Properties and units in the clinical laboratory sciences. Part XXVIII. NPU codes for characterizing subpopulations of the hematopoietic lineage, described from their clusters of differentiation molecules (IUPAC Technical Report)
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Evita Maria Lindholm
, Jens Magnus Bernth Jensen
Abstract
This document describes how the Nomenclature for Properties and Units (NPU) terminology can be applied to differentiate between cell subpopulations of the hematopoietic lineage. The clusters of differentiation molecules are included in the NPU syntax, together with its correct affiliations to indicate their presence or absence. This allows for identification and isolation of cell populations, subsets, and differentiation stages, which is essential for correct diagnosis and treatment of several malignancies and autoimmune diseases.
1 Preface
This document is Part XXVIII of a series on properties and units in the clinical laboratory sciences initiated in 1987. The series currently comprises:
Syntax and semantic rules [1]
Kind-of-property [2]
Elements (of properties) and their code values [3]
Properties and their code values [4]
Properties and units in thrombosis and hemostasis [5]
Properties and units in IOC-prohibited drugs [6]
Properties and units in clinical microbiology [7]
Properties and units in trace elements [8]
Properties and units in general clinical chemistry [9]
Coding systems: structure and guidelines [10]
Properties and units in clinical pharmacology and toxicology [11]
Properties and units in reproduction and fertility [12]
Properties and units in clinical allergology [13]
Nomenclature, properties, and units in clinical molecular biology [14]
Properties and units for transfusion medicine and immunohematology [15]
The NPU terminology, principles, and implementation – a user’s guide [16]
Properties and units in clinical molecular genetics [17]
Properties and units in the clinical laboratory sciences. Online dynamic NPU manual [18]
2 Introduction
The number of examination results from clinical laboratories in the health area has increased through the past decades. Coding of laboratory analyses is an efficient way of securing standardized and accurate recording of patient information, which can then serve as an invaluable resource for clinical treatment decisions, improved patient care, and medical research. The Nomenclature for Properties and Units (NPU) terminology was developed to support correct and standardized exchange of data across laboratories and eHealth (information and communication technology to improve efficiency, quality, and safety in the health and care sector) systems. To achieve this, each NPU definition (a laboratory code value string for communicating laboratory results based on precise and organized rules, further described under Section 3.1), needs to contain information that ensures similar interpretation of results between laboratories and even across countries. The NPU terminology has also been employed for the characterization of hematopoietic cells. However, due to certain limitations in the terminology’s rules and syntax, it has so far not been able to capture the complexity and phenotypic differences between subpopulations.
By the end of 1960, T-(thymus-dependent) and B-(bursa-independent) lymphocytes were described as two distinct lymphocyte populations, with distinct roles in the immune response. Prior to antigen stimulation, B- and T-lymphocytes appear morphologically similar, and differentiation of the two populations proved difficult. Several studies therefore failed to produce an easy and consistent method to differentiate functionally unique lymphocyte populations [19], [20], [21]. This changed with the development of monoclonal antibodies specific to clusters of differentiation (CD) molecules present on the lymphocyte cell surface, which could differentiate B- and T-lymphocytes much more effectively. In the decades that followed there was a rapid increase in the discovery of new CD molecules, further illustrating the complexities in lymphocyte development and function. Due to the rapid increase in the number of discovered CD molecules, and the absence of studies to differentiate whether the same molecule was recognized by other antibodies, the human leukocyte differentiation antigen (HLDA) workshops were initiated in 1982. The first workshop was sponsored by the International Union of Immunology Societies (IUIS) and the World Health Organization (WHO), and over the years, these HLDA workshops have used antibodies to characterize many of the molecules involved in immunological processes [22]. In addition, they have provided the CD nomenclature system, which is universally used and acknowledged. Currently, more than 350 different CD molecules have been identified [23], which enables identification of different cell types and the stage of differentiation.
In addition to different subtypes of B- and T-lymphocytes, analysis of other cell types such as NK cells, dendritic cells, and monocytes are equally important in current laboratory diagnostics [24], [25], [26]. This illustrates the need to extend the field of application of such codes beyond B- and T-lymphocytes, and in this respect, it is appropriate to use the CD nomenclature to characterize all subpopulations of the hematopoietic lineage [27]. Although identification and quantification of lymphocyte subpopulations by CD-specific antibodies and flow cytometry has been considered the most exact and reliable procedure to assess immunocompetence, leukocyte subsets and their specialized functions have also been characterized through sequencing and, more recently, gene microarrays [28].
