Autophagy induced by rapamycin and carbon-starvation have distinct proteome profiles in Aspergillus nidulans

Biotechnology and Bioengineering

Volumn 108, Issue 11, 2011, Pages 2705-2715

  Kim, Yonghyun ^a,b   Islam, Nazrul ^a   Moss, Bill J ^a   Nandakumar, M P ^a   Marten, Mark R ^a  

^a University of Marylandw Baltimore County   (United States)

^b Samsung Medical Center   (South Korea)

Author keywords

Autophagy; Cell wall; Filamentous fungi; Proteomics; Starvation; TOR

Indexed keywords

AUTOPHAGY; CELL WALLS; FILAMENTOUS FUNGI; PROTEOMICS; STARVATION; TOR;

ALDEHYDES; AMINO ACIDS; ASPERGILLUS; BIODEGRADATION; CARBON; CELLS; MOLECULAR BIOLOGY;

PROTEINS;

ALDEHYDE DEHYDROGENASE; ASPARTATE AMINOTRANSFERASE; CARBON; CELL CYCLE PROTEIN 37; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOSIDASE; PHOSPHORYLASE; PROTEIN 14 3 3; PROTEIN N MYRISTOYLTRANSFERASE; PROTEOME; RAPAMYCIN; TARGET OF RAPAMYCIN KINASE; TRYPTOPHAN SYNTHASE;

ARTICLE; ASPERGILLUS NIDULANS; AUTOPHAGY; CARBON SOURCE; CELL SURVIVAL; CONTROLLED STUDY; FUNGAL CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT LIMITATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEOMICS; STARVATION;

ASPERGILLUS NIDULANS; AUTOPHAGY; CARBON; FUNGAL PROTEINS; PROTEOME; SIROLIMUS;

EMERICELLA NIDULANS; FUNGI;

EID: 80053051178     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.23223     Document Type: Article

References (58)

