Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
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Pleiotropic Roles of Metalloproteinases in Hematological Malignancies: an Update

  • Chaudhary, Ajay K (Department of Immunohematology, National Institute of Immunohematology, KEM Hospital Campus) ;
  • Chaudhary, Shruti (Hematopathology Laboratory, Tata Memorial Hospital) ;
  • Ghosh, Kanjaksha (Department of Immunohematology, National Institute of Immunohematology, KEM Hospital Campus) ;
  • Nadkarni, A (Department of Immunohematology, National Institute of Immunohematology, KEM Hospital Campus)
  • Published : 2016.07.01
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Abstract

Controlled remodeling of the extracellular matrix (ECM) is essential for cell growth, invasion and metastasis. Matrix metalloproteinases (MMPs) are a family of secreted, zinc-dependent endopeptidases capable of degradation of ECM components. The expression and activity of MMPs in a variety of human cancers have been intensively studied. They play important roles at different steps of malignant tumor formation and have central significance in embryogenesis, tissue remodeling, inflammation, angiogenesis and metastasis. However, increasing evidence demonstrates that MMPs are involved earlier in tumorigenesis. Recent studies also suggest that MMPs play complex roles in tumor progression. MMPs and membrane type (MT)-MMPs are potentially significant therapeutic targets in many cancers, so that designing of specific MMP inhibitors would be helpful for clinical trials. Here, we review the pleiotropic roles of the MMP system in hematological malignancies in-vitro and in-vivo models.

Keywords

References

  1. Alcantara MB, Dass CR (2014). Pigment epithelium-derived factor as a natural matrix metalloproteinase inhibitor: a comparison with classical matrix metalloproteinase inhibitors used for cancer treatment. J Pharm Pharmacol, 66, 895-902. https://doi.org/10.1111/jphp.12218
  2. Bagby GC, Alter BP (2006). Fanconi anemia. Semin Hematol, 43, 147-56. https://doi.org/10.1053/j.seminhematol.2006.04.005
  3. Barille S, Akhoundi C, Collette M, et al (1997). Metalloproteinases in multiple myeloma: production of matrix metalloproteinase-9 (MMP-9), activation of proMMP-2, and induction of MMP-1 by myeloma cells. Blood, 90, 1649-55.
  4. Bernal T, Moncada-Pazos A, Soria-Valles C et al (2013). Effects of azacitidine on matrix metalloproteinase-9 in acute myeloid leukemia and myelodysplasia. Exp Hematol, 41, 172-9. https://doi.org/10.1016/j.exphem.2012.10.005
  5. Brown GD, Nazarali AJ (2010). Matrix metalloproteinase-25 has a functional role in mouse secondary palate development and is a downstream target of $TGF-{\beta}3$. BMC Dev Biol, 10, 93. https://doi.org/10.1186/1471-213X-10-93
  6. Campo E, Swerdlow SH, Harris NL et al (2011). The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood, 117, 5019-32. https://doi.org/10.1182/blood-2011-01-293050
  7. Chaudhary AK, Pandya S, Ghosh K et al (2013). Matrix metalloproteinase and its drug targets therapy in solid and hematological malignancies: an overview. Mutat Res, 753, 7-23. https://doi.org/10.1016/j.mrrev.2013.01.002
  8. Chaudhary AK, Pandya S, Mehrotra R et al (2011). Role of functional polymorphism of matrix metalloproteinase-2 (-1306 C/T and -168 G/T) and MMP-9 (-1562 C/T) promoter in oral submucous fibrosis and head and neck squamous cell carcinoma in an Indian. Biomarkers, 16, 577-86. https://doi.org/10.3109/1354750X.2011.609602
  9. Chaudhary AK, Singh M, Bharti AC, et al (2010). Genetic polymorphisms of matrix metalloproteinases and their inhibitors in potentially malignant and malignant lesions of the head and neck. Biomed Sci, 17, 10. https://doi.org/10.1186/1423-0127-17-10
  10. Chaudhary AK, Singh M, Bharti AC, et al (2010). Synergistic effect of stromelysin-1 (matrix metalloproteinase-3) promoter (-1171 5A->6A) polymorphism in oral submucous fibrosis and head and neck lesions. BMC Cancer, 10, 369. https://doi.org/10.1186/1471-2407-10-369
  11. Cianfrocca M, Cooley TP, Lee JY, et al (2002). Matrix metalloproteinase inhibitor COL-3 in the treatment of AIDS-related Kaposi's sarcoma: a phase I AIDS malignancy consortium study. J Clin Oncol, 20, 153-9.
