- About this Journal ·
- Abstracting and Indexing ·
- Advance Access ·
- Aims and Scope ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Pain Research and Treatment
Volume 2013 (2013), Article ID 217864, 8 pages
Role of NHE1 in Nociception
1Centro de Investigación y Posgrado y División Académica de Ciencias de la Salud, Universidad Juárez Autónoma de Tabasco, 86040 Villahermosa, TAB, Mexico
2Hospital Regional de Alta Especialidad “Dr. Juan Graham Casasús”, 86126 Villahermosa, TAB, Mexico
3Sección de Estudios de Posgrado e Investigación, Escuela Superior de Medicina, Instituto Politécnico Nacional, 11340 México, DF, Mexico
4Departamento de Farmacobiología, Centro de Investigación y de Estudios Avanzados (Cinvestav), Sede Sur, Calzada Tenorios 235, Colonia Granjas Coapa, 14330 México, DF, Mexico
Received 29 August 2012; Accepted 2 January 2013
Academic Editor: Pierangelo Geppetti
Copyright © 2013 Jorge Elías Torres-López et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- M. Chesler, “Regulation and modulation of pH in the brain,” Physiological Reviews, vol. 83, no. 4, pp. 1183–1221, 2003.
- A. Roos and W. F. Boron, “Intracellular pH,” Physiological Reviews, vol. 61, no. 2, pp. 296–434, 1981.
- J. R. Casey, S. Grinstein, and J. Orlowski, “Sensors and regulators of intracellular pH,” Nature Reviews Molecular Cell Biology, vol. 11, no. 1, pp. 50–61, 2010.
- J. W. Deitmer and C. R. Rose, “pH regulation and proton signalling by glial cells,” Progress in Neurobiology, vol. 48, no. 2, pp. 73–103, 1996.
- A. Hulikova, A. L. Harris, R. D. Vaughan-Jones, and P. Swietach, “Acid-extrusion from tissue: the interplay between membrane transporters and pH buffers,” Current Pharmaceutical Design, vol. 18, no. 10, pp. 1331–1137, 2012.
- L. K. Putney, S. P. Denker, and D. L. Barber, “The changing face of the Na+/H+ exchanger, NHE1: structure, regulation, and cellular actions,” Annual Review of Pharmacology and Toxicology, vol. 42, pp. 527–552, 2002.
- S. F. Pedersen, M. E. O'Donnell, S. E. Anderson, and P. M. Cala, “Physiology and pathophysiology of Na+/H+ exchange and Na+-K+-2Cl− cotransport in the heart, brain, and blood,” American Journal of Physiology, vol. 291, no. 1, pp. R1–R25, 2006.
- J. Pouysségur, “Molecular biology and hormonal regulation of vertebrate Na+/H+ exchanger isoforms,” Renal Physiology and Biochemistry, vol. 17, no. 3-4, pp. 190–193, 1994.
- J. Orlowski and S. Grinstein, “Na+/H+ exchangers of mammalian cells,” Journal of Biological Chemistry, vol. 272, no. 36, pp. 22373–22376, 1997.
- J. Orlowski and S. Grinstein, “Diversity of the mammalian sodium/proton exchanger SLC9 gene family,” Pflugers Archiv European Journal of Physiology, vol. 447, no. 5, pp. 549–565, 2004.
- S. F. Pedersen and P. M. Cala, “Comparative biology of the ubiquitous Na+/H+ exchanger, NHE1: lessons from erythrocytes,” Journal of Experimental Zoology Part A, vol. 301, no. 7, pp. 569–578, 2004.
- E. R. Slepkov, J. K. Rainey, B. D. Sykes, and L. Fliegel, “Structural and functional analysis of the Na+/H+ exchanger,” Biochemical Journal, vol. 401, no. 3, pp. 623–633, 2007.
- M. Obara, M. Szeliga, and J. Albrecht, “Regulation of pH in the mammalian central nervous system under normal and pathological conditions: facts and hypotheses,” Neurochemistry International, vol. 52, no. 6, pp. 905–919, 2008.