1. Abeliovich H. 2004. Regulation of autophagy by the target of rapamycin (Tor) proteins. In: Klionsky DJ, editor. Autophagy. Georgetown, TX: Landes Bioscience, p. 60-69.
2. Albrecht D, Kniemeyer O, Brakhage AA, Guthke R. 2010. Missing values in gel-based proteomics. Proteomics 10(6): 1202-1211.
3. Bartoszewska M, Kiel JAKW, Bovenberg RAL, Veenhuis M, van der Klei IJ. 2011. Autophagy deficiency promotes β-lactam production in Penicillium chrysogenum Appl Environ Microbiol 77(4): 1413-1422.
4. Bhargava S, Nandakumar MP, Roy A, Wenger KS, Marten MR. 2003a. Pulsed feeding during fed-batch fungal fermentation leads to reduced viscosity without detrimentally affecting protein expression. Biotechnol Bioeng 81(3): 341-347.
5. Bhargava S, Wenger KS, Marten MR. 2003b. Pulsed addition of limiting-carbon during Aspergillus oryzae fermentation leads to improved productivity of a recombinant enzyme. Biotechnol Bioeng 82(1): 111-117.
6. Bhargava S, Wenger KS, Marten MR. 2003c. Pulsed feeding during fed-batch Aspergillus oryzae fermentation leads to improved oxygen mass transfer. Biotechnol Prog 19(3): 1091-1094.
7. Browne SM, Al-Rubeai M. 2011. Analysis of an artificially selected GS-NS0 variant with increased resistance to apoptosis. Biotechnol Bioeng 108(4): 880-892.
8. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG. 2004. Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25(9): 1327-1333.
9. David H, Hofmann G, Oliveira AP, Jarmer H, Nielsen J. 2006. Metabolic network driven analysis of genome-wide transcription data from Aspergillus nidulans Genome Biol 7(11): R108.
10. Dechant R, Peter M. 2008. Nutrient signals driving cell growth. Curr Opin Cell Biol 20(6): 678-687.
11. Dementhon K, Paoletti M, Pinan-Lucarré B, Loubradou-Bourges N, Sabourin M, Saupe SJ, Clavé C. 2003. Rapamycin mimics the incompatibility reaction in the fungus Podospora anserina Eukaryot Cell 2(2): 238-246.
12. Diaz-Troya S, Perez-Perez ME, Florencio FJ, Crespo JL. 2008. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 4(7): 851-865.
13. Eckert SE, Kubler E, Hoffmann B, Braus GH. 2000. The tryptophan synthase-encoding trpB gene of Aspergillus nidulans is regulated by the cross-pathway control system. Mol Gen Genet 263(5): 867-876.
14. Fahien LA, MacDonald MJ. 2002. The succinate mechanism of insulin release. Diabetes 51(9): 2669-2676.
15. Flipphi M, Kocialkowska J, Felenbok B. 2003. Relationships between the ethanol utilization (alc) pathway and unrelated catabolic pathways in Aspergillus nidulans Eur J Biochem 270(17): 3555-3564.
16. Grimm LH, Kelly S, Krull R, Hempel DC. 2005. Morphology and productivity of filamentous fungi. Appl Microbiol Biotechnol 69(4): 375-384.
17. Hawle P, Horst D, Bebelman JP, Yang XX, Siderius M, van der Vies SM. 2007. Cdc37p is required for stress-induced high-osmolarity glycerol and protein kinase C mitogen-activated protein kinase pathway functionality by interaction with Hog1p and Slt2p (Mpk1p). Eukaryot Cell 6(3): 521-532.
18. Herrero J, Valencia A, Dopazo J. 2001. A hierarchical unsupervised growing neural network for clustering gene expression patterns. Bioinformatics 17(2): 126-136.
19. Hill TW, Kafer E. 2001. Improved protocols for Aspergillus minimal medium: Trace element and minimal medium salt stock solutions. Fungal Genet Newsl 48: 20-21.
20. Horgan GW. 2007. Sample size and replication in 2D gel electrophoresis studies. J Proteome Res 6(7): 2884-2887.
21. Ichimura T, Kubota H, Goma T, Mizushima N, Ohsumi Y, Iwago M, Kakiuchi K, Shekhar HU, Shinkawa T, Taoka M, et al. 2004. Transcriptomic and proteomic analysis of a14-3-3 gene-deficient yeast. Biochemistry 43(20): 6149-6158.
22. Johnson DR, Knoll LJ, Levin DE, Gordon JI. 1994. Saccharomyces cerevisiae contains four fatty acid activation (FAA) genes: An assessment of their role in regulating protein N-myristoylation and cellular lipid metabolism. J Cell Biol 127(3): 751-762.
23. Kakiuchi K, Yamauchi Y, Taoka M, Iwago M, Fujita T, Ito T, Song SY, Sakai A, Isobe T, Ichimura T. 2007. Proteomic analysis of in vivo 14-3-3 in teractions in the yeast Saccharomyces cerevisiae Biochemistry 46(26): 7781-7792.
24. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. 2000. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150(6): 1507-1513.
25. Kamada Y, Sekito T, Ohsumi Y. 2004. Autophagy in yeast: A TOR-mediated response to nutrient starvation. Curr Top Microbiol Immunol 279: 73-84.
26. Kaminskyj SGW. 2001. Fundamentals of growth, storage, genetics and microscopy of Aspergillus nidulans Fungal Genet Newsl 48: 25-31.
27. Karp NA, Spencer M, Lindsay H, O'Dell K, Lilley KS. 2005. Impact of replicate types on proteomic expression analysis. J Proteome Res 4(5): 1867-1871.
28. Karp NA, Feret R, Rubtsov DV, Lilley KS. 2008. Comparison of DIGE and post-stained gel electrophoresis with both traditional and SameSpots analysis for quantitative proteomics. Proteomics 8(5): 948-960.
