Cloning and expression of tachykinins and their association with kisspeptins in the brains of zebrafish

Journal of Comparative Neurology

Volumn 520, Issue 13, 2012, Pages 2991-3012

  Ogawa, Satoshi ^a   Ramadasan, Priveena Nair ^a   Goschorska, Maja ^a   Anantharajah, Aveena ^a   We Ng, Kai ^a   Parhar, Ishwar S ^a  

^a MONASH UNIVERSITY MALAYSIA   (Malaysia)

Author keywords

Habenula; Kiss2; Neurokinin; Tac

Indexed keywords

KISSPEPTIN; MESSENGER RNA; NEUROKININ A; NEUROKININ B; SUBSTANCE P; TACHYKININ;

ANIMAL TISSUE; ARTICLE; BRAIN; COMPUTER MODEL; CONTROLLED STUDY; DATA MINING; FEMALE; GENE; GENE EXPRESSION; GENE SEQUENCE; HABENULA; HYPOTHALAMUS; IN SITU HYBRIDIZATION; MALE; MESENCEPHALON; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY BULB; PREOPTIC AREA; PRIORITY JOURNAL; RHOMBENCEPHALON; TAC1 GENE; TAC2A GENE; TAC2B GENE; TELENCEPHALON; ZEBRA FISH;

ANIMALS; BRAIN; CLONING, MOLECULAR; IN SITU HYBRIDIZATION, FLUORESCENCE; KISSPEPTINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TACHYKININS; ZEBRAFISH;

EID: 84863574164     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23103     Document Type: Article

References (106)

