The mast cell: An evolutionary perspective

Enrico Crivellato, Domenico Ribatti

Research output: Contribution to journalArticle

61 Citations (Scopus)

Abstract

This review article is an attempt to trace the evolution of mast cells (MCs). These immune cells have been identified in all vertebrate classes as single-lobed cells containing variable amounts of membrane-bound secretory granules which store a large series of mediators, namely histamine, proteases, cytokines and growth factors. Other MC features, at least in mammals, are the c-kit receptor for the stem cell factor and the high-affinity receptor, FcεRI, for immunoglobulin E (IgE). The c-kit receptor also has been identified in fish MCs. The FcεRI receptor seems to be a more recent acquisition in MC phylogenesis given that IgE originated in mammalian species. Tryptase and histamine have also been recognized in MCs of teleost fish. Thus, a cell population with the overall characteristics of higher vertebrate MCs is identifiable in the most evolutionarily advanced fish species. Two potential MC progenitors have been identified in ascidians (urochordates which appeared approximately 500 million years ago): the basophil/MC-like granular haemocyte and the test cell. Both contain histamine and heparin, and provide defensive functions. Some granular haemocytes in Arthropoda also closely approximate the ultrastructure of modern MCs. The origin of MCs is probably to be found in a leukocyte ancestor operating in the context of a primitive local innate immunity and involved in phagocytic and killing activity against pathogens. From this type of defensive cell, the MC phylogenetic progenitor evolved into a tissue regulatory and remodelling cell, which was incorporated into the networks of recombinase activating genes (RAG)-mediated adaptive immunity in the Cambrian era, some 550 million years ago. Early MCs probably appeared in the last common ancestor we shared with hagfish, lamprey and sharks about 450-500 million years ago.

Original languageEnglish
Pages (from-to)347-360
Number of pages14
JournalBiological Reviews
Volume85
Issue number2
DOIs
Publication statusPublished - May 2010

Fingerprint

mast cells
Mast Cells
Proto-Oncogene Proteins c-kit
Fish
Histamine
Immunoglobulin E
Tryptases
Recombinases
Stem Cell Factor
Mammals
Pathogens
Heparin
Intercellular Signaling Peptides and Proteins
Peptide Hydrolases
histamine
Genes
Cells
Tissue
Cytokines
Membranes

Keywords

  • Adaptive immunity
  • Granular haemocytes
  • Innate immunity
  • Mast cells
  • Phylogeny
  • Urochordates
  • Vertebrates

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

The mast cell : An evolutionary perspective. / Crivellato, Enrico; Ribatti, Domenico.

In: Biological Reviews, Vol. 85, No. 2, 05.2010, p. 347-360.

Research output: Contribution to journalArticle

Crivellato, Enrico ; Ribatti, Domenico. / The mast cell : An evolutionary perspective. In: Biological Reviews. 2010 ; Vol. 85, No. 2. pp. 347-360.
@article{f407abd5d5554531ad9a67c089683d7b,
title = "The mast cell: An evolutionary perspective",
abstract = "This review article is an attempt to trace the evolution of mast cells (MCs). These immune cells have been identified in all vertebrate classes as single-lobed cells containing variable amounts of membrane-bound secretory granules which store a large series of mediators, namely histamine, proteases, cytokines and growth factors. Other MC features, at least in mammals, are the c-kit receptor for the stem cell factor and the high-affinity receptor, FcεRI, for immunoglobulin E (IgE). The c-kit receptor also has been identified in fish MCs. The FcεRI receptor seems to be a more recent acquisition in MC phylogenesis given that IgE originated in mammalian species. Tryptase and histamine have also been recognized in MCs of teleost fish. Thus, a cell population with the overall characteristics of higher vertebrate MCs is identifiable in the most evolutionarily advanced fish species. Two potential MC progenitors have been identified in ascidians (urochordates which appeared approximately 500 million years ago): the basophil/MC-like granular haemocyte and the test cell. Both contain histamine and heparin, and provide defensive functions. Some granular haemocytes in Arthropoda also closely approximate the ultrastructure of modern MCs. The origin of MCs is probably to be found in a leukocyte ancestor operating in the context of a primitive local innate immunity and involved in phagocytic and killing activity against pathogens. From this type of defensive cell, the MC phylogenetic progenitor evolved into a tissue regulatory and remodelling cell, which was incorporated into the networks of recombinase activating genes (RAG)-mediated adaptive immunity in the Cambrian era, some 550 million years ago. Early MCs probably appeared in the last common ancestor we shared with hagfish, lamprey and sharks about 450-500 million years ago.",
keywords = "Adaptive immunity, Granular haemocytes, Innate immunity, Mast cells, Phylogeny, Urochordates, Vertebrates",
author = "Enrico Crivellato and Domenico Ribatti",
year = "2010",
month = "5",
doi = "10.1111/j.1469-185X.2009.00105.x",
language = "English",
volume = "85",
pages = "347--360",
journal = "Biological Reviews of the Cambridge Philosophical Society",
issn = "0006-3231",
publisher = "Cambridge University Press",
number = "2",

