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The Genetic and Molecular Basis of Melanism in the Grey Squirrel (Sciurus Carolinensis) Helen Rebecca Mcrobie

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The Genetic and Molecular Basis of Melanism in the Grey Squirrel (Sciurus Carolinensis) Helen Rebecca Mcrobie ANGLIA RUSKIN UNIVERSITY THE GENETIC AND MOLECULAR BASIS OF MELANISM IN THE GREY SQUIRREL (SCIURUS CAROLINENSIS) HELEN REBECCA MCROBIE A thesis in partial fulfilment of the requirements of Anglia Ruskin University for the degree of Doctor of Philosophy Submitted: September 2014 Acknowledgments I am very grateful to Anglia Ruskin University for giving me the opportunity to undertake this project. Thank you goes to my first supervisor, Dr Peter Coussons, for support and advice throughout. Furthermore, this work would not have been possible without the cell culture laboratory which was established and managed by Peter. Thank you also goes to my second supervisor, Dr Linda King, for invaluable encouragement and guidance throughout. I am also grateful for the support and advice from my advisers, Dr Cristina Fanutti, Dr Martyn Symmons and Dr John O’Brien. Thank you also to Dr Alison Thomas for initiating the project. I am grateful for the assistance of Mark D’Arcy, Angela Wheatley, Dr Nancy Moncrief, Luca Lapini, Dr Caray Walker, Dr Nick Pugh, Dr PhilWarburton and Dr Phillip Pugh. An enormous thank you goes to my family for their inspiration, support and patience throughout this project. In particular I would like to say thank you to my dear husband Allan McRobie. Al’s constant encouragement and kindness have made all the difference. Thank you. i ANGLIA RUSKIN UNIVERSITY ABSTRACT FACULTY OF SCIENCE AND TECHNOLOGY DOCTOR OF PHILOSOPHY THE GENETIC AND MOLECULAR BASIS OF MELANISM IN THE GREY SQUIRREL (SCIURUS CAROLINENSIS) HELEN REBECCA MCROBIE SEPTEMBER 2014 The grey squirrel (Sciurus carolinensis) has wildtype and melanic (dark) colour morphs. Melanism is associated with variations in the melanocortin-1 receptor (MC1R) gene in a number of species. The MC1R protein is a G-protein coupled receptor, predominantly expressed in melanocytes, where it is a key regulator of pigment production. To investigate the genetic and molecular basis of melanism, the MC1R genes of the wildtype and melanic grey squirrel were sequenced. The wildtype (MC1R-wt) and melanic (MC1RΔ24) variants of the MC1R were then functionally characterised in a cell-based assay. The MC1R gene of the grey squirrel was found to have a 24 base pair (bp) deletion associated with melanism. The MC1R is typically activated by its agonist, the alpha-melanocyte stimulating hormone (α-MSH), which stimulates dark pigment production by raising intracellular cAMP levels. Conversely, the MC1R is inactivated by its inverse agonist, the agouti signalling protein (ASIP), which stops dark pigment production by lowering intracellular cAMP levels. To investigate the effects that the 24 bp deletion have on receptor function, MC1R-wt and MC1RΔ24 genes were transfected into HEK293 cells. Cells expressing either MC1R-wt or MC1RΔ24 were stimulated with α-MSH or ASIP and intracellular cAMP levels were measured. Unstimulated MC1RΔ24 cells showed higher basal activity than the MC1R-wt cells. Both MC1R-wt and MC1RΔ24 cells responded to α-MSH with a concentration-dependent increase in intracellular cAMP. However, while the MC1R- wt cells responded to ASIP with a concentration-dependent decrease in intracellular cAMP, MC1RΔ24 cells responded with an increase in cAMP. Melanism in the grey squirrel is associated with a 24 bp deletion in the MC1R. Cells expressing MC1RΔ24 have higher basal levels of cAMP than MC1R-wt cells. ASIP acts as an inverse agonist to the MC1R-wt but as an agonist to the MC1RΔ24. As MC1RΔ24 cells have higher levels of cAMP, and higher levels of cAMP lead to dark pigment production, the 24 bp deletion is the likely molecular cause of melanism in the grey squirrel. Key words: Sciurus carolinensis, grey squirrel, melanism, melanocortin-1 receptor. ii Publications McRobie, H.R., Thomas, A. and Kelly, J., 2009. The genetic basis of melanism in the gray squirrel (Sciurus carolinensis). The Journal of Heredity, 100 (6), pp.709-714. McRobie, H.R., King, L.M., Fanutti, C., Coussons, P.J., Moncrief, N.D. and Thomas, A.P., 2014. Melanocortin-1 receptor (MC1R) gene sequence variation and melanism in the gray (Sciurus carolinensis), fox (Sciurus niger), and red (Sciurus vulgaris) squirrel. The Journal of Heredity, 105 (3), pp.423-428. McRobie, H.R., King, L.M., Fanutti, C., Symmons, M.F. and Coussons, P.J., 2014. Agouti signalling protein is an inverse agonist to the wildtype and agonist to the melanic variant of the melanocortin-1 receptor in the grey squirrel (Sciurus carolinensis). FEBS Letters.588 (14) pp.2335-2343. iii Contents Acknowledgments....................................................................................................................... i