Numerous diseases are associated with alterations in peripheral blood lymphocyte subpopulations, including primary or congenital immunodeficiencies, in which certain lymphocyte subpopulations are absent or reduced [29], secondary immunodeficiencies, including HIV infection, which destroys the CD4+ T-cell subpopulation [30], systemic autoimmune diseases [31], infections [32], and cancer [33]. The need to communicate the different cell types and differentiation states is therefore of outmost importance for clinical decisions in diagnosis, prognosis, and patient monitoring. This report describes how the NPU terminology can adapt to the CD nomenclature, so results can be communicated in a precise and standardized way.
3 Objectives
The objective of this project is to define rules and principles to establish NPU definitions for describing subpopulations of the hematopoietic cell lineage by applying the CD nomenclature as the reference terminology.
3.1 The NPU terminology syntax and semantic content
The NPU terminology is an international medical laboratory terminology that presents and communicates millions of laboratory results yearly in various health care systems, supporting clinical decisions in diagnosis, prognosis, and patient monitoring. The NPU terminology is used for the communication of laboratory results between laboratory information systems, hospital patient records, GPs, and local and national data repositories, for health care professionals and citizens in the Scandinavian countries. In addition, the NPU terminology is used locally in some other countries. In addition to the NPU terminology, LOINC (Logical Observation Identifiers Names and Codes) represents another terminology for laboratory results, issued by the Regenstrief Institute (US) and with extensive use across both Europe and the United States. In contrast to NPU, which is based on metrological concepts with strict rules regarding the coding of the measurand and the result value, LOINC provides codes for analyses as offered by the laboratory.
Use of the NPU terminology allows clinical examination results to be recognized, compared, reused in calculations, extracted for research or statistics, and stored for documentation, without loss of meaning. The terminology has been developed since the 1990s with support from the international organizations IFCC (International Federation of Clinical Chemistry and Laboratory Medicine) in collaboration with IUPAC (International Union of Pure and Applied Chemistry).
The rules and principles for establishing NPU definitions require that all terms within the NPU definition are from an international approved terminology or classification. This secures a stable and unambiguous understanding of each concept used.
The NPU concept model identifies the examined properties of a patient, independent of the technology or procedure used to obtain the information. The NPU terminology consists of a code value of five unique numbers, and a unique NPU definition. The NPU definition encompasses essential information about an examination result or a measurement in a formal structure, identifying:
The part of the universe that is studied (the system), for example, plasma
The component examined in that system, for example, sodium ion
The investigated property (referred to as kind-of-property (k-o-p)) of the component in that system, for example, substance concentration
The measurement unit, preferably SI, is added as a quantitative measure. For example, milligram per liter
This is expressed through a prescribed syntax and identified with a NPU definition:
NPUXXXXX system – component; kind-of-property = ?* measurement unit
*The question mark (?) is present in all code definitions as a place holder for the result value.
Examples:
NPU03431 U – sodium ion; subst.c. = ? mmol/L
The result describes the concentration (“subst.c.”; substance concentration) of sodium ion in urine (“U”), where the result value should be returned in millimole per liter.
NPU02321 Ercs(B) – hemoglobin(Fe); subst.c. = ? mmol/L
The result describes the concentration (“subst.c.”; substance concentration) of hemoglobin in erythrocytes in blood (“Ercs(B)”), where the result value should be returned in millimole per liter.
NPU56029 marrow – hematopoietic stem cells; num.c. = ? × 106/L
The result describes the concentration (“num.c.”; number concentration) of hematopoietic stem cells in bone marrow, where the result value should be returned in concentration of 106 cells per liter.
3.2 CD molecules as preferred terms in NPU definitions for describing hematopoietic cells
Most cells can be identified by the proteins they express. The Universal Protein Resource (UniProt) is a knowledge data base for protein sequence and annotation of data, and this data base has become an important source for annotating proteins. This data base is also the primary choice when establishing NPU definitions for other proteins.
As described above, the CD nomenclature was established by the HLDA workshops [23]. This nomenclature has been universally adopted by the immunological community and is officially approved by the IUIS and sanctioned by the WHO [34], for identification and isolation of leukocyte populations, subsets, and differentiation stages. To further emphasize the international credibility of the use of CD molecules and their role in the immune system, the U.S. Food and Drug Administration (FDA) have requested that, for a monoclonal antibody to be used as a diagnostic reagent, it should be evaluated by the HLDA workshops. The list of CD molecules can be found on the Human Cell Differentiation Molecules (HCDM) (http://www.hcdm.org/) homepage. Each molecule is listed with their “CD name,” as well as their “National Center for Biotechnology Information (NCBI) name,” “Gene name,” and “NCBI other name.”
