Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis.

Hypoxia is important in both biomedical and environmental contexts and necessitates rapid adaptive changes in metabolic organization. Mammals, as air breathers, have a limited capacity to withstand sustained exposure to hypoxia. By contrast, some aquatic animals, such as certain fishes, are routinely exposed and resistant to severe environmental hypoxia. Understanding the changes in gene expression in fishes exposed to hypoxic stress could reveal novel mechanisms of tolerance that may shed new light on hypoxia and ischemia in higher vertebrates. Using cDNA microarrays, we have studied gene expression in a hypoxia-tolerant burrow-dwelling goby fish, Gillichthys mirabilis. We show that a coherent picture of a complex transcriptional response can be generated for a nonmodel organism for which sequence data were unavailable. We demonstrate that: (i) although certain shifts in gene expression mirror changes in mammals, novel genes are differentially expressed in fish; and (ii) tissue-specific patterns of expression reflect the different metabolic roles of tissues during hypoxia.

[1]  M. Soares,et al.  Normalization and subtraction: two approaches to facilitate gene discovery. , 1996, Genome research.

[2]  S. Keyse,et al.  Oxidative stress and heat shock induce a human gene encoding a protein-tyrosine phosphatase , 1992, Nature.

[3]  G. Semenza,et al.  Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. , 1994, The Journal of biological chemistry.

[4]  J. Cairney,et al.  Isolation of full-length cDNA clones using SMART cDNA and a biotin-streptavidin bead system. , 2000, BioTechniques.

[5]  G. Semenza,et al.  Hypoxia-inducible Factor-1 Mediates Transcriptional Activation of the Heme Oxygenase-1 Gene in Response to Hypoxia* , 1997, The Journal of Biological Chemistry.

[6]  W. Kaelin,et al.  Functions of the retinoblastoma protein. , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[7]  R. Boutilier,et al.  Surviving hypoxia without really dying. , 1999, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[8]  Aaron P. Campbell,et al.  Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[9]  P. Donohoe,et al.  The use of extracellular lactate as an oxidative substrate in the oxygen-limited frog. , 1999, Respiration physiology.

[10]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[11]  L. Wodicka,et al.  Genome-wide expression monitoring in Saccharomyces cerevisiae , 1997, Nature Biotechnology.

[12]  P. W. Hochachka,et al.  Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[13]  G. Semenza,et al.  Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. , 1999, Annual review of cell and developmental biology.

[14]  Y. Nakamura,et al.  Tob, a novel protein that interacts with p185erbB2, is associated with anti-proliferative activity. , 1996, Oncogene.

[15]  F. Kaye,et al.  Differential specificity for binding of retinoblastoma binding protein 2 to RB, p107, and TATA-binding protein , 1994, Molecular and cellular biology.

[16]  D. Botstein,et al.  Exploring the new world of the genome with DNA microarrays , 1999, Nature Genetics.

[17]  Ash A. Alizadeh,et al.  Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling , 2000, Nature.

[18]  A. Bloch,et al.  Tumor suppressor proteins as regulators of cell differentiation. , 1998, Cancer research.

[19]  L. Giudice,et al.  Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  T. Chard Insulin-like growth factors and their binding proteins in normal and abnormal human fetal growth. , 1994, Growth regulation.

[21]  M. Gassmann,et al.  Oxygen-regulated Transferrin Expression Is Mediated by Hypoxia-inducible Factor-1* , 1997, The Journal of Biological Chemistry.

[22]  Christian A. Rees,et al.  Systematic variation in gene expression patterns in human cancer cell lines , 2000, Nature Genetics.

[23]  G. Semenza HIF-1: mediator of physiological and pathophysiological responses to hypoxia. , 2000, Journal of applied physiology.

[24]  Yun-Fai Chris Lau,et al.  [20] Suppression subtractive hybridization: A versatile method for identifying differentially expressed genes , 1999 .

[25]  P. Brown,et al.  DNA arrays for analysis of gene expression. , 1999, Methods in enzymology.

[26]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  K. Storey Tissue-Specific Controls on Carbohydrate Catabolism during Anoxia in Goldfish , 1987, Physiological Zoology.

[28]  P. Burgers Overexpression of multisubunit replication factors in yeast. , 1999, Methods.

[29]  A. Whitmarsh,et al.  Signal transduction: A central control for cell growth , 2000, Nature.