ER stress and basement membrane defects combine to cause glomerular and tubular renal disease resulting from Col4a1 mutations in mice

DMM Disease Models and Mechanisms

Volumn 9, Issue 2, 2016, Pages 165-176

  Jones, Frances E ^a   Bailey, Matthew A ^b   Murray, Lydia S ^a   Lu, Yinhui ^c   McNeilly, Sarah ^a   SchloÌtzer Schrehardt, Ursula ^d   Lennon, Rachel ^c   Sado, Yoshikazu ^e   Brownstein, David G ^b   Mullins, John J ^b   Kadler, Karl E ^c   Van Agtmael, Tom ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e Shigei Medical Research Institute   (Japan)

Author keywords

Basement membrane; Collagen IV; Endoplasmic reticulum stress; Extracellular matrix; Kidney disease

Indexed keywords

ALDOSTERONE; AMILORIDE; AQUAPORIN 2; COLLAGEN TYPE 4; COLLAGEN TYPE 4 A1; FUROSEMIDE; RECOMBINANT ERYTHROPOIETIN; THIAZIDE DIURETIC AGENT; UNCLASSIFIED DRUG; VASOPRESSIN; COL4A1 PROTEIN, HUMAN;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATROPHY; BOWMAN CAPSULE; CONTROLLED STUDY; DIABETES INSIPIDUS; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; GLOMERULONEPHRITIS; GLOMERULUS BASEMENT MEMBRANE; GLOMERULUS FILTRATION; HEMATURIA; HENLE LOOP; HISTOPATHOLOGY; HYPOTENSION; KIDNEY TUBULE BASEMENT MEMBRANE; KIDNEY TUBULE DISORDER; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; POLYURIA; PRIORITY JOURNAL; PROTEINURIA; SODIUM ABSORPTION; ANIMAL; BASEMENT MEMBRANE; GENETICS; GLOMERULUS; HUMAN; KIDNEY TUBULE; METABOLISM; MUTATION; PATHOLOGY;

ANIMALS; BASEMENT MEMBRANE; COLLAGEN TYPE IV; ENDOPLASMIC RETICULUM STRESS; HUMANS; KIDNEY GLOMERULUS; KIDNEY TUBULES; MICE; MUTATION;

EID: 84957949102     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.021741     Document Type: Article

References (47)

