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The Journal of Headache and Pain

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Open Access 01-12-2013 | Research article

Phospholipase C activity increases in cerebrospinal fluid from migraineurs in proportion to the number of comorbid conditions: a case–control study

Authors: Alfred N Fonteh, Janice M Pogoda, Rainbow Chung, Robert P Cowan, Michael G Harrington

Published in: The Journal of Headache and Pain | Issue 1/2013

Abstract

Background

Migraineurs are more often afflicted by comorbid conditions than those without primary headache disorders, though the linking pathophysiological mechanism(s) is not known. We previously reported that phosphatidylcholine-specific phospholipase C (PC-PLC) activity in cerebrospinal fluid (CSF) increased during migraine compared to the same individual’s well state. Here, we examined whether PC-PLC activity from a larger group of well-state migraineurs is related to the number of their migraine comorbidities.

Methods

In a case–control study, migraineurs were diagnosed using International Headache Society criteria, and controls had no primary headache disorder or family history of migraine. Medication use, migraine frequency, and physician-diagnosed comorbidities were recorded for all participants. Lumbar CSF was collected between the hours of 1 and 5 pm, examined immediately for cells and total protein, and stored at −80°C. PC-PLC activity in thawed CSF was measured using a fluorometric enzyme assay. Multivariable logistic regression was used to evaluate age, gender, medication use, migraine frequency, personality scores, and comorbidities as potential predictors of PC-PLC activity in CSF.

Results

A total of 18 migraineurs-without-aura and 17 controls participated. In a multivariable analysis, only the number of comorbidities was related to PC-PLC activity in CSF, and only in migraineurs [parameter estimate (standard error) = 1.77, p = 0.009].

Conclusion

PC-PLC activity in CSF increases with increasing number of comorbidities in migraine-without-aura. These data support involvement of a common lipid signaling pathway in migraine and in the comorbid conditions.

Scher AI, Bigal ME, Lipton RB: Comorbidity of migraine. Curr Opin Neurol 2005,18(3):305–310. 10.1097/01.wco.0000169750.52406.a2PubMedCrossRef

Vos T, Flaxman AD, Naghavi M, Lozano R, Michaud C, Ezzati M, Shibuya K, Salomon JA, Abdalla S, Aboyans V, Abraham J, Ackerman I, Aggarwal R, Ahn SY, Ali MK, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Bahalim AN, Barker-Collo S, Barrero LH, Bartels DH, Basanez MG, Baxter A, Bell ML, Benjamin EJ, Bennett D, et al.: Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012,380(9859):2163–2196. 10.1016/S0140-6736(12)61729-2PubMedCrossRef

Cologno D, Buzzi MG, Carlesimo GA, Cicinelli P, Costa A, Fadda L, Formisano R, Marconi B, Pero S, Caltagirone C: Psychiatric disorders and pain location in unilateral migraineurs. J Headache Pain 2005,6(4):227–230. 10.1007/s10194-005-0192-zPubMedCentralPubMedCrossRef

Glover V, Jarman J, Sandler M: Migraine and depression: biological aspects. J Psychiatr Res 1993,27(2):223–231. 10.1016/0022-3956(93)90010-YPubMedCrossRef

Silberstein SD, Lipton RB, Breslau N: Migraine: association with personality characteristics and psychopathology. Cephalalgia 1995,15(5):358–369. discussion 336PubMedCrossRef

Wauquier A: Is there a common pharmacological link between migraine and epilepsy? Funct Neurol 1986,1(4):515–520.PubMed

Chu CH, Liu CJ, Fuh JL, Shiao AS, Chen TJ, Wang SJ: Migraine is a risk factor for sudden sensorineural hearing loss: a nationwide population-based study. Cephalalgia 2013,33(2):80–86. 10.1177/0333102412468671PubMedCrossRef

Schurks M, Winter AC, Berger K, Buring JE, Kurth T: Migraine and restless legs syndrome in women. Cephalalgia 2012,32(5):382–389. 10.1177/0333102412439355PubMedCentralPubMedCrossRef

Winawer MR, Connors R: Evidence for a shared genetic susceptibility to migraine and epilepsy. Epilepsia 2013,54(2):288–295. 10.1111/epi.12072PubMedCentralPubMedCrossRef

10.

Harrington MG, Fonteh AN, Arakaki X, Cowan RP, Ecke LE, Foster H, Huhmer AF, Biringer RG: Capillary endothelial Na(+), K(+), ATPase transporter homeostasis and a new theory for migraine pathophysiology. Headache 2010,50(3):459–478. 10.1111/j.1526-4610.2009.01551.xPubMedCrossRef

11.

