Topographical variation in the distributions of versican, aggrecan and perlecan in the foetal human spine reflects their diverse functional roles in spinal development

Histochemistry and Cell Biology

Volumn 132, Issue 5, 2009, Pages 491-503

  Smith, Susan M ^a   Whitelock, John M ^b   Iozzo, Renato V ^c   Little, Christopher B ^a   Melrose, James ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Aggrecan; Foetal human spine; Perlecan; Versican

Indexed keywords

AGGRECAN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; GAG PROTEIN; PERLECAN; VERSICAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; INTERVERTEBRAL DISK; NUCLEUS PULPOSUS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPINE; VERTEBRA BODY;

AGGRECANS; COLLAGEN TYPE I; COLLAGEN TYPE II; FETUS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; IMMUNOHISTOCHEMISTRY; SPINE; VERSICANS;

EID: 72849120533     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-009-0623-z     Document Type: Article

References (75)

1. Y Abiko M Nishimura F Rahemtulla I Mizoguchi T Kaku 2001 Immunohistochemical localisation of large chondroitin sulphate proteoglycan in porcine gingival epithelia Eur J Morphol 39 99 104 10.1076/ejom.39.2.99.7372 1:STN:280:DC%2BD38%2Flt1aktQ%3D%3D 11778745 (Pubitemid 32881434)
2. E Arikawa-Hirasawa H Watanabe H Takami JR Hassell Y Yamada 1999 Perlecan is essential for cartilage and cephalic development Nat Genet 23 354 358 10.1038/15537 1:CAS:528:DyaK1MXnt1GnsL4%3D 10545953 (Pubitemid 29526437)
3. E Arikawa-Hirasawa WR Wilcox AH Le N Silverman P Govindraj JR Hassell Y Yamada 2001 Dyssegmental dysplasia, Silverman-Handmaker type, is caused by functional null mutations of the perlecan gene Nat Genet 27 431 434 10.1038/86941 1:CAS:528:DC%2BD3MXjtFShsLs%3D 11279527 (Pubitemid 32268426)
4. E Arikawa-Hirasawa WR Wilcox Y Yamada 2001 Dyssegmental dysplasia, Silverman-Handmaker type: unexpected role of perlecan in cartilage development Am J Med Genet 106 254 257 10.1002/ajmg.10229 1:STN:280:DC%2BD387lvVSisw%3D%3D 11891676
5. E Arikawa-Hirasawa AH Le I Nishino I Nonaka NC Ho CA Francomano P Govindraj JR Hassell JM Devaney J Spranger RE Stevenson S Iannaccone MC Dalakas Y Yamada 2002 Structural and functional mutations of the perlecan gene cause Schwartz-Jampel syndrome, with myotonic myopathy and chondrodysplasia Am J Hum Genet 70 1368 1375 10.1086/340390 1:CAS:528:DC%2BD38XjsFGnsb8%3D 11941538 (Pubitemid 34450588)
6. RA Asher G Perides J-J Vanderhaeghen A Bignani 1991 Extracellular matrix of central nervous system white matter: demonstration of an hyaluronate-protein complex J Neurosci Res 28 410 421 10.1002/jnr.490280314 1:CAS:528: DyaK3MXitVChsLY%3D 1713274
7. RA Asher RJ Schiebe HD Keiser A Bignami 1995 On the existence of a cartilage like proteoglycan and link protein in the central nervous system Glia 13 294 308 10.1002/glia.440130406 1:STN:280:DyaK2MzktVakug%3D%3D 7615338
8. A Aspberg S Adam G Kostka R Timpl D Heinegard 1999 Fibulin-1 is a ligand for the C-type lectin domains of aggrecan and versican J Biol Chem 274 20444 20449 10.1074/jbc.274.29.20444 1:CAS:528:DyaK1MXks1Ojtro%3D 10400671 (Pubitemid 29340403)
