Distribution of neuropeptide FF-like immunoreactive structures in the lamprey central nervous system and its relation to catecholaminergic neuronal structures Manuel A. Pombal a, *, Jesu ´s M. Lo ´ pez b , Marı ´a C. de Arriba a , Manuel Megı ´as a , Agustı ´n Gonza ´ lez b a Neurolam Group, Department of Functional Biology and Health Sciences, Faculty of Biology, University of Vigo, 36310 Vigo, Spain b Department of Cell Biology, Faculty of Biology, University Complutense, 28040 Madrid, Spain 1. Introduction The octapeptide neuropeptide FF (NPFF, FLFQPQRF-amide) has been referred to as mammalian FMRF-NH 2 -like peptide, F-8-F-amide, or morphine modulating neuropeptide. The NPFF family consists of several different peptides: NPFF and neuropeptide AF (NPAF), both originally isolated from bovine brain by using antisera directed against the molluscan tetrapeptide FMRF-NH 2 [88]; neuropeptide SF (NPSF), primarily identified from the rat brain and spinal cord [89]; as well as different longer peptides such as NPA-NPFF wich is the most abundant in the rat spinal cord [9]; and SQA-NPFF, identified in human neuroblastoma transfected with human proNPFF transcript, and its homologue in mouse, SPA-NPFF [10]. Two precursors (proNPFF A and proNPFF B ) encoding peptides con- taining the PQRF-amide sequence have been recently cloned peptides 27 (2006) 1054–1072 article info Article history: Received 1 April 2005 Accepted 22 June 2005 Published on line 17 February 2006 Keywords: FMRFamide-related peptides Neuropeptides Immunohistochemistry Hypothalamus Agnathan Evolution abstract The neuropeptide FF (NPFF) is an octapeptide of the RFamide-related peptides (FaRPs) that was primarily isolated from the bovine brain. Its distribution in the CNS has been reported in several mammalian species, as well as in some amphibians. Therefore, in order to gain insight in the evolution on the expression pattern of this neuropeptide in vertebrates, we carried out an immunohistochemical study in the sea lamprey, Petromyzon marinus. The distribution of NPFF-like-immunoreactive (NPFF-ir) structures in the lamprey brain is, in general, comparable to that previously described in other vertebrate species. In lamprey, most of the NPFF-ir cells were found in the hypothalamus, particularly in two large populations, the bed nucleus of the tract of the postoptic commissure and the tuberomam- millary area. Numerous NPFF-ir cells were also observed in the rostral rhombencephalon, including a population in the dorsal isthmic gray and the reticular formation. Additional labeled neurons were found inside the preoptic region, the parapineal vesicle, the periven- tricular mesencephalic tegmentum, the descending trigeminal tract, the nucleus of the solitary tract, as well as in the gray matter of the spinal cord. The NPFF-ir fibers were widely distributed in the brain and the spinal cord, being, in general, more concentrated throughout the basal plate. The presence of NPFF-ir fibers in the lamprey neurohypophysis suggests that the involvement of NPFF-like substances in the hypothalamo-hypophyseal system had emerged early during evolution. # 2006 Elsevier Inc. All rights reserved. * Corresponding author. Tel.: +34 986 812390; fax: +34 986 812556. E-mail address: [email protected] (M.A. Pombal). available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/peptides 0196-9781/$ – see front matter # 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.peptides.2005.06.033
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Distribution of neuropeptide FF-like immunoreactivestructures in the lamprey central nervous systemand its relation to catecholaminergic neuronal structures
Manuel A. Pombal a,*, Jesus M. Lopez b, Marıa C. de Arriba a, Manuel Megıas a,Agustın Gonzalez b
aNeurolam Group, Department of Functional Biology and Health Sciences, Faculty of Biology, University of Vigo, 36310 Vigo, SpainbDepartment of Cell Biology, Faculty of Biology, University Complutense, 28040 Madrid, Spain
p e p t i d e s 2 7 ( 2 0 0 6 ) 1 0 5 4 – 1 0 7 2
a r t i c l e i n f o
Article history:
Received 1 April 2005