Schytz HW, Holst H, Arendt-Nielsen L, Olesen J, Ashina M: Cutaneous nociception and neurogenic inflammation evoked by PACAP38 and VIP. J Headache Pain 2010,11(4):309–316. 10.1007/s10194-010-0214-3PubMedCentralPubMedCrossRef

12.

Tassorelli C, Greco R, Armentero MT, Blandini F, Sandrini G, Nappi G: A role for brain cyclooxygenase-2 and prostaglandin-E2 in migraine: effects of nitroglycerin. Int Rev Neurobiol 2007, 82: 373–382.PubMedCrossRef

13.

Cui Y, Kataoka Y, Li QH, Yokoyama C, Yamagata A, Mochizuki-Oda N, Watanabe J, Yamada H, Watanabe Y: Targeted tissue oxidation in the cerebral cortex induces local prolonged depolarization and cortical spreading depression in the rat brain. Biochem Biophys Res Commun 2003,300(3):631–636. 10.1016/S0006-291X(02)02906-6PubMedCrossRef

14.

Welch SP: Interaction of the cannabinoid and opioid systems in the modulation of nociception. Int Rev Psychiatry (Abingdon, England) 2009,21(2):143–151. 10.1080/09540260902782794CrossRef

15.

Sugiura T: Physiological roles of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand. Biofactors 2009,35(1):88–97. 10.1002/biof.18PubMedCrossRef

16.

Marino E, Fanny B, Lorenzi C, Pirovano A, Franchini L, Colombo C, Bramanti P, Smeraldi E: Genetic bases of comorbidity between mood disorders and migraine: possible role of serotonin transporter gene. Neurol Sci 2009,31(3):387–391.PubMedCrossRef

17.

Burr RL, Jarrett ME, Cain KC, Jun SE, Heitkemper MM: Catecholamine and cortisol levels during sleep in women with irritable bowel syndrome. Neurogastroenterol Motil 2009,21(11):1148-e1197. 10.1111/j.1365-2982.2009.01351.xPubMedCentralPubMedCrossRef

18.

Martinez F, Castillo J, Pardo J, Lema M, Noya M: Catecholamine levels in plasma and CSF in migraine. J Neurol Neurosurg Psychiatry 1993,56(10):1119–1121. 10.1136/jnnp.56.10.1119PubMedCentralPubMedCrossRef

19.

Peterlin BL, Katsnelson MJ, Calhoun AH: The associations between migraine, unipolar psychiatric comorbidities, and stress-related disorders and the role of estrogen. Curr Pain Headache Rep 2009,13(5):404–412. 10.1007/s11916-009-0066-1PubMedCentralPubMedCrossRef

20.

Aviello G, Romano B, Izzo AA: Cannabinoids and gastrointestinal motility: animal and human studies. Eur Rev Med Pharmacol Sci 2008,12(Suppl 1):81–93.PubMed

21.

Russo EB: Clinical endocannabinoid deficiency (CECD): can this concept explain therapeutic benefits of cannabis in migraine, fibromyalgia, irritable bowel syndrome and other treatment-resistant conditions? Neuro Endocrinol Lett 2004,25(1–2):31–39.PubMed

22.

Ferrari A, Spaccapelo L, Pinetti D, Tacchi R, Bertolini A: Effective prophylactic treatments of migraine lower plasma glutamate levels. Cephalalgia 2009,29(4):423–429. 10.1111/j.1468-2982.2008.01749.xPubMedCrossRef

23.

Amilhon B, Lepicard E, Renoir T, Mongeau R, Popa D, Poirel O, Miot S, Gras C, Gardier AM, Gallego J, Hamon M, Lanfumey L, Gasnier B, Giros B: El Mestikawy S VGLUT3 (vesicular glutamate transporter type 3) contribution to the regulation of serotonergic transmission and anxiety. J Neurosci 2010,30(6):2198–2210. 10.1523/JNEUROSCI.5196-09.2010PubMedCrossRef

24.

Goadsby PJ, Sprenger T: Current practice and future directions in the prevention and acute management of migraine. Lancet Neurol 2010,9(3):285–298. 10.1016/S1474-4422(10)70005-3PubMedCrossRef

25.

Culpepper L: Generalized anxiety disorder and medical illness. J Clin Psychiatry 2009,70(Suppl 2):20–24. 10.4088/JCP.s.7002.04PubMedCrossRef

26.

Akundi RS, Candelario-Jalil E, Hess S, Hull M, Lieb K, Gebicke-Haerter PJ, Fiebich BL: Signal transduction pathways regulating cyclooxygenase-2 in lipopolysaccharide-activated primary rat microglia. Glia 2005,51(3):199–208. 10.1002/glia.20198PubMedCrossRef

27.

