Top

Published in:

Open Access 01-05-2017 | ORTHOPAEDIC HERITAGE"

Marshall R. Urist and the discovery of bone morphogenetic proteins

Authors: Lovorka Grgurevic, Marko Pecina, Slobodan Vukicevic

Published in: International Orthopaedics | Issue 5/2017

Abstract

Over the last 40 years International Orthopaedics has published a series of articles on bone morphogenetic proteins (BMPs) covering topics from basic research to clinical applications. This includes also work submitted from the Laboratory for Mineralized Tissues of the School of Medicine University of Zagreb. Accordingly, we felt obliged to give a short summary of Dr. Urist’s life and work as our gratitude to his discovery that demineralized bone matrix (DBM) activity induces bone when implanted ectopically into the muscle or under the skin due to bone inducing proteins, named BMPs.

Andriopoulos B Jr, Corradini E, Xia Y, Faasse SA, Chen S, Grgurevic L, Knutson MD, Pietrangelo A, Vukicevic S, Lin HY, Babitt JL (2009) BMP-6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nat Genet 41:482–487. doi:10.1038/ng.335 CrossRefPubMedPubMedCentral

Bauer H, Nilsson O (2001) Marshall Raymond Urist: 1914–2001. Acta Orthop Scand 72:318–319. doi:10.1080/00016470152846691 CrossRef

Bilic R, Simic P, Jelic M, Stern-Padovan R, Dodig D, Pompe H, Martinovic S, Ivankovic D, Pecina M, Vukicevic S (2006) Osteogenic protein-1 (BMP-7) accelerates healing of scaphoid non-union with proximal pole sclerosis. Int Orthop 30:128–134. doi:10.1007/s00264-005-0045-z CrossRefPubMedPubMedCentral

Brand RA (2009) Marshall R. Urist, 1914–2001. Clin Orthop 467:3049–6050. doi:10.1007/s11999-009-1067-4 CrossRefPubMedPubMedCentral

Buza JA III, Einhorn T (2016) Bone healing in 2016. Clin Cases Min Bone Metab 13:101–105. doi:10.11138/ccmbm/2016.13.2.101

Courvoisier A, Sailhan F, Laffenêtre O, Obert L, French Study Group of BMP in Orthopedic Surgery (2014) Bone morphogenetic protein and orthopaedic surgery: can we legitimate its off-label use? Int Orthop 38:2601–2605. doi:10.1007/s00264-014-2534-4 CrossRefPubMed

Das SP, Ganesh S, Pradhan S, Singh D, Mohanty RN (2014) Effectiveness of recombinant human bone morphogenetic protein-7 in the management of congenital pseudoarthrosis of the tibia: a randomised controlled trial. Int Orthop 38:1987–1992. doi:10.1007/s00264-014-2361-7 CrossRefPubMed

Dumic-Cule I, Brkljacic J, Rogic D, Bordukalo Niksic T, Tikvica Luetic A, Draca N, Kufner V, Trkulja V, Grgurevic L, Vukicevic S (2014) Systemically available bone morphogenetic protein two and seven affect bone metabolism. Int Orthop 38:1979–1985. doi:10.1007/s00264-014-2425-8 CrossRefPubMed

Dumic-Cule I, Pecina M, Jelic M, Jankolija M, Popek I, Grgurevic L, Vukicevic S (2015) Biological aspects of segmental bone defects management. Int Orthop 39:1005–1011. doi:10.1007/s00264-015-2728-4 CrossRefPubMed

10.

Fassbender M, Minkwitz S, Thiele M, Wildemann B (2014) Efficacy of two different demineralised bone matrix grafts to promote bone healing in a critical-size-defect: a radiological, histological and histomorphometric study in rat femurs. Int Orthop 38:1963–1969. doi:10.1007/s00264-014-2321-2 CrossRefPubMed

11.

Flouzat-Lachaniette CH, Ghazanfari A, Bouthors C, Poignard A, Hernigou P, Allain J (2014) Bone union rate with recombinant human bone morphogenic protein-2 versus autologous iliac bone in PEEK cages for anterior lumbar interbody fusion. Int Orthop 38:2001–2007. doi:10.1007/s00264-014-2301-6 CrossRefPubMed

12.

