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About us Medical Sciences Research Pathology Medical Biology Research Matrix accumulation, tissue repair and inflammation
University Medical Center Groningen


Regenerative medicine: Organ damage and repair

Broekema M, Harmsen MC, Koerts JA, Petersen AH, van Luyn MJ, Navis G, Popa ER. Determinants of tubular bone marrow-derived cell engraftment after renal ischemia/reperfusion in rats. Kidney Int 2005; 68(6):2572-81

Broekema M, Harmsen MC, van Luyn MJ, Koerts JA, Petersen AH, van Kooten TG, van Goor H, Navis G, Popa ER. Bone marrow-derived myofibroblasts contribute to the renal interstitial myofibroblast population and produce procollagen I after ischemia/reperfusion in rats. J Am Soc Nephrol 2007; 18(1):165-75

Broekema M, Harmsen MC, Koerts JA, van Kooten TG, Navis G, van Luyn MJ, Popa ER. Tubular engraftment and myofibroblast differentiation of recipient-derived cells after experimental kidney transplantation. Transplant 2007; 84(8):1003-11

van Amerongen MJ, Bou-Gharios G, Popa ER, van Ark J, Petersen AH, van Dam GM, van Luyn MJ, Harmsen MC. Bone marrow-derived myofibroblasts contribute functionally to scar formation after myocardial infarction. J Pathol 2008; 214(3):377-86

Broekema M, Harmsen MC, Koerts JA, van Kooten TG, Uges DR, Petersen AH, van Luyn MJ, Navis G, Popa ER. Ciclosporin does not influence bone marrow-derived cell differentiation to myofibroblasts early after renal ischemia/reperfusion. Am J Nephrol 2009; 30(1):73-83

Trzpis M, McLaughlin PM, van Goor H, Brinker MG, van Dam GM, de Leij LM, Popa ER, Harmsen MC. Expression of EpCAM is up-regulated during regeneration of renal epithelia. J Pathol 2008; 216(2):201-8

Popa ER, Harmsen MC, Tio RA, van der Strate BW, Brouwer LA, Schipper M, Koerts J, De Jongste MJ, Hazenberg A, Hendriks M, van Luyn MJ. Circulating CD34+ progenitor cells modulate host angiogenesis and inflammation in vivo. J Mol Cell Cardiol 2006; 41(1):86-96

Krenning G, Dankers PY, Drouven JW, Waanders F, Franssen CF, van Luyn MJ, Harmsen MC, Popa ER. Endothelial progenitor cell dysfunction in patients with progressive chronic kidney disease. Am J Physiol Renal Physiol. 2009; 296(6):F1314-22

van der Strate BW, Popa ER, Schipper M, Brouwer LA, Hendriks M, Harmsen MC, van Luyn MJ. Circulating human CD34+ progenitor cells modulate neovascularization and inflammation in a nude mouse model. J Mol Cell Cardiol 2007; 42(6):1086-97

Boersema M, Rienstra H, van den Heuvel M, van Luyn MJA, Navis GJ, Popa ER, Hillebrands JL. Minor recipient contribution to remodeling in chronic renal allograft dysfunction. Transplant 2009; 88:1386-92

Popa ER, Kas-Deelen AM, Hepkema BG, Van Son WJ, The TH, Harmsen MC. Donor-derived circulating endothelial cells after kidney transplantation. Transplant 2002; 74(9):1320-7

Popa ER, van der Strate BW, Brouwer LA, Tadema H, Schipper M, Fernandes B, Hendriks M, van Luyn MJ, Harmsen MC. Dependence of neovascularization mechanismson the molecular microenvironment. Tissue Eng 2007; 13(12):2913-21

Stem cells and tissue engineering

Lu ZF, Zandieh Doulabi B, Wuisman PI, Bank RA, Helder MN. Differentiation of adipose stem cells by nucleus pulposus cells: configuration effect. Biochem Biophys Res Commun 2007 ; 359:991-996

Lu ZF, Zandieh Doulabi B, Wuisman PI, Bank RA, Helder MN. Influence of collagen type II and nucleus pulposus cells on aggregation and differentiation of adipose tissue-derived stem cells. J Cell Mol Med 2008; 12:2812-2822

Hoogendoorn RJ, Lu ZF, Kroeze RJ, Bank RA, Wuisman PI & Helder MN. Adipose stem cells for intervertebral disc regeneration: current status and concepts for the future. J Cell Mol Med 2008; 12: 2205-2016.

