Metabolic energy sensors (AMPK and SIRT1), protein carbonylation, and cardiac failure as biomarkers of thermal stress in an intertidal limpet: linking energetic allocation with environmental temperature during aerial emersion

Guo-Dong Han1, Shu Zhang1, David J. Marshall2, Caihuan Ke1, Yun‐Wei Dong1
1[Xiamen University]
2Universiti Brunei Darussalam

Tóm tắt

SummaryThe effects of heat stress on organisms are manifested at the levels of organ function, metabolic activity, protein stability and gene expression. Here, we examined effects of high temperature on the intertidal limpet Cellana toreuma to determine how the temperatures at which organ failure (cardiac function), irreversible protein damage (carbonylation), and expression of genes encoding proteins involved in molecular chaperoning (hsp70 and hsp90) and metabolic regulation (ampk and sirt1) compare with field temperatures, which commonly exceed 30°C and can reach 46°C. Heart failure, indexed by the Arrhenius break temperature (ABT) was 34.3°C. Protein carbonylation rose significantly at 38°C. Genes for heat shock proteins HSP70 (hsp70) and HSP90 (hsp90), for two subunits of AMP-activated protein kinase (AMPK) (ampkα and ampkβ), and for histone/protein deacetylase SIRT1 (sirt1) all showed increased expression at 30°C. Temperatures of maximal expression differed among genes, as did temperatures at which up-regulation ceased. Expression patterns for ampk and sirt1 indicate that heat stress influenced cellular energy homeostasis; above ~30°C, up-regulation of ATP-generating pathways is suggested by elevated expression of genes for ampk; an altered balance between reliance on carbohydrate and lipid fuels is indicated by changes in expression of sirt1. These results show that C. toreuma commonly experiences temperatures that induce expression of genes associated with the stress response (hsp70 and hsp90) and regulation of energy metabolism (ampk and sirt1). At high temperatures, there is likely to be a shift away from anabolic processes like growth to catabolic processes, to provide energy for coping with stress-induced damage, notably to proteins.

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Tài liệu tham khảo

Abràmoff, 2004, Image processing with ImageJ, Biophotonics Int., 11, 36

Barry, 1995, Climate-related, long-term faunal changes in a California rocky intertidal community, Science, 267, 672, 10.1126/science.267.5198.672

Bergeron, 1999, Effect of AMPK activation on muscle glucose metabolism in conscious rats, Am. J. Physiol., 276, 938

Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3

Cantó, 2009, AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity, Nature, 458, 1056, 10.1038/nature07813

Chelazzi, 2001, Cardiac responses to abiotic factors in two tropical limpets, occurring at different levels of the shore, Mar. Biol., 139, 1079, 10.1007/s002270100603

Clark, 2008, Lack of an HSP70 heat shock response in two Antarctic marine invertebrates, Polar Biol., 31, 1059, 10.1007/s00300-008-0447-7

Clark, 2008, Antarctic marine molluscs do have an HSP70 heat shock response, Cell Stress Chaperones, 13, 39, 10.1007/s12192-008-0014-8

Connor, 2011, Circadian cycles are the dominant transcriptional rhythm in the intertidal mussel Mytilus californianus, Proc. Natl. Acad. Sci. USA, 108, 16110, 10.1073/pnas.1111076108

Dalle-Donne, 2003, Protein carbonyl groups as biomarkers of oxidative stress, Clin. Chim. Acta, 329, 23, 10.1016/S0009-8981(03)00003-2

Davenport, 2005, Effects of shore height, wave exposure and geographical distance on thermal niche width of intertidal fauna, Mar. Ecol. Prog. Ser., 292, 41, 10.3354/meps292041

Dong, 2011, Variations in cardiac performance and heat shock protein expression to thermal stress in two differently zoned limpets on a tropical rocky shore, Mar. Biol., 158, 1223, 10.1007/s00227-011-1642-6

Dong, 2008, Heat-shock protein 70 (Hsp70) expression in four limpets of the genus Lottia: interspecific variation in constitutive and inducible synthesis correlates with in situ exposure to heat stress, Biol. Bull., 215, 173, 10.2307/25470698

Dong, 2012, The impact of Yangtze River discharge, ocean currents and historical events on the biogeographic pattern of Cellana toreuma along the China coast, PLoS ONE, 7, e36178, 10.1371/journal.pone.0036178

