Functional characterization of an orexin neuropeptide in amphioxus reveals an ancient origin of orexin/orexin receptor system in chordate

  • Peng Wang
  • Meng Wang
  • Liping Zhang
  • Shenjie Zhong
  • Wanyue Jiang
  • Ziyue Wang
  • Chen Sun
  • Shicui ZhangEmail author
  • Zhenhui LiuEmail author
Research Paper


Amphioxus belongs to the subphylum cephalochordata, an extant representative of the most basal chordates, whose regulation of endocrine system remains ambiguous. Here we clearly demonstrated the existence of a functional orexin neuropeptide in amphioxus, which is able to interact with orexin receptor, activate both PKC and PKA pathways, decrease leptin expression, and stimulate lipogenesis. We also showed the transcription level of amphioxus orexin was affected by fasting or temperature, indicating a role of this gene in the regulation of energy balance. In addition, the expression of the amphioxus orexin was detected at cerebral vesicle, which has been proposed to be a homolog of the vertebrate brain. These data collectively suggest that a functional orexin neuropeptide has already emerged in amphioxus, which provide insights into the evolutionary origin of orexin in chordate and the functional homology between the cerebral vesicle and vertebrate brain.


amphioxus orexin neuropeptide evolution 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



This work was supported by the National Natural Science Foundation of China (31572259) and the Fundamental Research Funds for the Central Universities (201762003).

Supplementary material

11427_2018_9421_MOESM1_ESM.jpg (331 kb)
Supplementary material, approximately 228 KB.
11427_2018_9421_MOESM2_ESM.jpg (439 kb)
Supplementary material, approximately 228 KB.
11427_2018_9421_MOESM3_ESM.jpg (577 kb)
Supplementary material, approximately 228 KB.
11427_2018_9421_MOESM4_ESM.docx (25 kb)
Supplementary material, approximately 228 KB.


  1. Aitta-Aho, T., Pappa, E., Burdakov, D., and Apergis-Schoute, J. (2016). Cellular activation of hypothalamic hypocretin/orexin neurons facilitates short-term spatial memory in mice. Neurobiol Learn Mem 136, 183–188.CrossRefGoogle Scholar
  2. Alvarez, C.E., and Sutcliffe, J.G. (2002). Hypocretin is an early member of the incretin gene family. Neurosci Lett 324, 169–172.CrossRefGoogle Scholar
  3. Ammoun, S., Holmqvist, T., Shariatmadari, R., Oonk, H.B., Detheux, M., Parmentier, M., Akerman, K.E.O., and Kukkonen, J.P. (2003). Distinct recognition of OX1 and OX2 receptors by orexin peptides. J Pharm Exp Ther 305, 507–514.CrossRefGoogle Scholar
  4. Ammoun, S., Johansson, L., Ekholm, M.E., Holmqvist, T., Danis, A.S., Korhonen, L., Sergeeva, O.A., Haas, H.L., Akerman, K.E.O., and Kukkonen, J.P. (2006). OX1 orexin receptors activate extracellular signal-regulated kinase in chinese hamster ovary cells via multiple mechanisms: the role of Ca2+ influx in OX1 receptor signaling. Mol Endocrinol 20, 80–99.CrossRefGoogle Scholar
  5. Aston-Jones, G., Smith, R.J., Sartor, G.C., Moorman, D.E., Massi, L., Tahsili-Fahadan, P., and Richardson, K.A. (2010). Lateral hypothalamic orexin/hypocretin neurons: a role in reward-seeking and addiction. Brain Res 1314, 74–90.CrossRefGoogle Scholar
  6. Boss, C. (2014). Orexin receptor antagonists—a patent review (2010 to August 2014). Expert Opin Ther Patents 24, 1367–1381.CrossRefGoogle Scholar
