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The Phagocyte, Metchnikoff, and the Foundation of Immunology

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  • Authors: Giuseppe Teti1, Carmelo Biondo2, Concetta Beninati3
  • Editor: Siamon Gordon4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Metchnikoff Laboratory, Department of Pediatric, Gynecological, Microbiological and Biomedical Sciences, University of Messina, Messina, Italy; 2: Metchnikoff Laboratory, Department of Pediatric, Gynecological, Microbiological and Biomedical Sciences, University of Messina, Messina, Italy; 3: Metchnikoff Laboratory, Department of Pediatric, Gynecological, Microbiological and Biomedical Sciences, University of Messina, Messina, Italy; 4: Oxford University, Oxford, United Kingdom
    • Source: microbiolspec April 2016 vol. 4 no. 2 doi:10.1128/microbiolspec.MCHD-0009-2015
  • Received 14 May 2015 Accepted 17 July 2015 Published 22 April 2016
  • Giuseppe Teti, [email protected]
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  • Abstract:

    Since the ability of some cells to engulf particulate material was observed before Metchnikoff, he did not “discover” phagocytosis, as is sometimes mentioned in textbooks. Rather, he assigned to particle internalization the role of defending the host against noxious stimuli, which represented a new function relative to the previously recognized task of intracellular digestion. With this proposal, Metchnikoff built the conceptual framework within which immunity could finally be seen as an active host function triggered by noxious stimuli. In this sense, Metchnikoff can be rightly regarded as the father of all immunological sciences and not only of innate immunity or myeloid cell biology. Moreover, the recognition properties of his phagocyte fit surprisingly well with recent discoveries and modern models of immune sensing. For example, rather than assigning to immune recognition exclusively the function of eliminating nonself components (as others did after him), Metchnikoff viewed phagocytes as homeostatic agents capable of monitoring the internal environment and promoting tissue remodeling, thereby continuously defining the identity of the organism. No doubt, Metchnikoff’s life and creativity can provide, still today, a rich source of inspiration.

  • Citation: Teti G, Biondo C, Beninati C. 2016. The Phagocyte, Metchnikoff, and the Foundation of Immunology. Microbiol Spectrum 4(2):MCHD-0009-2015. doi:10.1128/microbiolspec.MCHD-0009-2015.

Key Concept Ranking

Innate Immune System
0.6115988
White Blood Cells
0.54470587
Immune Systems
0.5318197
Toll-Like Receptor 4
0.5086539
Toll-Like Receptor 2
0.50485235
0.6115988

References

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2. Mechnikov I. 1908. On the present state of the question of immunity in infectious diseases. Nobel lecture, December 11, 1908.
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7. Gourko H, Williamson DI, Tauber AI. 2000. Introduction, p 3–32. In Gourko H, Williamson DI, Tauber AI (ed), The Evolutionary Biology Papers of Elie Metchnikoff. Kluwer Academic Publishers, Dordrecht, The Netherlands. [CrossRef]
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19. Jungeblut CW, Berlot JA. 1926. The role of the reticulo-endothelial system in immunity. I. The role of the reticulo-endothelial system in the production of diphtheria antitoxin. J Exp Med 43:613–622. [PubMed][CrossRef]
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25. Metchnikoff E. 2000. The struggle for existence between parts of the animal organism, p 207–216. In Gourko H, Williamson DI, Tauber AI (ed), The Evolutionary Biology Papers of Elie Metchnikoff. Kluwer Academic Publishers, Dordrecht, The Netherlands.
26. Anderson KV, Jürgens G, Nüsslein-Volhard C. 1985. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42:779–789. [PubMed][CrossRef]
27. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. 1996. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973–983. [CrossRef]
28. Metchnikoff O. 1924. The Life of Elie Metchnikoff 1845–1916 (Lankester ER, transl). Constable, London, United Kingdom.
29. Metchnikoff E. 1905. Immunity in Infective Diseases (Binnie FG, transl). Cambridge University Press, Cambridge, United Kingdom.
30. Metchnikoff E. 1968. Lectures on the Comparative Pathology of Inflammation (Starling FA, Starling, EH, transl). Dover, New York, NY.
31. Seong SY, Matzinger P. 2004. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 4:469–478. [PubMed][CrossRef]
32. Pollard JW. 2009. Trophic macrophages in development and disease. Nat Rev Immunol 9:259–270. [PubMed][CrossRef]
33. Tauber AI. 2003. Metchnikoff and the phagocytosis theory. Nat Rev Mol Cell Biol 4:898–901. [PubMed][CrossRef]
34. Hotamisligil GS, Erbay E. 2008. Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol 8:923–934. [PubMed][CrossRef]
35. Efeyan A, Comb WC, Sabatini DM. 2015. Nutrient-sensing mechanisms and pathways. Nature 517:302–310. [PubMed][CrossRef]
36. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. 2006. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116:3015–3025. [PubMed][CrossRef]
37. Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, Prada PO, Hirabara SM, Schenka AA, Araújo EP, Vassallo J, Curi R, Velloso LA, Saad MJ. 2007. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 56:1986–1998. [PubMed][CrossRef]
38. Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME. 2008. Tlr-4 deficiency selectively protects against obesity induced by diets high in saturated fat. Obesity (Silver Spring) 16:1248–1255. [PubMed][CrossRef]
39. Ajuwon KM, Spurlock ME. 2005. Palmitate activates the NF-κB transcription factor and induces IL-6 and TNFα expression in 3T3-L1 adipocytes. J Nutr 135:1841–1846. [PubMed]
40. Akira S, Uematsu S, Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell 124:783–801. [PubMed][CrossRef]
41. Khazen W, M’bika JP, Tomkiewicz C, Benelli C, Chany C, Achour A, Forest C. 2005. Expression of macrophage-selective markers in human and rodent adipocytes. FEBS Lett 579:5631–5634. [PubMed][CrossRef]
42. Chung S, Lapoint K, Martinez K, Kennedy A, Boysen Sandberg M, McIntosh MK. 2006. Preadipocytes mediate lipopolysaccharide-induced inflammation and insulin resistance in primary cultures of newly differentiated human adipocytes. Endocrinology 147:5340–5351. [PubMed][CrossRef]
43. Levine B, Mizushima N, Virgin HW. 2011. Autophagy in immunity and inflammation. Nature 469:323–335. [PubMed][CrossRef]
44. Arnold G. 1909. Intra-cellular and general digestive processes in Planariae. Quart J Micro Sci 54:207.
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Abstract:

Since the ability of some cells to engulf particulate material was observed before Metchnikoff, he did not “discover” phagocytosis, as is sometimes mentioned in textbooks. Rather, he assigned to particle internalization the role of defending the host against noxious stimuli, which represented a new function relative to the previously recognized task of intracellular digestion. With this proposal, Metchnikoff built the conceptual framework within which immunity could finally be seen as an active host function triggered by noxious stimuli. In this sense, Metchnikoff can be rightly regarded as the father of all immunological sciences and not only of innate immunity or myeloid cell biology. Moreover, the recognition properties of his phagocyte fit surprisingly well with recent discoveries and modern models of immune sensing. For example, rather than assigning to immune recognition exclusively the function of eliminating nonself components (as others did after him), Metchnikoff viewed phagocytes as homeostatic agents capable of monitoring the internal environment and promoting tissue remodeling, thereby continuously defining the identity of the organism. No doubt, Metchnikoff’s life and creativity can provide, still today, a rich source of inspiration.

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The Phagocyte, Metchnikoff, and the Foundation of Immunology
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Citation: Teti G, Biondo C, Beninati C. 2016. The phagocyte, metchnikoff, and the foundation of immunology. microbiolspec 4(2): doi:10.1128/microbiolspec.MCHD-0009-2015
/content/microbiolspec/10.1128/microbiolspec.MCHD-0009-2015.fig1
FIGURE 1

Metchnikoff’s parents. Reproduced from reference 10 , with permission.

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FIGURE 1

Metchnikoff’s parents. Reproduced from reference 10 , with permission.

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FIGURE 2

Olga Metchnikoff. Reproduced from reference 10 , with permission.

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FIGURE 2

Olga Metchnikoff. Reproduced from reference 10 , with permission.

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FIGURE 3

Elie and Olga Metchnikoff. Reproduced from reference 15 , with permission.

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FIGURE 3

Elie and Olga Metchnikoff. Reproduced from reference 15 , with permission.

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FIGURE 4

Columnar cells from a flatworm showing intracellular digestion in planariae. Reproduced from reference 44 .

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FIGURE 4

Columnar cells from a flatworm showing intracellular digestion in planariae. Reproduced from reference 44 .

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FIGURE 5

Elie Metchnikoff at 46 years of age. Reproduced from reference 10 , with permission.

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FIGURE 5

Elie Metchnikoff at 46 years of age. Reproduced from reference 10 , with permission.

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FIGURE 6

Elie Metchnikoff and Alexandre Besredka, Institut Pasteur, 1914. Besredka was a medical doctor from Odessa who collaborated with Metchnikoff at the Institut Pasteur from 1897. Reproduced from reference 10 , with permission.

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FIGURE 6

Elie Metchnikoff and Alexandre Besredka, Institut Pasteur, 1914. Besredka was a medical doctor from Odessa who collaborated with Metchnikoff at the Institut Pasteur from 1897. Reproduced from reference 10 , with permission.

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FIGURE 7

Elie Metchnikoff portrait painted by Olga. Reproduced from reference 15 .

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FIGURE 7

Elie Metchnikoff portrait painted by Olga. Reproduced from reference 15 .

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FIGURE 8

Robert Koch visiting the Institut Pasteur, accompanied by Elie Metchnikoff (1904). Reproduced from reference 15 , with permission.

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FIGURE 8

Robert Koch visiting the Institut Pasteur, accompanied by Elie Metchnikoff (1904). Reproduced from reference 15 , with permission.

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FIGURE 9

Milestones in the life of Elie Metchnikoff.

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FIGURE 9

Milestones in the life of Elie Metchnikoff.

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