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. 2017 Apr 25;54(2):103–110. doi: 10.2141/jpsa.0160100

Gut Hormones and Regulation of Food Intake in Birds

Kazuhisa Honda 1,✉, Takaoki Saneyasu 1, Hiroshi Kamisoyama 1
PMCID: PMC7477125  PMID: 32908415

Abstract

Gut hormones act as appetite regulatory hormones in mammals. For example, the hunger hormone ghrelin, which is released from the stomach before food intake, stimulates appetite. In contrast, satiety hormones such as cholecystokinin, glucagon-like peptide-1, and peptide YY, which are released from the intestines after food intake, suppress appetite. The effects of these peptides on food intake have been shown to be similar in both mammals and fishes. However, evidence suggests that the physiological roles of these gut hormones may be different between birds and other vertebrates. This review summarizes the current information on the roles of gut hormones in the regulation of food intake in birds, especially in chickens.

Keywords: brain, chicken, gut hormones, hypothalamus, intestine

Introduction

The appetite regulatory system has been a focus of research for more than half a century (Woods, 2013). The brain integrates information from peripheral hormones, such as leptin, insulin and gut hormones, and consequently regulates food intake: adiposity hormones such as leptin and insulin are secreted in proportion to body fat and suppress food intake, whereas gut hormones are secreted before or after meals and regulate food intake (Woods, 2009; Sam et al., 2012; Williams and Elmquist, 2012). In chickens, central administration of leptin (Denbow et al., 2000) and insulin (Honda et al., 2007; Shiraishi et al., 2008) suppresses food intake. However, there is much debate on the physiological significance of leptin and insulin as adiposity hormones in birds. For example, the mRNA levels of leptin in adipose tissue were extremely low in chickens (Seroussi et al., 2016), zebra finches (Huang et al., 2014), and rock doves (Friedman-Einat et al., 2014) and relatively low in Japanese quail (Seroussi et al., 2016). Plasma insulin levels were not correlated with either abdominal fat mass or the mRNA levels of appetite-regulating neuropeptides in the hypothalamus in layer chickens (Honda et al., 2015a). Therefore, leptin and insulin may not be primarily involved as adiposity hormones in the regulation of food intake in chickens. Birds need to fly. Therefore, birds may have developed so as not to increase their body fat mass for flying. The physiological roles of adiposity signals in the appetite regulatory system might be lost in birds or developed subsequently in mammals. In other words, the appetite-regulating role of gut hormones in birds might be physiologically more important than that in mammals.

Many studies on the regulatory mechanism of food intake have revealed that gut hormones, such as ghrelin, cholecystokinin (CCK), glucagon-like peptide (GLP) -1, and peptide YY (PYY) play critical roles in the regulation of food intake in mammals. Ghrelin is released from the stomach and transmits the hunger signal to the brain before food intake, resulting in the stimulation of appetite. CCK, GLP-1, and PYY are released from the intestines and transmit satiety signals to the brain after food intake, resulting in the suppression of appetite (Woods, 2009; Sam et al., 2012; Williams and Elmquist, 2012). Recent studies on various species of fish have demonstrated the orexigenic effect of ghrelin (Riley et al., 2005; Matsuda et al., 2006a, 2006b; Penney and Volkoff, 2014) and anorexigenic effects of CCK (Himick and Peter, 1994; Volkoff et al., 2003; Penney and Volkoff, 2014; White et al., 2016), GLP-1 (Silverstain et al., 2001; White et al., 2016), and PYY (Gonzalez and Unniappan, 2010, 2016; Chen et al., 2013, 2015). These findings suggest that the appetite-regulating roles of the gut hormones may have been conserved among vertebrates. All the gut hormone genes are expressed in the gastrointestinal tract of chickens (Fig. 1): ghrelin mRNA is densely expressed in the proventriculus, the glandular stomach of chickens, whereas mRNAs of CCK, PYY, and proglucagon (the precursor of GLP-1) are expressed in the small intestine. These gut hormones might provide information about gastrointestinal transit and emptying to the brain. However, an increasing amount of evidence suggests the hypothesis that the physiological roles of these gut hormones in birds somewhat differ from those of other vertebrates. In this review, we summarize the current information on the possible role of gut hormones in the regulation of food intake in birds.

Fig. 1.

Fig. 1.

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Comparison of the mRNA levels of ghrelin, cholecystokinin (CCK), peptide YY (PYY) and proglucagon in the gastrointestinal tract of 8-day-old broiler chicks. Real-time PCR analysis was performed to quantify the mRNA levels of the gut hormones. The mRNA levels of ribosomal protein S17 (RPS17) were also analyzed as the internal standard. Values represent the mean±SEM of four birds. Different letters above each bar denote statistical significance (P<0.05, Tukey-Kramer test). Complementary DNAs of ghrelin and CCK were amplified with the primers as follows: ghrelin sense, 5′-CCC ACA TAT AAA AAC ATA CAG CAA CA-3′; ghrelin antisense, 5′-GCC TCG GCG ATG TAA TCT TG-3′; CCK sense, 5′-GCG CTG CTG GCC AAG TA-3′; and CCK antisense, 5′-GAC AGA GAA CCT CCC AGT GGA A-3′. Complementary DNAs of PYY, proglucagon, and RPS17 were amplified with the primers described previously (Honda et al., 2015d, Aoki et al., 2017). This experiment was approved by the Institutional Animal Care and Use Committee (Permission number: 25-08-01) and carried out according to the Kobe University Animal Experimental Regulation.

Ghrelin

Ghrelin is a peptide that was purified and identified in the stomach of rats as an endogenous ligand specific for the growth-hormone secretagogue receptor (Kojima et al., 1999). Wren et al. (2000) first reported that intraperitoneal (IP) administration of ghrelin stimulated food intake in freely feeding rats. They also demonstrated that ghrelin is the first circulating hormone to stimulate food intake in humans (Wren et al., 2000). However, a number of studies on ghrelin suggest that ghrelin functions as an anorexigenic peptide in birds (Table 1). For example, peripheral administration of ghrelin suppressed food intake in broiler chicks (Buyse et al., 2009; Geelissen et al., 2006; Ocłoń, 2011). These findings suggest that ghrelin does not function as a peripheral hunger hormone in chickens.

