Prostatic acid phosphatase reduces thermal sensitivity and chronic pain sensitization by depleting phosphatidylinositol 4,5-bisphosphate

Journal of Neuroscience

Volumn 30, Issue 31, 2010, Pages 10282-10293

  Sowa, Nathaniel A ^a,b   Street, Sarah E ^a   Vihko, Pirkko ^c,d   Zylka, Mark J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE PROSTATE ISOENZYME; ADENOSINE A1 RECEPTOR; ADENOSINE TRIPHOSPHATE; BRADYKININ; LYSOPHOSPHATIDIC ACID; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C; THROMBIN RECEPTOR; VANILLOID RECEPTOR 1;

ALLODYNIA; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; DISEASE ASSOCIATION; EMBRYO; HUMAN; HUMAN CELL; HYPERALGESIA; IN VIVO STUDY; INFLAMMATION; INHIBITION KINETICS; MALE; MOUSE; NERVE INJURY; NOCICEPTION; NOCICEPTIVE RECEPTOR; NOCICEPTIVE STIMULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; SENSITIZATION; SPINAL GANGLION; TEMPERATURE SENSITIVITY;

ANIMALS; CALCIUM; CELL LINE; ELECTROPHYSIOLOGY; GANGLIA, SPINAL; HOT TEMPERATURE; HUMANS; HYPERALGESIA; MALE; MICE; MICE, TRANSGENIC; NOCICEPTORS; PAIN MEASUREMENT; PAIN THRESHOLD; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN TYROSINE PHOSPHATASES; RECEPTOR, ADENOSINE A1; TRPV CATION CHANNELS; TYPE C PHOSPHOLIPASES;

EID: 77955387987     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2162-10.2010     Document Type: Article

References (63)

