Urinary collagen peptides: Source of markers for bone metabolic processes in kidney transplant recipients.
CTX
bone remodeling
collagen peptides
hydroxyproline
kidney
mass spectrometry
peptidome
proteases
transplantation
urine
Journal
Proteomics. Clinical applications
ISSN: 1862-8354
Titre abrégé: Proteomics Clin Appl
Pays: Germany
ID NLM: 101298608
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
revised:
21
04
2023
received:
28
12
2022
accepted:
06
06
2023
medline:
27
7
2023
pubmed:
27
6
2023
entrez:
27
6
2023
Statut:
ppublish
Résumé
Kidney transplant recipients (KTRs) are at an increased risk of fractures. Total urinary hydroxyproline excretion served as marker for bone resorption (BR) but was replaced by β-CrossLaps (CTX), a C-terminal collagen α-1(I) chain (COL1A1) telopeptide. We investigated the low-molecular-weight urinary proteome for peptides associated with changes in bone metabolism after kidney transplantation. Clinical and laboratory data including serum levels of CTX in 96 KTR from two nephrology centers were correlated with signal intensities of urinary peptides identified by capillary electrophoresis mass spectrometry. Eighty-two urinary peptides were significantly correlated with serum CTX levels. COL1A1 was the predominant peptide source. Oral bisphosphonates were administered for decreased bone density in an independent group of 11 KTR and their effect was evaluated on the aforementioned peptides. Study of the peptides cleavage sites revealed a signature of Cathepsin K and MMP9. Seventeen of these peptides were significantly associated with bisphosphonate treatment, all showing a marked reduction in their excretion levels compared to baseline. This study provides strong evidence for the presence of collagen peptides in the urine of KTR that are associated with BR and that are sensitive to bisphosphonate treatment. Their assessment might become a valuable tool to monitor bone status in KTR.
Identifiants
pubmed: 37365945
doi: 10.1002/prca.202200118
doi:
Substances chimiques
Collagen Type I
0
Biomarkers
0
Collagen
9007-34-5
Peptides
0
Diphosphonates
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2200118Informations de copyright
© 2023 The Authors. Proteomics - Clinical Applications published by Wiley-VCH GmbH.
Références
Weisinger, J. [C A A] R., Carlini, R. [C A A] L. G., Rojas, E., & Bellorin-Font, E. (2006). Bone disease after renal transplantation. Clinical Journal of the American Society of Nephrology, 1(6), 1300-1313. https://doi.org/10.2215/CJN.01510506
Sukumaran Nair, S., Lenihan, C. R., Montez-Rath, M. E., Lowenberg, D. W., Chertow, G. M., & Winkelmayer, W. C. (2014). Temporal trends in the incidence, treatment and outcomes of hip fracture after first kidney transplantation in the United States. American Journal of Transplantation, 14(4), 943-951. https://doi.org/10.1111/ajt.12652
Malluche, H. H., Monier-Faugere, M.-C., & Herberth, J. (2010). Bone disease after renal transplantation. Nature Reviews Nephrology, 6(1), 32-40. https://doi.org/10.1038/nrneph.2009.192
Nikkel, L. E., Hollenbeak, C. S., Fox, E. J., Uemura, T., & Ghahramani, N. (2009). Risk of fractures after renal transplantation in the United States. Transplantation, 87(12), 1846-1851. https://doi.org/10.1097/TP.0b013e3181a6bbda
Julian, B. A., Laskow, D. A., Dubovsky, J., Dubovsky, E. V., Curtis, J. J., & Quarles, L. D. (1991). Rapid loss of vertebral mineral density after renal transplantation. The New England Journal of Medicine, 325(8), 544-550. https://doi.org/10.1056/NEJM199108223250804
Kovvuru, K., Kanduri, S. R., Vaitla, P., Marathi, R., Gosi, S., Garcia Anton, D. F. G., Cabeza Rivera, F. H. C., & Garla, V. (2020). Risk factors and management of osteoporosis post-transplant. Medicina (Kaunas, Lithuania), 56(6), 302. https://doi.org/10.3390/medicina56060302
Bouquegneau, A., Salam, S., Delanaye, P., Eastell, R., & Khwaja, A. (2016). Bone disease after kidney transplantation. Clinical Journal of the American Society of Nephrology, 11(7), 1282-1296. https://doi.org/10.2215/CJN.11371015
Liu, Y., & Stein, E. M. (2020). Transplantation osteoporosis. Osteoporosis: Pathophysiology and clinical management, 419-448).