}

TY - JOUR

T1 - The mast cell

T2 - An evolutionary perspective

AU - Crivellato, Enrico

AU - Ribatti, Domenico

PY - 2010/5

Y1 - 2010/5

N2 - This review article is an attempt to trace the evolution of mast cells (MCs). These immune cells have been identified in all vertebrate classes as single-lobed cells containing variable amounts of membrane-bound secretory granules which store a large series of mediators, namely histamine, proteases, cytokines and growth factors. Other MC features, at least in mammals, are the c-kit receptor for the stem cell factor and the high-affinity receptor, FcεRI, for immunoglobulin E (IgE). The c-kit receptor also has been identified in fish MCs. The FcεRI receptor seems to be a more recent acquisition in MC phylogenesis given that IgE originated in mammalian species. Tryptase and histamine have also been recognized in MCs of teleost fish. Thus, a cell population with the overall characteristics of higher vertebrate MCs is identifiable in the most evolutionarily advanced fish species. Two potential MC progenitors have been identified in ascidians (urochordates which appeared approximately 500 million years ago): the basophil/MC-like granular haemocyte and the test cell. Both contain histamine and heparin, and provide defensive functions. Some granular haemocytes in Arthropoda also closely approximate the ultrastructure of modern MCs. The origin of MCs is probably to be found in a leukocyte ancestor operating in the context of a primitive local innate immunity and involved in phagocytic and killing activity against pathogens. From this type of defensive cell, the MC phylogenetic progenitor evolved into a tissue regulatory and remodelling cell, which was incorporated into the networks of recombinase activating genes (RAG)-mediated adaptive immunity in the Cambrian era, some 550 million years ago. Early MCs probably appeared in the last common ancestor we shared with hagfish, lamprey and sharks about 450-500 million years ago.

AB - This review article is an attempt to trace the evolution of mast cells (MCs). These immune cells have been identified in all vertebrate classes as single-lobed cells containing variable amounts of membrane-bound secretory granules which store a large series of mediators, namely histamine, proteases, cytokines and growth factors. Other MC features, at least in mammals, are the c-kit receptor for the stem cell factor and the high-affinity receptor, FcεRI, for immunoglobulin E (IgE). The c-kit receptor also has been identified in fish MCs. The FcεRI receptor seems to be a more recent acquisition in MC phylogenesis given that IgE originated in mammalian species. Tryptase and histamine have also been recognized in MCs of teleost fish. Thus, a cell population with the overall characteristics of higher vertebrate MCs is identifiable in the most evolutionarily advanced fish species. Two potential MC progenitors have been identified in ascidians (urochordates which appeared approximately 500 million years ago): the basophil/MC-like granular haemocyte and the test cell. Both contain histamine and heparin, and provide defensive functions. Some granular haemocytes in Arthropoda also closely approximate the ultrastructure of modern MCs. The origin of MCs is probably to be found in a leukocyte ancestor operating in the context of a primitive local innate immunity and involved in phagocytic and killing activity against pathogens. From this type of defensive cell, the MC phylogenetic progenitor evolved into a tissue regulatory and remodelling cell, which was incorporated into the networks of recombinase activating genes (RAG)-mediated adaptive immunity in the Cambrian era, some 550 million years ago. Early MCs probably appeared in the last common ancestor we shared with hagfish, lamprey and sharks about 450-500 million years ago.

KW - Adaptive immunity

KW - Granular haemocytes

KW - Innate immunity

KW - Mast cells

KW - Phylogeny

KW - Urochordates

KW - Vertebrates

UR - http://www.scopus.com/inward/record.url?scp=77950848877&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77950848877&partnerID=8YFLogxK

U2 - 10.1111/j.1469-185X.2009.00105.x

DO - 10.1111/j.1469-185X.2009.00105.x

M3 - Article

C2 - 19961471

AN - SCOPUS:77950848877

VL - 85

SP - 347

EP - 360

JO - Biological Reviews of the Cambridge Philosophical Society

JF - Biological Reviews of the Cambridge Philosophical Society

SN - 0006-3231

IS - 2

ER -