1. Basbaum AI, Bautista DM, Scherrer G, Julius D (2009) Cellular and molecular mechanisms of pain. Cell 139:267-284.
2. 4 ATP-gated channels through direct interactions. J Neurosci 28:12938-12945.
3. Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW 4th (2002) cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35:721-731.
4. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW 4th (2003) Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci U S A 100:12480-12485.
5. Boison D (2008) Adenosine as a neuromodulator in neurological diseases. Curr Opin Pharmacol 8:2-7.
6. Burnstock G (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659-797.
7. Campagnola L, Wang H, Zylka MJ (2008) Fiber-coupled light-emitting diode for localized photostimulation of neurons expressing channelrhodopsin-2. J Neurosci Methods 169:27-33.
8. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
9. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313.
10. Dale C, Vergnolle N (2008) Protease signaling to G protein-coupled receptors: implications for inflammation and pain. J Recept Signal Transduct Res 28:29-37.
11. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183-187.
12. Dickenson JM, Hill SJ (1998) Involvement of G-protein betagamma subunits in coupling the adenosine A1 receptor to phospholipase C in transfected CHO cells. Eur J Pharmacol 355:85-93.
13. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651-657.
14. Dolphin AC, Forda SR, Scott RH (1986) Calcium-dependent currents in cultured rat dorsal root ganglion neurones are inhibited by an adenosine analogue. J Physiol 373:47-61.
15. Eisenach JC, Rauck RL, Curry R (2003) Intrathecal, but not intravenous adenosine reduces allodynia in patients with neuropathic pain. Pain 105:65-70.
16. Elmes SJ, Millns PJ, Smart D, Kendall DA, Chapman V (2004) Evidence for biological effects of exogenous LPA on rat primary afferent and spinal cord neurons. Brain Res 1022:205-213.
17. Fairbanks CA (2003) Spinal delivery of analgesics in experimental models of pain and analgesia. Adv Drug Deliv Rev 55:1007-1041.
18. 2+ channels. J Neurosci 24:10980-10992.
19. Huang J, Zhang X, McNaughton PA (2006) Inflammatory pain: the cellular basis of heat hyperalgesia. Curr Neuropharmacol 4:197-206.
20. Hucho T, Levine JD (2007) Signaling pathways in sensitization: toward a nociceptor cell biology. Neuron 55:365-376.
21. Inoue M, Rashid MH, Fujita R, Contos JJ, Chun J, Ueda H (2004) Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat Med 10:712-718.
22. Jacobson KA, Gao ZG (2006) Adenosine receptors as therapeutic targets. Nat Rev Drug Discov 5:247-264.
23. Ji RR, Gereau RW 4th, Malcangio M, Strichartz GR (2009) MAP kinase and pain. Brain Res Rev 60:135-148.
24. Kelley GG, Kaproth-Joslin KA, Reks SE, Smrcka AV, Wojcikiewicz RJ (2006) G-protein-coupled receptor agonists activate endogenous phospholipase Cepsilon and phospholipase Cbeta3 in a temporally distinct manner. J Biol Chem 281:2639-2648.
25. Kim AY, Tang Z, Liu Q, Patel KN, Maag D, Geng Y, Dong X (2008) Pirt, a phosphoinositide-binding protein, functions as a regulatory subunit of TRPV1. Cell 133:475-485.
26. 2) is the endogenous lipid regulating TRPV1. J Biol Chem 283:26208-26216.
27. Kwon Y, Hofmann T, Montell C (2007) Integration of phosphoinositide-and calmodulin-mediated regulation of TRPC6. Mol Cell 25:491-503.
28. 1 adenosine receptor. Pain 94:315-324.
29. Li J, Perl ER (1994) Adenosine inhibition of synaptic transmission in the substantia gelatinosa. J Neurophysiol 72:1611-1621.
30. + channel activity. Diabetes 54:2852-2858.
31. Lishko PV, Procko E, Jin X, Phelps CB, Gaudet R (2007) The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 54:905-918.
32. Liu B, Zhang C, Qin F (2005) Functional recovery from desensitization of vanilloid receptor TRPV1 requires resynthesis of phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:4835-4843.
33. Loram LC, Harrison JA, Sloane EM, Hutchinson MR, Sholar P, Taylor FR, Berkelhammer D, Coats BD, Poole S, Milligan ED, Maier SF, Rieger J, Watkins LR (2009) Enduring reversal of neuropathic pain by a single intrathecal injection of adenosine 2A receptor agonists: a novel therapy for neuropathic pain. J Neurosci 29:14015-14025.
34. Lukacs V, Thyagarajan B, Várnai P, Balla A, Balla T, Rohacs T (2007) Dual regulation of TRPV1 by phosphoinositides. J Neurosci 27:7070-7080.
