Spaceflight engages heat shock protein and other molecular chaperone genes in tissue culture cells of Arabidopsis Thaliana

American Journal of Botany

Volumn 100, Issue 1, 2013, Pages 235-248

  Zupanska, Agata K ^a   Denison, Fiona C ^a   Ferl, Robert J ^a   Paul, Anna Lisa ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Arabidopsis thaliana; Brassicaceae; Gravity; Heat shock proteins; Hsp gene expression; Nonndifferentiated cells; Rt qpcr; Spacefl ight

Indexed keywords

ARABIDOPSIS PROTEIN; HEAT SHOCK PROTEIN; MESSENGER RNA;

DICOTYLEDON; GENE EXPRESSION; GROWTH FORM; HEAT SHOCK; MOLECULAR ANALYSIS; PROTEIN;

ARABIDOPSIS; ARTICLE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GRAVITY; HEAT SHOCK RESPONSE; METABOLISM; METHODOLOGY; PLANT GENE; SPACE FLIGHT; TISSUE CULTURE TECHNIQUE; WEIGHTLESSNESS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HYPERGRAVITY; RNA, MESSENGER; SPACE FLIGHT; TISSUE CULTURE TECHNIQUES; WEIGHTLESSNESS;

ARABIDOPSIS THALIANA; BRASSICACEAE;

EID: 84872003235     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1200343     Document Type: Article

References (72)