Vervloet, M. G., Brandenburg, V. M., & CKD-MBD working group of ERA-EDTA. (2017). Circulating markers of bone turnover. Journal of Nephrology, 30(5), 663-670. https://doi.org/10.1007/s40620-017-0408-8
Bourrillon, R., & Vernay, J. L. (1966). Deux glycopeptides a hydroxyproline dans l'urine humaine normale]. Biochimica et Biophysica Acta, 117(2), 319-330. https://doi.org/10.1016/0304-4165(66)90083-3
Krane, S. M., Muñoz, A. J., & Harris, E. D. (1967). Collagen-like fragments: Excretion in urine of patients with Paget's disease of bone. Science, 157(3789), 713-716. https://doi.org/10.1126/science.157.3789.713
Haddad, R. G., Couranz, S., & Aviolp, L. V. (1970). Nondialyzable urinary hydroxyproline as an index of bone collagen formation. The Journal of Clinical Endocrinology and Metabolism, 30(3), 282-287. https://doi.org/10.1210/jcem-30-3-282
Krane, S. M., Muñoz, A. J., & Harris, E. D. (1970). Urinary polypeptides related to collagen synthesis. Journal of Clinical Investigation, 49(4), 716-729. https://doi.org/10.1172/JCI106284
Smith, R., Russell, R. G., Bishop, M. C., Woods, C. G., & Bishop, M. (1973). Paget's disease of bone. Experience with a diphosphonate (disodium etidronate) in treatment. The Quarterly Journal of Medicine, 42(166), 235-256.
Szymanowicz, A., Malgras, A., Cosson, R., Randoux, A., & Borel, J. P. (1975). A column chromatography fractionation of the hydroxyproline-containing urinary peptides with continuous automatic detection. Annales de Biologie Clinique, 33(5), 351-358.
Manzke, E., Rawley, R., Vose, G., Roginsky, M., Rader, J. I., & Baylink, D. J. (1977). Effect of fluoride therapy on nondialyzable urinary hydroxyproline, serum alkaline phosphatase, parathyroid hormone, and 25-hydroxyvitamin D. Metabolism, 26(9), 1005-1010. https://doi.org/10.1016/0026-0495(77)90018-x
Niell, H. B., Neely, C. L., & Palmieri, G. M. (1981). The postabsorptive urinary hydroxyproline (spot-HYPRO) in patients with multiple myeloma. Cancer, 48(3), 783-787. https://doi.org/10.1002/1097-0142(19810801)48:3<783::aid-cncr2820480321>3.0.co;2-h
Minisola, S., Antonelli, R., Scarpiello, A., Medori, C., Valtorta, C., & Mazzuoli, G. (1984). Effects of age on the urinary excretion of total and non-dialyzable hydroxyproline. Ric Clinical Laboratory, 14(4), 649-655. https://doi.org/10.1007/BF02906305
Kivirikko, K. I. (1970). International review of connective tissue research. (pp. 93-163). Elsevier. https://doi.org/10.1016/B978-0-12-363705-5.50008-7
Adachi, J., Kumar, C., Zhang, Y., Olsen, J. V., & Mann, M. (2006). The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins. Genome Biology, R80, , 7(9), R80. https://doi.org/10.1186/gb-2006-7-9-R80
Zhao, M., Li, M., Yang, Y., Guo, Z., Sun, Y., Shao, C., Li, M., Sun, W., & Gao, Y. (2017). A comprehensive analysis and annotation of human normal urinary proteome. Scientific Reports, 7(1), 3024. https://doi.org/10.1038/s41598-017-03226-6
Di Meo, A., Batruch, I., Yousef, A. G., Pasic, M. D., Diamandis, E. P., & Yousef, G. M. (2017). An integrated proteomic and peptidomic assessment of the normal human urinome. Clinical Chemistry and Laboratory Medicine, 55(2), 237-247. https://doi.org/10.1515/cclm-2016-0390
