Androgen receptor enhances kidney stone-CaOx crystal formation via modulation of oxalate biosynthesis & oxidative stress

Molecular Endocrinology

Volumn 28, Issue 8, 2014, Pages 1291-1303

  Liang, Liang ^a,b   Li, Lei ^a,b   Tian, Jing ^a   Lee, Soo Ok ^a   Dang, Qiang ^a,b   Huang, Chiung Kuei ^c   Yeh, Shuyuan ^c   Erturk, Erdal ^c   Bushinsky, David ^c   Chang, Luke S ^a,b   He, Dalin ^b   Chang, Chawnshang ^d  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b George H Whipple Laboratory for Cancer Research   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^d CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; CALCIUM OXALATE; GLYOXYLIC ACID; HYDROXY ACID OXIDASE A; OXALIC ACID; PROTEIN P22; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; WHEWELLITE; 1,7-BIS(4-HYDROXY-3-METHOXYPHENYL)-1,4,6-HEPTATRIEN-3-ONE; CURCUMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; KIDNEY EPITHELIUM; KIDNEY INJURY; MAJOR CLINICAL STUDY; MALE; METABOLISM; MODULATION; MOUSE; NEPHROLITHIASIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; HEPG2 CELL LINE; KIDNEY CALCULI; KNOCKOUT MOUSE; PROTEIN DEGRADATION; SEX RATIO; SEXUAL DEVELOPMENT;

ANIMALS; CALCIUM OXALATE; CASE-CONTROL STUDIES; CURCUMIN; FEMALE; HEK293 CELLS; HEP G2 CELLS; HUMANS; KIDNEY CALCULI; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATIVE STRESS; PROTEOLYSIS; RECEPTORS, ANDROGEN; SEX CHARACTERISTICS; SEX DISTRIBUTION;

EID: 84905228306     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1047     Document Type: Article

References (69)

