The first-line cluster headache medication verapamil alters the circadian period and elicits sex-specific sleep changes in mice

References

• Abais JM, Xia M, Li G, Chen Y, Conley SM, Gehr TWB, Boini KM, Li PL. 2014. Nod-like receptor protein 3 (NLRP3) inflammasome activation and podocyte injury via thioredoxin-interacting protein (TXNIP) during hyperhomocysteinemia. J Biol Chem. 289(39):27159–27168. doi:https://doi.org/10.1074/jbc.M114.567537
   PubMed Web of Science ®Google Scholar
• Akerman S, Holland PR, Lasalandra MP, Goadsby PJ. 2009. Oxygen inhibits neuronal activation in the trigeminocervical complex after stimulation of trigeminal autonomic reflex, but not during direct dural activation of trigeminal afferents: harold g. wolff lecture award winner. Headache. 49(8):1131–1143. doi:https://doi.org/10.1111/j.1526-4610.2009.01501.x
   PubMed Web of Science ®Google Scholar
• Albrecht U. 2012. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron. 74(2):246–260. doi:https://doi.org/10.1016/j.neuron.2012.04.006
   PubMed Web of Science ®Google Scholar
• Arkink EB, Schmitz N, Schoonman GG, Van Vliet JA, Haan J, Van Buchem MA, Ferrari MD, Kruit MC. 2017. The anterior hypothalamus in cluster headache. 37. 11:1039–1050. doi:https://doi.org/10.1177/0333102416660550
   Google Scholar
• Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG. 2002. Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet. 32(6):435–443. doi:https://doi.org/10.1023/A:1020884312053
   PubMed Web of Science ®Google Scholar
• Barloese M, Lund N, Petersen A, Rasmussen M, Jennum P, Jensen R. 2015. Sleep and chronobiology in cluster headache. Cephalalgia. 35(11):969–978. doi:https://doi.org/10.1177/0333102414564892
   PubMed Web of Science ®Google Scholar
• Barloese M, Haddock B, Lund NT, Petersen A, Jensen R. 2018. Chronorisk in cluster headache: a tool for individualised therapy? Cephalalgia. 38(14):2058–2067. doi:https://doi.org/10.1177/0333102418769955.
   Google Scholar
• Blau JN, Engel HO. 2004. Individualizing treatment with verapamil for cluster headache patients. Headache J Head Face Pain. 44(10):1013–1018. doi:https://doi.org/10.1111/j.1526-4610.2004.04196.x
   PubMed Web of Science ®Google Scholar
• Bruera O, Sances G, Leston J, Levin G, Cristina S, Medina C, Barontini M, Nappi G, Figuerola MDL. 2008. Plasma melatonin pattern in chronic and episodic headaches. Evaluation during sleep and waking. Funct Neurol. 23(2):77–81.
   PubMed Web of Science ®Google Scholar
• Burish MJ, Chen Z, Yoo SH 2019. Emerging relevance of circadian rhythms in headaches and neuropathic pain. Acta Physiologica. 225(1). doi:https://doi.org/10.1111/apha.13161
   Google Scholar
• Burish MJ, Pearson SM, Shapiro RE, Zhang W, Schor LI. 2020. Cluster headache is one of the most intensely painful human conditions: results from the International Cluster Headache Questionnaire. Headache. doi:https://doi.org/10.1111/head.14021
   Google Scholar
• Chandra M, Shirani J, Shtutin V, Weiss LM, Factor SM, Petkova SB, Rojkind M, Dominguez-Rosales JA, Jelicks LA, Morris SA, et al. 2002. Cardioprotective effects of verapamil on myocardial structure and function in a murine model of chronic Trypanosoma cruzi infection (Brazil Strain): an echocardiographic study. Int J Parasitol. 32(2):207–215. doi:https://doi.org/10.1016/S0020-7519(01)00320-4
   PubMed Web of Science ®Google Scholar
• Chazot G, Claustrat B, Brun J, Jordan D, Sassolas G, Schott B. 1984. A chronobiological study of melatonin, cortisol growth hormone and prolactin secretion in cluster headache. Cephalalgia. 4(4):213–220. doi:https://doi.org/10.1046/j.1468-2982.1984.0404213.x
   PubMed Web of Science ®Google Scholar
