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PMID: 11773623 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Functional requirement of aquaporin-5 in plasma membranes of sweat glands.

Nejsum LN, Kwon TH, Jensen UB, Fumagalli O, Frøkiaer J, Krane CM, Menon AG, King LS, Agre PC, Nielsen S

Abstract

The distribution and function of aquaporins (AQPs) have not previously been defined in sweat glands. In this study, AQP1, AQP3, and AQP5 mRNA were demonstrated in rat paw by reverse transcription (RT)-PCR, but AQP2 and AQP4 were not. AQP1, AQP3, and AQP5 protein were confirmed in these tissues by immunoblotting. AQP1 was identified in capillary endothelial cells by immunohistochemical labeling, but not in sweat glands or epidermis. Abundant AQP3 expression was seen in basal levels of epidermis, but not in sweat glands. AQP2 and AQP4 were not observed in either skin or sweat glands. Immunohistochemical labeling revealed abundant AQP5 in secretory parts of rat and mouse sweat glands, where immunoelectron microscopy demonstrated abundant AQP5 labeling in the apical plasma membrane. AQP5 immunolabeling of human sweat glands yielded a similar pattern. To establish the role of AQP5 in sweat secretion, we tested the response of adult mice to s.c. injection of pilocarpine, as visualized by reaction of secreted amylase with iodine/starch. The number of active sweat glands was dramatically reduced in AQP5-null (-/-) mice compared with heterozygous (+/-) and wild-type (+/+) mice. We conclude that the presence of AQP5 in plasma membranes of sweat glands is essential for secretion, providing potential insight into mechanisms underlying mammalian thermoregulation, tactile sensitivity, and the pathophysiology of hyperhidrosis.

