Role of the evolutionarily conserved starvation response in anorexia nervosa

Molecular Psychiatry

Volumn 16, Issue 6, 2011, Pages 595-603

  Dwyer, D S ^a,b   Horton, R Y ^a   Aamodt, E J ^b  

^a Louisiana State University Health Sciences Center   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Akt; anorexia nervosa; FOXO; Insulin IGF 1

Indexed keywords

ANXIOLYTIC AGENT; F BOX PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; INSULIN; NEUROLEPTIC AGENT; NEUROTRANSMITTER; OLANZAPINE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; XANOMELINE;

AMBIVALENCE; ANOREXIA NERVOSA; ANXIETY DISORDER; APPETITE; BEHAVIOR THERAPY; BODY WEIGHT; CAENORHABDITIS ELEGANS; CALORIC RESTRICTION; CULTURAL FACTOR; DELUSION; DROSOPHILA MELANOGASTER; ENVIRONMENTAL FACTOR; EXPERIMENTAL MOUSE; FOOD INTAKE; GENE LOCATION; GENE MAPPING; GENETIC CONSERVATION; GENETIC RISK; HUMAN; MENTAL DISEASE; METABOLIC DISORDER; NONHUMAN; OBSESSION; PRIORITY JOURNAL; PROTEIN FUNCTION; PSYCHOSIS; PSYCHOTHERAPY; REGULATORY MECHANISM; REVIEW; SACCHAROMYCES CEREVISIAE; SIDE EFFECT; SIGNAL TRANSDUCTION; STARVATION;

ANIMALS; ANOREXIA NERVOSA; BIOLOGICAL EVOLUTION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MALE; MODELS, BIOLOGICAL; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION; STARVATION;

EID: 79957501400     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2010.95     Document Type: Review

References (94)