1. AGUELI, C., F. GERACI, G. GIUDICE, L. CHIMENTI, D. CASCINO, and G. SCONZO. 2001. A constitutive 70kDa heat-shock protein is localized on the fibres of spindles and asters at metaphase in an ATP-dependent manner: A new chaperone role is proposed. Biochem Journal 360: 413-419.
2. Albrecht-Buehler, G. 1992. The simulation of microgravity conditions on the ground. American Society for Gravitational and Space Biology Bulletin 5: 3-10.
3. BALUSKA, F., and K. H. HASENSTEIN. 1997. Root cytoskeleton: Its role in perception of and response to gravity. Planta 203: S69-S78.
4. BANIWAL, S. K., K. BHARTI, K. Y. C HAN, M. F AUTH, A. GANGULI, S. KOTAK, S. K. MISHRA, et al. 2004. Heat stress response in plants: A complex game with chaperones and more than twenty heat stress transcription factors. Journal of Biosciences 29: 471-487.
5. BOHNERT, H. J., Q. GONG, P. LI, and S. MA. 2006. Unraveling abiotic stress tolerance mechanisms-Getting genomics going. Current Opinion in Plant Biology 9: 180-188.
6. BUSCH, W., M. WUNDERLICH, and F. SCHOFFL. 2005. Identifi cation of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant Journal 41: 1-14.
7. CARLSSON, S. I., M. T. BERTILACCIO, E. BALLABIO, and J. A. MAIER. 2003. Endothelial stress by gravitational unloading: Effects on cell growth and cytoskeletal organization. Biochimica et Biophysica Acta 1642: 173-179.
8. CARMELIET, G., G. NYS, I. STOCKMANS, and R. BOUILLON. 1998. Gene expression related to the differentiation of osteoblastic cells is altered by microgravity. Bone 22: 139S-143S.
9. COGOLI, A. 1997. Signal transduction in T lymphocytes in microgravity. American Society for Gravitational and Space Biology Bulletin 10: 5-16.
10. CUBANO, L. A., and M. L. LEWIS. 2001. Effect of vibrational stress and spacefl ight on regulation of heat shock proteins hsp70 and hsp27 in human lymphocytes (Jurkat). Journal of Leukocyte Biology 69: 755-761.
11. ERDMANN, N., U. EFFMERT, S. FULDA, and S. OHEIM. 1997. Effect of gravity changes on the cyanobacterium Synechocystis sp. PCC 6803. Current Microbiology 35: 348-355.
12. FEDER, M. E., and G. E. HOFMANN. 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61: 243-282.
13. GROSSE, J., M. WEHLAND, J. PIETSCH, X. MA, C. ULBRICH, H. SCHULZ, K. SAAR, et al. 2012. Short-term weightlessness produced by parabolic fl ight maneuvers altered gene expression patterns in human endothelial cells. FASEB Journal 26: 639-655.
14. GRUENER, R., R. ROBERTS, and R. REITSTETTER. 1994. Reduced receptor aggregation and altered cytoskeleton in cultured myocytes after space-fl ight. Uchu Seibutsu Kagaku 8: 79-93.
15. HIRASAKA, K., T. NIKAWA, Y. ASANOMA, H. FUROCHI, Y. O NISHI, T. OGAWA, N. SUZUE, et al. 2005. Short-term hypergravity does not affect protein- ubiquitination and proliferation in rat L6 myoblastic cells. Uchu Seibutsu Kagaku 19: 3-7.
16. HOSON, T., S. KAMISAKA, Y. MASUDA, M. YAMASHITA, and B. BUCHEN. 1997. Evaluation of the three-dimensional clinostat as a simulator of weightlessness. Planta 203 (supplement): S187-S197.
17. HSIEH, M. H., J. T. CHEN, T. L. JINN, Y. M. CHEN, and C. Y. LIN. 1992. A class of soybean low molecular weight heat shock proteins: Immunological study and quantitation. Plant Physiology 99: 1279-1284.
18. Hughes-Fulford, M. 2003. Function of the cytoskeleton in gravisensing during spacefl ight. Advances in Space Research: The Offi cial Journal of the Committee on Space Research 32: 1585-1593.
19. INGBER, D. 1999. How cells (might) sense microgravity. FASEB Journal 13 (supplement): S3-S15.
20. INGBER, D. E. 2008. Tensegrity-based mechanosensing from macro to micro. Progress in Biophysics and Molecular Biology 97: 163-179.
21. KARMALI, F., and M. SHELHAMER. 2008. The dynamics of parabolic fl ight: Flight characteristics and passenger percepts. Acta Astronautica 63: 594-602.
22. KERN, V. D., F. D. SACK, N. J. WHITE, K. ANDERSON, W. WELLS, and C. MARTIN. 1999. Spacefl ight hardware allowing unilateral irradiation and chemical fi xation in petri dishes. Advances in Space Research: The Offi cial Journal of the Committee on Space Research 24: 775-778.
23. KISS, J. Z. 2000. Mechanisms of the early phases of plant gravitropism. Critical Reviews in Plant Sciences 19: 551-573.
24. KLAUS, D. M. 2001. Clinostats and bioreactors. American Society for Gravitational and Space Biology Bulletin 14: 55-64.
25. LEE, S., M. E. SOWA, J. M. CHOI, and F. T. TSAI. 2004. The ClpB/Hsp104 molecular chaperone-A protein disaggregating machine. Journal of Structural Biology 146: 99-105.