- R. A. Cardone, V. Casavola, and S. J. Reshkin, “The role of disturbed pH dynamics and the NA+/H+ exchanger in metastasis,” Nature Reviews Cancer, vol. 5, no. 10, pp. 786–795, 2005.
- M. Avkiran, “Protection of the ischaemic myocardium by Na+/H+ exchange inhibitors: potential mechanisms of action,” Basic Research in Cardiology, vol. 96, no. 4, pp. 306–311, 2001.
- L. Fliegel, “Regulation of myocardial Na+/H+ exchanger activity,” Basic Research in Cardiology, vol. 96, no. 4, pp. 301–305, 2001.
- K. Imahashi, F. Mraiche, C. Steenbergen, E. Murphy, and L. Fliegel, “Overexpression of the Na+/H+ exchanger and ischemia-reperfusion injury in the myocardium,” American Journal of Physiology, vol. 292, no. 5, pp. H2237–H2247, 2007.
- A. R. Cook, S. C. Bardswell, S. Pretheshan et al., “Paradoxical resistance to myocardial ischemia and age-related cardiomyopathy in NHE1 transgenic mice: a role for ER stress?” Journal of Molecular and Cellular Cardiology, vol. 46, no. 2, pp. 225–233, 2009.
- F. Mraiche, C. S. Wagg, G. D. Lopaschuk, and L. Fliegel, “Elevated levels of activated NHE1 protect the myocardium and improve metabolism following ischemia/reperfusion injury,” Journal of Molecular and Cellular Cardiology, vol. 50, no. 1, pp. 157–164, 2011.
- C. C. Aickin and R. C. Thomas, “An investigation of the ionic mechanism of intracellular pH regulation in mouse soleus muscle fibres,” Journal of Physiology, vol. 273, no. 1, pp. 295–316, 1977.
- C. Sardet, A. Franchi, and J. Pouysségur, “Molecular cloning of the growth-factor-activatable human Na+/H+ antiporter,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 53, no. 2, pp. 1011–1018, 1988.
- C. Sardet, A. Franchi, and J. Pouysségur, “Molecular cloning, primary structure, and expression of the human growth factor-activatable Na+/H+ antiporter,” Cell, vol. 56, no. 2, pp. 271–280, 1989.
- G. Kemp, H. Young, and L. Fliegel, “Structure and function of the human Na+/H+ exchanger isoform,” Channels, vol. 2, no. 5, pp. 329–336, 2008.
- D. Biemesderfer, J. Pizzonia, A. Abu-Alfa et al., “NHE3: a Na+/H+ exchanger isoform of renal brush border,” American Journal of Physiology, vol. 265, no. 5, pp. F736–F742, 1993.
- C. Bookstein, M. W. Musch, A. DePaoli et al., “A unique sodium-hydrogen exchange isoform (NHE-4) of the inner medulla of the rat kidney is induced by hyperosmolarity,” Journal of Biological Chemistry, vol. 269, no. 47, pp. 29704–29709, 1994.
- W. A. Hoogerwerf, S. C. Tsao, O. Devuyst et al., “NHE2 and NHE3 are human and rabbit intestinal brush-border proteins,” American Journal of Physiology, vol. 270, no. 1, pp. G29–G41, 1996.
- N. C. Zachos, M. Tse, and M. Donowitz, “Molecular physiology of intestinal Na+/H+ exchange,” Annual Review of Physiology, vol. 67, pp. 411–443, 2005.
- C. A. Klanke, Yan Ru Su, D. F. Callen et al., “Molecular cloning and physical and genetic mapping of a novel human Na+/H+ exchanger (NHE5/SLC9A5) to chromosome 16q22.1,” Genomics, vol. 25, no. 3, pp. 615–622, 1995.
- N. R. Baird, J. Orlowski, E. Z. Szabó et al., “Molecular cloning, genomic organization, and functional expression of Na+/H+ exchanger isoform 5 (NHE5) from human brain,” Journal of Biological Chemistry, vol. 274, no. 7, pp. 4377–4382, 1999.
