Skip to main content

Role of Calcium in Regulating Primary Sensory Neuronal Excitability

  • Chapter
  • First Online:
Sensory Nerves

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 194))

Abstract

The fundamental role of calcium ions (Ca2+) in an excitable tissue, the frog heart, was first demonstrated in a series of classical reports by Sydney Ringer in the latter part of the nineteenth century (1882a, b; 1893a, b). Even so, nearly a century elapsed before it was proven that Ca2+ regulated the excitability of primary sensory neurons. In this chapter we review the sites and mechanisms whereby internal and external Ca2+ can directly or indirectly alter the excitability of primary sensory neurons: excitability changes being manifested typically by variations in shape of the action potential or the pattern of its discharge.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 429.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 549.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 549.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adelman JP, Shen KZ, Kavanaugh MP, Warren RA, Wu YN, Lagrutta A, Bond CT, North RA (1992) Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron 9(2):209–216

    Article  PubMed  CAS  Google Scholar 

  • Atkinson NS, Robertson GA, Ganetzky B (1992) A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science 253:551–555

    Article  Google Scholar 

  • Ayar A, Storer C, Tatham EL, Scott RH (1999) The effects of changing intracellular Ca2+ buffering on the excitability of cultured dorsal root ganglion neurones. Neurosci Lett 271(3): 171–174

    Article  PubMed  CAS  Google Scholar 

  • Bader CR, Bertrand D, Schlichter R (1987) Calcium-activated chloride current in cultured sensory and parasympathetic quail neurones. J Physiol 394:125–148

    PubMed  CAS  Google Scholar 

  • Baimbridge K, Celio M, Rogers J (1992) Calcium-binding proteins in the nervous system. Trends Neuroscience 15:303–308

    Article  CAS  Google Scholar 

  • Belmonte C, Gallego R (1983) Membrane properties of cat sensory neurones with chemoreceptor and baroreceptor endings. J Physiol 342:603–614

    PubMed  CAS  Google Scholar 

  • Bird MM, Lieberman AR (1976) Microtubule fascicles in the stem processes of cultured sensory ganglion cells. Cell Tissue Res 169(1):41–47

    Article  PubMed  CAS  Google Scholar 

  • Blackshaw S, Sawa A, Sharp AH, Ross CA, Snyder SH, Khan AA (2000) Type 3 inositol 1,4,5-trisphosphate receptor modulates cell death. FASEB J 14(10):1375–1379

    Article  PubMed  CAS  Google Scholar 

  • Boehmerle W, Splittgerber U, Lazarus MB, McKenzie KM, Johnston DG, Austin DJ, Ehrlich BE (2006) Paclitaxel induces calcium oscillations via an inositol 1,4,5-trisphosphate receptor and neuronal calcium sensor 1-dependent mechanism. Proc Natl Acad Sci USA 103(48):18356–18361

    Article  PubMed  CAS  Google Scholar 

  • Bond CT, Herson PS, Strassmaier T, Hammond R, Stackman R, Maylie J, Adelman JP (2004) Small conductance Ca2+-activated K+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci 24(23):5301–5306

    Article  PubMed  CAS  Google Scholar 

  • Boulton AJ, Knight G, Drury J, Ward JD (1985) The prevalence of symptomatic, diabetic neuropathy in an insulin-treated population. Diabetes Care 8(2):125–128

    Article  PubMed  CAS  Google Scholar 

  • Carafoli E (1991) The calcium pumping ATPase of the plasma membrane. Annu Rev Physiol 53:531–547

    Article  PubMed  CAS  Google Scholar 

  • Catterall WA, Striessnig J, Snutch TP, Perez-Reyes E (2005) International Union of Pharmacology. XL. Compendium of voltage-gated ion channels: calcium channels. Pharmacol Rev 55(4): 579–581

    Google Scholar 

  • Chard PS, Bleakman D, Christakos S, Fullmer CS, Miller RJ (1993) Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J Physiol 472:341–357

    PubMed  CAS  Google Scholar 

  • Christian EP, Taylor GE, Weinreich D (1989) Serotonin increaes excitability of rabbit C-fiber neurons by two distinct mechanisms. J Applied Physiol 67:584–591

    CAS  Google Scholar 

  • Christian EP, Togo J, Naper KE (1994) Guinea pig visceral C-fiber neurons are diverse with respect to the K+ currents involved in action-potential repolarization. J Neurophysiol 71(2): 561–574

