Target-derived neurotrophins coordinate transcription and transport of Bclw to prevent axonal degeneration

Annals of Internal Medicine

Volumn 158, Issue 6, 2013, Pages 5195-5207

  Cosker, Katharina E ^a,b   Pazyra Murphy, Maria F ^a,b   Fenstermacher, Sara J ^a,b   Segal, Rosalind A ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOMYCIN; CASPASE 6; CYCLOHEXIMIDE; NEUROTROPHIN; PROTEIN BAX; PROTEIN BCL W; THIOURIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; FOOT PAD; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROFLUIDIC ANALYSIS; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; STIMULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; AXONAL TRANSPORT; AXONS; BCL-X PROTEIN; CASPASE 6; CELLS, CULTURED; FEMALE; GANGLIA, SPINAL; HUMANS; MALE; MICE; NERVE DEGENERATION; NERVE GROWTH FACTORS; PREGNANCY; PROTEINS; RATS; RNA, MESSENGER; SENSORY RECEPTOR CELLS; TRANSCRIPTION, GENETIC;

EID: 84877088374     PISSN: 00034819     EISSN: 15393704     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3862-12.2013     Document Type: Article

References (56)

1. Andreassi C, Riccio A (2009) To localize or not to localize: mRNA fate is in 3'UTRends. Trends Cell Biol 19:465-474.CrossRef Medline
2. Andreassi C, Zimmermann C, Mitter R, Fusco S, Devita S, Saiardi A, Riccio A (2010) An NGF-responsive element targets myoinositol monophospha-tase-1 mRNA to sympathetic neuron axons. Nat Neurosci 13:291-301.CrossRef Medline
3. Brumovsky P, Villar MJ, Hokfelt T (2006) Tyrosine hydroxylase is ex-pressed in a subpopulation of small dorsal root ganglion neurons in the adult mouse. Exp Neurol 200:153-165. CrossRef Medline
4. Campenot RB (1982) Development of sympathetic neurons in compart-mentalized cultures: II. Local control of neurite survival by nerve growth factor. Dev Biol 93:13-21. CrossRef Medline
5. Chen CY, Ezzeddine N, Shyu AB (2008) Messenger RNA half-life measure-ments in mammalian cells. Methods Enzymol 448:335-357. CrossRef Medline
6. Chowdary PD, Che DL, Cui B (2012) Neurotrophin signaling via long-distance axonal transport. Annu Rev Phys Chem 63:571-594. CrossRef Medline
7. Cosker KE, Segal RA (2010) The longer U(T)R, the further you go. Nat Neurosci 13:273-275. CrossRef Medline
8. Cosker KE, Courchesne SL, Segal RA (2008) Action in the axon: generation and transport of signaling endosomes. CurrOpinNeurobiol 18:270-275. CrossRef Medline
9. Courchesne SL, Karch C, Pazyra-Murphy MF, Segal RA (2011) Sensory neuropathy attributable to loss of Bcl-w. J Neurosci 31:1624-1634. CrossRef Medline
10. Court FA, Coleman MP (2012) Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci 35:364-372. CrossRef Medline
11. Danckwardt S, Gantzert AS, Macher-Goeppinger S, Probst HC, Gentzel M, Wilm M, Grone HJ, Schirmacher P, Hentze MW, Kulozik AE (2011) p38 MAPK controls prothrombin expression by regulated RNA 3'end processing. Mol Cell 41:298-310. CrossRef Medline
12. Donnelly CJ, Fainzilber M, Twiss JL (2010) Subcellular communication through RNA transport and localized protein synthesis. Traffic 11:1498-1505. CrossRef Medline
13. Gilley J, Coleman MP (2010) Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol 8:e1000300.CrossRef Medline
14. Ginty DD, Segal RA (2002) Retrograde neurotrophin signaling: Trk-ing along the axon. Curr Opin Neurobiol 12:268-274. CrossRef Medline
15. Guhaniyogi J, Brewer G (2001) Regulation of mRNA stability in mamma-lian cells. Gene 265:11-23.CrossRef Medline
16. Gumy LF, Yeo GS, Tung YC, Zivraj KH, Willis D, Coppola G, Lam BY, Twiss JL, Holt CE, Fawcett JQ (2011) Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17:85-98.CrossRef Medline
17. Hafezparast M, Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, Bowen S, Lalli G, Witherden AS, Hummerich H, Nicholson S, Morgan PJ, Oozageer R, Priestley JV, Averill S, King VR, Ball S, Peters J, Toda T, Yamamoto A, Hiraoka Y, et al (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300:808-812.CrossRef Medline
