Adiponectin protects against myocardial ischemia–reperfusion injury: a systematic review and meta-analysis of preclinical animal studies

Yue, Hongyi; Zhang, Qunhui; Chang, Senhao; Zhao, Xinjie; Wang, Mengjie; Li, Wenhua

doi:10.1186/s12944-024-02028-w

Lipids in Health and Disease

Table 1 Characteristic table of the literature

From: Adiponectin protects against myocardial ischemia–reperfusion injury: a systematic review and meta-analysis of preclinical animal studies

Author and Year	Species and gender	Week old and Weight	Anesthetic	Model and method	Treatment group		MI/RI Time	Comorbidity	Outcomes and P-Value	Mechanisms
Author and Year	Species and gender	Week old and Weight	Anesthetic	Model and method	APN and Duration	Administration	MI/RI Time	Comorbidity	Outcomes and P-Value	Mechanisms
Shibata et al. 2005 [26]	Queue a (WT): C57BL/6 mices, ND	10 to 12 weeks, ND	Pent	MIRI, ligation of LAD	2 × 10⁸ PFU, 3 d	IV	0.5 h/48 h	no	1. Infarct size: P < 0.05 2. Apoptotic rate: P < 0.05 3. LVEDP: P < 0.05 4. + dP/dtmax: P < 0.05 5. -dP/dtmax: P < 0.05 6. TNF-α: P < 0.05	AMPK↑/COX-2↑/apoptosis↓/proinflammatory cytokine↓
Shibata et al. 2005 [26]	Queue b (APN-KO): C57BL/6 mices, ND	10 to 12 weeks, ND	Pent	MIRI, ligation of LAD	2 × 10⁸ PFU, 3 d	IV	0.5 h/48 h	no	1. Infarct size: P < 0.01 2. Apoptotic rate: P < 0.05 3. TNF-α: P < 0.01	AMPK↑/COX-2↑/apoptosis↓/proinflammatory cytokine↓
Tao et al. 2007 [27]	Adult mices, male	ND	Isoflurane	MIRI, ligation of LAD	1 to 4 μg/g, 10 min	IP	0.5 h/3 h, 24 h	no	1. Infarct size: P < 0.01 2. Apoptotic rate: P < 0.01 3. LVEDP: P < 0.01 4. + dP/dtmax: P < 0.01 5. -dP/dtmax: P < 0.01 6. Caspase-3: P < 0.01 7. Superoxide production: P < 0.01	iNOS↓/gp91^phox protein↓/oxidative or nitrative stress↓
Wang et al. 2009 [28]	Queue a (WT): D157A mices, male	ND	Isoflurane	MIRI, ligation of LAD	2 μg/g, 10 min	IP	0.5 h/3 h, 24 h	no	1. Infarct size: P < 0.01 2. Apoptotic rate: P < 0.01 3. LVEDP: P < 0.05 4. + dP/dtmax: P < 0.05 5. -dP/dtmax: P < 0.05 6. Caspase-3: P < 0.01 7. Superoxide production: P < 0.01 8. LDH: P < 0.01	apoptosis↓/oxidative or nitrative stress↓ (Note: the antioxidative and antinitrative effects of APN in MIRI hearts are not mediated by AMPK)
Wang et al. 2009 [28]	Queue b (AMPK-DN): D157A mices, male	ND	Isoflurane	MIRI, ligation of LAD	2 μg/g, 10 min	IP	0.5 h/3 h, 24 h	no	1. Infarct size: P < 0.01 2. Apoptotic rate: P < 0.01 3. LVEDP: P < 0.05 4. + dP/dtmax: P < 0.05 5. -dP/dtmax: P < 0.05 6. Caspase-3: P < 0.05 7. Superoxide production: P < 0.05 8. LDH: P < 0.01
Kondo et al. 2010 [29]	Yorkshire-Duroc pigs, female	2 to 3 months, 29.55 to 31.95 kg	Pent	MIRI, ligation of LAD	0.03 μg/kg, 10 min	Arterial administration	0.75 h/24 h	no	1. Infarct size: P < 0.05 2. Apoptotic rate: P < 0.01 3. LVEDP: P < 0.05 4. + dP/dtmax: P < 0.05 5. -dP/dtmax: P < 0.05 6. TNF-α: P < 0.05	inflammation↓/apoptosis↓/oxidative stress↓
Wang et al. 2010 [30]	SD rats, male	8 to 10 weeks, 180 to 220 g	Urethane	MIRI, ligation of LAD	60 ng/g, 2 min	IV	0.5 h/1 h	no	1. Caspase-3: P < 0.01	AMPK↑/PPAR-γ↑/apoptosis↓
Chen 2011 [31]	SD rats, male	ND, 220 to 250 g	Pent	MIRI, ligation of LAD	60/120/180 ng/g, 30 min	IV	0.75 h/3 h	DM	1. Infarct size: P < 0.01 2. + dP/dtmax: P < 0.01 3. -dP/dtmax: P < 0.01 4. Caspase-3: P < 0.01 5. SOD: P < 0.01	NOS↑/SOD↑/oxidative stress↓
Liu et al. 2011 [32]	Queue a (WT): C57B1/6 J mices, male	8 to 12 weeks, ND	Isoflurane	MIRI, ligation of LAD	0.5 mg/kg, 10 min	IV	0.5 h/3 h	Trauma	1. Infarct size: P < 0.01 2. + dP/dtmax: P < 0.01 3. Caspase-3: P < 0.01 4. Superoxide production: P < 0.05	apoptosis↓/oxidative or nitrative stress↓
Liu et al. 2011 [32]	Queue b(APN-KO): C57B1/6 J mices, male	8 to 12 weeks, ND	Isoflurane	MIRI, ligation of LAD	0.5 mg/kg, 10 min	IV	0.5 h/3 h	Trauma	1. Infarct size: P < 0.01 2. + dP/dtmax: P < 0.01	apoptosis↓/oxidative or nitrative stress↓
Ma et al. 2011 [33]	Queue a (DM1d): Swiss mices, ND	6 to 8 weeks, ND	Isoflurane	MIRI, ligation of LAD	2 μg/g, 10 min	IP	0.5 h/3 h, 24 h	DM	1. Infarct size: P > 0.05 2. Apoptotic rate: P > 0.05 3. Caspase-3: P > 0.05 4. LDH: P > 0.05	AdipoR1↑/AMPK↑/LDH↓/apoptosis↓
Ma et al. 2011 [33]	Queue b (DM7d): Swiss mices, ND	6 to 8 weeks, ND	Isoflurane	MIRI, ligation of LAD	2 μg/g, 10 min	IP	0.5 h/3 h, 24 h	DM	1. Infarct size: P < 0.01 2. Apoptotic rate: P < 0.01 3. Caspase-3: P < 0.01 4. LDH: P < 0.01	AdipoR1↑/AMPK↑/LDH↓/apoptosis↓
Chen et al. 2011 [34]	SD rats, male	ND, 220 to 250 g	Pent	MIRI, ligation of LAD	180 ng/g, 30 min	IV	0.75 h/3 h	no	1. LVEDP: P < 0.05 2. LDH: P < 0.01	apoptosis↓/oxidative stress↓
Gao et al. 2012 [35]	C57 mices, male	4 to 6 weeks, 20 to 25 g	Isoflurane	MIRI, ligation of LAD	0.5 mg /kg, 10 min	IP	0.5 h/3 h, 24 h	no	1. LVEF: P < 0.05 2. Caspase-3: P < 0.05	ND
Guo 2013 [36]	SD rats, male	7 to 8 weeks, 220 to 250 g	Pent	MIRI, ligation of LAD	1 μg/kg, 10 min	IV	0.75 h/3 h	no	1. Infarct size: P < 0.05 2. Apoptotic rate: P < 0.05 3. LVEDP: P < 0.05 4. + dP/dtmax: P < 0.05 5. -dP/dtmax: P < 0.05 6. Caspase-3: P < 0.05 7. LDH: P < 0.05	apoptosis↓/LDH↓/CK-MB↓/arrhythmia↓
Zhang et al. 2013 [37]	Queue a (Scramble): D157A mices, male	ND	Isoflurane	MIRI, ligation of LAD	2 μg/g, 20 min	IP	0.5 h/3 h, 24 h	no	1. Infarct size: P < 0.01 2. LVEDP: P < 0.01 3. + dP/dtmax: P < 0.01 4. LVEF: P < 0.05 5. Caspase-3: P < 0.01 6. Apoptotic rate: P < 0.01 7. Superoxide production: P < 0.01	PKA activity↑/oxidative stress↓/IKK, IκB↓/NF-κB↓
Zhang et al. 2013 [37]	Queue b (PKA-KO): D157A mices, male	ND	Isoflurane	MIRI, ligation of LAD	2 μg/g, 20 min	IP	0.5 h/3 h, 24 h	no	1. Infarct size: P < 0.05 2. LVEDP: P < 0.05 3. + dP/dtmax: P < 0.05 4. LVEF: P > 0.05 5. Caspase-3: P > 0.05 6. Apoptotic rate: P > 0.05 7. Superoxide production: P < 0.01	PKA activity↑/oxidative stress↓/IKK, IκB↓/NF-κB↓
Guo et al. 2014 [38]	SD rats, ND	ND, 220 to 250 g	Pent	MIRI, ligation of LAD	1 μg/kg, 10 min	IV	0.75 h/3 h	DM	1. Infarct size: P < 0.05 2. Caspase-3: P < 0.05 3. SOD: P < 0.05	apoptosis↓/oxidative stress↓
Song et al. 2014 [39]	Queue a (WT): C57B1/6 J mices, ND	8 to 10 weeks, ND	Isoflurane	MIRI, ligation of LAD	2 μg/g, 7 d	IP	0.5 h/3 h, 24 h	renal failure	1. Infarct size: P < 0.05 2. Apoptotic rate: P < 0.01 3. Caspase-3: P < 0.05 4. LVEF: P < 0.01	AdipoR1↑/AMPK↑/iNOS↓/apoptosis↓/oxidative or nitrative stress↓
Song et al. 2014 [39]	Queue b (APN-KO): C57B1/6 J mices, ND	8 to 10 weeks, ND	Isoflurane	MIRI, ligation of LAD	2 μg/g, 7 d	IP	0.5 h/3 h, 24 h	renal failure	1. Infarct size: P < 0.05 2. Apoptotic rate: P < 0.01 3. Caspase-3: P < 0.05 4. LVEF: P < 0.01
Wang et al. 2014 [40]	C57BL/6 J mices, male	8 to 10 weeks, ND	Isoflurane	MIRI, ligation of LAD	2 μg /g, 10 min	IP	0.5 h/3 h, 24 h	no	1. Infarct size: P < 0.01 2. LVEF: P < 0.01	increased APPL1 expression
Gao et al. 2015 [41]	Queue a (WT): C57BL/6 mices, male	6 to 8 weeks, 20 to 25 g	Isoflurane	MIRI, ligation of LAD	0.5 mg/kg, 10 min	IP	0.5 h/3 h, 24 h	no	1. Infarct size: P < 0.01 2. Apoptotic rate: P < 0.05 3. LVEDP: P < 0.05 4. + dP/dtmax: P < 0.05 5. -dP/dtmax: P < 0.05 6. Caspase-3: P < 0.05 7. LVEF: P < 0.05	AMP-activated protein kinase phosphorylation↑/apoptosis↓/TNF-α↓
Gao et al. 2015 [41]	Queue b (APN-KO): C57BL/6 mices, male	6 to 8 weeks, 20 to 25 g	Isoflurane	MIRI, ligation of LAD	0.5 mg/kg, 10 min	IP	0.5 h/3 h,24 h	no	1. Infarct size: P < 0.05 2. Apoptotic rate: P < 0.05 3. Caspase-3: P < 0.01 4. LVEF: P < 0.05
Zhao et al. 2016 [42]	SD rats, ND	ND, 220 to 280 g	Chloral hydrate	MIRI, ligation of LAD	1.8 μg/g, 20 min	IV	0.5 h/2 h	no	1. LDH: P < 0.05 2. MDA: P < 0.05 3. SOD: P < 0.05	Lipid peroxidation↓/free radical scavenging↑
Potenza et al. 2019 [43]	SD rats, male	ND, 250 to 300 g	Pent	MIRI, Langendorff perfusion system	3 μg/mL, 3.5 h	Arterial administration	0.5 h/3 h	no	1. Infarct size: P < 0.05 2. LVEDP: P < 0.01	AMPK, LKB1↑/ eNOS↑/SIRT-1↑
Xing et al. 2020 [44]	SD rats, male	8 to 10 weeks, 250 to 300 g	Pent	MIRI ligation of LAD	5 μg /g, 15 min	IP	0.5 h/2 h	DM	1. Infarct size: P < 0.05	SphK1↓/S1P↓/phosphorylation of NF-κB↓
Wang et al. 2022 [45]	SD rats, male	4 weeks, 180 to 220 g	Pent	MIRI ligation of LAD	5 μg/g, 15 min	IP	0.5 h/2 h	no	1. LDH: P < 0.05	MIF↑/autophagy↓