To avoid misclassification based on different understanding of terms for the hematopoietic cell populations and based on the universal acceptance of the CD nomenclature, NPU definitions will be developed based on the expression of CD molecules, whenever these are available. This will provide consistency and uniformity in analyses referring to identical molecules. Furthermore, based on the international consensus on describing CD molecules with the abbreviation “CD,” this abbreviation will also be used when creating NPU definitions. For molecules with different names according to different nomenclatures, the CD nomenclature will be chosen in NPU definitions. For example, CD40 ligand will be referred to as CD154 in NPU definitions, since the former refers to the UniProt nomenclature.
This principle will also apply for NPU definitions where cell populations are clinically known through “common names,” like “helper,” “memory,” etc. This is important, as there is currently no concise and established nomenclature defining lymphocyte populations precisely. Therefore, a “helper, memory T-lymphocyte” can potentially be defined with different sets of CD molecules, as the publications of Valiathan and Apoil illustrate [35, 36].
3.3 CD molecules as separate terms within the NPU definitions
To enable NPU definitions to reflect the complexity in lymphocyte phenotypes through different expression of CD molecules, new NPU definitions will be developed with the appropriate cell type, i.e., B- or T-lymphocytes, as component, and with the different CD molecules as component specifications. This will allow both the component and the specifications to have their individual international approved term references. For example:
NPUXXXXX B – T-lymphocytes(CD4+;CD45RA−;CD197+); num.c. = ? × 109/L
The result describes the concentration (“num.c.”; number concentration) of CD4 positive, CD45RA positive, and CD197 positive T-lymphocytes in blood, where the result value should be returned in concentration of 109 cells per liter.
As described in Section 3.9, CD molecules which are known to always be expressed by the cell listed as component, will be omitted from the NPU definition. Therefore, CD3 is not included in the example above, as T-lymphocytes are listed as the component and CD3 is therefore assumed to be present.
3.4 Annotation of shared phenotypic characteristics between the main populations within the system and the subpopulation in the component
T-lymphocytes are identified through the cell surface molecule CD3 and are mainly composed of two predominant subsets, which are positive in their expression of either CD4 or CD8. The CD4 positive cells are known as T-helper lymphocytes, while the CD8 positive cells are known as cytotoxic T-lymphocytes. Several phenotypes of both the CD4 positive and the CD8 positive T-lymphocytes have been identified, and these subpopulations are frequently calculated as relative proportions of CD4 or CD8 positive T-cells. This means that the CD4 positive or the CD8 positive lymphocytes often represent the NPU “system.” As the investigated subpopulation is implied to have some of the phenotypic characteristics found in the main population, shared characteristics between the main population and the subpopulation will not be repeated in the “component” when developing NPU definitions. This is true whenever the kind-of-property is defined with “fraction.”
Furthermore, each term should be possible to use as both “system” and “component,” to ensure similar meaning of each concept. The system should therefore be described in the same form as the component, with the CD molecules placed in parenthesis as specifications.
Based on these principles, a potential NPU definition describing the fraction of CD154 positive T-lymphocytes among the CD4 positive T-lymphocyte population in blood, after some form of stimulation (“stim.”) will be defined as follows:
NPUXXXXX T-lymcs(CD4+;B) – T-lymphocytes(CD154+); arb.num.fr.(stim.; proc.) = ?
3.5 Annotating CD molecules as present, absent, or with a degree of positivity
Analyzing for the presence or absence of CD molecules on cell surfaces is currently mainly performed by fluorescent labeled antibodies binding to these cell-surface CD molecules. The fraction of cells belonging to each immunophenotype is then measured mainly by using flow cytometry. The signs “+” (plus) and “−” (minus) are added to the CD molecules to indicate the presence or absence, respectively, of that molecule on a cell or cell population. Designating CD molecules together with a “+” and “−” sign is according to the recommended CD nomenclature [34], and NPU definitions for these cell populations will therefore be developed accordingly. This involves that each CD molecule will require at least two term identifications (IDs) when creating NPU definitions, depending on whether it is present or absent.
The CD nomenclature recommends annotating the signs “+” and “−” using superscript, for example CD4+ instead of CD4+. However, to simplify the technical use of the NPU definitions in electronic health records, normal script for these signs will be employed in NPU definitions.