18. Heerssen HM, Pazyra MF, Segal RA (2004) Dynein motors transport acti-vated Trks to promote survival of target-dependent neurons. NatNeuro-sci 7:596-604.CrossRef Medline
19. Hillefors M, Gioio AE, Mameza MG, Kaplan BB (2007) Axon viability and mitochondrial function are dependent on local protein synthesis in sym-pathetic neurons. Cell Mol Neurobiol 27:701-716.CrossRef Medline
20. Kim EM, Kim J, Park JK, Hwang SG, Kim WJ, Lee WJ, Kang SW, Um HD (2012) Bcl-w promotes cell invasion by blocking the invasion-suppressing action of Bax. Cell Signal 24:1163-1172. CrossRef Medline
21. Leclerc GJ, Leclerc GM, Barredo JC (2002) Real-time RT-PCR analysis of mRNA decay: half-life of/3-actin mRNA in human leukemia CCRF-CEM and Nalm-6 cell lines. Cancer Cell Int 2:1. CrossRef Medline
22. Luo L, O'Leary DD (2005) Axon retraction and degeneration in develop-ment and disease. Annu RevNeurosci 28:127-156. CrossRef Medline
23. Marmigere F, Ernfors P (2007) Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 8:114-127.CrossRef Medline
24. Merino D, Khaw SL, Glaser SP, Anderson DJ, Belmont LD, Wong C, Yue P, Robati M, Phipson B, Fairlie WD, Lee EF, Campbell KJ, Vandenberg CJ, Cory S, Roberts AW, Ludlam MJ, Huang DC, Bouillet P (2012) Bcl-2, Bcl-x(L), and Bcl-w are not equivalent targets of ABT-737 and navitoclax (ABT-263) in lymphoid and leukemic cells. Blood 119:5807-5816.CrossRef Medline
25. Molliver DC, Snider WD (1997) Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons. J Comp Neurol 381:428-438.CrossRef Medline
26. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457:981-989.CrossRef Medline
27. Oleynikov Y, Singer RH (2003) Real-time visualization of ZBP1 association with /3-actin mRNA during transcription and localization. Curr Biol 13: 199-207. CrossRef Medline
28. O'Reilly LA, Print C, Hausmann G, Moriishi K, Cory S, Huang DC, Strasser A (2001) Tissue expression and subcellular localization of the pro-survival molecule Bcl-w. Cell Death Differ 8:486-494. CrossRef Medline
29. Pan F, Huttelmaier S, Singer RH, Gu W (2007) ZBP2 facilitates binding of ZBP1 to /3-actin mRNA during transcription. Mol Cell Biol 27: 8340-8351.CrossRef Medline
30. Pazyra-Murphy MF, Segal RA (2008) Preparation and maintenance of dor-sal root ganglia neurons in compartmented cultures. J Vis Exp 20.
31. Pazyra-Murphy MF, Hans A, Courchesne SL, Karch C, Cosker KE, Heerssen HM, Watson FL, Kim T, Greenberg ME, Segal RA (2009) A retrograde neuronal survival response: target-derived neurotrophins regulate MEF2D and bcl-w. J Neurosci 29:6700-6709.CrossRef Medline
32. Riccio A, Pierchala BA, Ciarallo CL, Ginty DD (1997) An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons. Science 277:1097-1100.CrossRef Medline
33. Ross AF, Oleynikov Y, Kislauskis EH, Taneja KL, Singer RH (1997) Charac-terization of a /3-actin mRNA zipcode-binding protein. Mol Cell Biol 17:2158-2165.Medline
34. Ross AJ, Waymire KG, Moss JE, Parlow AF, Skinner MK, Russell LD, MacGregor GR (1998) Testicular degeneration in Bclw-deficient mice. Nat Genet 18:251-256.CrossRef Medline
35. Sasaki Y, Vohra BP, Lund FE, Milbrandt J (2009) Nicotinamide mononucle-otide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinu-cleotide. J Neurosci 29:5525-5535.CrossRef Medline
36. Schoenmann Z, Assa-Kunik E, Tiomny S, Minis A, Haklai-Topper L, Arama E, Yaron A (2010) Axonal degeneration is regulated by the apoptotic machinery or a NAD+-sensitive pathway in insects and mammals. J Neu-rosci 30:6375-6386.CrossRef Medline
37. Segal RA (2003) Selectivity in neurotrophin signaling: theme and variations. Annu RevNeurosci 26:299-330.CrossRef Medline
