Skip to main content

Ion Channel Assessment

  • Protocol
  • First Online:
Animal Models of Acute Neurological Injuries II

Part of the book series: Springer Protocols Handbooks ((SPH))

  • 1452 Accesses

Abstract

Molecular mechanisms underlying subarachnoid hemorrhage (SAH)-induced cerebral vasospasm are complex and still partially unknown. Molecular-biological studies and clinical trials support a central role of ion channels, but further detailed studies have to evaluate their exact role during vasospasm following SAH.

This chapter focuses on methods and principles of ion channel assessment which includes the wide-spread spectrum of molecular-biological, electrophysiological, immunochemical, and functional methods.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

  1. Tani E, Matsumoto T (2004) Continuous elevation of intracellular Ca2+ is essential for the development of cerebral vasospasm. Curr Vasc Pharmacol 2(1):13–21

    Article  PubMed  CAS  Google Scholar 

  2. Jewell RP, Saundry CM, Bonev AD, Tranmer BI, Wellman GC (2004) Inhibition of Ca++ sparks by oxyhemoglobin in rabbit cerebral arteries. J Neurosurg 100(2):295–302

    Article  PubMed  CAS  Google Scholar 

  3. Wickman G, Lan C, Vollrath B (2003) Functional roles of the rho/rho kinase pathway and protein kinase C in the regulation of cerebrovascular constriction mediated by hemoglobin: relevance to subarachnoid hemorrhage and vasospasm. Circ Res 92(7):809–816

    Article  PubMed  CAS  Google Scholar 

  4. Ishiguro M, Morielli AD, Zvarova K, Tranmer BI, Penar PL, Wellman GC (2006) Oxyhemoglobin-induced suppression of voltage-dependent K+ channels in cerebral arteries by enhanced tyrosine kinase activity. Circ Res 99(11): 1252–1260

    Article  PubMed  CAS  Google Scholar 

  5. Jahromi BS, Aihara Y, Ai J, Zhang ZD, Weyer G, Nikitina E et al (2008) Temporal profile of potassium channel dysfunction in cerebrovascular smooth muscle after experimental subarachnoid haemorrhage. Neurosci Lett 440(1): 81–86

    Article  PubMed  CAS  Google Scholar 

  6. Ko EA, Han J, Jung ID, Park WS (2008) Physiological roles of K+ channels in vascular smooth muscle cells. J Smooth Muscle Res 44(2):65–81

    Article  PubMed  Google Scholar 

  7. Hagiwara S, Ozawa S, Sand O (1975) Voltage clamp analysis of two inward current mechanisms in the egg cell membrane of a starfish. J Gen Physiol 65(5):617–644

    Article  PubMed  CAS  Google Scholar 

  8. Hagiwara S (1975) Ca-dependent action potential. Membranes 3:359–381

    PubMed  CAS  Google Scholar 

  9. Hagiwara S, Byerly L (1981) Calcium channel. Annu Rev Neurosci 4:69–125

    Article  PubMed  CAS  Google Scholar 

  10. Perez-Reyes E, Cribbs LL, Daud A, Lacerda AE, Barclay J, Williamson MP et al (1998) Molecular characterization of a neuronal low voltage-activated T-type calcium channel. Nature 391: 896–900

    Article  PubMed  CAS  Google Scholar 

  11. Cribbs LL, Lee J-H, Yang J, Satin J, Zhang Y, Daud A et al (1998) Cloning and characterization of α1H from human heart, a member of the T-type calcium channel gene family. Circ Res 83:103–109

    Article  PubMed  CAS  Google Scholar 

  12. Lee JH, Daud AN, Cribbs LL, Lacerda AE, Pereverzev A, Klöckner U et al (1999) Cloning and expression of a novel member of the low voltage-activated T-type calcium channel family. J Neurosci 19:1912–1921

    PubMed  CAS  Google Scholar 

  13. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83(1):117–161

    PubMed  CAS  Google Scholar 

  14. Lin CL, Calisaneller T, Ukita N, Dumont AS, Kassell NF, Lee KS (2003) A murine model of subarachnoid hemorrhage-induced cerebral vasospasm. J Neurosci Methods 123(1):89–97

