Table 1. Identification of human primary... | Rockefeller University Press

Table 1.

Identification of human primary tumor CSC biomarkers using in vivo assays

Cancer	Animal	Type of injection	Treatment of recipient mice	Injection with Matrigel	Percentage of CSC-enriched population in tumor	Biomarkers	Minimal number of biomarker + cells to obtain a tumor	Reference
ALL (B-ALL)	NOD/SCID/IL2rγc^−/− newborns	Intravenous	Sublethal irradiation	No	82.50%	CD34⁺/CD19⁺	2–6 × 10⁴	Kong et al., 2008
AML	NOD/SCID	Intravenous	Sublethal irradiation	No	0.75%	CD34⁺/CD38⁻	2 × 10⁵	Bonnet and Dick, 1997
AML	NOD/SCID, NOD/SCID/β₂m^−/− and NOD/SCID/IL2rγc^−/−	Intravenous and intrabone	IVIG of CD122 pretreatment and sublethal irradiation	No	0.076% (*)	CD34⁺/CD38⁻ () or CD34⁺/CD38⁺ (*) (in samples with lowest CD34⁺/CD38⁻ fraction)	7.5 × 10³ () or 10⁶ (*)	Taussig et al., 2008
AML	NOD/SCID	Intrafemoral	IVIG of CD122 pretreatment and sublethal irradiation	No	0.06–0.00009% of bulk	NA	NA	Eppert et al., 2011
Bladder	Rag2γcDKO	Intradermal	NA	Yes	3–36.3%	CD44	100	Chan et al., 2009
Breast	NOD/SCID	Mammary fat pad	VP-16, estrogen pellets	No	11–35%	ESA⁺/CD44^high/CD24^low-neg	200	Al Hajj et al., 2003
Breast	NOD/SCID	Humanized mammary fat pad	Estrogen pellets	Yes	3–10%	ALDH-1⁺	500	Ginestier et al., 2007
Brain	NOD/SCID	Intracranial	NA	No	6–29%	CD133⁺	100	Singh et al., 2004
Colorectal	NOD/SCID	Renal capsule	Sublethal irradiation	Yes	1.8–24.5%	CD133⁺	100	O’Brien et al., 2007
Colorectal	NOD/SCID	Subcutaneous	NA	No	2.60%	ESA^high/CD44⁺	200	Dalerba et al., 2007
Colorectal	NOD/SCID	Subcutaneous	NA	Yes	3.50%	ALDH-1⁺	25 serially passaged	Huang et al., 2009
Head and neck squamous cell carcinoma	NOD/SCID and Rag2γcDKO	Subcutaneous	NA	Yes	10–12%	CD44⁺	5000	Prince et al., 2007
Liver	SCID	Intrahepatic	NA	No	2.50%	CD45⁻/CD90⁺	10³	Yang et al., 2008
Lung	SCID and NUDE	Subcutaneous, after in vitro expansion	NA	Yes	0.4–1.5%	CD133⁺	10⁴	Eramo et al., 2008
Lung	NOD/SCID/IL2rγc^−/−	Subcutaneous	NA	Yes	Median 15%	lin-/CD166⁺	≤500	Zhang et al., 2012
Melanoma	NOD/SCID	Subcutaneous	NA	No	1.6-20.4%	ABCB5⁺	10⁵	Schatton et al., 2008
Melanoma	Rag2γcDKO	Intradermal	NA	Yes	2.5–41%	CD271⁺	100	Boiko et al., 2010
Melanoma	NOD/SCID/IL2rγc^−/−	Subcutaneous	NA	Yes	NA	NA	1 (in 28% of cases)	Quintana et al., 2010
Melanoma	NUDE, (NOD/SCID, NOD/SCID/IL2rγc^−/−)	Subcutaneous	NA	Yes	8–11%	CD271⁺	1000	Civenni et al., 2011
Pancreatic	NOD/SCID	Subcutaneous and intrapancreatic	NA	Yes	0.2-0.8%	ESA⁺/CD44⁺/CD24⁺	100	Li et al., 2007
Pancreatic	NUDE	Intrapancreatic	NA	No	3.6 cells per high-power field	ESA⁺/CD133⁺	500	Hermann et al., 2007