9. G Bix RV Iozzo 2008 Novel interactions of perlecan: unravelling perlecan's role in angiogenesis Microsc Res Technol 71 339 348 10.1002/jemt.20562 1:CAS:528:DC%2BD1cXmvVSntLk%3D (Pubitemid 351620856)
10. JA Buckwalter RR Cooper JA Maynard 1976 Elastic fibers in human intervertebral discs J Bone Joint Surg Am 58 73 76 1:STN:280: DyaE287itVKmtg%3D%3D 1249115
11. JA Buckwalter A Pedrini-Mille V Pedrini C Tudisco 1985 Proteoglycans of human infant intervertebral disc. Electron microscopic and biochemical studies J Bone Joint Surg Am 67 284 294 1:STN:280:DyaL2M7gsFWgsw%3D%3D 3968121
12. JA Buckwalter PJ Roughley LC Rosenberg 1994 Age-related changes in cartilage proteoglycans: quantitative electron microscopic studies Microsc Res Technol 28 398 408 10.1002/jemt.1070280506 1:CAS:528:DyaK2MXhtVWku7Y%3D (Pubitemid 24222671)
13. RE Burgeson DW Hollister 1979 Collagen heterogeneity in human cartilage: identification of several new collagen chains Biochem Biophys Res Commun 87 1124 1131 10.1016/S0006-291X(79)80024-8 1:CAS:528:DyaE1MXktFGntLc%3D 465027 (Pubitemid 9163383)
14. D Chen M Zhao SE Harris Z Mi 2004 Signal transduction and biological functions of bone morphogenetic proteins Front Biosci 9 349 358 10.2741/1090 1:CAS:528:DC%2BD2cXhtFCku7k%3D 14766372
15. D Chen M Zhao GR Mundy 2004 Bone morphogenetic proteins Growth Factors 22 233 241 10.1080/08977190412331279890 1:CAS:528:DC%2BD2MXhtFWrsQ%3D%3D 15621726 (Pubitemid 40136452)
16. JR Couchman AV Ljubimov 1989 Mammalian tissue distribution of a large heparan sulfate proteoglycan detected by monoclonal antibodies Matrix 9 311 321 1:CAS:528:DyaL1MXlslWms7s%3D 2477673
17. CP DiPaola JC Farmer K Manova LA Niswander 2005 Molecular signaling in intervertebral disk development J Orthop Res 23 1112 1119 10.1016/j.orthres. 2005.03.008 1:CAS:528:DC%2BD2MXpslygsLk%3D 15936916 (Pubitemid 41245436)
18. Drury RAB, Wallington EA (1967) Carleton's histological technique, 5th edn. Oxford University Press, Oxford, pp 151-190
19. DR Eyre 1979 Biochemistry of the intervertebral disc Int Rev Connect Tissue Res 8 227 291 1:CAS:528:DyaE1MXlvFSlu74%3D 389859
20. DR Eyre H Muir 1976 Types I and II collagens in intervertebral disc. Interchanging radial distributions in annulus fibrosus Biochem J 157 267 270 1:CAS:528:DyaE28Xlt1Sht78%3D 962859
21. DR Eyre H Muir 1977 Quantitative analysis of types I and II collagens in human intervertebral discs at various ages Biochim Biophys Acta 492 29 42 1:CAS:528:DyaE2sXktVeisLs%3D 577186
22. W Gotz G Fischer R Herken 1991 Lectin binding pattern in the embryonal and early fetal human vertebral column Anat Embryol (Berl) 184 345 353 10.1007/BF00957896 1:STN:280:DyaK38%2FlvF2lsg%3D%3D
23. HE Gruber J Ingram K Leslie EN Hanley Jr 2008 Gene expression of types I, II, and VI collagen, aggrecan, and chondroitin-6-sulfotransferase in the human annulus: in situ hybridization findings Spine J 8 810 817 10.1016/j.spinee.2007. 07.387 18024225
24. E Gustafsson A Aszodi N Ortega EB Hunziker HW Denker Z Werb R Fassler 2003 Role of collagen type II and perlecan in skeletal development Ann N Y Acad Sci 995 140 150 10.1111/j.1749-6632.2003.tb03217.x 1:CAS:528: DC%2BD3sXlsVensrc%3D 12814946
