DNA damage and osmotic regulation in the kidney

American Journal of Physiology - Renal Physiology

Volumn 289, Issue 1 58-1, 2005, Pages

  Dmitrieva, Natalia I ^a   Burg, Maurice B ^a,b   Ferraris, Joan D ^a  

^a Laboratory of Kidney and Electrolyte Metabolism NHBLI   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Apoptosis; Cell cycle delay; Hypertonicity; Renal medulla

Indexed keywords

ATM PROTEIN; CHECKPOINT KINASE 1; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; HISTONE H2A; HYPERTONIC SOLUTION; KU ANTIGEN; MRE11 PROTEIN; PROTEIN P53; SODIUM CHLORIDE;

APOPTOSIS; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVATION; IN VIVO STUDY; KIDNEY CELL; KIDNEY CELL CULTURE; KIDNEY CONCENTRATING CAPACITY; KIDNEY MEDULLA; NONHUMAN; OSMOREGULATION; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

EID: 20844439227     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00041.2005     Document Type: Review

References (77)

1. Bakkenist CJ and Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506, 2003.
2. Bankir L. Urea and the kidney. In: The Kidney, edited by Brenner BM and Rector F. Philadelphia, PA: Saunders, 1996. p. 571-606.
3. Beck F, Dorge A, Rick R, and Thurau K. Intra- and extracellular element concentrations of rat renal papilla in antidiuresis. Kidney Int 25: 397-403, 1984.
4. Beere HM. "The stress of dying": the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 117: 2641-2651, 2004.
5. 2/M checkpoint symphony. Curr Opin Genes Dev 12: 92-97, 2002.
6. Bulavin DV, Higashimoto Y, Popoff IJ, Gaarde WA, Basrur V, Potapova O, Appella E, and Fornace AJ Jr. Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 411: 102-107, 2001.
7. Burg MB, Kwon ED, and Kultz D. Regulation of gene expression by hypertonicity. Annu Rev Physiol 59: 437-455, 1997.
8. Cai Q, Ferraris JD, and Burg MB. Greater tolerance of renal medullary cells for a slow increase in osmolality is associated with enhanced expression of HSP70 and other osmoprotective genes. Am J Physiol Renal Physiol 286: F58-F67, 2004.
9. Capasso JM, Rivard CJ, and Berl T. Long-term adaptation of renal cells to hypertonicity: role of MAP kinases and Na-K-ATPase. Am J Physiol Renal Physiol 280: F768-F776, 2001.
10. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio MJ, Redon C, Pilch DR, Olaru A, Eckhaus M, Camerini-Otero RD, Tessarollo L, Livak F, Manova K, Bonner WM, Nussenzweig MC, and Nussenzweig A. Genomic instability in mice lacking histone H2AX. Science 296: 922-927, 2002.
11. Chakravarty D, Cai Q, Ferraris JD, Michea L, Burg MB, and Kultz D. Three GADD45 isoforms contribute to hypertonic stress phenotype of murine renal inner medullary cells. Am J Physiol Renal Physiol 283: F1020-F1029, 2002.
12. Cohen DM, Wasserman JC, and Gullans SR. Immediate early gene and HSP70 expression in hyperosmotic stress in MDCK cells. Am J Physiol Cell Physiol 261: C594-C601, 1991.
13. Dahl SC, Handler JS, and Kwon HM. Hypertonicity-induced phosphorylation and nuclear localization of the transcription factor TonEBP. Am J Physiol Cell Physiol 280: C248-C253, 2001.
14. D'Amours D and Jackson SP. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat Rev Mol Cell Biol 3: 317-327, 2002.
15. De Boer J, Andressoo JO, de WJ, Huijmans J, Beems RB, van SH, Weeda G, van der Horst GT, van LW, Themmen AP, Meradji M, and Hoeijmakers JH. Premature aging in mice deficient in DNA repair and transcription. Science 296: 1276-1279, 2002.
16. Dmitireva NI and Burg MB. Importance of Ku86 for adaptation of cells to high NaCl (Abstract). J Am Soc Nephrol 15: 260A, 2004.
