A C. elegans Myc-like network cooperates with semaphorin and Wnt signaling pathways to control cell migration

Developmental Biology

Volumn 310, Issue 2, 2007, Pages 226-239

  Pickett, Christopher L ^a   Breen, Kevin T ^a   Ayer, Donald E ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Cell migration; ECM; Mondo; Myc; Plexin; Semaphorin; Wnt; catenin

Indexed keywords

BETA CATENIN; MAX PROTEIN; MML1 PROTEIN; MXL2 PROTEIN; MYC PROTEIN; SEMAPHORIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; COMPLEX FORMATION; ENERGY METABOLISM; EPIDERMIS; EUKARYOTE; EXTRACELLULAR MATRIX; GENE ACTIVATION; GENE AMPLIFICATION; GENE FUNCTION; GENE INTERACTION; GENE SEQUENCE; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL;

CAENORHABDITIS ELEGANS; EUKARYOTA;

EID: 34748922359     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.07.034     Document Type: Article

References (79)

1. In: Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., and Struhl K. (Eds). Current Protocols in Molecular Biology (1995), John Wiley and Sons, Inc
2. Ayer D.E., Laherty C.D., Lawrence Q.A., Armstrong A.P., and Eisenman R.N. Mad proteins contain a dominant transcription repression domain. Mol. Cell. Biol. 16 (1996) 5772-5781
3. Baird S.E., Fitch D.H., Kassem I.A., and Emmons S.W. Pattern formation in the nematode epidermis: determination of the arrangement of peripheral sense organs in the C. elegans male tail. Development 113 (1991) 515-526
4. Beckner M.E., Stracke M.L., Liotta L.A., and Schiffmann E. Glycolysis as primary energy source in tumor cell chemotaxis. J. Natl. Cancer Inst. 82 (1990) 1836-1840
5. Bhoite L.T., Yu Y., and Stillman D.J. The Swi5 activator recruits the Mediator complex to the HO promoter without RNA polymerase II. Genes Dev. 15 (2001) 2457-2469
6. Billin A.N., and Ayer D.E. The Mlx network: evidence for a parallel Max-like transcriptional network that regulates energy metabolism. Curr. Top. Microbiol. Immunol. 302 (2006) 255-278
7. Billin A.N., Eilers A.L., Queva C., and Ayer D.E. Mlx, a novel Max-like BHLHZip protein that interacts with the Max network of transcription factors. J. Biol. Chem. 274 (1999) 36344-36350
8. Billin A.N., Eilers A.L., Coulter K.L., Logan J.S., and Ayer D.E. MondoA, a novel basic helix-loop-helix-leucine zipper transcriptional activator that constitutes a positive branch of a max-like network. Mol. Cell. Biol. 20 (2000) 8845-8854
9. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
10. Chen M., O'Toole E.A., Li Y.Y., and Woodley D.T. Alpha 2 beta 1 integrin mediates dermal fibroblast attachment to type VII collagen via a 158-amino-acid segment of the NC1 domain. Exp. Cell. Res. 249 (1999) 231-239
11. Cole M.D., and Nikiforov M.A. Transcriptional activation by the Myc oncoprotein. Curr. Top. Microbiol. Immunol. 302 (2006) 33-50
12. Coller H.A., Grandori C., Tamayo P., Colbert T., Lander E.S., Eisenman R.N., and Golub T.R. Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3260-3265
13. Dalpe G., Zhang L.W., Zheng H., and Culotti J.G. Conversion of cell movement responses to Semaphorin-1 and Plexin-1 from attraction to repulsion by lowered levels of specific RAC GTPases in C. elegans. Development 131 (2004) 2073-2088
14. Dalpe G., et al. Vulva morphogenesis involves attraction of plexin 1-expressing primordial vulva cells to semaphorin 1a sequentially expressed at the vulva midline. Development 132 (2005) 1387-1400
15. Dang C.V. c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol. Cell. Biol. 19 (1999) 1-11
