Nicotine signaling and progression of chronic kidney disease in smokers

Biochemical Pharmacology

Volumn 86, Issue 8, 2013, Pages 1215-1223

  Jain, Gaurav ^a   Jaimes, Edgar A ^a,b  

^a University of Alabama at Birmingham   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Chronic kidney disease; Cigarette smoking; Fibrosis; Nicotine receptors; Reactive oxygen species

Indexed keywords

ALBUMIN; APOLIPOPROTEIN E; BUNGAROTOXIN RECEPTOR; CHOLINERGIC RECEPTOR; CYCLOOXYGENASE 2; FIBRONECTIN; MERTIATIDE TC 99M; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA10; NICOTINIC RECEPTOR ALPHA2; NICOTINIC RECEPTOR ALPHA4BETA2; NICOTINIC RECEPTOR ALPHA9; NICOTINIC RECEPTOR BETA2; PENTETATE TECHNETIUM TC 99M; PODOCIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ACUTE KIDNEY FAILURE; CANCER CELL CULTURE; CELL PROLIFERATION; CHRONIC KIDNEY DISEASE; COMORBIDITY; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DRUG CLEARANCE; DRUG EFFECT; ENDOTHELIUM CELL; GLOMERULUS FILTRATION RATE; HUMAN; HYPERTENSION; INJURY SEVERITY; KIDNEY; KIDNEY CELL; KIDNEY FUNCTION; KIDNEY PLASMA FLOW; KIDNEY POLYCYSTIC DISEASE; KIDNEY TRANSPLANTATION; NEPHRECTOMY; NEPHRITIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; SMOKING; SUBTOTAL NEPHRECTOMY; URINARY EXCRETION; VASCULAR SMOOTH MUSCLE;

EID: 84885632971     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.07.014     Document Type: Review

References (121)

1. Fagerstrom K. The epidemiology of smoking: health consequences and benefits of cessation. Drugs 2002;62(Suppl 2):1-9. (Pubitemid 34809710)
2. Boyle P. Cancer, cigarette smoking and premature death in Europe: a review including the Recommendations of European Cancer Experts Consensus Meeting, Helsinki, October 1996. Lung Cancer 1997;17:1-60. (Pubitemid 27261491)
3. McBride PE. The health consequences of smoking. Cardiovascular diseases. Med Clin North Am 1992;76:333-53.
4. Steenland K, Thun M, Lally C, Heath Jr. C. Environmental tobacco smoke and coronary heart disease in the American Cancer Society CPS-II cohort. Circulation 1996;94:622-8. (Pubitemid 26289214)
5. Hillege HL, Janssen WM, Bak AA, Diercks GF, Grobbee DE, Crijns HJ, et al. Microalbuminuria is common, also in a nondiabetic, nonhypertensive population, and an independent indicator of cardiovascular risk factors and cardiovascular morbidity. J Intern Med 2001;249:519-26. (Pubitemid 32823860)
6. Pinto-Sietsma SJ, Mulder J, Janssen WM, Hillege HL, de Zeeuw D, de Jong PE. Smoking is related to albuminuria and abnormal renal function in nondiabetic persons. Ann Intern Med 2000;133:585-91.
7. Halimi JM, Giraudeau B, Vol S, Caces E, Nivet H, Lebranchu Y, et al. Effects of current smoking and smoking discontinuation on renal function and proteinuria in the general population. Kidney Int 2000;58:1285-92.
8. Ishizaka N, Ishizaka Y, Toda E, Shimomura H, Koike K, Seki G, et al. Association between cigarette smoking and chronic kidney disease in Japanese men. Hypertens Res 2008;31:485-92. (Pubitemid 351597502)
9. Dyck RF, Hayward MN, Harris SB. Prevalence, determinants and co-morbidities of chronic kidney disease among First Nations adults with diabetes: results from the CIRCLE study. BMC Nephrol 2012;13:57.
