The molecular pathogenesis of HIV-1 associated nephropathy: Recent advances

Journal of Molecular Medicine

Volumn 89, Issue 5, 2011, Pages 429-436

  Papeta, Natalia ^a   Sterken, Roel ^a   Kiryluk, Krzysztof ^a   Kalyesubula, Robert ^b   Gharavi, Ali G ^a  

^a College of Physicians and Surgeons ^*  (United States)

^b MAKERERE UNIVERSITY   (Uganda)

Author keywords

eQTL; HIVAN; Network; Transcriptional regulation

Indexed keywords

APOL1 GENE; CHROMOSOME 22; GENE; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 ASSOCIATED NEPHROPATHY; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; KIDNEY DISEASE; MOLECULAR PATHOLOGY; NONHUMAN; PODOCYTE; QUANTITATIVE TRAIT LOCUS; REVIEW;

AIDS-ASSOCIATED NEPHROPATHY; ANIMALS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICE;

EID: 79955726397     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-010-0719-x     Document Type: Review

References (69)

1. UNAIDS (2010) Global report. UNAIDS report on the global AIDS epidemic. UNAIDS, Geneva
2. TK Rao EJ Filippone AD Nicastri SH Landesman E Frank CK Chen EA Friedman 1984 Associated focal and segmental glomerulosclerosis in the acquired immunodeficiency syndrome N Engl J Med 310 669 673 6700641 10.1056/ NEJM198403153101101 1:STN:280:DyaL2c7kt1SrsA%3D%3D (Pubitemid 14164641)
3. RM Selik RH Byers Jr MS Dworkin 2002 Trends in diseases reported on U.S. death certificates that mentioned HIV infection, 1987-1999 J Acquir Immune Defic Syndr 29 378 387 11917243 (Pubitemid 34288892)
4. MM Estrella RS Parekh A Abraham BC Astor LA Szczech K Anastos JA Dehovitz DJ Merenstein CL Pearce PC Tien MH Cohen SJ Gange 2010 The impact of kidney function at highly active antiretroviral therapy initiation on mortality in HIV-infected women J Acquir Immune Defic Syndr 55 217 220 20581688 10.1097/QAI.0b013e3181e674f4 1:CAS:528:DC%2BC3cXhtFyqtr%2FP
5. S Naicker J Fabian 2010 Risk factors for the development of chronic kidney disease with HIV/AIDS Clin Nephrol 74 51 56
6. U.S. Renal Data System (2010) USRDS 2010 annual data report: atlas of end-stage renal disease in the United States National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases. U.S. Renal Data System, Bethesda
7. CM Wyatt PE Klotman 2007 HIV-associated nephropathy in the era of antiretroviral therapy Am J Med 120 488 492 17524746 10.1016/j.amjmed.2007.01. 025 (Pubitemid 46764627)
8. J Fabian S Naicker 2009 HIV and kidney disease in sub-Saharan Africa Nat Rev Nephrol 5 591 598 19776781 10.1038/nrneph.2009.141
9. GM Lucas B Lau MG Atta DM Fine J Keruly RD Moore 2008 Chronic kidney disease incidence, and progression to end-stage renal disease, in HIV-infected individuals: a tale of two races J Infect Dis 197 1548 1557 18422458 10.1086/587994 (Pubitemid 351706485)
