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Structure of the enterocyte transcytosis compartments during lipid absorption

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Abstract

In spite of tremendous progress in deciphering the molecular mechanisms involved in intracellular transport in cell culture and in the test tube, many aspects of this process in situ remain unclear. Here, we examined lipid transcytosis in enterocytes in adult rats. Apical clathrin-coated buds and the ER exit sites were not found. After starvation, the Golgi complex was in a non-transporting state and contained many vesicles, but no intercisternal connections and typical the cis-most and the trans-most cisternae. Following the addition of the lipids in the form of chyme, pre-chylomicrons (pre-ChMs) were initially found in the tubules of the smooth SER attached to the basolateral plasmalemma below the belt composed of adhesive junctions (AJ) and always connected with other cisternae. However, the ER exit sites were still absent. Pre-ChMs moved into the cis-most cisterna and were concentrated in cisternal distensions at the trans-side of the Golgi complex. This induced attachment of the cis-most and the trans-most cisternae to the Golgi complex. Post-Golgi carriers fused with the basolateral plasmalemma and delivered ChMs outside. Overloading of enterocytes with lipids resulted in an accumulation of lipid droplets, an increase of the diameter of ChMs, and shift of the Golgi complex to the transporting state with the formation of intercisternal connections, attachment of the cis-most and the trans-most cisternae and disappearance of vesicles. These data are discussed from the functional point of view. In spite of tremendous progress in deciphering the molecular mechanisms involved in intracellular transport in cell culture and in the test tube, many aspects of this process in situ remain unclear. Here, we examined lipid transcytosis in enterocytes in adult rats. Apical clathrin-coated buds and the ER exit sites were not found. After starvation, the Golgi complex was in a non-transporting state and contained many vesicles, but no intercisternal connections and typical the cis-most and the trans-most cisternae. Following the addition of the lipids in the form of chyme, pre-chylomicrons (pre-ChMs) were initially found in the tubules of the smooth SER attached to the basolateral plasmalemma below the belt composed of adhesive junctions (AJ) and always connected with other cisternae. However, the ER exit sites were still absent. Pre-ChMs moved into the cis-most cisterna and were concentrated in cisternal distensions at the trans-side of the Golgi complex. This induced attachment of the cis-most and the trans-most cisternae to the Golgi complex. Post-Golgi carriers fused with the basolateral plasmalemma and delivered ChMs outside. Overloading of enterocytes with lipids resulted in an accumulation of lipid droplets, an increase of the diameter of ChMs, and shift of the Golgi complex to the transporting state with the formation of intercisternal connections, attachment of the cis-most and the trans-most cisternae and disappearance of vesicles. These data are discussed from the functional point of view.

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Fig. 1
Fig. 2

taken from the set of serial tomography images (images number 14, 17, 26, 51 and 63 from the set). AJs and actin filaments attached to them are coloured in red; actin bundles are coloured in green. The bundles attached to AJs are localized at the lateral areas of IDCs. These bundles could produce force, which contracts distended IDCs inducing movement of ChMs towards the basement membrane. (K) Protrusion (white arrow) of the dendritic cell (asterisk) within the basement membrane of enterocyte. (L) Pores in the enterocyte basement membrane. Scale bars: 2.5 µm (a); 270 nm (b–j); 1.2 µm (k); 30 µm (l)

Fig. 3
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Fig. 7

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Abbreviations

AJ:

Adhesive junction

APM:

Apical PM

Apo:

Apo-lipoprotein

BLPM:

Basolateral PM

ChM:

Chylomicron

CMC:

cis-Most cisterna

CLEM:

Correlative light-EM

EM:

Electron microscopy

ER:

Endoplasmic reticulum

ERES:

ER exit sites

FFA:

Free fatty acid

GC:

Golgi complex

GJ:

Gap junction

IDC:

Interdigitated contact

OTOTO:

Osmium-thiocarbohydrazide-osmium-thiocarbobydazide-osmium

PM:

Plasma membrane

pre-ChM:

Pre-chylomicron

SEM:

Scanning EM

SER:

Smooth ER

TJ:

Tight junction

TMC:

trans-Most cisterna

3DEM:

Three-dimensional EM

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Acknowledgements

We thank FIRC’s support of laboratory, INTAS (Project 99-4-1732), Telethon (E.1105), the Italian National Research Council (Convenzione CNR – Consorzio Mario Negri Sud to A.A.M.); FIRC (Italy) and Consorzio Mario Negri (Italy; to A.A.M.), Russian foundation of fundamental science (to I.V.S. and E.V.S.) for financial support. We acknowledge the Centre European of Nano-medicine (CEN Italy) for the possibility to use Tecnai 20 electron microscope; Dr. V. Sesorov for preparation of drawings, and Dr C. Wilson for discussion, critical suggestions and editing of the manuscript. We are especially grateful to our highly qualified reviewers, who have done a tremendous amount of work to improve our text, which without their work had no chance of being published.

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  1. Galina V. Beznoussenko and Alexander A. Mironov have equal contribution.

Authors and Affiliations

  1. Department of Anatomy, Ivanovo State Medical Academy, Ivanovo, Russia

    Irina S. Sesorova, Tatiana E. Kazakova & Maria A. Zdorikova

  2. Department of Anatomy, Saint Petersburg State Paediatric Medical University, St. Petersburg, Russia

    Natalia R. Karelina

  3. The FIRC Institute of Molecular Oncology, Via Adamello 16, 20139, Milan, Italy

    Ivan D. Dimov, Galina V. Beznoussenko & Alexander A. Mironov

  4. Institute of Protein Biochemistry, Consiglio Nazionale Delle Ricerche (CNR-IBP), Naples, Italy

    Seetharaman Parashuraman

  5. Laboratory of Renal Physiology, Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences, Torez Avenue, 44, 194223, St. Petersburg, Russia

    Elena V. Seliverstova

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Contributions

All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication. AM and GB designed the study and wrote the manuscript. IS participated in writing, made experiments and analyzed data. GB made electron microscopy. Others performed different experiments and approved the final version.

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Correspondence to Galina V. Beznoussenko or Alexander A. Mironov.

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The authors declare no conflict of interest. This article does not contain any study with humans, which was performed by the authors.

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All the institutional and national guidelines for the care and use of laboratory animals were followed. All experiments were approved by the decision of the Academic Committee of Saint Petersburg State Paediatric Medical University no. 10 from 23 September 2017 and decision of ethic committee of Ivanovo State Medical Academy (№1 from 5/XII, 2018) and in accordance with the ethical and legal standards of Russian Federation mentioned in the Order No. 755 of the Ministry of Health of the USSR of 12 August 1977 and Institutional Guidelines (in agreement with the rules of the Institutional Animal Care and Bioethics Committees).

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Supplementary file2 Figure S2. Structure of enterocytes after starvation (A) and during transcytosis of chylomicrons (B, C). (A) The thick (200-nm) Epon section of the enterocyte after rat starvation demonstrates the numerous tubules of the SER forming contacts with the BLPM. White arrows show tubules of the SER contacted with the BLPM which is situated below the adhesive junctions but above of the level at which the GC (asterisk) is usually visible. The near-plasmalemmal tubule of the SER (yellow arrow) is connected with the GER (red arrow). (A1) Enlargements of the area inside the white box in (D). (B, C) Serial sections of the GC after overloading of enterocyte with chyme. Disappearance (arrow) of the pores surrounding Golgi cisternal distensions. (D) Complicated ICD containing AJ inside (white arrows). Scale bars: 1000 nm (A); 300 nm (A1); 550 nm (B–D) (TIF 2931 kb)

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Sesorova, I.S., Karelina, N.R., Kazakova, T.E. et al. Structure of the enterocyte transcytosis compartments during lipid absorption. Histochem Cell Biol 153, 413–429 (2020). https://doi.org/10.1007/s00418-020-01851-3

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