Table 1. Effects of peripheral administration of gut hormones on food intake in birds.

Hormone Food intake Bird Dose Rout Reference
Orexigenic hormone in mammals
    Ghrelin Decreased Broiler chicken 1 nmol/bird IV Buyse et al., 2009
Decreased Broiler chicken 10 nmol/kg BW IV Geelissen et al., 2006
Decreased Broiler chicken 5–20 nmol/kg BW IP Ocłon, 2011
No change Layer chicken 500 pmol/bird IV Kaiya et al., 2007
Decreased Japanese quail 3 nmol/bird IP Shousha et al., 2005a
Increased Japanese quail 0.5–1 nmol/bird IP Shousha et al., 2005a
 
Anorexigenic hormones in mammals
    Cholecystokinin Decreased Layer chicken 2–8µg/kg BW IV Savory and Gentle, 1983
Decreased Broiler chicken 3.5–28µg/kg BW IP Covasa and Forbes, 1994
Decreased Layer chicken 10 nmol/kg BW IV Rodríguez-Sinovas et al., 1997
Decreased Layer chicken 60–300 nmol/kg BW IP Tachibana et al., 2012
    Glucagon-like peptide-1 Decreased Japanese quail 0.5–1 nmol/bird IP Shousha et al., 2007
No change Layer chicken 0.12–3 nmol/bird IP Tachibana et al., 2003
    Glucagon-like peptide-2 Decreased Broiler chicken 1.5 nmol/kg BW IV Honda et al., 2015d
    Peptide YY Decreased Broiler chicken 3–6 nmol/kg BW IV Aoki et al., 2017
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Abbreviations used: BW, body weight; IV, intravascular administration; IP, intraperitoneal administration

Ghrelin mRNA is densely expressed in the proventriculus of chickens (Kaiya et al., 2002) and ducks (Shao et al., 2010). Ghrelin mRNA and immunopositive cells have been detected in both the proventriculus and small intestine of the ostrich (Wang et al., 2009, 2011). In layer chicks and Japanese quail, plasma ghrelin levels were elevated after fasting, and the elevation of plasma ghrelin was reversed by refeeding (Shousha et al., 2005a; Kaiya et al., 2007). Avian ghrelin receptors have been identified in chickens (Tanaka et al., 2003), Japanese quail (Kitazawa et al., 2009), and ducks (Nie et al., 2009) and are widely distributed in the brain (Geelissen et al., 2003; Tanaka et al., 2003; Nie et al., 2009) and peripheral tissues (Geelissen et al., 2003; Tanaka et al., 2003; Kitazawa et al., 2009; Nie et al., 2009). Shousha et al. (2005a) reported that IP administration of low doses (0.5–1 nmol/bird) of ghrelin stimulated food intake in Japanese quail, although the highest dose (3 nmol/bird) of ghrelin suppressed food intake. These results are similar to the results of mammalian studies, although the effect of ghrelin on food intake in chickens differed from that in mammals. Chickens might not feel hungry, even when there are no digesta in their stomachs. However, the physiological roles of ghrelin might be different between bird species. Further studies are required to evaluate whether ghrelin suppresses food intake in other avian species.

Cholecystokinin

CCK is produced in the small intestines of chickens and ostrich (Jonson et al., 2000) and both small and large intestines of ducks (Castaldo and Lucini, 1991, 1994). Dietary protein, amino acids, and fat stimulate CCK release in chickens (Furuse, 1999). Peripheral administration of CCK suppressed food intake in chickens (Table 1) (Savory and Gentle, 1983; Covasa and Forbes, 1994; Rodríguez-Sinovas et al., 1997; Tachibana et al., 2012), and the satiety effect of CCK has been suggested to be mediated by the vagus nervous system in broiler chickens (Covasa and Forbes, 1994) as well as mammals (Ritter and Ladenheim, 1985; Smith et al., 1985; Moran et al., 1997). Administration of type A CCK receptor antagonist, but not type B receptor antagonist, increases the meal size in mammals (Moran et al., 1993; Beglinger et al., 2001; Reidelberger et al., 2003). Chicken CCK receptors have been cloned and widely expressed in the brain and peripheral tissues (Nilsson et al., 2003; Ohkubo et al., 2007). Dunn et al. (2013) reported that chickens with the high-growth type A CCK receptor haplotype are resistant to the anorectic effect of exogenously administered CCK. They suggested that the satiety set point was altered, and decreased expression of the type A CCK receptor was responsible for increased growth and body weight during the domestication of chickens. However, the physiological importance of CCK in chickens as a satiety hormone has not yet been elucidated. For example, potent stimulators of CCK release did not alter the food intake of chickens (Furuse, 1999). Devazepide, a cholecystokinin-A receptor antagonist, did not increase the food intake of chickens (Choi et al., 1994). Further studies are required to evaluate the physiological importance of CCK among various gut hormones in chickens.

Glucagon-like peptide-1

GLP-1 is released from the intestine in response to food ingestion in mammals (Tolhurst et al., 2009). A meta analysis revealed that intravascular administration of GLP-1 reduces energy intake in humans (Verdich et al., 2001). GLP-1 can directly stimulate anorectic pathways in the brain or indirectly stimulate them through the vagus nervous system (Abbott et al., 2005a; Van Bloemendaal et al., 2014). In chickens, frequencies of occurrence of GLP-1-immunoreactive cells were influenced by food deprivation (Monir et al., 2014a), dietary protein levels (Monir et al., 2014b), and dietary amino acids (Nishimura et al., 2015). GLP-1 immunoreactive cells were detected in the small intestine of ducks (Ding et al., 2013). GLP-1 receptor mRNA is widely distributed in both the brain and gastrointestinal tract of chickens (Huang et al., 2012). IP administration of GLP-1 significantly suppressed the food intake of Japanese quail (Shousha et al., 2007). However, the physiological importance of GLP-1 in birds as a satiety hormone has not yet been elucidated. For example, IP administration of GLP-1 did not influence food intake and crop emptying in layer chicks (Tachibana et al., 2003). In contrast, IP administration of GLP-1 suppresses food intake in Japanese quail (Shousha et al., 2007). Richards and McMurtry (2008) reported that plasma GLP-1 levels were not influenced by fasting and refeeding in broiler chickens. Further studies are required to evaluate the physiological importance of GLP-1 among various gut hormones in birds.