17. Dmitrieva N, Kultz D, Michea L, Ferraris J, and Burg M. Protection of renal inner medullary epithelial cells from apoptosis by hypertonic stress-induced p53 activation. J Biol Chem 275: 18243-18247, 2000.
18. Dmitrieva N, Michea L, and Burg MB. p53 Protects renal inner medullary cells from hypertonic stress by restricting DNA replication. Am J Physiol Renal Physiol 281: F522-F530, 2001.
19. Dmitrieva NI, Bulavin DV, and Burg MB. High NaCl causes Mre11 to leave the nucleus, disrupting DNA damage signaling and repair. Am J Physiol Renal Physiol 285: F266-F274, 2003.
20. Dmitrieva NI, Bulavin DV, Fornace AJ Jr, and Burg MB. Rapid activation of G2/M checkpoint after hypertonic stress in renal inner medullary epithelial (IME) cells is protective and requires p38 tease. Proc Natl Acad Sci USA 99: 184-189, 2002.
21. Dmitrieva NI and Burg MB. Living with DNA breaks is an everyday reality for cells adapted to high NaCl. Cell Cycle 3: 561-563, 2004.
22. Dmitrieva NI and Burg MB. Hypertonic stress response. Mutat Res 569: 65-74, 2005.
23. Dmitrieva NI, Cai Q, and Burg MB. Cells adapted to high NaCl have many DNA breaks and impaired DNA repair both in cell culture and in vivo. Proc Natl Acad Sci USA 101: 2317-2322, 2004.
24. Fei P and El-Deiry WS. P53 and radiation responses. Oncogene 22: 5774-5783, 2003.
25. Fenton RA, Chou CL, Stewart GS, Smith CP, and Knepper MA. Urinary concentrating defect in mice with selective deletion of phloretin-sensitive urea transporters in the renal collecting duct. Proc Natl Acad Sci USA 101: 7469-7474, 2004.
26. Ferraris JD, Persaud P, Williams CK, Chen Y, and Burg MB. cAMP-independent role of PKA in tonicity-induced transactivation of tonicity-responsive enhancer/osmotic response element-binding protein. Proc Natl Acad Sci USA 99: 16800-16805, 2002.
27. Ferraris JD, Williams CK, Persaud P, Zhang Z, Chen Y, and Burg MB. Activity of the TonEBP/OREBP transactivation domain varies directly with extracellular NaCl concentration. Proc Natl Acad Sci USA 99: 739-744, 2002.
28. Garner MM and Burg MB. Macromolecular crowding and confinement in cells exposed to hypertonicity. Am J Physiol Cell Physiol 266: C877-C892, 1994.
29. Han J, Lee JD, Bibbs L, and Ulevitch RJ. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265: 808-811, 1994.
30. Hasty P and Vijg J. Aging. Genomic priorities in aging. Science 296: 1250-1251, 2002.
31. Hoffmann EK and Simonsen LO. Membrane mechanisms in volume and pH regulation in vertebrate cells. Physiol Rev 69: 315-382, 1989.
32. Iliakis G, Wang Y, Guan J, and Wang H. DNA damage checkpoint control in cells exposed to ionizing radiation. Oncogene 22: 5834-5847, 2003.
33. Irarrazabal CE, Liu JC, Burg MB, and Ferraris JD. ATM, a DNA damage-inducible kinase, contributes to activation by high NaCl of the transcription factor TonEBP/OREBP. Proc Natl Acad Sci USA 101: 8809-8814, 2004.
34. Itoh T, Vamauchi A, Miyai A, Yokoyama K, Kamada T, Ueda N, and Fujiwara Y. Mitogen-activated protein kinase and its activator are regulated by hypertonic stress in Madin-Darby canine kidney cells. J Clin Invest 93: 2387-2392, 1994.
35. Kitamura H, Yamauchi A, Sugiura T, Matsuoka Y, Horio M, Tohyama M, Shimada S, Imai E, and Hori M. Inhibition of myo-inositol transport causes acute renal failure with selective medullary injury in the rat. Kidney Int 53: 146-153, 1998.
36. Ko BC, Lam AK, Kapus A, Fan L, Chung SK, and Chung SS. Fyn and p38 signaling are both required for maximal hypertonic activation of the OREBP/TonEBP. J Biol Chem 277: 46085-46092, 2002.