Eliason, 2011, Differences in thermal tolerance among sockeye salmon populations, Science, 332, 109, 10.1126/science.1199158

Etschmann, 2006, Selection of reference genes for quantitative real-time PCR analysis in canine mammary tumors using the GeNorm algorithm, Vet. Pathol., 43, 934, 10.1354/vp.43-6-934

Firth, 2009, The influence of multiple environmental stressors on the limpet Cellana toreuma during the summer monsoon season in Hong Kong, J. Exp. Mar. Biol. Ecol., 375, 70, 10.1016/j.jembe.2009.05.011

Frederich, 2009, AMP-activated protein kinase (AMPK) in the rock crab, Cancer irroratus: an early indicator of temperature stress, J. Exp. Biol., 212, 722, 10.1242/jeb.021998

Gilman, 2006, Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales, Proc. Natl. Acad. Sci. USA, 103, 9560, 10.1073/pnas.0510992103

Gracey, 2008, Rhythms of gene expression in a fluctuating intertidal environment, Curr. Biol., 18, 1501, 10.1016/j.cub.2008.08.049

Hardie, 2006, AMPK: a key sensor of fuel and energy status in skeletal muscle, Physiology, 21, 48, 10.1152/physiol.00044.2005

Helmuth, 2001, Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone, Biol. Bull., 201, 374, 10.2307/1543615

Helmuth, 2002, Climate change and latitudinal patterns of intertidal thermal stress, Science, 298, 1015, 10.1126/science.1076814

Helmuth, 2006, Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change, Annu. Rev. Ecol. Evol. Syst., 37, 373, 10.1146/annurev.ecolsys.37.091305.110149

Helmuth, 2006, Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change, Ecol. Monogr., 76, 461, 10.1890/0012-9615(2006)076[0461:MPOTSI]2.0.CO;2

Hochachka, 2002, Biochemical Adaptation: Mechanism and Process in Physiological Evolution, 10.1093/oso/9780195117028.001.0001

Hofmann, 2010, Living in the now: physiological mechanisms to tolerate a rapidly changing environment, Annu. Rev. Physiol., 72, 127, 10.1146/annurev-physiol-021909-135900

Houtkooper, 2012, Sirtuins as regulators of metabolism and healthspan, Nat. Rev. Mol. Cell Biol., 13, 225, 10.1038/nrm3293

Lima, 2009, Robolimpets: measuring intertidal body temperatures using biomimetic loggers, Limnol. Oceanogr. Methods, 7, 347, 10.4319/lom.2009.7.347

Lima, 2012, Three decades of high-resolution coastal sea surface temperatures reveal more than warming, Nat. Commun., 3, 704, 10.1038/ncomms1713

Lockwood, 2010, Transcriptomic responses to heat stress in invasive and native blue mussels (genus Mytilus): molecular correlates of invasive success, J. Exp. Biol., 213, 3548, 10.1242/jeb.046094

Logan, 2010, Transcriptional responses to thermal acclimation in the eurythermal fish Gillichthys mirabilis (Cooper 1864), Am. J. Physiol., 299, R843

Lushchak, 2006, Effects of different environmental oxygen levels on free radical processes in fish, Comp. Biochem. Physiol., 144B, 283, 10.1016/j.cbpb.2006.02.014

Miller, 2009, The role of temperature and desiccation stress in limiting the local-scale distribution of the owl limpet, Lottia gigantea, Funct. Ecol., 23, 756, 10.1111/j.1365-2435.2009.01567.x

Ng S. (2007). Resource Partitioning and Coexistence of Molluscan Grazers on Hong Kong Rocky Shores. PhD thesis, University of Hong Kong, Hong Kong.

