Table 2.
Summary of current limitations and areas for development in organoid culture for aging
GoalsApproachesChallenges
Increase developmental maturity of pluripotent stem cell–derived organoids Long-term culture (Nicholas et al., 2013; Takasato et al., 2016; Tzatzalos et al., 2016) Stem cells are highly sensitive to culture conditions, impeding robust protocols 
 In vivo maturation (Huch et al., 2013; Watson et al., 2014; Takebe et al., 2015)  
 Mechanical or electrical conditioning of muscle and cartilage (Ruan et al., 2016)  
 Improved culture conditions and differentiation protocols  
 Acceleration by small molecules (Chambers et al., 2012)  
Source culturable, age-varied human cells Surgical discards from elective surgery, transplant trimmings, and tissue peripheral to tumors Hard to source certain tissues, especially healthy, culturable adult cells 
  Cells adapt to culture and are not infinitely renewable 
  Nontumor peripheral tissue may differ from healthy tissue 
In vitro aging to model the effects of specific age-related lesions and provide a source of artificially aged cells Induced senescence by DNA damage or environmental stress (Busuttil et al., 2003; Parrinello et al., 2005; Nasto et al., 2013) Controversial which treatments best phenocopy aging 
 Long-term culture (Dos Santos et al., 2015)  
 Progeria mutations (Liu et al., 2011; Zhang et al., 2011; Miller et al., 2013)  
 Direct reprogramming of aged cells (Mertens et al., 2015)  
Mimic the effects of the aged ECM in vitro ECM from aged donors (Gullapalli et al., 2005; Williams et al., 2014; Stearns-Reider et al., 2017) Controversial which treatments best phenocopy aging 
 Glycation crosslinking (Rodriguez-Teja et al., 2015) ECM extraction from tissues can alter its mechanical properties, microstructure, and composition 
 Enzymatic crosslinking (Levental et al., 2009)  
Develop aging-relevant experimental readouts Epigenetic clock (Hannum et al., 2013; Horvath, 2013) Unclear which signs of aging are most important 
 Mutational analysis (Blokzijl et al., 2016) Require signs of aging that change appreciably across the span of an experiment 
 Protein/DNA oxidation  
 Protein aggregation  
 Tissue-specific functional assays  
Long-term maintenance of organoids in a stable, growth-arrested state Improved culture media Relatively few published maintenance conditions 
 Improved ECM and bioreactors Vetting culture conditions is lengthy 
Complete modeling of whole organs and physiological systems Co-culture with immune cells, stromal cells, and microbiome bacteria (Parrinello et al., 2005; Engevik et al., 2015; Plaks et al., 2015) Few good techniques for sophisticated organoid construction 
Increase throughput and reproducibility Vascularization (Auger et al., 2013) Powerful techniques are often cumbersome and low-throughput 
 Innervation (Workman et al., 2017)  
 In vivo implantation (Watson et al., 2014; Takebe et al., 2015)  
 Microfluidic access to apical/basal fluid reservoirs and fluid transport between organ systems (Vernetti et al., 2017)  
 Organ-specific ECM (Voytik-Harbin et al., 2007; Zhang et al., 2009; O’Brien et al., 2010)  
 Defined artificial ECMs may decrease lot-to-lot variability (Gjorevski et al., 2016)  
 Growth factor distribution within ECM gels for spatial control over growth and differentiation (Wylie et al., 2011)  
 Cell patterning for control over initial organoid shape and composition (Nelson et al., 2008; Todhunter et al., 2015)  
 3D-printed gels amenable to perfusion with control over large-scale tissue structure (Kolesky et al., 2016)  
 Morphological screening and sorting to enrich for correctly formed organoids (Arora et al., 2017)  
GoalsApproachesChallenges
Increase developmental maturity of pluripotent stem cell–derived organoids Long-term culture (Nicholas et al., 2013; Takasato et al., 2016; Tzatzalos et al., 2016) Stem cells are highly sensitive to culture conditions, impeding robust protocols 
 In vivo maturation (Huch et al., 2013; Watson et al., 2014; Takebe et al., 2015)  
 Mechanical or electrical conditioning of muscle and cartilage (Ruan et al., 2016)  
 Improved culture conditions and differentiation protocols  
 Acceleration by small molecules (Chambers et al., 2012)  
Source culturable, age-varied human cells Surgical discards from elective surgery, transplant trimmings, and tissue peripheral to tumors Hard to source certain tissues, especially healthy, culturable adult cells 
  Cells adapt to culture and are not infinitely renewable 
  Nontumor peripheral tissue may differ from healthy tissue 
In vitro aging to model the effects of specific age-related lesions and provide a source of artificially aged cells Induced senescence by DNA damage or environmental stress (Busuttil et al., 2003; Parrinello et al., 2005; Nasto et al., 2013) Controversial which treatments best phenocopy aging 
 Long-term culture (Dos Santos et al., 2015)  
 Progeria mutations (Liu et al., 2011; Zhang et al., 2011; Miller et al., 2013)  
 Direct reprogramming of aged cells (Mertens et al., 2015)  
Mimic the effects of the aged ECM in vitro ECM from aged donors (Gullapalli et al., 2005; Williams et al., 2014; Stearns-Reider et al., 2017) Controversial which treatments best phenocopy aging 
 Glycation crosslinking (Rodriguez-Teja et al., 2015) ECM extraction from tissues can alter its mechanical properties, microstructure, and composition 
 Enzymatic crosslinking (Levental et al., 2009)  
Develop aging-relevant experimental readouts Epigenetic clock (Hannum et al., 2013; Horvath, 2013) Unclear which signs of aging are most important 
 Mutational analysis (Blokzijl et al., 2016) Require signs of aging that change appreciably across the span of an experiment 
 Protein/DNA oxidation  
 Protein aggregation  
 Tissue-specific functional assays  
Long-term maintenance of organoids in a stable, growth-arrested state Improved culture media Relatively few published maintenance conditions 
 Improved ECM and bioreactors Vetting culture conditions is lengthy 
Complete modeling of whole organs and physiological systems Co-culture with immune cells, stromal cells, and microbiome bacteria (Parrinello et al., 2005; Engevik et al., 2015; Plaks et al., 2015) Few good techniques for sophisticated organoid construction 
Increase throughput and reproducibility Vascularization (Auger et al., 2013) Powerful techniques are often cumbersome and low-throughput 
 Innervation (Workman et al., 2017)  
 In vivo implantation (Watson et al., 2014; Takebe et al., 2015)  
 Microfluidic access to apical/basal fluid reservoirs and fluid transport between organ systems (Vernetti et al., 2017)  
 Organ-specific ECM (Voytik-Harbin et al., 2007; Zhang et al., 2009; O’Brien et al., 2010)  
 Defined artificial ECMs may decrease lot-to-lot variability (Gjorevski et al., 2016)  
 Growth factor distribution within ECM gels for spatial control over growth and differentiation (Wylie et al., 2011)  
 Cell patterning for control over initial organoid shape and composition (Nelson et al., 2008; Todhunter et al., 2015)  
 3D-printed gels amenable to perfusion with control over large-scale tissue structure (Kolesky et al., 2016)  
 Morphological screening and sorting to enrich for correctly formed organoids (Arora et al., 2017)  

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