Accepted 22 June 2005
Published on line 17 February 2006
Keywords:
FMRFamide-related peptides
Neuropeptides
Immunohistochemistry
Hypothalamus
Agnathan
Evolution
a b s t r a c t
The neuropeptide FF (NPFF) is an octapeptide of the RFamide-related peptides (FaRPs) that
was primarily isolated from the bovine brain. Its distribution in the CNS has been reported in
several mammalian species, as well as in some amphibians. Therefore, in order to gain
insight in the evolution on the expression pattern of this neuropeptide in vertebrates, we
carried out an immunohistochemical study in the sea lamprey, Petromyzon marinus. The
distribution of NPFF-like-immunoreactive (NPFF-ir) structures in the lamprey brain is, in
general, comparable to that previously described in other vertebrate species. In lamprey,
most of the NPFF-ir cells were found in the hypothalamus, particularly in two large
populations, the bed nucleus of the tract of the postoptic commissure and the tuberomam-
millary area. Numerous NPFF-ir cells were also observed in the rostral rhombencephalon,
including a population in the dorsal isthmic gray and the reticular formation. Additional
labeled neurons were found inside the preoptic region, the parapineal vesicle, the periven-
tricular mesencephalic tegmentum, the descending trigeminal tract, the nucleus of the
solitary tract, as well as in the gray matter of the spinal cord. The NPFF-ir fibers were widely
distributed in the brain and the spinal cord, being, in general, more concentrated throughout
the basal plate. The presence of NPFF-ir fibers in the lamprey neurohypophysis suggests that
the involvement of NPFF-like substances in the hypothalamo-hypophyseal system had
p e p t i d e s 2 7 ( 2 0 0 6 ) 1 0 5 4 – 1 0 7 2 1069
in the dorsal part of the cell column [7,11,17,57,79]. In addition,
the NPY-ir fibers appeared to originate from these cell bodies
and were restricted to the dorsal half of the spinal cord [11,79].
Because of NPFF-ir was occasionally seen in the same fibers
with NPY in the porcine spinal cord [83], these substances
could also colocalize to the same neurons. Double labeling
techniques are needed to test this hypothesis.
Fibers immunoreactive for FMRFamide did not form
discrete bundles, but were scattred diffusely throughout
diverse regions of the brain and rostral spinal cord
[12,19,54]. Concerning the neurohypophysis, labeled fibers
were observed in Ichthyomyzon unicuspis [19], but only present
to a limited extend in its anterior part (median eminence) in
Lampetra japonica [54]. In addition, no FMRFamide immunor-
eactivity was found in the neurohypohysis of the three species
of hagfish studied so far [15,28,85]; however, there is a rich
innervation by NPFF-ir fibers. Thus, whereas, the hypotha-
lamic immunoreactive cells for FMRF do not participate in
neuroendocrine mechanisms in hagfishes and their role in
lampreys appears to be very limited, those labeled for NPFF
appear to be highly involved in the regulation of the
neurohypophysis by the hypothalamo-hypophyseal system
(see Section 4.1.2).
4.3. Codistribution of NPFF and catecholamines
In the present study, the presence of NPFF in the catechola-
minergic cells has been investigated, since these substances
are present in neurons that show similar distribution patterns
[59,60,62,84]. If NPFF colocalizes with the catecholamine-
synthesizing enzyme TH, it could act as a cotransmitter in
catecholaminergic neurons and thus be involved in various
somatosensory and visceral functions. Although the NPFF-ir
cells were found in several places where interaction with
catecholaminergic cells could be expected, no colocalization
was found throughout the sea lamprey brain and spinal cord.
However, our findings are of significance in that they add
confirmation to the previously reported subdivisions of the
lamprey preoptic area and hypothalamus [65]. In addition, our
study showed an extensive codistribution of NPFF-ir and TH-ir
fibers in several regions or nuclei in the lamprey CNS. With
this technique, the TH-ir structures (green) and the NPFF-ir
structures (red) are well distinguished in separate neurons.
