Abstract
The Myc proto-oncogenes, their binding partner Max and their antagonists from the Mad family of transcriptional repressors have been extensively analysed in vertebrates. However, members of this network are found in all animals examined so far. Several recent studies have addressed the physiological function of these proteins in invertebrate model organisms, in particular Drosophila melanogaster. This review describes the structure of invertebrate Myc/Max/Mad genes and it discusses their regulation and physiological functions, with special emphasis on their essential role in the control of cellular growth and proliferation.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195
Amati B, Frank SR, Donjerkovic D, Taubert S (2001) Function of the c-Myc oncoprotein in chromatin remodeling and transcription. Biochim Biophys Acta 1471:M135–M145
Arsura M, Deshpande A, Hann SR, Sonenshein GE (1995) Variant Max protein, derived by alternative splicing, associates with c-Myc in vivo and inhibits transactivation. Mol Cell Biol 15:6702–6709
Atchley WR, Fitch WM (1995) Myc and Max: molecular evolution of a family of proto-oncogene products and their dimerization partner. Proc Natl Acad Sci U S A 92:10217–10221
Ayer DE, Lawrence QA, Eisenman RN (1995) Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell 80:767–776
Biegalke BJ, Heaney ML, Bouton A, Parsons JT, Linial M (1987) MC29 deletion mutants which fail to transform chicken macrophages are competent for transformation of quail macrophages. J Virol 61:2138–2142
Bellosta P, Hulf T, Diop SB, Usseglio F, Pradel J, Aragnol D, Gallant P (2005) Myc interacts genetically with Tip48/Reptin and Tip49/Pontin to control growth and proliferation during Drosophila development. Proc Nat Acad Sci U S A 102:11799
Benassayag C, Montero L, Colombié N, Gallant P, Cribbs D, Morello D (2005) Human c-Myc isoforms differentialy regulate cell growth and apoptosis in Drosophila. Mol Cell Biol 25:9897
Bishop JM (1983) Cellular oncogenes and retroviruses. Annu Rev Biochem 52:301–354
Blackwood EM, Eisenman RN (1991) Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc. Science 251:1211–1217
Bourbon HM, Gonzy-Treboul G, Peronnet F, Alin MF, Ardourel C, Benassayag C, Cribbs D, Deutsch J, Ferrer P, Haenlin M, et al (2002) A P-insertion screen identifying novel X-linked essential genes in Drosophila. Mech Dev 110:71–83
Bridges CB (1935) Drosophila melanogaster: legend for symbols, mutants, valuations. Drosophila Information Service 3:5–19
Britton JS, Lockwood WK, Li L, Cohen SM, Edgar BA (2002) Drosophila’s insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev Cell 2:239–249
Charron J, Malynn BA, Fisher P, Stewart V, Jeannotte L, Goff SP, Robertson EJ, Alt FW (1992) Embryonic lethality in mice homozygous for a targeted disruption of the N-myc gene. Genes Dev 6:2248–2257
Cheng SW, Davies KP, Yung E, Beltran RJ, Yu J, Kalpana GV (1999) c-MYC interacts with INI1/hSNF5 and requires the SWI/SNF complex for transactivation function. Nat Genet 22:102–105
Davis AC, Wims M, Spotts GD, Hann SR, Bradley A (1993) A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes Dev 7:671–682
Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167
Eilers AL, Billin AN, Liu J, Ayer DE (1999) A 13-amino acid amphipathic alpha-helix is required for the functional interaction between the transcriptional repressor Mad1 and mSin3A. J Biol Chem 274:32750–32756
Eisenman RN (2001) Deconstructing myc. Genes Dev 15:2023–2030
Elend M, Eilers M (1999) Cell growth: downstream of Myc—to grow or to cycle? Curr Biol 9:R936–R938
FitzGerald MJ, Arsura M, Bellas RE, Yang W, Wu M, Chin L, Mann KK, DePinho RA, Sonenshein GE (1999) Differential effects of the widely expressed dMax splice variant of Max on E-box vs initiator element-mediated regulation by c-Myc. Oncogene 18:2489–2498
Gallant P, Shiio Y, Cheng PF, Parkhurst SM, Eisenman RN (1996) Myc and Max homologs in Drosophila. Science 274:1523–1527
Gupta MP, Amin CS, Gupta M, Hay N, Zak R (1997) Transcription enhancer factor 1 interacts with a basic helix-loop-helix zipper protein, Max, for positive regulation of cardiac alpha-myosin heavy-chain gene expression. Mol Cell Biol 17:3924–3936
Heaney ML, Pierce J, Parsons JT (1986) Site-directed mutagenesis of the gag-myc gene of avian myelocytomatosis virus 29: biological activity and intracellular localization of structurally altered proteins. J Virol 60:167–176
