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Modern Imaging Technologies of Mast Cells for Biology and Medicine (Review)

Modern Imaging Technologies of Mast Cells for Biology and Medicine (Review)

Grigorev I.P., Korzhevskii D.E.
Key words: mast cells; histochemistry; immunohistochemistry; toluidine blue; safranin; alcian blue; tryptase; chymase.
2021, volume 13, issue 4, page 93.
DOI: https://doi.org/10.17691/stm2021.13.4.10

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Mast cells play an important role in the body defense against allergens, pathogens, and parasites by participating in inflammation development. However, there is evidence for their contributing to the pathogenesis of a number of atopic, autoimmune, as well as cardiovascular, oncologic, neurologic, and other diseases (allergy, asthma, eczema, rhinitis, anaphylaxis, mastocytosis, multiple sclerosis, rheumatoid arthritis, inflammatory gastrointestinal and pulmonary diseases, migraine, etc.). The diagnosis of many diseases and the study of mast cell functions in health and disease require their identification; so, the knowledge on adequate imaging techniques for mast cells in humans and different species of animals is of particular importance.

The present review summarizes the data on major methods of mast cell imaging: enzyme histochemistry, immunohistochemistry, as well as histochemistry using histological stains. The main histological stains bind to heparin and other acidic mucopolysaccharides contained in mast cells and stain them metachromatically. Among these are toluidine blue, methylene blue (including that contained in May-Grünwald–Giemsa stain), thionin, pinacyanol, and others. Safranin and fluorescent dyes: berberine and avidin — also bind to heparin. Longer staining with histological dyes or alcian blue staining is needed to label mucosal and immature mast cells.

Advanced techniques — enzyme histochemistry and especially immunohistochemistry — enable to detect mast cells high-selectively using a reaction to tryptases and chymases (specific proteases of these cells). In the immunohistochemical study of tryptases and chymases, species-specific differences in the distribution of the proteases in mast cells of humans and animals should be taken into account for their adequate detection. The immunohistochemical reaction to immunoglobulin E receptor (FcεRI) and c-kit receptor is not specific to mast cells, although the latter is important to demonstrate their proliferation in normal and malignant growth.

Correct fixation of biological material is also discussed in the review as it is of great significance for histochemical and immunohistochemical mast cell detection.

Fluorescent methods of immunohistochemistry and a multimarker analysis in combination with confocal microscopy are reported to be new technological approaches currently used to study various mast cell populations.

  1. Elieh Ali Komi D., Wohrl S., Bielory L. Mast cell biology at molecular level: a comprehensive review. Clin Rev Allergy Immunol 2020; 58(3): 342–365, https://doi.org/10.1007/s12016-019-08769-2.
  2. Metz M., Maurer M. Mast cells — key effector cells in immune responses. Trends Immunol 2007; 28: 234–241, https://doi.org/10.1016/j.it.2007.03.003.
  3. Piliponsky A.M., Acharya M., Shubin N.J. Mast cells in viral, bacterial, and fungal infection immunity. Int J Mol Sci 2019; 20(12): 2851, https://doi.org/10.3390/ijms20122851.
  4. Krystel-Whittemore M., Dileepan K.N., Wood J.G. Mast cell: a multi-functional master cell. Front Immunol 2016; 6: 620, https://doi.org/10.3389/fimmu.2015.00620.
  5. Olivera A., Beaven M.A., Metcalfe D.D. Mast cells signal their importance in health and disease. J Allergy Clin Immunol 2018; 142(2): 381–393, https://doi.org/10.1016/j.jaci.2018.01.034.
  6. Metcalfe D.D. Mast cells and mastocytosis. Blood 2008; 112(4): 946–956, https://doi.org/10.1182/blood-2007-11-078097.
  7. Rivellese F., Nerviani A., Rossi F.W., Marone G., Matucci-Cerinic M., de Paulis A., Pitzalis C. Mast cells in rheumatoid arthritis: friends or foes? Autoimmun Rev 2017; 16(6): 557–563, https://doi.org/10.1016/j.autrev.2017.04.001.
  8. da Silva E.Z., Jamur M.C., Oliver C. Mast cell function: a new vision of an old cell. J Histochem Cytochem 2014; 62(10): 698–738, https://doi.org/10.1369/0022155414545334.
  9. Varricchi G., de Paulis A., Marone G., Galli S.J. Future needs in mast cell biology. Int J Mol Sci 2019; 20(18): 4397, https://doi.org/10.3390/ijms20184397.
  10. Kutukova N.A., Nazarov P.G. Mast cells: a role in inflammation, tissue repair and fibrosis. Citokiny i vospalenie 2014; 13(2): 11–20.
  11. Binda M.M., Donnez J., Dolmans M.M. Targeting mast cells: a new way to treat endometriosis. Expert Opin Ther Targets 2017; 21(1): 67–75, https://doi.org/10.1080/14728222.2017.1260548.
  12. Aller M.A., Arias A., Arias J.I., Arias J. Carcinogenesis: the cancer cell-mast cell connection. Inflamm Res 2019; 68(2): 103–116, https://doi.org/10.1007/s00011-018-1201-4.
  13. Jones M.K., Nair A.A., Gupta M. Mast cells in neurodegenerative disease. Front Cell Neurosci 2019; 13: 171, https://doi.org/10.3389/fncel.2019.00171.
  14. Girolamo F., Coppola C., Ribatti D. Immunoregulatory effect of mast cells influenced by microbes in neurodegenerative diseases. Brain Behav Immun 2017; 65: 68–89, https://doi.org/10.1016/j.bbi.2017.06.017.
  15. Kempuraj D., Thangavel R., Selvakumar G.P., Zaheer S., Ahmed M.E., Raikwar S.P., Zahoor H., Saeed D., Natteru P.A., Iyer S., Zaheer A. Brain and peripheral atypical inflammatory mediators potentiate neuroinflammation and neurodegeneration. Front Cell Neurosci 2017; 11: 216, https://doi.org/10.3389/fncel.2017.00216.
  16. Bykov V.L. Secretory mechanisms and secretory products of mast cells. Morfologiia 1999; 115(2): 64–72.
  17. Mukai K., Tsai M., Saito H., Galli S.J. Mast cells as sources of cytokines, chemokines, and growth factors. Immunol Rev 2018; 282(1): 121–150, https://doi.org/10.1111/imr.12634.