    Article  PubMed  Google Scholar 

  15. Meguro T, Clower BR, Carpenter R, Parent AD, Zhang JH (2001) Improved rat model for cerebral vasospasm studies. Neurol Res 23(7):761–766

    Article  PubMed  CAS  Google Scholar 

  16. Cahill J, Calvert JW, Solaroglu I, Zhang JH (2006) Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 37(7):1868–1874

    Article  PubMed  Google Scholar 

  17. Yin W, Tibbs R, Aoki K, Badr A, Zhang J (2002) Metabolic alterations in cerebrospinal fluid from double hemorrhage model of dogs. Acta Neurochir Suppl 81:257–263

    PubMed  CAS  Google Scholar 

  18. Parra A, McGirt MJ, Sheng H, Laskowitz DT, Pearlstein RD, Warner DS (2002) Mouse model of subarachnoid hemorrhage associated cerebral vasospasm: methodological analysis. Neurol Res 24(5):510–516

    Article  PubMed  Google Scholar 

  19. Aihara Y, Jahromi BS, Yassari R, Nikitina E, Agbaje-Williams M, Macdonald RL (2004) Molecular profile of vascular ion channels after experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab 24(1):75–83

    Article  PubMed  CAS  Google Scholar 

  20. Ishiguro M, Murakami K, Link T, Zvarova K, Tranmer BI, Morielli AD et al (2008) Acute and chronic effects of oxyhemoglobin on voltage-dependent ion channels in cerebral arteries. Acta Neurochir Suppl 104:99–102

    Article  PubMed  CAS  Google Scholar 

  21. Amberg GC, Santana LF (2006) Kv2 channels oppose myogenic constriction of rat cerebral arteries. Am J Physiol Cell Physiol 291(2):C348–C356

    Article  PubMed  CAS  Google Scholar 

  22. Albarwani S, Nemetz LT, Madden JA, Tobin AA, England SK, Pratt PF et al (2003) Voltage-gated K+ channels in rat small cerebral arteries: molecular identity of the functional channels. J Physiol 551(Pt 3):751–763

    Article  PubMed  CAS  Google Scholar 

  23. Ploug KB, Sorensen MA, Strobech L, Klaerke DA, Hay-Schmidt A, Sheykhzade M et al (2008) K ATP channels in pig and human intracranial arteries. Eur J Pharmacol 601(1–3): 43–49

    Article  PubMed  CAS  Google Scholar 

  24. Rosenblum WI (2003) ATP-sensitive potassium channels in the cerebral circulation. Stroke 34(6):1547–1552

    Article  PubMed  CAS  Google Scholar 

  25. Wulf H, Hay-Schmidt A, Poulsen AN, Klaerke DA, Olesen J, Jansen-Olesen I (2008) Molecular studies of BKCa channels in intracranial arteries: presence and localization. Cell Tissue Res 334(3):359–369

    Article  PubMed  CAS  Google Scholar 

  26. Chrissobolis S, Ziogas J, Chu Y, Faraci FM, Sobey CG (2000) Role of inwardly rectifying K(+) channels in K(+)-induced cerebral vasodilatation in vivo. Am J Physiol Heart Circ Physiol 279(6):H2704–H2712

    PubMed  CAS  Google Scholar 

  27. Nikitina E, Zhang ZD, Kawashima A, Jahromi BS, Bouryi VA, Takahashi M et al (2007) Voltage-dependent calcium channels of dog basilar artery. J Physiol 580(Pt. 2):523–541

    PubMed  CAS  Google Scholar 

  28. Navarro-Gonzalez MF, Grayson TH, Meaney KR, Cribbs LL, Hill CE (2009) Non-L-type voltage-dependent calcium channels control vascular tone of the rat basilar artery. Clin Exp Pharmacol Physiol 36(1):55–66

    Article  PubMed  CAS  Google Scholar 

  29. Jahromi BS, Aihara Y, Ai J, Zhang ZD, Weyer G, Nikitina E et al (2008) Preserved BK channel function in vasospastic myocytes from a dog model of subarachnoid hemorrhage. J Vasc Res 45(5):402–415

    Article  PubMed  CAS  Google Scholar 

  30. Quan L, Sobey CG (2000) Selective effects of subarachnoid hemorrhage on cerebral vascular responses to 4-aminopyridine in rats. Stroke 31(10):2460–2465