1. Fairburn CG, Harrison PJ. Eating disorders. Lancet 2003; 361: 407-416. (Pubitemid 36164979)
2. Treasure JL. Getting beneath the phenotype of anorexia nervosa: the search for viable endophenotypes and genotypes. Can J Psychiatry 2007; 52: 212-219. (Pubitemid 46743467)
3. Bulik CM, Slof-Op't Landt MCT, van Furth EF, Sullivan PF. The genetics of anorexia nervosa. Annu Rev Nutr 2007; 27: 263-275. (Pubitemid 351373358)
4. Zandian M, Ioakimidis I, Bergh C, Södersten P. Cause and treatment of anorexia nervosa. Physiol Behav 2007; 92: 283-290. (Pubitemid 47381383)
5. Morris J, Twaddle S. Anorexia nervosa. Br Med J 2008; 334: 894-898. (Pubitemid 46724332)
6. Keel PK, Klump KL. Are eating disorders culture-bound syndromes? Implications for conceptualizing their etiology. Psychol Bull 2003; 129: 747-769. (Pubitemid 37394949)
7. Hoek HW. Incidence, prevalence and mortality of anorexia nervosa and other eating disorders. Curr Opin Psychiatry 2006; 19: 389-394. (Pubitemid 44317865)
8. Robergeau K, Joseph J, Silber TJ. Hospitalization of children and adolescents for eating disorders in the State of New York. J Adolesc Health 2006; 39: 806-810. (Pubitemid 44751503)
9. Keys A, Brozek J, Henschel A, Mickelsen O, Taylor HL. The Biology of Human Starvation. University of Minnesota Press: Minneapolis, MN, 1950.
10. Wang T, Hung CC, Randall DJ. The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 2006; 68: 223-251.
11. Emery PW. Metabolic changes in malnutrition. Eye 2005; 19: 1029-1034. (Pubitemid 41823759)
12. Schwartz MW, Dallman MF, Woods SC. Hypothalamic response to starvation: implications for the study of wasting disorders. Am J Physiol 1995; 269: R949-R957. (Pubitemid 3005939)
13. Barbieri M, Bonafe M, Franceschi C, Paolisso G. Insulin/IGF-1 signaling pathway: an evolutionarily conserved mechanism of longevity from yeast to humans. Am J Physiol 2003; 285: E1064-E1071. (Pubitemid 37296328)
14. Mazet F, Yu JK, Liberles DA, Holland LZ, Shimeld SM. Phylogenetic relationships of the Fox (Forkhead) gene family in the Bilateria. Gene 2003; 316: 79-89. (Pubitemid 37249355)
15. Kaufmann E, Knöchel W. Five years on the wings of fork head. Mec Dev 1996; 57: 3-20. (Pubitemid 26197454)
16. Van der Heide LP, Hoekman MF, Smidt MP. The ins and outs of Fox O shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J 2004; 380: 297-309. (Pubitemid 38788101)
17. Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci 2007; 120: 2479-2487. (Pubitemid 47323857)
18. Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 1992; 68: 1077-1090.
19. Zhu G, Spellman PT, Volpe T, Brown PO, Botstein D, Davis TN et al. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 2000; 406: 90-94. (Pubitemid 30460217)
20. Szilagyi Z, Batta G, Enczi K, Sipiczki M. Characterisation of two novel fork head gene homologues of Schizosaccharomyces pombe: their involvement in cell cycle and sexual differentiation. Gene 2005; 348: 101-109. (Pubitemid 40410021)
21. Pramila T, Wu W, Miles S, Noble WS, Breeden LL. The Forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes Dev 2006; 20: 2266-2278.
22. Dwyer DS, Donohoe DR, Aamodt EJ. Insulin/IGF-1 signaling in C. elegans regulates foraging and feeding. Soc Neurosci Abstr Online 2009 Program No. 275.18.
23. Mohri A, Kodama E, Kimura KD, Koike M, Mizuno T, Mori I. Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics 2005; 169: 1437-1450. (Pubitemid 40547455)
24. Kodama E, Kuhara A, Mohri-Shiomi A, Kimura KD, Okumura M, Tomioka M et al. Insulin-like signaling and the neural circuit for integrative behavior in C.elegans. Genes Dev 2006; 20: 2955-2960. (Pubitemid 44771730)
25. You Y, Kim J, Raizen DM, Avery L. Insulin, cGMP, and TGF-b signals regulate food intake and quiescence in C. elegans: a model for satiety. Cell Metab 2008; 7: 249-257. (Pubitemid 351285528)
26. Aschenbrenner K, Scholze N, Joraschky P, Hummel T. Gustatory and olfactory sensitivity in patients with anorexia and bulimia in the course of treatment. J Psychiatry Res 2008; 43: 129-137.
27. Roessner V, Bleich S, Banaschewski T, Rothenburger A. Olfactory deficits in anorexia nervosa. Eur Arch Psychiatry Clin Neurosci 2005; 255: 6-9. (Pubitemid 40558099)
