AbstractThe view of neutrophils has shifted from simple phagocytic cells, whose main function is to kill pathogens, to very complex cells that are also involved in immune regulation and tissue repair. These cells are essential for maintaining and regaining tissue homeostasis. Neutrophils can be viewed as double-edged swords in a range of situations.

摘要中性粒细胞的观点已经从主要功能是杀死病原体的简单吞噬细胞转变为也参与免疫调节和组织修复的非常复杂的细胞。这些细胞对于维持和恢复组织稳态至关重要。在一系列情况下，中性粒细胞可以被视为双刃剑。

The potent killing machinery necessary for immune responses to pathogens can easily lead to collateral damage to host tissues when inappropriately controlled. Furthermore, some subtypes of neutrophils are potent pathogen killers, whereas others are immunosuppressive or can aid in tissue healing. Finally, in tumor immunology, many examples of both protumorigenic and antitumorigenic properties of neutrophils have been described.

当不适当的控制时，对病原体的免疫反应所必需的有效杀伤机制很容易导致宿主组织的附带损伤。此外，一些中性粒细胞亚型是有效的病原体杀手，而另一些亚型是免疫抑制性的或可以帮助组织愈合。最后，在肿瘤免疫学中，已经描述了嗜中性粒细胞的促肿瘤发生和抗肿瘤发生特性的许多例子。

This has important consequences for cancer therapy, as targeting neutrophils can lead to either suppressed or stimulated antitumor responses. This review will discuss the current knowledge regarding the pro- and antitumorigenic roles of neutrophils, leading to the concept of a confused state of neutrophil-driven pro-/antitumor responses..

这对癌症治疗具有重要影响，因为靶向嗜中性粒细胞可导致抑制或刺激的抗肿瘤反应。这篇综述将讨论目前关于嗜中性粒细胞的促肿瘤和抗肿瘤作用的知识，导致中性粒细胞驱动的促肿瘤/抗肿瘤反应的混乱状态的概念。。

IntroductionNeutrophils as double-edged swords in the effector phase of the immune responseThe effector cells of the immune system have two faces as their beneficial functions are carried out via tissue damaging mechanisms [1]. The toxic effector functions associated with antimicrobial defense easily cause collateral damage to the host tissue, and in the case of hyperactivation, the increased damage outweighs the benefits [2].

引言中性粒细胞作为免疫反应效应阶段的双刃剑免疫系统的效应细胞具有两面性，因为它们的有益功能是通过组织损伤机制进行的。与抗菌防御相关的毒性效应功能很容易对宿主组织造成附带损害，在过度活化的情况下，增加的损害超过了益处（2）。

In addition to toxic effector neutrophils, other neutrophil phenotypes appear during wound healing, which aids in angiogenesis and tissue repair [3]. Tumors have also been described as wounds that never heal, and they can hijack the normal wound healing response for their own growth and spread [4]. A third two-sided role of neutrophils is found in tumor immunology, as the cells can be pro- and antitumorigenic depending on the phenotype of the neutrophil, the timing and the tumor type.Most mechanistic studies on the role of neutrophils in tumorigenesis are performed with mouse models.

除了毒性效应中性粒细胞外，其他中性粒细胞表型也出现在伤口愈合过程中，这有助于血管生成和组织修复。肿瘤也被描述为永远不会愈合的伤口，它们可以劫持正常的伤口愈合反应，使其自身生长和扩散。中性粒细胞的第三个双向作用是在肿瘤免疫学中发现的，因为根据中性粒细胞的表型，时间和肿瘤类型，细胞可以是促肿瘤和抗肿瘤的。大多数关于嗜中性粒细胞在肿瘤发生中的作用的机制研究是用小鼠模型进行的。

Unfortunately, the neutrophil compartment in mice is very different with respect to neutrophil functions. It is beyond the scope of this article to review them all [5, 6]. However, some differences, such as the number of cells, kinetics, receptors, phenotypes and nuclear morphology, are crucial for the translation of murine data related to neutrophil-mediated tumor immunology to humans.