Glucagon-like peptide-2

GLP-2 is produced from the same precursor of GLP-1 in mammals (Janssen et al., 2013) and chickens (Honda, 2016). Immunohistochemical and morphometric studies of chickens suggest that GLP-2 colocalizes with GLP-1 in the same secretory granules of L cells in the small intestine of chickens (Monir et al., 2014c; Nishimura et al., 2013). Intravascular administration of GLP-2 suppressed the food intake of chicks (Honda et al., 2015d). GLP-2 receptor mRNA is expressed in the brain and gastrointestinal tract of chickens (Richards & McMurtry, 2008; Mo et al., 2014). Therefore, it is possible that GLP-2 acts as a postprandial satiety hormone in chickens. Studies on humans have not reported the satiety effect of peripheral GLP-2 (Schmidt et al., 2003; Sorensen et al., 2003). The most apparent role for GLP-2 is its promotion of growth and function of the intestinal mucosa in mammals (Janssen et al., 2013). Thus, the physiological role of GLP-2 may be different between mammals and chickens.

Peptide YY

In 1992, PYY was isolated from the small intestine of adult layer chickens (Conlon and O'Harte, 1992). Amino acid sequence analysis revealed the presence of an additional N-terminal alanine residue, and an extract of the chicken intestine did not contain PYY3–36, the major form of PYY in mammals (Conlon and O'Harte, 1992). PYY-immunoreactive cells were detected in the duodenum and jejunum of chickens (El-Salhy et al., 1982). In contrast, PYY was abundantly expressed in the large intestine rather than the small intestine of mammals (Ekblad and Sundler, 2002; Zhou et al., 2006; Ueno et al., 2008). Recently, we identified the full-length cDNA sequence for chicken PYY and found that the PYY mRNA was densely expressed in the small intestine but not in the large intestines of chicks (Aoki et al., 2017). These findings clearly demonstrate that the N-terminal sequence of PYY and the production sites of PYY in the gastrointestinal tract are different between mammals and chickens.

The plasma concentration of PYY is elevated after feeding (Zwirska-Korczala et al., 2007; Stadlbauer et al., 2013) and after the intraintestinal administration of nutrients in mammals (Fu-Cheng et al., 1995). Peripheral administration of PYY3-36 reduces food intake in humans and rodents (Batterham et al., 2002; Martin et al., 2004; Degen et al., 2005; Scott et al., 2005; Chelikani et al., 2007). Peripheral PYY3-36 transmits satiety signals to the brain via the neuropeptide Y receptor Y2 (Y2R) in the hypothalamus and/or gastric vagal afferent nerves in mammals (McGowan and Bloom, 2004; Abbott et al., 2005b; Ueno et al., 2008). In chickens, PYY mRNA levels were significantly higher under ad libitum feeding conditions than under 12-h-fasting conditions (Aoki et al., 2017). An in vitro binding assay demonstrated that chicken PYY preferentially binds to Y2R (Salaneck et al., 2000). Y2R mRNA was expressed in the brain and peripheral tissues of chickens (Bromee et al., 2006). We recently found that the intravascular administration of chicken PYY significantly decreased the food intake of chicks in a dose-dependent manner (Aoki et al., 2017). These findings suggest that PYY may function as a satiety hormone in chickens as well as mammals.

Conclusions and Future Research

The appetite regulatory system of chickens has been a focus of research in recent decades. Increasing evidence has raised the hypothesis that the physiological roles of CCK, GLP-1, and PYY as satiety hormones have been conserved during the evolutional process in chickens. In addition, the anorexigenic action of other peptides expressed in the gastrointestinal tract, such as GLP-2 (Honda et al., 2015c), oxyntomodulin (Honda et al., 2014), growth hormone releasing hormone (Tachibana et al., 2015), and neuromedin U (Shousha et al., 2005b; Kamisoyama et al., 2007; Honda et al., 2015b), has been reported in birds. Birds need to fly. Therefore, birds may have developed not to increase intestinal content as much as possible. The satiety system regulated by gut hormones in birds may be more complex than we thought. The combinational effect of gut hormones, routes that mediate the satiety signals to the brain, and the mechanism underlying the integration of peripheral satiety signals in the brain need to be clarified. However, it is possible that unknown adipokines function as appetite-regulating hormones and/or influence the appetite-regulating effect of gut hormones in birds. Further studies might also be needed to clarify the relationship between adipokines and gut hormones in the appetite regulatory system in birds. Recent technical advances in avian transgenesis allow efficient extensions of experimental protocols and research areas (Park et al., 2013; Naito 2015), and therefore, in the future, highly developed genome editing technology will contribute to understanding the physiological importance of each gut hormone in birds.

Acknowledgments

We thank Miss Mika Okuda (Graduate school of agricultural science, Kobe University) and Mr. Shungo Nakayama (Faculty of Agriculture, Kobe University) for helpful assistance.