16. de Luis O., Valero M.C., and Jurado L.A. WBSCR14, a putative transcription factor gene deleted in Williams-Beuren syndrome: complete characterisation of the human gene and the mouse ortholog. Eur. J. Hum. Genet. 8 (2000) 215-222
17. Deplancke B., Mukhopadhyay A., Ao W., Elewa A.M., Grove C.A., Martinez N.J., Sequerra R., Doucette-Stamm L., Reece-Hoyes J.S., Hope I.A., Tissenbaum H.A., Mango S.E., and Walhout A.J. A gene-centered C. elegans protein-DNA interaction network. Cell 125 (2006) 1193-1205
18. Eilers A.L., Sundwall E., Lin M., Sullivan A.A., and Ayer D.E. A novel heterodimerization domain, CRM1, and 14-3-3 control subcellular localization of the MondoA-Mlx heterocomplex. Mol. Cell. Biol. 22 (2002) 8514-8526
19. Eisenmann D.M., Maloof J.N., Simske J.S., Kenyon C., and Kim S.K. The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. Development 125 (1998) 3667-3680
20. Emmons, S.W. (2005). "Male Development."
21. Ferguson E.L., and Horvitz H.R. The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways. Genetics 123 (1989) 109-121
22. Fernandez P.C., Frank S.R., Wang L., Schroeder M., Liu S., Greene J., Cocito A., and Amati B. Genomic targets of the human c-Myc protein. Genes Dev. 17 (2003) 1115-1129
23. Ferre-D'Amare A.R., Prendergast G.C., Ziff E.B., and Burley S.K. Recognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature 363 (1993) 38-45
24. Fleischer T.C., Yun U.J., and Ayer D.E. Identification and characterization of three new components of the mSin3A corepressor complex. Mol. Cell. Biol. 23 (2003) 3456-3467
25. Frye M., Gardner C., Li E.R., Arnold I., and Watt F.M. Evidence that Myc activation depletes the epidermal stem cell compartment by modulating adhesive interactions with the local microenvironment. Development 130 (2003) 2793-2808
26. Fujii T., Nakao F., Shibata Y., Shioi G., Kodama E., Fujisawa H., and Takagi S. Caenorhabditis elegans PlexinA, PLX-1, interacts with transmembrane semaphorins and regulates epidermal morphogenesis. Development 129 (2002) 2053-2063
27. Funasaka T., Yanagawa T., Hogan V., and Raz A. Regulation of phosphoglucose isomerase/autocrine motility factor expression by hypoxia. FASEB J. 19 (2005) 1422-1430
28. Gatenby R.A., Gawlinski E.T., Gmitro A.F., Kaylor B., and Gillies R.J. Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res. 66 (2006) 5216-5223
29. Giblin P.A., Hwang S.T., Katsumoto T.R., and Rosen S.D. Ligation of L-selectin on T lymphocytes activates beta1 integrins and promotes adhesion to fibronectin. J. Immunol. 159 (1997) 3498-34507
30. Gilleard J.S., Barry J.D., and Johnstone I.L. cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy-7. Mol. Cell. Biol. 17 (1997) 2301-2311
31. Ginzburg V.E., Roy P.J., and Culotti J.G. Semaphorin 1a and semaphorin 1b are required for correct epidermal cell positioning and adhesion during morphogenesis in C. elegans. Development 129 (2002) 2065-2078
32. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
33. Hilliard M.A., and Bargmann C.I. Wnt signals and frizzled activity orient anterior-posterior axon outgrowth in C. elegans. Dev. Cell 10 (2006) 379-390
34. Hodgkin J., Horvitz H.R., and Brenner S. Nondisjunction mutants of the nematode C. elegans. Genetics 91 (1979) 67-94
35. Hollenberg S.M., Sternglanz R., Cheng P.F., and Weintraub H. Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol. Cell. Biol. 15 (1995) 3813-3822
36. Honigberg L., and Kenyon C. Establishment of left/right asymmetry in neuroblast migration by UNC-40/DCC, UNC-73/Trio and DPY-19 proteins in C. elegans. Development 127 (2000) 4655-4668
