The Role of Aquaporins in Dendritic Cell Macropinocytosis

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 2000 Feb 24

PMID 10684866

Citations 48

Authors

A de Baey

A Lanzavecchia

Affiliations

Soon will be listed here.

Abstract

Immature dendritic cells (DCs) constitutively take up large volumes of fluid by macropinocytosis and concentrate the macrosolutes in the endocytic compartment. This concentration mechanism that is the basis of their high capacity to present soluble antigens requires that DCs be capable of rapidly exchanging water across their membranes. We report that two members of the aquaporin family, AQP3 and AQP7, are expressed in immature DCs and are downregulated after maturation. Treatment of DCs with p-chloromercuribenzenesulphonate (pCMBS), a mercuric drug that blocks aquaporins, inhibited uptake and concentration of macrosolutes taken up by fluid phase endocytosis and led to dramatic cell swelling. In contrast, pCMBS did not affect receptor-mediated endocytosis via the mannose receptor. These findings indicate that aquaporins represent essential elements of a volume control mechanism that allows DCs to concentrate macrosolutes taken up via macropinocytosis.

Citing Articles

Exploring Aquaporins in Human Studies: Mechanisms and Therapeutic Potential in Critical Illness.

Vrettou C, Issaris V, Kokkoris S, Poupouzas G, Keskinidou C, Lotsios N Life (Basel). 2025; 14(12.

PMID: 39768394 PMC: 11676363. DOI: 10.3390/life14121688.

Aquaporin Channels in Skin Physiology and Aging Pathophysiology: Investigating Their Role in Skin Function and the Hallmarks of Aging.

Karimi N, Ahmadi V Biology (Basel). 2024; 13(11).

PMID: 39596817 PMC: 11592281. DOI: 10.3390/biology13110862.

Peroxiporins and Oxidative Stress: Promising Targets to Tackle Inflammation and Cancer.

da Silva I, Mlinaric M, Lourenco A, Perez-Garcia O, cipak Gasparovic A, Soveral G Int J Mol Sci. 2024; 25(15).

PMID: 39125952 PMC: 11313477. DOI: 10.3390/ijms25158381.

Water channel aquaporin 4 is required for T cell receptor mediated lymphocyte activation.

Nicosia M, Lee J, Beavers A, Kish D, Farr G, McGuirk P J Leukoc Biol. 2023; 113(6):544-554.

PMID: 36805947 PMC: 10848298. DOI: 10.1093/jleuko/qiad010.

Aquaporins in Immune System.

Quan Y, Kan B, Yang B Adv Exp Med Biol. 2023; 1398:195-202.

PMID: 36717495 DOI: 10.1007/978-981-19-7415-1_13.

References

West M, BRETSCHER M, Watts C . Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol. 1989; 109(6 Pt 1):2731-9. PMC: 2115909. DOI: 10.1083/jcb.109.6.2731. View

Regnault A, Lankar D, Lacabanne V, Rodriguez A, Thery C, Rescigno M . Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J Exp Med. 1999; 189(2):371-80. PMC: 2192989. DOI: 10.1084/jem.189.2.371. View

Traunecker A, Oliveri F, Karjalainen K . Myeloma based expression system for production of large mammalian proteins. Trends Biotechnol. 1991; 9(4):109-13. DOI: 10.1016/0167-7799(91)90038-j. View

Verkman A . Water channels in cell membranes. Annu Rev Physiol. 1992; 54:97-108. DOI: 10.1146/annurev.ph.54.030192.000525. View

Grinstein S, Woodside M, Sardet C, Pouyssegur J, Rotin D . Activation of the Na+/H+ antiporter during cell volume regulation. Evidence for a phosphorylation-independent mechanism. J Biol Chem. 1992; 267(33):23823-8. View

Racoosin E, Swanson J . M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J Cell Sci. 1992; 102 ( Pt 4):867-80. DOI: 10.1242/jcs.102.4.867. View

Preston G, Jung J, Guggino W, Agre P . The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J Biol Chem. 1993; 268(1):17-20. View

Zhang R, van Hoek A, Biwersi J, Verkman A . A point mutation at cysteine 189 blocks the water permeability of rat kidney water channel CHIP28k. Biochemistry. 1993; 32(12):2938-41. DOI: 10.1021/bi00063a002. View

Racoosin E, Swanson J . Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol. 1993; 121(5):1011-20. PMC: 2119679. DOI: 10.1083/jcb.121.5.1011. View

10.

Echevarria M, FRINDT G, Preston G, Milovanovic S, Agre P, Fischbarg J . Expression of multiple water channel activities in Xenopus oocytes injected with mRNA from rat kidney. J Gen Physiol. 1993; 101(6):827-41. PMC: 2216749. DOI: 10.1085/jgp.101.6.827. View

11.

Agre P, Preston G, Smith B, Jung J, Raina S, Moon C . Aquaporin CHIP: the archetypal molecular water channel. Am J Physiol. 1993; 265(4 Pt 2):F463-76. DOI: 10.1152/ajprenal.1993.265.4.F463. View

12.

Sallusto F, Lanzavecchia A . Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 1994; 179(4):1109-18. PMC: 2191432. DOI: 10.1084/jem.179.4.1109. View

13.

Steinman R, Swanson J . The endocytic activity of dendritic cells. J Exp Med. 1995; 182(2):283-8. PMC: 2192115. DOI: 10.1084/jem.182.2.283. View

14.

Sallusto F, Cella M, Danieli C, Lanzavecchia A . Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med. 1995; 182(2):389-400. PMC: 2192110. DOI: 10.1084/jem.182.2.389. View

15.

King L, Agre P . Pathophysiology of the aquaporin water channels. Annu Rev Physiol. 1996; 58:619-48. DOI: 10.1146/annurev.ph.58.030196.003155. View

16.

Achard J, Bubien J, Benos D, Warnock D . Stretch modulates amiloride sensitivity and cation selectivity of sodium channels in human B lymphocytes. Am J Physiol. 1996; 270(1 Pt 1):C224-34. DOI: 10.1152/ajpcell.1996.270.1.C224. View

17.

Echevarria M, WINDHAGER E, FRINDT G . Selectivity of the renal collecting duct water channel aquaporin-3. J Biol Chem. 1996; 271(41):25079-82. DOI: 10.1074/jbc.271.41.25079. View

18.

Norbury C, Chambers B, Prescott A, Ljunggren H, Watts C . Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol. 1997; 27(1):280-8. DOI: 10.1002/eji.1830270141. View

19.

Ismailov I, Berdiev B, Shlyonsky V, Benos D . Mechanosensitivity of an epithelial Na+ channel in planar lipid bilayers: release from Ca2+ block. Biophys J. 1997; 72(3):1182-92. PMC: 1184502. DOI: 10.1016/S0006-3495(97)78766-6. View

20.

Cella M, Engering A, Pinet V, Pieters J, Lanzavecchia A . Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature. 1997; 388(6644):782-7. DOI: 10.1038/42030. View