26. LEWIS, M. L., and M. Hughes-Fulford. 2000. Regulation of heat shock protein message in Jurkat cells cultured under serum-starved and gravity-altered conditions. Journal of Cellular Biochemistry 77: 127-134.
27. LEYS, N., S. BAATOUT, C. ROSIER, A. DAMS, C. S'heeren, R. WATTIEZ, and M. MERGEAY. 2009. The response of Cupriavidus metallidurans CH34 to spacefl ight in the international space station. Antonie van Leeuwenhoek 96: 227-245.
28. LI, M., K. W. BERENDZEN, and F. SCHOFFL. 2010. Promoter specifi city and interactions between early and late Arabidopsis heat shock factors. Plant Molecular Biology 73: 559-567.
29. MANZANO, A. I., J. J. V AN LOON, P. C. CHRISTIANEN, J. M. Gonzalez-Rubio, F. J. MEDINA, and R. HERRANZ. 2012. Gravitational and magnetic fi eld variations synergize to cause subtle variations in the global transcriptional state of Arabidopsis in vitro callus cultures. BMC Genomics 13: 105.
30. MARTZIVANOU, M., and R. HAMPP. 2003. Hyper-gravity effects on the Arabidopsis transcriptome. Physiologia Plantarum 118: 221-231.
31. MILLAR, K. D., C. M. JOHNSON, R. E. EDELMANN, and J. Z. KISS. 2011. An endogenous growth pattern of roots is revealed in seedlings grown in microgravity. Astrobiology 11: 787-797.
32. Morey-Holton, E. R. 2003. The impact of gravity on life. In L. Rothschild and A. Lister [eds.], Evolution on planet Earth: The impact of the physical environment. Academic Press, New York, New York, USA.
33. MYERS, K. A., J. B. RATTNER, N. G. SHRIVE, and D. A. HART. 2007. Hydrostatic pressure sensation in cells: Integration into the tensegrity model. Biochemistry and Cell Biology 85: 543-551.
34. MYMRIKOV, E. V., A. S. Seit-Nebi, and N. B. G USEV. 2011. Large potentials of small heat shock proteins. Physiological Reviews 91: 1123-1159.
35. NATHAN, D. F., M. H. VOS, and S. L INDQUIST. 1997. In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proceedings of the National Academy of Sciences, USA 94: 12949-12956.
36. NELSON, E. S., and K. JULES. 2004. The microgravity environment for experiments on the International Space Station. Journal of Gravitational Physiology: A Journal of the International Society for Gravitational Physiology 11: 1-10.
37. NISHIZAWA, A., Y. YABUTA, E. YOSHIDA, T. MARUTA, K. YOSHIMURA, and S. SHIGEOKA. 2006. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant Journal 48: 535-547.
38. NOVER, L., K. BHARTI, P. D ORING, S. K. M ISHRA, A. G ANGULI, and K. D. SCHARF. 2001. Arabidopsis and the heat stress transcription factor world: How many heat stress transcription factors do we need? Cell Stress & Chaperones 6: 177-189.
39. OGURO, A., T. SAKURAI, Y. FUJITA, S. LEE, H. KUBOTA, K. NAGATA, and Y. ATOMI. 2006. The molecular chaperone HSP47 rapidly senses gravitational changes in myoblasts. Genes to Cells 11: 1253-1265.
40. PARSELL, D. A., A. S. KOWAL, M. A. SINGER, and S. LINDQUIST. 1994. Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372: 475-478.
41. PATEL, M. J., W. LIU, M. C. SYKES, N. E. WARD, S. A. RISIN, D. RISIN, and H. JO. 2007. Identifi cation of mechanosensitive genes in osteoblasts by comparative microarray studies using the rotating wall vessel and the random positioning machine. Journal of Cellular Biochemistry 101: 587-599.
42. PAUL, A.-L., R. J. FERL, and M. W. MEISEL. 2006. High magnetic fi eld induced changes of gene expression in arabidopsis. BioMagnetic Research and Technology 4: 7.
43. PAUL, A.-L., H. G. LEVINE, W. MCLAMB, K. L. NORWOOD, D. REED, G. W. STUTTE, H. W. WELLS, et al. 2005. Plant molecular biology in the space station era: Utilization of KSC fi xation tubes with RNAlater. Acta Astronautica 56: 623-628.
44. PAUL, A.-L., M. S. MANAK, J. D. MAYFIELD, M. F. REYES, W. B. GURLEY, and R. J. FERL. 2011. Parabolic fl ight induces changes in gene expression patterns in Arabidopsis thaliana. Astrobiology 11: 743-758.
45. PAUL, A.-L., A. K. ZUPANSKA, D. T. OSTROW, Y. ZHANG, Y. SUN, J. L. LI, S. SHANKER, et al. 2012. Spacefl ight transcriptomes: Unique responses to a novel environment. Astrobiology 12: 40-56.
46. PERRET, E., M. MOUDJOU, M. L. GERAUD, J. DERANCOURT, M. O. SOYERGOBILLARD, and M. BORNENS. 1995. Identifi cation of an HSP70-related protein associated with the centrosome from dinofl agellates to human cells. Journal of Cell Science 108: 711-725.
47. PIETSCH, J., J. BAUER, M. EGLI, M. INFANGER, P. WISE, C. ULBRICH, and D. GRIMM. 2011. The effects of weightlessness on the human organism and mammalian cells. Current Molecular Medicine 11: 350-364.
