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OtherReview Article

Pituitary Adenylate Cyclase-Activating Polypeptide and Its Receptors: 20 Years after the Discovery

David Vaudry, Anthony Falluel-Morel, Steve Bourgault, Magali Basille, Delphine Burel, Olivier Wurtz, Alain Fournier, Billy K. C. Chow, Hitoshi Hashimoto, Ludovic Galas and Hubert Vaudry
Pharmacological Reviews September 2009, 61 (3) 283-357; DOI: https://doi.org/10.1124/pr.109.001370
David Vaudry
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Anthony Falluel-Morel
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Steve Bourgault
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Magali Basille
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Delphine Burel
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Olivier Wurtz
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Alain Fournier
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Billy K. C. Chow
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Hitoshi Hashimoto
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Ludovic Galas
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Hubert Vaudry
Institut National de la Santé et de la Recherche Médicale U413, European Institute for Peptide Research (Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23), Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); EA4310, University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., H.V.); INRS-Institut Armand-Frappier, Institut National de la Recherche Scientifique, Laval, Québec, Canada (S.B., A.F.); International Laboratory Samuel de Champlain (D.V., A.F.-M., S.B., M.B., D.B., O.W., A.F., H.V.); School of Biological Sciences, the University of Hong Kong, Pokfulam, Hong Kong (B.K.C.C.); Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences (H.H.), the Osaka-Hamamatsu Joint Research Center for Child Mental Development, Graduate School of Medicine (H.H.), and United Graduate School of Child Development, Osaka University, Kanazawa University, and Hamamatsu University School of Medicine, Osaka, Japan (H.H.); and Regional Platform for Cell Imaging (PRIMACEN), University of Rouen, Mont-Saint-Aignan, France (D.V., A.F.-M., S.B., M.B., D.B., O.W., L.G., H.V.)
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Abstract

Pituitary adenylate cyclase-activating polypeptide (PACAP) is a 38-amino acid C-terminally α-amidated peptide that was first isolated 20 years ago from an ovine hypothalamic extract on the basis of its ability to stimulate cAMP formation in anterior pituitary cells (Miyata et al., 1989. PACAP belongs to the vasoactive intestinal polypeptide (VIP)-secretin-growth hormone-releasing hormone-glucagon superfamily. The sequence of PACAP has been remarkably well conserved during evolution from protochordates to mammals, suggesting that PACAP is involved in the regulation of important biological functions. PACAP is widely distributed in the brain and peripheral organs, notably in the endocrine pancreas, gonads, respiratory and urogenital tracts. Characterization of the PACAP precursor has revealed the existence of a PACAP-related peptide, the activity of which remains unknown. Two types of PACAP binding sites have been characterized: type I binding sites exhibit a high affinity for PACAP and a much lower affinity for VIP, whereas type II binding sites have similar affinity for PACAP and VIP. Molecular cloning of PACAP receptors has shown the existence of three distinct receptor subtypes: the PACAP-specific PAC1-R, which is coupled to several transduction systems, and the PACAP/VIP-indifferent VPAC1-R and VPAC2-R, which are primarily coupled to adenylyl cyclase. PAC1-Rs are particularly abundant in the brain, the pituitary and the adrenal gland, whereas VPAC receptors are expressed mainly in lung, liver, and testis. The development of transgenic animal models and specific PACAP receptor ligands has strongly contributed to deciphering the various actions of PACAP. Consistent with the wide distribution of PACAP and its receptors, the peptide has now been shown to exert a large array of pharmacological effects and biological functions. The present report reviews the current knowledge concerning the pleiotropic actions of PACAP and discusses its possible use for future therapeutic applications.