1. Buchholz NP, Abbas F, Afzal M, Khan R, Rizvi I, Talati J. The prevalence of silent kidney stones-an ultrasonographic screening study. J Pak Med Assoc. 2003;53:24-25.
2. Indridason OS, Birgisson S, Edvardsson VO, Sigvaldason H, Sigfusson N, Palsson R. Epidemiology of kidney stones in Iceland: a population-based study. Scand J Urol Nephrol. 2006;40:215-220.
3. Goldfarb DS. Increasing prevalence of kidney stones in the United States. Kidney Int. 2003;63:1951-1952.
4. Worcester EM, Coe FL. Clinical practice. Calcium kidney stones. N Engl J Med. 2010;363:954-963.
5. Watson JM, Shrewsberry AB, Taghechian S, et al. Serum testosterone may be associated with calcium oxalate urolithogenesis. J Endourol. 2010;24:1183-1187.
6. Sarada B, Satyanarayana U. Urinary composition in men and women and the risk of urolithiasis. Clin Biochem. 1991;24:487-490.
7. Yagisawa T, Ito F, Osaka Y, Amano H, Kobayashi C, Toma H. The influence of sex hormones on renal osteopontin expression and urinary constituents in experimental urolithiasis. J Urol. 2001;166: 1078-1082.
8. Fan J, Chandhoke PS, Grampsas SA. Role of sex hormones in experimental calcium oxalate nephrolithiasis. J Am Soc Nephrol 1999;10(suppl 14):S376-S380.
9. Lee YH, Huang WC, Chiang H, Chen MT, Huang JK, Chang LS. Determinant role of testosterone in the pathogenesis of urolithiasis in rats. J Urol. 1992;147:1134-1138.
10. Yoshioka I, Tsujihata M, Momohara C, Akanae W, Nonomura N, Okuyama A. Effect of sex hormones on crystal formation in a stone-forming rat model. Urology. 2010;75:907-913.
11. Li JY, Zhou T, Gao X, et al. Testosterone and androgen receptor in human nephrolithiasis. J Urol. 2010;184:2360-2363.
12. Wu MH, Ma WL, Hsu CL, et al. Androgen receptor promotes hepatitis B virus-induced hepatocarcinogenesis through modulation of hepatitis B virus RNA transcription. Sci Transl Med. 2010; 2:32r-35r.
13. Miyamoto H, Yang Z, Chen YT, et al. Promotion of bladder cancer development and progression by androgen receptor signals. J Natl Cancer Inst. 2007;99:558-568.
14. Lai KP, Yamashita S, Huang CK, Yeh S, Chang C. Loss of stromal androgen receptor leads to suppressed prostate tumourigenesis via modulation of pro-inflammatory cytokines/chemokines. EMBO Mol Med. 2012;8:791-807.
15. Yang Z, Chang YJ, Yu IC, et al. ASC-J9 ameliorates spinal and bulbar muscular atrophy phenotype via degradation of androgen receptor. Nat Med. 2007;13:348-353.
16. Yeh S, Tsai MY, Xu Q, et al. Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc Natl Acad Sci USA. 2002;99:13498-13503.
17. Ma WL, MA CL, Hsu CL, et al. Androgen receptor is a new potential therapeutic target for the treatment of hepatocellular carcinoma. Gastroenterology 2008;135:947-955.
18. Akerman ME, Pilch J, Peters D, Ruoslahti E. Angiostatic peptides use plasma fibronectin to home to angiogenic vasculature. Proc Natl Acad Sci USA. 2005;102:2040-2045.
19. Li H, Zhou X, Davis DR, Xu D, Sigmund CD. An androgen-inducible proximal tubule-specific Cre recombinase transgenic model. Am J Physiol Renal Physiol. 2008;294:F1481-F1486.
20. Shao X, Somlo S, Igarashi P. Epithelial-specific Cre/lox recombination in the developing kidney and genitourinary tract. J Am Soc Nephrol. 2002;13:1837-1846.
21. Okada A, Nomura S, Higashibata Y, et al. Successful formation of calcium oxalate crystal deposition in mouse kidney by intraabdominal glyoxylate injection. Urol Res. 2007;35:89-99.
22. Khand FD, Gordge MP, Robertson WG, Noronha-Dutra AA, Hothersall JS. Mitochondrial superoxide production during oxalate- mediated oxidative stress in renal epithelial cells. Free Radic Biol Med. 2002;32:1339-1350.
23. Lieske JC, Norris R, Swift H, Toback FG. Adhesion, internalization and metabolism of calcium oxalate monohydrate crystals by renal epithelial cells. Kidney Int. 1997;52:1291-1301.
24. Remmele W, Stegner HE. Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe. 1987;8:138-140.