However, sometimes they appeared somehow masked (show-
ing a yellow-like color), particularly in those areas of high
concentration of labeled fibers such as the neurohypophysis or
the postinfundibular commissure (see Fig. 5A). This is
certainly due to overlapping of fibers with different immunor-
eactivity (TH-ir or NPFF-ir) because of the thickness of the
sections (40 mm), but not because of colocalization of both
substances (TH and NPFF) in the same fiber.
Unfortunately, the presence of double labeled cells for NPFF
and TH in either the isthmic region, the nucleus of the solitary
tract, and the lateral spinal cord could not be studied because
of the absence of immunolabeling with the monoclonal anti-
TH antiserum used in our study. This was somehow expected
because the presence of catecholaminergic cell bodies in these
populations as revealed by using antisera against TH and/or
dopamine has been difficult to demonstrate in lampreys
[59,60,62]. As an example, all the anti-TH antibodies used
previously failed to detect any labeling in the nucleus of the
solitary tract and the lateral spinal cord [59,60,62], whereas,
some labeling was reported in both by using a non-
commercial anti-dopamine antibody [62,68].
5. Conclusions
The comparative analysis of the distribution of FMRF-ir and/
or NPY-ir with that of NPFF-ir structures in the lamprey CNS
showed a partial overlapping which suggests that a NPFF-
like peptide also exists in this animal. Furthermore, the NPFF
immunoreactive network of fibers appears to be well
developed in the brain of the lamprey, a living member of
the most primitive vertebrates. This study reveals that, in
general, the lamprey pattern of NPFF-ir elements is similar to
that previously reported for other vertebrates. In addition, the
organization of some of the NPFF-ir systems in the lamprey
CNS as, for example, the innervation of the neurohypophysis or
the spinal cord, comprises features of the anamniote (amphi-
bian) brain that are also common to all amniotes (mammals)
studied so far, thus being conservative to a surprisingly high
degree. Although more studies are needed, this also suggests
that the function of this neuropeptide could be conserved
through vertebrate evolution. Finally, the double immuno-
fluorescent experiments have shown that, in spite of the high
degree of codistribution found, colocalization of NPFF and TH
was absent in all labeled cell populations.
Acknowledgements
We want to express our gratitude to Dr. H.-Y.T. Yang for his
generous gift of the antiserum used in this study, and Dr. S.
Nagi for copy-editing suggestions. We also thank the Con-
sellerıa de Medio Ambiente of the Xunta de Galicia for their
kind permission to capture of the lampreys used in this study,
as well as M. Garcıa, J. Garcıa and J.A. Garea at the Center for
Control of Fishes of Ximonde (A Coruna). This study was
supported by grants from Ministerio de Ciencia y Technologıa-
FEDER (BFI2003-04479), Xunta de Galicia (PGIDT04P-
XIC31004PN), and University of Vigo (Z441-64102) to MAP,
and Ministerio de Ciencia y Tecnologıa (BFI2003-0559) to AG.
r e f e r e n c e s
[1] Aarnisalo A, Panula P. Neuropeptide FF in the lateral spinaland lateral cervical nuclei: evidence for contacts onspinothalamic neurons. Exp Brain Res 1998;119:159–65.
[2] Aarnisalo A, Tuominen RK, Nieminen M, Vaino P, Panula P.Evidence for prolactin releasing activity of neuropeptide FFin rats. Neuroendocrinol Lett 1997;18:191–6.
[3] Allard M, Theodosis DT, Rousselot P, Lombard MC,Simonnet G. Characterization and localization of a putativemorphine-modulating peptide, FLFQPQRFamide, in the ratspinal cord: biochemical and immunocytochemical studies.Neuroscience 1991;40:81–92.
[4] Auclair F, Lund JP, Dubuc R. Immunohistochemicaldistribution of tachykinins in the CNS of the lampreyPetromyzon marinus. J Comp Neurol 2004;479:328–46.
p e p t i d e s 2 7 ( 2 0 0 6 ) 1 0 5 4 – 1 0 7 21070
[5] Boer HH, Schot LP, Veenstra JA, Reichelt D.Immunocytochemical identification of neural elements inthe central nervous systems of a snail, some insects, a fish,and a mammal with an antiserum to the molluscan cardio-excitatory tetrapeptide FMRF-amide. Cell Tissue Res1980;213:21–7.
