Pubitemid 41546674)
21. Jenal, M., Trinh, E., Britschgi, C., Britschgi, A., Roh, V., Vorburger, S. A., Tobler, A., Leprince, D., Fey, M. F., Helin, K., and Tschan, M. P. (2009) The tumor suppressor gene hypermethylated in cancer 1 is transcriptionally regulated by E2F1. Mol. Cancer Res. 7, 916-922
22. Wang, C., Chen, L., Hou, X., Li, Z., Kabra, N., Ma, Y., Nemoto, S., Finkel, T., Gu, W., Cress, W. D., and Chen, J. (2006) Interactions between E2F1 and SirT1 regulate apoptotic response to DNA damage. Nat. Cell Biol. 8, 1025-1031 (Pubitemid 44314735)
23. Dehennaut, V., and Leprince, D. (2009) Implication of HIC1 (hypermethylated in cancer 1) in the DNA damage response. Bull. Cancer 96, E66-72
24. Carter, M. G., Johns, M. A., Zeng, X., Zhou, L., Zink, M. C., Mankowski, J. L., Donovan, D. M., and Baylin, S. B. (2000) Mice deficient in the candidate tumor suppressor gene Hic1 exhibit developmental defects of structures affected in the Miller-Dieker syndrome. Hum. Mol. Genet. 9, 413-419 (Pubitemid 30098735)
25. Pospichalova, V., Tureckova, J., Fafilek, B., Vojtechova, M., Krausova, M., Lukas, J., Sloncova, E., Takacova, S., Divoky, V., Leprince, D., Plachy, J., and Korinek, V. (2011) Generation of two modified mouse alleles of the Hic1 tumor suppressor gene. Genesis 49, 142-151
26. Pinte, S., Stankovic-Valentin, N., Deltour, S., Rood, B. R., Guérardel, C., and Leprince, D. (2004) The tumor suppressor gene HIC1 (hypermethylated in cancer 1) is a sequence-specific transcriptional repressor. Definition of its consensus binding sequence and analysis of its DNA binding and repressive properties. J. Biol. Chem. 279, 38313-38324 (Pubitemid 39295979)
27. Van Rechem, C., Boulay, G., Pinte, S., Stankovic-Valentin, N., Guérardel, C., and Leprince, D. (2010) Differential regulation of HIC1 target genes by CtBP and NuRD, via an acetylation/SUMOylation switch, in quiescent versus proliferating cells. Mol. Cell. Biol. 30, 4045-4059
28. Mohammad, H. P., Zhang, W., Prevas, H. S., Leadem, B. R., Zhang, M., Herman, J. G., Hooker, C. M., Watkins, D. N., Karim, B., Huso, D. L., and Baylin, S. B. (2011) Loss of a single Hic1 allele accelerates polyp formation in Apc(Δ716) mice. Oncogene 30, 2659-2669
29. Foveau, B., Boulay, G., Pinte, S., Van Rechem, C., Rood, B. R., and Leprince, D. (2012) The receptor tyrosine kinase EphA2 is a direct target gene of Hypermethylated in Cancer 1 (HIC1). J. Biol. Chem. 287, 5366-5378
30. Boulay, G., Malaquin, N., Loison, I., Foveau, B., Van Rechem, C., Rood, B. R., Pourtier, A., and Leprince, D. (2012) Loss of Hypermethylated in Cancer 1 (HIC1) in breast cancer cells contributes to stress induced migration and invasion through β-2 adrenergic receptor (ADRB2) misregulation. J. Biol. Chem. 287, 5379-5389
31. Deltour, S., Pinte, S., Guerardel, C., Wasylyk, B., and Leprince, D. (2002) The human candidate tumor suppressor gene HIC1 recruits CtBP through a degenerate GLDLSKK motif. Mol. Cell. Biol. 22, 4890-4901 (Pubitemid 34620422)
32. Van Rechem, C., Boulay, G., and Leprince, D. (2009) HIC1 interacts with a specific subunit of SWI/SNF complexes, ARID1A/BAF250A. Biochem. Biophys. Res. Commun. 385, 586-590
33. Stankovic-Valentin, N., Deltour, S., Seeler, J., Pinte, S., Vergoten, G., Guérardel, C., Dejean, A., and Leprince, D. (2007) An acetylation/deacetylation-SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity. Mol. Cell. Biol. 27, 2661-2675 (Pubitemid 46581356)
34. Laible, G., Wolf, A., Dorn, R., Reuter, G., Nislow, C., Lebersorger, A., Popkin, D., Pillus, L., and Jenuwein, T. (1997) Mammalian homologues of the Polycomb group gene enhancer of zeste mediate gene silencing in Drosophila heterochromatin and at S. cerevisiae telomeres. EMBO J. 16, 3219-3232 (Pubitemid 27234960)
35. Pasini, D., Bracken, A. P., Jensen, M. R., Lazzerini Denchi, E., and Helin, K. (2004) Suz12 is essential for mouse development and EZH2 histone methyltransferase activity. EMBO J. 23, 4061-4071 (Pubitemid 39472427)