Pent Pentobarbital sodium, PFU plaque-forming units, IV Intravenous injection, IP Intraperitoneal injection, IS infarct size, AAR area at risk, ND no description, WT wild-type, APN-KO APN gene knockout, AMPK-DN a mutant AMPKα2 subunit, MIRI myocardial ischemia/reperfusion injury, d day, h hour, min minute, LAD left anterior descending branch, SD Sprague–Dawley, COX-2 Cyclooxygenase-2, iNOS inducible NO synthase, gp91^phox nicotinamide adenine dinucleotide phosphate-oxidase, LVEDP left ventricular end-diastolic pressure, + dP/dtmax maximum rate of left ventricular pressure rise, -dP/dtmax maximum rate of left ventricular pressure decrease, LVEF left ventricular ejection fraction, DM diabetes mellitus, SOD superoxide dismutase, NO nitric oxide, NOS nitric oxide synthase, PKA-KO Protein kinase A knockout, CK-MB creatine kinase isoenzymes, APPL1 Recombinant Adiponectin Receptor 1, eNOS endothelial nitric oxide synthase, LKB1 Liver kinase B1, SIRT-1 sirtuin-1, SphK1 Sheath Amino Acid Kinase 1, S1P Sphingosine-1-phosphate, TNF-α tumor necrosis factor alpha, IHC immunohistochemical staining, PPAR-γ Peroxisome proliferator activated receptor, MIF migration inhibitory factor

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