  • α-MSH, α-melanocyte-stimulating hormone
  • AC, adenylyl cyclase
  • ARC, arcuate nucleus of the hypothalamus
  • Bcl-2, B-cell lymphoma 2
  • BDNF, brain-derived neurotrophic factor
  • cAMP, cyclic adenosine monophosphate
  • c-Jun, jun oncogene
  • CNS, central nervous system
  • CRE, cAMP responsive element
  • CREB, cAMP-responsive element-binding protein
  • CRH, corticotropin-releasing hormone
  • E, embryonic day
  • ECL, enterochromaffin-like
  • EGL, external granule cell layer
  • ERK, extracellular signal-regulated kinase
  • FSH, follicle-stimulating hormone
  • GH, growth hormone
  • GHRH, growth hormone-releasing hormone
  • GnRH, gonadotropin-releasing hormone
  • hCG, human chorionic gonadotropin
  • IGL, internal granule cell layer
  • IL, interleukin
  • JNK, c-Jun NH2-terminal kinase
  • kb, kilobase(s)
  • LH, luteinizing hormone
  • LI, like immunoreactivity
  • MAPK, mitogen-activated protein kinase
  • MEK, mitogen-activated protein kinase kinase
  • MIP, macrophage inflammatory protein
  • MSH, melanocyte-stimulating hormone
  • NMDA, N-methyl-d-aspartate
  • NO, nitric oxide
  • NPY, neuropeptide tyrosine
  • P, postnatal day
  • PAC1-R, PACAP-specific receptor
  • PACAP(6–38), amino acids 6 to 38 of PACAP
  • PACAP, pituitary adenylate cyclase-activating polypeptide
  • PACAP27, 27-amino acid form of PACAP
  • PACAP38, 38-amino acid form of PACAP
  • PACAP-LI, PACAP-like immunoreactivity
  • PAM, peptidyl glycine α
  • -amidating monooxygenase; PC, prohormone convertase
  • PCR, polymerase chain reaction
  • PHI, peptide histidine-isoleucine
  • PI3-K, phosphatidylinositol 3′-OH kinase
  • PKA, protein kinase A
  • PKC, protein kinase C
  • PLC, phospholipase C
  • POMC, pro-opiomelanocortin
  • PRL, prolactin
  • PRP, PACAP-related peptide
  • PVN, paraventricular nucleus
  • PYY, peptide tyrosine tyrosine
  • RO 25–1553, L-threoninamide, N-acetyl-L-histidyl-L-seryl-L-α-aspartyl-L-alanyl-L-valyl-L-phenylalanyl-L-threonyl-L-α-glutamyl-L-asparaginyl-L-tyrosyl-L-threonyl-L-lysyl-L-leucyl-L-arginyl-L-lysyl-L-glutaminyl-L-norleucyl-L-alanyl-L-alanyl-L-lysyl-L-lysyl-L-tyrosyl-L-leucyl-L-asparaginyl-L-α-aspartyl-L-leucyl-L-lysyl-L-lysylglycylglycyl-(25–21)-lactam
  • RT, reverse transcription
  • SCN, suprachiasmatic nucleus
  • Th, T helper
  • TRH, thyrotropin-releasing hormone
  • TSH, thyroid-stimulating hormone
  • VIP, vasoactive intestinal polypeptide
  • VPAC1-R, VIP/PACAP receptor, subtype 1
  • VPAC2-R, VIP/PACAP receptor, subtype 2
  • ZK98299, onapristone
  • © 2009 by The American Society for Pharmacology and Experimental Therapeutics
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Pharmacological Reviews: 61 (3)
Pharmacological Reviews
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September 2009
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Pituitary Adenylate Cyclase-Activating Polypeptide and Its Receptors: 20 Years after the Discovery

David Vaudry, Anthony Falluel-Morel, Steve Bourgault, Magali Basille, Delphine Burel, Olivier Wurtz, Alain Fournier, Billy K. C. Chow, Hitoshi Hashimoto, Ludovic Galas and Hubert Vaudry
Pharmacological Reviews September 1, 2009, 61 (3) 283-357; DOI: https://doi.org/10.1124/pr.109.001370

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Pituitary Adenylate Cyclase-Activating Polypeptide and Its Receptors: 20 Years after the Discovery

David Vaudry, Anthony Falluel-Morel, Steve Bourgault, Magali Basille, Delphine Burel, Olivier Wurtz, Alain Fournier, Billy K. C. Chow, Hitoshi Hashimoto, Ludovic Galas and Hubert Vaudry
Pharmacological Reviews September 1, 2009, 61 (3) 283-357; DOI: https://doi.org/10.1124/pr.109.001370
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