  7. Boss, C., and Roch, C. (2015). Recent trends in orexin research—2010 to 2015. Bioorg Med Chem Lett 25, 2875–2887.CrossRefGoogle Scholar
  8. Broberger, C., De Lecea, L., Sutcliffe, J.G., and Hökfelt, T. (1998). Hypocretin/orexin- and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J Comp Neurol 402, 460–474.CrossRefGoogle Scholar
  9. Butterick, T.A., Billington, C.J., Kotz, C.M., and Nixon, J.P. (2013). Orexin: pathways to obesity resistance? Rev Endocr Metab Disord 14, 357–364.CrossRefGoogle Scholar
  10. Campos, P.H.R.F., Labussière, E., Hernández-García, J., Dubois, S., Renaudeau, D., and Noblet, J. (2014). Effects of ambient temperature on energy and nitrogen utilization in lipopolysaccharide-challenged growing pigs1. J Anim Sci 92, 4909–4920.CrossRefGoogle Scholar
  11. Candiani, S., Moronti, L., Ramoino, P., Schubert, M., and Pestarino, M. (2012). A neurochemical map of the developing amphioxus nervous system. BMC Neurosci 13, 59.CrossRefGoogle Scholar
  12. Chan, J.L., Heist, K., DePaoli, A.M., Veldhuis, J.D., and Mantzoros, C.S. (2003). The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men. J Clin Invest 111, 1409–1421.CrossRefGoogle Scholar
  13. Chen, C.T., Dun, S.L., Kwok, E.H., Dun, N.J., and Chang, J.K. (1999). Orexin A-like immunoreactivity in the rat brain. Neurosci Lett 260, 161–164.CrossRefGoogle Scholar
  14. Chen, X.Y., Chen, L., and Du, Y.F. (2017). Orexin-A increases the firing activity of hippocampal CA1 neurons through orexin-1 receptors. J Neurosci Res 95, 1415–1426.CrossRefGoogle Scholar
  15. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D. G., and Thompson, J.D. (2003). Multiple sequence alignment with the clustal series of programs. Nucl Acids Res 31, 3497–3500.CrossRefGoogle Scholar
  16. Christopher, J.A. (2014). Small-molecule antagonists of the orexin receptors. Pharm Patent Analyst 3, 625–638.CrossRefGoogle Scholar
  17. Cutler, D.J., Morris, R., Sheridhar, V., Wattam, T.A.K., Holmes, S., Patel, S., Arch, J.R.S., Wilson, S., Buckingham, R.E., Evans, M.L., et al. (1999). Differential distribution of orexin-A and orexin-B immunoreactivity in the rat brain and spinal cord. Peptides 20, 1455–1470.CrossRefGoogle Scholar
  18. Date, Y., Ueta, Y., Yamashita, H., Yamaguchi, H., Matsukura, S., Kangawa, K., Sakurai, T., Yanagisawa, M., and Nakazato, M. (1999). Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci USA 96, 748–753.CrossRefGoogle Scholar
  19. Davis, J.F., Choi, D.L., Benoit, S.C., 2011. Orexigenic hypothalamic peptides behavior and feeding. In: Preedy, V.R., Watson, R.R., Martin, C.R. (Eds). Handbook of Behavior, Food and Nutrition. Heidelberg: Springer, 361–362.Google Scholar
  20. Deadwyler, S.A., Porrino, L., Siegel, J.M., and Hampson, R.E. (2007). Systemic and nasal delivery of orexin-A (Hypocretin-1) reduces the effects of sleep deprivation on cognitive performance in nonhuman primates. J Neurosci 27, 14239–14247.CrossRefGoogle Scholar
  21. de Lecea, L., Kilduff, T.S., Peyron, C., Gao, X.B., Foye, P.E., Danielson, P. E., Fukuhara, C., Battenberg, E.L.F., Gautvik, V.T., Bartlett II, F.S., et al. (1998). The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95, 322–327.CrossRefGoogle Scholar
