Table 2.

In vitro and ex vivo platelet-producing systems based on their design

PublicationBrief description of systemPlatelet generated per input cellMK species and originPlatelet functionalityBasis for design
Choi et al44  Static cell culture 240 per (proplatelet extending) MK Human peripheral blood Platelets aggregated in response to thrombin and ADP/fibrinogen. CD62 and activated integrin αIIbβ3 expression increased in response to thrombin and ADP, respectively. Static or perfused cellular culture 
Matsunaga et al78  Multistage cell culture 4 × 104 per starting CD34+ cell Human umbilical cord blood Platelets aggregated in response to ADP/fibrinogen. Platelet CD62P and activated integrin αIIbβ3 expression increased in response to ADP. 
Takayama et al79  Static cell culture ∼48 per hESC  hESC Platelets increased activated integrin αIIbβ3 expression in response to thrombin and ADP. Filopodia are also formed on fibrinogen coated surface. 
Lu et al80  Static cell culture 6.7 per MK hESC Platelets formed microaggregates, facilitated clot formation/retraction, and formed lamellipodia and filopodia in response to thrombin activation. In vivo function documented by incorporation of produced platelet-like particles into a newly formed thrombus in mice. 
Sullenbarger et al81  Perfused 3D hydrogel bioreactor 19.6 per starting CD34+ cell Human umbilical cord blood Platelets showed increased CD62 and CD63 expression following maximal thrombin stimulation. No statistical analysis was shown. Preactivation of platelets was present. 
Lasky et al82  Added shear forces and oxygenation Twofold to threefold increase in platelet numbers Platelet aggregation and CD62 and CD63 expression measured. Statistical analysis missing but a degree of aggregation occurred and an increase in the percentage of CD62- and CD63-expressing platelets when activated with thrombin. 
Dunois-larde et al69  Perfusion at high shear rates on vWf Not stated Human umbilical cord blood and bone marrow Platelets spread on fibrinogen-coated surface and increased CD62P expression in response to thrombin Shear forces;
turbulent and/or laminar flow 
Blin et al83  PDMS microfluidics pillar forest coated with vWf 3.7 per MK Human umbilical cord blood Platelets spread on fibrinogen-coated surface and exhibit cytoskeletal changes in response to thrombin. Significant increase in integrin αIIbβ3 in response to TRAP agonist. 
Ito et al84  Microfluidic pillar chamber
Static cell culture
8 L tank with turbulent flow 
14 per MK
<20 per MK
70-80 per MK 
Immortalized MK cell lines derived from hiPSCs Extensive flow cytometric, aggregation, and in vivo mouse bleeding time testing showing functional platelets in the various iterations of the bioreactor 
Strassel et al85  Successive pipetting of cultured cells 28 per MK Human peripheral blood In vitro function of platelet-like particles observed in a flow chamber and in vivo function documented by the incorporation of produced platelet-like particles into a newly formed thrombus in mice 
Pongérard et al86  Polypropylene spheres' fluidic system producing turbulent and laminar flow 100 per MK Increased expression of αIIbβ3 in response to a range of agonists. Higher survival of platelets when injected into a mouse when compared with control. 
Nakagawa et al87  Scaffolds with flow and ordered pores 0.6 per MK  hESC or hiPSCs
KhES-3 hESC clone
TkDA3-4 hiPSC clone
Mouse C3H10T1/2 cell line 
Increased expression of activated αIIbβ3 in ESC and iPSC-derived platelets in response to a range of agonists (no statistical analysis, n = 2) Bone-marrow mimetic 
Avanzi et al88  Nanofiber membranes and flow 100 per MK Human umbilical cord blood Increased CD62P expression upon stimulation with PMA (n = 1 shown) 
Martinez et al89  Bioreactor with slits and flow Not clearly stated Human peripheral blood Increased expression of CD62P on platelet-like particles upon stimulation with thrombin (no statistical analysis). Adherence to fibrinogen coated surface and spreads upon thrombin stimulation. 
Tozzi et al90  Bone-marrow niche replicate synthesized in silk fibroin 124 per MK  Human umbilical cord blood Increased expression of αIIbβ3 in response to thrombin 
Di Buduo et al91  3D porous silk sponge with ECM components, cytokines, and endothelium-derived proteins 5.6 per (seeded) MK  Human umbilical cord blood Adhesion to collagen under flow conditions and established actin reorganization. Increased expression of CD31 and CD42b upon stimulation with multiple agonists at once. Produced platelets mixed with native platelets during an ex vivo clot assay. 
Pallotta et al92  Silk microtubular bioreactor ∼200 per (proplatelet extending) MK (7% of all MKs) Human umbilical cord blood Increased expression of αIIbβ3 and CD62P following thrombin stimulation 
Thon et al93  PDMS microfluidics with ECM components + endothelial cells 42 per murine MK (∼20 in static culture)
∼30 per human MK 
Primary mouse bone marrow–derived MKs
hiPSCs 
Platelets form lamellipodia and filipodia when activated 
Fujiyama et al94  Ex vivo porcine thighbone 4.4 per MK  Human umbilical cord blood Increased expression of CD62P following thrombin stimulation (no statistical analysis) 
Zhao et al50  Ex vivo murine lungs vasculature perfusion
Microfluidic branching perfusion 
2997 per MK
492 per MK 
Primary mouse bone marrow–derived MKs In vitro and ex vivo system–produced platelets increased expression of αIIbβ3 and CD62P following stimulation with thrombin or CRP-XL. Ex vivo–generated platelets also incorporated into an in vitro thrombus containing native platelets. Lung vasculature mimetic 
PublicationBrief description of systemPlatelet generated per input cellMK species and originPlatelet functionalityBasis for design
Choi et al44  Static cell culture 240 per (proplatelet extending) MK Human peripheral blood Platelets aggregated in response to thrombin and ADP/fibrinogen. CD62 and activated integrin αIIbβ3 expression increased in response to thrombin and ADP, respectively. Static or perfused cellular culture 
Matsunaga et al78  Multistage cell culture 4 × 104 per starting CD34+ cell Human umbilical cord blood Platelets aggregated in response to ADP/fibrinogen. Platelet CD62P and activated integrin αIIbβ3 expression increased in response to ADP. 
Takayama et al79  Static cell culture ∼48 per hESC  hESC Platelets increased activated integrin αIIbβ3 expression in response to thrombin and ADP. Filopodia are also formed on fibrinogen coated surface. 
Lu et al80  Static cell culture 6.7 per MK hESC Platelets formed microaggregates, facilitated clot formation/retraction, and formed lamellipodia and filopodia in response to thrombin activation. In vivo function documented by incorporation of produced platelet-like particles into a newly formed thrombus in mice. 
Sullenbarger et al81  Perfused 3D hydrogel bioreactor 19.6 per starting CD34+ cell Human umbilical cord blood Platelets showed increased CD62 and CD63 expression following maximal thrombin stimulation. No statistical analysis was shown. Preactivation of platelets was present. 
Lasky et al82  Added shear forces and oxygenation Twofold to threefold increase in platelet numbers Platelet aggregation and CD62 and CD63 expression measured. Statistical analysis missing but a degree of aggregation occurred and an increase in the percentage of CD62- and CD63-expressing platelets when activated with thrombin. 
Dunois-larde et al69  Perfusion at high shear rates on vWf Not stated Human umbilical cord blood and bone marrow Platelets spread on fibrinogen-coated surface and increased CD62P expression in response to thrombin Shear forces;
turbulent and/or laminar flow 
Blin et al83  PDMS microfluidics pillar forest coated with vWf 3.7 per MK Human umbilical cord blood Platelets spread on fibrinogen-coated surface and exhibit cytoskeletal changes in response to thrombin. Significant increase in integrin αIIbβ3 in response to TRAP agonist. 
Ito et al84  Microfluidic pillar chamber
Static cell culture
8 L tank with turbulent flow 
14 per MK
<20 per MK
70-80 per MK 
Immortalized MK cell lines derived from hiPSCs Extensive flow cytometric, aggregation, and in vivo mouse bleeding time testing showing functional platelets in the various iterations of the bioreactor 
Strassel et al85  Successive pipetting of cultured cells 28 per MK Human peripheral blood In vitro function of platelet-like particles observed in a flow chamber and in vivo function documented by the incorporation of produced platelet-like particles into a newly formed thrombus in mice 
Pongérard et al86  Polypropylene spheres' fluidic system producing turbulent and laminar flow 100 per MK Increased expression of αIIbβ3 in response to a range of agonists. Higher survival of platelets when injected into a mouse when compared with control. 
Nakagawa et al87  Scaffolds with flow and ordered pores 0.6 per MK  hESC or hiPSCs
KhES-3 hESC clone
TkDA3-4 hiPSC clone
Mouse C3H10T1/2 cell line 
Increased expression of activated αIIbβ3 in ESC and iPSC-derived platelets in response to a range of agonists (no statistical analysis, n = 2) Bone-marrow mimetic 
Avanzi et al88  Nanofiber membranes and flow 100 per MK Human umbilical cord blood Increased CD62P expression upon stimulation with PMA (n = 1 shown) 
Martinez et al89  Bioreactor with slits and flow Not clearly stated Human peripheral blood Increased expression of CD62P on platelet-like particles upon stimulation with thrombin (no statistical analysis). Adherence to fibrinogen coated surface and spreads upon thrombin stimulation. 
Tozzi et al90  Bone-marrow niche replicate synthesized in silk fibroin 124 per MK  Human umbilical cord blood Increased expression of αIIbβ3 in response to thrombin 
Di Buduo et al91  3D porous silk sponge with ECM components, cytokines, and endothelium-derived proteins 5.6 per (seeded) MK  Human umbilical cord blood Adhesion to collagen under flow conditions and established actin reorganization. Increased expression of CD31 and CD42b upon stimulation with multiple agonists at once. Produced platelets mixed with native platelets during an ex vivo clot assay. 
Pallotta et al92  Silk microtubular bioreactor ∼200 per (proplatelet extending) MK (7% of all MKs) Human umbilical cord blood Increased expression of αIIbβ3 and CD62P following thrombin stimulation 
Thon et al93  PDMS microfluidics with ECM components + endothelial cells 42 per murine MK (∼20 in static culture)
∼30 per human MK 
Primary mouse bone marrow–derived MKs
hiPSCs 
Platelets form lamellipodia and filipodia when activated 
Fujiyama et al94  Ex vivo porcine thighbone 4.4 per MK  Human umbilical cord blood Increased expression of CD62P following thrombin stimulation (no statistical analysis) 
Zhao et al50  Ex vivo murine lungs vasculature perfusion
Microfluidic branching perfusion 
2997 per MK
492 per MK 
Primary mouse bone marrow–derived MKs In vitro and ex vivo system–produced platelets increased expression of αIIbβ3 and CD62P following stimulation with thrombin or CRP-XL. Ex vivo–generated platelets also incorporated into an in vitro thrombus containing native platelets. Lung vasculature mimetic 

Original publication, a brief description of the design, the platelet production efficiency, the species/cell origin of the MK, and the functionality of the produced cells are included. Efficiency is described as platelets generated per input MK (or per original stem cell if MK numbers were not provided).

ADP, adenosine 5′-diphosphate; ESC, embryonic stem cells; hESC, human embryonic stem cells; PDMS, polydimethylsiloxane.

When not clearly stated in the publication, the exhibited data were analyzed to estimate the platelet-producing efficiency.

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