    Article  PubMed  CAS  Google Scholar 

  31. Weyer GW, Jahromi BS, Aihara Y, Agbaje-Williams M, Nikitina E, Zhang ZD et al (2006) Expression and function of inwardly rectifying potassium channels after experimental subarachnoid hemorrhage. J Cereb Blood Flow Metab 26(3):382–391

    Article  PubMed  CAS  Google Scholar 

  32. Ishiguro M, Wellman TL, Honda A, Russell SR, Tranmer BI, Wellman GC (2005) Emergence of a R-type Ca2+ channel (CaV 2.3) contributes to cerebral artery constriction after subarachnoid hemorrhage. Circ Res 96(4): 419–426

    Article  PubMed  CAS  Google Scholar 

  33. Link TE, Murakami K, Beem-Miller M, Tranmer BI, Wellman GC (2008) Oxyhemoglobin-induced expression of R-type Ca2+ channels in cerebral arteries. Stroke 39(7):2122–2128

    Article  PubMed  CAS  Google Scholar 

  34. Iwasaki S, Momiyama A, Uchitel OD, Takahashi T (2000) Developmental changes in calcium channel types mediating central synaptic transmission. J Neurosci 20(1):59–65

    PubMed  CAS  Google Scholar 

  35. Fedchyshyn MJ, Wang LY (2005) Developmental transformation of the release modality at the calyx of Held synapse. J Neurosci 25(16):4131–4140

    Article  PubMed  CAS  Google Scholar 

  36. Urbano FJ, Piedras-Renteria E, Jun K, Shin H-S, Uchitel OD (2003) Altered properties of quantal neurotransmitter release at endplates of mice lacking P/Q-type Ca2+ channels. PNAS 100:3491–3496

    Article  PubMed  CAS  Google Scholar 

  37. Pagani R, Song M, McEnery M, Qin N, Tsien RW, Toro L et al (2004) Differential expression of alpha 1 and beta subunits of voltage dependent Ca2+ channel at the neuromuscular junction of normal and P/Q Ca2+ channel knockout mouse. Neuroscience 123(1):75–85

    Article  PubMed  CAS  Google Scholar 

  38. Pinto A, Moss F, Lang B, Boot J, Brust P, Williams M et al (1998) Differential effect of Lambert-Eaton myasthenic syndrome immunoglobulin on cloned neuronal voltage-gated calcium channels. Ann N Y Acad Sci 841:687–690

    Article  PubMed  CAS  Google Scholar 

  39. Giovannini F, Sher E, Webster R, Boot J, Lang B (2002) Calcium channel subtypes contributing to acetylcholine release from normal, 4-aminopyridine-treated and myasthenic syndrome auto-antibodies-affected neuromuscular junctions. Br J Pharmacol 136(8):1135–1145

    Article  PubMed  CAS  Google Scholar 

  40. Tanaka Y, Ando S (2001) Age-related changes in the subtypes of voltage-dependent calcium channels in rat brain cortical synapses. Neurosci Res 39(2):213–220

    Article  PubMed  CAS  Google Scholar 

  41. Lin MT, Hessinger DA, Pearce WJ, Longo LD (2003) Developmental differences in Ca2+-activated K+ channel activity in ovine basilar artery. Am J Physiol Heart Circ Physiol 285(2):H701–H709

    PubMed  CAS  Google Scholar 

  42. Bowles DK, Heaps CL, Turk JR, Maddali KK, Price EM (2004) Hypercholesterolemia inhibits L-type calcium current in coronary macro-, not microcirculation. J Appl Physiol 96(6): 2240–2248

    Article  PubMed  CAS  Google Scholar 

  43. Martini A, Bruno R, Mazzulla S, Nocita A, Martino G (2009) Angiotensin II regulates endothelial cell migration through calcium influx via T-type calcium channel in human umbilical vein endothelial cells. Acta Physiol (Oxf) 198(4):449–455. Epub 2009 Dec 18

    Google Scholar 

  44. Wang D, Yan B, Rajapaksha WR, Fisher TE (2009) The expression of voltage-gated Ca2+ channels in pituicytes and the up-regulation of L-type Ca2+ channels during water deprivation. J Neuroendocrinol 21(10):858–866

