Basic Study
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Nephrol. Jan 6, 2017; 6(1): 21-28
Published online Jan 6, 2017. doi: 10.5527/wjn.v6.i1.21
Acetylsalicylic acid interferes with embryonic kidney growth and development by a prostaglandin-independent mechanism
Simon J M Welham, Alexander J Sparrow, David S Gardner, Matthew J Elmes
Simon J M Welham, Alexander J Sparrow, Matthew J Elmes, Division of Nutritional Sciences, School of Biosciences, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
David S Gardner, School of Veterinary Medicine and Science, University of Nottingham, Loughborough, Leicestershire LE12 5RD, United Kingdom
Author contributions: Welham SJW devised studies, participated in all experimental work and wrote the manuscript; Sparrow AJ participated in organ culture experiments and measurements of growth; Gardner DS conducted statistical analysis and participated in manuscript preparation; Elmes MJ devised studies, participated in experimental work and wrote the manuscript.
Institutional review board statement: The present investigation was performed in accordance with the Home Office Guidance on the operation of the Animals (Scientific Procedures) Act (Great Britain Home Office, 2000). However, the study only used tissues from animals which fell outside of the ASPA remit (i.e., organs were isolated from fetuses before 2/3 gestation was completed) and thus no specific “procedures” were carried out requiring explicit ethical approval.
Conflict-of-interest statement: The authors declare that they have no competing interests.
Data sharing statement: Statistical code, and some datasets available from the corresponding author at simon.welham@nottingham.ac.uk.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Dr. Simon JM Welham, Division of Nutritional Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD, United Kingdom. simon.welham@nottingham.ac.uk
Telephone: +44-115-9516183 Fax: +44-115-9516129
Received: June 30, 2016
Peer-review started: July 1, 2016
First decision: September 5, 2016
Revised: September 22, 2016
Accepted: October 22, 2016
Article in press: October 24, 2016
Published online: January 6, 2017
Processing time: 181 Days and 15.4 Hours
Abstract
AIM

To evaluate the effects of the non-selective, non-steroidal anti-inflammatory drug (NSAID) acetylsalicylic acid (ASA), on ex vivo embryonic kidney growth and development.

METHODS

Pairs of fetal mouse kidneys at embryonic day 12.5 were cultured ex vivo in increasing concentrations of ASA (0.04-0.4 mg/mL) for up to 7 d. One organ from each pair was grown in control media and was used as the internal control for the experimental contralateral organ. In some experiments, organs were treated with ASA for 48 h and then transferred either to control media alone or control media containing 10 μmol/L prostaglandin E2 (PGE2) for a further 5 d. Fetal kidneys were additionally obtained from prostaglandin synthase 2 homozygous null or heterozygous (PTGS2-/- and PTGS2-/+) embryos and grown in culture. Kidney cross-sectional area was used to determine treatment effects on kidney growth. Whole-mount labelling to fluorescently detect laminin enabled crude determination of epithelial branching using confocal microscopy.

RESULTS

Increasing ASA concentration (0.1, 0.2 and 0.4 mg/mL) significantly inhibited metanephric growth (P < 0.05). After 7 d of culture, exposure to 0.2 mg/mL and 0.4 mg/mL reduced organ size to 53% and 23% of control organ size respectively (P < 0.01). Addition of 10 μmol/L PGE2 to culture media after exposure to 0.2 mg/mL ASA for 48 h resulted in a return of growth area to control levels. Application of control media alone after cessation of ASA exposure showed no benefit on kidney growth. Despite the apparent recovery of growth area with 10 μmol/L PGE2, no obvious renal tubular structures were formed. The number of epithelial tips generated after 48 h exposure to ASA was reduced by 40% (0.2 mg/mL; P < 0.05) and 47% (0.4 mg/mL; P < 0.01). Finally, growth of PTGS2-/- and PTGS2+/- kidneys in organ culture showed no differences, indicating that PTGS2 derived PGE2 may at best have a minor role.

CONCLUSION

ASA reduces early renal growth and development but the role of prostaglandins in this may be minor.

Keywords: Acetylsalicylic acid; Nephrogenesis; Kidney culture; Non-steroidal anti-inflammatory drug; Prostaglandins; Prostaglandin synthase 2

Core tip: Non-steroidal anti-inflammatory drugs (NSAIDs) are widely used as painkillers and are available without prescription. They act by inhibiting cyclooxygenase activity thereby preventing prostaglandin synthesis via the prostaglandin synthase enzymes prostaglandin synthase 1 (PTGS1) and PTGS2. Although NSAIDs cross the placenta, they are among the most common drugs prescribed during the first trimester of pregnancy and estimated prevalence of usage is more than 25% of pregnant women. NSAID use during pregnancy has been associated with abnormal renal development and renal failure in the offspring at birth. These may impact the individual throughout their adult life.