Macro Ck2 Accumulation in Tenofovir-Treated HIV Patients is Facilitated by Ck Oligomer Stabilization but is Not Predictive for Pathology

Lee K.N. , Csako G. , Bernhardt P. , Elin R.J. Relevance of macro creatine kinase type 1 and type 2 isoenzymes to laboratory and clinical data. Clin Chem 1994; 40: 1278–1283.

Schmid H. , Mühlbayer D. , Röling J. Macroenzyme creatine kinase (CK) type 2 in HIV-infected patients is significantly associated with TDF and consists of ubiquitous mitochondrial CK. Antivir Ther 2006; 11: 1071–1080.

Qin W. , Khuchua Z. , Cheng J. , Boero J. , Payne R.M. , Strauss A.W. Molecular characterization of the creatine kinases and some historical perspectives. Mol Cell Biochem 1998; 184: 153–167.

Schlattner U. , Tokarska-Schlattner M. , Wallimann T. Mitochondrial creatine kinase in human health and disease. Biochim Biophys Acta 2006; 1762: 164–180.

Wallimann T. , Hemmer W. Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 1994; 133–134: 193–220.

Wallimann T. , Tokarska-Schlattner M. , Schlattner U. The creatine kinase system and pleiotropic effects of creatine. Amino Acids 2011; 40: 1271–1296.

Neumann D. , Schlattner U. , Wallimann T. A molecular approach to the concerted action of kinases involved in energy homeostasis. Biochem Soc Trans 2003; 31: 169–174.

Soboll S. , Brdiczka D. , Jahnke D. Octamer-dimer transitions of mitochondrial creatine kinase in heart muscle. J Mol Cell Cardiol 1999; 31: 857–866.

Tokarska-Schlattner M. , Zaugg M. , da Silva R. Acute toxicity of doxorubicin on isolated perfused heart: response of kinases regulating energy supply. Am J Physiol Heart Circ Physiol 2005; 289: H37–H47.

Tokarska-Schlattner M. , Dolder M. , Gerber I. , Speer O. , Wallimann T. , Schlattner U. Reduced creatine stimulated respiration in doxorubicin challenged mitochondria: particular sensitivity of the heart. Biochim Biophys Acta 2007; 1767: 1276–1284.

Schlattner U. , Wallimann T. Octamers of mitochondrial creatine kinase differ in stability and membrane binding. J Biol Chem 2000; 275: 17314–17320.

Koch K. , Chen Y.X. , Feng J.Y. Nucleoside diphosphate kinase and the activation of antiviralphosphonate analogs of nucleotides: binding mode and phosphorylation of tenofovirderivatives. Nucleosides Nucleotides Nucleic Acids 2009; 28: 776–792.

Johnson A.A. , Ray A.S. , Hanes J. Toxicity of antiviral nucleoside analogs and the human mitochondrial DNA polymerase. J Biol Chem 2001; 276: 40847–40857.

Rodriguez-Nóvoa S. , Alvarez E. , Labarga P. , Soriano V. Renal toxicity associated with tenofovir use. Expert Opin Drug Saf 2010; 9: 545–559.

Herlitz L.C. , Mohan S. , Stokes M.B. , Radhakrishnan J. , D'Agati V.D. , Markowitz G.S. Tenofovir nephrotoxicity: acute tubular necrosis with distinctive clinical, pathological, and mitochondrial abnormalities. Kidney Int 2010; 78: 1171–1177.

Cooper R.D. , Tonelli M. Renal disease associated with antiretroviral therapy in the treatment of HIV. Nephron Clin Pract 2011; 118: c262–c268.

Fernandez-Fernandez B. , Montoya-Ferrer A. , Sanz A.B. Tenofovir nephrotoxicity: 2011 update. Aids Res Treat 2011; 2011: 354908.

Claas G.J. , Jülg B. , Goebel F.D. , Bogner J.R. Metabolic and anthropometric changes one year after switching from didanosine/stavudine to tenofovir in HIV-infected patients. Eur J Med Res 2007; 12: 54–60.

Stevens L.A. , Coresh J. , Greene T. , Levey A.S. Assessing kidney function–measured and estimated glomerular filtration rate. N Engl J Med 2006; 354: 2473–2483.

Cockcroft D.W. , Gault M.H. Prediction of creatinine clearance from serum creatinine. Nephron 1976; 16: 31–41.

