TRPM2 mediates the lysophosphatidic acid-induced neurite retraction in the developing brain

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 10, 2014, Pages 1987-1998

  Jang, Yongwoo ^a   Lee, Mi Hyun ^a   Lee, Jesun ^a   Jung, Jooyoung ^a   Lee, Sung Hoon ^a   Yang, Dong Jin ^a   Kim, Byung Woo ^c   Son, Hyeon ^c   Lee, Boyoon ^a   Chang, Sunghoe ^a   Mori, Yasuo ^d   Oh, Uhtaek ^a,b  

^a Seoul National University   (South Korea)

^b Institut Pasteur Korea   (South Korea)

^c Hanyang University College of Medicine   (South Korea)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

Lysophosphatidic acid; Neurite outgrowth; Neuritogenesis; TRP channels; TRPM2

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ADENOSINE DIPHOSPHATE RIBOSE; CLUSTERIN; LYSOPHOSPHATIDIC ACID; MESSENGER RNA; SMALL INTERFERING RNA; UO 126; LYSOPHOSPHOLIPID; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BRAIN CELL CULTURE; BRAIN DEVELOPMENT; CELL ISOLATION; CEREBROSPINAL FLUID; CONTROLLED STUDY; EMBRYO; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PC12 CELL LINE; PRIMARY CULTURE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SYNAPTOGENESIS; ANIMAL; BRAIN; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; GENETICS; HEK293 CELL LINE; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; NEURITE;

ADENOSINE DIPHOSPHATE RIBOSE; ANIMALS; BRAIN; CELLS, CULTURED; HEK293 CELLS; HUMANS; LYSOPHOSPHOLIPIDS; MICE; NEURITES; NEUROGENESIS; PC12 CELLS; RATS; TRPM CATION CHANNELS;

EID: 84919941343     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1436-4     Document Type: Article

References (53)

