Bone marrow cells as precursors of the tumor stroma

Experimental Cell Research

Volumn 319, Issue 11, 2013, Pages 1650-1656

  Worthley, Daniel L ^a   Si, Yiling ^a   Quante, Michael ^b   Churchill, Michael ^a   Mukherjee, Siddhartha ^a   Wang, Timothy C ^a  

^a Columbia University ^*  (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cancer; Carcinogenesis; Fibroblasts; Mesenchyme; Tumor microenvironment

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ADAM12 PROTEIN; ALPHA SMOOTH MUSCLE ACTIN; BONE MORPHOGENETIC PROTEIN 4; CALVASCULIN; COLLAGEN TYPE 10; DNA METHYLTRANSFERASE 1; FIBROBLAST ASSOCIATED ANTIGEN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN; SEPRASE; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; VIMENTIN;

ADJUVANT CHEMOTHERAPY; BONE DEVELOPMENT; BONE MARROW CELL; CANCER ASSOCIATED FIBROBLAST; CANCER PREVENTION; CANCER PROGNOSIS; CANCER THERAPY; CARCINOGENESIS; CELL DIFFERENTIATION; DNA METHYLATION; FIBROBLAST; HEMATOPOIESIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR MICROENVIRONMENT; VASCULAR SMOOTH MUSCLE;

CANCER; CARCINOGENESIS; FIBROBLASTS; MESENCHYME; TUMOR MICROENVIRONMENT;

ANIMALS; BONE MARROW CELLS; CELL TRANSFORMATION, NEOPLASTIC; FIBROBLASTS; HUMANS; NEOPLASMS; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 84879605585     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.03.006     Document Type: Review

References (66)