Schlattner U. , Eder M. , Dolder M. , Khuchua Z.A. , Strauss A.W. , Wallimann T. Divergent enzyme kinetics and structural properties of the two human mitochondrial creatine kinase isoenzymes. Biol Chem 2000; 381: 1063–1070.

Schlattner U. , Reinhart C. , Hornemann T. , Tokarska-Schlattner M. , Wallimann T. Single chain Fv antibodies directed against cytosolic creatine kinase isolated from a synthetic human phage display library. Biochim Biophys Acta 2002; 1579: 124–132.

Tokarska-Schlattner M. , Boissan M. , Munier A. The nucleoside diphosphate kinase D (nm23-H4) binds the mitochondrial inner membrane with high affinity to cardiolipin and couples nucleotide transfer with respiration. J Biol Chem 2008; 283: 26198–26207.

Wallimann T. , Schlösser T. , Eppenberger H.M. Function of M-line-bound creatine kinase as intramyofibrillar ATP regenerator at the receiving end of thephosphorylcreatine shuttle in muscle. J Biol Chem 1984; 259: 5238–5246.

Eder M. , Fritz-Wolf K. , Kabsch W. , Wallimann T. , Schlattner U. Crystal structure of human ubiquitous creatine kinase. Proteins 2000; 39: 216–225.

Tokarska-Schlattner M. , Wallimann T. , Schlattner U. Multiple interference of anthracyclines with mitochondrial creatine kinases: preferential damage of the cardiac isoenzyme and its implications for drug cardiotoxicity. Mol Pharmacol 2002; 61: 516–523.

Neumann D. , Woods A. , Carling D. , Wallimann T. , Schlattner U. Mammalian AMP-activated protein kinase: functional, heterotrimeric complexes by co-expression of subunits in Escherichia coli. Protein Expr Purif 2003; 30: 230–237.

Stein W. , Bohner J. , Renn W. , Maulbetsch R. Macro creatine kinase type 2: results of a prospective study in hospitalized patients. Clin Chem 1985; 31: 1959–1964.

Mercer D.W. , Talamo T.S. Multiple markers of malignancy in sera of patients with colorectal carcinoma: preliminary clinical studies. Clin Chem 1985; 31: 1824–1828.

Kiser J.J. , Aquilante C.L. , Anderson P.L. , King T.M. , Carten M.L. , Fletcher C.V. Clinical and genetic determinants of intracellular tenofovir diphosphate concentrations in HIV-infected patients. J Acquir Immune Defic Syndr 2008; 47: 298–303.

Millar I.D. , Hartley J.A. , Haigh C. Volume regulation is defective in renal proximal tubule cells isolated from KCNE1 knockout mice. Exp Physiol 2004; 89: 173–180.

Izzedine H. , Harris M. , Perazella M.A. The nephrotoxic effects of HAART. Nat Rev Nephrol 2009; 5: 563–573.

Kohler J.J. , Hosseini S.H. , Hoying-Brandt A. Tenofovir renal toxicity targets mitochondria of renal proximal tubules. Lab Invest 2009; 89: 513–519.

Lee H. , Hanes J. , Johnson K.A. Toxicity of nucleoside analogues used to treat AIDS and the selectivity of the mitochondrial DNA polymerase. Biochemistry 2003; 42: 14711–14719.

Perazella M.A. Tenofovir-induced kidney disease: an acquired renal tubular mitochondriopathy. Kidney Int 2010; 78: 1060–1063.

Guerrero M.L. , Beron J. , Spindler B. , Groscurth P. , Wallimann T. , Verrey F. Metabolic support of Na⁺ pump in apically permeabilized A6 kidney cell epithelia: role of creatine kinase. Am J Physiol 1997; 272: C697–C706.

Calza L. , Trapani F. , Tedeschi S. Tenofovir-induced renal toxicity in 324 HIV-infected, antiretroviral-naïve patients. Scand J Infect Dis 2011; 43: 656–660.

Cooper R.D. , Wiebe N. , Smith N. , Keiser P. , Naicker S. , Tonelli M. Systematic review and meta-analysis: renal safety of tenofovir disoproxil fumarate in HIV-infected patients. Clin Infect Dis 2010; 51: 496–505.

Mocroft A. , Kirk O. , Reiss P. Estimated glomerular filtration rate, chronic kidney disease and antiretroviral drug use in HIV-positive patients. AIDS 2010; 24: 1667–1678.

Vrouenraets S.M. , Fux C.A. , Wit F.W. Persistent decline in estimated but not measured glomerular filtration rate on tenofovir may refect tubular rather than glomerular toxicity. AIDS 2011; 25: 2149–2155.