  18. Wernersson S., Pejler G. Mast cell secretory granules: armed for battle. Nat Rev Immunol 2014; 14(7): 478–494, https://doi.org/10.1038/nri3690.
  19. Frossi B., Mion F., Sibilano R., Danelli L., Pucillo C.E.M. Is it time for a new classification of mast cells? What do we know about mast cell heterogeneity? Immun Rev 2018; 282(1): 35–46, https://doi.org/10.1111/imr.12636.
  20. Enerbäck L. Mast cells in rat gastrointestinal mucosa. I. Effects of fixation. Acta Pathol Microbiol Scand 1966; 66(3): 289–302, https://doi.org/10.1111/apm.1966.66.3.289.
  21. Enerbäck L. Mast cells in rat gastrointestinal mucosa. 2. Dye-binding and metachromatic properties. Acta Pathol Microbiol Scand 1966; 66(3): 303–312, https://doi.org/10.1111/apm.1966.66.3.303.
  22. Féger F., Varadaradjalou S., Gao Z., Abraham S.N., Arock M. The role of mast cells in host defense and their subversion by bacterial pathogens. Trends Immunol 2002; 23(3): 151–158, https://doi.org/10.1016/s1471-4906(01)02156-1.
  23. Church M.K., Levi-Schaffer F. The human mast cell. J Allergy Clin Immunol 1997; 99(2): 155–160, https://doi.org/10.1016/s0091-6749(97)70089-7.
  24. Dvorak A.M. Ultrastructural studies of human basophils and mast cells. J Histochem Cytochem 2005; 53(9): 1043–1070, https://doi.org/10.1369/jhc.5R6647.2005.
  25. Humphries D.E., Wong G.W., Friend D.S., Gurish M.F., Qiu W.T., Huang C., Sharpe A.H., Stevens R.L. Heparin is essential for the storage of specific granule proteases in mast cells. Nature 1999; 400(6746): 769–772, https://doi.org/10.1038/23481.
  26. Gusel’nikova V.V., Bekoyeva S.A., Korzhevskaya V.F., Fyodorova Y.A., Korzhevskiy D.E. Histochemical and immunohistochemical identification of human myocardial mast cells. Morfologiia 2015; 147(1): 80–86.
  27. Fyodorova Ye.A., Grigoriyev I.P., Syrtzova M.A., Sufiyeva D.A., Novikova A.D., Korzhevskiy D.E. Detection of morphological signs of mast cell degranulation in the human choroid plexus using different staining methods and immunohistochemistry. Morfologiia 2018; 153(2): 70–75.
  28. Fedorova E.A., Sufieva D.A., Grigorev I.P., Korzhevskii D.E. Mast cells of the human pineal gland. Adv Gerontol 2019; 9(1): 62–66, https://doi.org/10.1134/s2079057019010053.
  29. Atiakshin D., Samoilova V., Buchwalow I., Boecker W., Tiemann M. Characterization of mast cell populations using different methods for their identification. Histochem Cell Biol 2017; 147(6): 683–694, https://doi.org/10.1007/s00418-017-1547-7.
  30. Beil W.J., Schulz M., McEuen A.R., Buckley M.G., Walls A.F. Number, fixation properties, dye-binding and protease expression of duodenal mast cells: comparisons between healthy subjects and patients with gastritis or Crohn’s disease. Histochem J 1997; 29(10): 759–773, https://doi.org/10.1023/a:1026421303260.
  31. Buckley M., Walls A.F. Identification of mast cells and mast cell subpopulations. Methods Mol Med 2008; 138: 285–297, https://doi.org/10.1007/978-1-59745-366-0_24.
  32. Wingren U., Enerbäck L. Mucosal mast cells of the rat intestine: a re-evaluation of fixation and staining properties, with special reference to protein blocking and solubility of the granular glycosaminoglycan. Histochem J 1983; 15(6): 571–582, https://doi.org/10.1007/bf01954148.
  33. Welle M. Development, significance, and heterogeneity of mast cells with particular regard to the mast cell-specific proteases chymase and tryptase. J Leukoc Biol 1997; 61(3): 233–245, https://doi.org/10.1002/jlb.61.3.233.
  34. Luna L.G. Histopathologic methods and color atlas of special stains and tissue artifacts. Gaithersburg, MD: American Histolabs Inc., Publishing Division; 1992; p. 311–312.
  35. Hamouzova P., Cizek P., Bartoskova A., Novotny R. Different fixative solutions in the detection of mast cells in the canine and feline reproductive organs. Folia Morphol (Warsz) 2020; 79(2): 265–271, https://doi.org/10.5603/fm.a2019.0097.
  36. Kolset S.O., Prydz K., Pejler G. Intracellular proteoglycans. Biochem J 2004; 379(2): 217–227, https://doi.org/10.1042/bj20031230.
  37. Duelli A., Rönnberg E., Waern I., Ringvall M., Kolset S.O., Pejler G. Mast cell differentiation and activation is closely linked to expression of genes coding for the serglycin proteoglycan core protein and a distinct set of chondroitin sulfate and heparin sulfotransferases. J Immunol 2009; 183(11): 7073–7083, https://doi.org/10.4049/jimmunol.0900309.
  38. Frangogiannis N.G., Burns A.R., Michael L.H., Entman M.L. Histochemical and morphological characteristics of canine cardiac mast cells. Histochem J 1999; 31(4): 221–229, https://doi.org/10.1023/a:1003541332070.
  39. Matsson L. Presence of mast cells in various oral mucosal sites in juvenile and adult rats. Scand J Dent Res 1993; 101(5): 292–298, https://doi.org/10.1111/j.1600-0722.1993.tb01123.x.
  40. Broome M., Villarreal B. Differential staining of mast cells with toluidine blue. J Histotechnol 2012; 35(1): 27–30, https://doi.org/10.1179/2046023611y.0000000006.
  41. Xu L.R., Carr M.M., Bland A.P., Hall G.A. Histochemistry and morphology of porcine mast cells. Histochem J 1993; 25(7): 516–522, https://doi.org/10.1007/bf00159288.
  42. Valchanov K.P., Proctor G.B., Hartley R.H., Paterson K.L., Shori D.K. Enzyme histochemistry of rat mast cell tryptase. Histochem J 1998; 30(2): 97–103, https://doi.org/10.1023/a:1003231000051.
  43. Ghanem N.S., Assem E.S.K., Leung K.B.P., Pearce F.L. Guinea pig mast cells: comparative study on morphology, fixation and staining properties. Int Arch Allergy Appl Immunol 1988; 85(3): 351–357, https://doi.org/10.1159/000234531.