  22. Lecea, L., Sutcliffe, G.J., and Fabre, V. (2002). Hypocretins/orexins as integrators of physiological information: lessons from mutant animals. Neuropeptides 36, 85–95.CrossRefGoogle Scholar
  23. Diano, S., Horvath, B., Urbanski, H.F., Sotonyi, P., and Horvath, T.L. (2003). Fasting activates the nonhuman primate hypocretin (orexin) system and its postsynaptic targets. Endocrinology 144, 3774–3778.CrossRefGoogle Scholar
  24. Digby, J.E., Chen, J., Tang, J.Y., Lehnert, H., Matthews, R.N., and Randeva, H.S. (2006). Orexin receptor expression in human adipose tissue: effects of orexin-A and orexin-B. J Endocrinol 191, 129–136.CrossRefGoogle Scholar
  25. Ehrström, M., Gustafsson, T., Finn, A., Kirchgessner, A., Grybäck, P., Jacobsson, H., Hellström, P.M., and Näslund, E. (2005). Inhibitory effect of exogenous orexin a on gastric emptying, plasma leptin, and the distribution of orexin and orexin receptors in the gut and pancreas in man. J Clin Endocrinol Metab 90, 2370–2377.CrossRefGoogle Scholar
  26. Eisenhaber, F., and Bork, P. (1998). Wanted: subcellular localization of proteins based on sequence. Trends Cell Biol 8, 169–170.CrossRefGoogle Scholar
  27. España, R.A., Reis, K.M., Valentino, R.J., and Berridge, C.W. (2005). Organization of hypocretin/orexin efferents to locus coeruleus and basal forebrain arousal-related structures. J Comp Neurol 481, 160–178.CrossRefGoogle Scholar
  28. Farr, O.M., Gavrieli, A., and Mantzoros, C.S. (2015). Leptin applications in 2015. Curr Opin Endocrinol Diab Ob 22, 353–359.CrossRefGoogle Scholar
  29. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle Scholar
  30. Fronczek, R., van Geest, S., Frölich, M., Overeem, S., Roelandse, F.W.C., Lammers, G.J., and Swaab, D.F. (2012). Hypocretin (orexin) loss in Alzheimer's disease. Neurobiol Aging 33, 1642–1650.CrossRefGoogle Scholar
  31. Gatfield, J., Brisbare-Roch, C., Jenck, F., and Boss, C. (2010). Orexin receptor antagonists: a new concept in CNS disorders? ChemMedChem 5, 1197–1214.CrossRefGoogle Scholar
  32. Gundlach, A.L., Burazin, T.C., and Larm, J.A. (2001). Distribution, regulation and role of hypothalamic galanin systems: renewed interest in a pleiotropic peptide family. Clin Exp Pharm Physiol 28, 100–105.CrossRefGoogle Scholar
  33. Holland, L.Z. (2015). The origin and evolution of chordate nervous systems. Philos Trans R Soc B-Biol Sci 370, 20150048.CrossRefGoogle Scholar
  34. Holland, L.Z., Schubert, M., Kozmik, Z., and Holland, N.D. (1999). AmphiPax3/7, an amphioxus paired box gene: insights into chordate myogenesis, neurogenesis, and the possible evolutionary precursor of definitive vertebrate neural crest. Evol Dev 1, 153–165.CrossRefGoogle Scholar
  35. Horvath, T.L., Diano, S., and van den Pol, A.N. (1999). Synaptic interaction between hypocretin (orexin) and neuropeptide Y cells in the rodent and primate hypothalamus: a novel circuit implicated in metabolic and endocrine regulations. J Neurosci 19, 1072–1087.CrossRefGoogle Scholar
  36. Hu, B., Yang, N., Qiao, Q.C., Hu, Z.A., and Zhang, J. (2015). Roles of the orexin system in central motor control. Neurosci Biobehav Rev 49, 43–54.CrossRefGoogle Scholar
  37. Huesa, G., van den Pol, A.N., and Finger, T.E. (2005). Differential distribution of hypocretin (orexin) and melanin-concentrating hormone in the goldfish brain. J Comp Neurol 488, 476–491.CrossRefGoogle Scholar