10. A Reid W Stohr AS Walker IG Williams C Kityo P Hughes A Kambugu CF Gilks P Mugyenyi P Munderi J Hakim DM Gibb 2008 Severe renal dysfunction and risk factors associated with renal impairment in HIV-infected adults in Africa initiating antiretroviral therapy Clin Infect Dis 46 1271 1281 18444867 10.1086/533468 (Pubitemid 351589914)
11. TM Han S Naicker PK Ramdial AG Assounga 2006 A cross-sectional study of HIV-seropositive patients with varying degrees of proteinuria in South Africa Kidney Int 69 2243 2250 16672914 10.1038/sj.ki.5000339 1:STN:280: DC%2BD28zkslSqtA%3D%3D (Pubitemid 43882112)
12. EJ Schwartz LA Szczech MJ Ross ME Klotman JA Winston PE Klotman 2005 Highly active antiretroviral therapy and the epidemic of HIV+ end-stage renal disease J Am Soc Nephrol 16 2412 2420 15987747 10.1681/ASN.2005040340 1:CAS:528:DC%2BD2MXovVOku7o%3D (Pubitemid 41725059)
13. V Shahinian S Rajaraman M Borucki J Grady WM Hollander TS Ahuja 2000 Prevalence of HIV-associated nephropathy in autopsies of HIV-infected patients Am J Kidney Dis 35 884 888 10793023 10.1016/S0272-6386(00)70259-9 1:STN:280:DC%2BD3c3lsFWitQ%3D%3D (Pubitemid 30238201)
14. LA Bruggeman MD Ross N Tanji A Cara S Dikman RE Gordon GC Burns VD D'Agati JA Winston ME Klotman PE Klotman 2000 Renal epithelium is a previously unrecognized site of HIV-1 infection J Am Soc Nephrol 11 2079 2087 11053484 1:STN:280:DC%2BD3crgslaktQ%3D%3D
15. D Marras LA Bruggeman F Gao N Tanji MM Mansukhani A Cara MD Ross GL Gusella G Benson VD D'Agati BH Hahn ME Klotman PE Klotman 2002 Replication and compartmentalization of HIV-1 in kidney epithelium of patients with HIV-associated nephropathy Nat Med 8 522 526 11984599 10.1038/nm0502-522 1:CAS:528:DC%2BD38Xjt1Kgurs%3D (Pubitemid 34546757)
16. JA Winston LA Bruggeman MD Ross J Jacobson L Ross VD D'Agati PE Klotman ME Klotman 2001 Nephropathy and establishment of a renal reservoir of HIV type 1 during primary infection N Engl J Med 344 1979 1984 11430327 10.1056/NEJM200106283442604 1:STN:280:DC%2BD3MzntlGktw%3D%3D (Pubitemid 32568152)
17. LA Bruggeman PJ Nelson 2009 Controversies in the pathogenesis of HIV-associated renal diseases Nat Rev Nephrol 5 574 581 19776779 10.1038/nrneph.2009.139
18. V D'Agati 2003 Pathologic classification of focal segmental glomerulosclerosis Semin Nephrol 23 117 134 12704572 10.1053/snep.2003.50012 (Pubitemid 36397094)
19. L Barisoni W Kriz P Mundel V D'Agati 1999 The dysregulated podocyte phenotype: a novel concept in the pathogenesis of collapsing idiopathic focal segmental glomerulosclerosis and HIV-associated nephropathy J Am Soc Nephrol 10 51 61 9890309 1:STN:280:DyaK1M7gsFeitw%3D%3D (Pubitemid 29034942)
20. AG Gharavi T Ahmad RD Wong R Hooshyar J Vaughn S Oller RZ Frankel LA Bruggeman VD D'Agati PE Klotman RP Lifton 2004 Mapping a locus for susceptibility to HIV-1-associated nephropathy to mouse chromosome 3 Proc Natl Acad Sci USA 101 2488 2493 14983036 10.1073/pnas.0308649100 1:CAS:528: DC%2BD2cXhvVOitrg%3D (Pubitemid 38269338)