In some instances, CD molecules are expressed in various degrees of positivity, or antigen density, which needs to be communicated in a more detailed way than indicated by the affiliation “+”. Differences in antigen density, or expression level, can for example be due to cell activation level and functional differences, which again can affect disease or prognosis. Differences in antigen density are measured through mean fluorescence intensity (MFI) in flow cytometry. As MFI is set by the user for each experiment, and depends on fluorochrome strength, flow cytometry machine, laboratory settings etc., no exact definition can be set for the parameters that indicate the degree of positivity. In cases where the degree of positivity is important to report, the terms “high,” “intermediate,” and “low” (or alternatively “bright,” “mid,” and “dim”) are usually added to the CD molecule, in the same way as the signs “+” and “−” [34]. Therefore, and whenever appropriate, NPU definitions will be developed with the terms “high,” “intermediate,” and “low” added to the CD molecule.
An example where these affiliations are necessary are within the CD21 low B-lymphocyte subpopulation, which is enriched in a number of conditions with chronic immune stimulation including certain pathogenic infections (viral and parasitic) [37, 38] and autoimmune diseases [39, 40]. The need to characterize CD markers with “high” and “low” is also true for natural killer (NK) cells, which are an important part of the immune system, contributing to the defense against both pathogens and tumors [41]. These cells can be broadly divided into two major subgroups according to the expression density of CD16 and CD56 [42, 43].
For CD21 low B-lymphocytes, the following NPU definition will be developed:
NPUXXXXX B-lymcs(B) – B-lymphocytes (CD21low; CD38low); num.fr.(proc.) = ? %
The results describe the percentage of CD21 low and CD38 low B-lymphocytes among the whole B-lymphocyte population in blood.
3.6 NPU definitions represent the CD molecules in ascending order
Whenever several CD molecules are present as specifications within an NPU definition, we suggest that their sequence is ordered according to ascending order. That is, arranging the CD molecules from the lowest to the highest number within the NPU definition. If necessary, CD molecules should then be followed by additional proteins that are present as component specifications, in numerical and then alphabetical order.
Example:
NPUXXXXX T-lymcs(CD4+;B) – T-lymphocytes(CD38+;CD45RA+;CD197−;HLA-DR+);num.fr.(proc.) = ? %
The results describe the percentage of CD38 positive, CD45RA positive, CD197 negative and HLA-DR positive T-lymphocytes among the CD4 positive T-lymphocyte population in blood.
3.7 Use of percentage (%) as unit in NPU definitions
As described above, flow cytometry has been the most used procedure to quantify lymphocyte subpopulations [44]. Within this method, cell subpopulations are often calculated as a percentage of a parent population when reporting the results of these examinations. Within the NPU terminology, the kind of property “number fraction” is used to describe the number of a component divided by the number of the system. NPU definitions for characterization of lymphocyte subpopulations as a fraction of a larger cell population will therefore be developed with “number fraction” as kind of property. Although percentage is currently not widely accepted as a unit within the NPU terminology, this unit will be allowed for the NPU definitions examining immunophenotypes, to avoid confusion and misinterpretation amongst the clinicians who receive the laboratory results.
Example:
NPUXXXXX T-lymcs(CD4+; B) – T-lymphocytes(CD25+; CD127−); num.fr. = ? %
The results describe the percentage of CD25 positive and CD127 negative T-lymphocytes among the whole CD4 positive T-lymphocyte population in blood.
3.8 Adding clinically relevant search terms to facilitate the use of NPU definitions
The different subtypes of B- and T-lymphocytes are commonly described based on their specific function: helper/effector, cytotoxic, memory, regulatory, etc. [45]. In addition, T-lymphocytes can be characterized by physiological states through their expression of molecules for activation (HLA-DR and CD38), differentiation (CD45RA, CCR7, CD28, and CD27), senescence (CD57), exhaustion (PD1), and apoptosis (CD95, CD178, and CD102b).
Although NPU definitions represent a precise and uniform way of presenting and exchanging laboratory results, NPU definitions can be considered difficult to understand and not user friendly in clinical practice. However, the terms describing function and physiological state are interpretations of the CD molecules expressions. Since there is no consensus regarding which CD molecules need to be expressed to characterize a subpopulation by these phenotypic descriptions, this information will not be included within NPU definitions. Therefore, the Scandinavian countries, which are the countries with most extensive use of this terminology, have developed separate national short names for each NPU definition. These short names make the NPU definitions more useful and easily understandable for clinicians and laboratory personal, and can refer to the subpopulations with common nomenclature (e.g., naïve and memory). This could also be achieved by adding search terms to each NPU definition, which allows different and user-friendly descriptions of the subpopulation, while the NPU definitions are kept constant.