  44. Markey A.C., Churchill L.J., MacDonald D.M. Human cutaneous mast cells — a study of fixative and staining reactions in normal skin. Br J Dermatol 1989; 120(5): 625–631, https://doi.org/10.1111/j.1365-2133.1989.tb01347.x.
  45. Bandara G., Metcalfe D.D., Kirshenbaum A.S. Growth of human mast cells from bone marrow and peripheral blood-derived CD34+ pluripotent hematopoietic cells. Methods Mol Biol 2015; 1220: 155–162, https://doi.org/10.1007/978-1-4939-1568-2_10.
  46. Grigorev I.P., Korzhevskii D.E. Current technologies for fixation of biological material for immunohistochemical analysis (review). Sovremennye tehnologii v medicine 2018; 10(2): 156–165, https://doi.org/10.17691/stm2018.10.2.19.
  47. Gusel’nikova V.V., Sukhorukova E.G., Fedorova E.A., Polevshchikov A.V., Korzhevskiĭ D.E. A method for the simultaneous detection of mast cells and nerve terminals in the thymus in laboratory mammals. Neurosci Behav Physiol 2015; 45(4): 371–374, https://doi.org/10.1007/s11055-015-0084-x.
  48. Korzhevskii D.E., Grigorev I.P., Otellin V.A. Application of zinc-containing dehydrating fixatives for neurohistological studies. Morfologiia 2006; 129(1): 85–86.
  49. Korzhevskii D.E., Sukhorukova E.G., Gilerovich E.G., Petrova E.S., Kirik O.V., Grigor’ev I.P. Advantages and disadvantages of zinc-ethanol-formaldehyde as a fixative for immunocytochemical studies and confocal laser microscopy. Neurosci Behav Physiol 2014; 44(5): 542–545, https://doi.org/10.1007/s11055-014-9948-8.
  50. Petrova E.S., Kolos E.A., Chumasov E.I. Comparative study of the mast cells in the pancreas of young and aged rats. Mezdunarodnyj vestnik veterinarii 2018, 1: 54–59.
  51. Sergeeva E.S., Gusel’nikova V.V., Ermolaeva L.A., Belikov A.V., Fedotov D.Yu., Sufieva D.A., Semyashkina Yu.V., Antropova M.M., Korzhevskii D.E. The role of myofibroblasts and mast cells in oral mucosa repair after fractional laser treatment. Zurnal anatomii i gistopatologii 2019; 8(1): 59–67, https://doi.org/10.18499/2225-7357-2019-8-1-59-67.
  52. Rieger J., Twardziok S., Huenigen H., Hirschberg R.M., Plendl J. Porcine intestinal mast cells. Evaluation of different fixatives for histochemical staining techniques considering tissue shrinkage. Eur J Histochem 2013; 57(3): e21, https://doi.org/10.4081/ejh.2013.e21.
  53. Leclere M., Desnoyers M., Beauchamp G., Lavoie J.P. Comparison of four staining methods for detection of mast cells in equine bronchoalveolar lavage fluid. J Vet Intern Med 2006; 20(2): 377–381, https://doi.org/10.1892/0891-6640(2006)20[377:cofsmf]2.0.co;2.
  54. Enerbäck L. Berberine sulphate binding to mast cell polyanions: a cytofluorometric method for the quantitation of heparin. Histochemistry 1974; 42(4): 301–313, https://doi.org/10.1007/bf00492678.
  55. Chen X.J., Enerbäck L. Immature peritoneal mast cells in neonatal rats express the CTMC phenotype, as well as functional IgE receptors. APMIS 1999; 107(10): 957–965, https://doi.org/10.1111/j.1699-0463.1999.tb01497.x.
  56. Feyerabend T.B., Hausser H., Tietz A., Blum C., Hellman L., Straus A.H., Takahashi H.K., Morgan E.S., Dvorak A.M., Fehling H.J., Rodewald H.R. Loss of histochemical identity in mast cells lacking carboxypeptidase A. Mol Cell Biol 2005; 25(14): 6199–6210, https://doi.org/10.1128/mcb.25.14.6199-6210.2005.
  57. Galli S.J. New insights into “the riddle of the mast cells”: microenvironmental regulation of mast cell development and phenotypic heterogeneity. Lab Invest 1990; 62(1): 5–33.
  58. Janicki J.S., Brower G.L., Levick S.P. The emerging prominence of the cardiac mast cell as a potent mediator of adverse myocardial remodeling. Methods Mol Biol 2015; 1220: 121–139, https://doi.org/10.1007/978-1-4939-1568-2_8.
  59. Becker A.B., Chung K.F., McDonald D.M., Lazarus S.C., Frick O.L., Gold W.M. Mast cell heterogeneity in dog skin. Anat Rec 1985; 213(4): 477–531, https://doi.org/10.1002/ar.1092130402.
  60. Voronchikhin P.A., Syrtcova M.A., Talantov S.V., Erokhina I.L., Korzhevskiy D.E., Sukhorukova E.G., Okovitiy S.V., Kulikov A.V. Effect of metoprolol and bisoprolol on the course of experimental bronchial asthma. Biomedicina 2013; 1(2): 42–51.
  61. Yang B., Yu S., Cui Y., He J., Jin X., Wang R. Morphological analysis of the lung of neonatal yak. Anat Histol Embryol 2010; 39(2): 138–151, https://doi.org/10.1111/j.1439-0264.2009.00988.x.
  62. Korzhevskiy D.E., Sukhorukova E.G. Gistokhimicheskie metody okrashivaniya gistologicheskikh preparatov. V kn.: Korzhevskiy D.E., Gilerovich E.G., Kirik O.V., Sukhorukova E.G., Grigor’ev I.P. Morfologicheskaya diagnostika. Podgotovka materiala dlya gistologicheskogo issledovaniya i elektronnoy mikroskopii [Histochemical methods of staining histological preparations. In: Korzhevskiy D.E., Gilerovich E.G., Kirik O.V., Sukhorukova E.G., Grigor’ev I.P. Morphological diagnostics. Preparation of material for histological examination and electron microscopy]. Saint Petersburg: SpetsLit; 2013; p. 85–96.
  63. Blaies D.M., Williams J.F. A simplified method for staining mast cells with astra blue. Stain Technol 1981; 56(2): 91–94, https://doi.org/10.3109/10520298109067288.