1. Abrahamson, D. R., Hudson, B. G., Stroganova, L., Borza, D.-B. and St. John, P. L. (2009). Cellular origins of type IV collagen networks in developing glomeruli. J. Am. Soc. Nephrol. 20, 1471-1479.
2. Alamowitch, S., Plaisier, E., Favrole, P., Prost, C., Chen, Z., Van Agtmael, T., Marro, B. and Ronco, P. (2009). Cerebrovascular disease related to COL4A1 mutations in HANAC syndrome. Neurology 73, 1873-1882.
3. Babey, M., Kopp, P. and Robertson, G. L. (2011). Familial forms of diabetes insipidus: Clinical and molecular characteristics. Nat. Rev. Endocrinol. 7, 701-714.
4. Bailey, M. A., Mullins, J. J. and Kenyon, C. J. (2009). Mineralocorticoid and glucocorticoid receptors stimulate epithelial sodium channel activity in a mouse model of Cushing syndrome. Hypertension 54, 890-896.
5. Bateman, J. F., Boot-Handford, R. P. and Lamande?, S. R. (2009). Genetic diseases of connective tissues: Cellular and extracellular effects of ECM mutations. Nat. Rev. Genet. 10, 173-183.
6. Chen, Y. M., Zhou, Y., Go, G., Marmerstein, J. T., Kikkawa, Y. and Miner, J. H. (2013). Laminin beta2 gene missense mutation produces endoplasmic reticulum stress in podocytes. J. Am. Soc. Nephrol. 24, 1223-1233.
7. Chen, Z., Migeon, T., Verpont, M.-C., Zaidan, M., Sado, Y., Kerjaschki, D., Ronco, P. and Plaisier, E. (2015). HANAC syndrome Col4a1 mutation causes neonate glomerular hyperpermeability and adult glomerulocystic kidney disease. J. Am. Soc. Nephrol. [E-pub ahead of print] doi:10.1681/ASN.2014121217.
8. Chiang, C.-K., Nangaku, M., Tanaka, T., Iwawaki, T. and Inagi, R. (2013). Endoplasmic reticulum stress signal impairs erythropoietin production: A role for ATF4. Am. J. Physiol. Cell Physiol. 304, C342-C353.
9. Craigie, E., Evans, L. C., Mullins, J. J. and Bailey, M. A. (2012). Failure to downregulate the epithelial sodium channel causes salt sensitivity in Hsd11b2 heterozygote mice. Hypertension 60, 684-690.
10. Engin, F. and Hotamisligil, G. S. (2010). Restoring endoplasmic reticulum function by chemical chaperones: An emerging therapeutic approach for metabolic diseases. Diabetes Obes. Metab. 12 Suppl. 2, 108-115.
11. Favor, J., Gloeckner, C. J., Janik, D., Klempt, M., Neuhauser-Klaus, A., Pretsch, W., Schmahl, W. and Quintanilla-Fend, L. (2007). Type IV procollagen missense mutations associated with defects of the eye, vascular stability, the brain, kidney function and embryonic or postnatal viability in the mouse, Mus musculus: An extension of the Col4a1 allelic series and the identification of the first two Col4a2 mutant alleles. Genetics 175, 725-736.
12. Gabbi, C., Kong, X., Suzuki, H., Kim, H.-J., Gao, M., Jia, X., Ohnishi, H., Ueta, Y., Warner, M., Guan, Y. et al. (2012). Central diabetes insipidus associated with impaired renal aquaporin-1 expression in mice lacking liver X receptor beta. Proc. Natl. Acad. Sci. USA 109, 3030-3034.
13. Gould, D. B., Phalan, F. C., Breedveld, G. J., Van Mil, S. E., Smith, R. S., Schimenti, J. C., Aguglia, U., Van Der Knaap, M. S., Heutink, P. and John, S. W. M. (2005). Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science 308, 1167-1171.
14. Gould, D. B., Phalan, F. C., Van Mil, S. E., Sundberg, J. P., Vahedi, K., Massin, P., Bousser, M. G., Heutink, P., Miner, J. H., Tournier-Lasserve, E. et al. (2006). Role of COL4A1 in small-vessel disease and hemorrhagic stroke. N. Engl. J. Med. 354, 1489-1496.
15. Gould, D. B., Marchant, J. K., Savinova, O. V., Smith, R. S. and John, S. W. M. (2007). Col4a1 mutation causes endoplasmic reticulum stress and genetically modifiable ocular dysgenesis. Hum. Mol. Genet. 16, 798-807.
16. Hudson, B. G., Tryggvason, K., Sundaramoorthy, M. and Neilson, E. G. (2003). Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N. Engl. J. Med. 348, 2543-2556.