不幸的是，小鼠的中性粒细胞区室在中性粒细胞功能方面非常不同。对它们进行审查超出了本文的范围[5，6]。然而，一些差异，例如细胞数量，动力学，受体，表型和核形态，对于将与嗜中性粒细胞介导的肿瘤免疫学相关的鼠数据翻译为人类至关重要。

First, the number of neutrophils in the peripheral murine blood is much lower (≈10% in spf mice vs ≈60% in humans) [5, 6]. The differentiation time from the last division in the bone marrow and exit to the blood is <1 day in mice and 6 days in humans [7, 8]. Although the lifespan of human neutrophils is debated, as discussed later in this review, it is generally accepted that human neu.

首先，外周小鼠血液中嗜中性粒细胞的数量要低得多（spf小鼠约为10%，人类约为60%）[5,6]。从骨髓最后一次分裂到血液的分化时间在小鼠中小于1天，在人类中小于6天[7，8]。尽管人们对人类中性粒细胞的寿命存在争议，但正如本综述后面所讨论的，人们普遍认为人类中性粒细胞的寿命。

The mitotic pool of proliferative progenitors

增殖祖细胞的有丝分裂池

Despite the multitude of studies focusing on the neutrophil compartment in the bone marrow, little if any consensus is present on the pool sizes of the different neutrophil progenitors. The pool sizes of early progenitors, multipotential progenitors and myeloblasts are clearly small, and a large proportion of the more undifferentiated progenitor cells are not in the cycle [32].

尽管有大量研究关注骨髓中的中性粒细胞区室，但对于不同中性粒细胞祖细胞的池大小几乎没有共识。早期祖细胞、多能祖细胞和成髓细胞的池大小明显较小，大部分未分化的祖细胞不在周期中。

Therefore, these cells are important in maintaining the compartment but are not the main source of neutrophils, as the ‘flux’ through these cells is limited [9, 32, 33]. The largest population of neutrophil progenitors that highly proliferate are promyelocytes [19, 34]. As such, these promyelocytes are the main producers of cells of the mature neutrophil compartment, and their kinetics are rate limiting [9].

因此，这些细胞在维持隔室中很重要，但不是中性粒细胞的主要来源，因为通过这些细胞的“通量”是有限的[9,32,33]。高度增殖的中性粒细胞祖细胞数量最多的是早幼粒细胞[19，34]。因此，这些早幼粒细胞是成熟中性粒细胞区室细胞的主要生产者，其动力学是限速的。

Unfortunately, the size of the pool of promyelocytes is currently unclear. Multiple studies applying different technologies have attempted to estimate this number, and the data range is approximately twofold from 44 × 109 cells/individual to 72 × 109 cells [9, 25, 34]. There are multiple reasons for this difference.

不幸的是，早幼粒细胞库的大小目前尚不清楚。应用不同技术的多项研究试图估计这个数字，数据范围大约是44×109个细胞/个体到72×109个细胞的两倍[9,25,34]。这种差异有多种原因。

An important issue is the source of the bone marrow, as this tissue consists of a fluid phase and a bone niche. Many studies use bone marrow aspirates, which might overrepresent cells from the fluid phase and be relatively deficient in cells present in the bone niche [35]. Another way of collecting bone marrow is through trephine biopsies [36], but these biopsies are difficult to quantify and extrapolate.

一个重要的问题是骨髓的来源，因为这种组织由液相和骨龛组成。许多研究使用骨髓抽吸物，这可能会使液相细胞过度表达，而骨龛中存在的细胞相对缺乏。另一种收集骨髓的方法是通过环钻活检（36），但这些活检很难量化和推断。

Few studies have compared the two methods, but those that have been published conclude that the percentages of different progenitors in aspirates and trephine biopsies are similar [36]. Another complicating factor in the interpretation of bone marrow aspirates is hemodilution of .

很少有研究比较这两种方法，但已发表的研究得出结论，抽吸物和环钻活检中不同祖细胞的百分比相似（36）。解释骨髓抽吸物的另一个复杂因素是血液稀释。

The postmitotic pool of nonproliferative progenitors

非增殖祖细胞的有丝分裂后池

Next, the cells lose their capacity to divide and enter a differentiation/maturation program via meta-myelocytes and banded cells toward mature neutrophils that are mobilized to peripheral blood. For reasons similar to those for promyelocytes, only a few studies have determined the absolute pool sizes of postmitotic progenitors [28, 38].