  64. Sharma R., Saxena S. Comparative study of the presence of mast cells in periapical granulomas and periapical cysts by toluidine blue and astra blue: possible role of mast cells in the course of human periapical lesions. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004; 97(1): 59–63, https://doi.org/10.1016/s1079-2104(03)00378-0.
  65. Atyakshin D.A., Burtseva A.S., Sokolov D.A. Evaluation of the effectiveness of mast cells detection in mongolian gerbils jejunum mucosa using histochemical methods. Zurnal anatomii i gistopatologii 2016; 5(4): 85–89, https://doi.org/10.18499/2225-7357-2016-5-4-85-89.
  66. Atyakshin D.A., Gerasimova O.A., Meshkova V.Yu., Samodurova N.Yu., Samoilenko T.V., Shishkina V.V. Novel histochemical approach for evaluation of tryptase expression in the mast cell population. Zurnal anatomii i gistopatologii 2020; 9(3): 94–101, https://doi.org/10.18499/2225-7357-2020-9-3-94-101.
  67. Mutsaddi S., Kotrashetti V.S., Nayak R.S., Pattanshetty S.M. Comparison of histochemical staining techniques for detecting mast cells in oral lesions. Biotech Histochem 2019; 94(6): 459–468, https://doi.org/10.1080/10520295.2019.1597986.
  68. Al-Zghoul M.B., Al-Rukibat R.K., Alghadi M., Caceci T., Bani Ismail Z. Distribution and density of mast cells in camel small intestine and influence of fixation techniques. Eur J Histochem 2008; 52(4): 237–241, https://doi.org/10.4081/1222.
  69. Matin R., Tam E.K., Nadel J.A., Caughey G.H. Distribution of chymase-containing mast cells in human bronchi. J Histochem Cytochem 1992; 40(6): 781–786, https://doi.org/10.1177/40.6.1588024.
  70. Kube P., Audigé L., Küther K., Welle M. Distribution, density and heterogeneity of canine mast cells and influence of fixation techniques. Histochem Cell Biol 1998; 110(2): 129–135, https://doi.org/10.1007/s004180050274.
  71. Simoes J.P.C., Schoning P., Butine M. Prognosis of canine mast cell tumors: a comparison of three methods. Vet Pathol 1994; 31(6): 637–647, https://doi.org/10.1177/030098589403100602.
  72. Menétrey D., Dubayle D. A one-step dual-labeling method for antigen detection in mast cells. Histochem Cell Biol 2003; 120(5): 435–442, https://doi.org/10.1007/s00418-003-0581-9.
  73. Takahashi N., Tarumi W., Hamada N., Ishizuka B., Itoh M.T. Cresyl violet stains mast cells selectively: its application to counterstaining in immunohistochemistry. Zoolog Sci 2017; 34(2): 147–150, https://doi.org/10.2108/zs160162.
  74. Joseph S., Das S., Chand R., Roopa R., Thomas I.M. Comparison of toluidine blue vs thionin for mast cells in rat mesentery using Carnoy’s fixative. J Anat Soc India 2003; 52(2): 166–167.
  75. Zhou Y., Pan P., Yao L., Su M., He P., Niu N., McNutt M.A., Gu J. CD117-positive cells of the heart: progenitor cells or mast cells? J Histochem Cytochem 2010; 58(4): 309–316, https://doi.org/10.1369/jhc.2009.955146.
  76. Atyakshin D.A. Histochemical approaches to the evaluation of the participation of mast cells in the regulation of the fibrous component of the intercellular matrix of skin connective tissue. Zurnal anatomii i gistopatologii 2018; 7(3): 100–112, https://doi.org/10.18499/2225-7357-2018-7-3-100-112.
  77. Hals E. Some methods for fluorochromation and staining of rat mast cells with basic dyes. Eur J Oral Sci 1970; 78(1–4): 301–310, https://doi.org/10.1111/j.1600-0722.1970.tb02077.x.
  78. Abdalkhani A., Sellers R., Gent J., Wulitich H., Childress S., Stein B., Boissy R.E., Wysolmerski J.J., Foley J. Nipple connective tissue and its development: insights from the K14-PTHrP mouse. Mech Dev 2002; 115(1–2): 63–77, https://doi.org/10.1016/s0925-4773(02)00092-8.
  79. Shubich M.G. A new selective method of staining mast cells. Byulleten eksperimentalnoi biologii i meditsiny 1958; 46(12): 110.
  80. Atanasova D., Dandov A., Kirov T., Lazarov N. Mast cells in the rat carotid body. Acta Morphol Anthropol 2018; 25(1–2): 11–15.
  81. Spatz M. Bismarck brown as a selective stain for mast cells. Am J Clin Pathol 1960; 34(3): 285–287, https://doi.org/10.1093/ajcp/34.3_ts.285.
  82. Florenzano F., Bentivoglio M. Degranulation, density, and distribution of mast cells in the rat thalamus: a light and electron microscopic study in basal conditions and after intracerebroventricular administration of nerve growth factor. J Comp Neurol 2000; 424(4): 651–669, https://doi.org/10.1002/1096-9861(20000904)424:4651::aid-cne73.0.co;2-g.
  83. Krüger P.G., Bø L., Myhr K.M., Karlsen Å.E., Taule A., Nyland H.I., Mørk S. Mast cells and multiple sclerosis: a light and electron microscopic study of mast cells in multiple sclerosis emphasizing staining procedures. Acta Neurol Scand 1990; 81(1): 31–36, https://doi.org/10.1111/j.1600-0404.1990.tb00927.x.
  84. Tomasi V.H., Orrea S.C., Raimondi A.R., Itoiz M.E. A new technique for staining mast cells using ferroin. Biotech Histochem 2003; 78(5): 255–259, https://doi.org/10.1080/10520290310501630458.
  85. Shukla S.A., Veerappan R., Whittimore J.S., Ellen Miller L., Youngberg G.A. Mast cell ultrastructure and staining in tissue. Methods Mol Biol 2006; 315: 63–76, https://doi.org/10.1385/1-59259-967-2:063.
  86. Reber L.L., Sibilano R., Starkl P., Roers A., Grimbaldeston M.A., Tsai M., Gaudenzio N., Galli S.J. Imaging protective mast cells in living mice during severe contact hypersensitivity. JCI Insight 2017; 2(9): e92900, https://doi.org/10.1172/jci.insight.92900.