    PubMed  CAS  Google Scholar 

  • Cohen AC, Moore KA, Bangalore R, Jafri MS, Weinreich D, Kao JPY (1997) Ca2+-induced Ca2+ release mediates Ca2+ transients evoked by single action potentials in rabbit vagal afferents. J Physiol 499:315–328

    PubMed  CAS  Google Scholar 

  • Conigrave AD, Quinn SJ, Brown EM (2000) Cooperative multi-modal sensing and therapeutic implications of the extracellular Ca2+ sensing receptor. Trends Pharmacol Sci 10:401–407

    Article  Google Scholar 

  • Cordoba-Rodriguez R, Moore KA, Kao JP, Weinreich D (1999) Calcium regulation of a slow post-spike hyperpolarization in vagal afferent neurons. Proc Natl Acad Sci USA 96(14):7650–7657

    Article  PubMed  CAS  Google Scholar 

  • Crawford JH, Wootton JF, Seabrook GR, Scott RH (1997) Activation of Ca2+-dependent currents in dorsal root ganglion neurons by metabotropic glutamate receptors and cyclic ADP-ribose precursors. J Neurophysiol 77(5):2573–2584

    PubMed  CAS  Google Scholar 

  • Currie KPM, Scott RH (1992) Calcium-activated currents in cultured neurones from rat dorsal root ganglia. Br J Pharmacol 106:593–602

    PubMed  CAS  Google Scholar 

  • Dean WL, Chen D, Brandt PC, Vanaman TC (1997) Regulation of platelet plasma membrane Ca2+-ATPase by cAMP-dependent and tyrosine phosphorylation. J Biol Chem 272(24):15113–15119

    Article  PubMed  CAS  Google Scholar 

  • Dent MA, Raisman G, Lai FA (1996) Expression of type 1 inositol 1,4,5-trisphosphate receptor during axogenesis and synaptic contact in the central and peripheral nervous system of developing rat. Development 122(3):1029–1039

    PubMed  CAS  Google Scholar 

  • Deschenes M, Feltz P, Lamour Y (1976) A model for the estimate of the ionic basis of presynaptic inhibition: an intracellular analysis of the GABA induced depolarization in rat dorsal root ganglia. Brain Res 18:486–493

    Article  Google Scholar 

  • Devor M, Jänig W, Michaelis M (1994) Modulation of activity in dorsal root ganglion neurons by sympathetic activation in nerve-injured rats. J Neurophysiol 71(1):38–47

    PubMed  CAS  Google Scholar 

  • Duchen MR (1990) Effects of metabolic inhibition on the membrane properties of isolated mouse primary sensory neurones. J Physiol 424:387–409

    PubMed  CAS  Google Scholar 

  • Ertel EA, Campbell KP, Harpold MM, Hofmann F, Mori Y, Perez-Reyes E, Schwartz A, Snutch TP, Tanabe T, Birnbaumer L et al (2000) Nomenclature of voltage gatedcalcium channels Neuron 25:533–535

    Article  PubMed  CAS  Google Scholar 

  • Faber ES, Sah P (2003) Ca2+-activated K+ (BK) channel inactivation contributes to spike broadening during repetitive firing in the rat lateral amygdala. J Physiol 552(2):483–497

    Article  PubMed  CAS  Google Scholar 

  • Flatters SJ, Bennett GJ (2004) Ethosuximide reverses paclitaxel- and vincristine-induced painful peripheral neuropathy. Pain 109(1-2):150–161

    Article  PubMed  CAS  Google Scholar 

  • Fowler JC, Greene R, Weinreich D (1985) Two calcium-sensitive spike after-hyperpolarizations in visceral sensory neurones of the rabbit. J Physiol (Lond) 365:59–75

    CAS  Google Scholar 

  • Fox AJ, Barnes PJ, Venkatesan P, Belvisi MG (1997) Activation of large conductance potassium channels inhibits the afferent and efferent function of airway sensory nerves in the guinea pig. J Clin Invest 99:513–519

    Article  PubMed  CAS  Google Scholar 

  • Frings S, Reuter D, Kleene SJ (2000) Neuronal Ca2+-activated Cl− channels – homing in on an elusive channel species. Prog Neurobiol 60(3):247–289

