PACAP/GCGa Is an Important Modulator of the Amphioxus CNS-Hatschek’s Pit Axis, the Homolog of the Vertebrate Hypothalamic-Pituitary Axis in the Basal Chordates

The Hatschek’s pit in the cephalochordate amphioxus, an invertebrate deuterostome basal to chordates is suggested to be the functional homolog structure of the vertebrate adenohypophysis based on anatomy and expression of homologous neuroendocrine genes. However, the endocrine potential of the cepha...

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Main Authors: Jason S. W. On, Liuru Su, Hong Shen, Aloysius W. R. Arokiaraj, João C. R. Cardoso, Guang Li, Billy K. C. Chow
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Endocrinology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fendo.2022.850040/full
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author Jason S. W. On
Liuru Su
Liuru Su
Hong Shen
Aloysius W. R. Arokiaraj
João C. R. Cardoso
Guang Li
Billy K. C. Chow
author_facet Jason S. W. On
Liuru Su
Liuru Su
Hong Shen
Aloysius W. R. Arokiaraj
João C. R. Cardoso
Guang Li
Billy K. C. Chow
author_sort Jason S. W. On
collection DOAJ
description The Hatschek’s pit in the cephalochordate amphioxus, an invertebrate deuterostome basal to chordates is suggested to be the functional homolog structure of the vertebrate adenohypophysis based on anatomy and expression of homologous neuroendocrine genes. However, the endocrine potential of the cephalochordate Hatschek’s pit remains to be demonstrated as well as the physiological actions of the secreted neuropeptides. In this study, we have explored the distribution and characterize the potential function of the amphioxus PACAP/GCG precursor, which is the ortholog of the hypothalamic PACAP neuropeptide in vertebrates. In amphioxi, two PACAP/GCG transcripts PACAP/GCGa and PACAP/GCGbc that are alternative isoforms of a single gene with different peptide coding potentials were isolated. Immunofluorescence staining detected their expression around the nucleus of Rohde, supporting that this structure may be homologous of the neurosecretory cells of the vertebrate hypothalamus where abundant PACAP is found. PACAP/GCGa was also detected in the infundibulum‐like downgrowth approaching the Hatschek’s pit, indicating diffusion of PACAP/GCGa from the CNS to the pit via the infundibulum‐like downgrowth. Under a high salinity challenge, PACAP/GCGa was upregulated in amphioxi head and PACAP/GCGa treatment increased expression of GHl in Hatschek’s pit in a dose-dependent manner, suggesting that PACAP/GCGa may be involved in the regulation of GHl via hypothalamic-pituitary (HP)-like axis similar as in the vertebrates. Our results support that the amphioxus Hatschek’s pit is likely to be the functional homolog of pituitary gland in vertebrates.
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spelling doaj.art-a4c14f8045614860b8f5addbed1eca992022-12-22T02:40:44ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922022-04-011310.3389/fendo.2022.850040850040PACAP/GCGa Is an Important Modulator of the Amphioxus CNS-Hatschek’s Pit Axis, the Homolog of the Vertebrate Hypothalamic-Pituitary Axis in the Basal ChordatesJason S. W. On0Liuru Su1Liuru Su2Hong Shen3Aloysius W. R. Arokiaraj4João C. R. Cardoso5Guang Li6Billy K. C. Chow7School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, ChinaSchool of Biological Sciences, The University of Hong Kong, Hong Kong SAR, ChinaState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaSchool of Biological Sciences, The University of Hong Kong, Hong Kong SAR, ChinaSchool of Biological Sciences, The University of Hong Kong, Hong Kong SAR, ChinaComparative Endocrinology and Integrative Biology, Centre of Marine Sciences, Universidade do Algarve, Faro, PortugalState Key Laboratory of Cellular Stress Biology, School of Life Sciences, Xiamen University, Xiamen, ChinaSchool of Biological Sciences, The University of Hong Kong, Hong Kong SAR, ChinaThe Hatschek’s pit in the cephalochordate amphioxus, an invertebrate deuterostome basal to chordates is suggested to be the functional homolog structure of the vertebrate adenohypophysis based on anatomy and expression of homologous neuroendocrine genes. However, the endocrine potential of the cephalochordate Hatschek’s pit remains to be demonstrated as well as the physiological actions of the secreted neuropeptides. In this study, we have explored the distribution and characterize the potential function of the amphioxus PACAP/GCG precursor, which is the ortholog of the hypothalamic PACAP neuropeptide in vertebrates. In amphioxi, two PACAP/GCG transcripts PACAP/GCGa and PACAP/GCGbc that are alternative isoforms of a single gene with different peptide coding potentials were isolated. Immunofluorescence staining detected their expression around the nucleus of Rohde, supporting that this structure may be homologous of the neurosecretory cells of the vertebrate hypothalamus where abundant PACAP is found. PACAP/GCGa was also detected in the infundibulum‐like downgrowth approaching the Hatschek’s pit, indicating diffusion of PACAP/GCGa from the CNS to the pit via the infundibulum‐like downgrowth. Under a high salinity challenge, PACAP/GCGa was upregulated in amphioxi head and PACAP/GCGa treatment increased expression of GHl in Hatschek’s pit in a dose-dependent manner, suggesting that PACAP/GCGa may be involved in the regulation of GHl via hypothalamic-pituitary (HP)-like axis similar as in the vertebrates. Our results support that the amphioxus Hatschek’s pit is likely to be the functional homolog of pituitary gland in vertebrates.https://www.frontiersin.org/articles/10.3389/fendo.2022.850040/fullCNS-Hatschek’s pit axishypothalamic-pituitary axisamphioxusPACAP/GCGGHl
spellingShingle Jason S. W. On
Liuru Su
Liuru Su
Hong Shen
Aloysius W. R. Arokiaraj
João C. R. Cardoso
Guang Li
Billy K. C. Chow
PACAP/GCGa Is an Important Modulator of the Amphioxus CNS-Hatschek’s Pit Axis, the Homolog of the Vertebrate Hypothalamic-Pituitary Axis in the Basal Chordates
Frontiers in Endocrinology
CNS-Hatschek’s pit axis
hypothalamic-pituitary axis
amphioxus
PACAP/GCG
GHl
title PACAP/GCGa Is an Important Modulator of the Amphioxus CNS-Hatschek’s Pit Axis, the Homolog of the Vertebrate Hypothalamic-Pituitary Axis in the Basal Chordates
title_full PACAP/GCGa Is an Important Modulator of the Amphioxus CNS-Hatschek’s Pit Axis, the Homolog of the Vertebrate Hypothalamic-Pituitary Axis in the Basal Chordates
title_fullStr PACAP/GCGa Is an Important Modulator of the Amphioxus CNS-Hatschek’s Pit Axis, the Homolog of the Vertebrate Hypothalamic-Pituitary Axis in the Basal Chordates
title_full_unstemmed PACAP/GCGa Is an Important Modulator of the Amphioxus CNS-Hatschek’s Pit Axis, the Homolog of the Vertebrate Hypothalamic-Pituitary Axis in the Basal Chordates
title_short PACAP/GCGa Is an Important Modulator of the Amphioxus CNS-Hatschek’s Pit Axis, the Homolog of the Vertebrate Hypothalamic-Pituitary Axis in the Basal Chordates
title_sort pacap gcga is an important modulator of the amphioxus cns hatschek s pit axis the homolog of the vertebrate hypothalamic pituitary axis in the basal chordates
topic CNS-Hatschek’s pit axis
hypothalamic-pituitary axis
amphioxus
PACAP/GCG
GHl
url https://www.frontiersin.org/articles/10.3389/fendo.2022.850040/full
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