MeSH Terms
Animals Aquaporin 2 Aquaporin 3 Aquaporin 4 Aquaporin 5 Aquaporin 6 Aquaporins/biosynthesis,metabolism,physiology Cell Membrane/metabolism Heterozygote Immunoblotting Immunohistochemistry Kidney/metabolism Lung/metabolism Membrane Proteins Mice Mice, Transgenic Microscopy, Immunoelectron Muscarinic Agonists/pharmacology Pilocarpine/pharmacology RNA, Messenger/metabolism Rats Rats, Wistar Reverse Transcriptase Polymerase Chain Reaction Skin/metabolism Subcellular Fractions Sweat Glands/metabolism Water/chemistry
Chemicals
Aqp2 protein, mouse Aqp2 protein, rat Aqp3 protein, mouse Aqp3 protein, rat Aqp4 protein, mouse Aqp4 protein, rat Aqp5 protein, mouse Aqp5 protein, rat Aquaporin 2 Aquaporin 4 Aquaporin 5 Aquaporin 6 Aquaporins Membrane Proteins Muscarinic Agonists RNA, Messenger Pilocarpine Water Aquaporin 3
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Nejsum Lene N
The Water and Salt Research Center and the Department of Human Genetics, University of Aarhus, DK-8000 Aarhus, Denmark.
Kwon Tae-Hwan
Jensen Uffe B
Fumagalli Ornella
Frøkiaer Jørgen
Krane Carissa M
Menon Anil G
King Landon S
Agre Peter C
Nielsen Søren
References (41)
41 references, click to expand
  1. Rodent eccrine sweat glands: a case of multiple efferent innervation.
    Neuroscience. 1984 Mar;11(3):741-9 PMID: 6717807
  2. Anhidrosis (hypohidrosis) in Sjögren's syndrome.
    J Am Acad Dermatol. 1987 Jan;16(1 Pt 2):233-5 PMID: 3819059
  3. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  4. Development and properties of the secretory response in rat sweat glands: relationship to the induction of cholinergic function in sweat gland innervation.
    Dev Biol. 1987 Sep;123(1):179-90 PMID: 3622928
  5. Activation of salivary secretion: coupling of cell volume and [Ca2+]i in single cells.
    Science. 1989 Jun 30;244(4912):1582-5 PMID: 2500708
  6. Developmental expression of muscarinic cholinergic receptors and coupling to phospholipase C in rat sweat glands are independent of innervation.
    J Neurosci. 1991 Dec;11(12):3772-82 PMID: 1744689
  7. Evidence that M3 muscarinic receptors in rat parotid gland couple to two second messenger systems.
    Am J Physiol. 1991 Dec;261(6 Pt 1):C1063-73 PMID: 1722644
  8. Regulation of electrolyte and fluid secretion in salivary acinar cells.
    Am J Physiol. 1992 Dec;263(6 Pt 1):G823-37 PMID: 1476190
  9. CHIP28 water channels are localized in constitutively water-permeable segments of the nephron.
    J Cell Biol. 1993 Jan;120(2):371-83 PMID: 7678419
  10. Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7275-9 PMID: 8346245
  11. Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine.
    Science. 1994 Apr 1;264(5155):92-5 PMID: 8140421
  12. Examination of rat salivary glands for the presence of the aquaporin CHIP.
    Pflugers Arch. 1994 Oct;428(5-6):455-60 PMID: 7530838
  13. Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane.
    Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1013-7 PMID: 7532304
  14. Aquaporin-3 water channel localization and regulation in rat kidney.
    Am J Physiol. 1995 Nov;269(5 Pt 2):F663-72 PMID: 7503232
  15. Distribution of aquaporin-4 water channel expression within rat kidney.
    Am J Physiol. 1995 Dec;269(6 Pt 2):F775-85 PMID: 8594871
  16. Acquired generalized hypohidrosis/anhidrosis with subclinical Sjögren's syndrome: report of a case with diffuse syringolymphoid hyperplasia and lymphocytic sialadenitis.
    J Am Acad Dermatol. 1996 Aug;35(2 Pt 2):350-2 PMID: 8698925
  17. Adenovirus-mediated expression of aquaporin-5 in epithelial cells.
    J Biol Chem. 1996 Sep 6;271(36):22070-5 PMID: 8703015
  18. Polarized distribution of key membrane transport proteins in the rat submandibular gland.
    Pflugers Arch. 1997 Jan;433(3):260-8 PMID: 9064641
  19. Norepinephrine facilitates the development of the murine sweat response but is not essential.
    J Neurosci. 1997 Jun 1;17(11):4275-81 PMID: 9151744
  20. Expression of aquaporins in the rat ocular tissue.
    Exp Eye Res. 1997 Feb;64(2):203-9 PMID: 9176054
  21. Immunolocalization of aquaporin homologs in mouse lacrimal glands.
    Biochem Biophys Res Commun. 1997 Sep 29;238(3):891-5 PMID: 9325187
  22. Aquaporins in complex tissues. I. Developmental patterns in respiratory and glandular tissues of rat.
    Am J Physiol. 1997 Nov;273(5 Pt 1):C1541-8 PMID: 9374639
  23. Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat.
    Am J Physiol. 1997 Nov;273(5 Pt 1):C1549-61 PMID: 9374640
  24. Acetylcholine acts on M3 muscarinic receptors and induces the translocation of aquaporin5 water channel via cytosolic Ca2+ elevation in rat parotid glands.
    Biochem Biophys Res Commun. 1998 Apr 28;245(3):835-40 PMID: 9588201
  25. Dehydration reverses vasopressin antagonist-induced diuresis and aquaporin-2 downregulation in rats.
    Am J Physiol. 1998 Sep;275(3 Pt 2):F400-9 PMID: 9729513
  26. Treatment of hyperhidrosis.
    Dermatol Clin. 1998 Oct;16(4):863-9 PMID: 9891696
  27. Aquaporin-5 (AQP5), a water channel protein, in the rat salivary and lacrimal glands: immunolocalization and effect of secretory stimulation.
    Cell Tissue Res. 1999 Mar;295(3):513-21 PMID: 10022971
  28. Development of muscarinic receptors and regulation of secretory responsiveness in rodent sweat glands.
    Life Sci. 1999;64(6-7):381-5 PMID: 10069500
  29. Defective secretion of saliva in transgenic mice lacking aquaporin-5 water channels.
    J Biol Chem. 1999 Jul 16;274(29):20071-4 PMID: 10400615
  30. Water channel protein AQP3 is present in epithelia exposed to the environment of possible water loss.
    J Histochem Cytochem. 1999 Oct;47(10):1275-86 PMID: 10490456
  31. Aquaporin-1 water channels in short and long loop descending thin limbs and in descending vasa recta in rat kidney.
    Am J Physiol. 1995 Jun;268(6 Pt 2):F1023-37 PMID: 7541952
  32. Missense mutations in MIP underlie autosomal dominant 'polymorphic' and lamellar cataracts linked to 12q.
    Nat Genet. 2000 May;25(1):15-7 PMID: 10802646
  33. Persistent increase in the amount of aquaporin-5 in the apical plasma membrane of rat parotid acinar cells induced by a muscarinic agonist SNI-2011.
    FEBS Lett. 2000 Jul 21;477(3):253-7 PMID: 10908730
  34. Catecholamines are required for the acquisition of secretory responsiveness by sweat glands.
    J Neurosci. 2000 Oct 1;20(19):7362-9 PMID: 11007894
  35. Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjögren's syndrome patients.
    Lab Invest. 2001 Feb;81(2):143-8 PMID: 11232635
  36. Defective cellular trafficking of lacrimal gland aquaporin-5 in Sjögren's syndrome.
    Lancet. 2001 Mar 3;357(9257):688-9 PMID: 11247557
  37. Salivary acinar cells from aquaporin 5-deficient mice have decreased membrane water permeability and altered cell volume regulation.
    J Biol Chem. 2001 Jun 29;276(26):23413-20 PMID: 11290736
  38. Defective urinary concentrating ability due to a complete deficiency of aquaporin-1.
    N Engl J Med. 2001 Jul 19;345(3):175-9 PMID: 11463012
  39. Decreased pulmonary vascular permeability in aquaporin-1-null humans.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):1059-63 PMID: 11773634
  40. Eccrine glands of the rat. Response to induced sweating, hypertension, uremia, and alterations of sodium state.
    Arch Dermatol. 1968 Feb;97(2):189-201 PMID: 4295124
  41. Evidence for neurotransmitter plasticity in vivo: developmental changes in properties of cholinergic sympathetic neurons.
    Dev Biol. 1983 Aug;98(2):349-72 PMID: 6873459
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-01-08
Epub
2002-00-02
Pages
511-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC117591
Subset
IM
Grants
NHLBI NIH HHS · HL33991 · United States
NHLBI NIH HHS · HL61781 · United States
NEI NIH HHS · R01 EY011239 · United States
NHLBI NIH HHS · HL48268 · United States
NHLBI NIH HHS · R37 HL048268 · United States
NIDCR NIH HHS · DE138283 · United States
NHLBI NIH HHS · R01 HL033991 · United States
NHLBI NIH HHS · R01 HL048268 · United States
NEI NIH HHS · EY11239 · United States
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