1. Aizawa H, Bianco IH, Hamaoka T, Miyashita T, Uemura O, Concha ML, Russell C, Wilson SW, Okamoto H. 2005. Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus. Curr Biol 15: 238-243.
2. Anderson WG, Conlon JM, Hazon N. 1995. Characterization of the endogenous intestinal peptide that stimulates the rectal gland of Scyliorhinus canicula. Am J Physiol 268: R1359-1364.
3. Auclair F, Lund JP, Dubuc R. 2004. Immunohistochemical distribution of tachykinins in the CNS of the lamprey Petromyzon marinus. J Comp Neurol 479: 328-346.
4. Batten TF, Cambre ML, Moons L, Vandesande F. 1990. Comparative distribution of neuropeptide-immunoreactive systems in the brain of the green molly, Poecilia latipinna. J Comp Neurol 302: 893-919.
5. Broglio C, Rodríguez F, Gómez A, Arias JL, Salas C. 2010. Selective involvement of the goldfish lateral pallium in spatial memory. Behav Brain Res 210: 191-201.
6. Burgunder JM, Young WS 3rd. 1989. Neurokinin B and substance P genes are co-expressed in a subset of neurons in the rat habenula. Neuropeptides 13: 165-169.
7. Carter MS, Krause JE. 1990. Structure, expression, and some regulatory mechanisms of the rat preprotachykinin gene encoding substance P, neurokinin A, neuropeptide K, and neuropeptide gamma. J Neurosci 10: 2203-2214.
8. Champagne DE, Ribeiro JM. 1994. Sialokinin I and II: vasodilatory tachykinins from the yellow fever mosquito Aedes aegypti. Proc Natl Acad Sci U S A 91: 138-142.
9. Chen WJ, Orti G, Meyer A. 2004. Novel evolutionary relationship among four fish model systems. Trends Genet 20: 424-431.
10. Conlon JM, Larhammar D. 2005. The evolution of neuroendocrine peptides. Gen Comp Endocrinol 142: 53-59.
11. Conlon JM, Thim L. 1988. Isolation of the tachykinin, des[Ser1Pro2]scyliorhinin II from the intestine of the ray, Torpedo marmorata. Gen Comp Endocrinol 71: 383-388.
12. Conlon JM, Deacon CF, O'Toole L, Thim L. 1986. Scyliorhinin I and II: two novel tachykinins from dogfish gut. FEBS Lett 200: 111-116.
13. Conlon JM, O'Harte F, Peter RE, Kah O. 1991. Carassin: a tachykinin that is structurally related to neuropeptide-gamma from the brain of the goldfish. J Neurochem 56: 1432-1436.
14. Conlon JM, Adrian TE, Secor SM. 1997. Tachykinins (substance P, neurokinin A and neuropeptide gamma) and neurotensin from the intestine of the Burmese python, Python molurus. Peptides 18: 1505-1510.
15. Contestabile A, Villani L, Fasolo A, Franzoni MF, Gribaudo L, Oktedalen O, Fonnum F. 1987. Topography of cholinergic and substance P pathways in the habenulo-interpeduncular system of the rat. An immunocytochemical and microchemical approach. Neuroscience 21: 253-270.
16. Ding YQ, Shigemoto R, Takada M, Ohishi H, Nakanishi S, Mizuno N. 1996. Localization of the neuromedin K receptor (NK3) in the central nervous system of the rat. J Comp Neurol 364: 290-310.
17. Duarte CR, Schutz B, Zimmer A. 2006. Incongruent pattern of neurokinin B expression in rat and mouse brains. Cell Tissue Res 323: 43-51.
18. Ebner K, Sartori SB, Singewald N. 2009. Tachykinin receptors as therapeutic targets in stress-related disorders. Curr Pharm Des 15: 1647-1674.
19. Erspamer V, Anastasi A. 1962. Structure and pharmacological actions of eledoisin, the active endecapeptide of the posterior salivary glands of Eledone. Experientia 18: 58-59.
20. Erspaemer V, Anastasi A, Bertaccini G, Cei JM. 1964. Structure and pharmacological actions of physalaemin, the main active polypeptide of the skin of Physalaemus fuscumaculatus. Experientia 20: 489-490.
21. Felip A, Zanuy S, Pineda R, Pinilla L, Carrillo M, Tena-Sempere M, Gomez A. 2009. Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals. Mol Cell Endocrinol 312: 61-71.
22. Finger TE. 1984. Vagotomy induced changes in acetyl cholinesterase staining and substance P-like immunoreactivity in the gustatory lobes of goldfish. Anat Embryol (Berl) 170: 257-264.
23. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CVR, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ. 2007. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 148: 5752-5760.
24. Goto T, Tanaka T. 2002. Tachykinins and tachykinin receptors in bone. Microsc Res Tech 58: 91-97.
25. Goto-Kazeto R, Kight KE, Zohar Y, Place AR, Trant JM. 2004. Localization and expression of aromatase mRNA in adult zebrafish. Gen Comp Endocrinol 139: 72-84.
26. Guran T, Tolhurst G, Bereket A, Rocha N, Porter K, Turan S, Gribble FM, Kotan LD, Akcay T, Atay Z, Canan H, Serin A, O'Rahilly S, Reimann F, Semple RK, Topaloglu AK. 2009. Hypogonadotropic hypogonadism due to a novel missense mutation in the first extracellular loop of the neurokinin B receptor. J Clin Endocrinol Metab 94: 3633-3639.
27. Halpern ME, Liang JO, Gamse JT. 2003. Leaning to the left: laterality in the zebrafish forebrain. Trends Neurosci 26: 308-313.
28. Hökfelt T, Pernow B, Wahren J. 2001. Substance P: a pioneer amongst neuropeptides. J Intern Med 249: 27-40.
29. Holmberg A, Schwerte T, Pelster B, Holmgren S. 2004. Ontogeny of the gut motility control system in zebrafish Danio rerio embryos and larvae. J Exp Biol 207: 4085-4094.
30. Inagaki S, Senba E, Shiosaka S, Takagi H, Kawai Y, Takatsuki K, Sakanaka M, Matsuzaki T, Tohyama M. 1981. Regional distribution of substance P-like immunoreactivity in the frog brain and spinal cord: immunohistochemical analysis. J Comp Neurol 201: 243-254.
31. Jensen J. 1997. Co-release of substance P and neurokinin A from the Atlantic cod stomach. Peptides 18: 717-722.
32. Jensen J, Conlon JM. 1992. Substance-P-related and neurokinin-A-related peptides from the brain of the cod and trout. Eur J Biochem 206: 659-664.
33. Jensen J, Olson KR, Conlon JM. 1993. Primary structures and effects on gastrointestinal motility of tachykinins from the rainbow trout. Am J Physiol 265: R804-810.
34. Kågström J, Holmgren S, Olson KR, Conlon JM, Jensen J. 1996. Vasoconstrictive effects of native tachykinins in the rainbow trout, Oncorhynchus mykiss. Peptides 17: 39-45.
35. Kanda A, Iwakoshi-Ukena E, Takuwa-Kuroda K, Minakata H. 2003. Isolation and characterization of novel tachykinins from the posterior salivary gland of the common octopus Octopus vulgaris. Peptides 24: 35-43.
36. Kanda S, Akazome Y, Matsunaga T, Yamamoto N, Yamada S, Tsukamura H, Maeda K, Oka Y. 2008. Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology 149: 2467-2476.
37. Kemali M, Sada E, Miralto A. 1986. Structural, ultrastructural and immunohistochemical observations on the interpeduncular nucleus of the elasmobranch fish Scyllium stellare. Z Mikrosk Anat Forsch 100: 451-463.
38. Kitahashi T, Ogawa S, Parhar IS. 2009. Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 150: 821-831.
39. Kotani H, Hoshimaru M, Nawa H, Nakanishi S. 1986. Structure and gene organization of bovine neuromedin K precursor. Proc Natl Acad Sci U S A 83: 7074-7078.
40. Krause JE, Chirgwin JM, Carter MS, Xu ZS, Hershey AD. 1987. Three rat preprotachykinin mRNAs encode the neuropeptides substance P and neurokinin A. Proc Natl Acad Sci U S A 84: 881-885.
41. Kurtz MM, Wang R, Clements MK, Cascieri MA, Austin CP, Cunningham BR, Chicchi GG, Liu Q. 2002. Identification, localization and receptor characterization of novel mammalian substance P-like peptides. Gene 296: 205-212.
42. Kyle AL, Luo B-G, Magnus TH, Stell WK. 1995. Substance P-, F8Famide-, and A18Famide-like immunoreactivity in the nervus terminalis and retina of the goldfish Carassius auratus. Cell Tissue Res 280: 605-615.
43. Lancien F, Mimassi N, Conlon JM, Le Mevel JC. 2009. Central effects of trout tachykinins on heart rate variability in trout. Ann N Y Acad Sci 1163: 379-382.
44. Lee YR, Tsunekawa K, Moon MJ, Um HN, Hwang JI, Osugi T, Otaki N, Sunakawa Y, Kim K, Vaudry H, Kwon HB, Seong JY, Tsutsui K. 2009. Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 150: 2837-2846.