1. Quante M., Tu S.P., Tomita H., Gonda T., Wang S.S.W., Takashi S., et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011, 19(2):257-272.
2. Rhim A.D., Mirek E.T., Aiello N.M., Maitra A., Bailey J.M., McAllister F., et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012, 148(1-2):349-361.
3. Glaire M.A., El-Omar E.M., Wang T.C., Worthley D.L. The mesenchyme in malignancy: a partner in the initiation, progression and dissemination of cancer. Pharmacol. Ther. 2012, 1-11. Available from: 〈http://www.sciencedirect.com/science/article/pii/S0163725812001684〉.
4. Kidd S.S., Spaeth E.E., Watson K.K., Burks J.J., Lu H.H., Klopp A.A., et al. Origins of the tumor microenvironment: quantitative assessment of adipose-derived and bone marrow-derived stroma. PLoS One 2012, 7(2):e30563.
5. Worthley D.L., Ruszkiewicz A., Davies R. Human gastrointestinal neoplasia-associated myofibroblasts can develop from bone marrow-derived cells following allogeneic stem cell transplantation. STEM 2009, 27(6):1463-1468.
6. Morikawa S., Mabuchi Y., Kubota Y., Nagai Y., Niibe K., Hiratsu E., et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med. 2009, 206(11):2483-2496.
7. Park D., Spencer J.A., Koh B.I., Kobayashi T., Fujisaki J., Clemens T.L., et al. Endogenous bone marrow mscs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 2012, 10(3):259-272. Available from: 〈http://www.sciencedirect.com/science/MiamiMultiMediaURL/1-s2.0-S1934590912000616/1-s2.0-S1934590912000616-mmc1.pdf/274143/html/S1934590912000616/a8a097a61f5203f937c5f6c1068743a5/mmc1.pdf〉.
8. Hoggatt J., Scadden D.T. The stem cell niche: tissue physiology at a single cell level. J. Clin. Invest. 2012, 122(9):3029-3034.
9. Mendez-Ferrer S., Michurina T.V., Ferraro F., Mazloom A.R., MacArthur B.D., Lira S.A., et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010, 466(7308):829-834.
10. Ding L., Saunders T.L., Enikolopov G., Morrison S.J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012, 481(7382):457-462.
11. Caplan A.I. All MSCs are pericytes?. Cell Stem Cell 2008, 3(3):229-230.
12. Crisan M., Yap S., Casteilla L., Chen C.-W., Corselli M., Park T.S., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3(3):301-313.
13. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 2006, 8(4):315-317.
14. Shen J., Tsai Y.-T., Dimarco N.M., Long M.A., Sun X., Tang L. Transplantation of mesenchymal stem cells from young donors delays aging in mice. Sci. Rep. 2011, 1:67.
15. Grcevic D., Pejda S., Matthews B.G., Repic D., Wang L., Li H., et al. In vivo fate mapping identifies mesenchymal progenitor cells. Stem Cells 2012, 30(2):187-196.
16. Powell D.W., Pinchuk I.V., Saada J.I., Chen X., Mifflin R.C. Mesenchymal cells of the intestinal lamina propria. Annu. Rev. Physiol. 2011, 73:213-237.
17. Medema J.P., Vermeulen L. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature 2011, 474(7351):318-326.
18. Manieri N.A., Drylewicz M.R., Miyoshi H., Stappenbeck T.S. Igf2bp1 is required for full induction of Ptgs2 mRNA in colonic mesenchymal stem cells in mice. Gastroenterology 2012, 143(1):110-121.
19. Stappenbeck T.S., Miyoshi H. The role of stromal stem cells in tissue regeneration and wound repair. Science 2009, 324(5935):1666-1669.
20. Powell D.W., Saada J.I. Mesenchymal stem cells and prostaglandins may be critical for intestinal wound repair. Gastroenterology 2012, 143(1):19-22.
21. J.B. Sneddon, H.H. Zhen, K. Montgomery, M. van de Rijn, A.D. Tward, R. West, et al., Bone morphogenetic protein antagonist gremlin 1 is widely expressed by cancer-associated stromal cells and can promote tumor cell proliferation, in: Proceedings of the National Academy of Sciences of the United States of America. October 3 2006, 103(40) 14842-14847.
22. Mishra P.J., Mishra P.J., Humeniuk R., Medina D.J., Alexe G., Mesirov J.P., et al. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res. 2008, 68(11):4331-4339.
23. Kraman M., Bambrough P.J., Arnold J.N., Roberts E.W., Magiera L., Jones J.O., et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-a. Science 2010, 330(6005):827-830.
24. Orimo A., Weinberg R.A. Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 2006, 5(15):1597-1601.
25. Orimo A., Weinberg R.A. Heterogeneity of stromal fibroblasts in tumors. Cancer Biol. Ther. 2007, 6(4):618-619.
26. C.H. Österreicher, M. Penz-Österreicher, S.I. Grivennikov, M. Guma, E.K. Koltsova, C. Datz, et al., Fibroblast-specific protein 1 identifies an inflammatory subpopulation of macrophages in the liver, in: Proceedings of the National Academy of Sciences of the United States of America, January 4 2011 108(1) 308-313.
27. Jiang L., Gonda T.A., Gamble M.V., Salas M., Seshan V., Tu S., et al. Global hypomethylation of genomic DNA in cancer-associated myofibroblasts. Cancer Res. 2008, 68(23):9900-9908.
28. Erez N., Truitt M., Olson P., Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-[kappa]B-dependent manner. Cancer Cell 2010, 17(2):135-147.
29. Visvader J.E., Lindeman G.J. Cancer stem cells: current status and evolving complexities. STEM 2012, 10(6):717-728.
30. Dulauroy S., Di Carlo S.E., Langa F., Eberl G., Peduto L. Lineage tracing and genetic ablation of ADAM12(+) perivascular cells identify a major source of profibrotic cells during acute tissue injury. Nat. Med. 2012, 18:1262-1270. 10.1038/nm.2848.
31. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423(6937):332-336.
32. McLin V.A., Henning S.J., Jamrich M. The role of the visceral mesoderm in the development of the gastrointestinal tract. Gastroenterology 2009, 136(7):2074-2091.
33. Wilm B., Ipenberg A., Hastie N.D., Burch J.B.E., Bader D.M. The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 2005, 132(23):5317-5328.
34. Miyoshi H., Ajima R., Luo C.T., Yamaguchi T.P., Stappenbeck T.S. Wnt5a potentiates TGF-β signaling to promote colonic crypt regeneration after tissue injury. Science 2012, 338(6103):108-113.
35. Takashima Y., Era T., Nakao K., Kondo S., Kasuga M., Smith A.G., et al. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 2007, 129(7):1377-1388.