21. M Husain VD D'Agati JC He ME Klotman PE Klotman 2005 HIV-1 Nef induces dedifferentiation of podocytes in vivo: a characteristic feature of HIVAN AIDS 19 1975 1980 16260903 10.1097/01.aids.0000191918.42110.27 1:CAS:528: DC%2BD2MXhtFKmsb%2FK (Pubitemid 41669021)
22. TC Lu JC He ZH Wang X Feng T Fukumi-Tominaga N Chen J Xu R Iyengar PE Klotman 2008 HIV-1 nef disrupts the podocyte actin cytoskeleton by interacting with diaphanous interacting protein J Biol Chem 283 8173 8182 18234668 10.1074/jbc.M708920200 1:CAS:528:DC%2BD1cXjsFChu7Y%3D
23. TC Lu JC He PE Klotman 2007 Podocytes in HIV-associated nephropathy Nephron Clin Pract 106 c67 c71 17570932 10.1159/000101800 1:CAS:528: DC%2BD2sXmsVOisro%3D (Pubitemid 46933394)
24. JC He M Husain M Sunamoto VD D'Agati ME Klotman R Iyengar PE Klotman 2004 Nef stimulates proliferation of glomerular podocytes through activation of Src-dependent Stat3 and MAPK1, 2 pathways J Clin Invest 114 643 651 15343382 1:CAS:528:DC%2BD2cXnsVemtrY%3D (Pubitemid 39578754)
25. M Sunamoto M Husain JC He EJ Schwartz PE Klotman 2003 Critical role for Nef in HIV-1-induced podocyte dedifferentiation Kidney Int 64 1695 1701 14531802 10.1046/j.1523-1755.2003.00283.x 1:CAS:528:DC%2BD3sXpsVCrtrk%3D (Pubitemid 37323698)
26. R Tandon I Levental C Huang FJ Byfield J Ziembicki JR Schelling LA Bruggeman JR Sedor PA Janmey RT Miller 2007 HIV infection changes glomerular podocyte cytoskeletal composition and results in distinct cellular mechanical properties Am J Physiol Ren Physiol 292 F701 F710 10.1152/ajprenal.00246.2006 1:CAS:528:DC%2BD2sXjt1Gmtrk%3D (Pubitemid 46220539)
27. S Martinka LA Bruggeman 2006 Persistent NF-kappaB activation in renal epithelial cells in a mouse model of HIV-associated nephropathy Am J Physiol Ren Physiol 290 F657 F665 10.1152/ajprenal.00208.2005 1:CAS:528: DC%2BD28XjtFCntro%3D (Pubitemid 43724968)
28. MJ Ross S Martinka VD D'Agati LA Bruggeman 2005 NF-kappaB regulates Fas-mediated apoptosis in HIV-associated nephropathy J Am Soc Nephrol 16 2403 2411 15975999 10.1681/ASN.2004121101 1:CAS:528:DC%2BD2MXovVOku70%3D (Pubitemid 41725058)
29. M Albaqumi TJ Soos L Barisoni PJ Nelson 2006 Collapsing glomerulopathy J Am Soc Nephrol 17 2854 2863 16914539 10.1681/ASN.2006030225 1:CAS:528: DC%2BD28XhtFWksb7F (Pubitemid 44484675)
30. A Yadav S Vallabu D Kumar G Ding DN Charney PN Chander PC Singhal 2010 HIVAN phenotype: consequence of epithelial mesenchymal transdifferentiation Am J Physiol Ren Physiol 298 F734 F744 10.1152/ajprenal.00415.2009 1:CAS:528:DC%2BC3cXjsFGnu78%3D
31. PJ Nelson VD D'Agati JM Gries JR Suarez IH Gelman 2003 Amelioration of nephropathy in mice expressing HIV-1 genes by the cyclin-dependent kinase inhibitor flavopiridol J Antibiot Ther 51 921 929 1:CAS:528:DC%2BD3sXisleksLk%3D (Pubitemid 36503425)
32. PJ Nelson IH Gelman PE Klotman 2001 Suppression of HIV-1 expression by inhibitors of cyclin-dependent kinases promotes differentiation of infected podocytes J Am Soc Nephrol 12 2827 2831 11729253 1:CAS:528:DC%2BD38Xkt1Wj (Pubitemid 33115431)
