Promoter specific DNA methylation and gene expression of POMC in acutely underweight and recovered patients with anorexia nervosa

Journal of Psychiatric Research

Volumn 44, Issue 13, 2010, Pages 827-833

  Ehrlich, Stefan ^a,b   Weiss, Deike ^a   Burghardt, Roland ^a   Infante Duarte, Carmen ^a   Brockhaus, Simone ^a   Muschler, Marc A ^c   Bleich, Stefan ^c   Lehmkuhl, Ulrike ^a   Frieling, Helge ^c,d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Anorexia nervosa; Cortisol; CpG residues; Leptin; MRNA expression; Promoter specific DNA methylation; Proopiomelanocortin (POMC); MSH

Indexed keywords

LEPTIN; MESSENGER RNA; METHYL CPG BINDING PROTEIN; PROOPIOMELANOCORTIN; TRANSCRIPTION FACTOR E2F;

ADOLESCENT; ADULT; ANOREXIA NERVOSA; ARTICLE; BINDING SITE; BODY MASS; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA METHYLATION; EPIGENETICS; EXON; FEMALE; GENE EXPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MALNUTRITION; MOLECULAR INTERACTION; OUTCOME ASSESSMENT; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; UNDERWEIGHT;

EID: 77956338909     PISSN: 00223956     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2010.01.011     Document Type: Article

References (64)

