Two-dimensional differential in-gel electrophoresis proteomic approaches reveal urine candidate biomarkers in pediatric obstructive sleep apnea

American Journal of Respiratory and Critical Care Medicine

Volumn 180, Issue 12, 2009, Pages 1253-1261

  Gozal, David ^a   Jortani, Saeed ^b   Snow, Ayelet B ^b   Kheirandish Gozal, Leila ^a   Bhattacharjee, Rakesh ^b   Kim, Jinkwan ^b   Capdevila, Oscar Sans ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

Biomarkers; Children; Sleep apnea; Urine

Indexed keywords

ALPHA 1 MICROGLOBULIN; GLYCOPROTEIN; HISTONE ACETYLTRANSFERASE PCAF; KALLIKREIN; NUCLEIC ACID BINDING PROTEIN; OROSOMUCOID; OROSOMUCOID 1; OROSOMUCOID 2; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; SIGNAL PEPTIDE; TAMM HORSFALL GLYCOPROTEIN; TENASCIN; TRIBBLES HOMOLOG 2; TRISTETRAPROLIN; ULINASTATIN; UNCLASSIFIED DRUG; UROCORTIN III; ZINC FINGER PROTEIN 81;

ARTICLE; CHILD; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; IMMUNOBLOTTING; MAJOR CLINICAL STUDY; MALE; MASS SPECTROMETRY; POLYSOMNOGRAPHY; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN URINE LEVEL; PROTEOMICS; RECEIVER OPERATING CHARACTERISTIC; SCHOOL CHILD; SENSITIVITY AND SPECIFICITY; SLEEP APNEA SYNDROME; SNORING; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

BIOLOGICAL MARKERS; BLOTTING, WESTERN; CHILD; COHORT STUDIES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; MALE; MASS SPECTROMETRY; POLYSOMNOGRAPHY; PREDICTIVE VALUE OF TESTS; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; ROC CURVE; SENSITIVITY AND SPECIFICITY; SLEEP APNEA, OBSTRUCTIVE;

EID: 72549085929     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200905-0765OC     Document Type: Article

References (66)

