Type III collagen regulates osteoblastogenesis and the quantity of trabecular bone

Calcified Tissue International

Volumn 94, Issue 6, 2014, Pages 621-631

  Volk, Susan W ^a   Shah, Shalin R ^b   Cohen, Arthur J ^b   Wang, Yanjian ^a   Brisson, Becky K ^a   Vogel, Laurie K ^a   Hankenson, Kurt D ^c,d   Adams, Sherrill L ^b  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Bone formation; Extracellular matrix; Mineralization; Osteogenesis; Osteoporosis; Type III collagen

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ALKALINE PHOSPHATASE; COLLAGEN TYPE 3; DNA; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; BONE MASS; BONE MINERALIZATION; BONE STRUCTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; CRANIOFACIAL MORPHOLOGY; EHLERS DANLOS SYNDROME; EMBRYO; FEMUR; GENE EXPRESSION; GENOTYPE; IMAGE RECONSTRUCTION; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSTEOBLAST; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SKELETON; SKULL; THREE DIMENSIONAL IMAGING; TRABECULAR BONE; ANIMAL; CYTOLOGY; FEMALE; METABOLISM; MUTANT MOUSE STRAIN; OSTEOCLAST; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; COLLAGEN TYPE III; FEMALE; MICE; MICE, MUTANT STRAINS; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; X-RAY MICROTOMOGRAPHY;

EID: 84901976648     PISSN: 0171967X     EISSN: 14320827     Source Type: Journal    
DOI: 10.1007/s00223-014-9843-x     Document Type: Article

References (55)