References

  1. Abbott CR, Monteiro M, Small CJ, Sajedi A, Smith KL, Parkinson JR, Ghatei MA, Bloom SR. The inhibitory effects of peripheral administration of peptide YY (3–36) and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagal-brainstem-hypothalamic pathway. Brain Research, 1044: 127-131. 2005. a. [DOI] [PubMed] [Google Scholar]
  2. Abbott CR, Small CJ, Kennedy AR, Neary NM, Sajedi A, Ghatei MA, Bloom SR. Blockade of the neuropeptide Y Y2 receptor with the specific antagonist BIIE0246 attenuates the effect of endogenous and exogenous peptide YY(3-36) on food intake. Brain Research, 1043: 139-144. 2005. b. [DOI] [PubMed] [Google Scholar]
  3. Aoki K, Kondo M, Okuda M, Saneyasu T, Honda K, Kamisoyama H. Identification, expression analysis, and functional characterization of peptide YY in chickens (Gallus gallus domesticus). General and Comparative Endocrinology, 242: 11-17. 2017. [DOI] [PubMed] [Google Scholar]
  4. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, Wren AM, Brynes AE, Low MJ, Ghatei MA, Cone RD, Bloom SR. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature, 418: 650-654. 2002. [DOI] [PubMed] [Google Scholar]
  5. Beglinger C, Degen L, Matzinger D, D'Amato M, Drewe J. 2001. Loxiglumide, a CCK-A receptor antagonist, stimulates calorie intake and hunger feelings in humans. American Journal of Physiology, Regulatory, Integrative and Comparative Physiology, 280: R1149-R1154. 2001. [DOI] [PubMed] [Google Scholar]
  6. Bromée T, Sjödin P, Fredriksson R, Boswell T, Larsson TA, Salaneck E, Zoorob R, Mohell N, Larhammar D. Neuropeptide Y-family receptors Y6 and Y7 in chicken. Cloning, pharmacological characterization, tissue distribution and conserved synteny with human chromosome region. FEBS Journal, 273: 2048-2063. 2006. [DOI] [PubMed] [Google Scholar]
  7. Buyse J, Janssen S, Geelissen S, Swennen Q, Kaiya H, Darras VM, Dridi S. Ghrelin modulates fatty acid synthase and related transcription factor mRNA levels in a tissue-specific manner in neonatal broiler chicks. Peptides, 30: 1342-1347. 2009. [DOI] [PubMed] [Google Scholar]
  8. Castaldo L, Lucini C. An immunohistochemical study on the endocrine cells in the gastrointestinal tract of domestic duck. European Journal of Basic and Applied Histochemistry, 35: 131-143. 1991. [PubMed] [Google Scholar]
  9. Castaldo L, Lucini C. Ontogenesis of some endocrine cells in the duck gastrointestinal tract. European Journal of Histochemistry, 38: 319-26. 1994. [PubMed] [Google Scholar]
  10. Chelikani PK, Haver AC, Reidelberger RD. Effects of intermittent intraperitoneal infusion of salmon calcitonin on food intake and adiposity in obese rats. American Journal of Physiology, Regulatory, Integrative and Comparative Physiology, 293: 1798-1808. 2007. [DOI] [PubMed] [Google Scholar]
  11. Chen H, Zhang X, Hao J, Chen D, Liu J, Gao Y, Zhu J, Wu H, Lin F, Pu Y, Yuan D, Wei R, Zhou C, Wang T, Li Z. Molecular cloning, expression analysis, and appetite regulatory effect of peptide YY in Siberian sturgeon (Acipenser baerii). Gene, 563: 172-179. 2015. [DOI] [PubMed] [Google Scholar]
  12. Chen Y, Shen Y, Pandit NP, Fu J, Li D, Li J. Molecular cloning, expression analysis, and potential food intake attenuation effect of peptide YY in grass carp (Ctenopharyngodon idellus). General and Comparative Endocrinology, 187: 66-73. 2013. [DOI] [PubMed] [Google Scholar]
  13. Choi YH, Furuse M, Satoh S, Okumura J. Endogenous cholecystokinin is not a major regulator of food intake in the chicken. Journal of Comparative Physiology B, 164: 425-429. 1994. [DOI] [PubMed] [Google Scholar]
  14. Conłon JM, O'Harte F. The primary structure of a PYY-related peptide from chicken intestine suggests an anomalous site of cleavage of the signal peptide in preproPYY. FEBS Letters, 313: 225-228. 1992. [DOI] [PubMed] [Google Scholar]
  15. Covasa M, Forbes JM. Exogenous cholecystokinin octapeptide in broiler chickens: satiety, conditioned colour aversion, and vagal mediation. Physiology & Behavior, 56: 39-49. 1994. [DOI] [PubMed] [Google Scholar]
  16. Degen L, Oesch S, Casanova M, Graf S, Ketterer S, Drewe J, Beglinger C. Effect of peptide YY3-36 on food intake in humans. Gastroenterology, 129: 1430-1436. 2005. [DOI] [PubMed] [Google Scholar]
  17. Denbow DM, Meade S, Robertson A, McMurtry JP, Richards M, Ashwell C. Leptin-induced decrease in food intake in chickens. Physiology & Behavior, 69: 359-362. 2000. [DOI] [PubMed] [Google Scholar]
  18. De Silva A, Bloom SR. Gut hormones and appetite control: A focus on PYY and GLP-1 as therapeutic targets in obesity. Gut and Liver, 6: 10-20. 2012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ding B, Lenzi C, Pirone A. Immunohistochemical study on glucagon-like peptide-1 (GLP-1) and pituitary adenylate cyclase activating peptide (PACAP) in the small intestine of muscovy duck during the prehatching and posthatching periods. Journal of Poultry Science, 51: 35-41. 2013. [Google Scholar]