28. Fedoroff IC, Stoner SA, Andersen AE, Doty RL, Rolls BJ. Olfactory dysfunction in anorexia and bulimia nervosa. Int J Eat Disord 1995; 18: 71-77.
29. Rousseaux M, Muller P, Gahide I, Mottin Y, Romon M. Disorders of smell, taste and food intake in a patient with a dorsomedial thalamic infarct. Stroke 1996; 27: 2328-2330. (Pubitemid 26427214)
30. Gray JM, Hill JJ, Bargmann CI. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci USA 2005; 102: 3184-3191. (Pubitemid 40328020)
31. Wakabayashi T, Osada T, Shingai R. Serotonin deficiency shortens the duration of forward movement in Caenorhabditis elegans. Biosci Biotechnol Biochem 2005; 69: 1767-1770. (Pubitemid 41390167)
32. Donohoe DR, Phan T, Weeks K, Aamodt EJ, Dwyer DS. Antipsychotic drugs up-regulate tryptophan hydroxylase in ADF neurons of Caenorhabditis elegans: role of calcium-calmodulindependent protein kinase II and transient receptor potential vanilloid channel. J Neurosci Res 2008; 86: 2553-2563.
33. Hills T, Brockie PJ, Maricq AV. Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J Neurosci 2004; 24: 1217-1225. (Pubitemid 38177028)
34. Meguid MM, Fetissov SO, Varma M, Sato T, Zhang L, Laviano A et al. Hypothalamic dopamine and serotonin in the regulation of food intake. Nutrition 2000; 16: 843-857.
35. Kramer JM, Davidge JT, Lockyer JM, Staveley BE. Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev Biol 2003; 3: 1-14. (Pubitemid 38783255)
36. Britton JS, Lockwood WK, Li L, Cohen SM, Edgar BA. Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev Cell 2002; 2: 239-249. (Pubitemid 38351588)
37. Son JH, Baker H, Park DH, Joh TH. Drastic and selective hyperinnervation of central serotonergic neurons in a lethal neurodevelopmental mouse mutant, Anorexia (anx). Mol Brain Res 1994; 25: 129-134. (Pubitemid 24223272)
38. Tecott LH, Sun LM, Akana SF, Strack AM, Lowenstein DH, Dallman MF et al. Eating disorder and epilepsy in mice lacking 5-HT2C serotonin receptors. Nature 1995; 374: 542-546.
39. Zhou QY, Palmiter RD. Dopamine-deficient mice are severely hypoactive, adipsic and aphagic. Cell 1995; 83: 1197-1209. (Pubitemid 26007810)
40. Yamada M, Miyakawa T, Duttaroy A, Yamanaka A, Moriguchi T, Makita R et al. Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Nature 2001; 410: 207-212. (Pubitemid 32216592)
41. Gautam D, Han S-J, Duttaroy A, Mears D, Hamdan FF, Li JH et al. Role of the M3 muscarinic acetylcholine receptor in b-cell function and glucose homeostasis. Diabetes Obes Metab 2007; 9(Suppl 2): 158-169. (Pubitemid 47543138)
42. Liang B, Moussaif M, Kuan C, Gargus JJ, Sze JY. Serotonin targets the DAF-16/FOXO signaling pathway to modulate stress responses. Cell Metab 2006; 4: 429-440. (Pubitemid 44817353)
43. Burks DJ, de Mora JF, Schubert M, Withers DJ, Myers MG, Towery HH et al. IRS-2 pathways integrate female reproduction and energy homeostasis. Nature 2000; 407: 377-382.
44. Stoving RK, Chen J-W, Glintborg D, Brixen K, Flyvberg A, Horder K, Frystyk J. Bioactive insulin-like growth factor (IGF) I and IGFbinding protein-1 in anorexia nervosa. J Clin Endocrinol Metab 2007; 92: 2323-2329. (Pubitemid 46997141)
45. Boonstra VH, Arends NJ, Stijnen T, Blum WF, Akkerman O, Hokken-Koelega AC. Food intake of children with short stature born small for gestational age before and during a randomized GH trial. Hormone Res 2006; 65: 23-30. (Pubitemid 43177314)
46. Plum L, Schubert M, Bruning JC. The role of insulin receptor signaling in the brain. Trends Endocrinol Metab 2005; 16: 59-65. (Pubitemid 40270851)
47. Phillips LS, Harp JB, Goldstein S, Klein J, Pao C-I. Regulation and action of insulin-like growth factors at the cellular level. Proc Nutr Soc 1990; 49: 451-458.
48. Brismar K, Fernqvist-Forbes E, Wahren J, Hall K. Effect of insulin on the hepatic production of insulin-like growth factor-binding protein-1 (IGFBP-1), IGFBP-3, and IGF-1 in insulin-dependent diabetes. J Clin Endocrinol Metab 1994; 79: 872-878.
49. Satoh M, Yoshizawa A, Takesue M, Saji T, Yokoya S. Long-term effects of recombinant human insulin-like growth factor I treatment on glucose and lipid metabolism and the growth of a patient with congenital generalized lipodystrophy. Endocrine J 2006; 53: 639-645. (Pubitemid 44691016)
50. Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP et al. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 2007; 282: 30107-30119. (Pubitemid 350035296)
51. Hardie DG, Scott JW, Pan DA, Hudson ER. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 2003; 546: 113-120. (Pubitemid 36782291)
52. Kola B. Role of AMP-activated protein kinase in the control of appetite. J Neuroendocrinol 2008; 20: 942-951. (Pubitemid 351859112)
53. Minokoshi Y, Alquier T, Furukawa N, Kim Y-B, Lee A, Xue B et al. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 2004; 428: 569-574. (Pubitemid 38480541)
54. Sarbassov DD, Ali SM, Sabatini DM. Growing roles for the mTOR pathway. Curr Opin Cell Biol 2005; 17: 596-603. (Pubitemid 41540408)
55. Shaw RJ. LKB1 and AMP-activated protein kinase control of mTOR signaling and growth. Acta Physiol 2009; 196: 65-80.
56. Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, Choudhury AI et al. Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 2009; 326: 140-144.
57. Jia K, Chen D, Riddle DL. The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development 2004; 131: 3897-3906. (Pubitemid 39232150)
58. Estevez AO, Cowie RH, Gardner KL, Estevez M. Both insulin and calcium channel signaling are required for developmental regulation of serotonin synthesis in the chemosensory ADF neurons of Caenorhabditis elegans. Dev Biol 2006; 298: 32-44. (Pubitemid 44414793)
59. Ferri AL, Lin W, Mavromatakis YE, Sasaki H, Whitsett JA, Ang S-L. Foxa1 and Foxa2 regulate multiple phases of midbrain dopaminergic neuron development in a dosage-dependent manner. Development 2007; 134: 2761-2769. (Pubitemid 47307232)
60. Kim M-S, Pak YK, Jang P-G, Namkoong C, Choi Y-S, Won J-C et al. Role of hypothalamic Foxo1 in the regulation of food intake and energy homeostasis. Nat Neurosci 2006; 9: 901-906. (Pubitemid 43980504)
61. Weinkove D, Halstead JR, Gems D, Divecha N. Long-term starvation and ageing induce AGE-1/PI3-kinase-dependent translocation of DAF-16/FOXO to the cytoplasm. BMC Biol 2006; 4: 1.
62. Coburn CM, Mori I, Ohshima Y, Bargmann CI. A cyclic nucleotidegated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure. Development 1998; 125: 249-258. (Pubitemid 28064438)
63. Riediger T, Giannini P, Erguven E, Lutz T. Nitric oxide directly inhibits ghrelin-activated neurons of the arcuate nucleus. Brain Res 2006; 1125: 37-45. (Pubitemid 44838546)
64. Bulik CM, Sullivan PF, Tozzi F, Furberg H, Lichtenstein P, Pedersen NL. Prevalence, heritability, and prospective risk factors for anorexia nervosa. Arch Gen Psychiatry 2006; 63: 305-312. (Pubitemid 43345355)
65. Bacanu S-A, Bulik CM, Klump KL, Fichter MM, Halmi KA, Keel P et al. Linkage analysis of anorexia and bulimia nervosa cohorts using selected behavioral phenotypes as quantitative traits or covariates. Am J Med Genet B 2005; 139B: 61-68. (Pubitemid 41552300)
66. Devlin B, Bacan S-A, Klump KL, Bulik CM, Fichter MM, Halmi KA et al. Linkage analysis of anorexia nervosa incorporating behavioral covariates. Hum Mol Genet 2002; 11: 689-696. (Pubitemid 34285140)
67. Grice DE, Halmi KA, Fichter MM, Strober M, Woodside DB, Treasure JT et al. Evidence for a susceptibility gene for anorexia nervosa on chromosome 1. Am J Hum Genet 2002; 70: 787-792. (Pubitemid 34177934)
68. Bergen AW, van den Bree MB, Yeager M, Welch R, Ganjei JK, Haque K et al. Candidate genes for anorexia nervosa in the 1p33-36 linkage region: serotonin 1D and delta opioid receptor loci exhibit significant association to anorexia nervosa. Mol Psychiatry 2003; 8: 397-406. (Pubitemid 36609664)
69. Chagnon YC, Borecki IB, Perusse L, Roy S, Lacaille M, Chagnon M et al. Genome-wide search for genes related to the fat-free body mass in the Quebec Family Study. Metabolism 2000; 49: 203-207. (Pubitemid 30090884)
70. Wauman J, De Smet A, Catteeuw D, Belsham D, Tavernier J. Insulin receptor substrate 4 couples the leptin receptor to multiple signaling pathways. Mol Endocrinol 2008; 22: 965-977. (Pubitemid 351482831)
71. Bergh C, Södersten P. Anorexia nervosa, self-starvation and the reward of stress. Nat Med 1996; 2: 21-22. (Pubitemid 26029568)
72. Fessler DMT. The implications of starvation induced psychological changes for the ethical treatment of hunger strikers. J Med Ethics 2003; 29: 243-247.
