光声成像在关节炎性病变中的潜在临床应用价值

赵辰阳, 朱庆莉, 张睿, 齐振红, 杨萌, 姜玉新

赵辰阳, 朱庆莉, 张睿, 齐振红, 杨萌, 姜玉新. 光声成像在关节炎性病变中的潜在临床应用价值[J]. 协和医学杂志, 2021, 12(2): 232-237. DOI: 10.12290/xhyxzz.20190139
引用本文: 赵辰阳, 朱庆莉, 张睿, 齐振红, 杨萌, 姜玉新. 光声成像在关节炎性病变中的潜在临床应用价值[J]. 协和医学杂志, 2021, 12(2): 232-237. DOI: 10.12290/xhyxzz.20190139
ZHAO Chen-yang, ZHU Qing-li, ZHANG Rui, QI Zhen-hong, YANG Meng, JIANG Yu-xin. The Potential Value of Photoacoustic Imaging in the Assessment of Inflammatory Changes of Joints[J]. Medical Journal of Peking Union Medical College Hospital, 2021, 12(2): 232-237. DOI: 10.12290/xhyxzz.20190139
Citation: ZHAO Chen-yang, ZHU Qing-li, ZHANG Rui, QI Zhen-hong, YANG Meng, JIANG Yu-xin. The Potential Value of Photoacoustic Imaging in the Assessment of Inflammatory Changes of Joints[J]. Medical Journal of Peking Union Medical College Hospital, 2021, 12(2): 232-237. DOI: 10.12290/xhyxzz.20190139

光声成像在关节炎性病变中的潜在临床应用价值

基金项目: 

国家自然科学基金面上项目 61971447

国家自然科学青年基金 81301268

科技部科技合作专项基金 2015DFA30440

北京市自然科学基金 JQ18023

北京市科技新星计划项目 Z131108000413063

北京市科技新星交叉合作计划项目 xxjc201812

详细信息
    通讯作者:

    杨萌  电话:010-69155494, E-mail: yangmeng@pumch.cn

  • 中图分类号: R445.1; R684.3

The Potential Value of Photoacoustic Imaging in the Assessment of Inflammatory Changes of Joints

Funds: 

National Natural Science Foundation of China 61971447

Youth Program of National Natural Science Foundation of China 81301268

S & T Cooperation Program of China 2015DFA30440

Beijing Natural Science Foundation JQ18023

Beijing Nova Program Z131108000413063

Beijing Nova Program Interdisciplinary Cooperation Project xxjc201812

More Information
  • 摘要: 关节炎性疾病发病率逐年升高,给社会经济造成了巨大负担,其早期诊治具有重要意义。光声成像是一种新型光学影像技术,结合了光显像和超声波接收转换的优点,可对关节开展形态学、微血管及功能成像,并可通过外源性造影剂实现分子成像。近10年来,研究人员开发了一系列光声成像仪器,包括独立光声断层成像系统、多模态影像系统等,针对关节炎性疾病开展了动物实验和人体试验,证实其在关节炎性疾病诊断中的价值,其中配备手持光声探头的一体化双模态光声/超声成像系统易于临床转化,有较好的发展前景。
    Abstract: This decade has witnessed a growing prevalence of chronic arthritis all around the world. Early diagnosis of arthritis can be essential for timely treatment and a better prognosis. Photoacoustic imaging (PAI), a multi-functional imaging technique, has been applied for visualizing morphological structures of peripheral joints and small vessels in small joints. Blood oxygenation and other perfusion indexes can also be calculated by PAI, allowing functional evaluation of joint tissues. The exogenous photoacoustic contrast agent that is targeted at some specific molecular biomarkers enables molecular imaging with the use of photoacoustic modalities. Several photoacoustic computed tomography (PACT) modalities have been developed for joint imaging, including some dual-modality systems, which integrate a photoacoustic system with other imaging methods. Taking advantage of the stability and maturity of commercial US units, the co-registration of photoacoustic and ultrasound (PA/US) systems with a portable probe can be an essential step for future clinical translation and promotion. This kind of dual-modal imaging system takes the advantage of compactness and high cost-efficiency of commercial ultrasound systems, and permits noninvasive real-time PA/US imaging simultaneously. The feasi- bility of this type of dual-modality PA/US system in the evaluation of joint disease has been explored and validated by recent studies. Moreover, exogenous contrast agents can facilitate molecular PAI in arthritis by binding specific molecules to those photoacoustic dyes, enabling visualizing inflammatory changes of local joints and delivering therapeutic agents for treating arthritis. Currently, researchers are making efforts to eliminate reflection artifacts, and to enhance the quality and speed of PAI acquisition for diagnosing inflammatory arthritis.
  • 胃癌是起源于胃黏膜上皮细胞的恶性肿瘤,好发于东亚、南美、中美洲及东欧地区[1]。2018年全球范围内新增胃癌患者共计约103万,导致超过78万人死亡,使胃癌成为世界上第五大常见癌症及第三大癌症相关死亡原因[1]

