Pale and dark reddish melanic tawny owls differentially regulate the level of blood circulating POMC prohormone in relation to environmental conditions

Oecologia

Volumn 166, Issue 4, 2011, Pages 913-921

  Roulin, Alexandre ^a   Emaresi, Guillaume ^a   Bize, Pierre ^a   Gasparini, Julien ^a,b   Piault, Romain ^a,c   Ducrest, Anne Lyse ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Melanin based colouration; Melanocortin; Norms of reaction; Phenotypic plasticity; Pheomelanin; Proopiomelanocortin gene; Strix aluco

Indexed keywords

PIGMENT; PROOPIOMELANOCORTIN;

BLOOD; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL STRESS; FITNESS; GENE EXPRESSION; GENOTYPE; HERITABILITY; HOMEOSTASIS; HORMONE; MELANIN; PEPTIDE; PHENOTYPIC PLASTICITY; PHYSIOLOGICAL RESPONSE; PLEIOTROPY; RAPTOR; REACTION NORM;

ANIMAL; ARTICLE; BLOOD; CLUTCH SIZE; ENVIRONMENT; FEMALE; METABOLISM; OWL; PIGMENTATION; PLEIOTROPY;

ANIMALS; CLUTCH SIZE; ENVIRONMENT; FEMALE; GENETIC PLEIOTROPY; PIGMENTATION; PIGMENTS, BIOLOGICAL; PRO-OPIOMELANOCORTIN; STRIGIFORMES;

STRIGIFORMES; STRIX ALUCO;

EID: 79960316104     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-011-1955-7     Document Type: Article

References (61)

