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

Volumn 157, Issue 2, 2016, Pages 737-751

  Seroussi, Eyal ^a   Cinnamon, Yuval ^a   Yosefi, Sara ^a   Genin, Olga ^a   Smith, Julia Gage ^a   Rafati, Nima ^b   Bornelöv, Susanne ^b   Andersson, Leif ^b,c,d   Friedman Einat, Miriam ^a  

^a VOLCANI CENTER   (Israel)

^b UPPSALA UNIVERSITY   (Sweden)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^d TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA; TRANSCRIPTOME;

ABDOMINAL FAT; ADENOHYPOPHYSIS; ADIPOSE TISSUE; ADULT; ANAS PLATYRHYNCHOS; ANIMAL EXPERIMENT; ARTICLE; BRANCHIAL ARCH; CEREBELLUM; CONTROLLED STUDY; COTURNIX JAPONICA; EMBRYO DEVELOPMENT; ENDOCRINE FUNCTION; ENERGY BALANCE; GALLUS GALLUS; GENE IDENTIFICATION; IN SITU HYBRIDIZATION; LIMB BUD; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RNA SEQUENCE; SOMITE; ANIMAL; AUTOCRINE EFFECT; CARDIAC MUSCLE; CHICKEN; COTURNIX; DUCK; ENDOCRINE SYSTEM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; KIDNEY; MALE; METABOLISM; OVARY; PARACRINE SIGNALING; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TESTIS;

ADIPOSE TISSUE; ANIMALS; AUTOCRINE COMMUNICATION; BRANCHIAL REGION; CEREBELLUM; CHICKENS; COTURNIX; DUCKS; ENDOCRINE SYSTEM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; IN SITU HYBRIDIZATION; KIDNEY; LEPTIN; LIMB BUDS; MALE; MYOCARDIUM; OVARY; PARACRINE COMMUNICATION; PITUITARY GLAND, ANTERIOR; PURKINJE CELLS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, LEPTIN; RNA, MESSENGER; SOMITES; TESTIS; TRANSCRIPTOME;

EID: 84956884252     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1634     Document Type: Article

References (76)