10. Tozawa M, Iseki K, Iseki C, Oshiro S, Ikemiya Y, Takishita S. Influence of smoking and obesity on the development of proteinuria. Kidney Int 2002;62:956-62. (Pubitemid 35316725)
11. Tohidi M, Hasheminia M, Mohebi R, Khalili D, Hosseinpanah F, Yazdani B, et al. Incidence of chronic kidney disease and its risk factors, results of over 10 year follow up in an Iranian cohort. PLoS One 2012;7:e45304.
12. Yacoub R, Habib H, Lahdo A, Al Ali R, Varjabedian L, Atalla G, et al. Association between smoking and chronic kidney disease: a case control study. BMC Public Health 2010;10:731.
13. Lash JP, Go AS, Appel LJ, He J, Ojo A, Rahman M, et al. Chronic Renal Insufficiency Cohort (CRIC) Study: baseline characteristics and associations with kidney function. Clin J Am Soc Nephrol 2009;4:1302-11.
14. Garcia-Esquinas E, Loeffler LF, Weaver VM, Fadrowski JJ, Navas-Acien A. Kidney function and tobacco smoke exposure in US adolescents. Pediatrics 2013;131(5):e1415-23. http://dx.doi.org/10.1542/peds.2012-3201. Epub 2013 Apr 8.
15. Kheradmand A, Shahbazian H. The role of pretransplant smoking on allograft survival in kidney recipients. Urol J 2005;2:36-9.
16. Sung RS, Althoen M, Howell TA, Ojo AO, Merion RM. Excess risk of renal allograft loss associated with cigarette smoking. Transplantation 2001;71:1752-7. (Pubitemid 32622486)
17. Cardinal H, Hebert MJ, Rahme E, Houde I, Baran D, Masse M, et al. Modifiable factors predicting patient survival in elderly kidney transplant recipients. Kidney Int 2005;68:345-51. (Pubitemid 43181394)
18. Collins AJ, Foley RN, Chavers B, Gilbertson D, Herzog C, Johansen K, et al. United States Renal Data System 2011 Annual Data Report: atlas of chronic kidney disease & end-stage renal disease in the United States.AmJ kidney Dis 2012;59. A7, e1-420.
19. Huang MF, Lin WL, Ma YC. A study of reactive oxygen species in mainstream of cigarette. Indoor Air 2005;15:135-40.
20. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW. Mammalian nicotinic acetylcholine receptors: fromstructure to function. Physiol Rev 2009;89:73-120.
21. Rozental R, Aracava Y, Scoble GT, Swanson KL, Wonnacott S, Albuquerque EX. Agonist recognition site of the peripheral acetylcholine receptor ion channel complex differentiates the enantiomers of nicotine. J Pharmacol Exp Ther 1989;251:395-404. (Pubitemid 20005576)
22. Flores CM, DeCamp RM, Kilo S, Rogers SW, Hargreaves KM. Neuronal nicotinic receptor expression in sensory neurons of the rat trigeminal ganglion: demonstration of alpha3beta4, a novel subtype in the mammalian nervous system. J Neurosci 1996;16:7892-901. (Pubitemid 26405052)
23. McCallum SE, Collins AC, Paylor R, Marks MJ. Deletion of the beta 2 nicotinic acetylcholine receptor subunit alters development of tolerance to nicotine and eliminates receptor upregulation. Psychopharmacology 2006;184:314-27. (Pubitemid 43255848)
24. Wu J, Lukas RJ. Naturally-expressed nicotinic acetylcholine receptor subtypes. Biochem Pharmacol 2011;82:800-7.
25. Castro NG, Albuquerque EX. Alpha-bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability. Biophys J 1995;68:516-24.