  12. DeClerck YA, Perez N, Shimada H, et al (1992). Inhibition of invasion and metastasis in cells transfected with an inhibitor of metalloproteinases. Cancer Res, 52, 701-8.
  13. Deryugina EI, Quigley JP (2010). Pleiotropic roles of matrix metalloproteinases in tumor angiogenesis: contrasting, overlapping and compensatory functions. Biochim Biophys Acta, 1803, 103-20. https://doi.org/10.1016/j.bbamcr.2009.09.017
  14. Deschler B, Lubbert M (2006). Acute myeloid leukemia: epidemiology and etiology. Cancer, 107, 2099-107. https://doi.org/10.1002/cncr.22233
  15. Dezube BJ, Krown SE, Lee JY, et al (2006). Randomized phase II trial of matrix metalloproteinase inhibitor COL-3 in AIDSrelated Kaposi's sarcoma: an AIDS malignancy consortium study. J Clin Oncol, 24, 1389-94. https://doi.org/10.1200/JCO.2005.04.2614
  16. Edman K, Furber M, Hemsley P, et al (2011). “The discovery of MMP7 inhibitors exploiting a novel selectivity trigger”. Chem Med Chem, 6, 769-73. https://doi.org/10.1002/cmdc.201000550
  17. Egeblad M, Werb Z (2002). New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer, 2, 161-74. https://doi.org/10.1038/nrc745
  18. Eguchi T, Kubota S, Kawata K, et al (2008). Novel transcriptionfactor-like function of human matrix metalloproteinase 3 regulating the CTGF/CCN2 gene. Molecular Cellular Biol, 28, 2391-413. https://doi.org/10.1128/MCB.01288-07
  19. Epanchintsev A, Shyamsunder P, Verma RS, et al (2015). IL-6, IL-8, MMP-2, MMP-9 are overexpressed in Fanconi anemia cells through a $NF-{\kappa}B$/TNF-${\alpha}$ dependent mechanism. Mol Carcinog, 54, 1686-99. https://doi.org/10.1002/mc.22240
  20. Fanjul-Fernandez M, Folgueras AR, Cabrera S, et al (2010). Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models. Biochim Biophys Acta, 1803, 3-19. https://doi.org/10.1016/j.bbamcr.2009.07.004
  21. Farina AR, Cappabianca L, DeSantis G, et al (2011). Thioredoxin stimulates MMP-9 expression, de-regulates the MMP-9/TIMP-1 equilibrium and promotes MMP-9 dependent invasion in human MDA-MB-231 breast cancer cells. FEBS Lett, 585, 3328-36. https://doi.org/10.1016/j.febslet.2011.09.023
  22. Forsyth PA, Wong H, Laing TD, et al (1999). Gelatinase-A (MMP-2), gelatinase-B (MMP-9) and membrane type matrix metalloproteinase-1 (MT1-MMP) are involved in different aspects of the pathophysiology of malignant gliomas. British J Cancer, 79, 1828-35. https://doi.org/10.1038/sj.bjc.6990291
  23. Gallipoli P, Giotopoulos G, Huntly BJ (2015). Epigenetic regulators as promising therapeutic targets in acute myeloid leukemia. Ther Adv Hematol, 6, 103-19 https://doi.org/10.1177/2040620715577614
  24. Gao H, Peng C, Liang B, et al (2014). ${\beta}6$ Integrin induces the expression of metalloproteinase-3 and metalloproteinase-9 in colon cancer cells via ERK-ETS1 pathway. Cancer Lett, 354, 427-37 https://doi.org/10.1016/j.canlet.2014.08.017
  25. Graux C, Cools J, Michaux et al (2002). Cytogenetics and molecular genetics of Tcell acute lymphoblastic leukemia: from thymocyte to lymphoblast. Leukemia, 20, 1496-510.
  26. Greenberg PL, Young NS, Gattermann N (2002). Myelodysplastic syndromes. Hematol Am Soc Hematol Educ Program, 2002, 136-61.