1. Friedman J. 20 years of leptin: leptin at 20: an overview. J Endocrinol. 2014;223:T1-T8.
2. Considine RV, Sinha MK, Heiman ML, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334:292-295.
3. Friedman-Einat M, Camoin L, Faltin Z, et al. Serum leptin activity in obese and lean patients. Regul Pept. 2003;111:77-82.
4. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372:425-432.
5. Chen H, Charlat O, Tartaglia LA, et al. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell. 1996;84:491-495.
6. Lee GH, Proenca R, Montez JM, et al. Abnormal splicing of the leptin receptor in diabetic mice. Nature. 1996;379:632-635.
7. Montague CT, Farooqi IS, Whitehead JP, et al. Congenital leptin deficiency is associated with severe early-onset obesity in humans. Nature. 1997;387:903-908.
8. Strobel A, Issad T, Camoin L, Ozata M, Strosberg AD. A leptin missense mutation associated with hypogonadism and morbid obesity. Nat Genet. 1998;18:213-215.
9. Strosberg AD, Issad T. The involvement of leptin in humans revealed by mutations in leptin and leptin receptor genes. Trends Pharmacol Sci. 1999;20:227-230.
10. Farooqi IS, Wangensteen T, Collins S, et al. Clinical and molecular genetic spectrum of congenital deficiency of the leptin receptor. N Engl J Med. 2007;356:237-247.
11. Gibson WT, Farooqi IS, Moreau M, et al. Congenital leptin deficiency due to homozygosity for the Δ133G mutation: report of another case and evaluation of response to four years of leptin therapy. J Clin Endocrinol Metab. 2004;89:4821-4826.
12. Prieur X, Tung YC, Griffin JL, Farooqi IS, O'Rahilly S, Coll AP. Leptin regulates peripheral lipid metabolism primarily through central effects on food intake. Endocrinology. 2008;149:5432-5439.
13. Tartaglia LA. The leptin receptor. J Biol Chem. 1997;272:6093-6096.
14. Friedman JM. Leptin, leptin receptors, and the control of body weight. Nutr Rev. 1998;56:s38-s46; discussion s54-s75.
15. Li Z, Ceccarini G, Eisenstein M, Tan K, Friedman JM. Phenotypic effects of an induced mutation of the ObRa isoform of the leptin receptor. Mol Metab. 2013;2:364-375.
16. Hileman SM, Pierroz DD, Masuzaki H, et al. Characterizaton of short isoforms of the leptin receptor in rat cerebral microvessels and of brain uptake of leptin in mouse models of obesity. Endocrinology. 2002;143:775-783.
17. Barr VA, Lane K, Taylor SI. Subcellular localization and internalization of the four human leptin receptor isoforms. J Biol Chem. 1999;274:21416-21424.
18. Tu H, Kastin AJ, Hsuchou H, Pan W. Soluble receptor inhibits leptin transport. J Cell Physiol. 2008;214:301-305.
19. Schaab M, Kausch H, Klammt J, et al. Novel regulatory mechanisms for generation of the soluble leptin receptor: implications for leptin action. PLoS One. 2012;7:e34787.
20. Lou PH, Yang G, Huang L, Cui Y, et al. Reduced body weight and increased energy expenditure in transgenic mice over-expressing soluble leptin receptor. PLoS One. 2010;5:e11669.
21. Taouis M, Chen JW, Daviaud C, Dupont J, Derouet M, Simon J. Cloning the chicken leptin gene. Gene. 1998;208:239-242.
22. Ashwell CM, Czerwinski SM, Brocht DM, McMurtry JP. Hormonal regulation of leptin expression in broiler chickens. Am J Physiol. 1999;276:R226-R232.
23. Daković; N, T1272;ré;zol M, Pitel F, et al. The loss of adipokine genes in the chicken genome and implications for insulin metabolism. Mol Biol Evol. 2014;31:2637-2646.
24. Horev G, Einat P, Aharoni T, Eshdat Y, Friedman-Einat M. Molecular cloning and properties of the chicken leptin-receptor (CLEPR) gene. Mol Cell Endocrinol. 2000;162:95-106.
25. Ohkubo T, Tanaka M, Nakashima K. Structure and tissue distribution of chicken leptin receptor (cOb-R) mRNA. Biochim Biophys Acta. 2000;1491:303-308.
26. Adachi H, Takemoto Y, Bungo T, Ohkubo T. Chicken leptin receptor is functional in activating JAK-STATpathway in vitro. J Endocrinol. 2008;197:335-342.
27. Hen G, Yosefi S, Ronin A, et al. Monitoring leptin activity using the chicken leptin receptor. J Endocrinol. 2008;197:325-333.