25. M Handler PD Yurchenco RV Iozzo 1997 Developmental expression of perlecan during murine embryogenesis Dev Dyn 210 130 145 10.1002/(SICI)1097-0177(199710) 210:2<130::AID-AJA6>3.0.CO;2-H 1:CAS:528:DyaK2sXnt1Gmsrg%3D 9337134 (Pubitemid 27424258)
26. H Hashizume 1980 Three-dimensional architecture and development of lumber intervertebral discs Acta Med Okayama 34 301 314 1:STN:280: DyaL3M%2FlvFWgsg%3D%3D 6449129
27. AJ Hayes M Benjamin JR Ralphs 2001 Extracellular matrix in development of the intervertebral disc Matrix Biol 20 107 121 10.1016/S0945-053X(01)00125-1 1:CAS:528:DC%2BD3MXktVajsr4%3D 11334712 (Pubitemid 32396761)
28. DS Hickey DW Hukins 1980 X-ray diffraction studies of the arrangement of collagenous fibres in human fetal intervertebral disc J Anat 131 81 90 1:STN:280:DyaL3M%2FmvFGgtg%3D%3D 7440405
29. DS Hickey DW Hukins 1981 Collagen fibril diameters and elastic fibres in the annulus fibrosus of human fetal intervertebral disc J Anat 133 351 357 1:STN:280:DyaL387hvFymsw%3D%3D 7328042
30. Y Horiguchi JR Couchman AV Ljubimov H Yamasaki JD Fine 1989 Distribution, ultrastructural localization, and ontogeny of the core protein of a heparan sulfate proteoglycan in human skin and other basement membranes J Histochem Cytochem 37 961 970 1:CAS:528:DyaL1MXksFCktrg%3D 2659664
31. N Horii-Hayashi H Okuda K Tatsumi S Ishizaka M Yoshikawa A Wanaka 2008 Localization of chondroitin sulfate proteoglycan versican in adult brain with special reference to large projection neurons Cell Tissue Res 334 163 177 10.1007/s00441-008-0698-1 1:CAS:528:DC%2BD1cXhtlCjsrjN 18936977
32. MZ Ilic P Carter A Tyndall J Dudhia CJ Handley 2005 Proteoglycans and catabolic products of proteoglycans present in ligament Biochem J 385 381 388 10.1042/BJ20040844 1:CAS:528:DC%2BD2MXhvVCnsQ%3D%3D 15329049 (Pubitemid 40165070)
33. RV Iozzo 1994 Perlecan: a gem of a proteoglycan Matrix Biol 14 203 208 10.1016/0945-053X(94)90183-X 1:CAS:528:DyaK2cXlt1Oqsrk%3D 7921536 (Pubitemid 24136379)
34. RV Iozzo 1998 Matrix proteoglycans: from molecular design to cellular function Annu Rev Biochem 67 609 652 10.1146/annurev.biochem.67.1.609 1:CAS:528:DyaK1cXlsFOmsbo%3D 9759499 (Pubitemid 28411140)
35. RV Iozzo 2005 Basement membrane proteoglycans: from cellar to ceiling Nat Rev Mol Cell Biol 6 646 656 10.1038/nrm1702 1:CAS:528:DC%2BD2MXmvVGht74%3D 16064139 (Pubitemid 41081268)
36. RV Iozzo IR Cohen S Grassel AD Murdoch 1994 The biology of perlecan: the multifaceted heparan sulphate proteoglycan of basement membranes and pericellular matrices Biochem J 302 Pt 3 625 639 1:CAS:528:DyaK2cXlvFyqsLo%3D 7945186
37. Z Isogai A Aspberg DR Keene RN Ono DP Reinhardt LY Sakai 2002 Versican interacts with fibrillin-1 and links extracellular microfibrils to other connective tissue networks J Biol Chem 277 4565 4572 10.1074/jbc.M110583200 1:CAS:528:DC%2BD38XhsFSqt7g%3D 11726670 (Pubitemid 34968726)
38. NS Kalson S Richardson JA Hoyland 2008 Strategies for regeneration of the intervertebral disc Regen Med 3 717 729 10.2217/17460751.3.5.717 1:STN:280:DC%2BD1crks1aqsQ%3D%3D 18729796