1. Shen H, Recker RR, Deng HW (2003) Molecular and genetic mechanisms of osteoporosis: implications for treatment. Curr Mol Med 3:737-757 (Pubitemid 37536879)
2. Surgeon General (2004) Bone health and osteoporosis: a Report of the Surgeon General. U.S. Department of Health and Human Services, Rockville, MD
3. Burge R, Dawson-Hughes B, Solomon DH, King A, Tosteson A (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J Bone Miner Res 22:465-475 (Pubitemid 46797130)
4. Franceschi RT (1999) The developmental control of osteoblast-specific gene expression: role of specific transcription factors and the extracellular matrix environment. Crit Rev Oral Biol Med 10:40-57
5. Ge C, Yang Q, Zhao G, Yu H, Kirkwood KL, Franceschi RT (2012) Interactions between extracellular signal-regulated kinase 1/2 and p38 MAP kinase pathways in the control of RUNX2 phosphorylation and transcriptional activity. J Bone Miner Res 27:538-551
6. Epstein EH Jr (1974) (Alpha1(3))3 human skin collagen. Release by pepsin digestion and preponderance in fetal life. J Biol Chem 249:3225-3331
7. Smith LT, Holbrook KA, Byers PH (1982) Structure of the dermal matrix during development and in the adult. J Invest Dermatol 79:93s-104s (Pubitemid 12080833)
8. Tolstoshev P, Haber R, Trapnell BC, Crystal RG (1981) Procollagen mRNA levels and activity and collagen synthesis during the fetal development of sheep lung, tendon and skin. J Biol Chem 256:9672-9679 (Pubitemid 12234730)
9. Birk DE, Mayne R (1997) Localization of collagen types I, III, and V during tendon development. Eur J Cell Biol 72:352-361
10. Henkel W, Glanville RW (1982) Covalent crosslinking between molecules of type I and type III collagen. Eur J Biochem 122:205-231
11. Keene DR, Sakai LY, Bachinger HP, Burgeson RE (1987) Type III collagen can be present on banded collagen fibrils regardless of fibril diameter. J Cell Biol 105:2392-2402
12. Keene DR, Sakai LY, Burgeson RE (1991) Human bone contains type III collagen, type VI collagen and fibrillin. J Histochem Cytochem 38:59-69
13. Reddi AH, Gay R, Gay S, Miller EJ (1977) Transition in collagen types during matrix-induced cartilage, bone and bone marrow formation. Proc Natl Acad Sci USA 74:5589-5592
14. Silver MH, Foidart JM, Pratt RM (1981) Distribution of fibronectin and collagen during mouse limb and palate development. Differentiation 18:141-149 (Pubitemid 11083002)
15. Maehata Y, Takamizawa S, Ozawa S, Izukuri K, Kato Y, Sato S, Lee MC, Kimura A, Hara RI (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 Biol 26:371-381 (Pubitemid 46813224)
16. Chen XD, Dusevich V, Feng JQ, Manolagas SC, Jilka R (2007) Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts. J Bone Miner Res 22:1943-1956 (Pubitemid 351229311)
17. De Coster PJ, Martens LC, De Paepe A (2005) Oral health in prevalent types of Ehlers-Danlos syndromes. J Oral Pathol Med 34:298-307 (Pubitemid 40524971)
18. Stanitski DF, Nadjarian R, Stanitski CL, Bawle E, Tsipouras P (2000) Orthopaedic manifestations of Ehlers-Danlos syndrome. Clin Orthop Relat Res 376:213-221 (Pubitemid 30445698)
19. Yen JL, Lin SP, Chen MR, Niu DM (2006) Clinical features of Ehlers-Danlos syndrome. J Formos Med Assoc 105:475-480
20. Liu X, Wu H, Burne M, Krane S, Jaenisch R (1997) Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development. Proc Natl Acad Sci USA 94:1852-1856 (Pubitemid 27113925)
21. Volk SW, Wang Y, Mauldin EA, Liechty KW, Adams SL (2011) Diminished type III collagen promotes myofibroblast differentiation and increases scar deposition in cutaneous wound healing. Cells Tissues Organs 194:25-37
22. Richtsmeier JT, Baxter LL, Reeves RH (2000) Parallels of craniofacial maldevelopment in down syndrome and Ts65Dn mice. Dev Dyn 217:137-145 (Pubitemid 30080493)
23. Garreta E, Genové E, Borrós S, Semino CE (2006) Osteogenic differentiation of mouse embryonic stem cells and mouse embryonic fibroblasts in a three dimensional self-assembling peptide scaffold. Tissue Eng 12:2215-2227 (Pubitemid 44734980)
24. Legner CJ, Lepper C, van Wijnen AJ, Stein JL, Stein GS, Lian JB (2004) Primary mouse embryonic fibroblasts: a model of mesenchymal cartilage formation. J Cell Physiol 200:327-333 (Pubitemid 39006923)
25. Volk SW, Wang Y, Hankenson KD (2012) Effects of donor characteristics and ex vivo expansion on canine mesenchymal stem cell properties: implications for MSC-based therapies. Cell Transplant 21:2189-2200
26. Volk SW, Diefenderfer DL, Christopher SA, Haskins ME, Leboy PS (2005) Effects of osteogenic inducers on cultures of canine mesenchymal stem cells. Am J Vet Res 66:1729-1737 (Pubitemid 41644822)
27. Spinella-Jaegle S, Roman-Roman S, Faucheu C, Dunn FW, Kawai S, Galléa S, Stiot V, Blanchet AM, Courtois B, Baron R, Rawadi G (2001) Opposite effects of bone morphogenetic protein-2 and transforming growth factor-[beta]1 on osteoblast differentiation. Bone 29:323-330 (Pubitemid 32930058)
28. Benatti BB, Silverio KG, Casati MZ, Sallum EA, Nociti FH Jr (2008) Influence of aging on biological properties of periodontal ligament cells. Connect Tissue Res 49:401-408