26. Marks MJ, Stitzel JA, Romm E, Wehner JM, Collins AC. Nicotinic binding sites in rat and mouse brain: comparison of acetylcholine, nicotine, and alphabungarotoxin. Mol Pharmacol 1986;30:427-36. (Pubitemid 17202420)
27. Gopalakrishnan M, Buisson B, Touma E, Giordano T, Campbell JE, Hu IC, et al. Stable expression and pharmacological properties of the human alpha 7 nicotinic acetylcholine receptor. Eur J Pharmacol 1995;290:237-46.
28. Boksa P, Quik M, Mitchell JB, Collier B, O'Neil W, Quirion R. Pharmacological activity of N-methyl-carbamylcholine, a novel acetylcholine receptor agonist with selectivity for nicotinic receptors. Eur J Pharmacol 1989;173:93-108. (Pubitemid 20006781)
29. Grando SA, Horton RM, Pereira EF, Diethelm-Okita BM, George PM, Albuquerque EX, et al. A nicotinic acetylcholine receptor regulating cell adhesion and motility is expressed in human keratinocytes. J Invest Dermatol 1995;105:774-81. (Pubitemid 26006352)
30. Maus AD, Pereira EF, Karachunski PI, Horton RM, Navaneetham D, Macklin K, et al. Human and rodent bronchial epithelial cells express functional nicotinic acetylcholine receptors. Mol Pharmacol 1998;54:779-88. (Pubitemid 28523170)
31. Macklin KD, Maus AD, Pereira EF, Albuquerque EX, Conti-Fine BM. Human vascular endothelial cells express functional nicotinic acetylcholine receptors. J Pharmacol Exp Ther 1998;287:435-9. (Pubitemid 29140230)
32. Wessler I, Kirkpatrick CJ, Racke K. The cholinergic 'pitfall': acetylcholine, a universal cell molecule in biological systems, including humans. Clin Exp Pharmacol Physiol 1999;26:198-205. (Pubitemid 29128015)
33. Heeschen C, Weis M, Aicher A, Dimmeler S, Cooke JP. A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors. J Clin Invest 2002;110:527-36. (Pubitemid 34919707)
34. Jaimes E, Tian RX, Raij L. Nicotine: The link between cigarette smoking and the progression of renal injury. Am J Physiol Heart Circ Physiol 2007;292:H76-82. (Pubitemid 46115921)
35. Heeschen C, Jang JJ, Weis M, Pathak A, Kaji S, Hu RS, et al. Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med 2001;7:833-9. (Pubitemid 32691639)
36. Cucina A, Corvino V, Sapienza P, Borrelli V, Lucarelli M, Scarpa S, et al. Nicotine regulates basic fibroblastic growth factor and transforming growth factor beta1 production in endothelial cells. Biochem Biophys Res Commun 1999;257:306-12. (Pubitemid 29301440)
37. Cucina A, Sapienza P, Corvino V, Borrelli V, Randone B, Santoro-D'Angelo L, et al. Nicotine induces platelet-derived growth factor release and cytoskeletal alteration in aortic smooth muscle cells. Surgery 2000;127:72-8. (Pubitemid 30053692)
38. Cucina A, Sapienza P, Corvino V, Borrelli V, Mariani V, Randone B, et al. Nicotine-induced smooth muscle cell proliferation is mediated through bFGF and TGF-beta 1. Surgery 2000;127:316-22. (Pubitemid 30140630)
39. Carty CS, Soloway PD, Kayastha S, Bauer J, Marsan B, Ricotta JJ, et al. Nicotine and cotinine stimulate secretion of basic fibroblast growth factor and affect expression of matrix metalloproteinases in cultured human smooth muscle cells. J Vasc Surg 1996;24:927-34. discussion 34-5.
40. Roman J, Ritzenthaler JD, Gil-Acosta A, Rivera HN, Roser-Page S. Nicotine and fibronectin expression in lung fibroblasts: implications for tobacco-related lung tissue remodeling. FASEB J 2004;18:1436-8.