39. RG Lebaron 1996 Versican Perspect Dev Neurobiol 3 261 271 1:CAS:528:DyaK2sXisFWgtg%3D%3D 9117259
40. AV Ljubimov J Bartek JR Couchman LL Kapuller VV Veselov J Kovarik AG Perevoshchikov VA Krutovskikh 1992 Distribution of individual components of basement membrane in human colon polyps and adenocarcinomas as revealed by monoclonal antibodies Int J Cancer 50 562 566 10.1002/ijc.2910500412 1:STN:280:DyaK387msFCiuw%3D%3D 1371500
41. RU Margolis RK Margolis 1994 Aggrecan-versican-neurocan family proteoglycans Methods Enzymol 245 105 126 10.1016/0076-6879(94)45008-0 1:CAS:528:DyaK2MXmsV2iu7Y%3D 7539091
42. R Mayne JG Zettergren PM Mayne NW Bedwell 1980 Isolation and partial characterization of basement membrane-like collagens from bovine thoracic aorta Artery 7 262 280 1:CAS:528:DyaL3MXotV2gtA%3D%3D 7213017
43. M Mazzucato MR Cozzi P Pradella D Perissinotto A Malmstrom M Morgelin P Spessotto A Colombatti L De Marco R Perris 2002 Vascular PG-M/versican variants promote platelet adhesion at low shear rates and cooperate with collagens to induce aggregation FASEB J 16 1903 1916 10.1096/fj.02-0382com 1:CAS:528:DC%2BD38Xps1Ojur0%3D 12468455 (Pubitemid 35469145)
44. J Melrose S Smith S Knox J Whitelock 2002 Perlecan, the multidomain HS-proteoglycan of basement membranes, is a prominent pericellular component of ovine hypertrophic vertebral growth plate and cartilaginous endplate chondrocytes Histochem Cell Biol 118 269 280 1:CAS:528:DC%2BD38Xnslaqurg%3D 12376823
45. J Melrose S Smith P Ghosh J Whitelock 2003 Perlecan, the multidomain heparan sulfate proteoglycan of basement membranes, is also a prominent component of the cartilaginous primordia in the developing human fetal spine J Histochem Cytochem 51 1331 1341 1:CAS:528:DC%2BD3sXnvFGrtbo%3D 14500701
46. J Melrose S Smith J Whitelock 2004 Perlecan immunolocalises to perichondral vessels and canals in human foetal cartilagenous promordia in early vascular and matrix remodelling events associated with diarthrodial-joint development J Histochem Cytochem 52 1405 1413 10.1369/jhc.4A6261.2004 1:CAS:528:DC%2BD2cXhtVWgs7nJ 15505335 (Pubitemid 39518676)
47. J Melrose S Smith M Cake R Read J Whitelock 2005 Perlecan displays variable spatial and temporal immunolocalisation patterns in the articular and growth plate cartilages of the ovine stifle joint Histochem Cell Biol 123 561 571 10.1007/s00418-005-0789-y 1:CAS:528:DC%2BD2MXmt1Wgu7k%3D 16021525 (Pubitemid 41126075)
48. J Melrose S Smith M Cake R Read J Whitelock 2005 Spatial and temporal immunolocalisation of perlecan in the ovine meniscus Histochem Cell Biol 124 225 235 10.1007/s00418-005-0005-0 1:CAS:528:DC%2BD2MXhtFanu73N 16028067 (Pubitemid 41624207)
49. J Melrose AJ Hayes JM Whitelock CB Little 2008 Perlecan, the "jack of all trades" proteoglycan of cartilaginous weight-bearing connective tissues Bioessays 30 457 469 10.1002/bies.20748 1:CAS:528:DC%2BD1cXmvVSgtbg%3D 18404701 (Pubitemid 351588927)
50. J Melrose SM Smith CB Little RJ Moore B Vernon-Roberts RD Fraser 2008 Recent advances in annular pathobiology provide insights into rim-lesion mediated intervertebral disc degeneration and potential new approaches to annular repair strategies Eur Spine J 17 1131 1148 10.1007/s00586-008-0712-z 18584218