17. Hunter, R.W., Craigie, E., Homer, N. Z. M., Mullins, J. J. and Bailey, M. A. (2014). Acute inhibition of NCC does not activate distal electrogenic Na+ reabsorption or kaliuresis. Am. J. Physiol. Renal. Physiol. 306, F457-F467.
18. Hunter, R.W., Ivy, J. R., Flatman, P.W., Kenyon, C. J., Craigie, E., Mullins, L. J., Bailey, M. A. and Mullins, J. J. (2015). Hypertrophy in the distal convoluted tubule of an 11?-hydroxysteroid dehydrogenase type 2 knockout model. J. Am. Soc. Nephrol. 27, 1537-1548.
19. Inagi, R. (2009). Endoplasmic reticulum stress in the kidney as a novel mediator of kidney injury. Nephron Exp. Nephrol. 112, e1-e9.
20. Jeanne, M., Labelle-Dumais, C., Jorgensen, J., Kauffman,W. B., Mancini, G. M., Favor, J., Valant, V., Greenberg, S. M., Rosand, J. and Gould, D. B. (2012). COL4A2 mutations impair COL4A1 and COL4A2 secretion and cause hemorrhagic stroke. Am. J. Hum. Genet. 90, 91-101.
21. Kalluri, R., Shield, C. F., Todd, P., Hudson, B. G. and Neilson, E. G. (1997). Isoform switching of type IV collagen is developmentally arrested in X-linked Alport syndrome leading to increased susceptibility of renal basement membranes to endoproteolysis. J. Clin. Invest. 99, 2470-2478.
22. Khoshnoodi, J., Pedchenko, V. and Hudson, B. G. (2008). Mammalian collagen IV. Microsc. Res. Tech. 71, 357-370.
23. Kuo, D. S., Labelle-Dumais, C. and Gould, D. B. (2012). COL4A1 and COL4A2 mutations and disease: Insights into pathogenic mechanisms and potential therapeutic targets. Hum. Mol. Genet. 21, R97-R110.
24. Kuo, D. S., Labelle-Dumais, C., Mao, M., Jeanne, M., Kauffman, W. B., Allen, J., Favor, J. and Gould, D. B. (2014). Allelic heterogeneity contributes to variability in ocular dysgenesis, myopathy and brain malformations caused by Col4a1 and Col4a2 mutations. Hum. Mol. Genet. 23, 1709-1722.
25. Long, D. A., Kolatsi-Joannou, M., Price, K. L., Dessapt-Baradez, C., Huang, J. L., Papakrivopoulou, E., Hubank, M., Korstanje, R., Gnudi, L. and Woolf, A. S. (2013). Albuminuria is associated with too few glomeruli and too much testosterone. Kidney Int. 83, 1118-1129.
26. Mollet, G., Ratelade, J., Boyer, O., Muda, A. O., Morisset, L., Lavin, T. A., Kitzis, D., Dallman, M. J., Bugeon, L., Hubner, N. et al. (2009). Podocin inactivation in mature kidneys causes focal segmental glomerulosclerosis and nephrotic syndrome. J. Am. Soc. Nephrol. 20, 2181-2189.
27. Murray, L. S., Lu, Y., Taggart, A., Van Regemorter, N., Vilain, C., Abramowicz, M., Kadler, K. E. and Van Agtmael, T. (2014). Chemical chaperone treatment reduces intracellular accumulation of mutant collagen IV and ameliorates the cellular phenotype of a COL4A2 mutation that causes haemorrhagic stroke. Hum. Mol. Genet. 23, 283-292.
28. Nielsen, R. and Christensen, E. I. (2010). Proteinuria and events beyond the slit. Pediatr. Nephrol. 25, 813-822.
29. Ohse, T., Chang, A. M., Pippin, J. W., Jarad, G., Hudkins, K. L., Alpers, C. E., Miner, J. H. and Shankland, S. J. (2009). A new function for parietal epithelial cells: A second glomerular barrier. Am. J. Physiol. Renal Physiol. 297, F1566-F1574.
30. Pastor-Pareja, J. C. and Xu, T. (2011). Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and perlecan. Dev. Cell 21, 245-256.
31. Plaisier, E., Gribouval, O., Alamowitch, S., Mougenot, B., Prost, C., Verpont, M. C., Marro, B., Desmettre, T., Cohen, S. Y., Roullet, E. et al. (2007). COL4A1 mutations and hereditary angiopathy, nephropathy, aneurysms, and muscle cramps. N. Engl. J. Med. 357, 2687-2695.
32. Plaisier, E., Chen, Z., Gekeler, F., Benhassine, S., Dahan, K., Marro, B., Alamowitch, S., Paques, M. and Ronco, P. (2010). Novel COL4A1 mutations associated with HANAC syndrome: A role for the triple helical CB3[IV] domain. Am. J. Med. Genet A 152A, 2550-2555.