3.9 CD molecules with inferred or equivalent expression are omitted from NPU definitions
In clinical practice, the kits and methods used to detect the different subpopulations vary between laboratories. Due to the potential magnitude of new NPU definitions, certain rules are necessary to limit unnecessary NPU definitions describing the same subpopulations based on the use of different CD molecules. As seen in the examples above for T-lymphocytes, the CD3 molecule is not listed as a defining marker of this cell type. This is due to its inferred expression, as it is well acknowledged that all T-lymphocytes are CD3 positive. This is also true for CD19 in B-lymphocytes, which is known to be present on all B-lymphocytes. CD markers with inferred/unquestioned presence should be omitted from the NPU definitions whenever possible, and CD3 and CD19 are therefore omitted from the NPU definition whenever T-lymphocytes or B-lymphocytes are specified, respectively.
Some CD markers are considered equivalent in terms of detecting their presence or absence. This is true for the CD markers CD45RA and CD45RO, where CD45RA represents the long isoform of CD45 and CD45RO represents the shorter isoform. After antigen priming, T-lymphocytes downregulate the longer isoform CD45RA and reciprocally upregulate the shorter isoform CD45RO. These molecules have therefore been proposed as markers for naïve (CD45RA+/RO−) and memory (CD45RA−/RO+) T-lymphocytes [46]. For simplicity we have chosen to include only CD45RA in the NPU definitions for these subpopulations, but with the implied understanding that antibodies for CD45RO is considered equivalent for use. For example, for the following NPU definition the lab can choose whether they use antibodies detecting CD45RA+ or CD45RO− T-lymphocytes; NPUXXXXX T-lymcs(CD4+;B) – T-lymphocytes(CD45RA+); num.fr. = ? %
The results describe the percentage of CD45RA positive or CD45RO negative T-lymphocytes among the whole CD4 positive T-lymphocyte population in blood.
4 Discussion and conclusion
Laboratory terminologies are important for facilitating data exchange and aid in patient care in common and complex diseases. This document is the XXVIII of a series on properties and units in the clinical laboratory sciences, where the overall aim is to facilitate and harmonize laboratory examination results through common semantic and syntactic rules. The strict rules accompanying the NPU terminology allows unambiguous understanding of the examination results between different laboratories and institutions. However, due to the rapid advancements within technology and clinical research the last decade, continuous recommendations within special fields or areas are required for the terminology to remain relevant and applicable over time. In line with this, the current project defines rules and principles to establish NPU definitions for describing subpopulations of the hematopoietic cell lineage by applying the CD nomenclature as the reference terminology.
4.1 Future developments
The NPU terminology will continue to evolve through published reports and recommendations within special fields or areas where laboratory needs are identified. This way of maintaining the terminology has been found more appropriate than revising and updating original guidelines and reports for the NPU terminology.
4.2 Membership of sponsoring bodies
Membership of the IUPAC Chemistry and Human Health Division Committee during the period 2021–2024 was as follows:
President: Vladimir Gubala (United Kingdom), Vice President: Gerd Schnorrenberg (Germany); Secretary: Linda Johnston (Canada); Members: Titular Members; Vincenzo Abbate (United Kingdom), Djibril Fall (Senegal), Jaana Rysä (Finland), Awis Sukami Mohamad Sabere (Malaysia), Michele Saviano (Italy), Maria Emilia Sousa (Portugal), Associate Members; Neel Balu Balasubramanian (United States), Xiaohong Fang (China), Mette Mathiesen Janiurek (Denmark), Susan Northfield (Australia), Brandon C. Presley (United States), Silvana Raić-Malić (Croatia).
Membership of the IUPAC Subcommittee on Nomenclature for Properties and Units during the preparation of this report (2021–2024) was as follows:
Chair: Helle Møller Johannessen (Denmark); Members: Ivan Bruunshuus (Denmark), Rebecca Ceder (Sweden), Robert Flatman (Australia), Daniel Karlsson (Sweden), Young Bae Lee Hansen (Denmark), Gunnar Nordin (Sweden), Ulla Magdal Petersen (Denmark), Karin Toska (Norway).
Funding source: International Union of Pure and Applied Chemistry
Award Identifier / Grant number: 2021-022-1-700
Acknowledgment
This publication resulted from work carried out under IUPAC Chemistry and Human Health Division Project 2021-022-1-700.
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Research funding: International Union of Pure and Applied Chemistry, Grant Number: 2021-022-1-700.