Hedges SB (2002) The origin and evolution of model organisms. Nat Rev Genet 3:838–849
Hennig KM, Neufeld TP (2002) Inhibition of cellular growth and proliferation by dTOR overexpression in Drosophila. Genesis 34:107–110
Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149
Hopewell R, Ziff EB (1995) The nerve growth factor-responsive PC12 cell line does not express the Myc dimerization partner Max. Mol Cell Biol 15:3470–3478
Hulf T, Bellosta P, Furrer M, Steiger D, Svensson D, Barbour A, Gallant P (2005) Whole-genome analysis reveals a strong positional bias of conserved dMyc-dependent E-boxes. Mol Cell Biol 25:3401
Hurlin PJ, Steingrimsson E, Copeland NG, Jenkins NA, Eisenman RN (1999) Mga, a dual-specificity transcription factor that interacts with Max and contains a T-domain DNA-binding motif. EMBO J 18:7019–7028
Jiao R, Daube M, Duan H, Zou Y, Frei E, Noll M (2001) Headless flies generated by developmental pathway interference. Development 128:3307–3319
Johansson US, Parsons TJ, Irestedt M, Ericson PGP (2001) Clades within the ‘higher land birds’, evaluated by nuclear DNA sequences. J Zoolog Syst Evol Res 39:37–51
Johnston LA, Prober DA, Edgar BA, Eisenman RN, Gallant P (1999) Drosophila myc regulates cellular growth during development. Cell 98:779–790
Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, et al (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231–237
King MW, Blackwood EM, Eisenman RN (1993) Expression of two distinct homologues of Xenopus Max during early development. Cell Growth Differ 4:85–92
King RC, Burnett RG (1957) Oogenesis in adult Drosophila melanogaster. Growth 21:263–280
King RC, Vanoucek EG (1960) Oogenesis in adult Drosophila melanogaster. X. Studies on the behavior of the follicle cells. Growth 24:333–338
Koskinen PJ, Vastrik I, Makela TP, Eisenman RN, Alitalo K (1994) Max activity is affected by phosphorylation at two NH2-terminal sites. Cell Growth Differ 5:313–320
Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Loo LW, Secombe J, Little JT, Carlos LS, Yost C, Cheng PF, Flynn EM, Edgar BA, Eisenman RN (2005) The transcriptional repressor dMnt is a regulator of growth in Drosophila melanogaster. Mol Cell Biol 25:7078
Madhavan K, Bilodeau WD, Wadsworth SC (1985) Initial sequencing and analysis of the human genome. Mol Cell Biol 5:7–16
Maeda I, Kohara Y, Yamamoto M, Sugimoto A (2001) Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 11:171–176
Makela TP, Koskinen PJ, Vastrik I, Alitalo K (1992) Alternative forms of Max as enhancers or suppressors of Myc-ras cotransformation. Science 256:373–377
Maines JZ, Stevens LM, Tong X, Stein D (2004) Drosophila dMyc is required for ovary cell growth and endoreplication. Development 131:775
Mateyak MK, Obaya AJ, Adachi S, Sedivy JM (1997) Terminally differentiated skeletal myotubes are not confined to G0 but can enter G1 upon growth factor stimulation. Cell Growth Differ 8:1039–1048
McMahon SB, Van BH, Dugan KA, Copeland TD, Cole MD (1998) The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94:363–374
Miyamoto MM, Freire NP (2000) Evolution of CpG islands within the myc gene family. Mol Phylogenet Evol 16:475–481
Miyazaki T, Liu ZJ, Kawahara A, Minami Y, Yamada K, Tsujimoto Y, Barsoumian EL, Permutter RM, Taniguchi T (1995) Three distinct IL-2 signaling pathways mediated by bcl-2, c-myc, and lck cooperate in hematopoietic cell proliferation. Cell 81:223–231
Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424:277–283
Orian A, Van Steensel B, Delrow J, Bussemaker HJ, Li L, Sawado T, Williams E, Loo LW, Cowley SM, Yost C, et al (2003) Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev 17:1101–1114
Oster SK, Ho CS, Soucie EL, Penn LZ (2002) The myc oncogene: MarvelouslY Complex. Adv Cancer Res 84:81–154
Park J, Wood MA, Cole MD (2002) BAF53 forms distinct nuclear complexes and functions as a critical c-Myc-interacting nuclear cofactor for oncogenic transformation. Mol Cell Biol 22:1307–1316
Peyrefitte S, Kahn D, Haenlin M (2001) New members of the Drosophila Myc transcription factor subfamily revealed by a genome-wide examination for basic helix-loop-helix genes. Mech Dev 104:99–104
Pierce SB, Yost C, Britton JS, Loo LW, Flynn EM, Edgar BA, Eisenman RN (2004) dMyc is required for larval growth and endoreplication in Drosophila. Development 131:2317–2327
Prober DA, Edgar BA (2000) Ras1 promotes cellular growth in the Drosophila wing. Cell 100:435–446
