Genetic Basis for Sleep Regulation and Sleep Disorders

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Genetic Basis for Sleep Regulation and Sleep Disorders Genetic Basis for Sleep Regulation and Sleep Disorders David M. Raizen, M.D., Ph.D.,1,2 Thornton B.A. Mason, M.D., Ph.D., M.S.C.E.,2,3 and Allan I. Pack, M.B., Ch.B., Ph.D.1,4 ABSTRACT Sleep disorders arise by an interaction between the environment and the genetic makeup of the individual but the relative contribution of nature and nurture varies with diseases. At one extreme are the disorders with simple Mendelian patterns of inheritance such as familial advanced sleep phase syndrome, and at the other extreme are diseases such as insomnia, which can be associated with a multitude of medical and psychiatric conditions. In this article, we review data on the relative contribution of genetic and environmental factors in the pathogenesis of various sleep disorders. The understanding of many of these disorders has been advanced by the study of sleep and circadian rhythms in model laboratory organisms. We summarize this model system research and how it relates to human sleep disorders. The current challenge in this field is the identification of susceptibility genetic loci for complex diseases such as obstructive sleep apnea. We anticipate such identification will increase our ability to assess risk for disease before symptom onset and by doing so will shift the focus from treatment to prevention of disease. KEYWORDS: Sleep, genetics, circadian, homeostatic CIRCADIAN REGULATION OF SLEEP mammals, a retinal photoreceptor molecule—mela- AND CIRCADIAN SLEEP DISORDERS nopsin, which is found in retinal ganglion cells but not rods and cones—transduces the light entrainment The Circadian Clock signal. This signal is carried to the suprachiasmatic Virtually all organisms display biologic rhythms, nucleus (SCN), the site of the central circadian clock, called circadian rhythms, which are synchronized to by the retinohypothalamic tract (for review, see Peir- the 24-hour earth rotation cycle. In addition to son and Foster1). Another entrainment signal, re- Downloaded by: University of Pennsylvania Libraries. Copyrighted material. having an approximate 24-hour period, circadian stricted feeding, does not require the SCN.2 Finally, clocks have a few other key properties. First, they circadian clocks show temperature compensation, are free running. That is, they continue to keep time where the period remains constant at different tem- even in the absence of external cues. However, nor- peratures. Control of circadian rhythm of three phys- mally clocks are entrained to external cues provided by iological variables—sleep, core body temperature, and the environment. The best understood entraining melatonin secretion—is anatomically housed in neu- signal is light, which changes with sun exposure. In rons of the SCN in the hypothalamus. 1Center for Sleep and Respiratory Neurobiology, University of Penn- M.B., Ch.B., Ph.D., Center for Sleep and Respiratory Neurobiology, sylvania School of Medicine, Philadelphia, Pennsylvania; 2Department University of Pennsylvania School of Medicine, 125 South 31st Street, of Neurology, University of Pennsylvania School of Medicine, Phila- Suite 2100, Philadelphia, PA 19104-3403. delphia, Pennsylvania; 3Department of Pediatrics, Children’s Hospital Genetics of Common Neurologic Diseases; Guest Editor, John K. of Philadelphia, University of Pennsylvania School of Medicine, Fink, M.D. Philadelphia, Pennsylvania; 4Division of Sleep Medicine, Department Semin Neurol 2006;26:467–483. Copyright # 2006 by Thieme of Medicine, University of Pennsylvania School of Medicine, Phila- Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, delphia, Pennsylvania. USA. Tel: +1(212) 584-4662. Address for correspondence and reprint requests: Allan I. Pack, DOI 10.1055/s-2006-951619. ISSN 0271-8235. 467 468 SEMINARS IN NEUROLOGY/VOLUME 26, NUMBER 5 2006 In 1971, Ron Konopka and Seymour Benzer three human per genes, the possibility that there was a ushered in the modern era of circadian research when mutation in the per2 gene itself was immediately they published a description of the first three circadian appreciated. Indeed, there was a mutation of a con- mutants, which they had identified in the fruit fly served serine amino acid, in a region of the protein Drosophila melanogaster.3 These three mutants turned known to bind caseine kinase 1e.5 Tohetalwentonto out to be different mutations in the same gene, which demonstrate in vitro that this mutation causes reduced they named period or per. Per turned out to be an integral phosphorylation of PER by caseine kinase 1e.5 Given part of the core molecular machinery that makes up the what was known from work in Drosophila and rodents clock. There is one per gene in Drosophila but three about the mechanism of regulation of