Skip to main content
OSTI.GOVU.S. Department of Energy Office of Scientific and Technical Information
U.S. Department of Energy
Office of Scientific and Technical Information
 

Ni induces the CRR1-dependent regulon revealing overlap and distinction between hypoxia and Cu deficiency responses in Chlamydomonas reinhardtii

Journal Article · · Metallomics
DOI:https://doi.org/10.1039/C6MT00063K· OSTI ID:1424989
 [1];  [2];  [2];  [2];  [2]
  1. Univ. of California, Los Angeles, CA (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
  2. Univ. of California, Los Angeles, CA (United States)
+ Show Author Affiliations

The selectivity of metal sensors for a single metal ion is critical for cellular metal homeostasis. A suite of metal-responsive regulators is required to maintain a prescribed balance of metal ions ensuring that each apo-protein binds the correct metal. However, there are cases when non-essential metals ions disrupt proper metal sensing. Here, an analysis of the Ni-responsive transcriptome of the green alga Chlamydomonas reinhardtii reveals that Ni artificially turns on the CRR1-dependent Cu-response regulon. Since this regulon also responds to hypoxia, a combinatorial transcriptome analysis was leveraged to gain insight into the mechanisms by which Ni interferes with the homeostatic regulation of Cu and oxygen status. Based on parallels with the effect of Ni on the hypoxic response in animals, we propose that a possible link between Cu, oxygen and Ni sensing is an as yet uncharacterized prolyl hydroxylase that regulates a co-activator of CRR1. This analysis also identified transcriptional responses to the pharmacological activation of the Cu-deficiency regulon. Although the Ni-responsive CRR1 regulon is composed of 56 genes (defined as the primary response), 259 transcripts responded to Ni treatment only when a copy of the wild-type CRR1 gene was present. The genome-wide impact of CRR1 target genes on the transcriptome was also evident from the 210 transcripts that were at least 2-fold higher in the crr1 strain, where the abundance of many CRR1 targets was suppressed. Additionally, we identified 120 transcripts that responded to Ni independent of CRR1 function. Thus, the putative functions of the proteins encoded by these transcripts suggest that high Ni results in protein damage.

Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
Grant/Contract Number:
SC0012704
OSTI ID:
1424989
Report Number(s):
BNL--113169-2016-JAAM
Journal Information:
Metallomics, Journal Name: Metallomics Journal Issue: 7 Vol. 8; ISSN METAIR; ISSN 1756-5901
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (49)

