Drosophila dMRP4 regulates responsiveness to O2 deprivation and development under hypoxia

Physiological Genomics

Volumn 29, Issue 3, 2007, Pages 260-266

  Huang, He ^a   Haddad, Gabriel G ^a,b  

^a RADY CHILDREN'S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

ATP binding cassette transporter; Multidrug resistance associated protein; Overexpression; Oxygen deprivation; Screen; Survival

Indexed keywords

MULTIDRUG RESISTANCE PROTEIN 4; OXYGEN; DROSOPHILA PROTEIN; MRP4 PROTEIN, DROSOPHILA; MULTIDRUG RESISTANCE PROTEIN; UNCLASSIFIED DRUG;

ANOXIA; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DEVELOPMENT; DROSOPHILA; FLY; GENE MUTATION; GENE OVEREXPRESSION; GENETIC SCREENING; GLIA; GROWTH DISORDER; HYPOXIA; IN VIVO STUDY; LARVA; LETHALITY; LIFESPAN; MUSCLE; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; STUPOR; SURVIVAL; ANIMAL; ANIMAL EMBRYO; CELL HYPOXIA; DROSOPHILA MELANOGASTER; FEMALE; GENETIC TRANSFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OXYGEN CONSUMPTION; PHYSIOLOGY; PRENATAL DEVELOPMENT; TRANSGENIC ANIMAL;

DROSOPHILA MELANOGASTER; VERTEBRATA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL HYPOXIA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTATION; NEURONS; OXYGEN; OXYGEN CONSUMPTION; PHENOTYPE; TRANSFECTION;

EID: 34347270154     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00166.2006     Document Type: Article

References (45)