35. Luo MC, Zhang DQ, Ma SW, Huang YY, Shuster SJ, Porreca F, Lai J (2005) An efficient intrathecal delivery of small interfering RNA to the spinal cord and peripheral neurons. Mol Pain 1:29.
36. Ma L, Matsumoto M, Xie W, Inoue M, Ueda H (2009) Evidence for lysophosphatidic acid 1 receptor signaling in the early phase of neuropathic pain mechanisms in experiments using Ki-16425, a lysophosphatidic acid 1 receptor antagonist. J Neurochem 109:603-610.
37. Mills GB, Moolenaar WH (2003) The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer 3:582-591.
38. Milosevic I, Sørensen JB, Lang T, Krauss M, Nagy G, Haucke V, Jahn R, Neher E (2005) Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J Neurosci 25:2557-2565.
39. Murthy KS, Makhlouf GM (1995) Adenosine A1 receptor-mediated activation of phospholipase C-beta 3 in intestinal muscle: dual requirement for alpha and beta gamma subunits of Gi3. Mol Pharmacol 47:1172-1179.
40. Nakagawa T, Wakamatsu K, Zhang N, Maeda S, Minami M, Satoh M, Kaneko S (2007) Intrathecal administration of ATP produces long-lasting allodynia in rats: differential mechanisms in the phase of the induction and maintenance. Neuroscience 147:445-455.
41. Narita M, Ohsawa M, Mizoguchi H, Aoki T, Suzuki T, Tseng LF (2000) Role of the phosphatidylinositol-specific phospholipase C pathway in deltaopioid receptor-mediated antinociception in the mouse spinal cord. Neuroscience 99:327-331.
42. 2A receptor mediates microglial process retraction. Nat Neurosci 12:872-878.
43. Ostanin K, Saeed A, Van Etten RL (1994) Heterologous expression of human prostatic acid phosphatase and site-directed mutagenesis of the enzyme active site. J Biol Chem 269:8971-8978.
44. Ozaki S, DeWald DB, Shope JC, Chen J, Prestwich GD (2000) Intracellular delivery of phosphoinositides and inositol phosphates using polyamine carriers. Proc Natl Acad Sci U S A 97:11286-11291.
45. Park KA, Vasko MR (2005) Lipid mediators of sensitivity in sensory neurons. Trends Pharmacol Sci 26:571-577.
46. Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300:1284-1288.
47. Reppert SM, Weaver DR, Stehle JH, Rivkees SA (1991) Molecular cloning and characterization of a rat A1-adenosine receptor that is widely expressed in brain and spinal cord. Mol Endocrinol 5:1037-1048.
48. Rohacs T, Thyagarajan B, Lukacs V (2008) Phospholipase C mediated modulation of TRPV1 channels. Mol Neurobiol 37:153-163.
49. Sawynok J (2007) Adenosine and ATP receptors. Handb Exp Pharmacol 177:309-328.
50. Schneider G, Lindqvist Y, Vihko P (1993) Three-dimensional structure of rat acid phosphatase. EMBO J 12:2609-2615.
51. Schulte G, Robertson B, Fredholm BB, DeLander GE, Shortland P, Molander C (2003) Distribution of antinociceptive adenosine A1 receptors in the spinal cord dorsal horn, and relationship to primary afferents and neuronal subpopulations. Neuroscience 121:907-916.
52. Shields SD, Eckert WA 3rd, Basbaum AI (2003) Spared nerve injury model of neuropathic pain in the mouse: a behavioral and anatomic analysis. J Pain 4:465-470.
53. 1-adenosine receptors to mediate antinociception. PLoS ONE 4:e4248.
54. Sowa NA, Taylor-Blake B, Zylka MJ (2010) Ecto-5′-nucleotidase (CD73) inhibits nociception by hydrolyzing AMP to adenosine in nociceptive circuits. J Neurosci 30:2235-2244.
55. Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE (2006) Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol 128:509-522.
56. Suh BC, Hille B (2005) Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr Opin Neurobiol 15:370-378.
57. 3H]inositol-labeled phosphoinositide pools. J Cell Biol 143:501-510.
58. Várnai P, Thyagarajan B, Rohacs T, Balla T (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175:377-382.
59. Vihko P (1978) Characterization of the principal human prostatic acid phosphatase isoenzyme, purified by affinity chromatography and isoelectric focusing. Part II. Clin Chem 24:1783-1787.
60. Wang H, Ehnert C, Brenner GJ, Woolf CJ (2006) Bradykinin and peripheral sensitization. Biol Chem 387:11-14.
61. Wu WP, Hao JX, Halldner L, Lövdahl C, DeLander GE, Wiesenfeld-Hallin Z, Fredholm BB, Xu XJ (2005) Increased nociceptive response in mice lacking the adenosine A1 receptor. Pain 113:395-404.
62. Yao J, Qin F (2009) Interaction with phosphoinositides confers adaptation onto the TRPV1 pain receptor. PLoS Biol 7:e46.
63. Zylka MJ, Sowa NA, Taylor-Blake B, Twomey MA, Herrala A, Voikar V, Vihko P (2008) Prostatic acid phosphatase is an ectonucleotidase and suppresses pain by generating adenosine. Neuron 60:111-122.