Expression of the Lhx genes apterous and lim1 in an errant polychaete: implications for bilaterian appendage evolution, neural development, and muscle diversification

Abstract

BackgroundArthropod and vertebrate appendages appear to have evolved via parallel co-option of a plesiomorphic gene regulatory network. Our previous work implies that annelids evolved unrelated appendage-forming mechanisms; we therefore found no support for homology of parapodia and arthropodia at the level of the whole appendage. We expand on that study here by asking whether expression of the LIM homeobox (Lhx) genes apterous and lim1 in the annelid Neanthes arenaceodentata supports homology of the dorsal branches as well as the proximodistal axes of parapodia and arthropodia. In addition, we explore whether the neural expression of apterous and lim1 in Neanthes supports the putative ancestral function of the Lhx gene family in regulating the differentiation and maintenance of neuronal subtypes.ResultsBoth genes exhibit continuous expression in specific portions of the developing central nervous system, from hatching to at least the 13-chaetiger stage. For example, nerve cord expression occurs in segmentally iterated patterns consisting of diffuse sets of many lim1-positive cells and comparatively fewer, clustered pairs of apterous-positive cells. Additionally, continuous apterous expression is observed in presumed neurosecretory ganglia of the posterior brain, while lim1 is continuously expressed in stomatogastric ganglia of the anterior brain. apterous is also expressed in the jaw sacs, dorsal parapodial muscles, and a presumed pair of cephalic sensory organs, whereas lim1 is expressed in multiple pharyngeal ganglia, the segmental peripheral nervous system, neuropodial chaetal sac muscles, and parapodial ligules.ConclusionsThe early and persistent nervous system expression of apterous and lim1 in Neanthes juveniles supports conservation of Lhx function in bilaterian neural differentiation and maintenance. Our results also suggest that diversification of parapodial muscle precursors involves a complementary LIM code similar to those generating distinct neuronal identities in fly and mouse nerve cords. Expression of apterous and lim1 in discrete components of developing parapodia is intriguing but does not map to comparable expression of these genes in developing arthropod appendages. Thus, annelid and arthropod appendage development apparently evolved, in part, via distinct co-option of the neuronal regulatory architecture. These divergent patterns of apterous and lim1 activity seemingly reflect de novo origins of parapodia and arthropodia, although we discuss alternative hypotheses.

The pre-vertebrate origins of neurogenic placodes

“…After removing ambiguously aligned amino acids with Gblocks 38 , the 118-sequence data set (including five outgroup sequences for Ciona Glutamate, Smoothened, Frizzled and cAMP receptor-like proteins) contained 373 positions (including gaps). For optimal tree searches and measurement of nodal support, minimum evolution (ME), maximum likelihood (ML) and Bayesian inference (BI) criteria were used 39 .…”

The evolution of insect germline specification strategies

“…2). However, representatives of closely related crustacean [58] and collembolan [59] clades apparently produce maternal germ plasm, and there is even some evidence for a maternal germline determinant in the apterygote insect Thermobia [60] (Fig. 2).…”

“…Blue boxes indicate osk ortholog in the genome [5,7,9,11,12], a box with a question mark indicates that no large scale genomic or transcriptomic data has been published to help determine whether osk is present, those without indications appear to lack osk based on its absence in large scale sequencing projects [8,39,51–53]. Genus names in blue are those in which maternal provision mode is used [3,7,9,58,63], while those in red use zygotic induction [13,31,40,41,56,57,64]. Those in purple indicate that the presence of maternal provision has been proposed and/or independently derived [49,59,60].…”

LHX6 inhibits breast cancer cell proliferation and invasion via repression of the Wnt/β-catenin signaling pathway

“…Epigenetic alterations of tumor-suppressor genes, including promoter methylation and histone modification, are critical in the initiation and progression of multiple types of cancer, including breast cancer. Various studies have shown that LHX proteins are involved in cytoskeletal organization, organ development and oncogenesis (15,16). In the present study, increased expression of LHX6 was found to inhibit breast cancer cell growth and invasion.…”