The variations of nephrons and relevant function factors between hibernating and non-hibernating Daurian ground squirrels

doi:10.16829/j.slxb.150587

Abstract

Abstract:

Hibernation is an adaptive survival strategy through which the hibernating species copes with months of low ambient temperature and a lack of food. The Daurian ground squirrel (Spermophilus dauricus) is a typical fat-storing hibernator. To further investigate the renal adaptive mechanisms of hibernators, the nephronal morphology changes and the concentrations of serum creatinine, urine and antidiuretic hormone (ADH) were examined during summer active (July), winter hibernating (December), and early spring arousal (March) periods in the Daurian ground squirrel by the means of histology, blood biochemical analysis, and enzyme-linked immunosorbent assay. The gene expression of aquaporins (AQP1, AQP2,and AQP3), ADH receptor (V2R), and endothelial nitric oxide synthase (eNOS) were also examined by the means of real-time PCR. The density of glomerulus, relative diameter of distal tubules and proximal tubules, and ratio of corticomedullary proximal tubules to distal tubules were found to be lower during hibernating and arousal periods compared to active period. The concentration of serum creatinine and urine increased significantly during hibernating period compared to those during active and arousal periods. The serum ADH concentration and V2R gene expression level decreased significantly during hibernating period compared to those during active periods. The gene expression of AQP1 during hibernating period was higher than that during arousal period, and the AQP3 gene expression was lower than that during active period, while the AQP2 gene expression level did not change significantly. The eNOS gene expression during hibernating period was lower than that during arousal period. These results indicate that the Daurian ground squirrel lowered its renal function during hibernation. The aquaporins, eNOS, and ADH show functional adjustments to adapt to different periods. These results might provide a better understanding of the renal adaptation mechanism in hibernating animals.

Key words: Daurian ground squirrel, Hibernation, Kidney, Aquaporins, Antidiuretic hormone

摘要：

冬眠是动物应对冬季低温和食物匮乏的一种生存策略。达乌尔黄鼠 (Spermophilus dauricus) 是典型的贮脂类冬眠动物。为研究冬眠动物肾脏的适应机制，本实验采用组织学、血液生化分析及酶联免疫方法检测了夏季活动期 (7月) 、冬眠期 (12月) 和早春出眠后 (3月) 达乌尔黄鼠肾单位形态学及血清肌酐、尿素和抗利尿激素 (ADH) 的变化，并用qPCR方法检测了肾脏水通道蛋白基因 (AQP1、AQP2和AQP3)、ADH受体 (V2R) 及内皮型一氧化氮合酶基因 (eNOS) 的表达。结果发现，冬眠期和早春出眠期的达乌尔黄鼠肾小球密度、近曲小管和远曲小管的相对管径、皮质部近曲小管数与远曲小管数比值均低于夏季活动期；冬眠期血清肌酐和尿素浓度高于夏季活动期和早春出眠期，ADH浓度及其受体V2R基因表达低于夏季活动期；冬眠期AQP1基因表达高于早春出眠期，AQP3基因表达低于夏季活动期，AQP2基因表达无显著差异；冬眠期eNOS基因表达低于早春出眠期。这些结果表明冬眠的达乌尔黄鼠表现出较低的肾功能；不同时期的水通道蛋白，eNOS及ADH表现出适应性的功能调节。该实验结果丰富了对冬眠动物肾脏适应机制的认识。

关键词: 达乌尔黄鼠, 冬眠, 肾脏, 水通道蛋白, 抗利尿激素

CLC Number:

Q494

Xiujing ZHANG, Heng WANG, Qiumei ZHONG, Chenxi YANG, Jianli WANG. The variations of nephrons and relevant function factors between hibernating and non-hibernating Daurian ground squirrels[J]. ACTA THERIOLOGICA SINICA, 2022, 42(6): 677-686.

张修静, 王恒, 钟秋梅, 杨晨希, 王建礼. 冬眠和非冬眠状态达乌尔黄鼠肾单位及相关功能因子的比较[J]. 兽类学报, 2022, 42(6): 677-686.