  20. Dunn IC, Meddle SL, Wilson PW, Wardle CA, Law AS, Bishop VR, Hindar C, Robertson GW, Burt DW, Ellison SJ, Morrice DM, Hocking PM. Decreased expression of the satiety signal receptor CCKAR is responsible for increased growth and body weight during the domestication of chickens. American Journal of Physiology, Endocrinology and Metabolism, 304: E909-921. 2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ekblad E, Sundler F. Distribution of pancreatic polypeptide and peptide YY. Peptides, 23: 251-261. 2002. [DOI] [PubMed] [Google Scholar]
  22. El-Salhy M, Wilander E, Grimelius L, Terenius L, Lundberg JM, Tatemoto K. The distribution of polypeptide YY (PYY) - and pancreatic polypeptide (PP) - immunoreactive cells in the domestic fowl. Histochemistry, 75: 25-30. 1982. [DOI] [PubMed] [Google Scholar]
  23. Friedman-Einat M., Cogburn LA, Yosefi S, Hen G, Shinder D, Shirak A, Seroussi E. Discovery and characterization of the first genuine avian leptin gene in the rock dove (Columba livia). Endocrinology 155: 3376-3384. 2014. [DOI] [PubMed] [Google Scholar]
  24. Fu-Cheng X., Anini Y., Chariot J., Voisin T., Galmiche J.P., Rozé C., 1995. Peptide YY release after intraduodenal, intraileal, and intracolonic administration of nutrients in rats. Pflugers Archiv 431, 66-75. [DOI] [PubMed] [Google Scholar]
  25. Furuse M. Release and endogenous actions of the gastrin/cholecystokinin (CCK) family in the chicken. Journal of Experimental Zoology, 283: 448-454. 1999. [PubMed] [Google Scholar]
  26. Geelissen SME, Beck IME, Darras VM, Kuhn ER, Van der Geyten S. Distribution and regulation of chicken growth hormone secretagogue receptor isoforms. General and Comparative Endocrinology, 134: 167-174. 2003. [DOI] [PubMed] [Google Scholar]
  27. Geelissen SM, Swennen Q, Geyten SV, Kühn ER, Kaiya H, Kangawa K, Decuypere E, Buyse J, Darras VM. Peripheral ghrelin reduces food intake and respiratory quotient in chicken. Domestc Animal Endocrinology, 30: 108-116. 2006. [DOI] [PubMed] [Google Scholar]
  28. Gonzalez R, Unniappan S. Molecular characterization, appetite regulatory effects and feeding related changes of peptide YY in goldfish. General and Comparative Endocrinology, 166: 273-279. 2010. [DOI] [PubMed] [Google Scholar]
  29. Gonzalez R, Unniappan S. Mass spectrometry-assisted confirmation of the inability of dipeptidyl peptidase-4 to cleave goldfish peptide YY (1–36) and the lack of anorexigenic effects of peptide YY(3–36) in goldfish (Carassius auratus). Fish Physiology and Biochemistry, 42: 831-44. 2016. [DOI] [PubMed] [Google Scholar]
  30. Himick BA, Peter RE. CCK/gastrin-like immunoreactivity in brain and gut, and CCK suppression of feeding in goldfish. American Journal of Physiology, 267: R841-R851. 1994. [DOI] [PubMed] [Google Scholar]
  31. Honda K. Glucagon-related peptides and the regulation of food intake in chickens. Animal Science Journal, 87: 1090-1098. 2016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Honda K, Kamisoyama H, Saneyasu T, Sugahara K, Hasegawa S. Central administration of insulin suppresses food intake in chicks. Neuroscience Letters, 423: 153-157. 2007. [DOI] [PubMed] [Google Scholar]
  33. Honda K, Saneyasu T, Aoki K, Shimatani T, Yamaguchi T, Kamisoyama H, Correlation analysis of hypothalamic mRNA levels of appetite regulatory neuropeptides and several metabolic parameters in 28-day-old layer chickens. Animal Science Journal, 86: 517-522. 2015. a. [DOI] [PubMed] [Google Scholar]
  34. Honda K, Saneyasu T, Okuda M, Uemura T, Kamisoyama H. Glucagon and neuromedin U suppress food intake in broiler chicks. Journal of Poultry Science, 52: 268-278. 2015. b. [Google Scholar]
  35. Honda K, Saneyasu T, Shimatani T, Aoki K, Yamaguchi T, Nakanishi K, Kamisoyama H. Intracerebroventricular administration of chicken glucagon-like peptide-2 potently suppresses food intake in chicks. Animal Science Journal. 86: 312-318. 2015. c. [DOI] [PubMed] [Google Scholar]
  36. Honda K, Saneyasu T, Yamaguchi T, Shimatani T, Aoki K, Nakanishi K, Kamisoyama H. Intracerebroventricular administration of chicken oxyntomodulin suppresses food intake and increases plasma glucose and corticosterone concentrations in chicks, Neuroscience Letters, 564: 57-61. 2014. [DOI] [PubMed] [Google Scholar]
  37. Honda K, Shimatani T, Aoki K, Yamaguchi T, Kondo M, Saneyasu T, Kamisoyama H. Glucagon-like peptide-2 functions as anorexigenic peptide not only in the central nervous system but also in the peripheral circulation in broiler chicks. Journal of Poultry Science, 3: 183-187. 2015. d. [Google Scholar]
  38. Huang G, Li J, Fu H, Yan Z, Bu G, He X, Wang Y. Characterization of glucagon-like peptide 1 receptor (GLP1R) gene in chickens: functional analysis, tissue distribution, and identification of its transcript variants. Domestic Animal Endocrinology 43: 1-15. 2012. [DOI] [PubMed] [Google Scholar]
  39. Huang G, Li J, Wang H, Lan X, Wang Y. Discovery of a novel functional leptin protein (LEP) in zebra finches: evidence for the existence of an authentic avian leptin gene predominantly expressed in the brain and pituitary. Endocrinology, 155: 3385-3396. 2014. [DOI] [PubMed] [Google Scholar]
  40. Janssen P, Rotondo A, Mule F, Tack J. Review article: a comparison of glucagon-like peptides 1 and 2. Alimentary Pharmacology & Therapeutics, 37: 18-36. 2013. [DOI] [PubMed] [Google Scholar]