Knippenberg M, Helder MN, Zandieh Doulabi B, Bank RA, Wuisman PI & Klein-Nulend J. Differential effects of bone morphogenetic protein-2 and transforming growth factor-beta1 on gene expression of collagen-modifying enzymes in human adipose tissue-derived mesenchymal stem cells. Tissue Eng Part A 2009; 15:2213-2225

Lu ZF, Zandieh Doulabi B, Huang CL, Bank RA, Helder MN. Beta1 integrins regulate chondrogenesis and Rock signaling in adipose stem cells. Biochem Biophys Res Commun 2008, 372:547-552

Lu Z, Doulabi BZ, Huang C, Bank RA, Helder MN. Collagen type II enhances chondrogenesis in adipose tissue-derived stem cells by affecting cell shape. Tissue Eng Part A 2010 ; 16:81-90

Kroeze RJ, Helder MN, Roos WH, Wuite GJ, Bank RA, Smit TH. The effect of ethylene oxide, glow discharge and electron beam on the surface characteristics of poly(L-lactide-co-caprolactone) and the corresponding cellular response of adipose stem cells. Acta Biomater 2010 ; 6:2060-2065

Jurgens WJ, Kroeze RJ, Bank RA, Ritt MJ, Helder MN. Rapid attachment of adipose stromal cells on resorbable polymeric scaffolds facilitates the one-step surgical procedure for cartilage and bone tissue engineering purposes. J Orthop Res 2011; 29:853-860

Fernandes H, Dechering K, Van Someren E, Steeghs I, Apotheker M, Leusink A, Bank R, Janeczek K, Van Blitterswijk C, de Boer J. The role of collagen crosslinking in differentiation of human mesenchymal stem cells and MC3T3-E1 cells. Tissue Eng Part A 2009 ; 15:3857-3867

Fernandes H, Mentink A, Bank R, Stoop R, van Blitterswijk C, de Boer J. Endogenous collagen influences differentiation of human multipotent mesenchymal stromal cells. Tissue Eng Part A 2010 ; 16:1693-1702

Foreign body reaction

van Putten SM, Wübben M, Plantinga JA, Hennink WE, van Luyn MJ, Harmsen MC. Endotoxin contamination delays the foreign body reaction. J Biomed Mater Res A 2011; 98:527-34

van Putten SM, Wübben M, Hennink WE, van Luyn MJ, Harmsen MC. The downmodulation of the foreign body reaction by cytomegalovirus encoded interleukin-10. Biomaterials 2009; 30(5):730-5

Ye Q, Xing Q, Ren Y, Harmsen MC, Bank RA. Endo180 and MT1-MMP are involved in the phagocytosis of collagen scaffolds by macrophages and is regulated by interferon-gamma. Eur Cell Mater 2010; 20:197-209

Ye Q, Harmsen MC, van Luyn MJ, Bank RA. The relationship between collagen scaffold cross-linking agents and neutrophils in the foreign body reaction. Biomaterials 2010 ; 31:9192-9201

Ye Q, van Amerongen MJ, Sandham JA, Bank RA, van Luyn MJ, Harmsen MC. Site-specific tissue inhibitor of metalloproteinase-1 governs the matrix metalloproteinases-dependent degradation of crosslinked collagen scaffolds and is correlated with interleukin-10. J Tissue Eng Regen Med 2011 ; 5:264-274

Ye Q, Harmsen MC, Ren Y, Bank RA. The role of collagen receptors Endo180 and DDR-2 in the foreign body reaction against non-crosslinked collagen and gelatin. Biomaterials 2011; 32:1339-1350

Censi R, van Putten S, Vermonden T, di Martino P, van Nostrum CF, Harmsen MC, Bank RA, Hennink WE. The tissue response to photopolymerized PEG-p(HPMAm-lactate)-based hydrogels. J Biomed Mater Res A 2011; 97:219-229

Collagen in soft tissues

Walker LC, Overstreet MA, Siddiqui A, De Paepe A, Ceylaner G, Malfait F, Symoens S, Atsawasuwan P, Yamauchi M, Ceylander S, Bank RA Yeowell HN. A novel mutation in the lysyl hydroxylase 1 gene causes decreased lysyl hydroxylase activity in an Ehlers-Danlos VIA patient. J Invest Dermatol 2005; 124: 914-918

