Sarm1-mediated axon degeneration requires both SAM and TIR interactions

Journal of Neuroscience

Volumn 33, Issue 33, 2013, Pages 13569-13580

  Gerdts, Josiah ^a   Summers, Daniel W ^a   Sasaki, Yo ^a   DiAntonio, Aaron ^a   Milbrandt, Jeffrey ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CASPASE 3; LENTIVIRUS VECTOR; STERILE ALPHA MOTIF AND ARMADILLO MOTIF CONTAINING PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; FLUORESCENCE MICROSCOPY; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; MOUSE; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MULTIMERIZATION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL GANGLION; WESTERN BLOTTING;

ANIMALS; ARMADILLO DOMAIN PROTEINS; AXONS; CYTOSKELETAL PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GANGLIA, SPINAL; IMMUNOPRECIPITATION; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICROSCOPY, FLUORESCENCE; NERVE DEGENERATION; RECEPTORS, INTERLEUKIN-1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TRANSDUCTION, GENETIC;

EID: 84881495428     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1197-13.2013     Document Type: Article

References (45)

1. Akhouayri I, Turc C, Royet J, Charroux B (2011) Toll-8/Tollo negatively regulates antimicrobial response intheDrosophilarespiratory epithelium. PLoS Pathogens 7:e1002319.
2. Araki T, Sasaki Y, Milbrandt J (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305: 1010-1013.
3. Babetto E, Beirowski B, Russler EV, Milbrandt J, Diantonio A (2013) The Phr1 ubiquitin ligase promotes injury-induced axon self-destruction. Cell Rep 3:1422-1429.
4. Barrientos SA, Martinez NW, Yoo S, Jara JS, Zamorano S, Hetz C, Twiss JL, Alvarez J, Court FA (2011) Axonal degeneration is mediated by the mi-tochondrial permeability transition pore. J Neurosci 31:966-978.
5. Bhattacharya MR, Gerdts J, Naylor SA, Royse EX, Ebstein SY, Sasaki Y, Mil-brandt J, DiAntonio A (2012) A model of toxic neuropathy in Drosoph-ila reveals a role for MORN4 in promoting axonal degeneration. J Neurosci 32:5054-5061.
6. Blum ES, Abraham MC, Yoshimura S, Lu Y, Shaham S (2012) Control of nonapoptotic developmental cell death in Caenorhabditis elegans by a polyglutamine-repeat protein. Science 335:970-973.
7. Carty M, Goodbody R, Schröder M, Stack J, Moynagh PN, Bowie AG (2006) The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat Immunol 7:1074-1081.
8. Chen CY, Lin CW, Chang CY, Jiang ST, Hsueh YP (2011) Sarm1, a negative regulator of innate immunity, interacts with syndecan-2 and regulates neuronal morphology. J Cell Biol 193:769-784.
9. Chen M, Maloney JA, Kallop DY, Atwal JK, Tam SJ, Baer K, Kissel H, Ka-minker JS, Lewcock JW, Weimer RM, Watts RJ (2012) Spatially coordinated kinase signaling regulates local axon degeneration. J Neurosci 32: 13439-13453.
10. Chuang CF, Bargmann CI (2005) A Toll-interleukin 1 repeat protein at the synapse specifies asymmetric odorant receptor expression via ASK1 MAPKKK signaling. Genes Dev 19:270-281.
11. Coleman MP, Freeman MR (2010) Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci 33:245-267.
12. Coleman MP, Conforti L, Buckmaster EA, Tarlton A, Ewing RM, Brown MC, Lyon MF, Perry VH (1998) An 85-kb tandem triplication in the slow Wallerian degeneration (Wlds) mouse. Proc Natl Acad Sci USA 95: 9985-9990.
13. Dasgupta B, Milbrandt J (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci USA 104:7217-7222.
14. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38:D211-D222.
15. Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 147:742-758.
16. Gerdts J, Sasaki Y, Vohra B, Marasa J, Milbrandt J (2011) Image-based screening identifies novel roles for IkB kinase and glycogen synthase ki-nase 3 in axonal degeneration. J Biol Chem 286:28011-28018.
17. Hayakawa T, Kato K, Hayakawa R, Hisamoto N, Matsumoto K, Takeda K, Ichijo H (2011) Regulation of anoxic death in Caenorhabditis elegans by mammalian apoptosis signal-regulating kinase (ASK) family proteins. Genetics 187:785-792.
18. Hunter DA, Moradzadeh A, Whitlock EL, Brenner MJ, Myckatyn TM, Wei CH, Tung TH, Mackinnon SE (2007) Binary imaging analysis for comprehensive quantitative histomorphometry of peripheral nerve. J Neuro-sci Methods 166:116-124.
