Specific renal parenchymal-derived urinary extracellular vesicles identify age-associated structural changes in living donor kidneys

Journal of Extracellular Vesicles

Volumn 5, Issue 1, 2016, Pages

  Turco, Anne E ^a   Lam, Wing ^a   Rule, Andrew D ^b   Denic, Aleksandar ^b   Lieske, John C ^b   Miller, Virginia M ^a,b   Larson, Joseph J ^c   Kremers, Walter K ^c   Jayachandran, Muthuvel ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c Mayo Clinic   (United States)

Author keywords

arteriosclerosis; exosomes; fibrosis; glomerulosclerosis; microparticles; microvesicles; nephron hypertrophy; urinary vesicles

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1;

ADULT; AGE; AGED; ARTERIOSCLEROSIS; ARTICLE; CELL POPULATION; COLLECTING TUBULE CELL; CONTROLLED STUDY; DIAGNOSTIC TEST; EXOSOME; FEMALE; FLOW CYTOMETRY; GLOMERULOSCLEROSIS; HENLE LOOP; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERMETHOD COMPARISON; JUXTAGLOMERULAR CELL; KIDNEY BIOPSY; KIDNEY DONOR; KIDNEY EPITHELIUM; KIDNEY FIBROSIS; KIDNEY HYPERTROPHY; KIDNEY PARENCHYMA; KIDNEY PELVIS; KIDNEY STRUCTURE; KIDNEY TUBULE CELL; LIVING DONOR; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NEPHROSCLEROSIS; ORGAN DONOR; PODOCYTE; URINE SAMPLING;

EID: 85009240617     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.3402/jev.v5.29642     Document Type: Article

References (44)