1. Abdolmaleky H.M., Smith C.L., Zhou J.R., Thiagalingam S. Epigenetic alterations of the dopaminergic system in major psychiatric disorders. Methods in Molecular Biology 2008, 448:187-212.
2. Allende L.M., Corell A., Manzanares J., Madruga D., Marcos A., Madrono A., et al. Immunodeficiency associated with anorexia nervosa is secondary and improves after refeeding. Immunology 1998, 94:543-551.
3. Baltatzi M., Hatzitolios A., Tziomalos K., Iliadis F., Zamboulis C. Neuropeptide Y and alpha-melanocyte-stimulating hormone: interaction in obesity and possible role in the development of hypertension. International Journal of Clinical Practice 2008, 62:1432-1440.
4. Barsh G.S., Schwartz M.W. Genetic approaches to studying energy balance: perception and integration. Nature Reviews Genetics 2002, 3:589-600.
5. Bergendahl M., Wiemann J.N., Clifton D.K., Huhtaniemi I., Steiner R.A. Short-term starvation decreases POMC mRNA but does not alter GnRH mRNA in the brain of adult male rats. Neuroendocrinology 1992, 56:913-920.
6. Blalock J.E. Proopiomelanocortin and the immune-neuroendocrine connection. Annals of the New York Academy of Sciences 1999, 885:161-172.
7. Bleich S., Lenz B., Ziegenbein M., Beutler S., Frieling H., Kornhuber J., et al. Epigenetic DNA hypermethylation of the HERP gene promoter induces down-regulation of its mRNA expression in patients with alcohol dependence. Alcoholism: Clinical and Experimental Research 2006, 30:587-591.
8. Brady L.S., Smith M.A., Gold P.W., Herkenham M. Altered expression of hypothalamic neuropeptide mRNAs in food-restricted and food-deprived rats. Neuroendocrinology 1990, 52:441-447.
9. Brzoska T., Luger T.A., Maaser C., Abels C., Bohm M. Alpha-melanocyte-stimulating hormone and related tripeptides: biochemistry, antiinflammatory and protective effects in vitro and in vivo, and future perspectives for the treatment of immune-mediated inflammatory diseases. Endocrine Reviews 2008, 29:581-602.
10. Buzzetti R., McLoughlin L., Lavender P.M., Clark A.J., Rees L.H. Expression of pro-opiomelanocortin gene and quantification of adrenocorticotropic hormone-like immunoreactivity in human normal peripheral mononuclear cells and lymphoid and myeloid malignancies. The Journal of Clinical Investigation 1989, 83:733-737.
11. Clark A.J., Lavender P.M., Coates P., Johnson M.R., Rees L.H. In vitro and in vivo analysis of the processing and fate of the peptide products of the short proopiomelanocortin mRNA. Molecular Endocrinology 1990, 4:1737-1743.
12. Cowley M.A., Smart J.L., Rubinstein M., Cerdan M.G., Diano S., Horvath T.L., et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 2001, 411:480-484.
13. Cutuli M., Cristiani S., Lipton J.M., Catania A. Antimicrobial effects of alpha-MSH peptides. Journal of Leukocyte Biology 2000, 67:233-239.
14. Di Fiore B., Palena A., Felsani A., Palitti F., Caruso M., Lavia P. Cytosine methylation transforms an E2F site in the retinoblastoma gene promoter into a binding site for the general repressor methylcytosine-binding protein 2 (MeCP2). Nucleic Acids Research 1999, 27:2852-2859.
15. Duclos M., Corcuff J.B., Roger P., Tabarin A. The dexamethasone-suppressed corticotrophin-releasing hormone stimulation test in anorexia nervosa. Clinical Endocrinology (Oxf) 1999, 51:725-731.
16. Ehrlich S., Burghardt R., Weiss D., Salbach-Andrae H., Craciun E.M., Goldhahn K., et al. Glial and neuronal damage marker in patients with anorexia nervosa. Journal of Neural Transmission 2008, 115:921-927.
17. Ehrlich S., Franke L., Schneider N., Salbach-Andrae H., Schott R., Craciun E.M., et al. Aromatic amino acids in weight-recovered females with anorexia nervosa. International Journal of Eating Disorders 2009, 42:166-172.
18. Fetissov S.O., Hamze Sinno M., Coquerel Q., Do Rego J.C., Coeffier M., Gilbert D., et al. Emerging role of autoantibodies against appetite-regulating neuropeptides in eating disorders. Nutrition 2008, 24:854-859.
19. Fichter M., Quadflieg N. SIAB. Strukturiertes Inventar für Anorektische und Bulimische Essstörungen nach DSM-IV und ICD-10 1999, Huber, Bern.
20. Frieling H., Albrecht H., Jedtberg S., Gozner A., Lenz B., Wilhelm J., et al. Elevated cannabinoid 1 receptor mRNA is linked to eating disorder related behavior and attitudes in females with eating disorders. Psychoneuroendocrinology 2009, 34:620-624.