• Chen Z, Yoo S-H, Takahashi JS. 2018. Development and Therapeutic potential of small-molecule modulators of circadian systems. Annu Rev Pharmacol Toxicol. 58(1):231–252. doi:https://doi.org/10.1146/annurev-pharmtox-010617-052645
   PubMedGoogle Scholar
• Chen Z, Yoo S-HS-H, Park Y-SY-S, Kim K-HK-H, Wei S, Buhr E, Ye Z-Y, Pan H-LH-L, Takahashi JS. 2012. Identification of diverse modulators of central and peripheral circadian clocks by high-throughput chemical screening. Proc Natl Acad Sci U S A. 109(1):101–106. doi:https://doi.org/10.1073/pnas.1118034108
   PubMed Web of Science ®Google Scholar
• Clelland CD, Zheng Z, Kim W, Bari A, Pouratian N. 2014. Common cerebral networks associated with distinct deep brain stimulation targets for cluster headache. 34. 3:224–230. doi:https://doi.org/10.1177/0333102413509431
   Google Scholar
• Costa M, Squassina A, Piras IS, Pisanu C, Congiu D, Niola P, Angius A, Chillotti C, Ardau R, Severino G, et al. 2015. Preliminary transcriptome analysis in lymphoblasts from cluster headache and bipolar disorder patients implicates dysregulation of circadian and serotonergic genes. J Mol Neurosci. 56(3):688–695. doi:https://doi.org/10.1007/s12031-015-0567-9
   PubMed Web of Science ®Google Scholar
• DHHS, U. S. D. of H. and H. S., FDA, F. and D. A., & CDER, C. for D. E. and R. 2005. Guidance for industry estimating the maximum safe starting dose in initial clinical trials for therapeutics in adult healthy volunteers. https://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ucm078932.pdf
   Google Scholar
• Dickmeis T, Weger BD, Weger M. 2013. The circadian clock and glucocorticoids – interactions across many time scales. Mol Cell Endocrinol. 380(1–2):2–15. doi:https://doi.org/10.1016/j.mce.2013.05.012
   PubMed Web of Science ®Google Scholar
• Dong R, Liu P, Wee L, Butany J, Sole MJ. 1992. Verapamil ameliorates the clinical and pathological course of murine myocarditis. J Clin Invest. 90(5):2022–2030. doi:https://doi.org/10.1172/JCI116082
   PubMed Web of Science ®Google Scholar
• Duong HA, Robles MS, Knutti D, Weitz CJ. 2011. A molecular mechanism for circadian clock negative feedback. Science. 332(6036):1436–1439. doi:https://doi.org/10.1126/science.1196766
   PubMed Web of Science ®Google Scholar
• Edmonds SC, Adler NT. 1977. Food and light as entrainers of circadian running activity in the rat. Physiol Behav. 18(5):915–919. doi:https://doi.org/10.1016/0031-9384(77)90201-3
   PubMed Web of Science ®Google Scholar
• fda.gov. 2019. CALAN SR (verapamil hydrochloride) sustained-release oral caplets: labeling-package insert, suppl-44, reference ID: 4512000. https://www.accessdata.fda.gov/drugsatfda_docs/label/2019/019152s044lbl.pdf
   Google Scholar
• Fischera M, Marziniak M, Gralow I, Evers S. 2008. The incidence and prevalence of cluster headache: a meta-analysis of population-based studies. 28. 6:614–618. doi:https://doi.org/10.1111/j.1468-2982.2008.01592.x
   Google Scholar
• Harriott AM, Strother LC, Vila-Pueyo M, Holland PR. 2019. Animal models of migraine and experimental techniques used to examine trigeminal sensory processing. J Headache Pain. 20(1):91. doi:https://doi.org/10.1186/s10194-019-1043-7
   PubMed Web of Science ®Google Scholar
• Headache Classification Committee of the International Headache Society (IHS). 2018. The international classification of headache disorders, 3rd edition. Cephalalgia. 38(1):1–211. doi:https://doi.org/10.1177/0333102417738202
   Google Scholar
• Hughes S, Jagannath A, Hankins MW, Foster RG, Peirson SN. 2015. Photic regulation of clock systems. Methods Enzymol. 552:125–143. doi:https://doi.org/10.1016/bs.mie.2014.10.018
   PubMed Web of Science ®Google Scholar
• Jarrar RG, Black DF, Dodick DW, Davis DH. 2003. Outcome of trigeminal nerve section in the treatment of chronic cluster headache. Headache. 17(1):39–40. doi:https://doi.org/10.1212/01.wnl.0000055902.23139.16
