A microscopy-based screen employing multiplex genome sequencing identifies cargo-specific requirements for dynein velocity

Molecular Biology of the Cell

Volumn 25, Issue 5, 2014, Pages 669-678

  Tan, Kaeling ^a   Roberts, Anthony J ^a,b   Chonofsky, Mark ^a   Egan, Martin J ^a   Reck Peterson, Samara L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC DYNEIN; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN 1; ARP1 PROTEIN, ASPERGILLUS FUMAGATUS; FUNGAL PROTEIN; HYDROLYASE; KINESIN; MICROTUBULE ASSOCIATED PROTEIN;

ARTICLE; EMERICELLA NIDULANS; ENDOSOME; EUKARYOTIC CELL; FLUORESCENCE MICROSCOPY; GENOME; IN VITRO STUDY; INTRACELLULAR TRANSPORT; MACROMOLECULE; MICROTUBULE; MOTOR PERFORMANCE; MUTATION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; SCREENING; ASPERGILLUS NIDULANS; CELL ORGANELLE; GENETICS; METABOLISM; PHYSIOLOGY; TEMPERATURE; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

ASPERGILLUS NIDULANS; BIOLOGICAL TRANSPORT; CYTOPLASMIC DYNEINS; DYNEINS; FUNGAL PROTEINS; HYDRO-LYASES; KINESIN; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; ORGANELLES; PEROXISOMES; TEMPERATURE;

EID: 84896859482     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-09-0557     Document Type: Article

References (59)