29. Kikuma T, Ohneda M, Arioka M, Kitamoto K. 2006. Functional analysis of the ATG8 homologue Aoatg8 and role of autophagy in differentiation and germination in Aspergillus oryzae Eukaryot Cell 5(8): 1328-1336.
30. Kim Y, Nandakumar MP, Marten MR. 2007. Proteome map of Aspergillus nidulans during osmoadaptation. Fungal Genet Biol 44(9): 886-895.
31. Kim YG, Kim JY, Mohan C, Lee GM. 2009. Effect of Bcl-xL overexpression on apoptosis and autophagy in recombinant Chinese hamster ovary cells under nutrient-deprived condition. Biotechnol Bioeng 103(4): 757-766.
32. Klionsky DJ. 2007. Monitoring autophagy in yeast: The Pho8Delta60 assay. Methods Mol Biol 390: 363-371.
33. Klionsky DJ, Cuervo AM, Seglen PO. 2007. Methods for monitoring autophagy from yeast to human. Autophagy 3(3): 181-206.
34. Kraus PR, Hofmann AF, Harris SD. 2002. Characterization of the Aspergillus nidulans 14-3-3 homologue, ArtA. FEMS Microbiol Lett 210(1): 61-66.
35. Kumarathasan P, Mohottalage S, Goegan P, Vincent R. 2005. An optimized protein in-gel digest method for reliable proteome characterization by MALDI-TOF-MS analysis. Anal Biochem 346(1): 85-89.
36. Mandal AK, Lee P, Chen JA, Nillegoda N, Heller A, DiStasio S, Oen H, Victor J, Nair DM, Brodsky JL, et al. 2007. Cdc37 has distinct roles in protein kinase quality control that protect nascent chains from degradation and promote posttranslational maturation. J Cell Biol 176(3): 319-328.
37. Meijer WH, van der Klei IJ, Veenhuis M, Kiel JA. 2007. ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective cvt and pexophagy pathways also require organism-specific genes. Autophagy 3(2): 106-116.
38. Milewski S, Gabriel I, Olchowy J. 2006. Enzymes of UDP-GlcNAc biosynthesis in yeast. Yeast 23(1): 1-14.
39. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. 2008. Autophagy fights disease through cellular self-digestion. Nature 451(7182): 1069-1075.
40. Muthuvijayan V, Marten MR. 2004. In silico reconstruction of nutrient-sensing signal transduction pathways in Aspergillus nidulans In Silico Biol 4(4): 605-631.
41. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. 2009. Dynamics and diversity in autophagy mechanisms: Lessons from yeast. Nat Rev Mol Cell Biol 10(7): 458-467.
42. Nandakumar MP, Marten MR. 2002. Comparison of lysis methods and preparation protocols for 1-D and 2-D electrophoresis of Aspergillus oryzae intracellular proteins. Electrophoresis 23: 2216-2222.
43. Pinan-Lucarré B, Balguerie A, Clavé C. 2005. Accelerated cell death in Podospora autophagy mutants. Eukaryot Cell 4(11): 1765-1774.
44. Pollack JK. 2009. Study of the morphology and physiology of filamentous fungi during nutrient starvation using the parallel plate flow chamber. PhD Diss. University of Maryland Baltimore County.
45. Pollack JK, Li ZJ, Marten MR. 2008. Fungal mycelia show lag time before re-growth on endogenous carbon. Biotechnol Bioeng 100(3): 458-465.
46. Pollack JK, Harris SD, Marten MR. 2009. Autophagy in filamentous fungi. Fungal Genet Biol 46(1): 1-8.
47. Prick T, Thumm M, Kohrer K, Haussinger D, Vom Dahl S. 2006. In yeast, loss of Hog1 leads to osmosensitivity of autophagy. Biochem J 394(Pt 1): 153-161.
48. Ren M, Santhanam A, Lee P, Caplan A, Garrett S. 2007. Alteration of the protein kinase binding domain enhances function of the Saccharomyces cerevisiae molecular chaperone Cdc37. Eukaryot Cell 6(8): 1363-1372.
49. Richie DL, Fuller KK, Fortwendel J, Miley MD, McCarthy JW, Feldmesser M, Rhodes JC, Askew DS. 2007. Unexpected link between metal ion deficiency and autophagy in Aspergillus fumigatus Eukaryot Cell 6(12): 2437-2447.
50. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al. 2003. TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34(2): 374-378.
51. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. 2007. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26(7): 1749-1760.
52. Scott RC, Juhasz G, Neufeld TP. 2007. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol 17(1): 1-11.
53. Stephan JS, Yeh YY, Ramachandran V, Deminoff SJ, Herman PK. 2009. The Tor and PKA signaling pathways independently target the Atg1/Atg13 protein kinase complex to control autophagy. Proc Natl Acad Sci USA 106(40): 17049-17054.
54. Talbot NJ, Kershaw MJ. 2009. The emerging role of autophagy in plant pathogen attack and host defence. Curr Opin Plant Biol 12(4): 444-450.
55. van Heusden GP, Steensma HY. 2006. Yeast 14-3-3 proteins. Yeast 23(3): 159-171.
56. Wang S-J, Zhong J-J, Shang-Tian Y. 2007. Bioreactor engineering. Bioprocessing for value-added products from renewable resources. Amsterdam: Elsevier, p. 131-161.
57. Yang XX, Hawle P, Bebelman JP, Meenhuis A, Siderius M, van der Vies SM. 2007. Cdc37p is involved in osmoadaptation and controls high osmolarity-induced cross-talk via the MAP kinase Kss1p. FEMS Yeast Res 7(6): 796-807.
58. Zustiak MP, Pollack JK, Marten MR, Betenbaugh MJ. 2008. Feast or famine: Autophagy control and engineering in eukaryotic cell culture. Curr Opin Biotechnol 19(5): 518-526.