36. Bracken, A. P., Pasini, D., Capra, M., Prosperini, E., Colli, E., and Helin, K. (2003) EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J. 22, 5323-5335 (Pubitemid 37279943)
37. Van Rechem, C., Rood, B. R., Touka, M., Pinte, S., Jenal, M., Guérardel, C., Ramsey, K., Monté, D., Bégue, A., Tschan, M. P., Stephan, D. A., and Leprince, D. (2009) Scavenger chemokine (CXC motif) receptor 7 (CXCR7) is a direct target gene of HIC1 (hypermethylated in cancer 1). J. Biol. Chem. 284, 20927-20935
38. Dahl, J. A., and Collas, P. (2007) Q2 ChIP, a quick and quantitative chromatin immunoprecipitation assay, unravels epigenetic dynamics of developmentally regulated genes in human carcinoma cells. Stem Cells 25, 1037-1046 (Pubitemid 46572602)
39. Srinivasan, L., and Atchison, M. L. (2004) YY1 DNA binding and PcG recruitment requires CtBP. Genes Dev. 18, 2596-2601 (Pubitemid 39453098)
40. Morey, L., Brenner, C., Fazi, F., Villa, R., Gutierrez, A., Buschbeck, M., Nervi, C., Minucci, S., Fuks, F., and Di Croce, L. (2008) MBD3, a component of the NuRD complex, facilitates chromatin alteration and deposition of epigenetic marks. Mol. Cell. Biol. 28, 5912-5923
41. Reynolds, N., Salmon-Divon, M., Dvinge, H., Hynes-Allen, A., Balasooriya, G., Leaford, D., Behrens, A., Bertone, P., and Hendrich, B. (2011) NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb repressive complex 2 to direct gene repression. EMBO J. 31, 593-605
42. Stankovic-Valentin, N., Verger, A., Deltour-Balerdi, S., Quinlan, K. G., Crossley, M., and Leprince, D. (2006) A L225A substitution in the human tumor suppressor HIC1 abolishes its interaction with the corepressor CtBP. FEBS J. 273, 2879-2890
43. Deltour, S., Guerardel, C., and Leprince, D. (1999) Recruitment of SMRT/N-CoR-mSin3A-HDAC-repressing complexes is not a general mechanism for BTB/POZ transcriptional repressors, The case of HIC-1 and γFBP-B. Proc. Natl. Acad. Sci. U.S.A. 96, 14831-14836 (Pubitemid 30019725)
44. Long, J., Wang, G., Matsuura, I., He, D., and Liu, F. (2004) Activation of Smad transcriptional activity by protein inhibitor of activated STAT3 (PIAS3). Proc. Natl. Acad. Sci. U.S.A. 101, 99-104 (Pubitemid 38084210)
45. Bracken, A. P., Dietrich, N., Pasini, D., Hansen, K. H., and Helin, K. (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20, 1123-1136
46. Zhang, W., Zeng, X., Briggs, K. J., Beaty, R., Simons, B., Chiu Yen, R. W., Tyler, M. A., Tsai, H. C., Ye, Y., Gesell, G. S., Herman, J. G., Baylin, S. B., and Watkins, D. N. (2010) A potential tumor suppressor role for Hic1 in breast cancer through transcriptional repression of ephrin-A1. Oncogene 29, 2467-2476
47. Briggs, K. J., Corcoran-Schwartz, I. M., Zhang, W., Harcke, T., Devereux, W. L., Baylin, S. B., Eberhart, C. G., and Watkins, D. N. (2008) Cooperation between the Hic1 and Ptch1 tumor suppressors in medulloblastoma. Genes Dev. 22, 770-785 (Pubitemid 351439108)
48. Boyer, L. A., Plath, K., Zeitlinger, J., Brambrink, T., Medeiros, L. A., Lee, T. I., Levine, S. S., Wernig, M., Tajonar, A., Ray, M. K., Bell, G. W., Otte, A. P., Vidal, M., Gifford, D. K., Young, R. A., and Jaenisch, R. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441, 349-353 (Pubitemid 44050199)
49. Pasini, D., Malatesta, M., Jung, H. R., Walfridsson, J., Willer, A., Olsson, L., Skotte, J., Wutz, A., Porse, B., Jensen, O. N., and Helin, K. (2010) Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res. 38, 4958-4969
50. Briggs, K. J., Eberhart, C. G., and Watkins, D. N. (2008) Just say no to ATOH. How HIC1 methylation might predispose medulloblastoma to lineage addiction. Cancer Res. 68, 8654-8656
51. Ayrault, O., Zhao, H., Zindy, F., Qu, C., Sherr, C. J., and Roussel, M. F. (2010) Atoh1 inhibits neuronal differentiation and collaborates with Gli1 to generate medulloblastoma-initiating cells. Cancer Res. 70, 5618-5627
52. Grimmer, M. R., and Weiss, W. A. (2008) BMPs oppose Math1 in cerebellar development and in medulloblastoma. Genes Dev. 22, 693-699 (Pubitemid 351439098)