circadian period, separate per genes in mammals. a possible explanation for the short period that has been The 35 years of intense research that followed the shown in these FASPS patients is that the PER protein identification of per mutants have led to a remarkably mutation results in reduced phosphorylation of this detailed understanding of the molecular underpinnings protein, increasing its stability and cytoplasmic con- of the circadian clock.4 This clock mechanism, which is centration, and therefore promoting its precocious en- phylogenetically conserved and similar in flies and mam- try into the nucleus. Research is ongoing to test this mals, consists of a cell-autonomous transcriptional- model. translational negative feedback loop. At the core of the Recently, a genetic association study showed that clock are a pair of transcription factors, CLOCK and another single nucleotide polymorphism in the 50-un- BMAL1, that activate per gene transcription as well as translated region of per2 was more likely to be found in transcription of other genes, cryptochrome or cry (the patients with extreme morning preference than in pa- identity of this second gene is one arena in which tients with evening preference.7 The biochemical and mammals and fruit flies differ as in Drosophila, the cell biologic consequences of this polymorphism are PER partner is TIMELESS). The mRNA from these unknown. genes is transported to the cell cytoplasm, where it is Not long after the identification of the disease translated into protein. In the cytoplasm, PER proteins gene in this first FASPS family, a second gene causing form a heterodimer with CRY proteins; when this FASPS was identified in a different family. However, protein complex reaches a critical concentration, it trans- this time the trait was not linked to any of the three locates back into the nucleus. In the nucleus, this com- human per genes. It was instead linked to the protein plex then negatively regulates the positive transcriptional kinase casein kinase 1d.8 Amutationinaconserved activity of CLK:BMAL1, at which point the negative threonine resulted in reduced activity of the enzyme in feedback loop is completed. vitro. To show that this mutation was causing the A major determinant of the duration of this patient syndrome and was not simply a linked poly- molecular oscillation is the time it takes PER proteins to morphism, Xu and colleagues made elegant use of the reach the critical concentration in the cytoplasm to be previously established animal models for circadian transported back into the nucleus. Proteolytic degrada- rhythm studies by demonstrating an alteration of the tion lowers PER concentrations and therefore turns circadian clock in both mice and fruit flies.8 Although out to be a key site for regulation of this process. PER the in vivo phosphorylation substrate for casein kinase proteins are marked for degradation by phosphorylation 1d remains unknown, these findings show that protein by one or more protein kinases. Therefore, mutations in phosphorylation is a major determinant of the period of either the kinases themselves or in the amino acids in human circadian rhythms, just as it is in Drosophila, Downloaded by: University of Pennsylvania Libraries. Copyrighted material. PER, which the kinases phosphorylate, would be pre- mice, and hamsters. dicted to stabilize PER protein, expedite its nuclear entry, and therefore shorten the period of the clock. Delayed Sleep Phase Syndrome: Is There a Genetic Etiology? Advanced Sleep Phase Syndrome The identification of two genes, which are implicated in Thirty years after the publication of Konopka and the circadian clock of model organisms as the cause for Benzer’s pioneering work on per mutants in Drosophila, FASPS, leads to an optimistic expectation that for the a mutation in one of the three human per genes, per2, opposite phenotype, delayed sleep phase syndrome, was found to account for an autosomal-dominant circa- underlying genetic lesions will also be identified. This dian sleep disorder called familial advanced sleep phase optimism is tempered, however, by a few points. First, syndrome (FASPS).5 Affected members of this extended delayedsleepphasesyndromeismorecommonthan family have a sleep onset and waking time that are 3 to 4 advanced sleep phase syndrome; therefore, if there is a hours earlier than unaffected family members.6 When genetic predisposition, it is more likely to be genetically Ptacek and colleagues mapped the FASPS trait to a heterogeneous. Second, it is evident that environmental region of chromosome 2q known to contain one of the psychosocial variables influence the likelihood of GENETIC BASIS FOR SLEEP REGULATION AND SLEEP DISORDERS/RAIZEN ET AL 469 delayed sleep phase. Social activities, television shows, HOMEOSTATIC REGULATION OF SLEEP and Internet
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