The Svedberg Award 2005

Ruth Palmer
Umeå Center for Molecular Pathogenesis, Umeå University

Background
I was born in Kilmarnock, Scotland in 1970, and carried out my undergraduate studies in Biochemistry at the University of Dundee, Scotland. During this time I became interested in signal transduction, and was lucky enough to join the laboratory of Peter Parker at the Cancer Research UK (then called the Imperial Cancer Research Fund) where I worked on a then novel family of PKC related protein kinase and the signal transduction pathways they were involved in. I defended my PhD thesis in January 1996, after which I moved to San Diego, California to take up a post-doctoral position at the Salk Institute, in the laboratory of Tony Hunter. At this time I was still interested in signal transduction, but realized I wanted to learn more about genetics and how to use genetic model systems to address the complex problems we face in the field of signal transduction. During this time I began working with the small banana-fly Drosophila melanogaster, and utilizing the fly to tackle signal transduction via tyrosine kinases. In 1996 I moved to Umeå University in Sweden and have continued with this line of research. My group is based at the Umeå Center for Molecular Pathogenesis and focuses on addressing signal transduction in developmental processes using the banana-fly as our main tool.

Research
A wide range of processes are mediated by receptor tyrosine kinases (RTKs) and their signalling pathways. The growing list of processes regulated by these receptors across the phylogenetic tree is extremely broad, and includes induction of cell fates, guidance of cell and axon migration, and cell proliferation. Ligand binding to the extracellular domain induces activation of the kinase on the cytoplasmic side, which initiates the intracellular signalling. The activated RTKs phosphorylate themselves and cytoplasmic substrates, leading to activation of a number of downstream signalling molecules, and ultimately induce changes in gene expression and the phenotypic state of the cell. RTKs thus play important roles in cellular proliferation and differentiation. In addition, RTKs reveal oncogenic potential when their kinase activities are constitutively enhanced by point mutation, amplification, or rearrangement of the corresponding genes.
Mammalian Anaplastic Lymphoma Kinase (Alk) was originally identified as a member of the insulin receptor subfamily of RTKs that acquires transforming capability when truncated and fused to nucleophosmin (NPM) in the t(2;5) chromosomal rearrangement associated with a specific type of aggressive non-Hodgkin's lymphoma. To date, many chromosomal rearrangements leading to an activated Alk RTK have been described. However, when we began working on Alk in the Drosophila system, there were few insights into the normal structure of Alk and information on the function of this novel RTK was lacking.

Using Drosophila as our model system we were able to show that Alk-mediated signalling drives muscle fusion in the developing embryonic gut. As a result of this work we have been able to show that the Drosophila Alk RTK is the receptor, or part of a receptor complex, responsible for binding the recently identified Jeb protein. Jeb is a novel extracellular signalling molecule which is not transcribed in the visceral mesoderm itself, but in the neighboring somatic mesoderm, and is then specifically taken up by the visceral mesoderm cells. Jeb has been shown to be required for visceral mesoderm migration and differentiation.
Analysis of Jeb and Alk localization reveals a complex interplay between Jeb and the Alk positive visceral mesoderm. In wild-type embryos Jeb is expressed in cells ventral to the Alk positive visceral mesoderm clusters, and at the sites of contact between these cells a clear co-localisation of Jeb and Alk can be observed. The Alk positive visceral mesoderm cells, which contact the Jeb secreting mesoderm, respond to Jeb by differentiating. Together Jeb and Alk signal through an ERK mediated signalling pathway to drive specification of a particular cell type (founder cells) and subsequent fusion of the visceral mesoderm muscle cells. In the absence of either the Jeb ligand or Alk receptor tyrosine kinase function there is a critical failure in the fusion process within the visceral mesoderm. The targets of Jeb induced Alk-mediated signalling include the fusion determinant Duf/Kirre, together with the T-box transcription factor org-1, which explain the muscle fusion defects found Alk mutant animals [2-4].
Presently we continue to work on the signal transduction pathways regulated by Alk, and on understanding how these molecules function during developmental processes such as muscle development. Our goal is to map these basic mechanisms in Drosophila, which is less complex than mouse or human, and therefore aid n laying the basic groundwork for understanding these fundamental processes in higher organisms such as ourselves.

References:
1. Freeman M: Developmental biology: partners united. Nature 2003, 425:468-469.
2. Stute C, Schimmelpfeng K, Renkawitz-Pohl R, Palmer RH, Holz A: Myoblast determination in the somatic and visceral mesoderm depends on Notch signalling as well as on milliways(mili(Alk)) as receptor for Jeb signalling. Development 2004, 131:743-754.
3. Lee HH, Norris A, Weiss JB, Frasch M: Jelly belly protein activates the receptor tyrosine kinase Alk to specify visceral muscle pioneers. Nature 2003, 425:507-512.
4. Englund C, Lorén CE, Grabbe C, Varshney GK, Deleuil F, Hallberg B, Palmer RH: Jeb signals via the DAlk receptor tyrosine kinase to drive visceral muscle fusion. Nature 2003, 425:512-516.