Expression and distribution of octopus gonadotropin‐releasing hormone in the central nervous system and peripheral organs of the octopus (<i>Octopus vulgaris</i>) by in situ hybridization and immunohistochemistry

Tello

General and Comparative Endocrinology

et al. 2008

106

Successful reproduction in vertebrates depends upon the actions of gonadotropin-releasing hormone (GnRH). Despite the wide presence of GnRH in Phylum Chordata, GnRH has not been isolated in protostomes other than the common octopus. To provide information on the evolution of this critical hormone, we isolated the full-length cDNA of a GnRH-like molecule from the central nervous system of a gastropod mollusk, the sea hare Aplysia californica. The open reading frame of this cDNA encodes a protein of 147 amino acids. The molecular architecture of the deduced protein is highly homologous to that reported for the prepro-octopus GnRH (oct-GnRH) and consists of a putative signal peptide, a GnRH dodecapeptide, a downstream processing site, and a GnRH-associated peptide (GAP). The deduced amino acid sequence of the Aplysia GnRH (ap-GnRH) is QNYHFSNGWYAG and differs from oct-GnRH by only two amino acids. The transcript for ap-GnRH is widely expressed in the central nervous system (CNS), the ovotestis, and the atrial gland, an exocrine gland. Immunocytochemistry (ICC) using an antiserum against oct-GnRH detected immunoreactive neurons in all CNS ganglia examined, and the staining was abolished by the preadsorption of the antiserum with synthetic ap-GnRH. In sum, ap-GnRH sequence is the first gastropod GnRH-like molecule to be elucidated. Further, it represents one of the only two GnRH-like molecules found outside Phylum Chordata. These data refute the possibility that oct-GnRH arose singly in cephalopods by convergent evolution and provide valuable support for an ancient origin of GnRH during metazoan evolution.

Section: Discussionsupporting

confidence: 60%

Molecular cloning, expression pattern, and immunocytochemical localization of a gonadotropin-releasing hormone-like molecule in the gastropod mollusk, Aplysia californica

Tello

General and Comparative Endocrinology

et al. 2008

106

“…However, cells immunoreactive for GnRH have been identified in many metazoan lineages, often localized to neurons (reviewed in Rastogi et al, 2002;Gorbman and Sower, 2003), and a neuronally expressed GnRH peptide has been purified and sequenced in cephalopods (Iwakoshi et al, 2002;Iwakoshi-Ukena et al, 2004), indicating that GnRH-containing neurosecretory cells were present at least in the last common ancestor of bilaterians if not metazoans. In hemichordates, GnRH is found in specialized, probably exocrine neurosecretory cells of the epidermis (Cameron et al,'99) and has been suggested to act as a pheromone stimulating synchronized spawning (see also Gorbman and Sower, 2003).…”

Section: Evolution Of Gnrh-producing Neurosecretory Cells Derived Fromentioning

confidence: 99%

Evolutionary origins of vertebrate placodes: insights from developmental studies and from comparisons with other deuterostomes

2005

Ectodermal placodes comprise the adenohypophyseal, olfactory, lens, profundal, trigeminal, otic, lateral line, and epibranchial placodes. The first part of this review presents a brief overview of placode development. Placodes give rise to a variety of cell types and contribute to many sensory organs and ganglia of the vertebrate head. While different placodes differ with respect to location and derivative cell types, all appear to originate from a common panplacodal primordium, induced at the anterior neural plate border by a combination of mesodermal and neural signals and defined by the expression of Six1, Six4, and Eya genes. Evidence from mouse and zebrafish mutants suggests that these genes promote generic placodal properties such as cell proliferation, cell shape changes, and specification of neurons. The common developmental origin of placodes suggests that all placodes may have evolved in several steps from a common precursor. The second part of this review summarizes our current knowledge of placode evolution. Although placodes (like neural crest cells) have been proposed to be evolutionary novelties of vertebrates, recent studies in ascidians and amphioxus have proposed that some placodes originated earlier in the chordate lineage. However, while the origin of several cellular and molecular components of placodes (e.g., regionalized expression domains of transcription factors and some neuronal or neurosecretory cell types) clearly predates the origin of vertebrates, there is presently little evidence that these components are integrated into placodes in protochordates. A scenario is presented according to which all placodes evolved from an adenohypophyseal-olfactory protoplacode, which may have originated in the vertebrate ancestor from the anlage of a rostral neurosecretory organ (surviving as Hatschek's pit in present-day amphioxus).

J of Comparative Neurology

“…Some of these peptides are proposed to exist in the octopus. These include somatostatin (Feldman, 1986), FMRF-amide (Di Cosmo and Di Cristo, 1998;, gonadotropin-releasing hormone (Di Cosmo and Di Cristo, 1998;Iwakoshi-Ukena et al, 2004), galanin (Suzuki et al, 2000), neuropeptide Y (Suzuki et al, , 2003, calcitonin gene-related peptide , and corticotropin-releasing factor (Suzuki et al, 2003). These peptides have been localized in octopus by immunohistochemistry, mostly using antibodies against vertebrate-type peptides.…”

Section: Neurotransmitter-linked Molecules In Cephalopods and Vertebrmentioning

confidence: 99%

“…These peptides have been localized in octopus by immunohistochemistry, mostly using antibodies against vertebrate-type peptides. Except for FMRFamide (Loi and Tublitz, 1997) and gonadotropin-releasing hormone (Iwakoshi-Ukena et al, 2004), the chemical structures of these peptides in octopus are not exactly known. Since epitope composition appears relatively simple, such a small peptide may be structurally similar, if not identical, to each vertebrate counterpart.…”

Section: Neurotransmitter-linked Molecules In Cephalopods and Vertebrmentioning

confidence: 99%

First visualization of cholinergic cells and fibers by immunohistochemistry for choline acetyltransferase of the common type in the optic lobe and peduncle complex of Octopus vulgaris

D'Este

Kimura

Casini

et al. 2008

This study provides the first immunohistochemical evidence visualizing cholinergic octopus neurons containing choline acetyltransferase (ChAT), the synthetic enzyme of acetylcholine. Because the antiserum applied here was raised against a recombinant protein encoded by exons 7 and 8 of the rat gene for ChAT, and initially used for studies in mammals, to validate antibody specificity for the octopus counterpart enzyme we therefore used three methods. Immunoprecipitation using Pansorbin indicated that immunoreactive octopus brain molecules were capable of synthesizing acetylcholine. Western blot analysis after denatured gel electrophoresis of octopus brain extracts revealed a single band at Ϸ81 kDa. A gel slice containing the 81-kDa protein after native (nondenatured) gel electrophoresis exhibited high ChAT activity. All findings obtained with these three methods clearly indicated that the antiserum effectively recognizes octopus ChAT. The immunohistochemical use of the antiserum in the retina, optic lobe, and its neighboring peduncle complex detected enzyme-containing neuronal cell bodies in only two regions, the cell islands of the optic lobe medulla and the cortical layer of the posterior olfactory lobule. Immunoreactive fibers and probable nerve terminals were also found in the plexiform layer of the deep retina, within the stroma of the optic gland, and the neuropils of the optic lobe, peduncle lobe, and olfactory lobe. These results provide information on the morphology and distribution patterns of cholinergic neurons in the octopus visual system, a useful invertebrate model for learning and memory where the cholinergic system, as in higher vertebrates including mammals, plays an important role.