33. PJ Peters DM Moore J Mermin JT Brooks R Downing W Were A Kigozi K Buchacz PJ Weidle 2008 Antiretroviral therapy improves renal function among HIV-infected Ugandans Kidney Int 74 925 929 18614998 10.1038/ki.2008.305 1:CAS:528:DC%2BD1cXhtFWhtrbP
34. GM Lucas W Clarke J Kagaayi MG Atta DM Fine O Laeyendecker D Serwadda M Chen MJ Wawer RH Gray 2010 Decreased kidney function in a community-based cohort of HIV-Infected and HIV-negative individuals in Rakai, Uganda J Acquir Immune Defic Syndr 55 491 494 20613548 10.1097/QAI.0b013e3181e8d5a8
35. CM Wyatt S Morgello R Katz-Malamed C Wei ME Klotman PE Klotman VD D'Agati 2009 The spectrum of kidney disease in patients with AIDS in the era of antiretroviral therapy Kidney Int 75 428 434 19052538 10.1038/ki.2008.604 1:CAS:528:DC%2BD1MXhtF2ku7Y%3D
36. RC Kalayjian A Landay RB Pollard DD Taub BH Gross IR Francis A Sevin M Pu J Spritzler M Chernoff A Namkung L Fox A Martinez K Waterman SA Fiscus B Sha D Johnson S Slater F Rousseau MM Lederman 2003 Age-related immune dysfunction in health and in human immunodeficiency virus (HIV) disease: association of age and HIV infection with naive CD8+ cell depletion, reduced expression of CD28 on CD8+ cells, and reduced thymic volumes J Infect Dis 187 1924 1933 12792869 10.1086/375372 (Pubitemid 36724491)
37. AI Choi MG Shlipak PW Hunt JN Martin SG Deeks 2009 HIV-infected persons continue to lose kidney function despite successful antiretroviral therapy AIDS 23 2143 2149 19684507 10.1097/QAD.0b013e3283313c91
38. MW Smith M Dean M Carrington C Winkler GA Huttley DA Lomb JJ Goedert TR O'Brien LP Jacobson R Kaslow S Buchbinder E Vittinghoff D Vlahov K Hoots MW Hilgartner SJ O'Brien 1997 Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC), ALIVE Study Science 277 959 965 9252328 10.1126/science.277.5328.959 1:CAS:528: DyaK2sXltlGjtrg%3D (Pubitemid 27366682)
39. E Gonzalez H Kulkarni H Bolivar A Mangano R Sanchez G Catano RJ Nibbs BI Freedman MP Quinones MJ Bamshad KK Murthy BH Rovin W Bradley RA Clark SA Anderson RJ O'Connell BK Agan SS Ahuja R Bologna L Sen MJ Dolan SK Ahuja 2005 The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility Science 307 1434 1440 15637236 10.1126/science.1101160 1:CAS:528:DC%2BD2MXhslKrtLs%3D (Pubitemid 40321934)
40. BI Freedman JM Soucie SM Stone S Pegram 1999 Familial clustering of end-stage renal disease in blacks with HIV-associated nephropathy Am J Kidney Dis 34 254 258 10430971 10.1016/S0272-6386(99)70352-5 1:STN:280: DyaK1Mzmt1yruw%3D%3D (Pubitemid 29362089)
41. JC Stephens D Briscoe SJ O'Brien 1994 Mapping by admixture linkage disequilibrium in human populations: limits and guidelines Am J Hum Genet 55 809 824 7942858 1:STN:280:DyaK2M%2FivFersg%3D%3D (Pubitemid 24298979)