41. Arredondo J, Hall LL, Ndoye A, Nguyen VT, Chernyavsky AI, Bercovich D, et al. Central role of fibroblast alpha3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine. Lab Invest 2003;83:207-25. (Pubitemid 36255366)
42. Dasgupta P, Rastogi S, Pillai S, Ordonez-Ercan D, Morris M, Haura E, et al. Nicotine induces cell proliferation by beta-arrestin-mediated activation of Src and Rb-Raf-1 pathways. J Clin Invest 2006;116:2208-17. (Pubitemid 44162330)
43. Zhang S, Day I, Ye S. Nicotine induced changes in gene expression by human coronary artery endothelial cells. Atherosclerosis 2001;154:277-83. (Pubitemid 32146599)
44. Jaimes EA, Tian RX, Raij L. Nicotine: the link between cigarette smoking and the progression of renal injury. Am J Physiol Heart Circ Physiol 2007;292:H76-82. (Pubitemid 46115921)
45. Schneider NG, Olmstead RE, Franzon MA, Lunell E. The nicotine inhaler: clinical pharmacokinetics and comparison with other nicotine treatments. Clin Pharmacokinet 2001;40:661-84. (Pubitemid 32954989)
46. Jaimes EA, Galceran JM, Raij L. Angiotensin II induces superoxide anion production by mesangial cells. Kidney Int 1998;54:775-84. (Pubitemid 28397395)
47. Sharma P, Evans AT, Parker PJ, Evans FJ. NADPH-oxidase activation by protein kinase C-isotypes. Biochem Biophys Res Commun 1991;177(3):1033-40.
48. Sano M, Fukuda K, Sato T, Kawaguchi H, Suematsu M, Matsuda S, et al. ERK and p38 MAPK, but not NF-kappaB, are critically involved in reactive oxygen species-mediated induction of IL-6 by angiotensin II in cardiac fibroblasts. Circ Res 2001;89:661-9. (Pubitemid 34627065)
49. Tian W, Zhang Z, Cohen DM. MAPK signaling and the kidney. Am J Physiol Renal Physiol 2000;279:F593-604.
50. Choudhury GG, Karamitsos C, Hernandez J, Gentilini A, Bardgette J, Abboud HE. PI-3-kinase and MAPK regulate mesangial cell proliferation and migration in response to PDGF. Am J Physiol 1997;273:F931-8.
51. Hartsough MT, Mulder KM. Transforming growth factor beta activation of p44mapk in proliferating cultures of epithelial cells. J Biol Chem 1995;270:7117-24.
52. Hua P, Feng W, Ji S, Raij L, Jaimes EA. Nicotine worsens the severity of nephropathy in diabetic mice: implications for the progression of kidney disease in smokers. Am J Physiol Renal Physiol 2010;299:F732-9.
53. Jaimes EA, Tian RX, Joshi MS, Raij L. Nicotine augments glomerular injury in a rat model of acute nephritis. Am J Nephrol 2009;29:319-26.
54. Jaimes EA, Tian RX, Pearse D, Raij L. Up-regulation of glomerular COX-2 by angiotensin II: Role of reactive oxygen species. Kidney Int 2005;68:2143-53. (Pubitemid 43117788)
55. Wei Y, Sowers JR, Clark SE, Li W, Ferrario CM, Stump CS. Angiotensin IIinduced skeletal muscle insulin resistance mediated by NF-kappaB activation via NADPH oxidase. Am J Physiol Endocrinol Metab 2008;294:E345-51. (Pubitemid 351231460)
56. Arany I, Grifoni S, Clark JS, Csongradi E, Maric C, Juncos LA. Chronic nicotine exposure exacerbates acute renal ischemic injury. Am J Physiol Renal Physiol 2011;301:F125-33.
57. Arany I, Reed DK, Grifoni SC, Chandrashekar K, Booz GW, Juncos LA. A novel USTAT3-dependentmechanismmediates the deleterious effects of chronic nicotine exposure on renal injury. Am J Physiol Renal Physiol 2012;302:F722-9.