Good, D. M., Zürbig, P., Argilés, A., Bauer, H. W., Behrens, G., Coon, J. J., Dakna, M., Decramer, S., Delles, C., Dominiczak, A. F., Ehrich, J. H., Eitner, F., Fliser, D., Frommberger, M., Ganser, A., Girolami, M. A., Golovko, I., Gwinner, W., Haubitz, M., … Schmitt-Kopplin, P. (2010). Naturally occurring human urinary peptides for use in diagnosis of chronic kidney disease. Molecular and Cellular Proteomics, 9(11), 2424-2437. https://doi.org/10.1074/mcp.M110.001917
Kentsis, A., Monigatti, F., Dorff, K., Campagne, F., Bachur, R., & Steen, H. (2009). Urine proteomics for profiling of human disease using high accuracy mass spectrometry. Proteomics - Clinical Applications, 3(9), 1052-1061. https://doi.org/10.1002/prca.200900008
Maahs, D. M., Siwy, J., Argilés, À., Cerna, M., Delles, C., Dominiczak, A. F., Gayrard, N., Iphöfer, A., Jänsch, L., Jerums, G., Medek, K., Mischak, H., Navis, G. J., Roob, J. M., Rossing, K., Rossing, P., Rychlík, I., Schiffer, E., Schmieder, R. E., … Snell-Bergeon, J. K. (2010). Urinary collagen fragments are significantly altered in diabetes: a link to pathophysiology. PLoS One, 5(9), e13051. https://doi.org/10.1371/journal.pone.0013051
Magalhães, P., Pontillo, C., Pejchinovski, M., Siwy, J., Krochmal, M., Makridakis, M., Carrick, E., Klein, J., Mullen, W., Jankowski, J., Vlahou, A., Mischak, H., Schanstra, J. P., Zürbig, P., & Pape, L. (2018). Comparison of urine and plasma peptidome indicates selectivity in renal peptide handling. Proteomics - Clinical Applications, 12(5), 1700163. https://doi.org/10.1002/prca.201700163
Mosteller, R. D. (1987). Simplified calculation of body-surface area. The New England Journal of Medicine, 317(17), 1098. https://doi.org/10.1056/NEJM198710223171717
Levey, A. S. (1999). A more accurate method to estimate glomerular filtration rate from serum creatinine: A new prediction equation. Annals of International Medicine, 130(6), 461-470. https://doi.org/10.7326/0003-4819-130-6-199903160-00002
Wittke, S., Fliser, D., Haubitz, M., Bartel, S., Krebs, R., Hausadel, F., Hillmann, M., Golovko, I., Koester, P., Haller, H., Kaiser, T., Mischak, H., & Weissinger, E. M. (2003). Determination of peptides and proteins in human urine with capillary electrophoresis-mass spectrometry, a suitable tool for the establishment of new diagnostic markers. Journal of Chromatography A, 1013(1-2), 173-181. https://doi.org/10.1016/s0021-9673(03)00713-1
Jantos-Siwy, J., Schiffer, E., Brand, K., Schumann, G., Rossing, K., Delles, C., Mischak, H., & Metzger, J. (2009). Quantitative urinary proteome analysis for biomarker evaluation in chronic kidney disease. Journal of Proteome Research, 8(1), 268-281. https://doi.org/10.1021/pr800401m
Tofte, N., Lindhardt, M., Adamova, K., Bakker, S. J. L., Beige, J., Beulens, J. W. J., Birkenfeld, A. L., Currie, G., Delles, C., Dimos, I., Francová, L., Frimodt-Møller, M., Girman, P., Göke, R., Havrdova, T., Heerspink, H. J. L., Kooy, A., Laverman, G. D., Mischak, H., … Kilic, C., Early detection of diabetic kidney disease by urinary proteomics and subsequent intervention with spironolactone to delay progression (PRIORITY): A prospective observational study and embedded randomised placebo-controlled trial (2020). Early detection of diabetic kidney disease by urinary proteomics and subsequent intervention with spironolactone to delay progression (PRIORITY): a prospective observational study and embedded randomised placebo-controlled trial. Lancet Diabetes Endocrinol, 8(4), 301-312. https://doi.org/10.1016/S2213-8587(20)30026-7
