The landscape of tyrosine kinase inhibitors in sarcomas: looking beyond pazopanib

Figures & data

Figure 1. Kinase selectivity maps. Kinome-wide profiling measuring the dissociation constant (K_d), inhibitory constant (IC₅₀), or percent of control (POC) of the TKIs discussed within the review. The K_d data for imatinib, sunitinib, sorafenib, axitinib, cediranib, nintedanib, crizotinib, and dasatinib were obtained from PMID: 22037378 [16]. The K_d for regorafenib was obtained from PMID: 27734608 [17]. The IC₅₀ for anlotinib and sitravatinib were obtained from PMID: 29446853 and PMID: 26675259, respectively [19,20]. The POC for larotrectinib was obtained from PMID: 24162815 [51]. Abbreviations: CK1; Casein kinase 1, TK; Tyrosine kinase, STE; Sterile kinase, RGC; Receptor guanylate cyclase, CMGC; Cyclin-dependent kinase, mitogen-activated protein kinase, glycogen synthase kinase, and cyclin-dependent-kinase-like kinases, PI3K; Phosphoinositide 3-kinase, TKL; Tyrosine kinase-like, AGC; Protein kinases A, G, and C, CAMK; Ca²⁺/calmodulin-dependent protein kinase.

Table 1. Table of tyrosine kinase selectivity of tyrosine kinase inhibitors discussed within this review.

Tyrosine kinase inhibitors	Commonly targeted tyrosine kinases in order of selectivity	References
Imatinib	ABL1 < KIT < PDGFRB < PDGFRA (Kd)	[16]
Sunitinib	PDGFRB < KIT < PDGFRA < VEGFR2 < VEGFR1 < RET ≪ VEGFR3 ≪ NTRK1 ≪ ALK ≪ ABL1 < FGFR3 ≪ FGFR1/2 < NTRK2 ≪ FGFR4 = SRC ≪ NTRK3 ≪ MET (Kd)	[16]
Sorafenib	RET < KIT < VEGFR1 < PDGFRB < VEGFR2 < PDGFRA < VEGFR3 < ABL1 ≪ NTRK3 ≪ NTRK2 ≪ FGFR2 < FGFR1 ≪ FGFR3 ≪ FGFR4 < NTRK1 (Kd)	[16]
Regorafenib	RET < PDGFRB < PDGFRA < VEGFR1 < ABL1 < KIT < VEGFR3 < VEGFR2 ≪ NTRK3 (Kd)	[17]
Axitinib	PDGFRA < PDGFRB < KIT < VEGFR1 < VEGFR2 ≪ ABL1 < FGFR2 < RET < VEGFR3 < FGFR3 < FGFR1 ≪ MET ≪ NTRK1 (Kd)	[16]
Cediranib	PDGFRB < KIT < PDGFRA < VEGFR1 < VEGFR2 < VEGFR3 < RET < FGFR3 < FGFR2 < FGFR1 < SRC < ABL1 ≪ EGFR ≪ MET ≪ FGFR4 ≪ ALK (Kd)	[16]
Nintedanib	VEGFR2 < NTRK1 < KIT < PDGFRB < PDGFRA < NTRK2 < ALK < RET < NTRK3 < VEGFR1 < FGFR1 < FGFR3 < VEGFR3 ≪ MET < ABL1 ≪ FGFR2 ≪ SRC ≪ FGFR4 (Kd)	[16]
Anlotinib	VEGFR2 < VEGFR3 < KIT < VEGFR1 ≪ PDGFRB (IC50)	[20]
Sitravatinib	VEGFR3 < VEGFR2 = NTRK1 < VEGFR1 = KIT < NTRK2 < MET < PDGFRA < RET ≪ SRC ≪ ABL1 (IC50)	[19]
Crizotinib	MET < ALK < NTRK2 ≪ ABL1 < NTRK3 < NTRK1 ≪ SRC ≪ RET < VEGFR1 < EGFR < FGFR3 (Kd)	[16]
Dasatinib	ABL1 < SRC < PDGFRA < PDGFRB < KIT ≪ EGFR ≪ RET ≪ FGFR2 ≪ VEGFR2 ≪ FGFR1 < FGFR3 ≪ VEGFR1 (Kd)	[16]
Larotrectinib	NTRK1 = NTRK2 ≪ MET < EGFR < VEGFR1 = VEGFR3 < ABL1 = FGFR3 < RET < ALK = VEGFR2 = SRC < FGFR2 < FGFR1 < PDGFRA = PDGFRB	[51]

Key: K_d or IC₅₀ (x) of; x ≤ 1 nMol, x < 10 nMol, 10 ≤ x≤ 50 nMol, 50 ≤ x < 100 nMol, x ≥ 100 nMol. For larotrectinib, values expressed as a percent of control (POC); x≤ 10%, 10 ≤ x < 100, x ≥ 100.

Abbreviations: EGFR, Epidermal growth factor receptor, FGFR; Fibroblast growth factor receptor, IC₅₀; Inhibitory constant, K_d, Dissociation constant, NTRK; Neurotrophic receptor kinase, PDGFR; Platelet-derived growth factor receptor, VEGFR; Vascular endothelial growth factor receptor.

Table 2. Table summarizing the published results of each tyrosine kinase inhibitor discussed within this review.

	Study	Study Type	Patient Number	Chemotherapy Regimen	Subtypes (n)	Best Response	Survival
Imatinib	Chugh et al. [67]	Single arm phase II trial	190	Imatinib 300mg BD	Angiosarcoma (16)	Observed CBR 13.3%	mPFS – 2.76 months
					Ewing’s sarcoma (13)	Observed CBR 0%	mPFS – 1.68 months
					Fibrosarcoma (12)	Observed CBR 8.3%	mPFS – 1.92 months
					LMS (29)	Observed CBR 21.4%	mPFS – 2.76 months
					LPS (31)	Observed CBR 24.1%	mPFS – 3.72 months
					MFH (30)	Observed CBR 10.3%	mPFS – 1.92 months
					Osteosarcoma (27)	Observed CBR 19.2%	mPFS – 1.92 months
					MPNST (7)	Observed CBR 20%	mPFS – 1.92 months
					SS (22)	Observed CBR 15%	mPFS – 1.92 months
					RMS (2)	Observed CBR 0%	mPFS – 2.52 months
	Chugh et al. [68]	Single arm phase II trial	51	Imatinib 300mg BD	DT (51)	Stable Disease 84%	PFS at 3 years – 58%
	Penel et al. [69]	Single arm phase II trial	35	Imatinib 400mg OD	Progressive DT (35)	Complete Response 3% Partial Response 8.5% Stable Disease 80%	mPFS – 25 months
	Kasper et al. [70]	Single arm phase II trial	38	Imatinib 800mg OD	Progressive DT (38)	Partial Response 19%	PFS at 1 year – 59%
	Rutkowski et al. [71]	EORTC single arm phase II trial	16	Imatinib 400mg BD	Advanced or metastatic DFSP not amenable to curative surgery (24)	Partial Response 52.3% Stable Disease 28.6% Disease Progression 19%	PFS at 1 year – 59.7% mPFS – 20.4 months
		SWOG single arm phase II trial	8	Imatinib 400mg OD
Sunitinib	George et al. [74]	Single arm phase II trial	53	Sunitinib 37.5mg OD	Cohort A (18) – LMS (11), SFT (3), others (4)	n/a	Stable disease at 12 weeks – 11%
					Cohort B (21) – Sarcoma NOS (5), SS (4), LPS (2), Others (10)	Partial Response 4%	Stable disease at 12 weeks – 19%
					Cohort C (9) – Chordoma (9)	n/a	Stable disease at 12 weeks – 44%
	Jo et al. [75]	Single arm phase II trial	19	Sunitinib 37.5mg OD	DT (19)	Partial Response 26.3% Stable Disease 42.1%	Median duration of response – 8.2 months PFS at 2 years – 74.7%
	Stacchiotti et al. [76]	Retrospective case series	9	Sunitinib 37.5mg OD	Progressive or metastatic ASPS (9)	Partial Response 55% Stable Disease 33%	mOS – 19 months mPFS – 17 months
	Jagodzinska-Mucha et al. [77]	Retrospective case series	15	Sunitinib 37.5mg OD	Metastatic ASPS (15)	Partial Response 40% Stable Disease 53%	mOS – 56 months mPFS – 19 months
	Stacchiotti et al. [78]	Retrospective case series	31	Sunitinib 37.5mg OD	Progressive SFT (31)	Partial Response 6.5% Stable Disease 51.6%	mPFS – 6 months
	Stacchiotti et al. [80]	Retrospective case series	10	Sunitinib 37.5mg OD	Metastatic extraskeletal myxoid chondrosarcoma (10)	Partial Response 60% Stable Disease 20% Progressive Disease 20%	mPFS not reached at median follow-up – 8.5 months
Sorafenib	Ray-Coquard et al. [89]	Single arm phase II trial	41	Sorafenib 400mg BD	Superficial angiosarcoma (26)	Complete Response 5% Partial Response 5% Stable Disease 20%	mPFS – 1.8 months
					Visceral angiosarcoma (15)	Partial Response 15.4% Stable Disease 30.8%	mPFS – 3.8 months
	Gounder et al. [96]	Retrospective case series	26	Sorafenib 400mg OD	Aggressive DT (26)	25% Partial Response 70% Stable Disease	Median time to response – 10 months mPFS not reached with median follow-up – 6 months
	Gounder et al. [97]	Phase III trial	87	2:1 randomization to placebo or sorafenib 400mg OD	Aggressive DT (87)	Complete Response 2% Partial Response 30.6%	PFS at 1 year – 89% Hazard ratio for progression or death vs placebo – 0.13 (p < 0.0001)
Regorafenib	Mir el al. [99]	Placebo-controlled phase II trial	182	1:1 Randomization to placebo or regorafenib 160mg OD	LPS (43)	Stable Disease 45% Progressive Disease 55%	mPFS – 1.0 months vs 1.7 months in placebo (p = 0.70)
					LMS (56)	Stable Disease 86% Progressive Disease 11%	mPFS – 3.7 months vs 1.8 months in placebo (p = 0.0045)
					SS (27)	Partial Response 8% Stable Disease 77% Progressive Disease 15%	mPFS – 5.6 months vs 1.0 months in placebo (p < 0.0001)
					Other sarcomas (56)	Partial Response 11% Stable Disease 67% Progressive Disease 22%	mPFS – 2.9 months vs 1.0 months in placebo (p < 0.0061)
Axitinib	Stacchiotti et al. [101]	Single arm phase II trial	17	Axitinib 5mg BD	Advanced and progressive SFT (17)	Partial Response 41.2% Stable Disease 35.3%	mPFS – 5.1 months
Cediranib	Kummar et al. [106]	Single arm phase II trial	46	Cediranib 30mg OD	Metastatic, unresectable ASPS (46)	Partial Response 35%	Disease control at 6 months – 84%
						Stable Disease 60%
	Judson et al. [114]	Placebo-controlled phase II trial	48	2:1 randomization to placebo or cediranib 30mg OD	Metastatic, progressive ASPS (48)	Partial Response 19.4% Stable Disease 39.3%	Best median % change in sum of diameters of target lesion −15.7% vs + 1.2% in placebo (p < 0.0001) PFS at 12 months – 38.7%
Anlotinib	Chi et al. [122]	Single arm phase II trial	166	Anlotinib 12mg OD	LPS (13)	Partial Response 7.7%	mPFS −5.6 months
					LMS (26)	Partial Response 7.7%	mPFS – 11 months
					SS (47)	Partial Response 17%	Mpfs – 7.7 months
					Fibrosarcoma (18)	Partial Response 11.1%	mPFS – 5.6 months
					UPS (19)	Partial Response 5.5%	mPFS – 4.1 months
					ASPS (13)	Partial Response 46.2%	mPFS – 21 months
					CCS (7)	Partial Response 14.3%	mPFS – 11 months
					Others (23)	Partial Response 0%	mPFS – 2.8 months
Crizotinib	Schöffski et al. [130]	Single arm phase II trial	45	Crizotinib 250mg BD	Advanced or metastatic ASPS (45)	Partial Response 4.4% Stable Disease 86.7%	mPFS – 8.1 months
	Schöffski et al. [131]	Single arm phase II trial	19	Crizotinib 250mg BD	Advanced or metastatic ALK-positive IMT (12)	Objective Response 50%	PFS at 1 year – 73.3%
					Advanced or metastatic ALK-negative IMT (7)	Objective Response 14%	PFS at 1 year – 53.6%
	Schöffski et al. [132]	Single arm phase II trial	26	Crizotinib 250mg BD	Advanced or metastatic CCS with MET activation (26)	Partial Response 3.8% Stable Disease 65.4%	mPFS – 4.4 months
Dasatinib	Schuetze et al. [142]	Single arm phase II trial	109	Dasatinib 100mg BD	ASPS (12)	Choi ORR 8%	mPFS per Choi – 11 months
					Chondrosarcoma (33)	Choi ORR 15%	mPFS per Choi – 5.5 months
					Chodroma (32)	Choi ORR 19%	mPFS per Choi – 6.3 months
					ES (7)	Choi ORR 29%	mPFS per Choi – 7.9 months
					SFT (25)	Choi ORR 20%	mPFS per Choi – 2 months

Abbreviations: ASPS; Alveolar soft part sarcoma, BD; Bis die (twice daily), CBR; Clinical benefit rate, CCS; Clear cell sarcoma, DT: Desmoid tumor, ES; Epithelioid sarcoma, IMT; Inflammatory myofibroblastic tumor, LMS; Leiomyosarcoma, LPS; Liposarcoma, MFH ; Malignant fibrous histiocytoma, mOS; Median overall survival, mPFS; Median progression-free survival, MPNST; Malignant peripheral nerve sheath tumor, NOS; Not otherwise specified, OD; Omne die (once daily), ORR; Overall response rate, PFS; Progression-free survival, RMS; Rhabdomyosarcoma, SFT; Solitary fibrous tumor, SS; Synovial sarcoma, UPS; Undifferentiated pleomorphic sarcoma.

Table 3. Table summarizing the clinical trials of tyrosine kinase inhibitors presented by specific soft tissue sarcoma subtype.

	TKI	Study	Study Type	Patient Number	Chemotherapy Regimen	Best Response	Survival
DESMOID TUMORS	Imatinib	Chugh et al.[68]	Single arm phase II trial	51	Imatinib 300mg BD	10% Progressive Disease 84% Stable Disease 6% Not Evaluable	PFS at 1 year – 66% PFS at 3 years – 58%
		Penel et al. [69]	Single arm phase II trial	35	Imatinib 400mg OD	8.5% Progressive Disease 80% Stable Disease 3% Complete Response	Median follow-up – 34 months mPFS – 25 months
		Kasper et al. [70]	Single arm phase II trial	38	Imatinib 800mg OD	19% Partial Response	PFS at 1 year – 59%
	Sunitinib	Jo et al.[75]	Single arm phase II trial	19	Sunitinib 37.5mg OD	15.8% Progressive Disease 42.1% Stable Disease 26.3% Partial Response	Median duration of response – 8.2 months Median follow-up – 20.3 months PFS at 2 years – 74.7%
	Sorafenib	Gounder et al. [96]	Retrospective case series	26	Sorafenib 400mg OD	5% Progressive Disease 70% Stable Disease 25% Partial Response	Median time to response – 10 months Median follow-up – 6 months mPFS – not reached
		Gounder et al. [97]	Phase III trial	50	Sorafenib 400mg OD	30.6% Partial Response 2% Complete Response	PFS at 1 year – 81% Median time to response – 9.6 months
				37	Placebo	20% Partial Response	PFS at 1 year – 36%
SOLITARY FIBROUS TUMORS	Sunitinib	Stacchiotti et al. [78]	Retrospective case series	31	Sunitinib 37.5mg OD	42% Disease Progression 51.6% Stable Disease 6.5% Partial Response	mPFS – 6 months
	Axitinib	Stacchiotti et al. [101]	Single arm phase II trial	17	Axitinib 5mg BD	Partial Response 41.2% Stable Disease 35.3%	mPFS – 5.1 months
	Dasatinib	Schuetze et al. [142]	Single arm phase II trial	25	Dasatinib 100mg BD	Choi ORR 20%	mPFS per Choi – 2 months
ALVEOLAR SOFT PART SARCOMA	Sunitinib	Stacchiotti et al. [76]	Retrospective case series	9	Sunitinib 37.5mg OD	Partial Response 55% Stable Disease 33%	mOS – 19 months mPFS – 17 months
		Jagodzinska-Mucha et al. [77]	Retrospective case series	15	Sunitinib 37.5mg OD	Partial Response 40% Stable Disease 53%	mOS – 56 months mPFS – 19 months
	Cediranib	Kummar et al. [106]	Single arm phase II trial	46	Cediranib 30mg OD	Partial Response 35% Stable Disease 60%	Disease control at 6 months – 84%
		Judson et al. [114]	Placebo-controlled phase II trial	48	2:1 cediranib 30mg OD to placebo	Partial Response 19.4% Stable Disease 39.3%	Best median % change in sum of diameters of target lesion −15.7% vs + 1.2% in placebo (p < 0.0001)
							PFS at 12 months – 38.7%
	Anlotinib	Chi et al. [122]	Single arm phase II trial	13	Anlotinib 12mg OD	Partial Response 46.2%	mPFS – 21 months
	Crizotinib	Schöffski et al. [130]	Single arm phase II trial	45	Crizotinib 250mg BD	Partial Response 4.4% Stable Disease 86.7%	mPFS – 8.1 months
	Dasatinib	Schuetze et al. [142]	Single arm phase II trial	12	Dasatinib 100mg BD	Choi ORR 8%	mPFS per Choi – 11 months

Abbreviations: BD; Bis die (twice daily), mOS; Median overall survival, mPFS; Median progression-free survival, OD; Omne die (once daily), ORR; Objective response rate, PFS; Progression-free survival, TKI; Tyrosine kinase inhibitor.

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