51. J Melrose SM Smith MM Smith CB Little 2008 The use of Histochoice for histological examination of articular and growth plate cartilages, intervertebral disc and meniscus Biotechnol Histochem 83 47 53 10.1080/10520290801990414 1:CAS:528:DC%2BD1cXmsVWgs7k%3D (Pubitemid 351863904)
52. T Murakami E Wakamatsu N Tamahashi T Takahashi 1985 The functional significance of human notochord in the development of vertebral column. An electron microscopic study Tohoku J Exp Med 146 321 336 10.1620/tjem.146.321 1:STN:280:DyaL28%2FhvFOruw%3D%3D 4049373
53. AD Murdoch B Liu R Schwarting RS Tuan RV Iozzo 1994 Widespread expression of perlecan proteoglycan in basement membranes and extracellular matrices of human tissues as detected by a novel monoclonal antibody against domain III and by in situ hybridization J Histochem Cytochem 42 239 249 1:CAS:528: DyaK2cXhtlSgurY%3D 7507142
54. AG Nerlich N Boos I Wiest M Aebi 1998 Immunolocalization of major interstitial collagen types in human lumbar intervertebral discs of various ages Virchows Arch 432 67 76 10.1007/s004280050136 1:CAS:528:DyaK1cXjtlSmtw%3D%3D 9463590 (Pubitemid 28065841)
55. AI Olin M Morgelin T Sasaki R Timpl D Heinegard A Aspberg 2001 The proteoglycans aggrecan and Versican form networks with fibulin-2 through their lectin domain binding J Biol Chem 276 1253 1261 10.1074/jbc.M006783200 1:CAS:528:DC%2BD3MXmtVyqsQ%3D%3D 11038354 (Pubitemid 32096553)
56. M Rahmani BW Wong L Ang CC Cheung JM Carthy H Walinski BM McManus 2006 Versican: signaling to transcriptional control pathways Can J Physiol Pharmacol 84 77 92 10.1139/y05-154 1:CAS:528:DC%2BD28XktlCqsrw%3D 16845893 (Pubitemid 44011953)
57. SM Richardson A Mobasheri AJ Freemont JA Hoyland 2007 Intervertebral disc biology, degeneration and novel tissue engineering and regenerative medicine therapies Histol Histopathol 22 1033 1041 1:STN:280:DC%2BD2szhtFSrtg%3D%3D 17523081
58. T Samiric MZ Ilic CJ Handley 2004 Characterisation of proteoglycans and their catabolic products in tendon and explant cultures of tendon Matrix Biol 23 127 140 10.1016/j.matbio.2004.03.004 1:CAS:528:DC%2BD2cXlsFyrurg%3D 15246111 (Pubitemid 38891526)
59. JB Shepard HA Krug BA LaFoon S Hoffman AA Capehart 2007 Versican expression during synovial joint morphogenesis Int J Biol Sci 3 380 384 1:CAS:528:DC%2BD2sXhtVOmsrvK 17848983
60. JB Shepard DA Gliga AP Morrow S Hoffman AA Capehart 2008 Versican knock-down compromises chondrogenesis in the embryonic chick limb Anat Rec (Hoboken) 291 19 27
61. HP Sorensen RR Vives C Manetopoulos R Albrechtsen MC Lydolph J Jacobsen JR Couchman UM Wewer 2008 Heparan sulfate regulates ADAM12 through a molecular switch mechanism J Biol Chem 283 31920 31932 10.1074/jbc.M804113200 1:CAS:528:DC%2BD1cXhtlCjsbjE 18801731
62. R Sztrolovics J Grover G Cs-Szabo SL Shi Y Zhang JS Mort PJ Roughley 2002 The characterization of versican and its message in human articular cartilage and intervertebral disc J Orthop Res 20 257 266 10.1016/S0736-0266(01)00110-3 11918305 (Pubitemid 34218269)