37. Ko BC, Turck CW, Lee KW, Yang Y, and Chung SS. Purification, identification, and characterization of an osmotic response element binding protein. Biochem Biophys Res Commun 270: 52-61, 2000.
38. Kultz D. Osmotic regulation of DNA activity and the cell cycle. In: Environmental Stresses and Gene Responses, edited by Storey KB and Storey J. New York: Elsevier, 2000, p. 157-179.
39. Kultz D. Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67: 225-257, 2005.
40. Kultz D and Chakravarty D. Hyperosmolality in the form of elevated NaCl but not urea causes DNA damage in murine kidney cells. Proc Natl Acad Sci USA 98: 1999-2004, 2001.
41. Kultz D, Madhany S, and Burg MB. Hyperosmolality causes growth arrest of murine kidney cells. Induction of GADD45 and GADD153 by osmosensing via stress-activated protein kinase 2. J Biol Chem 273: 13645-13651, 1998.
42. Luo G, Yao MS, Bender CF, Mills M, Bladl AR, Bradley A, and Petrini JH. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc Natl Acad Sci USA 96: 7376-7381, 1999.
43. Mak SK and Kultz D. Gadd45 proteins induce G2/M arrest and modulate apoptosis in kidney cells exposed to hyperosmotic stress. J Biol Chem 279: 39075-39084, 2004.
44. Matsuda S, Kawasaki H, Moriguchi T, Gotoh Y, and Nishida E. Activation of protein kinase cascades by osmotic shock. J Biol Chem 270: 12781-12786, 1995.
45. Meek K, Gupta S, Ramsden DA, and Lees-Miller SP. The DNA-dependent protein kinase: the director at the end. Immunol Rev 200: 132-141, 2004.
46. Michea L, Ferguson DR, Peters EM, Andrews PM, Kirby MR, and Burg MB. Cell cycle delay and apoptosis are induced by high salt and urea in renal medullary cells. Am J Physiol Renal Physiol 278: F209-F218, 2000.
47. Miyakawa H, Woo SK, Dahl SC, Handler JS, and Kwon HM. Tonicity-responsive enhancer binding protein, a Rel-like protein that stimulates transcription in response to hypertonicity. Proc Natl Acad Sci USA 96: 2538-2542, 1999.
48. Nakanishi T, Balaban RS, and Burg MB. Survey of osmolytes in renal cell lines. Am J Physiol Cell Physiol 255: C181-C191, 1988.
49. Nakayama Y, Peng T, Sands JM, and Bagnasco SM. The TonE/ TonEBP pathway mediates tonicity-responsive regulation of UT-A urea transporter expression. J Biol Chem 275: 38275-38280, 2000.
50. Neuhofer W, Muller E, Burger-Kentischer A, Fraek ML, Thurau K, and Beck F. Pretreatment with hypertonic NaCl protects MDCK cells against high urea concentrations. Pflügers Arch 435: 407-414, 1998.
51. Neuhofer W, Woo SK, Na KY, Grunbein R, Park WK, Nahm O, Beck FX, and Kwon HM. Regulation of TonEBP transcriptional activator in MDCK cells following changes in ambient tonicity. Am J Physiol Cell Physiol 283: C1604-C1611, 2002.
52. Park Y and Gerson SL. DNA repair defects in stem cell function and aging. Annu Rev Med 56: 495-508, 2005.
53. Pastink A, Eeken JC, and Lohman PH. Genomic integrity and the repair of double-strand DNA breaks. Mutat Res 480-481: 37-50, 2001.
54. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, and Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886-895, 2000.
55. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, and Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868, 1998.
56. Santos BC, Pullman JM, Chevaile A, Welch WJ, and Gullans SR. Chronic hyperosmolarity mediates constitutive expression of molecular chaperones and resistance to injury. Am J Physiol Renal Physiol 284: F564-F574, 2003.
