Programmable 3D silk bone marrow niche for platelet generation ex vivo and modeling of megakaryopoiesis pathologies

Blood

Volumn 125, Issue 14, 2015, Pages 2254-2264

  Di Buduo, Christian A ^a,b   Wray, Lindsay S ^a,b,c   Tozzi, Lorenzo ^a,b,c   Malara, Alessandro ^a,b   Chen, Ying ^c   Ghezzi, Chiara E ^c   Smoot, Daniel ^c   Sfara, Carla ^d   Antonelli, Antonella ^d   Spedden, Elise ^e   Bruni, Giovanna ^a   Staii, Cristian ^e   De Marco, Luigi ^f,g   Magnani, Mauro ^d   Kaplan, David L ^c   Balduini, Alessandra ^a,b,c  

^a UNIVERSITY OF PAVIA   (Italy)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^c Tufts University   (United States)

^d UNIVERSITY OF URBINO   (Italy)

^e TUFTS UNIVERSITY   (United States)

^f CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

^g SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIAL; CYTOKINE; SILK;

ARTICLE; BIOCOMPATIBILITY; BIOENGINEERING; BLOOD COMPONENT; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; EX VIVO STUDY; EXTRACELLULAR MATRIX; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MODEL; PRIORITY JOURNAL; RIGIDITY; SHEAR STRENGTH; STEM CELL NICHE; SURFACE PROPERTY; THROMBOCYTE; THROMBOCYTOPOIESIS; TOPOGRAPHY; ADULT; ANIMAL; BOMBYX; BONE MARROW CELL; CELL CULTURE; CHEMISTRY; CYTOLOGY; FLOW CYTOMETRY; METABOLISM; MYELOID METAPLASIA; PATHOLOGY; PHYSIOLOGY; TISSUE ENGINEERING; TISSUE SCAFFOLD; VASCULAR ENDOTHELIUM;

ADULT; ANIMALS; BLOOD PLATELETS; BOMBYX; BONE MARROW CELLS; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELLS; HUMANS; MEGAKARYOCYTES; PRIMARY MYELOFIBROSIS; SILK; THROMBOPOIESIS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84926616230     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-08-595561     Document Type: Article

References (60)

1. DeZern AE, Sekeres MA. The challenging world of cytopenias: distinguishing myelodysplastic syndromes from other disorders of marrow failure. Oncologist. 2014;19(7):735-745.
2. Pallotta I, Lovett M, Kaplan DL, Balduini A. Three-dimensional system for the in vitro study of megakaryocytes and functional platelet production using silk-based vascular tubes. Tissue Eng Part C Methods. 2011;17(12):1223-1232.
3. Torisawa YS, Spina CS, Mammoto T, et al. Bone marrow-on-a-chip replicates hematopoietic niche physiology in vitro. Nat Methods. 2014;11(6):663-669.
4. Nakagawa Y, Nakamura S, Nakajima M, et al. Two differential flows in a bioreactor promoted platelet generation from human pluripotent stem cell-derived megakaryocytes. Exp Hematol. 2013;41(8):742-748.
5. Thon JN, Mazutis L, Wu S, et al. Platelet bioreactor-on-a-chip [published online ahead of print July 21, 2014. Blood., doi:10.1182/blood-2014-05-574913.
6. Morrison SJ, Scadden DT. The bone marrow niche for haematopoietic stem cells. Nature. 2014;505(7483):327-334.
7. Wang LD, Wagers AJ. Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat Rev Mol Cell Biol. 2011;12(10):643-655.
8. Inoue S, Osmond DG. Basement membrane of mouse bone marrow sinusoids shows distinctive structure and proteoglycan composition: a high resolution ultrastructural study. Anat Rec. 2001;264(3):294-304.
9. Ohta M, Sakai T, Saga Y, Aizawa S, Saito M. Suppression of hematopoietic activity in tenascin-C-deficient mice. Blood. 1998;91(11):4074-4083.
10. Jacenko O, Roberts DW, Campbell MR, McManus PM, Gress CJ, Tao Z. Linking hematopoiesis to endochondral skeletogenesis through analysis of mice transgenic for collagen X. Am J Pathol. 2002;160(6):2019-2034.
11. Winkler IG, Barbier V, Nowlan B, et al. Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat Med. 2012;18(11):1651-1657.
12. Rafii S, Shapiro F, Pettengell R, et al. Human bone marrow microvascular endothelial cells support long-term proliferation and differentiation of myeloid and megakaryocytic progenitors. Blood. 1995;86(9):3353-3363.
13. Avecilla ST, Hattori K, Heissig B, et al. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med. 2004;10(1):64-71.
14. Junt T, Schulze H, Chen Z, et al. Dynamic visualization of thrombopoiesis within bone marrow. Science. 2007;317(5845):1767-1770.
15. Vepari C, Kaplan DL. Silk as a Biomaterial. Prog Polym Sci. 2007;32(8-9):991-1007.
16. Lovett M, Cannizzaro C, Daheron L, Messmer B, Vunjak-Novakovic G, Kaplan DL. Silk fibroin microtubes for blood vessel engineering. Biomaterials. 2007;28(35):5271-5279.
17. Lawrence BD, Marchant JK, Pindrus MA, Omenetto FG, Kaplan DL. Silk film biomaterials for cornea tissue engineering. Biomaterials. 2009;30(7):1299-1308.
18. Rockwood DN, Preda RC, Yücel T, Wang X, Lovett ML, Kaplan DL. Materials fabrication from Bombyx mori silk fibroin. Nat Protoc. 2011;6(10):1612-1631.
19. Lovett ML, Cannizzaro CM, Vunjak-Novakovic G, Kaplan DL. Gel spinning of silk tubes for tissue engineering. Biomaterials. 2008;29(35):4650-4657.
20. Cox TR, Erler JT. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech. 2011;4(2):165-178.
21. Malara A, Gruppi C, Pallotta I, et al. Extracellular matrix structure and nano-mechanics determine megakaryocyte function. Blood. 2011;118(16):4449-4453.
22. Charras G, Sahai E. Physical influences of the extracellular environment on cell migration. Nat Rev Mol Cell Biol. 2014;15(12):813-824.
23. Balduini A, Pallotta I, Malara A, et al. Adhesive receptors, extracellular proteins and myosin IIA orchestrate proplatelet formation by human megakaryocytes. J Thromb Haemost. 2008;6(11):1900-1907.
24. Malara A, Gruppi C, Rebuzzini P, et al. Megakaryocyte-matrix interaction within bone marrow: new roles for fibronectin and factor XIII-A. Blood. 2011;117(8):2476-2483.
25. Lu Q, Wang X, Hu X, Cebe P, Omenetto F, Kaplan DL. Stabilization and release of enzymes from silk films. Macromol Biosci. 2010;10(4):359-368.
26. Gil ES, Panilaitis B, Bellas E, Kaplan DL. Functionalized silk biomaterials for wound healing. Adv Healthc Mater. 2013;2(1):206-217.
27. Malara A, Currao M, Gruppi C, et al. Megakaryocytes contribute to the bone marrowmatrix environment by expressing fibronectin, type IV collagen, and laminin. Stem Cells. 2014;32(4):926-937.
28. Ingram DA, Mead LE, Tanaka H, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104(9):2752-2760.
29. Thiele W, Krishnan J, Rothley M, et al. VEGFR-3 is expressed on megakaryocyte precursors in the murine bone marrow and plays a regulatory role in megakaryopoiesis. Blood. 2012;120(9):1899-1907.
30. Pitchford SC, Lodie T, Rankin SM. VEGFR1 stimulates a CXCR4-dependent translocation of megakaryocytes to the vascular niche, enhancing platelet production in mice. Blood. 2012;120(14):2787-2795.
31. Avraham H, Cowley S, Chi SY, Jiang S, Groopman JE. Characterization of adhesive interactions between human endothelial cells and megakaryocytes. J Clin Invest. 1993;91(6):2378-2384.
32. Cramer EM, Norol F, Guichard J, et al. Ultrastructure of platelet formation by human megakaryocytes cultured with the Mpl ligand. Blood. 1997;89(7):2336-2346.
33. Takayama N, Nishikii H, Usui J, et al. Generation of functional platelets from human embryonic stem cells in vitro via ES-sacs, VEGF-promoted structures that concentrate hematopoietic progenitors. Blood. 2008;111(11):5298-5306.
34. Nakamura S, Takayama N, Hirata S, et al. Expandable megakaryocyte cell lines enable clinically applicable generation of platelets from human induced pluripotent stem cells. Cell Stem Cell. 2014;14(4):535-548.
35. Mazo IB, von Andrian UH. Adhesion and homing of blood-borne cells in bone marrow microvessels. J Leukoc Biol. 1999;66(1):25-32.
36. Jiang J, Woulfe DS, Papoutsakis ET. Shear enhances thrombopoiesis and formation of microparticles that induce megakaryocytic differentiation of stem cells. Blood. 2014;124(13):2094-2103.
37. Mazzucato M, Cozzi MR, Battiston M, et al. Distinct spatio-temporal Ca21 signaling elicited by integrin alpha2beta1 and glycoprotein VI under flow. Blood. 2009;114(13):2793-2801.
38. Mazzucato M, Cozzi MR, Pradella P, Ruggeri ZM, De Marco L. Distinct roles of ADP receptors in von Willebrand factor-mediated platelet signaling and activation under high flow. Blood. 2004;104(10):3221-3227.
39. Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circ Res. 2007;100(12):1673-1685.
40. De Cuyper IM, Meinders M, van de Vijver E, et al. A novel flow cytometry-based platelet aggregation assay. Blood. 2013;121(10):e70-e80.
41. Tuszynski GP, Kornecki E, Cierniewski C, et al. Association of fibrin with the platelet cytoskeleton. J Biol Chem. 1984;259(8):5247-5254.
42. Rooney MM, Parise LV, Lord ST. Dissecting clot retraction and platelet aggregation. Clot retraction does not require an intact fibrinogen gamma chain C terminus. J Biol Chem. 1996;271(15):8553-8555.
43. Borges J, Mueller MC, Padron NT, Tegtmeier F, Lang EM, Stark GB. Engineered adipose tissue supplied by functional microvessels. Tissue Eng. 2003;9(6):1263-1270.
44. Wenger A, Stahl A, Weber H, et al. Modulation of in vitro angiogenesis in a three-dimensional spheroidal coculture model for bone tissue engineering. Tissue Eng. 2004;10(9-10):1536-1547.
45. Balduini A, Badalucco S, Pugliano MT, et al. In vitro megakaryocyte differentiation and proplatelet formation in Ph-negative classical myeloproliferative neoplasms: distinct patterns in the different clinical phenotypes. PLoS ONE. 2011;6(6):e21015.
46. Shin JW, Swift J, Spinler KR, Discher DE. Myosin-II inhibition and soft 2D matrix maximize multinucleation and cellular projections typical of platelet-producing megakaryocytes. Proc Natl Acad Sci USA. 2011;108(28):11458-11463.
47. Feng Q, Chai C, Jiang XS, Leong KW, Mao HQ. Expansion of engrafting human hematopoietic stem/progenitor cells in three-dimensional scaffolds with surface-immobilized fibronectin. J Biomed Mater Res A. 2006;78(4):781-791.
48. Dellatore SM, Garcia AS, Miller WM. Mimicking stem cell niches to increase stem cell expansion. Curr Opin Biotechnol. 2008;19(5):534-540.
49. Kim DH, Provenzano PP, Smith CL, Levchenko A. Matrix nanotopography as a regulator of cell function. J Cell Biol. 2012;197(3):351-360.
50. Zhang J, Pritchard E, Hu X, et al. Stabilization of vaccines and antibiotics in silk and eliminating the cold chain. Proc Natl Acad Sci USA. 2012;109(30):11981-11986.
51. Hamada T, Möhle R, Hesselgesser J, et al. Transendothelial migration of megakaryocytes in response to stromal cell-derived factor 1 (SDF-1) enhances platelet formation. J Exp Med. 1998;188(3):539-548.
52. Magnani M, Rossi L, Bianchi M, et al. Improved stability of 2, 3-bisphosphoglycerate during storage of hexokinase-overloaded erythrocytes. Biotechnol Appl Biochem. 1989;11(5):439-444.
53. Cabrales P, Tsai AG, Intaglietta M. Modulation of perfusion and oxygenation by red blood cell oxygen affinity during acute anemia. Am J Respir Cell Mol Biol. 2008;38(3):354-361.
54. Kaufman RM, Airo R, Pollack S, Crosby WH. Circulating megakaryocytes and platelet release in the lung. Blood. 1965;26(6):720-731.
55. Sullenbarger B, Bahng JH, Gruner R, Kotov N, Lasky LC. Prolonged continuous in vitro human platelet production using three-dimensional scaffolds. Exp Hematol. 2009;37(1):101-110.
56. Lasky LC, Sullenbarger B. Manipulation of oxygenation and flow-induced shear stress can increase the in vitro yield of platelets from cord blood. Tissue Eng Part C Methods. 2011;17(11):1081-1088.
57. Schlinker AC, Radwanski K, Wegener C, Min K, Miller WM. Separation of in-vitro-derived megakaryocytes and platelets using spinningmembrane filtration [published online ahead of print October 13, 2014]. Biotechnol Bioeng., doi: 10.1002/bit.25477.
58. Feng Q, Shabrani N, Thon JN, et al. Scalable generation of universal platelets from human induced pluripotent stem cells. Stem Cell Rev. 2014;3(5):817-831.
59. Lambert MP, Sullivan SK, Fuentes R, French DL, Poncz M. Challenges and promises for the development of donor-independent platelet transfusions. Blood. 2013;121(17):3319-3324.
60. Anitua E, Andia I, Ardanza B, Nurden P, Nurden AT. Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb Haemost. 2004;91(1):4-15.