    Article  PubMed  CAS  Google Scholar 

  • Fuchs A, Rigaud M, Sarantopoulos CD, Filip P, Hogan QH (2007) Contribution of calcium channel subtypes to the intracellular calcium signal in sensory neurons: the effect of injury. Anesthesiology 107(1):117–127

    Article  PubMed  CAS  Google Scholar 

  • Gallagher JP, Higashi H, Nishi I (1978) Characterization and ionic basis of GABA-induced depolarizations recorded in vitro from cat primary afferent neurons. J Physiol 275:263–282

    PubMed  CAS  Google Scholar 

  • Gallego R, Eyzaguirre C (1978) Membrane and action potential characteristics of A and C nodose ganglion cells studied in whole ganglia and in tissue slices. J Neurophysiol 41(5):1217–1232

    PubMed  CAS  Google Scholar 

  • Gold MS, Shuster MJ, Levine JD (1996) Role of a Ca2+-dependent slow afterhyperpolarization in prostaglandin E2-induced sensitization of cultured rat sensory neurons. Neurosci Lett 205(3):161–164

    Article  PubMed  CAS  Google Scholar 

  • Gover TD, Moreira TH, Kao JP, Weinreich D (2007a) Calcium homeostasis in trigeminal ganglion cell bodies. Cell Calcium 41(4):389–396

    Article  PubMed  CAS  Google Scholar 

  • Gover TD, Moreira TH, Kao JP, Weinreich D (2007b) Calcium regulation in individual peripheral sensory nerve terminals of the rat. J Physiol 578(Pt 2):481–490

    PubMed  CAS  Google Scholar 

  • Gover TD, Kao JP, Weinreich D (2003). Calcium signaling in single peripheral sensory nerve terminals. J Neurosci 23;4793–4797

    PubMed  CAS  Google Scholar 

  • Hablitz JJ, Heinemann U, Lux HD Step reductions in extracellular Ca2+ activate a transient inward current in chick dorsal root ganglion cells. Biophys J 50:753–757

    Google Scholar 

  • Hay M, Kunze DL (1994) An intermediate conductance calcium-activated potassium channel in rat visceral sensory afferent neurons. Neurosci Lett 167(1–2):179–182

    Article  PubMed  CAS  Google Scholar 

  • Hartzell C, Putzier I, Arreola J (2005). Calcium-activated chloride channels. Ann Rev Physiol 67: 719–758

    Article  CAS  Google Scholar 

  • Hille B (2001) Ion channels of excitable membranes, 3d edn. Sinauer, Sunderland, MA

    Google Scholar 

  • Hoesch RE, Yienger K, Weinreich D, Kao JP (2002) Coexistence of functional IP(3) and ryanodine receptors in vagal sensory neurons and their activation by ATP. J Neurophysiol 88(3):1212–1219

    PubMed  CAS  Google Scholar 

  • Honda CN (1995) Differential distribution of calbindin-D28K and parvalbumin in somatic and visceral sensory neurons. Neuro Science 68(3):883–892

    CAS  Google Scholar 

  • Hoesch RE, Weinreich D, Kao JP (2004) Localized IP3-evoked Ca2+ release activates a K+ current in primary vagal sensory neurons. J Neurophysiol 91(5):2344–2352

    Article  PubMed  CAS  Google Scholar 

  • Ishii TM, Silvia C, Hirschberg B, Bond CT, Adelman JP (1997) A human intermediate conductance calcium-activated potassium channel. Proc Natl Acad Sci USA 94:11651–11656

    Article  PubMed  CAS  Google Scholar 

  • Jafri MS, Moore KA, Taylor GE, Weinreich D (1997) Histamine H1 receptor activation blocks two classes of potassium current, IK(rest) and IAHP, to excite ferret vagal afferents. J Physiol 503.3:533–546

    Article  Google Scholar 

  • Jagodic MM, Pathirathna S, Nelson MT, Mancuso S, Joksovic PM, Rosenberg ER, Bayliss DA, Jevtovic-Todorovic V, Todorovic SM (2007) Cell-specific alterations of T-type calcium current in painful diabetic neuropathy enhance excitability of sensory neurons. J Neurosci 27(12):3305–3316

    Article  PubMed  CAS  Google Scholar 

  • Kostyuk E, Pronchuk N, Shmigol A (1995) Calcium signal prolongation in sensory neurones of mice with experimental diabetes. Neuroreport 6(7):1010–1012