1. Amaral MD, Pozzo-Miller L (2007) TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J Neurosci 27(19):5179–5189
2. Bito H, Furuyashiki T, Ishihara H, Shibasaki Y, Ohashi K, Mizuno K, Maekawa M, Ishizaki T, Narumiya S (2000) A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26(2):431–441
3. Buelow B, Song Y, Scharenberg AM (2008) The poly(ADP-ribose) polymerase PARP-1 is required for oxidative stress-induced TRPM2 activation in lymphocytes. J Biol Chem 283(36):24571–24583
4. Csanady L, Torocsik B (2009) Four Ca2+ ions activate TRPM2 channels by binding in deep crevices near the pore but intracellularly of the gate. J Gen Physiol 133(2):189–203
5. da Silva JS, Dotti CG (2002) Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 3(9):694–704
6. Dehay C, Kennedy H (2007) Cell-cycle control and cortical development. Nat Rev Neurosci 8(6):438–450
7. Fukushima N, Ishii I, Contos JJ, Weiner JA, Chun J (2001) Lysophospholipid receptors. Annu Rev Pharmacol Toxicol 41:507–534
8. Fukushima N, Weiner JA, Kaushal D, Contos JJ, Rehen SK, Kingsbury MA, Kim KY, Chun J (2002) Lysophosphatidic acid influences the morphology and motility of young, postmitotic cortical neurons. Mol Cell Neurosci 20(2):271–282
9. Gomez TM, Zheng JQ (2006) The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 7(2):115–125
10. Greka A, Navarro B, Oancea E, Duggan A, Clapham DE (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci 6(8):837–845
11. Harrison SM, Reavill C, Brown G, Brown JT, Cluderay JE, Crook B, Davies CH, Dawson LA, Grau E, Heidbreder C, Hemmati P, Hervieu G, Howarth A, Hughes ZA, Hunter AJ, Latcham J, Pickering S, Pugh P, Rogers DC, Shilliam CS, Maycox PR (2003) LPA1 receptor-deficient mice have phenotypic changes observed in psychiatric disease. Mol Cell Neurosci 24(4):1170–1179
12. Hecht JH, Weiner JA, Post SR, Chun J (1996) Ventricular zone gene-1 (vzg-1) encodes a lysophosphatidic acid receptor expressed in neurogenic regions of the developing cerebral cortex. J Cell Biol 135(4):1071–1083
13. Hill K, Benham CD, McNulty S, Randall AD (2004) Flufenamic acid is a pH-dependent antagonist of TRPM2 channels. Neuropharmacology 47(3):450–460
14. Hill K, McNulty S, Randall AD (2004) Inhibition of TRPM2 channels by the antifungal agents clotrimazole and econazole. Naunyn Schmiedebergs Arch Pharmacol 370(4):227–237
15. Hottiger MO, Boothby M, Koch-Nolte F, Luscher B, Martin NM, Plummer R, Wang ZQ, Ziegler M (2011) Progress in the function and regulation of ADP-ribosylation. Sci Signal 4(174):mr5
16. Hui H, McHugh D, Hannan M, Zeng F, Xu SZ, Khan SU, Levenson R, Beech DJ, Weiss JL (2006) Calcium-sensing mechanism in TRPC5 channels contributing to retardation of neurite outgrowth. J Physiol 572(Pt 1):165–172
17. Itagaki K, Kannan KB, Hauser CJ (2005) Lysophosphatidic acid triggers calcium entry through a non-store-operated pathway in human neutrophils. J Leukoc Biol 77(2):181–189
18. Jang Y, Jung J, Kim H, Oh J, Jeon JH, Jung S, Kim KT, Cho H, Yang DJ, Kim SM, Kim IB, Song MR, Oh U (2012) Axonal neuropathy-associated TRPV4 regulates neurotrophic factor-derived axonal growth. J Biol Chem 287(8):6014–6024
19. Jang Y, Lee Y, Kim SM, Yang YD, Jung J, Oh U (2012) Quantitative analysis of TRP channel genes in mouse organs. Arch Pharm Res 35(10):1823–1830
20. Kaczmarek JS, Riccio A, Clapham DE (2012) Calpain cleaves and activates the TRPC5 channel to participate in semaphorin 3A-induced neuronal growth cone collapse. Proc Natl Acad Sci U S A 109(20):7888–7892
21. Kingsbury MA, Rehen SK, Contos JJ, Higgins CM, Chun J (2003) Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding. Nat Neurosci 6(12):1292–1299
22. Koo JY, Jang Y, Cho H, Lee CH, Jang KH, Chang YH, Shin J, Oh U (2007) Hydroxy-alpha-sanshool activates TRPV1 and TRPA1 in sensory neurons. Eur J Neurosci 26(5):1139–1147
23. Ledesma MD, Dotti CG (2003) Membrane and cytoskeleton dynamics during axonal elongation and stabilization. Int Rev Cytol 227:183–219
24. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60(4):585–595
25. Levi A, Biocca S, Cattaneo A, Calissano P (1988) The mode of action of nerve growth factor in PC12 cells. Mol Neurobiol 2(3):201–226
26. Li Y, Mu Y, Gage FH (2009) Development of neural circuits in the adult hippocampus. Curr Top Dev Biol 87:149–174
27. Li Z, Van Aelst L, Cline HT (2000) Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat Neurosci 3(3):217–225
28. Luo L, O’Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127–156
29. Michaelsen K, Lohmann C (2010) Calcium dynamics at developing synapses: mechanisms and functions. Eur J Neurosci 32(2):218–223
