Functional crosstalk in culture between macrophages and trigeminal sensory neurons of a mouse genetic model of migraine

BMC Neuroscience

Volumn 13, Issue 1, 2012, Pages

  Franceschini, Alessia ^a,d   Nair, Asha ^a   Bele, Tanja ^c   van den Maagdenberg, Arn M J M ^b   Nistri, Andrea ^a   Fabbretti, Elsa ^a,c  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF NOVA GORICA   (Slovenia)

^d UNIVERSITY OF FERRARA   (Italy)

Author keywords

ATP; Neuroinflammation; P2X3 receptor; Pain; Purinergic receptor; Sensitization

Indexed keywords

PURINERGIC P2X3 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; EXPERIMENTAL MODEL; FAMILIAL HEMIPLEGIC MIGRAINE; GENE EXPRESSION; GENE MUTATION; GENETIC MODEL; MACROPHAGE; MIGRAINE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; SENSORY NERVE CELL; TRIGEMINUS GANGLION; WILD TYPE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; CALCIUM CHANNELS, L-TYPE; CALCIUM-BINDING PROTEINS; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; MACROPHAGES; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MUTATION; PATCH-CLAMP TECHNIQUES; PHAGOCYTOSIS; RECEPTORS, PURINERGIC P2X3; SENSORY RECEPTOR CELLS; TRIGEMINAL GANGLION; TUBULIN;

EID: 84869207413     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-13-143     Document Type: Article

References (35)