- E. Miyazaki, M. Sakaguchi, S. Wakabayashi, M. Shigekawa, and K. Mihara, “NHE6 protein possesses a signal peptide destined for endoplasmic reticulum membrane and localizes in secretory organelles of the cell,” Journal of Biological Chemistry, vol. 276, no. 52, pp. 49221–49227, 2001.
- N. Fukura, R. Ohgaki, M. Matsushita, N. Nakamura, K. Mitsui, and H. Kanazawa, “A membrane-proximal region in the C-terminal tail of NHE7 is required for its distribution in the trans-golgi network, distinct from NHE6 localization at endosomes,” Journal of Membrane Biology, vol. 234, no. 3, pp. 149–158, 2010.
- S. Wakabayashi, T. Pang, X. Su, and M. Shigekawa, “A novel topology model of the human Na+/H+ exchanger isoform 1,” Journal of Biological Chemistry, vol. 275, no. 11, pp. 7942–7949, 2000.
- R. Béliveau, M. Demeule, and M. Potier, “Molecular size of the Na+-H+ antiport in renal brush border membranes, as estimated by radiation inactivation,” Biochemical and Biophysical Research Communications, vol. 152, no. 1, pp. 484–489, 1988.
- P. Fafournoux, J. Noël, and J. Pouysségur, “Evidence that Na+/H+ exchanger isoforms NHE1 and NHE3 exist as stable dimers in membranes with a high degree of specificity for homodimers,” Journal of Biological Chemistry, vol. 269, no. 4, pp. 2589–2596, 1994.
- M. Krishna and H. Narang, “The complexity of mitogen-activated protein kinases (MAPKs) made simple,” Cellular and Molecular Life Sciences, vol. 65, no. 22, pp. 3525–3544, 2008.
- H. Wang, N. L. C. L. Silva, P. A. Lucchesi et al., “Phosphorylation and regulation of the Na+/H+ exchanger through mitogen-activated protein kinase,” Biochemistry, vol. 36, no. 30, pp. 9151–9158, 1997.
- A. N. Moor and L. Fliegel, “Protein kinase-mediated regulation of the Na+/H+ exchanger in the rat myocardium by mitogen-activated protein kinase-dependent pathways,” Journal of Biological Chemistry, vol. 274, no. 33, pp. 22985–22992, 1999.
- A. N. Moor, X. T. Gan, M. Karmazyn, and L. Fliegel, “Activation of Na+/H+ exchanger-directed protein kinases in the ischemic and ischemic-reperfused rat myocardium,” Journal of Biological Chemistry, vol. 276, no. 19, pp. 16113–16122, 2001.
- A. R. Khaled, A. N. Moor, A. Li et al., “Trophic factor withdrawal: p38 mitogen-activated protein kinase activates NHE1, which induces intracellular alkalinization,” Molecular and Cellular Biology, vol. 21, no. 22, pp. 7545–7557, 2001.
- R. S. Haworth, C. McCann, A. K. Snabaitis, N. A. Roberts, and M. Avkiran, “Stimulation of the plasma membrane Na+/H+ exchanger NHE1 by sustained intracellular acidosis. Evidence for a novel mechanism mediated by the ERK pathway,” Journal of Biological Chemistry, vol. 278, no. 34, pp. 31676–31684, 2003.
- J. Luo and D. Sun, “Physiology and pathophysiology of Na+/H+ exchange isoform 1 in the central nervous system,” Current Neurovascular Research, vol. 4, no. 3, pp. 205–215, 2007.
- P. Karki, E. Coccaro, and L. Fliegel, “Sustained intracellular acidosis activates the myocardial Na+/H+ exchanger independent of amino acid Ser703 and p90rsk,” Biochimica et Biophysica Acta, vol. 1798, no. 8, pp. 1565–1576, 2010.
- T. Tominaga, T. Ishizaki, S. Narumiya, and D. L. Barber, “p160ROCK mediates RhoA activation of Na-H exchange,” The EMBO Journal, vol. 17, no. 16, pp. 4712–4722, 1998.
- W. Yan, K. Nehrke, J. Choi, and D. L. Barber, “Nck-interacting kinase (NIK) phosphorylates the Na+-H+ exchanger NHE1 and regulates NHE1 activation by platelet-derived growth factor,” Journal of Biological Chemistry, vol. 276, no. 33, pp. 31349–31356, 2001.