1. Nyengaard JR, Bendtsen TF. Glomerular number and size in relation to age, kidney weight, and body surface in normal man. Anat Rec. 1992; 232: 194–201. http://dx.doi.org/10.1002/ar.1092320205 [PubMed Abstract].
2. Rule AD, Amer H, Cornell LD, Taler SJ, Cosio FG, Kremers WK, etal. The association between age and nephrosclerosis on renal biopsy among healthy adults. Ann Intern Med. 2010; 152: 561–7. http://dx.doi.org/10.7326/0003-4819-152-9-201005040-00006 [PubMed Abstract] [PubMed CentralFull Text].
3. Wang X, Vrtiska TJ, Avula RT, Walters LR, Chakkera HA, Kremers WK, etal. Age, kidney function, and risk factors associate differently with cortical and medullary volumes of the kidney. Kidney Int. 2014; 85: 677–85. http://dx.doi.org/10.1038/ki.2013.359 [PubMed Abstract] [PubMed CentralFull Text].
4. Duan X, Rule AD, Elsherbiny H, Vrtiska TJ, Avula RT, Alexander MP, etal. Automated assessment of renal cortical surface roughness from computerized tomography images and its association with age. Acad Radiol. 2014; 21: 1441–5. http://dx.doi.org/10.1016/j.acra.2014.05.014 [PubMed Abstract] [PubMed CentralFull Text].
5. Al-Said J, Brumback MA, Moghazi S, Baumgarten DA, O'Neill WC. Reduced renal function in patients with simple renal cysts. Kidney Int. 2004; 65: 2303–8. http://dx.doi.org/10.1111/j.1523-1755.2004.00651.x [PubMed Abstract].
6. Rodriguez-Castro EM, Cordova HR. Aging and the kidney. Bol Asoc Med P R. 2011; 103: 57–62. [PubMed Abstract].
7. Lee TH, D'Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J. Microvesicles as mediators of intercellular communication in cancer–the emerging science of cellular ‘debris’. Semin Immunopathol. 2011; 33: 455–67. http://dx.doi.org/10.1007/s00281-011-0250-3 [PubMed Abstract].
8. Duijvesz D, Burnum-Johnson KE, Gritsenko MA, Hoogland AM. Vredenbregt-van den Berg MS, Willemsen R, et al. Proteomic profiling of exosomes leads to the identification of novel biomarkers for prostate cancer. PLoS One. 2013; 8: 82589. http://dx.doi.org/10.1371/journal.pone.0082589.
9. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood. 1999; 94: 3791–9. [PubMed Abstract].
10. Jayachandran M, Lugo G, Heiling H, Miller VM, Rule AD, Lieske JC. Extracellular vesicles in urine of women with but not without kidney stones manifest patterns similar to men: a case control study. Biol Sex Differ. 2015; 6: 2. http://dx.doi.org/10.1186/s13293-015-0021-2 [PubMed Abstract] [PubMed CentralFull Text].
11. Knepper MA, Pisitkun T. Exosomes in urine: who would have thought…?. Kidney Int. 2007; 72: 1043–5. http://dx.doi.org/10.1038/sj.ki.5002510 [PubMed Abstract].
12. van Balkom BW, Pisitkun T, Verhaar MC, Knepper MA. Exosomes and the kidney: prospects for diagnosis and therapy of renal diseases. Kidney Int. 2011; 80: 1138–45. http://dx.doi.org/10.1038/ki.2011.292 [PubMed Abstract] [PubMed CentralFull Text].
13. Gamez-Valero A, Lozano-Ramos SI, Bancu I, Lauzurica-Valdemoros R, Borras FE. Urinary extracellular vesicles as source of biomarkers in kidney diseases. Front Immunol. 2015; 6: 6. http://dx.doi.org/10.3389/fimmu.2015.00006 [PubMed Abstract] [PubMed CentralFull Text].
14. Borges FT, Reis LA, Schor N. Extracellular vesicles: structure, function, and potential clinical uses in renal diseases. Braz J Med Biol Res. 2013; 46: 824–30. http://dx.doi.org/10.1590/1414-431X20132964 [PubMed Abstract] [PubMed CentralFull Text].
15. Elsherbiny HE, Alexander MP, Kremers WK, Park WD, Poggio ED, Prieto M, etal. Nephron hypertrophy and glomerulosclerosis and their association with kidney function and risk factors among living kidney donors. Clin J Am Soc Nephrol. 2014; 9: 1892–902. http://dx.doi.org/10.2215/CJN.02560314 [PubMed Abstract] [PubMed CentralFull Text].
16. Rule AD, Semret MH, Amer H, Cornell LD, Taler SJ, Lieske JC, etal. Association of kidney function and metabolic risk factors with density of glomeruli on renal biopsy samples from living donors. Mayo Clin Proc. 2011; 86: 282–90. http://dx.doi.org/10.4065/mcp.2010.0821 [PubMed Abstract] [PubMed CentralFull Text].
17. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF, 3rd, Feldman HI, etal. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009; 150: 604–12. [PubMed Abstract] [PubMed CentralFull Text].
18. Fernandez-Llama P, Khositseth S, Gonzales PA, Star RA, Pisitkun T, Knepper MA. Tamm-Horsfall protein and urinary exosome isolation. Kidney Int. 2010; 77: 736–42. http://dx.doi.org/10.1038/ki.2009.550 [PubMed Abstract] [PubMed CentralFull Text].
19. Kosanovic M, Jankovic M. Isolation of urinary extracellular vesicles from Tamm–Horsfall protein-depleted urine and their application in the development of a lectin-exosome-binding assay. Biotechniques. 2014; 57: 143–9. http://dx.doi.org/10.2144/000114208 [PubMed Abstract].
20. Jayachandran M, Miller VM, Heit JA, Owen WG. Methodology for isolation, identification and characterization of microvesicles in peripheral blood. J Immunol Methods. 2012; 375: 207–14. http://dx.doi.org/10.1016/j.jim.2011.10.012 [PubMed Abstract] [PubMed CentralFull Text].
21. Jayachandran M, Litwiller RD, Owen WG, Heit JA, Behrenbeck T, Mulvagh SL, etal. Characterization of blood borne microparticles as markers of premature coronary calcification in newly menopausal women. Am J Physiol Heart Circ Physiol. 2008; 295: 931–H8. http://dx.doi.org/10.1152/ajpheart.00193.2008.