Fu R, Selph S, McDonagh M, Peterson K, Tiwari A, Chou R, Helfand M (2013) Effectiveness and harms of recombinant human bone morphogenetic protein-2 in spine fusion: a systematic review and meta-analysis. Ann Intern Med 158:890–902. doi:10.7326/0003-4819-158-12-201306180-00006 CrossRefPubMed

13.

Hinsenkamp M, Collard JF (2015) Growth factors in orthopaedic surgery: demineralized bone matrix versus recombinant bone morphogenetic proteins. Int Orthop 39:137–147. doi:10.1007/s00264-014-2562-0 CrossRefPubMed

14.

Huggins C (1967) Endocrine-induced regression of cancers. Science 156:1050–1054CrossRefPubMed

15.

Huggins C (1967) Endocrine-induced regression of cancers. Cancer Res 27:1925–1930PubMed

16.

Johnson EE, Urist MR, Finerman GA (1988) Bone morphogenetic protein augmentation grafting of resistant femoral nonunions: a preliminary report. Clin Orthop 230:257–265

17.

Kaipel M, Schützenberger S, Hofmann AT, Ferguson J, Nau T, Redl H, Feichtinger GA (2014) Evaluation of fibrin-based gene-activated matrices for BMP2/7 plasmid codelivery in a rat nonunion model. Int Orthop 38:2607–2613. doi:10.1007/s00264-014-2499-3 CrossRefPubMed

18.

Keith B, Vitasek K, Manrodt K, Kling K (2016) Strategic sourcing in the new economy. Palgrave Macmillan US

19.

Pauk M, Grgurevic L, Brkljacic J, Kufner V, Bordukalo-Niksic T, Grabusic K, Razdorov G, Rogic D, Zuvic M, Oppermann H, Babitt JL, Lin HY, Volarevic S, Vukicevic S (2015) Exogenous BMP7 corrects plasma iron overload and bone loss in Bmp6−/− mice. Int Orthop 39:161–172. doi:10.1007/s00264-014-2550-4 CrossRefPubMed

20.

Pecina M, Giltaj LR, Vukicevic S (2001) Orthopaedic applications of osteogenic protein-1 (BMP-7). Int Orthop 25:203–208. doi:10.1007/s002640100262 CrossRefPubMedPubMedCentral

21.

Pecina M, Haspl M, Jelic M, Vukicevic S (2003) Repair of a resistant tibial non-union with a recombinant BMP-7. Int Orthop 27:320–321. doi:10.1007/s00264-003-0475-4 CrossRefPubMedPubMedCentral

22.

Pecina M, Jelic M, Martinovic S, Haspl M, Vukicevic S (2002) Articular cartilage repair: the role of bone morphogenetic proteins. Int Orthop 26:131–136. doi:10.1007/s00264-002-0338-4 CrossRefPubMedPubMedCentral

23.

Reddi AH (2003) Marshall R. Urist: a renaissance scientist and orthopaedic surgeon. J Bone Joint Surg Am 85:3CrossRefPubMed

24.

Schwarting T, Benölken M, Ruchholtz S, Frink M, Lechler P (2015) Bone morphogenetic protein-7 enhances bone-tendon integration in a murine in vitro co-culture model. Int Orthop 39:799–805. doi:10.1007/s00264-015-2688-8 CrossRefPubMed

25.

Simmonds MC, Brown JV, Heirs MK, Higgins JP, Mannion RJ, Rodgers MA, Stewart LA (2013) Safety and effectiveness of recombinant human bone morphogenetic protein-2 for spinal fusion: a meta-analysis of individual-participant data. Ann Intern Med 158:877–889CrossRefPubMed

26.

Song K, Krause C, Shi S, Patterson M, Sutto R, Grgurevic L, Vukicevic S, van Dinther M, Falb D, ten Dijke P, Alaoui-Ismaili MH (2010) Identification of a key residue mediating bone morphogenetic protein (BMP)-6 resistance to noggin inhibition allows for engineered BMPs with superior-agonist activity. J Biol Chem 285:12169–12180. doi:10.1074/jbc.M109.087197 CrossRefPubMedPubMedCentral

27.

Takigami J, Hashimoto Y, Yamasaki S, Terai S, Nakamura H (2015) Direct bone-to-bone integration between recombinant human bone morphogenetic protein-2-injected tendon graft and tunnel wall in an anterior cruciate ligament reconstruction model. Int Orthop 39:1441–1447. doi:10.1007/s00264-015-2774-y CrossRefPubMed

28.