53. Albagli, O., Dhordain, P., Deweindt, C., Lecocq, G., and Leprince, D. (1995) The BTB/POZ domain. A new protein-protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ. 6, 1193-1198
54. Stogios, P. J., Downs, G. S., Jauhal, J. J., Nandra, S. K., and Privé, G. G. (2005) Sequence and structural analysis of BTB domain proteins. Genome Biol. 6, R82
55. Boukarabila, H., Saurin, A. J., Batsché, E., Mossadegh, N., van Lohuizen, M., Otte, A. P., Pradel, J., Muchardt, C., Sieweke, M., and Duprez, E. (2009) The PRC1 Polycomb group complex interacts with PLZF/RARA to mediate leukemic transformation. Genes Dev. 23, 1195-1206
56. Adams-Cioaba, M. A., and Min, J. (2009) Structure and function of histone methylation binding proteins. Biochem. Cell Biol. 87, 93-105
57. Huang, Y., Fang, J., Bedford, M. T., Zhang, Y., and Xu, R. M. (2006) Recognition of histone H3 lysine-4 methylation by the double Tudor domain of JMJD2A. Science 312, 748-751
58. Corsini, L., and Sattler, M. (2007) Tudor hooks up with DNA repair. Nat. Struct. Mol. Biol. 14, 98-99
59. Friberg, A., Oddone, A., Klymenko, T., Müller, J., and Sattler, M. (2010) Structure of an atypical Tudor domain in the Drosophila Polycomb-like protein. Protein Sci. 19, 1906-1916
60. Bienz, M. (2006) The PHD finger, a nuclear protein-interaction domain. Trends Biochem. Sci 31, 35-40
61. Mellor, J. (2006) It takes a PHD to read the histone code. Cell 126, 22-24
62. Bracken, A. P., and Helin, K. (2009) Polycomb group proteins. Navigators of lineage pathways led astray in cancer. Nat. Rev. Cancer 9, 773-784
63. Schuettengruber, B., and Cavalli, G. (2009) Recruitment of Polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136, 3531-3542
64. Sing, A., Pannell, D., Karaiskakis, A., Sturgeon, K., Djabali, M., Ellis, J., Lipshitz, H. D., and Cordes, S. P. (2009) A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell 138, 885-897
65. Woo, C. J., Kharchenko, P. V., Daheron, L., Park, P. J., and Kingston, R. E. (2010) A region of the human HOXD cluster that confers Polycombgroup responsiveness. Cell 140, 99-110
66. Villa, R., Pasini, D., Gutierrez, A., Morey, L., Occhionorelli, M., Viré, E., Nomdedeu, J. F., Jenuwein, T., Pelicci, P. G., Minucci, S., Fuks, F., Helin, K., and Di Croce, L. (2007) Role of the Polycomb repressive complex 2 in acute promyelocytic leukemia. Cancer Cell 11, 513-525 (Pubitemid 46863505)
67. Herranz, N., Pasini, D., Díaz, V. M., Francí, C., Gutierrez, A., Dave, N., Escrivà, M., Hernandez-Muñoz, I., Di Croce, L., Helin, K., García de Herreros, A., and Peiró, S. (2008) Polycomb complex 2 is required for Ecadherin repression by the Snail1 transcription factor. Mol. Cell. Biol. 28, 4772-4781
68. Hansen, K. H., Bracken, A. P., Pasini, D., Dietrich, N., Gehani, S. S., Monrad, A., Rappsilber, J., Lerdrup, M., and Helin, K. (2008) A model for transmission of the H3K27me3 epigenetic mark. Nat. Cell Biol. 10, 1291-1300
69. Pasini, D., Bracken, A. P., Hansen, J. B., Capillo, M., and Helin, K. (2007) The Polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 27, 3769-3779 (Pubitemid 46726184)
70. Rood, B. R., Zhang, H., Weitman, D. M., and Cogen, P. H. (2002) Hypermethylation of HIC-1 and 17p allelic loss in medulloblastoma. Cancer Res. 62, 3794-3797 (Pubitemid 34728863)
71. Boldajipour, B., Mahabaleshwar, H., Kardash, E., Reichman-Fried, M., Blaser, H., Minina, S., Wilson, D., Xu, Q., and Raz, E. (2008) Control of chemokine-guided cell migration by ligand sequestration. Cell 132, 463-473 (Pubitemid 351191997)
72. Sierro, F., Biben, C., Martínez-Muñoz, L., Mellado, M., Ransohoff, R. M., Li, M., Woehl, B., Leung, H., Groom, J., Batten, M., Harvey, R. P., Martínez-A, C., Mackay, C. R., and Mackay, F. (2007) Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. U.S.A. 104, 14759-14764 (Pubitemid 350003216)
73. Dodelet, V. C., and Pasquale, E. B. (2000) Eph receptors and ephrin ligands. Embryogenesis to tumorigenesis. Oncogene 19, 5614-5619