Proteomic Analysis of Urine Exosomes Reveals Renal Tubule Response to Leptospiral Colonization in Experimentally Infected Rats

PLoS Neglected Tropical Diseases

Volumn 9, Issue 3, 2015, Pages

  RamachandraRao, Satish P ^a,b   Matthias, Michael A ^b   Mondrogon, Chanthel Kokoy ^a   Aghania, Eamon ^a   Park, Cathleen ^a   Kong, Casey ^a   Ishaya, Michelle ^a   Madrigal, Assael ^a   Horng, Jennifer ^a   Khoshaba, Roni ^a   Bounkhoun, Anousone ^a   Basilico, Fabrizio ^c   De Palma, Antonella ^c   Agresta, Anna Maria ^c   Awdishu, Linda ^a   Naviaux, Robert K ^b   Vinetz, Joseph M ^b   Mauri, Pierluigi ^c,d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CNR   (Italy)

^d SCUOLA SUPERIORE SANT ANNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSOMAL AMINOPEPTIDASE; TAMM HORSFALL GLYCOPROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; CONTROLLED STUDY; EXOSOME; FEMALE; LEPTOSPIROSIS; MALE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN CONTENT; PROTEOMICS; RAT; SCORING SYSTEM; TANDEM MASS SPECTROMETRY; URINALYSIS; WESTERN BLOTTING; ANIMAL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KIDNEY TUBULE; LIQUID CHROMATOGRAPHY; METABOLISM; MICROBIOLOGY; MULTIVARIATE ANALYSIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES; PROTEINURIA; SEX DIFFERENCE; STATISTICAL MODEL;

ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXOSOMES; FEMALE; HOST-PATHOGEN INTERACTIONS; KIDNEY TUBULES; LEPTOSPIROSIS; MALE; MODELS, STATISTICAL; MULTIVARIATE ANALYSIS; PROTEINURIA; PROTEOMICS; RATS; SEX FACTORS; TANDEM MASS SPECTROMETRY;

EID: 84928809235     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003640     Document Type: Article

References (88)

1. Bharti AR, Nally JE, Ricaldi JN, Matthias MA, Diaz MM, et al. (2003) Leptospirosis: a zoonotic disease of global importance. Lancet Infect Dis 3: 757–771. 14652202
2. Pappas G, Papadimitriou P, Siozopoulou V, Christou L, Akritidis N, (2008) The globalization of leptospirosis: worldwide incidence trends. Int J Infect Dis 12: 351–357. 18055245
3. Adler B, de la Pena Moctezuma A, (2010) Leptospira and leptospirosis. Vet Microbiol 140: 287–296. doi: 10.1016/j.vetmic.2009.03.012 19345023
4. Ko AI, Goarant C, Picardeau M, (2009) Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen. Nat Rev Microbiol 7: 736–747. doi: 10.1038/nrmicro2208 19756012
5. Monahan AM, Callanan JJ, Nally JE, (2008) Proteomic analysis of Leptospira interrogans shed in urine of chronically infected hosts. Infect Immun 76: 4952–4958. doi: 10.1128/IAI.00511-08 18765721
6. Nally JE, Monahan AM, Miller IS, Bonilla-Santiago R, Souda P, et al. (2011) Comparative proteomic analysis of differentially expressed proteins in the urine of reservoir hosts of leptospirosis. PLoS One 6: e26046. doi: 10.1371/journal.pone.0026046 22043303
7. Ko AI, Goarant C, Picardeau M, (2009) Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen. Nature reviews Microbiology 7: 736–747. doi: 10.1038/nrmicro2208 19756012
8. Chassin C, Picardeau M, Goujon JM, Bourhy P, Quellard N, et al. (2009) TLR4- and TLR2-mediated B cell responses control the clearance of the bacterial pathogen, Leptospira interrogans. Journal of immunology 183: 2669–2677. doi: 10.4049/jimmunol.0900506 19635914