1. Abenza JF, Pantazopoulou A, Rodriguez JM, Galindo A, Penalva MA (2009). Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 10, 57-75.
2. Bailleul B, Daubersies P, Galiegue-Zouitina S, Loucheux-Lefebvre MH (1989). Molecular basis of 4-nitroquinoline 1-oxide carcinogenesis. Jpn J Cancer Res 80, 691-697. (Pubitemid 20023036)
3. Barbour L, Hanna M, Xiao W (2006). Mutagenesis. In: Yeast Protocols, ed. W Xiao, Totowa, NJ: Humana Press, 121-127.
4. Cho C, Reck-Peterson SL, Vale RD (2008). Regulatory ATPase sites of cytoplasmic dynein affect processivity and force generation. J Biol Chem 283, 25839-25845.
5. Eckley DM, Gill SR, Melkonian KA, Bingham JB, Goodson HV, Heuser JE, Schroer TA (1999). Analysis of dynactin subcomplexes reveals a novel actin-related protein associated with the arp1 minifilament pointed end. J Cell Biol 147, 307-320.
6. Egan MJ, McClintock MA, Reck-Peterson SL (2012a). Microtubule-based transport in filamentous fungi. Curr Opin Microbiol 15, 637-645.
7. Egan MJ, Tan K, Reck-Peterson SL (2012b). Lis1 is an initiation factor for dynein-driven organelle transport. J Cell Biol 197, 971-982.
8. Erzberger JP, Berger JM (2006). Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu Rev Biophys Biomol Struct 35, 93-114. (Pubitemid 43877371)
9. Fernandez-Abalos JM, Fox H, Pitt C, Wells B, Doonan JH (1998). Plant-adapted green fluorescent protein is a versatile vital reporter for gene expression, protein localization and mitosis in the filamentous fungus, Aspergillus nidulans. Mol Microbiol 27, 121-130. (Pubitemid 28022582)
10. Galagan J et al. (2005). Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438, 1105-1115. (Pubitemid 41831674)
11. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO (2009). Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6, 343-345.
12. Hammer JA 3rd, Sellers JR (2012). Walking to work: roles for class V myosins as cargo transporters. Nat Rev. Mol Cell Biol 13, 13-26.
13. Hendricks AG, Lazarus JE, Perlson E, Gardner MK, Odde DJ, Goldman YE, Holzbaur EL (2012). Dynein tethers and stabilizes dynamic microtubule plus ends. Curr Biol 22, 632-637.
14. Horio T, Oakley B (2005). The role of microtubules in rapid hyphal tip growth of Aspergillus nidulans. Mol Biol Cell 16, 918-926. (Pubitemid 40165582)
15. Huang J, Roberts AJ, Leschziner AE, Reck-Peterson SL (2012). Lis1 acts as a "clutch" between the ATPase and microtubule-binding domains of the dynein motor. Cell 150, 975-986.
16. Ikenaga M, Ishii Y, Tada M, Kakunaga T, Takebe H (1975). Excision-repair of 4-nitroquinolin-1-oxide damage responsible for killing, mutation, and cancer. Basic Life Sci 5B, 763-771.
17. Imamula K, Kon T, Ohkura R, Sutoh K (2007). The coordination of cyclic microtubule association/dissociation and tail swing of cytoplasmic dynein. Proc Natl Acad Sci USA 104, 16134-16139. (Pubitemid 350099374)
18. Kon T, Nishiura M, Ohkura R, Toyoshima YY, Sutoh K (2004). Distinct functions of nucleotide-binding/hydrolysis sites in the four AAA modules of cytoplasmic dynein. Biochemistry 43, 11266-11274. (Pubitemid 39180370)
19. Laan L, Pavin N, Husson J, Romet-Lemonne G, van Duijn M, Lopez MP, Vale RD, Julicher F, Reck-Peterson SL, Dogterom M (2012). Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters. Cell 148, 502-514.
20. Lee IH, Kumar S, Plamann M (2001). Null mutants of the Neurospora actin-related protein 1 pointed-end complex show distinct phenotypes. Mol Biol Cell 12, 2195-2206. (Pubitemid 33049709)
21. Lee SB, Taylor JW (1990). Isolation of DNA from fungal mycelia and single spores. In: PCR Protocols: A Guide to Methods and Applications, ed. DGM Innis, J Sninsky, and T White, Orlando, FL: Academic Press, 282-287.
22. Lefrancois P, Euskirchen GM, Auerbach RK, Rozowsky J, Gibson T, Yellman CM, Gerstein M, Snyder M (2009). Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genomics 10, 37.
23. Lenz JH, Schuchardt I, Straube A, Steinberg G (2006). A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J 25, 2275-2286. (Pubitemid 44012211)
24. Li H, Durbin R (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760.
25. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079.
26. Ligon LA, Karki S, Tokito M, Holzbaur EL (2001). Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nat Cell Biol 3, 913-917.
27. Malone CJ, Misner L, Le Bot N, Tsai MC, Campbell JM, Ahringer J, White JG (2003). The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115, 825-836. (Pubitemid 38058495)
28. McKenna A et al. (2010). The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20, 1297-1303.
29. Meyer M, Stenzel U, Myles S, Prufer K, Hofreiter M (2007). Targeted high-throughput sequencing of tagged nucleic acid samples. Nucleic Acids Res 35, e97.
30. Moore JK, Stuchell-Brereton MD, Cooper JA (2009). Function of dynein in budding yeast: mitotic spindle positioning in a polarized cell. Cell Motil Cytoskeleton 66, 546-555.
31. Morris NR (1975). Mitotic mutants of Aspergillus nidulans. Genet Res 26, 237-254.
32. Muller J, Oma Y, Vallar L, Friederich E, Poch O, Winsor B (2005). Sequence and comparative genomic analysis of actin-related proteins. Mol Biol Cell 16, 5736-5748. (Pubitemid 41752222)