37. Iizuka K., Bruick R.K., Liang G., Horton J.D., and Uyeda K. Deficiency of carbohydrate response element-binding protein (ChREBP) reduces lipogenesis as well as glycolysis. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 7281-7286
38. Inghirami G., Grignani F., Sternas L., Lombardi L., Knowles D.M., and Dalla-Favera R. Down-regulation of LFA-1 adhesion receptors by c-myc oncogene in human B lymphoblastoid cells. Science 250 (1990) 682-686
39. Kagoshima M., and Ito T. Diverse gene expression and function of semaphorins in developing lung: positive and negative regulatory roles of semaphorins in lung branching morphogenesis. Genes Cells. 6 (2001) 559-571
40. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., and Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 (2003) 231-237
41. Kern A., Eble J., Golbik R., and Kuhn K. Interaction of type IV collagen with the isolated integrins alpha 1 beta 1 and alpha 2 beta 1. Eur. J. Biochem. 215 (1993) 151-159
42. Korswagen H.C. Canonical and non-canonical Wnt signaling pathways in Caenorhabditis elegans: variations on a common signaling theme. BioEssays 24 (2002) 801-810
43. Korswagen H.C., Herman M.A., and Clevers H.C. Distinct beta-catenins mediate adhesion and signalling functions in C. elegans. Nature 406 (2000) 527-532
44. Kryczek I., Wei S., Keller E., Liu R., and Zou W. Stromal derived factor (SDF-1/CXCL12) and human tumor pathogenesis. Am. J. Physiol.: Cell Physiol. 292 (2007) C987-C995
45. Lee L.A., and Dang C.V. Myc target transcriptomes. Curr. Top. Microbiol. Immunol. 302 (2006) 145-167
46. Levy Y., Ronen D., Bershadsky A.D., and Zick Y. Sustained induction of ERK, protein kinase B, and p70 S6 kinase regulates cell spreading and formation of F-actin microspikes upon ligation of integrins by galectin-8, a mammalian lectin. J. Biol. Chem. 278 (2003) 14533-14542
47. Li C., et al. Wnt5a participates in distal lung morphogenesis. Dev. Biol. 248 (2002) 68-81
48. Li M.V., Chang B., Imamura M., Poungvarin N., and Chan L. Glucose-dependent transcriptional regulation by an evolutionarily conserved glucose-sensing module. Diabetes 55 (2006) 1179-1189
49. Liu K.S., and Sternberg P.W. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14 (1995) 79-89
50. Liu Z., et al. C. elegans PlexinA PLX-1 mediates a cell contact-dependent stop signal in vulval precursor cells. Dev. Biol. 282 (2005) 138-151
51. Maloof J.N., Whangbo J., Harris J.M., Jongeward G.D., and Kenyon C. A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans. Development 126 (1999) 37-49
52. McCawley L.J., and Matrisian L.M. Tumor progression: defining the soil round the tumor seed. Curr. Biol. 11 (2001) R25-R27
53. Mello C.C., Kramer J.M., Stinchcomb D., and Ambros V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10 (1991) 3959-3970
54. Miller III D.M., Ortiz I., Berliner G.C., and Epstein H.F. Differential localization of two myosins within nematode thick filaments. Cell 34 (1983) 477-490
55. Mohler W.A., Simske J.S., Williams-Masson E.M., Hardin J.D., and White J.G. Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis. Curr. Biol. 8 (1998) 1087-1090
56. Nair S.K., and Burley S.K. X-ray structures of Myc-Max and Mad-Max recognizing DNA. Molecular bases of regulation by proto-oncogenic transcription factors. Cell 112 (2003) 193-205
57. Natarajan L., Jackson B.M., Szyleyko E., and Eisenmann D.M. Identification of evolutionarily conserved promoter elements and amino acids required for function of the C. elegans beta-catenin homolog BAR-1. Dev. Biol. 272 (2004) 536-557
58. Nelson W.J., and Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303 (2004) 1483-1487