58. Hukkanen J, Jacob 3rd P, Benzowitz NL. Metabolism and disposition kinetics of nicotine. Pharmacol Rev 2005;57:79-115. (Pubitemid 40283970)
59. Yeboah MM, Xue X, Duan B, Ochani M, Tracey KJ, Susin M, et al. Cholinergic agonists attenuate renal ischemia-reperfusion injury in rats. Kidney Int 2008;74:62-9. (Pubitemid 351841900)
60. Yeboah MM, Xue X, Javdan M, Susin M, Metz CN. Nicotinic acetylcholine receptor expression and regulation in the rat kidney after ischemia-reperfusion injury. Am J Physiol Renal Physiol 2008;295:F654-61.
61. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003;421:384-8. (Pubitemid 36157937)
62. Sadlier DM, Ouyang X, McMahon B, Mu W, Ohashi R, Rodgers K, et al. Microarray and bioinformatic detection of novel and established genes expressed in experimental anti-Thy1 nephritis. Kidney Int 2005;68:2542-61. (Pubitemid 43251000)
63. Hayashi K, Osada S, Shofuda K, Horikoshi S, Shirato I, Tomino Y. Enhanced expression of membrane type-1 matrix metalloproteinase in mesangial proliferative glomerulonephritis. J Am Soc Nephrol 1998;9:2262-71. (Pubitemid 28543804)
64. Hirose S, Yamamoto T, Feng L, Yaoita E, Kawasaki K, Goto S, et al. Expression and localization of cyclooxygenase isoforms and cytosolic phospholipase A2 in anti-Thy-1 glomerulonephritis. J Am Soc Nephrol 1998;9:408-16. (Pubitemid 28122865)
65. Jerde TJ, Mellon WS, Bjorling DE, Nakada SY. Evaluation of urothelial stretchinduced cyclooxygenase-2 expression in novel human cell culture and porcine in vivo ureteral obstruction models. J Pharmacol Exp Ther 2006;317:965-72. (Pubitemid 43764098)
66. Norregaard R, Jensen BL, Topcu SO, Nielsen SS, Walter S, Djurhuus JC, et al. Cyclooxygenase type 2 is increased in obstructed rat and human ureter and contributes to pelvic pressure increase after obstruction. Kidney Int 2006;70:872-81. (Pubitemid 44285964)
67. Bagi Z, Erdei N, Papp Z, Edes I, Koller A. Up-regulation of vascular cyclooxygenase-2 in diabetes mellitus. Pharmacol Rep 2006;58(Suppl):52-6.
68. Kellogg AP, Cheng HT, Pop-Busui R. Cyclooxygenase-2 pathway as a potential therapeutic target in diabetic peripheral neuropathy. Curr Drug Targets 2008;9:68-76. (Pubitemid 351201681)
69. Solari V, Piotrowska AP, Cascio S, Unemoto K, Chertin B, Puri P. Cyclooxygenase-2 up-regulation in reflux nephropathy. J Urol 2003;170:1624-7. (Pubitemid 37102429)
70. Tokuyama H, Hayashi K, Matsuda H, Kubota E, Honda M, Okubo K, et al. Differential regulation of elevated renal angiotensin II in chronic renal ischemia. Hypertension 2002;40:34-40. (Pubitemid 34755976)
71. Wang JL, Cheng HF, Shappell S, Harris RC. A selective cyclooxygenase-2 inhibitor decreases proteinuria and retards progressive renal injury in rats. Kidney Int 2000;57:2334-42. (Pubitemid 30340732)
72. Agarwal PK, van den Born J, van Goor H, Navis G, Gans RO, Bakker SJ. Renoprotective effects of long-term oral nicotine in a rat model of spontaneous proteinuria. Am J Physiol Renal Physiol 2012;302:F895-904.