  38. Jékely, G. (2013). Global view of the evolution and diversity of metazoan neuropeptide signaling. Proc Natl Acad Sci USA 110, 8702–8707.CrossRefGoogle Scholar
  39. Johansson, L., Ekholm, M.E., and Kukkonen, J.P. (2009). Regulation of OX1 orexin/hypocretin receptor-coupling to phospholipase C by Ca2+ influx. Br J Pharm 150, 97–104.CrossRefGoogle Scholar
  40. Kaslin, J., Nystedt, J.M., Östergård, M., Peitsaro, N., and Panula, P. (2004). The orexin/hypocretin system in zebrafish is connected to the aminergic and cholinergic systems. J Neurosci 24, 2678–2689.CrossRefGoogle Scholar
  41. Kelesidis, T., Kelesidis, I., Chou, S., and Mantzoros, C.S. (2010). Narrative review: the role of leptin in human physiology: emerging clinical applications. Ann Intern Med 152, 93–100.CrossRefGoogle Scholar
  42. Kotz, C., Nixon, J., Butterick, T., Perez-Leighton, C., Teske, J., and Billington, C. (2012). Brain orexin promotes obesity resistance. Ann New York Acad Sci 1264, 72–86.CrossRefGoogle Scholar
  43. Kukkonen, J.P., Holmqvist, T., Ammoun, S., and Akerman, K.E.O. (2002). Functions of the orexinergic/hypocretinergic system. Am J Physiol-Cell Physiol 283, C1567–C1591.CrossRefGoogle Scholar
  44. Kullgren, A., Jutfelt, F., Fontanillas, R., Sundell, K., Samuelsson, L., Wiklander, K., Kling, P., Koppe, W., Larsson, D.G.J., Björnsson, B.T., et al. (2013). The impact of temperature on the metabolome and endocrine metabolic signals in Atlantic salmon (Salmo salar). Comp Biochem Physiol A Mol Integr Physiol 164, 44–53.CrossRefGoogle Scholar
  45. Larsson, K.P., Peltonen, H.M., Bart, G., Louhivuori, L.M., Penttonen, A., Antikainen, M., Kukkonen, J.P., and Akerman, K.E.O. (2005). Orexin-A-induced Ca2+ entry. J Biol Chem 280, 1771–1781.CrossRefGoogle Scholar
  46. Leibowitz, S.F. (2005). Regulation and effects of hypothalamic galanin: relation to dietary fat, alcohol ingestion, circulating lipids and energy homeostasis. Neuropeptides 39, 327–332.CrossRefGoogle Scholar
  47. Li, J., Hu, Z., and de Lecea, L. (2014). The hypocretins/orexins: integrators of multiple physiological functions. Br J Pharm 171, 332–350.CrossRefGoogle Scholar
  48. Lund, P.E., Shariatmadari, R., Uustare, A., Detheux, M., Parmentier, M., Kukkonen, J.P., and Åkerman, K.E.O. (2000). The orexin OX1 receptor activates a novel Ca2+ influx pathway necessary for coupling to phospholipase C. J Biol Chem 275, 30806–30812.CrossRefGoogle Scholar
  49. Marcus, J.N., Aschkenasi, C.J., Lee, C.E., Chemelli, R.M., Saper, C.B., Yanagisawa, M., and Elmquist, J.K. (2001). Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 435, 6–25.CrossRefGoogle Scholar
  50. Mavanji, V., Butterick, T.A., Duffy, C.M., Nixon, J.P., Billington, C.J., and Kotz, C.M. (2017). Orexin/hypocretin treatment restores hippocampal-dependent memory in orexin-deficient mice. Neurobiol Learning Mem 146, 21–30.CrossRefGoogle Scholar
  51. Mei, S., Fei, W., and Zhou, S. (2011). Gene ontology based transfer learning for protein subcellular localization. BMC Bioinf 12, 44.CrossRefGoogle Scholar
  52. Mirabeau, O., and Joly, J.S. (2013). Molecular evolution of peptidergic signaling systems in bilaterians. Proc Natl Acad Sci USA 110, E2028–E2037.CrossRefGoogle Scholar
  53. Moellering, D.R., and Smith, D.L. (2012). Ambient temperature and obesity. Curr Obes Rep 1, 26–34.CrossRefGoogle Scholar