  87. Rozniecki J.J., Dimitriadou V., Lambracht-Hall M., Pang X., Theoharides T.C. Morphological and functional demonstration of rat dura mater mast cell–neuron interactions in vitro and in vivo. Brain Res 1999; 849(1–2): 1–15, https://doi.org/10.1016/s0006-8993(99)01855-7.
  88. Stefanov I.S., Vodenicharov A.P., Tsandev N.S., Sevrieva D. Histochemical study of heparin-positive mast cells in the terminal part of porcine ductus choledochus and papilla duodeni major. Anat Histol Embryol 2015; 45(5): 386–391, https://doi.org/10.1111/ahe.12207.
  89. Vodenicharov A., Tsandev N., Kostadinov G., Stefanov I. Comparative study of heparin- and toluidine blue positive mast cells in porcine lumbar spinal ganglia. Bulg J Vet Med 2018; 21(4): 391–396, https://doi.org/10.15547/bjvm.1090.
  90. Harem M.K., Liman N. Histochemical method for demonstrating quail mast cell types simultaneously. Biotech Histochem 2009; 84(6): 275–282, https://doi.org/10.3109/10520290902991394.
  91. Kett W.C., Osmond R.I., Moe L., Skett S.E., Kinnear B.F., Coombe D.R. Avidin is a heparin-binding protein. Affinity, specificity and structural analysis. Biochim Biophys Acta 2003; 1620(1–3): 225–234, https://doi.org/10.1016/s0304-4165(02)00539-1.
  92. Zhang Y., Ramos B.F., Jakschik B.A. Augmentation of reverse arthus reaction by mast cells in mice. J Clin Invest 1991; 88(3): 841–846, https://doi.org/10.1172/jci115385.
  93. Folkerts J., Gaudenzio N., Maurer M., Hendriks R.W., Stadhouders R., Tam S.Y., Galli S.J. Rapid identification of human mast cell degranulation regulators using functional genomics coupled to high-resolution confocal microscopy. Nat Protoc 2020; 15(3): 1285–1310, https://doi.org/10.1038/s41596-019-0288-6.
  94. Joulia R., L’Faqihi F.E., Valitutti S., Espinosa E. IL-33 fine tunes mast cell degranulation and chemokine production at the single-cell level. J Allergy Clin Immunol 2017; 140(2): 497-509.E10, https://doi.org/10.1016/j.jaci.2016.09.049.
  95. Weidner N., Austen K.F. Heterogeneity of mast cells at multiple body sites. Fluorescent determination of avidin binding and immunofluorescent determination of chymase, tryptase, and carboxypeptidase content. Pathol Res Pract 1993; 189(2): 156–162, https://doi.org/10.1016/s0344-0338(11)80086-5.
  96. Jones C.J.P., Mosley S.M., Jeffrey I.J.M., Stoddart R.W. Elimination of the non-specific binding of avidin to tissue sections. Histochem J 1987; 19(5): 264–268, https://doi.org/10.1007/bf01675685.
  97. Spirkoski J., Melo F.R., Grujic M., Calounova G., Lundequist A., Wernersson S., Pejler G. Mast cell apoptosis induced by siramesine, a sigma-2 receptor agonist. Biochem Pharmacol 2012; 84(12): 1671–1680, https://doi.org/10.1016/j.bcp.2012.09.028.
  98. Ivanova S., Repnik U., Bojic L., Petelin A., Turk V., Turk B. Lysosomes in apoptosis. Methods Enzymol 2008; 442: 183–199, https://doi.org/10.1016/s0076-6879(08)01409-2.
  99. Williams R.M., Webb W.W. Single granule pH cycling in antigen-induced mast cell secretion. J Cell Sci 2000; 113 Pt 21: 3839–3850.
  100. Pejler G., Rönnberg E., Waern I., Wernersson S. Mast cell proteases: multifaceted regulators of inflammatory disease. Blood 2010; 115(24): 4981–4990, https://doi.org/10.1182/blood-2010-01-257287.
  101. Irani A.M., Schwartz L.B. Mast cell heterogeneity. Clin Exp Allergy 1989; 19(2): 143–155, https://doi.org/10.1111/j.1365-2222.1989.tb02357.x.
  102. Miller H.R.P., Pemberton A.D. Tissue-specific expression of mast cell granule serine proteinases and their role in inflammation in the lung and gut. Immunology 2002; 105(4): 375–390, https://doi.org/10.1046/j.1365-2567.2002.01375.x.
  103. Lützelschwab C., Pejler G., Aveskogh M., Hellman L. Secretory granule proteases in rat mast cells. Cloning of 10 different serine proteases and a carboxypeptidase A from various rat mast cell populations. J Exp Med 1997; 185(1): 13–29, https://doi.org/10.1084/jem.185.1.13.
  104. Thorpe M., Fu Z., Albat E., Akula S., de Garavilla L., Kervinen J., Hellman L. Extended cleavage specificities of mast cell proteases 1 and 2 from golden hamster: сlassical chymase and an elastolytic protease comparable to rat and mouse MCP-5. PLoS One 2018; 13(12): e0207826, https://doi.org/10.1371/journal.pone.0207826.
  105. Zhongwei Y., Akula S., Fu Z., de Garavilla L., Kervinen J., Thorpe M., Hellman L. Extended cleavage specificities of rabbit and guinea pig mast cell chymases: two highly specific Leu-ases. Int J Mol Sci 2019; 20(24): 6340, https://doi.org/10.3390/ijms20246340.
  106. Huntley J.F., Newlands G.F., Gibson S., Ferguson A., Miller H.R. Histochemical demonstration of chymotrypsin like serine esterases in mucosal mast cells in four species including man. J Clin Pathol 1985; 38(4): 375–384, https://doi.org/10.1136/jcp.38.4.375.
  107. Farrugia B.L., Whitelock J.M., O’Grady R., Caterson B., Lord M.S. Mast cells produce a unique chondroitin sulfate epitope. J Histochem Cytochem 2016; 64(2): 85–98, https://doi.org/10.1369/0022155415620649.
  108. Wolters P.J., Pham C.T., Muilenburg D.J., Ley T.J., Caughey G.H. Dipeptidyl peptidase I is essential for activation of mast cell chymases, but not tryptases, in mice. J Biol Chem 2001; 276(21): 18551–18556, https://doi.org/10.1074/jbc.m100223200.
  109. Noviana D., Kono F., Nagakui Y., Shimizu H., Mamba K., Makimura S., Horii Y. Distribution and enzyme histochemical characterisation of mast cells in cats. Histochem J 2001; 33(11–12): 597–603, https://doi.org/10.1023/a:1016324515108.