  41. Jonson L, Schoeman N, Saayman H, Naude R, Jensen H, Johnsen AH. Identification of ostrich and chicken cholecystokinin cDNA and intestinal peptides. Peptides, 21: 1337-1344. 2000. [DOI] [PubMed] [Google Scholar]
  42. Kaiya H, Van Der Geyten S, Kojima M, Hosoda H, Kitajima Y, Matsumoto M, Geelissen S, Darras VM, Kangawa K. Chicken ghrelin: purification, cDNA cloning, and biological activity. Endocrinology, 143: 3454-3463. 2002. [DOI] [PubMed] [Google Scholar]
  43. Kaiya H, Saito ES, Tachibana T, Furuse M, Kangawa K. Changes in ghrelin levels of plasma and proventriculus and ghrelin mRNA of proventriculus in fasted and refed layer chicks. Domestic Animal Endocrinology, 32: 247-259. 2007. [DOI] [PubMed] [Google Scholar]
  44. Kamisoyama H, Honda K, Saneyasu T, Sugahara K, Hasegawa S. 2007. Central administration of neuromedin U suppresses food intake in chicks. Neuroscience Letters, 420: 1-5. 2007. [DOI] [PubMed] [Google Scholar]
  45. Kitazawa T, Maeda Y, Kaiya H. Molecular cloning of growth hormone secretagogue-receptor and effect of quail ghrelin on gastrointestinal motility in Japanese quail. Regulatory Peptides, 158: 132-42. 2009. [DOI] [PubMed] [Google Scholar]
  46. Kojima M, Hosoda H, Date Y, Nakazato M, Matuso H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide. Nature, 402: 656-660. 1999. [DOI] [PubMed] [Google Scholar]
  47. Martin NM, Small CJ, Sajedi A, Patterson M, Ghatei MA, Bloom SR. Pre-obese and obese agouti mice are sensitive to the anorectic effects of peptide YY(3–36) but resistant to ghrelin. International Journal of Obesity and Related Metabolic Disorders, 28: 886-893. 2004. [DOI] [PubMed] [Google Scholar]
  48. Matsuda K, Miura T, Kaiya H, Maruyama K, Shimakura S, Uchiyama M, Kangawa K, Shioda S. Regulation of food intake by acyl and des-acyl ghrelins in the goldfish. Peptides, 27: 2321-2325. 2006. a. [DOI] [PubMed] [Google Scholar]
  49. Matsuda K, Miura T, Kaiya H, Maruyama K, Uchiyama M, Kangawa K, Shioda S. Stimulatory effect of n-octanoylated ghrelin on locomotor activity in the goldfish, Carassius auratus. Peptides, 27: 1335-1340. 2006. b. [DOI] [PubMed] [Google Scholar]
  50. McGowan BM, Bloom SR. Peptide YY and appetite control. Current Opinion in Pharmacology, 4: 583-588. 2004. [DOI] [PubMed] [Google Scholar]
  51. Mo C, Zhong Y, Wang Y, Yan Z, Li J. Characterization of glucagon-like peptide 2 receptor (GLP2R) gene in chickens: functional analysis, tissue distribution, and developmental expression profile of GLP2R in embryonic intestine. Domestic Animal Endocrinology, 48, 1-6. 2014. [DOI] [PubMed] [Google Scholar]
  52. Monir MM, Hiramatsu K, Matsumoto S, Nishimura K, Takemoto C, Shioji T, Watanabe T, Kita K, Yonekura S, Roh SG. Influences of protein ingestion on glucagon-like peptide (GLP) -1-immunoreactive endocrine cells in the chicken ileum. Animal Science Journal, 85, 581-587. 2014. a. [DOI] [PubMed] [Google Scholar]
  53. Monir MM, Hiramatsu K, Yamasaki A, Nishimura K, Watanabe T. The influence of restricted feeding on glucagon-like peptide-1 (GLP-1) -containing cells in the chicken small intestine. Anatomia, Histologia, Embryologia, 43: 153-158. 2014. b. [DOI] [PubMed] [Google Scholar]
  54. Monir MM, Hiramatsu K, Nishimura K, Takemoto C, Watanabe T. Distribution of glucagon-like peptide (GLP) -2-immunoreactive cells in the chicken small intestine: antigen retrieval immunohistochemistry. Journal of Veterinary Medical Science, 76: 565-568. 2014. c. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Moran TH, Ameglio PJ, Peyton HJ, Schwartz GJ, McHugh PR. Blockade of type A, but not type B, CCK receptors postpones satiety in rhesus monkeys. American Journal of Physiology, 265: R620-R624. 1993. [DOI] [PubMed] [Google Scholar]
  56. Moran TH, Baldessarini AR, Salorio CF, Lowery T, Schwartz GJ. Vagal afferent and efferent contributions to the inhibition of food intake by cholecystokinin. American Journal of Physiology, 272: R1245-R1251. 1997. [DOI] [PubMed] [Google Scholar]
  57. Naito M. Embryo manipulation in chickens. Journal of Poultry Science, 52: 7-14. 2015. [Google Scholar]
  58. Nie Q, Fang M, Xie L, Peng X, Xu H, Luo C, Zhang D, Zhang X. Molecular characterization of the ghrelin and ghrelin receptor genes and effects on fat deposition in chicken and duck. Journal of Biomedicine & Biotechnology, 567120 2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Nilsson IB, Svensson SP, Monstein HJ. Molecular cloning of an unusual bicistronic cholecystokinin receptor mRNA expressed in chicken brain: a structural and functional expression study. Regulatory Peptides, 114: 37-43. 2003. [DOI] [PubMed] [Google Scholar]
  60. Nishimura K, Hiramatsu K, Monir MM, Takemoto C, Watanabe T. Ultrastructural study on colocalization of glucagon-like peptide (GLP) -1 with GLP-2 in chicken intestinal L-cells. Journal of Veterinary Medical Science 75, 1335-1339. 2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Nishimura K, Hiramatsu K, Watanabe T, Makino R, Sasaki N, Kita K. Amino acid supplementation to diet influences the activity of the L cells in chicken small intestine. Journal of Poultry Science, 52: 221-226. 2015. [Google Scholar]