Weissinger, E. M., Metzger, J., Schleuning, M., Schmid, C., Messinger, D., Beutel, G., Wagner-Drouet, E.-M., Schetelig, J., Baurmann, H., Rank, A., Stolzl, F., Schäfer-Eckart, K., Westphal, K., Bethge, W., Von Harsdorf, S., Bunjes, D. W., Heidenreich, D., Klein, S., Holler, E., … Ganser, A. (2021). A multicenter prospective, randomized, placebo-controlled phase II/III trial for preemptive acute graft-versus-host disease therapy. Leukemia, 35(6), 1763-1772. https://doi.org/10.1038/s41375-020-01059-3
Staessen, J. A., Wendt, R., Yu, Y. L., Kalbitz, S., Thijs, L., Siwy, J., Raad, J., Metzger, J., Neuhaus, B., Papkalla, A., von der Leyen, H., Mebazaa, A., Dudoignon, E., Spasovski, G., Milenkova, M., Canevska-Taneska, A., Salgueira Lazo, M., Psichogiou, M., Rajzer, M. W., Fuławka, Ł., … CRIT-CoV-U investigators. (2022). Predictive performance and clinical application of COV50, a urinary proteomic biomarker in early COVID-19 infection: A prospective multicentre cohort study. The Lancet Digital Health, 4(10), e727-e737. https://doi.org/10.1016/S2589-7500(22)00150-9
Piedrafita, A., Siwy, J., Klein, J., Akkari, A., Amaya-Garrido, A., Mebazaa, A., Sanz, A. B., Breuil, B., Montero Herrero, L., Marcheix, B., Depret, F., Fernandez, L., Tardif, E., Minville, V., Alves, M., Metzger, J., Grunenwald, E., Feuillet, G., Buléon, M., … Faguer, S. (2022). A universal predictive and mechanistic urinary peptide signature in acute kidney injury. Critical Care, 26(1), 344. https://doi.org/10.1186/s13054-022-04193-9
Klein, J., Papadopoulos, T., Mischak, H., & Mullen, W. (2014). Comparison of CE-MS/MS and LC-MS/MS sequencing demonstrates significant complementarity in natural peptide identification in human urine. Electrophoresis, 35(7), 1060-1064. https://doi.org/10.1002/elps.201300327
Klein, J., Eales, J., Zürbig, P., Vlahou, A., Mischak, H., & Stevens, R. (2013). Proteasix: A tool for automated and large-scale prediction of proteases involved in naturally occurring peptide generation. Proteomics, 13(7), 1077-1082. https://doi.org/10.1002/pmic.201200493
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of Royal Statistical Society: Series B Statistical Methodology, 57(1), 289-300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Gleiss, A., Dakna, M., Mischak, H., & Heinze, G. (2015). Two-group comparisons of zero-inflated intensity values: the choice of test statistic matters. Bioinformatics, 31(14), 2310-2317. https://doi.org/10.1093/bioinformatics/btv154
Ho, D. E., Imai, K., King, G., & Stuart, E. A. (2011). MatchIt: Nonparametric preprocessing for parametric causal inference. Journal of Statistical Software, 42(8), 1-28. https://doi.org/10.18637/jss.v042.i08
Zhang, Z.-Y., Nkuipou-Kenfack, E., Yang, W.-Y., Wei, F.-F., Cauwenberghs, N., Thijs, L., Huang, Q.-F., Feng, Y.-M., Schanstra, J. P., Kuznetsova, T., Voigt, J.-U., Verhamme, P., Mischak, H., & Staessen, J. A. (2018). Epidemiologic observations guiding clinical application of a urinary peptidomic marker of diastolic left ventricular dysfunction. Journal of the American Society of Hypertension, 12(6), 438-447. e4.e4. https://doi.org/10.1016/j.jash.2018.03.007