57. Sheikh-Hamad D, Di Mari J, Suki WN, Safirstein R, Watts BA III, and Rouse D. p38 Kinase activity is essential for osmotic induction of mRNAs for HSP70 and transporter for organic solute betaine in Madin-Darby canine kidney cells. J Biol Chem 273: 1832-1837, 1998.
58. Sheikh-Hamad D, Garcia-Perez A, Ferraris JD, Peters EM, and Burg MB. Induction of gene expression by heat shock versus osmotic stress. Am J Physiol Renal Fluid Electrolyte Physiol 267: F28-F34, 1994.
59. Sheikh-Hamad D and Gustin MC. MAP kinases and the adaptive response to hypertonicity: functional preservation from yeast to mammals. Am J Physiol Renal Physiol 287: F1102-F1110, 2004.
60. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3: 155-168, 2003.
61. Shim EH, Kim JI, Bang ES, Heo JS, Lee JS, Kim EY, Lee JE, Park WY, Kim SH, Kim HS, Smithies O, Jang JJ, Jin DI, and Seo JS. Targeted disruption of hsp70.1 sensitizes to osmotic stress. EMBO Rep 3: 857-861, 2002.
62. Smith GC and Jackson SP. The DNA-dependent protein kinase. Genes Dev 13: 916-934, 1999.
63. Terada Y, Inoshita S, Kanada S, Shimamura H, Kuwahara M, Ogawa W, Kasuga M, Sasaki S, and Marumo F. Hyperosmolality activates Akt and regulates apoptosis in renal tubular cells. Kidney Int 60: 553-567, 2001.
64. Uchida S, Garcia-Perez A, Murphy H, and Burg M. Signal for induction of aldose reductase in renal medullary cells by high external NaCl. Am J Physiol Cell Physiol 256: C614-C620, 1989.
65. Uhlik MT, Abell AN, Johnson NL, Sun W, Cuevas BD, Lobel-Rice KE, Horne EA, Dell'Acqua ML, and Johnson GL. Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat Cell Biol 5: 1104-1110, 2003.
66. Vilenchik MM and Knudson AG. Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci USA 100: 12871-12876, 2003.
67. Walker JR, Corpina RA, and Goldberg J. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 412: 607-614, 2001.
68. Woo SK, Dahl SC, Handler JS, and Kwon HM. Bidirectional regulation of tonicity-responsive enhancer binding protein in response to changes in tonicity. Am J Physiol Renal Physiol 278: F1006-F1012, 2000.
69. Woo SK, Lee SD, Na KY, Park WK, and Kwon HM. TonEBP/NFAT5 stimulates transcription of HSP70 in response to hypertonicity. Mol Cell Biol 22: 5753-5760, 2002.
70. Xanthoudakis S and Nicholson DVV. Heat-shock proteins as death determinants. Nat Cell Biol 2: E163-E165, 2000.
71. Xiao Y and Weaver DT. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res 25: 2985-2991, 1997.
72. Yancey PH, Burg MB, and Bagnasco SM. Effects of NaCl, glucose, and aldose reductase inhibitors on cloning efficiency of renal medullary cells. Am J Physiol Cell Physiol 258: C156-C163, 1990.
73. Yancey PH, Clark ME, Hand SC, Bowlus RD, and Somero GN. Living with water stress: evolution of osmolyte systems. Science 217: 1214-1222, 1982.
74. Zhang Z, Cai Q, Michea L, Dmitrieva N, Andrews P, and Burg M. Proliferation and osmotic tolerance of renal inner medullary epithelial cells in vivo and in cell culture. Am J Physiol Renal Physiol 283: F203-F208, 2002.
75. Zhang Z, Dmitrieva NI, Park JH, Levine RL, and Burg MB. High urea and NaCl carbonylate proteins in renal cells in culture and in vivo, and high urea causes 8-oxoguanine lesions in their DNA. Proc Natl Acad Sci USA 101: 9491-9496, 2004.
76. Zhou X, Ferraris JD, and Burg MB. Superoxides contribute to activation of TonEBP/OREBP by high NaCl (Abstract). J Am Soc Nephrol 15: 88A, 2005.
77. Zhu J, Petersen S, Tessarollo L, and Nussenzweig A. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr Biol 11: 105-109, 2001.