Prober DA, Edgar BA (2002) Interactions between Ras1, dMyc, and dPI3K signaling in the developing Drosophila wing. Genes Dev 16:2286–2299
Sarid J, Halazonetis TD, Murphy W, Leder P (1987) Evolutionarily conserved regions of the human c-myc protein can be uncoupled from transforming activity. Proc Natl Acad Sci U S A 84:170–173
Sawai S, Shimono A, Wakamatsu Y, Palmes C, Hanaoka K, Kondoh H (1993) Defects of embryonic organogenesis resulting from targeted disruption of the N-myc gene in the mouse. Development 117:1445–1455
Schmelzle T, Hall MN (2000) TOR, a central controller of cell growth. Cell 103:253–262
Schreiber-Agus N, Chin L, Chen K, Torres R, Rao G, Guida P, Skoultchi AI, DePinho RA (1995) An amino-terminal domain of Mxi1 mediates anti-Myc oncogenic activity and interacts with a homolog of the yeast transcriptional repressor SIN3. Cell 80:777–786
Schreiber-Agus N, Stein D, Chen K, Goltz JS, Stevens L, DePinho RA (1997) Drosophila Myc is oncogenic in mammalian cells and plays a role in the diminutive phenotype. Proc Natl Acad Sci U S A 94:1235–1240
Sears R, Leone G, DeGregori J, Nevins JR (1999) Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol Cell 3:169–179
Shilo B-Z, Weinberg RA (1981) DNA sequences homologous to vertebrate oncogenes are conserved in Drosophila melanogaster. Proc Natl Acad Sci USA 78:6789–6792
Shors ST, Efiok BJ, Harkin SJ, Safer B (1998) Formation of alpha-Pal/Max heterodimers synergistically activates the eIF2-alpha promoter. J Biol Chem 273:34703–34709
Sollenberger KG, Kao TL, Taparowsky EJ (1994) Structural analysis of the chicken max gene. Oncogene 9:661–664
Spencer CA, Groudine M (1991) Control of c-myc regulation in normal and neoplastic cells. Adv Cancer Res 56:1–48
Tapon N, Ito N, Dickson BJ, Treisman JE, Hariharan IK (2001) The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 105:345–355
Tonissen KF, Krieg PA (1994) Analysis of a variant Max sequence expressed in Xenopus laevis. Oncogene 9:33–38
Trumpp A, Refaeli Y, Oskarsson T, Gasser S, Murphy M, Martin GR, Bishop JM (2001) c-Myc regulates mammalian body size by controlling cell number but not cell size. Nature 414:768–773
Urao T, Yamaguchi-Shinozaki K, Mitsukawa N, Shibata D, Shinozaki K (1996) Molecular cloning and characterization of a gene that encodes a MYC-related protein in Arabidopsis. Plant Mol Biol 32:571–576
Vastrik I, Koskinen PJ, Alitalo R, Makela TP (1993) Alternative mRNA forms and open reading frames of the max gene. Oncogene 8:503–507
Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, et al (2001) The sequence of the human genome. Science 291:1304–1351
Vervoorts J, Luscher-Firzlaff JM, Rottmann S, Lilischkis R, Walsemann G, Dohmann K, Austen M, Luscher B (2003) Stimulation of c-MYC transcriptional activity and acetylation by recruitment of the cofactor CBP. EMBO Rep 4:1–7
Walker CW, Boom JD, Marsh AG (1992) First non-vertebrate member of the myc gene family is seasonally expressed in an invertebrate testis. Oncogene 7:2007–2012
Wanzel M, Herold S, Eilers M (2003) Transcriptional repression by Myc. Trends Cell Biol 13:146–150
Wood MA, McMahon SB, Cole MD (2000) An ATPase/helicase complex is an essential cofactor for oncogenic transformation by c-Myc. Mol Cell 5:321–330
Xue L, Noll M (2002) Dual role of the Pax gene paired in accessory gland development of Drosophila. Development 129:339–346
Yuan J, Tirabassi RS, Bush AB, Cole MD (1998) The C. elegans MDL-1 and MXL-1 proteins can functionally substitute for vertebrate MAD and MAX. Oncogene 17:1109–1118
Zaffran S, Chartier A, Gallant P, Astier M, Arquier N, Doherty D, Gratecos D, Semeriva M (1998) A Drosophila RNA helicase gene, pitchoune, is required for cell growth and proliferation and is a potential target of d-Myc. Development 125:3571–3584
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2006 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Gallant, P. (2006). Myc/Max/Mad in Invertebrates: The Evolution of the Max Network. In: Eisenman, R.N. (eds) The Myc/Max/Mad Transcription Factor Network. Current Topics in Microbiology and Immunology, vol 302. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-32952-8_9
Download citation
DOI: https://doi.org/10.1007/3-540-32952-8_9
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-23968-0
Online ISBN: 978-3-540-32952-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)