- X. Li, B. Alvarez, J. R. Casey, R. A. F. Reithmeier, and L. Fliegel, “Carbonic anhydrase II binds to and enhances activity of the Na+/H+ exchanger,” Journal of Biological Chemistry, vol. 277, no. 39, pp. 36085–36091, 2002.
- B. Bertrand, S. Wakabayashi, T. Ikeda, J. Pouysségur, and M. Shigekawa, “The Na+/H+ exchanger isoform 1 (NHE1) is a novel member of the calmodulin-binding proteins. Identification and characterization of calmodulin-binding sites,” Journal of Biological Chemistry, vol. 269, no. 18, pp. 13703–13709, 1994.
- S. Wakabayashi, T. Ikeda, T. Iwamoto, J. Pouysségur, and M. Shigekawa, “Calmodulin-binding autoinhibitory domain controls 'pH-sensing' in the Na+/H+ exchanger NHE1 through sequence-specific interaction,” Biochemistry, vol. 36, no. 42, pp. 12854–12861, 1997.
- T. Pang, X. Su, S. Wakabayashi, and M. Shigekawa, “Calcineurin homologous protein as an essential cofactor for Na+/H+ exchangers,” Journal of Biological Chemistry, vol. 276, no. 20, pp. 17367–17372, 2001.
- T. Pang, S. Wakabayashi, and M. Shigekawa, “Expression of calcineurin B homologous protein 2 protects serum deprivation-induced cell death by serum-independent activation of Na+/H+ exchanger,” Journal of Biological Chemistry, vol. 277, no. 46, pp. 43771–43777, 2002.
- H. C. Zaun, A. Shrier, and J. Orlowski, “Calcineurin B homologous protein 3 promotes the biosynthetic maturation, cell surface stability, and optimal transport of the Na+/H+ exchanger NHE1 isoform,” Journal of Biological Chemistry, vol. 283, no. 18, pp. 12456–12467, 2008.
- O. Aharonovitz, H. C. Zaun, T. Balla, J. D. York, J. Orlowski, and S. Grinstein, “Intracellular pH regulation by Na+/H+ exchange requires phosphatidylinositol 4,5-bisphosphate,” Journal of Cell Biology, vol. 150, no. 1, pp. 213–224, 2000.
- S. P. Denker, D. C. Huang, J. Orlowski, H. Furthmayr, and D. L. Barber, “Direct binding of the Na-H exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H+ translocation,” Molecular Cell, vol. 6, no. 6, pp. 1425–1436, 2000.
- A. K. Snabaitis, F. Cuello, and M. Avkiran, “Protein kinase B/Akt phosphorylates and inhibits the cardiac Na+/H+ Exchanger NHE1,” Circulation Research, vol. 103, no. 8, pp. 881–890, 2008.
- A. K. Snabaitis, R. D'Mello, S. Dashnyam, and M. Avkiran, “A novel role for protein phosphatase 2A in receptor-mediated regulation of the cardiac sarcolemmal Na+/H+ exchanger NHE1,” Journal of Biological Chemistry, vol. 281, no. 29, pp. 20252–20262, 2006.
- H. I. Rocha-González, G. Castañeda-Corral, C. I. Araiza-Saldaña et al., “Identification of the Na+/H+ exchanger 1 in dorsal root ganglion and spinal cord: its possible role in inflammatory nociception,” Neuroscience, vol. 160, no. 1, pp. 156–164, 2009.
- G. Castañeda-Corral, H. I. Rocha-González, B. Godínez-Chaparro, J. M. Jiménez-Andrade, and V. Granados-Soto, “Role of the spinal Na+/H+ exchanger in formalin-induced nociception,” Neuroscience Letters, vol. 501, no. 1, pp. 4–9, 2011.
- K. H. Steen, H. Wegner, and P. W. Reeh, “The pH response of rat cutaneous nociceptors correlates with extracellular [Na+] and is increased under amiloride,” European Journal of Neuroscience, vol. 11, no. 8, pp. 2783–2792, 1999.