Pontillo, C., Jacobs, L., Staessen, J. A., Schanstra, J. P., Rossing, P., Heerspink, H. J. L., Siwy, J., Mullen, W., Vlahou, A., Mischak, H., Vanholder, R., Zürbig, P., & Jankowski, J. (2017). A urinary proteome-based classifier for the early detection of decline in glomerular filtration. Nephrology Dialysis Transplantation, 32(9), 1510-1516. https://doi.org/10.1093/ndt/gfw239
Zhang, Z.-Y., Ravassa, S., Nkuipou-Kenfack, E., Yang, W.-Y., Kerr, S. M., Koeck, T., Campbell, A., Kuznetsova, T., Mischak, H., Padmanabhan, S., Dominiczak, A. F., Delles, C., & Staessen, J. A. (2017). Novel urinary peptidomic classifier predicts incident heart failure. Journal of the American Heart Association, 6(8), e005432. https://doi.org/10.1161/JAHA.116.005432
Metzger, J., Kirsch, T., Schiffer, E., Ulger, P., Mentes, E., Brand, K., Weissinger, E. M., Haubitz, M., Mischak, H., & Herget-Rosenthal, S. (2010). Urinary excretion of twenty peptides forms an early and accurate diagnostic pattern of acute kidney injury. Kidney International, 78(12), 1252-1262. https://doi.org/10.1038/ki.2010.322
Metzger, J., Negm, A. A., Plentz, R. R., Weismüller, T. J., Wedemeyer, J., Karlsen, T. H., Dakna, M., Mullen, W., Mischak, H., Manns, M. P., & Lankisch, T. O. (2013). Urine proteomic analysis differentiates cholangiocarcinoma from primary sclerosing cholangitis and other benign biliary disorders. Gut, 62(1), 122-130. https://doi.org/10.1136/gutjnl-2012-302047
Frantzi, M., Metzger, J., Banks, R. E., Husi, H., Klein, J., Dakna, M., Mullen, W., Cartledge, J. J., Schanstra, J. P., Brand, K., Kuczyk, M. A., Mischak, H., Vlahou, A., Theodorescu, D., & Merseburger, A. S. (2014). Discovery and validation of urinary biomarkers for detection of renal cell carcinoma. Journal of Proteomics, 98, 44-58. https://doi.org/10.1016/j.jprot.2013.12.010
Parker, B. L., Burchfield, J. G., Clayton, D., Geddes, T. A., Payne, R. J., Kiens, B., Wojtaszewski, J. F. P., Richter, E. A., & James, D. E. (2017). Multiplexed temporal quantification of the exercise-regulated plasma peptidome. Molecular and Cellular Proteomics, 16(12), 2055-2068. https://doi.org/10.1074/mcp.RA117.000020
Malluche, H. H., Monier-Faugere, M.-C., & Herberth, J. (2010). Bone disease after renal transplantation. Nature Reviews Nephrolology, 6(1), 32-40. https://doi.org/10.1038/nrneph.2009.192
Palmer, S. C., Chung, E. Y., & Mcgregor, D. O., Bachmann, F., Strippoli, G. F. (2019). Interventions for preventing bone disease in kidney transplant recipients. Cochrane Database of Systematic Reviews, 10(10), CD005015. https://doi.org/10.1002/14651858.CD005015.pub4
Weisinger, J. [C A A] R., Carlini, R [C A A]L. G., Rojas, E., & Bellorin-Font, E. (2006). Bone disease after renal transplantation. Clinical Journal of the American Society of Nephrology, 1(6), 1300-1313. https://doi.org/10.2215/CJN.01510506
Molnar, M. Z., Naser, M. S., Rhee, C. M., Kalantar-Zadeh, K., & Bunnapradist, S. (2014). Bone and mineral disorders after kidney transplantation: therapeutic strategies. Transplant Reviews, 28(2), 56-62. https://doi.org/10.1016/j.trre.2013.12.003