References
[1] H. Olesen. Eur. J. Clin. Chem. Clin. Biochem. 33, 627 (1995), https://doi.org/10.1016/0009-8981(96)85128-X.Search in Google Scholar
[2] D. Kenny, H. Olesen. Eur. J. Clin. Chem. Clin. Biochem. 35, 317 (1997).Search in Google Scholar
[3] I. Bruunshuus, W. Frederiksen, H. Olesen, I. Ibsen. Pure Appl. Chem. 69, 2577 (1997), https://doi.org/10.1351/pac199769122577.Search in Google Scholar
[4] H. Olesen, D. Kenny, I. Bruunshuus, I. Ibsen, K. Jørgensen, R. Dybkær, X. Fuentes-Arderiu, G. Hill, P. S. de Araujo, C. McDonald. Pure Appl. Chem. 69, 2583 (1997), https://doi.org/10.1351/pac199769122583.Search in Google Scholar
[5] M. Blomback, R. Dybkaer, K. Jorgensen, H. Olesen, S. Thorsen. Eur. J. Clin. Chem. Clin. Biochem. 33, 637 (1995).Search in Google Scholar
[6] H. Olesen, D. Cowan, I. Bruunshuus, K. Klempel, G. Hill. Pure Appl. Chem. 69, 1081 (1997), https://doi.org/10.1351/pac199769051081.Search in Google Scholar
[7] U. Forsum, H. Olesen, W. Frederiksen, B. Persson. Pure Appl. Chem. 72, 555 (2000), https://doi.org/10.1351/pac200072040555.Search in Google Scholar
[8] R. Cornelis, X. Fuentes-Arderiu, I. Bruunshuus. D. Templeton Pure Appl. Chem. 69, 2593 (1997), https://doi.org/10.1351/pac199769122593.Search in Google Scholar
[9] H. Olesen, I. Ibsen, I. Bruunshuus, D. Kenny, R. Dybkaer, X. Fuentes-Arderiu, G. Hill, P. S. De Araujo, C. McDonald. Pure Appl. Chem. 72, 747 (2000), https://doi.org/10.1351/pac200072050747.Search in Google Scholar
[10] H. Olesen, D. Kenny, R. Dybkær, I. Ibsen, I. Bruunshuus, X. Fuentes-Arderiu, G. Hill, P. S. de Araujo, C. McDonald. Pure Appl. Chem. 69, 2607 (1997), https://doi.org/10.1351/pac199769122607.Search in Google Scholar
[11] H. Olesen, D. Cowan, R. De La Torre, I. Bruunshuus, M. Rohde, D. Kenny. Pure Appl. Chem. 72, 479 (2000), https://doi.org/10.1351/pac200072030479.Search in Google Scholar
[12] H. Olesen, A. Giwercman, D. M. de Kretser, D. Mortimer, H. Oshima, P. Troen. Clin. Chem. Lab. Med. 36, 57 (1998), https://doi.org/10.1515/CCLM.1998.011.Search in Google Scholar PubMed
[13] I. Bruunshuus, L. K. Poulsen, H. Olesen. Pure Appl. Chem. 72, 1067 (2000), https://doi.org/10.1351/pac200072061067.Search in Google Scholar
[14] P. S. de Araujo, B. Zingales, P. Alía-Ramos, A. Blanco-Font, X. Fuentes-Arderiu, C. Mannhalter, K. Varming, S. Bojesen, I. Bruunshuus, H. Olesen. Pure Appl. Chem. 76, 1799 (2004), https://doi.org/10.1351/pac200476091799.Search in Google Scholar
[15] K. Varming, U. Forsum, I. Bruunshuus, H. Olesen. J. Int. Fed. Clin. Chem. Lab. Med. 15, 10 (2004).Search in Google Scholar
[16] U. M. Petersen, R. Dybkær, H. Olesen. Pure Appl. Chem. 84, 137 (2012), https://doi.org/10.1351/PAC-REP-11-05-03.Search in Google Scholar
[17] U. M. Petersen, A. Padro-Miquel, G. Taylor, J. M. Hertz, R. Ceder, X. Fuentes-Arderiu, J. T. den Dunnen. Clin. Chim. Acta 484, 122 (2018), https://doi.org/10.1016/j.cca.2018.05.028.Search in Google Scholar PubMed
[18] Y. B. L. Hansen, K. Toska, A. Lund, R. Flatman, R. Ceder. Pure Appl. Chem. 95, 125 (2023), https://doi.org/10.1515/pac-2021-1109.Search in Google Scholar
[19] P. S. Baur, G. B. Thurman, A. L. Goldstein. J. Immunol. 115, 1375 (1975), https://doi.org/10.4049/jimmunol.115.5.1375.Search in Google Scholar
[20] S. Roath, D. Newell, A. Polliack, E. Alexander, P.-S. Lin. Nature 273, 15 (1978), https://doi.org/10.1038/273015a0.Search in Google Scholar PubMed
[21] A. Polliack, S. M. Fu, S. D. Douglas, Z. Bentwich, N. Lampen, E. De Harven. J. Exp. Med. 140, 146 (1974), https://doi.org/10.1084/jem.140.1.146.Search in Google Scholar PubMed PubMed Central
[22] H. Zola, B. Swart. Cell Res. 15, 691 (2005), https://doi.org/10.1038/sj.cr.7290338.Search in Google Scholar PubMed
[23] Human cell differentiation molecules. Available from: http://www.hcdm.org/index.php/molecule-information Search in Google Scholar
[24] A. M. Abel, C. Yang, M. S. Thakar, S. Malarkannan. Front. Immunol. 13, 1869 (2018), https://doi.org/10.3389/fimmu.2018.01869.Search in Google Scholar PubMed PubMed Central
[25] J. Banchereau, R. M. Steinman. Nature 392, 245 (1998), https://doi.org/10.1038/32588.Search in Google Scholar PubMed
[26] F. Geissmann, M. G. Manz, S. Jung, M. H. Sieweke, M. Merad, K. Ley. Science 327, 656 (2010), https://doi.org/10.1126/science.1178331.Search in Google Scholar PubMed PubMed Central
[27] L. Ziegler-Heitbrock, P. Ancuta, S. Crowe, M. Dalod, V. Grau, D. N. Hart, P. J. Leenen, Y.-J. Liu, G. MacPherson, G. J. Randolph, J. Scherberich, J. Schmitz, K. Shortman, S. Sozzani, H. Strobl, M. Zembala, J. M. Austyn, M. B. Lutz. Blood 116, 16 (2010), https://doi.org/10.1182/blood-2010-02-258558.Search in Google Scholar PubMed
[28] T. Chtanova, R. Newton, S. M. Liu, L. Weininger, T. R. Young, D. G. Silva, F. Bertoni, A. Rinaldi, S. Chappaz, F. Sallusto, M. S. Rolph, C. R. Mackay. J. Immunol. 175, 7837 (2005), https://doi.org/10.4049/jimmunol.175.12.7837.Search in Google Scholar PubMed
[29] C. Picard, H. Bobby Gaspar, W. Al-Herz, A. Bousfiha, J.-L. Casanova, T. Chatila, Y. J. Crow, C. Cunningham-Rundles, A. Etzioni, J. L. Franco, S. M. Holland, C. Klein, T. Morio, H. D. Ochs, E. Oksenhendler, J. Puck, M. L. Tang, S. G. Tangye, T. R. Torgerson, K. E. Sullivan. J. Clin. Immunol. 38, 96 (2017), https://doi.org/10.1007/s10875-017-0464-9.Search in Google Scholar PubMed PubMed Central
[30] B. Palmer, N. Blyveis, A. P. Fontenot, C. C. Wilson. J. Immunol. 175, 8415 (2005), https://doi.org/10.4049/jimmunol.175.12.8415.Search in Google Scholar PubMed
[31] G. C. Alegria, P. Gazeau, S. Hillion, C. I. Daïen, D. Y. Cornec. Clin. Rev. Allergy Immunol. 53, 219 (2017), https://doi.org/10.1007/s12016-017-8608-5.Search in Google Scholar PubMed
[32] P. Hohlstein, H. Gussen, M. Bartneck, K. T. Warzecha, C. Roderburg, L. Buendgens, C. Trautwein, A. Koch, F. Tacke. J. Clin. Med. 8, 353 (2019), https://doi.org/10.3390/jcm8030353.Search in Google Scholar PubMed PubMed Central
[33] N. L. Mani, K. A. Schalper, C. Hatzis, O. Saglam, F. Tavassoli, M. Butler, A. B. Chagpar, L. Pusztai, D. L. Rimm. Breast Cancer Res. 18, 78 (2016), https://doi.org/10.1186/s13058-016-0737-x.Search in Google Scholar PubMed PubMed Central
[34] P. Engel, L. Boumsell, R. Balderas, A. Bensussan, V. Gattei, V. Horejsi, B.-Q. Jin, F. Malavasi, F. Mortari, R. Schwartz-Albiez, H. Stockinger, M. C. van Zelm, H. Zola, G. Clark. J. Immunol. 195, 4555 (2015), https://doi.org/10.4049/jimmunol.1502033.Search in Google Scholar PubMed
[35] R. Valiathan, K. Deeb, M. Diamante, M. Ashman, N. Sachdeva, D. Asthana. Immunobiology 219, 487 (2014), https://doi.org/10.1016/j.imbio.2014.02.010.Search in Google Scholar PubMed
[36] P. A. Apoil, B. Puissant-Lubrano, N. Congy-Jolivet, M. Peres, J. Tkaczuk, F. Roubinet, A. Blancher. Data Brief 12, 400 (2017), https://doi.org/10.1016/j.dib.2017.04.019.Search in Google Scholar PubMed PubMed Central