1. Sans Capdevila O, Kheirandish-Gozal L, Dayyat E, Gozal D. Pediatric obstructive sleep apnea: complications, management, and long-term outcomes. Proc Am Thorac Soc 2008;5:274-282. (Pubitemid 351237887)
2. Gozal D. Obstructive sleep apnea in children: implications for the developing central nervous system. Semin Pediatr Neurol 2008;15:100-106. (Pubitemid 351802264)
3. Gozal D, Kheirandish-Gozal L. Cardiovascular morbidity in obstructive sleep apnea: oxidative stress, inflammation, and much more. Am J Respir Crit Care Med 2008;177:369-375. (Pubitemid 351317579)
4. O'Brien LM, Mervis CB, Holbrook CR, Bruner JL, Smith NH, McNally N, McClimment MC, Gozal D. Neurobehavioral correlates of sleep-disordered breathing in children. J Sleep Res 2004;13:165-172. (Pubitemid 38829898)
5. Ferreira AM, Clemente V, Gozal D, Gomes A, Pissarra C, Cé sar H, Coelho I, Silva CF, Azevedo MHP. Snoring in Portuguese primary school children. Pediatrics 2000;106:E64.
6. O'Brien LM, Holbrook CR, Mervis CB, Klaus CJ, Bruner J, Raffield TJ, Rutherford J, Mehl RC, Wang M, Tuell A, et al. Sleep and neuro-behavioral characteristics in 5-7-year-old hyperactive children. Pediatrics 2003;111:554-563.
7. Urschitz MS, Guenther A, Eitner S, Urschitz-Duprat PM, Schlaud M, Ipsiroglu OS, Poets CF. Risk factors and natural history of habitual snoring. Chest 2004;126:790-800. (Pubitemid 39258033)
8. Kaditis AG, Finder J, Alexopoulos EI, Starantzis K, Tanou K, Gampeta S, Agorogiannis E, Christodoulou S, Pantazidou A, Gourgoulianis K, et al. Sleep-disordered breathing in 3,680 Greek children. Pediatr Pulmonol 2004;37:499-509. (Pubitemid 38680116)
9. Rosen CL, Larkin EK, Kirchner HL, Emancipator JL, Bivins SF, Surovec SA, Martin RJ, Redline S. Prevalence and risk factors for sleep-disordered breathing in 8- to 11-year-old children: association with race and prematurity. J Pediatr 2003;142:383-389. (Pubitemid 36521224)
10. Montgomery-Downs HE, O'Brien LM, Holbrook CR, Gozal D. Snoring and sleep-disordered breathing in young children: subjective and objective correlates. Sleep 2004;27:87-94. (Pubitemid 43906317)
11. Montgomery-Downs HE, Gozal D. Sleep habits and risk factors for sleep-disordered breathing in infants and young toddlers in Louisville, Kentucky. Sleep Med 2006;7:211-219.
12. Carroll JL, McColley SA, Marcus CL, Curtis S, Loughlin GM. Inability of clinical history to distinguish primary snoring from obstructive sleep apnea syndrome in children. Chest 1995;108:610-618.
13. Wang RC, Elkins TP, Keech D, Wauquier A, Hubbard D. Accuracy of clinical evaluation in pediatric obstructive sleep apnea. Otolaryngol Head Neck Surg 1998;118:69-73. (Pubitemid 28086436)
14. Bhattacharjee R, Dayyat E, Kheirandish-Gozal L, Capdevila OS, Gozal D. Nocturnal polysomnographic characteristics of habitually snoring children initially referred to pediatric ENT or sleep clinics. Sleep Med. 2009;10:1031-1034.
15. Schechter MS; Section on Pediatric Pulmonology, Subcommittee on Obstructive Sleep Apnea Syndrome. Technical report: diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics 2002;109:e69.
16. Krishna J, Shah ZA, Merchant M, Klein JB, Gozal D. Urinary protein expression patterns in children with sleep-disordered breathing: preliminary findings. Sleep Med 2006;7:221-227.
17. Larbi NB, Jefferies C. 2D-DIGE: comparative proteomics of cellular signaling pathways. Methods Mol Biol 2009;517:1-28.
18. Montgomery-Downs HE, O'Brien LM, Gulliver TE, Gozal D. Polysomnographic characteristics in normal preschool and early school-aged children. Pediatrics 2006;117:741-753. (Pubitemid 46063216)
19. Rechstschaffen A, Kales A. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Los Angeles: Brain Information Services/Brain Research Institute, University of California; 1968.
20. Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. EEG arousals: scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. Sleep 1992;15:173-184.
21. Christiansen MS, Blirup-Jensen S, Foged L, Larsen M, Magid E. A particle-enhanced turbidimetric immunoassay for quantitative determination of orosomucoid in urine: development, validation and reference values. Clin Chem Lab Med 2004;42:1168-1177. (Pubitemid 39481159)