30. Moughal NA, Waters CM, Valentine WJ, Connell M, Richardson JC, Tigyi G, Pyne S, Pyne NJ (2006) Protean agonism of the lysophosphatidic acid receptor-1 with Ki16425 reduces nerve growth factor-induced neurite outgrowth in pheochromocytoma 12 cells. J Neurochem 98(6):1920–1929
31. Nagamine K, Kudoh J, Minoshima S, Kawasaki K, Asakawa S, Ito F, Shimizu N (1998) Molecular cloning of a novel putative Ca2+ channel protein (TRPC7) highly expressed in brain. Genomics 54(1):124–131
32. Naziroglu M (2011) TRPM2 cation channels, oxidative stress and neurological diseases: where are we now? Neurochem Res 36(3):355–366
33. Nieto-Posadas A, Picazo-Juarez G, Llorente I, Jara-Oseguera A, Morales-Lazaro S, Escalante-Alcalde D, Islas LD, Rosenbaum T (2012) Lysophosphatidic acid directly activates TRPV1 through a C-terminal binding site. Nat Chem Biol 8(1):78–85
34. Nilius B, Voets T (2005) TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch 451(1):1–10
35. Nilius B, Voets T (2013) The puzzle of TRPV4 channelopathies. EMBO Rep 14(9):845
36. Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C, Stokes AJ, Zhu Q, Bessman MJ, Penner R, Kinet JP, Scharenberg AM (2001) ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 411(6837):595–599
37. Perraud AL, Takanishi CL, Shen B, Kang S, Smith MK, Schmitz C, Knowles HM, Ferraris D, Li W, Zhang J, Stoddard BL, Scharenberg AM (2005) Accumulation of free ADP-ribose from mitochondria mediates oxidative stress-induced gating of TRPM2 cation channels. J Biol Chem 280(7):6138–6148
38. Pool M, Thiemann J, Bar-Or A, Fournier AE (2008) NeuriteTracer: a novel ImageJ plugin for automated quantification of neurite outgrowth. J Neurosci Methods 168(1):134–139
39. Price RD, Yamaji T, Matsuoka N (2003) FK506 potentiates NGF-induced neurite outgrowth via the Ras/Raf/MAP kinase pathway. Br J Pharmacol 140(5):825–829
40. Roberts C, Winter P, Shilliam CS, Hughes ZA, Langmead C, Maycox PR, Dawson LA (2005) Neurochemical changes in LPA1 receptor deficient mice—a putative model of schizophrenia. Neurochem Res 30(3):371–377
41. Sano Y, Inamura K, Miyake A, Mochizuki S, Yokoi H, Matsushime H, Furuichi K (2001) Immunocyte Ca2+ influx system mediated by LTRPC2. Science 293(5533):1327–1330
42. Sato K, Malchinkhuu E, Muraki T, Ishikawa K, Hayashi K, Tosaka M, Mochiduki A, Inoue K, Tomura H, Mogi C, Nochi H, Tamoto K, Okajima F (2005) Identification of autotaxin as a neurite retraction-inducing factor of PC12 cells in cerebrospinal fluid and its possible sources. J Neurochem 92(4):904–914
43. Shim S, Goh EL, Ge S, Sailor K, Yuan JP, Roderick HL, Bootman MD, Worley PF, Song H, Ming GL (2005) XTRPC1-dependent chemotropic guidance of neuronal growth cones. Nat Neurosci 8(6):730–735
44. Shim S, Yuan JP, Kim JY, Zeng W, Huang G, Milshteyn A, Kern D, Muallem S, Ming GL, Worley PF (2009) Peptidyl-prolyl isomerase FKBP52 controls chemotropic guidance of neuronal growth cones via regulation of TRPC1 channel opening. Neuron 64(4):471–483
45. Tigyi G, Miledi R (1992) Lysophosphatidates bound to serum albumin activate membrane currents in Xenopus oocytes and neurite retraction in PC12 pheochromocytoma cells. J Biol Chem 267(30):21360–21367
46. Togashi K, Hara Y, Tominaga T, Higashi T, Konishi Y, Mori Y, Tominaga M (2006) TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J 25(9):1804–1815
47. Wen Z, Zheng JQ (2006) Directional guidance of nerve growth cones. Curr Opin Neurobiol 16(1):52–58
48. Xiang SY, Dusaban SS, Brown JH (2013) Lysophospholipid receptor activation of RhoA and lipid signaling pathways. Biochim Biophys Acta 1831(1):213–222
49. Xie Y, Gibbs TC, Meier KE (2002) Lysophosphatidic acid as an autocrine and paracrine mediator. Biochim Biophys Acta 1582(1–3):270–281
50. Yamamoto S, Shimizu S, Kiyonaka S, Takahashi N, Wajima T, Hara Y, Negoro T, Hiroi T, Kiuchi Y, Okada T, Kaneko S, Lange I, Fleig A, Penner R, Nishi M, Takeshima H, Mori Y (2008) TRPM2-mediated Ca2+influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat Med 14(7):738–747
51. Yung YC, Mutoh T, Lin ME, Noguchi K, Rivera RR, Choi JW, Kingsbury MA, Chun J (2011) Lysophosphatidic acid signaling may initiate fetal hydrocephalus. Sci Transl Med 3(99):99ra87
52. Zhang Z, Zhang W, Jung DY, Ko HJ, Lee Y, Friedline RH, Lee E, Jun J, Ma Z, Kim F, Tsitsilianos N, Chapman K, Morrison A, Cooper MP, Miller BA, Kim JK (2012) TRPM2 Ca2+ channel regulates energy balance and glucose metabolism. Am J Physiol Endocrinol Metab 302(7):E807–E816
53. Zhong Z, Zhai Y, Liang S, Mori Y, Han R, Sutterwala FS, Qiao L (2013) TRPM2 links oxidative stress to NLRP3 inflammasome activation. Nat Commun 4:1611