  110. Algermissen B., Bauer F., Schadendorf D., Kropp J.D., Czarnetzki B.M. Analysis of mast cell subpopulations (MCT, MCTC) in cutaneous inflammation using novel enzyme-histochemical staining techniques. Exp Dermatol 1994; 3(6): 290–297, https://doi.org/10.1111/j.1600-0625.1994.tb00291.x.
  111. Buckley M.G., McEuen A.R., Walls A.F. The detection of mast cell subpopulations in formalin-fixed human tissues using a new monoclonal antibody specific for chymase. J Pathol 1999; 189(1): 138–143, https://doi.org/10.1002/(sici)1096-9896(199909)189:1138::aid-path4003.0.co;2-h.
  112. Atyakshin D.A., Aralova M.V., Glukhov A.A. Molecular biological peculiarities of the must cells secretome of the lower limb skin in trophic ulcers of various etiologies. Zurnal anatomii i gistopatologii 2019; 8(1): 14–24, https://doi.org/10.18499/2225-7357-2019-8-1-14-24.
  113. Enkova E.V., Atiakshin D.A., Gaiskaya O.V., Hoperskaya O.V. Evaluation of the population of the mast cells of the decidual tissue and the status of vitamin D in women with undeveloped pregnancy in the embryonic period. Vestnik novyh medicinskih tehnologij 2018; 25(3): 21–27, https://doi.org/10.24411/1609-2163-2018-16141.
  114. Yamada M., Ueda M., Naruko T., Tanabe S., Han Y.S., Ikura Y., Ogami M., Takai S., Miyazaki M. Mast cell chymase expression and mast cell phenotypes in human rejected kidneys. Kidney Int 2001; 59(4): 1374–1381, https://doi.org/10.1046/j.1523-1755.2001.0590041374.x.
  115. Yao L., Baltatzis S., Zafirakis P., Livir-Rallatos C., Voudouri A., Markomichelakis N., Zhao T., Foster C.S. Human mast cell subtypes in conjunctiva of patients with atopic keratoconjunctivitis, ocular cicatricial pemphigoid and Stevens–Johnson syndrome. Ocul Immunol Inflamm 2003; 11(3): 211–222, https://doi.org/10.1076/ocii.11.3.211.17353.
  116. Beil W.J., Pammer J. In situ detection of the mast cell proteases chymase and tryptase in human lung tissue using light and electron microscopy. Histochem Cell Biol 2001; 116(6): 483–493, https://doi.org/10.1007/s00418-001-0339-1.
  117. Solari V., Unemoto K., Piaseczna Piotrowska A., Puri P. Increased expression of mast cells in reflux nephropathy. Pediat Nephrol 2004; 19(2): 157–163, https://doi.org/10.1007/s00467-003-1323-x.
  118. Walls A.F., Amalinei C. Detection of mast cells and basophils by immunohistochemistry. Methods Mol Biol 2020; 2163: 263–280, https://doi.org/10.1007/978-1-0716-0696-4_22.
  119. Grandi D., Massi M., Morini G. Long-term peripheral infusion of nociceptin/orphanin FQ promotes hyperplasia, activation and migration of mucosal mast cells in the rat gastric fundus. Peptides 2011; 32(4): 729–736, https://doi.org/10.1016/j.peptides.2011.01.012.
  120. Korkmaz O.T., Tunçel N., Tunçel M., Oncü E.M., Şahintürk V., Çelik M. Vasoactive intestinal peptide (VIP) treatment of Parkinsonian rats increases thalamic gamma-aminobutyric acid (GABA) levels and alters the release of nerve growth factor (NGF) by mast cells. J Mol Neurosci 2010; 41(2): 278–287, https://doi.org/10.1007/s12031-009-9307-3.
  121. Lennartsson J., Rönnstrand L. Stem cell factor receptor/c-Kit: from basic science to clinical implications. Physiol Rev 2012; 92(4): 1619–1649, https://doi.org/10.1152/physrev.00046.2011.
  122. Patel N., Mohammadi A., Rhatigan R. A comparative analysis of mast cell quantification in five common dermatoses: lichen simplex chronicus, psoriasis, lichen planus, lupus, and insect bite/allergic contact dermatitis/nummular dermatitis. ISRN Dermatol 2012; 2012: 759630, https://doi.org/10.5402/2012/759630.
  123. Kotov G., Landzhov B., Stamenov N., Stanchev S., Iliev A. Changes in the number of mast cells, expression of fibroblast growth factor-2 and extent of interstitial fibrosis in established and advanced hypertensive heart disease. Ann Anat 2020; 232: 151564, https://doi.org/10.1016/j.aanat.2020.151564.
  124. Atyakshin D.A., Nikityuk D.B., Klochkova S.V., Alexeeva N.T., Burtseva A.S. The participation of mast cells in adaptation of the stomach of mongolian gerbils to the gravitational factor. Zurnal anatomii i gistopatologii 2018; 7(1): 14–26, https://doi.org/10.18499/2225-7357-2018-7-1-14-26.
  125. Qi J.C., Li L., Li Y., Moore K., Madigan M.C., Katsoulotos G., Krilis S.A. An antibody raised against in vitro-derived human mast cells identifies mature mast cells and a population of cells that are FcɛRI+, tryptase–, and chymase– in a variety of human tissues. J Histochem Cytochem 2003; 51(5): 643–653, https://doi.org/10.1177/002215540305100510.
  126. Arber D.A., Tamayo R., Weiss L.M. Paraffin section detection of the c-kit gene product (CD117) in human tissues: value in the diagnosis of mast cell disorders. Hum Pathol 1998; 29(5): 498–504, https://doi.org/10.1016/s0046-8177(98)90066-1.
  127. Lammie A., Drobnjak M., Gerald W., Saad A., Cote R., Cordon-Cardo C. Expression of c-kit and kit ligand proteins in normal human tissues. J Histochem Cytochem 1994; 42(11): 1417–1425, https://doi.org/10.1177/42.11.7523489.
  128. Miettinen M., Lasota J. KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl Immunohistochem Mol Morphol 2005; 13(3): 205–220, https://doi.org/10.1097/01.pai.0000173054.83414.22.
  129. Ribatti D. The staining of mast cells: a historical overview. Int Arch Allergy Immunol 2018; 176(1): 55–60, https://doi.org/10.1159/000487538.