ABSTRACT ............................................................................................................................... ii Publications .............................................................................................................................. iii Contents .................................................................................................................................... iv Copyright Declaration .............................................................................................................. xv List of Figures ......................................................................................................................... xvi List of Tables ....................................................................................................................... xxiii Abbreviations ........................................................................................................................ xxiv Amino acids ....................................................................................................................... xxviii Chapter One: General Introduction......................................................................................... 1 1.1 Thesis Overview .......................................................................................................... 2 1.2 The Squirrel Family .................................................................................................... 4 1.2.1 The grey, fox and red squirrel: phenotypes ......................................................... 4 1.2.2 Geographic distribution of squirrels .................................................................... 9 1.3 Melanism .................................................................................................................. 15 1.4 Mammalian Pigmentation ......................................................................................... 18 1.4.1 Melanocytes ....................................................................................................... 18 1.4.2 Melanin synthesis............................................................................................... 20 1.4.3 Eumelanin and phaeomelanin ............................................................................ 23 1.4.4 Pigment type switching ...................................................................................... 24 iv 1.5 The Genetics of Pigmentation ................................................................................... 30 1.5.1 The melanocortin-1 receptor gene ..................................................................... 30 1.5.2 The melanocortin-1 receptor and pigmentation ................................................. 31 1.5.3 Mutations in the melanocortin-1 receptor gene associated with melanism ...... 32 1.5.4 Mutations in the melanocortin-1 receptor gene which lead to constitutively active receptors ................................................................................................................ 35 1.5.5 Deletions in the melanocortin-1 receptor gene associated with melanism ....... 35 1.5.6 Mutations in the melanocortin-1 receptor associated with lighter phenotypes . 37 1.5.7 Mutations in agouti signalling protein associated with melanism .................... 38 1.5.8 Mutations in agouti signalling protein associated with lighter phenotypes ...... 41 1.5.9 Mutation in other genes associated with melanism ........................................... 42 1.6 G-protein Coupled Receptors .................................................................................... 43 1.6.1 General features of G-protein coupled receptors ............................................... 43 1.6.2 Predicting the tertiary structure of G-protein coupled receptors ....................... 47 1.6.3 Active and inactive states of G-protein coupled receptors ................................ 48 1.6.4 Maintaining overall stability in G-protein coupled receptors ........................... 50 1.6.5 Conformational changes in G-protein coupled receptors during activation ...... 53 1.6.6 Constitutive activity of G-protein coupled receptors ......................................... 57 v 1.6.7 G-protein coupled receptor ligands and binding sites........................................ 58 1.7 Specific Features of Melanocortin Receptors ........................................................... 61 1.7.1 The melanocortin receptors ................................................................................ 61 1.7.2 Specific features of the melanocortin-1 receptor ............................................... 65 1.7.3 Life cycle of the melanocortin-1 receptor .......................................................... 66 1.7.4 Constitutive activity of melanocortin-1 receptors .............................................
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