21. Frieling H., Gozner A., Romer K.D., Lenz B., Bonsch D., Wilhelm J., et al. Global DNA hypomethylation and DNA hypermethylation of the alpha synuclein promoter in females with anorexia nervosa. Molecular Psychiatry 2007, 12:229-230.
22. Gavrila A., Chan J.L., Miller L.C., Heist K., Yiannakouris N., Mantzoros C.S. Circulating melanin-concentrating hormone, agouti-related protein, and alpha-melanocyte-stimulating hormone levels in relation to body composition: alterations in response to food deprivation and recombinant human leptin administration. Journal of Clinical Endocrinology & Metabolism 2005, 90:1047-1054.
23. Hancock S.D., Menard J.L., Olmstead M.C. Variations in maternal care influence vulnerability to stress-induced binge eating in female rats. Physiology & Behavior 2005, 85:430-439.
24. Hebebrand J., Muller T.D., Holtkamp K., Herpertz-Dahlmann B. The role of leptin in anorexia nervosa: clinical implications. Molecular Psychiatry 2007, 12:23-35.
25. Heijnen C.J., Kavelaars A., Ballieux R.E. Beta-endorphin: cytokine and neuropeptide. Immunological Reviews 1991, 119:41-63.
26. Inui A. Eating behavior in anorexia nervosa - an excess of both orexigenic and anorexigenic signalling?. Molecular Psychiatry 2001, 6:620-624.
27. Jeannotte L., Burbach J.P., Drouin J. Unusual proopiomelanocortin ribonucleic acids in extrapituitary tissues: intronless transcripts in testes and long poly(A) tails in hypothalamus. Molecular Endocrinology 1987, 1:749-757.
28. Kaye W.H., Berrettini W.H., Gwirtsman H.E., Chretien M., Gold P.W., George D.T., et al. Reduced cerebrospinal fluid levels of immunoreactive pro-opiomelanocortin related peptides (including beta-endorphin) in anorexia nervosa. Life Sciences 1987, 41:2147-2155.
29. Kim E.M., Welch C.C., Grace M.K., Billington C.J., Levine A.S. Chronic food restriction and acute food deprivation decrease mRNA levels of opioid peptides in arcuate nucleus. American Journal of Physiology 1996, 270:R1019-R1024.
30. Kim Y., Michael A.F. Hypocomplementemia in anorexia nervosa. Journal of Pediatrics 1975, 87:582-585.
31. Krieger D.T., Yamaguchi H., Liotta A.S. Human plasma ACTH, lipotropin, and endorphin. Advances in Biochemical Psychopharmacology 1981, 28:541-556.
32. Kromeyer-Hauschild K., et al. Perzentile für den Body Mass Index für das Kindes- und Jugendalter unter Heranziehung verschiedener deutscher Stichproben. Monatsschrift Kinderheilkunde 2001, 149:807-818.
33. Krude H., Biebermann H., Luck W., Horn R., Brabant G., Gruters A. Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nature Genetics 1998, 19:155-157.
34. Lacaze-Masmonteil T., de Keyzer Y., Luton J.P., Kahn A., Bertagna X. Characterization of proopiomelanocortin transcripts in human nonpituitary tissues. Proceedings of the National Academy of Sciences of the United States of America 1987, 84:7261-7265.
35. Lo Sauro C., Ravaldi C., Cabras P.L., Faravelli C., Ricca V. Stress, hypothalamic-pituitary-adrenal axis and eating disorders. Neuropsychobiology 2008, 57:95-115.
36. Lyons P.D., Blalock J.E. The kinetics of ACTH expression in rat leukocyte subpopulations. Journal of Neuroimmunology 1995, 63:103-112.
37. Marcos A., Nova E., Montero A. Changes in the immune system are conditioned by nutrition. European Journal of Clinical Nutrition 2003, 57(Suppl. 1):S66-S69.
38. McShane T.M., Petersen S.L., McCrone S., Keisler D.H. Influence of food restriction on neuropeptide-Y, proopiomelanocortin, and luteinizing hormone-releasing hormone gene expression in sheep hypothalami. Biology of Reproduction 1993, 49:831-839.
39. Medhurst A.D., Harrison D.C., Read S.J., Campbell C.A., Robbins M.J., Pangalos M.N. The use of TaqMan RT-PCR assays for semiquantitative analysis of gene expression in CNS tissues and disease models. Journal of Neuroscience Methods 2000, 98:9-20.
40. Miller D.B., O'Callaghan J.P. Neuroendocrine aspects of the response to stress. Metabolism 2002, 51:5-10.
41. Murgatroyd C., Patchev A.V., Wu Y., Micale V., Bockmuhl Y., Fischer D., et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nature Neuroscience 2009, 12:1559-1566.
42. Newell-Price J. Proopiomelanocortin gene expression and DNA methylation: implications for Cushing's syndrome and beyond. Journal of Endocrinology 2003, 177:365-372.
43. Newell-Price J., King P., Clark A.J. The CpG island promoter of the human proopiomelanocortin gene is methylated in nonexpressing normal tissue and tumors and represses expression. Molecular Endocrinology 2001, 15:338-348.