9. Murray GL, Morel V, Cerqueira GM, Croda J, Srikram A, et al. (2009) Genome-wide transposon mutagenesis in pathogenic Leptospira species. Infect Immun 77: 810–816. doi: 10.1128/IAI.01293-08 19047402
10. Ganoza CA, Matthias MA, Saito M, Cespedes M, Gotuzzo E, et al. (2010) Asymptomatic renal colonization of humans in the peruvian Amazon by Leptospira. PLoS Negl Trop Dis 4: e612. doi: 10.1371/journal.pntd.0000612 20186328
11. Looze C, Yui D, Leung L, Ingham M, Kaler M, et al. (2009) Proteomic profiling of human plasma exosomes identifies PPARgamma as an exosome-associated protein. Biochem Biophys Res Commun 378: 433–438. doi: 10.1016/j.bbrc.2008.11.050 19028452
12. Conde-Vancells J, Rodriguez-Suarez E, Embade N, Gil D, Matthiesen R, et al. (2008) Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J Proteome Res 7: 5157–5166. 19367702
13. Lancaster GI, Febbraio MA, (2005) Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem 280: 23349–23355. 15826944
14. Lancaster GI, Febbraio MA, (2005) Mechanisms of stress-induced cellular HSP72 release: implications for exercise-induced increases in extracellular HSP72. Exerc Immunol Rev 11: 46–52. 16385843
15. Levett PN, (2001) Leptospirosis. Clin Microbiol Rev 14: 296–326. 11292640
16. Turner LH, (1967) Leptospirosis. I. Trans R Soc Trop Med Hyg 61: 842–855. 5625167
17. Shevchenko A, Wilm M, Vorm O, Mann M, (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850–858. 8779443
18. Brambilla F, Lavatelli F, Di Silvestre D, Valentini V, Palladini G, et al. (2013) Shotgun protein profile of human adipose tissue and its changes in relation to systemic amyloidoses. J Proteome Res 12: 5642–5655. doi: 10.1021/pr400583h 24083510
19. Mauri P, Deho G, (2008) A proteomic approach to the analysis of RNA degradosome composition in Escherichia coli. Methods in enzymology 447: 99–117. doi: 10.1016/S0076-6879(08)02206-4 19161840
20. Paoletti AC, Parmely TJ, Tomomori-Sato C, Sato S, Zhu D, et al. (2006) Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors. Proc Natl Acad Sci U S A 103: 18928–18933. 17138671
21. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS, (2012) MetaboAnalyst 2.0—a comprehensive server for metabolomic data analysis. Nucleic Acids Res 40: W127–133. doi: 10.1093/nar/gks374 22553367
22. Xia J, Psychogios N, Young N, Wishart DS, (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic acids research 37: W652–660. doi: 10.1093/nar/gkp356 19429898
23. Ramachandra Rao SP, Wassell R, Shaw MA, Sharma K, (2007) Profiling of human mesangial cell subproteomes reveals a role for calmodulin in glucose uptake. Am J Physiol Renal Physiol 292: F1182–1189. 17200159
24. RamachandraRao SP, Zhu Y, Ravasi T, McGowan TA, Toh I, et al. (2009) Pirfenidone is renoprotective in diabetic kidney disease. J Am Soc Nephrol 20: 1765–1775. doi: 10.1681/ASN.2008090931 19578007
25. Riemann D, Kehlen A, Langner J, (1995) Stimulation of the expression and the enzyme activity of aminopeptidase N/CD13 and dipeptidylpeptidase IV/CD26 on human renal cell carcinoma cells and renal tubular epithelial cells by T cell-derived cytokines, such as IL-4 and IL-13. Clin Exp Immunol 100: 277–283. 7743667