48. QUEITSCH, C., S. W. HONG, E. VIERLING, and S. LINDQUIST. 2000. Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12: 479-492.
49. ROSS, M. D. 1984. The infl uence of gravity on structure and function of animals. Advances in Space Research: The Offi cial Journal of the Committee on Space Research 4: 305-314.
50. SALMI, M. L., and S. J. ROUX. 2008. Gene expression changes induced by space fl ight in single-cells of the fern Ceratopteris richardii. Planta 229: 151-159.
51. SCHARF, K. D., T. BERBERICH, I. EBERSBERGER, and L. NOVER. 2012. The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Biochimica et Biophysica Acta 1819: 104-119.
52. SCHATTEN, H., M. L. LEWIS, and A. CHAKRABARTI. 2001. Spacefl ight and clinorotation cause cytoskeleton and mitochondria changes and increases in apoptosis in cultured cells. Acta Astronautica 49: 399-418.
53. SCHLESINGER, M. J. 1994. How the cell copes with stress and the function of heat shock proteins. Pediatric Research 36: 1-6.
54. SCHOFFL, F., R. PRANDL, and A. REINDL. 1998. Regulation of the heatshock response. Plant Physiology 117: 1135-1141.
55. SCHWARZ, R. P., T. J. GOODWIN, and D. A. WOLF. 1992. Cell culture for three-dimensional modeling in rotating-wall vessels: An application of simulated microgravity. Journal of Tissue Culture Methods 14: 51-57.
56. SHIMADA, N., and S. J. MOORMAN. 2006. Changes in gravitational force cause changes in gene expression in the lens of developing zebrafi sh. Developmental Dynamics 235: 2686-2694.
57. SHORTER, J. 2011. The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS ONE 6: e26319.
58. SIDDIQUE, M., S. GERNHARD, P. VON Koskull-Doring, E. VIERLING, and K. D. SCHARF. 2008. The plant sHSP superfamily: Five new members in Arabidopsis thaliana with unexpected properties. Cell Stress & Chaperones 13: 183-197.
59. SIEVERS, A., and Z. HEJNOWICZ. 1992. How well does the clinostat mimic the effect of microgravity on plant cells and organs? American Society for Gravitational and Space Biology Bulletin 5: 69-75.
60. STAVES, M. P., R. W AYNE, and A. C. LEOPOLD. 1997. The effect of the external medium on the gravitropic curvature of rice (Oryza sativa, Poaceae) roots. American Journal of Botany 84: 1522-1529.
61. STUTTE, G. W., and M. ROBERTS. 2011. Biological Research in Canisters Symbiotic Nodulation in a Reduced Gravity Environment (BRIC-12.04.12 SyNRGE). Website http://www.nasa.gov/mission_pages/station/research/experiments/BRIC-SyNRGE.html. [accessed 24 June 2012].
62. SUN, W., M. VAN MONTAGU, and N. VERBRUGGEN. 2002. Small heat shock proteins and stress tolerance in plants. Biochimica et Biophysica Acta 1577: 1-9.
63. TABONY, J., N. POCHON, and C. PAPASEIT. 2001. Microtubule self-organisation depends upon gravity. Advances in Space Research: The Offi cial Journal of the Committee on Space Research 28: 529-535.
64. TODD, P. 1989. Gravity-dependent phenomena at the scale of the single cell. American Society of Gravitational and Space Biology 2: 95-113.
65. UVA, B. M., F. S TROLLO, F. RICCI, M. P ASTORINO, J. I. MASON, and M. A. MASINI. 2005. Morpho-functional alterations in testicular and nervous cells submitted to modelled microgravity. Journal of Endocrinological Investigation 28: 84-91.
66. VERSARI, S., A. VILLA, S. BRADAMANTE, and J. A. MAIER. 2007. Alterations of the actin cytoskeleton and increased nitric oxide synthesis are common features in human primary endothelial cell response to changes in gravity. Biochimica et Biophysica Acta 1773: 1645-1652.
67. VILLA, A., S. VERSARI, J. A. MAIER, and S. BRADAMANTE. 2005. Cell behavior in simulated microgravity: A comparison of results obtained with RWV and RPM. American Society for Gravitational and Space Biology Bulletin 18: 89-90.
68. VOLKMANN, D., and F. BALUSKA. 2006. Gravity: One of the driving forces for evolution. Protoplasma 229: 143-148.
69. WANG, W., B. V INOCUR, O. SHOSEYOV, and A. ALTMAN. 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9: 244-252.
70. WARD, N. E., N. R. PELLIS, S. A. RISIN, and D. RISIN. 2006. Gene expression alterations in activated human T-cells induced by modeled microgravity. Journal of Cellular Biochemistry 99: 1187-1202.
71. WEAVER, S., S. DUBE, A. MIR, J. QIN, G. SUN, R. RAMAKRISHNAN, R. C. JONES, et al. 2010. Taking qPCR to a higher level: Analysis of CNV reveals the power of high throughput qPCR to enhance quantitative resolution. Methods 50: 271-276.
72. YODER, T. L., H. Q. ZHENG, P. TODD, and L. A. STAEHELIN. 2001. Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots. Plant Physiology 125: 1045-1060.