29. Furth JJ, Allen RG, Tresini M, Keogh B, Cristofalo VJ (1997) Abundance of alpha 1(I) and alpha 1(III) procollagen and p21 mRNAs in fibroblasts cultured from fetal and postnatal dermis. Mech Ageing Dev 97:131-142 (Pubitemid 27283175)
30. Mays PK, Bishop JE, Laurent GJ (1988) Age-related changes in the proportion of types I and III collagen. Mech Ageing Dev 45:203-212 (Pubitemid 19004062)
31. Takeda K, Gosiewska A, Peterkofsky B (1992) Similar, but not identical, modulation of expression of extracellular matrix components during in vitro and in vivo aging of human skin fibroblasts. J Cell Phys 153:450-459
32. Varani J, Dame MK, Rittie L, Fligiel SE, Kang S, Fisher GJ, Voorhees JJ (2006) Decreased collagen production in chronologically aged skin: roles of age-dependent alteration in fibroblast function and defective mechanical stimulation. Am J Pathol 168:1861-1868 (Pubitemid 43825306)
33. Cooper TK, Zhong Q, Krawczyk M, Tae HJ, MÅller GA, Schubert R, Myers LA, Dietz HC, Talan MI, Briest W (2010) The haploinsufficient Col3a1 mouse as a model for vascular Ehlers-Danlos syndrome. Vet Pathol 47:1028-1039
34. Schultz GS, Davidson JM, Kirsner RS, Bornstein P, Herman IM (2011) Dynamic reciprocity in the wound microenvironment. Wound Rep Reg 19:134-148
35. Leight JL, Wozniak MA, Chen S, Lynch ML, Chen CS (2012) Matrix rigidity regulates a switch between TGF-beta 1 induced apoptosis and epithelial- mesenchymal transition. Mol Biol Cell 23:677-689
36. Hurme T, Kalimo H, Sandberg M, Lehto JM, Vuorio E (1991) Localization of type I and III collagen and fibronectin production in injured gastrocnemius muscle. Lab Invest 64:76-84
37. Liu SH, Yang RS, Al-Haikh R, Lane JM (1995) Collagen in tendon, ligament and bone healing. Clin Orthop Relat Res 318:265-278
38. Merkel JR, DiPaolo BR, Hallock GG, Rice DC (1988) Type I and type III collagen content of healing wounds in fetal and adult rats. Proc Soc Exp Biol Med 187:493-497
39. Briest W, Cooper TK, Tae HJ, Krawczyk M, McDonald DM, Talan MI (2011) Doxycycline ameliorates the susceptibility to aortic lesions in a mouse model for the vascular type of Ehlers-Danlos syndrome. J Pharmacol Exp Ther 337:621-627
40. Luo R, Jeong SJ, Jin Z, Strokes N, Li S, Piao X (2011) G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination. Proc Natl Acad Sci USA 108:12925-12930
41. Apaja-Sarkkinen M, Autio-Harmainen H, Alavaikko M, Risteli J, Risteli L (1986) Immunohistochemical study of basement membrane proteins and type III procollagen in myelofibrosis. Br J Haematol 63:571-580 (Pubitemid 16033578)
42. Becker J, Schuppan D, Benzian H, Bals T, Hahn EG, Cantaluppi C, Reichart P (1986) Immunohistochemical distribution of collagens type IV, V, and VI and of pro-collagens types I and III in human alveolar bone and dentine. J Histochem Cytochem 34:1417-1429 (Pubitemid 16005394)
43. Bentley S, Alabaster O, Foidart JM (1981) Collagen heterogeneity in normal human bone marrow. Br J Haematol 48:287-291 (Pubitemid 11054531)
44. Miller E (1973) A review of biochemical studies on the genetically distinct collagens of the skeletal system. Clin Orthop Relat Res 92:260-280
45. Muller P, Raisch K, Matzen K, Gay S (1977) Presence of type III collagen in bone from a patient with osteogenesis imperfecta. Eur J Pediatr 125:29-37 (Pubitemid 8089304)
46. Carter D, Sloan P, Aaron JE (1991) Immunolocalization of collagen types I and III, tenascin and fibronectin in intramembranous bone. J Histochem Cytochem 39:599-606
47. Luther F, Saino H, Carter DH, Aaron JE (2003) Evidence for an extensive collagen type III/VI proximal domain in the rat femur. Bone 32:652-659 (Pubitemid 37297389)
48. Stevenson K, Kucich U, Whitbeck C, Levin RM, Howard PS (2006) Functional changes in bladder tissue from type III collagen-deficient mice. Mol Cell Biochem 283:107-114
49. Germain DP (2007) Ehlers-Danlos syndrome type IV. Orphanet J Rare Dis 2:32-41
50. Balla B, Kósa JP, Kiss J, Borsy A, Podani J, Takács I, Lazáry A, Nagy Z, Bácsi K, Speer G, Orosz L, Lakatos P (2008) Different gene expression patterns in the bone tissue of aging and post-menopausal osteoporotic and non-osteoporotic women. Calcif Tissue Int 82:12-26
51. Willinghamm MD, Brodt MD, Lee KL, Stephens AL, Ye J, Silva MJ (2010) Age-related changes in bone structure and strength in female and male BALB/c mice. Calcif Tissue Int 86:470-483
52. Olsen BR, Reginato AM, Wang W (2000) Bone development. Annu Rev Cell Dev Biol 16:191-220 (Pubitemid 32037505)
53. 2-terminal propeptide of type I procollagen acts intracellularly to modulate cell function. J Biol Chem 281:38507-38518
54. Zhu Y, Oganesian A, Keene DR, Sandell LJ (1999) Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-beta1 and BMP2. J Cell Biol 144:1069-1080 (Pubitemid 29238979)
55. Zoppi N, Gardella R, DePaepe A, Barlati S, Colombi M (2004) Human fibroblasts with mutations in COL5A1 and COL3A1 genes do not organize collagens and fibronectin in the extracellular matrix, down-regulate α2β1 integrin, and recruit αvβ3 instead of α5β1 integrin. J Biol Chem 279:18157-18168 (Pubitemid 38623228)