22. DeLeo J. Receiver operating characteristic laboratory (ROCLAB): software for developing decision strategies that account for uncertainty. In: Ayyub BM, editor. Proceedings of the second international symposium on uncertainty modeling and analysis. Los Alamitos, CA: IEEE Computer Society Press; 1993. pp. 318-325.
23. Reiner A, Yekutieli D, Benjamini Y. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 2003;19:368-375. (Pubitemid 36284936)
24. Zolotarjova N, Martosella J, Nicol G, Bailey J, Boyes BE, Barrett WC. Differences among techniques for high-abundant protein depletion. Proteomics 2005;5:3304-3313. (Pubitemid 41192037)
25. Liu H, Sadygov RG, Yates JR III. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 2004;76:4193-4201. (Pubitemid 38943698)
26. Old WM, Meyer-Arendt K, Aveline-Wolf L, Pierce KG, Mendoza A, Sevinsky JR, Resing KA, Ahn NG. Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol Cell Proteomics 2005;4:1487-1502. (Pubitemid 41555475)
27. Nesvizhskii AI, Vitek O, Aebersold R. Analysis and validation of proteomic data generated by tandem mass spectrometry. Nat Methods 2007;4:787-797. (Pubitemid 350055575)
28. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci USA 2004;101:13368-13373. (Pubitemid 39209672)
29. Fukuoka S, Kobayashi K. Analysis of the C-terminal structure of urinary Tamm-Horsfall protein reveals that the release of the glycosyl phosphatidylinositol-anchored counterpart from the kidney occurs by phenylalanine-specific proteolysis. Biochem Biophys Res Commun 2001;289:1044-1048. (Pubitemid 34076295)
30. El-Achkar TM, Wu XR, Rauchman M, McCracken R, Kiefer S, Dagher PC. Tamm-Horsfall protein protects the kidney from ischemic injury by decreasing inflammation and altering TLR4 expression. Am J Physiol Renal Physiol 2008;295:F534-F544.
31. Serafini-Cessi F, Malagolini N, Cavallone D. Tamm-Horsfall glycoprotein: biology and clinical relevance. Am J Kidney Dis 2003;42:658-676. (Pubitemid 37187366)
32. Thornley C, Dawnay A, Cattell WR. Human Tamm-Horsfall glycoprotein: urinary and plasma levels in normal subjects and patients with renal disease determined by a fully validated radioimmunoassay. Clin Sci (Lond) 1985;68:529-535. (Pubitemid 15103432)
33. Lynn KL, Marshall RD. Excretion of Tamm-Horsfall glycoprotein in renal disease. Clin Nephrol 1984;22:253-257.
34. Pugia MJ, Valdes R Jr, Jortani SA. Bikunin (urinary trypsin inhibitor): structure, biological relevance, and measurement. Adv Clin Chem 2007;44:223-245.
35. Pugia MJ, Jortani SA, Basu M, Sommer R, Kuo HH, Murphy S, Williamson D, Vranish J, Boyle PJ, Budzinski D, Valdes R Jr, Basu SC. Immunological evaluation of urinary trypsin inhibitors in blood and urine: role of N- and O-linked glycoproteins. Glycoconj J 2007;24:5-15. (Pubitemid 44935060)
36. 1-Microglobulin: clinical laboratory aspects and applications. Clin Chim Acta 2004;346:107-118.
37. Guder WG, Hofmann W. Clinical role of urinary low molecular weight proteins: their diagnostic and prognostic implications. Scand J Clin Lab Invest Suppl 2008;241:95-98. (Pubitemid 351883666)
38. Khalyfa A, Capdevila OS, Buazza MO, Serpero LD, Kheirandish-Gozal L, Gozal D. Genome-wide gene expression profiling in children with non-obese obstructive sleep apnea. Sleep Med 2009;10:75-86.
39. Bhattacharjee R, Kheirandish-Gozal L, Pillar G, Gozal D. Cardiovascular complications of obstructive sleep apnea syndrome: evidence from children. Prog Cardiovasc Dis 2009;51:416-433.
40. Deng J, James CH, Patel L, Smith A, Burnand KG, Rahmoune H, Lamb JR, Davis B. Human tribbles homologue 2 is expressed in unstable regions of carotid plaques and regulates macrophage IL-10 in vitro. Clin Sci (Lond) 2009;116:241-248.
41. Gozal D, Capdevila OS, Kheirandish-Gozal L. Metabolic alterations and systemic inflammation in obstructive sleep apnea among nonobese and obese prepubertal children. Am J Respir Crit Care Med 2008;177:1142-1149. (Pubitemid 351717574)
42. Gozal D, Serpero LD, Sans Capdevila O, Kheirandish-Gozal L. Systemic inflammation in non-obese children with obstructive sleep apnea. Sleep Med 2008;9:254-259.
43. Gozal D, Kheirandish-Gozal L, Serpero LD, Sans Capdevila O, Dayyat E. Obstructive sleep apnea and endothelial function in school-aged nonobese children: effect of adenotonsillectomy. Circulation 2007;116:2307-2314. (Pubitemid 350100337)