接下来，细胞失去分裂的能力，并通过间充质骨髓细胞和带状细胞向动员到外周血的成熟嗜中性粒细胞进入分化/成熟程序。由于与早幼粒细胞相似的原因，只有少数研究确定了有丝分裂后祖细胞的绝对池大小[28，38]。

Most studies describe percentages of progenitors in aspirates rather than absolute numbers and show that the pool sizes of myelocytes, metamyelocytes and banded cells are similar [19, 25, 32]. The issue of the pool size of the last step, mature neutrophils, is unresolved. The estimates in the literature range from 99 × 109 cells to 415 × 109 cells in the total bone marrow [19, 25, 34, 39,40,41].

大多数研究描述了抽吸物中祖细胞的百分比，而不是绝对数量，并表明骨髓细胞，间充质细胞和带状细胞的池大小相似[19,25,32]。最后一步成熟中性粒细胞的池大小问题尚未解决。文献中的估计范围从总骨髓中的99×109个细胞到415×109个细胞[19,25,34,39,40,41]。

Together, a twofold difference in the estimated promyelocyte pool and a fourfold difference in the estimated mature neutrophil pool result in an eightfold range of estimated production. This lack of consensus precludes a detailed understanding of the neutrophil compartment..

总之，估计的早幼粒细胞库的两倍差异和估计的成熟中性粒细胞库的四倍差异导致估计产量的八倍范围。由于缺乏共识，无法对中性粒细胞区室进行详细了解。。

Basic kineticsIn addition to determining pool sizes, measuring the kinetics and tissue distribution can help clarify the potential roles and limitations of mature neutrophils. In particular, the relative longevity (t½ of multiple days) of neutrophils supports their role in immune regulation and in tumor immunology.

基本动力学除了确定池大小外，测量动力学和组织分布还有助于阐明成熟中性粒细胞的潜在作用和局限性。特别是，中性粒细胞的相对寿命（多天的t½）支持它们在免疫调节和肿瘤免疫学中的作用。

However, in the late fifties/early sixties of the last century, sizeable literature led to textbook knowledge that human neutrophils are short-lived in the peripheral blood (t½ of 7 h) [34, 42,43,44]. All these studies used essentially the same experimental approach of labeling neutrophils in vivo or in vitro with radioactive diisopropyl fluorophosphate (DFP), which irreversibly binds to neutrophil elastase [45] and followed the decay in radioactivity in blood neutrophils in time.

然而，在上个世纪五十年代末/六十年代初，大量文献导致教科书上的知识，即人类中性粒细胞在外周血中的寿命很短（t½为7小时）[34,42,43,44]。所有这些研究都使用了基本相同的实验方法，在体内或体外用放射性氟磷酸二异丙酯（DFP）标记嗜中性粒细胞，DFP不可逆地与嗜中性粒细胞弹性蛋白酶（45）结合，并随着血液嗜中性粒细胞放射性的衰减。

The implicit underlying hypothesis was that the half-life in peripheral blood equals the death of the cells in the neutrophil compartment. However, an alternative hypothesis of dilution of cells in a large population of neutrophils outside the peripheral blood (e.g., bone marrow) can explain the data at least equally well [9].More recent analyses applying stable isotope labeling in humans also did not support such a short half-life [7] but did not lead to a consensus on the lifetime of a mature neutrophil [8], leading to estimates between 1 and 5.6 days.

隐含的潜在假设是外周血中的半衰期等于中性粒细胞区室中细胞的死亡。然而，在外周血（例如骨髓）外的大量嗜中性粒细胞中稀释细胞的替代假设可以至少同样很好地解释数据（9）。最近在人类中应用稳定同位素标记的分析也不支持如此短的半衰期，但并没有就成熟中性粒细胞的寿命达成共识，导致估计在1至5.6天之间。

The reason for these contradictory findings lies in the uncertainties with respect to pool sizes and the unknown kinetics of promyelocytes [46, 47, 10].Tissue distributionApart from pool size and kinetics, the tissue distribution of the neutrophil compartment in homeostasis has not been well described.

