Expression of heat shock proteins in anoxic crucian carp (Carassius carassius): support for cold as a preparatory cue for anoxia.

The crucian carp (Carassius carassius) tolerates anoxia for days to months depending on temperature. During episodes of stress, heat shock proteins (HSPs) are important for limiting cellular damage, mainly by ensuring protein function. Accordingly, we hypothesized that anoxia would change the expression of HSPs and that this response would be temperature dependent. Real-time RT-PCR was used to investigate the effects of 1 and 7 days anoxia (A1 and A7) on the expression of HSP70a, HSP70b, HSC70, HSP90, and HSP30 in the brain and heart of 8 degrees C- and 13 degrees C-acclimated crucian carp. In general, the expression of all HSPs changed in response to anoxia, although varying in size and direction, and with organ and temperature. HSP70a expression increased drastically (approximately 10-fold) in A7 brains and hearts at 13 degrees C but not at 8 degrees C. HSC70 and HSP90 expression decreased in A7 brains (by 60-70%), but not in A7 hearts. HSC70 expression increased in A1 brains and hearts at both temperatures (by 60-160%), and HSP30 expression decreased in A7 brains and hearts at both temperatures (by 50-80%). Notably, normoxic fish showed 7- and 11-fold higher HSP70a expression in the brain and heart at 8 degrees C compared with 13 degrees C. This difference disappeared during anoxia, suggesting that cold may function as a cue for preconditioning the crucian carp's HSP70a expression to the approaching anoxic winter period.

[1]  F. Salloum,et al.  A Novel Role of MicroRNA in Late Preconditioning: Upregulation of Endothelial Nitric Oxide Synthase and Heat Shock Protein 70 , 2009, Circulation research.

[2]  G. Nilsson,et al.  Differential regulation of AMP-activated kinase and AKT kinase in response to oxygen availability in crucian carp (Carassius carassius). , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[3]  T. Kristensen,et al.  Expression of genes involved in excitatory neurotransmission in anoxic crucian carp (Carassius carassius) brain. , 2008, Physiological genomics.

[4]  P. Lutz,et al.  Effect of anoxia on the electroretinogram of three anoxia-tolerant vertebrates. , 2008, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[5]  G. Nilsson,et al.  Hypoxia inducible factor (HIF) — A threat to hypoxic survival? , 2008 .

[6]  T. Kristensen,et al.  Improved normalization of real-time reverse transcriptase polymerase chain reaction data using an external RNA control. , 2008, Analytical biochemistry.

[7]  M. Hermansson,et al.  Seasonal acclimatization of brain lipidome in a eurythermal fish (Carassius carassius) is mainly determined by temperature. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[8]  E. Solary,et al.  Heat shock proteins: essential proteins for apoptosis regulation , 2008, Journal of cellular and molecular medicine.

[9]  G. Semenza,et al.  Hypoxia-Inducible Factor 1 (HIF-1) Pathway , 2007, Science's STKE.

[10]  IAN R. BROWN,et al.  Heat Shock Proteins and Protection of the Nervous System , 2007, Annals of the New York Academy of Sciences.

[11]  D. Yellon,et al.  Myocardial reperfusion injury. , 2007, The New England journal of medicine.

[12]  M. Jäättelä,et al.  The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions , 2007, FEBS letters.

[13]  G. Semenza,et al.  RACK1 vs. HSP90: Competition for HIF-1α Degradation vs. Stabilization , 2007 .

[14]  M. Vornanen,et al.  Seasonal changes in glycogen content and Na+-K+-ATPase activity in the brain of crucian carp. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[15]  L. Pearl,et al.  Structure and mechanism of the Hsp90 molecular chaperone machinery. , 2006, Annual review of biochemistry.

[16]  G. Nilsson,et al.  HIF-1α and iNOS levels in crucian carp gills during hypoxia-induced transformation , 2006, Journal of Comparative Physiology B.

[17]  G. Hofmann,et al.  Turning up the heat: the effects of thermal acclimation on the kinetics of hsp70 gene expression in the eurythermal goby, Gillichthys mirabilis. , 2006, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[18]  G. Nilsson,et al.  Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius) , 2006, Journal of Experimental Biology.

[19]  H. Beere Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. , 2005, The Journal of clinical investigation.

[20]  J. Buchner,et al.  Some like it hot: the structure and function of small heat-shock proteins , 2005, Nature Structural &Molecular Biology.

[21]  G. Nilsson,et al.  Cell proliferation and gill morphology in anoxic crucian carp. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[22]  D. Latchman HSP27 and cell survival in neurones , 2005, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[23]  T. Bagnyukova,et al.  Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. , 2005, The international journal of biochemistry & cell biology.

[24]  N. Woo,et al.  Cloning and characterization of the hsp70 multigene family from silver sea bream: Modulated gene expression between warm and cold temperature acclimation. , 2005, Biochemical and biophysical research communications.

[25]  E. Solary,et al.  Small heat shock proteins HSP27 and alphaB-crystallin: cytoprotective and oncogenic functions. , 2005, Antioxidants & redox signaling.

[26]  J. Rogers,et al.  Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Charles E. Chapple,et al.  Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype , 2004, Nature.

[28]  A. Farrell,et al.  Maintained Cardiac Pumping in Anoxic Crucian Carp , 2004, Science.