Vautour, L. M., Melton, L. J., Clarke, B. L., Achenbach, S. J., Oberg, A. L., & Mccarthy, J. T. (2004). Long-term fracture risk following renal transplantation: A population-based study. Osteoporosis International, 15(2), 160-167. https://doi.org/10.1007/s00198-003-1532-y
Evenepoel, P., Behets, G. J., Viaene, L., & D'haese, P. C. (2017). Bone histomorphometry in de novo renal transplant recipients indicates a further decline in bone resorption 1 year posttransplantation. Kidney International, 91(2), 469-476. https://doi.org/10.1016/j.kint.2016.10.008
Perrin, P., Kiener, C., Javier, R.-M., Braun, L., Cognard, N., Gautier-Vargas, G., Heibel, F., Muller, C., Olagne, J., Moulin, B., & Ohlmann, S. (2017). Recent changes in chronic kidney disease-mineral and bone disorders and associated fractures after kidney transplantation. Transplantation, 101(8), 1897-1905. https://doi.org/10.1097/TP.0000000000001449
Meunier, P. J., Roux, C., Seeman, E., Ortolani, S., Badurski, J. E., Spector, T. D., Cannata, J., Balogh, A., Lemmel, E.-M., Pors-Nielsen, S., Rizzoli, R., Genant, H. K., & Reginster, J.-Y. (2004). The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis. The New England Journal of Medicine, 350(5), 459-468. https://doi.org/10.1056/NEJMoa022436
Cummings, S. R., Martin, J. S., Mcclung, M. R., Siris, E. S., Eastell, R., Reid, I. R., Delmas, P., Zoog, H. B., Austin, M., Wang, A., Kutilek, S., Adami, S., Zanchetta, J., Libanati, C., Siddhanti, S., & Christiansen, C. (2009). Denosumab for prevention of fractures in postmenopausal women with osteoporosis. The New England Journal of Medicine, 361(8), 756-765. https://doi.org/10.1056/NEJMoa0809493
Brown, J. P., Prince, R. L., Deal, C., Recker, R. R., Kiel, D. P., De Gregorio, L. H., Hadji, P., Hofbauer, L. C., Álvaro-Gracia, J. M., Wang, H., Austin, M., Wagman, R. B., Newmark, R., Libanati, C., San Martin, J., & Bone, H. G. (2009). Comparison of the effect of denosumab and alendronate on bmd and biochemical markers of bone turnover in postmenopausal women with low bone mass: A randomized, blinded, phase 3 trial*, blinded, phase 3 trial. Journal of Bone and Mineral Research, 24(1), 153-161. https://doi.org/10.1359/jbmr.0809010
Delmas, P. D., Recker, R. R., Chesnut, C. H., Skag, A., Stakkestad, J. A., Emkey, R., Gilbride, J., Schimmer, R. C., & Christiansen, C. (2004). Daily and intermittent oral ibandronate normalize bone turnover and provide significant reduction in vertebral fracture risk: Results from the BONE study. Osteoporosis International, 15(10), 792-798. https://doi.org/10.1007/s00198-004-1602-9
Fedarko, N. S. (2013). Osteoblast/osteoclast development and function in OI. In JR Shapiro, PH Byers, FH Glorieux, PD Sponseller (Eds.), Osteogenesis Imperfecta: A Translational Approach to Brittle Bone Disease (pp. 45-56). Elsevier Press.
Swaminathan, R. (2001). Biochemical markers of bone turnover. Clinica Chimica Acta, 313(1-2), 95-105. https://doi.org/10.1016/s0009-8981(01)00656-8
Pagani, F., Francucci, C. M., & Moro, L. (2005). Markers of bone turnover: Biochemical and clinical perspectives. Journal of Endocrinological Investigation, 28(Suppl 10), 8-13.