26. Look AT, Ashmun RA, Shapiro LH, Peiper SC, (1989) Human myeloid plasma membrane glycoprotein CD13 (gp150) is identical to aminopeptidase N. J Clin Invest 83: 1299–1307. 2564851
27. Natarajaseenivasan K, Shanmughapriya S, Velineni S, Artiushin SC, Timoney JF, (2011) Cloning, expression, and homology modeling of GroEL protein from Leptospira interrogans serovar autumnalis strain N2. Genomics Proteomics Bioinformatics 9: 151–157. doi: 10.1016/S1672-0229(11)60018-1 22196358
28. Vedhagiri K, Natarajaseenivasan K, Chellapandi P, Prabhakaran SG, Selvin J, et al. (2009) Evolutionary implication of outer membrane lipoprotein-encoding genes ompL1, UpL32 and lipL41 of pathogenic Leptospira species. Genomics Proteomics Bioinformatics 7: 96–106. doi: 10.1016/S1672-0229(08)60038-8 19944382
29. Fanton d'Andon M, Quellard N, Fernandez B, Ratet G, Lacroix-Lamande S, et al. (2014) Leptospira Interrogans induces fibrosis in the mouse kidney through Inos-dependent, TLR- and NLR-independent signaling pathways. PLoS Negl Trop Dis 8: e2664. doi: 10.1371/journal.pntd.0002664 24498450
30. Martinez SA, Hostutler RA, (2014) Distal renal tubular acidosis associated with concurrent leptospirosis in a dog. J Am Anim Hosp Assoc 50: 203–208. doi: 10.5326/JAAHA-MS-5993 24659721
31. Cesar KR, Romero EC, de Braganca AC, Blanco RM, Abreu PA, et al. (2012) Renal involvement in leptospirosis: the effect of glycolipoprotein on renal water absorption. PLoS One 7: e37625. doi: 10.1371/journal.pone.0037625 22701573
32. Araujo ER, Seguro AC, Spichler A, Magaldi AJ, Volpini RA, et al. (2010) Acute kidney injury in human leptospirosis: an immunohistochemical study with pathophysiological correlation. Virchows Arch 456: 367–375. doi: 10.1007/s00428-010-0894-8 20217429
33. Barrett-Connor E, Child CM, Carter MJ, (1970) Renal failure in leptospirosis. Southern medical journal 63: 580–583. 5446827
34. Hostutler RA, DiBartola SP, Eaton KA, (2004) Transient proximal renal tubular acidosis and Fanconi syndrome in a dog. J Am Vet Med Assoc 224: 1611–1614, 1605. 15154730
35. Khositseth S, Sudjaritjan N, Tananchai P, Ong-ajyuth S, Sitprija V, et al. (2008) Renal magnesium wasting and tubular dysfunction in leptospirosis. Nephrol Dial Transplant 23: 952–958. 17951309
36. Kuo HL, Lin CL, Huang CC, (2003) Reversible thick ascending limb dysfunction and aseptic meningitis syndrome: early manifestation in two leptospirosis patients. Ren Fail 25: 639–646. 12911169
37. Lin CL, Wu MS, Yang CW, Huang CC, (1999) Leptospirosis associated with hypokalaemia and thick ascending limb dysfunction. Nephrol Dial Transplant 14: 193–195. 10052507
38. Yang CW, Pan MJ, Wu MS, Chen YM, Tsen YT, et al. (1997) Leptospirosis: an ignored cause of acute renal failure in Taiwan. Am J Kidney Dis 30: 840–845. 9398130
39. Yang CW, Wu MS, Pan MJ, (2001) Leptospirosis renal disease. Nephrol Dial Transplant 16 Suppl 5: 73–77. 11509689
40. Monahan AM, Callanan JJ, Nally JE, (2009) Review paper: Host-pathogen interactions in the kidney during chronic leptospirosis. Vet Pathol 46: 792–799. doi: 10.1354/vp.08-VP-0265-N-REV 19429975