   Google Scholar
• Ji Lee M, Cho S-J, Wook Park J, Kyung Chu M, Moon H-S, Chung P-W, Myun Chung J, Sohn J-H, Kim B-K, Kim B-S, et al. 2019. Increased suicidality in patients with cluster headache. Cephalalgia. 033310241984566. doi:https://doi.org/10.1177/0333102419845660
   Google Scholar
• Johansson AS, Brask J, Owe-Larsson B, Hetta J, Lundkvist GBS. 2011. Valproic acid phase shifts the rhythmic expression of PERIOD2::LUCIFERASE. J Biol Rhythms. 26(6):541–551. doi:https://doi.org/10.1177/0748730411419775
   PubMed Web of Science ®Google Scholar
• Kandalepas PC, Mitchell JW, Gillette MU. 2016. Melatonin signal transduction pathways require e-box-mediated transcription of Per1 and Per2 to reset the SCN Clock at Dusk. PLoS One. 11(6):e0157824. doi:https://doi.org/10.1371/journal.pone.0157824
   PubMed Web of Science ®Google Scholar
• Lademann V, Jansen J-P, Evers S, Frese A. 2015. Evaluation of guideline-adherent treatment in cluster headache. Cephalalgia. 36(8):760–764. doi:https://doi.org/10.1177/0333102415612774
   PubMed Web of Science ®Google Scholar
• LeGates TA, Fernandez DC, Hattar S. 2014. Light as a central modulator of circadian rhythms, sleep and affect. Nat Rev Neurosci. 15(7):443–454. doi:https://doi.org/10.1038/nrn3743
   PubMed Web of Science ®Google Scholar
• Lemma GL, Wang Z, Hamman MA, Zaheer NA, Gorski JC, Hall SD. 2006. The effect of short- and long-term administration of verapamil on the disposition of cytochrome P450 3A and P-glycoprotein substrates. Clin Pharmacol Ther. 79(3):218–230. doi:https://doi.org/10.1016/j.clpt.2005.11.001
   PubMed Web of Science ®Google Scholar
• Leone M, Lucini V, D’Amico D, Grazzi L, Moschiano F, Fraschini F, Bussone G. 1998. Abnormal 24-hour urinary excretory pattern of 6-sulphatoxymelatonin in both phases of cluster headache. Cephalalgia. 18(10):664–667. doi:https://doi.org/10.1046/j.1468-2982.1998.1810664.x.
   Google Scholar
• Lewis P, Oster H, Korf HW, Foster RG, Erren TC. 2020. Food as a circadian time cue — evidence from human studies. Nat Rev Endocrinol. 16(4):213–223. doi:https://doi.org/10.1038/s41574-020-0318-z
   PubMed Web of Science ®Google Scholar
• Li J, Lu W-Q-Q, Beesley S, Loudon ASII, Meng Q-J-J. 2012. Lithium impacts on the amplitude and period of the molecular circadian clockwork. PLoS One. 7(3):1–8. doi:https://doi.org/10.1371/journal.pone.0033292
   Web of Science ®Google Scholar
• Liu AC, Welsh DK, Ko CH, Tran HG, Zhang EE, Priest AA, Buhr ED, Singer O, Meeker K, Verma IM, et al. 2007. Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell. 129(3):605–616. doi:https://doi.org/10.1016/j.cell.2007.02.047
   PubMed Web of Science ®Google Scholar
• Luurtsema G, Molthoff CFM, Schuit RC, Windhorst AD, Lammertsma AA, Franssen EJF. 2005. Evaluation of (R)-[11C]verapamil as PET tracer of P-glycoprotein function in the blood-brain barrier: kinetics and metabolism in the rat. Nucl Med Biol. 32(1):87–93. doi:https://doi.org/10.1016/j.nucmedbio.2004.06.007
   PubMed Web of Science ®Google Scholar
• May A, Leone M, Afra J, Linde M, Sándor PS, Evers S, Goadsby PJ. 2006. EFNS guidelines on the treatment of cluster headache and other trigeminal-autonomic cephalalgias. Eur J Neurol. 13(10):1066–1077. doi:https://doi.org/10.1111/j.1468-1331.2006.01566.x
   PubMed Web of Science ®Google Scholar
• May A, Bahra A, Büchel C, Frackowiak RSJ, Goadsby PJ. 1998. Hypothalamic activation in cluster headache attacks. Lancet. 352(9124):275–278. doi:https://doi.org/10.1016/S0140-6736(98)02470-2
   PubMed Web of Science ®Google Scholar
• May A, Schwedt TJ, Magis D, Pozo-rosich P, Evers S. 2018. Cluster headache. Nat Rev Dis Prim. 4:1–17. doi:https://doi.org/10.1038/nrdp.2018.6
