Inhibition of the plasma membrane Ca2+ Pump by CD44 receptor activation of tyrosine kinases increases the action potential afterhyperpolarization in sensory neurons

Journal of Neuroscience

Volumn 31, Issue 7, 2011, Pages 2361-2370

  Ghosh, Biswarup ^a   Li, Yan ^a   Thayer, Stanley A ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ION; CD44 RECEPTOR; CELL SURFACE RECEPTOR; FOCAL ADHESION KINASE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 4; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ARTICLE; CLEARANCE; CONTROLLED STUDY; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FEMALE; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE CELL;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; ANTIGENS, CD44; CALCIUM; CELL MEMBRANE; CELLS, CULTURED; ELECTRIC STIMULATION; ENZYME INHIBITORS; GANGLIA, SPINAL; INDOLES; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; PATCH-CLAMP TECHNIQUES; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; PROTEIN-TYROSINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 79951833494     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5764-10.2011     Document Type: Article

References (69)

1. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408:297-315.
2. Blake RA, Broome MA, Liu X, Wu J, Gishizky M, Sun L, Courtneidge SA (2000) SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol Cell Biol 20:9018-9027. (Pubitemid 32245931)
3. Bozulic LD, Malik MT, Dean WL (2007) Effects of plasma membrane Ca(2+) -ATPase tyrosine phosphorylation on human platelet function. J Thromb Haemost 5:1041-1046. (Pubitemid 46691735)
4. Burette A, Rockwood JM, Strehler EE, Weinberg RJ (2003) Isoform-specific distribution of the plasma membrane Ca2+ ATPase in the rat brain. J Comp Neurol 467:464-476. (Pubitemid 37467123)
5. Cabodi S, Di Stefano P, Leal Mdel P, Tinnirello A, Bisaro B, Morello V, Damiano L, Aramu S, Repetto D, Tornillo G, Defilippi P (2010) Integrins and signal transduction. Adv Exp Med Biol 674:43-54.
6. Caride AJ, Penheiter AR, Filoteo AG, Bajzer Z, Enyedi A, Penniston JT (2001) The plasma membrane calcium pump displays memory of past calcium spikes. Differences between isoforms 2b and 4b. J Biol Chem 276:39797-39804.
7. Chan CK, Wang J, Lin L, Hao Y, Chan SO (2007) Enzymatic removal of hyaluronan affects routing of axons in the mouse optic chiasm. Neuroreport 18:1533-1538. (Pubitemid 47476378)
8. Chen J, McLean PA, Neel BG, Okunade G, Shull GE, Wortis HH (2004) CD22 attenuates calcium signaling by potentiating plasma membrane calcium-ATPase activity. Nat Immunol 5:651-657. (Pubitemid 38811891)
9. Cordoba-Rodriguez R, Moore KA, Kao JPY, Weinreich D (1999) Calcium regulation of a slow post-spike hyperpolarization in vagal afferent neurons. Proc Natl Acad Sci U S A 96:7650-7657. (Pubitemid 29328335)
10. Di Leva F, Domi T, Fedrizzi L, Lim D, Carafoli E (2008) The plasma membrane Ca2+ ATPase of animal cells: structure, function and regulation. Arch Biochem Biophys 476:65-74.
11. Ditlevsen DK, Berezin V, Bock E (2007) Signalling pathways underlying neural cell adhesion molecule-mediated survival of dopaminergic neurons. Eur J Neurosci 25:1678-1684. (Pubitemid 46550009)
12. Dityatev A, Brückner G, Dityateva G, Grosche J, Kleene R, Schachner M (2007) Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev Neurobiol 67:570-588. (Pubitemid 47066941)
13. 2+ pump isoform 4b by phosphorylation of an inhibitory region downstream of the calmodulin-binding domain. J Biol Chem 271:32461-32467.
14. 2+ pump isoforms 2 and 3 and prevents binding of calmodulin. J Biol Chem 272:27525-27528.
15. Fernandes D, Zaidi A, Bean J, Hui D, Michaelis ML (2007) RNA(i)- induced silencing of the plasma membrane Ca(2+)- ATPase 2 in neuronal cells: effects on Ca(2+) homeostasis and cell viability. J Neurochem 102:454-465.
16. Filipp D, Julius M (2004) Lipid rafts: resolution of the "fyn problem?" Mol Immunol 41:645-656.
17. 2+ pump in rat brain - patterns of alternative splices seen by isoform-specific antibodies. J Biol Chem 272:23741-23747.
18. Fujita Y, Kitagawa M, Nakamura S, Azuma K, Ishii G, Higashi M, Kishi H, Hiwasa T, Koda K, Nakajima N, Harigaya K (2002) CD44 signaling through focal adhesion kinase and its anti-apoptotic effect. FEBS Lett 528:101-108. (Pubitemid 35258007)