28. Niv-Spector L, Raver N, Friedman-Einat M, et al. Mapping leptininteracting sites in recombinant leptin-binding domain (LBD) subcloned from chicken leptin receptor. Biochem J. 2005;390:475-484.
29. Friedman-Einat M, Seroussi E. Quack leptin. BMC Genomics. 2014;15:551.
30. Prokop JW, Schmidt C, Gasper D, et al. Discovery of the elusive leptin in birds: identification of several 'missing links' in the evolution of leptin and its receptor. PLoS One. 2014;9:e92751.
31. Burt DW. Chicken genome: current status and future opportunities. Genome Res. 2005;15:1692-1698.
32. Schmid M, Nanda I, Hoehn H, et al. Second report on chicken genes and chromosomes 2005. Cytogenet Genome Res. 2005;109:415-479.
33. Smith J, Bruley CK, Paton IR, et al. Differences in gene density on chicken macrochromosomes and microchromosomes. Anim Genet. 2000;31:96-103.
34. Zhang G, Li C, Li Q, et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science. 2014;346: 1311-1320.
35. Lovell PV, Wirthlin M, Wilhelm L, et al. Conserved syntenic clusters of protein coding genes are missing in birds. Genome Biol. 2014; 15:565.
36. Chevreux B, Pfisterer T, Drescher B, et al. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 2004;14:1147-1159.
37. Bonfield JK, Whitwham A. Gap5-editing the billion fragment sequence assembly. Bioinformatics. 2010;26:1699-1703.
38. Cinnamon Y, Ben-Yair R, Kalcheim C. Differential effects of Ncadherin-mediated adhesion on the development of myotomal waves. Development. 2006;133:1101-1112.
39. Rosenblum CI, Vongs A, Tota MR, et al. A rapid, quantitative functional assay for measuring leptin. Mol Cell Endocrinol. 1998; 143:117-123.
40. Friedman-Einat M, Cogburn LA, Yosefi S, et al. Discovery and characterization of the first genuine avian leptin gene in the rock dove (Columba livia). Endocrinology. 2014;155:3376-3384.
41. Sahdev S, Saini S, Tiwari P, Saxena S, Singh Saini K. Amplification of GC-rich genes by following a combination strategy of primer design, enhancers and modified PCR cycle conditions. Mol Cell Probes. 2007;21:303-307.
42. Cinnamon Y, Kahane N, Bachelet I, Kalcheim C. The sub-lip domain-a distinct pathway for myotome precursors that demonstrate rostral-caudal migration. Development. 2001;128:341-351.
43. Gushchanskaya ES, Artemov AV, Ulyanov SV, et al. The clustering of CpG islands may constitute an important determinant of the 3D organization of interphase chromosomes. Epigenetics. 2014;9:951-963.
44. Zhang F, Basinski MB, Beals JM, et al. Crystal structure of the obese protein leptin-E100. Nature. 1997;387:206-209.
45. Denver RJ, Bonett RM, Boorse GC. Evolution of leptin structure and function. Neuroendocrinology. 2011;94:21-38.
46. Prokop JW, Duff RJ, Ball HC, Copeland DL, Londraville RL. Leptin and leptin receptor: analysis of a structure to function relationship in interaction and evolution from humans to fish. Peptides. 2012; 38:326-336.
47. Elinav E, Niv-Spector L, Katz M, et al. Pegylated leptin antagonist is a potent orexigenic agent: preparation and mechanism of activity. Endocrinology. 2009;150:3083-3091.
48. Solomon G, Atkins A, Shahar R, Gertler A, Monsonego-Ornan E. Effect of peripherally administered leptin antagonist on whole body metabolism and bone microarchitecture and biomechanical properties in the mouse. Am J Physiol Endocrinol Metab. 2014;306: E14-E27.
49. Gertler A, Shinder D, Yosefi S, et al. Pegylated leptin antagonist with strong orexigenic activity in mice is not effective in chickens. J Exp Biol. 2014;217:180-184.
50. Liu X, Dunn IC, Sharp PJ, Boswell T. Molecular cloning and tissue distribution of a short form chicken leptin receptor mRNA. Domest Anim Endocrinol. 2007;32:155-166.
51. Resnyk CW, Carre W, Wang X, et al. Transcriptional analysis of abdominal fat in genetically fat and lean chickens reveals adipokines, lipogenic genes and a link between hemostasis and leanness. BMC Genomics. 2013;14:557.
