A C. Elegans Myc-like Network Cooperates with Semaphorin and Wnt Signaling Pathways to Control Cell Migration

Overview

Journal Dev Biol

Publisher Elsevier

Specialties Biology
Reproductive Medicine

Date 2007 Sep 11

PMID 17826759

Citations 29

Authors

Christopher L Pickett

Kevin T Breen

Donald E Ayer

Affiliations

Soon will be listed here.

Abstract

Myc and Mondo proteins are key regulators of cell growth, proliferation, and energy metabolism, yet often overlooked is their vital role in cell migration. Complex networks of protein-protein and protein-DNA interactions control the transcriptional activity of Myc and MondoA confounding their functional analysis in higher eukaryotes. Here we report the identification of the transcriptional activation arm of a simplified Myc-like network in Caenorhabditis elegans. This network comprises an Mlx ortholog, named MXL-2 for Max-like 2, and a protein that has sequence features of both Myc and Mondo proteins, named MML-1 for Myc and Mondo-like 1. MML-1/MXL-2 complexes have a primary function in regulating migration of the ray 1 precursor cells in the male tail. MML-1/MXL-2 complexes control expression of ECM components in the non-migratory epidermis, which we propose contributes to the substratum required for migration of the neighboring ray 1 precursor cells. Furthermore, we show that pro-migratory Wnt/beta-catenin and semaphorin signaling pathways interact genetically with MML-1/MXL-2 to determine ray 1 position. This first functional analysis of the Myc superfamily in C. elegans suggests that MondoA and Myc may have more predominant roles in cell migration than previously appreciated, and their cooperation with other pro-migratory pathways provides a more integrated view of their role in cell migration.

Citing Articles

The C. elegans Myc-family of transcription factors coordinate a dynamic adaptive response to dietary restriction.

Cornwell A, Zhang Y, Thondamal M, Johnson D, Thakar J, Samuelson A Geroscience. 2024; 46(5):4827-4854.

PMID: 38878153 PMC: 11336136. DOI: 10.1007/s11357-024-01197-x.

Neuronal MML-1/MXL-2 regulates systemic aging via glutamate transporter and cell nonautonomous autophagic and peroxidase activity.

Shioda T, Takahashi I, Ikenaka K, Fujita N, Kanki T, Oka T Proc Natl Acad Sci U S A. 2023; 120(39):e2221553120.

PMID: 37722055 PMC: 10523562. DOI: 10.1073/pnas.2221553120.

The ABL-MYC axis controls WIPI1-enhanced autophagy in lifespan extension.

Sporbeck K, Haas M, Pastor-Maldonado C, Schussele D, Hunter C, Takacs Z Commun Biol. 2023; 6(1):872.

PMID: 37620393 PMC: 10449903. DOI: 10.1038/s42003-023-05236-9.

Homeodomain-interacting protein kinase maintains neuronal homeostasis during normal aging and systemically regulates longevity from serotonergic and GABAergic neurons.

Lazaro-Pena M, Cornwell A, Diaz-Balzac C, Das R, Ward Z, Macoretta N Elife. 2023; 12.

PMID: 37338980 PMC: 10393298. DOI: 10.7554/eLife.85792.

The proline-rich domain of MML-1 is biologically important but not required for localization to target promoters.

Ceballos A, Esse R, Grishok A MicroPubl Biol. 2021; 2021.

PMID: 34778725 PMC: 8579147. DOI: 10.17912/micropub.biology.000498.

References

Eisenmann D, Maloof J, Simske J, Kenyon C, Kim S . The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. Development. 1998; 125(18):3667-80. DOI: 10.1242/dev.125.18.3667. View

Korswagen H, Herman M, Clevers H . Distinct beta-catenins mediate adhesion and signalling functions in C. elegans. Nature. 2000; 406(6795):527-32. DOI: 10.1038/35020099. View

Dang C . c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol Cell Biol. 1998; 19(1):1-11. PMC: 83860. DOI: 10.1128/MCB.19.1.1. View

Yamaguchi H, Wyckoff J, Condeelis J . Cell migration in tumors. Curr Opin Cell Biol. 2005; 17(5):559-64. DOI: 10.1016/j.ceb.2005.08.002. View