22. Segerer S, Nelson PJ, Schlondorff D. Chemokines, chemokine receptors, and renal disease: from basic science to pathophysiologic and therapeutic studies. J Am Soc Nephrol. 2000; 11: 152–76. [PubMed Abstract].
23. Lee SB, Kalluri R. Mechanistic connection between inflammation and fibrosis. Kidney Int Suppl. 2010; 22–6. http://dx.doi.org/10.1038/ki.2010.418.
24. Loyer X, Vion AC, Tedgui A, Boulanger CM. Microvesicles as cell-cell messengers in cardiovascular diseases. Circ Res. 2014; 114: 345–53. http://dx.doi.org/10.1161/CIRCRESAHA.113.300858 [PubMed Abstract].
25. Leroyer AS, Isobe H, Leseche G, Castier Y, Wassef M, Mallat Z, etal. Cellular origins and thrombogenic activity of microparticles isolated from human atherosclerotic plaques. J Am Coll Cardiol. 2007; 49: 772–7. http://dx.doi.org/10.1016/j.jacc.2006.10.053 [PubMed Abstract].
26. Gustafson CM, Shepherd AJ, Miller VM, Jayachandran M. Age- and sex-specific differences in blood-borne microvesicles from apparently healthy humans. Biol Sex Differ. 2015; 6: 10. http://dx.doi.org/10.1186/s13293-015-0028-8 [PubMed Abstract] [PubMed CentralFull Text].
27. Miller VM, Lahr BD, Bailey KR, Heit JA, Harman SM, Jayachandran M. Longitudinal effects of menopausal hormone treatments on platelet characteristics and cell-derived microvesicles. Platelets. 2015; 1–11. http://dx.doi.org/10.3109/09537104.2015.1023273.
28. Tatsumi K, Mackman N. Tissue Factor and Atherothrombosis. J Atheroscler Thromb. 2015; 22: 543–9. http://dx.doi.org/10.5551/jat.30940 [PubMed Abstract].
29. Hoy WE, Douglas-Denton RN, Hughson MD, Cass A, Johnson K, Bertram JF. A stereological study of glomerular number and volume: preliminary findings in a multiracial study of kidneys at autopsy. Kidney Int Suppl. 2003; 31–7. http://dx.doi.org/10.1046/j.1523-1755.63.s83.8.x.
30. Kwan G, Neugarten J, Sherman M, Ding Q, Fotadar U, Lei J, etal. Effects of sex hormones on mesangial cell proliferation and collagen synthesis. Kidney Int. 1996; 50: 1173–9.
31. Verzola D, Gandolfo MT, Salvatore F, Villaggio B, Gianiorio F, Traverso P, etal. Testosterone promotes apoptotic damage in human renal tubular cells. Kidney Int. 2004; 65: 1252–61. http://dx.doi.org/10.1111/j.1523-1755.2004.00497.x [PubMed Abstract].
32. Hannedouche T, Chauveau P, Kalou F, Albouze G, Lacour B, Jungers P. Factors affecting progression in advanced chronic renal failure. Clin Nephrol. 1993; 39: 312–20. [PubMed Abstract].
33. Stewart JH. End-stage renal failure appears earlier in men than in women with polycystic kidney disease. Am J Kidney Dis. 1994; 24: 181–3.
34. Schena FP. A retrospective analysis of the natural history of primary IgA nephropathy worldwide. Am J Med. 1990; 89: 209–15.
35. Gabow PA, Johnson AM, Kaehny WD, Kimberling WJ, Lezotte DC, Duley IT, etal. Factors affecting the progression of renal disease in autosomal-dominant polycystic kidney disease. Kidney Int. 1992; 41: 1311–9.
36. Wiggins JE, Goyal M, Sanden SK, Wharram BL, Shedden KA, Misek DE, etal. Podocyte hypertrophy, “adaptation,” and “decompensation” associated with glomerular enlargement and glomerulosclerosis in the aging rat: prevention by calorie restriction. J Am Soc Nephrol. 2005; 16: 2953–66. http://dx.doi.org/10.1681/ASN.2005050488 [PubMed Abstract].
37. Esposito C, Dal Canton A. Functional changes in the aging kidney. J Nephrol. 2010; 23(Suppl 15):S41–5. [PubMed Abstract].
38. Huber TB, Edelstein CL, Hartleben B, Inoki K, Jiang M, Koya D, etal. Emerging role of autophagy in kidney function, diseases and aging. Autophagy. 2012; 8: 1009–31. http://dx.doi.org/10.4161/auto.19821 [PubMed Abstract] [PubMed CentralFull Text].
39. Wiggins JE. Aging in the glomerulus. J Gerontol A Biol Sci Med Sci. 2012; 67: 1358–64. http://dx.doi.org/10.1093/gerona/gls157 [PubMed Abstract] [PubMed CentralFull Text].
40. Zhang J, Hansen KM, Pippin JW, Chang AM, Taniguchi Y, Krofft RD, etal. De novo expression of podocyte proteins in parietal epithelial cells in experimental aging nephropathy. Am J Physiol Renal Physiol. 2012; 302: 571–80. http://dx.doi.org/10.1152/ajprenal.00516.2011.
41. Miranda KC, Bond DT, McKee M, Skog J, Paunescu TG, Da Silva N, etal. Nucleic acids within urinary exosomes/microvesicles are potential biomarkers for renal disease. Kidney Int. 2010; 78: 191–9. http://dx.doi.org/10.1038/ki.2010.106 [PubMed Abstract] [PubMed CentralFull Text].
42. Beltrami C, Clayton A, Newbury LJ, Corish P, Jenkins RH, Phillips AO, etal. Stabilization of urinary microRNAs by association with exosomes and argonaute 2 protein. Non-Coding RNA. 2015; 1: 151–61. http://dx.doi.org/10.3390/ncrna1020151.
43. Lv LL, Cao YH, Pan MM, Liu H, Tang RN, Ma KL, etal. CD2AP mRNA in urinary exosome as biomarker of kidney disease. Clin Chim Acta. 2014; 428: 26–31. http://dx.doi.org/10.1016/j.cca.2013.10.003 [PubMed Abstract].
44. Murakami T, Oakes M, Ogura M, Tovar V, Yamamoto C, Mitsuhashi M. Development of glomerulus-, tubule-, and collecting duct-specific mRNA assay in human urinary exosomes and microvesicles. PLoS One. 2014; 9: 109074. http://dx.doi.org/10.1371/journal.pone.0109074.