[6] Boersma CJ, Sonnemans MA, Van Leeuwen FW.Immunocytochemical localization of neuropeptide FF(FMRFamide-like peptide) in the hypothalamo-neurohypophyseal system of Wistar and Brattlebororats by light and electron microscopy. J Comp Neurol1993;336:555–70.
[7] Bongianni F, Christenson J, Hokfelt T, Grillner S.Neuropeptide Y-immunoreactive spinal neurons makeclose appositions on axons of primary sensory afferents.Brain Res 1990;523:337–41.
[8] Bonini JA, Jones KA, Adham N, Forray C, Artymyshyn R,Durkin MM, et al. Identification and characterization of twoG protein-coupled receptors for neuropeptide FF. J BiolChem 2000;275:39324–31.
[9] Bonnard E, Burlet-Schiltz O, Frances B, Mazarguil H,Monsarrat B, Zajac JM, et al. Identification of neuropeptideFF-related peptides in rodent spinal cord. Peptides2001;22:1085–92.
[10] Bonnard E, Burlet-Schiltz O, Monsarrat B, Girard JP, ZajacJM. Identification of proNeuropeptide FFA peptidesprocessed in neuronal and non-neuronal cells and innervous tissue. Eur J Biochem 2003;270:4187–99.
[11] Brodin L, Rawitch A, Taylor T, Ohta Y, Ring H, Hokfelt T,et al. Multiple forms of pancreatic polypeptide-relatedcompounds in the lamprey CNS: partial characterizationand immunohistochemical localization in the brain stemand spinal cord. J Neurosci 1989;9:3428–42.
[12] Buchanan JT, Brodin L, Hokfelt T, Van Dongen PA, GrillnerS. Survey of neuropeptide-like immunoreactivityin the lamprey spinal cord. Brain Res 1987;408:299–302.
[13] Castro A, Becerra M, Anadon R, Manso MJ. Distribution anddevelopment of FMRFamide-like immunoreactive neuronalsystems in the brain of the brown trout, Salmo trutta fario.J Comp Neurol 2001;440:43–64.
[14] Chiba A, Honma Y, Oka S. Immunohistochemicallocalization of neuropeptide Y-like substance in the brainand hypophysis of the brown hagfish, Paramyxine atami.Cell Tissue Res 1993;271:289–95.
[15] Chiba A, Honma Y. FMRFamide-immunoreactive structuresin the brain of the brown hagfish, Paramyxine atami:relationship with neuropeptide Y-immunoreactivestructures. Histochemistry 1992;98:33–8.
[16] Chiba A. Distribution of neuropeptide Y-likeimmunoreactivity in the brain of the bichir, Polypterussenegalus, with special regard to the terminal nerve. CellTissue Res 1997;289:275–84.
[17] Chiba A. Immunohistochemical distribution ofneuropeptide Y-related substance in the brain andhypophysis of the arctic lamprey, Lethenteron japonica. BrainBehav Evol 1999;53:102–9.
[18] Crespo M, Moreno N, Lopez JM, Gonzalez A. Comparativeanalysis of neuropeptide FF-like immunoreactivity in thebrain of anuran (Rana perezi, Xenopus laevis) and urodele(Pleurodeles waltl) amphibians. J Chem Neuroanat2003;25:53–71.
[20] Elshourbagy NA, Ames RS, Fitzgerald LR, Foley JJ, ChambersJK, Szekeres PG, et al. Receptor for the pain modulatoryneuropeptides FF and AF is an orphan G protein-coupledreceptor. J Biol Chem 2000;275:25965–71.
[21] Ferrarese C, Iadarola MJ, Yang HY, Costa E. Peripheral andcentral origin of Phe–Met–Arg–Phe-amide immunoreactivityin rat spinal cord. Regul Pept 1986;13:245–52.