42. WH Kao MJ Klag LA Meoni D Reich Y Berthier-Schaad M Li J Coresh N Patterson A Tandon NR Powe NE Fink JH Sadler MR Weir HE Abboud SG Adler J Divers SK Iyengar BI Freedman PL Kimmel WC Knowler OF Kohn K Kramp DJ Leehey SB Nicholas MV Pahl JR Schelling JR Sedor D Thornley-Brown CA Winkler MW Smith RS Parekh 2008 MYH9 is associated with nondiabetic end-stage renal disease in African Americans Nat Genet 40 1185 1192 18794854 10.1038/ng.232 1:CAS:528:DC%2BD1cXhtFKht73O
43. JB Kopp MW Smith GW Nelson RC Johnson BI Freedman DW Bowden T Oleksyk LM McKenzie H Kajiyama TS Ahuja JS Berns W Briggs ME Cho RA Dart PL Kimmel SM Korbet DM Michel MH Mokrzycki JR Schelling E Simon H Trachtman D Vlahov CA Winkler 2008 MYH9 is a major-effect risk gene for focal segmental glomerulosclerosis Nat Genet 40 1175 1184 18794856 10.1038/ng.226 1:CAS:528:DC%2BD1cXhtFKht77E
44. G Genovese DJ Friedman MD Ross L Lecordier P Uzureau BI Freedman DW Bowden CD Langefeld TK Oleksyk AL Uscinski Knob AJ Bernhardy PJ Hicks GW Nelson B Vanhollebeke CA Winkler JB Kopp E Pays MR Pollak 2010 Association of trypanolytic ApoL1 variants with kidney disease in African Americans Science 329 841 845 20647424 10.1126/science.1193032 1:CAS:528:DC%2BC3cXpvV2iu7c%3D
45. G Genovese SJ Tonna AU Knob GB Appel A Katz AJ Bernhardy AW Needham R Lazarus MR Pollak 2010 A risk allele for focal segmental glomerulosclerosis in African Americans is located within a region containing APOL1 and MYH9 Kidney Int 78 698 704 20668430 10.1038/ki.2010.251
46. P Dickie J Felser M Eckhaus J Bryant J Silver N Marinos AL Notkins 1991 HIV-associated nephropathy in transgenic mice expressing HIV-1 genes Virology 185 109 119 1926769 10.1016/0042-6822(91)90759-5 1:CAS:528:DyaK3MXmslOrsLg%3D
47. JB Kopp ME Klotman SH Adler LA Bruggeman P Dickie NJ Marinos M Eckhaus JL Bryant AL Notkins PE Klotman 1992 Progressive glomerulosclerosis and enhanced renal accumulation of basement membrane components in mice transgenic for human immunodeficiency virus type 1 genes Proc Natl Acad Sci USA 89 1577 1581 1542649 10.1073/pnas.89.5.1577 1:CAS:528:DyaK38XhslaitL8%3D
48. LA Bruggeman S Dikman C Meng SE Quaggin TM Coffman PE Klotman 1997 Nephropathy in human immunodeficiency virus-1 transgenic mice is due to renal transgene expression J Clin Invest 100 84 92 9202060 10.1172/JCI119525 1:CAS:528:DyaK2sXksVOiu70%3D (Pubitemid 27311246)
49. N Paragas T Nickolas C Wyatt C Forster M Sise S Morgello B Jagla P Stella M Carnevali S Mattei A Bovino L Argentiero A Magnano L Allegri P Devarajan P Klotman V D'Agati A Gharavi J Barasch 2009 Urinary NGAL marks tubular disease in HIVAN J Am Soc Nephrol 20 1687 1692 19628667 10.1681/ASN.2009010065 1:CAS:528:DC%2BD1MXhtVers73J
50. J Zhong Y Zuo J Ma AB Fogo P Jolicoeur I Ichikawa T Matsusaka 2005 Expression of HIV-1 genes in podocytes alone can lead to the full spectrum of HIV-1-associated nephropathy Kidney Int 68 1048 1060 16105035 10.1111/j.1523-1755.2005.00497.x 1:CAS:528:DC%2BD2MXhtVCjt7zJ (Pubitemid 43246421)