    Article  PubMed  CAS  Google Scholar 

  • Kostyuk E, Svichar N, Shishkin V, Kostyuk P (1999) Role of mitochondrial dysfunction in calcium signalling alterations in dorsal root ganglion neurons of mice with experimentally-induced diabetes. Neuroscience 90(2):535–541

    Article  PubMed  CAS  Google Scholar 

  • Kruglikov I, Gryshchenko O, Shutov L, Kostyuk E, Kostyuk P, Voitenko N (2004) Diabetes-induced abnormalities in ER calcium mobilization in primary and secondary nociceptive neurons. Pflugers Arch 448(4):395–401

    Article  PubMed  CAS  Google Scholar 

  • Lancaster E, Oh EJ, Weinreich D (2001) Vagotomy decreases excitability in primary vagal afferent somata. J Neurophysiol 85:247–253

    PubMed  CAS  Google Scholar 

  • Lancaster E, Oh EJ, Gover T, Weinreich D (2002) Calcium and calcium-activated currents in vagotomized rat primary vagal afferent neurons. J Physiol 540(Pt 2):543–556

    Article  PubMed  CAS  Google Scholar 

  • Lee M-G, Kollarik M, Chaychoo B, Undem BJ (2004) Ionoteropic and metabotropic receptor mediated airway sensory nerve activation. Pulm Pharmacol Ther 17:355–360

    Article  PubMed  CAS  Google Scholar 

  • Li W, Gao SB, Lv CX, Wu Y, Guo ZH, Ding JP, Xu T (2007) Characterization of voltage- and Ca2+-activated K+ channels in rat dorsal root ganglion neurons. J Cell Physiol 212(2): 348–357

    Article  PubMed  CAS  Google Scholar 

  • Lokuta AJ, Komai H, McDowell TS, Valdivia HH (2002) Functional properties of ryanodine receptors from rat dorsal root ganglia. FEBS Lett 511(1–3):90–96

    Article  PubMed  CAS  Google Scholar 

  • Marrion NV, Tavalin SJ (1998) Selective activation of Ca2+-activated K+ channels by co-localized Ca2+ channels in hippocampal neurons. Nature 395(6705):900–905

    Article  PubMed  CAS  Google Scholar 

  • Matsuda Y, Yoshida S, Yonezawa T (1976) A Ca-dependent regenerative response in rodent dorsal root ganglion cells cultured in vitro. Brain Res 115(2):334–338

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto M, Inoue M, Hald A, Xie W, Ueda H (2006) Inhibition of paclitaxel-induced A-fiber hypersensitization by gabapentin. J Pharmacol Exp Ther 318(2):735–740

    Article  PubMed  CAS  Google Scholar 

  • Mayer ML (1985) A calcium-activated chloride current generates the afterdepolarization of rat sensory neurones in culture. J Physiol 364:217–239

    PubMed  CAS  Google Scholar 

  • McCallum JB, Kwok WM, Sapunar D, Fuchs A, Hogan QH (2006) Painful peripheral nerve injury decreases calcium current in axotomized sensory neurons. Anesthesiology 105(1):160–168

    Article  PubMed  CAS  Google Scholar 

  • McGuirk SM, Dolphin AC (1992) G-protein mediation in nociceptive signal transduction: an investigation into the excitatory action of bradykinin in a subpopulation of cultured rat sensory neurons. Neuroscience 49(1):117–128

    Article  PubMed  CAS  Google Scholar 

  • McPherson PS, Campbell KP (1993) The ryanodine receptor/Ca2+ release channel. J Biol Chem 268(19):13765–13768

    PubMed  CAS  Google Scholar 

  • Mielke S, Sparreboom A, Mross K (2006) Peripheral neuropathy: a persisting challenge in paclitaxel-based regimes. Eur J Cancer 42(1):24–30

    Article  PubMed  CAS  Google Scholar 

  • Mikoshiba K (2007) The IP3 receptor/Ca2+ channel and its cellular function. Biochem Soc Symp 74:9–22

    Article  PubMed  CAS  Google Scholar 

  • Mongan LC, Hill MJ, Chen MX, Tate SN, Collins SD, Buckby L, Grubb BD (2005) The distribution of small and intermediate conductance calcium-activated potassium channels in the rat sensory nervous system. Neuroscience 131(1):161–175

