Cloning of prodynorphin cDNAs from the brain of Australian and African lungfish: Implications for the evolution of the prodynorphin gene

Robert M. Dores, Cristina Sollars, Stephanie Lecaude, Jenny Lee, Phillip Danielson, Jasem Alrubaian, Isabelle Lihrman, J. M P Joss, Hubert Vaudry

Research output: Contribution to journalArticleResearchpeer-review

Abstract

In mammals the opioids Met-enkephalin and Leu-enkephalin are derived from a common precursor, proenkephalin, and as a result these neuropeptides are colocalized in enkephalinergic neurons. The mammalian scheme for enkephalinergic networks is not universal for all classes of sarcopterygian vertebrates. In an earlier study, distinct Met- and Leu-enkephalin-positive neurons were detected in the central nervous system (CNS) of the African lungfish, Protopterus annectens. More recently, characterization of proenkephalin cDNAs separately cloned from the CNS of P. annectens and the Australian lungfish, Neoceratodus forsteri, revealed that the proenkephalin gene in these species encodes only Met-enkephalin-related opioids. In the current study a fulllength prodynorphin cDNA (accession No. AY 445637) was cloned and sequenced from the CNS of N. forsteri. In addition to encoding α-neoendorphin, dynorphin A and dynorphin B sequences unique to the lungfish, two Leuenkephalin sequences, flanked by paired basic amino acid proteolytic cleavage sites, were detected in this precursor. The partial sequence of a P. annectens prodynorphin cDNA (accession No. AY445638) also encoded a Leu-enkephalin sequence and a novel YGGFF sequence. The presence of the Leu-enkephalin sequence in the lungfish prodynorphin precursors would explain the origin of the distinct Leu-enkephalin-positive neurons found in the African lungfish CNS. The realization that Met-enkephalin and Leu-enkephalin can be derived from distinct opioid-coding precursor genes calls into question the interpretation of comparative immunohistochemical studies that have mapped 'enkephalinergic' networks in non-mammalian vertebrates.

LanguageEnglish
Pages185-196
Number of pages12
JournalNeuroendocrinology
Volume79
Issue number4
DOIs
Publication statusPublished - 2004

Fingerprint

Leucine Enkephalin
Organism Cloning
Methionine Enkephalin
Complementary DNA
Brain
Central Nervous System
Opioid Analgesics
Genes
Neurons
Vertebrates
Dynorphins
Basic Amino Acids
Neuropeptides
preproenkephalin
Mammals
proenkephalin

Keywords

  • α-neoendorphin
  • Dynorphins
  • Enkephalins
  • Fish
  • Molecular neuroendocrinology
  • Morphinomimetic peptides

Cite this

Dores, Robert M. ; Sollars, Cristina ; Lecaude, Stephanie ; Lee, Jenny ; Danielson, Phillip ; Alrubaian, Jasem ; Lihrman, Isabelle ; Joss, J. M P ; Vaudry, Hubert. / Cloning of prodynorphin cDNAs from the brain of Australian and African lungfish : Implications for the evolution of the prodynorphin gene. In: Neuroendocrinology. 2004 ; Vol. 79, No. 4. pp. 185-196.
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abstract = "In mammals the opioids Met-enkephalin and Leu-enkephalin are derived from a common precursor, proenkephalin, and as a result these neuropeptides are colocalized in enkephalinergic neurons. The mammalian scheme for enkephalinergic networks is not universal for all classes of sarcopterygian vertebrates. In an earlier study, distinct Met- and Leu-enkephalin-positive neurons were detected in the central nervous system (CNS) of the African lungfish, Protopterus annectens. More recently, characterization of proenkephalin cDNAs separately cloned from the CNS of P. annectens and the Australian lungfish, Neoceratodus forsteri, revealed that the proenkephalin gene in these species encodes only Met-enkephalin-related opioids. In the current study a fulllength prodynorphin cDNA (accession No. AY 445637) was cloned and sequenced from the CNS of N. forsteri. In addition to encoding α-neoendorphin, dynorphin A and dynorphin B sequences unique to the lungfish, two Leuenkephalin sequences, flanked by paired basic amino acid proteolytic cleavage sites, were detected in this precursor. The partial sequence of a P. annectens prodynorphin cDNA (accession No. AY445638) also encoded a Leu-enkephalin sequence and a novel YGGFF sequence. The presence of the Leu-enkephalin sequence in the lungfish prodynorphin precursors would explain the origin of the distinct Leu-enkephalin-positive neurons found in the African lungfish CNS. The realization that Met-enkephalin and Leu-enkephalin can be derived from distinct opioid-coding precursor genes calls into question the interpretation of comparative immunohistochemical studies that have mapped 'enkephalinergic' networks in non-mammalian vertebrates.",
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Dores, RM, Sollars, C, Lecaude, S, Lee, J, Danielson, P, Alrubaian, J, Lihrman, I, Joss, JMP & Vaudry, H 2004, 'Cloning of prodynorphin cDNAs from the brain of Australian and African lungfish: Implications for the evolution of the prodynorphin gene', Neuroendocrinology, vol. 79, no. 4, pp. 185-196. https://doi.org/10.1159/000078100