45. Lehman MN, Coolen LM, Goodman RL. 2010. Minireview: Kisspeptin/Neurokinin B/Dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology 151: 3479-3489.
46. Leong JS, Jantzen SG, von Schalburg KR, Cooper GA, Messmer AM, Liao NY, Munro S, Moore R, Holt RA, Jones SJ, Davidson WS, Koop BF. 2010. Salmo salar and Esox lucius full-length cDNA sequences reveal changes in evolutionary pressures on a post-tetraploidization genome. BMC Genomics 11: 279.
47. Li S, Zhang Y, Liu Y, Huang X, Huang W, Lu D, Zhu P, Shi Y, Cheng CH, Liu X, Lin H. 2009. Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J Endocrinol 201: 407-418.
48. Lin XW, Peter RE. 1997. Goldfish gamma-preprotachykinin mRNA encodes the neuropeptides substance P, carassin, and neurokinin A. Peptides 18: 817-824.
49. Liu L, Conlon JM, Joss JM, Burcher E. 2002. Purification, characterization, and biological activity of a substance P-related peptide from the gut of the Australian lungfish, Neoceratodus forsteri. Gen Comp Endocrinol 125: 104-112.
50. Ljungdahl A, Hokfelt T, Nilsson G. 1978. Distribution of substance P-like immunoreactivity in the central nervous system of the rat-I. Cell bodies and nerve terminals. Neuroscience 3: 861-943.
51. Lucas LR, Hurley DL, Krause JE, Harlan RE. 1992. Localization of the tachykinin neurokinin B precursor peptide in rat brain by immunocytochemistry and in situ hybridization. Neuroscience 51: 317-345.
52. Macrae AD, Brenner S. 1994. One armed PCR (OA-PCR): amplification of genomic DNA from a single primer domain. Genomics 24: 176-178.
53. Marksteiner J, Sperk G, Krause JE. 1992a. Distribution of neurons expressing neurokinin B in the rat brain: immunohistochemistry and in situ hybridization. J Comp Neurol 317: 341-356.
54. Marksteiner J, Wahler R, Bellmann R, Ortler M, Krause JE, Sperk G. 1992b. Limbic seizures cause pronounced changes in the expression of neurokinin B in the hippocampus of the rat. Neuroscience 49: 383-395.
55. Mechaly AS, Vinas J, Piferrer F. 2011. Gene structure analysis of kisspeptin-2 (kiss2) in the Senegalese sole (Solea senegalensis): characterization of two splice variants of kiss2, and novel evidence for metabolic regulation of kisspeptin signaling in non-mammalian species. Mol Cell Endocrinol 339: 14-24.
56. Mi X, Yu H, Jia P, Zhang Z, Zhang L, Liu J. 2010. Two tachykinin-like peptides from skin secretions of Danio rerio. J Pept Sci 16: 81-84.
57. Mitani Y, Kanda S, Akazome Y, Zempo B, Oka Y. 2010. Hypothalamic kiss1 but not kiss2 neurons are involved in estrogen feedback in medaka (Oryzias latipes). Endocrinology 151: 1751-1759.
58. Morita Y, Finger TE. 1987a. Area postrema of the goldfish, Carassius auratus: ultrastructure, fiber connections, and immunocytochemistry. J Comp Neurol 256: 104-116.
59. Morita Y, Finger TE. 1987b. Topographic representation of the sensory and motor roots of the vagus nerve in the medulla of goldfish, Carassius auratus. J Comp Neurol 264: 231-249.
60. Mutolo D, Bongianni F, Cinelli E, Pantaleo T. 2010. Role of neurokinin receptors and ionic mechanisms within the respiratory network of the lamprey. Neuroscience 169: 1136-1149.
61. Nassel DR. 1999. Tachykinin-related peptides in invertebrates: a review. Peptides 20: 141-158.
62. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. 2009. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 29: 11859-11866.
63. Navarro VM, Castellano JM, McConkey SM, Pineda R, Ruiz-Pino F, Pinilla L, Clifton DK, Tena-Sempere M, Steiner RA. 2011. Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat. Am J Physiol Endocrinol Metab 300: E202-E210.
64. Nawa H, Kotani H, Nakanishi S. 1984. Tissue-specific generation of two preprotachykinin mRNAs from one gene by alternative RNA splicing. Nature 312: 729-734.