33. Rannikmae, K., Davies, G., Thomson, P. A., Bevan, S., Devan, W. J., Falcone, G. J., Traylor, M., Anderson, C. D., Battey, T. W. K., Radmanesh, F. et al. (2015). Common variation in COL4A1/COL4A2 is associated with sporadic cerebral small vessel disease. Neurology 84, 918-926.
34. Ron, D. and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529.
35. Sibon, I., Coupry, I., Menegon, P., Bouchet, J.-P., Gorry, P., Burgelin, I., Calvas, P., Orignac, I., Dousset, V., Lacombe, D. et al. (2007). COL4A1 mutation in Axenfeld-Rieger anomaly with leukoencephalopathy and stroke. Ann. Neurol. 62, 177-184.
36. Taylor, S. H., Al-Youha, S., Van Agtmael, T., Lu, Y.,Wong, J., McGrouther, D. A. and Kadler, K. E. (2011). Tendon is covered by a basement membrane epithelium that is required for cell retention and the prevention of adhesion formation. PLoS ONE 6, e16337.
37. Tomotaki, S., Mizumoto, H., Hamabata, T., Kumakura, A., Shiota, M., Arai, H., Haginoya, K. and Hata, D. (2014). Severe hemolytic jaundice in a neonate with a novel COL4A1 mutation. Pediatr. Neonatol. [E-pub ahead of print] doi:10.1016/j. pedneo.2014.04.001.
38. Tsaih, S.-W., Pezzolesi, M. G., Yuan, R., Warram, J. H., Krolewski, A. S. and Korstanje, R. (2009). Genetic analysis of albuminuria in aging mice and concordance with loci for human diabetic nephropathy found in a genome-wide association scan. Kidney Int. 77, 201-210.
39. Tsang, K. Y., Chan, D., Cheslett, D., Chan, W. C. W., So, C. L., Melhado, I. G., Chan, T.W. Y., Kwan, K. M., Hunziker, E. B., Yamada, Y. et al. (2007). Surviving endoplasmic reticulum stress is coupled to altered chondrocyte differentiation and function. PLoS Biol. 5, e44.
40. Vahedi, K. and Alamowitch, S. (2011). Clinical spectrum of type IV collagen (COL4A1) mutations: A novel genetic multisystem disease. Curr. Opin. Neurol. 24, 63-68.
41. Van Agtmael, T. and Bruckner-Tuderman, L. (2010). Basement membranes and human disease. Cell Tissue Res. 339, 167-188.
42. Van Agtmael, T., Schlotzer-Schrehardt, U., McKie, L., Brownstein, D. G., Lee, A.W., Cross, S. H., Sado, Y., Mullins, J. J., Poschl, E. and Jackson, I. J. (2005). Dominant mutations of Col4a1 result in basement membrane defects which lead to anterior segment dysgenesis and glomerulopathy. Hum. Mol. Genet. 14, 3161-3168.
43. Van Agtmael, T., Bailey, M. A., Schlotzer-Schrehardt, U., Craigie, E., Jackson, I. J., Brownstein, D. G., Megson, I. L. and Mullins, J. J. (2010). Col4a1 mutation in mice causes defects in vascular function and low blood pressure associated with reduced red blood cell volume. Hum. Mol. Genet. 19, 1119-1128.
44. Weng, Y.-C., Sonni, A., Labelle-Dumais, C., De Leau, M., Kauffman, W. B., Jeanne, M., Biffi, A., Greenberg, S. M., Rosand, J. and Gould, D. B. (2012). COL4A1 mutations in patients with sporadic late-onset intracerebral hemorrhage. Ann. Neurol. 71, 470-477.
45. Williams, S. E., Reed, A. A. C., Galvanovskis, J., Antignac, C., Goodship, T., Karet, F. E., Kotanko, P., Lhotta, K., Morinie?re, V., Williams, P. et al. (2009). Uromodulin mutations causing familial juvenile hyperuricaemic nephropathy lead to protein maturation defects and retention in the endoplasmic reticulum. Hum. Mol. Genet. 18, 2963-2974.
46. Yoneda, Y., Haginoya, K., Arai, H., Yamaoka, S., Tsurusaki, Y., Doi, H., Miyake, N., Yokochi, K., Osaka, H., Kato, M. et al. (2012). De novo and inherited mutations in COL4A2, encoding the type IV collagen alpha2 chain cause porencephaly. Am. J. Hum. Genet. 90, 86-90.
47. Yoneda, Y., Haginoya, K., Kato, M., Osaka, H., Yokochi, K., Arai, H., Kakita, A., Yamamoto, T., Otsuki, Y., Shimizu, S.-I. et al. (2013). Phenotypic spectrum of COL4A1 mutations: Porencephaly to schizencephaly. Ann. Neurol. 73, 48-57.