Bone marrow-derived myofibroblasts are the providers of pro-invasive matrix metalloproteinase 13 in primary tumor

Neoplasia (United States)

Volumn 14, Issue 10, 2012, Pages 943-951

  Lecomte, Julie ^a   Masset, Anne ^a   Blacher, Silvia ^a   Maertens, Ludovic ^a   Gothot, André ^a   Delgaudine, Marie ^a   Bruyère, Françoise ^b   Carnet, Oriane ^a   Paupert, Jenny ^a   Illemann, Martin ^c,d,e   Foidart, Jean Michel ^a   Lund, Ida K ^c,d   Høyer Hansen, Gunilla ^c,d   Noel, Agnes ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c FINSEN LABORATORY   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGENASE 3; MESSENGER RNA; PROTEOCHONDROITIN SULFATE; THY 1 ANTIGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CANCER INVASION; CELL INFILTRATION; CELL MIGRATION; COLONY FORMING UNIT; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MESENCHYMAL STEM CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 84867778212     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.121092     Document Type: Article

References (51)

1. Joyce JA and Pollard JW (2009). Microenvironmental regulation of metastasis. Nat Rev Cancer 9, 239-252.
2. Hanahan D and Weinberg RA (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
3. Carmeliet P and Jain RK (2011). Molecular mechanisms and clinical applications of angiogenesis. Nature 473, 298-307.
4. De Wever O, Demetter P, Mareel M, and Bracke M (2008). Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 123, 2229-2238.
5. Franco OE, Shaw AK, Strand DW, and Hayward SW (2010). Cancer associated fibroblasts in cancer pathogenesis. Semin Cell Dev Biol 21, 33-39.
6. Kalluri R and Zeisberg M (2006). Fibroblasts in cancer. Nat Rev Cancer 6, 392-401.
7. Tripathi M, Billet S, and Bhowmick NA (2012). Understanding the role of stromal fibroblasts in cancer progression. Cell Adh Migr 6, 231-235.
8. Kalluri R (2009). EMT: when epithelial cells decide to become mesenchymallike cells. J Clin Invest 119, 1417-1419.
9. Wels J, Kaplan RN, Rafii S, and Lyden D (2008). Migratory neighbors and distant invaders: tumor-associated niche cells. Genes Dev 22, 559-574.
10. Zhu W, Xu W, Jiang R, Qian H, Chen M, Hu J, Cao W, Han C, and Chen Y (2006). Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp Mol Pathol 80, 267-274.
11. Kidd S, Spaeth E, Dembinski JL, Dietrich M, Watson K, Klopp A, Battula VL, Weil M, Andreeff M, and Marini FC (2009). Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem Cells 27, 2614-2623.
12. De Boeck A, Pauwels P, Hensen K, Rummens JL, Westbroek W, Hendrix A, Maynard D, Denys H, Lambein K, Braems G, et al. (2012). Bone marrowderived mesenchymal stem cells promote colorectal cancer progression through paracrine neuregulin 1/HER3 signalling. Gut, E-pub ahead of print.
13. Mishra PJ, Mishra PJ, Humeniuk R, Medina DJ, Alexe G, Mesirov JP, Ganesan S, Glod JW, and Banerjee D (2008). Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res 68, 4331-4339.
14. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, and Weinberg RA (2007). Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449, 557-563.
15. Beacham DA and Cukierman E (2005). Stromagenesis: the changing face of fibroblastic microenvironments during tumor progression. Semin Cancer Biol 15, 329-341.
16. Noel A, Jost M, and Maquoi E (2008). Matrix metalloproteinases at cancer tumor-host interface. Semin Cell Dev Biol 19, 52-60.
17. Aimes RT and Quigley JP (1995). Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4-and 1/4-length fragments. J Biol Chem 270, 5872-5876.
18. Holmbeck K, Bianco P, Yamada S, and Birkedal-Hansen H (2004). MT1-MMP: a tethered collagenase. J Cell Physiol 200, 11-19.