1. Abt KF, Bock WF (1998) Seasonal variations in diet composition in farmland field mice Apodemus spp. and bank voles Clethrionomys glareolus. Acta Theoriol 43: 379-389.
2. Barna I, Koenig JI, Péczely P (1998) Characteristics of the proopiomelanocortin system in the outdoor-bred domestic gander. Gen Comp Endocrinol 109: 44-51.
3. Bell ME, McDonald TJ, Myers DA (2005) Proopiomelanocortin processing in the anterior pituitary of the ovine foetus after lesion of the hypothalamic paraventricular nucleus. Endocrinology 146: 2665-2673.
4. Bennett DC, Lamoreux ML (2003) The color loci of mice-a genetic century. Pigment Cell Res 16: 333-344.
5. Bertile F, Oudart H, Criscuolo F, Le Maho Y, Raclot T (2003) Hypothalamic gene expression in long-term fasted rats: relationship with body fat. Biochem Biophys Res Comm 303: 1106-1113.
6. Boswell T, Takeuchi S (2005) Recent developments in our understanding of the avian melanocortin system: its involvement in the regulation of pigmentation and energy homeostasis. Peptides 26: 1733-1743.
7. Chen JX, Tang Y-T, Yang J-X (2008) Changes of glucocorticoid receptor and levels of CRF mRNA, POMC mRNA in brain of chronic immobilization stress rats. Cell Mol Neurobiol 28: 237-244.
8. Chiao H, Foster S, Lipton TR, Star RA (1996) Alpha-melanocyte-stimulating hormone reduces endotoxin-induced liver inflammation. J Clin Invest 97: 2038-2044.
9. Coll AP, Farooqi IS, Challis BG, Yeo GS, O'Rahilly S (2004) Proopiomelanocortin and energy balance: insights from human and murine genetics. J Clin Endocrinol Metab 89: 2557-2562.
10. Cone RD (2006) Studies on the physiological functions of the melanocortin system. Endocr Rev 27: 736-749.
11. Dallman MF, Akana SF, Bhatnagar S, Bell ME, Choi S, Chu A, Horsley C, Levin N, Meijer O, Soriano LR, Strack AM, Viau V (1999) Starvation: early signals, sensors, and sequelae. Endocrinology 140: 4015-4023.
12. Daynes RA, Robertson BA, Burnham DK, Newton R (1987) Alpha-melanocyte-stimulating hormone exhibits target cell selectivity interleukin 1-inducible responses in vivo and in vitro. J Immunol 139: 103-109.
13. Ducrest A-L, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, colouration and behavioural syndromes. Trends Ecol Evol 23: 502-510.
14. Ellis C, Moar KM, Logie TJ, Ross AW, Morgan PJ, Mercer JG (2008) Diurnal profiles of hypothalamic energy balance gene expression with photoperiod manipulation in the Siberian hamster, Phodopus sungorus. Am J Physiol Regul Integr Comp Physiol 294: 1148-1153.
15. Galeotti P (2001) Tawny owl. BWP Update 3: 43-77.
16. Gasparini J, Bize P, Piault R, Wakamatsu K, Blount JD, Ducrest A-L, Roulin A (2009a) Strength and cost of mounting an immune response are associated with a heritable melanin-based color trait in female tawny owls. J Anim Ecol 78: 608-616.
17. Gasparini J, Piault R, Bize P, Roulin A (2009b) Synergetic and antagonistic interaction between different branches of the immune system is related to melanin-based colouration in nestling tawny owls. J Evol Biol 22: 2348-2353.
18. Getting SJ (2006) Targeting melanocortin receptors as potential novel therapeutics. Pharmacol Therapeut 111: 1-15.
19. Gonindard C, Goigoux C, Hollande E, D'Hinterland LD (1996) The administration of an alpha-MSH analogue reduces the serum release of IL-1 alpha and TNF alpha induced by the injection of a sublethal dose of lipopolysaccharides in the BALB/c mouse. Pigment Cell Res 9: 148-153.
20. Grabbe S, Bhardwaj RS, Mahnke K, Simon MM, Schwarz T, Luger TA (1996) Alpha-Melanocyte-stimulating hormone induces hapten-specific tolerance in mice. J Immunol 156: 473-478.
21. Granger N (2004) Plasma concentrations of adrenocorticotrophic hormone precursors in dogs with Cushing's disease: evaluation in the detetction of large pituitary adenoma. La Faculté de Médecine de Créteil, Ecole Nationale Vétérinaire d'Alfort 65.
22. Hedrick PW (2006) Genetic polymorphism in heterogeneous environments: the age of genomics. Annu Rev Ecol Evol Syst 37: 67-93.
23. Hoglund E, Balm PHM, Winberg S (2000) Skin darkening, a potential social signal in subordinate arctic charr (Salvelinus alpinus): the regulatory role of brain monoamines and pro-opiomelanocortin-derived peptides. J Exp Biol 203: 1711-1721.
24. Huang QH, Hruby VJ, Tatro JB (1998) Systemic alpha-MSH suppresses LPS fever via central melanocortin receptors independently of its suppression of corticosterone and IL-6 release. Am J Physiol Regul Integr Comp Physiol 275: 524-530.
25. Ito S, Wakamatsu (2008) Chemistry of mixed melanogenesis-pivotal roles of dopaquinone. Photochem Photobiol 84: 582-592.
26. Ito S, Wakamatsu K (2011) Human hair melanins: what we have learned and have not learned from mouse coat color pigmentation. Pigment Cell Melanoma Res (in press).
27. Kappeler L, Zizzari P, Grouselle D, Epelbaum J, Bluet-Pajot MT (2004) Plasma and hypothalamic peptide-hormone levels regulating somatotroph function and energy balance in fed and fasted states: a comparative study in four strains of rats. J Neuroendocrinol 16: 980-988.
28. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7: 1225-1241.
29. Krude H, Biebermann H, Luck W, Horn R, Brabant G, Grüters A (1998) Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nature Genet 19: 155-157.
30. Le Pape E, Passeron T, Giubellino A, Valencia JC, Wolber R, Hearing VJ (2009) Microarry analysis sheds light on the dedifferentiating role of agouti signal protein in murine melanocytes via the Mc1r. Proc Natl Acad Sci USA 106: 1802-1807.
31. Lerner AB, McGuire J (1979) Effect of alpha and beta melanocyte stimulating hormones on the skin color of man. Nature 189: 176-179.