这些矛盾发现的原因在于池大小的不确定性和早幼粒细胞的未知动力学[46，47，10]。组织分布从池的大小和动力学来看，中性粒细胞区室在体内平衡中的组织分布尚未得到很好的描述。

Here, two mutually exclusive hypotheses exist: the ‘tissue surveillance’ model and the ‘peripheral blood surveillance’ model.The fir.

在这里，存在两个相互排斥的假设：“组织监测”模型和“外周血监测”模型。冷杉。

Antitumor responses are characterized by immune mechanisms typical for chronic conditions and seem to be modulated mainly by N-MDSCs. However, it is possible that suppressive neutrophils characterized by CD11bbright/CD11cbright/CD62Ldim that are quickly mobilized during acute and chronic inflammation [111, 167] are also involved in the suppression of T-cell responses in and around tumors [168].

抗肿瘤反应的特征在于慢性病典型的免疫机制，并且似乎主要由N-MDSC调节。然而，在急性和慢性炎症期间迅速动员的以CD11bbright/CD11cbright/CD62Ldim为特征的抑制性中性粒细胞也可能参与抑制肿瘤内和周围的T细胞反应[111167]。

Although this concept has not been directly tested, CD62Llow neutrophils have been connected with immune suppression in and near tumors [169]. L-selectin is a complex marker because it is quickly shed upon stimulation of cells [170]. This makes it difficult to discriminate between CD62Llow cells originating from the bone marrow and cells that have been activated near or in the tumor.

虽然这一概念尚未直接测试，但CD62Llow中性粒细胞与肿瘤及其附近的免疫抑制有关（169）。L-选择素是一种复杂的标记物，因为它在刺激细胞时会迅速脱落。这使得很难区分源自骨髓的CD62Llow细胞和在肿瘤附近或肿瘤中被激活的细胞。

However, CD62Llow cells have been shown to be potent suppressors of T-cell function through the formation of an immune synapse and the production of ROS [111, 171]. This finding is very reminiscent of the suppressive mechanisms described for N-MDSCs. Notably, CD11bbright/CD11cbright/CD62Ldim cells are not immature but are similar in age to normal neutrophils and are 2 days older than banded neutrophils [128].Suppressive neutrophils characterized by differential expression of CD10CD10 (also called neprilysin, CALLA, neutral endopeptidase and enkephalinase) is a complex marker, as it is both a marker of late differentiation [107, 172] and an activation marker [108, 173].

然而，通过形成免疫突触和产生ROS，CD62Llow细胞已被证明是T细胞功能的有效抑制剂[111171]。这一发现让人想起了针对N-MDSC描述的抑制机制。值得注意的是，CD11bbright/CD11cbright/CD62Ldim细胞并不不成熟，但与正常嗜中性粒细胞的年龄相似，比带状嗜中性粒细胞大2天（128）。以CD10CD10（也称为中性溶酶，CALLA，中性内肽酶和脑啡肽酶）差异表达为特征的抑制性中性粒细胞是一种复杂的标志物，因为它既是晚期分化的标志物[107172]又是活化标志物[108173]。

The enhanced expression of CD10 upon stimulation in vitro follows the expression of Mac-1 (CD11b/CD18), suggesting that both markers are expressed in the same subcellular compartment [108, 174]. In addition to being expressed on the cell surface at low levels in resting neutrophils, intracellular Mac-1 is located in secretory vesicles .

体外刺激后CD10的增强表达遵循Mac-1（CD11b/CD18）的表达，表明两种标记物均在相同的亚细胞区室中表达[108174]。除了在静息中性粒细胞中以低水平在细胞表面表达外，细胞内Mac-1还位于分泌囊泡中。

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Respiratory Medicine and Center for Translational Immunology, University Medical Center Utrecht, Utrecht, The NetherlandsLeo Koenderman & Nienke VrisekoopAuthorsLeo KoendermanView author publicationsYou can also search for this author in.

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Keywordsneutrophilimmune suppressioncancertumor-associated neutrophilsconfused immune responsemyeloid derived suppressor cells

关键词嗜中性粒细胞免疫抑制癌相关嗜中性粒细胞感染的免疫反应髓样来源的抑制细胞