44. Naiki T, Saijou E, Miyaoka Y, Sekine K, Miyajima A. TRB2, a mouse Tribbles ortholog, suppresses adipocyte differentiation by inhibiting AKT and C/EBPβ. J Biol Chem 2007;282:24075-24082. (Pubitemid 47328047)
45. Fournier T, Medjoubi NN, Porquet D. Alpha-1-acid glycoprotein. Biochim Biophys Acta 2000;1482:157-171.
46. 1-acid glycoprotein. Biochim Biophys Acta 1977;492:291-302.
47. Mackiewicz A, Ganapathi MK, Schultz D, Kushner I. Monokines regulate glycosylation of acute-phase proteins. J Exp Med 1987;166:253-258. (Pubitemid 17101905)
48. 1-acid glycoprotein (orosomucoid) in human sera. J Exp Med 1993;177:657-666.
49. 1-acid glycoprotein. Clin Exp Immunol 1984;55:465-472.
50. 1-acid glycoprotein probably due to steric hindrance of the heparin-thrombin interaction. Thromb Res 1979;15:857-868.
51. 1-acid glycoprotein interacts with plasminogen activator inhibitor type 1 and stabilizes its inhibitory activity. J Biol Chem 2001;276:35305-35311.
52. Sörensson J, Matejka GL, Ohlson M, Haraldsson B. Human endothelial cells produce orosomucoid, an important component of the capillary barrier. Am J Physiol 1999;276:H530-H534. (Pubitemid 29100621)
53. 1-acid glycoprotein in moderately obese male subjects. Br J Clin Pharmacol 1984;18:941-946.
54. Raynaud-Simon A, Lafont S, Berr C, Dartigues JF, Le Bouc Y. Orosomucoid: a mortality risk factor in elderly people living in the community? Clin Nutr 2002;21:45-50.
55. Maachi M, Piéroni L, Bruckert E, Jardel C, Fellahi S, Hainque B, Capeau J, Bastard JP. Systemic low-grade inflammation is related to both circulating and adipose tissue TNFα, leptin and IL-6 levels in obese women. Int J Obes Relat Metab Disord 2004;28:993-997. (Pubitemid 38998704)
56. Christiansen MS, Iversen K, Larsen CT, Goetze JP, Hommel E, Mølvig J, Pedersen BK, Magid E, Feldt-Rasmussen B. Increased urinary orosomucoid excretion: a proposed marker for inflammation and endothelial dysfunction in patients with type 2 diabetes. Scand J Clin Lab Invest 2009;69:272-281.
57. Jiang H, Guan G, Zhang R, Liu G, Liu H, Hou X, Cheng J. Increased urinary excretion of orosomucoid is a risk predictor of diabetic nephropathy. Nephrology (Carlton) 2009;14:332-337.
58. Vassilev A, Yamauchi J, Kotani T, Prives C, Avantaggiati ML, Qin J, Nakatani Y. The 400 kDa subunit of the PCAF histone acetylase complex belongs to the ATM superfamily. Mol Cell 1998;2:869-875. (Pubitemid 128378994)
59. Ginouvès A, Ilc K, Macías N, Pouysségur J, Berra E. PHDs over-activation during chronic hypoxia "desensitizes" HIFα and protects cells from necrosis. Proc Natl Acad Sci USA 2008;105:4745-4750.
60. Chen CF, Chen LW, Chien CT, Wu MS, Tsai TJ. Renal kallikrein in chronic hypoxic rats. Clin Exp Pharmacol Physiol 1996;23:819-824.
61. Thongboonkerd V, Gozal E, Sachleben LR Jr, Arthur JM, Pierce WM, Cai J, Chao J, Bader M, Pesquero JB, Gozal D, et al. Proteomic analysis reveals alterations in the renal kallikrein pathway during hypoxia-induced hypertension. J Biol Chem 2002;277:34708-34716. (Pubitemid 35052359)
62. Amin R, Somers VK, McConnell K, Willging P, Myer C, Sherman M, McPhail G, Morgenthal A, Fenchel M, Bean J, et al. Activity-adjusted 24-hour ambulatory blood pressure and cardiac remodeling in children with sleep disordered breathing. Hypertension 2008;51:84-91. (Pubitemid 350307108)
63. Bell SE, Sanchez MJ, Spasic-Boskovic O, Santalucia T, Gambardella L, Burton GJ, Murphy JJ, Norton JD, Clark AR, Turner M. The RNA binding protein Zfp36l1 is required for normal vascularisation and post-transcriptionally regulates VEGF expression. Dev Dyn 2006;235:3144-3155. (Pubitemid 44749704)
64. Kwon HS, Shin HC, Kim JS. Suppression of vascular endothelial growth factor expression at the transcriptional and post-transcriptional levels. Nucleic Acids Res 2005;33:e74.
65. Gozal D, Lipton AJ, Jones KL. Circulating vascular endothelial growth factor levels in patients with obstructive sleep apnea. Sleep 2002;25:59-65. (Pubitemid 34072660)
66. Lavie L, Kraiczi H, Hefetz A, Ghandour H, Perelman A, Hedner J, Lavie P. Plasma vascular endothelial growth factor in sleep apnea syndrome: effects of nasal continuous positive air pressure treatment. Am J Respir Crit Care Med 2002;165:1624-1628. (Pubitemid 34693942)