  54. Mondal, M.S., Nakazato, M., Date, Y., Murakami, N., Hanada, R., Sakata, T., and Matsukura, S. (1999a). Characterization of orexin-A and orexin-B in the microdissected rat brain nuclei and their contents in two obese rat models. Neurosci Lett 273, 45–48.CrossRefGoogle Scholar
  55. Mondal, M.S., Nakazato, M., Date, Y., Murakami, N., Yanagisawa, M., and Matsukura, S. (1999b). Widespread distribution of orexin in rat brain and its regulation upon fasting. Biochem Biophys Res Commun 256, 495–499.CrossRefGoogle Scholar
  56. Murakami, M., Ohba, T., Kushikata, T., Niwa, H., Kurose, A., Imaizumi, T., Watanabe, H., Yanagisawa, T., Nakaji, S., Ono, K., et al. (2015). Involvement of the orexin system in sympathetic nerve regulation. Biochem Biophys Res Commun 460, 1076–1081.CrossRefGoogle Scholar
  57. Nambu, T., Sakurai, T., Mizukami, K., Hosoya, Y., Yanagisawa, M., and Goto, K. (1999). Distribution of orexin neurons in the adult rat brain1 published on the World Wide Web on 17 March 1999.1. Brain Res 827, 243–260.CrossRefGoogle Scholar
  58. Nixon, J.P., Kotz, C.M., Novak, C.M., Billington, C.J., Teske, J.A., 2012. Neuropeptides controlling energy balance: orexins and neuromedins. Handb Exp Pharm 209: 77–109.CrossRefGoogle Scholar
  59. Nixon, J.P., and Smale, L. (2007). A comparative analysis of the distribution of immunoreactive orexin A and B in the brains of nocturnal and diurnal rodents. Behav Brain Funct 3, 28.CrossRefGoogle Scholar
  60. North, M.O., Bell, D.D. (1990). Commercial Chicken Production Manual. 4th edition. New York: Chapman Hall.Google Scholar
  61. Ohkubo, T., Boswell, T., and Lumineau, S. (2002). Molecular cloning of chicken prepro-orexin cDNA and preferential expression in the chicken hypothalamus. Biochim Biophys Acta 1577, 476–480.CrossRefGoogle Scholar
  62. Park, J.H., Shim, H.M., Na, A.Y., Bae, J.H., Im, S.S., and Song, D.K. (2015). Orexin A regulates plasma insulin and leptin levels in a time-dependent manner following a glucose load in mice. Diabetologia 58, 1542–1550.CrossRefGoogle Scholar
  63. Peyron, C., Tighe, D.K., van den Pol, A.N., de Lecea, L., Heller, H.C., Sutcliffe, J.G., and Kilduff, T.S. (1998). Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18, 9996–10015.CrossRefGoogle Scholar
  64. Putnam, N.H., Butts, T., Ferrier, D.E.K., Furlong, R.F., Hellsten, U., Kawashima, T., Robinson-Rechavi, M., Shoguchi, E., Terry, A., Yu, J. K., et al. (2008). The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064–1071.CrossRefGoogle Scholar
  65. Rauch, M., Riediger, T., Schmid, H.A., and Simon, E. (2000). Orexin A activates leptin-responsive neurons in the arcuate nucleus. Pflugers Arch-Eur J Physiol 440, 699–703.CrossRefGoogle Scholar
  66. Sakurai, T. (2003). Orexin: a link between energy homeostasis and adaptive behaviour. Curr Opin Clin Nutr Metab Care 6, 353–360.CrossRefGoogle Scholar
  67. Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R.M., Tanaka, H., Williams, S.C., Richardson, J.A., Kozlowski, G.P., Wilson, S., et al. (1998). Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573–585.CrossRefGoogle Scholar
  68. Sakurai, T., Moriguchi, T., Furuya, K., Kajiwara, N., Nakamura, T., Yanagisawa, M., and Goto, K. (1999). Structure and function of human prepro-orexin gene. J Biol Chem 274, 17771–17776.CrossRefGoogle Scholar