Cancer	Animal	Type of injection	Treatment of recipient mice	Injection with Matrigel	Percentage of CSC-enriched population in tumor	Biomarkers	Minimal number of biomarker + cells to obtain a tumor	Reference
ALL (B-ALL)	NOD/SCID/IL2rγc^−/− newborns	Intravenous	Sublethal irradiation	No	82.50%	CD34⁺/CD19⁺	2–6 × 10⁴	Kong et al., 2008
AML	NOD/SCID	Intravenous	Sublethal irradiation	No	0.75%	CD34⁺/CD38⁻	2 × 10⁵	Bonnet and Dick, 1997
AML	NOD/SCID, NOD/SCID/β₂m^−/− and NOD/SCID/IL2rγc^−/−	Intravenous and intrabone	IVIG of CD122 pretreatment and sublethal irradiation	No	0.076% (*)	CD34⁺/CD38⁻ () or CD34⁺/CD38⁺ (*) (in samples with lowest CD34⁺/CD38⁻ fraction)	7.5 × 10³ () or 10⁶ (*)	Taussig et al., 2008
AML	NOD/SCID	Intrafemoral	IVIG of CD122 pretreatment and sublethal irradiation	No	0.06–0.00009% of bulk	NA	NA	Eppert et al., 2011
Bladder	Rag2γcDKO	Intradermal	NA	Yes	3–36.3%	CD44	100	Chan et al., 2009
Breast	NOD/SCID	Mammary fat pad	VP-16, estrogen pellets	No	11–35%	ESA⁺/CD44^high/CD24^low-neg	200	Al Hajj et al., 2003
Breast	NOD/SCID	Humanized mammary fat pad	Estrogen pellets	Yes	3–10%	ALDH-1⁺	500	Ginestier et al., 2007
Brain	NOD/SCID	Intracranial	NA	No	6–29%	CD133⁺	100	Singh et al., 2004
Colorectal	NOD/SCID	Renal capsule	Sublethal irradiation	Yes	1.8–24.5%	CD133⁺	100	O’Brien et al., 2007
Colorectal	NOD/SCID	Subcutaneous	NA	No	2.60%	ESA^high/CD44⁺	200	Dalerba et al., 2007
Colorectal	NOD/SCID	Subcutaneous	NA	Yes	3.50%	ALDH-1⁺	25 serially passaged	Huang et al., 2009
Head and neck squamous cell carcinoma	NOD/SCID and Rag2γcDKO	Subcutaneous	NA	Yes	10–12%	CD44⁺	5000	Prince et al., 2007
Liver	SCID	Intrahepatic	NA	No	2.50%	CD45⁻/CD90⁺	10³	Yang et al., 2008
Lung	SCID and NUDE	Subcutaneous, after in vitro expansion	NA	Yes	0.4–1.5%	CD133⁺	10⁴	Eramo et al., 2008
Lung	NOD/SCID/IL2rγc^−/−	Subcutaneous	NA	Yes	Median 15%	lin-/CD166⁺	≤500	Zhang et al., 2012
Melanoma	NOD/SCID	Subcutaneous	NA	No	1.6-20.4%	ABCB5⁺	10⁵	Schatton et al., 2008
Melanoma	Rag2γcDKO	Intradermal	NA	Yes	2.5–41%	CD271⁺	100	Boiko et al., 2010
Melanoma	NOD/SCID/IL2rγc^−/−	Subcutaneous	NA	Yes	NA	NA	1 (in 28% of cases)	Quintana et al., 2010
Melanoma	NUDE, (NOD/SCID, NOD/SCID/IL2rγc^−/−)	Subcutaneous	NA	Yes	8–11%	CD271⁺	1000	Civenni et al., 2011
Pancreatic	NOD/SCID	Subcutaneous and intrapancreatic	NA	Yes	0.2-0.8%	ESA⁺/CD44⁺/CD24⁺	100	Li et al., 2007
Pancreatic	NUDE	Intrapancreatic	NA	No	3.6 cells per high-power field	ESA⁺/CD133⁺	500	Hermann et al., 2007

Studies reporting the existence of enriched human CSC populations are listed. In the first five columns, the main parameters influencing the efficiency of tumor engraftment are listed. From left to right: the tumor entity, the type of immunocompromised mouse strain used, the route of transplantation of human tumor cells, preconditioning of the recipient mice, treatment of mice during the assay, and whether the tumor cells were mixed with Matrigel upon transplantation. In the next four columns, the main results of these studies are summarized. From left to right: the frequency of the identified CSC-enriched population observed in the given tumor entity, the biomarkers identified for this CSC-enriched population, and the minimal number of tumor cells expressing these biomarkers able to give rise to a human tumor as well as the reference of the corresponding study. *, results for the CD34⁺/CD38⁻ population. **, results for the CD34⁺/CD38⁺ population.

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