Pfeiffer BJ, Franklin CL, Hsieh FH, Bank RA, Phillips CL. Alpha 2(I) collagen deficient oim mice have altered biomechanical integrity, collagen content, and collagen crosslinking of their thoracic aorta. Matrix Biol 2005; 24:451-458

Balguid A, Rubbens MP, Mol A, Bank RA, Bogers AJ, van Kats JP, de Mol BA, Baaijens FP, Bouten CV. The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets-relevance for tissue engineering. Tissue Eng 2007; 13:1501-1511

Ponsioen TL, Deemter M, Bank RA, Snabel JM, Zijlstra GS, van der Worp RJ, Hooymans JM, Los LI. Mature enzymatic collagen cross-links, hydroxylysylpyridinoline and lysylpyridinoline, in the aging human vitreous. Invest Ophthalmaol Vis Sci 2009; 50:1041-1046

Rubbens MP, Mol A, Boerboom RA, Bank RA, Baaijens FP & Bouten CV. Intermittent straining accelerates the development of tissue properties in engineered herat valve tissue. Tissue Eng Part A 2008; 15:999-1008

van Deemter M, Ponsioen TL, Bank RA, Snabel JM, van der Worp RJ, Hooymans JM, Los LI. Pentosidine accumulates in the aging vitreous body: a gender effect. Exp Eye Res 2009 , 88:1043-1050

Lindeman JH, Ashcroft BA, Beenakker JW, van Es M, Koekkoek NB, Prins FA, Tielemans JF, Abdul-Hussien H, Bank RA, Oosterkamp TH. Distinct defects in collagen microarchitecture underlie vessel-wall failure in advanced abdominal aneurysms and aneurysms in Marfan syndrome. Proc Natl Acad Sci USA 2010 ; 107:862-865

Hosper NA, Eggink AJ, Roelofs LA, Wijnen RM, van Luyn MJ, Bank RA, Harmsen MC, Geutjes PJ, Daamen WF, van Kuppevelt TH, Tiemessen DM, Oosterwijk E, Crevels JJ, Blokx WA, Lotgering FK, van den Berg PP, Feitz WF. Intra-uterine tissue engineering of full-thickness skin defects in a fetal sheep model. Biomaterials 2010 ; 31:3910-3919

Akins ML, Luby-Phelps K, Bank RA, Mahendroo M. Cervical softening during pregnancy: regulated changes in collagen cross-linking and composition of matricellular proteins in the mouse. Biol Reprod 2011; 84:1053-1062

Modifications of collagen in healthy and diseased musculoskeletal tissues

Bank RA, Verzijl N. Lafeber FPJG, TeKoppele JM. Putative role of lysyl hydroxylase and pyridinoline cross-linking during adolescence in the occurrence of oseoarthritis at old age. Osteoarthr Cartil 2002; 10:127-134

Bank RA, Groener JE, van Gemund JJ, Maaswinkel PD, Hoeben KA, Schut HA & Everts V. Deficiency in N-acetylgalactosamine-6sulfate sulfatase results in collagen perturbations in cartilage of Morquio syndrome A patients. Mol Genet Metab 2009; 97:196-201

Vonk LA, Kroeze RJ, Doulabi BZ, Hoogendoorn RJ, Huang C, Helder MN, Everts V, Bank RA. Caprine articular, meniscus and intervertebral disc cartilage: an integral analysis of collagen network and chondrocytes. Matrix Biol 2010; 29:209-218

Bank RA, TeKoppele JM, Oostingh G, Hazleman BL, Riley GP. Lysyl hydroxylation and non-reducible crosslinking of human supraspinatus tendon collagen: changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis 1999 ; 58:35-41

Bank RA, Robins SP, Wijmenga C, Breslau-Siderius LJ, Bardoel AFJ, van der Sluijs HA, Pruijs HEH, TeKoppele JM. Defective collagen crosslinking in bone, but not in cartilage or ligament, in Bruck syndrome: indications for a bone-specific telopeptide lysyl hydroxylase on chromosome 17. Proc Natl Acad Sci USA 1999 ; 96:1054-1058

Wassen MHM, Lammens J, TeKoppele JM, Sakkers RJB, Liu Z, Verbout AJ, Bank RA. Collagen structure regulates fibril mineralization in osteogenesis as revealed by crosslink patterns in calcifying callus. J Bone Miner Res 2000 ; 15:1776-1785