  27. Hanahan D, Folkman J (1996). Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-64. https://doi.org/10.1016/S0092-8674(00)80108-7
  28. Harrison CJ, Haas O, Harbott J, et al (2010). Detection of prognostically relevant genetic abnormalities in childhood B-cell precursor acute lymphoblastic leukaemia: recommendations from the biology and diagnosis committee of the international berlin-frankfurt-munster study group. Br J Haem, 151, 132-42. https://doi.org/10.1111/j.1365-2141.2010.08314.x
  29. He QT, Bai XQ, Liu XW, et al (2014). 13. Protein and mRNA expression of CTGF, CYR61, VEGF-C and VEGFR-2 in bone marrow of leukemia patients and its correlation with clinical features. Zhongguo Shi Yan Xue Ye Xue Za Zhi, 22, 653-9.
  30. Hoek KS, Schlegel NC, Eichhoff OM, et al (2008). "Novel MITF targets identified using a two-step DNA microarray strategy". Pigment Cell Melanoma Res, 21, 665-76. https://doi.org/10.1111/j.1755-148X.2008.00505.x
  31. Hua H, Li M, Luo T, et al (2011). Matrix metalloproteinases in tumorigenesis: an evolving paradigm. Cell Mol Life Sci, 68, 3853-68. https://doi.org/10.1007/s00018-011-0763-x
  32. Hwang TL, Changchien TT, Wang CC, et al (2014). Claudin-4 expression in gastric cancer cells enhances the invasion and is associated with the increased level of matrix metalloproteinase-2 and -9 expression. Oncol Lett, 8, 1367-71. https://doi.org/10.3892/ol.2014.2295
  33. Iwata M, Pillai M, Ramakrishnan A et al (2007). Reduced expression of inducible gelatinase B/matrix metalloproteinase-9 in monocytes from patients with myelodysplastic syndrome: Correlation of inducible levels with the percentage of cytogenetically marked cells and with marrow cellularity. Blood, 109, 85-92. https://doi.org/10.1182/blood-2006-05-020289
  34. Janowska-Wieczorek A, Majka M, et al (2002). Bcr-ablpositive cells secrete angiogenic factors including matrix metalloproteinases and stimulate angiogenesis in vivo in Matrigel implants. Leukemia, 16, 1160-6. https://doi.org/10.1038/sj.leu.2402486
  35. Jiang L, Yu G, Meng W et al (2013). Overexpression of amyloid precursor protein in acute myeloid leukemia enhances extramedullary infiltration by MMP-2. Tumour Biol, 34, 629-36. https://doi.org/10.1007/s13277-012-0589-7
  36. Johansson N, Ahonen M, Kahari VM. (2000). Matrix metalloproteinases in tumor invasion. Cell Mol Life Sci. 57, 5-15. https://doi.org/10.1007/s000180050495
  37. Klein G, Schmal O, Aicher WK (2015). Matrix metalloproteinases in stem cell mobilization. Matrix Biol, 44-46, 175-83. https://doi.org/10.1016/j.matbio.2015.01.011
  38. Kuittinen O, Savolainen ER, Koistinen P, et al (2001). MMP-2 and MMP-9 expression in adult and childhood acute lymphatic leukemia (ALL). Leuk Res, 25, 125-31. https://doi.org/10.1016/S0145-2126(00)00104-1
  39. Lin LI, Lin DT, Chang CJ et al (2002). Marrow matrix metalloproteinases (MMPs) and tissue inhibitors of MMP in acute leukaemia: potential role of MMP-9 as a surrogate marker to monitor leukaemic status in patients with acute myelogenous leukaemia. Br J Haematol, 117, 835-41. https://doi.org/10.1046/j.1365-2141.2002.03510.x
  40. List AF, Vardiman J, Issa JP, et al (2004). Myelodysplastic syndromes. Hematol Am Soc Hematol Educ Program, 2004, 297-317.
  41. Lu XS, Sun W, Ge CY, et al (2013). Contribution of the PI3K/MMPs/$Ln-5{\gamma}2$ and EphA2/FAK/Paxillin signaling pathways to tumor growth and vasculogenic mimicry of gallbladder carcinomas. Int J Oncol, 42, 2103-15. https://doi.org/10.3892/ijo.2013.1897
  42. Luo D, Mari B, Stoll I, et al (2002). Alternative splicing and promoter usage generates an intracellular stromelysin 3 isoform directly translated as an active matrix metalloproteinase. J Biol Chem, 277, 25527-36. https://doi.org/10.1074/jbc.M202494200
  43. Ma J, Wang J, Fan W, et al (2013). Upregulated TIMP-1 correlates with poor prognosis of laryngeal squamous cell carcinoma. Int J Clin Exp Pathol, 15, 246-54.