Figures/Tables 5

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目标基因 Target gene	引物序列（5′-3′） Primer sequence （5′-3′）	片段大小 Product length （bp）
β-actin forward	ACTCGTCGTACTCCTGCTT	223
β-actin reverse	AAGACCTCTATGCCAACACC	223
AQP1 forward	TCAACCCAGCCGTCACAC	189
AQP1 reverse	CCTGGCCTGAGTTCACAC	189
AQP2 forward	GAGATCACGCCAGCAGAAAT	183
AQP2 reverse	GAAACCGATGGAGAGAGCAG	183
AQP3 forward	GTGATGTTTGGCTGTGGGTC	161
AQP3 reverse	GCAAAGGTCACAGCAGGATT	161
V2R forward	CGTCAAGTACCTGCAGATGG	171
V2R reverse	CTGAGAAGAAGCGAGAAGGC	171
eNOS forward	CACCGGCATCAGACCACA	189
eNOS reverse	GCCGACTCTGTACTTTCCTT	189

目标基因 Target gene	引物序列（5′-3′） Primer sequence （5′-3′）	片段大小 Product length （bp）
β-actin forward	ACTCGTCGTACTCCTGCTT	223
β-actin reverse	AAGACCTCTATGCCAACACC	223
AQP1 forward	TCAACCCAGCCGTCACAC	189
AQP1 reverse	CCTGGCCTGAGTTCACAC	189
AQP2 forward	GAGATCACGCCAGCAGAAAT	183
AQP2 reverse	GAAACCGATGGAGAGAGCAG	183
AQP3 forward	GTGATGTTTGGCTGTGGGTC	161
AQP3 reverse	GCAAAGGTCACAGCAGGATT	161
V2R forward	CGTCAAGTACCTGCAGATGG	171
V2R reverse	CTGAGAAGAAGCGAGAAGGC	171
eNOS forward	CACCGGCATCAGACCACA	189
eNOS reverse	GCCGACTCTGTACTTTCCTT	189

参数 Parameters	活动期 Active period （n = 6）	冬眠期 Hibernating period （n = 6）	出眠期 Arousal period （n = 5）
皮质浅层近曲小管相对管径 RDPS	0.94 ± 0.01^a	0.82 ± 0.02^b	0.75 ± 0.02^c
皮质中层近曲小管相对管径 RDPM	0.94 ± 0.01^a	0.80 ± 0.02^b	0.75 ± 0.02^c
髓旁近曲小管相对管径 RDPP	0.93 ± 0.01^a	0.80 ± 0.01^b	0.75 ± 0.02^c
皮质浅层远曲小管相对管径 RDDS	1.23 ± 0.02^a	1.04 ± 0.01^b	0.94 ± 0.01^c
皮质中层远曲小管相对管径 RDDM	1.23 ± 0.01^a	1.05 ± 0.01^b	0.94 ± 0.02^c
髓旁远曲小管相对管径 RDDP	1.22 ± 0.01^a	1.03 ± 0.01^b	0.94 ± 0.01^c
皮质部近曲小管数 / 远曲小管数 CPT / CDT	2.74 ± 0.05^a	2.36 ± 0.14^b	2.73 ± 0.12^a
近髓质近曲小管数 / 远曲小管数 JPT / JDT	3.83 ± 0.13^a	3.39 ± 0.12^a	3.79 ± 0.17^a
肾小球密度 GD （ind./mm²）	8.82 ± 0.52^a	7.22 ± 0.34^b	7.29 ± 0.49^b

参数 Parameters	活动期 Active period （n = 6）	冬眠期 Hibernating period （n = 6）	出眠期 Arousal period （n = 5）
皮质浅层近曲小管相对管径 RDPS	0.94 ± 0.01^a	0.82 ± 0.02^b	0.75 ± 0.02^c
皮质中层近曲小管相对管径 RDPM	0.94 ± 0.01^a	0.80 ± 0.02^b	0.75 ± 0.02^c
髓旁近曲小管相对管径 RDPP	0.93 ± 0.01^a	0.80 ± 0.01^b	0.75 ± 0.02^c
皮质浅层远曲小管相对管径 RDDS	1.23 ± 0.02^a	1.04 ± 0.01^b	0.94 ± 0.01^c
皮质中层远曲小管相对管径 RDDM	1.23 ± 0.01^a	1.05 ± 0.01^b	0.94 ± 0.02^c
髓旁远曲小管相对管径 RDDP	1.22 ± 0.01^a	1.03 ± 0.01^b	0.94 ± 0.01^c
皮质部近曲小管数 / 远曲小管数 CPT / CDT	2.74 ± 0.05^a	2.36 ± 0.14^b	2.73 ± 0.12^a
近髓质近曲小管数 / 远曲小管数 JPT / JDT	3.83 ± 0.13^a	3.39 ± 0.12^a	3.79 ± 0.17^a
肾小球密度 GD （ind./mm²）	8.82 ± 0.52^a	7.22 ± 0.34^b	7.29 ± 0.49^b

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