Place, 2008, Gene expression in the intertidal mussel Mytilus californianus: physiological response to environmental factors on a biogeographic scale, Mar. Ecol. Prog. Ser., 356, 1, 10.3354/meps07354

Pörtner, 2010, Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems, J. Exp. Biol., 213, 881, 10.1242/jeb.037523

Pörtner, 2006, Trade-offs in thermal adaptation: the need for a molecular to ecological integration, Physiol. Biochem. Zool., 79, 295, 10.1086/499986

Ruderman, 2010, AMPK and SIRT1: a long-standing partnership?, Am. J. Physiol., 298, E751

Sambandam, 2003, AMP-activated protein kinase (AMPK) control of fatty acid and glucose metabolism in the ischemic heart, Prog. Lipid Res., 42, 238, 10.1016/S0163-7827(02)00065-6

Sanders, 1991, Characterization of the stress protein response in two species of Collisella limpets with different temperature tolerances, Physiol. Zool., 64, 1471, 10.1086/physzool.64.6.30158225

Sokolova, 2012, Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates, Mar. Environ. Res., 79, 1, 10.1016/j.marenvres.2012.04.003

Somero, 2002, Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living, Integr. Comp. Biol., 42, 780, 10.1093/icb/42.4.780

Somero, 2010, The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’, J. Exp. Biol., 213, 912, 10.1242/jeb.037473

Somero, 2011, Comparative physiology: a ‘crystal ball’ for predicting consequences of global change, Am. J. Physiol., 301, R1

Somero, 2012, The physiology of global change: linking patterns to mechanisms, Ann. Rev. Mar. Sci., 4, 39, 10.1146/annurev-marine-120710-100935

Sørensen, 2003, The evolutionary and ecological role of heat shock proteins, Ecol. Lett., 6, 1025, 10.1046/j.1461-0248.2003.00528.x

Southward, 1995, Seventy years' observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature, J. Therm. Biol., 20, 127, 10.1016/0306-4565(94)00043-I

Stadtman, 2003, Free radical-mediated oxidation of free amino acids and amino acid residues in proteins, Amino Acids, 25, 207, 10.1007/s00726-003-0011-2

Stenseng, 2005, Evolutionary and acclimation-induced variation in the thermal limits of heart function in congeneric marine snails (genus Tegula): implications for vertical zonation, Biol. Bull., 208, 138, 10.2307/3593122

Stillman, 2002, Causes and consequences of thermal tolerance limits in rocky intertidal porcelain crabs, genus Petrolisthes, Integr. Comp. Biol., 42, 790, 10.1093/icb/42.4.790

Stillman, 1996, Adaptation to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (genus Petrolisthes): correlation of physiology, biochemistry and morphology with vertical distribution, J. Exp. Biol., 199, 1845, 10.1242/jeb.199.8.1845

Stillman, 2009, Seasonal and latitudinal acclimatization of cardiac transcriptome responses to thermal stress in porcelain crabs, Petrolisthes cinctipes, Mol. Ecol., 18, 4206, 10.1111/j.1365-294X.2009.04354.x

Tomanek, 2010, Variation in the heat shock response and its implication for predicting the effect of global climate change on species' biogeographical distribution ranges and metabolic costs, J. Exp. Biol., 213, 971, 10.1242/jeb.038034

Tomanek, 2012, Environmental proteomics of the mussel Mytilus: implications for tolerance to stress and change in limits of biogeographic ranges in response to climate change, Integr. Comp. Biol., 52, 648, 10.1093/icb/ics114

Tomanek, 2002, Physiological ecology of rocky intertidal organisms: a synergy of concepts, Integr. Comp. Biol., 42, 771, 10.1093/icb/42.4.771

Tomanek, 1999, Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography, J. Exp. Biol., 202, 2925, 10.1242/jeb.202.21.2925

Tomanek, 2002, Interspecific- and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): implications for regulation of hsp gene expression, J. Exp. Biol., 205, 677, 10.1242/jeb.205.5.677

Tomanek, 2010, The proteomic response of the mussel congeners Mytilus galloprovincialis and M. trossulus to acute heat stress: implications for thermal tolerance limits and metabolic costs of thermal stress, J. Exp. Biol., 213, 3559, 10.1242/jeb.041228

Wang, 2010, Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux, Science, 327, 1004, 10.1126/science.1179687

Westerheide, 2009, Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1, Science, 323, 1063, 10.1126/science.1165946

Williams, 1995, Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata, Mar. Ecol. Prog. Ser., 124, 89, 10.3354/meps124089

Wolcott, 1973, Physiological ecology and intertidal zonation in limpets (Acmaea): a critical look at ‘limiting factors’, Biol. Bull., 145, 389, 10.2307/1540048

Zhao, 2010, Regulation of cellular metabolism by protein lysine acetylation, Science, 327, 1000, 10.1126/science.1179689