    Article  PubMed  CAS  Google Scholar 

  45. Yokoyama K, Kurihara T, Makita K, Tanabe T (2003) Plastic change of N-type Ca channel expression after preconditioning is responsible for prostaglandin E2-induced long-lasting allodynia. Anesthesiology 99(6):1364–1370

    Article  PubMed  CAS  Google Scholar 

  46. Meguro T, Klett CP, Chen B, Parent AD, Zhang JH (2000) Role of calcium channels in oxyhemoglobin-induced apoptosis in endothelial cells. J Neurosurg 93(4):640–646

    Article  PubMed  CAS  Google Scholar 

  47. Yip S, Sastry BR (2000) Effects of hemoglobin and its breakdown products on synaptic transmission in rat hippocampal CA1 neurons. Brain Res 864(1):1–12

    Article  PubMed  CAS  Google Scholar 

  48. Nystoriak MA, Murakami K, Penar PL, Wellman GC (2009) Ca(v)1.2 splice variant with exon 9* is critical for regulation of cerebral artery diameter. Am J Physiol Heart Circ Physiol 297(5):H1820–H1828

    Article  PubMed  CAS  Google Scholar 

  49. Sehba FA, Flores R, Muller A, Friedrich V, Chen JF, Britz GW et al (2009) Adenosine A(2A) receptors in early ischemic vascular injury after subarachnoid hemorrhage. J Neurosurg 113(4):826–834

    Google Scholar 

  50. Matsui T, Sugawa M, Johshita H, Takuwa Y, Asano T (1991) Activation of the protein kinase C-mediated contractile system in canine basilar artery undergoing chronic vasospasm. Stroke 22(9):1183–1187

    Article  PubMed  CAS  Google Scholar 

  51. Obara K, Nishizawa S, Koide M, Nozawa K, Mitate A, Ishikawa T et al (2005) Interactive role of protein kinase C-delta with rho-kinase in the development of cerebral vasospasm in a canine two-hemorrhage model. J Vasc Res 42(1):67–76

    Article  PubMed  CAS  Google Scholar 

  52. Nishizawa S, Obara K, Nakayamal K, Koide M, Yokoyama T, Yokota N et al (2000) Protein kinase cdelta and alpha are involved in the development of vasospasm after subarachnoid hemorrhage. Eur J Pharmacol 398(1):113–119

    Article  PubMed  CAS  Google Scholar 

  53. Nishizawa S, Obara K, Koide M, Nakayama K, Ohta S, Yokoyama T (2003) Attenuation of canine cerebral vasospasm after subarachnoid hemorrhage by protein kinase C inhibitors despite augmented phosphorylation of myosin light chain. J Vasc Res 40(2):169–178

    Article  PubMed  CAS  Google Scholar 

  54. Ansar S, Edvinsson L (2008) Subtype activation and interaction of protein kinase C and mitogen-activated protein kinase controlling receptor expression in cerebral arteries and microvessels after subarachnoid hemorrhage. Stroke 39(1):185–190

    Article  PubMed  CAS  Google Scholar 

  55. Sakaki S, Ohue S, Kohno K, Takeda S (1989) Impairement of vascular reactivity and changes in intracellular calcium and calmodulin levels of smooth muscle cells in canine basilar arteries after subarachnoid hemorrhage. Neurosurgery 25(5):753–761

    Article  PubMed  CAS  Google Scholar 

  56. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  57. Flockerzi V, Oeken HJ, Hofmann F (1986) Purification of a functional receptor for calcium-channel blockers from rabbit skeletal-muscle microsomes. Eur J Biochem 161:217–224

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

We want to thank Prof. Toni Schneider for his constant support (Institute of Neurophysiology, University of Cologne, Germany).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Hänggi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Kamp, M.A., Steiger, HJ., Hänggi, D. (2012). Ion Channel Assessment. In: Chen, J., Xu, XM., Xu, Z., Zhang, J. (eds) Animal Models of Acute Neurological Injuries II. Springer Protocols Handbooks. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-61779-576-3_42

Download citation

  • DOI: https://doi.org/10.1007/978-1-61779-576-3_42

  • Published:

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-61779-575-6

  • Online ISBN: 978-1-61779-576-3

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics