Tissue engineered humanized bone supports human hematopoiesis in vivo

Biomaterials

Volumn 61, Issue , 2015, Pages 103-114

  Holzapfel, Boris M ^a,b   Hutmacher, Dietmar W ^a,c,d   Nowlan, Bianca ^e   Barbier, Valerie ^e   Thibaudeau, Laure ^a   Theodoropoulos, Christina ^a   Hooper, John D ^f   Loessner, Daniela ^a   Clements, Judith A ^f   Russell, Pamela J ^a,f   Pettit, Allison R ^e   Winkler, Ingrid G ^e   Levesque, Jean Pierre ^e  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f TRANSLATIONAL RESEARCH INSTITUTE   (Australia)

Author keywords

Bone organ; Engraftment; Hematopoietic stem cells; Humanized niche; Tissue Engineering; Transplantation

Indexed keywords

CELL ENGINEERING; CYTOLOGY; SCAFFOLDS (BIOLOGY); STEM CELLS; TISSUE ENGINEERING; TRANSPLANTATION (SURGICAL);

BIODEGRADABLE COMPOSITES; BIOLOGICAL FUNCTIONS; ENGRAFTMENT; HEMATOPOIETIC STEM CELLS; HUMAN MESENCHYMAL CELLS; HUMANIZED NICHE; MESENCHYMAL PROGENITOR CELLS; MORPHOLOGICAL FEATURES;

TISSUE;

COLLAGEN TYPE 1; OSTEOCALCIN; SCLEROPROTEIN; VON WILLEBRAND FACTOR; BONE PROSTHESIS;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE; BONE DENSITY; BONE MARROW CELL; BONE MATRIX; CELL DIFFERENTIATION; CONTROLLED STUDY; ERYTHROCYTE; FEMALE; FLOW CYTOMETRY; GRANULOCYTE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LYMPHOCYTE; MEGAKARYOCYTE; MESENCHYMAL STEM CELL; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCYTE; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; STEM CELL NICHE; TISSUE ENGINEERING; ANIMAL; BIOARTIFICIAL ORGAN; BONE DEVELOPMENT; BONE PROSTHESIS; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DEVICE FAILURE ANALYSIS; DEVICES; EQUIPMENT DESIGN; MESENCHYMAL STROMA CELL; PHYSIOLOGY; PROCEDURES; SYNTHESIS; TISSUE SCAFFOLD;

ANIMALS; BIOARTIFICIAL ORGANS; BONE DEVELOPMENT; BONE SUBSTITUTES; CELL DIFFERENTIATION; CELLS, CULTURED; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; FEMALE; HEMATOPOIESIS; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; OSTEOBLASTS; OSTEOGENESIS; STEM CELL NICHE; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84939131102     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.04.057     Document Type: Article

References (43)