19. Kammann M, Laufs J, Schell J, Gronenborn B (1989) Rapid insertional mu-tagenesis of DNA by polymerase chain reaction (PCR). Nucleic Acids Res 17:5404.
20. Kim CA, Bowie JU (2003) SAM domains: uniform structure, diversity of function. Trends Biochem Sci 28:625-628.
21. Kim Y, Zhou P, Qian L, Chuang JZ, Lee J, Li C, Iadecola C, Nathan C, Ding A (2007) MyD88-5 links mitochondria, microtubules, and JNK3 in neurons and regulates neuronal survival. JExp Med 204:2063-2074.
22. Komiya T, Mihara K (1996) Protein import into mammalian mitochondria. J Biol Chem 271:22105-22110.
23. Luo L, O'Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127-156.
24. Miller BR, Press C, Daniels RW, Sasaki Y, Milbrandt J, DiAntonio A (2009) A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat Neurosci 12:387-389.
25. Mink M, Fogelgren B, Olszewski K, Maroy P, Csiszar K (2001) A novel human gene (SARM) at chromosome 17q11 encodes a protein with a SAM motif and structural similarity to Armadillo/beta-catenin that is conserved in mouse, Drosophila, and Caenorhabditis elegans. Genomics 74:234-244.
26. Misko AL, Sasaki Y, Tuck E, Milbrandt J, Baloh RH (2012) Mitofusin2 mutations disrupt axonal mitochondrial positioning and promote axon degeneration. J Neurosci 32:4145-4155.
27. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, Hinkle G, Piqani B, Eisenhaure TM, Luo B, Grenier JK, Carpenter AE, Foo SY, Stewart SA, Stockwell BR, Hacohen N, Hahn WC, Lander ES, Sabatini DM, Root DE (2006) A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124:1283-1298.
28. Mukherjee P, Woods TA, Moore RA, Peterson KE (2013) Activation of the innate signaling molecule MAVS by bunyavirus infection upregu-lates the adaptor protein SARM1, leading to neuronal death. Immunity 38:705-716.
29. 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.
30. O'Neill LA, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7:353-364.
31. Osterloh JM, Yang J, Rooney TM, Fox AN, Adalbert R, Powell EH, Sheehan AE, Avery MA, Hackett R, Logan MA, MacDonald JM, Ziegenfuss JS, Milde S, Hou YJ, Nathan C, Ding A, Brown RH Jr, Conforti L, Coleman M, Tessier-Lavigne M, et al. (2012) dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 337:481-484.
32. Panneerselvam P, Singh LP, Ho B, Chen J, Ding JL (2012) Targeting of pro-apoptotic TLR adaptor SARM to mitochondria: definition of the critical region and residues in the signal sequence. Biochem J 442:263-271.
33. Panneerselvam P, Singh LP, Selvarajan V, Chng WJ, Ng SB, Tan NS, Ho B, Chen J, Ding JL (2013) T-cell death following immune activation is mediated by mitochondria-localized SARM. Cell Death Differ 20:478-489.
34. Qiao F, Bowie JU (2005) The many faces of SAM. Sci STKE STKE 2005:re7.
35. Sasaki Y, Vohra BP, Lund FE, Milbrandt J (2009a) Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. JNeurosci 29:5525-5535.
36. Sasaki Y, Vohra BP, Baloh RH, Milbrandt J (2009b) Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration in vivo. J Neurosci 29:6526-6534.
37. Saxena S, Caroni P (2007) Mechanisms of axon degeneration: from development to disease. Prog Neurobiol 83:174-191.
38. 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 Neurosci 30:6375-6386.
39. Simon DJ, Weimer RM, McLaughlin T, Kallop D, Stanger K, Yang J, O'Leary DD, Hannoush RN, Tessier-Lavigne M (2012) A caspase cascade regulating developmental axon degeneration. J Neurosci 32:17540-17553.
40. Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698-702.
41. Szretter KJ, Samuel MA, Gilfillan S, Fuchs A, Colonna M, Diamond MS (2009) The immune adaptor molecule SARM modulates tumor necrosis factor alpha production and microglia activation in the brainstem and restricts West Nile Virus pathogenesis. J Virol 83:9329-9338.
42. 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.
43. Wakatsuki S, Saitoh F, Araki T (2011) ZNRF1 promotes Wallerian degeneration by degrading AKT to induce GSK3B-dependent CRMP2 phosphorylation. Nat Cell Biol 13:1415-1423.
44. Wang JT, Medress ZA, Barres BA (2012) Axon degeneration: molecular mechanisms of a self-destruction pathway. J Cell Biol 196:7-18.
45. Wang MS, Davis AA, Culver DG, Wang Q, Powers JC, Glass JD (2004) Cal-pain inhibition protects against Taxol-induced sensory neuropathy. Brain 127:671-679.