41. Marotto PC, Ko AI, Murta-Nascimento C, Seguro AC, Prado RR, et al. (2010) Early identification of leptospirosis-associated pulmonary hemorrhage syndrome by use of a validated prediction model. J Infect 60: 218–223. doi: 10.1016/j.jinf.2009.12.005 20026189
42. Chakurkar G, Vaideeswar P, Pandit SP, Divate SA, (2008) Cardiovascular lesions in leptospirosis: an autopsy study. J Infect 56: 197–203. doi: 10.1016/j.jinf.2007.12.007 18262280
43. Daher Ede F, Junior Silva GB, Vieira AP, Souza JB, Falcao Fdos S, et al. (2014) Acute kidney injury in a tropical country: a cohort study of 253 patients in an infectious diseases intensive care unit. Rev Soc Bras Med Trop 47: 86–89. doi: 10.1590/0037-8682-0223-2013 24603743
44. Turhan V, Atasoyu EM, Solmazgul E, Evrenkaya R, Cavuslu S, (2005) Anicteric leptospirosis and renal involvement. Ren Fail 27: 491–492. 16060140
45. Turhan V, Polat E, Murat Atasoyu E, Ozmen N, Kucukardali Y, et al. (2006) Leptospirosis in Istanbul, Turkey: a wide spectrum in clinical course and complications. Scand J Infect Dis 38: 845–852. 17008227
46. Atasoyu EM, Turhan V, Unver S, Evrenkaya TR, Yildirim S, (2005) A case of leptospirosis presenting with end-stage renal failure. Nephrol Dial Transplant 20: 2290–2292. 16046514
47. Cetin BD, Harmankaya O, Hasman H, Gunduz A, Oktar M, et al. (2004) Acute renal failure: a common manifestation of leptospirosis. Ren Fail 26: 655–661. 15600257
48. Herath NJ, Kularatne SA, Weerakoon KG, Wazil A, Subasinghe N, et al. (2014) Long term outcome of acute kidney injury due to leptospirosis? A longitudinal study in Sri Lanka. BMC Res Notes 7: 398. doi: 10.1186/1756-0500-7-398 24964804
49. Barnes K, Kenny AJ, Turner AJ, (1994) Localization of aminopeptidase N and dipeptidyl peptidase IV in pig striatum and in neuronal and glial cell cultures. Eur J Neurosci 6: 531–537. 7912983
50. Semenza G, (1986) Anchoring and biosynthesis of stalked brush border membrane proteins: glycosidases and peptidases of enterocytes and renal tubuli. Annu Rev Cell Biol 2: 255–313. 3548768
51. Sanderink GJ, Artur Y, Siest G, (1988) Human aminopeptidases: a review of the literature. J Clin Chem Clin Biochem 26: 795–807. 3069949
52. Lendeckel U, Wex T, Reinhold D, Kahne T, Frank K, et al. (1996) Induction of the membrane alanyl aminopeptidase gene and surface expression in human T-cells by mitogenic activation. Biochem J 319 (Pt 3): 817–821. 8920985
53. Hooper NM, (1994) Families of zinc metalloproteases. FEBS Lett 354: 1–6. 7957888
54. Hooper NM, Hesp RJ, Tieku S, (1994) Metabolism of aspartame by human and pig intestinal microvillar peptidases. Biochem J 298 Pt 3: 635–639. 8141778
55. Mina-Osorio P, (2008) The moonlighting enzyme CD13: old and new functions to target. Trends Mol Med 14: 361–371. doi: 10.1016/j.molmed.2008.06.003 18603472
56. Villasenor-Cardoso MI, Frausto-Del-Rio DA, Ortega E, (2013) Aminopeptidase N (CD13) is involved in phagocytic processes in human dendritic cells and macrophages. Biomed Res Int 2013: 562984. doi: 10.1155/2013/562984 24063007
57. Ghosh M, McAuliffe B, Subramani J, Basu S, Shapiro LH, (2012) CD13 regulates dendritic cell cross-presentation and T cell responses by inhibiting receptor-mediated antigen uptake. J Immunol 188: 5489–5499. doi: 10.4049/jimmunol.1103490 22544935