  130. Medinger M., Kleinschmidt M., Mross K., Wehmeyer B., Unger C., Schaefer H.E., Weber R., Azemar M. c-kit (CD117) expression in human tumors and its prognostic value: an immunohistochemical analysis. Pathol Oncol Res 2010; 16(3): 295–301, https://doi.org/10.1007/s12253-010-9247-9.
  131. Pilloni L., Bianco P., Difelice E., Cabras S., Castellanos M.E., Atzori L., Ferreli C., Mulas P., Nemolato S., Faa G. The usefulness of c-Kit in the immunohistochemical assessment of melanocytic lesions. Eur J Histochem 2011; 55(2): e20, https://doi.org/10.4081/ejh.2011.e20.
  132. Sailasuta A., Ketpun D., Piyaviriyakul P., Theerawatanasirikul S., Theewasutrakul P., Rungsipipat A. The relevance of CD117-immunocytochemistry staining patterns to mutational exon-11 in c-kit detected by PCR from fine-needle aspirated canine mast cell tumor cells. Vet Med Int 2014; 2014: 787498, https://doi.org/10.1155/2014/787498.
  133. Andersson C.K., Bergqvist A., Mori M., Mauad T., Bjermer L., Erjefält J.S. Mast cell-associated alveolar inflammation in patients with atopic uncontrolled asthma. J Allergy Clin Immunol 2011; 127(4): 905-912.E127, https://doi.org/10.1016/j.jaci.2011.01.022.
  134. Stone K.D., Prussin C., Metcalfe D.D. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol 2010; 125(2 Suppl 2): S73–S80, https://doi.org/10.1016/j.jaci.2009.11.017.
  135. Ying S., Barata L.T., Meng Q., Grant J., Barkans J., Durham S.R., Kay A.B. High-affinity immunoglobulin E receptor (FcεRI)-bearing eosinophils, mast cells, macrophages and Langerhans’ cells in allergen-induced late-phase cutaneous reactions in atopic subjects. Immunology 1998; 93(2): 281–288, https://doi.org/10.1046/j.1365-2567.1998.00418.x.
  136. Johansson O., Virtanen M., Hilliges M., Yang Q. Histamine immunohistochemistry: a new and highly sensitive method for studying cutaneous mast cells. Histochem J 1992; 24(5): 283–287, https://doi.org/10.1007/bf01046843.
  137. Manning K.A., Pienkowski T.P., Uhlrich D.J. Histaminergic and non-histamine-immunoreactive mast cells within the cat lateral geniculate complex examined with light and electron microscopy. Neuroscience 1994; 63(1): 191–206, https://doi.org/10.1016/0306-4522(94)90016-7.
  138. Mallett C.L., Northrup N.C., Saba C.F., Rodriguez C.O., Rassnick K.M., Gieger T.L., Childress M.O., Howerth E.W. Immunohistochemical characterization of feline mast cell tumors. Vet Pathol 2013; 50(1): 106–109, https://doi.org/10.1177/0300985812441032.
  139. Alcañiz L., Vega A., Chacón P., El Bekay R., Ventura I., Aroca R., Blanca M., Bergstralh D.T., Monteseirin J. Histamine production by human neutrophils. FASEB J 2013; 27(7): 2902–2910, https://doi.org/10.1096/fj.12-223867.
  140. Walker A.K., Park W.M., Chuang J.C., Perello M., Sakata I., Osborne-Lawrence S., Zigman J.M. Characterization of gastric and neuronal histaminergic populations using a transgenic mouse model. PLoS One 2013; 8(3): e60276, https://doi.org/10.1371/journal.pone.0060276.
  141. Stead R.H., Perdue M.H., Blennerhassett M.G., Kakuta Y., Sestini P., Bienenstock J. The innervation of mast cells. In: The neuroendocrine-immune network. Freier S. (editor). Boca Raton: CRC Press; 1990; p. 19–37.
  142. Fernandez N.J., West K.H., Jackson M.L., Kidney B.A. Immunohistochemical and histochemical stains for differentiating canine cutaneous round cell tumors. Vet Pathol 2005; 42(4): 437–445, https://doi.org/10.1354/vp.42-4-437.
  143. Michaloudi H.C., Papadopoulos G.C. Mast cells in the sheep, hedgehog and rat forebrain. J Anat 1999; 195(4): 577–586, https://doi.org/10.1046/j.1469-7580.1999.19540577.x.
  144. Wilhelm M. Neuro-immune interactions in the dove brain. Gen Comp Endocrinol 2011; 172(1): 173–180, https://doi.org/10.1016/j.ygcen.2011.03.018.
  145. Berger M., Gray J.A., Roth B.L. The expanded biology of serotonin. Annu Rev Med 2009; 60: 355–366, https://doi.org/10.1146/annurev.med.60.042307.110802.
  146. Jiménez-Trejo F., Tapia-Rodríguez M., Queiroz D.B., Padilla P., Avellar M.C., Manzano P.R., Manjarrez-Gutiérrez G., Gutiérrez-Ospina G. Serotonin concentration, synthesis, cell origin, and targets in the rat caput epididymis during sexual maturation and variations associated with adult mating status: morphological and biochemical studies. J Androl 2007; 28(1): 136–149, https://doi.org/10.2164/jandrol.106.000653.
  147. Livermore S., Zhou Y., Pan J., Yeger H., Nurse C.A., Cutz E. Pulmonary neuroepithelial bodies are polymodal airway sensors: evidence for CO2/H+ sensing. Am J Physiol Lung Cell Mol Physiol 2015; 308(8): L807–L815, https://doi.org/10.1152/ajplung.00208.2014.
  148. Pai V.P., Marshall A.M. Intraluminal volume homeostasis: a common sertonergic mechanism among diverse epithelia. Commun Integr Biol 2011; 4(5): 532–537.
  149. Okamoto T., Barton M.J., Hennig G.W., Birch G.C., Grainger N., Corrigan R.D., Koh S.D., Sanders K.M., Smith T.K. Extensive projections of myenteric serotonergic neurons suggest they comprise the central processing unit in the colon. Neurogastroenterol Motil 2014; 26(4): 556–570, https://doi.org/10.1111/nmo.12302.
  150. Okaty B.W., Commons K.G., Dymecki S.M. Embracing diversity in the 5-HT neuronal system. Nat Rev Neurosci 2019; 20(7): 397–424, https://doi.org/10.1038/s41583-019-0151-3.