19. Balbin M, Fueyo A, Tester AM, Pendas AM, Pitiot AS, Astudillo A, Overall CM, Shapiro SD, and Lopez-Otin C (2003). Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat Genet 35, 252-257.
20. Ala-aho R and Kahari VM (2005). Collagenases in cancer. Biochimie 87, 273-286.
21. Freije JM, Diez-Itza I, Balbin M, Sanchez LM, Blasco R, Tolivia J, and Lopez-Otin C (1994). Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 269, 16766-16773.
22. Airola K, Johansson N, Kariniemi AL, Kahari VM, and Saarialho-Kere UK (1997). Human collagenase-3 is expressed in malignant squamous epithelium of the skin. J Invest Dermatol 109, 225-231.
23. Nielsen BS, Rank F, Lopez JM, Balbin M, Vizoso F, Lund LR, Dano K, and Lopez-Otin C (2001). Collagenase-3 expression in breast myofibroblasts as a molecular marker of transition of ductal carcinoma in situ lesions to invasive ductal carcinomas. Cancer Res 61, 7091-7100.
24. Johansson N, Vaalamo M, Grenman S, Hietanen S, Klemi P, Saarialho-Kere U, and Kahari VM (1999). Collagenase-3 (MMP-13) is expressed by tumor cells in invasive vulvar squamous cell carcinomas. Am J Pathol 154, 469-480.
25. Airola K, Karonen T, Vaalamo M, Lehti K, Lohi J, Kariniemi AL, Keski-Oja J, and Saarialho-Kere UK (1999). Expression of collagenases-1 and -3 and their inhibitors TIMP-1 and -3 correlates with the level of invasion in malignant melanomas. Br J Cancer 80, 733-743.
26. Pendas AM, Uria JA, Jimenez MG, Balbin M, Freije JP, and Lopez-Otin C (2000). An overview of collagenase-3 expression in malignant tumors and analysis of its potential value as a target in antitumor therapies. Clin Chim Acta 291, 137-155.
27. Lafleur MA, Drew AF, de Sousa EL, Blick T, Bills M, Walker EC, Williams ED, Waltham M, and Thompson EW (2005). Upregulation of matrix metalloproteinases (MMPs) in breast cancer xenografts: a major induction of stromal MMP-13. Int J Cancer 114, 544-554.
28. Nielsen BS, Egeblad M, Rank F, Askautrud HA, Pennington CJ, Pedersen TX, Christensen IJ, Edwards DR, Werb Z, and Lund LR (2008). Matrix metalloproteinase 13 is induced in fibroblasts in polyomavirus middle T antigen-driven mammary carcinoma without influencing tumor progression. PLoS One 3, e2959.
29. Lederle W, Hartenstein B, Meides A, Kunzelmann H, Werb Z, Angel P, and Mueller MM (2010). MMP13 as a stromal mediator in controlling persistent angiogenesis in skin carcinoma. Carcinogenesis 31, 1175-1184.
30. Lecomte J, Louis K, Detry B, Blacher S, Lambert V, Bekaert S, Munaut C, Paupert J, Blaise P, Foidart JM, et al. (2011). Bone marrow-derived mesenchymal cells and MMP13 contribute to experimental choroidal neovascularization. Cell Mol Life Sci 68, 677-686.
31. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, Lopez-Otin C, and Krane SM (2004). Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci USA 101, 17192-17197.
32. Brouard N, Driessen R, Short B, and Simmons PJ (2010). G-CSF increases mesenchymal precursor cell numbers in the bone marrow via an indirect mechanism involving osteoclast-mediated bone resorption. Stem Cell Res 5, 65-75.
33. Fusenig NE, Amer SM, Boukamp P, and Worst PK (1978). Characteristics of chemically transformed mouse epidermal cells in vitro and in vivo. Bull Cancer 65, 271-279.
34. Lund LR, Romer J, Bugge TH, Nielsen BS, Frandsen TL, Degen JL, Stephens RW, and Dano K (1999). Functional overlap between two classes of matrixdegrading proteases in wound healing. EMBO J 18, 4645-4656.