Tsuji K, Bandyopadhyay A, Harfe BD, Cox K, Kakar S, Gerstenfeld L, Einhorn T, Tabin CJ, Rosen V (2006) BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat Genet 38:1424–1429CrossRefPubMed

29.

Urist MR (1965) Bone: formation by autoinduction. Science 150:893–899CrossRefPubMed

30.

Urist MR, Strates BS (1971) Bone morphogenetic protein. J Dent Res 50:1392–1404CrossRefPubMed

31.

von Rüden C, Morgenstern M, Friederichs J, Augat P, Hackl S, Woltmann A, Bühren V, Hierholzer C (2016) Comparative study suggests that human bone morphogenetic proteins have no influence on the outcome of operative treatment of aseptic clavicle non-unions. Int Orthop 40:2339–2345. doi:10.1007/s00264-016-3262-8 CrossRef

32.

Vukicevic S, Grgurevic L (2009) BMP-6 and mesenchymal stem cell differentiation. Cytokine Growth Factor Rev 20:441–448. doi:10.1016/j.cytogfr.2009.10.020 CrossRefPubMed

33.

Vukicevic S, Oppermann H, Verbanac D, Jankolija M, Popek I, Curak J, Brkljacic J, Pauk M, Erjavec I, Francetic I, Dumic-Cule I, Jelic M, Durdevic D, Vlahovic T, Novak R, Kufner V, Bordukalo Niksic T, Kozlovic M, Banic Tomisic Z, Bubic-Spoljar J, Bastalic I, Vikic-Topic S, Peric M, Pecina M, Grgurevic L (2014) The clinical use of bone morphogenetic proteins revisited: a novel biocompatible carrier device OSTEOGROW for bone healing. Int Orthop 38:635–647. doi:10.1007/s00264-013-2201-1 CrossRefPubMed

34.

Vukicevic S, Sampath TK (eds) (2002) Bone morphogenetic proteins: from laboratory to clinical practice. Birkhäuser Verlag, Basel

35.

Vukicevic S, Sampath KT (eds) (2004) Bone morphogenetic proteins: regeneration of bone and beyond. Birkhäuser Verlag, Basel

36.

Vukicevic S, Sampath TK (eds) (2008) Bone morphogenetic proteins: from local to systemic therapeutics. Birkhäuser Verlag, Basel

37.

Vukicevic S, Sampath KT (eds) (2017) Bone morphogenetic proteins: systems biology regulators. Springer International Publishing AG. doi:10.1007/978-3-319-47507-3

38.

Vukicevic S, Stavljenic A, Pecina M (1995) Discovery and clinical applications of bone morphogenetic proteins. Eur J Clin Chem Clin Biochem 33(10):661–671PubMed

39.

Vukicevic S, Marusic A, Stavljenic A, Vinter I, Rudez V (1989) New bone formation in the autologous membranous bone transplanted into anterior abdominal wall. Plast Reconstr Surg 83:889–891CrossRefPubMed

40.

Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA (1988) Novel regulators of bone formation: molecular clones and activities. Science 242:1528–1534CrossRefPubMed

Title: Marshall R. Urist and the discovery of bone morphogenetic proteins
Authors: Lovorka Grgurevic
Marko Pecina
Slobodan Vukicevic
Publication date: 01-05-2017
Publisher: Springer Berlin Heidelberg
Published in: International Orthopaedics / Issue 5/2017
Print ISSN: 0341-2695
Electronic ISSN: 1432-5195
DOI: https://doi.org/10.1007/s00264-017-3402-9

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Marshall R. Urist and the discovery of bone morphogenetic proteins

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2017

Correlations between serum adipocytokine concentrations, disease stage, radiological status and total body fat content in the patients with primary knee osteoarthritis

The variability of vertebral body volume and pain associated with osteoporotic vertebral fractures: conservative treatment versus percutaneous transpedicular vertebroplasty

Comparison of two- and three-dimensional measurement of the Cobb angle in scoliosis

Transcutaneous carbon dioxide application accelerates muscle injury repair in rat models

Are advanced three-dimensional imaging studies always needed to measure the coronal knee alignment of the lower extremity?

Description and reproducibility assessment of a new computerised tomography scan index to measure the glenoid orientation in relation to the anterior glenoid surface