[22] Goossens N, Dierickx K, Vandesande F.Immunocytochemical demonstration of the hypothalamo-hypophysial vasotocinergic system of Lampetra fluviatilis.Cell Tissue Res 1977;177:317–23.
[23] Gouarderes C, Sutak M, Zajac JM, Jhamandas K.Antinociceptive effects of intrathecally administeredF8Famide and FMRFamide in the rat. Eur J Pharmacol1993;237:333–9.
[24] Greenberg MJ, Rao KR, Lehman HK, Price DA, Doble KE.Cross-phyletic bioactivity of arthropod neurohormonesand molluscan ganglion extracts: evidence of an extendedpeptide family. J Exp Zool 1985;233:337–46.
[25] Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y,Hosoya M, et al. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat CellBiol 2000;2:703–8.
[26] Jennings JB, Davenport TR, Varndell IM. FMRFamide-likeimmunoreactivity and arylamidase activity in turbellariansand nemerteans-evidence for a novel neurovascularcoordinating system in nemerteans. Comp BiochemPhysiol C 1987;86:425–30.
[27] Jhamandas JH, Jhamandas A, Harris KH. New centralprojections of neuropeptide FF: colateral branchingpathways in the brainstem and hypothalamus in the rat. JChem Neuroanat 2001;21:171–9.
[28] Jirikowski G, Erhart G, Grimmelikhuijzen CJ, Triepel J,Patzner RA. FMRF-amide-like immunoreactivity in brainand pituitary of the hagfish Eptatretus burgeri(Cyclostomata). Cell Tissue Res 1984;237:363–6.
[29] Kavaliers M. Inhibitory influences of mammalianFMRFamide (Phe–Met–Arg–Phe-amide)-related peptides onnociception and morphine- and stress-induced analgesia inmice. Neurosci Lett 1990;115:307–12.
[30] Kavaliers M, Colwell DD. Neuropeptide FF (FLFQPQRF-NH2)and IgG from neuropeptide FF antiserum affect spatiallearning in mice. Neurosci Lett 1993;157:75–8.
[31] Kivipelto L. Ultrastructural localization of neuropeptide FF,a new neuropeptide in the brain and pituitary of rats. RegulPept 1991;34:211–24.
[32] Kivipelto L, Aarnisalo AA, Panula P. Neuropeptide FF iscolocalized with catecholamine synthesizing enzymes inneurons of the nucleus of the solitary tract. Neurosci Lett1992;143:190–4.
[33] Kivipelto L, Majane EA, Yang H-YT, Panula P.Immunohistochemical distribution and partialcharacterization of FLFQPQRFamide-like peptides in thecentral nervous system of rats. J Comp Neurol1989;186:269–87.
[34] Kivipelto L, Panula P. Central neuronal pathwayscontaining FLFQPQRFamide-like (morphine-modulating)peptides in the rat brain. Neuroscience 1991;41:137–48.
[35] Kivipelto L, Panula P. Comparative distribution of neuronscontaining FLFQPQRF-amide-like (morphine-modulating)peptide and related neuropeptides in the rat brain. Eur JNeurosci 1991;3:175–85.
[36] Kivipelto L, Panula P. Origin and distribution ofneuropeptide-FF-like immunoreactivity in the spinal cordof rats. J Comp Neurol 1991;307:107–19.
[37] Kivipelto L, Rubenstein J, Yang HY, Panula P. Ontogeny ofthe F8Famide-like (morphine-modulating) peptides in thecentral nervous system of rats. J Comp Neurol1991;304:14–33.
[38] Kotani M, Mollereau C, Detheux M, Le Poul E, Brezillon S,Vakili J, et al. Functional characterization of a humanreceptor for neuropeptide FF and related peptides.Brit J Pharmacol 2001;133:138–44.
p e p t i d e s 2 7 ( 2 0 0 6 ) 1 0 5 4 – 1 0 7 2 1071
[39] Koyama H, Kishida R, Goris RC, Kusunoki T. Organization ofsensory and motor nuclei of the trigeminal nerve inlampreys. J Comp Neurol 1987;264:437–48.
