Characterization of a native angiotensin from an anciently diverged serine protease inhibitor in lamprey

Wong, Marty Kwok‐Shing; Takei, Yoshiyuki

doi:10.1530/joe-10-0422

Cited by 25 publications

(15 citation statements)

References 42 publications

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“…Considerable amounts of data have demonstrated that, in addition to the two main effector peptides of the brain RAS, ANG II and ANG III, ANG IV, and to a lesser extend ANG 1-7 are implicated in various physiological functions notably body fluid homeostasis and blood pressure regulation but also pituitary hormone release, thermoregulation, sexual, eating and locomotor behaviors, metabolism, learning, and memory (28,29,35,36,42,54). Compared with the central actions of the RAS on cardiovascular regulations, studies on the ventilatory effect are sparse and only the action of ANG II has been explored with conflicting results in mammals (13,31,33,37,41,50).The RAS has an ancient evolutionary history and most of its components are present in lampreys, elasmobranchs, and teleosts (29,32,38,46,53). In contrast to the well-known peripheral cardiovascular and osmoregulatory effects of ANG II (5,32,45), studies on the central action are sparse in fishes.…”

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confidence: 99%

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Central ventilatory and cardiovascular actions of angiotensin peptides in trout

Lancien

Wong

Arab

et al. 2012

American Journal of Physiology-Regulatory, Integrative and Comp

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In the brains of teleosts, angiotensin II (ANG II), one of the main effector peptides of the renin-angiotensin system, is implicated in various physiological functions notably body fluid and electrolyte homeostasis and cardiovascular regulation, but nothing is known regarding the potential action of ANG II and other angiotensin derivatives on ventilation. Consequently, the goal of the present study was to determine possible ventilatory and cardiovascular effects of intracerebroventricular injection of picomole doses (5-100 pmol) of trout [Asn(1)]-ANG II, [Asp(1)]-ANG II, ANG III, ANG IV, and ANG 1-7 into the third ventricle of unanesthetized trout. The central actions of these peptides were also compared with their ventilatory and cardiovascular actions when injected peripherally. Finally, we examined the presence of [Asn(1)]-ANG II, [Asp(1)]-ANG II, ANG III, and ANG IV in the brain and plasma using radioimmunoassay coupled with high-performance liquid chromatography. After intracerebroventricular injection, [Asn(1)]-ANG II and [Asp(1)]-ANG II two ANG IIs, elevated the total ventilation through a selective stimulatory action on the ventilation amplitude. However, the hyperventilatory effect of [Asn(1)]-ANG II was threefold higher than the effect of [Asp(1)]-ANG II at the 50-pmol dose. ANG III, ANG IV, and ANG 1-7 were without effect. In addition, ANG IIs and ANG III increased dorsal aortic blood pressure (P(DA)) and heart rate (HR). After intra-arterial injections, none of the ANG II peptides affected the ventilation but [Asn(1)]-ANG II, [Asp(1)]-ANG II, and ANG III elevated P(DA) (50 pmol: +80%, +58% and +48%, respectively) without significant decrease in HR. In brain tissue, comparable amounts of [Asn(1)]-ANG II and [Asp(1)]-ANG II were detected (ca. 40 fmol/mg brain tissue), but ANG III was not detected, and the amount of ANG IV was about eightfold lower than the content of the ANG IIs. In plasma, ANG IIs were also the major angiotensins (ca. 110 fmol/ml plasma), while significant but lower amounts of ANG III and ANG IV were present in plasma. In conclusion, our study suggests that the two ANG II isoforms produced within the brain may act as a neurotransmitter and/or neuromodulator to regulate the cardioventilatory functions in trout. In the periphery, two ANG IIs and their COOH-terminal peptides may act as a circulating hormone preferentially involved in cardiovascular regulations.

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“…The RAS has an ancient evolutionary history and most of its components are present in lampreys, elasmobranchs, and teleosts (29,32,38,46,53). In contrast to the well-known peripheral cardiovascular and osmoregulatory effects of ANG II (5,32,45), studies on the central action are sparse in fishes.…”

mentioning

confidence: 99%

Central ventilatory and cardiovascular actions of angiotensin peptides in trout

Lancien

Wong

Arab

et al. 2012

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Receptor internalization is triggered by ligand concentrations comparable to those in mammals and with similar kinetics [36]. Fourthly, injection of lamprey angiotensin II at 100–1000 pmol/kg provokes a cardiovascular response in cannulated conscious lampreys [37]. Blood pressure, however, is transiently decreased by the peptide, pointing to differences in pressure control mechanisms of lampreys and mammals.…”