51. N Papeta KT Chan S Prakash J Martino K Kiryluk D Ballard LA Bruggeman R Frankel Z Zheng PE Klotman H Zhao VD D'Agati RP Lifton AG Gharavi 2009 Susceptibility loci for murine HIV-associated nephropathy encode trans-regulators of podocyte gene expression J Clin Invest 119 1178 1188 19381020 10.1172/JCI37131 1:CAS:528:DC%2BD1MXlsFyrsbo%3D
52. KT Chan N Papeta J Martino Z Zheng RZ Frankel PE Klotman VD D'Agati RP Lifton AG Gharavi 2009 Accelerated development of collapsing glomerulopathy in mice congenic for the HIVAN1 locus Kidney Int 75 366 372 19092797 10.1038/ki.2008.625 1:CAS:528:DC%2BD1MXhtF2ku7g%3D
53. S Chua Jr Y Li SM Liu R Liu KT Chan J Martino Z Zheng K Susztak VD D'Agati AG Gharavi 2010 A susceptibility gene for kidney disease in an obese mouse model of type II diabetes maps to chromosome 8 Kidney Int 78 453 462 20520596 10.1038/ki.2010.160 1:CAS:528:DC%2BC3cXhtVWqur7E
54. RB Brem G Yvert R Clinton L Kruglyak 2002 Genetic dissection of transcriptional regulation in budding yeast Science 296 752 755 11923494 10.1126/science.1069516 1:CAS:528:DC%2BD38XjtlOnt70%3D (Pubitemid 34442007)
55. EE Schadt SA Monks TA Drake AJ Lusis N Che V Colinayo TG Ruff SB Milligan JR Lamb G Cavet PS Linsley M Mao RB Stoughton SH Friend 2003 Genetics of gene expression surveyed in maize, mouse and man Nature 422 297 302 12646919 10.1038/nature01434 1:CAS:528:DC%2BD3sXitFKmuro%3D (Pubitemid 36378355)
56. MV Rockman L Kruglyak 2006 Genetics of global gene expression Nat rev 7 862 872 10.1038/nrg1964 1:CAS:528:DC%2BD28XhtVyktLnP (Pubitemid 44607102)
57. J Behmoaras G Bhangal J Smith K McDonald B Mutch PC Lai J Domin L Game A Salama BM Foxwell CD Pusey HT Cook TJ Aitman 2008 Jund is a determinant of macrophage activation and is associated with glomerulonephritis susceptibility Nat Genet 40 553 559 18443593 10.1038/ng.137 1:CAS:528:DC%2BD1cXltFyksr4%3D (Pubitemid 351601221)
58. E Petretto R Sarwar I Grieve H Lu MK Kumaran PJ Muckett J Mangion B Schroen M Benson PP Punjabi SK Prasad DJ Pennell C Kiesewetter ES Tasheva LM Corpuz MD Webb GW Conrad TW Kurtz V Kren J Fischer N Hubner YM Pinto M Pravenec TJ Aitman SA Cook 2008 Integrated genomic approaches implicate osteoglycin (Ogn) in the regulation of left ventricular mass Nat Genet 40 546 552 18443592 10.1038/ng.134 1:CAS:528:DC%2BD1cXltFylu7c%3D (Pubitemid 351601220)
59. EE Schadt J Lamb X Yang J Zhu S Edwards D Guhathakurta SK Sieberts S Monks M Reitman C Zhang PY Lum A Leonardson R Thieringer JM Metzger L Yang J Castle H Zhu SF Kash TA Drake A Sachs AJ Lusis 2005 An integrative genomics approach to infer causal associations between gene expression and disease Nat Genet 37 710 717 15965475 10.1038/ng1589 1:CAS:528:DC%2BD2MXlslWhs7Y%3D (Pubitemid 41754887)
60. N Hubner CA Wallace H Zimdahl E Petretto H Schulz F Maciver M Mueller O Hummel J Monti V Zidek A Musilova V Kren H Causton L Game G Born S Schmidt A Muller SA Cook TW Kurtz J Whittaker M Pravenec TJ Aitman 2005 Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease Nat Genet 37 243 253 15711544 10.1038/ng1522 1:CAS:528:DC%2BD2MXhsFOqu7c%3D (Pubitemid 41716251)