[40] Kyle AL, Luo BG, Magnus TH, Stell WK. Substance P-,F8Famide-, and A18Famide-like immunoreactivity in thenervus terminalis and retina of the goldfish Carassiusauratus. Cell Tissue Res 1995;280:605–15.
[41] Labrouche S, Verdot L, Theodosis DT, Allard M, SimmonetG. Characterization of a morphine-modulating peptide,FLFQPQRFamide, in the rat hypophysis: biochemical andimmunochemical studies. Endocrinology 1993;132:2191–8.
[42] Lee CH, Wasowicz K, Brown R, Majane EA, Yang HY, PanulaP. Distribution and characterization of neuropeptideFF-like immunoreactivity in the rat nervous systemwith a monoclonal antibody. Eur J Neurosci1993;5:1339–48.
[43] Liu Q, Guan XM, Martin WJ, McDonald TP, Clements MK,Jiang Q, et al. Identification and characterization of novelmammalian neuropeptide FF-like peptides that attenuatemorphine-induced antinociception. J Biol Chem2001;276:36961–9.
[44] Majane EA, Casanova MF, Yang HY. Biochemicalcharacterization of FMRF-NH2-like peptides in spinal cordsof various mammalian species using specificradioimmunoassay. Peptides 1988;9:1137–44.
[45] Majane EA, Panula P, Yang H-YT. Rat brain regionaldistribution and spinal cord neuronal pathway ofFLFQPQRF-NH2, a mammalian FMRF-NH2-like peptide.Brain Res 1989;494:1–12.
[46] Majane EA, Yang HY. Distribution and characterization oftwo putative endogenous opioid antagonist peptides inbovine brain. Peptides 1987;8:657–62.
[47] Majane EA, Yang HY. FMRF-NH2-like peptide is deficient inthe pituitary gland of the Brattleboro rat. Peptides1990;11:345–9.
[48] Majane EA, Yang H-YT. Mammalian FMRF-NH2-likepeptide in rat pituitary: decrease by osmotic stimulus.Peptides 1991;12:1303–8.
[49] Majane EA, Zhu J, Aarnisalo A, Panula P. Origin ofneurohypophyseal neuropeptide FF (FLFQPQRF-NH2).Endocrinology 1993;133:1578–84.
[50] Malin D, Lake JR, Hammond MV, Fowler DE, Brown SL, SimsJL, et al. FMRFamide-like mammalian octapeptide: possiblerole in opiate dependence and abstinence. Peptides1990;11:969–72.
[51] Munz H, Claas B, Stumpf WE, Jennes L. Centrifugalinnervation of the retina by luteinizing hormone releasinghormone (LHRH)-immunoreactive telencephalic neurons inteleostean fishes. Cell Tissue Res 1982;222:313–23.
[52] Nieuwenhuys R, Nicholson C. Lampreys, petromyzontoidea.In: Nieuwenhuys R, ten Donkelaar HJ, Nicholson C, editors.The Central Nervous System of Vertebrates, vol. 1. Berlin:Springer-Verlag; 1998. p. 397–495.
[53] Oehlmann VD, Korte H, Sterner C, Korsching SI. Aneuropeptide FF-related gene is expressed selectively inneurons of the terminal nerve in Danio rerio. Mech Dev2002;117:357–61.
[54] Ohtomi M, Fujii K, Kobayashi H. Distribution ofFMRFamide-like immunoreactivity in the brain andneurohypophysis of the lamprey, Lampetra japonica. CellTissue Res 1989;256:581–4.
[55] Panula P, Aarnisalo AA, Wasowicz K. Neuropeptide FF, amammalian neuropeptide with multiple functions. ProgNeurobiol 1996;48:461–87.
[56] Panula P, Kivipelto L, Nieminen O, Majane EA, Yang H-YT.Neuroanatomy of morphine modulating neuropeptides.Med Biol 1987;65:127–35.