Bank RA, Sakkers RJB, Janus GJ, Wassen MHM, Pruijs HEH, van der Sluijs HA, TeKoppele JM. Pyridinium crosslinks in bone of patients with osteogenesis imperfecta: evidence for a normal intrafibrillar collagen packing. J Bone Miner Res 2000; 15:1330-1336

Ha-Vinh R, Alanay Y, Bank RA, Campos-Xavier AB, Zankl A, Superti-Furga A, BonafeL. Phenotypic and molecular characterization of Bruck syndrome (osteogenesis imperfecta with contractures of the large joints) caused by a recessive mutation in PLOD2. Am J Med Genet A 2004; 131:115-120

Silva MJ, Brodt MD, Wopenka B, Thomopoulos S, Williams D, Wassen MH, Ko M, Kusano N, Bank RA. Decreased collagen organization and content are associated with reduced strength of demineralized and intact bone in the SAMP6 mouse. J Bone Miner Res 2006; 21:78-88

van den Bos T, Speijer D, Bank RA, Brömme D & Everts V. Differences in matrix composition between calvaria and long bone in mice suggest differences in biomechanical properties and resorption: special emphasis on collagen. Bone 2008; 43:459-468

Vonk LA, Doulabi BZ, Huang CL, Helder MN, Everts V, Bank RA. Endoplasmic reticulum stress inhibits collagen synthesis independent of collagen-modifying enzymes in different chondrocyte populations and dermal fibroblasts. Biochem Cell Biol 2010 ; 88:539-552

Collagen in fibrosis

van der Slot AJ, Zuurmond A-M, Bardoel AF, Wijmenga C… Bank RA. Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem 2003; 278:40967-40972

van der Slot AJ, Zuurmond A-M, van den Bogaerdt AJ, Ulrich MM, Middelkoop E, Boers W, Ronday HK, DeGroot J, Huizinga TW, Bank RA. Increased formation of pyridinoline cross-links due to higher telopeptidyl lysyl hydroxyalse levels is a general fibrotic phenomenon. Matrix Biol 2004; 23:251-257

van der Slot AJ, van Dura EA, de Wit EC, DeGroot J, Huizinga TW, Bank RA, Zuurmond A-M. Elevated formation of pyridinoline cross-links by profibrotic cytokines is associated with enhanced lysyl hydroxylase 2b levels. Biochim. Biophys. Acta 2005; 1741:95-102

Zuurmond A-M, van der Slot AJ , Dura EA, DeGroot J & Bank RA. Minoxidil exerts di fferent inhibitory effects on gene expression of lysyl hydroxylase 1, 2 and 3: implications for collagen cross-linking and treatment of fibrosis. Matrix Biol 2005 ; 24:261-270

A.J. van der Slot, E.A. Dura, J. Attema, B. Blauw, J.DeGroot, T.W. Huizinga, A.-M. Zuurmond & R.A. Bank. The type of collagen cross-link determines the reversibility of experimental skin fibrosis. Biochim Biophys Acta 2005; 1740:60-67

Brinckmann J, Kim S, Wu J, Reinhardt DP, Batmunkh C, Metzen E, Notbohm H, Bank RA, Krieg T, Hunzelmann N. Interleukin 4 and prolonged hypoxia induce a higher gene expression of lysyl hydroxylase 2 and an altered cross-link pattern: important pathogenetic steps in early and late stage of systemic scleroderma? Matrix Biol 2005; 24:459-468

Takaluoma K, Hyry M, Lantto J, Sormunen R, Bank RA, Kivirikko KI, Myllyharju J, Soininen R. Tissue-specific changes in the hydroxylysine content and cross-links of collagens and alterations in fibril morphology in lysyl hydroxylase 1 knock-out mice. J Biol Chem 2007; 282:6588-6596

van den Bogaerdt AJ, van der Veen VC, van Zuijlen PP, Reijnen L, Verkerk M, Bank RA, Middelkoop E, Ulrich MM. Collagen cross-linking by adipose-derived mesenchymal stromal cells and scar-derived mesenchymal cells: Are mesenchymal stromal cells involved in scar formation? Wound Repair Regen 2009 ; 17:548-558