    1927年Warburg等[2]和Burk等[3]首次观察到,即使在氧供良好的环境中,肿瘤细胞也会消耗较多葡萄糖并产生大量乳酸,这一过程被称为“有氧糖酵解”或“温伯格效应”。有氧糖酵解过程中的糖酵解中间体可用于合成核苷酸、氨基酸和脂类,同时产生三磷酸腺苷(adenosine triphosphate,ATP),满足肿瘤和增殖细胞对大分子合成及能量的需求[4]。丙酮酸激酶(pyruvate kinase,PK)是糖酵解过程中的关键限速酶,其亚型丙酮酸激酶M2(PKM2)在多种肿瘤组织及细胞系中呈高表达,研究证明PKM2与肿瘤的发生、增殖、迁移等密切相关[5],但对其在胃癌中的作用及机制认识尚不全面,本文就PKM2在胃癌中的作用及可能的调控机制进行综述。

    哺乳动物的PK存在4种亚型,即PKM1、PKM2、PKL和PKR。PKM1主要存在于能量需求较高的组织中,如骨骼肌、心脏、大脑;PKM2主要存在于高增殖细胞和大部分肿瘤细胞内;PKL主要存在于肝脏、肠道内;PKR主要存在于红细胞内[5]。PKM1、PKM2由PKM基因通过选择性剪接产生,PKL、PKR由PKLR基因编码产生[6]。PKM1、PKL、PKR以稳定的四聚体形式存在;而PKM2则以二聚体和四聚体两种形式存在,二者在肿瘤细胞中的比例不固定,取决于不同的致癌蛋白作用[7]。PKM2二聚体对磷酸烯醇丙酮酸(phosphoenolpyruvate,PEP)的Km值高于其四聚体,因此将PEP转化为ATP和丙酮酸时活性较低,故PKM2二聚体更有利于有氧糖酵解,而四聚体则更有利于通过三羧酸循环产生ATP,PKM2二聚体与四聚体之间的动态平衡为增殖细胞调节自身合成及分解代谢创造了条件[7]

    越来越多的证据表明,PKM2可通过调节有氧糖酵解途径促进肿瘤的发展,在肿瘤发生中发挥关键作用[8-10]。作为糖酵解途径的关键限速酶,PKM2在糖酵解过程中将高能磷酸基从PEP转移至二磷酸腺苷(adenosine diphosphate,ADP),产生ATP和丙酮酸,丙酮酸随后被细胞浆中的乳酸脱氢酶还原为乳酸,或通过呼吸链引导产生高产量的ATP[11]。利用shRNA敲降癌细胞株中的PKM2后,可检测到细胞对葡萄糖的摄取及氧耗增加、乳酸生成减少,重新移入PKM2后这些变化可发生逆转,提示了PKM2促进了细胞增殖和异种移植瘤的形成[10],该研究结果表明PKM2的表达对于有氧糖酵解途径是必要的,并且这种代谢表型为肿瘤细胞提供了选择性生长优势。在缺氧条件下,细胞在缺氧诱导因子-1α(hypoxia inducible factor-1 alpha,HIF-1α)和c-Myc的调控下进行糖酵解,PKM2可与HIF-1α、c-Myc相互作用,共同调节糖酵解途径,促进肿瘤的发展[8-9]

    随着对细胞浆内蛋白成分研究的不断深入,PKM2调节细胞浆内信号转导的作用逐渐被认识。磷脂酰肌醇-3-激酶/蛋白激酶B/雷帕霉素靶蛋白[phosphatidylinositol-3-kinase(PI3K)/protein kinase B(Akt)/the mammalian target of Rapamycin(mTOR),PI3K/Akt/mTOR]信号通路在细胞增殖、迁移及代谢过程中发挥重要调控作用,PKM2是该信号通路的关键下游介质,介导信号通路的转导,共同调控多种肿瘤的发生发展[12-13]。瘦素通过上调PKM2可激活PI3K/Akt信号通路,介导乳腺癌上皮间质转化[14]。多数细胞内信号转导介质通过与磷-酪氨酸残基结合,组成特定的蛋白复合物以完成信号传递,PKM2作为磷-酪氨酸结合蛋白,可与成纤维细胞生长因子受体1、A-Raf、BCR-ABL等多种酪氨酸激酶相互作用,参与调节细胞内信号转导[15]。同时,PKM2还可与mRNA结合,介导翻译调控[16]

    PKM2除调节糖酵解途径及细胞内信号转导外,还参与细胞核内的基因转录与细胞凋亡。Yang等[17]首次发现,表皮生长因子受体可诱导PKM2核转位,细胞核内的PKM2与Y333磷酸化的β-连环蛋白结合,使组蛋白H3磷酸化、周期蛋白D表达增加,揭示了PKM2在细胞核内基因转录中的调控作用。Gao等[18]发现细胞核内的PKM2水平与细胞增殖能力呈正相关,并证实PKM2可通过磷酸化靶点STAT3 Y705激活MEK5转录,进而促进肿瘤的增殖等。PKM2可增加转录共激活因子p300的募集,促进HIF-1α的反式激活,在缺氧环境中重新编程癌细胞代谢[19-20]。PKM2还可与八聚体结合转录因子4(octamer-binding transcription factor 4,Oct4)的C-末端结合,增强Oct4介导的基因转录,促进肿瘤干细胞的自我更新与分化[21]。此外,有研究指出PKM2与细胞凋亡相关,PKM2可磷酸化B细胞淋巴瘤-2(B-cell lymphoma-2, Bcl-2)T69,阻止后者与Cul3的E3连接酶结合,进而抑制细胞凋亡[22]

    研究表明,PKM2在多种肿瘤组织中的表达高于正常组织,且其高表达与患者的不良预后相关[23-25],故推测PKM2表达增强在胃癌发展中发挥重要作用。

    为明确PKM2在胃癌中的表达,Shiroki等[7]研究发现PKM2不仅存在于胃癌组织,在正常胃组织及健康志愿者的胃黏膜内也有表达,且PKM2在胃癌患者及健康志愿者胃黏膜内的表达均高于PKM1,但该研究未发现胃癌发生过程中PKM1与PKM2亚型之间发生转换的证据。Wang等[26]亦证实了PKM2在胃癌组织中的表达高于邻近正常胃组织,并对PKM2表达水平与患者预后进行了Kaplan-Meier分析,发现PKM2高表达者的总生存期(overall survival,OS)为23个月,低表达者的OS为43个月,前者3年及5年生存率均低于后者,存在显著统计学差异。该团队进一步分析了PKM2表达与临床特点的相关性,并证实PKM2表达与胃癌淋巴结转移、肿瘤浸润及临床分期呈正相关,而利用shRNA下调PKM2表达后,体外胃癌细胞的增殖和迁移能力明显受到抑制。这些研究发现也得到了其他研究的进一步证实[27-30]。因此,目前认为PKM2可提高胃癌细胞的增殖、转移能力,其在胃癌组织中的高表达与患者的不良预后、临床及病理分期呈正相关。

    目前普遍认为,包括胃癌在内的多种实体瘤存在低氧区。在缺氧环境中,正常细胞可能出现细胞适应,或P53依赖的细胞凋亡,但肿瘤细胞可能由于获得P53或其他基因突变,以及代谢重编程等变化,能够在缺氧条件下生存、增殖[4, 31]。为分析缺氧条件下葡萄糖代谢相关酶在胃癌增殖中的作用,Kitayama等[32]使用4株耐缺氧胃癌细胞株和4株亲本细胞株,通过RT-PCR检测PKM2在内的代谢相关酶的mRNA表达水平,与亲本细胞株相比,耐缺氧肿瘤细胞株中的PKM2 mRNA表达水平明显增高;分别利用siRNA和紫草素下调PKM2表达水平后,所有细胞株内耐缺氧细胞的生长均受到显著抑制。该研究表明PKM2对于肿瘤细胞耐受缺氧可能发挥着至关重要的作用。此外,在缺氧条件下,PKM2还可调节HIF-1α和c-Myc的活性,促进肿瘤的发展[8-9]

    HIF-1α是一种转录因子,可激活编码蛋白质的基因转录,参与一系列肿瘤生物学方面的关键步骤,包括血管生成、代谢及细胞存活、侵袭和转移等[33-34]。PKM2可促进HIF-1α的反式激活,二者共同组成激活正反馈环,参与肿瘤细胞中葡萄糖代谢的重编程[19-20]。Chen等[35]对早期胃癌、晚期胃癌及浅表性胃炎组织中HIF-1α和PKM2表达进行检测,发现HIF-1α在早期及晚期胃癌组织中的表达均高于胃炎组织,但仅在晚期胃癌组织中的表达有显著性差异;随后将HIF-1α过表达质粒转染胃癌细胞株BGC823,发现HIF-1α的过表达增强了BGC823细胞的生存、侵袭和迁移能力;二甲双胍可抑制HIF-1α及PKM2的表达,降低胃癌细胞的能量供应,从而降低其生存与侵袭能力。

    c-Myc是Myc基因家族的重要成员,在肿瘤能量代谢、调节糖酵解过程中发挥关键作用[9]。Gao等[36]利用慢病毒转染胃癌细胞,分析PKM2、c-Myc下调对细胞增殖、凋亡、迁移及生长信号通路的影响,发现敲除胃癌细胞中的c-Myc可抑制其增殖能力和糖酵解水平,与单独敲除PKM2或c-Myc相比,同时敲除PKM2和c-Myc对胃癌细胞的抑制作用更明显,故推测二者可能存在相互作用,共同调节糖酵解途径。

