Integrin-linked kinase modulates longevity and thermotolerance in C. elegans through neuronal control of HSF-1

Aging Cell

Volumn 13, Issue 3, 2014, Pages 419-430

  Kumsta, Caroline ^a   Ching, Tsui Ting ^b,d   Nishimura, Mayuko ^a   Davis, Andrew E ^a   Gelino, Sara ^a   Catan, Hannah H ^a   Yu, Xiaokun ^b   Chu, Chu Chiao ^a   Ong, Binnan ^a   Panowski, Siler H ^c   Baird, Nathan ^c   Bodmer, Rolf ^a   Hsu, Ao Lin ^b   Hansen, Malene ^a  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Aging; C. elegans; Heat shock response; HSF 1; Integrin signaling; PAT 4 ILK

Indexed keywords

HEAT SHOCK TRANSCRIPTION FACTOR 1; INTEGRIN LINKED KINASE; CAENORHABDITIS ELEGANS PROTEIN; HEAT SHOCK FACTOR-1, C ELEGANS; INTEGRIN-LINKED KINASE; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTION FACTOR;

ADULT; ARTICLE; CAENORHABDITIS ELEGANS; CELL FUNCTION; CONTROLLED STUDY; DIET RESTRICTION; DROSOPHILA MELANOGASTER; EXTRACELLULAR MATRIX; FOOD INTAKE; GEL MOBILITY SHIFT ASSAY; HEAT SHOCK RESPONSE; HEAT TOLERANCE; HETEROZYGOTE; LIFE EXTENSION; LONGEVITY; MUSCLE FUNCTION; NEURONAL CONTROL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; STRESS; ANIMAL; GENETICS; METABOLISM; PHYSIOLOGY;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; HEAT-SHOCK RESPONSE; LONGEVITY; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84901477904     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12189     Document Type: Article

References (41)

1. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
2. Chiang WC, Ching TT, Lee HC, Mousigian C, Hsu AL (2012) HSF-1 regulators DDL-1/2 link insulin-like signaling to heat-shock responses and modulation of longevity. Cell 148, 322-334.
3. Curran SP, Ruvkun G (2007) Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet. 3, e56.
4. Dupuy D, Bertin N, Hidalgo CA, Venkatesan K, Tu D, Lee D, Rosenberg J, Svrzikapa N, Blanc A, Carnec A, Carvunis AR, Pulak R, Shingles J, Reece-Hoyes J, Hunt-Newbury R, Viveiros R, Mohler WA, Tasan M, Roth FP, Le Peuch C, Hope IA, Johnsen R, Moerman DG, Barabasi AL, Baillie D, Vidal M (2007) Genome-scale analysis of in vivo spatiotemporal promoter activity in Caenorhabditis elegans. Nat. Biotechnol. 25, 663-668.
5. Fisher BR, Heredia DJ, Brown KM (1996) Heat-induced alterations in embryonic cytoskeletal and stress proteins precede somite malformations in rat embryos. Teratog. Carcinog. Mutagen. 16, 49-64.
6. Goddeeris MM, Cook-Wiens E, Horton WJ, Wolf H, Stoltzfus JR, Borrusch M, Grotewiel MS (2003) Delayed behavioural aging and altered mortality in Drosophila beta integrin mutants. Aging Cell 2, 257-264.
7. GuhaThakurta D, Palomar L, Stormo GD, Tedesco P, Johnson TE, Walker DW, Lithgow G, Kim S, Link CD (2002) Identification of a novel cis-regulatory element involved in the heat shock response in Caenorhabditis elegans using microarray gene expression and computational methods. Genome Res. 12, 701-712.
8. Hansen M, Hsu AL, Dillin A, Kenyon C (2005) New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet. 1, 119-128.
9. Hansen M, Taubert S, Crawford D, Libina N, Lee SJ, Kenyon C (2007) Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6, 95-110.
10. Hsu AL, Murphy CT, Kenyon C (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300, 1142-1145.
11. Jensen LT, Moller TH, Larsen SA, Jakobsen H, Olsen A (2012) A new role for laminins as modulators of protein toxicity in Caenorhabditis elegans. Aging Cell 11, 82-92.
12. Jeong DE, Artan M, Seo K, Lee SJ (2012) Regulation of lifespan by chemosensory and thermosensory systems: findings in invertebrates and their implications in mammalian aging. Front Genet. 3, 218.
13. Johnson TE, de Castro E, Hegi de Castro S, Cypser J, Henderson S, Tedesco P (2001) Relationship between increased longevity and stress resistance as assessed through gerontogene mutations in Caenorhabditis elegans. Exp. Gerontol. 36, 1609-1617.
14. Knoll R, Postel R, Wang J, Kratzner R, Hennecke G, Vacaru AM, Vakeel P, Schubert C, Murthy K, Rana BK, Kube D, Knoll G, Schafer K, Hayashi T, Holm T, Kimura A, Schork N, Toliat MR, Nurnberg P, Schultheiss HP, Schaper W, Schaper J, Bos E, Den Hertog J, van Eeden FJ, Peters PJ, Hasenfuss G, Chien KR, Bakkers J (2007) Laminin-alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation 116, 515-525.
15. Lange A, Wickstrom SA, Jakobson M, Zent R, Sainio K, Fassler R (2009) Integrin-linked kinase is an adaptor with essential functions during mouse development. Nature 461, 1002-1006.
16. Lapierre LR, De Magalhaes Filho CD, McQuary PR, Chu CC, Visvikis O, Chang JT, Gelino S, Ong B, Davis AE, Irazoqui JE, Dillin A, Hansen M (2013) The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans. Nat Commun. 4, 2267.
17. Libina N, Berman JR, Kenyon C (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115, 489-502.
18. Link CD, Johnson CJ (2002) Reporter transgenes for study of oxidant stress in Caenorhabditis elegans. Methods Enzymol. 353, 497-505.
19. Mackinnon AC, Qadota H, Norman KR, Moerman DG, Williams BD (2002) C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr. Biol. 12, 787-797.
20. Mair W, Dillin A (2008) Aging and survival: the genetics of life span extension by dietary restriction. Annu. Rev. Biochem. 77, 727-754.
21. Mathur SK, Sistonen L, Brown IR, Murphy SP, Sarge KD, Morimoto RI (1994) Deficient induction of human hsp70 heat shock gene transcription in Y79 retinoblastoma cells despite activation of heat shock factor 1. Proc. Natl Acad. Sci. USA 91, 8695-8699.
22. McDonald PC, Fielding AB, Dedhar S (2008) Integrin-linked kinase-essential roles in physiology and cancer biology. J. Cell Sci. 121, 3121-3132.
23. Meissner B, Warner A, Wong K, Dube N, Lorch A, McKay SJ, Khattra J, Rogalski T, Somasiri A, Chaudhry I, Fox RM, Miller DM 3rd, Baillie DL, Holt RA, Jones SJ, Marra MA, Moerman DG (2009) An integrated strategy to study muscle development and myofilament structure in Caenorhabditis elegans. PLoS Genet. 5, e1000537.
24. Mendenhall AR, Tedesco PM, Taylor LD, Lowe A, Cypser JR, Johnson TE (2012) Expression of a single-copy hsp-16.2 reporter predicts life span. J. Gerontol. A Biol. Sci. Med. Sci. 67, 726-733.
25. Mori I, Ohshima Y (1995) Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376, 344-348.
26. Nishimura M, Kumsta C, Kaushik G, Diop S, Ding Y, Bisharat-Kernizan J, Catan H, Ross R, Engler A, Bodmer R, Hansen M, Ocorr K (2014) Dual role of β1-integrin and integrin-linked kinase in modulating cardiac aging. Aging Cell, in press.
27. Postel R, Vakeel P, Topczewski J, Knoll R, Bakkers J (2008) Zebrafish integrin-linked kinase is required in skeletal muscles for strengthening the integrin-ECM adhesion complex. Dev. biol. 318, 92-101.
28. Prahlad V, Morimoto RI (2011) Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins. Proc. Natl Acad. Sci. USA 108, 14204-14209.
29. Prahlad V, Cornelius T, Morimoto RI (2008) Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320, 811-814.
30. Qin J, Wu C (2012) ILK: a pseudokinase in the center stage of cell-matrix adhesion and signaling. Curr. Opin. Cell Biol. 24, 607-613.
31. Radovanac K, Morgner J, Schulz JN, Blumbach K, Patterson C, Geiger T, Mann M, Krieg T, Eckes B, Fassler R, Wickstrom SA (2013) Stabilization of integrin-linked kinase by the Hsp90-CHIP axis impacts cellular force generation, migration and the fibrotic response. EMBO J. 32, 1409-1424.
32. Santagata S, Hu R, Lin NU, Mendillo ML, Collins LC, Hankinson SE, Schnitt SJ, Whitesell L, Tamimi RM, Lindquist S, Ince TA (2011) High levels of nuclear heat-shock factor 1 (HSF1) are associated with poor prognosis in breast cancer. Proc. Natl Acad. Sci. USA 108, 18378-18383.
33. Tatar M, Khazaeli AA, Curtsinger JW (1997) Chaperoning extended life. Nature 390, 30.
34. Voellmy R (2004) On mechanisms that control heat shock transcription factor activity in metazoan cells. Cell Stress Chaperones 9, 122-133.
35. Walker GA, Lithgow GJ (2003) Lifespan extension in C. elegans by a molecular chaperone dependent upon insulin-like signals. Aging Cell 2, 131-139.
36. Walter MF, Petersen NS, Biessmann H (1990) Heat shock causes the collapse of the intermediate filament cytoskeleton in Drosophila embryos. Dev. Genet. 11, 270-279.
37. Williams BD, Waterston RH (1994) Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J. Cell Biol. 124, 475-490.
38. Winston WM, Molodowitch C, Hunter CP (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295, 2456-2459.
39. Wu C, Dedhar S (2001) Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J. Cell Biol. 155, 505-510.
40. Xavier IJ, Mercier PA, McLoughlin CM, Ali A, Woodgett JR, Ovsenek N (2000) Glycogen synthase kinase 3beta negatively regulates both DNA-binding and transcriptional activities of heat shock factor 1. J. Biol. Chem. 275, 29147-29152.
41. Zervas CG, Gregory SL, Brown NH (2001) Drosophila integrin-linked kinase is required at sites of integrin adhesion to link the cytoskeleton to the plasma membrane. J. Cell Biol. 152, 1007-1018.