Soluble nickel inhibits HIF-prolyl-hydroxylases creating persistent hypoxic signaling in A549 cells journal January 2006
Autophagy: cellular and molecular mechanisms journal February 2010
A Chlamydomonas gene encodes a G protein ? subunit-like polypeptide journal May 1990
The Cell Wall as a Barrier to Uptake of Metal Ions in the Unicellular Green Alga Chlamydomonas reinhardtii (Chlorophyceae) journal November 2000
Deregulation of transition metals homeostasis is a key feature of cadmium toxicity in Salmonella journal June 2014
Biogenesis and assembly of eukaryotic cytochrome c oxidase catalytic core journal June 2012
Ordering effects of cholesterol and its analogues journal January 2009
Signalling hypoxia by HIF hydroxylases journal December 2005
Differential analysis of gene regulation at transcript resolution with RNA-seq journal December 2012
Dysregulation of transition metal ion homeostasis is the molecular basis for cadmium toxicity in Streptococcus pneumoniae journal March 2015
The effects of mitochondrial iron homeostasis on cofactor specificity of superoxide dismutase 2 journal April 2006
Mechanisms of nickel toxicity in microorganisms journal January 2011
YeiR: a metal-binding GTPase from Escherichia coli involved in metal homeostasis journal January 2012
A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element journal December 2005
Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas journal December 2011
Copper economy in Chlamydomonas : Prioritized allocation and reallocation of copper to respiration vs. photosynthesis journal February 2015
Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide journal December 2003
Cluster analysis and display of genome-wide expression patterns journal December 1998
Induction of Coproporphyrinogen Oxidase in Chlamydomonas Chloroplasts Occurs via Transcriptional Regulation of Cpx1 Mediated by Copper Response Elements and Increased Translation from a Copper Deficiency-specific Form of the Transcript journal May 1999
Nickel Ions Inhibit Histone Demethylase JMJD1A and DNA Repair Enzyme ABH2 by Replacing the Ferrous Iron in the Catalytic Centers journal December 2009
Depletion of Intracellular Ascorbate by the Carcinogenic Metals Nickel and Cobalt Results in the Induction of Hypoxic Stress journal July 2004
The Mismetallation of Enzymes during Oxidative Stress journal August 2014
Lysosome-related Organelles as Mediators of Metal Homeostasis journal August 2014
Choosing the Right Metal: Case Studies of Class I Ribonucleotide Reductases journal August 2014
STAR: ultrafast universal RNA-seq aligner journal October 2012
Nickel-induced transformation shifts the balance between HIF-1 and p53 transcription factors journal September 1999
The Crd1 gene encodes a putative di-iron enzyme required for photosystem I accumulation in copper deficiency and hypoxia in Chlamydomonas reinhardtii journal May 2000
Characterization of novel genes induced by sexual adhesion and gamete fusion and of their transcriptional regulation in Chlamydomonas reinhardtii journal April 2008
Metal Ions-Stimulated Iron Oxidation in Hydroxylases Facilitates Stabilization of HIF-1α Protein journal December 2008
Oxygen Deficiency Responsive Gene Expression in Chlamydomonas reinhardtii through a Copper-Sensing Signal Transduction Pathway journal February 2002
Differential Expression of the Chlamydomonas [FeFe]-Hydrogenase-Encoding HYDA1 Gene Is Regulated by the COPPER RESPONSE REGULATOR1 journal June 2012
Evidence for Autocatalytic Cross-Linking of Hydroxyproline-Rich Glycoproteins during Extracellular Matrix Assembly in Volvox journal April 2002
The CRR1 Nutritional Copper Sensor in Chlamydomonas Contains Two Distinct Metal-Responsive Domains journal December 2010
Systems Biology Approach in Chlamydomonas Reveals Connections between Copper Nutrition and Multiple Metabolic Steps journal April 2011
Systems and Trans -System Level Analysis Identifies Conserved Iron Deficiency Responses in the Plant Lineage journal October 2012
COPPER RESPONSE REGULATOR1–Dependent and –Independent Responses of the Chlamydomonas reinhardtii Transcriptome to Dark Anoxia journal September 2013
The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales journal January 2006
A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii: A revised mineral nutrient supplement for Chlamydomonas journal March 2011
Superoxide poisons mononuclear iron enzymes by causing mismetallation: Superoxide poisons mononuclear iron enzymes journal June 2013
A Conserved Family of Prolyl-4-Hydroxylases That Modify HIF journal October 2001
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions journal October 2007
Activation of Autophagy by Metals in Chlamydomonas reinhardtii journal July 2015
Analysis of the High-Affinity Iron Uptake System at the Chlamydomonas reinhardtii Plasma Membrane journal March 2010
Copper-Dependent Iron Assimilation Pathway in the Model Photosynthetic Eukaryote Chlamydomonas reinhardtii journal October 2002
Copper Response Element and Crr1-Dependent Ni 2+ -Responsive Promoter for Induced, Reversible Gene Expression in Chlamydomonas reinhardtii journal October 2003
BioVenn – a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams journal January 2008
An Optimized, Chemically Regulated Gene Expression System for Chlamydomonas journal September 2008
eulerAPE: Drawing Area-Proportional 3-Venn Diagrams Using Ellipses journal July 2014
Genetic Dissection of Nutritional Copper Signaling in Chlamydomonas Distinguishes Regulatory and Target Genes journal October 2004

Similar Records

Related Subjects

59 BASIC BIOLOGICAL SCIENCES