    Article  PubMed  CAS  Google Scholar 

  • Moore KA, Cohen AS, Kao JP, Weinreich D (1998) Ca2+-induced Ca2+ release mediates a slow post-spike hyperpolarization in rabbit vagal afferent neurons. J Neurophysiol 79(2):688–694

    PubMed  CAS  Google Scholar 

  • Neylon CB, Nurgali K, Hunne B, Robbins HL, Moore S, Chen MX, Furness JB (2004) Intermediate-conductance calcium-activated potassium channels in enteric neurones of the mouse: pharmacological, molecular and immunochemical evidence for their role in mediating the slow afterhyperpolarization. J Neurochem 90(6):1414–1422

    Article  PubMed  CAS  Google Scholar 

  • Nordin M, Nyström B, Wallin U, Hagbarth KE (1984) Ectopic sensory discharges and paresthesiae in patients with disorders of peripheral nerves, dorsal roots and dorsal columns. Pain 20(3): 231–245

    Article  PubMed  CAS  Google Scholar 

  • Ogura H, Tachibana T, Yamanaka H, Kobayashi K, Obata K, Dai Y, Yoshiya S, Noguchi K (2007) Axotomy increases plasma membrane Ca2+ pump isoform4 in primary afferent neurons. Neuroreport 18(1):17–22

    Article  PubMed  CAS  Google Scholar 

  • Oh EJ, Weinreich D (2004) Bradykinin decreases K+ and increases Cl− conductances in vagal afferent neurones of the guinea pig. J Physiol 558(Pt 2):513–526

    Article  PubMed  CAS  Google Scholar 

  • Ooashi N, Futatsugi A, Yoshihara F, Mikoshiba K, Kamiguchi H (2005) Cell adhesion molecules regulate Ca2+-mediated steering of growth cones via cyclic AMP and ryanodine receptor type 3. J Cell Biol 170(7):1159–1167

    Article  PubMed  CAS  Google Scholar 

  • Philipson KD, Nicoll DA (2000) Sodium-calcium exchange: a molecular perspective. Annu Rev Physiol 62:111–133

    Article  PubMed  CAS  Google Scholar 

  • Polomano RC, Mannes AJ, Clark US, Bennett GJ (2001) A painful peripheral neuropathy in the rat produced by the chemotherapeutic drug, paclitaxel. Pain 94(3):293–304

    Article  PubMed  CAS  Google Scholar 

  • Pottorf WJ, Thayer SA (2002) Transient rise in intracellular calcium produces a long-lasting increasein plasma membrane calcium pump activity in rat sensory neurons. J Neurochem 83(4):1002–1008

    Article  PubMed  CAS  Google Scholar 

  • Ransom BR, Holz RW (1977) Ionic determinants of excitability in cultured mouse dorsal root ganglion and spinal cord cells. Brain Res 136(3):445–453

    Article  PubMed  CAS  Google Scholar 

  • Ringer S,(1882a) Regarding the Action of Hydrate of Soda, Hydrate of Ammonia, and Hydrate of Postash on the Ventricle of the Frog's Heart. J Physiol 3:195–202

    PubMed  CAS  Google Scholar 

  • Ringer S,(1882b) Concerning the Influence exerted by each of the Constituents of the Blood on the Contraction of the Ventricle. J Physiol 3:380–393

    PubMed  CAS  Google Scholar 

  • Ringer S,(1883a) A further Contribution regarding the influence of the different Constituents of the Blood on the Contraction of the Heart. J Physiol 3:29–42

    Google Scholar 

  • Ringer S,(1883b) A third contribution regarding the Influence of the Inorganic Constituents of the Blood on the Ventricular Contraction. J Physiol 3:222–225

    Google Scholar 

  • Sah P, Faber ES (2002) Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 66(5):345–353

    Article  PubMed  CAS  Google Scholar 

  • Salkoff L, Butler A, Ferreira G, Santi C, Wei A (2006) High-conductance potassium channels of the SLO family. Nat Rev Neurosci 7(12):921–931

    Article  PubMed  CAS  Google Scholar 

  • Schlichter R, Bader CR, Bertrand D, Dubois-Dauphin M, Bernheim L (1989) Expression of substance P and of a Ca2+-activated C1– current in quail sensory trigeminal neurons. Neuroscience 30:585–594