32. Lin JY, Fisher DE (2007) Melanocyte biology and skin pigmentation. Nature 445: 843-850.
33. Margaletic J, Bozic M, Grubesic M, Glavas M, Bäumler W (2005) Distribution and abundance of small rodents in Croatian forests. J Pest Sci 78: 99-103.
34. Meyerhoff JL, Oleshansky MA, Mougey EH (1988) Psychologic stress increases plasma levels of prolactin, cortisol, and POMC-derived polypeptides in man. Psychosom Med 50: 295-303.
35. Morgan C, Cone RD (2006) Melanocortin-5 receptor deficiency in mice blocks a novel pathway influencing pheromone-induced aggression. Behav Genet 36: 291-300.
36. Myers DA, Bell PA, Hyatt K, Mlynarczyk M, Ducsay CA (2005) Long term hypoxia enhances proopiomelanocortin processing in the near-term ovine fetus. Am J Physiol Regul Integr Comp Physiol 288: R1178-R1184.
37. Noguchi T, Makino S, Maruyama H, Hashimoto K (2006) Regulation of proopiomelanocortin gene transcription during single and repeated immobilization stress. Neuroendocrinology 84: 21-30.
38. Palermo F, Nabissi M, Cardinaletti G, Tibaldi E, Mosconi G, Polzonetti-Magni AM (2008) Cloning of sole proopiomelanocortin (POMC) cDNA and the effects of stocking density on POMC mRNA and growth rate in sole, Solea solea. Gen Comp Endocrinol 155: 227-233.
39. Piault R, Gasparini J, Bize P, Jenni-Eiermann S, Roulin A (2009) Pheomelanin-based coloration and the ability to cope with variation in food supply and parasitism. Am Nat 174: 548-556.
40. Pritchard LE, Turnbull AV, White A (2002) Pro-opiomelanocortin processing in the hypothalamus: impact on melanocortin signalling and obesity. J Endocrinol 172: 411-421.
41. Pulichino AM, Vallette-Kasic S, Couture C, Gauthier Y, Brue T, David M, Malpuech G, Deal C, van Vliet G, De Vroede M, Riepe FG, Partsch CJ, Sippell WG, Bergeroglu M, Atasay B, Drouin J (2003) Human and mouse TPIT gene mutations cause early onset pituitary ACTH deficiency. Genes Dev 17: 711-716.
42. Roulin A (2009) Covariation between eumelanic pigmentation and body mass only under specific conditions. Naturwissenschaften 96: 375-382.
43. Roulin A, Ducret B, Ravussin P-A, Altwegg R (2003) Female colour polymorphism covaries with reproductive strategies in the tawny owl Strix aluco. J Avian Biol 34: 393-401.
44. Roulin A, Gasparini J, Bize P, Ritschard M, Richner H (2008a) Melanin-based colourations signals strategies to cope with poor and rich environments. Behav Ecol Sociobiol 62: 507-519.
45. Roulin A, Ducret B, Bize P, Piault R, Ravussin P-A (2008b) Régime alimentaire de la chouette hulotte Strix aluco en Suisse romande de 1986 à 2007. Nos Oiseaux 55: 149-156.
46. Rousseau K, Kauser S, Pritcahrd LE, Warhurst A, Oliver RL, Slominski A, Wei ET, Thody AJ, Tobin DJ, White A (2007) Proopiomelanocortin (POMC), the ACTH/melanocortin precursor, is secreted by human epidermal keratinocytes and melanocytes and stimulates melanogenesis. FASEB J 21: 1844-1856.
47. Sanchez VC, Goldstein J, Stuart RC, Hovanesian V, Huo L (2004) Regulation of hypothalamic prohormone convertases 1 and 2 and effects on processing of prothyrotropin-releasing hormone. J Clin Invest 114: 357-369.
48. Schallreuter KU, Kothari S, Chavan B, Spencer JD (2008) Regulation of melanogenesis-controversies and new concepts. Exp Dermatol 17: 395-404.
49. Schwartz MW, Porte D (2005) Diabetes, obesity, and the brain. Science 307: 375-379.
50. Shahjahan M, Hamabata T, Motohashi E, Doi H, Ando H (2010) Differential expression of three types of gonadotropin-releasting hormone genes during the spawning season in grass puffer Takifugu niphobles. Gen Comp Endocrinol 167: 153-163.
51. Silvers WK (1979) The coat colors of mice. Springer, New York.
52. Slominski A (2009) Neuroendocrine activity of the melanocyte. Exp Dermatol 18: 760-763.
53. Slominski A, Wortsman J, Luger T, Paus R, Solomon S (2000) Corticotropin releasing hormone and proopiomelanocortin involvement in the cutaneous response to stress. Physiol Rev 80: 979-1020.
54. Slominski A, Tobin DJ, Shibahara S, Wortsman J (2004) Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev 84: 1155-1228.
55. Sturm RA (2006) A golden age of human pigmentation genetics. Trends Genet 22: 464-468.
56. Ugwu SO, Blanchard J, Door RT, Levine N, Brooks C, Hadley ME, Aickin M, Hruby VJ (1997) Skin pigmentation and pharmacokinetics of melanotan-I in humans. Biopharm Drug Dispos 18: 259-269.
57. van der Ploeg LH, Martin WJ, Howard AD, Nargund RP, Austin CP, Guan X, Drisko J, Cashen D, Sebhat I, Patchett AA, Figueroa DJ, Dilella AG, Connolly BM, Weinberg DH, Tan CP, Palyha OC, Pong S-S, MacNeil T, Rosenblum C, Vongs A, Tang R, Yu H, Sailer AW, Fong TM, Huang C, Tota MR, Chang RS, Stearns R, Tamvakopoulos C, Christ G, Drazen DL, Spar BD, Nelson RJ, MacIntyre E (2002) A role for the melanocortin 4 receptor in sexual function. Proc Natl Acad Sci USA 99: 11381-11386.
58. Walker WP, Gunn TM (2010) Shades of meaning: the pigment-type switching system as a tool for discovery. Pigment Cell Melanoma Res 23: 485-495.
59. Wessells H, Hruby VJ, Hackett J, Han G, Balse-Srinivasan P, Vanderah TW (2003) Ac-Nle-c[Asp-His-DPhe-Arg-Trp-Lys]-NH2 induces penile erection via brain and spinal melanocortin receptors. Neuroscience 118: 755-762.
60. Wilkinson CW (2006) Roles of acétylation and other post-translational modifications in melanocortin function and interactions with endorphins. Peptides 27: 453-471.
61. Yaswen L, Diehl N, Brennan MB, Hochgeschwender U (1999) Obesity in the mouse model of pro-opiomelanocortin deficiency responds to peripheral melanocortin. Nature Med 5: 1066-1070.