58. Chen L, Gao Z, Zhu J, Rodgers GP, (2007) Identification of CD13+CD36+ cells as a common progenitor for erythroid and myeloid lineages in human bone marrow. Exp Hematol 35: 1047–1055. 17588473
59. Inoi K, Goto S, Nomura S, Isobe K, Nawa A, et al. (1995) Aminopeptidase inhibitor ubenimex (bestatin) inhibits the growth of human choriocarcinoma in nude mice through its direct cytostatic activity. Anticancer Res 15: 2081–2087. 8572606
60. Wex T, Lendeckel U, Reinhold D, Kahne T, Arndt M, et al. (1997) Antisense-mediated inhibition of aminopeptidase N (CD13) markedly decreases growth rates of hematopoietic tumour cells. Adv Exp Med Biol 421: 67–73. 9330681
61. Chang YW, Chen SC, Cheng EC, Ko YP, Lin YC, et al. (2005) CD13 (aminopeptidase N) can associate with tumor-associated antigen L6 and enhance the motility of human lung cancer cells. Int J Cancer 116: 243–252. 15812828
62. Tani K, Ogushi F, Huang L, Kawano T, Tada H, et al. (2000) CD13/aminopeptidase N, a novel chemoattractant for T lymphocytes in pulmonary sarcoidosis. Am J Respir Crit Care Med 161: 1636–1642. 10806168
63. Larsen SL, Pedersen LO, Buus S, Stryhn A, (1996) T cell responses affected by aminopeptidase N (CD13)-mediated trimming of major histocompatibility complex class II-bound peptides. J Exp Med 184: 183–189. 8691132
64. Gabrilovac J, Breljak D, Cupic B, Ambriovic-Ristov A, (2005) Regulation of aminopeptidase N (EC 3.4.11.2; APN; CD13) by interferon-gamma on the HL-60 cell line. Life Sci 76: 2681–2697. 15792835
65. Amoscato AA, Prenovitz DA, Lotze MT, (1998) Rapid extracellular degradation of synthetic class I peptides by human dendritic cells. J Immunol 161: 4023–4032. 9780172
66. Tokuda N, Levy RB, (1996) 1,25-dihydroxyvitamin D3 stimulates phagocytosis but suppresses HLA-DR and CD13 antigen expression in human mononuclear phagocytes. Proc Soc Exp Biol Med 211: 244–250. 8633104
67. Soderberg C, Giugni TD, Zaia JA, Larsson S, Wahlberg JM, et al. (1993) CD13 (human aminopeptidase N) mediates human cytomegalovirus infection. J Virol 67: 6576–6585. 8105105
68. Soderberg C, Larsson S, Bergstedt-Lindqvist S, Moller E, (1993) Definition of a subset of human peripheral blood mononuclear cells that are permissive to human cytomegalovirus infection. J Virol 67: 3166–3175. 7684461
69. Yeager CL, Ashmun RA, Williams RK, Cardellichio CB, Shapiro LH, et al. (1992) Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357: 420–422. 1350662
70. Hansen GH, Delmas B, Besnardeau L, Vogel LK, Laude H, et al. (1998) The coronavirus transmissible gastroenteritis virus causes infection after receptor-mediated endocytosis and acid-dependent fusion with an intracellular compartment. J Virol 72: 527–534. 9420255
71. Nomura R, Kiyota A, Suzaki E, Kataoka K, Ohe Y, et al. (2004) Human coronavirus 229E binds to CD13 in rafts and enters the cell through caveolae. J Virol 78: 8701–8708. 15280478
72. van Hensbergen Y, Broxterman HJ, Hanemaaijer R, Jorna AS, van Lent NA, et al. (2002) Soluble aminopeptidase N/CD13 in malignant and nonmalignant effusions and intratumoral fluid. Clin Cancer Res 8: 3747–3754. 12473585