Section: Discussionmentioning

confidence: 94%

Origin of Serpin-Mediated Regulation of Coagulation and Blood Pressure

2014

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Vertebrates evolved an endothelium-lined hemostatic system and a pump-driven pressurized circulation with a finely-balanced coagulation cascade and elaborate blood pressure control over the past 500 million years. Genome analyses have identified principal components of the ancestral coagulation system, however, how this complex trait was originally regulated is largely unknown. Likewise, little is known about the roots of blood pressure control in vertebrates. Here we studied three members of the serpin superfamily that interfere with procoagulant activity and blood pressure of lampreys, a group of basal vertebrates. Angiotensinogen from these jawless fish was found to fulfill a dual role by operating as a highly selective thrombin inhibitor that is activated by heparin-related glycosaminoglycans, and concurrently by serving as source of effector peptides that activate type 1 angiotensin receptors. Lampreys, uniquely among vertebrates, thus use angiotensinogen for interference with both coagulation and osmo- and pressure regulation. Heparin cofactor II from lampreys, in contrast to its paralogue angiotensinogen, is preferentially activated by dermatan sulfate, suggesting that these two serpins affect different facets of thrombin’s multiple roles. Lampreys also express a lineage-specific serpin with anti-factor Xa activity, which demonstrates that another important procoagulant enzyme is under inhibitory control. Comparative genomics suggests that orthologues of these three serpins were key components of the ancestral hemostatic system. It appears that, early in vertebrate evolution, coagulation and osmo- and pressure regulation crosstalked through antiproteolytically active angiotensinogen, a feature that was lost during vertebrate radiation, though in gnathostomes interplay between these traits is effective.

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“…47 Serine proteases promote cartilage destruction in osteoarthritis. 48,49 Here, greater expression of CSF angiotensinogen in CSM-affected dogs, which had marked osteoarthritic changes of their cervical vertebrae, might be a compensatory increase in an attempt to inhibit the excess of protease activity that occurs in osteoarthritis.…”

Section: Discussionmentioning

confidence: 99%

Proteomic Analysis of Cerebrospinal Fluid in Canine Cervical Spondylomyelopathy

Martín-Vaquero

Costa

Allen

et al. 2015

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Study Design Prospective study. Objective To identify proteins with differential expression in the cerebrospinal fluid (CSF) from 15 clinically normal (control) dogs and 15 dogs with cervical spondylomyelopathy (CSM). Summary of Background Data Canine CSM is a spontaneous, chronic, compressive cervical myelopathy similar to human cervical spondylotic myelopathy. There is a limited knowledge of the molecular mechanisms underlying these conditions. Differentially expressed CSF proteins may contribute with novel information about the disease pathogenesis in both dogs and humans. Methods Protein separation was performed with two-dimensional electrophoresis. A Student’s t-test was used to detect significant differences between groups (P < 0.05). Three comparisons were made: 1) control versus CSM-affected dogs, 2) control versus non-corticosteroid treated CSM-affected dogs, and 3) non-corticosteroid treated CSM-affected versus corticosteroid treated CSM-affected dogs. Protein spots exhibiting at least a statistically significant 1.25-fold change between groups were selected for subsequent identification with capillary-liquid chromatography tandem mass spectrometry. Results A total of 96 spots had a significant average change of at least 1.25-fold in one of the three comparisons. Compared to the CSF of control dogs, CSM-affected dogs demonstrated increased CSF expression of eight proteins including vitamin D-binding protein, gelsolin, creatine kinase B-type, angiotensinogen, alpha-2-HS-glycoprotein, SPARC, calsyntenin-1, and complement C3, and decreased expression of pigment epithelium-derived factor, prostaglandin-H2 D-isomerase, apolipoprotein E, and clusterin. In the CSF of CSM-affected dogs, corticosteroid treatment increased the expression of haptoglobin, transthyretin isoform 2, cystatin C-like, apolipoprotein E, and clusterin, and decreased the expression of angiotensinogen, alpha-2-HS-glycoprotein, and gelsolin. Conclusions Many of the differentially expressed proteins are associated with damaged neural tissue, bone turnover, and/or compromised blood-spinal cord barrier. The knowledge of the protein changes that occur in CSM and upon corticosteroid treatment of CSM-affected patients will aid in further understanding the pathomechanisms underlying this disease.

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Characterization of a native angiotensin from an anciently diverged serine protease inhibitor in lamprey

Cited by 25 publications

References 42 publications

Central ventilatory and cardiovascular actions of angiotensin peptides in trout

Central ventilatory and cardiovascular actions of angiotensin peptides in trout

Origin of Serpin-Mediated Regulation of Coagulation and Blood Pressure

Proteomic Analysis of Cerebrospinal Fluid in Canine Cervical Spondylomyelopathy

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