1. Awasaki T, Ito K. Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr Biol 14: 668-677, 2004.
2. Bacon NC, Wappner P, O'Rourke JF, Bartlett SM, Shilo B, Pugh CW, Ratcliffe PJ. Regulation of the Drosophila bHLH-PAS protein Sima by hypoxia: functional evidence for homology with mammalian HIF-1 alpha. Biochem Biophys Res Commun 249: 811-816, 1998.
3. Bickler PE, Donohoe PH, Buck LT. Molecular adaptations for survival during anoxia: lessons from lower vertebrates. Neuroscientist 8: 234-242, 2002.
4. Bickler PE, Hansen BM. Hypoxia-tolerant neonatal CA1 neurons: relationship of survival to evoked glutamate release and glutamate receptormediated calcium changes in hippocampal slices. Brain Res Dev Brain Res 106: 57-69, 1998.
5. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415, 1993.
6. Chen L, Rio DC, Haddad GG, Ma E. Regulatory role of dADAR in ROS metabolism in Drosophila CNS. Brain Res Mol Brain Res 131: 93-100, 2004.
7. Dean M, Annilo T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 6: 123-142, 2005.
8. Dean M, Rzhetsky A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11: 1156-1166, 2001.
9. DiGregorio PJ, Ubersax JA, O'Farrell PH. Hypoxia and nitric oxide induce a rapid, reversible cell cycle arrest of the Drosophila syncytial divisions. J Biol Chem 276: 1930-1937, 2001.
10. Donohoe PH, West TG, Boutilier RG. Factors affecting membrane permeability and ionic homeostasis in the cold-submerged frog. J Exp Biol 203: 405-414, 2000.
11. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247, 2000.
12. Floyd RA. Antioxidants, oxidative stress, and degenerative neurological disorders. Proc Soc Exp Biol Med 222: 236-245, 1999.
13. Giaccia AJ, Simon MC, Johnson R. The biology of hypoxia: the role of oxygen sensing in development, normal function, and disease. Genes Dev 18: 2183-2194, 2004.
14. Gorr TA, Gassmann M, Wappner P. Sensing and responding to hypoxia via HIF in model invertebrates. J Insect Physiol 52: 349-364, 2006.
15. Haddad GG. Enhancing our understanding of the molecular responses to hypoxia in mammals using Drosophila melanogaster. J Appl Physiol 88: 1481-1487, 2000.
16. 2: lessons from invertebrate genetic models. Exp Physiol 91: 277-282, 2006.
17. 2 deprivation induces a major depolarization in brain stem neurons in the adult but not in the neonatal rat. J Physiol 429: 411-428, 1990.
18. Haddad GG, Jiang C. Mechanisms of anoxia-induced depolarization in brainstem neurons: in vitro current and voltage clamp studies in the adult rat. Brain Res 625: 261-268, 1993.
19. 2 deprivation in Drosophila melanogaster. Proc Natl Acad Sci USA 94: 10809-10812, 1997.
20. Kraut R, Menon K, Zinn K. A gain-of-function screen for genes controlling motor axon guidance and synaptogenesis in Drosophila. Curr Biol 11: 417-430, 2001.
21. Krishnan SN, Sun Y, Mohsenin A, Wyman RJ, Haddad GG. Behavioral and electrophysiologic responses of drosophila melanogaster to prolonged periods of anoxia. J Insect Physiol 43: 203-210, 1997.
22. Lavista-Llanos S, Centanin L, Irisarri M, Russo DM, Gleadle JM, Bocca SN, Muzzopappa M, Ratcliffe PJ, Wappner P. Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein similar. Mol Cell Biol 22: 6842-6853, 2002.
23. Li H, Chaney S, Roberts IJ, Forte M, Hirsh J. Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr Biol 10: 211-214, 2000.
24. Lin DM, Goodman CS. Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13: 507-523, 1994.
25. Liu G, Roy J, Johnson EA. Identification and function of hypoxia-response genes in Drosophila melanogaster. Physiol Genomics 25: 134-141, 2006.
26. Lutz PL, Edwards R, McMahon PM. γ-Aminobutyric acid concentrations are maintained in anoxic turtle brain. Am J Physiol Regul Integr Comp Physiol 249: R372-R374, 1985.
27. 2 deprivation in Drosophila melanogaster. J Clin Invest 107: 685-693, 2001.
28. 2 deprivation: an anoxia-regulated novel gene in Drosophila melanogaster. Brain Res Mol Brain Res 63: 217-224, 1999.
29. Monnier V, Girardot F, Cheret C, Andres O, Tricoire H. Modulation of oxidative stress resistance in Drosophila melanogaster by gene overexpression. Genesis 34: 76-79, 2002.
30. Moreau-Fauvarque C, Taillebourg E, Boissoneau E, Mesnard J, Dura JM. The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies. Mech Dev 78: 47-61, 1998.
31. Nilsson GE. Turnover of serotonin in brain of an anoxia-tolerant vertebrate, the crucian carp. Am J Physiol Regul Integr Comp Physiol 258: R1308-R1312, 1990.
32. Palladino MJ, Keegan LP, O'Connell MA, Reenan RA. A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell 102: 437-449, 2000.
33. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L, Wijnholds J, Balzarini J, Borst P. Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 63: 1094-1103, 2003.
34. Rorth P. A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc Natl Acad Sci USA 93: 12418-12422, 1996.
35. Rorth P, Szabo K, Bailey A, Laverty T, Rehm J, Rubin GM, Weigmann K, Milan M, Benes V, Ansorge W, Cohen SM. Systematic gain-of-function genetics in Drosophila. Development 125: 1049-1057, 1998.
36. Schinkel AH, Jonker JW. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 55: 3-29, 2003.
37. Seeburg PH. RNA helicase participates in the editing game. Neuron 25: 261-263, 2000.
38. Sheps JA, Ralph S, Zhao Z, Baillie DL, Ling V. The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. Genome Biol 5: R15, 2004.
39. Sick TJ, Rosenthal M, LaManna JC, Lutz PL. Brain potassium ion homeostasis, anoxia, and metabolic inhibition in turtles and rats. Am J Physiol Regul Integr Comp Physiol 243: R281-R288, 1982.
40. Tarnay JN, Szeri F, Ilias A, Annilo T, Sung C, Le Saux O, Varadi A, Dean M, Boyd CD, Robinow S. The dMRP/CG6214 gene of Drosophila is evolutionarily and functionally related to the human multidrug resistance-associated protein family. Insect Mol Biol 13: 539-548, 2004.
41. Trauner M, Boyer JL. Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev 83: 633-671, 2003.
42. Ultsch GR, Jackson DC. Long-term submergence at 3 degrees C of the turtle Chrysemys picta bellii in normoxic and severely hypoxic water. III. Effects of changes in ambient PO2 and subsequent air breathing. J Exp Biol 97: 87-99, 1982.
43. Val AL. Oxygen transfer in fish: morphological and molecular adjustments. Braz J Med Biol Res 28: 1119-1127, 1995.
44. Van Aubel RA, Smeets PH, Peters JG, Bindels RJ, Russel FG. The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J Am Soc Nephrol 13: 595-603, 2002.
45. Wingrove JA, O'Farrell PH. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98: 105-114, 1999.