Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 10, 2011, Pages 3982-3987

  Bounoutas, Alexander ^a,c   Kratz, John ^a   Emtage, Lesley ^a,d   Ma, Charles ^a,e   Nguyen, Ken C ^b   Chalfie, Martin ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d RUTGERS UNIVERSITY   (United States)

^e PhalanxBio Inc   (United States)

Author keywords

Gene regulation; Kinase

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; GENE EXPRESSION; MICROTUBULE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; TOUCH RECEPTOR NEURON;

ANIMALS; CAENORHABDITIS ELEGANS; COLCHICINE; GENE EXPRESSION; MICROTUBULES; MUTATION; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES;

CAENORHABDITIS ELEGANS;

EID: 79952764695     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1101360108     Document Type: Article

References (56)

1. Alberts B, et al. (2002) Molecular Biology of the Cell (Garland, New York), 4th Ed.
2. Conde C, Cáceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319-332.
3. Janmey PA (1998) The cytoskeleton and cell signaling: Component localization and mechanical coupling. Physiol Rev 78:763-781.
4. Chalfie M, Sulston J (1981) Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 82:358-370.
5. Chalfie M, Thomson JN (1979) Organization of neuronal microtubules in the nematode Caenorhabditis elegans. J Cell Biol 82:278-289. (Pubitemid 9224602)
6. Chalfie M, Thomson JN (1982) Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans. J Cell Biol 93:15-23. (Pubitemid 12117036)
7. Savage C, et al. (1989) mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev 3:870-881.
8. Chalfie M, Au M (1989) Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243:1027-1033. (Pubitemid 19072579)
9. Fukushige T, et al. (1999) MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J Cell Sci 112:395-403. (Pubitemid 29080661)
10. Bounoutas A, O'Hagan R, Chalfie M (2009) Touch sensitivity in Caenorhabditis elegans. Curr Biol 19:1362-1367.
11. Bounoutas A, Zheng Q, Nonet ML, Chalfie M (2009) The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation. Genetics 183:607-617, 601SI-604SI.
12. Nakata K, et al. (2005) Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120:407-420. (Pubitemid 40222434)
13. Grill B, et al. (2007) C. elegans RPM-1 regulates axon termination and synaptogenesis through the Rab GEF GLO-4 and the Rab GTPase GLO-1. Neuron 55:587-601. (Pubitemid 47223638)
14. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M (2009) Axon regeneration requires a conserved MAP kinase pathway. Science 323:802-806.
15. Way JC, Chalfie M (1989) The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev 3(12A):1823-1833. (Pubitemid 20023210)
16. Zhang Y, et al. (2002) Identification of genes expressed in C. elegans touch receptor neurons. Nature 418:331-335. (Pubitemid 34790684)
17. Duggan A, Ma C, Chalfie M(1998) Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 125:4107-4119. (Pubitemid 28515448)
18. O'Hagan R, Chalfie M, Goodman MB (2005) The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat Neurosci 8:43-50. (Pubitemid 41236730)
19. Gu G (1998) A Molecular Model of Mechanosensory Transduction in Caenorhabditis elegans in Department of Biological Sciences (Columbia Univ Press, New York).
20. Huang M, Gu G, Ferguson EL, Chalfie M (1995) A stomatin-like protein necessary for mechanosensation in C. elegans. Nature 378:292-295.
21. Zhang S, et al. (2004) MEC-2 is recruited to the putative mechanosensory complex in C. elegans touch receptor neurons through its stomatin-like domain. Curr Biol 14:1888-1896. (Pubitemid 39464811)
22. Altun-Gultekin Z, et al. (2001) A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128:1951-1969. (Pubitemid 32600460)
23. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263:802-805. (Pubitemid 24093206)
24. Poyurovsky MV, et al. (2003) Nucleotide binding by the Mdm2 RING domain facilitates Arf-independent Mdm2 nucleolar localization. Mol Cell 12:875-887. (Pubitemid 37352781)
25. Fang S, Jensen JP, Ludwig RL, Vousden KH, Weissman AM (2000) Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J Biol Chem 275:8945-8951. (Pubitemid 30180252)
26. Mishra L, et al. (1997) Praja1, a novel gene encoding a RING-H2 motif in mouse development. Oncogene 15:2361-2368. (Pubitemid 27496986)
27. Ramji DP, Foka P (2002) CCAAT/enhancer-binding proteins: Structure, function and regulation. Biochem J 365:561-575. (Pubitemid 34864439)