Ageing and degradation of collagen

Bank RA, Bayliss MT, Lafeber FPJG, Maroudas A, TeKoppele JM. Ageing and zonal variation in post-translational modification of collagen in normal human articular cartilage. The age-related increase in non-enzymatic glycation affects biomechanical properties of cartilage. Biochem J 1998; 330:345-351

Bank RA, Soudry M, Maroudas A, Mizrahi J, TeKoppele JM. The increased swelling and instantaneous deformation of osteoarthritic cartilage is highly correlated with collagen degradation. Arthr Rheum 2000; 43:2202-2210

Verzijl N, DeGroot J, Oldehinkel E, Bank RA, Thorpe SR, Baynes JW, Bayliss MT, Bijlsma JW, Lafeber FPJG, TeKoppele JM. Age-related accumulation of Maillard products in human articular cartilage collagen. Biochem J 2000; 350:381-387

Verzijl N, DeGroot J, Thorpe SR, Bank RA, Shaw JN, Lyons TJ, Bijlsma JW, Lafeber FPJG, Baynes JW, TeKoppele JM. Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 2000 ; 275:39027-39031

DeGroot J, Verzijl N, Wenting-Van Wijk MJ, Bank RA, Lafeber FPJG, Bijlsma JW, TeKoppele JM. Age-related decrease in susceptibility of human articular cartilage to matrix metalloproteinase-mediated degradation: the role of advanced glycation end products. Arthr Rheum 2001 ; 44:2562-2571

Verzijl N, DeGroot J, Bank RA, Bayliss MT, Bijlsma JW, Lafeber FPJG, Maroudas A, TeKoppele JM. Age-related accumulation of the advanced glycation endproduct pentosidine in human articular cartilage aggrecan: the use of pentosidine levels as a quantitative measure of protein turnover. Matrix Biol 2001; 20:409-417

Verzijl N, Bank RA, TeKoppele JM, DeGroot J. AGEing and osteoarthritis: a different perspective. Curr Opin Rheumatol 2003; 15:616-622

Vonk LA, Doulabi BZ, Huang C, Helder MN, Everts V, Bank RA. Preservation of the chondrocyte's pericellular matrix improves cell-induced cartilage formation. J Cell Biochem 2010 ; 110:260-271

Vonk LA, Doulabi BZ, Huang C, Helder MN, Everts V, Bank RA. Collagen-induced expression of collagenase-3 by primary chondrocytes is mediated by integrin╬▒1 and discoidin domain receptor 2: a protein kinase C-dependent pathway. Rheumatol 2011; 50:463-472

Riley GP, Curry V, DeGroot J, van El B, Verzijl N, Hazleman BL, BankRA. Matrix metalloproteinase activities and their relationship with collagen remodelling in tendon pathology. Matrix Biol 2002; 21:185-195

Collagen chemistry: methodology

Bank RA, Jansen EJ, Beekman B, TeKoppele JM. Amino acid analysis by reverse-phase high-performance liquid chromatography: improved derivatization and detection conditions with 9-fluorenylmethyl chloroformate. Anal Biochem 1996; 240:167-176

Bank RA, Jansen EJ, Beekman B, TeKoppele JM. Sensitive fluorimetric quantitation of pyridinium and pentosidine crosslinks in biological samples in a single high-performance liquid chromatographic run. J Chromatogr B 1997; 703:37-44

Bank RA, Beekman B, Tenni R, TeKoppele JM. Pre-column derivatization method for the measurement of glycosylated hydroxylysines of collagenous proteins. J Chromatogr B 1997 ; 703:267-272

Bank RA, Krikken M, Beekman B, Stoop R, Maroudas A, Lafeber FPJG, TeKoppele JM. A simplified measurement of degraded collagen in tissues: application in healthy, fibrillated and osteoarthritic cartilage. Matrix Biol 1997; 16:233-243

Basser PJ, Schneiderman R, Bank RA, Wachtel E, Maroudas A. Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique. Arch Biochem Biophys 1998; 351:207-219

Wang X, Bank RA, TeKoppele JM, Hubbard GB, Athanasiou KA, Agrawal CM. Effect of collagen denaturation on the toughness of bone. Clin Orthop Rel Res 2000 ; 371:228-239

Wang X, Li X, Bank RA, Agrawal CM. Effects of collagen unwinding and cleavage on the mechanical integrity of the collagen network in bone. Calcif Tissue Int 2002; 71:186-192

Last modified:16 December 2014 4.22 p.m.