版纳微型猪近交系同种异体肾移植技术体系的建立

doi:10.12300/j.issn.1674-5817.2025.033

实验动物与比较医学 ›› 2025, Vol. 45 ›› Issue (5): 623-633.DOI: 10.12300/j.issn.1674-5817.2025.033

版纳微型猪近交系同种异体肾移植技术体系的建立

张滢¹^,², 彭自伟¹^,³, 杨畅¹^,³, 王晶¹^,³, 赵红芳¹^,², 陈根⁴, 赵红业¹^,²()(), 魏红江¹^,²^,³()()

^1.云南农业大学云南省小型猪基因编辑与异种器官移植重点实验室, 昆明 650201
^2.云南农业大学动物医学院, 昆明 650201
^3.云南农业大学动物科学技术学院, 昆明 650201
^4.贵州省人民医院器官移植科, 贵阳 550002

收稿日期:2025-03-04 修回日期:2025-06-24 出版日期:2025-10-25 发布日期:2025-10-23
通讯作者:
赵红业（1974—），女，博士，教授，主要从事异种器官移植用供体猪的开发研究。E-mail：hongyezhao@ynau.edu.cn。ORCID：0000-0002-5900-3033

魏红江（1971—），男，博士，教授，主要从事异种器官移植研究。E-mail：weihongjiang@ynau.edu.cn。ORCID：0000-0002-5663-1093
作者简介:张滢（1993—），女，硕士研究生，主要从事异种器官移植相关研究。E-mail：zhangy_128@163.com
彭自伟（1997—），男，硕士研究生，主要从事异种器官移植相关研究。E-mail：1990615582@qq.com
基金资助:
云南省重大科技专项计划“人类重大疾病小型猪模型的构建及平台建设”(202102AA100054);云南省科技人才与平台计划项目“朱宁文专家工作站”(202305AF150131);贵州省卫生健康委科学技术基金项目“低氧介导netmin-1表达调节PI3K/AKT信号通路在肾移植术后肾脏缺血再灌注损伤中的研究”(GZWKJ2023-039)

Establishment of Allogeneic Kidney Transplantation Technical System in Banna Miniature Pig Inbred Strain

ZHANG Ying¹^,², PENG Ziwei¹^,³, YANG Chang¹^,³, WANG Jing¹^,³, ZHAO Hongfang¹^,², CHEN Gen⁴, ZHAO Hongye¹^,²()(), WEI Hongjiang¹^,²^,³()()

^1.Key Laboratory of Gene Editing and Xenotransplantation for Miniature Pigs in Yunnan Province, Yunnan Agricultural University, Kunming 650201, China
^2.College of Animal Medicine, Yunnan Agricultural University, Kunming 650201, China
^3.Faculty of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China
^4.Department of Organ Transplantation, Guizhou Provincial People's Hospital, Guiyang 550002, China

Received:2025-03-04 Revised:2025-06-24 Published:2025-10-25 Online:2025-10-23
Contact: ZHAO Hongye (ORCID: 0000-0002-5900-3033), E-mail: hongyezhao@ynau.edu.cn;
WEI Hongjiang(ORCID: 0000-0002-5663-1093), E-mail: weihongjiang@ynau.edu.cn

摘要/Abstract

摘要：

目的选用版纳微型猪近交系品系建立猪的同种异体肾脏移植手术技术体系，通过血常规检测、肝功能和肾功能检测评估受体猪的生理指标和移植肾脏的功能，为同种异体肾移植手术模型的制备提供参考数据。方法本研究共进行4例同种异体猪肾移植手术，其中1例为健康猪（R）接受单肾移植，2例为猪（DR1和DR2）单肾切除后肾移植，另1例为猪（DR3）双肾切除后肾移植。肾移植术前，采用交叉配血和补体依赖的细胞毒性（complement-dependent cytotoxicity，CDC）实验对供体猪与受体猪进行配型。肾移植术后，定期采集猪外周血样本进行血常规、肝功能和肾功能检测，并通过彩色多普勒超声技术检测移植肾的血流供应情况。实验到达终点后，剖取猪DR1双肾和猪DR3左肾并进行苏木精-伊红（hematoxylin-eosin，HE）染色，以评估未移植肾和移植肾的病理变化。结果受体猪DR1和DR3分别于术后17 d和30 d死亡，受体猪R和DR2在为期30 d的观察期内，状况良好。肝功能和肾功能检测结果显示，猪DR1术后1 d，丙氨酸氨基转移酶（alanine aminotransferase，ALT）水平升高（>1 000 U/L），术后7 d达到高峰（1 300 U/L），术后1 d天门冬氨酸氨基转移酶（aspartate aminotransferase，AST）即达到高峰（>3 000 U/L），术后17 d时ALT和AST的含量仍处于较高水平（ALT，500 U/L；AST，700 U/L）；猪R、DR2和DR3的ALT和AST的含量均于17 d左右恢复到正常水平。猪R血清中的肌酐（creatinine，Crea）含量较为稳定，术后未有上升；猪DR1和DR2的Crea含量在术后第1天时有一过性升高，之后逐渐恢复到正常水平（<100 μmol/L）；猪DR3的Crea水平在术后2~10 d均低于500 μmol/L，术后11~28 d间Crea含量升高，最高达到1 500 μmol/L，表明其肾脏逐渐失去功能。超声结果显示，受体猪R的术前阻力指数（resistive index，RI）为0.91，术后24 d肾皮质、髓质血流信号丰富，RI值为0.88，与未移植前的RI值接近。猪DR2术后17 d时的RI值为0.89，肾皮质血流较差，肾髓质较好。猪DR1在术后17 d时，移植肾中未检测到血流信号。HE染色结果显示，猪DR1未移植的健康右肾结构正常，移植的左肾肾小球结构模糊，细胞核溶解，表明左肾在取出之前已失去功能。猪DR3移植的左肾肾小球和肾小管中可见大量红细胞和淋巴细胞浸润，表明该肾脏移植后可能出现了凝血功能异常和排斥反应。结论本研究以版纳微型猪近交系为实验动物，实施了4例猪-猪的同种异体肾移植手术，术后借助血常规、肝功能、肾功能、彩色多普勒超声以及病理学检测，对受体猪的生理指标和移植肾脏的功能展开监测。本研究构建的猪-猪同种异体肾移植技术体系，可为临床医生开展肾移植手术奠定基础。

关键词: 版纳微型猪, 近交系, 同种异体肾移植, 技术体系

Abstract:

Objective To establish a technical system for allogeneic kidney transplantation surgery in pigs using the Banna miniature pig inbred strain, and to evaluate it through routine blood tests, liver and kidney function tests, thus providing reference data for the preparation of allogeneic kidney transplantation models. Methods A total of 4 cases of allogeneic kidney transplantation surgeries were performed, including 1 case of single kidney transplantation in a healthy pig, 2 cases of kidney transplantation after unilateral nephrectomy, and 1 case of kidney transplantation after bilateral nephrectomy. Before kidney transplantation, cross-matching and complement-dependent cytotoxicity (CDC) tests were used for matching between donor and recipient pigs. After kidney transplantation, peripheral blood samples were regularly collected from pigs for routine blood tests, liver function tests, and kidney function tests, and color Doppler ultrasound technology was used to detect blood supply to the transplanted kidneys. After reaching the experimental endpoint, both kidneys of pig DR1 and the left kidney of pig DR3 were collected and hematoxylin-eosin (HE) staining was performed to evaluate pathological changes in the transplanted kidneys. Results Recipient pigs DR1 and DR3 died at 17 days and 30 days after surgery respectively, while recipient pigs R and DR2 remained in good condition during the 30-day observation period. The results of liver and kidney function test showed that in pig DR1, alanine aminotransferase (ALT) levels increased on postoperative day 1 (>1 000 U/L), peaked on postoperative day 7 (1 300 U/L), and aspartate aminotransferase (AST) levels peaked on postoperative day 1 (>3 000 U/L). On postoperative day 17, ALT and AST levels remained high (ALT, 500 U/L; AST, 700 U/L). In pigs R, DR2, and DR3, ALT and AST levels returned to normal around day 17. Serum creatinine (Crea) levels in pig R remained stable without postoperative increase. Crea levels in pigs DR1 and DR2 showed transient elevation on postoperative day 1, then gradually returned to normal (<100 μmol/L). Crea levels in pig DR3 remained below 500 μmol/L from postoperative days 2-10, but increased between days 11-28, reaching up to 1 500 μmol/L, indicating gradual loss of kidney function. Ultrasound results showed that the preoperative resistive index (RI) of recipient pig R was 0.91. On postoperative day 24, renal cortex and medulla showed abundant blood flow signals with RI value of 0.88, which was close to the pre-transplantation RI value. For pig DR2, the RI value on postoperative day 17 was 0.89, with poor renal cortex blood flow and relatively good renal medulla blood flow. In pig DR1 on postoperative day 17, no blood flow signals were detected in the transplanted kidney. HE staining results showed that the non-transplanted healthy right kidney of pig DR1 had normal structure, while the transplanted left kidney showed blurred glomerular structure and nuclear dissolution, indicating that the left kidney had lost function before removal. In the transplanted left kidney of pig DR3, large numbers of red blood cells and lymphocyte infiltration were observed in glomeruli and renal tubules, indicating possible coagulation dysfunction and rejection reactions after kidney transplantation. Conclusion Banna miniature pig inbred strain is used as experimental animals to perform four cases of allogeneic pig-to-pig kidney transplantation. The physiological parameters of the recipient pig and the function of the transplanted kidney are monitored after surgery using routine blood tests, liver and kidney function tests, color Doppler ultrasound, and pathological examinations. The allogeneic pig-to-pig kidney transplantation technical system established in the study can provide a foundation for clinicians to conduct kidney transplantation surgeries.

Key words: Banna miniature pig, Inbred strain, Allogeneic kidney transplantation, Technical system

中图分类号:

Q95-33

张滢,彭自伟,杨畅,等. 版纳微型猪近交系同种异体肾移植技术体系的建立[J]. 实验动物与比较医学, 2025, 45(5): 623-633. DOI: 10.12300/j.issn.1674-5817.2025.033.

ZHANG Ying,PENG Ziwei,YANG Chang,et al. Establishment of Allogeneic Kidney Transplantation Technical System in Banna Miniature Pig Inbred Strain[J]. Laboratory Animal and Comparative Medicine, 2025, 45(5): 623-633. DOI: 10.12300/j.issn.1674-5817.2025.033.

图/表 7

表1 肾移植手术的实验动物分组

Table 1 Experimental animal grouping for kidney trans-plantation surgery

组别

Group

受体猪编号

Recipient pig number

供体猪编号

Donor pig number

健康猪接受单肾移植

Single kidney transplantation in a healthy pig

单肾切除后肾移植

Kidney transplantation after unilateral nephrectomy

DR1

DR2

DR1

双肾切除后肾移植

Kidney transplantation after

bilateral nephrectomy

DR3

图1 供体猪和受体猪的交叉配血实验结果注：A，猪R血清和猪D红细胞的配血结果；B，猪D血清和猪R红细胞的配血结果；C，猪DR1血清和猪DR2红细胞的配血结果；D，猪DR2血清和猪DR1红细胞的配血结果。标尺为50 μm。

Figure 1 Cross-matching test results between donor and recipient pigsNote： A， Cross-matching results between pig R serum and pig D red blood cells； B， Cross-matching results between pig D serum and pig R red blood cells； C， Cross-matching results between pig DR1 serum and pig DR2 red blood cells； D， Cross-matching results between pig DR2 serum and pig DR1 red blood cells. Scale bar = 50 μm.

图 2 供体猪和受体猪配型的CDC实验结果注：A～B，供体猪C2、C1、D与受体猪R的CDC配型流式图及其细胞死亡率；C～D，供体猪C2、C1、DR2与受体猪DR1的CDC配型流式图及其细胞死亡率；E～F，供体猪C2、C1、DR与受体猪DR2的CDC配型流式图及其细胞死亡率。

Figure 2 Results of the CDC assay between donor and recipient pigsNote： A-B， Flow cytometry results and cell death rate for the donor pig C2， C1， D versus recipient pig R in CDC matching test； C-D， Flow cytometry results and cell death rate for donor pig C2， C1， DR2 versus recipient pig DR1 in CDC matching test； E-F， Flow cytometry results and cell death rate for donor pig C2， C1， DR versus recipient pig DR2 in CDC matching test.

表2 同种异体猪肾移植手术情况

Table 2 Allogeneic pig kidney transplantation surgery conditions

供体猪或受体猪编号 Donor/recipient number	供体肾重量/g Donor kidney weight/g	热缺血时间 Warm ischemia time	冷缺血时间 Cold ischemia time	开放循环后开始排尿时间 Time to initiate urination after opening the loop
R	118.9	1 min 5 s	4 h 35 min	2 min
DR1	87.3	2 min 5 s	1 h 15 min	5 min
DR2	115.7	5 min	6 h 23 min	3 min
DR3	100.5	4 min	8 h 18 min	4 min

图3 肾移植前后供体猪和受体猪的血常规和肝功能、肾功能检测注：WBC，白细胞计数；Lym，淋巴细胞计数；Neu，中性粒细胞计数；ALT，丙氨酸氨基转移酶；AST，天门冬氨酸氨基转移酶；Crea，肌酐。血液采集过程中猪的采血有一定的难度，采血过程中会存在应激以及检测误差等，导致某个时间点的数据缺失。

Figure 3 Routine blood， liver， and kidney function test results of donor and recipient pigs before and after kidney transplantationNote： WBC， White blood cell count； Lym， Lymphocyte count； Neu， Neutrophil count； ALT， Alanine aminotransferase； AST， Aspartate aminotransferase； Crea， Creatinine. Blood collection in pigs is difficult and may cause stress and detection errors， leading to missing data at certain time points.

图4 供体猪和受体猪的肾脏血流监测注：A，猪R术前的超声图像；B，猪R术后24 d的超声图像；C，DR1猪术后17 d的超声图像；D，猪DR2术后17 d的超声图像。

Figure 4 Renal blood flow monitoring of donor and recipient pigsNote： A， Preoperative ultrasound image of pig R； B， Postoperative ultrasound image of pig R at 24 days； C， Postoperative ultrasound image of pig DR1 at 17 days； D， Postoperative ultrasound image of pig DR2 at 17 days.

图5 移植肾脏大体观察和HE染色注：A~C，依次为猪DR1未移植肾（对侧肾）、猪DR1移植肾和猪DR3移植肾脏的大体观；D~F，依次为猪DR1未移植肾（对侧肾）、猪DR1移植肾和猪DR3移植肾脏的剖面观；G，猪DR1未移植肾（对侧肾）HE染色结果；H，猪DR1移植侧肾HE染色结果，黑色方框内指示的是发生核溶解的肾小球；I，猪DR3移植肾HE染色结果，红色方框内指示的是淋巴细胞，黑色方框内指示的是红细胞。标尺为50 μm。

Figure 5 Gross observation and HE staining of transplanted kidneyNote： A-C， Gross appearance of the non-transplanted kidney （contralateral kidney） of pig DR1， transplanted kidney of pig DR1， and transplanted kidney of pig DR3， respectively； D-F， Sectional views of the non-transplanted kidney （contralateral kidney） of pig DR1， transplanted kidney of pig DR1， and transplanted kidney of pig DR3， respectively； G， HE staining of the non-transplanted kidney （contralateral kidney） of pig DR1； H， HE staining of the transplanted kidney of pig DR1， with glomeruli showing nuclear dissolution indicated by black boxes； I， HE staining of the transplanted kidney of pig DR3， with lymphocytes indicated by red boxes and red blood cells indicated by black boxes. Scale bar = 50 μm.

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版纳微型猪近交系同种异体肾移植技术体系的建立

Establishment of Allogeneic Kidney Transplantation Technical System in Banna Miniature Pig Inbred Strain

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