73. Korbonits M, Blaine D, Elia M, Powell-Tuck J. Metabolic and hormonal changes during the refeeding period of prolonged fasting. Eur J Endocrinol 2007; 157: 157-166. (Pubitemid 47233119)
74. Keel PK, Haedt A. Evidence-based psychosocial treatments for eating problems and eating disorders. J Clin Child Adolesc Psychol 2008; 37: 39-61.
75. Bowers WA. Basic principles for applying cognitive-behavioral therapy to anorexia nervosa. Psychiatr Clin North Am 2001; 24: 293-303. (Pubitemid 32523877)
76. Eisler I, Dare C, Hodes M, Russell G, Dodge E, le Grange D. Family therapy for adolescent anorexia nervosa: the results of a controlled comparison of two family interventions. J Child Psychol Psychiatry 2000; 41: 727-736.
77. Bulik CM, Berkman ND, Brownley KA, Sedway JA, Lohr KN. Anorexia nervosa treatment: a systematic review of randomized controlled trials. Int J Eat Disord 2007; 40: 310-320. (Pubitemid 46651306)
78. Fisher CA, Hetrick SE, Rushford N. Family therapy for anorexia nervosa. Cochrane Database Syst Rev 2010; 4: CD004780.
79. Zhu AJ, Walsh BT. Pharmacologic treatment of eating disorders. Can J Psychiatry 2002; 47: 227-234. (Pubitemid 34614679)
80. Ratzoni G, Gothelf D, Brand-Gothelf A, Reidman J, Kikinzon L, Gal G et al. Weight gain associated with olanzapine and risperidone in adolescent patients: a comparative prospective study. J Am Acad Child Adolesc Psychiatry 2002; 41: 337-343. (Pubitemid 38338156)
81. Dwyer DS, Weeks K, Aamodt EJ. Drug discovery based on genetic and metabolic findings in schizophrenia. Expert Rev Clin Pharmacol 2008; 1: 773-789.
82. Dwyer DS, Donohoe D, Lu X-H, Aamodt EJ. Mechanistic connections between glucose/lipid disturbances and weight gain induced by antipsychotic drugs. Int Rev Neurobiol 2005; 65: 211-247. (Pubitemid 43588584)
83. Mehler C, Wewetzer C, Schulze U, Warnke A, Theisen F, Dittmann RW. Olanzapine in children and adolescents with chronic anorexia nervosa. A study of five cases. Eur Child Adolesc Psychiatry 2001; 10: 151-157. (Pubitemid 32612154)
84. Bissada H, Tasca GA, Barber AM, Bradwejn J. Olanzapine in the treatment of low body weight and obsessive thinking in women with anorexia nervosa: a randomized, double-blind, placebocontrolled trial. Am J Psychiatry 2008; 165: 1281-1288.
85. Grinspoon S, Thomas L, Miller K, Herzog D, Klibanski A. Effects of recombinant human IGF-1 and oral contraceptive administration on bone density in anorexia nervosa. J Clin Endocrinol Metab 2002; 87: 2883-2891. (Pubitemid 34655358)
86. Misra M, McGrane J, Miller KK, Goldstein MA, Ebrahimi S, Weigel T et al. Effects of rhIGF-1 administration on surrogate markers of bone turnover in adolescents with anorexia nervosa. Bone 2009; 45: 493-498.
87. Clark RG. Recombinant human insulin-like growth factor 1 (IGF-1): risks and benefits of normalizing blood IGF-1 concentrations. Hormone Res 2004; 62(Suppl 1): 93-100. (Pubitemid 40529157)
88. Rosenbloom AL. Mecasermin (recombinant human insulin-like growth factor I). Adv Ther 2009; 26: 40-54.
89. Shekhar A, Potter WZ, Lightfoot J, Lienemann J, Dube S, Mallinckrodt C et al. Selective muscarinic receptor agonist xanomeline as a novel treatment approach for schizophrenia. Am J Psychiatry 2008; 165: 1033-1039.
90. Bodick NC, Offen WW, Levey AI, Cutler NR, Gauthier SG, Satlin A et al. Effects of xanomeline, a selective muscarinic receptor agonist, on cognitive function and behavioral symptoms in Alzheimer disease. Arch Neurol 1997; 54: 465-473. (Pubitemid 27172867)
91. Dubois A, Gross HA, Richter JE, Ebert MH. Effect of bethanechol on gastric functions in primary anorexia nervosa. Digest Dis Sci 1981; 26: 598-600. (Pubitemid 11093384)
92. You Y, Kin J, Cobb M, Avery L. Starvation activates MAP kinase through the muscarinic acetylcholine pathway in Caenorhabditis elegans pharynx. Cell Metab 2006; 3: 237-245.
93. Tissenbaum HA, Hawdon J, Perregaux M, Hotez P, Guarente L, Ruvkun G. A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. Proc Natl Acad Sci USA 2000; 97: 460-465. (Pubitemid 30055853)
94. Altar CA, Hunt RA, Jurata LW, Webster MJ, Derby E, Gallagher P et al. Insulin, IGF-1, and muscarinic agonists modulate schizophrenia- associated genes in human neuroblastoma cells. Biol Psychiatry 2008; 64: 1077-1087.