  62. Ohkubo T, Shamoto K, Ogino T. Structure and tissue distribution of cholecystokinin-1 receptor in chicken. Journal of Poultry Science, 44: 98-104. 2007. [Google Scholar]
  63. Ocłoń E, Pietras M. Peripheral ghrelin inhibits feed intake through hypothalamo-pituitary-adrenal axis-dependent mechanism in chicken. Journal of Animal Feed Science, 20: 118-130. 2011. [Google Scholar]
  64. Park TS, Kang KS, Han JY. Current genomic editing approaches in avian transgenesis. General and Comparative Endocrinology, 190: 144-148. 2013. [DOI] [PubMed] [Google Scholar]
  65. Penney CC, Volkoff H. Peripheral injections of cholecystokinin, apelin, ghrelin and orexin in cavefish (Astyanax fasciatus mexicanus): effects on feeding and on the brain expression levels of tyrosine hydroxylase, mechanistic target of rapamycin and appetite-related hormones. General and Comparative Endocrinology, 196: 34-40. 2014. [DOI] [PubMed] [Google Scholar]
  66. Reidelberger RD, Castellanos DA, Hulce M. Effects of peripheral CCK receptor blockade on food intake in rats. American Journal of Physiology, Regulatory, Integrative and Comparative Physiology, 285: R429-R437. 2003. [DOI] [PubMed] [Google Scholar]
  67. Richards MP, McMurtry JP. Expression of proglucagon and proglucagon-derived peptide hormone receptor genes in the chicken. General and Comparative Endocrinology, 156: 323-338. 2008. [DOI] [PubMed] [Google Scholar]
  68. Riley LG, Fox BK, Kaiya H, Hirano T, Grau EG. Long-term treatment of ghrelin stimulates feeding, fat deposition, and alters the GH/IGF-I axis in the tilapia, Oreochromis mossambicus. General and Comparative Endocrinology, 142: 234-240. 2005. [DOI] [PubMed] [Google Scholar]
  69. Ritter RC, Ladenheim EE. Capsaicin pretreatment attenuates suppression of food intake by cholecystokinin. American Journal of Physiology, 248: R501-R504. 1985. [DOI] [PubMed] [Google Scholar]
  70. Rodríguez-Sinovas A, Fernández E, Manteca X, Fernández AG, Goñalons E. CCK is involved in both peripheral and central mechanisms controlling food intake in chickens. American Journal of Physiology, 272: R334-R340. 1997. [DOI] [PubMed] [Google Scholar]
  71. Salaneck E, Holmberg SK, Berglund MM, Boswell T, Larhammar D. Chicken neuropeptide Y receptor Y2: structural and pharmacological differences to mammalian Y2. FEBS Letters, 484: 229-234. 2000. [DOI] [PubMed] [Google Scholar]
  72. Sam AH, Troke RC, Tan TM, Bewick GA. The role of the gut/brain axis in modulating food intake. Neuropharmacology, 63: 46-56. 2012. [DOI] [PubMed] [Google Scholar]
  73. Savory CJ, Gentle MJ. Effects of food deprivation, strain, diet and age on feeding responses of fowls to intravenous injections of cholecystokinin. Appetite, 4: 165-176. 1983. [DOI] [PubMed] [Google Scholar]
  74. Schmidt PT, Naslund E, Gryback P, Jacobsson H, Hartmann B, Holst JJ, Hellstrom PM. Peripheral administration of GLP-2 to humans has no effect on gastric emptying or satiety. Regulatory Peptides, 116: 21-25. 2003. [DOI] [PubMed] [Google Scholar]
  75. Scott V, Kimura N, Stark JA, Luckman SM. Intravenous peptide YY3-36 and Y2 receptor antagonism in the rat: effects on feeding behavior. Journal of Neuroendocrinology, 17: 452-457. 2005. [DOI] [PubMed] [Google Scholar]
  76. Seroussi E, Cinnamon Y, Yosefi S, Genin O, Smith JG, Rafati N, Bornelov S, Andersson L, Friedman-Einat M. Identification of the long-sought leptin in chicken and duck: Expression pattern of the highly GC-rich avian leptin fits an autocrine/paracrine rather than endocrine function. Endocrinology, 157: 737-751. 2016. [DOI] [PubMed] [Google Scholar]
  77. Shao Y, Liu S, Tang X, Gao J, Wu G, Li Z. Ontogeny of ghrelin mRNA expression and identification of ghrelin-immunopositive cells in the gastrointestinal tract of the Peking duck, Anas platyrhynchos. General and Comparative Endocrinology, 166: 12-18. 2010. [DOI] [PubMed] [Google Scholar]
  78. Shousha S, Nakahara K, Kojima M, Miyazato M, Hosoda H, Kangawa K, Murakami N. Different effects of peripheral and central ghrelin on regulation of food intake in the Japanese quail, General and Comparative Endocrinology, 141: 178-183. 2005. a. [DOI] [PubMed] [Google Scholar]
  79. Shousha S, Nakahara K, Nasu T, Sakamoto T, Murakami N. Effect of glucagon-like peptide-1 and -2 on regulation of food intake, body temperature and locomotor activity in the Japanese quail. Neuroscience Letters, 415: 102-107. 2007. [DOI] [PubMed] [Google Scholar]
  80. Shousha S, Nakahara K, Miyazato M, Kangawa K, Murakami N. Endogenous neuromedin U has anorectic effects in the Japanese quail. General and Comparative Endocrinology, 140: 156-163. 2005. b. [DOI] [PubMed] [Google Scholar]
  81. Shiraishi J, Yanagita K, Fujita M, Bungo T. Central insulin suppresses feeding behavior via melanocortins in chicks. Domestic Animal Endocrinology, 34: 223-228. 2008. [DOI] [PubMed] [Google Scholar]
  82. Silverstein JT, Bondareva VM, Leonard JB, Plisetskaya EM. 2001. Neuropeptide regulation of feeding in catfish, Ictalurus punctatus: a role for glucagon-like peptide-1 (GLP-1)? Comparative Biochemistry and Physiology, Part B, Biochemistry and Molecular Biology, 129: 623-631. 2001. [DOI] [PubMed] [Google Scholar]
