Identification and differential expression of human collagenase-3 mRNA species derived from internal deletion, alternative splicing, and defferent polyandenylation and transcription initiation sites

Osteoarthritis and Cartilage

Volumn 11, Issue 7, 2003, Pages 524-537

  Tardif, G ^a   Dupuis, M ^a   Reboul, P ^a   Geng, C S ^a   Pelletier, J P ^a   Ranger, P ^b   Martel Pelletier, Johanne ^a  

^a NOTRE DAME HOSPITAL   (Canada)

^b HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

Author keywords

Alternative splicing; Chondrocytes; Collagenase 3; Osteoarthritis; RNA processing; Transcription

Indexed keywords

COLLAGENASE 3; COMPLEMENTARY DNA; HEMOPEXIN; MESSENGER RNA;

ADULT; AGED; ALTERNATIVE RNA SPLICING; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL LINE; CHONDROSARCOMA; COLLAGEN DEGRADATION; COMPLEX FORMATION; CONTROLLED STUDY; DATA ANALYSIS; DNA LIBRARY; ENZYME ACTIVITY; GENE CONTROL; GENE DELETION; GENETIC CODE; GENETIC SCREENING; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROENVIRONMENT; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA HYBRIDIZATION; RNA SYNTHESIS; TRANSCRIPTION INITIATION SITE; UPREGULATION;

EID: 0037534158     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1063-4584(03)00079-7     Document Type: Article

References (66)