73. Schulz A, Schutten-Faber S, van Es N, Unland J, Schulte L, Kossmehl P, et al. Induction of albuminuria and kidney damage in SHR by transfer of chromosome 8 from Munich Wistar Fromter rats. Physiol Genomics 2012;44:110-6.
74. Macconi D, Bonomelli M, Benigni A, Plati T, Sangalli F, Longaretti L, et al. Pathophysiologic implications of reduced podocyte number in a rat model of progressive glomerular injury. Am J Pathol 2006;168:42-54. (Pubitemid 43062558)
75. Sharma K,McCue P, Dunn SR. Diabetic kidney disease in the db/db mouse.Am J Physiol Renal Physiol 2003;284:F1138-44. (Pubitemid 36578440)
76. Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, et al. Evidence that the diabetes gene encodes the leptin receptor: identification of amutation in the leptin receptor gene in db/db mice. Cell 1996;84:491-5. (Pubitemid 26060722)
77. Lee GH, Proenca R, Montez JM, Carroll KM, Darvishzadeh JG, Lee JI, et al. Abnormal splicing of the leptin receptor in diabetic mice. Nature 1996;379:632-5. (Pubitemid 26053452)
78. Obert DM, Hua P, Pilkerton ME, Feng W, Jaimes EA. Environmental tobacco smoke furthers progression of diabetic nephropathy. Am J Med Sci 2011;341:126-30.
79. Asaba K, Tojo A, Onozato ML, Goto A, Quinn MT, Fujita T, et al. Effects of NADPH oxidase inhibitor in diabetic nephropathy. Kidney Int 2005;67:1890-8. (Pubitemid 40577724)
80. Gorin Y, Block K, Hernandez J, Bhandari B, Wagner B, Barnes JL, et al. Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem 2005;280:39616-26. (Pubitemid 41713921)
81. Razani-Boroujerdi S, Boyd RT, Davila-Garcia MI, Nandi JS, Mishra NC, Singh SP, et al. T cells express alpha7-nicotinic acetylcholine receptor subunits that require a functional TCR and leukocyte-specific protein tyrosine kinase for nicotine-induced Ca2+ response. J Immunol 2007;179:2889-98.
82. Charpantier E, Wiesner A, Huh KH, Ogier R, Hoda JC, Allaman G, et al. Alpha7 neuronal nicotinic acetylcholine receptors are negatively regulated by tyrosine phosphorylation and Src-family kinases. J Neurosci 2005;25:9836-49. (Pubitemid 41528021)
83. Shimamura T, Morrison AB. A progressive glomerulosclerosis occurring in partial five-sixths nephrectomized rats. Am J Pathol 1975;79:95-106.
84. Tain YL, Freshour G, Dikalova A, Griendling K, Vitamin Baylis C. E reduces glomerulosclerosis, restores renal neuronal NOS, and suppresses oxidative stress in the 5/6 nephrectomized rat. Am J Physiol Renal Physiol 2007;292:F1404-10. (Pubitemid 46701867)
85. Heinrich J, Holscher B, Seiwert M, Carty CL, Merkel G, Schulz C. Nicotine and cotinine in adults' urine: The German Environmental Survey 1998. J Expo Anal Environ Epidemiol 2005;15:74-80. (Pubitemid 40170986)
86. Ziyadeh FN, Hoffman BB, Han DC, Iglesias-De La Cruz MC, Hong SW, Isono M. Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc Natl Acad Sci U S A 2000;97:8015-20. (Pubitemid 30460765)
87. Eddy AA. Molecular basis of renal fibrosis. Pediatr Nephrol 2000;15:290-301.
88. Metcalfe W. How does early chronic kidney disease progress? A background paper prepared for the UK Consensus Conference on early chronic kidney disease. Nephrol Dial Transplant 2007;22(Suppl 9):ix26-30.