33. Murakami K, Yasunaga T, Noguchi TQ, Gomibuchi Y, Ngo KX, Uyeda TQ, Wakabayashi T (2010). Structural basis for actin assembly, activation of ATP hydrolysis, and delayed phosphate release. Cell 143, 275-287.
34. Nayak T, Szewczyk E, Oakley CE, Osmani A, Ukil L, Murray SL, Hynes MJ, Osmani S, Oakley B (2006). A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172, 1557-1566.
35. Orr-Weaver TL, Szostak JW, Rothstein RJ (1983). Genetic applications of yeast transformation with linear and gapped plasmids. Methods Enzymol 101, 228-245. (Pubitemid 13071049)
36. Perlson E, Hendricks AG, Lazarus JE, Ben-Yaakov K, Gradus T, Tokito M, Holzbaur EL (2013). Dynein interacts with the neural cell adhesion molecule (NCAM180) to tether dynamic microtubules and maintain synaptic density in cortical neurons. J Biol Chem 288, 27812-27824.
37. Qiu W, Derr ND, Goodman BS, Villa E, Wu D, Shih W, Reck-Peterson SL (2012). Dynein achieves processive motion using both stochastic and coordinated stepping. Nat Struct Mol Biol 19, 193-200.
38. Reck-Peterson SL, Yildiz A, Carter AP, Gennerich A, Zhang N, Vale RD (2006). Single-molecule analysis of dynein processivity and stepping behavior. Cell 126, 335-348. (Pubitemid 44092968)
39. Requena N, Alberti-Segui C, Winzenburg E, Horn C, Schliwa M, Philippsen P, Liese R, Fischer R (2001). Genetic evidence for a microtubule-destabilizing effect of conventional kinesin and analysis of its consequences for the control of nuclear distribution in Aspergillus nidulans. Mol Microbiol 42, 121-132. (Pubitemid 34212166)
40. Schafer DA, Gill SR, Cooper JA, Heuser JE, Schroer TA (1994). Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin. J Cell Biol 126, 403-412. (Pubitemid 24226256)
41. Schmidt H, Gleave ES, Carter AP (2012). Insights into dynein motor domain function from a 3.3-A crystal structure. Nat Struct Mol Biol 19, 492-497, S1.
42. Seidel C, Moreno-Velasquez SD, Riquelme M, Fischer R (2013). Neurospora crassa NKIN2, a kinesin-3 motor, transports early endosomes and is required for polarized growth. Eukaryot Cell 12, 1020-1032.
43. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22, 1567-1572. (Pubitemid 40039460)
44. Sivagurunathan S, Schnittker RR, Razafsky DS, Nandini S, Plamann MD, King SJ (2012). Analyses of dynein heavy chain mutations reveal complex interactions between dynein motor domains and cellular dynein functions. Genetics 191, 1157-1179.
45. Subach OM, Gundorov IS, Yoshimura M, Subach FV, Zhang J, Gruenwald D, Souslova EA, Chudakov DM, Verkhusha VV (2008). Conversion of red fluorescent protein into a bright blue probe. Chem Biol 15, 1116-1124.
46. Szewczyk E, Nayak T, Oakley CE, Edgerton H, Xiong Y, Taheri-Talesh N, Osmani S, Oakley B, Oakley B (2006). Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 1, 3111-3120.
47. Taheri-Talesh N, Horio T, Araujo-Bazán L, Dou X, Espeso EA, Peñalva M, Osmani S, Oakley B (2008). The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell 19, 1439-1449. (Pubitemid 351805098)
48. Todd RB, Davis MA, Hynes MJ (2007a). Genetic manipulation of Aspergillus nidulans: heterokaryons and diploids for dominance, complementation and haploidization analyses. Nat Protoc 2, 822-830. (Pubitemid 46745579)
49. Todd RB, Davis MA, Hynes MJ (2007b). Genetic manipulation of Aspergillus nidulans: meiotic progeny for genetic analysis and strain construction. Nat Protoc 2, 811-821. (Pubitemid 46745578)
50. Vogel SK, Pavin N, Maghelli N, Julicher F, Tolic-Norrelykke IM (2009). Self-organization of dynein motors generates meiotic nuclear oscillations. PLoS Biol 7, e1000087.
51. Wong KH, Jin Y, Moqtaderi Z (2013). Multiplex Illumina sequencing using DNA barcoding. Curr Protoc Mol Biol Chapter 7, Unit 7.11.
52. Wortman JR et al. (2009). The 2008 update of the Aspergillus nidulans genome annotation: a community effort. Fungal Genet Biol 46 (Suppl 1), S2-S13.
53. Xiang X, Beckwith SM, Morris NR (1994). Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans. Proc Natl Acad Sci USA 91, 2100-2104. (Pubitemid 24092050)
54. Xiang X, Osmani AH, Osmani SA, Xin M, Morris NR (1995). NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol Biol Cell 6, 297-310.
55. Xiang X, Zuo W, Efimov VP, Morris NR (1999). Isolation of a new set of Aspergillus nidulans mutants defective in nuclear migration. Curr Genet 35, 626-630. (Pubitemid 29366579)
56. Yeh TY, Quintyne NJ, Scipioni BR, Eckley DM, Schroer TA (2012). Dynactin's pointed-end complex is a cargo-targeting module. Mol Biol Cell 23, 3827-3837.
57. Zhang J, Li S, Fischer R, Xiang X (2003). Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol Biol Cell 14, 1479-1488. (Pubitemid 36547416)
58. Zhang J, Yao X, Fischer L, Abenza JF, Penalva MA, Xiang X (2011). The p25 subunit of the dynactin complex is required for dynein-early endosome interaction. J Cell Biol 193, 1245-1255.
59. Zhang J, Zhuang L, Lee Y, Abenza JF, Penalva MA, Xiang X (2010). The microtubule plus-end localization of Aspergillus dynein is important for dynein-early-endosome interaction but not for dynein ATPase activation. J Cell Sci 123, 3596-3604.