1. Martel-Pelletier J, Tardif G, Fernandes JC, Pelletier JP. Metalloproteases and their modulation as treatment in osteoarthritis. In: Tsokos GC, Ed. Molecular Rheumatology. Totowa: Humana Press Inc 2000; 499-514.
2. Reboul P, Pelletier JP, Tardif G, Cloutier JM, Martel-Pelletier J. The new collagenase, collagenase-3, is expressed and synthesized by human chondrocytes but not by synoviocytes: a role in osteoarthritis. J Clin Invest 1996;97:2011-9.
3. Mitchell PG, Magna HA, Reeves LM, Lopresti-Morrow LL, Yocum SA, Rosner PJ, et al. Cloning, expression, and type II, collagenolytic activity of matrix metalloproteinase-13 from human osteoarthritic cartilage. J Clin Invest 1996;97:761-8.
4. Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G. Biochemical characterization of human collagenase-3. J Biol Chem 1996;271:1544-50.
5. Johansson N, Saarialho-Kere U, Airola K, Herva R, Nissinen L, Westermarck J, et al. Collagenase-3 (MMP-13) is expressed by hypertrophic chondrocytes, periosteal cells, and osteoblasts during human fetal bone development. Dev Dyn 1997;208:387-97.
6. Stahle-Backdahl M, Sandstedt B, Bruce K, Lindahl A, Jimenez MG, Vega JA, et al. Collagenase-3 (MMP-13) is expressed during human fetal ossification and re-expressed in postnatal bone remodeling and in rheumatoid arthritis. Lab Invest 1997;76:717-28.
7. Wernicke D, Seyfert C, Hinzmann B, Gromnica-Ihle E. Cloning of collagenase 3 from the synovial membrane and its expression in rheumatoid arthritis and osteoarthritis. J Rheumatol 1996;23:590-5.
8. Billinghurst RC, Dahlberg L, Ionescu M, Reiner A, Bourne R, Rorabeck C, et al. Enhanced cleavage of Type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest 1997;99:1534-45.
9. Westhoff CS, Freudiger D, Petrow P, Seyfert C, Zacher J, Kriegsmann J, et al. Characterization of collagenase 3 (matrix metalloproteinase 13) messenger RNA expression in the synovial membrane and synovial fibroblasts of patients with rheumatoid arthritis. Arthritis Rheum 1999;42:1517-27.
10. Lindy O, Konttinen YT, Sorsa T, Ding Y, Santavirta S, Ceponis A, et al. Matrix metalloproteinase 13 (collagenase 3) in human rheumatoid synovium. Arthritis Rheum 1997;40:1391-9.
11. Freije JM, Diez-Itza I, Balbin M, Sanchez LM, Blasco R, Tolivia J, et al. Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 1994;269:16766-73.
12. Johansson N, Airola K, Grenman R, Kariniemi AL, Saarialho-Kere U, Kahari VM. Expression of collagenase-3 (matrix metalloproteinase-13) in squamous cell carcinomas of the head and neck. Am J Pathol 1997;151:499-508.
13. Cazorla M, Hernandez L, Nadal A, Balbin M, Lopez JM, Vizoso F, et al. Collagenase-3 expression is associated with advanced local invasion in human squamous cell carcinomas of the larynx. J Pathol 1998;186:144-50.
14. Balbin M, Pendas AM, Uria JA, Jimenez MG, Freije JP, Lopez-Otin C. Expression and regulation of collagenase-3 (MMP-13) in human malignant tumors. APMIS 1999;107:45-53.
15. Pendas AM, Uria JA, Jimenez MG, Balbin M, Freije JP, Lopez-Otin C. An overview of collagenase-3 expression in malignant tumors and analysis of its potential value as a target in antitumor therapies. Clin Chim Acta 2000;291:137-55.
16. Vaalamo M, Mattila L, Johansson N, Kariniemi AL, Karjalainen-Lindsberg ML, Kahari VM, et al. Distinct populations of stromal cells express collagenase-3 (MMP-13) and collagenase-1 (MMP-1) in chronic ulcers but not in normally healing wounds. J Invest Dermatol 1997;109:96-101.
17. Moldovan F, Pelletier JP, Hambor J, Cloutier JM, Martel- Pelletier J. Collagenase-3 (matrix metalloprotease 13) is preferentially localized in the deep layer of human arthritic cartilage in situ: in vitro mimicking effect by transforming growth factor beta. Arthritis Rheum 1997;40:1653-61.
18. Hellio Le Graverand MP, Eggerer J, Sciore P, Reno C, Vignon E, Otterness I, et al. Matrix metalloproteinase-13 expression in rabbit knee joint connective tissues, influence of maturation and response to injury. Matrix Biol 2000;19:431-41.
19. Fernandes JC, Martel-Pelletier J, Lascau-Coman V, Moldovan F, Jovanovic D, Raynauld JP, et al. Collagenase-1 and collagenase-3 synthesis in early experimental osteoarthritic canine cartilage. An immunohistochemical study. J Rheumatol 1998; 25:1585-94.
20. Knauper V, Cowell S, Smith B, Lopez-Otin C, O'Shea M, Morris H, et al. The role of the C-terminal domain of human collagenase-3 (MMP-13) in the activation of procollagenase-3, substrate specificity, and tissue inhibitor of metalloproteinase interaction. J Biol Chem 1997;272:7608-16.