38. Segal RA, Bhattacharyya A, Rua LA, Alberta JA, Stephens RM, Kaplan DR, Stiles CD (1996) Differential utilization of Trk autophosphorylation sites. J Biol Chem 271:20175-20181. CrossRef Medline
39. Silos-Santiago I, Molliver DC, Ozaki S, Smeyne RJ, Fagan AM, Barbacid M, Snider WD (1995) Non-TrkA-expressing small DRG neurons are lost in TrkA deficient mice. J Neurosci 15:5929-5942.Medline
40. Simon DJ, Weimer RM, McLaughlin T, Kallop D, Stanger K, Yang J, O'Leary DD, Hannoush RN, Tessier-Lavigne M (2012) A caspase cascade regu-lated developmental axon degeneration. J Neurosci 32:17540-17553.CrossRef Medline
41. Skaper SD (2012) The neurotrophin family of neurotrophic factors: an overview. Methods Mol Biol 846:1-12.CrossRef Medline
42. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, Jin S, Johnson EF, Marsh KC, Mitten MJ, Nimmer P, Roberts L, Tahir SK, Xiao Y, Yang X, Zhang H, Fesik S, Rosenberg SH, Elmore SW (2008) ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 68:3421-3428.CrossRef Medline
43. Vohra BP, Sasaki Y, Miller BR, Chang J, DiAntonio A, Milbrandt J (2010) Amyloid precursor protein cleavage-dependent and -independent axonal degeneration programs share a common nicotinamide mononucleotide adenylyltransferase 1-sensitive pathway. J Neurosci 30:13729-13738.CrossRef Medline
44. Watson FL, Heerssen HM, Moheban DB, Lin MZ, Sauvageot CM, Bhattacha-ryya A, Pomeroy SL, Segal RA (1999) Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J Neurosci 19:7889-7900. Medline
45. Watson FL, Heerssen HM, Bhattacharyya A, Klesse L, Lin MZ, Segal RA (2001) Neurotrophins use the Erk5 pathway to mediate a retrograde sur-vival response. Nat Neurosci 4:981-988.CrossRef Medline
46. Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, Williams GG, Kendall M, Smith DS, Bassell GJ, Twiss JL (2007) Extracellular stimuli specifically regulate localized levels of individual neuronal mR-NAs. J Cell Biol 178:965-980.CrossRef Medline
47. Willis D, Li KW, Zheng JQ, Chang JH, Smit AB, Kelly T, Merianda TT, Sylvester J, van Minnen J, Twiss JL (2005) Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J Neurosci 25:778-791.CrossRef Medline
48. Yan C, Chen J, Chen D, Minami M, Pei W, Yin XM, Simon RP (2000) Overexpression of the cell death suppressor Bcl-w in ischemic brain: im-plications for a neuroprotective role via the mitochondrial pathway J Cereb Blood Flow Metab 20:620-630. Medline
49. Yan W, Samson M, Jegou B, Toppari J (2000) Bcl-w forms complexes with Bax and Bak, and elevated rations of Bax/Bcl-w and Bak/Bcl-w corre-spond to spermatogonial and spermatocyte apoptosis in the testis. Mol Endocrinol 14:682-699.CrossRef Medline
50. 2+-dependent growth cone guidance. Nat Neurosci 9:1265-1273. CrossRef Medline
51. Yoon BC, Zivraj KH, Holt CE (2009) Local translation and mRNA traffick-ing in axon pathfinding. Results Probl Cell Differ 48:269-288.CrossRef Medline
52. Yoon BC, Jung H, Dwivedy A, O'Hare CM, Zivraj KH, Holt CE (2012) Local translation of extranuclear lamin B promotes axon maintenance. Cell 148:752-764.CrossRef Medline
53. Zeiner GM, Cleary MD, Fouts AE, Meiring CD, Mocarski ES, Boothroyd JC (2008) RNA analysis by biosynthetic tagging using 4-thiouracil and ura-cil phosphoribosyltransferase. Methods Mol Biol 419:135-146.CrossRef Medline
54. Zhang HL, Singer RH, Bassell GJ (1999) Neurotrophin regulation of /3-actin mRNA and protein localization within growth cones. J Cell Biol 147:59-70.CrossRef Medline
55. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ (2001) Neurotrophin-induced transport of a /3-actin mRNP complex increases /3-actin levels and stimulates growth cone motility. Neuron 31:261-275.CrossRef Medline
56. Zivraj KH, Tung YC, Piper M, Gumy L, Fawcett JW, Yeo GS, Holt CE (2010) Subcellular profiling reveals distinct and developmentally regulated rep-ertoire of growth cone mRNAs. J Neurosci 30:15464-15478.CrossRef Medline