Cloning of prodynorphin cDNAs from the brain of Australian and African lungfish : Implications for the evolution of the prodynorphin gene. / Dores, Robert M.; Sollars, Cristina; Lecaude, Stephanie; Lee, Jenny; Danielson, Phillip; Alrubaian, Jasem; Lihrman, Isabelle; Joss, J. M P; Vaudry, Hubert.

In: Neuroendocrinology, Vol. 79, No. 4, 2004, p. 185-196.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Cloning of prodynorphin cDNAs from the brain of Australian and African lungfish

T2 - Neuroendocrinology

AU - Dores, Robert M.

AU - Sollars, Cristina

AU - Lecaude, Stephanie

AU - Lee, Jenny

AU - Danielson, Phillip

AU - Alrubaian, Jasem

AU - Lihrman, Isabelle

AU - Joss, J. M P

AU - Vaudry, Hubert

PY - 2004

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AB - In mammals the opioids Met-enkephalin and Leu-enkephalin are derived from a common precursor, proenkephalin, and as a result these neuropeptides are colocalized in enkephalinergic neurons. The mammalian scheme for enkephalinergic networks is not universal for all classes of sarcopterygian vertebrates. In an earlier study, distinct Met- and Leu-enkephalin-positive neurons were detected in the central nervous system (CNS) of the African lungfish, Protopterus annectens. More recently, characterization of proenkephalin cDNAs separately cloned from the CNS of P. annectens and the Australian lungfish, Neoceratodus forsteri, revealed that the proenkephalin gene in these species encodes only Met-enkephalin-related opioids. In the current study a fulllength prodynorphin cDNA (accession No. AY 445637) was cloned and sequenced from the CNS of N. forsteri. In addition to encoding α-neoendorphin, dynorphin A and dynorphin B sequences unique to the lungfish, two Leuenkephalin sequences, flanked by paired basic amino acid proteolytic cleavage sites, were detected in this precursor. The partial sequence of a P. annectens prodynorphin cDNA (accession No. AY445638) also encoded a Leu-enkephalin sequence and a novel YGGFF sequence. The presence of the Leu-enkephalin sequence in the lungfish prodynorphin precursors would explain the origin of the distinct Leu-enkephalin-positive neurons found in the African lungfish CNS. The realization that Met-enkephalin and Leu-enkephalin can be derived from distinct opioid-coding precursor genes calls into question the interpretation of comparative immunohistochemical studies that have mapped 'enkephalinergic' networks in non-mammalian vertebrates.

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KW - Dynorphins

KW - Enkephalins

KW - Fish

KW - Molecular neuroendocrinology

KW - Morphinomimetic peptides

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U2 - 10.1159/000078100

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