Ceruti S, Fumagalli M, Villa G, Verderio C, Abbracchio MP: Purinoceptor-mediated calcium signaling in primary neuron-glia trigeminal cultures. Cell Calcium 2008,43(6):576–590. 10.1016/j.ceca.2007.10.003PubMedCrossRef

28.

Li Y, Maher P, Schubert D: Phosphatidylcholine-specific phospholipase C regulates glutamate-induced nerve cell death. Proc Natl Acad Sci USA 1998,95(13):7748–7753. 10.1073/pnas.95.13.7748PubMedCentralPubMedCrossRef

29.

Baun M, Pedersen MH, Olesen J, Jansen-Olesen I: Dural mast cell degranulation is a putative mechanism for headache induced by PACAP-38. Cephalalgia 2012,32(4):337–345. 10.1177/0333102412439354PubMedCrossRef

30.

Govorunova EG, Moussaif M, Kullyev A, Nguyen KC, McDonald TV, Hall DH, Sze JY: A homolog of FHM2 is involved in modulation of excitatory neurotransmission by serotonin in C. elegans. PLoS One 2010,5(4):e10368. 10.1371/journal.pone.0010368PubMedCentralPubMedCrossRef

31.

Kim J, Nakajima K, Oomura Y, Wayner MJ, Sasaki K: Orexin-A and ghrelin depolarize the same pedunculopontine tegmental neurons in rats: an in vitro study. Peptides 2009,30(7):1328–1335. 10.1016/j.peptides.2009.03.015PubMedCrossRef

32.

Luconi R, Bartolini M, Taffi R, Vignini A, Mazzanti L, Provinciali L, Silvestrini M: Prognostic significance of personality profiles in patients with chronic migraine. Headache 2007,47(8):1118–1124. 10.1111/j.1526-4610.2007.00807.xPubMedCrossRef

33.

Steer RA, Ball R, Ranieri WF, Beck AT: Further evidence for the construct validity of the Beck depression Inventory-II with psychiatric outpatients. Psychol Rep 1997,80(2):443–446. 10.2466/pr0.1997.80.2.443PubMedCrossRef

34.

Bursac Z, Gauss CH, Williams DK, Hosmer DW: Purposeful selection of variables in logistic regression. Source Code Biol Med 2008, 3: 17. 10.1186/1751-0473-3-17PubMedCentralPubMedCrossRef

35.

Peterlin BL, Rapoport AM, Kurth T: Migraine and Obesity: Epidemiology, Mechanisms, and Implications. Headache 2009, 50: 631–648.PubMedCentralPubMedCrossRef

36.

D'Andrea G, D'Arrigo A, Dalle Carbonare M, Leon A: Pathogenesis of migraine: role of neuromodulators. Headache 2012,52(7):1155–1163. 10.1111/j.1526-4610.2012.02168.xPubMedCrossRef

37.

Moskowitz MA: Genes, proteases, cortical spreading depression and migraine: impact on pathophysiology and treatment. Funct Neurol 2007,22(3):133–136.PubMed

38.

Lin CC, Lee IT, Wu WB, Liu CJ, Hsieh HL, Hsiao LD, Yang CC, Yang CM: Thrombin Mediates Migration of Rat Brain Astrocytes via PLC, Ca, CaMKII, PKCalpha, and AP-1-Dependent Matrix Metalloproteinase-9 Expression. Mol Neurobiol 2013. 10.1007/s12035-013-8450-6

39.

Suzuki K, Saito SY, Ishikawa T: Involvement of phosphatidylcholine-specific phospholipase C in thromboxane A(2) receptor-mediated extracellular Ca(2)(+) influx in rat aorta. Eur J Pharmacol 2012,677(1–3):123–130. 10.1016/j.ejphar.2011.12.005PubMedCrossRef

40.

Phillips R, Ursell T, Wiggins P, Sens P: Emerging roles for lipids in shaping membrane-protein function. Nature 2009,459(7245):379–385. 10.1038/nature08147PubMedCentralPubMedCrossRef

41.

Li H, Zhang L, Yin D, Zhang Y, Miao J: Targeting phosphatidylcholine-specific phospholipase C for atherogenesis therapy. Trends Cardiovasc Med 2010,20(5):172–176. 10.1016/j.tcm.2011.02.002PubMedCrossRef

Title: Phospholipase C activity increases in cerebrospinal fluid from migraineurs in proportion to the number of comorbid conditions: a case–control study
Authors: Alfred N Fonteh
Janice M Pogoda
Rainbow Chung
Robert P Cowan
Michael G Harrington
Publication date: 01-12-2013
Publisher: Springer Milan
Published in: The Journal of Headache and Pain / Issue 1/2013
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI: https://doi.org/10.1186/1129-2377-14-60

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Phospholipase C activity increases in cerebrospinal fluid from migraineurs in proportion to the number of comorbid conditions: a case–control study

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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