   PubMed Web of Science ®Google Scholar
• McAllister RG, Kirsten EB. 1982. The pharmacology of verapamil. IV. Kinetic and dynamic effects after single intravenous and oral doses. Clin Pharmacol Ther. 31(4):418–426. doi:https://doi.org/10.1038/clpt.1982.54
   PubMed Web of Science ®Google Scholar
• McGeeney BE. 2018. Cluster Headache and Other Trigeminal Autonomic Cephalalgias. Semin Neurol. 38(6):603–607. doi:https://doi.org/10.1055/s-0038-1673682
   PubMed Web of Science ®Google Scholar
• Meneses-Santos D, Buonfiglio D. 2018. Chronic treatment with dexamethasone alters clock gene expression and melatonin synthesis in rat pineal gland at night. Nat Sci Sleep. 10:203–215. https://doi.org/10.2147/NSS.S158602
   PubMed Web of Science ®Google Scholar
• Moore RY, Eichler VB. 1972. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res. 42(1):201–206. doi:https://doi.org/10.1016/0006-8993(72)90054-6
   PubMed Web of Science ®Google Scholar
• Morris SA, Weiss LM, Factor S, Bilezikian JP, Tanowitz H, Wittner M. 1989. Verapamil ameliorates clinical, pathologic and biochemical manifestations of experimental chagasic cardiomyopathy in mice. J Am Coll Cardiol. 14(3):782–789. doi:https://doi.org/10.1016/0735-1097(89)90126-5
   PubMed Web of Science ®Google Scholar
• Naegel S, Holle D, Desmarattes N, Theysohn N, Diener H-C-C, Katsarava Z, Obermann M. 2014. Cortical plasticity in episodic and chronic cluster headache. NeuroImage Clin. 6:415–423. doi:https://doi.org/10.1016/j.nicl.2014.10.003
   PubMed Web of Science ®Google Scholar
• Nahm SS, Farnell YZ, Griffith W, Earnest DJ. 2005. Circadian regulation and function of voltage-dependent calcium channels in the suprachiasmatic nucleus. J Neurosci. 25(40):9304–9308. doi:https://doi.org/10.1523/JNEUROSCI.2733-05.2005
   PubMed Web of Science ®Google Scholar
• Nohara K, Kim E, Wirianto M, Mileykovskaya E, Dowhan W, Chen Z, Yoo SH. 2020. Cardiolipin Synthesis in Skeletal Muscle Is Rhythmic and Modifiable by Age and Diet. Oxid Med Cell Longev. doi:https://doi.org/10.1155/2020/5304768
   Google Scholar
• Nohara K, Mallampalli V, Nemkov T, Wirianto M, Yang J, Ye Y, Sun Y, Han L, Esser KA, Mileykovskaya E, et al. 2019. Nobiletin fortifies mitochondrial respiration in skeletal muscle to promote healthy aging against metabolic challenge. Nat Commun. 10(1):1–15. doi:https://doi.org/10.1038/s41467-019-11926-y
   PubMedGoogle Scholar
• Patke A, Murphy PJ, Onat OE, Krieger AC, Özçelik T, Campbell SS, Young MW. 2017. Mutation of the human circadian clock Gene CRY1 in familial delayed sleep phase disorder. Cell. 169(2):203–215.e13. doi:https://doi.org/10.1016/j.cell.2017.03.027
   PubMed Web of Science ®Google Scholar
• PDR L 2020. verapamil hydrochloride - Drug Summary. PDR: Prescribers’ Digital Reference. https://www.pdr.net/drug-summary/Verelan-verapamil-hydrochloride-960.2852
   Google Scholar
• Percie Du Sert N, Hurst V, Ahluwalia A, Alam S, MT A, Baker M, WJ B, Clark A, IC C, Dirnagl U, et al. 2020. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biol. 18(7):e3000410. doi:https://doi.org/10.1371/journal.pbio.3000410
   PubMed Web of Science ®Google Scholar
• Petersen AS, Barloese MCJJ, Snoer A, Soerensen AMS, Jensen RH. 2019. Verapamil and cluster headache: still a mystery. Narrative Rev Efficacy Mech Perspect. 59:8. doi:https://doi.org/10.1111/head.13603
   Google Scholar
• Portaluppi F, Smolensky MH, Touitou Y. 2010. Ethics and methods for biological rhythm research on animals and human beings. Chronobiol Int. 27(9–10):1911–1929. doi:https://doi.org/10.3109/07420528.2010.516381
   PubMed Web of Science ®Google Scholar
• Ralph MR, Foster RG, Davis FC, Menaker M. 1990. Transplanted suprachiasmatic nucleus determines circadian period. Science. 247(4945):975–978. doi:https://doi.org/10.1126/science.2305266