1. van den Maagdenberg AMJM, Haan J, Terwindt GM, Ferrari MD. Migraine: gene mutations and functional consequences. Curr Opin Neurol 2007, 20:299-305. 10.1097/WCO.0b013e3281338d1f, 17495624.
2. May A. New insights into headache: an update on functional and structural imaging findings. Nat Rev Neurol 2009, 5:199-209. 10.1038/nrneurol.2009.28, 19347025.
3. Ophoff RA, Terwindt GM, Vergouwe MN, van Eijk R, Oefner PJ, Hoffman SMG, Lamerdin JE, Mohrenweiser HW, Bulman DE, Ferrari M, Haan J, Lindhout D, van Ommen GB, Hofker MH, Ferrari MD, Frants RR. Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell 1996, 87:543-552. 10.1016/S0092-8674(00)81373-2, 8898206.
4. van den Maagdenberg AM, Pietrobon D, Pizzorusso T, Kaja S, Broos LA, Cesetti T, van de Ven RC, Tottene A, van der Kaa J, Plomp JJ, Frants RR, Ferrari MD. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41:701-710. 10.1016/S0896-6273(04)00085-6, 15003170.
5. Tottene A, Fellin T, Pagnutti S, Luvisetto S, Striessnig J, Fletcher C, Pietrobon D. Familial hemiplegic migraine mutations increase Ca2+ influx through single human CaV2.1 channels and decrease maximal CaV2.1 current density in neurons. Proc Natl Acad Sci USA 2002, 99:13284-13289. 10.1073/pnas.192242399, 130625, 12235360.
6. van den Maagdenberg AMJM, Pizzorusso T, Kaja S, Terpolilli N, Shapovalova M, Hoebeek FE, Barrett CF, Gherardini L, van de Ven RCG, Todorov B, Broos LAM, Tottene A, Gao Z, Fodor M, De Zeeuw CI, Frants RR, Plesnila N, Plomp JJ, Pietrobon D, Ferrari MD. High cortical spreading depression susceptibility and migraine-associated symptoms in CaV2.1 S218L mice. Ann Neurol 2010, 67:85-98. 10.1002/ana.21815, 20186955.
7. Tottene A, Conti R, Fabbro A, Vecchia D, Shapovalova M, Santello M, van den Maagdenberg AM, Ferrari MD, Pietrobon D. Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron 2009, 61:762-773. 10.1016/j.neuron.2009.01.027, 19285472.
8. Lauritzen M. Pathophysiology of the migraine aura. The spreading depression theory. Brain 1994, 117:199-210. 10.1093/brain/117.1.199, 7908596.
9. Nair A, Simonetti M, Birsa N, Ferrari MD, van den Maagdenberg AM, Giniatullin R, Nistri A, Fabbretti E. Familial hemiplegic migraine CaV2.1 channel mutation R192Q enhances ATP-gated P2X3 receptor activity of mouse sensory ganglion neurons mediating trigeminal pain. Mol Pain 2010, 6:48. 10.1186/1744-8069-6-48, 2940876, 20735819.
10. Giniatullin R, Nistri A, Fabbretti E. Molecular mechanisms of sensitization of pain-transducing P2X3 receptors by the migraine mediators CGRP and NGF. Mol Neurobiol 2008, 37:83-90. 10.1007/s12035-008-8020-5, 18459072.
11. Ceruti S, Villa G, Fumagalli M, Colombo L, Magni G, Zanardelli M, Fabbretti E, Verderio C, van den Maagdenberg AMJM, Nistri A, Abbracchio MP. Calcitonin gene-related peptide-mediated enhancement of purinergic neuron/glia communication by the algogenic factor bradykinin in mouse trigeminal ganglia from wild-type and R192Q CaV2.1 knock-in mice: implications for basic mechanisms of migraine pain. J Neurosci 2011, 31:3638-3649. 10.1523/JNEUROSCI.6440-10.2011, 21389219.
12. Moskowitz MA. Basic mechanisms in vascular headache. Neurol Clin 1990, 8:801-815.
13. Moskowitz MA. Neurogenic inflammation in the pathophysiology and treatment of migraine. Neurology 1993, 43(Suppl 3):S16-S20.
14. Hamed SA. The vascular risk associations with migraine: Relation to migraine susceptibility and progression. Atherosclerosis 2009, 205:15-22. 10.1016/j.atherosclerosis.2008.10.016, 19054516.
15. Pietrobon D, Striessnig J. Neurobiology of migraine. Nat Rev Neurosci 2003, 4:386-398. 10.1038/nrn1102, 12728266.
16. David S, Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 2011, 12:388-399. 10.1038/nrn3053, 21673720.
17. Simonetti M, Fabbro A, D'Arco M, Zweyer M, Nistri A, Giniatullin R, Fabbretti E. Comparison of P2X and TRPV1 receptors in ganglia or primary culture of trigeminal neurons and their modulation by NGF or serotonin. Mol Pain 2006, 2:11. 10.1186/1744-8069-2-11, 1448213, 16566843.
18. Ray A, Dittel BN. Isolation of Mouse Peritoneal Cavity Cells. J Vis Exp 2010, 35:1488. 3152216, 20110936.
19. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S. A novel gene Iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 1996, 224:855-862. 10.1006/bbrc.1996.1112, 8713135.
20. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 1998, 57:1-9.
21. Harrigan TJ, Abdullaev IF, Jourd'heuil D, Mongin AA. Activation of microglia with zymosan promotes excitatory amino acid release via volume-regulated anion channels: the role of NADPH oxidases. J Neurochem 2008, 106:2449-2462. 10.1111/j.1471-4159.2008.05553.x, 2574595, 18624925.
22. Färber K, Cheung G, Mitchell D, Wallis R, Weihe E, Schwaeble W, Kettenmann H. C1q, the recognition subcomponent of the classical pathway of complement, drives microglial activation. J Neurosci Res 2009, 87:644-652. 10.1002/jnr.21875, 2635544, 18831010.
23. D'Arco M, Giniatullin R, Simonetti M, Fabbro A, Nair A, Nistri A, Fabbretti E. Neutralization of nerve growth factor induces plasticity of ATP-sensitive P2X3 receptors of nociceptive trigeminal ganglion neurons. J Neurosci 2007, 27:8190-8201. 10.1523/JNEUROSCI.0713-07.2007, 17670966.
24. Etheredge JA, Murchison D, Abbott LC, Griffith WH. Functional compensation by other voltage-gated Ca2+ channels in mouse basal forebrain neurons with CaV2.1 mutations. Brain Res 2007, 1140:105-119.
25. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments. Clin Chem 2009, 2009(55):611-622.
26. Seifert S, Pannell M, Uckert W, Färber K, Kettenmann H. Transmitter- and hormoneactivated Ca2+ responses in adult microglia/brain macrophages in situ recorded after viral transduction of a recombinant Ca2+ sensor. Cell Calcium 2011, 49:365-375. 10.1016/j.ceca.2011.03.005, 21536328.
27. Villa G, Ceruti S, Zanardelli M, Magni G, Jasmin L, Ohara PT, Abbracchio MP. Temporomandibular joint inflammation activates glial and immune cells in both the trigeminal ganglia and in the spinal trigeminal nucleus. Mol Pain 2010, 6:89. 10.1186/1744-8069-6-89, 3017032, 21143950.
28. Fabbretti E, Nistri A. Regulation of P2X3 Receptor Structure and Function. CNS Neurol Disord Drug Targets 2012, Epub ahead of print.
29. Franceschini A, Hullugundi SK, van den Maagdenberg AM, Nistri A, Fabbretti E. Effects of LPS on P2X3 receptors of trigeminal sensory neurons and macrophages from mice expressing the R192Q Cacna1a gene mutation of familial hemiplegic migraine-1. Purinergic Signal 2012, Epub ahead of print.
30. Waeber C, Moskowitz MA. Migraine as an inflammatory disorder. Neurology 2005, 64(Suppl 2):S9-15.
31. Pietrobon D. CaV2.1 channelopathies. Pflugers Arch 2010, 460:375-393. 10.1007/s00424-010-0802-8, 20204399.
32. Burnstock G. Purinergic receptors and pain. Curr Pharm Des 2009, 15:1717-1735. 10.2174/138161209788186335, 19442186.
33. Sokolova E, Skorinkin A, Moiseev I, Agrachev A, Nistri A, Giniatullin R. Experimental and modeling studies of desensitization of P2X3 receptors. Mol Pharmacol 2006, 70:373-382.
34. Raddant AC, Russo AF. Calcitonin gene-related peptide in migraine: intersection of peripheral inflammation and central modulation. Expert Rev Mol Med. 2011, 13:e36. 3383830, 22123247.
35. Inoue K. The function of microglia through purinergic receptors: neuropathic pain and cytokine release. Pharmacol Ther 2006, 109:210-226. 10.1016/j.pharmthera.2005.07.001, 16169595.