- G. Castañeda-Corral, H. I. Rocha-González, Araiza-Saldañ et al., “Blockade of peripheral and spinal Na+/H+ exchanger increases formalin-induced long-lasting mechanical allodynia and hyperalgesia in rats,” Brain Research, vol. 1475, pp. 19–30, 2012.
- I. Khan, I. Siddique, F. M. Al-Awadi, and K. Mohan, “Role of Na+/H+ exchanger isoform-1 in human inflammatory bowel disease,” Canadian Journal of Gastroenterology, vol. 17, no. 1, pp. 31–36, 2003.
- I. Siddique and I. Khan, “Mechanism of regulation of Na-H exchanger in inflammatory bowel disease: role of TLR-4 signaling mechanism,” Digestive Diseases and Sciences, vol. 56, no. 6, pp. 1656–1662, 2011.
- A. Muthuraman, A. S. Jaggi, N. Singh, and D. Singh, “Ameliorative effects of amiloride and pralidoxime in chronic constriction injury and vincristine induced painful neuropathy in rats,” European Journal of Pharmacology, vol. 587, no. 1–3, pp. 104–111, 2008.
- J. Ferreira, A. R. S. Santos, and J. B. Calixto, “Antinociception produced by systemic, spinal and supraspinal administration of amiloride in mice,” Life Sciences, vol. 65, no. 10, pp. 1059–1066, 1999.
- C. N. Liu and C. J. Somps, “Na+H+ exchanger-1 inhibitors reduce neuronal excitability and alter Na+ channel inactivation properties in rat primary sensory neurons,” Toxicological Sciences, vol. 103, no. 2, pp. 346–353, 2008.
- J. C. Pettersen, L. Chouinard, R. L. Kerlin et al., “Neurotoxic effects of zoniporide: a selective inhibitor of the Na+/H+ exchanger isoform 1,” Toxicologic Pathology, vol. 36, no. 4, pp. 608–619, 2008.
- S. M. Hwang, N. Y. Koo, M. Jin et al., “Intracellular acidification is associated with changes in free cytosolic calcium and inhibition of action potentials in rat trigeminal ganglion,” Journal of Biological Chemistry, vol. 286, no. 3, pp. 1719–1729, 2011.
- I. Khan, F. M. Al-Awadi, and H. Abul, “Colitis-induced changes in the expression of the Na+/H+ exchanger isoform NHE-1,” Journal of Pharmacology and Experimental Therapeutics, vol. 285, no. 2, pp. 869–875, 1998.
- J. H. Shin, W. Namkung, C. H. Kim et al., “Expression of Na+/H+ exchanger isoforms in normal human nasal epithelial cells and functional activity of Na+/H+ exchanger 1 in intracellular pH regulation,” Acta Oto-Laryngologica, vol. 125, no. 3, pp. 286–292, 2005.
- BioGPS, http://biogps.org/#goto=welcome.
- N. L. Nakhoul, S. Abdulnour-Nakhoul, R. N. Khuri, E. M. Lieberman, and P. T. Hargittai, “Intracellular pH regulation in rat Schwann cells,” Glia, vol. 10, no. 3, pp. 155–164, 1994.
- Y. Yamamoto and K. Taniguchi, “Distribution of pH regulators in the rat laryngeal nerve: the spatial relationship between Na+/HCO3− cotransporters and Na+/H+ exchanger type 3,” Neuroscience Letters, vol. 368, no. 2, pp. 127–129, 2004.
- R. D. Saunders, Y. W. Brandon, and G. H. De Vries, “Role of intracellular pH in the axolemma- and myelin-induced proliferation of Schwann cells,” Journal of Neurochemistry, vol. 52, no. 5, pp. 1576–1581, 1989.
- Y. Liu, D. B. Kintner, V. Chanana et al., “Activation of microglia depends on Na+/H+ exchange-mediated H+ homeostasis,” Journal of Neuroscience, vol. 30, no. 45, pp. 15210–15220, 2010.