25. Li L, Xie H, Liang L, et al. Increased PrLZ-mediated androgen receptor transactivation promotes prostate cancer growth at castration- resistant stage. Carcinogenesis. 2013;34:257-267.
26. Ma Y, Mehta SL, Lu B, Li PA. Deficiency in the inner mitochondrial membrane peptidase 2-like (Immp21) gene increases ischemic brain damage and impairs mitochondrial function. Neurobiol Dis. 2011; 44:270-276.
27. Liu NC, Lin WJ, Yu IC, et al. Activation of TR4 orphan nuclear receptor gene promoter by cAMP/PKA and C/EBP signaling. Endocrine. 2009;36:211-217.
28. Yang L, Xie S, Jamaluddin MS, et al. Induction of androgen receptor expression by phosphatidylinositol 3-kinase/Akt downstream substrate, FOXO3a, and their roles in apoptosis of LNCaP prostate cancer cells. J Biol Chem. 2005;280:33558-33565.
29. Niu Y, Yeh S, Miyamoto H, et al. Tissue prostate-specific antigen facilitates refractory prostate tumor progression via enhancing ARA70-regulated androgen receptor transactivation. Cancer Res. 2008;68:7110-7119.
30. Knight J, Assimos DG, Easter L, Holmes RP. Metabolism of fructose to oxalate and glycolate. Horm Metab Res. 2010;42:868-873.
31. Baker PR, Cramer SD, Kennedy M, Assimos DG, Holmes RP. Glycolate and glyoxylate metabolism in HepG2 cells.AmJ Physiol Cell Physiol. 2004;287:C1359-C1365.
32. Postic C, Shiota M, Niswender KD, et al. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic _ cell-specific gene knock-outs using Cre recombinase. J Biol Chem. 1999;274:305-315.
33. Jones JM, Morrell JC, Gould SJ. Identification and characterization of HAOX1, HAOX2, and HAOX3, three human peroxisomal 2-hydroxy acid oxidases. J Biol Chem. 2000;275:12590-12597.
34. Kohler SA, Menotti E, Kühn LC. Molecular cloning of mouse glycolate oxidase. High evolutionary conservation and presence of an iron-responsive element-like sequence in the mRNA. J Biol Chem. 1999;274:2401-2407.
35. Nelson JD, Denisenko O, Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat Protoc. 2006;1: 179-185.
36. Hirose M, Yasui T, Okada A, et al. Renal tubular epithelial cell injury and oxidative stress induce calcium oxalate crystal formation in mouse kidney. Int J Urol. 2010;17:83-92.
37. Davalos M, Konno S, Eshghi M, Choudhury M. Oxidative renal cell injury induced by calcium oxalate crystal and renoprotection with antioxidants: a possible role of oxidative stress in nephrolithiasis. J Endourol. 2010;24:339-345.
38. Zuo J, Khan A, Glenton PA, Khan SR. Effect of NADPH oxidase inhibition on the expression of kidney injury molecule and calcium oxalate crystal deposition in hydroxy-L-proline-induced hyperoxaluria in the male Sprague-Dawley rats. Nephrol Dial Transplant. 2011;26:1785-1796.
39. Haider L, Fischer MT, Frischer JM, et al. Oxidative damage in multiple sclerosis lesions. Brain. 2011;134:1914-1924.
40. Werner SR, Prahalad AK, Yang J, Hock JM. RECQL4-deficient cells are hypersensitive to oxidative stress/damage: Insights for osteosarcoma prevalence and heterogeneity in Rothmund-Thomson syndrome. Biochem Biophys Res Commun. 2006;345:403-409.
41. Nielsen VK, Kemp E, Laursen T. Lactic dehydrogenase in kidney tissue and renal disease. Adaptive change of the synthesis in acute failure. Acta Med Scand. 1968;184:109-119.
42. Nakano Y, Banfi B, Jesaitis AJ, Dinauer MC, Allen LA, Nauseef WM. Critical roles for p22phox in the structural maturation and subcellular targeting of Nox3. Biochem J. 2007;403:97-108.
43. Khan SR, Khan A, Byer KJ. Temporal changes in the expression of mRNAofNADPHoxidase subunits in renal epithelial cells exposed to oxalate or calcium oxalate crystals. Nephrol Dial Transplant. 2011;26:1778-1785.
44. Impellizzeri D, Esposito E, Mazzon E, et al. Effect of apocynin, a NADPH oxidase inhibitor, on acute lung inflammation. Biochem Pharmacol. 2011;81:636-648.
45. Lai KP, Yamashita S, Huang CK, Yeh S, Chang C. Loss of stromal androgen receptor leads to suppressed prostate tumourigenesis via modulation of pro-inflammatory cytokines/chemokines. EMBO Mol Med. 2012;4:791-807.