36. Direkze N.C., Hodivala-Dilke K., Jeffery R., Hunt T., Poulsom R., Oukrif D., et al. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res. 2004, 64(23):8492-8495.
37. Kalluri R.R., Zeisberg M.M. Fibroblasts in cancer. Nat Rev Cancer 2006, 6(5):392-401. Available from: 〈http://pubget.com/paper/16572188?institution=columbia.edu〉.
38. Guo X., Oshima H., Kitmura T., Taketo M.M., Oshima M. Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J. Biol. Chem. 2008, 283(28):19864-19871.
39. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438(7069):820-827.
40. J.T. O'Connell, H. Sugimoto, V.G. Cooke, B.A. MacDonald, A.I. Mehta, V.S. LeBleu, et al., VEGF-A and tenascin-C produced by S100A4+ stromal cells are important for metastatic colonization, in: Proceedings of the National Academy of Sciences of the United States of America, September 20 2011 108(38) 16002-16007.
41. Peng H., Herzog E.L. Fibrocytes: emerging effector cells in chronic inflammation. Curr. Opin. Pharmacol. 2012, 12:1-6.
42. Ebihara Y.Y., Masuya M.M., Larue A.C.A., Fleming P.A.P., Visconti R.P.R., Minamiguchi H.H., et al. Hematopoietic origins of fibroblasts: II. In vitro studies of fibroblasts, CFU-F, and fibrocytes. Exp. Hematol. 2006, 34:219-229.
43. Shibata W., Ariyama H., Westphalen C.B., Worthley D.L., Muthupalani S., Asfaha S., et al. Stromal cell-derived factor-1 overexpression induces gastric dysplasia through expansion of stromal myofibroblasts and epithelial progenitors. Gut 2012, 62(2):192-200.
44. Hu B., Gharaee-Kermani M., Wu Z., Phan S.H. Epigenetic regulation of myofibroblast differentiation by DNA methylation. Am. J. Pathol. 2010, 177(1):21-28.
45. Yauch R.L., Gould S.E., Scales S.J., Tang T., Tian H., Ahn C.P., et al. A paracrine requirement for hedgehog signalling in cancer. Nature 2008, 455(7211):406-410.
46. Nik A.M., Reyahi A., Ponten F., Carlsson P. Foxf2 in intestinal fibroblasts reduces numbers of Lgr5+ stem cells and adenoma formation by inhibiting Wnt signaling. Gastroenterology 2013, 24:1-30.
47. Vokes S.A., Ji H., Wong W.H., McMahon A.P. A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev. 2008, 22(19):2651-2663.
48. Shaw A., Gipp J., Bushman W. Exploration of Shh and BMP paracrine signaling in a prostate cancer xenograft. Differentiation 2010, 79(1):41-47.
49. Scheel C., Eaton E.N., SH-J Li, Chaffer C.L., Reinhardt F., Kah K.-J., et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011, 145(6):926-940.
50. Straussman R., Morikawa T., Shee K., Barzily-Rokni M., Qian Z.R., Du J., et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nat. Cell Biol. 2012, 4.
51. Kaplan R.N., Rafii S., Lyden D. Preparing the soil: the premetastatic niche. Cancer research. AACR 2006, 66(23):11089-11093.
52. Peinado H., Alečković M., Lavotshkin S., Matei I., Costa-Silva B., Moreno-Bueno G., et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 2012, 18(6):883-891. Available from: 〈http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=22635005&retmode=ref&cmd=prlinks〉.
53. Olumi A.F., Grossfeld G.D., Hayward S.W., Carroll P.R., Tlsty T.D., Cunha G.R. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res. 1999, 59(19):5002-5011.
54. Adegboyega P.A., Ololade O., Saada J., Mifflin R., Di Mari J.F., Powell D.W. Subepithelial myofibroblasts express cyclooxygenase-2 in colorectal tubular adenomas. Clin. Cancer Res. 2004, 10(17):5870-5879.
55. Saada J.I., Pinchuk I.V., Barrera C.A., Adegboyega P.A., Suarez G., Mifflin R.C., et al. Subepithelial myofibroblasts are novel nonprofessional APCs in the human colonic mucosa. J. Immunol. 2006, 177(9):5968-5979.
56. Adegboyega P.A., Mifflin R.C., DiMari J.F., Saada J.I., Powell D.W. Immunohistochemical study of myofibroblasts in normal colonic mucosa, hyperplastic polyps, and adenomatous colorectal polyps. Arch. Pathol. Lab. Med. 2002, 126(7):829-836.
57. Bhowmick N.A., Neilson E.G., Moses H.L. Stromal fibroblasts in cancer initiation and progression. Nature 2004, 432(7015):332-337. Available from: 〈http://www.nature.com/doifinder/10.1038/nature03096〉.
58. Bhowmick N.A., Chytil A., Plieth D., Gorska A.E., Dumont N., Shappell S., et al. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004, 303(5659):848-851.
59. Trimboli A.J., Cantemir-Stone C.Z., Li F., Wallace J.A., Merchant A., Creasap N., et al. Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 2009, 461(7267):1084-1091. Available from: 〈http://www.nature.com/nature/journal/v461/n7267/abs/nature08486.html〉.
60. Olive K.P., Jacobetz M.A., Davidson C.J., Gopinathan A., McIntyre D., Honess D., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009, 324(5933):1457-1461. Available from: 〈http://stke.sciencemag.org/cgi/content/abstract/sci;324/5933/1457〉.
61. Nelson C.M., Bissell M.J. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 2006, 22:287-309.
62. DuFort C.C., Paszek M.J., Weaver V.M. Balancing forces: architectural control of mechanotransduction. Nat. Rev. Mol. Cell Biol. 2011, 12(5):308-319.
63. Gould A., Missailidis S. Targeting the hedgehog pathway: the development of cyclopamine and the development of anti-cancer drugs targeting the hedgehog pathway. Mini Rev. Med. Chem. 2011, 11(3):200-213.
64. D.V.T. Catenacci, N. Bahary, M.J. Edelman, S.R. Nattam, R. de Wilton Marsh, A. Kaubisch, et al., A phase IB/randomized phase II study of gemcitabine (G) plus placebo (P) or vismodegib (V), a hedgehog (Hh) pathway inhibitor, in patients (pts) with metastatic pancreatic cancer (PC): interim analysis of a University of Chicago phase II consortium study, ASCO Meeting Abstracts 2012 30(Suppl. 15) 4022.
65. V. Travaglione, C. Peacock, J. MacDougall, A novel HH pathway inhibitor, IPI-926, delays recurrence post-chemotherapy in a primary human SCLC xenograft model, AACR Meeting 2008.
66. Beatty G.L., Chiorean E.G., Fishman M.P., Saboury B., Teitelbaum U.R., Sun W., et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011, 331(6024):1612-1616.