[29]  L. Buck,et al.  Time-dependent expression of heat shock proteins 70 and 90 in tissues of the anoxic western painted turtle , 2004, Journal of Experimental Biology.

[30]  G. Nilsson,et al.  Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark , 2004, Journal of Experimental Biology.

[31]  P. Lutz,et al.  The Upregulation of Cognate and Inducible Heat Shock Proteins in the Anoxic Turtle Brain , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[32]  P. Klesius,et al.  Hypoxic conditions induce Hsp70 production in blood, brain and head kidney of juvenile Nile tilapia Oreochromis niloticus (L.) , 2004 .

[33]  H. Kondo,et al.  Temperature-dependent enhancement of cell proliferation and mRNA expression for type I collagen and HSP70 in primary cultured goldfish cells. , 2004, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[34]  P. Lutz,et al.  Anoxia Tolerant Brains , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[35]  K. Inoki,et al.  TSC2 Mediates Cellular Energy Response to Control Cell Growth and Survival , 2003, Cell.

[36]  C. Råbergh,et al.  Heat- and cold-inducible regulation of HSP70 expression in zebrafish ZF4 cells. , 2003, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[37]  M. Akbar,et al.  The Neuroprotective Effects of Heat Shock Protein 27 Overexpression in Transgenic Animals against Kainate-induced Seizures and Hippocampal Cell Death* , 2003, Journal of Biological Chemistry.

[38]  A. Moorman,et al.  Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data , 2003, Neuroscience Letters.

[39]  L. Neckers,et al.  Heat shock protein 90 as a molecular target for cancer therapeutics. , 2003, Cancer cell.

[40]  P. Schulte,et al.  Heat shock protein genes and their functional significance in fish. , 2002, Gene.

[41]  T. Südhof,et al.  A Trimeric Protein Complex Functions as a Synaptic Chaperone Machine , 2001, Neuron.

[42]  D. Latchman Heat shock proteins and cardiac protection. , 2001, Cardiovascular research.

[43]  M. Vornanen,et al.  Cold adaptation suppresses the contractility of both atrial and ventricular muscle of the crucian carp heart , 2001 .

[44]  B. Tufts,et al.  The effects of heat shock and acclimation temperature on hsp70 and hsp30 mRNA expression in rainbow trout: in vivo and in vitro comparisons , 2000 .

[45]  D. Mottet,et al.  Hypoxia‐induced activation of HIF‐1: role of HIF‐1α‐Hsp90 interaction , 1999 .

[46]  L. Sistonen,et al.  Effects of heat shock and hypoxia on protein synthesis in rainbow trout (Oncorhynchus mykiss) cells. , 1998, The Journal of experimental biology.

[47]  A. Farrell,et al.  β-Receptors and stress protein 70 expression in hypoxic myocardium of rainbow trout and chinook salmon. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[48]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[49]  M. Gaestel,et al.  Binding of non‐native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation , 1997, The EMBO journal.

[50]  D. Latchman,et al.  Focal cerebral ischaemia increases the levels of several classes of heat shock proteins and their corresponding mRNAs. , 1996, Brain research. Molecular brain research.

[51]  Johansson,et al.  Effects of anoxia on energy metabolism in crucian carp brain slices studied with microcalorimetry , 1995, The Journal of experimental biology.

[52]  M. Vornanen Seasonal and temperature-induced changes in myosin heavy chain composition of crucian carp hearts. , 1994, The American journal of physiology.

[53]  M. Vornanen Seasonal adaptation of crucian carp (Carassius carassius L.) heart: glycogen stores and lactate dehydrogenase activity , 1994 .

[54]  Göran E. Nilsson,et al.  Anoxic depression of spontaneous locomotor activity in crucian carp quantified by a computerized imaging technique , 1993 .

[55]  L. Hansen,et al.  Differential regulation of HSC70, HSP70, HSP90α, and HSP90β mRNA expression by mitogen activation and heat shock in human lymphocytes , 1991 .

[56]  R. Jennings,et al.  Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. , 1986, Circulation.

[57]  P. W. Hochachka Defense strategies against hypoxia and hypothermia. , 1986, Science.

[58]  Ma Hongbao,et al.  Hypoxia inducible factor (HIF) , 2010 .

[59]  T. Kristensen,et al.  Expression of genes involved in GABAergic neurotransmission in anoxic crucian carp brain (Carassius carassius). , 2009, Physiological genomics.

[60]  Katerina Sidera and Evangelia Patsavoudi Extracellular HSP90: An Emerging Target for Cancer Therapy , 2009 .

[61]  T. Obrenovitch Molecular physiology of preconditioning-induced brain tolerance to ischemia. , 2008, Physiological reviews.

[62]  G. Semenza,et al.  RACK1 vs. HSP90: competition for HIF-1 alpha degradation vs. stabilization. , 2007, Cell cycle.

[63]  R. Sievers,et al.  Heat-shock protein induction in rat hearts. A direct correlation between the amount of heat-shock protein induced and the degree of myocardial protection. , 1994, Circulation.

[64]  S. Lindquist,et al.  The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. , 1993, Annual review of genetics.

[65]  I. Holopainen,et al.  A note on seasonality in anoxia tolerance of crucian carp (Carassius carassius (L.)) in the laboratory , 1986 .