89. Gambaro G, Verlato F, Budakovic A, Casara D, Saladini G, Del Prete D, et al. Renal impairment in chronic cigarette smokers. J Am Soc Nephrol 1998;9:562-7. (Pubitemid 28186043)
90. Hallan S, de Mutsert R, Carlsen S, Dekker FW, Aasarod K, Holmen J. Obesity, smoking, and physical inactivity as risk factors for CKD: are men more vulnerable? Am J Kidney Dis 2006;47:396-405. (Pubitemid 43255172)
91. Briganti EM, Branley P, Chadban SJ, Shaw JE, McNeil JJ, Welborn TA, et al. Smoking is associated with renal impairment and proteinuria in the normal population: the AusDiab kidney study. Australian Diabetes, Obesity and Lifestyle Study. Am J Kidney Dis 2002;40:704-12.
92. Orth SR, Stockmann A, Conradt C, Ritz E, Ferro M, Kreusser W, et al. Smoking as a risk factor for end-stage renal failure in men with primary renal disease. Kidney Int 1998;54:926-31. (Pubitemid 28397411)
93. Stengel B, Couchoud C, Cenee S, Hemon D. Age, blood pressure and smoking effects on chronic renal failure in primary glomerular nephropathies. Kidney Int 2000;57:2519-26. (Pubitemid 30340750)
94. Gerstein HC, Mann JF, Pogue J, Dinneen SF, Halle JP, Hoogwerf B, et al. Prevalence and determinants of microalbuminuria in high-risk diabetic and nondiabetic patients in the Heart Outcomes Prevention Evaluation Study. The HOPE Study Investigators. Diabetes Care 2000;23:B35-9. (Pubitemid 30185776)
95. Andronico G, Rome M, Lo Cicero A, Parsi R, Seddio G, Ferraro-Mortellaro R. Renal plasma flow, filtration fraction and microalbuminuria in hypertensive patients: effects of chronic smoking. Nephrology (Carlton) 2005;10:483-6. (Pubitemid 41727273)
96. Mimran A, Ribstein J, DuCailar G, Halimi JM. Albuminuria in normals and essential hypertension. J Diabetes Complications 1994;8:150-6. (Pubitemid 24373882)
97. Horner D, Fliser D, Klimm HP, Ritz E. Albuminuria in normotensive and hypertensive individuals attending offices of general practitioners. J Hypertens 1996;14:655-60. (Pubitemid 26161121)
98. Regalado M, Yang S, Wesson DE. Cigarette smoking is associated with augmented progression of renal insufficiency in severe essential hypertension. Am J Kidney Dis 2000;35:687-94. (Pubitemid 30185515)
99. Chuahirun T, Khanna A, Kimball K, Wesson DE. Cigarette smoking and increased urine albumin excretion are interrelated predictors of nephropathy progression in type 2 diabetes. Am J Kidney Dis 2003;41:13-21. (Pubitemid 36043347)
100. Chuahirun T, Wesson DE. Cigarette smoking predicts faster progression of type 2 established diabetic nephropathy despite ACE inhibition. Am J Kidney Dis 2002;39:376-82. (Pubitemid 34174262)
101. Muhlhauser I, Sawicki P, Berger M. Cigarette-smoking as a risk factor for macroproteinuria and proliferative retinopathy in type 1 (insulin-dependent) diabetes. Diabetologia 1986;29:500-2. (Pubitemid 16050198)
102. Chase HP, Garg SK, Marshall G, Berg CL, Harris S, Jackson WE, et al. Cigarette smoking increases the risk of albuminuria among subjects with type I diabetes. JAMA 1991;265:614-7.
103. Chaturvedi N, Stephenson JM, Fuller JH. The relationship between smoking and microvascular complications in the EURODIAB IDDM Complications Study. Diabetes Care 1995;18:785-92.
104. Savage S, Nagel NJ, Estacio RO, Lukken N, Schrier RW. Clinical factors associated with urinary albumin excretion in type II diabetes. Am J Kidney Dis 1995;25:836-44.