    PKM2作为PI3K/Akt/mTOR信号通路的下游介质,通过介导该信号通路的活化,促进胃癌的进展[13, 37]。Lu等[37]利用特异性PI3K抑制剂LY294002处理胃癌细胞,发现其可抑制胃癌细胞的增殖,降低细胞活性,并显著增加早期凋亡率;分别用不同浓度的LY294002处理胃癌细胞后,发现p-Akt、p-mTOR、HIF-1α、PKM2的表达均下降,且下降程度呈剂量依赖性。因此,推测LY294002可能通过抑制PI3K/Akt/mTOR/PKM2信号通路进而抑制胃癌细胞的增殖及有氧糖酵解途径。Gao等[36]使用雷帕霉素抑制mTOR表达,结果发现STAT3、c-Myc、GLUT-1蛋白的表达水平明显降低,由此推测mTOR/PKM2和STAT3/c-Myc信号通路可相互作用,共同参与调控胃癌细胞的增殖和糖酵解水平,但其具体机制尚待进一步研究证实。

    细胞凋亡在机体发育、代谢调节、维持组织稳态等过程中发挥重要作用,与肿瘤的发生、发展、预后及耐药性密切相关[38-39]。在细胞内水平,细胞凋亡是由抗凋亡蛋白的丢失或促凋亡蛋白的激活引起,Bcl-2蛋白家族在细胞凋亡中的作用尤为关键[38]。Bcl-2家族包括抗凋亡蛋白(如Bcl-2、Bcl-xL、Mcl-1等),可促进细胞的生存;还包括促凋亡蛋白(如Bid、Bim、Bad、Bax、Bak等),可促使细胞死亡[38]

    Kwon等[40]利用GENT数据库检索了188例胃癌患者肿瘤组织PKM2表达情况,发现胃癌细胞中PKM2与Bcl-xL呈显著正相关;利用siRNA敲降Bcl-xL后,观察到胃癌细胞的生长受到显著抑制。故推测PKM2可能为胃癌细胞中Bcl-xL的重要上游调控因子,通过调控Bcl-xL以减少细胞凋亡,从而促进胃癌细胞增殖。

    PKM2是糖酵解过程中的关键限速酶,在肿瘤的发生、发展过程中发挥至关重要作用。在胃癌细胞中,PKM2与HIF-1α、c-Myc相互影响,共同调节糖酵解途径,通过介导PI3K/Akt/mTOR信号通路活化、调控细胞凋亡等促进胃癌细胞的生长、转移,抑制其细胞凋亡,最终促进胃癌的发展。因此,阻断PKM2这一关键限速酶,可能成为未来胃癌治疗研究的新方向。

    作者贡献:赵辰阳负责文献检索、文章撰写及修订;杨萌、朱庆莉、齐振红、姜玉新负责文章修订;张睿负责文献检索及文章修订。
    利益冲突:  无
  • 表  1   光声计算机断层成像相关研究结果

    超声传感器模式 仪器 实/试验模型 年份
    超声探头环形旋转[15-17] 3D PACT 小鼠、关节炎小鼠、人体手指 2006
    2007
    2008
    超声探头环形旋转[18-19] 3D PACT 手指模型、人体手指 2009
    环形超声传感器列阵[21] SD PACT 人体手指 2011
    半环形超声传感器列阵[22] 3D PACT 人体手指 2014
    弓形超声传感器列阵[23] 3D PACT 人体手指 2012
    PACT:光声计算机断层成像
    下载: 导出CSV

    表  2   双模态PA/US成像系统相关研究

    仪器 研究结果 年份
    PACT/USCT[24] 多波长显示人体手指关节内结构 2016
    PACT/USCT[25] 人体手指关节结构及微血管显像 2017
    PA系统+具备L10-5探头商用超声仪器[26-28] 关节炎小鼠踝关节治疗前后光声信号变化; 人体手指关节结构及微血管显像 2011
    2012
    2013
    具备手持光声探头PA/US成像[30-31] 健康人、关节炎患者手指关节结构及微血管显像 2014
    2017
    具备手持光声探头PA/US成像[33] 关节炎患者手指微血管显像、双波长血氧饱和度测定 2017
    PACT/USCT:光声计算机断层成像/超声计算机断层成像;PA:光声;PA/US:光声/超声成像
    下载: 导出CSV
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  • 收稿日期:  2019-07-14
  • 录用日期:  2019-12-12
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