Vrouenraets S.M. , Fux C.A. , Wit F.W. A comparison of measured and estimated glomerular filtration rate in successfully treated HIV-patients with preserved renal function. Clin Nephrol 2012; 77: 311–320.

Albini L. , Cesana B.M. , Motta D. A randomized, pilot trial to evaluate glomerular filtration rate by creatinine or cystatin C in naive HIV-infected patients after tenofovir/ emtricitabine in combination with atazanavir/ritonavir or efavirenz. J Acquir Immune Defic Syndr 2012; 59: 18–30.

Libório A.B. , Andrade L. , Pereira L.V. , Sanches T.R. , Shimizu M.H. , Seguro A.C. Rosiglitazone reverses tenofovir-induced nephrotoxicity. Kidney Int 2008; 74: 910–918.

Labarga P. , Barreiro P. , Martin-Carbonero L. Kidney tubular abnormalities in the absence of impaired glomerular function in HIV patients treated with tenofovir. AIDS 2009; 23: 689–696.

Buchacz K. , Young B. , Baker R.K. Renal function in patients receiving tenofovir with ritonavir/lopinavir or ritonavir/atazanavir in the HIV Outpatient Study (HOPS) cohort. J Acquir Immune Defic Syndr 2006; 43: 626–628.

Badiou S. , De Boever C.M. , Terrier N. , Baillat V. , Cristol J.P. , Reynes J. Is tenofovir involved in hypophosphatemia and decrease of tubular phosphate reabsorption in HIV-positive adults? J Infect 2006; 52: 335–338.

Ando M. , Yanagisawa N. , Ajisawa A. , Tsuchiya K. , Nitta K. Kidney tubular damage in the absence of glomerular defects in HIV-infected patients on highly active antiretroviral therapy. Nephrol Dial Transplant 2011; 26: 3224–3229.

Watanabe D. , Yoshino M. , Yagura H. Increase in serum mitochondrial creatine kinase levels induced by tenofovir administration. J Infect Chemother 2012; 18: 675–682.

Tarnopolsky M.A. , Parshad A. , Walzel B. , Schlattner U. , Wallimann T. Creatine transporter and mitochondrial creatine kinase protein content in myopathies. Muscle Nerve 2001; 24: 682–688.

Stadhouders A.M. , Jap P.H. , Winkler H.P. , Eppenberger H.M. , Wallimann T. Mitochondrial creatine kinase: a major constituent of pathological inclusions seen in mitochondrial myopathies. Proc Natl Acad Sci U S A 1994; 91: 5089–5093.

DeLuca M. , Hall N. , Rice R. , Kaplan N.O. Creatine kinase isozymes in human tumors. Biochem Biophys Res Commun 1981; 99: 189–195.

Pratt R. , Vallis L.M. , Lim C.W. , Chisnall W.N. Mitochondrial creatine kinase in cancer patients. Pathology 1987; 19: 162–165.

Kornacker M. , Schlattner U. , Wallimann T. Hodgkin disease-derived cell lines expressing ubiquitous mitochondrial creatine kinase show growth inhibition by cyclocreatine treatment independent of apoptosis. Int J Cancer 2001; 94: 513–519.

Soboll S. , Brdiczka D. , Jahnke D. Octamer-dimer transitions of mitochondrial creatine kinase in heart disease. J Mol Cell Cardiol 1999; 31: 857–866.

Wendt S. , Schlattner U. , Wallimann T. Differential effects of peroxynitrate on human mitochondrial creatine kinase isoenzymes: Inactivation and octamer destabilzation. J Biol Chem 2003; 278: 1125–1130.

Awama A.M. , Mazon H. , Vial C. , Marcillat O. Despite its high similarity with monomeric arginine kinase, muscle creatine kinase is only enzymatically active as a dimer. Arch Biochem Biophys 2007; 458: 158–166.

O'Gorman E. , Beutner G. , Dolder M. , Koretsky A.P. , Brdiczka D. , Wallimann T. The role of creatine kinase in inhibition of mitochondrial permeability transition. FEBS Lett 1997; 414: 253–257.

Schlattner U. , Forstner M. , Eder M. , Stachowiak O. , Fritz-Wolf K. , Wallimann T. Functional aspects of the X-ray structure of mitochondrial creatine kinase: a molecular physiology approach. Mol Cell Biochem 1998; 184: 125–140.