  44. Maquoi E, Sounni NE, Devy L, et al (2004). Anti-invasive, antitumoral, and antiangiogenic efficacy of a pyrimidine-2, 4, 6-trione derivative, an orally active and selective matrix metalloproteinases inhibitor. Clin Cancer Res, 10, 4038-47. https://doi.org/10.1158/1078-0432.CCR-04-0125
  45. Martignetti JA, Aqeel AA, Sewairi WA et al (2001). Mutation of the matrix metalloproteinase 2 gene (MMP2) causes a multicentric osteolysis and arthritis syndrome. Nat Genet, 28, 261-5. https://doi.org/10.1038/90100
  46. Matias-Roman S, Galvez BG, Genis L, et al (2005). Membrane type 1-matrix metalloproteinase is involved in migration of human monocytes and is regulated through their interaction with fibronectin or endothelium. Blood, 105, 3956-64. https://doi.org/10.1182/blood-2004-06-2382
  47. Mejia-Cristobal LM, Reus E, Lizarraga F, Espinosa M, et al (2015). Tissue inhibitor of metalloproteases-4 (TIMP-4) modulates adipocyte differentiation in vitro. Exp Cell Res, 335, 207-15. https://doi.org/10.1016/j.yexcr.2015.05.006
  48. Moon JW, Choi JH, Lee SK, et al (2015). Promoter hypermethylation of membrane type 3 matrix metalloproteinase is associated with cell migration in colorectal adenocarcinoma. Cancer Genet, 208, 261-70. https://doi.org/10.1016/j.cancergen.2015.04.009
  49. Nagase H, Visse R, Murphy G (2006). Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res, 69, 562-73. https://doi.org/10.1016/j.cardiores.2005.12.002
  50. Okumura AJ, Peterson LF, Okumura F, et al (2008). t(8;21) (q22;q22) Fusion proteins preferentially bind to duplicated AML1/RUNX1 DNA-binding sequences to differentially regulate gene expression. Blood, 112, 1392-401. https://doi.org/10.1182/blood-2007-11-124735
  51. Olczyk P, Mencner L, Komosinska-Vassev K (2014). The role of the extracellular matrix components in cutaneous wound healing. Biomed Res Int, 2014, 747584.
  52. Owen JL, Iragavarapu-Charyulu V, Gunja-Smith Z, et al (2003). Up-regulation of matrix metalloproteinase-9 in T lymphocytes of mammary tumor bearers: role of vascular endothelial growth factor. J Immunol, 171, 4340-51. https://doi.org/10.4049/jimmunol.171.8.4340
  53. Pan YX, Yang L, Wen SP, et al (2014). Expression and clinical significance of MMP-2 and MMP-9 in B acute lymphoblastic leukemia. Zhongguo Shi Yan Xue Ye Xue Za Zhi, 22, 640-3.
  54. Parvathy SS, Masocha W (2013). Matrix metalloproteinase inhibitor COL-3 prevents the development of paclitaxelinduced hyperalgesia in mice. Med Princ Pract, 22, 35-41. https://doi.org/10.1159/000341710
  55. Pegahi R, Poyer F, Legrand E, et al (2005). Spontaneous and cytokine-evoked production of matrix metalloproteinases by bone marrow and peripheral blood pre-B cells in childhood acute lymphoblastic leukaemia. Eur Cytokine Netw, 16, 223-32.