65. Noritake K, Matsuoka T, Ohsawa T, Shimomura K, Sanbuissho A, Uenoyama Y, Maeda K, Tsukamura H. 2011. Involvement of neurokinin receptors in the control of pulsatile luteinizing hormone secretion in rats. J Reprod Dev 57: 409-415.
66. Northcutt RG. 2006. Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494: 903-943.
67. Nozaki M, Gorbman A. 1986. Occurrence and distribution of substance P-related immunoreactivity in the brain of adult lampreys, Petromyzon marinus and Entosphenus tridentatus. Gen Comp Endocrinol 62: 217-229.
68. Page NM. 2004. Hemokinins and endokinins. Cell Mol Life Sci 61: 1652-1663.
69. Page NM, Morrish DW, Weston-Bell NJ. 2009. Differential mRNA splicing and precursor processing of neurokinin B in neuroendocrine tissues. Peptides 30: 1508-1513.
70. Patak E, Candenas ML, Pennefather JN, Ziccone S, Lilley A, Martín JD, Flores C, Mantecón AG, Story ME, Pinto FM. 2003. Tachykinins and tachykinin receptors in human uterus. Br J Pharmacol 139: 523-532.
71. Pennefather JN, Lecci A, Candenas ML, Patak E, Pinto FM, Maggi CA. 2004. Tachykinins and tachykinin receptors: a growing family. Life Sci 74: 1445-1463.
72. Piñuela C, Northcutt RG. 2007. Immunohistochemical organization of the forebrain in the white sturgeon, Acipenser transmontanus. Brain Behav Evol 69: 229-253.
73. Portavella M, Torres B, Salas C. 2004. Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24: 2335-2342.
74. Ramaswamy S, Seminara SB, Ali B, Ciofi P, Amin NA, Plant TM. 2010. Neurokinin B stimulates GnRH release in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus. Endocrinology 151: 4494-4503.
75. Ravina CG, Seda M, Pinto FM, Orea A, Fernández-Sánchez M, Pintado CO, Candenas ML. 2007. A role for tachykinins in the regulation of human sperm motility. Hum Reprod 22: 1617-1625.
76. Reiner A, Northcutt RG. 1987. An immunohistochemical study of the telencephalon of the African lungfish, Protopterus annectens. J Comp Neurol 256: 463-481.
77. Rodriguez-Moldes I, Manso MJ, Becerra M, Molist P, Anadon R. 1993. Distribution of substance P-like immunoreactivity in the brain of the elasmobranch Scyliorhinus canicula. J Comp Neurol 335: 228-244.
78. Ronnekleiv OK, Kelly MJ. 1984. Distribution of substance P neurons in the epithalamus of the rat: an immunohistochemical investigation. J Pineal Res 1: 355-370.
79. Sandoval-Guzman T, Rance NE. 2004. Central injection of senktide, an NK3 receptor agonist, or neuropeptide Y inhibits LH secretion and induces different patterns of Fos expression in the rat hypothalamus. Brain Res 1026: 307-312.
80. Satake H, Kawada T, Nomoto K, Minakata H. 2003. Insight into tachykinin-related peptides, their receptors, and invertebrate tachykinins: a review. Zool Sci 20: 533-549.
81. Schoofs L, Holman GM, Hayes TK, Nachman RJ, De Loof A. 1990. Locustatachykinin I and II, two novel insect neuropeptides with homology to peptides of the vertebrate tachykinin family. FEBS Lett 261: 397-401.
82. Selvaraj S, Kitano H, Fujinaga Y, Ohga H, Yoneda M, Yamaguchi A, Shimizu A, Matsuyama M. 2010. Molecular characterization, tissue distribution, and mRNA expression profiles of two Kiss genes in the adult male and female chub mackerel (Scomber japonicus) during different gonadal stages. Gen Comp Endocrinol 169: 28-38.
83. Severini C, Improta G, Falconieri-Erspamer G, Salvadori S, Erspamer V. 2002. The tachykinin peptide family. Pharmacol Rev 54: 285-322.
84. Shahjahan M, Motohashi E, Doi H, Ando H. 2010. Elevation of kiss2 and its receptor gene expression in the brain and pituitary of grass puffer during the spawning season. Gen Comp Endocrinol 169: 48-57.
85. Sharma SC, Berthoud VM, Breckwoldt R. 1989. Distribution of substance P-like immunoreactivity in the goldfish brain. J Comp Neurol 279: 104-116.
86. Suehiro Y, Yasuda A, Okuyama T, Imada H, Kuroyanagi Y, Kubo T, Takeuchi H. 2009. Mass spectrometric map of neuropeptide expression and analysis of the gamma-prepro-tachykinin gene expression in the medaka (Oryzias latipes) brain. Gen Comp Endocrinol 161: 138-145.