[57] Parker D, Soderberg C, Zotova E, Shupliakov O, Langel U,Bartfai T, et al. Co-localized neuropeptide Y and GABA have
complementary presynaptic effects on sensory synaptictransmission. Eur J Neurosci 1998;10:2856–70.
[58] Perry SJ, Yi-Kung Huang E, Cronk D, Bagust J, Sharma R,Walker RJ, et al. A human gene encoding morphinemodulating peptides related to NPFF and FMRFamide. FEBSLett 1997;409:426–30.
[59] Pierre J, Mabouche M, Suderevskaya EI, Reperant J, Ward R.Immunohistochemical localization of dopamine andits synthetic enzymes in the central nervous system ofthe lamprey Lampetra fluviatilis. J Comp Neurol1997;380:119–35.
[60] Pierre J, Rio JP, Mabouche M, Reperant J. Catecholaminesystems in the brain of cyclostomes, the lamprey, Lampetrafluviatilis. In: Smeets WJA, Reiner A, editors. Phylogeny andDevelopment of Catecholamine Systems in the CNS ofVertebrates. Cambridge: Cambridge University Press; 1994.p. 7–19.
[61] Pinelli C, D’Aniello B, Sordino P, Meyer DL, Fiorentino M,Rastogi RK. Comparative immunocytochemical study ofFMRFamide neuronal system in the brain of Danio rerio andAcipenser ruthenus during development. Brain Res DevBrain Res 2000;119:195–208.
[62] Pombal MA, El Manira A, Grillner S. Afferents of thelamprey striatum with special reference to thedopaminergic system—a combined tracing andimmunohistochemical study. J Comp Neurol1997;386:71–91.
[63] Pombal MA, Marın O, Gonzalez A. Choline acetyltransferaseimmunoreactivity in the hypothalamoneurohypophysialsystem of the lamprey. Eur J Morphol 1999;37:103–6.
[64] Pombal MA, Marın O, Gonzalez A. Distribution of cholineacetyltransferase-immunoreactive structures in thelamprey brain. J Comp Neurol 2001;431:105–26.
[65] Pombal MA, Puelles L. A prosomeric map of the lampreyforebrain based on calretinin immunocytochemistry,nissl stain and ancillary markers. J Comp Neurol1999;414:391–422.
[66] Roth BL, Disimone J, Majane EA, Yang H-YT. Elevations ofarterial pressure in rats by two new vertebrate peptidesFLFQPQRF-NH2 and AGEGLSSPFWSLAAPQRF-NH2, whichare immunoreactive to FMRF-NH2 antiserum.Neuropeptides 1987;10:37–42.
[67] Sasek CA, Elde RP. Distribution of neuropeptide Y-likeimmunoreactivity and its relationship to FMRF-amide-likeimmunoreactivity in the sixth lumbar and first sacralspinal cord segments of the rat. J Neurosci1985;5:1729–39.
[68] Schotland JL, Shupliakov O, Grillner S, Brodin L. Synapticand nonsynaptic monoaminergic neuron systems in thelamprey spinal cord. J Comp Neurol 1996;372:229–44.
[69] Soderberg C, Pieribone VA, Dahlstrand J, Brodin L,Larhammar D. Neuropeptide role of both peptide YY andneuropeptide Y in vertebrates suggested by abundantexpression of their mRNAs in a cyclostome brain.J Neurosci Res 1994;37:633–40.
[70] Sternberger LA. Immunocytochemistry. New York: Wiley;1979.
[71] Stinus L, Allard M, Gold L, Simonnet G. Changes in CNSneuropeptide FF-like material, pain sensitivity, and opiatedependence following chronic morphine treatment.Peptides 1995;16:1235–41.
[72] Sundblom DM, Panula P, Fyhrquist F. Neuropeptide FF-likeimmunoreactivity in human plasma. Peptides1995;16(2):347–50.