  83. Smith G, Jerome C, Norgren R. Afferent axons in the abdominal vagus mediate the satiety effects of cholecystokinin in rats. American Journal of Physiology, 249: R638-R641. 1985. [DOI] [PubMed] [Google Scholar]
  84. Sorensen LB, Flint A, Raben A, Hartmann B, Holst JJ, Astrup A. No effect of physiological concentrations of glucagon-like peptide-2 on appetite and energy intake in normal weight subjects. International Journal of Obesity, 27: 450-456. 2003. [DOI] [PubMed] [Google Scholar]
  85. Stadlbauer U, Arnold M, Weber E, Langhans W. Possible mechanisms of circulating PYY-induced satiation in male rats. Endocrinology, 154: 193-204. 2013. [DOI] [PubMed] [Google Scholar]
  86. Tachibana T, Matsuda K, Kawamura M, Ueda H, Khan MS, Cline MA. Feeding-suppressive mechanism of sulfated cholecystokinin (26-33) in chicks. Comparative Biochemistry and Physiology, Part A, Molecular and Integrative Physiology, 161: 372-378. 2012. [DOI] [PubMed] [Google Scholar]
  87. Tachibana T, Kubo S, Khan MS, Masuda K, Ukena K, Wang Y. Peripheral injection of chicken growth hormone-releasing hormone inhibits feeding behavior in chicks. Journal of Poultry Science, 53: 29-33. 2015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Tachibana T, Matsumoto M, Furuse M, Hasegawa S, Yoshizawa F, Sugahara K. Central, but not peripheral, glucagon-like peptide-1 inhibits crop emptying in chicks. Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology, 134: 777-781. 2003. [DOI] [PubMed] [Google Scholar]
  89. Tanaka M, Miyazaki T, Yamamoto I, Nakai N, Ohta Y, Tsushima N, Wakita M, Shimada K. Molecular characterization of chicken growth hormone secretagogue receptor gene. General and Comparative Endocrinology, 134: 198-202. 2003. [DOI] [PubMed] [Google Scholar]
  90. Tolhurst G, Reimann F, Gribble FM. Nutritional regulation of glucagon-like peptide-1 secretion. Journal of Physiology, 587: 27-32. 2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Ueno H, Yamaguchi H, Mizuta M, Nakazato M. The role of PYY in feeding regulation. Regulatory Peptides, 145: 12-16. 2008. [DOI] [PubMed] [Google Scholar]
  92. Van Bloemendaal L, Ten Kulve JS, la Fleur SE, Ijzerman RG, Diamant M. Effects of glucagon-like peptide 1 on appetite and body weight: focus on the CNS. Journal of Endocrinology 221: T1-T16. 2014. [DOI] [PubMed] [Google Scholar]
  93. Verdich C, Flint A, Gutzwiller JP, Naslund E, Beglinger C, Hellstrom PM, Long SJ, Morgan LM, Holst JJ, Astrup A. A meta-analysis of the effect of glucagon-like peptide-1 (7–36) amide on ad libitum energy intake in humans. Journal of Clinical Endocrinology and Metabolism, 86: 4382-4389. 2001. [DOI] [PubMed] [Google Scholar]
  94. Volkoff H, Eykelbosh AJ, Peter RE. Role of leptin in the control of feeding f goldfish Carassius auratus: interactions with cholecystokinin, neuropeptide Y and orexin A, and modulation by fasting. Brain Research, 972: 90-109. 2003. [DOI] [PubMed] [Google Scholar]
  95. Wang JX, Peng KM, Liu HZh, Song H, Chen X, Liu M. Distribution and developmental changes in ghrelin-immunopositive cells in the gastrointestinal tract of African ostrich chicks. Regulatory Peptides, 154: 97-101. 2009. [DOI] [PubMed] [Google Scholar]
  96. Wang JX, Li P, Peng KM, Jin SH. 2011. cDNA cloning of ghrelin and ontogeny of ghrelin mRNA expression in the gastrointestinal tract of African ostrich chicks. Regulatory Peptides, 167: 50-55. 2011. [DOI] [PubMed] [Google Scholar]
  97. White SL, Volkoff H, Devlin RH. 2016. Regulation of feeding behavior and food intake by appetite-regulating peptides in wild-type and growth hormone-transgenic coho salmon. Hormone and Behavior, 84: 18-28. 2016. [DOI] [PubMed] [Google Scholar]
  98. Williams KW, Elmquist JK. From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior. Nature Neuroscience, 15: 1350-1355. 2012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Woods SC. The control of food intake: behavioral versus molecular perspectives. Cell Metabolism, 9: 489-498. 2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Woods SC. Metabolic signals and food intake. Forty years of progress. Appetite, 71: 440-444. 2013. [DOI] [PubMed] [Google Scholar]
  101. Wren AM, Small CJ, Ward HL, Murphy KG, Dakin CL, Taheri S, Kennedy AR, Roberts GH, Morgan DG, Ghatei MA, Bloom SR. The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology, 141: 4325-4328. 2000. [DOI] [PubMed] [Google Scholar]
  102. Zhou J, Hegsted M, McCutcheon KL, Keenan MJ, Xi X, Raggio AM, Martin RJ. Peptide YY and proglucagon mRNA expression patterns and regulation in the gut. Obesity, 14: 683-689. 2006. [DOI] [PubMed] [Google Scholar]
  103. Zwirska-Korczala K, Konturek SJ, Sodowski M, Wylezol M, Kuka D, Sowa P, Adamczyk-Sowa M, Kukla M, Berdowska A, Rehfeld JF, Bielanski W, Brzozowski T. Basal and postprandial plasma levels of PYY, ghrelin, cholecystokinin, gastrin and insulin in women with moderate and morbid obesity and metabolic syndrome. Journal of Physiology and Pharmacology, 58: 13-35. 2007. [PubMed] [Google Scholar]

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