[37] E. D. Charles, C. Brunetti, S. Marukian, K. D. Ritola, A. H. Talal, K. Marks, I. M. Jacobson, C. M. Rice, L. B. Dustin. Blood 117, 5425 (2011), https://doi.org/10.1182/blood-2010-10-312942.Search in Google Scholar PubMed PubMed Central
[38] B. Terrier, F. Joly, T. Vazquez, P. Benech, M. Rosenzwajg, W. Carpentier, M. Garrido, P. Ghillani-Dalbin, D. Klatzmann, P. Cacoub, D. Saadoun. J. Immunol. 187, 6550 (2011), https://doi.org/10.4049/jimmunol.1102022.Search in Google Scholar PubMed
[39] C. Wehr, H. Eibel, M. Masilamani, H. Illges, M. Schlesier, H.-H. Peter, K. Warnatz. Clin. Immunol. 113, 161 (2004), https://doi.org/10.1016/j.clim.2004.05.010.Search in Google Scholar PubMed
[40] D. Saadoun, B. Terrier, J. Bannock, T. Vazquez, C. Massad, I. Kang, F. Joly, M. Rosenzwajg, D. Sene, P. Benech, L. Musset, D. Klatzmann, E. Meffre, P. Cacoub. Arthritis Rheum. 65, 1085 (2013), https://doi.org/10.1002/art.37828.Search in Google Scholar PubMed PubMed Central
[41] M. A. Cooper, T. A. Fehniger, M. A. Caligiuri. Trends Immunol. 22, 633 (2001), https://doi.org/10.1016/s1471-4906(01)02060-9.Search in Google Scholar PubMed
[42] K. Katchar, K. Söderström, J. Söderström, A. Eklund, J. Grunewald. Eur. Respir. J. 26, 77 (2005), https://doi.org/10.1183/09031936.05.00030805.Search in Google Scholar PubMed
[43] V. Béziat, D. Duffy, S. N. Quoc, M. Le Garff-Tavernier, J. Decocq, B. Combadière, P. Debré, V. Vieillard. J. Immunol. 186, 6753 (2011), https://doi.org/10.4049/jimmunol.1100330.Search in Google Scholar PubMed
[44] C. Ma, S. G. Tangye. Front. Immunol. 10, 2108 (2019), https://doi.org/10.3389/fimmu.2019.02108.Search in Google Scholar PubMed PubMed Central
[45] H. T. Maecker, J. P. McCoy, R. Nussenblatt. Nat. Rev. Immunol. 12, 191 (2012), https://doi.org/10.1038/nri3158.Search in Google Scholar PubMed PubMed Central
[46] A. N. Akbar, L. Terry, A. Timms, P. C. Beverley, G. Janossy. J. Immunol. 140, 2171 (1988), https://doi.org/10.4049/jimmunol.140.7.2171.Search in Google Scholar
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Articles in the same Issue
- Frontmatter
- In this issue
- IUPAC Technical Reports
- Terms of Latin origin relating to sample characterization (IUPAC Technical Report)
- Glossary of terms used in biochar research (IUPAC Technical Report)
- Properties and units in the clinical laboratory sciences. Part XXVIII. NPU codes for characterizing subpopulations of the hematopoietic lineage, described from their clusters of differentiation molecules (IUPAC Technical Report)
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- Capabilities and drawbacks of mass spectrometry in the forensic field: analysis of real cases dealing with toxicology and explosives
- Mapping the distribution of bioactive compounds and aroma/flavour precursors in green coffee beans with an integrated mass spectrometry-based approach
- Fire fighters and mass spectrometry: from the world of combustion to the molecular ion
- Special Topic: IUPAC Distinguished Women in Chemistry and Chemical Engineering Awards 2023; Guest Editor: Mary J. Garson
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- Regular Review Article
- A brief history of risk assessment for agrochemicals
- Regular Research Articles
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- Facile and green hydrothermal synthesis of MgAl/NiAl/ZnAl layered double hydroxide nanosheets: a physiochemical comparison
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