  69. Schwartz, M.W., Woods, S.C., Porte, D., Seeley, R.J., and Baskin, D.G. (2000). Central nervous system control of food intake. Nature 404, 661–671.CrossRefGoogle Scholar
  70. Sharf, R., Sarhan, M., Brayton, C.E., Guarnieri, D.J., Taylor, J.R., and DiLeone, R.J. (2010). Orexin signaling via the orexin 1 receptor mediates operant responding for food reinforcement. Biol Psychiatr 67, 753–760.CrossRefGoogle Scholar
  71. Shibahara, M., Sakurai, T., Nambu, T., Takenouchi, T., Iwaasa, H., Egashira, S.I., Ihara, M., and Goto, K. (1999). Structure, tissue distribution, and pharmacological characterization of Xenopus orexins. Peptides 20, 1169–1176.CrossRefGoogle Scholar
  72. Singletary, K.G., Delville, Y., Farrell, W.J., and Wilczynski, W. (2005). Distribution of orexin/hypocretin immunoreactivity in the nervous system of the green Treefrog, Hyla cinerea. Brain Res 1041, 231–236.CrossRefGoogle Scholar
  73. Skrzypski, M., T. Le, T., Kaczmarek, P., Pruszynska-Oszmalek, E., Pietrzak, P., Szczepankiewicz, D., Kolodziejski, P.A., Sassek, M., Arafat, A., Wiedenmann, B., et al. (2011). Orexin A stimulates glucose uptake, lipid accumulation and adiponectin secretion from 3T3-L1 adipocytes and isolated primary rat adipocytes. Diabetologia 54, 1841–1852.CrossRefGoogle Scholar
  74. Smart, D., Jerman, J.C., Brough, S.J., Rushton, S.L., Murdock, P.R., Jewitt, F., Elshourbagy, N.A., Ellis, C.E., Middlemiss, D.N., and Brown, F. (1999). Characterization of recombinant human orexin receptor pharmacology in a Chinese hamster ovary cell-line using FLIPR. Br J Pharm 128, 1–3.CrossRefGoogle Scholar
  75. Świtońska, M.M., Kaczmarek, P., Malendowicz, L.K., and Nowak, K.W. (2002). Orexins and adipoinsular axis function in the rat. Regul Pept 104, 69–73.CrossRefGoogle Scholar
  76. Takenoya, F., Hirayama, M., Kageyama, H., Funahashi, H., Kita, T., Matsumoto, H., Ohtaki, T., Katoh, S., Takeuchi, M., and Shioda, S. (2005). Neuronal interactions between galanin-like-peptide- and orexinor melanin-concentrating hormone-containing neurons. Regul Pept 126, 79–83.CrossRefGoogle Scholar
  77. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30, 2725–2729.CrossRefGoogle Scholar
  78. Tang, J., Chen, J., Ramanjaneya, M., Punn, A., Conner, A.C., and Randeva, H.S. (2008). The signalling profile of recombinant human orexin-2 receptor. Cell Signalling 20, 1651–1661.CrossRefGoogle Scholar
  79. Thorpe, A.J., Cleary, J.P., Levine, A.S., and Kotz, C.M. (2005). Centrally administered orexin A increases motivation for sweet pellets in rats. Psychopharmacology 182, 75–83.CrossRefGoogle Scholar
  80. Trivedi, P., Yu, H., MacNeil, D.J., Van der Ploeg, L.H.T., and Guan, X.M. (1998). Distribution of orexin receptor mRNA in the rat brain. FEBS Lett 438, 71–75.CrossRefGoogle Scholar
  81. Turunen, P.M., Ekholm, M.E., Somerharju, P., and Kukkonen, J.P. (2010). Arachidonic acid release mediated by OX1 orexin receptors. Br J Pharm 159, 212–221.CrossRefGoogle Scholar
  82. Volkoff, H., and Peter, R.E. (2001). Interactions between orexin A, NPY and galanin in the control of food intake of the goldfish, Carassius auratus. Regul Pept 101, 59–72.CrossRefGoogle Scholar