- L. Faff, C. Ohlemeyer, and H. Kettenmann, “Intracellular pH regulation in cultured microglial cells from mouse brain,” Journal of Neuroscience Research, vol. 46, no. 3, pp. 294–304, 1996.
- Y. Shi, V. Chanana, J. J. Watters, P. Ferrazzano, and D. Sun, “Role of sodium/hydrogen exchanger isoform 1 in microglial activation and proinflammatory responses in ischemic brains,” Journal of Neurochemistry, vol. 119, no. 1, pp. 124–135, 2011.
- R. W. Colburn, A. J. Rickman, and J. A. Deleo, “The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior,” Experimental Neurology, vol. 157, no. 2, pp. 289–304, 1999.
- S. X. Jin, Z. Y. Zhuang, C. J. Woolf, and R. R. Ji, “p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain,” Journal of Neuroscience, vol. 23, no. 10, pp. 4017–4022, 2003.
- M. D. Laird, J. R. Vender, and K. M. Dhandapani, “Opposing roles for reactive astrocytes following traumatic brain injury,” NeuroSignals, vol. 16, no. 2-3, pp. 154–164, 2008.
- D. J. Benos, S. McPherson, B. H. Hahn, M. A. Chaikin, and E. N. Benveniste, “Cytokines and HIV envelope glycoprotein gp120 stimulate Na+/H+ exchange in astrocytes,” Journal of Biological Chemistry, vol. 269, no. 19, pp. 13811–13816, 1994.
- M. O. Bevensee, M. Apkon, and W. F. Boron, “Intracellular pH regulation in cultured astrocytes from rat hippocampus. II. Electrogenic Na/HCO3 cotransport,” Journal of General Physiology, vol. 110, no. 4, pp. 467–483, 1997.
- J. H. Pizzonia, B. R. Ransom, and C. A. Pappas, “Characterization of Na+/H+ exchange activity in cultured rat hippocampal astrocytes,” Journal of Neuroscience Research, vol. 44, no. 2, pp. 191–198, 1996.
- P. Cengiz, N. Kleman, K. Uluc et al., “Inhibition of Na+/H+ exchanger isoform 1 is neuroprotective in neonatal hypoxic ischemic brain injury,” Antioxidants and Redox Signaling, vol. 14, no. 10, pp. 1803–1813, 2011.
- D. B. Kintner, A. Look, G. E. Shull, and D. Sun, “Stimulation of astrocyte Na+/H+ exchange activity in response to in vitro ischemia depends in part on activation of ERK1/2,” American Journal of Physiology, vol. 289, no. 4, pp. C934–C945, 2005.
- A. Mandal, M. Shahidullah, N. A. Delamere, and M. A. Terán, “Elevated hydrostatic pressure activates sodium/hydrogen exchanger-1 in rat optic nerve head astrocytes,” American Journal of Physiology, vol. 297, no. 1, pp. C111–C120, 2009.
- R. M. Touyz, S. Picard, E. L. Schiffrin, and C. F. Deschepper, “Cyclic GMP inhibits a pharmacologically distinct Na+/H+ exchanger variant in cultured rat astrocytes via an extracellular site of action,” Journal of Neurochemistry, vol. 68, no. 4, pp. 1451–1461, 1997.
- I. Siddique, F. Hasan, and I. Khan, “Suppression of Na+/H+ exchanger isoform-3 in human inflammatory bowel disease: lack of reversal by -aminosalicylate treatment,” Scandinavian Journal of Gastroenterology, vol. 44, no. 1, pp. 56–64, 2009.
- Z. H. Németh, E. A. Deitch, C. Szabó et al., “Na+/H+ exchanger blockade inhibits enterocyte inflammatory response and protects against colitis,” American Journal of Physiology, vol. 283, no. 1, pp. G122–G132, 2002.
- F. Kamachi, S. B. Hyun, N. Hirasawa, and K. Ohuchi, “Inhibition of lipopolysaccharide-induced prostaglandin E2 production and inflammation by the Na+/H+ exchanger inhibitors,” Journal of Pharmacology and Experimental Therapeutics, vol. 321, no. 1, pp. 345–352, 2007.