73. van Hal PT, Hopstaken-Broos JP, Prins A, Favaloro EJ, Huijbens RJ, et al. (1994) Potential indirect anti-inflammatory effects of IL-4. Stimulation of human monocytes, macrophages, and endothelial cells by IL-4 increases aminopeptidase-N activity (CD13; EC 3.4.11.2). J Immunol 153: 2718–2728. 7915741
74. Delmas B, Gelfi J, L'Haridon R, Vogel LK, Sjostrom H, et al. (1992) Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357: 417–420. 1350661
75. Petrovic N, Schacke W, Gahagan JR, O'Conor CA, Winnicka B, et al. (2007) CD13/APN regulates endothelial invasion and filopodia formation. Blood 110: 142–150. 17363739
76. Navarrete Santos A, Roentsch J, Danielsen EM, Langner J, Riemann D, (2000) Aminopeptidase N/CD13 is associated with raft membrane microdomains in monocytes. Biochem Biophys Res Commun 269: 143–148. 10694491
77. Riemann D, Hansen GH, Niels-Christiansen L, Thorsen E, Immerdal L, et al. (2001) Caveolae/lipid rafts in fibroblast-like synoviocytes: ectopeptidase-rich membrane microdomains. Biochem J 354: 47–55. 11171078
78. van Balkom BW, Pisitkun T, Verhaar MC, Knepper MA, (2011) Exosomes and the kidney: prospects for diagnosis and therapy of renal diseases. Kidney Int 80: 1138–1145. doi: 10.1038/ki.2011.292 21881557
79. Cheville NF, Huhn R, Cutlip RC, (1980) Ultrastructure of renal lesions in pigs with acute leptospirosis caused by Leptospira pomona. Vet Pathol 17: 338–351. 7368526
80. Alves VA, Gayotto LC, Yasuda PH, Wakamatsu A, Kanamura CT, et al. (1991) Leptospiral antigens (L. interrogans serogroup ictero-haemorrhagiae) in the kidney of experimentally infected guinea pigs and their relation to the pathogenesis of the renal injury. Exp Pathol 42: 81–93. 1879516
81. Lasser C, Eldh M, Lotvall J, (2012) Isolation and characterization of RNA-containing exosomes. J Vis Exp: e3037. doi: 10.3791/3037 22257828
82. Kokot F, Dulawa J, (2000) Tamm-Horsfall protein updated. Nephron 85: 97–102. 10867513
83. Mo L, Zhu XH, Huang HY, Shapiro E, Hasty DL, et al. (2004) Ablation of the Tamm-Horsfall protein gene increases susceptibility of mice to bladder colonization by type 1-fimbriated Escherichia coli. Am J Physiol Renal Physiol 286: F795–802. 14665435
84. Saemann MD, Weichhart T, Horl WH, Zlabinger GJ, (2005) Tamm-Horsfall protein: a multilayered defence molecule against urinary tract infection. Eur J Clin Invest 35: 227–235. 15816991
85. Cavallone D, Malagolini N, Serafini-Cessi F, (2001) Mechanism of release of urinary Tamm-Horsfall glycoprotein from the kidney GPI-anchored counterpart. Biochem Biophys Res Commun 280: 110–114. 11162486
86. Fukuoka S, Freedman SD, Yu H, Sukhatme VP, Scheele GA, (1992) GP-2/THP gene family encodes self-binding glycosylphosphatidylinositol-anchored proteins in apical secretory compartments of pancreas and kidney. Proc Natl Acad Sci U S A 89: 1189–1193. 1531535
87. Pisitkun T, Shen RF, Knepper MA, (2004) Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A 101: 13368–13373. 15326289
88. Gonzales PA, Pisitkun T, Hoffert JD, Tchapyjnikov D, Star RA, et al. (2009) Large-scale proteomics and phosphoproteomics of urinary exosomes. J Am Soc Nephrol 20: 363–379. doi: 10.1681/ASN.2008040406 19056867