Garnero, P., Sornay-Rendu, E., Chapuy, M.-C., & Delmas, P. D. (1996). Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis. Journal of Bone and Mineral Research, 11(3), 337-349. https://doi.org/10.1002/jbmr.5650110307
Jia, S., Gong, H., Zhang, Y., Liu, H., Cen, H., Zhang, R., & Fan, Y. (2022). Prediction of femoral strength based on bone density and biochemical markers in elderly men with type 2 diabetes mellitus. Frontiers in Bioengineering and Biotechnology, 10, 855364. https://doi.org/10.3389/fbioe.2022.855364
Sarkissian, A., Sivaraman, V., Bout-Tabaku, S., Ardoin, S. P., Moore-Clingenpeel, M., Mruk, V., Steigelman, H., Morris, K., & Bowden, S. A. (2019). Bone turnover markers in relation to vitamin D status and disease activity in adults with systemic lupus erythematosus. Lupus, 28(2), 156-162. https://doi.org/10.1177/0961203318815593
Khairallah, P., & Nickolas, T. L. (2022). Bone and mineral disease in kidney transplant recipients. Clinical Journal of the American Society of Nephrology, 17(1), 121-130. https://doi.org/10.2215/CJN.03410321
Maehata, Y., Takamizawa, S., Ozawa, S., Izukuri, K., Kato, Y., Sato, S., Lee, M.-C.-Il, Kimura, A., & Hata, R.-I. (2007). Type III collagen is essential for growth acceleration of human osteoblastic cells by ascorbic acid 2-phosphate, a long-acting vitamin C derivative. Matrix Biology, 26(5), 371-381. https://doi.org/10.1016/j.matbio.2007.01.005
Wan, L., Zou, W., Gao, D., Inuzuka, H., Fukushima, H., Berg, A. H., Drapp, R., Shaik, S., Hu, D., Lester, C., Eguren, M., Malumbres, M., Glimcher, L. H., & Wei, W. (2011). Cdh1 regulates osteoblast function through an APC/C-independent modulation of Smurf1. Molecular Cell, 44(5), 721-733. https://doi.org/10.1016/j.molcel.2011.09.024
Akbar, M. A., Nardo, D., Chen, M.-J., Elshikha, A. S., Ahamed, R., Elsayed, E. M., Bigot, C., Holliday, L. S., & Song, S. (2017). α-1 Antitrypsin Inhibits RANKL-induced osteoclast formation and functions. Molecular Medicine, 23, 57-69. https://doi.org/10.2119/molmed.2016.00170
Chellaiah, M., Kizer, N., Silva, M., Alvarez, U., Kwiatkowski, D., & Hruska, K. A. (2000). Gelsolin deficiency blocks podosome assembly and produces increased bone mass and strength. Journal of Cell Biology, 148(4), 665-678. https://doi.org/10.1083/jcb.148.4.665
Larson, S. R., Zhang, X., Dumpit, R., Coleman, I., Lakely, B., Roudier, M., Higano, C. S., True, L. D., Lange, P. H., Montgomery, B., Corey, E., Nelson, P. S., Vessella, R. L., & Morrissey, C. (2013). Characterization of osteoblastic and osteolytic proteins in prostate cancer bone metastases. Prostate, 73(9), 932-940. https://doi.org/10.1002/pros.22639
Vizovisek, M., Vidmar, R., Van Quickelberghe, E., Impens, F., Andjelkovic, U., Sobotic, B., Stoka, V., Gevaert, K., Turk, B., & Fonovic, M. (2015). Fast profiling of protease specificity reveals similar substrate specificities for cathepsins K, L and S K, L and S. Proteomics, 15(14), 2479-2490. https://doi.org/10.1002/pmic.201400460
Dodds, R. A., James, I. E., Rieman, D., Ahern, R., Hwang, S. M., Connor, J. R., Thompson, S. D., Veber, D. F., Drake, F. H., Holmes, S., Lark, M. W., & Gowen, M. (2001). Human osteoclast cathepsin K is processed intracellularly prior to attachment and bone resorption. Journal of Bone and Mineral Research, 16(3), 478-486. https://doi.org/10.1359/jbmr.2001.16.3.478
Henriksen, K., Sørensen, M. G., Nielsen, R. H., Gram, J., Schaller, S., Dziegiel, M. H., Everts, V., Bollerslev, J., & Karsdal, M. A. (2006). Degradation of the organic phase of bone by osteoclasts: a secondary role for lysosomal acidification. Journal of Bone and Mineral Research, 21(1), 58-66. https://doi.org/10.1359/JBMR.050905