  151. Pan H.R., Tian M., Xue J.B., Li S.M., Luo X.C., Huang X., Chen Z.H., Huang L. Mammalian taste bud cells utilize extragemmal 5-hydroxy-l-tryptophan to biosynthesize the neurotransmitter serotonin. Front Cell Neurosci 2018; 12: 461, https://doi.org/10.3389/fncel.2018.00461.
  152. Yokoyama T., Misuzu Y.Y., Yamamoto Y. Immunohistochemical localization of tryptophan hydroxylase and serotonin transporter in the carotid body of the rat. Histochem Cell Biol 2012; 140(2): 147–155, https://doi.org/10.1007/s00418-012-1066-5.
  153. Ranzil S., Ellery S., Walker D.W., Vaillancourt C., Alfaidy N., Bonnin A., Borg A., Wallace E.M., Ebeling P.R., Erwich J.J., Murthi P. Disrupted placental serotonin synthetic pathway and increased placental serotonin: potential implications in the pathogenesis of human fetal growth restriction. Placenta 2019; 84: 74–83, https://doi.org/10.1016/j.placenta.2019.05.012.
  154. He W., Wang X.Y., Shi H., Bai W.Z., Cheng B., Su Y.S., Yu X.C., Jing X.H., Zhu B. Cutaneous neurogenic inflammation in the sensitized acupoints induced by gastric mucosal injury in rats. BMC Complement Altern Med 2017; 17(1): 141, https://doi.org/10.1186/s12906-017-1580-z.
  155. Slominski A.T., Kim T.K., Kleszczyński K., Semak I., Janjetovic Z., Sweatman T., Skobowiat C., Steketee J.D., Lin Z., Postlethwaite A., Li W., Reiter R.J., Tobin D.J. Characterization of serotonin and N-acetylserotonin systems in the human epidermis and skin cells. J Pineal Res 2020; 68(2): e12626, https://doi.org/10.1111/jpi.12626.
  156. Maeda T., Miura Y., Fukuda K., Hayashi S., Kurosaka M. Decoy receptor 3 regulates the expression of tryptophan hydroxylase 1 in rheumatoid synovial fibroblasts. Mol Med Rep 2015; 12(4): 5191–5196, https://doi.org/10.3892/mmr.2015.4097.
  157. Ni W., Watts S.W. 5-Hydroxytryptamine in the cardiovascular system: focus on the serotonin transporter (SERT). Clin Exp Pharmacol Physiol 2006; 33(7): 575–583, https://doi.org/10.1111/j.1440-1681.2006.04410.x.
  158. Craig S.S., Irani A.M., Metcalfe D.D., Schwartz L.B. Ultrastructural localization of heparin to human mast cells of the MCTC and MCT types by labeling with antithrombin III-gold. Lab Invest 1993; 69(5): 552–561.
  159. Shurygina I.A., Shurygin M.G. Mast cell identification method for histological study. Mezdunarodnyj zurnal prikladnyh i fundamentalʹnyh issledovanij 2019; 12(1): 97–100, https://doi.org/10.17513/mjpfi.12961.
  160. Cárdenas-Rivera A., Campero-Romero A.N., Heras-Romero Y., Penagos-Puig A., Rincón-Heredia R., Tovar-Y-Romo L.B. Early post-stroke activation of vascular endothelial growth factor receptor 2 hinders the receptor 1-dependent neuroprotection afforded by the endogenous ligand. Front Cell Neurosci 2019; 13: 270, https://doi.org/10.3389/fncel.2019.00270.
  161. Fehrenbach H., Haase M., Kasper M., Koslowski R., Schuh D., Müller M. Alterations in the immunohistochemical distribution patterns of vascular endothelial growth factor receptors Flk1 and Flt1 in bleomycin-induced rat lung fibrosis. Virchows Arch 1999; 435(1): 20–31, https://doi.org/10.1007/s004280050390.
  162. Leplina O., Smetanenko E., Tikhonova M., Batorov E., Tyrinova T., Pasman N., Ostanin A., Chernykh E. Binding of the placental growth factor to VEGF receptor type 1 modulates human T cell functions. J Leukoc Biol 2020; 108(3): 1013–1024, https://doi.org/10.1002/jlb.2a0420-723rr.
  163. Scarpellini F., Klinger F.G., Rossi G., Sbracia M. Immunohistochemical study on the expression of G-CSF, G-CSFR, VEGF, VEGFR-1, Foxp3 in first trimester trophoblast of recurrent pregnancy loss in pregnancies treated with G-CSF and controls. Int J Mol Sci 2019; 21(1): 285, https://doi.org/10.3390/ijms21010285.
  164. Tyrsina E.G., Nikulitskiy S.I., Inshakov A.N., Ryabaya O.O. VEGF-R1 as a potential molecular target for anticancer therapy. Doklady Akademii nauk 2018; 478(1): 18–20, https://doi.org/10.1134/s1607672918010052.
  165. Mason C.A., Carter L.M., Mandleywala K., de Souza Franca P.D., Meyer J.P., Mamun T., Backer J.M., Backer M.V., Reiner T., Lewis J.S. Imaging early-stage metastases using an 18F-labeled VEGFR-1-specific single chain VEGF mutant. Mol Imaging Biol 2021; 23(3): 340–349, https://doi.org/10.1007/s11307-020-01555-z.
  166. Chen L.Z., Kan Y., Zhang Z.Y., Wang Y.L., Zhang X.N., Wang X.Y., He W., Jing X.H. Neuropeptide initiated mast cell activation by transcutaneous electrical acupoint stimulation of acupoint LI4 in rats. Sci Rep 2018; 8(1): 13921, https://doi.org/10.1038/s41598-018-32048-3.
  167. Khalil M., Ronda J., Weintraub M., Jain K., Silver R., Silverman A.J. Brain mast cell relationship to neurovasculature during development. Brain Res 2007; 1171: 18–29, https://doi.org/10.1016/j.brainres.2007.07.034.
  168. Tikoo S., Barki N., Jain R., Zulkhernain N.S., Buhner S., Schemann M., Weninger W. Imaging of mast cells. Immun Rev 2018; 282(1): 58–72, https://doi.org/10.1111/imr.12631.
Grigorev I.P., Korzhevskii D.E. Modern Imaging Technologies of Mast Cells for Biology and Medicine (Review). Sovremennye tehnologii v medicine 2021; 13(4): 93, https://doi.org/10.17691/stm2021.13.4.10


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