    Article  PubMed  CAS  Google Scholar 

  • Scott RH, McGuir SM, Dolphin AC (1988) Modulation of divalent cation-activated chloride ion currents. Br J Pharmacol 94:653–662

    PubMed  CAS  Google Scholar 

  • Scott RH, Sutton KG, Griffin A, Stapleton SR, Currie KP (1995) Aspects of calcium-activated chloride currents: a neuronal perspective. Pharmacol Ther 66:535–565

    Article  PubMed  CAS  Google Scholar 

  • Scroggs RS, Fox AP (1992) Multiple Ca2+ currents elicited by action potential waveforms in acutely isolated adult rat dorsal root ganglion neurons. J Neurosci 12(5):1789–1801

    PubMed  CAS  Google Scholar 

  • Shah M, Haylett DG (2000) Ca2+ channels involved in the generation of the slow afterhyperpolarization in cultured rat hippocampal pyramidal neurons. J Neurophysiol 83(5):2554–2561

    PubMed  CAS  Google Scholar 

  • Shishkin V, Potapenko E, Kostyuk E, Girnyk O, Voitenko N, Kostyuk P (2002) Role of mitochondria in intracellular calcium signaling in primary and secondary sensory neurons of rats. Cell Calcium 32:121–130

    Article  PubMed  CAS  Google Scholar 

  • Shmigol A, Verkhratsky A, Isenberg G (1995) Calcium-induced calcium release in rat sensory neurons. J Physiol 489 (Pt 3):627–636

    PubMed  CAS  Google Scholar 

  • Siau C, Xiao W, Bennett GJ (2006) Paclitaxel- and vincristine-evoked painful peripheral neuropathies: loss of epidermal innervation and activation of Langerhans cells. Exp Neurol 201(2):507–514

    Article  PubMed  CAS  Google Scholar 

  • Sung KW, Kirby M, McDonald MP, Lovinger DM, Delpire E (2000) Abnormal GABAA receptor-mediated currents in dorsal root ganglion neurones isolated from Na-K-2CL cotransporter null mice. J Neurosci 20:7531–7538

    Google Scholar 

  • Svichar N, Kostyuk P, Verkhratsky A (1997) Mitochondria buffer Ca2+ entry but not intracellular Ca2+ release in mouse DRG neurones. Neuroreport 8(18):3929–3932

    Article  PubMed  CAS  Google Scholar 

  • Svichar N, Shishkin V, Kostyuk E, Voitenko N (1998) Changes in mitochondrial Ca2+ homeostasis in primary sensory neurons of diabetic mice. Neuroreport 9(6):1121–1125

    Article  PubMed  CAS  Google Scholar 

  • Thayer SA, Miller RJ (1990) Regulation of the intracellular free calcium concentration in single rat dorsal root ganglion neurons in vitro. J Physiol (Lond) 425:85–115

    CAS  Google Scholar 

  • Thayer SA, Perney TM, Miller RJ (1988) Regulation of calcium homeostasis in sensory neurons by bradykinin. J Neurosci 11:4089–4097

    Google Scholar 

  • Thayer SA, Usachev YM, Pottorf WJ (2002) Modulating Ca2+ clearance from neurons. Front Biosci 7:d1255–d1279

    Article  PubMed  CAS  Google Scholar 

  • Undem BJ, Hubbard W, Weinreich D (1993) Immunologically-induced neuromodulation of guinea pig nodose ganglion neurons. J Auton Nerv Syst 44:35–44

    Article  PubMed  CAS  Google Scholar 

  • Undem BJ, Oh EO, Lancaster E, Weinreich D (2002) Effect of extracellular calcium on excitability of guinea pig airway vagal afferent nerves. J Neurophysiol 89:1196–1204

    Article  Google Scholar 

  • Undem BJ, Oh EJ, Lancaster E, Weinreich D (2003) Effect of extracellular calcium on excitability of guinea pig airway vagal afferent nerves. J Neurophysiol 89:1196–1204

    Google Scholar 

  • Usachev YM, DeMarco SJ, Campbell C, Strehler EE, Thayer SA (2002) Bradykinin and ATP accelerates Ca2+ efflux from rat sensory neurons via protein kinase C and the plasma membrane Ca2+ pump isoform 4. Neuron 33:113–122