105. Vergouwe Y, Soedamah-Muthu SS, Zgibor J, Chaturvedi N, Forsblom C, Snell-Bergeon JK, et al. Progression to microalbuminuria in type 1 diabetes: development and validation of a prediction rule. Diabetologia 2010;53:254-62.
106. Phisitkul K, Hegazy K, Chuahirun T, Hudson C, Simoni J, Rajab H, et al. Continued smoking exacerbates but cessation ameliorates progression of early type 2 diabetic nephropathy. Am J Med Sci 2008;335:284-91. (Pubitemid 351548647)
107. Sawicki PT, Didjurgeit U, Muhlhauser I, Bender R, Heinemann L, Berger M. Smoking is associated with progression of diabetic nephropathy. Diabetes Care 1994;17:126-31. (Pubitemid 24035307)
108. Biesenbach G, Grafinger P, Janko O, Zazgornik J. Influence of cigarettesmoking on the progression of clinical diabetic nephropathy in type 2 diabetic patients. Clin Nephrol 1997;48:146-50. (Pubitemid 27429599)
109. Chapman AB, Johnson AM, Gabow PA, Schrier RW. Overt proteinuria and microalbuminuria in autosomal dominant polycystic kidney disease. J Am Soc Nephrol 1994;5:1349-54. (Pubitemid 24977120)
110. Ozkok A, Akpinar TS, Tufan F, Kanitez NA, Uysal M, Guzel M, et al. Clinical characteristics and predictors of progression of chronic kidney disease in autosomal dominant polycystic kidney disease: a single center experience. Clin Exp Nephrol 2012;17(3):345-51. http://dx.doi.org/10.1007/s10157-012-0706-3. Epub 2012 Oct 2.
111. Ward MM, Studenski S. Clinical prognostic factors in lupus nephritis. The importance of hypertension and smoking. Arch InternMed 1992;152:2082-8.
112. Orth SR. Smoking and the kidney. J Am Soc Nephrol 2002;13:1663-72.
113. Lin SJ, Koford JK, Baird BC, Hurdle JF, Krikov S, Habib AN, et al. Effect of donors' intravenous drug use, cigarette smoking, and alcohol dependence on kidney transplant outcome. Transplantation 2005;80:482-6. (Pubitemid 41209416)
114. Agarwal R. Smoking, oxidative stress and inflammation: impact on resting energy expenditure in diabetic nephropathy. BMC Nephrol 2005;6:13.
115. Orth SR. Effects of smoking on systemic and intrarenal hemodynamics: influence on renal function. J Am Soc Nephrol 2004;15(Suppl 1):S58-63. (Pubitemid 38018458)
116. Halimi JM, Giraudeau B, Vol S, Caces E, Nivet H, Tichet J. The risk of hypertension in men: direct and indirect effects of chronic smoking. J Hypertens 2002;20:187-93. (Pubitemid 34913783)
117. Mann SJ, James GD, Wang RS, Pickering TG. Elevation of ambulatory systolic blood pressure in hypertensive smokers. A case-control study. JAMA 1991;265:2226-8.
118. Grassi G, Seravalle G, Calhoun DA, Bolla GB, Giannattasio C, Marabini M, et al. Mechanisms responsible for sympathetic activation by cigarette smoking in humans. Circulation 1994;90:248-53. (Pubitemid 24203687)
119. Orth SR. Smoking-A renal risk factor. Nephron 2000;86:12-26.
120. Halimi JM, Philippon C, Mimran A. Contrasting renal effects of nicotine in smokers and non-smokers. Nephrol Dial Transplant 1998;13:940-4. (Pubitemid 28161768)
121. Benck U, Clorius JH, Zuna I, Ritz E. Renal hemodynamic changes during smoking: effects of adrenoreceptor blockade. Eur J Clin Invest 1999;29:1010-8.