63. N Toriya T Takuma T Arakawa Y Abiko Y Sasano I Takahashi Y Sakakura F Rahemtulla I Mizoguchi 2006 Expression and localisation of versican during postnatal development of rat temporomandibular joint disc J Histochem Cell Biol 125 205 214 10.1007/s00418-005-0020-1 1:CAS:528:DC%2BD28Xhtlehtb8%3D (Pubitemid 43228194)
64. H Tsuji N Hirano H Ohshima H Ishihara N Terahata T Motoe 1993 Structural variation of the anterior and posterior anulus fibrosus in the development of human lumbar intervertebral disc. A risk factor for intervertebral disc rupture Spine 18 204 210 10.1097/00007632-199302000-00006 1:STN:280:DyaK3s7otFOlsQ%3D%3D 8441935
65. J Von Kossa 1901 Uber die in Organismus kunstlich erzeugbaren Verkalkungen Beitr Pathol Anat Allg Pathol 29 163 202
66. H Watanabe Y Yamada 2002 Chondrodysplasia of gene knockout mice for aggrecan and link protein Glycoconj J 19 269 273 10.1023/A:1025344332099 1:CAS:528:DC%2BD3sXmsFWit7s%3D 12975605 (Pubitemid 37174555)
67. JM Whitelock LD Graham J Melrose AD Murdoch RV Iozzo PA Underwood 1999 Human perlecan immunopurified from different endothelial cell sources has different adhesive properties for vascular cells Matrix Biol 18 163 178 10.1016/S0945-053X(99)00014-1 1:CAS:528:DyaK1MXjsVOrs7o%3D 10372557 (Pubitemid 29229702)
68. JM Whitelock J Melrose RV Iozzo 2008 Diverse cell signaling events modulated by perlecan Biochemistry 47 11174 11183 10.1021/bi8013938 1:CAS:528:DC%2BD1cXhtFygtLjK 18826258
69. TN Wight 2002 Versican: a versatile extracellular matrix proteoglycan in cell biology Curr Opin Cell Biol 14 617 623 10.1016/S0955-0674(02)00375-7 1:CAS:528:DC%2BD38XmvVCrtbk%3D 12231358 (Pubitemid 35247746)
70. DR Williams Jr AR Presar AT Richmond CH Mjaatvedt S Hoffman AA Capehart 2005 Limb chondrogenesis is compromised in the versican deficient hdf mouse Biochem Biophys Res Commun 334 960 966 10.1016/j.bbrc.2005.06.189 1:CAS:528:DC%2BD2MXmvFSju7Y%3D 16039617 (Pubitemid 41033213)
71. YJ Wu DP La Pierre J Wu AJ Yee BB Yang 2005 The interaction of versican with its binding partners Cell Res 15 483 494 10.1038/sj.cr.7290318 1:CAS:528:DC%2BD2MXhtFWnsbzJ 16045811 (Pubitemid 41653919)
72. BL Yang Y Zhang L Cao BB Yang 1999 Cell adhesion and proliferation mediated through the G1 domain of versican J Cell Biochem 72 210 220 10.1002/(SICI)1097-4644(19990201)72:2<210::AID-JCB5>3.0.CO;2-E 1:CAS:528:DyaK1MXjt1OqtQ%3D%3D 10022503 (Pubitemid 29021934)
73. BL Yang BB Yang M Erwin LC Ang J Finkelstein AJ Yee 2003 Versican G3 domain enhances cellular adhesion and proliferation of bovine intervertebral disc cells cultured in vitro Life Sci 73 3399 3413 10.1016/j.lfs.2003.06.018 1:CAS:528:DC%2BD3sXot12ju7w%3D 14572881 (Pubitemid 37311380)
74. Y Zhang HS An C Tannoury EJ Thonar MK Freedman DG Anderson 2008 Biological treatment for degenerative disc disease: implications for the field of physical medicine and rehabilitation Am J Phys Med Rehabil 87 694 702 10.1097/PHM.0b013e31817c1945 18716481
75. Zimmermann DR (2000) Versican. In: Iozzo RV (ed) Proteoglycans-structure. biology and molecular interactions. Marcel Dekker, New York, pp 327-341