35. Lund IK, Illemann M, Thurison T, Christensen IJ, and Hoyer-Hansen G (2011). uPAR as anti-cancer target: evaluation of biomarker potential, histological localization, and antibody-based therapy. Curr Drug Targets 12, 1744-1760.
36. Illemann M, Bird N, Majeed A, Laerum OD, Lund LR, Dano K, and Nielsen BS (2009). Two distinct expression patterns of urokinase, urokinase receptor and plasminogen activator inhibitor-1 in colon cancer liver metastases. Int J Cancer 124, 1860-1870.
37. Bisson C, Blacher S, Polette M, Blanc JF, Kebers F, Desreux J, Tetu B, Rosenbaum J, Foidart JM, Birembaut P, et al. (2003). Restricted expression of membrane type 1-matrix metalloproteinase by myofibroblasts adjacent to human breast cancer cells. Int J Cancer 105, 7-13.
38. Eccles SA, Box GM, Court WJ, Bone EA, Thomas W, and Brown PD (1996). Control of lymphatic and hematogenous metastasis of a rat mammary carcinoma by the matrix metalloproteinase inhibitor batimastat (BB-94). Cancer Res 56, 2815-2822.
39. Wang SS, Asfaha S, Okumura T, Betz KS, Muthupalani S, Rogers AB, Tu S, Takaishi S, Jin G, Yang X, et al. (2009). Fibroblastic colony-forming unit bone marrow cells delay progression to gastric dysplasia in a helicobacter model of gastric tumorigenesis. Stem Cells 27, 2301-2311.
40. Quante M, Tu SP, Tomita H, Gonda T, Wang SS, Takashi S, Baik GH, Shibata W, Diprete B, Betz KS, et al. (2011). Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 19, 257-272.
41. Studeny M, Marini FC, Dembinski JL, Zompetta C, Cabreira-Hansen M, Bekele BN, Champlin RE, and Andreeff M (2004). Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst 96, 1593-1603.
42. McAllister SS and Weinberg RA (2010). Tumor-host interactions: a far-reaching relationship. J Clin Oncol 28, 4022-4028.
43. Simmons PJ, Przepiorka D, Thomas ED, and Torok-Storb B (1987). Host origin of marrow stromal cells following allogeneic bone marrow transplantation. Nature 328, 429-432.
44. Yokota T, Kawakami Y, Nagai Y, Ma JX, Tsai JY, Kincade PW, and Sato S (2006). Bone marrow lacks a transplantable progenitor for smooth muscle type alpha-actin-expressing cells. Stem Cells 24, 13-22.
45. Direkze NC, Hodivala-Dilke K, Jeffery R, Hunt T, Poulsom R, Oukrif D, Alison MR, and Wright NA (2004). Bone marrow contribution to tumorassociated myofibroblasts and fibroblasts. Cancer Res 64, 8492-8495.
46. Guo X, Oshima H, Kitmura T, Taketo MM, and Oshima M (2008). Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J Biol Chem 283, 19864-19871.
47. Jeon ES, Moon HJ, Lee MJ, Song HY, Kim YM, Cho M, Suh DS, Yoon MS, Chang CL, Jung JS, et al. (2008). Cancer-derived lysophosphatidic acid stimulates differentiation of human mesenchymal stem cells to myofibroblast-like cells. Stem Cells 26, 789-797.
48. Zhou Y, Hagood JS, and Murphy-Ullrich JE (2004). Thy-1 expression regulates the ability of rat lung fibroblasts to activate transforming growth factor-beta in response to fibrogenic stimuli. Am J Pathol 165, 659-669.
49. Hagood JS, Prabhakaran P, Kumbla P, Salazar L, MacEwen MW, Barker TH, Ortiz LA, Schoeb T, Siegal GP, Alexander CB, et al. (2005). Loss of fibroblast Thy-1 expression correlates with lung fibrogenesis. Am J Pathol 167, 365-379.
50. Zigrino P, Kuhn I, Bauerle T, Zamek J, Fox JW, Neumann S, Licht A, Schorpp-Kistner M, Angel P, and Mauch C (2009). Stromal expression of MMP-13 is required for melanoma invasion and metastasis. J Invest Dermatol 129, 2686-2693.
51. Toriseva MJ, Ala-aho R, Karvinen J, Baker AH, Marjomaki VS, Heino J, and Kahari VM (2007). Collagenase-3 (MMP-13) enhances remodeling of threedimensional collagen and promotes survival of human skin fibroblasts. J Invest Dermatol 127, 49-59.