46. Negri AL, Spivacow FR, Del Valle EE, Forrester M, Rosende G, Pinduli I. Role of overweight and obesity on the urinary excretion of promoters and inhibitors of stone formation in stone formers. Urol Res. 2008;36:303-307.
47. Borghi L, Meschi T, Guerra A, et al. Essential arterial hypertension and stone disease. Kidney Int. 1999;55:2397-2406.
48. Weinberg AE, Patel CJ, Chertow GM, Leppert JT. Diabetic severity and risk of kidney stone disease. Eur Urol. 2014;65:242-247.
49. Robijn S, Hoppe B, Vervaet BA, D'Haese PC, Verhulst A. Hyperoxaluria: a gut-kidney axis? Kidney Int. 2011;11:1146-1158.
50. Fargue S, Lewin J, Rumsby G, Danpure CJ. Four of the most common mutations in primary hyperoxaluria type 1 unmask the cryptic mitochondrial targeting sequence of alanine:glyoxylate aminotransferase encoded by the polymorphic minor allele. J Biol Chem. 2013;288:2475-2484.
51. Hirose M, Tozawa K, Okada A, et al. Glyoxylate induces renal tubular cell injury and microstructural changes in experimental mouse. Urol Res. 2008;36:139-147.
52. Thamilselvan S, Khan SR, Menon M. Oxalate and calcium oxalate mediated free radical toxicity in renal epithelial cells: effect of antioxidants. Urol Res. 2003;31:3-9.
53. Tam NN, Gao Y, Leung YK, Ho SM. Androgenic regulation of oxidative stress in the rat prostate: involvement of NAD(P)H oxidases and antioxidant defense machinery during prostatic involution and regrowth. Am J Pathol. 2003;163:2513-2522.
54. Calo LA, Davis PA. NADPH oxidase subunits (NOX-1, p22phox, Rac-1) and tacrolimus-induced nephrotoxicity in a rat renal transplant model. Nephrol Dial Transplant 2007;22:2402.
55. Khan SR. Is oxidative stress, a link between nephrolithiasis and obesity, hypertension, diabetes, chronic kidney disease, metabolic syndrome? Urol Res. 2012;40:95-112.
56. Yoshihara H, Yamaguchi S, Yachiku S. Effect of sex hormones on oxalate-synthesizing enzymes in male and female rat livers. J Urol. 1999;161:668-673.
57. Regeer RR, Lee A, Markovich D. Characterization of the human sulfate anion transporter (hsat-1) protein and gene (SAT1; SLC26A1). DNA Cell Biol. 2003;22:107-117.
58. Stieger B. Regulation of the expression of the hepatocellular sulfateoxalate exchanger SAT-1 (SLC26A1) by glyoxylate: a metabolic link between liver and kidney? J Hepatol. 2011;54:406-407.
59. Krambeck AE, LeRoy AJ, Patterson DE, Gettman MT. Long-term outcomes of percutaneous nephrolithotomy compared to shock wave lithotripsy and conservative management. J Urol. 2008;179: 2233-2237.
60. Xue YQ, He DL, Chen XF, Li X, Zeng J, Wang XY. Shock wave induced kidney injury promotes calcium oxalate deposition. J Urol. 2009;182:762-765.
61. Borghi L, Meschi T, Amato F, et al. Urinary volume, water and recurrences in idiopathic calcium nephrolithiasis: a 5-year randomized prospective study. J Urol. 1996;155:839-843.
62. Taylor EN, Curhan GC. Diet and fluid prescription in stone disease. Kidney Int. 2006;70:835-839.
63. Seitz C, Liatsikos E, Porpiglia F, Tiselius HG, Zwergel U. Medical therapy to facilitate the passage of stones: what is the evidence? Eur Urol. 2009;56:455-471.
64. Pak CY, Sakhaee K, Fuller C. Successful management of uric acid nephrolithiasis with potassium citrate. Kidney Int. 1986;30:422-428.
65. Mortensen JT, Schultz A, Ostergaard AH. Thiazides in the prophylactic treatment of recurrent idiopathic kidney stones. Int Urol Nephrol. 1986;18:265-269.
66. Liatsikos EN, Katsakiori PF, Assimakopoulos K, et al. Doxazosin for the management of distal-ureteral stones. J Endourol. 2007;21: 538-541.
67. Moe OW. Kidney stones: pathophysiology and medical management. Lancet. 2006;367:333-344.
68. Coe FL, Evan A, Worcester E. Kidney stone disease. J Clin Invest. 2005;115:2598-2608.
69. Coe FL, Evan AP, Worcester EM, Lingeman JE. Review: Three pathways for human kidney stone formation. Urol Res. 2010;38:147-160.