Fujii T, Nakao F, Shibata Y, Shioi G, Kodama E, Fujisawa H . Caenorhabditis elegans PlexinA, PLX-1, interacts with transmembrane semaphorins and regulates epidermal morphogenesis. Development. 2002; 129(9):2053-63. DOI: 10.1242/dev.129.9.2053. View

Pan C, Howell J, Clark S, Hilliard M, Cordes S, Bargmann C . Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev Cell. 2006; 10(3):367-77. DOI: 10.1016/j.devcel.2006.02.010. View

Uyeda K, Repa J . Carbohydrate response element binding protein, ChREBP, a transcription factor coupling hepatic glucose utilization and lipid synthesis. Cell Metab. 2006; 4(2):107-10. DOI: 10.1016/j.cmet.2006.06.008. View

Beckner M, Stracke M, Liotta L, Schiffmann E . Glycolysis as primary energy source in tumor cell chemotaxis. J Natl Cancer Inst. 1990; 82(23):1836-40. DOI: 10.1093/jnci/82.23.1836. View

Coller H, Grandori C, Tamayo P, Colbert T, Lander E, Eisenman 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. 2000; 97(7):3260-5. PMC: 16226. DOI: 10.1073/pnas.97.7.3260. View

10.

Natarajan L, Jackson B, Szyleyko E, Eisenmann D . Identification of evolutionarily conserved promoter elements and amino acids required for function of the C. elegans beta-catenin homolog BAR-1. Dev Biol. 2004; 272(2):536-57. DOI: 10.1016/j.ydbio.2004.05.027. View

11.

Yamashita H, Takenoshita M, Sakurai M, Bruick R, Henzel W, Shillinglaw W . A glucose-responsive transcription factor that regulates carbohydrate metabolism in the liver. Proc Natl Acad Sci U S A. 2001; 98(16):9116-21. PMC: 55382. DOI: 10.1073/pnas.161284298. View

12.

Sterneck E, Muller C, Katz S, 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. 1992; 11(1):115-26. PMC: 556432. DOI: 10.1002/j.1460-2075.1992.tb05034.x. View

13.

Peifer M . Developmental biology: colon construction. Nature. 2002; 420(6913):274-5, 277. DOI: 10.1038/420274a. View

14.

Funasaka T, Yanagawa T, Hogan V, Raz A . Regulation of phosphoglucose isomerase/autocrine motility factor expression by hypoxia. FASEB J. 2005; 19(11):1422-30. DOI: 10.1096/fj.05-3699com. View

15.

Tamagnone L, Comoglio P . To move or not to move? Semaphorin signalling in cell migration. EMBO Rep. 2004; 5(4):356-61. PMC: 1299025. DOI: 10.1038/sj.embor.7400114. View

16.

Wade M, Wahl G . c-Myc, genome instability, and tumorigenesis: the devil is in the details. Curr Top Microbiol Immunol. 2006; 302:169-203. DOI: 10.1007/3-540-32952-8_7. View

17.

Li M, Chang B, Imamura M, Poungvarin N, Chan L . Glucose-dependent transcriptional regulation by an evolutionarily conserved glucose-sensing module. Diabetes. 2006; 55(5):1179-89. DOI: 10.2337/db05-0822. View

18.

Baird S, Fitch D, Kassem I, Emmons S . Pattern formation in the nematode epidermis: determination of the arrangement of peripheral sense organs in the C. elegans male tail. Development. 1991; 113(2):515-26. DOI: 10.1242/dev.113.2.515. View

19.

Hodgkin J, Horvitz H, Brenner S . Nondisjunction Mutants of the Nematode CAENORHABDITIS ELEGANS. Genetics. 1979; 91(1):67-94. PMC: 1213932. DOI: 10.1093/genetics/91.1.67. View

20.

Korswagen H . Canonical and non-canonical Wnt signaling pathways in Caenorhabditis elegans: variations on a common signaling theme. Bioessays. 2002; 24(9):801-10. DOI: 10.1002/bies.10145. View