Insulin Prohormone Processing, Distribution, and Relation to Metabolism in<i>Aplysia californica</i>

Floyd, Philip D.; Li, Lingjun; Rubakhin, Stanislav S.; Sweedler, Jonathan V.; Horn, Charles C.; Kupfermann, Irving; Alexeeva, Vera; Ellis, Timothy A.; Dembrow, Nikolai C.; Weiss, Klaudiusz R.; Vilim, Ferdinand S.

doi:10.1523/jneurosci.19-18-07732.1999

Cited by 116 publications

(107 citation statements)

References 42 publications

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“…In contrast, invertebrate insulin family members are more variable and serve in neuronal signaling, memory, reproduction, growth, and metabolism (8,9). In molluscs, insulins are primarily expressed in neuroendocrine cells, including neurons and cerebral ganglia (9,10). Molluscan and most other invertebrate insulins differ from the vertebrate hormone in containing two additional cysteines (one in each chain) that are assumed to form an additional disulfide between the A and B chain (9).…”

mentioning

confidence: 99%

Specialized insulin is used for chemical warfare by fish-hunting cone snails

Safavi-Hemami

Gajewiak

Karanth

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

147

173

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More than 100 species of venomous cone snails (genus Conus) are highly effective predators of fish. The vast majority of venom components identified and functionally characterized to date are neurotoxins specifically targeted to receptors, ion channels, and transporters in the nervous system of prey, predators, or competitors. Here we describe a venom component targeting energy metabolism, a radically different mechanism. Two fish-hunting cone snails, Conus geographus and Conus tulipa, have evolved specialized insulins that are expressed as major components of their venoms. These insulins are distinctive in having much greater similarity to fish insulins than to the molluscan hormone and are unique in that posttranslational modifications characteristic of conotoxins (hydroxyproline, γ-carboxyglutamate) are present. When injected into fish, the venom insulin elicits hypoglycemic shock, a condition characterized by dangerously low blood glucose. Our evidence suggests that insulin is specifically used as a weapon for prey capture by a subset of fish-hunting cone snails that use a net strategy to capture prey. Insulin appears to be a component of the nirvana cabal, a toxin combination in these venoms that is released into the water to disorient schools of small fish, making them easier to engulf with the snail's distended false mouth, which functions as a net. If an entire school of fish simultaneously experiences hypoglycemic shock, this should directly facilitate capture by the predatory snail.insulin shock | cone snails | conotoxins | nirvana cabal | venom

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mentioning

confidence: 99%

Specialized insulin is used for chemical warfare by fish-hunting cone snails

Safavi-Hemami

Gajewiak

Karanth

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

147

173

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“…In addition to Drosophila IPCs, insulin-producing neurons have also been demonstrated in other insects (11,12), molluscs (13,14), nematodes (15), protochordates (16), and urochordates (17), suggesting that an ancestral IPC type might have been neuronal. In contrast, insulin in mammals is produced by the endoderm-derived endocrine pancreas (18,19).…”

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confidence: 99%

Conserved role for the Drosophila Pax6 homolog Eyeless in differentiation and function of insulin-producing neurons

Clements

Hens²,

Francis³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Insulin/insulin-like growth factor (IGF) signaling constitutes an evolutionarily conserved pathway that controls growth, energy homeostasis, and longevity. In Drosophila melanogaster, key components of this pathway are the insulin-like peptides (Dilps). The major source of Dilps is a cluster of large neurons in the brain, the insulin-producing cells (IPCs). The genetic control of IPC development and function is poorly understood. Here, we demonstrate that the Pax6 homolog Eyeless is required in the IPCs to control their differentiation and function. Loss of eyeless results in phenotypes associated with loss of insulin signaling, including decreased animal size and increased carbohydrate levels in larval hemolymph. We show that mutations in eyeless lead to defective differentiation and morphologically abnormal IPCs. We also demonstrate that Eyeless controls IPC function by the direct transcriptional control of one of the major Dilps, dilp5. We propose that Eyeless has an evolutionarily conserved role in IPCs with remarkable similarities to the role of vertebrate Pax6 in ␤ cells of the pancreas.energy homeostasis ͉ evolutionarily conserved ͉ growth control ͉ target gene ͉ transcription factor

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“…Even with the wealth of genomic information available, direct biochemical measures are often required to determine the presence and particular form of the neuropeptides present throughout the central nervous system (CNS). Direct MALDI MS analysis of molluscan and insect neurons [1][2][3][4][5][6][7][8][9][10][11][12][13], connective nerve tissues [14], and even single peptidergic vesicles [15] provides information about gene products and their processing to bioactive neuropeptides. Mass profiling individually isolated neurons is the most common method for obtaining spatial information such as the cell-specific distribution of peptides within brain regions known as ganglia.…”

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confidence: 99%

Spatial profiling invertebrate ganglia using MALDI MS

Kruse

Sweedler

2003

J. Am. Soc. Mass Spectrom.

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108

100

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The ability of MALDI TOF MS to spatially map peptides and proteins directly from a tissue is an exciting advance to imaging mass spectrometry. Recent advances in instrumentation for MS have resulted in instruments capable of achieving several micron spatial resolution while acquiring high-resolution mass spectra. Currently, the ability to obtain high quality mass spectrometric images depends on sample preparation protocols that often result in limited spatial resolution. A number of sample preparation and matrix deposition protocols are evaluated for spatial profiling of Aplysia californica exocrine gland and neuronal tissues. Such samples are different from mammalian tissues, but make good targets for method optimization because of the wealth of biochemical information available on neuropeptide processing and distribution. Electrospray matrix deposition and a variety of freezing methods have been found to be optimum for these invertebrate tissues,

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Insulin Prohormone Processing, Distribution, and Relation to Metabolism inAplysia californica

Cited by 116 publications

References 42 publications

Specialized insulin is used for chemical warfare by fish-hunting cone snails

Specialized insulin is used for chemical warfare by fish-hunting cone snails

Conserved role for the Drosophila Pax6 homolog Eyeless in differentiation and function of insulin-producing neurons

Spatial profiling invertebrate ganglia using MALDI MS

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