21. Fosang AJ, Last K, Knauper V, Murphy G, Neame PJ. Degradation of cartilage aggrecan by collagenase-3 (MMP-13). FEBS Lett 1996;380:17-20.
22. Knauper V, Will H, Lopez-Otin C, Smith B, Atkinson SJ, Stanton H, et al. Cellular mechanisms for human procollagenase-3 (MMP-13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase a (MMP-2) are able to generate active enzyme. J Biol Chem 1996; 271:17124-31.
23. Borden P, Solymar D, Sucharczuk A, Lindman B, Cannon P, Heller RA. Cytokine control of interstitial collagenase and collagenase-3 gene expression in human chondrocytes. J Biol Chem 1996; 271:23577-81.
24. Ravanti L, Heino J, Lopez-Otin C, Kahari VM. Induction of collagenase-3 (MMP-13) expression in human skin fibroblasts by three-dimensional collagen is mediated by p38 mitogen-activated protein kinase. J Biol Chem 1999;274:2446-55.
25. Uria JA, Balbin M, Lopez JM, Alvarez J, Vizoso F, Takigawa M, et al. Collagenase-3 (MMP-13) expression in chondrosarcoma cells and its regulation by basic fibroblast growth factor. Am J Pathol 1998; 153:91-101.
26. Caron JP, Tardif G, Martel-Pelletier J, Di Battista JA, Geng C, Pelletier JP. Modulation of matrix metalloproteases 13 (collagenase 3) gene expression in equine chondrocytes by interleukin 1 and corticosteroids. Am J Vet Res 1996;57:1631-4.
27. Quinn CO, Scott DK, Brinckerhoff CE, Matrisian LM, Jeffrey JJ, Partridge NC. Rat collagenase. Cloning, amino acid sequence comparison, and parathyroid hormone regulation in osteoblastic cells. J Biol Chem 1990;265:22342-7.
28. Vincenti MP, Coon CI, Mengshol JA, Yocum S, Mitchell P, Brinckerhoff CE. Cloning of the gene for interstitial collagenase-3 (matrix metalloproteinase-13) from rabbit synovial fibroblasts: differential expression with collagenase-1 (matrix metalloproteinase-1 ). Biochem J 1998;331:341-6.
29. Altman RD, Asch E, Bloch DA, Bole G, Borenstein D, Brandt KD, et al. Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Arthritis Rheum 1986;29:1039-49.
30. Mankin HJ, Dorfman H, Lippiello L, Zarins A. Biochemical and metabolic abnormalities in articular cartilage from osteoarthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 1971;53:523-37.
31. Tardif G, Di Battista JA. Pelletier J-P, Martel-Pelletier J. Measurement of interleukin mRNA by Northern blotting using a non-radioactive detection method. In: O'Neill L, Ed. Interleukin Protocols. Totowa: Humana Press Inc 2000.
32. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389-402.
33. Fernandes JC, Tardif G, Martel-Pelletier J, Lascau-Coman V, Dupuis M, Moldovan F, et al. In vivo transfer of interleukin-1 receptor antagonist gene in osteoarthritic rabbit knee joints: prevention of osteoarthritis progression. Am J Pathol 1999; 154:1159-69.
34. Tardif G, Pelletier JP, Dupuis M, Hambor JE, Martel-Pelletier J. Cloning, sequencing and characterization of the 5′-flanking region of the human collagenase-3 gene. Biochem J 1997;323:13-6.
35. Fernandes JC, Martel-Pelletier J, Jovanovic D, Tardif G, Di Battista JA, Lascau-Coman V, et al. Effects of tenidap on canine experimental osteoarthritis. II: Study of the expression of collagenase-1 and IL1β by in situ hybridization. J Rheumatol 1998;25:951-8.
36. Mount SM. A catalogue of splice junction sequences. Nucleic Acids Res 1982;10:459-72.
37. Rogozin IB, Milanesi L. Analysis of donor splice sites in different eukaryotic organisms. J Mol Evol 1997; 45:50-9.
38. Pendas AM, Balbin M, Llano E, Jimenez MG, Lopez-Otin C. Structural analysis and promoter characterization of the human collagenase-3 gene (MMP-13). Genomics 1997;40:222-33.
39. Kornblihtt AR, Pesce CG, Alonso CR, Cramer P, Srebrow A, Werbajh S, et al. The fibronectin gene as a model for splicing and transcription studies. FASEB J 1996;10:248-57.
40. Uporova TM, Norton PA, Tuan RS, Bennett VD. Alternative splicing during chondrogenesis: cis and trans factors involved in splicing of fibronectin exon EIIIA. J Cell Biochem 1999;76:341-51.
41. Gong Q, Chan SJ, Bajkowski AS, Steiner DF, Frankfater A. Characterization of the cathepsin B gene and multiple mRNAs in human tissues: evidence for alternative splicing of cathepsin B pre-mRNA. DNA Cell Biol 1993;12:299-309.
42. Berquin IM, Cao L, Fong D, Sloane BF. Identification of two new exons and multiple transcription start points in the 5′-untranslated region of the human cathepsin-B-encoding gene. Gene 1995;159:143-9.
43. Zarrilli R, Bruni CB, Riccio A. Multiple levels of control of insulin-like growth factor gene expression. Mol Cell Endocrinol 1994;101:R1.