44. Oates E.L., Allaway G.P., Armstrong G.R., Boyajian R.A., Kehrl J.H., Prabhakar B.S. Human lymphocytes produce pro-opiomelanocortin gene-related transcripts. Effects of lymphotropic viruses. Journal of Biological Chemistry 1988, 263:10041-10044.
45. Poggioli R., Vergoni A.V., Bertolini A. ACTH-(1-24) and alpha-MSH antagonize feeding behavior stimulated by kappa opiate agonists. Peptides 1986, 7:843-848.
46. Putignano P., Dubini A., Toja P., Invitti C., Bonfanti S., Redaelli G., et al. Salivary cortisol measurement in normal-weight, obese and anorexic women: comparison with plasma cortisol. European Journal of Endocrinology 2001, 145:165-171.
47. Rajora N., Ceriani G., Catania A., Star R.A., Murphy M.T., Lipton J.M. Alpha-MSH production, receptors, and influence on neopterin in a human monocyte/macrophage cell line. Journal of Leukocyte Biology 1996, 59:248-253.
48. Rathner G., Waldherr K. Eating Disorder Inventory-2. Eine deutschsprachige Validierung mit Normen für weibliche und männliche Jugendliche. Zeitschrift für Klinische Psychologie, Psychiatrie und Psychotherapie 1997, 45:157-182.
49. Rees D.A., Hepburn P.J., McNicol A.M., Francis K., Jasani B., Lewis M.D., et al. Loss of ACTH expression in cultured human corticotroph macroadenoma cells is consistent with loss of the POMC gene signal sequence. Molecular and Cellular Endocrinology 2002, 189:51-57.
50. Rosenberger P., Muhlbauer E., Weissmuller T., Rommelspacher H., Sinha P., Wernecke K.D., et al. Decreased proopiomelanocortin mRNA in lymphocytes of chronic alcoholics after intravenous human corticotropin releasing factor injection. Alcoholism: Clinical and Experimental Research 2003, 27:1693-1700.
51. Rossi M., Kim M.S., Morgan D.G., Small C.J., Edwards C.M., Sunter D., et al. A C-terminal fragment of Agouti-related protein increases feeding and antagonizes the effect of alpha-melanocyte stimulating hormone in vivo. Endocrinology 1998, 139:4428-4431.
52. Schulz C., Paulus K., Lobmann R., Dallman M.F., Lehnert H. Endogenous ACTH, not only {alpha}-melanocyte stimulating hormone, reduces food intake mediated by hypothalamic mechanisms. American Journal of Physiology Endocrinology and Metabolism 2009.
53. Slominski A., Plonka P.M., Pisarchik A., Smart J.L., Tolle V., Wortsman J., et al. Preservation of eumelanin hair pigmentation in proopiomelanocortin-deficient mice on a nonagouti (a/a) genetic background. Endocrinology 2005, 146:1245-1253.
54. Smith A.I., Funder J.W. Proopiomelanocortin processing in the pituitary, central nervous system, and peripheral tissues. Endocrine Reviews 1988, 9:159-179.
55. Steinman L. Elaborate interactions between the immune and nervous systems. Nature Immunology 2004, 5:575-581.
56. Stephanou A., Fitzharris P., Knight R.A., Lightman S.L. Characteristics and kinetics of proopiomelanocortin mRNA expression by human leucocytes. Brain, Behavior, and Immunity 1991, 5:319-327.
57. Tsankova N.M., Berton O., Renthal W., Kumar A., Neve R.L., Nestler E.J. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nature Neuroscience 2006, 9:519-525.
58. Tung Y.C., Piper S.J., Yeung D., O'Rahilly S., Coll A.P. A comparative study of the central effects of specific proopiomelancortin (POMC)-derived melanocortin peptides on food intake and body weight in pomc null mice. Endocrinology 2006, 147:5940-5947.
59. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., et al. Epigenetic programming by maternal behavior. Nature Neuroscience 2004, 7:847-854.
60. Wikberg J.E., Muceniece R., Mandrika I., Prusis P., Lindblom J., Post C., et al. New aspects on the melanocortins and their receptors. Pharmacol Res 2000, 42:393-420.
61. Woods S.C., Seeley R.J., Porte D., Schwartz M.W. Signals that regulate food intake and energy homeostasis. Science 1998, 280:1378-1383.
62. Yi P., Melnyk S., Pogribna M., Pogribny I.P., Hine R.J., James S.J. Increase in plasma homocysteine associated with parallel increases in plasma S-adenosylhomocysteine and lymphocyte DNA hypomethylation. Journal of Biological Chemistry 2000, 275:29318-29323.
63. Zhang F., Chen Y., Heiman M., Dimarchi R. Leptin: structure, function and biology. Vitamins and Hormones 2005, 71:345-372.
64. Zhao S., Fernald R.D. Comprehensive algorithm for quantitative real-time polymerase chain reaction. Journal of Computational Biology 2005, 12:1047-1064.