  56. Poyer F, Coquerel B, Pegahi R, et al (2009). Secretion of MMP-2 and MMP-9 induced by VEGF autocrine loop correlates with clinical features in childhood acute lymphoblastic leukemia. Leuk Res, 33, 407-17. https://doi.org/10.1016/j.leukres.2008.08.019
  57. Ravera S, Capanni C, Tognotti D, et al (2015). Inhibition of metalloproteinase activity in FANCA is linked to altered oxygen metabolism. J Cell Physiol, 230, 603-9. https://doi.org/10.1002/jcp.24778
  58. Redondo-Munoz J, Ugarte-Berzal E, Garcia-Marco JA, et al (2008). Alpha4beta1 integrin and 190-kDa CD44v constitute a cell surface docking complex for gelatinase B/MMP-9 in chronic leukemic but not in normal B cells. Blood, 112, 169-78. https://doi.org/10.1182/blood-2007-08-109249
  59. Redondo-Munoz J, Ugarte-Berzal E, Terol MJ, et al (2010). Matrix metalloproteinase-9 promotes chronic lymphocytic leukemia b cell survival through its hemopexin domain. Cancer Cell, 17, 160-72. https://doi.org/10.1016/j.ccr.2009.12.044
  60. Ries C, Loher F, Zang C, et al (1999). Matrix metalloproteinase production by bone marrow mononuclear cells from normal individuals and patients with acute and chronic myeloid leukemia or myelodysplastic syndromes. Clin Cancer Res, 5, 1115-24.
  61. Riether C, Schurch CM, Ochsenbein AF (2015). Regulation of hematopoietic and leukemic stem cells by the immune system. Cell Death Differ, 22, 187-98. https://doi.org/10.1038/cdd.2014.89
  62. Roomi MW, Bhanap B, Roomi NW, et al (2014). In vitro inhibition of matrix metalloproteinases, invasion and growth of Fanconi anemia human FANCA and FANCC lymphoblasts by nutrient mixture. Exp Oncol, 36, 212-4.
  63. Roomi MW, Roomi NW, Bhanap B, et al (2013). Repression of matrix metalloproteinases and inhibition of cell invasion by a nutrient mixture, containing ascorbic acid, lysine, proline, and green tea extract on human Fanconi anemia fibroblast cell lines. Exp Oncol, 35, 20-4.
  64. Roy R, Zurakowski D, Wischhusen J, et al (2014). Urinary TIMP-1 and MMP-2 levels detect the presence of pancreatic malignancies. Br J Cancer, 111, 1772-9. https://doi.org/10.1038/bjc.2014.462
  65. Rudek MA, New P, Mikkelsen T, et al (2011). Phase I and pharmacokinetic study of COL-3 in patients with recurrent high-grade gliomas. J Neurooncol, 105, 375-81. https://doi.org/10.1007/s11060-011-0602-9
  66. Scrideli CA, Cortez MA, Yunes JA, et al (2010). mRNA expression of matrix metalloproteinases (MMPs) 2 and 9 and tissue inhibitor of matrix metalloproteinases (TIMPs) 1 and 2 in childhood acute lymphoblastic leukemia: potential role of TIMP1 as an adverse prognostic factor. Leuk Res, 34, 32-7. https://doi.org/10.1016/j.leukres.2009.10.007
  67. Shyamsunder P, Verma RS, Lyakhovich A (2015). ROMO1 regulates RedOx states and serves as an inducer of $NF-{\kappa}B$-driven EMT factors in Fanconi anemia. Cancer Lett, 361, 33-8. https://doi.org/10.1016/j.canlet.2015.02.020
  68. Sithu SD, English WR, Olson P, et al (2007). Membrane-type 1-Matrix Metalloproteinase Regulates Intracellular Adhesion Molecule-1 (ICAM-1)-mediated Monocyte Transmigration. J Biol Chem, 282, 25010-9. https://doi.org/10.1074/jbc.M611273200
  69. Song H, Fares M, Maguire KR, et al (2014). Cytotoxic effects of tetracycline analogues (doxycycline, minocycline and COL-3) in acute myeloid leukemia HL-60 cells. PLoS One, 9, 114457. https://doi.org/10.1371/journal.pone.0114457
  70. Stricker TP, Dumin JA, Dickeson SK, et al (2001). Structural analysis of the alpha(2) integrin I domain/procollagenase-1 (matrix metalloproteinase-1) interaction. J Biol Chem, 276, 29375-81. https://doi.org/10.1074/jbc.M102217200