1. Levesque J.P., Helwani F.M., Winkler I.G. The endosteal 'osteoblastic' niche and its role in hematopoietic stem cell homing and mobilization. Leukemia 2010, 24:1979-1992.
2. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978, 4:7-25.
3. Gong J.K. Endosteal marrow: a rich source of hematopoietic stem cells. Science 1978, 199:1443-1445.
4. Zhang J., Niu C., Ye L., Huang H., He X., Tong W.G., et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003, 425:836-841.
5. Ding L., Morrison S.J. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013, 495:231-235.
6. Greenbaum A., Hsu Y.M., Day R.B., Schuettpelz L.G., Christopher M.J., Borgerding J.N., et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013, 495:227-230.
7. Kiel M.J., Yilmaz O.H., Iwashita T., Terhorst C., Morrison S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005, 121:1109-1121.
8. Nakamura-Ishizu A., Suda T. Hematopoietic stem cell niche: an interplay among a repertoire of multiple functional niches. Biochim. Biophys. Acta 2013, 1830:2404-2409.
9. Karnoub A.E., Dash A.B., Vo A.P., Sullivan A., Brooks M.W., Bell G.W., et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007, 449:557-563.
10. Lane S.W., Scadden D.T., Gilliland D.G. The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood 2009, 114:1150-1157.
11. Camacho D.F., Pienta K.J. A multi-targeted approach to treating bone metastases. Cancer Metastasis Rev. 2014, 33:545-553.
12. Krebsbach P.H., Kuznetsov S.A., Satomura K., Emmons R.V., Rowe D.W., Robey P.G. Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 1997, 63:1059-1069.
13. Kuznetsov S.A., Krebsbach P.H., Satomura K., Kerr J., Riminucci M., Benayahu D., et al. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J. Bone Min. Res. 1997, 12:1335-1347.
14. Miura Y., Gao Z., Miura M., Seo B.M., Sonoyama W., Chen W., et al. Mesenchymal stem cell-organized bone marrow elements: an alternative hematopoietic progenitor resource. Stem Cells 2006, 24:2428-2436.
15. Sacchetti B., Funari A., Michienzi S., Di Cesare S., Piersanti S., Saggio I., et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007, 131:324-336.
16. Scotti C., Piccinini E., Takizawa H., Todorov A., Bourgine P., Papadimitropoulos A., et al. Engineering of a functional bone organ through endochondral ossification. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:3997-4002.
17. Song J., Kiel M.J., Wang Z., Wang J., Taichman R.S., Morrison S.J., et al. An in vivo model to study and manipulate the hematopoietic stem cell niche. Blood 2010, 115:2592-2600.
18. Groen R.W., Noort W.A., Raymakers R.A., Prins H.J., Aalders L., Hofhuis F.M., et al. Reconstructing the human hematopoietic niche in immunodeficient mice: opportunities for studying primary multiple myeloma. Blood 2012, 120:e9-e16.
19. Lee J., Li M., Milwid J., Dunham J., Vinegoni C., Gorbatov R., et al. Implantable microenvironments to attract hematopoietic stem/cancer cells. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:19638-19643.
20. Torisawa Y.S., Spina C.S., Mammoto T., Mammoto A., Weaver J.C., Tat T., et al. Bone marrow-on-a-chip replicates hematopoietic niche physiology in vitro. Nat. Methods 2014, 11:663-669.
21. Holzapfel B.M., Thibaudeau L., Hesami P., Taubenberger A., Holzapfel N.P., Mayer-Wagner S., et al. Humanised xenograft models of bone metastasis revisited: novel insights into species-specific mechanisms of cancer cell osteotropism. Cancer Metastasis Rev. 2013, 32:129-145.
22. Thibaudeau L., Quent V.M., Holzapfel B.M., Taubenberger A.V., Straub M., Hutmacher D.W. Mimicking breast cancer-induced bone metastasis in vivo: current transplantation models and advanced humanized strategies. Cancer Metastasis Rev. 2014, 33:721-735.
23. Brown T.D., Slotosch A., Thibaudeau L., Taubenberger A., Loessner D., Vaquette C., et al. Design and fabrication of tubular scaffolds via direct writing in a melt electrospinning mode. Biointerphases 2012, 7:13.
24. Holzapfel B.M., Wagner F., Loessner D., Holzapfel N.P., Thibaudeau L., Crawford R., et al. Species-specific homing mechanisms of human prostate cancer metastasis in tissue engineered bone. Biomaterials 2014, 35:4108-4115.
25. Vaquette C., Ivanovski S., Hamlet S.M., Hutmacher D.W. Effect of culture conditions and calcium phosphate coating on ectopic bone formation. Biomaterials 2013, 34:5538-5551.
26. Reichert J.C., Quent V.M., Burke L.J., Stansfield S.H., Clements J.A., Hutmacher D.W. Mineralized human primary osteoblast matrices as a model system to analyse interactions of prostate cancer cells with the bone microenvironment. Biomaterials 2010, 31:7928-7936.
27. Hesami P., Holzapfel B., Taubenberger A., Roudier M., Fazli L., Sieh S., et al. A humanized tissue-engineered in vivo model to dissect interactions between human prostate cancer cells and human bone. Clin. Exp. Metastasis 2014, 31:1-12.
28. Barbier V., Winkler I.G., Levesque J.P. Mobilization of hematopoietic stem cells by depleting bone marrow macrophages. Methods Mol. Biol. 2012, 904:117-138.
29. Bolland B.J., Kanczler J.M., Dunlop D.G., Oreffo R.O. Development of in vivo muCT evaluation of neovascularisation in tissue engineered bone constructs. Bone 2008, 43:195-202.
30. Haas A.R., Tuan R.S. Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: II. Stimulation by bone morphogenetic protein-2 requires modulation of N-cadherin expression and function. Differentiation 1999, 64:77-89.
31. Feng J.Q., Ward L.M., Liu S., Lu Y., Xie Y., Yuan B., et al. Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat. Genet. 2006, 38:1310-1315.
32. Purton L.E., Scadden D.T. Limiting factors in murine hematopoietic stem cell assays. Cell. Stem Cell. 2007, 1:263-270.
33. Winkler I.G., Pettit A.R., Raggatt L.J., Jacobsen R.N., Forristal C.E., Barbier V., et al. Hematopoietic stem cell mobilizing agents G-CSF, cyclophosphamide or AMD3100 have distinct mechanisms of action on bone marrow HSC niches and bone formation. Leukemia 2012, 26:1594-1601.
34. Shultz L.D., Lyons B.L., Burzenski L.M., Gott B., Chen X., Chaleff S., et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 2005, 174:6477-6489.
35. Winkler I.G., Barbier V., Wadley R., Zannettino A.C., Williams S., Levesque J.P. Positioning of bone marrow hematopoietic and stromal cells relative to blood flow in vivo: serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches. Blood 2010, 116:375-385.
36. Loessner D., Holzapfel B.M., Clements J.A. Engineered microenvironments provide new insights into ovarian and prostate cancer progression and drug responses. Adv. Drug Deliv. Rev. 2014, 79-80:193-213.
37. Rongvaux A., Takizawa H., Strowig T., Willinger T., Eynon E.E., Flavell R.A., et al. Human hemato-lymphoid system mice: current use and future potential for medicine. Annu Rev. Immunol. 2013, 31:635-674.
38. Ooi L.L., Zheng Y., Stalgis-Bilinski K., Dunstan C.R. The bone remodeling environment is a factor in breast cancer bone metastasis. Bone 2011, 48:66-70.
39. Mastro A.M., Gay C.V., Welch D.R. The skeleton as a unique environment for breast cancer cells. Clin. Exp. Metastasis 2003, 20:275-284.
40. Schneider J.G., Amend S.R., Weilbaecher K.N. Integrins and bone metastasis: integrating tumor cell and stromal cell interactions. Bone 2011, 48:54-65.
41. Thibaudeau L., Taubenberger A.V., Theodoropoulos C., Holzapfel B.M., Ramuz O., Straub M., et al. New mechanistic insights of integrin beta1 in breast cancer bone colonization. Oncotarget 2015, 6:332-344.
42. Auffray I., Dubart A., Izac B., Vainchenker W., Coulombel L. A murine stromal cell line promotes the proliferation of the human factor-dependent leukemic cell line UT-7. Exp. Hematol. 1994, 22:417-424.
43. Jiang X., Gurel O., Mendiaz E.A., Stearns G.W., Clogston C.L., Lu H.S., et al. Structure of the active core of human stem cell factor and analysis of binding to its receptor kit. Embo J. 2000, 19:3192-3203.