28. Robitaille H, Proulx R, Robitaille K, Blouin R, Germain L (2005) The mitogen-activated protein kinase kinase kinase dual leucine zipper-bearing kinase (DLK) acts as a key regulator of keratinocyte terminal differentiation. J Biol Chem 280:12732-12741.
29. Hirai S, et al. (2002) MAPK-upstream protein kinase (MUK) regulates the radial migration of immature neurons in telencephalon of mouse embryo. Development 129:4483-4495. (Pubitemid 35203731)
30. Hirai S, et al. (2006) The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex. J Neurosci 26:11992-12002. (Pubitemid 44772110)
31. Eto K, Kawauchi T, Osawa M, Tabata H, Nakajima K (2010) Role of dual leucine zipper-bearing kinase (DLK/MUK/ZPK) in axonal growth. Neurosci Res 66:37-45.
32. Hébert SS, et al. (2000) The mixed lineage kinase DLK is oligomerized by tissue transglutaminase during apoptosis. J Biol Chem 275:32482-32490.
33. Oetjen E, et al. (2006) Inhibition of membrane depolarisation-induced transcriptional activity of cyclic AMP response element binding protein (CREB) by the dual-leucine-zipper-bearing kinase in a pancreatic islet beta cell line. Diabetologia 49:332-342. (Pubitemid 43185402)
34. Hirai S, Izawa M, Osada S, Spyrou G, Ohno S (1996) Activation of the JNK pathway by distantly related protein kinases, MEKK and MUK. Oncogene 12:641-650. (Pubitemid 26059659)
35. Yan D, Wu Z, Chisholm AD, Jin Y (2009) The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138:1005-1018.
36. Lehner B, et al. (2006) Loss of LIN-35, the Caenorhabditis elegans ortholog of the tumor suppressor p105Rb, results in enhanced RNA interference. Genome Biol 7:R4.
37. Chang L, Jones Y, Ellisman MH, Goldstein LS, Karin M (2003) JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4:521-533. (Pubitemid 36437559)
38. Lewcock JW, Genoud N, Lettieri K, Pfaff SL (2007) The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56:604-620. (Pubitemid 350102027)
39. Dong C, Li Z, Alvarez R, Jr., Feng XH, Goldschmidt-Clermont PJ (2000) Microtubule binding to Smads may regulate TGF beta activity. Mol Cell 5:27-34. (Pubitemid 30105433)
40. Gordon-Weeks PR (2004) Microtubules and growth cone function. J Neurobiol 58:70-83.
41. Roos J, Hummel T, Ng N, Klämbt C, Davis GW (2000) Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26:371-382.
42. Erez H, et al. (2007) Formation of microtubule-based traps controls the sorting and concentration of vesicles to restricted sites of regenerating neurons after axotomy. J Cell Biol 176:497-507.
43. Whitmarsh AJ (2010) A central role for p38 MAPK in the early transcriptional response to stress. BMC Biol 8:47.
44. Metz R, Ziff E (1991) cAMP stimulates the C/EBP-related transcription factor rNFIL-6 to trans-locate to the nucleus and induce c-fos transcription. Genes Dev 5:1754-1766. (Pubitemid 121000007)
45. Sung YJ, Povelones M, Ambron RT (2001) RISK-1: A novel MAPK homologue in axoplasm that is activated and retrogradely transported after nerve injury. J Neurobiol 47:67-79. (Pubitemid 32240154)
46. Wang TH, et al. (1998) Microtubule-associated protein tau in development, degeneration and protection of neurons. J Biol Chem 273:4928-4936.
47. Stone AA, Chambers TC (2000) Microtubule inhibitors elicit differential effects on MAP kinase (JNK, ERK, and p38) signaling pathways in human KB-3 carcinoma cells. Exp Cell Res 254:110-119. (Pubitemid 30066737)
48. Yang Y, Zhu X, Chen Y, Wang X, Chen R (2007) p38 and JNK MAPK, but not ERK1/2 MAPK, play important role in colchicine-induced cortical neurons apoptosis. Eur J Pharmacol 576:26-33. (Pubitemid 47588251)
49. Kyriakis JM, Avruch J (2001) Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807-869. (Pubitemid 32267078)
50. Bray D, Thomas C, Shaw G (1978) Growth cone formation in cultures of sensory neurons. Proc Natl Acad Sci USA 75:5226-5229. (Pubitemid 9055276)
51. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
52. Savage C, et al. (1994) Mutations in the Caenorhabditis elegans beta-tubulin gene mec-7: Effects on microtubule assembly and stability and on tubulin autoregulation. J Cell Sci 107:2165-2175. (Pubitemid 24273483)
53. Calixto A, Chelur D, Topalidou I, Chen X, Chalfie M (2010) Enhanced neuronal RNAi in C. elegans using SID-1. Nat Methods 7:554-559.
54. Zhang S (2004) Stomatin Gene Family in Caenorhabditis elegans in Biological Sciences (Columbia Univ Press, New York), p 158.
55. Mello C, Fire A (1995) DNA transformation. Methods Cell Biol 48:451-482.
56. Hall DH (1995) Electron Microscopy and Three-Dimensional Image Reconstruction in Caenorhabditis elegans: Modern Biological Analysis of an Organism (Academic, New York), pp 394-436.