  71. Suminoe A, Matsuzaki A, Hattori H, et al (2007). Expression of matrix metalloproteinase (MMP) and tissue inhibitor of MMP (TIMP) genes in blasts of infant acute lymphoblastic leukemia with organ involvement. Leuk Res, 31, 1437-40. https://doi.org/10.1016/j.leukres.2007.01.015
  72. Sun X, Li Y, Yu W, et al (2008). MT1-MMP as a downstream target of BCR-ABL/ABL interactor 1 signaling: polarized distribution and involvement in BCR-ABL-stimulated leukemic cell migration. Leukemia, 22, 1053-6. https://doi.org/10.1038/sj.leu.2404990
  73. Tarhini AA, Lin Y, Yeku O, et al (2014). A four-marker signature of TNF-RII, $TGF-{\alpha}$, TIMP-1 and CRP is prognostic of worse survival in high-risk surgically resected melanoma. J Transl Med, 12, 19. https://doi.org/10.1186/1479-5876-12-19
  74. Tong H, Hu C, Yin X, et al (2013). A Meta-Analysis of the Relationship between Cigarette Smoking and Incidence of Myelodysplastic Syndromes. PLoS One, 8, 67537. https://doi.org/10.1371/journal.pone.0067537
  75. Travaglino E, Benatti C, Malcovati L, et al (2008). Biological and clinical relevance of matrix metalloproteinases 2 and 9 in acute myeloid leukaemias and myelodysplastic syndromes. Eur J Haematol, 80, 216-26. https://doi.org/10.1111/j.1600-0609.2007.01012.x
  76. Ugarte-Berzal E, Bailon E, Amigo-Jimenez I, et al (2012). A 17-residue sequence from the matrix metalloproteinase-9 (MMP-9) hemopexin domain binds ${\alpha}4{\beta}1$ integrin and inhibits MMP-9-induced functions in chronic lymphocytic leukemia B cells. J Biol Chem, 287, 27601-13. https://doi.org/10.1074/jbc.M112.354670
  77. Vundinti BR, Kerketta L, Jijina F, et al (2009). Cytogenetic study of myelodysplastic syndrome from India. Indian J Med Res, 130, 155-9.
  78. Wang C, Chen Z, Li Z, et al (2010). The essential roles of matrix metalloproteinase-2, membrane type 1 metalloproteinase and tissue inhibitor of metalloproteinase-2 in the invasive capacity of acute monocytic leukemia SHI-1 cells. Leuk Res, 34, 1083-90. https://doi.org/10.1016/j.leukres.2010.01.016
  79. Xu X, Ma J, Li C et al (2015). Regulation of chondrosarcoma invasion by MMP26. Tumour Biol, 36, 365-9. https://doi.org/10.1007/s13277-014-2657-7
  80. Yamaguchi N, Ito Y, Ohyashiki K (2005). Increased intracellular activity of matrix metalloproteinases in neutrophils may be associated with delayed healing of infection without neutropenia in myelodysplastic syndromes. Ann Hematol, 84, 383-8. https://doi.org/10.1007/s00277-004-0965-5
  81. Yana, I. and Seiki, M. (2002). MT-MMPs play pivotal roles in cancer dissemination. Clin Exp Metastasis, 19, 209-15. https://doi.org/10.1023/A:1015527220537
  82. Yang MX, Qu X, Kong BH, et al (2006). Membrane type 1-matrix metalloproteinase is involved in the migration of human monocyte-derived dendritic cells. Immunol Cell Biol, 84, 557-62. https://doi.org/10.1111/j.1440-1711.2006.01465.x
  83. Yang Z, Fan Y, Deng Z, et al (2012). Amyloid precursor protein as a potential marker of malignancy and prognosis in papillary thyroid carcinoma. Oncol Lett, 3, 1227-30. https://doi.org/10.3892/ol.2012.639
  84. Yeow KM, Kishnani NS, Hutton M, (2002). Sorsby's fundus dystrophy tissue inhibitors of metalloproteinases-3 (TIMP-3) mutants have unimpaired matrix metalloproteinase inhibitory activities, but affect cell adhesion to the extracellular matrix. Matrix Biol, 21, 75-88. https://doi.org/10.1016/S0945-053X(01)00180-9
  85. Yu XF, Han ZC (2006). Matrix metalloproteinases in bone marrow: roles of gelatinases in physiological hematopoiesis and hematopoietic malignancies. Histol Histopathol, 21, 519-31.
  86. Zhang G, Miyake M, Lawton A, et al (2014). Matrix metalloproteinase-10 promotes tumor progression through regulation of angiogenic and apoptotic pathways in cervical tumors. BMC Cancer, 14, 310. https://doi.org/10.1186/1471-2407-14-310