19. Garcia ML, Usachev YM, Thayer SA, Strehler EE, Windebank AJ (2001) Plasma membrane calcium ATPase plays a role in reducing Ca(2+)-mediated cytotoxicity in PC12 cells. J Neurosci Res 64:661-669. (Pubitemid 32520689)
20. Giannone G, Rondé P, Gaire M, Beaudouin J, Haiech J, Ellenberg J, Takeda K (2004) Calcium rises locally trigger focal adhesion disassembly and enhance residency of focal adhesion kinase at focal adhesions. J Biol Chem 279:28715-28723. (Pubitemid 38900156)
21. Girault J-A, Costa A, Derkinderen P, Studler J-M, Toutant M (1999) FAK and PYK2/CAK[beta] in the nervous system: a link between neuronal activity, plasticity and survival? Trends Neurosci 22:257-263.
22. Glezer I, Bittencourt JC, Rivest S (2009) Neuronal expression of Cd36, Cd44, and Cd83 antigen transcripts maps to distinct and specific murine brain circuits. J Comp Neurol 517:906-924.
23. Gomis A, Pawlak M, Balazs EA, Schmidt RF, Belmonte C (2004) Effects of different molecular weight elastoviscous hyaluronan solutions on articular nociceptive afferents. Arthritis Rheum 50:314-326. (Pubitemid 38084317)
24. Goodison S, Urquidi V, Tarin D (1999) CD44 cell adhesion molecules. Mol Pathol 52:189-196. (Pubitemid 29369203)
25. Grant SG, O'Dell TJ, Karl KA, Stein PL, Soriano P, Kandel ER (1992) Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258:1903-1910. (Pubitemid 23026728)
26. Grant SG, Karl KA, Kiebler MA, Kandel ER (1995) Focal adhesion kinase in the brain: novel subcellular localization and specific regulation by Fyn tyrosine kinase in mutant mice. Genes Dev 9:1909-1921.
27. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
28. Guerini D, Pan B, Carafoli E (2003) Expression, purification, and characterization of isoform 1 of the plasma membrane Ca2+ pump: focus on calpain sensitivity. J Biol Chem 278:38141-38148. (Pubitemid 37229064)
29. Habib T, Park H, Tsang M, de Alborán IM, Nicks A, Wilson L, Knoepfler PS, Andrews S, Rawlings DJ, Eisenman RN, Iritani BM (2007) Myc stimulates B lymphocyte differentiation and amplifies calcium signaling. J Cell Biol 179:717-731. (Pubitemid 350146257)
30. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J Biol Chem 271:695-701.
31. Hua Q, Knudson CB, Knudson W (1993) Internalization of hyaluronan by chondrocytes occurs via receptor-mediated endocytosis. J Cell Sci 106:365-375. (Pubitemid 23286807)
32. Iacob S, Knudson CB (2006) Hyaluronan fragments activate nitric oxide synthase and the production of nitric oxide by articular chondrocytes. Int J Biochem Cell Biol 38:123-133. (Pubitemid 41540723)
33. Ikeda K, Nakao J, Asou H, Toya S, Shinoda J, Uyemura K (1996) Expression of CD44H in the cells of neural crest origin in peripheral nervous system. Neuroreport 7:1713-1716. (Pubitemid 26348241)
34. Ilangumaran S, Borisch B, Hoessli DC (1999) Signal transduction via CD44: role of plasma membrane microdomains. Leuk Lymphoma 35:455-469. (Pubitemid 30015645)
35. Jensen TP, Filoteo AG, Knopfel T, Empson RM (2007) Pre-synaptic plasma membrane Ca2+ ATPase isoform 2a regulates excitatory synaptic transmission in rat hippocampal CA3. J Physiol 579:85-99.
36. Jiang D, Liang J, Noble PW (2007) Hyaluronan in tissue injury and repair. Annu Rev Cell Dev Biol 23:435-461.
37. Kim Y, Lee YS, Choe J, Lee H, Kim YM, Jeoung D (2008) CD44-epidermal growth factor receptor interaction mediates hyaluronic acid-promoted cell motility by activating protein kinase C signaling involving Akt, Rac1, Phox, reactive oxygen species, focal adhesion kinase, and MMP-2. J Biol Chem 283:22513-22528.
38. Kochlamazashvili G, Henneberger C, Bukalo O, Dvoretskova E, Senkov O, Lievens PM, Westenbroek R, Engel AK, Catterall WA, Rusakov DA, Schachner M, Dityatev A (2010) The extracellular matrix molecule hyaluronic acid regulates hippocampal synaptic plasticity by modulating postsynaptic L-type Ca(2+) channels. Neuron 67:116-128.
39. Lesley J, Hascall VC, Tammi M, Hyman R (2000) Hyaluronan binding by cell surface CD44. J Biol Chem 275:26967-26975.
40. Levitzki A, Gazit A (1995) Tyrosine kinase inhibition: an approach to drug development. Science 267:1782-1788.
41. Li R, Wong N, Jabali MD, Johnson P (2001) CD44-initiated cell spreading induces Pyk2 phosphorylation, is mediated by Src family kinases, and is negatively regulated by CD45. J Biol Chem 276:28767-28773.
42. Maness PF (1992) Nonreceptor protein tyrosine kinases associated with neuronal development. Dev Neurosci 14:257-270.