[73] Tang J, Yang HY, Costa E. Inhibition of spontaneous andopiate-modified nociception by an endogenousneuropeptide with Phe–Met–Arg–Phe–NH2-likeimmunoreactivity. Proc Natl Acad Sci USA 1984;81:5002–5.
p e p t i d e s 2 7 ( 2 0 0 6 ) 1 0 5 4 – 1 0 7 21072
[74] Tsuneki K. The neurohypophysis of cyclostomes as aprimitive hypothalamic center of vertebrates. Zool Sci1988;5:21–32.
[75] Uchiyama H, Reh TA, Stell WK. Immunocytochemical andmorphological evidence for a retinopetal projection inanuran amphibians. J Comp Neurol 1988;274:48–59.
[76] Ukena K, Iwakoshi E, Minakata H, Tsutsui K. A novel rathypothalamic RFamide-related peptide identified byimmunoaffinity chromatography and mass spectrometry.FEBS Lett 2002;512:255–8.
[77] Vallarino M, Feuilloley M, Thoumas JL, Demorgny R, MasiniMA, Vaudry H. Distribution of FMRFamide-likeimmunoreactivity in the brain of the lungfish Protopterusannectens. Peptides 1995;16:1187–96.
[78] Vallarino M, Salsotto-Cattaneo MT, Feuilloley M, Vaudry H.Distribution of FMRFamide-like immunoreactivity in thebrain of the elasmobranch fish Scyliorhynus canicula.Peptides 1991;12:1321–8.
[79] Van Dongen PA, Hokfelt T, Grillner S, Verhofstad AA,Steinbusch HW, Cuello AC, et al. Immunohistochemicaldemonstration of some putative neurotransmitters inthe lamprey spinal cord and spinal ganglia: 5-hydroxytryptamine-, tachykinin-, and neuropeptide-Y-immunoreactive neurons and fibers. J Comp Neurol1985;234:501–22.
[80] Vesselkin NP, Rio JP, Reperant J, Kenigfest NB, Adanina VO.Retinopetal projections in lampreys. Brain Behav Evol1996;48:277–86.
[81] Vilim FS, Aarnisalo AA, Nieminen ML, Lintunen M,Karlstedt K, Kontinen V, et al. Gene for pain modulatoryneuropeptide NPFF: induction in spinal cord by noxiousstimuli. Mol Pharmacol 1999;55:804–11.
[82] Von Bartheld CS. The terminal nerve and its relation withextrabulbar ‘‘olfactory’’ projections: lessons from lampreysand lungfishes. Microsc Res Tech 2004;65:13–24.
[83] Wasowicz K, Panula P. Distribution of neuropeptide FF inporcine spinal cord in comparison with other neuropeptidesand serotonin. J Comp Neurol 1994;346:530–40.
[84] Weigle C, Northcutt RG. The chemoarchitecture of theforebrain of lampreys: evolutionary implications bycomparisons with gnathostomes. Eur J Morphol1999;37:122–5.
[85] Wicht H, Northcutt RG. FMRFamide-like immunoreactivityin the brain of the Pacific hagfish, Eptatretus stouti(Myxinoidea). Cell Tissue Res 1992;270:443–9.
[86] Wirsig-Wiechmann CR, Basinger SF. FMRFamide-immunoreactive retinopetal fibers in the frog, Rana pipiens:demonstration by lesion and immunocytochemicaltechniques. Brain Res 1988;449:116–34.
[87] Wright DE, Demski LS. Organization of GnRH andFMRFamide systems in two primitive bony fishes (orderpolypteriformes). Brain Behav Evol 1996;47:267–78.
[88] Yang H-YT, Fratta W, Majane EA, Costa E. Isolation,sequencing, synthesis, and pharmacologicalcharacterization of two brain neuropeptides that modulatethe action of morphine. Proc Nat Acad Sci USA1985;82:7757–61.
[89] Yang H-YT, Martin B. Isolation and characterization of aneuropeptide from brain and spinal cord of the rat. SocNeurosci Abstr 1995;21:760.
[90] Yanez J, Pombal MA, Anadon R. Afferent and efferentconnections of the parapineal organ in lampreys: a tracttracing and immunocytochemical study. J Comp Neurol1999;403:171–89.