52. Simon J, Brisson GJ. Effect of two types of feed restriction, intermittent total starvation or intermittent protein starvation, on growth, lipogenesis, and fatty acid composition of liver and adipose tissues in chicks. Can J Physiol Pharmacol. 1972;50:634-644.
53. 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. 2014;155:3385-3396.
54. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol. 1951;88:49-92.
55. Gorissen M, Flik G. Leptin in teleostean fish, towards the origins of leptin physiology. J Chem Neuroanat. 2014;61-62:200-206.
56. Oldreive CE, Harvey J, Doherty GH. Neurotrophic effects of leptin on cerebellar Purkinje but not granule neurons in vitro. Neurosci Lett. 2008;438:17-21.
57. Forero-Vivas ME, Hernández-Cruz A. Increased firing frequency of spontaneous action potentials in cerebellar Purkinje neurons of db/db mice results from altered auto-rhythmicity and diminished GABAergic tonic inhibition. Gen Physiol Biophys. 2014;33:29-41.
58. Huang Y, Li Y, Burt DW, et al. The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat Genet. 2013;45:776-783.
59. Crespi EJ, Denver RJ. Leptin (ob gene) of the South African clawed frog Xenopus laevis. Proc Natl Acad Sci USA. 2006;103:10092-10097.
60. Rønnestad I, Nilsen TO, Murashita K, et al. Leptin and leptin receptor genes in Atlantic salmon: cloning, phylogeny, tissue distribution and expression correlated to long-term feeding status. Gen Comp Endocrinol. 2010;168:55-70.
61. Yu WH, Kimura M, Walczewska A, Karanth S, McCann SM. Role of leptin in hypothalamic-pituitary function. Proc Natl Acad Sci USA. 1997;94:1023-1028.
62. Clément K, Vaisse C, Lahlou N, et al. Amutation in thehumanleptin receptor gene causes obesity and pituitary dysfunction. Nature. 1998;392:398-401.
63. Boswell T, Dunn IC, Wilson PW, Joseph N, Burt DW, Sharp PJ. Identification of a non-mammalian leptin-like gene: characterization and expression in the tiger salamander (Ambystoma tigrinum). Gen Comp Endocrinol. 2006;146:157-166.
64. Malendowicz LK, Rucinski M, Belloni AS, Ziolkowska A, Nussdorfer GG. Leptin and the regulation of the hypothalamic-pituitaryadrenal axis. Int Rev Cytol. 2007;263:63-102.
65. Letizia C, Petramala L, Di Gioia CR, et al. Leptin and adiponectin mRNA expression from the adipose tissue surrounding the adrenal neoplasia. J Clin Endocrinol Metab. 2015;100:E101-E104.
66. Mendoza J, Pévet P, Felder-Schmittbuhl MP, Bailly Y, Challet E. The cerebellum harbors a circadian oscillator involved in food anticipation. J Neurosci. 2010;30:1894-1904.
67. Liu Q, Dalman M, Chen Y, et al. Knockdown of leptin A expression dramatically alters zebrafish development. Gen Comp Endocrinol. 2012;178:562-572.
68. Farooqi IS, Jebb SA, Langmack G, et al. Effects of recombinant leptin therapy in a child with congenital leptin deficiency. N Engl J Med. 1999;341:879-884.
69. Tickle C, Summerbell D, Wolpert L. Positional signalling and specification of digits in chick limb morphogenesis. Nature. 1975;254: 199-202.
70. Copeland DL, Duff RJ, Liu Q, Prokop J, Londraville RL. Leptin in teleost fishes: an argument for comparative study. Front Physiol. 2011;2:26.
71. Halasz B, Pupp L, Uhlarik S. Hypophysiotrophic area in the hypothalamus. J Endocrinol. 1962;25:147-154.
72. Joseph-Bravo P, Jaimes-Hoy L, Uribe RM, Charli JL. 60 years of neuroendocrinology: TRH, the first hypophysiotropic releasing hormone isolated: control of the pituitary-thyroid axis. J Endocrinol. 2015;226:T85-T100.
73. Banks WA, Clever CM, Farrell CL. Partial saturation and regional variation in the blood-to-brain transport of leptin in normal weight mice. Am J Physiol Endocrinol Metab. 2000;278:E1158-E1165.
74. Hoegg S, Brinkmann H, Taylor JS, Meyer A. Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol. 2004;59:190-203.
75. Haglund E, Sulkowska JI, He Z, Feng GS, Jennings PA, Onuchic JN. The unique cysteine knot regulates the pleotropic hormone leptin. PLoS One. 2012;7:e45654.
76. Shpilman M, Niv-Spector L, Katz M, et al. Development and characterization of high affinity leptins and leptin antagonists. J Biol Chem. 2011;286:4429-4442.