Binkley, N., Orwoll, E., Chapurlat, R., Langdahl, B. L., Scott, B. B., Giezek, H., & Santora, A. C. (2021). Randomized, controlled trial to assess the safety and efficacy of odanacatib in the treatment of men with osteoporosis. Osteoporosis International, 32(1), 173-184. https://doi.org/10.1007/s00198-020-05701-9
Colnot, C. L, Thompson, Z., Miclau, T., Werb, Z., & Helms, J. A. (2003). Altered fracture repair in the absence of MMP9. Development, 130(17), 4123-4133. https://doi.org/10.1242/dev.00559
Zhu, L., Tang, Y., Li, X.-Y., Keller, E. T., Yang, J., Cho, J.-S., Feinberg, T. Y., & Weiss, S. J. (2020). Osteoclast-mediated bone resorption is controlled by a compensatory network of secreted and membrane-tethered metalloproteinases. Science Translational Medicine, 12(529), eaaw6143. https://doi.org/10.1126/scitranslmed.aaw6143
Li, B., Ling Chau, J. F., Wang, X., & Leong, W. F. (2011). Bisphosphonates, specific inhibitors of osteoclast function and a class of drugs for osteoporosis therapy. Journal of Cellular Biochemistry, 112(5), 1229-1242. https://doi.org/10.1002/jcb.23049
Russell, R. G. G., Preston, C., Smith, R., Walton, R. J., & Woods, C. G. (1974). Diphosphonates in paget's disease. Lancet, 1(7863), 894-898. https://doi.org/10.1016/s0140-6736(74)90347-x
Mischak, H., Kolch, W., Aivaliotis, M., Bouyssié, D., Court, M., Dihazi, H., Dihazi, G. H., Franke, J., Garin, J., De Peredo, A. G., Iphöfer, A., Jänsch, L., Lacroix, C., Makridakis, M., Masselon, C., Metzger, J., Monsarrat, B., Mrug, M., Norling, M., … Vlahou, A. (2010). Comprehensive human urine standards for comparability and standardization in clinical proteome analysis. Proteomics Clinical Applications, 4(4), 464-478. https://doi.org/10.1002/prca.200900189
Ahmed, F. E. (2009). Sample preparation and fractionation for proteome analysis and cancer biomarker discovery by mass spectrometry. Journal of Separation Scinece, 32(5-6), 771-798. https://doi.org/10.1002/jssc.200800622
Rosen, H. N., Moses, A. C., Garber, J., Iloputaife, I. D., Ross, D. S., Lee, S. L., & Greenspan, S. L. (2000). Serum CTX: A new marker of bone resorption that shows treatment effect more often than other markers because of low coefficient of variability and large changes with bisphosphonate therapy. Calcified Tissue International, 66(2), 100-103. https://doi.org/10.1007/pl00005830
Avioli, L. V., & Prockop, D. J. (1967). Collagen Degradation and the response to parathyroid extract in the intact rhesus monkey*. Journal of Clinical Investigation, 46(2), 217-224. https://doi.org/10.1172/JCI105524
Weiss, P. H., & Klein, L. (1969). The quantitative relationship of urinary peptide hydroxyproline excretion to collagen degradation. Journal of Clinical Investigation, 48(1), 1-10. https://doi.org/10.1172/JCI105957
Prockop, D. J. (1964). Isotopic studies on collagen degradation and the urine excretion of hydroxyproline *. Journal of Clinical Investigation, 43(3), 453-460. https://doi.org/10.1172/JCI104930
Schanstra, J. P., Zürbig, P., Alkhalaf, A., Argiles, A., Bakker, S. J. L., Beige, J., Bilo, H. J. G., Chatzikyrkou, C., Dakna, M., Dawson, J., Delles, C., Haller, H., Haubitz, M., Husi, H., Jankowski, J., Jerums, G., Kleefstra, N., Kuznetsova, T., Maahs, D. M., … Vanholder, R. (2015). Diagnosis and prediction of CKD progression by assessment of urinary peptides. Journal of the American Society of Nephrology, 26(8), 1999-2010. https://doi.org/10.1681/ASN.2014050423