59. Noujaim D., van Golen C.M., van Golen K.L., Grauman A., and Feldman E.L. N-Myc and Bcl-2 coexpression induces MMP-2 secretion and activation in human neuroblastoma cells. Oncogene 21 (2002) 4549-4557
60. Orian A., van Steensel B., Delrow J., Bussemaker H.J., Li L., Sawado T., Williams E., Loo L.W., Cowley S.M., Yost C., Pierce S., Edgar B.A., Parkhurst S.M., and Eisenman R.N. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev. 17 (2003) 1101-1114
61. Pan C.L., Howell J.E., Clark S.G., Hilliard M., Cordes S., Bargmann C.I., and Garriga G. Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev. Cell 10 (2006) 367-377
62. Peifer, M. (2002). Developmental biology: colon construction. Nature 420, 274-5, 277.
63. Pettitt J., Wood W.B., and Plasterk R.H. cdh-3, a gene encoding a member of the cadherin superfamily, functions in epithelial cell morphogenesis in Caenorhabditis elegans. Development 122 (1996) 4149-4157
64. Pirity M., Blanck J.K., and Schreiber-Agus N. Lessons learned from Myc/Max/Mad knockout mice. Curr. Top. Microbiol. Immunol. 302 (2006) 205-234
65. Prasad B.C., and Clark S.G. Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development 133 (2006) 1757-1766
66. Rottmann S., and Luscher B. The Mad side of the Max network: antagonizing the function of Myc and more. Curr. Top. Microbiol. Immunol. 302 (2006) 63-122
67. Sans C.L., Satterwhite D.J., Stoltzman C.A., Breen K.T., and Ayer D.E. MondoA-Mlx heterodimers are candidate sensors of cellular energy status: mitochondrial localization and direct regulation of glycolysis. Mol. Cell. Biol. 26 (2006) 4863-4871
68. Schnabel H.a.S., and R. An organ-specific differentiation gene, pha-1, from Caenorhabditis elegans. Science 250 (1990) 686-688
69. Shu W., et al. Wnt7b regulates mesenchymal proliferation and vascular development in the lung. Development 129 (2002) 4831-4842
70. Simske J.S., and Hardin J. Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos. BioEssays 23 (2001) 12-23
71. Sterneck E., Muller C., Katz S., and Leutz A. Autocrine growth induced by kinase type oncogenes in myeloid cells requires AP-1 and NF-M, a myeloid specific, C/EBP-like factor. EMBO J. 11 (1992) 115-126
72. Tamagnone L., and Comoglio P.M. To move or not to move? Semaphorin signalling in cell migration. EMBO Rep. 5 (2004) 356-361
73. Uyeda K., and Repa J.J. Carbohydrate response element binding protein, ChREBP, a transcription factor coupling hepatic glucose utilization and lipid synthesis. Cell. Metab. 4 (2006) 107-110
74. Wade M., and Wahl G.M. c-Myc, genome instability, and tumorigenesis: the devil is in the details. Curr. Top. Microbiol. Immunol. 302 (2006) 169-203
75. Watnick R.S., Cheng Y.N., Rangarajan A., Ince T.A., and Weinberg R.A. Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell 3 (2003) 219-231
76. Yamaguchi H., Wyckoff J., and Condeelis J. Cell migration in tumors. Curr. Opin. Cell Biol. 17 (2005) 559-564
77. Yamashita H., Takenoshita M., Sakurai M., Bruick R.K., Henzel W.J., Shillinglaw W., Arnot D., and Uyeda K. A glucose-responsive transcription factor that regulates carbohydrate metabolism in the liver. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 9116-9121
78. Yuan J., Tirabassi R.S., Bush A.B., and Cole M.D. The C. elegans MDL-1 and MXL-1 proteins can functionally substitute for vertebrate MAD and MAX. Oncogene 17 (1998) 1109-1118
79. Zhang X.Y., DeSalle L.M., Patel J.H., Capobianco A.J., Yu D., Thomas-Tikhonenko A., and McMahon S.B. Metastasis-associated protein 1 (MTA1) is an essential downstream effector of the c-MYC oncoprotein. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 13968-13973