43. Mariotti A, Kedeshian PA, Dans M, Curatola AM, Gagnoux-Palacios L, Giancotti FG (2001) EGF-R signaling through Fyn kinase disrupts the function of integrin alpha6beta4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J Cell Biol 155:447-458.
44. Omri B, Crisanti P, Marty MC, Alliot F, Fagard R, Molina T, Pessac B (1996) The Lck tyrosine kinase is expressed in brain neurons. J Neurochem 67:1360-1364. (Pubitemid 26314189)
45. Pá szty K, Verma AK, Padányi R, Filoteo AG, Penniston JT, Enyedi A (2002) Plasma membrane Ca2+ ATPase isoform 4b is cleaved and activated by caspase-3 during the early phase of apoptosis. J Biol Chem 277:6822-6829.
46. 2+ current in rat dorsal root ganglion neurons. Pflugers Arch 426:214-220.
47. Ponta H, Sherman L, Herrlich PA (2003) CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4:33-45. (Pubitemid 36077255)
48. Pottorf WJ, Thayer SA (2002) Transient rise in intracellular calcium produces a long-lasting increase in plasma membrane calcium pump activity in rat sensory neurons. J Neurochem 83:1002-1008.
49. Richard KC, Bertolesi GE, Dunfield LD, McMaster CR, Nachtigal MW (2006) TSAd interacts with Smad2 and Smad3. Biochem Biophys Res Commun 347:266-272. (Pubitemid 44015673)
50. Ries A, Goldberg JL, Grimpe B (2007) A novel biological function for CD44 in axon growth of retinal ganglion cells identified by a bioinformatics approach. J Neurochem 103:1491-1505. (Pubitemid 47631812)
51. Salmond RJ, Filby A, Qureshi I, Caserta S, Zamoyska R (2009) T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn, influences T-cell activation, differentiation, and tolerance. Immunol Rev 228:9-22.
52. Simons SB, Escobedo Y, Yasuda R, Dudek SM (2009) Regional differences in hippocampal calcium handling provide a cellular mechanism for limiting plasticity. Proc Natl Acad Sci U S A 106:14080-14084.
53. Stahl WL, Eakin TJ, Owens JW Jr, Breininger JF, Filuk PE, Anderson WR (1992) Plasma membrane Ca 2+-ATPase isoforms: distribution of mRNAs in rat brain by in situ hybridization. Brain Res Mol Brain Res 16:223-231. (Pubitemid 23035964)
54. Strehler EE, Zacharias DA (2001) Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev 81:21-50. (Pubitemid 32096172)
55. Sundvold-Gjerstad V, Granum S, Mustelin T, Andersen TC, Berge T, Shapiro MJ, Shapiro VS, Spurkland A, Lea T (2005) The C terminus of T cell-specific adapter protein (TSAd) is necessary for TSAd-mediated inhibition of Lck activity. Eur J Immunol 35:1612-1620. (Pubitemid 40691441)
56. Taher TE, Smit L, Griffioen AW, Schilder-Tol EJ, Borst J, Pals ST (1996) Signaling through CD44 is mediated by tyrosine kinases. Association with p56lck in T lymphocytes. J Biol Chem 271:2863-2867.
57. Tamura M, Gu J, Danen EH, Takino T, Miyamoto S, Yamada KM (1999) PTEN interactions with focal adhesion kinase and suppression of the extracellular matrix-dependent phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 274:20693-20703.
58. 2+ clearance from neurons. Front Biosci 7:d1255-d1279.
59. Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513-609. (Pubitemid 28034534)
60. Turner JM, Brodsky MH, Irving BA, Levin SD, Perlmutter RM, Littman DR (1990) Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell 60:755-765.
61. Usachev YM, Khammanivong A, Campbell C, Thayer SA (2000) Particle-mediated gene transfer to rat neurons in primary culture. Pflugers Arch 439:730-738. (Pubitemid 30191147)
62. 2+ pump isoform 4. Neuron 33:113-122.
63. 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 26:311-318. (Pubitemid 43089544)
64. 2+ pump isoform 4a at its calmodulin binding domain. J Biol Chem 274:527-531.
65. Wan TC, Zabe M, Dean WL (2003) Plasma membrane Ca2+-ATPase isoform 4b is phosphorylated on tyrosine 1176 in activated human platelets. Thrombosis and Haemostasis 89:122-131. (Pubitemid 36149801)
66. Werth JL, Usachev YM, Thayer SA (1996) Modulation of calcium efflux from cultured rat dorsal root ganglion neurons. J Neurosci 16:1008-1015. (Pubitemid 26140856)
67. Yousefi S, Ma XZ, Singla R, Zhou YC, Sakac D, Bali M, Liu Y, Sahai BM, Branch DR (2003) HIV-1 infection is facilitated in T cells by decreasing p56lck protein tyrosine kinase activity. Clin Exp Immunol 133:78-90. (Pubitemid 36791945)
68. 2+ pump isoforms and splice variants in the human brain. Brain Res Mol Brain Res 28:263-272.
69. Zhao J, Guan JL (2009) Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev 28:35-49.