44. Grzybowska EA, Wilczynska A, Siedlecki JA. Regulatory functions of 3′UTRs. Biochem Biophys Res Commun 2001;288:291-5.
45. Edwalds-Gilbert G, Veraldi KL, Milcarek C. Alternative poly(A) site selection in complex transcription units: means to an end?. Nucleic Acids Res 1997; 25:2547-61.
46. Jackson RJ. Cytoplasmic regulation of mRNA function: the importance of the 3′ untranslated region. Cell 1993;74:9-14.
47. Tardif G, Pelletier JP, Dupuis M, Geng C, Cloutier JM, Martel-Pelletier J. Collagenase 3 production by human osteoarthritic chondrocytes in response to growth factors and cytokines is a function of the physiological state of the cells. Arthritis Rheum 1999; 42:1147-58.
48. Mengshol JA, Vincenti MP, Coon CI, Barchowsky A, Brinckerhoff CE. Interleukin-1 induction of collagenase 3 (matrix metalloproteinase 13) gene expression in chondrocytes requires p38, c-Jun N-terminal kinase, and nuclear factor kappaB: differential regulation of collagenase 1 and collagenase 3. Arthritis Rheum 2000;43:801-11.
49. Ala-aho R, Johansson N, Grenman R, Fusenig NE, Lopez-Otin C, Kahari VM. Inhibition of collagenase-3 (MMP-13) expression in transformed human keratinocytes by interferon-gamma is associated with activation of extracellular signal-regulated kinase-1,2 and STAT1. Oncogene 2000;19:248-57.
50. Johansson N, Westermarck J, Leppä S, Häkkinen L, Koivisto L, Lopez-Otin S, et al. Collagenase 3 (matrix metalloproteinase 13) gene expression by HaCaT keratinocytes is enhanced by tumor necrosis factor-α and transforming growth factor β. Cell Growth Differ 1997;8:243-50.
51. Uria JA, Jimenez MG, Balbin M, Freije JMP, Lopez-Otin C. Differential effects of transforming growth factor-beta on the expression of collagenase-1 and collagenase-3 in human fibroblasts. J Biol Chem 1998;273:9769-77.
52. Ravanti L, Hakkinen L, Larjava H, Saarialho-Kere U, Foschi M, Han J, et al. Transforming growth factor-beta induces collagenase-3 expression by human gingival fibroblasts via p38 mitogen-activated protein kinase. J Biol Chem 1999;274:37292-300.
53. Graveley BR. Alternative splicing: increasing diversity in the proteomic world. Trends Genet 2001;17: 100-7.
54. Lemaire R, Flipo RM, Migaud H, Fontaine C, Huet G, Dacquembronne E, et al. Alternative splicing of the 5′ region of cathepsin B pre-messenger RNA in rheumatoid synovial tissue. Arthritis Rheum 1997; 40:1540-2.
55. Makalowski W, Mitchell GA, Labuda D. Alu sequences in the coding regions of mRNA: a source of protein variability. Trends Genet 1994;10:188-93.
56. Mighell AJ, Markham AF, Robinson PA. Alu sequences. FEBS Lett 1997;417:1-5.
57. Hu SI, Klein M, Carozza M, Rediske J, Peppard J, Qi JS. Identification of a splice variant of neutrophil collagenase (MMP-8). FEBS Lett 1999;443:8-10.
58. Miller SJ, Suthiphongchai T, Zambetti GP, Ewen ME. p53 binds selectively to the 5′ untranslated region of cdk4, an RNA element necessary and sufficient for transforming growth factor beta-and p53-mediated translational inhibition of cdk4. Mol Cell Biol 2000; 20:8420-31.
59. Goldstein LA, Chen WT. Identification of an alternatively spliced seprase mRNA that encodes a novel intracellular isoform. J Biol Chem 2000;275:2554-9.
60. Morishita M, Kishino T, Furukawa K, Yonekura A, Miyazaki Y, Kanematsu T, et al. A 30-base-pair element in the first intron of SOX9 acts as an enhancer in ATDC5. Biochem Biophys Res Commun 2001;288:347-55.
61. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, et al. SOX9 directly regulates the type-II collagen gene. Nat Genet 1997;16:174-8.
62. Beier F, Vornehm S, Poschl E, von der Mark K, Lammi MJ. Localization of silencer and enhancer elements in the human type X collagen gene. J Cell Biochem 1997;66:210-8.
63. Liu Y, Li H, Tanaka K, Tsumaki N, Yamada Y. Identification of an enhancer sequence within the first intron required for cartilage-specific transcription of the alpha2(XI) collagen gene. J Biol Chem 2000; 275:12712-8.
64. Thornborrow EC, Patel S, Mastropietro AE, Schwartzfarb EM, Manfredi JJ. A conserved intronic response element mediates direct p53-dependent transcriptional activation of both the human and murine bax genes. Oncogene 2002;21:990-9.
65. Tasheva ES, Maki CG, Conrad AH, Conrad GW. Transcriptional activation of bovine mimecan by p53 through an intronic DNA-binding site. Biochim Biophys Acta 2001; 1517:333-8.
66. Ayoubi TA, Van De Ven WJ. Regulation of gene expression by alternative promoters. FASEB J 1996; 10:453-60.