87. Taylor JS, Van de Peer Y, Meyer A. 2001. Genome duplication, divergent resolution and speciation. Trends Genet 17: 299-301.
88. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK. 2009. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for neurokinin B in the central control of reproduction. Nat Genet 41: 354-358.
89. van Aerle R, Kille P, Lange A, Tyler CR. 2008. Evidence for the existence of a functional kiss1/kiss1 receptor pathway in fish. Peptides 29: 57-64.
90. Van Loy T, Vandersmissen HP, Poels J, Van Hiel MB, Verlinden H, Vanden Broeck J. 2010. Tachykinin-related peptides and their receptors in invertebrates: a current view. Peptides 31: 520-524.
91. Vecino E, Ekström P. 1992. Colocalization of neuropeptide Y (NPY)-like and FMRFamide-like immunoreactivities in the brain of the Atlantic salmon (Salmo salar). Cell Tissue Res 270: 435-442.
92. Vecino E, Sharma SC. 1992. The development of substance P-like immunoreactivity in the goldfish brain. Anat Embryol (Berl) 186: 41-47.
93. Villani L, Guarnieri T, Salsi U, Bollini D. 1991. Substance P in the habenulo-interpeduncular system of the goldfish. Brain Res Bull 26: 225-228.
94. Villani L, Dipietrangelo L, Pallotti C, Pettazzoni P, Zironi I, Guarnieri T. 1994. Ultrastructural and immunohistochemical study of the telencephalo-habenulo-interpeduncular connections of the goldfish. Brain Res Bull 34: 1-5.
95. Wang Y, O'Harte F, Conlon JM. 1992. Structural characterization of tachykinins (neuropeptide gamma, neurokinin A, and substance P) from a reptile, Alligator mississipiensis. Gen Comp Endocrinol 88: 277-286.
96. Wang Y, Barton BA, Nielsen PF, Conlon JM. 1999a. Tachykinins (substance P and neuropeptide gamma) from the brains of the pallid sturgeon, Scaphirhynchus albus and the paddlefish, Polyodon spathula (Acipenseriformes). Gen Comp Endocrinol 116: 21-30.
97. Wang Y, Barton BA, Thim L, Nielsen PF, Conlon JM. 1999b. Purification and characterization of galanin and scyliorhinin I from the hybrid sturgeon, Scaphirhynchus platorynchus x Scaphirhynchus albus (Acipenseriformes). Gen Comp Endocrinol 113: 38-45.
98. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 2009. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
99. Waugh D, Wang Y, Hazon N, Balment RJ, Conlon JM. 1993. Primary structures and biological activities of substance-P-related peptides from the brain of the dogfish, Scyliorhinus canicula. Eur J Biochem 214: 469-474.
100. Waugh D, Sower S, Bjenning C, Conlon JM. 1994. Novel tachykinins from the brain of the sea lamprey, Petromyzon marinus, and the skate, Raja rhina. Peptides 15: 155-161.
101. Waugh D, Bondareva V, Rusakov Y, Bjenning C, Nielsen PF, Conlon JM. 1995a. Tachykinins with unusual structural features from a urodele, the amphiuma, an elasmobranch, the hammerhead shark, and an agnathan, the river lamprey. Peptides 16: 615-621.
102. Waugh D, Groff KE, Platzack B, Youson JH, Olson KR, Conlon JM. 1995b. Isolation, localization, and cardiovascular activity of tachykinins from the stomach of the bowfin Amia calva. Am J Physiol 269: R565-571.
103. Weld MM, Maler L. 1992. Substance P-like immunoreactivity in the brain of the gymnotiform fish Apteronotus leptorhynchus: presence of sex differences. J Chem Neuroanat 5: 107-129.
104. Weld MM, Kar S, Maler L, Quirion R. 1994. The distribution of tachykinin binding sites in the brain of an electric fish (Apteronotus leptorhynchus). J Chem Neuroanat 7: 123-139.
105. Zhang Y, Lu L, Furlonger C, Wu GE, Paige CJ. 2000. Hemokinin is a hematopoietic-specific tachykinin that regulates B lymphopoiesis. Nat Immunol 1: 392-397.
106. Zlomuzica A, Dere E, Huston JP, de Souza Silva MA. 2008. NK(3) receptor agonism promotes episodic-like memory in mice. Neurobiol Learn Mem 90: 420-425.