  83. Wall, A., and Volkoff, H. (2013). Effects of fasting and feeding on the brain mRNA expressions of orexin, tyrosine hydroxylase (TH), PYY and CCK in the Mexican blind cavefish (Astyanax fasciatus mexicanus). General Comp Endocrinol 183, 44–52.CrossRefGoogle Scholar
  84. Wang, H., Liu, B., Li, H., and Zhang, S. (2016). Identification and biochemical characterization of polyamine oxidases in amphioxus: implications for emergence of vertebrate-specific spermine and acetylpolyamine oxidases. Gene 575, 429–437.CrossRefGoogle Scholar
  85. Wang, M., Li, L., Guo, Q., Zhang, S., Ji, D., and Li, H. (2016). Identification and expression of a new Ly6 gene cluster in zebrafish Danio rerio, with implications of being involved in embryonic immunity. Fish Shellfish Immunol 54, 230–240.CrossRefGoogle Scholar
  86. Wang, P., Wang, M., Ji, G., Yang, S., Zhang, S., and Liu, Z. (2017). Demonstration of a functional kisspeptin/kisspeptin receptor system in amphioxus with implications for origin of neuroendocrine regulation. Endocrinology 158, 1461–1473.CrossRefGoogle Scholar
  87. Wang, Y., and Zhang, S. (2012). EF1α is a useful internal reference for studies of gene expression regulation in amphioxus Branchiostoma japonicum. Fish Shellfish Immunol 32, 1068–1073.CrossRefGoogle Scholar
  88. Westerterp-Plantenga, M.S., van Marken Lichtenbelt, W.D., Strobbe, H., and Schrauwen, P. (2002). Energy metabolism in humans at a lowered ambient temperature. Eur J Clin Nutr 56, 288–296.CrossRefGoogle Scholar
  89. Wu, Q., Wang, Y., Ding, Y., Ma, S., Wu, Z., and Wei, F. (2017). A natural communication system on genome evolution. Sci China Life Sci 60, 432–435.CrossRefGoogle Scholar
  90. Wu, X., Zhang, S., Wang, Y., Zhang, B., Qu, Y., Jiang, X. (1995). The life history of Branchiostoma belcheri tsingtauense: age, growth and death. Oceanol Limnol Sin 26, 175–178.Google Scholar
  91. Xu, H., Wang, J., Chang, Y., Xu, J., Wang, Y., Long, T., and Xue, C. (2014). Fucoidan from the sea cucumber Acaudina molpadioides exhibits anti-adipogenic activity by modulating the Wnt/β-catenin pathway and down-regulating the SREBP-1c expression. Food Funct 5, 1547–1555.CrossRefGoogle Scholar
  92. Xue, J.Y., Zhang, S.C., Liu, N.G., and Liu, Z.H. (2006). Verification, characterization and tissue-specific expression of UreG, a urease accessory protein gene, from the amphioxus Branchiostoma belcheri. Acta Biochim Biophys Sin 38, 549–555.CrossRefGoogle Scholar
  93. Yamamoto, T., Suzuki, H., Uemura, H., Yamamoto, K., and Kikuyama, S. (2004). Localization of orexin-A-like immunoreactivity in prolactin cells in the bullfrog (Rana catesbeiana) pituitary. General Comp Endocrinol 135, 186–192.CrossRefGoogle Scholar
  94. Yokobori, E., Kojima, K., Azuma, M., Kang, K.S., Maejima, S., Uchiyama, M., and Matsuda, K. (2011). Stimulatory effect of intracerebroventricular administration of orexin A on food intake in the zebrafish, Danio rerio. Peptides 32, 1357–1362.CrossRefGoogle Scholar

Copyright information

© Malaysian Rubber Board 2019

Authors and Affiliations

  • Peng Wang
    • 1
  • Meng Wang
    • 1
  • Liping Zhang
    • 1
  • Shenjie Zhong
    • 1
  • Wanyue Jiang
    • 1
  • Ziyue Wang
    • 1
  • Chen Sun
    • 1
  • Shicui Zhang
    • 1
    Email author
  • Zhenhui Liu
    • 1
    Email author
  1. 1.Institute of Evolution & Marine Biodiversity, College of Marine Life ScienceOcean University of ChinaQingdaoChina

Personalised recommendations