    Article  PubMed  CAS  Google Scholar 

  • Usachev YM, Marsh AJ, Johanns TM, Lemke MM, Thayer SA (2006) Activation of protein kinase C in sensory neurons accelerates Ca2+ uptake into the endoplasmic reticulum. J Neurosci 26(1):311–318

    Article  PubMed  CAS  Google Scholar 

  • Verdru P, De Greef C, Mertens L, Carmeliet E, Callewaert G (1997) Na+–Ca2+ exchange in rat dorsal root ganglion neurons. J Neurophysiol 77:484–490

    PubMed  CAS  Google Scholar 

  • Vogalis F, Storm JF, Lancaster B (2003) SK channels and the varieties of slow after-hyperpolarizations in neurons. Eur J Neurosci 18:3155–3166

    Article  PubMed  Google Scholar 

  • Wächtler J, Mayer C, Grafe P (1998) Activity-dependent intracellular Ca2+ transients in unmyelinated nerve fibres of the isolated adult rat vagus nerve. Pflűgers Arch 435:678–686

    Article  PubMed  Google Scholar 

  • Wang MS, Davis AA, Culver DG, Wang Q, Powers JC, Glass JD (2004) Calpain inhibition protects against Taxol-induced sensory neuropathy. Brain 127(Pt 3):671–679

    PubMed  Google Scholar 

  • Weinreich D, Wonderlin WF (1987) Inhibition of calcium-dependent spike after-hyperpolarization increases excitability of rabbit visceral sensory neurones. J Physiol 394:415–427

    PubMed  CAS  Google Scholar 

  • Werth JL, Thayer SA (1994) Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons. J Neurosci 14:348–356

    PubMed  CAS  Google Scholar 

  • Werth JL, Usachev YM, Thayer SA (1996) Modulation of calcium efflux from cultured rat dorsal root ganglion neurons. J Neurosci 16(3):1008–1015

    PubMed  CAS  Google Scholar 

  • Wiernik PH, Schwartz EL, Strauman JJ, Dutcher JP, Lipton RB, Paietta E (1987) Phase I clinical and pharmacokinetic study of taxol. Cancer Res 47(9):2486–2493

    PubMed  CAS  Google Scholar 

  • Wuytack F, Raeymaekers L, Missiaen L (2002) Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 32(5–6):279–305

    Article  PubMed  CAS  Google Scholar 

  • Xiao W, Boroujerdi A, Bennett GJ, Luo ZD (2007) Chemotherapy-evoked painful peripheral neuropathy: analgesic effects of gabapentin and effects on expression of the alpha-2-delta type-1 calcium channel subunit. Neuroscience 144(2):714–720

    Article  PubMed  CAS  Google Scholar 

  • Xu A, Hawkins C, Narayanan N (1993) Phosphorylation and activation of the Ca2+-pumping ATPase of cardiac sarcoplasmic reticulum by Ca2+/calmodulin-dependent protein kinase. J Biol Chem 268(12):8394–8397

    Google Scholar 

  • Yusaf SP, Goodman J, Gonzalez IM, Bramwell S, Pinnock RD, Dixon AK, Lee K (2001) Streptozocin-induced neuropathy is associated with altered expression of voltage-gated calcium channel subunit mRNAs in rat dorsal root ganglion neurones. Biochem Biophys Res Commun 289(2):402–406

    Article  PubMed  CAS  Google Scholar 

  • Zhang XF, Gopalakrishnan M, Shieh CC (2003) Modulation of action potential firing by iberiotoxin and NS1619 in rat dorsal root ganglion neurons. Neuroscience 122, 1003–1011

    Article  PubMed  CAS  Google Scholar 

  • Zylinska L, Guerini D, Gromadzinska E, Lachowicz L (1998) Protein kinases A and C phosphorylate purified Ca2+-ATPase from rat cortex, cerebellum and hippocampus. Biochim Biophys Acta 1448(1):99–108

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Jessica Swartz for her valuable input to this work and for her critique of an earlier version of this manuscript. This work was supported by NIH grants NS22069 (D.W.) and ST32-NS007375 (T.D.G.).

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Gover, T., Moreira, T., Weinreich, D. (2009). Role of Calcium in Regulating Primary Sensory Neuronal Excitability. In: Canning, B., Spina, D. (eds) Sensory Nerves. Handbook of Experimental Pharmacology, vol 194. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-79090-7_16

Download citation

Publish with us

Policies and ethics