   PubMed Web of Science ®Google Scholar
• Römermann K, Wanek T, Bankstahl M, Bankstahl JP, Fedrowitz M, Müller M, Löscher W, Kuntner C, Langer O. 2013. (R)-[11C]verapamil is selectively transported by murine and human P-glycoprotein at the blood-brain barrier, and not by MRP1 and BCRP. Nucl Med Biol. 40(7):873–878. doi:https://doi.org/10.1016/j.nucmedbio.2013.05.012
   PubMed Web of Science ®Google Scholar
• Rozen TD, Fishman RS. 2012. Cluster headache in the United States of America: demographics, clinical characteristics, triggers, suicidality, and personal burden. Headache. 52(1):99–113. doi:https://doi.org/10.1111/j.1526-4610.2011.02028.x
   PubMed Web of Science ®Google Scholar
• Steinberg A, Fourier C, Ran C, Waldenlind E, Sjöstrand C, Belin AC. 2018. Cluster headache – clinical pattern and a new severity scale in a Swedish cohort. 38. 7:1286–1295. doi:https://doi.org/10.1177/0333102417731773
   Google Scholar
• Stephan FK, Zucker I. 1972. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci U S A. 69(6):1583–1586. doi:https://doi.org/10.1073/pnas.69.6.1583
   PubMed Web of Science ®Google Scholar
• Tamai TK, Nakane Y, Ota W, Kobayashi A, Ishiguro M, Kadofusa N, Ikegami K, Yagita K, Shigeyoshi Y, Sudo M, et al. 2018. Identification of circadian clock modulators from existing drugs. EMBO Mol Med. 10(5):e8724. doi:https://doi.org/10.15252/emmm.201708724
   PubMed Web of Science ®Google Scholar
• Teepker M, Menzler K, Belke M, Heverhagen JT, Voelker M, Mylius V, Oertel WH, Rosenow F, Knake S. 2012. Diffusion tensor imaging in episodic cluster headache. Headache. 52(2):274–282. doi:https://doi.org/10.1111/j.1526-4610.2011.02000.x
   PubMed Web of Science ®Google Scholar
• Tfelt-Hansen P, Tfelt-Hansen J. 2009. Verapamil for cluster headache. Clinical pharmacology and possible mode of action. Headache J Head Face Pain. 49(1):117–125. doi:https://doi.org/10.1111/j.1526-4610.2008.01298.x
   PubMed Web of Science ®Google Scholar
• Trejo-Gabriel-Galan JM, Aicua-Rapún I, Cubo-Delgado E, Velasco-Bernal C. 2018. Suicide in primary headaches in 48 countries: a physician-survey based study. Cephalalgia. 38(4):798–803. doi:https://doi.org/10.1177/0333102417714477.
   Google Scholar
• Waldenlind E, Gustafsson SA, Ekbom K, Wetterberg L. 1987. Circadian secretion of cortisol and melatonin in cluster headache during active cluster periods and remission. J Neurol Neurosurg Psychiatry. 50(2):207–213. doi:https://doi.org/10.1136/jnnp.50.2.207
   PubMed Web of Science ®Google Scholar
• Yang F-C-C, Chou K-H-H, Fuh J-L-L, Lee P-L-L, Lirng J-F-F, Lin -Y-Y-Y, Lin C-P-P, Wang S-J-J. 2015. Altered hypothalamic functional connectivity in cluster headache: a longitudinal resting-state functional MRI study. J Neurol Neurosurg Psychiatry. 86(4):437–445. doi:https://doi.org/10.1136/jnnp-2014-308122
   PubMed Web of Science ®Google Scholar
• Yin L, Wang J, Klein PS, Lazar MA. 2006. Nuclear receptor Rev-erbα is a critical lithium-sensitive component of the circadian clock. Science. 311(5763):1002–1005. doi:https://doi.org/10.1126/science.1121613
   PubMed Web of Science ®Google Scholar
• Yoo S-H, Kojima S, Shimomura K, Koike N, Buhr ED, Furukawa T, Ko CH, Gloston G, Ayoub C, Nohara K, et al. 2017. Period2 3′-UTR and microRNA-24 regulate circadian rhythms by repressing PERIOD2 protein accumulation. Proc Natl Acad Sci. 114(42):E8855–E8864. doi:https://doi.org/10.1073/pnas.1706611114
   PubMed Web of Science ®Google Scholar
• Yoo S-H, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong H-KH-K, Oh WJ, Yoo OJ, et al. 2004. PERIOD2::LUCIFERASEreal-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A. 101(15):5339–5346. doi:https://doi.org/10.1073/pnas.0308709101
   PubMed Web of Science ®Google Scholar