61. Y Chen J Zhu PY Lum X Yang S Pinto DJ MacNeil C Zhang J Lamb S Edwards SK Sieberts A Leonardson LW Castellini S Wang MF Champy B Zhang V Emilsson S Doss A Ghazalpour S Horvath TA Drake AJ Lusis EE Schadt 2008 Variations in DNA elucidate molecular networks that cause disease Nature 452 429 435 18344982 10.1038/nature06757 1:CAS:528:DC%2BD1cXjslCnurc%3D (Pubitemid 351450844)
62. V Emilsson G Thorleifsson B Zhang AS Leonardson F Zink J Zhu S Carlson A Helgason GB Walters S Gunnarsdottir M Mouy V Steinthorsdottir GH Eiriksdottir G Bjornsdottir I Reynisdottir D Gudbjartsson A Helgadottir A Jonasdottir A Jonasdottir U Styrkarsdottir S Gretarsdottir KP Magnusson H Stefansson R Fossdal K Kristjansson HG Gislason T Stefansson BG Leifsson U Thorsteinsdottir JR Lamb JR Gulcher ML Reitman A Kong EE Schadt K Stefansson 2008 Genetics of gene expression and its effect on disease Nature 452 423 428 18344981 10.1038/nature06758 1:CAS:528:DC%2BD1cXjslCnu74%3D (Pubitemid 351450845)
63. A Ghazalpour S Doss B Zhang S Wang C Plaisier R Castellanos A Brozell EE Schadt TA Drake AJ Lusis S Horvath 2006 Integrating genetic and network analysis to characterize genes related to mouse weight PLoS Genet 2 e130 16934000 10.1371/journal.pgen.0020130 (Pubitemid 44298493)
64. TB Huber C Kwoh H Wu K Asanuma M Godel B Hartleben KJ Blumer JH Miner P Mundel AS Shaw 2006 Bigenic mouse models of focal segmental glomerulosclerosis involving pairwise interaction of CD2AP, Fyn, and synaptopodin J Clin Invest 116 1337 1345 16628251 10.1172/JCI27400 1:CAS:528:DC%2BD28XksVWns7o%3D
65. K Basso AA Margolin G Stolovitzky U Klein R Dalla-Favera A Califano 2005 Reverse engineering of regulatory networks in human B cells Nat Genet 37 382 390 15778709 10.1038/ng1532 1:CAS:528:DC%2BD2MXislCmurY%3D
66. JF Ayroles MA Carbone EA Stone KW Jordan RF Lyman MM Magwire SM Rollmann LH Duncan F Lawrence RR Anholt TF Mackay 2009 Systems genetics of complex traits in Drosophila melanogaster Nat Genet 41 299 307 19234471 10.1038/ng.332 1:CAS:528:DC%2BD1MXitFKksbs%3D
67. A Tanay R Sharan M Kupiec R Shamir 2004 Revealing modularity and organization in the yeast molecular network by integrated analysis of highly heterogeneous genomewide data Proc Natl Acad Sci USA 101 2981 2986 14973197 10.1073/pnas.0308661100 1:CAS:528:DC%2BD2cXitlWhsbY%3D (Pubitemid 38327722)
68. R Bergholdt ZM Storling K Lage EO Karlberg PI Olason M Aalund J Nerup S Brunak CT Workman F Pociot 2007 Integrative analysis for finding genes and networks involved in diabetes and other complex diseases Genome Biol 8 R253 18045462 10.1186/gb-2007-8-11-r253 (Pubitemid 351917496)
69. R Bergholdt C Brorsson K Lage JH Nielsen S Brunak F Pociot 2009 Expression profiling of human genetic and protein interaction networks in type 1 diabetes PLoS ONE 4 e6250 19609442 10.1371/journal.pone.0006250